Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-28T04:02:04.072Z Has data issue: false hasContentIssue false

Chapter Fourteen - Manipulating parasites in an Arctic herbivore: gastrointestinal nematodes and the population regulation of Svalbard reindeer

from Part II - Understanding between-host processes

Published online by Cambridge University Press:  28 October 2019

By
R. Justin Irvine ,
Steve D. Albon ,
Audun Stien ,
Odd Halvorsen  and
Anja M. Carlsson
Edited by
Kenneth Wilson ,
Andy Fenton  and
Dan Tompkins
Kenneth Wilson
Affiliation:
Lancaster University
Andy Fenton
Affiliation:
University of Liverpool
Dan Tompkins
Affiliation:
Predator Free 2050 Ltd
Get access

Summary

The main drivers of Svalbard reindeer population dynamics are likely to be limited food resources, periods of harsh winter weather and their abundant parasitic nematode infections. To show parasite demographic impact requires three approaches: field observation to document life history and abundances of parasites/hosts; manipulation of infection to quantify the effect of parasite intensity on host fitness; appropriate population models of density-dependent transmission. We monitored the reindeer population and intensity of parasites in culled reindeer, and treated a randomly selected reindeer group with an anthelmintic, comparing their fitness with a control group. The two main nematode species differed in life histories. Ostertagia gruehneri infected reindeer over the summer. Marshallagia marshalli transmission was limited to the harsh arctic winter. This implies that our treatment only affected O. gruehneri and showed that reindeer fecundity depends on intensity of O. gruehneri infection, which varied between years and was positively related to host population size. Modelling this interaction suggested a role for O. gruehneri in reindeer population regulation. More experiments with a delayed anthelmintic treatment, designed to manipulate M. marshalli numbers over the winter, provided little evidence of this parasite’s impact on host population dynamics.

Keywords

population regulationmacroparasitesfecunditySvalbard reindeerhost–parasite dynamicsexperimental nematode reductionparasite life history
Type
Chapter
Information
Wildlife Disease Ecology
Linking Theory to Data and Application
 , pp. 397 - 426
Publisher: Cambridge University Press
Print publication year: 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albon, S.D., Irvine, R.J., Halvorsen, O., et al. (2017) Contrasting effects of summer and winter warming on body mass explain population dynamics in a food-limited Arctic herbivore. Global Change Biology, 23, 1374–1389. doi:10.1111/gcb.13435Google Scholar
Albon, S.D., Stien, A., Irvine, R.J., et al. (2002) The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London B, 269, 1625–1632.CrossRefGoogle ScholarPubMed
Anderson, R.M. & May, R. M. (1978) Regulation and stability of host–parasite population interactions. I. Regulatory processes. Journal of Animal Ecology, 47, 219–247.Google Scholar
Armour, J. (1989) The influence of host immunity on the epidemiology of trichostrongyle infections in cattle. Veterinary Parasitology, 32, 5–19.CrossRefGoogle ScholarPubMed
Arneberg, P., Folstad, I. & Karter, A.J. (1996) Gastrointestinal nematodes depress food intake in naturally infected reindeer. Parasitology, 112, 213–219.CrossRefGoogle ScholarPubMed
Arneberg, P., Skorping, A., Grenfell, B. & Read, A.F. (1998) Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London B, 265, 1283–1289. DOI 10.1098/rspb.1998.0431CrossRefGoogle Scholar
Begon, M., Townsend, C.R. & Harper, J. (2005) Ecology: From Individuals to Ecosystems, 4th edition. Oxford: Wiley-Blackwell.Google Scholar
Bjørkvoll, E., Lee, A.M., Grøtan, V., et al. (2016) Demographic buffering of life histories? Implications of the choice of measurement scale. Ecology, 97, 40–47.Google Scholar
Boag, B. & Thomas, R.J. (1977) Epidemiological studies on gastro-intestinal nematode parasites of sheep: the seasonal number of generations and succession of species. Research in Veterinary Science, 22, 62–77.Google Scholar
