Article activity feed

  1. Author Response

    Reviewer #1 (Public Review):

    The authors sought to investigate the diet of the early fossil bird Jeholornis and its implications for bird-plant interactions in early bird evolution.

    Major strengths were: 1) an exquisite near-complete cranial reconstruction of the early fossil bird Jeholornis from the Early Cretaceous of China, 2) a large sample of extant bird skulls (160) for the geometric morphometric analysis, and, 3) qualitative description of alimentary contents of extant birds.

    Major weaknesses were: 1) restriction of diet consideration to only granivory and frugivory, 2) under-detailed comparisons between the extant and extinct alimentary contents, 3) unclear explanation of the connection between early fossil birds and seed dispersal.

    Thanks for the summary of our work! To briefly reply to the weaknesses mentioned here (more details are provided in the following reply to the reviewer’s comments and suggestions):

    1. We have added supplementary analyses according to the reviewer’s suggestions, so this should have been addressed now. Our morphometric analyses attempt to explain the presence of seeds in the gut contents of some individuals of Jeholornis. We believe there are only two possible explanations of the presence of these seeds: granivory or frugivory. Therefore, we were initially motivated by the need to rigorously rule-out a granivorous explanation of the present of seeds in the gut of Jeholornis, which then would demonstrate the partially frugivorous diet of *Jeholornis *- it doesn’t have to be a specialist frugivore and its supplementary diet components don’t influence the inference that the presence of seeds results from fruit-consumption. Fruit-consumption is the key mechanism that we provide evidence of for the first time in early birds, and is central to the potential for mutualisms between plants and early birds. However, our supplementary geometric morphometric analyses do indicate some clues about its supplementary diets that are useful. In particular, they rule out some other diets e.g. piscivory or a probing diet.

    2. Our work is the first work we know to provide comparative data on the seed-containing gut contents of extant birds, as a tool to interpret fossil gut contents. For granivores and frugivores, we have done detailed 3D comparisons among several species. We think this is important, and we have done our best to document them clearly. However, for now, we have further clarified the images that we have presented, in response to a comment by referee 3 (see below). We hope that this also addresses the concerns of referee 1 here.

    3. By providing direct evidence of fruit-consumption in early birds, we provided evidence of the mechanism for potential bird-plant co-evolutionary mutualism during the Early Cretaceous. We are not showing the direct evidence of the mutualism, although note that plants invest energy in fruit production specifically to attract fruit-eating animals to act as seed dispersers. Therefore, the inference of mutualism is not far-fetched and is very likely, even if direct evidence is almost impossible to preserve in fossils - so that we tend to tone down this statement rather than making it too strong. More detailed analyses based on more new fossil discoveries in the future are expected to further explore the role of birds the Cretaceous Terrestrial Revolution. However, our study is the first step to evidence and discuss this ecological topic and the furthest we could go based on the current fossil discoveries. Nevertheless, this seems important and will be the base of future studies.

    The authors did not yet achieve their full aims because their methods limited the scope of their conclusions. Specifically, a third hypothesis that Jeholornis was neither granivorous nor frugivorous was not addressed in the study. This is especially poignant as the PCA data show overlap between the granivory and frugivory data points and the 'other diet' data points. If it is assumed that Jeholornis must be a granivore or a frugivore, then the results support frugivory over granivory for Jeholornis. However, as explained above, this assumption is not supported by the data provided so the third hypothesis needs to be tested.

