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AÇOREANA<br />
Revista de Estu<strong>dos</strong> Açoreanos
AÇOREANA<br />
Revista de Estu<strong>dos</strong> Açoreanos<br />
PROPRIEDADE <strong>da</strong><br />
Socie<strong>da</strong>de Afonso Chaves<br />
Associação de Estu<strong>dos</strong> Açorianos<br />
Sede: Edifício do Museu “Carlos Machado”<br />
Apartado 258 – 9501-903 Ponta Delga<strong>da</strong><br />
São Miguel, <strong>Açores</strong>, Portugal<br />
PRESIDENTE e EDITOR<br />
António M. de Frias Martins<br />
QUADRO EDITORIAL<br />
Brian Morton<br />
Scientific Associate<br />
Department of Zoology<br />
The Natural History Museum<br />
Cromwell Road<br />
London SW7 5BD, UK<br />
António Serralheiro<br />
Departamento de Geologia<br />
Universi<strong>da</strong>de de Lisboa, Portugal<br />
Paulo A.V. Borges<br />
Departamento de Ciências Agrárias<br />
Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>, Portugal<br />
PAGINAÇÃO<br />
CLASSICOR, LDA.<br />
IMPRESSÃO E ACABAMENTO<br />
EGA - Empresa Gráfica Açoreana, L<strong>da</strong><br />
Edição subsidia<strong>da</strong> pela<br />
Direcção Regional <strong>da</strong> Ciência,<br />
Tecnologia e Comunicações<br />
do Governo Regional <strong>dos</strong> <strong>Açores</strong><br />
Setembro de 2009<br />
TIRAGEM<br />
750 exemplares<br />
DEPÓSITO LEGAL<br />
113 234 / 98<br />
ISSN<br />
0874 - 0380<br />
Esta edição é totalmente impressa (à excepção <strong>da</strong> capa)<br />
em papel ecológico, sem cloro, áci<strong>dos</strong> ou branqueamentos ópticos
AÇOREANA<br />
Revista de Estu<strong>dos</strong> Açoreanos<br />
SUPLEMENTO 6 SETEMBRO 2009<br />
THE MARINE FAUNA AND FLORA OF THE AZORES<br />
Proceedings of the<br />
Third International Workshop of Malacology<br />
and Marine Biology<br />
Vila Franca do Campo, São Miguel, <strong>Açores</strong><br />
July 17-28, 2006<br />
Sponsored by<br />
Edited by<br />
Socie<strong>da</strong>de Afonso Chaves<br />
Departamento de Biologia<br />
Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong><br />
Ponta Delga<strong>da</strong>
C O N T E Ú D O / C O N T E N T S<br />
7 LIST OF PARTICIPANTS<br />
9 THE AZOREAN WORKSHOPS<br />
António M. de Frias Martins<br />
15 ILLUSTRATED CHECKLIST OF THE INFRALITTORAL MOLLUSCS OFF<br />
VILA FRANCA DO CAMPO<br />
António M. de Frias Martins, José Pedro Borges, Sérgio Ávila, Ana C. Costa,<br />
Patrícia Madeira & Brian Morton<br />
105 ASPECTS OF THE BIOLOGY AND FUNCTIONAL MORPHOLOGY OF<br />
TIMOCLEA OVATA (BIVALVIA: VENEROIDEA: VENERINAE) IN THE<br />
AÇORES, PORTUGAL, AND A COMPARISON WITH CHIONE ELEVATA<br />
(CHIONINAE)<br />
Brian Morton<br />
121 ANATOMY AND BIOLOGY OF MITRA CORNEA LAMARCK, 1811 (MOL-<br />
LUSCA, CAENOGASTROPODA, MITRIDAE) FROM THE AZORES<br />
M. G. Harasewych<br />
137 COMPARATIVE STUDY OF CHEMICAL DEFENCES FROM TWO<br />
ALLOPATRIC NORTH ATLANTIC SUBSPECIES OF HYPSELODORIS<br />
PICTA (MOLLUSCA: OPISTHOBRANCHIA)<br />
Helena Gaspar, Ana Isabel Rodrigues & Gonçalo Calado<br />
145 THE BIOLOGY OF THE ZONING SUBTIDAL POLYCHAETE DITRUPA<br />
ARIETINA (SERPULIDAE) IN THE AÇORES, PORTUGAL, WITH A<br />
DESCRIPTION OF THE LIFE HISTORY OF ITS TUBE<br />
Brian Morton & Andreia Salvador<br />
157 DRILLING PREDATION UPON DITRUPA ARIETINA (POLYCHAETA:<br />
SERPULIDAE) FROM THE MID-ATLANTIC AÇORES, PORTUGAL<br />
Brian Morton & E.M. Harper<br />
167 THE PYCNOGONIDS (ARTHROPODA: PYCNOGONIDA) OF SÃO<br />
MIGUEL, AZORES, WITH DESCRIPTION OF A NEW SPECIES OF<br />
ANOPLODACTYLUS WILSON, 1878 (PHOXICHILIDIIDAE)<br />
Roger N. Bamber & Ana Cristina Costa<br />
183 THE TANAIDACEANS (ARTHROPODA: PERACARIDA: TANAIDACEA)<br />
OF SÃO MIGUEL, AZORES, WITH DESCRIPTION OF TWO NEW<br />
SPECIES, AND A NEW RECORD FROM TENERIFE<br />
Roger N. Bamber & Ana Cristina Costa<br />
201 THE SOFT-SEDIMENT INFAUNA OFF SÃO MIGUEL, AZORES, AND A<br />
COMPARISON WITH OTHER AZOREAN INVERTEBRATE HABITATS<br />
Roger N. Bamber & Roni Robbins<br />
211 SHELL OCCUPANCY BY THE HERMIT CRAB CLIBANARIUS ERYTHRO-<br />
PUS (CRUSTACEA) ON THE SOUTH COAST OF SÃO MIGUEL, AÇORES<br />
Pedro Rodrigues & Roshan K. Rodrigo<br />
217 A CONSERVATIONAL APPROACH ON THE SEABIRD POPULATIONS<br />
OF ILHÉU DE VILA FRANCA DO CAMPO, AZORES, PORTUGAL<br />
Pedro Rodrigues, Joana Micael, Roshan K. Rodrigo & Regina T. Cunha<br />
227 REMEMBERING Joseph C. Britton (1942-2006)
1<br />
2<br />
3<br />
4<br />
5<br />
6 8 10<br />
12<br />
11<br />
7<br />
14 15<br />
9 13 16<br />
Third International Workshop on Malacology and Marine Biology. 1, António M. de Frias Martins;<br />
2, Brian Morton; 3, José Pedro Borges; 4, Ana Cristina Costa; 5, Roshan Rodrigo; 6, Jerry<br />
Harasewych; 7, Vera Malhão; 8, Sérgio Ávila; 9, Joana Xavier; 10, Roni Robbins; 11, Paola Rachello;<br />
12, Roger Bamber; 13, Patrícia Madeira; 14, Andreia Salvador; 15, Pedro Rodrigues; 16, Daniela<br />
Gabriel.<br />
LIST OF PARTICIPANTS<br />
Ana Cristina Costa - Departamento de Biologia, Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>, 9501-801<br />
Ponta Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal - accosta@uac.pt<br />
Andrea Cunha - Departamento de Biologia, Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>, 9501-801 Ponta<br />
Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal -andrea_cunha@linus.uac.pt<br />
Andreia Salvador - Environment: Coastal & Marine, The Natural History Museum,<br />
Cromwell Road, London SW7 5BD, United Kingdom - a.salvador@nhm.ac.uk<br />
António M. de Frias Martins - Departamento de Biologia, Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>,<br />
9501-801 Ponta Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal - frias@uac.pt<br />
Brian Morton - Scientific Associate, Department of Zoology, The Natural History<br />
Museum, Cromwell Road, London SW7 5BD, U.K. - prof_bsmorton@hotmail.com<br />
Daniela Gabriel - Departamento de Biologia, Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>, 9501-801 Ponta<br />
Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal - <strong>da</strong>nielagferreira@hotmail.com;<br />
dgabriel@uac.pt
Gonçalo Calado - IPM-Instituto Português de Malacologia, Zoomarine EN 125 KM 65,<br />
8200-864 Guia, Portugal - bagoncas@mail.telepac.pt<br />
Jerry Harasewych - Curator of Marine Mollusca, Smithsonian Institution, National Museum<br />
of Natural History, Department of Invertebrate Zoology, P.O. Box 37012 MRC 163,<br />
Washington DC 20013-7012, USA - HarasewychJ@si.edu<br />
Joana Micael - Departamento de Biologia, Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>, 9501-801 Ponta<br />
Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal - joanamicael@cimar.org; jomicap@hotmail.com<br />
Joana Xavier - Institute for Biodiversity and Ecosystem Dynamics (IBED), University of<br />
Amster<strong>da</strong>m, Faculty of Science, Mauritskade 57, 1092 AD Amster<strong>da</strong>m, Netherlands -<br />
xavier@science.uva.nl<br />
José Pedro Borges - IPM-Instituto Português de Malacologia, Zoomarine EN 125 KM 65,<br />
8200-864 Guia, Portugal - josepedroborges@sapo.pt<br />
Kathe Jensen - Reasearch Associate, Zoological Museum, Copenhagen; Sjælør Boulevard 49,<br />
2.tv., 2450 København SV, Denmark - KRJensen@zmuc.ku.dk<br />
Manuela Parente - Departamento de Biologia, Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>, 9501-801 Ponta<br />
Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal - mparente@uac.pt<br />
Maria Ana Dionísio - Departamento de Biologia, Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>, 9501-801 Ponta<br />
Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal - anamdionisio@gmail.com<br />
PaolaG. Rachello Dolmen - Institute for Biodiversity and Ecosystem Dynamics (IBED),<br />
University of Amster<strong>da</strong>m, Faculty of Science, Mauritskade 57, 1092 AD Amster<strong>da</strong>m,<br />
Netherlands - P.Rachello@student.uva.nl<br />
Patrícia Madeira - Departamento de Biologia, Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>, 9501-801 Ponta<br />
Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal - tamissa@hotmail.com<br />
Pedro Rodrigues - Departamento de Biologia, Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>, 9501-801 Ponta<br />
Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal - pedroreisrodrigues@yahoo.com<br />
Roger Bamber - Consultancy Leader, Environment: Coastal & Marine, The Natural History<br />
Museum, Cromwell Road, London SW7 5BD, United Kingdom - r.bamber@nhm.ac.uk<br />
Roni Robbins - Environment: Coastal & Marine, The Natural History Museum, Cromwell<br />
Road, London SW7 5BD, United Kingdom - r.robbins@nhm.ac.uk<br />
Roshan K. Rodrigo - No.47, Saman Mawatha, Gangula, Panadura, Sri Lanka -<br />
rodrigoroshan@yahoo.com<br />
Sérgio Ávila - Departamento de Biologia, Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>, 9501-801 Ponta<br />
Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal - avila@notes.uac.pt<br />
Vera Malhão - Departamento de Biologia, Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>, 9501-801 Ponta<br />
Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal - vmalhao@notes.uac.pt;<br />
veramalhao@hotmail.com
AÇOREANA, Suplemento 6, Setembro 2009: 9-13<br />
THE AZORES WORKSHOPS<br />
António M. de Frias Martins<br />
Socie<strong>da</strong>de Afonso Chaves, 9501-903 Ponta Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal<br />
e-mail: afonsochaves.sac@gmail.com<br />
Twenty-one years ago, as a joint initiative<br />
of Socie<strong>da</strong>de Afonso Chaves and<br />
the Department of Biology of the<br />
University of the Azores, and under the<br />
sponsorship of the local Municipality,<br />
about half a dozen foreign scientists gathered<br />
in Vila Franca do Campo and, setting<br />
up an improvised laboratory in the <strong>da</strong>rk<br />
and humid facilities of the local newspaper<br />
“A Crença”, made history with the<br />
realization of the 1 st International<br />
Workshop of Malacology. The workshop<br />
participants came from the most prestigious<br />
scientific institutions: the<br />
Universities of Hong Kong, Harvard,<br />
Rhode Island, Liverpool, from the<br />
Smithsonian Institution, the Muséum<br />
national d’Histoire naturelle, Paris and<br />
the California Academy of Sciences. With<br />
another half dozen local scientists and<br />
academics, and aspiring young students,<br />
science was made right there, next to one<br />
of Vila Franca’s most significant monuments<br />
to culture and education of: the<br />
“Externato”. So worried with the (primitive)<br />
logistics were the organizers that<br />
they did not think of registering the event<br />
photographically for posterity.<br />
Nevertheless, in 1990 the proceedings of<br />
this first workshop came to light and<br />
remain to<strong>da</strong>y a reference document for<br />
the scientific study of the Ilhéu de Vila<br />
Franca do Campo and of the malacological<br />
fauna of the Azorean littoral.<br />
The research workshops, as regular<br />
events, were popularized in the scientific<br />
community by Brian Morton when<br />
Professor of Marine Ecology at the<br />
University of Hong Kong and Director of<br />
the Swire Institute of Marine Science.<br />
Through them, every three years, Brian<br />
rendered available for invited specialists<br />
in various scientific fields two weeks of<br />
research, with but one requisite in return:<br />
to publish in the proceedings of the event<br />
at least one research paper on the marine<br />
biology of Hong Kong. Brian Morton had<br />
visited the Azores in 1965, as a Chelsea<br />
College graduate, and since then has<br />
developed a special appreciation for these<br />
islands. It was then that I had the opportunity<br />
of meeting him and, from that time<br />
on, a relationship based on friendship<br />
and mutual respect developed that time<br />
has only made stronger.<br />
The 2 nd workshop, in 1991, and this<br />
time in the facilities of the fish market in<br />
Vila Franca do Campo, attracted about 40<br />
participants, national and foreign, with<br />
the corresponding scientific production<br />
broadened to other endeavours of marine<br />
biology besides malacology. The spectrum<br />
of participants was equally widened<br />
to include Australia and Hong Kong, various<br />
American institutions (University of<br />
Rhode Island, Smithsonian Institution,
10 AÇOREANA<br />
2009, Sup. 6: 9-13<br />
Harbor Branch Oceanographic Institution,<br />
Field Museum of Natural History,<br />
Chicago, Texas Christian University, Long<br />
Island University) and a fair representation<br />
from Europe (Odense University,<br />
Zoological Museum, Copenhagen, both<br />
in Denmark, Antwerp University/Institut<br />
Royal des Sciences naturelles de Belgique;<br />
University Marine Biological Station,<br />
Millport, UK). The workshop added the<br />
novelty of a panel on Marine<br />
Conservation, sponsored by UNESCO’s<br />
National Committee. The proceedings of<br />
the workshop were published in 1995.<br />
Ecology of the <strong>Açores</strong> had been undertaken<br />
by the Socie<strong>da</strong>de Afonso Chaves to<br />
replace a workshop, so that a systematic<br />
and all-encompassing study of the littoral<br />
would be conducted and reported upon<br />
comprehensively for the benefit, especially<br />
of local students. On the other hand,<br />
the famous expeditions of Albert the 1 st ,<br />
Prince of Monaco, had unravelled some<br />
of the biological secrets of the great<br />
depths around the Azores. To know better<br />
that band between 50 and 200 metres,<br />
well known to the fishermen for its abun<strong>da</strong>nt<br />
fish life but practically absent from<br />
scientific publications due to lack of<br />
research directed at it, was then an obvious<br />
choice for a workshop project.<br />
This practical objective – to better<br />
know Azorean marine biodiversity – was<br />
linked to another, more theoretical goal,<br />
resulting from studies of the distribution<br />
of species through time. Knowing that<br />
After a long interval, marked by other<br />
types of events – for example, the production<br />
of the book Coastal Ecology of the<br />
<strong>Açores</strong>, in 1998 –, the Socie<strong>da</strong>de Afonso<br />
Chaves and the Department of Biology of<br />
the University of the Azores united in<br />
their efforts once again to promote, in the<br />
eternal capital of the island of São Miguel,<br />
from July 17 to 28 of 2006, the 3 rd<br />
International Workshop of Malacology<br />
and Marine Biology, under the auspices of<br />
the Municipality of Vila Franca do Campo<br />
and with the much-appreciated collaboration<br />
of the Clube Naval de Vila Franca<br />
do Campo.<br />
Although open to every aspect of science<br />
of interest to the participants, the 3 rd<br />
workshop had a specific objective: to<br />
research virtually unstudied grounds. In<br />
fact, the Azorean coastal zone has been<br />
profusely studied and the book Coastal<br />
cyclical variations in temperature resulting<br />
from the glaciations lead to the disappearance<br />
of species less a<strong>da</strong>pted to such<br />
fluctuations, could we find species of previous<br />
colder ages that have sought refuge<br />
deeper, where temperatures are lower?<br />
The solution to this double quest rested<br />
on a dredging plan down to 200 metres.<br />
In fact, as it transpired, samples of the sea<br />
bed off Vila Franca do Campo were taken<br />
down to 360 metres during the workshop.
MARTINS: THE AZORES WORKSHOPS 11<br />
The collected material has been deposited<br />
in the Department of Biology reference<br />
collection and remains available to everyone<br />
who desires to conduct further<br />
research on it.<br />
Honouring the core interest of the<br />
workshop – Malacology – special attention<br />
was paid to molluscs and a listing of<br />
those species collected is provided.<br />
However, many other inhabitants of the<br />
sea bed came up in the dredge.<br />
The larger fractions of such samples were<br />
sorted immediately and the finer fractions<br />
preserved for sorting later, in the<br />
laboratory.<br />
As in previous meetings, the proceedings<br />
of the 3 rd workshop are published.<br />
The papers included in the proceedings<br />
result from short projects that the participants<br />
had taken upon themselves to<br />
develop, on the basis of any particular scientific<br />
aspect judged appropriate for the<br />
short time available for gathering <strong>da</strong>ta.
12 AÇOREANA<br />
2009, Sup. 6: 9-13<br />
Whenever possible, a photographic<br />
record of each living animal was<br />
obtained. The wealth of species collected<br />
is a clear sign that this workshop needs to<br />
be continued.<br />
The scientific content of the workshop<br />
is the most visible, desirable, outcome of<br />
an effort that had its roots in the statutes<br />
of the oldest scientific society in the<br />
Azores - the Socie<strong>da</strong>de Afonso Chaves –<br />
and which are to promote the realization<br />
of scientific meetings dealing with the<br />
natural history of the Azores. As in previous<br />
events, the participation of the<br />
Department of Biology of the University of<br />
the Azores provided the scientific support.<br />
The warm hospitality of the Mayor of Vila<br />
Franca do Campo, Rui Melo, and the enthusiastic<br />
collaboration of the Clube Naval and<br />
its president, Paulo Melo, paved the way to<br />
comfortable and efficient logistics. The skill<br />
of Moisés Bolarinho, the skipper of the "Vila<br />
Franca" and the dedication of is crew took<br />
us to the best sites for successful dredging.<br />
The indispensable financing for this 3 rd<br />
workshop came from the DRCT – the<br />
regional governmental organism responsible<br />
for Science and Technology. The Luso-<br />
American Foun-<strong>da</strong>tion for Development<br />
(FLAD), the Foun<strong>da</strong>tion for Science and<br />
Technology (FCT) and the Municipality of<br />
Vila Franca do Campo were also generous<br />
in this area.
MARTINS: THE AZORES WORKSHOPS 13<br />
The choice of Vila Franca do Campo<br />
for the base camp of each workshop is<br />
somehow connected with the beautiful<br />
islet which is the ex-libris of this noble old<br />
capital of the island of São Miguel.<br />
Science is obviously the primary objective<br />
of these meetings. However, besides the<br />
knowledge acquired due to the research<br />
therein developed, there is a clear interest<br />
in fostering culture and education within<br />
the community. We are sure that the better<br />
knowledge about the Ilhéu de Vila<br />
Franca do Campo, in particular, resulting<br />
from the workshops has contributed to<br />
the strengthening of its stature as a nature<br />
reserve, cared for and respected by the<br />
thousands of users that visit it every summer.<br />
The prospect of an aquarium in<br />
Vila Franca do Campo has turned the<br />
attention of the local community towards<br />
one of its most precious resources - the<br />
sea.<br />
Finally, and, as a silent highlight of the<br />
workshop meetings, past, present and<br />
future, the generous offer of the founder<br />
of the workshop concept and of the Swire<br />
Institute of Marine Science, Professor<br />
Brian Morton, to help in the setting up of<br />
a Marine Biology Station in the facilities<br />
where this 3 rd workshop took place, will<br />
continue to bring to Vila Franca do<br />
Campo, a nucleus of resident researchers<br />
and academic guests from around the<br />
world who will undoubtedly act as a catalyst<br />
for science and education in the<br />
community which has so generously<br />
hosted these pioneering adventures.<br />
It is the belief of this author, his local<br />
colleagues and the groups of overseas scientists<br />
who have contributed, over the<br />
years, to the greater understanding of the<br />
unique marine life of the Azores in general<br />
and of the waters of Vila Franca do<br />
Campo in particular, that there is no better<br />
place where a permanent, international,<br />
marine research facility would not just<br />
flourish but would act as the archipelago’s<br />
flagship promoting marine conservation<br />
and technological advancement.<br />
For the benefit of all.
AÇOREANA, Suplemento 6, Setembro 2009: 15-103<br />
ILLUSTRATED CHECKLIST OF THE INFRALITTORAL MOLLUSCS<br />
OFF VILA FRANCA DO CAMPO<br />
António M. de Frias Martins 1 , José Pedro Borges 2 , Sérgio P. Ávila 3,4 , Ana C. Costa 1 ,<br />
Patrícia Madeira 3 & Brian Morton 5<br />
1<br />
CIBIO-Pólo <strong>Açores</strong>, Department of Biology, University of the Azores, 9501-801 Ponta Delga<strong>da</strong>, São Miguel,<br />
Azores, Portugal. e-mail: frias@uac.pt<br />
2<br />
IPM-Instituto Português de Malacologia, Zoomarine EN 125 KM 65, 8200-864 GUIA, Portugal<br />
3<br />
Marine PalaeoBiogeography group, Department of Biology, University of the Azores, 9501-801 Ponta Delga<strong>da</strong>,<br />
São Miguel, Azores, Portugal<br />
4<br />
Centro do IMAR <strong>da</strong> Universi<strong>da</strong>de <strong>dos</strong> <strong>Açores</strong>, 9901-862 Horta, Azores, Portugal<br />
5<br />
Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, U.K.<br />
ABSTRACT<br />
A list of the molluscan species dredged during the 3 rd International Workshop of<br />
Malacology and Marine Biology is presented. Positive identification has not been possible<br />
for a number of taxa. However, almost all species are illustrated so as to provide a practical<br />
guide to the species which may occur as beach drift and others which naturally range<br />
up into the interti<strong>da</strong>l.<br />
The distribution of the species at the various collecting stations is also presented as a<br />
table organized by depth, and identifying where specimens were collected alive or, in the<br />
case of bivalves, with both valves attached.<br />
RESUMO<br />
Apresenta-se uma listagem <strong>da</strong>s espécies de moluscos draga<strong>da</strong>s durante o 3º Workshop<br />
Internacional de Malacologia e Biologia Marinha. Uma identificação positiva não foi<br />
possível para um determinado número de taxa. No entanto, quase to<strong>da</strong>s as espécies estão<br />
ilustra<strong>da</strong>s, de modo a providenciar um guia prático para as que podem ocorrer no material<br />
arrojado nas praias e outras que naturalmente estendem a sua distribuição até ao<br />
interti<strong>da</strong>l.<br />
A distribuição <strong>da</strong>s espécies pelas várias estações de colheita é também apresenta<strong>da</strong><br />
numa tabela organiza<strong>da</strong> por profundi<strong>da</strong>de, identificando também onde os exemplares<br />
foram recolhi<strong>dos</strong> vivos ou, no caso <strong>dos</strong> bivalves, com ambas as valvas liga<strong>da</strong>s.<br />
INTRODUCTION<br />
The main purpose behind the 3 rd<br />
International Workshop of Malacology<br />
and Marine Biology was to test the hypothesis<br />
that the deeper, colder, waters around<br />
the Azorean islands acted as a refuge during<br />
the warm periods that interspersed<br />
glaciations. It is thought that when surface<br />
temperatures began to rise, cold-water<br />
species would likely follow their temperature<br />
optima by descending to appropriate<br />
depths. Present results, preliminary as<br />
they are, do not support such a suggestion.<br />
The extensive dredging has produced a<br />
wealth of information about the molluscan<br />
biodiversity of the sublittoral off Vila<br />
Franca do Campo, in a depth range poorly<br />
studied by previous authors in the Azores.<br />
This herein published list of 232 molluscan<br />
species and the pictorial representations of<br />
most of them is a contribution to that<br />
knowledge. The illustrations, whenever<br />
possible, were not only of the collected<br />
shells but of the living animals. This will<br />
provide students and researchers with an<br />
easier identification guide to facilitate<br />
their studies. Also, although in many
16 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
cases positive identifications were not<br />
possible, the provided illustrations supply<br />
a basis for further studies leading to<br />
more accurate taxonomic determinations.<br />
The micromolluscs are unevenly<br />
reported upon because the minimum<br />
dredge mesh was 2.5 mm and only some<br />
hauls were sieved to retain the residual<br />
1mm fraction.<br />
A list of the stations related to the<br />
workshop is provided (see Text figure 1).<br />
All species sorted are reported upon<br />
(Table 1), even though their shells could<br />
only have been transported from other<br />
habitats, including the interti<strong>da</strong>l. Such<br />
situations are commented upon for each<br />
species identified. To facilitate inferences<br />
related to depth distribution, the species<br />
collected alive or, in the case of bivalves,<br />
with both valves attached, are shown in<br />
bold in the Taxonomic List, and the sampling<br />
depths also indicated. Also, in<br />
Table 1 the stations are arranged by<br />
increasing depth and the state of the collected<br />
specimens (fragment, empty<br />
shell/one valve, with animal/two valves)<br />
is differentiated by variations in the density<br />
of their gray overlays, so as to give an<br />
overall pictorial view of the distribution<br />
of each taxon.<br />
The depth ranges of the species given<br />
by Poppe & Gotto (1991-1993) (P&G) and<br />
Macedo et al. (1999) (MM&B) are referred<br />
whenever possible. Also, where appropriate,<br />
reference is made to the species<br />
found alive in the nearby Ilhéu de Vila<br />
Franca do Campo (IVFC) (Martins, 2004).<br />
This is intended as a clarification to the<br />
distribution of these species in the<br />
dredged material.<br />
Previous works on Ilhéu de Vila<br />
Franca do Campo have listed the marine<br />
molluscs of that islet or of the shores nearby,<br />
and Ávila et al. (2000) have provided<br />
the most recent list of the shallow-water<br />
marine molluscs of São Miguel. For comparison<br />
purposes reference to these publications<br />
will be made under the appropriate<br />
taxa. Species are presented following<br />
their current systematic position as set<br />
out in CLEMAM (Check List of European<br />
Marine Molluscs) (http://www.somali.asso.fr/<br />
clemam/index.clemam.html).<br />
LIST OF SAMPLING STATIONS<br />
Forty-six stations were sampled during<br />
the workshop (Text figure 1). Stations 3-4,<br />
9-11, 17 were dive sites and are not included<br />
in this report, except in the notes provided<br />
under the respective station code.<br />
Stations 47-54 were sampled after the<br />
workshop timeframe but followed the<br />
same procedure and are, therefore included<br />
herein. Similarly, stations 56-58,<br />
sampled during fieldwork undertaken for<br />
the Malacology class of the Department of<br />
Biology of the University of the Azores,<br />
were added to the workshop material.<br />
Station 55 represented from the biological<br />
material collected from a stone snagged<br />
by a fishing net.<br />
STATION 1 – in front of the marina – Vila<br />
Franca do Campo.<br />
Date: 17-07-2006.<br />
Depth: 32 fathoms (57 m).<br />
Co-ordinates: N 37° 42’ 12” W 25° 25’ 09”.<br />
Collected by: Frias Martins, Brian Morton, Jerry<br />
Harasewych.<br />
Observations: (large dredge) two tows (A and B)<br />
pooled.<br />
STATION 2 – in front of the marina - Vila<br />
Franca do Campo.<br />
Date: 17-07-2006.<br />
Depth: 75 fathoms (135 m).<br />
Co-ordinates: N 37° 41’ 42” W 25° 25’ 22”.<br />
Collected by: Frias Martins, Brian Morton, Jerry<br />
Harasewych.<br />
Observations: (large dredge).<br />
STATION 3 – around Farilhão, SE of Ilhéu de<br />
Vila Franca do Campo.<br />
Date: 18-07-2006.<br />
Depth: 5-19 m.
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 17<br />
TEXT FIGURE 1. Distribution of the stations.<br />
Co-ordinates: —-<br />
Collected by: Joana Xavier, Paola Rachello, José<br />
Pedro Borges, Gonçalo Calado.<br />
Observations: (SCUBA) 1 ophiurid (10 m)<br />
Hypselodoris picta webbi (4 spcs.), Chromodoris<br />
purpurea (2 spcs.), Platydoris argo
18 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
(1 spc.), Flabellina (1 spc.), Hypselodoris<br />
mi<strong>da</strong>tlantica (1 spc.); Umbraculum<br />
umbraculum (1 spc. feeding on Halichondria<br />
aurantiaca).<br />
STATION 4 – off Cais do Tagarete, Vila Franca<br />
do Campo.<br />
Date: 18-07-2006.<br />
Depth: 7 m.<br />
Co-ordinates: —-<br />
Collected by: Gonçalo Calado, José Pedro<br />
Borges, Paola Rachello.<br />
Observations: (SCUBA).<br />
STATION 5<br />
Date: 19-07-2006.<br />
Depth: 23-24 fathoms (41-43 m)<br />
Co-ordinates: N 37° 42’ 02” W 25° 27’ 18”.<br />
Collected by: Brian Morton, Sérgio Ávila, Pedro<br />
Rodrigues.<br />
Observations: (dredge) 6 minute tow at 1.5<br />
knotts.<br />
STATION 6<br />
Date: 19-07-2006.<br />
Depth: 22-23 fathoms (40-41 m).<br />
Co-ordinates: N 37° 42’ 02” W 25° 27’ 13”.<br />
Collected by: Brian Morton, Sérgio Ávila, Pedro<br />
Rodrigues.<br />
Observations: (dredge) “earthworm” sand fish<br />
Apterichthus caecus (Linnaeus, 1758).<br />
STATION 7<br />
Date: 19-07-2006.<br />
Depth: 93-105 fathoms (167-189 m).<br />
Co-ordinates: N 37° 41’ 34” W 25° 27’ 34”.<br />
Collected by: Brian Morton, Sérgio Ávila, Pedro<br />
Rodrigues.<br />
Observations: (dredge) 10 min tow at 1.5 – 2<br />
knotts.<br />
STATION 8<br />
Date: 19-07-2006.<br />
Depth: 70-95 fathoms (126-171 m).<br />
Co-ordinates: N 37° 41’ 34” W 25° 27’ 15”.<br />
Collected by: Brian Morton, Sérgio Ávila, Pedro<br />
Rodrigues.<br />
Observations: (dredge) 6 minute tow at 1.5 – 2<br />
knotts.<br />
STATION 9 – Portinho <strong>da</strong> Ribeirinha.<br />
Date: 20-07-2006.<br />
Depth: 5-14 m.<br />
Co-ordinates: —-<br />
Collected by: Gonçalo Calado, Joana Xavier,<br />
Patrícia Madeira, Paola Rachello.<br />
Observations: (SCUBA) ophiurids.<br />
STATION 10 – wall and mouth of the marina –<br />
Vila Franca do Campo.<br />
Date: 20-07-2006.<br />
Depth: 6 m.<br />
Co-ordinates: —-<br />
Collected by: Gonçalo Calado, Patrícia Madeira.<br />
Observations: (SCUBA) echinoderms.<br />
STATION 11 – Ilhéu de Vila Franca do Campo<br />
(NE).<br />
Date: 19-07-2006.<br />
Depth: 16 m.<br />
Co-ordinates: —-<br />
Collected by: Gonçalo Calado, José Pedro<br />
Borges, Joana Xavier, Paola Rachello,<br />
Patrícia Madeira.<br />
Observations: (SCUBA).<br />
STATION 12<br />
Date: 21-07-2006.<br />
Depth: 53-67 fathoms (95-121 m).<br />
Co-ordinates: N 37° 41’ 39” W 25° 27’ 11”.<br />
Collected by: Brian Morton.<br />
Observations: (dredge).<br />
STATION 13<br />
Date: 21-07-2006.<br />
Depth: 47.9–40.8 fathoms (86-73 m).<br />
Co-ordinates: N 37° 41’ 34” W 25° 26’ 57”.<br />
Collected by: Brian Morton.<br />
Observations: (dredge).<br />
STATION 14<br />
Date: 21-07-2006.<br />
Depth: 25-26.2 fathoms (45-47 m).<br />
Co-ordinates: N 37° 41’ 51” W 25° 27’ 14”.<br />
Collected by: Brian Morton.<br />
Observations: (dredge).<br />
STATION 15<br />
Date: 21-07-2006.<br />
Depth: 25,7 – 26 fathoms (46-47 m).<br />
Co-ordinates: N 37° 41’ 52” W 25° 27’ 13”.<br />
Collected by: Brian Morton.<br />
Observations: (dredge).
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 19<br />
STATION 16<br />
Date: 21-07-2006.<br />
Depth: 9.9 – 11 fathoms (18-20 m).<br />
Co-ordinates: N 37° 42’ 39” W 25° 27’ 26”.<br />
Collected by: Brian Morton.<br />
Observations: (dredge).<br />
STATION 17 – mouth of Ilhéu de Vila Franca<br />
do Campo.<br />
Date: 20-07-2006.<br />
Depth: 6 m.<br />
Co-ordinates: —-<br />
Collected by: Andrea Cunha, Daniela Gabriel.<br />
Observations: (SCUBA) sponges, sand urchin,<br />
algae.<br />
STATION 18 – off Ribeira <strong>da</strong>s Tainhas.<br />
Date: 21-07-2006.<br />
Depth: 40 fathoms (72 m).<br />
Co-ordinates: N 37° 42’ 16” W 25° 24’ 45”.<br />
Collected by: Frias Martins, Brian Morton, Roger<br />
Bamber.<br />
Observations: (small dredge) 5 minute tow.<br />
STATION 19 – off Ribeira <strong>da</strong>s Tainhas.<br />
Date: 21-07-2006.<br />
Depth: 13 fathoms (23 m).<br />
Co-ordinates: N 37° 42’ 33” W 25° 24’ 53”.<br />
Collected by: Roger Bamber, Frias Martins, Brian<br />
Morton.<br />
Observations: (grab).<br />
STATION 20 – off Ribeira <strong>da</strong>s Tainhas.<br />
Date: 21-07-2006.<br />
Depth: 28 fathoms (50 m).<br />
Co-ordinates: N 37° 42’ 21” W 25° 24’ 43”.<br />
Collected by: Roger Bamber, Frias Martins, Brian<br />
Morton.<br />
Observations: (grab).<br />
STATION 21 – off Ribeira <strong>da</strong>s Tainhas.<br />
Date: 21-07-2006.<br />
Depth: 66 fathoms (118 m).<br />
Co-ordinates: N 37° 42’ 16” W 25° 24’ 34”.<br />
Collected by: Roger Bamber, Frias Martins, Brian<br />
Morton.<br />
Observations: (grab).<br />
STATION 22 – off Ribeira <strong>da</strong>s Tainhas.<br />
Date: 24-07-2006.<br />
Depth: 6 fathoms (11 m).<br />
Co-ordinates: N 37° 42’ 51” W 25° 24’ 45”.<br />
Collected by: Frias Martins, Brian Morton.<br />
Observations: (large dredge).<br />
STATION 23 – off Ribeira <strong>da</strong>s Tainhas.<br />
Date: 24-07-2006.<br />
Depth: 65-25 fathoms (117- 45 m).<br />
Co-ordinates: N 37° 42’ 05” W 25° 25’ 03”.<br />
Collected by: Frias Martins, Brian Morton.<br />
Observations: (large dredge)<br />
STATION 24 – off Ribeira <strong>da</strong>s Tainhas.<br />
Date: 24-07-2006.<br />
Depth: 65-27 fathoms (117-48 m).<br />
Co-ordinates: 37° 42’ 04” W 25° 25’ 02”.<br />
Collected by: Frias Martins, Brian Morton.<br />
Observations: (large dredge).<br />
STATION 25 – off Praia <strong>da</strong> Vinha <strong>da</strong> Areia.<br />
Date: 24-07-2006.<br />
Depth: 7.6 fathoms (14 m).<br />
Co-ordinates: N 37° 42’ 45” W 25° 25’ 24”.<br />
Collected by: Frias Martins, Brian Morton.<br />
Observations: (large dredge).<br />
STATION 26 – off Ribeira <strong>da</strong>s Tainhas.<br />
Date: 21-07-2006.<br />
Depth: 94 fathoms (169 m).<br />
Co-ordinates: N 37° 42’ 15” W 25° 24’ 28”.<br />
Collected by: Roger Bamber, Frias Martins, Brian<br />
Morton.<br />
Observations: (dredge).<br />
STATION 27 – off Ribeira <strong>da</strong>s Tainhas.<br />
Date: 24-07-2006.<br />
Depth: 60-55 fathoms (108-99 m).<br />
Co-ordinates: N 37° 42’ 01” W 25° 25’ 14”.<br />
Collected by: Sérgio Ávila.<br />
Observations: (large dredge) Holothuria.<br />
STATION 28– off Ribeira <strong>da</strong>s Tainhas.<br />
Date: 24-07-2006.<br />
Depth: 65-81 fathoms (117-145 m).<br />
Co-ordinates: N 37° 42’ 01” W 25° 25’ 01”.<br />
Collected by: Sérgio Ávila.<br />
Observations: (large dredge).<br />
STATION 29 – off Ribeira <strong>da</strong>s Tainhas.<br />
Date: 24-07-2006.<br />
Depth: 110-80 fathoms (198-144 m).<br />
Co-ordinates: N 37° 41’ 57” W 25° 25’ 08”.<br />
Collected by: Sérgio Ávila.<br />
Observations: (large dredge).
20 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
STATION 30 – off Ribeira <strong>da</strong>s Tainhas.<br />
Date: 24-07-2006.<br />
Depth: 35-19 fathoms (63-34 m).<br />
Co-ordinates: N 37° 42’ 17” W 25° 25’ 09”.<br />
Collected by: Sérgio Ávila.<br />
Observations: (large dredge).<br />
STATION 31 – off Cais do Tagarete, Vila<br />
Franca do Campo.<br />
Date: 25-07-2006.<br />
Depth: 29 fathoms (52 m).<br />
Co-ordinates: N 37° 42’ 07” W 25° 25’ 14”.<br />
Collected by: Frias Martins.<br />
Observations: (large dredge).<br />
STATION 32 – off Cais do Tagarete, Vila<br />
Franca do Campo.<br />
Date: 25-07-2006.<br />
Depth: 100 fathoms (180 m).<br />
Co-ordinates: N 37° 41’ 53” W 25° 25’ 15”.<br />
Collected by: Frias Martins.<br />
Observations: (large dredge).<br />
STATION 33 – off Rosto Branco, Água d’Alto.<br />
Date: 25-07-2006.<br />
Depth: 82-120 fathoms (147-216 m).<br />
Co-ordinates: N 37° 41” 08” W 25° 27’ 18”.<br />
Collected by: Frias Martins.<br />
Observations: (large dredge).<br />
STATION 34<br />
Date: 25-07-2006.<br />
Depth: 9.3 fathoms (17 m).<br />
Co-ordinates: N 37° 42’ 42” W 25° 24’ 38”.<br />
Collected by: Roger Bamber, Joana Xavier, Paola<br />
Rachello.<br />
Observations: (grab) two samples pooled.<br />
STATION 35<br />
Date: 25-07-2006.<br />
Depth: 12.7 fathoms (23 m).<br />
Co-ordinates: N 37° 42’ 37” W 25° 24’ 34”.<br />
Collected by: Roger Bamber, Joana Xavier, Paola<br />
Rachello.<br />
Observations: (grab) two samples pooled.<br />
STATION 36<br />
Date: 25-07-2006.<br />
Depth: 20 fathoms (36 m).<br />
Co-ordinates: N 37° 42’ 33” W 25° 24’ 35”.<br />
Collected by: Roger Bamber, Joana Xavier, Paola<br />
Rachello.<br />
Observations: (grab) two samples pooled.<br />
STATION 37<br />
Date: 25-07-2006.<br />
Depth: 130-75 fathoms (234-135 m) (G); 117-65<br />
fathoms (210-117 m) (H).<br />
Co-ordinates: N 37° 42’ 13” W 25° 24’ 36” (G)<br />
N 37° 41’ 59” W 25° 24’ 44” to N 37° 42’ 11”<br />
W 25° 24’ 45” (H).<br />
Collected by: Joana Xavier, Paola Rachello,<br />
Roger Bamber.<br />
Observations: (large dredge) G+H were pooled.<br />
STATION 38<br />
Date: 25-07-2006.<br />
Depth: 115-72 fathoms (207-129 m).<br />
Co-ordinates: N 37° 41’ 41” W 25° 25’ 06” to N<br />
37° 41’ 17” W 25° 25’ 10”.<br />
Collected by: Joana Xavier, Paola Rachello,<br />
Roger Bamber.<br />
Observations: (large dredge).<br />
STATION 39<br />
Date: 25-07-2006.<br />
Depth: 6.7 fathoms (12 m).<br />
Co-ordinates: N 37° 42’ 47” W 25° 25’ 34”.<br />
Collected by: Roger Bamber, Joana Xavier, Paola<br />
Rachello.<br />
Observations: (grab) two samples pooled.<br />
STATION 40 – off Amora, Ponta Garça.<br />
Date: 26-07-2006.<br />
Depth: 21 fathoms (38 m).<br />
Co-ordinates: N 37° 42’ 43” W 25° 21’ 33”.<br />
Collected by: Frias Martins, Jerry Harasewych.<br />
Observations: (small dredge).<br />
STATION 41 – off Amora, Ponta Garça.<br />
Date: 26-07-2006.<br />
Depth: 200-87 fathoms (360-156 m).<br />
Co-ordinates: N 37° 41’ 57” W 25° 22’ 08”.<br />
Collected by: Frias Martins, Jerry Harasewych.<br />
Observations: (large dredge); bottom drops suddenly<br />
to about 600 fathoms; tow up slope.<br />
STATION 42 – off Praia de Água d’Alto.<br />
Date: 26-07-2006.<br />
Depth: 83.6 fathoms (150 m).<br />
Co-ordinates: N 37° 42’ 35” W 25° 29’ 10”.<br />
Collected by: Frias Martins, Jerry Harasewych.<br />
Observations: (large dredge) rocky; octopus.<br />
STATION 43 – off Praia de Água d’Alto.<br />
Date: 26-07-2006.
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 21<br />
Depth: 130 fathoms (234 m).<br />
Co-ordinates: N 37° 41’ 44” W 25° 28’ 44”.<br />
Collected by: Frias Martins, Jerry Harasewych.<br />
Observations: (large dredge) rock.<br />
STATION 44 – off Praia de Água d’Alto.<br />
Date: 26-07-2006.<br />
Depth: 37 fathoms (66 m).<br />
Co-ordinates: N 37° 42’ 24” W 25° 28’ 59”.<br />
Collected by: Frias Martins, Jerry Harasewych.<br />
Observations: (small dredge).<br />
STATION 45 – off Vinha <strong>da</strong> Areia, Vila Franca<br />
do Campo.<br />
Date: 26-07-2006.<br />
Depth: 16.5 fathoms (30 m).<br />
Co-ordinates: N 37° 42’ 18” W 25° 25’ 26”.<br />
Collected by: Frias Martins, Jerry Harasewych.<br />
Observations: (small dredge) near sewage outlet.<br />
STATION 46 – off Vinha <strong>da</strong> Areia, Vila Franca<br />
do Campo.<br />
Date: 26-07-2006.<br />
Depth: 31 fathoms (56 m).<br />
Co-ordinates: N 37° 42’ 37” W 25° 25’ 18”.<br />
Collected by: Frias Martins, Jerry Harasewych.<br />
Observations: (small dredge).<br />
STATION 47 – off Vinha <strong>da</strong> Areia, Vila Franca<br />
do Campo.<br />
Date: 05-09-2006.<br />
Depth: 43 fathoms (77 m).<br />
Co-ordinates: N 37° 42’ 09” W 25° 25’ 04”.<br />
Collected by: Frias Martins, Patrícia Madeira,<br />
Henk van Goor.<br />
Observations: (small dredge).<br />
STATION 48 – off Vinha <strong>da</strong> Areia, Vila Franca<br />
do Campo.<br />
Date: 05-09-2006.<br />
Depth: 35 fathoms (63 m).<br />
Co-ordinates: N 37° 42’ 12” W 25° 25’ 09”.<br />
Collected by: Frias Martins, Patrícia Madeira,<br />
Henk van Goor.<br />
Observations: (small dredge).<br />
STATION 49 – off Vinha <strong>da</strong> Areia, Vila Franca<br />
do Campo.<br />
Date: 05-09-2006.<br />
Depth: 45 fathoms (81 m).<br />
Co-ordinates: N 37° 42’ 00” W 25° 25’ 15”.<br />
Collected by: Frias Martins, Patrícia Madeira,<br />
Henk van Goor.<br />
Observations: (small dredge).<br />
STATION 50 – off Vinha <strong>da</strong> Areia, Vila Franca<br />
do Campo.<br />
Date: 05-09-2006.<br />
Depth: 37 fathoms (66 m).<br />
Co-ordinates: N 37° 41’ 59” W 25° 25’ 22”.<br />
Collected by: Frias Martins, Patrícia Madeira,<br />
Henk van Goor.<br />
Observations: (small dredge).<br />
STATION 51 – off Amora, Ponta Garça.<br />
Date: 05-09-2006.<br />
Depth: 195 fathoms (351 m).<br />
Co-ordinates: N 37° 42’ 06” W 25° 20’ 47”.<br />
Collected by: Frias Martins, Patrícia Madeira,<br />
Henk van Goor.<br />
Observations: (large dredge) sponge, corals.<br />
STATION 52 – off Amora, Ponta Garça.<br />
Date: 05-09-2006.<br />
Depth: 150 fathoms (270 m).<br />
Co-ordinates: N 37° 42’ 07” W 25° 21’ 24”.<br />
Collected by: Frias Martins, Patrícia Madeira,<br />
Henk van Goor.<br />
Observations: (large dredge).<br />
STATION 53 – off Ponta Garça.<br />
Date: 05-09-2006.<br />
Depth: 177 fathoms (318 m).<br />
Co-ordinates: N 37° 42’ 01” W 25° 23’ 07”.<br />
Collected by: Frias Martins, Patrícia Madeira,<br />
Henk van Goor.<br />
Observations: (large dredge).<br />
STATION 54 – off Vinha <strong>da</strong> Areia, Vila Franca<br />
do Campo.<br />
Date: 05-09-2006.<br />
Depth: 37 fathoms (66 m).<br />
Co-ordinates: N 37° 42’ 11” W 25° 25’ 04”.<br />
Collected by: Frias Martins, Patrícia Madeira,<br />
Henk van Goor.<br />
Observations: (small dredge).<br />
STATION 55 – off Vila Franca do Campo.<br />
Date: 07-09-2006.<br />
Depth: 90 fathoms (162 m).<br />
Co-ordinates: —<br />
Collected by: Moisés Bolarinho, skipper of the<br />
fishing boat ‘Vila Franca’.
22 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
Observations: rock snagged on fishing gear;<br />
covered with mud, two white gorgonians,<br />
some sponges and living Chama.<br />
STATION 56 – off Vila Franca do Campo, east<br />
of Ilhéu.<br />
Date: 03-10-2006.<br />
Depth: 32 fathoms (58 m).<br />
Co-ordinates: N 37° 42’ 12” W 25° 25’ 08”.<br />
Collected by: Malacology class (Department of<br />
Biology, University of Azores).<br />
Observations: (small dredge) one tow 5 min<br />
and another 15 min, pooled.<br />
STATION 57 – off Vila Franca do Campo,<br />
west of Ilhéu.<br />
Date: 03-10-2006.<br />
Depth: 18 fathoms (32 m).<br />
Co-ordinates: N 37° 42’ 08” W 25° 26’ 49”.<br />
Collected by: Malacology class (Department of<br />
Biology, University of Azores).<br />
Observations: (small dredge) tow during 15<br />
min.<br />
STATION 58 – off Vila Franca do Campo,<br />
west of Ilhéu.<br />
Date: 03-10-2006.<br />
Depth: 18 fathoms (32 m).<br />
Co-ordinates: N 37° 42’ 08” W 25° 26’ 49”.<br />
Collected by: Malacology class (Department of<br />
Biology, University of Azores).<br />
Observations: (grab) 4 samples, pooled.<br />
TAXONOMIC LIST<br />
Phylum MOLLUSCA<br />
Class POLYPLACOPHORA Gray, 1821<br />
Order LEPIDOPLEURIDA Thiele, 1909<br />
Family Leptochitoni<strong>da</strong>e Dall, 1889<br />
Lepidochiton cimicoides (Monterosato, 1879)<br />
(Figure 1)<br />
Remarks: Specimens collected only at Station<br />
37; alive. Depth range: 0-50 m (P&G); 0-200 m<br />
(MM&B); this study, alive: 117-234 m.<br />
Order CHITONIDA Thiele, 1909<br />
Family Acanthochitoni<strong>da</strong>e Simroth, 1894<br />
Acanthochitona fascicularis (Linnaeus, 1767)<br />
(Figure 2)<br />
Remarks: Only loose valves were found; however,<br />
the number and freshness of the valves<br />
collected suggests that it could live on nearby<br />
rocky habitats. Ávila et al., 2000. Depth range:<br />
0-50 m (P&G); 0-200 m (MM&B); this study:<br />
30-129 m. Alive on IVFC (Martins, 2004).<br />
Class GASTROPODA Cuvier, 1797<br />
Subclass PROSOBRANCHIA Milne Edwards,<br />
1848<br />
Order ARCHAEOGASTROPODA Thiele, 1925<br />
Suborder DOCOGLOSSA Troschel, 1866<br />
Superfamily PATELLOIDEA Rafinesque, 1815<br />
Family Patelli<strong>da</strong>e Rafinesque, 1815<br />
Patella candei d’Orbigny, 1840<br />
Patella aspera Röding, 1798<br />
Remarks: Only small and very worn shells<br />
were found. These are known shallow water<br />
species and their presence in the samples is<br />
considered accidental. Alive on IVFC<br />
(Martins, 2004). Patella aspera has been incorrectly<br />
synonymized with P. ulyssiponensis<br />
Gmelin, 1791. Weber & Hawkins (2005) consider<br />
both genetically distinct, the name P.<br />
aspera referring to the Macaronesian populations<br />
whereas P. ulyssiponenis is applied to<br />
those in the continental coasts.<br />
Superfamily LOTIOIDEA Gray, 1840<br />
Family Lotii<strong>da</strong>e Gray, 1840<br />
Tectura virginea (O.F. Müller, 1776)<br />
(Figure 3)<br />
Remarks: Worn shells, in various degrees of<br />
preservation were found. The abun<strong>da</strong>nce,<br />
size and freshness of some specimens indicate<br />
that they could live on nearby rocky habitats.<br />
Ávila et al., 2000. Depth range: 0-100 m (P&G);<br />
this study: 14-360 m. Common alive on IVFC<br />
(Martins, 2004).<br />
Family Lepeti<strong>da</strong>e Gray, 1840<br />
Propilidium exiguum (Thompson, 1844)<br />
(Figure 4)<br />
Remarks: Only one specimen found. Depth<br />
range: 7-600 m (P&G); 1.480-2.190 m (MM&B,<br />
as P. ancyloide Forbes, 1849); this study: 156-<br />
360 m.<br />
Suborder VETIGASTROPODA Salvini-<br />
Plawén, 1980<br />
Superfamily FISSURELLOIDEA Fleming, 1822<br />
Family Fissurelli<strong>da</strong>e Fleming, 1822<br />
Emarginula sp.<br />
(Figure 5)<br />
Remarks: Only one specimen found, probably
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 23<br />
E. rosea Monterosato in Locard, 1892, or a juvenile<br />
of E. guernei Dautzenberg & Fischer, 1896.<br />
Depth range: 0-90 m (P&G); 0 m (MM&B); this<br />
study: 117-234 m.<br />
Family Scissurelli<strong>da</strong>e Gray, 1847<br />
Sinezona cingulata (O.G. Costa, 1861)<br />
(Figure 6)<br />
Remarks: Only one specimen found. Bullock et<br />
al., 1990 as Scissurella crispata Fleming, 1828;<br />
Bullock, 1995 as Schismope fayalensis<br />
Dautzenberg, 1889; Ávila et al., 2000. Depth<br />
range: 900 m (MM&B); this study: 117-145 m.<br />
Superfamily HALIOTOIDEA Rafinesque, 1815<br />
Family Halioti<strong>da</strong>e Rafinesque, 1815<br />
Haliotis coccinea Reeve, 1846<br />
(Figure 7)<br />
Remarks: Only small and worn shells were<br />
found. It is possible that the presence of shells<br />
in deeper water is accidental. Ávila et al., 2000.<br />
Depth range: 2-25 m (P&G; MM&B); this study:<br />
30-360 m. Common alive on IVFC (Martins,<br />
2004).<br />
?Haliotis sp.<br />
(Figure 8)<br />
Remarks: The only specimen collected had two<br />
holes topically similar to those of Haliotis and<br />
could be a juvenile. However, the shell morphology<br />
differs from that typical of the genus,<br />
namely the flattened columellar lip, and, therefore,<br />
it is only tentatively referred to Haliotis.<br />
Superfamily LEPETELLOIDEA Dall, 1882<br />
Family Lepetelli<strong>da</strong>e Dall, 1882<br />
Lepetella laterocompressa (de Rayneval & Ponzi,<br />
1854)<br />
(Figure 9)<br />
Remarks: Common in small fractions of deeper<br />
samples. Depth range, this study: 99-234 m.<br />
Family Addisonii<strong>da</strong>e Dall, 1882<br />
Addisonia excentrica (Tiberi, 1855)<br />
(Figure 10)<br />
Remarks: Only one specimen found. Depth<br />
range: 370-3.307 m (MM&B); this study: 117-<br />
234 m.<br />
Superfamily TROCHOIDEA Rafinesque, 1815<br />
Family Trochi<strong>da</strong>e Rafinesque, 1815<br />
Clelandella azorica Gofas, 2005<br />
(Figures 11-12)<br />
Remarks: Live specimens found only when the<br />
dredge hit hard surface. Endemic. Depth<br />
range, this study: 30-360 m; alive: 144-198 m.<br />
Clelandella sp.<br />
(Figure 13)<br />
Remarks: Rare. Depth range: 117-234 m.<br />
Jujubinus pseudogravinae Nordsieck, 1973<br />
(Figures 14-15)<br />
Remarks: Although live specimens were not collected,<br />
some shells were fresh, indicating that<br />
they could live in nearby habitats. Endemic.<br />
Ávila et al., 2000. Depth range: 0-200 m (P&G,<br />
MM&B, as J. exasperatus (Pennant, 1777)); this<br />
study: 18-360 m. Common alive on IVFC<br />
(Martins, 2004).<br />
Gibbula delgadensis Nordsieck, 1982<br />
(Figures 16-17)<br />
Remarks: Uncommon. Not collected alive but<br />
some shells were fresh, indicating that they<br />
could live in nearby habitats. Endemic. Depth<br />
range, this study: 38-234 m. Common alive on<br />
IVFC (Martins, 2004).<br />
Gibbula magus (Linnaeus, 1758)<br />
(Figures 18-22)<br />
Remarks: Common on sandy bottoms. The<br />
specimens from the Azores are smaller than<br />
their European conspecifics. Bullock et al.,<br />
1990; Ávila et al., 2000. Depth range: 0-70 m<br />
(P&G); this study: 14-360 m; alive: 18-360 m.<br />
Common alive on IVFC (Martins, 2004)<br />
Margarites sp.<br />
(Figure 23)<br />
Remarks: A few rolled specimens collected.<br />
Depth range, this study: 99-198 m.<br />
Family Solarielli<strong>da</strong>e Powell, 1951<br />
Solariella azorensis (Watson, 1886)<br />
(Figures 24-26)<br />
Remarks: Relatively common. Some ultrajuvenile<br />
specimens collected (Figure 26) fit<br />
the description provided by A<strong>da</strong>m &<br />
Knudsen (1969) for Rhodinoliotia roseotincta<br />
(Smith, 1871); since specimens of the latter<br />
species were not available for comparison, a<br />
decision on synonymy is not warranted.
