Circulatory organs of Diplura "Hexapoda#] the basic design in ...

PERGAMONInternational Journal of Insect Morphology 17 "0888# 60Ð68Circulatory organs of Diplura "Hexapoda#] the basic design inHexapoda

61B[!A[ Gereben!Krenn\ G[ Pass : International Journal of Insect Morpholo`y 17 "0888# 60Ð681[1[ Light microscopyThe specimens were _xed in Dubosq!Brasil mixtureand stored in 69) ethanol[ The isolated body parts weredehydrated with ethanol[ Using either acetone or pro!pylene oxide as an intermedium\ they were embedded inERL!3195 epoxy resin "Spurr medium# under vacuumimpregnation[ Serial semi!thin sections "0 mm# were madeon an ultramicrotome with glass knives or a diamondknife "Diatome# and stained in a mixture of 0) azure IIand 0) methylene blue in an aqueous 0) borax solutionfor approximately 29 s at 79>C[1[2[ Transmission electron microscopy "TEM#Specimens of Campodea au`ens were dissected and_xed in a 1) paraformaldehyde:1[4) glutaraldehydemixture and\ subsequently\ in 0) osmium tetroxide[Both _xatives were bu}ered in 9[0 M sodium cacodylate"pH 6[3#[ Dehydration and embedding were performedas described for semi!thin sections[ Ultrathin sectionswere stained in uranyl acetate "0 h\ 39>C# and lead citrate"79 s\ 19>C# in a LKB 1058 Ultrastainer and examinedwith a Zeiss EM 891 microscope[1[3[ In vivo observationsThe individuals were anaesthetized by carbon dioxidegas and _xed onto a glass plate with adhesive tape[ Hemo!lymph ~ow was examined by observing the hemocytemovement with a stereomicroscope using heat!protecting_lters[2[ Results2[0[ Dorsal vessel tube\ ostia and intracardiac valves2[0[0[ Campodea augensThe dorsal vessel is a straight tube extending from thehead to the 09th abdominal segment where it opens intoan enlarged hemolymph space\ which we call the caudalchamber "Fig[ 0#[Along the dorsal vessel|s course through the body\ itsdistance to the tergum varies[ Typically\ it runs closelybeneath the tergites[ In the head\ the _rst two thoracicsegments and in the 7th and 8th abdominal segments\however\ the dorsal vessel is more distant from the tergumand close to the intestine[The ostia are slits in the lateral wall of the dorsal vesseland measure about 19 mm in length[ Each ostium has twosmall valve ~aps\ which\ during systole\ prevent back~owof hemolymph from the dorsal vessel lumen into the bodycavity "Fig[ 1A#[ A total of nine pairs of ostia exists inthe dorsal vessel of Campodea au`ens\ two pairs in thethorax and seven in the abdomen[ The thoracic ostiapairs are both located in the metathorax\ one at theanterior and the other at the posterior margin of thissegment[ In the abdomen\ the ostia lie close to the respec!tive posterior margins of segments 0Ð6[Two intracardiac valves channel the hemolymph ~owwithin the dorsal vessel^ one is situated in its anterior andthe other one in its posterior region[ The anterior valveis located just in front of the _rst thoracic ostia pair[ The~aps of this valve allow hemolymph ~ow only towardsthe head[ The posterior intracardiac valve is in the 7thabdominal segment and\ in contrast\ forces the currenttowards the rear "Fig[ 1B#[ Hence\ there are two con!current ~ow directions in the dorsal vessel] before theintracardiac valve in the 7th abdominal segment\ hemo!lymph is being pumped towards the front\ after thatsegment towards the rear[ These anatomical _ndings arecon_rmed in vivo] the bidirectional hemolymph ~owwithin the dorsal vessel has actually been observed[2[0[1[ Catajapyx aquilonarisThe overall morphology of the dorsal vessel is verysimilar to that in Campodea au`ens[ Di}erences of noteoccur in its posterior region] an additional pair of ostia islocated in the middle of the 7th segment of the abdomen[Furthermore\ in the _rst part of that same segment\ thedorsal vessel experiences a localized diminishing of itsdiameter[In this species\ the dorsal vessel|s anterior intracardiacvalve is located in the middle of the metathorax and itspositioning prevents hemolymph back~ow towards therear as in Campodea[ The posterior intracardiac valve isof a di}erent type from that in Campodea] there are novalve ~aps\ but instead\ the vessel wall in the region ofthe last ostia is especially thickened narrowing the vessellumen[ In Catajapyx\ in vivo observations have exhibiteda bidirectional ~ow within the dorsal vessel\ as inCampodea[ Before the 7th abdominal segment\ hemo!lymph is being pumped towards the front\ after thatsegment towards the rear[2[1[ Structures associated with the dorsal vesselThe dorsal vessel is held in its position by connectivetissue _laments acting as suspending strands that span itfrom the tergal cuticle to skeletal muscles and the gut\ ordirectly to its accompanying fat tissue[ The suspendingstrands have a diameter of only a few mm and a length ofabout 49 mm[ They are especially numerous in the meso!and metathorax and in the 6th and 7th abdominalsegments[There is an acellular\ discontinuous lamella attachedto the ventral side of the dorsal vessel which can beregarded as a dorsal diaphragm[ It consists of singleportions in the ostia regions[ Despite their minute size\membrane portions are perforated and allow hemolymphpassage from the periintestinal area to the ostia of thedorsal vessel "Fig[ 1A#[

B[!A[ Gereben!Krenn\ G[ Pass : International Journal of Insect Morpholo`y 17 "0888# 60Ð68 62Fig[ 0[ Design of the circulatory organs in Campodea au`ens[ Dorsal vessel directly linked to the antennal vessels[ In the head\ circumoesophagealvessel ring with trumpet!shaped opening[ Posterior end of dorsal vessel continues into caudal chamber[ Hence\ one vessel each runs into the cerci[Two intracardiac valves within the dorsal vessel\ one in the thorax and the other in the 7th abdominal segment[ The abdominal valve makes possiblea bidirectional ~ow\ the ~ow shunt being in that same segment[ Arrows indicate the observed directions of hemolymph ~ow[In the 6th and 7th abdominal segments and in theposterior region of the metathorax\ there is one pair ofsingle muscle _bers that spans transversally from thedorso!lateral tergal cuticle to the dorsal vessel\ analogousto the situation of the alary muscles in other Hexapoda[2[2[ Antennal vesselsWithin the head\ the dorsal vessel runs closely alongthe dorsal side of the oesophagus up to the front ofthe brain where it ends in a distinct enlargement[ Someprecerebral pharynx dilators run through and beyond thelumen of this terminal bulb[ From its anterior region\ apair of vessels originates entering the antennae "Fig[ 1C#[The antennal vessels have a diameter of about 09 mmand run along the medial side of the antennae[ The vesselsare attached to both the antennal nerves and to theintegument along the entire antenna length[ Towards thetip of these appendages\ the vessels end in a terminalpore[ No muscle _bers could be found in the delicatevessel wall[ In vivo observations have revealed an e}erenthemolymph ~ow in the antennal vessel and an a}erent~ow in the antennal hemocoel[2[3[ Circumoesophageal vessel ringIn both Campodea and Catajapyx\ there is a con!spicuous circulatory structure in the head capsule] a vesselring just behind the brain\ which connects to the dorsalvessel and encompasses the oesophagus "Fig[ 1D#[ Ven!trally\ the vessel ring continues in a trumpet!shaped vesselwhose bell opens towards the head[ Hemolymph fromthe dorsal vessel must therefore pass through this openinginto the ventral part of the head capsule[2[4[ LegsOur investigation of Campodea au`ens has failed toreveal any distinct structures serving hemolymph cir!culation in the legs[ Their hemocoel is replete with muscle_bers[ In the tibia!tarsus joint region\ a tiny septum di!vides the hemolymph space in two for a small section ofthe leg[2[5[ Hemolymph supply of cerci2[5[0[ Campodea augensThe posterior end of the dorsal vessel tube is within

