Skip to main content
SpringerLink
Log in

Puumala hantavirus infection alters the odour attractiveness of its reservoir host

  • Behavioral ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The random-mixing assumptions of many parasite-transmission models are challenged if healthy individuals can alter their behaviour to reduce their risk of infection. Some pathogens reduce the attractiveness of their hosts’ excretions, for example, potentially altering contact rates and thus the predicted force of infection for pathogens transmissible by contact with excretions. For bank voles (Myodes glareolus), contact with contaminated urine is an important route of transmission for Puumala hantavirus (PUUV); however, it is not known whether PUUV infection changes the voles’ urinary odours or their attractiveness. Here, we use a Y-maze to test whether PUUV infection alters the attractiveness of male bank voles’ urine. We presented wild-caught PUUV-free male and female bank voles with PUUV-infected conspecific urine, uninfected urine and a water control, and measured the relative and absolute latency to first visit, number of visits, and total time bank voles spent investigating each treatment over 30 min. PUUV infection significantly altered the bank voles’ initial response to conspecific urine, with fewer visits and less time spent close to infected urine relative to uninfected urine, and less total time spent near the infected urine than the uninfected urine or control. These strong preferences weakened over the 30-min trial, however, partly due to a general decline in male activity, and there were no absolute differences between the treatments overall. This suggests that PUUV infection does change the attractiveness of bank vole urine to conspecifics, and we discuss the implications of these results for random-mixing assumptions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abolins SR, Pocock MJ, Hafalla JC, Riley EM, Viney ME (2011) Measures of immune function of wild mice, Mus musculus. Mol Ecol 20:881–892

    Article  CAS  PubMed  Google Scholar 

  • Aguilar TM, Maia R, Santos ESA, Macedo RH (2007) Parasite levels in blue-black grassquits correlate with male displays but not female mate preference. Behav Ecol 19:292–301

    Article  Google Scholar 

  • Apio A, Plath M, Wronski T (2005) Localised defecation sites: a tactic to avoid re-infection by gastro-intestinal tract parasites in bushbuck, Tragelaphus scriptus? J Ethol 24:85–90

    Article  Google Scholar 

  • Arakawa H, Cruz S, Deak T (2011) From models to mechanisms: odorant communication as a key determinant of social behavior in rodents during illness-associated states. Neurosci Biobehav 35:1916–1928

    Article  Google Scholar 

  • Begon M, Bennett M, Bowers RG, French NP, Hazel SM, Turner J (2002) A clarification of transmission terms in host-microparasite models: numbers, densities and areas. Epidemiol Infect 129:147–153

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Beltran-Bech S, Richard F-J (2014) Impact of infection on mate choice. Anim Behav 90:159–170

    Article  Google Scholar 

  • Bondrup-Nielson S, Karlsson F (1985) Movements and spatial patterns in populations of Clethrionomys species: a review. Ann Zool Fenn 22:385–392

    Google Scholar 

  • Boysen P, Eide DM, Storset AK (2011) Natural killer cells in free-living Mus musculus have a primed phenotype. Mol Ecol 20:5103–5110

    Article  CAS  PubMed  Google Scholar 

  • Carver S, Trueax J, Douglass R, Kuenzi A (2011) Delayed density-dependent prevalence of Sin Nombre virus infection in deer mice (Peromyscus maniculatus) in central and western Montana. J Wildl Dis 47:56–63

    Article  PubMed Central  PubMed  Google Scholar 

  • Childs JE, Glass GE, Korch GW, LeDuc JW (1989) Effects of hantaviral infection on survival, growth and fertility in wild rat (Rattus norvegicus) populations of Baltimore, Maryland. J Wildl Dis 25:469–476

    Article  CAS  PubMed  Google Scholar 

  • Christiansen E (1980) Urinary marking in wild bank voles, Clethrionomys glareolus, in relation to season and sexual status. Behav Neural Biol 28:123–127

    Article  Google Scholar 

  • Dass SAH, Vasudevan A, Dutta D, Soh LJT, Sapolsky RM, Vyas A (2011) Protozoan parasite Toxoplasma gondii manipulates mate choice in rats by enhancing attractiveness of males. PLoS One 6:e27229

