Spermatophore Diversity Within and Among the Hermit Crab Families, Coenobitidae, Diogenidae, and Paguridae (Paguroidea, Anomura, Decapoda)

10 Pages·1991·4 MB·English

by  C C Tudge

Reference: Biol Hull 181: 238-247. (October. 1991)
Spermatophore Diversity Within and Among the
Hermit Crab and
Families, Coenobitidae, Diogenidae,
Paguridae (Paguroidea, Anomura, Decapoda)
TUDGE
C. C.
Zoology Department, University ofQueensland, Queensland, 4072. Australia
Abstract. The spermatophore morphology of 13 species have been investigated for spermatophore morphology.
ofhermitcrabfrom thefamiliesCoenobitidae, Diogenidae These are listed below. Coenobitidae: Birgus latro (Lin-
and Paguridae is described and illustrated, and compar- naeus), Matthews, 1956; Tudge and Jamieson, 1991.
isons are made with existing descriptions to show that Coenohita rugosus H. Milne Edwards, Matthews, 1956.
spermatophore form, at the light microscope level, can Diogenidae: Clibanariusmisanthropus(R\sso), Mouchet,
beusedtoseparate three familiesofthePaguroidea. Sper- 1930, 1931. Dardanus arrosor (Herbst), Mouchet, 1931
matophores from members of the family Coenobitidae (as Pagurus arrosor). Dardanus asper (De Haan), Mat-
are robust in nature with large, ovoid-spherical ampullae thews, 1953. Dardanus punctulatus (Olivier), Matthews,
mounted on short, thick stalks. Members ofthe family 1956. Diogenespugilator(Roux), Mouchet, 1930, 1931.
Diogenidae have more fragile spermatophores with small Pagnrislesoculatiis(Fabricius), Mouchet, 1931. Aniculus
spherical ampullae mounted on long, slender stalks. The inaxiiniis Edmondson, Triiopagurus maxinuis (Herbst)
spermatophores ofmembers ofthe family Paguridae are and T. slrigatits (Herbst), Matthews, 1957 (as Aniculus
distinctive in possessing large, elongate, ampullae, an ac- strigalnx). Paguridae: Anapagurus hyndmanni (Thomp-
cessory ampulla at the base ofthe main ampulla and a son), Mouchet, 1930, 1931. Anapagurus brevicarpus A.
pseudo-stalk analogous with the true stalk of the Coe- Milne Edwardsand BouvierandA /cms(Bell), Mouchet,
nobitidae and Diogenidae. The occurrence of double- 1931. Cestopagurus timidus(Roux), Pagurusanachorelus
headed spermatophores (two ampullae on a single stalk) Risso, P. cuanensis (Thompson), P. excavatus (Herbst)
is recorded for the first time, in a Dardanus species. The and P. sculptimanus (Lucas), Mouchet, 1931 (all as Eu-
ultrastructure ofthe lateral ridge, which divides the am- pagurus). Pagurus prideaux Leach, Mouchet, 1931; Ha-
pulla ofthe paguroidean spermatophore into two halves, mon, 1937 (both asEupagurusprideauxi). Pagurusbern-
isdescribed usingbothscanningandtransmission electron hardus (Linnaeus), Mouchet, 1931; Chevaillier, 1970
microscopy. A simple, branching key for classifying the (both asEupagurusbernhardus). Pagurusnovizealandiae
investigated hermit crabs(from the familiesCoenobitidae, (Dana), Greenwood, 1972 (as P. novae-:ealandiae). Pa-
Diogenidae and Paguridae only) into their respective gurus excavatus (Herbst), Schaller, 1979 (as P. meticu-
family, based on thegross morphology oftheirspermato- /osus). All of these previous studies of spermatophore
phore, is presented. structure have been at the light microscope level.