24 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE I<br />
1. Leptochiton cimicoides (Monterosato, 1879) (Sta37)<br />
2. Acanthochitona fascicularis (Linnaeus, 1767) (Sta31)<br />
3. Tectura virginea (O.F. Müller, 1776) (Sta28)<br />
4. Propilidium exiguum (Thompson, 1844) (Sta41)<br />
5. Emarginula sp. (Sta37)<br />
6. Sinezona cingulata (O.G. Costa, 1861) (Sta28)<br />
7. Haliotis coccinea Reeve, 1846 (Sta26)<br />
8. ?Haliotis cf. coccinea Reeve, 1846 (juvenile) (Sta29)<br />
9. Lepetella laterocompressa (Rayneval & Ponzi, 1854) (Sta38)<br />
10. Addisonia excentrica (Tiberi, 1855) (Sta37)<br />
11. Clelandella azorica Gofas, 2005 (Sta29)<br />
12. Clelandella azorica Gofas, 2005 (Sta53)<br />
13. Clelandella sp. (Sta37)<br />
14. Jujubinus pseudogravinae Nordsieck, 1973 (Sta44)<br />
15. Jujubinus pseudogravinae Nordsieck, 1973 (Sta27)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 25
26 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE II<br />
16. Gibbula delgadensis Nordsieck, 1982 (Sta6)<br />
17. Gibbula delgadensis Nordsieck, 1982 (Sta46)<br />
18. Gibbula magus (Linnaeus, 1758) (Sta44)<br />
19. Gibbula magus (Linnaeus, 1758) (Vila Franca do Campo, 1991)<br />
20. Gibbula magus (Linnaeus, 1758) (Sta15)<br />
21. Gibbula magus (Linnaeus, 1758) (Sta15)<br />
22. Gibbula magus (Linnaeus, 1758) (Sta15)<br />
23. Margarites sp. (Sta29)<br />
24. Solariella azorensis Watson, 1886 (Sta29)<br />
25. Solariella azorensis Watson, 1886 (ultrajuvenile) (Sta12)<br />
26. Solariella azorensis Watson, 1886 (ultrajuvenile) (Sta12)<br />
27. Calliostoma hirondellei Dautzenberg & Fischer, 1896 (Sta37)<br />
28. Calliostoma lividum Dautzenberg 1927 (Sta37)<br />
29. Calliostoma lividum Dautzenberg 1927 (Sta45)<br />
30. Cirsonella gaudryi (Dautzenberg & Fisher, 1896) (Sta37)<br />
31. Tricolia pullus azorica (Dautzenberg, 1889) (Sta56)<br />
32. Tricolia pullus azorica (Dautzenberg, 1889) (Sta38)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 27
28 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE III<br />
33. Bittium cf. latreillii (Payraudeau, 1826) (Sta1)<br />
34. Bittium cf. latreillii (Payraudeau, 1826) (Sta40)<br />
35. Bittium latreillii (Payraudeau, 1826) (Sta32)<br />
36. Fossarus ambiguus (Linnaeus, 1758 (Sta28)<br />
37. Fossarus ambiguus (Linnaeus, 1758 (Sta2)<br />
38. Cheirodonta pallescens (Jeffreys, 1867) (Sta1)<br />
39. Cheirodonta pallescens (Jeffreys, 1867) (Sta12)<br />
40. Cheirodonta pallescens (Jeffreys, 1867) (Sta18)<br />
41. Cheirodonta pallescens (Jeffreys, 1867) (Sta28)<br />
42. Similiphora similior (Bouchet & Guillemot, 1978) (Sta18)<br />
43. Similiphora similior (Bouchet & Guillemot, 1978) (Sta25)<br />
44. Similiphora similior (Bouchet & Guillemot, 1978) (Sta56)<br />
45. Similiphora similior (Bouchet & Guillemot, 1978) (Sta40)<br />
46. Similiphora similior (Bouchet & Guillemot, 1978) (Sta6)<br />
47. Marshallora adversa (Montagu, 1803) (Sta13)<br />
48. Marshallora adversa (Montagu, 1803) (Sta44)<br />
49. Marshallora adversa (Montagu, 1803) Sta56)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 29
30 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE IV<br />
50. Marshallora adversa (Montagu, 1803) (Sta1)<br />
51. Marshallora adversa (Montagu, 1803) (Sta38)<br />
52. Marshallora adversa (Montagu, 1803) (Sta56)<br />
53. Marshallora adversa (Montagu, 1803) (Sta1)<br />
54. Marshallora adversa (Montagu, 1803) (Sta37)<br />
55. Marshallora cf. adversa (Montagu, 1803) (Sta32)<br />
56. Monophorus sp. (Sta1)<br />
57. Monophorus erythrosoma (Bouchet & Guillemot, 1978) (Sta54)<br />
58. Monophorus erythrosoma (Bouchet & Guillemot, 1978) (Sta56)<br />
59. Monophorus erythrosoma (Bouchet & Guillemot, 1978) (Sta40)<br />
60. Monophorus erythrosoma (Bouchet & Guillemot, 1978) (Sta24)<br />
61. Pogonodon pseudocanaricus (Bouchet, 1985) (Sta1)<br />
62. Monophorus thiriotae Bouchet, 1985 (Sta32)<br />
63. Monophorus thiriotae Bouchet, 1985 (Sta1)<br />
64. Monophorus thiriotae Bouchet, 1985 (Sta1)<br />
65. Strobiligera brychia (Bouchet & Guillemot, 1978) (Sta37)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 31
32 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE V<br />
66. Metaxia cf. abrupta (Watson, 1880) (Sta38)<br />
67. Cerithiopsis tubercularis (Montagu, 1803) (Sta2)<br />
68. Cerithiopsis tubercularis (Montagu, 1803) (Sta56)<br />
69. Cerithiopsis tiara (Monterosato, 1874) (Sta38)<br />
70. Cerithiopsis jeffreysi Watson, 1885 (Sta28)<br />
71. Cerithiopsis scalaris Locard, 1892 (Sta1)<br />
72. Cerithiopsis scalaris Locard, 1892 (Sta1)<br />
73. Cerithiopsis scalaris Locard, 1892 (Sta38)<br />
74. Cerithiopsis scalaris Locard, 1892 (Sta29)<br />
75. Cerithiopsis minima (Brusina, 1865) (Sta40)<br />
76. Cerithiopsis minima (Brusina, 1865) (Sta15)<br />
77. Cerithiopsis cf. minima (Brusina, 1865) (Sta2)<br />
78. Cerithiopsis cf. minima (Brusina, 1865) (Sta1)<br />
79. Cerithiopsis fayalensis Watson, 1886 (Sta28)<br />
80. Cerithiopsis fayalensis Watson, 1886 (Sta37)<br />
81. Krachia cf. guernei (Dautzenberg & Fischer, 1896) (Sta37)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 33
34 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE VI<br />
82. Epitonium turtonis (Turton, 1819) (Sta44)<br />
83. Epitonium clathrus (Linnaeus, 1758) (Sta44)<br />
84. Epitonium pulchellum (Bivona, 1832) (Sta12)<br />
85. Epitonium pulchellum (Bivona, 1832) (Sta27)<br />
86. Epitonium pulchellum (Bivona, 1832) (Sta56)<br />
87. Epitonium celesti (Ara<strong>da</strong>s, 1854) (Sta7)<br />
88. Epitonium celesti (Ara<strong>da</strong>s, 1854) (Sta44)<br />
89. Epitonium celesti (Ara<strong>da</strong>s, 1854) (Sta1)<br />
90. Epitonium celesti (Ara<strong>da</strong>s, 1854) (Sta1)<br />
91. Punctiscala cerigottana (Sturany, 1896) (Sta38)<br />
92. Opaliopsis atlantis (Clench & Turner, 1952) (Sta7)<br />
93. Cirsotrema cf. cochlea (Sowerby, 1844) (Sta31)<br />
94. Cirsotrema cf. cochlea (Sowerby, 1844) (Sta18)<br />
95. Acirsa subdecussata (Cantraine, 1835) (juvenile) (Sta1)<br />
96. Opalia hellenica (Forbes, 1844) (Sta48)<br />
97. Opalia sp. 1 (Sta27)<br />
98. Opalia sp. 2 (Sta38)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 35
36 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE VII<br />
99. Melanela bosci Payraudeau, 1826 (Sta37)<br />
100. Melanella cf. crosseana (Brusina, 1886) (Sta13)<br />
101. Melanella cf. crosseana (Brusina, 1886) (Sta2)<br />
102. Melanella cf. trunca (Watson, 1897) (Sta40)<br />
103. Parvioris microstoma (Brusina, 1864) (Sta2)<br />
104. Parvioris sp. (Sta2)<br />
105. Crinophteiros collinsi (Sykes, 1903) (Sta37)<br />
106. Sticteulima jeffreysiana (Brusina, 1869) (Sta12)<br />
107. Vitreolina sp. (Sta2)<br />
108. Vitreolina curva (Monterosato, 1884) (Sta1)<br />
109. Vitreolina curva (Monterosato, 1884) (Sta32)<br />
110. Pelseneeria minor Koehler & Vaney, 1908 (Sta28)<br />
111. Skeneopsis planorbis (Fabricius, 1870) (Sta1)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 37
38 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE VIII<br />
112. Rissoa guernei Dautzenberg, 1889 (Sta27)<br />
113. Rissoa guernei Dautzenberg, 1889 (Sta44)<br />
114. Rissoa guernei Dautzenberg, 1889 (Sta28)<br />
115. Rissoa sp. 1 (Sta28)<br />
116. Rissoa sp. 2 (Sta28)<br />
117. Setia subvaricosa Gofas, 1991 (Sta27)<br />
118. Setia subvaricosa Gofas, 1991 (Sta27)<br />
119. Setia cf. quisquiliarum (Watson 1886) (Sta41)<br />
120. Crisilla postrema (Gofas, 1991) (Sta27)<br />
121. Crisilla cf. postrema (Sta27)<br />
122. Crisilla cf. postrema (Sta28)<br />
123. Pseu<strong>dos</strong>etia azorica Bouchet & Warén, 1993 (Sta18)<br />
124. Pseu<strong>dos</strong>etia azorica Bouchet & Warén, 1993 (Sta38)<br />
125. Cingula trifasciata (A<strong>da</strong>ms, 1798) (Sta2)<br />
126. Manzonia unifasciata Dautzenberg, 1889 (Sta1)<br />
127. Manzonia unifasciata Dautzenberg, 1889 (Sta37)<br />
128. Manzonia unifasciata Dautzenberg, 1889 (Sta1)<br />
129. Onoba moreleti Dautzenberg, 1889 (Sta12)<br />
130. Onoba moreleti Dautzenberg, 1889 (Sta2)<br />
131. Onoba moreleti Dautzenberg, 1889 (Sta37)<br />
132. Onoba moreleti Dautzenberg, 1889 (Sta37)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 39
40 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE IX<br />
133. Alvania angioyi van Aartsen, 1982 (Sta1)<br />
134. Alvania angioyi van Aartsen, 1982 (Sta28)<br />
135. Alvania poucheti (Dautzenberg, 1889) (Sta1)<br />
136. Alvania poucheti (Dautzenberg, 1889) (Sta27)<br />
137. Alvania poucheti (Dautzenberg, 1889) (Sta32)<br />
138. Alvania mediolittoralis Gofas, 1989 (Sta1)<br />
139. Alvania punctura (Montagu, 1803) (Sta37)<br />
140. Alvania sp. (?tarsodes Watson, 1886) (Sta1)<br />
141. Alvania sleursi (Amati, 1987) (Sta1)<br />
142. Alvania sleursi (Amati, 1987) (Sta37)<br />
143. Alvania cancellata (<strong>da</strong> Costa, 1778) (Sta1)<br />
144. Alvania cancellata (<strong>da</strong> Costa, 1778) (Sta58)<br />
145. Alvania cancellata (<strong>da</strong> Costa, 1778) (Sta44)<br />
146. Alvania cancellata (<strong>da</strong> Costa, 1778) (Sta44)<br />
147. Alvania cancellata (<strong>da</strong> Costa, 1778) (Sta37)<br />
148. Alvania platycephala Dautzenberg & Fisher, 1896 (Sta41)<br />
149. Alvania platycephala Dautzenberg & Fisher, 1896 (Sta41)<br />
150. Alvania platycephala Dautzenberg & Fisher, 1896 (Sta37)<br />
151. Alvania platycephala Dautzenberg & Fisher, 1896 (Sta37)<br />
152. Alvania cimicoides (Forbes, 1844) (Sta37)<br />
153. Alvania cimicoides (Forbes, 1844) (Sta37)<br />
154. Alvania cf. cimicoides (Forbes, 1844) (Sta41)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 41
42 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE X<br />
155. Caecum wayae Pizzini & Nofroni, 2001 (Sta12)<br />
156. Caecum wayae Pizzini & Nofroni, 2001 (Sta18)<br />
157. Talassia cf. tenuisculpta (Watson 1873) (Sta37)<br />
158. Talassia cf. tenuisculpta (Watson 1873) (Sta27)<br />
159. Capulus ungaricus (Linnaeus, 1758) (Sta7)<br />
160. Lamellaria perspicua (Linnaeus, 1758) (Vila Franca do Campo, 1991)<br />
161. Lamellaria perspicua (Linnaeus, 1758) (Sta56)<br />
162. Trivia pulex (Solander in J.E. Gray, 1828 (Vila Franca do Campo, 1991)<br />
163. Trivia pulex (Solander in J.E. Gray, 1828 (Sta56)<br />
164. Trivia pulex (Solander in J.E. Gray, 1828 (Sta56)<br />
165. Trivia candidula (Gaskoin, 1835) (Sta44)<br />
166. Erato sp. (juvenile) (Sta2)<br />
167. Erato sp. (juvenile) (Sta38)<br />
168. Aperiovula juanjosensii Perez & Gomez, 1987 (Sta38)<br />
169. Notocochlis dillwynii (Payraudeau, 1826) (Sta53)<br />
170. Natica prietoi (Hi<strong>da</strong>lgo, 1873) (Sta15)<br />
171. Natica prietoi (Hi<strong>da</strong>lgo, 1873) (Sta40)<br />
172. Natica prietoi (Hi<strong>da</strong>lgo, 1873) (Sta56)<br />
173. Natica cf. prietoi (Hi<strong>da</strong>lgo, 1873) (Sta57)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 43
44 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XI<br />
174. Atlanta peronii Lesueur, 1817 (Sta13)<br />
175. Protatlanta souleyeti (E.A. Smith, 1888) (Sta13)<br />
176. Ocenebra erinaceus juvenile (Linnaeus, 1758) (Sta27)<br />
177. Ocenebra sp. (Sta56)<br />
178. Ocinebrina aciculata (Lamarck,1822) (Sta40)<br />
179. Ocinebrina cf. aciculata (Payraudeau, 1826) (Sta41)<br />
180. ? Ocinebrina aciculata (Lamarck,1822) (Sta40)<br />
181. ?Ocinebrina cf. aciculata (Payraudeau, 1826) (Sta27)<br />
182. ?Ocinebrina sp. (Sta15)<br />
183. Orania fusulus (Brocchi, 1814) (Sta1)<br />
184. Orania fusulus (Brocchi, 1814) (Sta1)<br />
185. Orania fusulus (Brocchi, 1814) (Sta41)<br />
186. Trophonopsis barvicensis (Johnston, 1825) (Sta29)<br />
187. Trophonopsis barvicensis (Johnston, 1825) (Sta29)<br />
188. Trophonopsis barvicensis (Johnston, 1825) (Sta29)<br />
189. Trophonopsis barvicensis (Johnston, 1825) (Sta44)<br />
190. Trophonopsis barvicensis (Johnston, 1825) (Sta27)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 45
46 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XII<br />
191. Trophonopsis barvicensis (Johnston, 1825) (Sta46)<br />
192. Trophonopsis barvicensis (Johnston, 1825) (Sta15)<br />
193. Trophonopsis cf. muricatus (Montagu,1803) (Sta5)<br />
194. Trophonopsis cf. muricatus (Montagu,1803) (Sta27)<br />
195. Coralliophila cf. meyendorfii (Calcara, 1845) (Sta7)<br />
196. Coralliophila panormitana (Monterosato, 1896) (Sta37)<br />
197. Stramonita haemastoma (Linnaeus, 1767) (Sta27)<br />
198. Gibberula vignali (Dautzenberg & Fischer 1896) (Sta41)<br />
199. Gibberula cf. lazaroi Contreras, 1992 (Sta37)<br />
200. Mitra cornea Lamarck, 1811 (Sta31)<br />
201. Pollia dorbignyi (Payraudeau, 1826) (Sta45)<br />
202. Pollia dorbignyi (Payraudeau, 1826) Ilhéu de Vila Franca do Campo.<br />
203. Nassarius incrassatus (Ström, 1768) (Sta40)<br />
204. Nassarius incrassatus (Ström, 1768) (Sta30)<br />
205. Nassarius incrassatus (Ström, 1768) (Sta26)<br />
206. Nassarius incrassatus (teratology) (Ström, 1768) (Sta40)<br />
207. Nassarius cf. cuvierii (Payraudeau, 1826). Juvenile (Sta44)<br />
208. Nassarius recidivus (Martens, 1876) (Sta53)<br />
209. Columbella a<strong>da</strong>nsoni Menke, 1853 (Sta44)<br />
210. Mitrella pallaryi (Dautzenberg, 1927) (Sta37)<br />
211. Anachis avaroides Nordsieck, 1975 (Sta44)<br />
212. Anachis avaroides Nordsieck, 1975 (Sta1)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 47
48 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XIII<br />
213. Brocchinia clenchi Petit, 1986 (Sta49)<br />
214. Brocchinia clenchi Petit, 1986 (Sta1)<br />
215. Mitromorpha azorensis Mifsud, 2001 (Sta46)<br />
216. Mitromorpha azorensis Mifsud, 2001 (Sta1)<br />
217. Bela nebula (Montagu, 1803) (Sta56)<br />
218. Bela nebula (Montagu, 1803) (Sta1)<br />
219. Bela nebula (Montagu, 1803) (Sta1)<br />
220. Bela nebula (Montagu, 1803) (Sta56)<br />
221. Bela nebula (Montagu, 1803) (Sta56)<br />
222. Bela nebula (Montagu, 1803) (Sta18)<br />
223. Mangelia cf. costata (Donovan, 1804) (Sta25)<br />
224. Mangelia cf. costata (Donovan, 1804) (Sta29)<br />
225. Mangelia cf. costata (Donovan, 1804) (Sta29)<br />
226. Mangelia cf. costata (Donovan, 1804) (Sta30)<br />
227. Mangelia cf. costata (Donovan, 1804) (Sta1)<br />
228. Mangelia cf. costata (Donovan, 1804) (Sta1)<br />
229. Mangelia cf. costata (Donovan, 1804) (Sta18)<br />
230. Raphitoma purpurea (Montagu, 1803) (Sta56)<br />
231. Raphitoma linearis (Montagu, 1803) (Sta40)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 49
50 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XIV<br />
232. Raphitoma cf. aequalis (Jeffreys, 1867) (Sta56)<br />
233. Raphitoma cf. aequalis (Jeffreys, 1867) (Sta27)<br />
234. Raphitoma cf. aequalis (Jeffreys, 1867) (Sta57)<br />
235. Raphitoma cf. aequalis (Jeffreys, 1867) (Sta56)<br />
236. Raphitoma cf. aequalis (Jeffreys, 1867) (Sta40)<br />
237. Raphitoma cf. aequalis (Jeffreys, 1867) (Sta5)<br />
238. Raphitoma cf. aequalis (Jeffreys, 1867) (Sta56)<br />
239. Raphitoma cf. aequalis (Jeffreys, 1867) (Sta30)<br />
240. Raphitoma cf. aequalis (Jeffreys, 1867) (Sta40)<br />
241. Raphitoma sp. (Sta58)<br />
242. Pleurotomella gibbera Bouchet & Warén, 1980 (Sta29)<br />
243. Pleurotomella gibbera Bouchet & Warén, 1980 (Sta32)<br />
244. Pleurotomella gibbera Bouchet & Warén, 1980 (Sta27)<br />
245. Pleurotomella cf. gibbera Bouchet & Warén, 1980 (Sta29)<br />
246. Teretia teres (Reeve, 1844) (Sta28)<br />
247. Teretia teres (Reeve, 1844) (Sta27)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 51
52 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XV<br />
248. Crassopleura maravignae (Bivona, 1838) (Sta56)<br />
249. Crassopleura maravignae (Bivona, 1838) (Sta50)<br />
250. Crassopleura maravignae (Bivona, 1838) (Sta37)<br />
251. Haedropleura septangularis (Montagu, 1803) (Sta15)<br />
252. Haedropleura septangularis (Montagu, 1803) (Sta56)<br />
253. Philippia krebsi (Mörch, 1875) (Sta46)<br />
254. Pseudotorinia architae (O.G. Costa, 1841) (Sta32)<br />
255. Pseudomalaxis zanclaeus (Philippi, 1844) (Sta37)<br />
256. Mathil<strong>da</strong> cochlaeformis Brugnone, 1873 (Sta29)<br />
257. Mathil<strong>da</strong> retusa Brugnone, 1873 (Sta37)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 53
54 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XVI<br />
258. ?Rissoella sp. 1 (Sta41)<br />
259. ?Rissoella sp. 2 (Sta2)<br />
260. Omalogyra atomus (Philippi, 1841) (Sta28)<br />
261. O<strong>dos</strong>tomella doliolum (Philippi, 1844) (Sta37)<br />
262. O<strong>dos</strong>tomella doliolum (Philippi, 1844) (Sta32)<br />
263. Chrysalli<strong>da</strong> cf. flexuosa (Monterosato, 1874 ex Jeffreys) (Sta41)<br />
264. O<strong>dos</strong>tomia bernardi Aartsen, Gittenberger & Goud, 1998 (Sta58)<br />
265. O<strong>dos</strong>tomia cf. verhoeveni Aartsen, Gittenberger & Goud, 1998 (Sta1)<br />
266. O<strong>dos</strong>tomia duureni Aartsen, Gittenberger & Goud, 1998 (Sta15)<br />
267. O<strong>dos</strong>tomia cf. striolata Forbes & Hanley, 1850 (Sta18)<br />
268. Eulimella sp. (Sta38)<br />
269. Turbonilla rufa (Philippi, 1836) (Sta1)<br />
270. Turbonilla lactea (Linnaeus, 1758) (Sta56)<br />
271. Turbonilla sp. 1 (Sta38)<br />
272. Turbonilla sp. 2 (Sta38)<br />
273. Turbonilla sp. 3 (Sta37)<br />
274. Turbonilla sp. 4 (Sta38)<br />
275. Ebala nitidissima (Montagu, 1803) (Sta28)<br />
276. Ebala nitidissima (Montagu, 1803) (Sta18)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 55
56 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XVII<br />
277. Colpo<strong>da</strong>spis pusilla Sars, 1870 (Sta7)<br />
278. Retusa truncatula (Bruguière, 1792) (Sta27)<br />
279. Retusa truncatula (Bruguière, 1792) (Sta1)<br />
280. Haminoea cf. orteai Talavera, Murillo & Templado, 1987 (Sta58)<br />
281. Atys macandrewi E.A. Smith, 1872 (Sta56)<br />
282. Atys sp. (Sta15)<br />
283. Philine approximans Dautzenberg & Fischer, 1896 (Sta13)<br />
284. Philine sp. (Sta18)<br />
285. ?Chelidonura africana Pruvot-Fol, 1953 (Sta37)<br />
286. Cavolinia inflexa (Lesueur, 1813) (Sta56)<br />
287. Cavolinia inflexa (Lesueur, 1813) (Sta29)<br />
288. Cavolinia tridentata (Forskal, 1775) (Sta37)<br />
289. Diacria trispinosa (Lesueur, 1821) (Sta50)<br />
290. Diacria trispinosa (Lesueur, 1821) (Sta12)<br />
291. Cuvierina atlantica (Bé, MacClintock & Currie, 1972) (Sta38)<br />
292. Clio pyrami<strong>da</strong>ta Linnaeus, 1767 (Sta29)<br />
293. Clio pyrami<strong>da</strong>ta Linnaeus, 1767 (Sta12)<br />
294. Limacina cf. helicina (Phipps, 1774) (Sta32)<br />
295. Limacina inflata (d’Orbigny, 1836) (Sta1)<br />
296. Umbraculum umbraculum (Lightfoot, 1786) (Sta31)<br />
297. Tylodina perversa (Gmelin, 1791) (Sta28)<br />
298. Williamia gussonii (O.G. Costa, 1829) (St12)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 57
58 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
Endemic. Depth range, this study: 14-360 m;<br />
alive from 14-207 m.<br />
Calliostomati<strong>da</strong>e Thiele, 1924<br />
Calliostoma hirondellei Dautzenberg & Fisher,<br />
1896<br />
(Figure 27)<br />
Remarks: Rare. Depth range, this study: 72-<br />
234 m.<br />
Calliostoma lividum Dautzenberg, 1927<br />
(Figures 28-29)<br />
Remarks: Sometimes subti<strong>da</strong>l in the Azores.<br />
Endemic. Ávila et al., 2000 as C. cf. conulus<br />
(Linnaeus, 1758). Depth range: 20-200 m<br />
(P&G and MM&B, as C. conulum (L.)); this<br />
study: 30-360 m. Alive on IVFC (Martins,<br />
2004).<br />
Superfamily TURBINOIDEA Rafinesque,<br />
1815<br />
Family Turbini<strong>da</strong>e Rafinesque, 1815<br />
Cirsonella gaudryi (Dautzenberg & Fisher,<br />
1896)<br />
(Figure 30)<br />
Remarks: Rare. Depth range, this study: 117-<br />
234 m.<br />
Family Phasianelli<strong>da</strong>e Swainson, 1840<br />
Tricolia pullus azorica (Dautzenberg, 1889)<br />
(Figures 31-32)<br />
Remarks: Some specimens were fresh, indicating<br />
that they could live in nearby habitats.<br />
Endemic. Bullock et al., 1990, Bullock, 1995<br />
and Knudsen, 1995 as T. pullus (Linnaeus,<br />
1758); Ávila et al., 2000. Depth range: interti<strong>da</strong>l-35<br />
m (P&G, as T. pullus (L.)); this study:<br />
14-360 m. Common alive on IVFC (Martins,<br />
2004).<br />
Order APOGASTROPODA Salvini-Plawén &<br />
Haszprunar, 1987<br />
Suborder CAENOGASTROPODA Cox, 1959<br />
Superfamily CERITHIOIDEA Fleming, 1822<br />
Family Cerithii<strong>da</strong>e Fleming, 1822<br />
Bittium cf. latreillii (Payraudeau, 1826)<br />
(Figures 33-34)<br />
Remarks: This form of Bittium has been questionably<br />
ascribed to B. latreillii, and awaits further<br />
study to clarify its taxonomic status.<br />
Shells are very common. Bullock et al., 1990<br />
and Bullock, 1995 as B. reticulatum (<strong>da</strong> Costa,<br />
1779); Ávila et al., 2000. Depth range: littoral<br />
(MM&B); this study: 14-360 m; alive at 38 m.<br />
Common alive on IVFC (Martins, 2004).<br />
Bittium latreillii (Payraudeau, 1826)<br />
(Figure 35)<br />
Remarks: Very rare. This specimen conforms to<br />
the description of B. latreillii. Depth range: littoral<br />
(MM&B); this study: 180 m.<br />
Family Planaxi<strong>da</strong>e Gray, 1850<br />
Fossarus ambiguus (Linaeus, 1758)<br />
(Figures 36-37)<br />
Remarks: Occurs regularly in the samples.<br />
Houbrick, 1990; Bullock, 1995; Knudsen, 1995;<br />
Ávila et al., 2000. Depth range: littoral<br />
(MM&B); this study: 30-180 m. Common alive<br />
on IVFC (Martins, 2004).<br />
Superfamily TRIPHOROIDEA Gray, 1847<br />
Triphori<strong>da</strong>e Gray, 1847<br />
NOTE: Triphorids were present in most samples.<br />
No living specimens were collected,<br />
although some shells appeared to be fresh;<br />
commonly, they exhibited clear signs of pre<strong>da</strong>tion.<br />
The species of this family are difficult to<br />
identify without information on the animal<br />
and the larval shell; the granulation of the<br />
spiral and basal cords is often less distinct and<br />
intermediate. Although tentatively identified<br />
to species, they are however illustrated<br />
profusely to record their variability, and<br />
to provide a basis for further, perhaps more<br />
accurate identifications. Information on<br />
www.naturamediterraneo.com, based on<br />
Bouchet & Guillemot (1978) and Bouchet<br />
(1984), was helpful for species identification.<br />
Cheirodonta pallescens (Jeffreys, 1867)<br />
(Figures 38-41)<br />
Remarks: Shell light-brown to whitish, uniformly<br />
coloured; protoconch bi-carinated; spiral<br />
cord 4 and basal cords smooth; supranumerary<br />
cords on last whorl. Depth range, this study:<br />
30-145 m.<br />
Similiphora similior (Bouchet & Guillemot, 1978)<br />
(Figures 42-46)<br />
Remarks: Shell brownish, variously coloured; 1 st<br />
whorl of protoconch uni-carinated, remaining<br />
bi-carinated; spiral cord 4 granulated, basal
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 59<br />
cords smooth; supranumerary cords on last<br />
whorl. Depth range, this study: 14-360 m.<br />
Marshallora adversa (Montagu, 1803)<br />
(Figures 47-54)<br />
Remarks: Shell brownish, variously coloured;<br />
protoconch bi-carinated; spiral cord 4 and<br />
basal cords smooth; tubercles on last whorl<br />
elongated; absence of supranumerary cords on<br />
last whorl. Depth range, this study: 30-234 m.<br />
Marshallora cf. adversa (Montagu, 1803)<br />
(Figure 55)<br />
Remarks: The presence of brownish markings<br />
between tubercles is reminiscent of M. thiriotae,<br />
but other characters indicate affinity with M.<br />
adversa. Depth range, this study: 46 m.<br />
Monophorus sp.<br />
(Figure 56)<br />
Remarks: Depth range, this study: 40-135 m.<br />
Monophorus erythrosoma (Bouchet & Guillemot,<br />
1978)<br />
(Figures 57-60)<br />
Remarks: Shell brownish, unicoloured or variously<br />
coloured; protoconch bi-carinated; spiral<br />
cord 4 granulated, basal cords 1-2 granulated, 3<br />
smooth; supranumerary cords on last whorl.<br />
Depth range, this study: 38-243 m.<br />
Monophorus thiriotae Bouchet, 1985<br />
(Figures 62-64)<br />
Remarks: Shell brownish, variously coloured;<br />
protoconch bi-carinated; spiral cord 4 granulated,<br />
basal cords 1-2 granulated, 3 smooth;<br />
absence of supranumerary cords on last whorl;<br />
brownish intertuberculary markings. Depth<br />
range, this study: 30-207 m.<br />
Pogonodon pseudocanaricus (Bouchet, 1985)<br />
(Figure 61)<br />
Remarks: Shell whitish, brown vertical markings;<br />
protoconch redish, bi-carinated; spiral cord 4<br />
granulated, basal cords 1-2 granulated. Only<br />
one apparently fresh specimen, but with last<br />
whorl crushed. Depth range, this study: 57 m.<br />
Strobiligera brychia (Bouchet & Guillemot,<br />
1978)<br />
(Figure 65)<br />
Remarks: Tubercles of spiral cord 1 smaller than<br />
those of remaining cords. Rare. Depth range,<br />
this study: 117-234 m.<br />
Metaxia cf. abrupta (Watson, 1880)<br />
(Figure 66)<br />
Remarks: Only one specimen collected, apparently<br />
a juvenile. Depth range, this study: 129-<br />
207 m.<br />
Family Cerithiopsi<strong>da</strong>e A<strong>da</strong>ms H. & A., 1853<br />
Cerithiopsis tubercularis (Montagu, 1803)<br />
(Figures 67-68)<br />
Remarks: Relatively rare. Depth range: littoral-<br />
100 m (MM&B); this study: 41-207m.<br />
Cerithiopsis tiara (Monterosato, 1874)<br />
(Figure 69)<br />
Remarks: Rare. Depth range, this study: 129-<br />
207 m.<br />
Cerithiopsis jeffreysi Watson, 1885<br />
(Figure 70)<br />
Remarks: Rare. Depth range, this study: 117-<br />
207 m.<br />
Cerithiopsis scalaris Locard, 1892<br />
(Figures 71-74)<br />
Remarks: Shells uncommon but some specimens<br />
appeared fresh. Depth range, this study:<br />
57-234 m.<br />
Cerithiopsis minima (Brusina, 1865)<br />
(Figures 75-76)<br />
Remarks: Uncommon. Depth range, this study:<br />
38-207 m.<br />
Cerithiopsis cf. minima (Brusina, 1865)<br />
(Figures 77-78)<br />
Remarks: Uncommon. Depth range, this study:<br />
57-135 m.<br />
Cerithiopsis fayalensis Watson, 1886<br />
(Figures 79-80)<br />
Remarks: Shells uncommon but some specimens<br />
appeared fresh. Depth range, this study:<br />
99-234 m.<br />
Krachia cf. guernei (Dautzenberg & Fischer,<br />
1896)<br />
(Figure 81)<br />
Remarks: Rare. Depth range, this study: 117-<br />
234 m.
60 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
Superfamily JANTHINOIDEA Gray, 1847<br />
Family Epitonii<strong>da</strong>e S.S. Berry, 1910 (1812)<br />
Gyroscala lamellosa (Lamarck, 1822)<br />
Remarks: Only one fragment. Depth range:<br />
Infralittoral to 620 m (MM&B); this study: 56 m.<br />
Epitonium turtonis (Turton, 1819)<br />
(Figure 82)<br />
Remarks: Rare. Depth range: 5-70 m (P&G); this<br />
study: 66m.<br />
Epitonium clathrus (Linnaeus, 1758)<br />
(Figure 83)<br />
Remarks: Rare. Depth range: 5-70 m (P&G); this<br />
study: 66-72 m.<br />
Epitonium pulchellum (Bivona, 1832)<br />
(Figures 84-86)<br />
Remarks: Not uncommon. Depth range: 20-40 m<br />
(P&G; MM&B); this study: 58-145 m.<br />
Epitonium celesti (Ara<strong>da</strong>s, 1854)<br />
(Figures 87-90)<br />
Remarks: Not uncommon. Depth range: 50-1250<br />
m (P&G; MM&B); this study: 57-207 m.<br />
Punctiscala cerigottana (Sturany, 1819)<br />
(Figure 91)<br />
Remarks: Rare. Only one <strong>da</strong>maged specimen<br />
found. Depth range: 50-600 m (MM&B); this<br />
study: 129-207 m.<br />
Opaliopsis atlantis (Clench & Turner, 1952)<br />
(Figure 92)<br />
Remarks: Rare. Only one <strong>da</strong>maged specimen<br />
found. Depth range: 810-825 m (MM&B); this<br />
study: 167-189 m.<br />
Cirsotrema cf. cochlea (Sowerby, 1844)<br />
(Figures 93-94)<br />
Remarks: Uncommon. The Azorean specimens<br />
are stouter and more globose than the illustrations<br />
consulted (P&G). Depth range:<br />
Infralittoral-60 m (MM&B); this study: 40-318 m;<br />
alive: 66-72 m.<br />
Acirsa subdecussata (Cantraine, 1835)<br />
(Figure 95)<br />
Remarks: Only one fresh specimen collected.<br />
Depth range: 12-500 m (P&G; MM&B); this study:<br />
57 m.<br />
Opalia hellenica (Forbes, 1844)<br />
(Figure 96)<br />
Remarks: Uncommon. Ávila et al., 2000. Depth<br />
range: 20-770 m (MM&B); this study: 63-234 m;<br />
alive: 66-81 m.<br />
Opalia sp. 1<br />
(Figure 97)<br />
Remarks: Rare. Depth range, this study: 99-<br />
108 m.<br />
Opalia sp. 2<br />
(Figure 98)<br />
Remarks: Only one shell collected, with broken<br />
tip. Depth range, this study: 129-207 m.<br />
Superfamily EULIMOIDEA Philippi, 1853<br />
Family Eulimi<strong>da</strong>e Philippi, 1853<br />
Melanella bosci Payraudeau, 1826<br />
(Figure 99)<br />
Remarks: Rare. Depth range: 10-150 m (P&G);<br />
this study: 45-234 m.<br />
Melanella cf. crosseana (Brusina, 1886)<br />
(Figures 100-101)<br />
Remarks: Uncommon. Depth range, this study:<br />
73-145 m.<br />
Melanella cf. trunca (Watson, 1897)<br />
(Figure 102)<br />
Remarks: Rare. Depth range, this study: 30-<br />
38 m.<br />
Parvioris microstoma (Brusina, 1864)<br />
(Figure 103)<br />
Remarks: Rare. Depth range, this study: 135 m.<br />
Parvioris sp.<br />
(Figure 104)<br />
Remarks: Rare. Depth range, this study: 135-<br />
207 m.<br />
Crinophteiros collinsi (Sykes, 1903)<br />
(Figure 105)<br />
Remarks: Rare. Depth range, this study: 117-<br />
234 m.<br />
Sticteulima jeffreysiana (Brusina, 1869)<br />
(Figure 106)<br />
Remarks: Rare. Depth range, this study: 95-<br />
121 m.
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 61<br />
Vitreolina sp.<br />
(Figure 107)<br />
Remarks: Rare. Depth range, this study: 135 m.<br />
Vitreolina curva (Monterosato, 1884)<br />
(Figures 108-109)<br />
Remarks: Rare. Depth range, this study: 57-180 m.<br />
Pelseneeria minor Koehler & Vaney, 1908<br />
(Figure 110)<br />
Remarks: Only one specimen collected. Depth<br />
range: 90-185 m (MM&B); this study: 117-145 m.<br />
Superfamily LITTORINOIDEA Children, 1834<br />
Family Littorini<strong>da</strong>e Children, 1834<br />
Littorina striata King & Broderip, 1832<br />
Remarks: This is a supralittoral species, and<br />
its presence in the dredged material is accidental.<br />
Melarhaphe neritoides (Linnaeus, 1758)<br />
Remarks: This is a supralittoral species, and its<br />
presence in the dredged material is accidental.<br />
Family Skeneopsi<strong>da</strong>e Ire<strong>da</strong>le, 1915<br />
Skeneopsis planorbis (Fabricius, 1870)<br />
(Figure 111)<br />
Remarks: Uncommon. Reported as very common<br />
(Bullock et al., 1990; Bullock, 1995). Knudsen, 1995;<br />
Ávila et al., 2000. Depth range: Infralittoral to 70m<br />
(P&G; MM&B); this study: 32-145 m. Common<br />
alive on IVFC (Martins, 2004).<br />
Superfamily RISSOOIDEA Gray, 1847<br />
Family Rissoi<strong>da</strong>e Gray, 1847<br />
Rissoa guernei Dautzenberg, 1889<br />
(Figures 112-114)<br />
Remarks: Uncommon but some specimens<br />
appeared fresh. Endemic. Reported as very common<br />
(Bullock et al., 1990; Ávila, 2000). Gofas, 1990;<br />
Knudsen, 1995; Ávila et al., 2000. Depth range, this<br />
study: 32-234 m. Common alive on IVFC<br />
(Martins, 2004).<br />
Rissoa sp. 1<br />
(Figure 115)<br />
Remarks: Rare. Depth range, this study: 117-145 m.<br />
Rissoa sp. 2<br />
(Figure 116)<br />
Remarks: Rare. Depth range, this study: 99-180 m.<br />
Setia subvaricosa Gofas, 1990<br />
(Figures 117-118)<br />
Remarks: Rare. Endemic. This species is<br />
common in 15-20 m (Gofas, 1990; Ávila, 2000).<br />
Ávila et al., 2000. Depth range, this study: 99-<br />
135 m. Collected alive at IVFC (Martins, 2004).<br />
Setia cf. quisquiliarum (Watson 1886)<br />
(Figure 119)<br />
Remarks: Rare. Endemic. Depth range, this<br />
study: 237-360 m.<br />
Crisilla postrema (Gofas, 1990)<br />
(Figure 120)<br />
Remarks: Rare. Endemic. Infralittoral to 20 m;<br />
collected alive at IVFC (Gofas, 1990). Bullock et<br />
al., 1990 as Rissoa pulcherima (Jeffreys, 1848);<br />
Bullock, 1995 as Alvania postrema. Depth range,<br />
this study: 56-360m.<br />
Crisilla cf. postrema (Gofas, 1990)<br />
(Figures 121-122)<br />
Remarks: Rare. Depth range, this study: 99-<br />
207 m.<br />
Pseu<strong>dos</strong>etia azorica Bouchet & Warén, 1993<br />
(Figures 123-124)<br />
Remarks: Rare. Endemic. Depth range, this<br />
study: 72-207 m.<br />
Cingula trifasciata (A<strong>da</strong>ms, 1798)<br />
(Figure 125)<br />
Remarks: Rarely collected. Specimens eroded,<br />
probably transported from the interti<strong>da</strong>l,<br />
where it is common. Depth range, this study:<br />
38-180 m.<br />
Manzonia unifasciata Dautzenberg, 1889<br />
(Figures 126-128)<br />
Remarks: Relatively common; probably transported<br />
from infralittoral zone where it is very<br />
common from 0-10 m (Ávila, 2003). Bullock et<br />
al., 1990 and Bullock, 1995 as M. crassa<br />
(Kanmacher, 1798); Gofas, 1990; Knudsen,<br />
1995; 1995; Ávila et al., 2003. Depth range, this<br />
study: 237-360 m. Collected alive at IVFC<br />
(Martins, 2004).<br />
Onoba moreleti Dautzenberg, 1889<br />
(Figures 129-132)<br />
Remarks: Uncommon. Endemic. Depth range,<br />
this study: 95-234 m.
62 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
Alvania angioyi van Aartsen, 1982<br />
(Figures 133-134)<br />
Remarks: Rare. Endemic. Infralittoral to 20 m<br />
(Gofas, 1990). Bullock et al., 1990 as A, watsoni<br />
(Schwartz MS) Watson, 1873; Bullock, 1995;<br />
Knudsen, 1995; Ávila et al. 2000. Depth range,<br />
this study: 57-360 m. Collected alive at IVFC<br />
(Martins, 2004).<br />
Alvania poucheti Dautzenberg, 1889<br />
(Figures 135-137)<br />
Remarks: Relatively common; some specimens<br />
appeared fresh. Endemic. Gofas, 1990;<br />
Bullock et al., 1990; Bullock, 1995; Knudsen,<br />
1995; Ávila et al. 2000. Depth range, this<br />
study: 38-207 m. Collected alive at IVFC<br />
(Martins, 2004).<br />
Alvania mediolittoralis Gofas, 1989<br />
(Figure 138)<br />
Remarks: Rare. Common interti<strong>da</strong>lly (Gofas,<br />
1990). Depth range, this study: 30-207 m.<br />
Alvania punctura (Montagu, 1803)<br />
(Figure 139)<br />
Remarks: Very rare. Depth range, this study:<br />
117-234 m.<br />
Alvania sp. (?tarsodes Watson, 1886)<br />
(Figure 140)<br />
Remarks: Very rare. Depth range, this study:<br />
57 m.<br />
Alvania sleursi (Amati, 1987)<br />
(Figures 141-142)<br />
Remarks: Common; some specimens appeared<br />
fresh. Infralittoral, common at 20 m (Gofas,<br />
1990; Knudsen, 1995). Depth range, this study:<br />
30-234 m.<br />
Alvania cancellata (<strong>da</strong> Costa, 1778)<br />
(Figures 143-147)<br />
Remarks: Common; some specimens appeared<br />
fresh. Infralittoral, most common at 20 m<br />
(Gofas, 1990; Knudsen, 1995). Depth range,<br />
this study: 30-360 m.<br />
Alvania platycephala Dautzenberg & Fischer,<br />
1896<br />
(Figures 148-151)<br />
Remarks: Rare. Endemic. Depth range, this<br />
study: 129-360 m.<br />
Alvania cimicoides (Hoenselaar & Goud,<br />
1998)<br />
(Figures 152-153)<br />
Remarks: Rare. Depth range, this study: 99-<br />
360 m. Collected alive at 117-234.<br />
Alvania cf. cimicoides (Hoenselaar & Goud,<br />
1998)<br />
(Figure 154)<br />
Remarks: Only one specimen collected. Depth<br />
range, this study: 156-360 m.<br />
Family Caeci<strong>da</strong>e Gray, 1850<br />
Caecum wayae Pizzini & Nofroni, 2001<br />
(Figures 155-156)<br />
Remarks: Common. Depth range, this study:<br />
57-171 m.<br />
Superfamily VANIKOROIDEA Gray, 1840<br />
Family Vanikori<strong>da</strong>e Gray, 1840<br />
Talassia cf. tenuisculpta (Watson, 1873)<br />
(Figures 157-158)<br />
Remarks: Rare. Depth range, this study: 99-234 m.<br />
Superfamily CAPULOIDEA Fleming, 1822<br />
Family Capuli<strong>da</strong>e Fleming, 1822<br />
Capulus ungaricus (Linnaeus, 1758)<br />
(Figure 159)<br />
Remarks: Rare. Depth range: sublittoral to 850<br />
m (P&G). Depth range, this study: 117-189 m.<br />
Superfamily VELUTINOIDEA Gray, 1850<br />
Family Velutini<strong>da</strong>e Gray, 1850<br />
Lamellaria perspicua (Linnaeus, 1758)<br />
(Figures 160-161)<br />
Remarks: Uncommon. Depth range: littoral to<br />
200 m (P&G; MM&B.) Depth range, this study:<br />
58-135 m. Collected alive at about 20 m, in previous<br />
workshop.<br />
Family Trivii<strong>da</strong>e Troschel, 1863<br />
Trivia pulex (Solander in J.E. Gray, 1828)<br />
(Figures 162-164)<br />
Remarks: Common. Depth range, this study:<br />
30-234 m. Ávila et al., 2000. Collected alive at<br />
about 20 m, during previous workshop.<br />
Trivia candidula (Gaskoin, 1835)<br />
(Figure 165)<br />
Remarks: Common; some specimens appeared<br />
fresh. Interti<strong>da</strong>l (MM&B). Ávila et al., 2000.<br />
Depth range, this study: 12-360 m.
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 63<br />
Erato sp.<br />
(Figures 166-167)<br />
Remarks: Rare; the specimens herein represented<br />
are tentatively identified as juveniles.<br />
Depth range, this study: 135-207 m<br />
Family Ovuli<strong>da</strong>e Feming, 1822<br />
Aperiovula juanjosensii Perez & Gomez, 1987<br />
(Figure 168)<br />
Remarks: Only a fragment was collected.<br />
Depth range, this study: 129-207 m.<br />
Superfamily NATICOIDEA Guilding, 1834<br />
Family Natici<strong>da</strong>e Guilding, 1834<br />
Notocochlis dillwynii (Payraudeau, 1826)<br />
(Figure 169)<br />
Remarks: Rare. Depth range: 1-25 m (MM&B;<br />
P&G); this study: 318 m<br />
Natica prietoi Hi<strong>da</strong>lgo, 1873<br />
(Figures 170-172)<br />
Remarks: Common, variable. Previously cited<br />
as Natica a<strong>da</strong>nsoni de Blainville, 1825 (Ávila et<br />
al., 2000). Depth range: infralittoral to 200 m<br />
(MM&B); this study: 14-360 m; alive: 18-<br />
318 m.<br />
Natica cf. prietoi Hi<strong>da</strong>lgo, 1873<br />
(Figure 173)<br />
Remarks: Rare. Depth range, this study: 32 m.<br />
Superfamily TONNOIDEA Suter, 1913<br />
Family Tonni<strong>da</strong>e Suter, 1913<br />
Phalium undulatum (Gmelin, 1791)<br />
Remarks: Only fragments. Depth range: 8-80<br />
m (P&G); infralittoral to 115 m (MM&B); this<br />
study: 32-207 m.<br />
Superfamily PTEROTRACHEOIDEA<br />
Rafinesque, 1814<br />
Family Atlanti<strong>da</strong>e Rang, 1829<br />
Atlanta peroni Lesueur, 1817<br />
(Figure 174)<br />
Remarks: Pelagic.<br />
Protatlanta souleyeti (E.A. Smith, 1888)<br />
(Figure 175)<br />
Remarks: Pelagic.<br />
Superfamily MURICOIDEA Rafinesque, 1815<br />
Family Murici<strong>da</strong>e Rafinesque, 1815<br />
Ocenebra erinaceus (Linnaeus, 1758)<br />
(Figure 176)<br />
Remarks: Rare. Only juveniles collected. Depth<br />
range: interti<strong>da</strong>l to150 m (P&G); this study: 32-<br />
207 m.<br />
Ocenebra sp.<br />
(Figure 177)<br />
Remarks: Uncommon. Depth range, this study:<br />
58-189 m.<br />
Ocinebrina aciculata (Lamarck, 1822)<br />
(Figure 178)<br />
Remarks: Relatively common. Ávila et al., 2000.<br />
Depth range: interti<strong>da</strong>l to at least 25 m (P&G); this<br />
study: 30-360 m.<br />
Ocinebrina cf. aciculata (Lamarck, 1822)<br />
(Figure 179)<br />
Remarks: Relatively common. Depth range, this<br />
study: 38-360 m.<br />
?Ocinebrina cf. aciculata (Lamarck, 1822)<br />
(Figures 180-181)<br />
Remarks: Uncommon. Depth range, this study:<br />
45-207 m.<br />
?Ocinebrina sp.<br />
(Figure 182)<br />
Remarks: Rare. Depth range, this study: 45-47 m.<br />
Orania fusulus (Brocchi, 1814)<br />
(Figures 183-185)<br />
Remarks: Depth range: 95-920 m (MM&B); 100-<br />
150 m (P&G); this study: 30-360 m; alive: 30-57 m.<br />
Trophonopsis barvicensis (Johnston, 1825)<br />
(Figures 186-192)<br />
Remarks: Commonly found. Depth range: 440-550<br />
m (MM&B); this study: 32-207 m.<br />
Trophonopsis cf. muricatus (Montagu, 1803)<br />
(Figures 193-194)<br />
Remarks: Commonly found. Ávila et al., 2000.<br />
Depth range: 10-200 m, with records down to<br />
2000 m (MM&B; P&G); this study: 41-108 m.<br />
Coralliophila cf. meyendorfii (Calcara, 1845)<br />
(Figure 195)<br />
Remarks: Uncommon. Depth range: infralittoral<br />
to circalittoral (MM&B); this study: 30-189 m.<br />
Coralliophila panormitana (Monterosato, 1896)<br />
(Figure 196)<br />
Remarks: Rare. Depth range: below low tide to<br />
640m (P&G); this study: 99-234 m.
64 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
Stramonita haemastoma (Linnaeus, 1767)<br />
(Figure 197)<br />
Remarks: Uncommon; specimens rolled, mostly<br />
juvenile, probably transported from the littoral.<br />
Knudsen, 1995 as Thais haemastoma flori<strong>da</strong>na<br />
(Conrad, 1837); Ávila et al., 2000. Depth range:<br />
interti<strong>da</strong>l to 3 m (P&G); this study: 32-360 m.<br />
Alive on IVFC (Martins, 2004).<br />
Family Cystici<strong>da</strong>e Stimpson, 1865<br />
Gibberula vignali (Dautzenberg & Fischer 1896)<br />
(Figure 198)<br />
Remarks: Rare. Depth range, this study: 156-360m.<br />
Gibberula cf. lazaroi Contreras, 1992<br />
(Figure 199)<br />
Remarks: Rare. Could be a juvenile of G. vignali,<br />
but resembles Gibberula lazaroi, described from the<br />
interti<strong>da</strong>l of Pico and Terceira islands (Contreras,<br />
1992). Depth range, this study: 117-234 m.<br />
Family Mitri<strong>da</strong>e Swainson, 1831<br />
Mitra cornea Lamarck, 1811<br />
(Figure 200)<br />
Remarks: Uncommon; specimens rolled, mostly<br />
juveniles. Knudsen, 1995 as M. nigra (Gmelin,<br />
1791); Ávila et al., 2000. Depth range: interti<strong>da</strong>l<br />
to 40 m (MM&B, as M. cornicula (Linnaeus);<br />
this study: 30-207 m; alive at IVFC (Martins,<br />
2004).<br />
Superfamily BUCCINOIDEA Rafinesque, 1815<br />
Family Buccini<strong>da</strong>e Rafinesque, 1815<br />
Pollia dorbignyi (Payraudeau, 1826)<br />
(Figures 201-202)<br />
Remarks: one fresh fragment. Depth range: in and<br />
just above littoral zone (MM&B; P&G); this study:<br />
30 m; alive at IVFC (Martins, 2004).<br />
Family Nassarii<strong>da</strong>e Ire<strong>da</strong>le, 1916<br />
Nassarius incrassatus (Ström, 1768)<br />
(Figures 203-206)<br />
Remarks: Common, mostly fragmented shells.<br />
Ávila et al., 2000. Depth range: interti<strong>da</strong>l to 200 m<br />
(MM&B; P&G); this study: 18-.360 m.<br />
Nassarius cf. cuvierii (Payraudeau, 1826)<br />
(Figure 207)<br />
Remarks: One juvenile specimen collected.<br />
Depth range: in and just above littoral zone<br />
(MM&B; P&G); this study: 66 m.<br />
Nassarius recidivus (Martens, 1876)<br />
(Figure 208)<br />
Remarks: Rare. Depth range, this study: 167-318 m.<br />
Family Columbelli<strong>da</strong>e Swainson, 1840<br />
Columbella a<strong>da</strong>nsoni Menke, 1853<br />
(Figure 209)<br />
Remarks: Uncommon, mostly fragmented shells;<br />
some juveniles appeared fresh. Knudsen, 1995;<br />
Ávila et al., 2000. Depth range: 4-1402 m (MM&B,<br />
as C. rustica (Linnaeus)); this study: 30-360 m;<br />
common alive at IVFC (Martins, 2004).<br />
Mitrella pallaryi (Dautzenberg, 1758)<br />
(Figure 210)<br />
Remarks: Rare. Depth range: 40-200 m (MM&B;<br />
P&G); this study: 129-360 m.<br />
Anachis avaroides Nordsieck, 1975<br />
(Figures 211-212)<br />
Remarks: Common. Ávila et al., 2000. Depth<br />
range: infralittoral (MM&B), this study: 30-207 m;<br />
common alive at IVFC (Martins, 2004).<br />
Superfamily CANCELLARIOIDEA Forbes &<br />
Hanley, 1851<br />
Family Cancellarii<strong>da</strong>e Forbes & Hanley, 1851<br />
Brocchinia clenchi Petit, 1986<br />
(Figures 213-214)<br />
Remarks: Frequent in some samples. Depth range,<br />
this study: 40-07 m; alive: 58-81 m.<br />
Superfamily CONOIDEA Fleming, 1822<br />
Family Coni<strong>da</strong>e Fleming, 1822<br />
Mitromorpha (Mitrolumna) azorensis Mifsud, 2001<br />
(Figures 215-216)<br />
Remarks: Uncommon. Bullock, 1995 as Mitrolumna<br />
olivoidea (Cantraine, 1835); Ávila et al., 2000.<br />
Depth range, this study: 30-207 m<br />
Bela nebula (Montagu, 1803)<br />
(Figures 217-222)<br />
Remarks: Common throughout the sampled depth<br />
range. Ávila et al., 2000. Depth range: 10-30 m<br />
(P&B); this study: 14-360 m; alive: 38-169 m.<br />
Mangelia cf. costata (Montagu, 1803)<br />
(Figures 223-229)<br />
Remarks: Common. Depth range: infralittoral<br />
40 m (MM&B); this study: 14-360 m; alive: 66-<br />
189 m.
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 65<br />
Raphitoma purpurea (Montagu, 1803)<br />
(Figure 230)<br />
Remarks: Uncommon. Depth range, this study:<br />
30-207 m<br />
Raphitoma linearis (Montagu, 1803)<br />
(Figure 231)<br />
Remarks: Uncommon. Depth range: Interti<strong>da</strong>l to<br />
200 m (P&G); this study: 38-234 m.<br />
Raphitoma cf. aequalis (Jeffreys, 1867)<br />
(Figures 232-240)<br />
Remarks: Common. Depth range: interti<strong>da</strong>l<br />
(MM&B); this study: 14-360 m; alive: 46-58 m.<br />
Raphitoma sp.<br />
(Figure 241)<br />
Remarks: Rare. Depth range, this study: 32-207 m.<br />
Pleurotomella gibbera Bouchet & Warén, 1980<br />
(Figures 242-244)<br />
Remarks: Rare. Depth range, this study: 72- 234 m.<br />
Pleurotomella cf. gibbera Bouchet & Warén, 1980<br />
(Figure 245)<br />
Remarks: Rare. Depth range, this study: 144-198m.<br />
Teretia teres (Reeve, 1844)<br />
(Figures 246-247)<br />
Remarks: Rare. Depth range: 30-1385 (MM&B);<br />
this study: 99-234 m.<br />
Family Drillii<strong>da</strong>e Olsson, 1964<br />
Crassopleura maravignae (Bivona, 1838)<br />
(Figures 248-250)<br />
Remarks: Common at deeper sandy bottoms.<br />
Ávila et al., 2000. Depth range, this study: 14-360<br />
m; alive at: 58-234 m.<br />
Family Turri<strong>da</strong>e H. & A. A<strong>da</strong>ms, 1853<br />
Haedropleura septangularis (Montagu, 1803)<br />
(Figures 251-252)<br />
Remarks: Uncommon. Ávila et al., 2000. Depth<br />
range: 7-70 m (P&G); this study: 30-207 m<br />
Subclass HETEROBRANCHIA Gray, 1840<br />
Order HETEROSTROPHA Fischer P., 1885<br />
Superfamily ARCHITECTONICOIDEA Gray,<br />
1850<br />
Family Architectonici<strong>da</strong>e Gray, 1850<br />
Philippia krebsi (Mörch, 1875)<br />
(Figure 253)<br />
Remarks: Rare. Depth range, this study: 56-207 m.<br />
Pseudotorinia architae (Costa O.G., 1841)<br />
(Figure 254)<br />
Remarks: Rare. Ávila et al., 2000. Depth range,<br />
this study: 180-234 m; alive at: 180m.<br />
Pseudomalaxis zancleus (Philippi, 1844)<br />
(Figure 255)<br />
Remarks: Rare. Depth range: 644 m (MM&B);<br />
this study: 117-234 m.<br />
Superfamily MATHILDOIDEA Dall, 1889<br />
Family Mathildi<strong>da</strong>e Semper, 1865<br />
Mathil<strong>da</strong> cochlaeformis Brugnone, 1873<br />
(Figure 256)<br />
Remarks: Rare; only one fresh, broken shell. Depth<br />
range: 1205 m (MM&B); this study: 144-198 m.<br />
Mathil<strong>da</strong> retusa (Brocchi, 1814)<br />
(Figure 257)<br />
Remarks: Rare; only one specimen collected.<br />
Depth range, this study: 117-234 m.<br />
Superfamily RISSOELLOIDEA Gray, 1850<br />
Family Rissoelli<strong>da</strong>e Gray, 1850<br />
?Rissoella sp. 1<br />
(Figure 258)<br />
Remarks: Rare. Depth range, this study: 156-360m.<br />
? Rissoella sp. 2<br />
(Figure 259)<br />
Remarks: Rare. Depth range, this study: 135 m.<br />
Superfamily OMALOGYROIDEA Sars, 1878<br />
Family Omalogyri<strong>da</strong>e Sars, 1878<br />
Omalogyra atomus (Philippi, 1841)<br />
(Figure 260)<br />
Remarks: Rare; only one specimen; however,<br />
the rarity of minute species can be seen as an<br />
artefact of sampling, for most of the fine fraction<br />
was discarded. Bullock et al. (1990) reported<br />
it to be very common on algal samples.<br />
Bullock, 1995; Knudsen, 1995; Ávila et al., 2000.<br />
Depth range: interti<strong>da</strong>l to 20 m (MM&B); this<br />
study: 117-145 m.<br />
Superfamily PYRAMIDELLOIDEA Gray, 1840<br />
Family Pyramidelli<strong>da</strong>e Gray, 1840<br />
O<strong>dos</strong>tomella doliolum (Philippi, 1844)<br />
(Figures 261-262)<br />
Remarks: Rare; one very fresh shell collected.<br />
Ávila et al., 2000. Depth range: 10-800 m<br />
(MM&B); this study: 180-234 m.
66 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
Chrysalli<strong>da</strong> cf. flexuosa (Monterosato, 1874 ex<br />
Jeffreys)<br />
(Figure 263)<br />
Remarks: Rare. Depth range, this study: 156-<br />
300 m.<br />
O<strong>dos</strong>tomia bernardi Aartsen, Gittenberger &<br />
Goud, 1998<br />
(Figure 264)<br />
Remarks: Common in fine fractions. Endemic.<br />
Depth range, this study: 30-360m.<br />
O<strong>dos</strong>tomia cf. verhoeveni Aartsen, Gittenberger<br />
& Goud, 1998<br />
(Figure 265)<br />
Remarks: Uncommon. Depth range, this study:<br />
30-207 m.<br />
O<strong>dos</strong>tomia duureni Aartsen, Gittenberger &<br />
Goud, 1998<br />
(Figure 266)<br />
Remarks: Rare. Depth range, this study: 57 m.<br />
O<strong>dos</strong>tomia cf. striolata Forbes & Hanley, 1850<br />
(Figure 267)<br />
Remarks: Rare. Depth range, this study: 72-<br />
234 m.<br />
Eulimella sp.<br />
(Figure 268)<br />
Remarks: Rare. Depth range, this study: 129-<br />
207 m.<br />
Turbonilla rufa (Philippi, 1836)<br />
(Figure 269)<br />
Remarks: Rare. Depth range, this study: 57-<br />
234 m.<br />
Turbonilla lactea (Linnaeus, 1758)<br />
(Figure 270)<br />
Remarks: Regularly present. Ávila, 2000.<br />
Depth range: Infralittoral to 80 m (MM&B); this<br />
study: 30-207 m.<br />
Turbonilla sp. 1<br />
(Figure 271)<br />
Remarks: Rare. Depth range, this study: 129-207 m.<br />
Turbonilla sp. 2<br />
(Figure 272)<br />
Remarks: Rare. Depth range, this study: 144-<br />
234 m.<br />
Turbonilla sp. 3<br />
(Figure 273)<br />
Remarks: Rare. Depth range, this study: 129-<br />
207 m.<br />
Turbonilla sp. 4<br />
(Figure 274)<br />
Remarks: Rare. Depth range, this study: 129-<br />
207 m.<br />
Family Murchisonelli<strong>da</strong>e Casey, 1905<br />
Ebala nitidissima (Montagu, 1803)<br />
(Figures 275-276)<br />
Remarks: Uncommon. Depth range, this<br />
study: 57-145 m.<br />
Subclass OPISTHOBRANCHIA Milne-<br />
Edwards, 1848<br />
Order CEPHALASPIDEA Fischer P., 1883<br />
Family Diaphani<strong>da</strong>e Odhner, 1914<br />
Colpo<strong>da</strong>spis pusilla Sars, 1870<br />
(Figure 277)<br />
Remarks: Rare. Depth range, this study: 135-<br />
189 m.<br />
Family Retusi<strong>da</strong>e Thiele, 1925<br />
Retusa truncatula (Bruguière, 1792)<br />
(Figures 278-279)<br />
Remarks: Common. Mikkelsen, 1995. Depth<br />
range: below low tide to 200 m (P&G); this<br />
study: 38-145 m.<br />
Family Haminoei<strong>da</strong>e Pilsbry, 1895<br />
Haminoea cf. orteai Talavera, Murillo &<br />
Templado, 1987<br />
(Figure 280)<br />
Remarks: Uncommon. Mikkelsen, 1995.<br />
Depth range, this study: 32-145 m.<br />
Atys macandrewi E.A. Smith, 1872<br />
(Figure 281)<br />
Remarks: Uncommon. Mikkelsen, 1995.<br />
Depth range, this study: 58-145 m.<br />
Atys sp.<br />
(Figure 282)<br />
Remarks: Rare. Depth range, this study: 46-47 m.<br />
Family Philini<strong>da</strong>e Gray, 1850<br />
Philine approximans Dautzenberg & Fisher, 1896<br />
(Figure 283)<br />
Remarks: Rare. Depth range, this study: 86-234 m.
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 67<br />
Philine sp.<br />
(Figure 284)<br />
Remarks: Rare. Depth range, this study: 72 m.<br />
Family Aglaji<strong>da</strong>e Pilsbry, 1895<br />
?Chelidonura africana Pruvot-Fol, 1953<br />
(Figure 285)<br />
Remarks: Rare. Depth range, this study: 117-<br />
234 m.<br />
Order THECOSOMATA de Blainville, 1824<br />
Family Cavolinii<strong>da</strong>e Gray, 1850<br />
Cavolinia inflexa (Lesueur, 1813)<br />
(Figures 286-287)<br />
Remarks: Common; it is a pelagic species.<br />
Cavolinia tridentata (Forskal, 1775)<br />
(Figure 288)<br />
Remarks: Common; it is a pelagic species.<br />
Diacria trispinosa (Lesueur, 1821)<br />
(Figures 289-290)<br />
Remarks: Rare; it is a pelagic species.<br />
Cuvierina atlantica (Bé, MacClintock & Currie,<br />
1972)<br />
(Figure 291)<br />
Remarks: Rare; it is a pelagic species.<br />
Clio pyrami<strong>da</strong>ta (Lesueur, 1821)<br />
(Figures 292-293)<br />
Remarks: Rare; it is a pelagic species.<br />
Family Limacini<strong>da</strong>e Gray, 1840<br />
Limacina cf. helicina (Phipps, 1774)<br />
(Figure 294)<br />
Remarks: Rare. Limacina helicina is a boreal,<br />
pelagic species; the specimens of the Azores,<br />
however, resemble those reported to this<br />
species elsewhere (Rolán, 2005).<br />
Limacina inflata (d’Orbigny, 1836)<br />
(Figure 295)<br />
Remarks: Rare; it is a pelagic species.<br />
Order NOTASPIDEA Fischer P., 1883<br />
Family Umbraculi<strong>da</strong>e Dall, 1889<br />
Umbraculum umbraculum (Lightfoot, 1786)<br />
(Figure 296)<br />
Remarks: Uncommon. Depth range, this study:<br />
52-198 m.<br />
Family Tylodini<strong>da</strong>e Gray, 1847<br />
Tylodina perversa (Gmelin, 1791)<br />
(Figure 297)<br />
Remarks: Rare. Depth range, this study: 117-<br />
145 m.<br />
Subclass PULMONATA Cuvier, 1817<br />
Superfamily SIPHONARIOIDEA Gray, 1827<br />
Family Siphonarii<strong>da</strong>e Gray, 1827<br />
Williamia gussonii (O.G. Costa, 1829)<br />
(Figure 298)<br />
Remarks: Uncommon. Ávila et al., 2000. Depth<br />
range, this study: 40-180 m.<br />
Order ARCHAEOPULMONATA<br />
Superfamily ELLOBIOIDEA Pfeiffer, 1854<br />
Family Ellobii<strong>da</strong>e Pfeiffer, 1854<br />
Ovatella vulcani (Morelet, 1860)<br />
Remarks: Only one shell; this is a suprati<strong>da</strong>l<br />
pulmonate.<br />
Pedipes pedipes Bruguière, 1789<br />
Remarks: Only one shell; this is a suprati<strong>da</strong>l<br />
pulmonate.<br />
Class BIVALVIA Linnaeus, 1758<br />
Order PTEROMORPHIA Beurlen, 1944<br />
Superfamily ARCOIDA Stoliczka, 1871<br />
Family Arci<strong>da</strong>e Lamarck, 1809<br />
Arca tetragona Poli, 1795<br />
(Figure 299)<br />
Remarks: Common. This species lives on hard<br />
substrates. Bullock, 1995; Ávila et al., 2000.<br />
Depth range: interti<strong>da</strong>l to 900 m (MM&B); low<br />
tide to 120 m (P&G); this study: 30-360 m.<br />
Asperarca nodulosa (O.F. Müller, 1776)<br />
(Figure 300)<br />
Remarks: Rare. Depth range: low tide to 1000 m<br />
(P&G); interti<strong>da</strong>l to 3300 m (MM&B); this<br />
study: 117-234 m.<br />
Family Noetii<strong>da</strong>e Stewart, 1930<br />
Bathyarca philippiana (Nyst, 1848)<br />
(Figures 301-302)<br />
Remarks: Rare. Depth range: around 150 m (P&G);<br />
60-1200 m (MM&B); this study: 117- 360 m.<br />
Family Limopsi<strong>da</strong>e Dall, 1895<br />
Limopsis minuta Philippi, 1836<br />
(Figure 303)<br />
Remarks: Rare. Depth range: 40-1400m
68 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XVIII<br />
299. Arca tetragona Poli, 1795. Loose valves (Sta8)<br />
300. Asperarca nodulosa (O.F. Müller, 1776). Loose valves (Sta37)<br />
301. Bathyarca philippiana (Nyst, 1848) (Sta41)<br />
302. Bathyarca philippiana (Nyst, 1848) (juvenile) (Sta37)<br />
303. Limopsis minuta Philippi, 1836 (Sta1)<br />
304. Gregariella semigranata (Reeve, 1858) (Sta28)<br />
305. Rhomboidella prideauxi (Leach, 1815) (Sta13)<br />
306. Pecten jacobeus (Linnaeus, 1758) (Sta26)<br />
307. Pecten jacobeus (Linnaeus, 1758) (juvenile) (Sta18)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 69
70 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XIX<br />
308. Aequipecten commutatus (Monterosato, 1875) (Sta29)<br />
309. Aequipecten commutatus (Monterosato, 1875) (Sta23)<br />
310. Aequipecten opercularis (Linnaeus, 1758) (Sta8)<br />
311. Aequipecten opercularis (Linnaeus, 1758) (Sta5)<br />
312. Bractechlamys corallinoides (d’Orbigny, 1840) (Sta26)<br />
313. Bractechlamys corallinoides (d’Orbigny, 1840) (Sta5)<br />
314. Bractechlamys corallinoides (d’Orbigny, 1840) (Sta23)<br />
315. Palliolum incomparabile (Risso, 1826) (Sta29)<br />
316. Palliolum incomparabile (Risso, 1826) (Sta29)<br />
317. Palliolum incomparabile (Risso, 1826) (Sta7)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 71
72 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XX<br />
318. Chlamys flexuosa (Poli, 1795) (Sta7)<br />
319. Talochlamys pusio (Linnaeus, 1758) (Sta26)<br />
320. Talochlamys pusio (Linnaeus, 1758) (Sta26)<br />
321. Pododesmus patelliformis (Linnaeus, 1761) (Sta56)<br />
322. Limaria hians (Gmelin, 1791) (Sta56)<br />
323. Neopycnodonte cochlear (Poli, 1795) (Sta55)<br />
324. Myrtea spinifera (Montagu, 1803) (Sta37)<br />
325. Lucinoma borealis (Linnaeus, 1767) (Sta37)<br />
326. Lucinoma borealis (Linnaeus, 1767) (Sta37)<br />
327. Thyasira flexuosa (Montagu, 1803) (Sta7)<br />
328. Diplodonta berghi (Dautzenberg & Fischer, 1897) (Sta32)<br />
329. Diplodonta berghi (Dautzenberg & Fischer, 1897) (Sta40)<br />
330. Diplodonta berghi (Dautzenberg & Fischer, 1897) (Sta46)<br />
331. Diplodonta trigona (Scacchi, 1835) (Sta56)<br />
332. Diplodonta trigona (Scacchi, 1835) (Sta29)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 73
74 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XXI<br />
333. Chama gryphoides (Linnaeus, 1758) (Sta55)<br />
334. Chama gryphoides (Linnaeus, 1758) (Sta37)<br />
335. Kurtiella pelluci<strong>da</strong> (Jeffreys, 1881) (Sta27)<br />
336. Kurtiella pelluci<strong>da</strong> (Jeffreys, 1881) (Sta7)<br />
337. Basterotia clancula von Cosel, 1995. Loose valves (juvenile) (Sta28)<br />
338. Basterotia clancula von Cosel, 1995. Loose valves (Sta12)<br />
339. Cardita calyculata (Linnaeus, 1758) (Sta24)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 75
76 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XXII<br />
340. ?Crassatina sp. (Sta46)<br />
341. Papillicardium papillosum (Poli, 1791) (Sta47)<br />
342. Papillicardium papillosum (Poli, 1791) (Sta57)<br />
343. Papillicardium papillosum (Poli, 1791) (Sta56)<br />
344. Papillicardium papillosum (Poli, 1791) (Sta15)<br />
345. Papillicardium papillosum (Poli, 1791) (Sta5)<br />
346. Papillicardium papillosum (Poli, 1791) (Sta5)<br />
347. Parvicardium vroomi van Aartsen, Menkhorst & Gittenberger, 1984. Loose<br />
valves (Sta27)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 77
78 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XXIII<br />
348. Tellina incarnata Linnaeus, 1758 (Sta57)<br />
349. Tellina pygmaea Lovén, 1846 (Sta48)<br />
350. Tellina pygmaea Lovén, 1846 (Sta12)<br />
351. Tellina pygmaea Lovén, 1846 (Sta57)<br />
352. Tellina pygmaea Lovén, 1846 (Sta5)<br />
353. Tellina pygmaea Lovén, 1846 (Sta57)<br />
354. Arcopagia balaustina (Linnaeus, 1758) (Sta43)<br />
355. Arcopagia balaustina (Linnaeus, 1758) (Sta37)<br />
356. Arcopagia balaustina (Linnaeus, 1758) (Sta7)<br />
357. ?Tellina sp. (Sta28)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 79
80 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XXIV<br />
358. Gari costulata (Turton, 1822) (Sta15)<br />
359. Gari costulata (Turton, 1822) (Sta31)<br />
360. Ervilia castanea (Montagu, 1803) (Sta26)<br />
361. Ervilia castanea (Montagu, 1803) (Sta31)<br />
362. Azorinus chamasolen (<strong>da</strong> Costa, 1778) (juvenile) (Sta44)<br />
363. Azorinus chamasolen (<strong>da</strong> Costa, 1778) (Sta40)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 81
82 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XXV<br />
364. Coralliophaga lithophagella (Lamarck, 1819) (Sta37)<br />
365. Coralliophaga lithophagella (Lamarck, 1819) (Sta37)<br />
366. Coralliophaga lithophagella (Lamarck, 1819) (juvenile) (Sta53)<br />
367. Coralliophaga lithophagella (Lamarck, 1819) (juvenile) (Sta37)<br />
368. Venus casina Linnaeus, 1758 (Sta54)<br />
369. Venus verrucosa Linnaeus, 1758 (Sta1)<br />
370. Venus verrucosa Linnaeus, 1758 (Sta26)<br />
371. Globivenus effossa (Philippi, 1836) (Sta41)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 83
84 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XXVI<br />
372. <strong>Timoclea</strong> <strong>ovata</strong> (Pennant, 1777) (Sta48)<br />
373. <strong>Timoclea</strong> <strong>ovata</strong> (Pennant, 1777) (Sta56)<br />
374. <strong>Timoclea</strong> <strong>ovata</strong> (Pennant, 1777) (Sta15)<br />
375. Gouldia minima (Montagu, 1803) (Sta5)<br />
376. Gouldia minima (Montagu, 1803) (Sta56)<br />
377. Gouldia minima (Montagu, 1803) (Sta15)<br />
378. Gouldia minima (Montagu, 1803) (Sta15)<br />
379. Gouldia minima (Montagu, 1803) (Sta27)<br />
380. Callista chione (Linnaeus, 1758) (Sta40)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 85
86 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
PLATE XXVII<br />
381. Hiatella arctica (Linnaeus, 1767) (Sta32)<br />
382. Hiatella arctica (Linnaeus, 1767) (Sta18)<br />
383. Gastrochaena dubia (Pennant, 1777) (Sta32)<br />
384. Nototeredo norvagica (Spengler, 1792) (Sta12)<br />
385. Teredora malleolus (Turton, 1822) (Sta1)<br />
386. Xyloredo sp. (Sta56)<br />
387. Xyloredo sp. (Sta56)<br />
388. Thracia papyracea (Poli, 1791) (Sta13)<br />
389. Cardiomya costellata (Deshayes, 1835) (Sta23)<br />
390. Cuspi<strong>da</strong>ria atlantica Allen & Morgan, 1981 (Sta38)
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 87
88 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
(MM&B); continental shelves down to 900 m<br />
(P&G); this study: 57 m.<br />
Superfamily MYTILOIDA de Férussac, 1822<br />
Family Mytili<strong>da</strong>e Rafinesque, 1815<br />
Gregariella semigranata (Reeve, 1858)<br />
(Figure 304)<br />
Remarks: Common. Morton, 1995 as Trichomusculus<br />
semigranatus. This species lives on<br />
hard substrata. Depth range, this study: 30-<br />
360m; alive: 66 m.<br />
Rhomboidella prideauxi (Leach, 1815)<br />
(Figure 305)<br />
Remarks: Rare. Depth range, this study: 73-<br />
180 m.<br />
Superfamily PTERIOIDA Newell, 1965<br />
Family Pectini<strong>da</strong>e Rafinesque, 1815<br />
Pecten jacobeus (Linnaeus, 1758)<br />
(Figures 306-307)<br />
Remarks: Uncommon. Depth range: 25-250 m<br />
(P&G); this study: 40-360 m; alive: 72 m.<br />
Aequipecten commutatus (Monterosato, 1875)<br />
(Figures 308-309)<br />
Remarks: Uncommon. Ávila et al., 2000. Depth<br />
range: 30-250 m; this study: 40-360 m; alive:<br />
180 m.<br />
Aequipecten opercularis (Linnaeus, 1758)<br />
(Figures 310-311)<br />
Remarks: Common. Ávila et al., 2000. Depth<br />
range: low tide to 400 m (P&G; MM&B); this<br />
study: 38-360 m; alive: 41-171 m.<br />
Bractechlamys corallinoides (d’Orbigny, 1840<br />
(Figures 312-314)<br />
Remarks: Common. Depth range: 3-100 m<br />
(P&G); this study: 38-360 m.<br />
Palliolum incomparbile (Risso, 1826)<br />
(Figures 315-317)<br />
Remarks: Common. Ávila et al., 2000. Depth<br />
range: 10-250 m (P&G); infralittoral to 2000 m<br />
(MM&B); this study: 30-360 m.<br />
Chlamys flexuosa (Poli, 1795)<br />
(Figure 318)<br />
Remarks: Very rare. Ávila et al., 2000. Depth<br />
range: 30-250 m (P&G); this study: 45-189 m.<br />
Talochlamys pusio (Linnaeus, 1758)<br />
(Figures 319-320)<br />
Remarks: Common. Ávila et al., 2000 as<br />
Crassadoma pusio. Depth range: from a few<br />
meters to 150 m (P&G, as Hinnites distortus<br />
(<strong>da</strong> Costa, 1778)); 100-2300 (MM&B, as Chlamys<br />
distorta (<strong>da</strong> Costa, 1778)); this study: 30-<br />
360 m. Collected alive at IVFC (Martins,<br />
2004).<br />
Family Anomii<strong>da</strong>e Rafinesque, 1815<br />
Pododesmus patelliformis (Linnaeus, 1761)<br />
(Figure 321)<br />
Remarks: Common. Depth range: interti<strong>da</strong>l to<br />
50 m (P&G); interti<strong>da</strong>l to 450 m (MM&B); this<br />
study: 14-360 m.<br />
Family Limi<strong>da</strong>e Rafinesque, 1815<br />
Limaria hians (Gmelin, 1791)<br />
(Figure 322)<br />
Remarks: Common. Ávila et al., 2000. Depth<br />
range: low tide to 100 m (P&G); low tide to 450<br />
m (MM&B); this study: 30-360 m. Collected<br />
alive at IVFC (Martins, 2004).<br />
Superfamily OSTREOIDA de Férussac, 1822<br />
Family Gryphaei<strong>da</strong>e Vyalov, 1936<br />
Neopycnodonte cochlear (Poli, 1795)<br />
(Figure 323)<br />
Remarks: Common. Ávila et al., 2000. Depth<br />
range: 45-250 m (P&G); this study: 41-360 m;<br />
alive: 66-162 m.<br />
Order HETERODONTA Neumayr, 1884<br />
Superfamily VENEROIDA H. & A. A<strong>da</strong>ms,<br />
1857<br />
Family Lucini<strong>da</strong>e Fleming, 1828<br />
Myrtea spinifera (Montagu, 1803)<br />
(Figure 324)<br />
Remarks: Rare. Depth range: 7-250 m (P&G);<br />
this study: 117-234 m.<br />
Lucinoma borealis (Linnaeus, 1767)<br />
(Figures 325-326)<br />
Remarks: Common. Bullock, 1995. Range:<br />
interti<strong>da</strong>l to 500 m (P&G); interti<strong>da</strong>l to 1500 m<br />
(MM&B); this study: 30-360 m; alive: 95-351 m.<br />
This species was collected alive at IVFC about<br />
20 cm deep into the sandy substratum (pers.<br />
obs., AMFM).
