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Home , Charybdis (crab), Charybdis hellerii

28 December 1995 PROCEEDINGS OF THE BIOLOGICAI. SOCIETY OF WASHINGTON 108(4):643-648. 1995 hellerii (Milne Edwards, 1867), a nonindigenous portunid crab (Crustacea: : Brachyura) discovered in the Indian River lagoon system of

Rafael Lemaitre Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560, U.S.A.

Abstract.—The portunid crab (Milne Edwards, 1867), a species of Indo-Pacilic origin, is reported from the Indian River lagoon system of Florida. Although this species was reported in 1987-1988 from , Co- lombia, and , this is the fii^t subsequent record in the western At- lantic, and the first in the continental . The specimens found in the Indian River include adults of both sexes (one female ovigerous), and juveniles, indicating that the population is reproducing and that this nonindig- enous species has become established in the region. This species must now be considered present in the tropical western Atlantic at least across the entire Caribbean region. Recognition characters of C. hellerii are provided, as well as a summary of what is known about its distribution, biology, and probable method of arrival. Comments on other marine decapods introduced in eastern North America are included.

On 20 April 1995, two adult specimens, kay (1989) where it was also collected in a male and an ovigerous female of Charyb- 1988. Although there have been no subse- dis hellerii (Milne Edwards, 1867), a species quent published reports of this species, it has of Indo-Pacific origin, were caught in baited been found repeatedly since 1988 in the traps in the Indian River lagoon system of Santa Marta area of Colombia (N. H. Cam- Florida in the vicinity of the Ft. Pierce Inlet. pos, pers. comm.). The present report of C. The male, 74 X 49 mm of carapace width hellerii in eastern North America extends the X carapace length, remained alive in an range of this species in the western Atlantic aquarium for over a month until it was sac- across the Caribbean region, to include sub- rificed. The ovigerous female (.54 X 39 mm), tropical Florida. died the same day it was captured. Follow- Keys for the identification of species of ing an announcement at The So- Charybdis as well as illustrations of C. hel- ciety's summer meeting (Lemaitre 1995) of lerii, are available in a number of publica- the discovery of these specimens, several re- tions (e.g., Chopra 1935, Leene 1938, Ste- searchers (see names in acknowledgments) phenson et al. 1957, Stephenson 1972, G6- working in the Indian River during the pe- mez & Martinez-Iglesias 1990). However, for riod May-August 1995, informed me that the benefit of researchers working in the New they had found additional adults and juve- World who may not have easy access to the niles in the Sebastian and Fort Pierce Inlets. earlier, more detailed taxonomic references, it Charybdis hellerii was first collected in seems appropriate to include here the most the western Atlantic in 1987 (Fig. I), in important recognition characters of this new- Cuba by G6mez & Martfnez-Iglesias (1990), ly introduced species. Such information may in Venezuela by Hem^dez & Bolaiios facilitate future discovery and monitoring of (1995), and in Colombia by Campos & Tiir- populations of this portunid crab. 644 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

Fig. 1. Map showing collecting dates and locations of capture of Charybdis hellerii (Milne Edwards, 1867) in chronological order: 1, 2, Cuba: NE coast, Bahta Gibara (Provincia Holgufn), and S coast, Bahfa Cienfuegos (Provincia Cienfuegos) (G6mez & Martfnez-Iglesias 1990); 3, NE Venezuela: Ensenada de "nirpialito, Golfo de Cariaco (Estado Sucre) (Hem&ndez & Bolaiios 1995); 4, 5, Colombia: Bahfa de Portete (Guajira). and Bahfa Chengue (Magdalena) (Campos & TUrkay 1989); 6, eastern USA: Indian River, Ft. Pierce, Florida (this report).

