Variation in anti-parasite behaviour and infection among larval amphibian species

Along with immune defences, many animals exhibit effective anti-parasite behaviours such as parasite avoidance and removal that influence their susceptibility to infection. Host ecology and life history influence investment into comparatively fixed defences such as innate immunity but may affect the strength of anti-parasite behaviours as well. We investigated activity levels in five different species of larval amphibian with varying life histories and ecology in control, novel food stimulus, and trematode parasite (Echinoparyphium sp.) threat conditions. There was a significant interaction of species and treatment given that American toad (Bufo americanus), wood frog (Lithobates sylvaticus), and bullfrog (Lithobates catesbeianus) tadpoles generally increased their activity when parasite infectious stages were present while grey tree frogs (Hyla versicolor) and northern leopard frogs (Lithobates pipiens) did not, even though activity was negatively related to infection. In addition, there was considerable variation among species in their susceptibility to parasitism, with infection prevalence ranging from 17 % in bullfrog tadpoles to 70 % in wood frogs. However, amphibian life history (larval and adult traits) was not related to parasitism or level of anti-parasite behaviour at the species level. Consequently, we suggest that future investigations include more species with a range of life history traits and also consider host ecology, particularly if conspicuous anti-parasite behaviours are more likely in amphibian species that experience a relatively low risk of predation.     

Modelling Parasite Transmission in a Grazing System: The Importance of Host Behaviour and Immunity

Parasitic helminths present one of the most pervasive challenges to grazing herbivores. Many macro-parasite transmission models focus on host physiological defence strategies, omitting more complex interactions between hosts and their environments. This work represents the first model that integrates both the behavioural and physiological elements of gastro-intestinal nematode transmission dynamics in a managed grazing system. A spatially explicit, individual-based, stochastic model is developed, that incorporates both the hosts’ immunological responses to parasitism, and key grazing behaviours including faecal avoidance. The results demonstrate that grazing behaviour affects both the timing and intensity of parasite outbreaks, through generating spatial heterogeneity in parasite risk and nutritional resources, and changing the timing of exposure to the parasites’ free-living stages. The influence of grazing behaviour varies with the host-parasite combination, dependent on the development times of different parasite species and variations in host immune response. Our outputs include the counterintuitive finding that under certain conditions perceived parasite avoidance behaviours (faecal avoidance) can increase parasite risk, for certain host-parasite combinations. Through incorporating the two-way interaction between infection dynamics and grazing behaviour, the potential benefits of parasite-induced anorexia are also demonstrated. Hosts with phenotypic plasticity in grazing behaviour, that make grazing decisions dependent on current parasite burden, can reduce infection with minimal loss of intake over the grazing season. This paper explores how both host behaviours and immunity influence macro-parasite transmission in a spatially and temporally heterogeneous environment. The magnitude and timing of parasite outbreaks is influenced by host immunity and behaviour, and the interactions between them; the incorporation of both regulatory processes is required to fully understand transmission dynamics. Understanding of both physiological and behavioural defence strategies will aid the development of novel approaches for control.     

Absence of a Context‐General Behavioural Syndrome in a Solitary Predator

The correlation of seemingly unrelated behaviours into behavioural syndromes has been established in a wide range of species and taxa. However, most studies report on short‐term behavioural correlations without insight into individual consistency or temporal stability of the behavioural syndrome. Here, we examine the individual repeatability of single behaviours, and the presence and temporal stability of a context‐general behavioural syndrome in a solitary piscivorous predator, the pike (Esox lucius). Behavioural measurements on the same individuals were quantified independently through time and across three contexts: activity in the presence of a competitor, exploration of a novel environment and boldness under predation risk. There was no indication of a temporally stable behavioural syndrome, consisting of boldness, activity and exploration, nor were individuals consistent in the separate behaviours, contradicting the general assertion of its taxonomic prevalence. Furthermore, the study did not provide support for size or growth‐dependent behaviour in this size‐dimorphic species in conditions of limited food availability. The study highlights the importance of independent multiple observations of individual behaviour across time or contexts when measuring behavioural repeatability and covariation.     

