Artigo Revisado por pares

The influence of parasites on faecal glucocorticoid metabolite levels in raccoons: an experimental assessment in a natural setting

2010; Wiley; Volume: 282; Issue: 2 Linguagem: Inglês

10.1111/j.1469-7998.2010.00717.x

ISSN

1469-7998

Autores

Ryan J. Monello, Joshua J. Millspaugh, RAMI J. WOODS, Matthew E. Gompper,

Tópico(s)

Dermatological diseases and infestations

Resumo

Journal of ZoologyVolume 282, Issue 2 p. 100-108 The influence of parasites on faecal glucocorticoid metabolite levels in raccoons: an experimental assessment in a natural setting R. J. Monello, R. J. Monello Department of Fisheries and Wildlife Sciences, University of Missouri, Columbia, MO, USASearch for more papers by this authorJ. J. Millspaugh, J. J. Millspaugh Department of Fisheries and Wildlife Sciences, University of Missouri, Columbia, MO, USASearch for more papers by this authorR. J. Woods, R. J. Woods Department of Fisheries and Wildlife Sciences, University of Missouri, Columbia, MO, USASearch for more papers by this authorM. E. Gompper, M. E. Gompper Department of Fisheries and Wildlife Sciences, University of Missouri, Columbia, MO, USASearch for more papers by this author R. J. Monello, R. J. Monello Department of Fisheries and Wildlife Sciences, University of Missouri, Columbia, MO, USASearch for more papers by this authorJ. J. Millspaugh, J. J. Millspaugh Department of Fisheries and Wildlife Sciences, University of Missouri, Columbia, MO, USASearch for more papers by this authorR. J. Woods, R. J. Woods Department of Fisheries and Wildlife Sciences, University of Missouri, Columbia, MO, USASearch for more papers by this authorM. E. Gompper, M. E. Gompper Department of Fisheries and Wildlife Sciences, University of Missouri, Columbia, MO, USASearch for more papers by this author First published: 08 June 2010 https://doi.org/10.1111/j.1469-7998.2010.00717.xCitations: 18 Correspondence Ryan J. Monello, National Park Service, Biological Resource Management Division, 1201 Oak Ridge Dr. Suite 200, Fort Collins, CO 80525, USA.Email: [email protected] Editor: Virginia Hayssen Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract Parasites and glucocorticoid hormones interact and affect a variety of processes within vertebrates, such as immune system function and reproduction. The nature of the relationship between parasite infection and glucocorticoid levels has received relatively little attention among free-ranging animals and results of experimental research in natural settings are equivocal. We conducted a parasite-reduction experiment to determine if reductions in nematodes or ectoparasites affect levels of faecal glucocorticoid metabolites (FGM) in adult raccoons. Individual raccoons were randomly assigned to a parasite-reduction treatment (ivermectin injection and Frontline Plus® application) or control group (saline injection) and recaptured within 30 days to assess treatment-related differences in parasitism and FGM levels. Treated animals had reduced nematode and ectoparasite communities. The most common and energetically expensive ectoparasite of raccoons in the region, the American dog tick, was reduced five-fold from an average of 19.3 ± 2.5 (se) to 3.4 ± 8 ticks per animal, and was unable to feed to repletion on treated animals. The prevalence of four out of seven nematode species was significantly lower in treated versus control animals; prevalence of these four nematodes ranged from 0 to 19% among treated animals and from 21 to 55% among control animals. The parasite infracommunity was also significantly reduced; the average number of nematode species per individual was 2.5 ± 0.3 in treated animals and 1.1 ± 0.2 in control animals, and the average number of ectoparasite species per individual was 2.3 ± 0.1 on treated animals and 1.1 ± 0.12 on control animals. No differences in FGM values were observed within individuals or between treatment and control groups following parasite-reduction treatments, indicating that the observed reductions in nematodes and ectoparasites had no effect on FGM levels of raccoons across the time frame of this study. References Allan, S.A. (2001). Ticks. In Parasitic diseases of wild mammals: 72–106. W.M. Samuel, M.J. Pybus & A.A. Kocan (Eds). Ames: Iowa State Press. Arriero, E., Moreno, J., Merino, S. & Martßnez, J. (2008). Habitat effects on physiological stress response in nestling blue tits are mediated through parasitism. Physiol. Biochem. Zool. 81, 195–203. Bauer, C. & Gey, A. (1995). Efficacy of six anthelmintics against luminal stages of Baylisascaris procyonis in naturally infected raccoons (Procyon lotor). Vet. Parasitol. 