Abstract
Blood-sucking ectoparasites have often a strong impact on the behaviour of their hosts. The annual insect harassment of reindeer (Rangifer tarandus tarandus) has increased in the southern part of the Finnish reindeer herding area because of the recent invasion of a blood-feeding ectoparasitic louse-fly, the deer ked (Lipoptena cervi). We studied the impact of the deer ked on the behaviour of reindeer. Twelve reindeer were infested with a total of 300 keds/reindeer on six occasions in a 5-week period during the deer ked flight season in autumn, while six non-infested reindeer were used as controls. Behavioural patterns indicating potential stress were monitored by visual observation from August to December. The infested reindeer displayed more incidences of restless behaviour than the controls. Shaking and scratching were the most common forms of restless behaviour after infestation of deer keds. Increased grooming was also observed after the transplantation and also later, 1 month after the infestation. Based on the results, the deer ked infestation can cause acute behavioural disturbance in reindeer and, thus, could pose a potential threat to reindeer welfare. Antiparasitic treatment with, e.g. ivermectin, may increase the welfare of parasitized reindeer by reducing deer keds. If the deer ked infestation intensity on the reindeer herding area increases and restless behaviour of reindeer becomes more common, the present results can help in further evaluation of the duration and magnitude of behavioural changes.
Similar content being viewed by others
References
Agnew P, Koella JC, Michalakis Y (2000) Host life history responses to parasitism. Microbes Infect 2:891–896
Anderson JR, Nilssen AC (1998) Do reindeer aggregate on snow patches to reduce harassment by parasitic flies or to thermoregulate? Rangifer 18:3–17
Beaumont LJ, Hughes L (2002) Potential changes in the distributions of latitudinally restricted Australian butterfly species in response to climate change. Glob Change Biol 8:954–971
Bequaert J (1953) The Hippoboscidae or louse-flies (Diptera) of mammals and birds. Part I. Structure, physiology and natural history. Entomol Am 32(33):1–442
Bergman AM (1917) Om renens oestrider. Entomologisk Tidsskrift 38(1–32):113–146 (in Swedish)
Böse R, Petersen K (1991) Lipoptena cervi (Diptera), a potential vector of Megatrypanum trypanosomes of deer (Cervidae). Parasitol Res 77:723–725
Boulinier T, McCoy KD, Sorci G (2001) Dispersal and parasitism. In: Clobert J, Danchin E, Dhont AA, Nichols JD (eds) Dispersal. Oxford University Press, New York, pp 169–179
Cederlund G, Liberg O (1995) Rådjuret, viltet, ekologin och jakten. Almqvist & Wiksell, Uppsala (in Swedish)
Dehio C, Sauder U, Hiestand R (2004) Isolation of Bartonella schoenbuchensis from Lipoptena cervi, a blood-sucking arthropod causing deer ked dermatitis. J Clin Microbiol 42:5320–5323
Evans GO (1950) Studies on the bionomics of the sheep ked, Melophagus ovinus L. in west Wales. Bull Ent Res 40:459–478
Fitze PE, Tschirren B, Richner H (2004) Life history and fitness consequences of ectoparasites. J Anim Ecol 73:216–226
Gothe R, Schöl H (1994) Deer keds (Lipoptena cervi) in the accompanying equipment of the Late Neolithic human mummy from the Similaun, South Tyrol. Parasitol Res 80:81–83
Haarløv N (1964) Life cycle and distribution pattern of Lipoptena cervi (L.) (Dipt., Hippobosc.) on Danish deer. Oikos 15:93–129
Hackman W, Rantanen T, Vuojolahti P (1983) Immigration of Lipoptena cervi (Diptera, Hippoboscidae) in Finland, with notes on its biology and medical significance. Notulae Entomol 63:53–59
Hagemoen R, Reimers E (2002) Reindeer summer activity pattern in relation to weather and insect harassment. J Anim Ecol 71:883–892
Härkönen L, Härkönen S, Kaitala A, Kaunisto S, Kortet R, Laaksonen S, Ylönen H (2010) Predicting range expansion of an ectoparasite—the effect of spring and summer temperatures on deer ked (Lipoptena cervi) performance along a latitudinal gradient. Ecography 33:906–912
