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Nematodes Found in the Opossum (Didelphis virginiana) and Four Other Species of Mammals in Central Kentucky in 1991 PDF

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Trans. Ky. Acad. Set, 56(3-4), 1995, 128-133 Nematodes Found in the Opossum (Didelphis virginiana) and Four Other Species of Mammals in Central Kentucky in 1991 Eugene T. Lyons, Sharon C. Tolliver, and Shelby Stamper Department ofVeterinary Science, Gluck Equine Research Center, UniversityofKentucky, Lexington, KY40546-0099 AND Brad Snyder Southeastern CooperativeWildlife Disease Study, College ofVeterinary Medicine, UniversityofGeorgia, Athens, GA 30602 Abstract Opossums (n = 50), striped skunks (n = 3), eastern cottontail rabbits (n = 2), muskrats (n = 2), and a coyote,collectedonhorsefarms (n = 14)incentralKentuckyinthefallof1991,wereexaminedforinternal helminths. AU parasites (nematodes, cestodes, and trematodes) recovered were counted. Only nematodes were identified. Speciesofnematodes recoveredfrom opossumswere Capillaria spp., Physalopteraturgida, Strongijloides spp., Longistriata didelphis, Viannaia viannai, and Cruzia americana; striped skunks were Gongijlonema spp., Physaloptera maxillaris, Baylisascaris columnaris, and Strongyloides spp.; eastern cot- tontail rabbits were Oheliscoides cunicidi, Trichostrongyluscalcaratus, and Trichurisleporis; muskratswere Physaloptera spp. and Trichostrongylusspp.; the coyote (onlysmall intestineexamined)wereMolineusbar- hatus, and Uncinariastenocephala. Introduction 1 female, and—1 sex not recorded; eastern cot- Several species of wild mammals were col- tontail ra—bbits 2 adults/1 male and 1 female; lected in central Kentucky in 1991 on farms muskra—ts 1 adult and 1 juvenile/2 females; where leptospirosis had been found in horses. coyote 1 adult male. The purpose was to determine if they were Organs examined for parasites were: lungs carriers for this disease in horses. Collecting (includingthe trachea), liver, esophagus, stom- the mammals provided an opportunity to ex- ach, small intestine, and large intestine. Snips amine some of them for internal parasites. of the lungs, liver, and esophagus were re- Mostly opossums, and lesser numbers of moved for other researchers before a parasi- skunks, eastern cottontail rabbits, muskrats, tologic examination was done. Therefore, and a coyote, were examined for helminths. some parasite specimens from these tissues, Total counts were made for all parasites re- which were examined in fresh condition for covered, but only nematodes were identified. parasites with a stereoscopic microscope (at about 30X), may have been "lost." The gas- Materials and Methods trointestinal tract was separated into stomach, A total of 50 opossums {Didelphis virgini- small intestine, and large intestine, including ana), 3 striped skunks {Mephitis rnephitis), 2 cecum. Contents were emptied into separate eastern cottontail rabbits {Sijlvilagusfioridan- containers and then each segmentwas washed iis), 2 muskrats {Ondatra zibethica), and 1 several times with water. Rinses were added coyote {Canis latrans) were collected from 14 to the appropriate container of contents and horse farms in central Kentucky between No- this material was preserved with 5% formalin. vember 8 and December 12, 1991 for parasi- The gastrointestinal tract was then opened tologic examination. They were trapped by with scissors and any parasites observed by personnel from the Southeastern Cooperative gross examination were removed. Next, each Wildlife Disease Study, University ofGeorgia. portion ofthe gastrointestinal tract was placed — The age/sex categories were: opossums 38 in containers of artificial digestive juice (1% adults and 12—juveniles/26 males and 24 fe- pepsin and 1% HCl in an incubator at 37°C) males; skunks 2 adults and 1juvenile/1 male. for about 3 hours; then, the mucosal side was 128 — Nematodes in Kentucky Mammals Lyons et al. 129 Tablr 1. Data on internal parasites recovered from opossnnis in a surxeyin central Kentncky. OpossumsIn = 50) R.M.K,. Nematodes Capillaha spp.