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dobson AP, Hudson PJ (1995) Microparasites: observed patterns in wild animal populations. In: Grenfell BT, Dobson AP (eds) Ecology of infectious diseases in natural populations. Cambridge University Press, Cambridge, pp 52–89

    Chapter  Google Scholar 

  • Escutenaire S, Chalon P, De Jaegere F, Karelle-Bui L, Mees G, Brochier B, Rozenfeld F, Pastoret PP (2002) Behavioral, physiologic, and habitat influences on the dynamics of Puumala virus infection in bank voles (Clethrionomys glareolus). Emerging Infect Dis 8:930–936

    Article  PubMed Central  PubMed  Google Scholar 

  • Gavrilovskaya IN, Apekina NS, Bernshtein AD, Demina VT, Okulova NM, Myasnikov YA, Chumakov MP (1990) Pathogenesis of hemorrhagic fever with renal syndrome virus infection and mode of horizontal transmission of hantavirus in bank voles. Arch Virol 1:S57–S62

    Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds—a role for parasites. Science 218:384–387

    Article  CAS  PubMed  Google Scholar 

  • Hardestam J, Karlsson M, Falk KI, Olsson G, Klingstrom J, Lundkvist A (2008) Puumala hantavirus excretion kinetics in bank voles (Myodes glareolus). Emerging Infect Dis 14:1209–1215

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hart BL (1990) Behavioral adaptations to pathogens and parasites: five strategies. Neurosci Biobehav 14:273–294

    Article  CAS  Google Scholar 

  • Henderson D, Bird DM, Rau ME, Negro JJ (1995) Mate choice in captive American kestrels, Falco sparverius, parasitized by a nematode, Trichinella pseudospiralis. Ethology 101:112–120

    Article  Google Scholar 

  • Hoffmeyer I (1982) Responses of female bank voles (Clethrionomys glareolus) to dominant and subordinate conspecific males and to urine odors from dominant vs subordinate males. Behav Neural Biol 36:178–188

    Article  CAS  PubMed  Google Scholar 

  • Hughes NK, Korpimäki E, Banks PB (2010a) The predation risks of interspecific eavesdropping: weasel-vole interactions. Oikos 119:1210–1216

    Article  Google Scholar 

  • Hughes NK, Price CJ, Banks PB (2010b) Predator attraction to prey olfactory signals places conspecific receivers at risk. PLoS One 5:e13114

    Article  PubMed Central  PubMed  Google Scholar 

  • Hughes NK, Kelley JL, Banks PB (2012) Dangerous liaisons: the predation risks of receiving social signals. Ecol Lett 15:1326–1339

    Article  PubMed  Google Scholar 

  • Hurst JL (2009) Female recognition and assessment of males through scent. Behav Brain Res 200:295–303

    Article  CAS  PubMed  Google Scholar 

  • Hutchings MR, Kyriazakis I, Papachristou TG, Gordon IJ, Jackson F (2000) The herbivores’ dilemma: trade-offs between nutrition and parasitism in foraging decisions. Oecologia 124:242–251

    Article  Google Scholar 

  • Kallio ER, Klingstrom J, Gustafsson E, Manni T, Vaheri A, Henttonen H, Vapalahti O, Lundkvist A (2006a) Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. J Gen Virol 87:2127–2134

    Article  CAS  PubMed  Google Scholar 

  • Kallio ER, Poikonen A, Vaheri A, Vapalahti O, Henttonen H, Koskela E, Mappes T (2006b) Maternal antibodies postpone hantavirus infection and enhance individual breeding success. Proc R Soc Lond B 273:2771–2776

    Article  Google Scholar 

  • Kallio ER, Voutilainen L, Vapalahti O, Vaheri A, Henttonen H, Koskela E, Mappes T (2007) Endemic hantavirus infection impairs the winter survival of its rodent host. Ecology 88:1911–1916

