Groomingstructure and function m someterrestrial Crustacea

JE,FFG.HOLMQUIST* N atio nal Audubon Soc iety Researc h Department, Tavernier,F lorida, USA * Presentaddress: Department o.f Biological Sciences,Florida StateUniversity, U.S.A.

ABSTRACT

The terrestrialenvironment, with a unique set of fouling parameters,has been invaded by certainamphipod, isopod, and decapod species. In an effort to characterizegrooming in these ,behavior of representativeorganisms was recorded,and grooming appendages were examinedwith light and scanningelectron microscopy. The mouthpartsand gnatho- pods, particularly the scale-bearingsecond pair, were the primary amphipod grooming appendages.Isopods most frequentlyused the mouthpartsand first pereiopodsfor grooming, but all pereiopodsperformed some acts. The mouthpartswere armed with both scalesand setae,whereas the first pereiopodsmade use of a seta-linedcarpal groove and the seto-ce proximal propodus.Hermit crabsused specialized setae on the third maxillipedesand fifth pereiopodsfor most groomingbut usedthe unmodifiedfirst, second,and third pereiopodsas well. Most brachyurangrooming was performedwith modified setaeon the third maxilli- pedalpalps and epipods,with a row of simple setaeon eachchelipede merus, and with the 'semiterres- chelipedefingers. The unspecializedwalking legsrubbed each other. Terrestrial, trial', and aquaticamphipods of the superfamilyTalitroidea have basically similar grooming behaviorbut differ in morphology.Although thereis a paucityof literatureon aquaticisopod, hermit crab, and brachyurangrooming, particularly with regard to speciestaxonomically closeto the terrestrialcrustaceans, minor differencesin groomingbehavior and morphology betweenthe two groupsappear to be the rule.

I INTRODUCTION

Only threecrustacean orders have representatives that can claim a truly successfulassault on the terrestrialenvironment: , , and Decapoda.Those species that have attainedsome degree of successon land encountera varietyof problems.These organisms mustguard against dehydration by modificationof activity patternsand respiratory, excretory, andecdysal mechanisms. Furthermore, terrestrial crustaceans have compensated structurally for the lack of a supportivemedium and developed new reproductivestrategies. In additionto the aboveproblems, terrestrial crustaceans are subjectto fouling pressures ratherdifferent from thoseof an aquaticenvironment. Articular membranesmay be abraded by granularmatter (Koepcke& Koepcke 1953),and sensoryorgans are more likely to be 95 96 JeffG.Holmquist damagedor disruptedby debristhan are the receptors of marinecrustaceans (Price & Holdich 1980).Land crabsare colonized by nematodes(Carson 1967),mites, Drosophilc larvae, and copepods(literature reviewed by Bright & Hogue 1972),andtheir exoskeletonsare degraded by certainbacteria (Iversen & Beardsley1976). Sowbugs are fouled by amoebae,ciliates, rotifers,and nematodes(literature reviewed by Vandel 1960)and are actively parasitizedby tachinidfly larvae(Bedding 1965, Sassaman & Garthwaite1984). Beach hoppers are ofren infestedwith mites (Canaris1962, Scurlock 7975,Kitron 1980).Nevertheless, terrestrial crustaceansare certainly under less epizoic pressure, as Bauer (1981) observes, than are their marine counterparts.In light of this unique fouling scenario,how do theseanimals groom, andwhat morphologicaladaptations abet this groomingbehavior? In an effort to answerthis question,several terrestrial species were investigated:the leaf- litter inhabiting,cosmopolitan amphipodsTalitroides alluaudi (4) and Talitroidestopitotum

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Figure 1. Representativegnathopod types. A. Simple (unguiform) first gnathopod of female Tethorchzstia n. sp. B. Mittenlike second gnathopod of female Talitroides topitotwn. C. Subihelate first gnathopod of male grillus. Note fields of scalesin B and C. C-carpus;D-dactylus; M-merus; P-propodui;Uar = SOp (from Holmquist I 982). Groomingstructure andfunction in someterrestrial crustacea 97

(4); a conglobatingisopod, Cubaris murina (4), and a non-conglobatingisopod, Iaevis(4); the hermit crabCoenobita clypeatus (4); and the land crabCardisoma guanhumi (3+). (The numbersin parenthesesrefer to the organisms'positions on Powers & Bliss's '5' (1983)scale of terrestrialadaptation, with a indicatinga very high degreeof tenestriality (someeven xeric) and a'l' a low degree(midlittoral).) The ensuingmaterial on C.murina, P.laevis,C.clypeatu.s, and C.guanhumiis new; the Amphipoda section summarizesand extendsrelevant portions of previouswork (Holmquist 1981, 1982, 1985).The functional morphology of grooming in these organismsis comparedwith availableinformation on comparablemarine and grade 2and3 crustaceans.

2 MATERIALS AND METHODS

A11 specimenswere collected from the Florida Keys by hand, with the exception of Cardisoma,which were takenwith a PVC modificationof Bamwell's (1982)Philippine crab trap.Because virtually all of their groomingmovements were performedventrally and thus hiddenfrom dorsalview the isopodswere observedin a transparentcontainer placed on top of the clear glassstage of an inverteddissecting microscope, thus providing a ventral view. Coenobitaclypeatus andCardiosoma guanhumi were observedin both the lab and the field. Someof the hermitswere ffansfenedto surrogate,glass shells so that movementsof the fifth pereiopodscould be observed.Movements were recordedwith a Minolta )(L 401 Super-8 movie cameraand a Wild PhotomakroscopM 400 in conjunctionwith a Wild Photoautomat MPS 55. Morphological examinationswere carried out with light and scanningelectron micro- scopy.In preparationfor SEM, dissectedappendages were ultrasonicallycleaned, fixed with cold3%oglutaraldehyde in 0.1 M sodiumcacodylate buffer for two hours,and rinsed in buffer. They were then dehydratedin an ethanol seriesand critical-point dried. Specimenswere coatedwith 60Vogoldl$}Vo palladium and examinedwith an ISI-DS 130 or JEOL JSM-3JC scanningelecffon microscope.

3 AMPHIPODA

3.1 Morphology The superfamilyTalitroidea is unusualin that it includesrepresentatives from a variety of markedly different habitats.The first two pairs of pereiopods,or gnathopods(Fig. 1), of marine (Hyalidae: Parhyale hnwaiensis)and freshwater (Hyalellidae: Hyalella azteca) species,grade 3 beach hoppers (: Orchestia grillus and Tethorchestian.sp. (Bousfield,pers. comm.)), and terrestrial(grade 4) leaf litter inhabitants(Talitridae Talitroi- des alluaudi and T.topitotum)were examinedby Holmquist (1982), who emphasizedthe groomingstructures of theseappendages. Unlike most talitroideans,T.alluaudi andT.topitotum are neotenic.The sexesthus have similar gnathopodstructure, the maleslacking the largesubchelate gnathopod characteristic of manyother species. The first gnathopodsare simple (unguiform) and are armed with stout, 'mittenlike' but unspecialized,setae (Figs. 1A, 2A). The secondgnathopods are and have pellucidlobes (Hurley 1959,1968) on the propodus,carpus, and merusGigs. 18, 2B). In bothT.alluaudi andT.topitotum,these lobes cornprise about one-quarter of the total surface 98 JeffG.Holmquist

