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.     

Obligate larval inhibition of Ostertagia gruehneri in Rangifer tarandus? Causes and consequences in an Arctic system

SUMMARY Larval inhibition is a common strategy of Trichostrongylidae nematodes that may increase survival of larvae during unfavourable periods and concentrate egg production when conditions are favourable for development and transmission. We investigated the propensity for larval inhibition in a population of Ostertagia gruehneri, the most common gastrointestinal Trichostrongylidae nematode of Rangifer tarandus. Initial experimental infections of 4 reindeer with O. gruehneri sourced from the Bathurst caribou herd in Arctic Canada suggested that the propensity for larval inhibition was 100%. In the summer of 2009 we infected 12 additional reindeer with the F1 and F2 generations of O. gruehneri sourced from the previously infected reindeer to further investigate the propensity of larval inhibition. The reindeer were divided into 2 groups and half were infected before the summer solstice (17 June) and half were infected after the solstice (16 July). Reindeer did not shed eggs until March 2010, i.e. 8 and 9 months post-infection. These results suggest obligate larval inhibition for at least 1 population of O. gruehneri, a phenomenon that has not been conclusively shown for any other trichostrongylid species. Obligate inhibition is likely to be an adaptation to both the Arctic environment and to a migratory host and may influence the ability of O. gruehneri to adapt to climate change.     

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 d(2)) 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.     

Population Densities,Vegetation Green-Up,and Plant Productivity: Impacts on Reproductive Success and Juvenile Body Mass in Reindeer

Global warming is expected to cause earlier springs and increased primary productivity in the Arctic. These changes may improve food availability for Arctic herbivores, but may also have negative effects by generating a mismatch between the surge of high quality food in the spring and the timing of reproduction. We analyzed a 10 year dataset of satellite derived measures of vegetation green-up, population densities, calf body masses and female reproductive success in 19 reindeer (Rangifer tarandus) populations in Northern Norway. An early onset of spring and high peak plant productivity had positive effects on calf autumn body masses and female reproductive success. In addition, body masses and reproductive success were both negatively related to population density. The quantity of food available, as determined by the onset of vegetation green-up and plant productivity over the summer were the main drivers of body mass growth and reproductive success. We found no evidence for an effect of the speed of spring green-up. Nor did we detect a negative mismatch between early springs and subsequent recruitment. Effects of global warming on plant productivity and onset of spring is likely to positively affect sub-Arctic reindeer.     

Development and application of a delayed-release anthelmintic intra-ruminal bolus system for experimental manipulation of nematode worm burdens

In order to quantify the impact of parasites on host population dynamics, experimental manipulations that perturb the parasite-host relationship are needed but, logistically, this is difficult for wild hosts. Here, we describe the use of a delayed-release anthelmintic delivery system that can be administered when the hosts can be captured and its activity delayed until a more appropriate period in the host-parasite cycle. Our model system is Svalbard reindeer infected with a nematode parasite, Marshallagia marshalli, which appears to accumulate during the Arctic winter. To determine the extent to which this occurs and the effect on host fitness, reindeer need to be treated with anthelmintics in late autumn but they can only be caught and handled in April. To solve this problem, we devised an intra-ruminal capsule that releases the anthelmintic from up to 6 months after being administered. The capsule was trialed in cannulated sheep and red deer to determine optimum capsule orifice size and release rates. Capsules were estimated to release placebo for 100-153 days followed by abamectin for 22-34 days. To test the efficacy of treatment in reindeer, capsules were administered in April and retrieved in October. All capsules had fully released the anthelmintic and treated reindeer had significantly lower worm burdens than controls. Thus, success of this system allows repeated treatment over several years to test the effect of winter parasitism on host fitness.     

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.     

