An Integrated Landscape of Fear and Disgust: The Evolution of Avoidance Behaviors Amidst a Myriad of Natural Enemies

Doherty, Jean‐François; Ruehle, Brandon

doi:10.3389/fevo.2020.564343

Cited by 23 publications

(19 citation statements)

References 47 publications

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“…The question of how trait responses to parasites compare with those to predators lacks thorough testing, however, and in no small part owing to the lack of an adequate framework for drawing such comparisons. Frameworks for trait responses made in fear [13,14] and disgust [9,25] constrain the focus to trait responses to perceived risk of predation or parasitism, prior to being captured or infected. Yet, systematic examination of non-lethal effects must go beyond fear or disgust to consider the trait responses made throughout interactions.…”

Section: Introductionmentioning

confidence: 99%

Broadening the ecology of fear: non-lethal effects arise from diverse responses to predation and parasitism

et al. 2021

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Research on the ‘ecology of fear’ posits that defensive prey responses to avoid predation can cause non-lethal effects across ecological scales. Parasites also elicit defensive responses in hosts with associated non-lethal effects, which raises the longstanding, yet unresolved question of how non-lethal effects of parasites compare with those of predators. We developed a framework for systematically answering this question for all types of predator–prey and host–parasite systems. Our framework reveals likely differences in non-lethal effects not only between predators and parasites, but also between different types of predators and parasites. Trait responses should be strongest towards predators, parasitoids and parasitic castrators, but more numerous and perhaps more frequent for parasites than for predators. In a case study of larval amphibians, whose trait responses to both predators and parasites have been relatively well studied, existing data indicate that individuals generally respond more strongly and proactively to short-term predation risks than to parasitism. Apart from studies using amphibians, there have been few direct comparisons of responses to predation and parasitism, and none have incorporated responses to micropredators, parasitoids or parasitic castrators, or examined their long-term consequences. Addressing these and other data gaps highlighted by our framework can advance the field towards understanding how non-lethal effects impact prey/host population dynamics and shape food webs that contain multiple predator and parasite species.

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Section: Introductionmentioning

confidence: 99%

Broadening the ecology of fear: non-lethal effects arise from diverse responses to predation and parasitism

et al. 2021

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“…The same is true for prey of micropredators, which act like parasites by feeding without killing. This distinguishing characteristic of host-parasite and micropredator-prey interactions is not factored into the Lima and Dill (1990) framework, nor it is factored into new conceptual frameworks for disgust [15,24], a form of parasite avoidance. Surviving while being fed on by parasites or micropredators opens up a broad range of responses that slow or stop feeding, or otherwise minimize its impact.…”

Section: Existing Trait Response Frameworkmentioning

confidence: 99%

“…Here, we compare trait responses to predation and parasitism, considering how variation in their frequency and strength may drive differences in how non-lethal effects accrue in prey and hosts. Building on recent conceptual developments [21,24], our goal is to establish a quantitative foundation for estimating non-lethal effects in real ecosystems, which contain multiple predator and parasite species. We draw from consumer-resource theory to construct a general framework for estimating trait responses that accounts for the variable consumer strategies of predators and parasites.…”

Section: Introductionmentioning

confidence: 99%

Broadening the ecology of fear: non-lethal effects arise from diverse responses to predation and parasitism

Daversa

Hechinger

Madin

et al. 2019

Preprint

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18Individuals can alter their behaviour and other traits to reduce threats from predators 19 and parasites. However, predators and parasites likely elicit different responses, 20 which subsequently lead to different non-lethal effects. We created a sequentially 21 structured framework to examine trait responses to distinct predatory and parasitic 22 beyond the predator vs. parasite dichotomy toward a broader consumer-resource 35 perspective will facilitate understanding of non-lethal effects in complex, multi-36 trophic food webs. 37 attack, combat consumption (Fig. 1) 1 . This temporal sequence implies that trait 113 responses to minimize consumption can be driven by multiple biological mechanisms. 114 1 These classifications are similar to "avoidance", "escape attack", and "escape capture" defined by Lima & Dill (1990) for behavioural responses of prey to predator encounters, though we propose this alternative terminology as a more comprehensive categorization of the diversity of trait responses elicited by different predators and parasites.

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“…Overall, we predict that risky behaviors will be more frequent at late stages of carcass decomposition and in heterospecific carcasses. This study may provide important insights to further understand the landscape of disgust associated with carrion, as well as the possible epidemiological consequences of this host behavior (Buck et al 2018 ; Weinstein et al 2018a ; Doherty and Ruehle 2020 ; Moleón and Sánchez-Zapata 2021 ). This kind of study may be especially relevant in the current SARS-CoV-2 pandemic context, which has highlighted the need to investigate the forms of transmission of this emerging pathogen (Wong et al 2020 ) in wild species, especially in mesocarnivores (Leroy et al 2020 ; Tiwari et al 2020 ).…”

Section: Introductionmentioning

confidence: 96%

Understanding potential implications for non-trophic parasite transmission based on vertebrate behavior at mesocarnivore carcass sites

2021

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High infection risk is often associated with aggregations of animals around attractive resources. Here, we explore the behavior of potential hosts of non-trophically transmitted parasites at mesocarnivore carcass sites. We used videos recorded by camera traps at 56 red fox (Vulpes vulpes) carcasses and 10 carcasses of other wild carnivore species in three areas of southeastern Spain. Scavenging species, especially wild canids, mustelids and viverrids, showed more frequent rubbing behavior at carcass sites than non-scavenging and domestic species, suggesting that they could be exposed to a higher potential infection risk. The red fox was the species that most frequently contacted carcasses and marked and rubbed carcass sites. Foxes contacted heterospecific carcasses more frequently and earlier than conspecific ones and, when close contact occurred, it was more likely to be observed at heterospecific carcasses. This suggests that foxes avoid contact with the type of carcass and time period that have the greatest risk as a source of parasites. Overall, non-trophic behaviors of higher infection risk were mainly associated with visitor-carcass contact and visitor contact with feces and urine, rather than direct contact between visitors. Moreover, contact events between scavengers and carnivore carcasses were far more frequent than consumption events, which suggests that scavenger behavior is more constrained by the risk of acquiring meat-borne parasites than non-trophically transmitted parasites. This study contributes to filling key gaps in understanding the role of carrion in the landscape of disgust, which may be especially relevant in the current global context of emerging and re-emerging pathogens. Graphical abstract

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An Integrated Landscape of Fear and Disgust: The Evolution of Avoidance Behaviors Amidst a Myriad of Natural Enemies

Cited by 23 publications

References 47 publications

Broadening the ecology of fear: non-lethal effects arise from diverse responses to predation and parasitism

Broadening the ecology of fear: non-lethal effects arise from diverse responses to predation and parasitism

Broadening the ecology of fear: non-lethal effects arise from diverse responses to predation and parasitism

Understanding potential implications for non-trophic parasite transmission based on vertebrate behavior at mesocarnivore carcass sites

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