CRUSTACEAN RESEARCH, NO. 22 : 11-20. 1993

A new genus of (: )

Rafael Lemaitre

Abstract. — A new monotypic genus, removed from Sympagurus and placed in Bivalvopagurus, is described for Bivalvopagurus, new genus. The new genus Sympagurus sinensis (de Saint Laurent), a is diagnosed and its only redescribed species of Parapaguridae known so far and illustrated. only from the China Sea. The new genus The material used for this study remains is distinguished from other genera in the deposited in the Museum national d'Hist- family by the presence of paired pleopods oire naiurelle. Paris (MNHN), and at the in both sexes, calcification of the shield, National Museum of Natural History, posterior carapace, and tcrgites of the Smithsonian Institution, Washington, D. C. first two abdominal somites, and symmetry (USNM). The following abbreviations are of the uropods and telson. The only species used: SL. length of shield (to the nearest in the new genus commonly uses a bivalve 0.1 mm), measured from the tip of the ros- shell with an actinian as means of par- trum to the midpoint of the posterior mar- tially protecting its abdomen. This species gin of the shield; and MUSORSTOM, expe- is redescribed and illustrated, and some dition of the MNHN and the office de la evolutionary comments are made. Recherche Scientifique et Technique Outre- Mer. Introduction Systematic Account Among the species assigned by Lemaitre F'amily Parapaguridae Smith, 1882 (1989: 37) to the heterogeneous genus Bivalvopagurus new genus Sympagurus Smith, 1883, was Parapagurus sinensis. a species briefly described by de Diagnosis. Shield distinctly broader Saint Laurent (1972) based on two speci- than long, well calcified. Eyestalks stout. mens from the China Sea. The assignment Posterior carapace short (less than length of was made based exclusively on the informa- shield), broad, den.sely setose, calcified. tion contained in de Saint Laurent's descrip- Antennal peduncles and acicles overreach- tion of this species. A recent examination of ing eyestalks; flagellum dorsoventrally the types as well as additional material of flattened; fourth segment armed with dor- this species has brought to light two signifi- sodistal spine. Epistomial spine absent. cant characters not mentioned in de Saint Eleven pairs of phyllobranchiae or interme- Laurent's original description: the presence diate branchiae. Right cheliped elongate; of paired pleopods in both sexes, and the palm rounded mesially, with weakly symmetry of the uropods and telson. These delimited dorsolateral margin. Left che- characters, together with the degree of cal- liped evenly calcified. Ambulatory legs cification of the shield, posterior carapace (second and third pereopods) long, well and tergites of the first and second abdomi- exceeding extended right cheliped; dactyls nal somites, clearly exclude this species from nearly .straight. Abdomen very short in Sympagurus or any other genus of Para- relation to ccphalothorax; tergites of first . Therefore. S. sinensis is herein and second somites well calcified; second 12 R. LEMAITRE somite with left pieuron terminating ventral- ond pleopods in the males and the second in ly in small subtriangular lobe. Telson and the females, are paired, and the telson and uropods symmetrical. Males with paired uropods are asymmetrical. Additionally, symmetrical