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Social environment and weather during early life influence gastro-intestinal parasite loads in a group-living mammal

  • Behavioral ecology - Original research
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Abstract

Conditions experienced during early life have been frequently shown to exert long-term consequences on an animal’s fitness. In mammals and birds, the time around and shortly after weaning is one of the crucial periods early in life. However, little is known about how social and abiotic environmental conditions experienced around this time affect fitness-related traits such as endoparasite loads. We studied consequences of social interactions and rainy weather conditions around and after weaning on gastro-intestinal nematode loads in juvenile European rabbits Oryctolagus cuniculus. Infestations with the gastric nematode Graphidium strigosum and with the intestinal nematode Passalurus ambiguus were higher in animals experiencing more rain during early life. This might have been due to the higher persistence of nematodes’ infective stages outside the host body together with the animals’ lower energy allocation for immune defence under more humid and thus energetically challenging conditions. In contrast, infestations with P. ambiguus were lower in animals with more positive social interactions with mother and litter siblings. We propose that social support provided by familiar group members buffered negative stress effects on immune function, lowering endoparasite infestations. This is supported by the negative correlation between positive social behaviour and serum corticosterone concentrations, indicating lower stress in juveniles which integrated more successfully into the social network of their group. In conclusion, the findings offer a pathway showing how differences in the abiotic environment and social life conditions experienced early in life could translate into long-term fitness consequences via the effects on endoparasite loads.

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References

  • Bates D, Maechler M, Bolker B (2013) lme4: Linear mixed-effects models using S4 classes. R package version 0.999999-2, http://CRAN.R-project.org/package=lme4

  • Boag B, Lello J, Fenton A, Tompkins DM, Hudson PJ (2001) Patterns of parasite aggregation in the wild European rabbit Oryctolagus cuiniculus. Int J Parasitol 31:1421–1428

    Article  PubMed  CAS  Google Scholar 

  • Browne WJ, Subramanian SV, Jones K, Goldstein H (2005) Variance partitioning in multilevel logistic models that exhibit overdispersion. J R Stat Soc: Ser 168:599–613

    Article  Google Scholar 

  • Cohen S, Syme SL (1985) Social support and health. Academic Press, San Diego, USA

    Google Scholar 

  • Cowan DP (1987) Aspects of the social organization of the European wild rabbit (Oryctolagus cuniculus). Ethology 75:197–210

    Article  Google Scholar 

  • DeVries AC, Glasper ER, Detillion CE (2003) Social modulation of stress responses. Physiol Behav 79:399–407

    Article  PubMed  CAS  Google Scholar 

  • Dobson AP, Hudson PJ, Lyles AM (1992) Macroparasites: worms and others. In: Crawley MJ (ed) Natural enemies: the population biology of predators. Parasites and diseases. Blackwell, Oxford, pp 248–329

    Google Scholar 

  • Donald AD, Dineen JK, Symons LEA (1982) Biology and control of endoparasites. Academic Press, Sydney, Australia

    Google Scholar 

  • Dunsmore JD, Dudzinski ML (1968) Relationship of numbers of nematode parasites in wild rabbits, Oryctolagus cuniculus (L.) to host, sex, age and season. J Parasitol 54:462–474

    Article  Google Scholar 

  • Faulborn KW, Fenske M, Pitze lL, König A (1979) Effects of an intravenous injection of tetracosactid on plasma corticosteroid and testosterone levels in unstressed male rabbits. Acta Endocrinol 91:511–518

    PubMed  CAS  Google Scholar 

  • Fitze PS, Clobert J, Richner H (2004) Long-term life-history consequences of ectoparasite-modulated growth and development. Ecology 85:2018–2026

    Article  Google Scholar 

  • Foster LB, Dunn RT (1974) Single-antibody technique for radioimmunoassay of cortisol in unextracted serum or plasma. Clin Chem 20:365–368

    PubMed  CAS  Google Scholar 

  • Gause WC, Urban JF, Stadecker MJ (2003) The immune response to parasitic helminths: insights from murine models. Trends Immunol 24:227–269

    Article  Google Scholar 

  • Hakkarainen H, Huhta E, Koskela E, Mappes T, Soveri T, Suorsa P (2007) Eimeria-parasites are associated with a lowered mother’s and offspring’s body condition in island and mainland populations of the bank vole. Parasitology 134:23–31

