Effects of fleas on nest success of Arctic barnacle geese: experimentally testing the mechanism

Parasites have detrimental effects on their hosts’ fitness. Therefore, behavioural adaptations have evolved to avoid parasites or, when an individual is already in contact with a parasite, prevent or minimize infections. Such anti‐parasite behaviours can be very effective, but can also be costly for the host. Specifically, ectoparasites can elicit strong host anti‐parasite behaviours and interactions between fleas (Siphonaptera) and their hosts are one of the best studied. In altricial bird species, nest fleas can negatively affect both parent and offspring fitness components. However, knowledge on the effects of fleas on precocial bird species is scarce. Research on geese in the Canadian Arctic indicated that fleas have a negative impact on reproductive success. One possible hypothesis is that fleas may affect female incubation behaviour. Breeding females with many fleas in their nest may increase the frequency and/or duration of incubation breaks and could even totally desert their nest. The aim of our study was to 1) determine if a similar negative relationship existed between flea abundance and reproductive success in our study colony of Arctic breeding barnacle geese Branta leucopsis and 2) experimentally quantify if such effects could be explained by a negative effect of nest fleas on female behaviour. We compared host anti‐parasite and incubation behaviour between experimentally flea‐reduced and control nests using wildlife cameras and temperature loggers. We found that flea abundance was negatively associated with hatching success. We found little experimental support, however, for changes in behaviour of the breeding female as a possible mechanism to explain this effect.     

On the capacity of macroparasites to control insect populations

A graphical model of the population dynamics of macroparasites and their hosts is developed. Three principal means by which the parasites can be regulated are considered: reduction in host density as a result of parasite-induced host mortality, reduction in host density as a result of parasite-induced host sterility, and competition among parasites within multiply-infected hosts. The means by which parasites are regulated has a major effect on the degree to which they can depress host population densities. In particular, a parasite that sterilizes its host is expected to reduce host density more than one that causes an equivalent decline in host fitness through increased mortality. A special case of the model is developed for herbivorous insects that, in the absence of parasites, are limited by larval food resources. Parasites that are regulated via parasite-induced host sterility will control the insect populations below the level set by larval resources if the threshold host density for the parasites (N(T)) is less than the ratio of carrying capacity to net reproductive rate of the insects (K/R). Data are presented showing that all three means of parasite regulation, but especially parasite-induced host sterility, can operate in Howardula aoronymphium, a nematode parasite of mycophagous Drosophila flies. Data from a field cage experiment show that, if these nematodes are regulated primarily via reductions in host density due to this sterility, the parameters N(T), K, and R are such that Howardula is likely to play an important role in controlling Drosophila populations. However, this conclusion must be tempered by the fact that these nematodes also cause increased host mortality and experience within-host competition, making the conditions for parasite control of the flies more stringent.     

Host defence versus intraspecific competition in the regulation of infrapopulations of the flea Xenopsylla conformis on its rodent host Meriones crassus

Mechanisms that regulate parasite populations may influence the evolution of hosts and parasites, as well as the stability of host-parasite dynamics but are still poorly understood. A manipulation experiment on the grooming ability of rodent hosts (Meriones crassus) and flea (Xenopsylla conformis) densities on these hosts successfully disentangled two possible regulating mechanisms: (i) behavioural defence of the host and (ii) intraspecific competition among parasites, and revealed their importance in suppressing the feeding of fleas. Moreover, the results suggest that flea competition is direct and is not mediated by host grooming, immune response, or parasite-induced damage to the host. These mechanisms, together with interspecific competition and density-dependent parasite-induced host damage, may limit the parasite burden on an individual host and may prevent parasites from overexploiting their host population.     

Relative fitness of a generalist parasite on two alternative hosts: a cross‐infestation experiment to test host specialization of the hen flea Ceratophyllus gallinae (Schrank)

Host range is a key element of a parasite's ecology and evolution and can vary greatly depending on spatial scale. Generalist parasites frequently show local population structure in relation to alternative sympatric hosts (i.e. host races) and may thus be specialists at local scales. Here, we investigated local population specialization of a common avian nest‐based parasite, the hen flea Ceratophyllus gallinae (Schrank), exploiting two abundant host species that share the same breeding sites, the great tit Parus major (Linnaeus) and the collared flycatcher Ficedula albicollis (Temminck). We performed a cross‐infestation experiment of fleas between the two host species in two distinct study areas during a single breeding season and recorded the reproductive success of both hosts and parasites. In the following year, hosts were monitored again to assess the long‐term impact of cross‐infestation. Our results partly support the local specialization hypothesis: in great tit nests, tit fleas caused higher damage to their hosts than flycatcher fleas, and in collared flycatcher nests, flycatcher fleas had a faster larval development rates than tit fleas. However, these results were significant in only one of the two studied areas, suggesting that the location and history of the host population can modulate the specialization process. Caution is therefore called for when interpreting single location studies. More generally, our results emphasize the need to explicitly account for host diversity in order to understand the population ecology and evolutionary trajectory of generalist parasites.     

