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Invasion rate of deer ked depends on spatiotemporal variation in host density

Published online by Cambridge University Press:  13 February 2014

C. M. Meier ,
D. Bonte ,
A. Kaitala  and
O. Ovaskainen
C. M. Meier*
Affiliation:
Swiss Ornithological Institute, Seerose 1, CH-6204 Sempach, Switzerland
D. Bonte
Affiliation:
Terrestrial Ecology Unit, Department of Biology, Ghent University, K.L. Ledeganckstraat 35, 9000 Gent, Belgium
A. Kaitala
Affiliation:
Animal Ecology, Department of Biology, University of Oulu, P.O. Box 3000, 90014, Finland
O. Ovaskainen
Affiliation:
Metapopulation Research Group, Department of Biosciences, University of Helsinki, PO Box 65, 00014, Finland
*
*Author for correspondence Phone: +41(0)414629710 Fax: +41(0)414629710 E-mail: christoph.meier@vogelwarte.ch
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Abstract

Invasive parasites are of great global concern. Understanding the factors influencing the spread of invading pest species is a first step in developing effective countermeasures. Growing empirical evidence suggests that spread rates are essentially influenced by spatiotemporal dynamics of host–parasite interactions, yet approaches modelling spread rate have typically assumed static environmental conditions. We analysed invasion history of the deer ked (Lipoptena cervi) in Finland with a diffusion–reaction model, which assumed either the movement rate, the population growth rate, or both rates may depend on spatial and temporal distribution of moose (Alces alces), the main host of deer ked. We fitted the model to the data in a Bayesian framework, and used the Bayesian information criterion to show that accounting for the variation in local moose density improved the model's ability to describe the pattern of the invasion. The highest ranked model predicted higher movement rate and growth rate of deer ked with increasing moose density. Our results suggest that the historic increase in host density has facilitated the spread of the deer ked. Our approach illustrates how information about the ecology of an invasive species can be extracted from the spatial pattern of spread even with rather limited data.

Keywords

diffusion–reaction modelspatiotemporal spread rateinsectrange expansion
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 3 , June 2014 , pp. 314 - 322
Copyright
Copyright © Cambridge University Press 2014 

