Skip to main content
SpringerLink
Log in

Adaptations to the Arctic: low-temperature development and cold tolerance in the free-living stages of a parasitic nematode from Svalbard

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

For nematodes with a direct life cycle, transmission is highly dependent on temperature-related development and survival of the free-living stages. Therefore, in the Arctic, where the winter lasts from October to May, nematode transmission is expected to be focused in the short summer season, yet there is strong evidence that as well as focussing egg output during winter months, the nematode parasite, Marshallagia marshalli, infects Svalbard reindeer during the Arctic winter when temperatures are persistently below freezing. To investigate the potential for development and survival of eggs and infective third-stage larvae in winter and therefore the possibility of for winter transmission, we ran a series of low-temperature laboratory experiments. These provide five key insights into the transmission and survival of the free-living stages of M. marshalli: (1) eggs hatched at temperatures as low as 2 °C, but not below 0 °C, (2) eggs were viable and developed after being exposed to sub-zero temperatures for up to 28 months, (3) infective-stage larvae survived for up to 80 days at 5 °C, (4) infective-stage larvae could survive rapid exposure to temperatures below −30 °C, and (5) desiccation resistance may be important for long-term larval survival at low temperatures. Together, these results indicate that eggs deposited during the winter are highly tolerant of prevailing environmental conditions and have the potential for rapid development with the onset of spring. It is therefore likely that the parasite remains in the egg stage in the faeces during the winter of deposition, hatch and develop into the infective larval stage in the summer, remaining viable on the tundra until the reindeer host returns to the winter feeding grounds the following winter.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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 Biol Sci 269(1500):1625–1632. doi:10.1098/rspb.2002.2064

    Article  CAS  Google Scholar 

  • Andersen FL, Levine ND (1968) Effect of desiccation on survival of free-living stages of Trichostrongylus colubriformis. J Parasitol 54(1):117–128. doi:10.2307/3276885

    Article  PubMed  CAS  Google Scholar 

  • Anderson R (1992) Nematode parasites of vertebrates: their development and transmission. C.A.B International, Cambridge

    Google Scholar 

  • Anderson R, May R (1978) Regulation and stability of host-parasite population interaction. I. Regulatory processes. J Anim Ecol 47:219–247

    Article  Google Scholar 

  • Ávila-Jiménez ML, Coulson SJ, Solhoy T, Sjoblom A (2010) Overwintering of terrestrial Arctic arthropods: the fauna of Svalbard now and in the future. Polar Res 29:127–137

    Article  Google Scholar 

  • Bale JS, Hayward SAL (2010) Insect overwintering in a changing climate. J Exp Biol 213(6):980–994. doi:10.1242/jeb.037911

    Article  PubMed  CAS  Google Scholar 

  • Carlsson AM, Justin Irvine R, Wilson K, Piertney SB, Halvorsen O, Coulson SJ, Stien A, Albon SD (2012) Disease transmission in an extreme environment: nematode parasites infect reindeer during the Arctic winter. Int J Parasitol 42(8):786–795

    Article  Google Scholar 

  • Coulson S, Hodkinson ID, Strathdee A, Bale JS, Block W, Worland MR, Webb NR (1993) Simulated climate change: the interaction between vegetation type and microhabitat temperature at Ny Alesund, Svalbard. Polar Biol 13(1):67–70

    Article  Google Scholar 

  • Coulson SJ, Hodkinson ID, Block W, Webb NR, Worland MR (1995a) Low summer temperatures: a potential mortality factor for high arctic soil microarthropods? J Insect Physiol 41(9):783–792. doi:10.1016/0022-1910(95)00027-r

    Article  CAS  Google Scholar 

  • Coulson SJ, Hodkinson ID, Strathdee AT, Block W, Webb NR, Bale JS, Worland MR (1995b) Thermal environments of Arctic soil organisms during winter. Arct Alp Res 27(4):364–370

    Article  Google Scholar 

  • Crossan J, Paterson S, Fenton A (2007) Host availability and the evolution of parasite life-history strategies. Evolution 61(3):675–684

    Article  PubMed  Google Scholar 

  • Dobson AP, Hudson PJ (1992) Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in Red grouse. II. Population models. J Anim Ecol 61(2):487–498

    Article  Google Scholar 

  • Halvorsen O, Bye K (1999) Parasites, biodiversity, and population dynamics in an ecosystem in the High Arctic. Vet Parasitol 84(3–4):205–227

    Article  PubMed  CAS  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. Int J Parasitol 29(4):567–579

