Nematodes and Acanthocephalans of Raccoons (Procyon Lotor}, with a New Geographical Record for Centrorhynchus Conspectus (Acanthocephala) in South Carolina, U.S.A
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J. Helminthol. Soc. Wash. 66(2), 1999 pp. 11 1-114 Nematodes and Acanthocephalans of Raccoons (Procyon lotor}, with a New Geographical Record for Centrorhynchus conspectus (Acanthocephala) in South Carolina, U.S.A. MICHAEL J. YABSLEY AND GAYLE PITTMAN NoBLET1 Department of Biological Sciences, Clemson University, Clemson, South Carolina 29634-1903, U.S.A. (e-- mail: [email protected]; [email protected]) ABSTRACT: From April 1997 through April 1998, 128 raccoons (Procyon lotor (Linnaeus)) collected from 7 sites representing 4 physiographic areas in South Carolina were examined for gastrointestinal helminth parasites. Four species of nematodes (Gnathostoma procyonis (Chandler), Physaloptera rara Hall and Wigdor, Arthroce- phahis lotoris (Schwartz), and Molineus barhatus Chandler) and 2 species of acanthocephalans (Macracantho- rhynchus ingens (von Linstow) and Centrorhynchus conspectus Van Cleave and Pratt) were collected. The finding of 11 immature C. conspectus in 3 South Carolina raccoons represents a new geographical record for this species. KEY WORDS: Centrorhynchus conspectus, raccoon, Procyon lotor, Nematoda, Acanthocephala, helminths, Gnathostoma procyonis, Physaloptera rara, Arthrocephalus lotoris, Molineus barbatus, Macracanthorhynchus ingens, South Carolina, U.S.A. The raccoon (Procyon lotor (Linnaeus, 1758)) farm areas of Horry County (Lower Coastal Plains is an omnivore that ranges over most of North North, LCPN); Site 4 included both beach and wooded habitats in the tourist area of Myrtle Beach, Horry America and occurs in both rural and urban set- County (LCPN); Site 5 was a swamp located on the tings. Consequently, the range of zoonoses for Savannah River in Hampton County (Lower Coastal raccoons is important in assessing risk to hu- Plains South, LCPS); and Sites 6 and 7 were both on mans and domestic animals. In South Carolina, barrier islands located in Charleston County (LCPS). John's Island (Site 6), next to and continuous with the only limited studies on helminth parasites of rac- mainland at times of low tide, is primarily forest and coons have been reported previously (Harkema farmland with many freshwater ponds, whereas Sea- and Miller, 1964; Stansell, 1974). More recent brook Island (Site 7) is a small residential island about reports of serious human illnesses from the 1.5 km offshore, which lacks freshwater habitats. Each northern and midwestern United States, such as raccoon was subjected to multiple evaluations, which cerebrospinal nematodiasis because of infection included not only our study of gastrointestinal hel- minth parasites, but also seroprevalence, culture and with the gastrointestinal nematode Baylisascaris DNA studies for Trypanosoma cruzi, and museum procyonis (Stefanski and Zarnowski, 1951), led study specimens. In addition, most animals were in- to the current study, which includes raccoons cluded in a trap-type capture effectiveness study con- collected statewide from a wide variety of hab- ducted by the South Carolina Department of Natural itats (e.g., mountains, farms, urban areas, beach- Resources (SCDNR). Raccoons were either euthanized by intramuscular es, swamps, and barrier islands), allowing for a injection of 0.2 ml/kg ketamine/xylazine followed by comparison of parasite burdens and consider- intraperitoneal injection of 1 ml/kg sodium pentobarbital, ation of human health risks associated with these or were hunter-shot. Stomach and intestines from each parasites (Williams et al., 1997; Boschetti and animal were examined as soon as possible after death Kasznica, 1995). (within 1-2 hr). However, animals from 2 of the phys- iographic regions (Sites 3-7) were frozen at — 4°C for 1-3 mo prior to examination for helminths because of Materials and Materials the use of the animals for a trap-type study conducted Raccoons (n = 128) were collected between April by the International Association of Fish and Wildlife 1997 and April 1998 with foot-hold traps or wire live- Agencies. Therefore, trematodes and cestodes were ex- traps. Traps were set at 7 sites that included 4 of the cluded from the overall analyses because freezing of a 5 physiographic areas of South Carolina. Site 1 in- large number of hosts resulted in difficult collection cluded both urban and waterfowl management areas and unreliable identification of flatworms. (WMA) in Pickens County (Foothills); Site 2 was a All nematodes collected from the stomachs and WMA in Union County (Piedmont); Site 3 was inland small intestines of raccoons were preserved and stored in a 70% ethanol-5% glycerine solution. Representative specimens of each nematode were mounted