I > 1\27 ~h a -(iOL, PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON 1 1 313 ):761-7 75. 2000. Description of Bermudacaris harti, a new , and species (Crustacea: : ) from anchialine caves of Bermuda

Arthur Anker and Thomas M. lliffe

(AA) Laboratoire de Biologie des Invertkbrks hlarins el Malacologie, hlus6um National a' Histoire Naturelle, 55, rue de Buffon, 75005, P2tih. France, e-mail: anker@mnhn. fr (TMI) Department of Marine Biology, Texas A&hl University at Galveston, Galveston. Texas 77553- 1 675, U.S.A., e-mail: iliffelo tarnug.tamu.edu

Abstract.-A new genus is proposed for an unusual new species of alpheid shrimp, Bermudacaris harti, inhabiting subterranean anehialine caves on the Ber- muda Islands. This unique cavernicolous new species, has been confused with Autonzate dolichognatha, de Man, 1 888, a species widely distributed in tropical marine shallow waters. The new genus sliows some affinities with Automate de Man, 1888 and can be distinguished from the latter genus by several important features, such as subsjrnmetrical first chelipeds with dactylus in ventral position, and presence of appendix masclilina in males. This rew species is unusual among the Alpheidae in the considerable reduction of corneal pigmentation, especially in female, most likely an adaptation to the cave environment. The presence of few large eggs in the female suggests that the new species has low fecundity and abbreviated larval development, which might result from its troglobitic life- style. The relationships of the new genus to Automate are discussed in some detail. Presumably marine ancestors of this troglobitic species entered anchialine cave: from neighborjizg shailow, marine wa~ers.

In an important contributio~to the A rctornate dolichognatha is present1 y knowledge of the cavernicolous caridean considered a widely distributed, pantropical fauna of Bermuda Islands in the Western species found in shallow marine mraters, Atlantic Ocean, Hart & Manning (1981; mainiy on soft substrates (Chace 1972, 453, figs. 56-77) reported Autonzate doli- 1988; Banner & Banner 1973, Manning & chognatha de Man, 1888 from an anchia- Chace 1990). Har; & Manning ( 198 1) is the line cave near Tucker's Town. Hart & Man- first and only report of a member of the ning reported two specimens, and included genus Acctomate de Man, 1888 from caves, short comments on spinulation of pereio- and the authors suggested that the Bermu- pods, branchial formula and color. AI- dan caves could be an "unusual anchialine though a full description of these specime~is habitat" for this species. was not provided, the figures alone were During a \isit to the Smithsonian Insti- sufficient to raise suspicions concerning tution, Washington, D.C. in 1999, the first their identity. Possibly, the two specimens a~thorwas able to examine the two speci- were misidentified because A. dolic.hogrza- mens from Bermuda. A third specimen ttza had been previously reported from identified as Automate dolichognatha, an coastal waters of Bermuda by Markham & ovigerous female, was collected in 1582 in McDermott (1 980, as A. gardineri Couti- Christie's Cave, Bermuda. After compari- &re). Molthuis (1993) used Hart & Man- :,ens of these ~hreespecimens with those ning's (1 98 1) figures in his recent catalogue reported as Automate dolichognatha from of caridean genera. Ascension Isiand by Manning & Chace 762 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