areaof the four distal segmentsand are coveredwith broad expansesof bristle-likescales Gigs. 18, 28, C, D), which arearranged in irregularrows. The scalesof [email protected]) occur in smallerpatches and appearto be somewhatmore filifonn than thoseof T.alluaudi Grg.2C). Femalesof the sexually dimorphic Orchestiacomplex have first fig. lA) and second gnathopodsquite similar to thoseof Talttroides.However, unlike Talitroide.r, orchestid males have small subchelate(Fig. 1C) first gnathopodsand large subchelatesecond gnathopods. Both sexespossess echinatefields on the variousgnathopodal lobes. These fields of scales have been described from O.gammarellus (Charniaux-Cotton lg57), O.cavimana, O'medtterranea, O.montagui,O.gammarellus, and Platorchestia platensis (Graf & Sellem 1910) and from o.grillus and,Tethorchestian. sp. (Holmquist lg1z).In conrrastto the bristle-likescales of Talitroides, thoseof orchestidsresemble small fans@ig. 34) with broad basesand three to eleven spinulesor teeth.In orchestidfemales, these fan-like or radiate scalesmake up echinatefields on the propodus,ca{pus, and merusof the secondgnathopod, asinTalitroides. The first gnathopodis simpleGrg. lA). However,the male,slarge second gnathopodhas no radiate scales,which areinstead borne by propodaland carpal lobes on the first gnathopod(Fig. lC). As in the orchestids,the males of the aquaticHyaletla azteca andparhyale hawaiensis have small subchelate first gnathopodsand large subchelatesecond gnathopods. Females have four subchelategnathopods, all of which are basically similar to the male first gnetthopod.Whereas Talitroides, Orchestia, and Tethorchestiahave broad expansesof a single scaletype' presumed the grooming structuresof the aquaticspecies are much more concentratedand are of several types. Females carry these structureson both pairs of gnathopods;gnathopod I aloneis soarmed in themale.

3.2 Behavior

The talitroidean speciesdescribed above were also investigatedwith regard to grooming behavior (Holmquist 1981). Tatitroides alluaudi was later discussedin more detail by Holmquist (1985). The mouthpartsand first and secondgnathopods serve as grooming appendagesin all of thesetalitroidean species. Talitroides alluaudi and T.topitotumdemonstrate basically similar grooming behavior, althoughT'alluaudi has a somewhatlarger and more diverserepertoirJ of grooming acts. Most movements areipsi- andunilateral, although some are contra- or bilateral.Appendages areeither 'scrubbed' 'brushed' repeatedlyback and forth or in a proximal-to-distaldirection - a unidirectionalgrooming movement never occurs from the tip of an appendageto the proximal end' The secondgnathopod arches into a characteristicsickle-like configuration whengrooming (Fig juxtaposing 1B), thus theechinate fields (Fig. 28, C, D) on rhepropodus, carpus,and merus. Receptor appendages are drawn acrossthese processses. The long antennae are groomedby the first and/orsecond gnathopods. The gnathopod(s) typically move dorsally and anteriorly past the head and continueventrally, thus tracing a semicircle and brushing the entire antenna.Alternatively, the antennaeare sometimes loweredto the gnathopodsfor grooming. At times,the secondgnathopod will brusheither the reducedfirst antenna or the lateral headand eye in conjunctionwith an antennagrooming movement' The antennaeare also groomed by the maxillae; a first gnathopodgrurp, tn! antennalflagellum and pulls it to the mouthparts.The gnathopodand maxillipedal palps then hold the flagellumin placewhile it is chewedby rhem-axillae. Groomingstructure andfunction in someterrcstrial crustacea 99

Talitroidesalso expends a greatdeal of energygrooming pereiopods 3-7 and the uropods and does so with a variety of movements.These appendages are scrubbedor brushedby a singlefirst or secondgnathopod or by eitheror bothpairs of gnathopods.The animalflexes its body into a 'tI' shapein order to perform the majority of these acts, with the flexion increasingas the most posterior appendagesare groomed. A given appendageis often groomedby the mouth and gnathopodssimultaneously. For instance,the amphipodwill flex the body and grasp the proximal segmentsof the sixth pereiopod with both pairs of gnathopods,causing the distal segmentsto extend to the buccal mass. The then straightensthe body,causing the distal segmentsto be scrapedthrough the mouth and the proximal segmentsto be brushedbetween the two setsof gnathopods.This typeof movement often occursrepeatedly. Lessenergy is devotedto groominggeneral body surfacesthan to grooming appendages, particularlythe antennae,presumably because sensory structures are more heavily concen- tratedon the appendagesthan on the rest of the body.The non-appendagebody surfacesare scrubbedalmost exclusively by the two setsof gnathopods.The gnathopodsoften must work their way dorsally betweenthe coxal plates or epimera (two types of lateral shield-like processes)in order to reachmany of the lateralbody surfaces.The dorsal surfacesof these land hoppersremain virtually ungroomed.The body is flexed into a 'U' in order for the gnathopodsto reach the most posteriorareas. In T.alluaudi,but not T.topttotumor other investigatedtalitroideans, the two sixth pereiopodselevate and either alternately or synchro- nouslyscrub the anteriorabdomen. After every few acts,the gnathopodsare alsogroomed. Each gnathopodcan be scrubbed againstits opposite,and the first gnathopodscan be scrubbedby the second.Both pairs of gnathopodsare cleanedby the mouthparts;the maxillipedesare particularly active. Thus all material gleanedfrom the body is eventuallyhandled by the mouthparts.These clumps of materialare 1) worked away from the mandiblesand maxillae by the maxillipedesand first gnathopodsuntil the accumulationfalls away, 2) taken from the mouthpartsby the first gnathopodand stuck to nearbysubsffate, or 3) ingested.Grooming acts occur singly more oftenthan in combination,although up to threemovements can be performedsimultaneously (e.g.,a first gnathopodis cleanedby the mouthparts,while a secondgnathopod scrubs the fourth pereiopod and the sixth pereiopodsscrub the abdomen).In both T.alluaudi and T.topitotum,the secondgnathopods, equipped with scales(Figs. lB,2B., C, D), havea greater repertoireof groomingmovements than do the first gnathopods(Fig. 2A). BecauseTalitroi- desis neotenicand grooming structuresare distributed similarly in the male and the female, the groomingbehaviors of the two sexesare similar. In the sexuallydimorphic OrchesttaandTethorchestia (grade 3), eachsex demonstrates a groomingrepertoire that is distinctboth from thatof the othersex and fromthat of Talitroides. In the orchestids,the female's secondgnathopod, using the radiatescales @ig. 3.A) on the gnathopodallobes, performs the majority of gooming movements.The female's first gnathopod@ig. 1A) groomsas well, but doesso less frequently and has a smallerrepertoire of movementsthan does the second gnathopodof Orchestia and Tethorchesriaor the comparablefirst gnathopodof Talitroides. Orchestidmales, in contrast,perform all grooming actswith the first gnathopods(Fig. 1C),directing the fieldsof radiatescales @ig. 3,{) against appendagesand other body surfaces.The large secondgnathopod does not groom and is usuallymotionless, tucked closely beneath the body.The mouthpartsare used for cleaningin both sexes.Although the male's secondgnathopod does not groom, and the brunt of the male's groomingis doneby the first gnathopod,Orchestia andTethorchestia as male/female 'composites' demonstrategrooming repertoires quite similar to that of Talitroides. 100 JeffG.Holmquist