Except for Triiopagurus maximus and T. strigatus
Introduction (Matthews 1957),the hermitcrabspreviouslystudied have
atypically pedunculatespermatophorethatcanbedivided
The infraorder Anomura consists of 13 families of into three major regions: a sperm-filled ampulla, acolum-
which only 6 have been investigated for spermatophore nar stalk of variable length, and a foot or pedestal. The
morphology. Representatives ofthree hermitcrab families ampulla hasapartition orlineofdivisionthatrunsaround
in the superfamily Paguroidea (sensit McLaughlin, 1983) the lateral edge and separatesthe ampulla intotwo halves.
Thissuturelineisthepointofweaknesswheretheampulla
Received 12 April 1991;accepted 17 July 1991. breaks to release the spermatozoa prior to fertilization.
238
HERMIT CRAB SPERMATOPHORE DIVERSITY 239
Earlier pioneers in hermit crab spermatophore mor- The malereproductive system wasdissected from fresh
phology include Mouchet (1930, 1931) and Matthews specimens, 10% buffered formalin-fixed or 3% glutaral-
1953, 1956, 1957), whose important contributions to this dehyde-fixed specimens. The spermatophores were teased
(
fieldalsocoveredotherdecapods. Thesereferences, along out ofthe distal part ofthe vasdeferens onto microscope
with many other paperson decapod spermatophores, are slides. Spermatophores were viewed and photographed
adequatelytabulatedin Dudenhausen andTalbot(1983). with an Olympus BH2 microscope equipped with No-
Some additional, more recent, references to anomuran marski interference contrast optics. After the initial glu-
and brachyuran spermatophore studies can be found in taraldehyde fixation and first phosphate buffer wash, the
Mann's (1984) book on spermatophores. Studies on her- fixation procedure for transmission electron microscopy
mitcrabspermatophores havebeen neglected forthepast wascarriedoutinaLynx-el. MicroscopyTissue Processor.
10 years, except for a recent review by Hinsch (1991); Portions oftMhe vas deferens were fixed in 3% glutaralde-
although some important works on brachyuran (Jeyalec- hyde in 0.2 phosphate buffer (pH 7.2) for 1 h at 4C.
tumieand Subramoniam, 1989;Subramoniam, 1991)and They were washed in phosphate buffer (3 washes in 15
caridean shrimp(Chow eta/.. 1989) spermatophores have min), postfixed in phosphatebuffered 1% osmium tetrox-
been published. Comparisons of the functional mor- ide for 80 min; similarly washedin bufferand dehydrated
phology ofgenitalia and subsequent sperm transfer and through ascending concentrations ofethanol (40-100%).
storage mechanisms among taxa can provide useful in- After being infiltrated and embedded in Spurr's epoxy
formation on phylogenetic relationships and evolutionary resin (Spurr, 1969), thin sections (50-80 nm thick) were
divergence; especially in the Decapoda (Bauer, 1986, cut on a LKB 2128 UM IV microtome with a diamond
1991). The present paper describes and illustrates the knife. Sections were placed on carbon-stabilized colloidin-
spermatophorestructureof13speciesofhermitcrab, from coated 200 ^m mesh copper grids and stained in 6%
3 families in the Paguroidea, and introducesa simple key aqueous uranyl acetate for40 min; rinsed in distilled wa-
to classify these hermit crabs to family, based on light ter; stained with Reynold's lead citrate (Reynolds, 1963)
microscope observations oftheir spermatophores. for 20 min; and further rinsed in distilled water. Micro-
graphsweretaken on a Hitachi 300transmission electron
Materials and Methods microscope at 80 kV.
