Museum Victoria, formerly the Museum of Victoria, was formed in

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Contents

1 > Biology of the Anomura - foreword to this special issue

R. Lemaitre and C.C. Tudge

3 > Neurobiology of the Anomura: Paguroidea, Galatheoidea and Hippoidea

D.H. Paul

13 > Terrestrial adaptations in the Anomura (Crustacea: Decapoda)

P. Greenaway

27 > Marine hermit crabs as indicators of freshwater inundation on tropical shores

S. G. Dunbar, M. Coates and A. Kay

35 > Hermit crab population ecology on a shallow coral reef (Bailey’s Cay, Roatan, Honduras): octopus predation and hermit crab shell use

S. L. Gilchrist

45 > Population dynamics and epibiont associations of hermit crabs (Crustacea: Decapoda: Paguroidea on Dog Island, Florida

F. Sandford

53 > The morphology of cardiac and pyloric foregut of Aegla platensis Schmitt (Crustacea: Anomura: Aeglidae)

T. S. Castro and G. Bond-Buckup

59 > Circadian and seasonal variations of the metabolism of carbohydrates in Aegla ligulata (Crustacea: Anomura: Aeglidae)

G. T. Oliveira, FA. Fernandes, G. Bond-Buckup, A.A. Bueno and R.S.M. Silva

63 > Endemic and enigmatic: the reproductive biology of Aegla (Crustacea: Anomura: Aeglidae) with observations on sperm structure

C. C. Tudge

71 > A worldwide list of hermit crabs and their relatives (Anomura: Paguroidea) reported as hosts of Isopoda Bopyridae

J.C. Markham

79 > Geographic and distributional patterns of western Atlantic Porcellanidae (Crustacea: Decapoda: Anomura), with an updated list of

species

B. Warding, A. Hiller and R. Lemaitre

87 > A checklist of marine anomurans (Crustacea: Decapoda) of Pakistan, northern Arabian Sea

FA. Siddiqui and Q.B. Kazmi

91 > Calcinus hermit crabs from Easter Island, with biogeographic considerations (Crustacea: Anomura: Diogenidae)

J. Poupin, C.B. Boyko and G.L. Guzman

99 > Hermit crab species of the genus Clibanarius (Crustacea: Decapoda: Diogenidae) from mangrove habitats in Papua, Indonesia, with

description of a new species

D. L. Rahayu

1 05 > A new genus and species of hermit crab (Crustacea: Anomura: Paguridae) from Taiwan

R. Lemaitre

111 > Illustrated keys to families and genera of the superfamily Paguroidea (Crustacea: Decapoda: Anomura), with diagnoses of genera of

Paguridae

PA. McLaughlin

145 > A new theoretical approach for the study of monophyly of the Brachyura (Crustacea: Decapoda) and its impact on the Anomura

M. Tavares

Memoirs of Museum Victoria 60(1): 1 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

Biology of the Anomura — foreword to this special issue

Rafael Lemaitre' and Christopher C. Tudge'-^

‘Department of Systematic Biology, National Museum of Natural History, Smithsonian Institution, Washington, DC

20013-7012, USA (lemaitre.rafael@nmnh.si.edu)

^Biology Department, American University, 4400 Massachusetts Ave, NW, Washington, DC 20016-8007, USA

(ctudge@american.edu or tudge.christopher@nmnh.si.edu)

The Latin name Anomura, widely in use since the mid nine-

teenth century, is attributed to MacLeay (1838) even though the

names Anomalia and Anomala are the oldest (McLaughlin and

Holthuis, 1985). Ever since the concept of the group was first

proposed by Latreille (1816) albeit in the vernacular form

“anomaux”, there has been controversy over its composition,

classification and evolutionary relationships. Most carcinol-

ogists currently accept that the Anomura consist of the

Lomisoidea, Galatheoidea, Hippoidea and Paguroidea (e.g.

Martin and Davis, 2001). However, to some, the interpretation

of the Thalassinoidea and Dromiacea — groups that have drifted

in and out (current consensus is that both are out) of the

Anomura — continues to prove problematical.

Interest in the study of the systematics and biology of the

Anomura has been renewed in the last decade or so. This has

been a most welcome development for this group has tradition-

ally been one of the least understood of decapod crustaceans. In

part, this interest has been fueled by a remarkable increase in

descriptive works documenting anomuran diversity throughout

the world oceans, in particular from the deep sea and from the

Indo-Pacific region, but also of the South American endemic

freshwater family Aeglidae. Equally important have been stud-

ies on biological aspects of semi-terrestrial, shallow- water, and

deep-sea vent-associated species. Key fossil discoveries have

been made in Paguridae, Lithodidae and Aeglidae. A number of

ground-breaking studies have been published using modern

phylogenetic methods to analyse new or improved data from

adult and larval morphology, mitochondrial DNA, gene

rearrangement, and sperm ultrastructure. As a result, a fresh

although still hotly debated picture of anomuran evolution is

emerging.

An opportunity to organise a symposium. Biology of the

Anomura, the first devoted exclusively to this group, came with

the Fifth International Crustacean Congress (ICC5), 9-13 July

2001, in Melbourne, Australia. Altogether, 51 authors pre-

sented 11 oral papers and 14 posters on one day during the

Congress. This volume of the Memoirs of Museum Victoria

presents 16 papers by 26 authors, and represents but a

cross-section of the groups and fields now under study by

anomuran co-workers worldwide. Included are two important

review papers on neurobiology and semi-terrestrial adapta-

tions; three on ecology of hermit crabs; three on morphology,

metabolism, and reproduction of the endemic Aeglidae; six on

taxonomy, including modern keys to all families and genera of

hermit crabs with diagnoses of genera of Paguridae; one on

porcellanid biogeography; and one providing a new theoretical

approach to resolving the long-standing problem of whether the

Podotremata crabs belong in the Brachyura or Anomura. Not

all those who attended the symposium submitted manuscripts

for this volume. Others who could not attend the Congress

submitted papers for this volume.

As coordinators of the Symposium, and editors of this vol-

ume, we trust this will be the first of many symposia and papers

focusing on the fascinating and challenging group that are the

anomurans.

References

Latreille, P.A. 1816. Les Crustaces, les Arachnides et les Insectes. Vol.

3, pp. i-xxix, 1-653 in; Cuvier, C., Le regne animal distribue

d’apres son organisation . . . (first edition). Deterville: Paris.

(Crustacea: pp. 5-72).

MacLeay, W.S., 1838. Illustrations of the Annulosa of South Africa;

being a portion of the objects of natural history chiefly collected

during an expedition into the interior of South Africa, under the

direction of Dr. Andrew Smith, in the years 1834, 1835, and 1836;

fitted out by “The Cape of Good Hope Association for exploring

Central Africa”. Pp. 1-75, pis 1-4 in; Smith, A. Illustrations of the

zoology of South Africa (Invertebrata). Smith, Elder & Co.:

London.

Martin, J.W., and Davis, G.E. 2001. An updated classification of the

Recent Crustacea. Natural History Museum of Los Angeles County,

Science Series 39: 1-124.

McLaughlin, P.A., and Holthuis, L.B. 1985. Anomura versus Anomala.

Crustaceana 49; 204-209.

Memoirs of Museum Victoria 60(1): 3-11 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

Neurobiology of the Anomura: Paguroidea, Galatheoidea and Hippoidea

Dorothy Hayman Paul

Department of Biology, University of Victoria, Box 3020, Victoria, BC V8W3N5, Canada (dhp@uvvm.uvic.ca)

Abstract Paul, D.H. 2003. Neurobiology of the Anomura: Paguroidea, Galatheoidea and Hippoidea. In: Lemaitre, R., and Tudge,

C.C. (eds). Biology of the Anomura. Proceedings of a symposium at the Fifth International Cmstacean Congress,

Melbourne, Australia, 9-13 July 2001. Memoirs of Museum Victoria 60(1): 3-11.

Anomurans are valuable subjects for neurobiological investigations because of their diverse body forms and behav-

iours. Comparative analyses of posture and locomotion in members of different families reveal that peripheral differences

(in skeleton and musculature) account for much of the behavioural differences between hermit crabs and macrurans

(crayfish), squat lobsters and crayfish, hippoid sand crabs and squat lobsters, and albuneid and hippid sand crabs, and

that there are correlated differences in the central nervous systems. The order of evolutionary change in discrete neural

characters can be reconstructed by mapping them onto a phylogeny obtained from other kinds of data, such as molecu-

lar and morphological. Such neural phylogenies provide information about the ways in which neural evolution has oper-

ated. They are also useful in developing hypotheses about function of specific neural elements in individual species that

would not be forthcoming from research on single species alone. Finally, comparative neurobiological data constitute a

largely untapped reservoir of information about anomuran biology and anomuran relationships that, as more becomes

available, may be helpful in systematics and phylogenetics.

Keywords Cmstacea, Anomura, neurobiology

Introduction

The diversity of body forms and behaviours that have evolved

within the Anomura (Fig. 1) offer neurobiologists numerous

opportunities to examine variants in form and function in iden-

tified neurons and neural circuits mediating specific move-

ments or elements of behaviour and the relationships between

them. This is because discrete and identifiable neural differ-

ences are expected to underlie inter-specific differences in

behaviour ranging from single movements of individual

appendages to agonistic interactions. The variants in amplitude

and order of pereopod joint movement during locomotion or

posturing during social encounters, or in the social behaviours

themselves, may therefore be viewed as the results of natural,

as opposed to invasive, experiments to manipulate different

neurophysiological and neuroanatomical parameters in the

nervous system of one taxonomic group (Antonsen and Paul,

1997, 2000, 2002; Faulkes and Paul, 1997b, 1998; Paul, 1991).

In addition to investigating mechanistic issues in neuroscience,

such comparative research can begin to address such funda-

mental questions in evolutionary neurobiology as: How con-

servative are neurons and neuronal circuits? Are some

morphological and physiological features more easily (i.e.,

often) modified than others during behavioural evolution?

What constraints on changing complex neuronal networks are

imposed by the necessity that they remain functional through

speciation? We are far from achieving definitive answers to any

of these questions, particularly the last one, but the comparative

data on the neurobiology of some anomurans summarized here

indicate the direction toward which the answers are likely to lie.

From an entirely different perspective, comparative research on

adult and embryonic nervous systems can provide taxonomists

and evolutionary biologists with useful characters to supple-

ment other types of data used to construct phylogenies

(Breidbach and Kutsch, 1995; Harzsch and Waloszek, 2000;

Sandeman and Scholtz, 1995; Scholtz and Richter, 1995;

Strausfeld, 1998; Whitington, 1995; Whitington and Bacon,

1997). This is because nervous systems are relatively conserva-

tive through evolution (compared with other internal tissues

and organ systems), although not to the degree once thought

(Whitington, 1995; this review). Species differences between

identified neurons and neural connections can be recognized

because they stand out against a background of highly con-

served neural architecture. Most comparative work has been at

higher taxonomic levels, and the Anomura, considering their

diversity, are under-represented even in studies focusing on

Decapoda.

Comparative neurobiological research. Neurons and neuro-

behavioural circuits do not fossilize, which makes recognition

of modern surrogates for ancestral neural traits essential for an

understanding of nervous system evolution. In external

Dorothy Hayman Paul

S Munida Galathea Blepharipoda Lipidopa Emerita

quadrispina strigosa occidentalis califomica analoga

FAC

hMoG

Porcellanidae Galatheidae

Albuneidae Hippidae

gait4 ^

switch

nonspiking TUSR

spiking TUSR

leg 4~nropod^

nonG ^nropod

beating

Galatheoidea

fTTTTl hMoG

Hippoidea

legs-nonG^

walking ^ digging^

RSM

MoG

Pagnroidea

spiking TUSR

Astacidea

Thalassinidea

Anomura Brachyura

nonG

VTF

lgI

MG, LG, MoG, nonG, FAC, VTF, walking (CPG/leg)

Figure 1. Neural characters and systems discussed mapped onto a partial phylogeny of Reptantia (based on Morrison et al., 2001, and Schram,

2001). Filled boxes: character present; hatched boxes: character modified; open boxes: character lost. AT - anterior telson muscle and moto-

neuron; FAC - fast, anterior, contralateral flexor motoneurons; hMoG - homologue of MoG (Sillar and Heitler, 1985); MG - medial giant

interneuron pair; LG - lateral giant interneurons; MG - medial giant intemeurons; “MG” - modified MG system (Heitler and Fraser, 1986, 1987);

MoG - motor giant flexor motoneuron; nonG - non-giant (as opposed to LGs, or MGs) interneuron system for swimming by repetitive tail-

flipping; RSM - return stroke muscle and motoneurons; TUSR - telson-uropod stretch receptor (nonspiking: graded potentials transmitted;

spiking: receptor potential converted to action potentials). VTF - ventral telson flexor muscle. 1. It is debated whether homologues of macruran

MG and LG neurons have been retained in brachyuran thoracic nerve cord. Retention of MG homologues could be expected for their direct con-

nections to leg promotor motoneurons, which in crayfish cause the legs to extend forward, thus contributing to the rearward trajectory of the MG-

triggered tailflips (Heitler and Fraser, 1989). The LG neurons have no known output to thoracic leg musculature in macrurans and are presumed

absent from Brachyura. If LG homologues are present, then their losses from the thalassinid and anomuran lineages occurred independently.

2. The stereotyped movements of sand crabs’ (Hippoidea) digging legs differ between legs 2/3 and leg 4, corresponding, respectively, to back-

ward walking and forward walking movements in other species (Faulkes and Paul, 1998). 3. Rhythmic movements of the legs and “tail” co-occur

in Hippoidea, whereas their homologues (walking and tailflipping) in walking species are mutually excusive (Faulkes and Paul, 1997a). 4. Right

and left legs of each segment alternate at onset of digging, then switch to bilateral synchrony (Faulkes and Paul, 1997b). 5. Rhythmic digging

movements of the fourth legs are coordinated with uropod strokes (homologue of nonG flexions) rather than with the anterior legs (Faulkes and

Paul, 1997a). Not included are the changes from the ancestral macmran condition in aminergic systems and agonistic behaviours of

M. quadrispina (Antonsen and Paul, 1997, 2001).

Neurobiology of the Anomura

morphology and modes of locomotion, galatheids most closely

resemble macruran reptantians, such as crayfish. The external

form of crayfish, particularly of the abdomen and tailfan, is

similar to that of the early fossil decapod Paleopalaemon new-

berryi (Schram et al., 1978). Similar morphology suggests

similar behaviour, in this case, posture and uses of the “tail”,

making neurobiological data on sensory and motor systems in

crayfish for the most part suitable surrogates for the ancestral

decapod condition. Therefore, regardless of specific phylo-

genetic relationships, many neurobiological features of cray-

fishes may reasonably be considered surrogates for the

ancestral condition of homologous features in anomurans

(Paul, 1989a, 1991; Paul et al., 1985, 2002).

Anomuran neurobiology

Anomurans have, by definition, modified the ancestral mac-

ruran reptantian “tail” (abdomen and tailfan). The most obvious

coiTelated neural difference from their macruran ancestors is

fusion of the first abdominal with the last thoracic ganglia,

leaving five free abdominal ganglia in the “tail”, the homo-

logues of macruran abdominal ganglia 2 through 6. The cytoar-

chitecture of abdominal ganglion 1 in galatheids and hippoids

has not substantially changed, however, so that identification of

homologues of its neurons with those in the more posterior

abdominal ganglia, as well as with neurons in macruran

abdominal ganglia, is relatively straightforward (Antonsen and

Paul, 2001a; Mittenthal and Wine, 1978; Wallis et al., 1995;

Wilson and Paul, 1987). Nineteenth and early twentieth

century neurobiologists (or, in the vocabulary of the time, zool-

ogists, anatomist, physiologists) described a plethora of inter-

esting features about crustacean, including some anomuran,

behaviours and nervous systems (see references in Bullock and

Horridge, 1965), many of which could profitably be revisited

with modern research tools. For example, Alexandrowicz

(1951, 1952,1954), through unparalleled use of methylene blue

staining, described details of dorsal muscle receptor organs

(analogues of mammalian muscle spindles) in numerous crus-

taceans, including pagurids. Alexandrowicz ’s exquisite illus-

trations fostered pioneering electrophysiological work on these

sense organs which continues today (Macmillan, 2002;

Macmillan and Patullo, 2001; Pilgrim, 1960).

Although most often studied in macruran decapods

(Macmillan, 2002), bilateral pairs of segmentally arranged

muscle receptor organs (MRO) are present in Hoplocarida

(Alexandowicz, 1954) and Syncarida (Wallis, 1995) and, there-

fore, presumed ancestral in Malacostraca. Further investigation

of the MROs that have been described in galatheid squat lob-

sters (Pilgrim, 1960; Wallis et al., 1994) and pagurid species

(Alexandrowicz, 1952; Pilgrim, 1960, 1974), as well as inves-

tigations in other anomurans, are certain to provide insight into

how evolutionary modifications in this array of ancient sense

organs contribute to the distinctive postures and forms of

locomotion in the Anomura (Wallis et al., 1994).

Motor systems - from familiar to novel fonns of posture and

movement. The paired, dorsal, medial giant (MG) and lateral

giant (LG) intemeurons in the nerve cords of macruran species

and hermit crabs were the first neurons in crustacean central

nervous systems to be recognized as re-identifiable neurons

(see references in Bullock and Horridge, 1965); investigations

of their physiology, inter-connections with other neurons, roles

in locomotion, and, more recently, in agonistic behaviours in

crayfish continue to inform us about how crustacean behav-

iours are mediated, as well as about general mechanism of

nervous system function (Edwards et al., 1999; Wine, 1984).

Crayfish’s MG and LG neurons, with associated motor giant

and segmental giant neurons, coordinate the rapid and power-

ful flexions of the abdomen-tailfan called tailflips (Edwards et

al., 1999; Wine, 1984). Anomurans have modified (Paguroidea)

or lost (Galatheoidea, Hippoidea) these giant interneuron

systems (Fig. 1). Only the MG system, including the segmental

and motor giant neurons, is retained, with modifications, in

pagurids to subserve their new mode of escape: rapid with-

drawal into their gastropod shell (Chappie, 1966; Heitler and

Fraser, 1986, 1987; Umbach and Lang, 1981). Some repercus-

sions in the pagurid nervous system of acquiring a hydrostatic

skeleton, asymmetrical abdomen, and use of the last two pairs

of pereopods to transport gastropod shells for shelter have been

investigated (Bent and Chappie, 1977; Chappie, 1966, 1969 a,

b, c, 1973; 1993; Chappie and Hearney, 1976; Herreid and Full,

1986) , but many interesting questions remain, such as the

control of the tailfan’s grip on the shell and of the asymmetric

swimmerets, when present. The partial reversion to tailfan sym-

metry in pagurid species using straight shells (Imafuku and

Ando, 1999) has likely engendered some modifications in the

muscles and reflex control of the “tail” from those in pagurids

hoisting spiraled shells (see Chappie, 1966, 1969b, 1973); are

they reversions to the macruran condition or new permutations

of the asymmetric sensory - motor systems of other pagurids?

The retention of the MG interneurons and related circuitry in

pagurids (also in Thalassinidea: Bullock and Horridge, 1965;

Paul, pers. obs.) illustrates that evolutionarily conserved

neuronal networks can retained the ability to coordinate

movements in the face of substantial alterations in peripheral,

skeleto-muscular systems.

Galatheoidea and Hippoidea have apparently lost both MGs

and LGs (Sillar and Heitler, 1985; Paul, 1991; Wilson and Paul,

1987) . However, both perform repetitive tailflipping, rapid

extensions-flexions of the “tail”, such as used by crayfish for

swimming, and which are presumably mediated by homo-

logues of crayfish’s non-giant circuitry for swimming (this cir-

cuitry is called non-giant, nonG, because neither MGs nor LGs

are involved) (Paul, 1981a, 1991; Sillar and Heitler, 1985;

Wilson and Paul, 1987). Unexpectedly, the two squat lobster

species that have been investigated differ in their complement

of fast flexor motoneurons, although their tailflipping behav-

iours appear to be indistinguishable (Fig. 1). In Galathea

strigosa, the clusters of fast flexor motoneurons are similar to

those in crayfish, including homologues of crayfish’s segmen-

tally repeated motor-giant motoneurons (Fig. 1, hMoG) which

have, however, lost the specialized features associated with

electrical coupling to the giant interneurons and become mor-

phologically similar to other fast flexor motoneurons (Sillar

and Heitler, 1985). Munida quadrispina, by contrast, has not

only lost motor-giant homologues but also the entire cluster of

Dorothy Hayman Paul

anterior contralateral fast flexor motoneurons (Wilson and

Paul, 1987). Since no functional or behavioural correlates of

these neural differences are evident, it appears that evolution-

ary changes in nervous systems during speciation occasionally

occur independently of altered morphology or behaviour. Such

events would leave overtly similar sibling species with

different potential for subsequent neurobehavioural evolution.

Other squat lobsters should be investigated to determine

whether these data are representative of these genera, in which

case they would suggest that Mimida is more derived than

Galathea.

Porcelain crabs (Porcellanidae) flap their small, flat

abdomens rhythmically to swim upside down (Hsueh et al.,

1998) and to stabilize their descent to the bottom after dropping

off vertical surfaces (Paul, pers. obs.). This is presumably a

reduced form of the vigorous swimming movements exhibited

by Galatheidae and crayfish, and therefore homologous to non-

giant tailflipping. Nothing is known about the musculature,

motoneurons, or the central circuitry executing this porcellanid

behaviour, but it is an almost certainty that porcellanids lost

MoG, as have M. quadrispina and the Hippoidea, rather than

transferred them into ordinary fast flexor motoneurons, as

occurred in G. strigosa (hMoG in Fig. 1).

Non-giant tailflipping was also retained in both families of

sand crabs (Hippoidea; Fig. 1). In albuneid species, this is evi-

dent as the tail- “flapping” they use, along with rowing move-

ments of their pereopods, to swim awkwardly upside down -

like porcelain crabs described above - (Paul, 1981a) as well as

to assist the pereopods when digging into sand (Faulkes and

Paul, 1997a, b, 1998). The retention of non-giant tailflipping in

hippid sand crabs is less obvious, because they keep their

abdomen flexed beneath them and beat their highly modified

uropods rapidly both to swim (Paul 1971, 1981a) and assist the

pereopods in digging (Faulkes and Paul, 1997a, b, 1998).

Homologies between individual muscles in sand crabs and

Other decapod species have been confirmed by examination of

their innervations, specifically the locations and morphologies

of the motoneurons innervating them, which are highly con-

served (Paul, 1981b; Paul et al, 1985), but evidence for the

homology of hippids’ swimming-by-uropod- beating and tail-

flipping is indirect but substantial: numerous similarities

between motor patterns and between homologous motoneurons

activating functionally divergent, homologous muscles (Paul,

1981a, b, 1991; Paul et al., 1985; Fig. 1). Direct tests of this

hypothesis will require comparison of the neuronal circuits for

these two behaviours, and little is known about either of them,

other than that both rely on central pattern generation (Paul,

1979; Reichert et al., 1981; see Discussion).

Much of the difference in form between uropod beating and

tailflipping can be accounted for by biomechanical differences,

due to changes in the uropod articulation and the telson-uropod

musculature in hippids (Paul, 1981a, b, 1991; Paul et al., 1985).

However, hippids’ superb adaptation to life in the swash zone

of exposed sandy beaches, where they are tireless swimmers

and champions for speed among burrowing species (Dugan et

al., 2000), required two evolutionary novelties in addition to

rearrangements and modifications of ancestral neural and

muscular traits: a muscle and a stretch receptor. The uropod

return-stroke muscle in the telson, innervated by three

motoneurons (two excitatory, one inhibitory), occurs only in

hippoids (Paul et al., 1985); it is very small in albuneids, but

has become one of the largest muscles in the body of hippids.

Without it, the large return stroke movement of the uropod in

hippids would be impossible (Paul, 1981b; Paul et al., 1985).

This new movement is monitored by a new telson-uropod

stretch receptor that is unique to hippids.

Novel stretch receptors. Telson-uropod stretch receptors (Fig.

1, TUSR) are found only in squat lobsters (Galatheidae) and

sand crabs (Hippoidea) (Maitland et al., 1982; Paul, 1972; Paul

and Wilson, 1994; Wilson and Paul, 1990). They are close and

approximately parallel to the anterior Telson-Uropodalis mus-

cle (= the hippid Dorso-Medial muscle), which is relatively

larger than its homologue in macrurans and occupies the space

in the anterior telson vacated by the loss of the macruran

Anterior Telson muscle (Paul et al., 1985). The sensory neurons

of the TUSRs are unusual because they are monopolar and their

somata are located in the last, sixth abdominal, ganglion of the

ventral nerve cord; i.e., their central morphology, like that of

similar stretch receptors associated with the macruran swim-

merets and macruran and brachyuran pereopods, resembles that

of motoneurons (Bush, 1976). Typical mechanosensory neurons

in arthropods are bi- or multipolar and their cell bodies lie out-

side the central nervous system, close to the periphery. Telson-

uropod stretch receptors apparently evolved twice, first in the

galatheoid-hippoid common ancestor and again in hippids.

Alternatively, the first telson-uropod stretch receptor could

have evolved prior to the paguroid divergence and was subse-

quently lost in hermit crabs. The TUSRs in Galathea strigosa,

Munida quadrispina, and Blepharipoda occidentalis (Maitland

et al., 1982; Paul and Wilson, 1994) and Lepidopa californica

(Paul, pers. obs.) are morphologically and physiologically very

similar and presumed homologues. The central location and

morphology of their sensory neurons are similar, and these

neurons generate conventional action potentials when their

peripheral dendrites are stretched by elevation of the uropod

(Maitland et al., 1982; Paul and Wilson, 1994). No comparable

proprioceptors monitoring movement of the basal joint of the

uropod have been found in any macruran or pagurid, which

suggests that the greater freedom of movement of the uropods

in galatheoids and hippoids (Paul et al., 1985) may have made

the evolution of a proprioceptor to monitor whole limb move-

ment advantageous. The abdomen-propodite chordotonal organ

in the uropod of crayfish originates from the third nerve of the

sixth abdominal ganglion as this nerve enters the uropod (Field

et al., 1990). Since its proximal attachment is flexible, this

receptor would be unsuited to monitoring movement across the

much more mobile articulation of the uropod with segment 6

in squat lobsters and sand crabs (Paul et al., 1985), and no

anomuran homologue of this crayfish stretch receptor has been

found.

The hippid telson-uropod stretch receptor (examined in

detail in Emerita analoga and E. talpoida: Paul, 1972; Paul and

Bruner, 1999; Wilson and Paul, 1990, and anatomically identi-

cal in Hippa pacifica and E. austroafricanus: Paul, pers. obs.)

is in a comparable position to the TUSRs in the tailflipping

Neurobiology of the Anomura

anomurans and it, too, responds to uropod elevation and, in par-

ticular, the uropod remotion brought about by contraction of the

return-stroke muscle, unique to hippoids and much enlarged in

Hippidae, as described above. However, the different positions

of the somata and projections of the neurites of the sensory

neurons in the sixth abdominal ganglion are strong evidence

that the TUSRs in hippids and the tailflipping anomurans

(Albuneidae, Galatheidae) are not homologues (Paul and

Wilson, 1994). The hippid sensory neurons are also physiolog-

ically dissimilar: they are nonspiking, that is, they are incapable

of generating action potentials, as can the galatheids and

albuneid receptors, but instead transmit afferent signals in the

form of graded depolarizations which mimic in form and

amplitude the stretch applied to the receptor strand (Paul and

Bruner, 1999). Apparently the transformation of the stem

(albuneid-like?) hippoid tailfan into the extraordinary tailfan of

hippids (Paul et al., 1985) included the replacement of the

ancestral, spiking telson-uropod stretch receptor by a new one

that ostensibly serves the same function, that is, sensing eleva-

tion of the uropod and activating resistance reflexes in homol-

ogous uropod muscles. The caveat here, however, is that the

functional details, behavioural roles, and synaptic connections

are still poorly understood for any of these receptors.

Nevertheless, it appears that during hippid evolution, the spik-

ing sensory neurons of the receptor in their tailflipping ances-

tors were not converted to nonspiking neurons, as was initially

assumed (Bush, 1976; Paul, 1991). Paul and Bruner (1999)

discuss the hypothesis that evolution of the physiological prop-

erties of these nonspiking sensory neurons may have been

determined by their interconnections with nonspiking cells in

the central pattern generator for swimming. Observations from

two lines of research in other reptantians suggest this hypo-

thesis. One is that certain swimmeret motoneurons are

coupled to swimmeret interneurons in their hemiganglion

(Heitler, 1978; Paul and Mulloney, 1985). The second is that

nonspiking stretch receptors morphologically similar to those

in hippids are interconnected with the pattern generators for the

limb whose movement they monitor (thoracic walking legs:

Sillar and Skorupski, 1986; abdominal swimmerets: Paul,

1989b). Whatever the adaptive drive for the unusual physio-

logical properties of the hippids’ sensory neurons, the repeated

appearance of telson-uropod stretch receptors in Anomura

demonstrates that new types of neurons can be added to

inherited sensory-motor systems in the course of behavioural

evolution.

Modular nei~vous systems and central pattern generators. The

evolutionary potential of segmental body plans has long been

recognized, and the ontogenetic mechanisms by which seg-

mental characters may be selectively lost, added, moved, or

modified are becoming apparent through the applications of

genetic and molecular techniques to a variety of taxa amenable

to such research (Giribet et al., 2001). Unfortunately, ano-

murans, indeed most crustaceans, are not among the latter, pri-

marily due to their complex life cycles. But fortunately, their

segmental nervous systems are amenable to detailed mor-

phological and physiological analyses, which allow detailed

comparative investigation of the neural substrates for their

divergent behaviours. Much of this material has been recently

reviewed (Paul, 1991; Paul et al., 2002), so here I will highlight

a few of the issues and refer readers to the research publications

for substantive details and further discussion.

Neural networks driving repetitive movements such as

underly locomotion, respiration, chewing, and other rhythmic

behaviours have at then* core central pattern generators (pace-

maker neurons or small assemblies of neurons). The best

known are the central pattern generators of the stomatogastric

nervous system in crustaceans (Harris- Warrick et al., 1992).

The stomatogastric system is clearly an ancient network that

has been largely conserved morphologically. Variations in

physiological details (synaptic properties, neuromodulators,

etc.) have been uncovered, but not extensively investigated in

the context of anomuran phytogeny or in relation to the ecolo-

gy and habits of different species (Katz and Harris- Warrick,

1999). Paired segmental pattern generating modules control the

limbs of crustaceans, each limb being under the control of the

adjacent hemiganglionic center (Mulloney and Hall, 2000

Murchison et al., 1993). Much less is known about cellular

composition and network operations of these hemigangionic

centers than about the stomatogastric system. They clearly dif-

fer in cellular composition - local intemeurons, many nonspik-

ing, form the core of the motor pattern-generating network,

rather than motoneurons, as in the stomatogastric nervous

system, nevertheless largely similar mechanisms appear to be

used (e.g. graded potential, reciprocal inhibition, multiplicities

of ion channels with differing kinetics). Testable hypotheses

about species dilferences can be formulated, therefore, even

without complete knowledge of the particular pattern

generators in question.

Divergences in pereopod use in posture and locomotion in

galatheids and hippoids, accompanying modifications in tho-

racic segmental morphology and endophragmal skeleton, have

been correlated with specific alterations in musculature,

motoneurons, and motor patterns in various studies (Antonsen

and Paul, 2000; Faulkes and Paul, 1997a, b, 1998). Each seg-

mental ganglion in the ventral nerve cord of crustaceans con-

tains a pair of central pattern generating circuits (one/limb)

(Mulloney and Hall, 2000; Murchison et al., 1993).

Interneuronal connections between hemiganglionic centers

allow bilateral and longitudinal coordination of motor activity

produced by these hemiganglionic centers (Namba and

Mulloney, 1999). The evolutionary potential of this functional-

ly flexible aiTangement has been exploited extensively in the

evolution of the hippoid digging behaviour, a mosaic derived

by amalgamation of two disparate forms of ancestral locomo-

tion, walking and non-giant tailflipping (Faulkes and Paul,

1997a, b, 1998). Later divergences of phase couplings among

the digging legs and between the legs and “tail” accompanied

divergence of the two sand crab families, Albuneidae and

Hippidae (Faulkes and Paul, 1997a, b, 1998; Fig. 1).

Comparative neurobiological studies of other anomuran

behaviours are likely to provide inferences about how modular

systems of neurons function and evolve, as well as illuminating

the biology of the Anomura per se. For example, the modified

posture and gait of hermit crabs, associated with their

asymmetrical abdomen and transport of gastropod shells into

Dorothy Hayman Paul

which they “retreat” rapidly (Chappie, 1966, 1973; Herreid and

Full, 1986), must have entailed changes in pereopod neuro-

musculature and its central control. These remain to be

explored. Snow’s (1975a, b) study of antennular flicking in

pagurids could also be profitably pursued. One may suppose

that flicking is underlain by hemiganglionic pattern-generating

circuitry similar (serially homologous) to that controlling

pleopods and pereopods (Murchison et ah, 1993).

The basal musculature of crustacean limbs is often

extremely complex and may include muscles with multiple

heads and specialized functions. Divergence in segmentally

repeated neuromuscular elements between segments in one

species and in the same segment in different species clearly

contributes to the postural and locomotory peculiarities of

individual species. This is illustrated by the study of Antonsen

and Paul (2000) on the leg depressor muscle in M. quadrispina,

which highlights the need for more, detailed analyses of the

functional morphology and innervation of such muscles,

including the central structure of their motoneurons, in

order to understand how the central neural networks (and

neuromodulators, see below) produce species characteristic

behaviours.

Neuromodulation and social behaviours. Hormones and neuro-

modulators regulate the expression of the moment-to-moment

behaviours produced by sensory-motor systems emphasized in

this review. They confer functional, as well as evolutionary,

flexibility on neurobehavioural networks (Katz and Harris-

Warrick, 1999). The involvement of serotonin and octopamine

in agonistic behaviours of crayfish and other crustaceans is well

known (Huber et al., 1997), but an understanding of the sites

and mechanisms of action of these biogenic amines is very

incomplete (Panksepp and Huber, 2002). Unlike crayfish,

Munida quadrispina (Galatheidae) neither form social hierar-

chies nor fight, although during agonistic encounters, they per-

form rather stereotyped gestures and behaviours that resemble

those performed by dominant and subordinate crayfish

(Antonsen and Paul, 1997). Nevertheless, as in crayfish, injec-

tion of controlled doses of serotonin or octopamine into the

hemolymph of M. quadrispina induces, respectively, “domi-

nant” or “subordinate” gestures and behaviours in isolated ani-

mals (are they displaying to a phantom conspecific?). Most

remarkably, serotonin-injected animals engage in full-blown

fights when paired with an un-injected individual (which tries,

unsuccessfully unless rescued by the experimenter, to retreat)

(Antonsen and Paul, 1997). Evidently M. quadrispina have not

lost the “fight center”, but the “interest in fighting”, perhaps

due to the loss of a particular synapse or expression of a sero-

tonin (or other) receptor at some critical point in the circuitry

involved in controlling agonistic behaviour (Antonsen and

Paul, 1997). Information on the social behaviours of other

galatheid genera is largely lacking, and circumspection should

be used in interpreting differences in cheliped length, or other

morphological characters, as indicators of a species’ agonistic

behaviour (Creasey et al., 2000). Comparisons of immuno-

cytochemical maps of serotonergic and octopaminergic

neurons reveal both striking similarities and discrete differ-

ences between these systems in M. quadrispina and crayfish.

demonstrating that conserved and modified components of

neuro-modulatory networks can be identified (Antonsen and

Paul, 2001, 2002). Much more research is needed to clarify the

functional organization of these aminergic systems and their

interconnections with the rest of the nervous system in

M. quadrispina, and other anomurans should be similarly

investigated. The variants in social behaviour evident among

anomuran species constitute a largely untapped source of

information about mechanisms of neuromodulation and their

evolution.

Discussion

By placing the neural characters discussed above on a partial

phylogeny of the Reptantia which includes anomurans’ closest

relatives (Fig. 1), several suppositions about neurobehavioral

evolution in Anomura can be drawn. This exercise also both

highlights under-studied groups and suggests experimentally

testable hypotheses about specific neuronal systems in partic-

ular species. The seven characters listed at the base, with the

possible exception of nonG (the circuitry for repetitive tailflip-

ping that does not involve either sets of giant interneurons), are

ubiquitous among macruran decapod groups, including natant-

ian taxa (Paul, 1989a; Paul et al., 1985), although they are most

fully described in astacidean species, primarily of crayfish

(Wine, 1984). These characters are not equivalent in that some

are individual neurons, whereas others are neuronal systems

identified by their mediation of specific behaviours; few

re-identifiable neurons in the latter have been described, but as

they become known, they will constitute additional characters

that will be useful for analysis of neuro-behavioural evolution

or in phylogenetic reconstructions. The losses preceding

and accompanying the divergence of the anomuran groups

included major elements of macrurans’ startle/escape systems

(one or both of the giant interneurons - see Fig. 1 footnote 1),

as well as certain components of the massive tail neuromuscu-

lature, and were seminal for the anomuran radiation (Paul et al.,

1985). In particular, the demise of both LG and MG interneu-

rons in Galatheoidea and Hippoidea would have reduced con-

straints against modification of tailfan form, neuromusculature,

and central motor systems controlling locomotion that were

present in their macruran ancestors (Paul et al. 1985, 2002).

This permitted the diversification of morphology and behaviour

so evident in galatheoid and hippoid anomurans.

The number of evolutionary modifications of retained

neural characters (hatched boxes in Fig. 1) is clearly a gross

underestimation, because, as explained above, most are func-

tional neural networks (e.g., the nonG circuitry for swimming,

the CPGs, central pattern generators, producing rhythmic limb

movements) in which an unknown number of neuronal and

synaptic changes are likely to have occurred, but remain to be

identified. One additional change in tailfan neuromusculature

not yet mentioned or included in Fig, 1 was pivotal to the

evolution of the hippid sand crabs’ novel mode of swimming by

beating the uropods. This was the conversion of an axial

muscle into an appendage muscle by changing its insertion; in

all tailflipping species (including galatheids and albuneids), the

PTF (posterior telson flexor) muscle is the terminal member of

Neurobiology of the Anomura

the concatenated series of fast flexor muscles that mediate the

abdominal flexions or power strokes in tailflips (Dumont and

Wine, 1987). The PTF homologue in hippid sand crabs inserts

on the ventral rim of the uropod coxa, adjacent to the insertion

of the uropod power-stroke muscle (homologue of the macru-

ran posterior telson-uropodalis muscle), so that, rather than

flexing the telson on the abdomen, it assists in uropod promo-

tion during uropod beating (Paul et ak, 1985). The homology

between components of the power-stroke neuromusculature

(muscles and motoneurons) for uropod beating and tailflipping

provides substantive evidence for the homology of the neural

circuitries for swimming by uropod beating and tailflipping

(Fig. 1: nonG-» uropod beating). This hypothesis originated

with the observation that at high frequencies of uropod beating,

a small extension of the anterior abdomen occurs with each

uropod return stroke (= extension phase of tailflipping; Paul,

1971). Further support for the hypothesis of homology of these

dissimilar behaviours is that rhythmic bursting of the motoneu-

rons innervating the PTF homologue in hippids is very promi-

nent in the uropod motor pattern generated by isolated nerve

cords of Emerita analoga (Paul, 1979); i.e., uropod beating,

like nonG tailflipping (Reichert et al. 1981), is organized by a

central pattern-generating circuit that does not require sensory

feedback to sustain its generation of alternating activity in

power- stroke (flexion) and return- stroke (extension) moto-

neurons. Regardless of the validity of this hypothesis, the

evolution of hippids’ novel mode of swimming combined

the considerable evolutionary flexibility in behaviour permis-

sible by peripheral changes in skeleto-musculature with

the evolutionary potential derived from crustaceans’ com-

plex neuromusculature (Paul et al., 1985; Antonsen and Paul,

2000).

The extent and nature of alterations in inherited networks

into which new neural elements have been incorporated (Fig. 1,

black boxes in anomuran portion of the tree) are as yet unex-

plored. Some may have been minimal: the uropod return-stroke

muscle (RSM) in the hippoid telson is a new muscle that is

functionally and probably evolutionarily related to the uropod

remoter muscle in the sixth abdominal segment, the latter being

common to decapods with tailfans (Paul, 1981b; Paul et al.,

1985). Thus, the appearance of the hippoid RSM may be an

example of evolution of neuromusculature by division or dupli-

cation of ancestral neuromuscular elements (Antonsen and

Paul, 2000). Since the actions of the return-stroke and remoter

muscles are synergistic, uropod remotion, little central change

may have occurred. The addition of the telson-uropod stretch

receptors (Fig. 1, TUSRs), on the other hand, is expected to

have necessitated adjustments in the sensory-motor circuitry in

the terminal ganglion, and perhaps more anteriorly. The

replacement of the spiking TUSR by a nonspiking TUSR in the

evolution of the Hippidae, discussed above, is surprising. Does

it mean that seniority plays a role in neural evolution? Neurons

“recently” added to neuronal circuits could be more expendable

than more ancient members of circuits, because they are not as

highly interconnected, something which may happen gradually

over time. This would restrain the rate at which structural

changes in neuronal networks appear over evolutionary time.

Other neural characters besides those included in Fig. 1

confer evolutionary flexibility on neurobehavioural networks.

In particular, the complexity and subtlety of neuromodulatory

actions at many central and peripheral levels is only beginning

to be understood (Katz and Harris- Warrick, 1999; Panksepp

and Huber, 2002). The potential for change at discrete loci in a

neuromodulatory system to dramatically alter a species

behavior is exemplified by the loss in M. quadrispina of “the

will” but not “the means” to fight conspecifics (Antonsen and

Paul (1997). The diverse behaviours, generally smaller number

of neurons, and, in some cases, simplifications of circuitry

clearly make anomurans valuable subjects for many kinds of

neurobiological research. Comparative investigations of their

nervous systems are beginning to reveal the multiple levels at

which neural evolution occurs.

Acknowledgements

Thanks to Adrian Wenner, University of California Santa

Barbara, for the specimens of Hippa pacifica and Emerita aus-

troafricanus. The author’s research is supported by grant

#8183-00 from the Natural Science and Engineering Research

Council of Canada.

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Memoirs of Museum Victoria 60(1): 13-26 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

Terrestrial adaptations in the Anomura (Crustacea: Decapoda)

Peter Greenaway

School of Biological Science, University of New South Wales, Sydney 2052, Australia (p.greenaway@unsw.edu.au)

Abstract Greenaway, P. 2003. Terrestrial adaptations in the Anomura (Crustacea; Decapoda). In: Lemaitre, R., and Tudge, C.C.

(eds). Biology of the Anomura. Proceedings of a symposium at the Fifth International Crustacean Congress, Melbourne,

Australia, 9-13 July 2001. Memoirs of Museum Victoria 60(1); 13-26.

In this review, morphologieal, physiologieal and behavioural adaptations to life on land by anomurans are considered.

The most terrestrial group are the Coenobitidae and these have developed terrestrial adaptations broadly similar to those

of the terrestrial braehyurans. The coenobitids have developed two evolutionary, terrestrial lines. Coenobita spp. retain

the protective gastropod shell and this has placed a set of constraints on morphological, physiological and behavioural

development particularly in regard to gas exchange, osmoregulation and excretion. Birgus do not carry molluscan shells

after the juvenile stages and, freed from its constraints, reach larger size and have developed terrestrial adaptations that

closely parallel those of the brachyuran land crabs. Shell retention by Coenobita has resulted in development of novel

abdominal gas exchange organs whilst purine excretion by B. latro seems to be unique amongst land crabs. Crabs of both

genera are well adapted to life on land in terms of sensory, respiratory, excretory and osmoregulatory functions and they

can also moult, mate and lay eggs effectively on land. Several species have the functional ability to live in a range of

habitats from rainforest to arid scrubland but their penetration of these habitats is limited to small islands or to a narrow

coastal strip. This is probably due to the retention of pelagic larval stages and to the lack of molluscan shells of suitable

dimensions and strength in inland situations, which restrict the range to a manageable distanee from the sea.

Keywords Cmstacea, Anomura, terrestrial adaptations, Coenobita, Birgus

Introduction

On land, the Anomura are represented principally by the

Coenobitidae which include 15 species of shell-carrying terres-

trial hermit-crabs {Coenobita) and the robber or coconut crab

Birgus latro (Linnaeus, 1767), the largest terrestrial arthropod

(to 3 kg). Although there are relatively few species of

Coenobita, individuals are numerous in tropical and subtropical

maritime regions particularly supralittoral areas and small

islands, although some penetrate further inland. Certain species

are restricted to beaches (e.g. C. perlatus (H. Milne Edwards,

1837), C. scaevola (Forskal 1775), C. spinosus (H. Milne

Edwards, 1837), C. cavipes (Stimpson, 1838) while several

other species may penetrate long distances inland, e.g. C.

clypeatus (Herbst, 1791) on Curasao, C. rubescens (Greeff) and

C. brevimanus (Dana, 1852) in rainforest, C. compressus (H.

Milne Edwards) (de Wilde; 1973; Burggren and McMahon,

1988). Coenobita rugosus (H. Milne Edwards, 1837) may live

on the beach or penetrate inland in situations where fresh water

is available (Yamaguchi, 1938; Vannini, 1976). The closely

related Diogenidae also show terrestrial tendencies but typic-

ally occupy intertidal and mangrove habitats, e.g. Diogenes,

Calcinus, Clibanarius. There are also a number of intertidal

amphibious species in the Porcellanidae, that tolerate emersion

but are not normally active out of water e.g. Petrolisthes.

The adoption of terrestrial habits seems to be a compara-

tively recent evolutionary development (as with terrestrial

braehyurans) and the oldest coenobitid fossils are

from the Lower Miocene (Table 1). The coenobitid line of

evolution is entirely terrestrial apart from the planktonic larval

stages. Successful transition from aquatic to terrestrial life

requires a number of physiological adaptations some of

which are immediately essential for survival out of water while

others are less immediately important and may be developed

progressively over a much longer period of adaptation

(Table 2).

The reader is also referred to Burggren and McMahon

(1988) and reviews in “The Compleat Crab” (Mantel, 1992) for

further literature on certain aspects of terrestrial adaptations of

anomurans.

Gas exchange

Anomurans have developed a number of different adaptations

for aerial gas exchange some of which are convergently similar

to those described for braehyurans (Burggren, 1988; McMahon

and Greenaway 1999) and others, such as the novel abdominal

respiratory organ, that are unique and have developed as a

response to living in a mollusc shell.

Peter Greenaway

Table 1. Origin of teiTestrial anomurans. Tj are aquatic and can survive

brief emersion with some limited degree of terrestrial activity. T 2 are

amphibious and voluntarily active out of water for substantial periods

e.g. air-breathing intertidal crustaceans. T 3 aie amphibious species res-

ident, and principally active, on land but which require regular immer-

sion in standing water (often in burrows) and water is required for

breeding (e.g. supralittoral species and amphibious freshwater forms).

T 4 are terrestrial species which do not require immersion

in standing water but which need periodic access to water for

reproduction (from Greenaway, 1999). Fossil data from Glaessner

(1969).

Infraorder Anomura

Terrestriality

Earliest Fossil

Superfamily Coenobitoidea

Family Coenobitidae

T 3 -T 4

Lower Miocene

Family Diogenidae

T 1 -T 3

Upper Cretaceous

Superfamily Galatheoidea

Family Porcellanidae

Upper Cretaceous

The gill number and area in brachyuran crabs decreases as

terrestrialness increases (e.g. McMahon and Burggren 1988;

Greenaway, 1999) and this trend is also evident in the phyllo-

branch gills of the Coenobitidae. Birgus latro has the smallest

weight specific gill area measured for any terrestrial decapod

(area (mm2) = 152.1 x mass (g)-^^^) (Greenaway, 1999) and

they play little role in oxygen uptake (Greenaway et ah, 1988).

Instead, oxygen uptake by B. latro occurs across the large,

evaginated, branchiostegal lungs (Cameron and Mecklenburg,

1973; Greenaway et al., 1988) supplied with venous blood from

the ventral sinuses (Semper, 1878; Harms 1932), a develop-

ment parallel to that seen in the larger terrestrial brachyurans.

The cuticle and epidermis making up the lung membrane are

extremely attenuated (Harms, 1932; Storch and Welsch, 1984)

and blood is directed to the exchange surface by connective

tissue partitions similar in organisation to those described for

brachyuran land crabs (e.g. Farrelly and Greenaway, 1993).

Evidence gained from direct measurements of pre- and post-

branchial CO 2 , from the distribution of carbonic anhydrase and

from experimental gill ablation is supportive of a strong

continued role of the gills in CO 2 elimination. However, this is

supplemented by pulmonary excretion and during exercise CO 2

elimination is equally partitioned between the two organs

(Smatresk and Cameron, 1981; Greenaway et al., 1988; Morris

and Greenaway, 1990).

The gills of Coenobita are also markedly reduced (Harms,

1932) and weight specific gill area of C. scaevola (expressed

per unit live weight) is of the same order as for B. latro

(Achituv and Ziskind, 1985). However, the mollusc shells in

which hermit crabs live physically constrain development of

branchiostegal lungs. Consequently these lungs are small, lack

surface amplification, have relatively long blood/gas diffusion

distances and a poorly organised blood supply compared to

lungs of B. latro (Harms, 1932; C.A. Farrelly, pers. comm.).

With gills reduced and lung development restricted, the coeno-

bitids have developed a third site for aerial gas exchange, the

dorsal surface of the abdomen. The attenuated cuticle and epi-

dermal cells covering this region form a thin respiratory mem-

brane in contact with the air carried in the upper part of the mol-

lusc shell. The membrane receives a rich supply of venous

blood via a highly organised network of respiratory vessels and

oxygenated blood passes forwards to the pericardium where it

mixes with blood returned from the gills and branchiostegites

(Bouvier, 1890; Harms, 1932; Greenaway, 1999; Farrelly and

Greenaway, 2001). It is not clear how the air in the shell above

this respiratory organ is renewed but the carapace movements

described by a number of authors (e.g. McMahon and

Burggren, 1979) might drive convective exchange of shell air.

The ventral surface of the abdomen is frequently bathed in shell

water and is not modified for aerial gas exchange. The shell

water could potentially act as a dump for respiratory CO 2 but as

its CO 2 capacity is small this function will be limited.

A fourth type of gas exchange organ has developed in

certain evolutionary lines of porcelain crabs (Petrolisthes).

These species have oval patches of very thin cuticle on the

meral joints of their walking legs similar to the “gas windows”

described in certain small burrowing, intertidal brachyurans

(Maitland, 1986). At least in larger species of Petrolisthes, these

Table 2. The requirement for physiological and behavioural changes on emergence from water. Tj - T 4 as in Table 1 ; T 5 are fully terrestrial species

able to conduct all biological activities on land (Greenaway, 1999).

Physiological function Immediate requirement for physiological or morphological Grade at which adaptation is

adaptation on emersion? essential

Oxygen uptake

Yes, morphological modifications required immediately

CO 2 output

Yes, required immediately

Salt regulation

No, if water is regularly available for immersion

T 3 ^

Evaporative water loss

No, if water is available in microhabitat as behavioural regulation will suffice

Nitrogen excretion

No, if emersion periods are relatively brief

Temperature regulation

No, temperature can be regulated behaviourally if water or shelter available

Sensory reception

Sound - not immediate

Photo - immediate

Chemo - Loss of aquatic chemoreception compensated by vision

T2-3

Locomotion and support

No, pre-adapted to support on land or utilise support of mollusc shell

Moulting

No, not if animal can moult in water

Reproduction

Yes, commonly needs at least behavioural changes and often some morphological

and physiological adaptation

Ti-5

Terrestrial adaptations in Anomura

play a demonstrable role in aerial gas exchange, particularly at

higher temperatures, and they may allow the animals to remain

aerobic during emersion at low tide (Stillman and Somero,

1996; Stillman, 2000). The selective pressures favouring devel-

opment of gas windows have not been clearly identified. In

brachyurans they are associated with small body size and bur-

rowing habits that may favour selection for external gas

exchange sites rather than bulky lungs (Maitland, 1986). The

extreme flattening of the carapace of Petrolisthes, which allows

exploitation of shallow cavities beneath littoral rocks and

stones, may place similar constraints on lung development in

porcellanids.

Ventilation of the gills and lungs of coenobitids is effected

by the scaphognathites. In B. latro the ventilation rate is deter-

mined by alteration of the frequency of beating of the scaphog-

nathites and stroke volume remains more or less constant over

the frequency range. Control of ventilation is primarily by CO2

and scaphognathite frequency is linearly related to the PCO2 of

the inspired am There is also a secondary stimulation in

response to low partial pressures of oxygen (<90 Torr) in

inspired air (Cameron and Mecklenburg, 1973; Smatresk and

Cameron, 1981) so that the pattern of control of breathing is

similar to that of terrestrial animals generally. By contrast

ventilatory response of C. clypeatus to PCO2 is low, even at

high partial pressures, and the primary control of ventilation is

by PO2 (McMahon and Burggren, 1979), a scenario similar to

that in water breathing animals. These authors suggested that

Coenobita might retain aquatic respiratory patterns by cir-

culation of shell water over the gills but there are no behav-

ioural or physiological data that support this. The animals will

commonly encounter elevated PCO2 both while retracted into

the shell for long periods and when buried in the sand during

diurnal periods of inactivity (Vannini, 1975b; Achituv and

Ziskind, 1985). An alternate explanation for their insensitivity

to CO2 may be that it is an adaptation to high environmental

CO2 (common in burrow-dwelling animals) rather than reten-

tion of “aquatic” gas exchange. Vertical movements of the cara-

pace have been described in B. latro and in Coenobita but are

not believed to contribute in any systematic or significant

manner to gas exchange by gills or lungs, which are well ven-

tilated by the scaphognathites (Borradaile, 1903; Harms, 1932;

Cameron and Mecklenburg, 1973; McMahon and Burggren,

1979). The enhanced frequency of carapace movements during

hypoxia and hypercapnia, reported in C. clypeatus, may, how-

ever, be concerned with ventilation of the abdominal respu-

atory organ. In resting animals ventilation is not continuous,

particularly in Coenobita, and given the high oxygen content

and diffusion rate of oxygen in air, diffusion may provide ade-

quate delivery of oxygen to the respiratory surface between

bouts of ventilation.

The coenobitids have developed a number of features that

are characteristic of terrestrial air-breathers, elevated partial

pressure of CO2 (PCO2), high bicarbonate levels and carbon

dioxide-based ventilatory control (in B. latro) although oxygen

affinity and arterial oxygen tensions are not obviously different

from those of aquatic decapods.

About 90% of oxygen transported by the blood of coeno-

bitids is carried by haemocyanin with only around 10% in

simple solution (Wheatly et al., 1986; Greenaway et al., 1988).

Oxygen capacity is at the upper end of the range for decapod

crustaceans (1.85 mmol.L-i in B. latro, 1.51 mmol.L-i in

C. compressus). The respiratory pigments of coenobitids have

oxygen affinities that lie in the midrange of values for aquatic

decapods; P50 = 12-19 Torr in resting and exercised Coenobita

and 13.6 Torr at 30 C in resting B. latro (Morris and Bridges,

1986; Morris et al., 1988). The oxygen tension (PO2) of oxy-

genated (arterial) blood of resting crabs reflects this moderate

affinity; B. latro, 44 Torr, C. compressus 14 Torr. Arterial PO2

of B. latro falls during exhausting exercise but in C. compres-

sus it doubles whilst venous PO2 remains unchanged. The

oxygen affinity of the haemocyanin of B. latro exhibits a large

Bohr shift between pH 8-7.3 and a sharply decreased response

below this pH range. This facilitates oxygen delivery during

exercise but ensures that oxygen loading is not compromised at

the lower pH values engendered by severe exercise (Wheatly et

al., 1986; Greenaway et al., 1988). In B. latro, the pigment is

highly and uniformly sensitive to temperature over a wide

range (Morris et al., 1988) but as the species normally lives in

stenothermal tropical forests the affinity is unlikely to be

adversely affected by temperature. In Coenobita, haemocyanin

is largely insensitive to temperature within its preferred range

(25-30°C) although sensitive at higher and lower temperatures

(Morris and Bridges, 1986). Most species of Coenobita occupy

more exposed habitats than B. latro, and experience a wider

range of temperature, so that it is advantageous to have consis-

tent oxygen affinity over their normal temperature range for

activity. The haemocyanins of coenobitids are insensitive to

the usual chemical modulators of oxygen affinity utilised by

aquatic decapods (lactate, urate, Mg2+) and the animals rely

more on mechanical means (ventilation and perfusion) to

modulate oxygen delivery. Birgus latro can increase ventilation

>5 in exercise (Smatresk and Cameron, 1981; Greenaway et

al, 1988).

Oxygen consumption (MO2) of terrestrial coenobitids is

within the range for other terrestrial crabs (McMahon and

Burggren, 1988) and oxygen consumption (MO2) increases

with temperature (Qjo 2.6-2.7 in C. clypeatus and C. rugosus)

(Burggren and McMalion, 1981). Oxygen delivery keeps pace

with elevated metabolism due to the temperature sensitivity of

haemocyanin, elevation of arterial PO2 and modulation of

ventilation and perfusion (McMahon and Burggren, 1988). The

MO2 can be elevated 3.4 fold over resting levels in C. com-

pressus (Wheatly et al., 1985). The coenobitids appear to be

specialised for endurance locomotion and on treadmills

C. compressus voluntarily maintains walking speeds of

0.02-0.03 km.h-i for periods as long as 5h and distances up to

150 m. Respiratory and circulatory adjustments to exercise are

complete within 30 min of the onset of exercise and thereafter

activity is aerobic with no accumulation of lactate (Wheatly et

al., 1985). On firm substrates in the field, sustained aerobic

exercise at speeds of 0.23 km.h-i (max. 0.4 km.h-i) is also

common (Vannini, 1976; Herreid and Full 1986a,b). B. latro

too, can cover long distances (Greenaway, 2001). The coen-

obitids are less able to sustain high levels of exercise and

B. latro rapidly becomes refractory when high levels of exer-

cise are enforced. When threatened in the field, animals may

Peter Greenaway

“crouch” (Helfman, 1977a) or move rapidly for just long

enough to back into crevices or climb trees and they seldom

“run” unless caught in the open. Coenobita retreat into their

shells when threatened rather than attempting to escape but

C. variabilis and C. compressus will often run and are known

to abandon their shells when pursued (A.W. Harvey, pers.

comm.). The shell carried by hermit crabs doubles the meta-

bolic cost of locomotion at slow walking speeds but this cost

falls as speed increases and is -1.3 the shell-less rate when

higher speeds are maintained (Herreid and Full, 1986b).

Salt and water balance

Salt and water regulation of land crabs have been reviewed by

Greenaway (1988) and Wolcott (1992) and the reader is

referred to these papers for details of earlier work.

Water gain. The mechanism of water uptake is related to the

habitat and osmoregulatory practices of species and individ-

uals. The more terrestrial anomurans avoid immersion and

utilise fresh water from pools, rainwater, dew and damp sub-

strates. The water is taken up by the chelae and passed to the

densely setose third maxillipeds (Vannini, 1975b; Greenaway,

1988) from which it may be then ingested or passed to the

reservoir of shell water via the branchial chambers (de Wilde,

1973). Beach-dwelling coenobitids drink seawater or extract it

from damp sand and often immerse themselves to flush the

shell. Coenobita rugosus in Somalia make use of fresh water

from damp sand following rain but in dry weather migrate

nightly to the beach from dry foraging areas in sand dunes in

order to access damp sand in the intertidal zone. C. clypeatus is

reported to ingest damp, friable limestone for its water content

(de Wilde, 1973).

Water requirements. A few quantitative studies have been made

of water usage by terrestrial anomurans but most have been lab-

oratory studies in which the conditions of measurement may

not reflect field requirements. Water usage in the laboratory by

B. latro is 16-20 mL.kg-i.d-i (Greenaway et ah, 1990) but in

the field rates are much higher (-48 mL.kg-hd-i) and this has

also been reported for brachyurans (Greenaway, 1994; 2001).

Drinking by shelled hermits in the laboratory has been

measured (de Wilde, 1973), but the data are not in a format that

facilitate comparison and fluid ingested may be partitioned

between the gut and shell water making it difficult to distin-

guish between turnovers of body and shell water. Drinking

rates of coenobitids increase rapidly with the salinity of the

drinking water (de Wilde, 1973; Greenaway et al., 1990) as a

result of the inability of the crabs to produce excretory fluid

that is significantly hyperosmotic to the haemolymph. Thus

when saline water is provided for drinking, intake must be con-

siderably enhanced, as much of the volume gained is needed to

excrete the salt load and the net gain of pure water, required to

replace evaporative loss, is small. Tolerance of saline water is

thus critically dependent on the rate of evaporative loss (Taylor

et al., 1993).

Water requirement is to a large extent a function of evapo-

rative water loss which in turn depends on cuticular permeab-

ility and crab behaviour. Intertidal hermit crabs (Clibanarius)

have high evaporative water loss rates which increase further

(x3) if the animals are removed from their shells (Herreid,

1969a). In Coenobita scaevola removal from the shell

increased evaporative loss by only 11% (Achituv and Ziskind,

1985) and the terrestrial hermits may have a lower permeabili-

ty. Tolerance to water loss is reportedly high (50% body water)

in the intertidal Clibanarius vittatus (Young, 1978) but lower

(30%) in C. clypeatus (de Wilde, 1973) and Petrolisthes elon-

gatus (H. Milne Edwards, 1837) (20.8%) (Jones and

Greenwood, 1982).

Water reserves. The water carried in the shell of terrestrial

hermit crabs can amount to 30-50% of the wet weight of the

animal (de Wilde, 1973). This water has an osmotic concen-

tration similar to that of the blood and is used as a reservoir to

replace evaporative losses and may be added to or replaced

during drinking or immersion. Coenobita spp. also have two

distensible sacs of the abdominal wall which expand after

drinking and can accommodate considerable increase in

volume of the haemolymph (de Wilde, 1973).

Behavioural regulation of water loss. Like many terrestrial

animals, coenobitids modify their behaviour to minimise evap-

orative water loss, particularly under hot and dry conditions,

and they characteristically are most active in the higher night-

time humidities. They detect and orient to water vapour

(Vannini and Ferretti, 1997) and in experimental humidity

gradients, C. clypeatus selects areas of maximum humidity

whilst avoiding wet substrates (de Wilde, 1973). Although

coenobitid species are primarily nocturnal, sudden rises in day-

time humidity, or a brief shower, often initiate diurnal activity

(Ball, 1972; de Wilde, 1973; Vannini, 1976; Alexander, 1979).

Osmoregulation. Anomurans are separable, on the basis of their

osmoregulatory behaviour, into amphibious, intertidal forms,

such as porcelain crabs and diogenid hermit crabs, and the more

terrestrial coenobitids. The former are immersed twice daily

and ai'e generally either osmoconformers or weak osmoregul-

ators (Davenport, 1972a,b,c; Jones, 1977; Young, 1979;

Sabourin and Stickle, 1980) although stronger regulatory

ability must be present in Clibanarius fonticola (McLaughlin

and Murray, 1990) which inhabits freshwater pools.

The coenobitids exhibit a continuum of osmoregulatory

behaviour; some species are restricted to supralittoral habitats

and drink seawater while others penetrate inland and prefer

dilute water (Table 3). In beach-dwelling coenobitids that drink

seawater, the inability to produce hyperosmotic excretory fluid

and the effects of evaporative water loss and dietary salt intake,

result in blood and shell water concentrations hyperosmotic to

seawater (Table 3). The main osmoregulatory tactic in these

animals is to flush the shell reservoir with seawater at regular

intervals either by immersion or by drinking. This allows

replacement of fluid losses and facilitates loss of salt from the

body fluids to shell water but sets a minimum concentration for

the blood similar to that of seawater.

Coenobita spp. that live away from the beach do not

usually have access to seawater and indeed these species prefer

dilute water unless they are depleted of salt (de Wilde, 1973).

As the drinking water is dilute the animals can and do maintain

Terrestrial adaptations in Anomura

Table 3. Osmoregulation in terrestrial coenobitids. SW = sea water; FW = fresh water.

Species

Distribution

Drinking

Water

Blood Cone,

mosm

Shell water

mosm

Source

C. scaevola

Beach only

Achituv and Ziskind (1985)

C. perlatus

Beaches/atolls, small islands

>SW 1020-1500

>SW 970-1260

Gross (1964),

Gross and Holland 1960

C. cavipes

C. rugosus

Beach and vicinity

FW/SW

<SW 865-975

<SW

Gross et al. (1966)

Vannini (1975b)

C. clypeatus

Beach and inland

<SW 969

<SW 915-945

de Wilde (1973)

C. brevimanus

Coastal forest dense vegetation

<SW 840

<SW -762-908

Gross (1964)

B. latro

Inland

<SW 650-750

No shell water

Taylor et al. (1993)

Greenaway (2001)

shell water and body fluid concentrations well below that of

seawater (Table 3). The salt in their shell water must originate

from the diet, perhaps via urine released into the shell, and pre-

sumably is available to the animal via branchial uptake or

ingestion.

The normal ranges of osmotic concentration maintained by

coenobitids are well established (Table 3) and it is known that

the crabs maintain their shell water isosmotic with the body

fluids (summarised in Greenaway, 1988). However the mech-

anisms of regulation in the shelled hermit crabs have not been

studied. Regulation is potentially complex as it may involve

exchanges of water and ions between numerous compartments

including the shell water, crab tissues, the excretory system and

the outside environment. The urine is isosmotic and on release

from the antennal organs may potentially be voided, drunk,

passed to the branchial chambers for ion recovery or added to

the shell water. Similarly, fluid released from the branchial

chambers after salt recovery could be voided or added to the

shell water. Only drinking and flushing have been examined to

date. When crabs of either group have access to waters of dif-

fering salinities they can regulate shell water within the pre-

ferred range behaviourally by selective drinking and promotion

of evaporation (Gross, 1955; 1964; de Wilde, 1973). Crabs

have a strong ability to assess the salinity of water bodies and

C. clypeatus can discriminate differences in salinity of only

0.18-0.36 (de Wilde, 1973), whilst C. rugosus can distinguish

between airborne odours of fresh and saline water (Vannini and

Ferretti, 1997). Although differential drinking may be utilized

for osmoregulation by beach-dwelling animals and in atoll pop-

ulations, it is not useful in the more inland situations where

generally only fresh water is available (Wolcott, 1992). There

different mechanisms must be used.

Osmoregulation in B. latro differs from the patterns seen in

other coenobitids as, in the absence of a mollusc shell, the body

fluids are regulated directly against the environment. In com-

mon with other coenobitids, B. latro has a preferred range of

blood concentration and is remarkably tolerant of haemo-

concentration. In most natural field situations, only fresh water

is available for drinking, and B. latro maintains its blood con-

centration in the range 650-750 mosm, with the lower blood

concentrations preferred in wet conditions and maintained even

if salt intake and excretion are high (Greenaway, 2001). Where

only saline water is available (e.g. atolls), the osmotic concen-

tration of the body fluids becomes elevated; the animals will

tolerate concentrations in excess of 1100 mosm for long

periods (Gross, 1964; Taylor et ah, 1993).

Salt regulation in B. latro is convergently similar to that of

the terrestrial brachyurans. Urine of similar osmotic concen-

tration and ionic composition to the blood is released from the

antennal organs. Some volume recovery occurs by drinking and

the residual volume is passed to the branchial chambers where

salt recovery conforms to homeostatic needs. Turnover of salt

in the field is high (7.8 mmol.kg-hd-i) but regulation of body

sodium is readily achieved when drinking fresh water

(Greenaway, 2001). When dietary salt intake is low, the final

excretory fluid is extremely dilute (<10 mmol.L-i Na) but, with

access to saline water, the animals respond rapidly with

increases in intake, in flow and in concentration of the urine

and in the concentration of the released excretory fluid. When

sea water is drunk, the excretory fluid released is isosmotic or

marginally hyperosmotic to the blood (Greenaway et ah, 1990;

Taylor et al., 1993; Greenaway, 2001). Once elevated, how-

ever, blood concentrations can only be reduced if crabs have

access to drinking water of lower osmotic concentration than

the blood.

