Arne Skorping

Host densities as determinants of abundance in parasite communities

Several epidemiological models predict a positive relationship between host population density and abundance of directly transmitted macroparasites. Here, we generalize these, and test the prediction by a comparative study. We used data on communities of gastrointestinal strongylid nematodes from 19 mammalian species, representing examination of 6670 individual hosts. We studied both the average abundance of all strongylid nematodes within a host species, and the two components of abundance, prevalence and intensity. The effects of host body weight, diet, fecundity and age at maturity and parasite body size were controlled for directly, and the phylogenetically independent contrast method was used to control for confounding factors more generally. Host population density and average parasite abundance were strongly positively correlated within mammalian taxa, and across all species when the effects of host body weight were controlled for. Controlling for other variables did not change this. Even when looking at single parasite species occurring in several host species, abundance was highest in the host species with the highest population density. Prevalence and intensity showed similar patterns. These patterns provide the first macroecological evidence consistent with the prediction that transmission rates depend on host population density in natural parasite communities.

Empirical support for optimal virulence in a castrating parasite.

The trade-off hypothesis for the evolution of virulence predicts that parasite transmission stage production and host exploitation are balanced such that lifetime transmission success (LTS) is maximised. However, the experimental evidence for this prediction is weak, mainly because LTS, which indicates parasite fitness, has been difficult to measure. For castrating parasites, this simple model has been modified to take into account that parasites convert host reproductive resources into transmission stages. Parasites that kill the host too early will hardly benefit from these resources, while postponing the killing of the host results in diminished returns. As predicted from optimality models, a parasite inducing castration should therefore castrate early, but show intermediate levels of virulence, where virulence is measured as time to host killing. We studied virulence in an experimental system where a bacterial parasite castrates its host and produces spores that are not released until after host death. This permits estimating the LTS of the parasite, which can then be related to its virulence. We exposed replicate individual Daphnia magna (Crustacea) of one host clone to the same amount of bacterial spores and followed individuals until their death. We found that the parasite shows strong variation in the time to kill its host and that transmission stage production peaks at an intermediate level of virulence. A further experiment tested for the genetic basis of variation in virulence by comparing survival curves of daphniids infected with parasite spores obtained from early killing versus late killing infections. Hosts infected with early killer spores had a significantly higher death rate as compared to those infected with late killers, indicating that variation in time to death was at least in part caused by genetic differences among parasites. We speculate that the clear peak in lifetime reproductive success at intermediate killing times may be caused by the exceptionally strong physiological trade-off between host and parasite reproduction. This is the first experimental study to demonstrate that the production of propagules is highest at intermediate levels of virulence and that parasite genetic variability is available to drive the evolution of virulence in this system.

Life history covariation in intestinal nematodes of mammals

Using data on 66 species from 18 families and 6 orders, we examine patterns of interspecific covariation in female size, egg size, time from infection to production of infective stages (prepatency period), duration of reproduction (patency period), and fecundity in mammalian intestinal nematodes. Nematode species with shorter prepatency periods are smaller, have lower rates of somatic growth, lower fecundity and shorter reproductive periods; those with longer prepatency periods have the opposite suite of characters. These patterns are very different from that found in interspecific analyses of life history variation in other taxa. This may be a consequence of the energy-rich environment intestinal nematodes exploit, though comparable studies of free-living nematodes or other soft-bodied invertebrate phyla have not yet been done. The advantages of delaying reproduction, with the subsequent increase in fecundity and reproductive lifespan, depend on a number of factors, such as the relative importance of prepatency in the determination of parasite generation times, and adult mortality rates. Contrary to previous claims, nematode egg size is shown to be highly variable (as variable as female size), yet this variation is not associated with

