Birds and plants have a close relationship that has developed over millions of years. Birds became diverse and abundant around 135 million years ago. Shortly after, plants started developing new and different kinds of fruits. Today, fruit-eating birds help plants to reproduce by spreading seeds in their droppings. This suggests that birds and plants have coevolved, changing together over time. But it is not clear exactly how their relationship started.

One species that might hold the answers is an early bird species known as Jeholornis. It lived in China in the Early Cretaceous, around 120 million years ago. Palaeontologists have discovered preserved seeds inside its fossilised remains. The question is, how did they get there? Some birds eat seeds directly, cracking them open or grinding them up in the stomach to extract the nutrients inside. Other birds swallow seeds when they are eating fruit. If Jeholornis belonged to this second group, it could represent one of the early steps in plant-bird coevolution.

Hu et al. scanned and reconstructed a preserved Jeholornis skull and compared it to the skulls, especially the mandibles, of modern birds, including species that grind seeds, species that crack seeds and species that eat fruits, leaving the seeds whole. The analyses ruled out seed cracking. But it could not distinguish between seed grinding and fruit eating. Hu et al. therefore compared the seed remains found inside Jeholornis fossils to seeds eaten by modern birds. The fossilised seeds were intact and showed no evidence of grinding. This suggests that Jeholornis ate whole fruits for at least part of the year.

At around the time Jeholornis was alive, the world was entering a phase called the Cretaceous Terrestrial Revolution, which was characterized by an explosion of new species and an expansion of both flowering plants and birds. This finding opens new avenues for scientists to explore how plant and birds might have evolved together. Similar analyses could unlock new information about how other species interacted with their environments.

Birds are among the most speciose extant vertebrate groups, playing unique ecological roles through their diverse flight and dietary adaptations (Prum et al., 2015). Crown-group birds include both specialised and opportunistic frugivores, that collectively are major consumers of fruits and important agents of seed dispersal. However, the occurrence of fruit consumption among early birds, outside the crown-group, is not yet clear. The early ecological diversification of birds in the Early Cretaceous (>130 Ma) (Yang et al., 2020) was a landmark event in the evolution of terrestrial ecosystems, adding considerably to species richness of terrestrial ecosystems (Benson, 2018a; Yu et al., 2021), and with impacts on the evolutionary histories of other flying groups (Benson et al., 2014b; Clapham and Karr, 2012). This was followed by a considerable long-term expansion of the abundance and disparity of fruits and fruit-like structures through much of the Cretaceous (Eriksson et al., 2000a; Eriksson, 2008), as part of the major floral transition from gymnosperm- to angiosperm-dominated floras that is often referred to as the ‘Cretaceous Terrestrial Revolution’ (KTR) (Benton, 2010; Lloyd et al., 2008). A macroevolutionary connection between early birds and this important event of fruit evolution has been suggested (Pejchar et al., 2008; Sekercioglu, 2006; Tiffney, 2004), but is so far unsubstantiated by fossil evidence of fruit consumption by early birds, limiting our understanding of the evolutionary origins of an important aspect of plant–animal interactions.

The Jeholornithiformes from the Early Cretaceous Jehol Biota of China are one of the earliest-diverging avian lineages and are morphologically very distinct from crown-group birds, retaining an elongate, bony tail, which is absent in all other birds except for the Late Jurassic Archaeopteryx (Wang et al., 2018; Zhou and Zhang, 2002). They also possess several advanced, flight-related morphologies, suggesting a unique form of powered flight (O’Connor et al., 2013; Zheng et al., 2020; Zhou and Zhang, 2002). The most abundant jeholornithiform, Jeholornis, has been interpreted as the earliest granivorous bird, based on the reportedly ‘deep’ mandible and traces identified as seeds preserved in the abdominal area (Zhou and Zhang, 2002). Reduced dentition and the presence of a gastric mill further suggest a herbivorous diet (O’Connor et al., 2018). However, there is no consensus on whether seeds entered the gut of Jeholornis, and other early birds, through deliberate and destructive seed consumption (granivory), or through consumption of fleshy propagules such as true angiosperm fruits or gymnosperm arils (herein referred to as ‘fruit consumption’ for convenience, encompassing both consumption of all types of fleshy diaspores, not limited to true fruits) (Ksepka et al., 2019; Mayr et al., 2020; O’Connor, 2019; O’Connor et al., 2018; O’Connor and Zhou, 2020). Indeed, a recent review identified these as ‘seed meals’ without clarification (Miller and Pittman, 2021). Clarifying between these two hypotheses has significant implications with regard to the early evolution of bird–plant interactions, because fruit consumption could result in beneficial co-evolutionary mutualism, whereas seed consumption does not. This therefore is relevant to understanding whether early birds could have been important agents of seed dispersal with a potential mutualistic co-evolutionary influence on plant evolution during the KTR.

Interpretations regarding diet in Jeholornis and other potentially granivorous early birds (Ksepka et al., 2019; Zheng et al., 2018; Zheng et al., 2011) have previously been framed using qualitative observations and subjective assessments, with minimal formal comparison to extant species, and in the absence of a detailed understanding of jeholornithiform cranial anatomy (Lefèvre et al., 2014; O’Connor et al., 2012; O’Connor et al., 2018; Zhou and Zhang, 2003; Zhou and Zhang, 2002). We here report an exquisitely preserved new Jeholornis specimen, STM 3–8, from the Shandong Tianyu Museum of Nature, Pingyi, China. We use high quality three-dimensional (3D) data acquired through the synchrotron tomography to reveal the key cranial features of this taxon and build a precise and almost complete cranial reconstruction of this key stem bird. This information is used to test and determine the two diet hypotheses of Jeholornis, through geometric morphometric (GMM) analyses of the mandible (3D) and cranium (2D), and high-resolution computed tomography (CT) 3D visualisations of the alimentary contents of extant birds. Our approach demonstrates the importance of applying multiple methods simultaneously to solve complex palaeoecological questions.

Digital reconstruction of an exceptionally well-preserved new specimen of the early-diverging bird Jeholornis reveals a plesiomorphic, diapsid skull, sharing numerous features with non-avian theropods. These features include a complete postorbital bar, unreduced squamosal, and unmodified palate (Hu et al., 2020b, Hu et al., 2019; Rauhut et al., 2018), reinforcing evidence for an early-diverging phylogenetic position among birds (Wang et al., 2018; Zhou and Zhang, 2002). Nevertheless, compared to Archaeopteryx (Rauhut, 2014; Rauhut et al., 2018), Jeholornis also possesses clear diet-related specialisations of the rostrum including partial fusion of the premaxillae and a strongly reduced dentition.

Our GMM analyses reveal that the mandibular and cranial shapes of Jeholornis and Sapeornis are distinct from those of seed-cracking granivorous birds, consistent with earlier assumptions that the delicate, vestigial dentary teeth of Jeholornis would be too prone to damage if used to de-husk hard foods (Ksepka et al., 2019; Mayr et al., 2020; O’Connor et al., 2018; O’Connor and Zhou, 2020), and contrary to previous claims that the reportedly ‘deep’ mandible of Jeholornis is suitable for such a behaviour (Zhou and Zhang, 2002). Although their mandibular and cranial shapes occupy the morphospace in which several diets overlap, including frugivory and gastric seed-grinding granivory, these diets can be distinguished through comparing the condition of ingested remains in the alimentary tract in modern birds.

Known stomach contents preserved in Jeholornis take two forms in different fossil specimens, which include: (1) individuals with sparsely distributed and entirely intact seeds (Figure 3A–C; Zhou and Zhang, 2002), and (2) those with a relatively small concentration of gastroliths without any seed remains (Figure 3D; O’Connor et al., 2018). Our comparisons with modern birds indicate that the first group of Jeholornis individuals ingested fleshy propagules (fruit consumption), rather than consuming seeds for nutrient extraction (destructive seed consumption). We cannot interpret the presence of gastroliths in the second group of individuals, because gastroliths are widespread in extant birds with a wide range of diets for example insectivory, granivory, and frugivory (Gionfriddo and Best, 1996; O’Connor, 2019; Piersma et al., 1993; Wings, 2007), making it impossible to infer diet from this evidence alone. Crucially, no Jeholornis specimen preserves seeds and gastroliths together (O’Connor, 2019; O’Connor and Zhou, 2020) (and preserved seeds within Jeholornis are not abraded), which would be required as evidence for seed-grinding granivory.

Variation in alimentary contents among individuals of Jeholornis are best interpreted as evidence of seasonal variation in diet, or potentially other intraspecific variation in diet (O’Connor, 2019; O’Connor et al., 2018). Though the influence of preservational biases cannot be completely excluded yet, the recurring occurrence of specific sets of stomach contents among individuals suggests that these reflect habitual rather than exceptional dietary variation. It is possible that Jeholornis consumed fleshy propagules during the seasons in which such food sources were available, but fed on other food sources during other seasons, which is also consistent with the seasonal climate of the western Liaoning region during the Early Cretaceous (Ding et al., 2006). However, we currently lack strong evidence of what diet items were consumed by Jeholornis in addition to fruits. 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). Seasonal dietary shifts are widely known in modern birds that feed on fruits as a substantive part of their diet such as Ruffed Grouse (Bonasa umbellus) and Hoatzin (Opisthocomus hoazin) (Billerman et al., 2020), since plants usually bear fruits only in certain seasons rather than throughout the year (Corlett, 1998; Howe, 1986; Jordano, 2014; Wilman et al., 2014). Our findings suggest that the dietary flexibility of fruit consumption may be traced back to the earliest stages of bird evolution.