An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence

Epidemiological models predict a positive relationship between host population density and abundance of macroparasites. Here I lest these by a comparative study. I used data on communities of four groups of parasites inhabiting the gastrointestinal tract of mammals, nematodes of the orders Oxyurida. Ascarida. Enoplida and Spirurida. respectively. The data came from 44 mammalian species and represent examination of 16886 individual hosts. I studied average prevalence of all nematodes within an order in a host species, a measure of community level abundance, and considered the potential confounding effects of host body weight, fecundity, age at maturity and diet. Host population density was positively correlated with parasite prevalence within the order Oxyurida, where all species have direct life cycles. Considering the effects of other variables did not change this. This supports the assumption that parasite transmission rate generally is a positive function of host population density_: It also strengthens the hypothesis that host densities generally act as important determinants of species richness among directly transmitted parasites and suggests that negative influence of such parasites on host population growth rate increase with increasing host population density among host species. Within the other three nematode orders, where a substantial number of the species have indirect life cycles, no relationships between prevalence and host population density were seen, Again. considering the effects of other variables did not affect this conclusion. This suggests that host population density is a poor predictor of species richness of indirectly transmitted parasites and that effects of such parasites on host population dynamics do not scale with host densities among species of hosts.     

Do Svalbard reindeer regulate standing crop in the absence of predators?

The Svalbard reindeer is the only mammalian herbivore in Adventdalen (78°N), Svalbard, where it has no natural predators. To test if herbivores in the absence of predators regulate standing crop to a level independent of productivity, which is one of the predictions of the “exploitation ecosystems” model, herbivore exclosures were set up in 1992 in Salix heath, Luzula heath, Cassiope heath, and Alopecurus meadow in Adventdalen. Standing crop of vascular plants was harvested and measured inside and outside the exclosures in 1994, when the reindeer population was at peak density (ca 5.4 animals km⁻²), and in 1996, when the reindeer density was about 30% lower (ca 3.7 animals km⁻²). Standing dead material was reduced by grazing in the Luzula heath in 1994. However, we found no effect of grazing, year, or interactions between grazing and year on live standing crop. Also contrary to the predictions from the model, differences in standing crop between vegetation types were highly significant. Mean biomass of plant material was lowest in the Alopecurus meadow (36 g m⁻²), two fold higher in the Luzula heath, and about threefold higher in the Salix heath and Cassiope heath, indicating that reindeer do not regulate standing crop to the same level on a local scale. The predictive power of the “exploitation ecosystems” model is low due to lack of recognition of the importance of plant chemistry, plant compensation ability, variation in forage availability during the year, parasites functioning as predators, and adverse weather conditions, which may cause density-independent variations in fecundity and mortality of reindeer. Received: 28 December 1997 / Accepted: 6 April 1998     

蚜茧蜂产卵对寄主龄期的选择与其对蚜虫种群影响大小的计算机模拟研究

利用苦苣菜蚜-苦苣菜蚜茧蜂混合种群系统模拟模型,通过改变种群参数、初始虫量和温度条件,探讨了蚜茧蜂产卵选择寄主龄期特性对整个种群系统行为的影响,并比较了这一特性与蜂产卵量两者的相对重要性。结果表明,蜂产卵对寄主龄期选择特性的改变可明显改变其对蚜虫种群增长影响的程度,当产卵选择特性改变,产卵量在多数情况下必须要大幅度直至成倍的增减,才能补偿其对蚜虫种群的控制作用。不过,当蜂产卵嗜好三龄、二龄、四龄若蚜时(这在蚜茧蜂中较普遍),其作用和产卵无选择性时基本相似。     