first and second pleopods, and the only species in Bivalvopagurus, B. paired asymmetrical third to fifth pleopods; sinensis, most commonly uses a bivalve shell first and second modified as gonopods, first with an actinian to protect its very short with subtriangular distal lobe, second with abdomen, whereas species of short exopod and strongly twisted distal use gastropod shells. segment; third to fifth pleopods biramous on left side, uniramous and reduced on right Bivalvopagurus sinensis side. Females with paired asymmetrical (de Saint Laurent, 1972) second to fifth pleopods, biramous on left Figs. 1-4 side (rami crossed on second to fourth), uniramous and reduced on right side. Parapagurus sinensis de Saint Laurent, 1972: 116, figs. 12,24. Type species. — Parapagurus sinensis de Sympagurus sinensis: Lemaitre, 1989: 37. Saint Laurent, 1972. Type material. — ^ holotype (SL 9.0 Etymology. — A compound name using mm), MNHN Pg. 1238; cf paratype (SL the mollusk class Bivalvia, in reference to 7.3 mm), MNHN Pg. 2239; Fisheries the common usage of a bivalve shell to Research Station Hong Kong, Cruise 7, shield its abdomen by the only species in the Station 55. Transect 172, 16'19.3'N, I14°29' genus. Gender: masculine. E, 220 m, [no date]. Remarks. — This new genus is most Additional material. — Philippines, closely allied to Strobopagurus Lemaitre, MUSORSTOM, Station 50, 25 March 1976, 1989. The two genera share a number of 13°49.2'N, 120°01.8'E, 415-510 m: 2 cf (SL characters: a broad shield, flattened anten- 9.7, 10.3 mm), I ? (SL 9.7 mm), 1 ovig. ^ nular fiagella, slender chelipeds, straight (SL 10.5 mm), USNM 265139; 61 cf (SL 7.0 dactyls of the ambulatory legs, and shape of -12.0 mm), 17 ^ (SL 5.5-9.0 mm), 56 ovig. the first and second pleopods in the males. ^ (SL 6.5-9.5 mm), MNHN. The pattern of lines and sulci on the poste- rior carapace is also similar in both genera, Redescription. — Shield (Fig. la, b) ap- although in Bivalvopagurus they are more proximately 1.3 times as broad as long, marked. However, in several important evenly calcified. Dorsal surface strongly characters, Bivalvopagurus is clearly distinct convex, densely "covered with fine setae. from Strobopagurus. In Bivalvopagurus, the Rostrum bluntly subtriangular, with low shield, posterior carapace, and tergites of dorsal ridge. Anterior margins straight. the first and second abdominal somites, are Lateral projections broadly subtriangular, well calcified. In contrast, in Strobopagurus with small terminal spine and I or 2 small the shield is weakly calcified, and the poste- spines lateral to terminal spine. Antero- rior carapace and abdominal tergites are lateral margins slightly sloping, often with soft, uncalcified. In the new genus, the small spine medially on one side. Lateral rostrum and lateral projections of the shield margins subparallel at least on anterior 1/2, are considerably more developed than in with setose lobe posteriorly. Posterior Strobopagurus. In Bivalvopagurus the margin broadly rounded. Posterior cara- pleopods are paired in both sexes, and the pace shorter than shield, densely covered telson and uropods are symmetrical, where- with fine setae (setae longer on branchio- as in Strobopagurus only the first and sec- stegite); cardiac sulcus extending to poste- A NEW GENUS OF PARAPAGLRIDAE 13

