Associations and interactions between gorgonians ... - Porifera Brasil

Porifera Research: Biodiversity, Innovation and Sustainability - 2007443Associations and interactions between gorgoniansand spongesElizabeth L. McLean (*) , Paul M. YoshiokaDepartment of Marine Sciences at the University of Puerto Rico – Mayagüez , PO Box 9013, Lajas, PR 00667-3264.elmclean@sbcglobal.net, p_yoshioka@cima.uprm.eduAbstract: The biodiversity of sessile marine invertebrates in coral reefs may be highly dependent upon associations andinteractions between species. In this study we describe the associations (i.e. physical contact between organisms) andsubsequent interactions (e.g. competitive overgrowth, mutualistic effects) between sponges and gorgonians in La Parguera,southwest coast of Puerto Rico. Nearly half (15/32) of the sponge species were epibiotic on other sessile organisms. Thenumber of gorgonian colonies associated with sponges was positively correlated with the relative abundances of the gorgoniantaxa indicating that associations with sponges are generally random in nature. For instance, Pseudopterogorgia spp. wasthe most abundant gorgonian taxa and was the most often associated with sponges. Ecological interactions often involvedovergrowth of gorgonians including Pseudopterogorgia americana, Gorgonia ventalina and Pseudoplexaura spp. by spongessuch as Desmapsamma anchorata, Iotrochota birotulata, Dysidea janiae and Monanchora barbadensis. Of the 14 mostabundant gorgonian taxa, three were only mildly affected by sponges, and tissues of the remaining were killed by overgrowth.In contrast to negative effects, field observations suggest that Briareum asbestinum has mutualistic interactions with sponges.These results indicate that epibiotic associations may be a major factor for the high biodiversity of sponges in Caribbean reefs.As indicated by their relationships with gorgonians, these associations are largely random. However, interactions with theassociated organisms appear to be species-specific.Keywords: biodiversity, coral reef, gorgonians, sponges, species associationsIntroductionSpace on marine hard substratum is a limiting resourcefor numerous sessile organisms in coral reefs (Jackson 1977,Connell 1978) and is a major factor affecting biodiversity inthis habitat. Organisms growing in close proximity will oftencompete for suitable substrate by overgrowing, crowding,undercutting, digesting, overshadowing, or poisoning eachother (Bakus et al. 1986). These interactions can affect theorganization and function of reef communities (Buss andJackson 1979, Wulff 2005). Stebbing (1973) and Wahle(1980) observed that competitive interactions that occuramong sessile organisms are often intense because of theirinability to change locations. These competitive interactionsmay be influenced by many factors including habitat conditionsas well as by competitive hierarchies or networks (Buss andJackson 1979). In addition to negative (competitive) effects,interactions with scleractinian corals may have beneficial(mutualistic) effects by increasing coral survival (Goreauand Hartman 1963, Wulff and Buss 1979). Sponges may alsoenhance biodiversity by harbouring numerous invertebratespecies (Neves and Omena 2003, Ribeiro et al. 2003). Spongesalso clear up the water column, increase primary productivityby recycling nutrients and serve as food for other organisms(Reiswig 1971, Diaz and Rützler 2001, Wulff 2001).In this study we describe the associations and interactionsof sponges with other sessile organisms with special attentionto the gorgonians. To avoid misunderstanding, it should benoted that associations and interactions are not synonymous.Associations refer to the physical contact between spongesand gorgonians; whereas interactions refer to the post-contactecological outcome of the association.Interactions often involves overgrowth, defined here asthe elevation of the growing edge of one individual over theedge of another one (Stebbing 1973). Overgrowth generallyinvolves the death of the overgrown tissue although recoverycan occur in some instances (Buss and Jackson 1979, Russ1981). Specific overgrowth mechanisms include differentialgrowth rates (Buss and Jackson 1979, see also Lang 1973)and allelochemicals (Buss and Jackson 1979). Jackson andBuss (1975), Suchanek et al. (1983) and Aerts and van Soest(1996) suggest that these mechanisms are generally welldevelopedin sponges enabling them to outcompete corals forspace. Other interactions include standoff situations (Aerts2000), where growth of both organisms ceases at the contactboundary and intermingled growth which may benefit bothspecies by increasing structural support and predator defenses(eg., Wulff 1997).Materail and methodsThe study site is located at a depth of 6.7 m off of MediaLuna reef (17° 56.2’ N, 67° 3.2’W) in La Parguera, southwestcoast of Puerto Rico (see Yoshioka and Yoshioka 1989).