Antibiotic treatment and post-handling survival of reindeer calves in Alaska

Free ranging reindeer (Rangifer tarandus tarandus) are driven into corral systems and handled each summer on the Seward Peninsula (Alaska, USA). During June and July of 1995-96 reindeer calves were inspected for injury, handled, weighed, and randomly treated with long-acting oxytetracycline. Calves that returned to subsequent handlings within the same year, received treatment only if they had been treated during their first handling. The effects of prophylactic antibiotic treatment and other factors, including weight, handling related injury, and sex on post-handling survival in reindeer calves were evaluated. Return rates of yearlings in 1996 and 1997 were analyzed using logistic regression. Weight change of calves between handlings was examined using a general linear model. Calf weight and handling injury were the only factors that significantly affected calf survival. No factor had a significant effect on calf weight change between handlings. Apparently, long-acting oxytetracycline was not an effective prophylactic treatment for this capture operation. The benefits of prophylactic antibiotic treatment have not been quantified and further studies of the effects and efficacy of prophylactic treatments are recommended. Ineffective treatments should be avoided because they may add additional stress to the captured animal. Managers should evaluate the potential effectiveness of a prophylactic treatment before indiscriminately applying one. Preventing calf injuries was the most effective method of reducing post-handling mortality in this study and should be given a high priority in the design of capture operations.     

Development and availability of the free-living stages of Ostertagia gruehneri, an abomasal parasite of barrenground caribou (Rangifer tarandus groenlandicus), on the Canadian tundra

Climate change in the Arctic is anticipated to alter the ecology of northern ecosystems, including the transmission dynamics of many parasite species. One parasite of concern is Ostertagia gruehneri, an abomasal nematode of Rangifer ssp. that causes reduced food intake, weight loss, and decreased pregnancy rates in reindeer. We investigated the development, availability, and overwinter survival of the free-living stages of O. gruehneri on the tundra. Fecal plots containing O. gruehneri eggs were established in the Northwest Territories, Canada under natural and artificially warmed conditions and sampled throughout the growing season of 2008 and the spring of 2009. Infective L3 were present 3-4 weeks post-establishment from all trials under both treatments, except for the trial established 4 July 2008 under warmed conditions wherein the first L3 was recovered 7 weeks post-establishment. These plots were exposed to significantly more time above 30°C than the natural plots established on the same date, suggesting a maximum temperature threshold for development. There was high overwinter survival of L2 and L3 across treatments and overwintering L2 appeared to develop to L3 the following spring. The impact of climate change on O. gruehneri is expected to be dynamic throughout the year with extreme maximum temperatures negatively impacting development rates.     

Effects of maternal parasite load on offspring life-history traits in the common lizard (Lacerta vivipara)

We studied the effect of maternal ectoparasite load (measured at parturition) on the life-history traits of the offspring of the host Lacerta vivipara, the European common lizard. The ectoparasite, a mite belonging to the family Laelapidae, had a detrimental effect on its host: parasite load was associated with increased host mortality, and was negatively correlated with host body mass. Parasite load was persistent over time, suggesting that parasite load can be predictable. Offspring of highly parasitised mothers had higher values of several fitness components early in life than offspring of parasite-free mothers or lightly infested mothers. This was expressed in terms of increased F₁ yearling growth rate, and reproductive investment at first reproduction (measured as F₂ hatchling mass). These results are interpreted as a host adaptation to attenuate the impact of parasites. Indeed, if high parasite loads arise from long exposure time to a constant population of parasites, and if the negative effects of parasites are additive over time, hosts could reduce the impact of parasites simply by investing more during the earlier stages of life. Naturally, having better performance early in life should lead to higher mortality rates and/or lower fecundity later in life.     

The role of helminths in the biological control of mammals

Biological control of invertebrates has been successful while that of vertebrates has been, with the exception of myxomatosis in rabbits, unsuccessful; reasons for this are discussed. Demographic studies of small mammals suggest that population regulation occurs by several different mechanisms, more than one of which may be acting at the same time. Coevolution is an important phenomenon in host-parasite associations, nevertheless parasites may limit host population abundance. The basis of the regulatory effect on the host population is that parasite-induced host mortality or reduction in fecundity is density-dependent. Increasing evidence of the density-dependent effects of helminths on host survival and reproduction is forthcoming from laboratory studies but has not been confirmed in the field. The theory that a helminth parasite may regulate mammal population abundance has been verified recently in the laboratory. A multidisciplinary research programme aimed at understanding the mechanisms responsible for formation of house mouse (Mus domesticus) plagues and seeking strategies to reduce mouse numbers is discussed. One aspect of the work involves investigation of the potential of the nematode, Capillaria hepatica, as a biological agent in the control of wild mice in the cereal-growing regions of Australia. Biological control of mammals is viewed within the context of integrated pest management. A helminth species which reduces host survival or fecundity at an increasing rate as host abundance increases has a role in host population regulation. There is potential to capitalize on that role and apply the helminth as a biological agent in the control of mammals which have attained pest status.     

