Climate change effects on terrestrial parasitic nematodes: Where are the knowledge gaps?

Climate change is expected to affect parasitic nematodes and hence possibly parasite-host dynamics and may have far-reaching consequences for animal health, livestock production, and ecosystem functioning. However, there has been no recent overview of current knowledge to identify how studies could contribute to a better understanding of terrestrial parasitic nematodes under changing climates. Here we screened almost 1,400 papers to review 57 experimental studies on the effects of temperature and moisture on hatching, development, survival, and behaviour of the free-living stages of terrestrial parasitic nematodes with a direct life cycle in birds and terrestrial mammals. Two major knowledge gaps are apparent. First, research should study the temperature dependency curves for hatching, development, and survival under various moisture treatments to test the interactive effect of temperature and moisture. Second, we specifically advocate for more studies that investigate how temperature, and its interaction with moisture, affect both vertical and horizontal movement of parasitic nematodes to understand infection risks. Overall, we advocate for more field experiments that test environmental effects on life-history traits and behaviour of parasitic nematodes in their free-living stages under natural and realistic circumstances. We also encourage studies to expand the range of used hosts and parasitic nematodes because 66% of results described in the available studies use sheep and cattle as hosts and 32% involve just three nematode species. This new comprehension brings attention to understudied abiotic impacts on terrestrial parasitic nematodes and will have broader implications for livestock management, wildlife conservation, and ecosystem functioning in a rapidly warming climate.

Age, sex, density, winter weather, and population crashes in Soay sheep.

Quantifying the impact of density, extrinsic climatic fluctuations, and demography on population fluctuations is a persistent challenge in ecology. We analyzed the effect of these processes on the irregular pattern of population crashes of Soay sheep on the St. Kilda archipelago, United Kingdom. Because the age and sex structure of the population fluctuates independently of population size, and because animals of different age and sex respond in different ways to density and weather, identical weather conditions can result in different dynamics in populations of equal size. In addition, the strength of density-dependent processes is a function of the distribution of weather events. Incorporating demographic heterogeneities into population models can influence dynamics and their response to climate change.

Is there a cost of parasites to caribou?

SUMMARY: Macroparasites potentially play a significant but often ignored role in the ecology and dynamics of wild ruminant populations. In the Arctic, parasites may impact on host populations by exacerbating the effects of seasonal and limited forage availability on the condition, fecundity and survival of individuals. We studied the effects of abomasal nematode parasites and warble flies, Hypoderma tarandi, on condition and pregnancy of caribou Rangifer tarandus in the Dolphin-Union herd, Nunavut, Canada. By the end of winter, female caribou over 2 years old showed a significant decrease in body weight with increasing nematode burden, and a decrease in back fat depth with increasing warble abundance. These effects were exaggerated in the non-pregnant fraction of the population. High warble larvae burdens were also associated with significantly reduced probability of being pregnant. Our research demonstrates a negative relationship between parasites and caribou condition that may have consequences for their fitness. Additionally, we discuss the possibility that muskox Ovibos moschatus share some parasite species with the caribou and could lead to elevated burdens in the sympatric host. Parasites may have been a contributory factor in a previous winter range-shift of the caribou herd and this may reflect a form of apparent competition between the two ungulate species.

Parasite-associated polymorphism in a cyclic ungulate population.

An unmanaged population of Soay sheep living on Hirta, St Kilda, Scotland is persistently unstable, fluctuating between about 600 and 1600 individuals. Population crashes occurring approximately every 3 years are primarily due to winter food shortage. In this paper we show that sheep experimentally relieved of their gastrointestinal nematodes (predominantly Teladorsagia spp.) survived a crash better than matched controls, showing that nematode parasites contribute to the probability that a sheep dies in a crash. We also show that over three successive crashes mortality was significantly different between individuals of the three different genotypes at the diallelic adenosine deaminase locus (Ada). FF animals were most likely to die, SS animals had an intermediate probability of dying, and FS animals were least likely to die. Finally, three independent lines of evidence suggest that nematode burdens differ between the three Ada genotypes. First, in August, heterozygous females are less likely to have nematode eggs in their faeces than homozygous females. Second, at lambing, the periparturient rise in faecal egg count was highest in homozygous FF individuals. Finally, during the Autumn mating season, heterozygous males has lower faecal egg counts than homozygotes, although this relation was complicated by interactions with year and age of male. These results are consistent with the idea that Ada allele frequencies are maintained in the sheep population by parasite-associated selection.

