Faecal egg counts from field experiment reveal density dependence in helminth fecundity: Strongyloides robustus infecting grey squirrels (Sciurus carolinensis)
- 229 Downloads
Investigation of endo-macroparasite infections in living animals relies mostly on indirect methods aimed to detect parasite eggs in hosts’ faeces. However, faecal flotation does not provide quantitative information on parasite loads, whereas faecal egg count (FEC) techniques may not give reliable estimates of parasite intensity, since egg production may be affected by density-dependent effects on helminth fecundity. We addressed this issue using Eastern grey squirrels (Sciurus carolinensis) and their gastrointestinal nematode Strongyloides robustus to assess the performance of coprological techniques and to investigate factors affecting parasite fecundity. We compared results of gut examination, flotation and McMaster FECs in 65 culled grey squirrels. Sensitivity and specificity of flotation were 81.2 % (Confidence Interval, CI 54.3–95.9 %) and 85.7 % (CI 72.7–94.1 %), respectively, resulting in low positive predictive values when infection prevalence is low. Individual parasite fecundity (no. of eggs/adult female worm) was negatively affected by S. robustus intensity, leading to a non-linear relationship between parasite load and eggs/gram of faeces (EPG). As a consequence, whereas flotation may be a valid method to perform the first screening of infection status, FECs are not a reliable method to estimate S. robustus intensity, since diverse values of EPG may correspond to the same number of parasites. Neither the amount of analysed faeces nor the season had any effect on EPG, indicating that the observed reduction in helminth fecundity is likely caused exclusively by density-dependent processes such as competition among worms or host immune response.
KeywordsHelminth fecundity Faecal egg count Faecal flotation Parasite intensity
We would like to thank Cuneo Province and private estates owners for allowing field collection. Many thanks also to Leila Luise and Sara Vedovato for their assistance with laboratory analysis.
Sampling of grey squirrels was carried out with authorizations by Cuneo Province (Permit No. 473, 12 May 2011) and the Italian Institute for Environmental Protection and Research (ISPRA). All sampling protocols were chosen to minimise animal stress and suffering. Squirrels were euthanised immediately after capture following EC and AVMA guidelines (Close et al. 1996, 1997; Leary et al. 2013).
- Christensen CM, Barnes EH, Nansen P, Roepstorff A, Slotved H-C (1995) Experimental Oesophagostomum dentatum infection in the pig: worm populations resulting from single infections with three doses of larvae. Int J Parasitol 25:1491–1498. doi: 10.1016/0020-7519(95)00085-2 PubMedCrossRefGoogle Scholar
- Davidson WR (1976) Endoparasites of selected populations of gray squirrels (Sciurus carolinensis) in the southeastern United States. Proc Helminthol Soc Wash 43:211–216Google Scholar
- Elkins DB, Sithithaworn P, Haswell-Elkins M, Kaewkes S, Awacharagan P, Wongratanacheewin S (1991) Opisthorchis viverrini: relationships between egg counts, worms recovered and antibody levels within an endemic community in Northeast Thailand. Parasitology 102:283–288. doi: 10.1017/S0031182000062600 PubMedCrossRefGoogle Scholar
- Leary SL, Underwood W, Anthony R, Cartner S, Corey D, Grandin T, Greenacre C, Gwaltney-Brant S, McCrackin M, Meyer R, Miller D, Shearer J, Yanong R (2013) AVMA guidelines for the euthanasia of animals. https://www.avma.org/KB/Policies/Documents/euthanasia.pdf
- MAFF (1977) Manual of veterinary parasitological laboratory techniques. Her Majesty’s Stationary Office, LondonGoogle Scholar
- Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Roepstorff A, Bjørn H, Nansen P, Barnes EH, Christensen CM (1996) Experimental Oesophagostomum dentatum infections in the pig: worm populations resulting from trickle infections with three dose levels of larvae. Int J Parasitol 26:399–408. doi: 10.1016/0020-7519(96)00006-9 PubMedCrossRefGoogle Scholar
- Romeo C, Pisanu B, Ferrari N, Basset F, Tillon L, Wauters LA, Martinoli A, Saino N, Chapuis J-L (2013) Macroparasite community of the Eurasian red squirrel (Sciurus vulgaris): poor species richness and diversity. Parasitol Res 112:3527–3536. doi: 10.1007/s00436-013-3535-8 PubMedCrossRefGoogle Scholar
- Romeo C, Wauters LA, Ferrari N, Lanfranchi P, Martinoli A, Pisanu B, Preatoni D, Saino N (2014) Macroparasite fauna of alien grey squirrels (Sciurus carolinensis): composition, variability and implications for native species. PLoS One 9:e88002. doi: 10.1371/journal.pone.0088002 PubMedCentralPubMedCrossRefGoogle Scholar
- Thrusfield M (2013) Veterinary epidemiology. Wiley, OxfordGoogle Scholar
- Wilson K, Bjørnstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE, Read AF, Skorping A (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The ecology of wildlife diseases. Oxford University Press, Oxford, pp 6–44Google Scholar