BULLETIN OF MARINE SCIENCE, 51(2): 218-223, 1992

DEEPWATER POPULATIONS OF THE WESTERN ATLANTIC BERMUDENSIS (: CARAPIDAE)

James C. Tyler, C. Richard Robins, C. Lavett Smith and R, Grant Gilmore

ABSTRACT

During operations of the Johnson SEA-LINK submersible in the Lesser Antilles in 1989 and off Belize and Mexico in 1990, we collected sea cucumbers at depths between 45-235 m. Examination revealed a high incidence of tenuis larvae and exceptionally large and deeply pigmented adult pearl fish in Holothuria lentiginosa and Eostichopus arnesoni.

The western Atlantic pearlfish, Carapus bermudensis, is an obligate inquiline in holothurians. Its known geographic range is from Bermuda, southern Florida, and the northeastern Gulf of Mexico through the Caribbean to northern South America (Dawson, 1971; Haburay et al., 1974; Trott, 1981; Valentine and Goeke, 1983). It usually is found in depths of less than 34 m (Smith and Tyler, 1969) but sometimes as deep as 75-80 m off the Atlantic coast of Florida (Miller and Pawson, 1979) and 46 m off Colombia (Koster and Caycedo, 1979). In shallow water its preferred host is Actinopyga agassizi but it also has been recorded from: H%thuria mexicana, H. /entiginosa, Se/enkothuria g/aberrima, and Thee/othuria princeps (all of the preceding in Holothuriidae, Aspidochirotida); Astichopus mul- tifidus and Isostichopus badinotus (both in Stichopodidae, Aspidochirotida); and Thyone sp. (Phyllophoridae, Dendrochirotida) (Trott, 1970; 1981; Smith et a1., 1981; Markle and Olney, 1990, and contained references; above records are given with contemporary generic allocations). Sizes, depths, localities, hosts, infestation rates and catalogue numbers for the SEA-LINKspecimens of C. bermudensis are listed in Table 1. These specimens increase the maximum known depth of occurrence of C. bermudensis from 80 m (Miller and Pawson, 1979) to 235 m (the depth of 150 m given by Markle and Olney, 1990: 374, for Carapus sp., does not apply to C. bermudensis, pers. comm., J. Olney). The SEA-LINKspecimens also include the first reports of C. bermudensis in Eostichopus arnesoni (Family Stichopodidae) and in any member of the family Synallactidae (Mesothuria sp.) (both Aspidochirotida). Since the tail often is truncated, and because tenuis larvae shrink during meta- morphosis to about 113 oftheir maximum length, Smith et al. (1981) used the more reliable head length in their study of 1,174 specimens of C. bermudensis from shallow water at Bimini, Bahamas. The maximum adult size reported by them was 19.5 mm HL. Using a linear regression calculated from the data in their table 1 (TL = 12.6 + 6.89 HL, r = 0.86), this converts to 147 mm TL. Smith et al. (1981) also estimated hypothetical maximum sizes (Laoof the Van Bertalanffy equation) for two cohorts from shallow water to be 19.2 and 22.0 mm HL, roughly equivalent to 144 and 164 mm TL, respectively. This is in good agreement with the maximum size of 165 mm reported by Trott (1970). In their systematic revision of the , Markle and Olney (1990) reported a maximum size for C. bermudensis of 197 mm TL and 26.1 mm HL. This specimen (University of Miami 34558) was collected 75 miles ENE of George- town, Guyana, in a trawl at 52-67 m, 18 May 1968 (R/V CALAMARSTATION413) and is the basis of the maximum size of about 200 mm given by Robins et al.