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.

Density-dependent selection in a fluctuating ungulate population.

Despite considerable theoretical interest no direct examples of density-dependent natural selection acting on simple polymorphic variation have been documented in a natural population. Here we show that the magnitude of selective differences in survival between phenotypes in two conspicuous polymorphisms of coat colour and horn type in Soay sheep Ovis aries living on St Kilda, Scotland are associated with marked changes in population density. Selection is strongest in years of high density but weak in years of low density. In addition to direct observations of density-dependent 'soft' selection in a natural population, the analysis revealed that the level of overcompensatory mortality (responsible for promoting population instability) was higher after accounting for genetic variation in the coat and horn morph traits. The results emphasize the importance of understanding the interaction between selection and population demography for both genetic and ecological studies of natural populations.

Microsatellites reveal heterosis in red deer.

The fitness consequences of inbreeding and outbreeding are poorly understood in natural populations. We explore two microsatellite-based variables, individual heterozygosity (likely to correlate with recent inbreeding) and a new individual-specific internal distance measure, mean d2 (focusing on events deeper in the pedigree), in relation to two measures of fitness expressed early in life, birth weight and neonatal survival, in 670 red deer calves (Cervus elaphus) born on the Isle of Rum between 1982 and 1996. For comparison, we also analyse inbreeding coefficients derived from pedigrees in which paternity was inferred by molecular methods. Only 14 out of 231 calves (6.1%) had non-zero inbreeding coefficients, and neither inbreeding coefficient nor individual heterozygosity was consistently related to birth weight or neonatal survival. However, mean d2 was consistently related to both fitness measures. Low mean d2 was associated with low birth weight, especially following cold Aprils, in which foetal growth is reduced. Low mean d2 was also associated with low neonatal survival, but this effect was probably mediated by birth weight because fitting birth weight to the neonatal survival model displaced mean d2 as an explanatory variable. We conclude that in the deer population fitness measures expressed early in life do not show evidence of inbreeding depression, but they do show evidence of heterosis, possibly as a result of population mixing. We also demonstrate the practical problems of estimating inbreeding via pedigrees compared with a direct marker-based estimate of individual heterozygosity. We suggest that, together, individual heterozygosity and mean d2, estimated using microsatellites, are useful tools for exploring inbreeding and outbreeding in natural population.

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.

The population dynamics of Ostertagia gruehneri in reindeer: a model for the seasonal and intensity dependent variation in nematode fecundity.

The gastrointestinal nematode Ostertagia gruehneri is a parasite of reindeer that can have a significant impact on host population dynamics. To gain a better understanding of the population dynamics of O. gruehneri, we parameterise a model for its fecundity that describes the observed seasonal and intensity dependent pattern of faecal egg counts well. The faecal egg count model is combined with a model for the seasonal faecal production rate of Svalbard reindeer to obtain quantitative estimates of the fecundity of O. gruehneri. The model is used to evaluate the relative contribution to pasture contamination of variation in the abundance of O. gruehneri and variation in reindeer densities. It is concluded that due to the intensity dependence in nematode fecundity, variation in reindeer population densities is likely to be the most important of these factors for pasture contamination.

Faecal avoidance and the risk of infection by nematodes in a natural population of reindeer.