Control of flea populations in a simulated home environment model using lufenuron, imidacloprid or fipronil

Control strategies were evaluated over a 6-month period in a home simulation model comprising a series of similar carpeted pens, housing matched groups of six cats, in which the life-cycle of the flea Ctenocephalides felis felis Bouche (Siphonaptera: Pulicidae) had been established. Additional adult fleas were placed on the cats at intervals to mimic acquisition of extraneous fleas from outside the home. Treatment strategies included a single subcutaneous deposition of injectable lufenuron supported by initial treatments with a short-acting insecticidal spray, or monthly topical applications of imidacloprid or fipronil. An untreated control group indicated that conditions were suitable for flea replication and development. Controls had to be combed on 18 occasions to remove excessive flea burdens and two developed allergic reactions. Lufenuron cats were combed once and required two insecticidal treatments in the first month to achieve control. Even so, small flea burdens were constantly present thereafter. Imidacloprid and fipronil treatments appeared to give virtually complete control throughout. Single fleas were found on imidacloprid cats on two occasions, whereas none were recovered from fipronil cats at any time after the first treatment. Tracer cats were used to monitor re-infestation rates at the end of the trial period. Small numbers of host-seeking fleas were demonstrated in all treatment pens, indicating that total eradication had not been accomplished. It is concluded that the home environment simulation model incorporating tracer animals could provide a powerful tool for studying flea population dynamics under controlled conditions but improved techniques are needed for quantifying other off-host life-cycle stages.     

On the equivalence of host local adaptation and parasite maladaptation: an experimental test

In spatiotemporally varying environments, host-parasite coevolution may lead to either host or parasite local adaptation. Using reciprocal infestations over 11 pairs of plots, we tested local adaptation in the hen flea and its main host, the great tit. Flea reproductive success (number of adults at host fledging) was lower on host individuals from the same plot compared with foreign hosts (from another plot), revealing flea local maladaptation. Host reproductive success (number of fledged young) for nests infested by foreign fleas was lower compared with the reproductive success of controls, with an intermediate success for nests infested by local fleas. This suggests host local adaptation although the absence of local adaptation could not be excluded. However, fledglings were heavier and larger when reared with foreign fleas than when reared with local fleas, which could also indicate host local maladaptation if the fitness gain in offspring size offsets the potential cost in offspring number. Our results therefore challenge the traditional view that parasite local maladaptation is equivalent to host local adaptation. The differences in fledgling morphology between nests infested with local fleas and those with foreign fleas suggest that flea origin affects host resource allocation strategy between nestling growth and defense against parasites. Therefore, determining the mechanisms that underlie these local adaptation patterns requires the identification of the relevant fitness measures and life-history trade-offs in both species.     

Population dynamics of host-parasite interactions in a cockroach-oxyuroid system

Host-parasite interactions of an urban cockroach, Blattella germanica , and its oxyuroid parasite, Blatticola blattae , were investigated. Life history data of host and parasites were collected under laboratory conditions. These data were used to model the effect of the parasite on the population dynamics of the host in order to understand the parasite's impact on the host population. The aggregation of parasites within a host was under-dispersed. Hosts normally were found to be infected with only one male and one female and rarely two or three. However, the primary sex ratio after hatching was 1.1 (males/females). Female parasite longevity equalled the life span of its host. B. blattae had a significant impact on the survival rate of the cockroach larvae and their time to reach maturity, but no effect on the survival rate of the adults. Infected host females produced fewer first oothecae than uninfected ones. Using the population parameters a simple model was developed to estimate the parasite's effect on the population dynamics of its host. According to the model the parasite suppresses the cockroach populations by ca 11%. Hence, the effect of the parasite does not appear strong enough to be used as a biological control agent by itself.     