Collection sites and dates for the species in this paper Forscanning electron microscopy, 3% glutaraldehyde-
fixed spermatophores were dehydrated through a graded
are as follows:
series of ethanol (80-100%) at 10 min intervals. They
Family Coenobitidae were then dried after being placed in a drop ofether and
IslBainrdgsi,tSslWatPraoc(ifLiicn,nOacetuosbe1r7,671)9,88M;alCaoietnaobIsiltaandb.rSeovliommaonnm sPphuitlitpesr 5c0o5atsecdanwnitihnggeollde;ctrmoincrmoigcrraopshcsopweeraet 2t0a-k3en0koVn. a
Dana 1852, Coenobitaperlatus H. Milne Edwards 1837 Results
andCoenobitantgosusH. Milne Edwards 1837,Suwarrow
Atoll National Park, Cook Islands, SW Pacific, August, Family Coenobitidae
1990; Coenobita spinosus H. Milne Edwards 1837, Dar- The tripartite, pedunculate spermatophores ofBirgits
win, Northern Territory, Australia, May, 1990. latro are approximately 650 nm in length from pedestal
to apex ofthe ampulla. The sperm-filled ampulla is 440
FamilyDiogenidae
fj.m long and 450 ^m wide and forms an inverted heart-
Calciumlatens(Randall 1839), Calcinusmimitus Bui- shape (Fig. 1A). The stalk of the spermatophore is ap-
tendijk 1937 and Clibanarius corallinus (H. Milne Ed- proximately 100 /urn in length. The spermatophore is lat-
wards 1848), Heron Island, Queensland, Australia, De- erally widerthan deep, and therefore is slightly spatulate
cember, 1990; Clibanarius virescens(Krauss 1843). Dun- and is composed oftwo halves, which meet at the lateral
wich. North Stradbroke Island, Queensland, Australia, edge as a raised ridge (Fig. 3A). This ridge is 20 ^m thick
April, 1990; Dardanus lagopodes (Forskal 1775) and while the remaining spermatophore wall is only 10 nm
Dardanus megistos (Herbst 1804), Heron Island, thick. Underadouble Mallory'sstainingprocedure(Mai-
Queensland, Australia, December, 1990; Diogenes gar- lory, 1936) the spermatophore wall is shown to be com-
dineriAlcock 1905, Mooloolaba, Queensland, Australia, posedoftwo layers: an inner, darkerstaininglayer, which
October, 1990. isdiscontinuous at the ridge, and an outer, lighterstaining
layer, which covers the entire ampulla and increases in
Family Paguridae
thickness at the ridge.
Pagtints hirtimanus Miers 1880, Heron Island, ThepedunculatespermatophoresofCoenobitaspinosus
Queensland. Australia, December, 1990. are similar in shape to those of Birgus latro but much
240 TUDGE
C. C.
Coenobita
rugosus
Coenobita
^'^--' spinosus
Coenobita
Coenobita perlatus
J brevimanus
Clibanarius
corallinus
Clibanarius
virescens
urus
hirtimanus
Diogenes
gardineri
M
HERMIT CRAB SPERMATOPHORE DIVERSITY 241
smaller (Fig. IB). Each individual spermatophore is ap- Clibanarius is similarto that ofthe Calcinusspecies. Cli-
proximately 170 jum in length from base ofthe pedestal banariits virescens has a small spermatophore, only 150
to the top ofthe ampulla. The ampulla, which is approx- ^m long with a short, thin stalk 70 ^m long and 10 ^m
imately 1 10^m long, iscomposed oftwo halvesthatjoin wide. The ampulla is 75 p.m in length and width and has
ata conspicuous lateral ridge. The stalk ofthe spermato- ventrally directed projections(25 /urn long) which appear
phore isonly 20 j/m long. Thewidth oftheampulla from to be extensions ofthe lateral ridge (Fig. 1H). The distal
ridge to ridge is approximately 1 10 nm, while the depth end ofthe stalk penetrates into the ampulla as a dorsally
ofthe ampulla is only 100 ^m. This gives the ampulla a directed projection.
