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The Role of Carrion in the Landscapes of Fear and Disgust: A Review and Prospects

The Role of Carrion in the Landscapes of Fear and Disgust: A Review and Prospects diversity Review The Role of Carrion in the Landscapes of Fear and Disgust: A Review and Prospects 1 , 2 Marcos Moleón * and José A. Sánchez-Zapata Department of Zoology, University of Granada, 18071 Granada, Spain Department of Applied Biology, University Miguel Hernández, 03202 Elche, Spain; toni@umh.es * Correspondence: mmoleonpaiz@hotmail.com or mmoleon@ugr.es Abstract: Animal behavior is greatly shaped by the ‘landscape of fear ’, induced by predation risk, and the equivalent ‘landscape of disgust’, induced by parasitism or infection risk. However, the role that carrion may play in these landscapes of peril has been largely overlooked. Here, we aim to emphasize that animal carcasses likely represent ubiquitous hotspots for both predation and infection risk, thus being an outstanding paradigm of how predation and parasitism pressures can concur in space and time. By conducting a literature review, we highlight the manifold inter- and intra- specific interactions linked to carrion via predation and parasitism risks, which may affect not only scavengers, but also non-scavengers. However, we identified major knowledge gaps, as reviewed articles were highly biased towards fear, terrestrial environments, vertebrates, and behavioral re- sponses. Based on the reviewed literature, we provide a conceptual framework on the main fear- and disgust-based interaction pathways associated with carrion resources. This framework may be used to formulate predictions about how the landscape of fear and disgust around carcasses might influence animals’ individual behavior and ecological processes, from population to ecosystem functioning. We encourage ecologists, evolutionary biologists, epidemiologists, forensic scientists, and conservation biologists to explore the promising research avenues associated with the scary and disgusting facets of carrion. Acknowledging the multiple trophic and non-trophic interactions among dead and live animals, including both herbivores and carnivores, will notably improve our understanding of the overlapping pressures that shape the landscape of fear and disgust. Citation: Moleón, M.; Sánchez-Zapata, J.A. The Role of Keywords: carcass; confrontational scavenging; disease risk; facultative scavenger; landscape of Carrion in the Landscapes of Fear peril; marine ecosystems; parasite risk; predator risk; terrestrial ecosystems and Disgust: A Review and Prospects. Diversity 2021, 13, 28. https:// doi.org/10.3390/d13010028 1. Introduction Received: 3 December 2020 Recently, Buck et al. [1] and Weinstein et al. [2] formalized a correspondence between Accepted: 11 January 2021 predator and parasite avoidance behaviors. They argued how infection risk must determine Published: 13 January 2021 a three-dimensional ‘landscape of disgust’ equivalent to the ‘landscape of fear ’ induced Publisher’s Note: MDPI stays neu- by predation risk (defined by [1] as “the relative levels of predation risk experienced by a tral with regard to jurisdictional clai- prey individual, represented as peaks and valleys on the landscape”). In this way, animal ms in published maps and institutio- behavior is largely shaped by perceived risk (from either predators or parasites), leading nal affiliations. 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 Copyright: © 2021 by the authors. Li- from direct encounters with enemies, but frequently rely on indirect cues linked to risk censee MDPI, Basel, Switzerland. situations or resources, regardless of actual presence of predators or parasites (e.g., [5]). This article is an open access article Thus, through inducing fear and disgust, predators and parasites lead to a pervasive distributed under the terms and con- ‘landscape of peril’ [6] that may indirectly affect individuals and populations, as well as ditions of the Creative Commons At- communities and ecosystems via cascading effects [1,2,6]. tribution (CC BY) license (https:// If we delve into this integrative, general view, many scary (i.e., related to the landscape creativecommons.org/licenses/by/ of fear) and disgusting (i.e., related to the landscape of disgust) facets of animal carcasses 4.0/). Diversity 2021, 13, 28. https://doi.org/10.3390/d13010028 https://www.mdpi.com/journal/diversity Diversity 2021, 13, 28 2 of 14 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. Under- standing 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 veteri- nary 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 com- plementary 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. Diversity 2021, 13, 28 3 of 14 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 de- sign (field study, observational; field study, experimental; field study, quasi-experimental; mesocosm experiment; other). “Quasi-experimental” studies refer to those in which carcasses or artifi- cial 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 3.1. General Results We obtained more articles concerned with fear (75%, n = 39) than with disgust (25%, n = 13). No article empirically explored simultaneously both types of risk. Moreover, scien- tists became interested later on disgust than on fear, according to the year of publication of these articles (Figure 1A). Most articles on fear, and all articles on disgust, involved terrestrial ecosystems or mesocosms. Thus, representation of articles dealing with aquatic environments was scarce (Figure 1B). Most articles focused on present-day assemblages, while all studies concerned with prehistorical times were related to the predation (mainly) and infection risk faced at carcass sites by early hominins (Figure 1C). There were more articles studying vertebrates than invertebrates (Figure 1D), with the latter being mainly as- sociated with marine and freshwater systems. Effects on visitors to carrion sites, as recorded in the reviewed articles, were mostly behavioral; only a few articles involved demographic effects (in all cases, related to bird nest predation), and none explored physiological effects on visitor species (Figure 1E). Studies on predation risk were mostly observational and quasi-experimental, though experimental approaches (all in mesocosm systems) were fre- quently used to assess parasitism risk. In addition, the intentional deployment of carcasses (and artificial nests) was normally associated with the use of camera-traps for monitoring bait use by animals, especially in disgust-related studies (Figure 1F). Most present-day studies were conducted in Australia, USA, and Europe, while all studies on early hominins were done with material from eastern Africa (Figure 1G). Diversity 2021, 13, 28 4 of 14 Diversity 2021, 13, x 4 of 14 Figure 1. Distribution of reviewed articles according to publication year (A), ecosystem (B), period (C), type of animals at (potential) risk (D), effects of the risks on such animals (E), study design (different bars) and observation method Figure 1. Distribution of reviewed articles according to publication year (A), ecosystem (B), period (C), type of animals at (within (potential) risk bars) (F), (D and ), eff geographic ects of the risk location s on su (Gc ).hSee anim main als ( text E), study design (different bars for details. ) and observation method (within bars) (F), and geographic location (G). See main text for details. 