From individual heterogeneity to population-level overdispersion: quantifying the relative roles of host exposure and parasite establishment in driving aggregated helminth distributions

In most host-parasite systems, variation in parasite burden among hosts drives transmission dynamics. Heavily infected individuals introduce disproportionate numbers of infective stages into host populations or surrounding environments, causing sharp increases in frequency of infection. Parasite aggregation within host populations may result from variation among hosts in exposure to infective propagules and probability of subsequent establishment of parasites in the host. This is because individual host heterogeneities contribute to a pattern of parasite overdispersion that emerges at the population level. We quantified relative roles of host exposure and parasite establishment in producing variation in parasite burdens, to predict which hosts are more likely to bear heavy burdens, using big brown bats (Eptesicus fuscus) and their helminths as a model system. We captured bats from seven colonies in Michigan and Indiana, USA, assessed their helminth burdens, and collected data on intrinsic and extrinsic variables related to exposure, establishment, or both. Digenetic trematodes had the highest prevalence and mean abundance while cestodes and nematodes had much lower prevalence and mean abundance. Structural equation modeling revealed that best-fitting models to explain variations in parasite burden included genetic heterozygosity and immunocompetence as well as distance to the nearest water source and the year of host capture. Thus, both differential host exposure and differential parasite establishment significantly influence heterogeneous helminth burdens, thus driving population-level patterns of parasite aggregation.     

Microparasite transmission to <Emphasis Type="Italic">Daphnia magna</Emphasis> decreases in the presence of conspecifics

Single parasite species often have a range of different hosts which vary in their ability to sustain the parasite. When foraging for food, alternative hosts with similar feeding modes may compete for the infective stages of trophically transmitted parasites. If some of the infective stages end up in unsuitable hosts, transmission of the parasite to the focal host is decreased. I studied whether the presence of conspecifics alters the probability of an uninfected susceptible recipient Daphnia becoming infected by a microparasite and if this effect depends on whether the added conspecifics themselves are susceptible or resistant to infection. The presence of both susceptible and resistant conspecifics decreased the probability of infection in recipients. This effect was dependent on the density of the conspecifics but was not found to be related to their size. In addition, when Daphnia were placed in medium derived from crowded Daphnia populations, the probability of infection in recipients decreased as compared to that in standard medium. This implies that decreases in transmission probability are not caused by dilution of spores through food competition only, but also by indirect interference mediated through infochemicals released by Daphnia. Since Daphnia have been found to respond to crowding by decreasing their filtering rate, the decrease in transmission is probably caused by decreased intake of spores in crowded conditions. The presence of conspecifics can thus decrease microparasite transmission in Daphnia which may have important consequences for epidemiology and evolution of Daphnia parasites.     

Geographic variation in life cycle strategies of a progenetic trematode

Numerous parasite species have evolved complex life cycles with multiple, subsequent hosts. In trematodes, each transmission event in multi-host life cycles selects for various adaptations, one of which is facultative life cycle abbreviation. This typically occurs through progenesis, i.e., precocious maturity and reproduction via self-fertilization within the second intermediate host. Progenesis eliminates the need for the definitive host and facilitates life cycle completion. Adopting a progenetic cycle may be a conditional strategy in response to environmental cues related to low probability of transmission to the definitive host. Here, the effects of environmental factors on the reproductive strategy of the progenetic trematode Stegodexamene anguillae were investigated using comparisons among populations. In the 3-host life cycle, S. anguillae sexually reproduces within eel definitive hosts, whereas in the progenetic life cycle, S. anguillae reproduces by selfing within the metacercaria cyst in tissues of small fish intermediate hosts. Geographic variation was found in the frequency of progenesis, independent of eel abundance. Progenesis was affected by abundance and length of the second intermediate fish host as well as encystment site within the host. The present study is the first to compare life cycle strategies among parasite populations, providing insight into the often unrecognized plasticity in parasite developmental strategies and transmission.     

Parasitic worms: strategies of host finding, recognition and invasion

Many parasitic worms enter their hosts by active invasion. Their transmission success is often based on a mass production of invasive stages. However, most stages show a highly specific host-finding behaviour. Information on host-finding mechanisms is available mainly for trematode miracidia and cercariae and for nematode hookworms. The larvae find and recognise their hosts, in some cases even with species specificity, via complex sequences of behavioural patterns with which they successively respond to various environmental and host cues. There is often a surprisingly high diversity of host-recognition strategies. Each parasite species finds and enters its host using a different series of cues. For example, different species of schistosomes enter the human skin using different recognition sequences. The various recognition strategies may reflect adaptations to distinct ecological conditions of transmission. Another question is how, after invasion, parasitic worms find their complex paths through their host's tissues to their often very specific microhabitats. Recent data show that the migrating parasite stages can follow local chemical gradients of skin and blood compounds, but their long-distance navigation within the host body still remains puzzling.

