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

Round 1

Reviewer 1 Report

Overall I feel that this paper makes a worthwhile advancement to the field of scavenging ecology. I have just a few comments that I think will strengthen the paper and provide some clarity.

In the first paragraph, I think the authors should explicitly state what the landscape of fear is. Currently the only description is “the ‘landscape of fear’ induced by predation risk” and I think a sentence or two with more detail about the landscape of fear would make the concept more clear.

Last paragraph of introduction- this could benefit from a little more discussion of why the topic is important to investigate. Currently it only mentions “eco-evolutionary implications” which is a bit vague. To me, stating that the aim is to “emphasize the central role” comes across as a bit circular in that you already know the role to be central and are setting out to provide evidence for this. I think something along the lines of “examining the role that carrion plays in landscapes of fear” or “assessing the extent to which carrion constitutes a landscape of fear” would be better. Also, I think some more explicit aims could be beneficial because it isn’t entirely clear to me what the aims are. In particular, I find the “main ways” to be vague and should be replaced by something more specific like the “ecological/biological mechanisms by which…”

Also, it should be stated somewhere that “scary” is “landscape of fear.” Using “disgusting” in reference to “landscape of disgust” is apparent, but not as much with fear since it doesn’t go from noun to adjective as smoothly.

Examining the geographic locations of these studies could also be interesting to show where studies on these topics have and have not been done. The last paragraph on page 5 indicates that many of the studies were on prehistoric hominins. It would be interesting to break up the studies into prehistoric/not prehistoric or something similar as I would think these would be very different in nature. The former would be more about scavenging and human evolution whereas I think the latter may be more informative for examining how fear and disgust shape scavenging assemblages in the present day.

Is physiological missing from figure 1D? Even if it is zero, it should still be in the figure since this is a category that was considered. Also somewhere it could be helpful (maybe in the last section) to provide examples of each of these mechanisms evaluated. It isn’t immediately apparent to me what a physiological effect of the carcass would be. Also considering the lack of physiological responses- do the authors have any speculation as to why this is? I’m just wondering if the most common methodologies employed in scavenging studies (camera trapping or direct observations) would preclude detecting certain responses such as physiological. To this end, it could be beneficial to broadly categorize the methodologies used in the studies.

Figures 4 and 5 provide a good illustration for all the conceivable pathways and which of these have been investigated. Just curious here- is there also a hypothetical pathway going from the canid to the lion for disgust? If the lion is physically deterring the subordinate species from accessing the carcass, couldn’t the lion be infected with a parasite through this interaction?

There are also some further factors that may influence the landscape of disgust/fear. Landscape of disgust may be dynamic temporally if seasonal changes in weather lead to changes in infection risk. There may also be an interaction with the carcass and the traditional notion of the landscape of fear- scavenging may be riskier in habitats where predation risk is higher. There is an opportunity here to elaborate further on the factors impacting the extent to which a scavenger perceives the carcass as scary or disgusting, although this may be too speculative in nature for the authors’ liking given the rather limited scope of research on these topics.

Also, check the citations. In the text of methods, Haddaway 2015 is reference 14, but is reference 63 in the reference section.

Author Response

Overall I feel that this paper makes a worthwhile advancement to the field of scavenging ecology. I have just a few comments that I think will strengthen the paper and provide some clarity.
** Our response: We thank you for your overall positive assessment and constructive comments.

In the first paragraph, I think the authors should explicitly state what the landscape of fear is. Currently the only description is “the ‘landscape of fear’ induced by predation risk” and I think a sentence or two with more detail about the landscape of fear would make the concept more clear.

** Our response: We have included the definition provided by Buck et al.

Last paragraph of introduction- this could benefit from a little more discussion of why the topic is important to investigate. Currently it only mentions “eco-evolutionary implications” which is a bit vague.

** Our response: We have done some rewording and added a couple of sentences in the Introduction to make more explicit why the topic is important to investigate: “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]”.