(1990), and with several other specimens rounded. Eyestalks subconical, anterior por- reported by Chace ( 1972, as A. gardineri), tion visible in dorsal and lateral views, cor- we have concluded, that the Bermuda spec- neal pigmentation reduced or absent. Man- imens are not A. dolichognatha, but a new dible with normally developed incisor and undescribed species having several impor- molar processes, and with 2-segmented tant features which do not agree with the palp. Ultimate segment of third maxilliped generic diagnosis of Automate de Man, distally armed with slender spines. First pe- 1888, as given by de Man (1 888), Banner reiopods subsymmetrical, equal in size, car- & Banner (1973) and Chace (1988). These ried extended and elevated, with dactylus three specimens could not be assigned to situated ventrally; chelae laterally com- any genus in the Alpheidae, although the pressed, without significant armature; ad- presence of the distinct cardiac notch and hesive discs and linea impressa absent. Sec- the robust first chelipeds clearly indicate ond pereiopods with 5-segmented carpus, that they belong to this family. Therefore, second article longest. Third pereiopods a new monotypic alpheid genus is estab- with dactylus simple, propodus armed with lished herein for this new species. spines. Sixth abdominal segment without articulated plate. Second pleopods of male Material and Methods with appendix interna and appendix mas- culina. Telson distally truncated, with 2 Specimens were examined and dissected pairs of spines on postero-lateral margin; with the aid of binocular microscope and anal tubercles absent. Branchial formula: all original illustrations were made using a pleurobranchs on P 1-5, podobranch on camera lucida. The material used in this Mxp2, arthrobranch on Mxp3, epipods on study remains deposited in the National Mxp 1-3 and P 1-4, setobranchs on PI -5, ex- Museum of Natural History, Smithsonian opods on Mxp 1 -3. Institution, Washington D.C. (USNM), and Type species.--Bermudacaris harti, new in the Muskum National d'Histoire Natu- species. relle, Paris (MNHN). Species included.-Only the type-spe- Measurements of carapace length (CL) cies. and total length (TL) are in millimeters. Etymology.--Generic name derived from Other abbrevia1.jons used in the text: P = the locality of collection, Bermuda Island, pereiopod, Mxp = maxilliped. and the Greek karis, shrimp. Gender is fem- The following specimens were used for inine. comparison: Automate dolichognatha de Man, 1 888, Ascension Island, Atlantic Bermudacaris harti, new species Ocean (USNM 256773), Caribbean Sea Figs. 1-4 (USNM 136069, reported as A. gardineri Coutikre by Chace 1972), Madagascar Automate dolichognatha-Hart & Man- (MNHN 4567, 457 1 ); Automate evermanni ning, 198 1 :44 1, 453, figs. 56-77.-Hol- Rathbun, 1901, Principe Island, Gulf of thuis, 1986:592; 1993: 198, fig. 190 (in Guinea (MNHN 3450). part.).--Manning & Hart, I989:3 13. Automate cf. dolichognatha-Iliffe, Family Alpheidae Rafinesque, 18 1 5 1994:420.--Hobbs, 1994:98, 102 (not Automate dolichognatha de Man, 1888) Bermudacaris, new genus Material examined.--Holotype: oviger- Diagnosis.-Carapace slightly com- ous female (CL 3.9, TL 1 1.3, Bermuda Isl., pressed laterally, smooth; rostrum devel- Christie's Cave, 24 Oct 1982, coll. T. M. oped as broadly rounded median projection; Iliffe, (specimen in excellent condition, not orbital teeth lacking; pterygostomial region dissected, with both first pereiopods at- VOLUME 1 13. NUMBER 3 tached) (USNM 25078 1 ). Paratypes: male ing antennular peduncle; scaphocerite (CL 2.9, TL 10). Bermuda Isl., Tucker's broadly rounded anteriorly, with strong lat- Town, Tucker's Town Cave, 15 May 1980, eral spine reaching to about middle of car- coll. W. Sterrer and T. M. Iliffe, about 12 pocerite; basicerite with small ventral tooth. m deep (USNM 1 840 1 4); male (CL 3.6, TL Mouthparts not dissected (see paratype 1 I ), Bermuda Isl., Tucker's Town, Tucker's description). Third maxilliped reaching far Town Cave, 26 Aug 1980, coll. T. M. Iliffe beyond antennular peduncle when extend- & C. W. Hart, about 12 m deep (USNM ed; exopod short (about 0.6 of length of an- 184015). tepenultimate segment); antepenultimate Diagnosis.-Frontal margin lacking or- segment flattened proximally, slightly en- bital teeth, with rounded, rostral projection; larged and thickened distally; ultimate seg- subconical eyestalks dorsally exposed, with ment triangular in cross-section, bearing ap- reduced corneal pigmentation; first pereio- proximately 12 semicircular rows of strong pods subequal in size and shape, with dac- setae on mesio-ventral side, and several tylus in inverted (ventral) position; articu- groups of spines on distal half of dorsal lated flap on sixth abdominal segment ab- margin; coxa with blunt lateral plate, and sent. slender strap-like epipod (mastigobranch); Description.--Holotype (Fig. 1 a, b). corresponding articulation surface of Mxp3 Ovigerous female carrying 3 large eggs with small arthrobranch. (maximum size 1.3 X 1 mm). Carapace First pereiopods subsymmetrical and al- smooth, without setae or grooves. Anterior most equal in size, possibly carried elevated margin of carapace with short, broadly and slightly twisted mesially (Fig. la); su- rounded, median rostral projection; orbital perior margin of ischium with 3 distinct spi- teeth lacking; infra-corneal angle only nules curved anteriorly; merus triangular in slightly protruding; pterygostomial angle section, not enlarged or excavated, with rounded; ventral margin of carapace several small spinules on superior margin; straight, without emarginations, not. fringed distal margins of merus rounded, without with setae; posterior margin of carapace acute teeth; carpus cup-shaped, with tiny with well marked cardiac notch. Eyestalks spinules on dorsal margin; chela and carpus subconical, enlarged at base, distal half vis- forming angle about 90" with merus and is- ible in dorsal and lateral views; cornea re- chium; chela smooth, compressed laterally, duced, without pigmentation (Fig. 1 b). palm as long as dactylus; dactylus situated Ocellary beak not distinct. in ventral position; both cutting edges un- Antennular peduncles somewhat flat- armed, with exception of small irregular tened dorso-ventrally; second article slight- teeth proximal to dactylar articulation; fin- ly longer than first, and twice as long as gers apically crossing when closed; superior third article; stylocerite distally acute, only margin of palm and fixed finger bearing slightly overreaching first antennular arti- conspicuous long setae. cle, with statocyst well developed; ventral Second pereiopods very long and slender, carina of first article represented by small reaching far beyond antenna1 peduncle acute tooth, situated on mesial margin prox- when fully extended; merus and ischium imal to second article; strong tooth protrud- elongated and slightly setose; carpus 5-seg- ing from base of first antennular article mented; second segment longest; propor- (only visible in ventro-lateral view); stylo- tions of carpal articles (from proximal to cerite and anterior margins of articles with distal) approximately equal to 10: 16:7:6:7; conspicuous elongated setae; external fla- chelae slender, simple; dactylus slightly gellum not biramous, with fifth to tenth seg- longer than palm; tufts of small setae pres- ments bearing 7 tufts of long aesthetascs. ent on both movable and fixed fingers. Carpocerite of antenna distinctly overreach- Third to fifth pereiopods slender, setose; PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