Fig. 1. Bivalvopagurus sinensis (de Saint Laurent, 1972), paralype, male. MNHN Pg. 2239: a, dorsal view of cephalothorax (including cephalic appendages and nnh pereopods), and abdomen showing portion of bivalve shell (s) and actinian wall (arrow); b, shield with cephalic ap(>enduges and anterior portion of branchiostegite, left lateral view; c. left basal antennular segment, dorsal view: d, right antennal peduncle, lateral view; e, ventral view of sternum of thoracic somites (including part of first to third pereopods, and fourth and fifth pereopods), showing bivalve shell (s) with actinian (arrow). Scales equal 4 mm (a, b, d, e), and 2 mm (c). 14 R. LEMAITRE

Fig. 2. Bivahopagurus sinensis (de Saint Laurent, 1972), male (SL 10.3 mm), USNM 265139. Left mouthparts, internal view: a, mandible: b, maxillule; c, maxilla; d, first maxilliped; e, second maxilliped; f, third maxilliped. Scale equals 2 mm. A NEW GENUS OF PARAPAGHRIDAE 15 rior margin of carapace; sulcus cardiobran- with strong ventromesial distal spine. Sec- chialis short, weakly marked; linea ond segment with dorsolateral distal angle anomurica extending posteriorly nearly to produced, terminating in strong spine (occa- margin of carapace, bifurcated anteriorly sionally bifid or with additional small spine near shield (lateral branch of linea weakly ventrally); mesial margin with strong spine marked). on dorsodistal angle. First segment armed Ocular peduncles stout, half length of with 1-2 small spines on lateral face; shield, with short setae dorsally; corneae ventromesial angle produced, terminating in strongly dilated. Ocular acicies subtrian- 3-4 small spines. Antennal acicies exceed- gular, directed upward, terminating in ing distal margin of corneae by about 1/3 strong spine (occasionally bifid on one length of acicle; mesial margin armed with side); separated basally by slightly more 6-12 spines. than basal width of 1 acicle. Chelipeds dissimilar, slender, finely Mandible (Fig. 2a) with 3-segmented setose. Right chelipcd (Fig. 3a) with fingers palp. Maxillule (Fig. 2b) with external lobe crossing at tips when closed, terminating in of endopod weakly developed, internal lobe inwardly curved calcareous claws; cutting with long terminal seta. MaKilla (Fig. 2c) edge of fingers with irregularly sized calcare- with endopod slightly exceeding distal ous teeth. Dactyl about as long as palm, margin of scaphognathite First maxilliped with row of small spines on mesial margin; (Fig. 2d) with endopod subequal to exopod dorsal and ventral faces unarmed except for in distal extension. Second maxilliped (Fig. row of tufts of setae parallel to cutting edge. 2e) without distinguishing characters. Fixed finger with small spines on lateral Third maxilliped (Fig. 20 with crista margin (spines diminishing in size distally dentata formed of 11 corneous-tipped teeth and eventually lacking). Palm distinctly increasing in size proximally; basis with longer than broad (about 1.3 times as long mesial tooth. Sternite of third maxillipeds as-broad); mesial and lateral faces with with small spine on each side of midline. irregular rows of small spines; dorsal sur- Epistomial spine absent. Labral spine pre- face with 2 median longitudinal rows of sent. small spines, and scattered small spines on Antennular peduncle long, slender, lateral half; ventral surface covered with exceeding distal margin of corneae by about small tubercles or spines. Carpus with row 1/4 length of penultimate segment; ventral of spines near dorsodistal margin; dorsal flagellum formed of 5-7 articles Ultimate and dorsomesial margin with row of spines; segment slightly more than twice length of mesial, lateral and ventral faces with numer- penultimate, with scattered setae. Basal ous small spines or tubercles. Merus with segment (Fig. Ic) short, about as broad as row of small spines on dorsal margin; long; lateral face with strong ventromesial ventromesial and ventrolateral margins spine, distal subrectangular lobe armed with armed with small spines. Ischium with I or 2 spines, and 1 small spine proximally. ventral face armed with spines. Coxa with Antennal peduncle (Fig. 1 a, d) exceeding long setae on ventromesial margin, and row distal margin of cornea by about 1/3 length of spines on ventrodistal margin. of fifth segment. Flagellum long, exceeding Left uheliped (Fig. 3b) evenly calcified, dactyls of second and third pereopods; arti- finely setose (setae short on chela, long on cles with pair of very short setae (less than merus and carpus). Fingers crossing at tips half length of I article). Fifth segment when closed, terminating in inwardly unarmed, with row of few setae on lateral curved sharp corneous claws; with scattered and mesial margins. Fourth segment with tufts of setae on dorsal and ventral surfaces; dorsolateral distal spine. Third segment cutting edge of fixed finger with evenly 16 R. LEMAITRE

Fig. 3. Bivalvopagurus sinensis (de Saint Laurent, 1972), paratype, male, MNHN Pg. 2239: a, right cheliped, dorsal view; b, left cheliped, dorsal view; c, right second pereopod, lateral view; d, right third pereopod, lateral view; e, dactyl and propodus of left fourth pereopod, lateral view; f, dactyl and propodus of left fifth perepod, lateral view. Scales equal 4 mm (a-d), and 1 mm (e, 0- sized, small calcareous teeth. Dactyl slight- small tubercles. Carpus with 3 strong spines ly longer than palm; cutting edge with row near dorsodistal margin; dorsal face with 2 of closely set corneous spinules. Palm with longitudinal rows of small spines (1 mesial- lateral and mesial faces with small spines; ly, 1 laterally); mesial and lateral faces with dorsal surface with dorsomedian row of small tubercles or spines. Merus with dor- small spines proximally, and dorsomesial sodistal spine, and ventromesial and row of spines; ventral surface with scattered ventrolateral row of spines. Ischium with A NEW GENUS OF PARAPAGURIDAE 17