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 89<br />
Family Thyasiri<strong>da</strong>e Dall, 1900<br />
Thyasira flexuosa (Montagu, 1803)<br />
(Figure 327)<br />
Remarks: Rare. Depth range: 10-2000 m (P&G);<br />
infralittoral to 2190 m (MM&B); this study:<br />
135-360 m.<br />
Family Ungulini<strong>da</strong>e A<strong>da</strong>ms, H. & A., 1857<br />
Diplodonta berghi (Dautzenberg & Fischer,<br />
1897)<br />
(Figures 328-330)<br />
Remarks: Uncommon. Depth range: 130-1360<br />
m (MM&B); this study: 38-234 m.<br />
Diplodonta trigona (Sacchi, 1835)<br />
(Figures 331-332)<br />
Remarks: Common. Depth range, this study:<br />
30-360 m; alive: 30-198 m.<br />
Family Chami<strong>da</strong>e Lamarck, 1809<br />
Chama gryphoides (Linnaeus, 1758)<br />
(Figures 333-334)<br />
Remarks: Common. Depth range: interti<strong>da</strong>l to<br />
200 m (P&G; MM&B); this study: 41-360 m;<br />
alive: 162-234 m.<br />
Family Montacuti<strong>da</strong>e Clark, 1855<br />
Kurtiella pelluci<strong>da</strong> (Jeffreys, 1881)<br />
(Figures 335-336)<br />
Remarks: Uncommon. Depth range, this study:<br />
40-360 m; alive: 99-207 m.<br />
Family Sportelli<strong>da</strong>e Dall, 1899<br />
Basterotia clancula von Cosel, 1995<br />
(Figures 337-338)<br />
Remarks: Common. Depth range, this study:<br />
18-360 m.<br />
Family Carditi<strong>da</strong>e Fleming, 1828<br />
Cardita calyculata (Linnaeus, 1758)<br />
(Figure 339)<br />
Remarks: Common. Bullock, 1995; Ávila et al.,<br />
2000. Depth range: low tide to 200 m (MM&B;<br />
P&G); this study: 30-360 m; alive: 38-117 m.<br />
Alive at IVFC (Martins, 2004).<br />
Family Crassatelli<strong>da</strong>e Férussac, 1822<br />
?Crassatina sp.<br />
(Figure 340)<br />
Remarks: Rare. One valve, tentatively assigned<br />
to this genus. Depth range, this study:<br />
56 m.<br />
Family Cardii<strong>da</strong>e Lamarck, 1809<br />
Papillicardium papillosum (Poli, 1791)<br />
(Figures 341-346)<br />
Remarks: Very common. Ávila et al., 2000.<br />
Depth range: infralittoral to 60 m (MM&B); this<br />
study: 45-360 m; alive: 45-318 m.<br />
Parvicardium vroomi van Aartsen, Menkhorst &<br />
Gittenberger, 1984<br />
(Figure 347)<br />
Remarks: Common. Ávila et al., 2000. Depth<br />
range, this study: 46-360 m.<br />
Family Tellini<strong>da</strong>e de Blainville, 1814<br />
Tellina incarnata Linnaeus, 1758<br />
(Figure 348)<br />
Remarks: Common. Ávila et al., 2000. Depth<br />
range: interti<strong>da</strong>l to 85 m (MM&B; P&G);<br />
this study: 18-360 m; alive: 18-72 m. This<br />
species was taken alive at IVFC about 20 cm<br />
deep into the sandy substrata (pers. obs.,<br />
AMFM).<br />
Tellina pygmaea Lovén, 1846<br />
(Figures 349-353)<br />
Remarks: Very common. Depth range: interti<strong>da</strong>l<br />
to 150 m; this study: 18-360 m. Collected<br />
alive throughout its range. Authors report T.<br />
donacina Linnaeus, 1758 as living in the Azores<br />
(Ávila et al., 2000); however, all the specimens<br />
herein collected conform to the representation<br />
of T. pygmaea instead.<br />
Arcopagia balaustina Linnaeus, 1758<br />
(Figures 354-355)<br />
Remarks: Common. Depth range: infralittoral<br />
to 750 m (MM&B; P&G); this study: 46-360 m;<br />
alive: 66-360 m.<br />
? Tellina sp.<br />
(Figure 356)<br />
Remarks: Rare; only one valve, tentatively<br />
assigned to this genus. Depth range, this<br />
study: 117-145.<br />
Family Psammobii<strong>da</strong>e Fleming, 1828<br />
Gari costulata (Turton, 1822)<br />
(Figures 357-359)<br />
Remarks: Common. Ávila et al., 2000. Depth<br />
range: infralittoral to 150 m, most abun<strong>da</strong>nt 35-<br />
60 m (MM&B; P&G); this study: 18-360 m;<br />
alive: 18-66 m.
90 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
Family Semeli<strong>da</strong>e Stoliczka, 1870 (1850)<br />
Ervilia castanea (Montagu, 1803)<br />
(Figures 360-361)<br />
Remarks: The commonest bivalve in the Azores<br />
(Morton, 1990). Bullock, 1995; Ávila et al., 2000.<br />
Depth range: 30-100 m (P&G); interti<strong>da</strong>l to<br />
1800 m (MM&B); this study: 18-360 m; collected<br />
alive throughout its range. Alive at IVFC<br />
(Martins, 2004).<br />
Family Solecurti<strong>da</strong>e d’Orbigny, 1846<br />
Azorinus chamasolen (<strong>da</strong> Costa, 1778)<br />
(Figures 362-363)<br />
Remarks: Rare. Depth range, this study: 38-66<br />
m; alive: 66 m.<br />
Family Trapezi<strong>da</strong>e d’Orbigny, 1846<br />
Coralliophaga lithophagella (Lamarck, 1819)<br />
(Figures 364-367)<br />
Remarks: Uncommon. Depth range: 33-200 m<br />
(MM&B; P&G); this study: 57-360 m; alive: 162-<br />
234 m.<br />
Family Veneri<strong>da</strong>e Rafinesque, 1815<br />
Venus casina Linnaeus, 1758<br />
(Figure 368)<br />
Remarks: Common. Ávila et al., 2000. Depth<br />
range: 5-200 m (P&G); this study: 32-360 m;<br />
alive: 32-180 m.<br />
Venus verrucosa Linnaeus, 1758<br />
(Figures 369-370)<br />
Remarks: Uncommon. Depth range: interti<strong>da</strong>l<br />
to 100 m (MM&B; P&G); this study: 46-360;<br />
alive: 32-66 m.<br />
Globivenus effossa (Philippi, 1836)<br />
(Figure 371)<br />
Remarks: Rare. Ávila et al., 2000. Depth range:<br />
50-300 m (P&G); this study: 156-360; taken<br />
alive throughout the range.<br />
<strong>Timoclea</strong> <strong>ovata</strong> (Pennant, 1777)<br />
(Figures 372-374)<br />
Remarks: Very common. Ávila et al., 2000.<br />
Depth range: 4-200 m (P&G); this study: 46-360<br />
m; alive: 30-360 m.<br />
Gouldia minima (Montagu, 1803)<br />
(Figures 375-379)<br />
Remarks: Very common. Ávila et al., 2000.<br />
Depth range: interti<strong>da</strong>l to 200 m (MM&B;<br />
P&G); this study: 18-360 m; alive: 38-<br />
360 m.<br />
Callista chione (Linnaeus, 1758)<br />
(Figure 380)<br />
Remarks: Common. Ávila et al., 2000. Depth<br />
range: interti<strong>da</strong>l to 180 m (MM&B; P&G); this<br />
study: 18-360 m; alive: 38-81 m.<br />
Superfamily MYOIDA Stoliczka, 1870<br />
Family Hiatelli<strong>da</strong>e Gray, 1824<br />
Hiatella arctica (Linnaeus, 1767)<br />
(Figures 381-382)<br />
Remarks: Uncommon; possibly young specimens<br />
of this species. Ávila et al., 2000. Depth<br />
range: interti<strong>da</strong>l to 1400 m (MM&B; P&G); this<br />
study: 72-207 m.<br />
Family Gastrochaeni<strong>da</strong>e Gray, 1840<br />
Gastrochaena dubia (Pennant, 1777)<br />
(Figure 383)<br />
Remarks: Rare; one valve tentatively assigned to<br />
this species. Depth range, this study: 180 m.<br />
Family Teredini<strong>da</strong>e Rafinesque, 1815<br />
Nototeredo norvagica (Spengler, 1792)<br />
(Figure 384)<br />
Remarks: Rare. This species lives in drifting<br />
wood.<br />
Teredora malleolus (Turton, 1822)<br />
(Figure 385)<br />
Remarks: Rare. This species lives in drifting<br />
wood.<br />
Family Xylophagi<strong>da</strong>e Purchon, 1941<br />
Xyloredo sp.<br />
(Figures 396-387)<br />
Remarks: Common. This species lives in<br />
sunken wood. Depth range, this study: 32-<br />
360 m.<br />
Order ANOMALODESMATA Dall, 1889<br />
Superfamily PHOLADOMYOIDA Newell,<br />
1965<br />
Family Thracii<strong>da</strong>e Stoliczka, 1870<br />
Thracia papyracea (Poli, 1791)<br />
(Figure 388)<br />
Remarks: Common. Ávila et al., 2000. Depth<br />
range: interti<strong>da</strong>l to 50 m (MM&B; P&G as T.<br />
phaseolina (Lamarck, 1818)); this study: 30-360<br />
m; alive: 32-198 m.
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 91<br />
Family Cuspi<strong>da</strong>rii<strong>da</strong>e Dall, 1886<br />
Cardiomya costellata (Deshayes, 1833)<br />
(Figure 389)<br />
Remarks: Common. Depth range: 18-200 m<br />
(P&G); infralittoral to 1400 m (MM&B); this<br />
study: 40-360 m; alive: 46-198 m.<br />
Cuspi<strong>da</strong>ria atlantica Allen & Morgan, 1981<br />
(Figure 390)<br />
Remarks: Rare. Depth range, this study: 129-<br />
207 m.<br />
Class CEPHALOPODA Schneider, 1784<br />
Subclass COLOIDEA Bather, 1788<br />
Order OCTOPODA Leach, 1818<br />
Suborder INCIRRATA Grimpe, 1916<br />
Family Octopodi<strong>da</strong>e d’Orbigny, 1840<br />
Octopus vulgaris Cuvier, 1797<br />
(Figure 391)<br />
Remarks: One very young specimen collected<br />
alive on a crevice of a dredged rock. Depth<br />
range, this study: 150 m.<br />
ACKNOWLEDGEMENTS<br />
We thank Serge Gofas, Henk Dijsktra,<br />
Emílio Rolán and Marco Oliverio for their<br />
kind contributions to the identities of many<br />
species. Sérgio P. Ávila was supported by<br />
grant SFRH/BPD/22913/2005 (FCT –<br />
Fun<strong>da</strong>ção para a Ciência e Tecnologia) of the<br />
Portuguese government. IMAR-DOP/UAc<br />
(UI&D #531 and ISR LA#9) is funded by<br />
FCT/MCTES– Lisbon and DRCT/Azores<br />
through pluri-annual and programmatic<br />
funding schemes (part FEDER).<br />
LITERATURE CITED<br />
ADAM, W., & J. KNUDSEN, 1969.<br />
Quelques genres de mollusques<br />
prosobranches marins inconnus ou<br />
peu connus de l’Afrique<br />
Occidentale. Bulletin de l’Institut<br />
royal des Sciences naturelles de<br />
Belgique, 44(27): 1-69.<br />
ÁVILA, S.P., 2000. The shallow-water<br />
Rissoi<strong>da</strong>e (Mollusca, Gastropo<strong>da</strong>)<br />
of the Azores and some aspects of<br />
their ecology. Iberus, 18(2): 51-76.<br />
ÁVILA, S.P., 2003. The littoral molluscs<br />
(Gastropo<strong>da</strong>, Bivalvia and<br />
Polyplacophora) of São Vicente,<br />
Capelas (São Miguel Island,<br />
Azores): ecology and biological<br />
associations to algae. Iberus, 21(1):<br />
11-33.<br />
ÁVILA, S.P., J.M.N. AZEVEDO, J.M.<br />
GONÇALVES, J. FONTES & F.<br />
CARDIGOS, 2000. Checklist of the<br />
shallow-water marine molluscs of<br />
the Azores: 2 - São Miguel island.<br />
Açoreana, 9(2): 139-173.<br />
BOUCHET, P., 1984. Les Triphori<strong>da</strong>e<br />
de Mediterranée et le proche<br />
Atlantique (Mollusca, Gastropo<strong>da</strong>).<br />
Lavori Società Italiana di<br />
Malacologia, 21: 5-58. [not seen]<br />
BOUCHET, P., & H. GUILLEMOT,<br />
1978. The Triphora perversa complex<br />
in Western Europe. Journal of<br />
Molluscan Studies, 44: 344-356.<br />
BULLOCK, R.C., 1995. The distribution<br />
of the molluscan fauna associated<br />
with the interti<strong>da</strong>l coralline<br />
algal turf of a partially submerged<br />
volcanic crater, the Ilhéu de Vila<br />
Franca, São Miguel, Azores. In:<br />
MARTINS, A.M.F. (ed.), The marine<br />
fauna and flora of the Azores.<br />
Proceedings of the Second International<br />
Workshop of Malacology and<br />
Marine Biology, Vila Franca do<br />
Campo, São Miguel, Azores.<br />
Açoreana, Supplement [4]: 9-55.<br />
BULLOCK, R.C., TURNER, R.D. &<br />
R.A. FRALICK, 1990. Species richness<br />
and diversity of algal - associated<br />
micromolluscan communities<br />
from São Miguel, <strong>Açores</strong>. In:<br />
MARTINS, A.M.F. (ed.), The marine<br />
fauna and flora of the Azores.<br />
Proceedings of the First International<br />
Workshop of Malacology São Miguel,<br />
Azores. Açoreana, Supplement [2]:<br />
39-58.
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CONTRERAS, J.A., 1992. Una nuova<br />
Gibberula <strong>da</strong>lle Isole Azzorre<br />
(Gastropo<strong>da</strong>, Marginelli<strong>da</strong>e). La<br />
Conchiglia, 262: 44-45.<br />
GOFAS, S., 1990. The littoral<br />
Rissoi<strong>da</strong>e and Anabathri<strong>da</strong>e of São<br />
Miguel, Azores. In: MARTINS,<br />
A.M.F. (ed.), The marine fauna and<br />
flora of the Azores. Proceedings of the<br />
First International Workshop of<br />
Malacology São Miguel, Azores.<br />
Açoreana, Supplement [2]: 97-134.<br />
HOUBRICK, J., 1990. Anatomy,<br />
reproductive biology and systematic<br />
position of Fossarus ambiguous<br />
(Linné) (Fossarinae: Planaxi<strong>da</strong>e:<br />
Prosobranchia). In: MARTINS,<br />
A.M.F. (ed.), The marine fauna and<br />
flora of the Azores. Proceedings of the<br />
First International Workshop of<br />
Malacology São Miguel, Azores.<br />
Açoreana, Supplement [2]: 59-73.<br />
KNUDSEN, J., 1995. Observations on<br />
reproductive strategy and zoogeography<br />
of some marine<br />
Prosobranch Gastropods (Mollusca)<br />
from the Azores. In:<br />
MARTINS, A.M.F. (ed.), The marine<br />
fauna and flora of the Azores.<br />
Proceedings of the Second International<br />
Workshop of Malacology and<br />
Marine Biology, Vila Franca do<br />
Campo, São Miguel, Azores.<br />
Açoreana, Supplement [4]: 135-158.<br />
MACEDO, M.C.C., M.I.C. MACEDO<br />
& J.P. BORGES, 1999. Conchas<br />
Marinhas de Portugal, 516 pp.<br />
Editorial Verbo, Lisboa.<br />
MARTINS, A.M.F., 2004. The Princess’<br />
Ring, 99 pp. Intermezzo-Audiovisuais,<br />
L<strong>da</strong>., Lisboa.<br />
MIKKELSEN, P.M., 1995. Cephalaspids<br />
of the Azores. In:<br />
MARTINS, A.M.F. (ed.), The marine<br />
fauna and flora of the Azores.<br />
Proceedings of the Second<br />
International Workshop of Malacology<br />
and Marine Biology, Vila Franca do<br />
Campo, São Miguel, Azores.<br />
Açoreana, Supplement [4]: 193-215.<br />
MORTON, B., 1990. The biology and<br />
functional morphology of Ervilia<br />
castanea (Bivalvia: Tellinacea) from<br />
the Azores. In: MARTINS, A.M.F.<br />
(ed.), The marine fauna and flora<br />
of the Azores. Proceedings of the<br />
First International Workshop of<br />
Malacology São Miguel, Azores.<br />
Açoreana, Supplement [2]: 75-96.<br />
MORTON, B, 1995. The biology and<br />
functional morphology of Trichomusculus<br />
semigranatus (Bivalvia:<br />
Mytiloidea) from the Azores. In:<br />
MARTINS, A.M.F. (ed.), The marine<br />
fauna and flora of the Azores.<br />
Proceedings of the Second International<br />
Workshop of Malacology and<br />
Marine Biology, Vila Franca do<br />
Campo, São Miguel, Azores.<br />
Açoreana, Supplement [4]: 279-295.<br />
POPPE, G.T., & Y. GOTO, 1991-1993.<br />
European Seashells, vol. 1 [1991]<br />
(Polyplacophora, Caudofoveata,<br />
Solenogastra, Gastropo<strong>da</strong>), 352 pp;<br />
vol. 2 [1993] (Scaphopo<strong>da</strong>,<br />
Bivalvia, Cephalopo<strong>da</strong>), 221 pp.<br />
Verlag Christa Hemmen,<br />
Wiesbaden.<br />
ROLÁN, E., 2005. Malacological Fauna<br />
from the Cape Verde Archipelago, 455<br />
pp. ConchBooks, Hackenheim.
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 93<br />
FIGURE 391. Octopus vulgaris Cuvier, 1797 (Sta42)
94 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
TABLE 1. Distribution of the species dredged during the workshop. See text for station descrip-<br />
TAXA<br />
STATIONS<br />
3<br />
9<br />
2<br />
5<br />
3<br />
4<br />
1<br />
6<br />
3<br />
5<br />
1<br />
9<br />
POLYPLACOPHORA<br />
Lepidochiton cimicoides<br />
Acanthochitona fascicularis v v v v v<br />
4<br />
5<br />
5<br />
7<br />
5<br />
8<br />
3<br />
6<br />
4<br />
0<br />
0<br />
6<br />
0<br />
5<br />
1<br />
4<br />
1<br />
5<br />
2<br />
0<br />
3<br />
1<br />
4<br />
6<br />
0<br />
1<br />
5<br />
6<br />
3<br />
0<br />
4<br />
8<br />
GASTROPODA<br />
Patella candei v v v v v v<br />
Patella ulyssiponensis v v v v v v v<br />
Tectura virginea v v v v v v v v v v v v<br />
Propilidium exiguum<br />
Emarginula sp.<br />
Sinezona cingulata<br />
Haliotis coccinea v v f f v<br />
? Haliotis sp.<br />
Lepetella laterocompressa<br />
Addisonia excentrica<br />
Clelandella azorica<br />
v<br />
Clelandella sp.<br />
Jujubinus pseudogravinae v v v v v v v v v v v v v v<br />
Gibbula delgadensis v v v v<br />
Gibbula magus v + v v + + + + + + v + v v + v<br />
Margarites sp.<br />
Solariella azorensis + f f +<br />
Calliostoma lividum v f v f f<br />
Calliostoma hirondellei<br />
Cirsonella gaudryi<br />
Tricolia pullus azorica f v v v v f v v v v<br />
Bittium cf. latreillii v v v v v + v v v v v v v v v<br />
Bittium latreillii<br />
Fossarus ambiguus v f<br />
Cheirodonta pallescens v v v v v v<br />
Similiphora similior v v v v v v v v v<br />
Marshallora adversa v v v v v v<br />
Marshallora cf. adversa<br />
v<br />
Monophorus sp. v v v<br />
Monophorus erythrosoma v v v v v<br />
Monophorus thiriotae v v v v v<br />
Pogonodon pseudocanaricus<br />
f<br />
Strobiligera.brychia<br />
Metaxia cf. abrupta<br />
Cerithiopsis tubercularis v v v v<br />
Cerithiopsis tiara<br />
Cerithiopsis jeffreysi<br />
Cerithiopsis scalaris<br />
v<br />
Cerithiopsis minima v v v<br />
Cerithiopsis cf. minima<br />
v<br />
Cerithiopsis fayalensis<br />
Krachia cf. guernei<br />
Gyroscala lamellosa<br />
f<br />
Epitonium turtonis<br />
Epitonium clathrus<br />
Epitonium pulchellum<br />
v<br />
Epitonium celesti v v<br />
Punctiscala cerigottana
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 95<br />
tion. f, fragment; v, rolled shell or single valve; +, with live animal or both valves.<br />
4<br />
4<br />
5<br />
0<br />
5<br />
4<br />
1<br />
8<br />
4<br />
7<br />
4<br />
9<br />
1<br />
3<br />
2<br />
7<br />
2<br />
3<br />
2<br />
4<br />
2<br />
1<br />
1<br />
2<br />
0<br />
2<br />
2<br />
8<br />
4<br />
2<br />
2<br />
6<br />
0<br />
8<br />
3<br />
2<br />
0<br />
7<br />
2<br />
9<br />
3<br />
8<br />
3<br />
3<br />
3<br />
7<br />
4<br />
3<br />
5<br />
2<br />
5<br />
3<br />
5<br />
1<br />
4<br />
1<br />
5<br />
5<br />
v v f v v v<br />
+<br />
f v v v v v f f f<br />
f v v v v f v v v v v<br />
v v v v v v v v v v v v v v v v v v<br />
v<br />
v<br />
v<br />
v v f v v v v f v v<br />
v<br />
v v v v v<br />
v<br />
v v v v v + v v f v v<br />
f<br />
v<br />
v v v v v v f f f v v v v f v v v v v<br />
v v v v v v v v<br />
v v + v v v v v v v v v v v f f v v v f v v +<br />
v v v<br />
f v + v v v + f + + f v<br />
v v f v f v f f v v v<br />
v v v<br />
v<br />
f v f v v v v v v v v v v v<br />
v v v v v v v v v v v v v v v v v v v v v<br />
v<br />
v v v v v<br />
v v v v v<br />
v v v v v v v v v v v v<br />
v v v v v v v v v v v v v<br />
v<br />
v<br />
v<br />
v v v v v<br />
v v v v<br />
v<br />
v<br />
v v v<br />
v<br />
v<br />
v<br />
v v v v<br />
v v v<br />
v<br />
v v v v<br />
v v<br />
v<br />
v<br />
v<br />
v v v v<br />
v v v v v<br />
v
96 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
TABLE 1. Distribution of the species dredged during the workshop. See text for station descrip-<br />
STATIONS<br />
TAXA<br />
Acirsa subdecussata<br />
Opalia hellenica<br />
3<br />
9<br />
2<br />
5<br />
3<br />
4<br />
1<br />
6<br />
3<br />
5<br />
1<br />
9<br />
4<br />
5<br />
5<br />
7<br />
Opalia sp. 1<br />
Opalia sp. 2<br />
Melanella bosci<br />
Melanella cf. crosseana<br />
Melanella cf. trunca v v<br />
Parvioris microstoma<br />
Parvioris sp.<br />
Crinophteiros collinsi<br />
Sticteulima jeffreysiana<br />
Vitreolina sp.<br />
Vitreolina curva<br />
v<br />
Pelseneeria minor<br />
Littorina striata v f v<br />
Melarhaphe neritoides<br />
v<br />
Skeneopsis planorbis v v<br />
Rissoa guernei v v v<br />
Rissoa sp. 1<br />
Rissoa sp. 2<br />
Setia subvaricosa<br />
Setia cf. quisquiliarum<br />
Crisilla postrema v v v<br />
Crisilla cf. postrema<br />
Pseu<strong>dos</strong>etia azorica<br />
Cingula trifasciata v f<br />
Manzonia unifasciata v v v v<br />
Onoba moreleti<br />
Alvania angioyi v v<br />
Alvania poucheti v v<br />
Alvania mediolittoralis v v v<br />
Alvania punctura<br />
Alvania sp. (?tarsodes)<br />
v<br />
Alvania sleursi v v v v v v<br />
Alvania cancellata v v v v v v v v v v v<br />
Alvania platycephala<br />
Alvania cimicoides<br />
Alvania cf. cimicoides<br />
Caecum wayae<br />
v<br />
Talassia cf. tenuisculpta<br />
Capulus ungaricus<br />
Lamellaria perspicua<br />
v<br />
Trivia pulex v v v v v v v v f<br />
Trivia candidula v v v v v v v v v<br />
Erato sp.<br />
Aperiovula juanjosensii<br />
Notocochlis dillwynii<br />
Natica prietoi v + v + + + v v + + v v v f v<br />
Natica cf. prietoi<br />
v<br />
Phalium undulatum f f<br />
Atlanta peronii<br />
Protatlanta souleyeti<br />
Ocenebra erinaceus v v<br />
5<br />
8<br />
3<br />
6<br />
4<br />
0<br />
0<br />
6<br />
0<br />
5<br />
1<br />
4<br />
1<br />
5<br />
2<br />
0<br />
3<br />
1<br />
4<br />
6<br />
0<br />
1<br />
v<br />
5<br />
6<br />
3<br />
0<br />
4<br />
8<br />
v
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 97<br />
tion. f, fragment; v, rolled shell or single valve; +, with live animal or both valves. (cont.)<br />
4<br />
4<br />
5<br />
0<br />
5<br />
4<br />
1<br />
8<br />
4<br />
7<br />
4<br />
9<br />
1<br />
3<br />
2<br />
7<br />
2<br />
3<br />
2<br />
4<br />
2<br />
1<br />
1<br />
2<br />
0<br />
2<br />
2<br />
8<br />
4<br />
2<br />
2<br />
6<br />
0<br />
8<br />
3<br />
2<br />
0<br />
7<br />
2<br />
9<br />
3<br />
8<br />
3<br />
3<br />
3<br />
7<br />
4<br />
3<br />
5<br />
2<br />
5<br />
3<br />
5<br />
1<br />
4<br />
1<br />
5<br />
5<br />
+ + + v v v<br />
v<br />
v<br />
v v v<br />
v v v<br />
v<br />
v<br />
v<br />
v<br />
v<br />
v<br />
v v<br />
v<br />
f<br />
f<br />
v v v<br />
v v v v v v v v v v<br />
v<br />
v v v v<br />
v v<br />
v v<br />
v v v v v v<br />
v v v<br />
v<br />
v<br />
v v<br />
v v v v v v v v<br />
v v f v v<br />
v v v v v v v v v<br />
v v v v v v v<br />
v v v v v v<br />
v<br />
v v v v v v v v v<br />
v v v v v v v v v v v v v v v v<br />
v v v<br />
v v + v<br />
v<br />
v v v v v<br />
v<br />
v<br />
v v<br />
v v v<br />
v v v v v f f f f<br />
v v v v v v v v v v v f<br />
v<br />
v<br />
f<br />
+<br />
+ v v v + v + v v v f f f f + v v<br />
f f f<br />
v<br />
v<br />
v v v
98 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
TABLE 1. Distribution of the species dredged during the workshop. See text for station descrip-<br />
STATIONS<br />
TAXA<br />
Ocinebrina cf. aciculata<br />
3<br />
9<br />
2<br />
5<br />
3<br />
4<br />
1<br />
6<br />
3<br />
5<br />
1<br />
9<br />
4<br />
5<br />
5<br />
7<br />
?Ocinebrina cf. aciculata v v v v<br />
?Ocinebrina sp.<br />
v<br />
Orania fusulus + + v v +<br />
Trophonopsis barvicensis v v v v v v v<br />
Trophonopsis cf. muricatus<br />
v<br />
Coralliophila cf. meyendorffi v v v v<br />
Carolliophila panormitana<br />
Stramonita haemastoma v v v v v<br />
Gibberula vignali<br />
Gibberula cf. lazaroi<br />
Mitra cornea v v v v v<br />
Pollia dorbignyi<br />
f<br />
Nassarius incrassatus f v v v v f v v v v v v<br />
Nassarius cf. cuvierii<br />
Nassarius recidivus<br />
Columbella a<strong>da</strong>nsoni v v v v f f f v v f<br />
Mitrella pallaryi<br />
Anachis avaroides v v v v v v<br />
Brocchinia clenchi v v v v v v +<br />
Mitromorpha azorensis v v v v v v<br />
Bela nebula v v v + v v v v v v + + v<br />
Mangelia cf. costata v v v v<br />
Raphitoma purpurea v v v v<br />
Raphitoma linearis v v<br />
Raphitoma cf. aequalis v v v v v v + v v v + v f<br />
Raphitoma sp. v v v<br />
Pleurotomella gibbera<br />
Pleurotomella cf. gibbera<br />
Teretia teres<br />
Crassopleura maravignae v v v v v v v v v + v<br />
Haedropleura septangularis v v v v v v v v<br />
Philippia krebsi<br />
v<br />
Pseudotorinia architae<br />
Pseudomalaxis zanclaeus<br />
Mathil<strong>da</strong> cochlaeformis<br />
Mathil<strong>da</strong> retusa<br />
?Rissoella sp. 1<br />
?Rissoella sp. 2<br />
Omalogyra atomus<br />
O<strong>dos</strong>tomella doliolum<br />
Chrysalli<strong>da</strong> cf. flexuosa<br />
O<strong>dos</strong>tomia bernardi v v v v v<br />
O<strong>dos</strong>tomia cf. verhoeveni v v v<br />
O<strong>dos</strong>tomia duureni<br />
v<br />
O<strong>dos</strong>tomia cf. striolata<br />
Eulimella sp.<br />
Turbonilla rufa<br />
v<br />
Turbonilla lactea v v f v v<br />
Turbonilla sp. 1<br />
Turbonilla sp. 2<br />
Turbonilla sp. 3<br />
Turbonilla sp. 4<br />
5<br />
8<br />
3<br />
6<br />
4<br />
0<br />
v<br />
0<br />
6<br />
0<br />
5<br />
1<br />
4<br />
1<br />
5<br />
2<br />
0<br />
3<br />
1<br />
4<br />
6<br />
0<br />
1<br />
5<br />
6<br />
3<br />
0<br />
4<br />
8
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 99<br />
tion. f, fragment; v, rolled shell or single valve; +, with live animal or both valves. (cont.)<br />
4<br />
4<br />
5<br />
0<br />
5<br />
4<br />
1<br />
8<br />
4<br />
7<br />
4<br />
9<br />
1<br />
3<br />
2<br />
7<br />
2<br />
3<br />
2<br />
4<br />
2<br />
1<br />
1<br />
2<br />
0<br />
2<br />
2<br />
8<br />
4<br />
2<br />
2<br />
6<br />
0<br />
8<br />
3<br />
2<br />
0<br />
7<br />
2<br />
9<br />
3<br />
8<br />
3<br />
3<br />
3<br />
7<br />
4<br />
3<br />
5<br />
2<br />
5<br />
3<br />
5<br />
1<br />
4<br />
1<br />
5<br />
5<br />
v v v<br />
v v v v v<br />
f v v v v v f f v<br />
v v v v v v v v v v<br />
v<br />
v v v<br />
v<br />
v<br />
v v v v v f v f<br />
v<br />
v<br />
v v v v v<br />
v f v v f v f v v v v f v f<br />
v<br />
f f v f v<br />
v f v v v v v v v f v v f<br />
f v f<br />
v v v v v v v v v v v v v v<br />
v + v + v v v v v v v v v<br />
v v v v<br />
+ + v + + v v v + f + v v + v v v v v v<br />
+ v v v v + v v v v v<br />
v f f v<br />
v v v v v v v v f v v v v<br />
v v v v v v v v v v v v v v v v v<br />
v v v v v v v v<br />
v v v v v v<br />
v<br />
v v v<br />
v + v + v v v v v v f v v v v v v + v v v<br />
v v v v v v<br />
v<br />
+ v v v<br />
v<br />
f<br />
v<br />
v<br />
v<br />
v<br />
v f v<br />
v<br />
v v v v v v v v v<br />
v v v v v v<br />
v<br />
v v v v<br />
v<br />
v<br />
v<br />
v<br />
v<br />
v<br />
v<br />
v
100 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
TABLE 1. Distribution of the species dredged during the workshop. See text for station descrip-<br />
TAXA<br />
STATIONS<br />
3<br />
9<br />
2<br />
5<br />
3<br />
4<br />
1<br />
6<br />
3<br />
5<br />
1<br />
9<br />
4<br />
5<br />
Retusa truncatula v v<br />
Haminoea cf. orteai v v<br />
Atys macandrewi<br />
v<br />
Atys sp.<br />
v<br />
Philine approximans<br />
Philine sp.<br />
?Chelidonura africana<br />
Cavolinia inflexa v v v v v v v v v v<br />
Cavolinia tridentata<br />
Diacria trispinosa f v f<br />
Cuvierina atlantica<br />
Clio pyrami<strong>da</strong>ta v v<br />
Limacina cf. helicina<br />
Limacina inflata<br />
v<br />
Umbraculum umbraculum<br />
v<br />
Tylodina perversa<br />
Williamia gussonii<br />
v<br />
Ovatella vulcani<br />
Pedipes pedipes<br />
5<br />
7<br />
5<br />
8<br />
3<br />
6<br />
4<br />
0<br />
0<br />
6<br />
0<br />
5<br />
1<br />
4<br />
1<br />
5<br />
2<br />
0<br />
3<br />
1<br />
4<br />
6<br />
0<br />
1<br />
5<br />
6<br />
3<br />
0<br />
4<br />
8<br />
BIVALVIA<br />
Arca tetragona v f v v v v v v v v<br />
Asperarca nodulosa<br />
Bathyarca philippiana<br />
Limopsis minuta<br />
v<br />
Gregariella semigranata v v v v v v v v v v v v<br />
Rhomboidella prideauxi<br />
Pecten jacobaeus f v<br />
Aequipecten commutatus f v v v<br />
Aequipecten opercularis v v + + f + + v v f v<br />
Bractechlamys corallinoides v v v v f v v v<br />
Palliolum incomparabile f v v f<br />
Chlamys flexuosa<br />
v<br />
Talochlamys pusio v v v v v v v v v v v v<br />
Pododesmus patelliformis v v v v v v v v v<br />
Limaria hians v f v v v v v f v<br />
Neopycnodonte cochlear v v v<br />
Myrtea spinifera<br />
Lucinoma borealis v v v v v v<br />
Thyasira flexuosa<br />
Diplodonta berghi v v v<br />
Diplodonta trigona + + + v v v v + v<br />
Chama gryphoides v v<br />
Kurtiella pelluci<strong>da</strong> v v<br />
Basterotia clancula v v v v v v v<br />
Cardita calyculata v + v v v v v v v<br />
?Crassatina sp.<br />
v<br />
Papillicardium papillosum + + + v + + + v + v + + v<br />
Parvicardium vroomi v v v<br />
Tellina incarnata + + + v v v v v v v v v<br />
Tellina pygmaea + + + + + + + + + + + + + + +<br />
Arcopagia balaustina<br />
f<br />
?Tellina sp.
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 101<br />
tion. f, fragment; v, rolled shell or single valve; +, with live animal or both valves. (cont.)<br />
4<br />
4<br />
5<br />
0<br />
5<br />
4<br />
1<br />
8<br />
4<br />
7<br />
4<br />
9<br />
1<br />
3<br />
2<br />
7<br />
2<br />
3<br />
2<br />
4<br />
2<br />
1<br />
1<br />
2<br />
0<br />
2<br />
2<br />
8<br />
v v v v v<br />
v f v<br />
v v f v v v<br />
4<br />
2<br />
2<br />
6<br />
0<br />
8<br />
3<br />
2<br />
0<br />
7<br />
2<br />
9<br />
3<br />
8<br />
3<br />
3<br />
3<br />
7<br />
4<br />
3<br />
5<br />
2<br />
5<br />
3<br />
5<br />
1<br />
4<br />
1<br />
5<br />
5<br />
v v v v<br />
v<br />
v<br />
v v v v v v v v v v v v v v v v v v v v<br />
v f v v<br />
v v v v f f<br />
v v v f v v v<br />
v v v v v v v v v v v v v<br />
v v v<br />
v v v v v v v v<br />
v v v f<br />
v<br />
v v v v<br />
v<br />
v<br />
v v v v v v v v v v v v v v v v v v v v v<br />
v<br />
v v<br />
+ v v v v v v v v v v f v v v v v v<br />
v<br />
v<br />
+ v f f v f v f<br />
v v + v v f v v v v v f v<br />
+ v v + v v v v + v v v + v + v v v v v v v f<br />
v v v v v v v v v v v v v v v v f v v<br />
+ v v v v v v + + v v v v v v<br />
v<br />
v<br />
v v v v v v v v v v v v v v v v v v v v<br />
v v v v v v v v v v v v v v v<br />
v v v v v v v v v v v v f v f v v f v v<br />
+ v f v v v v v v v v v +<br />
v<br />
v v v v v v v + + v + + + v + + + + v<br />
v v v v v<br />
v v v v v v v<br />
+ v v v v v + v + v + + v v v + v v v v<br />
v v v + v v v + v v v +<br />
v + v v v + + v v v v<br />
v v v v v v v v v v v v<br />
v + v v + v + v v v v v v v v v v v<br />
+ + + + + v + + + + + + v v v + v v + v + v v<br />
v v v v v v v v v v v<br />
v v v + v v v v v v v v v v v v<br />
+ + + + + + + + + v + + + v v + v v v + v + v +<br />
+ v v + + + + + + f + + + + + v + v +<br />
v
102 AÇOREANA<br />
2009, Sup. 6: 15-103<br />
TABLE 1. Distribution of the species dredged during the workshop. See text for station descrip-<br />
STATIONS<br />
TAXA<br />
Azorinus chamasolen<br />
Coralliophaga lithophagella<br />
3<br />
9<br />
2<br />
5<br />
3<br />
4<br />
1<br />
6<br />
3<br />
5<br />
1<br />
9<br />
4<br />
5<br />
5<br />
7<br />
Venus casina + v v v v v v + v + v<br />
Venus verrucosa + +<br />
Globivenus effossa<br />
<strong>Timoclea</strong> <strong>ovata</strong> v + + + + + + + + + + + + +<br />
Gouldia minima v + + + + + + + v + + v<br />
Callista chione v v + v v v v v v v + v v<br />
Hiatella arctica<br />
Gastrochaena dubia<br />
Nototeredo norvagica<br />
Teredora malleolus v v<br />
Xyloredo sp. v v v v v v<br />
Thracia papyracea v + v + v v v v v v v v<br />
Cardiomya costellata v v + + + v<br />
Cuspi<strong>da</strong>ria atlantica<br />
5<br />
8<br />
3<br />
6<br />
4<br />
0<br />
v<br />
0<br />
6<br />
0<br />
5<br />
1<br />
4<br />
1<br />
5<br />
2<br />
0<br />
3<br />
1<br />
4<br />
6<br />
0<br />
1<br />
v<br />
5<br />
6<br />
3<br />
0<br />
4<br />
8<br />
CEPHALOPODA<br />
Octopus vulgaris
MARTINS ET AL: INFRALITORAL MOLLUSCS OFF VILA FRANCA DO CAMPO 103<br />
tion. f, fragment; v, rolled shell or single valve; +, with live animal or both valves. (cont.)<br />
4<br />
4<br />
5<br />
0<br />
5<br />
4<br />
1<br />
8<br />
4<br />
7<br />
4<br />
9<br />
1<br />
3<br />
2<br />
7<br />
2<br />
3<br />
2<br />
4<br />
2<br />
1<br />
1<br />
2<br />
0<br />
2<br />
2<br />
8<br />
4<br />
2<br />
+<br />
v v + v + v v v +<br />
v v + v v + v v v v + + v v v + v v v v v<br />
+ v v v v v v v v v<br />
v v f v +<br />
+ + + + + + + + + + + + + v v + + + + + + + v +<br />
v + v + v + + + + v + + + v v + v v + + v + v<br />
v + + v v + v v v v v v v v v v v v v<br />
v v v v v v<br />
v<br />
v v<br />
v<br />
v v v v v v v v v v v v v v v v v v<br />
v v v + v + v v v v v v v v v + v v v v<br />
v v + + v + + + + v + v + + v f v f<br />
v<br />
2<br />
6<br />
0<br />
8<br />
3<br />
2<br />
0<br />
7<br />
2<br />
9<br />
3<br />
8<br />
3<br />
3<br />
3<br />
7<br />
4<br />
3<br />
5<br />
2<br />
5<br />
3<br />
5<br />
1<br />
4<br />
1<br />
5<br />
5<br />
+
AÇOREANA, Suplemento 6, Setembro 2009: 105-119<br />
ASPECTS OF THE BIOLOGY AND FUNCTIONAL MORPHOLOGY OF TIMOCLEA<br />
OVATA (BIVALVIA: VENEROIDEA: VENERINAE) IN THE AÇORES, PORTUGAL,<br />
AND A COMPARISON WITH CHIONE ELEVATA (CHIONINAE)<br />
Brian Morton<br />
Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, U.K.<br />
e-mail: prof_bmorton@hotmail.co.uk<br />
ABSTRACT<br />
<strong>Timoclea</strong> <strong>ovata</strong> occurs in the Açorean offshore seabed down to ~200 metres depth.<br />
Here, however, it only grows to half (10 mm) the shell length of conspecifics in European<br />
continental waters. In the <strong>Açores</strong> also, T. <strong>ovata</strong> is drilled by a naticid pre<strong>da</strong>tor - probably<br />
Natica prietoi. This is the first report of naticid drilling pre<strong>da</strong>tion upon T. <strong>ovata</strong>.<br />
The shell and the organs of the mantle cavity and visceral mass, and their ciliary currents,<br />
are described (for the first time) and compared specifically with representatives of<br />
the Chioninae (within which it was traditionally placed), including the Western Pacific<br />
Bassina calophylla and the Western Atlantic Chione elevata (also illustrated herein).<br />
Anatomically all three species are similar to each other, reflecting the inherent conservatism<br />
of the venerid bauplan. An interesting aspect of the complex surface architectures<br />
of the shells of T. <strong>ovata</strong>, B. calophylla and C. elevata is that they are not successful in protecting<br />
individuals from, in particular, naticid pre<strong>da</strong>tion even though one supposes that<br />
this is what they are for. That is, in the pre<strong>da</strong>tor-prey “arms race”, naticids are clearly winning.<br />
Notwithstanding, the complex shell architecture may also fulfill other functions<br />
such as stabilizing these shallow burrowers in soft sediments.<br />
In other bivalve lineages, “success” has been achieved through reproductive and/or<br />
anatomical specializations. However, the two most widely distributed and, possibly, most<br />
“successful” modern bivalve lineages are the Mytiloidea and heterodont Veneroi<strong>da</strong> that<br />
are generally but not exclusively dominant on rocky and soft marine habitats, respectively.<br />
This success has been achieved by reproductive and anatomical conservatism. Thus,<br />
one can take virtually any mytilid or any venerid and they will be, as this study demonstrates<br />
for <strong>Timoclea</strong> <strong>ovata</strong>, generally similar to other representatives of their respective families.<br />
RESUMO<br />
<strong>Timoclea</strong> <strong>ovata</strong> ocorre nos fun<strong>dos</strong> costeiros <strong>dos</strong> mares <strong>dos</strong> <strong>Açores</strong> até uma<br />
profundi<strong>da</strong>de de ~200 metros. Aqui, porém, cresce apenas até metade (10 mm) do<br />
comprimento de concha <strong>dos</strong> seus conspecíficos em águas continentais Europeias.<br />
Também nos <strong>Açores</strong> T. <strong>ovata</strong> é perfura<strong>da</strong> por um pre<strong>da</strong>dor naticídeo – provavelmente<br />
Natica prietoi. Este é o primeiro registo de pre<strong>da</strong>ção por perfuração de um naticídeo em T.<br />
<strong>ovata</strong>.<br />
Descrevem-se (pela primeira vez) a concha e os órgãos <strong>da</strong> cavi<strong>da</strong>de palial e massa<br />
visceral, e as suas correntes ciliares, e comparam-se especificamente com outros<br />
representantes <strong>dos</strong> Chioninae, incluindo Bassina calophylla do Pacífico Oeste e Chione<br />
elevata do Atlântico Oeste (também ilustra<strong>da</strong> aqui). Anatomicamente as três chioninas são<br />
muito semelhantes entre si, reflectindo o conservantismo inerente do bauplan venerídeo.<br />
Um aspecto interessante <strong>da</strong> complexa arquitectura <strong>da</strong> superfície <strong>da</strong> concha chionina,<br />
incluindo T. <strong>ovata</strong>, é não ser muito bem sucedi<strong>da</strong> em proteger os seus representantes de,<br />
em particular, pre<strong>da</strong>ção por naticídeos embora se pense ser esta a sua função. Isto é, na<br />
“corri<strong>da</strong> às armas” de pre<strong>da</strong>dor-presa, os naticídeos estão claramente a ganhar. Não
106 AÇOREANA<br />
2009, Sup. 6: 105-119<br />
(Figure 5B). Jones (1979) compared the<br />
anatomy of Chione cancellata (Linnaeus,<br />
1767) with those of other chionines.<br />
Morton & Knapp (2004) re-examined<br />
some aspects of the anatomy of the<br />
Atlantic C. elevata and compared it with<br />
the Pacific Bassina calophylla, specifically<br />
with regard to how the shell architecture,<br />
in particular, protects (or rather does not)<br />
the contained animal from drilling pre<strong>da</strong>tors<br />
of the Natici<strong>da</strong>e.<br />
<strong>Timoclea</strong> <strong>ovata</strong> has a wide distribution<br />
from northern Norway and Iceland south<br />
to Angola (West Africa). It is also recorded<br />
from the Canary Islands, the <strong>Açores</strong><br />
and the Mediterranean and Black Sea.<br />
Despite this wide distribution there is, as<br />
noted above, little known about the<br />
anatomy of T. <strong>ovata</strong> and little also about<br />
its basic biology. Labrune et al. (2007)<br />
described changes in the species composition<br />
of the macrofauna of the Bay of<br />
Banyuls-sur-Mer in the Mediterranean<br />
between 1967 and 2003 noting that the<br />
greatest changes were in the T. (as Venus)<br />
<strong>ovata</strong> community between 1967-1968 and<br />
1994. The size frequency distribution of a<br />
population of T. <strong>ovata</strong> from the Pliocene of<br />
Volpedo, Italy, was described by Benigni<br />
& Corselli (1981) and Dauvin (1985)<br />
undertook a study of the population<br />
dynamics of a Recent population of the<br />
same species from the Bay of Moraix in<br />
the Mediterranean noting there to be<br />
pluri-annual variations in recruitment,<br />
growth and production, thereby explainobstante,<br />
a arquitectura <strong>da</strong> concha chionina pode também exercer outras funções tais<br />
como estabilizar estes escavadores superficiais nos sedimentos finos.<br />
Noutras linhagens de bivalves, o “sucesso” foi conseguido mediante especializações<br />
reprodutivas e/ou anatómicas. No entanto, as duas linhagens de bivalves modernos mais<br />
largamente distribuí<strong>da</strong>s e, possivelmente, melhor sucedi<strong>da</strong>s são os Mytiloidea e os<br />
heterodontes Veneroi<strong>da</strong> que são geralmente mas não exclusivamente dominantes em<br />
habitats marinhos rochoso e mole, respectivamente. Tal sucesso foi conseguido mediante<br />
conservantismo reprodutivo e anatómico. Assim, pode tomar-se virtualmente qualquer<br />
mitilídeo ou qualquer venerídeo e eles serão, como este estudo demonstra para os<br />
Chioninae, respectivamente muito semelhantes aos seus outros representantes.<br />
INTRODUCTION<br />
<strong>Timoclea</strong> <strong>ovata</strong> (Pennant, 1777) was classified<br />
by Keen (1969) as a member of<br />
the Chioninae Frizzell, 1936 (Veneroidea,<br />
Veneri<strong>da</strong>e), representatives of which have<br />
been studied anatomically by Ansell<br />
(1961), Jones (1979), Morton (1985) and<br />
Morton & Knapp (2004). Morton (1985)<br />
compared Bassina calophylla (Philippi,<br />
1836) (Chioninae) with Irus irus<br />
(Linnaeus, 1758) (Tapetinae A<strong>da</strong>ms &<br />
A<strong>da</strong>ms, 1852). Subsequently, however,<br />
Coan et al. (1997) synonymized the<br />
Chioninae with the Venerinae<br />
Rafinesque, 1815. Kappner & Bieler<br />
(2006) have, most recently, and on the<br />
basis of a much broader gene sequencing<br />
study, argued, however, that the<br />
Chioninae, with Chione cancellata<br />
(Linnaeus, 1767) as its type species, is a<br />
distinct entity from the Venerinae as proposed<br />
by Canapa et al. (2003). Kappner &<br />
Bieler (2006), however, have also demonstrated<br />
that <strong>Timoclea</strong> Brown, 1827 should<br />
be placed within the Venerinae and not<br />
within the Chioninae.<br />
Ansell (1961) compared the anatomy<br />
of the British species of Veneracea<br />
(Veneroidea) but, surprisingly, had little<br />
to say about <strong>Timoclea</strong> (as Venus) <strong>ovata</strong> noting<br />
only that, in common with Gafrarium<br />
minimum (Montagu, 1803), the inner apertures<br />
of the siphons possessed membranes<br />
that, in the case of the inhalant,<br />
directed the incoming water dorsally
MORTON: TIMOCLEA OVATA IN THE AZORES 107<br />
ing the observations of Labrune et al.<br />
(2007). Anfossi & Brambilla (1981) noted<br />
that T. <strong>ovata</strong> has been a member of the<br />
Mediterranean’s detrital biocenosis since<br />
at least the Pleistocene. In terms of pre<strong>da</strong>tion,<br />
only Mienis (2003) has noted that<br />
the starfish Astropecten aranciacus<br />
(Linnaeus, 1758) preys upon T. <strong>ovata</strong>.<br />
This study was the first to be undertaken<br />
on <strong>Timoclea</strong> <strong>ovata</strong> in the <strong>Açores</strong>, a<br />
species initially recorded from there by<br />
Morton (1967). The study’s aims were<br />
three fold: (i), to obtain support for (or<br />
not) the proposal of Kappner & Bieler<br />
(2006) that T. <strong>ovata</strong> should be placed in the<br />
Venerinae; (ii), to document information<br />
on the biology of this species in the<br />
remote mid-Atlantic <strong>Açores</strong> and (iii), to<br />
provide a picture of its anatomy that<br />
might explain facets of its biology and<br />
give clues to the success of the venerid<br />
bauplan.<br />
MATERIALS AND METHODS<br />
Biology<br />
For ten <strong>da</strong>ys from 17-26 July 2006, the<br />
sea bed off the southern coast of the<br />
island of São Miguel, <strong>Açores</strong>, was<br />
sampled using a benthic box dredge at six<br />
stations to the east and west of Ilhéu de<br />
Vila Franca do Campo. Station details are<br />
described by Martins et al. (2009). Station<br />
depths ranged from –50 to -250 metres<br />
C.D.. All living and empty shells of<br />
<strong>Timoclea</strong> <strong>ovata</strong> (plus any living naticids)<br />
were sorted from the samples. These<br />
were analyzed in the following manner.<br />
Living individuals of <strong>Timoclea</strong> <strong>ovata</strong><br />
were measured along their greatest<br />
lengths using vernier calipers to the nearest<br />
0.5 mm. Empty shell valves were<br />
identified and both left and right ones<br />
were measured in the same manner.<br />
Empty valves were also examined for<br />
drill holes. Where these were encountered,<br />
the following records were made<br />
of: (i), which valve and (ii), the location of<br />
each drill hole was plotted on master<br />
illustrations of the left and right valves.<br />
Statistical analyses<br />
The <strong>da</strong>taset comprising the numbers<br />
of living, empty and drilled shell valves of<br />
<strong>Timoclea</strong> <strong>ovata</strong> among the six stations was<br />
tested for normality and homogeneity of<br />
variances using the Shapiro-Wilk test and<br />
Levene statistic, respectively, both at the<br />
p = 0.05 level of significance before<br />
ANOVA. One-way ANOVA’s were performed<br />
on the <strong>da</strong>taset to test the null<br />
hypothesis that there were no significant<br />
differences in these variables among locations.<br />
Where differences were detected,<br />
Student’s Newman-Keuls (SNK) tests<br />
were carried out to identify where the differences<br />
lay. The shell lengths of living T.<br />
<strong>ovata</strong> and empty and drilled valves were<br />
also compared using a one-way ANOVA<br />
and the Student’s Newman-Keuls (SNK)<br />
test.<br />
Anatomy<br />
Living individuals of <strong>Timoclea</strong> <strong>ovata</strong><br />
were observed alive in aquaria. Other living<br />
animals were dissected and drawings<br />
made of the anatomy, notably the organs<br />
of the mantle cavity. The ciliary currents<br />
in the mantle cavity were detected using a<br />
suspension of carmine in seawater.<br />
Living individuals of Chione elevata from<br />
Flori<strong>da</strong> were also examined in the same<br />
way.<br />
RESULTS<br />
Biology<br />
Living individuals of <strong>Timoclea</strong> <strong>ovata</strong><br />
were collected from all six stations and<br />
there was no significant difference in the<br />
numbers collected between them. Figure<br />
1 illustrates length frequency histograms<br />
for A, living individuals, B and C, empty<br />
left right shell valves, respectively, and D
108 AÇOREANA<br />
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and E, drilled left and right shell valves,<br />
again respectively. Living shells ranged<br />
in shell length from 1.5 mm to 9.0 mm, as<br />
did, approximately, the empty and drilled<br />
valves. One empty right valve was 10 mm<br />
in length.<br />
shell length showed that the valves of<br />
empty and drilled individuals, irrespective<br />
of whether they were the right or left<br />
valves, did not significantly differ in<br />
terms of mean shell length (p >0.05)<br />
whereas the valves of living individuals<br />
were significantly smaller than the empty<br />
valves (except for the drilled left valves,<br />
probably due to the small sample size).<br />
Figure 2 shows outline drawings of<br />
the left and right shell valves and the<br />
numbers and the distribution pattern of<br />
naticid drill holes made in them. There<br />
were over twice as many in the right<br />
(n=33) as in the left (n=15) valves and the<br />
pattern of distribution was unusual in<br />
that they were not near the umbones (an<br />
often favoured location for drilling gastropod<br />
pre<strong>da</strong>tors, as will be discussed).<br />
Rather, they seemed to be located mostly<br />
over the position of the pallial line, that is,<br />
where the thick, recessed, mantle edge is<br />
united to the shell internally.<br />
FIGURE 1. <strong>Timoclea</strong> <strong>ovata</strong>. Five histograms<br />
showing the size distributions of A, living individuals;<br />
B, empty left and C, right shell valves;<br />
C, and D, drilled left and right shell valves,<br />
respectively.<br />
The results of the ANOVA show that<br />
there were significant differences<br />
between the collected <strong>Timoclea</strong> <strong>ovata</strong> shells<br />
of the various categories, that is, living,<br />
empty and drilled valves, in term of their<br />
mean shell lengths (F = 6.96, p
MORTON: TIMOCLEA OVATA IN THE AZORES 109<br />
posteriorly, so that the beaks are distinctly<br />
prosogyrate (Figure 3A) and result<br />
from a strong tangential pattern of<br />
growth. This gives the shell its equilateral<br />
shape that increases during ontogeny<br />
so that the juvenile is more oval, the adult<br />
more angular.<br />
FIGURE 3. <strong>Timoclea</strong> <strong>ovata</strong>. Five stylized views<br />
of the shell and illustrated from A, the right<br />
side; B, dorsally; C, ventrally; D, anteriorly and<br />
E, posteriorly. (x—-y is the approximate position<br />
of the greatest width to the shell.) For<br />
other abbreviations see page 119.<br />
In dorsal view (Figure 3B), there is a<br />
small anterior, heart-shaped, lunule (LU)<br />
(as defined by Carter, 1967) each valve<br />
here also interlocking by means of marginal<br />
denticles as in Chione elevata<br />
(Morton & Knapp, 2004). Unlike other<br />
venerids, however, the lunule is not well<br />
defined because it is sculptured like the<br />
remainder of the shell but is defined by a<br />
light indentation and is coloured slightly<br />
differently. The more oval juvenile shell<br />
(JS) is also illustrated. There is no distinct<br />
posterior escutcheon because the ligament<br />
is internal, although it can be seen<br />
as a thin, black, line extending posterior<br />
to the umbones about one quarter of the<br />
way towards the posterior margin. The<br />
ventral shell valve margins (Figure 3C)<br />
are interlocked virtually everywhere<br />
along the extent of the shell margin by the<br />
expanding radial ribs. The shell valves of<br />
T. <strong>ovata</strong> are thus very difficult to separate,<br />
again like those of C. elevata (Morton &<br />
Knapp, 2004). Figures 3B & C also show<br />
the approximate position of the greatest<br />
shell width (x-y). It lies just posterior to<br />
the umbones above the ligament.<br />
The shell is illustrated in anterior view<br />
in Figure 3D and again shows the lunule<br />
(LU) and juvenile shell (JS). The greatest<br />
width to the shell when seen from this<br />
perspective (x-y) is dorsal to the mid<br />
point of the dorso-ventral height of the<br />
shell. A similar situation is seen when the<br />
shell is illustrated from the posterior perspective<br />
(Figure 3E).<br />
The shell of <strong>Timoclea</strong> <strong>ovata</strong> is illustrated<br />
in internal view in Figure 4A. The left<br />
valve (Figure 4A) has a hinge plate with<br />
an elongate posterior cardinal tooth and<br />
two other larger teeth more centrally<br />
placed. These are here interpreted as a<br />
central cardinal and robust anterior (but<br />
more centrally located, unlike the elongate<br />
posterior cardinal tooth) cardinal<br />
tooth, all arising from the umbo (U).<br />
There are no lateral teeth. The ligament<br />
(L) is internal and opisthodetic. Also well<br />
defined are anterior (AA) and a larger<br />
posterior (PA) adductor muscle scars.<br />
These are connected by a thick pallial line<br />
(PL) that has a similarly thick, short, pallial<br />
sinus (PS). Both are deeply inset from<br />
the valve margin and this is characterized<br />
by a scalloped edge internal to which,<br />
extending virtually all the way round are<br />
marginal denticles (MD) that interlock<br />
with those of the other valve. The interi-
110 AÇOREANA<br />
2009, Sup. 6: 105-119<br />
or of the shell is polished and is typically<br />
white although in those individuals with<br />
an external coloration, the interior reflects<br />
this as an orange-lilac stain. The hinge<br />
plate of the right valve similarly also has<br />
three (a central cardinal, elongate posterior<br />
lateral and more central and robust<br />
anterior lateral) teeth (Figure 4B).<br />
FIGURE 4. <strong>Timoclea</strong> <strong>ovata</strong>. A, An interior view<br />
of the left shell valve and B, an interior view of<br />
the right hinge plate. For abbreviations see<br />
page 119.<br />
FIGURE 5. <strong>Timoclea</strong> <strong>ovata</strong>. An individual illustrated<br />
in its life position in the sediment.<br />
The external appearance of the shell is<br />
illustrated from the right side in Figure 5.<br />
Each valve has a stout sculpture of ~50<br />
ribs that radiate from the umbones and<br />
because each valve has strong commarginal<br />
lamellae too, there are nodes on the<br />
ribs giving the shell a rough, file like, feel<br />
to the touch. As noted above the shell is<br />
often uniformly coloured light brown<br />
although those of most individuals are<br />
patterned with streaks and blotches of<br />
pink, red or brown. And some individuals<br />
have two radiating (antero- and postero-ventrally)<br />
bands of pigmentation, as<br />
illustrated in Figure 5.<br />
Tebble (1966) records that <strong>Timoclea</strong><br />
<strong>ovata</strong> has a maximum shell length of 19<br />
mm while Dauvin (1985) identified a figure<br />
of 15.1 mm for this species in the<br />
Mediterranean. As noted above, however,<br />
the largest Açorean individual<br />
collected had a shell length of but 10 mm.<br />
The siphons<br />
living individual of <strong>Timoclea</strong> <strong>ovata</strong> is<br />
illustrated in Figure 5 from the right side.<br />
Anteriorly, there is a large digging foot.<br />
Posteriorly, there is a pair of separated<br />
siphons. The exhalant siphon is conical<br />
and a ring of 12 short tentacles sub-apically<br />
surrounds its transparent coneshaped<br />
aperture. About 12 yellow-brown<br />
stripes arise from between each tentacle<br />
and extend inwards. The inhalant siphon<br />
is much larger in diameter and is fringed<br />
apically by a circlet of ~24 long siphonal<br />
tentacles. As with the exhalant about 24<br />
yellow-brown stripes extend inwards.<br />
Where each stripe unites with the tentacular<br />
rings, there is a <strong>da</strong>rker brown spot.