Femalesof the fresh-waterHyalella azteca and the marine Parhyale ha,vaiensisuse specializedscales and setae on boththe first andsecond gnathopods for grooming.The male's large secondgnathopod is not usedin grooming;the first gnathopods,armed with the same gtooming microstructuresseen in the female, perform all of the male's grooming move- ments. As in the semi-terrestrialspecies, grooming in these aquatic amphipodsclosely resemblesthat of the terrestrial Talitroides; the males simply do not perform second gnathopodmovements. The pellucid lobes, with their echinatefield of scales,are prominent featuresof the investigatedgrade 3 and 4 amphipods.Maclntyre (1954)and Duncan (1981) noted that the lobesare used to combthe ocistegitesand eggs, whereas Hurley (1959)hypothesized a 'tactile sensoryfunction.'Graf & Sellem(1970) have variously suggested that the fields of scalesare an adaptationfor grooming or feeding or, drawing from permeability experimentsby Graf & Magniez (1969),that they might have a physiologicalfunction such as respiration.Morino (1981) observedfemales scraping sand grains with the pellucid lobes and then holding the lobesup to broodedyoung, thus presumably transferring food. On the basisof the behavioral observationsin this study,it is hereheld that the echinatefields are grooming sffuctures.A dualfunction is, of course,quite possible. The selectiveadvantage of largemale secondgnathopods (used in at leastsome species for agonisticbehavior (Borowsky 1984))apparently outweighs that of a secondpair of grooming appendagesfor semi-terrestrialand aquatictalitroideans. An obviousparallel is the display chelipedeof male fiddler crabs,which cannotbe usedfor food gathering.Aside from the

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Figure4. Distalbuccalareaof Cubaris murina (ventralview). Note scalesof rightmaxilla andparagnathsand small disto-lateralsetae of left maxillule exopod.j-junction of paragnaths;lb-labrum; lmln-left maxillule endopod; lmlx-left maxillule exopod; lmp-left maxillipede; mn-mandibles;pl-maxillipedal palp; pr-paragnarh;rmlx-stout spinesand setaeof largely obscuredright maxillule exopod;rm2-right maxilla; x l4l. Groomingstructure andfunction in someterrestrial crustacea 101

grooming actionsof the male secondgnathopods, stemming directly from the neotenyof Talitroides,the behaviorof land hoppersdiffers little from that of their semi-terrestrialand aquaticrelatives. Behavioral solutions to aquaticepizoite growth may alsohave proven to be adequateresponses to the new fouling pressuresencountered as talitroideansinvaded the 'fine-tuning' wrack line and leaf litter. Morphological might then have resulted in the different grooming microstructureobserved in aquatic,semi-terrestrial, and terrestrialtali- troideans.

4 ISOPODA

4.7 Morphology

The groomingappendages of Porcellio laevis andCubaris murina were the mouthpartsand pereiopods,particularly the first pereiopod(see below). The mouthparts(Fig. 4) of the two speciesare quite similar. Of particular interest to this discussionare the setae of the maxillules'exopodsand scales(microtrichia) of the maxillaeandparagnaths. The exopodof the maxillule @ig. 4) bore a strong,disto-lateral spine and severalspine-like setae, which projected distally and mesially.The disto-lateralmargin of the exopod was iumed with smaller,distally directedsimple setae figs. 38, 4). The distalmaxillae and mesial paragnaths (Fig. 4) were thickly besetwith scales(Fig. 3C) that appearedto be quite similar to the scales describedby Wahrberg (192D and Nordenstam(1933), the aiguilles (needles)of Cals 'fine (1972),and the setae'of Hassall(1977). The scalesof P.laevisandC.murina demonstrat- ed the type of gradationdescribed by both Nordenstamand Cals, with proximal scales, consistingof severalacute projections from a commonbase, yielding distally to longer,single structureswithout distinct basalportions. Such scalesare presentin a variety of terrestrial flMahrberg,Hassall) and marine Q.{ordenstam, Cals) isopods. The ventral marginsof the pereiopodsGig. 3D) were armedwith the stout setae(trichia) trig. 3E) describedby Holdich (1984).These structures were presenton the merus,carpus, and propodusof each leg, excepting 1) the meri and carpi of the first, second,and third pereiopodsin the rnale@ig. 6,{) and 2) theproximal propodusof the first pereiopodin both sexesFigs. 3D, 6A). On the merusand carpusof the male,the stout setaewere replacedby otherswith finger-likeprojections (Fig. 6A, B). Such a configurationis frequentlyencoun- teredinoniscideanmales (Vandel 1925,1960, 1962,DeLuca 1965). By contrast,females had particularly stout setaeon the venftal merusand carpusof the first pereiopod(Fig. 3D). In both males and females,the proximal ventral propodusbore rows of small simple setae, which were directeddistally (Figs.3D, 6A, C). Both sexesof each specieshad an unusual organ on the anterior surface of the first pereiopod@ig. 6,4).The structurewas concave, beginning at theproximal third of the ca{pus andwidening as it continuedto its terminationat the disto-ventralborder. This carpalgroove was denselypacked with distally directedsetae @ig. 6D), the tips of which formed a slightly convergentpattern along the groove's midline @ig. 6'{). Thesesetae ranged from slender, simple forms to apically serratesetae with lateral setulesand gradedfrom one type to the otherwithin the groove. An examinationof the taxonomicliterature indicates that first pereiopodventral propodal organsof sometype arevery commonin the terrestrialIsopoda. The propodalstructures are often complementedwith carpal grooves, as describedhere and by Holdich (1984) for 102 JeffG.Holmquist

Porcellio scaber,or with adjacentorgans on the disto-venffalcarpus (Schultz 1984,Schultz & Johnson1984).

4.2 Behavior The grooming behaviorsof Porcellio laevis and Cubaris murina were remarkablysimilar. The following accountis applicableto both species;specific differences are noted. All of the mouthpartsand pereiopods functioned to varying degreesas groomingappend- ages.Although the mouthpartsdid not groomthe antennae,they did devotemuch attentionto the pereiopods.An appendagewas cleanedin one of two ways. In the first method, a leg movedtowards the antero-lateralbuccal mass. The pereiopodwas broughtinto contactwith the disto-lateralportions of the ipsilateralmouthparts (Fig. 4), which were rapidly opening and closing.The appendagewas pulled laterally and was thus scrapedagainst the maxilli- pedalpalp (Fig. 4), the mesially directedscales (Fig. 3C) of the maxilla and paragnath(Fig. 4), and setaeof the lateralmaxillule (Fig. 3B). This methodwas often usedto cleanthe first pereiopodprior to an antennarub. Alternatively,an appendagewas positionedmidventrally and was graspedby the maxillipedal palps trig. 4). Depending on the intensity of the movement,the leg was graspedonly by themaxillipedal palps and maxillae or additionallyby the greatlyextended exopods of the maxillule (the endopodswere possiblyused as well) or even the mandibles(Fig. a). At its most extreme,this act causedthe carpus,propodus, and dactylusto passbetween or acrossthe heavily sclerotizedmandibular processes, the stout distal spinesof the maxillule, the scalesof the paragnathsand maxillae,and the palps of the maxillipedes.The mouthpartseither simply graspedthe withdrawingpereiopod, thus scrap- ing it, or actively worked the appendagebetween them. Sometimesthe first and second pereiopodswere cleanedsimultaneously. Neighboring legs often held a pereiopodto the mouthpartsfor grooming (e.g., both sixth pereiopodsassisted the fifth). As an isopod 'U' groomedprogressively more posterior appendages, the body bentinto an ever-increasing shape.This bendingwas evenevident as the animal gtoomedthe secondpereiopod and was quitemarked during groomingof thehindmost pereiopods. The first throughsixth pereiopods were routinely cleaned.Only C.murinawas observedto groom the seventhpereiopod, and this species spent more time orally grooming posterior appendagesthan did P.laevis, presumablybecause of its conglobatingability.