slightly spatulate shape, with the ridge running around The spermatophore of Clibanarius corallinus is twice
the lateral edge. The ampulla is surrounded by a sper- the length (300 ^m) ofthat ofClibanarius virescens, but
matophore wall 2 ^m in thickness, which increases to 3 otherwise it is morphologically similar (Fig. II). The 220
nm at the ridge, and is filled with many closely packed nm stalk is slightly wider at 15 nm. The ampulla is 60
spermatozoa, separated byanextracellular matrix. Ultra- ^m long and 75 pm wide and possesses the same exten-
structural studies show the ridge to be a break in the fi- sions ofthe lateral ridge, although the extensions in this
brillar structure ofthis wall (Fig. 3C). species are only 12 ^m in length. The ampulla is only
The spermatophores of Coenobita nigosus are larger slightly penetrated by a broad dorsal projection at the
than those of Coenobita spinosus. being 190 ^m long, distal end ofthe stalk (Figs. II, 2E).
with an ampullar length and width of 150 and 100 ^m. Dardanus lagopodes has a distinctive spermatophore,
respectively. The ampulla, which is slightly more elongate in comparison to the rest of the Paguroidea studied, in
than either Birgus latro or Coenobita spinosus, sits on a that some have two ampullae at the apex ofa single stalk
stalk 32 urn high (Fig. 1C). (Figs. U, 2D). Ofthe observed spermatophores, approx-
Coenobitabrevimamishasaspermatophore 290/urn in imately 20% were double-headed. Both single and double-
length which is composed ofa stalk that is 90 nm long headed spermatophores were the same length, and each
and an ampulla that is 180 ^m long and 1 10 jum wide. had similar ampullae. The spermatophores were 600 ^m
Although the ampulla is larger than that of Coenobita long with a 530 p.m stalk, that had a mean width of 20
rugosus, its shape is very similar (Figs. ID, 2A). ^m. Each ampulla was 70 nm long and 80 ^m wide. In
Thespermatophore ofCoenobitaperlatusisthe largest the spermatophores with two ampullae the stalk forked
ofthe four species of Coenobita studied. At 600 ^m in only at the most distal 50-70 mm (Fig. 2D).
length, it is only slightly smaller than the spermatophore ThespermatophoresofDardanusmegistosareverydif-
ofBirgus latro (Fig. 1A). The ampulla, 400 nm long and ferent from that ofDardanus lagopodes in both size and
230 ^m wide, is similar in shape to those of Coenobita morphology (Figs. IK, 2B). They appear more similarto
rugosusand Coenobitabrevimamisand issituatedon top thespermatophoresofthetwo Calcinusspecies. Dardanus
ofa stalk that is 180 ^m long (Fig. IE). megistos has a spermatophore that is only 160 /urn long,
astalkthatis90^m longand 20^m wideandanampulla
FamilyDiogenidae thatis60nmlongand45nmwide.AsinCalcinusminutus
The spermatophores ofCalcinus minutus are 180 //m and Calcinus latens(Figs. 1F, G), thestalk gradually wid-
long, composed of a stalk that is 1 10 jum long and an ens distally so as to appear to envelop the ampulla, but
ampulla 60 /urn long and 70 ^m wide. The stalk is very unlike these species, the broad end ofthe stalk projects
slender, only 10 /um wide, and gradually thickens distally considerably into the ventral aspect of the ampulla
toenvelopthesphericalampulla(Figs. IF, 3D).Thisshape (Fig. IK).
is also found in Calcinus latens, but the entire spermato- The spermatophore of Diogenes gardineri is different
phore is smaller in the latter. The over-all length ofthe from those of any of the other diogenid genera in this
spermatophore ofCalcinuslatensis 150^m, thethin stalk paper. The entire spermatophore is 430 ^m in length,
being 110 ^m long and 15 ^m wide, and the ampulla with 300 /um of that being the thin (15 ^m) stalk. The
dimensions are 50 by 50 /um (Figs. 1G, 2C). ampulla is approximately square in outline with length
The spermatophore morphology ofthe two species of and width dimensions both being 130 ^m. The ampulla
Figure 1. Semidiagrammatic representationsofspermatophoresofhermit crabs from three familiesof
the Paguroidea. (A-E) Coenobitidae. A. Birgus latro, B. Coenobita spinosus, C. Coenobita rugosus, D.