We tested whether Svalbard reindeer (Rangifer tarandus platyrhynchus) minimise the risk of gastro- intestinal nematode infection by avoiding patches with a high density of faeces. This experiment was performed in preferred summer foraging habitat. The possibility that reindeer assess infection risk on the basis of faecal contamination levels across plant communities was determined by measuring the distribution of faeces in seven plant communities, and nematode developmental success in two plant communities with contrasting soil moisture content. We explored whether variation within individual reindeer in the levels of infection by gastro-intestinal nematodes was related to their diet. Reindeer avoided pastures where faecal contamination was increased, and thereby potentially reduced the risk of becoming infected by Trichostrongyle nematodes. Dung density was inversely related to soil moisture content, with high densities of faeces in dry plant communities and low densities in wet communities. However, nematode developmental success was positively related to soil moisture content, and was highest in the wetter sites. Thus, by avoiding dry areas with high dropping densities, reindeer would tend to feed in wetter areas where nematodes thrive. Therefore, dung density may be an unreliable predictor of the risk of infection. The absence of a strong relationship between an individual's infection level and its diet might be due to the unpredictability of pasture infection level.

Trading forage quality for quantity? Plant phenology and patch choice by Svalbard reindeer.

Plant phenology of Luzula heathland plots in Spitsbergen (78°N) was manipulated by adding or removing snow, which altered the time for plots (2 m×2 m; n=10) to become snow-free. A 2-week difference in snowmelt, equivalent to approximately one-sixth of the growing season, was achieved between advanced (first to be snow-free) and delayed (last to be snow-free) treatments, which influenced plant biomass and plant quality. Nitrogen content of the forage species decreased with time after snowmelt, whereas C:N ratio increased. Manipulation of snowmelt led to a shift in "phenological time", without altering these plant quality parameters as such. Early in the growing season, Svalbard reindeer (Rangifer tarandus platyrhynchus) selected the advanced plots which had been snow-free for longest, presumably because of the greater biomass of both Luzula confusa and Salix polaris, major components of reindeer diet at that time of the year. Moreover, the proportion of live Luzula leaves was highest in advanced plots, relative to both unmanipulated control and delayed plots. In contrast, plant quality, measured as nitrogen content and C:N ratio of leaves, was lowest in the preferred plots. Phenolic content did not differ among treatments, and is therefore unlikely to play a role in reindeer selection for plots with early snowmelt. Unlike in temperate regions, where selection for plant quality seems to be of major importance, selection for plant quantity might be an outcome of generally low levels of plant biomass and high forage quality during the growing season in the high Arctic. Reindeer selection for high plant biomass is likely to lead to a more favourable nitrogen and energy return than selection for high plant quality.

Comparison of plasma progesterone, transrectal ultrasound and pregnancy specific proteins (PSPB) used for pregnancy diagnosis in reindeer.

The study aimed to compare plasma progesterone concentrations, rectal ultrasonography and plasma concentrations of pregnancy-specific protein B (PSPB) used for pregnancy diagnosis in reindeer. A total of 1,595 blood plasma samples were collected between 1991 and 1996 from 3 semidomestic reindeer (Rangifer tarandus tarandus) herds on the Norwegian mainland (Magerøy, Sørøy, Filefjell) and from 92 wild Svalbard reindeer (Rangifer tarandus platyrhynchus). Samples were collected between January and late April. Plasma levels of progesterone and PSPB were measured and used as indicators of pregnancy. In addition, animals from the Filefjell herd and the Svalbard reindeer were investigated using transrectal ultrasound. The results showed that plasma progesterone lower than 7 nmol l-1 rarely occurs in females diagnosed pregnant either by ultrasound or by observing a calf at foot 7 months after blood sampling. A very good agreement was found between plasma progesterone and PSPB when used for pregnancy diagnosis. On the Norwegian mainland, but not to the same extent on Svalbard, a high proportion of females with a high progesterone concentration was diagnosed not pregnant by ultrasound. This probably reflects a high rate of false negative diagnoses by the ultrasound method rather than false positives in the progesterone analysis.

Low-level parasitic worm burdens may reduce body condition in free-ranging red deer (Cervus elaphus).