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References

Araujo, M.B. & Luoto, M. (2007) The importance of biotic interactions for modelling species distributions under climate change. Global Ecology and Biogeography 16, 743–753.CrossRefGoogle Scholar
Bjorneraas, K., Solberg, E.J., Herfindal, I., Van Moorter, B., Rolandsen, C.M., Tremblay, J.P., Skarpe, C., Saether, B.E., Eriksen, R. & Astrup, R. (2011) Moose Alces alces habitat use at multiple temporal scales in a human-altered landscape. Wildlife Biology 17(1), 44–54.CrossRefGoogle Scholar
Burgman, M.A. & Fox, J.C. (2003) Bias in species range estimates from minimum convex polygons: implications for conservation and options for improved planning. Animal Conservation 6, 19–28.CrossRefGoogle Scholar
Burton, O.J., Phillips, B.L. & Travis, J.M.J. (2010) Trade-offs and the evolution of life-histories during range expansion. Ecology Letters 13, 1210–1220.CrossRefGoogle ScholarPubMed
Cook, A., Marion, G., Butler, A. & Gibson, G. (2007) Bayesian inference for the spatio-temporal invasion of alien species. Bulletin of Mathematical Biology 69, 2005–2025.CrossRefGoogle ScholarPubMed
Duodu, S., Madslien, K., Hjelm, E., Molin, Y., Paziewska-Harris, A., Harris, P.D., Colquhoun, D.J. & Ytrehus, B. (2013) Bartonella infections in deer keds (Lipoptena cervi) and moose (Alces alces) in Norway. Applied and Environmental Microbiology 79(1), 322–327.CrossRefGoogle ScholarPubMed
Eraud, C., Boutin, J.M., Roux, D. & Faivre, B. (2007) Spatial dynamics of an invasive bird species assessed using robust design occupancy analysis: the case of the Eurasian collared dove (Streptopelia decaocto) in France. Journal of Biogeography 34, 1077–1086.CrossRefGoogle Scholar
Evans, A.M. & Gregoire, T.G. (2007) A geographically variable model of hemlock woolly adelgid spread. Biological Invasions 9, 369–382.CrossRefGoogle Scholar
Ficetola, G.F., Maiorano, L., Falcucci, A., Dendoncker, N., Boitani, L., Padoa-Schioppa, E., Miaud, C. & Thuiller, W. (2010) Knowing the past to predict the future: land-use change and the distribution of invasive bullfrogs. Global Change Biology 16, 528–537.CrossRefGoogle Scholar
Fisher, R. (1937) The wave of advance of advantageous genes. Annals of Eugenics 7, 355–369.CrossRefGoogle Scholar
Fujisaki, I., Pearlstine, E.V. & Mazzotti, F.J. (2010) The rapid spread of invasive Eurasian Collared Doves Streptopelia decaocto in the continental USA follows human-altered habitats. Ibis 152, 622–632.CrossRefGoogle Scholar
Gilbert, M., Gregoire, J.C., Freise, J.F. & Heitland, W. (2004) Long-distance dispersal and human population density allow the prediction of invasive patterns in the horse chestnut leafminer Cameraria ohridella . Journal of Animal Ecology 73, 459–468.CrossRefGoogle Scholar
Haarlov, N. (1964) Life cycle and distribution pattern of Lipoptena cervi(L.) (Dipt., Hippobosc.) on Danish deer. Oikos 15, 93–129.CrossRefGoogle Scholar
Hackman, W. (1972) Algens lusfluga, en ostlig invandrare i Finland. The louse fly, an eastern immigrant in Finland. Memoranda Soc Fauna Flora Fennica 48, 45–47.Google Scholar
Hackman, W. (1977) Hirven taikarpanen ju sen levittaytyminen. The deer-fly, Lipoptena cervi, invading Finland. Luonnon Tutkija 81, 75–77.Google Scholar
Hackman, W. (1979) Alglusflugans, Lipoptena cervi, invandringshistoria i Finland. The deer ked, Lipoptena cervi, its history of spread in Finland. Entomologisk-Tidskrift 100(3–4), 208–210.Google Scholar
Hackman, W., Rantanen, T. & Vuojolahti, P. (1983) Immigration of Lipoptena cervi (Diptera, Hippoboscidae) in Finland, with notes on its biology and medical significance. Notulae-Entomologicae 63, 53–59.Google Scholar
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 (Diptera: Hippoboscidae) performance along a latitudinal gradient. Ecography 33, 906–912.CrossRefGoogle Scholar
Härkönen, L., Kaitala, A., Kaunisto, S. & Repo, T. (2012) High cold tolerance through four seasons and all free-living stages in an ectoparasite. Parasitology 139, 926–933.CrossRefGoogle Scholar
Härkönen, L., Hurme, E. & Kaitala, A. (2013) Unexpected seasonal variation in offspring size and performance in a viviparous ectoparasite. Parasitology 139, 229–936.CrossRefGoogle Scholar