Coenobitabrevimamis. E. Coenobilaperlatus. (F-L) Diogenidae. F. Calcinusminutus. G. Calcinuslalens,
H.Clibanariusvirescens. I. Clibanariuscorallinus.J.Dardanuslagopodes. K. Dardanusmegistos. L.Diogenes
gardineri. (M) Paguridae. M. Pagitrushirtimanus. Drawn from light micrographs. All tothe samescale,a;
ampulla, aa;accessory ampulla, p;pedestal, s;spermatozoa, st; stalk.
242 C. C. JUDGE
is penetrated ventrally by a thin projection, which origi- dividuals ofBirgus latro was later observed and reported
nates at the distal end ofthe stalk, to a depth of60 nm by Helfman (1977). He also observed several terrestrial
(Figs. 1L, 2G-I). matings in the semi-terrestrial hermit crab, Coenobita
perlatus. These observations indicate that, in the Coe-
nobitidae, spermatophore transfer and fertilization can
Family Pagwidae
occur on land. The robust nature ofthe spermatophores
The spermatophores of the single representative col- in this family may be an adaptation to facilitate sper-
lected from this family, Pagurus hirtimanm, are mor- matophore survival on the external surface ofthe female
phologically very different from any other Paguroidea in while she is on land. Large spermatophores with short,
this paper. The spermatophores, although considered to thick stalks would be harder to damage or dislodge from
bestalked (pedunculate), do notappeartohaveadefinite thegelatinousspermatophoricmassattached tothefemale
stalk lifting the ampulla above the pedestal. Another im- than slender stalked spermatophores.
portant difference is the presence of a secondary or ac-
cessoryampulla, atthebaseofthemainampullabut much Diogenidae
smallerthan the latter(Figs. 1M, 2F). Thisaccessory am-
pulla hasonlybeen described in representatives from this The Diogenidae is a large hermit crab family encom-
family. The entire spermatophore ofPagunis liirtimanus passing many genera including Calcinus. Clibanaritis,
is400//m in length and the attached stalk is 100 i*m long Dan/anus, andDiogenes. Therepresentativesinthisstudy,
by 50 ^m wide. The main ampulla is 280 ^m long and from the above genera, show a great diversity of sper-
150 j/m wide while the accessory ampulla is only 36 j/m matophore form (Figs. 1F-L), but within the limits ofa
long and 12 ^m wide (Fig. 1M). The accessory ampulla characteristic familial morphology. The spermatophores
is often devoid ofspermatozoa but may contain one or generally have long, thin stalks (less than 20 jum in di-
two sperm cells (Fig. 2F). ameter) and small spherical ampullaeapproximately 50-
70 jim in size. The investigated Diogenesganiineri is an
Discussion exception to the latter case, as it has larger ampullar di-
mensions (Figs. 1L, 2G-I).
Coenobitidae Eachofthegeneracanbedistinguishedbyitspossession
of specific structural features. These distinctive generic
The spermatophores ofthe five representatives in the formscan becomplicatedbyunusual morphologies, such
Coenobitidae(Fig. 1A-E)all showasimilarover-all mor- as the double-headed spermatophores of Dardanus la-
phology and only size differences distinguish them. The gopodes (Figs. U, 2D). The 20% occurrence rate ofthis
spermatophores in this family are characterized by large form among the majority of single-headed spermato-
spherical toovoidampullaewith short thick stalks, giving phores suggests that they might not be aberrant. This is
them agenerally robustappearance. I considerthegenera the first record ofdouble-headed spermatophores in the
intheCoenobitidaetobeeithersemi-terrestrial, Coenobita Diogenidae (also for the Paguroidea), and further study
spp., or terrestrial, Birgus latro. based on their differing may reveal whether this is more common among other
abilities to withstand desiccation and their subsequent
genera.
