Cartilage on the furculae of living birds and the extinct bird Confuciusornis: a preliminary analysis and implications for flight style inferences in Mesozoic birds
Received date: 2020-11-20
Online published: 2021-04-20
The early evolution of flight is one of the most studied topics in vertebrate paleontology. Living birds have evolved to utilize a variety of flight styles, but studies focused on inferring flight strategies in Mesozoic birds are often contradictory and without a clear consensus, making it necessary to find additional informative characteristics that can be useful for inferences in fossils. Virtually nothing is known about the histology of the avian pectoral girdle, even though skeletal and joint tissues are key candidates to solve form-function relationships. Avian secondary cartilage found on the dermal bones of the avian skeleton is influenced by epigenetics and only forms when joints are stimulated by muscle contractions. As the only dermal bone in the avian postcranium, the furcula is a potential site for the formation of furcular secondary cartilage and merits further attention. It is still unknown whether adult living birds and fossil birds have furcular secondary cartilage. Here we present histological analyses conducted on the furcula-coracoid articulation in three living birds (Spilopelia chinensis, the Spotted dove; Passer montanus, the Eurasian tree sparrow; and Apus apus, the Common swift), taxa that utilize different flight styles, and one of the most common fossil birds of the Jehol Biota, Confuciusornis. Secondary cartilage was identified on the furculae of the living birds and of Confuciusornis, representing the first report of furcular secondary cartilage in the fossil record. Clear differences in secondary cartilage morphologies were observed in the living species, but additional data is required to establish a strong form-function relationship that could be useful for making inferences in Mesozoic birds.
Key words： Evolution of flight; birds; Confuciusornis; furcula; histology; secondary cartilage
WU Qian, Jingmai K. O’CONNOR, LI Zhi-Heng, Alida M. BAILLEUL . Cartilage on the furculae of living birds and the extinct bird Confuciusornis: a preliminary analysis and implications for flight style inferences in Mesozoic birds[J]. Vertebrata Palasiatica, 2021 , 59(2) : 106 -124 . DOI: 10.19615/j.cnki.1000-3118.201222
| [1] | Bailleul A M, Hall B K, Horner J R, 2012. First evidence of dinosaurian secondary cartilage in the post-hatching skull of Hypacrosaurus stebingeri (Dinosauria, Ornithischia). PLoS ONE, 7(4):e36112 |
| [2] | Bailleul A M, Hall B K, Horner J R, 2013. Secondary cartilage revealed in a non-avian dinosaur embryo. PLoS ONE, 8(2):e56937 |
| [3] | Bailleul A M, Witmer L M, Holliday C M, 2017. Cranial joint histology in the mallard duck (Anas platyrhynchos): new insights on avian cranial kinesis. J Anat, 230(3):444-460 |
| [4] | Bailleul A M, Li Z H, O’Connor J K et al., 2019a. Origin of the avian predentary and evidence of a unique form of cranial kinesis in Cretaceous ornithuromorphs. Proc Natl Acad Sci USA, 116:24696-24706 |
| [5] | Bailleul A M, O’Connor J K, Schweitzer M H, 2019b. Dinosaur paleohistology: review, trends and new avenues of investigation. PeerJ, 2019(9):1-45 |
| [6] | Baumel J, Raikow R, 1993. Arthrologia. In: Baumel J J, King A S, Breazile J E et al. eds. Handbook of Avian Anatomy: Nomina Anatomica Avium, 2nd ed. Cambridge, Massachusetts: Publications of the Nuttall Ornithological Club. 133-187 |
| [7] | Bishop C M, Butler P J, 2015. Flight. In: Scanes C G, Sturkie P D eds. Sturkie’s Avian Physiology. London: Elsevier/Academic Press. 919-967 |
| [8] | Bruderer B, Peter D, Boldt A et al., 2010. Wing-beat characteristics of birds recorded with tracking radar and cine camera. Ibis, 152(2):272-291 |
| [9] | Brusatte S L, Lloyd G T, Wang S C et al., 2014. Gradual assembly of avian body plan culminated in rapid rates of evolution across the dinosaur-bird transition. Curr Biol, 24(20):2386-2392 |
| [10] | Butler P J, 2016. The physiological basis of bird flight. Philos Trans R Soc B, 371:20150384 |
