ABSTRACT

Among more than 800 known species of hermit crabs, very few have been reported to be able to occupy both spiral and straight microhabitats, i.e., gastropod and scaphopod shells, worm tubes, etc. These species are of interest for understanding the effects of microhabitats on crab morphology.
During routine work with large collections of Parapaguridae, I found specimens of at least five species occupying either gastropod or scaphopod shells: Parapagurus pilosimanus, Parapagurus sp., Sympagurus dimorphus, Oncopagurus minutus, and O. monstrosus. These species usually use spiraled microhabitats, and only rarely straight shells.
Differences in uropod and telson symmetry and in pleopod morphology in specimens of similar size of each species living in straight and spiral habitats were analyzed. The small number of specimens examined does not allow to present a clear conclusion, but it seems that for species that normally live in gastropod shells, living in a straight shell does not, or only slightly, influence telson and uropod symmetry.

INTRODUCTION

Among the more than 800 species of hermit crabs described (McLaughlin, 1983), there are so-called "shell specialists" and "shell generalists" (Hazlett, 1989), i.e., the former prefer shells of one or several gastropod species, whereas the latter use a wide variety of shells. Also, there are species and genera adapted to living in straight shelters, such as scaphopod shells, polychaete tubes, pieces of wood, etc. These include, for instance, Orthopagurus, Discorsopagurus, Paguritta, and Xylopagurus in the Paguridae, and Calcinus in the Diogenidae. However, there are only a few known species that have been documented to be able to occupy both straight and spiral shelters.
In the literature, I found records of only four such species: Australeremis cooki (Filhol, 1883), specimens of which were found in both serpulid tubes and gastropod shells (McLaughlin & Gunn, 1992); Pagurus bernhardus (Linnaeus, 1758), usually occupying gastropod shells but sometimes shells of Dentalium (cf. Selbie, 1921); Discorsopagurus schmitti (Stevens, 1925), normally a tube-dwelling species whose juveniles, under experimental conditions, can enter both spiral and straight shelters (Gherardi & McLaughlin, 1995); and Calcinus tubularis (Linnaeus, 1767), living in both gastropod shells and in tubes (Kinzelbach, 1990; Busato et al., 1998). Some species of Paguristes in the Indian Ocean also occupy both types of shelters (pers. observ.). Other cases of diogenids living in uncommon shelters were reported by Markham (1977): Calcinus verrilli (Rathbun, 1901) in vermetid shells; and Asakura (1987): Calcinus latens (Randall, 1840) in shells of Vermetidae, Conidae, and Cypraeidae.
Such species could provide interesting information concerning the influence of the shelter on crab morphology, and also on their ecology and behaviour.
The deep-water hermit crab family Parapaguridae comprises 63 species, currently assigned to 10 genera and inhabiting the depth range of 50 to 5000 m, being one of the most deep-living families of decapods. While studying parapagurid collections, I found several specimens occupying a variety of straight shelters. These specimens can be assigned to known species, which are usually gastropod shell dwellers. The present paper reports these cases. Whenever possible, the specimens from straight shelters were compared to gastropod shell dwellers of the same species and similar size, obtained from nearby stations. Two parapagurids, up till now known to live only in scaphopod shells — Tsunogaipagurus chuni (Balss, 1911) and Sympagurus spinimanus (Balss, 1911) — have also been examined for this study.

MATERIALS AND METHODS
Below is a list of specimens found in various straight microhabitats. The material remains deposited in the following museums and institutions: P.P. Shirshov Institute of Oceanology, Russian Academy of Sciences, Moscow (IORAN); Zoological Museum of the Moscow Lomonosov State University (ZMUM); Senckenberg-Museum, Frankfurt a. M. (SMF); Museum für Naturkunde, Berlin (MNB); Zoologische Staatssammlung, München (ZMB); and The Natural History Museum, London (NHM).

Abbreviations: SL – shield length, measured from the tip of the rostrum to the midpoint of the posterior edge of the shield; R.V. – research vessel; DTE – Deutsche Tiefsee Expedition; PI – pleopods.

