Skip to main content
SpringerLink
Log in

Parasite load and seasonal migration in red deer

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

Abstract

Northern deer populations are typically partially migratory, but the relationship between migratory movements and parasites has received little attention. Migration often involves movement from a low-elevation winter range towards a summer range at higher elevation. In Europe these movements may also involve a gradient in abundance of Ixodes ricinus ticks, but whether tick loads on deer differ depending on migration tactic has not been quantified. Based on the examination of ears from 49 red deer (Cervus elaphus) marked with global positioning system collars, we provide the first evidence that the tick loads of deer covering longer distances between their winter and summer range, resulting in higher difference in elevation, are lower. Our study highlights that only the resident part of the red deer population will be available as year-round hosts to ticks, while a large part of the red deer population is unavailable to ticks for most of the tick questing season due to seasonal migration to higher elevation. Predicted changes in the migratory behaviour of ungulates could hence affect the proportion of the host population available to ticks in the future.

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.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Albon SD, Langvatn R (1992) Plant phenology and the benefits of migration in a temperate ungulate. Oikos 65:502–513

    Article  Google Scholar 

  • Albon SD, Stien A, Irvine RJ, Langvatn R, Ropstad E, Halvorsen O (2002) The role of parasites in the dynamics of a reindeer population. Proc R Soc Lond Ser B 269:1625–1633

    Article  CAS  Google Scholar 

  • Altizer S, Bartel R, Han BA (2011) Animal migration and infectious disease risk. Science 331:296–302

    Article  CAS  PubMed  Google Scholar 

  • Apollonio M, Andersen R, Putman R (2010) European ungulates and their management in the 21st century. Cambridge University Press, Cambridge

    Google Scholar 

  • Bischof R, Loe LE, Meisingset EL, Zimmermann B, Van Moorter B, Mysterud A (2012) A migratory ungulate in the pursuit of spring: jumping or surfing the green wave? Am Nat 180:407–424

    Article  PubMed  Google Scholar 

  • Bolger DT, Newmark WD, Morrison TA, Doak DF (2008) The need for integrative approaches to understand and conserve migratory ungulates. Ecol Lett 11:63–77

    PubMed  Google Scholar 

  • Bunnefeld N, Börger L, Van Moorter B, Rolandsen CM, Dettki H, Solberg EJ, Ericsson G (2011) A model-driven approach to quantify migration patterns: individual, regional and yearly differences. J Anim Ecol 80:466–476

    Article  PubMed  Google Scholar 

  • Cagnacci F, Focardi S, Heurich M, Hewison AJM, Kjellander P, Linnell JDC, Mysterud A, Neteler M, Delucchi L, Ossi F, Urbano F (2011) Partial migration in roe deer: migratory and resident tactics are end points of a behavioural gradient determined by ecological factors. Oikos 120:1790–1802

    Article  Google Scholar 

  • Christie CE (2007) Can life history strategies explain differences in grooming activity in red deer (Cervus elaphus)? Master of Science. University of Bergen, Norway

    Google Scholar 

  • Folstad I, Nilssen AC (1990) Abundance of warble fly larvae Hypoderma tarandi (L.) (Diptera: Oestridae) in reindeer Rangifer tarandus tarandus (L.) and its relation to reindeer postcalving migration. Rangifer Spec Iss 3:239

  • Folstad I, Nilssen AC, Halvorsen O, Andersen JH (1991) Parasite avoidance: the cause of post-calving migrations in rangifers? Can J Zool 69:2423–2429

    Article  Google Scholar 

  • Fryxell JM, Sinclair ARE (1988) Causes and consequences of migration by large herbivores. Trend Ecol Evol 3:237–241

    Article  CAS  Google Scholar 

  • Fyumagwa RD, Runyoro V, Horak IG, Hoare R (2007) Ecology and control of ticks as disease vectors in wildlife of the Ngorongoro Crater, Tanzania. South Afr J Wildl Res 37:79–90

    Article  Google Scholar 

  • Gaillard J-M, Yoccoz NG (2003) Temporal variation in survival of mammals: a case of environmental canalization? Ecology 84:3294–3306

    Article  Google Scholar 

  • Gaillard J-M, Festa-Bianchet M, Yoccoz NG (1998) Population dynamics of large herbivores: variable recruitment with constant adult survival. Trends Ecol Evol 13:58–63

    Article  CAS  PubMed  Google Scholar 

  • Gallivan GJ, Culverwell J, Girdwood R, Surgeoner GA (1995) Ixodid ticks of impala (Aepyceros melampus) in Swaziland: effect of age class, sex, body condition and management. South Afr J Zool 30:178–186

    Article  Google Scholar 

  • Gilbert L (2010) Altitudinal patterns of tick and host abundance: a potential role for climate change in regulating tick-borne diseases? Oecologia 162:217–225

    Article  PubMed  Google Scholar 

  • Gilbert L, Maffey GL, Ramsay SL, Hester AJ (2012) The effect of deer management on the abundance of Ixodes ricinus in Scotland. Ecol Appl 22:658–667