a

Fig. 1. Bemudacaris harti, new species, a, b, female holotype (USNM 250781). c-j, male paratype (USNM 184014). a, habitus with natural position of legs; b, frontal region in dorsal view; c, habitus; d, e, frontal region in lateral and dorsal views; f, gills; g, telson and uropods; h, detail of uropod diaresis and lateral spine; i, telson, lateral view; j, same, detail of posterior margin. Scales: 1 mm, except for c (2 mm); fig. h without scale. Figs. c, f-i after Hart & Manning, 1981. VOLUME 1 13, NUMBER 3 765 ischium with spine on inferior margin; car- pheidae. Mandible complete, with 2-seg- pus and mews unarmed; propodus of P3 mented palp, well developed molar process, and P4 armed with 6-8 spines on inferior and robust incisor process distally bearing margin, including a pair of slender apical 5 strong teeth. Maxillula with bilobed palp, spines proximal to dactylar articulation; each lobe bearing 1 long plumose seta; in- propodus of P5 more slender, (about 1.5 ferior lacinia with dense cover of setae on times longer than propodus of P3), bearing distal portion (Fig. 4d) Maxilla bearing nar- only few spines and well-developed groom- row scaphognathite fringed with short se- ing brush, composed of about 10-1 2 tufts tae, deeply incised upper lacinia, and small of long setae; dactylus of P3-5 slender, palp. First maxilliped with slender palp sligh~lycurved, without trace of secondary bearing short setae on lateral margin; lower unguis; coxae of PI-4 with strap-like epi- endite with several long plumose setae; ex- pods. opod with rather feebly developed caridean Abdominal segments rounded ventrally; lobe, fringed with plumose setae (Fig. 4g); sixth pleosomite without articulated flap at epipod large and rounded. Second maxilli- postero-ventral angle; margin of preanal ped without distinguishing characters; exo- plate slightly convex, not protruding. First pod elongated; epipod small, mesially with pleopod with reduced endopod. Second to small rounded podobranch (Fig. 4i). fifth pleopod each bearing long appendix Renzarks.-The specimen dissected and interna, reaching distal margin of endopod. illustrated by Hart & Manning (USNM Uropods distinctly exceeding posterior mar- 184014) is in quite poor condition having gin of telson; protopod with acute outer the frontal and anteroventral regions seri- tooth; exopod with diaresis slightly curved, ously damaged, and most legs detached. ending in acute lateral tooth; lateral spine The maxilla and the second maxilliped ap- well developed; endopod without specific pear to be missing. To verify Hart & Man- structures. Telson relatively broad, tapering ning's figures, the mouthparts have been distally, with 2 pairs of dorsal spines situ- dissected and partly illustrated from another ated in its distal half, at some distance from paratype (USNM 184015) in much better lateral margin; posterior margin short, condition. about 0.2 of telson length, almost straight, Two additional specimens collected in with 2 spines at each angle, inner spines the caves of Bermuda Island belong to the about 3 times longer than outer, 1 median new species (field notes by T. M. Tliffe), but pair of very long thickened setae overreach- could not be located in the collections of ing inner spines, and numerous more slen- the USNM. These are not treated as para- der setae directed upwards. Branchial for- types: 1 ovigerous female, CL 4.5 (with 4 mula as given in generic diagnosis. eggs, 1 X 1.7 mm), Green Bay Cave, New Paratypes (Figs. lc-j, 2, 3, 4). Differ Harrington Sound Passage, 27 Aug 198 1, from holotype in external margin of eye- coll D. Williatns, caught by hand while stalks bearing subapically a small but dis- swimming in mid-water about 15 m deep. tinct pigmented area (Fig. Id, e); infra-cor- 1 female, CL 4.4, Bat Cave. Government neal angle of frontal margin of carapace, Quarry, 12 December 198 1, silt substrate at above basicerite, apparently more protrud- 22.5 m., coll T. M. lliffe,. by hand, water ing (incorrectly figured as a small tooth by anoxic between 1 and 10 m, together with Hart & Manning 198 1, fig. 58). Endopod of T?lyhlat_va sp. (not collected) at 10-20 m. second male pleopod bears slender appen- Color in 1zfe.-Uniformly whitish, lack- dix interna and much shorter, stout appen- ing any other color (Hart & Manning 198 1 ). dix masculina, distally bearing strong setae Eggs yellow when collected but brownish (Fig. 2k). after preservation in alcohol. Mouthparts (Fig. 4a-h) typical for Al- Et_vmology.-After Charles Willard Hart PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

Fig. 2. Bennudacaris harti, new species, a-e, h-j, 1-n, paratype (USNM. 184014); f, g, k, paratype (USNM 184015). a, right first pereiopod, external view; b, same, detail of right chela and carpus, mesial view; c, d, left first pereiopod, inner and outer views; e, third maxilliped; f, same, detail of proximal region; g, h, same, details of ultimate segment; i, first pleopod; j, same, detail of endopod; k, second pleopod; 1, antennule, inner view; m, scaphocerite; n, antenna1 peduncle, ventral view. Scales: 1 mm, except figs. f, g, k, m (0.5 mm): figs h-j without scale. (Figs. a, h-j after Hart & Manning, 1981). VOLUME 113, NUMBER 3 767

Fig. 3. Bermudacaris harti, new species, paratype (USNM 184014). a, second pereiopod; b, third pereiopod; c, fourth pereiopod; d, fifth pereiopod; e, detail of apical part of propodus and dactylus of third pereiopod. Scales: 1 mm.