The high complexity, specificity and diversity of host-recognition strategies suggest that host finding and host recognition are important determinants in the evolution of parasite life cycles.     

Parasite-induced alteration of plastic response to predation threat: increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis

Larvae of many trophically-transmitted parasites alter the behaviour of their intermediate host in ways that increase their probability of transmission to the next host in their life cycle. Before reaching a stage that is infective to the next host, parasite larvae may develop through several larval stages in the intermediate host that are not infective to the definitive host. Early predation at these stages results in parasite death, and it has recently been shown that non-infective larvae of some helminths decrease such risk by enhancing the anti-predator defences of the host, including decreased activity and increased sheltering. However, these behavioural changes may divert infected hosts from an optimal balance between survival and foraging (either seeking food or a mate). In this study, this hypothesis was tested using the intermediate host of the acanthocephalan parasite Pomphorhynchus laevis, the freshwater amphipod Gammarus pulex. We compared activity, refuge use, food foraging and food intake of hosts experimentally infected with the non-infective stage (acanthella), with that of uninfected gammarids. Behavioural assays were conducted in four situations varying in predation risk and in food accessibility. Acanthella-infected amphipods showed an increase in refuge use and a general reduction in activity and food intake. There was no effect of parasite intensity on these traits. Uninfected individuals showed plastic responses to water-borne cues from fish by adjusting refuge use, activity and food intake. They also foraged more when the food was placed outside the refuge. At the intra-individual level, refuge use and food intake were positively correlated in infected gammarids only. Overall, our findings suggest that uninfected gammarids exhibit risk-sensitive behaviour including increased food intake under predation risk, whereas gammarids infected with the non-infective larvae of P. laevis exhibit a lower motivation to feed, irrespective of predation risk and food accessibility.     

Avian cestodes affect the behaviour of their intermediate host Artemia parthenogenetica: an experimental study

The brine shrimp Artemia parthenogenetica (Crustacea, Branchiopoda) is intermediate host for several cestode species whose final hosts are waterbirds. Previous field studies have shown that brine shrimps infected with cestodes have a bright red colour and are spatially segregated in the water column. However, the ethological mechanisms explaining such field observations are unknown. Changes in appearance and behaviour induced by trophically transmitted parasites have been shown to increase the risk of predation by the final host. In this experimental study, we compared the behaviour of uninfected Artemia and those infected by avian cestodes. We found that parasitised individuals behave differently from unparasitised ones in several ways. In contrast to uninfected individuals, infected brine shrimps were photophilous and showed increased surface-swimming behaviour. These observations suggest that the modified behaviour (in addition to the bright red colour of the majority of the infected individuals) results in infected brine shrimps becoming more vulnerable to avian final hosts, which facilitates parasite transmission. We discuss our results in terms of the adaptive nature of behavioural changes and their potential implications for the hypersaline ecosystem.     

Life history and virulence are linked in the ectoparasitic salmon louse Lepeophtheirus salmonis

Models of virulence evolution for horizontally transmitted parasites often assume that transmission rate (the probability that an infected host infects a susceptible host) and virulence (the increase in host mortality due to infection) are positively correlated, because higher rates of production of propagules may cause more damages to the host. However, empirical support for this assumption is scant and limited to microparasites. To fill this gap, we explored the relationships between parasite life history and virulence in the salmon louse, Lepeophtheirus salmonis, a horizontally transmitted copepod ectoparasite on Atlantic salmon Salmo salar. In the laboratory, we infected juvenile salmon hosts with equal doses of infective L. salmonis larvae and monitored parasite age at first reproduction, parasite fecundity, area of damage caused on the skin of the host, and host weight and length gain. We found that earlier onset of parasite reproduction was associated with higher parasite fecundity. Moreover, higher parasite fecundity (a proxy for transmission rate, as infection probability increases with higher numbers of parasite larvae released to the water) was associated with lower host weight gain (correlated with lower survival in juvenile salmon), supporting the presence of a virulence–transmission trade‐off. Our results are relevant in the context of increasing intensive farming, where frequent anti‐parasite drug use and increased host density may have selected for faster production of parasite transmission stages, via earlier reproduction and increased early fecundity. Our study highlights that salmon lice, therefore, are a good model for studying how human activity may affect the evolution of parasite virulence.     

