Morphometric analysis of the cervical vertebral series in extant birds with implications for Mesozoic avialan feeding ecology
Received date: 2023-11-07
Online published: 2024-03-06
The inference of Mesozoic avialan bird diets previously relied on traditional methods such as morphological comparisons among taxa and direct evidence such as identifiable stomach contents. However, the application of these approaches has been limited because of uncommon preservation of relevant fossil evidence. We searched for additional informative characteristics to help develop new methods to assess the diet of fossil birds. In particular, the morphology of the avialan neck is highly modularized and plays roles in multiple functions including food acquisition. The structure of and variation among the cervical vertebrae likely reflects the demands of feeding ecology in fossil and extant birds because the avialan neck evolved to, at least in part, replace the forelimbs by assisting with activities such as cranioinertial feeding and other ecological functions. Here, we utilize morphometric and statistical analyses to establish an initial quantitative relationship between cervical morphology and dietary modes in both extant and extinct birds. This morphometric framework derived from the cervical morphology of living birds is used as a basis to estimate the diet categories of five taxa of Mesozoic birds. The results indicate that there is a quantitative correlation between cervical morphology differentiation and their interrelated feeding modes. The enantiornithine taxa examined exhibit cervical morphologies similar to extant insectivorous or carnivorous birds. The ornithurine species show cervical morphologies that are more aligned with generalist or herbivorous birds, and exhibit preliminary morphological features tied to aquatic adaptions. These findings are consistent in part with other direct fossil evidence, as well as hypotheses developed from other skeletal comparisons. Therefore, the cervical vertebral series, as a skeletal system closely linked to food acquisition, can serve as one of the valuable metrics to provide information for inferring the diet of long extinct Mesozoic birds.
Key words： Mesozoic birds; cervical morphology; diet; ecological variation
LIU Bi-Ying , Thomas A. STIDHAM , WANG Xiao-Ping , LI Zhi-Heng , ZHOU Zhong-He . Morphometric analysis of the cervical vertebral series in extant birds with implications for Mesozoic avialan feeding ecology[J]. Vertebrata Palasiatica, 2024 , 62(2) : 99 -119 . DOI: 10.19615/j.cnki.2096-9899.240305
| [1] | Blomberg S P, Garland T Jr, Ives A R, 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution, 57: 717-745 |
| [2] | B?hmer C, Rauhut O W M, W?rheide G, 2015. Correlation between Hox code and vertebral morphology in archosaurs. Proc R Soc B-Biol Sci, 282: 20150077 |
| [3] | B?hmer C, Plateau O, Cornette R et al., 2019. Correlated evolution of neck length and leg length in birds. R Soc Open Sci, 6: 181588 |
| [4] | Chiappe L, Walker C, 2002. Skeletal morphology and systematics of the Cretaceous Euenantiornithes (Ornithothoraces:Enantiornithes). In: ChiappeL M, WitmerL M, eds. Mesozoic Birds:Above the Heads of Dinosaurs. Berkeley: University of California Press. 240-267 |
| [5] | Cobley M J, Rayfield E J, Barrett P M, 2013. Inter-vertebral flexibility of the ostrich neck: implications for estimating sauropod neck flexibility. PLoS One, 8: e72187 |
| [6] | Cooney C R, Bright J A, Capp E J R et al., 2017. Mega-evolutionary dynamics of the adaptive radiation of birds. Nature, 542: 344-347 |
| [7] | Falk A R, Lamsdell J C, Gong E, 2021. Principal component analysis of avian hind limb and foot morphometrics and the relationship between ecology and phylogeny. Paleobiology, 47: 314-336 |
| [8] | Freckleton R P, Harvey P H, Pagel M, 2002. Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat, 160: 712-726 |