DEEP-SEA HERMIT CRABS IN STRAIGHT SHELLS
Specimens of Normally Shell-Dwelling Species Found in Various Straight Shelters

Parapagurus pilosimanus S.I. Smith, 1879 (fig. 1C)

Description of the species: see Lemaitre (1989).
Material examined: 1 male (SL = 2.1 mm) (IORAN DecPa(48)), R.V. Vityaz II, 2nd cruise, Sta. 161, 28.vi.1982, depth 3340–3440 m, 29°51.1'N 28°07.0'W, North Atlantic, in a scaphopod shell with encrusting zoanthid.
Remarks: PI I: not seen; PI II: paired, symmetrical, biramous; PI III–V: paired, asymmetrical, left biramous, right uniramous, one-segmented. Uropods slightly asymmetrical.

Parapagurus sp. (fig. 1D, E)
Material examined: 1 male (SL = 5.9 mm), 1 ovigerous female (SL = 4.8 mm) (ZMUM, Ma-unident.), R.V. Kurchatov, 2nd cruise, Sta. 23 NS, 28.vi.1967, depth 3500–3040 m, 20°20.5'N 62°10.0'E, Arabian Sea, in scaphopod shells without anthozoan symbionts.
Remarks: Fully developed, adult pleopods. Uropods slightly asymmetrical.



Sympagurus dimorphus (Studer, 1883) (fig. 1B, 2C–F)

Description of the species: see Lemaitre (1989). Description of the specimen: see Zhadan (in press).
Material examined: 1 male (SL = 3.4 mm) (IORAN DecPa(10)), R.V. Vityaz II, 17th cruise, Sta. 2764, 24.xii.1988, depth 910–920 m, 33°10.3'S 43°41.0'E, western Indian Ocean, in a scaphopod shell without anthozoan symbionts.
Remarks: Fully developed, adult pleopods. Uropods asymmetrical.


Oncopagurus minutus (Henderson, 1896) (fig. 2A, B)

Description of the species: see Lemaitre (1996); Zhadan (in press).
Material examined: 1 female (SL = 2.3 mm) (NHM London 1896:9.8.24), HMS Investigator, Sta. 150, 29.xi.1893, depth 719 fathoms (1308.6 m), 7°05'45"N 75°04'00"E, Laccadive Sea, in a scaphopod shell.
Remarks: Fully developed, adult pleopods. Uropods slightly asymmetrical.


Oncopagurus mironovi Zhadan, 1997 (fig. 1A)

Description of the species: see Zhadan (1997).
Material examined: 1 juvenile male (SL = 1.1 mm) (IORAN DecPa(223)), R.V. Professor Stockman, Sta. 1957, 29.iv.1987, depth 570–575 m, 24°56.5'S 88°31.6'W, Sala-y-Gomez, in a pteropod shell.
Remarks: PI I: seen only as small buds; PI II: asymmetrical. Uropods and telson symmetrical. Also, many adult specimens from this station were found living in zoanthid colonies, where pteropod shells or polychaete tubes served as "initial shells" (fig. 1A).


Oncopagurus monstrosus (Alcock, 1894)

Description of the species: see Lemaitre (1996); Zhadan (in press).
Material examined: 2 juveniles (SL = 1.1–1.3 mm), 1 female (SL = 1.5 mm) (SMF 240110), R.V. Meteor, Sta. Me5-267, 13.iii.1987, depth 359–362 m, 13°11.5'N 47°20.5'E, Gulf of Aden, in scaphopod shells.
Remarks:
Juvenile (SL = 1.1 mm): PI I not seen; PI II–V paired, symmetrical, biramous; uropods and telson symmetrical.
Juvenile (SL = 1.3 mm): PI I not seen; PI II paired, incompletely developed; PI III–V unpaired, present only on the left; uropods and telson asymmetrical.
Female (SL = 1.5 mm): fully developed pleopods (female type); uropods and telson asymmetrical.