To me, stating that the aim is to “emphasize the central role” comes across as a bit circular in that you already know the role to be central and are setting out to provide evidence for this. I think something along the lines of “examining the role that carrion plays in landscapes of fear” or “assessing the extent to which carrion constitutes a landscape of fear” would be better.

** Our response: We have changed “emphasize the central role” to “examine the role”.

Also, I think some more explicit aims could be beneficial because it isn’t entirely clear to me what the aims are. In particular, I find the “main ways” to be vague and should be replaced by something more specific like the “ecological/biological mechanisms by which…”.

** Our response: We have now specified what we mean by “main ways”: “, 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”.

Also, it should be stated somewhere that “scary” is “landscape of fear.” Using “disgusting” in reference to “landscape of disgust” is apparent, but not as much with fear since it doesn’t go from noun to adjective as smoothly.

** Our response: We now explain in the first sentence of the second paragraph of the Introduction that “scary” relates to the landscape of fear and “disgusting” relates to the landscape of disgust.

Examining the geographic locations of these studies could also be interesting to show where studies on these topics have and have not been done. The last paragraph on page 5 indicates that many of the studies were on prehistoric hominins. It would be interesting to break up the studies into prehistoric/not prehistoric or something similar as I would think these would be very different in nature. The former would be more about scavenging and human evolution whereas I think the latter may be more informative for examining how fear and disgust shape scavenging assemblages in the present day.

** Our response: We have redone the Fig. 1 to include a map of the geographic location of the reviewed studies and a graphic summarizing the proportion of fear- and disgust-related articles that dealt with prehistoric and historic periods. Moreover, we have added some text to comment on the main findings.

Is physiological missing from figure 1D? Even if it is zero, it should still be in the figure since this is a category that was considered.

** Our response: We have included this category in the Fig. 1D (now Fig. 1E).

Also somewhere it could be helpful (maybe in the last section) to provide examples of each of these mechanisms evaluated. It isn’t immediately apparent to me what a physiological effect of the carcass would be.

** Our response: Now we specify in the Introduction that predation and parasitism risk may have different physiological effects on victims, such as stress. As we now state in the last section, “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”.

Also considering the lack of physiological responses- do the authors have any speculation as to why this is? I’m just wondering if the most common methodologies employed in scavenging studies (camera trapping or direct observations) would preclude detecting certain responses such as physiological. To this end, it could be beneficial to broadly categorize the methodologies used in the studies.

** Our response: We have redone the Fig. 1 to include a graphic summarizing the main study design approaches used in the reviewed articles (field observation, field experiment, field quasi-experiment, mesocosm experiment, other), as well as the main observation methods (direct, camera-trap, other). Moreover, we have added some text to comment on the main findings.

Figures 4 and 5 provide a good illustration for all the conceivable pathways and which of these have been investigated. Just curious here- is there also a hypothetical pathway going from the canid to the lion for disgust? If the lion is physically deterring the subordinate species from accessing the carcass, couldn’t the lion be infected with a parasite through this interaction?

** Our response: You are absolutely right; we have made bidirectional the arrow that links the canid and the lion (and the one that links both canids).

There are also some further factors that may influence the landscape of disgust/fear. Landscape of disgust may be dynamic temporally if seasonal changes in weather lead to changes in infection risk. There may also be an interaction with the carcass and the traditional notion of the landscape of fear- scavenging may be riskier in habitats where predation risk is higher. There is an opportunity here to elaborate further on the factors impacting the extent to which a scavenger perceives the carcass as scary or disgusting, although this may be too speculative in nature for the authors’ liking given the rather limited scope of research on these topics.

** Our response: We have added some more discussion on the factors that may influence the landscape of disgust/fear: “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]”. Moreover, we now specify: “However, fully understanding of animal behavior around carrion resources require exploring simultaneously different sources of risk [1], as avoiding one risk may increase [69] or decrease [70] another”. While we could add much more discussion on the aspects highlighted by both reviewers, we prefer not to do that in order to keep the focus on the big picture.