Bye, K. (1987). Abomasal nematodes from three Norwegian wild reindeer populations. Canadian Journal of Zoology, 65, 677–680.CrossRefGoogle Scholar
Bye, K. & Halvorsen, O. (1983). Abomasal nematodes of the Svalbard reindeer (Rangifer tarandus platyrhynchus Vrolik). Journal of Wildlife Diseases, 19, 101–103.CrossRefGoogle ScholarPubMed
Bye, K., Halvorsen, O. & Nilssen, K. (1987) Immigration and regional distribution of abomasal nematodes of Svalbard reindeer. Journal of Biogeography, 14, 451–458.Google Scholar
Carlsson, A.M., Albon, S.D., Coulson, S.J., et al. (2018) Little impact of over-winter parasitism on a free-ranging ungulate in the high Arctic. Functional Ecology; 32, 1046–1056. https://doi.org/10.1111/1365–2435.13037Google Scholar
Carlsson, A.M., Irvine, R.J., Wilson, K., et al. (2012) Disease transmission in an extreme environment: nematode parasites infect reindeer during the Arctic winter. International Journal of Parasitology, 42,786–795. doi:10.1016/j.ijpara.2012.05.007.Google Scholar
Carlsson, A.M., Irvine, R.J., Wilson, K. & Coulson, S.J. (2013) Adaptations to the Arctic: low-temperature development and cold tolerance in the free-living stages of a parasitic nematode from Svalbard. Polar Biology, 36, 997–1005. doi:10.1007/s00300-013-1323-7.Google Scholar
Carlsson, A.M., Wilson, K. & Irvine, R.J. (2012) Development and application of a delayed-release anthelmintic intra-ruminal bolus system for experimental manipulation of nematode worm burdens. Parasitology, 139, 1086–1092.Google Scholar
Colditz, I.G., Watson, D.L., Gray, G.D. & Eady, S.J. (1996) Some relationships between age, immune responsiveness and resistance to parasites in ruminants. International Journal for Parasitology, 26, 869–877. doi:10.1016/S0020-7519(96)80058-0.Google Scholar
Coulson, T., Catchpole, E.A., Albon, S.D., et al. (2001) Age, sex, density, winter weather, and population crashes in Soay sheep. Science, 292, 1528–1531.Google Scholar
Crofton, H.D. (1957) Nematode parasite populations in sheep on lowland farms. III. The seasonal incidence of species. Parasitology, 47, 304–318.CrossRefGoogle ScholarPubMed
Crofton, H.D. (1963) Nematode parasite populations in sheep and on pasture. Technical Communication No. 35 of the Commonwealth Bureau of Helminthology. St Albans, UK.Google Scholar
Dallas, J.F., Irvine, R.J., Halvorsen, O. & Albon, S.D. (2000) Identification by polymerase chain reaction (PCR) of Marshallagia marshalli and Ostertagia gruehneri from Svalbard reindeer. International Journal of Parasitology, 30, 863–866.Google Scholar
Drózdz, J. (1965) Studies on helminths and helminthiases in Cervidae. I. Revision of the subfamily Ostertagiinae Sarwar, 1956 and an attempt to explain the phylogenesis of its representatives. Acta Parasitologica Polonica, 13, 445–481.Google Scholar
Drózdz, J. (1995) Polymorphism in the Ostertagiinae Lopez-Neyra, 1947 and comments on the systematics of these nematodes. Systematic Parasitology, 32, 91–99.Google Scholar
El-Azazy, O.M.E. (1995) Seasonal changes and inhibited development of the abomasal nematodes of sheep and goats in Saudi Arabia. Veterinary Parasitology, 58, 91–98.CrossRefGoogle ScholarPubMed
Forbes, A.B., Huckle, C.A., Gibb, M.J., Rook, A.J. & Nuthall, R. (2000) Evaluation of the effects of nematode parasitism on grazing behaviour, herbage intake and growth in young grazing cattle. Veterinary Parasitology, 90, 111–118.Google Scholar
Fox, M.T. (1997) Pathophysiology of infection with gastrointestinal nematodes in domestic ruminants: recent developments. Veterinary Parasitology, 72, 285–308.Google Scholar
Førland, E.J., Benestad, B., Hanssen-Bauer, I., Haugen, J.E. & Skaugen, T.E. (2011) Temperature and precipitation development at Svalbard 1900–2100. Advances in Meteorology, 2011, 893790. doi:10.1155/2012/893790.Google Scholar
Gjelten, H.J., Nordli, O., Isaksen, K., et al. (2016) Air temperature variations and gradients along the coast and fjords of western Spitsbergen. Polar Biology, 35, 29878. doi.org/10.3402/polar.v35.29878Google Scholar