    Article  PubMed  CAS  Google Scholar 

  • Helle H, Koskela E, Mappes T (2012) Life in varying environments: experimental evidence for delayed effects of juvenile environment on adult life history. J Anim Ecol 81:573–582

    Article  PubMed  Google Scholar 

  • Hendrichs H (1978) The social organisation of mammal populations. Säugetierkd Mitt 26:81–116

    Google Scholar 

  • Hennessy MB (1997) Hypothalamic-pituitary-adrenal responses to brief social separation. Neurosci Biobehav Rev 21:11–29

    Article  PubMed  CAS  Google Scholar 

  • Hennessy MB, Kaiser S, Sachser N (2009) Social buffering of the stress response: diversity, mechanisms, and functions. Front Neuroendocrinol 30:470–482

    Article  PubMed  CAS  Google Scholar 

  • Henry JP, Stephens PM (1977) Stress, health and the social environment: a sociobiological approach to medicine. Springer, Berlin, Germany

    Book  Google Scholar 

  • Hernandez AD, Poole A, Cattadori IM (2013) Climate changes influence free-living stages of soil-transmitted parasites of European rabbits. Glob Change Biol 19:1028–1042

    Article  Google Scholar 

  • Hillegrass MA, Waterman JM, Roth JD (2010) Parasite removal increases reproductive success in a social African ground squirrel. Behav Ecol 21:696–700

    Article  Google Scholar 

  • Hudson PJ, Newborn D, Dobson AP (1992) Regulation and stability of a free-living host-parasite system Trichostrongylus-Tenuis in red grouse in monitoring and parasite reduction experiments. J Anim Ecol 61:477–486

    Article  Google Scholar 

  • Hudson R, Bilkó Á, Altbäcker V (1996) Nursing, weaning and the development of independent feeding in the rabbit (Oryctolagus cuniculus). Zeitschr Säugetierkd Mammal Biol 61:39–48

    Google Scholar 

  • Irvine RJ (2006) Parasites and the dynamics of wild mammal populations. Anim Sci 82:775–781

    Article  Google Scholar 

  • Kaiser S, Kirtzeck M, Hornschuh G, Sachser N (2003) Sex-specific difference in social support—a study in female guinea pigs. Physiol Behav 79:297–303

    Article  PubMed  CAS  Google Scholar 

  • Kikusui T, Winslow JT, Mori Y (2006) Social buffering: relief from stress and anxiety. Philos Trans R Soc Lond B Biol Sci 361:2215–2228

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Klein SL (2000) The effects of hormones on sex differences in infection: from genes to behavior. Neurosci Biobehav Rev 24:627–638

    Article  PubMed  CAS  Google Scholar 

  • Kötsche W, Gottschalk C (1990) Krankheiten der Kaninchen und Hasen. Fischer, Jena, Germany

    Google Scholar 

  • Kreuder C, et al. (2003) Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998-2001. J Wildl Dis 39:495–509

    Article  PubMed  CAS  Google Scholar 

  • Künkele J, von Holst D (1996) Natal dispersal in the European wild rabbit. Anim Behav 51:1047–1059

    Article  Google Scholar 

  • Lello J, Boag B, Fenton A, Stevenson IR, Hudson PJ (2004) Competition and mutualism among the gut helminths of a mammalian host. Nature 482:840–844

    Article  Google Scholar 

  • Lello J, Boag B, Hudson PJ (2005) The effect of single and concomitant pathogen infections on condition and fecundity of the wild rabbit (Oryctolagus cuniculus). Int J Parasitol 35:1509–1515

    Article  PubMed  CAS  Google Scholar 

  • Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348

    Article  PubMed  Google Scholar 

  • Lloyd S (1996) Environmental influences on host immunity. In: Grenfell BT, Dobson AP (eds) Ecology of infectious diseases in natural populations. Cambridge University Press, Cambridge, pp 327–361

    Google Scholar 

  • Martiniaková M, Omelka R, Grosskopf B, Sirotkin AV, Chrenek P (2008) Sex-related variation in compact bone microstructure of the femoral diaphysis in juvenile rabbits. Acta Vet Scand 50:15

    Article  PubMed  PubMed Central  Google Scholar 

  • Massoni J, Cassone J, Durette-Desset MC, Audebert F (2011) Development of Graphidium strigosum (Nematoda, Haemonchidae) in its natural host, the rabbit (Oryctolagus cuniculus) and comparison with several Haemonchidae parasites of ruminants. Parasitol Res 109:25–36