Jr., retired USNM curator, in recognition of sist primarily of inland limestone caves that his research on the decapod fauna of Ber- extend down to sea level and contain tidally mudan caves, and who also collected the influenced brackish pools. More or less ex- holotype. tensive networks of underwater cave pas- Habitat.-More than 90 anchialine caves sages often interconnect these otherwise are known from Bermuda, most of which seemingly isolated cave pools. An exceed- are clustered in the area between Castle ingly rich and diverse troglobitic fauna in- Harbour and Harrington Sound. They con- habits these caves, including more than 50 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

Fig. 4. Bermudacaris harti, new species, a-d, f, paratype (USNM 184014); e, g-i, paratype (USNM 184015). ax, mandible, d, maxillula: e, maxilla; f, first maxilliped; g, same, detail of exopod; h, second maxilliped; i, same in mesial view, detail of podobranch. Scales: 0.5 mm. endemic species (Sket & Iliffe 1980, Iliffe The extensive descriptions of the caves of et al. 1983, Iliffe 1994). Bermuda may be found in Kornicker & 11- Bermudacaris harti has been found in iffe (1989), and Iliffe (1993). Tuckers Town four caves, all located in the northeastern Cave is an isolated cave located on the part of the main island of Bermuda (Fig. 6). Tuckers Town peninsula between Castle VOLUME 1 13. NUMBER 3 769

Harbour and the South Shore of Bermuda. also located along the shoreline of Castle The cave is entered by way of a 13 m deep Harbour. The cave was uncovered during vertical shaft that opens into a dimly illu- quarrying operations in the 1960's. It con- minated. sea level pool measuring 12 by 18 tained two pools reaching depths of at least m. The sand-bottom pool slopes steeply 23 m. In December 198 1, salinity in the down to a large, completely submerged pool was 6.5760 at the surface. 23.0%~at 1 cavern in total darkness with depths to 21 m. 35.2%~at 10 m and 35.7% at 19 m. m. This cavern is about 80 m long by 20 Surface water temperature was 19.1"C, in- m wide, and 10 m high. In October 198 1, creasing to 21.2"C at 19 m. A specimen of salinity in the pool was 22.7%~at the sur- Berrnudacaris harti was collected in 15-20 face. 27.5% at I m, 34.3%~at 10 m and m depths. below a layer of polluted, anoxic 35.5% at 2 1 m. Temperature increased with water. Other troglobitic species from this depth, from 17.8"C at the surface to 2 1 S0C cave include the shrimp T~phlatyailiflei. In at 21 m, while dissolved oxygen decreased 1980, rubbish was bulldozed into one of the from 6.1 1 mlll at the surface to 2.97 at 21 m. Tides in the cave occur 58 minutes later cave pools, grossly polluting the water (11- than tides in the open ocean, and with an iffe et al. 1984). The cave was completely amplitude 62% that of open ocean tides. destroyed by quarrying in the mid 1980's. Specimens of Berrnudacaris harti were col- Green Bay Cave is the longest cave in lected at about 15 m depth. Other notable Bermuda with more than 2 km of explorer troglobitic species in this cave include the underwater passageways. The cave is lo- shrimps Tvphlatya ilifSei Hart & Manning. cated on the peninsula separating Harring- 198 1, Barbouria cubensis (Von Martens, ton Sound from the North Lagoon. It has 1872) and Parhippolyte sterreri (Hart & two entrances, one at the end of Green Bay Manning, 1 98 1 ), the mictacean Mictocaris on Harrington Sound, and another. an in- halope Bowman & Iliffe, 1985, the halo- land sinkhole, known as Cliff Pool. Aver- cyprid ostracods Spelaeoecia berrnudensis age depth in the cave is 18 m. In March Angel & Iliffe. 1987, Micropolycope shx 1982, salinity in the Cliff Pool entrance was Kornicker & Iliffe, 1989 and Polycopissa 21.3% at the surface, 27.3%~at 1 m. 36.2% anax Kornicker & ~liffe,1989, and the cal- at 10 m and 36.3% at 18 m. Surface water anoid copepod Enantiosis sp. temperature was 20.0°C, decreasing to Christie's Cave is located just 30 m from 18.7"C at 18 m. A specimen of Berrnuda- the edge of Castle Harbour. The cave con- caris harti was collected at mid water in 15 tains a clear 8 m-deep pool just inside a m depth from a more hydrologically isolat- collapsed entrance. No cave passages were ed section of the cave. Other troglobitic found extending away from the pool. In Oc- species from this cave include the unique tober 1983. surface salinity in the pool was shrimp Procaris chacei Hart & Manning. 6.9700, increasing to 19.5%0at 1 m. Surface 1986; the halocyprid ostracod Spelaeoecia water temperature was 1 8.2"C7 increasing to bernzudensis; and the mictacean Mictocaris 20.4"C at 1 m. A Berrnudacaris harti spec- - - imen was collected from the bottom in 8 m halope. depth. Other troglobitic species from this Interestingly, two other alpheids have cave include the archiannelid polychaete been found in the Green Bay Cave system, Nerilla sp.; the calanoid copepods Erebo- but to our knowledge this data has never nectes nesioticus Fosshagen & Iliffe, 1985 been published. These are: Svnalpheus cf. and Exurnella sp., and the halocyprid ostra- sanctithornae Coutiere, 1909 (juvenile spec- cods Spelaeoecia berrnudensis and Polv- imen, CL 3.0, in "yellow sponge"), and Al- copissa anax. pheus cf. nornzal~niKingsley, 1878 (small Bat Cave (Government Quarry Cave) is male, CL 3.5). PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

Fig. 5. Automate dolichognatha de Man, 1888 (ax) and A. evermanni Rathbun, 1901 (d, e). a, anterior region of A. dolichognatha from Ascension Isl. (female, USNM 256773); b, abdomen of ovigerous female of A. dolichognatha, probably from Djibouti (after Coutikre, 1899, without scale); c, d, details of ultimate segment of third maxilliped of A. dolichognatha from Madagascar (MNHN 4571) and A. evermanni from Gulf of Guinea (MNHN 3450); e, second maxilliped of A. evermanni in mesial view, detail of podobranch (MNHN 3450). Scales: 1 mm.