Life history interactions with environmental conditions in a host–parasite relationship and the parasite's mode of transmission

The microsporidian parasite Edhazardia aedis is capable of vertical or horizontal transmission among individuals of its host, the mosquito Aedes aegypti, and either mode of transmission may follow the other. We show that following the horizontal infection of host larvae, the parasite's subsequent mode of transmission largely depends on host life history traits and their responses to different environmental conditions. In two experiments the intensity of larval exposure to infection and the amount of food available to them were simultaneously manipulated. One experiment followed the dynamics of host development and the parasite's production of spores while the other estimated the outcome of their relationship. Host life history traits varied widely across treatment conditions while those of the parasite did not. Of particular importance was the host's larval growth rate. Horizontal rather than vertical transmission by the parasite was more likely as low food and high dose conditions favoured slower larval growth rates. This pattern of transmission behaviour with host growth rate can be considered in terms of reproductive value: the potential vertical transmission success that female mosquitoes offer the parasite decreases as larval growth rates slow and makes them more attractive to exploitation for horizontal transmission (requiring host mortality). However, the lack of variation in the parasite's life history traits gave rise in some conditions to low estimates for both its vertical and horizontal transmission success. We suggest that the unresponsive behaviour of the parasite's life history traits reflects a bet-hedging strategy to reduce variance in its overall transmission success in the unpredictable environmental conditions and host larval growth rates that this parasite encounters in nature.     

Weaving animal temperament into food webs: implications for biodiversity

Recent studies into community level dynamics are revealing processes and patterns that underpin the biodiversity and complexity of natural ecosystems. Theoretical food webs have suggested that species‐rich and highly complex communities are inherently unstable, but incorporating certain characteristics of empirical communities, such as allometric body size scaling and non‐random interaction distributions, have been shown to enhance stability and facilitate species coexistence. Incorporating individual level traits and variability into food web theory is seen as a future pathway for this research and our growing knowledge of individual behaviours, in the form of temperament (or personality) traits, can inform the direction of this research. Temperament traits are consistent differences in behaviour between individuals, which are repeatable across time and/or across ecological contexts, such as aggressive or boldness behaviours that commonly differ between individuals of the same species. These traits, under the framework of behavioural reaction norms, show both individual consistency as well as contextual and phenotypic plasticity. This is likely to contribute significantly to the effects of individual trait variability and adaptive trophic behaviour on the structure and dynamics of food webs, which are apparently stabilizing. Exploring the role of temperament in the context of community ecology is a unique opportunity for cross‐pollination between ecological fields, and can provide new insights into community stability and biodiversity.     

Host behaviour drives parasite genetics at multiple geographic scales: population genetics of the chewing louse,Thomomydoecus minor

Pocket gophers and their symbiotic chewing lice form a host–parasite assemblage known for a high degree of cophylogeny, thought to be driven by life history parameters of both host and parasite that make host switching difficult. However, little work to date has focused on determining whether these life histories actually impact louse populations at the very fine scale of louse infrapopulations (individuals on a single host) at the same or at nearby host localities. We used microsatellite and mtDNA sequence data to make comparisons of chewing‐louse (Thomomydoecus minor) population subdivision over time and over geographic space where there are different potential amounts of host interaction surrounding a zone of contact between two hybridizing pocket‐gopher subspecies. We found that chewing lice had high levels of population isolation consistent with a paucity of horizontal transmission even at the very fine geographic scale of a single alfalfa field. We also found marked genetic discontinuity in louse populations corresponding with host subspecies and little, if any, admixture in the louse genetic groups even though the lice are closely related. The correlation of louse infrapopulation differentiation with host interaction at multiple scales, including across a discontinuity in pocket‐gopher habitat, suggests that host behaviour is the primary driver of parasite genetics. This observation makes sense in light of the life histories of both chewing lice and pocket gophers and provides a powerful explanation for the well‐documented pattern of parallel cladogenesis in pocket gophers and chewing lice.     