Grenfell, B.T. (1988) Gastrointestinal nematode parasites and the stability and productivity of intensive ruminant grazing systems. Philosophical Transactions of the Royal Society of London B, 321, 541–563.Google Scholar
Grenfell, B.T. (1992) Parasitism and the dynamics of ungulate grazing systems. American Naturalist, 139, 907–929.Google Scholar
Grenfell, B.T., Wilson, K., Finkenstädt, B.F., et al. (1998) Noise and determinism in synchronized sheep dynamics. Nature, 394, 674–677.Google Scholar
Gulland, F.M.D. (1992) The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology, 105, 493–503.CrossRefGoogle ScholarPubMed
Halvorsen, O. & Bye, K. (1986). Parasitter i svalbardrein 1. Rundmark i lùpen [in Norwegian]. In: Øritsland, N.A. (ed.), Svalbardreinen og dens livsgrunnlag (pp. 120–133). Oslo: Universitetsforlaget.Google Scholar
Halvorsen, O. & Bye, K. (1999) Parasites, biodiversity, and population dynamics in an ecosystem in the High Arctic. Veterinary Parasitology, 84, 205–227.Google Scholar
Halvorsen, O., Stien, A., Irvine, J., Langvatn, R. & Albon, S. (1999) Evidence for continued transmission of parasitic nematodes in reindeer during the Arctic winter. International Journal of Parasitology, 29, 567–579.CrossRefGoogle ScholarPubMed
Hansen, B.B., Aanes, R., Herfindal, I., Kohler, J. & Sæther, B-E. (2011) Climate, icing, and wild arctic reindeer: past relationships and future prospects. Ecology, 92, 1917–1923.Google Scholar
Hansen, B.B., Aanes, R. & Sæther, B-E. (2010) Feeding-crater selection by High-arctic reindeer facing ice-blocked pastures. Canadian Journal of Zoology, 88, 170–177.Google Scholar
Hansen, B.B., Isaksen, K., Benestad, R.E., et al. (2014) Warmer and wetter winters: characteristics and implications of an extreme event in the High Arctic. Environmental Research Letters, 9, 114021. doi:10.1088/1748-9326/9/11/114021Google Scholar
Heinzmann, D., Barbour, A.D. & Torgerson, P.R. (2009) Compound processes as models for clumped parasite data. Mathematical Biosciences, 222(1), 27–35. DOI:10.1016/j.mbs.2009.08.007.Google Scholar
Hoar, B., Eberhardt, A. & Kutz, S. (2012a) Obligate larval inhibition of Ostertagia gruehneri in Rangifer tarandus? Causes and consequences in an Arctic system. Parasitology, 139, 1339–1345. doi:10.1017/S0031182012000601CrossRefGoogle Scholar
Hoar, B.M., Ruckstuhl, K. & Kutz, S. (2012b) Development and availability of the free-living stages of Ostertagia gruehneri, an abomasal parasite of barrenground caribou (Rangifer tarandus groenlandicus) on the Canadian tundra. Parasitology, 139, 1093–1100.Google Scholar
Hoberg, E.P., Galbreath, K.E., Cook, J.A., Kutz, S.J. & Polley, L. (2012) Northern host–parasite assemblages: history and biogeography on the borderlands of episodic climate and environmental transition. Advances in Parasitology, 79, 1–97.CrossRefGoogle ScholarPubMed
Hoberg, E.P., Kocan, A.A. & Richard, L.G. (2001) Gastrointestinal strongyles in wild ruminants. In: Samuel, W.M., Pybus, M.J. & Kocan, A.A. (eds.), Parasitic Diseases of Wild Mammals (pp. 193–227). London: Manson Publishing/Veterinary Press.Google Scholar
Hudson, P.J., Cattadori, I.M., Boag, B. & Dobson, A.P. (2006) Climate disruption and parasite–host dynamics: patterns and processes associated with warming and the frequency of extreme climatic events. Journal of Helminthology, 80, 175–182.Google Scholar
Hutchings, M.R., Kyriazakis, I., Papachristou, T.G., Gordon, I.J. & Jackson, F. (2000) The herbivores’ dilemma: trade-offs between nutrition and parasitism in foraging decisions. Oecologia, 124, 242–251.Google Scholar
Igrashev, I.K. (1973) Helminths and Helminthoses of the Karakul Sheep. Tashkent, Uzbekistan: National Academy of Sciences of the Uzbekistan Soviet Socialist Republic, Institute of Zoology and Parasitology.Google Scholar
Irvine, R.J. (2000) Use of moxidectin treatment in the investigation of abomasal nematodiasis in wild reindeer (Rangifer tarandus platyrhynchus). Veterinary Record, 147, 570–573.CrossRefGoogle ScholarPubMed
Irvine, R.J. (2001) Contrasting life-history traits and population dynamics in two co-existing gastrointestinal nematodes of Svalbard reindeer. PhD Thesis. University of Stirling, Stirling.Google Scholar
