Parasitology Research

, Volume 114, Issue 12, pp 4451–4461 | Cite as

Alaria mesocercariae in the tails of red-sided garter snakes: evidence for parasite-mediated caudectomy

  • Emily J. Uhrig
  • Sean T. Spagnoli
  • Vasyl V. Tkach
  • Michael L. Kent
  • Robert T. Mason
Original Paper

Abstract

Trematodes of the genus Alaria develop into an arrested stage, known as mesocercariae, within their amphibian second intermediate host. The mesocercariae are frequently transmitted to a non-obligate paratenic host before reaching a definitive host where further development and reproduction can occur. Snakes are common paratenic hosts for Alaria spp. with the mesocercariae often aggregating in the host’s tail. In the current study, we used morphological examination and molecular analyses based on partial sequences of nuclear large ribosomal subunit gene and mitochondrial cytochrome C oxidase subunit 1 gene to identify larvae in the tails of red-sided garter snakes (Thamnophis sirtalis parietalis) as mesocercariae of Alaria marcianae, Alaria mustelae, and Alaria sp. as well as metacercariae of Diplostomidae sp. of unknown generic affiliation. We assessed infection prevalence, absolute and relative intensity, and associated pathological changes in these snakes. Infection prevalence was 100 % for both male and female snakes. Infection intensity ranged from 11 to more than 2000 mesocercariae per snake tail but did not differ between the sexes. Gross pathological changes included tail swelling while histopathological changes included mild inflammation and the presence of mucus-filled pseudocysts surrounding mesocercariae, as well as the compression and degeneration of muscle fibers. Our results indicate that mesocercariae can lead to extensive muscle damage and loss in both sexes which likely increases the fragility of the tail making it more prone to breakage. As tail loss in garter snakes can affect both survival and reproduction, infection by Alaria mesocercariae clearly has serious fitness implications for these snakes.