Härkönen L, Hurme E, Kaitala A (2013) Unexpected seasonal variation in offspring size and performance of a viviparous ectoparasite. Parasitology 140:229–236
Hart BL (1990) Behavioral adaptations to pathogens and parasites: five strategies. Neurosci Biobehav Rev 14:273–294
Hart BL (1994) Behavioural defence against parasites: interaction with parasite invasiveness. Parasitology 109:139–151
Hase A (1940) Über Lipoptena cervi L. und über die Wirkung ihrer Stiche. (Dipt. Pupipara.). Parasitol Res 11:410–418
Helle T, Aspi J, Lempa K, Taskinen E (1992) Strategies to avoid biting flies by reindeer: field experiment with silhouette traps. Ann Zool Fenn 29:69–74
Ivanov VI [Иванов ВИ] (1981) [Spread of the deer ked Lipoptena cervi L. (Diptera, Hippoboscidae) in Belarus, its biology and deleterious effects]. Dissertation, Veterinary Academy of Moscow (in Russian)
Kaitala A, Kortet R, Härkönen S, Laaksonen S, Härkönen L, Kaunisto S, Ylönen H (2009) Deer ked, an ectoparasite of moose in Finland: a brief review of its biology and invasion. Alces 45:85–88
Kaunisto S, Kortet R, Härkönen L, Härkönen S, Ylönen H, Laaksonen S (2009) New bedding site examination-based method to analyse deer ked (Lipoptena cervi) infection in cervids. Parasitol Res 104:919–925
Kortet R, Härkönen L, Hokkanen P, Härkönen S, Kaitala A, Kaunisto S, Laaksonen S, Kekäläinen J, Ylönen H (2010) Experiments on the ectoparasitic deer ked that often attacks humans; preferences for body parts, colour and temperature. Bull Entomol Res 100:279–285
Kynkäänniemi S-M, Kortet R, Härkönen L, Kaitala A, Paakkonen T, Mustonen A-M, Nieminen P, Härkönen S, Ylönen H, Laaksonen S (2010) Threat of an invasive parasitic fly, the deer ked (Lipoptena cervi), to reindeer (Rangifer tarandus tarandus): experimental infection and treatment. Ann Zool Fenn 47:28–36
Laaksonen S, Oksanen A, Orro T, Norberg H, Nieminen M, Sukura A (2008) Efficacy of different treatment regimes against setariosis (Setaria tundra, Nematoda: Filarioidea) and associated peritonitis in reindeer. Acta Vet Scand 50:49
Laaksonen S, Solismaa M, Kortet R, Kuusela J, Oksanen A (2009) Vectors and transmission dynamics for Setaria tundra (Filarioidea; Onchocercidae), a parasite of reindeer in Finland. Parasit Vectors 2:3
Laaksonen S, Pusenius J, Kumpula J, Venäläinen A, Kortet R, Oksanen A, Hoberg E (2010) Climate change promotes the emergence of serious disease outbreaks for filarioid nematodes. Ecohealth 7:7–13
Lemke P, Ren J et al (2007) Observations: Changes in snow, ice and frozen ground. Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Cambridge university press. United Kingdom and New York, Cambridge, pp 337–383
Madslien K, Ytrehus B, Vikøren T, Malmsten J, Isaksen K, Hygen H, Solberg E (2011) Hair-loss epizootic in moose (Alces alces) associated with massive deer ked (Lipoptena cervi) infestation. J Wildl Dis 47:893–906
McLaughlin RF, Addison EM (1986) Tick (Dermacentor albipictus)-induced winter hair-loss in captive moose (Alces alces). J Wildl Dis 22:502–510
Moore J (2002) Parasites and behavior of animals. Oxford University Press, New York
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
Nelson WA (1962) Development in sheep of resistance to the ked Melophagus ovinus (L.). I. Effects of seasonal manipulation of infestations. Exp Parasitol 12:41–44
Nelson WA (1984) Effects of nutrition of animals on their ectoparasites. J Med Entomol 21:621–635
Paakkonen T, Mustonen A-M, Roininen H, Niemelä P, Ruusila V, Nieminen P (2010) Parasitism of the deer ked, Lipoptena cervi, on the moose, Alces alces, in eastern Finland. Med Vet Entomol 24:411–417
Paakkonen T, Mustonen A-M, Käkelä R, Kiljander T, Kynkäänniemi S-M, Laaksonen S, Solismaa M, Aho J, Kortet R, Puukka K, Saarela S, Härkönen L, Kaitala A, Ylönen H, Nieminen P (2011) Experimental infection of the deer ked (Lipoptena cervi) has no negative effects on the physiology of the captive reindeer (Rangifer tarandus tarandus). Vet Parasitol 179:180–188