    Article  PubMed  CAS  Google Scholar 

  • Hoar B, Rucksthul K, Kutz SJ (2012a) 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(8):1093–1100

    Article  PubMed  Google Scholar 

  • Hoar BM, Eberhardt AG, Kutz SJ (2012b) Obligate larval inhibition of Ostertagia gruehneri in Rangifer tarandus? Causes and consequences in an Arctic system. Parasitology I139(10):1339–1345

    Article  Google Scholar 

  • Hrabok JT, Oksanen A, Nieminen A, Waller PJ (2006) Population dynamics of nematode parasites of reindeer in the sub-arctic. Vet Parasitol 142(3–4):301–311. doi:10.1016/j.vetpar.2006.07.024

    Article  PubMed  CAS  Google Scholar 

  • Hudson PJ, Newborn D, Dobson AP (1992) Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in Red grouse. I. Monitoring and parasite reduction experiments. J Anim Ecol 61(2):477–486

    Article  Google Scholar 

  • Igrashev IK (1973) Helminths and helminthoses of the Karakul sheep. National academy of sciences of the Uzbekistan Soviet Socialist Republic, Institute of Zoology and Parasitology, Tashkent, Uzbekistan

  • Irvine RJ (2001) Contrasting life-history traits and population dynamics in two co-existing gastrointestinal nematodes of Svalbard reindeer. University of Stirling, Stirling

    Google Scholar 

  • Irvine RJ, Stien A, Halvorsen O, Langvatn R, Albon SD (2000) Life-history strategies and population dynamics of abomasal nematodes in Svalbard reindeer (Rangifer tarandus platyrhynchus). Parasitology 120(Pt 3):297–311

    Article  PubMed  Google Scholar 

  • Irvine RJ, Stien A, Dallas JF, Halvorsen O, Langvatn R, Albon SD (2001) Contrasting regulation of fecundity in two abomasal nematodes of Svalbard reindeer (Rangifer tarandus platyrhynchus). Parasitology 122(Pt 6):673–681

    PubMed  CAS  Google Scholar 

  • Jonsdottir IS (2005) Terrestrial ecosystems on Svalbard: heterogeneity, complexity and fragility from an Arctic Island perspective. Biology and Environment 105B (3, Sp. Iss. SI):155–165. doi:10.3318/bioe.2005.105.3.155

  • Kutz SJ, Ducrocq J, Verocai GG, Hoar BM, Colwell DD, Beckmen BB, Polley L, Elkin B, Hoberg EP (2012) Parasites in ungulates of Arctic North America and Greenland: a view of contemporary diversity, ecology and impact in a world under change. Adv Parasitol 79:99–252

    PubMed  Google Scholar 

  • Lee RE (2010) A primer on insect cold-tolerance. In: Denlinger DL, Lee RE (eds) Low temperature biology of insects. Cambridge University Press, New York, pp 3–34

    Chapter  Google Scholar 

  • Makovcova K, Jankovska I, Vadlejch J, Langrova I, Vejl P, Lytvynets A (2009) The contribution to the epidemiology of gastrointestinal nematodes of sheep with special focus on the survival of infective larvae in winter conditions. Parasitol Res 104(4):795–799. doi:10.1007/s00436-008-1258-z

    Article  PubMed  Google Scholar 

  • May R, Anderson R (1978) Regulation and stability of host-parasite population interaction. II. Destabalizing processes. J Anim Ecol 47:249–267

    Article  Google Scholar 

  • Morgan ER, Medley GF, Torgerson PR, Shaikenov BS, Milner-Gulland EJ (2007) Parasite transmission in a migratory multiple host system. Ecol Model 200(3–4):511–520. doi:10.1016/j.ecolmodel.2006.09.002

    Article  Google Scholar 

  • O′Connor LJ, Walkden-Brown SW, Kahn LP (2006) Ecology of the free-living stages of major trichostorngylid parasites of sheep. Vet Parasitol 14:1–15

    Article  Google Scholar 

  • Punsvik T, Syvertsen A, Staaland H (1979) Reindeer grazing in Advendalen, Svalbard. In: Reimers E, Gaare E, Skjenneberg S (eds) Proceedings of the second international reindeer/caribou symposium, Norway, pp 115–123

  • Sinclair BJ, Vernon P, Klok CJ, Chown SL (2003) Insects at low temperatures: an ecological perspective. Trends Ecol Evol 18(5):257–262. doi:10.1016/s0169-5347(03)00014-4