The evidence for fruit consumption in Jeholornis demonstrates that early birds with seeds preserved in the abdominal area cannot be identified as granivores without further evidence from cranial morphology, or the co-occurrence of abraded or fragmented seeds with gastroliths. It was recently suggested that Sapeornis, Eogranivora, and even some enantiornithines may have consumed fruits (Ksepka et al., 2019; Mayr et al., 2020). However, the evidence for this remains equivocal. Sapeornis and Eogranivora preserve apparently whole seeds in the crop, but only gastroliths in the abdominal area (Zheng et al., 2018; Zheng et al., 2011), consistent with both seed-grinding granivory and passerine-like seed-cracking (Figure 4C, D). Therefore, Jeholornis is so far the only Mesozoic bird that provides strong evidence of fruit consumption. However, this should not be taken as evidence that fruit consumption was rare. Direct evidence on diet in fossil birds is rare and preserved gut contents are limited to just a few individuals from a small number of Early Cretaceous fossil deposits in China and Europe (O’Connor, 2019; Miller and Pittman, 2021). Given this low level of current knowledge, evidence for fruit consumption in Jeholornis is important in demonstrating for the first time that at least some early birds ate fruits.

Flight-related anatomical specialisations suggest that Jeholornis was a competent flier in spite of its early-diverging phylogenetic position (Pei et al., 2020; O’Connor et al., 2013; Zheng et al., 2020; Zhou and Zhang, 2002). Although flight is not an exclusive adaptation to fruit consumption, compared to non-volant animals, flight allows birds and bats to more easily obtain patchily distributed but energy-rich food sources in difficult to access and widely dispersed locations, including fruits (Benson et al., 2018b, Benson et al., 2014a; Maurer, 1998), and may in part explain the high prevalence of fruit consumption (and especially the consumption of small fruits such as berries) among extant birds compared to most other tetrapod groups (Tiffney, 2004; Tiffney, 1992).

Although true fruits are only present in angiosperms, seed ferns, and gymnosperms evolved functionally analogous fleshy-coated propagules such as arils and other fleshy accessory tissues much earlier (Tiffney, 1986; Tiffney, 2004; Herrera, 1989; Lovisetto et al., 2012; Contreras et al., 2017; Herendeen et al., 2017). Such structures represent specialisations for animal-mediated seed dispersal. Early fruit-producing angiosperms were present by the Early Cretaceous (Eriksson et al., 2000b), alongside multiple groups of gymnosperms with fleshy propagules including cycadales, ginkgoales, and gnetales (Tiffney, 1986; Tiffney, 2004; Wu, 1999) – which are also present in Jehol Biota (Leng and Friis, 2003; Sun et al., 2001). The alimentary contents preserved in Jeholornis were preliminarily described as ginkgo-like seeds (Zhou and Wu, 2006) and more likely to be gymnospermous due to their relatively large sizes, but have not been confidently identified with detailed comparisons with all the potential Early Cretaceous fruits/arils. In addition, although the poor preservation of these ingested seeds prevents any detailed taxonomic identification, three morphotypes have been grouped in previous studies based on size and shape: morphotype-1 in smaller size with a circular shape and curved striations, morphotype-2 in larger size with an oval shape, and morphotype-3 in similar size to morphotype-1 but with a strongly tapered pole (O’Connor et al., 2018). Therefore, considering that early birds such as those from the Jehol Biota would encounter both gymnosperms and angiosperms, we suggest that during the origin of fruit consumption among birds, early frugivorous birds were likely to be opportunistic and targeted fleshy propagules from both groups, rather than being ‘gymnosperm specialists’.

Given the importance of frugivorous birds today as agents of seed dispersal (Pejchar et al., 2008; Sekercioglu, 2006; Tiffney, 2004), the early occurrence of fruit consumption in birds may signify the origin of an important component of modern-like biotic dispersal systems, providing new opportunities for co-evolutionary mutualisms, though future research is expected to provide solid confirmation for this hypothesis. The occurrence of specialised seed dispersal by animals during the Early Cretaceous has previously been proposed indirectly, based on the presence of aril-producing gymnosperms and early fruit-producing angiosperms (Eriksson, 2008; Eriksson et al., 2000a). However, the identification of these fruit eaters has been uncertain and fruit consumption was almost unmentioned in the recent review of early bird diets, owing to the lack of available evidence (Miller and Pittman, 2021). Evidence for fruit consumption in Jeholornis provides direct evidence of fruit consumption in early birds, long before the origin of the bird crown-group. This provides an important indication of the possibility that birds were recruited by plants for seed dispersal very early in their evolutionary history, during the Early Cretaceous.

Fossil birds have low preservation potential and are known primarily from sites of exceptional preservation. Outside of the Jehol Biota, the fossil record of early birds is poorly sampled, both in space and time. However, evidence from less complete fossil remains suggests that birds had a wide geographic distribution by the Early Cretaceous (Chiappe and Witmer, 2002; Close et al., 2009), suggesting a ‘hidden’ taxonomic, and most likely ecological, diversity of Mesozoic birds. Diversification of birds therefore may explain, at least in part, the evolutionary expansion of fruit abundance, especially angiosperm fruits, that occurred through the Cretaceous (Eriksson, 2008; Eriksson et al., 2000a). Direct evidence for the diet of extinct species is rare. However, evidence in Jeholornis indicates the potential for at least opportunistic fruit consumption among early birds in general. It therefore increases support for the hypothesis that bird–plant interactions are likely to have played at least some role in the Cretaceous Terrestrial Revolution (Tiffney, 2004). Specifically, the occurrence of fruit consumption in one of the earliest-diverging bird lineages raises the possibility of synergistic evolutionary influences, with birds enabling seed dispersal for plants, and obtaining a rich energy resource in return (Muller-Landau and Hardesty, 2005; Dennis, 2007; Jordano, 2014; Carlo and Morales, 2016; Carlo et al., 2022). New discoveries and comparative analyses are required to test this hypothesis, by deeper insights into the ecologies of early bird species, and the potential role of the birds during the transition from gymnosperm- to angiosperm-dominated floras.

The new specimen reported here (Jeholornis STM 3-8) is housed and available for future researchers to check at Shandong Tianyu Museum of Nature, China. The original CT scanning slices and segmented STL files of Jeholornis STM 3-8 and involved modern birds, and the alimentary contents of selected modern birds are available in Morphosource (https://www.morphosource.org/projects/0000C1212; https://www.morphosource.org/projects/00000C420; https://www.morphosource.org/projects/0000C1080). Other data that support this study are available in Figshare (DOI: 10.6084/m9.figshare.13217672), including the rotating videos of the original/reassembled cranial 3D models of Jeholornis STM 3-8 and the 3D models of the alimentary contents of selected modern birds, and the landmark data and taxa lists used in GMM analyses. Further information and requests for resources should be directed to and will be fulfilled by the Lead Contacts, Yan Wang (wangyan6696@lyu.edu.cn) and Han Hu (han.hu@earth.ox.ac.uk).

1. 1. Adams DC
   2. Otárola-Castillo E
   3. Paradis E

   (2013) geomorph: an R package for the collection and analysis of geometric morphometric shape data

   Methods in Ecology and Evolution 4:393–399.

   https://doi.org/10.1111/2041-210X.12035

   • Google Scholar
2. 1. Benson RBJ
   2. Campione NE
   3. Carrano MT
   4. Mannion PD
   5. Sullivan C
   6. Upchurch P
   7. Evans DC

   (2014a) Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage

   PLOS Biology 12:e1001853.

   https://doi.org/10.1371/journal.pbio.1001853

   • PubMed
   • Google Scholar
3. 1. Benson RBJ
   2. Frigot RA
   3. Goswami A
   4. Andres B
   5. Butler RJ

   (2014b) Competition and constraint drove Cope’s rule in the evolution of giant flying reptiles

   Nature Communications 5:3567.

   https://doi.org/10.1038/ncomms4567

   • PubMed
   • Google Scholar
4. 1. Benson RBJ

   (2018a) Dinosaur macroevolution and macroecology

   Annual Review of Ecology, Evolution, and Systematics 49:379–408.

   https://doi.org/10.1146/annurev-ecolsys-110617-062231

   • Google Scholar
5. 1. Benson RBJ
   2. Hunt G
   3. Carrano MT
   4. Campione N
   5. Mannion P

   (2018b) Cope’s rule and the adaptive landscape of dinosaur body size evolution

   Palaeontology 61:13–48.

   https://doi.org/10.1111/pala.12329

   • Google Scholar
6. 1. Benton MJ

   (2010) The origins of modern biodiversity on land

   Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365:3667–3679.

   https://doi.org/10.1098/rstb.2010.0269

   • PubMed
   • Google Scholar
7. Book

   1. Billerman SM
   2. Keeney BK
   3. Rodewald PG
   4. Schulenberg TS

   (2020) Birds of the World

   Ithaca, NY, USA: Cornell Laboratory of Ornithology.

   https://doi.org/10.2173/bow

   • Google Scholar
8. 1. Bjarnason A
   2. Benson R

   (2021) A 3D geometric morphometric dataset quantifying skeletal variation in birds

   MorphoMuseuM 7:e125.

   https://doi.org/10.18563/journal.m3.125

   • Google Scholar
9. 1. Carlo TA
   2. Morales JM

   (2016) Generalist birds promote tropical forest regeneration and increase plant diversity via rare-biased seed dispersal

   Ecology 97:1819–1831.

   https://doi.org/10.1890/15-2147.1

   • PubMed
   • Google Scholar
10. 1. Carlo TA
    2. Cazetta E
    3. Traveset A
    4. Guimarães PR
    5. McConkey KR

    (2022) Special issue: fruits, animals and seed dispersal: timely advances on a key mutualism

    Oikos 2022:e09220.

    https://doi.org/10.1111/oik.09220

    • Google Scholar
11. Book

    1. Chiappe LM
    2. Witmer LM

    (2002)

    Mesozoic Birds: Above the Heads of Dinosaurs

    Berkeley: University of California Press.

