Parasite insight: assessing fitness costs, infection risks and foraging benefits relating to gastrointestinal nematodes in wild mammalian herbivores

Abstract

Mammalian herbivores are typically infected by parasitic nematodes, which are acquired through direct, faecal-oral transmission. These parasites can cause significant production losses in domestic livestock, but much less is known about impacts on wild mammalian hosts. We review three elements of parasitism from the host's perspective: fitness costs of infection, risks of infection during foraging and benefits of nutritious pasture. The majority of wildlife studies have been observational, but experimental manipulation is increasing. Treatment with anthelmintics to manipulate parasite load has revealed varied impacts of parasites on fitness variables across host species, but has not produced consistent evidence for parasite-induced anorexia or impaired body condition. Some experimental studies of infection risk have manipulated faecal contamination and detected faecal avoidance by hosts. Only two field studies have explored the trade-off between infection risk and nutritional benefit generated by avoidance of contaminated patches. Overall, field studies of costs, risks and benefits of the host-parasite relationship are limited and few have examined more than one of these elements. Parasitism has much in common with predation, and future insights into anti-parasite responses by wild hosts could be gained from the conceptual and technical developments in research on anti-predator behaviour.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Divergent strategies in faeces avoidance between two cercopithecoid primates

“…Similarly, bonobos did not avoid contaminated food that was put in contact with conspecific faeces in front of them, if the latter got covered and the food alone was presented to them [15]. Finally, it is also likely that a three-way trade-off between disgust (infection risk), hunger (energy or nutrient requirements) [11,18] and information acquisition may mediate the expression of avoidance, potentially in divergent ways depending on the type of food reward and the type of contaminant or test stimulus presented, and of course the sensory modality being invoked.…”

“…Among substrates known to harbour infectious agents, faeces are known to elicit avoidance behaviour in a wide range of animal species, including insects [8], rodents [9], ungulates [10], marsupials [11] and proboscids [12]. This is for good reason, as a multitude of infectious organisms (e.g.…”

Patterns of helminth infection in Kenyan elephant populations

“…In addition, previous studies on Rhodesian elephants have recorded much higher mean egg burden reaching 2072 with a range of 512-4382 [5]. Faecal egg counts or egg burden are often used to assess parasite burdens but have inherent pitfalls as they are subject to numerous variables that confound cause-effect relationships [43]. The few studies that have ever correlated egg burden to worm burdens have had variable outcomes [44][45][46][47].…”

Evolution of pathogen and parasite avoidance behaviours

“…These factors did not exactly mirror the transmission routes of infection but, instead, reflected different kinds of behavioural tasks involved in parasite avoidance. These six strategies for parasite avoidance may be universal, and examples in many other species can be found throughout this special edition, for example, fish avoid conspecifics of atypical appearance or with lesions [22], nematodes and primates avoid contaminated foods [18,20], mice avoid sex with infected conspecifics [19], bees are hygienic [21] and birds and ruminants avoid unhygienic environments [17,23]. Heterospecific avoidance behaviour has been rarely reported in the animal literature but could be expected to occur when other species serve as vectors or intermediate hosts of specific parasites.…”

“…A further pattern emerging from this special issue is a general shift in the field from anecdotal reports of observed behaviour to the experimental testing of hypotheses, which has proven possible in captive species as diverse as bees [21] and bonobos [20], and, in some cases, in the wild as well [22,23]. It is also exciting to see how cross-disciplinary collaboration is bearing fruit, for example, where geneticists, cell biologists and behavioural scientists are collaborating to provide a complete picture of nematode infection avoidance behaviour [18].…”