Intensive Farming: Evolutionary Implications for Parasites and Pathogens

An increasing number of scientists have recently raised concerns about the threat posed by human intervention on the evolution of parasites and disease agents. New parasites (including pathogens) keep emerging and parasites which previously were considered to be ‘under control’ are re-emerging, sometimes in highly virulent forms. This re-emergence may be parasite evolution, driven by human activity, including ecological changes related to modern agricultural practices. Intensive farming creates conditions for parasite growth and transmission drastically different from what parasites experience in wild host populations and may therefore alter selection on various traits, such as life-history traits and virulence. Although recent epidemic outbreaks highlight the risks associated with intensive farming practices, most work has focused on reducing the short-term economic losses imposed by parasites, such as application of chemotherapy. Most of the research on parasite evolution has been conducted using laboratory model systems, often unrelated to economically important systems. Here, we review the possible evolutionary consequences of intensive farming by relating current knowledge of the evolution of parasite life-history and virulence with specific conditions experienced by parasites on farms. We show that intensive farming practices are likely to select for fast-growing, early-transmitted, and hence probably more virulent parasites. As an illustration, we consider the case of the fish farming industry, a branch of intensive farming which has dramatically expanded recently and present evidence that supports the idea that intensive farming conditions increase parasite virulence. We suggest that more studies should focus on the impact of intensive farming on parasite evolution in order to build currently lacking, but necessary bridges between academia and decision-makers.

Parasite Abundance, Body Size, Life Histories, and the Energetic Equivalence Rule

If common processes generate size‐abundance relationships among all animals, then similar patterns should be observed across groups with different ecologies, such as parasites and free‐living animals. We studied relationships among body size, life‐history traits, and population intensity (density in infected hosts) among nematodes parasitizing mammals. Parasite size and intensity were negatively correlated independently of all other parasite and host factors considered and regardless of type of analyses (i.e., nonphylogenetic or phylogenetically based statistical analyses, and across or within communities). No other nematode life‐history traits had independent effects on intensity. Slopes of size‐intensity relationships were consistently shallow, around −0.20 on log‐log scale, and thus inconsistent with the energetic equivalence rule. Within communities, slopes converged toward this global value as size range increased. A summary of published values suggests similar convergence toward a global value around −0.75 among free‐living animals. Steeper slopes of size‐abundance relationships among free‐living animals could be related to fundamental differences in ecologies between parasites and free‐living animals, although such generalizations require reexamination of size‐abundance relationships among free‐living animals with regard to confounding factors, in particular by use of phylogenetically based statistical methods. In any case, our analyses caution against simple generalizations about patterns of animal abundance.

The evolution of tissue migration by parasitic nematode larvae.

Migration by nematode larvae through the tissues of their mammalian hosts can cause considerable pathology, and yet the evolutionary factors responsible for this migratory behaviour are poorly understood. The behaviour is particularly paradoxical in genera such as Ascaris and Strongylus in which larvae undergo extensive migrations which begin and end in the same location. The orthodox explanation for this apparently pointless behaviour is that a tissue phase is a developmental requirement following the evolutionary loss of skin penetration or intermediate hosts. Yet tissue migration is not always necessary for development, and navigation and survival in an array of different habitats must require costly biochemical and morphological adaptations. Migrating larvae also risk becoming lost or killed by the host. Natural selection should therefore remove such behaviour unless there are compensating benefits. Here we propose that migration is a selectively advantageous life-history strategy. We show that taxa exploiting tissue habitats during development are, on average, bigger than their closest relatives that develop wholly in the gastrointestinal tract. Time to reproduction is the same, indicating that worms with a tissue phase during development grow faster. This previously unsuspected association between juvenile habitat and size is independent of any effects of adult habitat, life-cycle, or host size, generation time or diet. Because fecundity is intimately linked with size in nematodes, this provides an explanation for the maintenance of tissue migration by natural selection, analogous to the pre-spawning migrations of salmon.

Sexually Selected Color in Male Sticklebacks: A Signal of Both Parasite Exposure and Parasite Resistance?

