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 helminth 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 physiographic 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

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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 • -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

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. ingens infection in High prevalences of both the raccoon hook- humans has been reported (Dingley and Beaver, worm, A. lotoris, and the trichostrongylid, M. 1985). barbatus, frequently have been reported in pre- Six species of the acanthocephalan genus vious surveys (Harkema and Miller, 1964; Cole Centrorhynchus have been reported from North and Shoop, 1987). In the present study, however, American birds of prey; however, little is known overall prevalence of A. lotoris and M. barbatus about the life cycle, geographical distribution, or was 28.1 and 12.5%, respectively (Table 1). prevalence of these acanthocephalan species. Data from Seabrook Island are consistent with Read (1950) demonstrated experimentally that those of Harkema and Miller (1962), who pre- Centrorhynchus spinosus (Kaiser, 1893) was ca- viously reported an almost complete absence of pable of developing to adults in laboratory rats, A. lotoris and M. barbatus from Cape Island, suggesting that members of this genus have the South Carolina. These investigators suggested ability to complete development not only in bird that the low prevalence of these 2 nematodes on definitive hosts, but also in mammalian hosts. coastal islands was due possibly to the detri- One raccoon from John's Island (Site 6) and 2 mental effect of high tides, salinity of soil, and raccoons from the Horry County inland site (Site dry habitats on the free-living larval stages of 3) were infected with immature C. conspectus. these helminths. Additionally, seasonal varia- Prior to the current study, immature forms of C. tions have been documented, with lower preva- conspectus had been reported from 26 mammals lence during winter months (Smith et al., 1985), representing 6 host species (3 Didelphis virgi- which could have contributed to the lower num- niana Kerr, 1792, Virginia opossum; 3 P. lotor, bers observed in the current survey. raccoon; 17 Mustela vison Schreber, 1775, mink; Although B. procyonis was not collected from 1 Spilogale putorius (Linnaeus, 1758), spotted any raccoon examined in this study, surveillance skunk; 1 Blarina brevicauda Gray, 1838, short- for this parasite should be continued because of tailed shrew; and 1 Urocyon cinereoargenteus its medical and veterinary significance and its Schreber, 1775, gray fox) from 5 states (Virgin- reported widespread distribution in the United ia, Arkansas, North Carolina, Ohio, and Florida) States (Kazacos and Boyce, 1989). Based on re- (Nickol, 1969; see Richardson and Nickol, ports from southeastern states, Jones and Mc- 1995). The largest number of worms previously Ginnes (1983) suggested that B. procyonis was reported from any individual mammalian host found primarily in the more mountainous re- was 2 worms, whereas 1 raccoon in the current gions. The northwestern range of our study site, survey from the inland Horry County site (Site although classified as "Foothills," is not truly 3) was infected with 9 C. conspectus (see Rich- mountainous, which might account for the lack ardson and Nickol, 1995). Several owl species, of B. procyonis. In contrast, however, B. pro- including Bubo virginianus (Gmelin, 1788), the cyonis recently was found in 70% of 33 rac- great horned owl; Otus asio (Linnaeus, 1758), coons examined in southern coastal Texas (Kerr the eastern screech owl; and Strix varia Barton, et al., 1997). These investigators suggested that 1799, the barred owl, have been reported as de- the nematode could have been acquired by in- finitive hosts for C. conspectus (Richardson and gestion of larvae in migratory wild birds, intro- Nickol, 1995). No intermediate host has been duced from infected translocated raccoons, or identified, although cystacanths of C. conspectus the result of a northern expansion from Latin have been found in paratenic hosts (Nerodia si- America. This recent finding of B. procyonis in pedon (Linnaeus, 1758), the water snake, from southern Texas and limited reports from the ad- North Carolina; Rana clamitans Latreille, 1801, jacent state of Georgia (only 2 reports, each of the aquatic green frog, from Virginia; and Des-