Epidemic size determines population-level effects of fungal parasites on Daphnia hosts

Parasites frequently reduce the fecundity, growth, and survival of individual hosts. How often do these virulent effects reduce the density of host populations? Spectacular examples show that recently invaded parasites can severely impact host populations—but what about parasites persisting long-term in host populations? We have addressed this issue using a zooplankton host (Daphnia dentifera) that becomes infected with a fungal microparasite (Metschnikowia bicuspidata). We combined observations of epidemics in nine lakes over 6 years, fine-scale sampling of three epidemics, and a mesocosm experiment. Most epidemics remained small (<10% maximum prevalence) and exerted little influence on host densities. However, larger epidemics more severely depressed the populations of their hosts. These large/severe epidemics started and peaked earlier than smaller/benign ones. The larger epidemics also exerted particularly negative effects on host densities at certain lags, reflecting the delayed consequences of infection on fecundity reduction and host mortality. Notably, negative effects on the juvenile stage class manifested later than those on the adult stage class. The results of the experiment further emphasized depression of host density by the fungus, especially on the density of the juvenile stage class. Consequently, this common parasite reduces the density of host populations when conditions foster larger outbreaks characterized by an earlier start and earlier peak. Given these considerable effects on host density seen in a number of large epidemics, parasitism may sometimes rank highly among other factors (predation, resource availability) driving the population dynamics of these hosts.     

The ecology and phylogeny of oomycete infections in Asplanchna rotifers

1. Recently, the potential for parasites to influence the ecology and evolution of their zooplankton hosts has been the subject of increasing study. However, most research to date has focussed on Daphnia hosts, and the potential for parasites to influence other zooplankton taxa remains largely unstudied. 2. During routine sampling of zooplankton in a eutrophic lake, we observed that the rotifer Asplanchna girodi was often infected with a parasitic oomycete. Epidemics of this parasite occurred frequently, with three separate events in a single year. Prevalence at peak infection ranged from 29 to 41% and epidemics lasted from 17 to 56 days. Our data indicate that high densities of the host population are required for epidemics to occur. 3. Our morphological and molecular analyses suggest that this parasite is in the genus Pythium. Most Pythium spp. are plant pathogens, but our study supports recent work on Daphnia, suggesting that Pythium spp. are also important parasites of zooplankton. 4. As the parasite in this study was recalcitrant to cultivation, we developed an alternative method to verify its identity. Our approach used quantitative PCR to show that the ribosomal sequences identified increased with increasing density of infected hosts and, thus, were associated with the parasite. This approach should be generally applicable to other plankton parasites that are difficult to cultivate outside their hosts. 5. Infections significantly reduced host fecundity, lifespan and population growth rate. As a result of the virulence of this parasite, it is likely to influence the population ecology and evolution of its Asplanchna host, and may be a useful model system for studies on host–parasite coevolutionary dynamics.     

To eat or not to eat infected food: a bug’s dilemma

Parasites can adversely affect host population densities, but predators can regulate disease by reducing the density of susceptible hosts and consuming parasites contained in infected hosts. Some parasites induce phenotypic modifications in their hosts that potentially lead to increased predation. We investigated the role of parasite-induced modified appearance in the interactions between the crustacean Daphnia magna, its bacterial parasite Pasteuria ramosa, and its predator, the backswimmer Anisops sp. Our aim was to test the backswimmer’s prey preference between infected and uninfected D. magna to find out whether infection by P. ramosa can affect predation risk by Anisops. We found that Anisops sp. had a strong preference for uninfected D. magna under light, but under dark conditions the preference was reversed, which suggests that the modified appearance is the cause of this preference. Such anti-parasite preference by Anisops sp. could strongly influence host population dynamics as loss of fecundity, disease mortality, and predation are additive, resulting in host population decline.     

