PROCEEDINGS OFTHE BIOLOGICAL SOCIETY OF WASHINGTON 113(3):761-775. 2000. Description of Bermudacaris hard, a new genus, and species (Crustacea: Decapoda: Alpheidae) from anchialine caves of Bermuda Arthur Anker and Thomas M. IHffe (AA) Laboratoire de Biologic des Invertebres Marins et Malacologie, Museum National d'Histoire Naturelle, 55, rue de Buffon, 75005, Paris, France, e-mail: [email protected] A&M (TMI) Department of Marine Biology, Texas University at Galveston, Galveston, Texas 77553-1675, U.S.A., e-mail: [email protected] — Abstract. ^A new genus is proposed for an unusual new species of alpheid shrimp, Bermudacaris harti, inhabiting subterranean anchialine caves ontheBer- muda Islands. This unique cavemicolous new species, has been confused with Automate dolichognatha, de Man, 1888, a species widely distributed in tropical marine shallow waters. The new genus shows some affinities withAutomate de Man, 1888 and can be distinguished from the latter genus by several important features, such as subsymmetrical first chelipeds with dactylus in ventral position, andpresence ofappendix masculinain males. This new 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 Ufe- style. The relationships of the new genus to Automate are discussed in some detail. Presumably marine ancestors ofthis troglobitic species entered anchialine caves from neighboring shallow, marine waters. In an important contribution to the Automate dolichognatha is presently knowledge of the cavemicolous caridean considered a widely distributed, pantropical fauna of Bermuda Islands in the Western species found in shallow marine waters, Atlantic Ocean, Hart & Manning (1981: mainly on soft substrates (Chace 1972, 453, figs. 56—77) reported Automate doli- 1988; Banner & Banner 1973, Manning & chognatha de Man, 1888 from an anchia- Chace 1990). Hart & Manning (1981) is the line cave nearTucker's Town. Hart & Man- first and only report of a member of the ning reported two specimens, and included genus Automate de Man, 1888 from caves, short comments on spinulation of pereio- and the authors suggested that the Bermu- pods, branchial formula and color. Al- dan caves could be an "unusual anchialine though a full description ofthese specimens habitat" for this species. was not provided, the figures alone were During a visit to the Smithsonian Insti- sufficient to raise suspicions concerning tution, Washington, D.C. in 1999, the first their identity. Possibly, the two specimens author was able to examine the two speci- were misidentified because A. dolichogna- mens from Bermuda. A third specimen tha had been previously reported from identified as Automate dolichognatha, an coastal waters of Bermuda by Markham & ovigerous female, was collected in 1982 in McDermott (1980, as A. gardineri Couti- Christie's Cave, Bermuda. After compari- ere). Holthuis (1993) used Hart & Man- sons of these three specimens with those ning's (1981) figures in his recentcatalogue reported as Automate dolichognatha from of caridean genera. Ascension Island by Manning & Chace 762 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OFWASHINGTON (1990), and with several other specimens rounded. Eyestalks subcorneal, anteriorpor- 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. Firstpe- 1888, as given by de Man (1888), 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 lineaimpressa 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 PI-5, podobranch on camera lucida. The material used in this Mxp2, arthrobranch on Mxp3, epipods on study remains deposited in the National Mxpl-3 and Pl-4, setobranchs on Pl-5, ex- Museum of Natural History, Smithsonian opods on Mxpl-—3. Institution, Washington D.C. (USNM), and Type species. Bermudacaris harti, new in the Museum 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 abbreviations used in the text: P = the locality of collection, Bermuda Island, pereiopod, Mxp = maxilliped. and the Greekkaris, shrimp. Genderis fem- The following specimens were used for inine. comparison: Automate dolichognatha de Man, 1888, Ascension Island, Atlantic Bermudacaris harti, new species Ocean (USNM 256773), Caribbean Sea Figs. 1-4 (USNM 136069, reported as A. gardineri Coutiere by Chace 1972), Madagascar Automate dolichognatha—Hart & Man- (MNHN 4567, 4571); Automate evermanni ning, 1981:441, 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, 1989:3—13. Automate cf. dolichognatha Iliffe, Family Alpheidae Rafinesque, 1815 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 1.5), BermudaIsl., 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 113, NUMBER 3 763 tached) (USNM 250781). 