Discussion especially enlarged, carried extended, ele- vated, and are almost symmetrical. The The new genus Bermudacaris shares sev- merus is slender, the chela rather slim, the eral characters with Automate de Man, cutting edges of both fingers unarmed, and 1888. In both, the frontal region is similar, the dactylus is situated clearly in ventral po- with partly exposed parallel eyestalks; the sition (Figs. lc, 2b-d). In contrast to Ber- exopod of Mxp3 is short (only slightly mudacaris, all species of Automate possess overreaching distal half of penultimate seg- asymmetrical and unequal first chelipeds ment); the spines on superior margin of ul- (Fig. 5a), with major cheliped bearing en- timate segment of Mxp3 are present; the larged, rounded or rectangular palm, dac- second pereiopod is elongated and has sim- tylus always situated in dorsal position, cut- ilar proportions of carpal articles; and there ting edges of fingers usually armed with is no deep bifurcation on the external fla- large teeth (Fig. 5a), and stout, ventrally ex- gellum of the antennule. Other features cavated merus. common to these two genera are also shared The presence of appendix masculina in by numerous other, not closely related al- male specimens of Bermudacaris harti and pheid genera. its absence in all males of species of Au- Using the most recent key of alpheid tomate (Coutibre 1899, D. M. & A. H. Ban- genera (Holthuis 1993), Bermudacaris ner 1973, pers. obs.) is another feature use- would key out to Automate, but the new ful for the separation of the two genera. As- genus differs from Automate in several im- suming that the presence of an appendix portant points, notably those concerning masculina is a plesiomorphic state for Al- first chelipeds and appendix masculina. The pheidae, and for all , its absence in first chelipeds of Bermudacaris are unique Automate can be explained by a secondary within Alpheidae. In both sexes they are not loss. VOLUME 113, NUMBER 3

Fig. 6. Map of Bermuda Island showing the locations of caves: Tucker's Town, Christie's, Government Quarry and Green Bay Caves.