3.2. Interaction Pathways and Research Effort 3.2. Interaction Pathways and Research Effort Figure 2 shows our conceptual model for the main fear- and disgust-based interac- Figure 2 shows our conceptual model for the main fear- and disgust-based interac- tion pathways associated with carcasses of carnivore and herbivore species. In general, tion pathways associated with carcasses of carnivore and herbivore species. In general, while animals may be mainly disgusted by carcasses themselves, scare is genuinely related while animals may be mainly disgusted by carcasses themselves, scare is genuinely re- to other animals that may be attracted to the carcass for any reason or present by chance in lated to other animals that may be attracted to the carcass for any reason or present by its vicinities. chance in its vicinities. Diversity 2021, 13, 28 5 of 14 Diversity 2021, 13, x 5 of 14 Figure 2. Animal carcasses may be both disgusting and scary. However, the parasite and predator risks vary widely Figure 2. Animal carcasses may be both disgusting and scary. However, the parasite and predator risks vary widely ac- according to the species identity of the carcass and its visitors. (A) Carnivores visiting carnivore carcasses may face both cording to the species identity of the carcass and its visitors. (A) Carnivores visiting carnivore carcasses may face both predation and infection risk. Parasites may be transmitted to carnivores by either the carcass or other carnivore visitors, predation and infection risk. Parasites may be transmitted to carnivores by either the carcass or other carnivore visitors, with the probability of transmission being proportional to their phylogenetic relationship [29,30]. (B) Herbivore carcasses with the probability of transmission being proportional to their phylogenetic relationship [29,30]. (B) Herbivore carcasses are relatively are relativelysafe for carnivor safe for carnivor es in terms of es in terms of direct parasite direct parasite transm transmis ission (at sion (at least least, , rega rrding egarding direct l direct ife cy life cle parasite cycle parasites), s), but these carnivores may still be subject of parasite and predation risk from other carnivores. Herbivores may be at predation but these carnivores may still be subject of parasite and predation risk from other carnivores. Herbivores may be at and parasitism risk at both carnivore and herbivore carcass sites, with the latter representing comparatively higher risk of predation and parasitism risk at both carnivore and herbivore carcass sites, with the latter representing comparatively acquiring parasites. Interactions among carnivores are more frequent at large carcasses [31] and in the absence of vultures higher risk of acquiring parasites. Interactions among carnivores are more frequent at large carcasses [31] and in the absence [32], which are highly efficient scavengers [33,34]. Arrow width is roughly proportional to the intensity of risk. of vultures [32], which are highly efficient scavengers [33,34]. Arrow width is roughly proportional to the intensity of risk. Diversity 2021, 13, 28 6 of 14 Diversity 2021, 13, x 6 of 14 Among the different pathways associated with carnivore carrion, only the risk of Among the different pathways associated with carnivore carrion, only the risk of ac- acquiring parasites through intra-guild and, especially, intra-specific scavenging received quiring parasites through intra-guild and, especially, intra-specific scavenging received some scientific interest within the reviewed articles (e.g., [35–37]; Figure 3A). some scientific interest within the reviewed articles (e.g., [35–37]; Figure 3A). Figure 3. Research effort devoted to the main fear- and disgust-related interaction pathways around (A) carnivore and (B) Figure 3. Research effort devoted to the main fear- and disgust-related interaction pathways around (A) carnivore and herbivore carrion, according to our literature review. Those pathways for which we found at least one article are shown (B) herbivore carrion, according to our literature review. Those pathways for which we found at least one article are shown by black arrows (we use grey arrows otherwise). Arrow width is proportional to the number of articles. by black arrows (we use grey arrows otherwise). Arrow width is proportional to the number of articles. Regarding herbivore carcasses (Figure 3B), most studies have focused on the preda- Regarding herbivore carcasses (Figure 3B), most studies have focused on the predation tion risk affecting species that are present in the vicinities of carcass sites, both herbivores risk affecting species that are present in the vicinities of carcass sites, both herbivores (e.g., [8,38–40]) and, mostly, carnivores (e.g., [9,41–47]). Within these articles, several stud- (e.g., [8,38–40]) and, mostly, carnivores (e.g., [9,41–47]). Within these articles, several studies ies explored how Plio/Pleistocene hominins were subject of predation risk while exploit- explored how Plio/Pleistocene hominins were subject of predation risk while exploiting ing large carcasses (a process called confrontational/aggressive/active/power scavenging), large carcasses (a process called confrontational/aggressive/active/power scavenging), according to paleontological evidences and behavioral, ecological, and energetics model- according to paleontological evidences and behavioral, ecological, and energetics modelling ling (e.g., (e.g [13 ., ,[48 13, ]), 48]) behavioral , behavior studies al studie ofs of modern modern hum human hunter an hunter-gat -gatherer herer societies [49] societies [49] or other or primates [50], and other procedures [51]. Other studies have focused on several aspects of Diversity 2021, 13, 28 7 of 14 parasitism, especially the risk of acquiring parasites from meat consumption by carnivores (e.g., [52–54]). 3.3. Carrion Is Disgusting Mammalian carnivores avoid feeding on other carnivore carcasses, especially of conspecifics, likely to reduce exposure to parasites [35–37]. These findings highlight that the risk of direct infection is higher among phylogenetically close organisms, which share more parasite species [1,29,30,37]. In turn, the carnivore carrion-avoidance behavior of carnivores enables a wide array of indirect ecological effects, both consumptive (e.g., scavenging of mammalian carnivore carcasses by a well-structured community of insects) and non- consumptive (e.g., hair collection by birds for nest construction), linked to carnivore carcasses [37,55]. This, together with the observation that grazers avoid foraging near herbivore carcasses to prevent infectious risk (e.g., [2,53,56]), indicates that dead animals may disgust both scavenging and non-scavenging species (Figure 3). However, effects of carrion on vegetation growth may lead to increased disease risk for herbivores that are attracted to carcass sites once carrion has been removed, in a sort of ecological trap that favors infection by highly resistant pathogens [11]. Regarding the mechanism by which scavengers may discriminate risky carcasses, some carnivores such as mammalian meso-carnivores seem to rely on carrion odor (e.g., to distinguish intra- from inter-specific carrion [37]), while others such as ants and beetles may detect the presence of certain pathogens by smelling or tasting their metabolites in the carcass [52]. In addition to meat-borne parasites, other pathogens present at carcass sites could be transmitted to any animal that approaches at a sufficient distance [11,53,57]. In addition, carcasses may indirectly favor parasite transmission among the scavengers that come into contact while scavenging, a circumstance that would be especially plausible in the absence of vultures [32], which are specialized, obligate scavengers that quickly remove carcasses [33,34,58]. However, these and other mechanisms of carcass-mediated infection risk (Figure 3) remain largely speculative and need