Fig. 4. Bivalvopagurus sinensis (de Saint Laurent, 1972), paratype, male, MNHN Pg. 2239. a, male right first pleopod, mesial view; b, male right second pleopod, lateromesial view; c, male left third pleopod, lateral view; d, e, f, male right third (d), fourth (e), and fifth if) pleopods, lateral view; g, uropods and telson, dorsal view. Scales equal I mm (a-c), O.S mm (d-0. and 2 mm (g). ventral face armed with spines. Coxa with corneous claw; ventral margin unarmed, or long setae on ventromesial margin, and row at most with 2 3 minute spinules; with of spines on ventrodistal margin. dorsal row and short dorsomesial distal row Ambulatory legs (second and third per- of setae. Propodi armed with small spines eopods; Fig. 3c, d) long, slender, exceeding dorsally; ventral margin with row of small right cheliped by nearly full length of dactyl tubercles bearing spinules. Carpi with of ambulatory leg. Dactyls long (about 1.4 strong dorsodistal spine and row of spines times as long as propodus), terminating in on dorsal margin. Meri with small tubercles 18 R. LEMAITRE or spines on dorsal and ventral faces (tuber- the South China Sea; 200-415 m. cles and spines larger on ventral than on dorsal face). Meri, carpi, and propodi with Remarks. — In the original description setae dorsally. Ischia with spines on ventral of this species de Saint Laurent (1972: 116- face. Coxae with 2-4 spines on ventral face 118) indicated that only the male holotype near anteroproximal angle. Anterior lobe and female paratype were known. I have of sternite (Fig. le) of third pereopods examined the holotype and paratype, and broadly and narrowly subtriangular, un- have found that they are both males. De armed, setose. Saint Laurent also reported that the first Fourth pereopod (Fig. 3e) subchelate. pleopod of the male exhibits a short Dactyl subtriangular, terminating in strong- exopod, but this is evidently a typographi- ly curved corneous claw, and ventrolaleral cal error as a short exopod is present only row of small scales. Propodal rasp with 1 on the second pleopod of males. row of ovate scales (occasionally with 2 rows on proximal 1/5). Fifth pereopod (Fig. 30 subchelate; propodal rasp forming Evolutionary Comments subtriangular area less than half length of The Parapaguridae, as currently interpret- propodus. Coxae of fourth and fifth per- ed, contains the following genera and num- eopods densely setose, more so in females. ber of species: Parapagurus Smith, 11 Eleven pairs of phyllobranchiate or inter- species; Sympagurus Smith, 28 species and mediate gills. 3 subspecies; Strobopagurus, three species; Uropods (Fig. 4g) with elongated and four monotypic taxa, Tylaspis anomala exopods. Telson (Fig. 4g) divided into Henderson, 1888, Probeebei mirabilis anterior and posterior lobes by weak Boone, 1926, Typhlopagurus foresli de Saint median cleft; terminal margin of posterior Laurent, 1972, and Bivalvopagurus sinensis. lobes separated by shallow, unarmed broad As previously mentioned, Bivalvopagurus is sinus, each lobe with 5-13 small corneous most closely allied to Strobopagurus, as spines. judged by the similarities of the shield, Male left third (Fig. 4c) to fifth pleopods antennular fiagella, dactyls of ambulatory with short exopods; right third to fifth legs, and distinctive first and second pleopods (Fig. 4d, e, 0 reduced to short pleopods in the males. Several other charac- (often inconspicuous) setose buds masked ters exhibited by Bivalvopagurus, are shared by tuft of setae. Female second to fourth with Tylaspis and Probeebei. These charac- pleopods with crossed rami, fifth with short ters include calcification of the shield, pos- exopod (rami not crossed); right pleopods terior carapace and abdomen; tendency reduced to short setose buds (second the towards carcinization; and symmetry of the largest, remaining often inconspicuous). uropods and telson. The presence of these characters in Bivalvopagurus, Tylaspis, and Habitat and symbiotic associations. — Probeebei, however, is not necessarily Most of the specimens examined were found indicative of a close phylogenetic relation- using a small shell of a bivalve mollusk with ship. The calcification of thecephalothorax an unidentified actinian growing on it (Fig. and carcinization are believed to have la, e). The shell covers only part of the evolved independently in various hermit abdomen. The mouth and tentacles of the crab groups (McLaughlin, 1983), and is actinian face the sternum of the hermit, and found in various degrees in members of the walls surround and extend the margins genera of other families (e. g. Paguridae: of the shell. Labidochirus Benedict, Ostraconotus A. Distribution. — So far known only from Milne Edwards; Diogenidae: Tisea A NEW GENUS OF PARAPAGURIDAE 19