MORTON: TIMOCLEA OVATA IN THE AZORES 111<br />
Mid-ventrally, the mantle possesses a line<br />
of papillae and pallial fusions, where they<br />
occur, are of the inner folds only, that is,<br />
type A (Yonge, 1982). The siphons are<br />
illustrated in greater detail in Figure 6.<br />
FIGURE 7. <strong>Timoclea</strong> <strong>ovata</strong>. The ciliary currents<br />
of the left mantle lobe after after removal of the<br />
left shell valve and mantle and the body. For<br />
abbreviations see page 119.<br />
FIGURE 6. <strong>Timoclea</strong> <strong>ovata</strong>. A detail of the<br />
siphons.<br />
The ciliary currents of the organs of the mantle<br />
cavity<br />
The ciliary currents of the left mantle<br />
lobe of <strong>Timoclea</strong> <strong>ovata</strong> are illustrated in<br />
Figure 7. The pallial currents sweep particles<br />
of material in a clockwise direction<br />
towards the antero-dorsal regions of the<br />
mantle cavity and then downwards, so<br />
that particles end up in a ventral marginal<br />
rejection tract that transports such<br />
unwanted material towards the base of<br />
the inhalant siphon (IS) where it accumulates<br />
as balls of pseudofaecal matter (PM).<br />
These little balls are periodically ejected<br />
from the mantle cavity, via the inhalant<br />
siphon, by sharp contractions of the<br />
adductor muscles that create the pallial<br />
pressure necessary to do so.<br />
The right ctenidium of <strong>Timoclea</strong> <strong>ovata</strong><br />
is illustrated in Figure 8A. Each ctenidium<br />
is homorhabdic, eulamellibranchiate<br />
and comprises two unequal demibranchs.<br />
The inner demibranch (ID) is large and<br />
extends anteriorly from beneath the posterior<br />
adductor muscle (PA) up into the<br />
sub-umbonal cavity and ends on the postero-ventral<br />
face of the anterior adductor<br />
muscle (AA). The outer demibranch<br />
(OD) is dorso-ventrally short and and, as<br />
with the inner, extends anteriorly from<br />
beneath the posterior adductor muscle to<br />
a position just posterior of the hinge plate,<br />
beneath the ligament (L). This demibranch<br />
is thus foreshortened anteriorly.<br />
The ciliary currents of the right ctenidium<br />
are illustrated in transverse section<br />
in Figure 8B. The ciliary currents are of<br />
Type C (1) (Atkins, 1937), typical of many<br />
eulamellibranchs and, specifically, Venus<br />
fasciata (<strong>da</strong> Costa, 1778), Dosinia lupinus<br />
(Linnaeus, 1758), Venerupis aurea (Gmelin,<br />
1791) and Venerupis rhomboides (Pennant,<br />
1777) (Ansell, 1961). Ctenidia with a ciliation<br />
of type C (1) have oralward acceptance<br />
tracts located in the ctenidial axis<br />
and in the ventral marginal food groove<br />
of the inner demibranch (ID) only. Hence,<br />
particles filtered by the ascending lamella<br />
of the outer demibranch (OD) pass downward<br />
(although some may dorsally be<br />
carried anteriorly) (Figure 8A) and on<br />
reaching the ventral margin of this demi-
112 AÇOREANA<br />
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FIGURE 8. <strong>Timoclea</strong> <strong>ovata</strong>. A, The ciliary currents<br />
of the ctenidium as seen from the right<br />
side after removal of the right shell valve<br />
and mantle. B, A diagrammatic transverse<br />
section through the right ctenidium showing<br />
the ciliary currents. For abbreviations see<br />
page 119.<br />
branch, turn, and pass upwards on the<br />
descending lamella towards the ctenidial<br />
axis. In the food groove of the ctenidial<br />
axis they pass anteriorly. Ciliary currents<br />
on the inner demibranch are largely<br />
downward towards the ventral margin<br />
that has an anteriorly directed food<br />
groove. Because the outer demibranch is<br />
anteriorly foreshortened, at its anterior<br />
terminus, particles arriving here in the<br />
ctenidial axis pass on to the descending<br />
lamella of the inner demibranch. Thus,<br />
particles arrive at the ctenidial labial palp<br />
junction in (i), the ventral marginal food<br />
groove of the inner demibranch and (ii),<br />
in the ctenidial axis tract, also of the inner<br />
demibranch.<br />
The ctenidial-labial palp junction is of<br />
Category II (Stasek, 1964) and the palps<br />
(LP) are small, each possessing no more<br />
than five pleats that would, in the typical<br />
bivalve, have a sorting function, either<br />
accepting or rejecting particles of possible<br />
food according to size. Only those particles<br />
passing directly into the oral grooves<br />
of the palps from the acceptance tracts in<br />
the ctenidial axes, an arrangement that<br />
characterizes bivalves with a<br />
ctenidial/labial palp junction of Category<br />
II (Stasek, 1964), are forwarded directly to<br />
the mouth. The reduced size and sorting<br />
ability of the labial palps may be a reflection<br />
of the low numbers and narrow size<br />
limits of particles in the Açorean waters of<br />
the mid-Atlantic. Similarly, small labial<br />
palps have been recorded for Fragum erugatum<br />
(Tate, 1889), an inhabitant of oligotrophic,<br />
high salinity waters in Australia<br />
(Morton, 2000). Throughout its wide geographical<br />
range, however, T. <strong>ovata</strong> may<br />
occur in a variety of sediment types<br />
although it seems to prefer well-sorted<br />
gravels, as in the <strong>Açores</strong>, in which case<br />
the small labial palps are an a<strong>da</strong>ptation to<br />
sediments and overlying waters low in<br />
particulates.<br />
The ciliary currents of the right side of<br />
the visceral mass of <strong>Timoclea</strong> <strong>ovata</strong> are<br />
illustrated in Figure 9. On the surface of<br />
the right side of the visceral mass, the ciliary<br />
currents move material in a clockwise<br />
direction, anteriorly above and posteriorly<br />
below. Eventually, all such<br />
currents become directed downwards<br />
and feed into a rejection tract that passes<br />
accumulated material posteriorly where<br />
it falls off the posterior edge of the visceral<br />
mass onto the mantle. Ciliary currents<br />
on the foot (F) also pass material into this<br />
rejection tract. Particles that fall off the<br />
visceral mass are subjected to the ciliary<br />
currents of the mantle (Figure 7).<br />
Also illustrated in Figure 9 are some<br />
details of the structure of the visceral<br />
mass. Below and just posterior to the<br />
hinge plate, below the ligament (L), there<br />
is a heart (H) and posterior to this the<br />
brown, paired, kidneys (K). Anterior to<br />
the hinge plate is the <strong>da</strong>rk brown digestive<br />
diverticula (DD). The gut has not
MORTON: TIMOCLEA OVATA IN THE AZORES 113<br />
FIGURE 9. <strong>Timoclea</strong> <strong>ovata</strong>. The ciliary currents of the right side of the visceral mass after removal<br />
of the right shell valve, mantle and ctenidium. Also illustrated are some details of the structure of<br />
the visceral mass. For abbreviations see page 119.<br />
been examined in detail, but a conjoined<br />
style sac and mid gut (CSS/MG) leaves<br />
the postero-ventral edge of the stomach<br />
and passes postero-ventrally into the visceral<br />
mass. Eventually, the extremely thin<br />
mid gut (MG) separates from this and<br />
makes a single, simple loop upwards<br />
back towards the stomach but then passes<br />
posteriorly, penetrating the ventricle of<br />
the heart as the rectum (R) which passes<br />
over the posterior adductor muscle (PA)<br />
to terminate on its posterior surface as an<br />
anus.<br />
A final anatomical point is that, surprisingly,<br />
the pe<strong>da</strong>l retractor muscles are<br />
minute. The posterior pe<strong>da</strong>l retractor<br />
muscle (Figure 9, PPR) is located next to<br />
the antero-dorsal edge of the posterior<br />
adductor (PA) while the anterior pe<strong>da</strong>l<br />
retractor muscle (APR) is even smaller<br />
and located on the postero-dorsal edge of<br />
the anterior adductor muscle (AA). I use<br />
the word ‘surprisingly’ above, because,<br />
despite these tiny muscles, the foot is further<br />
surprisingly, very active. Hence, its<br />
movements must be largely related to<br />
hydrostatically induced pressure<br />
changes, as will be discussed.<br />
Comparison with Chione elevata<br />
Aspects of the anatomy and the ciliary<br />
currents of the ctenidium of Chione elevata<br />
are illustrated in Figure 10 and as seen<br />
from the right side after removal of the<br />
right shell valve and mantle. This drawing<br />
should be compared with the corresponding<br />
one for <strong>Timoclea</strong> <strong>ovata</strong> (Figure 8).<br />
In C. elevata, the shell has a lunule (L)<br />
beneath which are located interlocking<br />
denticles. The shell also has interlocking
114 AÇOREANA<br />
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valve margins and there are three hinge<br />
teeth in each valve, that is, what is here<br />
interpreted as anterior (ALT) and posterior<br />
lateral (PLT) and a large central cardinal<br />
teeth (CT). Jones (1979) also identifies<br />
three teeth in each valve of Chione cancellata<br />
(Linnaeus, 1767), C. paphia (Linnaeus,<br />
1767) and C. un<strong>da</strong>tella (Sowerby, 1835) but<br />
refers to them as anterior, central and posterior<br />
cardinal teeth, as decribed above<br />
for <strong>Timoclea</strong> <strong>ovata</strong>.<br />
Internally, Chione elevata has anterior<br />
(AA) and posterior (PA) adductor muscles<br />
and anterior (APR) and posterior<br />
(PPR) pe<strong>da</strong>l retractor muscles that are<br />
larger than those of <strong>Timoclea</strong> <strong>ovata</strong>. There<br />
is an extensive pe<strong>da</strong>l gape (PG) as in T.<br />
<strong>ovata</strong>, a large digging foot (F) and a mantle<br />
margin (MM) lined with mantle papillae<br />
(MP), all, again, as in T. <strong>ovata</strong>. The<br />
inhalant (IS) and exhalant (ES) siphons of<br />
C. elevata are very similar in structure to<br />
those of T. <strong>ovata</strong> and both have similarly<br />
organized ctenidia with ciliary currents of<br />
Type C (1) (Atkins, 1937). Both, therefore,<br />
have ctenidial-labial palp junction of<br />
Category II (Stasek, 1964). The labial<br />
palps of C. elevata are relatively larger<br />
than those of T. <strong>ovata</strong>, possibly because it<br />
inhabits shallow coastal waters off<br />
Flori<strong>da</strong>, U.S.A..<br />
In conclusion therefore Chione elevata<br />
and <strong>Timoclea</strong> <strong>ovata</strong> are similar anatomically,<br />
even though gene sequencing places<br />
FIGURE 10. Chione elevata. The ciliary currents of the ctenidium as seen from the right side after<br />
removal of the right shell valve and mantle. For abbreviations see page 119.
MORTON: TIMOCLEA OVATA IN THE AZORES 115<br />
them in two different sub-families, that is,<br />
the Chioninae and Venerinae, respectively<br />
(Kappner & Bieler, 2006). Importantly,<br />
such similarities now suggest convergence<br />
between the two thick-shelled and<br />
surface ornamented genera demonstrating<br />
the success, at least in part, of the veneroidean<br />
body plan as a whole and which<br />
seems to be based around anatomical<br />
conservatism.<br />
DISCUSSION<br />
Poppe & Gotto (1993) record a depth<br />
distribution of between 4 m to 200 m for<br />
<strong>Timoclea</strong> <strong>ovata</strong>, as does Tebble (1966),<br />
approximately. It is thus unsurprising that<br />
no differences in population numbers<br />
were recorded with depth from the<br />
Açorean dredge samples (50-200 m).<br />
Poppe & Gotto (1993) similarly note that T.<br />
<strong>ovata</strong> individuals from the northern part of<br />
the species’ range are larger than southern<br />
conspecifics. This may explain why the T.<br />
<strong>ovata</strong> individuals from Açorean waters are<br />
small (half the length of northern conspecifics),<br />
but it may also be because of the<br />
low levels of nutrients available to this<br />
species in the depauperate waters of the<br />
central Atlantic.<br />
Very little is known about the pre<strong>da</strong>tor-prey<br />
relationships of the Açorean<br />
marine fauna (Morton et al., 1998). In<br />
terms of the pre<strong>da</strong>tory gastropods, on<br />
rocky shores in the <strong>Açores</strong>, Thais haemastoma<br />
(Linnaeus, 1767) drills the interti<strong>da</strong>l<br />
mussel Gregariella semigranata (Reeve,<br />
1858) at the posterior margin (Morton,<br />
1995a). In Europe, Ansell (1960, 1982)<br />
demonstrated that Polinices alderi (Forbes,<br />
1838) drilled the bivalves Venus striatula <strong>da</strong><br />
Costa, 1778 and Tellina tenuis (<strong>da</strong> Costa,<br />
1778) whereas in the <strong>Açores</strong>, P. alderi<br />
attacked the commonest shallow subti<strong>da</strong>l<br />
bivalve, Ervilia castanea (Montagu, 1803),<br />
by drilling in a stereotypical, posterior,<br />
position (Morton, 1990a).<br />
Morton & Harper (2009) have studied<br />
the drill holes made in the tubes of the<br />
serpulid polychaete Ditrupa arietina (O.F.<br />
Müller, 1776) from depths of 50-200<br />
metres in the <strong>Açores</strong> and concluded that<br />
the only pre<strong>da</strong>tor present in the samples<br />
from which the tubes were collected was<br />
Natica prietoi Hi<strong>da</strong>lgo, 1873, formerly<br />
identified as Natica a<strong>da</strong>nsoni de Blainville,<br />
1825. Since the specimens of <strong>Timoclea</strong><br />
<strong>ovata</strong> reported upon here came from the<br />
same dredge samples it seems possible<br />
(likely) that N. prietoi made the holes in<br />
the shell of this species too. Confirmation<br />
of this is, however, required.<br />
Notwithstanding, Kabat (1990) has<br />
reviewed the literature on naticid pre<strong>da</strong>tion<br />
and there are no records of <strong>Timoclea</strong><br />
<strong>ovata</strong> as prey. This is thus the first record<br />
of naticid pre<strong>da</strong>tion, possibly by N. prietoi<br />
on T. <strong>ovata</strong>, although Vermeij (1980)<br />
reports that <strong>Timoclea</strong> marica (Linnaeus,<br />
1758) is drilled (laterally, as with T. <strong>ovata</strong>)<br />
by an unknown gastropod in Guam.<br />
Morton & Knapp (2004) identified an<br />
almost equal distribution of drill holes<br />
(and attempts) between the two valves of<br />
Chione elevata. Most of the drill holes<br />
were distributed around the postero-dorsal<br />
region of the shell and there were few<br />
failed drill holes. Finally, only a very few<br />
of the drill holes were over the shell<br />
lamellae and were at inter-lamellar<br />
spaces. That is, if the lamellae have<br />
evolved as anti-pre<strong>da</strong>tion devices, they<br />
are not very successful, in this case from<br />
the naticid Naticarius canrena (Linnaeus,<br />
1758). This is not the case with the also<br />
heavily sculptured Bassina calophylla<br />
(Chioninae) in the Indo-West Pacific<br />
(Ansell & Morton, 1985; 1987), where the<br />
shell lamellae do protect the bivalve<br />
inhabitant, except from species of edge<br />
drilling naticids, that is, Polinices tumidus<br />
(Swainson, 1844) and Polinices melanostomus<br />
(Gmelin, 1791).<br />
<strong>Timoclea</strong> <strong>ovata</strong> has a shell that, superfi-
116 AÇOREANA<br />
2009, Sup. 6: 105-119<br />
cially, would appear to offer much protection<br />
against drilling pre<strong>da</strong>tors. Protective<br />
characteristics include a relatively stout<br />
shell with tightly fitting valve margins,<br />
ventrally interlocking ribs, similarly interlocking<br />
denticles that occur all around the<br />
valve margins and large hinge teeth.<br />
Each adductor muscle is also large, facilitating<br />
sustained adduction and the pallial<br />
line is deeply inset within the shell margin.<br />
A thick shell characteristically protects<br />
bivalves from drilling pre<strong>da</strong>tors, for<br />
example, Corbula crassa Hinds, 1843 in<br />
Hong Kong (Morton, 1990b), although<br />
Borzone (1988) showed that a species of<br />
Polinices, as demonstrated here for N. prietoi<br />
Hi<strong>da</strong>lgo, 1873 and T. <strong>ovata</strong>, selectively<br />
drilled its prey, Venus antiqua King &<br />
Broderip, 1831, in the thickest region of<br />
the shell, that is, umbonally. Natica catena<br />
(<strong>da</strong> Costa, 1778) similarly bores its prey,<br />
the subti<strong>da</strong>l Donax vittatus (<strong>da</strong> Costa,<br />
1778) around the umbones (Negus, 1975).<br />
The anatomies of various representatives<br />
of the Chioninae have been<br />
described. These include Bassina calophylla<br />
(Morton, 1985) and Chione elevata (formerly<br />
identified as C. cancellata) (Jones,<br />
1979; Morton & Knapp, 2004) while<br />
Ansell (1961) has described the anatomies<br />
of the representatives of the Veneri<strong>da</strong>e<br />
(including a little about <strong>Timoclea</strong> <strong>ovata</strong>)<br />
that occur in British waters. The most<br />
obvious feature of the studied representatives<br />
of the Veneri<strong>da</strong>e is their anatomical<br />
conservatism. Hence, illustrations of the<br />
ctenidia within the mantle cavity of T.<br />
<strong>ovata</strong> (Venerinae), and C. elevata (illustrated<br />
herein: Figs 8 & 10, respectively) and B.<br />
calophylla (Morton, 1985, fig. 10)<br />
(Chioninae) are virtually identical, differing<br />
only in labial palp size. It is well<br />
known that palp size in the Bivalvia is<br />
related to the degree of sorting necessary<br />
for the particle load in the inhalant<br />
stream. Thus, the Hong Kong continental<br />
shelf species B. calophylla has large palps,<br />
the Floridian C. elevata has intermediate<br />
sized palps (Figure 10) while T. <strong>ovata</strong> has<br />
tiny palps (Figure 8). That is, because of<br />
high nutrient loading in continental shelf<br />
waters, B. calophylla needs big palps to<br />
reject a surfeit of unwanted particles<br />
whereas, oppositely, T. <strong>ovata</strong> in mid-<br />
Atlantic waters has little need to reject<br />
anything and has tiny palps. <strong>Timoclea</strong><br />
<strong>ovata</strong> has also, for the same reason, a<br />
short, narrow, mid-gut.<br />
Morton (1995b) pointed out that the<br />
two most widely distributed and, possibly,<br />
most “successful” modern bivalve<br />
lineages are the Mytiloidea and heterodont<br />
Veneroi<strong>da</strong> that are generally but<br />
not exclusively dominant on rocky and<br />
soft marine habitats, respectively. This<br />
has been achieved by reproductive (virtually<br />
all representatives being broadcast<br />
spawners) and anatomical conservatism.<br />
Thus, one can take virtually any mytilid<br />
or any venerid and they will be, as this<br />
study demonstrates for <strong>Timoclea</strong> <strong>ovata</strong>,<br />
similar to the other representatives of<br />
each order. In other bivalve lineages,<br />
more limited “success” has been achieved<br />
through reproductive and/or anatomical<br />
specialisms (Morton, 1995b). But the true<br />
inheritors of the bivalve bauplan are the<br />
modern Mytiloidea and Veneroidea.<br />
One interesting aspect of this “success”,<br />
however, is that, as discussed here,<br />
the complex surface architectures of the<br />
shell of the chionine Chione elevata and the<br />
venerine <strong>Timoclea</strong> <strong>ovata</strong> have not been successful<br />
in protecting representatives from,<br />
in particular, naticid pre<strong>da</strong>tion even<br />
though one instinctively supposes that<br />
that is what it is for. That is, in the pre<strong>da</strong>tor-prey<br />
“arms race”, naticids are clearly<br />
winning but the chionine shell architecture<br />
may also fulfill other functions such<br />
as the stability of the shallow burrowing<br />
<strong>Timoclea</strong> <strong>ovata</strong>, and other chionines, in soft<br />
sediments – a habitat that their shell<br />
architectures suit them ideally to.
MORTON: TIMOCLEA OVATA IN THE AZORES 117<br />
ACKNOWLEDGEMENTS<br />
I am grateful to Prof. A.M. Frias Martins<br />
(University of the <strong>Açores</strong>) for funding this<br />
research and for much practical help and<br />
warm hospitality during my stay on São<br />
Miguel. I also thank a number of University<br />
of the <strong>Açores</strong> students who helped with<br />
sample sorting and Dr. K.F. Leung (Hong<br />
Kong) for statistical advice.<br />
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GUIZIENA & J.M. AMAROUX, 2007.<br />
Long-term comparison of soft bottom<br />
macrobenthos in the Bay Banyuls-sur-<br />
Mer (north-western Mediterranean Sea):<br />
a reappraisal. Journal of Sea Research, 58:<br />
125-143.<br />
MARTINS, A.M.F, J.P. BORGES, S.P.<br />
ÁVILA, A.C. COSTA, P. MADEIRA & B.<br />
MORTON, 2009. Illustrated checklist of<br />
the infralittoral molluscs off Vila Franca<br />
do Campo. In: MARTINS, A.M.F. (ed.),<br />
The Marine Fauna and Flora of the Azores<br />
(Proceedings of the Third International<br />
Workshop of Malacology and Marine<br />
Biology, São Miguel 2006). Açoreana,<br />
Supplement 6: 15-103.<br />
MIENIS, H.K., 2003. <strong>Timoclea</strong> <strong>ovata</strong> in de<br />
maag van Astropecten aranciacus. Spirula,<br />
331: 26.<br />
MORTON, B., 1967. Malacological Report.<br />
In: Final Report, Chelsea College Azores<br />
Expedition, 1965. pp. 30-39. University of<br />
London, London<br />
MORTON, B., 1985. Aspects of the biology<br />
and functional morphology of Irus irus<br />
(Bivalvia: Veneri<strong>da</strong>e: Tapetinae) with a<br />
comparison of Bassina calophylla<br />
(Chioninae). In: MORTON, B., & D.<br />
DUDGEON (eds.), Proceedings of the<br />
Second International Workshop on the<br />
Malacofauna of Hong Kong and southern<br />
China, Hong Kong 1983, pp. 321-336.<br />
Hong Kong University Press, Hong<br />
Kong.<br />
MORTON, B., 1990a. The biology and<br />
functional morphology of Ervilia<br />
castanea (Bivalvia: Tellinacea) from the<br />
Azores. In: MARTINS, A.M.F. (ed.),<br />
Proceedings of the First International<br />
Workshop of Malacology, São Miguel,<br />
Azores, 1988. Açoreana, Supplement [2]:<br />
75-96.<br />
MORTON, B., 1990b. The functional morphology<br />
of Corbula crassa (Bivalvia:<br />
Corbuli<strong>da</strong>e) with special reference to<br />
shell structure and formation. In: MOR-<br />
TON, B. (ed.), Proceedings of the Second<br />
International Marine Biological Workshop:<br />
The Marine Flora and Fauna of Hong Kong<br />
and southern China (II), Hong Kong, 1986,<br />
pp. 1055-1073. Hong Kong University<br />
Press, Hong Kong.<br />
MORTON, B., 1995a. The biology and<br />
functional morphology of Trichomusculus<br />
semigranatus (Bivalvia:<br />
Mytiloidea) from the Azores. In:<br />
MARTINS, A.M.F. (ed.), The Marine<br />
Fauna and Flora of the Azores. Proceedings<br />
of the Second International Workshop of<br />
Malacology and Marine Biology, São<br />
Miguel, Azores, 1991. Açoreana,<br />
Supplement [4]: 279-295.<br />
MORTON, B. 1995b. Chapter 29. The evolutionary<br />
history of the Bivalvia. In: TAY-<br />
LOR, J.D (ed.). The Origin and<br />
Evolutionary Radiation of the Mollusca, pp.<br />
337-359. Oxford: Oxford University<br />
Press.<br />
MORTON, B., 2000. The biology and functional<br />
morphology of Fragum erugatum<br />
(Bivalvia: Cardii<strong>da</strong>e) from Shark Bay,<br />
Western Australia: the significance of its<br />
relationship with entrained zooxanthellae.<br />
Journal of Zoology, London, 251: 39-52.<br />
MORTON, B., & E.M. HARPER, 2009.<br />
Drilling pre<strong>da</strong>tion upon Ditrupa arietina
MORTON: TIMOCLEA OVATA IN THE AZORES 119<br />
(Polychaeta: Serpuli<strong>da</strong>e) from the mid-<br />
Atlantic <strong>Açores</strong>, Portugal. In: MARTINS,<br />
A.M. (ed.), The Marine Fauna and Flora of<br />
the Azores. (Proceedings of the Third<br />
International Workshop of Malacology and<br />
Marine Biology, São Miguel, Azores, 2006.<br />
Açoreana, Supplement 6: 157-165.<br />
MORTON, B., & KNAPP, M., 2004.<br />
Pre<strong>da</strong>tor-prey interactions between<br />
Chione elevata (Bivalvia: Chioninae) and<br />
Naticarius canrena (Gastropo<strong>da</strong>:<br />
Natici<strong>da</strong>e) in the Flori<strong>da</strong> Keys, U.S.A.<br />
Malacologia, 46: 295-308.<br />
MORTON, B., J.C. BRITTON, & A.M. de<br />
FRIAS MARTINS, 1998. Coastal Ecology<br />
of the <strong>Açores</strong>, pp. i-x + 249. Ponta<br />
Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal:<br />
Socie<strong>da</strong>de Afonso Chaves.<br />
NEGUS, M., 1975. An analysis of boreholes<br />
drilled by Natica catena (Da Costa) in the<br />
valves of Donax vittatus (Da Costa).<br />
Proceedings of the Malacological Society of<br />
London, 41: 353-356.<br />
POPPE, G.T., & Y. GOTO, 1993. European Sea<br />
Shells. Volume II. (Scaphopo<strong>da</strong>, Bivalvia,<br />
Cephalopo<strong>da</strong>), 221 pp. Wiesbaden:<br />
Hemmen.<br />
STASEK, C.R., 1964. Synopsis and discussion<br />
of the association of ctenidia and<br />
labial palps in the bivalved Mollusca.<br />
The Veliger, 6: 91-97.<br />
TEBBLE, N., 1966. British Bivalve Seashells,<br />
212 pp. London: Trustees of the British<br />
Museum (Natural History).<br />
VERMEIJ, G.J., 1980. Drilling pre<strong>da</strong>tion of<br />
bivalves in Guam: some paleoecological<br />
implications. Malacologia, 19: 329-334<br />
YONGE, C.M., 1982. Mantle margins with a<br />
revision of siphonal types in the<br />
Bivalvia. Journal of Molluscan Studies, 48:<br />
102-103.<br />
ABBREVIATIONS USED IN THE<br />
FIGURES<br />
AA Anterior adductor muscle or<br />
scar<br />
ALT Anterior lateral tooth<br />
APR Anterior pe<strong>da</strong>l retractor muscle<br />
AU Auricle (of heart)<br />
CSS/MG Conjoined style sac and mid<br />
gut<br />
CT Cardinal tooth<br />
DD Digestive diverticula<br />
ES Exhalant siphon<br />
F Foot<br />
H Heart<br />
ID Inner demibranch<br />
ILP Inner labial palp<br />
IS Inhalant siphon<br />
JS Juvenile shell<br />
K Kidney<br />
L Ligament<br />
LP Labial palp<br />
LU Lunule<br />
MD Marginal denticles<br />
MG Mid gut<br />
MM Mantle margin<br />
MP Mantle papillae<br />
OD Outer demibranch<br />
OLP Outer labial palp<br />
PA Posterior adductor muscle or<br />
scar<br />
PG Pe<strong>da</strong>l gape<br />
PL Pallial line<br />
PLT Posterior lateral tooth<br />
PM Pseudofaecal mass<br />
PPR Posterior pe<strong>da</strong>l retractor<br />
muscle<br />
PS Pallial sinus<br />
R Rectum<br />
U Umbo<br />
V Ventricle (of heart)
AÇOREANA, Suplemento 6, Setembro 2009: 121-135<br />
ANATOMY AND BIOLOGY OF MITRA CORNEA LAMARCK, 1811 (MOLLUSCA,<br />
CAENOGASTROPODA, MITRIDAE) FROM THE AZORES<br />
M. G. Harasewych<br />
Dept. of Invertebrate Zoology, MRC-163, National Museum of Natural History,<br />
Smithsonian Institution, PO Box 37012, Washington, D.C. 20013-7012. USA.<br />
e-mail: Harasewych@si.edu<br />
ABSTRACT<br />
Mitra cornea Lamarck, 1811, a member of the taxonomically complex group of small<br />
brown miters, is described anatomically, including observations on shell ultrastructure<br />
and diet. Morphological features confirm its taxonomic placement within the genus Mitra,<br />
and indicate a closer relationship with the western African Mitra nigra than with the<br />
Mediterranean Mitra cornicula. Mitra cornea shares the morphological a<strong>da</strong>ptations of the<br />
anterior alimentary system that have evolved in conjunction with a specialized sipunculan<br />
diet, and that appear to be fairly uniform within the Mitrinae. Studies on the composition<br />
and pharmacological effects of the secretions of the salivary glands and hypobranchial<br />
gland are needed to better interpret the origin and evolutionary pathways that gave rise<br />
to the extreme trophic specialization of the Mitri<strong>da</strong>e.<br />
RESUMO<br />
Descreve-se anatomicamente Mitra cornea Lamarck, 1811, um membro do grupo<br />
taxonomicamente complexo de pequenas mitras castanhas, incluindo-se observações<br />
sobre a estrutura <strong>da</strong> concha e sobre a dieta. As características morfológicas confirmam a<br />
sua localização taxonómica no género Mitra e indicam um relacionamento mais chegado<br />
com Mitra nigra, <strong>da</strong> África ocidental, do que com a mediterrânea Mitra cornicula. Mitra<br />
cornea possui as a<strong>da</strong>ptações morfológicas <strong>da</strong> porção anterior do sistema alimentar que<br />
evoluíram juntamente com uma dieta especializa<strong>da</strong> de sipúnculos, e que parece ser<br />
bastante uniforme dentro <strong>dos</strong> Mitrinae. São necessários estu<strong>dos</strong> sobre a composição e<br />
efeitos farmacológicos <strong>da</strong>s secreções <strong>da</strong>s glândulas salivares e <strong>da</strong> glândula hipobranquial<br />
para melhor se interpretar a origem e os percursos evolutivos que fizeram aparecer a<br />
especialização trófica extrema <strong>dos</strong> Mitri<strong>da</strong>e.<br />
INTRODUCTION<br />
The Mitri<strong>da</strong>e comprise a diverse and<br />
cosmopolitan family of pre<strong>da</strong>tory<br />
neogastropods that are common in the<br />
tropics, but are also present in temperate<br />
seas. Mitrids usually occur at interti<strong>da</strong>l<br />
to subti<strong>da</strong>l depths, but extend into the<br />
bathyal zone (Cernohorsky, 1976;<br />
Ponder, 1998). Taylor (1993) noted that<br />
Mitri<strong>da</strong>e are perhaps the most trophically<br />
specialized family of Neogastropo<strong>da</strong>,<br />
as all species studied to <strong>da</strong>te have been<br />
found to feed exclusively on Sipuncula<br />
(e.g., Kohn, 1970; Fukuyama &<br />
Nybakken, 1983; Loch, 1987; Taylor,<br />
1989; 1993).<br />
The mitrid fauna of the Azores is not<br />
diverse, with the family represented by<br />
two Recent species. Mitra zonata Marryat,<br />
1818, is easily distinguished by its large<br />
size and two-toned periostracum that is<br />
lighter in color along the apical portion of<br />
the shell above the suture. Cernohorsky<br />
(1976:367) regarded this Recent taxon to<br />
be a subspecies of the Pliocene Mitra<br />
(Mitra) fusiformis (Brocchi, 1814). He<br />
reported it to be limited to the western<br />
Mediterranean and northwestern Africa,<br />
but it has since been documented to occur
122 AÇOREANA<br />
2009, Sup. 6:121-135<br />
in the Azores by Burnay & Martins (1988).<br />
Martins (2004:94) noted that this species<br />
lives on offshore, sandy bottoms.<br />
A smaller species that inhabits the<br />
interti<strong>da</strong>l and subti<strong>da</strong>l rocky substrates of<br />
the Azores has a long and complicated<br />
taxonomic history. Multiple names have<br />
been applied to various phenotypes of<br />
small, smooth, <strong>da</strong>rk brown mitrids that<br />
inhabit the Mediterranean and eastern<br />
Atlantic. Rolán et al. (1997) reviewed the<br />
systematics of the “<strong>da</strong>rk brown<br />
Mitri<strong>da</strong>e”, concluded that three morphologically<br />
similar species are involved, and<br />
apportioned the multiple available names<br />
among them. According to these authors,<br />
Mitra cornicula (Linnaeus, 1758) is endemic<br />
to the Mediterranean Sea, Mitra<br />
nigra (Gmelin, 1791) ranges from the Cape<br />
Verde Islands to Angola, while the broad<br />
ranging Mitra cornea Lamarck, 1811, overlaps<br />
the range of the other two, occurring<br />
in the western Mediterranean Sea, the<br />
Macaronesian Archipelagos (Azores,<br />
Canaries, and Cape Verde Islands) and<br />
along the west coast of Africa as far south<br />
as Angola. The Mediterranean M. cornicula<br />
can be easily distinguished by its<br />
smaller shell size (to 25 mm), brown shell<br />
and brown periostracum, larger protoconch<br />
(320 µm) with fewer whorls ( 1¼),<br />
an animal that is entirely white, and a distinctive<br />
radula with lateral teeth that<br />
retain prominent dentition along their<br />
entire width (Rolan et al., 1997:fig. 16D).<br />
Mitra nigra and M. cornea are more similar<br />
in protoconch size, radular morphology,<br />
and periostracal color. Mitra nigra reaches<br />
a larger shell size (to 70 mm, compared<br />
to 40 mm for M. cornea) and has a black<br />
shell and brown to reddish-violet animal,<br />
while M. cornea has a light brown to pale<br />
grey shell and a distinctive white animal<br />
with yellow stripes along the tentacles<br />
and lateral margins of the foot (see<br />
Martins, 2004:65, fig. M). It should be<br />
noted, however, that this distinctive coloration<br />
is evident in living animals, but<br />
alcohol preserved specimens are brownish,<br />
becoming stained as the hypobranchial<br />
gland exu<strong>da</strong>te oxidizes to a<br />
purplish brown.<br />
Thus, the small brown mitrids of the<br />
Azores are Mitra cornea Lamarck, 1811.<br />
Earlier literature (e.g. Dautzenberg, 1889)<br />
may refer to this species as Mitra fusca<br />
Reeve, 1844, which, however, is a junior<br />
synonym of M. cornea and is preoccupied<br />
by Mitra fusca Swainson, 1831, an Indo-<br />
Pacific species. Cernohorsky (1969:972,<br />
fig. 28) designated as lectotype for Mitra<br />
cornea Lamarck, 1811, a specimen from<br />
the west coast of Africa, thus fixing its<br />
type locality. He regarded this taxon to be<br />
a synonym of M. cornicula, a species that<br />
is endemic to the Mediterranean and<br />
readily distinguished from M. cornea on<br />
the basis of shell and radular morphology.<br />
Mitra aquitanica Locard, 1892, is an<br />
unnecessary replacement name for Mitra<br />
fusca Reeve, 1844 non Swainson, 1831.<br />
Azorean records of Mitra cornea were,<br />
until recently, reported as Mitra nigra<br />
(e.g., Cernohorsky, 1976:371; Knudsen,<br />
1995:152; Morton et al., 1998:57, 65, 76).<br />
The present study documents the<br />
anatomy, shell morphology and biology<br />
of Mitra cornea from São Miguel, Azores,<br />
in order to provide a basis for more comprehensive<br />
studies of the systematics and<br />
relationships of the three small, smooth<br />
mitrids of the eastern Atlantic and<br />
Mediterranean Sea.<br />
MATERIALS AND METHODS<br />
Numerous specimens were collected<br />
from algae covered interti<strong>da</strong>l rocks along<br />
the SW wall of the fishing pier in Vila<br />
Franca do Campo, São Miguel, Azores<br />
[N37° 42’ 49.75”, W25 25’ 52.10”] (USNM<br />
1114338). Additional specimens were collected<br />
on shallow (< 1 m) subti<strong>da</strong>l rocky<br />
ledges along the southern rim of the
HARASEWYCH: ANATOMY AND BIOLOGY OF MITRA CORNEA 123<br />
crater of Ilhéu de Vila Franca, São Miguel,<br />
Azores [N37° 42’ 18.75”, W25° 26’ 35.33”]<br />
(USNM 1114340).<br />
Specimens were maintained and<br />
observed in seawater. The shells of a subset<br />
of specimens were cracked in a vice,<br />
and the animals irritated with forceps until<br />
they everted their proboscis. These animals<br />
were then preserved in 70% ethanol<br />
and transferred to 95% ethanol for storage.<br />
Animals were dissected, portions critical<br />
point dried and examined with a scanning<br />
electron microscope.<br />
SYSTEMATICS<br />
Class GASTROPODA<br />
Order Neogastropo<strong>da</strong> Wenz, 1943<br />
Family Mitri<strong>da</strong>e Swainson, 1831<br />
Genus Mitra Lamarck, 1798<br />
Mitra cornea Lamarck, 1811<br />
Synonymy<br />
Mitra cornea Lamarck, 1811<br />
Mitra fusca Reeve, 1844 non Mitra<br />
fusca Swainson, 1831<br />
Mitra aquitanica Locard, 1892<br />
Description<br />
Shell morphology: Shell (Figures 1, 2) small<br />
for genus (to 34 mm), thick, biconic,<br />
fusiform, with elongate aperture and 4<br />
heavy columellar folds. Protoconch<br />
increasing from ≈ 110 µm to ≈ 1.2 mm in 4<br />
¼ evenly rounded, conical whorls, badly<br />
eroded or missing on most specimens.<br />
Transition to teleoconch indistinct, marked<br />
by change in surface from glossy to matte,<br />
and onset of spiral sculpture consisting of<br />
narrow, pitted furrows separating adjacent<br />
broad, low, spiral cords. Teleoconch of up<br />
to 7+ smooth, evenly convex whorls.<br />
Suture adpressed, irregular, showing evidence<br />
of axial lamellae. Spiral sculpture of<br />
low, abutting spiral cords separated by a<br />
series of closely spaced pits in early<br />
whorls, that become sharply incised furrows<br />
in later whorls, and largely obscure<br />
except along the anterior third of the final<br />
whorl. Axial sculpture consists of low,<br />
nearly obscure lamellae that are most evident<br />
at the suture of smaller specimens<br />
(Figure 2) from which the periostracum<br />
has been removed. Pitting, periostracum,<br />
and repaired breaks (Figure 2, rb) obscure<br />
the sculpture of larger specimens.<br />
Aperture elongated, tapering posteriorly<br />
beneath suture to form anal sulcus. Outer<br />
lip smooth, thickened, nearly straight<br />
along middle portion, rounded and dorsally<br />
reflected anteriorly to form siphonal<br />
notch. Inner lip with narrow, glazed<br />
inductura, four broad columellar folds<br />
(Figure 3, cf), decreasing in prominence<br />
from posterior to anterior, and a siphonal<br />
fold (Figure 3, sf). Siphonal notch broad,<br />
siphonal fasciole usually absent, but may<br />
be weak and short in larger specimens.<br />
External shell color ranges from <strong>da</strong>rk<br />
chestnut brown to purplish gray and may<br />
be solid or banded. Aperture is white,<br />
especially the columellar folds, but brown<br />
color is visible through the white glaze<br />
near the anterior and posterior margins of<br />
the aperture. Periostracum thin, chestnut<br />
brown. Operculum absent.<br />
Shell ultrastructure: (Figure 4) Shell composed<br />
of four distinct crystal layers. The<br />
innermost layer (Figure 4, in) (≈ 90 µm)<br />
comprising the glaze is whitish, while the<br />
remaining layers are golden brown. The<br />
crystal faces of the next layer (Figure 4,<br />
per) (≈ 275 µm) are crossed-lamellar, and<br />
oriented perpendicular to the growing<br />
edge of the shell. They are also perpendicular<br />
to the crystal faces of the adjacent<br />
crossed lamellar layer (Figure 4, par) (≈ 435<br />
µm), which are parallel to the growing<br />
edge. A prismatic layer (Figure 4, ou)<br />
(≈ 120 µm) is outermost.<br />
External anatomy: (Figure 5) The soft tissues<br />
comprise 2½ whorls, of which the
124 AÇOREANA<br />
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FIGURES 1-4. Mitra cornea Lamarck, 1811. 1. USNM 1114338, interti<strong>da</strong>l rocks along the SW wall of the<br />
fishing pier in Vila Franca do Campo , São Miguel, Azores. 2. USNM 1114340, subti<strong>da</strong>l (< 1 m) rocky<br />
ledges along the southern rim of the crater of Ilhéu de Vila Franca, São Miguel, Azores. 3. Shell fractured<br />
to reveal columella. 4. shell ultrastructure. Surface parallel to growing edge of shell, ¼ whorl behind<br />
the lip. cf, columellar fold; in, innermost shell layer; ou, outer, prismatic shell layer; par, crossed-lamellar<br />
aragonite, crystal faces parallel to growing edge; per, crossed-lamellar aragonite, crystal faces perpendicular<br />
to crowing edge; rb, repaired break; sf, siphonal fold.
HARASEWYCH: ANATOMY AND BIOLOGY OF MITRA CORNEA 125<br />
FIGURES 5-10. Anatomical features of Mitra cornea Lamarck, 1811. 5. Male specimen, lateral view. 6.<br />
Roof of mantle cavity. 7. Alimentary system, semi-diagramatic. 8. Lateral view of anterior proboscis,<br />
opened from right side. 9. Female reproductive system. 10. Male reproductive system. a, anus; ag, albumen<br />
gland; ae, anterior esophagus; bc, bursa copulatrix; cg, capsule gland; cm, columellar muscle; ct,<br />
ctenidium; dg, digestive gland; dsg, duct of salivary gland; ep, epiproboscis; fo, female opening; hg,<br />
hypobranchial gland; ig, ingesting gland; k, kidney; m, mouth; me, mantle edge; ng, nephridial gland;<br />
nr, nerve ring; os, osphradium; p, penis; pb, proboscis; pc, pericardium; pp, peristomal papillae; pro,<br />
prostate gland; r, rectum; rg, rectal gland; rmc, rear of mantle cavity; rr, radular ribbon; s, siphon; sg, salivary<br />
gland; sto, stomach; sv, seminal vesicle; t, testis; td, testicular duct; vd, vas deferens; vor, ventral<br />
odontophoral retractor muscle.
126 AÇOREANA<br />
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mantle cavity spans ¾ whorl, the kidney<br />
¼ whorl, and the digestive gland and<br />
gonad 1½ whorls. The columellar muscle<br />
is long, narrow, attaching to the shell 1 ¼<br />
whorl behind the mantle edge. The foot is<br />
long, narrow, rectangular (L/W ≈ 2.0),<br />
with a deep propodial groove along the<br />
anterior edge. In living specimens, the<br />
foot is bright white with a narrow, bright<br />
yellow band along the lateral edges of the<br />
foot and outer edges of the tentacles as far<br />
as the eyes. The color is rapidly lost in<br />
alcohol preserved specimens, which<br />
become progressively <strong>da</strong>rker brown over<br />
time. The siphon is long and muscular.<br />
Mantle cavity: (Figure 6) The arrangement<br />
of mantle cavity organs is similar to that<br />
of most neogastropods. The mantle edge<br />
is thin and smooth, somewhat thickened<br />
at the right margin. The osphradium<br />
(Figure 6, os) is bipectinate, large, brownish,<br />
with 64-73 filaments above the ganglion<br />
and 52-60 below. The ctenidium<br />
(Figure 6, ct) is twice a broad and twice as<br />
long as the osphradium. A large renal<br />
organ (Figure 5, k), in which the primary<br />
and secon<strong>da</strong>ry lamellae do not interdgitate<br />
[termed Meronephridiens by Perrier<br />
(1889)] forms the right, rear wall of mantle<br />
cavity. The short, broad pericardium<br />
(Figure 5, pc), with a narrow nephridial<br />
gland (Figure 5, ng) lies to the left of the<br />
kidney. The hypobranchial gland (Figure<br />
6, hg) is broad and thick, occupying much<br />
of the dorsal roof of the mantle cavity<br />
between the osphradium and gonoduct.<br />
It produces a copious viscous secretion<br />
that is clear at first, but becomes yellowish<br />
then purple, and finally <strong>da</strong>rk brown.<br />
The color is alcohol soluble and stains the<br />
tissues of preserved specimens.<br />
Alimentary system: (Figure 7) The pleurombolic<br />
proboscis (Figures 5, 7 pb) is<br />
moderately long (extends to ≈ 1.5 x Shell<br />
length), broad, especially distally, enclosing<br />
a large, compact buccal mass and<br />
epiproboscis (Figures 5, 7, 8, 13-22, ep), an<br />
extensible muscular introvert unique to<br />
mitrids. When retracted, the proboscis is<br />
slightly folded within proboscis sheath<br />
and fills nearly the entire cephalic hemocoel.<br />
The buccal mass is broad, with a<br />
short, muscular, peristomal rim lined<br />
with evertable papillae surrounding the<br />
mouth. The odontophore and radular<br />
ribbon are large, with strong protractor<br />
and retractor muscles.<br />
The radular ribbon (Figures 11, 12) is<br />
short and broad (L/W ≈ 3.8; L = 1.9 mm, W<br />
= 500 µm), consisting of 45-57 rows of<br />
teeth, and may be slightly asymmetrical,<br />
with left lateral teeth 5-14% wider than<br />
right in some specimens. The rachidian<br />
teeth (Figure 11, rt) have five strong,<br />
curved cusps emerging from a weakly<br />
trapezoi<strong>da</strong>l basal plate that is broader at<br />
the posterior end. Each of the five cusps<br />
has a broad, thick dorsal surface continuous<br />
with the anterior end of the basal<br />
plate, and a sharply tapering, knife-like<br />
posterior-ventral edge that descends to<br />
the posterior end of the basal plate. The<br />
central cusp is longest, lateral cusps are<br />
shortest. The lateral teeth (Figure 11, lat)<br />
have a complex, semi-recurved basal<br />
plate that it broad, thin and flat along its<br />
outer edge, becoming narrower, thicker,<br />
with its anterior edge raised by up to 35º<br />
along the inner 1/3 of its length. Each<br />
tooth has 14-18 cusps. The 2 nd → 4 th from<br />
the inner edge are strongest, with the<br />
same knife-like structure as the cusps on<br />
the rachidian teeth. The remaining teeth<br />
become more conical and diminish in<br />
length and size toward the lateral edge,<br />
with the outermost 0.18 of the basal plate<br />
lacking discernible cusps.<br />
The epiproboscis is a long, anteriorly<br />
tapering, muscular rod, consisting of a<br />
central core of longitudinal muscles, surrounded<br />
by circular muscles and encased<br />
in an inner and outer sheath. From its
HARASEWYCH: ANATOMY AND BIOLOGY OF MITRA CORNEA 127<br />
FIGURES 11-12. Radula of Mitra cornea Lamarck, 1811. 11. Dorsal view of half row of radular<br />
teeth. 12. Oblique view of radular teeth. lat, lateral tooth; rt, rachidian tooth.<br />
opening just below the mouth (Figures 8,<br />
22, m), the epiproboscis runs mid-ventrally<br />
beneath the buccal mass, recurving<br />
dorsally to form a U-shaped bend behind<br />
the buccal mass to become attached to the<br />
odontophore by a short, broad retractor<br />
muscle. The large, ascinous salivary<br />
glands (Figure 7, sg) are situated above<br />
the nerve ring (Figure 7, nr) in the anterior<br />
portion of the cephalic hemocoel,<br />
generally to the right of the retracted proboscis.<br />
The ducts from these glands run<br />
anteriorly alongside the esophagus, joining<br />
the epiproboscis at the bend, running<br />
at first ventrally, then medially within the<br />
epiproboscis, merging into a single opening<br />
at its tip (Figures 13, 22, sd).<br />
The anterior esophagus is broad, and<br />
flat above the buccal mass (Figure 19, ae),<br />
with low longitudinal ridges, but<br />
becomes narrower and more circular posterior<br />
(Figure 21, ae) to the bend in the<br />
epiproboscis. The esophagus passes<br />
through the nerve ring without forming a<br />
distinctive valve of Leiblein, broadens to<br />
form a crop-like structure, and runs posteriorly<br />
to join a broad, muscular stomach.<br />
Neither a gland of Leiblein nor<br />
accessory salivary glands are present.<br />
The stomach (Figure 7, sto) has a muscular<br />
gizzard between the esophagus and<br />
the closely spaced ducts of the digestive<br />
glands. The intestinal region has low longitudinal<br />
ridges that lead to the long<br />
intestine, which runs along the kidney<br />
and pericardium before entering the rear<br />
of the mantle cavity. The rectum (Figure<br />
7, r) runs alongside the pallial gonoduct,<br />
forming the anus (Figures 7, 9, a) anterior<br />
to the gonoduct, but some distance from<br />
the mantle edge. A long, narrow rectal<br />
gland (Figure 7, rg) runs along the roof of<br />
the mantle cavity nearly its entire length,<br />
before joining the rectum near its anterior<br />
margin.<br />
Of the 20 specimens of Mitra cornea<br />
dissected, 7 were found to have essentially<br />
intact sipunculans (Golfingia sp. = G.<br />
margaritaceum fide Morton et al. 1998:76)<br />
within their gut, usually in the crop or<br />
stomach. No other recognizable prey was<br />
found within any of the specimens.<br />
Male reproductive system: The testis<br />
(Figure 10, t) is yellowish, lining the<br />
right ventral side of the digestive gland.<br />
A duct leading anteriorly expands to<br />
form the broad, highly convoluted seminal<br />
vesicle (Figure 10, sv) near the anterior<br />
margin of the digestive gland. From
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FIGURES 13-16. Proboscis tip of Mitra cornea Lamarck, 1811, showing extension of the epiproboscis.<br />
13. Lateral and 14. frontal views of proboscis tip in early stage of extension of epiproboscis.<br />
15. lateral and 16. frontal views of proboscis tip with epiproboscis extended. Arrows in figure 15<br />
indicate planes of section for figures 17-21. ep, epiproboscis; m, mouth; pb, proboscis; pp, peristomal<br />
papillae; s, siphon; sd, salivary duct opening; t, cephalic tentacle.<br />
there, the renal vas deferens runs along<br />
the surface of the nephridium without<br />
giving rise to a gonopericardial duct,<br />
entering the pallial cavity where it<br />
expands to form the prostate gland<br />
(Figure 10, pro). The prostate gland is<br />
open to the pallial cavity along its broad<br />
posterior portion, but forms a closed<br />
duct anteriorly that descends to the floor<br />
of the mantle cavity (Figure 10, vd) and<br />
runs to the base of the penis (Figures 5,<br />
10, p), situated behind the right cephalic<br />
tentacle. The penis is broad basally,<br />
strongly recurved, with a flagellate<br />
pseudo-papilla, with the duct opening<br />
at its tip.
HARASEWYCH: ANATOMY AND BIOLOGY OF MITRA CORNEA 129<br />
FIGURES 17-22. Proboscis tip of Mitra cornea Lamarck, 1811. 17-21. Transverse sections through proboscis<br />
tip shown in figure 15. 22. Saggital section through proboscis tip in figure 13. ae, anterior esophagus;<br />
bv, blood vessel; dop, dorsal odontophoral protractor muscle; ep, epiproboscis; eps, epiproboscis<br />
sheath; es, epiproboscis sheath; lm, longitudinal muscle; m, mouth; odc, odontophoral cartilage; pp,<br />
peristomal papillae; pr, peristomal rim; rs, radular sac; rt, radular teeth; sd, salivary duct; vor, ventral<br />
odontophoral retractor muscle.
130 AÇOREANA<br />
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Female reproductive system: The ovary lies<br />
along the right side of the digestive gland<br />
and dominates the uppermost visceral<br />
whorls. The oviduct runs anteriorly from<br />
the ovary, along the kidney and pericardium<br />
without giving rise to a gonopericardial<br />
duct, before entering the rear of the<br />
mantle cavity. The pallial gonoduct<br />
(Figure 9) consists of an albumen gland,<br />
ingesting gland, capsule gland and bursa<br />
copulatrix. The albumen gland (Figure<br />
9, ag) is tall, narrow, and glandular, with<br />
ventral channel. The ingesting gland<br />
(Figure 9, ig) is situated between the<br />
albumen gland and long capsule gland<br />
(Figure 9, cg). The large, muscular bursa<br />
copulatrix (Figure 9, bc) is situated above<br />
the female opening (Figure 9, fo) and<br />
above and anterior to the capsule gland.<br />
A prominent ventral pe<strong>da</strong>l gland is situated<br />
along the ventral mid-line of the<br />
foot, just anterior to the bursa copulatrix.<br />
Reproductive Biology: Knudsen (1995:153,<br />
fig. 13) illustrated the egg capsule and<br />
pre-hatching larva of this species [as<br />
Mitra nigra], noting that development<br />
was pelagic in this species. It was not<br />
known whether the larva develops into a<br />
sinusigera larva during the pelagic<br />
phase.<br />
DISCUSSION<br />
As the number of mitrids species that<br />
have been studied anatomically increases,<br />
all have been found to have a highly<br />
specialized anterior alimentary system<br />
with a broad, extensible, muscular proboscis<br />
and a uniquely evolved muscular<br />
epiproboscis that is extended through<br />
the mouth (Figures 13, 14, pp), and<br />
through which pass the ducts of the salivary<br />
glands, joining into a single duct<br />
before emptying at its tip (Figures 13, 14,<br />
sd). In mitrids, the accessory salivary<br />
glands and gland of Leiblein are absent<br />
and the valve of Leiblein is greatly<br />
reduced or absent. These anatomical<br />
structures are a<strong>da</strong>ptations to a specialized<br />
diet consisting nearly exclusively of<br />
sipunculans (see Taylor, 1993 and references<br />
therein). The diet of more than 30<br />
species of mitrids has been studied, yet<br />
there is but a single report of one individual<br />
of one species, feeding on a<br />
nemertean (Fukuyuma and Nybakken,<br />
1983).<br />
The earliest fossil record for family<br />
Mitri<strong>da</strong>e <strong>da</strong>tes to the basal Late<br />
Cretaceous [Cenomanian / Turonian]<br />
(Tracey et al. 1993:152), with most modern<br />
genera diverging during the Miocene<br />
(Cernohorsky, 1970:fig. 180). Yet all surviving<br />
lineages have a well developed<br />
epiproboscis, and lack accessory salivary<br />
glands and a gland of Leiblein, suggesting<br />
an early common origin of this specialized<br />
body plan, a<strong>da</strong>pted for preying<br />
on sipunculans. Relatively few neogastropods<br />
prey occasionally on sipunculans<br />
[eg., Vasum, Drupa, Bursa] and, other<br />
than Mitri<strong>da</strong>e, only a few species of<br />
Drupina feed exclusively on them (Taylor<br />
1989:271).<br />
Sipuncula is a small phylum with<br />
only about 150 species worldwide<br />
(Cutler, 1994:3). Sipunculans live in a<br />
variety of habitats, burrowing in rock,<br />
sand or rubble bottoms at all depths.<br />
The diversity of Mitri<strong>da</strong>e is somewhat<br />
greater, at 377 living species<br />
(Cernohorsky, 1970:Table 1).<br />
In the tropics, mitrid diversity is high<br />
and species partition their habitat by<br />
substrate type (e.g., Taylor, 1989:fig. 7),<br />
although multiple species can co-occur<br />
in the same general habitat (e.g. thick<br />
sand). In the Azores, the two mitrid<br />
species appear to partition their habitat,<br />
with M. cornea inhabiting interti<strong>da</strong>l to<br />
subti<strong>da</strong>l reef platforms and boulder rubble,<br />
while M. zonata occurs in offshore<br />
sandy substrates. Sipunculan diversity
HARASEWYCH: ANATOMY AND BIOLOGY OF MITRA CORNEA 131<br />
in the Azores somewhat exceeds mitrid<br />
diversity.<br />
Interpretation of the function of the<br />
epiproboscis has varied over the years.<br />
Several authors have proposed that the<br />
epiproboscis serves as a venomous organ<br />
(Vayssiere, 1901; Cernohorsky, 1970), is<br />
used for both offense and defense<br />
(Vayssiere, 1901), or applies the products<br />
of the salivary glands to the sipunculan<br />
prey (Risbec, 1928; Ponder, 1972, 1998).<br />
There has also been some question as to<br />
whether the salivary gland secretion<br />
weakens the prey integument, serves as<br />
a relaxant to prevent prey contraction, or<br />
acts as an adhesive substance to facilitate<br />
the removal of sipunculans from their<br />
burrows (West, 1990:774).<br />
Several authors have reported on the<br />
feeding behavior of mitrids with varying<br />
levels of detail. Loch (1987) reported that<br />
the epiproboscis is extended during<br />
feeding and inserted into its prey, and is<br />
thought to deliver salivary secretions.<br />
Taylor (1989:262) suggested that the peristomal<br />
papillae [“circum-oral, brush like<br />
structure”] can be everted during feeding<br />
and may function to grip prey, noting<br />
that, while mitrids have a large radula<br />
with long, multicuspate lateral teeth,<br />
these teeth may be used to assist with<br />
swallowing the prey, as the sipunculans<br />
and not shredded.<br />
The most detailed observations of<br />
feeding behavior were those of West<br />
(1990), who reported that Mitra i<strong>da</strong>e<br />
located its prey with its siphon, first<br />
touching it with the siphon edge and<br />
cephalic tentacles before extending its<br />
proboscis. The peristomal rim then<br />
grasps the prey in a series of rapid eversions<br />
and contractions and the snail<br />
retracts its proboscis in attempts to pull<br />
the sipunculan from the substratum. If<br />
the prey cannot be extracted and swallowed<br />
whole, secretions from the salivary<br />
gland are applied and the radula<br />
used to rasp a hole in the integument.<br />
The epiproboscis is then inserted into the<br />
hole, entangling the sipunculan viscera<br />
and pulling them into the mitrid buccal<br />
mass. This alternating extension and<br />
retraction of the epiproboscis is repeated<br />
multiple times. The proboscis periodically<br />
further envelopes the sipunculan<br />
and eventually frees the sipunculan from<br />
the substratum, by grasping the integument<br />
with the radula and retracting the<br />
odontophore. This behavior is characteristic<br />
of members of the subfamily<br />
Mitrinae, which includes Mitra cornea.<br />
Later, West (1991:710) reported on<br />
the feeding in Mitra catalinae, a member<br />
of the subfamily Cylindromitrinae. As in<br />
Mitrinae, the proboscis was extended,<br />
the peristome flared to grasp the prey<br />
and the radula was used to rasp a small<br />
hole in the integument through which<br />
the epiproboscis was inserted. However,<br />
in this species, the epiproboscis was<br />
“rhythmically passed in and out of the<br />
hole” pumping sipunculan coelomic fluids<br />
and eggs into the buccal cavity and<br />
down the esophagus of the mitrid, without<br />
ingesting either viscera or the entire<br />
sipunculan. West (1991:710) noted that<br />
the sipunculans “survived the feeding<br />
session,” suggesting parasitism rather<br />
than pre<strong>da</strong>tion in this mitrid species.<br />
Ponder (1972:335) raised the question<br />
of how the epiproboscis might have<br />
evolved. He suggested that the ducts of<br />
the salivary glands migrated ventrally,<br />
and that their openings moved from lateral<br />
positions on the buccal mass to a<br />
ventral anterior position at the edge of<br />
the mouth. The next hypothesized stage<br />
was their placement on a papilla that<br />
eventually became invaginated and elongated.<br />
Ponder noted that the salivary<br />
glands of mitrids have a second type of<br />
secretory cell not present in related families,<br />
and that these cells may produce a<br />
toxin. It is interesting to note, that
132 AÇOREANA<br />
2009, Sup. 6:121-135<br />
although the salivary glands are ascinous<br />
and typical of salivary glands of other<br />
neogastropods, the position of the ducts,<br />
including their becoming fused into a single<br />
duct before emerging medially at the<br />
ventral anterior edge of the buccal mass is<br />
typical of the ducts of accessory salivary<br />
glands, which are absent in Mitri<strong>da</strong>e.<br />
West (1991) noted that the epiproboscis<br />
shows structural and functional affinities<br />
with other molluscan subradular organs,<br />
and hypothesized that it developed from<br />
the musculature of the buccal mass, while<br />
the sheaths were derived from the walls<br />
of the buccal cavity. According to the<br />
Ponder model, the primary function of<br />
the epiproboscis is the targeted application<br />
of salivary gland secretions. The<br />
West model is based on a primarily<br />
mechanical function of the epiproboscis.<br />
West (1991:716) commented that the ventral<br />
migration of the salivary gland ducts<br />
“to connect with the formative epiproboscis”<br />
might have changed, or enhanced<br />
its function, but that it is difficult to assess<br />
the evolutionary importance of this event<br />
without knowledge of the function of salivary<br />
gland secretions”.<br />
While the morphological a<strong>da</strong>ptations<br />
of the anterior alimentary system that<br />
have evolved in conjunction with a specialized<br />
sipunculan diet are now well<br />
documented within the Mitri<strong>da</strong>e, nothing<br />
is known of the chemical a<strong>da</strong>ptations,<br />
including the composition and physiological<br />
effects of the secretions of the salivary<br />
glands, which are delivered to the prey<br />
through the epiproboscis. The salivary<br />
glands of related gastropods have been<br />
shown to produce neurotoxins with<br />
acetylcholine-like effects that are used to<br />
overcome prey with a paralytic secretion<br />
(West et al., 1998). Still others contain proteinaceous<br />
toxins that are hemolytic and<br />
lethal (Shiomi et al., 2002). Given that the<br />
Mitri<strong>da</strong>e represent an a<strong>da</strong>ptive radiation<br />
following an early [Upper Cretaceous]<br />
a<strong>da</strong>ptation to a highly specialized diet,<br />
the structure, specificity and toxicology of<br />
salivary gland secretions represent a fertile<br />
area for the study of chemical evolution<br />
within Mollusca, and interactions of<br />
pre<strong>da</strong>tor and prey.<br />
Similarly, the hypobranchial gland of<br />
mitrids is voluminous, and noted for producing<br />
substantial quantities of a<br />
secretion that oxidizes to form a purple<br />
pigment. Numerous authors since<br />
Dubois (1909) have documented that, in<br />
addition to chromogens, hypobranchial<br />
gland secretions from various<br />
neogastropods contain numerous toxic<br />
and paralytic compounds, including<br />
choline esters, serotonin and various<br />
biogenic amines (eg., Shiomi et al., 1998).<br />
The hypobranchial gland of the neogastropod<br />
Thais haemastoma (which co-occurs<br />
with Mitra cornea) contains multiple<br />
active components, including one that<br />
produces a stimulatory effect on blood<br />
pressure, and another that acts as a neuromuscular<br />
blocking agent of the depolarizing<br />
type (Hyang & Mir, 1971). Some<br />
muricids have been observed to use<br />
hypobranchial gland secretions to<br />
immobilize prey (Naegel & Alvarez,<br />
2005:426). Other taxa, including trochids<br />
(Kelley et al., 2003) and pleurotomariids<br />
(Harasewych, 2002) have been shown to<br />
use hypobranchial gland secretions to<br />
repel pre<strong>da</strong>tors.<br />
Despite the exceptionally thick shells,<br />
periostracum and overgrowth of calcified<br />
encrusting organisms, cleaned shells of<br />
many Mitra cornea show evidence of multiple<br />
repaired breaks (Figure 2, rb). This<br />
high incidence of unsuccessful pre<strong>da</strong>tion<br />
(measured as frequency of shell repair) is<br />
an indication of high exposure to crushing<br />
pre<strong>da</strong>tion as well as of the ability to<br />
survive such attacks by pre<strong>da</strong>tors.<br />
Among shallow water gastropods,<br />
Vermeij (1989) reported that the incidence<br />
of unsuccessful pre<strong>da</strong>tion was greatest in
HARASEWYCH: ANATOMY AND BIOLOGY OF MITRA CORNEA 133<br />
the Indo-West Pacific and lowest in the<br />
Atlantic. Frequencies of unsuccessful<br />
pre<strong>da</strong>tion of 0.5 breaks per individual<br />
were uncommon, and never averaged<br />
more than 1 break per individual for the<br />
most prey-resistent taxa. Repaired breaks<br />
on just the last whorl of the shell of Mitra<br />
cornea range from 0-5 [mean = 1.95, n =<br />
20], suggesting both an exceptionally<br />
high rate of attack, and ability to survive<br />
attack. While this points to the possible<br />
use of hypobranchial gland secretions as<br />
a chemical defense against pre<strong>da</strong>tors, it<br />
does not preclude the presence of other<br />
compounds or other uses for the secretory<br />
products of the hypobranchial gland.<br />
ACKNOWLEDGEMENTS<br />
I am grateful to Prof. António Frias<br />
Martins and to his staff and students for<br />
organizing the Third International<br />
Workshop of Malacology in Vila Franca<br />
do Campo, São Miguel, Azores. This<br />
Workshop was a joint organization of<br />
Socie<strong>da</strong>de Afonso Chaves and the<br />
Department of Biology of the University<br />
of the Azores. Support from FLAD<br />
(Portuguese-American Foun<strong>da</strong>tion for<br />
Development) is gratefully acknowledged.<br />
Thanks to Marilyn Schotte for<br />
assistance with histology and to Yolan<strong>da</strong><br />
Villacampa for Scanning Electron<br />
Micrographs.<br />
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DES, 1997. On some <strong>da</strong>rk species<br />
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the Atlantic. La Conchiglia, 29(285):<br />
11-23.<br />
SHIOMI K., M. ISHII, K. SHIMAKURA,<br />
Y. NAGASHIMA & M. CHINO, 1998.<br />
Tigloylcholine: a new choline ester<br />
toxin from the hypobranchial gland of<br />
two species of muricid gastropods<br />
(Thais Clavigera and Thais Bronni).<br />
Toxicon, 36(5): 795-798.<br />
SHIOMI, K., Y. KAWASHIMA, M.<br />
MIZUKAMI & Y. NAGASHIMA,<br />
2002. Properties of proteinaceous toxins<br />
in the salivary gland of the marine<br />
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TAYLOR, J.D., 1989. The diet of coral-reef<br />
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with a review of other species of the<br />
family. Journal of Natural History, 23:<br />
261-278.<br />
TAYLOR, J.D., 1993. Dietary and<br />
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gastropods (Mitri<strong>da</strong>e) at Rottnest<br />
Island, Western Australia. In: WELLS,<br />
F.E., D.I. WALKER, H. KIRKMAN &<br />
R. LETHBRIDGE (eds.), Proceedings of<br />
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583-599. Western Australian<br />
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TRACEY, S., J.A. TODD & D.H. ERWIN,<br />
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BENTON, M.J. (ed.), The Fossil Record<br />
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VAYSSIÈRE, A., 1901. Étude zoologique<br />
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WEST, D., E.B. ANDREWS, A.R.<br />
McVEAN, M.C. THORNDYKE & J.D.<br />
TAYLOR, 1998. Presence of a toxin in<br />
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Cymatium intermedius that targets<br />
nicotinic acetylcholine receptors.<br />
Toxicon, 36(1): 25-29.<br />
WEST, T.L., 1990. Feeding behaviour and<br />
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Marine Science, 46: 761-779.<br />
WEST, T.L., 1991. Functional morphology<br />
of the proboscis of Mitra catalinae Dall,<br />
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mitrid proboscis. Bulletin of Marine<br />
Science, 48: 702-718.