    • Google Scholar
12. 1. Clapham ME
    2. Karr JA

    (2012) Environmental and biotic controls on the evolutionary history of insect body size

    PNAS 109:10927–10930.

    https://doi.org/10.1073/pnas.1204026109

    • PubMed
    • Google Scholar
13. 1. Close RA
    2. Vickers-Rich P
    3. Trusler P
    4. Chiappe LM
    5. O’connor J
    6. Rich TH
    7. Kool L
    8. Komarower P

    (2009) Earliest Gondwanan bird from the Cretaceous of southeastern Australia

    Journal of Vertebrate Paleontology 29:616–619.

    https://doi.org/10.1671/039.029.0214

    • Google Scholar
14. 1. Contreras DL
    2. Duijnstee IAP
    3. Ranks S
    4. Marshall CR
    5. Looy CV

    (2017) Evolution of dispersal strategies in conifers: Functional divergence and convergence in the morphology of diaspores

    Perspectives in Plant Ecology, Evolution and Systematics 24:93–117.

    https://doi.org/10.1016/j.ppees.2016.11.002

    • Google Scholar
15. 1. Corlett RT

    (1998) Frugivory and seed dispersal by vertebrates in the Oriental (Indomalayan) Region

    Biological Reviews of the Cambridge Philosophical Society 73:413–448.

    https://doi.org/10.1017/s0006323198005234

    • PubMed
    • Google Scholar
16. Book

    1. Dennis AJ

    (editors) (2007) Seed Dispersal: Theory and Its Application in a Changing World

    Wallingford, UK: CABI.

    https://doi.org/10.1079/9781845931650.0000

    • Google Scholar
17. 1. Ding Q
    2. Tian N
    3. Wang Y
    4. Jiang Z
    5. Chen S
    6. Wang D
    7. Zhang W
    8. Zheng S
    9. Xie A
    10. Zhang G
    11. Liu Z

    (2006) Fossil coniferous wood from the Early Cretaceous Jehol Biota in western Liaoning, NE China: New material and palaeoclimate implication

    Cretaceous Res 61:57–70.

    https://doi.org/10.1016/j.cretres.2015.12.011

    • Google Scholar
18. 1. Elzanowski A
    2. Wellnhofer P

    (1996) Cranial morphology of Archaeopteryx : evidence from the seventh skeleton

    Journal of Vertebrate Paleontology 16:81–94.

    https://doi.org/10.1080/02724634.1996.10011286

    • Google Scholar
19. 1. Eriksson O
    2. Friis EM
    3. Löfgren P

    (2000a) Seed size, fruit size, and dispersal systems in Angiosperms from the Early Cretaceous to the Late Tertiary

    The American Naturalist 156:47–58.

    https://doi.org/10.1086/303367

    • PubMed
    • Google Scholar
20. 1. Eriksson O
    2. Friis EM
    3. Pedersen KR
    4. Crane PR

    (2000b) Seed size and dispersal systems of Early Cretaceous angiosperms from Famalicão, Portugal

    International Journal of Plant Sciences 161:319–329.

    https://doi.org/10.1086/314248

    • PubMed
    • Google Scholar
21. 1. Eriksson O

    (2008) Evolution of seed size and biotic seed dispersal in angiosperms: paleoecological and neoecological evidence

    International Journal of Plant Sciences 169:863–870.

    https://doi.org/10.1086/589888

    • Google Scholar
22. 1. Field DJ
    2. Hanson M
    3. Burnham D
    4. Wilson LE
    5. Super K
    6. Ehret D
    7. Ebersole JA
    8. Bhullar BAS

    (2018) Complete Ichthyornis skull illuminates mosaic assembly of the avian head

    Nature 557:96–100.

    https://doi.org/10.1038/s41586-018-0053-y

    • PubMed
    • Google Scholar
23. 1. Gionfriddo JP
    2. Best LB

    (1996)

    Grit-use patterns in North American birds: the influence of diet, body size, and gender

    The Wilson Bulletin 108:685–696.

    • Google Scholar
24. 1. Goodall C

    (1991) Procrustes methods in the statistical analysis of shape

    Journal of the Royal Statistical Society 53:285–321.

    https://doi.org/10.1111/j.2517-6161.1991.tb01825.x

    • Google Scholar
25. Conference

    1. Gureyev TE
    2. Sanchez del Rio M
    3. Chubar O
    4. Nesterets Y
    5. Ternovski D
    6. Thompson D
    7. Wilkins SW
    8. Stevenson AW
    9. Sakellariou A
    10. Taylor JA

    (2011) Toolbox for advanced x-ray image processing

    SPIE Optical Engineering + Applications.

    https://doi.org/10.1117/12.893252

    • Google Scholar
26. 1. He HY
    2. Wang XL
    3. Zhou ZH
    4. Wang F
    5. Boven A
    6. Shi GH
    7. Zhu RX

    (2004) Timing of the Jiufotang Formation (Jehol Group) in Liaoning, northeastern China, and its implications

    Geophysical Research Letters 31:e019790.

    https://doi.org/10.1029/2004GL019790

    • Google Scholar
27. 1. Herendeen PS
    2. Friis EM
    3. Pedersen KR
    4. Crane PR

    (2017) Palaeobotanical redux: Revisiting the age of the angiosperms

    Nature Plants 3:e17015.

    https://doi.org/10.1038/nplants.2017.15

    • PubMed
    • Google Scholar
28. 1. Herrera CM

    (1989) Seed dispersal by animals: A role in angiosperm diversification?

    The American Naturalist 133:309–322.

    https://doi.org/10.1086/284921

    • Google Scholar
29. Book

    1. Howe HF

    (1986)

    Seed dispersal by fruit-eating birds and mammals

    In: Murray DR, editors. Seed Dispersal. Sydney, Australia: Academic Press. pp. 123–189.

    • Google Scholar
30. 1. Hu H
    2. Sansalone G
    3. Wroe S
    4. McDonald PG
    5. O’Connor JK
    6. Li Z
    7. Xu X
    8. Zhou Z

    (2019) Evolution of the vomer and its implications for cranial kinesis in Paraves

    PNAS 116:19571–19578.

    https://doi.org/10.1073/pnas.1907754116

    • PubMed
    • Google Scholar
31. 1. Hu H
    2. O’Connor JK
    3. McDonald PG
    4. Wroe S

    (2020a) Cranial osteology of the Early Cretaceous Sapeornis chaoyangensis (Aves: Pygostylia)

    Cretaceous Research 113:104496.

    https://doi.org/10.1016/j.cretres.2020.104496

    • Google Scholar
32. 1. Hu H
    2. O’Connor JK
    3. Wang M
    4. Wroe S
    5. McDonald PG

    (2020b) New anatomical information on the bohaiornithid Longusunguis and the presence of a plesiomorphic diapsid skull in Enantiornithes

    Journal of Systematic Palaeontology 18:1481–1495.

    https://doi.org/10.1080/14772019.2020.1748133

    • Google Scholar
33. Book

    1. Jordano P

    (2014)

    Fruits and Frugivory In

    In: Gallagher RS, editors. Seeds: The Ecology of Regeneration of Plant Communities (3rd edn). Wallingford: CABI. pp. 18–61.

    • Google Scholar
34. 1. Ksepka DT
    2. Grande L
    3. Mayr G

    (2019) Oldest finch-beaked birds reveal parallel ecological radiations in the earliest evolution of Passerines

    Current Biology 29:657–663.

    https://doi.org/10.1016/j.cub.2018.12.040

    • PubMed
    • Google Scholar
35. 1. Lefèvre U
    2. Hu D
    3. Escuillié F
    4. Dyke G
    5. Godefroit P

    (2014) A new long-tailed basal bird from the Lower Cretaceous of north-eastern China

    Biological Journal of the Linnean Society 113:790–804.

    https://doi.org/10.1111/bij.12343

    • Google Scholar
36. 1. Leng Q
    2. Friis EM

    (2003) Sinocarpus decussatus gen et sp nov, a new angiosperm with basally syncarpous fruits from the Yixian Formation of Northeast China

    Plant Systematics and Evolution 241:77–88.

    https://doi.org/10.1007/s00606-003-0028-8

    • Google Scholar
37. 1. Lloyd GT
    2. Davis KE
    3. Pisani D
    4. Tarver JE
    5. Ruta M
    6. Sakamoto M
    7. Hone DWE
    8. Jennings R
    9. Benton MJ

    (2008) Dinosaurs and the Cretaceous Terrestrial Revolution

    Proceedings. Biological Sciences 275:2483–2490.

    https://doi.org/10.1098/rspb.2008.0715

    • PubMed
    • Google Scholar
38. 1. Lovisetto A
    2. Guzzo F
    3. Tadiello A
    4. Toffali K
    5. Favretto A
    6. Casadoro G

    (2012) Molecular analyses of MADS-box genes trace back to Gymnosperms the invention of fleshy fruits