The role of host traits, season and group size on parasite burdens in a cooperative mammal

The distribution of parasites among hosts is often characterised by a high degree of heterogeneity with a small number of hosts harbouring the majority of parasites. Such patterns of aggregation have been linked to variation in host exposure and susceptibility as well as parasite traits and environmental factors. Host exposure and susceptibility may differ with sexes, reproductive effort and group size. Furthermore, environmental factors may affect both the host and parasite directly and contribute to temporal heterogeneities in parasite loads. We investigated the contributions of host and parasite traits as well as season on parasite loads in highveld mole-rats (Cryptomys hottentotus pretoriae). This cooperative breeder exhibits a reproductive division of labour and animals live in colonies of varying sizes that procreate seasonally. Mole-rats were parasitised by lice, mites, cestodes and nematodes with mites (Androlaelaps sp.) and cestodes (Mathevotaenia sp.) being the dominant ecto- and endoparasites, respectively. Sex and reproductive status contributed little to the observed parasite prevalence and abundances possibly as a result of the shared burrow system. Clear seasonal patterns of parasite prevalence and abundance emerged with peaks in summer for mites and in winter for cestodes. Group size correlated negatively with mite abundance while it had no effect on cestode burdens and group membership affected infestation with both parasites. We propose that the mode of transmission as well as social factors constrain parasite propagation generating parasite patterns deviating from those commonly predicted.     

Inter- and intraspecific conflicts between parasites over host manipulation

Host manipulation is a common strategy by which parasites alter the behaviour of their host to enhance their own fitness. In nature, hosts are usually infected by multiple parasites. This can result in a conflict over host manipulation. Studies of such a conflict in experimentally infected hosts are rare. The cestode Schistocephalus solidus (S) and the nematode Camallanus lacustris (C) use copepods as their first intermediate host. They need to grow for some time inside this host before they are infective and ready to be trophically transmitted to their subsequent fish host. Accordingly, not yet infective parasites manipulate to suppress predation. Infective ones manipulate to enhance predation. We experimentally infected laboratory-bred copepods in a manner that resulted in copepods harbouring (i) an infective C plus a not yet infective C or S, or (ii) an infective S plus a not yet infective C. An infective C completely sabotaged host manipulation by any not yet infective parasite. An infective S partially reduced host manipulation by a not yet infective C. We hence show experimentally that a parasite can reduce or even sabotage host manipulation exerted by a parasite from a different species.     

Life cycle truncation in a trematode: does higher temperature indicate shorter host longevity?

The typical three-host life cycle of most trematodes creates transmission challenges for which a variety of adaptations have evolved to increase the probability of transmission. Some species can abbreviate their life cycle via progenesis, the precocious maturation of the parasite in the second intermediate host resulting in the production of eggs through self-fertilisation without requiring a definitive host. Adoption of the progenetic life cycle may be a conditional strategy in response to different environmental cues related to low probability of transmission to the definitive host. Using high water temperature and/or limited diet as experimental stressors, we tested the effect of body condition and life span of the fish second intermediate host on facultative truncation of the typical three-host life cycle by progenesis in Stegodexamene anguillae. The results suggest that environmental cues, such as temperature and encystment site, may signal transmission opportunities to the parasite so that it may adjust its developmental strategy accordingly. Indeed, a greater proportion of worms became progenetic at higher temperatures, and progenesis was more common among worms encysted in the gonads or body cavity of their fish hosts than among those in other host tissues. These findings highlight the often unrecognised plasticity in parasite developmental and transmission strategies.     

Phylogenetic inference from platyhelminth life-cycle stages

Studies of the life cycle stages of digeneans and oncophoreans (= monogeneans and cestodes) indicate that these two groups had separate origins from free-living rhabdocoel-like ancestors and that the original single-host life cycles became 2-host cycles through accidental ingestion, in digeneans by free-swimming adults being ingested by vertebrates, and in cestodes by eggs being ingested by invertebrates. In both lines a third host was incorporated as a means of increasing the efficiency of transfer between hosts, in digeneans between the primary mollusc and the secondary vertebrate, and in cestodes between the secondary (“first intermediate”) host and the primary vertebrate host.     

Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans

Several parasite species have the ability to modify their host's phenotype to their own advantage thereby increasing the probability of transmission from one host to another. This phenomenon of host manipulation is interpreted as the expression of a parasite extended phenotype. Manipulative parasites generally affect multiple phenotypic traits in their hosts, although both the extent and adaptive significance of such multidimensionality in host manipulation is still poorly documented. To review the multidimensionality and magnitude of host manipulation, and to understand the causes of variation in trait value alteration, we performed a phylogenetically corrected meta‐analysis, focusing on a model taxon: acanthocephalan parasites. Acanthocephala is a phylum of helminth parasites that use vertebrates as final hosts and invertebrates as intermediate hosts, and is one of the few parasite groups for which manipulation is predicted to be ancestral. We compiled 279 estimates of parasite‐induced alterations in phenotypic trait value, from 81 studies and 13 acanthocephalan species, allocating a sign to effect size estimates according to the direction of alteration favouring parasite transmission, and grouped traits by category. Phylogenetic inertia accounted for a low proportion of variation in effect sizes. The overall average alteration of trait value was moderate and positive when considering the expected effect of alterations on trophic transmission success (signed effect sizes, after the onset of parasite infectivity to the final host). Variation in the alteration of trait value was affected by the category of phenotypic trait, with the largest alterations being reversed taxis/phobia and responses to stimuli, and increased vulnerability to predation, changes to reproductive traits (behavioural or physiological castration) and immunosuppression. Parasite transmission would thereby be facilitated mainly by changing mainly the choice of micro‐habitat and the anti‐predation behaviour of infected hosts, and by promoting energy‐saving strategies in the host. In addition, infection with larval stages not yet infective to definitive hosts (acanthella) tends to induce opposite effects of comparable magnitude to infection with the infective stage (cystacanth), although this result should be considered with caution due to the low number of estimates with acanthella. This analysis raises important issues that should be considered in future studies investigating the adaptive significance of host manipulation, not only in acanthocephalans but also in other taxa. Specifically, the contribution of phenotypic traits to parasite transmission and the range of taxonomic diversity covered deserve thorough attention. In addition, the relationship between behaviour and immunity across parasite developmental stages and host–parasite systems (the neuropsychoimmune hypothesis of host manipulation), still awaits experimental evidence. Most of these issues apply more broadly to reported cases of host manipulation by other groups of parasites.     

Host manipulation as a parasite transmission strategy when manipulation is exploited by non-host predators

Trophically transmitted parasites often alter their intermediate host's phenotype, thereby predisposing hosts to increased predation. This is generally considered to be a parasite strategy evolved to enhance transmission to the next host. However, the adaptive value of host manipulation is not clear, as it may be associated with costs, such as increased susceptibility to predator species that are unsuitable next hosts for the parasites. Thus, it has been proposed that, to be adaptive, manipulation should be specific by predisposing hosts more strongly to predation by target hosts (next host in the life cycle) than to non-hosts. Here we formally evaluate this prediction, and show that manipulation does not have to be specific to be adaptive. However, when manipulation is nonspecific, it needs to effectively increase the overall predation risk of infected hosts if it is to increase the parasite transmission probability. Thus, when initial predation risk is low, even highly nonspecific manipulation strategies can be adaptive. However, when initial predation risk is high, manipulation needs to be more specific to increase parasite transmission success. Therefore, nonspecific host manipulation may evolve in nature, but the adaptive value of a certain manipulation strategy can vary among different parasite populations depending on the variation in initial predation risk.     

The evolution of complex life cycles when parasite mortality is size- or time-dependent

In complex cycles, helminth larvae in their intermediate hosts typically grow to a fixed size. We define this cessation of growth before transmission to the next host as growth arrest at larval maturity (GALM). Where the larval parasite controls its own growth in the intermediate host, in order that growth eventually arrests, some form of size- or time-dependent increase in its death rate must apply. In contrast, the switch from growth to sexual reproduction in the definitive host can be regulated by constant (time-independent) mortality as in standard life history theory. We here develop a step-wise model for the evolution of complex helminth life cycles through trophic transmission, based on the approach of Parker et al. [2003a. Evolution of complex life cycles in helminth parasites. Nature London 425, 480-484], but which includes size- or time-dependent increase in mortality rate. We assume that the growing larval parasite has two components to its death rate: (i) a constant, size- or time-independent component, and (ii) a component that increases with size or time in the intermediate host. When growth stops at larval maturity, there is a discontinuous change in mortality to a constant (time-independent) rate. This model generates the same optimal size for the parasite larva at GALM in the intermediate host whether the evolutionary approach to the complex life cycle is by adding a new host above the original definitive host (upward incorporation), or below the original definitive host (downward incorporation). We discuss some unexplored problems for cases where complex life cycles evolve through trophic transmission.     