further empirical support. Besides carcass type, carrion-related infection risk—and the duration of the infective period—may be dependent on many other factors, such as parasite identity, carcass origin, the degree of starvation shown by the scavenger, and climatic conditions (e.g., [35,41,59]). Given the important ecological, evolutionary, and sanitary implications of the management of wild [60] and domestic animal carcasses [61], these issues require urgent scientific atten- tion. 3.4. Carrion Is Scary Herbivore carcass sites may be avoided by other herbivores because of high proba- bility of predator–prey encounters (e.g., [8,38,40]; Figure 3B). Indeed, the probability of predation of ground-nesting birds increases near both predictable and unpredictable car- rion resources [39,62]. The increased predation risk around carcasses is mainly explained by the fact that most predators behave also as facultative scavengers that are, to a greater or lesser extent, attracted to carrion [63,64]. This predation risk is likely higher at large carcasses because they are visited by more and larger predator species than smaller car- casses [7,31]. In addition to herbivores, small and medium-sized carnivores also avoid carcasses to prevent the risk of confronting dominant predators (e.g., [5,9,43,45,47,65]). In fact, the risk of being attacked by a larger predator, such as lion (Panthera leo) and spotted hyaena (Crocuta crocuta), may be so high that certain sympatric mammalian carnivores, such as cheetahs (Acinonyx jubatus) and wild dogs (Lycaon pictus), very rarely scavenge [66]. Cheetahs, even leave their own kills once satiated, no matter how much meat may be left [67]. However, how carnivores and herbivores behave at carnivore carcasses in relation to predation risk is virtually unknown (but see [41,65]; Figure 3A). In these cases, carcasses of predators may also be scary by themselves, as other scavengers that are within the prey base of the dead predators might even avoid the risk of inspecting such carcasses. Diversity 2021, 13, 28 8 of 14 The risk that a given animal, either scavenger or not, is willing to accept at a carcass site may depend on several factors, such as sociality. For instance, spotted hyaenas are able to even displace lions from a carcass provided that the former outnumber the latter by a factor of 4 and no male lions are present at the carcass [68]. Coyotes (Canis latrans) may also displace wolves (C. lupus) from their kills when the former are in numerical advantage [9]. In addition, both hyaenas and (alpha) coyotes may trade off greater risk for high-quality carrion, as dominant carnivores may also facilitate carrion supply and detection [9,68]. Finally, hungry, sick, unexperienced, or senescent scavengers are probably more prone to face risky situations (e.g., [44,65,69]), though this needs further empirical confirmation. 3.5. Conclusions and Directions for Further Research Overall, this review highlights the manifold inter- and intra-specific interactions linked to carrion via predation and parasitism risks, which may affect not only carrion consumers, but also non-consumers. Animal carcasses are an outstanding paradigm of how predation and parasitism pressures can concur in space and time, which is a major gap in predator- and parasite-avoidance scientific knowledge [1]. Carcasses may represent hotspots of infection and predation risk to both carnivores and herbivores, although the risk is highly dependent on a number of factors, such as carcass identity (Figure 2) and the size of the animals visiting carcass sites. For instance, large herbivores and top predators will be more reactive to parasite than to predator risk [1]. Thus, the multiple predator and parasite risk pathways that may arise around carnivore (Figure 2A) and herbivore carrion (Figure 2B), which are far more diverse than previously recognized, may differ qualitatively and quantitatively. However, fully understanding of animal behavior around carrion resources requires exploring simultaneously different sources of risk [1], as avoiding one risk may increase [70] or decrease [71] another. Furthermore, Buck et al. [1] argue that “because predators are generally more mobile than parasites, the predator-induced landscape of fear might be more dynamic than the parasite-induced landscape of disgust”. We highlight that, given the generally unpredictable and ephemeral nature of carrion [63,64,72], the very different life cycles of different parasite species [73], and the seasonality associated with their infective stages [74], carcass-induced landscape of disgust may be also highly dynamic. The conceptual framework of the landscape of peril might also benefit from empirical evidence of aquatic ecosystems addressing key issues that differentiate them from terrestrial ones. For example, parasites in aquatic environments are more mobile than in terrestrial ecosystems, due to both active (i.e., locomotion and motility) and passive (e.g., currents and tides) transport through water [18]. Other relevant differences between terrestrial and aquatic systems relate to the cues to detect predators and parasites, which may differ quali- tatively and quantitatively between air and water. In general, while visual, auditory and mechanosensory cues play a more prominent role in terrestrial environments, chemical cues are substantially more used by aquatic animals [18]. Comparative studies on how animals perceive and avoid predation and parasitism risk at carcass sites in terrestrial vs. aquatic environments are virtually absent, which opens exciting avenues for further research. The conceptual model we present here (Figure 2) allows formulating predictions about how the landscape of fear and disgust around carcasses might influence animals’ individual behavior and ecological processes, from population to ecosystem functioning. This could be especially useful in the current global change scenario, which includes high rates of species extinctions, invasions, and re-colonizations of both predators and parasites (e.g., [75]), as well as a growing evidence of the effect of human footprint on scavenger guilds [7]. In addition, our literature review has clearly shown that the research effort so far on predator and parasite risks associated with carrion has been highly unevenly distributed through the different interaction pathways, with most studies dealing with predation risk at vertebrate herbivore carcasses in terrestrial ecosystems (Figure 3). Thus, there is ample room and motivation for future investigation. Furthermore, most research has focused on behavioral responses (particularly, avoidance) of different species in relation Diversity 2021, 13, 28 9 of 14 to fear and disgust. However, to which extent are these behaviors innate or learned is an open question [36]. Moreover, other individual responses (e.g., physiological), as well as the effects at the population, community, and ecosystem levels remain largely unexplored and require further empirical evidence. While physiological responses have not been explored so far in a carrion context (to our knowledge), it is reasonable to think that the risks associated with carrion may exert different physiological costs (e.g., transitory and chronic stress) on animals visiting carcass sites, such as prey and subordinate predators. Future research might benefit from the application of novel (including experimental) methods in scavenging ecology and its interaction with different disciplines, as well as from the spatiotemporal quantification of carrion biomass [28,76] and the long-term monitoring of carcasses and scavenger guilds in different ecosystems [7]. Finally, besides freshwater and marine studies, terrestrial studies from tropical biomes would be especially welcome, as most research (for the historical period context) so far has focused on temperate, Mediterranean, and boreal systems. In conclusion, future research should study the trade-offs and synergistic effects of both predator and parasite risk associated with carcasses of different nature and size in contrasting ecosystems and seasons, as well as the relative importance of these and other selective pressures. These ecological processes may have important consequences for animals facing predator and parasite risks, with individual costs ranging from diminished feeding rate to death, which may lead to wide ecological, evolutionary, epidemiological, forensic, and conservation implications. Acknowledging the multiple trophic (e.g., [64]) and non-trophic (e.g., [77]) ways in which dead animals directly and indirectly interact with living animals, including both herbivores and carnivores, will notably improve our understanding of the overlapping pressures that shape the landscape of fear and disgust. Author Contributions: M.M. and J.A.S.