Keywords

Trematodes Alaria Snakes Thamnophis Histopathology Molecular Identification 

References

  1. Aleksiuk M, Stewart KW (1971) Seasonal changes in the body composition of the garter snake (Thamnophis sirtalis parietalis) at northern lattitudes. Ecology 52:485–490. doi:10.2307/1937631 CrossRefGoogle Scholar
  2. Anthony RM, Rutitzky LI, Urban JF, Stadecker MJ, Gause WC (2007) Protective immune mechanisms in helminth infection. Nat Rev Immunol 7:975–987PubMedCentralCrossRefPubMedGoogle Scholar
  3. Behm CA, Ovington KS (2000) The role of eosinophils in parasitic helminth infections: insights from genetically modified mice. Parasitol Today 16:202–209CrossRefPubMedGoogle Scholar
  4. Bosma NJ (1934) The life history of the trematode Alaria mustelae, Bosma, 1931. Trans Am Microsc Soc 53:116–153. doi:10.2307/3222088 CrossRefGoogle Scholar
  5. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583CrossRefPubMedGoogle Scholar
  6. Chandler AC (1942) The morphology and life cycle of a new strigeid, Fibricola texensis, parasitic in raccoons. Trans Am Microsc Soc 61:156–167CrossRefGoogle Scholar
  7. Cooper WE, Alfieri KJ (1993) Caudal autotomy in the eastern garter snake, Thamnophis s. sirtalis. Amphibia-Reptilia 14:86–89CrossRefGoogle Scholar
  8. Fernandes BJ, Cooper JD, Cullen JB, Freeman RS, Ritchie AC, Scott AA, Stuart PF (1976) Systemic infection with Alaria americana (Trematoda). Can Med Assoc J 115:1111–1114PubMedCentralPubMedGoogle Scholar
  9. Fernandes FR, Cruz LD, Linhares AX (2012) Effects of sex and locality on the abundance of lice on the wild rodent Oligoryzomys nigripes. Parasitol Res 111:1701–1706CrossRefPubMedGoogle Scholar
  10. Fitch HS (2003) Tail loss in garter snakes. Herpetol Rev 34:212–213Google Scholar
  11. Foster N, Elsheikha HM (2012) The immune response to parasitic helminths of veterinary importance and its potential manipulation for future vaccine control strategies. Parasitol Res 110:1587–1599CrossRefPubMedGoogle Scholar
  12. Freeman RS, Stuart PF, Cullen JB, Ritchie AC, Mildon A, Fernandes BJ, Bonin R (1976) Fatal human infection with mesocercariae of the trematode Alaria americana. Am J Trop Med Hyg 25:803–807PubMedGoogle Scholar
  13. Goldberg SR, Bursey CR (2002) Gastrointestinal helminths of the blackneck garter snake, Thamnophis cyrtopsis (Colubridae). West N Am Naturalist 62:243–245Google Scholar
  14. Gregory PT, Stewart KW (1975) Long-distance dispersal and feeding strategy of the red-sided garter snake (Thamnophis sirtalis parietalis) in the Interlake of Manitoba. Can J Zool 53:238–245CrossRefGoogle Scholar
  15. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  16. Hofer DP, Johnson AD (1970) Alaria mustelae, A. marcianae, and A. arisaemoides: chemical nature of mesocercarial capsule. Trans Am Microsc Soc 89:254–259. doi:10.2307/3224382 CrossRefGoogle Scholar
  17. Jiménez-Ruiz FA, García-Prieto L, De León GPP (2009) Helminth infracommunity structure of the sympatric garter snakes Thamnophis eques and Thamnophis melanogaster from the Mesa Central of Mexico. J Parasitol 88:454–460CrossRefGoogle Scholar
  18. Johnson A (1968) Life History of Alaria marcianae (La Rue, 1917) Walton, 1949 (Trematoda: Diplostomatidae). J Parasitol 54:324–332CrossRefPubMedGoogle Scholar
  19. Johnson AD (1979) Morphology and Life History of Alaria mustelae Bosma 1931 (Trematoda: Diplostomatidae) from Minnesota Mustelids. J Parasitol 65:154–160CrossRefPubMedGoogle Scholar
  20. Klein SL (2000) Hormones and mating system affect sex and species differences in immune function among vertebrates. Behav Process 51:149–166CrossRefGoogle Scholar
  21. Klion AD, Nutman TB (2004) The role of eosinophils in host defense against helminth parasites. J Allergy Clin Immunol 113:30–37CrossRefPubMedGoogle Scholar
  22. La Rue GR (1917) Two new larval trematodes from Thamnophis marciana and Thamnophis eques. Occas Pap Mus Zool Univ Mich 35:1–14Google Scholar
  23. Lafferty KD (1999) The evolution of trophic transmission. Parasitol Today 15:111–115CrossRefPubMedGoogle Scholar
  24. Locke SA, McLaughlin JD, Lapierre AR, Johnson PTJ, Minchella DJ (2011) Linking larvae and adults of Apharyngostrigea cornu, Hysteromorpha triloba, and Alaria mustelae (Diplostomoidea: Digenea) using molecular data. J Parasitol 97:846–851. doi:10.1645/GE-2775.1 CrossRefPubMedGoogle Scholar
  25. Matuschka F-R, Bannert B (1987) Cannibalism and autotomy as predator–prey relationship for monoxenous sarcosporidia. Parasitol Res 74:88–93CrossRefPubMedGoogle Scholar
  26. McClelland EE, Smith JM (2011) Gender specific differences in the immune response to infection. Arch Immunol Ther Exp 59:203–213. doi:10.1007/s00005-011-0124-3 CrossRefGoogle Scholar
  27. Möhl K, Große K, Hamedy A, Wüste T, Kabelitz P, Lücker E (2009) Biology of Alaria spp. and human exposition risk to Alaria mesocercariae—a review. Parasitol Res 105:1–15. doi:10.1007/s00436-009-1444-7 CrossRefPubMedGoogle Scholar
  28. Moszczynska A, Locke SA, McLaughlin JD, Marcogliese DJ, Crease TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase i gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Mol Ecol Resour 9 (Suppl. 1): 75–82. doi:10.1111/j.1755-0998.2009.02634.xGoogle Scholar