60, 155–159. Belden, L.K. & Kiesecker, J.M. (2005). Glucocorticosteroid hormone treatment of larval treefrogs increases infection by Alaria sp. trematode cercariae. J. Parasitol. 91, 686–688. Bloomer, S.E., Willebrand, M.T., Keith, I.M. & Keith, L.B. (1995). Impact of helminth parasitism on a snowshoe hare population in central Wisconsin: a field experiment. Can. J. Zool. 73, 1891–1898. Bourgeon, S. & Raclot, T. (2006). Corticosterone selectively decreases humoral immunity in female eiders during incubation. J. Exp. Biol. 209, 4957–4965. Bowman, D.D. (1999). Georgis' parasitology for veterinarians. Philadelphia: W.B. Saunders Company. Chapman, B.R. & George, J.E. 1991. The effects of ectoparasites on cliff swallow growth and survival. In Bird-parasite interactions: ecology, evolution, and behaviour: 69–92. J.E. Loye & M. Zuk (Eds). New York,: Oxford University Press. Craig, L.E, Norris, D.E., Sanders, M.L, Glass, G.E. & Schwartz, B.S. (1996). Acquired resistance and antibody response of raccoons (Procyon lotor) to sequential feedings of Ixodes scapularis (Acari: Ixodidae). Vet. Parasitol. 63, 291–301. Creel, S. (2005). Dominance, aggression, and glucocorticoid levels in social carnivores. J. Mammal. 86, 255–264. Evans, R.H. (2002). Raccoons and relatives (Carnivora, Procyonidae). In Zoological restraint and anesthesia. D. Heard (Ed.). Ithaca: International Veterinary Information Service. Available at http://www.ivis.org/special_books/Heard/evans/chapter_frm.asp?LA=1. Festa-Bianchet, M. (1991). Numbers of lungworm larvae in feces of bighorn sheep: yearly changes, influence of host sex, and effects on host survival. Can. J. Zool. 69, 547–554. Fowles, J.R., Fairbrother, A., Fix, M., Schiller, S. & Kerkvliet, N.I. (1993). Glucocorticoid effects on natural and humoral immunity in mallards. Dev. Comp. Immunol. 17, 165–177. Goldstein, E.J., Millspaugh, J.J., Washburn, B.E., Brundige, G.C. & Raedeke, K.J. (2005). Relationships among fecal lungworm loads, fecal glucocorticoid metabolites, and lamb recruitment in free-ranging Rocky Mountain bighorn sheep. J. Wildl. Dis. 41, 416–425. Grau, G.A., Sanderson, G.C. & Rogers, J.P. (1970). Age determination in raccoons. J. Wildl. Mgmt. 34, 364–372. Gregson, J.D. (1973). Tick paralysis: an appraisal of natural and experimental data. Monograph No. 9. Ottawa: Canada Department of Agriculture. Grotjan, H.E. & Keel, B.A. (1996). Data interpretation and quality control. In Immunoassays: 51–93. E.P. Diamandis & T.K. Christopoulos (Eds). New York: Academic Press. Handa, R.J., Burgess, L.H., Kerr, J.E. & O'Keefe, J.A. (1994). Gonadal steroid hormone receptors and sex differences in the hypothalamo–pituitary–adrenal axis. Horm. Behav. 28, 464–476. Hanley, K.A. & Stamps, J.A. (2002). Does corticosterone mediate bidirectional interactions between social behaviour and blood parasites in the juvenile black iguana, Ctenosaura similis? Anim. Behav. 63, 311–322. Hill, R.E. Jr, Zimmerman, J.J., Greve, J.H. & Beran, G.W. (1991). Use of ivermectin against several nematodes in naturally infected raccoons (Procyon lotor). J. Zoo Wildl. Med. 22, 417–420. Huber, S., Palme, R. & Arnold, W. (2003). Effects of season, sex, and sample collection on concentrations of fecal cortisol metabolites in red deer (Cervus elaphus). Gen. Comp. Endocrinol. 130, 48–54. Jeffcoate, S.L. (1981). Efficiency and effectiveness in the endocrinology laboratory. San Diego: Academic Press. Keay, J.M., Jatinder Singh, B.S., Gaunt, M.C. & Kaur, T. (2006). Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: a literature review. J. Zoo Wildl. Med. 37, 234–244. Kenagy, G.J. & Place, N.J. (2000). Seasonal changes in plasma glucocorticoids of free-living female yellow-pine chipmunks: effects of reproduction and capture and handling. Gen. Comp. Endocrinol. 117, 189–199. Kitaysky, A.S., Kitaiskaia, E.V., Piatt, J.F. & Wingfield, J.C. (2003). Benefits and costs of increased levels of corticosterone in seabird chicks. Horm. Behav. 43, 140–149. Maier, S.F. & Watkins, L.R. (1999). Bidirectional communication between the brain and the immune system: implications for behaviour. Anim. Behav. 57, 741–751. Maizels, R.M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M.D. & Allen, J.E. (2004). Helminth parasites – masters of regulation. Immunol. Rev. 201, 89–116. Martin, L.B. (2009). Stress and immunity in wild vertebrates: timing is everything. Gen. Comp. Endocrinol. 163, 70–76. Millspaugh, J.J. & Washburn, B.E. (2004). Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. Gen. Comp. Endocrinol. 