First bone-cracking dog coprolites provide new insight into bone consumption in Borophagus and their unique ecological niche

  1. Xiaoming Wang  Is a corresponding author
  2. Stuart C White  Is a corresponding author
  3. Mairin Balisi  Is a corresponding author
  4. Jacob Biewer  Is a corresponding author
  5. Julia Sankey  Is a corresponding author
  6. Dennis Garber  Is a corresponding author
  7. Z Jack Tseng
  1. Natural History Museum of Los Angeles County, United States
  2. American Museum of Natural History, United States
  3. University of California, United States
  4. California State University, United States
  5. California State University Stanislaus, United States
  6. Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, United States

Peer review process

This article was accepted for publication as part of eLife's original publishing model.

History

  1. Version of Record updated
  2. Version of Record published
  3. Accepted
  4. Received

Decision letter

  1. Jessica C Thompson
    Reviewing Editor; Emory University, United States

In the interests of transparency, eLife includes the editorial decision letter and accompanying author responses. A lightly edited version of the letter sent to the authors after peer review is shown, indicating the most substantive concerns; minor comments are not usually included.

Thank you for submitting your article "First bone-cracking dog coprolites provide insight into bone consumption in Borophagus and their unique ecological niche" for consideration by eLife. Your article has been favorably evaluated by Diethard Tautz (Senior Editor) and three reviewers, one of whom, Jessica Thompson (Reviewer #1), is a member of our Board of Reviewing Editors. The following individuals involved in review of your submission have agreed to reveal their identity: Lars Werdelin (Reviewer #2); Katherina Bastl (Reviewer #3).

The reviewers have discussed the reviews with one another and the Reviewing Editor has drafted this decision to help you prepare a revised submission. Our goal is to provide the essential revision requirements as a single set of instructions, so that you have a clear view of the revisions that are necessary for us to publish your work.

Summary:

This study contributes to our understanding of the structure of the North American carnivore guilds of the Oligocene-Pliocene. It uses data from coprolite size, shape, and bony inclusions to corroborate and extend current work on comparative functional morphology of borophagine dogs and hyenas. The paper offers new independent, empirical evidence for convergent evolution of bone-crushing morphologies/adaptations in multiple carnivore lineages, and examines the role of this adaptation in ecological structure and faunal turnover.

Essential revisions:

This is a well-written and thorough study that makes a novel contribution to understanding convergent evolution of bone-crushing morphologies/adaptations in multiple carnivore lineages. The following essential revisions should be made to enable acceptance.

1) The coprolite data essentially reinforce what was already understood based on bony morphology, so the discussion of the ecological implications should be emphasized. For example, the final sentence is probably the most important insight/conclusion and it would increase the impact of the paper to extend this discussion. This should be done in light of points -4, below.

2) There should be a much more specific discussion of how the bone-crunching adaptation is actually operationalized ecologically, and what implications this would have for adaptations/niches in other lineages when Borophagus goes extinct. This should be done through explicit connection to other aspects of anatomy in modern carnivores, especially spotted and striped hyenas, in order to add nuance to the discussion of the ecological positioning of Borophagus. This additional discussion does not need to be extensive, but simply more specific and detailed (a reworking of the present discussion), with greater emphasis on explicit comparisons over general descriptions.

3) The focus on wolves and spotted hyenas has turned the Discussion entirely to the topic of "bone-eating top predators" (this begs the question of how a "top predator" is defined and how much bone eating is required for a species to be considered a "bone-eater"), and away from any consideration that Borophagus may be more ecologically akin to striped, rather than spotted hyenas. Thus, the section on the "Evolution of the Bone-Eating Top Predator" needs to be either rewritten as a broader discussion of the ecological role of B. parvus, or deleted.

4) The authors should seek to find a way to obtain a value for spotted hyena gastric acid if they are to make an argument about diet based on that characteristic. Similarly, a comparison of gut morphology of canids and hyenids and their implications for bone consumption would be useful (specifically, the role of regurgitates versus passing of bone). If a published value (or personal communication from a cited source) truly does not exist for gastric acid, then this section should be de-emphasized because it is otherwise somewhat speculative.

5) Although Figure 7 is appealing, a more instructional Figure 7 would be of the bony morphology of Borophagus that provides supporting evidence for the bone-crunching adaptation. The figures would also benefit from more explicit visual comparisons of scats between extant carnivorans at Figure 1, rather than a picture from a website of only hyena scat.

https://doi.org/10.7554/eLife.34773.022

Author response

Essential revisions:

This is a well-written and thorough study that makes a novel contribution to understanding convergent evolution of bone-crushing morphologies/adaptations in multiple carnivore lineages. The following essential revisions should be made to enable acceptance.