Method of capture.—The traps used were north of South Bridge (about 20 m from the cylindrical, and consisted of 50 cm-long mainland shoreline, in 4 m depth). After sections of PVC pipe of 20 cm diameter. capture, the specimens were transported to The ends of each cylinder trap were fitted the laboratories of the Smithsonian Marine with cone entrances made of galvanized Station at Link Port, Florida. The adult hardware cloth with a 1 cm mesh size. The male and ovigerous female specimens have cones were placed at each end with the nar- been deposited in the collections of the Na- row end facing the inside of the pipe. A tional Museum of Natural History, Smith- small plastic bait basket was tied in the sonian Institution, Washington, D.C., under midsection of each trap. Bait used was mul- catalogue number USNM 275907. let, purchased locally. Arrays of four traps were fixed to a long line, with a 20 kg lead Family weight on each end of the line. Two such Charybdis hellerii (Milne Edwards, 1867) arrays were left overnight in the vicinity of Figs. 1, 2 the Ft. Pierce Inlet: one in a channel south of Little Jim Island (in 1.5 m depth); and Recognition characters.—Carapace with another in the Ft. Pierce turning basin just dorsal surface naked; anterolateral margin VOLUME 108, NUMBER 4 64S

^ *—"^ 4 ylt^^^F l'-^^ W%^... E^^l )Wf WL^^m-r^ ^ ^I^^^^^S^^^^^^K' J. ic£:l«% "^ u>» ^ IT Fig. 2. Charybdis hellerii (Milne Edwards, 1867), male (74 X 49 mm), channel south of Little Jim Island, Ft. Pierce, Florida, USNM 275907. with 6 sharp, black-tipped teeth (including for light purple area on upper, inner surface outer orbital). Frontal region with 6 prom- of palm, and dark purple on dorsal surfaces inent teeth: 2 inner orbitals plus 4 blunt of distal 4 segments of walking and swim- submedians, latter reaching slightly in ad- ming legs. Carapace with pale green or whit- vance of orbitals. Chela stout; palm with 5 ish areas on frontal, hepatic and epibranchial strong black-tipped spines on dorsal face. regions. Fingers of chelipeds dark purple. Swimming leg with merus and carpus each Distribution.—Indo-Pacific: , Phil- armed with strong black-tipped spine on ippines, , , , posterior margin distally; propodus with and throughout the , including row of spines on posterior margin. Sixth ab- the (Stephenson 1972, Kathirvel & dominal segment of male about as broad as Gopalakrishnan 1974, Vannini 1976, Javed long, posterodistal margins rounded; telson & Mustaquim 1994). Eastern Mediterranean: bluntly triangular, basal width less than dis- Israel, and Egypt (Steinitz 1929, Galil 1992). tal width of sixth abdominal segment. Male Western Atlantic: eastern Florida, Cuba, Co- first gonopods, when viewed in situ, reach- lombia, and Venezuela (Campos & Tiirkay ing approximately to suture between fifth 1989, G6mez & Martfnez-Iglesias 1990, and sixth thoracic somite, diverging in dis- Hemdndez & Bolafios 1995, this report). tal third; each with row of about 25 slender Biology.—This species is considered spines on lateral margin distally (spines di- commercial in southeast Asia (Moosa minishing in length distally). 1981). Not much is known about its biol- Coloration.—Overall dark green except ogy. The larvae of C. hellerii, for example. 646 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON have not been described. Other species of Iglesias (1990:71), it is also possible that Charybdis for which the complete larval this species was introduced in one or more development is known, have five to six sites and subsequently dispersed via larval zoeal stages and a megalopa (Greenwood & stages to various other coastal environments Fielder 1980). Fecundity of C. hellerii, as in the region. expressed by number of eggs, has been re- Presence in the Indian River of adults, in- ported to range from 22,517 to 292,050 cluding at least one ovigerous female, and eggs per female (Siddiqui & Ahmed 1992). juveniles, leaves little doubt that a reproduc- Other congeneric species (e.g., C. cruciata, ing population exists in this area and that the C. hoplites pusilla, C. natator, C. feriatus) species is already established. The scant in- with biology probably similar to that of C. formation available on the biology of C. hel- hellerii, are known to spawn year round but lerii indicates the potential of this species to with peaks in early spring and fall, and have successfully colonize marine ecosystems of fecundities ranging from 181,230 to South Florida and the . 