Parasite-mediated competition in Anolis lizards

Summary On many small Caribbean islands, two species of Anolis lizard coexist, but the two are typically very different in body size. The two Anolis of St. Maarten, however, are exceptional because they are similar in size and are known to be strongly competitive. One species, A. gingivinus, appears the stronger competitor and occurs throughout the island; the other, A. wattsi, is found only in the central hills. The malarial parasite Plasmodium azurophilum very rarely infects A. wattsi, but in some locations is very common in A. gingivinus. Wherever malaria infects A. gingivinus, A. wattsi is present, but wherever malaria is absent, only A. gingivinus occurs. This pattern of coincidence of malaria and coexistence of both Anolis is observed over distances of only a few hundred meters. The parasite infects both red and white blood cells of A. gingivinus and causes important pathology: immature erthrocytes increase in abundance, blood hemoglobin decreases, monocytes and neutrophils increase, and infected white cells are less likely to produce acid phosphatase. These results argue that malaria mediates competition between the two species and determines the present distribution of the lizards on St. Maarten. This kind of parasite-mediated competition could be common if susceptibility to parasitic infection varies among competitors. The distribution of malaria in the Anolis of Caribbean islands suggests this parasite can play an important role in Anolis community ecology.     

Apparent competition between parasitoids mediated by a shared hyperparasitoid

Cocoons of the specialist parasitoid Cotesia melitaearum , which attacks the Glanville fritillary butterfly in the Åland islands of SW Finland, are parasitized by the generalist hyperparasitoid Gelis agilis . We added experimentally to the system a second host species for G. agilis , C. glomerata , with which C. melitaearum does not compete for resources. After the one-time addition of the second parasitoid the natural populations of C. melitaearum declined in the treatment, as predicted by the apparent competition theory.     

Species coexistence under resource competition with intraspecific and interspecific direct competition in a chemostat

Competition theory has developed separately for direct competition and for exploitative competition. However, the combined effects of the two types of competition on species coexistence remain unclear. To examine how intraspecific and interspecific direct competition contributes to the coexistence of species competing for a single resource, we constructed a chemostat-type resource competition model. With general functions for intraspecific and interspecific direct competition, we derived necessary and sufficient conditions (except for a critical case that rarely occurs in a biological sense) that determine the number of stably coexisting species. From these conditions, we found that the number of coexisting species is determined just by the invasibility of each species into subcommunities with a smaller number of species. In addition, using a combination of rigorous mathematical theory and a simple graphical method, we can demonstrate how the stronger intraspecific direct competition facilitates species invasion, leading to a larger number of coexisting species.     

Parasite-mediated growth patterns and nutritional constraints in a cavity-nesting bird

1. Trade-offs between growth and immunity of nestling birds can be influenced by parasites, but the magnitude of these effects may depend on availability of critical dietary nutrients. Owing to their importance for both immune system function and growth, dietary carotenoids have the potential to mediate parasite-induced developmental strategies of avian hosts. 2. The effects of ectoparasitic blow flies Protocalliphora spp. and dietary carotenoids (lutein and zeaxanthin) on immune function and patterns of growth in nestling mountain bluebirds Sialia currucoides were investigated by combining parasite removal and carotenoid supplementation treatments in a 2 x 2 design. 3. Supplemental carotenoids enhanced nestlings' T-cell-mediated immune response following intradermal injection of phytohaemagglutinin. 4. The effect of carotenoid supplementation on rate of mass gain depended on whether broods were exposed to parasites: among parasitized broods, those receiving supplemental carotenoids gained mass more rapidly than nonsupplemented broods, whereas there was no effect of supplemental carotenoids on growth of mass in broods that had parasites removed. This suggests that additional dietary carotenoids allowed nestlings to compensate for the otherwise detrimental effects of parasites on mass gain. For length of the eighth primary feather at fledging, early and late broods differed in their response to parasitism: early broods showed an increase in feather length when parasites were removed, while nestlings in late broods had shorter feathers in the absence of parasites. We suggest that this may reflect within-season variation in parasite-mediated growth strategies of nestlings. 5. Maternal condition was positively associated with mass, condition and rate of feather growth of offspring under all conditions, and also influenced nestling immunocompetence, but only in the absence of parasites. 6. We conclude that dietary carotenoids alleviate some of the detrimental effects of parasites on nestling birds; however, parasites also appear to specifically influence other growth and resource allocation strategies, and possibly constrain maternal or genetic effects on offspring phenotype, irrespective of dietary carotenoid availability.     