63B[!A[ Gereben!Krenn\ G[ Pass : International Journal of Insect Morpholo`y 17 "0888# 60Ð68Fig[ 1[ Campodea au`ens[ "A# Cross section through dorsal region of 6th abdominal segment[ Note the dorsal vessel with ostium^ the dorsal diaphragmbelow makes hemolymph passage possible "arrowhead#^ "B# sagittal section through 7th abdominal segment showing the intracardiac valve thatenforces the posteriorly directed hemolymph ~ow^ "C# horizontal section through frontal region of the head and antenna bases[ Terminal bulb ofdorsal vessel with cut of precerebral pharynx dilators in cross section[ Anterior end with origin of vessel extending into left antenna^ "D# horizontalsection through head[ Detail with the dorsal vessel between the two halves of the brain[ Note the circumoesophageal vessel ring originating from thedorsal vessel "arrowheads#[the 09th abdominal segment[ There\ it opens into thevoluminous caudal chamber "Fig[ 2A#[ This hemolymphspace is delimited by a septum made up of connectivetissue and by the integument[ Rectum dilators extendwithin the caudal chamber[ Contraction of these musclesmust inevitably lead to compression of this chamber[From the caudal chamber\ one vessel runs to eachcercus "Fig[ 2B#[ These vessels are attached to the cercalintegument\ have a diameter of about 04 mm and extendlaterally within the cerci "Fig[ 2C#[In vivo observations reveal that the e}erent ~ow runsin the cercal vessel[ Hemolymph from the vessel tipmerges in the cercal hemocoel and returns to the bodycavity "Fig[ 3A#[2[5[1[ Catajapyx aquilonarisAs in Campodea\ the posterior end of the dorsal vesselcontinues into the caudal chamber^ its dimensions aremuch smaller than that in Campodea[ The caudal cham!ber branches into two small channels near the end of theabdomen[ The channels run directly beneath the terguminto the forceps!shaped cerci[ In vivo observations ofCatajapyx aquilonaris show that as of the 7th abdominalsegment\ hemolymph ceases its anteriorly directed ~owand starts ~owing towards the rear[ The e}erent hemo!lymph ~ow runs through the channels and back into thegeneral body cavity via the cercal hemocoels "Fig[ 3B#[3[ DiscussionThe present study has revealed that the circulatoryorgans of Diplura largely deviate from the textbookscheme given for this organ system in insects"Wigglesworth\ 0861^ Gullan and Cranston\ 0883^ Seifert\0884#[ These incongruities warrant special interest with

B[!A[ Gereben!Krenn\ G[ Pass : International Journal of Insect Morpholo`y 17 "0888# 60Ð68 64Fig[ 2[ Campodea au`ens[ "A# Sagittal section through last abdominal segment[ Dorsal vessel opens into voluminous caudal chamber delimited bythe integument and by a septum^ "B# cross section through last abdominal segment[ Caudal chamber continuing laterally into cercal vessel^ "C# crosssection through cercal vessel attached to integument "TEM#[ The wall contains no muscle _bers[Fig[ 3[ Design of circulatory vessels and hemolymph ~ow within the posterior part of the dorsal vessel and within the cerci[ "A# Campodea au`ens^"B# Catajapyx aquilonaris[ Arrows indicate ~ow directions[ Note di}erences in number of ostia\ intracardiac valve types and in hemolymph negotiationthrough cercal vessels "A# or channels "B#[