444This site has no emergent reefs, is characterized by a lowtopographic relief, and is exposed to wave action generatedby trade winds. Gorgonians are the visually dominant sessilemacroinvertebrate taxa at this study site.Sponges and their associations with gorgonians weresurveyed during December 2005 – February 2006 in a 1 x 20m belt transect. The nature of interaction between gorgonianand sponges (eg, overgrowth of the gorgonian) was inferredfrom five monitoring surveys between October 2003 – January2005 at approximately four month intervals. Gorgonians inthis transect have been monitored since 1983 (Yoshioka andYoshioka 1989, Yoshioka 1998, 2005). To determine whetherassociations were positive, random or negative we comparedthe observed frequencies of sponge – gorgonian associationsto expected values based on the relative abundances ofgorgonian species. For instance, the association would bepositive if the observed frequency of a gorgonian speciesoccurring with sponges is greater than expected value basedon its relative abundance. Photographs were also taken forreference purposes.ResultsA total of 32 demosponge species were found in the studyarea. Of these, 18 (56%) were growing on other sessileorganisms (Table 1). The vast majority (15/18) of thesesponges were associated with gorgonians, probably becausegorgonians constituted the greatest proportion of bioticsubstrate (at least in terms of their visual dominance) at thestudy site. Sponges were associated with 4.1% (71/1730) ofthe gorgonian colonies. Desmapsamma anchorata, Dysideajaniae, and Iotrochota birotulata were the sponges mostcommonly found on gorgonians. The associations betweengorgonian and sponge species are given in Table 2. Gorgoniansmost commonly associated with sponges were also the mostabundant gorgonian taxa in the transesct: Pseudopterogorgiaspp., Pseudoplexaura spp., and Gorgonia ventalina.In terms of quantitative relationships, the proportions ofgorgonian colonies associated with sponges were significantlycorrelated (r 2 = 0.899, p < 0.01) with the relative abundancesof the gorgonian taxa (Fig. 1). The 95% CL of the regressionslope is not significantly different from 1.00 ( 0.72 – 1.02)indicating that proportions of sponge associated gorgonianTable 1: Sponge species and their substrates in the study area. Abiotic substrates include rock, rubble and sediment. Three additionalunidentified sponges (likely pertaining to order Dendroceratida and Order Halisarcida) were found only on abiotic substrates.SpeciesSubstrateAbiotic EpibioticCommentsAmphimedon compressa Duch. and Mich., 1864 yes yes On rocks, sediments, gorgonians and other spongesA. viridis Duch. and Mich., 1864 yes yes On rocks, sediments and gorgoniansCliona varians (Duch. and Mich., 1864) yes no On rocks and rubbleAplysina spp. Nardo, 1834 yes yes On rocks and gorgoniansArtemisina melana Vosmaer, 1885 yes no On sedimentsCallyspongia vaginalis Lamarck, 1814 yes yes On rocks and gorgonians. Often with zoanthids and brittle stars onits surfaceC. plicifera Lamarck, 1814 yes no On rocks. Often with zoanthids and brittle stars on its surfaceChondrilla nucula Schmidt,1862 yes no On sediments and coral rubble. Often binds coral rubbleCinachyra spp. Sollas, 1886 yes no On sediments. Often covered with brown algae and sandCliona delitrix Pang, 1974 yes yes Overgrows and bores dead/live corals. Often with zoanthids andbrittle starsC. caribbaea (Langae) Carter, 1882 (Pang, 1973) yes yes Overgrows and bores dead/live corals and hydrocoralsDesmapsamma anchorata Carter, 1882 yes yes