Inducible defenses,competition and shared predation in planktonic food chains

Ecologists have long debated the role of predation in mediating the coexistence of prey species. Theory has mainly taken a bitrophic perspective that excludes the effects of inducible defenses at different trophic levels. However, inducible defenses could either limit or enhance the effects of predation on coexistence, by means of effects on bottom-up control and population stability. Our aim was to investigate how inducible defenses at different trophic levels affect the possibilities for predator-mediated coexistence, as opposed to competitive exclusion, in replicated experimental plankton communities. In particular, we analyzed how the presence or absence of inducible defenses in algal basal prey affected the outcome of competition between an inducible defended and an undefended herbivore, in the presence or absence of a carnivore. We found the undefended herbivore to be a superior competitor in the absence of predation. This outcome was reversed in the presence of a shared carnivore: populations of the undefended herbivore then strongly declined. The extent of this population decline differed between food webs based on undefended as opposed to inducible defended algal prey. In the former the undefended herbivore became undetectable for most of the duration of the experiment. In the latter the undefended herbivore also crashed to low densities, but it could still be detected during most of the experiment. In food webs based on inducible defended algae, the carnivore failed to reach high densities and exerted weaker top-down control on the two competing herbivores. We conclude that the inducible defense in one of our two competing herbivores allowed the outcome of competition to be reversed when a shared carnivore was added. Inducible defenses in algae did not change this outcome, but they significantly delayed extinction of the undefended herbivore. Predation itself did not promote coexistence in these experimental plankton communities.     

Parasite-mediated predation between native and invasive amphipods

Parasites can structure biological communities directly through population regulation and indirectly by processes such as apparent competition. However, the role of parasites in the process of biological invasion is less well understood and mechanisms of parasite mediation of predation among hosts are unclear. Mutual predation between native and invading species is an important factor in determining the outcome of invasions in freshwater amphipod communities. Here, we show that parasites mediate mutual intraguild predation among native and invading species and may thereby facilitate the invasion process. We find that the native amphipod Gammarus duebeni celticus is host to a microsporidian parasite, Pleistophora sp. (new species), with a frequency of infection of 0-90%. However, the parasite does not infect three invading species, G. tigrinus, G. pulex and Crangonyx pseudogracilis. In field and laboratory manipulations, we show that the parasite exhibits cryptic virulence: the parasite does not affect host fitness in single-species populations, but virulence becomes apparent when the native and invading species interact. That is, infection has no direct effect on G. d. celticus survivorship, size or fecundity; however, in mixed-species experiments, parasitized natives show a reduced capacity to prey on the smaller invading species and are more likely to be preyed upon by the largest invading species. Thus, by altering dominance relationships and hierarchies of mutual predation, parasitism strongly influences, and has the potential to change, the outcome of biological invasions.     

Parasite-mediated selection in experimental metapopulations of Daphnia magna

In metapopulations, only a fraction of all local host populations may be infected with a given parasite species, and limited dispersal of parasites suggests that colonization of host populations by parasites may involve only a small number of parasite strains. Using hosts and parasites obtained from a natural metapopulation, we studied the evolutionary consequences of invasion by single strains of parasites in experimental populations of the cyclical parthenogen Daphnia magna. In two experiments, each spanning approximately one season, we monitored clone frequency changes in outdoor container populations consisting of 13 and 19 D. magna clones, respectively. The populations were either infected with single strains of the microsporidian parasites Octosporea bayeri or Ordospora colligata or left unparasitized. In both experiments, infection changed the representation of clones over time significantly, indicating parasite-mediated evolution in the experimental populations. Furthermore, the two parasite species changed clone frequencies differently, suggesting that the interaction between infection and competitive ability of the hosts was specific to the parasite species. Taken together, our results suggest that parasite strains that invade local host populations can lead to evolutionary changes in the genetic composition of the host population and that this change is parasite-species specific.     