| [9] | Harmon L J, Weir J T, Brock C D et al., 2007. GEIGER: investigating evolutionary radiations. Bioinformatics, 24: 129-131 |
| [10] | Heidweiller J, 1989. Post natal development of the neck system in the chicken (Gallus domesticus). Am J Anat, 186: 258-270 |
| [11] | Hu H, Zhou Z H, O’Connor J K et al., 2014. A subadult specimen of Pengornis and character evolution in Enantiornithes. Vert PalAsiat, 52(1): 77-97 |
| [12] | Kambic R E, Biewener A A, Pierce S E, 2017. Experimental determination of three-dimensional cervical joint mobility in the avian neck. Front Zool, 14: 37 |
| [13] | Kamilar J M, Cooper N, 2013. Phylogenetic signal in primate behaviour, ecology and life history. Philos Trans R Soc B-Biol Sci, 368: 20120341 |
| [14] | Kardong K V, 2012. Vertebrates:Comparative Anatomy, Function, Evolution. New York: McGraw-Hill. 294-324 |
| [15] | Kembel S W, Cowan P D, Helmus M R et al., 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26: 1463-1464 |
| [16] | Krings M, Nyakatura J A, Fischer M S et al., 2014. The cervical spine of the American Barn Owl (Tyto furcata pratincola): I. Anatomy of the vertebrae and regionalization in their S-shaped arrangement. PLoS One, 9: e91653 |
| [17] | Krings M, Nyakatura J A, Boumans M L L M et al., 2017. Barn owls maximize head rotations by a combination of yawing and rolling in functionally diverse regions of the neck. J Anat, 231: 12-22 |
| [18] | Li Z H, Clarke J A, 2016. The craniolingual morphology of waterfowl (Aves, Anseriformes) and its relationship with feeding Mode revealed through contrast-enhanced X-Ray computed tomography and 2D morphometrics. Evol Biol, 43: 12-25 |
| [19] | Li Z H, Zhou Z H, Wang M et al., 2014. A new specimen of large-bodied basal Enantiornithine Bohaiornis from the Early Cretaceous of China and the inference of feeding ecology in Mesozoic birds. J Paleontol, 88: 99-108 |
| [20] | Li Z H, Wang M, Stidham T A et al., 2022. Novel evolution of a hyper-elongated tongue in a Cretaceous enantiornithine from China and the evolution of the hyolingual apparatus and feeding in birds. J Anat, 240: 627-638 |
| [21] | Liu Y, Chen S, 2021. The CNG Field Guide to the Birds of China. Changsha: Hunan Science and Technology Press. 1-636 |
| [22] | Marek R D, 2023. A surrogate forelimb: evolution, function and development of the avian cervical spine. J Morphol, 284: e21638 |
| [23] | Marek R D, Falkingham P L, Benson R B J et al., 2021. Evolutionary versatility of the avian neck. Proc R Soc B-Biol Sci, 288: 20203150 |
| [24] | Miller C V, Pittman M, 2021. The diet of early birds based on modern and fossil evidence and a new framework for its reconstruction. Biol Rev, 96: 2058-2112 |
| [25] | Miller C V, Pittman M, Wang X et al., 2023. Quantitative investigation of pengornithid enantiornithine diet reveals macrocarnivorous ecology evolved in birds by Early Cretaceous. iScience, 26: 106211 |
| [26] | O’Connor J K, 2019. The trophic habits of early birds. Palaeogeogr, Palaeoclimatol, Palaeoecol, 513: 178-195 |
| [27] | O’Connor J K, Chiappe L, 2011. A revision of enantiornithine (Aves: Ornithothoraces) skull morphology. J Syst Palaeontol, 9: 135-157 |
| [28] | O’Connor J K, Wang X R, Chiappe L et al., 2009. Phylogenetic support for a specialized clade of Cretaceous Enantiornithine birds with information from a new species. J Vert Paleont, 29: 188-204 |
| [29] | Paradis E, Claude J, Strimmer K, 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20: 289-290 |
| [30] | Revell L J, 2009. Size-correction and principal components for interspecific comparative studies. Evolution, 63: 3258-3268 |
| [31] | Revell L J, 2012. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol, 3: 217-223 |
| [32] | Rico-Guevara A, Sustaita D, Gussekloo S et al., 2019. Feeding in birds:thriving in terrestrial, aquatic, and aerial niches. In: BelsV, Whishaw I eds. Cham: Springer. 643-693 |