AÇOREANA, Suplemento 6, Setembro 2009: 137-143<br />
COMPARATIVE STUDY OF CHEMICAL DEFENCES FROM TWO ALLOPATRIC<br />
NORTH ATLANTIC SUBSPECIES OF HYPSELODORIS PICTA (MOLLUSCA:<br />
OPISTHOBRANCHIA)<br />
Helena Gaspar 1 , Ana Isabel Rodrigues 1 & Gonçalo Calado 2<br />
1 Instituto Nacional de Engenharia, Tecnologia e Inovação, I.P. (INETI), Est. Paço do Lumiar, Ef. F, 1649-038<br />
Lisboa, Portugal. e-mail helena.gaspar@ineti.pt<br />
2 Facul<strong>da</strong>de de Engenharias e Ciências Naturais, Universi<strong>da</strong>de Lusófona de Humani<strong>da</strong>des e Tecnologias.<br />
Av. do Campo Grande, 376 1749 - 024 Lisboa PORTUGAL<br />
ABSTRACT<br />
Different mixtures of furanosesquiterpenes characterized the defensive metabolites of<br />
the two populations of the nudibranchs Hypselodoris picta azorica and Hypselodoris picta<br />
webbi from the NW Atlantic, studied here for the first time. The known furonosesquiterpenes<br />
tavacfuran and longifolin were found in both subspecies, whereas micorcionin-1<br />
was only present in Hypselodoris picta azorica.<br />
RESUMO<br />
O estudo de duas populações de nudibrânquios Hypselodoris picta azorica e Hypselodoris<br />
picta webbi do Atlântico NW, descrito pela primeira vez neste artigo, mostrou que os seus<br />
metabolitos de defesa são misturas diferentes de furanosesquiterpenos. Em ambas as<br />
populações foram encontra<strong>dos</strong> os metabolitos tavacfurano e longifolina, tendo a<br />
microcionina-1 sido identifica<strong>da</strong> apenas na subespécie Hypselodoris picta azorica.<br />
INTRODUCTION<br />
Nudibranchs are shell-less opisthobranch<br />
molluscs that, in the course<br />
of evolution have developed several<br />
defensive strategies which include the<br />
use of secon<strong>da</strong>ry metabolites to avoid<br />
pre<strong>da</strong>tion (Wägele, 2006). These compounds<br />
can be accumulated from<br />
dietary sources, biosynthesised de novo<br />
or bio-transformed from dietary<br />
metabolites in order to provide the<br />
nudibranchs with more effective defensive<br />
allomones or non toxic compounds<br />
(Cimino, 1993, 1999). Most species of<br />
the genus Hypselodoris (Family<br />
Chromodori<strong>da</strong>e) store their allomones<br />
in high levels of concentrations, on special<br />
mantle glands denominated MDFs<br />
(Mantle Dermal Formations). These<br />
glands are strategically located near the<br />
vital organs, gills and rhinophores, or<br />
even ventrally along the mantle margin.<br />
They are regarded as the development<br />
of a chemical defensive mechanism in<br />
the course of opisthobranchs’ evolution<br />
(Wägele, 2006; García-Gómez, 1990;<br />
Fontana, 1993).<br />
Previous chemo-ecological studies of<br />
Hypselodoris picta (previously known as<br />
H. webbi or Glossodoris valenciennesi)<br />
showed that this species, like other<br />
Hypselodoris, accumulates in the mantle<br />
(especially in MDFs) furanosesquiterpenes,<br />
longifolin (1) being usually the<br />
main metabolite (Figure 1; Table 1). This<br />
compound, initially isolated from the<br />
terrestrial Japanese plant Actino<strong>da</strong>phne<br />
longifolia (Hayashi, 1972 fide Guella,<br />
1985), was the major metabolite found in<br />
a Mediterranean population of the<br />
marine sponge Dysidea fragilis (Avila,<br />
1991) and has antifee<strong>da</strong>nt and ichthyodeterrent<br />
activities (Fontana, 1993).<br />
Ecological experiments performed with<br />
Mediterranean populations of H. picta<br />
showed the transference of sponge<br />
metabolites into the MDFs and supported<br />
the dietary origin of Hypselodoris’<br />
allomones (Fontana, 1994b).
138 AÇOREANA<br />
2009, Sup. 6: 137-143<br />
FIGURE 1. Chemical structures of furanosesquiterpenes present in different populations of<br />
Hypselodoris picta.<br />
TABLE 1 – Furanosesquiterpenes present in different Mediterranean populations of Hypselodoris picta.
GASPAR ET AL: CHEMICAL DEFENCES OF HYPSELODORIS PICTA 139<br />
Hypselodoris picta (Schultz, 1836)<br />
seems to be widespread in the Atlantic<br />
Ocean. So far, five geographic subspecies<br />
are assigned, H. picta azorica being<br />
restricted to the Azorean Archipelago,<br />
whereas H. picta webbi spreads from the<br />
Caribbean to the Canary Islands and the<br />
Iberian Peninsula (Ortea et al., 1996). The<br />
colour pattern varies consistently (Figure<br />
2), but their internal anatomy is still very<br />
similar (Alejandrino & Valdés, 2006). No<br />
genetic <strong>da</strong>ta are available to <strong>da</strong>te. In this<br />
paper, we report a comparative study of<br />
chemical defences of these two allopatric<br />
subspecies of Hypselodoris picta from the<br />
North Atlantic, H. picta webbi from the<br />
Algarve (SW coast of Europe) and H. picta<br />
azorica from Azores, with the aim to clarify:<br />
(1) what are the defensive metabolites<br />
of H. picta azorica; (2) and if the two subspecies<br />
have the same chemical profile.<br />
MATERIALS AND METHODS<br />
Biological material. The molluscs were collected<br />
by SCUBA in two stations:<br />
Hypselodoris picta azorica (6 specimens July<br />
2006, 2 specimens September 2008) at<br />
Ilhéu de Vila Franca do Campo, S. Miguel<br />
Island, Azores, Portugal, and Hypselodoris<br />
picta webbi (2 specimens July 2006, 2 specimens<br />
August 2008) at Portimão, Algarve,<br />
Portugal. The taxonomic identification of<br />
H. picta was made by one of us (G.C.).<br />
Voucher specimens (preserved in<br />
absolute ethanol) are deposited at<br />
“Instituto Português de Malacologia”,<br />
Portugal, reference numbers IPM.MO.005<br />
and IPM.MO.006, respectively.<br />
Chemical analysis. Silica-gel chromatography<br />
was performed using precoated<br />
Merck F 254<br />
plates and Silica gel Merck<br />
Kieselgel 60. 1 H NMR spectra were<br />
acquired in CDCl 3<br />
or C 6<br />
D 6<br />
on a Bruker<br />
AMX-300 operating at 300 MHz.<br />
Two frozen nudibranchs of each subspecies,<br />
collected in 2006, were dissected<br />
and differentiated in mantle dermal formations<br />
(MDFs), the remaining of mantle<br />
and digestive glands. All the dissected<br />
sections were separately extracted three<br />
times with acetone by sonication. The<br />
concentrated extracts were partitioned<br />
between diethyl ether and water. The<br />
resulting diethyl ether extracts were compared<br />
by TLC (Thin Layer Chromatography).<br />
The Erlich positive metabolite,<br />
with R f<br />
= 0.2 in n-hexane, present in<br />
both subspecies, was isolated from the<br />
mantle extract (4 mg) of one specimen of<br />
H. picta webbi (fresh weight 8.3 g). The<br />
mantle extract was chromatographed<br />
on a silica-gel column packed with<br />
n-hexane and eluted with a gradient of<br />
n-hexane/diethyl ether. Fractions eluted<br />
with n-hexane were concentrated to give<br />
2 mg of compound 1 (Figure 1).<br />
FIGURE 2. Live specimens of the Hypselodoris picta studied herein: A - H. p. azorica (photo Peter<br />
Wirtz); B - H p. webbi (photo Rita Coelho).
140 AÇOREANA<br />
2009, Sup. 6: 137-143<br />
We were unable to isolate the main<br />
furanosesquiterpene presented in H. picta<br />
azorica collected in 2006 because, due to<br />
its high instability, it had suffered degra<strong>da</strong>tion<br />
during the isolation procedure.<br />
Each frozen mollusc (4 specimens)<br />
collected in 2008 was separately<br />
immersed in acetone and extracted by<br />
sonication (3 times, 2 min). The concentrated<br />
extracts were partitioned between<br />
diethyl ether and water. The resulting<br />
mantle extracts were compared by TLC<br />
and 1 H NMR analysis.<br />
RESULTS<br />
We have chemically investigated for<br />
the first time the nudibranch Hypselodoris<br />
picta azorica and a population of the nudibranch<br />
Hypselodoris picta webbi from the<br />
NW Atlantic. The TLC analysis of diethyl<br />
ether extracts revealed the presence of at<br />
least two Erlich positive compounds in<br />
both subspecies. H. picta webbi showed<br />
two main Erlich positive metabolites (R f<br />
=<br />
0.2 and 0.3 in n-hexane) and H. picta azorica<br />
additionally showed the presence of<br />
one or two less polar compounds (R f<br />
= 0.7<br />
and 0.8 in n-hexane). Each analysed specimen<br />
showed the same metabolite pattern<br />
in the extracts obtained from the different<br />
anatomic parts. The less polar metabolite<br />
was identified as microcionin-1 (7) by<br />
TLC comparison with an authentic sample<br />
(Figure 1). We were unable to isolate<br />
the furanosesquiterpene with R f<br />
= 0.7, the<br />
main metabolite of H. picta azorica collected<br />
in 2006, due to its instability. The component<br />
with R f<br />
= 0.2, isolated from one<br />
specimen of H. picta webbi collected in<br />
2008, was identified as longifolin (1). The<br />
1<br />
H NMR signals (either in CDCl 3<br />
or C 6<br />
D 6<br />
)<br />
of this metabolite were identical to those<br />
reported in the literature (Guella, 1985).<br />
Longifolin was also identified by NMR as<br />
the main furanosesquiterpene in the mantle<br />
extract obtained from H. picta azorica<br />
collected in 2008 (Figure 3a). The analysis<br />
of 1 H NMR spectrum (Figure 3b) of the<br />
mantle extract from H. picta webbi, collected<br />
in 2008, allowed the identification of<br />
tavacfuran (11), the compound with R f<br />
=<br />
0.3, as the main furanosesquiterpene<br />
(Figure 1). The 1 H NMR signals attributed<br />
to both compounds in the NMR<br />
spectra of mantle extracts (Figure 3) are<br />
similar to those previous reported <strong>da</strong>ta<br />
(Guella, 1985). The results concerning the<br />
furanosesquiterpenes are summarized in<br />
Table 2.<br />
TABLE 2 – Furanosesquiterpenes found in Hypselodoris picta in this study.
GASPAR ET AL: CHEMICAL DEFENCES OF HYPSELODORIS PICTA 141<br />
FIGURE 3. 1 H NMR (300MHz, CDCl 3<br />
) from diethyl ether extracts of Hypselodoris mantle: a)<br />
Hypselodoris picta azorica; b) Hypselodoris picta webbi.<br />
DISCUSSION<br />
In the mantle of Hypselodoris picta azorica<br />
and Hypselodoris picta webbi the<br />
furosesquiterpenes longifolin (1) and<br />
tavacfuran (11) were identified by 1 H<br />
NMR (Figure 3). TLC comparison of the<br />
mantle extracts showed that these typical<br />
sponge metabolites were found in all<br />
analysed specimens but in different relative<br />
proportions (Table 2). Longifolin (1)<br />
has usually been found as the main<br />
metabolite of H. picta from Mediterranean<br />
(Table 1). Tavacfuran (11), a compound<br />
first reported on a mixture of<br />
Mediterranean sponges (Guella, 1985)
142 AÇOREANA<br />
2009, Sup. 6: 137-143<br />
and already isolated from other<br />
Hypselodoris species (Fontana, 1993), was<br />
now found for the first time in H. picta.<br />
The TLC analysis allowed the identification<br />
of microcionin-1 (7) in all the specimens<br />
of H. picta azorica. It is worth noting<br />
that a Mediterranean population of<br />
H. picta is able to transfer microcionin-1<br />
(7) and other sponge metabolites into<br />
MDFs (Fontana, 1994b).<br />
The high concentration of furanosesquiterpenes,<br />
such as longifolin (1)<br />
and tavacpallescencin (11) in the mantle<br />
(including MDFs), suggests that, as in<br />
other Hypselodoris, they play an important<br />
role as defensive metabolites. This<br />
study showed that the chemical profiles<br />
of H. picta azorica and H. picta webbi are<br />
different, as expected, since previous<br />
studies support the idea that most of<br />
these furanosesquiterpene compounds<br />
are accumulated from dietary sources<br />
(Avila, 1991; Fontana, 1994b). However,<br />
the presence of longifolin (1) in H. picta<br />
subspecies living at distant geographical<br />
areas could suggest two different scenaria:<br />
(a) the ability to biosynthesized de<br />
novo this allomone or (b) the ability to<br />
select sponges rich in longifolin (1)<br />
(Avila, 1991; Cimino 1993). Therefore,<br />
the origin of longifolin in H. picta still<br />
remains to be clarified.<br />
ACKNOWLEDGEMENTS<br />
We thank Professor António Frias<br />
Martins for the invitation to participate<br />
in the 3 rd Workshop of Marine Biology,<br />
held in Vila Franca do Campo, where<br />
some of the specimens were collected.<br />
We thank Rita Coelho (IPM) and Lucas<br />
Cervera (University of Cadiz) for collecting<br />
the other specimens. We are<br />
deeply grateful to FCT (VERMEJJ –<br />
PTDC/MAR/65854/2006) for financial<br />
support.<br />
LITERATURE CITED<br />
ALEJANDRINO, A., & Á. VALDÉS, 2006.<br />
Phylogeny and biogeography of the<br />
Atlantic and Eastern Pacific Hypselodoris<br />
Stimpson, 1855 (Nudibranchia,<br />
Chromodoridi<strong>da</strong>e) with the description<br />
of a new species from the<br />
Caribbean Sea. Journal of Molluscan<br />
Studies, 72: 189-198.<br />
AVILA, C., G. CIMINO, A. FONTANA,<br />
M. GAVAGNIN, J. ORTEA & E.<br />
TRIVELLONE, 1991. Defensive Strategy<br />
of two Hypselodoris Nudibranchs<br />
from Italian and Spanish Coasts.<br />
Journal of Chemistry Ecology, 17: 625-<br />
636.<br />
CIMINO, G., S. DE ROSA, S. DE<br />
STEFANO & G. SODANO, 1982. The<br />
Chemical Defense of Four Mediterranean<br />
Nudibranchs. Comparative<br />
Biochemistry and Physiology, 73B: 471-<br />
474.<br />
CIMINO, G., & G. SODANO, 1993.<br />
Biosynthesis of Secon<strong>da</strong>ry Metabolites<br />
in Marine Molluscs. In:<br />
SCHEUER P.J. (ed.), Marine natural<br />
products – diversity and biosynthesis.<br />
Topics in current chemistry vol. 167: 78-<br />
115. Spring-Verlag; Berlin.<br />
CIMINO, G., & M.T. GHISELIN, 1999.<br />
Chemical defense and evolutionary<br />
trends in biosynthetic capacity among<br />
dorid nudibranchs (Mollusca: Gastropo<strong>da</strong>:<br />
Opistobranchia). Chemoecology,<br />
9: 187-307.<br />
FONTANA, A., A. AVILA, E. MARTI-<br />
NEZ, J. ORTEA, E. TRIVELLONE &<br />
G. CIMINO, 1993. Defensive<br />
allomones in three species of<br />
Hypselodoris (Gastropo<strong>da</strong>: Nudibranchia)<br />
from the Cantabrian Sea.<br />
Journal of Chemistry and Ecology, 19:<br />
339-356.<br />
FONTANA, A., E. TRIVELLONE, E.<br />
MOLLO, C. CIMINO, C. AVILA, E.<br />
MARTINEZ & J. ORTEGA, 1994a.
GASPAR ET AL: CHEMICAL DEFENCES OF HYPSELODORIS PICTA 143<br />
Further chemical Studies of Mediterranean<br />
and Atlantic Hypselodoris<br />
nudibranchs: A new furnosesquiterpenoid<br />
from Hypselodoris webbi.<br />
Journal of Naural Products, 57(4): 510-<br />
513.<br />
FONTANA, A., F. GIMÉNEZ, A. MARIN,<br />
E. MOLLO & G. CIMINO, 1994b.<br />
Transfer of secon<strong>da</strong>ry metabolites<br />
from the sponges Dysidea fragilis and<br />
Pleraplysilla spinifera to the mantle dermal<br />
formations (MDFs) of the nudibranch<br />
Hypselodoris webbi. Experientia,<br />
50: 510-516.<br />
GARCÍA-GÓMEZ, J.C., G. CIMINO & A.<br />
MEDINA, 1990. Studies on the defensive<br />
behaviour of Hypselodoris species<br />
(Gastropo<strong>da</strong>: Nudibranchia): ultrastructure<br />
and chemical analysis of<br />
mantle dermal formations (MDFs).<br />
Marine Biology, 106: 245-250.<br />
GUELLA, G., I. MANCINI, A. GUER-<br />
RIERO & F. PIETRA, 1985. New<br />
Furano-sesquiterpenoids from<br />
Meditterranean Sponges. Helv. Chem.<br />
Acta, 68, 1276-1282.<br />
ORTEA, J., A. VALDÉS & J.C. GARCÍA-<br />
GÓMEZ, 1996. Revisión de las<br />
especies atlánticas de la familia<br />
Chromodoridi<strong>da</strong>e (Mollusca: Nudibranchia)<br />
de grupo cromático azul<br />
[Review of the Atlantic species<br />
of the family Chromodoridi<strong>da</strong>e<br />
(Mollusca: Nudibranchia) of the blue<br />
chromatic group]. Avicennia Suppl. 1:<br />
1-165.<br />
WÄGELE, H., M. BALLESTEROS & C.<br />
AVILA, 2006. Defensive Gandular<br />
Structure in opisthobranchs Molluscs<br />
– from histology to ecology. Oceanography<br />
and Marine Biology: An Annual<br />
Review, 44: 197-276.
AÇOREANA, Suplemento 6, Setembro 2009: 145-156<br />
THE BIOLOGY OF THE ZONING SUBTIDAL POLYCHAETE DITRUPA ARIETINA<br />
(SERPULIDAE) IN THE AÇORES, PORTUGAL, WITH A DESCRIPTION OF THE<br />
LIFE HISTORY OF ITS TUBE<br />
Brian Morton & Andreia Salvador<br />
Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, U.K.<br />
e-mail addresses: prof_bmorton@hotmail.co.uk; a.salvador@nhm.ac.uk<br />
ABSTRACT<br />
In the <strong>Açores</strong>, Portugal, the steeply descending continental shelf is characterized at different<br />
depths by two endobenthic suspension feeding species: the shallower-living (0-~100<br />
metres) bivalve Ervilia castanea and the deeper-residing serpulid (~100–250 metres) Ditrupa<br />
arietina. As a dominant member of the continental shelf fauna, D. arietina provides a habitat<br />
for a number of epibiont species that attach to its tubes anteriorly. These include the<br />
cemented, introduced, serpulid Hydroides elegans, three species of foraminiferans and a<br />
number of species of, mostly unidentifiable, bryozoans. Tubes of D. arietina are also drilled<br />
and, hence, pre<strong>da</strong>ted by a prosobranch naticid gastropod, possibly Natica prietoi. Ditrupa<br />
arietina lives for ~2 years with most growth occurring during the first year and with sexual<br />
maturity also occurring in the first year of life so that, post reproduction and death, its<br />
tube becomes available for secon<strong>da</strong>ry colonization by Aspi<strong>dos</strong>iphon muelleri (Sipuncula). At<br />
this time, anterior epibionts die, because the sipunculan orientates the tube anterior end<br />
down, but further epibionts can now colonize the posterior end of the tube. With time and<br />
wear, the tube slowly degenerates. Throughout its life history, therefore, the tube of D. arietina<br />
functions as an inhabitable substratum and is thus a locally important Açorean habitat<br />
for a suite of other epibenthic species.<br />
Ditrupa arietina is herein recognized as a significant component of the continental shelf<br />
endobenthos at depths of ~200 metres, mirroring the significance of the bivalve Ervilia castanea<br />
at generally shallower depths. The ecological importance of these two species is<br />
hence in urgent need of further detailed study, especially with regard to the productivity<br />
of the Açorean seabed.<br />
RESUMO<br />
Nos <strong>Açores</strong>, a plataforma continental que desce abruptamente caracteriza-se, a<br />
diferentes profundi<strong>da</strong>des, por duas espécies endobênticas filtradoras de matérias em<br />
suspensão: o bivalve de pouca profundi<strong>da</strong>de (0-~100 metros) Ervilia castanea e o serpulídeo<br />
de maiores profundi<strong>da</strong>des (~100-250 metros) Ditrupa arietina. Elemento dominante <strong>da</strong><br />
fauna <strong>da</strong> plataforma continental, D. arietina proporciona habitat para uma quanti<strong>da</strong>de de<br />
espécies epibiontes que se fixam ao seu tubo anteriormente. Incluem-se nestes o<br />
serpulídeo fixo Hydroides elegans, três espécies de foraminíferos e uma série de briozoários<br />
na maioria não identificáveis. Os tubos de D. arietina são também perfura<strong>dos</strong> e, por isso,<br />
pre<strong>da</strong><strong>dos</strong> por um gastrópode prosobrânquio naticídeo, provavelmente Natica prietoi.<br />
Ditrupa arietina vive por ~2 anos ocorrendo a maior parte do crescimento durante o<br />
primeiro ano e a maturi<strong>da</strong>de sexual ocorrendo o primeiro ano de vi<strong>da</strong> pelo eu, após a<br />
reprodução e a morte, o seu tubo fica acessível para colonização secundária por<br />
Aspi<strong>dos</strong>iphon muelleri (Sipuncula). Por essa altura, os epibiontes anteriores morrem porque<br />
o sipúnculo orienta para baixo a extremi<strong>da</strong>de anterior do tubo, mas outros epibiontes<br />
podem agora colonizar a extremi<strong>da</strong>de posterior do tubo. Com o tempo e uso, o tubo<br />
degenera lentamente. Durante a sua história de via, assim, o tubo de D. arietina funciona<br />
como substrato habitável e é, por isso, um habitat Açoriano localmente importante para<br />
uma série de outras espécies.
146 AÇOREANA<br />
2009, Sup. 6: 145-156<br />
Como componente significativo do endobentos <strong>da</strong> plataforma continental a<br />
profundi<strong>da</strong>des abaixo de ~200 metros, espelhando o significado do bivalve Ervilia castanea<br />
em profundi<strong>da</strong>des geralmente menores, a importância ecológica destas duas espécies<br />
necessita estudo ulterior pormenorizado, especialmente no que respeita a produtivi<strong>da</strong>de<br />
do fundo marinho Açoriano.<br />
INTRODUCTION<br />
Morton & Britton (1995, table 1)<br />
showed that offshore from Vila<br />
Franca do Campo, São Miguel, <strong>Açores</strong>,<br />
the abun<strong>da</strong>nces of members of the<br />
benthic community were consistent, save<br />
for Ditrupa arietina (O.F. Müller, 1776)<br />
whose numbers differed significantly<br />
between stations. These authors also<br />
noted that empty tubes of D. arietina were<br />
occupied by the sipunculan Aspi<strong>dos</strong>iphon<br />
muelleri Diesing, 1851, but not by the<br />
hermit crab Anapagurus laevis (Bell, 1845).<br />
It is known that many species of tubebuilding<br />
polychaetes form dense aggregations<br />
or “patches” within marine softbottom<br />
habitats (Bolam & Fernandes,<br />
2002) although in the Bay of Blanes<br />
(northwest Mediterranean), Ditrupa arietina<br />
showed seasonal peaks of abun<strong>da</strong>nce<br />
in May and June of 1993, 1994 and 1995<br />
(Sardá et al., 1999). Similarly, since the<br />
late 1980’s, D. arietina has increased in<br />
abun<strong>da</strong>nce all along the northwest coast<br />
of the Mediterranean, numbers reaching<br />
up to 3,000 individuals·m² and adversely<br />
affecting the functioning of the coastal<br />
benthic ecosystem in the region (Gremare<br />
et al., 1998a, b).<br />
The strictly dioecious serpulid Ditrupa<br />
arietina has a reproductive period lasting<br />
from November to May in the bay of<br />
Banyuls-sur-Mer in the northwestern<br />
Mediterranean, with recruitment beginning<br />
as early as January and ending in<br />
July but with a peak in April-May<br />
(Charles et al., 2003) explaining the observation<br />
by Sardá et al. (1999) of a peak in<br />
seasonal abun<strong>da</strong>nce between May-June in<br />
the same region. The planktonic life is ~3<br />
weeks long with metamorphosis being<br />
completed quickly post-settlement<br />
(Charles et al., 2003). Ditrupa arietina lives<br />
for ~2 years, with most growth and sexual<br />
maturity being achieved during the<br />
first year (Medernach et al., 2000).<br />
Hence, although much is known<br />
about the biology of Ditrupa arietina in the<br />
Mediterranean, there is nothing known<br />
about it in the <strong>Açores</strong>, Portugal, save for<br />
the paper by Morton & Britton (1995)<br />
mentioned above. Morton & Britton<br />
(2000) also showed that the marine flora<br />
and fauna of the <strong>Açores</strong> have the<br />
strongest biogeographic links with the<br />
Mediterranean. The aim of the present<br />
paper was thus to determine if, as in the<br />
Mediterranean, D. arietina occupied a particular<br />
and similar depth zone. We also<br />
wished to investigate if there were any<br />
depth distributions in the <strong>Açores</strong> between<br />
living individuals of D. arietina and the<br />
empty tubes occupied by Aspi<strong>dos</strong>iphon<br />
muelleri. Finally, it is known that in the<br />
Mediterranean, tubes of D. arietina, both<br />
occupied and unoccupied, are colonized<br />
by an encrusting fauna the major components<br />
of which are bryozoans (Gambi &<br />
Jerace, 1997). We wanted to see if this<br />
associated fauna was replicated in the<br />
<strong>Açores</strong>, or would it be, as with other taxa,<br />
much reduced (Morton & Britton, 2000).<br />
Finally, we wanted to determine if the<br />
tube of D. arietina had a life history, once<br />
the animal that had secreted it died. That<br />
is, it is known that the tube becomes occupied<br />
by Aspi<strong>dos</strong>iphon muelleri (Morton &<br />
Britton, 2000), but what is the complete<br />
life history of the tube?
MORTON & SALVADOR: THE BIOLOGY OF DITRUPA ARIETINA 147<br />
TAXONOMIC NOTE<br />
Most authors, for example, Nelson-<br />
Smith & Gee (1966), follow Fauvel (1953)<br />
and recognize a single, worldwide,<br />
species of Ditrupa, that is, D. arietina (O.F.<br />
Müller, 1776). ten Hove & Smith (1990),<br />
however, justified the recognition of a<br />
separate species, D. gracillima Grube,<br />
1878, from the Indo-Pacific and deep<br />
water ecophenotypes of which had previously<br />
been identified as D. arietina var.<br />
monilifera.<br />
MATERIALS AND METHODS<br />
For eleven <strong>da</strong>ys from 17 - 28 July 2006,<br />
the sea bed on the southern coast of the<br />
island of São Miguel, <strong>Açores</strong>, was sampled<br />
using a benthic box dredge at six stations<br />
to the east and west of the islet of<br />
Ilhéu de Vila Franca do Campo. The stations<br />
were designated E1, E2, E3 and W1,<br />
W2 and W3 and located at approximate<br />
depths of 100 (E1 and W1), 200 (E2 and<br />
W2) and 250 metres (E3 and W3) (Figure<br />
1). The reader is referred to Martins et al.<br />
FIGURE 1. A map of the southern coast of São Miguel Island, showing the six sampling sites to<br />
the east (E1- E3) and west (W1 - W3) of Ilhéu de Vila Franca do Campo.
148 AÇOREANA<br />
2009, Sup. 6: 145-156<br />
(2009) for a full description of the stations<br />
and their accurate locations. Dredges<br />
were towed at a stan<strong>da</strong>rd speed (5 knots)<br />
for ten minutes and on reaching the surface<br />
sieved using seawater through a 1<br />
mm mesh sieve.<br />
Two 500 ml sub-samples of sediment<br />
were removed from each dredge sample<br />
and sorted using dissecting binocular<br />
microscopes. All living individuals of<br />
Ditrupa arietina were collected from the<br />
first sample and the lengths of their tubes<br />
measured to the nearest 1 mm using a dissecting<br />
microscope (x10) with a 1 mm<br />
graduated scale. From these <strong>da</strong>ta, it has<br />
been possible to construct histograms of<br />
the population structure of D. arietina at<br />
the six sampling locations (Figure 2). The<br />
living individuals were also used in simple<br />
studies of burrowing behaviour.<br />
All empty tubes and fragments of<br />
Ditrupa arietina were removed from the<br />
second sample and measured along their<br />
greatest lengths to the nearest 1 mm using<br />
a dissecting microscope (x10) with a graduated<br />
scale. Each tube and fragment was<br />
then examined and divided into categories.<br />
These were: (i), those individuals<br />
occupied by Aspi<strong>dos</strong>iphon muelleri; (ii),<br />
those with either anterior or posterior<br />
encrustations of attached biota and (iii),<br />
those with a drill hole. Some D. arietina<br />
tubes that had drill holes were also occupied<br />
by A. muelleri and had epibiont<br />
encrustations. Such individuals were<br />
placed in their own sub-categories.<br />
Data analysis<br />
One-factor analysis of variance<br />
(ANOVA) on untransformed <strong>da</strong>ta with a<br />
statistical significance criterion set at p =<br />
0.05 was conducted as the statistical technique<br />
used to examine for any differences<br />
in the <strong>da</strong>tasets between the six sampling<br />
stations and hence depth. Any significant<br />
results obtained by the ANOVA were dif-<br />
FIGURE 2. Histograms showing the length frequency distribution of living Ditrupa arietina individuals<br />
at the six stations to the east (E1 - E3) and west (W1 - W3) of Ilhéu de Vila Franca do<br />
Campo, São Miguel, <strong>Açores</strong>.
MORTON & SALVADOR: THE BIOLOGY OF DITRUPA ARIETINA 149<br />
ferentiated using a post-hoc Student’s<br />
Newman-Kuels (SNK) test to identify<br />
where the detected differences lay (Zar,<br />
1984). The <strong>da</strong>ta were analyzed using SAS<br />
(Version 9.1.3).<br />
RESULTS<br />
Statistical analyses<br />
Figure 2 are histograms showing the<br />
length frequency distribution of living<br />
Ditrupa arietina individuals at the six stations<br />
to the east (E1 - E3) and west (W1 -<br />
W3) of Ilhéu de Vila Franca do Campo,<br />
São Miguel, <strong>Açores</strong>. The results of a oneway<br />
ANOVA on these living individuals<br />
of D. arietina collected from the three sampling<br />
depths were significantly different<br />
(F=68.55; p=0.0031). The results of a posthoc<br />
Student’s Newman-Keuls test further<br />
indicated that the numbers of living individuals<br />
were significantly higher (p>0.05)<br />
at both the east (E2) and west (W2) ~200<br />
metre depth stations.<br />
Figure 3 are histograms showing the<br />
length frequency distributions of all tubes<br />
no longer occupied by Ditrupa arietina<br />
and, at the six stations to the east (E1 - E3)<br />
and west (W1 - W3) of Ilhéu de Vila<br />
Franca do Campo, São Miguel, <strong>Açores</strong>.<br />
The results of a second one-way ANOVA<br />
on the <strong>da</strong>taset indicated that there was no<br />
significant difference in the total numbers<br />
of Ditrupa arietina tubes collected at the<br />
sample depths of ~100, ~200 and ~250<br />
metres (F=0.36; p=0.7250). Similarly, there<br />
were no significant differences between<br />
stations and depths in the incidences of<br />
tubes that (i), were occupied by<br />
Aspi<strong>dos</strong>iphon muelleri; (ii), possessed<br />
encrusting bryozoans and other attached<br />
organisms either anteriorly or posteriorly,<br />
nor (iii), in the incidences of pre<strong>da</strong>ted,<br />
that is, drilled tubes. A more detailed<br />
study of the drill holes in the tubes D.<br />
arietina is reported upon by Morton &<br />
Harper (2009).<br />
Behaviour<br />
When living individuals of Ditrupa<br />
arietina and tubes occupied by<br />
Aspi<strong>dos</strong>iphon muelleri were placed on the<br />
surface of samples of natural sediment<br />
obtained in the dredges, they both<br />
FIGURE 3. Histograms showing the length frequency distributions of all Ditrupa arietina tubes<br />
either empty or occupied by Aspi<strong>dos</strong>iphon muelleri (plus tube fragments) at the six stations to the<br />
east (E1 - E3) and west (W1 - W3) of Ilhéu de Vila Franca do Campo, São Miguel, <strong>Açores</strong>.
150 AÇOREANA<br />
2009, Sup. 6: 145-156<br />
attempted to re-burrow. Ditrupa arietina<br />
burrowed with the posterior end of the<br />
tube down, so that the serpulid’s crown of<br />
tentacles projected above the sediment<br />
surface. Conversely, A. muelleri burrowed<br />
anterior end down so that its head was<br />
within the sediment.<br />
Epibionts<br />
Table 1 gives a list of the epibionts collected<br />
and identified from the tubes of<br />
Ditrupa arietina. The most obvious<br />
epibiont was the cemented serpulid<br />
Hydroides elegans (Haswell, 1883) that has<br />
probably been introduced into Açorean<br />
waters in historical times, possibly<br />
attached to boats or in ballast waters<br />
(Morton & Britton, 2000). Other epibionts<br />
included three species of foraminiferans,<br />
that is, the bright red Miniacina miniacea<br />
Pallas, 1776, Cassidulina obtusa<br />
Williamson, 1858 and Elphidium crispum<br />
(Linnaeus, 1767), and a number of<br />
species, mostly unidentifiable, of bryozoans.<br />
Also present were the egg capsules<br />
of gastropods (all unidentifiable).<br />
All the species identified in Table 1 have a<br />
north-eastern Atlantic/Mediterranean distribution,<br />
except for M. miniacea which<br />
occurs in the warmer central Atlantic<br />
from the Mediterranean to the Caribbean.<br />
Life history of the Ditrupa arietina tube<br />
The suggested life history of the tube<br />
of Ditrupa arietina is illustrated in Figure<br />
4. A living individual of D. arietina is<br />
illustrated in Figure 4A. The tube is cylindrical,<br />
slightly curved and resembles an<br />
elephant’s tusk or, more appropriately, a<br />
scaphopod, and anteriorly swollen<br />
although the mouth typically narrows<br />
again at its anterior extremity. There are<br />
numerous constrictions, or flanges, to the<br />
shell that is also variably patterned with<br />
circlets of orange-brown pigmentation.<br />
Because the contained worm is bright red,<br />
the tubes of living individuals are also<br />
redder than their empty counterparts.<br />
The 19 branchial filaments are also bright<br />
red (sometimes red banded) and the operculum<br />
is a membranous cup or funnel<br />
closed distally by a flat, brownish, chiti-<br />
TABLE 1. A list of encrusting species herein recorded as attached to the tubes of Ditrupa arietina<br />
from the six stations to the east (E1 - E3) and west (W1 - W3) of Ilhéu de Vila Franca do Campo.<br />
São Miguel, <strong>Açores</strong>.<br />
Phylum Species Notes<br />
Foraminifera Miniacina miniacea Pallas, 1776 Mediterranean, Caribbean (down to 2000 metres)<br />
Cassidulina obtusa Williamson, Northern Europe, Mediterranean, Canaries<br />
1858<br />
Elphidium crispum (Linnaeus, Mediterranean, Gulf of Cadiz, West Africa<br />
1767)<br />
Gymnolaemata: Celleporina hassalli (Johnston, British Isles<br />
Cheilostomata 1847)<br />
Cheilostoma 1<br />
Cheilostoma 2<br />
Stenolaemata: Crisia cf. eburnea (Linnaeus, Northern Europe, British Isles<br />
Cyclostomata 1758)<br />
Tervia irregularis (Meneghini, Northern Europe, Mediterranean<br />
1844)<br />
Disporella spp.<br />
Cyclostome 1<br />
Cyclostome 2<br />
Cyclostome 3<br />
Polychaeta: Hydroides elegans (Haswell, Near cosmopolitan; unintentionally introduced (Morton<br />
Serpuli<strong>da</strong>e 1883)<br />
& Britton, 2000)
MORTON & SALVADOR: THE BIOLOGY OF DITRUPA ARIETINA 151<br />
FIGURE 4. Ditrupa arietina. A, A living individual in its tube and (A¹) in its life position in the sediment;<br />
B, the anterior end of a tube with encrusting organisms; C, a drill hole (probably) made by<br />
the naticid Natica prietoi; D, an empty, drilled and anteriorly encrusted, tube occupied by<br />
Aspi<strong>dos</strong>iphon muelleri and (D¹) in its life position in the sediment; E, an anteriorly encrusted tube<br />
occupied by A. muelleri; F, a fragment of unoccupied tube colonized by encrusting organisms and<br />
F, a fragment of tube.
152 AÇOREANA<br />
2009, Sup. 6: 145-156<br />
nous plate thickened in the centre to form<br />
a boss. Living individuals of D. arietina<br />
(Figure 4, A¹) live in the sediment, posterior<br />
end down and with the swollen anterior<br />
end situated above the surface. The<br />
anterior end of the tube is often encrusted<br />
with epibionts (Figure 4, B). Figure 4C<br />
illustrates a drill hole probably made by<br />
the naticid Natica prietoi Hi<strong>da</strong>lgo, 1873<br />
(see Morton & Harper, 2009). Following<br />
death, the tube of D. arietina is occupied<br />
by Aspi<strong>dos</strong>iphon muelleri (Figure 4D) at<br />
which time the anterior epibionts also die<br />
because the sipunculan lives head down<br />
in the sediment (illustrated in Figure 4<br />
[D¹]). With the posterior end of the tube<br />
now projecting above the sediment surface,<br />
it becomes encrusted by epibionts<br />
(Figure 4E), such that the tube becomes<br />
more eroded with age (Figure 4F) until<br />
only fragments remain (Figure 4G). As<br />
noted above we could obtain no statistically<br />
different station and hence depth<br />
distributions in the various categories of<br />
D. arietina tubes either occupied by A<br />
muelleri or encrusted either anteriorly or<br />
posteriorly. It thus seems that upon the<br />
death of D. arietina, its tube becomes<br />
widely distributed throughout the<br />
Açorean offshore seabed, probably by<br />
water movements acting upon it.<br />
DISCUSSION<br />
Labrune et al. (2007) analyzed the softbottom<br />
polychaete assemblages of the<br />
Gulf of Lions in the northwest<br />
Mediterranean and showed that at virtually<br />
stations associated with “littoral” fine<br />
muds and with depths of between 10–20<br />
metres the fauna was characterized by<br />
high abun<strong>da</strong>nces and high biomasses due<br />
to the presence of large numbers of<br />
Ditrupa arietina. Similarly, Cosentino &<br />
Giacobbe (2006) showed that, also in the<br />
Mediterranean, maximum mollusc/polychaete<br />
diversities (H’) occurred at depths<br />
of between 10–20 metres but that this<br />
decreased beyond this corresponding to<br />
the peak in the core population of D. arietina<br />
at depths of between 30-40 metres<br />
and abun<strong>da</strong>nces of >500 individuals·250·cm².<br />
Sardá et al. (2000) demonstrated<br />
that following sand extraction at<br />
depths of between 10–30 metres in the<br />
Tordera River, Bay of Blanes in the northwest<br />
Mediterranean, numbers of D. arietina<br />
initially remained stable, but numbers<br />
rose sharply during the following spring<br />
and autumn possibly due to re-colonization<br />
of the dredged sea bed.<br />
In May, that is, spring, coinciding with<br />
the periods of greatest abun<strong>da</strong>nces,<br />
growth and reproductive period in<br />
Ditrupa arietina, individuals spent only<br />
25% of the time feeding compared with<br />
50% of the time during the rest of the year<br />
(Jor<strong>da</strong>na et al., 2000). The size spectrum<br />
of particles filtered by D. arietina was<br />
rather large and ranged between 1µm-<br />
50µm with planktonic and benthic<br />
diatoms, haptophytes, bacteria and<br />
cyanobacteria being collected and<br />
absorbed at efficiencies of 84.7, 70.9, 72.3<br />
and 63.7%, respectively (Jor<strong>da</strong>na et al.,<br />
2001a). Ditrupa arietina selectively filters<br />
picoplankton this accounting for, on a<br />
yearly basis, 15% of ingested chlorophylla<br />
with 95% of this figure being accounted<br />
for by picoeukaryotes (Jor<strong>da</strong>na et al.,<br />
2001b). The maximum weight specific<br />
clearance rate for D. arietina was 15.7<br />
ml.hour¯¹·mg·¯¹, about seven times less<br />
than for the polychaete Euchone papillosa<br />
(M. Sars, 1851), because of the latter’s relatively<br />
larger tentacle crown (Riisgård et<br />
al. 2002).<br />
From the above research in the<br />
Mediterranean, two important facts<br />
emerge that have relevance to Ditrupa arietina<br />
in the <strong>Açores</strong>. First, that D. arietina<br />
occurs at a relatively shallow depth of<br />
between 10-30 metres and, second, being<br />
a benthic suspension feeder it assists in
MORTON & SALVADOR: THE BIOLOGY OF DITRUPA ARIETINA 153<br />
the clarification of the water column especially<br />
when the species occurs in large<br />
numbers. This study demonstrates that<br />
in the <strong>Açores</strong>, D. arietina occurs at a depth<br />
of ~ 200 metres. This distinctive difference<br />
in depths may be related to light,<br />
that is, in the <strong>Açores</strong>, oceanic waters allow<br />
colonization to a greater depth than in the<br />
(recently) more turbid Mediterranean.<br />
Or, such a difference may be related to<br />
food availability in the form of picoplankton<br />
that D. arietina feeds on, since this is<br />
likely to be less abun<strong>da</strong>nt in the <strong>Açores</strong>,<br />
thereby, somehow, influencing depth<br />
preference. It is also possible that the two<br />
factors may be acting synergistically in<br />
the <strong>Açores</strong> and/or in concert with other<br />
factors such as sediment grain size and<br />
disturbance.<br />
Morton (1990) studied the bivalve<br />
Ervilia castanea (Montagu, 1803) collected<br />
offshore from Vila Franca do Campo, São<br />
Miguel, and recorded it from depths of<br />
between 0-40 metres although the species<br />
is known to occur from ~800-1800 metres<br />
in the <strong>Açores</strong> and 130 metres in the<br />
Canary Islands (Smith, 1885), but possibly<br />
only as empty shells. This study of<br />
Ditrupa arietina collected few living E. castanea<br />
from the depths sampled, but many<br />
empty valves. Hence, in the <strong>Açores</strong>, the<br />
deeply shelving continental shelf (Figure<br />
1), appears to be characterized at two<br />
depths by two endobenthic suspension<br />
feeding species: the shallower living (0-<br />
~100 metres) bivalve Ervilia castanea and<br />
the deeper residing serpulid (~100 –250<br />
metres) D. arietina.<br />
Gambi et al. (1996) analyzed polychaete<br />
community structure at 32 stations<br />
distributed from 2–105 metres depth in<br />
the southern Tyrrhenian Sea (Italy) and<br />
showed that Ditrupa arietina was dominant<br />
at depths of between 26-30 metres<br />
and enhanced the spatial complexity,<br />
species composition and diversity and<br />
community structure of the habitat by<br />
virtue of the range of diversity of<br />
epibionts attached to its tube. Gambi &<br />
Jerace (1997) analyzed the epibionts on D.<br />
arietina tubes from three bays in the<br />
southern Tyrrhenian Sea and identified a<br />
wide range of species, including<br />
foraminiferans, sponges, hydroids, bryozoans<br />
and tubiculous polychaetes.<br />
Epibiosis percentages varied from site to<br />
site and between years. This study of the<br />
epibionts attached to the tubes of D. arietina<br />
identified a number of species<br />
including, most dominantly, the cemented<br />
serpulid Hydroides elegans (Haswell,<br />
1883). Other epibionts included three<br />
species of foraminiferans and a number of<br />
species of bryozoans.<br />
The only pre<strong>da</strong>ted tubes of Ditrupa<br />
arietina that could be identified in this<br />
study appeared to have been drilled by<br />
the prosobranch naticid gastropod Natica<br />
prietoi (see Morton & Harper, 2009).<br />
Ditrupa arietina lives for ~2 years<br />
(Medernach et al., 2000), with most<br />
growth occurring during the first year.<br />
As Morton & Harper (2009) show, tubes<br />
of many sizes are attacked by the naticid<br />
although, generally, larger ones were<br />
favoured. Such a generalization is probably<br />
related to the relationship between<br />
pre<strong>da</strong>tor and prey sizes, but if it is true<br />
that larger individuals are generally preferred<br />
by N. prietoi, then clearly, these are<br />
adults, sexual maturity also occurring in<br />
the first year of life (Medernach et al.,<br />
2000), so that post reproduction the tube<br />
becomes available for colonization by<br />
Aspi<strong>dos</strong>iphon muelleri, anterior epibionts<br />
then die, but further epibiotic organisms<br />
can now colonize the posterior end of the<br />
tube and slowly the tube degenerates.<br />
Subsequent to the death of the original<br />
inhabitant, the tube of Ditrupa arietina<br />
provides secon<strong>da</strong>ry accommo<strong>da</strong>tion for<br />
Aspi<strong>dos</strong>iphon muelleri and throughout its<br />
life history it functions as an inhabitable<br />
substratum and hence a locally important
154 AÇOREANA<br />
2009, Sup. 6: 145-156<br />
Açorean habitat for a suite of epibionts. It<br />
is also apparent that D. arietina is an overwhelmingly<br />
dominant and therefore highly<br />
significant component of the Açorean<br />
endobenthos at depths of ~200 metres,<br />
mirroring the significance of the bivalve<br />
Ervilia castanea at generally shallower<br />
depths (Morton, 1990). It is finally clear, as<br />
this study now suggests, that the ecological<br />
significance of these two species is in<br />
urgent need of further, much more<br />
detailed study, especially with regard to<br />
their role in the productivity of the inshore<br />
Açorean continental shelf seabed.<br />
ACKNOWLEDGEMENTS<br />
The authors are grateful to Prof. A.M.<br />
Frias Martins (University of the <strong>Açores</strong>) for<br />
funding this research and for much practical<br />
help and warm hospitality during their<br />
stay on São Miguel. We are also grateful to<br />
a number of University of the <strong>Açores</strong> students<br />
who helped with sample sorting and<br />
to Dr. K.F. Leung (Environmental<br />
Protection Department, Hong Kong SAR<br />
Government, China) for statistical advice<br />
and help. Mary Spencer Jones (Natural<br />
History Museum, London) is thanked for<br />
identifying the bryozoans.<br />
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AÇOREANA, Suplemento 6, Setembro 2009: 157-165<br />
DRILLING PREDATION UPON DITRUPA ARIETINA (POLYCHAETA:<br />
SERPULIDAE) FROM THE MID-ATLANTIC AÇORES, PORTUGAL<br />
Brian Morton & E.M. Harper<br />
Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK. E-mail:<br />
prof_bmorton@hotmail.co.uk<br />
Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EQ, UK. E-mail:<br />
emh21@cam.ac.uk<br />
ABSTRACT<br />
A small, but significant proportion of the empty tubes of the free-living serpulid<br />
Ditrupa arietina dredged from the seabed off São Miguel, <strong>Açores</strong>, were punctured by small<br />
round holes. Analysis of these holes shows that they are typically single, made from the<br />
outside of the tube and located preferentially, suggesting that they represent the work of<br />
a pre<strong>da</strong>tor. The likely identity of the pre<strong>da</strong>tor is discussed but based on the co-occurrence<br />
in the dredges and the fact that most of the holes have a distinctive countersunk morphology,<br />
it is suggested that they were made by the small naticid Natica prietoi. If so, this<br />
study is the first record of such a pre<strong>da</strong>tor/prey relationship.<br />
RESUMO<br />
Uma pequena mas significativa porção de tubos do serpulídeo livre Ditrupa arietina<br />
draga<strong>dos</strong> do fundo marinho ao largo de São Miguel, <strong>Açores</strong>, estavam perfura<strong>dos</strong> por<br />
pequenos orifícios redon<strong>dos</strong>. Análise desses orifícios mostra que eles são tipicamente<br />
singulares, feito a partir do exterior do tubo e localiza<strong>dos</strong> preferencialmente, sugerindo<br />
que representam o trabalho de um pre<strong>da</strong>dor. Discute-se a identi<strong>da</strong>de provável do<br />
pre<strong>da</strong>dor mas, com base na co-ocorrência nas dragagens e no facto de que a maioria <strong>dos</strong><br />
orifícios possui uma distinta morfologia chanfra<strong>da</strong>, sugere-se que foram feitos pelo<br />
pequeno naticídeo Natica prietoi. Assim sendo, este estudo é o primeiro registo de tal<br />
relação pre<strong>da</strong>dor/presa.<br />
INTRODUCTION<br />
Although polychaete worms are a<br />
major source of food for a number of<br />
pre<strong>da</strong>tory taxa including fish, gastropods<br />
and birds, most of our knowledge is<br />
focused on pre<strong>da</strong>tion of the larger errant<br />
taxa. For example, amongst the pre<strong>da</strong>tory<br />
gastropods, representatives of the<br />
Murici<strong>da</strong>e, Columbelli<strong>da</strong>e, Fasciolarii<strong>da</strong>e,<br />
Vasi<strong>da</strong>e and Buccini<strong>da</strong>e as well as many<br />
conoideans are specialist worm pre<strong>da</strong>tors<br />
(Pearce & Thorson, 1967; Taylor, 1978a, b,<br />
1980; Taylor et al., 1980; Shimek, 1984;<br />
Taylor & Lewis, 1995). Similarly, many<br />
wading birds are specialist pre<strong>da</strong>tors<br />
upon interti<strong>da</strong>l endobenthic polychaetes<br />
(Goss-Custard, 1975).<br />
In contrast, little appears to be known<br />
about pre<strong>da</strong>tory activities upon the tubedwelling<br />
Serpuli<strong>da</strong>e (Polychaeta) despite<br />
their cosmopolitan occurrence and frequently<br />
high abun<strong>da</strong>nce. There is, however,<br />
observational evidence that gastropods<br />
(Taylor & Morton, 1996; Tan &<br />
Morton, 1998), fish (Bosence, 1979;<br />
Witman & Cooper, 1983) and crustaceans<br />
(Bosence, 1979) feed on serpulids and, in<br />
the case of the buccinid gastropod Engina<br />
armillata (Reeve, 1846) in Hong Kong,<br />
they are its prey of choice (Tan & Morton,<br />
1998). Additionally, the development of<br />
calcareous tubes, a well-developed<br />
“fright response” (Poloczanska et al.,<br />
2004) and, in the case of encrusting<br />
species, an often cryptic habit suggest
158 AÇOREANA<br />
2009, Sup. 6: 157-165<br />
that the evolution of the Serpuli<strong>da</strong>e may<br />
have been influenced by pre<strong>da</strong>tion pressure.<br />
Part of the problem in recognising<br />
pre<strong>da</strong>tory activity on serpulid worms<br />
undoubtedly results from their typically<br />
cryptic lifestyles that make direct observations<br />
difficult. Indirect methods to<br />
detect pre<strong>da</strong>tory activity on serpulids<br />
must rely on analyses of the pre<strong>da</strong>tor’s<br />
gut contents to recognise setae (Taylor &<br />
Morton, 1996) or the identification of any<br />
characteristic <strong>da</strong>mage to the tube caused<br />
by a pre<strong>da</strong>tor, although for many pre<strong>da</strong>tors,<br />
for example E. armillata, which was<br />
recorded feeding via the prey’s aperture<br />
(Tan & Morton, 1998), no such characteristic<br />
<strong>da</strong>mage results.<br />
In this paper we describe drill holes<br />
made in the tube of the endobenthic serpulid<br />
Ditrupa arietina (Müller, 1776) from<br />
the subti<strong>da</strong>l seabed off the island of São<br />
Miguel in the <strong>Açores</strong> (Portugal). We present<br />
evidence that these are the result of<br />
pre<strong>da</strong>tion and further discuss evidence<br />
as to the likely culprit(s).<br />
Ditrupa arietina (Müller, 1776)<br />
Ditrupa arietina is a widespread<br />
endobenthic serpulid worm, common in<br />
the Mediterranean where it achieves<br />
high densities and there is evidence in<br />
some areas that its abun<strong>da</strong>nce is increasing<br />
(Gremare et al., 1998a, b; Bolam &<br />
Fernandes, 2002; Labrune et al., 2007).<br />
The worm secretes a curved, tuskshaped,<br />
calcareous tube up to 23 mm<br />
long and about 3 mm across at its widest<br />
point. It lives within the sediment, the<br />
narrowest posterior end down, with an<br />
anterior bulge (about 10% of the tube)<br />
exposed above the substratum. This<br />
anterior bulge houses the circlet of twenty<br />
feeding tentacles when they are<br />
retracted and the anterior aperture is<br />
sealed by a further tentacle bearing an<br />
operculum. Morton & Salvador (2009,<br />
figure 4) illustrate a living D. arietina in<br />
its life position in the sediment.<br />
The species has been recorded as a<br />
dominant member of soft-bottom communities<br />
at depths of 100–250 metres in<br />
the <strong>Açores</strong> where the tubes of dead individuals<br />
also provide domiciles for the<br />
sipunculan worm Aspidopsiphon muelleri<br />
Diesing, 1851 (Morton & Britton, 1995;<br />
Morton & Salvador, 2009).<br />
MATERIALS AND METHODS<br />
During July 2006, large numbers of<br />
the serpulid polychaete Ditrupa arietina<br />
were collected from depths of between<br />
50-200 metres off Vila Franca do Campo,<br />
São Miguel, <strong>Açores</strong>. The samples were<br />
collected and processed as reported in<br />
Morton & Salvador (2009). Following initial<br />
observations that some tubes were<br />
perforated by drill holes, the tubes of<br />
dead individuals were separated and<br />
inspected for evidence of such drilling.<br />
For each holed tube, the following <strong>da</strong>ta<br />
were collected: tube length to the nearest<br />
1 mm using vernier callipers, number of<br />
drillholes per tube and the morphology of<br />
the drillhole. Further observations were<br />
made on the morphology of the drillholes<br />
of a small number of specimens by scanning<br />
electron microscopy (SEM). These<br />
specimens were prepared by cleaning in<br />
an ultrasonic bath prior to mounting<br />
them, coated in gold, for SEM (JEOL 820 –<br />
University of Cambridge).<br />
Finally, the mean tube lengths plus<br />
stan<strong>da</strong>rd deviations of intact living individuals<br />
of Ditrupa arientina and those<br />
with drill holes were compared using a<br />
t-test.<br />
RESULTS<br />
Holed individuals of Ditrupa arietina<br />
were identified from each of the six sampling<br />
stations, described by Martins et al.
MORTON & HARPER: DRILLING PREDATION UPON DITRUPA ARIETINA 159<br />
(2009), but no significant differences in<br />
numbers were obtained between them<br />
with regard to the incidence of drilled<br />
tubes (see Morton & Salvador, 2009 for<br />
details). In total 5,453 tubes of D. arietina<br />
were retrieved and examined and from<br />
which we identified 104 fragments and<br />
intact empty tubes with holes in them,<br />
that is, approximately 1.9% of all empty<br />
tubes examined. The vast majority of the<br />
tubes were perforated by a single drillhole<br />
but a few had two or even three complete<br />
holes. No incomplete holes were<br />
observed nor any that showed signs of<br />
repair or healing by the occupant. All<br />
were drilled perpendicular to the surface<br />
of the tube and were clearly produced<br />
from the outside, as evidenced by a wider<br />
outer diameter.<br />
All holes in the tubes of Ditrupa arietina<br />
were small, with an outer diameter of<br />
less than 700 µm. In outline, the perforations<br />
were mostly circular (Figure 1A, B)<br />
but a few were more elliptical (Figure 1C).<br />
The outer edges of the drillholes were<br />
clearly defined, and SEM observations of<br />
the surface of the tube adjacent to the hole<br />
show no obvious signs of either dissolution<br />
or rasping. The inner perforations<br />
were rather more ragged and smaller<br />
than the outer diameter. Most of the holes<br />
we have examined had curved walls leading<br />
to a countersunk morphology,<br />
although some (Figure 1D) were more<br />
straight-sided.<br />
The positions of drill holes in the<br />
tubes of Ditrupa arietina are shown in<br />
Figure 2. It is clear that most are located<br />
in the mid portion of the tube, below the<br />
anterior bulge. Although they occur all<br />
around the circumference of the tube, the<br />
distribution of the holes is not uniform,<br />
there being a clear preference for the concave<br />
aspect.<br />
The length distributions of a sub-sample<br />
(n = 376) of living Ditrupa arietina<br />
recorded by Morton & Salvador (2009) are<br />
FIGURE 1. Scanning electron micrographs of a<br />
variety of drill holes in the tubes of Ditrupa arietina<br />
collected from the seabed offshore from<br />
Vila Franca do Campo, São Miguel, <strong>Açores</strong>, in<br />
2006. Scale bars represent 100 µm for A and B<br />
and 200 µm C and D.<br />
FIGURE 2. Histograms showing the size distributions<br />
(tube lengths) of living (white) and<br />
drilled (black) individuals of Ditrupa arietina<br />
collected from the seabed offshore from Vila<br />
Franca do Campo, São Miguel, <strong>Açores</strong>, in 2006.<br />
plotted together with the same <strong>da</strong>ta for<br />
drilled individuals in Figure 3. Although<br />
virtually all sizes of D. arietina tubes were<br />
drilled (from 5-21 mm tube lengths), the<br />
mean length of the drilled D. arietina
160 AÇOREANA<br />
2009, Sup. 6: 157-165<br />
tubes (n = 102) was 12.7 (S.D. 4.3) whereas<br />
that of the tubes occupied by living D.<br />
arietina (n = 378) was 14.9 (S.D. 2.8). The<br />
result of the t-test showed that the means<br />
of the two samples were significantly different<br />
(p =
MORTON & HARPER: DRILLING PREDATION UPON DITRUPA ARIETINA 161<br />
support of this contention, no marginellids<br />
are reported from the Açorean fauna<br />
and the trawls in which the drilled D. arietina<br />
were collected contained a number<br />
of individuals of Natica prietoi Hi<strong>da</strong>lgo,<br />
1873, formerly identified as Natica a<strong>da</strong>nsoni<br />
de Blainville, 1825 (see Gubbioli &<br />
Nofroni, 1998), and no nudibranchs of<br />
any species. Further evidence to support<br />
a naticid origin for the drill holes is the<br />
preferred position in an area of the tube<br />
that would be embedded in the sediment<br />
and hence accessible only to an endobenthic<br />
pre<strong>da</strong>tor. Naticids are, moreover,<br />
known to be highly specific with regard<br />
to the position on the prey’s exoskeleton<br />
chosen for attack (Thomas, 1976; Kabat,<br />
1990).<br />
Martins et al. (2009), although recording<br />
one living specimen of Natica dilwinii<br />
Payraudeau, 1826, dredged at 300 m<br />
depth off Vila Franca do Campo, consider<br />
that Natica prietoi is definitively the most<br />
common naticid recorded alive from the<br />
<strong>Açores</strong>, as described in this study.<br />
Notwithstanding, Morton (1990) recorded<br />
living Natica intricata (Donovan, 1804)<br />
from Ilhéu de Vila Franca, São Miguel,<br />
and was reported by this author to feed,<br />
by drilling, on the tellinoidean bivalve<br />
Ervilia castanea Montagu, 1803. Other<br />
naticids have also been reported to occur<br />
in the <strong>Açores</strong> (Table 1), but these are generally<br />
records of empty shells. Euspira<br />
pulchella (Risso, 1826) has been recorded<br />
from the seabed at 2,000 metres depth in<br />
the <strong>Açores</strong> by Ávila et al. (1998). Natica<br />
variabilis Recluz in Reeve, 1855 was<br />
recorded from the offshore sea-bed of São<br />
Miguel by Morton & Britton (1995) and<br />
by Ávila et al. (1998). Natica alderi Forbes,<br />
1838 was recorded from São Jorge by<br />
Morton (1967) and, finally, Ávila et al.<br />
(1998) records Polinices lacteus (Guilding,<br />
1834).<br />
One further point which may have<br />
some bearing on these disparate records<br />
(except for Natica prietoi that, as this study<br />
shows, is numerous on the offshore seabed<br />
at ~ 200 metres depth), is that the<br />
Caribbean species Natica canrena<br />
(Linnaeus, 1758) has been recorded from<br />
the <strong>Açores</strong> by Morton & Britton (1998),<br />
Morton et al. (1998) and Ávila et al. (1998),<br />
an occurrence explained by the former<br />
authors as a chance event resulting from<br />
this species having a teleplanic larva<br />
(Laursen, 1981). The same argument has<br />
been presented for the occasional recorded<br />
occurrence of the North African<br />
Polinices lacteus in the <strong>Açores</strong> (Laursen,<br />
1981; Ávila et al., 1998; Morton et al.,<br />
1998).<br />
Natica prietoi is a small species (~ 10<br />
mm in shell diameter) and was the only<br />
naticid collected along with the samples,<br />
in the same trawls, of Ditrupa arietina<br />
reported upon by Morton & Salvador<br />
(2009) and herein. It seems, therefore,<br />
that Natica prietoi is a plausible candi<strong>da</strong>te<br />
TABLE 1. A species list of Natici<strong>da</strong>e recorded from the <strong>Açores</strong><br />
Species Location References<br />
Natica prietoi Hi<strong>da</strong>lgo, 1873 São Miguel Martins et al., 2009; this study.<br />
Natica dillwinii Payraudeau, 1826 São Miguel Martins et al., 2009.<br />
Natica a<strong>da</strong>nsoni de Blainville, 1825 São Miguel Ávila et al., 1998.<br />
Natica intricata (Donovan, 1804) São Miguel Morton, 1990; Ávila et al., 1998.<br />
Euspira pulchella (Risso, 1826) 2,000 metres Ávila et al., 1998<br />
Natica variabilis Recluz in Reeve, 1855 São Miguel Morton & Britton, 1995; Ávila et al., 1998.<br />
Natica alderi (Forbes, 1838) São Jorge Morton, 1967.<br />
Natica canrena (Linnaeus 1758)<br />
Natica canrena (Linnaeus 1758)<br />
Laursen, 1981; Morton et al., 1998; Ávila et<br />
Polinices lacteus (Guilding, 1834)<br />
Polinices lacteus (Guilding, 1834)<br />
al., 1998; Morton & Britton, 2000.<br />
Laursen, 1981; Ávila et al., 1998; Morton et<br />
al., 1998.