-Z. conceived the study, conducted the literature review, wrote the manuscript and agreed to its submission. All authors have read and agreed to the published version of the manuscript. Funding: M.M. was supported by a research contract Ramón y Cajal from the MINECO (RYC- 2015-19231). This study was partly funded by the Spanish Ministry of Economy, Industry and Competitiveness and EU ERDF funds through the projects CGL2015-66966-C2-1-2-R and CGL2017- 89905-R. Conflicts of Interest: The authors declare no conflict of interest. Appendix A References A1. Articles Reviewed. Articles Identified in the Google Scholar Search Only Are Marked with an Asterisk 1. *Allen, M.L.; Elbroch, L.M.; Wilmers, C.C.; Witmer, H.U. The comparative effects of large carnivores on the acquisition of carrion by scavengers. Am. Nat. 2015, 185, 822–833. 2. Allen, M.L.; Wilmers, C.C.; Elbroch, L.M.; Golla, J.M.; Witmer, H.U. The importance of motivation, weapons, and foul odors in driving encounter competition in carnivores. Ecology 2016, 97, 1905–1912. 3. *Archer, M.S.; Elgar, M.A. Effects of decomposition on carcass attendance in a guild of carrion-breeding flies. Med. Vet. Entomol. 2003, 17, 263–271. 4. *Archer, M.S.; Elgar, M.A. Female breeding-site preferences and larval feeding strategies of carrion-breeding Calliphoridae and Sarcophagidae (Diptera): A quantitative analysis. Aust. J. Zool. 2003, 51, 165–174. 5. Atwood, T.C.; Gese, E.M. Coyotes and recolonizing wolves: Social rank mediates risk-conditional behaviour at ungulate carcasses. Anim. Behav. 2008, 75, 753–762. 6. *Blanco, G.; Cardells, J.; Garijo-Toledo, M.M. Supplementary feeding and endoparasites in threatened avian scavengers: Coprologic evidence from red kites in their wintering stronghold. Environ. Res. 2017, 155, 22–30. 7. Blumenschine, R.J. Hominid carnivory and foraging strategies, and the socio-economic function of early archaeolog- ical sites. Philos. Trans. R. Soc. Lond. B 1991, 334, 211–221. 8. *Blumenschine, R.J.; Cavallo, J.A.; Capaldo, S.D. Competition for carcasses and early hominid behavioral ecology: A case study and conceptual framework. J. Hum. Evol. 1994, 27, 197–213. 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Non-trophic functions of carcasses: From death to the nest. Front. Ecol. Environ. 2016, 14, 340–341. [CrossRef] http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Diversity Multidisciplinary Digital Publishing Institute

The Role of Carrion in the Landscapes of Fear and Disgust: A Review and Prospects

Diversity , Volume 13 (1) – Jan 13, 2021

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diversity Review The Role of Carrion in the Landscapes of Fear and Disgust: A Review and Prospects 1 , 2 Marcos Moleón * and José A. Sánchez-Zapata Department of Zoology, University of Granada, 18071 Granada, Spain Department of Applied Biology, University Miguel Hernández, 03202 Elche, Spain; toni@umh.es * Correspondence: mmoleonpaiz@hotmail.com or mmoleon@ugr.es Abstract: Animal behavior is greatly shaped by the ‘landscape of fear ’, induced by predation risk, and the equivalent ‘landscape of disgust’, induced by parasitism or infection risk. However, the role that carrion may play in these landscapes of peril has been largely overlooked. Here, we aim to emphasize that animal carcasses likely represent ubiquitous hotspots for both predation and infection risk, thus being an outstanding paradigm of how predation and parasitism pressures can concur in space and time. By conducting a literature review, we highlight the manifold inter- and intra- specific interactions linked to carrion via predation and parasitism risks, which may affect not only scavengers, but also non-scavengers. However, we identified major knowledge gaps, as reviewed articles were highly biased towards fear, terrestrial environments, vertebrates, and behavioral re- sponses. Based on the reviewed literature, we provide a conceptual framework on the main fear- and disgust-based interaction pathways associated with carrion resources. This framework may be used to formulate predictions about how the landscape of fear and disgust around carcasses might influence animals’ individual behavior and ecological processes, from population to ecosystem functioning. We encourage ecologists, evolutionary biologists, epidemiologists, forensic scientists, and conservation biologists to explore the promising research avenues associated with the scary and disgusting facets of carrion. Acknowledging the multiple trophic and non-trophic interactions among dead and live animals, including both herbivores and carnivores, will notably improve our understanding of the overlapping pressures that shape the landscape of fear and disgust. Citation: Moleón, M.; Sánchez-Zapata, J.A. The Role of Keywords: carcass; confrontational scavenging; disease risk; facultative scavenger; landscape of Carrion in the Landscapes of Fear peril; marine ecosystems; parasite risk; predator risk; terrestrial ecosystems and Disgust: A Review and Prospects. Diversity 2021, 13, 28. https:// doi.org/10.3390/d13010028 1. Introduction Received: 3 December 2020 Recently, Buck et al. [1] and Weinstein et al. [2] formalized a correspondence between Accepted: 11 January 2021 predator and parasite avoidance behaviors. They argued how infection risk must determine Published: 13 January 2021 a three-dimensional ‘landscape of disgust’ equivalent to the ‘landscape of fear ’ induced Publisher’s Note: MDPI stays neu- by predation risk (defined by [1] as “the relative levels of predation risk experienced by a tral with regard to jurisdictional clai- prey individual, represented as peaks and valleys on the landscape”). In this way, animal ms in published maps and institutio- behavior is largely shaped by perceived risk (from either predators or parasites), leading nal affiliations. 