Cestoda: Tetraphyllidea: Triloculariidae) in Urotrygon Sp

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Distribution Extension of Escherbothrium molinae Berman and Brooks, 1994 (Cestoda: Tetraphyllidea: Triloculariidae) in Urotrygon sp. from the Pacific Coast of Mexico

Francisco Zaragoza-Tapia Universidad Autónoma del Estado de Hidalgo, [email protected]

Scott Monks Universidad Autónoma del Estado de Hidalgo, [email protected]

Griselda Pulido-Flores Universidad Autónoma del Estado de Hidalgo, [email protected]

Juan Violante-González Universidad Autónoma de Guerrero, [email protected]

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Zaragoza-Tapia, Francisco; Monks, Scott; Pulido-Flores, Griselda; and Violante-González, Juan, "Distribution Extension of Escherbothrium molinae Berman and Brooks, 1994 (Cestoda: Tetraphyllidea: Triloculariidae) in Urotrygon sp. from the Pacific Coast of Mexico" (2013). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 761. https://digitalcommons.unl.edu/parasitologyfacpubs/761

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Zaragoza-Tapia, Monks, Pulido-Flores & Violante-González in CheckList (2013) 9(5). Copyright 2013, CheckList and authors. Used by permission. Check List 9(5): 1124–1125, 2013 © 2013 Check List and Authors Chec List ISSN 1809-127X (available at www.checklist.org.br) Journal of species lists and distribution

n Distribution extension of Escherbothrium molinae Berman and Brooks, 1994 (Cestoda: Tetraphyllidea: Triloculariidae)

istributio in Urotrygon D

1 1* 1 2

raphic , Scott Monks g sp. from the Pacific Coast of Mexico eo Francisco Zaragoza-Tapia , Griselda Pulido-Flores and Juan Violante-González G n o 1 Universidad Autónoma del Estado de Hidalgo, Centro de Investigaciones Biológicas, Laboratorio de Morfología Animal. Carretera Pachuca- Tulancingo Km. 4.5, Mineral de la Reforma, Apartado Postal 1-69, CP. 42001. Pachuca, Hidalgo, México.

otes 2 Universidad Autónoma de Guerrero,[email protected] Unidad Académica de Ecología Marina. Gran Vía Tropical No. 20, Fraccionamiento Las Playas, CP. 39390, N Acapulco, Guerrero, México. * Corresponding author. E-mail: Abstract: Cestodes collected from the spiral valves of the stingray Urotrygon Escherbothrium molinae and the Guanacaste coast, Costa Rica; this work represents the second report of sp.the from species the since Pacific the coast original of Mexico description were andidentified extends as its distribution north to Acapulco, Berman and Guerrero, Brooks, Mexico. 1994. The first report of the species was from the Gulf of Nicoya