    Thank you very much for stating the concern of our study. It seems that there is some misunderstanding here about our study. Our analyses attempt to explain how seeds entered the gut content of Jeholornis, not to predict diet in the absence of evidence from gut content. That is why we tested between just two alternative explanations of the gut contents in our original analyses: (1) That seeds entered the gut through granivory (seed-consumption); and (2) That seeds entered the gut through frugivory (fruit-consumption). Based on this combined evidence of seeds in the gut, comparative study of the gut contents of extant birds, plus morphometrics of the skull and mandible, we claimed partial (possibly seasonal) frugivory - a form of facultative frugivory for this lineage. Therefore, we are not claiming specialised frugivory in *Jeholornis *as the reviewer might think. However, we acknowledge that the word 'frugivorous' might be misleading to some readers, who could interpret it as meaning 'specialised frugivorous'. To avoid this misunderstanding, we did consistently use adjectives such as 'partial', 'seasonal' and 'opportunistic' in our initial submission. And we have tried to reinforce this in our revised manuscript. For example, we converted some instances of ‘frugivory’ to ‘fruit-consumption’ to indicate the act of consuming fruit rather than a perceived idea of specialised frugivory.

    We may also need to emphasize here that, the seed dispersal and frugivore ecology studies of the modern taxa show that, for most frugivores, fleshy fruits are a non-exclusive food resource, which is supplemented with other foods like animal prey and plants (Howe, 1986; Corlett, 1998; Jordano, 2000; Wilman et al., 2014). In addition, plants usually bear fruits only in certain seasons rather than being available throughout the year, which makes strictly specialized frugivore very rare. Therefore, avian frugivores occupy a wide range of diet space that is highly overlapping with some other diets. However, to reply to the comment from the reviewer and also make this clearer to some other readers, we conducted supplemental analyses by dividing 'other diets' further to test what diets *Jeholornis *possibly/impossibly had as supplements of frugivory. The results of them were shown in Figure 2 - figure supplements 3, Figure 2 - figure supplements 4 and Figure 2 - figure supplements 5 now. We revised and added these texts into the manuscript to describe the added supplemental analyses:

    “Our main analysis is intended to test why seeds entered the gut of *Jeholornis *by distinguishing between two hypotheses, either (i) fruit consumption or (ii) seed consumption (Figure 2, Figure 2 - figure supplements 2).”

    “Our supplemental analysis includes a further split of “Other diets”, separating the “Other diets” category into: (1) Probing for invertebrates; (2) Grabbing/pecking for invertebrates (Figure 2 - figure supplements 3); (3) Piscivores; (4) Animal-dominated omnivores; (5) Carnivores (Figure 2 - figure supplements 4); (6) Nectarivores; (7) Omnivores; (8) Plant-dominated omnivores (Figure 2 - figure supplements 5). Our prior expectation is that these analyses will not provide an unambiguous classification of the diet of *Jeholornis *on their own, because craniomandibular shape data does not completely differentiate among diets in birds (Navalon et al., 2019), but that they may be capable of ruling out the occurrence of some diets.”

    The results of these supplemental analyses are as the descriptions we added in the manuscript:

    “Our supplemental analyses exclude *Jeholornis *from possessing a probing diet, which occupy negative PC1 values (Figure 2 - figure supplements 3), as well as being a piscivore, which occupy positive PC2 values (Figure 2 - figure supplements 4). However, it cannot be distinguished from other diets such as the grabbing/pecking for invertebrates and omnivory (Figure 2 - figure supplements 3, 4, 5). Euclidean distances in the full multivariate shape space suggest that the mandible of *Jeholornis *is relatively similar to those of various omnivorous (e.g. Podica), seed-grinding (e.g. Calandrella), frugivorous (e.g. Crax), and invertebrate pecking (e.g. Picus) birds (Figure 2 - Source data 3).

    “Similar to the results of the mandible analyses, the results of the supplemental analyses of cranial shape also exclude *Jeholornis *from possessing a probing diet, which occupy negative PC1 values (Figure 2 - figure supplements 3), as well as being a piscivore, which occupy positive PC2 values (Figure 2 - figure supplements 4).The other diets are also undistinguishable in the supplemental analyses of cranial shape (Figure 2 - figure supplements 3, 4, 5). Euclidean distances in the multivariate shape space, excluding PC3 (which describes the large-scale differences between stem- and crown-group birds) suggest that the cranium of *Jeholornis *is relatively similar to those of various frugivorous (e.g. Manucodia), seed-grinding (e.g. Pedionomus) and invertebrate pecking (e.g. Hymenops) birds (Figure 2 - Source data 4).”