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.     

Innovation as part of a wider behavioural syndrome in the guppy: The effect of sex and body size

Recent work on animal personalities has shown that individuals within populations often differ consistently in various types of behaviour and that many of these behaviours correlate among individuals to form behavioural syndromes. Individuals of certain species have also been shown to differ in their rate of behavioural innovation in arriving at novel solutions to new and existing problems (e.g., mazes, novel foods). Here, we investigate whether behaviours traditionally studied in personality research are correlated with individual rates of innovation as part of a wider behavioural syndrome. Guppies (Poecilia reticulata) of both sexes from three different wild population sources were assessed: (a) exploration of an open area; (b) speed through a three‐dimensional maze; (c) investigation of a novel object; and (d) attraction to a novel food. The covariance structure (syndrome structure) was examined using structural equation modelling. The best model separated behaviours relating to activity in all contexts from rates of exploration/investigation and innovation. Innovative behaviour (utilizing new food and moving through a novel area) in these fish therefore forms part of the same syndrome as the traditional shy‐bold continuum (exploration of an open area and investigation of a novel object) found in many animal personality studies. There were no clear differences in innovation or syndrome structure between the sexes, or between the three different populations. However, body size was implicated as part of the behavioural syndrome structure, and because body size is highly correlated with age in guppies, this suggests that individual behavioural differences in personality/innovation in guppies may largely be driven by developmental state.     

Host and parasite life history interplay to yield divergent population genetic structures in two ectoparasites living on the same bat species

Host–parasite interactions are ubiquitous in nature. However, how parasite population genetic structure is shaped by the interaction between host and parasite life history remains understudied. Studies comparing multiple parasites infecting a single host can be used to investigate how different parasite life history traits interplay with host behaviour and life history. In this study, we used 10 newly developed microsatellite loci to investigate the genetic structure of a parasitic bat fly (Basilia nana). Its host, the Bechstein's bat (Myotis bechsteinii), has a social system and roosting behaviour that restrict opportunities for parasite transmission. We compared fly genetic structure to that of the host and another parasite, the wing‐mite, Spinturnix bechsteini. We found little spatial or temporal genetic structure in B. nana, suggesting a large, stable population with frequent genetic exchange between fly populations from different bat colonies. This contrasts sharply with the genetic structure of the wing‐mite, which is highly substructured between the same bat colonies as well as temporally unstable. Our results suggest that although host and parasite life history interact to yield similar transmission patterns in both parasite species, the level of gene flow and eventual spatiotemporal genetic stability is differentially affected. This can be explained by the differences in generation time and winter survival between the flies and wing‐mites. Our study thus exemplifies that the population genetic structure of parasites on a single host can vary strongly as a result of how their individual life history characteristics interact with host behaviour and life history traits.     

Condition-dependent virulence in a horizontally and vertically transmitted bacterial parasite

Virulence is a key component of parasite fitness. Its expression and selective value may not only depend on the features of the parasite's life cycle, but also on host genotype or environmental conditions. Using the freshwater ciliate Paramecium caudatum and its endonuclear bacterial parasite Holospora undulata , we measured variation in virulence (reduction in host division and survival), parasite load and fidelity of vertical transmission for (i) different stages of infection (associated with different opportunities for vertical and horizontal transmission), (ii) different host clones, and (iii) two food conditions. Later stages of infection dedicated to horizontal transmission were more virulent than earlier stages which rely on vertical transmission only. Besides, investment in horizontal transmission decreased the efficacy of vertical transmission, indicating a tradeoff between the two pathways. This may explain the phenotypic plasticity of transmission mode of this parasite. To some extent, virulence, parasite load and transmission fidelity varied with host clone identity and food treatment (higher virulence at low food). These results suggest that virulence is not a constant property of the parasite, and that a single (and simple) relationship between virulence and transmission does not exist.     