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 ventraltooth. m deep (USNM 184014); male (CL 3.6, TL Mouthparts not dissected (see paratype 11), 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- «fe C. W. Hart, about 12 m deep (USNM ed; exopod short (about 0.6 oflength ofan- 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 eyestaUcs dorsally exposed, with ment triangularin 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. la, b). corresponding articulation surface ofMxp3 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 carriedelevated margin of carapace with short, broadly and slightly twisted mesially (Fig. la); su- rounded, median rostral projection; orbital periormargin ofischiumwith 3 distinctspi- 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 halfvis- 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. lb). 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 whenclosed; 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 Secondpereiopods very long and slender, carina of first article represented by small reaching far beyond antennal peduncle acute tooth, situatedon mesial marginprox- 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 notbiramous, with fifthto 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 ofantennadistinctly overreach- Third to fifth pereiopods slender, setose; 764 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OFWASHINGTON Fig. I. Bennudacaris harti, new species, a, b, female holotype (USNM 250781). c-j, maleparatype(USNM 184014). a, habitus with natural position oflegs; 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 ofuropoddiaresis and lateral spine; i, teison, lateral view;j, same, detail ofposterior margin. Scales: 1 mm, except for c (2 mm); fig. h without scale. Figs, c, f-i after Hart & Manning, 1981. VOLUME 113, NUMBER 3 765 ischium with spine on inferior margin; car- pheidae. Mandible complete, with 2-seg- pus and merus unarmed; propodus of P3 mented palp, well developed molarprocess, 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-developedgroom- row scaphognathite fringed with short se- ing brush, composed of about 10-12 tufts tae, deeply incised upper lacinia, and small of long setae; dactylus of P3-5 slender, palp. First maxilliped with slender palp slightly curved, without trace of secondary bearing short setae on lateral margin; lower unguis; coxae of Pl-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 round—ed podobranch (Fig. 4i). fifth pleopod each bearing long appendix Remarks. The specimen dissected and interna, reaching distal margin of endopod. illustrated by Hart & Manning (USNM Uropods distinctly exceeding posteriormar- 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 pejir 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 andpartly illustratedfrom 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. Iliffe), but pair ofvery long thickened setaeoverreach- 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. Ic-j, 2, 3, 4). Differ Harrington Sound Passage, 27 Aug 1981, from holotype in external margin of eye- coll D. Williams, caught by hand while m stalks bearing subapically a small but dis- swimming in mid-water about 15 deep. tinct pigmented area (Fig. Id, e); infira-cor- 1 female, CL 4.4, Bat Cave, Government neal angle of frontal margin of carapace, Quarry, 12 December 1981, silt substrate at above basicerite, apparently more protrud- 22.5 m., coll T M. Iliffe,. by hand, water ing (incorrectly figured as a small tooth by anoxic between 1 and 10 m, together with Hart & Manning 1981, fig. 58). Endopod of Typhlatya sp. (n—ot collected) at 10-20 m. second male pleopod bears slender appen- Color in life. Uniformly whitish, lack- dix interna and much shorter, stout appen- ing any othercolor (Hart & Manning 1981). dix masculina, distally bearing strong setae Eggs yellow when collected but brownish (Fig. 2k). after preservat—ion in alcohol. Mouthparts (Fig. 4a-h) typical for Al- Etymology. After Charles Willard Hart 766 PROCEEDINGS OFTHE BIOLOGICAL SOCIETY OF WASHINGTON Fig. 2. Bermudacaris 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 ofright chela and carpus, mesial view; c, d, left first pereiopod, innerand outer views; e, third maxilliped; f, same, detail ofproximal region; g, h, same, details ofultimate segment; i, first pleopod;j, same, detail ofendopod; k, second pleopod; 1, antennule, inner view; m, scaphocerite; n, antennal peduncle, ventral view. Scales: 1 mm, except figs, f, g, k, m (0.5 mm); figsh-j without scale. (Figs, a, h-j after Hart & Manning, 1981). VOLUME 113, NUMBER 3 767 Fig. 3. Bermudacarisharti, new species, paratype (USNM 184014). a, secondpereiopod; b, thirdpereiopod; c, fourth pereiopod; d, fifth pereiopod; e, detail of apical part of propodus and dactylus of third pereiopod. Scales: 1 mm. USNM Jr., retired curator, in recognition of sist primarily ofinland 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 50 768 PROCEEDINGS OFTHE BIOLOGICAL SOCIETY OF WASHINGTON Fig. 4. Bermudacarisharti, newspecies,a-d, f,paratype(USNM 184014);e,g-i,paratype(USNM 184015). a-c, mandible, d, maxillula; e, maxilla; f, first maxilliped; g, same, detail of exopod; h, second maxilliped; i, same in mesial view, detail ofpodobranch. 