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 Copyright: © 2021 by the authors. Li- from direct encounters with enemies, but frequently rely on indirect cues linked to risk censee MDPI, Basel, Switzerland. situations or resources, regardless of actual presence of predators or parasites (e.g., [5]). This article is an open access article Thus, through inducing fear and disgust, predators and parasites lead to a pervasive distributed under the terms and con- ‘landscape of peril’ [6] that may indirectly affect individuals and populations, as well as ditions of the Creative Commons At- communities and ecosystems via cascading effects [1,2,6]. tribution (CC BY) license (https:// If we delve into this integrative, general view, many scary (i.e., related to the landscape creativecommons.org/licenses/by/ of fear) and disgusting (i.e., related to the landscape of disgust) facets of animal carcasses 4.0/). Diversity 2021, 13, 28. https://doi.org/10.3390/d13010028 https://www.mdpi.com/journal/diversity Diversity 2021, 13, 28 2 of 14 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. Under- standing 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 veteri- nary 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 com- plementary 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. Diversity 2021, 13, 28 3 of 14 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 de- sign (field study, observational; field study, experimental; field study, quasi-experimental; mesocosm experiment; other). “Quasi-experimental” studies refer to those in which carcasses or artifi- cial 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 3.1. General Results We obtained more articles concerned with fear (75%, n = 39) than with disgust (25%, n = 13). No article empirically explored simultaneously both types of risk. Moreover, scien- tists became interested later on disgust than on fear, according to the year of publication of these articles (Figure 1A). Most articles on fear, and all articles on disgust, involved terrestrial ecosystems or mesocosms. Thus, representation of articles dealing with aquatic environments was scarce (Figure 1B). Most articles focused on present-day assemblages, while all studies concerned with prehistorical times were related to the predation (mainly) and infection risk faced at carcass sites by early hominins (Figure 1C). There were more articles studying vertebrates than invertebrates (Figure 1D), with the latter being mainly as- sociated with marine and freshwater systems. Effects on visitors to carrion sites, as recorded in the reviewed articles, were mostly behavioral; only a few articles involved demographic effects (in all cases, related to bird nest predation), and none explored physiological effects on visitor species (Figure 1E). Studies on predation risk were mostly observational and quasi-experimental, though experimental approaches (all in mesocosm systems) were fre- quently used to assess parasitism risk. In addition, the intentional deployment of carcasses (and artificial nests) was normally associated with the use of camera-traps for monitoring bait use by animals, especially in disgust-related studies (Figure 1F). Most present-day studies were conducted in Australia, USA, and Europe, while all studies on early hominins were done with material from eastern Africa (Figure 1G). Diversity 2021, 13, 28 4 of 14 Diversity 2021, 13, x 4 of 14 Figure 1. Distribution of reviewed articles according to publication year (A), ecosystem (B), period (C), type of animals at (potential) risk (D), effects of the risks on such animals (E), study design (different bars) and observation method Figure 1. Distribution of reviewed articles according to publication year (A), ecosystem (B), period (C), type of animals at (within (potential) risk bars) (F), (D and ), eff geographic ects of the risk location s on su (Gc ).hSee anim main als ( text E), study design (different bars for details. ) and observation method (within bars) (F), and geographic location (G). See main text for details. 3.2. Interaction Pathways and Research Effort 3.2. Interaction Pathways and Research Effort Figure 2 shows our conceptual model for the main fear- and disgust-based interac- Figure 2 shows our conceptual model for the main fear- and disgust-based interac- tion pathways associated with carcasses of carnivore and herbivore species. In general, tion pathways associated with carcasses of carnivore and herbivore species. In general, while animals may be mainly disgusted by carcasses themselves, scare is genuinely related while animals may be mainly disgusted by carcasses themselves, scare is genuinely re- to other animals that may be attracted to the carcass for any reason or present by chance in lated to other animals that may be attracted to the carcass for any reason or present by its vicinities. chance in its vicinities. Diversity 2021, 13, 28 5 of 14 Diversity 2021, 13, x 5 of 14 Figure 2. Animal carcasses may be both disgusting and scary. However, the parasite and predator risks vary widely Figure 2. Animal carcasses may be both disgusting and scary. However, the parasite and predator risks vary widely ac- according to the species identity of the carcass and its visitors. (A) Carnivores visiting carnivore carcasses may face both cording to the species identity of the carcass and its visitors. (A) Carnivores visiting carnivore carcasses may face both predation and infection risk. Parasites may be transmitted to carnivores by either the carcass or other carnivore visitors, predation and infection risk. Parasites may be transmitted to carnivores by either the carcass or other carnivore visitors, with the probability of transmission being proportional to their phylogenetic relationship [29,30]. (B) Herbivore carcasses with the probability of transmission being proportional to their phylogenetic relationship [29,30]. (B) Herbivore carcasses are relatively are relativelysafe for carnivor safe for carnivor es in terms of es in terms of direct parasite direct parasite transm transmis ission (at sion (at least least, , rega rrding egarding direct l direct ife cy life cle parasite cycle parasites), s), but these carnivores may still be subject of parasite and predation risk from other carnivores. Herbivores may be at predation but these carnivores may still be subject of parasite and predation risk from other carnivores. Herbivores may be at and parasitism risk at both carnivore and herbivore carcass sites, with the latter representing comparatively higher risk of predation and parasitism risk at both carnivore and herbivore carcass sites, with the latter representing comparatively acquiring parasites. Interactions among carnivores are more frequent at large carcasses [31] and in the absence of vultures higher risk of acquiring parasites. Interactions among carnivores are more frequent at large carcasses [31] and in the absence [32], which are highly efficient scavengers [33,34]. Arrow width is roughly proportional to the intensity of risk. of vultures [32], which are highly efficient scavengers [33,34]. Arrow width is roughly proportional to the intensity of risk. Diversity 2021, 13, 28 6 of 14 Diversity 2021, 13, x 6 of 14 Among the different pathways associated with carnivore carrion, only the risk of Among the different pathways associated with carnivore carrion, only the risk of ac- acquiring parasites through intra-guild and, especially, intra-specific scavenging received quiring parasites through intra-guild and, especially, intra-specific scavenging received some scientific interest within the reviewed articles (e.g., [35–37]; Figure 3A). some scientific interest within the reviewed articles (e.g., [35–37]; Figure 3A). Figure 3. Research effort devoted to the main fear- and disgust-related interaction pathways around (A) carnivore and (B) Figure 3. Research effort devoted to the main fear- and disgust-related interaction pathways around (A) carnivore and herbivore carrion, according to our literature review. Those pathways for which we found at least one article are shown (B) herbivore carrion, according to our literature review. Those pathways for which we found at least one article are shown by black arrows (we use grey arrows otherwise). Arrow width is proportional to the number of articles. by black arrows (we use grey arrows otherwise). Arrow width is proportional to the number of articles. Regarding herbivore carcasses (Figure 3B), most studies have focused on the preda- Regarding herbivore carcasses (Figure 3B), most studies have focused on the predation tion risk affecting species that are present in the vicinities of carcass sites, both herbivores risk affecting species that are present in the vicinities of carcass sites, both herbivores (e.g., [8,38–40]) and, mostly, carnivores (e.g., [9,41–47]). Within these articles, several stud- (e.g., [8,38–40]) and, mostly, carnivores (e.g., [9,41–47]). Within these articles, several studies ies explored how Plio/Pleistocene hominins were subject of predation risk while exploit- explored how Plio/Pleistocene hominins were subject of predation risk while exploiting ing large carcasses (a process called confrontational/aggressive/active/power scavenging), large carcasses (a process called confrontational/aggressive/active/power scavenging), according to paleontological evidences and behavioral, ecological, and energetics model- according to paleontological evidences and behavioral, ecological, and energetics modelling ling (e.g., (e.g [13 ., ,[48 13, ]), 48]) behavioral , behavior studies al studie ofs of modern modern hum human hunter an hunter-gat -gatherer herer societies [49] societies [49] or other or primates [50], and other procedures [51]. Other studies have focused on several aspects of Diversity 2021, 13, 28 7 of 14 parasitism, especially the risk of acquiring parasites from meat consumption by carnivores (e.g., [52–54]). 3.3. Carrion Is Disgusting Mammalian carnivores avoid feeding on other carnivore carcasses, especially of conspecifics, likely to reduce exposure to parasites [35–37]. These findings highlight that the risk of direct infection is higher among phylogenetically close organisms, which share more parasite species [1,29,30,37]. In turn, the carnivore carrion-avoidance behavior of carnivores enables a wide array of indirect ecological effects, both consumptive (e.g., scavenging of mammalian carnivore carcasses by a well-structured community of insects) and non- consumptive (e.g., hair collection by birds for nest construction), linked to carnivore carcasses [37,55]. This, together with the observation that grazers avoid foraging near herbivore carcasses to prevent infectious risk (e.g., [2,53,56]), indicates that dead animals may disgust both scavenging and non-scavenging species (Figure 3). However, effects of carrion on vegetation growth may lead to increased disease risk for herbivores that are attracted to carcass sites once carrion has been removed, in a sort of ecological trap that favors infection by highly resistant pathogens [11]. Regarding the mechanism by which scavengers may discriminate risky carcasses, some carnivores such as mammalian meso-carnivores seem to rely on carrion odor (e.g., to distinguish intra- from inter-specific carrion [37]), while others such as ants and beetles may detect the presence of certain pathogens by smelling or tasting their metabolites in the carcass [52]. In addition to meat-borne parasites, other pathogens present at carcass sites could be transmitted to any animal that approaches at a sufficient distance [11,53,57]. In addition, carcasses may indirectly favor parasite transmission among the scavengers that come into contact while scavenging, a circumstance that would be especially plausible in the absence of vultures [32], which are specialized, obligate scavengers that quickly remove carcasses [33,34,58]. However, these and other mechanisms of carcass-mediated infection risk (Figure 3) remain largely speculative and need further empirical support. Besides carcass type, carrion-related infection risk—and the duration of the infective period—may be dependent on many other factors, such as parasite identity, carcass origin, the degree of starvation shown by the scavenger, and climatic conditions (e.g., [35,41,59]). Given the important ecological, evolutionary, and sanitary implications of the management of wild [60] and domestic animal carcasses [61], these issues require urgent scientific atten- tion. 3.4. Carrion Is Scary Herbivore carcass sites may be avoided by other herbivores because of high proba- bility of predator–prey encounters (e.g., [8,38,40]; Figure 3B). Indeed, the probability of predation of ground-nesting birds increases near both predictable and unpredictable car- rion resources [39,62]. The increased predation risk around carcasses is mainly explained by the fact that most predators behave also as facultative scavengers that are, to a greater or lesser extent, attracted to carrion [63,64]. This predation risk is likely higher at large carcasses because they are visited by more and larger predator species than smaller car- casses [7,31]. In addition to herbivores, small and medium-sized carnivores also avoid carcasses to prevent the risk of confronting dominant predators (e.g., [5,9,43,45,47,65]). In fact, the risk of being attacked by a larger predator, such as lion (Panthera leo) and spotted hyaena (Crocuta crocuta), may be so high that certain sympatric mammalian carnivores, such as cheetahs (Acinonyx jubatus) and wild dogs (Lycaon pictus), very rarely scavenge [66]. Cheetahs, even leave their own kills once satiated, no matter how much meat may be left [67]. However, how carnivores and herbivores behave at carnivore carcasses in relation to predation risk is virtually unknown (but see [41,65]; Figure 3A). In these cases, carcasses of predators may also be scary by themselves, as other scavengers that are within the prey base of the dead predators might even avoid the risk of inspecting such carcasses. Diversity 2021, 13, 28 8 of 14 The risk that a given animal, either scavenger or not, is willing to accept at a carcass site may depend on several factors, such as sociality. For instance, spotted hyaenas are able to even displace lions from a carcass provided that the former outnumber the latter by a factor of 4 and no male lions are present at the carcass [68]. Coyotes (Canis latrans) may also displace wolves (C. lupus) from their kills when the former are in numerical advantage [9]. In addition, both hyaenas and (alpha) coyotes may trade off greater risk for high-quality carrion, as dominant carnivores may also facilitate carrion supply and detection [9,68]. Finally, hungry, sick, unexperienced, or senescent scavengers are probably more prone to face risky situations (e.g., [44,65,69]), though this needs further empirical confirmation. 3.5. Conclusions and Directions for Further Research Overall, this review highlights the manifold inter- and intra-specific interactions linked to carrion via predation and parasitism risks, which may affect not only carrion consumers, but also non-consumers. Animal carcasses are an outstanding paradigm of how predation and parasitism pressures can concur in space and time, which is a major gap in predator- and parasite-avoidance scientific knowledge [1]. Carcasses may represent hotspots of infection and predation risk to both carnivores and herbivores, although the risk is highly dependent on a number of factors, such as carcass identity (Figure 2) and the size of the animals visiting carcass sites. For instance, large herbivores and top predators will be more reactive to parasite than to predator risk [1]. Thus, the multiple predator and parasite risk pathways that may arise around carnivore (Figure 2A) and herbivore carrion (Figure 2B), which are far more diverse than previously recognized, may differ qualitatively and quantitatively. However, fully understanding of animal behavior around carrion resources requires exploring simultaneously different sources of risk [1], as avoiding one risk may increase [70] or decrease [71] another. Furthermore, Buck et al. [1] argue that “because predators are generally more mobile than parasites, the predator-induced