Odd Halvorsen

The role of parasites in the dynamics of a reindeer population

Even though theoretical models show that parasites may regulate host population densities, few empirical studies have given support to this hypothesis. We present experimental and observational evidence for a host–parasite interaction where the parasite has sufficient impact on host population dynamics for regulation to occur. During a six year study of the Svalbard reindeer and its parasitic gastrointestinal nematode Ostertagia gruehneri we found that anthelminthic treatment in April–May increased the probability of a reindeer having a calf in the next year, compared with untreated controls. However, treatment did not influence the over–winter survival of the reindeer. The annual variation in the degree to which parasites depressed fecundity was positively related to the abundance of O. gruehneri infection the previous October, which in turn was related to host density two years earlier. In addition to the treatment effect, there was a strong negative effect of winter precipitation on the probability of female reindeer having a calf. A simple matrix model was parameterized using estimates from our experimental and observational data. This model shows that the parasite–mediated effect on fecundity was sufficient to regulate reindeer densities around observed host densities.

Life-history strategies and population dynamics of abomasal nematodes in Svalbard reindeer ( Rangifer tarandus platyrhynchus )

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.

Congruent responses to weather variability in high arctic herbivores

Assessing the role of weather in the dynamics of wildlife populations is a pressing task in the face of rapid environmental change. Rodents and ruminants are abundant herbivore species in most Arctic ecosystems, many of which are experiencing particularly rapid climate change. Their different life-history characteristics, with the exception of their trophic position, suggest that they should show different responses to environmental variation. Here we show that the only mammalian herbivores on the Arctic islands of Svalbard, reindeer (Rangifer tarandus) and sibling voles (Microtus levis), exhibit strong synchrony in population parameters. This synchrony is due to rain-on-snow events that cause ground ice and demonstrates that climate impacts can be similarly integrated and expressed in species with highly contrasting life histories. The finding suggests that responses of wildlife populations to climate variability and change might be more consistent in Polar regions than elsewhere owing to the strength of the climate impact and the simplicity of the ecosystem.

Contrasting regulation of fecundity in two abomasal nematodes of Svalbard reindeer (Rangifer tarandus platyrhynchus)

Stability of trichostrogylid populations indicates that some form of density-dependent regulation occurs which could act through fecundity. We present evidence for intraspecific density-dependent effects in 1 of 2, dominant, abomasal nematodes species (Ostertagia gruehneri) of Svalbard reindeer (Rangifer tarandus platyrhynchus). We found evidence in O. gruehneri, for density-dependent regulation of female worm length in April, July and October 1999. However, it is only in July that female worm length explains the variation in the number of eggs in utero which is also related to egg production per female worm only in this month and not at other times of the year. The seasonal pattern in faecal egg output in this species focuses egg production in the summer months when conditions are favourable to transmission. In contrast, we found no evidence in the other common species (Marshallagia marshalli) for density-dependent regulation of female worm length during or the number of eggs in utero. Faecal egg output in M. marshalli was positively related to worm burden but not to the mean number of eggs in utero. Neither inter-specific interactions nor host body condition appeared to influence worm fecundity. The contrasting patterns of density-dependent regulation of fecundity provides further evidence for divergent life-histories in this nematode community.

On the relationship between social status of host and risk of parasitic infection

The observation that many parasites are transmitted in the food chain and that dominant host individuals take most of the food, lead to the hypothesis that there is a positive relationship between high status of host and risk of infection (contact) with such parasites. The hypothesis was tested in the field using reindeer and the nematode Elaphostrongylus rangiferi as a model system. In a reindeer herd with subclinical infections, the heaviest calves (i.e. the calves of dominant mothers) were those which were infected. This is in accordance with the hypothesis. This relationship between dominant hosts and parasites may lower the overall pathogenicity of the parasite relative to that which would be observed with random transmission. This would also result in increased suppression of host population growth, counteract inbreeding within the dominant segment of the population, and act as a mechanism of stabilizing selection.

Evidence for continued transmission of parasitic nematodes in reindeer during the Arctic winter

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.

Parasites, biodiversity, and population dynamics in an ecosystem in the high arctic

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 reindeers 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.

DNA evidence that Ostertagia gruehneri and Ostertagia arctica (Nematoda: Ostertagiinae) in reindeer from Norway and Svalbard are conspecific.

DNA sequences of ITS-1 and ITS-2 of rDNA were determined for 16 individual adult males each of Ostertagia gruehneri and Ostertagia arctica from Svalbard reindeer (Rangifer tarandus platyrhynchus) and Eurasian tundra reindeer (R. t. tarandus). Each ITS was virtually identical in O. gruehneri and O. arctica and the three mixed bases detected were shared by both species. Our results strongly suggest that O. gruehneri and O. arctica are dimorphic males of the same species.

Resistance to abomasal nematodes and individual genetic variability in reindeer

Resistance to parasites is believed to have a widespread influence on demographic and adaptive processes. In systems where parasites impose a fitness cost on their host, heterozygotes may be selected because they are more resistant to parasites than homozygotes. Our objective was to assess the relationships between genomewide individual heterozygosity and abomasal nematode burdens in female Svalbard reindeer (Rangifer tarandus platyrhynchus) after the effects of host age, locality, season, and year had been accounted for. Samples were obtained from 306 female reindeer that were culled and genotyped at nine microsatellite loci. Reindeer in our study populations are mainly parasitized by the gastrointestinal nematodes Ostertagia gruehneri and Marshallagia marshalli. The infection intensity of each parasite differed between subpopulations, and among host age classes, seasons and years. We found no significant relationships between abomasal worm burdens, or lumen and mucosa larvae, of either O. gruehneri or M. marshalli and individual heterozygosity (or mean d2) alone or in interactions with host age, locality, and year. Although we analysed one of the largest data set available to date on gastrointestinal nematodes of a wild ruminant, we used a typical data set of nine genetic neutral markers that may have had low power to detect heterozygosity–fitness correlations. We conclude that the proportion of the variance in parasite resistance explained by individual heterozygosity for neutral genetic markers is low in Svalbard reindeer and in vertebrates in general, and we suggest that the candidate‐gene approach might be more fruitful for further research on gene–fitness correlations.

Identification by polymerase chain reaction (PCR) of Marshallagia marshalli and Ostertagia gruehneri from Svalbard reindeer

A polymerase chain reaction (PCR) assay to identify two common abomasal nematodes Marshallagia marshalli and Ostertagia gruehneri of Svalbard reindeer was developed. Species-specific PCR primers were designed from internal transcribed spacer (ITS)-2 sequences of rDNA and validated using morphologically identified adult male and female nematodes. Using the species-specific primers, a 110 bp fragment was amplified from M. marshalli and its minor morph Marshallagia occidentalis and a 149 bp fragment was amplified from Ostertagia gruehneri and its minor morph Ostertagia arctica. No PCR products were amplified from the third rare species, Teladorsagia circumcincta, or DNA from the reindeer host. The assay provides a useful tool to estimate species composition for both sexes in this nematode community.