Regulation of ungulate populations by parasites relies on establishing a density-dependent relationship between infection and vital demographic rates which may act through the effect of parasites on body condition. We examine evidence for parasite impacts in 285 red deer (Cervus elaphus) harvested during 1991 and 1992 on the Isle of Rum. In the abomasa, prevalence of nematodes was 100% and the most abundant genus observed were Ostertagia species, however, mean intensity of infection was low (less than 1000) relative to other studies. Additional species, also present in low numbers, included Nematodirus spp., Capillaria spp., Cooperia spp., Monieza expanza, Oesophagostomum venulosum and Trichuris ovis. Lungworm (Dictyocaulus spp.) and tissue worm (Elaphostronygylus cervi) larvae were also observed in faecal samples. There was no evidence for acquired immunity to abomasal nematodes. Despite low levels of infection, both adult male and female deer showed significant negative correlation between indices of condition (kidney fat index, dressed carcass weight and larder weight) and intensity of Ostertagia spp. infection. However, there was no evidence that pregnancy rate in females was related to intensity of infection. For calves, there was no relationship between body condition and intensity of infection. The apparent subclinical effects of low-level parasite infection on red deer performance could alternatively be due to animals in poorer nutritional state being more susceptible to infection. Either way the results suggest that further studies of wild populations are justified, in particular where high local host densities exist or alternative ungulate hosts are present, and, where experimental treatments are tractable.

Sex ratio variation in gastrointestinal nematodes of Svalbard reindeer; density dependence and implications for estimates of species composition.

Estimates of the intensity and abundance of species provide essential data for ecological, evolutionary and epidemiological studies of gastrointestinal nematode communities. These estimates are typically derived from the species composition of adult males when only males have readily scorable species-specific morphological traits. Such estimation assumes that all species in the community have the same adult sex ratio. We evaluated this assumption for the trichostrongyle nematodes Ostertagia gruehneri and Marshallagia marshalli in infracommunities in Svalbard reindeer by identifying to species adult females using a polymerase chain reaction assay. The proportion of males was found to be slightly higher in O. gruehneri than in M. marshalli. Evidence for seasonal variation and density dependence in the adult sex ratio was only found for O. gruehneri. Possible demographic mechanisms for such sex ratio variation are discussed, and stochastic models that generate density-dependent sex ratios proposed. Sex ratio variation caused substantial bias in some male-based estimates of intensity of infection, while substantial and consistent bias in estimates of abundances was only evident in late winter samples. Our results suggest that estimating sex ratios can be particularly important in individual host level studies of nematode species of low abundance.

Blastocyst development and conceptus sex selection in red deer Cervus elaphus: studies of a free-living population on the Isle of Rum.

Skewing of the sex ratio at birth occurs in red deer in response to dominance status, with dominant hinds giving birth to a higher proportion of male calves than subordinates. To investigate the physiological basis for this phenomenon, reproductive tracts were collected from red deer during a cull for management purposes carried out on the Island of Rum, Scotland. Blastocysts were flushed from the uterus and sexed by polymerase chain reaction using Y chromosome-specific primers. Concentrations of interferon (measured as antiviral activity) in uterine flushings, of oxytocin receptors in endometrium, and of progesterone in jugular venous blood were measured, and ovarian morphology was recorded. Times of mating were determined retrospectively from calving dates observed during the following spring. Changes in uterine and fetal weights and sizes confirmed the degree of reproductive synchrony. Intervals between stages of blastocyst development (spherical, tubular, filamentous, and attached) derived from the observed incidence of each form showed that approximate times of blastocyst elongation and attachment were 13 and 30 days after conception, respectively. Hinds carrying male blastocysts were in better body condition (higher kidney fat weights, P = 0.025) than those carrying females. Interferon was detectable in uterine flushings from 1 of 7 hinds carrying early filamentous blastocysts and 5 of 12 hinds carrying late filamentous blastocysts, but in no case where the blastocysts were male (P = 0.035). Oxytocin receptor concentrations in caruncular endometrium (but not in intercaruncular endometrium) were lower in pregnant than in nonpregnant hinds (P < 0.05), but there was no correlation with interferon concentrations in flushings. Corpora luteal concentrations of oxytocin ranged from 1.8 to 51.2 micrograms/g tissue and declined with advancing blastocyst development. The data are consistent with the hypothesis that sexual dimorphism in trophoblast interferon production leads to differential blastocyst loss and hence to sex ratio skewing on the basis of dominance status.