Salt resorption from urine released to the branchial cham-

bers is effected by transport mechanisms in the branchial

epithelium (Morris et al., 1991) and, as the crab normally

drinks only fresh water, a high rate of branchial ion recovery is

the default condition. Branchial ion transport is controlled by

the blood-borne hormone dopamine. Elevation of the blood

concentration is believed to increase the circulating level of

dopamine which stimulates an increase of the [cAMP] in the

branchial epithelium which in turn results in deactivation of

Na+K+-ATPase (Morris et al., 2000). Thus B. latro has devel-

oped an ion regulatory mechanism that normally conserves ions

by production of a dilute excretory fluid suited to the particular

requirements of its normal habitat. When faced with the rela-

tively uncommon circumstance of high salt intake, then

branchial transport is down regulated to increase salt output. In

situations where B. latro has access to both dilute and saline

drinking water, e.g. on small islands and atolls, it too can regu-

late its body fluid concentration by differential drinking (Gross,

1955; Combs et al., 1992).

B. latro has developed a flexible system of osmoregulation

that combines a high degree of physiological and behavioural

regulation of salt and water balance with tolerance of large

fluctuations in blood osmolality. These adaptations enable the

Peter Greenaway

species to regulate effectively in environments where only

fresh drinking water is available and also on small islands

where, seasonally, seawater becomes the sole source of drink-

ing water.

Nitrogenous excretion

Uniquely amongst the terrestrial crustaceans studied, B. latro

has adopted a terrestrial excretory pattern and eliminates

purines in lengths of white excreta (Greenaway and Morris,

1989). In initial enzymatic analyses, the purine was identified

as uric acid (Greenaway and Morris, 1989), but recent HPLC

studies have revealed that both uric acid and guanine are pres-

ent at a ratio of 2:1 (P. Greenaway, pers. obs.). The white

faeces are made up of billions of small spherules of purine 1-2

pm in diameter produced by R cells in the tubules of the midgut

gland and released periodically into the gut in coordinated

bouts of secretion (Dillaman et al., 1999). The purine excreted

is synthesised de novo and a key enzyme in this process, xan-

thine dehydrogenase, is present at high activities in the midgut

gland (Dillaman et al., 1999).

In Coenobita, faeces are deposited outside the shell and any

faecal elimination of purines or ammonium could readily be

established. Excretion of ammonia, either in gaseous form or in

excreted fluid, could also be easily assessed but the necessary

measurements have not been performed. Excretory products in

the blood offer few clues to the excretory mechanism used;

urea is not detectable, ammonia levels are reportedly low and

although uric acid is somewhat elevated (Henry and Cameron,

1981) this could be connected with purine storage in the tissues.

At the present time the mechanism of N excretion is obscure

and investigation of the excretory mechanisms employed by the

shell-carrying hermits is urgently needed.

Purine is stored in large amounts in connective tissue cells

throughout the bodies of Coenobita and B. latro, (Henry and

Cameron, 1981; Greenaway and Morris, 1989) as well as other

land crabs (Linton and Greenaway, 1997a). In the brachyuran

land crab Gecarcoidea natalis (Pocock, 1888), this stored

purine is synthesised de novo, and it is likely that synthetic

ability is common to the brachyuran and anomuran land crabs

that store purines (Linton and Greenaway, 1997b). A storage

excretion function has been ascribed to the urate accumulated

by G. natalis (Linton and Greenaway, 1998; 2000). Although

this function is possible in Coenobita it seems unlikely in

B. latro where N is excreted as purine and is not therefore con-

strained by water availability as in G. natalis. The possibility

that purine stored in B. latro functions as a remobilisable N

reserve needs to be investigated.

Feeding and diet

The terrestrial anomurans are catholic feeders and eat fallen

fruits and seeds, mangrove propagules, a wide variety of other

plant material, strand line detritus, animal faeces and animal

carcases varying from small invertebrates to fish, giant tor-

toises, birds, goats and donkeys (Grubb, 1971; de Wilde, 1973;

Vannini, 1976; Barnes, 1997a). Much of the normal diet is plant

material, but near human habitations resident populations

C. cavipes may become reliant on human faeces and refuse

(Barnes, 1997a). On Aldabra, C. rugosus exploits fresh tortoise

faeces (Grubb, 1971). A number of species of Coenobita climb

bushes and small trees (reviewed by von Hagen, 1977) where it

is likely that they forage on plant material or perhaps scale and

other insects. In mangroves, however, climbing by C. cavipes

and C. rugosus seems not to be primarily oriented towards

feeding (Barnes, 1997b).

Birgus latro is a little more selective in its diet but also

exploits a wide range of plant and animal materials. It par-

ticularly favours high energy plant material notably seeds rich

in carbohydrate or lipids (e.g. Pandanus elatus (Ridl., 1906),

Calophyllum inophyllum (Linnaeus, 1753), Cocos nucifera

(Linnaeus, Aleurites moluccana ((L.) Willd., 1805), and

it will rip away and discard the fleshy material of soft fruits

such as custard apples (Annona reticulata (L., 1753)) and

papaya {Carica papaya L.) to access the seeds. Fruits and

kernels of the sago pdXmArenga listen (Becc., 1891) are par-

ticularly attractive, as is the carbohydrate-rich pith. Birgus latro

will climb the tall trunks of A. listeri, Pandanus and C. papaya

to reach the fruits but most animals wait for fruit to fall and

aggregations of several hundred animals are reported beneath

preferred fruiting trees (Hicks et al., 1990). The large chela,

which can develop forces of 90 kPa, (Hicks, Rumpff and

Yorkston, 1990) is used to open the very hard nuts of

A. moluccana and C. inophyllum and the animals readily open

Macadamia nuts in the laboratory. Large animals can strip the

husk from fallen coconuts and open the hard inner shell at the

“eyes”. They investigate, can-y away and attempt to open any

unusual object and will visit garbage bins hence their common

name, robber crab. The crabs are also active predators. On

Christmas Island, they feed extensively on the gecarcinid crabs

Gecarcoidea natalis and Cardisoma hirtipes (Dana, 1852),

which they stalk or dig out from shallow burrows (Hicks et al.,

1990; Greenaway, 2001). On Aldabra they are reported to prey

on hatchling tortoises (Swingland in Alexander, 1979) and on

the land crab Cardisoma carnifex (Herbst, 1794). Foraging is

dependent on humidity, and marked or radio-tagged B. latro

forage infrequently in dry weather but nightly in moist

conditions (Reese, 1987; Fletcher et al., 1990b; Greenaway,

2001 ).

Birgus latro stores lipids and glycogen in the R cells of the

midgut gland (Chakravarti and Eisler, 1961; Lawrence, 1970;

Storch et al., 1982; Dillaman et al., 1999). The midgut gland

fills the abdomen and can expand substantially to accommodate

food reserves, which may allow survival for more than a year

without feeding (Storch et al., 1982).

There is no information on the digestive physiology of

Coenobita although there are several studies on the masticato-

ry apparatus of hermit crabs (Schaefer, 1970; Caine, 1975;

Kunze and Anderson 1979). Recently Wilde and Greenaway

(1998, 2001) measured rates of assimilation of nutrients by B.

latro (Table 4) and these data may be applicable to the family

Coenobitidae in general.

Birgus latro has a very high ability to utilise fats and storage

polysaccharides of both plant and animal origin and addition-

ally can digest significant amounts of plant fibre such as hemi-

celluloses, cellulose and lignin. Protein assimilation from plant

Terrestrial adaptations in Anomura

material is 65-70% and the animals efficiently digest chitin

from crab skeletons. Birgus latro and probably other coen-

obitids clearly have the ability to digest a wide range of food

materials from plant fibre through to protein and chitin, which

helps to explain their catholic feeding habits. It also clarifies

some of the more bizarre aspects of feeding in the group, such

as feeding on faeces. To coenobitids, vertebrate faeces are a

rich food source as they contain undigested plant fibre, mucous

and animal protein in the form of sloughed-off intestinal cells

and waste enzymes. Additionally, the products of microbial

digestion in the lower alimentary tract of vertebrates com-

monly pass out in the faeces and these, and the microbes them-

selves, will be utilised by Coenobita. Faeces represent a con-

siderably higher quality diet than, for example, shoreline plant

detritus. In the long term, eating faeces may entail the risk of

becoming a secondary host for vertebrate parasites but the

gastric mill may well be an effective protection against many

infective stages.

Table 4. Assimilation of food components by Birgus latro fed on arti-

ficial diets. Data from Wilde and Greenaway (2001, and pers. obs.).

Diets consisted of starch, coconut, sunflower seed, hazelnuts and bran

ground and blended into an agai’ base. The crab diet was prepared from

dried and powdered Gecarcoidea natalis blended in agar.

High fat diet

% assimilation

High

carbohydrate

Crab

diet

Dry matter

75.5

71.7

64.7

Lipid

87.4

70.8

Carbohydrate

98.1

89.4

Hemieellulose

Cellulose

Lignin

Chitin

92.8

82.1

72.7

64.5

69.4

65.2

Coenobitids can detect food odours from distances exceed-

ing 5 m (Dunham and Gilchrist, 1988) but they are attracted

preferentially by the odours of foods that they have not eaten

recently rather than foods recently eaten. This negative prefer-

ence induction lasts 6-9 h after a change of foods (Thacker,

1996; 1998) and presumably facilitates avoidance of particular

nutritional deficiencies that might be incurred by reliance on a

single food type or, alternatively, the accumulation of toxins.

Thermoregulation

Many coenobitid species occupy tropical beach habitats where

high daytime insolation and temperatures enforce nocturnal

activity patterns. Where rainfall is low or vegetation cover

poor, inland distribution is generally restricted (e.g. Coenobita

scaevola on Red Sea coasts (Achituv and Ziskind, 1985).

Behavioural means are used to avoid overheating. Coenobita

seek cool, humid daytime refuges under beach debris, or in

litter and under shrubs and tree roots at the top of beaches.

Coenobita scaevola and C. rugosus bury themselves up to 20

cm in the sand to avoid direct insolation and as a result body

temperature seldom exceeds 35°C (Vannini, 1976; Achituv and

Ziskind, 1985). The more inland species also seek daytime

refuges; C. brevimanus clusters in groups under logs in rain-

forest on Christmas Island and in piles of coconut debris

(Gross, 1964), while B. latro favours rock crevices, hollow logs

and trees (Fletcher et ah, 1990b; Greenaway, 2001). Activity is

largely nocturnal but often begins before sunset as insolation

drops. In cold weather Coenobita become inactive and remain

buried in the sand or under debris (George and Jones, 1984).

Although behavioural thermoregulation is predominant in

the Red Sea species, C. scaevola, all shell water has generally

been lost by the time crabs emerge from burrows at the end of

the day and their first action is to refill the shell with sea water

(Achituv and Ziskind, 1985). The evaporation of this water will

facilitate heat loss.

Role of the shell in terrestrial life

The terrestrial hermit crabs live in and carry around a protec-

tive molluscan shell, a habit that predated terrestrial life. Shell-

carrying provides certain advantages in the terrestrial life of

these crabs as it reduces evaporative water loss, provides a

reservoir of salt and water that increases survival time under

desiccating conditions, allows for foraging further from water

sources and removes the immediate need to develop new

methods of ionic regulation. Additionally, it assists in thermo-

regulation and offers protection against predators (Herreid,

1969b; de Wilde, 1973; McMahon and Burggren, 1979;

Achituv and Ziskind, 1985).

Dependence on a shell imposes a new set of constraints as

well as offering some advantages. Potentially, population size

and stmcture, and particularly penetration inland, may be

limited by the availability of suitable shells of marine gas-

tropods. Whilst shell availability may not be limiting in some

situations (e.g. Quirimba Island (Barnes, 1999) it is evident

from crab behaviour that shells are a limiting resource gener-

ally. Thus C. brevimanus may attack and kill the muricacean

gastropod Acanthina in order to obtain the shell (McLean

1974), C. clypeatus are reported to collect and stockpile empty

mollusc shells for later use (Gilchrist, 1995), and shell

exchange amongst conspecifics is common (Hazlett, 1981).

Groups of crabs congregate to exchange shells, and the avail-

ability of a large vacant shell triggers a cascade of shell

exchange with progressively smaller animals taking part until

the vacated shell is too small for the remaining participants.

Similar behaviour occurs following the death of an individual;

Coenobita are attracted by the odour of dead conspecifics and

aggregate around them. Shell exchange is believed to be an

evolutionarily conserved behaviour inherited from marine

ancestors (Small and Thacker, 1994). If suitable shells of ter-

restrial origin are available inland they are utilised; Coenobita

on Vanuatu and Guam use shells of the introduced land snail

Achatina fulica (Bowdich, 1822) (Fletcher et ah, 1991a; A.W.

Harvey, pers. comm.). Occasionally other structures such as

small coconut shells or bamboo may be used in place of mol-

lusc shells, but use of structures other than the shells of marine

gastropods is rare.

Heavy shells result in high energy expenditure for loco-

Peter Greenaway

motion and in reduced speed and mobility but offer greater pro-

tection from predation. Small shells are lighter but may restrict

growth and lead to smaller clutch sizes for females. Coenobita

compressus seems to prefer shells with a high internal

volume/weight ratio, which optimises these conflicting

requirements (Osomo et al., 1998).

The restrictions imposed by shell dependence probably

determine population size, size distribution and inland dis-

persal. Whilst the mollusc shell is an effective behavioural

solution to many of the physiological problems that animals

must face on land, it decreases the selective pressures for

physiological solutions to these problems and reinforces

dependence on shells. Birgus latro is the only coenobitid crab

that no longer relies on mollusc shells (once past the juvenile

stage). Independence from shells removes restrictions on body

size and significantly, B. latro is the largest of the coenobitids

(to 3 kg), and its physiological adaptations to terrestrial life

parallel those of brachyuran crabs. These adaptations have not

obviously resulted in more effective or widespread penetration

of terrestrial habitats than in other coenobitids; B. latro is more

or less restricted to maritime and island forest habitats, while

C. clypeatus penetrates both drier habitats and further inland.

Locomotion and movements

Although coenobitids appear cumbersome and generally carry

heavy mollusc shells, they have strong locomotor ability

(Herreid and Full, 1988) and are often excellent climbers

ascending shrubs, saplings and trees (Barnes, 1997b; von

Hagen, 1977). The shelled forms climb with the chelae and the

pointed dactyls of the pereopods that hook around small

branches or grip the surface. Birgus latro has long needle-like

terminations of the dactyls of the walking legs and uses these to

grip bark on large tree trunks or irregularities in rock surfaces.

They can sling themselves upside down from small branches

and grip vertical rock faces and overhangs.

The heavily calcified walking legs easily support the large

body of B. latro which is carried clear of the ground during

locomotion although the crab squats on the curled abdomen at

rest. Coenobita use the chelae and the next two pairs of pereo-

pods in locomotion. An alternating tripod gait is normal, with

forward thrust provided largely by the second pereopods (R2,

L2) while the first pereopods (chelae) are used mainly in

support. The abdomen and mollusc shell are usually carried

clear of the ground during locomotion although large shells

may be dragged. At rest the shell lies on the ground (Herreid

and Full, 1986a).

Hermit crabs are capable of sustained locomotion at slow

walking speeds, and journeys up to 500 m in a night have been

recorded during breeding migrations (de Wilde, 1973). The for-

aging range for beach living Coenobita, where food and water

are co-located, is relatively small; they generally move within

a 30 m radius and may have particular home sites and home

ranges (Herreid and Full 1986a; Brodie 1998). Where food and

water sources are separated, animals may migrate between

them nightly (e.g. C. rugosus), but longer forays inland occur

when the animals are freed from a fixed water source by wet

conditions (Vannini, 1976). Birgus latro are not fixed in their

foraging pattern and many seem to have a number of home sites

that they move between. At other times they appear to be

nomadic, and radio-tagged animals may move as much 500 m

through rain forest in 24 h (Fletcher et al., 1990b; Greenaway,

2001) to locate fruiting trees.

Sensory adaptations

Terrestrial animals rely chiefly on vision, olfaction and sound

detection to provide information about the environment, and

the relevant sensory organs of emergent species must be able to

function in air rather than water. Land crabs have developed

aerial visual and olfactory systems but appear to show less

reliance on sound. Despite functional changes in sensory

systems the gross anatomy of the brain remains similar in

aquatic and terrestrial species of anomurans (Sandeman et al.,

1993).

Coenobita rugosus has ridges on the left chela and second

left pereopod that resemble a stridulatory apparatus (Vannini,

1976), and these have also been observed in several other

species (A.W. Harvey, pers. comm.). The species is reported to

produce chirping sounds (Borradaile, 1903). Coenobita pur-

pureas (Stimpson, 1838) make sounds (Imafuku and Ikeda,

1990), as does C. violascens (Heller, 1852) when captured

(Nakasone, 1988a). Birgus latro has been reported to make a

continuous ticking sound (Grubb, 1971), but there are no other

records of sound production by the species, and Grubb (1971)

may have detected scaphognathite activity which can be

audible. As some species of Coenobita emit sounds it is likely

that they also have sound receptors but, although there are

anecdotal reports of sensitivity to sound (Borradaile, 1903),

visual and vibration sensing cannot be ruled out. Vannini

(1976) has suggested that orientation in transdunal migrations

of C. rugosus may be to either the noise, or vibrations, gener-

ated by breaking waves.

Coenobitids have apposition eyes similar to those of other

diurnal arthropods (Spears, 1983). On behavioural evidence

vision is evidently an important sense, but to date there are no

physiological studies on vision in the group.

Olfaction is highly developed and centred on the first anten-

nae. These are in constant palpatory movement when the crabs

are active, and the movements maximise the volume of air

sampled and perhaps provide directional information on

sources of odours. The first antennae of coenobitids differ from

those of aquatic decapods as the basal joints are quite long and

enable the two sensitive flagella to touch and sample the

ground as well as a large volume of air above and around the

crab. The sensory units (aesthetascs) of C. compressus are short

and blunt and more similar to those of terrestrial insects than to

those of aquatic decapods, including aquatic hermit crabs, and

this may be a familial trait. These differences are believed to be

concerned with adaptation for detection of volatile chemicals in

air and perhaps with restriction of antennular water loss

(Ghiradella et al. 1968a; 1968b). The species also appears to

lack aesthetascs on the dactyls although these are present in

aquatic decapods.

Both B. latro and Coenobita detect food from a distance and

aggregate around significant food sources. Birgus latro seems

Terrestrial adaptations in Anomura

particularly effective at detecting fruit and aggregates around

opened coconuts, pith of sago palms and fruiting trees. It also

quickly detects road kills and other carrion. Coenobita cavipes

is attracted by a variety of volatile food odours but can detect

nonvolatile foods only by contact (Rittschof and Sutherland,

1986). Coenobita can also detect water vapour; and species that

penetrate inland, such as C. rugosus and C. brevimanus, can

distinguish between the odour of fresh water and sea water,

although this sense is poorly developed in beach dwelling

species such as C. cavipes and C. perlatus (Vannini and

Ferretti, 1997). Where individuals are numerous, location of

food may be facilitated socially with animals locating food

sources by observing behaviour of their neighbours rather than

by detection of food per se (Kurta, 1982).

The coenobitids are characterised by retention of the long

filiform second antennae seen in aquatic anomurans. These are

highly mobile and seem to be used to investigate and locate

solid objects in the environment in a manner similar to that of

their aquatic relatives and astacurans. There have been no

specific studies on their role in the Coenobitidae.

The coenobitids possess considerable ability to orient, navi-

gate and home (Vannini and Cannicci, 1995). Coenobita

clypeatus orient to a few preferred breeding sites from

wide areas of the hinterland (de Wild, 1973). Populations of

C. rugosus may occupy a distinct home area in which they

remain for periods of a year or more whilst not necessarily

occupying any specific home site (Vannini, 1976). Likewise the

aquatic diogenid, Clibanarius laevimanus (Randall, 1840),

forms clusters amongst mangroves between foraging periods,

and stays within a home area even though it may change clus-

ters within the area (Gherardi and Vannini, 1992). Coenobita

rugosus orient to visual cues if landmarks are visible and in

uniform environments utilises celestial cues. Orientation to

locate the home beach using celestial cues involves learning,

since a particular home beach on an island or atoll may face in

any direction (Vannini and Chelazzi, 1981). Coenobita is also

sensitive to directional air movements, and in the absence of

other cues they may use wind currents as a source of direct-

ional information for navigation (Vannini, 1975a; Vannini and

Chelazzi, 1981; Vannini and Ferretti, 1997).

Moulting and growth

Birgus latro is long-lived and grows slowly with maximum size

reached only after 40-60 y (Fletcher et al., 1990a; Fletcher et

al., 1991b). Coenobita too may be long-lived, and lifespan in

the larger species exceeds 10 years (Chace, 1972). Longevity

and slow growth in litter-eating terrestrial brachyurans have

been linked with a low N intake (Linton and Greenaway, 2000)

but other explanations for the longevity of coenobitids may be

necessary as many coenobitids have an appreciable intake of

animal material in the diet.

In preparation for the moult, B. latro digs a burrow up to 1

m long and seals itself inside for 3-16 weeks. This period

increases with body size. Adults moult annually, usually in the

winter months (Held, 1965; Fletcher et al., 1990a; 1991b).

Typically premoult animals enter their burrows with their

abdomens markedly swollen by food reserves and increased

blood volume. After moulting the animal eats its exuviae,

which contribute organic materials and calcium salts needed for

the new skeleton. Certain brachyuran land crabs reabsorb cal-

cium from the old skeleton in premoult, store it in the body and

reuse it to calcify the new skeleton (Greenaway, 1985; 1993),

but there are no data regarding premoult storage of calcium in

B. latro. As the species moult in burrows and eat their exuviae,

significant internal storage mechanisms may not have been

developed. The growth increment at the moult in large animals

is hard to assess as linear measurements increase only slightly,

and the changes in body water, food reserves and abdominal

size make mass changes an unreliable indicator of increased

size. Reported increases in linear dimensions following moult-

ing are 1-16% with large crabs showing the smallest

increments (Held, 1965; Fletcher et al., 1990a; 1991b).

Very little information is available in regard to moulting of

Coenobita. Coenobita clypeatus is reported to hide during the

process most of which occurs in the shell (de Wilde, 1973).

There is a noticeable reduction in activity for several days prior

to the moult and after ecdysis the exuviae are positioned just in

front of the mouth of the shell (A.W. Harvey, pers. comm.).

During calcification the new soft skeleton of the chelae and

other walking legs is moulded to fit the shape of the shell. If the

animal increases markedly in size it may no longer fit neatly

within the old shell and a rapid trade up in shell size may be

necessary to avoid water loss and predators. There is no infor-

mation available on calcium balance or storage through the

moult or on growth increments of Coenobita. Coenobita

clypeatus grows up to 500 g if large-enough shells are available

(de Wilde, 1973).

Autotomy of limbs is uncommon amongst the land crabs,

and coenobitids are no exception. Autotomy generally only

occurs if limbs are severely damaged or infected, and the

incidence of missing chelae in B. latro is very low (Grubb,

1971). This may reflect the greater importance of the limbs in

locomotion and feeding in terrestrial crabs, the major invest-

ment in replacing the lost protein from a diet low in nitrogen

and the relatively long intervals between moults. It is sig-

nificant that amongst the terrestrial brachyurans only the car-

nivorous grapsids readily shed limbs. Given their high N intake

and rapid growth rates this is an affordable tactic.

Reproduction

No terrestrial anomurans complete the reproductive process on

land, and all species retain marine larval stages although, as in

Coenobita variabilis (McCulloch, 1909), these may be abbre-

viated (Harvey, 1992). Substantial reproductive adaptations to

terrestrial life have nevertheless been achieved within the group

and location of sexual partners, courtship, mating, and the

extrusion and early development of eggs all occur on land. The

animals also possess the necessary behaviours to time and

orient their breeding migrations to the sea and select particular

conditions of lunar and tidal cycles for spawning. Many of

these behaviours may differ within a species as the direction

of the sea, time of the wet season, and direction and strength of

ocean currents may vary within the geographical range.

The spawning period of B. latro varies over its distribution

Peter Greenaway

range and probably reflects the seasonal occurrence of

favourable weather conditions and ocean currents. Spawning

on Christmas Island coincides with the onset and main peak of

the wet season, which provide optimal conditions for migration

to the coast for spawning. The downward migration is an indi-

vidual affair but the return journey may involve coordinated

groups (Schiller et al., 1991). As mating precedes migration it

is likely that males do not migrate to the coast. Mating lasts

only a few minutes during which the male lays the female on

her back and deposits a mass of spermatophores around the

oviducal apertures at the base of the third pereopods (Helfman,

1977b; Schiller et al., 1991). The spermatophores are robust,

gelatinous stmctures about 650 pm high glued to the exoskele-

ton by the pedestal. A short stalk rises from the pedestal and

bears a heart-shaped ampulla, which contains the spermatozoa

(Tudge, 1991). Eggs (~ 100,000) are laid after mating and are

attached to the pleopods and carried throughout the develop-

mental period (27-29 days) before release into the sea. The

crabs release eggs at night between the first and last quarter of

the moon. They do not generally spawn from beaches (Schiller

et al., 1991) but instead descend cliffs or walk over intertidal

platforms until they encounter wet rock or pools. On contact

with seawater, the females orient the abdomen towards the

water and advance cautiously until wave wash stimulates

hatching. Only 1-2 waves are needed for complete hatching of

the zoeae. Birgus latro usually has four planktonic zoeal stages

that are believed to be dispersed primarily by surface currents.

The postlarval, megalopal stage is epibenthic, and on reaching

the shallow water larvae search for and occupy mollusc shells

before emergence onto land. They burrow in sand and meta-

morphose to the first crab stage that emerges after 3^ weeks

(Reese and Kinzie, 1968). Juveniles may live in mollusc shells

until they reach a carapace length of ~15mm and thereafter

abandon the shell.

Coenobita clypeatus reach sexual maturity in their second

year at weights of 1-2 g, although they can reach 500 g in

weight. The early onset of sexual maturity may allow self-

sustaining populations in areas where large shells are rare or

unavailable. Populations of Coenobita that live inland migrate

to coastal breeding sites where it is believed that mating takes

place (Yamaguchi, 1938; de Wilde, 1973). Males are thought to

detect females by means of chemosensory and visual clues, and

both sexes partially emerge from their shells for mating during

which spermatophores, similar to those of B. latro, are trans-

ferred to the female (Reese, 1987). The smallest females pro-

duce around 10^ eggs and the largest adults perhaps 5x10^ (de

Wilde, 1973). Eggs are released into the sea about 30 d after

laying and C. clypeatus avoids immersion during this process

(de Wilde, 1973). The larvae hatch in the water as zoeae and

take 3-7 weeks to pass through up to five zoeal stages before

megalopae appear (Provenzano, 1962; Nakasone 1988b). By

contrast C. variabilis have only two non-feeding zoeae and

reach the megalopal stage in 6-7 days (Harvey, 1992).

Megalopae feed in all species and soon begin to search for mol-

lusc shells. With or without shells the megalopae emerge from

the water and bury themselves on the beach where they meta-

morphose and resurface as juvenile crabs (Harvey, 1992;

Brodie, 1999). Megalopae will not metamorphose in water, and

there are conflicting reports on survival of megalopae that

metamorphose without shells (Harvey, 1992).

Pelagic larvae are important to enable wide distribution of

coenobitids. The planktonic stages generally last 2-4 weeks

and whether they encounter a terrestrial habitat depends on the

direction and strength of ocean currents and prevailing weather

conditions. Thus megalopae may return to the home or to

neighbouring islands, be dispersed down current to new islands

or be transported unpredictably sometimes over very long dis-

tances. The possibility of not encountering a suitable island is

obviously high; recruitment of B. latro appears to be rare,

although whether this results from the reclusive fossorial nature

of the megalopae, from irregular recruitment, or both, is

unclear (Reese, 1987; Schiller et al., 1991). The longevity of B.

latro means that regular recruitment is unnecessary for pop-

ulation survival, and it may even be an adaptation to erratic

recruitment. The distributions of many coenobitid species are

very wide, e.g. B. latro is distributed throughout the Indian and

Pacific oceans. This distribution is thought to be the result of a

population explosion in the Pleistocene. Currently the Indian

Ocean and Pacific populations appear to be separate, whilst

continued genetic exchange persists between Pacific island

populations (Lavery et al., 1996a, b).

The life styles of Coenobita and B. latro diverge after 1-2

years (Harms, 1932; Reese, 1987), when the juvenile B. latro

abandon shell living and undergo morphological changes to

adopt the adult body form.

Summary

The Porcellanidae, Diogenidae and Coenobitidae have all

developed amphibious or terrestrial life styles but only the

latter show significant independence from water. Coenobitids

conduct essentially all functions on land although they must

have access to the sea to release larvae into the water.

Terrestrial adaptations developed by coenobitids generally par-

allel those of terrestrial brachyurans, but as their morphological

and behavioural starting points for the colonisation of land dif-

fered, some significant differences are apparent between the

terrestrial representative of the two groups. The family

Coenobitidae has a small number of species but is very suc-

cessful (in terms of the number of individuals) in tropical

maritime and island environments. A number of species have

powerful osmoregulatory ability and maintain salt balance with

only freshwater to drink but the mechanisms involved require

further study. Birgus latro has developed purine excretion but

the nitrogenous excretory products and their mechanism of

elimination in Coenobita have not been studied. Aerial gas

exchange is enabled by well-developed branchiostegal lungs in

B. latro, whilst Coenobita, constrained by the shells in which

they live, have developed a novel abdominal gas exchange

organ in addition to gills and lungs. The relative contributions

of each to overall gas exchange are unknown. The coenobitids,

unlike the brachyuran land crabs, have long filiform second

antennae used as touch and mechanoreceptors, and share good

visual capability and a well developed olfactory sense in air.

Whilst many terrestrial and semi-terrestrial brachyurans have

evolved direct development the coenobitids all retain marine

Terrestrial adaptations in Anomura

larval stages. This restricts inland penetration, as the animals

must be able to migrate back to the coast to shed their larvae

into seawater, and is probably responsible for their limited

distribution. For Coenobita, the situation is aggravated by the

relative paucity of large snail shells in inland situations, and the

relatively thin walls of these shells that offer little protection

against large predators.

From available evidence, it is clear that the terrestrial adap-

tations made by the coenobitids have allowed them to success-

fully occupy a number of terrestrial niches ranging from the

supra littoral zone to several kilometres inland in habitats

that range between semi-desert and rainforest. Further pene-

tration may not be possible without reproductive adaptations

to eliminate aquatic larval stages and, for Coenobita, prob-

ably independence from the necessity to carry a mollusc

shell.

Acknowledgements

I am grateful to Alan Harvey for supplying helpful information

on the biology of Coenobita.

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Memoirs of Museum Victoria 60(1): 27-34 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

Marine hermit crabs as indicators of freshwater inundation on tropical shores

S.G. Dunbar,! ’2 m. Coates' and A. Kay^

iSchool of Biological and Environmental Sciences, Central Queensland University, Roekhampton, Qld 4702, Australia

2CRC for Coastal Zone, Estuary and Waterway Management, Indooroopilly, Qld 4068, Australia {present address:

Marine Biology, Graduate School of Natural Sciences, Loma Linda University, Loma Linda, Ca. 92350, USA

sdunbar@ns.llu.edu)

^Queensland Parks and Wildlife Service, PO Box 3130, Rockhampton Shopping Pair, Qld 4701, Australia

Abstract Dunbar, S.G., Coates, M., and Kay, A. 2003. Marine hermit crabs as indicators of freshwater inundation on tropical

shores. In: Lemaitre, R., and Tudge, C.C. (eds). Biology of the Anomura. Proceedings of a symposium at the Pifth

International Cmstacean Congress, Melbourne, Australia, 9-13 July 2001. Memoirs of Museum Victoria 60(1); 27-34.

The marine hermit crabs, Clibanarius taeniatus (H. Milne -Edwards, 1848) and C. virescens (Krauss, 1843) are com-

mon rocky intertidal speeies along the coast of Queensland, Australia. Laboratory experiments in dilute (8%o) seawater

at 15°, 25° and 35°C over an extended period (up to 77 h) showed that C. taeniatus had significantly better survival than

C. virescens. In extended exposure to a low salinity, estuarine environment C. taeniatus also survived significantly bet-

ter than C. virescens. Repeated sampling at selected sites revealed that a site with no freshwater influence maintained a

low percentage of C. taeniatus and high percentage of C. virescens, while at a site influenced by regular, low level fresh-

water runoff, the percentage of C. taeniatus remained high. A survey of the Queensland coast, showed that C. virescens

tended to be more dominant on open coasts uninfluenced by freshwater, while C. taeniatus tended to be more abundant

in areas influeneed by freshwater. These two species therefore are a convenient indicator system for the influence of

freshwater on tropical intertidal rocky shores and may therefore constitute an important management tool in areas

experiencing coastal development with concomitant storm water runoff into marine habitats.

Keywords Crustacea, Anomura, hermit crab, Diogenidae, Clibanarius taeniatus, Clibanarius virescens, salinity, tropical,

temperature

Introduction

Intense coastal development that has been typical of temperate

regions, is now increasing in the tropical regions of the globe

(Johannes and Betzer, 1975; Vernberg, 1981). Coastal develop-

ment can result in a range of pollutants being discharged into

coastal habitats. Examples are untreated, or partially treated

sewage, chemical effluent from a variety of industrial sources

and storm water runoff from residential areas. This last source

of pollution is of increasing importance in tropical areas exper-

iencing extensive residential development in the coastal zone.

Many tropical areas are subject to episodes of heavy rainfall. It

is well known that during floods, unusually large volumes of

freshwater runoff from rivers can have severe impacts on

marine habitats, particularly intertidal habitats (Goodbody,

1961; Fotheringham, 1975; Coates, 1992; Forbes and Cyrus,

1992; Van Woesik et al., 1995). Thus, fresh water itself may act

as a pollutant in the sense of having detrimental effects on

marine habitats. Artificial drainage systems tend to concentrate

storm water runoff from residential areas into a few points.

Storm water drains can cause episodic inundation by fresh

water, lasting for several days or weeks, in areas that would not

normally experience freshwater runoff, or would experience it

only rarely. A convenient indicator system able to detect effects

of episodic freshwater runoff into marine habitats would be

useful in assessing the impacts of installations such as storm

water drains.

Ward (2000: 436) defined environmental indicators as

“measurable variables that track changes in important ele-

ments, functions or issues in the environment, uses of natural

resources, or management of the environment.” Indicators

should be simple, direct and easy to interpret if they are to be

used in large scale reporting (Ward, 2000). Further, an indi-

cator needs to be specific to the type of pollution concerned.

There is a long history of the use of marine invertebrates as

indicators of the presence and intensity of pollution (Reish,

1972). For example, an increase in the abundance of the poly-

chaete Capitella capitata (Fabricius, 1780) has been shown to

indicate pollution (probably increased nitrates and phosphates)

from domestic outfalls (Filice, 1954; Kitamori and Funae,

1959, 1960; Reish, 1959; Kitamori, 1963; Bellan, 1967).

Imposex in marine gastropods is an indicator of the antifouling

agent Tributyltin (Bright and Ellis, 1989; Stickle et al., 1990;

Nias, 1991; Nias et al., 1993). Filter feeding oysters and

mussels are often used as indicators of lipid-soluble pollutants

S.G. Dunbar, M. Coates and A. Kay

in the marine environment (Riedel et al., 1995; Chen et al.,

1996; Al-Madfa et al., 1998).

Hermit crabs are common in tropical intertidal areas of the

world and occupy the empty shells of marine gastropods (e.g.

Ball and Haig, 1974; Fotheringham, 1975; Abrams, 1981;

Gherardi, 1990; Gherardi and Nardone, 1997; Barnes, 1997).

However, unlike the original gastropod owner of the shell, they

are unable to completely seal off the aperture of the shell in

times of environmental stress, such as dilution of seawater by

fresh water. These factors may make hermit crabs better indi-

cators of changes occurring in intertidal conditions and com-

munity structures than snails, clams and oysters which can

temporarily seal out unfavourable changes in surrounding con-

ditions (Gilles, 1972; Vermeij, 1993; Willmer et al., 2000; and

see review by Underwood, 1979). Further, hermit crabs, like

many other decapods, tend to have a limited capacity for

osmotic regulation. Consequently, they are vulnerable to

osmotic stress caused by freshwater inundation resulting in the

dilution of sea water. Species, however, may differ in their tol-

erance to dilution of their blood and body fluids, and therefore,

in their survival during episodes of freshwater inundation. It is

rather surprising then, that scientific investigations into the use

of hermit crabs as indicators of ecological health are limited to

a single study by Lyla and Ajmal Khan (1996) who used the

estuarine hermit crab, Clibanarius longitarsus (De Haan, 1849)

as an indicator of changes in heavy metals (iron and man-

ganese) in the Vellar estuary, India, over a period of one year.

Lyla et al. (1998) are the only authors, to our knowledge, that

have proposed the use of hermit crabs as test organisms for

detecting environmental impacts.

Clibanarius taeniatus and C. virescens are closely related

species of intertidal hermit crabs common to rocky shores of

tropical eastern Australia. Preliminary observations indicated

that although the two species have overlapping distributions

(Dunbar, 2001), C. virescens dominates open coast areas not

normally influenced by fresh water while C. taeniatus was

more common in areas influenced by fresh water. The present

study was undertaken to document the differences in distribu-

tion of the two species and to determine if the species differ in

their tolerance of osmotic stress. On the basis of the findings of

this study we argue that these two species can serve as an indi-

cator system for the detection of changes that may occur in

rocky intertidal environments caused by storm water runoff

from residential areas.

Materials and methods

Survival tests. Experiments investigated the survival of

C. taeniatus and C. virescens exposed to dilute sea water at

three different temperatures. Hermit crabs were collected from

the field and immediately transported to the laboratory where

they were kept in aquaria under a 12 h light; 12 h dark regime

and acclimated in a constant temperature room at 25±2°C in

36%o sea water for at least 7 days before being exposed to treat-

ment conditions. Individuals were selected for testing without

regard to weight or shell type and no effort was made to sex

individuals. Individual hermit crabs remained in their original

shells throughout the course of the experiments.

Fifteen individuals of each species were randomly selected

and individually placed in 250 ml perspex chambers in 50 ml

of 8%o sea water diluted with distilled, deionised water. The 30

test chambers were then placed into a constant temperature

water bath to maintain a treatment temperature of 15°, 25° or

35° ± 1.0°C. Controls at each temperature were carried out with

15 individuals of each species in 36%o. At irregular intervals

throughout the experiment, hermit crabs were observed for

signs of life. Individuals that did not respond to slight chamber

shaking or abdominal prodding by movement of the pereopods,

antennules or maxillipeds, were considered dead and removed

from the chamber. The interval in which each hermit crab died

was recorded.

Estuarine translocation. Clibanarius taeniatus and C. virescens

were collected from a common intertidal area without respect

to size, shell species or sex. Crabs were transported to the

control and experimental sites in the estuary of the Fitzroy

River, Rockhampton in an open container in approximately 2 L

of 36%o water. Upstream treatment sites were chosen that pro-

vided prolonged exposure to a range of dilute sea water from

7-13%o. Control sites farther downstream were chosen to pro-

vide prolonged exposure to a range of approximately 27-34%o.

At the treatment sites chambers made of PVC pipe and con-

taining either six of each species, or 12 of one species of vari-

able size, shell species and sex were randomly assigned to

seven concrete blocks. Each block had three chambers attached

to it. Chambers were kept just below the surface of the water by

securing them to the top one metre of a length of rope tied to a

concrete block on one end, and a Styrofoam buoy on the other.

Hermit crabs were exposed to experimental conditions for 48 h

(repetition 1) and 28 h (repetition 2). The time of exposure for

repetition 2 was reduced in an effort to increase the number of

animals surviving. The total number of chambers initially

established for the two repetitions was 42, however, seven

chambers were lost during the course of the experiment. At

the control site, four blocks with three chambers each were

initially established as for the treatment sites, giving 12 con-

trol chambers. One control chamber was lost during the

experiment.

Upon retrieval of the chambers, each group of crabs was

placed in a bath of 36%o sea water and given approximately 3

min to revive. Each individual was inspected for signs of life

(as described above). Each hermit crab was used only once.

The total number of “Alive” versus “Dead” of both species for

the 35 treatment and 11 control replicates was analysed by

Chi-squared 2x2 contingency table.

Repeated sampling at selected sites. Two sites within the

Woongarra Marine Park in Queensland were selected for

repeated sampling.

(1) Hoffmans Rocks (24°50.4'S, 152°28.7'E). This rocky

intertidal site is located on an open coast. There are no storm

water drains or natural creeks at this site. This site was divided

into six sectors and at each sampling time tide pools in each

sector were sampled by random collections of between approx-

imately 50 and 200 hermit crabs which were then identified and

counted.

(2) Bauer Street (24°48.9'S, 152°28.0'E). At this site a

Marine hermit crabs as indicators of fresh water

storm water drain carries freshwater runoff from a natural creek

onto a rocky intertidal area. Freshwater flow is continuous but

of low volume except at times of heavy local rainfall. A series

of tide pools extends from the top of the shore at the opening of

the storm water drain to near the bottom of the intertidal area.

The total area here was greater than at Hoffmans Rocks, and so

was divided into nine sectors and at each sampling time tide

pools within each sector were sampled as above. The two sites

were sampled on the same days on 20 February and 20 May

2000 and 23 Mar and 24 Jun 2001.

Survey of Queensland coast. Field surveys of 86 rocky inter-

tidal sites were carried out along the coast of Queensland, from

Redcliffe (27°15.8'S, 153°06.3"E) to Cape Kimberley

(16°16.7'S, 145°29.rE) between March, 2000 and Eebruary,

2001 (Eig. 1). Latitude and longitude were recorded for each

site and, where possible, salinity was recorded. An estimation

of the influence of freshwater inundation on each site was made

on the basis of proximity to rivers, creeks, or storm water drains

according to map locations, data on general directions of wind-

wave currents and personal observations. At each site, surveys

were done at low tide and transects were laid at three different

heights corresponding to low, mid-, and high shore at increas-

Figure 1 . The rocky shore area of Queensland, Australia, covered by

the coastal survey. Inset shows the geographical location of this coastal

region.

ing distance from and parallel to the water line. Ten tide pools

were sampled along each of these transects and the relative

abundances of C. taeniatus, C. virescens, other hermit crab

species and empty gastropod shells were recorded.

Unfortunately, detailed, continuous sea-water and tempera-

ture data were not available for these intertidal sites on the

north-eastern coast of Australia. Nevertheless, inshore sea-

water temperatures can exceed 30°C during summer in these

areas (Eig. 3).

Results

Survival. Eigures 2 A, B and C show the survival of the hermit

crabs Clibanarius taeniatus and C. virescens in 8%o sea water

at 15°, 25° and 35°C. Erom these figures it can be clearly seen

that C. taeniatus survives significantly better than C. virescens

in dilute sea water at all three temperatures. Although both

species have shortened survival times in dilute sea water at the

highest temperature, this was especially detrimental to C.

virescens. Survival for both species is longest at the acclimation

temperature of 25°C. In controls (36%c) at 15° and 25 °C both

species had 100% survival after 83 and 73 h of exposure,

respectively. In 8%c at 35°C, all C. virescens were dead by 16.5

h while 55% of C. taeniatus were still alive (Eig. 2 C). In the

control at 35 °C there was no significant difference in survival

between species up to 29 h (x2i=1.88, P>0.05). After 42 h how-

ever, C. taeniatus had survived significantly better than C.

virescens (x^i=4.26, P<0.05), although 40% of C. virescens

were still alive after 78 h (Eigure 2 D).

Estuarine translocation. At control sites where water was

27-34%o, there was 100% survival of both species over 48 h of

exposure (Table 1). At treatment sites, which were 7-13%o,

30.9% of C. taeniatus survived, while only 0.7% of C.

virescens survived exposure for up to 48 h. These results repre-

sented a highly significant difference 85.84, P<0.001) in

survival between species in favour of C. taeniatus.

Table 1. Results from 11 eontrol replicates and 35 treatment replicates

of the estuarine environment translocation comparing the proportion

surviving between Clibanarius taeniatus and Clibanarius virescens.

Alive

Dead

Total

Controls

C. taeniatus

C. virescens

Treatments

C. taeniatus

C. virescens

298

300

Repeated sampling at selected sites. The results of sampling at

Hoffmans Rocks and Bauer Street are summarised in Table 2.

At Hoffmans Rocks, with no freshwater influence, the percent-

age of C. taeniatus remained low and C. virescens dominated.

Although there was some variation among sampling times at

Bauer Street, the percentage of C. taeniatus remained high at

this freshwater influenced site.

S.G. Dunbar, M. Coates and A. Kay

B D

Figure 2. A. Survival of CUbanarius taeniatus (shaded bars) and CUbanarius virescens (black bars) in 8%o seawater at 15°C. B. Survival of

Clibanarius taeniatus (shaded bars) and CUbanarius virescens (black bars) in 8%o sea water at 25°C. C. Survival of CUbanarius taeniatus

(shaded bars) and CUbanarius virescens (black bars) in 8%o sea water at 35°C. D. Survival of CUbanarius taeniatus (shaded bars) and CUbanarius

virescens (black bars) in 36%o sea water (control) at 35°C.

DATE

Figure 3. Daily shoreline salinity (dark line) and temperature (shaded line) readings between April, 1989, and January, 1992, along Keppel Bay.

Arrows A indicate regular, seasonal flood events on a local scale, arrow B indicates an irregular, flood event on a large, catchment scale. From

Coates, unpublished data.

Marine hermit crabs as indicators of fresh water

Table 2. Relative abundances (%) of Clibanarius taeniatus and

C. virescens at Hoffmans Rocks and Bauer Street. Survey dates and

total sample sizes (N) are indicated.

Survey dates 2000 2001

20 Feb

20 May

23 Mar

24 Jun

Hoffmans Rocks

C. taeniatus

1.8

0.4

3.5

10.1

C. virescens

98.2

99.6

96.5

89.9

1092

782

877

307

Bauer Street

C. taeniatus

47.4

38.3

61.4

55.2

C. virescens

52.6

61.7

38.6

44.8

1119

911

1400

1108

Survey of Queensland coast. Field surveys along a section of

the Queensland coast (Fig. 1) have demonstrated a differential

trend in the distribution of C. taeniatus and C. virescens. In

Table 3 all sites in which C. taeniatus and/or C. virescens were

present have been separated into those sites which are not influ-

enced by fresh water and those which are influenced by fresh

water for prolonged periods by rivers, streams, or storm water

drains. This table clearly indicates that in areas devoid of fresh-

water outfalls, such as Conical L, and open coastline sites such

as Five Rocks and Double Island Point, the intertidal habitat

was completely dominated by C. virescens and no C. taeniatus

were recorded. At sites near rivers, streams, or storm water out-

falls, there was a tendency for there to be a reduction in the rel-

ative abundance of C. virescens and an increase in the relative

abundance of C. taeniatus (Table 3).

Discussion

Laboratory studies indicated a higher tolerance of C. taeniatus,

compared to C. virescens, to dilute sea water over extended

periods of exposure. Survival in dilute sea water was shortest at

the highest temperature, but the combination of low salinity

and high temperature was especially devastating to

C. virescens. Prolonged exposure to low salinity in the field

resulted in a significant difference in survival in favour of

C. taeniatus. Clibanarius virescens showed a much lower tol-

erance to low salinity than did C. taeniatus in an environment

where there was little relief from fresh water. This has signifi-

cance for tropical coastal zones in the vicinity of freshwater

outfalls prone to seasonal flood events. Endean et al. (1956)

recognised that there were many rocky sites along the

Queensland coast that could be affected by fresh water from

nearby river outfalls. Data they obtained indicated that large

enough volumes of fresh water were carried by the Burdekin

and Fitzroy Rivers, in particular, into their respective bays as to

considerably reduce the salinity of nearby coastal waters. They

further emphasised that (of the sites they visited) the areas most

likely to be affected by river outfall would be Point Vernon,

near the Mary River and Yeppoon and Cape Capricorn (Curtis

Island), near the Fitzroy River. Their analysis also showed that

the majority of rainfall occurs over the summer months, during

which time long periods of calm weather in lagoonal areas lead

to relatively little mixing and surface salinities that are fre-

quently low. Daily records collected by Coates (unpublished

data) showed that shoreline salinity in Keppel Bay (23°23.7"S,

150°53.4"E) was reduced by both local, seasonal flooding (Eig.

Table 3. Relative abundances (%) of Clibanarius taeniatus and C. virescens at sites along the eastern coast of Queensland, Australia. Sites have

been divided into those with no freshwater influence and those influenced by fresh water, and are arranged from south (top) to north (bottom).

Site Latitude, Longitude Salinity (%o) C. taeniatus C. virescens

Not Influenced by Fresh Water

Wickham Pt

26°48.2'S, 153°08.8^E

100

Moffat Head

26°47.5'S, 153°08.9T

0.6

99.4

Pt Cartwright

26°40.7'S, 153°08.3'E

100

Alexandra Headlands

26°40.3'S, 153°06.6T

100

Double Island Pt

25°56.2'S, 153°11.3'E

100

Woongarra Marine Park

24°50.4^S, 152°28.7^E

7.0

93.0

N Middle Rock

24°17.0'S, 151°57.LE

100

Rocky Pt

24°14.0'S, 151°56.2'E

100

Yellow Patch

24°30.4'S, 15L13.3T

38.2

44.4

55.5

Cape Capricorn (Curtis I.)

23°29.LS, 151°13.9T

38.2

100

Long Beach (Great Keppel I.)

23°11.6'S, 150°50.8'E

100

W. Shellving Bch (Grt Keppel I.)

23°11.3'S, 150°50.6^E

100

E. Shellving Bch (Grt Keppel I.)

23°11.2'S, 150°50.6'E

100

Conical I.

23°03.3^S, 150°52.7^E

100

Five Rocks

22°48.LS, 150°48.5^E

0.1

99.9

Lamberts Beach

21°03.8'S, 149°13.5T

19.4

80.6

Pandanas Bay (Long I.)

20°20.4^S, 148°51.0^E

3.3

96.7

Back Beach (Long I.)

20°20.2'S, 148°51.3'E

3.6

96.4

Bauer Bay (S Mole I.)

20°15.6'S, 148°50.LE

100

Horseshoe Bay

19°58.7^S, 148°15.7'E

2.2

97.8

Bingil Bay

17°50.rS, 146°06.0T

100

Nudey Beach (Fitzroy I.)

16°56.2'S, 145°59.0'E

100

N Welcome Bay (Fitzroy I.)

16°55.9'S, 145°59.3'E

100

N Ellis Beach

16°42.9^S, 145°39.LE

100

Port Douglas

16°29.rS, 145°28.2'E

29.9

1.0

99.0

Dayman Pt

16°22.9'S, 145°24.9'E

100

S.G. Dunbar, M. Coates and A. Kay

Table 3 — Continued.

Site

Latitude, Longitude

Salinity (%o)

C. taeniatus

C. virescens

Influenced by Fresh Water

Woody Pt (Moreton Bay)

27°15.8'S, 153°06.3T

100

S Scott Pt (Moreton Bay)

27°15.3'S, 153°06.6T

100

N North Bluff (Big Woody I.)

25°16.4'S, 152°56.8T

100

Datum Pt.(Big Woody I.)

25°16.3^S, 152°56.6'E

100

Sandy White Memorial Park.

25°16.3'S, 152°50.0'E

100

The Gables (Pt Vernon)

25°14.8'S, 152°49.6T

100

Burmm Heads

25°11.0'S, 152°36.9^E

100

Elliott Heads

24°55.2^S, 152°29.6'E

79.8

20.2

Bargara (2nd Storm Drain)

24°48.9^S, 152°28.0T

35.5

38.1

61.9

Bargara (N. of Bauer St.)

24°48.8'S, 152°27.8^E

35.7

47.1

52.9

Burnett Heads (middle)

24°46.rS, 152°25.rE

95.9

4.1

Burnett Heads (N. end)

24°45.7^S, 152°24.9'E

69.5

30.5

Turkey Beach

24°04.4^S, 15r39.LE

100

Parsons Pt

23°51.2^S, 151°17.4'E

100

Emu Pt

23°15.5'S, 150°50.0^E

34.4

76.0

24.0

S Cooee Bay

23°08.5^S, 150°45.7'E

35.5

76.0

24.0

Eishermans Beach

23°08.5'S, 150°45.7'E

35.2

87.8

12.2

Clairview

22°07.0'S, 149°32.2^E

100

Zelma Beach

21°21.6^S, 149°18.7'E

89.6

10.4

S Hay Pt

2ri7.8^S, 149°17.6'E

85.3

14.7

Dudgeon Pt

21°14.8'S, 149°15.2'E

84.6

15.4

Slade Bay

2r04.3^S, 149°13.rE

100

Mast (Slade Pt)

2r03.9'S, 149°13.4'E

100

Dolphin Heads

2r02.0^S, 149°ll.rE

89.3

10.7

St Helens Beach

20°49.4^S, 148°50.2T

23.3

100

Midge Pt

20°38.9'S, 148°43.6^E

32.2

93.7

6.3

Tooloakea

19°08.7^S, 146°34.9'E

28.8

100

3, arrows A) as well as large, irregular catchment scale flood-

ing (Fig. 3, arrow B). During the latter event, Coates (1992)

found that salinities less than 15%o persisted on rocky shores in

that area for up to 13 days. In addition, it can be seen by inspec-

tion of Figure 3, that low salinities can coincide with peak

summer temperatures, resulting in the combined stress of low

salinity and high temperature.

Sampling over time at a site with no freshwater influence

and a site influenced by fresh water showed that C. taeniatus

had a low relative abundance at the former, where C. virescens

dominated, but had a high relative abundance at the latter. Field

surveys along the Queensland coast found that in intertidal

areas along the open coast, with no freshwater influence,

C. virescens was highly abundant while C. taeniatus was in

low abundance, or absent. However, at sites influenced by

freshwater flows there were high relative abundances of

C. taeniatus.

On the basis of the present study we suggest that C. taenia-

tus is adapted to intertidal areas which experience some fresh-

water flow over the long term. Clibanarius virescens, on the

other hand, although intolerant of fresh water, dominates over

C. taeniatus in areas without freshwater influence. Further

research is required to determine why C. virescens is dominant

in areas without freshwater influences. In addition to fresh-

water, factors such as differences in feeding behaviours and the

availability of food sources may also play very important roles

in affecting the large scale distribution of C. taeniatus and

C. virescens. Kunze and Anderson (1979) found that these

particular species had slight differences in their feeding mech-

anisms. They reported that C. taeniatus is predominantly a soft

food detritivore, while C. virescens is both detritivorous and

macrophagous and uses the chelae and crista dentata for tri-

turition. Clibanarius taeniatus does not appear to use the

chelipeds to tear Zostera sp. seagrasses apart, unless the tissue

is decayed and already breaking down. Instead, this species

uses the chelipeds to scrape epiphytic algae from the laminae of

Zostera sp. (Kunze and Anderson, 1979). The geographical dis-

tribution of C. taeniatus and C. virescens may also be affected

by the ability of larval recruits to detect, avoid or survive low

salinity waters. It has become increasingly clear that the larvae

of a great many marine invertebrates are not only able to dis-

criminate between favourable and unfavourable habitats

(Levinton, 1995; Willmer et al., 2000 and see review by

Morgan, 1995), but are also able to delay metamorphosis under

unfavourable conditions (see review by Crisp, 1976).

In areas experiencing increased freshwater influence it is

expected that there will be an increase in the relative abundance

of C. taeniatus and a concomitant decrease in the relative abun-

dance of C. virescens. These species therefore constitute a use-

ful indicator system of new, long-term sources of freshwater

inundation, whether natural or anthropogenic, in intertidal

areas.

Intertidal hermit crabs are relatively easy to sample and

identify in the field and are common in tropical intertidal areas.

With increased residential and commercial development in

tropical coastal areas, storm water runoff has the potential to act

Marine hermit crabs as indicators of fresh water

as a “pollutant” in intertidal areas. The presence of an easy to

use indicator system, such as the one described here, constitutes

a valuable tool for managers responsible for the well being of

coastal areas. It would be most interesting to trial this system

by monitoring the site of a proposed coastal development

where C. virescens is highly abundant, both prior to and after

the introduction of storm water drains.

There is evidence that other pairs of hermit crab species in

Other areas have similar distribution patterns to C. taeniatus

and C. virescens (Ball and Haig 1974; Abrams 1980; Bertness

1981; Gherardi and Nardone 1997; Barnes 1997; Turra and

Leite 1999). We suggest that it would be worthwhile to deter-

mine if such similarly distributed pairs of hermit crab species

would also constitute indicator systems on other tropical coasts

where there is a potential threat from residential storm water

runoff.

Acknowledgements

SGD wishes to extend special thanks to Sabine Dunbar who

assisted in surveys at many of the sites. Thanks also to Owen

Witt, John Williams, Megan Dale and Kevin Strychar for assis-

tance with field surveys. Jason Scriffignano is thanked for his

assistance with mapping. This work was supported by a

Cooperative Research Centre for Coastal Zone, Estuary and

Waterway Management (CRC CZEWM) scholarship to SGD, a

CQU Centre for Land and Water Resource Management

(CLWRM) grant to MC, and a CQU Merit grant to MC.

Collections of hermit crabs in the Woongarra Marine Park were

made as part of the Rocky Reef Watch Project of Queensland

Parks and Wildlife Service coordinated by AK.

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Memoirs of Museum Victoria 60(1): 35-44 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

Hermit crab population ecology on a shallow coral reef (Bailey’s Cay, Roatan,

Honduras): octopus predation and hermit crab shell use

Sandra L. Gilchrist

New College of Florida, 5700 N. Tamiami Trail, Sarasota, Florida 34243, USA (gilchrist@ncf.edu)

Abstract Gilchrist, S.L. 2003. Hermit crab population ecology on a shallow coral reef (Bailey’s Cay, Roatan, Honduras): octopus

predation and hermit crab shell use. In: Lemaitre, R., and Tudge, C.C. (eds). Biology of the Anomura. Proceedings of a

symposium at the Fifth International Crustacean Congress, Melbourne, Australia, 9-13 July 2001. Memoirs of Museum

Victoria 60(1): 35-44.

Shells can be a limiting factor in allowing hermit crab populations to increase. Predators of gastropod molluscs and of

hermit crabs release shells into reef environments where hermit crabs find and cycle them within their populations.

Predators also play a role in distributing shells among hermit crab species. To highlight how octopuses influence shell

availability to hermit crabs, observations were made on members of Octopus vulgaris Cuvier, 1797 and O. briareus

Robson, 1929 at Bailey’s Cay Reef (Roatan, Honduras) during July and August each of three years, 1999-2001 . In addi-

tion to feeding while foraging. Octopus vulgaris and O. briareus individuals create shell and debris middens outside of

their temporary dens. These middens concentrate shells and food for hermit crabs in the reef environment where locat-

ing an empty shell could be difficult. However, because hermit crabs are prey items for octopuses, hermit crabs using the

middens risk predation from the den occupant. Relatively small hermit crab species such as Pagurus brevidactylus

(Stimpson, 1858) and P. criniticomis (Dana, 1852) were found commonly in dens and among middens, opening the

possibility that the den functions as a refugium for some species as well.

Keywords Cmstacea, Anomura, hermit crab, predation, shell use, octopus

Introduction

Hermit crabs generally do not procure shells directly from live

molluscs (Hazlett, 1981; for an exception see Rutherford,

1977). Recycling of postmortem shells from gastropods and

from live or postmortem hermit crabs is common (Bertness,

1982; Wilber and Herrnkind, 1984). Because shell availability

has been shown to be important in determining hermit crab

population size, hermit crab shell use has been widely investi-

gated both in the lab and in the field (Benvenuto and Gherardi,

2001; Elwood et al., 1979; Garcia and Mantelatto, 2001; Hahn,

1998; Hazlett, 1996; Osorno et al., 1998; Siu and Lee, 1992;

Vance, 1972 inter alia). Predators on gastropods and hermit

crabs provide a variety of shells for habitation by hermit crabs

(Carikker, 1981; Mather, 1991; Tirelli et al., 2000). Sustainable

recycling requires hermit crabs to assess continually the quali-

ty of resources within the recycle pool. Some predators leave

shells intact with little apparent damage (Gilchrist, 1984; Jory

and Iversen, 1983; Ray and Stoner, 1995) while other predators

crush or smash the shells beyond use for hermit crabs (Brown

et al., 1979; Hsueh et al., 1992; Hughes, 2000; Seed and

Hughes, 1995; Vermeij, 1977; Yamada and Boulding, 1998).

However, LaBarbera and Merz (1992) noted decreases in shell

strength after removal of the living gastropod, suggesting that

even intact shells begin deterioration upon entering the hermit

crab use cycle.

The cycle of shells among gastropods and hermit crabs is

not well known in coral reef environments. Octopuses consume

both crustaceans and molluscs, making their potential impact

on hermit crab shell cycling complex. They can prey upon her-

mit crabs as well as crustaceans that are hermit crab predators.

In addition, they not only consume gastropods that can provide

shells for hermit crabs, they also carry prey from various parts

of the reef back to a den location. Mather et al. (1997) specul-

ated that hermit crabs are sometimes associated with octopus

dens as scavengers opportunistically feeding on remains of

prey left in middens and dens. Some workers have indicated

hermit crabs as prey items for octopuses in field studies

(Iribarne et al., 1993) while other researchers have used hermit

crab zoeae as prey in food searching studies of octopus par-

alarvae (Navarro and Villanueva, 2000; Villanueva et al.,

1996). Octopuses can crush or drill their prey. They may also

extract gastropod or hermit crab prey through shell apertures,

leaving a relatively intact shell. The fact that octopuses not only

feed on hermit crabs, but can also concentrate shell and food

resources in middens formed outside of their dens suggested

that their role in the cycling process should be examined more

S.L. Gilchrist

closely in the reef system. The types of shells entering the her-

mit crab shell cycle for this study were noted at Bailey’s Cay

reef by observing octopuses in the field to determine thek role

in the hermit crab shell cycle.

Methods

Description of sampling area. The eastern reef area surround-

ing Bailey’s Cay provides an opportunity to examine the hermit

crab shell cycle under field conditions. The Cay is located with-

in the Roatan Marine Preserve, so no spearfishing is allowed in

the area and only artisanal line fishing from traditional canoes

is permitted. Bailey’s Cay is part of a collapsed volcanic ridge

surrounded by patch reefs to the east ending with a reef wall

that drops nearly vertically to about 30 m. There is a wall that

drops vertically to 35 m with a narrow shelf to the north. A boat

channel about 15 m deep between Bailey’s Cay and Roatan

bounds the southern part of the reef. Thus, because of the water

depth surrounding the reefs of the cay, once hermit crabs and

molluscs metamorphose from the plankton, they are surround-

ed by deeper water, restricting movements from the area.

General octopus foraging observations. Octopuses were active

both day and night. They were observed using focal animal and

focal area techniques (Altman, 1974) during July and August of

1999-2001 at the same area of the eastern reef of Bailey’s Cay.

The sampling area was approximately 5000 m2, extending from

shallow seagrass through the top of the forereef.

Though observations were made on octopuses and their

dens in the same area for three years, it is unlikely that the

octopuses were the same individuals each year. The life span of

these animals is limited and they grow rapidly (Hanlon, 1983).

The size of each octopus observed was small (3-5 cm head

diameter; estimated using the methods described by Aronson,

1982), suggesting that they were juveniles. To facilitate obser-

vations, dens of octopuses in the sampling area were identified

and marked discreetly. Observation areas were chosen where

the minimum distance between conspecific dens was 5 m while

minimum distance for different species was approximately 12

m for octopuses observed in 1999-2001. Obseiwers using

SCUBA or snorkeling remained at 2-3 m from foraging octo-

puses. Only animals that habituated to presence of observers

were used for collecting foraging data. (The area is frequented

during the day by recreational snorkelers and swimmers, thus

octopuses are not in an isolated habitat). Colour changes and

movements of octopuses were clearly visible from 3 m. The

visibility was determined by horizontal and vertical secchi

measurements.

In July- August of each year, 5-7 octopuses were identified

for behavioural observations. However, only data for 3 individ-

uals of O. vulgaris were analyzed each year because some octo-

puses were eaten by moray eels or were injured during the

sampling period. Each year, 3 individuals were each followed

for at least 20 minutes for each of three consecutive days (60

minutes total for each) as they emerged from their dens, gener-

ally in late afternoon or early evening. Individuals of O. bri-

areus (one in 1999 and two each in 2000 and 2001 which sur-

vived the entire sampling period without injury; 5 total) were

observed most often in early evening and at night; they were

rarely active outside of the den during daylight hours. Each

animal was observed for a minimum of 20 minutes and a max-

imum of 30 minutes as it emerged from the den and proceeded

with foraging for each of 3 consecutive days. Civil dusk in the

area occurs around 7:30 CST during July and August. Lights

were used after civil dusk. These lights were not directly

applied to octopuses as they foraged. Indirect lighting did not

result in colour changes by the octopuses and the animals con-

tinued to forage for several hours. The observations of foraging

allowed establishment of general feeding areas, feeding

duration and habitats visited. Remains discarded by foraging

O. vulgaris and O. briareus individuals were collected and

categorised by shell type, organism consumed. Characteristic

behaviours exhibited by octopuses described by Hanlon and

Messenger (1996) and Mather (1991) were used to suggest

items eaten away from the den, though specific numbers from

foraging were not determined over the enthe foraging time of

octopuses in this study. Postmortem gastropod shells were

identified by remains of muscles or flesh attached to shells.

Gastropod shells recovered with no remaining flesh were cate-

gorised as formerly occupied by hermit crabs. Gastropod shell

fragments were noted separately because former occupant

could not be determined clearly for most fragments. A shell was

considered a fragment for this study if at least two whorls

beyond the protoconch were intact.

Hermit crab observations at octopus dens. After establishing

den areas and general foraging patterns for O. vulgaris, remains

in middens were collected and catalogued daily for seven con-

secutive days. Octopus briareus individuals generally con-

sumed prey while hunting (about 80% eaten away from the

den), however, the small middens formed by these animals

were also sampled for seven consecutive days. Two active dens

of O. vulgaris and one of O. briareus were selected in August

2001 for more focused hermit crab observations.

Active den sites for both octopus species were observed for

hermit crab activity every 30 minutes for a two-hour period

starting an hour before sunset. A circular area of one-metre

diameter was outlined around each den using plastic tent pegs

driven into the substrate. The 1-m area was considered the den

area while the den was the physical shelter used by the octopus.

As background information, two circles with 1 m diameters

were marked elsewhere in the seagrass and in the coral rubble

to examine hermit crab activity independent of the den sites.

Hermit crabs found in the den area and around octopus dens

were removed after the octopus left for a foraging bout. The

background areas were sampled for hermit crabs around the

same time. Live gastropods and postmortem shells were also

collected within the den, den area, and background sites.

Hermit crabs were removed from the den sites for seven con-

secutive days. Marked crabs in marked shells were returned to

their original collection areas each day. Dactyls were clip-

coded (Gilchrist, 1984) to allow recognition of returned hermit

crabs. Hermit crab species were identified and individuals with

their shells were measured using plastic calipers (precision 0.01

mm) and marked. Postmortem gastropod shells and live

gastropods were marked.

Hermit crab ecology on a shallow coral reef

In a previous study (Gilchrist, 2000), shield length was

found to have the highest correlation (0.78) with shell width (an

indicator of shell size) for all hermit crab species combined, so

shield length is used to indicate hermit crab size in this study.