    Article  PubMed  Google Scholar 

  • Kallio-Kokko H, Laakkonen J, Rizzoli A, Tagliapietra V, Cattadori I, Perkins SE, Hudson PJ, Cristofolini A, Versini W, Vapalahti O, Vaheri A, Henttonen H (2006) Hantavirus and arenavirus antibody prevalence in rodents and humans in Trentino, Northern Italy. Epidemiol Infect 134:830–836

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kavaliers M, Colwell DD, Ossenkopp KP, Perrot-Sinal TS (1997) Altered responses to female odors in parasitized male mice: neuromodulatory mechanisms and relations to female choice. Behav Ecol Sociobiol 40:373–384

    Article  Google Scholar 

  • Kavaliers M, Choleris E, Pfaff DW (2005) Genes, odours and the recognition of parasitized individuals by rodents. Trends Parasitol 21:423–429

    Article  CAS  PubMed  Google Scholar 

  • Klein SL (2003) Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol Behav 79:441–449

    Article  CAS  PubMed  Google Scholar 

  • Kruczek M (1997) Male rank and female choice in the bank vole, Clethrionomys glareolus. Behav Processes 40:171–176

    Article  CAS  PubMed  Google Scholar 

  • Mazurkiewicz M (1971) Shape, size and distribution of home ranges of Clethrionomys glareolus (Schreber, 1780). Acta Theriol 16:23–60

    Article  Google Scholar 

  • McCallum H, Barlow N, Hone J (2001) How should pathogen transmission be modelled? Trends Ecol Evol 16:295–300

    Article  PubMed  Google Scholar 

  • McLennan DA, Brooks DR (1991) Parasites and sexual selection: a macroevolutionary perspective. Q Rev Biol 66:255–286

    Article  CAS  PubMed  Google Scholar 

  • Mills JN, Schmidt K, Ellis BA, Calderon G, Enria DA, Ksiazek TG (2007a) A longitudinal study of hantavirus infection in three sympatric reservoir species in agroecosystems on the Argentine Pampa. Vector-Borne Zoonotic Dis 7:229–240

    Article  PubMed  Google Scholar 

  • Mills SC, Grapputo A, Koskela E, Mappes T (2007b) Quantitative measure of sexual selection with respect to the operational sex ratio: a comparison of selection indices. Proc R Soc Lond B 274:143–150

    Article  CAS  Google Scholar 

  • Netski D, Thran BH, Jeor SS (1999) Sin Nombre virus pathogenisis in Peromyscus maniculatus. J Virol 73:585–591

    CAS  PubMed Central  PubMed  Google Scholar 

  • Niklasson B, Hornfeldt B, Lundkvist A, Bjorsten S, LeDuc J (1995) Temporal dynamics of Puumala virus antibody prevalence in voles and of nephropathia epidemica incidence in humans. Am J Trop Med Hyg 53:134–140

    CAS  PubMed  Google Scholar 

  • Olsson GE, Leirs H, Henttonen H (2010) Hantaviruses and their hosts in Europe: reservoirs here and there, but not everywhere? Vector Borne Zoonotic Dis 10:549–561

    Article  PubMed  Google Scholar 

  • Penn D, Potts WK (1998) Chemical signals and parasite-mediated sexual selection. Trends Ecol Evol 13:391–396

    Article  CAS  PubMed  Google Scholar 

  • Rozenfeld FM, Denoel A (1994) Chemical signals involved in spacing behavior of breeding female bank voles (Clethrionomys glareolus Schreber-1780, Microtidae, Rodentia). J Chem Ecol 20:803–813

    Article  CAS  PubMed  Google Scholar 

  • Rozenfeld FM, Le Boulange E, Rasmont R (1987) Urine marking by male bank voles (Clethrionomys glareolus Schreber, 1780; Microtidae, Rodentia) in relation to their social rank. Can J Zool 65:2594–2601

    Article  Google Scholar 

  • Sauvage F, Langlais M, Yoccoz NG, Pontier D (2003) Modelling hantavirus in fluctuating populations of bank voles: the role of indirect transmission on virus persistence. J Anim Ecol 72:1–13