Figure 5. Porcellio /aevlsgrooming antennaewith first pereiopod.Pereiopod I hasjust brushedproximal antennal scgmentswith ventralpropodus and rotated, bringing carpalgroove into contactwith distal segments. Figure 2. A. Simple first gnathopodof Talitroides alluaudi; c-carpus; d-dactylus; m-merus; p-propodus; x275.8. Echinate fields on the mittenlike secondgnathopodof T.allwudi;x275. C. Enlargement of propodal scalesin B; x 1,200. D. Scalesfrom second gnathopod of T.topitoturn:x 5,060. (From Holmquist 1982.) Figure 3. A. Scales from lnale Tetlnrchcstia n. sp. first gnathopod (note variation in form); x 3,550 (from Holmquist 1982). B. Setaefrom distolateral exopdof Cubaris murinamaxillule; xl,29O. C. Scalesfrom C.murina distal maxilla; x 1,290. D. Posterio-ventral view of female Porcellio laevis firstpereiopod, from propodus-68. (p) to ischium (i); note propodal grooming organ (arrow) and stout venral setae(s); c-carpus; ---"rus; x f,. Storrt setafrom carpus of above; x 380. Figure 6. A. Anterior surface of distal carpus (c) and proximal propodus (p) from male Cubaris mnrina first pereiopod; note seta-linedcarpal groove and ventral setaeof carpus and proximal propodus; x 160. B. Ventral setae from male C.rnwina first pereiopod; x 350. C. Ventral propodal grooming setaeof Porcellio laevis first pereiopod; x M5. D. Setaefrom carpal groove of P.laevisfirst pereiopod; note setules;x 2000. Figure 7. Coenobita clypeatus. A. Propodal shell-gripping scalesfrom fifth pereiopod; x 180. B. Thirdmaxillipede endopod (mesial view); setaeof dactylus and dense meral, carpal, and propodal band are D2 serrate setae, with exception of some apical simple setae; b-basis; c-carpus; cx-coxa; d-dactylus; iischium; m-merus; p-propodus; x-exopod; x 6. C. Third maxillipede endopod (lateral view); x 6. D. Dorsal grooming surfaces of fifth pereiopod, bearing simple, Dl serrate(D1), andplumodenticulate (pd) setae;x 6. '&Hffl $$al W[$IH

Figure 8. Coenobita clypeatw. A. Ventral grooming surfaces of fifth pereiopod, armed with simple, Dl serrate (Dl), and plumodenticulate (pd) setae, as well as shell-gripping scales (sg); c-carpus; d-dactylus; m-merus; p-propodus; x 6. B. Type D2 serrate setaefrom third maxillipede propodus; note marginal serrations and central scales; x735. C. Type Dl serrate seta from fifth pereiopod dactylus; note subapical pore (anow); x 1,215. D. Plumodenticulate setafrom fifth pereiopod propodus; x 355. l@ioj, !i(q)I(tl i. ++G.,

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Figure 9. A. Magnification of Fig. 8D Coenobita clypeatus plumodenticulate seta, showing cornblike setules and central groove; x 3460. B. Coenobita clypeatus scrubbing right antennule (horizontal arrow) with both third maxillipedes (vertical anow); x 2. C. Coenobita clypeatus brushing left antenna (white anow) with left third rnaxillipede (black arrow); x2.D.Inner surface of palp from Cailisoma guanhwni third maxillipede, with simple (ss), trisenate (t), pappose(pp), and cuspidate (cs) setae;c-carpus; d-dactylus; p-propodus; x 13. Figure 10. Cardisorna guanhwni. A. Outer surface of third maxillipedal palp, showing location of simple (ss), trisenate (t), and pappose (pp) seta€; c-carpus; d-dactylus; p-propodus; x 9. B. Mesial edge of third maxiilipede dactylus and propodus, demonstrating denseconcentration of setae;x 12. C. Cuspidate setaefrorn carpus of palp; x 130. D. Trisenate setaefrom propodus of palp; x235. Figure I 1. Cardisorna guanhwni. A. Distal portion of serrateseta, with stout recurved teeth, from epipod of second maxillipede; x320. B. Serratesetae, with many fine sehrles,also from epipod of secondmaxillipeie; this type fai tnC.guanhurni;x465. Tqe go.mmon C. Stout simple setae,on cheliped mirus, used to scrub branchiostegite; x 7. Dt Thirdmaxillipedes grooming eyestalks;crab's rightpalphas rounded eye's posterior and will continue ilesially, while left palp has progressedfrrther; black arrow indicates position of stouisetae for groorning branchiostegiie (white arrow); x0.8 (S. Sprun|. Groomingstructure andfunction in someterrestrial crustacea 103