Inspection behaviour and inter-individual cooperation in juvenile qingbo: the effects of prior predator exposure and food deprivation

The predation pressure and food availability to which individuals are exposed during their life histories shape inspection behaviour in animals. In this study, we aimed to test whether such behaviours varied with prior experience (predation, starvation or both treatments) or measurement condition (with or without the presence of a predator; here, the snakehead fish, Channa argus) in the fish species Spinibarbus sinensis, known as qingbo. Unexpectedly, prior predator experience showed no significant effect on inspection behaviour as demonstrated by either the frequency or the duration of each activity outside shelter or on cooperation as demonstrated by the inter-individual distance or synchronization of speed. This may have been due to the different adjustments in behaviour among individuals (more shelter use vs. more inspection), the predator treatment used in the present study (exposure to caged predator rather than direct predation) and/or a species-specific strategy in the qingbo. The starved fish displayed shorter inspection latency, increased inspection behaviour and greater cooperation when measured without the predator; however, when measured in the presence of the predator, the starved fish showed increased inspection frequency but shorter inspection duration, possibly due to the compromise between energy needs and predation risk. Similar to those of the predation group, the fish from the double-treated group showed no difference in inspection behaviour compared to the control group under the predator-absent condition, while the high-frequency, short-duration inspection behaviours remained the same as in the starved group. These findings suggested that the adjustment of inspection behaviour and related cooperation are rather complicated according to either predator experience or food deprivation, partially due to the inter-individual differences in behavioural adjustment and/or different environmental conditions.     

Host behaviour alteration by its parasite: from brain gene expression to functional test

Many parasites with complex life cycles modify their intermediate hosts'' behaviour, presumably to increase transmission to their final host. The threespine stickleback (Gasterosteus aculeatus) is an intermediate host in the cestode Schistocephalus solidus life cycle, which ends in an avian host, and shows increased risky behaviours when infected. We studied brain gene expression profiles of sticklebacks infected with S. solidus to determine the proximal causes of these behavioural alterations. We show that infected fish have altered expression levels in genes involved in the inositol pathway. We thus tested the functional implication of this pathway and successfully rescued normal behaviours in infected sticklebacks using lithium exposure. We also show that exposed but uninfected fish have a distinct gene expression profile from both infected fish and control individuals, allowing us to separate gene activity related to parasite exposure from consequences of a successful infection. Finally, we find that selective serotonin reuptake inhibitor-treated sticklebacks and infected fish do not have similarly altered gene expression, despite their comparable behaviours, suggesting that the serotonin pathway is probably not the main driver of phenotypic changes in infected sticklebacks. Taken together, our results allow us to predict that if S. solidus directly manipulates its host, it could target the inositol pathway.     

Differential influence of Pomphorhynchus laevis (Acanthocephala) on brain serotonergic activity in two congeneric host species

The physiological mechanisms by which parasites with complex life cycles manipulate the behaviour of their intermediate hosts are still poorly understood. In Burgundy, eastern France, the acanthocephalan parasite Pomphorhynchus laevis inverses reaction to light in its amphipod host Gammarus pulex, but not in Gammarus roeseli, a recent invasive species. Here, we show that this difference in manipulation actually reflects a difference in the ability of the parasite to alter brain serotonergic (5-HT) activity of the two host species. Injection of 5-HT in uninfected individuals of both host species was sufficient to inverse reaction to light. However, a difference in brain 5-HT immunocytochemical staining levels between infected and uninfected individuals was observed only in G. pulex. Local adaptation of the parasite to the local host species might explain its inability to manipulate the behaviour and nervous system of the invasive species.     

Natural selection,plasticity and the emergence of a behavioural syndrome in the wild

Individuals often show consistent behavioural differences where behaviours can form integrated units across functionally different contexts. However, the factors causing and maintaining behavioural syndromes in natural populations remain poorly understood. In this study, we provide evidence for the emergence of a behavioural syndrome during the first months of life in wild brown trout (Salmo trutta). Behavioural traits of trout were scored before and after a 2‐month interval covering a major survival bottleneck, whereupon the consistency and covariance of behaviours were analysed. We found that selection favoured individuals with high activity levels in an open‐field context, a personality trait consistent throughout the duration of the experiment. In addition, a behavioural syndrome emerged over the 2 months in the wild, linking activity to aggressiveness and exploration tendency. These novel results suggest that behavioural syndromes can emerge rapidly in nature from interaction between natural selection and behavioural plasticity affecting single behaviours.     