Gastropod shell length, shell width from center axis, shell aper-

ture length and shell aperture width were measured for all intact

shells (those used by hermit crabs, live gastropods, and post

mortem gastropod shells). In addition, number of disassociated

gastropod opercula at the site was determined and these

opercula were removed.

Other researchers have noted that field observations of octo-

puses generally yield few data (Forsythe and Hanlon, 1997),

confining short-term studies to descriptive analyses. Thus, data

were collected to show general trends in contributions to the

hermit crab shell cycle for this study.

Results

General observations. Dens of Octopus vulgaris were mainly

among isolated coral heads or dead coral within the grassbed

while those of O. briareus were sometimes found in isolated

coral heads but were most often located in crevices within the

forereef. The average water depth for the dens of O. vulgaris

sampled in this study was 20±3 cm while the average for those

of O. briareus was 41 ±5 cm. Mather et al. (1997) and Forsythe

and Hanlon (1997) noted that some octopuses modify habitats

in den construction. Dens in the grassbeds were modified by the

octopuses that placed rubble, large shells, and other materials

around the den opening. Typically, a shell or other object was

held by the octopus resident to block the den opening partially.

Some excavation was also observed for O. vulgaris individuals.

Dens of O. briareus did not show similar modifications; indi-

viduals of this species seemed to find a crevice and to use this

area with little modification. Individuals of O. vulgaris were

observed clearing their dens of materials frequently while

individuals of O. briareus were not noted for removing items

from the dens. During the sampling periods each year, members

of O. vulgaris showed den fidelity, returning repeatedly to the

same dens (it is unclear whether the same octopus returned

to the den, but an animal of similar size returned to the den)

while O. briareus individuals used a single den primarily,

but also sheltered periodically at secondary den sites,

returning to the primary den after a few days. Because of

differences in den use, data for O. briareus were more difficult

to obtain.

Visibility at the site as measured by horizontal and

vertical secchi was in excess of 30 m each of the sampling

days.

Octopus foraging observations. Feeding ranges for the O. vul-

garis individuals each year were generally ovoid, encompass-

ing seagrass areas, isolated coral heads, and patch reefs. The

majority (70-80%) of foraging time was spent in seagrass and

coral rubble. At least one octopus each year was eaten or

injured by an eel (green moray Gymnothorax funebris,

Ranzani, 1840) when foraging in the forereef while no deaths

or major injuries (such as loss of an arm) were observed for

octopuses foraging in seagrass and coral rubble. Descriptions

of feeding behaviours are modified from those made by Mather

(1991). The most common feeding behaviours in the seagrass

were “webover” (body web and arms spread out to form sac

over part of the environment, typically accompanied by a

blanching of web if prey captured) and “crawl-poke” (moving

while exploring substrate with one or more arms, stopping

periodically to probe among seagrasses, into holes or around

objects). When foraging away from the den in the seagrasses

and surrounding rubble, individuals of O. vulgaris concen-

trated feeding on Calappa flammea (Herbst, 1794), Hepatus

epheliticus (Linnaeus, 1763), Cataleptodius floridanus

(Gibbes, 1850), Eurypanopeus dissimilis (Benedict and

Rathbun, 1891), Mithraculus forceps (A. Milne Edwards,

1875), Oliva sp., chitons (including Tonicia elegans (Frembley,

1827) and Craspedochiton hemphilli (Pillsbry, 1893)), a variety

of clams such as Macrocallista maculata Linnaeus, 1758 and

Nucula proxima Say 1822, and gastropods such as Modulus

modulus (Linnaeus, 1758), Natica livida Pfeiffer, 1840 and

Cerithium atratum (Born, 1778) based on observations of prey

struggling beneath the web and remains observed. As noted by

Forsythe and Hanlon (1997) for another octopus species,

individuals of O. vulgaris were followed by wrasses

{Thalassoma bifasciatum (Bloch, 1791) and Halichoeres bivi-

tattus (Bloch, 1791)) during foraging, with fish snapping at

material around the octopus and the octopuses seemingly

ignoring the fish. Octopuses were not observed eating fish

while foraging.

On the coral heads and patch reefs, crawl-poke and web-

over were commonly observed behaviours of individuals of

O. vulgaris. Chitons (primarily Acanthochitona spiculosa

Reeve, 1847, Chiton tuberculatus Linnaeus, 1758 and

Acanthopleura granulata (Gmelin, 1791)) and individuals of

Mithraculus forceps were typical prey. “Tuck-hold” behaviour

where the octopus held a large prey item under the web

(evidenced by one or two arms folded at their bases and a bulge

or movement under the web), was more frequent near den sites

while “pull-tuck-consume” where the animal is using the

suckers at the base of the arms to pull apart a clam or to hold a

prey while tearing or drilling (evidenced by shortening of arms,

blanching of web, and remains jettisoned; see description given

in Nixon and Maconnachie, 1988) was observed away from the

den. Only two O. vulgaris individuals were directly observed

eating hermit crabs while foraging among coral. In both

instances (occurring during August 2000), the hermit crabs

were Paguristes puncticeps Benedict 1901 (confirmed from

examining discarded appendages and shields) in shells of juve-

nile (less than 45 mm shell length; Stoner et al., 1998) Strombus

gigas Linnaeus, 1758. One octopus consumed a mean of 8 her-

mit crabs/foraging bout and the other ate a mean of 14/foraging

bout. Other prey items were captured by O. vulgaris indi-

viduals and returned to their dens for consumption. Table 1

shows the observed numbers of hermit crabs eaten by octopus-

es while foraging along with the relative condition of the shell

released during the observation periods. By far, the most

common method used by the octopuses for feeding on hermit

crabs was removal through the shell aperture, resulting in a

shell with little visible damage.

SI. Gilchrist

Table 1. Numbers of shells from hermit crab (HC) and gastropod (G) prey after predation by octopuses for 1999-2001 foraging observations in

seagrass, patch reef, reef and forereef areas combined. The number of octopuses included in the observations is given in parentheses. Shell frag-

ments (F) that contain the apex are noted. Numbers of predators are given in parentheses. For octopuses, data reflect only prey not returned to

dens. Category 1 - no damage, category 2 - aperture chipped, category 3 - body whorl peeled, and category 4 - apex removed or shell crushed.

Shells reused by hermit crabs (RS) are given for each category. Two hermit crabs escaped from an individual of O. vulgaris.

Predator species

Shell condition by category

HC G RS

Octopus vulgaris (9)

9 3 1

Octopus briareus (5)

0 3 0

Table 2. Middens formed by Octopus species (where prey is

at least 5% by number of midden content for all dens combined; listed with most

common item first; modeled after Mather, 1991) returning from foraging. Hermit crab species are indicated by an asterisk.

1999

2000

2001

Macrocallista maculata

Natica livida

Oliva sp.

Leucozonia nassa

Cerithium atratum

Oliva sp.

Echinometra lucunter

OCTOPUS VULGARIS

Crustaceans

Pitho sp.

Mithraculus forceps

Calappa flammea

Calappa gallus

Hepatus epheliticus

Cataleptodius floridanus

Eurypanopeus dissimilis

*Dardanus venosus

*Paguristes puncticeps

Molluscs

Nucula proxima

Natica livida

Macrocallista maculata

Oliva circinata

Acanthochitona spiculosa

Modulus modulus

Echinoderms

Pitho sp.

Mithraculus forceps

Cataleptodius floridanus

Calappa gallus

*Paguristes puncticeps

*Calcinus tibicen

*Paguristes cadenati

Macrocallista maculata

Acanthochitona spiculosa

Natica livida

Leucozonia nassa

Cerithium atratum

Oliva sp.

Pitho sp

Mithraculus forceps

Calappa gallus

*Calcinus tibicen

*Paguristes puncticeps

OCTOPUS BRIAREUS

Crustaceans

Mithraculus forceps

Calappa flammea

*Paguristes puncticeps

Molluscs

Macrocallista maculata

Conus mindanus

Echinoderms

Mithraculus forceps

Acantochitona spinculosa

Cyphoma gibbosum

Tripneustes ventricosis

Echinometra sp.

Mithraculus forceps

Eurypanopeus sp.

Calappa flammea

Calappa gallus

Macrocallista maculate

Acanthochitona spincul

Tripneustes ventricosis

Echinometra sp.

Individuals of O. briareus also exhibited an ovoid feeding

range each year, overlapping the areas where O. vulgaris indi-

viduals had dens and did their foraging. However, O. briareus

individuals concentrated their feeding among the patch reef

corals and forereef areas using crawl-poke behaviour. When

moving between seagrass and coral patches, these octopuses

swam short distances, blended with the substrate, and swam

again, repeating this until reaching the seagrass. Rarely did

individuals crawl on the open substrate between patch reef

corals and the seagrass. Snake eels {Ophichthus cruentifer

(Goode and Bean, (1896)) and green morays (Gymnothorax

funebris) were observed eating O. briareus individuals as well

as biting off arms both in dens and while foraging. Some for-

aging occurred in seagrasses where the webover was most com-

mon behaviour, and Calappa flammea and C. gallus (Herbst,

1903) were most often consumed. Appendages from

Mithraculus species and Pitho species were also found after

octopuses captured prey, as were shells and remains from

Strombus gigas and Leucozonia nassa (Gmelin, 1791).

Individuals of O. briareus were observed consuming hermit

crabs each year. One octopus in the 2001 sampling season was

seen eating 3 hermit crabs during a single feeding bout. All of

Hermit crab ecology on a shallow coral reef

the hermit crabs eaten were Paguristes puncticeps in Strombus

gigas shells. Each hermit crab consumed was eaten away from

the den, apparently being extracted through the shell aperture

(Table 1). Appendages were jettisoned as the hermit crabs were

consumed and the shells were left behind. Postmortem shells

were used by hermit crabs (Table 1) which sometimes brought

the shells liberated from octopus foraging back to the den site.

Observations at octopus dens. Octopuses at dens had post-

mortem gastropod shells (from hermit crabs or from gas-

tropods) comprise least 40% (by number) of their midden and

den area contents for each of the three years surveyed in this

study. It was difficult to determine how many hermit crabs were

consumed at dens because remains were primarily appendages

and a few shields. Table 2 lists the types of remains recovered

in the octopus middens and den areas. During 2001, only one

O. briareus individual accumulated a large amount of hermit

crab material in its midden and den area (72% by weight). One

of the shells in its midden had been marked from a den in the

2000 sampling year, presumably worn by a hermit crab that had

been eaten or that had exchanged a shell at the midden in 2001.

The octopus had a small head diameter (about 3 cm) and was

the smallest specimen observed in the area. However, this indi-

vidual was eaten before the end of the observation period and

was not considered in the final analyses of den materials.

Live hermit crabs were found in dens and around middens

(Table 3) of O. vulgaris and O. briareus. Two hermit crab

species, Pagurus criniticornis and P. brevidactylus, were found

in and around dens commonly. These species are considered

den associates. Individuals of P. criniticornis (mean shield

length 3.1 ±0.6 mm) were found most often within O. vulgaris

dens and middens. Individuals of P. criniticornis represented

the largest group of hermit crabs associated with dens (Table 3).

Some individuals exchanged shells for those discarded by an

octopus in a midden (Table 4). Individuals of P. criniticornis

were observed feeding on remains of prey left by octopuses

both in the den and at the middens. Some individuals of

P. criniticornis remained in the den and midden area for all

seven sampling days. Individuals of P. brevidactylus (mean

shield length 4.2±0.3 mm) were also found inside dens of

O. vulgaris within the seagrass area. These species of hermit

crab occupied dens and middens primarily found in seagrass

areas, however, dens in coral were difficult to observe fully.

Individuals of P. brevidactylus observed in and around dens of

both octopus species did use shells procured by the octopuses

(Table 4). Only about 23% of the crabs occupying shells and

fragments were new to the den sites over the entire time period

sampled.

Four Other hermit crab species, Paguristes puncticeps,

Paguristes cadenati Forest, 1954, Calcinus tibicen (Herbst,

1791), and Phimochirus holthuisi (Provenzano, 1961), were

visitors to dens and middens, but were considered den/midden

transients. They did not remain at the den sites or middens for

more than 1-2 days. Paguristes puncticeps (mean shield length

13.3±3 mm) and C. tibicen (mean shield length 13.7±4 mm)

individuals were found almost exclusively in den and midden

areas of O. vulgaris individuals located on patch reefs and in

the fore reef. However, there was a difference in the sizes of

Table 3. Median number per day of live hermit erabs, mollusc shells,

and opercula found at den sites of Octopus vulgaris (two den areas

observed seven days), O. briareus (one den area observed seven days)

and two background areas in August 2001. Opercula were also count-

ed, marked and returned because muscle still attached that could serve

as a hermit crab attractant. D = den, M = midden, B = background.

0. vulgaris

0. briarius

Hermit crabs

Calcinus tibicen

Paguristes cadenati

Paguristes puncticeps

Phimochirus holthuisi

Dardanus venosus

Petrochirus diogenes

Pagurus criniticornis

Pagurus brevidactylus

Mollusc shells

Macrocallista maculata

Acanthochitona spinculosa

Cyphoma gibbosum

Natica livida

Nucula proxirna

Oliva sp.

Oliva circinata

Modulus modulus

Glyphoturris rugima

Polinices lateus

Leucozonia nassa

Astraea tecta

Cymatium partenopeum

Cerithium atratum

Strombus gigas

Trignostoma pulchra

Opercula

Table 4. Hermit crabs occupying shells and fragments returned to three

octopus dens (two O. vulgaris and one O. briareus) over a seven day

period in August 2001 . The total includes cumulative number of her-

mit crabs each day, thus some individuals are counted more than one

time in the total. Hermit crabs counted more than once are indicated

in parentheses. A = total observed around dens and middens, B = in

shells from middens, C = in fragments from middens

Calcinus tibicen

43 (7)

9(2)

Dardanus venosus

7(2)

Paguristes cadenati

31(3)

4(1)

Paguristes puncticeps

87 (11)

12(1)

2(1)

Pagurus brevidactylus

238 (71)

27(4)

9(6)

Pagurus criniticornis

371 (112)

52(15)

35 (11)

Petrochirus diogenes

Phimochirus holthuisi

39 (3)

7(1)

hermit crabs inside the dens and in the den/midden area. The

P. puncticeps individuals collected from inside the dens of the

O. vulgaris individuals were all relatively small (mean

shield length <5 mm) while those found in the middens and

S.L. Gilchrist

surrounding areas were larger (mean shield length >17 mm).

Most hermit crabs found with O. briareus were collected from

the middens, rarely within the dens. Dens were generally with-

in coral crevices and were hard to access. Phimochirus

holthuisi (mean shield length 6.5±2 mm) and Paguristes punc-

ticeps individuals were observed feeding on prey remains from

both species of octopuses as well as taking shells from the

middens. Individuals of Petrochirus diogenes (Linnaeus, 1758)

and Dardanus venosus (H. Milne Edwards, 1848) were not

observed taking shells or fragments from the sites.

Transient hermit crab species commonly removed shells

from middens of both octopus species, but did not change

shells at the midden site. Thus, a shell was not deposited back

into the midden if a shell exchange occurred.

The control areas sampled near the dens yielded small

numbers of live gastropods, gastropod shells and hermit crabs.

The controls were in seagrass and patch reef/rubble/reef areas.

The largest number of gastropods found per square m was

seven while the largest number of herTnit crabs collected per

square m was eight. Consistently, control area in seagrass beds

yielded hermit crabs and gastropods while the one located in

patch reef/coral rubble/reef had few, if any, hermit crabs or gas-

tropods visible. In sandy areas among the rubble and patch

reefs, both hermit crabs and gastropods tended to bury. The

highest number of empty shells per square m in either of

the control areas was 13; these were mostly small specimens

(<0.5 cm) of Cyphoma gibbosum (Linnaeus, 1758) (a shell not

often occupied by hermit crabs at this site), Conus mindanas

Hwass, 1792, Glyphoturris rugirinia (Dali, 1889), and

Cerithium atratum (Table 2).

Discussion

Octopus vulgaris and O. briareus individuals feed opportunis-

tically, consuming some prey while foraging and other prey at

their dens. Hermit crabs formed a part of the diet both during

foraging and at the dens. Some octopuses in the present study

seemed to specialise on molluscs while others most frequently

discarded remains of crustaceans. Octopuses reared in the lab-

oratory feed preferentially on crustaceans (Boletzky and

Hanlon, 1983), though molluscs and other prey also are con-

sumed readily. Some species of octopods use the radulae and

beak to rasp holes in mollusc shells or operculum (Arnold

and Arnold 1969; Wodinsky, 1969) and crustacean prey (Boyle

and Knobloch, 1981). Octopuses that drill take much longer to

handle prey than those that pull open shells (Fiorito and

Gherardi, 1999). The differences in handling time for prey

items varies, typically with crustaceans requhing less handling

than molluscs. Some crustaceans and gastropods are crushed by

octopus beaks (Ambrose, 1986; Voight, 2000) while others are

envenomated. Crustaceans may be envenomated through the

eye (Giisley et al., 1996) or other less chitinous body regions,

making it difficult to determine cause of death from remains.

However, in the present study, some crustaceans also escaped

from octopuses, suggesting a trade-off for octopuses in con-

sumption and handling. Hermit crabs occupying thick shells

into which they could withdraw completely posed a challenge

for the octopuses, requiring drilling of the shells to access the

hermit crabs. Some hermit crabs were abandoned by the forag-

ing octopuses as prey in this study, although hermit crabs in

thick shells such as Strombus were also pulled out through the

shell apertures as well. Other researchers have noted that

removal of both hermit crabs and gastropods through the aper-

ture is a common feeding strategy for octopuses (Brooks and

Mariscal, 1985; Fawcet, 1984).

Postmortem shells from both molluscs and hermit crabs

released by individuals of O. vulgaris and O. briareus observed

foraging around Bailey’s Cay were typically not drilled, though

drilling is a well-documented feeding strategy for these species

of octopuses (Nixon, 1987). Drilling often takes more time than

other feeding strategies. For some species of hermit crabs

(Pechenik and Lewis, 2000), drilled shells might have been

avoided when possible. LaBarbera and Merz (1992) recognised

that postmortem gastropod shells do change in strength not

only from major breaks but also from microfractures.

Octopuses observed in present study removed the gastropod or

hermit crab through the shell aperture primarily, leaving intact

shells that were available to hermit crabs. There was little or no

visible damage to shell apertures. Several authors have shown

that many factors, including shell thickness and epibionts, are

important in resistance to predation by crabs and other

duraphagous predators (Diet! and Alexander, 1995; Kamat et

al., 2000; Palmer 1979, 1985 and 1990; Voight, 2000) that

include octopuses. These same shell features are important in

hermit crab choices of shells. Researchers (Elwood and Neal,

1992; Hazlett et al., 1996; Imafuku, 1994; McLean, 1974, inter

alia) have found that hermit crabs transferring shells can

experience decreases in shell quality from erosion, epibionts

and change of fit. There was little evidence that hermit crabs

using postmortem shells from predation by octopuses experi-

enced decreases in overall shell quality. Shells liberated by

octopuses in the present study had few epibionts with the

exception of hydroids and no erosion of shells was observed for

the shells recycled (Table 1). However, change of fit was not

examined in the field experiments.

Gastropod and bivalve shells with flesh attached are dis-

carded as the octopuses move through their foraging ranges. It

is difficult to quantify how much the post mortem gastropod

shells contribute to the shell economy of hermit crabs over time

with a series of short observations. However, it is clear that

large, intact shells are made available and that chemical cues

from degrading flesh may attract hermit crabs to the resource

(Chiussi et al., 2001; Hazlett and Rittschof, 1997; Rittschof,

1980; Rittschof et al., 1992). Postmortem shells from gas-

tropods in the present study generally contained some remain-

ing flesh. Rittschof (1992) noted that several aspects of hermit

crab activities can be modulated by degradation products from

gastropod flesh including feeding, alarm, shell selection, and

aggregation. In a highly three dimensional habitat like a

seagrass-reef system, finding gastropod shells visually may be

difficult. Empty gastropod shells are not a common com-

modity in benthic environments as shown in the background

values in the present study (Table 3) as well as noted by other

researchers (Leite et al., 1998; Scully, 1983; Vance, 1972)

observing different habitats. The chemical signal from degrad-

ing gastropod flesh could give additional information to guide

Hermit crab ecology on a shallow coral reef

crabs to shells. Even if the signal is not displayed over long dis-

tances, the information could be important to a hermit crab in

determining whether to investigate a shell. Weissburg and

Zimmer-Faust (1993) and Moore and Atema (1991) showed

how crustaceans use chemical signals to derive fine-scale infor-

mation about prey. Several authors (Benoit et ah, 1997; Hazlett,

1996; Small and Thacker, 1994) have shown the importance of

chemoreceptive stimuli for shell seeking by different species of

hermit crabs. Hermit crabs investigating shells in the present

study were observed eating and removing flesh from shells,

though only two transfers of hermit crabs from old shells were

observed for shells deposited by foraging octopuses. However,

marked shells redeposited in the sampling area were removed

and shells were left behind in the same general area. Some her-

mit crabs in marked shells that were deposited after foraging by

octopuses also were found at middens, indicating that shells

were exchanged by hermit crabs.

Interestingly, though individuals of both species had over-

lapping foraging ranges, members of O. briareus concentrated

their feeding activities in the forereef and coral rubble/patch

reef areas while individuals of O. vulgaris concentrated efforts

in seagrass and patch reef corals. Octopuses are highly mobile

predators, foraging once or twice a day at Bailey’s Cay.

Individuals of O. vulgaris almost always made two foraging

trips while members of O. briareus rarely ventured forth twice.

This difference may be related to the growth rates of the two

species. Octopus vulgaris has a more rapid growth rate and

food conversion ratio than O. briareus, suggesting that addi-

tional forays are necessary for maintaining growth and devel-

opment (Mangold and Boletzky, 1973). This could have con-

tributed to the larger middens found outside O. vulgaris dens.

Ambrose (1984) and Forsythe and Hanlon (1997) have shown

that octopuses may also learn the distributions of some prey,

choosing their foraging areas and prey species accordingly. In

addition to learning the prey distribution through mapping of an

area, octopuses likely learn to avoid predators as well. Mather

and O’ Dor (1991) noted that foraging strategies and predation

risk can influence feeding choices of octopuses. Predators such

as eels were common at Bailey’s Cay, not only killing octo-

puses but also removing arms. Loss of arms could lead to infec-

tions as well as decreased foraging or mating abilities. There

were switches in prey exploitation during the three years of

sampling. In 2000 and 2001 sampling seasons, there was a

decline in live coral at the sampling site, with algal growth

increasing. This may account for chitons and echinoderms

{Echinometra lucimter (Linnaeus, 1758) and Tripneiistes ven-

tricosis (Lamarck, 1916)) becoming a more important part of

the diets for both species of octopuses (Table 2) in the coral

rubble/patch reef areas and the forereef.

Though foraging octopuses may offer a widely dispersed

resource for hermit crab use, the dens and middens provide a

stationary source of food and shells for hermit crabs.

Crustaceans dominated the number of prey remains deposited

in middens for both octopus species (approximately 55%, 63%

and 33% for 1999-2001, respectively, of total prey observed in

middens for O. vulgaris and 62%, 45% and 29% for 1999-

2001, respectively, of prey in middens for O. briareus).

Examining remains at middens and dens more closely reveals

that the foraging behaviours of the two octopuses offer differ-

ent degrees of potential resources for hermit crabs. In this sam-

pling area at Bailey’s Cay, hermit crabs were more closely

associated with dens of Octopus vulgaris both as prey and as

recyclers at middens and dens. Neither of the octopus species

had hermit crabs as significant parts of their diets during the

observation periods, though for some octopuses, hermit crabs

may be a preferred item. In the items noted for Table 2, hermit

crabs did not constitute more than 19% of the midden remains

by number for any year. It is unclear from other field studies

what the consumption rates of hermit crabs in the field might

be because middens are sampled for prey remains only

(Anderson et ah, 1999). Given that close examination of shells

at a midden is required to determine whether a gastropod or

hermit crab may have occupied the shell most recently, it is

likely that hermit crabs have been underestimated in diets of

octopuses determined only from prey remains at middens in

other studies.

Shell resources at middens are available to a range of hermit

crab sizes. Some shells were left intact while others were

peeled or crushed, leaving a shell apex suitable for smaller

crabs. Hermit crabs attracted to the middens sometimes

remained for several days. For Calcinus tibicen. Brown et al.

(1993) noted that presence of potential competitors for shells

lengthened the time of shell assessment. This suggests that indi-

viduals of C. tibicen at middens and dens may have remained

at the sites manipulating shells longer than if other hermit crabs

were not present. When members only of C. tibicen were pres-

ent at predation sites, researchers noted that shell assessment

time was not significantly shorter than when other species of

hermit crabs were present. However, variation in assessment

time did occur between genera of shells, as Brown et al. (1993)

also reported. Few direct aggressive interactions were observed

at the den or midden sites in the present study for individuals of

C. tibicen, especially between crabs of different sizes. For

larger crabs, movement around an occupied octopus den could

elicit a feeding response from the octopus. On one occasion, an

O. vulgaris individual was observed to dart from a den during

mid-day, pounce on and consume an individual of Paguristes

cadenati Forest, 1954 and Paguristes puncticeps engaged in an

aggressive encounter at a midden. Shells and appendages from

both individuals were jettisoned into the midden after about 10

minutes. In laboratory experiments, Kobayashi (1986) found

that octopuses presented with three different size classes of

hermit crabs in ideal shells selected the largest hermit crabs in

90% of the trials.

Individuals of Pagurus criniticornis and P brevidactylus

may use the sites for refugia as well as for finding shells and for

feeding. These hermit crabs may associate with occupied octo-

pus dens and surrounding middens to decrease risk of con-

sumptionby other predators. Octopus vulgaris individuals have

been shown to ignore small hermit crabs in experimental c

onditions (Tirelli et al., 2000), suggesting that they have a

minimal prey size. The small hermit crabs within the dens are

not accessible to other duraphagous predators while the octopus

is in residence. Pagurus criniticornis and P brevidactylus indi-

viduals in dens were observed feeding on remains left attached

to shells by octopuses. Most often in middens, members of

S.L. Gilchrist

P. criniticomis and P. brevidactylus were found consuming

remains from bivalves and echinoderms. Fish bones within

dens were also cleaned of flesh. In addition to protection from

predation and access to food at the dens, the smaller crabs also

selected shells from nearby middens. Shells used from middens

were sometimes so large that the hermit crabs were unable to

move them. One individual of P. puncticeps (shield length 4.1

mm) was observed occupying a Strombus gigas shell (shell

length 17.4 mm) in the same location over a seven day period.

For hermit crabs found commonly around dens in grassbeds,

octopuses bringing shells back from over the entire reef may

give access to new resources not commonly available in the

grassbeds.

Ramsay et al. (1997) noted that individuals of Pagurus

bernhardus (Linnaeus, 1758) attracted to small patches of food

showed increased numbers of aggressive interactions. These

researchers found that size frequency of visitors at carrion sites

in the field varied relative to patch size with larger hermit crabs

being prevalent at smaller patches. They suggested that these

larger individuals were superior intraspecific competitors for

the resource. In the present study, individuals of O. vulgaris and

O. briareus created different sizes of middens outside of their

dens, offering hermit crabs of different species relatively vary-

ing patches of food and types of shells. Regardless of patch

size, however, smaller hermit crabs did not flee the area as

described by Ramsay et al. (1997) for P. bernhardus when con-

fronted by either a larger conspecific or a larger hermit crab of

another species. Smaller hermit crabs in the present study

retreated into the openings of the octopus dens or plunged into

the midden mound. Movement into the middens likely allowed

the hermit crabs not only to avoid larger hermit crabs but also

to shift shells in middens, potentially encountering new shells

for assessment.

All of the shells within the middens were not necessarily

from octopus predation. Hermit crabs selecting shells from

middens could contribute a shell back to the middens. When

another hermit crab uses the shell left behind, this is referred to

as indirect shell transfer. Hazlett et al. (1996) showed that

indirect transfer of shells between hermit crab species at pre-

dation sites (areas where predators consume prey) does occur.

The middens function as predation sites, attracting hermit crabs

to shells and food by chemical cues. Crustacean predators (i.e.

Menippe mercenaria (Say, 1918)) also visited the middens.

These predators smashed empty gastropod shells, removing

flesh remnants from them as well as feeding on predatory gas-

tropods such as Nassarius vibex (Say, 1822) and Cancellaria

nodulifera Sowerby, 1825 attracted to prey remains at the

middens. Thus, these crustacean predators also contributed to

the shell middens of the octopuses. Shells that were smashed

still yielded category 4 shells with the apices intact. These

shells were readily taken by small hermit crabs. Morton and

Yuen (2000) showed that interspecific competition for carrion

does occur between hermit crabs and gastropods. However, no

direct interference was noted at the midden sites in this study.

Thi'ee parts of the methodology used for the current study

may have affected the observations at dens and middens. First,

hermit crab species that are consumed by octopuses may

approach dens and middens when the predators are not in resi-

dence to obtain shells and to feed on flesh remaining in shells.

The present study did not focus on an ethogram of activities at

unoccupied dens. Brooks (1989) indicated that at least two

species of hermit crabs, including Dardanus venosus that is

found at Bailey’s Cay, could detect octopuses through chemical

cues. Further experiments may indicate that other hermit crab

species at Bailey’s Cay also have this ability, allowing them to

reduce risk of predation by octopuses yet take advantage of the

shells available in middens and dens. Second, the method of

removing shells from the site each day may have influenced the

numbers, sizes and types of hermit crabs (Gilchrist, 1984;

Rittschof, 1980) and other attendants (Rahman et al., 2000)

attracted to the middens and dens by decreasing the amount and

types of flesh degradation products over time. This could

decrease the number of hermit crabs available to octopuses as

prey at middens in this study and could have influenced the

removal of shells from middens and dens. However, the octo-

puses are known to do housecleaning of the dens and middens

(Mather, 1991, 1994), removing debris from the area on a reg-

ular basis. Finally, by sampling over a short time period during

the same time of year, a full picture of potential contributions

of octopuses to hermit crab shell cycling is not possible.

Cycling of shells within the Bailey’s Cay system is complex.

Octopus dens and middens provide a concentrated resource of

shells as well as food for hermit crabs, augmenting opportun-

ities for both intra- and interspecific shell exchanges in the reef

system. Species such as P. criniticomis and P. brevidactylus

also have individuals that shelter within octopus dens without

being eaten.

Acknowledgements

This work was supported, in part, by the New College

Foundation through a Faculty Development Grant. Staff

members of the Roatan Institute of Marine Sciences (RIMS)

were helpful in logistics of field work and undergraduates in

the New College Coral Reef Program assisted with all aspects

of the field research. The Jack and Rhoda Pritzker Marine

Biology Research Center provided support for work in

Honduras. Thanks to Dr. M. Imafuku and to anonymous

reviewers who made suggestions to improve the manuscript.

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Memoirs of Museum Victoria 60(1): 45-52 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

Population dynamics and epibiont associations of hermit crabs (Crustacea:

Decapoda: Paguroidea) on Dog Island, Florida

Floyd Sandford

Abstract

Keywords

Department of Biology, Coe College, Cedar Rapids, Iowa 52402, USA (fsandfor@coe.edu)

Sandford, F. 2003. Population dynamics and epibiont associations of hermit crabs (Cmstacea: Decapoda; Paguroidea) on

Dog Island, Florida. In: Lemaitre, R., and Fudge, C.C. (eds). Biology of the Anomura. Proceedings of a symposium at

the Fifth International Crustacean Congress, Melbourne, Australia, 9-13 July 2001. Memoirs of Museum Victoria 60(1):

45-52.

Periodic belt transects and daily shoreline surveys in January and in June-July over a 10-year period (1992-2001)

were used to study the seven species of hermit crabs most common in the upper intertidal zone of a low energy bay with

a 960 m shoreline at the east end of Dog Island, Florida, and their association with three common shell epibionts in the

area: the Florida hermit-crab sponge, Pseudospongosorites suberitoides, the cloak anemone, Calliactis tricolor, and the

hydrozoan Hydractinia echinata. Of 15,052 hermit crabs sampled, Pagurus longicarpus, Pagurus pollicaris, and

Pagurus impressus were prevalent in January (88% of all animals) and Clibanarius vittatus dominated in the summer

(86% of all animals). The following associations were highly significant: P impressus with P suberitoides, P pollicaris

with H. echinata, and Petrochirus diogenes with C. tricolor. C. vittatus rarely had anemones, and P impressus were

never found in shells with H. echinata and showed a significant tendency, whether in sponge or shell shelters, to become

stranded compared to other pagurid species. Hermit crab sponges were commonly used as shelters by only two of the

hermit crab species, P. impressus and Paguristes hummi. Together these two species accounted for 99% of the 1077

animals found in sponges. Hermit crab sponges varied yearly in abundance from plentiful to uncommon, and nearly half

(1030 of 2107, or 49%) were empty.

Cmstacea, Anomura, hermit crab, population dynamics, epibiont

Introduction

Studies of hermit crabs on Dog Island, Florida, a barrier island

in the north-eastern comer of the Gulf of Mexico, over a 10

year period have shown the seven most co mm on species

encountered in intertidal waters surrounding the island to be as

follows: Pagurus longicarpus Say, 1817, Pagurus pollicaris

Say, 1817, Pagurus impressus (Benedict, 1892), Pagurus

stimpsoni (A. Milne Edwards and Bouvier, 1893), Paguristes

hummi Wass, 1955, Petrochirus diogenes (Linnaeus, 1758),

and Clibanarius vittatus (Bose, 1802). Pagurus longicarpus

and C. vittatus are intertidal species (Strasser and Price, 1999;

W. Herrnkind, pers. comm.). Clibanarius vittatus is a hardy

species that often enters the upper intertidal and can spend days

out of water (Rudloe, 1984). Pagurus pollicaris is primarily a

shallow subtidal to lower intertidal species, and the other four

are typically shallow to deep subtidal (Strasser and Price, 1999;

Herrnkind, pers. comm.), although P. impressus moves into the

intertidal zone during the winter months (Sandford and Brown,

1997). As is tme for most hermit crabs, all seven species occu-

py gastropod shells but two, P. impressus and P hummi, com-

monly use sponge shelters (Wass, 1955; Wells, 1969; Sandford

and Kelly-Borges, 1997). The sponge, Pseudospongosorites

suberitoides Diaz et al., 1993 (reclassified by McCormack and

Kelly, 2002) is one of the compact and colourful hermit-crab

sponges, a unique group of sponges (order Hadromerida,

family Suberitidae) reported from many different locations

worldwide (Sandford and Kelly-Borges, 1997). Hermit-crab

sponges typically colonise a living or dead gastropod shell,

although other substrates (e.g. other mollusc shells, inanimate

objects such as floating docks or wharf pilings) are used

(Sandford and Brown, 1997). The sponge eventually overgrows

the shell which becomes increasingly more deeply enclosed

within the sponge mass. If the shell is occupied by a hermit

crab, the crab eventually vacates the shell and occupies a cham-

ber within the sponge body, moving about in the sponge with

only its anterior end visible through an opening maintained by

the crab. Nearly all hermit-crab sponges worldwide are found

in deep water, typically recovered by dredging, but on Dog

Island such sponges are abundant in the intertidal zone in the

winter months when P. impressus in sponge shelters bring

sponges near shore. In the laboratory, P impressus often switch

from sponges into available shells, abandoning the sponges

(Sandford, 1995). Because sponges are more easily affected by

F. Sandford

wave action than are shells, hermit crabs in sponges near shore-

line are more likely to be affected by waves or beached

by receding tides. During the month of January many

sponges, both empty and occupied by hermit crabs, are found

near the shoreline, or stranded and drying on shore (Sandford,

1995).

Two other commonly encountered shell epibionts in the area

are the cloak anemone, Calliactis tricolor (Phylum Cnidaria,

Class Anthozoa) and the “snail fur” hydrozoan Hydractinia

echinata (Phylum Cnidaria, Class Hydrozoa).

To determine annual and seasonal population changes for

the hermit crab species and to check for specificity in the three

mentioned epibiont associations, a study was conducted on

Dog Island for 10 consecutive years (1992-2001).

Methods

Study site. Studies were conducted on Dog Island, St George

Sound, Florida (29°49.30"N, 84°34.30'W) annually since 1992,

during the month of January (1992-2001) and during June-July

for 4 years (1993, 1996, 1998, and 1999). Dog Island is the

easternmost of a chain of barrier islands bounding the southern

perimeter of Apalachicola Bay and St George Sound in the NE

Gulf of Mexico. It is a true barrier island, made of uncon-

solidated sand overlying the SW-dipping limestone bedrock of

the Florida platform. The island lies about 6 km offshore from

the N. Florida panhandle, and is 11 km long and 1.2 km at its

widest. All transect work was done in the intertidal zone of a

north-facing bay at the east end of the island. The bay has a 960

m shoreline and a sandy and sand/mud bottom with scattered

seagrass beds of manatee grass, Syringodium fdiforme and tur-

tle grass Thallasia testudinum. Water depth ranged from 0.3 to

1.3 m at mean low tide. At 1500 h in January water tempera-

tures ranged from 12.5-18. 5°C (normally 14-17°). January

2001 was atypical with temperatures as low as U°C. Work

consisted of periodic belt transect surveys, daily shoreline

surveys, and shell/sponge switching experiments.

Shoreline surveying. Shoreline surveys were conducted once

(0700-1000 h), and often twice (1400-1700 h), daily. All

sponges and hermit crabs stranded on shore or in the water

within 0.5 m from shoreline were collected and identified.

Surveys included the shoreline of the 960 m low energy beach

of the bay study site, in addition to two adjoining shores — a

contiguous 700 m stretch of low energy bay beach on St George

Sound up to the inlet of a tidal salt marsh and 2,300 m of high

energy Gulf beach at the extreme east end of the island - a total

of 3,960 m of shoreline. For the months of January 1992-2001

the surveys totalled 140 days and 338 h survey time; the

summer surveys totalled 37 days and 59 h of survey time.

Belt transect surveying. In the belt transect surveys from one to

four persons moved from one end of the bay to the other, col-

lecting all hermit crabs stranded on shore and from shoreline

into the intertidal zone to within 8 m from shoreline. All hermit

crabs were identified to species, shell type and presence of epi-

bionts noted, then released 200 m away in St George Sound. All

sampling was done on a rising tide and usually froml 600-1 800

h. Sixty-six transects were taken: 46 from January 1993-2001,

and 20 in the summer. Because no transect sampling was done

the first year, all analyses of hermit crab populations were

based on data from the last nine years of the study.

Testing for shelter preference and fidelity in Pagurus impressus.

Previous studies in the laboratory (Sandford, 1995) showed that

individuals of P. impressus prefer shell shelters. To determine

shelter preference and shelter fidelity for recently field caught

animals, shell/sponge switching experiments were conducted

on Dog Island for three years, January 1994-1996. Shelter

fidelity was measured by the tendency of animals to remain in

their original shelters over the course of up to a 3 day testing

and observation period.

Pagurus impressus in shell or sponge shelters collected

during shoreline and belt transect surveys were isolated, then

tested within 48-72 h of capture. Of 209 animals collected and

used for testing, 126 were in sponges and 83 in shells of the

gastropod Strombus alatus. All were juveniles or small adults

with chela 4.5-10.0 mm long. To control for shell type prefer-

ence, only animals found in S. alatus shells, a preferred shell

for P. impressus (Table 4), were used in testing. Empty sponges

and empty Strombus alatus shells were also collected. All shells

and sponges used as shelter choices in the tests were field col-

lected, either empty or previously occupied by individuals of

P. impressus. All empty sponges were healthy (i.e. good colour

with no bleaching and compact with a dense, non-flabby tex-

ture) and all empty S. alatus shells were undamaged and

epibiont-free.

Initial Test. Each animal was placed between an empty

S. alatus shell and an empty sponge at the center of a round

(diameter 11.2 cm) plastic container, with a 1 cm depth of sand

on the bottom and a 5 cm deep water column above the sub-

strate surface. Water temperature ranged with outside tempera-

ture, from 12° to 19°C. Shelter choices were in the center of the

chamber 1 cm apart with their opposite sides an equal distance

from the walls of the chamber. Shelters were positioned with

apertures or openings up and new sea water added after each

trial. The choice shelter was of equal or slightly larger size than

that occupied by the crab. The test lasted 30 minutes. Animals

that switched into a new shelter were noted, then released and

not tested again. It was noted whether the animal switched

short-term (remained in the new shelter for <3 min) or long-

term (remained in the new shelter for >3 min; crabs that

remained in the new shelter for >3 min rarely returned to their

original shelter).

Follow-up test. Any animal that did not switch into a new

shelter during the initial test was immediately returned to its

original container along with the two empty choice shelters and

observed periodically for 72 h. All animals that switched into

new shelters were noted; for such animals the test was consid-

ered ended if the animal remained in the new shelter for >24 h.

Data was analysed for significance using Minitab statistical

software.

Results

Sponge abundance. Sponges varied in abundance by season

and from year to year. A total of 2107 sponges were collected

in ten years. Sponges were common in the winter (99.3% of all

Population dynamics and epibiont associations of hermit crabs

specimens) and uncommon in the summer, and approximately

half were without a hermit crab occupant (Table 1). Sponge

abundance in January varied on an annual basis and in a rough-

ly cyclical way: sponges were abundant in 1994, common in

1992 and 1996, less common in 1993, 1995, 1997, 1999, and

2000, and uncommon in 1998 and 2001. In 1992, the first year

of the study, hermit crab sponges were numerous and 358 were

collected; 197 (55%) were occupied by a hermit crab, all of

which were Pagurus impressus. But hermit crabs in sponges

are more easily stranded on shore than those in shells and no

transect sampling was done in 1992. To control for sampling

bias, all analyses of associations between hermit crabs and

sponges were restricted to the data gathered by both transect

and shoreline sampling from 1993 to 2001.

Hermit crabs of Dog Island. A total of 15,052 hermit crabs, rep-

resenting seven species, were surveyed over the ten year

period. The four most common species {P. impressus,

P poUicaris, P. longicarpus, and C. vittatus) comprised over

98% of all hermit crabs sampled annually (Table 2). All

species, with the exception of C. vittatus, were most prevalent

during the winter. In January individuals of three species,

Pagurus impressus, P longicarpus, and P poUicaris, consti-

tuted 96% of all animals sampled; the most prevalent species

was the intertidal species P longicarpus which comprised 41%

of all animals sampled (Table 2). The typically subtidal

species P diogenes, P hummi, and P. stimpsoni occurred

sporadically. In the summer, individuals of C. vittatus domin-

ated the intertidal zone, along with some individuals of

P longicarpus and P poUicaris, whereas the other species

were rare (Table 2).

Association of hermit crab species with sponge shelters. Two

species, Pagurus impressus and Paguristes hummi, were com-

monly found in sponge shelters. Individuals of three other

species, P. longicarpus, P. poUicaris, and C. vittatus, rarely

used sponge shelters (< 0.5%) (Table 3). Over half of all P.

impressus and nearly a third of all P. hummi found were in

sponges. The difference in use of sponges as shelters between

P. impressus and P. hummi compared to the other 3 species was

highly significant {yf = 9608, df = 2, P < 0.001). Although indi-

viduals of both P. impressus and P. hummi were found in

sponges, the greater association with sponges by P. impressus

was significant (two sided test for equality of two proportions,

Z = 5.14, P < 0.001). Individuals of P. impressus showed a

highly significant association with sponge shelters compared to

all other species and to P. poUicaris, the third most common

species using sponges (Table 3). Of all 1494 P. impressus

collected from 1993-2001, most (56%) were in sponges,

compared to only 7 of 1,621 P. poUicaris found in sponges

(two sided test for equality of two proportions, Z = 42.6,

P< 0.001).

Most of the 1,077 occupied sponges in the study contained

individuals of Pagurus impressus and most of the sponges

collected in the study were found stranded on shore, but a

noticeable association of P. impressus with sponge shelters is

also evident for all animals collected in water during the belt

transect surveys (Table 4). A total of 454 P. impressus individ-

uals were collected in the surveys from 1993-2001. Of these

Table 1. Hermit crab sponge abundance on Dog Island, Florida, by

season, over a ten-year period (

1992-2001).

Time of year

Empty With hermit crabs

Total

Winter (Jan 1992-2001)

1017

1075

2092

Summer (1993, 1996,

1998-1999)

Total

1030

1077

2107

194 were in sponges (42.7%) and 260 were in shells (57.3%).

Individuals of P. impressus used 15 shell types, but three,

Strombus alatus, Cantharus cancellarius, and Busy con con-

trarium, were used by 72% of all individuals (Table 4).

Because nearly all her mi t crab-occupied sponges, whether col-

lected in water or on shore, contained individuals of P. impres-

sus and because the frequency with which empty sponges were

found in January varied annually (from 87% in 1997 to 19% in

2000) the data for 1993-2001 were analyzed to see if the

number of empty sponges sampled correlated with the number

of P. impressus surveyed. Poor correlations were found for both

(i) the total number of P. impressus surveyed (in both sponges

and shells) (R2 = 0.44) and (ii) only the P. impressus found in

shells (R2 = 0.27).

Association of four hermit crab species with the hydroid

Hydractinia echinata. For the four most common hermit crab

species, 13,995 individuals were in shells, and of these, 1343

(9.6%) were covered with hydroids of Hydractinia echinata

(Table 5). The association of the hydroid with the four hermit

crab species was dramatically non-random. No individuals of

P. impressus or of C. vittatus were associated with hydroids,

whereas 66% of P. poUicaris and 8% of P. longicarpus were in

hydroid-covered shells (Table 5). The differences between the

three pagurids were all highly significant (two-sided tests for

the equality of two proportions: P. poUicaris vs P. impressus,

Z = 55.5, P < 0.001; P poUicaris vs P. longicarpus, Z = 44.9, P

< 0.001; P. longicarpus vs P. impressus, Z = 17.6, P < 0.001).

Hydroids of H. echinata were found on all gastropod shell

types commonly used by hermit crabs on Dog Island. However,

to check for the possible effects of shell substrate on hydroid

growth, the association of H. echinata with only shells of the

ribbed whelk, Cantharus cancellarius, was examined (Table 6).

Younger animals of all three pagurid species commonly use

Cantharus cancellarius shells. This was especially true for

individuals of P. poUicaris as over half (56%) of all animals

sampled were in Cantharus shells, and 92% of these were cov-

ered by H. echinata. Cantharus shells were more likely to be

covered by hydroids than other shell types and as was the case

with all shells (Table 5), the associations of the three pagurid

species in hydroid-covered Cantharus shells are all signifi-

cantly different from one another (two-sided tests for equality

of two proportions: P. poUicaris vs P. impressus, Z = 102.3,

P < 0.001 ; P. poUicaris vs P. longicarpus, Z = 47.1, P < 0.001;

P. longicarpus vs P. impressus, Z = 15.3, P < 0.001). Pagurus

poUicaris is commonly associated with hydroids, P. longicar-

pus significantly less so, and P. impressus never uses Cantharus

shells with hydroids (Table 6).

F. Sandford

Table 2. Summary of hermit crabs collected by belt transect and shoreline surveys for nine years, 1993-2001, by season.

Winter

Summer

Species

% of % of all % of % of all

Total Number species animals Number species animals

Pagurus impressus

Pagurus pollicaris

Pagurus longicarpus

Clibanarius vittatus

Petrochirus diogenes

Paguristes hummi

Pagurus stimpsoni

unidentified

1,494

1,489

99.7

27.6

0.3

<0.1

1,621

1,471

90.7

27.3

150

9.3

<1.5

3,399

2,203

64.8

40.9

1,196

35.2

12.4

8,323

0.2

8,310

99.8

86.0

97.4

0.7

2.6

<0.1

117

116

99.1

2.2

0.9

<0.1

100.0

1.0

0.0

100.0

0.1

0.0

Totals 15,052 5,389

Table 3. Association of Pagurus impressus and Paguristes hummi, two

species commonly found in sponges, with five other hermit crab

species that rarely or never used sponge shelters for nine years

(1993-2001).

Species

Numbers

% in sponges

Pagurus impressus

1,494

55.5

Paguristes hummi

117

32.5

Pagurus pollicaris

1,621

0.4

Pagurus longicarpus

3,399

0.1

Clibanarius vittatus

8,323

<0.1

Petrochirus diogenes

Pagurus stimpsoni

Unidentified

Total

15,052

5.85

Table 4. Shelters occupied by 454 individuals of Pagurus impressus

collected in 66 belt transect surveys, 1993-2001.

Shelter

Numbers

% total

% of shell species

in sponges

194

42.7

in shells;

260

57.3

Strombus alatus

29.2

Cantharus cancellarius

23.9

Busycon contrarium

19.2

Busycon spiratum

7.7

Chicoreus dilectus

4.6

others (10 spp.)

15.4

Total

454

100.0

Table 5. Association of the four most common hermit crab species (for

all individuals found in shells) with the hydroid Hydractinia echinata

on Dog Island, Florida, for nine years, 1993-2001

Species

Numbers in shells

Percent with

H. echinata

Pagurus impressus

622

Pagurus pollicaris

1,614

65.6

Pagurus longicarpus

3,397

8.4

Clibanarius vittatus

8,322

Total

13,995

9.6

100.0

9,663

100.0

Table 6. Association of three pagurids with shells of Cantharus can-

cellarius, with or without the hydroid, Hydractinia echinata, on Dog

Island, Florida for nine years, 1993-2001.

Species

Numbers

% in

% with

in Shells

Cantharus

H. echinata

Pagurus impressus

662

23.3

0.0

Pagurus pollicaris

1,614

56.4

92.0

Pagurus longicarpus

3,397

28.8

19.2

Total 5,673

Table 7. Association of five hermit crab species found in shells with

the cloak anemone, Calliactis tricolor, on Dog Island, Florida, for nine

years, 1993-2001.

Species Numbers in shells % with C. tricolor

Pagurus impressus

662

1.3

Pagurus pollicaris

1,614

5.5

Pagurus longicarpus

3,397

Clibanarius vittatus

8,322

0.1

Petrochirus diogenes

66.7

Total

14,034

1.2

Table 8. Test of shelter preference for 126 individuals of Pagurus

impressus captured in sponges. Initial test lasting 30 minutes, check-

ing whether the crab switched into another sponge, into a Strombus

alatus shell, into both sponge and shell, or did not switch. Two-tailed

binomial probability test, Hq: Psponge = 0-5, P = 0.0004, significant.

Switched from sponge into:

Numbers

Sponge

7.1

Shell

25.4

Both

3.2

no switch

64.3

Total

126

100.0

Population dynamics and epibiont associations of hermit crabs

Table 9. Test of shelter preference for 83 individuals of Pagurus

impressus in Strombus alatus shells. Initial test lasting 30 minutes test-

ing whether the hermit crab switched from its shell into a sponge, into

another Strombus alatus shell, into both sponge and shell, or did not

switch. Two-tailed binomial probability test, Hq! Psheii = 0-5, P =

0.0006, significant.

Switched from sponge into:

Number

sponge

1.2

shell

18.1

both

1.2

no switch

79.5

Total

100.0

Association of five hermit crab species with the cloak anemone,

Calliactis tricolor. The individuals of all four species present in

shells that were checked for H. echinata (Table 5) were also

examined for the presence of the cloak anemone, Calliactis tri-

color. Data for a fifth species, Petrochirus diogenes, was also

recorded; this species never used sponges (Table 3) or shells

covered with H. echinata, but was commonly found carrying

one or more anemones (Table 7). A total of 14,034 individuals

of the five species was collected in shells, of which 173 had

anemones, nearly all of large size (basal diameter >1 cm).

Anemones were never found on shells occupied by P. long-

icarpus and only rarely (<1%) found on shells containing

C. vittatus. Anemones occurred with individuals of P. impres-

sus and P pollicaris about 5-7% of the time and were com-

monly found on shells used by P. diogenes. Of 39 P. diogenes

surveyed, 26 (67%) had anemones. Of these, anemone number

ranged from one to eleven individuals (mean = 3.8).

The association of P. impressus with anemones was signifi-

cantly less than P. diogenes and significantly greater than

C. vittatus (two-sided tests for equality of two proportions:

P. impressus vs C. vittatus, Z = 7.07, P < 0.001 ; P. impressus

vs P. diogenes, Z = 7.80, P < 0.001). No significant difference

was found between P. impressus and P. pollicaris in terms of

their association with anemones (Z = 1.50, P = 0.13).

Inciden ce of stranding on shore. Clibanarius vittatus is a hardy

species that often leaves the water and can remain on shore for

days at a time (Rudloe, 1984). During the summer transects,

many individuals of C. vittatus, the dominant species in the bay

during the summer, were found on shore. For example, in

the five belt transects conducted during June 1999, 1,218

C. vittatus individuals were collected, and 404 (33.3%) were on

shore.

Individuals of Pagurus impressus in sponge shelters are

commonly stranded on shore. However, hermit crabs in shells

are also often stranded on shore in January, and such shells are

often occupied by a P. impressus, sometimes P. pollicaris, and

only rarely by another hermit crab species. To determine

whether individuals of P. impressus in shells had a greater like-

lihood of becoming stranded than other species, the stranding

of individuals of P. impressus in shells was compared with

P. pollicaris, the other species often found on shore. During the

five years, January 1997-2001, 1,124 P. pollicaris in shells

were surveyed, 1,074 in the water and 54 (4.8 %) on shore.

Over the same period 283 R impressus in shells were surveyed,

126 in the water and 157 (55.5%) on shore. Compared to

P. pollicaris, individuals of P. impressus in shells show a sign-

ficantly greater likelihood of becoming stranded on shore (two-

sided test for equality of two proportions, Z = 16.8, P < 0.001),

and are even more likely to be found on shore than the hardy

upper intertidal species C. vittatus.

Shelter preference and fidelity for Pagurus impressus. (i). Initial

and follow-up test for animals in sponges. In the initial choice

test lasting 30 minutes, of 126 P. impressus in sponges, 45

animals (36%) switched into a different shelter, showing a sig-

nificant preference for shells (P = 0.0004) (Table 8). In the fol-

low-up test for the 81 animals that did not switch in the initial

test, 43 (53%) switched shelters; of these, 42 of 43 (97.7%)

selected the shell (P < 0.0001). In summary, 88 of the 126

(70%) animals captured in sponges switched into a new shelter,

showing a highly significant preference for shells over sponges.

(ii). Initial and follow-up test for animals in shells. In the

initial choice test, of 83 animals captured in S. alatus shells, 17

animals (20%) switched into a new shelter, showing a signifi-

cant preference for other S. alatus shells (P = 0.0006) (Table 9).

In the follow-up test of the 66 animals that did not switch in the

initial test, 25 (38%) switched into a new shelter, always choos-

ing a shell (P < 0.0001). In summary, 42 of the 83 (51%)

P. impressus captured in S. alatus shells switched into a new

shelter, showing a highly significant preference for other shells,

not sponges. Results show that individuals of Pagurus impres-

sus, a species commonly found in hermit crab sponges in the

Dog Island area, exhibit a significant preference for shell

shelters. The likelihood with which animals switch shelters

depends on shelter type. In the shelter preference tests shelter-

fidelity was also significantly higher for animals in shells

(31/83 or 37.3%) than for those in sponges (19/126 or 15.1%)

(X2= 13.63, dfl,P< 0.001).

Nearly all switches in the follow-up tests were long-term

and >24 h. Animals in shells that switched long-term (24-72 h),

always switched into other shells, never sponges. Animals in

sponges showed more variability in response and a greater inci-

dence of switching. Most animals in sponges (59%) switched

into a shell, and the majority (42/48 or 87.5%) remained long-

term (24-72 h). Many more animals in sponges (16%, com-

pared to 3%) switched into both shelter choices and many of

these switched into and used all three available shelters during

the follow-up test. Several animals switched from seven to nine

times between all three shelters during a 48 h period.

Discussion

The fact that only one or two species of hermit crabs (i.e.

Pagurus impressus in the intertidal zone and both P. impressus

and Paguristes hummi in the subtidal zone) commonly use

sponge shelters in the Gulf of Mexico is similar to situations in

other locations where hermit crab sponges occur. In Hokkaido,

Japan, nearly all hermit crab sponges are occupied by Pagurus

pectinatus (Stimpson), 1858 and in southwest England and

Scotland by Pagurus cuanensis Thompson, 1843 (H. Mukai,

F. Sandford

pers. comm.; Sandford, pers. obs.). In other localities with her-

mit crab sponges, however, up to nine or more species use

sponge shelters (e.g. British Columbia (Kozloff, 1987),

Mikawa Bay, Japan (Tanaka, 1995), and the Mediterranean

(Vosmaer, 1933).

In nearly every location where hermit crab sponges have

been reported, they occur in deep water and are only retrievable

by scuba, trawling, dredging or other means (e.g. octopus

traps). Dog Island is unusual in that hermit crab sponges are

common near shore or on shore. This is partially due to the

behaviour of P. impressus, a typically subtidal species that

often uses sponge shelters, which migrates into the intertidal

zone in the winter, bringing sponges closer to shore. When

animals in sponges switch into available shells, the empty

sponges are abandoned and easily washed on shore. Nearly half

of all sponges collected in the surveys were empty. Although

the presence of hermit crab sponges in the intertidal zone of

Dog Island in the winter is largely due to individuals of

P. impressus transporting them from the subtidal zone near to

shore, the number of empty sponges found each year from 1993

to 2001 did not correlate with the number of P impressus

surveyed. This suggests that sponge abundance at the study

site is not due solely to the behaviour of P. impressus but to

other factors, such as weather and tides, or the biology and

reproduction of the sponges.

Recently field-caught juvenile individuals of P impressus, a

majority in sponge shelters, exhibit significant shell preference.

Animals in either shell or sponge shelters usually switch into

shells, not into sponges, supporting results of previous studies

on individuals maintained in the laboratory in mixed-species

assemblages or in conspecific groups (Sandford, 1994, 1995).

A shell preference was also indicated by differences in short-

term versus long-term switching. Animals switching into shells

from either shells or sponges, usually remained in shell shelters

long-term (i.e. >5 minutes, and typically at least 24-48 h).

Animals switching from one sponge into another typically

exhibited no such long-term bias. Crabs in sponges showed sig-

nificantly reduced shelter fidelity, and were more likely to

switch shelters, usually into shells. In areas where they occur,

hermit crab sponges are used as alternative shelters by shell-

dwelling hermit crabs, although sponges are less preferred and

are likely suboptimal shelters.

These results contradict the suggestion (Benedict, 1900;

Vosmaer, 1933; Rabaud, 1937; Hart, 1971) that one possible

benefit of use of a sponge shelter by a hermit crab is the advan-

tage of a longer term association with a living, growing home

and a reduced need to change shelters compared to hermit crabs

in shells. Encrusting sponges and bryozoans are the only gas-

tropod shell epibionts associated with hermit crabs which

would allow the crab to retain a shell shelter for a longer peri-

od by constantly growing and effectively enlarging the volume

of the shelter (Stachowitsch, 1980; Taylor, 1994). Although it

has been suggested that encrusting symbionts growing on gas-

tropod shells may reduce the frequency of switching, Taylor

(1994) noted that this has never been documented by long-term

observations of individual hermit crabs. This study confirms

that individuals of P. impressus using sponge shelters do not

typically exhibit long-term attachments. A similar tendency to

leave sponges and enter shells occurs for Paguristes hummi

(Sandford, unpubl. data), the only other hermit crab found in

the area that commonly uses sponges (Wass, 1955; Wells, 1969;

Williams, 1984).

Shell/sponge switching has not been studied in sponge/crab

associations from elsewhere, but in many locales only certain

hermit crab species occur as the typical sponge occupants (e.g.

Pagurus cuanensis and Paguristes eremita in Suberites

domuncula from the North Aegean Sea (Voultsiadou-Koukoura

and Koukouras, 1993), Pagurus cuanensis in Suberites sp.

from the Adriatic Sea (Stachowitsch, 1980), the Irish coast

(Selbie, 1921) or south-western England and the western coast

of Scotland (Allen, 1967; Sandford, pers. obs.), and Pagurus

pectinatus in Suberites ficus from Hokkaido, Japan (Sandford,

pers. obs.). Shell preference for sponge-using hermit crabs

from these and other locations is not known.

Wilber (1990) speculated that hermit crabs change shells

frequently and Abrams (1987), studying shell switching in five

hermit crab species, found that the percentage of individuals

that switched shells ranged from 40% in Pagurus hemphilli

to 81% in P samuelis. In this study 47/83 P impressus

(57%) switched from one S. alatus shell into another, a figure

consistent with Abrams’ (1987) findings.

Use of sponges as shelters can be costly. Sponges interfere

with burying in the substrate, and are more easily influenced by

tides and currents or beached by waves. On Dog Island hermit

crabs in sponges are seen rolling about in the swash zone and

are often washed ashore. The crabs often die from desiccation

but the sponges rehydrate successfully when reimmersed.

Since use of sponge shelters is costly and P impressus juve-

niles prefer shell shelters, why are so many found occupying

sponges? Several possibilities exist. Juvenile P impressus

either use sponge shelters because (i) they confer some

survival advantage, (ii) appropriate shells are scarce, or (iii)

they are out-competed by more aggressive species such as

P pollicaris.

Sponges may confer survival advantages, especially to

small or juvenile individuals of P impressus, the typical occu-

pants. Nybakken (1996) considered the sponge/hermit crab

association an example of true mutualism, with the sponge

deterring crab predators with its disagreeable taste. Taylor

(1994) noted that shell-encrusting bryozoans may reduce pre-

dation because of shell thickening, chamber enlargement, and

camouflage. These same arguments could apply for shell-over-

growing sponges, and there is some evidence to suggest that

hermit crabs in sponges are less likely to be attacked or eaten

by blue crabs, Callinectes sapidus, a typical predator, either

because of a chemical, texture, or camouflage factor (Farley,

pers. comm.; Sandford, pers. obs.).

In laboratory conditions, use of sponges by individuals of

P. impressus increases as shells become less available

(Sandford, 1995) so in the field crabs may use sponges in those

habitats where shells are relatively scarce. Shell scarcity is a

limiting factor for hermit crabs (Kellogg, 1976, 1977; Hazlett,

1981; Pace, 1993) and may be a major factor explaining the

large number of P impressus using sponge shelters in the Dog

Island area.

Shell use and aggression in hermit crabs are linked (Hazlett,

Population dynamics and epibiont associations of hermit crabs

1981) and it has been suggested (Rudloe, 1999) and there is

some evidence (Kellogg, 1977; Hazlett, 1980; Sandford, pers.

obs.) that individuals of P. impressus are less aggressive or less

competitive than other hermit crab species. Sympatric hermit

crab species can coexist in spite of shell competition by

exhibiting different shell preferences, habitat preferences, or

other biological differences (Hazlett, 1981). Kellogg (1977) in

Beaufort Harbor, North Carolina, studied many of the same

hermit crab species as in this study. He found that hermit crab

populations there were shell-limited and that both P. impressus

and P. hummi individuals were infrequently found in inshore

areas, and were likely to be outcompeted by P. pollicaris

and P. longicarpus. In the Dog Island area individuals

of both P impressus and P hummi may use the sponges

as less favoured alternative shelters as a consequence of such

competition.

The possible benefits of sponge shelters remain undeter-

mined, but it is now clear that sponges are suboptimal shelters

that may affect locomotion and increase mortality risks

from dehydration due to stranding. Although many juvenile

and some adult individuals of P. impressus use sponges for

extended periods, most switch into shells when available.

For the other two epibionts studied, Calliactis tricolor and

Hydractinia echinata, the results clearly show a significant

association of P pollicaris with the hydroid H. echinata and

a significant lack of association of both P. impressus and

C. vittatus with the same hydroid. The cloak anemone

Calliactis was associated with three species (P pollicaris,

P impressus, and especially P diogenes) and not associated

with two others {P. longicarpus and C. vittatus). The common

association of Calliactis tricolor with P diogenes found in this

study has been noted by Rudloe (1984) who has found

P. diogenes individuals with as many as 20 anemones.

The association of anemones with P. impressus,

P pollicaris, and P diogenes is to be expected, as they frequent

subtidal hard bottom habitats more optimal for anemones.

Conversely, the two intertidal species, P. longicarpus and

C. vittatus, that live in sandy bottom habitats which are less

optimal for anemones, lacked anemones. The deficiency of

anemones on shells occupied by C. vittatus may also be related

to the fact that C. vittatus is the hardiest of all hermit crab

species in the Gulf of Mexico, and often leaves the water for

days at a time (Rudloe, 1984, 1999). Under such circumstances,

any anemones carried on the shells would desiccate. Any asso-

ciation of C. vittatus with C. tricolor is non-symbiotic in nature

(Brooks et al., 1995). Individuals of Calliactis tricolor are

found rarely attached to shells occupied by C. vittatus but it is

not certain whether anemones do not discriminate (Brooks et.

al., 1995; Sandford, pers. obs.) or actually avoid C. vittatus as

reported by Rudloe (1984).

The lack of association of P longicarpus with the anemone

may also be due to this hermit crab’s burying behaviour.

Although features such as shell size or shell damage affect the

switching behaviour and survival of species like P pollicaris

(McClintock, 1985), Kuhlmann (1992) concluded that for P

longicarpus burying behaviour is probably more important

than shell features as an anti-predator factor. The burying

behaviour of P longicarpus, in addition to its intertidal zone

habitat and smaller size relative to the other species examined

for anemones, likely explains the absence of anemones on

shells occupied by this species. Individuals of P pollicaris also

commonly bury in the substrate (McLean, 1974), commonly

associate with C. tricolor (Rudloe, 1999), and were often found

with anemones in this study, so their greater association with

the anemone relative to P. longicarpus is most likely explained

by their greater exposure to habitats in the subtidal zone where

anemones more commonly occur.

A preferential association of H. echinata with certain hermit

crab species was reported by Yund and Parker (1989). The com-

plete absence of H. echinata on shells used by C. vittatus may

be explained by this species’ preference for the upper intertidal

zone and/or its tendency to spend time on shore. The total lack

of association of the hydroid with P. impressus is most likely

due to the rejection of hydroid-covered shells by individuals of

this species.

Acknowledgements

I am grateful to the many Coe College students who assisted

me in my field work on Dog Island each January from 1993 to

2001, to Gavin Cross and Peggy Knott for their help, to Sharon

Sandford for her advice and support, and to Dan Rittschof for

his helpful comments on an early draft of the ms. I am espe-

cially indebted to Guest Editors, Rafael Lemaitre and Chris

Tudge, and three anonymous reviewers for their critically

useful comments on the final draft.

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Memoirs of Museum Victoria 60(1): 53-57 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

The morphology of cardiac and pyloric foregut of Aegla platensis Schmitt

(Crustacea: Anomura: Aeglidae)

Thais da Silva Castro and Georgina Bond-Buckup

Universidade Federal do Rio Grande do Sul, Departamento de Zoologia, Av. Bento Gonfalves, 9500, predio 43435, CEP

91501-970 Porto Alegre, RS, Brazil (GBB; ginabb@ufrgs.br)

Abstract Castro, T.S., and Bond-Buckup, G. 2003. The morphology of cardiac and pyloric foregut of Aegla platensis Schmitt

(Crustacea; Anomura: Aeglidae). In; Lemaitre, R., and Tudge, C.C. (eds). Biology of the Anomura. Proceedings of a

symposium at the Fifth International Crustacean Congress, Melbourne, Australia, 9-13 July 2001. Memoirs of Museum

Victoria 60(1): 53-57.

The aeglid crab, Aegla platensis Schmitt 1942, is endemic to fresh waters in temperate and subtropical regions of

South America. The cardiac and pyloric foregut of southern Brazilian specimens of A. platensis were fixed in buffered

10% formalin and prepared for scanning electron microscopy. In the cardiac foregut, the gastric mill, lateral wall and car-

diac-pyloric valve ossicles were identified, while in the pyloric foregut, dorsally, ventrally and laterally supported ossi-

cles were characterised. These results show the complexity of the A. platensis foregut and support the hypothesis that the

most complex gastric mills are found in the Brachyura and Anomura.