    These results are briefly merged into the discussion part:

    “Mandibular and cranial shape excludes *Jeholornis *from being having a probing/piscivorous diet, and is consistent with omnivory, grabbing/pecking for invertebrates, or processing foliage (using the gastric mill).”

    The existed main morphometric analyses show that a seed-cracking diet can be ruled out as an explanation of the presence of seeds in the gut of Jeholornis, which is its primary goal. In addition, our intention of this study is to show evidence for at least seasonal fruit consumption in some of the earliest birds (not specialised frugivorous), which all three reviewers seem to agree is a well-founded conclusion, and the bigger picture insights of our paper arise from that. Here with the new supplementary analyses inspired by the reviewer, the diet of *Jeholornis *is more detailed in our study, which may interest more readers concerning about the diet components of early birds.

    The cranial reconstruction of Jeholornis and the alimentary content data for extant birds would be invaluable to the community. The geometric morphometric data are presented in a way that obscures how much overlap there is between dietary categories (non-frugivore and non-granivore diets are grouped as 'other diets'), so the utility of these data is unclear. This aspect has hampered the ability of the authors to reconstruct diet in Jeholornis and, thus, the bigger picture insights that can be drawn from these results, limiting the likely impact of the work.

    Thank you very much for the positive comments about our cranial reconstruction of *Jeholornis *and the alimentary content data for extant birds.

    It was not our intention to obscure the overlaps between the mandible/cranial shape of frugivorous birds, and those of other birds. In fact, we believed that this was clear from the plots, and from the way we described results in the text that various birds with ‘other diets’ could have similar mandible/cranial shape to Jeholornis. This degree of overlap is also expected based on recent studies that found evidence for only quite diffuse relationships between cranial form and diet in birds (Navalón et al., 2019). However, we also see the point that some readers might be curious about the nature of particular datapoints and it would be useful to clarify this. We therefore added supplementary analyses according to the reviewer’s comment/suggestion by dividing the 'other diets' category into several much more detailed categories, so the concern of the reviewer here that “the non-frugivore and non-granivore diets are grouped as 'other diets' is expected to have been addressed here.

    Jeholornis is one of the earliest fossil birds, so understanding its diet and ecological role is important for understanding Mesozoic ecosystems and the emergence of modern ones.

    Thank you very much for this good explanation of the importance of this study, and it also is what we believed when we wrote the manuscript. We hope that the referee will be satisfied with the efforts we made to address their initial comments that that our paper on the ecology and morphology of *Jeholornis *can be published in an appropriate venue.

    Reviewer #3 (Public Review):

    Hu et al. reported on a new specimen of the early bird Jeholornis, including a nearly complete skull. Using geometric morphometrics data collected from 3D and 2D retro-deformed reconstructions of its skull, the authors convincingly dismiss a seed-cracking feeding strategy for the taxon. They then use comparisons of 3D reconstructions of ingested seeds to extant birds with known feeding strategies to convincingly argue that Jeholornis was likely at least partially frugivorous. As such, this study provides the strongest evidence yet that early birds such as Jeholornis may have played a role in bird-mediated seed dispersal strategies in the Mesozoic.

    Generally, the data presented in this paper support the authors' interpretations. The specimen at the core of this study is truly spectacular, and the authors' retro-deformation of its skull is skilled. The results of the authors' geometric morphometric analyses support their inference that Jeholornis was likely not a seed-cracker. Their comparisons of ingested seed shapes also convincingly supported a partially frugivorous diet. I especially applaud the authors' detailed description of their process of retro-deformation of the fossil skull (an example many should follow, including myself) as well as making both their raw data and their reconstructed surfaces available online.

    Thank you very much for the summary of our work!

    However, there are a few major and several minor issues that I believe need to be addressed.