Copyright © 2011, The Helminthological Society of Washington 114 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 66(2), JULY 1999 inognathus fuscus (Green, 1818), the northern Kazacos, K. R., and W. M. Boyce. 1989. Baylisas- caris larva migrans. Journal of the American Vet- dusky salamander and Plethodon glutinosus erinary Medical Association 195:894-903. (Green, 1818), the slimy salamander from Lou- Kerr, C. L., S. C. Henke, and D. B. Pence. 1997 isiana) (Nickol, 1969; see Richardson and Nick- Baylisascariasis in raccoons from southern coastal ol, 1995). The finding of 11 immature C. con- Texas. Journal of Wildlife Diseases 33:653-655. spectus in 3 South Carolina raccoons represents Lincoln, R. C., and R. C. Anderson. 1973. The re- lationship of Physaloptera maxillaris (Nematoda: a new geographical record for this species. The Physalopteroidea) to skunk (Mephitis mephitis). collection only of immature C. conspectus from Canadian Journal of Zoology 51:437-441. raccoons in this study supports earlier reports Miyazaki, I. 1960. On the genus Gnathostoma and that suggested that wild mammals are aberrant human gnathostomiasis, with special reference to Japan. Experimental Parasitology 9:338-370. hosts for this parasite (Richardson, 1993). Morgan, B. B. 1941. A summary of Physalopterinae (Nematoda) of North America. Proceedings of the Acknowledgments Helminthological Society of Washington 8:28-30. Nickol, B. B. 1969. Acanthocephala of Louisiana Cau- The authors thank Osborne E. (Buddy) Baker data with notes on the life history of Centrorhyn- III, SCDNR, for aid in procuring coastal raccoon chus conspectus. American Midland Naturalist 81: specimens, and Dr. William C. Bridges, Jr., De- 262-265. partment of Experimental Statistics, Clemson Read, C. P. 1950. The rat as an experimental host of Centrorhynchus spinosus (Kaiser, 1893), with re- University, for assistance with statistical meth- marks on host specificity of the Acanthocephala. ods. Transactions of the American Microscopical So- ciety 69:179-182. Literature Cited Richardson, D. J. 1993. Acanthocephala of the Vir- ginia opossum (Didelphis virginiand) in Arkansas, Babero, B. B., and J. R. Shepperson. 1958. Some with a note on the life history of Centrorhynchus helminths of raccoons in Georgia. Journal of Par- wardae (Centrorhynchidae). Journal of the Hel- asitology 44:519. minthological Society of Washington 60:128-130. Boschetti, A., and J. Kasznica. 1995. Visceral larva , and B. B. Nickol. 1995. The genus Centro- migrans induced eosinophilic cardiac pseudotu- rhynchus (Acanthocephala) in North America mor: a cause of sudden death in a child. Journal with description of Centrorhynchus robustus n. of Forensic Sciences 40:1097-1099. sp., redescription of Centrorhynchus conspectus, Cole, R. A., and W. L. Shoop. 1987. Helminths of and a key to species. Journal of Parasitology 81: the raccoon (Procyon lotor) in western Kentucky. 737-772. Journal of Parasitology 73:762-768. Smith, R. A., M. L. Kennedy, and W. E. Wilhelm. Dingley, D., and P. C. Beaver. 1985. Macracantho- 1985. Helminth parasites of the raccoon (Procyon rhynchus ingens from a child in Texas. American lotor) from Tennessee and Kentucky. Journal of Journal of Tropical Medicine and Hygiene 34: Parasitology 71:599-601. 918-920. Stansell, K. B. 1974. Internal parasites of coastal rac- Harkema, R., and G. C. Miller. 1962. Helminths of coons with notes on changes in parasite burdens Procyon lotor solutus from Cape Island, South after transportation and release in the upper Pied- Carolina. Journal of Parasitology 48:333-335. mont section of South Carolina. Statewide Wild- , and . 1964. Helminth parasites of the life Research Project, South Carolina Wildlife and raccoon, Procyon lotor, in the southeastern United Marine Resources Department, 112 pp. States. Journal of Parasitology 50:60-66. Williams, C. K., R. D. McKown, J. K. Veatch, and Jones, E. J., and B. S. McGinnes. 1983. Distribution R. D. Applegate. 1997. Baylisascaris sp. found of adult Baylisascaris procyonis in raccoons from in a wild northern bobwhite (Colinus virginianus). Virginia. Journal of Parasitology 69:653. Journal of Wildlife Diseases 33:158-160.