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11 4 1707 the journal of biodiversity data 6 August 2015 Check List Notes on Geographic Distribution Check List 11(4): 1707, 6 August 2015 doi: http://dx.doi.org/10.15560/11.4.1707 ISSN 1809-127X © 2015 Check List and Authors

Distribution extension of Acanthobothrium cartagenensis Brooks & Mayes, 1980 (Tetraphyllidea: Onchobothriidae) in jamaicensis (Cuvier, 1816) (: ) from Quintana Roo, México

Scott Monks*, Griselda Pulido-Flores, and Marcelo Lara-Sánchez

Universidad Autónoma del Estado de Hidalgo, Apartado Postal 1-10, Pachuca 42001, Hidalgo, México * Corresponding author. E-mail: [email protected]

Abstract: The collection of eight specimens of W) (collected February 1999), four from Isla Contoy, Acanthobothrium cartagenensis on the coast of Quintana Quintana Roo (20°48ʹ N, 086°47ʹ W) (February 1999), Roo, México extends the geographic distribution of the one from Isla Cozumel, El Paso de los Cedros, Quintana species from the original locality (Cartagena, ) Roo (20°31ʹ N, 086°57ʹ W) (February 1999), and two to at least the northeastern limit of the Mexican coast of from Xcalak, Quintana Roo (18°16ʹ16ʺ N, 087°50ʹ07ʺ W) the Caribbean Sea. The species is a parasite of Urobatis (October 1998) (see Pulido-Flores and Monks 2005 for jamaicensis, a common of the tropical western a detailed map). Individual stingrays were maintained Atlantic. This species has not been reported since the on ice until necropsied, when the intestinal tract was original description in 1980. removed and examined according to Monks et al. (1996). All ecto- and endohelminths were fixed in AFA Key words: geographic distribution, range extension, (Alcohol-Formalin-Acetic Acid) and then transferred Caribbean, , Cestoda, stingray to 70% ethyl alcohol. The Monogenea (ectohelminths) were reported by Pulido-Flores and Monks (2005), but the endohelminths remained unprocessed until this Urobatis jamaicensis (Cuvier, 1816) (Yellow Stingray; present study. One of the eight stingrays (a female) from Raya redonda de estero) (Urotrygonidae), host of Acan- Xcalak, was infected with specimens later identified as thobothrium cartagenensis Brooks & Mayes, 1980 inhab- Acanthobothrium cartagenensis. Worms were stained its sandy, muddy, or seagrass bottoms in shallow in- using Mayer’s carmalum, cleared in Methyl Salicylate, shore waters, commonly near coral reefs. Adults grow and mounted in Canada balsam for examination as to a maximum of 36 cm across the disk-like body and a whole mounts. Voucher specimens were deposited in the short tail with a well-developed caudal fin. Its color is Colección Nacional de Helmintos, Instituto de Biología, variable but distinctive, dorsally either light-on-dark or Universidad Nacional Autónoma de México, México dark-on-light reticulations forming spots and blotches, México (CNHE-9706), the Harold W. Manter Laboratory, and can rapidly change the tonality of this coloration to University of Nebraska-Lincoln, U.S.A (HWML-101020), improve its camouflage (Froese and Pauly 2011). Hel- and the Colección de Helmintos, Universidad Autónoma minths are an important component of our biodiversity, del Estado de Hidalgo, México (CHE-P00061). even though their hosts are the principle focus of most Brooks and Mayes (1980) described A. cartagenensis conservation efforts, as discussed by Zaragosa-Tapia et from a single specimen taken from a stingray al. (2013). This report is a part of the process of docu- (U. jamaicensis) collected near Cartagena, Colombia. menting the rediscovery of little-known species of hel- This specimen was characterized as being relatively minths before they become extinct (Brooks et al. 2002). small, with 13 proglottids, a short spinose peduncle, a Eight specimens of Urobatis jamaicensis were collected V-shaped ovary, 21–26 testes, and the genital pore pre- by local fishermen and examined for intestinal helminths equatorial, as well as having the general characteristics as part of a study of the parasites of stingrays of the of the Acanthobothrium. The specimens that we Yucatán Peninsula, México (Pulido-Flores and Monks collected (Figure 1) conform to this description in these 2005); one from Ría Lagartos, Yucatán (21°36ʹ N, 088°14ʹ and the other features included in their description.