    Article  Google Scholar 

  • Slocombe JO (1974) Overwintering of bovine gastrointestinal nematodes in south western Ontario. Can J Comp Med Rev Can Med Comp 38(1):90–93

    CAS  Google Scholar 

  • Sommerville RI, Davey KG (2002) Diapause in parasitic nematodes: a review. Can J Zool Rev Can Zool 80:1817–1840

    Article  Google Scholar 

  • Sorensen GG, Holmstrup M (2011) Cryoprotective dehydration is widespread in Arctic springtails. J Insect Physiol 57(8):1147–1153

    Article  PubMed  Google Scholar 

  • Stien A, Irvine RJ, Langvatn R, Albon SD, Halvorsen O (2002) The population dynamics of Ostertagia gruehneri in reindeer: a model for the seasonal and intensity dependent variation in nematode fecundity. Int J Parasitol 32(8):991–996

    Article  PubMed  CAS  Google Scholar 

  • Stromberg BE (1998) Environmental factors influencing transmission. Vet Parasitol 72(3–4):247–264

    Google Scholar 

  • Tompkins D, Dobson A, Arneberg P, Begon M, Cattadori I, Greenman J, Heesterbeek J, Hudson P, Newborn D, Puliese A, Rizzoli A, Rosá R, Wilson K (2002) Parasites and host population dynamics. In: Hudson P (ed) The ecology of wildlife disease. Oxford University Press, New York, pp 45–62

    Google Scholar 

  • Troell K, Waller P, Hoglund J (2005) The development and overwintering survival of free-living larvae of Haemonchus contortus in Sweden. J Helminthol 79:373–379

    Article  PubMed  CAS  Google Scholar 

  • van Dijk J, Morgan ER (2008) The influence of temperature on the development, hatching and survival of Nematodirus battus larvae. Parasitology 135(2):269–283. doi:10.1017/s0031182007003812

    PubMed  Google Scholar 

  • van Dijk J, Morgan ER (2011) The influence of water on the migration of infective trichostrongyloid larvae onto grass. Parasitology 138(6):780–788. doi:10.1017/s0031182011000308

    Article  Google Scholar 

  • Wang HS, Kang L (2005) Effect of cooling rates on the cold hardiness and cryoprotectant profiles of locust eggs. Cryobiology 51(2):220–229

    Article  PubMed  CAS  Google Scholar 

  • Wharton DA (2003) The environmental physiology of Antarctic terrestrial nematodes: a review. J Comp Physiol B 173(8):621–628

    Article  PubMed  CAS  Google Scholar 

  • Wharton DA, Allan GS (1989) Cold tolerance mechanisms of the free-living stages of Trichostrongylus colubriformis (Nematoda). J Exp Biol 145:353–369

    PubMed  CAS  Google Scholar 

  • William SM, Margo PJ, Alan KA (eds) (2001) Parasitic diseases of wild mammals, 2nd edn. Iowa State University Press, Ames

    Google Scholar 

Download references

Acknowledgments

We thank Sysselmannen (Governor of Svalbard), Svalbard, for permission to carry out fieldwork. We are grateful to the logistics team at the University Centre of Svalbard for logistic support in the field, and the field teams for capturing the reindeer and collecting faecal samples, especially Steve Albon, Audun Stien, Leif Egil Loe, Erik Ropstad and Veibjorn Veiberg. We would also like to thank Fredrik Samuelsson for participation and help in initial laboratory trials. We are also grateful to Steve Albon for his assistance in editing the manuscript. This work was funded by the Macaulay Development Trust and a NERC-CASE studentship (NE/F01354x/1) awarded to K. Wilson, S.D. Albon, R.J. Irvine and S.J. Coulson.

Author information

Authors and Affiliations

  1. Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, UK

    A. M. Carlsson & K. Wilson

  2. The James Hutton Institute, Craigiebuckler, Aberdeen, AB15 8QH, Scotland, UK

    A. M. Carlsson & R. J. Irvine

  3. Department of Arctic Biology, University Centre in Svalbard, PO Box 156, 9171, Longyearbyen, Norway

    A. M. Carlsson & S. J. Coulson

Authors
  1. A. M. Carlsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. J. Irvine
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. J. Coulson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. M. Carlsson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carlsson, A.M., Irvine, R.J., Wilson, K. et al. Adaptations to the Arctic: low-temperature development and cold tolerance in the free-living stages of a parasitic nematode from Svalbard. Polar Biol 36, 997–1005 (2013). https://doi.org/10.1007/s00300-013-1323-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-013-1323-7

Keywords

Search

Navigation