Keywords Cmstacea, Anomura, Aeglidae, foregut, morphology

Introduction

Aeglid crabs are the only anomurans that occur on the sur-

face and underground in the fresh waters of subtropical and

temperate South America (Bond-Buckup and Buckup, 1994).

Morphological studies of the internal organization of the

foreguts of decapod crustaceans can reveal their feeding habits

(Kunze and Anderson, 1979; Ngoc-Ho, 1984). Huang et al.

(1998) analysed the distribution and taxonomy of two closely

related species of genus Ocypode (Crustacea, Brachyura), con-

cluding that these species could be differentiated not only in

various external characters, but also by the structure of their

foreguts. They suggested that the structure of the gastric mill

could be used as an additional character to define genera and

families.

Information on the structure of the decapod foregut can be

interpreted phylogenetically and it has been argued that the

structural complexity of the gastric mill reflects the evolution-

ary relationships between decapods, with diet and size acting as

modifying factors (Dali and Mortiary, 1983). In a cladistic

study of the Brachyura, for example, Brbsing et al. (2001)

investigated the characteristics of the cardiac foregut ossicles

and proposed a new phylogeny for this group based on this

character. Felgenhauer and Abele (1989) have suggested that

the basic structure of the foregut in the lower Decapoda is

closely related to phylogeny, although details of the structures

may be related to diet.

This paper elucidates the morphology of the cardiac and

pyloric foreguts of Aegla platensis Schmitt, 1942, a species

widely distributed in the freshwater systems of Uruguay,

Argentina and southern Brazil.

Materials and methods

We examined 80 specimens of Aegla platensis collected in the

River Gravatai drainage-basin (29°46"S, 50°53"W) in the

southern Brazilian state of Rio Grande do Sul (RGS), along

with other specimens selected from the crustacean collection of

the Zoology Department of the Federal University of RGS

(UFRGS). Foreguts were dissected and fixed in buffered 10%

formalin, and dorsal, ventral and para-sagittal cuts made.

Foreguts were prepared for scanning electron microscopy as

described by Felgenhauer (1987), using a model CPD 030 crit-

ical point dryer (BAL-TEC) with subsequent gold-coating, and

later, the photomicroscopy being carried out in a JEOL JSM

580 scanning electron microscope (15 and 20 KV) at the

Electron Microscopy Center, UERGS. Ossicles were described

and identified based on the nomenclature of Ngoc-Ho (1984)

and Kunze and Anderson (1979).

Results

The cardiac foregut ossicles include the gastric mill, lateral

wall and cardiac-pyloric valve ossicles (Table 1), together with

the dorsal, ventral and lateral ossicles of pyloric region.

IS. Castro and G. Bond-Buckup

Table 1 . Ossicles of the foregut of Aegla platensis.

Ossicle

Paired

Unpaired

Tooth

Gastric Mill

Mesocardiac

Pterocardiac

Urocardiac

Zygocardiac

Pyloric

Propyloric

Exopyloric

Lateral Cardiac

Pectineal

Prepectineal

Postpectineal

Inferior lateral cardiac

Subdentate

Cardiopyloric Valve

Anterior of cardiopyloric valve

Dorsal Pyloric

Posterior mesopyloric

Uropyloiic

Ventral Pyloric

Anterior inferior pyloric

Middle inferior pyloric

Posterior inferior pyloric

Transverse pyloric

Lateral Pyloric

Anterior pleuropyloric

Middle pleuropyloric

Posterior pleuropyloric

The foregut of Aegla platensis presents two well-defined

regions: the cardiac foregut at the anterior end and the pyloric

foregut at the posterior end (Fig. 1). The cardiac foregut (region

A in Fig. 1) is guarded at the entrance by a pair of oesophageal

valves (Fig. 8, ve), and consists of a large triangular chamber,

supported by thin calcified plates, and by a set of very thick cal-

cified ossicles. The central urocardiac ossicle bears the median

tooth (Fig. 5), and is articulated to the large central mesocardiac

ossicle anteriorly, and to the propyloric ossicle posteriorly (Fig.

1). The mesocardiac ossicle articulates with the paired ptero-

cardiac ossicles laterally, and these ossicles, to the paired zygo-

cardiac ossicles, which bear the lateral teeth (Fig. 6), being

responsible for mastication and triturating of food entering

from the oesophagus. The paired pectineal ossicles of the later-

al wall bear the accessory teeth (Fig. 7), which assist in push-

ing material into the central region of the foregut. This elabo-

rate apparatus of trituration, composed by the median tooth of

urocardiac ossicle, lateral teeth of zigocardiac ossicles, and

accessory teeth of the pectineal ossicles, is highly calcified and

is often called “gastric mill”. A peculiarity of the zigocardiac

ossicles is the occurrence of a series of spines at their anterior

margin (Fig. 6, zs), structures not so far recorded in the litera-

ture for any other decapod. The remaining ossicles of the car-

diac foregut, serve to support the foregut chamber in the same

way as the ossicles and chitinous plates of the lateral walls do,

for example, the paired inferior lateral cardiac and the post-

pectineal ossicles (Fig. 8) and the cardio-pyloric valve. In the

analysed foreguts it was possible to see that some ossicles of

lateral wall were fused (e.g. the prepectineal were fused with

the pectineal). On the other hand, ossicles such as the inferior

cardiac, posterior-lateral cardiac, supra-ampullar, mesopyloric

posterior and the lateral ossicles of the cardio-pyloric valve

were not observed in A. platensis. The pyloric foregut is a

smaller chamber, posterior to the cardiac foregut (region B in

Fig. 1), and is made up of various ossicles, valves, grooves,

ridges, channels and two rounded ampullae, all of which con-

stitute the filtering mechanism of the foregut. The pyloric

foregut is internally divided into dorsal and ventral regions,

shown in Fig. 2, with the dorsal region possessing a central

channel and the pleuropyloric valve (Fig. 8) which allows the

passage of large particles into the intestine and acts in the pro-

duction of the faecal pellets. The ventral region is characterised

by two ampullae (Figures 2 and 3), which constitute the most

important structure of this part of the foregut, carrying out the

filtering of the food particles by the setae, and which are exter-

nally characterised by two calcified semi-circular plates. The

interior of the pyloric ampullae is divided into two chambers,

the superior chamber containing the filter-press and the infer-

ior chamber (Fig. 3) containing parallel longitudinal grooves.

The filter-press adjusts to the concave shape of the inferior

chamber, compressing food particles against the parallel

grooves, and then trapping larger particles within a series of

setae (Fig. 3).

The cardiac and pyloric foreguts are separated by the

cardiac-pyloric valve (Fig. 4), a structure which regulates the

passage of triturated food particles from the gastric mill to the

pyloric foregut where they are further filtered.

Discussion

The general morphology of the cardiac and pyloric foreguts of

A. platensis is similar to that described by Icely and Nott (1992)

for decapods in the infraorders Astacidea, Thalassinidea,

Palinura, Anomura and Brachyura. The basic structure of the

decapod foregut is confirmed for the A. platensis foregut in this

work, although there are differences which probably reflect the

type of food that is being treated in the foregut.

Compared with the diogenid anomurans Clibanarius taenia-

tus, C. virescens, Paguristes squamosus and Dardanus setifer

(Kunze and Anderson, 1979), the cardiac foregut structures of

A. platensis are well-developed, with this last species pre-

senting a complex cardiac foregut equipped with specialised

mechanisms for the trituration of food. These specialised mech-

anisms can be seen in the robust and ornamented medial

(Fig. 5) and lateral (Fig. 6) teeth, as well as the accessory teeth

(Fig. 7) which are elongate with a greater number of spines,

when compared with the diogenids studied by Kunze and

Anderson (1979). On the other hand, the spines observed at the

anterior margin of the zigocardiac ossicles problably increases

the capacity of triturating food particles. This complex form of

foregut can be associated with macrophagy and predation in

which large particles are ingested (Dali and Mortiary, 1983).

Macrophagy and predation are well characterised in A. platen-

sis, an omnivorous species feeding on aquatic insect larvae and

Morphology of the foregut oiAegla platensis

Figures 1-7. 1. Dorsal view of cardiac and pyloric foreguts of Aegla platensis Schmitt. The cardiac foregut region (A) and the pyloric foregut

region (B) are indicated by lines. Abbreviations: am, pyloric ampullae; eo, exopyloric ossicle; me, mesocardiac ossicle; mo, mesopyloric pos-

terior ossicle; pa, anterior pleuropyloric ossicle; py, pyloric ossicle; po, propyloric ossicle; pt, pterocardiac ossicle; uc, urocardiac ossicle; up,

uropyloric ossicle; zc, zygocardiac ossicle (scale bar: 1mm). 2. Ampullae of pyloric foregut. Abbreviation: am, pyloric ampullae (scale bar: 1mm).

3. Internal view of the inferior chamber of the ampullae. Abbreviations: am, pyloric ampullae; Ig, longitudinal parallel grooves; se, setae (scale

bar: 0.15mm). 4. Cardiopyloric valve (scale bar: 0.5mm). 5. Median tooth of the urocardiac ossicle. Abbreviation: mt, median tooth (scale bar:

0.5mm). 6. Zygocardiac ossicle with the lateral teeth and spines. Abbreviations: It, lateral teeth; zs, zygocardiac spines; zp, zygocardiac molar

processes (scale bar: 1mm). 7. Accessory teeth of the pectineal ossicle. Abbreviations: at, accessory teeth; st, accessory teeth spines; pe, pectineal

ossicle (scale bar: 0.15 mm).

IS. Castro and G. Bond-Buckup

Figure 8. Sagittal half of the foregut showing internal organisation. Abbreviations: am, pyloric ampullae; at, accessory teeth; ic, inferior lateral

cardiac ossicle; It, lateral teeth; me, mesocardiac ossicle; pe, pectineal ossicle; ps, postpectineal ossicle; pt, pterocardiac ossicle; uc, urocardiac

ossicle; vc, cardiopyloric valve; ve, esophageal valve; vp, pleuropyloric valve; zc, zygocardiac ossicle (scale bar: 0.65mm).

macrophytes (Bueno and Bond-Buckup, 2001). The differences

between the foreguts of the aeglids and diogenids in terms of

the specialisation of the gastric mill may reflect different feed-

ing habits of these species, as was suggested by Kunze and

Anderson (1979) for the diogenid species. The variation

between foreguts is more marked when considering the cardiac

foregut ossicles, which may be fused or absent (Meiss and

Norman, 1977) Inversely, the inferior cardiac, posterior-lateral

cardiac, supra-ampular, mesopyloric posterior and the lateral

ossicles of the cardio-pyloric valve have been observed in other

anomurans, Clibanarius taeniatus, C. virescens, Paguristes

squamosus and Dardanus setifer (Kunze and Anderson, 1979)

and Galathea squamifera (Ngoc-Ho, 1984). It is possible that

the ossicles not seen in A. platensis were indeed present but

their identification was not possible because they were strong-

ly fused with other ossicles.

The basic organisation of the cardiac ossicles of A. platensis

follows the same arrangement found in the majority of

decapods, all of which (except for some Caridea) present an

elaborate food trituration mechanism — the gastric mill

(McLaughlin, 1983; Growns and Richardson, 1990).

Meiss and Norman (1977), stated that decapod infraorders

with species which have more complex gastric mills (e.g.

Brachyura and paguroid Anomura) have a smaller mesocardiac

ossicle, a well developed pyloric ossicle and large urocardiac

and zygocardiac ossicles. The structural complexity of the

cardiac foregut of A. platensis, observed in our sample, sup-

ports this hypothesis.

Acknowlegments

We wish to thank the anonymous reviewers whose spent sever-

al hours reading and reviewing this work and the Conselho

Nacional de Pesquisas - CNPq- in Brazil for his financial

support to this investigation. This is contribution n.375 from

DZ/UFRGS.

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Aeglidae). Program, Abstracts and List of Participants of the

Fifth International Crustacean Congress. Melbourne, Australia.

P46.

Dali, W., and Mortiary, D.J.W. 1983. Functional aspects of nutrition

and digestion. Pp. 215-261 in: Mantel, L.H. (ed). The biology of

Crustacea: internal anatomy and physiological regulation. Vol.5.

Academic Press: New York.

Felgenhauer, B.E. 1987. Techniques for preparing cmstaceans for

scanning electron microscopy. Journal of Crustacean Biology 7(1):

71-76.

Felgenhauer, B.E., and Abele, L.G. 1989. Evolution of the foregut in

the lower Decapoda. Pp. 205-219 in: Eelgenhauer, B.E., Watling,

L., and Thistle, A.B. (eds). Functional morphology of feeding and

grooming in Crustacea. Cricstacean Issues 10. A.A.Balkema,

Rotterdam.

Growns, I.O., and Richardson, A.M.M. 1990. A comparison of the

gastric mills of nine species of prastacid erayfish from a range of

habitats, using multivariate morphometries (Decapoda,

Astacoidea). Crustaceana 58(1): 33-44.

Huang, J.E., Yang, S.L., and Ng, P.K.L.1998. Notes on the taxonomy

and distribution of two closely related species of ghost crabs,

Ocypode sinensis and Ocypode cordinianus (Deaepoda, Brachyura,

Ocypodidade). Crustaceana 71(8): 943-954.

Morphology of the foregut oiAegla platensis

Icely, J.D., and Nott, J.A. 1992. Digestion and Absortion; Digestive

system and associated organs. Pp. 147-201 in; Harrison, F.W., and

Humes, A.G. (eds). Microscopic anatomy of invertebrates. Vol.lO.

Wiley-Liss Inc: New York

Kunze, J., and Anderson, D.T. 1979. Functional morphology of the

mouthparts and gastric mill in the hermit crabs. Australian Journal

of Marine and Freshwater Research 30; 683-722.

McLaughlin, P. 1983. Internal anatomy. Pp.1-52 in; Mantel, L.H. (ed).

The biology of Crustacea. Vol. 5. Internal anatomy and physio-

logical regulation. Academic Press: New York.

Meiss, D.E., and Norman, R.S. 1977. A comparative study of the

stomatogastric system of several decapod Crustacea. I. Skeleton.

Journal of Morphology 152: 21-54.

Ngoc-Ho, N. 1984. The functional anatomy of the foregut of

Porcellana platycheles and a comparison with Galathea squam-

ifera and Upogebia deltaura (Crustacea: Decapoda). Journal of

Zoology 203:511-535.

Memoirs of Museum Victoria 60(1): 59-62 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

Circadian and seasonal variations in the metabolism of carbohydrates in Aegla

ligulata (Crustacea: Anomura: Aeglidae)

G.T. Oliveira,' F.A. Fernandes,' G. Bond-Buckup,^ A.A. Bueno^ and R.S.M. Sieva-^

' Departamento de Ciencias Fisiologicas, Faculdade de Biociencias, PUCRS, Av. IPIRANGA, 6681/ Pd.l2A- CEP;

90619-900 Porto Alegre, RS, Brazil (guendato@pucrs.br)

^ Departamento de Zoologia e Programa de P 6 s-Gradua 9 ao em Biologia Animal, Instituto de Biociencias, UFRGS, Av.

Bento Gonsalves, 9500, predio 43435, sala 217- CEP: 91501-970 Porto Alegre, RS, Brazil (ginabb@ufrgs.br)

^ Departamento de Eisiologia, Instituto de Ciencias Basicas da Saude, UERGS, Rua Sarmento Leite, 500, Lab. 10 CEP:

90050-170 Porto Alegre, RS, Brazil (roselis@vortex.ufrgs.br)

Abstract Oliveira, G.T., Eernandes, FA., Bond-Buckup, G., Bueno, A.A. and Silva, R.S.M. 2003. Circadian and seasonal varia-

tions of the metabolism of carbohydrates m Aegla ligulata (Crustacea; Anomura: Aeglidae). In: Lemaitre, R., and Tudge,

C.C. (eds). Biology of the Anomura. Proceedings of a symposium at the Fifth International Cmstacean Congress,

Melbourne, Australia, 9-13 July 2001. Memoirs of Museum Victoria 60(1): 59-62.

The aim of this study is to evaluate the effect of circadian and seasonal variations on the metabolism of carbohydrates

in different tissues of the freshwater anomuran Aegla ligulata Bond-Buckup and Buckup, 1994. Samples of A. ligulata

were collected monthly from August 1999 to August 2000 in Tainhas, Sao Francisco de Paula, RS, Brazil, at 0600 h,

1200 h and 1800 h. Samples of haemolymph and tissues (hepatopancreas, gills and muscle) were taken to determine glu-

cose and glycogen levels. Data indicated the presence of high levels of haemolymphatic glucose, especially in spring,

and we also found circadian differences between males and females. These variations seem to be related to the repro-

ductive period of the species, food availability and the degree of environmental exploration. These factors lead to dif-

ferent metabolic adjustments in distinct species of cmstaceans.

Keywords Crastacea, Anomura, Aeglidae, metabolism

Introduction

Crustaceans are exposed to many environmental variables that

follow annual and daily cycles differing with geographical

region, and which cause behavioural, feeding and metabolic

alterations. Study of intermediate metabolism in crustaceans

has shown high inter-and intra- specific variability, which

makes it difficult to determine a standard metabolic profile.

This variability can occur because of several factors such as

habitat, stage in the moult cycle, sexual maturity (especially in

females), feeding state, food at hand and seasonality, since

these factors determine differential metabolic response.

Glucose is the principal monosaccharide present in the

haemolymph of crustaceans and it serves six main purposes:

synthesis of mucopolysaccharides, synthesis of chitin, syn-

thesis of ribose and nicotinamide adenine dinucleotide phos-

phate reduced (NADPH), the formation of pyruvate, and the

synthesis of glycogen (Hochachka et al., 1970; Chang and

O’Connor, 1983; Herreid and Full, 1988).

The main glycogen reserves in crustaceans are the muscle,

the hepatopancreas, the branchiae and the haemocytes. The

storage place of this polysaccharide varies according to the

species (Johnston and Davies, 1972; Herreid and Full, 1988).

The absence of a central glycogen deposit seems to be an adap-

tation of several classes of animals to changes in environ-

mental factors (Hochachka et al., 1970). The stored glycogen is

utilized in molting, adaptation to hypoxia and/or anoxia,

osmoregulation, growth, in the different stages of reproduction,

and during fasting periods (Hu, 1958; Chang and O’Connor,

1983; Kucharski and Silva, 1991a, 1991b; Oliveira and Da

Silva, 2000; Oliveira et al., 2001a, b).

Since very little is known about the physiology of Aegla, the

aim of this study is to evaluate the effect of circadian and

seasonal variations on the metabolism of carbohydrates in

different tissues of the freshwater anomuran Aegla ligulata.

Material and methods

Samples of Aegla ligulata were collected at 0600, 1200 noon

and 1800 h one day, every month from August 1999 to August

2000 in the region of Tainhas, Sao Francisco de Paula, RS,

Brazil. The animals were separated according to sex, samples

of haemolymph were collected in the field with a syringe con-

taining potassium oxalate (10%) as an anti-clotting agent. The

G.T. Oliveira, F.A. Fernandes, G. Bond-Buckup, A.A. Bueno and R.S.M. Silva

Males

Winter

1 2 3

Females

Winter

Figure 1. Circadian and seasonal variations of haemolymphatic glucose levels in Aegla ligulata Bond-Buckup and Backup, 1994, males and

females. Data are given as mean ± SEM. The number of animals at each point varied between 15 and 20. The same letter denotes significantly

different means (P< 0.05). * denotes significantly different means of the spring (Sep, Oct and Nov), winter (Jun, Jul and Aug), summer (Dec, Jan

and Feb) and autumn (Mar, Apr and May). Numbers 1, 2 and 3 stand for the collection times: 0600, 1200 and 1800 h, respectively.

animals and the haemolymph samples were frozen in the field.

In the lab, the tissues (hepatopancreas, branchiae and muscle)

were removed and grouped according to collection time. Tissue

glycogen was extracted following Van Handel (1965) and

determined to be glucose (enzymatic oxidase method) upon

acid hydrolysis (HCl) and neutralisation (Na 2 C 03 ), and the

results were expressed in mmol g“^ The levels of haemolym-

phatic glucose were dosed according to the enzymatic oxidase

method (Biodiagnostica: enz-color glucose kit), and the results

were expressed in mmol 1“^ The number of animals collected

varied between 15 and 45 per season of the year (winter: June,

July and August; spring: September, October and November;

summer: December, January and February; autumn: March,

April and May).

For the statistical analysis of the circadian and seasonal vari-

ations found, a one-way ANOVA test was used, followed by

Tukey’s comparison test. For the comparison between sexes, a

t-Test for the independent samples was used. The significance

level adopted was 5%, and the statistical analyses were carried

out in the program Statistical Package for the Social Sciences

(SPSS) for Windows. The Sigma Stat software was used to con-

firm parametrisation of the data.

Results and discussion

The concentrations of tissue glycogen and glucose in the

haemolymph in this study were similar to those of other crus-

tacean species, including those of the same genus {Aegla

platensis) (Kucharski and Da Silva, 1991b; Oliveira et ah,

2001b). The behaviour of such metabolic parameters, however,

differs in relation to circadian and seasonal variations.

The levels of haemolymphatic glucose of males and females

did not vary during the day (Fig.l). Males presented higher

glycemic levels (p<0.05) than females at 1800 h in the summer,

and at 0600 h and 1800 h in the winter. Females, however,

had higher levels than males only at 1200 h in spring. Such

findings suggest differences in exploration and/or feeding

time for males and females. Studies on A. ligulata, developed

by Bueno and Bond-Buckup (2001), have shown an increase

both in feeding activity and repletion degree at 1800 h, regard-

less of season of the year. Furthermore, in the autumn

months of March, April and May, no difference was found in

males or females. In this period. May, Bueno and Bond-Buckup

(2000) found a higher number of females with eggs in this

species.

Variations of the metabolism of carbohydrates in Aegla

Females

I 4

C5 *=

Hepatopancreas

O 00

^ rh » ’

^cogen

mol/g

<Ji

Figure 2. Seasonal variation of glycogen levels in tissues of males and females of Aegla ligulata Bond-Buckup and Buckup, 1994. Data are given

as mean ± SEM. The number of animals in each point varied between 40 and 60. The same letter denotes significantly different means (P< 0.05).

Numbers 1, 2, 3 and 4 stand for seasons: winter (Jun, Jul and Aug), spring (Sep, Oct and Nov), sununer (Dec, Jan and Feb) and autumn (Mar, Apr

and May), respectively.

In spring the highest concentrations of haemolymphatic

glucose were found both in males and females; they were sig-

nificantly higher than those found in the winter, summer and

autumn. Similar results were found elsewhere, in the region of

Taquara, for the crustacean A. platensis (Oliveira et ah, 2001b).

Bueno and Bond-Buckup (2001) working with A. ligulata,

mentioned that food is more plentiful in the environment in

spring and this secies presented higher feeding activity. The

food items of A. ligulata varied according to season; in spring

there is a predominant consumption of macrophytes and, in

summer and autumn, insects are consumed in the same propor-

tion. In winter, however, insects are the predominant food item.

These results permitted Bueno and Bond-Buckup (2001) to

characterize A. ligulata as an opportunistic omnivore.

Haemolymphatic glucose is the result of influx of intestinal

glucose, of the gluconeogenic pathway and utilisation

of this hexose in different processes (Hu, 1958; Chang and

O’Connor, 1983; Herreid and Full, 1988; Oliveira and Da

Silva, 1997).

There were no variations during the day for glycogen

levels in different tissues in males or females; for this reason

data from different times were grouped for in the study of sea-

sonality. No seasonal variations in tissue glycogen levels were

found in females. The males in winter, however, showed

hepatopancreatic glycogen levels 3 and 2.5 times as high

(p<0.05) as those verified in summer and autumn, respectively

(Fig. 2). In winter the exploratory activity of Aegla is reduced,

and this fact is reflected by the difficulty of collection. In other

crustaceans a shorter activity period and decreased metabolism

have been observed, as well as a higher glycogen level in the

hepatopancreas during winter, June-August (Kucharski and Da

Silva, 1991b; Nery and Santos, 1993). This fact may account

for the higher glycogen levels in the hepatopancreas during

winter. Different results were found in females of A. platensis

(Oliveira et ah, 2001b). In this species seasonal variations were

found in the levels of tissue glycogen, where the hepatopan-

creas showed higher values in autumn (p<0.05) than in other

seasons and males did not show seasonal variation (Oliveira et

ah, 2001b).

The different tissues analysed seem to have the same

capacity to store glycogen in both males and females (Fig. 2).

According to Hochachka et al. (1970), this independence from

a central deposit of glycogen seems to be an important adapta-

tion of animals with an exoskeleton and open circulation, since

their blood would flow slowly and under low pressure, leading

to less effective distribution of glucose to the tissues. The cir-

culatory systems are highly efficient and controlled in a com-

plex manner, and cardiac outflow is not distributed equally

among the vascular circuits during activity and hypoxia

(McMahon, 2001). This adaptation would allow for animals to

respond faster and more effectively to different environmental

stresses. As the glycogen values in different tissues of both

sexes were compared, no significant differences were found. It

can be noted that such findings differ from those for a popula-

tion of Aegla platensis (Oliveira et al., 2001b).

Acknowledgements

This work was supported in part by grants from FAPERGS,

CNPq and Program of the Post-Graduation in Animal

Biology/UFRGS. The authors thank reviewers for their

assistance.

G.T. Oliveira, F.A. Fernandes, G. Bond-Buckup, A.A. Bueno and R.S.M. Silva

References

Bueno, A.A.P., and Bond-Buckup, G. 2000. Dinamica populacional de

Aegla ligulata (Crustacea, Aeglidae). I Congresso brasileiro sobre

Crustaceos, Sao Pedro, SP, Brasil, 16 a 20 de outubro. P 63.

Bueno, A.A.P, and Bond-Buckup, G. 2001. Feeding habits of Aegla

ligulata Bond-Buckup & Buckup (Decapoda, Anomura, Aeglidae).

Abstracts, Fifth International Crustacean Congress, Melbourne,

Australia, 9-13 July 2001. P. 46.

Chang, E., and O’Connor, J.D. 1983. Metabolism and transport of

carbohydrates and lipids. Pp . 263-287 in: Mantell, L.H. (ed.). The

biology of Crustacea. Vol. 5. Internal anatomy and physiological

regulation. Academic Press: New York.

Herreid, C.F., and Full, R.J. 1988. Energetics and locomotion. Pp.

333-377 in: Burggren, W.W., and McMahon, B.R. (eds). Biology of

the land crabs. Cambridge University Press: Cambridge.

Hochachka, P.W., Somero, G.N., Schneider, D.E., Freed, J.M. 1970.

The organization and control of metabolism in the cmstacean gill.

Comparative Biochemistry and Physiology 33: 529-548.

Hu, A.S.L. 1958. Glucose metabolism in the crab Hemigrapsus nudus.

Archives of Biochemistry and Biophysics 75: 387-395.

Johnston, M.A., and Davies, PS. 1972. Carbohydrates of the

hepatopancreas and blood tissues of Carcinus. Comparative

Biochemistry and Physiology 4 IB: 433^43.

Kucharski, L.C.R., and Da Silva, R.S.M. 1991a. Effect of diet com-

position on the carbohydrate and lipid metabolism in an estuarine

crab, Chasmagnathus granulata (Dana, 1851). Comparative

Biochemistry and Physiology 99 A: 215-218.

Kucharski, L.C.R., and Da Silva, R.S.M. 1991b. Seasonal variation on

the energy metabolism in an estuarine crab, Chasmagnathus gran-

ulata (Dana, 1851). Comparative Biochemistry and Physiology

lOOA (3): 599-602.

McMahon, B.R. 2001. Control of cardiovascular function and its evo-

lution in Crustacea. Journal of Experimental Biology. 204:

923-932.

Nery, L.E.M., and Santos, F.A. 1993. Carbohydrate metabolism during

osmoregulation in Chasmagnathus granulata Dana, 1851

(Crustacea, Decapoda). Comparative Biochemistry and Physiology

106B (3): 747-753.

Oliveira, G.T., and Da Silva, R.S.M. 1997. Gluconeogenesis of

hepatopancreas of Chasmagnathus granulata crabs maintained on

high-protein or carbohydrate rich diets. Comparative Biochemistry

and Physiology 118 A (4): 1429-1435.

Oliveira, G.T., and Da Silva, R.S.M. 2000. Hepatopancreas gluconeo-

genesis during hyposmotic stress in crabs Chasmagnathus granula-

ta maintained on high-protein or carbohydrate-rich diets.

Comparative Biochemistry and Physiology 127B: 375-381.

Oliveira, G.T., Rossi, I.C.C., and Da Silva, R.S.M. 2001a.

Carbohydrate metabolism during anoxia and post-anoxia recovery

in Chasmagnathus granulata crabs maintained on high-protein or

carbohydrate -rich diets. Marine Biology 139(2): 335-342.

Oliveira, G.T., Fernandes, F.A., Bond-Buckup, G., Bueno, A.A., and

Da Silva, R.S.M. 2001b. Circadian and seasonal variations of the

metabolism of carbohydrates in Aegla platensis (Crustacea,

Aeglidae). Abstracts, Fifth International Crustacean Congress,

Melbourne, Australia, 9-13 July 2001. P. 117.

Van Handel, E. 1965. Estimation of glycogen in small amount soft

tissue. Analytical Biochemistry 11: 256-265.

Memoirs of Museum Victoria 60(1): 63-70 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

Endemic and enigmatic: the reproductive biology of Aegla (Crustacea: Anomura:

Aeglidae) with observations on sperm structure

Christopher C. Tudge

Biology Department, American University, 4400 Massachusetts Ave. NW, Washington, DC 20016-8007, USA and

Department of Systematic Biology, National Museum of Natural History, Smithsonian Institution, Washington, DC

20560-0163, USA (ctudge@american.edu and tudge.christopher@nmnh.si.edu)

Abstract Tudge, C.C., 2003. Endemic and enigmatic; the reproductive biology of Aegla (Cmstacea: Anomura: Aeglidae) with

observations on sperm structure. In: Lemaitre, R., and Tudge, C.C. (eds). Biology of the Anomura. Proceedings of a sym-

posium at the Fifth International Crustacean Congress, Melbourne, Australia, 9-13 July 2001. Memoirs of Museum

Victoria 60(1): 63-70.

The endemic South American family of freshwater anomurans, Aeglidae, consists of three genera: the fossils

Haumuriaegla Feldmann and Protaegla Feldmann et al., and the extant Aegla Leach. In Aegla there are >60 described

species from Argentina, Bolivia, Brazil, Chile, Paraguay, and Uruguay, between 20°S and 50°S. Very little is known

about the reproductive biology of Aegla. This paper summarises this information based on study of the extensive pre-

served collections in the National Museum of Natural History, Smithsonian Institution, and on data from the literature.

The data presented includes female reproductive cycles, mating behavior, external reproductive morphology of males

and females, and internal reproductive morphology of males. Areas for future research in the reproductive biology of

aeglids are indicated. The ultrastructure of spermatophore-like lobes and spermatozoa are described and illustrated for

males of Aegla longirostri Bond-Buckup and Buckup and Aegla rostrata Jara. No distinctly structured spermatophores

are present, and spherical sperm cells appear polymorphic. Both these characteristics are unusual, although not unique,

for an anomuran crab.

Keywords Cmstacea, Anomura, Aeglidae, Aegla, reproduction, sperm

Introduction

The anomuran family Aeglidae Dana, 1852 contains more than

60 species in the genus Aegla Leach, 1820 and two fossil

species Haumuriaegla glaessneri Feldmann, 1984 and

Protaegla miniscula Feldmann et ah, 1998. The species of

Haumuriaegla was found in late Cretaceous marine rocks at

Cheviot, New Zealand (Feldmann, 1984), while Protaegla is

from marine red limestone in quarries at Tepexi, Mexico

(Feldmann et ah, 1998). The fossil species are the only

members of the family outside South America. Extant species

of Aegla have a limited distribution across six countries in

South America between latitudes 20° S and 50° S (see Bond-

Buckup and Buckup, 1994, 1998, 1999 for reviews on aeglid

taxonomy and biogeography). The restricted range of Aegla is

very similar to the endemic South American parastacid fresh-

water crayfish genera, Parastacus Huxley 1878, Samastacus

Riek, 1971, and Virilastacus Hobbs, 1991, and suggests a

similar route of colonisation. In fact, their ranges overlap so

extensively that Riek (1971) suggested that competitive

exclusion by aeglids forced crayfish out of streams and rivers

and into burrowing lifestyles along river banks and fields.

The discovery of the fossil Haumuriaegla in marine rocks in

New Zealand (Feldmann, 1984) strengthened the arguments of

Ortmann (1902) that aeglids invaded South America from the

sea on the southern Pacific coast and then extended their range

eastwards into freshwater systems, toward the Atlantic coast.

Dispersal in the opposite direction (Atlantic to Pacific) has

been suggested by others (Schmitt, 1942b; Ringuelet, 1949;

Morrone and Lopretto, 1994, 1995) and is based on the

premise that the least ornamented morphology, seen in the

Atlantic species of Aegla, is the plesiomorphic condition. The

fact that the Cretaceous fossil Haumuriaegla is heavily orna-

mented with spines and tubercles would seem to contradict this

argument. The recent discovery of the fossil Protaegla in early

Cretaceous marine rocks in Mexico, extends the stratigraphic

and geographic range of the family, and adds further support to

the marine origin of the family.

Crandall et al. (2000) have suggested that the sister-group to

the parastacid crayfish of South America are Australian and

New Zealand genera (based on the 16s mitochondrial gene).

This result may suggest a similar dispersal and colonisation

route for parastacids and Aeglidae.

The early confusion surrounding the taxonomy and

C.C. Judge

systematics of the genus Aegla was discussed by Martin and

Abele (1988) and Bond-Buckup and Buckup (1994, 1998,

1999) who listed described species, distributions, and refer-

ences. The relationship of Aeglidae to the other anomuran fam-

ilies remains unresolved. Milne Edwards and Bouvier (1894;

243 and 311) derived the aeglids from marine hermit crabs and

placed them on a direct lineage to the galatheids. Recently,

Martin (1985, 1989) and Martin and Abele (1988) linked

aeglids with hermit crabs (paguroids and coenobitoids) rather

than with the galatheids, although a sister-group relationship

with the Galatheoidea had been suggested earlier by Martin and

Abele (1986). Representatives of the Aeglidae were included in

some recent phylogenetic analyses of anomuran relationships

(McLaughlin and Lemaitre, 1997; Perez-Losada et al., 2001,

2002) but were absent from an analysis based on reproductive

characters (Tudge, 1997). Further, some species of Aegla have

been the subject of more focused studies of intrageneric rela-

tionships (Schuldt et al., 1988; D' Amato and Corach, 1997),

biogeographic studies on areas of endemism (Morrone and

Lopretto, 1994, 1995), and more recently phylogeny within the

Chilean representatives of the family (Perez-Losada et al.,

2000 ) .

This paper summarizes available information on reproduc-

tion in Aegla for the first time. Particular aspects of the repro-

ductive biology of aeglids that still require investigation are

highlighted. Novel data on the form of spermatophore-like

lobes in the male reproductive system and light microscope and

ultrastructural observations of spermatozoa of A. longirostri

Bond-Buckup and Buckup, 1994 and A. ro strata idX2i, 1977 are

also presented.

Materials and methods

A single male of Aegla rostrata was collected by Dr Carlos Jara

from Lake Rinihue, Valdivia Provence, Chile on 13 Nov 1995.

The gonads were removed and fixed in 3% glutaraldehyde in

phosphate buffer. A squash of tissue was examined and

photographed through a Leitz Orthoplan 2 microscope with

Nomarski phase contrast, and attached Wild Photoautomat

MPS 45 photomicrography system. Kodak T-Max 100 ASA

black and white film was used. The remainder of the tissue was

processed for transmission electron microscopy (TEM).

Gonads were dissected from three species of Aegla, collect-

ed by Mr Perez-Losada on 30 Oct 2000, in Rio Grande do Sul,

Brazil, and fixed in 3% glutaraldehyde in phosphate buffer.

Specimens of A. grisella Bond-Buckup and Buckup, 1994 and

A. spinipalma Bond-Buckup and Buckup, 1994 were collected

in the Sangao River and the Capingui River, respectively, while

a single A. longirostri was collected from the Carreiro River.

Light microscope observations were made of the fixed tissues

before they were processed for TEM (see Tudge et al., 2001).

Seven additional specimens of Aegla were collected by Mr

Perez-Losada in Chile and Argentina, 17-24 Feb 2000, fixed in

70% ETOH: A. affinis Schmitt, 1942, Maula River, Province of

Taloa, Chile; A. papudo Schmitt, 1942, Rabuco River, Province

of Quillota, Chile; A. neuquensis Schmitt, 1942, Chico River,

Province of Mendoza, Argentina; A. pewenchae Jara, 1994,

Lake Lialuia, Chile. External and internal reproductive

morphology of all specimens was observed.

The identified aeglid collection (958 specimens from 22

species, including types) of the National Museum of Natural

History, Smithsonian Institution, Washington D.C. (USNM)

was examined, and sex ratio, date of collection, and presence of

ovigerous females were recorded. Data for ovigerous females

was supplemented from the literature.

Results and discussion

Sex ratio. The sex ratio (males to females) of an Aegla species

was first reported as approximately 1:1 by Mouchet (1932, as

Aeglea laevis). However, this species does not occur in

Uruguay (G. Bond-Buckup and L. Buckup, pers. comm.) and

therefore must be attributed to another taxon, possibly

A. uruguayana Schmitt, 1942 or A. platensis Schmitt, 1942.

Subsequent authors have stated that the sex ratio is usually 1 : 1

but may vary according to time of year, season, and where in

the river specimens were collected (Bahamonde and Lopez,

1961; Lopez, 1965; Bums, 1972). More recently, Bueno and

Bond-Buckup (2000) found a sex ratio of 1.08:1, in populations

of A. platensis in the Mineiro River, Brazil and a ratio of 1 : 1

has been recorded for A. castro Schmitt, 1942 in Ponta Grossa,

Brazil, by Swiech-Ayoub and Masunari (2001b).

Aeglids are gregarious animals known to congregate in

large numbers at the river's edge, especially during the spawn-

ing season (Bahamonde and Lopez, 1961; Burns, 1972; Martin

and Abele, 1988). After mating, the number of females is great-

est on the riverbanks, while the males return to the deeper water

in the centre of the river. This sex-specific separation of habitat

at this time may account for the observation by Mouchet

(1932), that no males of Aegla sp. (as Aeglea laevis) were

found at the end of winter (September-October) around

Montevideo, Uruguay.

When investigating the sex ratio in the aeglid collection at

USNM, the Aegla holdings were found to be biased toward

male specimens (4:1). This under-representation of females

across all 22 species in the collection further compounded the

search for ovigerous females, of which there were only 40

specimens (4.2%). The paucity of female specimens in the

USNM collections represents a collection bias favouring males,

and enhanced by local cultural and ethical practices of not col-

lecting ovigerous females (L. Buckup and G. Bond-Buckup,

pers. comm.).

Mating. Aeglids are sexually dimorphic in a number of fea-

tures. These include: the presence of abdominal pleopods in

females over 12 mm carapace length (cl), a larger carapace

(both length and width) in males, larger and unequal chelipeds

in males, narrower abdomens in males, and difference in loca-

tion of the ventral gonopores (Bahamonde and Lopez, 1961;

Burns, 1972). An ovigerous female of 9.87 mm cl was found by

Bueno and Bond-Buckup (2000) for A. platensis, and appears

to be the smallest female with eggs recorded to date. As far as

can be ascertained, observations on mating behaviour have not

previously been documented for any species of Aegla. No

information appears to be available on whether pre- or post-

copulatory mate guarding occurs or where mating occurs in the

moult cycle. However, two instances (one in the wild and one

in an aquarium) of finding male-female pairs in a sternum to

Reproductive biology of Aegla

sternum position, engaged in mating behavior, were recounted

to me (J. W. Martin, pers. comm). On both occasions the

animals separated upon being disturbed and no evidence of

sperm transfer was seen. A ventral to ventral mating position

would seem the most obvious for these crabs as has been

commonly illustrated for other anomurans (e.g. Kamalaveni,

1949; Efford, 1967; Hazlett, 1968; Helfman, 1977; Wada et al.,

1997; Hess and Bauer, 2002).

There is no published information about the size at sexual

maturity for males of any Aegla species. Female size at sexual

maturity has been recorded as a minimum of 12.5 mm cl (all

mature by 20.5 mm) (Bahamonde and Lopez, 1961; Burns,

1972) for female A. laevis, and between 9.8 mm and 17.7 mm

cl (Bueno and Bond-Buckup, 2000) in female A. platensis.

Female reproductive biology. Sexually mature females of

Aegla can be distinguished from males primarily in the pres-

ence of four pairs of abdominal pleopods, and position of the

gonopores (= genital pores) on the coxae of the third pereopods

(P3) (Bahamonde and Lopez, 1961; Bums, 1972; Martin and

Abele, 1988). Illustrations of the gonopores and the pleopods in

females of A. platensis can be found in Martin and Abele (1988,

figs 10 and 16). The pleopods are used to carry fertilized eggs

during the spawning period, and during this time eggs are

groomed often to keep them aerated and clean of ectoparasites

(Martin and Felgenhauer, 1986). Burns (1972) stated that

females do not moult while brooding eggs, but no further infor-

mation is available on the synchrony of the moult cycle and the

reproductive cycle in Aegla. The eggs are spherical, small and

have been described as pale yellow, orange, or reddish

(Mouchet, 1932; Bahamonde and Lopez, 1961; Lopez, 1965;

Burns, 1972; Jara, 1977). Measurements of aeglid egg diameter

vary between species and have been recorded as 0.8-1.35 mm

(Lopez and Sawaya, 1960; Bahamonde and Lopez, 1961;

Lopez, 1965) in A. laevis, 1. 1-1.5 mm (Lopez and Sawaya,

1960; Lopez, 1965) in A. paulensis Schmitt, 1942 (as A. ode-

brechtii paulensis), 1.2 mm (Jara, 1977) in A. rostrata, 2.2 mm

(Swiech-Ayoub and Masunari, 2001b) in A. castro. Bahamonde

and Lopez (1961: fig. 17) illustrated eggs attached to the female

and further provide information on the range and frequency of

egg size and numbers per female in A. laevis. The fecundity of

females has been stated as 64-255 (Lopez, 1965) eggs per

female in A. paulensis, an average of 100 (Jara, 1977) in

A. rostrata, and 90-204, average = 121 (Swiech-Ayoub and

Masunari, 2001a) in A. longirostri.

The eggs have abundant yolk, direct development, no free-

swimming larval forms and therefore hatch as juveniles, resem-

bling adults (Mouchet, 1932; Martin, 1989; Bond-Buckup et

al., 1996, 1998, 1999; Bueno and Bond-Buckup, 1996). The

complete embryonic development of Aegla platensis has

recently been documented as occurring in ten distinct, post-

fertilisation, morphological stages (Lizardo-Daudt and

Bond-Buckup, 2002).

The timing of spawning differs between species and

between populations of the same species. Females of Aegla

castro and A. longirostri live for about two years, and can

reproduce in both years (Swiech-Ayoub and Masunari, 2001a,

2001b). A review of literature and examination of specimens in

the USNM collections reveal that in 13 species of Aegla,

ovigerous females have been found in every month except

November and December (Fig. 1). However, in A. platensis

some ovigerous females were collected in these months (Bueno

and Bond-Buckup, 2000) making it the only species that poten-

tially breeds all year round. Spawning times and/or collection

of ovigerous females can be found in Swiech-Ayoub and

Masunari (2001a, b) for A. castro, Jara (1989) for A. denti-

culata Nicolet, 1849, in Mouchet (1932), Bahamonde and

Lopez (1961) and Burns (1972) for A. laevis, in Lopez (1965)

for A. paulensis, in Rodrigues and Hebling (1978) for

A. perobae Hebling and Rodrigues, 1977, in Bueno and Bond-

Buckup (2000) for A. platensis, and in Jara (1977) for

A. rostrata. The internal morphology of the female repro-

ductive system has yet to be described or illustrated in the

literature.

Male reproductive biology. Aeglid males have no easily

observed abdominal pleopods, but some vestigial pleopodal

remnants have been recorded (Martin and Abele, 1988) on

abdominal segments 3 and 4 in Aegla platensis. The male gono-

pores are on the coxal segment of pereopod 5 (P5) (Burns,

1972; Martin and Abele, 1988), as with all decapods, but

aeglids have an additional, tube-like extension. This tube was

first illustrated in Aeglidae by Milne Edwards and Bouvier

(1894: 240, fig. 30), and the taxonomic significance of the sex-

ual tube morphology was recognised by Schmitt (1942a: 28).

He stated that there "seem to be some differences in the relative

proportions of the protruding sperm ducts on the reduced fifth

legs" between A. abtao Schmitt, 1942 and A. concepcionensis

Schmitt, 1942 and that the importance of this observation was

being investigated.

As has been recorded in many freshwater crayfish, intersex

males (exhibiting both male and female secondary sexual char-

acteristics) have been observed in several species of Aegla

(L. Buckup and G. Bond-Buckup, pers. comm.).

Lopretto (1978a) described the internal and external mor-

phology of the fifth pereopod of 12 species of Argentine

aeglids, including detailed drawings, and photographs, showing

the fine structure of P5 and associated tube. Lopretto recog-

nised the systematic and phylogenetic importance of this male

sexual character, established a specific nomenclature for its

structure, devised a key to these species based on P5 and tube

morphology, and carefully documented tube diversity across

these Argentine species. In doing so, she established several

distinctive species groups based solely on P5 and tube charac-

teristics (Lopretto, 1978a, 1978b, 1979, 1980a, 1980b, 1981).

Internal morphology of the reproductive system of male

aeglids is virtually unknown. Mouchet (1932) stated that an

Aegla species (as Aeglea laevis) males do not have sper-

matophores and recognised that this was exceptional among

galatheoids. Lopretto (1978a: 288) vaguely described the male

reproductive system as seen under the light microscope and

noted small capsules with cellular elements and delicate inter-

mediary connective threads. Lopretto's remarks could refer to

spermatozoa with microtubular arms bundled into lobes within

the testis and vas deferens, as observed in Tudge and Scheltinga

(2002) and during this study (Fig. 2).

C.C. Judge

Month

Species

A. laevis laevW

A. denticulata^

A. papudo

A. Parana

A. platensis^

A. castro^

A. prado

A. schmitti

A. uruguayana

A. neuquensis

A. perobe^

A. rostrata^

A. paulensis^

Jan Feb Mar Apr May Jun Jul Aug Sept Oct Nov Dec

2 1

Figure 1. Occurrence of ovigerous females of Aegla species obtained from literature sources and USNM specimens. Total USNM speci-

mens examined = 958 (40 ovigerous females). Symbols; ' Bahamonde and Lopez (1961); ^ Jara (1989); ^ Bueno and Bond-Buckup (2000);

^ Swiech-Ayoub and Masunari (2001a, 2001b); ^ Rodrigues and Hebling (1978); ® Jara (1977); ^ Lopez (1965). Shading = range from literature

sources indicated. Solid black bar = number from USNM collection for that month.

Mouchet's (1932) statement on spermatophores is supported

by observations presented herein of the male reproductive mor-

phology (Fig. 2A) in Aegla rostrata. No distinct, encapsulated,

spermatophores were observed in the vas deferens of A. ros-

trata, and instead there are only thin walled, spherical to

oblong, lobes containing the sperm cells. These lobes were

approximately 0.5-1 mm in size and bound by a thin, translu-

cent membrane. Terminally, some exhibited a distinct line or

fold, which may represent some sort of lumen. Presumably

these blind-ending, spermatophoric lobes, empty into a

common duct, or ducts, in the testis or vas deferens.

When a squash of these lobes was made on to a slide and

observed using transmitted light microscopy, their contents

revealed many different sized and shaped cells. Among this

array of cells the spermatozoa were periodically scattered (Fig.

2B). Although themselves polymorphic, the sperm cells dis-

played a distinct suite of characteristics that identified them as

decapod/anomuran sperm cells (Jamieson and Tudge, 2000;

Tudge and Scheltinga, 2002). The roughly spherical to ovoid

cells contained a smaller spherical vesicle (sometimes clearly

ring-shaped) at one pole, and an adjacent coarse granular zone

(Fig. 2B-G). These small vesicles represent the acrosome

vesicles embedded in the cytoplasmic region. More obviously

the spermatozoa were seen to have long, filamentous arms radi-

ating from the central cell mass. The number and position of

these arms is variable, from none being visible, to a maximum

of three (Fig. 2E, G). Analysis at the electron microscope level

(Tudge and Scheltinga, 2002; this study Fig. 3) revealed these

filaments, or arms, to be the bundles of microtubules common

to all anomuran spermatozoa recorded to date (Tudge, 1997;

Jamieson and Tudge, 2000).

Under the transmission electron microscope the spermato-

zoa of Aegla rostrata, although slightly irregular in shape, were

found to have a consistent ultrastructure. The spherical to ovoid

sperm cells are approximately 5 pm wide and 4 pm in height

(through the acrosomal axis), with the acrosome vesicle being

1.5 pm in diameter. The entire sperm cell can be divided into

two hemispheres; the upper (or acrosomal) one containing the

Reproductive biology oiAegla

Figure 2. Light micrographs of Aegla rostrata Jara, 1977. A, Spermatophoric lobes; B-G, Squash of spermatophoric lobe contents showing sper-

matozoa (arrowheads) scattered amongst assorted cells (Asterisk in E and G indicate individual spermatozoa with three microtubular arms).

C.C. Judge

Figure 3. Transmission electron micrograph of spermatozoon of Aegla

longirostri Bond-Buckup and Buckup, 1994 in longitudinal section.

Abbreviations: av, acrosome vesicle; cy, cytoplasm; m, mitochon-

drion; ms, membrane system; mt, microtubular bundle; n, nucleus;

p, perforatorial column; pm, periacrosomal material.

acrosome and cytoplasmic elements, the lower (or nuclear) one

the nucleus (Tudge and Scheltinga, 2002; this study Figs 3, 4).

The acrosome vesicle is irregular in shape and is composed of

an electron-dense outer ring with an electron-pale central area.

This central column can be posteriorly penetrated by irregular

intrusions. Cytoplasmic elements include many circular mito-

chondria, membrane bundles or arrays, and sometimes a

centriole is visible immediately posterior to the acrosome. The

nucleus is coarsely granular, more electron-dense than the cyto-

plasm, and is penetrated by the bases of the microtubular arms,

which are mostly evident as short bundles of microtubules in

oblique section (Tudge and Scheltinga, 2002; this study Figs 3,

4). All the spermatozoa observed exhibited the above

ultrastructural characteristics, with differences between sperm

cells being in their overall shape, and in the irregular, often

crenulated, dense region of the acrosome.

In summary, it can be clearly seen that much research is still

needed to gather basic information on reproductive cycles and

morphology in aeglids. Areas of future research that would be

fruitful include, but are not restricted to, observations on mat-

ing behaviour, timing of mating during the moult cycle, sperm

transfer mechanisms, male sexual tube(?) morphology and

microstructure, male and female reproductive system gross

morphology, egg ultrastructure, and further spermatophore and

sperm cell ultrastructure. The latter is needed to confirm that

the novel observations provided above, and in Tudge and

Scheltinga (2002), are representative for the genus and family.

Acknowledgements

The author wishes to thank Carlos Jara (Universidad Austral de

Chile, Chile), Ludwig Buckup, Georgina Bond-Buckup

Figure 4. Semidiagrammatic representation of longitudinal section of

spermatozoon of Aegla longirostri Bond-Buckup and Buckup, 1994,

based on a micrograph (Fig. 3).

(Universidade Federale do Rio Grande do Sul, Porto Alegre,

Brazil), and Marcos Perez-Losada (Brigham Young University,

Utah, USA) for collecting specimens of aeglids from various

localities in Chile, Argentina, and Brazil. Alexandre Almeida

(Universidade Estadual de Santa Cruz, Brazil) and Alessandra

Bueno (Universidade Federale do Rio Grande do Sul, Porto

Alegre, Brazil) are thanked for providing important literature.

Dave Scheltinga and Lina Daddow (Department of Zoology

and Entomology, University of Queensland, Australia) provid-

ed expert assistance with the fixation and processing for trans-

mission electron microscopy of the aeglid reproductive materi-

al. This research was started when the author was a

Smithsonian Institution Postdoctoral Eellow (1995-1996) in the

then Department, and now section, of Invertebrate Zoology,

NMNH, Washington DC, and was completed while a research

associate (1999-2002) at the same institution. Kristian

Eauchald and Rafael Lemaitre are thanked for access to facili-

ties within that Department.

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America. Proceedings of the Biological Society of Washington

115(1); 118-128.

Tudge, C.C., Scheltinga, D.M., and Jamieson, B.G.M. 2001.

Spermatozoal morphology in the "symmetrical" hermit crab,

Pylocheles (Bathycheles) sp. (Cmstacea, Decapoda, Anomura,

Paguroidea, Pylochelidae). Zoosystema 23(1): 117-130.

Wada, S., Ashidate, M., and Goshima, S. 1997. Observations on the

reproductive behavior of the spiny king crab Paralithodes brevipes

(Anomura: Lithodidae). Crustacean Research 26: 56-61.

Memoirs of Museum Victoria 60(1): 71-77 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

A worldwide list of hermit crabs and their relatives (Anomura: Paguroidea)

reported as hosts of Isopoda Bopyridae

John C. Markham

Abstract

Keywords

Arch Cape Marine Laboratory, 108 W. Markham Avenue, Arch Cape, OR 97102-0105, USA (jmarkham@seasurf.com)

Markham, J.C., 2003. A worldwide list of hermit crabs and their relatives (Anomura: Paguroidea) reported as hosts of

Isopoda Bopyridae. In; Lemaitre, R., and Tudge, C.C. (eds). Biology of the Anomura. Proceedings of a symposium at

the Fifth International Crustacean Congress, Melbourne, Australia, 9-13 July 2001. Memoirs of Museum Victoria 60(1):

71-77.

Hermit crabs and their relatives in the anomuran superfamily Paguroidea are among the most frequently reported hosts

of bopyrid isopods, all species of which are parasites of decapod crustaceans in general. This report serves, for the first

time, to collect the widely scattered records of paguroid infestation into a single list with both host and parasite names

updated to conform with the currently accepted nomenclature; each entry includes the geographical locality for the occur-

rence of each species of parasite on each species of host and the citation of the publication in which it was reported. The

known host paguroids are in the Diogenidae (48 species plus 3 others not identified to species), Lithodidae (6), Paguridae

(52 + 7), and Parapaguridae (3 + 1). Their parasites belong to three bopyrid subfamilies, the Pseudioninae (32 species

occurring in the branchial chambers of hosts), the Athelginae (41 species clinging to the abdomens of their hosts), and

the Bopyrophryxinae (one species attached simultaneously to branchiae and abdomen of their hosts).

Cmstacea, Anomura, Paguroidea, Isopoda, Bopyridae, species list

Introduction

The epicaridean isopod family Bopyridae contains just over

500 described species worldwide in ten subfamilies, all of

which parasitise decapod crustaceans as adults. With one

exception, all known species are external parasites. Seventy-

four are known to infest hosts in the anomuran superfamily

Paguroidea.

So far, there are reports of 48 species of Diogenidae plus

three others identified only to genus serving as bopyrid hosts,

six species of Lithodidae, 52 species of Paguridae plus seven

identified only to genus or family, and three species of

Parapaguridae plus one identified only to genus. Their parasites

belong to three bopyrid subfamilies: Pseudioninae, the largest

and probably most primitive subfamily, whose species are

branchial parasites mainly of Anomura in general; the rather

small and evidently fairly advanced subfamily Athelginae, all

of whose species are dorsoabdominal parasites of paguroids

alone; and the monotypic subfamily Bopyrophryxinae, whose

single species is simultaneously a branchial and abdominal par-

asite of a parapagurid. Published records of the occurrences of

paguroid-infesting bopyrid isopods have been very widely scat-

tered; it is hoped that this compilation, by bringing them all

together for the first time, will be useful to readers seeking

information about both the hosts and their parasites.

The following is a list of all known Paguroidea hosts, their

recorded Bopyridae parasites, their known localities and refer-

ences reporting them. The families of the superfamily

Paguroidea are in accordance with the most recently published

classification of Martin and Davis (2001). The names of the

hosts and parasites have been corrected, as needed, to conform

with the most current taxonomic opinion, so they are not nec-

essarily those previously used in the original publications.

Superfamily Paguroidea

Coenobitidae

No records known.

Diogenidae

Allodardanus bredinii Haig and Provenzano, 1965:

Parathelges tumidipes Markham, 1972, Athelginae; Bermuda

(Markham, 1978).

Calcinus elegans (H. Milne Edwards, 1848): Parapagurion

calcinicola Shiino, 1933, Pseudioninae; Seto, Japan (Shiino,

1933).

C. morgani Rahayu and Forest, 1998: Propseudione rhom-

bicosoma Shiino, 1933, Pseudioninae; Irian Jaya, Indonesia

(Haig and Ball, 1988). Pseudostegias macdermotti Williams

and Boyko, 1999, Athelginae; Bali, Indonesia (Williams and

Boyko, 1999).

J.C. Markham

C. laevimanus (Randall, 1839): Propseudione rhombi-

cosoma Shiino, 1933, Pseudioninae; Seto, Japan (Shiino,

1933). Parathelges weberi Nierstrasz and Brender a Brandis,

1923, Athelginae; Maiwara, Papua New Guinea (Danforth,

1971), Irian Jaya, Indonesia (Haig and Ball, 1988).

C. latens (Randall, 1839): Pseudione calcinii (Shiino,

1958), Pseudioninae; Japan (Shiino, 1958).

C. lineapropodus Morgan and Forest, 1991: Parapagurion

calcinicola Shiino, 1933, Pseudioninae; Irian Jaya, Indonesia

(Haig and Ball, 1988). Anathelges muelleri Nierstrasz and

Brender a Brandis 1931, Athelginae; Irian Jaya, Indonesia

(Haig and Ball, 1988). Athelges sp., Athelginae; Irian Jaya,

Indonesia (Haig and Ball, 1988).

Ciliopagurus strigatus (Herbst, 1804): Athelges sp.,

Athelginae; Irian Jaya, Indonesia (Haig and Ball, 1988).

Clibanarius albidigitus Nobili, 1901: Bopyrissa magellan-

ica Nierstrasz and Brender a Brandis, 1931, Pseudioninae;

Pacific coast, Costa Rica (Nierstrasz and Brender a Brandis,

1931).

C. antillensis Stimpson, 1862: Asymmetrione clibanarii

Markham, 1975, Pseudioninae; Caribbean coast, Colombia

(Markham, 1988).

C. bimaculatus (De Haan, 1849): Asymmetrione asymmet-

rica (Shiino, 1933), Pseudioninae; Tanabe Bay, Japan (Shiino,

1933). Bopyrissa pyriforma (Shiino, 1958), Pseudioninae; Hong

Kong (Markham, 1982). Pseudione clibanaricola Shiino, 1933,

Pseudioninae; Tanabe Bay, Japan (Shiino, 1933).

Pseudostegias setoensis Shiino, 1933, Athelginae; Seto, Japan

(Shiino, 1933); Hong Kong (Markham, 1982).

C. digueti Bouvier, 1898: Pseudione sp., Pseudioninae; Gulf

of California, Mexico (Brusca, 1980).

C. englaucus Ball and Haig, 1972: Asymmetrione asymmet-

rica (Shiino, 1933), Pseudioninae; Irian Jaya, Indonesia (Haig

and Ball, 1988).

C. erythropus (Latreille, 1818): Bopyrissa fraiseii (Carayon,

1943), Pseudioninae; Arcachon, France (Bourdon, 1968).

Parathelges cardonae R. and M. Codreanu, 1968, Athelginae;

Corsica (Codreanu, 1968); Baleares Islands (Bonnier, 1900);

Mediterranean coast of Africa (Codreanu, 1961). Parathelges

racovitzai Codreanu, 1940, Athelginae; Corsica (Altes, 1962).

C. merguiensis de Man, 1888: Bopyrissa liberorum

Markham, 1985, Pseudioninae; Phuket, Thailand (Markham,

1985b). Pseudostegias dulcilacuum Markham, 1982,

Athelginae; Phuket, Thailand (Markham, 1985b).

C. padaverensis de Man, 1888: Pseudostegias setoensis

Shiino, 1933, Athelginae; Phuket, Thailand (Markham, 1985b).

C. signatus Heller, 1861: Asymmetrione shiinoi Codreanu et

al., 1965, Pseudioninae; Red Sea (Codreanu et al., 1965).

C. striolatus Dana, 1852: Pseudostegias setoensis Shiino,

1933, Athelginae; Taiwan (Shiino, 1958).

C. taeniatus (H. Milne Edwards, 1848): Pseudostegias

setoensis Shiino, 1933, Athelginae; Queensland, Australia

(Dunbar and Coates, 2000).

C. tricolor (Gibbes, 1840): Asymmetrione clibanarii

Markham, 1975, Pseudioninae; Florida, USA; Bahamas;

Caribbean coast, Colombia (Markham, 1988). Bopyrissa wolffi

Markham, 1978, Pseudioninae; Bermuda; Florida, USA;

Bahamas; Quintana Roo, Mexico; Puerto Rico (Markham,

1978; Markham et al., 1990). Parathelges occidentalis

Markham, 1972, Athelginae; Florida, USA; Bahamas;

Quintana Roo, Mexico (Markham, 1972). Stegias clibanarii

Richardson, 1904, Athelginae; Bermuda; Caribbean (Markham,

1979).

C. virescens (Krauss, 1843): Pseudostegias setoensis

Shiino, 1933, Athelginae; Queensland, Australia (Dunbar and

Coates, 2000). Unidentified, Indian Ocean coast. South Africa

(Barnard, 1950).

C. vittatus (Bose, 1802): Bopyrissa wolffi Markham, 1978,

Pseudioninae; North Carolina and Texas, USA (Markham,

1978).

Clibanarius sp. aff. longitarsus (De Haan, 1849): Pseudione

novaeguineensis Danforth, 1971, Pseudioninae; Maiwara,

Papua New Guinea (Danforth, 1971).

Clibanarius sp. aff. tricolor (Gibbes, 1840): Asymmetrione

clibanarii Markham, 1975, Pseudioninae; Ascension Island

(Markham, 1978).

Clibanarius sp.: Asymmetrione sp., Pseudioninae;

Puntarenas, Costa Rica (Markham, 1975). Bopyrella magellan-

ica Nierstrasz and Brender a Brandis, 1931, Pseudioninae;

Puntarenas, Costa Rica (Nierstrasz and Brender a Brandis,

1931).

Clibanarius sp.: Pseudione brandaoi Brian and Darteville,

1941, Pseudioninae; Congo (Brian and Darteville, 1941).

Clibanarius sp.: Pseudostegias atlantica Lemos de Castro,

1965, Athelginae; Ceara and Alagoas, Brazil (Lemos de Castro,

1965).

Dardanus arrosor (Herbst, 1796): Asymmetrione dardani

Bourdon, 1968, Pseudioninae; Atlantic coast, Morocco

(Bourdon, 1968). Parathelges carolii Codreanu, 1968,

Athelginae; Naples, Italy (Codreanu, 1968).

D. fucosus Biffar and Provenzano, 1972: Parathelges

tumidipes Markham, 1972, Athelginae; Jamaica (Markham,

1972).

D. gardineri Alcock, 1905: Athelges aegyptius Codreanu et

al., 1965, Athelginae; Red Sea (Codreanu et al., 1965). Athelges

caudalis Barnard, Athelginae; Inhambane, Mozambique

(Barnard, 1955).

D. rnegistos (Herbst, 1804): Athelginae, unidentified;

unspecified locality, Australia (Jones and Morgan, 1994).

Dardanus sp.: Pagurian tuberculata Shiino, 1933,

Pseudioninae; Tanabe Bay, Japan (Shiino, 1933).

Diogenes edwardsii (De Haan, 1849): Bopyrissa pyriforma

(Shiino, 1958), Pseudioninae; Mie Prefecture, Japan (Shiino,

1958); Hong Kong (Markham, 1982); southwest Korea (Kim

and Kwon, 1988). Athelges takanoshimensis Ishii, 1914,

Athelginae; Hong Kong (Markham, 1982). Pseudostegias dul-

cilacuum Markham, 1982, Athelginae; Hong Kong (Markham,

1982).

D. merguiensis de Man, 1888: Bopyrissa dawydoffi

(Codreanu and Codreanu, 1963), Pseudioninae; Thanh Hoa,

Vietnam (Codreanu and Codreanu, 1963).

D. pugilator (Roux, 1829): Bopyrissa diogeni (Popov,

1927), Pseudioninae; Black Sea; Channel Islands (Bourdon,

1968). Athelges paguri (Rathke, 1843), Athelginae; Roscoff,

France (Bourdon, 1967). Parathelges racovitzai Codreanu,

1940, Athelginae; Black Sea, Romania (Codreanu, 1940).

Hermit crabs and their relatives, hosts of Isopoda Bopyridae

Isocheles pilosus (Holmes, 1900): Asymmetrione ambodis-

torta Markham, 1985, Pseudioninae; California, USA

(Markham, 1985a).

Paguristes anahuachis Glassell, 1938: Pseudione sp.,

Pseudioninae; Gulf of California, Mexico (Brusca, 1980).

P. emerita (Linnaeus, 1767): Athelges pelagosae Babic,

1912, Athelginae; Adriatic Sea (Babic, 1912).

P. hummi Wass, 1955: unidentified. Florida, USA (Camp et

ah, 1977).

P. markhami Sandberg, 1996: Athelginae, unidentified;

Turks and Caicos Islands (Markham, 1978).

P. monoporus Morgan, 1987: Bopyrissa (?) sp.,

Pseudioninae; Man Jay a, Indonesia (Haig and Ball, 1988).

Parapagurion calcinicola Shiino, 1933, Pseudioninae; Phuket,

Thailand (Markham, 1985b). Parathelges whiteleggei

Nierstrasz and Brender a Brandis, 1931, Athelginae; Man Jaya,

Indonesia (Haig and Ball, 1988).

P. oculatus (Fabricius, 1775): Asymmetrione foresti

(Bourdon, 1968), Pseudioninae; Western Mediterranean

(Bourdon, 1968).

P oxyophthalmiis Holthuis, 1959: Parathelges piriformis

Markham, 1972, Athelginae; Caribbean coast, Colombia

(Markham, 1978).

P. perspicax (Nobili, 1906): Allathelges pakistanensis

Kazmi and Markham, 1999, Athelginae; Karachi, Pakistan

(Kazmi and Markham, 1999).

P. robustus Forest and de Saint Laurent, 1967: Pseudione

biacuta Bourdon, 1979, Pseudioninae; Uruguay (Bourdon,

1979).

P. subpilosus Henderson, 1888: Pseudostegias otagoensis

Page, 1985, Athelginae; Otago, New Zealand (Page, 1985).

P. tortugae Schmitt, 1933: Asymmetrione desuitor

Markham, 1975 (?), Pseudioninae; Abrolhos Bank, Brazil

(Bourdon, 1979). Parapagurion irnbricata Markhkam, 1978,

Pseudioninae; Cuba (Markham, 1978).

Strigopagurus boreonotus Forest, 1995: Pseudostegias

setoensis Shiino, 1933, Athelginae; Chesterfield Islands

(Markham, 1994).

Lithodidae

Dermaturus mandtii Brandt, 1850: Pseudione giardi Caiman,

1898, Pseudioninae; Alaska (Markham, 1975). Unidentified

branchial parasite, Pseudioninae?; Hokkaido, Japan

(Minemizu, 2000).

Hapalogaster dentata (De Haan, 1844): Pseudostegias

hapalogasteri Shiino, 1950, Athelginae; Mie, Japan (Shiino,

1950).

Lithodes murrayi Henderson, 1888: Unidentified,

Pseudioninae?; Crozet Islands (Vinuesa, 1989).