in glyc- 1 Corresponding author. erine jelly. Acanthocephalans collected from the small 111 Copyright © 2011, The Helminthological Society of Washington 12 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 66(2), JULY 1999 intestine were placed in water until the proboscis evert- "E a 0) NO ed, preserved in acetic acid-formalin-alcohol (AFA), 00 C — >O ^J" ^j" CO ^N c — — oo ON •* ON and stored in 70% ethanol. Temporary wet mounts and J. J. J. J. ' ' OJj s permanent Mayer's acid carmine-stained mounts in 3 o Canada balsam were made for identification. Voucher ^ specimens deposited at the U.S. National Parasite Col- 5 3 tfl __ t^ q GO V") t~-; NO ON CO P~; lection in Beltsville, Maryland, have been assigned " , i O V~l CO NO • — CN sON USNPC accession numbers 87838-87843. Fisher's ex- iH C +1 +1 +1 +1 +1 +1 9 CN r- ON NO r- t- act test was used to detect significant differences (P < c M •^t oo ON CO ON CO a CO — CN 0.05) in helminth prevalence (%) between study sites. * Two-thirds of the animals caught were male, and 85% E o U of all animals were mature. Because of the large bias •a oo toward males and adults, no statistical analyses were £ — 00 00 CO CO ^^ a •f2 ^t CO CN -^ V~) CN performed. a a u CN ON NO NO OO CO j3 s ~ IO ^1" CO • — ' NO 0 to "~ Results and Discussion « U NO — ^ CM ^^ >-^ ^-~. ^^ r-~ ^^ Of the 128 raccoons examined, 103 (80%) *j 2 u o o ** c — o were infected with 1 or more of the 4 nematodes o C O — O TJ- C and 2 acanthocephalans listed in Table 1. Gna- JS thostoma procyonis Chandler, 1942, and Phy- ^^ « ™ !o oo ^ ^ in ^ B u V) — ^ ^t ON i/~) ON i ^ saloptera rara Hall and Wigdor, 1918, were re- 1 •g NO CN >/1 — NO — "o a covered primarily from the stomach. Arthroce- CJ 0 u c c -^ ^ phalus (=Placoconus) lotoris (Schwartz, 1925) ,g f^ C S — o ^-. 10 CO oo r- CN — oo o and Molineus barbatus Chandler, 1942, were 1) ,, o .•s ii ON >O t — • "^" 00 O collected from the posterior and anterior ends of ~ V5 ,., CN CN N the small intestine, respectively. Both Macra- |> 'o u canthorhynchus ingens (von Linstow, 1879) and 1 •* ^ 1 C 00 CN — NO C Qq Centrorhynchus conspectus Van Cleave and e c s O — CO CN OO O o C3 ~" Pratt, 1940, were recovered exclusively from the o U u u C3 small intestine. Interestingly, 96.1% of raccoons 03 e £ ^ ^ ^^ ^ ^ ^ !c r — r^- CN t— NO — examined from Sites 1-6 were infected with at (U 00 .S II least 1 helminth species, whereas only 5 of 26 i — — CO — ON (N E (19.2%) raccoons examined from Seabrook Is- 0 tM land (Site 7) were infected. (N >0 0 ^ O ^ O ^ Gnathostoma procyonis, a stomach nematode C a u •* O •* O CN C JS X s CN O CN O — O that forms large nodules in the mucosa, was a found at Sites 3 and 5 in significantly larger u u *o . — X , — s , * ^ — s o " CN numbers than at other sites (Table 1). Extensive 1) — CO O CO -3" C .S II 00 ^ *t O >/~> OO CN O freshwater habitats were present at both sites, 1 CN — •— providing a favorable environment for the re- s •o quired first intermediate host, which is 1 of sev- e __ a c ..... eral species of cyclopoid copepods (Miyazaki, VI fll ^ tjo <u .« o ^ "3 oo J- oo oo" oo So oo oo 1960). In contrast, no infections of G. procyonis o were observed at 2 coastal locations (Sites 4 and "S E u 7), which lacked permanent freshwater habitats. e Physaloptera rara, a spirurid nematode recov- o c^ ered from both the stomach and small intestine "3 I; 5 •e >• -Ii ^ of hosts, does not require the presence of fresh- OJ water habitats, because raccoons become infect- 'S -^2 ^ Ci. 03 a K c -^ K ed by ingestion of various terrestrial arthropods D. E O (e.g., Gryllus pennsylvanicus Burmeister, 1838, G X s *s» ~S? "B "S5 "*^- "35* c« tL) Pennsylvania field cricket; Blattella germanica • •S X *^- ^ Q" S ^ l-H u ^ S^"^J"-* CJ "^"^ a. "O ^; *^. O ^ O C ^ (Linnaeus, 1767), German cockroach; and Cen- JU . 00 tophiles spp., camel crickets) (Lincoln and An- 2 c5 2*5i?hP § ^ t: £^ -^^^ ^§^ derson, 1973). Compared to all other sites, a sig- H S £ <» w Copyright © 2011, The Helminthological Society of Washington YABSLEY AND NOBLET—HELMINTHS OF RACCOONS 13 nificantly higher prevalence of P. ram was ob- a single infected raccoon [Babero and Shepper- served in raccoons trapped at Site 1, with urban- son, 1958; Kazacos and Boyce, 1989]) suggests captured animals dominating the number of the possibility of introduction of this nematode infected animals. Because broad host specificity into South Carolina. has been documented for physalopteroids, do- The most prevalent parasite collected was the mesticated animals could accumulate large num- acanthocephalan M. ingens. Infections occurred bers of these worms by ingesting an infected in- in raccoons from all study sites, with an overall termediate host that commonly occurs in urban prevalence of 53%. Although not considered a settings (Morgan, 1941). threat to public health, M.