The remaining grooming movementswere all performedby the pereiopods.By far the most commonof theseacts was the rubbing of an antennaby the ipsilateralfirst leg (Fig. 5). This pereiopodwas first cleanedby the mouthpartsas describedabove. Then the antenna moved posteriorlyand venfrally,where the propodusfigs. 3D 6A) of the first leg hooked over it at about mid-length. The propodus was then drawn laterally,scraping the dorsal surfaceof the antennawith its proximo-ventralsetae @g. 6C). As the pereiopodextended from the body, the pereiopodrotated, bringing the ventro-lateral surfaceof the antennainto contactwith the distally directedsetae of the carpalgroove Gigs. 5, 6A, D). This movement occurredrapidly and often repeatedly.At times, it was performedbilaterally and synchro- nously and occasionallywithout useof the carpalgroove. Rarely, the secondleg brushedthe antennain conjunctionwith the first leg. The antennaalso removed offending material via a seriesof quick slapsagainst the subsffateor by scrapingagainst a leaf or soil clod. The mouthpartswere groomedby the first pereiopods,which were positionedanteriorly and then drawn posteriorly.This movement was usually bilateral and synchronous,but occasionallyunilateral. The pereiopodsgroomed each other in a variety of ways.The secondleg crossedthe first andscrubbed the latter'sgrooming organs. At timesa pereiopodwas held directly away from the body and was scrubbedbetween its two neighbors,which had hookedpropodi over the intermediateappendage. The most commontype of leg groomingwas the mutual scrubbing of adjacentpereiopods, in which each simultaneouslygroomed and was groomed. The dactylus,propodus, and carpuswere not involved in thesemovements. Sometimes three appendages,particularly the second,third, andfourth pereiopods,scrubbed each other. All of theseacts were ipsilateralwith the exceptionof the mutual grooming of the two seventh pereiopods.At times,the first four pereiopodpairs engaged in mutual scrubswhile alsobeing cleanedby the mouthparts.Up to three of the anteriordactyli and propodi were inserted betweenthe mouthpartsfor grooming,while variousneighboring pereiopods scrubbed the carpi andmeri of the subjectappendages. As seenabove, the groomingbehaviors of P.laevisand C.murina werevirtually identical, as was that of a third grade 4 species,Porcellionides floria, which was somewhatless rigorously observed.Reports on semi-terrestrialand aquatic isopods indicate differing approachesto the fouling problem.The groomingof the mouthpafis,by the first pereiopods, of the grade3 Eurydicepulchra andE.ffinis (Jones1968) is the sameas rhar demonstrated by the grade4 isopods.However, unlike the woodlice,Eurydice uses a setosemaxillipedal palp to cleanthe inner mouthparts.The intertidal genusDynamene possesses a long mandibular palp, which groomsthe antennalflagellum (Holdich l97l). The mouthpartsof the examined terrestrialspecies did not groom the antennaeat all. The subtidalArcturella srnuoyaeuses its first pereiopodsto groom a varietyof surfaces,including the eyesand cephalon,and actually usesthe antennaefor grooming the dorsum and posteriorbody and pereiopods(Moreira 1973).Cubaris murina, Porcellio laevis, andPorcetlionides floria did not groom with the antennaeand did not groom the cephalonand eyes or, for that matter,any non-appendage areas.Although someof thesedifferences are striking, it may be that they areas much due to the tremendousrange of marineisopod body form as to differencesin fouling pressures. Basedon the woodlousegrooming behavior presented here, it is apparentthat the setaeof the first pereiopod'sproximal propodusGig. 64' C) and carpalgroove (Figs. 5, 64, D) are importantin grooming.Verhoeff (1908-09) and Wahrberg(1922) reached the sameconclu- sion concerningsimilar organs on a number of woodlice. Schultz (1984) and Schultz & Johnson(1984) attributeda grooming function to structureson the proximal propodal and 104 JeffG.Holmquist distal carpalmargins of variousterrestrial isopods. The presentwork demonsffatesthat the maxillipedalpalps, scales of the maxillaeand paragnaths, lateral setae of the maxillules,and sclerotizedbiting surfacesof themaxillules and mandibles are important grooming structures as well. The stout setae(trichia) of all sevenpereiopod pairs (Fig. 3E) also have a role in grooming adjacentlegs (Holdich 1984). Although the location of denseventral standsof carpal and meral setaeSig. 6A, B) on the first three pereiopodsin the male suggestsa 'drum' groomingfunction, these organs didnotperform this activity.Male sowbugstypically or brush the anterior pereiopodsagainst a female's dorsum during courtship behavior (Legrand1958, Patanb 1959, Mead 1964,1965,1961,Sutton 1980). It seemsprobable that the ventralsetal organs abet this behavior. Schmalfuss(1977,1978) has suggestedthat the tergal plaques(or microscales)of terresffialisopods function primarily as passiveanti-fouling devices,preventing the adher- enceof small wet particles.However, Powell & Haicrow (1982)observed that theseplaques arenot necessarilyterresffial adaptations and that their functionis still unclear.

5 ANOMURA

5.I Morphology As will be seen beloW Coenobita clypeatusused the mouthparts(particularly the third maxillipedes)and the first, second,third, and fifth pereiopodsas grooming organs.The stubby,reduced fourth legs,with largerfields of shell-grippingscales @ig. 7A) than the fifth legs,did not appearto function in grooming.Although the chelipedesand secondand third pereiopodswere secondarygrooming appendages,they did not possessmodified sffuctures for theprocess. The walking legswere instead provided with the stout,simple setae described fromC.perlatus by Hamilton(1 983). The primary grooming appendageswere the third maxillipedes@ig. 78, C) and fifth pereiopods(Figs. 7D, 8A). The merus,carpus, propodus, and dactylusof the third maxilli- pedal endopod @ig. 78, C) were the only mouthpart segmentsthat contactednon-oral appendages.These segmentswere heavily besetwith Type D2 serratesetae (Fig. 88) of Factor's(1978) classification scheme, which is followedhere. These setae also appeared to be identicalto thosefigured by Bauer(1975). Smaller numbers of TypeI simplesetae were also present. The distal tip of the roundeddactylus was armedprimarily with simplesetae (Fig. 78, C). The remainderwas denselycovered with serratesetae, although the externalface was more sparselysetose (Fig. 7C). With this exceptionof the dactylus,the externalendopod face was virtually nude fig.7C). Mesially,a bandof setaeran from the proximal third of the merusto the distal propodus(Fig. 7B). This band was largely composedof serratesetae, with some simplesetae interspersed. There was some gtadation in form of the D2 serratesetae; some had an increasednumber of medianscales, whereas others approached the C3 modified plumo- denticulatesetae of the exopods.A11 of thesesetae were closely appliedto the maxillipede surfaceand were directeddistally (Frg.7B). The setaearising from the propoduswere larger than thoseof the dactylus,with setaeof the carpusand distal meruslarger still. As Roberts (1968)observed for Paguruslongicarpus andP.pollicaris, the long serratesetae of the carpus overlappedthose of the propodus.Setae of the distal merus,in turn, overlappedthose of the carpus.The meralsetae became progressively smaller and fewer in numberproximally. Very Groomingstructure andfunction in someterrestrial crustacea 105 sparseserrate setae occuned adjacentto the setalband. The secondmaxillipedes were also armedwith serratesetae accompanied by scatteredsimple setae. The setal complement of the fifth pereiopodswas quite different from that of the maxillipedes. Type D1 serrate setae (Fig. 8C) were common and demonstratedsome variation at the tips. Also presentwas an unusual setal type (Figs. 8D, 9A) that closely resembledThomas's (1970) setobranchsetae, although there was no mid-shaft articulation. Theyperhaps integrate best with Factor's(1978) scheme as C5 plumodenticulatesetae, a type addedto Factor'sframework by Schembri(1982a, b). As with Factor'sC3 plumodenticulate setae,there were no proximal setules,and the tip of the shaftwas sickle-shapedas Schembri described.Type I simplesetae were alsopresent. Most of the posteriorsurface of the dactyluswas armedwith shell-gnppingscales (Figs. 7A, 8A). Ventrally and anteriorly,the dactyluswas coveredwith serratesetae and scattered simple setae.The posterior surfaceof the propoduswas also coveredwith shell-gripping scales.Otherwise, with the exception of a small mesial band of bare exoskeleton,the propodus was thickly beset with setae.Distally, these setaewere primarily senate, but plumodenticulatesetae were more commonproximally and becamethe dominanttype near the carpalmargin. The lateralcarpus was bareexcept for a seriesof plumodenticulatesetae borderingthe propodus.A denseclump of long plumodenticulatesetae was found on the distal venfto-mesialangle, with a somewhatsmaller clump distally and dorsally.Similar, progressivelysmaller setal clumps occurred proximal to thesegroupings, with an occasional simple setapresent. The lateral surfaceof the long meruswas devoid of setae,which were present,though relatively sparse, on thedorsal, ventral, and mesial surfaces. These setae were primarily plumodenticulatedistally, but serratesetae became more commonproximally.

