2018 ◽  
Vol 373 (1751) ◽  
pp. 20170256 ◽  
Author(s):  
Cecile Sarabian ◽  
Val Curtis ◽  
Rachel McMullan

All free-living animals are subject to intense selection pressure from parasites and pathogens resulting in behavioural adaptations that can help potential hosts to avoid falling prey to parasites. This special issue on the evolution of parasite avoidance behaviour was compiled following a Royal Society meeting in 2017. Here we have assembled contributions from a wide range of disciplines including genetics, ecology, parasitology, behavioural science, ecology, psychology and epidemiology on the disease avoidance behaviour of a wide range of species. Taking an interdisciplinary and cross-species perspective allows us to sketch out the strategies, mechanisms and consequences of parasite avoidance and to identify gaps and further questions. Parasite avoidance strategies must include avoiding parasites themselves and cues to their presence in conspecifics, heterospecifics, foods and habitat. Further, parasite avoidance behaviour can be directed at constructing parasite-retardant niches. Mechanisms of parasite avoidance behaviour are generally less well characterized, though nematodes, rodents and human studies are beginning to elucidate the genetic, hormonal and neural architecture that allows animals to recognize and respond to cues of parasite threat. While the consequences of infection are well characterized in humans, we still have much to learn about the epidemiology of parasites of other species, as well as the trade-offs that hosts make in parasite defence versus other beneficial investments like mating and foraging. Finally, in this overview we conclude that it is legitimate to use the word ‘ disgust' to describe parasite avoidance systems, in the same way that ‘fear' is used to describe animal predator avoidance systems. Understanding disgust across species offers an excellent system for investigating the strategies, mechanisms and consequences of behaviour and could be a vital contribution towards the understanding and conservation of our planet's ecosystems. This article is part of the Theo Murphy meeting issue ‘Evolution of pathogen and parasite avoidance behaviours'.


2018 ◽  
Vol 373 (1751) ◽  
pp. 20170196 ◽  
Author(s):  
Sarah E. Bush ◽  
Dale H. Clayton

Birds have many kinds of internal and external parasites, including viruses, bacteria and fungi, as well as protozoa, helminths and arthropods. Because parasites have negative effects on host fitness, selection favours the evolution of anti-parasite defences, many of which involve behaviour. We provide a brief review of anti-parasite behaviours in birds, divided into five major categories: (i) body maintenance, (ii) nest maintenance, (iii) avoidance of parasitized prey, (iv) migration and (v) tolerance. We evaluate the adaptive significance of the different behaviours and note cases in which additional research is particularly needed. We briefly consider the interaction of different behaviours, such as sunning and preening, and how behavioural defences may interact with other forms of defence, such as immune responses. We conclude by suggesting some general questions that need to be addressed concerning the nature of anti-parasite behaviour in birds. This article is part of the Theo Murphy meeting issue ‘Evolution of pathogen and parasite avoidance behaviours’.


2011 ◽  
Vol 278 (1719) ◽  
pp. 2777-2783 ◽  
Author(s):  
Oliver Krüger

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.


1991 ◽  
Vol 69 (9) ◽  
pp. 2423-2429 ◽  
Author(s):  
Ivar Folstad ◽  
Arne C. Nilssen ◽  
Odd Halvorsen ◽  
Johan Andersen

Intensities of warble fly larvae, Hypoderma tarandi (L.), were examined in slaughtered reindeer (Rangifer tarandus tarandus L.) from different summer grazing areas of Finnmark County, northern Norway. To test the hypothesis that larval abundance decreases with increase in post-calving migration distance (i.e., distance from calving grounds), herds with differing migration distances were sampled. The prevalence of infection in the total sample of 1168 animals was 99.9%. The study revealed significant differences in larval abundance among herds from different summer grazing areas. Herds with post-calving migrations have significantly lower larval abundances than herds remaining on or near the calving grounds for the whole summer. Between-herds variation in abundance of H. tarandi larvae is assumed to reflect differing densities of the infective stage (adult flies) on the herds' summer ranges. Larval abundance in a herd is in turn negatively correlated with the distance between the main larval shedding areas (i.e., calving grounds) and the areas of greatest transmission (i.e., summer pastures). These results are discussed in relation to transmission of other parasites common to Rangifer and suggest that this host's post-calving migration may be a behavioural adaptation that reduces levels of parasitic infections.


2012 ◽  
Vol 84 (3) ◽  
pp. 539-545 ◽  
Author(s):  
Fabrice Lalubin ◽  
Pierre Bize ◽  
Juan van Rooyen ◽  
Philippe Christe ◽  
Olivier Glaizot

2007 ◽  
Vol 274 (1620) ◽  
pp. 1839-1844 ◽  
Author(s):  
M.R Hutchings ◽  
K.J Knowler ◽  
R McAnulty ◽  
J.C McEwan

Livestock breeding programmes have created resistant (R) and susceptible (S) sheep that differ in their ability to control parasites through their immune function but potentially also their grazing behaviour (i.e. parasite avoidance). Using the Perendale genetic lines, we tested the hypothesis that R-sheep avoid parasites more effectively, reducing their parasite exposure/challenge, compared with S-sheep. However, in grazing systems, parasite-rich areas are also forage rich, suggesting that parasite avoidance behaviours are associated with nutritional penalties. We first created a naturally heterogeneous sward structure of gaps and tussocks and then used focal behavioural observations to quantify the sward selection of R- and S-sheep. Tussock swards were more nitrogen rich (41%), offered increased forage intake rates (32%) and contained 17 times more parasite larvae than gap swards. All the animals avoided grazing the tussock swards. However, the R-sheep grazed the tussock swards to a lesser degree than the S-sheep. We conclude that selection for genetic resistance has resulted in animals that, despite being well armed to fight parasitism through improved immune function, adopt parasite avoidance strategies with associated nutritional disadvantages. This experiment highlights the role of host behaviour in the control of parasitism and suggests that animals can be bred to avoid disease.