The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation

Numerous parasites with complex life cycles are able to manipulate the behaviour of their intermediate host in a way that increases their trophic transmission to the definitive host. Pomphorhynchus laevis, an acanthocephalan parasite, is known to reverse the phototactic behaviour of its amphipod intermediate host, Gammarus pulex, leading to an increased predation by fish hosts. However, levels of behavioural manipulation exhibited by naturally-infected gammarids are extremely variable, with some individuals being strongly manipulated whilst others are almost not affected by infection. To investigate parasite age and parasite intensity as potential sources of this variation, we carried out controlled experimental infections on gammarids using parasites from two different populations. We first determined that parasite intensity increased with exposure dose, but found no relationship between infection and host mortality. Repeated measures confirmed that the parasite alters host behaviour only when it reaches the cystacanth stage which is infective for the definitive host. They also revealed, we believe for the first time, that the older the cystacanth, the more it manipulates its host. The age of the parasite is therefore a major source of variation in parasite manipulation. The number of parasites within a host was also a source of variation. Manipulation was higher in hosts infected by two parasites than in singly infected ones, but above this intensity, manipulation did not increase. Since the development time of the parasite was also different according to parasite intensity (it was longer in doubly infected hosts than in singly infected ones, but did not increase more in multi-infected hosts), individual parasite fitness could depend on the compromise between development time and manipulation efficiency. Finally, the two parasite populations tested induced slightly different degrees of behavioural manipulation.     

The population biology of parasite-induced changes in host behavior

The ability of parasites to change the behavior of infected hosts has been documented and reviewed by a number of different authors (Holmes and Bethel, 1972; Moore, 1984a). This review attempts to quantify the population dynamic consequences of this behavior by developing simple mathematical models for the most frequently recorded of such parasite life cycles. Although changes in the behavior of infected hosts do occur for pathogens with direct life cycles, they are most commonly recorded in the intermediate hosts of parasites with complex life cycles. All the changes in host behavior serve to increase rates of transmission of the parasites between hosts. In the simplest case the changes in behavior increase rates of contact between infected and susceptible conspecific hosts, whereas in the more complex cases fairly sophisticated manipulations of the host's behavioral repertory are achieved. Three topics are dealt with in some detail: (1) the behavior of the insect vectors of such diseases as malaria and trypanosomiasis; (2) the intermediate hosts of helminths whose behavior is affected in such a way as to make them more susceptible to predation by the definitive host in the life cycle; and (3) the behavior and fecundity of molluscs infected with asexually reproducing parasitic flatworms. In each case an expression is derived for R0, the basic reproductive rate of the parasite when first introduced into the population. This is used to determine the threshold numbers of definitive and intermediate hosts needed to maintain a population of the pathogen. In all cases, parasite-induced changes in host behavior tend to increase R0 and reduce the threshold number of hosts required to sustain the infection. The population dynamics of the interaction between parasites and their hosts are then explored using phase plane analyses. This suggests that both the parasite and intermediate host populations may show oscillatory patterns of abundance. When the density of the latter is low, parasite-induced changes in host behavior increase this tendency to oscillate. When intermediate host population densities are high, parasite population density is determined principally by interactions between the parasites and their definitive hosts, and changes in the behavior of intermediate hosts are less important in determining parasite density. Analysis of these models also suggests that both asexual reproduction of the parasite within a host and parasite-induced reduction in host fecundity may be stabilizing mechanisms when they occur in the intermediate hosts of parasite species with indirect life cycles.(ABSTRACT TRUNCATED AT 400 WORDS)     

Two different strategies of host manipulation allow parasites to persist in intermediate–definitive host systems

Trophically transmitted parasites start their development in an intermediate host, before they finish the development in their definitive host when the definitive host preys on the intermediate host. In intermediate–definitive host systems, two strategies of host manipulation have been evolved: increasing the rate of transmission to the definitive host by increasing the chance that the definitive host will prey on the intermediate host, or increasing the lifespan of the parasite in the intermediate host by decreasing the predation chance when the intermediate host is not yet infectious. As the second strategy is less well studied than the first, it is unknown under what conditions each of these strategies is prevailed and evolved. We analysed the effect of both strategies on the presence of parasites in intermediate–definitive host systems with a structured population model. We show that the parasite can increase the parameter space where it can persist in the intermediate–definitive host system using one of these two strategies of host manipulation. We found that when the intermediate host or the definitive host has life‐history traits that allow the definitive host to reach large population densities, that is high reproduction rate of the intermediate host or high conversion efficiency of the definitive host (efficiency at which the uninfected definitive host converts caught intermediate hosts into offspring), respectively, evolving manipulation to decrease the predation chance of the intermediate host will be more beneficial than manipulation to increase the predation chance to enhance transmission. Furthermore, manipulation to decrease the predation chance of the intermediate host results in higher population densities of infected intermediate hosts than manipulation that increases the predation chance to enhance transmission. Our study shows that host manipulation in early stages of the parasite development to decrease predation might be a more frequently evolved way of host manipulation than is currently assumed.     