    Molecular Biology and Evolution 29:409–419.

    https://doi.org/10.1093/molbev/msr244

    • PubMed
    • Google Scholar
39. 1. Maurer B a

    (1998) The evolution of body size in birds. II. The role of reproductive power

    Evolutionary Ecology 12:935–944.

    https://doi.org/10.1023/A:1006564105504

    • Google Scholar
40. 1. Mayr G
    2. Pohl B
    3. Hartman S
    4. Peters DS

    (2007) The tenth skeletal specimen of Archaeopteryx

    Zoological Journal of the Linnean Society 149:97–116.

    https://doi.org/10.1111/j.1096-3642.2006.00245.x

    • Google Scholar
41. 1. Mayr G
    2. Kaye TG
    3. Pittman M
    4. Saitta ET
    5. Pott C

    (2020) Reanalysis of putative ovarian follicles suggests that Early Cretaceous birds were feeding not breeding

    Scientific Reports 10:19035.

    https://doi.org/10.1038/s41598-020-76078-2

    • PubMed
    • Google Scholar
42. 1. Miller CV
    2. Pittman M

    (2021) The diet of early birds based on modern and fossil evidence and a new framework for its reconstruction

    Biological Reviews of the Cambridge Philosophical Society 96:2058–2112.

    https://doi.org/10.1111/brv.12743

    • PubMed
    • Google Scholar
43. Book

    1. Muller-Landau HC
    2. Hardesty BD

    (2005) Seed dispersal of woody plants in tropical forests: concepts, examples, and future directions

    In: Burslem D, Pinard M, Hartley S, editors. Biotic Interactions in the Tropics: Their Role in the Maintenance of Species Diversity. Cambridge: Cambridge University Press. pp. 267–309.

    https://doi.org/10.1017/CBO9780511541971.012

    • Google Scholar
44. 1. Navalón G
    2. Bright JA
    3. Marugán-Lobón J
    4. Rayfield EJ

    (2019) The evolutionary relationship among beak shape, mechanical advantage, and feeding ecology in modern birds

    Evolution; International Journal of Organic Evolution 73:422–435.

    https://doi.org/10.1111/evo.13655

    • PubMed
    • Google Scholar
45. 1. O’Connor JK
    2. Chiappe LM

    (2011) A revision of enantiornithine (Aves: Ornithothoraces) skull morphology

    Journal of Systematic Palaeontology 9:135–157.

    https://doi.org/10.1080/14772019.2010.526639

    • Google Scholar
46. 1. O’Connor JK
    2. Sun C
    3. Xu X
    4. Wang X
    5. Zhou Z

    (2012) A new species of Jeholornis with complete caudal integument

    Historical Biology 24:29–41.

    https://doi.org/10.1080/08912963.2011.552720

    • Google Scholar
47. 1. O’Connor J
    2. Wang X
    3. Sullivan C
    4. Zheng X
    5. Tubaro P
    6. Zhang X
    7. Zhou Z

    (2013) Unique caudal plumage of Jeholornis and complex tail evolution in early birds

    PNAS 110:17404–17408.

    https://doi.org/10.1073/pnas.1316979110

    • PubMed
    • Google Scholar
48. 1. O’Connor J
    2. Wang X
    3. Sullivan C
    4. Wang Y
    5. Zheng X
    6. Hu H
    7. Zhang X
    8. Zhou Z

    (2018) First report of gastroliths in the Early Cretaceous basal bird Jeholornis

    Cretaceous Research 84:200–208.

    https://doi.org/10.1016/j.cretres.2017.10.031

    • Google Scholar
49. 1. O’Connor JK

    (2019) The trophic habits of early birds

    Palaeogeography, Palaeoclimatology, Palaeoecology 513:178–195.

    https://doi.org/10.1016/j.palaeo.2018.03.006

    • Google Scholar
50. 1. O’Connor JK
    2. Zhou Z

    (2020) The evolution of the modern avian digestive system: insights from paravian fossils from the Yanliao and Jehol biotas

    Palaeontology 63:13–27.

    https://doi.org/10.1111/pala.12453

    • Google Scholar
51. 1. Pei R
    2. Pittman M
    3. Goloboff PA
    4. Dececchi TA
    5. Habib MB
    6. Kaye TG
    7. Larsson HCE
    8. Norell MA
    9. Brusatte SL
    10. Xu X

    (2020) Potential for powered flight neared by most close avialan relatives, but few crossed its thresholds

    Current Biology 30:4033–4046.

    https://doi.org/10.1016/j.cub.2020.06.105

    • PubMed
    • Google Scholar
52. 1. Pejchar L
    2. Pringle RM
    3. Ranganathan J
    4. Zook JR
    5. Duran G
    6. Oviedo F
    7. Daily GC

    (2008) Birds as agents of seed dispersal in a human-dominated landscape in southern Costa Rica

    Biological Conservation 141:536–544.

    https://doi.org/10.1016/j.biocon.2007.11.008

    • Google Scholar
53. 1. Piersma T
    2. Koolhaas A
    3. Dekinga A

    (1993) Interactions between stomach structure and diet choice in shorebirds

    The Auk 110:552–564.

    https://doi.org/10.2307/4088419

    • Google Scholar
54. 1. Prum RO
    2. Berv JS
    3. Dornburg A
    4. Field DJ
    5. Townsend JP
    6. Lemmon EM
    7. Lemmon AR

    (2015) A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing

    Nature 526:569–573.

    https://doi.org/10.1038/nature15697

    • PubMed
    • Google Scholar
55. 1. Rauhut OWM

    (2014) New observations on the skull of Archaeopteryx

    Paläontologische Zeitschrift 88:211–221.

    https://doi.org/10.1007/s12542-013-0186-0

    • Google Scholar
56. 1. Rauhut OWM
    2. Foth C
    3. Tischlinger H

    (2018) The oldest Archaeopteryx (Theropoda: Avialiae): a new specimen from the Kimmeridgian/Tithonian boundary of Schamhaupten, Bavaria

    PeerJ 6:e4191.

    https://doi.org/10.7717/peerj.4191

    • PubMed
    • Google Scholar
57. 1. Rohlf FJ
    2. Slice D

    (1990) Extensions of the procrustes method for the optimal superimposition of landmarks

    Systematic Zoology 39:40.

    https://doi.org/10.2307/2992207

    • Google Scholar
58. 1. Sekercioglu CH

    (2006) Increasing awareness of avian ecological function

    Trends Ecol Evol 21:464–471.

    https://doi.org/10.1016/j.tree.2006.05.007

    • Google Scholar
59. 1. Soons J
    2. Herrel A
    3. Genbrugge A
    4. Aerts P
    5. Podos J
    6. Adriaens D
    7. de Witte Y
    8. Jacobs P
    9. Dirckx J

    (2010) Mechanical stress, fracture risk and beak evolution in Darwin’s ground finches (Geospiza)

    Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365:1093–1098.

    https://doi.org/10.1098/rstb.2009.0280

    • PubMed
    • Google Scholar
60. 1. Soons J
    2. Genbrugge A
    3. Podos J
    4. Adriaens D
    5. Aerts P
    6. Dirckx J
    7. Herrel A

    (2015) Is beak morphology in Darwin’s finches tuned to loading demands?

    PLOS ONE 10:e0129479.

    https://doi.org/10.1371/journal.pone.0129479

    • PubMed
    • Google Scholar
61. Book

    1. Sun G
    2. Zheng S
    3. Dilcher D
    4. Wang Y
    5. Mei S

    (2001)

    Early Angiosperms and Their Associated Plants from Western Liaoning

    China. Shanghai: Science and Technology Education Publishing House.

    • Google Scholar
62. Book

    1. Tiffney BH

    (1986) Evolution of seed dispersal syndromes according to the fossil record in

    In: Murray DR, editors. Sydney. Academic Press. pp. 273–305.

    https://doi.org/10.2307/2399037

    • Google Scholar
63. 1. Tiffney BH

    (1992)

    The role of vertebrate herbivory in the evolution of land plants

    Palaeobotanist 41:87–97.

    • Google Scholar
64. 1. Tiffney BH

    (2004) Vertebrate dispersal of seed plants through time

    Annual Review of Ecology, Evolution, and Systematics 35:1–29.