Hastings, A., Cuddington, K., Davies, K.F., Dugaw, C.J., Elmendorf, S., Freestone, A., Harrison, S., Holland, M., Lambrinos, J., Malvadkar, U., Melbourne, B.A., Moore, K., Taylor, C. & Thomson, D. (2005) The spatial spread of invasions: new developments in theory and evidence. Ecology Letters 8, 91–101.CrossRefGoogle Scholar
Heikkinen, S. (2000) Hirven Vuosi. Suomen Riisti 46, 82–91.Google Scholar
Hochkirch, A. & Damerau, M. (2009) Rapid range expansion of a wing-dimorphic bush-cricket after the 2003 climatic anomaly. Biological Journal of Linnean Society 97, 118–127.CrossRefGoogle Scholar
Holway, D.A. (1998) Factors governing rate of invasion: a natural experiment using Argentine ants. Oecologia 115, 206–212.CrossRefGoogle ScholarPubMed
Kadoya, T. & Washitani, I. (2010) Predicting the rate of range expansion of an invasive alien bumblebee (Bombus terrestris) using a stochastic spatio-temporal model. Biological Conservation 143, 1228–1235.CrossRefGoogle Scholar
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.Google Scholar
Keeling, M.J., Woolhouse, M.E.J., Shaw, D.J., Matthews, L., Chase-Topping, M., Haydon, D.T., Cornell, S.J., Kappey, J., Wilesmith, J. & Grenfell, B.T. (2001) Dynamics of the 2001 UK foot and mouth epidemic: stochastic dispersal in a heterogeneous landscape. Science 294, 813–817.CrossRefGoogle Scholar
Kortet, R., Härkönen, L., Hokkanen, P., Härkönen, S., Kaitala, A., Kaunisto, S., Laaksonen, S., Kekäläinen, J. and Ylönen, H. (2010) Experiments on the ectoparasitic deer ked that often attacks humans; preferences for body parts, colour and temperature. Bulletin of Entomological Research 100, 279–285.CrossRefGoogle ScholarPubMed
Kot, M., Lewis, M.A. & Van den Driessche, P. (1996) Dispersal data and the spread of invading organisms. Ecology 77, 2027–2042.CrossRefGoogle Scholar
Kuefler, D., Avgar, T. & Fryxell, J.M. (2012) Rotifer population spread in relation to food, density and predation risk in an experimental system. Journal of Animal Ecology 81, 323–329.CrossRefGoogle Scholar
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 the reindeer (Rangifer tarandus tarandus): experimental infection and treatment. Annales Zoologici Fennici 47, 28–36.CrossRefGoogle Scholar
Laukkanen, A., Ruoppi, P. & Mäkinen-Kiljunen, S. (2005) Deer ked-induced occupational allergic rhinoconjunctivitis. Annals of Allergy, Asthma and Immunology 94, 604–608.CrossRefGoogle ScholarPubMed
Liebhold, A.M. & Tobin, P.C. (2008) Population ecology of insect invasions and their management. Annual Review of Entomology 53, 387–408.CrossRefGoogle ScholarPubMed
Lockwood, J.L., Hoopes, M.F. & Marchetti, M.P. (2007) Invasion Ecology. Oxford, UK, Blackwell Publishing.Google Scholar
Loxdale, H.D., Lushai, G. (1999) Slaves of the environment: the movement of herbivorous insects in relation to their ecology and genotype. Philosophical Transactions of the Royal Society of London Series B – Biological Sciences 354, 1479–1495.CrossRefGoogle Scholar
Luoma, A. (2002) Moose Hunting in Finland – management of a heavily harvested population. Dissertation, University of Helsinki, Helsinki.Google Scholar
Mack, R.N., Simberloff, D., Lonsdale, W.M., Evans, H., Clout, M. & Bazzaz, F.A. (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10, 689–710.CrossRefGoogle Scholar
Madslien, K., Ytrehus, B., Viljugrein, H., Solberg, E.J., Bråten, K.R. & Mysterud, A. (2012) Factors affecting deer ked (Lipoptena cervi) prevalence and intensity in moose (Alces alces) in Norway. Parasites and Vectors 5, 251–261.CrossRefGoogle ScholarPubMed
Nygrén, T. (1987) The history of moose in Finland. Swedish Wildlife Research Supplement 1, 49–54.Google Scholar
Ovaskainen, O., Rekola, H., Meyke, E. & Arjas, E. (2008) Bayesian methods for analyzing movements in heterogeneous landscapes from mark-recapture data. Ecology 89, 542–554.CrossRefGoogle ScholarPubMed
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. Medical and Veterinary Entomology 24, 411–417.CrossRefGoogle ScholarPubMed