L. santolla (Molina, 1872): unidentified, Pseudioninae?;

Beagle Channel, Argentina (Vinuesa, 1989).

Neolithodes diomediae (Benedict, 1894): Pseudione tuber-

culata Richardson, 1904, Pseudioninae; Pampas, Argentina

(Richardson, 1904); South Georgia (Vinuesa, 1989).

Paralomis granulosa (Jacquinot, 1847): Pseudione tuber-

culata Richardson, 1904, Pseudioninae; Beagle Channel,

Argentina (Roccatagliata and Lovrich, 1999).

Paguridae

Anapagurus breviaculeatus Fenizia, 1937: Athelges tenuicaud-

is Sars, 1898, Athelginae; Mediteranean coast, Spain (Garcia-

Gomez, 1994).

A. chiroacanthus (Lilljeborg, 1856): Pseudione hyndmanni

(Bate and Westwood, 1868), Pseudioninae; Denmark; English

Channel (Bourdon, 1968). Athelges tenuicaudis Sars, 1898,

Athelginae; Scandinavia; British Isles; France (Sars, 1898).

A. hyndmanni (Bell, 1846): Athelges tenuicaudis Sars, 1898,

Athelginae; Atlantic coast, France (Bourdon, 1964).

A. japonicus Ortmann, 1892: unidentified branchial,

Pseudioninae?; Sagami Bay, Japan (Miyake, 1978).

A. laevis (Bell, 1845): Pseudione hyndmanni (Bate and

Westwood, 1868), Pseudioninae; English Channel; Spain

(Bourdon, 1968). Athelges paguri (Rathke, 1843), Athelginae.

Britain (Naylor, 1963).

Aniculus aniculus (Herbst, 1791): Parathelges aniculi

(Whitelegge, 1897), Athelginae; Eunafuti Atoll (Whitelegge,

1897).

Catapagurodes fragilis (Melin, 1939): unidentified

abdominal, Athelginae?; Sagami Bay, Japan (Miyake, 1978).

Iridopagurus caribbensis (A. Milne Edwards, 1893):

Stegophryxus hyptius Thompson, 1902, Athelginae; Western

Elorida, USA (Garcia-Gomez, 1983).

I. iris (A. Milne Edwards, 1880): Pseudionella sp.,

Pseudioninae; Venezuela (Markham, 1978).

1. margaritensis Garcia-Gomez, 1983: Parathelges occiden-

talis Markham, 1972, Athelginae; Venezuela (Markham, 1972).

Stegophryxus hyptius Thompson, 1902, Athelginae; Curasao

(Garcia-Gomez, 1983).

7. occidentalis (Eaxon, 1893): unidentified; Cocos Island,

Costa Rica (Garcia-Gomez, 1983).

Iridopagurus sp,: Asymmetrione desultor Markham, 1975,

Pseudioninae; Belize (Markham, 1988).

Lophopagurus (Lophopagurus) lacertosus (Henderson,

1888): unidentified branchial, Pseudioninae?; New Zealand

(Eorest et al., 2000). Unidentified abdominal, Athelginae?;

New Zealand (Eorest et al., 2000).

L. (L.) lacertosus (Henderson, 1888)?: Pseudione hynd-

manni (Bate and Westwood, 1868), Pseudioninae; New

Zealand (Page, 1985). Athelges lacertosi Pike, 1961,

Athelginae; New Zealand (Page, 1985).

L. (L.) thompsoni (Eilhol, 1885)?: Athelges lacertosi Pike,

1961, Athelginae; New Zealand (Pike, 1961).

L. (Australeremus) cooki (Eilhol, 1883): Athelges lacertosi

Pike, 1961, Athelginae; New Zealand (Page, 1985).

L. (A.) triserratus (Ortmann, 1892): Pseudione intermedia

Nierstrasz and Brender a Brandis, 1932, Pseudioninae; Sagami

and Misaki, Japan (McLaughlin and Gunn, 1992).

Manucornplanus ungulatus (Studer, 1863): Parathelges

occidentalis Markham, 1972, Athelginae; North Carolina, USA

(Markham, 1972).

Pagurus aleuticus (Benedict, 1892): Pseudione giardi

Caiman, 1898, Pseudioninae; Alaska and Washington, USA

(Markham, 1975).

P annulipes (Stimpson, 1860): Pseudionella markhami

(Adkison and Heard, 1978), Pseudioninae; North Carolina and

J.C. Markham

Georgia, USA (Adkison and Heard, 1978). Stegophryxus

hyptius Thompson, 1902, Athelginae; North Carolina, USA;

Gulf of Mexico (Markham, 1974).

P. arenisaxatilis Harvey and McLaughlin, 1991:

Stegophryxus sp., Athelginae; Gulf of California,

Mexico; Pacific coast, Costa Rica (Harvey and McLaughlin,

1991).

P. armatus (Dana, 1851): Pseudione giardi Caiman, 1898,

Pseudioninae; Washington, USA (Nyblade, 1974).

P beringanus (Benedict, 1892): Pseudione giardi Caiman,

1898, Pseudioninae; Washington, USA (Markham, 1975).

Athelges paguri (Rathke, 1843), Athelginae; Norway to

Belgium; Britain (Sars, 1898; Perez, 1934).

P. brevidactylus (Stimpson, 1859): Asymmetrione de suitor

Markham, 1975, Pseudioninae; Caribbean coast, Colombia

(Markham, 1988). Pseudionella markhami (Adkison and

Heard, 1978), Pseudioninae; Caribbean coast, Colombia

(Markham, 1988). Parathelges foliatus Markham, 1972,

Athelginae; Barbados; Cura 9 ao (Markham, 1978). Parathelges

piriformis Markham, 1972, Athelginae; Bermuda (Markham,

1978) . Stegophryxus hyptius Thompson, 1902, Athelginae;

Florida, USA (Markham, 1978).

P. capillatus (Benedict, 1892): Pseudione giardi Caiman,

1898, Pseudioninae; Washington, USA (Nyblade, 1974).

P. criniticornis (Dana, 1852): Pseudionella deflexa

Bourdon, 1979, Pseudioninae; Southern Brazil (Bourdon,

1979) .

P. cuanensis (Bell, 1845): Athelges bilobus Sars, 1898,

Athelginae; Denmark; English Channel (Bourdon, 1967).

Athelges cladophorus Gerstaecker, 1862, Athelginae; British

Isles (Bonnier, 1900). Athelges paguri (Rathke, 1843),

Athelginae; France (Hesse, 1876).

P dubius (Ortmann, 1892): Athelges takanoshimensis Ishii,

1914, Athelginae; Korea (Kim and Kwon, 1988). Parathelges

enoshimensis Shiino, 1950, Athelginae; Korea (Kim and Kwon,

1988).

P hirsutiusculus Dana, 1851: Pseudione giardi Caiman,

1898, Pseudioninae; Alaska and Washington, USA (Markham,

1975).

P. japonicus (Stimpson, 1859): Athelges takanoshimensis

Ishii, 1914, Athelginae; Seto, Japan (Shiino, 1958).

P. kulkanii Sankoli, 1962: Parathelges neotenuicaudis

(Shyamasundari et ah, 1993), Athelginae; Eastern India

(Shyamasundari et al., 1993); Karachi, Pakistan (Markham and

Kazmi, 1998).

P lanuginosus De Haan, 1849 (s. 1.): Athelges takano-

shimensis Ishii, 1914, Athelginae; Tokyo Bay, Japan (Shiino,

1958).

P. longicarpus Say, 1817: Asymmetrione Markham,

1975, Pseudioninae; North Carolina, USA (Markham, 1975).

Stegophryxus hyptius Thompson, 1902, Athelginae;

Massachusetts to Georgia, USA (Markham, 1974).

P maclaughlinae Garcia-Gomez, 1982: Stegophryxus hyp-

tius Thompson, 1902, Athelginae; Florida, USA (Markham,

1988).

P. maculosus Komai and Imafuku, 1996: Athelges

takanoshimensis Ishii, 1914, Athelginae; Honshu, Japan

(Nagasawa et al., 1996).

P. megalops (Stimpson, 1858): unidentified; Sagami Bay,

Japan (Miyake, 1978).

P. middendorffi Brandt, 1851: Pseudione hyndmanni (Bate

and Westwood, 1868)?, Pseudioninae; Hokkaido, Japan

(Shiino, 1958). Athelges takanoshimensis Ishii, 1914,

Athelginae; Eastern Russia; Japan; Korea (Kim and Kwon,

1988).

P ochotensis Brandt, 1851: Pseudione giardi Caiman, 1898,

Pseudioninae; Alaska, USA (Markham, 1975).

P pectinatus (Stimpson, 1858): Athelges takanoshimensis

Ishii, 1914, Athelginae; Japan; Korea (Kim and Kwon, 1988).

P prideauxii Leach, 1815: Pseudione hyndmanni (Bate and

Westwood, 1868)7, Pseudioninae; Scotland (Henderson, 1886).

Athelges prideauxii Giard and Bonnier, 1890, Athelginae;

Scotland; France; Italy (Pike, 1953). Athelges sp., Athelginae;

Norway (Samuelson, 1970).

P provenzanoi Forest and de Saint Laurent, 1967:

Asymmetrione de suitor Markham, 1975, Pseudioninae;

Antigua; Bonaire; Cura 9 ao (Markham, 1978). Parathelges

piriformis Markham, 1972, Athelginae; Bahamas (Markham,

1978). Stegophryxus hyptius Thompson, 1902, Athelginae;

Cura 9 ao (Markham, 1978).

P pubescens (Krpyer, 1838): Pseudione hyndmanni (Bate

and Westwood, 1868), Pseudioninae; Norway; Iceland; Faeroe

Islands; Britain (Bourdon, 1968).

P. stimpsoni (A. Milne Edwards and Bouvier, 1893):

Asymmetrione Markham, 1975, Pseudioninae; Florida,

USA (Markham, 1975). Pseudionella markhami (Adkison and

Heard, 1978), Pseudioninae; Caribbean coast, Colombia

(Markham, 1988). Stegophryxus hyptius Thompson, 1902,

Athelginae; Florida, USA (Markham, 1974).

P brachiomastus (Thallwitz, 1892): Athelges takanoshi-

mensis Ishii, 1914, Athelginae; Korea (Kim and Kwon, 1988).

P venturensis Coffin, 1957: Pseudione sp., Pseudioninae;

California, USA (Miller, 1975).

P vetaultae Harvey and McLaughlin, 1991: Stegophryxus

sp., Athelginae; Pacific coast, Costa Rica (Harvey and

McLaughlin, 1991).

Pagurus sp.: Pseudione intermedia Nierstrasz and Brender

a Brandis, 1932, Pseudioninae; Misaki, Japan (Shiino, 1972).

Pagurus sp.: Pseudionella attenuata Shiino, 1949,

Pseudioninae; Seto, Japan (Shiino, 1949).

Pagurus sp.: Anathelges resupinatus (Muller, 1871),

Athelginae; Florianopolis, Brazil (Muller, 1871).

Pagurus sp.: Parathelges enoshimensis Shiino, 1950,

Athelginae; Enoshima, Japan (Shiino, 1950).

Pagurus sp.: Stegophryxus thompsoni Nierstrasz and

Brender a Brandis, 1931, Athelginae; Valparaiso, Chile

(Nierstrasz and Brender a Brandis, 1931).

Pagurus sp.: Parathelges whiteleggei Nierstrasz and

Brender a Brandis, 1931, Athelginae; Java Sea (Nierstrasz and

Brender a Brandis, 1931).

Parapagurodes constans (Stimpson, 1858): Athelges

takanoshimensis Ishii, 1914, Athelginae; Tokyo Bay, Japan

(Shiino, 1958).

P laurentae McLaughlin and Haig, 1973: Stegophryxus

hyphalus Markham, 1974, Athelginae; California, USA; Baja

California, Mexico (Markham, 1974).

Hermit crabs and their relatives, hosts of Isopoda Bopyridae

P. makarovi Mclaughlin and Haig, 1973: Stegophryxus

hyphalus Markham, 1974, Athelginae; California, USA; Baja

California, Mexico (Markham, 1974).

Propagurus haigae (McLaughlin, 1997): Unidentified

branchial, Pseudioninae?; New Caledonia (McLaughlin and de

Saint Laurent, 1998).

Pylopagurus ungulatus (Studer, 1883): Parathelges occi-

dentalis Markham, 1972, Athelginae; North Carolina, USA

(Markham, 1972).

Tomopagums cokeri (Hay, 1917): Athelginae, unidentified;

Quintana Roo, Mexico (Markham, 1978).

Pagurid, unidentified: Anathelges mossambica Barnard,

1956, Athelginae; Mozambique (Barnard, 1956).

Pagurid, unidentified: Stegophryxus minutus Markham,

1992, Athelginae; Hong Kong (Markham, 1992).

Family Parapaguridae

Oncopagurus bicristatus (A. Milne Edwards, 1880):

Pleurocyptella paguri Bourdon, 1979?, Pseudioninae; Azores

(Bourdon, 1981).

O. monstrosus (Alcock, 1905): Bopyrophryxus branchiab-

dominalis Codreanu, 1965, Bopyrophryxinae; Kei Islands,

Indonesia (Codreanu, 1965).

Parapagurus pilosimanus Smith, 1879: Pleurocyptella

paguri Bourdon, 1979, Pseudioninae; Azores (Bourdon, 1979).

Parapagurus sp.: Parapagurion imbricata Markham, 1978,

Pseudioninae; Caribbean coast, Colombia (Markham, 1978).

Pylochelidae

No records known.

Discussion

It is difficult to infer many generalisations about the occurrence

of the parasites considered, because they do not fit into dis-

cernible patterns. Of the species of the Pseudioninae known to

infest paguroids, most belong to genera not known from hosts

outside of that superfamily. The exceptions are the nine species

of Pseudione, among whose other species (totalling more

than 50) are parasites of many other anomurans, numerous

thalassinideans and some deep-water carideans; and

Pleurocryptella paguri Bourdon, known from one or two

species of Parapagurus, whose congeneric species are all par-

asites of galatheids. Despite their markedly different appear-

ance from other paguroids, the lithodids bear parasites closely

related to those of hosts in other paguroid families; all of their

branchial parasites are assignable to Pseudione {P. giardi

Caiman being reported as a parasite of both a lithodid and sev-

eral species of hermit crabs); and the single lithodid-infesting

abdominal bopyrid, Pseudostegias hapalogasteri Shiino, is in a

genus whose other species infest hermit crabs. Most genera of

parasites containing more than single species infest both dio-

genids and pagurids, but all seven species of the pseudionine

genus Bopyrissa infest only diogenids, while all four species of

the athelgine genus Stegophryxus infest only pagurids. The

most widespread species is Pseudione hyndmanni (Bate and

Westwood), reported from six host species of pagurids in

western Europe (Bourdon, 1968), another in New Zealand

(Page, 1985), and possibly one in Japan (Shiino, 1958). It

seems to be an analogue of the closely similar Pseudione

giardi Caiman, which infests five species of Pagurus and the

lithodid Dermaturus mandtii in northwestern North America

(Markham, 1975; Nyblade, 1974). Among abdominal parasites,

Athelges spp. infest many different pagurids in Europe (Sars,

1898; Bourdon, 1967), while A. takanoishimensis Ishii infests

ten species of pagurids in the western Pacific (Kim and Kwon,

1988; Nagasawa et al., 1996; Shiino, 1958).

Acknowledgments

I am deeply indebted to Patsy McLaughlin for patiently and

thoroughly reading the list of paguroid names, remedying my

errors and omissions and providing the currently accepted

names of the species. Rafael Lemaitre and Christopher Boyko

furnished elusive nomenclatorial information, while Rafael

Lemaitre and Chris Tudge provided necessary editorial assis-

tance. Anonymous reviewers made valuable suggestions for the

improvement of the manuscript.

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Memoirs of Museum Victoria 60(1): 79-85 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

Geographic and depth distributional patterns of western Atlantic Porcellanidae

(Crustacea: Decapoda: Anomura), with an updated list of species

Bernd Werding', Alexandra Hiller', and Raeael Lemaitre-

'Institut fiir Tierokologie und Spezielle Zoologie der Justus-Liebig-Universitat Giessen, Heinrich-Buff-Ring 29

(Tierhaus), D-35392 Giessen, Germany (Bernd.Werding@allzool.bio.uni-giessen.de, Alexandra.Hiller-Galvis@allzo-

ol.bio.uni-giessen.de)

"Department of Systematic Biology, National Museum of Natural History, Smithsonian Institution, Washington, DC

20560-7012, USA (lemaitre.rafael@nmnh.si.edu)

Abstract Werding, B., Hiller, A., and Lemaitre, R. 2003. Geographic and distributional patterns of western Atlantic Porcellanidae

(Crustacea; Decapoda: Anomura), with an updated list of species. In: Lemaitre, R., and Tudge, C.C. (eds). Biology of the

Anomura. Proceedings of a symposium at the Fifth International Crustacean Congress, Melbourne, Australia, 9-13 July

2001. Memoirs of Museum Victoria 60(1): 79-85.

Information on horizontal and vertical distributions of all known western Atlantic species of Porcellanidae is sum-

marised, and an updated list of the 48 currently valid species is presented. The distributions and zoogeographic affinities

of the group are discussed. In the western Atlantic, the Caribbean- West Indies region is the richest in number of species

with 43, of which 40 species occur in the southern Caribbean. Species numbers decrease towards the peripheral regions

of Florida, with 17 species, and Brazil, with 19 species (including two endemics). The Caribbean- West Indies porcellanid

fauna shares 17 species with tropical Florida and 17 with tropical Brazil. There is a clear similarity in species composi-

tion between the tropical faunas of Florida and Brazil, sharing 1 1 species. Based on depth ranges, the species can be

divided into “intertidal” (range < 7 m) and “sublittoral” (range > 7 m) species. A relationship was observed between depth

distributions and geographic ranges of western Atlantic porcellanids: “sublittoraT species have wide geographic ranges,

presumably as result of greater dispersal potential and ability to colonise a variety of ecological habitats; “intertidal”

species have narrow geographic ranges, presumably as result of lower dispersal ability and narrow ecological require-

ments. For western Atlantic porcellanids, the Amazon River delta and the Florida Current are dispersal barriers more

effective for “intertidal” than for “sublittoral” species.

Keywords Cmstacea, Anomura, Porcellanidae, western Atlantic, biogeography, distribution patterns, dispersal patterns

Introduction

Since Haig’s (1956) compilation of the Porcellanidae from the

western North Atlantic, a good deal of taxonomic work has

been done on this family in the western Atlantic, particularly in

Panama and other parts of the Caribbean (e.g. Gore, 1970,

1974, 1982; Gore and Abele, 1973, 1976; Werding, 1977, 1982,

1983, 1984, 1992, 1996; Scelzo, 1982; Hernandez et al., 1999;

Lemaitre and Campos, 2000; Werding et al., 2001; Werding and

Hiller, 2001, Werding and Hiller, in press; Werding and Kraus,

in press), the south-western Gulf of Mexico (e.g. Rickner,

1975), and Brazil (Veloso and Melo, 1993). Some areas, how-

ever, remain incompletely explored such as the Caribbean coast

of Central America north of Panama, parts of the Greater

Antilles and the Bahamas, and the Guy anas in north-eastern

South America. Nevertheless, the relatively detailed records

that already exist of porcellanids from the western Atlantic

allow a reasonable assessment of their horizontal and vertical

distributional patterns as well as zoogeographic affinities.

According to a list of valid species by Werding (1992) and

updated herein, the total number of species for the entire west-

ern Atlantic is 48, although it is recognised that there are two

widely distributed and morphologically highly variable taxa,

Petrolisthes armatus (Gibbes, 1850) and P. galathinus (Bose,

1902), believed to represent complexes of species. The western

Atlantic porcellanid fauna is third in the world in richness after

the Indo- West-Pacific, with some 110 species, and the eastern

Pacific, with about 90 species. The region with the least

number of species is the eastern Atlantic with only 15 species

known so far. The porcellanid fauna of the western Atlantic has

the strongest affinity with that of the eastern Pacific, sharing ten

genera, whereas only five genera are shared with each of the

eastern Atlantic, and Indo-West Pacific regions. The eastern

Atlantic has eight genera in common with the Indo-West

Pacific. The biogeography of the porcellanid fauna from the

Pacific coast of the Americas was discussed by Carvacho

(1980); however, that of the Atlantic porcellanids has never

B. Werding, A. Hiller and R. Lemaitre

been discussed on a comprehensive basis. In this study, the geo-

graphic and depth distributions, zoogeographic affinities, and

possible ecological factors that affect species dispersal of these

anomuran crabs across the entire western Atlantic are discussed

for the first time.

Distributional patterns and zoogeographic affinities

Geographic patterns. Based on the relatively detailed distribu-

tional records now available of porcellanids from the western

Atlantic (see Table 1), the fauna of these crabs from this part of

the world can be characterised as a homogeneous assemblage

with a concentration of species in the southern Caribbean (40

species), and decreasing in number of species towards periph-

eral areas to the north (Florida) and south (Brazil). The porcel-

lanid fauna of the Antilles, Bahamas and Bermuda, an area that

comprises the tropical West Indian Province of Briggs (1974),

is distinguished from that of the southern Caribbean by a lower

species number (34 species). The almost complete lack of

strictly temperate species in the western Atlantic implies that

the family is represented in the northern Gulf of Mexico, and

on the eastern coast of the United States by eurythermal, tropi-

cal species that can range northward to those northern regions.

The only strictly warm temperate species found north of the

tropical western Atlantic is Euceramus praelongus Stimpson,

1860, known from the north-eastern coast of the United States

(Delaware Bay) to the northern Gulf of Mexico (Texas). South

of the tropical western Atlantic, in tropical Brazil and temper-

ate South America, the situation is somewhat similar. With the

exception of Pachycheles greeleyi (Rathbun, 1900) from

Brazil, all tropical species found there are also present in the

southern Caribbean. Two species, Pachycheles chubutensis

Boschi, 1963, and P laevidactylus Ortmann, 1892, are temper-

ate in distribution in South America, although the latter does

extend far into the tropics of Brazil (Boschi, 1963; Harvey and

De Santo, 1996). A very particular case is P. robsonae Glassell,

1945, an eastern Pacific species that has been found in the

vicinity of the Atlantic opening of the Panama Canal (Haig,

1960; Gore and Abele, 1976) where it has migrated repeatedly

without becoming successfully established in the Caribbean.

The overwhelming majority of western Atlantic porcellanid

species (43 out of 48) has a Caribbean- West Indian distribution

(Fig. 1). The exceptional species richness of the southern

Caribbean is accentuated by the presence of at least three

endemic species: Neopisosoma orientale Werding, 1986,

known from Trinidad, Petrolisthes gertrudae Werding, 1996,

known from Guadeloupe and Bonaire, and P. cristobalensis

Gore, 1970, known from a limited area around the Panama

Canal. Quite possibly three other species recently discovered in

the Colombian Caribbean might also represent endemics, two

from Islas del Rosario, Petrolisthes sanmartini Werding and

Hiller, in press, and P. sp. ( being named by Werding and Kraus,

in press), and Porcellana lillyae Lemaitre and Campos, 2000,

from the Gulf of Morrosquillo. Other species such as

Pachycheles chacei Haig, 1956, P. susanae Gore and Abele,

1973, and probably Petrolisthes magdalenensis Werding, 1978,

are restricted to limited areas of the South American Atlantic

continental coast and adjacent islands. Pachycheles greeleyi,

from Brazil, represents the only tropical endemic that occurs to

the south of the Caribbean- West Indian region. Pachycheles

laevidactylus does reach the tropics of Brazil, but its main

distribution is on the temperate Atlantic coast of South America.

Patterns in number of species. A decrease in number of species

can be observed from the Caribbean towards the north and

south (Fig. 1). From a total of 43 species known from the

Caribbean- West Indian region, 40 are present in the southern

Caribbean and 34 in the Antilles. Only 17 species occur in trop-

ical Florida, and 19 in tropical Brazil. All 17 Florida species are

found also in the Caribbean- West Indian region. A similar situ-

ation can be observed in the Brazilian fauna where 17 of the 19

species that occur there are also found in the Caribbean- West-

Indian region; only two are restricted in distribution,

Pachycheles greeleyi, and P. laevidactylus, ranging from Brazil

to Argentina. There is a noticeable similarity in species com-

position between the faunas of Florida and tropical Brazil, with

11 species in common. Only six of the 17 species that occur in

Florida are not represented in tropical Brazil, and six of the

Brazilian species that range into the Caribbean- West-Indian

fauna are not present in Florida.

Patterns in depth and relative geographic ranges. A summaiy

is presented (Table 2 ) of the depth (intertidal vs sublittoral)

and relative geographic distributions of all tropical species

from Florida, the Caribbean- West Indies, and Brazil, based on

a critical review of the literature, and additional data (Werding,

1992; pers. obs.). Two strictly temperate species, Euceramus

praelongus and Pachycheles chubutensis, and the eastern

Pacific immigrant, Petrolisthes robsonae, are excluded as they

are not part of the tropical western Atlantic porcellanid fauna.

The study of the geographic and depth distributions of por-

cellanids (Table 2) from the three regions shows that 22 species

(20 in the Caribbean- West Indies, and 2 in Brazil) have a

“limited” geographic range restricted to only one of the

regions, whereas 23 species have a “wide” geographic range

and are present in two or all three of the regions. Twenty-five

species can be considered “intertidal”, although some can be

found down to 7 m in depth. Of those, 2 1 species are “limited”

in range to either the Caribbean (19 species) or Brazil (2

species). Twenty species are found below 7 m in depth and are

“sublittoral”; of these, all but Porcellana lillyae have a “wide”

geographic range.

A comparison of the distributions of “intertidal” and “sub-

littoral” species from the three regions studied (Table 2, Fig. 2)

shows that 14 or 70% of the “sublittoral” species of the

Caribbean- West-Indian fauna occur in tropical Florida where

they make up 82.4% of that fauna. Sixteen species or 80% from

the Caribbean- West Indian fauna are shared with the Brazilian

fauna where they make up 84.2% of that fauna. When the

“intertidal” species are considered, only three species or 13%

of the Caribbean- West Indian fauna occur in Florida, represent-

ing 17.6% of that fauna. Just one “intertidal” species or 4.3% of

the Caribbean- West Indian fauna has been found in Brazil,

making up only 5.3% of that fauna. Altogether, 11 or 55% of

the Caribbean- West Indian “sublittoral” species are common to

both Florida and Brazil, whereas no “intertidal” species are

common to both of these peripheral regions.

Distributional patterns of western Atlantic Porcellanidae

Table 1. List of currently valid species of porcellanids from the western Atlantic, and their geographic distributions. (Petrolisthes sp. is an

undescribed species being named by Werding and Kraus, in press).

Species

Clastotoechus Haig, 1960

C. nodosus (Streets, 1872)

•

C. vanderhorsti (Schmitt, 1924)

•

Euceramus Stimpson, 1860

E. praelongus Stimpson, 1860

•

Megalobrachium Stimpson, 1858

M. mortenseni Haig, 1962

•

M. poeyi (Guerin, 1855)

•

M. roseum (Rathbun, 1900)

•

M. soriatum (Say, 1818)

•

Minyocerus Stimpson, 1858

M. angustus (Dana, 1852)

•

Neopisosoma (Haig, 1960)

N. angustifrons (Benedict, 1901)

•

N. curacaoense (Schmitt, 1924)

•

N. neglectum Werding, 1986

•

N. orientate Werding, 1986

•

Pachycheles Stimpson, 1858

P. ackleianus A. Milne- Edwards, 1880

•

P. chacei Haig, 1956

•

P chubutensis Boschi, 1963

•

P cristobalensis Gore, 1970

•

P greeleyi (Rathbun, 1900)

•

P. laevidactylus (Ortmann, 1892)

•

P. monilifer (Dana, 1852)

•

P. pilosus (H. Milne Edwards, 1837)

•

P riisei (Stimpson, 1859)

•

P. rugimanus A. Milne- Edwards, 1880

•

P. serratus (Benedict, 1901)

•

P. susanae Gore and Abele, 1973

•

Parapetrolisthes Haig, 1962

P tortugensis (Glassell, 1945)

•

Petrolisthes Stimpson, 1858

P amoenus (Guerin, 1855)

•

P armatus (Gibbes, 1850)

•

P. caribensis^trdimg, 1983

•

P. columbiensis^tr(^Lmg, 1983

•

P. dissimulate Gore, 1983

•

P. galathinus (Bose, 1802)

•

P. gertrudae Werding, 1996

•

P jugosus (Streets, 1872)

•

P magdalenensis Werding, 1978

•

P. marginatus Stimpson, 1859

•

P. politus (Gray, 1831)

•

P. quadratus Benedict, 1901

•

P robsonae Glassell, 1945

•

P. rosariensis Werding, 1978

•

P. sanmartini Werding and Hiller, in press

•

P. sp.

•

P. tonsorius Haig, 1960

•

P. tridentatus Stimpson, 1859

•

Pisidia Leach, 1820

P brasiliensis Haig, 1968

•

Polyonyx Stimpson, 1858

P. gibbesi Haig, 1956

•

• ?

•

Force liana Lamarck, 1801

P lillyae Lemaitre and Campos, 2000

•

P. sayana (Leach, 1820)

•

P. sigsbeiana A. Milne- Edwards, 1880

•

Total number of species

1. temperate North America; 2. northern Gulf of Mexico; 3. tropical Florida; 4. Bahamas; 5. Greater Antilles; 6. Lesser Antilles; 7. south-west-

ern Gulf of Mexico to Costa Rica; 8. Panama; 9. Colombia; 10. Venezuela; 11. Guyanas; 12. Tropical Brazil; 13. temperate Brazil.

B. Werding, A. Hiller and R. Lemaitre

Table 2. List of porcellanid species from the tropical western Atlantic with their general and relative geographic distributions, and arranged

according to depth range. Abbreviations: Eu, eulittoral; C-WI, Caribbean- West Indies.

Species

Depth

(m)

Geographic range

Elorida 1

C-WI 2

Brazil 3

Wide

Limited

Depth range

Sublittoral Intertidal

(> 7 m) (> 7 m)

Clastotoechus nodosus

•

Neopisosoma curacaoense

•

Neopisosoma neglectum

•

Neopisosoma orientate

•

Petrolisthes quadratus

•

Petrolisthes tonsorius

•

Petrolisthes tridentatus

•

Neopisosoma angustifrons

Eu<l

•

Pachycheles cristobalensis

•

Petrolisthes marginatus

2,3

•

Clastotoechus vanderhorsti

Eu<3

•

Pachycheles susanae

•

Petrolisthes magdalenensis

•

Petrolisthes politus

1,2

•

Petrolisthes sp.

•

Pachycheles chacei

•

Petrolisthes sanmartini

•

Pachycheles greeleyi

•

Pachycheles laevidactylus

•

Pachycheles serratus

•

Petrolisthes columbiensis

•

Petrolisthes dissimulatus

•

Petrolisthes gertrudae

•

Petrolisthes jugosus

Eu<6

1,2

•

Pachycheles pilosus

Eu<7

1,2

•

Pachycheles riisei

<10

1,2,3

•

Megalobrachium roseum

<14

2,3

•

Petrolisthes caribensis

<22

1,2

•

Petrolisthes rosariensis

<24

2,3

•

Megalobrachium mortenseni

<30

2,3

•

Petrolisthes armatus

<30

1,2,3

•

Pisidia brasiliensis

<31

2,3

•

Pachycheles monilifer

<33

1,2,3

•

Petrolisthes amoenus

<37

1,2,3

•

Parapetrolisthes tortugensis

<40

1,2

•

Megalobrachium poeyi

<46

1,2

•

Polyonyx gibbesi

<47

1,2,3

•

Petrolisthes galathinus

<54

1,2,3

•

Minyocerus angustus

<59

2,3

•

Pachycheles ackleianus

<81

1,2,3

•

Porcellana sayana

<92

1,2,3

•

Porcellana lillyae

<100

•

Megalobrachium soriatum

<111

1,2,3

•

Pachycheles rugimanus

<145

1,2,3

•

Porcellana sigsbeiana

<393

1,2,3

•

Discussion

Origins of porcellanid fauna and general factors affecting dis-

tributions. The modern porcellanid fauna of tropical America

(Table 1), like other faunas from this area, is derived from the

tertiary Caribbean Province which included the tropical eastern

Pacific until the closure of the Central American land bridge at

the end of Pliocene (Woodring, 1974). The speciation events

that took place after the final closure of the Panamanian isth-

mus approximately 3 million years ago (Ekman, 1953; Briggs,

1974; Marshall et ah, 1979), combined with the southward dis-

placement during the Pleistocene of tropical species from

northern regions such as Florida, can be used to explain the

concentration of porcellanid species seen in the modern

Caribbean- West Indies and the southern Caribbean faunas.

After displacement, most tropical species became extinct in

Distributional patterns of western Atlantic Porcellanidae

Figure 1 . Comparison of the tropical porcellanid faunas from different

regions of the western Atlantic. Large, simple circles indicate total

number of species in Florida and Brazil regions; small, simple circles

indicate species shared by regions; double circle indicates species in

Caribbean- West Indian region; rectangle indicates species in southern

Caribbean; oval indicates species in the Antilles.

Figure 2. Comparison of intertidal and sublittoral porcellanid faunas of

the Caribbean- West-Indies (rectangle) and peripheral (ovals) regions

of tropical Florida and Brazil. Italics indicate intertidal (left) and

sublittoral (right) species; numbers on dashed lines, and near solid

lines connecting rectangle and ovals, are species in common between

faunas.

Florida, and recolonisation aided by ocean currents likely

occurred when climatic conditions became favourable again.

The colonisation success of porcellanids can be attributed

primarily to dispersal and ecological potentials of the species.

Species with broad ecological potentials and capable of com-

peting with species already established in the region being

colonised, can be expected to be more successful in conquering

new areas than those species with narrow habitat requirements,

and that seems to apply to the western Atlantic porcellanids.

That ecological characteristics of species can affect their distri-

butions has been documented for other marine organisms such

as fishes and molluscs: fish species living on rocky shores are

generally less widely distributed than those living on soft bot-

toms (Rosenblatt, 1963); intertidal gastropods are generally

less well dispersed, and have more endemic species than deep-

er living gastropods (Vermeij, 1972); molluscs inhabiting rocky

surfaces, in some cases, tend to have more endemics than

those inhabiting neighbouring boulders (Vermeij and Porter,

1971); shallow-water infaunal bivalves living in depths of 1 m

or less have wider geographical distributions than those in

deeper waters because the former tolerate a wider range of

environmental conditions than the latter (Jackson, 1974).

Among crustaceans, stomatopod species living in shallow-

water or having a broad depth range, tend to occupy a wider

geographical area than those limited to greater depths (Reaka,

1980).

Dispersal factors. There is a remarkable similarity in species

composition between the porcellanid faunas of tropical Florida

and Brazil. Species that have become successfully established

on distant, peripheral regions, and thus have wide distribution-

al ranges, also have greater abilities to cross barriers and over-

come suboptimal ecological conditions. The crab stages of por-

cellanids are incapable of long-range migrations, and thus any

significant dispersal is primarily confined to the larvae. The lar-

val development of porcellanids undergoes two zoeal stages

which take no more than two weeks under tropical conditions,

followed by a megalopa stage that settles quickly, and alto-

gether lasts on average a maximum of about three weeks (see

Gore, 1972; Warding and Muller, 1990; Hernandez, 1999).

Since dispersal ability of larvae can be considered similar in

most species, their dispersal success will largely depend on the

ability of adults to adapt to varying ecological conditions.

B. Werding, A. Hiller and R. Lemaitre

During this study it has been observed that in western Atlantic

porcellanids, the extent of depth distribution often is indicative

of ecological requirements. Many western Atlantic porcellanids

(e.g. species of Clastotoechus, Neopisosoma, and Petwlisthes

quadratus) are restricted to the intertidal where they live in nar-

rowly defined habitats on hard substrates of the upper littoral

(Werding, 1977, 1978). Such habitats are often isolated and

separated by large distances of soft-bottom structures. Another,

more ubiquitous assemblage of species has wider ranges of

depth distribution, and are found in a variety of substrates and

habitats. Among the deeper sublittoral species, only the

presumably commensal species Porcellana sigsbeiana

A. Milne Edwards, 1880, P. lillyae and Pachycheles rugimanus

A. Milne Edwards, 1880, do not fit this pattern since they

depend on the depth range of their host (Werding, 1983).

Geographic and depth ranges. The depth distributions of

western Atlantic porcellanids show a clear relationship with

geographic range (see Table 2). The majority of species found

at greater depths are geographically the most widespread, and

can be found in the peripheral regions (Elorida, Brazil). As pre-

viously mentioned, the ability to live in a broad depth range

provides additional possibilities for settling in a wide range of

habitats. After the planktonic life of the zoeae, the megalopae

need to find a suitable substrate or risk perishing. Thus, the

probability of success increases proportionally to the variety of

habitats acceptable to a given species. Some “intertidal”

Caribbean species, like Neopisosoma angustifrons (Benedict,

1901), N. neglectum Werding, 1986 and Clastotoechus nodosus

(Streets, 1872), must find a highly structured intertidal fouling

community or otherwise they will not survive (Werding, 1978).

Coastal areas with such characteristics are normally scattered,

and separated by large distances of sandy beaches. Even islands

with large, rich reef structures such as the Colombian Islas del

Rosario (off mainland Colombia) or Isla Providencia (on the

western Caribbean), do not provide adequate habitats for such

ecologically naiTOw species (Werding, 1982, 1984). In contrast,

for “sublittoral”, wide-ranging species like those of the genus

Megalobrachium Stimpson, 1858, the alternatives are by far

more numerous since they are able to settle in boulder habitats,

dead coral, hard substrates on seagrass meadows, or sponge

communities in deeper waters.

Barrier effects. Two major barriers are usually considered in

zoogeographic discussions of the western Atlantic fauna. To the

south, the mouth of the Amazon River, and to the north, the

Elorida Current. The coastline between the mouths of the rivers

Orinoco and Amazon, with numerous additional freshwater

effluents in the Guyana region, covers a length of about 2,700

km. In regard to this southern barrier, an interesting case

relevant to porcellanids is that reported for fishes by Collette

and Riitzler (1977). These authors documented a rich reef

fish fauna associated with a diverse West-Indian sponge

fauna below the massive freshwater influence of the Amazon

River, in salinities ranging from 34.5 to 36.4%o, and depths of

48 to 73 m. They concluded that this river system functions as

a barrier primarily for the dispersal of shallow-water reef

organisms. Such conclusion is applicable as well to porcel-

lanids, and is supported by the distributions of species; only

one intertidal species, Petrolisthes marginatus, and sixteen

sublittoral species, occur on both sides of this barrier.

The Elorida Current is considered a distributional barrier

between the Antilles and Elorida (Briggs, 1974), and is of a

completely different nature, although its effectiveness as an

obstacle for the dispersal of decapod crustaceans has some-

times been questioned (e.g. Lemaitre, 1984). In the Straits of

Elorida, the distance between Cuba and southern Elorida reach-

es only a maximum of some 200 km, and the Elorida Current

does seem to impede the easy passage of some planktonic

larvae between the Greater Antilles and southern Elorida.

However, the crossing of larvae of many species is facilitated

by the existence of numerous small islands and shoals border-

ing the margins of the Straits that serve as stepping stones for

colonisation, and increase the successful establishment of pop-

ulations. The data show that the Florida Current is a selective

barrier for the intertidal species since only three of them

{Petrolisthes politus, P. jugosus and Pachycheles pilosus) are

present on both sides of that barrier whereas 14 sublittoral

species fulfil that condition.

Concluding remarks. The distributional and ecological factors

mentioned in this study do provide at least one explanation of

the origins and patterns of relative richness and composition of

porcellanids in the regions of Florida, Caribbean- West Indies,

and Brazil. However, it is clear that much more information is

needed on western Atlantic porcellanids in order to fully under-

stand historical tracks of dispersal that have lead to the modern

fauna of these crabs. It would be critical, for example, to con-

duct studies on phylogenetic biogeography and systematics of

western Atlantic porcellanids using molecular evidence, such

as the one now available for species of Petrolisthes and Pachy-

cheles in the eastern Pacific (Stillman and Reeb, 2001). Further

data on the geological and geophysical history of these regions,

and ecology and ontogeny of the species, will also allow a

clearer evaluation of any correspondence between distribution-

al and ecological patterns in Porcellanidae from these regions.

Acknowledgements

Financial support for this study was provided by the German

DAAD, and the Colombian INVEMAR-COLCIENCIAS

project (code No. 210509-10401), and INVEMAR-FONADE

administrative agreement (code No. 001065). We thank

Christopher C. Tudge, Michael Tiirkay, Alan W. Harvey, and an

anonymous reviewer, for useful comments on the manuscript.

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Arabian Sea

Feroz a. Siddiqui and Quddusi B. Kazmi

Marine Reference Collection and Resource Center, University of Karachi, Karachi-75270, Pakistan

(qbkazmi @ mrcrc .ku.edu .pk)

Abstract Siddiqui, F.A., and Kazmi, Q.B. 2003. A checklist of marine anomurans (Cmstacea; Decapoda) of Pakistan, northern

Arabian Sea. In: Lemaitre, R., and Tudge, C.C. (eds). Biology of the Anomura. Proceedings of a symposium at the Fifth

International Cmstacean Congress, Melbourne, Australia, 9-13 July 2001. Memoirs of Museum Victoria 60(1): 87-89.

A checklist of marine Anomura from Pakistan is presented. A review of the literature showed that the anomuran fauna

comprises 45 species representing 16 genera and six families arranged in three superfamilies. The family Diogenidae is

best represented, with 23 species in five genera; the families Coenobitidae and Paguridae each have a single genus with

three species in the former, and two species in the latter; the family Porcellanidae has 15 species in seven genera; where-

as the families Albuneidae and Hippidae are each represented with one species. The list contains information on habitat

and geographical distribution.

Keywords Cmstacea, Anomura, Pakistan, checklist

Introduction

The potential for exploitation of biological resources of the

northern Arabian Sea and Pakistan coastal waters has been

recently recognised (Thompson and Tirmizi, 1995). The

resources of this region are subjected to considerable human

pressure. The invertebrate fauna is poorly known and hence the

human effects on the fauna are difficult to assess. Although

there have been a few attempts to investigate and document the

diversity of anomurans (Mustaquim, 1972; Tirmizi and

Siddiqui, 1981, 1982; Tirmizi et al., 1982, 1989) there is urgent

need to update this information. The checklist of the Crustacea

Decapoda and Stomatopoda (Tirmizi and Kazmi, 1983) now

needs revision in light of additions and changes to species of

Diogenes (McLaughlin and Holthuis, 2001).

The present paper is a checklist of the anomurans from

intertidal or subtidal regions of the Pakistan coast. Families are

listed according to the classification of Martin and Davis

(2001) with genera and species alphabetical within each

family. The list is based on information provided by scientists

working in Pakistan and from literature. Each record is fol-

lowed by information on habitat and geographical distribution,

and its first report in the literature. * denotes a new record from

the region.

Checklist

Superfamily Galatheoidea Samouelle, 1819

Porcellanidae Haworth, 1825

Ancylocheles Haig, 1978

Ancylocheles gravelei (Sankolli, 1963). Pakistan; west coast

of India; Gulf of Mannar; Australia. Under stones, in small

pools to a depth of about 16 m (Tirmizi et al., 1982).

Enosteoides Johnson, 1970

Enosteoides ornatus (Stimpson, 1858). Pakistan; Korea;

China; Hong Kong; Vietnam; Gulf of Thailand; Singapore;

Japan; Australia. Under stones (Tirmizi et al., 1982).

Pachycheles Stimpson, 1852

Pachycheles natalensis (Krauss, 1843). Western Indian

Ocean; Pakistan; Africa; Oman. In rock crevices near low water

mark. (Mustaquim, 1972).

Pachycheles tomentosus Henderson, 1893. Western Indian

Ocean; Pakistan; western India; southern India; South Africa;

Madagascar; Red Sea; Gulf of Aden; Persian Gulf. In holes and

crevices of rocks near low water mark (Mustaquim, 1972).

Petrolisthes Stimpson, 1858

Petrolisthes boscii (Audouin, 1826). Indo-West Pacific;

Pakistan; Taiwan; Hong Kong; Gulf of Thailand; Japan;

Australia; Oman; Red Sea; Persian Gulf. In rocky pools under

stones, and in sand near low water mark (Mustaquim, 1972).

Petrolisthes lamarckii (Leach, 1820). Indo-west Pacific;

Pakistan. Under large stones (Mustaquim, 1972).

Petrolisthes leptocheles (Heller, 1861). Pakistan; India;

FerozA. Siddiqui and Quddusi B. Kazmi

Somalia; Red Sea; Gulf of Aden; Oman; Persian Gulf. Under

stones (Mustaquim, 1972).

Petrolisthes ornatus Paulson, 1875. Pakistan; Gulf of

Kutch; India; Sri Lanka; Comoro Island; Madagascar;

Mozambique; Zanzibar; Red Sea; Gulf of Aden; Gulf of Oman;

Persian Gulf. Under stones (Mustaquim, 1972).

Petrolisthes rufescens (Heller, 1861). Pakistan; Indo-west

Pacific; Pakistan; Gulf of Kutch; eastern Africa; Nicobar

Island; Madagascar; Comoros; Somalia; Red Sea; Gulf of

Aden; Persian Gulf. Under stones (Mustaquim, 1972).

Pisidia Leach, 1820

Pisidia dehaanii (Krauss, 1843). Pakistan; India; Bay of

Bengal; South Africa; Oman; Persian Gulf. Under stones from

small pools (Mustaquim, 1972).

Pisidia delagoae (Barnard, 1955). Pakistan; South Africa;

Oman. Under stones in small pools (Tirmizi et ah, 1982).

Pisidia gordoni (Johnson, 1970). Pakistan; India; Australia;

South Africa; Red Sea; Gulf of Aden; Persian Gulf. Sublittoral,

occasionally found in littoral zone under stones (Tirmizi et ah,

1989).

Polyonyx Stimpson, 1858

Polyonyx hendersoni Southwell, 1909. Pakistan; western

India; Sri Lanka; Japan; Korea; Hong Kong; Western Australia

and Queensland, Australia. Under stones (Tirmizi et ah, 1982).

Polyonyx loimicola Sankolli, 1965. Pakistan; and India.

Buried under mud (Tirmizi et el., 1989).

Raphidopus Stimpson, 1858

Raphidopus ciliatus Stimpson, 1858. Pakistan; Korea;

Formosa Strait; China; Hong Kong; Gulf of Thailand;

Singapore; Japan; Australia; Malay Peninsula. Muddy bottom

(Tirmizi and Ghani, 1994).

Superfamily Hippoidea Latreille, 1825

Albuneidae Stimpson, 1858

Albunea Fabricius, 1793

Albunea steinitzi Holthuis, 1958. Pakistan; Philippines;

Western Australia; Red Sea: Gulf of Aden. In littoral sand

(Tirmizi, 1978).

Hippidae Latreille, 1825.

Emerita Scopoli, Mil

Emerita holthuisi Sankolli, 1965. Pakistan; India. In littoral

sand (Tirmizi, 1977).

Superfamily Paguroidea Latreille, 1802

Coenobitidae Dana, 1851

Coenobita Latreille, 1826

Coenobita perlatus H. Milne Edwards, 1837. Pakistan;

Samoa; Mauritius. Semi-terrestrial, in sandy shore (Ahmed and

Khan, 1971).

Coenobita rugosus H. Milne Edwards, 1837. Pakistan; Bay

of Bengal; west coast of America. Semi-terrestrial, in rocky and

sandy shores (Ahmed and Khan, 1971).

Coenobita scaevola (EorskM, 1775). Northern Arabian Sea;

Pakistan; Red Sea; Gulf of Aden; Oman. Semi-terrestrial, more

abundant above sandy shores and tidal zone (Tirmizi and

Siddiqui, 1981).

Diogenidae Ortmann, 1892

Calcinus Dana, 1851

'^Calcinus elegans H. Milne Edwards, 1837. Pakistan;

Hawaiian Island to East Africa. Rocky shore (Siddiqui, pers.

obs.).

Calcinus latens (Randall, 1840). Indo-Pacific region;

Pakistan; Maldives; Australia; Hawaiian Islands; eastern

Africa; Red Sea; Gulf of Aden; Oman. Rocky shore (Tirmizi

and Siddiqui, 1981).

Clibanarius Dana, 1852

Clibanarius aequabilis Dana 1852. Pakistan; Sri Lanka;

Mergui; Malay Peninsula; Tahiti; western Africa. Muddy and

sandy shores (Ahmed and Khan, 1971). This record appears to

be in error.

Clibanarius arethusa De Man, 1888. Pakistan; Bay of

Bengal. Rocky shore (Ahmed and Khan, 1971).

Clibanarius clibanarius (Herbst, 1791). Pakistan;

Andamans to Tahiti. Muddy and sandy beaches (Tirmizi and

Siddiqui, 1981).

Clibanarius infraspinatus Hilgendorf, 1869. Indo-Pacific;

northern Arabian Sea; Pakistan; Bay of Bengal; Malay

Archipelago; eastern Australia; Red Sea. Muddy and sandy

beaches (Ahmed and Khan, 1971).

Clibanarius padavensis De Man, 1888. Indo-Pacific;

Pakistan to Singapore; East Indies; Australia; New Caledonia.

Muddy and sandy shores (Ahmed and Khan, 1971).

Clibanarius signatus Heller, 1861. Northern Arabian

Sea; Pakistan; Oman; Red Sea. Common on rocky and sandy

shores, rare on muddy shore (Tirmizi and Siddiqui, 1981).

Clibanarius striolatus Dana, 1852. Karachi, Pakistan; Gulf

of Aden; Seychelles and eastward to Tahiti; Australia. Rocky

and muddy shores (Alcock, 1905).

Clibanarius virescens (Krauss, 1843). Pakistan; Australia;

Japan; Philippine and Eiji Islands; Hong Kong; eastern Africa;

Red Sea; Gulf of Aden; Oman; Persian Gulf. Rocky shore

(Tirmizi and Siddiqui, 1981).

Dardanus Paulson, 1857

Dardanus setifer (H. Milne Edwards, 1836). Pakistan and

eastward to Hong Kong; Australia; southern and eastern Africa.

Offshore (Tirmizi and Siddiqui, 1981).

Dardanus vulnerans (Thalwitz, 1892). Pakistan; New

Guinea; Bay of Bengal; Persian Gulf. Offshore (Tirmizi and

Siddiqui, 1981).

Diogenes Dana, 1852

"^Diogenes alias McLaughlin and Holthuis, 2001. Pakistan;

eastern Indian Peninsula; Borneo; South China Sea. Offshore

on muddy bottom. Tirmizi and Siddiqui’s (1981) report of D.

diogenes (Herbst, 1791) from Pakistan is actually D. alias

(McLaughlin and Holthuis, 2001).

Diogenes avarus Heller, 1865. Northern Arabian Sea;

Pakistan; Vietnam; Philippine Islands; Indonesia; Thailand;

northern and western Australia; eastern Africa; Red Sea. Rocky

shore (Tirmizi and Siddiqui 1981).

Checklist of marine anomurans of Pakistan

Diogenes bicristimanus Alcock, 1905. Pakistan; India;

South Africa; South Arabia. Rocky shore (Tirmizi and Siddiqui

1982).

Diogenes costatus Henderson, 1888. Northern Arabian Sea;

Pakistan; south-eastern India; Red Sea (Ahmed and Khan,

1971).

Diogenes custos (Fabricius, 1798). Indo-Pasific; Pakistan;

Madras; eastern Australia. Rocky shore. Tirmizi and Siddiqui’s

(1981) report of Diogenes? affinis, and Henderson’s (1893)

D. planimanus and D. violaceus are actually D. custos

(McLaughlin and Holthuis, 2001).

"^Diogenes dubius (Herbst, 1804). Pakistan; Indian Seas;

Bay of Bengal; south-eastern Australia. Muddy shore. Reported

from Pakistan (Tirmizi and Siddiqui, 1981) as D. custos

(Fabricius, 1798) (McLaughlin and Holthuis, 2001).

Diogenes sp. Northern Arabian Sea; Pakistan. Rocky shores.

Reported from Pakistan (Tirmizi and Siddiqui, 1981) as D. gut-

tatus Henderson, 1888, but could possibly be D. granulimanus

Miers, 1880, or an undescribed species (P. McLaughlin, in litt.).

^Diogenes ?fasciatus Rahayu and Forest, 1995. Pakistan;

and Indonesia. In creek area. Identification tentative

(P. McLaughlin, in litt.).

^Diogenes ?karwarensis Nayak and Neelkantan, 1989.

Pakistan; and India. In creek area. Identification tentative

(P. McLaughlin, in litt.).

*Diogenes ?klaasi Rahayu and Forest 1995. Pakistan;

Indonesia. In creek area. Identification tentative

(P. McLaughlin, in litt.).

^Diogenes ?manaarensis (Henderson, 1893). Pakistan;

Mergui; Philippine; Australia; eastern Africa; Red Sea. Rocky

and sandy shore. Reported from Pakistan (Tirmizi and

Siddiqui, 1981) as D. jousseaumei (Bouvier, 1897), may be

D. ?manaarensis (Henderson 1893) (P. McLaughlin, in litt.).

Paguristes DdiUdi, 1851

Paguristes perspicax Nobili, 1906. Pakistan; Red Sea;

Persian Gulf. Rocky shores (Tirmizi and Siddiqui, 1981).

Paguridae Latreille, 1802

Pagurus Fabricius, 1775

Pagurus kulkarnii Sankolli, 1962. Pakistan; India;

Thailand. Rocky shores (Tirmizi and Siddiqui, 1981).

Pagurus sp. Pakistan. Offshore (Tirmizi and Siddiqui,

1981).

Acknowledgements

The first author is grateful to Patsy A. McLaughlin, Shannon

Point Marine Centre, Western Washington University,

Washington, U.SA, for taking interest in the pagurids of

Pakistan, and help in determination the status of several

species. The initial work on this checklist was done by the

second author as a part of a project funded by the Faculty

Grants, University of Karachi. She is grateful to Rafael

Lemaitre, National Museum of Natural History Smithsonian

Institution, Washington, DC, USA, and Chris Tudge, American

University, Washington, DC, USA, for the invitation to

contribute to this volume.

References

Ahmed, J., and Khan, M.D. 1971. "Pagurids" in the collection of

Zoological Survey Department. Records of the Zoological Survey of

Pakistan 2(2); 11-16.

Alcock, A. 1905. Anomura. Fasc. 1. Pagurids. Catalogue of the Indian

decapod Crustacea in Collection of the Indian Museum 2; i-xi,

1-197, pis 1-16 Indian Museum: Calcutta.

Martin, J. W and Davis, G.E. 2001. An updated classification of the

Recent Crustacea. Natural History Museum of Los Angeles County,

Science Series 39: 1-124.

McLaughlin. PA., and Holthuis, L.B. 2001. In pursuit of J.F.W.

Herbsf s, species of Diogenes (Anomura: Paguridea: Diogenidae).

Journal of Crustacean Biology 21(1); 249-265.

Mustaquim, J. 1972. Species of porcellanid crabs from Karachi.

Pakistan Journal of Zoology 4(2); 153-159, figs 1-7.

Thompson, M.F., and Tirmizi, N.M. (eds). The Arabian Sea. Living

marine resources and the environment. Vanguard Books (Pvt.) Ltd:

Pakistan. 732 pp.

Tirmizi, N.M. 1977. On Ernerita holthuisi Sankolli, 1965 from

Pakistan (Decapoda, Hippidae). Crustaceana 32(1): 108-109, figs

1-7.

Tirmizi, N.M. 1978. On the presence of Albunea steinitzi Holthuis in

the northern Arabian Sea (Decapoda, Hippidea). Crustaceana

35(1): 94-95, figs 1-8.

Tirmizi, N.M., and Ghani, N. 1994. An Indian Ocean record for a por-

cellanid crab Raphidopus ciliatus Stimpson, 1858. Pakistan

Journal of Marine Sciences 3(1): 69-72, fig. 1.

Tirmizi, N.M., and Kazmi, Q.B. 1983. Carcinological studies in

Pakistan, with remarks on species of the Red Sea and the

Mediterranean. In: Marine Sciences in the Red Sea. Bulletin of the

Institute of Oceanography and Fisheries 9: 347-380. Published in

cooperation with AIBS.

Tirmizi, N.M., and Siddiqui, F.A. 1981. An illustrated key to the iden-

tification of northern Arabian Sea pagurids. Institute of Marine

Biology, Centre of Excellence, University of Karachi, Pakistan.

Publication 1: 1-31, figs 1-25.

Tirmizi, N.M., and Siddiqui, F.A. 1982. The marine fauna of Pakistan:

I. Hermit crabs (Crustacea, Anomura). University Grants

Commission, Sector H-9: Islamabad. 108 pp., 45 figs.

Tirmizi, N.M., Yaqoob, M., and Siddiqui, F.A. 1982. An illustrated key

to the identification of anomurans (Porcellanidae, Albuneidae and

Hippidae of the northern Arabian Sea). Institute of Marine Biology,

Centre of Excellence, University of Karachi, Pakistan, Publication.

2: 1-29, figs 1-11.

Tirmizi, N.M., Yaqoob, M., and Siddiqui, F.A. 1989. Marine fauna of

Pakistan: 3. Porcellanid crabs (Cmstacea, Anomura). Centre of

Excellence in Marine Biology, University of Karachi, Pakistan,

Publication 6: 1-46.

Memoirs of Museum Victoria 60(1): 91-97 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

Calcinus hermit crabs from Easter Island, with biogeographic considerations

(Crustacea: Anomura: Diogenidae)

Joseph Poupin', Christopher B. Boyko^ and Guillermo L. Guzman^

'Institut de Recherche de I'Ecole navale, IRENav, Ecole navale, Lanveoc-Poulmic, BP 600, 29240 Brest Naval, Prance

(poupin @ ecole-navale.fr)

^Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York,

NY 10024, USA (cboyko@amnh.org)

^Museo del Mar Universidad Arturo Prat, Casilla 121, Iquique, Chile (gguzman@cec.unap. cl)

Abstract Poupin, J., Boyko, C.B., and Guzman, G.L. 2003. Calcinus hermit crabs from Easter Island, with biogeographic consid-

erations (Crustacea: Anomura; Diogenidae). In; Lemaitre, R., and Tudge, C.C. (eds). Biology of the Anomura.

Proceedings of a symposium at the Pifth International Cmstacean Congress, Melbourne, Australia, 9-13 July 2001.

Memoirs of Museum Victoria 60(1): 91-97.

Prom collections made in 1998 and 1999, three species of Calcinus are recorded from Easter I.: Calcinus pascuensis

Haig, 1974; C. imperialis Whitelegge, 1901; and C. vachoni Porest, 1958. A redescription of Calcinus pascuensis is

given and a neotype is selected. Occurrence of Calcinus imperialis is confirmed by examination of almost 80 specimens,

including many juveniles. Calcinus vachoni is recorded for the first time from the island. The Easter I. Calcinus fauna

is compared with that of other localities in the Pacific, and biogeographic affinities are discussed.

Keywords Cmstacea, Anomura, Diogenidae, Calcinus, biogeography, Easter Island

Introduction

Easter Island (27°10'S, 109°20'W), located 3800 km off the

Chilean coast, and separated by 2200 km from Pitcairn I. to the

west, is the most isolated island in the South Pacific. The coast

line is rocky with only a few sandy and cobble beaches. Its cli-

mate is subtropical; the surface sea temperature range is

22-24°C in the summer, and 16-18°C in the winter. Although

the water is cool, there are extensive amounts of living coral

around the island but diversity of coral species is low. Because

of its isolated position and high percentages of endemic taxa,

and despite a surface area of only 106 km^ Easter L, in con-

junction with nearby small Sala y Gomez L, 415 km to the east,

is usually treated as a distinct biogeographic province in the

Pacific (Briggs, 1974).

The Anomura known from the island consist so far of only

seven species: Calcinus pascuensis Haig, 1974, Pylopagur-

opsis garciai McLaughlin and Haig, 1989, Petrolisthes

extremus Kjopp and Haig, 1994, Albuneidae sp. and Calcinus

imperialis Whitelegge, 1901 (DiSalvo et ah, 1988),

Phylladiorhynchus integrirostris (Dana, 1853) (Baba, 1991),

and Tylaspis anomala Henderson, 1885 (Lemaitre, 1998). In

1998 and 1999 new intertidal and shallow water collections of

hermit crabs were made during the Chilean CIMAR-5 cruise

and the American United States National Park Service

Expedition to the island. More than a hundred specimens of the

genus Calcinus were obtained, with only three species repre-

sented: C. pascuensis Haig, 1974, C. imperialis Whitelegge,

1901, and C. vachoni Eorest, 1958. Although low in diversity,

these new collections are of interest for at least two reasons.

Eirst, they allow a redescription of C. pascuensis, previously

known from only a single incomplete male. Second, they can

be used to discuss the biogeographic affinities of Easter I. with

neighbouring localities in the Indo-Pacific region.

Materials and methods. Most of the specimens were collected

between 16 Aug and 1 Sep 1999, during the United States

National Park Service Expedition to Easter Island. The collec-

tors were Christopher B. Boyko, John Tanacredi (United

States National Park Service, Gateway), Rick and Susan

Reanier, Ellen Marsh, Dennis Hubbard (Oberlin College,

Ohio), and Henry Tonnemacher (Seven Seas, Ltd., Virgin

Islands). A few additional specimens were collected during a

1998 Expedition (19-24 Aug). The aim of both expeditions was

primarily archaeological. Most hermit crabs were collected

intertidally by hand, and a few by SCUBA in depths down to

23 m. Other specimens were collected by Guillermo Guzman,

during the oceanographic CIMAR-5 Chilean cruise, on board

the AGOR Vidal Gormaz from 29 Oct to 15 Nov 1999. The

Calcinus were collected by hand in the Easter I. locality of

Hanga Roa and its adjacent shores. An additional specimen,

collected at Easter I. in March 1984 and deposited in the

J. Poupin, C.B. Boyko and G.L. Guzman

collections of the Museo Zoologico Universidad de

Concepcion, Chile, was obtained through the courtesy of Dr J.

N. Artigas.

The measurement (mm), shield length, taken from tip of

rostrum to posterior edge of the shield, is included for all

specimens. Abbreviations are: AMNH, American Museum of

Natural History, New York; MNHN, Museum national

d’Histoire naturelle, Paris; MZUC, Museo Zoologico

Universidad de Concepcion, Chile; P2, P3, second and third

pereopods.

Calcinus pascuensis Haig, 1974

Figure 1

Calcinus pascuensis Haig, 1974: 27, figs 1-6 (type locality: Easter

I.). — Retamal, 1981: 19. — DiSalvo et al., 1988: 458. — Poupin and

McLaughlin, 1998; 24.

Material examined. Neotype (herein selected). Easter I., off Hanga

Otea, 26 Aug 1999, 21 m, D. Hubbard, 1 male 5.3 mm (AMNH

18177).

Other specimens (all from Easter I.). Off Ana O Keke, Poike, 1 male

4.0 mm (AMNH 18178), 1 female 3.9 mm (MNHN Pg 5948). Oroi

Point, 1 female 1.5 mm (AMNH 18179). Hanga Tee O Vaihu, 1 male

1.8 mm (AMNH 18180). La Perouse Bay, 2 males 1.9-2. 1 mm, 1

female 1.7 mm (AMNH 18181). Piko, 3 males 1. 7-2.0 mm, 2 females

1.3- 1. 7 mm (AMNH 18182). Te Pito Kura, 1 male 3.0 mm, 3 females

1. 4- 2.2 mm (AMNH 18183). Piko, 1 male 3.6 mm (AMNH 18184).

Hanga Roa, 1 male 2.6 mm, 1 female 2.4 mm (MNHN Pg 6092).

Diagnosis. Ocular acicle with a single terminal spine. Chelipeds,

P2 and P3 with long and distally plumose setae, typically with

club-like aspect. Outer face of left palm regularly convex.

Upper margin of right palm with 4 or 5 strong corneous-tipped

spines. Dactyls of P2 and P3 equal to or slightly shorter than

propodi; distal degree of setation similar for both pereopods,

without distal brush of setae on P3. Telson with 2-16 (usually

10) spines on lateral and posterior margins of left posterior

lobe, and 2-7 (usually 6) spines on right posterior lobe.

Redescription. Shield 0.8 as broad as long; anterior margin between

rostrum and lateral projections slightly concave; anterolateral margin

setose; anterolateral plate of branchiostegite aimed by row of spinules

on dorsal margin. Rostrum broad, obtusely triangular, largely exceed-

ing small lateral projections. Ocular acicle subtriangular, terminated by

single acute spine. Ocular peduncle 0.8- 1.0 as long as shield, left

slightly longer than right; diameter of cornea included 5-7 times in

peduncular length (Pig. la).

Antennular peduncle extending to distal 0.25 of ocular peduncle;

basal segment usually with 3 spinules at ventrolateral distal angle;

penultimate segment unarmed; ultimate segment unarmed, equal to

O. 33 of shield length. Antennal peduncle reaching to distal 0.33 of ocu-

lar peduncle, furnished with long and distally plumose setae. Pirst seg-

ment minutely spinose at ventrolateral distal angle. Second segment

with dorsolateral distal angle produced, terminating in strong bifid

spine; dorsomesial surface inflated, produced as strong spine. Third

segment with ventrodistal spine. Pourth segment with distodorsal

spine. Pifth segment long and unarmed. Antennal flagellum over-

reaching distal end of P2. Antennal acicle surpassing distal end of

penultimate segment of antennal peduncle, produced as strong spine,

upwardly curved; dorsolateral margin with 2 spines; dorsomesial

mai'gin with 2-3 spines.

Left cheliped larger than right (Pig. lb). Merus subtriangular in

cross-section; outer and inner surfaces flat; outer lower margin usually

with single spine at distal angle; inner lower margin with 2 or 3 distal

spines. Caipus broad, much shorter than meras. Outer face with proini-

nent submedian tubercle, occasionally with few additional smaller

tubercles; distolateral margin with small granules or tubercles, spine-

tipped in juveniles. Upper margin with single terminal spine and, in

smaller specimens, few additional posterior spines. Inner and lower

faces smooth. Chela 0.9-1. 6 as long as shield and 1. 4-2.0 as long

as width. Outer face of palm regularly convex, slightly tuberculate;

upper margin with row of 6-8 spiny tubercles; outer lower margin

rounded, smooth or slightly tuberculate. Inner face rounded, with

tuft of setae below articulation of dactyl; inner lower margin some-

what angular with row of faint granules, prolonged by sharp row of

tubercules on inner face of fixed finger. Pingers spooned at tips. Dactyl

0.6 time as long as entire chela, with tufts of long setae on lower

margin; cutting edge with 2 or 3 large calcareous teeth on proximal

0.5. Pixed finger forming large hiatus with dactyl; cutting edge with

large calcareous tooth on distal 0.5, and 1 or 2 smaller teeth on

proximal 0.5.

Right cheliped shorter than left, reaching to base of fingers of left

chela, or little beyond, when extended (Pig. Ic). Meras compressed;

upper margin sharp with few long setae; outer and inner lower margins

each with 2 or 3 distal spines. Carpus much shorter than meras; outer

face with median tubercle and 1 or 2 additional smaller ones; distal

margin with several corneous-tipped tubercles, somewhat eroded in

larger specimens, those proximate to upper and lower margins larger

than others; upper margin with 3 strong spines, the distalmost one

largest. Outer face of chela with distally plumose setae and several

tubercles in distal upper half; upper margin with 5 strong

corneous-tipped spines. Pingers spooned at tips. Dactyl 0.5 as long as

whole chela; upper margin with a double row of 4 or 5 small corneous-

tipped spines; cutting edge with two median calcareous teeth. Pixed

finger with outer face tuberculate; cutting edge forming small hiatus

with dactyl, armed with 2-4 triangular teeth.