65B[!A[ Gereben!Krenn\ G[ Pass : International Journal of Insect Morpholo`y 17 "0888# 60Ð68regard to both functional morphology and phylogenyand will be discussed against the recently ~ared up argu!ment on the phylogenetic relationships among majorarthropod groups "Wheeler et al[\ 0882^ Averof andAkam\ 0884^ Friedrich and Tautz\ 0884# and on thosebetween basic hexapod lineages "Kristensen\ 0878\ 0880^Kukalova!Peck\ 0880^ Stys and Zrzavy\ 0883^ Koch\0886#[3[0[ Antennal vessels connected to the dorsal vesselDiplura are the only hexapod group in which the an!tennal vessels are directly connected to the dorsal vessel"Pass\ 0880#[ In pterygotes\ antennal vessels may alsobe connected to the dorsal vessel\ albeit via voluminousfrontal sacs "Odonata] Pass\ 0880^ Trichoptera] Pass\0880^ Lepidoptera] Schneider and Kaissling\ 0848#[Undoubtedly\ the major force for hemolymph supplywithin the antennal vessels is the pumping activity ofthe dorsal vessel[ In addition\ the action of precerebralpharynx dilators contributes to this task[ They are locatedwithin the anterior bulbous end of the dorsal vessel[ Theircontraction inevitably causes bulb compression\ rein!forcing hemolymph ~ow into the antennal vessels[ Theantennal vessel walls do not contain muscle _bers^ elasticas the walls may be\ they are incapable of any activecontraction[In contrast\ other Hexapoda have antennal vessels thatare at least primarily separate from the dorsal vessel[In Archaeognatha and Zygentoma\ the antennal vesselsform ampullary enlargements with valved ostia at theirproximal ends which are not pulsatile[ In most otherinsects\ however\ the ampullae are pulsatile due to associ!ated muscles "Pass\ 0880\ 0887#[Since Diplura share the feature of antennal vesselsconnected to the dorsal vessel with myriapods and someprimitive crustaceans\ this can be considered the ple!siomorphic character state in hexapods "Fahlander\ 0827^Siewing\ 0845^ Pass\ 0880#[3[1[ Circumoesophageal vessel ring in the headIn the Diplura head\ we have found a conspicuousring!shaped vessel arching around the oesophagus\ whichwe call the circumoesophageal vessel ring[ It directlynegotiates hemolymph from the dorsal vessel into theventral portion of the head capsule[ In Diplura\ this struc!ture has hitherto gone unnoticed[ Similar structures weredescribed in other Hexapoda[ They were originally des!ignated {sinus perintestinal| in Collembola "Denis\ 0817#\{bras lateral de l|aorte cephalique| in Machilis "Bitsch\0852# and {bras aortique latero!oesophagien| in Ther!mobia "Chaudonneret\ 0849#[ With the latter two\Diplura share a ventral trumpet!shaped openingregarded as a vessel of its own "{aorte ventrale| in Machilisand {aorte sous!oesophagienne| in Thermobia#[ Designand position of these vessels in Archaeognatha and Zyg!entoma so closely resemble those in Diplura that we mayinfer a homology[ This type of vessel is obviously absentin Pterygotes\ which leads us to conclude that it has beendiscarded somewhere along their stem lineage[ Lack ofa circumoesophageal vessel ring can then be seen as asynapomorphy of Pterygota[The mandibular arch in the head of chilopods is a verysimilar structure whence a small vessel branches o} intothe mandibles "Fahlander\ 0827^ Rilling\ 0857#[ Apartfrom the apparent lack of such a mandibular vessel inDiplura\ the respective vessel rings in the two taxa arevery similar with regard to their designs "including thetrumpet!shaped opening# and to their positioning[ Vesselrings may be ancestral characters of the arthropod cir!culatory systems and had originally connected the dorsalto the ventral longitudinal vessel[ In the respective taxa\we are probably confronted with remnants of reductionseries[ The conspicuous similarity of these vessel rings inChilopoda and Diplura may then be interpreted as asynapomorphy of the