| [11] | Canoville A, Schweitzer M H, Zanno L E, 2019. Systemic distribution of medullary bone in the avian skeleton: ground truthing criteria for the identification of reproductive tissues in extinct Avemetatarsalia. BMC Evol Biol, 19(1):71 |
| [12] | Carter D R, Orr T E, Fyhrie D P et al., 1987. Influences of mechanical stress on prenatal and postnatal skeletal development. Clin Orthop Relat Res, 219:237-250 |
| [13] | Chiappe L M, Ji S A, Ji Q et al., 1999. Anatomy and systematics of the Confuciusornithidae (Theropoda, Aves) from the Late Mesozoic of northeastern China. Bull Am Mus Nat Hist, 242:1-89 |
| [14] | Chiappe L M, Di L, Serrano F J et al., 2019a. Anatomy and flight performance of the early enantiornithine bird Protopteryx fengningensis: information from new specimens of the Early Cretaceous Huajiying Formation of China. Anat Rec, 303(4):716-731 |
| [15] | Chiappe L M, Meng Q J, Serrano F et al., 2019b. New Bohaiornis-like bird from the Early Cretaceous of China: enantiornithine interrelationships and flight performance. PeerJ, 7:e7846 |
| [16] | Chinsamy A, Marugán-Lobón J, Serrano F J et al., 2020. Osteohistology and life history of the basal pygostylian, Confuciusornis sanctus. Anat Rec, 303(4):949-962 |
| [17] | Close R A, Rayfield E J, 2012. Functional morphometric analysis of the furcula in Mesozoic birds. PLoS ONE, 7(5):e36664 |
| [18] | Dececchi T A, Larsson H C, 2011. Assessing arboreal adaptations of bird antecedents: testing the ecological setting of the origin of the avian flight stroke. PLoS ONE, 6(8):e22292 |
| [19] | Dial K P, Jackson B E, Segre P, 2008. A fundamental avian wing-stroke provides a new perspective on the evolution of flight. Nature, 451:985 |
| [20] | Falk A R, Kaye T G, Zhou Z H et al., 2016. Laser fluorescence illuminates the soft tissue and life habits of the Early Cretaceous bird Confuciusornis. PLoS ONE, 11(4):e0167284 |
| [21] | Feo T J, Field D J, Prum R O, 2015. Barb geometry of asymmetrical feathers reveals a transitional morphology in the evolution of avian flight. Proc R Soc B-Biol Sci, 282:20142864 |
| [22] | Fürbringer M, 1888. Untersuchungen zur Morphologie und Systemat der V?gel II. Allgemeiner Theil. Amsterdam: Verlag von T J. Van Holkema. 1-884 |
| [23] | Hall B K, 1967. The distribution and fate of the adventitious cartilage in the skull of the eastern rosella, Platycerus eximius (Aves : Psittaciformes). Aust J Zool, 15(4):685 |
| [24] | Hall B K, 1972. Immobilization and cartilage transformation into bone in the embryonic chick. Anat Rec, 173(4):391-404 |
| [25] | Hall B K, 1986. The role of movement and tissue interactions in the development and growth of bone and secondary cartilage in the clavicle of the embryonic chick. Development, 93(1):133-152 |
| [26] | Hall B K, 2000. The evolution of the neural crest in vertebrates. In: Olsson L, Jacobson C O eds. Regulatory Processes in Development, Wenner-Gren International Series Vol. 76. London: Portland Press. 101-113 |
| [27] | Hall B K, 2001. Development of the clavicles in birds and mammals. J Exp Zool, 289(3):153-161 |
| [28] | Hall B K, Vickaryous M K, 2015. Merrythoughts of the past and present: revisiting the homology of the furcula. In: Belinda-Emonds O R P, Powell G L, Jamniczky H A eds. All Animals are Interesting. A Festschrift in Honour of Anthony P. Russell. Oldenburg Germany: BIS-Verlag -Carl von Ossietzky University. 439-454 |
| [29] | Hou L H, Martin L D, Zhou Z H et al., 1999. A diapsid skull in a new species of the primitive bird Confuciusornis. Nature, 399:679-682 |
| [30] | Hui C A, 2002. Avian furcula morphology may indicate relationships of flight requirements among birds. J Morphol, 251(3):284-293 |
| [31] | Jenkins F A, 1993. The evolution of the avian shoulder joint. Am J Sci, 293(A):253-267 |
| [32] | Jenkins F A, Dial K P, Goslow G E, 1988. A cineradiographic analysis of bird flight: the wishbone in starlings is a spring. Science, 241:1495-1498 |
| [33] | Jiang B, Zhao T, Regnault S et al., 2017. Cellular preservation of musculoskeletal specializations in the Cretaceous bird Confuciusornis. Nat Commun, 8(1):1-10 |
| [34] | Kardong K V, 2019. Vertebrates: Comparative Anatomy, Function, Evolution. 8th ed. New York, NY: McGraw-Hill Education. 1-817 |