1) The coprolite data essentially reinforce what was already understood based on bony morphology, so the discussion of the ecological implications should be emphasized. For example, the final sentence is probably the most important insight/conclusion and it would increase the impact of the paper to extend this discussion. This should be done in light of points -4, below.

We have added a new section at end of this paper called “Consideration of the ecological role of Borophagus” as well as expanding the sections on “Reconstructing the potential ecological role of Borophagus” and “Social hunting”. These additions provide substantial new discussion related to ecological implications.

2) There should be a much more specific discussion of how the bone-crunching adaptation is actually operationalized ecologically, and what implications this would have for adaptations/niches in other lineages when Borophagus goes extinct. This should be done through explicit connection to other aspects of anatomy in modern carnivores, especially spotted and striped hyenas, in order to add nuance to the discussion of the ecological positioning of Borophagus. This additional discussion does not need to be extensive, but simply more specific and detailed (a reworking of the present discussion), with greater emphasis on explicit comparisons over general descriptions.

We agree. Our new section (Consideration of the ecological role of Borophagus) focuses on the unique combination of borophagine craniodental morphology (strongly trending toward bone-crushing) and their apparently less than thorough digestion of bones. After their extinction before Pleistocene, these distinct morphological traits are either poorly developed or absent among modern North American carnivorans. This suggests that there is no ecological morphological equivalent of Borophagus in modern day North American food webs. Bone crushing carnivorans also play a significant role as decomposers, such as extant spotted hyenas, in accelerating nutrient cycling pathways and in bypassing invertebrate and microbe decomposers in the detrital food web.

3) The focus on wolves and spotted hyenas has turned the Discussion entirely to the topic of "bone-eating top predators" (this begs the question of how a "top predator" is defined and how much bone eating is required for a species to be considered a "bone-eater"), and away from any consideration that Borophagus may be more ecologically akin to striped, rather than spotted hyenas. Thus, the section on the "Evolution of the Bone-Eating Top Predator" needs to be either rewritten as a broader discussion of the ecological role of B. parvus, or deleted.

Indeed, the spotted hyena is an extreme example of "bone-eating top predators" in modern carnivore guilds, although bone-crushing adaptations, as shown in craniodental specializations, are not uncommon in the late Cenozoic. We use the spotted hyena as a relatively well-studied case for comparison, but we are mindful that borophagine canids are probably more analogous in its ecomorphology to the brown and stripped hyenas. The latter, however, also have a long history of independent evolution from the canids, with very different starting points in dental batteries and their loci of maximum mechanical bite forces (Werdelin, 1989). We accept the reviewers’ suggestion and added a new paragraph in this section (now called “Reconstructing the potential ecological role of Borophagus”) to address their concerns.

4) The authors should seek to find a way to obtain a value for spotted hyena gastric acid if they are to make an argument about diet based on that characteristic. Similarly, a comparison of gut morphology of canids and hyenids and their implications for bone consumption would be useful (specifically, the role of regurgitates versus passing of bone). If a published value (or personal communication from a cited source) truly does not exist for gastric acid, then this section should be de-emphasized because it is otherwise somewhat speculative.

Despite an extensive search (including contacting ecologists and physiologists), we were unable to obtain an acidity value for spotted hyenas stomach from a published source. Therefore, we have tempered our discussion with additional cautionary notes.

5) Although Figure 7 is appealing, a more instructional Figure 7 would be of the bony morphology of Borophagus that provides supporting evidence for the bone-crunching adaptation. The figures would also benefit from more explicit visual comparisons of scats between extant carnivorans at Figure 1, rather than a picture from a website of only hyena scat.

This is a good idea. We added a new Figure 7 featuring a skull, lower jaw, and teeth of Borophagus secundus. This figure helps to illustrate typical cranial and dental adaptations in borophagine bone-crushing species. For comparison, we have also added a photo of a wolf scat in Figure 1.

https://doi.org/10.7554/eLife.34773.023

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  1. Xiaoming Wang
  2. Stuart C White
  3. Mairin Balisi
  4. Jacob Biewer
  5. Julia Sankey
  6. Dennis Garber
  7. Z Jack Tseng
(2018)
First bone-cracking dog coprolites provide new insight into bone consumption in Borophagus and their unique ecological niche
eLife 7:e34773.
https://doi.org/10.7554/eLife.34773

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https://doi.org/10.7554/eLife.34773