Developmental programming: Cumulative effects of increased pre-hatching corticosterone levels and post-hatching unpredictable food availability on physiology and behaviour in adulthood

Prolonged exposure to stress during development can have long-term detrimental effects on health and wellbeing. However, the environmental matching hypothesis proposes that developmental stress programs physiology and behaviour in an adaptive way that can enhance fitness if early environments match those experienced later in life. Most research has focused on the harmful effects that stress during a single period in early life may exert in adulthood. In this study, we tested the potential additive and beneficial effects that stress experienced during both pre- and post-hatching development may have on adult physiology and behaviour. Japanese quail experienced different stress-related treatments across two developmental life stages: pre-hatching corticosterone (CORT) injection, post-hatching unpredictable food availability, both pre- and post-hatching treatments, or control. In adulthood, we determined quails' acute stress response, neophobia and novel environment exploration. The pre-hatching CORT treatment resulted in attenuated physiological responses to an acute stressor, increased activity levels and exploration in a novel environment. Post-hatching unpredictable food availability decreased adults' latency to feed. Furthermore, there were cumulative effects of these treatments across the two developmental stages: quail subjected to both pre- and post-hatching treatments were the most explorative and risk-taking of all treatment groups. Such responses to novel environments could enhance survival in unpredictable environments in later life. Our data also suggest that these behavioural responses may have been mediated by long-term physiological programming of the adrenocortical stress response, creating phenotypes that could exhibit fitness-enhancing behaviours in a changing environment.     

Differential propagation of the metazoan parasite Myxobolus cerebralis by Limnodrilus hoffmeisteri, Ilyodrilus templetoni, and genetically distinct strains of Tubifex tubifex

Whirling disease, caused by the parasite Myxobolus cerebralis, has infected rainbow trout (Oncorhynchus mykiss) and other salmonid fish in the western United States, often with devastating results to native populations but without a discernible spatial pattern. The parasite develops in a complex 2-host system in which the aquatic oligochaete Tubifex tubifex is an obligate host. Because substantial differences in whirling disease severity in different areas of North America did not seem explainable by environmental factors or features of the parasite or its fish host, we sought to determine whether ecological or genetic variation within oligochaete host populations may be responsible. We found large differences in compatibility between the parasite and various laboratory strains of T. tubifex that were established from geographic regions with different whirling disease histories. Moreover, 2 closely related species of tubificids, Limnodrilus hoffmeisteri and Ilyodrilus templetoni, which occur naturally in mixed species assemblages with T. tubifex, were incompatible with M. cerebralis. Virulence of the parasite was directly correlated with the numbers of triactinomyxon spores that developed within each strain of T. tubifex. Thus, the level of virulence was directly related to the compatibility between the host strain and the parasite. Genetic analyses revealed relationships that were in agreement with the level of parasite production. Differences in compatibilities between oligochaetes and M. cerebralis may contribute to the spatial variance in the severity of the disease among salmonid populations.     

Brain‐encysting trematodes and altered monoamine activity in naturally infected killifish Fundulus parvipinnis