dependence on the marine environment. All the representatives in the Diogenidae are aquatic;
In the Paguroidea, spermatophores are attached to the mating and fertilization occur in water. Spermatophores
exoskeleton ofthe female hermit crab or on the surface are placed externally on eitherthe carapace ofthe female
ofthetemporarily inhabited gastropodshell, bythesticky or the gastropod shell she inhabits. The fact that desic-
baseorpedestal (Matthews, 1956; Greenwood, 1972), and cation ofthe spermatophoric massisnot a problem in an
generallyareembeddedinagelatinousmass. Inanaquatic aquatic habitat may be reflected in the fragile structure
habitat, the spermatophoric mass does not dry out and of the slender-stalked spermatophores of these species.
thus can be carried around for long periods; but for ter- The long slender stalks in Clibanarius cora/linus. Dar-
restrial species or species that venture from the water for danus lagopodes, and Diogenes gardineri (Figs. II, J, L)
periods oftime, desiccation ofthe spermatophoric mass may reflect the needto usethewaterfortheextrasupport
is a problem. Matthews (1956) assumed that copulation, ofthe sperm-filled ampullae.
spermatophore deposition, and fertilization in the semi-
terrestrial species, Coenohita rugosus, and the terrestrial
Paguridae
coconut crab, Birgus latro, occurred in water, mainly be-
cause the remainder ofthe reproductive cycle is aquatic The 12 species within the family Paguridae have been
andalsobecause noone hadobservedaterrestrial mating studied forspermatophore morphology(seeIntroduction),
in this family. making it the most studied familyofthe Paguroidea. The
One instance ofterrestrial copulation between two in- single species for which the spermatophore is illustrated
HERMIT CRAB SPERMATOPHORE DIVERSITY 243
Figure2. Lightmicrographsofspermatophoresofhermitcrabs.(A)Coenobitabrevimanus(Coenobitidae).
(B)Dardanusmegislos(Diogemdae).(C)Caleinuslatent(Diogenidae).(D)Dardanu.tlagopodes(Diogenidae).
Notethedouble-headed spermatophores. (E) Clibanariuscorallinus(Diogenidae). (F) Pagunishinimamit
(Pagundae). Detail ofthe accessory ampulla containing a single spermatozoa. (G-I) Diogenes gardineri
(Diogenidae). Seriesofthree micrographs from the proximal to thedistal end ofthe vasdeferensshowing
the progressive lengthening ofthe spermatophore stalk, a: ampulla, aa; accessory ampulla, p: pedestal, s;
spermatozoa, st;stalk.
244 C. C. JUDGE
and described in this paper conforms with the general This process of stalk lengthening, whether there is a
familial morphology (Fig. 1M). Pagurid spermatophores pseudo-stalk or a true stalk, occurs during maturation of
differ from those ofthe Coenobitidae and Diogenidae in all spermatophores ofthe Paguroidea, with theexception
three important ways: of Trizopagurus maximus and Trizopagurus strigatus
(Matthews, 1957). Ifspermatophore morphology is to be
1. Although considered pedunculate (Greenwood, compared between species, care must be taken to obtain
1972), the spermatophores ofthe Paguridae tend to have only mature spermatophores from the most distal portion
only a short stalk, which is often incorporated into the of the vas deferens or to use extruded spermatophores.
pedestal and gives the appearance of being non-pedun- Immaturespermatophore morphologyofonefamilymay
culate (Matthews, 1957). Greenwood (1972), following beconsistentwith the mature spermatophore form ofan-
the terminology ofMouchet (1931), divided the vas def- other family. An example ofthis can be seen in Figure
erens of the hermit crab, Pagitrus novizealandiae, into 2G-I, where the short stalked, immature spermatophore
nine discrete regions. The different musculature in each ofDiogenesgardineri is reminiscent ofa coenobitid type
ofthe nine regions is responsible forfragmentation ofthe spermatophore, whilethe maturespermatophore from the
continuoussperm ribbon intospermatophores. Thepres- distal vas deferens shows clearly its diogenid origins
ence or absence ofeach ofthe nine regions dictates the
(Fig. 1L).