    https://doi.org/10.1146/annurev.ecolsys.34.011802.132535

    • Google Scholar
65. 1. Tobias JA
    2. Sheard C
    3. Pigot AL
    4. Devenish AJM
    5. Yang J
    6. Sayol F
    7. Neate-Clegg MHC
    8. Alioravainen N
    9. Weeks TL
    10. Barber RA
    11. Walkden PA
    12. MacGregor HEA
    13. Jones SEI
    14. Vincent C
    15. Phillips AG
    16. Marples NM
    17. Montaño-Centellas FA
    18. Leandro-Silva V
    19. Claramunt S
    20. Darski B
    21. Freeman BG
    22. Bregman TP
    23. Cooney CR
    24. Hughes EC
    25. Capp EJR
    26. Varley ZK
    27. Friedman NR
    28. Korntheuer H
    29. Corrales-Vargas A
    30. Trisos CH
    31. Weeks BC
    32. Hanz DM
    33. Töpfer T
    34. Bravo GA
    35. Remeš V
    36. Nowak L
    37. Carneiro LS
    38. Moncada R AJ
    39. Matysioková B
    40. Baldassarre DT
    41. Martínez-Salinas A
    42. Wolfe JD
    43. Chapman PM
    44. Daly BG
    45. Sorensen MC
    46. Neu A
    47. Ford MA
    48. Mayhew RJ
    49. Fabio Silveira L
    50. Kelly DJ
    51. Annorbah NND
    52. Pollock HS
    53. Grabowska-Zhang AM
    54. McEntee JP
    55. Carlos T Gonzalez J
    56. Meneses CG
    57. Muñoz MC
    58. Powell LL
    59. Jamie GA
    60. Matthews TJ
    61. Johnson O
    62. Brito GRR
    63. Zyskowski K
    64. Crates R
    65. Harvey MG
    66. Jurado Zevallos M
    67. Hosner PA
    68. Bradfer-Lawrence T
    69. Maley JM
    70. Stiles FG
    71. Lima HS
    72. Provost KL
    73. Chibesa M
    74. Mashao M
    75. Howard JT
    76. Mlamba E
    77. Chua MAH
    78. Li B
    79. Gómez MI
    80. García NC
    81. Päckert M
    82. Fuchs J
    83. Ali JR
    84. Derryberry EP
    85. Carlson ML
    86. Urriza RC
    87. Brzeski KE
    88. Prawiradilaga DM
    89. Rayner MJ
    90. Miller ET
    91. Bowie RCK
    92. Lafontaine R-M
    93. Scofield RP
    94. Lou Y
    95. Somarathna L
    96. Lepage D
    97. Illif M
    98. Neuschulz EL
    99. Templin M
    100. Dehling DM
    101. Cooper JC
    102. Pauwels OSG
    103. Analuddin K
    104. Fjeldså J
    105. Seddon N
    106. Sweet PR
    107. DeClerck FAJ
    108. Naka LN
    109. Brawn JD
    110. Aleixo A
    111. Böhning-Gaese K
    112. Rahbek C
    113. Fritz SA
    114. Thomas GH
    115. Schleuning M

    (2022) AVONET: Morphological, ecological and geographical data for all birds

    Ecology Letters 25:581–597.

    https://doi.org/10.1111/ele.13898

    • PubMed
    • Google Scholar
66. 1. van der Meij MAA
    2. Bout RG

    (2008) The relationship between shape of the skull and bite force in finches

    The Journal of Experimental Biology 211:1668–1680.

    https://doi.org/10.1242/jeb.015289

    • PubMed
    • Google Scholar
67. 1. Wang Y
    2. Wang M
    3. O’Connor JK
    4. Wang X
    5. Zheng X
    6. Zhang X

    (2016) A new Jehol enantiornithine bird with three-dimensional preservation and ovarian follicles

    Journal of Vertebrate Paleontology 36:e1054496.

    https://doi.org/10.1080/02724634.2015.1054496

    • Google Scholar
68. 1. Wang M
    2. Hu H

    (2017) A comparative morphological study of the jugal and quadratojugal in early birds and their dinosaurian relatives

    Anatomical Record 300:62–75.

    https://doi.org/10.1002/ar.23446

    • PubMed
    • Google Scholar
69. 1. Wang M
    2. Stidham TA
    3. Zhou Z

    (2018) A new clade of basal Early Cretaceous pygostylian birds and developmental plasticity of the avian shoulder girdle

    PNAS 115:10708–10713.

    https://doi.org/10.1073/pnas.1812176115

    • PubMed
    • Google Scholar
70. 1. Wang M
    2. Zhou Z

    (2019) A new enantiornithine (Aves: Ornithothoraces) with completely fused premaxillae from the Early Cretaceous of China

    Journal of Systematic Palaeontology 17:1299–1312.

    https://doi.org/10.1080/14772019.2018.1527403

    • Google Scholar
71. 1. Wang X
    2. Huang J
    3. Kundrát M
    4. Cau A
    5. Liu X
    6. Wang Y
    7. Ju S

    (2020) A new jeholornithiform exhibits the earliest appearance of the fused sternum and pelvis in the evolution of avialan dinosaurs

    Journal of Asian Earth Sciences 199:e104401.

    https://doi.org/10.1016/j.jseaes.2020.104401

    • Google Scholar
72. 1. Wilman H
    2. Belmaker J
    3. Simpson J
    4. de la Rosa C
    5. Rivadeneira MM
    6. Jetz W

    (2014) Eltontraits 1.0: Species-level foraging attributes of the world’s birds and mammals

    Ecology 95:e2027.

    https://doi.org/10.1890/13-1917.1

    • Google Scholar
73. 1. Wings O

    (2007)

    A review of gastrolith function with implications for fossil vertebrates and a revised classification

    Acta Palaeontologica Polonica 52:1–16.

    • Google Scholar
74. 1. Wu S

    (1999)

    A preliminary study of the jehol flora from western liaoning

    Palaeoworld 11:7–57.

    • Google Scholar
75. 1. Xu X
    2. Wu XC

    (2001) Cranial morphology of Sinornithosaurus millenii Xu et al. 1999 (dinosauria: Theropoda: Dromaeosauridae) from the Yixian Formation of Liaoning, China

    Canadian Journal of Earth Sciences 38:1739–1752.

    https://doi.org/10.1139/e01-082

    • Google Scholar
76. 1. Xu X
    2. Norell MA
    3. Kuang X
    4. Wang X
    5. Zhao Q
    6. Jia C

    (2004) Basal tyrannosauroids from China and evidence for protofeathers in tyrannosauroids

    Nature 431:680–684.

    https://doi.org/10.1038/nature02855

    • PubMed
    • Google Scholar
77. 1. Xu X
    2. Pittman M
    3. Sullivan C
    4. Choiniere JN
    5. Tan Q
    6. Clark JM
    7. Norell MA
    8. Wang S

    (2015)

    The taxonomic status of the Late Cretaceous dromaeosaurid Linheraptor exquisitus and its implications for dromaeosaurid systematics

    Vertebrata PalAsiatica 53:29–62.

    • Google Scholar
78. 1. Yang S
    2. He H
    3. Jin F
    4. Zhang F
    5. Wu Y
    6. Yu Z
    7. Li Q
    8. Wang M
    9. O’Connor JK
    10. Deng C
    11. Zhu R
    12. Zhou Z

    (2020) The appearance and duration of the Jehol Biota: Constraint from SIMS U-Pb zircon dating for the Huajiying Formation in northern China

    PNAS 117:14299–14305.

    https://doi.org/10.1073/pnas.1918272117

    • PubMed
    • Google Scholar
79. 1. Yu Y
    2. Zhang C
    3. Xu X

    (2021) Deep time diversity and the early radiations of birds

    PNAS 118:e2019865118.

    https://doi.org/10.1073/pnas.2019865118

    • PubMed
    • Google Scholar
80. 1. Zheng X
    2. Martin LD
    3. Zhou Z
    4. Burnham DA
    5. Zhang F
    6. Miao D

    (2011) Fossil evidence of avian crops from the Early Cretaceous of China

    PNAS 108:15904–15907.

    https://doi.org/10.1073/pnas.1112694108

    • PubMed
    • Google Scholar
81. 1. Zheng X
    2. O’Connor JK
    3. Wang X
    4. Wang Y
    5. Zhou Z

    (2018) Reinterpretation of a previously described Jehol bird clarifies early trophic evolution in the Ornithuromorpha

    Proceedings. Biological Sciences 285:20172494.

    https://doi.org/10.1098/rspb.2017.2494

    • PubMed
    • Google Scholar
82. 1. Zheng X
    2. Sullivan C
    3. O’Connor JK
    4. Wang X
    5. Wang Y
    6. Zhang X
    7. Zhou Z

    (2020) Structure and possible ventilatory function of unusual, expanded sternal ribs in the Early Cretaceous bird Jeholornis

    Cretaceous Research 116:104597.

    https://doi.org/10.1016/j.cretres.2020.104597

    • Google Scholar
83. 1. Zhou Z
    2. Zhang F

    (2002) A long-tailed, seed-eating bird from the Early Cretaceous of China

    Nature 418:405–409.

    https://doi.org/10.1038/nature00930

    • PubMed
    • Google Scholar
84. 1. Zhou Z
    2. Zhang F

    (2003) Jeholornis compared to Archaeopteryx, with a new understanding of the earliest avian evolution

    Die Naturwissenschaften 90:220–225.

    https://doi.org/10.1007/s00114-003-0416-5

    • PubMed
    • Google Scholar
85. 1. Zhou Z
    2. Wu X

    (2006) The rise of ginkgoalean plants in the early Mesozoic: a data analysis

    Geological Journal 41:363–375.

    https://doi.org/10.1002/gj.1049

    • Google Scholar

Decision letter after peer review:

Thank you for submitting your article "Earliest evidence for frugivory and seed dispersal by birds" for consideration by eLife. Your article has been reviewed by three peer reviewers, and the evaluation has been overseen by a Reviewing Editor and Christian Rutz as the Senior Editor. The following individuals involved in the review of your submission have agreed to reveal their identity: Nathan Jud (Reviewer #2); Chris Torres (Reviewer #3).

The reviewers have discussed their reviews with one another, and the Senior Editor has drafted this decision letter to help you prepare a revised submission.

Essential revisions:

The reviewers agreed that this is an exceptional specimen, but have raised reservations about the analyses and inferences presented. In light of their feedback, we would like to request the following essential revisions:

1. Please critically evaluate the alternative hypothesis that Jeholornis is neither frugivorous nor granivorous and that the observed gut contents instead represent facultative frugivory. In our view, addressing this point requires additional analyses, rather than just text revision.

