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First report of Ochetosoma aniarum (Digenea: Ochetosomatidae) from the Brazos water snake, Nerodia harteri (Serpentes: Colubridae), in Texas, with a summary of definitive hosts of this parasite.

The Brazos water snake, Nerodia harteri, is a medium-sized colubrid endemic to the Brazos River system of 11 counties of northcentral Texas (Dorcas & Mendelson 1991; Conant & Collins 1998; Dixon 2000; Werler & Dixon 2000; Ernst & Ernst 2003). Discovered in 1936 in Palo Pinto County in the Brazos River, the species was later described by Trapido (1941). This snake fills a unique niche within this riverine habitat typified by fast-flowing rocky stream riffles of the upper Brazos River and two of its tributaries. Although not currently listed as federally threatened or endangered by the U.S. Fish and Wildlife Service, the species is considered threatened by the Texas Parks and Wildlife Department (TPWD 2007). In addition, N. harteri is globally listed G2 (NatureServe 2007) due to its restricted range and habitat requirements.

Detailed information is available on various aspects of the natural history of this snake (Mecham 1983; Scott et al. 1989); however, very little is known about its parasites. McAllister & Upton (1989) reported three eimerians and a Cryptosporidium sp. from Brazos water snakes from Somervell and Palo Pinto counties, and Upton et al. (1989) further described a Cryptosporidium sp. in a single N. harteri from the latter county. The only previous report on helminth parasites was by Rossi & Rossi (2000) who reported Strongyloides sp. and unidentified filiarial worms from captive N. harteri.

On 18 July 1987 and again between 6 May 1988 and 29 July 1988, 10 juvenile and adult N. harteri (four males, six females; SVL range = 340-710 mm, mean [+ or -] 1SD = 547.5 [+ or -] 113.4 mm) were collected by hand or tong from two sites on the Brazos River, one below Possum Kingdom Dam, 11.3 km SW Graford off FM 4, Palo Pinto County (n = 3, 32[degrees] 52.02'N, 98[degrees] 25.03'W), and the other 8.0 km S Glen Rose off FM 200, Somervell County (n = 7, 32[degrees] 16.16'N, 97[degrees] 39.51'W). Several of these snakes were the same specimens reported in McAllister & Upton (1989). Specimens were placed in individual collecting bags on ice and within 24 hr anesthetized with sodium pentobarbital (Nembutal[R]) overdose, and their gastrointestinal tract from their mouth to cloaca examined for helminth parasites. Trematodes were fixed in 10% neutral buffered formalin, transferred to 70% ethanol, stained with Semichon's acetocarmine, and mounted in Canada Balsam. Voucher specimens of parasites are deposited in the United States National Parasite Collection (USNPC), Beltsville, Maryland, USA, as USNPC 84293. Snake voucher specimens are deposited in the Arkansas State University Museum, Herpetological Collection, State University, Arkansas, as ASUMZ 8420, 11221, 11762-11766, and the Cedar Valley College Collection (CVC), Lancaster, Texas, as 880520-18, 880708-6, and 880729-1.

One of 10 (10%) N. harteri (655 mm SVL female, CVC 880708-6) collected from the Somervell County site on 8 July 1988 was found to be infected in its mouth with four specimens of the digenean trematode Ochetosoma aniarum. This was the only helminth found in this small sample of snakes. The parasite was originally described by Leidy (1890) as Distomum aniarum from the northern water snake, Nerodia sipedon, from Pennsylvania. In addition, Dubois & Mahon (1959) listed Renifer acetabular is, R. orula, R. natricis, R. texanus, and R. wardi as synonyms of O. aniarum. It would appear that Dubois & Mahon (1959) were unaware that Skrjabin & Antipin (1957) had previously transferred the above species of Renifer to Ochetosoma. The current arthors are in agreement with the latter synonymy although some disagreement currently exists (see Ernst & Ernst 2006).

This parasite has previously been reported in two viperids and several colubrid snakes from various North American localities, including Texas (Table 1). From this summation it is obvious that most of these hosts are semiaquatic or aquatic species (primarily Nerodia spp.) that occasionally feed on frogs.
Table 1. North American definitive hosts of Ochetosoma aniarum.
Variously reported as synonyms Neorenifer aniarum, Neorenifer
acetabularis, Renifer acetabularis, R. orula, R. natricis, R. texanus,
and R. wardi. Host scientific names follow Crother et al. (2000) and
Crother et al. (2003).