| [35] | Liu D, Chiappe L M, Serrano F et al., 2017. Flight aerodynamics in enantiornithines: information from a new Chinese Early Cretaceous bird. PLoS ONE, 12(10):e0184637 |
| [36] | McGonnell I M, 2001. The evolution of the pectoral girdle. J Anat, 199:189-194 |
| [37] | Mitchell J, Legendre L J, Lefèvre C et al, 2017. Bone histological correlates of soaring and high-frequency flapping flight in the furculae of birds. Zoology, 122:90-99 |
| [38] | Müller G B, 2003. Embryonic motility: environmental influences and evolutionary innovation. Evol Dev, 5(1):56-60 |
| [39] | Murray P D, Drachman D B, 1969. The role of movement in the development of joints and related structures: the head and neck in the chick embryo. Development, 22(3):349-371 |
| [40] | Murray P D F, Smiles M, 1965. Factors in the evocation of adventitious (secondary) cartilage in the chick embryo. Aust J Zool, 13(3):351-382 |
| [41] | Nudds R L, Dyke G J, 2010. Narrow primary feather rachises in Confuciusornis and Archaeopteryx suggest poor flight ability. Science, 328:887-889 |
| [42] | O’Connor P M, 2004. Pulmonary pneumaticity in the postcranial skeleton of extant Aves: a case study examining Anseriformes. J Morphol, 261(2):141-161 |
| [43] | Persson M, 1983. The role of movements in the development of sutural and diarthrodial joints tested by long-term paralysis of chick embryos. J Anat, 137(3):591-599 |
| [44] | Pollard A S, Boyd S, McGonnell I M et al., 2017. The role of embryo movement in the development of the furcula. J Anat, 230(3):435-443 |
| [45] | Ponomartsev S, Valasek P, Patel K et al., 2017. Neural crest contribution to the avian shoulder girdle and implications to girdle evolution in vertebrates. Biol Comm, 62(1):26-37 |
| [46] | Ponton F, Montes L, Castanet J et al., 2007. Bone histological correlates of high-frequency flapping flight and body mass in the furculae of birds: a phylogenetic approach. Biol J Linn Soc, 91(4):729-738 |
| [47] | Russell A P, Joffe D J, 1985. The early development of the quail (Coturnix c. japonica) furcula reconsidered. J Zool, 206(1):69-81 |
| [48] | Schepelmann K, 1990. Erythropoietic bone marrow in the pigeon: development of its distribution and volume during growth and pneumatization of bones. J Morphol, 203(1):21-34 |
| [49] | Senter P, 2006. Scapular orientation in the theropods and basal birds, and the origin of flapping flight. Acta Palaeontol Pol, 51(2):305-313 |
| [50] | Serrano F J, Chiappe L M, 2017. Aerodynamic modelling of a Cretaceous bird reveals thermal soaring capabilities during early avian evolution. J R Soc Interface, 14:20170182 |
| [51] | Serrano F J, Palmqvist P, Chiappe L M et al., 2017. Inferring flight parameters of Mesozoic avians through multivariate analyses of forelimb elements in their living relatives. Paleobiology, 43(1):144-169 |
| [52] | Serrano F J, Chiappe L M, Palmqvist P et al., 2018. Flight reconstruction of two European enantiornithines (Aves, Pygostylia) and the achievement of bounding flight in Early Cretaceous birds. Palaeontology, 61(3):359-368 |
| [53] | Shatkovska O V, Ghazali M, 2017. Relationship between developmental modes, flight styles, and wing morphology in birds. Eur Zool J, 84(1):390-401 |
| [54] | Usherwood J R, 2016. Physiological, aerodynamic and geometric constraints of flapping account for bird gaits, and bounding and flap-gliding flight strategies. J Theor Biol, 408:42-52 |
| [55] | Vazquez R J, 1992. Functional osteology of the avian wrist and the evolution of flapping flight. J Morphol, 211(3):259-268 |
| [56] | Vickaryous M K, Hall B K, 2010. Comparative development of the crocodylian interclavicle and avian furcula, with comments on the homology of dermal elements in the pectoral apparatus. J Exp Zool, 314B(3):196-207 |
| [57] | Wang X, Tang H K, Clarke J A, 2019a. Flight, symmetry and barb angle evolution in the feathers of birds and other dinosaurs. Biol Lett, 15(12):9-14 |
| [58] | Wang M, O’Connor J K, Zhou Z H, 2019b. A taxonomical revision of the Confuciusornithiformes (Aves: Pygostylia). Vert PalAsiat, 57:1-37 |
| [59] | Witten P E, Hall B K, 2003. Seasonal changes in the lower jaw skeleton in male Atlantic salmon (Salmo salar L.): remodelling and regression of the kype after spawning. J Anat, 203(5):435-450 |
/
| 〈 |
|
〉 |