landscape of fear might be more dynamic than the parasite-induced landscape of disgust”. We highlight that, given the generally unpredictable and ephemeral nature of carrion [63,64,72], the very different life cycles of different parasite species [73], and the seasonality associated with their infective stages [74], carcass-induced landscape of disgust may be also highly dynamic. The conceptual framework of the landscape of peril might also benefit from empirical evidence of aquatic ecosystems addressing key issues that differentiate them from terrestrial ones. For example, parasites in aquatic environments are more mobile than in terrestrial ecosystems, due to both active (i.e., locomotion and motility) and passive (e.g., currents and tides) transport through water [18]. Other relevant differences between terrestrial and aquatic systems relate to the cues to detect predators and parasites, which may differ quali- tatively and quantitatively between air and water. In general, while visual, auditory and mechanosensory cues play a more prominent role in terrestrial environments, chemical cues are substantially more used by aquatic animals [18]. Comparative studies on how animals perceive and avoid predation and parasitism risk at carcass sites in terrestrial vs. aquatic environments are virtually absent, which opens exciting avenues for further research. The conceptual model we present here (Figure 2) allows formulating predictions about how the landscape of fear and disgust around carcasses might influence animals’ individual behavior and ecological processes, from population to ecosystem functioning. This could be especially useful in the current global change scenario, which includes high rates of species extinctions, invasions, and re-colonizations of both predators and parasites (e.g., [75]), as well as a growing evidence of the effect of human footprint on scavenger guilds [7]. In addition, our literature review has clearly shown that the research effort so far on predator and parasite risks associated with carrion has been highly unevenly distributed through the different interaction pathways, with most studies dealing with predation risk at vertebrate herbivore carcasses in terrestrial ecosystems (Figure 3). Thus, there is ample room and motivation for future investigation. Furthermore, most research has focused on behavioral responses (particularly, avoidance) of different species in relation Diversity 2021, 13, 28 9 of 14 to fear and disgust. However, to which extent are these behaviors innate or learned is an open question [36]. Moreover, other individual responses (e.g., physiological), as well as the effects at the population, community, and ecosystem levels remain largely unexplored and require further empirical evidence. While physiological responses have not been explored so far in a carrion context (to our knowledge), it is reasonable to think that the risks associated with carrion may exert different physiological costs (e.g., transitory and chronic stress) on animals visiting carcass sites, such as prey and subordinate predators. Future research might benefit from the application of novel (including experimental) methods in scavenging ecology and its interaction with different disciplines, as well as from the spatiotemporal quantification of carrion biomass [28,76] and the long-term monitoring of carcasses and scavenger guilds in different ecosystems [7]. Finally, besides freshwater and marine studies, terrestrial studies from tropical biomes would be especially welcome, as most research (for the historical period context) so far has focused on temperate, Mediterranean, and boreal systems. In conclusion, future research should study the trade-offs and synergistic effects of both predator and parasite risk associated with carcasses of different nature and size in contrasting ecosystems and seasons, as well as the relative importance of these and other selective pressures. These ecological processes may have important consequences for animals facing predator and parasite risks, with individual costs ranging from diminished feeding rate to death, which may lead to wide ecological, evolutionary, epidemiological, forensic, and conservation implications. Acknowledging the multiple trophic (e.g., [64]) and non-trophic (e.g., [77]) ways in which dead animals directly and indirectly interact with living animals, including both herbivores and carnivores, will notably improve our understanding of the overlapping pressures that shape the landscape of fear and disgust. Author Contributions: M.M. and J.A.S.-Z. conceived the study, conducted the literature review, wrote the manuscript and agreed to its submission. All authors have read and agreed to the published version of the manuscript. Funding: M.M. was supported by a research contract Ramón y Cajal from the MINECO (RYC- 2015-19231). This study was partly funded by the Spanish Ministry of Economy, Industry and Competitiveness and EU ERDF funds through the projects CGL2015-66966-C2-1-2-R and CGL2017- 89905-R. Conflicts of Interest: The authors declare no conflict of interest. Appendix A References A1. Articles Reviewed. Articles Identified in the Google Scholar Search Only Are Marked with an Asterisk 1. *Allen, M.L.; Elbroch, L.M.; Wilmers, C.C.; Witmer, H.U. The comparative effects of large carnivores on the acquisition of carrion by scavengers. Am. Nat. 2015, 185, 822–833. 2. Allen, M.L.; Wilmers, C.C.; Elbroch, L.M.; Golla, J.M.; Witmer, H.U. The importance of motivation, weapons, and foul odors in driving encounter competition in carnivores. Ecology 2016, 97, 1905–1912. 3. *Archer, M.S.; Elgar, M.A. Effects of decomposition on carcass attendance in a guild of carrion-breeding flies. Med. Vet. Entomol. 2003, 17, 263–271. 4. *Archer, M.S.; Elgar, M.A. Female breeding-site preferences and larval feeding strategies of carrion-breeding Calliphoridae and Sarcophagidae (Diptera): A quantitative analysis. Aust. J. Zool. 2003, 51, 165–174. 5. Atwood, T.C.; Gese, E.M. Coyotes and recolonizing wolves: Social rank mediates risk-conditional behaviour at ungulate carcasses. Anim. Behav. 2008, 75, 753–762. 6. *Blanco, G.; Cardells, J.; Garijo-Toledo, M.M. Supplementary feeding and endoparasites in threatened avian scavengers: Coprologic evidence from red kites in their wintering stronghold. Environ. Res. 2017, 155, 22–30. 7. Blumenschine, R.J. Hominid carnivory and foraging strategies, and the socio-economic function of early archaeolog- ical sites. Philos. Trans. R. Soc. Lond. B 1991, 334, 211–221. 8. *Blumenschine, R.J.; Cavallo, J.A.; Capaldo, S.D. Competition for carcasses and early hominid behavioral ecology: A case study and conceptual framework. J. Hum. Evol. 1994, 27, 197–213. Diversity 2021, 13, 28 10 of 14 9. Blumenschine, R.J.; Stanistreet, I.G.; Njau, J.K.; Bamford, M.K.; Masao, F.T.; Albert, R.M.; Stollhofen, H.; Andrews, P.; Prassack, K.A.; McHenry, L.J.; et al. Environments and hominin activities across the FLK Peninsula during Zinjanthropus times (1.84 Ma), Olduvai Gorge, Tanzania. J. Hum. Evol. 2012, 63, 364–383. 10. *Cortés-Avizanda, A.; Selva, N.; Carrete, M.; Donázar, J.A. Effects of carrion resources on herbivore spatial distribu- tion are mediated by facultative scavengers. Basic Appl. Ecol. 2009, 10, 265–272. 11. Cortés-Avizanda, A.; Carrete, M.; Serrano, D.; Donázar, J.A. Carcasses increase the probability of predation of ground-nesting birds: A caveat regarding the conservation value of vulture restaurants. Anim. Conserv. 2009, 12, 85–88. 12. Cunningham, C.X.; Johnson, C.N.; Barmuta, L.A.; Hollings, T.; Woehler, E.J.; Jones, M.E. Top carnivore decline has cascading effects on scavengers and carrion persistence. Proc. R. Soc. B 2018, 285, 20181582. 