218 TYLER ET AL.: DEEPWATER PEARLFISH POPULATIONS 219

-N I I I I I "-N

o __ ci. .. ~~-.:-.:l::i "' :t :t:::t:: r.:.ir.:.i:t:::t::r.:.i ~~~~

M C\ONt""- "'" ~ ~~NO ~ ~ ~ ~~O~_~~~NNNN~~~_O~~OO~N-~ ~~~~J~~~~~~~~~~J~=~~~~~~ ~ O~O~-- ~ ~ ~

C\C\","00 00 00 t""- t""- t.:t.:OO 00 ~~ ~~ NN NN UU UU --Cl::Cl:: --Cl::Cl:: 220 BULLETIN OF MARINE SCIENCE, VOL. 51, NO.2, 1992

(1986). Apparently C. bermudensis reaches appreciably larger sizes in water of 45 m and greater depth than in shallow water. All of the adult pearlfish that we have examined that were more than 160 mm TL came from water depths of 45 m and more. However, the three tenuis specimens from deep water holothurians are about the same size as those collected in shallow water, up to 168 mm TL com- pared with 183 mm maximum TL in 47 tenuis from the Bahamas (Smith et ai., 1981). Tbe larger size, deeper pigmentation, and different hosts ofthe deepwater spec- imens collected by the SEA-LINKraised the possibility that they might represent a previously unknown species of western Atlantic Carapus. However, we find no morphological differences between the deepwater specimens and those from shal- low water other than larger size and deeper coloration (nor did Markle and Olney, 1990; most of their specimens were from shallow water, with only a few having been trawled at apparently greater but unspecified depths, pers. comm., J. Olney, with the deepwater specimens not specifically compared with those from shallower water). We consider the specimens from deep and shallow water to be the same species. In both forms the pectoral rays (excluding the dorsal rudimentary ray) number 17 or 18, the abdominal vertebrae are 17 or 18, occasionally 16, and the caudal vertebrae in most specimens with apparently complete tails range from 110 to 115. We are not able to count the dorsal and anal rays because of the lack of ossification posteriorly in our radiographed and cleared and stained specimens but in all other features listed by Markle and Olney (1990)-numbers of dorsal and anal rays anterior to vertebra 31, vertebrae anterior to dorsal and anal origins, and anal rays anterior to dorsal-fin origin-there is complete agreement between the shallow- and deepwater forms. The deepwater specimens have much the same melanophore pattern as those from shallow water but the pigmentation is much more intense (Fig. 1). The following color descriptions were taken from preserved specimens after 2 days in formalin. ADULT.Body translucent, increasingly so toward the thinner attenuate tail re- gion, except for increasing amounts of brownish gray pigment posteriorly along the midlateralline, turning to reddish brown on the distal eighth of the body. Dorsal and anal fins pale, including at the extreme distal tip of the tail, where the pale color of the fins forms a pale border around the deeper reddish brown of this region. Abdomen chalky white, the white extending into interradial membranes of anterior third of anal fin. About 25 to 28 oblong and glistening pearly subsurface markings over the midlateral region of the body from the rear of the head back about two-fifths the length of the body. Pearly markings becoming reduced to small bright spots posteriorly. Abdominal region between the pearly blotches distinctly marked by about five chalky white oblong to oval bars separated by ventral extensions of the dark gray pigment of the midlateral region. Large me- lanophores forming brownish black irregular blotches and bars across the back from the head, along the base of the low to the rear of the tail where the pigment becomes concentrated and incorporated into the reddish brown back- ground. Similar irregular blotches and bars ofmelanophores occur along the lower side of the body and anal-fin base from the end of the abdomen posteriorly but with only a few melanophores along the mid ventral edge ofthe abdomen anterior to the high anal fin. Head densely pigmented in brownish gray from between the eyes to the first of the irregular bars across the back. Glistening pearly subsurface patches on the head, around and posteroventral to the eye, on the opercle, sub- opercle, anteroventral region of the preopercle, and on the lower jaw showing through the overlapping maxilla; silvery color also on the branchiostegals and isthmus. Head with irregular dark gray melanophores scattered over the snout, TYLER ET AL.: DEEPWATER PEARLFISH POPULATIONS 221