The spread of fecally transmitted parasites in socially-structured populations

Mammals are infected by a wide array of gastrointestinal parasites, including parasites that also infect humans and domesticated animals. Many of these parasites are acquired through contact with infectious stages present in soil, feces or vegetation, suggesting that ranging behavior will have a major impact on their spread. We developed an individual-based spatial simulation model to investigate how range use intensity, home range overlap, and defecation rate impact the spread of fecally transmitted parasites in a population composed of social groups (i.e., a socially structured population). We also investigated the effects of epidemiological parameters involving host and parasite mortality rates, transmissibility, disease-related mortality, and group size. The model was spatially explicit and involved the spillover of a gastrointestinal parasite from a reservoir population along the edge of a simulated reserve, which was designed to mimic the introduction pathogens into protected areas. Animals ranged randomly within a "core" area, with biased movement toward the range center when outside the core. We systematically varied model parameters using a Latin hypercube sampling design. Analyses of simulation output revealed a strong positive association between range use intensity and the prevalence of infection. Moreover, the effects of range use intensity were similar in magnitude to effects of group size, mortality rates, and the per-contact probability of transmission. Defecation rate covaried positively with gastrointestinal parasite prevalence. Greater home range overlap had no positive effects on prevalence, with a smaller core resulting in less range overlap yet more intensive use of the home range and higher prevalence. Collectively, our results reveal that parasites with fecal-oral transmission spread effectively in socially structured populations. Future application should focus on parameterizing the model with empirically derived ranging behavior for different species or populations and data on transmission characteristics of different infectious organisms.     

Depression of host population abundance by direct life cycle macroparasites

Simple population models are used to identify the factors which determine the degree to which direct life cycle macroparasites depress their host populations from disease free equilibrium levels. The impact of parasitic infection is shown to be related to a range of biological characteristics of the host and parasite. The most important theoretical predictions are as follows: (1) certain threshold conditions must be satisfied (concerning host density and the rates of host and parasite reproduction) to enable the pathogen to persist with the host population; (2) parasites of low to intermediate pathogenicity are the most effective suppressors of host population growth while highly pathogenic species are likely to cause their own extinction but not that of their host; (3) the statistical distribution of parasite numbers per host has a major influence on the degree of host population depression; (4) host population with high reproductive potential are better able to withstand the impact of pathogens; (5) density dependent constraints on parasite population growth within, or on the host, whether induced by competition for finite resources or immunological attack, restrict the regulatory influence of the parasites; (6) parasites with the ability to multiply directly within the host are the most effective suppressors of host population growth and may cause the extinction of the host and hence themselves.Theoretical predictions are discussed in light of (a) the use of pathogens as biological control agents of pest species and (b) the effects of disease control on host population growth.     

Ruminating on complexity: macroparasites of wildlife and livestock

Recent advances in ecology have improved our understanding of the role of parasites in the dynamics of wildlife populations. However, conditions that prevail in many wildlife systems, such as host movement, contact with livestock, and heterogeneity in the environment of the parasite outside of the host, have largely been ignored in existing models of macroparasite transmission. We need to refine these models if we are to stand a chance of developing effective parasite control strategies. New quantitative approaches enable us to address key complexities and make better use of scarce data, and these should enhance our efforts to understand and control emerging problems of interspecific parasite transmission.     

Use of parasite regulation of host endocrinology to enhance the potential of biological control

The implications of parasite regulation of host endocrinology for successful biological control have not been fully appreciated. Insect parasites regulate host metamorphosis in a number of different ways. For a given host (pest) situation, each form of host regulation has its own advantages and disadvantages. Careful selection of a parasite based upon its mode lf host regulation can enhance the potential for biological control success. A basic knowledge of the endocrine basis for parasite regulation of its host will enable prediction of whether a parasite can regulate, and survive in, a host to which it has not been previously exposed.     

The Evolution of Taxonomic Diversity in Helminth Assemblages of Mammalian Hosts

Several studies have searched for the key forces behind the diversification of parasite assemblages over evolutionary time. All of these studies have used parasite species richness as their measure of diversity, thus ignoring the relatedness among parasite species and the taxonomic structure of the assemblages. This information is essential, however, if we want to elucidate which processes have caused an assemblage of parasites to acquire new species. Here, we performed a comparative analysis across 110 species of mammalian hosts in which we evaluated the effects of four host traits (body mass, population density, geographic range, and basal metabolic rate) on the diversity of their assemblages of helminth endoparasites. As measures of diversity, we used parasite species richness, as well as the average taxonomic distinctness of the assemblage and its variance; the latter measures are based on the taxonomic distance between two parasite species, computed across all possible species pairs in an assemblage. Unlike parasite species richness, both the average taxonomic distinctness and its variance were unaffected by the number of hosts examined. These two measures of parasite diversity also proved highly repeatable among host populations of the same mammalian species; in contrast, parasite species richness was unreliable as a species character, as it varied as much within a host species than among different host species. Using phylogenetically independent contrasts, and correcting for potential confounding variables, we found that host population density correlated positively with parasite species richness. There were, however, no other relationships between any of the four host traits investigated and either of our measures of parasite diversity. The processes facilitating the taxonomic diversification of parasite assemblages thus remain unclear, but their elucidation will be necessary if we are to fully understand parasite evolution.     

