Published December 20, 2022 | Version v1
Journal article Open

Generalist diet of Microraptor zhaoianus included mammals

  • 1. School of Biological and Behavioural Sciences, Queen Mary University of London, London, U.K.
  • 2. Division of Natural Sciences, Mount Marty College, Yankton, South Dakota, U.S.A.
  • 3. Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada
  • 4. Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China
  • 5. Redpath Museum, McGill University, Quebec, Canada. hans.ce.larsson@mcgill.ca

Description

Gut contents are extremely important for inferring trophic interactions between extinct species. These are, however, very rare in the fossil record and it is not always possible to accurately identify both the carnivore and the consumed organisms. Here we describe the remains of a small fossil mammal foot preserved inside the body cavity of the holotype specimen of the small feathered dinosaur Microraptor zhaoianus. This adds to the known diversity of diet for this genus, which also consumed birds, fish, and lizards. Previous interpretations that Microraptor was an arboreal hunter of birds and adept hunter of fish are not supported. Although the various known stomach contents would be plausible prey items based on size, there is no clear evidence that any of them were predated rather than scavenged, and Microraptor likely did both and foraged in multiple habitats

Files

journalOfVertebratePaleontology.10.1080_02724634.2022.2144337.pdf

Files (721.1 kB)

Additional details

Identifiers

LSID
urn:lsid:plazi.org:pub:F222DD67FFF7FFEBA20BF0663E55D843

References

  • Alexander, D. E., Gong, E., Martin, L. D., Burnham, D. A. & Falk, A. R. (2010). Model tests of gliding with different hindwing configurations in the four-winged dromaeosaurid Microraptor gui. Proceedings of the National Academy of Sciences, 107, 2972-2976.
  • Barsbold, R., & Osmolska, H. (1999). The skull of Velociraptor (Theropoda) from the Late Cretaceous of Mongolia. Acta Palaeontologica Polonica, 44, 189-219.
  • Birn-Jeffery, A. V., Miller, C. E., Naish, D., Rayfield, E. J., & Hone, D. W. (2012). Pedal claw curvature in birds, lizards and Mesozoic dinosaurs-complicated categories and compensating for mass-specific and phylogenetic control. PLoS ONE, 7(12).
  • Blumenschine, R. J. (1986). Carcass consumption sequences and the archaeological distinction of scavenging and hunting. Journal of Human Evolution, 15, 639-659.
  • Bock, W. J. (1966). An approach to the functional analysis of bill shape. The Auk, 83, 10-51.
  • Carbone, C., Mace, G. M., Roberts, S. C., & Macdonald, D. W. (1999). Energetic constraints on the diet of terrestrial carnivores. Nature, 402, 286-288.
  • Carbone, C., Teacher, A., & Rowcliffe, J. M. (2007). The costs of carnivory. PLoS Biology, 5, e22.
  • Charig, A. J., & Milner, A. C. (1997). Baryonyx walkeri, a fish-eating dinosaur from the Wealden of Surrey, Bulletin of the Natural History Museum, Geology Series, 53, 11-70.
  • Chatterjee, S., & Templin, R. J. (2007). Biplane wing planform and flight performance of the feathered dinosaur Microraptor gui. Proceedings of the National Academy of Sciences, 104, 1576-1580.
  • Chen, M., & Luo, Z. X. (2013). Postcranial skeleton of the Cretaceous mammal Akidolestes cifellii and its locomotor adaptations. Journal of Mammalian Evolution, 20, 159-189.
  • Chin, K. (2012). What did dinosaurs eat: coprolites and other direct evidence of dinosaur diets. In J. O. Farlow & M. J. Brett-Surman (Eds.), The Complete Dinosaur (pp. 371-382). Indiana University Press.
  • Chin, K., Tokaryk, T. T., Erickson, G. M., & Calk, L. C. (1998). A kingsized theropod coprolite. Nature, 393, 680-682.
  • Christiansen, P., & Farina R. A. (2004). Mass prediction in theropod dinosaurs. Historical Biology, 16, 85-92.
  • Christiansen, P., & Wroe, S. (2007). Bite forces and evolutionary adaptations to feeding ecology in carnivores. Ecology, 88, 347-358.
