**1. Introduction**

Recently, Buck et al. [1] and Weinstein et al. [2] formalized a correspondence between predator and parasite avoidance behaviors. They argued how infection risk must determine a three-dimensional 'landscape of disgust' equivalent to the 'landscape of fear' induced by predation risk (defined by [1] as "the relative levels of predation risk experienced by a prey individual, represented as peaks and valleys on the landscape"). In this way, animal behavior is largely shaped by perceived risk (from either predators or parasites), leading to high-risk sites avoidance and preference for low-risk patches [1,2]. Either jointly or independently, these natural enemies may lead to fitness costs in their victims through physiological (e.g., chronic stress [3]) and behavioral (e.g., changes in habitat preferences [4]) effects. Strikingly, these physiological responses and behavioral decisions not only result from direct encounters with enemies, but frequently rely on indirect cues linked to risk situations or resources, regardless of actual presence of predators or parasites (e.g., [5]). Thus, through inducing fear and disgust, predators and parasites lead to a pervasive 'landscape of peril' [6] that may indirectly affect individuals and populations, as well as communities and ecosystems via cascading effects [1,2,6].

If we delve into this integrative, general view, many scary (i.e., related to the landscape of fear) and disgusting (i.e., related to the landscape of disgust) facets of animal carcasses

**Citation:** Moleón, M.; Sánchez-Zapata, J.A. The Role of Carrion in the Landscapes of Fear and Disgust: A Review and Prospects. *Diversity* **2021**, *13*, 28. https:// doi.org/10.3390/d13010028

Received: 3 December 2020 Accepted: 11 January 2021 Published: 13 January 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

can be inferred. In doing so, it rapidly comes to light that carrion probably represents ubiquitous—as it is produced in all biomes—hotspots for both predation and infection risk. On one hand, predators of different trophic levels are usually attracted to carcasses worldwide [7], which may lead to predation risk to not only herbivores (e.g., [8]), but also subordinate predators (e.g., [9]). On the other hand, carrion has long been considered a prominent source of pathogens that can put scavenging animals (e.g., [10]) and other species that may be present at carcass sites (e.g., [11]) at risk. For instance, the behavioral and cognitive repertoire of modern humans are probably shaped in part by the exposure of earliest hominins to the risks of being killed or injured while scavenging large herbivore carcasses and acquiring parasites when consuming a decaying piece of meat [12–14]. Pressures associated with predation and parasitism risk at carrion resources seem to be so pervasive that even some plants have taken advantage of them. In particular, species of genera *Rafflesia*, *Aristolochia*, and *Helicodiceros*, among others, could use thanatosis (i.e., olfactory feigning of carrion) to not only attract pollinators, but also deter herbivores, especially during the flowering period [15].

However, we are just starting to uncover the manifold ecological and evolutionary ramifications of carrion within the context of predation and parasitism risks. Research on this topic is especially needed given the ongoing global environmental change. Understanding how animals thrive in the changing landscape of peril associated with carrion could provide important insights for the conservation of threatened scavengers. Moreover, studying how animals behave around carcass sites could reveal key findings of veterinary and epidemiological interest, which is particularly relevant in the current context of zoonotic diseases [16].

Our general aim is to examine the role that carrion plays in the landscapes of fear and disgust, which has been largely overlooked in the scientific literature despite its crucial eco-evolutionary, epidemiological, and management implications. Through a bibliographic review, we will identify the main ways in which carrion may be scary and disgusting, namely the principal interaction pathways between carcasses and their visitors (both carnivores and herbivores) that expose the former to predators and parasites at carcass sites. Here, predators and scavengers are defined as gatherers and miners, respectively, of live animals [17], with parasites including macroparasites, protists, fungi, bacteria, and viruses [18]. Then, we will determine the main knowledge gaps and provide ideas for future investigation on this emerging and highly promising research topic.

#### **2. Material and Methods**

Following guidelines provided by Haddaway et al. [19], we used the Web of Science to conduct a systematic review of the scientific literature on the landscapes of fear and disgust associated with carrion. Specifically, using the "Topic search" (i.e., title, abstract, and keywords), we searched for "articles" appearing prior to November 2020 that included the following combinations of terms: "landscape of fear" OR "fear" OR "predat\* risk" AND "carrion" OR "carcass" OR "scaveng\*"; and "landscape of disgust" OR "disgust" OR "parasit\* risk" OR "parasit\* avoidance" OR "disease risk" OR "disease avoidance" OR "infection risk" OR "infection avoidance" AND "carrion" OR "carcass" OR "scaveng\*" (Appendix A). We further restricted our search in a two-steps process (e.g., [20]). First, title and abstract were screened to ensure we only included empirical studies dealing with the general topic of this review. Second, we read the full content of the selected articles, excluding articles mentioning only superficially in the introduction and discussion the searched terms, e.g., to motivate the study or suggest future research needs. Through this procedure, we obtained 26 articles. Then, we used Google Scholar to identify additional papers, restricting the search to the first 30 papers for each combination of terms. This complementary search provided 26 articles not identified previously in the Web of Science. In total, we obtained a final set of 52 articles for in-depth review (see References A1 for a complete list of reviewed references), which we consider sufficient to infer global patterns of research effort and relative differences among distinct interaction pathways.

76

We divided the selected articles in two main groups, depending on whether they were concerned with fear or disgust. Then, from each article, we obtained the following information. First, we extracted general data: year of publication; ecosystem under study (*terrestrial*, *coastal*, *marine*, *freshwater*); geographic location (i.e., the country where the study was conducted); period under study (*prehistorical*, *historical*); animals involved in the study (i.e., scavengers and non-scavengers that may feed or inspect around carcasses; *vertebrates*, *invertebrates*); the type of effects—studied, detected, or presumed—that the fear or disgust exerted on such species (*behavioral*, *physiological*, *demographic*, *non-specified*), and study design (*field study, observational*; *field study, experimental*; *field study, quasi-experimental*; *mesocosm experiment*; *other*). "Quasi-experimental" studies refer to those in which carcasses or artificial nests were placed in locations selected by the researchers, but no other condition was manipulated. For each field and mesocosm study, we also recorded the observation method (*direct observation*, *camera-trap*, *other*). Second, we identified the ways in which carrion and visitors to carrion sites could lead to predation or parasitism risk to these or other visitors. This, along with other key reviews on the topic (e.g., [21–27]), was the basis to elaborate a conceptual framework on the main interaction pathways around carrion resources that are related to fear and disgust. In the latter case, we distinguished consumptive (trophic) and non-consumptive (non-trophic) processes. We represented the framework separately for herbivore and carnivore carcasses, given that their decomposition process, persistence time in the environment, and associated risks are neatly different [28]. Third, we recorded the number of articles selected in the review that were related to each pathway, with the aim of identifying major knowledge gaps that could be key targets for future research.

## **3. Results and Discussion**