    1. The implications for possible bird-mediated seed dispersal are clear in this study, but they are not conclusive. Rather, the authors (convincingly) demonstrate that Jeholornis was at least partially frugivorous -- a necessary component of such a mutualistic interaction. The authors do not demonstrate that such an interaction actually occurs. These results are nonetheless exciting and important, but I think certain statements in the paper are too strong. A notable example is the title - "Earliest evidence for frugivory and seed dispersal by birds." I would strongly urge the addition of a single word to better reflect the data presented: "Earliest evidence for frugivory and possible seed dispersal by birds." Similarly, in lines 328-329 -- "Strong indications for at least seasonal frugivory in *Jeholornis *provides direct evidence of [specialised seed-dispersal by animals during the Early Cretaceous] for the first time" -- is not true. This paper does not provide direct evidence for this, but does provide a mechanism consistent with this. There are a handful of other statements in the paper that I think should be toned down to account for this.

    Thanks for the helpful suggestions! We have revised the title to be “Earliest evidence for frugivory and potential seed dispersal by birds”, and revised this sentence to be “Evidence for at least seasonal frugivory in *Jeholornis *provides direct evidence of fruit-consumption by early birds, long before the origin of the bird crown-group. This provides an important indication of the likelihood that birds were recruited by plants for seed-dispersal very early in their evolutionary history, during the Early Cretaceous” now. We also revised through the manuscript to tone down some similar statements about the seed dispersal, such as “…indicating that birds may have been recruited for seed dispersal during the earliest stages of the avian radiation.”.

    1. Much more information should be given about the new Jeholornis specimen. In the supplement, the authors state that "a few post cranial elements" (p. 17, line 352) are preserved along with the skull -- which elements? They should be figured and briefly described in the supplement. This is of relevance to the core assumption of the paper, namely that this individual belonged to Jeholornis -- the taxonomic assignment is based partially on the tail morphology -- which I assume means that, minimally, a complete tail is preserved. The authors also mention the pelvic morphology of the new specimen, so I assume at least some part of the pelvis is preserved. These should all be figured. Most anatomical discussion is limited to the skull (and especially the palate), which is understandable, given the focus of the paper. However, with that in mind, more attention should be paid to the retro-deformation of the skull. Figure 1 is quite attractive, but I'm confused by the differences in depicted preservation between the 3D (Fig. 1C, D) and 2D (Fig. 1E, F) reconstructions. For example, the braincase is not shown in panel C but is in panel E -- why? Is its shape inferred from other specimens for panel E? Again, I very much appreciate the inclusion of near step-by-step description of how the rostrum was retro-deformed. Minimally, a few comments on what isn't preserved would be useful.
    1. We added the photograph of the whole slab of *Jeholornis *STM 3-8 as Figure 1 - figure supplements 1 here (the eLife format for supplementary figures), and revised this sentence to be “…and a few postcranial elements including the vertebral column, the pelvic girdle and fragmentary hindlimbs.” now. As you could see from the photograph, there are very few valid information could be extracted from the incompletely preserved postcranial elements. Considering this paper is focusing on the skull, we only mentioned the relatively better-preserved tail and pelvis in the taxonomic part.

    2. We added “Dashed-lines indicate the elements not preserved but suspected to exist.” in the legend of Figure 1, and added the details of reconstructions of unpreserved elements in the end of CT scans and digital reconstructions in Materials and Methods part: “However, since the braincase is too flattened to be used as the reference for 3D retrodeformation, it was omitted in Figure1C and reconstructed according to its common shape in early birds in Figure 1E. The ectopterygoid is not preserved but suspected to exist as discussed in the Cranial Anatomy part, therefore it was reconstructed according to the shape of this element among other stem birds e.g. *Archaeopteryx *and *Sapeornis *(Elzanowski and Wellnhofer, 1996; Hu et al., 2019).”