Parasite-mediated selection and the role of sex and diapause in Daphnia

To gain insight into parasite-mediated natural selection, we studied a natural population of the crustacean Daphnia magna during a severe epidemic of the bacterial parasite Pasteuria ramosa. We also investigated the relationship between susceptibility and the production of resting eggs, which are only produced during the sexual phase of reproduction. Live host samples were taken before and after this epidemic and resistance to P. ramosa was examined in the laboratory. Host clones collected after the epidemic were more resistant to P. ramosa than were those collected pre-epidemic, which is consistent with parasite-mediated selection. In our study population, asexually reproducing females were observed across the entire study period, but females carrying resting eggs were observed only prior to the epidemic. For hosts isolated in this pre-epidemic period, we found evidence that those carrying resting eggs (at the time of collection) were more susceptible than those that were reproducing asexually. This was especially apparent for measures of parasite growth, although not all measures of infection success conclusively supported this pattern. Nevertheless, the data suggest that some genotypes invest heavily in diapause at the expense of immunocompetence. Sex could therefore inhibit the evolution of resistance because each spring new genotypes will hatch from resting eggs that are relatively susceptible as they were not exposed to the previous years bout of parasite-mediated selection.     

Disentangling interference competition from exploitative competition in a crab–bivalve system using a novel experimental approach

In predator–prey relationships such as those between crabs and their bivalve prey, interference competition is a topic of intense investigation as it can have profound consequences on the dynamics of both predator and prey populations. However in laboratory experiments – also those on crab–bivalve systems – workers never adequately disentangled interference competition from exploitative competition, as prey depletion was never compensated. Hitherto, experimental studies on crab–bivalve systems lack direct behavioural observations and have provided only indirect and thus inconclusive evidence of interference competition. We studied interference competition in adult male shore crabs Carcinus maenas that foraged on blue mussels Mytilus edulis. We developed a novel type of experimental tank to replenish each consumed mussel, and thus to keep prey levels constant. We conducted two experiments in which we varied number of crabs (1, 2, 4) and number of mussels (first experiment: 4, 8, 16, 32; second experiment: 8, 32, 128) and directly observed the foraging behaviour of crabs (foraging area=0.25 m²). In the first experiment, feeding rates decreased with increasing crab density only at mussel density 16 because both search time and time spent in agonistic interactions increased. At other mussel densities, variation in crab density did not affect feeding rates, possibly because of low statistical power and the narrow range of mussel densities offered. In the second experiment feeding rates decreased with increasing crab density because crabs spent more time in agonistic interactions and handling their prey. Feeding rates increased with increasing mussel density. Overall, crabs spent on average 14–18% of their foraging time in agonistic behaviours, while on three out of 64 occasions feeding rates decreased because mussels were stolen (kleptoparasitism). Concluding, we have shown that interference competition occurs in absence of prey depletion, while conducting direct behavioural observations aid to identify the behavioural processes that underlie interference competition.     

The effects of social structure and sex-biased transmission on macroparasite infection

Mathematical models of disease dynamics tend to assume that individuals within a population mix at random and so transmission is random, and yet, in reality social structure creates heterogeneous contact patterns. We investigated the effect of heterogeneity in host contact patterns on potential macroparasite transmission by first quantifying the level of assortativity in a socially structured wild rodent population (Apodemus flavicollis) with respect to the directly-transmitted macroparasitic helminth, Heligmosomoides polygyrus. We found the population to be disassortatively mixed (i.e. male mice mixing with female mice more often than same sex mixing) at a constant level over time. The macroparasite H. polygyrus has previously been shown to exhibit male-biased transmission so we used a Susceptible-Infected (SI) mathematical model to simulate the effect of increasing strengths of male-biased transmission on the prevalence of the macroparasite using empirically-derived transmission networks. When transmission was equal between the sexes the model predicted macroparasite prevalence to be 73% and infection was male biased (82% of infection in the male mice). With a male-bias in transmission ten times that of the females, the expected macroparasite prevalence was 50% and was equally prevalent in both sexes, results that both most closely resembled empirical dynamics. As such, disassortative mixing alone did not produce macroparasite dynamics analogous to those from empirical observations; a strong male-bias in transmission was also required. We discuss the relevance of our results in the context of network models for transmission dynamics and control.     

Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite

The adaptive trade-off theory for the evolution and maintenance of parasite virulence requires that virulence be genetically correlated with other fitness characteristics of the parasite. Many theoretical models rely on a positive correlation between virulence and transmissibility. They assume that high parasite replication rates are associated with a high probability of transmission (and, hence, increased parasite fitness), but also with high levels of damage to the host (high virulence). Schistosomes are macroparasites with an indirect life cycle involving a mammalian and a molluscan host. Here we demonstrate, through the development of five substrains, a genetic basis for schistosome virulence. We used these substrains further in order to investigate the presence of parasite fitness traits that were genetically correlated with virulence. High virulence in the (mouse) definitive host was, as predicted, positively correlated with parasite replication. In contrast, in the (snail) intermediate host high virulence was associated with low parasite replication rates. Variation in infectivity to and parasite replication in the definitive host was suggested as a compensating mechanism for the maintenance of virulence in the snail host. This is the first report of a trade-off in parasite reproductive success across hosts in an indirectly transmitted macroparasite.     

Reduction of egg size in natural populations of threespine stickleback infected with a cestode macroparasite

Manifestations of infectious disease may represent host adaptations to avoid or reduce the effects of infection on host fitness, parasite manipulations that benefit the pathogen's fitness, or nonadaptive side effects of parasitism. Threespine stickleback fish (Gasterosteus aculeatus) from Alaska and the cestode macroparasite Schistocephalus solidus provide an excellent system for study of the effects of parasitism on host egg size because females in populations there are capable of producing clutches of eggs in the face of substantial infection, contrary to the inhibition of reproduction that has been observed in other stickleback populations or other species of fish. A side effect resulting in reduction of mean ovummass among infected females was predicted based on the egg production process in female stickleback, the considerable energy and resource demands of S. solidus, and the chronic and progressive nature of the effects the macroparasite should have on the host fish. In each of 9 populations of G. aculeatus representing replicate natural experiments in lakes scattered across the Matanuska-Susitna Valley and the Kenai Peninsula of south-central Alaska and among all populations combined, the mean ovum mass of infected female fish is significantly reduced in comparison with that of uninfected females taken from the same population at the same time. Reduction in mean female egg mass ranged from 8 to 32% across all populations. To examine whether reduction in mean female ovum mass was a nonadaptive side effect or an adaptation, relatively large data sets from 2 of the populations were used. Mean ovum mass of infected females was predicted to decrease directly in relation to parasite index (PI) if the diminution in mean egg mass were the result of a nonadaptive side effect resulting from host nutrient loss. Alternatively, the absence of a relationship between PI and reduction in ovum mass is predicted if decreases in mean female ovum mass result from host or parasite adaptation (or both) because lightly infected hosts should show a response similar to that of heavily infected ones. In each of the 2 populations, there is a significant, negative relationship between mean female ovum mass and PI, demonstrating a correlation between the decrease in ovum mass and the level of infection. Thus, the results are consistent with the hypothesis that the reductions in mean female egg mass represent side effects of parasitism involving nutrient theft. Moreover, the proportional decline in egg mass with increasing PI apparently differed between the 2 populations, and there was no significant relationship between mean percent decrease in mean female ovum mass and mean PI across populations. These observations suggest that unknown ecological and evolutionary factors influence the degree of reduction in mean ovum mass in a population-specific manner.     

