Phyllodistomum centropomi sp. n. (Digenea

Zootaxa 1056: 43–51 (2005) www.mapress.com/zootaxa/

ISSN 1175-5326 (print edition)

Copyright © 2005 Magnolia Press

ISSN 1175-5334 (online edition)

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Phyllodistomum centropomi sp. n. (Digenea: Gorgoderidae), a parasite of the fat snook, Centropomus parallelus (Osteichthyes: Centropomidae), in the Papaloapan River at Tlacotalpan, Veracruz State, Mexico BERENIT MENDOZA-GARFIAS & GERARDO PÉREZ-PONCE DE LEÓN 1 Laboratorio de Helmintología, Instituto de Biología, UNAM, Ap. Postal 70-153, C.P. 04510, México D.F., México 1 corresponding author: [email protected]

Abstract Phyllodistomum centropomi n. sp. (Digenea: Gorgoderidae) is described from the urinary bladder of Centropomus parallelus (Osteichthyes: Centropomidae) from the Papaloapan River in Veracruz State, Mexico. This species is distinguished from its congeners in North America, either marine or freshwater, in having the vitelline glands located in a posterolateral position to the ovary and the margin of the hindbody possessing slight undulations with muscular indentations from the level of testes to the posterior end of the body. The new species most closely resembles P. mayesi Brooks & MacDonald, 1986, a parasite of Trachycorystes insignis in the Río Atrato, in the vicinity of Quibdo, Choco, Colombia, since both possesses postovarian paired vitelline glands, but P. centropomi differs by having muscular undulations on the margin of hindbody and an oral sucker/acetabulum ratio close to unity. Key words: Gorgoderidae, Phyllodistomum, Centropomus parallelus, Digenea, Taxonomy, México.

Introduction Members of Centropomus Lacepède, 1802 are important high-level carnivores in Eastern Pacific and western Atlantic coastal waters and associated with estuaries and rivers (Tringali et al., 1999). Six species inhabit several river drainages in the Gulf of Mexico slope: Centropomus ensiferus Poey, 1860, C. mexicanus Bocourt, 1868, C. parallelus Poey, 1860, C. pectinatus Poey, 1860, C. poeyi Chavez, 1961, and C. undecimalis (Bloch,1792). Particularly, the fat snook, C. paralellus, is distributed in coastal waters from southern Florida (USA), along the coast of the Gulf of Mexico to the Atlantic coast

Accepted by N. Dronen: 25 Aug. 2005; published: 30 Sept. 2005

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in Florianopolis, Brazil. This species inhabits estuaries and lagoons, penetrating into freshwater (Castro-Aguirre et al., 1999). Currently, 12 species of digeneans have been reported from this host in localities of two Mexican States, Tabasco and Veracruz; however, with the exception of two papers (Lamothe-Argumedo et al., 1989; LamotheArgumedo & Pineda-López, 1990), all represent records of species commonly found in other host species but as no voucher specimens are deposited in museum collections, the identifications cannot be confirmed (Pineda-López, 1985; Pineda-Lopez et al., 1985; Chavez et al., 1990). Only two cryptogonimid digeneans collected from the intestine of the fat snook in localities of the Grijalva river drainage, in Tabasco State, were described as new species: Neochasmus olmecus Lamothe-Argumedo, Pineda-López, & Andrade-Salas, 1989, and Olmeca laurae Lamothe-Argumedo & Pineda-López, 1990. In Mexico, four nominal species of the gorgoderid genus Phyllodistomum Braun, 1899 have been recorded: Phylodistomum lacustri (Loewen, 1929) Lewis, 1935, P. mirandai Lamothe, 1969, P. marinae Bravo & Manter, 1957 and P. carangis Manter, 1947. Phyllodistomum lacustri is the only species of the genus found in freshwater fishes of Mexico and its presence has been recorded in several host species (Pérez-Ponce de León et al., 1996; Vidal-Martínez et al., 2001; Pérez-Ponce de León & Choudhury, 2002). The latter three are marine representatives of this genus (Bravo & Manter, 1957; LamotheArgumedo et al., 1997). In this paper a new species of gorgoderid is described parasitising the urinary bladder of the fat snook C. parallelus and compared to other nominal species of Phyllodistomum.

Material and methods Fish were collected in the Papaloapan River, Veracruz State (18°36’28”N, 95°39’06”W), particularly at the village of Tlacotalpan. This represents an estuarine portion of the basin, a few kilometers before opening into the Gulf of Mexico. This river drains to the Gulf of Mexico slope and represent the second largest river system in Mexico. In total, 39 fat snook were collected between March, 2000 and September, 2004. Specimens obtained from the urinary bladder were placed in 6.5% saline, fixed by sudden immersion in hot formalin (4%), stored in 70% ethanol and stained with Mayer´s paracarmine or Ehrlich´s haematoxylin. Worms were dehydrated, cleared in methyl salicylate and mounted in Canada balsam. Figures were drawn with the aid of a drawing tube. Measurements are given of 14 ovigerous specimens in micrometers and presented as a range followed by the mean in parentheses. Type-specimens were deposited at the Colección Nacional de Helmintos, Mexico City (CNHE), Mexico City and U.S. National Parasite Collection, Beltsville, Maryland (USNPC). For comparison, the following specimens of Phyllodistomum were examined: P. lacustri, CNHE 1278, 1524, 1523, 4218, 4225, 4233, 4234, vouchers; P. mirandai (CNHE) 923, holotype, 924, paratypes, 4285, vouchers; and P. carangis (CNHE) 1112, 1798, 3109 vouchers.

