Anti-parasite Behaviour Research Articles

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.

Reversible Cysteine Protease Inhibitors Show Promise for a Chagas Disease Cure

The cysteine protease cruzipain is essential for the viability, infectivity, and virulence of Trypanosoma cruzi, the causative agent of Chagas disease. Thus, inhibitors of cruzipain are considered promising anti-T. cruzi chemotherapeutic agents. Reversible cruzipain inhibitors containing a nitrile "warhead" were prepared and demonstrated 50% inhibitory concentrations (IC50s) as potent as 1 nM in baculovirus-generated cruzipain enzyme assays. In epimastigote and intracellular amastigote in vitro assays, the most potent compounds demonstrated antiparasitic behavior in the 5 to 10 μM IC50 range; however, trypomastigote production from the amastigote form was ∼90 to 95% inhibited at 2 μM. Two key compounds, Cz007 and Cz008, with IC50s of 1.1 and 1.8 nM, respectively, against the recombinant enzyme were tested in a murine model of acute T. cruzi infection, with oral dosing in chow for 28 days at doses from 3 to 50 mg/kg of body weight. At 3 mg/kg of Cz007 and 3 mg/kg of Cz008, the blood parasitemia areas under the concentration-time curves were 16% and 25% of the untreated group, respectively. At sacrifice, 24 days after immunosuppression with cyclophosphamide, parasite presence in blood, heart, and esophagus was evaluated. Based on negative quantitative PCR results in all three tissues, cure rates in surviving animals were 90% for Cz007 at 3 mg/kg, 78% for Cz008 at 3 mg/kg, and 71% for benznidazole, the control compound, at 50 mg/kg.

Nest Sanitation as the Evolutionary Background for Egg Ejection Behaviour and the Role of Motivation for Object Removal

Higher interclutch colour variation can evolve under the pressure of brood parasitism to increase the detection of parasitic eggs. Nest sanitation could be a prerequisite for the evolution of anti-parasite defence in terms of egg ejection. In this respect, we used nest sanitation behaviour as a tool to identify: i) motivation and its underlying function and, ii) which features provoke ejection behaviour. Therefore, we experimentally tested whether size, colour or shape may influence ejection behaviour using artificial flat objects. We found a high interclutch variation in egg colouration and egg size in our tree sparrow (Passer montanus) population. Using colour and size we were in fact able to predict clutch affiliation for each egg. Our experiments further revealed the existence of direct anti-parasite behaviours and birds are able to recognise conspecific eggs, since only experimentally-deposited eggs have been removed. Moreover, experiments with different objects revealed that the motivation of tree sparrows to remove experimental objects from their nests was highest during egg laying for objects of varying size, most likely because of parasitism risk at this breeding stage. In contrary, motivation to remove white objects and objects with edges was higher during incubation stage as behavioural patterns connected to hatching started to emerge. The fact that rejection rate of our flat objects was higher than real egg ejection, suggests that egg ejection in tree sparrows and probably more general in small passerines, to be limited by elevated costs to eject eggs with their beaks. The presence of anti-parasite behaviour supports our suggestion that brood parasitism causes variation in egg features, as we have found that tree sparrows can recognise and reject conspecific eggs in their clutch. In conclusion, in tree sparrows it seems that nest sanitation plays a key role in the evolution of the removal of parasitic eggs.

The parasite‐driven‐wedge model of parapatric speciation

AbstractThe parasite‐driven‐wedge model provides a mechanism of parapatric speciation (the evolution of adjacent species across the range of an ancestral species without allopatric separation). Regionally localized coevolutionary races between parasites and their hosts result in three locally adaptive antiparasite behaviors: mating and other social preference for local conspecifics, avoidance of nonlocal conspecifics and philopatry (limited dispersal). These three behaviors comprise behavioral immunity. They become linked within individuals through linkage disequilibrium. Genetic immunity to local parasites also links through the same genetic mechanism with the traits of behavioral immunity. These linked traits are mutually reinforcing in that as any one increases in frequency due to its adaptiveness, the others do as well. Also, preference for locals is self‐reinforcing because both the locals preferred and those preferring them have the same preference. These events create a wedge and associated boundaries that effectively fractionate and diversify the original range of a species, leading to the genesis of contiguous multiple species from one. The higher the parasite stress in a region, the greater the frequency and intensity of the parasite‐driven wedge in splitting species. We do not deny an important role for allopatric speciation, but argue that parasite‐driven parapatric processes will be relatively predominant in regions of high parasite adversity (e.g. low latitudes), leading to the high diversity of species in the regions. The fractionation of host populations through the parasite‐driven wedge also diversifies parasites, leading to even greater geographic localization of host–parasite races. Methods are discussed for empirically distinguishing parasite‐driven parapatric speciation and allopatric speciation. We hypothesize that host coevolution with beneficial symbionts may also be an engine of parapatric speciation by way of a wedge‐like process.