162 AÇOREANA<br />
2009, Sup. 6: 157-165<br />
for the identity of the pre<strong>da</strong>tor responsible<br />
for the holes in D. arietina.<br />
If the above conclusion is correct, this<br />
is the first record of a naticid attacking a<br />
serpulid polychaete. We are aware of<br />
only one other report, by Paine (1963),<br />
who observed a single individual of<br />
Neverita duplicata (Say, 1822) attacking the<br />
sabellid Owenia fusiformis delle Chiaje,<br />
1841.<br />
The incidence of multiple, complete,<br />
drillholes in a small number of tubes is<br />
curious (Fig. 1D). Simultaneous drilling<br />
by multiple individuals, although reported<br />
upon for muricids (Brown &<br />
Alexander, 1994; Taylor & Morton, 1996),<br />
is unlikely in naticids because of the manner<br />
in which such pre<strong>da</strong>tors handle their<br />
prey that is (albeit in other species)<br />
enveloped by the foot of the attacker<br />
which would preclude access by another<br />
would-be pre<strong>da</strong>tor. It is possible, however,<br />
that they represent sequential attacks,<br />
the first two of which were failures<br />
although they were evidently complete,<br />
in the sense that they perforate the full<br />
thickness of the tube, they may have been<br />
non-functional (Kitchell et al., 1986).<br />
Another possibility is that they were<br />
caused by another pre<strong>da</strong>tory taxon and<br />
we do note that the multiple holes illustrated<br />
in Figure 1D are more straightsided<br />
than are most of the others and thus<br />
more like muricid drill holes (Carriker,<br />
1981). Moreover, muricids are known to<br />
feed in clusters of conspecifics and sympatric<br />
species (Abe, 1980; Tong, 1986;<br />
Taylor & Morton, 1996). This raises the<br />
possibility of there being a muricid pre<strong>da</strong>tor<br />
on the offshore seabed that also feeds<br />
on Ditrupa arietina.<br />
Notwithstanding, this study appears<br />
to be the first to record significant drilling<br />
pre<strong>da</strong>tion upon Ditrupa arietina although<br />
Tan & Morton (1998) record the buccinid<br />
Engina armillata aperturally (but never<br />
drilling) attacking cemented serpulids in<br />
Hong Kong. In the <strong>Açores</strong>, the only significant<br />
pre<strong>da</strong>tor captured in the dredges<br />
with D. arietina was the naticid Natica<br />
a<strong>da</strong>nsoni. However, we conclude, in the<br />
light of this study, that further research is<br />
needed to establish the pre<strong>da</strong>tor-prey<br />
relationship(s) on and in the Açorean offshore<br />
seabed.<br />
ACKNOWLEDGEMENTS<br />
The authors are grateful to Prof. A.M.<br />
de Frias Martins, University of the<br />
<strong>Açores</strong>, for organising the workshop at<br />
which this research was undertaken and<br />
for providing the boat facilities allowing<br />
collection of the samples herein reported<br />
upon. Ms. Andreia Salvador (The<br />
Natural History Museum, London) is<br />
thanked for assistance with the sorting of<br />
the samples.<br />
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Socie<strong>da</strong>de Afonso Chaves, Ponta<br />
Delga<strong>da</strong>, São Miguel.<br />
PAINE, R.T., 1963. Trophic relationships of<br />
8 sympatric pre<strong>da</strong>tory gastropods.<br />
Ecology, 49: 63-73.<br />
PEARCE, J.B., & G. THORSON, 1967. The<br />
feeding and reproductive biology of<br />
the red whelk, Neptunea antiqua (L.)<br />
(Gastropo<strong>da</strong>, Prosobranchia). Ophelia,<br />
4: 277-314.<br />
POLOCZANSKA, E.S., D.J. HUGHES &<br />
M.T. BURROWS, 2004. Underwater<br />
television observations of Serpula vermicularis<br />
(L.) reefs and associated<br />
mobile fauna in Loch Creran,<br />
Scotland. Estuarine, Coastal and Shelf<br />
Science, 61: 425-435.<br />
PONDER, W.F., & J.D. TAYLOR, 1992.<br />
Pre<strong>da</strong>tory shell drilling by two species<br />
of Austroginella (Gastropo<strong>da</strong>:<br />
Marginelli<strong>da</strong>e). Journal of Zoology, 228:<br />
317-328.<br />
SHIMEK, R.L., 1984. The diets of Alaskan<br />
Neptunea. Veliger, 26: 274-281.<br />
TAN, K.S., & B. MORTON, 1998. The<br />
ecology of Engina armillata<br />
(Gastropo<strong>da</strong>: Buccini<strong>da</strong>e) in the Cape<br />
d’Aguilar Marine Reserve, Hong<br />
Kong, with particular reference to its<br />
preferred prey (Polychaeta:<br />
Serpuli<strong>da</strong>e). Journal of Zoology,<br />
London, 244: 391-403.<br />
TAYLOR, J.D., 1978a. Habitats and diets<br />
of pre<strong>da</strong>tory gastropods at Addu<br />
Atoll, Maldives. Journal of<br />
Experimental Marine Biology and<br />
Ecology, 31: 83-103.<br />
TAYLOR, J.D., 1978b. The diet of<br />
Buccinum un<strong>da</strong>tum and Neptunea antiqua<br />
(Gastropo<strong>da</strong>: Buccini<strong>da</strong>e). Journal<br />
of Conchology. 29: 309-318.<br />
TAYLOR, J.D., 1980. Diets and habitats of<br />
shallow water pre<strong>da</strong>tory gastropods<br />
around Tolo Channel, Hong Kong. In:<br />
MORTON, B. (Ed.). The Malacofauna of<br />
Hong Kong and Southern China.<br />
Proceedings of the First International<br />
Workshop on the Malacofauna of Hong<br />
Kong and Southern China: Hong Kong<br />
1977, pp. 163-180. Hong Kong<br />
University Press, Hong Kong.<br />
TAYLOR, J.D., & A. LEWIS, 1995. Diet<br />
and radular morphology of Peristernia<br />
and Latirolagena (Gastropo<strong>da</strong>:<br />
Fasciolarii<strong>da</strong>e) from Indo-Pacific coral<br />
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1143-1154.<br />
TAYLOR, J.D., & B. MORTON, 1996. The<br />
diets of pre<strong>da</strong>tory gastropods in the
MORTON & HARPER: DRILLING PREDATION UPON DITRUPA ARIETINA 165<br />
Cape d’Aguilar Marine Reserve,<br />
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TAYLOR, J.D., N.J. MORRIS & C.N. TAY-<br />
LOR, 1980. Food specialization and<br />
the evolution of pre<strong>da</strong>tory marine<br />
gastropods. Palaeontology, 23: 375-409.<br />
THOMAS, R.D.K., 1976. Gastropod pre<strong>da</strong>tion<br />
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of Glycymeris glycymeris (Bivalvia)<br />
from the Eastern United States.<br />
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(Gastropo<strong>da</strong>: Murici<strong>da</strong>e) in Hong<br />
Kong. Asian Marine Biology, 3: 163-<br />
178.<br />
VERSTRAETEN, J., & F. NOLF, 2004.<br />
Natica a<strong>da</strong>nsoni de Blainville, 1825 and<br />
Natica prietoi Hi<strong>da</strong>lgo, 1873: two similar<br />
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Neptunea, 3: 13-28.<br />
WITMAN, J.D., & R.A. COOPER, 1983.<br />
Disturbance and contrasting patterns<br />
of population structure in the brachiopod<br />
Terebratulina septentrionalis<br />
(Couthouy) from two subti<strong>da</strong>l habitats.<br />
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Biology and Ecology, 73: 57-79.<br />
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tube-boring nudibranch mollusc from<br />
the Central and West Pacific.<br />
American Zoologist, 9: 903-907.
AÇOREANA, Suplemento 6, Setembro 2009: 167-182<br />
THE PYCNOGONIDS (ARTHROPODA: PYCNOGONIDA) OF SÃO MIGUEL,<br />
AZORES, WITH DESCRIPTION OF A NEW SPECIES OF ANOPLODACTYLUS<br />
WILSON, 1878 (PHOXICHILIDIIDAE)<br />
Roger N. Bamber 1 & Ana Cristina Costa 2<br />
1<br />
The Natural History Museum, Cromwell Road, London SW7 5BD, U.K.<br />
e-mail: roger.bamber@artoo.co.uk<br />
2<br />
CIBIO-Pólo <strong>Açores</strong>, Department of Biology, University of the Azores, 9501-801 Ponta Delga<strong>da</strong>, São Miguel, Azores, Portugal<br />
ABSTRACT<br />
During the Third International Workshop of Malacology and Marine Biology in São<br />
Miguel, Azores, in July 2006, sampling of algae, and of the littoral and sublittoral benthos<br />
was undertaken in order to characterize the smaller marine arthropod fauna of this region,<br />
including pycnogonids. In the event, 50 specimens of Pycnogoni<strong>da</strong>, representing six<br />
species and including a new species of Anoplo<strong>da</strong>ctylus, were collected. In addition, previous<br />
pycnogonid material collected around São Miguel in 1996 and 1997 was analyzed,<br />
from 112 samples of which a further 3705 pycnogonid specimens were identified, representing<br />
eight species, three additional to the above six. All of this material is described<br />
below. The zoogeography of the fifteen species now recorded from the Azores is analyzed,<br />
and the likely origins of the Azorean pycnogonid fauna are discussed.<br />
RESUMO<br />
Durante o 3º Workshop Internacional de Malacologia e Biologia Marinha em São<br />
Miguel, <strong>Açores</strong>, em Julho de 2006, realizaram-se amostragens de algas e o bentos do litoral<br />
e sublitoral com vista a caracterizar a fauna de artrópodes marinhos de reduzi<strong>da</strong>s<br />
dimensões <strong>da</strong> região, incluindo picnogonídeos. Na ocasião foram recolhi<strong>dos</strong> 50<br />
exemplares de Pycnogoni<strong>da</strong>, representando seis espécies e incluindo uma nova espécie de<br />
Anoplo<strong>da</strong>ctylus. Para além disso, analisou-se material de picnogonídeos, previamente<br />
recolhido em São Miguel em 1996 e 1997, de 112 amostragens <strong>da</strong>s quais mais 3705<br />
espécimes de picnogonídeos foram identifica<strong>dos</strong>, representando oito espécies, três <strong>da</strong>s<br />
quais para além <strong>da</strong>s seis atrás referi<strong>da</strong>s. Todo este material é descrito em segui<strong>da</strong>.<br />
Analisa-se a zoogeografia <strong>da</strong>s quinze espécies agora regista<strong>da</strong>s para os <strong>Açores</strong> e discutese<br />
a provável origem <strong>da</strong> fauna de picnogonídeos Açorianos.<br />
INTRODUCTION<br />
Pycnogonids are a group of the arthropods<br />
with minimal dispersive ability<br />
(Bamber, 1998); the larvae are not planktonic,<br />
and there are only limited examples<br />
of adults swimming, and then not as a<br />
directional migratory movement (Arnaud<br />
& Bamber, 1987). A few genera, such as<br />
the deep-water (Bathypallenopsis) and the<br />
generally shallow-water Anoplo<strong>da</strong>ctylus,<br />
are known to live upon medusae, and<br />
thus obtain passive dispersion in the<br />
plankton (Lebour, 1916; Arnaud &<br />
Bamber, 1987; Bamber, 2002). Some<br />
species are known to have spread in fouling<br />
communities on ship’s hulls (Krapp &<br />
Sconfietti, 1983; Bamber, 1985).<br />
The Azores are a group of islands<br />
somewhat isolated in the north-east<br />
Atlantic, lying adjacent to the Mid-<br />
Atlantic Ridge some 1600 km west of<br />
Portugal and 1730 km southeast of<br />
Newfoundland. The main surface water<br />
currents reaching the archipelago bring<br />
waters from two directions: the Azores<br />
drift, a diffuse southerly arm of the Gulf<br />
Stream breaking off from the North
168 AÇOREANA<br />
2009, Sup. 6: 167-182<br />
Atlantic Drift supplies water from the<br />
Americas, while the somewhat less-significant<br />
western eddies of the Canary<br />
Current bring waters from Spain and<br />
North Africa; below these, the midwater<br />
current brings warm, hyperhaline water<br />
from the Mediterranean outflow (Morton<br />
et al., 1998; Gofas, 1990). For the passively-dispersing<br />
Pycnogoni<strong>da</strong>, therefore, it is<br />
of some interest to determine the suite of<br />
species which has colonized this archipelago,<br />
and their provenance.<br />
The only previous specific study of<br />
the Pycnogoni<strong>da</strong> of the Azores was that<br />
reported by Arnaud (1974), who recorded<br />
ten species from shallow waters, including<br />
the discovery of the currently<br />
Azorean-endemic Achelia anomala, as well<br />
as four species from waters of >500 m<br />
depth. Other previous records of pycnogonids<br />
in the Azores were noted by<br />
Loman (1912), Bouvier (1917), Arnaud<br />
(1978), Stock (1971; 1990) and Bamber<br />
(2002), although a number of these were<br />
from abyssal depths. Munilla & Sanchez<br />
(1988) reported on pycnogonids from the<br />
Canary Islands.<br />
The twelve species recorded previously<br />
in litt. from the Azores, from depths<br />
shallower than 100 m, are:<br />
Family Ammothei<strong>da</strong>e:<br />
Achelia anomala Arnaud, 1974 (currently<br />
endemic);<br />
A. echinata Hodge, 1864;<br />
Tanystylum orbiculare Wilson, 1878.<br />
Family Phoxichilidii<strong>da</strong>e:<br />
Anoplo<strong>da</strong>ctylus angulatus (Dohrn 1881);<br />
A. maritimus Hodgson, 1915;<br />
A. petiolatus (Kroyer, 1844);<br />
A. pygmaeus (Hodge, 1864).<br />
Family Callipalleni<strong>da</strong>e:<br />
Callipallene emaciata (Dohrn, 1881)<br />
Family Endei<strong>da</strong>e:<br />
Endeis spinosa (Montagu, 1808);<br />
E. straughani Clark, 1970 (see Stock,<br />
1990; an Australian species, possibly<br />
a misidentification, or an<br />
immigrant via ships’-hull-fouling,<br />
see Bamber, 1979 [as E. picta])<br />
Family Rhynchothoraci<strong>da</strong>e:<br />
Rhynchothorax philopsammum Hedgpeth,<br />
1951;<br />
R. monnioti Arnaud 1974.<br />
No members of the speciose family<br />
Nymphoni<strong>da</strong>e have yet been recorded.<br />
During the Third International<br />
Workshop of Malacology and Marine<br />
Biology at Vila Franca do Campo, on the<br />
island of São Miguel, Azores, in July 2006,<br />
sampling of the littoral and sublittoral<br />
benthos around São Miguel was undertaken<br />
in order to characterize the smaller<br />
marine arthropod fauna of this region,<br />
including pycnogonids. In the event, 50<br />
specimens representing six species, one<br />
new to science, were collected. In addition,<br />
a previous collection from around<br />
the island was made available, from 112<br />
samples from which a further 3705 pycnogonid<br />
specimens were identified, representing<br />
eight species, three additional<br />
to the above six. All of this material is<br />
described below.<br />
MATERIAL AND METHODS<br />
The present material comes from two<br />
sources. During the Workshop at Vila<br />
Franca do Campo in July 2006, a number<br />
of littoral and infralittoral habitats on the<br />
island of São Miguel were sampled for<br />
pycnogonids, including crevice habitats,<br />
macroalgae and soft sediments. The principal<br />
sampling areas were the littoral sediments,<br />
rocks and algae below the Clube<br />
Naval building (the old Vila Franca do<br />
Campo abattoir); the sediments and algae<br />
within the flooded crater of the Ilhéu de<br />
Vila Franca; and the soft sediments off<br />
Vila Franca do Campo (ca N37° 43’ W<br />
25°25’), from 12 to 200 m depth. Offshore<br />
sediments were sampled using a 0.025 m 2
BAMBER & COSTA: PYCNOGONIDS FROM SÃO MIGUEL 169<br />
van Veen grab and various dredges. All<br />
samples were washed through a 0.5 mm<br />
mesh sieve, and specimens sorted alive.<br />
Some of these specimens were fixed in<br />
absolute ethanol to allow DNA analysis.<br />
Extensive material collected in 1996<br />
and 1997, from infralittoral rocky-substratum<br />
sites around São Miguel, was also<br />
analysed in detail. Replicate samples of<br />
algae (Stypocaulon scoparia, Halopteris filicina<br />
and Zonaria tournefortii) were collected<br />
by SCUBA diving at depths from between<br />
5 and 16 m. Details of the sampling and<br />
protocols are given by Costa & Ávila<br />
(2001). The sampling sites, anti-clockwise<br />
around the Island from the north-west,<br />
were Mosteiros, Ponta <strong>da</strong> Ferraria, Santa<br />
Clara , Pesqueiro, Emissário, Sinaga,<br />
Atalha<strong>da</strong>, Ribeira <strong>da</strong> Praia, Caloura, Porto<br />
de Vila Franca do Campo, Ilhéu de Vila<br />
Franca, Ribeira Quente, Faial <strong>da</strong> Terra,<br />
Nordeste, Porto Formoso, Ladeira de<br />
Velha, Ribeirinha, Lactoaçoreana, Cofaco<br />
and São Vicente. These sites variously<br />
represented exposed and sheltered<br />
shores, undisturbed, naturally disturbed<br />
(near shallow-water vent sites or stream<br />
mouths) and polluted shores.<br />
Voucher and type-material has been<br />
lodged in the collections of The Natural<br />
History Museum, London (NHM). The<br />
higher taxonomy is based on Arnaud &<br />
Bamber (1987). All measurements are<br />
axial, measured dorsally for the trunk<br />
and proboscis (trunk length being from<br />
the anterior margin of the cephalon to the<br />
posterior margin of the fourth lateral<br />
processes), laterally for oviger and legs.<br />
SYSTEMATICS<br />
Family Ammothei<strong>da</strong>e Dohrn, 1881<br />
Achelia echinata Hodge, 1864<br />
Figure 1A<br />
Material: 1 male, 2 females, 1 subadult,<br />
WVF011, northeastern side of Ilhéu de<br />
Vila Franca do Campo, 16 m, scuba dive<br />
collection by Gonçalo Calado, José Pedro<br />
Borges, Joana Xavier, Paola Rachello,<br />
Patrícia Madeira, 20 July 2006. 3 males, 4<br />
females, 2 subadults, WVF040, off Amora,<br />
Ponta Garça, São Miguel, Azores, N37°<br />
42’ 720” W25° 21’ 554”, 37.8 m depth,<br />
small dredge sample, 26 July 2006, coll.<br />
António de Frias Martins & Jerry<br />
Harasewych. 1 female, 1 subadult, littoral<br />
rock scrape, Vila Franca do Campo<br />
marina, 19 July 2006, coll. Kathe Jensen. 1<br />
male with eggs, Isl. 24.5, mid-lagoon<br />
algae, within the flooded crater of the<br />
Ilhéu de Vila Franca, 24 July 2006, coll. A.<br />
Salvador, R. Robbins & R.B.<br />
12 specimens, Mosteiros, 8 November<br />
1996; 139 specimens, Mosteiros, 17 June<br />
1997; 41 specimens, Ponta <strong>da</strong> Ferraria, 17<br />
June 1997; 53 specimens, Santa Clara, 7<br />
November 1996; 201 specimens, Santa<br />
Clara, 12 June 1997; 20 specimens,<br />
Pesqueiro, 7 November 1997; 21<br />
specimens, Emissário, 2 November 1996;<br />
237 specimens, Emissário, 12 June 1997;<br />
37 specimens, Sinaga, 30 May 1997; 1<br />
specimen, Atalha<strong>da</strong>, 25 October 1996; 246<br />
specimens, Atalha<strong>da</strong>, 30 May 1997; 32<br />
specimens, Ribeira <strong>da</strong> Praia, 25 October<br />
1996; 70 specimens, Ribeira <strong>da</strong> Praia, 16<br />
June 1997; 61 specimens, Caloura, 14<br />
October 1996; 119 specimens, Caloura, 26<br />
June 1997; 48 specimens, Porto de Vila<br />
Franca do Campo, 9 May 1997; 8<br />
specimens, Ilhéu de Vila Franca do<br />
Campo, 24 October 1996; 47 specimens,<br />
Ilhéu de Vila Franca do Campo, 16 June<br />
1997; 44 specimens, Ribeira Quente, 18<br />
June 1997; 5 specimens, Faial <strong>da</strong> Terra, 17<br />
October 1996; 59 specimens, Faial <strong>da</strong><br />
Terra, 30 May 1997; 19 specimens,<br />
Nordeste, 21 November 1966; 143<br />
specimens, Nordeste, 2 May 1997; 36<br />
specimens, Porto Formoso, 30 October<br />
1996; 140 specimens, Porto Formoso, 19<br />
June 1997; 13 specimens, Ladeira <strong>da</strong><br />
Velha, 19 June 1997; 16 specimens,<br />
Ribeirinha, 8 October 1996; 140
170 AÇOREANA<br />
2009, Sup. 6: 167-182<br />
specimens, Ribeirinha, 25 June 1997; 10<br />
specimens, Lactoaçoreana, 14 October<br />
1996; 76 specimens, Lactoaçoreana, 25<br />
June 1997; 5 specimens, Cofaco, 25 June<br />
1997; 13 specimens, São Vicente, 7<br />
October 1996; 18 specimens, São Vicente,<br />
6 May 1997; all coll. João Brum & A.C.C.<br />
Remarks: with a total of 2146 specimens<br />
from 110 samples listed above, Achelia<br />
echinata is easily the commonest shallowwater<br />
pycnogonid in the Azores (occurring,<br />
for example, at every sampling site<br />
in 1996 and 1997). In the light of the<br />
potential for cryptic sibling species in this<br />
taxon, specimens collected in alcohol<br />
were analysed for their 16s DNA to compare<br />
with specimens from England which<br />
had already been analysed as part of a<br />
larger project (Bamber et al., in prep.) and<br />
showed 100% agreement. All the<br />
Azorean material was collected in association<br />
with algae, on which, inter alia, this<br />
species is known to feed (Bamber &<br />
Davis, 1982).<br />
Ammothella longipes (Hodge, 1864)<br />
Figure 1B<br />
Ammothoa longipes Hodge, 1864<br />
Achelia longipes sens. auctt.;<br />
Achelia magnirostris (Dohrn, 1881)<br />
Material: 1 specimen, Atalha<strong>da</strong>, 30 May<br />
1997; 1 specimen, Ribeira <strong>da</strong> Praia, 16<br />
June 1997; 16 specimens, Porto de Vila<br />
Franca do Campo, 9 May 1997; 6<br />
specimens, Ribeira Quente, 18 June 1997;<br />
31 specimens, Lactoaçoreana, 25 June<br />
1997; all coll. João Brum & A.C.C.<br />
Remarks: This species has been recorded<br />
from the Atlantic coasts of Europe<br />
(England being the type-locality), the<br />
Mediterranean and North Africa, as well<br />
as the Canaries (Sanchez & Munilla,<br />
1989), but had not been recorded previously<br />
from the Azores. It is readily distinguished<br />
from sympatric Achelia echinata<br />
by the fleshy, glabrous dorsodistal<br />
tubercles on the lateral processes, the lack<br />
of spinose tubercles on the lateral<br />
processes and coxae, and in having nine<br />
palp articles (A. echinata having eight).<br />
Family Phoxichilidii<strong>da</strong>e Sars, 1891<br />
Anoplo<strong>da</strong>ctylus amora sp. nov.<br />
Figure 2.<br />
Material: 1 male, holotype<br />
(NHM.2007.416), 1 male, 1 subadult<br />
female, paratypes (NHM.2007.417-418),<br />
VWF040, off Amora, Ponta Garça, São<br />
Miguel, Azores, N37° 42’ 720” W25° 21’<br />
554”, 37.8 m depth, small dredge sample,<br />
26 July 2006, coll. António de Frias<br />
Martins & Jerry Harasewych; 1 subadult<br />
male, Vila Franca do Campo marina, São<br />
Miguel, Azores, littoral rock scraping, 19<br />
July 2006, coll. Kathe Jensen.<br />
2 males, paratypes (NHM.2007.419-<br />
420), Caloura, 26 June 1997; 1 male,<br />
paratype (NHM.2007.421), Ilhéu de Vila<br />
Franca do Campo, 16 June 1997; 1<br />
subadult male, 1 female, paratypes<br />
(NHM.2007.422-423), Faial <strong>da</strong> Terra, 30<br />
May 1997; all coll. João Brum & A.C.C.<br />
Description of male: habitus typical of the A.<br />
petiolatus form, trunk (Figure 2A, B) almost<br />
glabrous, with segment articulations<br />
between cephalon, trunk segment two and<br />
trunk segment three. Cephalon overhanging<br />
proboscis base to half proboscis length,<br />
lateral anterior margin with slight shoulders<br />
bearing short seta; dome-shaped ocular<br />
tubercle slightly taller than wide, without<br />
distal tubercle, with four pigmented eyes<br />
and laterodistal sensory pit; oviger attachment<br />
on mid-ventral surface of first lateral<br />
process. Lateral processes shorter than segment<br />
width, separated by less than their<br />
own diameter, with simple anterodistal seta<br />
and very small dorsodistal tubercle (little<br />
more than a swelling). Abdomen simple,<br />
sub-clavate, angled upward at about 45º,<br />
exceeding distal edge of coxa 1 of leg 4, sub-
BAMBER & COSTA: PYCNOGONIDS FROM SÃO MIGUEL 171<br />
FIGURE 1. A, Achelia echinata, entire, dorsal (modified after Sars, 1893); B, Ammothoella longipes,<br />
entire, dorsal.
172 AÇOREANA<br />
2009, Sup. 6: 167-182<br />
distally bearing pair of lateroventral spines<br />
and single mid-dorsal spine.<br />
Proboscis stout, parallel-sided, one-third<br />
as long as trunk.<br />
Chelifore (Figure 2C) scape of one article,<br />
slender, with sparse dorsal and distal<br />
setae; chela compact, fingers just shorter<br />
than palm, palm and moveable finger<br />
setose, cutting edges naked. Palp absent.<br />
Oviger (Figure 2D) of six articles, proximal<br />
article short, compact; article 2 (O2)<br />
three times as long as wide, with single dor-<br />
FIGURE 2. Anoplo<strong>da</strong>ctylus amora sp. nov., male holotype, A, lateral and B, dorsal; C, right chelifore; D, left<br />
oviger; E, third left leg; F, detail of distal articles of third leg; G, coxa 2 and femur of male A. petiolatus.<br />
Scale line = 1 mm for A and B, 0.4 mm for C and D, 0.8 mm for E, 0.3 mm for F, 0.5 mm for G.
BAMBER & COSTA: PYCNOGONIDS FROM SÃO MIGUEL 173<br />
sal and ventral setae; O3 longest, 2.3 times<br />
length of O2, slender, with sparse dorsal and<br />
ventral setae; O4 just shorter than O2,<br />
curved, with dorsodistal setae; O5 0.6<br />
times as long as O4, with numerous setae<br />
pointing proximally; O6 compact, acornshaped,<br />
half length of O5, with outer and<br />
ventral setae pointing proximally.<br />
Third leg (Figure 2E) elongate, not<br />
slender. Coxa 1 compact, with sparse distal<br />
setae, without dorsal tubercle; coxa 2<br />
almost three-times as long as coxa 1, 2.5<br />
times as long as wide, with pronounced<br />
ventrodistal genital spur; coxa 3 just more<br />
than half length of coxa 2. Femur stout,<br />
less than four times as long as wide, twice<br />
as long as coxa 2, setose, without conspicuous<br />
dorsodistal spur; cement-gland tube<br />
externally very short, arising at 0.6 the<br />
length of the femur, extending subcutaneously<br />
half way to proximal end of<br />
femur. Tibia 1 shorter than femur (0.9<br />
times femur length), setose as figured;<br />
tibia 2 five times as long as wide, as long<br />
as femur, more densely setose, longest<br />
dorsodistal seta not on a spur. Tarsus<br />
small, triangular, with numerous ventral<br />
and single dorsal setae. Propodus (Figure<br />
2F) with distinct heel, with two large<br />
proximal and five slender distal heel<br />
spines; sole with row of seven simple submarginal<br />
setae in distal two-thirds, seven<br />
short, recurved marginal spines and distal<br />
lamina for 30% of sole length. Main<br />
claw two-thirds as long as propodus, auxiliary<br />
claws small, lateral, slender, 0.15<br />
times length of main claw.<br />
Description of female: generally as male,<br />
but ovigerous legs absent, femur swollen;<br />
no ventral tubercles on proboscis.<br />
Measurements of holotype male (mm). –<br />
Trunk length: 1.91; trunk segment 2<br />
length: 0.29; width across 2nd lateral<br />
processes: 0.99; abdomen length: 0.42;<br />
proboscis length: 0.53.<br />
Lengths of oviger articles 1 to 6<br />
respectively: 0.13; 0.31; 0.73; 0.27; 0.17;<br />
0.09.<br />
Fourth leg, lengths of coxa 1: 0.24;<br />
coxa 2: 0.69; coxa 3: 0.38; femur: 1.40<br />
(width 0.36); tibia 1: 1.23; tibia 2: 1.40<br />
(width 0.28); tarsus: 0.12; propodus: 0.55;<br />
main claw: 0.37; auxiliary claw: 0.06.<br />
Etymology: named after the location on<br />
São Miguel off which the type-locality<br />
lies.<br />
Remarks: there are two previously<br />
described species of Anoplo<strong>da</strong>ctylus which<br />
have a subcutaneous proximal extension<br />
of the cement gland tube, viz. A. erectus<br />
Cole, 1904 from the Pacific (the Americas<br />
from Chile to British Columbia, Hawaii,<br />
Polynesia, Japan, Korea and Hong Kong)<br />
at depths of 0 to 90 m, and A. amoybios<br />
Bamber, 2004 from Atlantic Equatorial<br />
Africa (Gabon and Equatorial Guinea) at<br />
depths of 36 to 63 m (see Stock, 1955;<br />
Müller, 1990; Bamber, 2004). Both of these<br />
species also share the characters of a sixarticled<br />
ovigerous leg, the ocular tubercle<br />
overhanging the proboscis, small auxiliary<br />
claws and a propo<strong>da</strong>l lamina. A.<br />
amoybios, the only other Atlantic species,<br />
is immediately distinct in having dorsodistal<br />
tubercles on coxa 1 of all legs. A.<br />
erectus normally has conspicuous dorsodistal<br />
tubercles on the lateral processes,<br />
unlike the present species. In addition, A.<br />
erectus is conspicuously more slender<br />
than A. amora sp. nov, femur and tibia 2<br />
length:width ratios being 5.3 and 7.7<br />
respectively (3.9 and 5 respectively in A.<br />
amora), and the width across trunk segment<br />
2 is four times the length of the segment<br />
(
174 AÇOREANA<br />
2009, Sup. 6: 167-182<br />
(Krøyer, 1844) from the Azores, at depths<br />
between 1 and 30 m; that species is readily<br />
distinguished from A. amora by its<br />
cement gland configuration (without subcutaneous<br />
extension, see Figure 2G).<br />
Anoplo<strong>da</strong>ctylus angulatus (Dohrn, 1881)<br />
Figure 3A to C<br />
Material: 1 female, WVF011, northeastern<br />
side of Ilhéu de Vila Franca do Campo, 16<br />
m, scuba dive collection by Gonçalo<br />
Calado, José Pedro Borges, Joana Xavier,<br />
Paola Rachello, Patrícia Madeira, 20 July<br />
2006.1 male, 3 females, 1 subadult, Isl.<br />
24.4, attached littoral algae, south wall<br />
within the flooded crater of the Ilhéu de<br />
Vila Franca, 24 July 2006, coll. A.<br />
Salvador, R. Robbins & R.B.; 2 males with<br />
eggs, 1 male, 4 females, 2 subadults, Isl.<br />
24.5, mid-lagoon algae, within the flooded<br />
crater of the Ilhéu de Vila Franca, 24<br />
July 2006, coll. A. Salvador, R. Robbins &<br />
R.B.<br />
1 specimen, Mosteiros, 8 November<br />
1996; 2 specimens, Mosteiros, 17 June<br />
1997; 1 specimen, Santa Clara, 7<br />
November 1996 ; 3 specimens, Santa<br />
Clara, 12 June 1997; 12 specimens,<br />
Pesqueiro, 7 November 1997; 2<br />
specimens, Emissário, 2 November 1996;<br />
24 specimens, Emissário, 12 June 1997; 4<br />
specimens, Sinaga, 30 May 1997; 25<br />
specimens, Atalha<strong>da</strong>, 30 May 1997; 1<br />
specimen, Ribeira <strong>da</strong> Praia, 25 October<br />
1996; 5 specimens, Ribeira <strong>da</strong> Praia, 16<br />
June 1997; 7 specimens, Caloura, 26 June<br />
1997; 6 specimens, Porto de Vila Franca<br />
do Campo, 9 May 1997; 2 specimens,<br />
Ribeira Quente, 18 June 1997; 10<br />
specimens, Nordeste, 2 May 1997; 1<br />
specimen, Porto Formoso, 30 October<br />
1996; 3 specimens, Porto Formoso, 19 June<br />
1997; 4 specimens, Ladeira <strong>da</strong> Velha, 19<br />
June 1997; 10 specimens, Ribeirinha, 25<br />
June 1997; 1 specimen, Cofaco, 25 June<br />
1997;2 specimens, São Vicente, 6 May<br />
1997; all coll. João Brum & A.C.C.<br />
Remarks: the commonest species of<br />
Anoplo<strong>da</strong>ctylus in the Azores, A. angulatus<br />
is also known from the Mediterranean,<br />
the Atlantic coasts of Northern Europe<br />
and North Africa (Morocco), as well as<br />
the Canary Islands. It is an algal-associated<br />
species without a conspicuous overhang<br />
of the anterior of the cephalon, and<br />
distinguished from sympatric specimens<br />
of A. virescens (also occurring in algae) by<br />
the marked angular distal corners of the<br />
proboscis (Figure 3B).<br />
Anoplo<strong>da</strong>ctylus maritimus Hodgson, 1915<br />
Figure 3D<br />
Incl. A. parvus Giltay, 1934; non-A. parvum<br />
(Hilton, 1942) = A. hokkaidoensis (Utinomi,<br />
1954).<br />
Material: 1 specimen, Emissário, 12 June<br />
1997; 2 specimens, Caloura, 26 June 1997;<br />
15 specimens, Porto de Vila Franca do<br />
Campo, 9 May 1997; 1 specimen, Ilhéu de<br />
Vila Franca do Campo, 24 October 1996; 2<br />
specimens, Ilhéu de Vila Franca do<br />
Campo, 16 June 1997; 10 specimens,<br />
Lactoaçoreana, 25 June 1997; all coll. João<br />
Brum & A.C.C.<br />
Remarks: Anoplo<strong>da</strong>ctylus maritimus has<br />
been recorded previously throughout<br />
Macaronesia, other than which it is a<br />
species of the Atlantic coast of the<br />
Americas (see discussion below) but has<br />
not been recorded from the Atlantic<br />
coasts of mainland Europe, North Africa<br />
or the Mediterranean.<br />
Anoplo<strong>da</strong>ctylus pygmaeus (Hodge, 1864)<br />
Figure 3E, F<br />
Material: 1 female, Isl. 24.4, attached lowlittoral<br />
algae, south wall within the flooded<br />
crater of the Ilhéu de Vila Franca;1<br />
female, Isl. 24.5, mid-lagoon algae, within<br />
the flooded crater of the Ilhéu de Vila<br />
Franca; both 24 July 2006, coll. A.<br />
Salvador, R. Robbins & R.B.
BAMBER & COSTA: PYCNOGONIDS FROM SÃO MIGUEL 175<br />
FIGURE 3. A to C, Anoplo<strong>da</strong>ctylus angulatus: A, entire, dorsal; B, proboscis, ventral; C, distal leg articles<br />
(lam = lamina); D, A. maritimus, distal leg articles; E and F, A. pygmaeus: E, body, lateral; F, third<br />
leg, entire; G to H, A. virescens: G, proboscis, ventral; H, distal leg articles.
176 AÇOREANA<br />
2009, Sup. 6: 167-182<br />
1 specimen, Pesqueiro, 7 November<br />
1997; 4 specimens, Porto de Vila Franca<br />
do Campo, 9 May 1997; 1 specimen, Faial<br />
<strong>da</strong> Terra, 30 May 1997; 1 specimen,<br />
Ribeirinha, 25 June 1997; all coll. João<br />
Brum & A.C.C.<br />
Remarks: Anoplo<strong>da</strong>ctylus pygmaeus is a<br />
small species (as its name suggests), similar<br />
to A. petiolatus but with a less-marked<br />
anterior cephalic overhang and with distinct<br />
distal spines on the dorsodistal<br />
tubercles of the lateral processes; auxiliary<br />
claws are absent. It has been recorded<br />
throughout the North Atlantic and<br />
Mediterranean, including the Canaries<br />
and the Azores, in shallow water (the<br />
record from 3850 m depth on the Cape<br />
Verde Slope by Bamber & Thurston, 1993,<br />
is presumed to be a result of samplinggear<br />
contamination from the fouling community<br />
on the ship’s hull).<br />
Anoplo<strong>da</strong>ctylus virescens (Hodge, 1864)<br />
Figure 3G, H<br />
Material: 1 female, WVF040, off Amora,<br />
Ponta Garça, São Miguel, Azores, N37°<br />
42’ 720” W25° 21’ 554”, 37.8 m depth,<br />
small dredge sample, 26 July 2006, coll.<br />
António de Frias Martins & Jerry<br />
Harasewych.<br />
Remarks: while isolated females of this<br />
genus can be difficult to identify to<br />
species, Anoplo<strong>da</strong>ctylus virescens, with its<br />
trunk segmentation only between somites<br />
1, 2 and 3, its presence of small auxiliary<br />
claws, its lack of propo<strong>da</strong>l lamina, of dorsodistal<br />
lateral-process tubercles, of ventral<br />
proboscis tubercles and of chela teeth,<br />
is only confusable with A. robustus<br />
(Dohrn, 1881), but the latter species has<br />
angulate corners to its proboscis, unlike<br />
the present species. A. virescens is known<br />
from the north-east Atlantic from the<br />
United Kingdom to Morocco and<br />
throughout the Mediterranean. This is the<br />
first record of this species for the Azores.<br />
Family Callipalleni<strong>da</strong>e Hilton, 1942<br />
Callipallene emaciata (Dohrn, 1881)<br />
Figure 4A<br />
Material: 1 male, 3 females, 1 juvenile, Isl.<br />
24.4, attached low-littoral algae, south<br />
wall within the flooded crater of the Ilhéu<br />
de Vila Franca; 5 females, 1 male, Isl. 24.5,<br />
mid-lagoon algae, within the flooded<br />
crater of the Ilhéu de Vila Franca; both 24<br />
July 2006, coll. A. Salvador, R. Robbins &<br />
R.B.<br />
4 specimens, Mosteiros, 8 November<br />
1996; 118 specimens, Mosteiros, 17 June<br />
1997; 12 specimens, Ponta <strong>da</strong> Ferraria, 17<br />
June 1997; 24 specimens, Santa Clara, 7<br />
November 1996; 61 specimens, Santa<br />
Clara, 12 June 1997; 17 specimens,<br />
Pesqueiro, 7 November 1997; 27<br />
specimens, Emissario, 2 November 1996;<br />
179 specimens, Emissario, 12 June 1997;<br />
26 specimens, Sinaga, 30 May 1997; 1<br />
specimen, Atalha<strong>da</strong>, 25 October 1996; 222<br />
specimens, Atalha<strong>da</strong>, 30 May 1997; 35<br />
specimens, Ribeira <strong>da</strong> Praia, 25 October<br />
1996; 29 specimens, Ribeira <strong>da</strong> Praia, 16<br />
June 1997; 18 specimens, Caloura, 14<br />
October 1996; 133 specimens, Caloura, 26<br />
June 1997; 24 specimens, Porto de Vila<br />
Franca do Campo, 9 May 1997; 29<br />
specimens, Ilhéu de Vila Franca do<br />
Campo, 16 June 1997; 13 specimens,<br />
Ribeira Quente, 18 June 1997; 4<br />
specimens, Faial <strong>da</strong> Terra, 17 October<br />
1996; 21 specimens, Faial <strong>da</strong> Terra, 30 May<br />
1997; 4 specimens, Nordeste, 21<br />
November 1966; 51 specimens, Nordeste,<br />
2 May 1997; 25 specimens, Porto Formoso,<br />
30 October 1996; 69 specimens, Porto<br />
Formoso, 19 June 1997; 5 specimens,<br />
Ladeira <strong>da</strong> Velha, 19 June 1997; 29<br />
specimens, Ribeirinha, 8 October 1996; 67<br />
specimens, Ribeirinha, 25 June 1997; 14<br />
specimens, Lactoaçoreana, 14 October<br />
1996; 26 specimens, Lactoaçoreana, 25<br />
June 1997; 4 specimens, Cofaco, 25 June
BAMBER & COSTA: PYCNOGONIDS FROM SÃO MIGUEL 177<br />
1997; 17 specimens, São Vicente, 7<br />
October 1996; 1 specimen, São Vicente, 6<br />
May 1997; all coll. João Brum & A.C.C.<br />
Remarks: the European shallow-water<br />
species of the genus Callipallene are small,<br />
cryptic species normally associated with<br />
epizoan turfs of bryozoans and hydroids.<br />
The distinction of these taxa was analysed<br />
by Stock (1952), since when his subspecies<br />
have been raised to full specific rank (C.<br />
brevirostris (Johnston, 1837), C. emaciata, C.<br />
FIGURE 4. A to B, Callipallene emaciata: A, entire, dorsal; B, distal; leg articles; C, Endeis spinosa,<br />
entire, dorsal (after Bamber, 1983).
178 AÇOREANA<br />
2009, Sup. 6: 167-182<br />
tiberi (Dohrn, 1881), C. phantoma (Dohrn,<br />
1881)). While C. brevirostris is the commonest<br />
species on the Atlantic coasts of<br />
North Europe, the present species is the<br />
only Callipallene recorded from the shallow<br />
waters of the Azores (the deeperwater<br />
C. producta Sars, 1888 has been<br />
recorded off the Azores (Bouvier, 1917;<br />
Arnaud, 1974) at depths >800 m), and is<br />
more commonly associated with algae<br />
than are the other species listed above.<br />
All the Azorean specimens were collected<br />
from algae, the species being the second<br />
commonest recorded (occurring, for<br />
example, at every sampling site in 1996<br />
and 1997).<br />
Family Endei<strong>da</strong>e Norman, 1908<br />
Endeis spinosa (Montagu, 1808)<br />
Figure 4B<br />
Material: 3 specimens, Mosteiros, 8<br />
November 1996; 3 specimens, Santa<br />
Clara, 12 June 1997; 1 specimen, Sinaga,<br />
30 May 1997; 5 specimens, Atalha<strong>da</strong>, 30<br />
May 1997; 9 specimens, Ribeira <strong>da</strong> Praia,<br />
16 June 1997; 1 specimen, Caloura, 14<br />
October 1996; 4 specimens, Caloura, 26<br />
June 1997; 1 specimen, Porto de Vila<br />
Franca do Campo, 9 May 1997; 2<br />
specimens, Ilhéu de Vila Franca do<br />
Campo, 16 June 1997; 1 specimen, Ribeira<br />
Quente, 18 June 1997; 2 specimens, Faial<br />
<strong>da</strong> Terra, 30 May 1997; 1 specimen,<br />
Nordeste, 2 May 1997; 2 specimens, Porto<br />
Formoso, 19 June 1997; 1 specimen,<br />
Lactoaçoreana, 14 October 1996; 1<br />
specimen, Lactoaçoreana, 25 June 1997; 1<br />
specimen, São Vicente, 6 May 1997; all<br />
coll. João Brum & A.C.C.<br />
Remarks: a widespread North Atlantic<br />
species, where its only native congener is<br />
Endeis charyb<strong>da</strong>ea (Dohrn, 1881) on<br />
European coasts. Stock’s (1990) record of<br />
E. meridionalis (Böhm, 1879) from Cape<br />
Verde is highly suspect. E. mollis<br />
(Carpenter, 1904) may be a Lessepsian<br />
immigrant to the Mediterranean. While<br />
the larval biology of this species is<br />
unknown, there is evidence of its waterborne<br />
transport, perhaps by association<br />
with hydromedusae.<br />
DISCUSSION<br />
There are now fifteen species of shallow-water<br />
pycnogonids recorded from<br />
the Azores: Ammothoella longipes,<br />
Anoplo<strong>da</strong>ctylus virescens and A. amora sp.<br />
nov. are newly recorded for the islands<br />
from the present study. Achelia echinata,<br />
Anoplo<strong>da</strong>ctylus angulatus and Callipallene<br />
emaciata are common.<br />
Analysis of the provenance of these<br />
species is somewhat challenged by the<br />
presence of species which have in the past<br />
been misidentified, early records worldwide<br />
depending on what was at the time<br />
a limited literature, and a limited understanding<br />
of specific characters.<br />
For example, Achelia echinata, a species<br />
with a type locality in the United<br />
Kingdom, has been recorded in the literature<br />
not only throughout the north-east<br />
Atlantic and Mediterranean (an accepted<br />
distribution), but also from China and<br />
Japan (as subspecies), from California<br />
and Alaska. Recent molecular work<br />
(Bamber et al. in prep.) has shown not<br />
only that the material from the Azores is<br />
fully conspecific with material from the<br />
United Kingdom, but also that the<br />
Chinese-Japanese “subspecies” is in fact a<br />
distinct species. The North- and East-<br />
Pacific material is highly suspect, and is<br />
not accepted herein.<br />
Rhynchothorax anophtalmus Arnaud,<br />
1972, recorded as such from the Azores by<br />
Arnaud (1974), was synonymized with R.<br />
philopsammum Hedgpeth, 1951 by Arnaud<br />
& Krapp (1990), when comparing specimens<br />
from the Mediterranean and from<br />
California: R. philopsammum is a<br />
Californian species, also recorded from
BAMBER & COSTA: PYCNOGONIDS FROM SÃO MIGUEL 179<br />
the Subantarctic, Pacific Mexico,<br />
Magellanic Chile, a number of Pacific<br />
Islands and Belize. Other than the Pacific<br />
material , the species is recorded (as R.<br />
anophtalmus) from Azores and the<br />
Mediterranean. Rhynchothorax is an interstitial<br />
genus which would not be expected<br />
to be transported by ships’-hull fouling or<br />
by floating weed. With this disparity in<br />
zoogeography, closer examination may<br />
yet show these two taxa to be distinct.<br />
Records of R. monnioti (type-locality the<br />
Azores) from Brazil and Trini<strong>da</strong>d<br />
(Arnaud & Krapp, 1990; Child, 1988) are<br />
dubious, and not accepted herein.<br />
In the light of the above, the species<br />
currently known from the Azores show a<br />
number of zoogeographies:<br />
- two currently endemic species – Achelia<br />
anomala (not recorded since the original<br />
discovery and description:<br />
Arnaud, 1974), and Anoplo<strong>da</strong>ctylus<br />
amora (recorded herein for the first<br />
time); Morton & Britton (2000) point<br />
out that endemism is low in these<br />
islands owing to their “youthfulness”<br />
(earliest emergence about 8 My ago),<br />
and such species are likely to be found<br />
elsewhere in the future;<br />
- two species from Macaronesia and the<br />
Mediterranean - Rhynchothorax anophtalmus<br />
from the Mediterranean; R.<br />
monnioti from the Mediterranean and<br />
the Canary Islands;<br />
- three species from the North-east<br />
Atlantic, the Mediterranean and<br />
North Africa (Morocco) – Ammothoella<br />
longipes, Anoplo<strong>da</strong>ctylus angulatus,<br />
Anoplo<strong>da</strong>ctylus virescens (the first two<br />
also recorded elsewhere in the<br />
Macaronesian system);<br />
- five species found in the Mediterranean<br />
and throughout the<br />
North Atlantic, including the<br />
Americas – Achelia echinata,<br />
Anoplo<strong>da</strong>ctylus petiolatus, Anoplo<strong>da</strong>ctylus<br />
pygmaeus, Callipallene emaciata and<br />
Endeis spinosa: closer study may yet<br />
distinguish cryptic species within<br />
these <strong>da</strong>ta;<br />
- a species found throughout the southern<br />
North Atlantic – Tanystylum orbiculare<br />
(distribution as the previous group 4,<br />
but not including the European<br />
Atlantic coasts);<br />
- a species from Macaronesia and the<br />
West Atlantic only – Anoplo<strong>da</strong>ctylus<br />
maritimus, recorded from Madeira,<br />
Cape Verde Islands, the Canaries and<br />
the Americas from Chesapeake Bay<br />
through the Gulf of Mexico and the<br />
Caribbean to Brazil;<br />
- an immigrant species – Endeis straughani<br />
(if a valid record), a species native<br />
to Australia but since recorded in<br />
ship’s-hull-fouling from Ghana<br />
(Bamber, 1979, as E. picta; Staples,<br />
1982).<br />
Apart from the presently endemic<br />
species and the anthropogenic immigrant,<br />
all but one of these species are also<br />
found in the Mediterranean, and of these<br />
all but the two Rhynchothorax species are<br />
recorded from Morocco. Five of these<br />
twelve species have not been found in the<br />
Western Atlantic. These <strong>da</strong>ta give a<br />
strong indication that the pycnogonid<br />
fauna of the Azores is largely of an easterly<br />
origin, from the Mediterranean, North<br />
Africa or Atlantic Europe.<br />
The notable exception is<br />
Anoplo<strong>da</strong>ctylus maritimus, recorded from<br />
the Azores, the Canary Islands, Cape<br />
Verde and Madeira (see Fage & Stock,<br />
1966; Stock, 1990; Child, 1992), and found<br />
in nine of the samples from 1996 and<br />
1997. This species is also found in the<br />
Americas (see above), including in the<br />
Sargasso Sea, and is commonly recorded<br />
amongst floating Sargassum (Bourdouillon,<br />
1955; Stock, 1954; Stock,<br />
1957; McCloskey, 1973; Stock,1992; Child,<br />
1992); indeed, Hodgson (1915) found it in<br />
floating Sargassum south of the Azores. In
180 AÇOREANA<br />
2009, Sup. 6: 167-182<br />
addition, Stock (1994) recorded “>500<br />
specimens” of A. maritimus associated<br />
with surface-floating hydroids in the<br />
mid-Atlantic, at 24.75°N 44 to 53°W.<br />
Drift dispersal in algae as a viable<br />
means of passive migration by pycnogonids<br />
was analyzed by Bamber (1998).<br />
Perhaps significantly, other species<br />
recorded amongst Sargassum are Endeis<br />
spinosa, Anoplo<strong>da</strong>ctylus petiolatus and<br />
Tanystylum orbiculare (see Timmermann,<br />
1932; Hedgpeth, 1948), and the first two<br />
of these have been recorded on Sargassum<br />
in the vicinity of the Azores (Hedgpeth,<br />
1948: Figure 7).<br />
Finally, it is notable that the most<br />
diverse genus recorded, Anoplo<strong>da</strong>ctylus,<br />
includes species which are known to live<br />
upon medusae, and thus obtain passive<br />
dispersion in the plankton (see<br />
Introduction, above); the comparatively<br />
widespread distribution of Anoplo<strong>da</strong>ctylus<br />
species is commonly attributed to this<br />
process (see Bamber, 1998 for discussion).<br />
Thus, the proximity and known distributions<br />
of most species would favour colonization<br />
by species from the east<br />
(Mediterranean, North Africa, Atlantic<br />
Southern Europe), and as far as we know<br />
this can be the only source of five of the<br />
species discussed above; Morton &<br />
Britton (2000) found that most components<br />
of the Azorean marine fauna show<br />
affiliation with the Mediterranean and<br />
southern Europe. However, the incidence<br />
of species recorded in the Americas in<br />
floating algae gives a mechanism for<br />
transport, which would argue for colonization<br />
from the west. In reality, pycnogonid<br />
colonization of the shallow water<br />
habitats of the Azores may be attributed<br />
to both processes. However, the mechanism<br />
of immigration from the east<br />
remains purely speculative.<br />
For the species occurring in the 1996<br />
and 1997 <strong>da</strong>ta in sufficient numbers for<br />
interpretation, no trends were detected in<br />
relation to disturbance or exposure,<br />
although Anoplo<strong>da</strong>ctylus amora only<br />
occurred at non-polluted sites.<br />
ACKNOWLEDGEMENTS<br />
We are indebted to Roni Robbins for<br />
assistance in the field collecting and sample<br />
analysis in 2006, to Andreia Salvador<br />
for sampling assistance in Ilhéu de Vila<br />
Franca, to João Brum for assistance in the<br />
diver-collections in 1996 and 1997, to<br />
Brian Morton for discussions on the origins<br />
of the Azorean fauna, particularly to<br />
António de Frias Martins for the organisation<br />
of, and inviting us to the<br />
Workshop, and to the other participants<br />
at the workshop for samples and for<br />
entertainment.<br />
LITERATURE CITED<br />
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ARNAUD, F., 1978. A new species of<br />
Ascorhynchus (Pycnogoni<strong>da</strong>) found<br />
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99-104.<br />
ARNAUD, F., & R.N. BAMBER, 1987.<br />
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BAMBER, R.N., 1979. A new species of<br />
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BAMBER, R.N., 1983. The Marine Fauna<br />
of the Cullercoats District, No. 12:
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BAMBER, R.N., 1998. Zoogeographic<br />
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BAMBER, R.N., 2002. Bathypelagic pycnogonids<br />
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BAMBER, R.N., 2004. Two new pycnogonids<br />
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BAMBER, R.N., & M.H. DAVIS, 1982.<br />
Feeding of Achelia echinata Hodge<br />
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and Ecology, 60: 181-187.<br />
BAMBER R.N., & M.H. THURSTON,<br />
1993. Deep water pycnogonids of the<br />
Cape Verde Slope. Journal of the<br />
Marine Biological Association of the<br />
United Kingdom, 73: 837-861.<br />
BOURDILLON, A., 1955. Les<br />
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Président Theodore Tissier. Revue des<br />
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BOUVIER, E.L., 1917. Pycnogonides provenant<br />
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de S.A.S. le Prince de Monaco (1885-<br />
1913). Résultats des Campagnes<br />
Scientifiques accomplies sur son Yacht par<br />
Albert I er Prince Souverain de Monaco,<br />
51: 1-56; Plates I-IV.<br />
CHILD, C.A., 1988. Pycnogoni<strong>da</strong> from<br />
Al<strong>da</strong>bra Atoll. Bulletin of the the<br />
Biological Society of Washington, 8: 45-<br />
78, 9 figures.<br />
CHILD, C.A., 1992. Shallow-water<br />
Pycnogoni<strong>da</strong> of the Gulf of Mexico.<br />
Memoirs of the Hourglass Cruises, 9(1):<br />
1-86.<br />
COSTA A.C. & S.P. ÁVILA, 2001.<br />
Macrobenthic mollusc fauna<br />
inhabiting Halopteris spp. subti<strong>da</strong>l<br />
fronds in São Miguel, Azores. Scientia<br />
Marina, 63: 117-126.<br />
FAGE, L., & J.H. STOCK, 1966.<br />
Pycnogonides. Résultats Scientifiques<br />
du Campagne de la Calypso aux îles de<br />
Cap Vert (1959). 7. Annales de I’Institut<br />
Océanographique de Monaco, 44: 315-<br />
327; 1-4.<br />
GOFAS, S., 1990. The littoral Rissoi<strong>da</strong>e<br />
and Anabathri<strong>da</strong>e of São Miguel,<br />
Azores. . In: MARTINS, A.M.F. (ed.),<br />
Proceedings of the First International<br />
Workshop of Malacology, São Miguel,<br />
Azores, 1988. Açoreana, Supplement<br />
[2]: 97-134.<br />
HEDGPETH, J.W., 1948. The<br />
Pycnogoni<strong>da</strong> of the western North<br />
Atlantic and the Caribbean.<br />
Proceedings of the United States National<br />
Museum, 97(3216): 157-342; 3 charts.<br />
HODGSON, T.V., 1915. The Pycnogoni<strong>da</strong><br />
collected by the Gauss in the Antarctic<br />
regions, 1901-3; preliminary report.<br />
Annals and Magazine of Natural History,<br />
(8), 15(85): 141-149.<br />
KRAPP, F., & R. SCONFIETTI, 1983.<br />
Ammothea hilgendorfi (Böhm, 1879), an<br />
adventitious pycnogonid new for the<br />
Mediterranean Sea. Marine Ecology,<br />
4(2): 123-132.<br />
LEBOUR, M.V., 1916. Notes on the life<br />
history of Anaphia petiolata (Kröyer).<br />
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11(1): 51-56.<br />
LOMAN, J.C.C., 1912. Note préliminaire<br />
sur les “Po<strong>dos</strong>omata” (Pycnogonides)
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du Musée Océanographique de<br />
Monaco. Bulletin de l’Institut<br />
Océanographique, Monaco, 238: 14 pp.;<br />
Plates A-K.<br />
McCLOSKEY, L.R., 1973. Pycnogoni<strong>da</strong>.<br />
Marine flora and fauna of the northeastern<br />
United States. United States<br />
Department of Commerce, NOAA<br />
Technical Reports NWFS CIRC-386: 1-<br />
12; 25 figs.<br />
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The origins of the coastal and marine<br />
flora and fauna of the Azores.<br />
Oceanography and Marine Biology: an<br />
Annual Review, 38: 13-84.<br />
MORTON, B., J.C. BRITTON & A.M.F.<br />
MARTINS 1998. Coastal Ecology of the<br />
<strong>Açores</strong>, 249 pp. Socie<strong>da</strong>de Afonso<br />
Chaves, Ponta Delga<strong>da</strong>.<br />
MÜLLER, H.-G., 1990. Flachwasser-<br />
Pantopoden von Bora-Bora,<br />
Gesellschaftsinseln, S-Pazifik, mit<br />
zwei<br />
Neubeschreibungen.<br />
Senckenbergiana marit., 70: 185-201.<br />
MUNILLA, T, & E. SANCHEZ, 1988.<br />
Ecologia de los primeros<br />
Picnogóni<strong>dos</strong> litorales Canarios. VI<br />
Simposio Iberico de Estudio del Bentos<br />
Marino, Palma de Mallorca, 9-22 Sep.<br />
1988. 1988: p. 61.<br />
SANCHEZ E,. & T. MUNILLA, 1989.<br />
Estudio ecologico de los primeros picnogoni<strong>dos</strong><br />
litorales de las islas<br />
Canarias. Cahiers de Biologie Marine,<br />
30: 49-67.<br />
SARS, G.O., 1891. Pycnogonidea.<br />
Norwegian North-Atlantic Expedition,<br />
1876-1878, 6(Zool. 20): 1-163; Plates I-<br />
XV.<br />
STAPLES, D.A., 1982. Pycnogoni<strong>da</strong> of the<br />
Calliope River and Auckland Creek,<br />
Queensland. Memoirs of the<br />
Queensland Museum, 20(3): 455-471.<br />
STOCK, J.H., 1952. Revision of the<br />
European representatives of the genus<br />
Callipallene Flynn. Beaufortia, 1(13): 1-<br />
15.<br />
STOCK, J.H., 1954. Four new Tanystylum<br />
species, and other Pycnogoni<strong>da</strong> from<br />
the West Indies. Studies on the Fauna of<br />
Curaçao, 5(24): 115-129.<br />
STOCK, J.H., 1955b. Pycnogoni<strong>da</strong> from<br />
the West Indies, Central America and<br />
the Pacific Coast of North America.<br />
Papers from Dr Th. Mortensen’s<br />
Pacific Expedition 1914-1916.<br />
Videnskabelige Meddelelser fra Dansk<br />
Naturhistorisk Forening i Kjøbenhavn,<br />
117: 209-266.<br />
STOCK, J.H., 1957. Pantopoden aus dem<br />
Zoologischen Museum Hamburg. 2 (=<br />
IV-VI). Mitteilungen aus dem<br />
Zoologischen Museum in Hamburg, 55:<br />
81-106.<br />
STOCK, J.H., 1971. Pycnogonides<br />
récoltés durant la campagne<br />
Noratlante en Atlantique Nord.<br />
Bulletin Zoölogisch Museum,<br />
Universiteit van Amster<strong>da</strong>m, 2(4): 25-28.<br />
STOCK, J.H., 1990. Macaronesian<br />
Pycnogoni<strong>da</strong>. CANCAP Project.<br />
Contribution No. 78. Zoologische<br />
Mededelingen, 63: 205-233.<br />
STOCK, J.H., 1992. Pycnogoni<strong>da</strong> from<br />
southern Haiti. Tijdschrift voor<br />
Entomologie, 135: 113-139.<br />
STOCK, J.H., 1994. Indo-West Pacific<br />
Pycnogoni<strong>da</strong> collected by some major<br />
oceanographic expeditions.<br />
Beaufortia, 44(3): 17-77.<br />
TIMMERMANN, G., 1932.<br />
Biogeographische Untersuchungen<br />
über die Lebensgemeinschaft des treibenden<br />
Golfkrautes. Zeitschrift für<br />
Morphologie und Oekologie des Tieres,<br />
25: 288-355.
AÇOREANA, Suplemento 6, Setembro 2009: 183-200<br />
THE TANAIDACEANS (ARTHROPODA: PERACARIDA: TANAIDACEA) OF SÃO<br />
MIGUEL, AZORES, WITH DESCRIPTION OF TWO NEW SPECIES, AND A NEW<br />
RECORD FROM TENERIFE<br />
Roger N. Bamber 1 & Ana Cristina Costa 2<br />
1<br />
The Natural History Museum, Cromwell Road, London SW7 5BD, U.K. e-mail: r.bamber@artoo.co.uk<br />
2<br />
CIBIO-Pólo <strong>Açores</strong>, Department of Biology, University of the Azores, 9501-801 Ponta Delga<strong>da</strong>, São Miguel,<br />
Azores, Portugal<br />
ABSTRACT<br />
During the Third International Workshop of Malacology and Marine Biology in São<br />
Miguel, Azores, in July 2006, sampling of the littoral and sublittoral benthos was undertaken<br />
in order to characterize the smaller marine arthropod fauna of this region, including<br />
tanai<strong>da</strong>ceans. In the event, 338 tanai<strong>da</strong>cean specimens representing three species were<br />
collected; two of these species, Leptochelia caldera and Paratanais martinsi, are new to science.<br />
In addition, previous tanai<strong>da</strong>cean material collected around São Miguel in 1996 and<br />
1997 was analyzed, from which a further 272 specimens (three species, one not found in<br />
2006) were identified. No apseudomorph tanai<strong>da</strong>ceans were found. All of the material is<br />
described, and an attempt is made to investigate the provenance of the Azorean<br />
tanai<strong>da</strong>cean fauna, although the general lack of <strong>da</strong>ta from the North-east Atlantic precludes<br />
any reasonable interpretation other than some possible links with the<br />
Mediterranean. However, recent material of Zeuxo exsargasso collected from Tenerife, in<br />
the Canary Islands, does suggest Macaronesian links with the West Atlantic.<br />
RESUMO<br />
Durante o 3º Workshop Internacional de Malacologia e Biologia Marinha em São<br />
Miguel, <strong>Açores</strong>, em Julho de 2006, fizeram-se amostragens do bentos litoral e sublitoral de<br />
modo a caracterizar a fauna de pequenos artrópodes marinhos dessa região, incluindo os<br />
tanaidáceos. Assim, recolheream-se 338 espécimens de tanaidáceos representando três<br />
espécies; duas dessas espécies, Leptochelia caldera e Paratanais martinsi, são novas para a<br />
ciência. Para além disso, analisou-se material recolhido previamente à volta de São Miguel<br />
em 1996 e 1997, do qual foram identifica<strong>dos</strong> 272 especimens ( três espécies, uma <strong>da</strong>s quais<br />
não encontra<strong>da</strong> em 2006). Não se encontraram tanaidáceos apseudomorfos. Todo o<br />
material foi descrito, e abordou-se a questão <strong>da</strong> proveniência <strong>da</strong> fauna tanaidácea<br />
Açoreana, embora a ausência generaliza<strong>da</strong> de <strong>da</strong><strong>dos</strong> do Nordeste Atlântico impeça<br />
qualquer interpretação razoável para além de algumas possíveis ligações com o<br />
Mediterrâneo. No entanto, material recente de Zeuxo exsargasso recolhido em Tenerife,<br />
Ilhas Canárias, sugere ligações Macaronésicas com o Atlântico Oeste.<br />
INTRODUCTION<br />
The Azores are a group of islands<br />
somewhat isolated in the north-east<br />
Atlantic, lying adjacent to the Mid-<br />
Atlantic Ridge some 1300 km west of<br />
Portugal and 1730 km southeast of<br />
Newfoundland. The main surface water<br />
currents reaching the archipelago bring<br />
waters from two directions: the Azores<br />
Drift, a diffuse southerly arm of the Gulf<br />
Stream breaking off from the North<br />
Atlantic Drift supplies water from the<br />
Americas, while the somewhat less-significant<br />
western eddies of the Canary<br />
Current bring waters from Spain and<br />
North Africa; below these, the midwater<br />
current brings warm, hyperhaline water
184 AÇOREANA<br />
2009, Sup. 6: 183-200<br />
from the Mediterranean outflow (Gofas,<br />
1990; Morton et al., 1998). This hydrography<br />
clearly has implications for the colonization<br />
of the islands by benthic marine<br />
species.<br />
Tanai<strong>da</strong>ceans are a group of the<br />
arthropods with minimal dispersive ability;<br />
the larvae are not planktonic, and<br />
there are only limited examples of adults<br />
swimming (Bamber, 1998). Some species<br />
are known to have spread in fouling communities<br />
on ship’s hulls (Bamber, 1977),<br />
and others are known to live in floating<br />
algae (Sieg, 1980) or ectoparasitically on<br />
turtle tests and on manatees (see Morales-<br />
Vela et al., 2008). It is therefore of some<br />
interest to determine the suite of species<br />
which has colonized the Azores archipelago,<br />
and their provenance.<br />
Previous records of tanai<strong>da</strong>ceans from<br />
the Azores are very sparse, and largely<br />
incidental, although Dollfus (1897)<br />
reported on the tanai<strong>da</strong>cean material collected<br />
around the Azores during the<br />
cruise of the Hirondelle in 1887 and 1888.<br />
All but two of the species recorded in litt.<br />
are from deep-water (>100 m; mostly<br />
>500 m). Dollfus (1897) reported<br />
Leptochelia savignyi Krøyer, 1842 from<br />
Horta; despite the controversy regarding<br />
earlier records of sibling species of this<br />
taxon, Dollfus’ records appear to be substantiated<br />
(see below); L. savignyi was<br />
described originally from Madeira, so its<br />
occurrence in the Azores is not surprising.<br />
Dollfus (1897) also recorded Tanais<br />
dulongii (Audouin, 1826) (as Tanais<br />
cavolinii Milne-Edwards, 1828) from Baïe<br />
de Fayal, and described as new<br />
T. grimaldii from Horta, distinguishing the<br />
two on the shape of the cephalon (his new<br />
species having a shorter cephalon) and<br />
the number of uropod articles; there is<br />
doubt whether his T. dulongii specimens<br />
were in fact of that species (see below);<br />
Morton et al. (1998) mention the occurrence<br />
of Tanais in littoral algal mats.<br />
Finally, the record of “Paratanais atlanticus”<br />
of Dollfus (1897) is incertae sedis, but<br />
not attributable to Paratanais (see below).<br />
The nine confirmed species recorded<br />
from around the Azores are:<br />
Suborder Apseudomorpha<br />
Leviapseudes lepto<strong>da</strong>ctylus (Bed<strong>da</strong>rd,<br />
1886), Azores 1830 m.<br />
Suborder Tanaidomorpha<br />
Superfamily Tanaoidea<br />
Tanais grimaldii Dollfus, 1897, Azores,<br />
littoral, 5-6 m.<br />
Superfamily Paratanaoidea<br />
Siphonolabrum mirabile Lang, 1872,<br />
Azores 3500-4165 m.<br />
Agathotanais hanseni Lang, 1971, E.<br />
Pacific & Azores, 2861-4165 m<br />
Leptognathia abyssorum (Dollfus, 1897),<br />
Azores, 1287 m.<br />
Paratyphlotanais richardi (Dollfus, 1897),<br />
W Ireland, Azores, 699-1287 m.<br />
Typhlotanais spiniventris Dollfus, 1897,<br />
Azores, 130-1287 m.<br />
Mesotanais dubius Dollfus, 1897,<br />
Azores, 1287 m.<br />
Leptochelia savignyi Krøyer, 1842,<br />
Azores, 5 to 6 m.<br />
During the Third International<br />
Workshop of Malacology and Marine<br />
Biology at Vila Franca do Campo, São<br />
Miguel, in July 2006, sampling of the littoral<br />
and sublittoral benthos was undertaken<br />
in order to characterize the smaller<br />
marine arthropod fauna of this region,<br />
including tanai<strong>da</strong>ceans. In the event, 338<br />
specimens representing three species<br />
were collected; two of these species are<br />
new to science. In addition, a previous<br />
collection from around the island was<br />
made available, from which a further 272<br />
specimens (three species, one additional<br />
to the above three) were identified. No<br />
apseudomorph tanai<strong>da</strong>ceans were found.