Density-dependent host selection in ectoparasites: An application of isodar theory to fleas parasitizing rodents

Parasites should make the same decisions that every animal makes regarding fitness reward. They can maximize reproductive success by selection of those habitats that guarantee the greatest fitness output. We consider the host population as a habitat of a parasite population. Consequently, hosts (=habitats) that differ quantitatively or qualitatively will support different numbers of parasites. The nature of habitat selection can be detected by isodars, lines along which habitat selection yields equivalent fitness reward. We applied this approach to study host selection of five fleas, each infesting two desert rodents. Xenopsylla conformis, Xenopsylla ramesis, Nosopsyllus iranus theodori and Stenoponia tripectinata medialis parasitize Gerbillus dasyurus and Meriones crassus. Synosternus cleopatrae pyramidis parasitizes Gerbillus andersoni allenbyi and Gerbillus pyramidum. Three fleas ( X. conformis, X. ramesis and S. c. pyramidis) were able to perceive quantitative (amount of the resource; e.g. organic matter in the nest for flea larvae) and/or qualitative (pattern of resource acquisition; e.g. host defensiveness) differences between hosts. Two other fleas did not perceive between-host differences. X. conformis was a density-dependent host selector that showed sharp selectivity at low density. X. ramesis and S. c. pyramidis were density-independent host selectors with a direct correspondence of density with habitat quality. N. i. theodori and S. t. medialis were non-selectors with no relationship at all between density and host quality. The results of the application of the isodar theory suggest that ectoparasites, like other animals, behave as if they are able to make choices and decisions that favour environments in which their reproductive benefit is maximized.     

Host phenology regulates parasite–host demographic cycles and eco‐evolutionary feedbacks

Parasite–host interactions can drive periodic population dynamics when parasites overexploit host populations. The timing of host seasonal activity, or host phenology, determines the frequency and demographic impact of parasite–host interactions, which may govern whether parasites sufficiently overexploit hosts to drive population cycles. We describe a mathematical model of a monocyclic, obligate‐killer parasite system with seasonal host activity to investigate the consequences of host phenology on host–parasite dynamics. The results suggest that parasites can reach the densities necessary to destabilize host dynamics and drive cycling as they adapt, but only in some phenological scenarios such as environments with short seasons and synchronous host emergence. Furthermore, only parasite lineages that are sufficiently adapted to phenological scenarios with short seasons and synchronous host emergence can achieve the densities necessary to overexploit hosts and produce population cycles. Host‐parasite cycles also generate an eco‐evolutionary feedback that slows parasite adaptation to the phenological environment as rare advantageous phenotypes can be driven extinct due to a population bottleneck depending on when they are introduced in the cycle. The results demonstrate that seasonal environments can drive population cycling in a restricted set of phenological patterns and provide further evidence that the rate of adaptive evolution depends on underlying ecological dynamics.     

Coevolutionary arms races: increased host immune defense promotes specialization by avian fleas

We investigated the relationship between host defense and specialization by parasites in comparative analyses of bird fleas and T-cell mediated immune response of their avian hosts, showing that fleas with few main host species exploited hosts with weak or strong immune defenses, whereas flea species that parasitized a large number of host species only exploited hosts with weak immune responses. Hosts with strong immune responses were exploited by a larger number of flea species than hosts with weak responses. A path analysis model with an effect of T-cell response on the number of host species, or a model with host coloniality directly affecting host T-cell response, which in turn affected the number of host species used by fleas, best explained the data. Therefore, parasite specialization may have evolved in response to strong host defenses.     

Random parasite encounters coupled with condition-linked immunity of hosts generate parasite aggregation

Parasite aggregation is viewed as a natural law in parasite-host ecology but is a paradox insofar as parasites should follow the Poisson distribution if hosts are encountered randomly. Much research has focused on whether parasite aggregation in or on hosts is explained by aggregation of infective parasite stages in the environment, or by heterogeneity within host samples in terms of host responses to infection (e.g., through representation of different age classes of hosts). In this paper, we argue that the typically aggregated distributions of parasites may be explained simply. We propose that aggregated distributions can be derived from parasites encountering hosts randomly, but subsequently by parasites being 'lost' from hosts based on condition-linked escape or immunity of hosts. Host condition should be a normally distributed trait even among otherwise homogeneous sets of hosts. Our model shows that mean host condition and variation in host condition have different effects on the different metrics of parasite aggregation. Our model further predicts that as host condition increases, parasites become more aggregated but numbers of attending parasites are reduced overall and this is important for parasite population dynamics. The effects of deviation from random encounter are discussed with respect to the relationship between host condition and final parasite numbers.     