3,200,000 million eggs per female (Pillai & Marine decapods introduced in eastern Nair 1970, 1976; Campbell 1984; Sumpton North America.—Charybdis hellerii is the 1990). Charybdis hellerii prefers soft bot- third marine decapod to be introduced and tom, although it is also found in rocky bot- become established in the North American tom and among live coral, and ranges from Atliuitic coast. The other two being the west- the intertidal to 51 m in depth (Stephenson em Pacific grapsid crab Hemigrapsus san- et al. 1957, Galil 1992). Javed & Musta- guineus (see Williams & McDermott 1990, quim (1994) recently reported specimens of McDermott 1991), and the European portun- C. hellerii from Pakistan that were carrying id crab Carcinus maenas (see Hedgpeth acorn barnacles (Chelonibia patula) on the 1993, Carlton & Geller 1993, Cohen et al. carapace and chelipeds. 1995, Carlton & Cohen 1996). Hemigrapsus Timing and method of introduction.— sanguineus is now known from Cape Cod Reports on the presence of C. hellerii in the to Chesapeake Bay (J. T. Carlton, G. Ruiz, Caribbean and Florida suggest that the ar- A. H. Hines, Jr., pers. comms.). Carcinus rival of this species in the region occurred maenas is the oldest decapod introduction to in relatively recent times, probably in the eastern North America. This species is late 1980's (see Fig. 1). Campos & Turkay known to have been present in eastern North (1989), and G6mez & Martfnez-Iglesias America at least since the early 1800's, al- (1990), observed that the presence of C. though it was then known under the name hellerii in Colombia and Cuba was corre- lated with increased ship traffic coming Cancer granulatus Say, 1817 [see Rathbun from the eastern Mediterranean where this 1930:15, under Carcinides maenas (Linnae- species migrated via the Suez Canal and is us)]. By the late 1800's, C. maenas was well now firmly established (Steinitz 1929, Galil established from Cape Cod to New Jersey 1992). Campos & Turkay (1989:122) indi- (Smith 1879), and currently is known to be cated the possibility that the species arrived established from Nova Scotia to New Jersey in ballast water or "clinging to the ships (Cohen et al. 1995). It has also been intro- trunk". Transport in ballast water is the duced to and is established in Australia, most probable explanation for the arrival of South Africa, Japan, and Pacific North this species to the Caribbean and eastern America (Le Roux et al. 1990, Carlton & Florida. It is unlikely that crabs could cling Cohen 1996). Curiously, the older published to the hull of any modem ship, although information on this species does not mention crabs could be transported by ships in how it reached eastem North America. Re- fouled sea chests or fouled seawater intake cently, Cohen et al. (1995) have indicated pipes. As suggested by G6mez & Martfnez- that the global dispersal of C. maenas ap- VOLUME 108, NUMBER 4 647 pears to be linked to the movement of fouled improved the manuscript. The following in- and bored wooden ships. dividuals also supplied useful information: At least five other marine decapods have Dave K. Camp (Florida Marine Research been considered in the literature as "intro- Institute, St. Petersburg, Florida), A. J. duced" in eastern North America but have Provenzano, Jr. (Old Dominion University, not become established. Of these, two Indo- Norfolk, Virginia), M. Tavares (Universi- West Pacific penaeids {Penaeus japonicus, dade Sta. Ursula. Rio de Janeiro, ), E. P. monodon) and two eastern Pacific pen- L. Wenner (Marine Resources Research In- aeids (P. stylirostris, P. vannamei) are cul- stitute, Charleston, ), A. B. tured extensively in South Carolina, Flori- Williams (National Marine Fisheries Ser- da, and Texas, and while specimens of the