Overcompensation and population cycles in an ungulate.

Although theoretical studies show that overcompensatory density-dependent mechanisms can potentially generate regular or chaotic fluctuations in animal numbers, the majority of realistic single-species models of invertebrate populations are not overcompensatory enough to cause sustained population cycles. The possibility that overcompensation may generate cycles or chaos in vertebrate populations has seldom been considered. Here we show that highly overcompensatng density-dependent mortality can generate recurrent population crashes consistent with those observed in a naturally limited population of Soay sheep. The observed interval of three or more years between crashes points to sharp 'focusing' of mortality over a narrow range of population density.

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.

Antler length of yearling red deer is determined by population density, weather and early life-history.

In red deer, yearling antler length is a largely nutrition-mediated phenotypic character, and is therefore sometimes used as an indirect estimate of range quality and population condition. However, the parameters affecting yearling antler length have been little studied. We analyse the contributions of density, weather and maternal effects on yearling antler length of 581 individual stags born 1970-1996 on the Isle of Rum (Scotland). We show that antler length is a good measure of yearling condition: the probability of overwinter survival in yearlings that developed antlers was 3 times higher than for yearlings that did not develop antlers, and yearling antler length was correlated with the number of antler points the following year. Between years, variation in yearling antler length was best explained by variation in red deer density and June temperature at 12 months of age. Both of these variables were negatively correlated with antler length, and most likely this effect is due to changes in nutrient availability. Population density affects biomass availability for the individual, while low temperatures in early summer prolong the availability of high forage quality. At the individual level, antler length increased with birth weight and decreased with birth date, reflecting the persistent and pervasive influence of conditions in early life.

Fitness costs of gestation and lactation in wild mammals.

Like a number of plants, some mammals commonly produce more progeny than they can afford to rear, terminating investment in some or even all of their offspring once the resources available for breeding are known. Adaptive interpretations of juvenile wastage rely on the argument that the costs of gestation are small compared to those of feeding offspring. Though energetic evidence supports this conclusion, it is unsafe to assume that the relative costs of gestation and lactation to the mother's survival and future reproductive success follow the same pattern because lactation commonly coincides with the period of maximum food availability. Controlling for individual variation, we show that in wild red deer (Cervus elaphus L) any costs of gestation to the mother's subsequent survival and reproductive success are slight compared to those of lactation.

COUNTERVAILING SELECTION IN DIFFERENT FITNESS COMPONENTS IN FEMALE RED DEER.

In individually monitored red deer (Cervus elaphus) living in the North Block of the Isle of Rhum, Scotland, juvenile survival is related to the genotype at the enzyme loci Mpi and Idh-2 (each with two alleles, f and s). To establish whether other fitness components also are related to genetic differences, we examined whether age at first breeding, fecundity, and adult survival of females were related to genotype at the same loci. Fertility in females shot outside the study area was also analyzed in relation to Mpi and Idh-2 genotype. The analyses controlled for phenotypic and environmental factors affecting female reproductive performance. At Mpi, f-carrying females in the study area bred earlier than ss individuals and tended to be more fecund. However, no association was found between Mpi genotype and adult survival. In culled females, Mpi f-carriers were more likely to be pregnant than ss females. At Idh-2, homozygous females in the study area started breeding earlier than heterozygous females. Idh-2 fs and ss females were more fecund than ff females though this relationship was complicated by an interaction with spring temperature in the year of birth. When the population was at high density, adult survival of Idh-2 ss females was better than survival of ff females, which was, in turn, better than survival of fs females. No association was found between Idh-2 genotype and fertility in culled females. Overall, the associations found in female reproductive measures favor those genotypes that survive particularly badly over the first two years of life. This result supports the idea that countervailing selection in different fitness components (antagonistic pleiotropy) is a common and powerful force maintaining polymorphism in natural populations. It may also explain how fitness components can have large heritabilities while overall fitness may have a low heritability.