** Lungs — M 3.0 3 1 (2) FM&F 00--77*** 22..12 4496 2222 ((4444)) G.i. tract M 0-S 2.1 30 14 (28) F 0-11 3.1 68 22 (44) M&F 0-11 3.9 98 25 (50) Phijsaloptcni tiirgida*' Imm 2^,300 474.8 23,265 49 (100) M 3-53 18.4 899 49 (100) F 2-79 20.0 978 49 (100) M&F 6-131 38.3 1,877 49 (100) Total 10-i,314 518.4 25,918 50 (100) Strongijloides spp. 0^2 15.0 45 3 (6) Longistriata didelphis M 0-23 4.7 85 18 (36) Liv\gistriaia/\'iannaia F 0-21 7.3 198 27 (54) Viauiiaia viannai M 0-2 1.7 5 3 (6) Cnizia americana Imm 0-1,800 63.1 2,271 36 (72) M 0-242 62.7 2,821 45 (90) F 0-305 75.9 3,568 47 (94) M&F 0-547 135.9 6,389 48 (96) Total 0-1,804 180.4 8,660 48 (96) Imm-Unidentified 0-39 6.8 129 19 (38) Total Nematodes 12-6,119 703.7 35,187 50 (100) Cestodes 0-510 114.4 1,487 13 (26) Trematodes 0-421 69.1 2,419 35 (70) *Mean =valuetorinfectedopossums;**Capillariaspp.—fromlung probaliK'C didelpliKandfromgastrointestinaltract,probablyC lon^icauiia. Sexofonespecimennotdetermined,butincludeddatawithfemales:** *Includes776fromoneopossumtorwhichonlytotalnumbercounted;M =i F = female;Imm = Immature washed under running water while being various reference publications (1-29). Ces- rubbed by hand to remove loosened material. todes and trematodes were not identified. This material and the digest were preserved with 5% formalin; the remainder of the walls Results and Discussion was discarded. Digestionwas done to free par- For the opossums (Table 1), the 2 most asites associated with the walls and mucus. prevalent species of nematodes were Physa- For the single coyote collected, only the small loptera turgida (100%) and Cnizia americana intestine was examined for parasites. (96%). The liigh prevalence of both of these The fixed contents, water rinses, and digests species is similar to that reported by several from the gastrointestinal tract were washed other investigators (4, 11, 18, 30-32). Num- into a series ofsieves (10, 20, 40, 60, and 100 bers of male versus female specimens per in- mesh). Residue was examined for helminths fected animal ranged (mean number/infected with the aid of a stereoscopic microscope at opossum) from 3 to 53 (18.4) and 2 to 79 (20), about 30X. Total counts ofall helminths were respectively, for P. turgida and from to 242 done. Nematodes were identified by usage of (62.7) and to 305 (75.9), respectively for C. — — 130 Trans. Kentucky Academy of Science 56(3-4) Table 2. Data on numberofopossums infectedwith internal parasites relative to farm where collected. Internalparasites Nematode.s Capillariaspp. No. Physal- Stdes. Im Umgi- Farmno. Lungs GItract optera spp. Un-ID itriata** Viannaia Cnizia Cestodes Trematodes No. ofopossums infected 1 3 1 2 3 1 3 3 2 2 3 2 2 3 2 1 2 1 2 3 2 2 1 2 4 5 2 2 5 3 5 1 2 5 1 1 1 1 1 6 6 2 5 6 1 4 6 6 5 6 7 1 1 1 1 1 1 8 3 1 3 3 1 2 1 2 9 4 3 1 4 3 1 4 4 10 4 2 1 4 3 1 4 11 1 1 1 1 1 12 3 2 3 3 3 13 8 2 7 8 1 6 2 8 1 6 14 6 4 5 6 1 6 6 4 5 Total 50 22 25 50 3 19 28 3 48 13 35 (T) inf. (44) (50) (100) (6) (38) (56) (6) (96) (26) (70) *Completenames Physalopterahirgida;Strongylvidesspp;Im. = Immature(Unidentified);LongistriatadidelpliK,Viannaiaviannai,Cntziaamericatia. **-LongistriatadidelphiscategoryincludesL.didelphismalesandlongistriata/Viannaiafemales. americana. Immature specimens (determined Capillaria didelphis was less in 1 study (32) only by much smaller size than adults) varied and more in another (18) compared to that of in number (mean) from 2 to 4,300 (474.8) for Capillaria spp. in the lungs of