The influence of a parasite community on the dynamics of a host population: a longitudinal study on willow ptarmigan and their parasites

Despite the fact that most host populations are infected by a community of different parasite species, the majority of empirical studies have focused on the interaction between the host and a single parasite species. Here, we explore the hypothesis that host population dynamics are affected both by single parasite species and by the whole parasite community. We monitored population density and breeding productivity of two populations of willow ptarmigan ( Lagopus lagopus ) in northern Norway for 8 and 11 years, respectively, and sampled eukaryotic endoparasites. We found that increasing abundances of the cestode Hymenolepis microps was associated with increased breeding mortality and reduced annual growth rate of the host population in both areas, and reduced host body mass and body condition in the area where such data were available. In one of the areas, the abundance of the nematode Trichostrongylus tenuis was associated with reductions in host body mass, body condition and breeding mortality and the filaroid nematode Splendidofilaria papillocerca was negatively related to host population growth rates. The parasite community was also negatively related to host fitness parameters, suggesting an additional community effect on host body mass and breeding mortality, although none of the parasites had a significant impact on their own. The prevalence of parasites with very different taxonomical origins tended to covary within years, suggesting that variability in the parasite community was not random, but governed by changes in host susceptibility or environmental conditions that affected exposure to parasites in general. Other variables including climate, plant production and rodent densities were not associated with the recorded demographic changes in the host population.     

Infection success in novel hosts: an experimental and phylogenetic study of Drosophila-parasitic nematodes

Surprisingly little is known about what determines a parasite's host range, which is essential in enabling us to predict the fate of novel infections. In this study, we evaluate the importance of both host and parasite phylogeny in determining the ability of parasites to infect novel host species. Using experimental lab assays, we infected 24 taxonomically diverse species of Drosophila flies (Diptera: Drosophilidae) with five different nematode species (Tylenchida: Allantonematidae: Howardula, Parasitylenchus), and measured parasite infection success, growth, and effects on female host fecundity (i.e., virulence). These nematodes are obligate parasites of mushroom-feeding Drosophila, particularly quinaria and testacca group species, often with severe fitness consequences on their hosts. We show that the potential host ranges of the nematodes are much larger than their actual ranges, even for parasites with only one known host species in nature. Novel hosts that are distantly related from the native host are much less likely to be infected, but among more closely related hosts, there is much variation in susceptibility. Potential host ranges differ greatly between the related parasite species. All nematode species that successfully infected novel hosts produced infective juveniles in these hosts. Most novel infections did not result in significant reductions in the fecundity of female hosts, with one exception: the host specialist Parasitylenchus nearcticus sterilized all quinaria group hosts, only one of which is a host in nature. The large potential host ranges of these parasites, in combination with the high potential for host colonization due to shared mushroom breeding sites, explain the widespread host switching observed in comparisons of nematode and Drosophila phylogenies.     

Competing for blood: the ecology of parasite resource competition in human malaria–helminth co‐infections

Ecological theory suggests that co‐infecting parasite species can interact within hosts directly, via host immunity and/or via resource competition. In mice, competition for red blood cells (RBCs) between malaria and bloodsucking helminths can regulate malaria population dynamics, but the importance of RBC competition in human hosts was unknown. We analysed infection density (i.e. the concentration of parasites in infected hosts), from a 2‐year deworming study of over 4000 human subjects. After accounting for resource‐use differences among parasites, we find evidence of resource competition, priority effects and a competitive hierarchy within co‐infected individuals. For example reducing competition via deworming increased Plasmodium vivax densities 2.8‐fold, and this effect is limited to bloodsucking hookworms. Our ecological, resource‐based perspective sheds new light into decades of conflicting outcomes of malaria–helminth co‐infection studies with significant health and transmission consequences. Beyond blood, investigating within‐human resource competition may bring new insights for improving human health.