Paakkonen T, Mustonen A-M, Käkelä R, Laaksonen S, Solismaa M, Aho J, Puukka K, Nieminen P (2012) The effects of an abundant ectoparasite, the deer ked (Lipoptena cervi), on the health of moose (Alces alces) in Finland. Parasitol Res 111:1223–1232
Parmesan C, Ryrholm N, Stefanescu C, Hill JK, Thomas CD, Descimon H, Huntley B, Kaila L, Kullberg J, Tammaru T, Tennent WJ, Thomas JA, Warren M (1999) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399:579–583
Poulin R (1995) “Adaptive” changes in the behaviour of parasitized animals: a critical review. Int J Parasitol 25:1371–1383
Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, Princeton NJ
Reimers E (1982) Winter mortality and population trends of reindeer on Svalbard, Norway. Arct Antarct Alp Res 14:295–300
Samuel WM (1991) Grooming by moose (Alces alces) infested with the winter tick, Dermacentor albipictus (Acari): a mechanism for premature loss of winter hair. Can J Zool 69:1255–1260
Samuel WM (2007) Factors affecting epizootics of winter ticks and mortality of moose. Alces 34:39–48
Sokolov VE, Chernova OF (1987) Morphology of the skin of moose (Alces alces L.). Swedish Wildlife Research Suppl 1:367–375
Timisjärvi J, Nieminen M, Sippola AL (1984) The structure and insulation properties of the reindeer fur. Comp Biochem Physiol A 79:601–609
Toupin B, Huot J, Manseau M (1996) Effect of insect harassment on the behaviour of the Riviere George caribou. Arctic 49:375–382
Välimäki P, Madslien K, Malmsten J, Härkönen L, Härkönen S, Kaitala A, Kortet R, Laaksonen S, Mehl R, Redford L, Ylönen H, Ytrehus B (2010) Fennoscandian distribution of an important parasite of cervids, the deer ked (Lipoptena cervi), revisited. Parasitol Res 107:117–125
Välimäki P, Kaitala A, Madslien K, Härkönen L, Várkonyi G, Heikkilä J, Jaakola M, Ylönen H, Kortet R, Ytrehus B (2011) Geographical variation in host use of a blood-feeding ectoparasitic fly: implications for population invasiveness. Oecologia 166:985–995
Vanhanen H, Veteli T, Päivinen S, Kellomäki S, Niemelä P (2007) Climate change and range shifts in two insect defoliators: gypsy moth and nun moth—a model study. Silva Fennica 41:621–638
Weladji RB, Klein DR, Holand Ø, Mysterud A (2002) Comparative response of Rangifer tarandus and other northern ungulates to climatic variability. Rangifer 22:29–46
Weladji RB, Holand Ø, Almøy T (2003) Use of climatic data to assess the effect of insect harassment on the autumn weight (Rangifer tarandus) calves. J Zool 260:79–85
Acknowledgments
We want to thank Jari Ylönen, Milla Solismaa, Anu Ruohomäki, Anna Honkanen, Pertti Rautio, the Biological Research Facility Unit of the University of Oulu and Finnish Food Safety Authority for their help during the experiment. We thank also the University of Oulu, Vetcare Oy and the Ministry of Agriculture and Forestry (Makera), Oulu University Scholarship Foundation (S-M.K.), Finnish Concordia Fund (S-M.K.) and Finnish Cultural Foundation (S-M.K.) for the financial support for this study. Thanks also to Arctic Doctoral Programme ARKTIS (Arctic Centre, University of Lapland) and Graduate School of the Unversity of Oulu (UniOgs) for their support to this study (S-M.K.). We also want to thank Panu Välimäki for his useful comments for this manuscript.
The experiment complied with the current laws of Finland and was conducted by the permission of the Committee on Animal Experiments of the University (licence decision STH378A; 16 May 2007/ESLH-2007-03532/Ym-23).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kynkäänniemi, SM., Kettu, M., Kortet, R. et al. Acute impacts of the deer ked (Lipoptena cervi) infestation on reindeer (Rangifer tarandus tarandus) behaviour. Parasitol Res 113, 1489–1497 (2014). https://doi.org/10.1007/s00436-014-3790-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-014-3790-3