Field evidence for apparent competition mediated via the shared parasites of two gamebird species

Although apparent competition mediated via shared parasites is potentially an important force influencing community structure, there is limited evidence to demonstrate its occurrence in the field. Here we show that the intensity of infection by the caecal nematode Heterakis gallinarum picked up by naive grey partridges, both maintained in pens and released on six gamebird estates in the UK, is significantly correlated with the intensity of infection recorded in the previous year from pheasants on those estates. Furthermore, the worm burdens picked up appeared to be sufficient to negatively influence host condition. These results provide evidence that infection from pheasants determines the worm burdens of partridges in the field, supporting the hypothesis that parasite-mediated apparent competition with the pheasant may be a factor influencing the decline and subsequent recovery of wild grey partridges.     

Indirect competition for pollinators is weak compared to direct resource competition: pollination and performance in the face of an invader

Invasive plants have the potential to reduce native plant abundance through both direct and indirect interactions. Direct interactions, such as competition for soil resources, and indirect interactions, such as competition for shared pollinators, have been shown to influence native plant performance; however, we know much less about how these interactions influence native plant abundance in the field. While direct competitive interactions are often assumed to drive declines in native abundance, an evaluation of their influence relative to indirect mechanisms is needed to more fully understand invasive plant impacts. We quantified the direct effects of resource competition by the invasive perennial forb, Euphorbia esula (Euphorbiaceae), on the recruitment, subsequent performance, and ultimate adult abundance of the native annual, Clarkia pulchella (Onagraceae). We contrast these direct effects with those that indirectly resulted from competition for shared pollinators. Although E. esula dramatically reduced pollinator visitation to C. pulchella, plants were only weakly pollen-limited. Pollen supplementation increased the number of seeds per fruit from 41.28 to 46.38. Seed addition experiments revealed that the impacts of ameliorating pollen limitation only increased potential recruitment by 12.3 %. In contrast, seed addition experiments that ameliorated direct competition with E. esula resulted in an increase in potential future recruitment of 574 %. Our results show that, while the indirect effects of competition for pollinators can influence plant abundance, its effects are dwarfed by the magnitude of direct effects of competition for resources.     

A direct effect of competition on food choice by pigeons

Previous research on food choice of pigeons foraging alone and in competition showed an indirect response to the competitor, mediated by the resource depletion associated with the competitor. This experiment showed, in addition, that pigeons can adjust their food choice in direct response to the competitor itself. Pigeons foraged for large, preferred grains of maize and smaller, unpreferred grains of wheat presented in bowls covered with sawdust. In a within-subject design, pigeons were tested alone or in competition with another pigeon. In competition, a higher choice proportion of the wheat grains was observed on the first two choices out of 48 items, and this effect increased with time in the experiment. This result underscores the role of learning in group foraging behaviour. It also suggests a possible ecological implication: that individuals that learn faster may enjoy a competitive advantage in terms of reduced delay in responding to the presence of a conspecific.     

Parasite-mediated evolution of the functional part of the MHC in primates

The major histocompatibility complex (MHC) is a key model of genetic polymorphism, but the mechanisms underlying its extreme variability are debated. Most hypotheses for MHC diversity focus on pathogen-driven selection and predict that MHC polymorphism evolves under the pressure of a diverse parasite fauna. Several studies reported that certain alleles offer protection against certain parasites, yet it remains unclear whether variation in parasite pressure more generally covaries with allelic diversity and rates of molecular evolution of MHC across species. We tested this prediction in a comparative study of 41 primate species. We characterized polymorphism of the exon 2 of DRB region of the MHC class II. Our phylogenetic analyses controlled for the potential effects of neutral mutation rate, population size, geographic origin and body mass and revealed that nematode species richness associates positively with nonsynonymous nucleotide substitution rate at the functional part of the molecule. We failed to find evidence for allelic diversity being strongly related to parasite species richness. Continental distribution was a strong predictor of both allelic diversity and substitution rate, with higher values in Malagasy and Neotropical primates. These results indicate that parasite pressure can influence the different estimates of MHC polymorphism, whereas geography plays an independent role in the natural history of MHC.