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 & Il- 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 ofthe main island ofBermuda (Fig. 6). Tuckers Town peninsula between Castle VOLUME 113, NUMBER 3 769 Harbour and the South Shore of Bermuda. also located along the shoreline of Castle m The cave is entered by way ofa 13 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 1981, salinity in the down to a large, completely submerged pool was 6.5%o at the surface, 23.0%o at 1 cavern in total darkness withmdepths to 21 m, 35.2%o at 10 m and 35.7%o at 19 m. m. This cavern is about 80 long by 20 Surface water temperature was 19.1°C, in- m m wide, and 10 high. In October 1981, creasing to 21.2°C at 19 m. A specimen of salinity in the pool was 22.7%o at thme sur- Bermudacaris harti was collected in 15—20 face, 27.5%o at 1 m, 34.3%o at 10 and m depths, below a layer ofpolluted, anoxic 35.5%o at 21 m. Temperature increasedwith water. Other troglobitic species from this depth, from 17.8°C at the surface to 21.5°C at 21 m, while dissolved oxygen decreased cave include the shrimp Typhlatya ilijfei. In 1980, rubbish was bulldozed into one ofthe from 6.11 ml/1 at the surface to 2.97 at 21 m. Tides in the cave occur 58 minutes later cave pools, grossly polluting the water (II- 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 ofBermudacaris 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 Typhlatya ilijfei Hart & Manning, cated on the peninsula separating Harring- 1981, Barbouria cubensis (Von Martens, ton Sound from the North Lagoon. It has 1872) and Parhippolyte sterreri (Hart & two entrances, one at the end ofGreen Bay Manning, 1981), the mictacean Mictocaris on Harrington Sound, and another, an in- halope Bowman & Diffe, 1985, the halo- land sinkhole, known as Cliff Pool. Aver- cyprid ostracods Spelaeoecia bermudensis age depth in the cave is 18 m. In March Angel & Diffe, 1987, Micropolycope styx 1982, salinity in the CliffPool entrance was Komicker & Diffe, 1989 and Polycopissa 21.3%o at the surface, 27.3%o at 1 m, 36.2%o anax Komicker & Diffe, 1989, and the cal- at 10 m and 36.3%o at 18 m. Surface water anoid copepod Enantiosis sp. temperature was 20.0°C, decreasing to m Christie's Cave is locatedjust 30 from 18.7°C at 18 m. A specimen of Bermuda- 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 fromthepool. In Oc- species from this cave include the unique tober 1983, surface salinity in the pool was & shrimp Procaris chacei Hart Manning, 6.9%o, increasing to 19.5%o at 1 m. Surface 1986; the halocyprid ostracod Spelaeoecia watertemperature was 18.2°C, increasingto A bermudensis; and the mictacean Mictocaris 20.4°C at 1 m. Bermudacaris harti spec- m halope. imen was collected from the bottom in 8 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 & Diffe, 1985 been published. These are: Synalpheus cf. and Exumella sp., and the halocyprid ostra- sanctithomae Coutiere, 1909 (juvenile spec- cods Spelaeoecia bermudensis and Poly- imen, CL 3.0, in "yellow sponge"), andA/- copissa anax. pheus cf. normanni Kingsley, 1878 (small Bat Cave (Government Quarry Cave) is male, CL 3.5). 770 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON Fig. 5. Automate dolichognatha de Man, 1888 (a-c) and A. evermanni Rathbun, 1901 (d, e). a, anterior region ofA. dolichognatha from Ascension Isl. (female, USNM 256773); b, abdomen ofovigerous female of A. dolichognatha, probably from Djibouti (afterCoutiere, 1899, withoutscale); c, d, details ofultimatesegment ofthirdmaxillipedofA. dolichognatha fromMadagascar(MNHN4571) andA. evermannifromGulfofGuinea (MNHN 3450); e, second maxilliped ofA. 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 ventralpo- with partly exposed parallel eyestalks; the sition (Figs. Ic, 2b-d). In contrast to Ber- exopod of Mxp3 is short (only slightly mudacaris, all species ofAutomate possess overreaching distal halfofpenultimate seg- asymmetrical and unequal first chelipeds ment); the spines on superior margin oful- (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 ofcarpal 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 ofBermudacaris harti and pheid genera. its absence in all males of species of Au- Using the most recent key of alpheid tomate (Coutiere 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 ofthe 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 Caridea, 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.