vice, Washington, D.C.), and J. D. Williams latter three have been found in the wild as (National Biological Survey, Gainesville, escapees from the shrimp farms, no repro- Florida). This study was supported by the ducing populations have been reported Smithsonian Marine Station at Link Port, (Wenner & Knott 1992). The Asian Erioch- Ft. Pierce, Florida, and is contribution no. eir sinensis or "Chinese mitten crab", is 387 from that Station. believed to have arrived to eastern North America in ship ballast water (Nepszy & Literature Cited Leach 1973). Adults of E. sinensis have been steadily collected in the Great Lakes, Campbell. G. R. 1984. A comparative study of adult most in Lake Erie, since the early 1970's to sexual behaviour and larval ecology of three commercially important portunid crabs from the 1994 (J. T. Carlton, pers. comm.). However, Moreton Bay region of Queensland, Australia. since E. sinensis is catadromous, it cannot Unpublished Ph.D. Thesis, University of reproduce in the Great Lakes. One transient Queensland, 2S3 pp. specimen of Eriocheir sinensis was found Campos, N. H., & M. TUrkay. 1989. On a record of in Louisiana in 1987 but has not been found Charybdis helleri from the Caribbean coast of Colombia.—Senckenbergiana Maritime 20(3/ there since (D. L. Felder, pers. comm.). This 4):119-123. species apparently has also been transported Carlton, J. T, &. A. N. Cohen. 1996. Episodic global as a live food item sold in Asian-American dispersal in shallow water marine organisms: markets (Horwath 1988, 1989). the case history of the European green crab Carcinus maenas.—Journal of Biogeography (in press). Acknowledgments , & J. B. Geller. 1993. Ecological roulette: the global transport of nonindigenous marine or- I thank Woody Lee, Smithsonian Marine ganisms.—Science 261:78-82. Station Link Port, Ft. Pierce, Florida, for his Chopra, B. 1935. Further notes on Crustacea Decap- invaluable help in trap building, navigation- oda in the Indian Museum. 8. On the decapod Crustacea collected by the Bengal Pilot Survey al guidance through the Indian River, and off the mouth of (he River Hooghly. Brachyg- assistance during trips to the Station. For natha (Oxyrhyncha and Brachyrhyncha).—Rec- providing me with information on addition- ord of the Indian Mascum 37:463-514. al specimens of Charybdis hellerii found in Cohen, A. N., J. T Carlton. & M. C. Fountain. 1995. the Indian River, I thank D. L. Felder (Uni- Introduction, dispersal and potential impacts of the green crab Carcinus maenas in San Fran- versity of Southwestern Ix)uisiana, Lafa- cisco Bay, California.—Marine Biology 122: yette), and A. H. Hines, Jr., and R. B. Man- 225-237. ning (both from the Smithsonian Institution, Galil, B. S. 1992. EriUcan decapods in the Levant. Washington, D.C.). I am particularly grate- Biogeography in motion.—Bulletin de I'lnstitut ful to J. T. Carlton (Williams College-Mys- oc^nographique, Monaco, no. special 9:115- 123. tic Seaport, Connecticut), and an anony- G6mez, C, & J. C. Martinez-Iglesias. 1990. Reciente mous reviewer for extensive comments and hallazgo de la especie indopacffica Charybdis up-to-date information that considerably helleri (A. Milne Edwards, 1867) (Crustacea: 648 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

Decapoda: Portunidae:) en aguas cubanas.—Ca- nal of the Fisheries Research Board of Canada ribbean Journal of Science 26 (l-2):70-72. 30(12)1:1909-1910. Greenwood, J. G.. & D. R. Fielder. 1980. The zoeal Pillai, K. K., & N. B. Nair. 1970. Observations on the stages and megalopa of Charybdis callianassa reproductive cycles of some crabs from the (Herbst) (Decapoda: Portunidae:), reared in the south-west coast of India.—Journal of the Ma- laboratory.—Proceedings of the Royal Society rine Biology Association of India 10:384-386. of Queensland 91:61-76. , & . 1976. Observations on the breed- Hedgpeth, J. W. 1993. Foreign invaders.—Science ing biology of some crabs from the southwest 261:34-35. coast of India.—Journal of the Marine Biology Hem^dez, G., & J. Bolaiios. 