Figure 1. Deeply pigmented 165 mm TL adult of Carapus bermudensis from JSL Dive 1773 off Bequia at 64-m depth, AMNH 98277. upper and lower jaws and opercles, least so over the preopercular region. Pink of the gills showing through the branchiostegal and lower opercular area. Pectoral fins pale, with one or two large melanophores at fleshy base. TENUIS.Translucent and colorless except for light scattering of small reddish orange spots over the head and on the abdomen, and along the base of the anal fin. A scattering of darker melanophores on snout, around brain vault and pos- terodorsal region of abdominal cavity. Posteriorly on the body small dark me- lanophores are present along with the orange spots on the base of the anal fin, these small blackish gray melanophores replacing the orange dots at the extreme posterior end ofthe attenuate body. Dark spots also present along the dorsal ridge of the body, unaccompanied by orange. There are relatively few records of C. bermudensis from the southern and western parts of its range. For example, adult pearl fish and their preferred hosts are uncommon in shallow water around Carrie Bow Cay, Belize; we know of only one record of an adult C. bermudensis from Carrie Bow and it (Table 1) was recovered from an Actinopyga agassizi, the preferred host, in water 1-2 m deep. Only two other adults of C. bermudensis have been collected on the Belize Barrier Reef to our knowledge: one (Virginia Institute of Marine Science 8551') at Cay Glory (north of Carrie Bow) from Holothuria mexicana in water 2 m deep; the other (Table 1) at Glovers Reef (east of Carrie Bow) from Eostichopus arnesoni at 37 m depth. In spite of our familiarity with holothurians and many hours of snorkeling in shallow water and scuba diving in deeper water, our own searches for adult pearlfish during many trips to Carrie Bow between 1986 and 1991 have produced only three specimens of Actinopyga, none of which contained a pearlfish. We also have examined more than 50 specimens of other species of holothurians from Carrie Bow without finding a pearlfish. However, we have taken a fair number of free swimming tenuis larvae at Carrie Bow in fixed nets set at night in areas of swift current and in light traps, including one series of 10 individuals from a trap set for 1 h (18:45 to 19:45) on 20 November 1989. We have also collected jelly masses that we suspect to be pearl fish egg rafts on several occasions at Carrie Bow, although these eggs are not sufficiently developed to be identified with certainty. Unless there are hosts that we simply have not located, this appears to be a case where a species with an extremely specialized microhabitat is able to maintain its population in areas where that microhabitat is rare. There are three possible sources of eggs and larvae for the Carrie Bow samples: (I) they are produced by adults in shallow water some distance from the Carrie Bow area; (2) they are produced locally by rare adults around Carrie Bow; or (3) they are produced by deepwater adults and carried by upwelling currents into the shallows along the barrier reef. The fact that the eggs (if they indeed are egg masses 222 BULLETINOFMARINESCIENCE,VOL.51, NO.2, 1992 of pearlfishes) are in early developmental stages would seem to indicate that they were produced locally. The presence of groups of 2 to 10 tenuis in individual samples also would seem to argue against long distance transport in shallow water where bottom turbulence and eddys would tend to disperse larvae. The scarcity of adults in the shallow water habitats of the immediate vicinity would seem to rule out local egg and larvae production. Therefore, we consider it highly likely that the tenuis larvae in our traps came from deepwater individuals. Although none of the deepwater specimens were sexually active, the testes of the larger specimens (AMNH 98277-78) appeared to be normal late stage II as defined by Smith et aI. (1981). We suggest that the eggs and larvae produced by the deepwater pearlfishes drift in the open sea and that some of them are carried onto the reef and into the lagoon. It is apparent that most of the tenuis that arrive at the vicinity of Carrie Bow will be unable to find shallow water hosts and will simply die off or be eaten by predators, although some may be swept back out to sea to settle into deep water where they join the deepwater populations. It is well known that in shallow water C. bermudensis leaves the host at night to feed on (Smith et aI., 1981). At Bear Cut, Dade County, Florida, adults of C. bermudensis have been seined at night, also indicating that the pearlfish leave their hosts to forage openly. In spite of the fact that ichthyologists in the SEA-LINKsubmersible were closely scanning the bottom for fishes, no pearlfish were seen, even though it was continuously dark at those depths and much of the dive time also was during the night-time darkness at the surface. Furthermore, the only food found in the stomachs of the deepwater specimens appeared to be the remains oftenuis larvae. Smith et aI. (1981) commented that cannibalism on tenuis larvae is a major feeding pattern at some times of the year. When volume of prey is considered as well as numbers and frequency of occurrence, the tenuis larvae constitute a major part of the diet, and our limited data suggest that this may be even more important in the deepwater populations. For this obligate inquiline species, cannibalism may well be a highly specialized method of food gathering.