5.2 Behavior The third maxillipedesand fifth pereiopodsperformed the majority of movements,including all of the more complex actions, and were suprisingly dexterous.Coenobita clypeatus devotedmost of its groomingenergy to the eyesand antennulesand did so with the mesial surfacesof the dactylus, propodus, ca{pus, and distal merus of the third maxillipedal endopods(Fig. 7B). An eyestalkwas groomedby one (ipsilateral)or both maxillipedes.The eyestalkdipped ventrally and was met by a third maxillipede,which hookedits dactylusover theproximal portion andapplied the serratesetae of themesial propodus and dactylus against the eyestalk.(The antennaehad meanwhile swung laterally to allow access.)The maxillipede was pulled ventrally,brushing the eyestalk'sfull length.If both maxillipedeswere used,the two dactyli werepositioned together at the baseof the eyestalksand were drawn ventrally in unison.The antennulesmay alsobe groomedby either(ipsilateral) or both maxillipedes.The 'V', antennuleswere bent upward forming an inverted while the maxillipedewas raisedto meetthe proximal part of the appendage.The maxillipedewas then pulled venffally,brushing the antennulewith its serratesetae and pulling it ventrally as well. When both maxillipedes groomed an antennule,they at times continuedto gasp the flagellum at the end of the movement.The maxillipedesthen scrubbedthe flagellumbetween them @ig. 9B), working alternatelyup and down aswould a pair of pistons.Eye andantennule grooming movements were often combined,with the maxillipede(s)first brushing the eyestalk,then continuing ventrally to the antennule.The antennalpeduncle and proximal flagellum were brushedby the ipsilateralthird maxillipede@ig. 9C). The third maxillipedesalso groomedthe mesial anddorsolateral surfaces of the chelipedemeri andthe venffal surfaceof the cephalothorax. 106 JeffG.Holmquist

The threepairs of walking legs (chelipedesincluded) groornedthemselves by scrubbing againsteach other in variouscombinations of two or threeappendages. The dactyli,propodi, and carpi were most important in thesemovements. In addition, the fingers of the minor chelipedepicked at the surfaceof the major chelipede. The chelate fifth pereiopods were quite flexible and extended as far forward as the chelipedes.Most groomingwas performedwith the plumodenticulateGig. 8D) and serrate ffig. 8C) setaeof the carpus,propodus, and dactylus (Figs. 7D, 8A), and virtually all 'scrubs'. movementswere The fingersusually openedand closedslightly when grooming; similar actionhas been described from the fifth pereiopodsof a porcellanidcrab (Bauer,this volume) and the secondpereiopods of hippolytid shrimp(Bauer 1975).Coenobita clypeatus often extendedslightly from its gastropodshell during fifth pereiopodalgrooming, with the anteriorabdomen thus becoming visible. The fifth pereiopodsscrubbed the basalsegments of the chelipedesand all of the secondand thirdpereiopods with theexception of thedactyli. All of pereiopod4 was scrubbed.The fifth pereiopodsalso groomedmost of the central and posteriorcarapace, including the branchialchamber, and much of the abdomen.Interestingly, the shellwas alsothoroughly scrubbed, perhaps in an effort to rid therefuge of thegreen algae describedby Magnus (1960) and Ball (1972). The fifth pereiopodsgroomed much of the shell'sinterior, particularly the columellaand inner andouter lips, aswell asthe exteriorlips. Theseappendages did not function exclusivelyas grooming organs,as they also use their laterallysituated gripping scales(Fig. 7A) to bracethe body againstthe shell (Johnson7965, Vuillemin1970). After everyfew groomingacts, the fifth pereiopodsmoved anteriorly, in unison,to meetthe two third maxillipedes,which were extendedposteriorly beneath the body.The plumodenti- culateand serratesetae of the posteriorappendages were then scrubbedby the maxillipedes. The third rnaxillipedes,in turn, were scrubbedagainst each other and/oragainst the second maxillipedesafter a groomingbout. The interior mouthpartshad a self-cleaningfunction as well. Thus, the maxillipedesgroomed the anteriorportion of the body (especiallythe sensory structures),the walking legsgroomed each other, and the fifth pereiopodsscrubbed the most posteriorareas (Table 1). Two movementswere, at times, performed simultaneously,e.g., mutualleg scrubsand antennule gtooming. Although groomingmay occurat any time, it was mostfrequent and intense immediately after a rain andwas oftenperformed in standingwater if it was available.Water is clearly an important debris-flushingmedium in Sesarmaand Cyclograpsas(Alexander & Ewer 1969),Uca (Crane7975), and Cardisoma (see below). The unusualplumodenticulate setae (Fig. 8D) of the fifth pereiopodswere clearly usedto scrub the body surfaces.The Dl serratesetae of the fifth pereiopod(Fig. 8C) and the D2 serrate setae (Fig. 88) of the maxillipedes were also observed to effect grooming in

Table l. Division of labor between grooming appendagesof Coenobita clypeatus.Groomed structuresare, in order, the eyestalks,antennules, antennae, third maxillipedes,cephalothorax, pereiopods (1-5), abdomen,and shell.

Grooming appendages Groomed structures Eys Anl kA Mx3 Cth Pel PeZ Pe3 Pe4 Pe5 Abd shl Mx3 +++++ ++ Pel ++ Pe2 ++

Pc3 f Pc5 ++++ Groomingstructure andfunctionin someterrestrial crustacea 107

C.clypeatus,as do similar selratesetae in Pagurus (Roberts1968, Schembri 1982a).The maxillipedal serratesetae of a variety of marine hermits have been implicated in feeding behavior@oberts 1968,Greenwood 1972, Kunze & Anderson 1979,Schembri 1982a); the D2 setaeof C.clypeatuswere also used for this purpose.The groomingsetae, particularly the serratesetae, may alsoserve in a sensorycapacity (Derby 1982). Although the aesthetascsof Coenobita are strikingly shorter than those of its marine counterparts(Ghiradella et al. 1968a,1968b), the terrestrialhermit's maxillipedalsetae were easilyas long (in termsof setallength/mouthpart length) as those found in salt-waterspecies. Serratesetae on the distal merus of the third maxillipede, for instance,extended to the proximal third of the propodus(Fig. 7B). However,whereas the maxillipedalsetae of marine hermitstypically projectorally and away from the flexor margin (Roberts1968, Greenwood 1972,Caine 1975,Kunze & Anderson 1979,Schembri 1982a),those of C.clypeatuswere very closely applied to the mouthpart surfaces.Also, the setaeof the secondand third maxillipedefingers of C.clypeatuswerealmost entirely D2 serratesetae, with a few scattered simple setae,instead of the wide variety of types found in marine pagurids (Kunze & Anderson1979, Schembri 1982a). Both the acuteangle of setalinsertion and the homogene- ity of setaltypes are probably adaptations to terrestrialfeeding limitations rather than fouling pressures.Mostaquatichermitcrabsmakeuseof anumberof feedingtechniques (Boltt 1961, Roberts 1968,Greenwood 1972, Caine 1975,Kunze & Anderson 1979,Schembri 1982a). However,in the absenceof a buoyantmedium, filter feedingis impossible,and approachesto otherprocesses, such as detrital feeding, may berestricted. With a reducedfeeding repertoire, fewer setaltypes might be needed,and setalarrangements would emphasizegrasping rather than straining functions. Setaeprojecting away from the appendagewould serve little purposeand would be exposedto breakageand dehydration.An alternativemay be the arrangementfound in C.c ly p eatu s . The grooming behaviorof C.clypeatu.swas similar in generaland in most detailsto that describedfrom a number of marinehermit crabs(Makarov 1962,Vuillemin 7961,Roberts 1968, Snow 1973, Field 7977, Bauer 1981, Schembri 1982a).However, some minor differencesare apparent.Unlike the land hermit, Pagurus rubricatus grooms the secondand third pereiopodswith the third maxillipedes(Schembri 1982a).Field (1977) demonsrrared that tlre third maxillipedesof P.ochotensisgroom the antennulesabout 20 times as often as theydo theeyes. In conffast,C.clypeat rs groomedthe eyesat leastas often asthe antennules. Indeed,the majority of eyeand antennule grooming movements were performed in combina- tion. It may be that the increasedrole of visual cuesin terrestrialdecapod social communica- tion (Wright 1966,Ache 7982,Salmon & Hyatt 1983)requires, in turn, increasedmainre- nanceofthe eyes.