P2 noticeably exceeding cheliped (Pig. Id). Meras as long as propo-

dus; lateral and mesial faces compressed; dorsal and ventral margins

with long, distally plumose setae; ventral margin with row of some-

what spiny granules; distolateral angle armed with single spine. Carpus

0.6 as long as propodus; lateral face inflated, mesial face flattened;

dorsal margin with strong subdistal spine and smaller posterior spine;

ventral margin with few plumose setae. Propodus feebly curved, sub-

ovate in cross-section, slightly shorter than shield length, with several

tufts of long, distally plumose setae. Dactyl strongly curved, about 0.9

as long as propodus, terminating in strong corneous claw; ventral

margin with few long simple setae, amied with 6-9 acute spines.

P3 slightly overreaching tip of cheliped (Pig. le). Merus about

as long as propodus; lateral face smoothly curved; mesial face

slightly concave; dorsal and ventral margins with several tufts

of long, distally plumose setae; distolateral angle with spine. Carpus

0.7 times as long as propodus; dorsal and ventral margins with

plumose setae; dorsodistal margin with strong terminal spine, some-

times with smaller additional posterior spine. Propodus 0.8 as long as

shield length, subovate in cross-section, with tufts of long plumose

setae mainly near dorsal and ventral margins. Dactyl as long as

propodus; setation weak and similar to dactyl of P2; ventral margin

with 7-9 acute spines.

Sternite of P3 with anterior lobe subrectangular; ventral surface

swollen in 2 rounded projections, furnished with setae. Telson with left

posterior lobe considerably larger than right; lateral margin armed with

8-10 spines, posterior margin with 3-6 spines (Pig. If). Right poster-

ior lobe regularly curved, without clear separation between posterior

and lateral margins, armed with 6-8 spines.

Calcinus from Easter Island

Figure 1. Calcinus pascuensis Haig, 1974, neotype male 5.3 mm (AMNH 18177): a, anterior portion of shield and cephalic appendages; b, left

cheliped, outer view; c, right chela, outer view; d, left P2, lateral view; e, left P3, lateral view; f, telson, ventral view; g, detail of setae, from ven-

tral margin of P2. Scale bars equal 1 mm. Colour pattern after 18 months in alcohol.

Colour. After 18 months in alcohol, coloration still very clear on larg-

er specimens. Shield orange, fading to white posteriorly. Posterior

carapace white. Ocular acicle pink to orange, terminal spine white.

Ocular peduncle with basal pink ring (almost white in smaller speci-

mens), median orange area, and narrow white ring close to cornea.

Antennular peduncle with dark orange blotches on proximal segment;

median segment and proximal half of terminal segment orange; distal

half of terminal segment pale blue to white; flagella yellow. Antennal

peduncle orange on 4 proximal segments (spines white), yellow on ter-

minal segment and flagellum. Antennal acicle orange with white at tips

of spines. Cheliped with large irregular brown patches on pink to

cream-white background. Outer and inner faces of merus with brown

proximal and distal patches, separated by white median area; outer and

inner faces of carpus with median sub triangular brown patches; outer

face of chela with 2 brown median patches, a large one on the upper

half and a smaller one along ventral margin; inner face of chela with 1

median brown patch. P2 and P3 with pink background. Lateral faces of

meri, carpi and propodi with 2 orange brown stripes, forming 2 con-

tinuous lines on the 3 segments. Mesial faces with similar pattern, the

2 lines being less regular and reduced to elongated spots on meri and

carpi. Dactyls with few elongated orange brown spots. Abdomen and

telson white.

Distribution. Easter I.

Habitat. Hard bottoms, from shore to depth of 23 m. Gastropod shells

used are: Coralliophila violacea, Nerita sp., Planaxis akuana.

Strombus maculatus, and perhaps also Erosaria caputdraconis,

Fossarus cumingii, Neothais nesiotes, and Nodilittorina pyramidalis

pascua (empty shells of these molluscs were found in vials containing

loose crabs of different species).

Remarks. The holotype of Calcinus pascuensis was lost during

the transfer of the Allan Hancock Foundation collections to the

Los Angeles County Museum (G. Davis, pers. comm.). As the

original description of the species was based solely on the

incomplete holotype, a neotype has been selected herein.

A few morphological variations have been observed. In

juveniles smaller than 1.6 mm the ocular peduncles are only

0. 6-0.7 times as long as shield instead of 0. 8-1.0 in larger spec-

imens. The ocular acicle has typically a single terminal spine on

17 specimens out of 20, but a few other armaments have been

observed: 1 additional spinule, unilaterally; two terminal spines

on each acicle; and two spines on one acicle and three on the

other. The left chela presents several variations according to sex

or size. It is usually shorter in females, only 0.9-1. 1 times as

long as shield versus 1.0-1. 6 in males. The aspect of its upper

margin varies from almost smooth to armed with a row of six

to eight spines. These spines are more acute in juveniles and

also cover the upper half of the outer face of the chela. The

armament of the telson varies with size. In specimens larger

than 3.0 mm, it consists of 11-16 spines on the left posterior

J. Poupin, C.B. Boyko and G.L. Guzman

lobe and six to eight on the right posterior lobe. In smaller spec-

imens the number of spines is reduced to two to eight spines on

the left posterior lobe and two to three spines on the right pos-

terior lobe.

In armament of the ocular acicle (simple) and telson (sever-

al spines on both posterior lobes), aspect of outer face of the left

chela (regularly convex), and similar sparse pilosity on distal

P2 and P3, Calcinus pascuensis is most similar to C. incon-

spicuus Morgan, 1991. However, the two species are easily

differentiated by coloration: chelipeds, P2 and P3 in C. incon-

spicuus are almost uniformly coloured while in C. pascuensis

there are patches on the chelae and stripes on P2 and P3. They

also differ in armament of the telson, the spines of the left

posterior lobe being present only on the posterior margin in

C. inconspicuus, whereas they are on the posterior and lateral

margins in C. pascuensis.

Calcinus pascuensis is distinguishable from the other Indo-

West Pacific species by the remarkable coloration of walking

legs. A similar pattern is observed in C. anani Poupin and

McLaughlin, 1998, but the stripes on the propodi and dactyls

merge in an intricate network of reticulations. Calcinus pas-

cuensis is also unique in the setae on the outer face of the right

chela, and on the dorsal and ventral margins of P2 and P3.

These setae are distally plumose, which give them a club-like

aspect (Fig. 1 g). Although plumose setae are sometimes

observed in other species, they are not club-like shaped and are

inserted only on the disto ventral margins of P2 and P3.

Calcinus imperialis Whitelegge, 1901

Calcinus imperialis Whitelegge, 1901: 48, pi. 9 (type locality: Lord

Howe I.).— Grant and McCulloch, 1907: 154.— Chilton, 1911; 552.—

DiSalvo et al., 1988: 458.— Morgan, 1991: 882, figs 21-23.— Tudge,

1995: 11, pi. 1, fig. If. — Poupin, 1997; 697, figs 3f, 5c, 7d. — Forest et

al., 2000: 15. — Forest and McLaughlin, 2000: 79.

Not Calcinus imperialis. — Wooster, 1984: 130. — Poupin, 1996: 14

(= Calcinus isabellae Poupin, 1997).

Material examined (all from Easter I.). Hanga Poukura, 1 female 1.8

mm (AMNH 18185). Hanga Tee, 1 male 1.5 mm (AMNH 18186).

Easter I., 2 males 1.9-2.0 mm (AMNH 18187), 3 females 1.7-2.9 mm,

discoloured specimens 1 male 1.9 mm, 1 female 1.6 mm (AMNH

18188). Easter I., 1 female 2.7 mm (AMNH 18189). Tongariki, 1

female 2.1 mm (AMNH 18190). Hanga Tee O Vaihu, discoloured spec-

imens 2 males 1.3-1.7 mm (AMNH 18191). Hanga Tee O Vaihu, 6

males 1. 4-3.4 mm, 4 females 1.4-2. 2 mm, 1 juvenile 1.3 mm, dis-

coloured specimens 6 juveniles 0.9- 1.4 mm (AMNH 18192). La

Perouse Bay, 2 males 1.9-3. 8 mm, discoloured specimens 2 males

1.1-1. 4 mm, 1 female 1.0 mm, 5 juveniles 0.9-1. 0 mm (AMNH

18193). Te Pito Kura, 3 males 2.3-2.9 mm, 1 female 1.8 mm, dis-

coloured specimens 7 males 1.0-1 .7 mm, 4 females 1.2-1. 5 mm

(AMNH 18194). Anakena, 2 males 1.6-3.5 mm, 2 females 1.6-2.2 mm

(AMNH 18195). Anakena, 2 males 1.9-3. 5 mm, 2 females 1.6-3. 3

mm, discoloured specimen 1 female 1.3 mm (AMNH 18196). One

Makihi, 1 male 4.4 mm (AMNH 18197). Hanga Roa, 2 males 2.8-4.4

mm, discoloured specimens 9 males 1.3-1. 9 mm, 3 females 1.6-2. 1

mm (MNHN Pg 6093).

Diagnosis. Ocular acicle with a single terminal spine. Ocular

peduncle 0.7-1. 0 times as long as shield; diameter of cornea

included approximately 5 times in peduncular length.

Anterolateral plate of branchiostegite with fringe of long setae

on its dorsal margin (no spinules). Left chela 0. 8-1.3 times as

long as shield, comparatively larger in adult males. Outer face

of palm feebly granular, with several proximal tubercles; lower

half with 2 or 3 circular or subcircular depressions; upper mar-

gin armed with 3-5 spiny tubercles; lower margin denticulated

and carinate, carena continuing onto fixed finger (see remarks).

Carpus armed with several stout spines along anterior and

upper margins and on outer face. Right palm with 4 or 5 cor-

neous-tipped spines on upper margin; outer face tuberculate. P3

with distinct brush of setae on ventral margin of dactyl and

distal part of propodus; dactyl about 0.8 times as long as propo-

dus. Telson armed with single spine on terminal margin of each

posterior lobe.

Colour, (live coloration from Poupin, 1997). Shield and ocular pedun-

cles green olive. Antennular and antennal peduncles yellow. Chelae

green olive with purplish-blue spines and tubercles, tip of fingers

white. Dactyls of chelae with 2 red spots near base, on inside and out-

side. P2 and P3 banded in light yellow, black, and green olive.

Abdomen and telson white.

After 1 .5 y in alcohol, coloration still clear on Easter I. specimens

although slightly different from live coloration. Shield white, some-

times cream on distal half. Antennular and antennal peduncles chlorine

yellow. Palms of chelae orange to brown, fading to white distally;

tubercles and spines blue. Dactyls of chelae with 2 red spots near base,

on inside and outside. P2 and P3 banded in white, red-brown, and

orange.

Distribution. South Pacific 14-34° S. Eastern Australia to

Easter L, including Vanuatu, New Caledonia, Norfolk I.,

Kermadec Is, and French Polynesia. Not found in the Indian

Ocean or in North Pacific, and the report from these areas by

Forest and McLaughlin (2000: 79) is erroneous (J. Forest, pers.

comm.).

Habitat. This species is a non-obligate coral associate (genus

Pocillopora). On Easter I. it uses gastropod shells of Caducifer

decapitata englerti, Erosaria caputdraconis, Fossarus cumin-

gii, Neothais nesiotes, Nerita sp., Planaxis akuana, Pascula

citrica, and Nodilittorina pyramidalis pascua. Two specimens

(AMNH 18187) were parasitised by the bopyrid isopod,

Pseudionella akuaku Boyko and Williams, 2001.

Remarks. The occurrence of Calcinus imperialis in Easter L,

although already mentioned by DiSalvo et al. (1988), had been

overlooked in the taxonomic literature. These new collections

are the second record of this species on Easter I. and show that

it is very common around the island.

Examination of Calcinus imperialis specimens herein

reported, reveals intraspecific variations. Unusual armament of

the ocular acicle includes one additional small spine, on one or

both sides (13 specimens out of 79) or up to three terminal

spines, on one side (a single specimen). The distal brush of

setae on P3 is somewhat weak on a few small specimens. The

two or three circular or subcircular depressions on the outer

face of the chela are attenuated, or even totally absent, on spec-

imens smaller than 2.0 mm. The outer face of the palm is either

regularly convex or only slightly concave on its lower half. In

these cases identification can still be made by careful examin-

ation of the lower margins of the palm and fixed finger, which

are almost always carinated. In combination with the armament

Calcinus from Easter Island

of the ocular acicle and telson, this character was very useful in

identifying many juveniles lacking colour. The carina was

missing only on a 1.6 mm female (AMNH 18188) although it

was easily identified as C. imperialis by the faint remains of red

spots at the bases of the dactyls of the chelae.

Calcinus vachoni Forest, 1958

Calcinus vachoni Forest, 1958: 285, figs 2, 3, 9, 10, 15, 19 (type

locality: near NhaTrang, Vietnam). — Baba, 1982: 58. — Morgan, 1990:

11, fig. 2; 1991: 905, figs 60-62. — Gherardi and McLaughlin, 1994:

624.— Poupin, 1997: 712, figs 6e-f, 8a-f— Shih and Lee, 1997: 22,

figs 1-3.— Shih, 1998: 93, figs 33-35.— Kato and Okuno, 2001: 74.

Calcinus seurati. — Matsuzawa, 1977: pi. 79, fig. 3. — Miyake,

1983: 113.— Nomura et al., 1988: 113.— Takeda, 1994: 194, fig. 2. Not

Calcinus seurati Forest, 1951.

Not Calcinus vachoni. — ^Lewinsohn, 1982: 53 (= Calcinus guamen-

sis Wooster, 1984, see Distribution).

Material examined (all specimens from Easter L). Los Motus, in

Pocillopora coral, 1 male 3.7 mm (MZUC FI 198, 3257). Te Pito Kura,

1 male 1.2 mm (AMNH 18198). Hanga Roa, discoloured specimens 1

male 1.6 mm, 1 female 1.7 mm (MNHN Pg 6094).

Diagnosis. Ocular acicle with 2-5 terminal spines.

Anterolateral plate of branchiostegite with fringe of long setae

on dorsal margin, unarmed. Outer face of left chela regularly

convex, slightly granulate; lower margin of palm rounded;

upper margin unarmed, rounded or weakly cornered. Right

chela with 5-7 corneous spines on upper margin. Distal setation

of P3 more pronounced than on distal P2 but not forming real

brush of setae. Telson with 4-9 spines on left posterior lobe

(3-5 on posterior margin and 1^ on lateral margin) and 3-9

spines on right posterior lobe.

Colour (hve coloration from Poupin, 1997). Oculai' peduncle gray-blue

to cream with a large dark patch of variable extension: from absent to

almost covering all the peduncle. Antennular peduncle and its flagella,

blue. Distal segment of antennal peduncle orange; flagellum orange.

Cheliped almost totally gray-blue turning to white on fingers of chela.

P2 and P3 uniformly cream. In Easter I. specimens examined herein

coloration has almost totally faded.

Distribution. Widely distributed in Indo-West Pacific,

27°N-27°S. Mauritius, Western Australia, Vietnam, Taiwan,

Micronesia, Japan, French Polynesia, and Easter L. According

to Gherardi and McLaughlin (1994), the record from Somalia

(Lewinsohn, 1982) is in fact referable to Calcinus guamensis

Wooster, 1984.

Habitat. Hard bottom and facultative associate of Pocillopora

corals. It uses gastropod shells of Drupa spp., Drupella spp..

Conus spp., Mitra spp., Latirus spp., Cymatium spp.,

Coralliophila spp., and Cronia spp. (Shih and Lee, 1997: 25).

Remarks. Separation of the poorly preserved specimens herein

reported of Calcinus vachoni from discoloured juveniles of

C. imperialis, can be difficult. The characters that are most use-

ful are: armament of ocular acicle and telson, aspect of left

chela, and in the case of one specimen, faint traces of coloration

(ocular peduncle, white with cream patch distally, and distal

segment of antennular peduncle blue).

In armament of the ocular acicle and telson, general aspects

of left and right chelae, and distal setation of P3, Calcinus

vachoni is similar to Calcinus gouti Poupin, 1997, from French

Polynesia, and Calcinus laurentae Haig and McLaughlin, 1984,

from Hawaii. However, these three species are very distinctive

in their coloration (see Poupin, 1997; Hoover, 1998). The

ocular peduncle is gray-blue to cream with a large dark patch in

C. vachoni-, orange with narrow white ring close to cornea in

C. laurentae-, and proximally pink, grading to pale pink or

white distally in C. gouti. The distal antennular segment is blue

in C. vachoni-, light orange or white in C. laurentae-, and white

to cream in C. gouti. The chela is gray-blue turning to white

distally in C. vachonv, brown turning to white distally in

C. laurentae-, and white or cream with a submedian dark spot

on outer face in C. gouti. P2 and P3 are uniformly cream in

C. vachoni-, red-orange turning to pinkish distally in

C. laurentae-, and cream with pink rings in C. gouti. In addition

to coloration, Calcinus vachoni is also distinguished by the

upper margin of the left chela, unarmed and often weakly cor-

nered, whereas it has some spines and is rounded in the two

other species.

Discussion

Knowledge of the Easter Island Calcinus fauna has been

obtained as result of past expeditions to the island. Since the

first collections of Decapoda made during the 1904 Albatross

Eastern Pacific Expedition, more than ten scientific missions

have studied this fauna. The most important collections were

obtained during the 1958 Scripps Institution of Oceanography

DOWNWIND Expedition, with a rock dredge operated

between 40 and 100 m, in La Perouse Bay; the 1964-1965

Canadian British Columbia Medical Expedition to Easter

Island, with many shore collections made by Messrs Efford and

Mathias; the 1972 Expedicion de Isla de Pascua, organised by

the Institute Central de Biologfa, Universidad de Concepcion,

with intertidal collections and SCUBA dives between 8 and 10

m; and the 1985 and 1986 National Geographic Expedition,

with intensive collections from inshore to depths of 60 m, by

SCUBA dives, and also baited traps around 100 m. As no spe-

cial attention was paid to the Calcinus during these expeditions

it is possible that more species occur around the island, espe-

cially in poorly sampled subtidal areas. Nonetheless, because of

the large collection studied here, it can be stated that Calcinus

species are reasonably well known. A comparison of Easter I.

fauna with other places in the Indo-West Pacific (Table 1)

shows that: (1) the Easter I. fauna is remarkably impoverished;

(2) the island must be included in the Indo-West Pacific region;

and (3) it is a distinct province.

Easter I. has a clearly depauperate Calcinus fauna compared

to other Indo-West Pacific areas. Some species that are com-

mon and easily collected by hand in neighbouring Erench

Polynesian Islands, such as C. seurati or C. laevimanus, are

absent from Easter I. The Western Pacific has the richest fauna

(22 species. Table 1) with a decline in the number of species to

the east (18 species in Erench Polynesia, 11 species in Hawaii,

and 3 species on Easter L). This trend is similar to that observed

in shore fishes (Randall, 1998, 1999). Such low

number of species in Easter I. can be attributed to its isolation;

low surface area which reduces the chance of settlement by

J. Poupin, C.B. Boyko and G.L. Guzman

Table 1. Species of Calcinus in the western and central Pacific. Western Pacific: Japan to Australia, including Taiwan, Micronesia, and Indonesia.

French Polynesia: Marquesas, Society, Tuamotu, Austral and Gambler. Species in bold occur only in one region.

Western Pacific (Asakura, 2002; Asakura and Nomura, 2001; Asakura and Tachikawa, 2000; Morgan, 1991; Poupin, 1997; Poupin and

McLaughlin, 1998; Rahayu and Forest, 1999; Shih, 1998)

C. anani Poupin and McLaughlin, 1998; C. areolatus Rahayu and Forest, 1999; C. argus Wooster, 1984; C. elegans (H. Milne Edwards, 1836);

C. gaimardii (H. Milne Edwards, 1848); C. guamensis Wooster, 1984; C. haigae Wooster, 1984; C. irnperialis Whitelegge, 1901; C. incoii-

spicuus Morgan, 1991 (Australia); C. isabellae Poupin, 1997; C. kurozumii Asakura and Tachikawa, 2000 (Mariana); C. laevirnanus (Randall,

1840); C. latens (Randall, 1840); C. lineapropodus Morgan and Eorest, 1991; C. minutus Buitendijk, 1937; C. morgani Rahayu and Eorest, 1999;

C. pulcher Eorest, 1958; C. revi Poupin and McLaughlin, 1998; C. seurati Eorest, 1951; C. sirius Morgan, 1991 (Austtalia); C. spicatus Eorest,

1951; C. vachoni Eorest, 1958.

French Polynesia (Poupin, 1997; Poupin and McLaughlin, 1998; Raliayu and Eorest, 1999)

C. anani Poupin and McLaughlin, 1998); C. elegans (FI. Milne Edwards, 1836); C. gouti Poupin, 1997 (Tuamotu and Society); C. guamensis

Wooster, 1984; C. haigae Wooster, 1984; C. hakahau Poupin and McLaughlin, 1998 (Marquesas); C. irnperialis Whitelegge, 1901; C. isabellae

Poupin, 1997; C. laevirnanus (Randall, 1840); C. latens (Randall, 1840); C. minutus Buitendijk, 1937; C. morgani Rahayu and Eorest, 1999;

C. nitidus Heller, 1865 (Tuamotu and Society); C. orchidae Poupin, 1997 ( Marquesas); C. revi Poupin and McLaughlin, 1998; C. seurati Eorest,

1951; C. spicatus Forest, 1951; C. vachoni Eorest, 1958

Hawaii (Haig and McLaughlin, 1984; Hoover, 1998; Rahayu and Eorest, 1999)

C. argus Wooster, 1984; C. elegans (H. Milne Edwards, 1836); C. gaimardii (H. Milne Edwards, 1848)?; C. guamensis Wooster, 1984; C. haigae

Wooster, 1984; C. hadetti Haig and McLaughlin, 1984; C. laevirnanus (Randall, 1840); C. latens (Randall, 1840); C, laurentae Haig and

McLaughlin, 1984; C. morgani Rahayu and Eorest, 1999?; C. seurati Eorest, 1951

Easter I. (this study)

C. irnperialis Whitelegge, 1901; C. pascuensis Haig, 1974; C. vachoni Eorest, 1958

oceanic larvae; subtropical nature with low sea temperature and

low coral diversity; and monotonous rocky coast, offering few

ecological niches.

The affinities of Easter I. are clearly with the Indo-

West Pacific, and the island can be considered the eastern-

most outpost of this region. The three local Calcinus species do

not have affinities with any of the eastern Pacific species:

C. californiensis Bouvier, 1898, C. explorator Boone, 1930,

and C. obscurus Stimpson, 1859. The eastern Pacific species

are characterised by the upper margin of the right chela being

smooth or only slightly granulated, whereas the Easter I.

Calcinus, like almost all other Indo-West Pacific species, have

four or five strong, corneous-tipped spines on this margin. The

presence in Easter I. of C. vachoni, a species widely distributed

in the Indo-West Pacific, is futher evidence of the Indo-

West Pacific affinities of the island. Moreover, the occurrence

of C. irnperialis points to the close affinities between Easter I.

and islands that lie along the southern edge of the tropical

Pacific such as those of south of Tuamotu, Rapa I., Kermadec

I. and Norfolk L. A similar observation has been documented

for molluscs by Rehder (1980: 14, figs 6-9).

Although hardly significant for such a limited number of

species, the presence of one endemic species, Calcinus

pascuensis, out of three present on the island, represents the

highest percentage of endemicity for the regions separated in

Table 1 . This high rate of endemicity for Calcinus hermit crabs,

combined with extreme geographical isolation, supports the

view that this small island is a distinct biogeographic province

within the Indo-West Pacific region.

Acknowledgements

We are grateful to several colleagues for their help during this

work: N. Ngoc-Ho facilitated access to MNHN collections;

George E. Davis, searched for the holotype of Calcinus pas-

cuensis in the Los Angeles County Museum collection, unfor-

tunately in vain; M. Retamal and J. N. Artigas arranged for the

loan of a specimen deposited in the collections of the

Universidad de Concepcion. J. Randall and M. Tavares aided in

the bibliographic research. Eunding to Christopher Boyko for

the Invertebrate Survey of Easter I. was provided by the United

States National Park Service, Gateway National Recreation

Area, Division of Natural Resources, as part of a Science

Museum of Long Island/Explorers Club five-year research

expedition to explore the impacts of El Nino events on World

Heritage Sites.

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Memoirs of Museum Victoria 60(1): 99-104 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

Hermit crab species of the genus Clibanarius (Crustacea: Decapoda: Diogenidae)

from mangrove habitats in Papua, Indonesia, with description of a new species

Dwi Listyo Rahayu

Research Center for Oceanography, Indonesian Institute of Sciences (LIPI), Jl. Pasir Putih 1, Ancol Timur, PO. Box

4801/JKTF, Jakarta 11048, Indonesia (dwilistyo@email.com)

Abstract Rahayu, D.L. 2003. Hermit crab species of the genus Clibanarius (Cmstacea: Decapoda: Diogenidae) from mangrove

habitats in Papua, Indonesia, with description of a new species. In: Lemaitre, R., and Tudge, C.C. (eds). Biology of the

Anomura. Proceedings of a symposium at the Fifth International Crustacean Congress, Melbourne, Australia, 9-13 July

2001. Memoirs of Museum Victoria 60(1): 99-104

A new species of hermit crab, Clibanarius harisi, is described from mangrove and estuarine areas in the south coast

of Papua, Indonesia. The new species is separated from its congeners by the presence of a strong spine on the ven-

tromesial margin of the merus, and the absence of longitudinal stripes on the second and third pereopods. Clibanarius

ambonensis Rahayu and Forest, 1992 and C. antennatus Rahayu and Forest, 1992, are reported for the second time, and

a new colour variation of C. longitarsus (De Haan, 1 849) is documented.

Keywords Cmstacea, Anomura, Diogenidae, Clibanarius, new species

Introduction

Among the decapod crustaceans collected during the Biological

Monitoring Program of the Environmental Department of

Perseroan Terbatas Freeport Indonesia (PT. Freeport Indonesia)

in the south coast of Papua, Indonesia (04°40'-05°05'S,

136°35'-137°20'E), four species of hermit crabs belonging to

the genus Clibanarius were found in mangrove and estuarine

areas.

Species of Clibanarius from Indonesia are well studied

(Buitendijk, 1937; Haig and Ball, 1988; Rahayu and Forest,

1992; Rahayu, 1999), nevertheless a new species has been dis-

covered. The present paper describes Clibanarius harisi sp.

nov., live coloration of C. ambonensis Rahayu and Forest,

1992, and C. antennatus Rahayu and Forest, 1992, and records

a new colour variation in C. longitarsus De Haan, 1849.

The material is deposited in the Zoological Museum, Bogor

(MZB), and Research Center for Oceanography, Jakarta, of the

Indonesian Institute of Sciences, Indonesia (RCO); Marine and

Coastal Laboratory of Environmental Department of PT.

Freeport Indonesia in Timika, Papua, Indonesia (PTFI);

Zoological Reference Collection of the Raffles Museum,

National University of Singapore (ZRC); and Museum nation-

al d’Histoire naturelle, Paris, France (MNHN). Specimen

measurements (mm) refer to shield length, measured from

the tip of rostrum to the posterior border of shield. Colour

descriptions are of live material.

Clibanarius ambonensis Rahayu and Forest

Clibanarius ambonensis Rahayu and Forest, 1992: 753, figs 2b,

3c, d.

Material examined. Pulau Kamora, sandy mud, 20 Jun 2000, 3

females (2 ovigerous), 2. 3-2. 7 mm (RCO 0102), and 23 Jun 2000, 1

male, 1.9 mm, J. Volosin (PTFI).

Diagnosis. Shield almost as long as broad. Ocular peduncles

little shorter than shield, diameter 0.2 of peduncles; ocular

acicles with 4 or 5 denticles. Antennular peduncles reaching

slightly beyond base of cornea. Antennal peduncles not reach-

ing completely base of cornea; antennal acicles not exceeding

proximal margin of last peduncular segment. Chelipeds nearly

equal; dorsolateral faces of propodi covered with dense small

conical tubercles, dorsal margins of carpi each with single

distal acute spine. Dactyls of second and third pereopods about

the same length as propodi, 9 small spines on ventral margin.

Colour in life. Shield whitish with brown spots. Ocular pedun-

cles bluish-white, dorsal surface with narrow dark brown

longitudinal stripe; proximal part brown. Ocular acicles brown

with bluish- white spines. Antennal peduncles bluish- white with

dark brown longitudinal stripe on dorsal surface of fifth seg-

ment. Chelipeds brown with light blue spines; dactyls bluish-

white with 2 longitudinal brown stripes on dorsal surfaces.

Second and third pereopods bluish-white with brown longi-

tudinal stripes on lateral surfaces: dactyls and meri with 3

100

Dwi Listyo Rahayu

longitudinal stripes, propodi with 4 longitudinal stripes, carpi

with 2 longitudinal stripes.

Distribution. Ambon and Halmahera islands, Maluku,

Indonesia, now extended eastward to the south coast of Papua.

Remarks. The present specimens agree well with the original

description of the species by Rahayu and Forest (1992), except

for one minor difference. The dactyls of the second and third

pereopods of Papua specimens are slightly shorter than the

propodi, while Rahayu and Forest (1992) described them as

approximately the same length. Clibanarius ambonensis is

recognisable by the number of longitudinal stripes on the

ocular peduncles and second and third pereopods as described

above.

Clibanarius ambonensis resembles C. striolatus Dana,

1852. The shield of the two species is almost as long as broad;

the ocular peduncles are stout, longer than the antennal and

antennular peduncles; the dactyls of the second and third pere-

opods are approximately the same length as propodi. Live spec-

imens can be distinguished by their coloration. The general

colour of C. striolatus is yellowish green or brownish green

with large brown longitudinal stripes on the second and third

pereopods, while C. ambonensis is brownish blue or whitish

blue with nan'ower brown longitudinal stripes on the pere-

opods. In addition, C. ambonensis possesses a longitudinal

stripe on the dorsal surface of the ocular peduncles, which is

absent in C. striolatus.

Clibanarius antennatus Rahayu and Forest

Clibanarius antennatus Rahayu and Forest, 1992: 755, figs 2c,

3e,f.

Material examined. Sungai Kamora, sandy mud, 8 Jun 2000, 10 males,

3.0-3. 8 mm, 8 females (6 ovigerous), 2. 8-3.5 mm (PTFI), and 11 Jul

2001, 2 males, 3.3, 3.6 mm, 10 females (5 ovigerous), 2.7-3.42 mm,

D.L. Rahayu (RCO 0103).

Diagnosis. Shield longer than broad. Ocular peduncles stout,

shorter than shield, cornea inflated, diameter 0.3 of peduncles;

ocular acicles with 1 or 2 denticles. Antennal and antennular

peduncles reaching middle of cornea; antennal acicles short,

reaching slightly beyond middle of fourth peduncular segment.

Chelipeds subequal, right cheliped longer and broader than left;

dorsolateral faces of propodi covered with dark tipped conical

tubercles, dorsal margins of carpi each with 3 acute spines.

Dactyls of second and third pereopods notably arched, 1.5 to

1.8 longer than propodi.

Colour in life. Shield mottled light blue or bluish-white and

dark brown. Ocular peduncles bluish- white, dorsal surface with

1 thin, brown coloured, interrupted longitudinal stripe.

Antennular peduncles transparent bluish-white. Antennal

peduncles brown with white longitudinal stripe on dorsal sur-

face of fourth and fifth segments; first and second segments

dark brown; antennal acicles dark brown with white spines.

Chelipeds brown with blue spines; tips of fingers light brown

or whitish-orange. Second and third pereopods bluish-white or

light blue with brown longitudinal stripes over entire length;

meri with 2 stripes; carpi with 3 stripes; propodi with 4

stripes: 1 very naiTOw stripe on dorsal margin, 1 broader and 1

narrower median stripe with distal and proximal parts broad-

ened and 1 narrow, interrupted stripe on ventral margin; dactyls

with 2 interrupted stripes.

Distribution. Barombong, South Sulawesi, Indonesia (type

locality), now extended eastwards to south coast of Papua.

Remarks. Morphological characters and colour pattern of

Papua specimens agree well with Rahayu and Forest’s (1992)

description of Clibanarius antennatus except for the number of

longitudinal stripes on the carpi and propodi of the second and

third pereopods. Their colour description was based on materi-

al preserved in alcohol, possibly faded, leaving only two stripes

on the carpi of the pereopods (there are three stripes in the live

animal), and no interrupted stripe on the ventral margins of the

propodi (there is an interrupted stripe in the live animal).

Clibanarius longitarsus (De Haan)

Pagurus longitarsus De Haan, 1849; 211, fig. 3.

Clibanarius longitarsus. — ^Fize and Serene, 1955: 83, fig. 11, pl.3,

figs 1, 7, 10, 13.— Lee, 1969: 44.— Dechance, 1964; 31, fig. 4.—

Lewinsohn, 1969: 18. — Lewinsohn, 1982: 38. — Khan and Natarajan,

1984: 8, fig. 6.— Morgan, 1987: 172.— Haig and Ball, 1988: 163.—

Rahayu and Forest, 1992: 762, figs 4b, 5b, 6b.

Material examined. Sungai Jaramaya, mud, 12 Nov 1999, 4 males, 2.8,

7.4, 8.1, 9.3 mm ; 2 females, 3.0, 5.4 mm, and 8 Dec 1999, 4 females,

3.5, 3.9, 4.1, 6.5 mm, D.L. Rahayu (PTFI); Ajkwa, mud, 20 Jan 2000,

1 female, 5.8 mm; 21 Jun 2000, 1 male, 8.5 mm, 2 females (1 oviger-

ous), 5.0, 6.9 mm, D.L. Rahayu (MNHN); Kamora, sandy mud, 4 Apr

2000, 2 females 7.3 mm, and 8 Jun 2000, 1 female, 4.2 mm, D.L.

Rahayu (PTFI); Pulau Bidadari, sandy mud, 21 Jun 2000, 7 males, 2.8,

4.9, 5.0, 5.2, 5.6, 7.4, 9.0 mm; 6 females, 3.3, 4.2, 4.3, 4.4, 4.6, 4.7 mm,

D.L. Rahayu (RCO 0104).

Diagnosis. Shield longer than broad. Ocular peduncles approx-

imately 0.8 length of shield; ocular acicles terminating in sim-

ple or bifid spine. Antennular peduncles as long as or slightly

longer than ocular peduncles. Antennal peduncles barely reach-

ing base of cornea; antennal acicles not reaching distal margin

of fourth peduncular segment. Chelipeds subequal, right slight-

ly longer and more robust than left; dorsomesial margins of

carpi each with 1 corneous-tipped spines distally; dorsal sur-

faces of palms and dactyls with irregular rows of sometimes

corneous-tipped spines. Dactyls of second and third pereopods

about 1.5 length of propodi, ventral margin with row of

corneous spinules.

Colour in life. Shield mottled brown and blue or light brown

with several blue patches. Rostrum, lateral projections and

anterior margin between rostrum and lateral projections, white.

Ocular peduncles brownish-orange, transparent, dorsoproximal

surface with dark brown marking; corneas black; ocular acicles

brown with white spines. Antennular peduncles brown, dorsal

surface with longitudinal bluish-white stripe. Antennal pedun-

cles brown; fourth and fifth segments brown, dorsal surface

with bluish-white longitudinal stripe. First, second and t hi rd

segments brown; antennal acicles brown with white spines.

Chelipeds brown with blue or blue-green tubercles and

spines; spines with black corneous tips. Pereopods brown with

blue and orange stripes over entire length. Lateral surfaces of

A new species of Clibanarius

101

meri each with oblique orange stripe; carpi with 1 orange and 1

blue longitudinal stripe on lateral faces. Propodi with 3 longi-

tudinal stripes: 1 orange stripe bordered by fine red lines on

dorsal margin; next, blue metallic median stripe bordered by

dark brown lines; and 1 orange stripe next to ventral margin.

Dorsal margin of dactyls each with longitudinal orange stripe,

lateral face with longitudinal blue stripes bordered by dark

brown lines; ventral margin whitish-orange. Mesial surfaces of

carpi and meri brown with blue marking; mesial surfaces of

dactyls and propodi same as lateral surfaces.

Distribution. Indo-West Pacific, from Red Sea and Indian

Ocean, Malay Archipelago to Japan and Australia.

Remarks. The very common and widespread intertidal hermit

crab, C. longitarsus, is very variable in coloration (Fize and

Serene, 1955; Ball and Haig, 1972; Morgan, 1987). The Papua

specimens agree well with Fize and Serene’s (1955) description

and illustration, and Rahayu and Forest’s (1992) illustration.

Some specimens have the same coloration as described by

Morgan (1987) from Darwin and Port Essington, Australia.

However, most of the specimens reported herein have the

coloration as described above. The blue median longitud-

inal stripe on the lateral face of each pereopod, a specific

character of this species, is more intense in the specimens col-

lected in dense mangrove habitats. The orange stripes on the

pereopods and proximal brown fleck or spot on the dorsal

surface of each ocular peduncle, have never been recorded

previously.

Clibanarius harisi sp. nov.

Figure 1

Material examined. Holotype. Stn EM 334, 4°49.39'S, 136°38.10'E,

2. 7-6. 9 m, otter trawl, 14 Eeb 2000, 1 female, 6.8 mm, A. Haris (MZB

Cru 1500).

Paratypes. Stn EM 279, 04°48.15’S, 136°50.59'E, 4.S-5.7 m, otter

trawl, 7 and 14 Eeb 2000, 2 males, 10. 1 and 6.5 mm, 1 female, 8.2 mm,

A. Haris (ZRC 2002.0271); collected with holotype, 1 male 11.1 mm

(MZB Cm 1501); Pulau Kamora, intertidal, 8 Jun and 16 Oct 2000, 2

males, 2.5 and 3.2 mm, 3 females, 2.4, 4.0 and 4.1 mm, D.L. Rahayu

(RCO CaOlOl).

Other material. Stn EM 275, 04°52.67'S, 136°47.22'E, 5.4-7.2 m,

otter trawl, 17 Dec 1997, 1 male 5.1 mm, K. Hortle (PTEI); Poriri,

intertidal, 15 Eeb and 4 Aug 1999, 1 male, 6.1 mm 1 female, 11.1 mm,

A. Haris (MNHN); stn EM 430, 04°56.48'S, 137°3.19'E, 3-4 m, trawl,

16 Eeb and 17 Mar 2000, 1 male, 5.1 mm, 1 female, 2.7 mm, A. Haris

(RCO 0105); stn EM 332, 04°48.61'S, 136°39.14’E, 1.8-5 .4 m, otter

trawl, 14 Eeb 2000, 1 female, 6.2 mm, A. Haris (PTEI); stn EM 772,

04°56.84'S, 137°7.39'E, 6 m, otter trawl, 19 Mar 2000, 1 male, 6.6 mm,

A. Haris (PTEI).

Description. Shield slightly longer than broad; dorsal surface

with scattered tubercles and sparse tufts of setae, lateral mar-

gins rounded and armed with 2 or 3 teeth. Rostrum triangular,

acute, longer than lateral projections, exceeding bases of ocular

acicles. Lateral projections broadly triangular terminating in

lor 2 small teeth.

Ocular peduncles slender, inflated basally, about 0.8 length

of shield, reaching distal 0.8 of antennular peduncles. Corneas

weakly dilated, diameter approximately 0.16 length of

peduncles. Ocular acicles small, triangular, with 4 or 5

marginal spines.

Antennular peduncles slender; ultimate, penultimate and

basal segments unarmed.

Antennal peduncles reaching distal 0.8 of ocular peduncles.

First segment short with small spinule on distolateral margin;

second segment with dorsolateral distal angle produced, term-

inating in small spine; 1 spinule on distomesial margin; third

segment with ventrodistal spine; fourth segment with small

dorsodistal spine; fifth segment unarmed. All segments with

scattered setae. Antennal acicles exceeding base of fifth pedun-

cular segment, terminating in acute spine; mesial margin with 5

corneous spines.

Chelipeds subequal, right slightly larger than left, armament

similar, scarcely setose. Merus with row of crenulations along

dorsal margin; ventrolateral margin with large and pointed

tubercles, 2 strong spines distally; ventromesial margin with

row of tubercles, 1 strong pointed tooth proximally. Carpus half

length of meiois, dorsomesial margin with 3 strong spines and 2

weak tubercles; dorsal surface with scattered large and small

tubercles; mesial and ventral faces nearly smooth. Palm as long

as or slightly longer than carpus, dorsomesial margin with

longitudinal row of spines; dorsal surface with irregular, wide-

ly-spaced longitudinal rows of spines, dorsolateral face with

irregular rows of pointed tubercles, continuing onto fixed

finger; mesial face with blunt tubercles. Fixed finger

slightly broader than dactyl; cutting edge with large median

tooth followed by smaller teeth, terminating in large corneous

claw; dorsal surface covered with conical tubercles. Dactyl

slender, as long as or slightly shorter than palm; cutting

edge with large median tooth followed by smaller teeth, term-

inating in large corneous claw; dorsal surface with row of

pointed tubercles, decreasing in size distally; dorsomesial

margin with row of pointed tubercles; mesial face with row

of tubercles.

Second and third pereopods sparsely setose, moderately

long, generally similar from left to right. Second pereopods

with meri almost 1.5 times length of carpi; dorsal margins

unarmed, ventral margins each with 1 strong distal spine and

row of spinules proximally. Carpi 0.7 length of meri, dorsodis-

tal margins each with 1 strong, corneous-tipped spine and 1

weaker spine. Propodi slender, 1.4 length of carpi, 3.6 longer

than wide, unarmed, lateral faces slightly flattened. Dactyls

slightly curved, 1.3 length of propodi, terminating in small cor-

neous claws; dorsal margins each with shallow longitudinal

groove and dense and stiff tufts of setae; lateral faces each with

3 shallow longitudinal grooves: first groove 0.75 length of

dactyl; second groove wider, 0.5 length of dactyl; third groove

longer and very narrow; mesial faces each with 1 longitudinal

groove; ventral margins each with row of spinules in distal half.

Third pereopods stouter than the second; meri each with distal

spine on ventral margin; carpi 1.8 length of meri, dorsodistal

margins each with strong, corneous-tipped spine; propodi stout,

1.2 length of carpi, 2.7 longer than wide, unarmed, lateral faces

slightly flattened; dactyls 1.5 longer than propodi; grooves on

dorsal margins and lateral faces, and row of spinules on ventral

margins similar to second pereopods.

Telson with asymmetrical posterior lobes, left longer than

102

Dwi Listyo Rahayu

Figure 1. Clibanarius harisi sp. nov. Holotype, female, 6.8 mm (ZRC Cm 1500). a, shield and cephalic appendages, dorsal view; b, left cheliped,

dorsomesial view; c, left cheliped, lateral view; d, left chela, dorsal view; e, second left pereopod, lateral view; f, third left pereopod, lateral view;

g, telson, dorsal view. Scale = 2 mm. Setae omitted except on t hi rd left pereopod.

A new species of Clibanarius

103

right, separated by shallow median cleft; terminal margins each

with strong spines, smaller spines on right margin.

Colour in life. Shield yellowish-white with 2 brown spots on

dorsal surface. Ocular peduncles light olive-green with 3 longi-

tudinal brown stripes; 1 broad stripe on dorsal surface, tapering

distally, broadened proximally; lateral and mesial faces each

with 1 narrow stripe. Penultimate segments of antennular

peduncles bluish-brown, ultimate segments brown. Antennal

peduncles and antennal acicles brown. Chelipeds generally

greenish-brown; meri, carpi and palms greenish-brown with

blue spines; fixed fingers and dactyls light brown or red-brown

with bluish- white spines, claws black, Meri and carpi of second

and third pereopods dark greenish-brown; propodi and dactyls

greenish-brown. In smaller specimens, dactyls and propodi

greenish-orange.

In alcohol, chelipeds, pereopods and ocular peduncles red-

orange. Longitudinal stripes on ocular peduncles dark red.

Etymology. This species is dedicated to Mr Abdul Haris who

collected most specimens of this species.

Distribution. South coast of Papua, Indonesia; 0-7.2 m depth.

Remarks. Most species of Clibanarius that possess longitudinal

stripes on the dorsal surfaces of the ocular peduncles also have

longitudinal stripes on the second and third pereopods, such as

Clibanarius ambonensis, C. antennatus, C. bistriatus Rahayu

and Forest, 1992, C. clibanarius (Herbst, 1791), C. eurystemus

(Hilgendorf, 1878), C. fonticola McLaughlin and Murray,

1990, C. infraspinatus (Hilgendorf, 1869), C. padavensis De

Man, 1888, C. rhabdodactylus Forest, 1953, C. signatus FieWer,

1861, C. taeniatus (Milne Edwards, 1848), and C. zebra Dana,

1852. However, C. harisi possesses longitudinal stripes on the

dorsal surface of the ocular peduncles, and lacks longitudinal

stripes on the pereopods. The most similar species to C. harisi

is C. infraspinatus. Both species possess a strong spine on the

ventromesial margins of the meri of the chelipeds, and longitu-

dinal stripes on the dorsal surfaces of the ocular peduncles.

Clibanarius harisi differs from C. infraspinatus by the pres-

ence of longitudinal sulci on the lateral faces of the dactyls of

the second and third pereopods, the absence of row of spines on

the dorsal margin of the carpus of each second pereopod and

the absence of longitudinal stripes on the lateral faces of the

second and third pereopods. In addition, the shield of C. infra-

spinatus is more elongate and the spines on the propodi of the

chelipeds are stronger than in C. harisi.

The coloration preserved in alcohol is uniform red, similar

to C. clibanarius described by De Man (1888: 237) based on

specimens in the Berlin Zoological Museum. The photograph

of the type specimen of C. clibanarius from the Berlin

Zoological Museum given by Sakai (1999) has no visible lon-

gitudinal stripes on the pereopods. However, McLaughlin

(pers, comm.) examined the type specimen and confirmed the

presence of faint longitudinal lines on the ocular peduncles and

pereopods as mentioned by Alcock (1905). The presence of

faint longitudinal stripes on the pereopods, and the absence of

a strong spine on the ventromesial margin of the meri of the

chelipeds distinguish C. clibanarius from C. harisi.

Acknowledgements

I thank Dr P.A. McLaughlin for kindly providing the informa-

tion on the type specimen of Clibanarius clibanarius in the

Berlin Zoological Museum, Germany, and her comments on the

manuscript. I am grateful to Prof. J. Forest for sparing his valu-

able time to examine the specimens of C. harisi sp. nov and

commenting on the manuscript. Thorough and useful com-

ments by Drs Rafael Lemaitre and Chris Tudge and anonymous

reviewers improved this manuscript. I also thank the members

of Marine and Coastal Section of Environmental Department of

PT. Freeport Indonesia in Timika, Papua, Indonesia for assist-

ing in the collection of material.

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Leiden.

Haig, J., and Ball. E.E. 1988. Hermit crabs from north Australian and

eastern Indonesian waters (Crustacea Decapoda: Anomura:

Paguroidea) collected during the 1975 Alpha Helix Expedition.

Records of the Australian Museum 40: 151-196.

Khan, S.A., and Natarajan, R. 1984. Hermit crabs of Porto Novo coast.

Records of the Zoological Survey of India, Occasional Paper 67:

1-25.

Lee, S.C. 1969. Anomuran Crustacea of Taiwan. Part I. Diogenidae.

Bulletin of the Institute of Zoology, Academia Sinica 8: 39-57.

Lewinsohn, Ch. 1969. Die Anomuren des Roten Meeres (Cmstacea

Decapoda: Paguridea, Galatheidea, Hippidea). Zoologische

Verhandelingen 104; 1-213.

Lewinsohn, C.,1982. Researches on the coast of Somalia. The shore

and the dune of Sar Uanle. Diogenidae, Paguridae and

Coenobitidae. Monitore Zoologico Italiano, Supplemento\6{2):

35-68.

Morgan, G.J. 1987. Hermit crabs (Decapoda, Anomura; Coenobitidae,

Diogenidae, Paguridae) of Darwin and Port Essington, Northern

Australia. The Beagle, Records of the Northern Territory Museum

of Arts and Science A(l): 165-186.

Rahayu, D.L. 1999. Descriptions of two new species of hermit crabs

Clibanarius rubroviria and C. rutilus (Crustacea: Decapoda:

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Anomura: Diogenidae) from Indonesia. Raffles Bulletin of Zoology

47 (2): 299-307.

Rahayu, D.L., and Forest, J. 1992. Le genre Clibanarius (Crustacea,

Decapoda, Diogenidae) en Indonesia, avec la description de six

especes nouvelles. Bulletin du Museum national d’Histoire

naturelle, Paris (4) 14 (3-4): 745-779.

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Shikoku University 6: 1-45.

Memoirs of Museum Victoria 60(1): 105-110 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

A new genus and species of hermit crab (Crustacea: Anomura: Paguridae)

from Taiwan

Rafael Lemaitre

Department of Systematic Biology, National Museum of Natural History, Smithsonian Institution, Washington, DC

20560-7012, USA (lemaitre.rafael@nmnh.si.edu)

Abstract Lemaitre, R. 2003. A new genus and species of hermit crab (Cmstacea: Anomura: Paguridae) from Taiwan. In: Lemaitre,

R., and Tudge, C.C. (eds). Biology of the Anomura. Proceedings of a symposium at the Fifth International Crustacean

Congress, Melbourne, Australia, 9-13 July 2001. Memoirs of Museum Victoria 60(1): 105-110.

A new monotypic hermit crab genus, Chanopagurus (Paguridae), is described for a new species, C. atopos, based on

an ovigerous female specimen collected in deep water (880 m) off the coast of Taiwan. The single specimen is unique in

having: 13 pairs of quadriserial gills which include two reduced but functional pleurobranchs on the fifth and sixth tho-

racic somites; ocular peduncles concave mesially; reduced, unpigmented corneas located lateroventrally; ocular acicles

each armed with very small spine; unpaired left gonopore; and paired first pleopods. The new species shares with

Propagurus McLaughlin and de Saint Laurent, the presence of reduced pleurobranchs on the fifth and sixth thoracic

somites. The superficial resemblance of C. atopos with species of Tomopaguropsis Alcock, in having subequal chelipeds,

and long, dense setae on the antennae, chelipeds and second and third pereopods, is considered homoplasy.

Keywords Cmstacea, Anomura, Paguridae, taxonomy, Chanopagurus, new genus, new species

Introduction

While studying hermit crabs obtained in deep waters off

Taiwan during a joint Taiwanese-French cruise (TAIWAN

2000, July-August, 2000), a female specimen of Paguridae was

encountered that could not be assigned to any known genus.

The combined presence of 13 pairs of quadriserial gills, sube-

qual chelipeds, unpaired left gonopore and paired first pleopods

are distinctive among Paguridae. In addition, the concave shape

of the mesial surfaces of the ocular peduncles, the lateroventral

placement of the unpigmented corneas, and unusually small

spines on the ocular acicles, are striking. The specimen clearly

represents a separate lineage for which a new genus and species

are herein described and illustrated.

Gill terminology follows McLaughlin and de Saint Laurent

(1998: 161). Forest et al. (2000: 24) is followed in the interpre-

tation of the ocular peduncle, which is provided basally with a

small calcified plate referred to as the “ocular acicle”. The term

“semichelate” was defined by McLaughlin (1997: 435). Shield

length (SL) is measured from the tip of the rostrum to the mid-

point of the posterior margin of the shield.

Chanopagurus gen. nov.

Type species. Chanopagurus atopos sp. nov.

Diagnosis. 13 pairs of quadriserial gills (Fig. la): 2 arthro-

branchs on each of third maxillipeds and first to fourth pere-

opods, 1 reduced but functional pleurobranch on fifth and sixth

thoracic somites (above second and third pereopods), and 1

well-developed pleurobranch on seventh thoracic somite

(above fourth pereopods). Shield well calcified. Rostral lobe

unarmed, not exceeding lateral projections. Cornea lateroven-

tral. Ocular acicle with small spine. Posterior carapace almost

entirely membranous. Antennal peduncle with supernumerary

segmentation. Maxillule with external endopodal lobe not

recurved. Third maxillipeds widely separated basally; ischium

with crista dentata well developed, and 1 accessory tooth.

Chelipeds subequal in length. Second and third pereopods sim-

ilar except for slightly longer meri on right pereopods. Sixth

thoracic stemite (of third pereopods) divided into anterior and

posterior lobes by distinct, membranous hinge. Abdomen not

reduced, membranous except for moderately calcified tergite of

sixth somite. Tergite of sixth somite with transverse furrow

dividing tergite into anterior and posterior portions, each por-

tion having weak, median longitudinal depression. Uropods

asymmetrical, left larger than right. Telson symmetrical, with

distinct lateral indentations separating anterior and posterior

lobes, latter each with “half-moon” contour and blade-like lat-

eral margin. Female with unpaired left gonopore; with paired

first and biramous left second to fifth pleopods. Male unknown.

Etymology. This genus is named for Dr Tin- Yam Chan

(NTOU), in recognition of his outstanding efforts to advance

our knowledge of the Taiwanese crustacean fauna. The genus

106

R. Lemaitre

name is a combination of his last name with the Greek

pagourus meaning crab. Masculine.

Remarks. Chanopagurus is the sixth genus of Paguridae with

13 pairs of quadriserial gills; the others are: Bathypaguropsis

McLaughlin, 1994, Propagurus McLaughlin and de Saint

Laurent, 1998, Tomopaguroides Balss, 1912, Tomopaguropsis

Alcock, 1905, and Xylopagurus A. Milne Edwards, 1880.

Chanopagurus shares with Propagurus the presence of reduced

or moderately well developed pleurobranchs on the fifth and

sixth thoracic somites. As in the Pylopaguropsis group of

pagurid genera (cf. de Saint Laurent-Dechance, 1966)

Chanopagurus seems to be undergoing an evolutionary process

leading to reduction or loss of pleurobranchs similar to that in

Propagurus (see McLaughlin and de Saint Laurent, 1998).

Chanopagurus shows only homoplastic similarity to

Tomopaguropsis, in having species with subequal chelipeds,

and numerous setae on the antennal peduncles and flagella,

chelipeds and second and third pereopods. Chanopagurus dif-

fers from Propagurus and Tomopaguropsis in important char-

acters, for example, the shape and location of the corneas, ocu-

lar acicles, number of rows of scales on the propodal rasp of the

fourth pereopods, number of female gonopores, number of

pleopods in females, and shape of telson. Although reduction of

ocular peduncles and corneas has occurred frequently in some

Pylochelidae, Paguridae, Parapaguridae, it rarely is accom-

panied by a shift in the position of the corneas or a change in

the shape of the peduncles as seen in this new species. The

lateroventral position of the corneas, and concave mesial sur-

face of the ocular peduncles (Figs Ic-e) in C. atopos, are

unique autapomorphies among Paguridae. Although the short

ocular acicles, each armed with a very small spine in C. atopos,

are unusual among Paguridae, a similar condition does occur in

Probeebei mirabilis Boone, 1926, a highly specialized deep-sea

parapagurid (de Saint Laurent, 1972; Lemaitre, 1998).

Chanopagurus atopos sp. nov.

Figures 1-3

Material examined. Holotype: South China Sea, off Taiwan,

22°14.8'N, 120°02.8T, 880 m, 29 Jul 2000 (TAIWAN 2000 station

CP 23), National Taiwan Ocean University, Keelung, Taiwan, NTOU

H-23a (ovigerous female, SL 6.0 mm).

Description of holotype. Shield (Fig. lb) about as broad as

long; anterolateral margins sloping; posterior margin truncate;

accessory portions extending posteriorly slightly beyond poste-

rior margin, delimited by deep grooves; dorsal surface with

numerous tufts of short transverse or oblique rows of setae.

Rostral lobe not exceeding lateral projections, broadly rounded.

Lateral projections subtriangular, strongly produced and each

armed with prominent terminal spine. Branchiostegites calci-

fied dorsodistally; anterodistal margins rounded, setose.

Posterior carapace with small calcareous anterolateral tubercle

on each side, and small calcified portion adjacent to posterior

margin of shield lateral to each cardiac sulcus.

Ocular peduncles (Fig. Ib-e) short, stout, inflated and near-

ly contiguous basally, tapering distally; dorsal surface with tuft

of few setae medially; dorsomesial margin well defined by low.

setose lobes; mesial surface (Fig. Id) concave medially, with

small setose tubercle submedially. Cornea reduced, surface

weakly convex, unpigmented. Ocular acicles (Fig. Ic) nearly

contiguous basally, about 3 times as broad as long, each with

very small calcareous spine pointing anteromesially.

Antennular peduncle (Fig. lb), when fully extended, over-

reaching ocular peduncle by 0.5 length of penultimate segment.

Ultimate segment about 2.3 times as long as penultimate seg-

ment; dorsal surface with short setae. Penultimate segment with

few setae dorsally. Basal segment with acute spine on dorsolat-

eral margin. Ventral flagellum with 6 articles. Antennal pedun-

cle (Fig. lb) strong and nearly as long as shield length, over-

reaching ocular peduncles by full length of fourth peduncular

segment. Fifth segment nearly twice as long as fourth segment;

with setae laterally. Fourth segment with few setae laterally.

Third segment with small spine on ventrodistal margin. Second

segment with dorsolateral, distal angle produced, terminating in

strong simple (left) or bifid (right) spine; dorsomesial distal

angle with prominent spine. First segment with small spine at

laterodistal margin, and 2 small spines on ventrodistal margin.

Acicle long, reaching distal margin of fifth antennal segment;

broadly curving laterally (dorsal view), terminating in strong

spine; mesial margin with dense, long simple setae. Flagellum

relatively short, not overreaching right cheliped; articles with

numerous long, simple setae 1-4 times as long as each anten-

nal article.

Mouthparts not dissected. Mandible with incisor edge near-

ly straight, calcified. Maxillule with external endopodal lobe

short, internal endopodal lobe bearing 3 long distal setae. First

maxilliped with multiarticulate flagellum. Maxilla with elon-

gate, slender endopod reaching distal margin of adjoining

endite. Second maxilliped without distinguishing characters.

Th ir d maxilliped with crista dentata (Fig. If) of 13 or 14

corneous-tipped teeth; accessory tooth on inner face of ischium

placed submedially; basis with 3 corneous-tipped teeth on

mesial margin. Third thoracic sternite (of third maxillipeds;

Fig. If) with strong corneous-tipped spine on each side of

midline.

Chelipeds subequal in length; right slightly longer, stouter.

Right cheliped (Fig. Ig) with dorsal surfaces of carpus and

chela covered with numerous tufts or short transverse rows of

long, simple, stiff setae. Dactyl and fixed finger weakly curved

ventrally, lacking spines; dactyl about as long as mesial margin

of palm, terminating in blunt corneous claw; cutting edges each

with 2 large, rounded calcareous teeth on proximal half, and

row of short, fused corneous teeth distally. Palm about as broad

as long, unarmed except for small, setose tubercles on dorsal

and ventral surfaces; mesial and lateral margins rounded; ven-

tral surface smooth except for scattered tufts of setae proxim-

ally, and long setae near base of fixed finger. Carpus slightly

broadened distally; unarmed except for distal dorsomesial spine

and low setose tubercles on dorsal surface; ventral surface

smooth except for scattered setae. Merus with short transverse

rows of setae on dorsal margin; lateral, mesial, and ventral sur-

faces smooth except for scattered setae; ventral surface with

small ventromesial and ventrolateral spines distally. Ischium

with scattered setae; ventral surface with small ventromesial

and ventrolateral spines distally. Left cheliped (Fig. Ih) with

108

R. Lemaitre

Figure 2. Chanopagurus atopos sp. nov., holotype female ovigerous (NTOU H-23a): a, left second pereopod, lateral; b, dactyl of same, mesial;

c, left third pereopod, lateral; d, dactyl of same, mesial; e, propodus and dactyl of left fourth pereopod, lateral; f, propodus and dactyl of left fifth

pereopod, lateral. Scales equal 1 mm (a-d), and 0.5 mm (e, f).

dorsal surfaces of carpus and chela covered with numerous

tufts or short transverse rows of long, simple, stiff setae. Dactyl

and fixed finger weakly curved ventrally, each terminating in

blunt corneous claw; dactyl about 1.5 times as long as mesial

margin of palm; cutting edges each with row of short, fused

corneous teeth distally, on fixed finger corneous teeth inter-

spersed with short calcareous teeth. Palm lacking spines; dorsal

surface with very small setose tubercles; ventral surface smooth

except for long setae near base of fixed finger. Carpus with

dorsodistal spine; dorsal surface with weak longitudinal depres-

sion; mesial margin strongly sloping; ventral surface smooth

except for scattered setae. Merus with short, transverse rows of

long setae on dorsal margin; lateral, mesial, and ventral sur-

faces smooth except for scattered setae; ventral surface with

small ventromesial and ventrolateral spines distally. Ischium

with scattered setae; ventral surface with small ventromesial

and ventrolateral spines distally.

Second and third pereopods (Figs 2a-d) with meri, carpi,

propodi and dactyls having numerous, long stiff setae on later-

al and mesial surfaces; meri, caipi and propodi with low tuber-

cles transverse rows of long stiff setae. Dactyls (Figs 2b, d)

broadly curved, each terminating in sharp, corneous claw,

about 1.7 (second pereopod) to 1.9 (third pereopod) as long as

propodus; with dorsal and dorsomesial distal rows of long

setae; with ventromesial row of 3-8 spinules. Propodi lacking

spines. Carpi each with dorsodistal spine. Meri lacking spines.

Ischia with scattered tufts of setae on lateral face and dorsal

margin. Sixth thoracic stemite (of third pereopods; Fig. 3a)

with anterior lobe subrectangular, setose, with 6 small sub-

distal spines. Fourth pereopod (Fig. 2e) semichelate, with long

setae dorsally on merus, carpus, propodus and dactyl. Dactyl

subtriangular, terminating in sharp, corneous claw; with ven-

trolateral row of closely-set corneous spines; no preungual

process. Propodus with rasp consisting of single row of ovate

New hermit crab from Taiwan

109

Figure 3. Chanopagurus atopos sp. nov., holotype female ovigerous (NTOU H-23a): a, anterior and posterior lobes of sixth thoracic sternite, ven-

tral (setae omitted); b, female coxae and eighth thoracic sternite, and part of abdomen (lower) showing first pleopods, ventral; c, uropods and tel-

son, dorsal. Scales equal 0.5 mm (a), and 1 mm (b, c).

scales distally, and 2 rows proximally; lateroventral surface and

ventral margin setose. Fifth pereopod (Fig. 2f) chelate; chela

with dense, long setae on dorsal and ventral margins distally.

Propodal rasp occupying subtriangular area not reaching mid-

point of segment, consisting of small, closely-set rounded

scales. Merus and carpus with long setae on dorsal and ventral

margins.

Uropods (Fig. 3c) with left exopod about 3 times as long as

broad, somewhat sickle- shaped, and about twice as long as

right exopod; rasps of exopod and endopod consisting of small,

closely-set rounded scales. Telson (Fig. 3c) longer than broad,

with scattered short setae dorsally; anterior lobes setose disto-

laterally; with lateral angles of posterior lobes each produced as

prominent spine with minute corneous tip; posterior lobes sep-

arated by U-shaped median cleft, concave inner margins with 1

(right) or 2 (left) minute, blunt spines.

Female first pleopods (Fig. 3b) slender, overreaching ventral

margin of eighth thoracic sternite (sternite of fifth pereopods);

with few short setae distally; segmentation not apparent. Eggs

large, diameter about 1.8 mm.

Male. Unknown.

Colour. In preservative, uniformly orangish, with yellowish

setae.

Distribution and habitat. Off Taiwan, South China Sea; 880 m;

inhabiting a gastropod shell.

Etymology. Atopos, Greek, meaning out of place, odd, or

strange, referring to the unusual characteristics of the ocular

peduncles, corneas and ocular acicles.

Acknowledgements

I thank T.-Y. Chan (NTOU) and A. Crosnier (Museum national

d’Histoire naturelle, Paris), for allowing me to study the hermit

crabs from the Taiwanese-French cruise. The critical comments

on the manuscript by P. A. McLaughlin (Western Washington

University) are greatly appreciated.

110

R. Lemaitre

References

Forest, J., de Saint Laurent, M., McLaughlin, P.A., and Lemaitre, R.

2000. The marine fauna of New Zealand; Paguridea (Decapoda:

Anomura) exclusive of the Lithodidae. NIWA Biodiversity Memoir

114: 1-250.

Lemaitre, R. 1998. Revisiting Tylaspis anomala Henderson, 1885

(Parapaguridae), with comments on its relationships and evolution.

Zoosy sterna 20: 289-305.

McLaughlin, PA. 1997. Cmstacea Decapoda: Hermit crabs of the fam-

ily Paguridae from the KARUBAR Expedition in Indonesia. In;

Crosnier, A. (ed.), Resultats des Campagnes MUSORSTOM,

Volume 16. Memoires du Museum national d’Histoire naturelle

172: 433-572.

McLaughlin, P.A., and de Saint Laurent, M. 1998. A new genus for

four species of hermit crabs formerly assigned to the genus Pagurus

Fabricius (Decapoda; Anomura: Paguridae). Proceedings of the

Biological Society of Washington 111: 158-187.

de Saint Laurent, M. 1972. Sur la famille des Parapaguridae Smith,

1882. Description de Typhlopagurus foresti gen. nov., et de quinze

especes ou sous-especes nouvelles de Parapagurus Smith

(Cmstacea, Decapoda). Bijdragen tot de Dierkunde 42: 97-123.

de Saint Laurent- Dechance, M. 1966. Remarques sur la classification

de la famille des Paguridae et sur la position systematique d'

Iridopagurus de Saint Laurent. Diagnose d' Anapagrides gen. nov.

Bulletin du Museum national d'Histoire naturelle, Paris, 2e series,

38: 257-265.

Memoirs of Museum Victoria 60(1): 111-144 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

Illustrated keys to families and genera of the superfamily Paguroidea (Crustacea:

Decapoda: Anomura), with diagnoses of genera of Paguridae

Patsy A. McLaughlin

Shannon Point Marine Center, Western Washington University, 1900 Shannon Point Road, Anacortes, Washington,

98221-9081B, USA (patsy@sos.net)

Abstract McLaughlin, PA. 2003. Illustrated keys to families and genera of the superfamily Paguroidea (Crustacea: Decapoda:

Anomura), with diagnoses of genera of Paguridae. In: Lemaitre, R., and Tudge, C.C. (eds). Biology of the Anomura.

Proceedings of a symposium at the Fifth International Cmstacean Congress, Melbourne, Australia, 9-13 July 2001.

Memoirs of Museum Victoria 60(1): 111-144.

Keys, with illustrations of selected diagnostic characters, are provided for the seven families and 122 genera of the

anomuran Superfamily Paguroidea, commonly known as hermit crabs and king crabs. In addition, abbreviated diagnoses

are presented for the 69 genera presently assigned to the family Paguridae.

Keywords Cmstacea, Anomura, Paguroidea, Paguridae, keys, diagnoses

Introduction

The interest in, and attendance at, the symposium on Biology of

the Anomura at the Fifth International Crustacean Congress,

2001, indicates the recent focus on this group of decapod

crustaceans by researchers in several disciplines (e.g. Martin

and Abele, 1986, 1988; Tudge and Jamieson, 1991;

Cunningham et al., 1992; Elwood and Neil, 1992; Tudge, 1992,

1997a, b; Richter and Scholtz, 1994; Scholtz and Richter, 1995;

d’Amato and Corach, 1997; McLaughlin and Lemaitre, 1997,

2001a; Tudge et al., 1998; Morrison and Cunningham, 1999;

Forster and Baeza, 2001; Macpherson and Machordom, 2001;

Tudge et al., 2001). Much of this attention has been directed to

the morphologically very diverse assemblage commonly

known as hermit crabs and king crabs (Fig. 1). It is not surpris-

ing that perusal of some of these references demonstrates the

lack of agreement among carcinologists on changes in the clas-

sification of this group from 1987 to 2001. Specifically,

because of endophragmal differences, Forest (1987) reinstated

the superfamily Coenobitoidea Dana, 1851, that had been sup-

pressed by McLaughlin (1983), combining it with the super-

family Paguroidea Latreille, 1802, under the Section Paguridea.