Other, less stiiking points of difference mate dolichognatha; pleosomites relatively between the new genus and Automate are: well developed and more rounded, partially shape of frontal margin not emarginate in covering large eggs in female of Bermu- Bermudacaris vs. broadly emarginate in dacaris vs. pleosomites weakly developed Automate; shape of eyestalks subconical, in females of Automate (Figs. la, c, 5b). not juxtaposed in Bermudacaris vs. more or For all the reasons cited above, the new less cylindrical, parallel and juxtaposed me- species could not be assigned to Automate sially in Automate; eyes depigmented or without significant changes in the diagnosis with reduced pigmentation in Bermudacaris of this genus. vs. well-pigmented in Automate (Fig. 5a); The observed difference between the fe- small acute antennular carina present in male and the males in the pigmentation of Bermudacaris vs. absent in all species of eyes is highly unusual for alpheids and pos- Automate; third to fifth pereiopods slender sibly for all caridean shrimps. In the holo- in Bermudacaris vs. robust in Automate; is- typic female of Bermudacaris almost no chium of fifth leg with small spine in Ber- pigmented area is apparent on the eyestalks mudacaris vs. unarmed in Automate; few (3 (Fig. lb), while both paratypic males pre- or 4), very large eggs in female of Ber- sent a small, but distinct black spot proxi- mudacaris vs. numerous, small eggs (0.3 X mal to the anterior margin (Fig. le). With 0.5 mrn, Bhuti et al. 1977, Coutikre 1899, only one female specimen, it would be see fig. 5b, pers. obs.) in females of Auto- speculative to suggest a sexual dimorphism 772 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON in pigmentation of cornea, and more spec- very large eggs suggesting highly abbrevi- imens of both sexes are needed to investi- ated development and low fecundity of B. gate further this interesting feature. harti, are features certainly related with the Bervzudacaris harti has a small podob- evolution in an environment characterized ranch inserted near the base of the epipod of by deficiency of light and fluctuation of sa- the second maxilliped. This podobranch was linity. not illustrated by Hart & Manning ( 1981 : It is probable that the Bermudan caves 454, fig. 66), but its existence has been noted were colonized by a marine ancestor of B. in the branchial fortnula. It is generally ab- harti, which could also be those of the mod- sent in all members of the family Alpheidae, ern species of Automate. Indeed, all anchia- but its presence has been shown in many line caves in Bermuda still have an under- Hippolytidae (Coutikre 1899). Within Al- ground connection with the sea as is evi- pheidae a podobranch has been observed in denced by their tidal fluctuations and fully Automate branchialis Holthuis & Gottlieb, marine salinities at depth (Hart & Manning 1958, A. rugosa Coutikre, 1902 (see Wick- 1 98 1 ). Generally, these caves comprise cre- sten 198 1 ), A. anacanthopus de Man, 19 10, vicular habitats in rock extending potential- A. rectifrons Chace, 1972, and A. evermanni ly from the sea surface to the deep sea, Rathbun, 1901 (Fig. 5e), in which it is par- therefore these habitats could have been en- ticularly well developed and acutely pro- tered anywhere in the water column (Man- duced; the podobranch has not been ob- ning et al. 1986). This would explain the served in A. dolichogilatha and is also lack- presence of both deep-sea and shallow wa- ing in A. salomoni Coutihre, 1908. The pres- ter (epigean), or both old and recent forms ence of this podobranch could indicate a in caves. closer relationship of the new genus to spe- Bermuda originated on the Mid-Atlantic cies showing this structure, or in general to Ridge and was formed about 100 million the genus Automate. years ago (Manning et al. 1986). Hart et al. The ultimate segment of the third max- ( 1985) stated that there are significant ties illiped of Beri?~udacarisharti, new species, between marine cave fauna and the fauna bears numerous rows of thick setae on its of deep sea. that caves can contain very old ventral side (Fig. 2h); and strong spines elements ("Mesozoic relicts"), and that along its superior margin (Fig. 2g). Similar they could serve as refuges over long pe- spines are found ir~Automate dolichogiza- riods of time, especially during periods of tha (Fig. 5c). A. evermanni (Fig. 5d), A. glaciation (lliffe et al. 1983). These state- brarzchialis (Holthuis & Gottlieb 1958), A. ments, though partially explaining the dis- anacanthopus and also in other species of tribution patterns of many cave inhabitants, Automate. To our knowledge, this type of can not explain the origin of Bermudacaris. armature has never been observed in other All modern species of Automate (and gen- alpheid genera: when strong spines are pre- erally all Alpheidae) are found in shallow sent on the ultimate segment. they are al- waters, excluding the hypothesis of an an- ways situated on its distal part or on the cestral form coming from the deep sea. apex itself. Also Bermuducaris cannot be considered a Thus, Bermudacaris harti could either relict form. since it shares many characters derive from the ancestors common to both of modern Alpheidae (such as those shared B. and Automate or could represent a with Autoinate). A more probable explana- "highly modified species" of Automate, tion would be the relatively late coloniza- adapted to the unique anchialine cave en- tion of Bermudan caves by a marine, prob- vironment, which is radically different from ably shallow-water ancestor. This ancestor the usual habitat of recent species of Au- frequented crevicular habitats (marine tomate. Almost depigmented eyes, and few caves), from which it could progressively VOLUME 1 13. NUMBER 3 773

penetrate into limestone anchialine caves, in the Pacific Ocean; these are Metabetaeus situated at considerable distance from the Iohena Banner & Banner, 1960 from Ha- sea. waii (Holthuis 1973), and Hamalj9heus A similar hypothesis has been put for- acanthops Bruce & Iliffe, 1991 from Sa- ward by Manning et al. (1986: 160-161), moa. to explain the distribution of two closely In addition to Bermudacaris harti, four related species of Typhlatya. The salt-water other species of troglobitic caridean precursors of modern Typhla~aspecies shrimps from three families inhabit anchia- could frequent crevicular habitats along the line caves of Bermuda: Parhippolyte ster- Mid-Atlantic Ridge while the continents reri, Barbouria cubensis, nphlatya ilzjfei were approximated. Also, Manning et al. and Procaris chacei (Hart & Manning, ( 1986) briefly mentioned that a similar sce- 198 1, 1986), illustrating the relatively high nario could explain the puzzling distribu- level of diversity of this habitat: Procaris tion of the two populations of Procaris in chacei, and Bermudacaris harti seem to be the Atlantic. very uncommon, in contrast to relatively More recently a common littoral crab, abundant Barbouria cubensis and Tjphla- Panopeus Iacustris Schramm, was reported tya iliffei. Only four individuals of Bermu- to be relatively abundant in several Ber- dacris harti were collected in 11 years of mudan caves (Manning & Hart 1989). cave diving in Bermuda by the junior au- Crabs found in caves differed from those thor. Unfortunately, the anchialine caves of living on the open shore in their colour pat- Bermuda are more and more exposed to the tern (being much lighter), and in having lit- anthropogenic activities (Iliffe et al. 1984), tle wear on the fingers of the chelae, pos- but we hope that the unique, endemic cave sibly the initial changes induced by life in fauna of this island group can be preserved a cave environment. for the future generations. Bermudacaris harti is a seventh alpheid reported from crevicular habitats (marine, Acknowledgments anchialine or freshwater), and it seems to be the most adapted to life in caves. Recent The senior author is indebted to R. Le- cave investigations show that Alpheidae maitre (USNM) for assistance during my seem to be relatively well represented in stay at the Smithsonian Institution, and to this particular environment. Other cavernic- the Office of Fellowships and Grants of the olous alpheid species are Potamalpheops Smithsonian Institution for financial sup- stygicola (Hobbs, 1973) from freshwater port, without which this study would not caves in Oaxaca, Mexico (Hobbs 1973, have been possible. Special thanks to C. 1 983); Potarnalpheops pininsulae Bruce & Tudge, for his great help during and after Iliffe 1992 from freshwater lime-stone my stay at the Smithsonian Institution. The caves in Ile des Pins, New Caledonia; Sal- manuscript benefitted considerably from the moneus sketi Fransen, 1992 from marine suggestions made by F? Noel and M. de caves in the nortern Adriatic Sea; Yagero- Saint-Laurent (Museum National d' Histoire caris cozumel Kensley, 1988 from marine Naturelle, Paris, France), S. De Grave (De- caves off Cozumel, western Mexico [trans- partment of Zoology and Ecology, ferred from Hippolytidae to Alpheidae by Aquatic Services Unit, Cork, Ireland), A. L. Chace & Kensley (1 992)], and an undes- Vereshchaka (P.P. Shirshov Institute of cribed species of Potamalpheops from a Oceanology, Russian Academy of Sciences, freshwater cave system in northern Pala- Moscow, Russia), K.-I. Hayashi (National wan, Philippines (Anker, pers. obs.). Two Fisheries University, Shimonoseki, Japan), other stygophilic alpheids have been re- and C. Tudge (American University, Wash- ported from anchialine lava pools and tubes ington D.C., U.S.A.). 774 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