1995. Additions to the Association of India 15:754—770. anomuran and brachyutan fauna of northeastern Rathbun, M. J. 1930. The cancroid crabs of America Venezuela. The Crustacean Society Summer of the families Euryalidae. Portunidae, Atele- Meeting, May 25-27, 1995 [abstract). cyclidae, Cancridae and Xanthidae.—United States National Museum Bulletin 152:1-593. Horwath, J. L. 1988. Injurious wildlife: mitten crabs. Say. T. S. 1817. On a new of the Crustacea, Proposed rule.—Federal Register 53(219): and the species on which it is established.— 45784--*5787. Journal of the Academy of Natural Sciences of . 1989. Importation or shipment of injurious Philadelphia l(4):49-64. wildlife: mitten crabs. Final rule.—Federal Reg- Siddiqui, G., & M. Ahmed. 1992. Fecundities of some ister 54(98):22285-22289. marine brachyuran crabs from Karachi (Paki- Javed, M., & J. Mustaquim. 1994. New record of an stan).—Pakistan Journal of Zoology 24:43-45. acorn barnacle. Chelonibia palula (Cirripedia, Smith, S. I. 1879. The stalked-eyed of the Thoracica) from Pakistan.—Crustaceana 66: Atlantic coast of North America north of Cape 124-126. Cod.—Transactions of the Connecticut Acade- Kathirvel, M., & K. N. Gopalakrishnan. 1974. On the my of Arts and Sciences 5:27-136. pis. 8-12. occurrence of Charybdis (Charybdis) hellerii (A. Steinitz. W. 1929. Die Wanderung indopazifischer Ar- Milne Edwards) (Decapoda: Portunidae) along ten Ins Mittelmeer seit Beginn der Quartarper- the west coast of India.—^Journal of the Marine iode.—Internationale Revue der gesamten Hy- Biological Association of India 16:286-287. drobiologie Hydrographie 22:1-90, figs. 1-9. Leene, J. E. 1938. The Decapoda Brachyura of the Stephenson, W. 1972. An annotated check list and key Siboga Expedition. 7. Brachygnatha: Portuni- to the Indo-West-Pacific swimming crabs (Crus- dae.—Monograph of the Siboga Expeditie tacea: Decapoda: Portunidae).—Royal Society 39C'. Livre 131:1-156. of Bulletin 10:1-64. Lemaitre, R. 1995. A nonindigenous portunid crab Stephenson. W, J. J. Hudson, & B. Campbell. 1957. discovered in the Indian River lagoon system of The Australian portunids (Crustacea: Portuni- Florida. The Crustacean Society Summer Meet- dae). II. The genus Charybdis.—Australian ing, May 25-27, 1995 [abstract]. Journal of Marine and Freshwater Research 8: Le Roux, P. J., G. M. Branch. & M. A. R Joska. 1990. 491-507. On the distribution, diet and possible impact of Sumpton, W. 1990. Biology of the rock crab C/iary*- the invasive European shore crab Carcinus dis nataior (Herbst) (Brachyura: Portunidae).— maenas (L.) along the south African coast.— Bulletin of Marine Science 46:425-431. South African Journal of Marine Science 9:85- Vannini. M. 1976. Researches on the coast of Soma- lia. The shore and the dune of Sar Uanle. 8. 92. Notes on Atelecyclidac and Portunidae (Decap- McDermott, J. J. 1991. A breeding population of the oda Brachyura).—Monitorc Zoologico Italiano, western Pacific crab Hemigrapsus sanguineus Italian Journal of Zoology, suppl. 8(2):119-127. (Crustacea: Decapoda: Grapsidae) established Wenner, E. L., & D. M. Knott. 1992. Occurrence of on the Atlantic coast of North America.—Bio- Pacific White Shrimp, Penaeus vannamei, in logical Bulletin 181:195-198. coastal waters of South Carolina. Pp. 173-181 Milne Edwards, A. 1867. Description de quelques es- in M. Richard DeVoe, ed.. Proceedings of the pices nouveltes de Crustac£s Brachyures.—An- Conference and Workshop—introductions and nales de la Society Entomologique de France, transfers of marine species, achieving a balance series 4, 7:263-288. between economic development and resource Moosa. K. 1981. Crustac& d^apodes: Portunidae. protection. Hilton Head, South Carolina. 198 R^sulUts des Campagnes MUSORSTOM I— pp. Philippines (18-28 Mars 1976).—Collection Williams, A. B.. & J. J. McDermott. 1990. An eastern M6moires ORSTOM 91:141-150. United States record for the western Indo-Pa- Nepszy. S. J., & J. H. Leach. 1973. First record of the cific crab, Hemigrapsus sanguineus (Crustacea: Chinese mitten crab, Eriocheir sinensis, (Crus- Decapoda: Grapsidae).—Proceedings of the Bi- tacea: Brachyura) from North America.—^Jour- ological Society of Washington 103:108-109.