Forest’s (1987) and Forest et al.’s (2000) information, based on

unpublished observations of Mme M. de Saint Laurent,

Museum national d’Histoire naturelle, Paris, apparently was

not sufficiently convincing to Martin and Davis (2001), who in

their Updated classification of Recent Crustacea, once again

suppressed the Coenobitoidea and grouped all hermit crab

families under the Superfamily Paguroidea. As pointed out by

Holthuis (1993), the category, section, was defined by the third

edition of International Code of Zoological Nomenclature

(1985) as a subdivision of a genus. The fourth edition (1999),

article 10.4, reaffirms that definition. Although the Code does

not deal with taxonomic levels above the family group, the use

of the term, section, in other hierarchical levels does not seem

appropriate. Therefore, I have adopted the classification of the

Anomura proposed by Martin and Davis (2001).

To complicate matters even further, there has been an

explosion of new genera over the past two decades, as well as

additions to and other changes in the hierarchy. Thus it

appeared that the presentation of an illustrated set of keys to the

families and genera of the Superfamily Paguroidea, would

benefit not only new-comers to the field of paguroid syste-

matics, but to specialists in other disciplines as well. The user

of the keys contained herein will not be hampered, whether he

or she concurs with the Martin and Davis (2001) classification

or the classification of Forest (1987) and Forest et al. (2000).

Although within the Diogenidae, several of the larger gen-

era have been reported on in considerable detail (e.g. Forest,

1984, 1995; Morgan, 1991; Poupin, 1997; Rahayu and Forest,

1993, 1995), as have the Lithodidae (Dawson and Yaldwyn,

1985; Macpherson, 1988), Pylochelidae (Forest, 1987),

Coenobitidae (Nakasone, 1988), and Parapaguridae (Lemaitre,

1989, 1996, 1997, 1999), such is not the case for the family

Paguridae. The few comprehensive studies of this family have

been, for the most part, regional and/or not easily accessed (e.g.

McLaughlin and Haig,1984, 1989; McLaughlin, 1 997 ; Asakura,

2000, 2001). Therefore, while keys to all of the genera are

112

RA. McLaughlin

presented, the key to the family Paguridae is supplemented

with an overview of the morphology of the family itself, and

abbreviated diagnoses of the 69 genera (including two

subgenera) currently recognised.

The key to families is an adaptation of that presented by

McLaughlin and Lemaitre (2001c) when they introduced the

new family Pylojacquesidae. Portions of the keys to the genera

have been adapted from Forest (1984, 1987), Macpherson

(1988), Lemaitre (1996), McLaughlin (1997), Forest and

McLaughlin (2000), de Saint Laurent and McLaughlin (2000),

McLaughlin and Lemaitre (2001b), Asakura (2001), and

Lemaitre and McLaughlin (in press). In some instances, intra-

generic variability has made it necessary, either to key individ-

ual species that do not conform entirely with particular diag-

nostic characters of the genus, or to key the genus more than

once. In these instances, the notation (in part) follows the

generic name and author.

Terminology, for the most part, follows that of Forest and

McLaughlin (2000) for Coenobitidae and Diogenidae, de Saint

Laurent and McLaughlin (2000) for the Paguridae, and

Lemaitre (2000) for the Parapaguridae; however, the interpre-

tation of quadriserial gills employed by Lemaitre (in press) has

been used in preference to the more general terminology of

McLaughlin and de Saint Laurent (1998). Enumeration of body

somites follows that of Pilgrim (1973), while that of thoracom-

eres follows that of Forest et al. (2000). Terminology for the

Lithodidae follows that of Sandberg and McLaughlin (1998)

for the cephalothorax and its appendages, and that of

McLaughlin and Paul (2002) for the abdominal tergites. The

illustrations of key characters provided throughout should pre-

clude any necessity to refer to these earlier works to utilise the

keys; however, it must be emphasised that the illustrations are

of characters and not necessarily of those of particular genera.

As was noted by Forest et al. (2000), the ocular peduncles

are thought to be two or three- segmented. The references to the

ultimate and penultimate segments of the ocular peduncles

refer to the distal-most and median segments, respectively. The

first segments are believed to be represented by a fused seg-

ment most frequently reported as the “ocular lobe(s)”, which

usually is unarmed, but may be provided with a pair of small

spines. Sandberg and McLaughlin (1998: 11, fig. 3A) and

Forest et al. (2000: 24, figs lb, Ic) have defined the ocular aci-

cle as a small calcified plate basally on the penultimate pedun-

cular segment. In contrast, Boyko and Harvey (1999: 383, fig.

2A) have contended that the ocular acicle is not part of the

plate, but only an anterodorsal spine or plate-like extension of

the “proximal” peduncular segment. Unfortunately, Boyko and

Harvey’s definition applies only to those species where some

type of projection is produced from the plate itself, which is not

the case in all hermit crabs. The “ocular plate” of some

Pylochelidae is nothing more than the plate itself. To say then

that these species lack ocular acicles does not seem justified, as

there is no evidence to suggest a lack of homology between the

simple ocular plate and the ocular plate that has developed a

projection of one form or another. In the keys presented herein,

the term ocular acicle refers to the entire calcified plate whose

projected portion, if present, may be simple (represented by a

single spinose process) bifid, (with two distal spines) or

multispinose (having three or more spines on the distal

margin).

Certain species of the Coenobitidae possess calcified, tubu-

lar elongations of one or both coxae of pereopod 5 in males;

however, only in males of a number of genera of the Paguridae

are membranous, chitinous, or weakly calcified sexual tubes

developed. When present, these structures provide diagnostic

characters of significant importance. Although most descrip-

tions have included the orientation of the sexual tube (e.g.

across the ventral body surface, toward the exterior, etc.),

heretofore, these tubes have been described only in very gener-

alised terms, such as long, short, coiled, or with a terminal fila-

ment. For the purposes of the key to the Paguridae, four more

precisely defined descriptive terms pertaining to tube length,

have been adopted herein, i.e., very short (< length of coxa

measured on its ventral surface), short, (1-2 coxal lengths),

medium (>2-5 coxal lengths), long (>5 coxal lengths).

Additionally, a very slight protuberance is referred to in the key

as a papilla. Keys to the genera are arranged according to the

key to the families, and do not imply any phylogenetic rela-

tionships. The family Pylojacquesidae McLaughlin and

Lemaitre, 2001c is represented only by the monotypic genus

Pylojacquesia.

Keys to the families of Paguroidea

1. Antennules with upper rami of flagella terminating

bluntly, somewhat “stick-like” (Figs la, b, 2h) (semiterres-

trial) Coenobitidae

— Antennules with upper rami of flagella terminating in

tapered filament, not “stick-like” (Figs Ic-g, k-q, 2i, j, 3a,

c-j, m) (marine, estuarine) 2

2. Paired pleopods on abdominal somites 2-5; abdominal

tergites 1-5 well defined, well calcified (Fig. Ic)

Pylochelidae

— No paired pleopods on abdominal somites 4 and 5 ; abdom-

inal tergites variable, but most frequently not well calcified

(Figs Id-g, i, 1-p, 3a) 3

3. Maxilliped 3 generally approximate basally (Figs 2a-c);

chelipeds equal, subequal or unequal, left frequently

largest (Figs Id-g) Diogenidae

— Maxilliped 3 generally widely separated basally (Figs

2d-f); chelipeds unequal or less frequently subequal, right

usually largest (Figs li-q) 4

4. Mandible with incisor process mostly corneous, armed

with prominent, acute teeth (Fig. 4i); sternite XI distinctly

separated from sternite XII by membranous area (Fig. 21)

Pylojacquesidae

— Mandible with incisor process calcareous (Fig. 4j) or with

only mesial edge corneous, lacking acute teeth; sternite XI

not distinctly separated from sternite XII, usually fused

(Fig. 2m) 5

5. Pereopod 4 developed as normal walking leg (Figs li-k;

3b, 8h); body crab-like; abdomen recurved and carried

under cephalothorax (Figs Ij, k) Lithodidae

— Pereopod 4 not developed as normal walking leg (Figs

11-q, 3a); body not crab-like; abdomen usually not

recurved and carried under cephalothorax 6

Illustrated keys to the families and genera of Paguroidea

113

6. Exopod of maxilliped 1 with flagellum (Fig. 4m)

Paguridae

— Exopod of maxilliped 1 without flagellum (Fig. 4n) ....

Parapaguridae

Key to genera of Coenobitidae

1. Pereopod 4 elongate, chelate; abdomen somewhat flexed

(Fig la); rostrum well developed . . Birgus Leach, 1815

— Pereopod 4 short, not chelate; abdomen spirally twisted

(Fig lb); rostrum obsolete . . . .Coenobita Latreille, 1829

Key to genera of Pylochelidae

1. Shield incompletely separated from posterior carapace,

linea transversalis not apparent medially (Figs 3c, e);

telson divided into anterior and posterior articulating

plates (Fig. 5a) 2

— Shield completely separated from posterior carapace, linea

transversalis clearly apparent medially (Figs 3d, f-h);

telson not divided into anterior and posterior articulating

plates (Fig. 5b) 3

2. Shield approximately as long as broad; anterior margin

with median concavity and rarely rostral spinule (Fig. 3c);

corneas always hemispherical

Pylocheles A. Milne-Edwards, 1880

— Shield distinctly broader than long; anterior margin with

rounded rostral lobe (Fig. 3e) or with short rostral spine;

corneas reduced or absent (Fig. 3e)

Cheiroplatea Bate, 1888

3. Penultimate segments of ocular peduncles without ocular

acicles developing squamiform or spiniform anterior

projections (Figs 3f, h) 4

— Penultimate segments of ocular peduncles with ocular aci-

cles each developing triangular or squamiform anterior

projection (Figs 3d, i, j, m) 6

4. Penultimate segments of ocular peduncles each with well

developed, rounded or subrectangular plate (Fig. 3f);

telson with pair of oblique lateral incisions, terminal mar-

gin with prominent median cleft; maxilliped 2 without

epipod Pomatocheles Miers, 9

— Penultimate segments of ocular peduncles each with

reduced, narrow, calcified plate (Fig. 3g, h); telson with or

without pair of oblique lateral incisions, but never promi-

nent, terminal margin with or without median cleft; maxil-

liped 2 with epipod (Fig. 4o) 5

5. Shield as long as broad; rostral spine short, without acces-

sory ventral spine; ultimate segments of ocular peduncles

spinose, conical and tapered (Fig. 3g); telson rectangular,

longer than broad, with pair of faint, oblique, lateral

grooves, terminal margin with slight median notch

Parapylocheles Alcock, 1901

— Shield broader than long; rostrum very prominent, with

accessory ventral subdistal spine; ultimate segments of

ocular peduncles unarmed, basally swollen (Fig. 3h); tel-

son subquadrate, slightly broader than long, without pair of

faint, oblique, lateral grooves, terminal margin entire . . .

Cancellocheles Forest, 1987

6. Abdominal somites, pleopods 3-5, and uropods symmetri-

cal; telson subrectangular, longer than broad, usually with

transverse line of flexion delimiting rounded posterior

lobes (Fig. 5b); maxilliped 3 without epipod (Fig. 4q)

Trizocheles Forest, 1987

— Abdominal somites, pleopods 3-5, and uropods asymmet-

rical; telson variable; maxilliped 3 with epipod (Fig. 4p)

Mixtopagurus A. Milne-Edwards, 1880

Key to genera of Diogenidae

1. Well developed arthrobranchs present on arthrodial

membranes at bases of cheliped and maxilliped 3;

pleurobranch present on somite XI (thoracomere 5, above

pereopod 2) (Fig. 4a) 2

— Reduced or vestigial arthrobranchs present on arthrodial

membranes at bases of cheliped and maxilliped 3; no

pleurobranch present on somite XI (thoracomere 5, above

pereopod 2) (Fig. 4c)

Pseudopaguristes McLaughlin, 2002

2. 14 pairs of gills; pleurobranch present on somite XIV (tho-

racomere 8, above pereopod 5) (Fig. 4a) 3

— 13 pairs of gills; no pleurobranch present on somite XIV

(thoracomere 8, above pereopod 5) (Fig. 4b) 14

3. Endopod of maxillule with well developed external lobe

(Fig. 4k) 4

— Endopod of maxillule without well developed external

lobe (Fig. 41) 8

4. Ischium of maxilliped 3 with well developed crista

dentata (Figs 2b-f) 5

— Ischium of maxilliped 3 without well developed crista

dentata (Fig. 2a) 12

5. Chelipeds equal or unequal, each with stridulatory

mechanism developed on mesial face of palm (Fig. 6a) 6

— Chelipeds markedly unequal, left largest; neither with

stridulatory mechanism developed on mesial face of palm

(Fig. 6b) Allodardanus Haig and Provenzano, 1965

6. Chelipeds with acute, corneous-tipped spines on carpi and

chelae; males often with pleopod 2 paired, endopod well

developed, reduced or absent (Fig. 7g)

Strigopagurus Forest, 1995

— Chelipeds with tubercles or transverse striate on carpi and

chelae; males without pleopod 2 paired 7

7. Chelipeds equal or left larger; carpus and palm with trans-

verse striae bordered with fine setae (Fig. 6c); dactyls of

ambulatory legs equal to or longer than propodi; females

with unpaired pleopods 2-5 egg-carrying

Ciliopagurus Forest, 1995

— Chelipeds equal, carpus and palm covered with generally

blunt tubercles; dactyls of ambulatory legs much shorter

than propodi; females with unpaired pleopod 5 non egg-

carrying Trizopagurus Forest, 1952

8. Chelae symmetrical, together forming operculum (Fig.

6d); uropods symmetrical (Fig. 8j)

Cancellus H. Milne Edwards, 1836

— Chelae symmetrical or asymmetrical, together not forming

operculum; uropods generally asymmetrical 9

114

P.A. McLaughlin

9. Chelipeds unequal, right distinctly larger

Petrochirus Stimpson, 1858

— Chelipeds subequal or unequal, left usually at least

slightly larger 10

10. Shield with prominent Y-shaped linea in posterior half

(Figs 8a, c); posterior carapace primarily membranous; left

cheliped slightly to considerably larger than right .... 1 1

— Shield without prominent Y-shaped linea (Fig. 8b, 1);

posterior carapace well calcified; chelipeds subequal . . .

Tisea Morgan and Forest, 1991

1 1 . Rostrum triangular; ocular acicles each with prominent tri-

angular or subtriangular acicular projection (Figs 8a, b);

chelipeds and ambulatory legs with ring-like transverse

striae (Fig. 6e); females with well-developed brood pouch

(Fig. Id) Aniculus Dana, 1852

— Rostrum broadly rounded or obsolete (Fig. 8c, 1); ocular

acicles each with subrectangular or subquadrate acicular

projection (Fig. 8c); chelipeds and ambulatory legs most

often without ring-like transverse striae; females without

brood pouch Dardanus Paul’ son, 1875

12. Antennal flagella with microscopic setae

Pseudopagurus Forest, 1952

— Antennal flagella with paired, moderate to long setae

(Fig. 2k) 13

13. Chelipeds equal or slightly subequal, similar, dactyls open-

ing in generally horizontal plane (Fig. 6f)

Isocheles Stimpson, 1858

— Chelipeds unequal and dissimilar; dactyls opening in

almost vertical plane (Fig. 6g) .Loxopagurus Forest, 1964

14. Males with pleopods 1 and/or 2 paired, modified as

gonopods (Figs 7a, e, f); females with (Figs 2m, 7b, c) or

without pleopod 1 paired, modified 15

— No paired pleopods in either sex 16

15. Pereopod 4 chelate (Fig. 5t); unpaired pleopods 3-5 occur-

ring on either right or left side of abdomen

Paguropsis Henderson, 1888

— Pereopod 4 not chelate; unpaired pleopods 3-5 occurring

on left side of abdomen only . . . Paguristes Dana, 1851

16. Chelipeds subequal (Fig. IQ 17

— Chelipeds unequal, left appreciable larger (Figs Id, e, g). . . .

17. Ocular acicles bi or multispinose, contiguous or closely set

(Fig. If, 8b); posterior margin of abdominal somite 6

unarmed Clibanarius Dana, 1852

— Ocular acicles simple, widely separated (Figs 3a, d);

posterior margin of abdominal somite 6 spinulose

Bathynarius Forest, 1989

18. Rostrum obsolete, roundly subtriangular or broadly round-

ed, intercalary rostral process present, well developed,

reduced or vestigial (Fig. 3i) Diogenes Dana, 1851

— Rostrum moderate to well developed, triangular,

intercalary rostral process absent . . .Calcinus Dana, 1851

Key to genera of Lithodidae

1. Abdomen usually soft, membranous, sac-like; abdominal

tergites 3-5 not fully calcified (Figs li, 9a-d) rostral

process short, broad, triangular, not usually overreaching

distal margins of corneas 2

— Abdomen generally firm, at least partially calcified, not

sac-like; abdominal tergites 3-5 usually well calcified

(Figs 9f-k), sometimes with median areas membranous;

rostral process well-developed, prominent, truncate or

spiniform (Fig. 8f, h), overreaching distal margins of

corneas (Fig. 3b) 6

2. Tergite of abdominal somite 2 divided into median, paired

lateral and paired marginal plates (Figs 9a, b, d, e, h) . 3

— Tergite of abdominal somite 2 divided into paired lateral

and marginal plates, median plate virtually nonexistent

(Fig. 9c) Placetron Schalfeew, 1892

3. Median plate of abdominal somite 2 well calcified or with

cluster of calcified granules (Figs 9a, b) 4

— Median plate of abdominal somite 2 membranous (Fig. 9d)

4. Carapace well calcified, dorsal surface and margins armed

with numerous subequal spines; rostral process with dorsal

and lateral spines Acantholithodes Holmes, 1895

— Carapace weakly calcified, dorsal surface lacking spines

but setose or pubescent; rostral process simple, lacking

dorsal and lateral spines (Fig. li)

Hapalogaster Brandt, 1850

5. Surface of carapace covered with squamose prominences,

chelipeds tuberculate (Fig. 6p)

Oedignathus Benedict, 1895

— Surface of carapace and chelipeds covered with transverse

ridges or crests (Fig. 6q) Dermaturus Brandt, 1850

6. Carapace nearly smooth, unarmed, broader than long and

completely covering ambulatory legs when legs are drawn

in against body (Figs Ih, 8h); rostral process broad, com-

pressed, distally truncate (Fig. Ih, 8h)

Cryptolithodes Brandt, 1848

— Carapace armed with granules, tubercles or spines, not

broader than long and not completely covering ambulatory

legs when legs are drawn in against body; rostral process

variable in shape, but not compressed and distally truncate

7. Sternite of somite XI (pereopods 2) with deep longitudinal

medial groove or pit (Fig. 2n) 8

— Sternite of somite XI (pereopods 2) without deep

longitudinal medial groove or pit 10

8. Tergite of abdominal somite 2 subdivided into median and

paired lateral and marginal plates (Figs 9a, b, d, e, h) .9

— Tergite of abdominal somite 2 usually subdivided into

median and paired marginal plates (Fig. 9i), rarely

undivided Latreille, 1806

9. Tergites of abdominal somites 3-5 with only spinulose or

spiniform nodules calcified (Fig. 9e) in males; females

with lateral plates of left side well delineated; antennal aci-

cle usually absent

NeoUthodes A. Milne-Edwards and Bouvier, 1894

— Tergites of abdominal somites 3-5 with lateral plates

clearly delineated in both sexes, median plate with nodular

calcification, accessory marginal plates well developed

(Figs 9h, i); antennal acicle present

Paralithodes Brandt, 1848

Illustrated keys to the families and genera of Paguroidea

115

10. Tergite of abdominal somite 2 subdivided into 3-5 well

calcified plates (Figs 9 e, f, h, i) 11

— Tergite of abdominal somite 2 undivided (Figs 9g, j, k) . .

11. Tergite of abdominal somite 2 subdivided into 3 plates

(median and paired laterals) (Fig. 9f)

Phyllolithodes Brandt, 1848

— Tergite of abdominal somite 2 subdivided into 5 plates

(median, paired lateral and marginal) (Figs 9e, h )

Rhinolithodes Brandt, 1848

12. Rostral process thick, non-spiniform, hammer-shaped (Fig.

Ij); antennal acicle small, rudimentary; tergites of abdom-

inal somites 4 and 5 with median plates irregularly

calcified Sculptolithodes Makarov, 1934

— Rostral process more or less spiniform; antennal acicle

well-developed; tergites of abdominal somites 4 and 5

with median plates regularly and entirely calcified (Figs 9f,

g,j,k) 13

13. Rostral process formed by anterior process (basal spine)

and dorsal spine or granule (Fig. 8g)

Glyptholithodes Faxon, 1895

— Rostral process formed by anterior process (basal spine)

and at least 1 pair of dorsal spines (Fig. 8f) 14

14. Lateral tergal plates of abdominal somite 3 entire (Figs 9f,

j); antennal acicle moderately spinulose; walking leg 3

always equal to or longer than carapace width

Paralomis White, 1856

— Lateral tergal plates of abdominal somite 3 each with small

accessory plates sundered anteromedially (Figs 9g, k);

antennal acicle extremely spinulose; walking leg 3 never

equal to or longer than carapace width

Lopholithodes Brandt, 1848

Pylojacquesidae

Pylojacquesia McLaughlin and Lemaitre, 2001c

See figs 2d, 1, 3j, 5w, 7i.

Key to genera of Paguridae

1. Gill formula includes 3 well developed or reduced pleuro-

branchs, 1 each on somites XI-XIII (thoracomeres 5-7,

above pereopods 2-4) (Fig. 4b) 2

— Gill formula includes fewer than 3 pleurobranchs

(Figs 4c, d) 10

2. Pleurobranchs on somites XI and XII (thoracomeres 5 and

6, above pereopods 2 and 3) reduced, rudimentary or

vestigial 3

— Pleurobranchs on somites XI and XII (thoracomeres 5 and

6, above pereopods 2 and 3) well developed 4

3. Chelipeds markedly unequal; female with paired

gonopores on coxae of pereopod 3 (Fig. 2m)

. . . Propagurus McLaughlin and de Saint Laurent, 1998

— Chelipeds subequal; female with single gonopore on coxa

of left pereopod 3 Chanopagurus Lemaitre, 2003

4. No unpaired pleopods in males; tergite of abdominal

somite 6 strongly calcified 5

— Some unpaired pleopods in males; tergite of abdominal

somite 6 not strongly calcified 6

5. Chela of right cheliped with large spine at base of dactyl

(Fig. 6j); males with paired, modified pleopods land 2;

abdominal tergite 6 operculate (Fig. 8d)

Xylopagurus A. Milne-Edwards, 1880

— Chela of right cheliped without large spine at base of

dactyl; males without paired, modified pleopod 1;

abdominal tergite 6 not operculate

Lithopagurus Provenzano, 1968

6. Males with (Fig. 7a) or without at least 1 pair of modified

pleopods; females with or without pleopod 1 paired,

modified 7

— Males with no pleopods paired, modified; females with

pleopod 1 paired, modified (Figs 7b, c) 9

7. Males with pleopod 2 paired, modified

Tomopaguroides Balss, 1912

— Males without pleopod 2 paired, modified 8

8. Right cheliped much larger than left, with massive chela

(Fig. 6k) Bathypaguropsis McLaughlin, 1994

— Right cheliped only slightly larger than left, chela not

massive Tomopaguropsis Alcock, 1905

9. Right cheliped with dactyl opening obliquely (Fig. 6h);

pereopod 4 semichelate (Figs 5n, p, r, s, v); protopods of

uropods without elongate spine

Pylopaguwpsis Alcock, 1905

— Right cheliped with dactyl opening horizontally (Fig. 6f);

pereopod 4 not semichelate; protopods of uropods each

with elongate spine (Fig. 5j)

Munidopagurus A. Milne-Edwards, 1880

10. Pleurobranch present on somite XII (thoracomere 7, above

pereopod 4) (Eig. 4d) 11

— No pleurobranch present above pereopod 4 70

11. Arthrobranchs well developed on maxilliped 3 (Eigs 4a,

b, d) 12

— Arthrobranchs rudimentary, vestigial or absent on

maxilliped 3 (Eig. 4c) 74

12. Gill structure distally or deeply quadriserial (Eigs 4g, h) .

— Gill structure biseiial (Eig. 4f) 21

13. Crista dentata of maxilliped 3 with 1 or more accessory

teeth (Eigs 2c, f) 14

— Crista dentata of maxilliped 3 without accessory tooth

(Eigs 2b, d, e) 19

14. Chelipeds subequal (Eig. If, q) 15

— Chelipeds distinctly unequal, right largest (Eigs li-p) . . .

15. Eemales with paired, modified pleopod 1 (Eigs 7b, c) ...

Michelopagurus McLaughlin, 1997

— Eemales without paired, modified pleopod 1 16

16. Rostrum triangular; ventral margins of dactyls of

ambulatory legs each with row of corneous spinules ....

Pagurodes Henderson, 1888

— Rostrum broadly rounded; ventral margins of dactyls of

ambulatory legs each with row of long stiff bristles ....

Pseudopagurodes McLaughlin, 1997

17. Males with short (1-2 coxal lengths) left sexual tube

(Eigs 7m-o, q); females with paired, modified pleopod 1

(Figs 7b, c) Tarrasopagurus McLaughlin, 1997

116

P.A. McLaughlin

— Males with medium (>2-5 coxal lengths) to long (>5 coxal

lengths) right sexual tube (Figs 7h, j- m); females without

paired, modified pleopod 1 18

18. Male right sexual tube directed across body ventrally from

right to left (Figs 7j, k, m); female with paired gonopores

(Fig. 2m) Cestopagurus Bouvier, 1897

— Male right sexual tube directed toward exterior (Figs 7h, i,

1); female with single left gonopore

Trichopagurus de Saint Laurent, 1968

19. Chelipeds subequal, right stronger, but not appreciable

longer . Jridopagurus de Saint Laurent-Dechance, 1966a

— Chelipeds distinctly unequal; right usually appreciably

longer 20

20. Male with very short (<1 coxal length) to short (1-2 coxal

lengths) left sexual tube (Figs 7h-o, q); female with paired,

modified pleopod 1 (Figs 7b, c)

Pagurojacquesia de Saint Laurent and McLaughlin, 2000

— Male with moderate (>2-5 coxal lengths) to long

(>5 coxal lengths) left sexual tube (Fig. 7p); female

without paired, modified pleopod 1

Turleania McLaughlin, 1997

21. Lateral margins of shield each developed into pair of blunt

or spiniform, wing-like processes (Fig. 3k)

Porcellanopagums Filhol, 1885a

— Lateral margins of shield not developed into pak of blunt

or spiniform, wing-like projections 22

22. Males with very short (<1 coxal length) to long sexual

tube(s) (>5 coxal lengths) (Figs 7h-q) 23

— Males without sexual tube(s) (Figs 7r, s) 45

23. Females with paired, modified pleopod 1 (Figs 7b, c) . 24

— Females without paired, modified pleopod 1 25

24. Carpus of right cheliped strongly produced ventrally (Fig.

6o); uropods asymmetrical

Goreopagurus McLaughlin, 1988

— Carpus of right cheliped not strongly produced ventrally;

uropods symmetrical or nearly so (Fig. 8j)

Pylopagurus A. Milne-Edwards and Bouvier, 1891 (part)

25. Distinct male sexual tube produced from gonopore on only

1 coxa (Fig. 7o, p), papilla present or absent from opposite

gonopore 26

— Distinct male sexual tubes produced from gonopores on

both coxae (Figs 7h-n, q) 37

26. Males with left sexual tube 27

— Males with right sexual tube 31

27. Right chela markedly larger than left 28

— Right chela not markedly larger than left

Spiwpaguriis Stimpson, 1858

28. Telson with transverse indentation (Figs 5b, c, f-i); male

with paired gonopores (Figs 21, m) 29

— Telson without transverse indentation (Figs 5d, e, J, k);

male sometimes without right gonopore (Fig. 7p)

Micropagurus McLaughlin, 1986

29. Telson with terminal margin(s) unarmed (Figs 5e, i, j) 30

— Telson with terminal margin(s) armed with spines (Figs 5d,

f, g, k) Anapagurus Henderson, 1886

30. Telson with terminal margin entire (Figs 5d, e); ocular

peduncles with corneas strongly dilated (Fig. 3m)

Forestopagurus Garcia-Gomez, 1994

— Telson with terminal margin marked by prominent median

cleft (Figs 5b, c, f-i); ocular peduncles with corneas

reduced Pygmaeopagurus McLaughlin, 1986

31. Females with paired gonopores 32

— Females with single gonopore on coxa of left pereopod 3

Anapagrides de Saint Laurent-Dechance, 1966b (part)

32. Males with 3 or fewer unpaired pleopods 33

— Males with 4 unpaired pleopods

Acanthopagurus de Saint Laurent, 1968 (part)

33. Sexual tube very short (<1 coxal length) to moderate (>2-5

coxal lengths) 34

— Sexual tube long (>5 coxal lengths) 35

34. Rostral lobe broadly rounded; pereopod 4 with single row

of corneous scales in propodal rasp (Figs 5p, q, u); sexual

tube of moderate length, directed toward exterior

Catapagurus A. Milne-Edwards, 1880

— Rostral lobe triangular; pereopod 4 with 2 or more rows of

corneous scales in propodal rasp (Eigs 5n, r, s, v); sexual

tube short or very short, directed anteriorly or posteriorly

Parapagurodes McLaughlin and Haig, 1973 (part)

35. Right sexual tube directed toward exterior and upward

across dorsal body surface . . .Hemipagurus Smith, 1881

— Right sexual tube directed toward exterior, but not over

dorsal body surface (Eigs 7i, 1) 36

36. Sexual tube terminating in elongate filament (Eig. 7h) . . .

Nematopaguroides Eorest and de Saint Laurent, 1968

(part)

— Sexual tube not terminating in elongate filament

Solenopagurus de Saint Laurent, 1968

37. Abdomen reduced (Eigs li, 1, n-p); males without paired or

unpaired pleopods; females only with unpaired uniramous

pleopods 2-4 38

— Abdomen well developed (Eigs ld-g,m); males usually

with some unpaired pleopods; females with unpaired

biramous pleopods 2-4, usually also with reduced pleopod

5 39

38. Rostrum developed as prominent slender spine; pereopod

5 subchelate (Eigs 5w, x)

Alainopagurus Lemaitre and McLaughlin, 1995

— Rostrum broad, blunt or subacute, upturned; pereopod 5

weakly chelate (Eig. 5y)

Alainopaguroides McLaughlin, 1997

39. Eemales with paked, modified pleopod 1

. . Nematopagurus A. Milne-Edwards and Bouvier, 1892

— Eemales without paired, modified pleopod 1 40

40. Right sexual tube very short (<1 coxal length) to short (1-2

coxal lengths) 41

— Right sexual tube long (>5 coxal lengths)

.Nematopaguroides pusillus Eorest and de Saint Laurent,

1968

41. Antennal acicles each with row of spines (Eigs 8b, c, 1) . .

Alloeopagurodes Komai, 1998

— Antennal acicles without row of spines 42

42. Propodal rasp of pereopod 4 with 2 or more rows of

corneous scales (Eigs 5r, s, v)

Parapagurodes McLaughlin and Haig, 1973 (part)

— Propodal rasp of pereopod 4 with 1 row of corneous scales

(Pigs 5o, p, q) 43

Illustrated keys to the families and genera of Paguroidea

117

43. Lateral projections prominently produced; telson with

rounded posterior lobes, each armed with few long, slen-

der, corneous spines (Fig. 5g)

Icelopa gurus McLaughlin, 1997

— Lateral projections not prominently produced; telson with

obtusely subtriangular posterior lobes, each armed with

few minute spinules 44

44. Coxa of right pereopod 5 in males with short sexual tube,

coxa of left pereopod 5 usually without papilla; females

with paired gonopores

Acanthopagurus de Saint Laurent, 1968 (part)

— Coxa of right pereopod 5 in males with very short sexual

tube, coxa of left pereopod 5 with or without papilla;

females with single left gonopore

Anapagrides de Saint Laurent-Dechance, 1966 (part)

45. Females with paired, modified pleopod 1 46

— Females without paired, modified pleopod 1 60

46. Abdomen reduced; males without unpaired pleopods;

females with unpaired pleopods 2-4

Protoniopagurus Lemaitre and McLaughlin, 1996

— Abdomen not reduced; males with some unpaired

pleopods; females with unpaired pleopods 2-5 47

47. Right cheliped markedly elongate

Ceratopagurus Yokoya, 1933

— Right cheliped not markedly elongate 48

48. Protopods of uropods prominently produced posteriorly

(Fig. 5j); dorsal surface of right chela commonly with

characteristic covering of mushroom-shaped tubercles . .

Agaricochirus McLaughlin, 1981

— Protopods of uropods not prominently produced posterior-

ly; dorsal surface of right chela usually without character-

istic covering of mushroom- shaped tubercles 49

49. Spines on dorsal surfaces of chelae with basal rosettes

(Fig. 6m) Rhodochirus McLaughlin, 1981

— Spines on dorsal surfaces of chelae without basal rosettes

50. Propodal rasp of pereopod 4 with more than one row of

corneous scales (Figs 5r, s, v) 51

— Propodal rasp of pereopod 4 with one row of corneous

scales (Figs 5p, q, u) 53

51. Left chela triangular or subtriangular in cross-section,

dactyl and fixed finger not dorsoventrally flattened . . 52

— Left chela not triangular or subtriangular in cross-section,

dactyl and fixed finger dorsoventrally flattened

Manucomplanus McLaughlin, 1981

52. Telson with lateral indentations suggesting division into

anterior and posterior portions (Figs 5b, f-i)

Anisopagurus McLaughlin, 1981

— Telson without lateral indentations suggesting division into

anterior and posterior portions (Figs 5d, e)

Enallopaguropsis McLaughlin, 1981

53. Ocular acicles simple (Figs 3a, m, 8a); coxae of male

pereopods 5 symmetrical 54

— Ocular acicles multispinose (Fig 8e); coxae of male

pereopods 5 asymmetrical

Pylopaguridum McLaughlin and Lemaitre, 2001b

54. Telson with lateral indentations suggesting division into

anterior and posterior portions (Figs 5b, f-i) 55

— Telson without lateral indentations suggesting division into

anterior and posterior portions (Figs 5d, e)

Enallopagurus McLaughlin, 1981

55. Chela of right cheliped subovate to subcircular, margins

unarmed, weakly tuberculate or minutely crenulate and/or

serrate, but never armed with prominent, blunt or acute

spines (Figs 6i, o) 56

— Chela of right cheliped variable, margins armed with

prominent, blunt or acute spines or tubercles (Figs 61, m)

56. Pereopod 4 with large, very prominent pre ungual process

at base of claw (Fig. 5p, s, u)

Phimochirus McLaughlin, 1981

— Pereopod 4 without large, very prominent preungual

process at base of claw (Figs 5o, q, r)

Pylopagurus A. Milne-Edwards and Bouvier, 1891 (part)

57. Dactyl and fixed finger of left chela excavated ventrally,

spoon- shaped

Tomopagurus A. Milne-Edwards and Bouvier, 1893 (part)

— Dactyl and fixed finger of left chela not excavated

ventrally, not spoon-shaped 58

58. Right chela circumscribed by row of dorsomesial, dorso-

proximal and dorsolateral marginal spines (Eig. 61); left

cheliped with rotation of propodal-carpal articulation 45 °-

90° from horizontal plane

Lophopagurus {Australeremus) McLaughlin, 1981

— Right chela not circumscribed by row of dorsomesial,

dorsoproximal and dorsolateral marginal spines; left

cheliped with rotation of propodal-carpal articulation

much less than 45° from horizontal plane 59

59. Left chela with midline elevated into prominent keel or

crest (Eig. 6n)

Lophopagurus (Lophopagurus) McLaughlin, 1981

— Left chela with midline sometimes elevated, but not into

prominent keel or crest Haigia McLaughlin, 1981

60. Antennal peduncle with prominent, hooked spine at lat-

erodistal margin of segment 1 (Eig. 8k)

Tomopagurus wassi McLaughlin, 1981

— Antennal peduncle without prominent, hooked spine at lat-

erodistal margin of segment 1 61

61. Ultimate segment of antennular peduncles with very long

seta provided with long paired setules (Eig. 2i); abdomen

elongate, generally straight

Pagurus imafukui McLaughlin and Konishi, 1994

— Ultimate segment of antennular peduncles without very

long seta provided with long paired setules; abdomen

variable 62

62. Coxae of male pereopod 5 asymmetrical (Eigs 7s, t) . 63

— Coxae of male pereopod 5 generally symmetrical (Eigs

2m, 7r) 64

63. Male with 3 unpaired pleopods; coxa of right pereopod 5

produced, gonopore masked by tuft of long, stiff setae

(Eig. 7s) Pagurixus Melin, 1939

— Male without pleopods; coxa of left pereopod 5 produced,

gonopore masked by tuft of long, stiff setae (Eig. 7t) ...

Paguridium Eorest, 1961

64. Males with both coxae of pereopod 5 produced, gonopores

each masked by tuft of long, stiff setae; telson with

118

P.A. McLaughlin

markedly concave terminal margin, outer angles acute,

with extremely prominent pair of spines adjacent to

median cleft (Fig. 5h)

Diacanthums McLaughlin and Forest, 1997

— Males without coxae of pereopods 5 produced; telson

without markedly concave terminal margin, outer angles

variable, without extremely prominent pair of spines

adjacent to median cleft 65

65. Telson with distinct transverse indentation (Figs 5b,c, f-i)

— Telson without distinct transverse indentation (Figs 5d,

e, j) Discorsopagums McLaughlin, 1974

66. Posterior portion of cephalothorax, at least in part calcified

(Fig. 11); abdomen reduced Labidochirus Benedict, 1892

— Posterior portion of cephalothorax membranous; abdomen

well developed (Figs Id-g, m) 67

67. Left chela with pronounced counterclockwise torsion;

pereopods 4 each with prominent circular “type A P4 struc-

ture” on lateral face of dactyl (Fig. 5v)

Elassochirus Benedict, 1892

— Left chela without pronounced counterclockwise torsion;

pereopod 4 without prominent circular “type A P4

structure” on lateral face of dactyl 68

68. Uropods generally asymmetrical; abdomen spirally flexed

Pagurus Fabricius, 1775

— Uropods generally symmetrical; abdomen not spirally

flexed 69

69. Males with 3 unpaired pleopods; females with 4 unpaired

pleopods Orthopagurus Stevens, 1927

— Males without unpaired pleopods; females with 3 unpaired

pleopods Paguritta Melin, 1939

70. Crista dentata with 3 or 4 very large, widely-spaced spine-

like teeth (Fig. 2g)

Scopaeopagums McLaughlin and Hogarth, 1998

— Crista dentata well developed or reduced, but never with

only 3 or 4 widely-spaced spine-like teeth 71

71. Ambulatory dactyls paddle-shaped (Fig. In); females with

paired gonopores; males with right sexual tube

Ostraconotus A. Milne-Edwards, 1880

— Ambulatory dactyls not paddle-shaped; females with sin-

gle left gonopore; males with pair of sexual tubes ... 72

72. Lateral margins of shield not drawn out into 3 prominent

lobes; males with some unpaired pleopods; females with-

out paired, modified pleopod 1 73

— Shield with lateral margins each drawn out into 3 promi-

nent lobes (Fig. 31); males without unpaired pleopods;

females with paired, modified pleopod 1

Solitariopagurus Tiirkay, 1986

73. Males with 3 unpaired pleopods; left sexual tube partially

obscured by tufts of setae

. . .Catapaguroides A. Milne-Edwards and Bouvier, 1892

— Males with 4 unpaired pleopods

Decaphyllus de Saint Laurent, 1968

74. Rostrum strongly deflected downward, with prominent

epu'ostral spine (Fig. 8i)

Enneophyllus McLaughlin, 1997

— Rostrum not strongly deflected downward, without

prominent epirostral spine 75

75. Male sexual tube with terminal fringe of dense curved

setae; no preungual process at base of claw of pereopod 4

Enneopagurus McLaughlin, 1997

— Male sexual tube without terminal fringe of dense curved

setae; preungual process developed at base of claw of pere-

opod 4 Enneobranchus Garcia-Gomez, 1988

Key to genera of Parapaguridae

1. Corneas present 2

— Corneas absent (Fig. 81)

Typhlopagurus de Saint Laurent, 1972

2. Rostrum short, not exceeding ocular peduncles 3

— Rostrum long, often exceeding ocular peduncles (Fig. Iq)

Probeebei Boone, 1926

3. Ocular acicles distinctly developed (Figs 8a-c, e, 1) ... 4

— Ocular acicles weakly developed or obsolete (Fig. Ip)

Tylaspis Henderson, 1885

4. Posterior carapace mostly membranous; unpaired left

pleopods 3-5 5

— Posterior carapace calcified; asymmetrically paired

pleopods 3-5 Bivalvopagurus Lemaitre, 1993

5. Shield about as broad or broader than long; rostrum

bluntly triangular or broadly rounded; abdomen flexed . 6

— Shield distinctly longer than broad; rostrum acutely

triangular; abdomen straight

Tsunogaipagurus Osawa, 1995

6. Shield distinctly broader than long; dactyls of ambulatory

legs straight or nearly so; corneas strongly dilated (Fig.

3m); pleopod 2 of male with short exopod and strongly

twisted distal segment (Fig. 7e)

Strobopagurus Lemaitre, 1989

— Shield about as broad as long; dactyls of ambulatory legs

curved; corneas moderately or weakly dilated; pleopod 2

of male lacking exopod and distal segment not twisted

(Fig. If) (rarely absent) 7

7. Vestigial pleurobranch present on each side of somite XIV

(thoracomere 8, above pereopod 5) (Fig. 4e)

Sympagurus Smith, 1883

— Vestigial pleurobranch absent on each side of somite XIV

(thoracomere 8, above pereopod 5) 8

8. Epistomial spine straight (Fig. 8m) or absent 9

— Epistomial spine strongly curved upward

Oncopagurus Lemaitre, 1996

9. Gill structure hi- or quadriserial (Figs 4f-h); segment 4

of antennal peduncle armed with dorsodistal spine;

length of ocular peduncles, including corneas, at least half

length of shield Paragiopa gurus Lemaitre, 1996

— Gill structure quadriserial (Figs 4g, h); segment 4 of anten-

nal peduncle unarmed; length of ocular peduncles, includ-

ing corneas, less than half length of shield (except

P arapagurus bouvieri SiQhhing, 1910)

Parapagurus Smith, 1879

Illustrated keys to the families and genera of Paguroidea

119

Paguridae Latreille, 1802

In the abbreviated generic diagnoses presented, characters

common to the family are not repeated. Statements simply of

pleopod number refer to the unpaired left pleopods. The

expression “distally divided” (formerly “intermediate”) is used

to indicate gill lamellae (Fig. 4g) that while not deeply or

completely subdivided, do show partial distal cleavage or

distinct indentations. Genera are arranged in alphabetical

order.

Diagnosis. Cephalothorax usually with only shield weakly to

strongly calcified; rostrum produced as median projection or

rounded lobe; lateral projections usually well developed. Gills

bi- or quadriserial phyllobranchia, 8-13 pairs. Ocular pedun-

cles with penultimate segments each provided with acicle.

Antennal acicles most commonly with only terminal spine.

Maxillipeds 3 separated by moderate to broad sternal plate;

ischium usually with well developed crista dentata, sometimes

reduced, with or without 1 or more accessory teeth. Chelipeds

unequal or subequal, right generally larger. Ambulatory legs

with dactyls and propodi usually similar from right to left,

occasionally dissimilar; dactyls usually with ventral row of cor-

neous spines; carpi usually armed with at least dorsodistal

spine. Pereopod 4 usually semichelate, sometimes subchelate,

infrequently chelate or simple; preungual process present or

absent at base of claw; rarely circular sensory structure (type A

P4 structure, cf. McLaughlin, 1974) on lateral face of dactyl.

Fifth pereopods usually chelate, occasionally subchelate.

Males usually with paired gonopores on coxae of pereopod 5,

occasionally only with single left gonopore; membranous,

chitinous, or very weakly calcified sexual tube frequently

developed in conjunction with gonopore on one or both coxae;

usually without, but occasionally with pleopods 1 and/or 2

paired and modified; with or without unpaired left pleopods on

abdominal somites 3-5 or 2-5. Females usually with paired

gonopores on coxae of pereopod 3, occasionally only single left

gonopore; often without, but frequently with, pleopod 1 paired

and modified; with unpaired left pleopods on somites 2-5, or

less frequently, 2-4. Uropods usually asymmetrical, occasion-

ally symmetrical. Telson usually with lateral indentations

separating anterior and posterior portions; posterior lobes

usually separated by median cleft. Type genus: Pagurus

Fabricius, 1775.

Acanthopagurus de Saint Laurent, 1968

Diagnosis. Gills biserial, 11 pairs. Rostrum obtusely and round-

ly triangular. Ocular acicles simple. Crista dentata with 1 acces-

sory tooth. Right cheliped much stronger than left. Sternite of

somite XII (thoracomere 6, pereopods 3) with subsemicircular

anterior lobe. Pereopod 4 semichelate; propodal rasp with 1

row of corneous scales; no preungual process. Male with short,

massive sexual tube on right coxa of pereopod 5, directed

obliquely toward midline; left coxa without sexual tube, or pos-

sibly with small papilla protruding from gonopore; pleopods

3-5. Female with pleopods 2-5. Telson with terminal margins

oblique. Type species: Anapagurus ?dubius A. Milne-Edwards

and Bouvier, 1900.

Agaricochirus McLaughlin, 1981

Diagnosis. Gills biserial, 11 pairs. Rostrum obtusely triangular.

Ocular acicles simple. Crista dentata with 1 accessory tooth.

Right chela generally ovate, armature usually as mushroom-

shaped tubercles. Carpi of ambulatory legs lacking dorsodistal

spine. Sternite of somite XII (thoracomere 6, pereopods 3) with

anterior lobe absent, reduced and styliform, or small and sub-

quadrate. Pereopod 4 semichelate; propodal rasp with several

rows of corneous scales; preungual process small. Coxae of

male pereopods 5 occasionally with slight papilla protruding

from one or both gonopores; pleopods 3-5. Female with paired,

modified pleopod 1; pleopods 2-5. Uropods symmetrical or

nearly so, protopods produced posteriorly. Telson with median

cleft usually broadly U-shaped, posterior lobes usually sym-

metrical, terminal margins unarmed. Type species;

Pylopagurus boletifer A. Milne-Edwards and Bouvier, 1893.

Alainopaguroides McLaughlin, 1997

Diagnosis. Gills biserial, 11 pairs. Anterior carapace vaulted

and generally well calcified, with anterolateral regions slightly

depressed. Rostrum obtusely triangular. Ocular acicles simple.

Crista dentata somewhat reduced, 1 accessory tooth. Chelipeds

subequal; right stronger, but not necessarily longer. Sternite of

somite XII (thoracomere 6, pereopods 3) with narrow, trans-

verse anterior lobe. Pereopod 4 weakly semichelate, propodal

rasp rudimentary; prominent tubular preungual process.

Abdomen reduced; tergal plates of somites 2-5 sometimes very

faintly delineated. Male with moderate, stout sexual tube on

coxa of right pereopod 5, left often with very short tube; no

unpaired pleopods. Female pleopods 2-4. Uropods gener-

ally symmetrical. Telson with terminal margins narrowly to

broadly oblique. Type species: Alainopaguroides lemaitrei

McLaughlin, 1997.

Alainopagurus Lemaitre and McLaughlin, 1995

Diagnosis. Gills biserial, 11 pairs. Anterior carapace vaulted

and generally well calcified, with anterolateral regions distinct-

ly globular. Ocular acicles multispinose. Crista dentata with 1

accessory tooth. Right cheliped stronger, but not markedly

longer. Sternite of somite XII (thoracomere 6, pereopods 3)

with narrow, transverse anterior lobe. Pereopod 4 subchelate,

propodal rasp with 1 row of corneous spines; no preungual

process. Pereopod 5 subchelate. Male with stout, moderate sex-

ual tubes of approximately equal length on coxae of both pere-

opods 5, each with long setae mesially and terminally; no

unpaired pleopods. Female with single gonopore opening pos-

teriorly on coxa of left pereopod 3; pleopods 2-4 only.

Abdomen reduced; tergal plate of somite 2 weakly delineated;

tergal plates of somites 3-5 clearly defined, chitinous or very

weakly calcified. Uropods symmetrical. Telson with terminal

margin entire. Type species: Alainopagurus crosnieri Lemaitre

and McLaughlin, 1995.

Alloeopagurodes Komai, 1998

Diagnosis. Gills biserial, 11 pairs. Ocular acicles simple.

Rostrum prominent, lateral projections reduced. Antennal

120

P.A. McLaughlin

acicles each with row of spines on mesial surface. Crista den-

tata with 1 accessory tooth. Right cheliped elongate in large

males. Sternite of somite XII (thoracomere 6, pereopods 3)

with subrectangular anterior lobe, margin spinose. Pereopod 4

semichelate; propodal rasp with 1 row of corneous scales; no

preungual process. Right coxa of pereopod 5 in male with

short, mesially directed sexual tube; coxa of left with very short

sexual tube; pleopods 3-5. Female with pleopods 2-5. Telson

with terminal margins rounded. Type species: Alloeopagurod.es

spiniacicula Komai, 1998.

Anapagrides de Saint Laurent-Dechance, 1966

Diagnosis. Gills biserial, 11 pairs. Rostrum triangular. Ocular

acicles simple. Crista dentata with 1 accessory tooth. Chelipeds

unequal; right appreciably larger. Sternite of somite XII (thora-

comere 6, pereopods 3) with anterior lobe subrectangular to

subcircular. Pereopod 4 semichelate, propodal rasp with 1 row

of corneous scales. Male with short, posteriorly directed sexu-

al tube on right coxa of pereopod 5; pleopods 3-5. Female with

single gonopore on coxa of left pereopod 3; pleopods 2-5.

Telson with terminal margins straight to oblique. Type species:

Eupagurus (Spiropagurus) facetiis Melin, 1939.

Anapagurus Henderson, 1886

Diagnosis. Gills biserial, 11 pairs. Rostrum as rounded lobe.

Ocular acicles simple; ocular lobes unarmed or with pair of

spines. Crista dentata with 1 accessory tooth. Chelipeds gross-

ly unequal, right much larger. Sternite of somite XII (thora-

comere 6, pereopods 3) with subrectangular anterior lobe.

Pereopod 4 semichelate; propodal rasp with 1 row of corneous

scales; no preungual process. Coxa of left pereopod 5 in male

with short to moderate sexual tube directed toward exterior and

often curved over abdomen dorsally; coxa of right sometimes

with short sexual tube; pleopods 3-5. Females with pleopods

2-5. Telson with terminal margins generally oblique. Type

species: Pagurus laevis Bell, 1846.

Anisopagurus McLaughlin, 1981

Diagnosis. Gills biserial, 11 pairs. Rostrum well developed or

reduced to rounded lobe. Ocular acicles simple or multispinose.

Crista dentata with 1 accessory tooth. Right chela usually sub-

operculate. Left cheliped with propodal-carpal articulation

rotated 0-45° from perpendicular. Sternite of somite XII (tho-

racomere 6, pereopods 3) with subrectangular to subtriangular

anterior lobe. Pereopod 4 semichelate; propodal rasp with 3 or

4 rows of corneous scales; preungual process usually moder-

ately well developed. Males with pleopods 3-5. Females with

pleopod 1 paired, modified; pleopods 2-5. Telson with terminal

margins rounded, sometimes somewhat excavated. Type

species: Pylopagurus bartletti A. Milne-Edwards, 1880

Bathypaguropsis McLaughlin, 1994

Diagnosis. Gills quadriserial, 13 pairs. Rostrum well devel-

oped. Ocular acicles simple. Crista dentata with 1 accessory

tooth. Right cheliped massive, chela operculate or nearly so;

propodal-carpal articulation approximately 30° from perpendi-

cular; left cheliped with propodal-carpal articulation with

30-60° counterclockwise rotation. Sternite of somite XII

(thoracomere 6, pereopods 3) with subrectangular anterior lobe.

Pereopod 4 semichelate; propodal rasp of lor more, sometimes

incomplete, rows of corneous scales; no preungual process.

Male with pleopods 2-5. Female with pleopods 2-5. Telson

with terminal margins oblique. Type species: Bathypaguropsis

yaldwyni McLaughlin, 1994.

Catapaguroides A. Milne-Edwards and Bouvier, 1892

Diagnosis. Gills biserial, 10 pairs, no pleurobranch on somite

XIII (thoracomere 7, above arthrobranchs of pereopod 4).

Rostrum as rounded lobe. Ocular acicles simple. Crista dentata

more or less reduced, no accessory tooth. Chelipeds unequal,

right appreciably stronger. Sternite of somite XII (thoracomere

6, pereopods 3) with roundly rectangular anterior lobe.

Pereopod 4 semichelate; propodal rasp with 1 row of corneous

scales; no preungual process. Pereopod 5 semichelate. Male

with moderate to long sexual tube on coxa of right pereopod 5,

directed from right to left under thorax and recurved anteriorly;

coxa of left with very short or short tube concealed between 2

thick tufts of sternal setae; pleopods 3-5. Female with single

gonopore on coxa of left pereopod 3; pleopods 2-5. Telson with

terminal margins straight or oblique. Type species:

Catapaguroides microps A. Milne-Edwards and Bouvier, 1892.

Catapagurus A. Milne-Edwards, 1880

Diagnosis. Gills biserial, 11 pairs. Rostrum as broadly rounded

lobe. Ocular acicles simple. Crista dentata somewhat reduced,

with 1 accessory tooth. Chelipeds elongate, unequal, right

stouter than left. Sternite of somite XII (thoracomere 6, pere-

opods 3) with subrectangular anterior lobe. Pereopod 4 semi-

chelate; propodal rasp with 1 row of corneous scales; preungual

process prominent. Coxa of right pereopod 5 of male with mod-

erate sexual tube, curving toward exterior over lateral side of

abdomen, left coxa occasionally with very slightly protruded

papilla; pleopods 3-5. Female with pleopods 2-4 or 2-5.

Telson with terminal margins oblique. Type species:

Catapagurus sharreri A. Milne-Edwards, 1880. (Generic

diagnosis restricted by Asakura, 2001)

Ceratopagurus Yokoya, 1933

Diagnosis. Gills biserial, 11 pairs. Rostrum as broadly rounded

lobe. Ocular acicles simple. Crista dentata with 1 accessory

tooth. Chelipeds subequal, similar, moderately long and slen-

der. Sternite of somite XII (thoracomere 6, pereopods 3) not

known. Pereopod 4 semichelate; propodal rasp with several

rows of corneous scales. Male with pleopods 3-5. Female with

pleopod 1 paired, modified; pleopods 2-5. Telson unknown.

Type species: Ceratopagurus pilosimanus Yokoya, 1933.

Cestopagurus Bouvier, 1897

Diagnosis. Gills distally quadriserial, 11 pairs. Rostrum promi-

nent, acutely triangular. Ocular acicles simple. Crista dentata

Illustrated keys to the families and genera of Paguroidea

121

with 1 accessory tooth. Chelipeds very unequal; right much

stronger and distinctly sexually dimorphic. Sternite of somite

Xll (thoracomere 6, pereopods 3) with roundly rectangular

anterior lobe. Pereopod 4 semichelate; propodal rasp with 1

row of corneous scales; no preungual process. Male with long

sexual tube on right coxa of pereopod 5, orientated toward left

across ventral body surface; left coxa without gonopore, or

with gonopore and very short sexual tube directed toward right;

pleopods 3-5. Female with pleopods 2-5. Telson with terminal

margins horizontal to oblique. Type species: Cestopagurus

coMt/en Bouvier, 1897.

Chanopagurus Lemaitre, 2003

Diagnosis. Gills quadriserial, 13 pairs (11 pairs presumably

functional), pleurobranchs of somites XI and XII (thora-

comeres 5 and 6, above pereopods 2 and 3) reduced or rudi-

mentary. Rostrum broadly rounded. Corneas reduced, located

ventrolaterally on ultimate peduncular segments. Ocular acicles

simple, basally contiguous. Crista dentata well developed, and

1 accessory tooth. Chelipeds subequal Sternite of somite XII

(thoracomere 6, pereopod 3) divided into anterior and posterior

lobes by distinct, membranous hinge. Pereopod 4 semichelate,

propodal rasp with 1-2 rows of corneous scales, no preungual

process. Male unknown. Female with single gonopore on coxa

of left pereopod 3; pleopod 1 paired, modified; pleopods 2-5.

Uropods asymmetrical. Telson symmetrical, with distinct

lateral indentations, posterior lobes each with “half-moon” con-

tour and blade-like lateral margin. Type species. Chanopagurus

atopos Lemaitre, 2003.

Decaphyllus de Saint Laurent, 1968

Diagnosis. Gills biserial, 8-10 pairs, no pleurobranchs on

somites XI, XII, XIII (thoracomeres 5-7, above pereopods

2-A), arthrobranchs of maxilliped 3 small, vestigial or absent.

Ocular acicles simple. Crista dentata reduced, no accessory

tooth. Chelipeds subequal in length, but right appreciably

stronger. Sternite of somite Xll (thoracomere 6, pereopods 3)

with subsemicircular or subovate anterior lobe. Pereopod 4

simple, without propodal rasp; no preungual process. Pereopod

5 semichelate. Male with long sexual tube developed on coxa

of right pereopod 5, directed from right to left across ventral

body surface and curved anteriorly; left with short sexual tube

directed from left to right; pleopods 2-5. Female with single

gonopore on coxa of left pereopod 3; pleopods 2-5. Telson

without lateral indentations; terminal margin entire or with

minute median cleft. Type species; Decaphyllus spinicornis de

Saint Laurent, 1968.

Diacanthurus McLaughlin and Forest, 1997

Diagnosis. Gills biserial, 11 pairs. Rostrum obsolete or as

broadly rounded lobe. Ocular acicles simple. Crista dentata

with 1 accessory tooth. Chelipeds unequal; left cheliped with

some degree of clockwise rotation of propodal-carpal articula-

tion, dorsolateral margin of chela weakly to strongly inflated

proximally. Sternite of somite Xll (thoracomere 6, pereopods

3) with subsemicircular anterior lobe. Pereopod 4 semichelate;

propodal rasp with several rows of corneous scales; no pre-

ungual process. Male with pleopods 3-5. Females with

pleopods 2-5. Telson with posterior lobes each contoured as

"half-moon"; blade-like lateral margin and acute terminal angle

broadly separated by U-shaped median cleft, inner margins

each with 1 prominent spine in basal half. Type species:

Eupagurus spinulimanus Miers, 1876.

Discorsopagums McLaughlin, 1974

Diagnosis. Gills biserial, 1 1 pairs. Rostrum obtusely triangular.

Ocular acicles simple. Crista dentata with 1 accessory tooth.

Chelipeds unequal, right larger. Sternite of somite XII (thora-

comere 6, pereopods 3) with semicircular anterior lobe.

Pereopod 4 semichelate; propodal rasp with multiple rows of

corneous scales; no preungual process. Male with or without

slight papilla protruding from gonopores on one or both coxae

of pereopods 5; pleopods 3-5 or 2-5. Female with pleopods

2-5. Abdomen straight or slightly flexed, not twisted; tergites

of somites 3-4 paired, incompletely fused chitinous plates; ter-

gite 6 strongly calcified. Uropods symmetrical. Telson with or

without slight lateral indentations; terminal margin entire,

straight or concave. Type species: Pylopagurus schmitti

Stevens, 1925.

Elassochirus Benedict, 1892

Diagnosis. Gills biserial, 11 pairs. Rostrum triangular. Ocular

acicles simple. Crista dentata with 1 accessory tooth. Chelipeds

unequal, right considerably larger, carpus often with wing-like

expansions; left with propodal-carpal rotation approximately

90° counterclockwise. Sternite of somite XII (thoracomere 6,

pereopods 3) with roundly rectangular to subsemiovate anter-

ior lobe. Pereopod 4 weakly semichelate; dactyl with circular

sensory structure on lateral face (Fig. 3v); propodal rasp with

several rows of corneous scales; no preungual process. Male

with pleopods 3-5, rarely only 3-4. Female with pleopods 2-5.

Telson with terminal margins oblique. Type species:

Bernhardus tenuimanus Dana, 1851.

Enallopaguropsis McLaughlin, 1981

Diagnosis. Gills biserial, 11 pairs. Rostrum triangular. Ocular

acicles simple. Crista dentata with 1 accessory tooth. Right

chela suboperculate; left cheliped with propodal -carpal rota-

tion of approximately 60° from perpendicular. Sternite of

somite Xll (thoracomere 6, pereopods 3) with anterior lobe as

single capsulate seta. Pereopod 4 semichelate; propodal rasp

with several rows of corneous scales; preungual process small

to moderately large. Male usually without sexual tubes, occa-

sionally with very short tube or papilla from one or both gono-

pores; with pleopods 3-5. Female with pleopod 1 paired, mod-

ified; pleopods 2-5. Abdomen straight or slightly flexed.

Telson without lateral indentations, terminal margin convex,

entire or with shallow median concavity. Type species:

Pylopagurus guatemoci Glassell, 1937.

122

P.A. McLaughlin

Enallopagurus McLaughlin, 1981

Diagnosis. Gills biserial, 11 pairs. Rostrum triangular. Ocular

acicles simple. Crista dentata with 1 accessory tooth. Right

chela subovate; left cheliped with propodal-carpal rotation of

15-30° from perpendicular. Stemite of somite Xll (thoracom-

ere 6, pereopods 3) with anterior lobe subcircular to sub-

quadrate. Pereopod 4 semichelate; propodal rasp with 1 row of

corneous scales; preungual process moderately small. Male

usually without sexual tubes, occasionally with very short tube

or papilla, most frequently on right coxa; with pleopods 3-5.

Female with pleopod 1 paired, modified; pleopods 2-5.

Abdomen straight or slightly flexed. Telson without lateral

indentations, terminal margin convex, entire or with incon-

spicuous median indentation. Type species: Pylopagurus

spinicarpus Glassell, 1938.

Enneobranchus Garcfa-Gomez, 1988

Diagnosis. Gills distally quadriserial, 9 pairs, pleurobranch on

somite XIII (thoracomere 7, above arthrobranchs of pereopod

4) but arthrobranchs absent from arthrodial membrane of max-

illiped 3. Rostrum as rounded lobe. Ocular acicles simple.

Crista dentata without accessory tooth. Chelipeds subequal,

right stronger. Sternite of somite XII (thoracomere 6, pereopods

3) with marginally armed, subrectangular anterior lobe.

Pereopod 4 simple; propodal rasp with 1 row of corneous

scales; preungual process prominent. Male with moderate to

long, coiled sexual tube on coxa of left pereopod 5; right coxa

sometimes with papilla or very short sexual tube; pleopods 3-5.

Female with pleopods 2-5. Telson with terminals straight or

oblique. Type species: Enneobranchus flavioculatus Garcia-

Gomez, 1988.

Enneopagurus McLaughlin, 1997

Diagnosis. Gills quadriserial; 9 pairs, pleurobranch on somite

XIII (thoracomere 7, above arthrobranchs of pereopod 4) but

arthrobranchs absent from arthrodial membranes of maxilliped

3. Rostrum triangular, not deflected. Ocular acicles simple.

Crista dentata without accessory tooth. Chelipeds subequal,

right more robust. Sternite of somite XII (thoracomere 6, pere-

opods 3) with subquadrate anterior lobe. Pereopod 4 semi-

chelate; propodal rasp with 1 row of scales; no preungual

process. Pereopod 5 semichelate. Coxa of left pereopod 5 of

male with moderate, rather stout sexual tube directed exter-

iorly and dorsally, terminally somewhat spatulate and with

fringe of dense curved setae; right occasionally with protruded

papilla; pleopods 3-5. Female with pleopods 2-5. Telson

with lateral indentations weakly indicated; terminal

margins oblique. Type species. Enneopagurus garciagomezi

McLaughlin, 1997.

Enneophyllus McLaughlin, 1997

Diagnosis. Biserial gills, 9 pairs, pleurobranch on somite XIII

(thoracomere 7, above arthrobranchs of pereopod 4) but arthro-

branchs absent from arthrodial membrane of maxilliped 3.

Rostrum well developed, strongly depressed. Ocular acicles

simple. Crista dentata somewhat reduced, without accessory

tooth. Chelipeds unequal, right appreciably larger. Stemite of

somite XII (thoracomere 6, pereopods 3) with small anterior

lobe. Pereopod 4 semichelate, propodal rasp with 1 row of cor-

neous scales; no preungual process. Pereopod 5 weakly semi-

chelate. Coxa of left pereopod 5 of male with long, basally

stout sexual tube directed exteriorly and curved dorsally across

abdomen from left to right; coxa of right without sexual tube;

pleopods 3-5. Female u nk nown. Abdomen straight. Telson

with very weak transverse indentations; terminal margins

oblique. Type species: Enneophyllus spinirostris McLaughlin,

1997.

Forestopagurus Garcfa-Gomez, 1994

Diagnosis. Gills biserial, 11 pairs. Rostrum as rounded lobe.

Ocular acicles simple. Crista dentata with 1 accessory tooth.

Chelipeds markedly unequal, right elongate in large males.

Stemite of somite XII (thoracomere 6, pereopod 3) with sub-

rectangular anterior lobe. Pereopod 4 semichelate; propodal

rasp with 1 row of corneous scales; no preungual process. Male

with moderate sexual tube on coxa of left pereopod 5; right

without sexual tube; no unpaired pleopods. Female with

pleopods 2-4. Telson with terminal margin entire. Type

species: Anapagurus drachi Forest, 1966.

Goreopagurus McLaughlin, 1988

Diagnosis. Gills biserial, 11 pairs. Rostmm obtusely triangular.

Ocular acicles simple. Crista dentata with 1 accessory tooth.

Chelipeds grossly unequal, right very elongate, with promi-

nently produced ventral carpal margin. Sternite of somite XII

(thoracomere 6, pereopods 3) with subovate to subrectangular

anterior lobe. Pereopod 4 semichelate; propodal rasp with 1

row of corneous scales; preungual process present or absent.

Male with short, posteriorly or laterally directed sexual tube on

coxa of right pereopod 5; left coxa often with papilla or very

short sexual tube; pleopods 3-5. Female with pleopod 1 paired,

modified; pleopods 2-5. Telson with terminal margins straight

or oblique. Type species: Pagurus piercei Wass, 1963.

Haigia McLaughlin, 1981

Diagnosis. Gills biserial, 11 pairs. Rostrum narrowly triangular.

Ocular acicles simple. Crista dentata with 1 accessory tooth.

Chelipeds unequal; right cheliped with chela subquadrate to

subrectangular. Sternite of somite XII (thoracomere 6, pere-

opods 3) with subsemicircular to roundly subrectangular ante-

rior lobe. Pereopod 4 semichelate; propodal rasp with 1 row of

corneous scales; no preungual process. Male with pleopods

3-5. Female with pleopod 1 paired, modified, pleopods 2-5.

Abdomen flexed or straight. Telson with terminal margins

straight or slightly excavated. Type species: Pylopagurus

diegensis Scanland and Hopkins, 1969.

Hemipagurus Smith, 1881

Diagnosis. Gills biserial, 11 pairs. Rostrum as broadly rounded

lobe. Ocular acicles simple. Crista dentata somewhat reduced.