    1. The figures are visually attractive but I found some of them confusing or unclear. See my comments above regarding Figure 1. Despite the red arrows in Figure 4 and the supplemental figure, I was hard pressed to understand precisely what set the indicated seeds apart from the rest. In some cases I could see slight "dents" where one or two of the arrows indicated, but it was hard for me to see, even when I zoomed in on my screen. I think inset panels featuring zoom-ins on the indicated regions would be very useful in making the point the authors intend. Also, I don't know if the supplemental image naming/number scheme was imposed by the journal or is a choice by the authors, but I found it baffling. Something more traditional (like "Fig. S1" or "Supplemental Figure 1") would be much more efficient.
    1. We have clarified the confusions in Figure 1 as suggested. For Figure 4 and related supplementary figures, the 3D reconstructed seeds are pretty clear, such as the broken ones in Figure 4B. The broken seeds in the scanning slices are more difficult to observe as the reviewer said, since the seed husks are very thin so that they are only slightly brighter, and that’s why we put the red arrows indicating the breakages there. To help readers observe them easier, we added some zoom-in panels and line drawings for the representative ones (not all of them since otherwise it would be too many) now as suggested by the reviewer;

    2. The supplementary image naming/number scheme was imposed by the journal, and it would be more clear when the paper is digitally published, since these supplementary images will be connected to links in the legends of the main figures.

    Was this evaluation helpful?
  2. Evaluation Summary:

    This article will be of interest to paleobiologists studying the evolution of avian diets and/or prehistoric ecosystem dynamics. The study uses an exceptional new specimen of an early diverging stem bird with a near-complete skull, to reassess diet in the taxon and explore possible early mechanisms for bird-mediated seed dispersal. The claim for frugivory is currently insufficiently supported.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their name with the authors.)

    Was this evaluation helpful?
  3. Reviewer #1 (Public Review):

    The authors sought to investigate the diet of the early fossil bird Jeholornis and its implications for bird-plant interactions in early bird evolution.

    Major strengths were: 1) an exquisite near-complete cranial reconstruction of the early fossil bird Jeholornis from the Early Cretaceous of China, 2) a large sample of extant bird skulls (160) for the geometric morphometric analysis, and, 3) qualitative description of alimentary contents of extant birds.

    Major weaknesses were: 1) restriction of diet consideration to only granivory and frugivory, 2) under-detailed comparisons between the extant and extinct alimentary contents, 3) unclear explanation of the connection between early fossil birds and seed dispersal.

    The authors did not yet achieve their full aims because their methods limited the scope of their conclusions. Specifically, a third hypothesis that Jeholornis was neither granivorous nor frugivorous was not addressed in the study. This is especially poignant as the PCA data show overlap between the granivory and frugivory data points and the 'other diet' data points. If it is assumed that Jeholornis must be a granivore or a frugivore, then the results support frugivory over granivory for Jeholornis. However, as explained above, this assumption is not supported by the data provided so the third hypothesis needs to be tested.

    The cranial reconstruction of Jeholornis and the alimentary content data for extant birds would be invaluable to the community. The geometric morphometric data are presented in a way that obscures how much overlap there is between dietary categories (non-frugivore and non-granivore diets are grouped as 'other diets'), so the utility of these data is unclear. This aspect has hampered the ability of the authors to reconstruct diet in Jeholornis and, thus, the bigger picture insights that can be drawn from these results, limiting the likely impact of the work.

    Jeholornis is one of the earliest fossil birds, so understanding its diet and ecological role is important for understanding Mesozoic ecosystems and the emergence of modern ones.

    Was this evaluation helpful?
  4. Reviewer #2 (Public Review):

    Hu et al. describe the skull morphology and gut contents of Jeholornis. They show the gut contains uncracked seeds and the beak shape is more like that of frugivorous or omnivorous birds than like seed-cracking or seed-grinding granivorous birds. Instead, available evidence suggests that Jeholornis consumed seeds while feeding on accessory tissues associated with the seeds, perhaps fruits. The comparisons with modern bird beaks and alimentary contents are detailed and demonstrate the utility of CT scans and digital reconstructions for studies of comparative biology using museum specimens.