Anchialine cave research in Bermuda 190719 10. part 5: Farnily Alpheidae.-Smith- was supported by grants from the National sonian Contributions to Zoology 466: 1 -99. . & B. Kensley. 1992. The cardiac notch in Science Foundation (DEB-8001 836, BSR- Decapods.-Journal of' Biology 12: 82 15673). the Explorers Club, Earthwatch. 442-447. the National Speleological Society, and the Coutiere. H. 1899. Les "Alpheidae". morphologie ex- Bermuda Government to the junior author. terne et interne. formes larvaires. bionomie.- Appreciation is expressed to Drs. Boris Annales des Sciences Naturelles. Zoologie. ser- Sket, and Wolfgang Sterrer, who assisted ie 8. 9: 1-560, figs. 1409. pls. 1-6. . 1902. Sur quelques especes nouvelles du greatly with the initiation of these investi- genre A~ltotnarclde Man.-Bulletin du Museum gations. Members of the Bermuda Cave d'Histoire Naturelle 8:337-342. Diving Association, especially Robert Pow- . 1908. Sur quelques nouvelles especea er, Paul Hobbs, Derek Gibbons, Mary Van dTAlpheidae.-Bulletin de la Societe Philomat- Soeren and Mark Aspery, helped with cave hique de Paris. serie 9. 10: 191-2 16. . 19OC1. The American species of' Snapping diving collections Shritrlps of the genus SynnIphru,~.-Proceed- ings ol' the United States National Museum Literature Cited 36( 1659 ): 1 -93. Fosshagen. A.. & T. M. Iliffe. 1985. Two new genera of Calanoida and a new order of Copepoda. Pla- Angel. M. V.. & T. M. Iliffe. 1987. Spelaroc.ir1 her- tycopyoida. from marine caves on Bermuda.- rnudrnsis. new genus. new species. a halocyprid Sarsia, 70:345-358. ostracod from marine caves in Bermuda.-Jour- Fransen. C. H. J. M. 1992. Saltnoneu.~skrti. a new nal of Crustacean Biology 754 1553. species of Alpheid shrimp (Crustacea Decapo- Banner. A. H. & D. M. Banner. 1960. Contributions to the Knowledge of the Alpheid Shrimp of the da: Caridea) frorn a submarine cave in the Adri- atic.-Zoologische Mededelingen. Leiden Pacific Ocean. part V11: On Met~ihetaru.sBor- radaiule. with a new species frorn Hawaii.-Pa- 65(1 1):171-179. cific Science 15:299-303. Hart. C. W.. Jr.. & R. B. Manning. 1981. The caver- nicolou:, caridean shrimps from Bermuda (Al- .&- . 1973. The Alpheid Shrimp of Aus- tralia, part I: the lower genera.-Records of the pheidae. Hippolytidae, and Atyidae).-Journal Australian Museum 28( 15):291-382. of Crustacean Biology 1 :44 1-456. Bhuti. G. S.. S. Shakuntala. & K. N. Sankolli. 1977. .&- , 1986. Two new shrimps (Proczri- Laboratory reared algheid larvae of the genera didae and Agostocarididae. new family) frorn Automato. Athanas and S?;nalph~~u.s(Crustacea, marine caves of the western North Atlantic.- Decapoda. Alpheidae).Proceedings of the Journal of Crustacean Biology 6:408-4 16. Symposium on Warm Water Zooplankton, Spe- . & T. M. Iliffe. 1985. The fauna of Atlantic cial Publication UNESCO/NIO, 1977. pp. 588- marine caves: evidence of dispersal by sea floor 600. spreading while maintaining ties to deep wa- Bowman, T. E.. & T. M. Iliffe. 1985. Mic.tocari.s lzul- ters.-Proceedings of the Biological Society of' ope, a new unusual peracaridan crustacean from Washington 98:288-292. marine caves on Bermuda.-Journal of Crusta- Hobbs. H. H.. Jr. 1973. Two new troglobitic shrimps cean Biology 558-73. (Decapoda: Alpheidae and Palaemonidae) from Bruce. A. J. & T. M. Iliffe. 1991. Hamalphr~~sacan- Oaxaca. Mexico.-Association for Mexican thops. new genus. new species. a stygiophilic Cave Studies Bulletin 5:73-80, figs. 1-3. alpheid shrimp from a Samoan lava tube.- . 1983. The African shrimp genus Potamal- Journal of Crustacean Biology I 1583-593. pheops in Mexico (Decapoda: Alpheidae).- .&- . 1992. Potamalphrop,~pininsuluc~ Crustaceana 44:22 1-224. sp. nov., a new stygiophilic shrimp from New Hobbs, H. H., 111. 1994. Biogeography of subterranean Caledonia (Crustacea: Decapoda: Alpheidae).- decapods in North and Central America and the Stygologia 87(4):231-242. Caribbean region (Caridea, Astacidea. Brach- Chace, E A.. Jr 1972. The shrimps of the Smithsonian- yura).-Hydrobiologia 287:95-I 04. Bredin Caribbean Expedition with a summary Holthuis. L. B. 1973. Caridean shrimps found in land- of the West Indian shallow water species (Crus- locked saltwater pools at four Indo-West Pacific tacea Decapoda: Natantia).-Smithsonian Con- localities (Sinai Peninsula. Funafuti Atoll. Maui tributions to Zoology 98: I - 179. and Hawaii Islands). with the description of one . 1988. The Caridean shrimps (Crustacea: De- new genus and four new species.-Zoologische capoda) of the Albatross Philippine Expedition, Verhandelingen, Leiden 128:1-48, pls. 1-7. VOLUME 113. NUMBER 3 775