Also, check the citations. In the text of methods, Haddaway 2015 is reference 14, but is reference 63 in the reference section.

** Our response: As stated above in our response to the Academic Editor, when we submitted the ms, the references for the main text were separated from the references included in the Appendix. This is because not all references found in the literature review are cited in the main text. However, it looks like all references were joined in a single “References” section after submission, which has led to this and other confusions among the reviewers. To avoid similar confusion among the readership, we have asked to maintain both sets of references separated.

Reviewer 2 Report

This manuscript is a literature review addressing the knowledge gaps in the role carrion plays in mediating cascading effects in the landscapes of fear and disgust. It pinpoints important perspectives of study in this area of research, and gives an opportunity to think more globally about both landscapes -not always separately. This is a well-written and interesting review but I also think that its potential to reach the appropriate audiences could be maximized by addressing the following points:

1/ The ‘landscape of peril’ is mentioned in the abstract and as a keyword but remains absent from the rest of the text. I recommend the introduction of this new concept in the main text. It should be emphasized as this is the formulation of one of the main outcome of this review.

2/ The references (numbered in the main text) do not match with the numbers in the list of references at the end of the text, which is confusing. For example, [1] and [2] in the main text are 50. And 51. in the list. Logically, I thus assumed that [3] was 52. Cunningham et al. 2018.

3/ In the Methods, the authors state that they divided the selected papers in two main groups, one for fear and one for disgust. Does that mean that no empirical study has attempted to address the two together yet? If so, it may be good to mention it. In addition, it remains unclear why some empirical studies found in the list of references are not part of the reviewed/selected articles, e.g. 52.

4/ The use of the term ‘disgust’ in behavioral ecology is very recent (see e.g. Sarabian et al. 2018; Evolution of pathogen and parasite avoidance behaviours). Other similar empirical studies as the ones selected for this review exist, though the terminology is different and does not use the keywords used for the search (e.g. ‘parasite avoidance’ instead of ‘parasite risk’), which may be an additional limitation to the number of studies found for ‘disgust’.

5/ The rules of predator and pathogen avoidance in aquatic environments may be different than in terrestrial environments -maybe even more when it comes to the spread and perception of sensory cues from carcasses. Potential differences across these environments remain completely unaddressed in the discussion. The authors may get some insights from a previous review on parasite avoidance in aquatic environments (Behringer et al. 2018).

6/ Figure 2: The fact that herbivores are also susceptible to parasites at carnivore carcass sites is mentioned in the legend but not reflected in the illustration (A). It may also be useful to remind readers what ‘parasites’ encompass, e.g. all pathogenic and non-pathogenic organisms with a parasitic way of life (Combes 2001, Parasitism: the ecology and evolution of intimate interactions) including bacteria, viruses, protozoans, nematodes.

7/ Following up on what ‘parasites’ are/mean, it may also be useful to explain why parasite infection risk at carcass sites is dynamic. Indeed, infectious stages from these different parasites and pathogens vary over time and across types (e.g. bacteria/viruses vs nematodes).

Author Response

This manuscript is a literature review addressing the knowledge gaps in the role carrion plays in mediating cascading effects in the landscapes of fear and disgust. It pinpoints important perspectives of study in this area of research, and gives an opportunity to think more globally about both landscapes -not always separately. This is a well-written and interesting review but I also think that its potential to reach the appropriate audiences could be maximized by addressing the following points:

** Our response: We thank you for your overall positive assessment. We have addressed your constructive comments as follows:

1/ The ‘landscape of peril’ is mentioned in the abstract and as a keyword but remains absent from the rest of the text. I recommend the introduction of this new concept in the main text. It should be emphasized as this is the formulation of one of the main outcome of this review.