    Was this evaluation helpful?
  5. Reviewer #3 (Public Review):

    Hu et al. reported on a new specimen of the early bird Jeholornis, including a nearly complete skull. Using geometric morphometrics data collected from 3D and 2D retro-deformed reconstructions of its skull, the authors convincingly dismiss a seed-cracking feeding strategy for the taxon. They then use comparisons of 3D reconstructions of ingested seeds to extant birds with known feeding strategies to convincingly argue that Jeholornis was likely at least partially frugivorous. As such, this study provides the strongest evidence yet that early birds such as Jeholornis may have played a role in bird-mediated seed dispersal strategies in the Mesozoic.

    Generally, the data presented in this paper support the authors' interpretations. The specimen at the core of this study is truly spectacular, and the authors' retro-deformation of its skull is skilled. The results of the authors' geometric morphometric analyses support their inference that Jeholornis was likely not a seed-cracker. Their comparisons of ingested seed shapes also convincingly supported a partially frugivorous diet. I especially applaud the authors' detailed description of their process of retro-deformation of the fossil skull (an example many should follow, including myself) as well as making both their raw data and their reconstructed surfaces available online.

    However, there are a few major and several minor issues that I believe need to be addressed.

    1. The implications for possible bird-mediated seed dispersal are clear in this study, but they are not conclusive. Rather, the authors (convincingly) demonstrate that Jeholornis was at least partially frugivorous -- a necessary component of such a mutualistic interaction. The authors do not demonstrate that such an interaction actually occurs. These results are nonetheless exciting and important, but I think certain statements in the paper are too strong. A notable example is the title - "Earliest evidence for frugivory and seed dispersal by birds." I would strongly urge the addition of a single word to better reflect the data presented: "Earliest evidence for frugivory and *possible* seed dispersal by birds." Similarly, in lines 328-329 -- "Strong indications for at least seasonal frugivory in Jeholornis provides direct evidence of [specialised seed-dispersal by animals during the Early Cretaceous] for the first time" -- is not true. This paper does not provide *direct* evidence for this, but *does* provide a mechanism consistent with this. There are a handful of other statements in the paper that I think should be toned down to account for this.

    2. Much more information should be given about the new Jeholornis specimen. In the supplement, the authors state that "a few post cranial elements" (p. 17, line 352) are preserved along with the skull -- which elements? They should be figured and briefly described in the supplement. This is of relevance to the core assumption of the paper, namely that this individual belonged to Jeholornis -- the taxonomic assignment is based partially on the tail morphology -- which I assume means that, minimally, a complete tail is preserved. The authors also mention the pelvic morphology of the new specimen, so I assume at least some part of the pelvis is preserved. These should all be figured. Most anatomical discussion is limited to the skull (and especially the palate), which is understandable, given the focus of the paper. However, with that in mind, more attention should be paid to the retro-deformation of the skull. Figure 1 is quite attractive, but I'm confused by the differences in depicted preservation between the 3D (Fig. 1C, D) and 2D (Fig. 1E, F) reconstructions. For example, the braincase is not shown in panel C but is in panel E -- why? Is its shape inferred from other specimens for panel E? Again, I very much appreciate the inclusion of near step-by-step description of how the rostrum was retro-deformed. Minimally, a few comments on what isn't preserved would be useful.

    3. The figures are visually attractive but I found some of them confusing or unclear. See my comments above regarding Figure 1. Despite the red arrows in Figure 4 and the supplemental figure, I was hard pressed to understand precisely what set the indicated seeds apart from the rest. In some cases I could see slight "dents" where one or two of the arrows indicated, but it was hard for me to see, even when I zoomed in on my screen. I think inset panels featuring zoom-ins on the indicated regions would be very useful in making the point the authors intend. Also, I don't know if the supplemental image naming/number scheme was imposed by the journal or is a choice by the authors, but I found it baffling. Something more traditional (like "Fig. S1" or "Supplemental Figure 1") would be much more efficient.

    Was this evaluation helpful?