138, 189–199. Millspaugh, J.J., Woods, R.J., Hunt, K.E., Raedeke, K.J., Brundige, G.C., Washburn, B.E. & Wasser, S.E. (2001). Fecal glucocorticoid assays and the physiological stress response in elk. Wildl. Soc. Bull. 29, 899–907. Monello, R.J. (2009). Experimentally assessing the influence of resource availability and social aggregation on the parasites of raccoons. Unpublished PhD dissertation, University of Missouri. Monello, R.J. & Gompper, M.E. (2007). Biotic and abiotic predictors of tick (Dermacentor variabilis) abundance and engorgement on free-ranging raccoons (Procyon lotor). Parasitology 134, 2053–2062. Monello, R.J. & Gompper, M.E. (2009). Relative importance of demographics, locale, and seasonality underlying louse and flea parasitism of raccoons (Procyon lotor). J. Parasitol. 95, 56–62. Monello, R.J. & Gompper, M.E. (2010). Differential effects of experimental increases in sociality on ectoparasites of free-ranging raccoons. J. Anim. Ecol. 79, 602–609. Muehlenbein, M.P. (2006). Intestinal parasite infections and fecal steroid levels in wild chimpanzees. Am. J. Phys. Anthropol. 130, 546–550. O'Fegan, P.O. (2000). Validation. In Immunoassays: 211–238. E.P. Diamandis & T.K. Christopoulos (Eds). New York: Academic Press. Palme, R., Fischer, P., Schilddorfer, H. & Ismail, M.N. (1996). Excretion of infused 14C-steroid hormones via faeces and urine in domestic livestock. Anim. Reprod. Sci. 43, 43–63. Pedersen, A.B. & Greives, T.J. (2008). The interaction of parasites and resources cause crashes in a wild mouse population. J. Anim. Ecol. 77, 370–377. Place, N.J. & Kenagy, G.J. (2000). Seasonal changes in plasma testosterone and glucocorticoids in free-living male yellow-pine chipmunks and the response to capture and handling. J. Comp. Physiol. B 170, 245–251. Raouf, S.A., Smith, L.C., Bromberger Brown, M., Wingfield, J.C. & Brown, C.R. (2006). Glucocorticoid hormone levels increase with group size and parasite load in cliff swallows. Anim. Behav. 71, 39–48. Reeder, D.M. & Kramer, K.M. (2005). Stress in free-ranging mammals: integrating physiology, ecology, and natural history. J. Mammal. 86, 225–235. Reeder, D.M., Kunz, T.H. & Widmaier, E.P. (2004). Baseline and stress-induced glucocorticoids during reproduction in the variable flying fox, Pteropus hypomelanus (Chiroptera: Pteropodidae). J. Exp. Zool. Part A 301, 682–690. Roberts, M.L., Buchanan, K.L., Hasselquist, D. & Evans, M.R. (2007). Effects of testosterone and corticosterone on immunocompetence in the zebra finch. Horm. Behav. 51, 126–134. Saino, N., Suffritti, C., Martinelli, R., Rubolini, D. & Moller, A.P. (2003). Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling barn swallows (Hirundo rustica). Behav. Ecol. 14, 318–325. Sapolsky, R.M. (1985). Stress-induced suppression of testicular function in the wild baboon: role of glucocorticoids. Endocrinology 116, 2273–2278. Sapolsky, R.M. (2005). The influence of social hierarchy on primate health. Science 308, 648–703. Schatz, S. & Palme, R. (2001). Measurement of faecal cortisol metabolites in cats and dogs: a non-invasive method for evaluating adrenocortical function. Vet. Res. Commun. 25, 271–287. Schwartz, C.W. & Schwartz, E.R. (2001). The wild mammals of Missouri. Columbia: University of Missouri Press. Taillon, J. & Côté, S.D. (2008). Are faecal hormone levels linked to winter progression, diet quality and social rank in young ungulates? An experiment with white-tailed deer (Odocoileus virginianus) fawns. Behav. Ecol. Sociobiol. 62, 1591–1600. Washburn, B.E., Millspaugh, J.J., Schulz, J.H., Jones, S.B. & Mong, T. (2003). Using fecal glucocorticoids for stress assessment in mourning doves. Condor 105, 696–706. Wasser, S.K., Hunt, K.E., Brown, J.L., Cooper, K., Crockett, C.M., Bechert, U., Millspaugh, J.J., Larson, S. & Monfort, S.L. (2000). A generalized fecal glucocorticoid assay for use in a diverse array of non-domestic mammalian and avian species. Gen. Comp. Endocrinol. 120, 260–275. Wingfield, J.C. & Farner, D.S. (1993). Endocrinology of reproduction in wild species. Avian Biol. 9, 163–327. Wingfield, J.C., O'Reilly, K.M. & Astheimer, L.B. (1995). Modulation of the adrenocortical responses to acute stress in Arctic birds: a possible ecological basis. Am. Zool. 35, 299–306. Wright, A.N. & Gompper, M.E. (2005). Altered parasite assemblages in raccoons in response to manipulated resource availability. Oecologia 144, 148–156. Young, K.M., Walker, S.L., Lanthier, C., Waddell, W.T., Monfort, S.L. & Brown, J.L. (2004). Noninvasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses. Gen. Comp. Endocrinol. 137, 148–165. Citing Literature Volume282, Issue2October 2010Pages 100-108 ReferencesRelatedInformation

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