6 BRACHYURA

6.1 Morphology

In Cardisomaguanhumi, the palps of the third maxillipede(Figs. 9D, 10A) were the most commonlyused grooming structures and,like thoseof ocypodids(Koepcke & Koepcke1953, Crane 1975) and grapsids(Alexander & Ewer 1969,Felgenhauer & Abele 1983), were denselysetose (Fig. 10B). Four basic types of setaewere apparent,and, as in the previous discussion,Factor's (1978) setalclassification will be followed. The dactylusand propodus bore groupsof long, Type I simple setae(Fig. 10B). Also present,primarily on the carpus, 108 IeffG.Holmquist were H1 cuspidatesetae (Fig. 10C).Type 82 papposesetae covered much of the palp and were interestingin that they were plumosebasally, but were papposealong the remainderof the shaft. This configurationis identical to that of the papposesetae figured by Thomas (1970).TypeEtriserrate(Fig.10D)setaewerealsoinsertedovermuchofthepalpsandwere very similar to otherType E triserratesetae illustrated by Schembri(1982a). There was some variationof this type,with somesetae resembling Type C3 plumodenticulatesetae basally but becoming triserratedistally. On the tip of the dactyluswas a concenffationof long simplesetae (Figs. 9D, 10A, B). The inner surfaceof the dactyluswas almostentirely coveredwith triserratesetae, except for the lateraledge, which was virtually devoid of setae.Conversely, only the mesial edge of the outer dactylar surface bore setae- a thin margin of triserrateand papposetypes. The disto-lateraledge of the propoduswas fringed with long simple setae,whereas the mesial edgewas armedwith a densesetal brush, predominantly triserrate distally, but increasingly papposeproximally. The carpuswas fringed with densepappose setae extending from near the baseof the lateraledge, to the inner andouter faces of the propodalmargin, and around to the midpoint of the mesialedge. Cuspidate setae were present among the pappose setae of the inner distal fringe and alsoformed a seriesrunning the lengthof the inner carpus. As with other brachyurans(Bonadaile 1922,Vuillemin 7967,Wamer 1977,Bauer 1981, this volume), the setosemaxillipedal epipodsof C.guanhumiextended well into the gill chamber,with thefirst epipodabove and the secondand third epipodsbelow the gills. Curious Type D1 serratesetae, similar to thosedescribed by Walker (1974)and Bauer (this volume), with stout, recurvedteeth and finely taperingtips ffig. 11A), were present.The setaeof C.guanhumihad two rows of teeth versusa single row in the portunid Cronius tumidulus (Bauer,this volume). However,other Type D1 serratesetae @ig. 11B) predominatedon the epipodsof C.guanhumi.Thesesetae had many smallerapically directed teeth that continued to the tip of the shaft.A few scatteredsetules were often presentat the baseof the serrated portion.About 10 to 15 of thesesetae occurred for eachof the former type. Although the four pairs of walking legs were usedfor grooming,they did not appearto possessspecialized grooming structures.Neither do the distal chelipedesegments bear the tuberculateridges of Sesarmacatenata and Cyclograpsuspunctatus (Alexander & Ewer 1969)or the serrationsand setaeof many fiddlers (Crane 1975) usedfor gtooming in these lattercrabs. However, the chelipedemerus and ischium bore a row of stout,simple setae Gig. 11C).The majority of thesesetae arose from themerus, which was concave(excepting on the adultmale major chelipede),thus fitting againstthe convexbranchiostegal region ffig. 11D). The major chelipedemerus of the mature male was long and straight, and setaewere restrictedto the ischium and proximal merus.The inner chelipedesurfaces of a number of Sesarmaspecies are armed with serrate,instead of simple, setae(Milne Edwards 1873, Felgenhauer& Abele 1983).

6.2 Behavior Cardisomaguanhumi used all five pairsof pereiopodsand the mouthparts (primarily the third maxillipedes)to groom its body.The most frequentlyperformed movement was the groom- ing of the eyestalk and interorbital area by the third maxillipedes (Fig. l lD). Prior to grooming, the eyestalkwas deflectedvennally, sometimesinto its orbit. The maxillipedal palp extendeddorsally, the entire maxillipedeswung laterally,and the palp reachedaround the eye, first contactingit posteriorly.The maxillipedethen recoiled,working the triserrate Groomingstructure andfunction in someterrestrial crustacea 109