13. Daleo, P.; Alberti, J.; Avaca, M.S.; Narvarte, M.; Martinetto, M.; Iribarne, O. Avoidance of feeding opportunities by the whelk Buccinanops globulosum in the presence of damaged conspecifics. Mar. Biol. 2012, 159, 2359–2365. 14. *DeVault, T.L.; Rhodes, O.E., Jr. Identification of vertebrate scavengers of small mammal carcasses in a forested landscape. Acta Theriol. 2002, 47, 185–192. 15. Fialho, V.S.; Rodrigues, V.B.; Elliot, S.L. Nesting strategies and disease risk in necrophagous beetles. Ecol. Evol. 2018, 8, 3296–3310. 16. Fodrie, F.J.; Brodeur, M.C.; Toscano, B.J.; Powers, S.P. Friend or foe: Conflicting demands and conditional risk taking by opportunistic scavengers. J. Exp. Mar. Biol. Ecol. 2012, 422–423, 114–121. 17. *Foltan, P.; Puza, V. To complete their life cycle, pathogenic nematode-bacteria complexes deter scavengers from feeding on their host cadaver. Behav. Process. 2009, 80, 76–79. 18. Frank, S.C.; Blaalid, R.; Mayer, M.; Zedrosser, A.; Steyaert, S.M.J.G. Fear the reaper: Ungulate carcasses may generate an ephemeral landscape of fear for rodents. R. Soc. Open Sci. 2020, 7, 191644. 19. García-García, F.J.; Reyes-Martínez, M.J.; Ruiz-Delgado, M.C.; Sánchez-Moyano, J.E.; Castro-Casas, M.; Pérez-Hurtado, A. Does the gathering of shellfish affect the behavior of gastropod scavengers on sandy beaches? A field experiment. J. Exp. Mar. Biol. Ecol. 2015, 467, 1–6. 20. Halley, D.J. Interspecific dominance and risk-taking in three species of corvid scavenger. J. Yamashina Inst. Ornithol. 2001, 33, 44–50. 21. *Hunter, J.S.; Durant, S.M.; Caro, T.M. To flee or not to flee: Predator avoidance by cheetahs at kills. Behav. Ecol. Sociobiol. 2007, 61, 1033–1042. 22. *Jennelle, C.S.; Samuel, M.D.; Nolden, C.A.; Berkley, E.A. Deer carcass decomposition and potential scavenger exposure to chronic wasting disease. J. Wildl. Manage. 2009, 73, 655–662. 23. Jones, M.E. The function of vigilance in sympatric marsupial carnivores: The eastern quoll and the Tasmanian devil. Anim. Behav. 1998, 56, 1279–1284. 24. *Lev-Yadun, S.; Gutman, M. Carrion odor and cattle grazing. Comm. Integr. Biol. 2013, 6, e26111. 25. *Lupo, K.D. Experimentally derived extraction rates for marrow: Implications for body part exploitation strategies of Plio-Pleistocene hominid scavengers. J. Archaeol. Sci. 1998, 25, 657–675. 26. *Mattisson, J.; Rauset, G.R.; Odden, J.; Andrén, H.; Linnell, J.D.C.; Persson, J. Predation or scavenging? Prey body condition influences decision-making in a facultative predator, the wolverine. Ecosphere 2016, 7, e01407. 27. McKillup, S.C.; McKillup, R.V. The decision to feed by a scavenger in relation to the risks of predation and starvation. Oecologia 1994, 97, 41–48. 28. *Moleón, M.; Sánchez-Zapata, J.A.; Sebastián-González, E.; Owen-Smith, N. Carcass size shapes the structure and functioning of an African scavenging assemblage. Oikos 2015, 124, 1391–1403. 29. Moleón, M.; Martínez-Carrasco, C.; Muellerklein, O.C.; Getz, W.M.; Muñoz-Lozano, C.; Sánchez-Zapata, J.A. Carnivore carcasses are avoided by carnivores. J. Anim. Ecol. 2017, 86, 1179–1191. 30. Monahan, C.M. Tha Hadza carcass transport debate revisited and its archaeological implications. J. Archaeol. Sci. 1998, 25, 405–424. 31. Morton, B.; Chan, K. Hunger rapidly overrides the risk of predation in the subtidal scavenger Nassarius siquijorensis (Gastropoda: Nassariidae): An energy budget and a comparison with the intertidal Nassarius festivus in Hong Kong. J. Exp. Mar. Biol. Ecol. 1999, 240, 213–228. 32. *Muñoz-Lozano, C.; Martín-Vega, D.; Martínez-Carrasco, C.; Sánchez-Zapata, J.A.; Morales-Reyes, Z.; Gonzálvez, M.; Moleón, M. Avoidance of carnivore carcasses by vertebrate scavengers enables colonization by a diverse community of carrion insects. PLoS ONE 2019, 14, e0221890. 33. *Navarro, F.K.S.P.; Rezende, R. de S.; Gonçalves, J.F., Jr. Experimental assessment of temperature increase and presence of predator carcass changing the response of invertebrate shredders. Biota Neotrop. 2013, 13. Diversity 2021, 13, 28 11 of 14 34. Oliver, J.S. Estimates of hominid and carnivore involvement in the FLK Zinjanthropus fossil assemblage: Some so- cioecological implications. J. Hum. Evol. 1994, 27, 267–294. 35. *Olson, Z.H.; Beasley, J.C.; Rhodes, O.E., Jr. Carcass type affects local scavenger guilds more than habitat connectivity. PLoS ONE 2016, 11, e0147798. 36. O’Malley, C.; Elbroch, L.M.; Lendrum, P.E.; Quigley, H. Motion-triggered video cameras reveal spatial and temporal patterns of red fox foraging on carrion provided by mountain lions. PeerJ 2018, 6, e5324. 37. *Pereira, H.; Detrain, C. Pathogen avoidance and prey discrimination in ants. R. Soc. Open Sci. 2020, 7, 191705. 38. *Ragir, S.; Rosenberg, M.; Tierno, P. Gut morphology and the avoidance of carrion among chimpanzees, baboons, and early hominids. J. Anthropol. Res. 2000, 56, 477–512. 39. *Rees, J.D.; Webb, J.K.; Crowther, M.S.; Letnic, M. Carrion subsidies provided by fishermen increase predation of beach-nesting bird nests by facultative scavengers. Anim. Conserv. 2015, 18, 44–49. 40. Rees, J.D., Crowther, M.S., Kingsford, R.T., Letnic, M. Direct and indirect effects of carrion subsidies in an arid range- land: Carrion has positive effects on facultative scavengers and negative effects on a small songbird. J. Arid Environ. 2020, 179, 104174. 41. Rose, L.; Marshall, F. Meat eating, hominid sociality, and home bases revisited. Curr. Anthropol. 1996, 37, 307–338. 42. *Schlacher, T.A.; Strydom, S.; Connolly, R.M. Multiple scavengers respond rapidly to pulsed carrion resources at the land-ocean interface. Acta Oecol. 2013, 48, 7–12. 43. Schlacher, T.A.; Weston, M.A.; Lynn, D.; Schoeman, D.S.; Huijbers, C.M.; Olds, A.D.; Masters, S.; Connolly, R.M. Conservation gone to the dogs: When canids rule the beach in small coastal reserves. Biodivers. Conserv. 2015, 24, 493–509. 44. *Selva, N.; Jedrzejewska, ˛ B.; Jedrzejewski, ˛ W.; Wajrak, A. Factors affecting carcass use by a guild of scavengers in European temperate woodland. Can. J. Zool. 2005, 83, 1590–1601. 45. *Siva-Jothy, J.A.; Monteith, K.M.; Vale, P.F. Navigating infection risk during oviposition and cannibalistic foraging in a holometabolous insect. Behav. Ecol. 2018, 29, 1426–1435. 46. Steinbeiser, C.M.; Wawrzynowski, C.A.; Ramos, X.; Olson, Z.H. Scavenging and the ecology of fear: Do animal carcasses create islands of risk on the landscape? Can. J. Zool. 2017, 96, 229–236. 47. *Tranter, C.; LeFevre, L.; Evison, S.E.F.; Hughes, W.O.H. Threat detection: Contextual recognition and response to parasites by ants. Behav. Ecol. 2015, 26, 396–405. 48. Turner, W.C.; Kausrud, K.L.; Krishnappa, Y.S.; Cromsigt, J.P.G.M.; Ganz, H.H.; Mapaure, I.; Cloete, C.C.; Havarua, Z.; Küsters, M.; Getz, W.M.; et al. Fatal attraction: Vegetation responses to nutrient inputs attract herbivores to infectious anthrax carcass sites. Proc. R. Soc. B 2014, 281, 20141785. 49. *van Dijk, J.; Andersen, T.; May, R.; Andersen, R.; Andersen, R.; Landa, A. Foraging strategies of wolverines within a predator guild. Can. J. Zool. 2008, 86, 966–975. 50. *Wikenros, C.; Sand, H.; Ahlqvist, P.; Liberg, O. Biomass flow and scavengers use of carcasses after re-colonization of an apex predator. PLoS ONE 2013, 8, e77373. 51. Wikenros, C.; Ståhlberg, S.; Sand, H. Feeding under high risk of intraguild predation: Vigilance patterns of two medium-sized generalist predators. J. Mammal. 2014, 95, 862–870. 52. Willems, E.P.; van Schaik, C.P. The social organization of Homo ergaster: Inferences from anti-predator responses in extant primates. J. Hum. Evol. 2017, 109, 11–21. 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Published: Jan 13, 2021

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