** Our response: We have explained this term in the first paragraph of the Introduction.

2/ The references (numbered in the main text) do not match with the numbers in the list of references at the end of the text, which is confusing. For example, [1] and [2] in the main text are 50. And 51. in the list. Logically, I thus assumed that [3] was 52. Cunningham et al. 2018.

** Our response: As stated above in our response to the Academic Editor, when we submitted the ms, the references for the main text were separated from the references included in the Appendix. This is because not all references found in the literature review are cited in the main text. However, it looks like all references were joined in a single “References” section after submission, which has led to this and other confusions among the reviewers. To avoid similar confusion among the readership, we have asked to maintain both sets of references separated.

3/ In the Methods, the authors state that they divided the selected papers in two main groups, one for fear and one for disgust. Does that mean that no empirical study has attempted to address the two together yet? If so, it may be good to mention it.

** Our response: We have now specified in Results that “None article empirically explored simultaneously both types of risk”.

In addition, it remains unclear why some empirical studies found in the list of references are not part of the reviewed/selected articles, e.g. 52.

** Our response: Reference no. 52 was included in our literature review indeed. Please see our response to your comment no. 2 above.

4/ The use of the term ‘disgust’ in behavioral ecology is very recent (see e.g. Sarabian et al. 2018; Evolution of pathogen and parasite avoidance behaviours). Other similar empirical studies as the ones selected for this review exist, though the terminology is different and does not use the keywords used for the search (e.g. ‘parasite avoidance’ instead of ‘parasite risk’), which may be an additional limitation to the number of studies found for ‘disgust’.

** Our response: We have included the terms “parasite* avoidance”, “infection avoidance” and “disease avoidance” in our search (see Methods). However, despite this terms have been widely used in the scientific literature, we only found three additional articles related to carrion (WoS: 1 valid article; Google Scholar: 2 additional valid articles). Thus, there are no major changes in our results and conclusions. We have modified the figures when appropriate.

5/ The rules of predator and pathogen avoidance in aquatic environments may be different than in terrestrial environments -maybe even more when it comes to the spread and perception of sensory cues from carcasses. Potential differences across these environments remain completely unaddressed in the discussion. The authors may get some insights from a previous review on parasite avoidance in aquatic environments (Behringer et al. 2018).

** Our response: Undoubtedly, you identified another very important point here. We have included a new paragraph on this regard in the last section: “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 qualitatively 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”.

6/ Figure 2: The fact that herbivores are also susceptible to parasites at carnivore carcass sites is mentioned in the legend but not reflected in the illustration (A).

** Our response: We have added the missing arrow to Figs. 2A and 3A.

It may also be useful to remind readers what ‘parasites’ encompass, e.g. all pathogenic and non-pathogenic organisms with a parasitic way of life (Combes 2001, Parasitism: the ecology and evolution of intimate interactions) including bacteria, viruses, protozoans, nematodes.

** Our response: Now, we have specified that “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]”.

7/ Following up on what ‘parasites’ are/mean, it may also be useful to explain why parasite infection risk at carcass sites is dynamic. Indeed, infectious stages from these different parasites and pathogens vary over time and across types (e.g. bacteria/viruses vs nematodes).

** Our response: We have done some rewording and added a new sentence to expand this idea: “We highlight that, given the generally unpredictable and ephemeral nature of carrion [61,62,73], the very different life cycles of different parasite species [71], and the seasonality associated with their infective stages [72], carcass-induced landscape of disgust may be also highly dynamic. […] 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]”.

Round 2

Reviewer 2 Report

I thank the authors for their responses to my previous comments and for revising their manuscript accordingly. I do not have further comments beside two typos to consider: 

• Abstract: I would stick to 'landscape of peril' and not 'landscapes of peril' - the former reflecting the combination of both landscapes of fear and disgust
• Conclusions: In the last sentence, here I would put the plural form for "landscapes of fear and disgust"