form ofthe spermatophore in the Paguroidea. In the Pa-
guridae, regions fourand six (areas ofstalk secretion and
elongation respectively) are absent. This led Matthews Spermatophore lateral ridge
(1957) to state that the spermatophores of members of The conspicuous lateral partition seen by Mouchet
the Paguridae were non-pedunculate. However, Green- (1930) on the ampulla ofthe spermatophore ofDiogenes
wood (1972) found that therewasastalk in Pagunts nov- pugilatorand laterby Hamon(1937)inasimilarposition
izealandiaebutthat isismoulded from thecapsulesheath. for Pagitrusprideaux (as Eupagurusprideauxi) was cor-
He suggested that, in accordance with Mouchet's (1931) rectly identified by both workersasthejoining line ofthe
description ofthe spermatophores of other members of two halves ofthe ampulla. Hamon (1937) called thispar-
thePaguridae, a"pseudo-pedicule" formsthestalkinthis tition the"lignedesuture" andshowed thatitran around
family, which is analogous to the true stalk in the Coe- theelongatespermatophore ofPagiirusprideauxandwas
nobitidae and Diogenidae. where the two halves ofthe ampulla separated to release
2. The ampullae are often elongate or cylindrical in the contained spermatozoa. Hamon also suggested two
nature and fairly large. main mechanisms of spermatophore dehiscence: one
3. Most importantly, the spermatophores have a sec- being changes in internal pressure due to mechanical or
ondary, smaller ampulla, which is termed the accessory osmotic forces and the other being the chemical disso-
ampulla. This accessory ampulla is found at the base of lution ofthe suture that unites the two halves ofthe am-
the main ampulla andgenerallycontains no spermatozoa, pulla.
although oneortwoindividual spermatozoa maybepres- Thissuture line,orlateral ridge, hasnowbeen recorded
ent (Fig. 3D). This accessory ampulla is formed by the in species from three paguroidean families, the Coenob-
vesiculation ofthe empty sperm column sheath that sep- itidae [Birgus latro, Tudge and Jamieson, 1991; present
arates each ofthe developing main ampullae (Mouchet, study (Fig. 3A); Coenobita spinosus, present study (Fig.
1931;Matthews, 1957). Therhythmic musclecontractions 3C)], the Diogenidae [Calcinus minutus, Clibanarius vi-
ofthe reproductive tract fold the continuous sperm col- rescens. present study (Figs. 3B, D); Diogenespugilator,
umn into partially closed arches filled with developing Mouchet, 1930], and the Paguridae (Pagiirus prideaux,
spermatozoa, with the compressed empty sperm column Hamon, 1937).
in between. In the Coenobitidae and Diogenidae the Lightmicroscopestudiesusing Mallory'sstainingtech-
elongation ofthe stalk is sufficient to stretch this empty niques, scanning electron microscope studies (Fig. 3A),
sperm column sheath and obscure it. Mouchet (1931) il- and transmission electron microscopestudies(Fig. 3B, C)
lustrated an accessory ampulla in the developing sper- show that the lateral ridge isa thickening oftheampullar
matophore ofthe diogenid Pagitristes oculatus, but it is spermatophore wall. The spermatophore wall ofCoeno-
absent from the mature spermatophore. Because regions bita spinosus is fibrillar in nature, and at the lateral ridge
four and six are absent in the Paguridae, stalk elongation there is a break in this structure (Fig. 3C). Although the
is not significant. The sperm column sheath is, therefore, ridge is structurally thicker than the remainder of the
notstretched, leavingan empty vesicleatthebase ofeach spermatophore wall, this gap in the fibrous matrix is a
main ampulla. Some spermatozoa may be sealed in this weakness where splitting ofthe two ampullar halves oc-
vesiclebuttheirrelease, upondehiscenceofthe main am- curs. A similarbreak in thespermatophorewall structure
pulla, is doubtful. is seen in Clibanarius virescens(Fig. 3B), but an external
HERMIT CRAB SPERMATOPHORE DIVERSITY 245
Figure3. (A) Birgiislatro(Coenobitidae). Scanningelectron micrograph oftwosperniatophoresshowing
conspicuouslateral ridge. (BandC)Transmission electron micrographsshowingdetail ofthe lateral ndge.