Individual variation in parasite exposure is often overlooked in studies of the role of parasites in the evolution of mate choice. Here we outline how androgen and carotenoid dependent red breeding coloration might broadcast reliable information about parasite exposure and genetic resistance to common parasites in a population of male three-spined sticklebacks (Gasterosteus aculeatus). Copepods, which are important prey for sticklebacks contain carotenoids essential for development of breeding coloration, but are also intermediate hosts for common parasites of sticklebacks. Of the five parasite species found in 46 males, only those three transmitted through copepods show associations with intensity of red breeding coloration

Is population density a species character? Comparative analyses of the nematode parasites of mammals

An increasingly popular approach to the question of what determines population density is to compare the characteristics of common and rare species. However, if densities vary wildly between populations or through times or are poorly sampled, the search for species level traits may be fruitlesss and perhaps not even justified. For example, parasite densities have been considered too variable for comparative analyses. Here, we use repeatability analysis on data of 62 species of mammalian nematodes where population density of each species was measured in at least two different host populations, and analysed three measures of parasite density: intensity, abundance and prevalence (abundance = prevalence x intensity). About half of the variation in population intensity was found between parasite species rather than between populations within species. For abundance there were significant, but less pronounced differences between parasite species. Population intensity and abundance also differed significantly across the 25 host species sampled. For prevalences interpopulation variation within both parasite and host species may be too dominating for cross-species analyses to be fruitful. In line with this prevalence and intensity were only weakly correlated, and had different frequency distributions. Intensity followed a log-normal distribution across both population estimates and species means; population prevalence estimates were bimodally distributed, but species means were normally distributed. Thus, despite striking variation within species, differences in population intensity between mammalian nematode species are identifiable from literature surveys. suggesting that comparative studies may be important for understanding intensity variation. More generally, repeatability analyses may also guide meaningful comparisons of cross-species analyses made in different species assemblages.

Standard sampling techniques underestimate prevalence of avian hematozoa in willow ptarmigan (Lagopus lagopus)

A total of 68 willow ptarmigan (Lagopus lagopus L.) was collected during September 1995 from two localities in Troms County, northern Norway. Thin blood smears were prepared and examined for blood parasites. Of the 68 willow ptarmigan examined, 94% harbored one or more species of hematozoa. There were four (6%), 44 (65%), 16 (24%), and four (6%) birds infected by zero, one, two, and three species of parasites, respectively. Prevalences at the coastal locality, Kattfjord (n=43), were Leucocytozoon lovati 86%, Trypanosoma avium (26%), and microfilariae (30%). At the inland locality, Iselvdalen (n=25), prevalences were L. lovati 96%, T. avium 12%, and microfilariae 0%. We also searched connective tissues for the filaroid nematode Splendidofilaria papillocerca; in Kattfjord this parasite only occurred in adult hosts where prevalence was 94%, but the parasite was not found in Iselvdalen. To estimate the efficiency of parasite detection by standard blood sampling techniques, we sampled peripheral blood from the brachial wing vein and blood from the pulmonary system from willow ptarmigan. Sampling peripheral blood from the brachial vein led to underestimates of the prevalence of microfilariae. There was no significant difference between L. lovati and T. avium prevalence in blood collected from the brachial vein or deep circulation. Age of host had a strong impact on prevalence, especially for S. papillocerca and microfilariae.

ASPECTS OF THE LIFE CYCLE AND PATHOGENESIS OF ELAPHOSTRONGYLUS CERVI IN RED DEER (CERVUS ELAPHUS)

Aspects of the migratory life cycle and pathogenesis of Elaphostrongylus cervi were studied in red deer (Cervus elaphus) using 2 farmed calves experimentally infected with 450 third-stage larvae killed 40 and 45 days postinfection and using 3 wild calves and 3 wild yearlings with natural infections killed during autumn hunting. A full necropsy was carried out on the experimental calves, but only the head, eviscerated carcass, and lungs were examined from the naturally infected animals. Histological examination included extensive studies of the central nervous system (CNS), spinal nerve roots, and lungs. The experimental calves had prepatent infections, with many immature adult nematodes in the CNS, whereas the wild calves showed CNS lesions indicating a very recent E. cervi infection. The yearlings had patent infections, with many mature E. cervi in their skeletal muscles, reflecting acquisition of infection during the previous summer. Our findings showed that E. cervi develop to the adult stage in the CNS (subarachnoid spaces) and subsequently migrate into the skeletal muscles, where the mature nematodes live in reproductive pairs and groups. In the nervous system, the nematode caused encephalomyelitis, focal encephalomalacia and gliosis, meningitis, radiculitis, ganglionitis, and perineuritis.