Parapagurid Species Known Only as Scaphopod Shell

DwellersSympagurus spinimanus (Balss, 1911) (fig. 3a–j)

Description of the species: see Zhadan (in press).
Material examined: Holotype male (SL = 4.3 mm) (MNB 16460), R.V. Valdivia, Sta. DTE-254, 25.iii.1899, depth 977 m, 00°29.0'S 42°47.6'E, off Kenya, in a scaphopod shell.
Remarks: PI I seen only as small buds. Male PI II asymmetrical, probably incompletely developed: left biramous, two-segmented, with exopod; right uniramous, one-segmented. PI III–V paired, asymmetrical: left biramous with short exopods; right uniramous, reduced to short setose buds. Telson only slightly asymmetrical. Uropods asymmetrical, the left slightly larger than the right.


Tsunogaipagurus chuni (Balss, 1911) (fig. 3k–m)

Description of the species: see Osawa (1995, 1996); Zhadan (in press).
Material examined:

• Lectotype male (SL = 7.0 mm) (MNB 16462), R.V. Valdivia, Sta. DTE-253, 25.iii.1899, depth 638 m, 00°27.4'S 42°47.3'E, off Kenya.
• Paralectotypes:
• 1 male (SL = 7.0 mm), 1 female (SL = 5.4 mm) (MNB 16462)
• 1 male (SL = 7.8 mm), 1 female (SL = 5.9 mm) (ZSM 314/1), same data as lectotype
• 1 male (SL = 4.3 mm) (MNB 16461), Sta. DTE-254, 25.iii.1899, depth 977 m, 00°29.0'S 42°47.6'E, off Kenya
• All specimens found in large scaphopod shells.
• Remarks: All specimens with fully developed adult pleopods. Uropods and telson varying from symmetrical to very slightly asymmetrical.

Discussion

Ecological Remarks
Finding a specimen in a straight shelter was always a rare occasion. Therefore, living in straight shells is more likely an exception for species that normally dwell in gastropod shells, likely due to the unavailability of spirally coiled shells. Based on the material listed and some literature data, juveniles appear to use untypical shelters more frequently than adults. However, the actual extent of this phenomenon is unclear, as data on microhabitat use are often unavailable or unreported.

Morphological remarks

The question "How does the habitat influence hermit crab morphology?" has been discussed in literature for a long time (Agassiz, 1875; Thompson, 1903; Balss, 1912; Makarov, 1938). Species which can live in both straight and spiral microhabitats seem to be good objects for studying this problem. But there are few works considering this aspect. McLaughlin & Gunn (1992) mentioned that specimens of Australeremus cooki from polychaete tubes had symmetrical uropods and telson, whereas in specimens from gastropod shells these are asymmetrical. Gherardi & McLaughlin (1995) studied larval and early juvenile development of Discorsopagurus schmitti, normally a tube-dwelling crab. The authors offered the juveniles various housings, such as polychaete tubes and gastropod shells, in order to find possible morphological differences between specimens using various types of housing. They found no significant differences in morphology and in developmental processes between the two groups of crabs: in both groups, for example, uropods and telsons were symmetrical. At the same time, variability in pleopod and uropod development within each group was quite high.
From the specimens studied and numerous comparative material, I tried to analyze the influence of the straight shelter on three characters: shape of body and abdomen; shape of uropods and telson; and pleopod morphology.