    Article  CAS  PubMed  Google Scholar 

  • Gunn A, Irvine RJ (2003) Subclinical parasitism and ruminant foraging strategies: a review. Wildl Soc Bull 31:117–126

    Google Scholar 

  • Handeland K, Qviller L, Vikøren T, Viljugrein H, Lillehaug A, Davidson RK (2013) Ixodes ricinus infestation in free-ranging cervids in Norway—a study based upon ear examinations of hunted animals. Vet Parasitol 195:142–149

    Article  PubMed  Google Scholar 

  • Harris G, Thirgood S, Hopcraft JGC, Cromsigt JPGM, Berger J (2009) Global decline in aggregated migrations of large terrestrial mammals. Endanger Species Res 7:55–76

    Article  Google Scholar 

  • Hebblewhite M, Merrill EH (2007) Multiscale wolf predation risk for elk: does migration reduce risk? Oecologia 152:377–387

    Article  PubMed  Google Scholar 

  • Hebblewhite M, Merrill E, McDermid G (2008) A multi-scale test of the forage maturation hypothesis in a partially migratory ungulate population. Ecol Monogr 78:141–166

    Article  Google Scholar 

  • Hersh MH, LaDeauS L, Prevaitali MA, Ostfeld RS (2014) When is a parasite not a parasite? Effects of larval tick burdens on white-footed mouse survival. Ecology 95:1360–1369

    Article  PubMed  Google Scholar 

  • Jaenson TGT, Lindgren E (2011) The range of Ixodes ricinus and the risk of contracting Lyme borreliosis will increase northwards when the vegetation period becomes longer. Ticks Tick Borne Dis 2:44–49

    Article  PubMed  Google Scholar 

  • Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993

    Article  CAS  PubMed  Google Scholar 

  • Jore S, Viljugrein H, Hofshagen M, Brun-Hansen H, Kristoffersen A, Nygard K, Ottesen P, Saevik B, Ytrehus B, Brun E (2011) Multi-source analysis reveals latitudinal and altitudinal shifts in range of Ixodes ricinus at its northern distribution limit. Parasite Vector 4:84

    Article  Google Scholar 

  • Kiffner C, Lödige C, Alings M, Rühe F (2011a) Attachment site selection of ticks on roe deer, Capreolus capreolus. Exp Appl Acarol 53:79–94

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kiffner C, Lödige C, Alings M, Vor T, Rühe F (2011b) Body-mass or sex-biased tick parasitism in roe deer (Capreolus capreolus)? A GAMLSS approach. Med Vet Entomol 25:39–45

    Article  CAS  PubMed  Google Scholar 

  • Langvatn R (1986) Size and weight relationships in Norwegian red deer (Cervus elaphus atlanticus, Lønnberg). In: H. Reuss (ed.) Rotwild–cerf rouge–red deer. Conseil International de la Chasse et de la Conservation du Gibier (CIC), Graz, Austria

    Google Scholar 

  • Levi T, Kilpatrick AM, Mangel M, Wilmers CC (2012) Deer, predators, and the emergence of Lyme disease. Proc Natl Acad Sci USA 109:10942–10947

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Madslien K, Ytrehus B, Viljugrein H, Solberg EJ, Bråten KR, Mysterud A (2012) Prevalence and density of deer keds (Lipotena cervi) on moose (Alces alces) at the colonization border. Parasite Vector 5:e251

    Article  Google Scholar 

  • Mannelli A, Bertolotti L, Gern L, Gray J (2012) Ecology of Borrelia burgdorferi sensu lato in Europe: transmission dynamics in multi-host systems, influence of molecular processes and effects of climate change. FEMS Microbiol Rev 36:837–861

    Article  CAS  PubMed  Google Scholar 

  • Medlock JM, Hansford KM, Bormane A, Derdakova M, Estrada-Peña A, George JC, Golovljova I, Jaenson TGT, Jensen JK, Jensen PM, Kazimirova M, Oteo JA, Papa A, Pfister K, Plantard O, Randolph SE, Rizzoli A, Santos-Silva MM, Sprong H, Vial L, Hendrickx G, Zeller H, van Bortel W (2013) Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasite Vector 6:1

    Article  Google Scholar 

  • Milner JM, Bonenfant C, Mysterud A, Gaillard J-M, Csányi S, Stenseth NC (2006) Temporal and spatial development of red deer harvesting in Europe—biological and cultural factors. J Appl Ecol 43:721–734

    Article  Google Scholar 

  • Mooring MS, Hart BL (1997) Self grooming in impala mothers and lambs: testing the body size and tick challenge principles. Anim Behav 53:925–934

    Article  Google Scholar 

  • Mooring MS, Samuel WR (1998) Tick-removal grooming by elk (Cervus elaphus): testing the principles from the programmed-grooming hypothesis. Can J Zool 76:740–750

    Article  Google Scholar 

  • Mooring MS, Samuel WM (1999) Premature loss of winter hair in free-ranging moose (Alces alces) infested with winter ticks (Dermacentor albipictus) is correlated with grooming rate. Can J Zool 77:148–156