Morgan and Forest; Coenobitidae: Birgus Leach). Carcinization also has occurred in Acknowledgments other families, but most notably I wish to thank Alain Crosnier and in the Lithodidae. The symmetry of the Michdle de Saint Laurent for arranging the uropods and telson, in the past considered a loan of type material, and deposition of primitive character (see Russell, 1962), has representative material obtained during the been shown to be a condition influenced by MUSORSTOM Expedition in the USNM. the type of habitat used (e. g cochlean, tubiculous, spongicolous; see McLaughlin & Gunn, 1992, McLaughlin & Lemaitre, Literature Cited 1993). Boone, L.. 1926. l.'nusual deep-sea Crustacea, some The presence of paired pleopods in forms secured by the Arcturus Oceanographic Expedition. Zoological Society Bulletin, 29 Bivahopagurus sinensis is of interest to the (2): 69 72. study of the evolution of these appendages Forest, J , 1987. L.es F'yiochelidae ou "Pagures symmetriques" (Crustacea Coenobitidae). in hermit crabs. In other hermit crab fami- R&ultals des Campagnes MUSORSTOM 3. lies, paired pleopods occur in adults only in Memoires du Museum national d'Histoire naturelle, ser. A. Paris, (Zoologie), 137: 1 254, the family Pylochelidae (see F'orest, 1987). pis. 19. In pylochelids, however, the pleopods differ Henderson. J. R., 1888. Report on the Anomura from those of B. sinensis in being symmetri- collected by H. M. S. Challenger during the years 1873 76. Report on the Scientific Results cal (except in Mixtopagiirus paradoxus A. of the Voyage of H. M. S. Challenger during Milne Edwards), and in that the second to the years 1873-76, Zoology, 27: xi + 221 pp, pis. I 21. fifth pleopods are biramous on both sides. Lemaitre. R., 1989. Revision of the genus Para- According to McLaughlin (1983), pleopod pagurus (Anomura: Paguroidea: Parapagur- evolution in hermit crabs has proceeded idae), including redcscriptions of the western Atlantic species. Zoologische Verhandelingen, first through the practice of concealment 253: I 106. and subsequent protection of the abdomen McLaughlin. P. A., 1983. Hermit crabs — are they reallv polyphylctic ?. Journal of by some external means. In particular, the Biology, i (4): 608-621. use of gastropod shells has led lo the com- ,& Gunn. S. W., 1992. Revision of Pylopagurus and Tomopagurus (Crustacea: plete loss of pleopods on one side, and the Decapoda: Paguridae). with the descriptions of development of asymmetry in the uropods new genera and Npecies. Part IV. Lophopagur- and telson. Bivahopagurus sinensis usually us McLaughlin and Australeremus McLaugh- lin. Memoirs of the Museum of Victoria, S3 protects its abdomen with a bivalve shell (1): 43 99. and an actinian, and its pleopods are paired , & Lemaitre. R., 1993. A review of the hermit crab genus Paguriiia (Decapoda: and asymmetrical, except for the first and Anomura: Paguridae) with descriptions of second pair in males, which are symmetrical three new species. The Raffles Bulletin of and modified as gonopods. If McLaughlin's Zoology, 41 (I): 1-29. Russell, E. S., 1962. The diversity of . An view of pleopod evolution is invoked to evolutionary study. Acta Biotheoretica, 13 explain the pleopod condition of B. sinen- (suppl I): 1 151. Saint Laurent. M.de, 1972. Sur la famille des sis, it would indicate that the ancestor (or Parapaguridac Smith, 1882. Description de ancestors) of this parapagurid used gas- TypMopagurus foresli gen. nov., et de quinze espdces ou sous-esp6ces nouvelles de Para- tropod shells for shelter, but thai a decrease pagurus Smith (Crustacea, Decapoda). Bij- in the use of gastropods shells led to a dragen tot de Dierkunde, 42 (2): 97-123. reduction of pleopods on the right side. Smith, S. I., 1882. XVII. Report on the Crustacea. Part I. Decapoda. Reports on the dredging, Alternatively, it is also possible that the under the supervision of Alexander Agassiz, on presence of rudimentary pleopods on the the east coast of the United States, during the summer of 1880, by the U.S. Coast Survey right side represents an neotenic condition Steamer "Blake" commander J. R. Bartletl U. S. unrelated to a cochlean habitat. N., commanding. Bulletin of the Museum of Comparative Zoology, Harvard College, 10 (I): 20 R. LEMAITRE

1-108. 1883. Preliminary report on the Brachyura and Anomura dredged in deep water off the Department of Invertebrate Zoology, National south coast of New England by the United Museum of Natural History, Smithsonian Institu- States Fish Commission in 1880, 1881, and tion, Washington, D.C. 20S60, USA. 1882. Proceedings of the United States National Museum, 6 (1): 1-57.