Search

Parasitic nematodes are found in almost all wild vertebrate populations but few studies have investigated these host-parasite relationships in the wild. For parasites with free-living stages, the external environment has a major influence on life-history traits, and development and survival is generally low at sub-zero temperatures. For reindeer that inhabit the high Arctic archipelago of Svalbard, parasite transmission is expected to occur in the summer, due to the extreme environmental conditions and the reduced food intake by the host in winter. Here we show experimentally that, contrary to most parasitic nematodes, Marshallagia marshalli of Svalbard reindeer is transmitted during the Arctic winter. Winter transmission was demonstrated by removing parasites in the autumn, using a novel delayed-release anthelmintic bolus, and estimating re-infection rates in reindeer sampled in October, February and April. Larval stages of nematodes were identified using molecular tools, whereas adult stages were identified using microscopy. The abundance of M. marshalli adult worms and L4s increased significantly from October to April, indicating that reindeer were being infected with L3s from the pasture throughout the winter. To our knowledge, this study is the first to experimentally demonstrate over-winter transmission of a gastro-intestinal nematode parasite in a wild animal. Potential mechanisms associated with this unusual transmission strategy are discussed in light of our knowledge of the life-history traits of this parasite., (Copyright © 2012 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.)

The observation that the total abundance of adult nematodes in the abomasum of Svalbard reindeer increases between October and April suggests adaptation to cope with the Arctic winter. Here we investigate the extent to which selection has led to similar life-history strategies in the 3 most numerous trichostrongyle species. The life-histories are found to differ markedly. We use flexible statistical models for the abundance and dispersion of parasites in the host population. One of the taxa, Marshallagia marshalli, was most abundant and had its highest egg output in the winter. In contrast, the abundance of the most common taxa, Ostertagia gruehneri, m. gruehneri was stable or declined from autumn to late winter, and the closely related taxa, O. gruehneri, m. arcticus, showed a similar over winter drop. The faecal egg output of these 2 taxa was highest in summer, as found in temperate trichostrongyle species. Despite the apparent contamination of summer pastures with O. gruehneri, calves showed negligible burdens until their second summer and the abundance of infection reached an asymptote within their third year. In contrast, the abundance of M. marshalli in calves showed a rapid increase over the first summer and by late winter was similar to peak levels found in adults (8000 worms). This increase could not be accounted for by the developing abomasum larvae population and is therefore evidence for transmission over the winter for this taxa. While M. marshalli showed little between-year variation, O. gruehneri showed 2-fold fluctuation in the abundance of infection. O. gruehneri may therefore play a role in the fluctuating population dynamics of the host. Since there was no apparent decline in abundance with host age in any of the 3 taxa there was no evidence of reindeer mounting an immune response.

The abomasa of 163 Svalbard reindeers (Rangifer tarandus platyrhynchus) from Nordenskiöld Land, Spitsbergen (78 degrees N, 15 degrees E) were examined for adult and juvenile nematodes. Spitsbergen has midnight sun from late April to late August, arctic night from late October to mid-February, permafrost, and snow cover from October to June. Plant growth is restricted to 6-8 weeks, usually starting mid-June. In the reindeer calves, which are born in June prevalence and intensity of infection increased over the winter. All young (1 year) and adult (older than 1 year) reindeers were infected. Variations in worm burden, fraction of adult nematodes, male to female ratio in the nematodes, number of adult nematodes, number of juvenile nematodes, and distribution of juvenile nematodes on length groups were analysed for relationships with sex and age of host, and time of the year. The material was further analysed for relationships between the reindeer's content of stored fat and worm burden and its elements. It is concluded that transmission of nematodes to the reindeer continues over the winter and that arrested larval development has not been strongly selected for in this High Arctic locality. Infection continued to increase in adult males but not in adult females with age. This is explained as a balance between gain and loss of worms in the females connected to levelling off of food intake at end of somatic growth. In adult male reindeers there was a negative trend between stored fat and infection at all seasons. In reproducing females there were significant negative relationships in winter-spring, while in yeld females no significant relationship was found. The nematodes belonged to the following taxa: Ostertagia gruehneri m. gruehneri, O. gruehneri m. arcticus, Marshallagia marshalli m. marshalli, M. marshalli. m. occidentalis, Teladorsagia circumcincta m. circumcincta, T. circumcincta. m. trifurcata, and T. circumcincta. m. davtiani. There appears not to be any specially adapted species among the helminth parasites of reindeer (Rangifer tarandus) and muskoxen (Ovibos moschatus) in the High Arctic. In the Low Arctic Uminmakstrongylus pallikuukensis of muskoxen may be an example of such adaptation.

Living in the high Arctic, the Svalbard reindeer (Rangifer tarandus platyrhynchus) and its trichostrongyle nematodes experience a long cold winter from October to late May/early June. Over this period, transmission would be expected to be low. However, in culled reindeer the abundance of infection increased from autumn to late winter, providing evidence for continued transmission within this period. To our knowledge this is the first time this has been demonstrated in a climate with temperatures consistently below 0 degrees C. In one winter (1996-1997), the average fraction of nematodes found as larvae in the abomasal mucosa increased from around 10% to 50% between October and March. This suggests that arrested development took place throughout the winter. We found no evidence for an efficient acquired immune response towards the nematodes. The abundance of infection did not tend to decrease with increasing host age after an earlier peak, but levelled off instead, as predicted by a simple immigration-death model. In the late winter when the nutritional plane is low, both adult reindeer and calves had high worm burdens at intensities that may affect their condition and fitness.