Escherbothrium molinae was described by Berman taxa and the bifurcating structure of the medial bothridial and Brooks (1994) based on 35 specimens taken from septa of E. molinae. Therefore, they placed it into the several individuals of Urotrygon chilensis (Günther, 1871) family Triloculariidae. Others have suggested that the (Chondrichthyes: Myliobatiformes: Urolophidae), the genus should be moved to the Rhinebothriinae, but formal Chilean round ray, collected in the Gulf of Nicoya and taxonomic studies of this question are still wanting. the Guanacaste coast, Costa Rica. Since that date the To date, the only known species of Escherbothrium is a species has been mentioned in publications by Brooks parasite of elasmobranchs, Urotrygon and Barriga (1995), Brooks et al. (1999), and Caira et al. (1999), among others, but it has not been reported again. bothridia, each bothridium with apical suckersp. It has and a muscular singular As part of a continuing study of the helminth parasites type of scolex with 4 pedicellated bothridia, cup-shaped of stingrays of the Acapulco and Jalisco, nine stingrays The specimens we collected conform to the description (Urotrygon sp.) were collected from waters off Bahía de establishedsepta dividing by it into Berman 4 large and and Brooks 2 small (1994)loculi (Figures in this 1-2). and Chamela, Jalisco, Mexico (19°31’ N; 105°04’ W) (three in July the other features included in their description; Figures U. munda from Golfo de Santa Elena, Playa Cuajiniquil, Costa Rica The most often overlooked components of the 2001(10°57 and’ N ,six 85°48’ in January W) (February 2004); five 1996); specimens and 34 of stingrays biodiversity1-2 are provided of a to country aid in the are identification those organisms of specimens. with life (Urotrygon sp.) from Bahía de Acapulco, Guerrero (16°50’ problems with particular species (Poulin 2004; Brooks and stingrays were maintained on ice until examined and the Hobergcycles as2008), parasites. only specialists Unless are there concerned are health-related about their intestinalN; 99°53’ W)tract (October removed 2012) and examined by local fishermen. according Individual to (Monks presence or the possibility of their extinction; it is doubtful et al. and then transferred to 70% ethyl alcohol. Three stingrays 2012). This is partly because the public sees parasites as (July 1996).2001) and Ectohelminths three of the and 34 endohelminthsstingrays (October were 2012) fixed diseasesif a species that of mustparasite be curedwill ever rather make than the an“Red indispensable List” (IUCN were infected with eight specimens of E. molinae. Worms part of natural systems (Brooks and McLennan 2002). This lack of emphasis has resulted in there being few carmalum, cleared in Methyl Salicylate, and mounted in reports of their distributions except in the specialized Canadawere stained balsam usingfor examination Delafield’s as hematoxylin whole mounts. or Voucher Mayer’s literature, and many helminths have only been reported specimens were deposited in the Colección Nacional de in the original descriptions. Despite the usefulness of distribution records of parasites to our understanding and the Harold W. Manter Laboratory, University of of the ecology and evolution of parasites and their Helmintos, IBUNAM, Mexico (CNHE-8513, CNHE-8514); hosts (Brooks and McLennan 1993; Brooks and Hoberg 2000; Poulin 1999), this trend has yet to be reversed. establishedNebraska-Lincoln, the genus U.S.A (HWML-49850 and described to E. HWML-49853). molinae; the This report of the range extension of Escherbothrium nameIn of the the original genus was work, inspired Berman by andthe artwork Brooks of (1994), M. C. molinae Berman and Brooks, 1994 is offered to Escher. They examined the holotype and paratypes of provide information useful for those classes of studies. Zyxibothrium Hayden and Campbell, 1981 and illustrations E. molinae in Guerrero and of the scolex of Pentaloculum Alexander, 1963, and they Jalisco, suggests that individuals of U. chilensis are moving noted a marked similarity between the scoleces of those (possiblyFinally, migrating) the finding within of the limits of the range of

1124 Zaragoza-Tapia et al. | Distribution extension of Escherbothrium molinae

or U. rogersi (or both species were included), but we cannot be sure beyond assigning them to Urotrygon sp. Both parasitological and ichthyological knowledge

would benefit from a thorough study of this genus that would correlate morphology and molecular identification. Acknowledgments: The authors thank all those who made possible the collection and examination of specimens. Scott L. Gardner and Gabor Racz, Curator and Collection Manager, respectively, at the HWML,

material of the collection and literature in the laboratory archives. This and Mary Hanson Pritchard, Affiliate of the HWML, provided access to

study was supported by funds from the Project: Inventario Ambiental thisy Establecimiento manuscript was de prepared Indicadores during Regionales a Postdoctoral de la research Red Temática: visit to theCalidad HWML Ambiental by the authors y Desarrollo and supported Sustentable by funds (PROMEP-SEP). from the Patronato Part of

del Estado de Hidalgo (UAEH), and the Consorcio de Universidades MexicanasUniversitario (CUMEX). (Gerardo Soza The Castelán, Consejo NacionalPresident), de Universidad Ciencia y TecnologíaAutónoma

Literature(CONACYT) provided Cited a scholarship (No.432427) to FZ-T. Berman, R., and D.R. Brooks. 1994. Escherbothrium molinae n. gen. et n. sp. (Eucestoda: Tertraphyllidea: Triloculariidae) in Urotrygon chilensis (Chondrichthyes: Myliobatiformes: Urolophidae) from the Gulf of Nicoya, Costa Rica. Journal of Parasitology Brooks, D.R. and R. Barriga. 1995. Serendip deborahae n. sp. (Eucestoda: Tetraphyllidea: Serendipidae n. fam.) in Rhinoptera 80: 775-780. steindachneri Evermann and Jenkins, 1891 (Chondrichthyes: Myliobatiformes: Myliobatidae) from Southeastern Ecuador. Journal of Parasitology