Family/Host Locale Reference

Colubridae

 Coluber constrictor unknown Wallander (1968)
 constrictor

 C. constrictor Nebraska Brooks (1979)
 flaviventris

 C. constrictor foxii unknown Wallander (1968)

 Farancia abacura unknown MacCallum (1921)
 abacura

 Heterodon platirhinos Texas Harwood (1932)

 unknown Wallander (1968)

 Heterodon simus unknown Wallander (1968)

 Lampropeltis getula Florida Parker (1941)
 floridana

 unknown Wallander (l968)

 L. getula holbrooki Louisiana Rabalais (l969)

 Texas Dronen & Guidry (1977)

 Nerodia cyclopion Florida Parker (1941)

 Illinois Dyer & Ballard (1991)

 Louisiana Rabalais (1969); Brooks
 (1979); Fontenot & Font
 (1996)

 Mississippi Byrd (1935)

 N. erythrogaster North Carolina Collins (1969)
 erythrogaster

 Tennessee Parker (1941)

 N. erythrogaster Alabama Detterline et al. (1984)
 flavigaster

 Arkansas (Lonoke previously unpublished
 County)

 Illinois Dyer (1999)

 Louisiana Rabalais (1969); Brooks
 (1979)

 Mississippi Byrd (1935)

 N. erythrogaster Mexico (Nuevo Jimnez & Caballero (1975)
 transversa Leon)

 Texas Curfman & Davidson (1966);
 previously unpublished

 N. fasciata confluens Louisiana Rabalais (1969); Brooks
 (1979); Fontenot& Font
 (1996)

 Texas Harwood (1932)

 N. fasciata fasciata Louisiana Rabalais (1969)

 N. fasciata Florida Parker (1941)
 pictiventris

 N. harteri Texas This study (new host
 record)

 N. rhombifer rhombifer Illinois Dyer (1999)

 Kansas Crow (1913)

 Louisiana Rabalais (1969); Fontenot &
 Font (1996)

 Mississippi Byrd (1935); (1937)

 Tennessee Parker (1941)

 N. sipedon pleuralis Alabama Detterline et al. (1984)

 North Carolina Collins (1969)

 Texas Harwood (1932)

 N. sipedon sipedon Michigan Talbot (1934)

 Pennsylvania Leidy (1890)

 N. taxispilota Georgia Camp (1980)

 North Carolina Collins (1969)

 Seminatrix pygaea Florida Parker (1941)

Viperidae

 Agkistrodon piscivorus Louisiana Rabalais (1969)
 leucostoma

 A. piscivorus North Carolina Collins (1969)
 piscivorus


In the life cycle, eggs containing miracidia hatch after being eaten by pulmonate snails (Physa spp.) and develop into daughter sporocysts. After leaving snails, cercariae penetrate and encyst in tadpoles of the genera Lithobates, Hyla and Pseudacris, which, when fed to snakes of the genus Nerodia, adult flukes occurred in the mouth and esophagus of definitive hosts 35 days later (Byrd 1935; Walker 1939; Schell 1985). Although N. harteri most often feeds on small fishes, primarily minnows (Tennant 1984; Werler & Dixon 2000) related neonate Concho water snakes, N. paucimaculata, has been reported to eat cricket frogs, Acris crepitans, by Greene et al. (1994). This may help explain the low prevalence of O. aniarum in N. harteri.

ACKNOWLEDGMENTS

We thank B. D. Earle (Cedar Valley College) for assistance with collecting, owners of I. F. Anderson Farms (Lonoke, Arkansas) for allowing the senior author to collect on their properties, and the Arkansas Game and Fish Commission and Texas Parks and Wildlife Department for Scientific Collecting Permits nos. 775, and SPR-044-1 and SPR-0390-027, respectively, issued to C.T.M.

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CTM at: drctmcallister@aol.com

Chris T. McAllister and Charles R. Bursey

Department of Physical & Life Sciences Chadron State College Chadron, Nebraska 69337 and Department of Biology Pennsylvania State University-Shenango Campus Sharon, Pennsylvania 16146
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Author:McAllister, Chris T.; Bursey, Charles R.
Publication:The Texas Journal of Science
Date:Feb 1, 2008
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