    Article  PubMed  Google Scholar 

  • Møller AP, Allander K, Duvfa R (1990) Fitness effects of parasites on passerine birds: a review. In: Blondel J, Gosler A, Lebreton JD, McCleery R (eds) Population biology of passerine birds. Springer, Berlin, pp 269–280

    Chapter  Google Scholar 

  • Mykytowycz R (1956) A survey of endoparasites of the wild rabbit, Oryctolagus cuniculus (L.) in Australia. Wildl Res 1:19–25

    Article  Google Scholar 

  • Nickel EA, Haupt W (1986) Experimental studies on the course and consequences of infection with Graphidium strigosum (Nematoda, Trichostrongylidae) in Oryctolagus cuniculus (domestic rabbit). Angew Parasitol 27:215–219

    PubMed  CAS  Google Scholar 

  • O’Connor LJ, Walkden-Brown SW, Kahn LP (2006) Ecology of the free-living stages of major trichostrongylid parasites of sheep. Vet Parasitol 142:1–15

    Article  PubMed  Google Scholar 

  • Oppelt C, Starkloff A, Rausch P, von Holst D, Rödel HG (2010) Major histocompatibility complex variation and age-specific endoparasite load in subadult European rabbits. Mol Ecol 19:4155–4167

    Article  PubMed  CAS  Google Scholar 

  • Owen D (1972) Common parasites of laboratory rodents and lagomorphs. Stationery Office Books, UK

    Google Scholar 

  • Palomares F (2001) Comparison of 3 methods to estimate rabbit abundance in a Mediterranean environment. Wildl Soc Bull 29:578–585

    Google Scholar 

  • Pathak AK, Pelensky C, Boag B, Cattadori IM (2012) Immuno-epidemiology of chronic bacterial and helminth co-infections: observations from the field and evidence from the laboratory. Int J Parasitol 42:647–655

    Article  PubMed  Google Scholar 

  • Petrovan SO, Barrio IC, Ward AI, Wheeler PM (2011) Farming for pests? Local and landscape-scale effects of grassland management on rabbit densities. Eur J Wildl Res 57:27–34

    Article  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, www.R-project.org, Vienna, Austria

  • Richardson B, Wood DH (1982) Experimental ecological studies on a subalpine rabbit population. I. Mortality factors acting on emergent kittens. Aust Wildl Res 9:443–450

    Article  Google Scholar 

  • Rödel HG, Dekker JJA (2012) Influence of weather factors on population dynamics of two lagomorph species based on hunting bag records. Eur J Wildl Res 58:923–932

    Article  Google Scholar 

  • Rödel HG, Bora A, Kaetzke P, Khaschei M, Hutzelmeyer H, von Holst D (2004a) Over-winter survival in subadult European rabbits: weather effects, density dependence, and the impact of individual characteristics. Oecologia 140:566–576

    Article  PubMed  Google Scholar 

  • Rödel HG, Bora A, Kaiser J, Kaetzke P, Khaschei M, von Holst D (2004b) Density-dependent reproduction in the European rabbit: a consequence of individual response and age-dependent reproductive performance. Oikos 104:529–539

    Article  Google Scholar 

  • Rödel HG, Monclús R, von Holst D (2006) Behavioral styles in European rabbits: social interactions and responses to experimental stressors. Physiol Behav 89:180–188

    Article  PubMed  Google Scholar 

  • Rödel HG, Starkloff A, Bruchner B, von Holst D (2008) Social environment and reproduction in female European rabbits (Oryctolagus cuniculus): benefits of the presence of litter sisters. J Comp Psychol 122:73–83

    Article  PubMed  Google Scholar 

  • Rödel HG, von Holst D, Kraus C (2009) Family legacies: short- and long-term fitness consequences of early-life conditions in female European rabbits. J Anim Ecol 78:789–797

    Article  PubMed  Google Scholar 

  • Rodriguez M, Cohen S (1998) Social support. In: Friedman H (ed) Encyclopedia of mental health. Academic Press, New York, pp 535–644

    Google Scholar 

  • Sapolsky RM (1992) Neuroendocrinology of the stress-response. In: Becker JB, Breedlove SM, Crews D (eds) Behavioral endocrinology. MIT Press, Cambridge, pp 287–324

