Stibarobdella Moorei (Oka, 1910): New Distribution and Host Records Istributio

n Annelida, Hirudinida, Stibarobdella moorei (Oka, 1910): New distribution and host records istributio

D Alison Carlos Wunderlich 1*, Otto Bismarck Fazzano Gadig 2, Teodoro Vaske Júnior 2 and Marcelo Antonio Amaro Pinheiro 2 raphic g

eo 1 Universidade Estadual Paulista (UNESP), Instituto de Biociências de Botucatu, Departamento de Parasitologia. Distrito de Rubião Júnior s/n. CEP G n o

18618-9Vicente, SP,70. BrBotucatu,asil. SP, Brasil. 2 Universidade Estadual [email protected] (UNESP), Campus Experimental do Litoral Paulista (CLP). Praça Infante D. Henrique s/n. CEP 11330-900. São otes

N * Corresponding author. E-mail: Abstract: The present report is the northernmost capture of the piscicolid leech Stibarobdella moorei in the western South S. moorei skate Atlantoraja cyclophora. Stibarobdella moorei bottomAtlantic trawlOcean. around This is of also the Sãothe firstPaulo time coast, southeastern is found Brazil. associated A brief todescription a batoid fish of the in themorphology Brazilian ofcoast, the parasite the eyespot and a discussion on the taxonomic status of the S. moorei was are foundpresented. fixed in the dorsal side of a male eyespot skate, caught by

The only group of annelids known to include species S) to the Gulf of San Jorge, Argentina (47° S) (Menni and that parasitize elasmobranchs is the Hirudinea, or leeches Stehmann 2000; Oddone and Vooren 2004). (Caira and Healy 2004). Marine leeches are well known as Specimens of Atlantoraja cyclophora, were caught by parasitic of numerous elasmobranch species around the bottom trawl during III Oceanographic Cruiser organized world, and such parasitism is restrict to marine leeches of by Universidade Estadual Paulista (UNESP/CLP) in October Piscicolidae (Benz and Bullard 2004; Utevsky and Trontelj 2008, onboard the research vessel “Soloncy Moura” (South 2004). Approximately 20 known species of leeches have been reported from the skin of the sharks and rays (Caira specimen was collected about 100 m deep in a transect and Healy 2004). Regarding marine leeches parasitizing betweenCoast Fisheries 24°25’41.4” Research S, 44°57’49.8” Center - CEPSUL/ICM-Bio). W and 24°26’14.6” The S, elasmobranchs in Brazil, few data records are available. 44°59’22.4” W. Studies of leeches of the elasmobranchs are scarce in Brazilian waters and thus the species list are incomplete, (2003) and Furiness et al. (2007) and the systematic due to lack of interest in this subject, because of the very arrangementParasite morphometry follows Furiness and identification et al. (2007), follow Sotowho low number of specialists working along the Brazilian considered S. moorei as the valid name and S. loricata, coast (Schlenz 1999; Christoffersen 2008). alcohol and deposited in the Helminthological Collection associations, when he recorded Branchellion ofas the a junior Departamento synonym. de The Parasitologia specimen wasof the fixed Instituto in 70% de cownoseSchlenz rays (1999) (Rhinoptera was the first to reportsRhinobatos leech-fish sp.) Biociências (CHIBB), Universidade Estadual Paulista and spotted eagle ray (Aetobatus narinari (Euphrasen, sp. fixed to (UNESP), municipality of Botucatu, state of São Paulo, 1790)) in Cananéia, southern sp.), guitarfish coast of São ( Paulo. More Brazil. recently, Stibarobdella macrothella (Schmarda, 1861) One 450 mm total length (TL) male specimen of the was found on cooper shark (Carcharhinus brachyurus eyespot skate (A. cyclophora) was captured with a 97 (Günther, 1870)) in southern Brazil by Soto (2000) and on mm TL marine leech S. moorei (Voucher – CHIBB 5021) the Caribbean sharpnose shark Rhizoprionodon porosus parasitizing its dorsal side. The parasite attachment (Poey, 1861) from northeastern Brazil (Naércio Menezes, caused two typical circleson host epidermal tissue (Figure personal communication). Stibarobdella moorei (Oka, 1), which were represented by a major lesion (oral sucker 1910) (Hirudinea, Piscicolidae) was found as parasite of = os) and a minor one (caudal sucker = cs). three angel sharks (Squatina argentina, (Marini, 1930), S. The general morphology of the S. moorei specimen guggenheim Marini, 1936 and S. punctata Marini, 1936) and on sandtiger shark Carcharias taurus et al. (2007) in having the diagnostic characters to 1810, from southern Brazil (cited as S. loricata (Harding, distinguishherein examined from fitsall other the description known Stibarobdella presented by species, Furiness as 1924) by Soto (2003)). Rafinesque, follows: no eyes; small, terminal caudal sucker; large, very S. moorei (Oka, 1910) deeply cupped oral sucker with marginal fringe; and three (Hirudinida) in a new elasmobranch host, the eyespot pairs of small marginal papillae (Figure 1). Concerning skateIn thisAtlantoraja article, we cyclophora first report (Regan, 1903) (Rajidae: these two last features, previous studies consider S. moorei Arhynchobatinae), an endemic batoid elasmobranch that and S. loricata as distinct species on the basis of the oral inhabits the bottom of the continental shelf and slope of sucker morphology (smooth margins and lacking papillae the western South Atlantic, from Rio de Janeiro, Brazil (22° in S. moorei and fringed margin and three pairs of papillae