  29. Odlaug TO (1940) Morphology and life history of the trematode, Alaria intermedia. Trans Am Microsc Soc 59:490–510. doi:10.2307/3222994 CrossRefGoogle Scholar
  30. Olivier L, Odlaug TO (1938) Mesocercaria intermedia n. sp. (Trematoda: Strigeata) with a note on its further development. J Parasitol 24:369–374CrossRefGoogle Scholar
  31. Pearson JC (1956) Studies on the life cycles and morphology of the larval stages of Alaria arisaemoides Augustine and Uribe, 1927 and Alaria canis LaRue and Fallis, 1936 (Trematoda: Diplostomidae). Can J Zool 34:295–387CrossRefGoogle Scholar
  32. Perry-Richardson JJ, Schofield CW, Ford NB (1990) Courtship of the garter snake, Thamnophis marcianus, with a description of a female behavior for coitus interruption. J Herpetol 24:76–78. doi:10.2307/1564292 CrossRefGoogle Scholar
  33. Pisani GR (1976) Comments on the courtship and mating mechanics of Thamnophis (Reptilia, Serpentes, Colubridae). J Herpetol 10:139–142. doi:10.2307/1562795 CrossRefGoogle Scholar
  34. Placyk JS, Burghardt GM (2005) Geographic variation in the frequency of scarring and tail stubs in eastern gartersnakes (Thamnophis s. sirtalis) from Michigan, USA. Amphibia-Reptilia 26:353–358. doi:10.1163/156853805774408568 CrossRefGoogle Scholar
  35. Portier J, Vallée I, Lacour SA, Martin-Schaller R, Ferté H, Durand B (2014) Increasing circulation of Alaria alata mesocercaria in wild boar populations of the Rhine Valley, France, 2007–2011. Vet Parasitol 199:153–159. doi:10.1016/j.vetpar.2013.09.029 CrossRefPubMedGoogle Scholar
  36. Poulin R (1996) Sexual inequalities in helminth infections: a cost of being male? Am Nat 147:287–295CrossRefGoogle Scholar
  37. Pulis EE, Tkach VV, Newman RA (2011) Helminth parasites of the wood frog, Lithobates sylvaticus, in prairie pothole wetlands of the northern Great Plains. Wetlands 31:675–685CrossRefGoogle Scholar
  38. Rau ME, Gordon DM (1978) Overwintering of helminths in the garter snake (Thamnophis sirtalis sirtalis). Can J Zool 56:1765–1767CrossRefGoogle Scholar
  39. Riehn K, Hamedy A, Alter T, Lücker E (2011) Development of a PCR approach for differentiation of Alaria spp. mesocercariae. Parasitol Res 108:1327–1332CrossRefPubMedGoogle Scholar
  40. Riffkin M, Seow HF, Jackson D, Brown L, Wood P (1996) Defence against the immune barrage: helminth survival strategies. Immunol Cell Biol 74:564–574CrossRefPubMedGoogle Scholar
  41. Sharpilo VP, Tkach VV (1989) Transmammary transmission of Alaria alata mesocercariae (Trematoda, Alariidae) from lactating females of paratenic hosts to offspring. Vestn Zool 5:81–83Google Scholar
  42. Shine R, Olsson MM, Moore IT, LeMaster MP, Mason RT (1999) Why do male snakes have longer tails than females? Proc R Soc Lond B Biol Sci 266:2147–2151CrossRefGoogle Scholar
  43. Shine R, Langkilde T, Wall M, Mason RT (2006) Temporal dynamics of emergence and dispersal of garter snakes from a communal den in Manitoba. Wildl Res 33:103–111CrossRefGoogle Scholar
  44. Shoop WL (1988) Trematode transmission patterns. J Parasitol 74:46–59CrossRefPubMedGoogle Scholar
  45. Shoop WL, Corkum KC (1981) Epidemiology of Alaria marcianae mesocercariae in Louisiana. J Parasitol 67:928–931. doi:10.2307/3280722 CrossRefPubMedGoogle Scholar
  46. Shoop WL, Corkum KC (1984) Pathway of mesocercariae of Alaria marcianae (Trematoda) through the mammary glands of lactating mice. J Parasitol 70:333–336. doi:10.2307/3281560 CrossRefPubMedGoogle Scholar
  47. Sparkman AM, Palacios MG (2009) A test of life-history theories of immune defence in two ecotypes of the garter snake, Thamnophis elegans. J Anim Ecol 78:1242–1248. doi:10.1111/j.1365-2656.2009.01587.x CrossRefPubMedGoogle Scholar
  48. Tăbăran F, Sándor AD, Marinov M, Cătoi C, Mihalca AD (2013) Alaria alata infection in European mink. Emerg Infect Dis 19:1547–1549. doi:10.3201/eid1909.130081 PubMedCentralCrossRefPubMedGoogle Scholar
  49. Theodoropoulos G, Hicks SJ, Corfield AP, Miller BG, Carrington SD (2001) The role of mucins in host–parasite interactions: part II–helminth parasites. Trends Parasitol 17:130–135CrossRefPubMedGoogle Scholar
  50. Tkach VV, Pawlowski J (1999) A new method of DNA extraction from the ethanol-fixed parasitic worms. Acta Parasitol 44:147–148Google Scholar
  51. Turner HF (1958) The life history of Fibricola cratera (Barker and Noll, 1915) DuBois, 1932 (Trematoda: Diplostomatidae). Iowa State University. Retrospective Theses and Dissertations. Paper 1624. http://lib.dr.iastate.edu/rtd/1624
  52. Wasiluk A (2013) Alaria alata infection-threatening yet rarely detected trematodiasis. Diagn Lab 49:33–37Google Scholar
  53. Willis L, Threlkeld ST, Carpenter CC (1982) Tail loss patterns in Thamnophis (Reptilia: Colubridae) and the probable fate of injured individuals. Copeia 1982:98. doi:10.2307/1444273 CrossRefGoogle Scholar
  54. Zuk M (2009) The sicker sex. PLoS Pathog 5, e1000267. doi:10.1371/journal.ppat.1000267 PubMedCentralCrossRefPubMedGoogle Scholar
  55. Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1024CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Integrative BiologyOregon State UniversityCorvallisUSA
  2. 2.Department of Biomedical SciencesOregon State UniversityCorvallisUSA
  3. 3.Department of BiologyUniversity of North DakotaGrand ForksUSA
  4. 4.Department of MicrobiologyOregon State UniversityCorvallisUSA

Personalised recommendations