ACKNOWLEDGMENTS

We thank Captain Daniel Schwartz and the crew ofthe R/V SEWARDJOHNSONand the pilots of the Johnson SEA-LINKfor their skill and cooperation in collecting the sea cucumbers from deep water. D. Scheidt, R. Brockmeyer, and M. Peterson provided help in preserving the specimens and took the photograph in Figure 1. D. Tyler collected tenuis larvae in set plankton nets at Carrie Bow Cay. Identifications of holothurians were provided by D. Pawson, Smithsonian Institution, and J. Miller, Harbor Branch Oceanographic Institution, Inc., who also made available to us other lots of pearl fishes collected by the Johnson SEA-LINK.J. Olney offered many useful suggestions in reviewing the manu- script. This is contribution No. 869 of the Harbor Branch Oceanographic Institution, Inc., No. 262 of the Smithsonian Marine Station at Linkport, and No. 341 of the Smithsonian Caribbean Reef Ecosystems Program.

LITERATURECITED

Dawson, C. E. 1971. Records of the pearlfish, Carapus bermudensis, in the northern Gulf of Mexico and ofa new host species. Copeia 1971: 730-731. Haburay, K., R. W. Hastings, D. DeVries and J. Massey. 1974. Tropical marine fishes from Pensacola, Florida. Fla. Sci. 37: 105-109. Koster, F. and E. I. Caycedo. 1979. Primer hallazgo de Astichopus multifidus (Echinodermata: Holothurioidea, Stichopodiidae) y Carapus bermudensis (Pisces: , Carapidae) en el Caribe colombiano, con notas sobre esta nueva asociacion. Bol. Mus. del Mar (Univ. Bogota, Jorge Tadeo Lozano) 9: 30-36. TYLERETAL.:DEEPWATERPEARLFISHPOPULATIONS 223

Markle, D. F. and J. E. Olney. 1990. Systematics of the pearlfishes (Pisces: Carapidae). Bull. Mar. Sci. 47: 269-410. Miller, J. E. and D. L. Pawson. 1979. A new subspecies of Holothuria lentiginosa Marenzeller from the Western Atlantic (Echinodermata: Holothuroidea). Proc. BioI. Soc. Wash. 91: 912- 922. Robins, C. R., G. C. Ray and J. Douglass. 1986. A field guide to Atlantic Coast fishes of North America. Peterson Field Guide Series No. 32. Houghton Mifflin Company, Boston. 354 pp. Smith, C. L. and J. C. Tyler. 1969. Observations on the commensal relationships of the western Atlantic pearlfish, Carapus bermudensis, and holothurians. Copeia 1969( I): 206-208. --, -- and M. N. Feinberg. 1981. Population ecology and biology of the pearl fish (Carapus bermudensis) in the lagoon at Bimini, Bahamas. Bull. Mar. Sci. 31: 876-902. Trott, L. B. 1970. Contributions to the biology of carapid fishes (: Gadiformes). Univ. Calif. Publ. Zool. 89: 1-41, pis. 1-16. --. 1981. A general review of the pearlfishes (Pisces, Carapidae). Bull. Mar. Sci. 31: 623-629. Valentine, J. F. and G. D. Goeke. 1983. First record of Holothuria lentiginosa enodis Miller and Pawson (Echinodermata: Holothuroidea) in the northern Gulf of Mexico. Northeast Gulf Sci. 6(2): 155-156.

DATEACCEPTED: November 19, 1991.

ADDRESSES:(J.C.T.) National Museum oJNatural History, Smithsonian Institution, Washington D.C. 20560; (C.R.R.) Rosenstiel School oj Marine and Atmospheric Science, University oj Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149-1098; (C.L.S.) Department oj Herpetology and Ich- thyology, American Museum oJNatural History, New York, New York 10024; (R.G.G.) Harbor Branch Oceanographic Institution, Inc., 5600 Old Dixi Highway, Fort Pierce, Florida 33946.