This paper presents novel evidence to address mechanisms by which trematode parasites effect behavioural changes in naturally infected fish hosts. California killifish Fundulus parvipinnis infected with the brain‐encysting trematode Euhaplorchis californiensis display conspicuous swimming behaviours that render them 30 times more likely to be eaten by birds, the parasite's final host. Prevalence of E. californiensis reaches nearly 100% in most F. parvipinnis populations, with parasite biomass constituting almost 2% of F. parvipinnis biomass in some locations. Despite having thousands of cysts on their brains, infected fish grow and mature at rates comparable to those of uninfected populations. The lack of general pathology combined with the specificity of the altered behaviours suggests that the behavioural changes are due to parasite manipulation. The monoamine neurotransmitters serotonin and dopamine, which control locomotion and social behaviour in fishes and other vertebrates, were examined to explore the underlying mechanisms of this behaviour modification. Whereas previous studies were similarly conducted with experimentally infected fish, in this study, brain dopaminergic and serotonergic activity were analysed in naturally infected fish to assess how E. californiensis may alter F. parvipinnis monoamines in a naturally occurring system. A parasite density‐associated decrease in serotonergic activity occurred in the hippocampus of naturally infected fish, as well as a decrease in dopaminergic activity in the raphe nuclei, suggesting that E. californiensis inhibits serotonin and dopamine signaling in naturally infected F. parvipinnis. The neurochemical profile of infected fish is consistent with the hypothesis that E. californiensis affects brain monoaminergic systems in order to induce impulse‐driven, active, and aggressive behaviour in its hosts.     

Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare

Parasites with complex life cycles, relying on trophic transmission to a definitive host, very often induce changes in the behaviour or appearance of their intermediate hosts. Because this usually makes the intermediate host vulnerable to predation by the definitive host, it is generally assumed that the parasite's transmission rate is increased, and that the modification of the host is, therefore, of great adaptive significance to the parasite. However, in the ecological "real world" other predators unsuitable as hosts may just as well take advantage of the facilitation process and significantly erode the benefit of host manipulation. Here we show that the intertidal New Zealand cockle (Austrovenus stutchburyi), manipulated by its echinostome trematode (Curtuteria australis) to rest on the sediment surface fully exposed to predation from the avian definitive host, is also subject to sublethal predation from a benthic feeding fish (Notolabrus celidotus, Labridae). The fish is targeting only the cockle-foot, in which the parasite preferentially encysts, reducing the infection intensity of manipulated cockles to levels comparable with those in non-manipulated, buried cockles. Based on the frequency and intensity of the foot cropping and predation rates on surfaced cockles by avian hosts, it is estimated that 2.5% of the parasite population in manipulated cockles is transmitted successfully whereas 17.1% is lost to fish. We argue that the adaptive significance of manipulation in the present system depends critically on the feeding behaviour of the definitive host. If cockles constitute the majority of prey items, there will be selection against manipulation. If manipulated cockles are taken as an easily accessible supplement to a diet composed mostly of other prey organisms, behavioural manipulation of the cockle host appears a high risk, high profit transmission strategy. Both these feeding behaviours of birds are known to occur in the field.     

Lifespan and age,but not residual reproductive value or condition,are related to behaviour in wild field crickets

Individuals frequently show long‐term consistency in behaviour over their lifetimes, referred to as “personality.” Various models, revolving around the use of resources and how they are valued by individuals, attempt to explain the maintenance of these different behavioural types within a population, and evaluating them is the key for understanding the evolution of behavioural variation. The pace‐of‐life syndrome hypothesis suggests that differences in personalities result from divergent life‐history strategies, with more active/risk‐taking individuals reproducing rapidly but dying young. However, studies of wild animals provide only limited support for key elements of this and related hypotheses, such as a negative relationship between residual reproductive value and activity. Furthermore, alternative models make divergent predictions regarding the relationship between risk‐taking behaviours and variables consistent in the short‐term, such as condition. To test these predictions, we regularly measured willingness to leave a shelter and the activity level of wild adult field crickets (Gryllus campestris) at both short and long intervals over their entire adult lives. We found some support for a pace‐of‐life syndrome influencing personality, as lifespan was negatively related to willingness to leave the shelter and activity. Crickets did not appear to protect their “assets” however, as estimates of residual reproductive value were not related to behaviour. Although there was considerable variance attributed to the short‐term consistency, neither trait was affected by phenotypic condition, failing to support either of the models we tested. Our study confirms that behaviours may covary with some life‐history traits and highlights the scales of temporal consistency that are more difficult to explain.