1. Body and abdomen.
In all specimens from straight shelters, the abdomen and the whole body were absolutely straight (figs. 1B-D, 2C), but the question is whether this is a predetermined condition or under the influence of habitat (Gherardi & McLaughlin, 1995). Another notable peculiarity of parapagurids can help answer this question. It is well known that many parapagurids live in symbiosis with zoanthids, which build shelters for them (Carlgren, 1923; Balss, 1912; Lemaitre, 1989). Presumably, the juvenile hermit occupies a small shell, and a zoanthid larva settles on it. Then, as the crab grows and the shell becomes too small for it, the zoanthid begins to enlarge the shell, adding new whorls to it, and both benefit from this: the crab does not have to search for a new, larger shell, and the zoanthid is not abandoned by the crab. The "initial" shell very soon dissolves or becomes completely embedded in the zoanthid tissue. In large colonies it is not seen from the outside, and the crab lives in a spiral cavity in the cartilaginous colony. The majority of the species of Parapagurus and Sympagurus live in obligatory symbiosis with zoanthids, and so does Oncopagurus mironovi. But in this case, there are juveniles that occupy not only gastropod shells but also pteropod shells and polychaete tubes. One could expect that the shape of the colony will depend on the "initial" shell, as on some trigger, from which the hermit and the zoanthid begin to grow. At least in the case of O. mironovi this is not true. Zoanthid colonies growing on different initial shells, i.e. turbospiral and planospiral gastropod shells and straight polychaete and pteropod tubes, are generally similar in shape (fig. 1A). So, we can conclude that after the hermit begins to grow "freely" outside the "initial" shell, together with the zoanthid, it grows in a certain way that is somewhat turbospiral in shape. The observations performed indicate that possibly the spiral body form of those hermit crabs which normally live in gastropod shells is predetermined.

2. Uropods and telson.
Juveniles cannot be considered here because in species where juvenile development was studied, the asymmetry of the pleopods develops through the first crab stages (McLaughlin et al., 1989). Therefore, for juveniles we cannot say whether symmetry or asymmetry is an effect of shelter or is a normal state for this stage. In all adult or later juvenile specimens from straight shelters (Parapagurus sp., P. pilosimanus, S. dimorphus, O. minutus), uropods and telson were asymmetrical and generally similar to those of conspecific specimens of similar size (fig. 2). So, in these parapagurids, uropod and telson symmetry seems to be a predetermined character also, not or weakly influenced by the habitat. This agrees with the results obtained by Gherardi & McLaughlin (1995). But the position of uropods and telson, at least in preserved specimens, differs between crabs from different shelters. Specimens from gastropod shells have uropods and telson extended and stretched, obviously used for fixation inside the shell, whereas in straight specimens uropods and telson are bent beneath the abdomen and strongly pressed against it (fig. 2D).

3. Pleopod morphology.
In adult specimens from straight shelters pleopods were completely developed and did not differ significantly from gastropod shell-dwelling conspecifics. For juveniles the material is insufficient for any comparison. Furthermore, the variability in pleopod development in juveniles is high (Lemaitre & McLaughlin, 1992; Gherardi & McLaughlin, 1995).
Thus, it seems that in those parapagurid species that are normally gastropod shell dwellers, living in a straight microhabitat influences the shape of the body, but only until the microhabitat is large enough for the hermit to live completely inside it, and this does not or only slightly influence telson and uropod symmetry. In the light of these evaluations, it is interesting to discuss those parapagurids which are known only from scaphopod shells: Tsunogaipagurus chuni and Sympagurus spinimanus. The former is known by seven specimens, five of the type series and two recently found in Japan, while the latter is known only by the holotype. In T. chuni, uropods and telson vary from symmetrical to very slightly asymmetrical (fig. 3I). In pagurids, uropods and telson are symmetrical mainly in those species and genera which are specialized straight shelter dwellers, such as Paguritta spp. (McLaughlin & Lemaitre, 1993) and Discorsopagurus (cf. Gherardi & McLaughlin, 1995). So, we can assume that symmetry of uropods and telson characterizes "true" straight shell dwellers, and T. chuni most probably belongs to this group. Opposite to this, the holotype of S. spinimanus has asymmetrical uropods and telson (fig. 3H-J), incompletely developed male first and second pleopods (fig. 3B, C), and paired asymmetrical pleopods III–V (fig. 3D–G), which may be interpreted as a juvenile condition. This specimen could be an unusual juvenile of a species normally using gastropod shells, adults of which are as yet unknown.

ACKNOWLEDGEMENTS
I thank Dr. Vassily Spiridonov, ZMUM, and Dr. Michael Türkay, SMF, for interesting and helpful discussions on the subject considered in the present paper. I am very grateful to all museums and institutions and their curators who made the material available for me. I thank two anonymous referees for their critical review of the manuscript.

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First received 24 July 1998.
Final version accepted 30 November 1998.