Faecal avoidance and selective foraging: do wild mice have the luxury to avoid faeces?

Host–parasite interactions are a key determinant of the population dynamics of wild animals, and behaviours that reduce parasite transmission and infection may be important for improving host fitness. While antiparasite behaviours have been demonstrated in laboratory animals and domesticated ungulates, whether these behaviours operate in the wild is poorly understood. Therefore, examining antiparasite behaviours in natural populations is crucial for understanding their ecological significance. In this study, we examined whether two wild rodents (white-footed mice, Peromyscus leucopus, and deer mice, Peromyscus maniculatus), selectively foraged away from conspecific faeces or avoided faeces altogether, and whether faecal gastrointestinal parasite status affected their behaviour. We also tested whether wild mice, when nesting, avoided using material that had previously been used by healthy or parasite-infected conspecifics. Our results, in contrast to laboratory mouse studies, suggest that wild mice do not demonstrate faecal avoidance, selective foraging or selective use of nesting material; they preferred being near faeces and did not differentiate between faeces from parasitized and uninfected conspecifics. Behavioural avoidance to reduce parasite infection may still represent an important strategy; however, mice in our study population appeared to favour the opportunity to feed and nest over the risks of coming into contact with faecal-transmitted parasites. Furthermore, the presence of conspecific faeces may actually provide a positive cue of a good foraging or nesting location. Ultimately, balancing the trade-off of performing antiparasite behaviours to reduce infection with missing an important feeding or nesting opportunity may be very different for animals in the wild facing complex and stochastic environments.

Infection deflection: hosts control parasite location with behaviour to improve tolerance

Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behaviours affect infection location within the host's body and whether parasite distribution ultimately affects tolerance of infection. To assess these questions, we exposed both anaesthetized (no behaviour) and non-anaesthetized Hyla femoralis tadpoles to plagiorchiid cercariae (larval trematodes), and quantified resistance, tolerance (relationship between mass change and infection intensity) and encystment location. Non-anaesthetized tadpoles had significantly more infections in their tail region than anaesthetized tadpoles, which had the majority of their infections in the head. This pattern indicates that parasites preferred to infect the head, but that hosts shunted infections to the tail when possible. Furthermore, there was a significant effect of encystment location on tolerance, with head-infected tadpoles having poorer tolerance to infection than tail-infected tadpoles. Variance partitioning suggests that, among infected tadpoles, behaviour contributed more to tolerance than resistance. These results suggest that, in addition to using behaviour to resist parasites, H. femoralis tadpoles also use behaviour to enhance infection tolerance by deflecting infections posteriorly, away from their vital sensory organs. These findings highlight the need to assess how widespread and important behaviour is to the tolerance of infections.

Factors Affecting the Presence and Abundance of Generalist Ectoparasites in Nests of Three Sympatric Hole-Nesting Bird Species

Abstract. Nesting cavities constitute micro-environments very likely to be colonized by ectoparasites which feed on blood of the incubating female and the nestlings. Given the negative impact of ectoparasites on nestlings there will be selection on hosts to minimize ectoparasite loads through behavioural defenses. We have addressed the implications of ectoparasitism in three sympatric avian cavity-nesters, namely Pied Flycatchers Ficedula hypoleuca, Blue Tits Cyanistes caeruleus and Nuthatches Sitta europaea, to explore if differences in prevalence and abundance of generalist ectoparasites (blowflies, fleas and mites) can be related to interspecific differences in their nest size, nest composition and cavity microclimate. Furthermore, we have aimed at detecting if interspecific variation in the incidence and intensity of anti-parasite behaviours is a consequence of the abundance of ectoparasites. Differences in nest composition among host species appear not to be the main factor explaining ectoparasite lo...