| [33] | Tambussi C P, de Mendoza R, Degrange F J et al., 2012. Flexibility along the neck of the Neogene terror bird Andalgalornis steulleti (Aves Phorusrhacidae). PLoS One, 7: e37701 |
| [34] | Terray L, Plateau O, Abourachid A et al., 2020. Modularity of the neck in birds (Aves). Evol Biol, 47: 97-110 |
| [35] | Upchurch P, Barrett P M, 2000. The evolution of sauropod feeding mechanisms. In: Sues H D ed. Evolution of Herbivory in Terrestrial Vertebrates:Perspectives from the Fossil Record. Cambridge: Cambridge University Press. 79-122 |
| [36] | van der Leeuw A H J, Bout R G, Zweers G A, 2015. Control of the cranio-cervical system during feeding in birds. Am Zool, 41: 1352-1363 |
| [37] | Venables B, Ripley B, 2002. Modern Applied Statistics With S. New York: Springer. 1-465 |
| [38] | Wang M, 2023. A new specimen of Parabohaiornis martini (Avialae: Enantiornithes) sheds light on early avian skull evolution. Vert PalAsiat, 61(2): 90-107 |
| [39] | Wang M, Lloyd G T, 2016. Rates of morphological evolution are heterogeneous in Early Cretaceous birds. Proc R Soc B-Biol Sci, 283: 20160214 |
| [40] | Wang X R, Shen C Z, Liu S Z et al., 2015. New material of Longipteryx (Aves: Enantiornithes) from the Lower Cretaceous Yixian Formation of China with the first recognized avian tooth crenulations. Zootaxa, 3941: 565-578 |
| [41] | Wilkinson D M, Ruxton G D, 2012. Understanding selection for long necks in different taxa. Biol Rev, 87: 616-630 |
| [42] | Wu Y, 2021. Molecular phyloecology suggests a trophic shift concurrent with the evolution of the first birds. Commun Biol, 4: 547 |
| [43] | Xu X, Zhou Z H, Wang Y et al., 2020. Study on the Jehol Biota: recent advances and future prospects. Sci China Earth Sci, 63: 757-773 |
| [44] | Zelenkov N V, 2017. Early Cretaceous Enantiornithine birds (Aves, Ornithothoraces) and establishment of the Ornithuromorpha morphological type. Paleontol J, 51: 628-642 |
| [45] | Zelenkov N V, Averianov A O, 2016. A historical specimen of enantiornithine bird from the Early Cretaceous of Mongolia representing a new taxon with a specialized neck morphology. J Syst Palaeontol, 14: 319-338 |
| [46] | Zhang F C, Zhou Z H, Hou L H et al., 2001. Early diversification of birds: evidence from a new opposite bird. Chinese Sci Bull, 46: 945-949 |
| [47] | Zheng X T, O’Connor J K, Huchzermeyer F et al., 2014. New specimens of Yanornis indicate a piscivorous diet and modern alimentary canal. PLoS One, 9: e95036 |
| [48] | Zhou S, O’Connor J K, Wang M, 2014a. A new species from an ornithuromorph (Aves: Ornithothoraces) dominated locality of the Jehol Biota. Chinese Sci Bull, 59: 5366-5378 |
| [49] | Zhou S, Zhou Z H, O’Connor J K, 2014b. A new piscivorous ornithuromorph from the Jehol Biota. Hist Biol, 26: 608-618 |
| [50] | Zhou Z H, Zhang F C, 2002. A long-tailed, seed-eating bird from the Early Cretaceous of China. Nature, 418: 405-409 |
| [51] | Zhou Z H, Zhang F C, 2005. Discovery of an ornithurine bird and its implication for Early Cretaceous avian radiation. Proc Nat Acad Sci USA, 102: 18998-19002 |
| [52] | Zhou Z H, Zhang F C, 2007. Mesozoic birds of China-a synoptic review. Front Biol China, 2: 1-14 |
| [53] | Zhou Z H, Clarke J, Zhang F C et al., 2004. Gastroliths in Yanornis: an indication of the earliest radical diet-switching and gizzard plasticity in the lineage leading to living birds? Naturwissenschaften, 91: 571-574 |
| [54] | Zhou Z H, Clarke J, Zhang F C, 2008. Insight into diversity, body size and morphological evolution from the largest Early Cretaceous enantiornithine bird. J Anat, 212: 565-577 |
| [55] | Zhou Z H, Zhang F C, Li Z H, 2009. A new basal ornithurine bird (Jianchangornis microdonta gen. et sp. nov.) from the Lower Cretaceous of China. Vert PalAsiat, 47(4): 299-310 |
| [56] | Zhou Z H, Meng Q, Zhu R et al., 2021. Spatiotemporal evolution of the Jehol Biota: responses to the North China craton destruction in the Early Cretaceous. Proc Nat Acad Sci USA, 118: e2107859118 |
/
| 〈 |
|
〉 |