  • Cobb, S. E. & Sellers, W. I. (2020). Inferring lifestyle for Aves and Theropoda: a model based on curvatures of extant avian ungual bones. PloS ONE, 15, e0211173.
  • Cohen, J. E., Pimm, S. L., Yodzis, P., & Saldana, J. (1993). Body sizes of animal predators and animal prey in food webs. Journal of Animal Ecology, 62, 67-78.
  • Collins P. W., Guthrie, D. A., Rick, T. C., & Erlandson, J. M. (2010). Analysis of prey remains excavated from an historic bald eagle nest site on San Miguel Island, California. Proceedings of the Sixth California Islands Symposium. Arcata, CA: Institute for Wildlife Studies: 103-120.
  • Costa, G. C. (2009). Predator size, prey size, and dietary niche breadth relationships in marine predators. Ecology, 90, 2014-2019.
  • Currie, P. J., & Chen, P. (2001) Anatomy of Sinosauropteryx prima from Liaoning, northeastern China. Canadian Journal of Earth Sciences, 38, 1705-1727. https://doi.org/10.1139/e01-050
  • Currie, P. J. & Evans, D. C. (2020). Cranial anatomy of new specimens of Saurornitholestes langstoni (Dinosauria,Theropoda, Dromaeosauridae) from the Dinosaur Park Formation (Campanian) of Alberta. Anatomical Record, 303, 691-715.
  • Currie, P. J. & Jacobsen. A. R. (1995): An azhdarchid pterosaur eaten by a velociraptorine theropod. Canadian Journal of Earth Sciences, 32, 922-925.
  • Dal Sasso, C., & Maganuco, S. (2011). Scipionyx samniticus (Theropoda: Compsognathidae) from the Lower Cretaceous of Italy. Memorie della Societa Italiana di Scienze Naturali e del Museo Civico di Storia Naturale di Milano, 37, 1-281.
  • Dececchi, T. A., & Larsson, H. C. E. (2011). Assessing arboreal adaptations of bird antecedents: testing the ecological setting of the origin of the avian flight stroke. PLoS ONE, 6, e22292.
  • Dececchi, T. A., Larsson, H. C. E., & Habib, M. B. (2016). The wings before the bird: an evaluation of flapping-based locomotory hypotheses in bird antecedents. PeerJ, 4, e2159.
  • Dececchi, T. A., Larsson, H. C. E., Pittman, M. & Habib, M. B. (2020a). High flyer or high fashion? A comparison of flight potential among small bodied paravians. Bulletin of the American Museum of Natural History, 420, 295-320.
  • Dececchi, T. A., Mloszewska, A. M., Holtz, T. R., Habib, M. B., & Larsson, H. C. E. (2020b). The fast and the frugal: Divergent locomotory strategies drive limb lengthening in theropod dinosaurs. PLoS ONE, 15, e0223698.
  • Dececchi, T. A., Roy, A., Pittman, M., Kaye, T. G., Xu, X., Habib, M. B., Larsson, H.C.E., Wang, X., & Zhang, X. (2020c). Aerodynamics show membrane-winged were a poor gliding dead-end. iScience, 23, 101574.
  • DeVault, T. L., Rhodes, Jr. O. E., & Shivik, J. A. (2003). Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos, 102, 225-234.
  • Dodson, P. (1975). Functional and ecological significance of relative growth in Alligator. Journal of Zoology, 175, 315-355.
  • Dyke, G., De Kat, R., Palmer, C., Van Der Kindere, J., Naish, D., & Ganapathisubramani, B. (2013). Aerodynamic performance of the feathered dinosaur Microraptor and the evolution of feathered flight. Nature Communications, 4, 1-9.
  • Evans, S. E., & Wang, Y. (2010). A new lizard (Reptilia: Squamata) with exquisite preservation of soft tissue from the Lower Cretaceous of Inner Mongolia, China. Journal of Systematic Palaeontology, 8, 81-95.
  • Farhadinia, M. S., Hosseini-Zavarei, F., Nezami, B., Harati, H., Absalan, H., Fabiano, E., & Marker, L. (2012). Feeding ecology of the Asiatic cheetah Acinonyx jubatus venaticus in low prey habitats in northeastern Iran: Implications for effective conservation. Journal of Arid Environments, 87, 206-211.
  • Fiorillo, A. R. (1991). Prey bone utilisation by predatory dinosaurs. Palaeogeography, Palaeoclimatology, Palaeoecology, 88, 157-166.
  • Fowler, D. W., Freedman, E. A., Scannella, J. B., & Kambic, R. E. (2011). The predatory ecology of Deinonychus and the origin of flapping in birds. PLoS ONE, 6, e28964.