BAMBER & COSTA: TANAIDACEANS FROM SÃO MIGUEL 185<br />
In addition, recently collected material<br />
from Tenerife, in the Canary Islands,<br />
kindly supplied to us by Brian Morton,<br />
revealed a new record of a tanai<strong>da</strong>cean,<br />
relevant to the origins of the<br />
Macaronesian fauna. All of the material is<br />
described below.<br />
MATERIAL AND METHODS<br />
The present Azores material comes<br />
from two sources. During the Workshop<br />
at Vila Franca do Campo in July 2006, a<br />
number of littoral and infralittoral habitats<br />
on the island of São Miguel were sampled<br />
for tanai<strong>da</strong>ceans, including crevice<br />
habitats, macroalgae and soft sediments.<br />
The principal sampling areas were the littoral<br />
sediments, rocks and algae below<br />
the Clube Naval building (the old Vila<br />
Franca do Campo abattoir); the sediments<br />
and algae within the caldera of the Ilhéu<br />
de Vila Franca; and the soft sediments off<br />
Vila Franca do Campo (ca N37º 43’ W25º<br />
25’), from 12 to 200 m depth. Offshore<br />
sediments were sampled using a 0.025 m 2<br />
van Veen grab and various dredges. All<br />
samples were washed through a 0.5 mm<br />
mesh sieve, and specimens sorted alive.<br />
Some of these specimens were fixed in<br />
absolute ethanol to allow DNA analysis.<br />
Extensive material collected in 1996<br />
and 1997, from 11 (1996) and 20 (1997)<br />
infralittoral rocky-substratum sites<br />
around São Miguel, was also analysed in<br />
detail. Samples of algae (Stypocaulon scoparia,<br />
Halopteris filicina and Zonaria tournefortii)<br />
were collected by SCUBA diving at<br />
depths from between 5 and 16 m. Details<br />
of the sampling and protocols are given<br />
by Costa & Ávila (2001). The sampling<br />
sites, anti-clockwise around the Island<br />
from the north-west, were Mosteiros,<br />
Ponta <strong>da</strong> Ferraria, Santa Clara, Pesqueiro,<br />
Emissário, Sinaga, Atalha<strong>da</strong>, Ribeira <strong>da</strong><br />
Praia, Caloura, Porto de Vila Franca do<br />
Campo, Ilhéu de Vila Franca, Ribeira<br />
Quente, Faial <strong>da</strong> Terra, Nordeste, Porto<br />
Formoso, Ladeira de Velha, Ribeirinha,<br />
Lactoaçoreana, Cofaco and São Vicente.<br />
These sites variously represented exposed<br />
and sheltered shores, undisturbed, naturally<br />
disturbed (near shallow-water vent<br />
sites or stream mouths) and polluted<br />
shores.<br />
Finally, a collection of littoral algal<br />
turf was made from a rocky interti<strong>da</strong>l<br />
platform at Playa de Fanabe, Costa Adeje,<br />
Tenerife, Canary Islands, in June 2007,<br />
from which a further species not found in<br />
the São Miguel material was extracted.<br />
Terminology used herein recognizes<br />
the first pair of antennae as antennules,<br />
the second pair as the antennae. The first<br />
maxilla is termed the maxillule. The first<br />
pair of pereopods (of six) is the pair<br />
immediately posterior to the chelipeds.<br />
Serially repetitive body-parts, such as the<br />
pereonites and subdivisions of antennal<br />
flagella are segments, others (such as the<br />
parts of the limb) are articles. Total length<br />
is measured axially from the tip of the<br />
rostrum to the posterior edge of the pleotelson;<br />
measurements were made dorsally<br />
on the body and antennules, and laterally<br />
on the pereopods and antennae. The<br />
term ‘spines’ is used in the traditional<br />
sense to distinguish between rigid ‘thornlike’<br />
structures and the more flexible<br />
‘hair-like’ setae (in keeping with their etymology<br />
and all historic literature); nonarticulating<br />
spine-shaped extensions of<br />
the cuticle are considered to be apophyses;<br />
comb–rows of fine setules, occasionally<br />
present on maxillae and pereopod<br />
articles, inter alia, are referred to as<br />
microtrichia.<br />
Voucher and type-material has been<br />
lodged in the collections of The Natural<br />
History Museum, London (NHM). The<br />
higher taxonomy is based on Guţu & Sieg<br />
(1999).
186 AÇOREANA<br />
2009, Sup. 6: 183-200<br />
SYSTEMATICS<br />
SÃO MIGUEL MATERIAL<br />
Suborder TANAIDOMORPHA Sieg, 1980<br />
Superfamily Tanaoidea Dana, 1849<br />
Family Tanai<strong>da</strong>e Dana, 1849<br />
Subfamily Tanainae Dana, 1849<br />
Genus Tanais Latreille, 1831<br />
Tanais grimaldii Dollfus, 1897<br />
Figure 1A, B<br />
Sieg, 1980, pp. 84-91; Figure 31, 22.<br />
Material: 1 female with oostegites, 1<br />
female with empty brood pouch, 2<br />
subadult females, 2 neuters, 1 manca<br />
(Registration N os NHM.2007.764-771), Isl.<br />
24.2, drift algae within the flooded crater<br />
of the Ilhéu de Vila Franca, 24 July 2006,<br />
coll. A. Salvador, R. Robbins & R.B.; 12<br />
females with oostegites, 4 brooding<br />
females, 6 males, 148 neuters, 24 mancae<br />
(NHM.2007.772-781), Isl. 24.4, attached<br />
low-littoral algae, south wall of the flooded<br />
crater of the Ilhéu de Vila Franca, 24<br />
July 2006, coll. A. Salvador, R. Robbins &<br />
R.B.; 4 females with oostegites, 1 brooding<br />
female, 4 males, 31 subadult females,<br />
42 neuters, 28 mancae, Isl. 24.5, midlagoon<br />
algae, within the flooded crater of<br />
the Ilhéu de Vila Franca, 24 July 2006, coll.<br />
A. Salvador, R. Robbins & R.B.; 2 neuters,<br />
2 mancae (NHM.2007.782-785), WVF011,<br />
northeastern side of Ilhéu de Vila Franca<br />
do Campo, 16 m, scuba dive collection by<br />
Gonçalo Calado, José Pedro Borges, Joana<br />
Xavier, Paola Rachello, Patrícia Madeira,<br />
20 July 2006.<br />
1 brooding female, 1 neuter, 1 manca<br />
II, Mosteiros, 17 June 1997; 1 neuter, 1<br />
manca II, Ponta <strong>da</strong> Ferraria, 17 June 1997;<br />
3 females (1 brooding), 2 males, 1 manca,<br />
Emissário, 2 November 1996; 1 manca,<br />
Atalha<strong>da</strong>, 30 May 1997; 1 female, 4<br />
neuters, 15 mancae, Caloura, 26 June<br />
1997; 5 neuters, 1 manca, Ribeira Quente,<br />
November 1996; 1 manca, Ribiera Quente,<br />
18 June 1997; 1 manca, Nordeste, 21<br />
November 1996; 1 male, 1 brooding<br />
female, 1 neuter, 2 mancae. Nordeste, 2<br />
May 1997; 1 female, Porto Formoso, 30<br />
October 1996; 4 males, 1 female with oostegites,<br />
3 neuters, 2 mancae, Porto<br />
Formoso, 19 June 1997; 2 males, 3 mancae,<br />
Ladeira <strong>da</strong> Velha, 19 June 1997; 4 females<br />
(1 brooding, 2 with oostegites), 1 male,<br />
4neuters, 1 manca, Ribeirinha, 8 October<br />
1996; 2 females with oostegites, 7 neuters,<br />
5 mancae, Ribeirinha, 25 June 1997; 4<br />
females (1 brooding), 8 neuters, 9 mancae,<br />
Lactoaçoreana, 25 June 1997; 1 male, 1<br />
female, Cofaco, 7 October 1996; 4 females<br />
(1brooding), 7 males, 6 neuters, 1 manca,<br />
São Vicente, 7 October 1996; 3 females, 3<br />
neuters, 6 mancae, São Vicente, 6 May<br />
1997. All coll. A.C.C. & João Brum.<br />
Remarks: Tanais grimaldii is one of the only<br />
two littoral tanai<strong>da</strong>cean species recorded<br />
previously from the Azores: the typelocality<br />
is Horta (Faial), at 5 to 6 m depth<br />
(Dollfus, 1897). T. grimaldii is distinguished<br />
from its only northeast Atlantic<br />
congener, T. dulongii (Audouin, 1826) by<br />
the conformation of the laciniae mobili of<br />
the mandibles (see Sieg, 1980, Figure 31),<br />
but also adults of the present species have<br />
one more article in the uropod (basis plus<br />
three-segmented endopod: Figure 1B)<br />
than does T. dulongii (basis plus two-segmented<br />
endopod). Dollfus (1897) also<br />
recorded Tanais dulongii (Audouin, 1826)<br />
(as Tanais cavolinii Milne-Edwards, 1828)<br />
from Baie de Fayal, distinguishing it and<br />
T. grimaldii on the shape of the cephalon<br />
(his new species having a shorter<br />
cephalon) and the number of uropod articles;<br />
it is unclear whether his specimens<br />
of putative T. dulongii were fully mature,<br />
as only adult T. grimaldii have four segments<br />
to the uropod endopod (T. dulongii<br />
can be distinguished from immature<br />
T. grimaldii with three-segmented
BAMBER & COSTA: TANAIDACEANS FROM SÃO MIGUEL 187<br />
FIGURE 1. A, B, Tanais grimaldii Dollfus, 1897: A, dorsal; B, uropod; C to E, Leptognathia breviremis<br />
(Lilljeborg, 1864): C, dorsal; D, uropod; E, cheliped. (A redrawn after Sars, 1886; B, Azores specimen;<br />
C to E modified from Sars, 1899).<br />
endopods, as the penultimate segment is<br />
twice as long as the ultimate segment in<br />
the former, only slightly longer in the latter).<br />
Dollfus did not examine the<br />
mandibular structure, and indeed would<br />
have been unaware of its significance.<br />
It is likely that all previous records of<br />
Tanais dulongii from the Azores in fact<br />
refer to T. grimaldii. The present species is<br />
also recorded from the Italian<br />
Mediterranean (Gulf of Naples, Ischia<br />
and Linosa); there are unconfirmed<br />
records from the western Mediterranean<br />
and Casablanca (Sieg, 1980).<br />
All the material reported above was<br />
collected from algae at less than 17 m<br />
depth. Brooding females and mancae<br />
were present in all the months sampled<br />
(May, June, July, October and November).<br />
Superfamily Paratanaoidea Lang, 1949<br />
Family Anarthruri<strong>da</strong>e Lang, 1971<br />
Subfamily Leptognathiinae Sieg, 1976<br />
Genus Leptognathia Sars, 1882
188 AÇOREANA<br />
2009, Sup. 6: 183-200<br />
cf. Leptognathia breviremis (Lilljeborg,<br />
1864)<br />
Figure 1C to E<br />
Material: 1 headless specimen, Ponta <strong>da</strong><br />
Ferraria, 17 June 1997, coll. A.C.C. & João<br />
Brum.<br />
This <strong>da</strong>maged specimen is almost<br />
unidentifiable; the cheliped and uropods are<br />
appropriate to L. breviremis. This species is<br />
known from the eastern North Atlantic, but<br />
has been recorded (dubiously) from the<br />
North Pacific. A figure of L. breviremis (modified<br />
from Sars, 1899) is given to aid possible<br />
recognition of this taxon in the Azores in<br />
future (Figure 1, C to E).<br />
Family Leptochelii<strong>da</strong>e Lang, 1973<br />
Genus Leptochelia Dana, 1849<br />
Leptochelia caldera sp. nov.<br />
Figures 2, 3<br />
Material: 1 female with oostegites, holotype<br />
(NHM.2007.424), 1 male, allotype<br />
(NHM.2007.425), 13 females, paratypes<br />
(NHM.2007.426-435), Isl. 24.4, attached<br />
low-littoral algae, south wall of the flooded<br />
crater of the Ilhéu de Vila Franca, 24<br />
July 2006, coll. A. Salvador, R. Robbins &<br />
R.B.; 2 females, paratypes<br />
(NHM.2007.436-437), Isl. 24.5, midlagoon<br />
algae, within the flooded crater of<br />
the Ilhéu de Vila Franca, 24 July 2006, coll.<br />
A. Salvador, R. Robbins & R.B..<br />
2 females, Pesqueiro, 7 November<br />
1997; 3 males, 32 females (3 brooding), 5<br />
neuters, Emissário, 2 November 1996; 3<br />
females, 1 male, Emissário, 12 June 1997; 1<br />
manca, Sinaga, 30 May 1997; 4 males, 40<br />
females (2 brooding), 9 neuters, 2 mancae,<br />
Atalha<strong>da</strong>, 25 October 1996; 1 male, 14<br />
females, 7 neuters, Atalha<strong>da</strong>, 30 May<br />
1997; 1 female, Caloura, 26 June 1997; 1<br />
neuter, Faial <strong>da</strong> Terra, 12 June 1997; 1<br />
female, 1 neuter, Nordeste, 12 May 1997; 1<br />
male, 1 neuter, Ribeirinha, 8 October 1996;<br />
all coll. A.C.C. & João Brum.<br />
Description of female: body (Figure 2A)<br />
slender, holotype 3.6 mm long, 7.3 times<br />
as long as wide. Cephalothorax subrectangular,<br />
1.6 times as long as wide, as<br />
long as pereonites 2 and 3 together, with<br />
slight rostrum, eyelobes rounded, eyes<br />
present and black, single setae at posterior<br />
of eyelobes and posterolaterally. Six<br />
free pereonites; pereonite 1 shortest, pereonites<br />
2 and 3 subequal, 1.3 times as long<br />
as pereonite 1; pereonites 4 and 5 subequal<br />
(pereonite 4 longest) and 1.25 times<br />
as long as pereonite 2; pereonite 6 just<br />
longer than pereonite 1 (all pereonites<br />
respectively 1.9, 1.4, 1.3, 1.1, 1.0 and 1.4<br />
times as wide as long). Pleon of five free<br />
subequal pleonites bearing pleopods;<br />
each pleonite about 3.5 times as wide as<br />
long, with paired lateral setae. Pleotelson<br />
(Figure 2M) semicircular, 0.16 times as<br />
long as pleon, 2.8 times as wide as long,<br />
with paired lateral setae, paired posterolateral<br />
setae on each side and two distal<br />
setae.<br />
Antennule (Figure 2D) of four tapering<br />
articles, proximal article 3.6 times as<br />
long as wide, 1.5 times as long as distal<br />
three articles together, with two long<br />
outer and single short dorsal and inner<br />
setae; second article twice as long as wide,<br />
distal outer seta shorter than article; third<br />
article 1.3 times as long as second and<br />
with one aesthetasc; fourth article minute,<br />
eccentric, with five distal setae.<br />
Antenna (Figure 2G) of six articles,<br />
proximal article compact, naked; second<br />
article as long as wide, with single ventrodistal<br />
and dorsodistal slender spines;<br />
third article 1.3 times as long as wide,<br />
with dorsodistal slender spine; fourth<br />
article longest, three times as long as<br />
wide; fifth article half as long as fourth;<br />
sixth article minute.<br />
Labrum (Figure 2H) rounded, setose,<br />
typical of genus. Left mandible (Figure<br />
2I) with crenulate lacinia mobilis wider<br />
than pars incisiva, proximal crenulation
BAMBER & COSTA: TANAIDACEANS FROM SÃO MIGUEL 189<br />
FIGURE 2. Leptochelia caldera sp. nov., A, holotype female, dorsal; B, allotype male, dorsal; C, allotype<br />
male, lateral; D, female antennule; E, male antennule; F, male antenna; G, female antenna; H,<br />
labrum, lateral; I, left mandible; J, maxillule and maxilla; K, maxilliped; L, epignath; M, pleotelson<br />
and left uropod. Scale line = 1 mm for A, B and C, 0.2 mm for D to G and M, 0.1 mm for H to L.
190 AÇOREANA<br />
2009, Sup. 6: 183-200<br />
on pars incisiva, pars molaris with strong<br />
rugosity; right mandible similar but without<br />
lacinia mobilis. Labium typical of<br />
genus, distally finely setose, without<br />
palp. Maxillule (Figure 2J) with seven<br />
long and two short distal spines and<br />
setose margins; palp of two articles with<br />
two distal setae; maxilla simple, ovoid.<br />
Maxilliped (Figure 2K) palp first article<br />
naked, second article with one outer and<br />
three inner setae, and distal seta exceeding<br />
distal margin of third palp article;<br />
third and fourth articles with filtering<br />
rows of six and seven setae respectively,<br />
third article with two further inner distal<br />
setae, fourth article with submarginal<br />
outer seta; basis with three long setae<br />
extending to third palp article; endites<br />
distally with single outer seta and one<br />
inner rounded and two robust spatulate<br />
spines. Epignath (Figure 2L) elongate,<br />
arcuate, with setose margin distally and<br />
proximally.<br />
Cheliped (Figure 3A) with rounded,<br />
compact basis 1.9 times as long as wide,<br />
with inner distal seta; merus subtriangular<br />
with three ventral setae; carpus 1.9<br />
times as long as wide, with three midventral<br />
setae; propodus typical for the genus,<br />
fixed finger with three ventral and three<br />
inner setae, cutting edge crenulate, setal<br />
row at base of <strong>da</strong>ctylus of three setae;<br />
<strong>da</strong>ctylus with proximal seta.<br />
Pereopod 1 (Figure 3C) longer than<br />
other pereopods, coxa with seta and<br />
rounded apophyses; basis slender, 4.1<br />
times as long as wide, with dorsoproximal<br />
seta; ischium compact with one seta;<br />
merus just shorter than carpus; carpus<br />
with three distal setae, longest of which is<br />
0.4 times length of propodus; propodus<br />
as long as carpus and merus together,<br />
with three <strong>dos</strong>rodistal setae on slight<br />
mound, one ventrodistal seta; <strong>da</strong>ctylus<br />
slender, extending into shorter slender<br />
unguis, the two together as long as propodus.<br />
Pereopod 2 (Figure 3D) more compact<br />
than pereopod 1; basis 3 times as<br />
long as wide; ischium with 2 setae, longer<br />
seta longer than ischium width; merus<br />
longer than carpus, merus with strong<br />
ventrodistal spine, carpus with shorter<br />
ventrodistal spine; propodus with paired<br />
dorsodistal setae and ventrodistal spine;<br />
merus, carpus and propodus with ventral<br />
microtrichia; <strong>da</strong>ctylus and short unguis<br />
together 0.6 times as long as propodus;<br />
<strong>da</strong>ctylus (Figure 3E) with collar of fine<br />
setules at half length and dorsodistal<br />
setule. Pereopod 3 (Figure 3F) similar to<br />
pereopod 2, including longer seta on<br />
ischium and <strong>da</strong>ctylus setulation, but carpus<br />
longer than merus and with short<br />
outer distal seta.<br />
Pereopod 4 (Figure 3G) basis stout, 2.4<br />
times as long as wide; ischium with two<br />
short setae; merus shorter than carpus,<br />
merus with two short, ventrodistal<br />
spines, carpus with outer, ventral and<br />
inner curved distal spines; propodus<br />
longer than carpus, with two ventrodistal<br />
short spines, four dorsodistal setae, one<br />
as long as <strong>da</strong>ctylus; <strong>da</strong>ctylus and unguis<br />
partially fused into a claw, curved.<br />
Pereopods 5 (Figure 3H) and 6 as pereopod<br />
4, but with pereopod 5 propodus<br />
with fewer distal setae.<br />
Pleopods all alike, typical for the<br />
genus, with single dorsal plumose seta on<br />
basis.<br />
Uropod (Figure 2M) biramous, basis<br />
naked; exopod of one segment, 0.7 times<br />
as long as proximal endopod segment,<br />
outer distal seta longer than inner distal<br />
seta; endopod of six segments, distal segments<br />
slender.<br />
Description of male: typical primary male,<br />
half length of female (allotype length<br />
1.7 mm), body (Figure 2B, C) more compact,<br />
cephalon just longer than pereonites<br />
1 to 3 together, with large eyelobes bearing<br />
conspicuous black eyes; pereonite 1<br />
shortest, pereonites 2 to 6 progressively
BAMBER & COSTA: TANAIDACEANS FROM SÃO MIGUEL 191<br />
FIGURE 3. Leptochelia caldera sp. nov., A, female cheliped; B, male cheliped; C, pereopod 1; D, pereopod<br />
2; E, detail of distal articles of pereopod 2; F to H, pereopods 3, 4 and 5 respectively. Scale<br />
line = 0.2 mm for A to D and F to H, 0.1 mm for E.
192 AÇOREANA<br />
2009, Sup. 6: 183-200<br />
longer, pereonite 4 1.7 times as long as<br />
pereonite 1. Five free pleonites, subequal<br />
in length, pleotelson just longer than<br />
pleonite 5. Sexual dimorphism as follows.<br />
Antennule (Figure 2E) elongate, first<br />
peduncle article arcuate, 4 times as long<br />
as wide; second article 0.6 times as long as<br />
first with ventrodistal penicillate setae<br />
and 2 midventral simple setae; third article<br />
0.6 times as long as second, with dorsodistal<br />
seta; flagellum of 7 segments,<br />
first with 4 proximal and 5 distal aesthetascs,<br />
segments 2 to 5 with 4, 4, 3 and 3<br />
distal aesthetascs respectively; segments 6<br />
and 7 more slender than others. Antenna<br />
(Figure 2F) similar to that of female but<br />
more compact. Mouthparts atrophied.<br />
Cheliped (Figure 3B) larger than that<br />
of female; carpus slender, 3.6 times as<br />
long as wide, with ventrodistal invagination<br />
to accommo<strong>da</strong>te propodus on reflexion;<br />
propodus fixed finger shorter than<br />
palm, with two inner tooth-like apophyses<br />
on cutting edge; moveable finger with<br />
spinules along cutting edge.<br />
Pleopods more setose than those of<br />
female.<br />
Etymology: caldera (from the Spanish<br />
cauldron) is a volcanic crater, the 2006<br />
type-material of this species having been<br />
collected from the sea-water-flooded<br />
crater of Ilhéu de Vila Franca.<br />
Remarks: there are four recorded species<br />
of Leptochelia with only 3 maxilliped<br />
basis setae, none of them occurring in the<br />
North Atlantic or Mediterranean, viz.<br />
L. itoi Ishimaru, 1982 (from Japan),<br />
L. lusei Bamber & Bird, 1997 (from Hong<br />
Kong), L. nobbi Bamber, 2005 (from<br />
Western Australia) and a species from<br />
Queensland, Australia (Bamber, in<br />
press). Of these four, only L. nobbi has a<br />
proximal antennule article more than 3<br />
times as long as wide, but that species<br />
has a compact basis to pereopod 1 (only<br />
three times as long as wide) and a uropod<br />
exopod only half as long as the<br />
proximal endopod segment length.<br />
Despite its much more compact proximal<br />
antennule peduncle article (2.5 times<br />
as long as wide), L. itoi shows most similarity<br />
to L. caldera sp. nov., but the cheliped<br />
basis of the Japanese species is<br />
more compact (1.5 times as long as<br />
wide), the distal seta of antennule<br />
peduncle article 2 is as long as the article<br />
(shorter in L. caldera), and the <strong>da</strong>ctylus<br />
plus claw of the first pereopod is much<br />
longer than the propodus (1.33 times as<br />
long, compared with subequal in length<br />
in L. caldera).<br />
The number of maxilliped basis setae<br />
in L. neapolitana Sars, 1882 is not known,<br />
but that species again differs from<br />
L. caldera in that the proximal antennule<br />
peduncle article is shorter (three times as<br />
long as wide), the uropod exopod is less<br />
than half the length of the proximal<br />
endopod segment, the <strong>da</strong>ctylus plus<br />
claw of the first pereopod is much longer<br />
than the propodus (1.36 times as long)<br />
and the cheliped basis more compact<br />
(1.35 times as long as wide).<br />
The male of the present species is<br />
generally very similar to the male of<br />
L. dubia sensu Sars, 1886 (non Krøyer,<br />
1842), but that species has longer anterior<br />
pereonites, and is without the degree<br />
of ventrodistal invagination on the cheliped<br />
carpus shown by L. caldera (and the<br />
female of Sars’ species has five maxilliped<br />
basis setae). The male of L. neapolitana<br />
has a similar cheliped to the present<br />
species, but has fewer antennule flagellum<br />
segments and more attenuate pereonites.<br />
None of the species described previously<br />
has the peculiar collar of setules at<br />
half length on the <strong>da</strong>ctylus of pereopods<br />
two and three shown by Leptochelia<br />
caldera.
BAMBER & COSTA: TANAIDACEANS FROM SÃO MIGUEL 193<br />
Dollfus (1897) recorded a male and a<br />
female of Leptochelia savignyi Krøyer,<br />
1842 from Horta at 5 to 6 m depth. This<br />
taxon has been the subject of some confusion<br />
over the last 150 years (including<br />
erroneous synonymy with L. dubia<br />
Krøyer, 1842), and it is now apparent<br />
that numerous species of Leptochelia<br />
await distinction based on morphological<br />
features of both genders which were<br />
not examined in any detail before<br />
Ishimaru (1985) (see Bamber, 2005 for<br />
discussion). From his subsequent report<br />
on Mediterranean and Atlantic species<br />
(Dollfus, 1898), it is apparent that<br />
Dollfus distinguished L. savignyi correctly<br />
on the basis of four longer articles in<br />
the antennule of the female (inter alia).<br />
There is debate whether the extra antennular<br />
article is an intermediate feature of<br />
a female changing into a male in a genus<br />
known to show progynous hermaphroditism<br />
(e.g. Smith, 1906); while this trend<br />
has been observed in some taxa of<br />
Leptochelia (R. Heard, pers. comm.), the<br />
male of L. savignyi sensu Sars, 1886 is a<br />
primary male, while Larsen & Rayment<br />
(2002) found this antennular structure a<br />
consistent feature of females of their new<br />
species L. elongata, including an ovigerous<br />
paratype. Dollfus (1898) reported a<br />
number of collections including females<br />
attributed to L. savignyi from the<br />
Mediterranean and the eastern Atlantic,<br />
implying a frequency of this antennular<br />
morphology unlikely to be shown only<br />
by transitional hermaphrodite specimens.<br />
His records from the Azores are<br />
thus accepted as valid, and L. savignyi<br />
sensu Sars, 1886 (see Figure 6A, B) is<br />
accepted as the same as L. savignyi<br />
Krøyer, 1842.<br />
Krøyer (1842) named a third species<br />
of Leptochelia, “Tanais” edwardsii, also<br />
from Madeira, but based only on the<br />
male. While it is possible that this taxon<br />
may never be confirmed (it is assumed to<br />
be the male of L. savignyi), from his figure<br />
(Krøyer, 1842: pl.2: Figures 13-19) it<br />
does not have the same antennular or<br />
pleotelson proportions as L. caldera.<br />
Family Paratanai<strong>da</strong>e Lang, 1949<br />
Sufamily Paratanaidinae Lang, 1949<br />
Genus Paratanais Dana, 1852<br />
Paratanais martinsi sp. nov.<br />
Figures 4, 5<br />
?Paratanais euelpis Monod, 1925, non<br />
Paratanais euelpis Barnard, 1920.<br />
Non- Paratanais atlanticus Dollfus,<br />
1897 (incertae sedis)<br />
Material: 1 female with brood pouch (in<br />
tube), holotype (NHM.2007.438), 1 female<br />
dissected, 2 females, 1 manca, 1 headless<br />
female, paratypes,(NHM.2007.439-440),<br />
WVF040, off Amora, Ponta Garça, São<br />
Miguel, Azores, 37º42’720”N<br />
25º21’554”W, 37.8 m depth, small dredge<br />
sample, 26 July 2006, coll. António de<br />
Frias Martins & Jerry Harasewych.<br />
Description of female: body (Figure 4A)<br />
elongate, slender, 4.2 mm long, eight<br />
times as long as wide, colour translucent<br />
white, eyes black. Cephalothorax subrectangular,<br />
1.2 times as long as wide, with<br />
slight rounded rostrum, single mid-lateral<br />
setae; eyes present, pigmented. Six free<br />
cylindrical pereonites; pereonite 1 shortest,<br />
with single anterolateral setae; pereonites<br />
2 and 3 subequal, twice as long as<br />
pereonite 1, also with single anterolateral<br />
setae; pereonites 4 and 5 subequal (pereonite<br />
4 longest), 1.2 times as long as pereonite<br />
2, pereonite 6 just shorter than pereonite<br />
2 (all pereonites respectively 2, 1.1,<br />
1.0, 0.9, 0.9 and 1.2 times as wide as long).<br />
Pleon of five free subequal pleonites bearing<br />
pleopods; pleonites 4.5 times as wide<br />
as long; pleonites 1 to 4 with one<br />
plumose, articulating lateral seta on each<br />
side, pleonite 5 with simple lateral seta.
194 AÇOREANA<br />
2009, Sup. 6: 183-200<br />
Pleotelson semicircular, short, 1.9 times as<br />
wide as long, distally with paired dorsal<br />
and paired terminal setae.<br />
Antennule (Figure 4B) of four articles,<br />
proximal article 2,3 times as long as wide,<br />
second article 1.3 times as long as wide,<br />
about one-third length of first, with dorsal<br />
seta longer than article length; third<br />
article nearly two-thirds length of second;<br />
distal article slender, longer than second<br />
and third articles together, with five distal<br />
setae and single aesthetasc.<br />
Antenna (Figure 4C) of six articles,<br />
proximal article compact, naked; second<br />
article with long ventrodistal and short<br />
dorsodistal apophyses each bearing seta;<br />
third article as long as wide, naked, with<br />
dorsodistal spine; fourth article just<br />
longer than second, with two distal simple<br />
setae; fifth article half as long as<br />
fourth with two distal setae; sixth article<br />
minute with five longer and one shorter<br />
distal setae.<br />
Labrum (Figure 4D) apically rounded,<br />
setose. Left mandible (Figure 4E)<br />
with crenulate pars incisiva and wide,<br />
crenulate lacinia mobilis; pars molaris<br />
robust with elaborate marginal “teeth”.<br />
Right mandible (Figure 4F) without<br />
lacinia mobilis, pars molaris less elaborate.<br />
Labium (Figure 4G) simple, finely<br />
setose, with fine outer marginal spinule,<br />
without palp. Maxillule (Figure 4H)<br />
with seven longer and two shorter distal<br />
spines, palp slender with two long distal<br />
setae; maxilla ovoid, naked. Maxilliped<br />
(Figure 4I) endites characteristic of<br />
genus, wide with denticulate outer margin,<br />
two inner distal ovate tubercles and<br />
single inner seta; palp first article naked,<br />
second article inner margin with two<br />
simple setae and shorter distal spine,<br />
outer margin with distal seta; third article<br />
with three inner bidenticulate spines,<br />
adjacent shorter simple spine; fourth<br />
article with four inner bidenticulate<br />
spines, single inner submarginal and<br />
outer simple setae; single inner spine on<br />
basis exceeding distal margin of endites.<br />
Epignath (Figure 4J) ribbon-like,<br />
glabrous but with two fine distal setae.<br />
Cheliped (Figure 5A) compact, carpus<br />
1.2 times as long as wide; propodus<br />
wider than long, fixed finger short with<br />
lamellate apophyses on cutting edge, terminal<br />
spine indistinct; <strong>da</strong>ctylus with<br />
dorsoproximal simple seta.<br />
Pereopod 1 (figue 5B) longer than<br />
others, coxa simple with seta; basis slender,<br />
arcuate, five times as long as wide;<br />
ischium compact with single seta; merus<br />
1.5 times as long as carpus; propodus 1.2<br />
times as long as merus, with one ventral<br />
and three dorsal distal setae; <strong>da</strong>ctylus<br />
with distinct, slender claw, both together<br />
as long as propodus. Pereopod 2 (Figure<br />
5C) similar to pereopod 1, but more compact,<br />
basis 3.1 times as long as wide,<br />
ischium with tow setae, merus shorter<br />
than carpus with ventral microtrichia<br />
and ventrodistal spine, carpus with ventral<br />
microtrichia, two ventrodistal and<br />
one larger inner distal spines. Pereopod<br />
3 (Figure 5D) similar to pereopod 2.<br />
Pereopod 4 (Figure 5E) basis robust, 2.2<br />
times as long as wide; merus 0.8 times as<br />
long as carpus, each with spination as<br />
pereopod 3; propodus longer than carpus<br />
with mid-dorsal penicillate seta,<br />
dorsodistal slender spine and ventrodistal<br />
stout spine; <strong>da</strong>ctylus and claw forming<br />
unguis, curved, two-thirds as long as<br />
propodus. Pereopod 5 (Figure 5F) as<br />
pereopod 4. Pereopod 6 (Figure 5G) as<br />
pereopod 4, but propodus more compact<br />
with two ventrodistal spines and three<br />
dorsodistal setae adjacent to slender<br />
spine.<br />
Pleopods (Figure 4K) all alike, with<br />
naked basis, endopod with single inner<br />
plumose seta; exopod without setae on<br />
inner margin.<br />
Uropod (Figure 5H) basis naked,<br />
endopod of two segments, exopod of one
BAMBER & COSTA: TANAIDACEANS FROM SÃO MIGUEL 195<br />
FIGURE 4. Paratanais martinsi sp. nov., A, holotype, dorsal; B, antennule; C, antenna; D, labrum;<br />
E, left mandible; F, right mandible; G, labium; H, maxillule and maxilla; I, maxilliped; J, epignath:<br />
K, pleopod (plumose nature of all setae not shown). Scale line = 1 mm for A, 0.2 mm for B and C,<br />
0.1 for D to J.
196 AÇOREANA<br />
2009, Sup. 6: 183-200<br />
segment, shorter than proximal segment<br />
of endopod.<br />
Male unknown.<br />
Etymology: named after António de Frias<br />
Martins, in gratitude for his assistance in<br />
attending the workshop, and exemplary<br />
hospitality.<br />
Remarks: the genus Paratanais has been<br />
capably diagnosed by Lang (1973). The<br />
only species from the North Atlantic<br />
attributed previously to Paratanais are all<br />
incertae sedis. Bate & Westwood (1868)<br />
described “Paratanais” rigidus from one<br />
specimen collected from Laminaria holdfasts<br />
off Glasgow, western Scotland: while<br />
their four-articled antennule is appropriate,<br />
they carefully describe the uropod<br />
rami as both being of one segment, and an<br />
elongate, slender chela; their species is<br />
not a member of the genus Paratanais, but<br />
with the inadequate description and figures<br />
must remain incertae sedis. P. limicola<br />
FIGURE 5. Paratanais martinsi sp. nov., A, cheliped; B to G, pereopods 1 to 6 respectively; H, uropod.<br />
Scale line = 0.2 mm for A to G, 0.15 mm for H.
BAMBER & COSTA: TANAIDACEANS FROM SÃO MIGUEL 197<br />
Harger, 1878 (see Harger, 1880, for<br />
description and figures) has a three-articled<br />
antennule, and the uropod has two<br />
segments in the exopod and five in the<br />
endopod: Harger himself (1880) moved<br />
this species, apparently correctly, to<br />
Leptochelia. Dollfus (1897) described<br />
“Paratanais” atlanticus from 130 m depth<br />
off the Azores, based on a male and two<br />
females; although the description is<br />
somewhat cursory, and the figures inadequate,<br />
his species clearly had a three-articled<br />
antennule in the female, and the uropod<br />
had a two-segmented exopod and a<br />
three-segmented endopod; Dollfus’<br />
species thus cannot be a member of the<br />
genus Paratanais. Finally, Monod (1925)<br />
suspected a specimen from 110 m depth<br />
off Morocco to be P. euelpis Barnard, 1920<br />
(a species adequately refigured by Lang,<br />
1973), but without full confidence (and<br />
without description or figure). It is possible<br />
that his specimen, if indeed of this<br />
genus, was of the present species.<br />
In having the setose apophyses on the<br />
second article of the antenna, more characteristic<br />
of species of Leptochelia,<br />
Paratanais martinsi sp. nov. is similar only<br />
to P. gaspodei Bamber, 2005, with which it<br />
also shares the elongate, slender uropod<br />
segments, and the short chela. The present<br />
species differs from P. gaspodei in a<br />
number of characters, including being<br />
generally more slender (pleonites 3, 4 and<br />
5 as long as or longer than wide, all wider<br />
than long in P. gaspodei), with more slender<br />
articles in the antennule and antenna<br />
(proximal peduncle article of antennule<br />
less than twice as long as wide in<br />
P. gaspodei), in the inner spines on the<br />
maxilliped basis exceeding the distal margin<br />
of the endites (not reaching the margin<br />
in P. gaspodei), and with the merus of<br />
pereopod 1 being 1.5 times as long as the<br />
carpus (subequal in length in P. gaspodei).<br />
With regard to the possible Moroccan<br />
record of Monod (1925), P. euelpis also has<br />
a shorter merus to pereopod 1, and is<br />
without the apophyses on the second article<br />
of the antenna, as well as differences<br />
in mouthpart setation.<br />
TENERIFE MATERIAL<br />
Superfamily Tanaoidea Dana, 1849<br />
Family Tanai<strong>da</strong>e Dana, 1849<br />
Subfamily Pancolinae Sieg, 1980<br />
Genus Zeuxo Templeton, 1840<br />
Zeuxo (Parazeuxo) exsargasso Sieg, 1980<br />
Figure 6 C, D<br />
Zeuxo (Parazeuxo) exsargasso<br />
1980, 217-221, figure 61.<br />
Sieg,<br />
Material: 3 males, 3 females with<br />
oostegites, 1 brooding female<br />
(NHM.2007.757-763), 1 female with<br />
oostegites (dissected), rocky interti<strong>da</strong>l<br />
platform covered in algal turf, Playa de<br />
Fanabe, Costa Adeje, Tenerife, 27 June<br />
2007. Coll. B Morton.<br />
Remarks: Zeuxo exsargasso was only<br />
known from the type collection from<br />
floating Sargassum natans, 20 miles southeast<br />
of Bermu<strong>da</strong> (Sieg, 1980). Its presence<br />
in the Canary Islands implies the possibility<br />
of transport by drift from America via<br />
the Gulf Stream and the Azores and<br />
Canary Currents. The only other recorded<br />
species of Zeuxo in north-eastern<br />
Atlantic waters is the only-distantly-related<br />
Zeuxo (Zeuxo) holdichi Bamber, 1990,<br />
known from the Atlantic shores of France<br />
and Portugal and the English Channel<br />
(Bamber, 1990; & unpubl. <strong>da</strong>ta). Zeuxo<br />
species are distinguished from Tanais<br />
species in their having five dorsallydemarcated<br />
pleonites (Tanais has only<br />
four), and no dorsal rows of plumose<br />
setae on the pleon (Tanais has conspicuous<br />
rows on pleonites 1 and 2); the uropod<br />
of Z. exsargasso has five segments<br />
(Figure 6D).
198 AÇOREANA<br />
2009, Sup. 6: 183-200<br />
DISCUSSION<br />
There are now five species of shallowwater<br />
tanai<strong>da</strong>cean recorded from the<br />
Azores, Tanais grimaldii, Leptochelia savignyi<br />
sensu stricto, Leptochelia caldera,<br />
Paratanais martinsi and the unconfirmed<br />
Leptognathia from Ponta <strong>da</strong> Ferraria.<br />
The present <strong>da</strong>ta demonstrate that<br />
Azorean tanai<strong>da</strong>cean fauna inhabits littoral<br />
to infralittoral algae, is generally<br />
sparse, but may show a relatively high<br />
degree of endemism. For the only species<br />
occurring in the 1996 and 1997 <strong>da</strong>ta in sufficient<br />
numbers for interpretation, Tanais<br />
grimaldii, no trends were detected in relation<br />
to disturbance or exposure.<br />
Unfortunately, these taxa give little<br />
information on the origins of the Azorean<br />
fauna. The Leptognathia specimen tells<br />
nothing. The two species described as<br />
new above are as yet unknown from elsewhere:<br />
Leptochelia is a worldwide genus,<br />
while Paratanais is predominantly southern<br />
hemisphere in distribution (Australia,<br />
Subantarctica, South Africa) but also<br />
found in the Indo-West Pacific, the Kurile<br />
Islands and California.<br />
T. grimaldii has been recorded from<br />
the Mediterranean (Adriatic) by Sars<br />
(1886, as T. cavolinii), his figure clearly<br />
showing the appropriate uropod structure.<br />
Sieg (1980) attributes the record of<br />
T. chevreuxi from the Moroccan coast by<br />
Monod (1925) to T. grimaldii, but regards<br />
it as doubtful, as he did the record from<br />
the Bay of Naples by Smith (1906); neither<br />
author gives a description or figure, and<br />
the decision of Sieg (loc. cit.) is based on<br />
their attributing the authority for their<br />
name to Sars, 1886. Both of these records<br />
are surely incertae sedis. There are no pub-<br />
FIGURE 6. A and B, Leptochelia savignyi: A, dorsal; B, antennule (redrawn after Sars, 1886). C and<br />
D, Zeuxo (Parazeuxo) exsargasso (Tenerife specimen): A, dorsal; B, pleotelson and uropods, dorsal.
BAMBER & COSTA: TANAIDACEANS FROM SÃO MIGUEL 199<br />
lished records of Tanais species from the<br />
Canary Islands or from Madeira.<br />
While there has been confusion over<br />
the years regarding Leptochelia savignyi<br />
(see above), the type locality is Madeira,<br />
and the only other valid records (other<br />
than those of Dollfus, 1897; 1898) are<br />
those of Sars (1886) from the<br />
Mediterranean, from the Ligurian Sea<br />
and off Sicily.<br />
Thus there are a few indications that<br />
the Azorean tanai<strong>da</strong>cean fauna may have<br />
links with the Mediterranean, but not<br />
elsewhere. Morton & Britton (2000)<br />
found that most components of the<br />
Azorean marine fauna show affiliation<br />
with the Mediterranean and southern<br />
Europe. However, the discovery of Zeuxo<br />
exsargasso in Tenerife strongly implies colonization<br />
from the western Atlantic to<br />
Macaronesia via the Gulf Stream, the<br />
Azores Current and the Canary Current<br />
(see Timmermann, 1932, for a discussion<br />
on faunistic transport in Sargassum).<br />
It is undoubtedly the case that the<br />
tanai<strong>da</strong>cean fauna of Macaronesia is very<br />
understudied, and that of the<br />
Mediterranean and Atlantic coasts of<br />
Europe and North Africa is little better<br />
known, still relying heavily on 19th century<br />
information. At the same time the<br />
speciation of such taxa as Leptochelia<br />
around the North-east Atlantic and<br />
Mediterranean needs proper study.<br />
ACKNOWLEDGEMENTS<br />
We are indebted to Roni Robbins for<br />
assistance in the field collecting and sample<br />
analysis in 2006, to Andreia Salvador<br />
for sampling assistance in Ilhéu de Vila<br />
Franca, to João Brum for assistance in the<br />
diver collections in 1996 and 1997, to<br />
Brian Morton for collecting the Tenerife<br />
material, to António de Frias Martins for<br />
the organisation of, and inviting us to, the<br />
2006 Workshop, and to the other participants<br />
at the workshop for samples and<br />
for entertainment.<br />
LITERARURE CITED<br />
BAMBER, R.N., 1977. On mobile littoral<br />
environments. Porcupine Newsletter,<br />
1(4): 62-63.<br />
BAMBER, R.N., 1990. A new species of<br />
Zeuxo (Crustacea: Tanai<strong>da</strong>cea) from<br />
the French Atlantic coast. Journal of<br />
Natural History, 24: 1587-1596.<br />
BAMBER, R.N., 1998. Zoogeographic<br />
trends in some Hong Kong arthropods.<br />
In: MORTON, B. (ed.), The<br />
Marine Biology of the South China Sea.<br />
Proceedings of the Third International<br />
Conference on the Marine Biology of the<br />
South China Sea. Hong Kong, 28 October<br />
- 1 November 1996. pp. 91-112. Hong<br />
Kong: Hong Kong University Press.<br />
BAMBER, R.N., 2005. The Tanai<strong>da</strong>ceans<br />
(Arthropo<strong>da</strong>: Crustacea: Peracari<strong>da</strong>:<br />
Tanai<strong>da</strong>cea) of Esperance, Western<br />
Australia, Australia. In: WELLS, F.E.,<br />
D.J. WALKER & G.A. KENDRICK<br />
(eds), Proceedings of the Twelfth International<br />
Marine Biological Workshop:<br />
The Marine Flora and Fauna of<br />
Esperance, Western Australia, pp. 613-<br />
728. Western Australia Museum,<br />
Perth.<br />
BATE, C.S., & J.O. WESTWOOD, 1868. A<br />
History of the British Sessile-Eyed<br />
Crustacea, 2: 117-154. John Van Voorst,<br />
London.<br />
COSTA, A.C., & S.P. ÁVILA, 2001.<br />
Macrobenthic mollusc fauna<br />
inhabiting Halopteris spp. subti<strong>da</strong>l<br />
fronds in São Miguel, Azores. Scientia<br />
Marina, 63: 117-126.<br />
DOLLFUS, A., 1897. Note préliminaire<br />
sur les Tanaidæ recueillis aux <strong>Açores</strong><br />
pen<strong>da</strong>nt les campagnes de l’Hirondelle<br />
(1887-1888). Bulletin de la Société<br />
Zoologique, France, 21: 207-215.<br />
DOLLFUS, A., 1898. Campagnes de la
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Melita. Tanai<strong>da</strong>e récoltes par M. Ed.<br />
Chevreux <strong>da</strong>ns l’Atlantique et <strong>da</strong>ns la<br />
Méditerranée. Memoires de la Société<br />
Zoologique, France, 11: 33-47.<br />
GOFAS, S., 1990. The littoral Rissoi<strong>da</strong>e<br />
and Anabathri<strong>da</strong>e of São Miguel,<br />
Azores. In: MARTINS, A.M.F. (ed),<br />
The Marine Fauna and Flora of the<br />
Azores (Proceedings of the First<br />
International Workshop of Malacology,<br />
São Miguel, 1988). Açoreana, 1990<br />
Supplement: 97-134.<br />
GUTU, M., & J. SIEG, 1999. Ordre<br />
Tanaï<strong>da</strong>cés (Tanai<strong>da</strong>cea Hansen,<br />
1895). Mémoires de l’Institute<br />
Océanographique, Monaco, 19: 353-389.<br />
HARGER, O., 1880. Appendix E. The<br />
Natural History of Marine Animals,<br />
XIV. Report on the marine Isopo<strong>da</strong> of<br />
New England and adjacent waters.<br />
Report of the United States Commission<br />
of Fish and Fisheries, 6: Report of the<br />
Commissioner for 1878, pp. 295-449,<br />
plates 1-13.<br />
ISHIMARU, S-i., 1985. A new species of<br />
Leptochelia (Crustacea, Tanai<strong>da</strong>cea)<br />
from Japan, with a redescription of L.<br />
savignyi (Kroyer, 1842). Publications of<br />
the Seto Marine Biological Laboratory,<br />
30(4/6): 241-267.<br />
KRØYER, H., 1842. Nye Arter af Slægten<br />
Tanais. Naturhistorishe Tiddskrift, 4:<br />
167-188.<br />
LANG, K., 1973. Taxonomische und phylogenetische<br />
Untersuchungen über<br />
die Tanai<strong>da</strong>ceen (Crustacea). 8. Die<br />
Gattung Leptochelia Dana, Paratanais<br />
Dana, Heterotanais G.O. Sars und<br />
Nototanais Richardson. Dazu einige<br />
Bemerkungen über die Monokonophora<br />
und ein Nachtrag.<br />
Zoologica Scripta, 2: 197-229.<br />
LARSEN, K., & H. RAYMENT, 2002. New<br />
species of Leptochelia (Crustacea:<br />
Tanai<strong>da</strong>cea) from the An<strong>da</strong>man Sea,<br />
north-eastern Indian Ocean. Phuket<br />
Marine Biological Center Special<br />
Publication, 32(1): 17-31.<br />
MONOD, T., 1925. Tanai<strong>da</strong>cés et isopodes<br />
aquatiques de l’Afrique occidentale<br />
et septentrionale. 1 er partie:<br />
Tanai<strong>da</strong>cea, Anthuri<strong>da</strong>e, Valvifera.<br />
Bulletin de la Société des Sciences<br />
Naturelles du Maroc, 5(3): 61-85.<br />
MORALES-VELA, B., E. SUAREZ-<br />
MORALES, J. PADILLA-SALDIVAR<br />
& R.W. HEARD, 2008. The tanaid<br />
Hexapleomera robusta (Crustacea:<br />
Peracari<strong>da</strong>) from the Caribbean manatee,<br />
with comments on other crustacean<br />
epibionts. Journal of the Marine<br />
Biological Association of the United<br />
Kingdom, 88: 591-596.<br />
MORTON, B., & J.C. BRITTON, 2000.<br />
The origins of the coastal and marine<br />
flora and fauna of the Azores.<br />
Oceanography and Marine Biology: an<br />
Annual Review, 38: 13-84.<br />
MORTON, B., J.C. BRITTON & A.M.F.<br />
MARTINS, 1998. Coastal Ecology of the<br />
<strong>Açores</strong>, 249 pp. Socie<strong>da</strong>de Afonso<br />
Chaves, Ponta Delga<strong>da</strong>.<br />
SARS, G.O., 1886. Nye bidrag til kundskaben<br />
om Middelhavets invertebratfauna.<br />
III. Middelhavets saxisopoder<br />
(Isopo<strong>da</strong> chelifera). Archiv for<br />
Mathematik og Naturvidenskab, 11: 263-<br />
368.<br />
SARS, G.O., 1899. An account of the<br />
Crustacea of Norway with short descriptions<br />
and figures of all the species. II.<br />
Isopo<strong>da</strong>, 265 pp. + pls. 1-18. Bergen<br />
Museum, Christiania.<br />
SIEG, J., 1980. Taxonomische Monographie<br />
der Tanai<strong>da</strong>e Dana 1849<br />
(Crustacea: Tanai<strong>da</strong>cea). Abhandlungen<br />
der Senckenbergischen Naturforschenden<br />
Gesellschaft, 537: 1-267.<br />
SMITH, G., 1906. High and low dimorphism,<br />
with an account of certain<br />
Tanai<strong>da</strong>e of the Bay of Naples.<br />
Mitteilungen aus der Zoologischen<br />
Station zu Neapel, 17: 312-340.<br />
TIMMERMANN, G., 1932. Biogeographische<br />
Untersuchungen über die<br />
Lebensgemeinschaft des treibenden<br />
Golfkrautes. Zeitschrift für Morphologie<br />
und Oekologie des Tieres, 25: 288-355.
AÇOREANA, Suplemento 6, Setembro 2009: 201-210<br />
THE SOFT-SEDIMENT INFAUNA OFF SÃO MIGUEL, AZORES, AND A<br />
COMPARISON WITH OTHER AZOREAN INVERTEBRATE HABITATS<br />
Roger N. Bamber & Roni Robbins<br />
The Natural History Museum, Cromwell Road, London SW7 5BD, U.K. e-mail: roger.bamber@artoo.co.uk<br />
ABSTRACT<br />
During the Third International Workshop of Malacology and Marine Biology in the<br />
Azores in July 2006, sampling of the littoral and sublittoral soft-sediment benthos around<br />
Vila Franca do Campo, São Miguel, was undertaken in order to characterize the benthic<br />
infaunal communities, and to compare the faunal density and diversity with the communities<br />
associated with algae.<br />
The sedimentary infauna was particularly sparse, with the average number of species<br />
and individuals per sample being 4.4 and 25 respectively. Although density and diversity<br />
were greatest between 20 and 40 m depth, there was no community trend with depth<br />
down to 250 m. The dominant taxa were actively mobile species. By contrast, the fauna<br />
of algal habitats was far denser and more species rich: these samples had an average of 17<br />
species and 360 individuals per sample.<br />
These results indicate an unstructured, impoverished sedimentary infauna, dominated<br />
by errant taxa which can tolerate unstable sediments, and not well-characterized as a<br />
community. The impoverishment of sedimentary benthos of this part of the Azores is<br />
attributed to sediment instability.<br />
SUMÁRIO<br />
Durante o 3º Workshop Internacional de Malacologia e Biologia Marinha nos <strong>Açores</strong><br />
em Julho de 2006, foram feitas amostragens do bentos do sedimento móvel do litoral e<br />
sublitoral perto de Vila Franca do Campo, São Miguel, com vista a caracterizar as<br />
comuni<strong>da</strong>des bentónicas <strong>da</strong> infauna e comparar a densi<strong>da</strong>de e diversi<strong>da</strong>de <strong>da</strong> infauna com<br />
as comuni<strong>da</strong>des associa<strong>da</strong>s às algas.<br />
A infauna sedimentar era particularmente esparsa, sendo o número médio de espécies<br />
e indivíduos por amostragem 4,4 e 25, respectivamente. Embora a densi<strong>da</strong>de e a<br />
diversi<strong>da</strong>de fossem as mais eleva<strong>da</strong>s entre os 20 e os 40 m de profundi<strong>da</strong>de, não se notou<br />
tendência na comuni<strong>da</strong>de com a profundi<strong>da</strong>de até aos 250 m. Os taxa dominantes eram<br />
espécies activamente móveis. Em contraste, a fauna <strong>dos</strong> habitats algais era de longe mais<br />
densa e mais rica em espécies: ali se registou a média de 17 espécies e 360 indivíduos por<br />
amostra.<br />
Estes resulta<strong>dos</strong> indicam uma infauna sedimentar não estrutura<strong>da</strong>, empobreci<strong>da</strong>,<br />
domina<strong>da</strong> por taxa errantes que podem tolerar sedimentos instáveis, e não bem<br />
caracteriza<strong>da</strong> coo comuni<strong>da</strong>de. O empobrecimento do bentos sedimentar desta parte <strong>dos</strong><br />
<strong>Açores</strong> atribui-se à instabili<strong>da</strong>de do sedimento.<br />
INTRODUCTION<br />
The Azores are a group of islands<br />
somewhat isolated in the north-east<br />
Atlantic, lying adjacent to the Mid-<br />
Atlantic Ridge some 1300 km west of<br />
Portugal and 1730 km southeast of<br />
Newfoundland. The main surface water<br />
currents reaching the archipelago bring<br />
waters from two directions: the Azores<br />
Drift, a diffuse southerly arm of the Gulf<br />
Stream breaking off from the North<br />
Atlantic Drift supplies water from the<br />
Americas, while the somewhat less-sig-
202 AÇOREANA<br />
2009, Sup. 6: 201-210<br />
nificant western eddies of the Canary<br />
Current bring waters from Spain and<br />
North Africa; below these, the midwater<br />
current brings warm, hyperhaline water<br />
from the Mediterranean outflow (Gofas,<br />
1990; Morton et al., 1998; Morton &<br />
Britton, 2000). This hydrography clearly<br />
has implications for the colonization of<br />
the islands by benthic marine species.<br />
While there have been a number of<br />
previous studies on the fauna associated<br />
with the rocky shores, or with littoral and<br />
infralittoral algae (e.g. Hawkins et al.,<br />
1990; Bullock et al., 1990; Bullock, 1995;<br />
taxa reviewed by Morton & Britton, 2000),<br />
and which have normally been taxon specific<br />
(see papers by Chapman et auctt. in<br />
Morton, 1990), there have been few published<br />
studies of the soft-sediment communities,<br />
largely owing to their recognized<br />
sparseness. Morton (1990) points<br />
out that there was at that time no information<br />
on the soft shores of the Azores, as<br />
virtually all are high energy beaches,<br />
“superficially devoid of significant life”<br />
(see also Morton et al., 1998). Two surveys<br />
had been conducted of the soft-sediment<br />
fauna of the sheltered habitat within the<br />
flooded crater of Ilhéu de Vila Franca, one<br />
in 1988 and one in 1995 (Morton, 1990;<br />
Wells, 1995 respectively).<br />
During the Third International<br />
Workshop of Malacology and Marine<br />
Biology in the Azores in July 2006, sampling<br />
of the littoral and sublittoral softsediment<br />
benthos off Vila Franca do<br />
Campo was undertaken in order to gain<br />
some insight into the communities present.<br />
Some sites were sampled within the<br />
flooded crater of the Ilhéu de Vila Franca<br />
to compare with the findings of the 1988<br />
and 1991 studies. Comparisons were<br />
made between the invertebrate fauna of<br />
quantitative (grab plus shore collected)<br />
and qualitative (dredge) benthic samples,<br />
as well as the fauna associated with<br />
infralittoral algae.<br />
METHODS<br />
Quantitative samples were collected<br />
using a 0.025 m 2 Peterson grab, taking<br />
two replicates per sampling station.<br />
Littoral and infralittoral sands were sampled<br />
quantitatively using a plastic scoop,<br />
also to 0.05 m 2 . The samples were sieved<br />
across a 0.5 mm mesh and sorted live.<br />
Qualitative samples were collected<br />
using a variety of dredges, towed at 1 to 2<br />
knots for between 6 and 10 minutes.<br />
Crustaceans, pycnogonids, polychaetes,<br />
sipunculans, phoronids and echinoderms<br />
from these samples were retained<br />
serendipitously.<br />
The depths of the grab and dredge<br />
samples ranged between 12 and 250 m.<br />
Position fixing was by GPS.<br />
Qualitative algal samples were collected<br />
either from littoral rocks (sample<br />
Island 24.10), or from sublittoral sites in<br />
the crater of Ilhéu de Vila Franca.<br />
Material as collected from the dredge<br />
samples was also analyzed from one<br />
SCUBA collection on algae, sponges, etc.,<br />
at 16 m depth.<br />
All taxa were identified to species<br />
where possible. Nomenclature and<br />
authorities are as in Costello et al. (2001).<br />
Sample numbers are prefixed “Island” for<br />
those collected within the Ilhéu de Vila<br />
Franca, otherwise “WVF”.<br />
RESULTS<br />
The sampling sites analyzed are listed<br />
in Table 1, with depths, sampling gear<br />
and univariate community statistics.<br />
Quantitative samples<br />
The twelve grab and shore-collected<br />
quantitative samples were analyzed<br />
together. The complete faunal <strong>da</strong>ta from<br />
these samples is given in Appendix 1. It<br />
is immediately apparent that the benthic<br />
infauna is indeed sparse: only one of the
BAMBER & ROBBINS: THE SOFT-SEDIMENT INFAUNA OFF SÃO MIGUEL 203<br />
TABLE 1. List of samples, with depth, sampling gear and univariate ‘community’ statistics.<br />
Sample Date depth,<br />
m<br />
sampling<br />
gear<br />
species individuals species<br />
richness<br />
Shannon-<br />
Weiner H'<br />
Evenness<br />
WVF005 19/7/06 42 dredge 7 15 2.216 2.28 0.8121<br />
WVF006 19/7/06 40 dredge 10 12 3.622 3.252 0.9788<br />
WVF007 19/7/06 178 dredge 10 26 2.762 2.887 0.8689<br />
WVF008 19/7/06 148 dredge 4 6 1.674 1.792 0.8962<br />
WVF011 20/7/06 16 scuba 26 196 4.574 3.861 0.8315<br />
WVF015 21/7/06 46 dredge 11 17 3.53 3.293 0.9518<br />
WVF016 21/7/06 19 dredge 8 24 2.203 2.772 0.924<br />
WVF019 21/7/06 23 grab 16 91 3.325 3.033 0.7581<br />
WVF020 21/7/06 50 grab 7 14 2.274 2.407 0.8573<br />
WVF021 21/7/06 118 grab 2 2<br />
Island24.1 24/7/06 0 scoop 1 17<br />
Island24.2 24/7/06 drift weed 16 129 3.087 2.845 0.7113<br />
Island24.3 24/7/06 0.5 scoop 0<br />
Island24.4 24/7/06 0.3 weed 25 719 3.505 3.328 0.7259<br />
Island24.5 24/7/06 0.5 weed 27 606 3.913 3.456 0.7352<br />
Island24.6 24/7/06 0.3 scoop 0<br />
Island24.7 24/7/06 0.5 scoop 0<br />
Island24.9 24/7/06 0.3 scoop 0<br />
Island24.10 24/7/06 0 weed scrape 3 7<br />
WVF034 25/7/06 16.7 grab 5 12 1.61 1.781 0.7669<br />
WVF035 25/7/06 23 grab 8 46 1.828 2.519 0.8398<br />
WVF036 25/7/06 36 grab 8 105 1.504 1.668 0.556<br />
WVF039 25/7/06 12 grab 1 1<br />
WVF040 26/7/06 38 dredge 5 20 1.335 1.882 0.8106<br />
WVF041 25/7/06 250 dredge 6 12 2.012 2.355 0.9112<br />
littoral/infralittoral samples contained<br />
any macrofauna, that on the sand bar in<br />
Ilhéu de Vila Franca (Island24.1) containing<br />
17 individuals of the errant isopod<br />
Eurydice affinis. Similarly, the grab samples<br />
at 12 m (WVF039) contained only a<br />
single specimen of the bivalve Ervilia castanea.<br />
Figure 1 shows the distribution<br />
with depth of faunal density (numbers<br />
per 0.05 m2), number of species and<br />
Shannon-Weiner diversity. The greatest<br />
faunal density and number of species<br />
occur between 20 and 40 m depth, but values<br />
are consistently low, with the average<br />
number of species and individuals per<br />
sample being 4.4 and 25 respectively.<br />
The community diversity is generally<br />
low, Shannon-Weiner index values ranging<br />
between 1 and 3, and also peaks at<br />
around 20 to 40 m depth, although, owing<br />
to the proportionately higher number of<br />
species (7) in a sparse fauna (n=14) at station<br />
WVF020, diversity remains in the<br />
upper range to 50 m.<br />
Dominant taxa were actively mobile<br />
species, the mysid Gastrosaccus normani,<br />
the amphipods Microdeutopus versiculatus<br />
and Harpinia laevis, the polychaete<br />
Armandia polyophthalma and the pre<strong>da</strong>tory<br />
polychaete Glycera capitata. The most<br />
numerous sessile species was the tubicolous<br />
polychaete Myriochele oculata,
204 AÇOREANA<br />
2009, Sup. 6: 201-210<br />
FIGURE 1. Univariate community parameters by depth for the sedimentary infauna, quantitative<br />
samples only.<br />
although that species was constrained to<br />
two stations. Indeed, of the 28 species<br />
recorded, 21 are actively mobile species<br />
less reliant on sedimentary-habitat stability.<br />
Qualitative samples<br />
The complete faunal <strong>da</strong>ta from the<br />
dredge samples is given in Appendix 2.<br />
These samples are not directly comparable<br />
as no molluscs were analyzed (they<br />
having been removed for other studies),<br />
and the univariate community statistics<br />
are only indicative, as the samples were<br />
not quantitative (although the Shannon-<br />
Weiner diversity index is relatively sample-size-independent).<br />
The fauna was again found to be<br />
sparse and inconsistent, 29 of the 42<br />
species recorded occurring in only one<br />
sample. Although no dredges shallower<br />
than 19 m were analyzed, there was an<br />
indication that the numbers of species<br />
and individuals were highest around 19<br />
to 50 m depth, similar to the results from<br />
the grab sample results, but the sample at<br />
178 m (WVF007) had high density and<br />
species number. Average numbers of<br />
species and individuals were 7.5 and 16.5<br />
respectively.<br />
The dominant taxa were again actively<br />
mobile species, including amphipods,<br />
decapods, errant polychaetes, while the<br />
only obligately sessile taxa were tubicolous<br />
species, the tanai<strong>da</strong>cean Paratanais<br />
martinsi, the spionid polychaete Spio<br />
armata and the phoronid Phoronis muelleri,<br />
each occurring only once.<br />
Overall, although extra species were<br />
found from the dredge samples (which<br />
had taken a larger volume per sample),<br />
the fauna was relatively similar to that<br />
found in the grab samples.<br />
Algal and other samples<br />
The non-sedimentary samples were<br />
analyzed in order to compare faunal densities<br />
and species complements of the<br />
non-infaunal community.<br />
Appendix 3 lists the complete faunal<br />
<strong>da</strong>ta from these samples, which comprise<br />
a scuba-collection (WVF011), floating<br />
(Island 24.2), submerged (Island 24.4,<br />
island 24.5) or littorally attached
BAMBER & ROBBINS: THE SOFT-SEDIMENT INFAUNA OFF SÃO MIGUEL 205<br />
(Island 24.10) algae in the Ilhéu de Vila<br />
Franca lagoon.<br />
It is immediately apparent that the<br />
fauna of these habitats was far denser and<br />
more species rich. Even though the littoral<br />
rock-pool algal sample was impoverished,<br />
the algal samples had an average of 17<br />
species and 360 individuals per sample.<br />
The dominant species were the crevicial<br />
or algal-associated polychaete<br />
Platynereis dumerilii, and peracarid crustaceans,<br />
notably algal-associated<br />
amphipods (Hyale spp., Erichthonius spp.,<br />
Microdeutopus versiculatus, Corophium acutum,<br />
Caprella acanthifera), isopods<br />
(Dynamene bidentata, Cymodoce truncata,<br />
Paranthura costana) and tanai<strong>da</strong>ceans<br />
(Tanais grimaldii), together with algalassociated<br />
pycnogonids (Anoplo<strong>da</strong>ctylus<br />
pygmaeus, A. angulatus) and the only<br />
cumacean recorded during the 2006 surveys,<br />
Cumella limicola. However, other<br />
dominant species (the polychaete Fabricia<br />
stellata, the amphipod Dexamine spinosa)<br />
are taxa which commonly occur in sediments,<br />
but which were not recorded away<br />
from the algae.<br />
Most of the species recorded from the<br />
scuba sample, collected from 16 m depth<br />
to the north-east off Ilhéu de Vila Franca,<br />
were the same as those dominant taxa<br />
from the algal samples, confirming this<br />
dense and diverse community is not<br />
restricted to the sheltered waters of the<br />
crater lagoon.<br />
DISCUSSION<br />
The <strong>da</strong>ta from both sets of sedimentary<br />
infaunal samples were subjected to<br />
multivariate analysis simply on presence<br />
or absence of species, owing to the qualitative<br />
nature of the dredge samples. The<br />
<strong>da</strong>ta set was reduced to those 30 taxa<br />
occurring as more than one individual in<br />
the survey, and to those samples with<br />
some fauna.<br />
The dendrogram of sample similarity<br />
(Figure 2) shows relatively poor clustering<br />
owing to the sparse and patchy nature<br />
of the fauna. Sample WVF040 is quite distinct,<br />
the three species recorded there<br />
(two pycnogonids and a tanai<strong>da</strong>cean) not<br />
being found elsewhere; this sample was<br />
not analyzed further. Similar reasons<br />
account for the isolation of samples<br />
WVF007, WVF008 and Island24.1. The<br />
remaining six grab samples and five<br />
dredge samples show that there is, in fact,<br />
no particular trend with depth in the<br />
community, dredge sample WVF041,<br />
taken at 250 m, falling comfortably within<br />
the subcluster of four grab samples taken<br />
at depths between 16.7 and 36 m. This<br />
lack of a trend is confirmed by the nonparametric<br />
ordination by multidimensional<br />
scaling (MDS) (Figure 3).<br />
Although the stations WVF007 and<br />
WVF008, both deeper than 140 m, are isolated,<br />
the species which distinguish them,<br />
Onuphis eremita and Ebalia tuberosa, are<br />
not species confined to deeper water.<br />
These results indicate an unstructured,<br />
impoverished sedimentary infauna,<br />
dominated by errant taxa which can<br />
tolerate unstable sediments, and not wellcharacterized<br />
as a community, thus not<br />
showing any particular community<br />
trends with depth. This fauna is most<br />
impoverished in shallow depths (
206 AÇOREANA<br />
2009, Sup. 6: 201-210<br />
FIGURE 2. Dendrogram by Bray-Curtis similarity (%) for sedimentary benthic infaunal samples<br />
(presence-absence <strong>da</strong>ta).<br />
which would most readily recruit. It was<br />
notable that the densest algal-associated<br />
communities occurred sublittorally, most<br />
littoral algae of the adjacent São Miguel<br />
shoreline supporting little of no fauna.<br />
ACKNOWLEDGEMENTS<br />
We are indebted to Andreia Salvador<br />
for sampling assistance in Ilhéu de Vila<br />
Franca, to António de Frias Martins for<br />
FIGURE 3. MDS ordination based on the similarity<br />
<strong>da</strong>ta from figure 2, with circles of diameter<br />
proportional to sample depth.<br />
the organisation of, and inviting us to the<br />
Workshop, and to the other participants<br />
at the workshop for samples, assistance<br />
with the boat-work, discussion and entertainment.<br />
LITERATURE CITED<br />
BULLOCK, R.C., 1995. The distribution<br />
of the molluscan fauna associated<br />
with the interti<strong>da</strong>l coralline algal turf<br />
of a partially submerged volcanic<br />
crater, the Ilhéu de Vila Franca, São<br />
Miguel, Azores. In: MARTINS, A.M.F.<br />
(ed.), The Marine Fauna and Flora of the<br />
Azores (Proceedings of the Second<br />
International Workshop of Malacology<br />
and Marine Biology, São Miguel, 1991).<br />
Açoreana, Supplement [4]: 9-55.<br />
BULLOCK, R.C., R.D. TURNER & R.A.<br />
FRALICK, 1990. Species richness and<br />
diversity of algal-associated micromolluscan<br />
communities from São<br />
Miguel, Azores. In: MARTINS, A.M.F.<br />
(ed.), The Marine Fauna and Flora of the<br />
Azores (Proceedings of the First<br />
International Workshop of Malacology,
BAMBER & ROBBINS: THE SOFT-SEDIMENT INFAUNA OFF SÃO MIGUEL 207<br />
São Miguel, 1988). Açoreana,<br />
Supplement [2]: 39-58.<br />
COSTELLO, M.J., C. EMBLOW & R.<br />
WHITE (eds.), 2001. European<br />
Register of marine Species. A checklist<br />
of the marine species in Europe<br />
and a bibliography of guides to their<br />
identification. Patrimoines Naturels,<br />
50: 463 pp.<br />
GOFAS, S., 1990. The littoral Rissoi<strong>da</strong>e<br />
and Anabathri<strong>da</strong>e of São Miguel,<br />
Azores. In: MARTINS, A.M.F. (ed.),<br />
The Marine Fauna and Flora of the<br />
Azores (Proceedings of the First<br />
International Workshop of Malacology,<br />
São Miguel, 1988). Açoreana,<br />
Supplement [2]: 97-134.<br />
HAWKINS, S.J., L.P. BURNAY, A. NETO,<br />
R. TRISTÃO <strong>da</strong> CUNHA & A.M. de<br />
FRIAS MARTINS, 1990. A description<br />
of the zonation patterns of molluscs<br />
and other biota on the south coast of<br />
São Miguel, Azores. In: MARTINS,<br />
A.M.F. (ed.), The Marine Fauna and<br />
Flora of the Azores (Proceedings of the<br />
First International Workshop of<br />
Malacology, São Miguel, 1988).<br />
Açoreana, Supplement [2]: 21-38.<br />
MORTON, B., 1990. The interti<strong>da</strong>l ecology<br />
of Ilhéu de Vila Franca – a<br />
drowned volcanic crater in the<br />
Azores. In: MARTINS, A.M.F. (ed.),<br />
The Marine Fauna and Flora of the<br />
Azores (Proceedings of the First<br />
International Workshop of Malacology,<br />
São Miguel, 1988). Açoreana,<br />
Supplement [2]: 3-20.<br />
MORTON, B. & J.C. BRITTON, 2000. The<br />
origins of the coastal and marine flora<br />
and fauna of the Azores.<br />
Oceanography and Marine Biology: an<br />
Annual Review, 38: 13-84.<br />
MORTON, B., J.C. BRITTON & A.M.F.<br />
MARTINS, 1998. Coastal Ecology of the<br />
<strong>Açores</strong>, 249pp. Socie<strong>da</strong>de Afonso<br />
Chaves, Ponta Delga<strong>da</strong>.<br />
WELLS, F.E., 1995. An investigation of<br />
marine invertebrate communities in<br />
the sediments of Ilhéu de Vila Franca<br />
off the island of São Miguel, Azores.<br />
In: MARTINS, A.M.F. (ed.), The Marine<br />
Fauna and Flora of the Azores<br />
(Proceedings of the Second International<br />
Workshop of Malacology and Marine<br />
Biology, São Miguel, 1991). Açoreana,<br />
Supplement [4]: 57-65.