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posterior ends and the hooks are longer and thinner; the bothridia of A. electricolum are strongly developed, sessile (attached with a velum to the scolex at the posterior ends), and the hooks are short, stout, and robust (Brooks and Mayes 1978). Acanthobothrium cartagenensis and A. colombianum have hooks that are more similar in form (Figure 1A), but the scolex of A. cartagenensis is smaller than that of A. colombianum, and the bothridia of the former species are more tear- drop shaped (wider near posterior end) and those of the latter are more oval (wider in the middle). In processed material, each species can be distinguished easily using the information in the original descriptions (Brooks and Mayes 1980); i.e., such characters as the size of the apical suckers, shape and size of hooks, ratio of length of bothridial loculi, the number of testes and the shape of the ovary (Figure 1A and B). Urobatis jamaicensis is distributed from throughout the Grand Caribbean from Florida, U.S.A. to , Yucatan and to northern South America, but it has been reported from as far north as North Carolina, U.S.A. (Froese and Pauly 2011), although migration patterns have not been investigated. Its food consists of crustaceans, other benthic organisms, and small bony fishes (McEachran and Fechhelm 1998); it is likely that one of these groups serve as intermediate host for these cestodes. The Figure 1. Acanthobothrium cartagenensis Brooks & Mayes, 1980 from Caribbean Current directly connects the waters off Urobatis jamaicensis (Cuvier, 1816), in Quintana Roo, México. A. Scolex; Colombia with those of the Caribbean coast of México B. Terminal proglottid. AS = apical suckers; GP = genital pore; H = Hooks; (Carton and Chao 1999), so even if the stingrays do * marks isthmus of ovary; arrows mark septa that divide anterior, middle, not migrate any great distance, the currents could and posterior loculi. Bar = 200 μm. carry infected intermediate hosts from Colombia to , but only in that direction. The report of this Until the present account, there has not been a second cestode in México is particularly important because report of the species. it is the first species of Acanthobothrium reported Based on four characteristics (length, number of from the Caribbean coast and the second species of segments, number of testes, and symmetry of the cestode reported in stingrays from the eastern coast ovarian lobes), Ghoshroy and Caira (2001) proposed of México (Pulido-Flores and Monks 2014). 10 categories as an aid in the identification of species of Acanthobothrium. A category 9 species is longer than ACKNOWLEDGEMENTS 15 mm, has less than 50 proglottids, less than 80 testes, The authors thank all those who made possible and the left and right lobes of the ovary are symmetrical; the examination of specimens, especially Scott L. characteristics of A. cartagenensis. Of the species of Gardner and Gabor Racz, Curator and Collection Acanthobothrium reported from the Caribbean, only Manager, respectively, at the HWML, and Mary A. cartagenensis, A. colombianum Brooks & Mayes, Hanson Pritchard, Affiliate of the HWML, who 1980 (in U. jamaicensis), and A. electricolum Brooks & provided access to literature in the laboratory Mayes, 1978 [in Narcine brasiliensis (Olfers, 1831)] (see archives. Part of this manuscript was prepared during Brooks and Mayes, 1978 and Brooks and Mayes, 1980 a postdoctoral research visit to the HWML by SM for original descriptions of each species), are category 9 and GP-F; the HWML provided office and laboratory species (Ghoshroy and Caira 2001). Thus, for purposes space, access to computers, the reprint collection, and of identification, comparison with the above-mentioned microscopes. This study was supported by funds from species is most useful. the Patronato Universitario (Gerardo Soza Castelán, For identification, even in unprocessed material, President), Universidad Autónoma del Estado de A. cartagenensis and A. colombianum have more delicate Hidalgo (UAEH), and the Consorcio de Universidades bothridia (Figure 1A), which are unattached at the Mexicanas (CUMEX).