Irvine, R.J., Stien, A., Dallas, J.F., et al. (2001) Contrasting regulation of fecundity in two abomasal nematodes of Svalbard reindeer (Rangifer tarandus platyrhynchus). Parasitology, 122, 673–681.Google Scholar
Irvine, R.J., Stien, A., Halvorsen, O., Langvatn, R. & Albon, S.D. (2000) Life-history strategies and population dynamics of abomasal nematodes in Svalbard reindeer (Rangifer tarandus platyrhynchus). Parasitology, 120, 297–311.Google Scholar
Jolles, A.E. & Ezenwa, V.O. (2015) Ungulates as model systems for the study of disease processes in natural populations. Journal of Mammalogy, 96, 4–15.Google Scholar
Kattsov, V.M., Källén, E., Symon, C., Arris, L. & Hill, B. (2005) Future climate change: modeling and scenarios for the Arctic. In: Arctic Climate Impact Assessment (pp. 100–150). www.acia.uaf.eduGoogle Scholar
Kutz, S.J., Ducrocq, J., Verocai, G.G., et al. (2012) Parasites in ungulates of Arctic North America and Greenland: a view of contemporary diversity, ecology, and impact in a world under change. Advances in Parasitology, 79, 99–252.Google Scholar
Kutz, S.J., Hoberg, E.P., Polley, L. & Jenkins, E.J. (2005) Global warming is changing the dynamics of Arctic host–parasite systems. Proceedings of the Royal Society of London B, 272, 2571–2576. doi:10.1098/rspb.2005.3285Google Scholar
Kutz, S.J., Jenkins, E.J., Veitch, A.M., et al. (2009) The Arctic as a model for anticipating, preventing, and mitigating climate change impacts on host–parasite interactions. Veterinary Parasitology, 3, 217–228.CrossRefGoogle Scholar
Lebreton, J.-D., Burnham, K. P., Clobert, J. & Anderson, D. R. (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecological Monographs, 62, 67–118.Google Scholar
May, R.M. & Anderson, R.M. (1978) Regulation and stability of host–parasite population interactions. II. Destabilising processes. Journal of Animal Ecology, 47, 249–267.CrossRefGoogle Scholar
McCallum, H. (2000) Population Parameters. Oxford: Blackwell Science Ltd.Google Scholar
McCallum, H., Fenton, A., Hudson, P.J., et al. (2017) Breaking beta: deconstructing the parasite transmission function. Philosophical Transactions of the Royal Society of London Series B, 372, 20160084. doi:10.1098/rstb.2016.0084Google Scholar
Milner, J.M., Stien, A., Irvine, R.J., et al. (2003) Body condition in Svalbard reindeer and the use of blood parameters as indicators of condition and fitness. Canadian Journal of Zoology, 81, 1566–1578.Google Scholar
Morgan, E.R., Medley, G.F., Torgerson, P.R., Shaikenov, B.S. & Milner-Gulland, E.J. (2007) Parasite transmission in a migratory multiple host system. Ecological Modelling, 200, 511–520. doi:10.1016/j.ecolmodel.2006.09.002.Google Scholar
Morgan, E.R., Shaikenov, B., Torgerson, P.R., Medley, G.F. & Milner-Gulland, E.J. (2005) Helminths of Saiga antelope in Kazakhstan: implications for conservation and livestock production. Journal of Wildlife Diseases, 41, 149–162. https://doi.org/10.7589/0090-3558-41.1.149.Google Scholar
Murray, D.L., Cary, J.R. & Keith, L.B. (1997) Interactive effects of sublethal nematodes and nutritional status on snowshoe hare vulnerability to predation. Journal of Animal Ecology, 66, 250–264.Google Scholar
Omsjoe, E.H., Stien, A., Irvine, R.J., et al. (2009) Evaluating capture stress and its effect on reproductive success of Svalbard reindeer. Canadian Journal Zoology, 87, 73–85.Google Scholar
Pedersen, A.B. & Fenton, A. (2015) The role of antiparasite treatment experiments in assessing the impact of parasites on wildlife. Trends in Parasitology, 31, 200–211. 10.1016/j.pt.2015.02.004.Google Scholar
Pedersen, A.B. & Grieves, T. J. (2008) The interaction of parasites and resource cause crashes in a wild mouse population. Journal of Animal Ecology, 77, 370–377.Google Scholar
Redpath, S.M., Mougeot, F., Leckie, F.M., Elston, D.A. & Hudson, P. J. (2006) Testing the role of parasites in driving the cyclic population dynamics of a gamebird. Ecology Letters, 9, 410–418.Google Scholar