THE EFFECTS OF PARASITES ON HUMAN BEHAVIOUR: AN EVOLUTIONARY PERSPECTIVE

Parasites and predators possess serious threats to humans throughout our evolutionary history. Although the impact of predators in modern world is lower than previously, parasites still influence morbidity and mortality of contemporary humans. From the evolutionary perspective, selective pressures caused by parasites should favour individuals that successfully avoid objects/subjects which transmit parasitic diseases and/or those who are successful in combats with them. There is growing evidence for the existence of evolved anti-parasite behaviours in animals, beginning with invertebrates and ending with primates. Avoidance of infected individuals, grooming and self-medication are most common behavioural strategies that are believed to reduce the transmission of parasites. Here we review recent evidence suggesting that several behavioural and emotional traits in humans evolved as a response to selective pressure caused by parasites. Disgust sensitivity and pathogen threat may be a mechanism that generates both a cross-cultural variation in preferences for certain facial traits, as well as drivers of religious diversity, political stability of countries, parenting cognitive abilities and prevalence of extraversion and openness to new ideas. Finally, we declare areas for a future research based on questions guided by the evolutionary perspective. Key words: evolution, human, parasites, psychology.

Antiparasite behavior

Antiparasite behavior

Infectious personalities: behavioural syndromes and disease risk in larval amphibians

Behavioural consistency or predictability through time and/or different contexts ('syndromes' or 'personality types') is likely to have substantial influence on animal life histories and fitness. Consequently, there is much interest in the forces driving and maintaining various syndromes. Individual host behaviours have been associated with susceptibility to parasitism, yet the role of pre-existing personality types in acquiring infections has not been investigated experimentally. Using a larval amphibian-trematode parasite model system, we report that tadpoles generally showed consistency in their activity level in response to both novel food and parasite exposure. Not only were individual activity level and exploration in the novel food context correlated with each other and with anti-parasite behaviour, all three were significant predictors of host parasite load. This is the first empirical demonstration that host behaviours in other contexts are related to behaviours mitigating infection risk and, ultimately, host parasite load. We suggest that this system illustrates how reliably high levels of activity and exploratory behaviour in different contexts might maximize both energy acquisition and resistance to trematode parasites. Such benefits could drive selection for the behavioural syndrome seen here owing to the life histories and ecological circumstances typical of wood frog (Lithobates sylvaticus) larvae.

Nest defence against avian brood parasites is promoted by egg-removal events in a cowbird–host system

Recent studies of birds have found that the antiparasite behaviour of host species is modified by social learning. We tested whether individual or social learning modifies the nest defence of yellow warblers, Setophaga petechia, against the parasitic brown-headed cowbird, Molothrus ater. Using field experiments, we exposed warblers to simulated events of nest parasitism and predation, or allowed them to observe conspecifics mobbing a cowbird. Intensity of nest defence by yellow warblers was greater after simulated threats at their nest than after they had observed mobbing of cowbirds by conspecifics. Warblers defended their nests more aggressively when they perceived a cowbird as an egg predator rather than as a parasite. Higher predation than parasitism frequencies probably explain the more prompt change in defence when cowbirds were encountered as egg predators. Annual fluctuations in frequencies of both parasitism and predation suggest that defence acquired via observing conspecifics may contain outdated information and probably explains the warblers’ reliance on individually learned over socially learned defence.

Seasonal increase in intensity of nest defence against little cuckoos by Japanese bush warblers

Avian brood parasitism reduces the reproductive success of hosts. Thus, hosts have evolved antiparasite strategies such as rejection of parasitic eggs and aggressive nest defence against brood parasites. Japanese bush warblers, Cettia diphone , do not reject the parasitic eggs of little cuckoos, Cuculus poliocephalus , because their eggs mimic warblers’ eggs. To examine whether Japanese bush warblers show nest defence behaviour against their parasite, I investigated the responses of the warblers to a little cuckoo dummy. Japanese bush warblers are residents, while little cuckoos are summer visitors; thus, the warblers start breeding earlier than the cuckoos. Accordingly, the risk of being parasitized increases as the season progresses. Therefore, I also examined whether the intensity of nest defence differed before and after cuckoo arrival. Japanese bush warblers showed remarkably aggressive responses to the cuckoo dummy, and levels of aggression were higher after the cuckoo arrived. These results suggest that Japanese bush warblers adaptively adjust their nest defence behaviour in response to increased risk of being parasitized. This study indicates that differences in migratory habits between hosts and brood parasites produce seasonal changes in antiparasite behaviour.