208 AÇOREANA<br />
2009, Sup. 6: 201-210<br />
APPENDIX 1. Complete benthic faunal <strong>da</strong>ta from quantitative sedimentary samples<br />
WVF WVF WVF Island Island Island Island Island WVF WVF WVF WVF<br />
Sample 019 020 021 24.1 24.3 24.6 24.7 24.9 034 035 036 039 TOTAL<br />
SIPUNCULA<br />
Golfingia minuta 2 2<br />
ANNELIDA<br />
Glycera capitata 9 1 6 6 22<br />
Glycera tesselata 3 3<br />
Glycinde nordmanni 1 1<br />
Eumi<strong>da</strong> cf. bahusiensis 1 1<br />
Scoloplos armiger 1 1<br />
Spio armata 2 2<br />
Armandia polyophthalma 24 7 7 4 42<br />
Myriochele oculata 4 70 74<br />
Ditrupa arietina 1 3 4<br />
ARTHROPODA<br />
Crustacea<br />
Mysi<strong>da</strong>cea<br />
Gastrosaccus normani 22 1 1 18 8 50<br />
Anchialina agilis 1 1 2<br />
Amphipo<strong>da</strong><br />
Harpinia laevis 14 5 14 33<br />
Synchelidium haplocheles<br />
5 5<br />
Erichthonius punctatus 1 1<br />
Microdeutopus versiculatus 6 1 2 5 1 15<br />
Ampithoe rubricata 1 1<br />
Caprella penantis 1 1<br />
Isopo<strong>da</strong><br />
Eurydice affinis 1 1 17 19<br />
Decapo<strong>da</strong><br />
Atyaephyra desmaresti 1 1<br />
Processa edulis 1 1<br />
Crangon trispinosus 2 2<br />
Parthenope expansa 1 1<br />
MOLLUSCA<br />
Bivalvia<br />
Ervilia castanea 1 1 2<br />
Moerella donacina 1 1<br />
Solemya sp. 1 1<br />
ECHINODERMATA<br />
Echinocardium flavescens<br />
4 3 7<br />
Echinocyamus pusillus 1 3 1 5<br />
No. of Species 16 7 2 1 0 0 0 0 6 10 10 1 28<br />
No. of Individuals 91 14 2 17 0 0 0 0 13 53 109 1 300
BAMBER & ROBBINS: THE SOFT-SEDIMENT INFAUNA OFF SÃO MIGUEL 209<br />
APPENDIX 2. Faunal <strong>da</strong>ta from qualitative dredge samples (Mollusca not included)<br />
Sample WVF005 WVF006 WVF007 WVF008 WVF015 WVF016 WVF040 WVF041 TOTAL<br />
SIPUNCULA<br />
Golfingia margaritacea 1 1<br />
Golfingia minuta 1 1<br />
ANNELIDA<br />
Harmothoe spp. 4 3 7<br />
Glycera capitata 1 2 4 7<br />
Glycera tesselata 1 3 4<br />
Glycinde nordmanni 1 1<br />
Nereis pelagica 3 3<br />
Nereis diversicolor 2 2<br />
Eulalia cf. expusilla 1 1<br />
Spio armata 1 1<br />
Armandia polyophthalma 1 1<br />
Pisione remota 1 1<br />
Onuphis eremita 6 1 7<br />
Hyalinoecia tubicola 1 1 2<br />
ARTHROPODA<br />
Pycnogoni<strong>da</strong><br />
Achelia echinata 9 9<br />
Anoplo<strong>da</strong>ctylus virescens 1 1<br />
Anoplo<strong>da</strong>ctylus amora 3 3<br />
Crustacea<br />
Mysi<strong>da</strong>cea<br />
Gastrosaccus normani 1 1 4 2 8<br />
Amphipo<strong>da</strong><br />
Ampelisca spinipes 1 1<br />
Erichthonius punctatus 1 1<br />
Erichthonius difformis 7 1 4 12<br />
Microdeutopus versiculatus<br />
2 2<br />
Melita gladiosa 2 2<br />
Lembos websteri 1 1<br />
Isopo<strong>da</strong><br />
Eurydice affinis 1 1 3 5<br />
Tanai<strong>da</strong>cea<br />
Paratanais martinsi 6 6<br />
Decapo<strong>da</strong><br />
Processa edulis 1 2 3<br />
Crangon trispinosus 6 6<br />
Anapagurus laevis 1 1<br />
Paguri<strong>da</strong>e indet. 1 2 3<br />
Galathea intermedia 1 3 4<br />
Scyllarus arctus 1 1<br />
Ebalia tuberosa 7 3 10<br />
Liocarcinus arcuatus 1 1<br />
Liocarcinus marmoreus 4 4<br />
Liocarcinus pusillus 1 1<br />
Pilumnoides inglei 1 1<br />
Parthenope expansa 1 1 2<br />
Macropodia rostrata 1 1<br />
PHORONIDA<br />
Phoronis muelleri 1 1<br />
ECHINODERMATA<br />
Echinocardium flavescens 2 2<br />
Echinocyamus pusillus 1 1<br />
No. of Species 7 10 10 4 10 8 5 6 42<br />
No. of Individuals 15 12 26 6 17 24 20 12 132
210 AÇOREANA<br />
2009, Sup. 6: 201-210<br />
APPENDIX 3. Faunal <strong>da</strong>ta from algal samples<br />
Sample WVF011 Island 24.2 Island 24.4 Island 24.5 Island 24.10 TOTAL<br />
SIPUNCULA<br />
Golfingia margaritacea 1 1<br />
ANNELIDA<br />
Harmothoe spp. 4 2 1 7<br />
Nereis pelagica 2 2<br />
Platynereis dumerilii 13 47 162 129 351<br />
Nainereis cf. laevigata 2 2<br />
Euphrosyne armadillo 1 1<br />
Polyophthalmus pictus 4 2 5 1 12<br />
Eupolymnia nebulosa 1 1<br />
Fabricia stellata 4 12 13 29<br />
ARTHROPODA<br />
Pycnogoni<strong>da</strong><br />
Achelia echinata 4 1 5<br />
Callipallene emaciata 6 6 12<br />
Anoplo<strong>da</strong>ctylus amora 0<br />
Anoplo<strong>da</strong>ctylus pygmaeus<br />
1 1 2<br />
Anoplo<strong>da</strong>ctylus angulatus 1 5 9 15<br />
Crustacea<br />
Amphipo<strong>da</strong><br />
Ampelisca aequicornis A 3 3<br />
Ampelisca aequicornis B 3 3<br />
Erichthonius punctatus 12 1 8 3 24<br />
Erichthonius difformis 42 4 43 51 140<br />
Microdeutopus versiculatus 26 1 51 37 115<br />
Melita gladiosa 3 1 4<br />
Lembos websteri 13 13<br />
Ampithoe rubricata 3 1 13 7 1 25<br />
Dexamine cf. spinosa 12 27 31 25 95<br />
Hyale nilssoni 8 9 82 85 184<br />
Hyale perieri 4 4<br />
Corophium acutum 2 55 57<br />
Caprella penantis 2 4 2 8<br />
Caprella acanthifera 18 17 21 56<br />
Isopo<strong>da</strong><br />
Paranthura costana 1 1 11 9 22<br />
Eurydice affinis 18 18<br />
Dynamene bidentata 3 22 13 38<br />
Cymodoce truncata 3 7 5 15<br />
Janira maculosa 1 7 8<br />
Tanai<strong>da</strong>cea<br />
Tanais grimaldii 4 7 194 110 315<br />
Leptochelia caldera 15 2 17<br />
Cumacea<br />
Cumella limicola 6 11 11 28<br />
Decapo<strong>da</strong><br />
Thoralus cranchi 1 1<br />
Clibanarius erythropus 4 4<br />
Paguri<strong>da</strong>e indet. 5 5<br />
Pilumnus hirtellus 2 2<br />
MOLLUSCA<br />
Gastropo<strong>da</strong><br />
Setia subvaricosa 1 5 6 12<br />
Rissoa guernei 1 1<br />
No. of Species 26 16 25 27 3 41<br />
No. of Individuals 196 129 719 606 7 1657
AÇOREANA, Suplemento 6, Setembro 2009: 211-216<br />
SHELL OCCUPANCY BY THE HERMIT CRAB CLIBANARIUS ERYTHROPUS<br />
(CRUSTACEA) ON THE SOUTH COAST OF SÃO MIGUEL, AÇORES<br />
Pedro Rodrigues 1 & Roshan K. Rodrigo 2<br />
1<br />
CIBIO-Pólo <strong>Açores</strong>, Department of Biology, University of the Azores, 9501-801 Ponta Delga<strong>da</strong>, São Miguel,<br />
Azores, Portugal. e-mail: pedrorodrigues@uac.pt<br />
2<br />
Faculty of Science, Department of Zoology, University of Colombo, Colombo 7, Sri Lanka<br />
ABSTRACT<br />
The importance of gastropod shells to hermit crabs is well known. The strong association<br />
between hermit crabs and their adopted shells influences almost all aspects of their<br />
biology and there is a strong correlation between the sizes of the shell and the crustacean.<br />
The hermit crab Clibanarius erythropus is abun<strong>da</strong>nt on the rocky shores of the <strong>Açores</strong>.<br />
However, there are few references to the ecology of this species. The aim of the present<br />
study was thus to evaluate the occupancy of mollusc shell species by C. erythropus on the<br />
south coast of the island of São Miguel. Shells of Columbella a<strong>da</strong>nsoni had the highest occupancy<br />
rate followed by Mitra cornea and Stramonita haemostoma. The significant differences<br />
in the estimated shell volumes available for C. erythropus suggests that juveniles choose<br />
Nassarius incrassatus, medium sized hermits prefer Pollia dorbignyi, C. a<strong>da</strong>nsoni and M.<br />
cornea, and the largest adults opt for S. haemastoma shells.<br />
RESUMO<br />
A importância <strong>da</strong>s conchas de gastrópodes para os berna<strong>dos</strong>-eremitas é bem<br />
conheci<strong>da</strong>. A forte associação entre os bernar<strong>dos</strong>-eremita e as suas adopta<strong>da</strong>s conchas<br />
influencia grandemente quase to<strong>dos</strong> os aspectos <strong>da</strong> sua biologia, existindo uma forte<br />
correlação entre o tamanho <strong>da</strong> concha e o tamanho do crustáceo. O bernado-eremita<br />
Clibanarius erythopus é uma espécie muito abun<strong>da</strong>nte nas costas rochosas. To<strong>da</strong>via, são<br />
raras as referências à ecologia e à biologia desta espécie. O presente estudo teve como<br />
objectivo avaliar a ocupação de conchas de espécies de moluscos por C. erythropus na costa<br />
sul de São Miguel. Conchas de Columbella a<strong>da</strong>nsoni obtiveram a maior taxa de ocupação,<br />
segui<strong>da</strong>s de Mitra cornea e de Stramonita haemastoma. As diferenças significativas no<br />
volume de concha estimado acessível a C. erythropus sugerem que os juvenis escolhem<br />
conchas de Nassarius incrassatus, os de tamanho médio preferem conchas de Pollia<br />
dorbignyi, C. a<strong>da</strong>nsoni e M. cornea, e os adultos maiores optam por conchas de S.<br />
haemastoma.<br />
INTRODUCTION<br />
The importance of gastropod shells to<br />
hermit crabs is well known; such<br />
shells particularly supplying protection<br />
against pre<strong>da</strong>tors (Vance, 1972) and physical<br />
stresses (Reese, 1969) due to the fact<br />
that the crabs have a soft, vulnerable<br />
abdomen. Shells can be found either<br />
empty, obtained by confrontations<br />
between individual crabs, or by removal<br />
of the gastropod (Elwood & Neil, 1992).<br />
The availability of shells is the main factor<br />
limiting populations of hermit crabs<br />
(Kellog, 1976) and they usually partition<br />
shell resources according to size<br />
(Bertness, 1981; Scully, 1983; Neil, 1985)<br />
and/or their own body size (Mitchell,<br />
1975), shell shape, weight and volume<br />
(Reese, 1963; Kuris & Brody, 1976;<br />
Conover, 1978). Interspecific competition<br />
among hermit crabs for shell resources<br />
may also be avoided by partitioning habitats.<br />
Partitioning also occurs between
212 AÇOREANA<br />
2009, Sup. 6: 211-216<br />
hermit crabs and other species such as<br />
sipunculans (Morton & Britton, 1995).<br />
Hermit crabs that occupy large shells<br />
can better resist to desiccation, thermal<br />
stress and pre<strong>da</strong>tion (Rittschof et al.,<br />
1995). However, heavy shells may limit<br />
reproduction and growth because of the<br />
high-energy cost of locomotion (Bertness,<br />
1981). For another hand, small shells render<br />
the crabs more vulnerable to pre<strong>da</strong>tion<br />
and may reduce their growth rate<br />
(Hazlett, 1981; Angel, 2000). The strong<br />
association between hermit crabs and<br />
their adopted shells influences greatly<br />
almost all aspects of their biology<br />
(Hazlett, 1981) and there is a strong correlation<br />
between shell and crab sizes<br />
(Abrams et al., 1986; Botelho & Costa,<br />
2000; Sant’Anna et al., 2006).<br />
The hermit crab Clibanarius erythropus<br />
(Latreille, 1818) is a common species<br />
along the Mediterranean shores and<br />
Atlantic coasts from United Kingdom to<br />
the <strong>Açores</strong> (Ingle, 1993). In the Açorean<br />
archipelago, C. erythropus is abun<strong>da</strong>nt on<br />
rocky shores, including tide pools<br />
(Morton et al., 1998). However, references<br />
to the general ecology and biology of this<br />
species are few (Gherardi, 1991).<br />
The aim of the present study was to<br />
evaluate the occupancy of mollusc shell<br />
species by Clibanarius erythropus in the<br />
south coast of São Miguel island.<br />
MATERIAL AND METHODS<br />
FIGURE 1. Location of the sampling sites on<br />
São Miguel. A. Ilhéu de Vila Franca do Campo;<br />
B. Vila Franca do Campo Harbour; C. Roí<strong>da</strong> <strong>da</strong><br />
Praia; D. Ponta <strong>da</strong> Galera; E. Baía do Cruzeiro.<br />
The study was carried out on the<br />
south coast of São Miguel during July<br />
2006 as part of the 3 rd International<br />
Workshop on the Malacology and Marine<br />
Biology of the <strong>Açores</strong> covered in Vila<br />
Franca do Campo, São Miguel, <strong>Açores</strong>.<br />
Five populations of Clibanarius erythropus<br />
were studied for shell occupancy<br />
(Figure 1).<br />
The hermit crabs were hand-sampled<br />
by snorkelling for ten minutes to stan<strong>da</strong>rdize<br />
capture effort and brought alive<br />
to the laboratory where individuals and<br />
shells were identified according to Wirtz<br />
(1995) and Morton et al. (1998). The occupied<br />
shells were measured (total shell<br />
length and shell width) using vernier callipers<br />
to the nearest 0.01 mm. The volume<br />
of each shell was estimated according to<br />
Morton & Britton (1995) by squaring the<br />
shortest linear measurement (width) and<br />
multiplying this value by the longest linear<br />
measurement (length).<br />
A Chi-square test was applied to the<br />
five most common occupied shell species.<br />
The relationship between those and the<br />
estimated volume was also subjected to<br />
analysis of variance (ANOVA) against the<br />
null hypothesis that different shell species<br />
have the same volume available for<br />
Clibanarius erythropus.<br />
RESULTS<br />
Eleven species of gastropod shells<br />
occupied by Clibanarius erythropus were<br />
collected and frequency of occupation at<br />
each site is identified in Table 1.<br />
Columbella a<strong>da</strong>nsoni Menke, 1853, Mitra<br />
cornea (Lamarck, 1811) and Stramonita<br />
haemastoma (Linnaeus, 1766) were the<br />
most commonly occupied shells, followed<br />
by Pollia dorbignyi (Payraudeau,<br />
1826) and Nassarius incrassatus (Ström,<br />
1768).
RODRIGUES & RODRIGO: SHELL OCCUPANCY BY CLIBANARIUS ERYTHROPUS 213<br />
TABLE 1. The frequency of mollusc shells occupied by Clibanarius erythropus from the different<br />
sampling sites on São Miguel.<br />
Mollusc shell Site A Site B Site C Site D Site E TOTAL<br />
Pollia dorbignyi (Payraudeau, 1826) 6 1 0 34 0 41<br />
Columbella a<strong>da</strong>nsoni Menke, 1853 54 41 51 67 31 244<br />
Stramonita haemastoma (Linnaeus, 1766) 6 15 81 25 15 142<br />
Mitra cornea (Lamarck, 1811) 1 46 0 27 84 158<br />
Nassarius incrassatus (Ström, 1768) 10 4 5 4 0 23<br />
Calliostoma lividum Dautzenberg, 1927 1 0 0 0 0 1<br />
Coralliophila meyendorffii (Calcara, 1845) 0 4 0 0 0 4<br />
Melarphe neritoides (Linnaeus, 1756) 0 0 0 1 0 1<br />
Littorina striata King & Broderip, 1832 0 0 0 0 5 5<br />
Jujubinus sp. 0 0 0 0 1 1<br />
Bittium cf. latreillii (Payraudeau, 1826) 0 0 0 0 2 2<br />
TOTAL: 78 111 137 158 138 622<br />
The Chi-square test, comparing the<br />
total number of the five commonest occupied<br />
shells from the different sampling<br />
sites, indicated a significantly different<br />
proportion of species occupied by<br />
Clibanarius erythropus (χ 2 = 386.1, p
214 AÇOREANA<br />
2009, Sup. 6: 211-216<br />
ability of certain gastropods influences<br />
their pattern of shell utilization in the natural<br />
habitat as the crabs tend to be opportunistic<br />
with regards to the shells they<br />
inhabit (Botelho & Costa, 2000). The significant<br />
differences in the estimated shell<br />
volume available for Clibanarius erythropus,<br />
the presence of empty shells (personal<br />
observations), and that the crab<br />
requires different shell sizes atdifferent<br />
stages of their growth (Morton & Britton,<br />
1995), suggests that juvenile C. erythropus<br />
individuals choose Nassarius incrassatus<br />
shells, middle size individuals prefer<br />
Pollia dorbignyi, Columbella a<strong>da</strong>nsoni and<br />
Mitra cornea shells, and larger adults opt<br />
for Stramonita haemastoma shells. This is<br />
in accor<strong>da</strong>nce with the study of Botelho &<br />
Costa (2000) where it was reported that<br />
hermit crabs of < 8.6 mm occupied all<br />
shell species, whereas those > 8.6 mm<br />
were found only in S. haemastoma shells.<br />
Smaller crabs occupied Littorina striata<br />
and N. incrassatus shells.<br />
ACKNOWLEDGMENTS<br />
We are grateful to Professor António<br />
M. de Frias Martins for the opportunity to<br />
undertake this research, and Professor<br />
Brian Morton for the review of this paper.<br />
This project was supported by the Third<br />
International Workshop on Malacology<br />
and Marine Biology, Vila Franca do<br />
Campo, São Miguel, <strong>Açores</strong><br />
The experiments performed for the<br />
present study comply with the laws of the<br />
country in which they were performed.<br />
LITERATURE CITED<br />
ABRAMS, P.A., C. NYBLADE & S.<br />
SHELDON, 1986. Resource partitioning<br />
and competition for shells in a<br />
subti<strong>da</strong>l hermit crab species assemblage.<br />
Oecologia, 69: 429-445.<br />
ANGEL, J.E., 2000. Effects of shell fit in<br />
the biology of the hermit crab Pagurus<br />
longicarpus (Say). Journal of<br />
Experimental Marine Biology and<br />
Ecology, 243(2): 169-184.<br />
BERTNESS, M.D., 1981. The influence of<br />
shell-type on hermit crab growth and<br />
clutch size. Crustaceana, 40(2): 197-<br />
205.<br />
BOTELHO, A., & A.C. COSTA, 2000.<br />
Shell occupancy of the interti<strong>da</strong>l hermit<br />
crab Clibanarius erythropus<br />
(Decapo<strong>da</strong>, Diogeni<strong>da</strong>e) on São<br />
Miguel (Azores). Hydrobiologia, 440:<br />
111-117.<br />
CONOVER, M., 1978. Importance of various<br />
shell characteristics to the shell<br />
selection behavior of the hermit crabs.<br />
Journal of Experimental Marine Biology<br />
and Ecology, 32: 131-142.<br />
ELWOOD, R.W., & S.J. NEIL, 1992.<br />
Assessments and Decisions, 192 pp.<br />
Chapman & Hall, London.<br />
GHERARDI, F., 1991. Relative growth,<br />
population structure and shell-utilization<br />
of the hermit crab Clibanarius erythropus<br />
in the Mediterranean. Oebalia,<br />
17: 181-196.<br />
HAZLETT, B., 1981. The behavioural<br />
ecology of hermit crabs. Annual<br />
Review of Ecology and Systematics, 12: 1-<br />
22.<br />
INGLE, R., 1993. Hermit Crabs of the<br />
Northeastern Atlantic Ocean and the<br />
Mediterranean Sea, 495 pp. Chapman<br />
& Hall, London.<br />
KELLOG, C.W., 1976. Gastropod shells: a<br />
potentially limiting resource for hermit<br />
crabs. Journal of Experimental<br />
Marine Biology and Ecology, 22: 101-<br />
111.<br />
KURIS, A.M., & M.S. BRODY, 1976. Use<br />
of principal components analysis to<br />
describe the snail shell resource for<br />
hermit crabs. Journal of Experimental<br />
Marine Biology and Ecology, 22: 69-77.<br />
MITCHELL, K.A., 1975. An analysis of<br />
shell occupation by two sympatric
RODRIGUES & RODRIGO: SHELL OCCUPANCY BY CLIBANARIUS ERYTHROPUS 215<br />
species of hermit crab. I. Ecological factors.<br />
Biological Bulletin, 149: 205-213.<br />
MORTON, B., & J.C. BRITTON, 1995.<br />
Partitioning of shell resources by<br />
Aspi<strong>dos</strong>iphon muelleri (Sipuncula) and<br />
Anapagurus laevis (Crustacea) in the<br />
Azores. IN: MARTINS, A.M.F. (ed.),<br />
The Marine Fauna and Flora of the<br />
Azores (Proceedings of the Second<br />
International Workshop of Malacology<br />
and Marine Biology, São Miguel, 1991).<br />
Açoreana, Supplement [4]: 67-77.<br />
MORTON, B., J.C. BRITTON & A.M.F.<br />
MARTINS, 1998. Ecologia Costeira <strong>dos</strong><br />
<strong>Açores</strong>, x + 249 pp. Socie<strong>da</strong>de Afonso<br />
Chaves, Ponta Delga<strong>da</strong>.<br />
NEIL, S.J., 1985. Size assessment and<br />
cues: studies of hermit crab contests.<br />
Behaviour, 92: 22-38.<br />
REESE, E.S., 1963. The behavioral mechanisms<br />
underlying shell selection by<br />
hermit crabs. Behaviour, 21: 78-126.<br />
REESE, E.S., 1969. Behavioral a<strong>da</strong>ptations<br />
of interti<strong>da</strong>l hermit crabs.<br />
American Zoologist, 9: 343-355.<br />
RITTSCHOF, D., J. SARRICA & D.<br />
RUBENSTEIN, 1995. Shell dynamics<br />
and microhabitat selection by striped<br />
legged hermit crabs, Clibanarius vittatus<br />
(Bose). Journal of Experimental<br />
Marine Biology and Ecology, 192(2): 157-<br />
172.<br />
SANT’ANNA, B., C.M. ZANGRANDE,<br />
L.D.A. REIGADA & M.A.A.<br />
PINHEIRO, 2006. Shell utilization<br />
pattern of the hermit crab Clibanarius<br />
vittatus (Crustacea, Anomura) in an<br />
estuary at São Vicente, State of São<br />
Paulo, Brazil. Iheringia, Série Zoologia,<br />
96(2): 261-266.<br />
SCULLY, E.P., 1983. The behavioural ecology<br />
of competition and resource utilization<br />
among hermit crabs. In:<br />
REBACH, S., & D. DUNHAM (eds.),<br />
Studies in A<strong>da</strong>ptation: The behavior of<br />
higher Crustacea, pp. 23-55. John<br />
Wiley, New York.<br />
VANCE, R.R., 1972. The role of shell adequancy<br />
in behavioural interactions<br />
involving the hermit crab Pagurus<br />
longicarpus. Marine Biology, 104: 31-39.<br />
WIRTZ, P., 1995. Unterwasserfuhrer<br />
Madeira-Kanaren-Azoren, 247 pp.<br />
Stephanie Naglschmid, Stuttgart.
AÇOREANA, Suplemento 6, Setembro 2009: 217-225<br />
A CONSERVATIONAL APPROACH ON THE SEABIRD POPULATIONS OF ILHÉU<br />
DE VILA FRANCA DO CAMPO, AZORES, PORTUGAL<br />
Pedro Rodrigues 1 , Joana Micael 1 , Roshan K. Rodrigo 2 & Regina T. Cunha 1<br />
1<br />
CIBIO-Pólo <strong>Açores</strong>, Department of Biology, University of the Azores, 9501-801 Ponta Delga<strong>da</strong>, São Miguel,<br />
Azores, Portugal. e-mail: pedrorodrigues@uac.pt<br />
2<br />
Faculty of Science, Department of Zoology, University of Colombo, Colombo 7, Sri Lanka<br />
ABSTRACT<br />
This study was performed to identify the seabird species occurring on Ilhéu de Vila<br />
Franca do Campo (IVFC) off São Miguel island, Azores, giving a special emphasis on the<br />
description of their ecology and threats. Flush counts, ground searches and raft counts<br />
were conducted and two types of natural habitats were identified. The results confirmed<br />
the nesting of two en<strong>da</strong>ngered species and revealed three other possible breeders enhancing<br />
the importance of the islet for the protection and conservation of Azorean seabird populations.<br />
Although playing an important role on the conservation of Cory’s shearwater<br />
and Common tern populations, the islet can be threatened by continuous habitat degra<strong>da</strong>tion<br />
by human disturbance. The implementation of a habitat restoration program is<br />
suggested for the islet in a near future.<br />
RESUMO<br />
Foi feito um levantamento <strong>da</strong>s espécies de aves marinhas que ocorrem no Ilhéu de Vila<br />
Franca do Campo, com especial ênfase para a sua ecologia e ameaças. Foram realiza<strong>da</strong>s<br />
contagens visuais, procura de ninhos e contagem de janga<strong>da</strong>s ao longo de todo o ilhéu e<br />
zonas adjacentes, confirmando a nidificação de duas espécies ameaça<strong>da</strong>s e a possibili<strong>da</strong>de<br />
de nidificação de outras três. A identificação de dois tipos de habitats naturais evidencia<br />
a importância do ilhéu para a protecção e conservação <strong>da</strong>s populações de aves marinhas.<br />
Apesar do importante papel na conservação <strong>da</strong>s populações de cagarros e garajauscomuns,<br />
o ilhéu de Vila Franca do Campo continua a ser ameaçado por uma contínua<br />
degra<strong>da</strong>ção <strong>dos</strong> seus habitats devido à acção humana. Este trabalho sugere, num futuro<br />
próximo, a implementação de medi<strong>da</strong>s proteccionistas e um programa de restauração <strong>dos</strong><br />
habitats naturais deste ilhéu.<br />
INTRODUCTION<br />
The Azorean archipelago, located in the<br />
north Atlantic Ocean, has always been<br />
recognized as an interesting place for<br />
birds, mainly seabirds, not only due to the<br />
coast line with steep scarps but also to its<br />
geographical location (N36-39º, W25-31º)<br />
that represents an ornithological transition<br />
between temperate and tropical<br />
zones (Monteiro et al., 1996a, b).<br />
Thirteen seabird species are known to<br />
occur in the Azores. The regular breeders<br />
are Bulwer’s petrel (Bulweria bulwerii),<br />
Cory’s shearwater (Calonectris diomedia<br />
borealis), Manx shearwater (Puffinus puffinus),<br />
Little shearwater (Puffinus baroli),<br />
Band-rumped storm-petrel (Oceanodroma<br />
castro), Monteiro’s storm petrel<br />
(Oceanodroma monteiroi), Yellow-legged<br />
gull (Larus michaelis atlantis), Common<br />
tern (Sterna hirundo) and Roseate tern (S.<br />
dougallii). There are two occasional<br />
breeders, Red-billed tropicbird (Phaethon<br />
aethereus) and Sooty tern (Onychoprion fuscatus),<br />
a possible breeder, Cape Verde<br />
petrel (Pterodroma feae), and a possible former<br />
breeder, White-faced storm-petrel<br />
(Pelagodroma marina) (Le Grand et al.,<br />
1984; Monteiro et al., 1996a).
218 AÇOREANA<br />
2009, Sup. 6: 217-225<br />
The archipelago accounts for the<br />
largest population of Cory’s shearwater of<br />
the world with more than 180.000 couples<br />
(79% of the European population)<br />
(Rodrigues & Nunes, 2002). Also representative<br />
are the populations of Bandrumped<br />
storm-petrel, 915 to 1240 couples<br />
(around 25% of the European population),<br />
Little shearwater, 800 to 1500 couples<br />
(around 20% of the European population)<br />
(Monteiro et al., 1999), Roseate tern<br />
with more than 1000 couples (60% of the<br />
European population) and Common tern,<br />
around 2000 couples (5% of the European<br />
population) (Rodrigues & Nunes, 2002).<br />
All these seabird species have a vulnerable<br />
status, except Roseate tern which<br />
is in Danger, and the Common tern with a<br />
Favourable Conservation status<br />
(Rodrigues & Nunes, 2002).<br />
Most seabird populations breeding in<br />
Azores have been suffering dramatic historical<br />
declines as a consequence of major<br />
habitat degra<strong>da</strong>tion, mainly by human<br />
activities from the late 15 th century on,<br />
and the introduction of mammalian<br />
FIGURE 1. Ilhéu de Vila Franca do Campo with identified habitats, burrows and nests cavities.<br />
C - Vegetated Sea Cliffs of the Macaronesian Coasts habitat; H - Endemic Macaronesian Heaths<br />
habitat; F - Forests of iron trees; V – vineyards; + Common tern (CT) nests; * Cory’s shearwater (CS)<br />
burrows/nests cavities; CS destroyed nest; CS abandoned nest; CS abandoned egg; CT<br />
destroyed nest; CT abandoned nest; CT abandoned egg; Area of public permitted access.
RODRIGUES ET AL: SEABIRD CONSERVATION AT ILHÉU DE VILA FRANCA 219<br />
pre<strong>da</strong>tors (Monteiro et al., 1996b), so they<br />
tend to breed on isolated islets and sea<br />
cliffs, free of pre<strong>da</strong>tors and human disturbance,<br />
with natural habitats without invasive<br />
alien species (Monteiro et al., 1996b;<br />
Ramos et al., 1997; Groz & Pereira, 2005).<br />
One of these islets is the Ilhéu de Vila<br />
Franca do Campo (IVFC) (Figure 1), 1.2<br />
km south of São Miguel island.<br />
Several studies were published on the<br />
islet’s biota, describing its general topography<br />
and biological characteristics,<br />
mainly about its marine life and coastal<br />
ecology (Martins, 1978, 1995, 2004;<br />
Morton, 1990; Britton, 1995; Backeljau et<br />
al., 1995; Morton et al., 1998) revealing the<br />
ecological and geological importance of<br />
the place.<br />
Some surveys targeting Cory’s shearwater<br />
and terns were made in the Azores<br />
(del Nevo et al., 1993; Bolton, 2001 and<br />
Monteiro et al., unpublished report) but<br />
none of them went to the islet. Monteiro<br />
et al. (1999) estimated 0 to 10 Bandrumped<br />
storm-petrel couples breeding on<br />
the islet.<br />
Due to the unique importance of the<br />
IVFC as an agglomeration of various<br />
micro-ecosystems, the Azorean<br />
Government established it as a Nature<br />
Reserve in 1983, as provided by the<br />
Regional Legislative Decree nº 3/83/A, of<br />
March 3 rd , and some rules were implemented<br />
with the intention to preserve<br />
and protect the islet; the public access was<br />
restricted to the lagoon, the marine area<br />
of the reserve was extended to 30 m deep,<br />
and fishing and any underwater activity<br />
were forbidden. In spite of these protection<br />
measures, the flora and fauna in the<br />
islet and its lagoon have suffered a significant<br />
negative impact caused by the flood<br />
of people mostly during the summer<br />
(Morton et al., 1998). The islet is popular<br />
for recreation and between May and<br />
September a boat brings in about 400 persons<br />
a <strong>da</strong>y.<br />
This study was developed to identify<br />
the breeding species of seabirds on IVFC,<br />
giving special emphasis to habitat characterization<br />
and threats, thus contributing<br />
to the conservation and protection of<br />
the islet’s natural habitats and their<br />
seabird populations.<br />
MATERIAL AND METHODS<br />
The study was carried out on the<br />
IVFC (N37º42.30’, W25º26.52’), during<br />
July 2006, in the course of the 3 rd international<br />
Workshop on Malacology and<br />
Marine Biology in Vila Franca do<br />
Campo, São Miguel, Azores (Figure 1).<br />
The islet is a drowned volcanic crater<br />
with a surface area of 61.640 m 2 , accessed<br />
by a narrow channel, but with several<br />
fissures also connecting the lagoon with<br />
the sea outside. The main length of the<br />
islet is 420 m from east to west, reaches<br />
an altitude of 62 meters, and is divided<br />
into two portions: the Big islet, that constitutes<br />
almost all the islet’s area and the<br />
Small islet on the northeast side. There<br />
are also several rocks of different sizes,<br />
outstanding the Farilhão with 32.5 m,<br />
and Baixa <strong>da</strong> Cozinha with 19.4 m. On<br />
the islet there is an internal lagoon connected<br />
to the open sea trough chaps and<br />
underwater tunnels. Inside the lagoon<br />
there is a small pier where people enter<br />
the islet (Martins, 2004).<br />
The habitat characterisation of the<br />
islet was made in loco following the<br />
Interpretation Manual of European<br />
Union Habitats (European Habitats<br />
Committee, 1991).<br />
Three different methods were conducted<br />
to identify the seabird species of<br />
the islet, and to estimate species abun<strong>da</strong>nce<br />
and number of breeding pairs:<br />
1. Flush counts<br />
Six boat rides, of 15 minutes each,<br />
were undertaken for flush counts of<br />
seabirds and to observe the external
220 AÇOREANA<br />
2009, Sup. 6: 217-225<br />
coast zone of the islet. The method consisted<br />
on counting the number of individuals<br />
visible from the boat (eye view),<br />
at different hours of the <strong>da</strong>y, three rides<br />
in the morning and three on the afternoon.<br />
Species were identified and all the<br />
individuals standing on the islet or flying<br />
over the sea were counted.<br />
2. Ground searches<br />
Two ground searches were made for<br />
occupied nests of terns and<br />
Porcellariiformes (Figure 1). Signs of<br />
occupation included the presence of an<br />
adult, eggs or chicks in a visible nest<br />
chamber. In sites where a nest chamber<br />
was not visible, a burrow was considered<br />
to be occupied if it was of sufficient size<br />
to accommo<strong>da</strong>te a bird or if there was<br />
one or more evidences of occupation<br />
(e.g. faeces; shed breast feathers, excavated<br />
soil or absence of obstructing vegetation<br />
or spider webs in the burrow’s<br />
entrance).<br />
3. Raft counts<br />
During the breeding season, Cory’s<br />
shearwater characteristically form flocks<br />
(called “rafts”) on the sea, with the number<br />
of individuals increasing by the end<br />
of the <strong>da</strong>y, waiting for nightfall to fly up<br />
to the breeding colony (Mallet &<br />
Coghlan, 1964). According to Rich<strong>da</strong>le<br />
(1963) and Skira (1991) over half of the<br />
adult shearwaters at a colony are<br />
expected to be non-breeders.<br />
Raft counts were conducted for<br />
Cory’s shearwater from two places, one<br />
on the top of the south side of the islet,<br />
and another from Ponta de São Pedro<br />
(N37º42.39’, W25º26.41’) on the coast of<br />
São Miguel island and in front of the<br />
islet; raft counts were made by the end of<br />
the <strong>da</strong>y, starting exactly at 08:00 pm, for<br />
45 minutes long, using binoculars (10 X<br />
50).<br />
All the methods applied in this study<br />
involved two replicates from two different<br />
observers.<br />
RESULTS<br />
Habitats<br />
Two types of natural habitats were<br />
identified on the IVFC (Figure 1): i)<br />
Vegetated Sea Cliffs of the Macaronesian<br />
Coasts habitat, dominated by the endemic<br />
fescue (Festuca petraea), with associated<br />
plants such as rush (Juncus acutus),<br />
wild carrot (Daucus carota), seaside goldenrod<br />
(Soli<strong>da</strong>go sempervirens) and rock<br />
samphire (Crithmum maritimum); ii)<br />
Endemic Macaronesian Heaths habitat<br />
dominated by the endemic green heather<br />
(Erica azorica), with associated plants<br />
such as laurel (Laurus azorica), Myrica<br />
faya, Cyrtomium falcatum, Holcus rigidus<br />
and Euphorbia azorica. This last habitat<br />
presents plenty of exotic plants such as<br />
the giant reed (Arundo donax), used in the<br />
past for protective barriers of the vineyards,<br />
tamarisks (Tamarix gallica), brambles<br />
(Rubus ulmifolius) and australian pittosporum<br />
(Pittosporum undulatum).<br />
On the higher southern and western<br />
inner slopes of the Big islet there are two<br />
small “forests” of iron trees (Metrosideros<br />
tomentosa) and vineyards (Vitis labrusca),<br />
although they are no longer cultivated.<br />
Seabirds<br />
There was evidence of two species of<br />
seabirds breading on the islet (Figure 1),<br />
Cory’s shearwater and Common tern,<br />
but three more species were registered,<br />
Little shearwater, Band-rumped stormpetrel<br />
and Roseate tern, although at present<br />
without any breeding evidence.<br />
Table 1 shows avifauna abun<strong>da</strong>nce<br />
determined through the different methods<br />
used.<br />
Cory’s shearwater breeds on Big islet<br />
with Vegetated Sea Cliffs of the<br />
Macaronesian Coasts habitat where 34<br />
burrows and nests cavities were found,<br />
and on slopes of Endemic Macaronesian<br />
Heaths habitat that exhibited 10 burrows
RODRIGUES ET AL: SEABIRD CONSERVATION AT ILHÉU DE VILA FRANCA 221<br />
TABLE 1. Seabird abun<strong>da</strong>nce from flush and raft counts and number of couples from occupied<br />
nests/burrows on the Ilhéu de Vila Franca do Campo. SD = Stan<strong>da</strong>rd Deviation.<br />
Species<br />
Flush counts<br />
(individuals)<br />
Mean ± SD<br />
Ground searches<br />
(couples)<br />
Raft counts<br />
(individuals)<br />
Mean ± SD<br />
Cory’s shearwater 154 ± 22.6 44 395 ± 21.2<br />
Common tern 325 ± 35.4 80 -<br />
Roseate tern 2 - -<br />
Little shearwater 1 - -<br />
Band-rumped storm-petrel 1 - -<br />
and nests cavities. The three nests found<br />
on Small islet were destroyed or abandoned.<br />
Common terns breed on two external<br />
rocks of the islet, Baixa <strong>da</strong> Cozinha (10<br />
nests) and Farilhão (19 nests), and on the<br />
external coast of the Small islet with<br />
Vegetated Sea Cliffs of the Macaronesian<br />
Coasts habitat (41 nests).<br />
Occasional observations on the populations<br />
of Cory’s shearwater and<br />
Common terns allowed identification of<br />
chicks being reared, incubating parents,<br />
destroyed and abandoned nests and<br />
abandoned eggs (Table 2). It was not possible<br />
to identify the exact number of eggs<br />
laid per couple of Common terns.<br />
Evidences of human disturbance were<br />
found near potential seabird nests,<br />
including recreation, wastes, and van<strong>da</strong>lism<br />
such as broken eggs and burrows<br />
destruction. There were an equivalent<br />
percentage of abandoned nests in both<br />
populations (11%) and about 18% of<br />
Cory’s shearwater nests and 5% of<br />
Common tern nests were destroyed.<br />
Nearly 7% of Cory’s shearwater eggs and<br />
1% of Common tern eggs were abandoned<br />
by the progenitors.<br />
DISCUSSION<br />
The Vegetated Sea Cliffs of the<br />
Macaronesian Coasts habitat of the IVFC<br />
are well preserved probably because they<br />
occur on the external rocks of the islet and<br />
on inaccessible cliffs, but also because<br />
they are highly influenced by salt-water<br />
spray where exotic plants cannot grow.<br />
According to Sjögren (1973) the association<br />
Festucetum petreae is characteristic of<br />
Azores coastal habitats, occurring mainly<br />
in the sea cliffs. The characteristic species<br />
of this association is the common endemic<br />
Festuca petraea, which usually develops<br />
coastal prairies. Other species are found<br />
in this association, such as the common<br />
Soli<strong>da</strong>go sempervirens and Crithmum maritimum,<br />
the less common Tolpis succulenta<br />
and even rarest endemic plants like<br />
Azorina vi<strong>da</strong>lii and Myosotis maritima.<br />
The Endemic Macaronesian Heaths<br />
habitat was much degraded with exotic<br />
plants such as Arundo donax, Lantana<br />
TABLE 2. Number of observations on Cory’s shearwater and Common tern nests on Ilhéu de Vila<br />
Franca do Campo.<br />
Species<br />
Used<br />
nests<br />
Destroyed<br />
nests<br />
Abandoned<br />
nests<br />
Abandoned<br />
eggs<br />
Incubating<br />
couples<br />
Rearing<br />
chicks<br />
Cory’s shearwater 44 8 5 3 9 6<br />
Common tern 80 4 9 1 37 11
222 AÇOREANA<br />
2009, Sup. 6: 217-225<br />
camara and Pittosporum undulatum.<br />
According to the Convention on<br />
Biological Diversity, invasive alien species<br />
which introduction and/or spread threatens<br />
biological diversity are now considered<br />
the second cause of biodiversity loss<br />
at a global level, after direct habitat<br />
destruction (Shine et al., 2000; Groz &<br />
Pereira, 2005).<br />
The methods used in this study to<br />
estimate species abun<strong>da</strong>nce and number<br />
of breeding pairs were effective because<br />
they complemented each other giving a<br />
broader view of the colonies. These<br />
results confirmed nesting of two en<strong>da</strong>ngered<br />
species and listed three other possible<br />
breeders revealing the importance of<br />
the IVFC for the protection and conservation<br />
of seabirds.<br />
Cory’s shearwater breeds generally in<br />
the inaccessible sea cliffs of the islet and<br />
less in slopes with Macaronesian vegetation.<br />
The differences between the numbers<br />
of burrows and nests found in the<br />
Vegetated Sea Cliffs of the Macaronesian<br />
Coasts habitat and in the Endemic<br />
Macaronesian Heaths habitat are probably<br />
related to human disturbance and<br />
degra<strong>da</strong>tion of this last habitat with invasive<br />
alien species that are a threat to<br />
seabird populations (Groz & Pereira,<br />
2005). Adults arrive in colonies by late-<br />
February, lay eggs from late-May to early-<br />
June and hatching is relatively synchronous,<br />
most chicks hatching between 18<br />
and 31 July (Granadeiro, 1991). Young<br />
birds fledge from late-October to early-<br />
November (Monteiro et al., 1996b). They<br />
lay only one egg per year and do not<br />
replace it if it is <strong>da</strong>maged or lost soon<br />
after laying, so there is an ecological significance<br />
when a couple looses their egg,<br />
all the dispended energy is lost and it is<br />
one less breading couple.<br />
Common terns breed in inaccessible<br />
rocks with Vegetated Sea Cliffs of the<br />
Macaronesian Coasts habitat, where<br />
human disturbance is almost absent, and<br />
where they can avoid possible pre<strong>da</strong>tors.<br />
Adults arrive in colonies by early-April,<br />
egg laying occurs from early-May to mid-<br />
June and they stay in colonies until late-<br />
September (Monteiro et al., 1996b). A<br />
clutch of 2-4 (usually 3) eggs is laid. One<br />
brood per season is typical but re-nesting<br />
is common when the first nest is<br />
destroyed (Peterson, 1988). This study<br />
indicates that the colony on IVFC represents<br />
at least 18% of the Azorean total population.<br />
Although being a protected species,<br />
populations of these seabirds are becoming<br />
smaller than in the past, they have been<br />
chased and hunted by humans, and suffered<br />
with pre<strong>da</strong>tion from introduced<br />
mammals and from deforestation<br />
(Monteiro et al., 1996b).<br />
The suite of terns and shearwaters is of<br />
major international conservation<br />
importance (Rodrigues & Nunes, 2002).<br />
Their breeding distributions in the Atlantic<br />
Ocean are concentrated in Europe and<br />
most species have small world populations<br />
(Monteiro et al., 1999) being classified as<br />
globally threatened species (Collar et al.,<br />
1994). The Azorean population of Cory’s<br />
shearwater decreased around 50% between<br />
1996 and 2001 (Rodrigues & Nunes, 2002),<br />
and a similar situation was observed for<br />
Common tern populations, estimated<br />
around 4000 breeding couples for 1992 (del<br />
Nevo et al. 1993), against 2000 breeding<br />
couples for year 2000 (Rodrigues & Nunes,<br />
2002), probably due to the impact of continuous<br />
lost of their habitats.<br />
People’s access to nests and burrows<br />
represents an important threat over<br />
seabirds in the islet, and several impacts<br />
from recreation and van<strong>da</strong>lism, are leading<br />
to their distraction from normal activities;<br />
parents spend less time tending young<br />
birds or eggs, flying away from nests, leaving<br />
eggs or chicks vulnerable to pre<strong>da</strong>tors<br />
and amenity, nests are destroyed and
RODRIGUES ET AL: SEABIRD CONSERVATION AT ILHÉU DE VILA FRANCA 223<br />
seabirds entirely abandon the colonies.<br />
These impacts can affect Azorean seabirds,<br />
particularly Common terns, since the<br />
colony of IVFC represents one of the<br />
largest in the Azores.<br />
Due to the importance of the Azores<br />
archipelago for seabirds in Europe, it is<br />
fun<strong>da</strong>mental to protect every natural habitat<br />
and to conserve the few areas where<br />
they breed, usually steep scarps and islets<br />
(Monteiro et al, 1996b, 1999; Ramos et al.,<br />
1997).<br />
In conclusion, results from the present<br />
work indicate that IVFC plays an important<br />
role on the conservation of Cory’s<br />
shearwater and Common tern populations,<br />
since hundreds of couples of these two<br />
species breed on the islet. But this importance<br />
can be threatened by the continuous<br />
degra<strong>da</strong>tion of their habitats.<br />
Seabirds become mature at a late age,<br />
experience low annual fecundity, often<br />
refrain from breeding, and enjoy annual<br />
adult survival rates as high as 98%. This<br />
suite of life history characteristics limits the<br />
capacity for seabird populations to recover<br />
quickly from major perturbations, and presents<br />
important conservation challenges<br />
(Russell, 1999).<br />
An urgent management plan for IVFC<br />
is necessary, in order to conserve the natural<br />
habitats of the islet and protect their<br />
seabird populations.<br />
According to Groz & Pereira (2005),<br />
islets habitats are expected to respond<br />
rapidly to habitat restoration, so it is urgent<br />
to implement an habitat restoration program<br />
and a major efficient islet control to<br />
people access, in order to improve seabirds<br />
breeding conditions on the islet. A welldesigned<br />
legal and institutional framework<br />
is essential to provide a basis for effective<br />
eradication and control measures of alien<br />
plant species (Shine et al., 2000), control of<br />
soil erosion and multiplication and reintroduction<br />
of native flora. A mark-recapture<br />
analysis is useful for tracking demographic<br />
changes in a population over time<br />
(i.e., assessing population size, adult survival,<br />
and juvenile recruitment) (Brichetti et<br />
al., 2000) and could be used to evaluate the<br />
effect of the habitat restoration programme.<br />
Moreover, seabirds are believed to constitute<br />
useful samplers of the marine environmental<br />
since they have been recognized<br />
as potentially useful and economical indicators<br />
of the status of marine environment<br />
and, in particular, the status of commercially<br />
important prey stocks (Furness &<br />
Greenwood, 1993).<br />
ACKNOWLEDGEMENTS<br />
We are grateful to Professor António M.<br />
de Frias Martins for the opportunity to<br />
undertake this research.<br />
This project was supported by the<br />
Third International Workshop of<br />
Malacology and Marine Biology, Vila<br />
Franca do Campo, São Miguel, Azores, July<br />
2006.<br />
The experiments performed for the present<br />
study comply with the laws of the<br />
country in which they were performed.<br />
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Remembering<br />
Joseph C. Britton (1942-2006)<br />
with Brian Morton and Fred Wells at his side, at the 2nd International Workshop of Malacology<br />
and Marine Biology, Vila Franca do Campo (1991)<br />
Joseph Cecil Britton passed away on 29 th November 2006. His life intersected the<br />
Azores in 1991, when he attended the 2nd International Workshop of Malacology and<br />
Marine Biology, and stayed linked to these islands from then on. I first met Joe at one<br />
of the Hong Kong workshops in 1989. Always polite and respectful, a true companion<br />
in science, beer and joie de vivre, Joe’s good humour made him a valued member of the<br />
team of scientists he joined here in the mutual search for knowledge. He knew that he<br />
was path finding, but this only increased his determination to help Azorean scientists<br />
and students understand their rich marine cultural heritage. His accumulated wealth of<br />
information about marine ecology flowed easily through his elegant discourse (albeit<br />
with a true Texan twang) and his calm devotion to work fostered in everyone a sense of<br />
duty. One of Joe Britton’s greatest contributions to the Azores, and one in which I was<br />
privileged to be part of, was the book Coastal Ecology of the <strong>Açores</strong>, one of a series of<br />
monographs created by Brian Morton, about the shores of Hong Kong and of Texas.<br />
Other works about the ecology and conservation of the Azores followed and, at the time<br />
of his death, he was compiling a huge list of publications related to the marine biology<br />
of the Azores. The completion of this task would form a lasting memorial to him and<br />
his work. Joe Britton was a member of the Editorial Board of Açoreana. A true friend,<br />
Joe will be missed, but his memory will be with us forever.
AÇOREANA é a revista <strong>da</strong> Socie<strong>da</strong>de Afonso Chaves<br />
- Associação de Estu<strong>dos</strong> Açoreanos e visa publicar<br />
trabalhos devota<strong>dos</strong> principalmente às diversas áreas <strong>da</strong><br />
história natural <strong>dos</strong> <strong>Açores</strong>. AÇOREANA está indexa<strong>da</strong> em<br />
BYOSIS, é envia<strong>da</strong> para Zoological Record e distribuí<strong>da</strong> em<br />
regime de troca por bibliotecas de vários países.<br />
Os manuscritos, em Português, Francês ou Inglês,<br />
incluirão um RESUMO e tradução deste numa <strong>da</strong>quelas<br />
línguas. O formato conformar-se-á com o de números<br />
posteriores a 2000. To<strong>da</strong>s as partes do manuscrito (texto,<br />
referências, tabelas, legen<strong>da</strong>s) serão <strong>da</strong>ctilografa<strong>da</strong>s a dois<br />
espaços. Nomes de géneros e espécies serão sublinha<strong>dos</strong>;<br />
to<strong>da</strong>s as outras indicações serão deixa<strong>da</strong>s ao critério do<br />
editor. As ilustrações deverão ser executa<strong>da</strong>s de forma a<br />
permitir uma utilização eficiente do espaço útil (página,<br />
125x180 mm; coluna, 62x180 mm); letras e números<br />
deverão permanecer perfeitamente legíveis após a redução.<br />
As referências no texto seguirão uma <strong>da</strong>s seguintes formas:<br />
‘Dance (1986) descreveu …‘ ou ‘ … (Morton, 1965) …‘ ou ‘…<br />
(Nobre, 1924, 1930; Martins, 1989a, b; Hawkins et al., 1990;<br />
Martins & Ripken, 1998;).’ A bibliografia é lista<strong>da</strong><br />
alfabeticamente e os nomes <strong>dos</strong> autores repeti<strong>dos</strong> sempre<br />
que necessário; os nomes <strong>da</strong>s revistas são apresenta<strong>dos</strong> por<br />
extenso. A listagem bibliográfica (BIBLIOGRAFIA<br />
CITADA) seguirá o formato <strong>dos</strong> números posteriores a<br />
2000, conforme se exemplifica:<br />
HOUBRICK, R.S., 1990. Anatomy, reproductive biology<br />
and systematic position of Fossarus ambiguus (Linné)<br />
(Fossarinae: Planaxi<strong>da</strong>e; Prosobranchia). In:<br />
MARTINS, A.M.F. (ed.), The Marine Fauna and Flora of<br />
the Azores (Proceedings of the First International Workshop<br />
of Malacology, São Miguel, 1988). Açoreana, Supplement<br />
[2]: 59-73.<br />
LEAL, J.H., & P. BOUCHET, 1991. Distribution patterns and<br />
dispersal of prosobranch gastropods along a seamount<br />
chain in the Atlantic Ocean. Journal of the Marine<br />
Biological Association of the United Kingdom, 71 (1): 11-<br />
25.<br />
MORELET, A., 1860. Notice sur l’Histoire Naturelle des <strong>Açores</strong><br />
suivie d’une description des Mollusques terrestres de cet<br />
Archipel, 216 pp. J.-B. Baillière et Fils, Paris.<br />
Tabelas e ilustrações virão após BIBLIOGRAFIA<br />
CITADA, constando no manuscrito o lugar apropriado para<br />
a sua integração; as ilustrações devem ser numera<strong>da</strong>s em<br />
série única; as legen<strong>da</strong>s <strong>da</strong>s figuras serão apresenta<strong>da</strong>s<br />
separa<strong>da</strong>mente após as ilustrações.<br />
Aceitam-se notas curtas que não deverão exceder três<br />
páginas <strong>da</strong>ctilografa<strong>da</strong>s a dois espaços. Normalmente não<br />
comportarão sumário ou subtítulos.<br />
Para salvaguar<strong>da</strong>r a interpretação na<br />
eventuali<strong>da</strong>de de desformatação do material digital, uma<br />
cópia impressa completa com tabelas, legen<strong>da</strong>s e ilustrações<br />
será submeti<strong>da</strong> ao editor, juntamente com uma cópia em<br />
CD ou via e.mail.<br />
SEPARATAS. O primeiro autor receberá 50 separatas<br />
grátis; cópias adicionais a preço de custo poderão ser<br />
requisita<strong>da</strong>s no acto <strong>da</strong> devolução <strong>da</strong>s provas.<br />
CORRESPONDÊNCIA. Enviar para o editor, Prof.<br />
António M. de Frias Martins, Socie<strong>da</strong>de Afonso Chaves -<br />
Associação de Estu<strong>dos</strong> Açoreanos, Apartado 258, 9501-903<br />
Ponta Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal. E.mail:<br />
afonsochaves.sac@gmail.com<br />
AÇOREANA is the journal of the Socie<strong>da</strong>de Afonso<br />
Chaves - Associação de Estu<strong>dos</strong> Açoreanos and aims at the<br />
publication of works devoted mainly to the various areas<br />
of the natural history of the Azores. AÇOREANA is<br />
indexed by BIOSIS, sent to Zoological Record, and distributed<br />
via exchange to libraries throughout the world.<br />
The manuscripts, in Portuguese, French or English,<br />
should include a concise ABSTRACT with a translation of<br />
it in one of those languages. The format of the manuscript<br />
should follow that of the issues after 2000. All<br />
parts of the manuscript (text, references, tables, legends)<br />
should be typed double-spaced. Underline all genus and<br />
species names; leave all other indications to the editor.<br />
The illustrations should be carefully executed to allow<br />
full utilization of space (full page, 125x180 mm; one column,<br />
62x180 mm); letters and numbers should remain<br />
perfectly easy to read after reduction. References in the<br />
text should take one of the following forms: ‘Morelet<br />
(1860) described …‘ or ‘ … (Morelet, 1860) …‘ or ‘…<br />
(Morelet & Drouët, 1857; Morelet, 1860; Nobre, 1924,<br />
1930; Martins, 1989a, b; Hawkins et al., 1990).’<br />
References are listed alphabetically, the authors’ names<br />
repeated; journal titles are cited in full. Bibliographic<br />
listing should follow the format of the issues after 2000,<br />
according to the examples:<br />
HOUBRICK, R.S., 1990. Anatomy, reproductive biology<br />
and systematic position of Fossarus ambiguus (Linné)<br />
(Fossarinae: Planaxi<strong>da</strong>e; Prosobranchia). In:<br />
MARTINS, A.M.F. (ed.), The Marine Fauna and Flora<br />
of the Azores (Proceedings of the First International<br />
Workshop of Malacology, São Miguel, 1988). Açoreana,<br />
Supplement [2]: 59-73.<br />
LEAL, J.H., & P. BOUCHET, 1991. Distribution patterns<br />
and dispersal of prosobranch gastropods along a<br />
seamount chain in the Atlantic Ocean. Journal of the<br />
Marine Biological Association of the United Kingdom, 71<br />
(1): 11-25.<br />
MORELET, A., 1860. Notice sur l’Histoire Naturelle des<br />
<strong>Açores</strong> suivie d’une description des Mollusques terrestres<br />
de cet Archipel, 216 pp. J.-B. Baillière et Fils, Paris.<br />
Tables and illustrations should come after LITERA-<br />
TURE CITED, but there should be in the manuscript an<br />
indication of their insertion; the legends for the illustrations<br />
should be presented separately after the illustrations.<br />
Short notes can also be submitted, not exceeding<br />
three pages typed double-spaced. Normally they should<br />
not include a summary or headings.<br />
To safeguard interpretation of eventually deformatted<br />
digital material, one printed copy complete with<br />
tables, legends and illustrations should be submitted to<br />
the editor, along with a copy in CD or via e.mail.<br />
REPRINTS. The first author receives 50 reprints free<br />
of charge; additional copies, at cost price, can be ordered<br />
when returning the proofs.<br />
CORRESPONDENCE. Manuscripts and<br />
correspondence related to the journal should be<br />
addressed to the editor, Prof. António M. de Frias<br />
Martins, Socie<strong>da</strong>de Afonso Chaves — Associação de<br />
Estu<strong>dos</strong> Açoreanos, Apartado 258, 9501-903 Ponta<br />
Delga<strong>da</strong>, São Miguel, <strong>Açores</strong>, Portugal. E.mail:<br />
afonsochaves.sac@gmail.com