controversial taxon Antennata[3[2[ Dorsal vessel with bidirectional hemolymph ~owThe dorsal vessel with its paired ostia as well as thedorsal diaphragm are generally considered a syn!apomorphy of arthropods "Weygoldt\ 0868#[ The almostentire lack of alary muscles and of the dorsal diaphragmin Diplura needs to be a derived condition commensuratewith the minute body size of these animals[ According toRichards "0852#\ no ventral diaphragm could be detected[A uniform design of the dorsal vessel without a di}er!entiation into anterior aorta and posterior heart seems tobe the plesiomorphic character state in Hexapoda[ Thisis also supported by the presence of the two thoracic ostia"Nutting\ 0840^ Krenn and Pass\ 0883#[ According to thebasic arthropod design\ the dorsal vessel exhibits a pairof ostia in each segment[ In Campodea\ the ostia pairfrom the mesothorax has probably been shifted into themetathorax and must therefore be considered a derivedcharacter state[ The position of this ostia pair at thevery margin of the metathoracic segment supports thisinterpretation[Hemolymph ~ow patterns in the abdomen are of muchinterest[ While the dorsal vessel with its open posteriorend has been known since Grassi "0776# and a backward~ow behind the 7th abdominal segment since Marten"0839#\ the structures for hemolymph supply to the ter!minal body appendages have been obscure[ Ostia aremissing in the terminal segments as of the 7th abdominalsegment in Campodea and as of the 8th one in Catajapyx[The bidirectional hemolymph ~ow is undoubtedly a stu!pendous feature of the dipluran dorsal vessel[ There aretwo ~ow directions within the dorsal vessel] before the7th abdominal segment\ hemolymph is being pumpedtowards the front\ behind that segment towards the rear[

B[!A[ Gereben!Krenn\ G[ Pass : International Journal of Insect Morpholo`y 17 "0888# 60Ð68 66Fig[ 4[ Distribution of the various character states in the circulatory organs of the basic Hexapoda and in their possible sister groups mapped onto acladogram "relationships of Hexapoda according to Kristensen\ 0880#[This bidirectional ~ow pattern is facilitated through theposterior intracardiac valve[ In Campodea\ the intra!cardiac valves may have originally been derived fromreduced ostia as has been postulated for the intracardiacvalves of other insect species "Popovici!Basnosanu\ 0894^Gerould\ 0827#[Bidirectional ~ow patterns have also been observed inother basic hexapods "Fig[ 4^ Archaeognatha] Bar\ 0801^Barth\ 0852^ Zygentoma] Rousset\ 0863^ Ephemeroptera]Meyer\ 0820^ Gereben!Krenn and Pass\ unpublisheddata#[ This condition can therefore be regarded ple!siomorphic in Hexapoda[ Functionally\ it is related to thehemolymph supply of the long body appendages found inthese animals[ Outgroup comparison has yielded thatalso some crustaceans possess a bidirectional hemolymph~ow in their dorsal vessels "Siewing\ 0845#[3[3[ Caudal chamber\ cercal vessels and channelsWhether or not the common hexapod ancestor borecerci is in dispute "Kristensen\ 0880^ Kukalova!Peck\0880^ Bitsch\ 0883#[ It goes without doubt\ however\ thatDiplura are the most basic of the recent taxa to have suchappendages[ The present study examines their supplywith hemolymph for the _rst time[ In both Campodeaand Catajapyx\ the tubular dorsal vessel communicatesvia the caudal chamber with the structures supplyinghemolymph to the cerci[ These structures are dissimilar in