Brood parasitism selects for no defence in a cuckoo host

In coevolutionary arms races, like between cuckoos and their hosts, it is easy to understand why the host is under selection favouring anti-parasitism behaviour, such as egg rejection, which can lead to parasites evolving remarkable adaptations to 'trick' their host, such as mimetic eggs. But what about cases where the cuckoo egg is not mimetic and where the host does not act against it? Classically, such apparently non-adaptive behaviour is put down to evolutionary lag: given enough time, egg mimicry and parasite avoidance strategies will evolve. An alternative is that absence of egg mimicry and of anti-parasite behaviour is stable. Such stability is at first sight highly paradoxical. I show, using both field and experimental data to parametrize a simulation model, that the absence of defence behaviour by Cape bulbuls (Pycnonotus capensis) against parasitic eggs of the Jacobin cuckoo (Clamator jacobinus) is optimal behaviour. The cuckoo has evolved massive eggs (double the size of bulbul eggs) with thick shells, making it very hard or impossible for the host to eject the cuckoo egg. The host could still avoid brood parasitism by nest desertion. However, higher predation and parasitism risks later in the season makes desertion more costly than accepting the cuckoo egg, a strategy aided by the fact that many cuckoo eggs are incorrectly timed, so do not hatch in time and hence do not reduce host fitness to zero. Selection will therefore prevent the continuation of any coevolutionary arms race. Non-mimetic eggs and absence of defence strategies against cuckoo eggs will be the stable, if at first sight paradoxical, result.

Neatness depends on season, age, and sex in Iberian ibex Capra pyrenaica

Heterogeneity in host compatibility is one of the main hypotheses proposed to explain uneven resistance to parasites and uneven parasite load between hosts. It suggests that differences between hosts modulate their predispositions as suitable environments for their potential parasites. Interesting studies of antiparasitic behavior have reported the existence of behavioral traits that are capable of removing foreign particles and of reducing the success of parasitic infections. These traits favor host neatness, although little is known about the heterogeneity of neatness. We used a standardized pseudoinfection with pseudoectoparasites (PEPs) to test the effects of sex, age, and season on the loss of PEPs by hosts as a means of exploring the factors determining neatness in the Iberian ibex Capra pyrenaica. Behavioral observations were also performed to analyze investment in antiparasitic behavior in terms of sex, age, and season. The life span of PEPs peaked in the period December--January, decreased with host age, and was longer in females than in males. Investment in antiparasitic behavior is also associated with both sex and age and season but in a different pattern with interactions between such factors. Our results disagree with the hypothesis that small-bodied animals should be less compatible to carry contact-transmitted particles, such as ectoparasites, in comparison with larger animals. This preexisting hypothesis is thus an inadequate way of predicting host neatness. Consequently, our experiment underlines the importance that nonimmunological traits play in determining heterogeneity in host compatibility to contact-transmitted foreign bodies and helps improve understanding of neatness and of host--parasite systems. Copyright 2011, Oxford University Press.

Video analysis of host–parasite interactions in nests of Darwin’s finches

AbstractParasites place their hosts under strong selection for adaptive traits that increase parasite resistance. The initial impact of invasive parasites has rarely been observed and can be particularly strong on naïve hosts with limited prior exposure to parasites.Philornis downsiis an introduced fly to the Galapagos Islands whose parasitic larvae cause high mortality in nestlings of Darwin's finches. We used a within-nest camera system and nest monitoring data to examine this new host–parasite interaction in the wild. ManyP. downsiflies entered finch nests with incubated eggs or nestlings but only when parent finches were not present. ParasiticP. downsilarvae were observed to emerge from the nest base at night to feed both internally and externally on nestlings. Adult and nestling Darwin’s finches exhibit grooming and avoidance behaviours in the presence ofP. downsiparasites. Specifically, in nests with high parasite intensity, nestlings increased self-preening behaviour, ate larvae and stood on top of one another. Female finches probed into their nestling’s nares (first instar larvae reside in the nares) and probed into the nest base (second and third larvae reside in the nest base during the day). These findings shed light on the emergence of anti-parasite behaviour as well as host–parasite relationships after recent parasitism in a naïve host.