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MENDOZA-GARFIAS & PÉREZ-PONCE DE LEÓN

For scanning electron microscopy (SEM) study, digeneans were washed in phosphatebuffer (pH 7.3), fixed in hot 4% formalin, post fixed in 1% osmium tetroxide for 1h., dehydrated through a graded series of ethyl alcohol, subjected to critical point drying with carbon dioxide and then sputter-coated with gold. They were mounted on metal stubs with silver paste, coated with gold and examined in a Hitachi Stereoscan Model S-2469N at 15 kV.

Results Family Gorgoderidae Looss, 1901 Genus Phylodistomum Braun, 1899

Phyllodistomum centropomi n. sp. Type-host: Centropomus paralellus Poey, 1860 Type-locality: Papaloapan River at Tlacotalpan, Veracruz State, Mexico (18°36’28”N, 95°39’06”W). Site: Urinary bladder. Type material : Holotype No. 4504 and 9 paratypes (4505) deposited in the Colección Nacional de Helmintos, Mexico City, Mexico (CNHE). Two paratypes deposited in the U.S. National Parasite Collection, Beltsville, Maryland (USNPC) No. 096463–096464. Prevalence of infection (infected hosts/analyzed hosts, percentage): 13/39, 33.33%. Mean abundance: 26 worms/39 hosts (0.66 worms per analyzed host). Etymology: This species is named after the host generic name. Description (Figs 1A–B, 2A–D) Body oblong, expanded posterior to ventral sucker, aspinous, with undulations in lateral margins of hindbody, 1796–2610 (2200) long by 1252–1651 (1450) wide at level of posterior region. Forebody sub-cylindrical, representing 1/3 of total body length. Hindbody discoid, with 3 or 4 slight undulations possessing series of muscular indentations from the level of testes to posterior extremity. Tegument with numerous papillae. Oral sucker 219–275 (248) x 214–274 (248), subterminal, showing 20 dome-type papillae in symmetrical arrangement. Ventral sucker in second quarter of body, not occupying full body width, 232–286 (250) x 206–279 (251). Sucker ratios: lengths of oral sucker to acetabulum 1:1.08–1:1.18 (1:1.09); widths of same organs: 1:0.83–1:1.33 (1:1.02). Prepharynx and pharynx lacking. Esophagus 97–215 (138) long by 10–34 (20) wide. Ceca long, narrow, running laterally along the body and terminating at end of hindbody.

A NEW PHYLLODISTOMUM


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FIGURE 1. Phyllodistomum centropomi n. sp. A) Holotype, ventral view, scale-bar: 100 µm. B) Paratype, detail of the terminal ends of the reproductive tracts, scale-bar: 10 µm. C = Ceca, MI = muscular indentations, O = Ovary, OS = Oral sucker , SV = Seminal Vesicle, T = Testes, UN = Undulations, U = Uterus, VG = Vitelline glands, VS = Ventral sucker

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FIGURE 2. A) Scanning Electron Microscopy of the of the forebody of P. centropomi, showing genital pore. B) Oral sucker showing the stylet scar. C) Ventral sucker showing 2 internal domelike papillae. D) Higher magnification of body surface showing a dome-like papillae.

Testes 2, slightly lobed, symmetrical, in middle region of body, postovarian; right 259–402 (332) long, 225–388 (266) wide; left 230–559 (346) long, 194–347 (270) wide. Seminal vesicle saclike in appearance, 80–109 (95) long, opening via genital pore. Pars prostatica and ejaculatory duct not observed. Genital pore mid-ventral, between acetabulum and intestinal bifurcation. Ovary entire, ovoid, anterior and oblique to right testis, 150–195 (169) long, 135–229 (192) wide. Oviduct arises dorsally, giving off Laurer´s canal and receiving common vitelline duct, opens into the ootype which is surrounded by Mehlis´ gland. Uterus arises from ootype, filling extra- and inter-cecal area, occupying most of hindbody, ascending arm followed by muscular metraterm which opens via genital pore. Eggs from distal portion of uterus oval 19–32 (25) long, 15–24 (19) wide. Vitelline glands comprises 2 compact oval masses, located posterolaterally to ovary; right 91–130 (111) long, 80–117 (95) wide; left 99–153 (120) long, 83–134 (99) wide. I-shaped excretory bladder tubular, dorsal to uterus, extends to level of testes. Excretory pore terminal.