(B)Clibanariusvirescens(Diogenidae).Notetheapparentplugofmaterialinthelateralridge.(C)Coenobita
spinosus (Coenobitidae). (D) Caldnus mimilus (Diogenidae). Light micrograph showing splitting ofthe
spermatophoreampullaatthelateral ridgetoreleasespermatozoa.(Arrowindicatesthepointofseparation
ofthetwoampullarhalves), a; ampulla, em; extracellular matrix, r; lateral ridge, sispermatozoa, sw; sper-
matophore wall.
plug appears to cement the two halves of the ampulla cautious, however, in drawing homologies between spe-
together in this species. Release ofspermatozoa from the cies based on spermatophore form and modes ofsperm
splittinglateral ridgeofaspermatophoreofCaldnusmin- transferbefore the modes offormation, chemical nature,
iitus is seen in Figure 3D. and ultrastructural morphology ofthe spermatophores
Spermatophore morphology and modes of sperm inquestion havebeenstudied indepth. Similarly, caution
transfer provide some clarification of systematic prob- has to be exercised when phylogenetic hypotheses are
lemsat familial and generic levels(Schaller, 1979; Bauer, formulated on limited data sets and small numbers of
1986)andsometimesevenatthespecificlevel(Matthews, representatives from the selected taxa. Both Clark (1981)
1953, 1956). The phylogenetic value ofspermatophore and Mann (1984) state that particular modes ofsperm
form and sperm transfer mode has been demonstrated transfer used by organisms may be more directly influ-
in pseudoscorpions by Weygoldt (1966). One has to be enced by the habitat of those organisms than the phy-
246 C. C. TUDGE
PAGURIDAE DIOGENIDAE COENOBITIDAE
Long, thin slalk Short, thick stalk
Small, spherical ampulla Large, ovoid ampulla
Presenceof main
ampulla and
accessory ampulla
Presenceof
mam ampulla only
Tripartite pedunculate
paguroidean spermatophore:
consisting of an ampulla,
slalkandpedestal
Figure4. A branchingkeytoclassifytheinvestigated hermitcrabsintotheirrespectivefamilybasedon
thestructureoftheirspermatophores. Spermatophores nottoscale.
logenetic relationships. It seems very likely that both Acknowledgments
habitat and phylogeny influence spermatophore mor- I wish to acknowledge the assistance ofMr. S. Lavery
phology ofany particular taxa. Forexample, intheCoe- for supplying the SW Pacific specimens and Mr. S. Fitz-
nobitidae, the move to a semi-terrestrial or terrestrial simmons for helping to collect on Heron Island. Many
lifestyle from a marine one may have influenced the thanksto Mr. S. Cook (Queensland Museum)and Dr. G.
shape of the spermatophores of the species concerned, Morgan (Western Australian Museum) for identifying
but the over-all tripartite, pedunculate spermatophore many of the species, and to Mrs. L. Daddow (Zoology
plan is phylogenetically set. Department, University of Queensland) and Mr. D.
In the Paguroidea, light microscope observations of Waddell (Electron Microscope Centre, University of
spermatophores can be used successfully to distinguish Queensland) for valuable technical assistance. I also wish
the three separate families and possibly even apply at the to acknowledge the help ofthe staffat Heron Island Re-
generic level, but more species will have to be studied to search Station, Great Barrier Reef, Queensland. The
beconfidentataspecificlevel. Someexceptionshavebeen helpfulandconstructivesuggestionsofthereviewerswere
recorded, as in the case of Cestopagnrus timidus also greatly appreciated.
(Mouchet, 1431, as Eitpagurm timidus}, in which a pa-
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