On rocks, sediments, buoy lines, gorgonians, hydrocorals, zoanthidsand other sponges.Dysidea janiae Duch. and Mich., 1864 yes yes On gorgonians and very common on buoy linesEctyoplasia ferox Duch. and Mich., 1864 yes no On sediments, rocks and rubbleHaliclona implexiformis Hechtel, 1966 yes no On rocks and coral rubbleIotrochota birotulata Ridley, 1884 yes yes On sediments, rocks and gorgonians. Often with zoanthids andbrittle stars on its surfaceIrcinia strobilina Lamarck, 1816 yes yes On sediments, rocks, rubble and gorgoniansMonanchora barbadensis Hechtel, 1969 yes yes On coral rubble and gorgoniansM. unguifera van Soest, 1984 yes yes On rocks, rubble and gorgoniansMycale laevis Carter, 1882 yes yes On numerous hard coral speciesM. carmigropila Hajdu and Rützler, 1998 yes yes On rocks and gorgoniansM. laxissima Duch. and Mich., 1864 yes no On sediments, rocks and rubbleNeofibularia notilangere Duch. and Mich., 1864 yes no On sediments and dead coral. Harbors numerous invertebratesNiphates erecta Duch. and Mich., 1864 yes yes On sediments, gorgonians and other sponges. Often with zoanthidsand brittle starsNiphates caycedoi (Zea and van Soest 1986) yes yes On sediments, rocks, rubble and gorgoniansPlakortis spp. Schulze, 1880 yes no On sediments, rocks and rubbleScopalina ruetzleri Wiedenmeyer, 1977 yes yes On sediments, corals, gorgonians, hydrocorals and other spongesVerongula rigida Esper, 1794 yes no On sediments, rocks and rubbleXestospongia proxima Duch. and Mich., 1864 yes yes On sediments, rocks, rubble and gorgonians

Table 2: Associations of sponges and gorgonians. The values represent the number of observed incidences. See gorgonian taxa code givenin Fig. 1.445Sponge species Br Ecal Emam Esuc/ElaxGorgonian speciesGv Mur Mflv PflxPh/PhkPsx Pa Pte Plla Total %Amphimedon compressa 1 2 2 2 1 7 0.075Amphimedon erina 1 4 1 1 1 3 11 0.118Callyspongia vaginalis 1 0 0.000Chondrilla nucula 1 0 1 0.011Desmapsamma anchorata 9 5 4 1 2 3 5 20 0.215Dysidea janiae 1 1 2 26 30 0.323Iotrochota birotulata 3 7 1 6 1 1 1 3 9 8 6 43 0.462Ircinia strobilina 1 2 2 1 2 1 7 16 0.172Monanchora unguifera 1 1 1 1 8 3 15 0.161Mycale laevis 1 1Mycale laxisima 1 1 0 2 0.022Mycale carmigropila 1 0 0 0.000Niphates erecta 3 1 2 1 2 3 6 18 0.194Niphates caycedoi 1 0 1 0.011Scopalina ruetzleri 1 1 2 1 5 0.054Xestospongia proxima 2 2 0.022Total 14 18 2 18 11 2 4 12 15 21 67 1 3 171Fig. 1: Relative abundances (percentages) of colonies of gorgonian species versus the relative abundances associated with sponges. Gorgonianabundances derived from Yoshioka and Yoshioka (1989). Br = Briareum asbestinum was excluded from the regression analysis. Taxa codegorgonians in decreasing order of abundance are Pa = Pseudopterogorgia americana Gmelin, 1791 and Pseudopterogorgia acerosa Pallas,1766; Ecal = Eunicea calyculata Ellis and Solander, 1786 and E. tourneforti Milne Edwards and Haime, 1857; Psx = Pseudoplexaura spp.Houttuyn 1772; Esuc = Eunicea succinea Pallas, 1766, Elax = E. laxispica Lamarck, 1815; Gv = Gorgonia ventalina Linnaeus, 1758; Pflx= Plexaura flexuosa Lamouroux, 1821; Ph = Plexaura homomalla Esper, 1792. The less abundant unlabeled taxa in the figure include: Mur= Muricea elongata Lamouroux, 1821 - M. muricata Pallas, 1766; Mflv = Muriceopsis flavida Lamarck, 1815; Plla = Plexaurella spp.; Esp. 7 = Eunicea sp. 7, Emam = Eunicea mammosa Lamouroux, 1816; Elac = Eunicea laciniata Duchassaing and Michelotti, 1860; Efus =Eunicea fusca Duchassaing and Michelotti, 1860; E sp. 2 = Eunicea sp. 2; Pte = Pterogorgia anceps Pallas, 1766.