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Remarks

1056 The new species possesses two diagnostic traits: Vitelline glands located posterolaterally to the ovary, and a hindbody with slight undulations each possessing muscular indentations. Indentations were observed in live as well as in preserved specimens, so they are not a result of a fixation artifact. This combination of characters distinguishes the new species from all of its congeners. However, the position of the two vitelline glands or the muscular indentations are not unique traits in species of Phyllodistomum since other gorgoderids, such as some species of Xystretum Linton, 1910 found in India, also exhibit them (Ahmad, 1982). In the Americas, the only other species of Phyllodistomum with a vitelline glands located in a posterolateral position with respect to the ovary is P. mayesi Brooks & MacDonald, 1986, a species described from Trachycorystes insignis in Río Atrato, vicinity Quibdo, Choco, Colombia, however P. centropomi sp. nov. is different in some characteristics such as the size of the body, the size of the testes and the suckers ratio. The body in P. mayesi is larger, testes are shorter and oral sucker/acetabulum length and width ratios is 1:2, meaning that ventral sucker is almost twice the size of the oral sucker. Pllodistomum centropomi sp. nov. also resembles P. marinae, a species described from Mycteroperca pardalis Gilbert, 1892 off La Paz, state of Baja California Sur (Bravo & Manter, 1957) in having the lateral margins of hindbody provided with muscular indentations, however, the new species is different from P. marinae by the position of the vitelline glands with respect to the ovary. In P. marinae, the vitelline bodies are located anteriorly to the ovary. In addition to P. marinae, there are 2 species of Phyllodistomum infecting marine fishes in Mexican coastal waters. The new species differ from P. carangis, a species found in the body-cavity of the carangid Citula dorsalis Gill, 1863 off the coast of Nayarit and Sinaloa (Winter, 1957) and in Trachinotus rhodopus Gill, 1863 off the coast of Chamela Bay, Jalisco (Pérez-Ponce de León et al., 1999), in the oblong body shape and in having entire vitelline bodies. In P. carangis the body is elongate and the vitelline masses are trilobate. The new species differs further from P. mirandai, a species described from the urinary bladder of Sphoeroides annulatus Jenyns, 1842 off the coast of Oaxaca, in that the suckers ratio approximates to the unity rather than being 1: > 2.

Discussion Members of the genus Phyllodistomum have been reported from numerous freshwater and marine fish and amphibians throughout the world. It currently contains more than 100 species (Cribb, 1987), 30 of them exclusively found in freshwater fishes of North America (Hoffman, 1999; Helt, et al., 2003), and only 3 species were described from South America (Travassos et al.,1969; Brooks & MacDonald, 1986; Thatcher, 1993). Gibson (1996) pointed out that species of Phyllodistomum are known for their considerable 48



variation in features, such as egg size, sucker ratio, body shape, etc., and that these features are severely affected by fixation techniques. Considering this, Gibson (1996) proposed that only 6 species of Phyllodistomum would be recognized in North America, a position not accepted by some authors (see Hoffman,1999; Helt et al., 2003). In Mexico, 4 species of Phyllodistomum have been recorded, three of them in marine fishes (LamotheArgumedo, 1969; Bravo & Manter, 1957; Winter, 1957), but only one, P. lacustri, has been recorded in different host species in freshwater fishes in 7 states of the Mexican Republic: Campeche, Chiapas, Jalisco, Michoacán, Tabasco, Tamaulipas and Veracruz (Pérez-Ponce de León et al., 1996; Lamothe-Argumedo et al., 1997; Vidal-Martínez et al., 2001). The only species of Phyllodistomum described from freshwater fishes in Mexico is P. lacustri. It has been recorded as part of the core fauna of ictalurid catfishes in different river basins in the country (see Pérez-Ponce de León & Choudhury, 2002, 2005). Authors such as Vidal-Martínez et al., (2001) allocated the specimens of Phyllodistomum they found in four species of cichlids in southeastern Mexico to P. lacustri. In our opinion, based on the description and drawing provided by these authors (p. 41) their material does not correspond to P. lacustri, but, since no specimens are available for examination, the identity of their material remains questionable. Phyllodistomum lacustri is characterized by having a crenulate margin of the hindbody, i.e. the body margin is composed of a series of small muscular expansions. In this respect and in the position of the vitellaria between the ovary and the acetabulum, it differs from the new species. We have examined more than 60 individuals of Ictalurus furcatus (Lesueur, 1840), a common host for P. lacustri, from the Papaloapan River basin, the same basin from which the new species is described, during the last 2 years and no specimens of P. lacustri have been found. The new species appears to be specific to Centropomus parallelus; however, a closer examination of other species of snook in the Gulf of Mexico slope will determine whether or not this gorgoderid is specific to the host or to all species of Centropomus.

Acknowledgments Thanks are due to Rogelio Rosas Valdez, David Osorio Sarabia, Virginia León Regagnon and Luis García Prieto, Biology Institute, UNAM for their assistance during field work. We thank two anonymous reviewers whose comments greatly improved the original version of this manuscript. This study was partially supported by grant from the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica, Universidad Nacional Autónoma de México (PAPIIT-UNAM) No. IN240904 and IN220605.



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