    Article  Google Scholar 

  • Telfer S, Birtles R, Bennett M, Lambin X, Paterson S, Begon M (2008) Parasite interactions in natural populations: insights from longitudinal data. Parasitology 135:767–781

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tersago K, Schreurs A, Linard C, Verhagen R, Van Dongen S, Leirs H (2008) Population, environmental, and community effects on local bank vole (Myodes glareolus) Puumala virus infection in an area with low human incidence. Vector Borne Zoonotic Dis 8:235–244

    Article  CAS  PubMed  Google Scholar 

  • Tersago K, Verhagen R, Leirs H (2011) Temporal variation in individual factors associated with hantavirus infection in bank voles during an epizootic: implications for Puumala virus transmission dynamics. Vector Borne Zoonotic Dis 11:715–721

    Article  PubMed  Google Scholar 

  • Thomas F, Adamo S, Moore J (2005) Parasitic manipulation: where are we and where should we go? Behav Process 68:185–199

    Article  Google Scholar 

  • van der Wal R, Irvine J, Stein A, Shepherd M, Albon SD (2000) Faecal avoidance and the risk of infection by nematodes in a natural population of reindeer. Oecologia 124:19–25

    Article  Google Scholar 

  • Walsh PT, McCreless E, Pedersen AB (2013) Faecal avoidance and selective foraging: do wild mice have the luxury to avoid faeces? Anim Behav 86:559–566

    Article  PubMed Central  PubMed  Google Scholar 

  • Wyatt TD (2003) Pheromones and animal behaviour. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Yamazaki K, Boyse EA, Bard J, Curran M, Kim D, Ross SR, Beauchamp GK (2002) Presence of mouse mammary tumor virus specifically alters the body odor of mice. Proc Natl Acad Sci 99:5612–5615

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yanagihara R, Amyx HL, Gajdusek DC (1985) Experimental infection with Puumala virus, the etiologic agent of nephropathia epidemica, in bank voles (Clethrionomys glareolus). J Virol 55:34–38

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ylönen H, Viitala J (1991) Social overwintering and food distribution in the bank vole Clethrionomys glareolus. Ecography 14:131–137

    Article  Google Scholar 

  • Ylönen H, Sundell J, Tiilikainen R, Eccard JA, Horne T (2003) Weasels’ (Mustela nivalis nivalis) preference for olfactory cues of the vole (Clethrionomys glareolus). Ecology 84:1447–1452

    Article  Google Scholar 

Download references

Acknowledgments

This study was partially funded by EU grant FP7-261504 EDENext and is catalogued by the EDENext Steering Committee as EDENext212 (http://www.edenext.eu). We gratefully acknowledge the University of Antwerp for financial support (BOF-GOA project FFB3567), the Agency for Nature and Forest for permits and assistance, and Olli Vapalahti for providing IFA slides. We also thank Simon Baeckens, Indra Jacobs and Sam Puls for their assistance in the field, and Benny Borremans, Jonas Reijniers, Stefan Vandongen, Luc De Bruyn and Natalie Van Houtte for laboratory and statistical assistance. Ethical approval for this experiment was given by the University of Antwerp’s Animal Ethics Committee (approval no. 2012-14). N. K. H. is a postdoctoral research fellow with the Fonds Wetenschappelijk Onderzoek—Vlaanderen, and S. H. was supported by a University of Antwerp BOF fellowship.

Author information

Authors and Affiliations

  1. Evolutionary Ecology Group, Department of Biology, University of Antwerp, Groenenborgerlaan 171, 2020, Antwerp, Belgium

    Nelika K. Hughes, Sanne Helsen, Katrien Tersago & Herwig Leirs

Authors
  1. Nelika K. Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sanne Helsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katrien Tersago
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Herwig Leirs
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Nelika K. Hughes or Herwig Leirs.

Additional information

Communicated by Janne Sundell.

N. K. Hughes and S. Helsen contributed equally to the work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hughes, N.K., Helsen, S., Tersago, K. et al. Puumala hantavirus infection alters the odour attractiveness of its reservoir host. Oecologia 176, 955–963 (2014). https://doi.org/10.1007/s00442-014-3072-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-3072-x

Keywords

Search

Navigation