Illustrated keys to the families and genera of Paguroidea

123

with 1 accessory tooth. Chelipeds elongate, unequal, right

stouter. Stemite of somite XII (thoracomere 6, pereopods 3)

with rectangular, sometimes armed, anterior lobe. Pereopod 4

semichelate; propodal rasp with 1 row of corneous scale; pre-

ungual process prominent. Right coxa of pereopod 5 of male

with long sexual tube directed toward exterior and curved over

dorsal surface of abdomen toward left; left coxa sometimes

with papilla or very short sexual tube; pleopods 3-5. Female

with pleopods 2-5. Telson with terminal margins oblique. Type

species: Hemipagurus gracilis Smith, 1881. (Genus reinstated

by Asakura, 2001)

Icelopagurus McLaughlin, 1997

Diagnosis. Gills biserial, 11 pairs. Rostrum triangular. Ocular

acicles simple. Crista dentata somewhat reduced, with 1 acces-

sory tooth. Chelipeds elongate, subequal, right stouter. Stemite

of somite XII (thoracomere 6, pereopods 3) with subrectang-

ular anterior lobe. Pereopod 4 semichelate; propodal rasp with

1 row of spiniform scales; preungual process tubular. Coxa of

right pereopod 5 of male with stout, short sexual tube directed

posteriorly and externally; left usually with very short sexual

tube; pleopods 3-5. Female with pleopods 2-5. Telson with ter-

minal margins rounded. Type species: Icelopagurus crosnieri

McLaughlin, 1997.

Iridopagurus de Saint Laurent-Dechance, 1966

Diagnosis. Gills quadriserial, 11 pairs. Rostrum as broadly

rounded or very obtusely triangular lobe. Ocular acicles simple.

Crista dentata without accessory tooth. Chelipeds subequal.

Stemite of somite XII (thoracomere 6, pereopods 3) with sub-

semicircular to subrectangular anterior lobe. Pereopod 4 sim-

ple; propodal rasp with 1 row of corneous scales; preungual

process present or absent. Male with long, coiled sexual tube on

coxa of left pereopod 5 ; tube development on right coxa vary-

ing from simple papilla to short sexual tube; pleopods 3-5.

Female with pleopods 2-5. Telson with terminal margins usu-

ally straight. Type species: Spiropagurus iris A. Milne-Edwards

and Bouvier, 1893.

Labidochirus Benedict, 1892

Diagnosis. Gills biserial, 11 pairs. Carapace, exclusive

of branchiostegites, generally heavily calcified throughout;

posterior carapace broader than shield. Rostrum prominent.

Ocular acicles simple, obscured basally by anterior

margin of shield. Crista dentata with 1 accessory tooth.

Chelipeds subequal or unequal, right larger. Stemite of

somite XII (thoracomere 6, pereopods 3) with subrectangular

anterior lobe, usually armed with spines medianly. Pereopod 4

simple; propodal rasp with 1 or 2 rows of corneous scales; no

preungual process. Male without unpaired pleopods. Female

with pleopods 2-5. Abdomen reduced. Telson with terminal

margins straight. Type species: Pagurus splendescens Owen,

1839.

Lithopagurus Provenzano, 1968

Diagnosis. Gills biserial, 13 pairs. Rostmm triangular. Ocular

acicles simple. Crista dentata with 1 accessory tooth. Chelipeds

grossly unequal; right chela operculate. Stemite of somite XII

(thoracomere 6, pereopods 3) with subquadrate anterior lobe.

Pereopod 4 semichelate; propodal rasp with several rows of

corneous scales; apparently no preungual process. Pereopod 5

minutely chelate. Male with pleopod 2 paired, modified; no

unpaired pleopods. Female with pleopods 2-4. Abdomen

reduced. Uropods generally symmetrical. Telson without later-

al indentations; terminal margin entire. Type species:

Lithopagurus yucatanicus Provenzano, 1968.

Lophopagurus (Australeremus) McLaughlin, 1981

Diagnosis. Gills biserial, 11 pairs. Rostmm triangular. Ocular

acicles simple. Crista dentata with 1 accessory tooth. Chelipeds

unequal; right chela subrectangular to subtriangular; dorsal sur-

face of palm usually circumscribed by row of dorsomesial,

dorsoproximal and dorsolateral marginal spines; left chela

with dorsolateral margin elevated, at least proximally, and fre-

quently expanded; propodal-carpal rotation variable. Stemite of

somite XII (thoracomere 6, pereopods 3) with subsemicircular,

subovate or slender rod-like anterior lobe. Pereopod 4 semi-

chelate; propodal rasp with 1 row of corneous scales; preungual

process minute. Male with pleopods 3-5. Female with pleopod

1 paired, modified; pleopods 2-5. Abdomen frequently straight

or only weakly flexed. Uropods symmetrical or asymmetrical.

Telson with terminal margins straight, oblique or rounded. Type

species: Eupagurus cookii Filhol, 1883.

Lophopagurus {Lophopagurus) McLaughlin, 1981

Diagnosis. Gills biserial, 11 pairs. Rostrum triangular. Ocular

acicles simple. Crista dentata with 1 accessory tooth. Chelipeds

unequal; right chela with dorsomesial margin depressed, dorsal

surface with sloping or concave dorsomesial component; left

chela with dorsal midline elevated into prominent keel or crest.

Ambulatory legs with dactyl and propodus of left pereopod 3

sometimes dissimilar. Stemite of somite XII (thoracomere 6,

pereopods 3) with subsemicircular to subrectangular anterior

lobe, occasionally armed. Pereopod 4 semichelate; propodal

rasp with 1 row of scales; usually no preungual process. Male

with pleopods 3-5. Female with pleopod 1 paired, modified;

pleopods 2-5. Telson with terminal margins straight, oblique or

rounded. Type species: Eupagurus thompsoni Filhol, 1885b.

Manucomplanus McLaughlin, 1981

Diagnosis. Gills biserial, 11 pairs. Rostrum broadly triangular

or rounded. Ocular acicles simple. Crista dentata with 1 acces-

sory tooth. Chelipeds unequal; right cheliped exhibiting con-

siderable sexual dimorphism; left cheliped with propodal-

carpal articulation rotated 15-45°. Stemite of somite XII

(thoracomere 6, pereopod 3) with elongate, slender or acutely

triangular, usually spinulose, anterior lobe. Pereopod 4 semi-

chelate; propodal rasp with several rows of corneous scales;

preungual process usually well developed. Male with pleopods

124

P.A. McLaughlin

3-5. Female with pleopod 1 paired, modified; pleopods 2-5.

Telson with terminal margins oblique or rounded. Type species:

Eupagurus (Elassochirus) corallinus Benedict, 1892 (=

Eupa gurus ungulatus Stiider, 1883).

Michelopagurus McLaughlin, 1997

Diagnosis. Gills quadriserial, 11 pairs. Rostrum as broadly

rounded or obtusely and bluntly triangular lobe. Ocular acicles

simple. Crista dentata with 1 accessory tooth, Chelipeds sub-

equal, right appreciably stouter. Sternite of somite XII

(thoracomere 6, pereopods 3) with subrectangular anterior lobe.

Pereopod 4 semichelate; propodal rasp with 1 row, or rarely

incomplete double of scales; no distinctive preungual process.

Right, left, or both coxae of pereopods 5 of male with short sex-

ual tube partially masked by tuft of setae; pleopods 3-5. Female

with paired, modified pleopod 1; pleopods 2-5. Telson with ter-

minal margins rounded. Type species: Pagurodes Umatulus

Henderson, 1888.

Micropagurus McLaughlin, 1986

Diagnosis. Gills biserial, 11 pairs. Rostrum as rounded lobe or

obsolete. Ocular acicles multispinose. Crista dentata with 1

accessory tooth. Chelipeds unequal, right largest. Sternite of

somite XII (thoracomere 6, pereopods 3) with broad, subrec-

tangular anterior lobe. Pereopod 4 semichelate; propodal rasp

with 1-3 rows of corneous scales; no preungual process. Coxa

of left pereopod 5 of male with moderate to long sexual tube;

right with or without gonopore; pleopods 3-5. Female with

pleopods 2-5. Telson without lateral indentations; terminal

margin entire. Type species: Micropagurus devaneyi

McLaughlin, 1986.

Munidopagurus A. Milne-Edwards, 1880

Diagnosis. Gills biserial, 13 pairs. Rostrum acute. Ocular aci-

cles simple. Crista dentata with 1 accessory tooth. Chelipeds

elongate, unequal, right longer and somewhat stronger. Sternite

of somite XII (thoracomere 6, pereopods 3) with bluntly sub-

triangular anterior lobe. Pereopod 4 unusually elongate, simple;

propodal rasp replaced by row of setae; no preungual process.

Male without unpaired pleopods. Female with pleopod 1

paired, modified; pleopods 2-4. Uropods symmetrical, pro-

topods each with prominent, posteriorly directed spine. Telson

without lateral indentations, terminal margin entire. Type

species: Eupagurus macrocheles A. Milne-Edwards, 1880.

Nematopaguroides Forest and de Saint Laurent, 1968

Diagnosis. Gills biserial, 11 pairs. Rostrum as broadly rounded

or obtusely triangular lobe. Ocular acicles simple. Crista denta-

ta with 1 accessory tooth. Chelipeds subequal or somewhat

unequal, right usually largest. Sternite of somite XII (thora-

comere 6, pereopods 3) with irregularly subrectangular anteri-

or lobe. Pereopod 4 semichelate; propodal rasp of 1 row of

corneous scales; preungual process usually present. Male with

moderate to long sexual tube on coxa of right pereopod 5,

usually directed obliquely toward exterior and with terminal

filament; left coxa with or without short to moderate sexual

tube; pleopods 3-5. Females with pleopods 2-5. Telson with

terminal margins oblique. Type species: Nematopaguroides

fagei Forest and de Saint Laurent, 1968.

Nematopagurus A. Milne-Edwards and Bouvier, 1892

Diagnosis. Gills biserial, 11 pairs. Rostrum as weakly and

obtusely subtriangular, broadly rounded or obsolete lobe.

Ocular acicles simple. Crista dentata with 1 accessory tooth.

Chelipeds moderately long and slender; subequal, with right

generally slightly longer and/or more robust. Sternite of somite

XII (thoracomere 6, pereopods 3) with subsemiovate to round-

ly rectangular anterior lobe. Pereopod 4 semichelate; propodal

rasp with 1 row of scales; no preungual process. Male with

moderate to long, often distally filamentous, sexual tube on

coxa of right pereopod 5, orientated from right to left across

ventral body surface; coxa of left with papilla, very short or

short sexual tube; pleopods 3-5. Females with pleopod 1

paired, modified; pleopods 2-5. Telson with terminal margins

straight, rounded, somewhat oblique, or prominently oblique.

Type species: Nematopagurus longicornis A. Milne-Edwards

and Bouvier, 1892.

Orthopagurus Stevens, 1927

Diagnosis. Gills biserial, 11 pairs. Rostrum prominent. Ocular

acicles simple. Crista dentata with 1 accessory tooth. Chelipeds

unequal, right considerably larger, suboperculate. Sternite of

somite XII (thoracomere 6, pereopods 3) with subovate anteri-

or lobe. Pereopod 4 semichelate; propodal rasp with several

rows of corneous scales; no preungual process. Male with

pleopods 3-5. Eemale with pleopods 2-5. Abdomen straight or

slightly flexed; tergites chitinous, usually in form of lateral

plates, tergite of somite 5 entire; tergite of somite 6 strongly

calcified. Telson with terminal margins straight. Type species:

Pagurus minimus Holmes, 1900.

Ostraconotus A. Milne-Edwards, 1880

Diagnosis. Gills biserial, 10 pairs, no pleurobranch on somite

XIII (thoracomere 7, above pereopod 4). Cephalothorax nearly

completely calcified. Rostrum as rounded lobe. Ocular acicles

simple. Crista dentata reduced, without accessory tooth.

Chelipeds unequal, right largest. Pereopods 2 and 3 with pad-

dle-shaped dactyls. Sternite of somite XII (thoracomere 6, pere-

opods 3) with elongate, slender, subrectangular anterior lobe.

Pereopod 4 with broadly expanded and flattened propodus, no

propodal rasp; dactyl elongate, simple. Pereopod 5 subchelate.

Male with long sexual tube on coxa of right pereopod 5; coxa

of left without sexual tube or with papilla; no unpaired

pleopods. Eemale with pleopods 2-4. Abdomen reduced.

Uropods symmetrical. Telson with terminal margin entire. Type

species: Ostraconotus spatulipes A. Milne-Edwards, 1880.

Paguridium Eorest, 1961

Diagnosis. Gills biserial, 11 pairs. Rostrum as broadly rounded

lobe. Ocular acicles simple. Crista dentata with 1 accessory

Illustrated keys to the families and genera of Paguroidea

125

tooth. Chelipeds unequal, right largest. Sternite of somite XII

(thoracomere 6, pereopod 3) not described. Pereopod 4 semi-

chelate; propodal rasp with 1 row of corneous scales. Male with

coxae of pereopod 5 markedly asymmetrical; gonopore on coxa

of left masked by tuft of long, stiff setae directed from left to

right and extending across ventral body surface, usually also

with papilla or very short sexual tube; no unpaired pleopods.

Female with pleopods 2-5. Telson with terminal margins

straight. Type species: Eupagurus ?minimus Chevreux and

Bouvier, 1892.

Paguritta Melin, 1939

Diagnosis. Gills biserial, 11 pairs. Rostrum triangular. Ocular

acicle simple or bifid. Antennal flagella with paired very long

setae armed with prominent setules on each article. Crista den-

tata with 1 accessory tooth. Chelipeds unequal; right apprecia-

bly larger. Sternite of somite XII (thoracomere 6, pereopods 3)

with subrectangular or subquadrate anterior lobe, anterior

margin usually with few blunt spines. Pereopod 4 semichelate,

propodal rasp with 1 row of corneous scales; no preungual

process. Male usually with papilla or very short sexual tube one

or both coxae of pereopods 5; no unpaired pleopods. Female

with pleopods 2-4. Uropods symmetrical. Telson with terminal

margins straight. Type species: Paguritta gracilipes Melin,

1939.

Pagurixus Melin, 1939

Diagnosis. Gills biserial, 11 pairs. Rostrum triangular. Ocular

acicles simple. Crista dentata with 1 accessory tooth. Chelipeds

markedly unequal; right chela exhibiting considerable sexual

dimorphism, often greatly swollen or extremely elongate in

large males. Sternite of somite XII (thoracomere 6, pereopods

3) with anterior lobe subrectangular or subquadrate. Pereopod

4 semichelate; propodal rasp with 1 row of corneous scales; no

preungual process. Male with coxae of pereopod 5 asymmetri-

cal, right largest; gonopore of right coxa of pereopod 5

obscured by tuft of moderate to long, stiff setae directed toward

left; pleopods 3-5. Female with paired gonopores or single

gonopore on coxa of left pereopod 3; pleopods 2-5. Telson with

terminal margins straight, rounded or oblique. Type species:

Eupagurus (Pagurixus) boninensis Melin, 1939.

Pagurodes Henderson, 1888

Diagnosis. Gills quadriserial, 11 pairs. Rostrum triangular.

Ocular acicles simple. Crista dentata with 1 accessory tooth.

Chelipeds elongate, subequal, right stouter. Sternite of somite

XII (thoracopod 6, pereopods 3) with marginal spinules on sub-

rectangular anterior lobe. Pereopods 4 semichelate; propodal

rasp with 1 row of corneous scales; no preungual process. Coxa

of right pereopod 5 of male with stout, short to moderate sexu-

al tube directed posteriorly, coxa of left sometimes with papil-

la or very short sexual tube; pleopods 3-5. Females with

pleopods 2-5. Telson with terminal margins oblique or nearly

perpendicular. Type species: Pagurodes inarmatus Henderson,

1888.

Pagurus Fabricius, 1775

Diagnosis. Gills biserial, 11 pairs. Rostrum variable. Ocular

acicles simple, bifid or multispinous. Crista dentata with 1 or

more accessory teeth. Chelipeds generally very unequal, right

usually appreciably larger. Sternite of somite XII (thoracomere

6, pereopods 3) with variably- shaped anterior lobe. Pereopod 4

usually semichelate; propodal rasp with 1 to several rows of

corneous scales; with or without preungual process. Male usu-

ally without, rarely with slight papilla protruded from gonopore

on one or both coxae of pereopod 5; with no paired, modified

pleopods, usually with unpaired pleopods 2-5 or 3-5, rarely

without unpaired pleopods. Female usually with paired, rarely

with single left gonopore on coxa(e) of pereopods 3; without

paired pleopod 1, usually with unpaired pleopods 2-5, rarely

2-4. Abdomen usually spirally twisted, occasionally straight.

Uropods asymmetrical, infrequently symmetrical. Telson with

terminal margins rounded, straight or oblique, usually with

median cleft. Type species: Cancer bernhardus Linnaeus, 1758

[as defined by lectotype selection by Forest and Holthuis

(1955: 312): specimen figured by Swammerdam (1737: pi. 2

fig- 1)]

Pagurojacquesia de Saint Laurent and McLaughlin, 2000

Diagnosis. Gills quadriserial, 11 pairs. Rostrum as rounded

lobe. Ocular acicles simple. Crista dentata without accessory

tooth. Chelipeds subequal, right stronger, but not always

longer. Sternite of somite XII (thoracomere 6, pereopods 3)

with armed or unarmed, subovate to subquadrate anterior lobe.

Pereopod 4 subchelate or very weakly semichelate; propodal

rasp with 1 row of corneous scales; no preungual process.

Pereopod 5 subchelate. Coxa of left pereopod 5 of male with

club-like, stout, very short to moderate left sexual tube direct-

ed toward exterior and provided with terminal tufts of very long

setae, coxa of right with small gonopore; pleopods 3-5.

Females with paired, modified pleopod 1, pleopods 2-5. Telson

with terminal margins very oblique. Type species: Jacquesia

polymorpha de Saint Laurent and McLaughlin, 1999.

Parapagurodes McLaughlin and Haig, 1973

Diagnosis. Gills biserial, or occasionally distally quadriserial;

11 pairs. Rostrum triangular. Ocular acicles simple. Crista den-

tata with 1 accessory tooth. Chelipeds unequal, right largest.

Sternite of somite XII (thoracomere 6, pereopods 3) with

roundly subrectangular anterior lobe. Pereopod 4 semichelate;

propodal rasp with 2 or more rows of corneous scales; usually

with small preungual process. Coxa of right pereopod 5 of male

with very short to short sexual tube, left with or without

similarly very short to short sexual tube; pleopods 3-5. Female

with pleopods 2-5. Telson with terminal margins rounded or

oblique. Type species: Parapagurodes makarovi McLaughlin

and Haig, 1973.

Phimochirus McLaughlin, 1981

Diagnosis. Gills biserial, 11 pairs. Rostrum usually triangular,

occasionally only as rounded lobe. Ocular acicles simple.

126

RA. McLaughlin

Crista dentata with 1 to several accessory teeth. Chelipeds

markedly unequal; right chela subovate to subcircular. Sternite

of somite XII (thoracopod 6, pereopods 3) with subsemiovate

to subsemicircular anterior lobe. Pereopod 4 semichelate;

propodal rasp with 1 row of corneous scales; preungual process

prominent. Male with pleopods 3-5. Female with pleopod 1

paired, modified; pleopods 2-5. Telson with terminal margins

oblique. Type species: Eupagurus operculatus Stimpson, 1859.

Porcellanopagurus Filhol, 1885a

Diagnosis. Gills biserial, 11 pairs. Anterior carapace vaulted

and well calcified; lateral margins of shield each developed into

2 blunt or spiniform, wing-like projections. Rostrum triangular

or truncated. Ocular acicles simple, obscured from dorsal view

by broad rostrum. Posterior carapace well calcified anteriorly

and usually drawn out into projecting lobes. Crista dentata with

1 accessory tooth. Chelipeds unequal, right appreciably larger.

Sternite of somite XII (thoracomere 6, pereopod 3) with broad,

subrectangular lobe. Pereopod 4 usually semichelate; propodal

rasp with 1 row of corneous scales; no preungual process. Male

with coxae of pereopods 5 sometimes expanded posteroven-

trally, but usually without very short sexual tube developed;

without unpaired pleopods. Female with paired gonopores

located posteriorly on coxae of pereopods 3; pleopods 2-A.

Abdomen reduced, usually globular, with tergites at least faint-

ly delineated. Uropods generally symmetrical. Telson often

carried ventrally; terminal margin rounded, enthe or with slight

median cleft. Type species: Porcellanopagurus edwardsi

Filhol, 1885a.

Propagurus McLaughlin and de Saint Laurent, 1998

Diagnosis. Gills generally quadriserial, 13 pairs (11 or 12 pairs

presumably functional), with pleurobranch on somite XI (tho-

racomere 5, above pereopod 2) rudimentary or well-developed,

pleurobranch on somite XII (thoracomere 6, above pereopod 3)

always rudimentary. Rostrum triangular. Ocular acicles simple.

Crista dentata with 1 accessory tooth. Chelipeds unequal; right

longer and stronger. Sternite of somite XII (thoracomere 6,

pereopods 3) with subsemicircular, to roundly subrectangular

anterior lobe. Pereopod 4 semichelate; propodal rasp with 2 to

several rows of corneous scales; no preungual process. Male

with pleopods usually 3-5, occasionally 2-5. Females

with pleopods 2-5. Telson with terminal margins generally

oblique. Type species: Pagurus gaudichaudii H. Milne

Edwards, 1836.

Protoniopagurus Lemaitre and McLaughlin, 1996

Diagnosis. Gill biserial, 11 pairs. Rostrum obtusely triangular.

Ocular acicles simple or bifid. Crista dentata with 1 accessory

tooth. Chelipeds subequal; right slightly larger, both suboper-

culate. Sternite of somite XII (thoracomere 6, pereopods 3)

with small subquadrate anterior lobe. Pereopod 4 semichelate;

propodal rasp with 10-12 rows of corneous scales; no preun-

gual process. Male without unpaired pleopods. Female with

pleopod 1 paired, modified; pleopods 2-4. Abdomen reduced.

Uropods symmetrical. Telson with terminal margin entire. Type

species: Protoniopagurus bioperculatus Lemaitre and

McLaughlin, 1996.

Pseudopagurodes McLaughlin, 1997

Diagnosis. Gills distally quadriserial, 11 pairs. Rostrum

reduced and rounded. Ocular acicles simple. Crista dentata with

1 accessory tooth. Chelipeds subequal, right somewhat

stronger. Sternite of somite XII (thoracomere 6, pereopods 3)

with roundly subrectangular anterior lobe. Pereopod 4 semi-

chelate; propodal rasp with 1 row of corneous scales; no

preungual process. Coxa of right pereopod 5 of male with

long sexual tube, stout proximally and drawn out into filament

distally. Female with pleopods 2-5. Telson with oblique ter-

minal margins. Type species: Pagurodes piliferus Henderson,

1888.

Pygmaeopagurus McLaughlin, 1986

Diagnosis. Gills biserial, 11 pairs. Rostrum triangular. Ocular

acicles simple. Crista dentata with 1 accessory tooth. Chelipeds

grossly unequal; right exceptionally large. Sternite of somite

XII (thoracomere 6, pereopods 3) with semicircular anterior

lobe. Pereopod 4 simple or weakly semichelate; propodal rasp

with 1 row of corneous scales; no preungual process. Male with

short to moderate, rod-like sexual tube on coxa of left pereopod

5, no gonopore on coxa of right; pleopods 3-5. Female with

single gonopore on coxa of left pereopod 3; pleopods 2-5.

Telson with terminal margins oblique. Type species:

Pygmaeopagurus hadrochirus McLaughlin, 1986.

Pylopaguridium McLaughlin and Lemaitre, 2001

Diagnosis. Gills biserial, 11 pairs. Rostrum triangular. Ocular

acicles multispinose. Crista dentata with 1 accessory tooth.

Right cheliped markedly larger than left, subrectangular, oper-

culate. Sternite of somite XII (thoracomere 6, pereopods 3)

with subsemicircular or subovate anterior lobe, usually armed

with few small spines. Pereopod 4 semichelate; propodal rasp

with 1 row of corneous scales; no preungual process. Male with

paired gonopores, but coxae of pleopods 5 asymmetrical, left

produced posteriorly; pleopods 3-5. Female with pleopod 1

paired, modified; pleopods 2-5. Telson with terminal margins

straight. Type species: Pylopaguridium markhami McLaughlin

and Lemaitre, 2001b.

Pylopaguropsis Alcock, 1905

Diagnosis. Gills biserial, 13 pairs. Rostrum triangular. Ocular

acicles simple. Crista dentata with 1 accessory tooth. Right che-

liped usually massive, chela operculate or semioperculate;

dactyl frequently articulating obliquely with palm. Ambulatory

legs with dactyls and propodi of pereopods 3 frequently dis-

similar. Sternite of somite XII (thoracomere 6, pereopods 3)

with subsemicircular to subrectangular anterior lobe. Pereopod

4 semichelate; propodal rasp with 1 to 4 rows of corneous

scales, with or without preungual process. Male with pleopods

3-5. Female with pleopod 1 paired, modified; pleopods 2-5.

Telson with terminal margins oblique, concave or straight. Type

species: Pylopagurus magnimanus Henderson, 1896.

Illustrated keys to the families and genera of Paguroidea

127

Pylopagurus A. Milne-Edwards and Bouvier, 1891

Diagnosis. Gills biserial, 11 pairs. Rostrum acute. Ocular aci-

cles simple. Crista dentata with 1 accessory tooth. Right che-

liped markedly larger than left; chela subcircular to subrectan-

gular, operculate. Stemite of somite XII (thoracomere 6, pere-

opods 3) with nan'ow subovate, subquadrate, or subsemicircu-

lar anterior lobe. Pereopod 4 semichelate; propodal rasp with 1

row of corneous scales; preungual process small to very promi-

nent. Male usually without, but occasionally with papilla or

very short sexual on one or both coxae of pereopod 5 ; pleopods

3-5. Female with pleopod 1 paired, modified; pleopods 2-5.

Abdomen straight or rarely flexed. Uropods symmetrical or

nearly so. Telson with terminal margins concave or oblique.

Type species: Eupagurus discoidalis A. Milne-Edwards, 1880

Rhodochirus McLaughlin, 1981

Diagnosis. Gills biserial, 11 pairs. Rostrum obtusely triangular

or as broadly rounded lobe. Ocular acicles simple. Crista den-

tata with 1 accessory tooth. Right chela subovate to sub-

quadrate; at least some spines or tubercles with basal rosettes.

Sternite of somite XII (thoracomere 6, pereopods 3) with sub-

semicircular to subquadrate anterior lobe. Pereopod 4 semi-

chelate; propodal rasp with 1 row of corneous scales; preungual

process well developed. Male with pleopods 3-5. Female with

pleopod 1 paired, modified; pleopods 2-5. Telson with terminal

margins oblique. Type species: Pylopagurus rosaceus A.

Milne-Edwards and Bouvier, 1893.

Scopaeopagurus McLaughlin and Hogarth, 1998

Diagnosis. Gills biserial, 10 pairs, no pleurobranch on somite

XIII (on thoracomere 7, above arthrobranchs of pereopod 4).

Rostrum triangular. Ocular adcles simple. Crista dentata con-

sisting of 2 or 3 strong curved, spine-like teeth; no accessory

tooth. Chelipeds grossly unequal, right massive. Sternite of

somite XII (thoracomere 6, pereopods 3) with roundly rectan-

gular anterior lobe. Pereopod 4 weakly semichelate; propodal

rasp with 1 row of corneous scales; no preungual process. Male

with short sexual tube on coxa of left pereopod 5, coxa of right

with only small papilla; pleopods 2-5. Females with single

gonopore on coxa of left pereopod 3; pleopods 2-5. Telson with

terminal margins oblique. Type species: Scopaeopagurus

megalochirus McLaughlin and Hogarth, 1998.

Solenopagurus de Saint Laurent, 1968

Diagnosis. Gills distally quadriserial, 11 pairs. Rostrum as

broadly rounded lobe. Ocular acicles simple. Crista dentata

with 1 accessory tooth. Chelipeds subequal, right somewhat

longer and stronger. Sternite of somite XII (thoracomere 6,

pereopods 3) with subsemicircular to subquadrate anterior lobe.

Propodus and dactyl of left pereopod 3 dissimilar in having

numerous plumose setae on lateral faces. Pereopod 4 semi-

chelate; propodal rasp with 1 row of corneous scales; preungual

process usually present. Male with long sexual tube on coxa of

right pereopod 5, directed toward exterior and curved dorsally,

coxa of left usually with small papilla; pleopods 3-5. Female

with pleopods 2-5. Telson with terminal margins straight or

oblique. Type species: Cestopagurus lineatus Wass, 1963.

Solitariopagurus Tiirkay, 1986

Diagnosis. Gills biserial, 10 pairs, no pleurobranch on somite

XIII (thoracomere 7, above arthrobranchs of pereopod 4).

Anterior carapace vaulted and strongly calcified; lateral mar-

gins of shield each developed into 3 blunt or spiniform lobes;

posterior carapace lobe consisting of elongate median and

small lateral elements. Rostrum prominent. Ocular acicles

reduced, simple; hidden from dorsal view by anterior margin of

shield. Crista dentata with 1 accessory tooth. Right cheliped

much stronger, but not appreciably longer than left. Sternite of

somite XII (thoracomere 6, pereopods 3) with subrectangular

anterior lobe. Pereopod 4 subchelate; propodal rasp with 1 row

of corneous scales; no preungual process. Pereopod 5 sub-

chelate. Male with stout, short to moderate, equal or unequal

sexual tubes developed on coxae of both pereopods 5, right

frequently longer; each with long setae subterminally and ter-

minally; no unpaired pleopods. Female with single gonopore

posteriorly on coxa of left pereopod 3; pleopods 2-A. Abdomen

reduced; tergal plate of abdominal somite 2 weakly delineated;

tergal plates of somites 3-5 clearly defined. Uropods symmet-

rical; protopods each with very prominent, posteriorly directed

spine. Telson with terminal margin entire. Type species:

Solitariopagurus profundus Tiirkay, 1986.

Spiropagurus Stimpson, 1858

Diagnosis. Gills biserial, 11 pau's. Rostrum as broadly rounded

lobe. Ocular acicles simple. Crista dentata with 1 accessory

tooth. Chelipeds subequal, right usually slightly stronger, but

not necessarily longer. Sternite of somite XII (thoracomere 6,

pereopods 3) with anterior lobe narrowly subrectangular, occa-

sionally obsolete. Pereopod 4 semichelate; propodal rasp with

1 row of corneous scales; no preungual process. Male with

long, usually coiled, terminally blunt sexual tube on coxa of left

pereopod 5, right without sexual tube but sometimes with small

papilla; pleopods 3-5. Female with pleopods 2-5. Telson with

characteristic, acutely triangular posterior lobes (Fig. 3c), ter-

minal margins very oblique. Type species: Pagurus spiriger De

Haan, 1849.

Tarrasopagurus McLaughlin, 1997

Diagnosis. Gills distally quadriserial, 11 pairs. Rostrum obtuse-

ly triangular or broadly rounded, with 1 or more marginal spin-

ules. Ocular acicles simple. Crista dentata with 1 accessory

tooth. Chelipeds markedly unequal, right considerably longer

and stronger. Sternite of somite XII (thoracomere 6, pereopods

3) with semicircular anterior lobe. Pereopod 4 semichelate;

propodal rasp with 1 row of corneous scales; no preungual

process. Male with short sexual tube on coxa of left pereopod

5, directed anteriorly or posteriorly, right sometimes also with

short or very short tube developed, sometimes with only papil-

la; pleopods 3-5. Female with pleopod 1 paired, modified;

pleopods 2-5. Telson with terminal margins oblique. Type

species: Tarrasopagurus rostrodenticulatus McLaughlin, 1997.

128

P.A. McLaughlin

Tomopaguroides Balss, 1912

Diagnosis. Gills quadriserial, 13 pairs. Rostrum triangular.

Ocular acicles simple. Crista dentata not described. Chelipeds

grossly unequal, right largest. Sternite of somite Xll (thora-

comere 6, pereopods 3) with small, triangular anterior lobe.

Pereopod 4 semichelate; propodal rasp with 1, possibly 2, rows

of corneous scales; apparently no preungual process. Male with

pleopod 2 paired, modified; pleopods 3-5. Female unknown.

Abdomen straight, tergite of somite 5 as thickened, possibly

calcified plate; uropods symmetrical. Telson terminal margin

not described. Type species: Parapagurus valdiviae Balss,

1911.

Tomopaguropsis Alcock, 1905

Diagnosis. Gills quadriserial, 13 pairs. Rostrum triangular.

Ocular acicles simple. Crista dentata with 1 accessory tooth.

Chelipeds subequal; right usually somewhat more robust.

Subquadrate anterior lobe of sternite of somite XII (thoracom-

ere 6, pereopod 3) with convex median, marginally setose, ele-

vation. Pereopod 4 semichelate; propodal rasp with several

rows of corneous scales; no preungual process. Male with or

without pleopod 1 paired, modified; pleopods 2-5. Female with

pleopods 2-5. Telson with terminal margins rounded. Type

species: Tomopaguropsis lantana Alcock, 1905.

Tomopagurus A. Milne-Edwards and Bouvier, 1893

Diagnosis. Gills biserial, 11 pairs. Rostrum triangular or some-

times only broadly rounded lobe. Ocular acicles simple. Crista

dentata with 1 accessory tooth. Chelipeds unequal, right appre-

ciably larger. Sternite of somite XII (thoracomere 6, pereopods

3) with subovate to subsemicircular anterior lobe. Pereopod 4

semichelate; propodal rasp with 1 row of corneous scales; pre-

ungual process prominent. Male usually without, rarely with

pleopod 1 paired but reduced or vestigial; pleopods 3-5.

Female usually with pleopod 1 paired, modified, rarely without

pleopod 1; pleopods 2-5. Telson with terminal margins oblique.

Type species: Tomopagurus rubropunctatus A. Milne-Edwards

and Bouvier, 1893.

Trichopagurus de Saint Laurent, 1968

Diagnosis. Gills distally quadriserial, 11 pairs. Rostrum trian-

gular. Ocular acicles simple. Crista dentata with 1 accessory

tooth. Chelipeds unequal, some degree of sexual dimorphism.

Sternite of somite XII (thoracomere 6, pereopods 3) with sub-

rectangular anterior lobe. Pereopod 4 semichelate; propodal

rasp with 1 row of corneous scales; no preungual process. Coxa

of male right pereopod 5 with moderate sexual tube directed

toward the exterior; left with very short tube; pleopods 3-5.

Eemale with single gonopore on coxa of left pereopod 3;

pleopods 2-5. Type species: Catapaguroides ?trichophthalmm

Eorest, 1954.

Turleania McLaughlin, 1997

Diagnosis. Gills quadriserial, 11 pairs. Rostrum narrowly trian-

gular. Ocular acicles simple or multispinous. Crista dentata

without accessory tooth. Chelipeds unequal or subequal, right

appreciably stouter, but not necessarily longer. Sternite of

somite XII (thoracomere 6, pereopods 3) with generally sub-

quadrate anterior lobe. Pereopod 4 semichelate; propodal rasp

with 1 row of scales corneous scales; no preungual process.

Coxa of left pereopod 5 of male with moderate to long, often

weakly spiraled sexual tube provided with sparse terminal tuft

of stiff setae; right occasionally with papilla; pleopods 3-5.

Eemales with pleopods 2-5. Telson with terminal margins

oblique. Type species: Laurentia albatrossae McLaughlin and

Haig, 1996a.

Xylopagurus A. Milne Edwards, 1880

Diagnosis. Gills biserial or distally quadriserial, 13 pairs.

Rostrum obtusely triangular. Ocular acicles multispinose.

Crista dentata with 1 accessory tooth. Chelipeds grossly

unequal; palm of right with prominent spine or protuberance at

mesial dorsodistal angle. Sternite of somite XII (thoracomere 6,

pereopods 3) with narrow or subtriangular anterior lobe.

Pereopod 4 semichelate; propodal rasp with numerous rows of

small, corneous scales; no preungual process. Pereopod 5 sub-

chelate, sometimes sexual dimorphic. Male with pleopods 1

and 2 paired, modified; no unpaired pleopods. Female with

pleopods 2-4. Tergites of abdominal somites 2-5 as narrow cal-

cified plates, tergite 6 heavily calcified and operculate; uropods

symmetrical. Telson without lateral indentations, broader than

long, terminal margin entire. Type species: Xylopagurus rectus

A. Milne-Edwards, 1880.

Acknowledgements

The author most gratefully acknowledges the financial support

of the Pacific Northwest Shell Club and Museum Victoria in

providing funds for page charges for this manuscript. Thanks

are also due those authors who allowed the reproduction and/or

adaptation of their original illustrations. The meticulous

reviews provided by A. Asakura, P. Clark, J. Eorest, R.

Lemaitre and C. Tudge considerably improved the usefulness

of these keys. This is a scientific contribution from the Shannon

Point Marine Center, Western Washington University.

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de Saint Laurent-Dechance, M. 1966a. Iridopagurus, genre nouveau

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151-173.

de Saint Laurent-Dechance, M. 1966b. Remarques sur la classification

de la famille des Paguridae et sur la position systematique

d’ Iridopagurus de Saint Laurent. Diagnose d’ Anapagrides gen.

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134

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1-236.

Illustrated keys to the families and genera of Paguroidea

135

Figure 1 . Morphological diversity among members of the Paguroidea. a, b, Coenobitidae, c, Pylochelidae; d-g, Diogenidae; h-k, Lithodidae, l-o,

Paguridae, p, q, Parapaguridae: a, Birgus latro Leach; b, Coenohita clypeatus (Fabricius); c, Trizocheles spinosus (Henderson); d, AUodardanus

hredini Haig and Provenzano; e, Dardanus venosus (H. Milne Edwards); f, CUbanarius arethusa De Man; g, Calcimis tibicen (Herbst); h,

Cryptolithodes sitchensis Brandt; i, Hapalogaster dentata (De Haan); j, Sculptolithodes derjugini Makarov; k, Lithodes murrayi Henderson; 1,

Labidochirus splendescens (Owen); m, Propagurus gaudichaudi (H. Milne Edwards); n, Ostraconotus spatidipes A. Milne-Ed wards; o,

Porcellanopaguriis edwurdsi Eilhol; p, Tylaspis anomala Henderson; q, Probeebei mirabilis Boone, [a, f after Alcock, 1905; b, from Chace and

Hobbs, 1969; c, k, p, from Henderson, 1888; d, e, g, after Chace et al. 1985; h, from Makarov, 1938; i, j, from Vinogradov, 1950; 1 from

McLaughlin, 1974; m, from Benedict, 1901 as Eupagurus patagonensis Benedict; n, after A. Milne-Edwards and Bouvier, 1893; o, after Eorest,

195 1 ; q, from Wolff, 1961; not to scale.]

136

P.A. McLaughlin

Figure 2. Bases and paired basis-ischium of maxilliped 3; a, Coenobitidae - Coenobita clypeatus (Fabricius); b, Diogenidae - Clibanarius vitta-

tus (Bose); c, Pylochelidae - Mixtopagurus paradoxus A. Milne- Edwards; d, Pylojacquesidae - Pylojacquesia colemani McLaughlin and

Lemaitre; e, Parapaguridae - Parapagurus pilosimanus Smith; f, Paguridae - Pagurus pollicaris Say; g, reduced teeth on crista dentata of ischi-

um, Scopaeopagurus rnegalochirus McLaughlin and Hogarth.

Antennular and antennal flagella, h-j, antennular flagella: h, Coenobitidae; i, Pagurus imafukui McLaughlin and Konishi; j, generalised fla-

gella of Diogenidae, Paguridae and Parapaguridae; k, antennal flagellum with paired ventral setae.

Thoracic stemites and coxae of pereopods; 1, Pylojacquesia colemani McLaughlin and Lemaitre; m, generalised Paguridae; n, Lithodes aeq-

uispinus Benedict (sternites X and XI only; groove and pit of sternite XI indicate by arrow). Abbreviations; act = accessory tooth (teeth) indicat-

ed by arrows; ap = anterior portion; C 1-5 = coxae of pereopods 1-5; gp = gonopore; mh = membranous hinge; pp = posterior portion, [a-f, 1,

from McLaughlin and Lemaitre, 2001c; g, from McLaughlin and Hogarth, 1998; h, from McLaughlin and Dworschak, 2001; i from McLaughlin

and Konishi, 1994; j, from Forest et al. 2000; k, from McLaughlin and Haig, 1996b, m, adapted from McLaughlin, 1974; not to scale]

Illustrated keys to the families and genera of Paguroidea

137

Figure 3. Basic morphology: a, diagrammatic pagurid (whole animal, dorsal view); b, diagrammatic lithodid (whole animal, dorsal view).

Cephalothorax or shield, with or without cephalic appendages; c-h Pylochelidae; i, Diogenidae; j, Pylojacquesidae; k-m Paguridae. c,

Pylocheles', d, Trizocheles\ e, Cheiroplatea; f, Pomatocheles\ g, Parapylocheles', h, Cancellocheles\ i, Diogenes', j, Pylojacquesia', k,

Porcellanopagurus', 1, Solitariopagurus', m, Hernipagurus. Abbreviations: aa = antennal acicle; ant. = antenna; antu = antennule; c, cornea; car =

carpus; eg = cervical groove; dac = dactyl; If = fixed finger; irp = intercalary rostral process; la = linea anomurica; If ch = left cheliped; If ur =

left uropod; Ip = lateral projection; It = linea transversalis; mer = mems; oa = ocular acicle; op = ocular peduncle; P2-5 = pereopods 2-5; pel =

posterior carapace lobe; pcme = posterior carapace median element; pl3-5 = pleopods 3-5; plm = palm; pmp = posterior median plate; pop = pos-

tocular projection; pro = propodus; r = rostrum or rostral lobe; rt ch = right cheliped; s = shield; si 1-3 = shield lobes 1-3; t6 = abdominal tergite

6; tel = telson. [a, b, adapted from Sandberg and McLaughlin, 1998; c, d from Forest et al. 2000; e-h, from Forest, 1987; i, from McLaughlin and

Clark, 1997; j, from McLaughlin and Lemaitre, 2001c; k, 1, from McLaughlin, 2000; m, from McLaughlin, 1997 (as Catapagurus)', not to scale.]

Illustrated keys to the families and genera of Paguroidea

139

Figure 4. Gills: a, left gill series of 14 pairs (paired arthrobranchs on arthrodial membranes of maxilliped 3, chela, and pereopods 2-4; single

pleurobranchs on somites XI, XII, XIII, and XIV (thoracomeres 5-8, above pereopods 2-5); b, left gill series of 13 pairs (paired arthrobranchs on

arthrodial membranes of maxilliped 3, chela, and pereopods 2-4; single pleurobranchs on somites XI, XII, and XIII (thoracomeres 5-7, above

pereopods 2-4); c, left gill series with paired arthrobranchs reduced or vestigial on arthrodial membranes of maxilliped 3 and cheliped; pleuro-

branchs absent from somites XI and XIV (thoracomeres 5 and 8, above pereopods 2 and 5); left gill series of 11 pairs (paired arthrobranchs

on arthrodial membranes of maxilliped 3, chela, and pereopods 2 - 4 ; single pleurobranch on somite XIII (thoracomere 7, above pereopod 4);

e, vestigial pleurobranch (indicated by arrow) on somite XIV (thoracomere 8, above pereopod 5) in some parapagurids; f, biserial gill lamella;

g, distally divided quadriserial gill lamella; h, deeply divided quadriserial gill lamella.

Mandible: i, Pylojacquesidae; j, Paguridae.

Maxillule: k, with external lobe (indicated by arrow) of endopod well developed, recurved; 1, with external lobe (indicated by arrow) of endo-

pod weakly developed or obsolete, not recurved.

Maxilliped 1 : m, with exopodal flagellum; n, without exopodal flagellum.

Maxilliped 2: o, with epipod.

Maxilliped 3: p, with epipod; q, without epipod.

Abbreviations: arth = arthrobranch; eh = cheliped; epip = epipod; fla = flagellum; mxp = maxilliped 3; pleu = pleurobranch; 2-5 = coxae of pere-

opods 2-5. [e, from Lemaitre, 1989; f-h, 1-n, q from Forest et al. 2000; i, from McLaughlin and Lemaitre, 2001c; j, from McLaughlin, 1974; k,

o, p, from Forest, 1987; not to scale].

140

P.A. McLaughlin

Figure 5. Representative telsons; a, b, Pylochelidae; c-j, Paguridae; k, Parapaguridae.

Sixth abdominal tergite, protopods of uropods and telson: j, Munidopagurus.

Dactyl and propodus of pereopod 4: 1, o, simple; m, q, subchelate; n, r, semichelate with multiple rows of corneous scales in propodal rasp and

no preungual process; p, u, t, semichelate with single row of corneous scales in propodal rasp and preungual process at base of claw; s, semi-

chelate with multiple rows of corneous scales in propodal rasp and preungual process at base of claw; t, chelate; v, semichelate with “type A” (cf.

McLaughlin, 1974) sensory stracture on lateral face of dactyl.

Dactyl and propodus of pereopod 5; w, x subchelate; y, semichelate; z, chelate, [a, b, n, from Forest and McLaughlin, 2000; c, from Lewinsohn,

1982; d, e, from McLaughlin, 1982; f-i from McLaughlin, 1997; j, adapted from Provenzano, 1971; k, from Lemaitre, 1996; 1, o-q, s, u, y, from

McLaughlin, 1997; m, from McLaughlin and Lemaitre, 1997; q, w, from McLaughlin and Lemaitre, 2001c, v, from McLaughlin, 1974; x, after

Lemaitre, 1998; not to scale].

Illustrated keys to the families and genera of Paguroidea

141

Figure 6. Chelipeds: a, left chela of Ciliopagums (mesial view) showing stridulating mechanism (indicated by an'ows); b, left chela of

Allodardanus (mesial view) lacking stridulating mechanism; c, left chela and carpus of Ciliopagurus (lateral view); d, chelae of Cancellus togeth-

er forming operculum; e, left carpus and chela of Aniculus; f, left chela and carpus of Isocheles (dorsal view), with dactyl opening horizontally

(as indicated by arrow), g, left chela and carpus of Loxopagurus (dorsolateral view) with dactyl opening vertically (as indicated by arrow); h, right

chela and carpus of Paragiopagurus (dorsal view) with dactyl opening obliquely (as indicated by arrow); i, right chela of Pyiojacquesia\ j, right

chela of Xyiopagurus-, k, right chela of Bathypaguropsis\ 1, right chela of lujphopagurus (Australerenius); m, right chela of Rhodochirus; n, left

chela of Lophopagurus (Lophopagiirus); o, right carpus and chela of Goreopagurus (lateral view); p, right carpus and chela of Oedignathus

(mesial view); q, right carpus and chela of Dennaturus (mesial view), [a, c, from Forest, 1952; b, after Flaig and Provenzano, 1965; d, after Mayo,

1973; e, from McLaughlin and Hoover, 1995; f, g, from Forest and de Saint Laurent, 1968; h, from Lemaitie, 1996; i, from McLaughlin and

Lemaih'e, 2001c; j, from Lemaitre, 1995; k, from McLaughlin, 1994; 1, n, from McLaughlin and Gumi, 1992; m, from Williams, 1984; o, from

McLaughlin and Haig, 1995; k, 1, after Vinogradov, 1950; not to scale].

142

P.A. McLaughlin

Figure 7. Secondary sexual appendages and structures: a, coxae of pereopods 5 and abdominal somites 1 and 2 of male with pleopods 1 and 2

paired, modified; b, c, coxae of pereopods 5 and abdominal somite 1 of female with pleopod 1 paired, modified; d, female brood pouch; e-g, male

pleopod 2; h-q, male sexual tubes; r, male gonopores without sexual tube development; s, coxa of right pereopod 5 of male with gonopore masked

by tuft of stiff setae; t, coxa of left pereopod 5 of male with gonopore masked by tuft of stiff setae, [a, from Forest et al. 2000; b, from McLaughlin

and Haig, 1995; c, q, r, from McLaughlin and Lemaitre, 2001b; d, from McLaughlin and Provenzano, 1975; e, f, from Lemaitre, 1989; g, from

Forest, 1995; i-n from McLaughlin, 1997; h, from Wang and McLaughlin, 2000; p, from McLaughlin, 1986; s, from Melin, 1939; t, from Forest,

1961; not to scale].

Illustrated keys to the families and genera of Paguroidea

143

Figure 8. Additional morphological characters: a, c, shield with Y-shaped posterior groove; b, shield without Y-shaped posterior groove; d, last

thoracic somite and abdomen of Xylopagurus (dorsal view); e, multifid ocular acicles; f, Lithodes rostral spine complex; g, dorsal and ventral ros-

tral spines of Glyptolithodes\ h, Cryptolithodes (ventral view) with carapace covering body and appendages; i, rostmm with epirostral spine (lat-

eral view); j, symmetrical uropods and posterior portion of abdominal tergite 6, plus telson (dorsal view) k, right antennal peduncle witli hooked

spine (indicated by arrow) on lateral margin of segment 1 ; 1, shield of Typhlopagurus showing spinose ocular and antennal acicles and lack of

ocular peduncles; m, parapagurid epistome and labrum. Abbreviations: apr = anterior rostral process; ds = dorsal spine(s); es = epistomial spine;

Is = labral spine; vs = ventral spine; 6 indicates abdominal tergite 6. [a, from McLaughlin and Hoover, 1996; b, from Forest and de Saint Laurent,

1968; c, from Forest and McLaughlin, 2000; d, from Lemaitre, 1995; e, McLaughlin and Murray, 1990; f, from Vinogradov, 1950; g, after Haig,

1974; h, from Makarov, 1938; i, from McLauglilin, 1997; j, from McLaughlin and Lemaitre, 1993; k, from McLaughlin, 1981; 1, from de Saint

Laurent, 1972; m, after Lemaitre, 1989; not to scale].

144

RA. McLaughlin

Figure 9. Lithodid abdominal tergites: a, Acantholithodes tergites 1 and 2, tergites 3-6 and telson; b, Hopalogaster tergites 1-3; c, Placetron ter-

gites 1 and 2, tergites 3-6 and telson, showing female asymmetry in tergites 3-5; d, OecUgnathus tergites 1-3; e, Neolithodes tergites 1 and 2,

tergites 3-6 and telson; f, Phyllolithodes tergites 1 and 2, tergites 3-6 and telson; g, Lopholithodes tergite 1+2, tergites 3-6 and telson;

h, Pamlithodes tergites 1 and 2, tergites 3-6 and telson; i, Lithodes tergites 1 and 2, tergites 3-6 and telson; j, Paralomis tergite 1+2, tergites

3-6 and telson; k, Cryptolithodes tergite 1+2. tergites 3-6 and telson. Abbreviations: am = accessory marginal plates; ap = accessory plate;

la = lateral plate, m = marginal plate; M = median plate; t = telson; tergites are numbered 1-6. [a-i, k from McLaughlin and Lemaitre, 2001a.;

j adapted from Macpherson, 1988; not to scale].

Memoirs of Museum Victoria 60(1): 145-149 (2003)

ISSN 1447-2546 (Print) 1447-2554 (On-line)

http://www.museum.vic.gov.au/memoirs

A new theoretical approach for the study of monophyly of the Brachyura

(Crustacea: Decapoda) and its impact on the Anomura

Marcos Tavares

Universidade Santa Ursula, Institute de Ciencias Biologicas e Ambientais, Rua Fernando Ferrari, 75, Rio de Janeiro

22231-040, Brazil

Present address: Museu de Zoologia, Universidade de Sao Paulo, SP 04263-000, Brazil (mtavares@altemex.com.br)

Abstract Tavares, M. 2003. A new theoretical approach for the study of monophyly of the Brachyura (Cmstacea; Decapoda) and

its impact on the Anomura. In: Lemaitre, R., and Tudge, C.C. (eds). Biology of the Anomura. Proceedings of a sympo-

sium at the Fifth International Cmstacean Congress, Melbourne, Australia, 9-13 July 2(K)l. Memoirs of Museum Victoria

60(1); 145-149.

The primitive crabs consist of the Cyclodorippidae Ortmann, 1892; Cymonomidae Bouvier, 1897; Dromiidae de Haan,

1833; Dynomenidae Ortmann, 1892; Homolodromiidae Alcook, 1900; Homolidae de Haan, 1839; Latreilliidae

Stimpson, 1858; Phyllotymolinidae Tavares, 1998; Poupiniidae Guinot, 1991; and Raninidae de Haan, 1841. The prim-

itive crabs were transferred for the first time from the Brachyura to the Anomura by H. Milne Edwards (1832). Since

then, they have been moved, individually or collectively, from the Anomura to the Brachyura and vice-versa with each

successive revision. The high classification of both, Anomura and Brachyura, will not attain stability until the systemat-

ic position of the primitive crabs is established on a firm basis. The question of whether the Podotremata, in whole or in

part, belongs or not to the Brachyura is discussed herein from a cladistic perspective. The argument is made that there

are four different assumptions hidden within this question, and that only when they are explicitly considered will real

progress be made towards a better understanding of brachyuran interrelationships.

Keywords Cmstacea, Brachyura, Podotremata, Anomura, Dromiidae, Dynomenidae, Homolodromiidae, Homolidae, Latreilliidae,

Poupiniidae, Cyclodorippidae, Cymonomidae, Phyllotymolinidae, Raninidae, cladistics, phylogeny, classification

Introduction

Whether the Brachyura (Podotremata Guinot, 1977 -i-

Heterotremata Guinot, 1977 -i- Thoracotremata Guinot, 1977)

are monophyletic or not has long been disputed by decapod-

ologists. Efforts to address the question of brachyuran mono-

phyly include the analysis of larval features (e.g. Williamson,

1976; Williamson and Rice, 1996; Rice, 1980; 1981a; 1981b;

1983; Martin, 1991; McLay et ah, 2001); the fossil record (e.g.

Glaessner, 1969: 439; Schram and Mapes, 1984; Guinot, 1993;

Bishop et al., 1998; Guinot and Tavares, 2001); eye structure

and optics (e.g. Fincham, 1980; 1984; 1988; Gaten, 1998);

spermatozoa ultrastructure (Jamieson, 1990; 1994; Jamieson et

al., 1995; Guinot et al., 1994; 1998); and molecular techniques

(e.g. Spears et al., 1992).

Questions related to the monophyly of the Brachyura are

examined here from a cladistic perspective. One persistent

problem is whether the Podotremata, or part thereof, belongs to

the Brachyura or not. The primitive crabs were formally placed

in the Brachyura by Latreille (1802) (see Guinot and Tavares,

in press). Because primitive crabs share with Anomura the

female gonopore on the coxa of the third pereopod, and their

abdomen and abdominal appendages also share overall similar-

ities, H. Milne Edwards (1832) argued that they should be

transferred from Brachyura to Anomura. Since then, the primi-

tive crabs have been moved to the Anomura or retained in the

Brachyura with each successive revision. A number of taxo-

nomic schemes have been proposed accordingly: e.g. Anomura

Pterygura (true anomurans) versus Anomura Apterura (primi-

tive crabs) (H. Milne Edwards, 1837); Brachyura Anomala

(primitive crabs) versus Brachyura genuina (true crabs)

(Alcock, 1899; Stebbing, 1910); Podotremata (primitive crabs)

versus Eubrachyura (true crabs, Heterotramata -i-

Thoracotremata) (Guinot, 1977; de Saint Laurent, 1980).

Although Guinot’s classification has attained broad acceptance,

the lack of a general consensus on the systematic position of the

primitive crabs has generated substantial instability in the clas-

sification (e.g. Bowman and Abele, 1982; Martin and Davis,

2001). The systematic position of the primitive crabs is a major

concern in decapodology, and the higher classification of both

Anomura and Brachyura cannot be stable while their position

remains unsettled.

The question of whether the Podotremata, or part of it,

belongs or not to the Brachyura is investigated here from a

146

Marcos Tavares

cladistic perspective. Four points are hidden within this issue.

In the way it has been previously formulated, an objective

answer to the question “Do the Podotremata, or part of it,

belongs to the Brachyura” cannot be provided. It must be noted

that the answer entirely depends upon the concept that one

wishes to apply to the Brachyura. Rice (1980: 289) implied as

much when he mentioned that “The position of the more prim-

itive crab-like groups was a particularly contentious problem

during the last century when ... the dromiids, homolids and

raninids individually or collectively, seemed to move in or out

of the Brachyura with each successive revision”. It is worth

noting that the question of whether the Brachyura is mono-

phyletic traditionally appears in terms of groups that should

move in or out. When the problem is approached simply in

terms of “in or out”, the answer cannot be but largely subjec-

tive. Subjectivity arises when one wishes to understand how

two groups (e.g. primitive crabs versus true crabs) are related to

each other: taken alone two groups will always be related to

each other at some level (Fig. 1). Therefore, lumping or split-

ting is largely a subjective decision. In other words, lumping or

splitting depends on the level of generality (Nelson, 1978;

Wiley, 1981: 126) of the character(s) selected to define the

group.

In the case of Brachyura, the assemblage Heterotremata +

Thoracotremata (= Eubrachyura de Saint Laurent, 1980) is

defined by at least two unambiguous synapomorphies, namely

the female sexual opening (vulva) on sternite 6 (Hartnoll, 1968;

Guinot, 1977; 1979; Tavares and Secretan, 1993), and the pres-

ence of a sella turcica (Audouin and Milne Edwards, 1827; H.

Milne Edwards, 1851; Bourne, 1922; Gordon, 1963; Secretan,

1998). If the sternal position of the female sexual opening, and

the sella turcica are used to delimit the Brachyura, the

Podotremata should be removed. However, use of a more gen-

eralised synapomorphy renders possible inclusion of

Podotremata, or part, in the Brachyura. Indeed, since H. Milne

Edwards (1832), parts or all of what is now the Podotremata

have frequently been transferred (to the Anomura) or left in the

Brachyura according to the level of generality of the characters

that have been chosen. The study by Spears et al. (1992: 446)

typically illustrated this situation. They obtained results from

sequence-divergence estimates and phytogenies inferred by

maximum parsimony analyses of aligned nucleotide sequences,

which “suggest that (1) the Raninidae demarcate the lower limit

of the Brachyura, and form a distinct lineage that diverged early

from the lineage leading to other members of this infraorder, as

indicated by a number of autapomorphic characters in the 18S

rRNA molecule; and (2) the Dromiidae should be removed

from the Brachyura...”. From Spears et al.’s (1992) results it

follows that there are three possible solutions to “demarcate the

lower limit of the Brachyura”: (1) set the lower limit at the base

of the branch that unites the Heterotremata with the

Thoracotremata; (2) set the lower limit, as Spears et al. (1992)

did, at the base of the branch that unites the Raninidae with the

group (Heterotremata + Thoracotremata); and (3) set the lower

limit at the base of the branch that unites part of the Dromiidae

with the group Raninidae + (Heterotremata + Thoracotremata).

All solutions are equivalent but which one is to be retained

depends entirely upon the level of generality of the character(s)

chosen to demarcate the Brachyura. Williamson and Rice

(1996: 285) implicitly expressed a similar opinion: “Spears et

al. (1992) interpreted their molecular data as ‘clearly’ exclud-

ing the dromiids from the Brachyura, but the definition of this

group is somewhat arbitrary whether based on morphological

or molecular data. Under a slightly wider definition, the rRNA

data may be interpreted as supporting the inclusion of Dromia,

but not Hypoconcha, in the Brachyura.”

In addition to difficulties inherent to the monophyly of the

Brachyura, one should consider the framework implicit in the

way the problem is posed. From a cladistic perspective, and

depending on the existence or not of evidence for a mono-

phyletic Brachyura (Podotremata + Heterotremata +

Thoracotremata), and/or a monophyletic Podotremata, there are

four assumptions in the traditional discussion. These assump-

tions have so far not been clearly formulated because they have

been confused by the question “Do the Podotremata or part of

it belong in the brachyurans” (Tavares, 1993).

Only when those four assumptions are explicitly taken into

consideration will progress be made towards a better under-

standing of brachyuran interrelationships. While new answers

are not provided herein, it is believed that new questions are

necessary to shed new light on the problem. All four assump-

tions consider that both Heterotremata + Thoracotremata and

the Decapoda are monophyletic (Burkenroad, 1981; Guinot,

1979; Guinot and Tavares, 2001; Schram, 2001).

Assumption 1: The Brachyura (Podotremata +

Heterotremata + Thoracotremata) is monophyletic as is the sub-

clade Podotremata (Fig. 2). The corollary of this assumption is

that the Podotremata is the sister group of Heterotremata +

Thoracotremata group. This means that under assumption 1

there is no issue of which podotreme family is most closely

related to the Heterotremata + Thoracotremata clade. This con-

trasts dramatically with trends in the literature concerned with

establishing the lower limit of the brachyurans.

Scholtz and Richter (1995) proposed seven synapomorphies

of the Brachyura. Guinot and Tavares (2001) suggested that the

double spermatheca (sensu Tavares and Secretan, 1993) consti-

tutes a synapomorphy shared by all Podotremata and not found

in any other Decapoda so far. From the above perspective, it

becomes clear that to concentrate on whether such characters

can really be interpreted as synapomorphies appears more rea-

sonable than to raise questions, a priori, about the lower level

of the brachyurans.

Assumption 2: The Brachyura (Podotremata +

Heterotremata + Thoracotremata) is monophyletic; the

Podotremata is para- or polyphyletic (Fig. 3).

The corollary to this assumption is that at least one of the ten

families currently included in the Podotremata is more closely

related to the Heterotremata + Thoracotremata group than to

the remaining families of Podotremata. Should such be the case

it then becomes relevant to search for the group of podotrema-

tous crabs that is the sister taxon of the eubrachyurans

(Heterotremata + Thoracotremata). The search for the “lower

limit” of the Brachyura only becomes necessary if the “lower

limit” is interpreted to be the most basal branch of the brachyu-

ran clade.

Assumption 3: The Brachyura (Podotremata +

A new approach to the monopoly of Brachyura

147

Bradiyura

Hrachyiira

Brachyura

Pud 0 Ire mala

Assumption 4; corolltiry 1

Assumplion j

Doeapoda

Figure 1 . Synapomorphy “d” supports the inclusion of the Podotremata (P) in the Brachyura, while the use of less generalized synapomorphies

(a, b) in the definition will result in the exclusion of the Podotremata from the Brachyura. Synapomorphies: a, female sexual opening on thoracic

sternite 6; b, presence of sella turcica; c, paired spermatheca; d, intertagmal phragma fused with thoracic interosternite 8/7 (pers. obs.). Other

abbreviations: H, Heterotremata; Th, Thoracotremata.

Figure 2. Assumption 1: both the Brachyura (H + Th + P) and Podotremata (P) are monophyletic. Under assumption 1 it makes no sense to search

for the “lower limit” of the Brachyura. Synapomorphies and abbreviations as in Fig. 1 .

Figure 3. Assumption 2: Brachyura (H + Th + P) monophyletic; Podotremata (P) not monophyletic. Under assumption 2 it becomes meaningful

to search for the sister taxa of the Heterotremata + Thoracotremata clade. Synapomorphies and abbreviations as in Fig. 1 .

Figure 4. Assumption 3: Brachyura (H + Th + P) not monophyletic; Podotremata (P) monophyletic. Under assumption 3 searching for the “lower

limit” of the Brachyura among the Podotremata makes no sense. Synapomorphies and abbreviations as in Fig. 1.

Figure 5. Assumption 4: both Brachyura (H + Th + P) and Podotremata (P) not monophyletic. According to corollary 1 searching for the sister

taxa of the Heterotremata + Thoracotremata clade and searching for the most basal branch of the brachyuran clade becomes truly relevant. Note

that one set of the Podotremata is positioned as paraphyletic complex closely related to the Heterotremata + Thoracotremata clade (H-Th).

Synapomorphies and abbreviations as in Fig. 1 .

Figure 6. Assumption 4; corollary 2. Searching for the most basal branch of the brachyuran clade (“the lower limit”) among the Podotremata is

completely meaningless. Note that none of the Podotremata (P) is closely related to the Heterotremata + Thoracotremata clade; all form a para-

phyletic complex more closely related to some other group of decapods. Synapomorphies and abbreviations as in Fig. 1.

148

Marcos Tavares

Heterotremata + Thoracotremata) are not monophyletic; the

clade Podotremata is monophyletic (Fig. 4). The corollary to

this assumption is that the Podotremata is more closely related

to some other group of decapods (e.g. Anomura), than to the

Heterotremata + Thoracotremata clade. This means that the

name Brachyura would include only the group Heterotremata +

Thoracotremata. Under this assumption, searching for the

lower limit of the Brachyura among the podotrematous crabs

makes no sense.

Assumption 4: The Brachyura (Podotremata +

Heterotremata + Thoracotremata) is not monophyletic; the

Podotremata is not monophyletic (Fig. 5). This assumption has

two corollaries, as far as the Podotremata is concerned. First,

one paraphyletic set of the ten families of Podotremata may be

more closely related to the Heterotremata + Thoracotremata,

with the rest of the families forming another assemblage more

closely related to some other group of decapods (e.g.

Anomura). The Brachyura should then consist of the

Heterotremata + Thoracotremata + the related set of

podotrematous crabs (e.g. families 5-9; Fig. 5). In this case, the

search for the sister taxon of the Heterotremata +

Thoracotremata group, and the search for the most basal branch

of the brachyuran clade, becomes relevant.

Second corollary, none of the Podotremata is closely related

to the Heterotremata + Thoracotremata group. This means that

all Podotremata are a paraphyletic complex closely related to

some other group of decapods (e.g. Anomura) (Fig. 6). The

term Brachyura would then apply only to the Heterotremata +

Thoracotremata group, and a search for the most basal branch

of the brachyuran clade, “the lower limit” among the

Podotremata, is meaningless.

Conclusions

It is worth noting the central role played by the concept of

monophyly of the Podotremata.

If the monophyletic status of the Podotremata cannot be

demonstrated, then it is likely that: (1) at least one family or any

monophyletic assemblage (of nine families at most, out of the

ten existing families of Podotremata) is related to the

Heterotremata + Thoracotremata clade; and (2) the podotreme

families are more closely related to some other group of

decapods (likely the Anomura) than to the Heterotremata +

Thoracotremata.

On the other hand, if the monophyly of the Podotremata is

confirmed it is not possible to have only part of the

Podotremata closely related to the Heterotremata +

Thoracotremata. In that case, all members of the Podotremata

are equally related to the Heterotremata + Thoracotremata

clade or none of them are, and searching for the lower limit of

the brachyurans among the Podotremata is meaningless. In

another words, a priori questions about “the lower limit of the

Brachyura” compromises a far more important and central

question, which is the monophyletic status of the Podotremata.

The “lower limit” issue (the most basal branch of the brachyu-

ran clade) only becomes truly relevant if the monophyletic

status of the Podotremata cannot be demonstrated.

The inclusion of both, the primitive crabs and the

Thalassinidea (since Borradaile, 1903) in the Anomura resulted

in two major obstacles to the stability of higher anomuran clas-

sification. Currently, there is little doubt that the Thalassinidea

should be set apart from the anomurans (Scholtz and Richter,

1995; McLaughlin and Lemaitre, 1997; Tudge, 1997), and thus,

their unlikely return no longer threatens the stability of the

higher classification of anomurans. In contrast, the lingering

uncertainties about the systematic position of the primitive

crabs is a permanent threat to the stability of the higher classi-

fication of both Anomura and Brachyura. It is apparent that this

situation has affected anomuran classification less than

brachyuran classification, even though the Anomura is a much

smaller group. It is a fortune that students of decapod phyto-

geny have refrained from rushing into new taxonomic schemes

for the Anomura until a more clear outline of the decapod tree

history emerges.

Acknowledgements

Early drafts of this manuscript were discussed with Daniele

Guinot (Museum national d’Histoire naturelle, Paris) and Gary

C. B. Poore (Museum Victoria, Melbourne). Criticisms from

Rafael Lemaitre and Christopher Tudge (Smithsonian

Institution, and American University, Washington DC), and

from three referees greatly improved the final draft of the man-

uscript. Paulo Cesar Onofre (Universidade Santa Ursula, Rio de

Janeiro) prepared the illustrations. This research has been sup-

ported by CNPq (process 300915/97-7).

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