opossums cur- P. turgida and to 1,800 (63.1) for C. ameri- rently investigated. Strongyloides spp. (21) cana. The 2 next highest prevalent nematode and Viannaia viannai (14) are apparently un- species were Longistriata/Viannaia females common in opossums. The highest total num- (54%) and Capillaria spp. (probably C. longi- ber ofnematodes in an individual opossum in cauda) (50%) from the gastrointestinal tract. the present study was 6,119; it had the great- Longistriata didelphis males were found in est number of immature P. turgida and C. 36% of the opossums. Two other reports in- ainericana. dicated higher prevalence (18, 30) for L. di- Cestodes (0 to 510; mean = 114.4) were delphis. For C. longicauda, lower infection recovered from 26% of the opossums; trema- rates were found in 2 studies (4, 18) than for todes were highly prevalent (70%). The num- Capillaria spp. from the gastrointestinal tract ber ofspecimens oftrematodes varied from in the present study. The number of male L. to 421 (mean = 69.1) per opossum. Data on didelphis varied (mean) from to 23 (4.7) and the number of opossums infected with inter- of female Longistriata/Viannaia from to 21 nal parasites on each farm are recorded (Table (7.3). Capillaria spp. males vs. females were 2). Prevalences ofthe various species or types to 8 (mean = 2.1) and to 11 (3.1), respec- of parasites were highest on Farm No. 6. tively. Most of the Longistriata/Viannaia fe- The 3 skunks examined (Table 3) were all male specimens are probably L. didelphis be- infected with the nematodes Physaloptera cause so few male V. viannai were found. The maxillaris, Baylisascaris columnaris, and females were grouped together because of Strongyloides spp.; Gongylonema spp. were similarities in features. Other nematode spe- found in 1 skunk. Cestodes were present inall cies recovered (prevalence) were: from the 3 individuals, but trematodes in none. Preva- lungs Capillaria spp. (probably—C. didelphis) lence of P. maxillaris in several other studies (44%), and from the intestines unidentified varied greatly (16, 33-35). Baylisascaris co- immatures (38%), Strongyloides spp. (6%), lumnaris were much more prevalent in 2 oth- and Viannaia viannai (6%). Prevalency for er studies (34, 35). Strongyloides spp. were — Nematodes in Kentucky Mammai.s Lyons et al. 1.31 Table 3. Intemal parasites recovered from skunks, eastern cottontail rabbits, innskrats, and a coyote. No i)tparasites .\ninial'iinfecte.l l>ar..Nit,-s Ha„K.- Mean* Tclal No {V,} Skunks (n = 3) Nemat(xles Goniiijlonerna spp. M — 1 1 1 (33) F 1 1 1 (33) M&F 1-1 2 2 1 (33) P/iijsah)ptera maxillaris Inini 295-1,828 921.67 2,765 3 (100) M 30-53 39.00 117 3 (100) F 71-97 80.00 240 3 (100) M&F 102-150 119.00 357 3 (100) Total 400-1,978 1,040.67 3,122 3 (100) Balisascariscolumnaris M 1-18 7.00 21 3 (100) F 3-9 6.67 20 3 (100) M&F 4-27 13.67 41 3 (100) Strongijloides spp. 1-93 38.33 115 3 (100) Cestodes 10-92 39.67 119 3 (100) Eastern cottontail rabbits {n = 2) Obeliscoidesctinictili M 3-4 3.50 7 2 (100) F 1-1 1.00 2 2 (100) M&F 4^ 4.50 9 2 (100) Trichostroni^tjluscalcaratus M 2-2 2.00 4 2 (100) F 4-6 5.00 10 2 (100) M&F 6-8 7.00 14 2 (100) Triclmtislepoiis — M — 1.00 1 1 (50) Cestodes 3.00 3 1 (50) Trematodes 2,570 2,570 1 (50) Muskrats (i1 = 2) Nematodes Phtjsaloptera spp. (Imm) 1-1 1.00 2 2 (100) Trichostrongijlus spp. M — 3.00 3 1 (50) F 4.00 4 1 (50) M&F —3-A 3.50 7 1 (50) Cestodes 2.00 2 1 (50) Trematodes 37-3,758 189.75 3,795 2 (100) Coyote (n = 1) Molincusbarhatus — M — 3.00 3 1 (100) F 5.00 5 1 (100) M&F S-5 8.00 8 1 (100) Uncinanastenocephala M — 6.00 6 1 (100) F 2.00 2 1 (100) M&F 2-6 8.00 8 1 (100) — Cestodes .39.00 39 1 (100) *Mean =valueforinfectedanimals. Imm = Immature;M = male;F = female — 132 Trans. Kentucky Academy of Science 56(3-4) found to be less prevalent by 2 researchers 2. Andrews, C, L. and W. R. Davidson, 1980. Endo- (34, 36). Gongylonenia longispiculum were of parasitesofselectedpopulationsofcottontailrabbits {Syl- low prevalence in 1 study (36). vilagusfloridanus) in the southeastern United States. J. For both cottontail rabbits examined (Table Wildl. Dis. 16:395-401. 