Check List | Volume 7 | Issue 3 | 2011 360 Wunderlich et al. | New distribution and host records of Stibarobdella moorei in S. loricata). Furiness et al. (2007) resurrect S. moorei and (Rajidae) from Tasmanian waters, Australia, was also regard S. loricata as junior synonym of S. moorei clarifying recorded infected by this species, but no further additional that in the original description of S. moorei by Oka (1910) data was presented (Furiness et al. 2007). Moreover, the there are no data on the papillae number or arrangement, present report extends the previous known western South and the oral sucker was described as smooth. A more Atlantic distribution of the species to a northernmost position (about 24°26’ S) in relation to the data reported revealed the presence of three pairs of papillae and fringed by Soto (2003) in the latitude 29°34’ S. oralcareful sucker type margins, specimen as re-examination described early by for these S. authorsloricata This widespread distributional pattern of Stibarobdella by Harding (1924) who did not examine the S. moorei (notably S. macrothella, another marine leech recorded holotype. as parasitic of elasmobranch in Brazilian waters) is often Stibarobdella moorei is known to occur in the Indian explained by the highly mobile and power swimming Ocean (Oka 1910), Japan and Tasmania (Furiness et al. hosts, since most elasmobranch species targeted by Stibarobdella spp. are “wide ranging sharks” (Sawyer et species in the Atlantic Ocean (as S. loricata), parasitizing al. 1975; Williams 1982; Sawyer 1986; Benz and Bullard four2007). shark Soto species (2003) from presented southern the Brazil. first Previous record ofknown this 2004; Furiness et al. 2007). Despite the fact that S. macrothella is regarded as parasitic of oceanic sharks and Squatina and Carcharias that the species of Stibarobdella feed primarily on sharks tauruspositively), totaling identified four elasmobranch species (Soto hosts 2003). were Herein coastal is (Sawyer 1986). Thus the bottom sea associated marine demersal-benthic sharks (threeS. moorei A. cyclophora elasmobranchpresented the host first forrecord S. moorei of on an identified theleech Pontobdellinae life, the more couldadequate be thecriteria elasmobranchs to distinguish general host batoid fish, , becoming the fifth identified specificity among the representatives parasites leech of . One unidentified skate A B

Figure 1. Terminal views of the caudal sucker (a) and oral sucker (b), in the last one showing the marginal fringe and three pairs of small papillae that characterize marine leech Stibarobdella moorei. This specimen was captured on dorsal epidermis of an adult male Atlantoraja cyclophora (total length, TL = 450mm) (photo inferior left), with the occurrence of two epidermal whitish rounded lesion next the left ocellus (photo inferior right), caused by the oral and caudal sucker (os and cs, respectively).