446species are equivalent to their relative abundances in thestudy site. This result indicates that the number of coloniesof the gorgonian species associated with sponges are mostlydetermined by the abundances of the gorgonian species.Associations between sponges and gorgonian species can bedescribed as random in this respect. A notable exception tothis overall random pattern was Briareum, which was foundhighly associated with sponges relative to its low abundance.Most interactions with sponges had negative effects ongorgonians as observed in the overgrowth (smothering) ofvarious gorgonian species by sponges such as Desmapsammaanchorata, Dysidea janiae and Iotrochota birotulata.Smothering could be ‘direct’ in the sense that the spongeadhered directly to the tissue/skeleton of the overgrownorganism (i.e., direct smothering, Fig. 2) or ‘indirect’ wherelethal or non lethal effects occurred without the adherenceof the sponge tissue (i.e., indirect smothering). These andother interactions are given in Table 3. These interactionswere often species-specific. For instance, Desmapsammaanchorata usually outcompeted Pseudopterogorgia spp.by direct overgrowth but tissue discoloration of Gorgoniaventalina adjacent to the growing edge of Desmapsamma(Fig. 3) indicated the presence of allelochemicals.A notable exception to the negative interactionswith gorgonians was observed between Briareum andDesmapsamma anchorata, Amphimedon compressa, andMycale carmigropila. In these cases, Briareum and spongecolonies were intertwined and no indications of negativeinteractions were observed.DiscussionWe stress that the results of this study are preliminary inthe sense that future observations will increase the numberof sponges and associated species as well as species-specificinteractions. Nevertheless, some general inferences can bemade about Caribbean sponges and the biodiversity of coralreefs. As in the case of tropical rainforests where the treecanopy accounts for much of the biodiversity, the gorgonian‘canopy’ serves as a habitat for many sponge species. Ourresults thus indicate that the high biodiversity of sponges ispartially attributable to their ability to circumvent substratespace limitation in coral reefs (Connell 1978) by growingepibiotically on other sessile organisms (Rützler 1970). Inturn, sponges harbor numerous invertebrate species (Nevesand Omena 2003, Ribeiro et al. 2003).The associations and interactions of sponges with otherspecies also affect the biodiversity of sponges. Our resultssuggest that, with the exception of Briareum, the relativeabundance of gorgonian taxa largely determines theirassociations with sponges. This pattern represents a randomassociation in the sense that the probability of a gorgoniancolony being associated with sponges is equal amongindividuals of all gorgonian species. In contrast to patternsof associations, interactions between sponges and gorgoniansare often species-specific. Depending upon the speciesinvolved negative interactions may involve direct or indirectsmothering or allelochemicals. Also, in addition to negativeinteractions, the intertwined growth morphology observedbetween Briareum and various sponges may be indicativeFig. 2: Adherence of Dysidea janiae to Pseudoplexaura spp. Directsmothering of the tissue of Pseudoplexaura spp. caused by theovergrowing Dysidea janiae.Table 3: Sponges associated with gorgonians and their modes ofinteraction.SpeciesAmphimedon compressaAmphimedon erinaCallyspongia vaginalisDesmapsamma anchorataDysidea janiaeIotrochota birotulataIrcinia strobilinaMonanchora arbusculaMonanchora unguiferaMycale laevisMycale microsigmatosaNiphates erectaScopalina ruetzleriXestospongia caycedoiInteractionsovergrowth, smothering andintertwined growthsmotheringsmotheringovergrowth, smothering andintertwined growthovergrowth, smotheringovergrowth, smotheringovergrowth, smotheringovergrowthsmotheringsmotheringintertwined growthovergrowth, smotheringsmotheringsmothering

447Fig. 3: Overgrowth of a Gorgoniaventalina colony by Desmapsammaanchorata. A. May 2004; B.January 2005. Note the dying/dead tissue (arrow) in front of theDesmapsamma anchorata colonyindicating allelopathic effects.of a mutualistic interaction. Wulff (1997) documented thatintertwined growth of sponge species has mutualistic effects(see also Calcinai et al. 2004).Jackson (1977) suggests that the nature of interactionsis related to various biological characteristics, such asdifferences in growth rates and morphologies of the spongeand associated organism. The inferred allelochemical effectsof Desmapsamma anchorata on Gorgonia ventalina areconsistent with the observations of Buss and Jackson (1979).Combined with possible mutualistic effects of Desmapsammaanchorata with Briareum and negative (overgrowth)interactions with other gorgonians, these results indicate thatvariations in species-specific interactions may be a majorfactor underlying the high biodiversity of coral reef systems.AcknowledgementsWe are grateful to Sven Zea for his assistance on the identificationof sponge species and to Klaus Rützler for revision and providinginsights on the manuscript. We thank E. Rodriguez, C. Prada, and A.Mercado for their assistance in the field, the staff of the Departmentof Marine Sciences of the University of Puerto Rico Mayagüez forall their help and support. Funding was provided by NOAA – CRESprogram (NA 17OP2919).ReferencesAerts LAM (2000) Dynamics behind standoff interactions in threereef sponge species and the coral Montastraea cavernosa. MarEcol 21: 191-204Aerts LAM, van Soest RWM (1996) Quantification of sponge/coralinteractions in a physically stressed reef community, NE Colombia.Mar Ecol Progr Ser 148: 125-134Bakus GJ, Targett NM, Schulte B (1986) Chemical ecology ofmarine organisms: an overview. J Chem Ecol 12: 951-987Buss LW, Jackson JBC (1979) Competitive networks: nontransitivecompetitive relationships in cryptic coral reef environment. AmNat 113: 223-234Calcinai B, Bavestrello G, Cerrano C (2004) Dispersal andassociation of two alies species in the Indonesian coral reefs:the octocoral Carijoa riisei and the demosponge Desmapsammaanchorata. J Mar Biol Assoc UK 84: 937-941

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