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 crustaceans,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: Amphipoda, Isopoda, 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 '\) 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 Orchestia 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, Porcellio 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 (Talitridae: 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