    Google Scholar 

  • Scheiber IBR, Weiß BM, Frigerio D, Kotrschal K (2005) Active and passive social support in families of greylag geese (Anser anser). Behaviour 142:1535–1557

    Article  PubMed  PubMed Central  Google Scholar 

  • Schwarzer R, Knoll N (2007) Functional roles of social support within the stress and coping process: a theoretical and empirical overview. Int J Psychol 42:243–252

    Article  Google Scholar 

  • Seltmann MW, Ruf T, Rödel HG (2009) Effects of body mass and huddling on resting metabolic rates of post-weaned European rabbits under different simulated weather conditions. Funct Ecol 23:1070–1080

    Article  Google Scholar 

  • Sibly RM, Collett D, Promislow DEL, Peacock DJ, Harvey PH (2009) Mortality rates of mammals. J Zool 243:1–12

    Article  Google Scholar 

  • Stromberg BE (1997) Environmental factors influencing transmission. Vet Parasitol 72:247–264

    Article  PubMed  CAS  Google Scholar 

  • Tompkins DM, Begon M (1999) Parasites can regulate wildlife populations. Parasitol Today 15:311–313

    Article  PubMed  CAS  Google Scholar 

  • Vandegrift KJ, Raffel TR, Hudson PJ (2009) Parasites prevent summer breeding in white-footed mice, Peromyscus leucopus. Ecology 89:2251–2258

    Article  Google Scholar 

  • Visser HG (1998) Development of temperature regulation. In: Starck JM, Rickleys RE (eds) Avian growth and development. Oxford University Press, Oxford, pp 117–156

    Google Scholar 

  • von Holst D (1998) The concept of stress and its relevance for animal behavior. Adv Study Behav 27:1–131

    Article  Google Scholar 

  • von Holst D (2001) Social stress in wild mammals in their natural habitat. In: Broom DM (ed) Coping with challenge: welfare in animals including humans. Dahlem University Press, Berlin, pp 317–335

    Google Scholar 

  • von Holst D, Hutzelmeyer H, Kaetzke P, Khaschei M, Rödel HG, Schrutka H (2002) Social rank, fecundity and lifetime reproductive success in wild European rabbits (Oryctolagus cuniculus). Behav Ecol Sociobiol 51:245–254

    Article  Google Scholar 

  • Wallage Drees JM (1989) A field study on seasonal changes in the circadian activity of rabbits. Zeitsch Säugetierkd Mammal Biol 54:22–30

    Google Scholar 

  • Wascher CAF, Bauer AC, Holtmann AR, Kotrschal K (2012) Environmental and social factors affecting the excretion of intestinal parasite eggs in graylag geese. Behav Ecol 23:1276–1283

    Article  Google Scholar 

  • Wilson K et al (2001) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeck JAP, Dobson AP (eds) The ecology of wildlife diseases. Oxford University Press, Oxford, pp 6–44

    Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Article  Google Scholar 

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Acknowledgments

We are grateful to Dietrich von Holst for his support and for helpful discussions. We thank Alexandra Deibl, Christina Herold, Christina Landmann, Nina Lang, Lilian Shehata, Franziska Weber, Martin Seltmann, Simon Anthofer and Florian Kirchmann for their help with the data collection. We also thank Andrea Berger, Antje Halwas and Inge Zerenner-Fritzsche for excellent technical assistance. We are grateful to Theodora Steineck for providing valuable advice on methods for the quantification of endoparasites, and to Johannes Luers for kindly providing data sets of the meteorological station of the University of Bayreuth. This research was financially supported by the German Research Foundation DFG (RO2431/2-1).

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  1. Laboratoire d’Ethologie Expérimentale et Comparée E.A. 4443 (LEEC), Université Paris 13, Sorbonne Paris Cité, 93430, Villetaneuse, France

    Heiko G. Rödel

  2. Department of Animal Physiology, University of Bayreuth, 95440, Bayreuth, Germany

    Anett Starkloff

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  1. Heiko G. Rödel
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  2. Anett Starkloff
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Correspondence to Heiko G. Rödel.

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Communicated by Herwig Leirs.

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Rödel, H.G., Starkloff, A. Social environment and weather during early life influence gastro-intestinal parasite loads in a group-living mammal. Oecologia 176, 389–398 (2014). https://doi.org/10.1007/s00442-014-3017-4

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