Beyond immunity: quantifying the effects of host anti-parasite behavior on parasite transmission

A host's first line of defense in response to the threat of parasitic infection is behavior, yet the efficacy of anti-parasite behaviors in reducing infection are rarely quantified relative to immunological defense mechanisms. Larval amphibians developing in aquatic habitats are at risk of infection from a diverse assemblage of pathogens, some of which cause substantial morbidity and mortality, suggesting that behavioral avoidance and resistance could be significant defensive strategies. To quantify the importance of anti-parasite behaviors in reducing infection, we exposed larval Pacific chorus frogs (Pseudacris regilla) to pathogenic trematodes (Ribeiroia and Echinostoma) in one of two experimental conditions: behaviorally active (unmanipulated) or behaviorally impaired (anesthetized). By quantifying both the number of successful and unsuccessful parasites, we show that host behavior reduces infection prevalence and intensity for both parasites. Anesthetized hosts were 20-39% more likely to become infected and, when infected, supported 2.8-fold more parasitic cysts. Echinostoma had a 60% lower infection success relative to the more deadly Ribeiroia and was also more vulnerable to behaviorally mediated reductions in transmission. For Ribeiroia, increases in host mass enhanced infection success, consistent with epidemiological theory, but this relationship was eroded among active hosts. Our results underscore the importance of host behavior in mitigating disease risk and suggest that, in some systems, anti-parasite behaviors can be as or more effective than immune-mediated defenses in reducing infection. Considering the severe pathologies induced by these and other pathogens of amphibians, we emphasize the value of a broader understanding of anti-parasite behaviors and how co-occurring stressors affect them.

Health Is Associated With Antiparasite Behavior and Fear of Disease-Relevant Animals in Humans

Evolutionary arms races between humans and parasites resulted in a set of behavioral adaptations that serve as parasite-avoidance mechanisms. We investigated associations among reported health of the respondent, antiparasite behavior, and sensitivity to disgust and fear of disease-relevant and irrelevant animals. Ninety-seven participants (15–19 years old) rated their fear and disgust at 25 colorful pictures of disease-relevant and disease-irrelevant invertebrates. Consistent with previous work, we found that participants reported greater fear and disgust of disease-relevant invertebrates relative to disease-irrelevant invertebrates. Better perceived health correlated with lower fear of disease-relevant invertebrates. Sensitivity to disgust correlated with reported antiparasite behaviors. Contrary to expectations, we found a positive correlation between antiparasite behavior and reported health, which suggests that antiparasite behavior influences perceived health (but not vice versa), and we found that males perform more antiparasite behaviors than females. These results support the idea that disgust and fear of disease-relevant objects are adaptive emotions that prevent contact with contagious objects, especially in individuals with low perceived health.

The association between disgust, danger and fear of macroparasites and human behaviour

Evolutionary explanations of disgust propensity propose that disgust is an adaptation which helps us to decrease the likelihood of being infected by pathogens. To test this hypothesis, we examined human fear, disgust and self-perceived danger as a response on colourful pictures of disease-relevant and disease-irrelevant invertebrates. Furthermore, we also examined a possible link between these variables and human anti-parasite behaviour. We found that participants clearly distinguished between disease-relevant and disease-irrelevant group of animals, and that females always scored higher than males. Moreover, there were associations between ratings of fear, disgust and danger and human anti-parasite behaviour. Our results support the hypothesis that human emotions and behaviours are shaped by natural selection.

How Birds Combat Ectoparasites

Birds are plagued by an impressive diversity of ectoparasites, ranging from feather-feeding lice, to feather- degrading bacteria. Many of these ectoparasites have severe negative effects on host fitness. It is therefore not surprising that selection on birds has favored a variety of possible adaptations for dealing with ectoparasites. The functional signifi- cance of some of these defenses has been well documented. Others have barely been studied, much less tested rigorously. In this article we review the evidence - or lack thereof - for many of the purported mechanisms birds have for dealing with ectoparasites. We concentrate on features of the plumage and its components, as well as anti-parasite behaviors. In some cases, we present original data from our own recent work. We make recommendations for future studies that could im- prove our understanding of this poorly known aspect of avian biology.

Cost of exposure to trematode cercariae and learned recognition and avoidance of parasitism risk by fathead minnowsPimephales promelas

Fathead minnowsPimephales promelasexposed to cercariae of the trematodeOrnithodiplostomumsp. incurred a significant mass loss 17 days after exposure to 20 or 120 cercariae. Parasite‐naïveP. promelasshowed no evidence of innate recognition or avoidance of cercariae. After a single exposure to cercariae, however, fish responded to chemical and visual cues of dead (thawed) cercariae with a reduction in activity. Encounter rate with cercariae, and hence infection rate, increased with fish activity. The data indicated that experiencedP. promelasassociated parasitism risk with novel chemical and visual cues that later triggered avoidance behaviour. Parallels and interactions between antiparasite behaviour and antipredator behaviour open new avenues for behavioural ecological research in risk‐sensitive decision‐making.