2. The (co-)evolutionary implications of this discovery remain unclear as presented, and need to be explored further. The seeds are perhaps more likely gymnospermous than angiospermous. There are multiple origins of fleshy accessory tissues in gymnosperms, suggesting that plants were recruiting vertebrate seed dispersers repeatedly, and although crown birds may not be ancestrally frugivorous, the multiple origins of frugivory in crown birds suggests dietary lability. The abundance of animal-dispersed plants, and the frequency with which frugivory evolved in crown birds means that the appearance of facultative, opportunistic, or seasonal frugivory in stem birds is perhaps not particularly surprising.

3. What is the evidence that seed dispersal by frugivorous birds enhances diversification rates through increased speciation rates or decreased extinction rates in either plants or birds? Please cite relevant studies that evaluated this hypothesis.

4. The treatment of the plant material seems weak, as the seeds are not described and the brief mention of gymnospermous accessory tissues masks complex plant-animal interactions related to seed dispersal among non-angiosperms. Please improve documentation and analyses.

5. Please address the points raised in the reviewers' full reports, which are appended below.

6. Given the concerns raised, there was a feeling that claims were worded too strongly, and that language should be toned down throughout.

Please note that, in light of the fact that the study's key claim currently seems insufficiently supported, we will send your revised manuscript out for re-evaluation and that eventual acceptance is not guaranteed.

Reviewer #1 (Recommendations for the authors):

Our main comment is related to experimental design as the possibility that Jeholornis was not a specialist granivore or frugivore was not evaluated to the same extent as granivory and frugivory in your study. This third hypothesis would be important to address using multiple methods simultaneously. This is supported by the PCA data where there is overlap between the granivory and frugivory data points and the 'other diet' data points.

The idea of a bird-plant link in the Early Cretaceous is interesting and could be spelled out more, along with further consideration of the uncertainties revealed in key studies e.g., Hulme 2002.

Hulme, P.E., 2002. Seed-eaters: Seed Dispersal, Destruction and Demography. Seed dispersal and frugivory: Ecology, evolution, and conservation, p.257.

However, this is secondary to our main comment above which is related to experimental design and the data incompletely supporting the conclusions proposed.

We suggest two options to consider [### Note from the Senior Editor: our clear preference is Option 2 ###]:

1) Narrow the scope of the conclusions to those which can be well supported by the data available i.e., a study showing that, for the seed components of the diet of Jeholornis, whether granivory or frugivory is most supported.

2) Alternatively, we suggest to undertake a more holistic diet analysis based on multiple lines of evidence that tests hypothesis 3 and then using the results to inform the conclusions (which may or may not be related to granivory or frugivory).

We hope you find the comments provided helpful.

Reviewer #2 (Recommendations for the authors):

As far as I can tell, the descriptions and comparisons of skull morphology are detailed and well done. The argument that Jeholornis was not a seed cracker is strong, and the interpretation of Jeholornis as at least seasonally frugivorous is well-reasoned. It does nicely show that volant birds were recruited for endozoochory early. It will be a pleasure to see this published. Nonetheless, I do have some minor questions and concerns/recommendations about the botany and co-evolutionary implications that I think would make the manuscript stronger, along with some minor suggestions regarding the writing clarity that can be adopted at the authors' discretion.

Line 60. Using plesiomorphic as an adverb strikes me as odd. It seems to me the meaning the sentence is unchanged if the word plesiomorphically is omitted and instead it reads "retaining an elongate bony tail"

Line 64. In what way is Jeholornis the most representative jeholornithiform? Are other jeholornithiforms somehow less representative?

Line 75. Consider substituting or adding "seed predation" alongside granivory. This widely used term emphasizes the ecological difference between feeding on seeds vs. other forms of herbivory as it kills a "whole plant."

Line 77. Consider changing to "mutualistic co-evolutionary influence," or perhaps "co-diversification" is what you mean; however, see my comment about lines 342-343 below.

Like 86. "Complete" or "precise" might be a better word choice than "accurate." Are previous reconstructions inaccurate? Perhaps they are just incomplete or poorly resolved, but not inaccurate.

Line 95. Because of its phylogenetic position… Because modifies a verb, in this case "studied" "Due to" means "caused by". Or, to put it another way, Jeholornis has been frequently studied because of its phylogenetic position.

Line 130. I suggest "indicates that rostral fusion evolved earlier (or deeper in bird phylogeny) than previously thought." I also suggest that the authors point out what other characters it now precedes to emphasize the point that paleontology reveals the order of character changes along branches.

Line 225: I don't think the parentheses are necessary.

Lines 260-263. I encourage the authors to describe the seeds, or at least to summarize the morphological diversity, number of types, (and perhaps their organization) if they were all previously described in O'Connor et al. (2018). What are their morphology, dimensions, and size variation? Do all of them have longitudinal striations? Based on the figures, these seeds appear to be quite large for Cretaceous angiosperms (Tiffney 1984; Eriksson et al. 2000; 2008). Is it more likely that these are seeds of a gymnospermous plant? I suspect so.

Lines 274-277. The hypothesis about seasonal frugivory in Jeholornis is both reasonable and interesting. Some indication of warm climate with seasonality of precipitation is supported elsewhere in the Jehol biota by Ding et al.'s (2016) analysis of fossil woods. It may be worth citing that work.

Lines 305-315. Extant gymnosperms that use endozoochory for seed dispersal use a variety of accessory tissues, not just arils. Ginkgo, cycads, and some extinct groups have a fleshy sarcotesta (outer seed coat). An aril is a fleshy appendage of the seed coat or the funiculus. Some gymnosperms have fleshy subtending bracts (Ephedra), and some have fleshy accessory tissues such as bracts (Ephedra), cones (Juniperus), receptacle and epimatium (Podocarpaceae), or fleshy cones with numerous seeds (Juniperus). See Tiffney (1986, 2004); Herrera (1989); Lovisetto et al. (2012); Contreras et al. (2017); Nigris et al. (2021). I suggest Herrera (1989) as an earlier citation than Herendeen et al. (2017) for line 306.

Line 318. Why small? What does small mean? Small enough to fit in their mouth?

Line 321. I suggest "early and repeated" instead of "ancient". It appears to be clear that there are multiple origins of frugivory/omnivory within crown group birds, and it is not clear that the MRCA of crown-group birds was frugivorus (Felice et al. 2019). This lability in bird diet and repeated origin of frugivory might actually better support the authors' argument that diffuse coevolution between angiosperms and frugivorous birds contributed the KTR. There is now good evidence that volant birds have been repeatedly recruited by plants as endozoochorous seed dispeserers, even prior to the evolution of the MRCA of extant birds.

Line 342-343. Can you provide a citation linking dispersal mode to diversification rate? Eriksson and Bremer (1992) in the journal 'Evolution' found no relationship between dispersal mode and diversification rate in angiosperms, although Carlo and Morales (2015) in the journal 'Ecology' showed evidence that frugivorous birds increase plant α diversity.

Essential revisions:

The reviewers agreed that this is an exceptional specimen, but have raised reservations about the analyses and inferences presented. In light of their feedback, we would like to request the following essential revisions:

1. Please critically evaluate the alternative hypothesis that Jeholornis is neither frugivorous nor granivorous and that the observed gut contents instead represent facultative frugivory. In our view, addressing this point requires additional analyses, rather than just text revision.

Additional analyses and dissection of the morphometric results have been added, and details of them are provided in the following reply to Reviewer 1. These additional analyses delimit among a larger number of dietary categories than our original analyses, which we believe is what Referee 1 required.

Note that our original manuscript did claim facultative frugivory, and we had consistently used the terms ‘seasonal frugivory’ or ‘partial frugivory’ in our initial submission. Also that we suggested explicitly that Jeholornis may have taken other diet items including e.g. insectivory. Nevertheless, we have attempted to clarify this further in the revised manuscript (also see below in the reply to Reviewer 1). In particular, we now refer more often to ‘fruit consumption’, describing the behaviour of taking fruit instead of a dietary class. Note that this is not so different to many extant birds, which show different levels of frugivory, mainly taking fruit (including many temperate birds taking berries) or only as a proportion of the diet rather than their strict diet class.

2. The (co-)evolutionary implications of this discovery remain unclear as presented, and need to be explored further. The seeds are perhaps more likely gymnospermous than angiospermous. There are multiple origins of fleshy accessory tissues in gymnosperms, suggesting that plants were recruiting vertebrate seed dispersers repeatedly, and although crown birds may not be ancestrally frugivorous, the multiple origins of frugivory in crown birds suggests dietary lability. The abundance of animal-dispersed plants, and the frequency with which frugivory evolved in crown birds means that the appearance of facultative, opportunistic, or seasonal frugivory in stem birds is perhaps not particularly surprising.

We think this point may be separated to three parts:

1) By providing direct evidence of fruit-consumption in early stem birds, we provided the mechanism for the bird-plant co-evolutionary mutualism. Our study provides the first direct clear evidence of habitual fruit-consumption in an early-diverging bird outside the crown group, and this is the importance of our findings. Direct evidence of co-evolution itself is almost impossible to preserve in fossils. Therefore, even in our initial submission, we opted to tone down the relevant statements rather than making them too strong and specific. We generally restricted our discussions to the first step to this topic – the existence of the mechanism not the actual, direct evidence of this mutualism.