    Article  Google Scholar 

  • Mooring MS, Benjamin JE, Harte CR, Herzog NB (2000) Testing the interspecific body size principle in ungulates: the smaller they come, the harder they groom. Anim Behav 60:35–45

    Article  PubMed  Google Scholar 

  • Mooring MS, Reisig DD, Niemeyer JM, Osborne ER (2002) Sexually and developmentally dimorphic grooming: a comparative survey of the ungulata. Ethology 108:911–934

    Article  Google Scholar 

  • Mysterud A (2013) Ungulate migration, plant phenology, and large carnivores: “the times they are a-changin”. Ecology 94:1257–1261

    Article  PubMed  Google Scholar 

  • Mysterud A, Yoccoz NG, Stenseth NC, Langvatn R (2000) Relationships between sex ratio, climate and density in red deer: the importance of spatial scale. J Anim Ecol 69:959–974

    Article  Google Scholar 

  • Mysterud A, Langvatn R, Yoccoz NG, Stenseth NC (2001) Plant phenology, migration and geographic variation in body weight of a large herbivore: the effect of a variable topography. J Anim Ecol 70:915–923

    Article  Google Scholar 

  • Mysterud A, Loe LE, Zimmermann B, Bischof R, Veiberg V, Meisingset EL (2011) Partial migration in expanding red deer populations at northern latitudes—a role for density dependence? Oikos 120:1817–1825

    Article  Google Scholar 

  • Mysterud A, Hatlegjerde IL, Sørensen OJ (2014) Attachment site selection of life stages of Ixodes ricinus ticks on a main large host in Europe, the red deer (Cervus elaphus). Parasite Vector 7:510

    Google Scholar 

  • Ostfeld RS, Canham CD, Oggenfuss K, Winchcombe RJ, Keesing F (2006) Climate, deer, rodents, and acorns as determinants of variation in Lyme-disease risk. PLoS Biol 4:1058–1068

    Article  CAS  Google Scholar 

  • Qviller L, Risnes-Olsen N, Bærum KM, Meisingset EL, Loe LE, Ytrehus B, Viljugrein H, Mysterud A (2013) Landscape level variation in tick abundance relative to seasonal migration pattern of red deer. PLoS One 6:1

    Google Scholar 

  • Qviller L, Grøva L, Viljugrein H, Klingen I, Mysterud A (2014) Temporal pattern of questing tick Ixodes ricinus density at differing elevations in the coastal region of western Norway. Parasite Vector 7:179

    Article  Google Scholar 

  • Sente C, Meisingset EL, Evans AL, Wedul SJ, Zimmermann B, Arnemo JM (2014) Reversible immobilization of free-ranging red deer (Cervus elaphus atlanticus) with xylazine-tiletamine-zolazapam and atipamezole. J Wildl Dis 20:359–363

    Article  Google Scholar 

  • St Juliana JR, Khokhlova IS, Wielebnowski N, Kotler BP, Krasnov BR (2014) Ectoparasitism and stress hormones: strategy of host exploitation, common host-parasite history and energetics matter. J Anim Ecol 83:1113–1123

    Article  PubMed  Google Scholar 

  • Stuen S, Handeland K, Frammarsvik T, Bergstrom K (2001) Experimental Ehrlichia phagocytophilia infection in red deer (Cervus elaphus). Vet Rec 149:390–392

    Article  CAS  PubMed  Google Scholar 

  • Woldehiwet Z (2010) The natural history of Anaplasma phagocytophilum. Vet Parasitol 167:108–122

    Article  CAS  PubMed  Google Scholar 

  • Wood CL, Lafferty KD (2013) Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trend Ecol Evol 28:239–247

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to the hunters for help in sampling ears and other data on GPS-marked red deer which were harvested, and to Anders Herland for examining the ears for ticks. This study was funded by the Norwegian Research Council and the Norwegian Environment Agency (project TickDeer, 203786/E40).

Author contribution statement

A. M. designed the study. E. L. M. collected the data. A. M., L. Q. and H. V. analysed the data. A. M. wrote the manuscript; other authors provided editorial advice.

Author information

Authors and Affiliations

  1. Department of Biosciences, Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, Blindern, P.O. Box 1066, 0316, Oslo, Norway

    Atle Mysterud, Lars Qviller & Hildegunn Viljugrein

  2. The Norwegian Institute of Bioeconomy Research, 6630, Tingvoll, Norway

    Erling L. Meisingset

  3. Norwegian Veterinary Institute, Sentrum, P.O. Box 750, 0106, Oslo, Norway

    Hildegunn Viljugrein

Authors
  1. Atle Mysterud
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lars Qviller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Erling L. Meisingset
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hildegunn Viljugrein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Atle Mysterud.

Additional information

Communicated by Jean-Michel Gaillard.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mysterud, A., Qviller, L., Meisingset, E.L. et al. Parasite load and seasonal migration in red deer. Oecologia 180, 401–407 (2016). https://doi.org/10.1007/s00442-015-3465-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3465-5

Keywords

Search

Navigation