Reimers, E. (1977) Population dynamics of two subpopulations of reindeer in Svalbard. Arctic and Alpine Research, 9, 369–381.CrossRefGoogle Scholar
Reimers, E. (1982) Winter mortality and population trends of reindeer on Svalbard, Norway. Arctic and Alpine Research, 14, 295–300. doi:10.2307/1550792.Google Scholar
Reimers, E. & Ringberg, T. (1983) Seasonal changes in body weights of Svalbard reindeer from birth to maturity. Acta Zoologica Fennica, 175, 69–72.Google Scholar
Ropstad, E., Johansen, O., King, C., et al. (1999) Comparison of plasma progesterone, transrectal ultrasound and pregnancy specific proteins (PSPB) used for pregnancy diagnosis in reindeer. Acta Veterinaria Scandinavia, 40, 151–162.Google Scholar
Solberg, E.J., Jordhøy, P., Strand, O., et al. (2001) Effects of density-dependence and climate on the dynamics of a Svalbard reindeer population. Ecography, 24, 441–451.Google Scholar
Stien, A., Ims, R.A., Albon, S.D., et al. (2012) Congruent responses to weather variability in high arctic herbivores. Biology Letters, 8, 1002–1005.Google Scholar
Stien, A., Irvine, R.J., Langvatn, R., et al. (2002a) The impact of gastrointestinal nematodes on wild reindeer: experimental and cross-sectional studies. Journal of Animal Ecology, 71, 937–945.Google Scholar
Stien, A., Irvine, R.J., Langvatn, R., Albon, S.D. & Halvorsen, O. (2002b) The population dynamics of Ostertagia gruehneri in reindeer: a model for the seasonal and intensity dependent variation in nematode fecundity. International Journal of Parasitology, 32, 991–996.Google Scholar
Stien, A., Loe, L.E., Mysterud, A., et al. (2010) Icing events trigger range displacement in a high-arctic ungulate. Ecology, 91, 915–920.Google Scholar
Tompkins, D.M. & Begon, M. (1999) Parasites can regulate wildlife populations. Parasitology Today, 15, 311–313.Google Scholar
Tompkins, D.M., Dobson, A.P., Arneberg, P., et al. (2002) Parasites and host population dynamics. In: Hudson, P., Rizzoli, A., Grenfell, B., Heesterbeek, H. & Dobson, A. (eds.), The Ecology of Wildlife Diseases (pp. 45–62). New York, NY: Oxford University Press.Google Scholar
Tompkins, D.M., Dunn, A. M., Smith, M. J. & Telfer, S. (2011) Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology, 80, 19–38.Google Scholar
Townsend, S.E., Newey, S., Thirgood, S.J., Matthews, L. & Haydon, D.T. (2009) Can parasites drive population cycles in mountain hares? Proceedings of the Royal Society of London B, 276, 1611–1617. doi:10.1098/rspb.2008.1669.Google Scholar
Tyler, N.J.C. (1987) Natural limitation of the abundance of the high Arctic Svalbard reindeer. PhD thesis, University of Cambridge.Google Scholar
Tyler, N.J.C., Forchhammer, M.C. & Øritsland, N.A. (2008) Nonlinear effects of climate and density in the dynamics of a fluctuating population of reindeer. Ecology, 98, 1675–1686.Google Scholar
Tyler, N. & Øritsland, N.A. (1989) Why don’t Svalbard reindeer migrate? Holarctic Ecology, 12, 369–376.Google Scholar
Tyler, N. & Øritsland, N.A. (1999) Varig ustabilitet og bestandsregulering hos Svalbardrein (in Norwegian). In: Bengtson, S.A., Mehlum, F. & Severinsen, T. (eds.), Svalbardtundraens økologi (pp. 139–147). Tromsø: Norsk Polarinstituttmdelelser nr. 150.Google Scholar
Vandergrift, K.J., Raffel, T.R. & Hudson, P.J. (2008) Parasites prevent summer breeding in white-footed mice, Peromyscus leucopus. Ecology, 89, 2251–2258.Google Scholar
Van der Wal, R. & Stien, A. (2014) High-arctic plants like it hot: a long-term investigation of between-year variability in plant biomass. Ecology, 95, 3414–3427.CrossRefGoogle Scholar
Wegener, C. & Odasz-Albrigtsen, A.M. (1998) Do Svalbard reindeer regulate standing crop in the absence of predators? A test of the “exploitation ecosystems” model. Oecologia, 116, 202–206.Google Scholar
White, G.C. & Burnham, K.P. (1999) Program Mark: survival estimation from populations of marked animals. Bird Study, 46, S120–S139.Google Scholar
Wilson, K. & Grenfell, B.T. (1997) Generalised linear modelling for parasitologists. Parasitology Today, 13, 33–38.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×