Conflict between parasites with different transmission strategies infecting an amphipod host

Competition between parasites within a host can influence the evolution of parasite virulence and host resistance, but few studies examine the effects of unrelated parasites with conflicting transmission strategies infecting the same host. Vertically transmitted (VT) parasites, transmitted from mother to offspring, are in conflict with virulent, horizontally transmitted (HT) parasites, because healthy hosts are necessary to maximize VT parasite fitness. Resolution of the conflict between these parasites should lead to the evolution of one of two strategies: avoidance, or sabotage of HT parasite virulence by the VT parasite. We investigated two co-infecting parasites in the amphipod host, Gammarus roeseli: VT microsporidia have little effect on host fitness, but acanthocephala modify host behaviour, increasing the probability that the amphipod is predated by the acanthocephalan's definitive host. We found evidence for sabotage: the behavioural manipulation induced by the Acanthocephala Polymorphus minutus was weaker in hosts also infected by the microsporidia Dictyocoela sp. (roeselum) compared to hosts infected by P. minutus alone. Such conflicts may explain a significant portion of the variation generally observed in behavioural measures, and since VT parasites are ubiquitous in invertebrates, often passing undetected, conflict via transmission may be of great importance in the study of host-parasite relationships.     

The trophic vacuum and the evolution of complex life cycles in trophically transmitted helminths

Parasitic worms (helminths) frequently have complex life cycles in which they are transmitted trophically between two or more successive hosts. Sexual reproduction often takes place in high trophic-level (TL) vertebrates, where parasites can grow to large sizes with high fecundity. Direct infection of high TL hosts, while advantageous, may be unachievable for parasites constrained to transmit trophically, because helminth propagules are unlikely to be ingested by large predators. Lack of niche overlap between propagule and definitive host (the trophic transmission vacuum) may explain the origin and/or maintenance of intermediate hosts, which overcome this transmission barrier. We show that nematodes infecting high TL definitive hosts tend to have more successive hosts in their life cycles. This relationship was modest, though, driven mainly by the minimum TL of hosts, suggesting that the shortest trophic chains leading to a host define the boundaries of the transmission vacuum. We also show that alternative modes of transmission, like host penetration, allow nematodes to reach high TLs without intermediate hosts. We suggest that widespread omnivory as well as parasite adaptations to increase transmission probably reduce, but do not eliminate, the barriers to the transmission of helminths through the food web.     

Competitive Growth Strategies in Intermediate Hosts: Experimental Tests of a Parasite life-History Model Using the Cestode, Schistocephalus solidus

In parasites with a complex life cycle, the fitness of an individual depends on its probability of reaching the final host and on its fecundity. Because larval growth in intermediate hosts may affect both transmission and adult size, selection should optimize growth patterns that are conditional on the presence and number of conspecific competitors. A recent model predicts that the total parasite volume per host should increase with intensity if larvae are able to vary growth depending on the number of conspecifics in the host (Life History Strategy hypothesis, i.e. LHS). Further, we would here expect growth rates to increase with intensity. By contrast, under the simplest alternative hypothesis of Resource Constraints (i.e. RC), the total parasite volume should remain constant. We experimentally infected copepods Macrocyclops albidus with the cestode Schistocephalus solidus to achieve 1, 2 or 3 parasites per host taking care that hosts had similar quality status at each infection level, and compared larval growth trajectories at the three intensity levels. The asymptotic total parasite volume was larger in double and triple infections than in single infections. Furthermore, the asymptotic total parasite volume was significantly larger in triple than in double infections but only in larger copepods that were less constrained by a host-size ceiling effect. These results, together with the fact that growth rates increased with intensity, support the LHS hypothesis: procercoids of a tapeworm may “count” their conspecific competitors in their first intermediate host to harvest its resources strategically until the next step in their complex life cycle. Co-ordinating editor: A. Biere