3), 2 nematode species, Trichostrongylus cal- 3. Babero, B. B. 1957. Some helminths from lUinois caratus and Oheliscoides cuniculi, were recov- opossums. J. Parasit. 43:232. ered. One rabbit was also infected with Tri- 4. Babero, B. B. 1960. Further studies on helminths ofthe opossum, Didelphis virginiana, with a description churis leporis. Cestodes and trematodes were ofa newspecies from this host. Parasit. 46:455-463. 3p1r,es3e7n)tiinndi1cartaebdbigtr.eaFtoluyrvaortihaebrlerperpoervtasle(n2c,e1o7,f hel5.minBtechksetotf,tJ.heV.mausnkdraVt..GaOlnlidcacJt.hriao.z.19z6i7h.ethAicsaurMvielyleor,f O. cuniculi and T. calcaratus in this species of 1912, in Portage County, Ohio. Parasit. 53:1169-1172. J. rabbit. For T. leporis, 3 investigators reported 6. Butterworth, E. W. and M. Beverley-Burton. 1977. (2, 17, 37) lower infection rates than in the Capillanadidelphis n. sp. (Nematoda:Trichuroidea) from current survey. the opossum, Didelphisvirginiana L. in Georgia. Can. J. The 2 muskrats examined (Table 3) were Zool. 55:616-619. infected with the nematodes, Physaloptera 7. Chandler,A. C. 1932. AnewspeciesofLongisfriato spp. (immature) and Trichostrongylus spp. In (Nematoda) from thecotton rat, Sigmodonhispidus, with addition, cestodes were recovered from 1 notes on the divisionofthe Heligmosominaeintogenera. muskrat and trematodes from both muskrats. J. Parasit. 19:25-31. Physaloptera spp. have been previously found 8. Chandler, A. C. 1933. Notes on the helminth par- asites ofthe opossum (Didelphis virginiana) in southeast (23). Trichostrongylus calcaratus were found Texas, with descriptions of four new species. Proc. U.S. in a few animals in 2 studies (5, 20). Nat. Mus. 81:1-15. In the small intestine of the coyote, the 9. Chandler,A. C. 1942. Thehelminthsofraccoonsin nematodes, Molineus harhatus and Uncinaria EastTexas. Parasit. 28:255-268. J. stenocephala, were present. Also, cestodes 10. Conti, A. 1984. Helminths offoxes and coyotes J. (not Echinococcus spp.), but no trematodes, in Flordia. Proc. Helm. Soc. Wash. 51:36.5-367. were found. Both ofthe species ofnematodes 11. Crites, L. 1956. AredescriptionofCruziaamer- J. were evident previously in low numbers of icana, a nematode parasitic in the opossum, Didelphis coyotes (10, 24). marsupialis virginiana. J. Parasit. 42:68-72. This survey ofinternal parasites gave an in- 12. Dikmans, G. 1932. A newnematodeworm, Vian- dication of species, prevalence, and numbers naiahursohscura fromtheopossum,withanoteonother in some of the wild mammals in the central parasites ofthe opossum. Proc. U.S. Nat. Mus. 79:1-6. 13. Dikmans, G. 1935. New nematodes ofthe genus Kentuckyarea. Especiallymeaningful are data from opossums for which a much greater Longistriata in rodents. J. Wash. Acad. Sci. 25:72-81. 14. Dikmans, G. 1943. The occurrence of Viannaia number were examined than for the other viannai Travassos (Nematoda:Hehgmosomidae) in opos- hosts. Also, further information was obtained sums in North America. Proc. Helm. Soc. Wash. 10:6-7. for Kentucky, supplementing previous surveys 15. Dyer,W. G. 1969. Helminthsofthestripedskunk, for helminths in muskrats in Madison County Mephitis mephitis, in North America. Am. Midi. Nat. 82: (20) and in eastern cottontail rabbits in west- 601-605. ern Kentucky (37). 