Phillips, B.L. (2012) Range shift promotes the formation of stable range edges. Journal of Biogeography 39, 153–161.CrossRefGoogle Scholar
Phillips, B.L., Brown, G.P., Travis, J.M.J. & Shine, R. (2008) Reid's paradox revisited: the evolution of dispersal kernels during range expansion. American Naturalist 172, S34–S48.CrossRefGoogle ScholarPubMed
Pioz, M., Guis, H., Crespin, L., Gay, E., Calavas, D., Durand, B., Abrial, D. & Ducrot, C. (2012) Why did bluetongue spread the way it did? Environmental factors influencing the velocity of bluetongue virus serotype 8 eqizootic wave in France. PLoS ONE 7(8), e43360.CrossRefGoogle ScholarPubMed
Pitt, J.P.W., Worner, S.P. & Suarez, A.V. (2009) Predicting Argentine ant spread over the heterogeneous landscape using a spatially explicit stochastic model. Ecological Applications 19, 1176–1186.CrossRefGoogle ScholarPubMed
Pusenius, J., Tykkyläinen, R., Wallén, M., Karhapää, A., Jouko, K. & Kimmo, M. (2009) Riistakannat 2009: Hirvikannan koko ja vasatuotto vuonna 2008. Riista-ja kalatalous-selvityksiä 18, 9–14.Google Scholar
Schwarz, G. (1978) Estimation dimension of a model. Annals of Statistics 6, 461–464.CrossRefGoogle Scholar
Sebert-Cuvillier, E., Simon-Goyheneche, V., Paccaut, F., Chabrerie, O., Goubet, O. & Decocq, G. (2008) Spatial spread of an alien tree species in a heterogeneous forest landscape: a spatially realistic simulation model. Landscape Ecology 23, 787–801.CrossRefGoogle Scholar
Shigesada, N., Kawasaki, K. & Takeda, Y. (1995) Modeling stratified diffusion in biological invasions. American Naturalist 146, 229–251.CrossRefGoogle Scholar
Skellam, J.G. (1951) Random dispersal in theoretical populations. Biometrika 38, 196–218.CrossRefGoogle ScholarPubMed
Thuiller, W., Richardson, D.M., Pysek, P., Midgley, G.F., Hughes, G.O. & Rouget, M. (2005) Niche-based modelling as a tool for predicting the risk of alien plant invasions at a global scale. Global Change Biology 11, 2234–2250.CrossRefGoogle ScholarPubMed
Tiilikainen, R., Solberg, E.J., Nygrén, T. & Pusenius, J. (2012) Spatio-temporal relationship between calf body mass and population productivity in Fennoscadian moose Alces alces . Wildlife Biology 18(3), 304–317.CrossRefGoogle Scholar
Tobin, P.C. (2007) Space-time patterns during the establishment of a nonindigenous species. Population Ecology 49, 257–263.CrossRefGoogle Scholar
Tobin, P.C., Berec, L. & Liebhold, A.M. (2011) Exploiting Allee effects for managing biological invasions. Ecology Letters 14, 615–624.CrossRefGoogle ScholarPubMed
Travis, J.M.J. & Dytham, C. (2002) Dispersal evolution during invasions. Evolutionary Ecology Research 4, 1119–1129.Google Scholar
Turchin, P. (1998) Quantitative Analysis of Movement. Sunderland, Massachusetts, Sinauer Associates Inc.Google Scholar
Urban, M.C., Phillips, B.L., Skelly, D.K. & Shine, R. (2008) A toad more travelled: the heterogeneous invasion dynamics of cane toads in Australia. The American Naturalist 171, E134–E148.CrossRefGoogle ScholarPubMed
Välimaki, 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. Parasitology Research 107, 117–125.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Van den Bosch, F., Metz, J.A.J. & Diekmann, O. (1990) The velocity of spatial population expansion. Journal of Mathematical Biology 28, 529–565.CrossRefGoogle Scholar
Vander Wal, E., Paquet, P.C. & Andrés, J.A. (2012) Influence of landscape and social interactions on transmission of diseases in a social cervid. Molecular Ecology 21, 1271–1282.CrossRefGoogle Scholar
Von Brander, T. (1976) Massenauftreten der Hirschlausfliege Lipoptena cervi 1971 in Sudostfinnland; Mass outbreak of the deer hippoboscid Lipoptena cervi in 1971 in south-eastern Finland. Angewandte Parasitolologie 17, 168–169.Google Scholar
With, K.A. (2002) The landscape ecology of invasive spread. Conservation Biology 16, 1192–1203.CrossRefGoogle Scholar
Zoological Museum Finland (1988) Vuoden 1985 tulokset suomalaisen hyönteislajin levinneisyyskartoituksesta; Results of mapping the distribution of 21 species of insects in Finland in 1985. Notulae-Entomologicae 68, 9–24.Google Scholar
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