. 1986. Decapoda. Pp. 589-6 15 it1 L. Botosa- I! from Anchjialine Caves in Bermuda.- neanu. ed., Stygiofauna Mundi. A faunistic. dis- Srnithbonian Contributions to Zoology 475: 1 - tributional. and ecological synthesis of the 88. world Sauna inhabiting subterranean waters (in- Man. J. G. de. 1888. Bericht iiber die von Herrn Dr. cluding the marine interstitial) E.J. Brill. Lei- J. Brock im Indischen Archipel gesammelten den. 740 pp. Decapoden und Stomatopoden.-Archiv fiir . 1993 The recenl genera of the Caridean and Naturgeschichte 53( I ):2 15-600. plc. 7-22a. Stenopodidean Shrimps (Crustacea Decapoda): . 19 10. Diagnoses of new species of Macrurous with an appendix on the order Amphionidacea. Decapod Crustacea from the "Siboga Expedi- Leiden: Nationaal Natuurhistorisch Museum. tion".-Ti-jdschrift der Nederlandsche Dierkun- 328 pp. dige Vereeniging 1 1 (4):287-3 19. . & Gottlieb. E. 1958. An annotated list of the Manning. R. B.. & E A. Chace Jr. 1990. Decapod and Decapod Crustacea of the Mediterranean Coasl Stomatopod Crustacea from Ascension Island. 01' Israel. with an appendix listing the Decapoda South Atlantic Ocean.-Smithsonian Contribu- of' the Eastern Mediterranean.-Bulletin of the tions to Zoology 503: 1-9 1. Research Council of Israel 7B( 1-2): 1-126, pls. , & C. W. Hart. Jr. 1989. The occurrence of 1-3. P~lnoprus1uc.u.stri.s Schramm in marine caves of Iliffe. T. M. 1993. A review of submarine caves and Bermuda.-Crustaceana 57(3):313-3 15. cave biology of Bermuda.-Boletin de la So- . XL T. M. lliffe. 1986. Mesozoic relicts in ma- ciedad Venezolana Espeleologia 27:39-45. rine caves of Bermuda.-Stygologia 2( 112): . 1994. Bermuda. Pp. 3 17-424 in V. Decu, and 156-166. C. Juberthie eds.. Encyclopaedia Biospeologica. Markharn. J. C.. & J. J. McDermott. 1980. A tabulation vol. 1. Society of Biospeleology. Paris. 880 pp. of the Crustacea Decapoda of Bermuda.-Pro- . C. W. Harl. Jr.. & R. B. Manning. 1983. Bio- ceedings of the Biological Society of Washing- geography and the caves of Bermuda.--Nature ton 93: 1266- 1276. 302(5904):141-142. Martens. E. von. 1872. ijber Cubanische Crustaceen . T. D. Jickells. & M. S. Brewer. 1984. Organic nach den Salnmlungen Dr. J. Gund1ach's.-Ar- pollution of an inland marine cave from Ber- chiv fiir Naturgeschichte 38:77-147. muda.-Marine Environmental Research 12: Ratinesque. C. S. 18 15. Analyse de la Nature ou Tab- 173- 189. leau de I'Univers et des Corps organises Paler- Kensley. B. E 1988. New species and records of cave mo. 223 pp. shrimps from the Yucatan Peninsula (Decapoda: Rathbun. M. J. 1901. The Brachyura and Macrura of Agostocarididae and Hippolytidae).-Journal of Puerto Rico.-United States Fish Commission Crustacean Biology 8:688-699. Bulletin 20(2):1- 137. Kingsley. J. S. 1878. A Synopsis of the North Amer- Sltet. B.. & T. M. Iliffe. 1980. Cave fauna of Bermuda. ican Species of the Genus A1phru.s.--Bulletin lnternationale-Revue der gesamten Hydrobiol- of the United States Geological Survey. 4: 189- ogie 65:87 1-882. 199. Wicksten. M. 198 1. Eastern Pacitic species of Auto- Kornicker. L. S.. & T. M. Iliffe. 1989. Ostracoda (My- mrltc~.Proceedingsof the Biological Society of odocopina. Cladocopina. Halocypridina) Main- Washington 94: 1 104- 1 109.