Searching for generality in the patterns of parasite abundance and distribution: Ectoparasites of a South African rodent, Rhabdomys pumilio

We studied abundance and distribution of seven ectoparasite species (fleas Chiastopsylla rossi and Dynopsyllus ellobius, a louse Polyplax arvicanthis, mites Androlaelaps fahrenholzi and Laelaps giganteus and two ticks Haemaphysalis elliptica and Hyalomma truncatum) exploiting the same populations of the rodent host Rhabdomys pumilio in South Africa. We considered three general patterns of abundance and distribution, namely (i) aggregated distribution of parasites amongst individual hosts; (ii) positive relationships between mean parasite abundance and their prevalence; and (iii) applicability of a simple epidemiological model based on mean parasite abundance and its variance to predict the observed patterns of prevalence. Our aims were to evaluate the relative role of host- versus parasite-associated factors by looking at similarity amongst different parasites in these patterns. In general, all parasites demonstrated strong similarity in each of the three patterns of abundance and distribution. However, the strength of these patterns differed amongst parasite species. We conclude that these patterns are driven mainly by hosts, but differences are caused by differences between various life-history traits of parasite species. Our results support the idea that general laws apply to parasite population ecology.     

Diversity and the maintenance of sex by parasites

The Red Queen hypothesis (RQH) predicts that parasite‐mediated selection will maintain sexual individuals in the face of competition from asexual lineages. The prediction is that sexual individuals will be difficult targets for coevolving parasites if they give rise to more genetically diverse offspring than asexual lineages. However, increasing host genetic diversity is known to suppress parasite spread, which could provide a short‐term advantage to clonal lineages and lead to the extinction of sex. We test these ideas using a stochastic individual‐based model. We find that if parasites are readily transmissible, then sex is most likely to be maintained when host diversity is high, in agreement with the RQH. If transmission rates are lower, however, we find that sexual populations are most likely to persist for intermediate levels of diversity. Our findings thus highlight the importance of genetic diversity and its impact on epidemiological dynamics for the maintenance of sex by parasites.     

Effect of sexual segregation on host-parasite interaction: Model simulation for abomasal parasite dynamics in alpine ibex (Capraibex)

We investigated whether sexual segregation might affect parasite transmission and host dynamics, hypothesising that if males are the more heavily infected sex and more responsible for the transmission of parasite infections, female avoidance of males and the space they occupy could reduce infection rates. A mathematical model, simulating the interaction between abomasal parasites and a hypothetical alpine ibex (Capraibex) host population composed of its two sexes, was developed to predict the effect of different degrees of sexual segregation on parasite intensity and on host abundance. The results showed that when females tended to be segregated from males, and males were distributed randomly across space, the impact of parasites was the lowest, resulting in the highest host abundance, with each sex having the lowest parasite intensity. The predicted condition that minimises the impact of parasites in our model was the one closest to that observed in nature where females actively seek out the more segregated sites while males are less selective in their ranging behaviour. The overlapping of field observation with the predicted optimal strategy lends support to our idea that there might be a connection between parasite transmission and sexual segregation. Our simulations provide the biological boundaries of host-parasite interaction needed to determine a parasite-mediated effect on sexual segregation and a formalised null hypothesis against which to test future field experiments.     

Abundance patterns of two Oropsylla (Ceratophyllidae: Siphonaptera) species on black-tailed prairie dog (Cynomys ludovicianus) hosts.

Behavioral, genetic, and immune variation within a host population may lead to aggregation of parasites whereby a small proportion of hosts harbor a majority of parasites. In situations where two or more parasite species infect the same host population there is the potential for interaction among parasites that could potentially influence patterns of aggregation through either competition or facilitation. We studied the occurrence and abundance patterns of two congeneric flea species on black-tailed prairie dog (Cynomys ludovicianus) hosts to test for interactions among parasite species. We live-trapped prairie dogs on ten sites in Boulder County, CO and collected their fleas. We found a non-random, positive association between the two flea species, Oropsylla hirsuta and O. tuberculata cynomuris; hosts with high loads of one flea species had high loads of the second species. This result suggests that there is no interspecific competition among fleas on prairie dog hosts. Host weight had a weak negative relationship to flea load and host sex did not influence flea load, though there were slight differences in flea prevalence and abundance between male and female C. ludovicianus. While genetic and behavioral variation among hosts may predispose certain individuals to infection, our results indicate apparent facilitation among flea species that may result from immune suppression or other flea-mediated factors.