We think that the evidence of fruit-consumption in stem birds that we provided here is important. The referee summary suggests that this might be thought to be likely, even in absence of evidence. But that is a hypothesis and is contingent on various factors, in particular that crown-group birds are a good model for stem birds, in spite of various anatomical and functional differences. Our data provides a test of this hypothesis, which is important beyond the supposition of what might have been likely or unlikely in absence of evidence. It is worth noting that fruit, and other animal-dispersed reproductive structures (e.g. the fleshy diaspores of gymnosperms) were probably not as abundant in the Early Cretaceous as they are today (e.g. see works by Ericksson on fruit evolution). Therefore, the world was not the same back then as it is today, and it is not strictly correct to say that the high frequency of fruit-consumption by birds today makes the occurrence of fruit-consumption in the Early Cretaceous unsurprising. In fact, the importance and frequency of this interaction today is precisely what makes it so important to find direct evidence on the question of whether it happened at all in the Early Cretaceous.

2) This point is also mentioned in the “Line 321” comment from Reviewer 2. The lability in bird diet and multiple origins of frugivory in crown birds actually supports our argument that although we cannot decide the gymnosperm or angiosperm affiliation of the gut content in Jeholornis yet, considering that early birds such as those from the Jehol Biota would encounter both gymnosperms and angiosperms, early frugivorous birds were likely to be opportunistic and targeted small, fleshy propagules from both groups, rather than being ‘gymnosperm specialists’.

3) As we stated in the Discussion part: “The occurrence of specialised seed-dispersal by animals during the Early Cretaceous has previously been proposed indirectly, based on the presence of aril-producing gymnosperm and early fruit-producing angiosperms (Eriksson, 2008; Eriksson et al., 2000a). However, the identification of these frugivores has been uncertain and frugivory was almost unmentioned in the recent review of early bird diets (Miller and Pittman, 2021). Evidence for at least seasonal frugivory in Jeholornis provides direct evidence of frugivores and thus indicated highly likely seed-dispersal by animals during the Early Cretaceous for the first time.” We evidenced a long-standing speculation in this area that many researchers are interested – we think this is how important scientific works are made. It is like a “missing link” has been supposed to exist between birds and non-avian reptiles for a long time, but the discovery of Archaeopteryx evidenced it and showed the world how it looks – maybe also not “surprising” but no doubt important and inspiring.

Eriksson O. 2008. Evolution of seed size and biotic seed dispersal in Angiosperms: Paleoecological and Neoecological Evidence. Int J Plant Sci 169:863–870. doi:10.1086/589888

Eriksson O, Friis EM, Löfgren. 2000. Seed size, fruit size, and dispersal systems in Angiosperms from the Early Cretaceous to the Late Tertiary. Am Nat 156:47–58. doi:10.1086/303367

Miller CV, Pittman M. 2021. The diet of early birds based on modern and fossil evidence and a new framework for its reconstruction. Biol Rev. doi:10.1111/brv.12743

3. What is the evidence that seed dispersal by frugivorous birds enhances diversification rates through increased speciation rates or decreased extinction rates in either plants or birds? Please cite relevant studies that evaluated this hypothesis.

Reply to this point are provided in the following reply to Reviewer 2’s comment of “Line 342-343”.

4. The treatment of the plant material seems weak, as the seeds are not described and the brief mention of gymnospermous accessory tissues masks complex plant-animal interactions related to seed dispersal among non-angiosperms. Please improve documentation and analyses.

Reply to this point are provided in the following reply to Reviewer 2’s comment of “Line 260-263”.

5. Please address the points raised in the reviewers' full reports, which are appended below.

Every point in the reviewers’ reports is addressed point to point.

6. Given the concerns raised, there was a feeling that claims were worded too strongly, and that language should be toned down throughout.

We toned down the statement throughout the manuscript, and details are provided in the following reply to Reviewer 3’s comment of point 1.

Please note that, in light of the fact that the study's key claim currently seems insufficiently supported, we will send your revised manuscript out for re-evaluation and that eventual acceptance is not guaranteed.

Reviewer #1 (Recommendations for the authors):

Our main comment is related to experimental design as the possibility that Jeholornis was not a specialist granivore or frugivore was not evaluated to the same extent as granivory and frugivory in your study. This third hypothesis would be important to address using multiple methods simultaneously. This is supported by the PCA data where there is overlap between the granivory and frugivory data points and the 'other diet' data points.

The idea of a bird-plant link in the Early Cretaceous is interesting and could be spelled out more, along with further consideration of the uncertainties revealed in key studies e.g., Hulme 2002.

Hulme, P.E., 2002. Seed-eaters: Seed Dispersal, Destruction and Demography. Seed dispersal and frugivory: Ecology, evolution, and conservation, p.257.

However, this is secondary to our main comment above which is related to experimental design and the data incompletely supporting the conclusions proposed.

We suggest two options to consider [### Note from the Senior Editor: our clear preference is Option 2 ###]:

1) Narrow the scope of the conclusions to those which can be well supported by the data available i.e., a study showing that, for the seed components of the diet of Jeholornis, whether granivory or frugivory is most supported.

2) Alternatively, we suggest to undertake a more holistic diet analysis based on multiple lines of evidence that tests hypothesis 3 and then using the results to inform the conclusions (which may or may not be related to granivory or frugivory).

We hope you find the comments provided helpful.

Thank you very much for the comment and suggested solutions. We have replied to this in details in the previous “An Appraisal of Whether the Authors Achieved their Aims, and Whether the Results Support their Conclusions: ” part, since this is also the main point there. As we said there, there might be some misunderstanding about our study because that the word 'frugivorous' might be misleading to 'specialised frugivorous' to some readers including the reviewer. Actually Option 1 it seems what we claimed all along the manuscript that Jeholornis is at least partially frugivorous but not a specialist frugivore. We only need to rigorously rule out a granivorous explanation of the presence of seeds in the gut of Jeholornis, to demonstrate the partially frugivorous diet of Jeholornis, then we could indicate the occurrence of bird-plant interactions in Early Cretaceous. As we also replied in the previous part: 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, and therefore avian frugivores occupy a wide range of diet space that is highly overlapping with some other diets. Therefore, this would not represent a narrowing of the scope of our conclusions ('at least partial frugivory') as concerned by the reviewer. However, to avoid this kind of understanding, as we stated in previous part: we use adjectives such as 'partial', 'seasonal' and 'opportunistic' as many as we could in the revised manuscript.

Knowing its holistic diet as the Option 2 may not be actually that necessary to our seed dispersal story, so that has almost no relation with our main goal in this study, but we agree that maybe some other readers will also be interested in a more detailed diet of this early avian lineage. Therefore, we conducted supplemental analyses by dividing 'other diets' further to test what diets Jeholornis possibly/impossibly had as supplements of frugivory, which would be testing the reviewer’s 'hypothesis 3'. We excluded some diets in the supplemental analyses and pointed out that what diet are possible to supplement fruits when the fruit resources are not available. More details were described in the previous part of reply. We expect these additional analyses would address the reviewer’s concern here.

Reviewer #2 (Recommendations for the authors):

As far as I can tell, the descriptions and comparisons of skull morphology are detailed and well done. The argument that Jeholornis was not a seed cracker is strong, and the interpretation of Jeholornis as at least seasonally frugivorous is well-reasoned. It does nicely show that volant birds were recruited for endozoochory early. It will be a pleasure to see this published. Nonetheless, I do have some minor questions and concerns/recommendations about the botany and co-evolutionary implications that I think would make the manuscript stronger, along with some minor suggestions regarding the writing clarity that can be adopted at the authors' discretion.

Thank you very much for supporting our claim!

Line 60. Using plesiomorphic as an adverb strikes me as odd. It seems to me the meaning the sentence is unchanged if the word plesiomorphically is omitted and instead it reads "retaining an elongate bony tail"

Revised as suggested.

Line 64. In what way is Jeholornis the most representative jeholornithiform? Are other jeholornithiforms somehow less representative?

We have changed this to ‘…the most abundant jeholornithiform…’. Currently there are only two valid genera among the Jeholornithiformes: Jeholornis and Kompsornis. As we said in Taxonomy of Jeholornis STM 3-8 in Materials and methods section, “The validity of another recently reported jeholornithiformes, Kompsornis longicaudus (Wang et al., 2020) needs more discussions since only one specimen is used to erect it, while no detailed comparisons have been done to the numerous specimens which have been assigned to Jeholornis before”.

Line 75. Consider substituting or adding "seed predation" alongside granivory. This widely used term emphasizes the ecological difference between feeding on seeds vs. other forms of herbivory as it kills a "whole plant."

Revised as suggested. We also added the term through the manuscript when necessary.

Line 77. Consider changing to "mutualistic co-evolutionary influence," or perhaps "co-diversification" is what you mean; however, see my comment about lines 342-343 below.

We revised it to be "mutualistic co-evolutionary influence".

Like 86. "Complete" or "precise" might be a better word choice than "accurate." Are previous reconstructions inaccurate? Perhaps they are just incomplete or poorly resolved, but not inaccurate.

We revised it to be “the most precise cranial reconstruction of a stem bird to date” as suggested.

Line 95. Because of its phylogenetic position… Because modifies a verb, in this case "studied" "Due to" means "caused by". Or, to put it another way, Jeholornis has been frequently studied because of its phylogenetic position.

We revised it to be “Jeholornis has been frequently studied and cited because of its key phylogenetic position” as suggested.

Line 130. I suggest "indicates that rostral fusion evolved earlier (or deeper in bird phylogeny) than previously thought." I also suggest that the authors point out what other characters it now precedes to emphasize the point that paleontology reveals the order of character changes along branches.