Check List | Volume 7 | Issue 3 | 2011 361 Wunderlich et al. | New distribution and host records of Stibarobdella moorei habitat, more than the imprecise terms “sharks” or “rays”. Christoffersen, M.L. 2008. A Catalogue of the Piscicolidae, Ozobranchidae, In an updated list of elasmobranchs host for S. macrothella and Arhynchobdellida (Annelida, Clitellata, Hirudinea) from South America. Neotropical Biology and Conservation provided by Yamaguchi et al. (2008), there are at least Furiness, S., J.L. Williams, K. Nagasawa and E.M. Burreson. 2007. A 3(1): 39-48. and surrounding waters, including redescriptions of three species. sharks and four are rays, but in fact 14 of the listed species Journalcollection of Parasitology of fish leeches (Hirudinida: Piscicolidae) from Japan 22 positively identified elasmobranchs, of which 18 are Harding, W.A. 1924. Descriptions of some new leeches from India, Burma and Ceylon. Annal and Magazine93(4): 875-883. of Natural History are coastal-demersal or benthic and the remaining are Menni, R.C. and M.F.W. Stehmann. 2000. Distribution, environment and Therefore, based on the above mentioned facts, the 14: 491-493. regardedcoastal-oceanic worldwide pelagic. distributional pattern of S. moorei and Revista del Museo Argentino de Ciencias Naturales S. macrothella must be reviewed because most recorded Oddone,biology M.C. of batoid and fishes C.M. off Vooren. Argentina, 2004. Uruguay Distribution, and Brazil. abundance A review. elasmobranch hosts do not exhibit a global distribution and morphometry of Atlantoraja cyclophora 2(1): (Regan, 69-109. 1903) (Elasmobranchii: Rajidae) in southern Brazil, Southwestern Atlantic. pattern, some worldwide pelagic sharks recorded as hosts Neotropical Ichthyology (e.g., Carcharhinus leucas Valenciennes, 1839, C. limbatus Oka, A. 1910. Synopsis der Japanischen Hirudineen, mit Diagnosen der (Valenciennes, 1839), and Galeocerdo cuvier (Péron and Neuen Species. Annotationes 2(3): Zoologicae137-144. Japonenses Sawyer, R.T. 1986. Leech biology and behaviour. Vol. II. Feeding biology, Lesueur, 1822) are more associated to coastal areas, ecology, and systematics. Oxford: Clarendon Press. 375 7: 165-183. p. and there are no evidences of transoceanic migratory Sawyer, R.T., A.R. Lawler and R.M. Overstreet. 1975. Marine leeches of the Carcharhinus eastern United States and the Gulf of Mexico with a key to the species. movements (with the possible exception for Journal of Natural History falciformis (Bibron, 1839) and C. longimanus (Poey, 1861), In A.E. Migotto and C.G. Tiago both also recorded as hosts for S. macrothella). Due to (ed.). Biodiversidade do 9: Estado 633-667. de São Paulo, Brasil: síntese do the complex Stibarobdella taxonomy, the lack of more Schlenz,conhecimento E. 1999. Hirudinea; ao final do p. século 183-184. XX. 3: Invertebrados Marinhos. São p. most elasmobranch hosts are coastal nearshore species, Soto,Paulo: J.M.R. Fundação 2000. Marine de Amparo leech, a Stibarobdella Pesquisa do Estado macrothela de São (Schimarda, Paulo. 310 itconclusive is possible studies that S. on moorei host specificity,comprises actually and the a fact species that 1861) (Hirudinea, Piscicolidae), parasitic on the whaler shark, Carcharhinus brachyurus (Günther, 1870) Chondrichthyes, complex rather than a single worldwide distributed Carcharhinidae), in southern Brazilian waters. Revista Brasileira de species. Biologia Finally, more elucidative taxonomic studies, including Soto, J.M.R. 2003. The marine leech Stibarobdella loricata (Harding, 1924) (Hirudinea,60(4): Piscicolidae), 713-714. parasitic on the angel shark Squatina spp. and sandtiger shark Carcharias taurus molecular sequence data, are suggested to solve this waters. Brazilian Journal Biology Rafinesque, 1810 (Chondrichthyes, Squatinidae, Carchariidae) in southern Brazilian question. Acknowledgments: The authors would like to thank to the South leeches (Hirudinea, Piscicolidae) 63(4): based 691-694. on mitochondrial DNA Utevsky, S. Y. and P. Trontelj. 2004. PhylogeneticZoologica Scripta relationships 33: 375–385. of fish Yamauchi, T., Y. Ota and K. Nagasawa. 2008. Stibarobdella macrothela tripCoast of Fisheries III Oceanographic Research CenterCruiser - CEPSUL/ICM-Bio,of UNESP/CLP; Fundação Santa Catarina) de Amparo and sequences(Annelida, Hirudinida,and morphological Piscicolidae) data. from elasmobranchs in Japanese crew of the research vessel “Soloncy Moura” for support during the field waters, with new host records. Biogeography toà Pesquisa authors; do UNESP Estado General de São Administration, Paulo (FAPESP) in and supporting Conselho theNacional research de adjacent regions. Proceedings of the Helminthological 10: 53-57. Society of cruises;Desenvolvimento and João Científico Pedro Barreiros e Tecnológico (Universidade (CNPq), dos for Açores,individual Portugal) grants Williams,Washington E.H.Jr. 1982. Leeches of some marine fishes of Porto Rico and for the valuable manuscript comments. 49: 323-325. Literature Cited Benz, G.W. and S.A. Bullard. 2004. Metazoan Parasites and Associates of Chondrichthyans with Emphasis on Taxa Harmful to Captive In M.D. Smith, D.T. Warmolts, D.A. Thoney and R.E. Hueter (ed.). The Elasmobranch Husbandry Manual: Captive Care of Hosts;Sharks, p. Rays 325-416 and their Relatives. Ohio: Special Publication of the Ohio : March 2011 Biological Survey. : May 2011 Caira, J.N. and C.J. Healy. 2004. Elasmobranchs as Hosts of Metazoan Received : May 2011 In J.C. Carrier, J.A. Musick and M.R. Heithaus. Last Revised : June 2011 (ed.). Biology of Sharks and Their Relatives. New York: CRC Press. Accepted : Luis Ernesto Arruda Bezerra Parasites; p. 523-551 Published online Editorial responsibility

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