2014 ◽  
Vol 281 (1795) ◽  
pp. 20141785 ◽  
Author(s):  
Wendy C. Turner ◽  
Kyrre L. Kausrud ◽  
Yathin S. Krishnappa ◽  
Joris P. G. M. Cromsigt ◽  
Holly H. Ganz ◽  
...  

Parasites can shape the foraging behaviour of their hosts through cues indicating risk of infection. When cues for risk co-occur with desired traits such as forage quality, individuals face a trade-off between nutrient acquisition and parasite exposure. We evaluated how this trade-off may influence disease transmission in a 3-year experimental study of anthrax in a guild of mammalian herbivores in Etosha National Park, Namibia. At plains zebra ( Equus quagga ) carcass sites we assessed (i) carcass nutrient effects on soils and grasses, (ii) concentrations of Bacillus anthracis (BA) on grasses and in soils, and (iii) herbivore grazing behaviour, compared with control sites, using motion-sensing camera traps. We found that carcass-mediated nutrient pulses improved soil and vegetation, and that BA is found on grasses up to 2 years after death. Host foraging responses to carcass sites shifted from avoidance to attraction, and ultimately to no preference, with the strength and duration of these behavioural responses varying among herbivore species. Our results demonstrate that animal carcasses alter the environment and attract grazing hosts to parasite aggregations. This attraction may enhance transmission rates, suggesting that hosts are limited in their ability to trade off nutrient intake with parasite avoidance when relying on indirect cues.


2016 ◽  
Vol 283 (1838) ◽  
pp. 20161148 ◽  
Author(s):  
Ines Klemme ◽  
Anssi Karvonen

Cognitive abilities related to the assessment of risk improve survival. While earlier studies have examined the ability of animals to learn to avoid predators, learned parasite avoidance has received little interest. In a series of behavioural trials with the trematode parasite Diplostomum pseudospathaceum , we asked whether sea trout ( Salmo trutta trutta ) hosts show associative learning in the context of parasitism and if so, whether learning capacity is related to the likelihood of infection mediated through host personality and resistance. We show that animals are capable of learning to avoid visual cues associated with the presence of parasites. However, avoidance behaviour ceased after the likely activation of host resistance following consecutive exposures during learning, suggesting that resistance to infection outweighs avoidance. Further, we found a positive relationship between learning ability and boldness, suggesting a compensation of risky lifestyles through increased investment in cognitive abilities. By contrast, an increased risk of infection due to low resistance was not balanced by learning ability. Instead, these traits were positively related, which may be explained by inherent physiological qualities controlling both traits. Overall, the results demonstrate that parasitism, in addition to other biological interactions such as predation, is an important selective factor in the evolution of animal cognition.


2018 ◽  
Vol 373 (1751) ◽  
pp. 20170207 ◽  
Author(s):  
Tom R. Kupfer ◽  
Daniel M. T. Fessler

Currently, disgust is regarded as the main adaptation for defence against pathogens and parasites in humans. Disgust's motivational and behavioural features, including withdrawal, nausea, appetite suppression and the urge to vomit, defend effectively against ingesting or touching sources of pathogens. However, ectoparasites do not attack their hosts via ingestion, but rather actively attach themselves to the body surface. Accordingly, by itself, disgust offers limited defence against ectoparasites. We propose that, like non-human animals, humans have a distinct ectoparasite defence system that includes cutaneous sensory mechanisms, itch-generation mechanisms and grooming behaviours. The existence of adaptations for ectoparasite defence is supported by abundant evidence from non-human animals, as well as more recent evidence concerning human responses to ectoparasite cues. Several clinical disorders may be dysfunctions of the ectoparasite defence system, including some that are pathologies of grooming, such as skin picking and trichotillomania, and others, such as delusory parasitosis and trypophobia, which are pathologies of ectoparasite detection. We conclude that future research should explore both distinctions between, and overlap across, ectoparasite defence systems and pathogen avoidance systems, as doing so will not only illuminate proximate motivational systems, including disgust, but may also reveal important clinical and social consequences. This article is part of the Theo Murphy meeting issue ‘Evolution of pathogen and parasite avoidance behaviours'.


Parasitology ◽  
2019 ◽  
Vol 146 (12) ◽  
pp. 1564-1570 ◽  
Author(s):  
Monika K. Mierzejewski ◽  
Collin J. Horn ◽  
Lien T. Luong

AbstractHabitat avoidance is an anti-parasite behaviour exhibited by at-risk hosts that can minimize exposure to parasites. Because environments are often heterogeneous, host decision-making with regards to habitat use may be affected by the presence of parasites and habitat quality simultaneously. In this study we examine how the ovipositing behaviour of a cactiphilic fruit fly, Drosophila nigrospiracula, is affected by the presence of an ectoparasitic mite, Macrocheles subbadius, in conjunction with other environmental factors – specifically the presence or absence of conspecific eggs and host plant tissue. We hypothesized that the trade-off between site quality and parasite avoidance should favour ovipositing at mite-free sites even if it is of inferior quality. We found that although flies avoided mites in homogeneous environments (86% of eggs at mite-free sites), site quality overwhelmed mite avoidance. Both conspecific eggs (65% of eggs at infested sites with other Drosophila eggs) and host plant tissue (78% of eggs at infested sites with cactus) overpowered mite avoidance. Our results elucidate the context-dependent decision-making of hosts in response to the presence of parasites in variable environments, and suggest how the ecology of fear and associated trade-offs may influence the relative investment in anti-parasite behaviour in susceptible hosts.


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