We revised it to be “Its occurrence in Jeholornis indicates that rostral fusion of premaxillae evolved phylogenetically deeper among birds than previously thought.” as suggested.

Line 225: I don't think the parentheses are necessary.

Parentheses were deleted as suggested.

Lines 260-263. I encourage the authors to describe the seeds, or at least to summarize the morphological diversity, number of types, (and perhaps their organization) if they were all previously described in O'Connor et al. (2018). What are their morphology, dimensions, and size variation? Do all of them have longitudinal striations? Based on the figures, these seeds appear to be quite large for Cretaceous angiosperms (Tiffney 1984; Eriksson et al. 2000; 2008). Is it more likely that these are seeds of a gymnospermous plant? I suspect so.

We added the summary of descriptions and more likely gymnosperm affinity of the ingested seeds in the paragraph discussing the identification of these seeds: “The alimentary contents preserved in Jeholornis were preliminarily described as ginkgo-like seeds (Zhou and Wu, 2006) and more likely to be gymnosperm due to their relatively large sizes, but have not been confidently identified with detailed comparisons with all the potential Early Cretaceous fruits/arils. In addition, although the poor preservation of these ingested seeds prevents any detailed taxonomic identification, three morphotypes have been grouped in previous studies based on size and shape: morphotype-1 in smaller size with a circular shape and curved striations, morphotype-2 in larger size with an oval shape, and morphotype-3 in similar size to morphotype-1 but with a strongly tapered pole (O’Connor et al., 2018).”

Lines 274-277. The hypothesis about seasonal frugivory in Jeholornis is both reasonable and interesting. Some indication of warm climate with seasonality of precipitation is supported elsewhere in the Jehol biota by Ding et al.'s (2016) analysis of fossil woods. It may be worth citing that work.

Thank you very much for the helpful citation information, it was added now.

Lines 305-315. Extant gymnosperms that use endozoochory for seed dispersal use a variety of accessory tissues, not just arils. Ginkgo, cycads, and some extinct groups have a fleshy sarcotesta (outer seed coat). An aril is a fleshy appendage of the seed coat or the funiculus. Some gymnosperms have fleshy subtending bracts (Ephedra), and some have fleshy accessory tissues such as bracts (Ephedra), cones (Juniperus), receptacle and epimatium (Podocarpaceae), or fleshy cones with numerous seeds (Juniperus). See Tiffney (1986, 2004); Herrera (1989); Lovisetto et al. (2012); Contreras et al. (2017); Nigris et al. (2021). I suggest Herrera (1989) as an earlier citation than Herendeen et al. (2017) for line 306.

Thank you very much for the helpful knowledge from the botanical view! This sentence was revised to be: “Although true fruits are only present in angiosperms, seed ferns and gymnosperms evolved functionally analogous fleshy-coated propagules (arils) and other fleshy accessory tissues much earlier (Tiffney, 1986, 2004; Herrera, 1989; Lovisetto et al., 2012; Contreras et al., 2017; Herendeen et al., 2017).” now.

Line 318. Why small? What does small mean? Small enough to fit in their mouth?

Yes we mean small enough for the early birds to swallow, in which way Jeholornis did it. We deleted the word ‘small’ to avoid confusion.

Line 321. I suggest "early and repeated" instead of "ancient". It appears to be clear that there are multiple origins of frugivory/omnivory within crown group birds, and it is not clear that the MRCA of crown-group birds was frugivorus (Felice et al. 2019). This lability in bird diet and repeated origin of frugivory might actually better support the authors' argument that diffuse coevolution between angiosperms and frugivorous birds contributed the KTR. There is now good evidence that volant birds have been repeatedly recruited by plants as endozoochorous seed dispeserers, even prior to the evolution of the MRCA of extant birds.

Thanks for the suggestion, we agree and revised this part to be “…the early and most likely repeated origin of frugivory in birds…” now.

Line 342-343. Can you provide a citation linking dispersal mode to diversification rate? Eriksson and Bremer (1992) in the journal 'Evolution' found no relationship between dispersal mode and diversification rate in angiosperms, although Carlo and Morales (2015) in the journal 'Ecology' showed evidence that frugivorous birds increase plant α diversity.

Thank you very much for the suggestion! We added Muller-Landau and Hardesty (2005), Dennis et al. (2007), Jordano (2014), Carlo et al. (2022), to support the mutualisms of frugivory and seed dispersal by animals here, which is one of the most studied mutualisms about biodiversity. We may also want to clarify here that our work supports the hypothesis that “bird-plant interactions played a role in the Cretaceous Terrestrial Revolution”, but we are not testing if it has a more important role than other factors e.g. insect pollination – we are far from reaching enough fossil information from either the bird or the insect side to test this at this moment. The mutualisms of frugivory and seed dispersal by animals among extant taxa are enough to confirm the benefit of the appearance of a new mutualistic mechanism like frugivory of birds in early KTR stage.

The study in Eriksson and Bremer (1992) about the extant dispersal mode to diversification rate are actually about comparisons of the influence of dispersal mode to other factors like insect pollination. In Eriksson and Bremer (1992), they were mostly claiming that (1) pollination systems and (2) life forms are more important factors than (3) animal dispersal. In addition, they emphasized that these three hypotheses are not mutually exclusive, and “several mechanisms in concert determine variation in diversification rate in plant”. They also emphasized that this evaluation was restricted for explaining present-day angiosperm diversification. We think the comparisons of influence of mostly insect involved biotic interactions and birds/mammals for present plants cannot be directly applied to the transitional, early KTR stage. Eriksson and Bremer (1992) also agreed that for the deeper evolutionary history, “a positive influence on diversification by animal dispersal, may have been important during Early Tertiary, but is nevertheless not detectable in a data set based on extant number of species.”.

We also added Carlo and Morales (2016) here as you mentioned (we think this is the paper you were talking about), since comparatively, the work in Carlo and Morales (2016) focusing on the speed and diversity of early successional forests resembled more to the early stage of KTR, while the angiosperms are also of much lesser abundance at that period.

Carlo TA, Morales JM (2016). Generalist birds promote tropical forest regeneration and increase plant diversity via rare‐biased seed dispersal. Ecology 97(7): 1819–1831.

Carlo TA, Cazetta E, Traveset A, Guimarães PR, McConkey KR. 2022. Fruits, animals and seed dispersal: timely advances on a key mutualism. Oikos, 2022: e09220.

Dennis AJ, editor. 2007. Seed dispersal: theory and its application in a changing world. CABI, Wallingford, UK.

Jordano P. 2014. Fruits and frugivory In: Gallagher RS, editor. Seeds: The Ecology of Regeneration of Plant Communities, 3rd edn. CABI, Wallingford, UK. pp. 18–61.

Muller-Landau HC, Hardesty BD. 2005. Seed dispersal of woody plants in tropical forests: concepts, examples, and future directions In: Burslem D, Pinard M, Hartley S, editors. Biotic interactions in the tropics: Their role in the maintenance of species diversity. Cambridge: Cambridge University Press. pp. 267–309.

Author details

1. Han Hu

   1. Department of Earth Sciences, University of Oxford, Oxford, United Kingdom
   2. Zoology Division, School of Environmental and Rural Sciences, University of New England, Armidale, Australia

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   han.hu@earth.ox.ac.uk

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5926-7306

2. Yan Wang

   Institute of Geology and Paleontology, Linyi University, Linyi, China

   Contribution

   Conceptualization, Resources, Funding acquisition, Investigation, Writing – review and editing

   For correspondence

   wangyan6696@lyu.edu.cn

   Competing interests

   No competing interests declared

3. Paul G McDonald

   Zoology Division, School of Environmental and Rural Sciences, University of New England, Armidale, Australia

   Contribution

   Supervision, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

4. Stephen Wroe

   Zoology Division, School of Environmental and Rural Sciences, University of New England, Armidale, Australia

   Contribution

   Supervision, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

5. Jingmai K O'Connor

   1. Field Museum of Natural History, Chicago, United States
   2. Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China
   3. Chinese Academy of Sciences Center for Excellence in Life and Paleoenvironment, Beijing, China

   Contribution

   Investigation, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

6. Alexander Bjarnason

   Department of Earth Sciences, University of Oxford, Oxford, United Kingdom

   Contribution

   Data curation, Formal analysis, Investigation

   Competing interests

   No competing interests declared

7. Joseph J Bevitt

   Australian Centre for Neutron Scattering, Australian Nuclear Science and Technology Organisation, Sydney, Australia

   Contribution

   Resources, Funding acquisition, Investigation

   Competing interests

   No competing interests declared

8. Xuwei Yin

   Shandong Tianyu Museum of Nature, Linyi, China

   Contribution

   Resources, Investigation

   Competing interests

   No competing interests declared

9. Xiaoting Zheng

   1. Institute of Geology and Paleontology, Linyi University, Linyi, China
   2. Shandong Tianyu Museum of Nature, Linyi, China

   Contribution

   Resources, Investigation

   Competing interests

   No competing interests declared

10. Zhonghe Zhou

    1. Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China
    2. Chinese Academy of Sciences Center for Excellence in Life and Paleoenvironment, Beijing, China

    Contribution

    Conceptualization, Resources, Supervision, Funding acquisition, Investigation, Writing – review and editing

    Competing interests

    No competing interests declared

11. Roger BJ Benson

    Department of Earth Sciences, University of Oxford, Oxford, United Kingdom

    Contribution

    Conceptualization, Formal analysis, Supervision, Investigation, Methodology, Writing – original draft, Writing – review and editing

    Competing interests

    No competing interests declared

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