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LITERATURE CITED Monks, S., D.R. Brooks and G. Pérez-Ponce de León. 1996. A new Brooks, D.R. and M.A. Mayes. 1978. Acanthobothrium electricolum species of Acanthobothrium Van Beneden, 1849 (Eucestoda: sp. n. and A. lintoni Goldstein, Henson, and Schlicht, 1969 Tetraphyllidea: Onchobothriidae) in Dasyatis longus Garman (Cestoda: Tetraphyllidea) from Narcine brasiliensis (Olfers) (: Myliobatiformes: Dasyatididae) from Chamela (Chondrichthyes: Torpedinidae) in Colombia. Journal of Bay, Jalisco, Mexico. Journal of Parasitology 82(3): 484–488. Parasitology 64(4): 617–619. doi: 10.2307/3279945 doi: 10.2307/3284090 Brooks, D.R. and M.A. Mayes. 1980. Cestodes in four species Pulido-Flores, G. and S. Monks. 2005. Monogenean parasites of euryhaline stingrays from Colombia. Proceedings of the of some elasmobranchs (Chrondrichthyes) from the Yucatán Helminthological Society of Washington 47(1): 22–29. Peninsula, México. Comparative Parasitology 72(1): 69–74. doi: Brooks, T.M., R.A. Mittermeier, C.G. Mittermeier, G.A.B. da Fonseca, 10.1654/4049 A.B. Rylands, W.R. Konstant, P. Flick, J. Pilgrim, S. Oldfield, G. Pulido-Flores, G. and S. Monks. 2014. Distribution extension of Magin and C. Hilton-Taylor. 2002. Habitat loss and extinction Glyphobothrium zwerneri Williams and Campbell, 1977 (Tetraphyl- in the hotspots of biodiversity. Conservation Biology 16(4): lidea: Serendipeidae) from the cownose ray Rhinoptera bonasus 909–923. doi: 10.1046/j.1523-1739.2002.00530.x (Mitchill, 1815) (Myliobatiformes: Myliobatidae) from Campeche, Carton, J.A. and Y. Chao. 1999. Caribbean Sea eddies inferred from México. Check List 10(1): 211–212. doi: 10.15560/2.1.211 TOPEX/POSEIDON altimetry and a 1/6º Atlantic Ocean model Zaragoza-Tapia, F., S. Monks, G. Pulido-Flores and J. Violante­ simulation. Journal of Geophysical Research 104(C4): 7743–7752. Gonzalez. 2013. Distribution extension of Escherbothrium molinae doi: 10.1029/1998JC900081 Berman and Brooks, 1994 (Cestoda: Tetraphyllidea: Triloculari- Froese, R. and D. Pauly, (eds.). 2011. Fishbase. Accessed at http:// idae) in sp. from the Pacific Coast of Mexico. Check List www.fishbase.org, 15 November 2013. 9(5): 1126–1128. http://www.checklist.org.br/getpdf?NGD078-13 Ghoshroy, S. and J.N. Caira. 2001. Four new species of Acanthobothrium (Cestoda: Tetraphyllidea) from the Dasyatis Authors’ contribution statement: SM and GP-F collected and brevis in the Gulf of California, Mexico. Journal of Parasitology processed the specimens, ML-S characterized and identified the 87(2): 354–372. doi: 10.1645/0022-3395(2001)087[0354:FNSOAC specimens, and SM and GP-F wrote the text. ]2.0.CO;2 McEachran, J.D. and J.D. Fechhelm. 1998. Fishes of the Gulf of Received: 20 March 2014 Mexico. Volume 1: Myxiniformes to Gasterosteiformes. Austin, Accepted: 8 June 2015 Texas: University of Texas Press. 1112 pp. Academic editor: Simone Chinicz Cohen

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