67B[!A[ Gereben!Krenn\ G[ Pass : International Journal of Insect Morpholo`y 17 "0888# 60Ð68the two species which is probably related to the di}erentmodes of cerci insertion[ In Catajapyx\ the cercal chan!nels run directly beneath the dorsal cuticle into theforceps!shaped cerci[ In Campodea\ vessels run muchdeeper within the body until they continue in the _liformcerci[In contrast to that in Catajapyx\ the caudal chamberin Campodea is compressible via rectum dilators[ Hence\what we have here is an additional pumping structureanalogous to the terminal bulb at their anterior end ofthe dorsal vessel[In Campodea\ the structure of the vessels in both theantennae and cerci are similar[ Cercal vessels also existin other basic Hexapoda and also in basic Pterygota "Fig[4#[ Their modes of communication with the dorsal vesselare manifold and as yet quite obscure[ In exopterygotes\as in Plecoptera\ the cercal vessels stand loose from thedorsal vessel and speci_c suction pumps at the cercusbases serve the circulation in the appendages "Pass\ 0876#[4[ ConclusionWith regard to their circulatory organs\ the Dipluramay be seen as a {missing link| between insects and otherarthropods "Fig[ 4#[ According to the prevailing concep!tion\ the hexapod ancestor is supposed to have had arather small body size "Kraus and Kraus\ 0883#[ Conse!quently\ it may have possessed a largely reduced vesselsystem[ Diplura\ despite their minute size\ have retainedsome of the original circulatory organ features\ whichthey share with the possible sister groups of Hexapoda\that is\ the circumoesophageal vessel ring and the factthat the peripheral vessels are linked to the dorsal vessel[The circumoesophageal vessel ring has been lost some!where at the evolutionary origin of Pterygota[ The anten!nal vessels have probably been decoupled from the dorsalvessel along the stem lineage of Ectognatha\ whichnecessitated the development of accessory pulsatileorgans "Pass\ 0880\ in press#[ The cercal vessels weredecoupled from the dorsal vessel in basic exopterygotes\which likewise entailed the appearance of speci_c acces!sory pulsatile organs "Pass\ 0876#[ The change of hemo!lymph ~ow modes within the dorsal vessel frombidirectional to unidirectional may be judged from a per!spective of hemolymph supply to the cerci[ While thebasic hexapod groups feature a bidirectional hemolymph~ow\ exopterygotes "with the only exception of Ephemer!optera# exhibit an unidirectional ~ow towards the head[In higher insects\ heartbeat reversal evolved as still an!other ~ow mode "Gerould\ 0827^ Wasserthal\ 0871\ 0885#[Recently\ the monophyletic status of Diplura has beendismissed "Bilinski\ 0872^ Stys\ Zrzavy and Weyda\ 0882^Stys and Zrzavy\ 0883# but again advocated "Koch\0886#[ The present study has failed to produce data con!tributing to this issue[ Yet comparative analysis lets usconclude that the circulatory system of Diplura possessesthe highest number of plesiomorphic characters amongextant Hexapoda and may provide a clue to the situationin their common ancestor[AcknowledgmentsWe are very grateful to G[ Rothe and T[ Gatschneggfor their excellent technical assistance\ to H[ Grillitschand T[ Gatschnegg for their help with the illustrations\to E[ Christian for the determination of specimens\ to J[Bitsch\ H[W[ Krenn and L[T[ Wasserthal for criticallyreading the manuscript and to T[ Micholitsch for linguis!tic assistance[ This study was supported by the AustrianScience Foundation "Project P 09520!BIO#[ReferencesAverof\ M[\ Akam\ M[\ 0884[ Insect!crustacean relationships] insightsfrom comparative developmental and molecular studies[ Philo!sophical Transactions of the Royal Society of London 236 "ser[ B#\182Ð292[Barth\ R[\ 0852[ UÝber das Zirkulationssystem einer Machilide "Thy!sanura#[ Memorias do Instituto Oswaldo Cruz Rio de Janeiro 50\260Ð288[Bar\ H[\ 0801[ Beitrage zur Kenntnis der Thysanuren[ Jenaische Zeit!schrift fur Naturwissenschaften 37\ 0Ð81[Bilinski\ S[\ 0872[ Di}erentiation 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