Brooks, D.R. and E.P. Hoberg. 2000. Triage for the biosphere: the need and81: 80-84. rationale for taxonomic inventories and phylogenetic studies of parasites. Comparative Parasitology

sloshing bucket: the evolutionary biology67: 1-25. of emerging infectious Brooks,diseases. D.R. and Evolution: E.P. Hoberg. Education 2008. and Darwin’s Outreach necessary misfit and the Brooks, D.R., F. Marques, C. Perroni and C. Sidagis. 1999. Scyphophyllidium uruguayense n sp. (Eucestoda: Tetraphyllidea) 1: 2-9. in Mustelus mento (Cope, 1877) (Chondrichthyes: Carcharhiniformes: Triakidae) from la Paloma, Uruguay. Journal of Parasitology Brooks, D.R. and D.A. McLennan. 1993. Parascript: parasites and the language of evolution 85: 490-495. Press. 429 p. Brooks, D.R. and D.A. McLennan.. Washington, 2002. D. The C.: Smithsonian nature of diversity: Institution an evolutionary voyage of discovery. Chicago: The University of Chicago Figure 1-2. Scolex of Escherbothrium molinae Berman and Brooks, 1994 Press. 668 p. from Urotrygon sp. (Günther, 1871) from Acapulco, Guerrero, Mexico. 1. Caira, J.N., K. Jensen and C.J. Healy. 1999. On the phylogenetic Escherbothrium molinae, photo. 2. Escherbothrium molinae, drawing. Bar relationships among tetraphyllidean, lecanicephalidean and = 150 μm diphyllidean tapeworm genera. Systematic Parasitology Listados faunísticos de México. VII. Catálogo sistemático de las rayas y especies afines 42: de 77-151. México Castro-Aguirre,(Chondrichthyes: J.L. and Elasmobranchii: H. Espinosa-Pérez. Rajiformes: 1996. Batoideiomorpha). Fishbase 2012). From this second report, and the distance betweenthe species each (Castro-Aguirre known locality, and it is Espinosa-Pérez obvious that further 1996; FishBase. 2012. Fishbase. Version 02-2013. Electronic database México, D. F.: Instituto de Biologia, UNAM. 75 p. studies must be carried out for a fuller understanding of IUCN Red the distribution of E. molinae, particularly in the localities Listaccessible Categories at http//www.fishbase.org/. and Criteria. Version 3.1. Captured Second edition. on 11 March Gland 2013. and between Mexico and Costa Rica. Molecular studies could IUCN, International Union for Conservation of Nature. 2012. In W. shed light on this hypothesis and provide information Fischer,Cambridge: F. Krupp, IUCN. 32W. p.Schneider, C. Sommer, K.E. Carpenter and V.H. about the potential “passive migration” of E. molinae. McEachran,Niem (ed.). J.D. Guia 1995. FAO Urolophidae. para Identification Rayas redondas;de Especies p. para 786-792 lo Fines de The stingrays should also be studied with the same goal. la Pesca. Pacifico Centro-Oriental. Roma: FAO. 1996. A new species The taxa from Mexico that are host for E. molinae are of Acanthobothrium Van Beneden, 1849 (Eucestoda: Tetraphyllidea: Monks,Onchobothriidae) S., D.R. Brooks and in G.Dasyatis Pérez-Ponce longus de León. Garman (Chondrichthyes: Both U. chilensis (Günther, 1872) and U. rogersi (Jordan Myliobatiformes: Dasyatididae) from Chamela Bay, Jalisco, Mexico. Journal of Parasitology anddifficult Starks, to distinguish1895) are common and assign along to athis particular coast, and species. there Poulin, R. 1999. The functional importance of parasite in animal are occasional reports of U. nana Miyake and McEachran, communities: many roles 82: at484-488. many levels? International Journal for Parasitology

The morphology (i.e., coloration, etc.) of these species is grossly underestimated 29: 903-914. component of biodiversity? Diversity & variable1988 (see and Castro-Aguirreeach is virtually and indistinguishable Espinosa-Pérez to 1996).casual Poulin,Distributions R. 2004. Parasite species richness in New Zealand fishes: a observation; assignment to species is based primarily 10: 31-37. on the form of the pupil cover of the eye (McEachran : April 2013 : August 2013 1995; Fishbase 2012). Thus, we are relatively sure that Received : October 2013 the stingrays collected in Mexico are either U. chilensis Accepted : Simone Chinicz Cohen Published online Editorial responsibility 1125