setaeof the propodusand dactylus@ig. 10B, D) aroundthe eye, down the eyestalk,and acrossthe interorbitalarea, usually including the antennae.The cuspidatesetae of the carpus were sometimesbrushed over the orbit lip and epistome.As Crane (1975) observedfor fiddlers,the act moved from distal to proximal - uncommonfor a unidirectionalgrooming act. The palps, at times, scrubbedthe interorbitalarea without grooming the eyestalks.The third maxillipedes, together with the secondmaxillipedes, also cleaned the tips of the chelipedefingers. After a seriesof grooming acts, the third maxillipedal palps scrubbed againsteach other and againstthe secondmaxillipedes. Debris was droppedto the substrate, ingested,or picked away by a chelipede.The epipodsof the maxillipedesswept the gill surfacesas a direct result of endopodalmovements and/or their own musculature,thus draggingthe epipodalsetae Gig. 11A, B) acrossthe gills. Such epipodalgrooming is a common brachyuranfeature (Bonadaile 1922,Hiatt 1948,Vuillemin 1967,Walker 1914, Warner1977, Bauer 1981, this volume). The densestands of triserratesetae Figs. 9D, 108), with their comb-likeserrations, were clearly the dominant grooming setaeof the maxillipedal palp, although they also helped support large morsels during feeding (pers. obs.) and could function as chemo- and/or mechanoreceptors,as Derby (1982)found for someserrate setae. The cuspidatesetae served in grooming,as well. The role of the papposesetae is somewhatmore problematical.Some papposesetae, particularly those of the lateral edgesof the proximal propodusand distal ca4)us,did come in contactwith the antennaeand interorbitalarea during grooming, and Farmer (1974) has suggestedthat pappose setae function in the cleaning of adjacent mouthpartsffuctures. Nevertheless, pappose setae seem rather delicate and fragile in compa- rison to the typically robust and strongly serrategrooming setaeof decapodcrustaceans (Roberts 1968, Thomas 1910, Bauer 1915, 1977, 1981, Hindley & Alexander 1978, Schembri1981, 1982a, b). Alternatively,Thomas (1970) has hypothesized a supporringrole in food collectionand transfer, and Schembri has proposed a mechanicalfunction, as screens, gaskets,etc. (1981) or a sensory(1982b) role for papposeserae. The chelipedeswere also often used to groom the eyestalks,which was somewhat surprisingin view of thedisparity of sizeand strength of thetwo structures.The chelipede(s) delicatelygrasped the eyestalknear the baseand brushedalong its surface.An eyestalkwas groomed by the ipsilateral or contralateralchelipede or both chelipedesin unison. A chelipededactylus also often scrubbedthe orbit. The branchiostegitewas groomedby three different methods. 1) The concavechelipede merus and ischium circularly scrubbedthe convexbranchiostegite, and occasionallythe lateralcarapace, with the stout simple setaeof the inner surfacesGig. 1lC) combing the branchiostegitesetae. 2) With fingers somewhat separated,the contralateralchelipede tips (sometimesjust thedactylus) brushed the branchio- stegitefrom ventrolateralto dorsomedial.As the fingersneared the buccal area,they were apposedand were cleanedby the maxillipedes.3) The contralateralchelipede picked at clumps of debris fouling the branchiostegalsetae. This picking sometimesextended to the thoracic stema and abdomen.A chelipedegroomed its oppositeeither by picking at the other'ssurface with thefinger tips or by scrubbingthe outer propodus and dactylus against the inner propodusof the other claw. Material gatheredfrom the body was either transferredto the maxillipedesor wiped againstthe substrate. Mutual scrubbing of the pereiopods(including the chelipedes)was a rather common occurrenceand was accomplishedin threeways. 1) The posteriorsurface of an appendage and the anterior surfaceof the following leg were scrubbedtogether. 2) Two pereiopods crossedover eachother, with the forwardpereiopod's anterior surface thus scrubbing against 110 JeffG.Holmquist the posteriorof the following appendage.3) Two appendages(e.g., the secondand fourth pereiopods)met over the depressedintervening appendage,with the posterior of the leading leg and the forward edge of the posteriorleg performing a mutual scrub.At times, all ten pereiopodswere involved in mutual scrubssimultaneously, although the chelipedesdid not performthe lattertwo typesof movements.The secondpereiopodsometimes usedits narrow lateraledge or dactylustip againstthe chelipede. As in Coenobita clypeatus,grooming in Cardisomaguanhumi was most frequent and intensefollowing rain or when the animal was in standingwater. If the water was deep enough,the anteriorcarapace submerged by tilting forward, and the eyestalkswere washed by repeateddips into the water-filledorbits. Foambathing, in which bubblesproduced by the mouthpartsdisperse fluid aboutthe body, occurredin partially submergedor emergentcrabs. This actionhas been variously interpreted as a method of thermoregulation(Altevogt 1968),pheromone distribution (Wright 1966), waterreserve aeration (Lindberg 1980,Jacoby 1981), or cleansing(Schone & Schone1963, Brownscombe1965, Lindberg 1980, Jacoby 1981). Grooming behavior has also been recordedfrom a number of other amphibiouscrabs. Pearse(1912), investigatingUca (grades l+ to 3), notedthat the walking legs and chelaeare grooming appendagesand emphasizedattention to the eyestalks.Crane (1975) statedthat submersionis themajor cleansingmethod in fiddler crabs.She also recorded the groomingof theeyestalks by 1) depressioninto wet sockets,2) graspingwith the chelae,or 3) brushingby the third maxillipedal palp. The chelae groom each other, and the first through fifth pereiopodsengage in mutual scrubs.She found no obvious interspecificdifferences. The eyestalksof Ocypode(grade 3) are groomedby the palps of the third maxillipede and by setae lining the orbits (Koepcke& Koepcke 1953,Vannini 1980). The minor chelipedeis cleaned by the maxillipedesand the major by the adjacenttwo walking legs (Vannini 1980),and the mouthpartsscrub each other (Koepcke & Koepcke1953). The soldier crab, Mictyris longicarpu.s(Mictyridae) (grade 2), performs what must certainlybe the mostacrobatic grooming movement recorded from the Brachyura.According to Cameron(1966), the crab,following emergence,falls on its back,thus removing accumu- 'half lated sand,and then flips upright again.This somersault'is executedin less than a second.Mictyris alsogrooms the eyestalksand mouthparts with the chelae. Cott (1929), investigatingSesarma meinerti (grade 3), describedthe grooming of the branchiostegalregion by serratesetae on the concave surface of the chelipede merus. Sesarmabidentatum (3) and S.verleyi(3) also use serratesetae on the concavemerus to groomthe branchiostegite, while S.reticulatum,S.rubinofforum,S.rectum,S.aequatoriale(all grade3), and S.jarvisi(4+) usein additionsetae on the carpus(Felgenhauer & Abele 1983). The latterauthors also recorded the groomingof the epistomalregion of S.reticulatumbythe setaeon the third maxillipedalpalp. Alexander& Ewer (1969) also emphasizedthe use of stoutmeral setaein branchiostegalgrooming in S.catenata(3) andCyclograpsus punctatus (3). The mouthparts,eyes, and antennaeare groomed by setaeon the palp of the third maxillipede. The chelae pick at the mouthparts,the branchiostegite,the sterna,and the pereiopodsand scrub the eyes, antennae,and mouthpartswith tuberculateridges on the propodi. The walking legs engagein mutual scrubswith the chelaeand each other.These grapsids,like fiddler crabs, also clean themselvesby submersion.Lindberg (1980) and Jacoby(1981) described action pattems from Hemigrapsusoregonensts (2) andH.nudu.s (2), respectively.They reportvirtually identicalbehavior: the chelipedesrub or pick at the buccal area,thoracic sterna, abdomen, and opposingchelipede; the legs scrubeach other,and the Groomingstructure andfunction in someterrestrial crustacea 111 third maxillipedalpalp cleansthe eyestalk.Jacoby called attentionto the closeresemblance betweenaquatic and amphibious brachyuran grooming behavior. Wright (1966)recorded grooming from a varietyof grade4 (Gecarcinusquadrarus), grade 3 (Cardisoma cressum, (Jcidesoccidentalis, Grapsus grapsus, Goniopsispulchra), and grade2 (Pachygrapsuscrassipes, P.transversus, Sesarma sulcatum, Hemigrapsus oregonen- sis,H.nudu.r, and Goetice americanus)crabs of the families Gecarcinidaeand Grapsidae. Like Jacoby(1981), Wright sffessedthe similarity of groomingin thesespecies, stating that 'all cleaningpattems seen in one speciesalso are seenin the others.'The chelaescrub each other,the mouthparts,the sterna,the abdomen,and the eggs of femalesin berry.The eyestalks aregroomed by the typical movementsof the third maxillipedalpalps, while the walking legs scrub each other, the chelae, and sometimesthe ventral body. Wright emphasizedthe secondaryrole of grooming as a displacementactivity (intense,incomplete, and nonfunc- tional behaviorevoked by the thwartingof oneor more drives)in thesespecies, as did Crane (1957, 1975) for ocypodids. There does,indeed, seem to be remarkablesimilarity of grooming behaviornoted in the above reports. Grooming of the eyestalksby the third maxillipedal palp is obviously a prevalentmovement, as is scrubbingof thebranchiostegite by the chelipedemerus, gtooming of the mouthpartsand oppositechelipede by the chelipedefingers, and mutual pereiopod scrubbing.Based on the availableinformation, there is no indicationof markeddifferences in brachyurangrooming behavior as a responseto varyingdegrees of tenestriality.

ACKNOWLEDGMENTS

I am grateful to R.Bauer,B.Felgenhauer, H.Powell, and an anonymousreviewer for their instructivecomments on the paperand to R.Baerwald,M.Coffroth, D.Holmquist,M.Reeve, and M.Syms for generouslyproviding laboratoryfacilities and other assistance.G.Schultz kindly identifiedrepresentative isopods, and M.Goreau and PMartin assistedwith the SEM. Specialthanks also to K.Haingefor typing the manuscript.

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