16. Erickson, A. B. 1946. Incidenceofwormparasites in Minnesota MusteUdaeandhostlists andkeys to North Acknowledgments American species. Am. Midi. Nat. 36:494-509. The investigation reported in this paper 17. Erickson, A. B. 1947. Helminth parasites ofrab- (No. 95-4-072) was made in connection with bits ofthe genus, Syvilagus. J. Wildl. MgtW. 11:255-263. a project of the Kentucky Agricultural Exper- L.1S8e.lf.Fel1d9m72a.n,CDh.araBc.,teJr.isAt.icMsooorfe,coMm.monHhaerlrimsi,ntahnsdoJ.f iment Station and is published with the ap- the Virginia opossum, (Didelphis virginiana) from North proval ofthe director. Carolina. Lab. An. Sci. 22:183-189. 19. Graybill,H.W. 1924. Anewspeciesofroundworm Literature Cited ofthe genus Trichostrongylusfrom the rabbit. Proc. U.S. 1. Anderson, R. C. 1992. Nematode parasites ofver- Nat. Mus. 66:1-3. tebrates,theirdevelopmentandtransmission. CABI, Uni- 20. Harley J. P. 1972. A survey of the helminths of versity Press, Cambridge, England (Distributed U.S.A. themuskratOndatraz. zihethica Miller, 1972,inMadison The UniversityofArizona Press, Tucson), 578 pp. County, Kentucky. Tran. Ky. Acad. Sci. 33:13-15. — Nematodes in Kentucky Mammai,s Lyons et al. 133 21. Little, M. D. 1966. Seven new species of Sfroii- 29. Yorke, W. and P A. Maplestone. 1926. The nem- ^ijlokles (Neniatoda) from Louisiana. J. Parasit. 52:85-97. atode parasites of vertebrates. P. Blaldston's Son & Co., 22. Morgan, B. 194L A summary ofthe Physalopter- Philadelphia,536 pp. inae (Nematoda) of North America. Proc. Helm. Soc. 30. C;ra\-, J. B. and R. C. Anderson. 1982. Observa- Wash. 8:28-30. tions on Turgichi turgida (Rudolphi, 1819) (Nematoda: 23. Penn, G. H., Jr. 1942. Parasitological survey of Physalopteroidea) in the American opossum {Didclphis Louisiana muskrats. J. Parasit. 28:348-349. virginiana). J. Wildl. Dis. 18:279-285. 24. Seesee, F. M., M. C. Sterner, and D. E. Worlev. 31. Holloway, H. L., Jr. 1966. Helminths of rabbits 1983. Helminths of the coyote {Canis latrans Sav) in and opossums at Mountain Lake, Virginia. Bull. Wildl. Montana. J. Wildl. Dis. 19:54-55. Dis. Assoc. 2:38-39. 25. Skrjabin, K. I., N. P Shikliobaloxa, and R. S. 32. Miller, G. C. and R. Harkema. 1970. Helminths Shul'ts. 1954. Trichostrongv'lids of animals and man. In ofthe opossum (Didelphis virginiana) in North CaroHna. K. I. Skrjabin (ed.) Essentials ofnematodolog\, \'ol. III. Proc. Helm. Soc. Wash. 37:36-39. IzdatelstvoAcad. Nauk. S.S.S.R., Moscow. IsraelProgram 33. Dyer,W. B. 1970. Helminthsofthestripedskunk. for ScientificTranslations, Jenisalem, 1960. Mephitis mephitis Schreber, in North Dakota. Proc. 26. Skrjabin, K. I., N. P. Shikhobalova, R. S. Shults. Helm. Soc. Wash. 37:92-93. 1954. Dictyocauhdae, HeligmosomatidaeandOllulanidae 34. Goldberg, A. 1954. Parasites of skunks in the ofanimals. In K. I. Skrjabin (ed.) Essentials of nemato- Belts\ille, Mar\land area. Proc. Helm. Wash. Soc. 21:29- dolog).Vol. I\'. Izdatel'stvoAcad. Nauk. S.S.S.R., Moscow. 34. Israel Program for Scientific Translations, Jerusalem, 35. Mead, R. A. 1963. Some aspects ofparasitism in 1971. 27. Skrjabin, K. I., A. A. Sobolev, and V. M. Ivaskin. skunks ofthe SacramentoValleyofCalifornia. Am. Midi. 1967. Spinirata of animals and man and the diseases Nat. 70:164-167. caused bv them. Thehizioidea. Part 4. In K. I. Skrjabin 36. Babero, B. B. 1960. A survev of parasitism in (ed.) Essentials of nematodology. Vol. XVI. Izdatel'stvo skimks(Mephitismephitis)in Louisiana,withobser\ations Acad. Nauk. S.S.S.R., Moscow. Israel Program for Sci. on pathological damages due to helminthiasis. J. Parasit. Translations, Jerusalem, 1971. 46:26-27 (Abstr.). 28. Travassos,L. 1937. RevisaodafamiliaTrichostron- 37. Strohlein, D. A. and B. M. Christensen. 1983. gylidae Leiper, 1912. Monographias do InstltutoOswaldo Metazoan parasites of the eastern cottontail rabbit in Cruz, Rio de Janerio. western Kentuck-\-. J. Wildl. Dis. 19:20-23.

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