  • Frederickson, J. A., Engel, M. H., & Cifelli, R. L. (2020). Ontogenetic dietary shifts in Deinonychus antirrhopus (Theropoda; Dromaeosauridae): Insights into the ecology and social behavior of raptorial dinosaurs through stable isotope analysis. Palaeogeography, Palaeoclimatology, Palaeoecology, 552, 109780.
  • Freimuth, W. J., Varricchio, D. J., Brannick, A. L., Weaver, L. N. & Wilson Mantilla, G. P. (2021). Mammal-bearing gastric pellets potentially attributable to Troodon formosus at the Cretaceous Egg Mountain locality, Two Medicine Formation, Montana, USA. Palaeontology, 64, 699-725.
  • Holtz, T. R., (2003). Dinosaur predation. In P. H. Kelley, M. Kowalewski, and T. A. Hansen. Predator-Prey Interactions in the Fossil Record (pp. 325-340). Springer.
  • Hone, D., Tsuihiji, T., Watabe, M., & Tsogtbaatr, K. (2012). Pterosaurs as a food source for small dromaeosaurs. Palaeogeography, Palaeoclimatology, Palaeoecology, 331, 27-30.
  • Hone, D. W., & Rauhut, O. W. (2010). Feeding behaviour and bone utilization by theropod dinosaurs. Lethaia, 43, 232-244.
  • Hone, D. W., & Watabe, M. (2010). New information on scavenging and selective feeding behaviour of tyrannosaurids. Acta Palaeontologica Polonica, 55, 627-635.
  • Hone, D. W. E., Choiniere, J., Sullivan, C., Xu, W., Pittman, M., & Tan, Q. (2010). New evidence for a trophic relationship between the dinosaurs Velociraptor and Protoceratops. Palaeogeography, Palaeoclimatology, Palaeoecology, 291, 488-492.
  • Hone, D. W. E., & Holtz Jr., T. R. (2017). A century of spinosaurs-a review and revision of the Spinosauridae with comments on their ecology. Acta Geologica Sinica-English Edition, 91, 1120-1132.
  • Hone, D. W. E., & Tanke, D. H. (2015). Pre-and postmortem tyrannosaurid bite marks on the remains of Daspletosaurus (Tyrannosaurinae: Theropoda) from Dinosaur Provincial Park, Alberta, Canada. PeerJ, 3: e885.
  • Hwang, S. H., Norell, M. A., Qiang, J., & Keqin, G. (2004). A large compsognathid from the Early Cretaceous Yixian Formation of China. Journal of Systematic Palaeontology, 2, 13-30.
  • Jacobsen, A. R. (1998) Feeding behavior of carnivorous dinosaurs as determined by tooth marks on dinosaur bones. Historical Biology, 13, 17-26.
  • Ji, Q., & Ji, S. A. (1997). Advance in the study of the avian Sinosauropteryx prima. Chinese Geology, 242, 30-32.
  • Ji, S. A., Ji, Q., Lu, J., & Yuan, C. (2007). A new giant compsognathid dinosaur with long filamentous integuments from Lower Cretaceous of Northeastern China. Acta Geologica Sinica, 81, 8-15.
  • Kiat, Y., Balaban, A., Sapir, N., O' Connor, J. K., & Xu, A. (2020). Sequential molt in a feathered dinosaur and implications for early paravian ecology and locomotion. Current Biology, 30, 18.
  • Kozlowski, J., & Gawelczyk, A. T. (2002). Why are species' body size distributions usually skewed to the right? Functional Ecology, 16, 419-432.
  • Lariviere, S., & Pasitschniak-Arts, M. (1996). Vulpes vulpes. Mammal Species, 537, 1-11.
  • Larsson, H. C. E., Hone, D. W. E., Dececchi, T.A., Sullivan, C., & Xu, X. (2010). The winged non-avian dinosaur Microraptor fed on mammals: implications for the Jehol Biota ecosystems. Journal of Vertebrate Paleontology, 30A, 39.
  • Leakey, L. N., Milledge, S. A. H., Leakey, S. M., Edung, J., Haynes, P., Kiptoo, D. K., & McGeorge, A. (1999). Diet of striped hyaena in northern Kenya. African Journal of Ecology, 37, 314-326.
  • Li, Q., Gao, K. Q., Meng, Q., Clarke, J. A., Shawkey, M. D., D' Alba, L., Pei, R., Ellison, M., Norell, M. A., & Vinther, J. (2012). Reconstruction of Microraptor and the evolution of iridescent plumage. Science, 335, 1215-1219.
  • Luo, Z. X., Ji, Q., Wible, J. R., & Yuan, C. X. (2003). An Early Cretaceous tribosphenic mammal and metatherian evolution. Science, 302, 1934-1940.
  • Maxwell, W. D., & Ostrom, J. A. (1995). Taphonomy and paleobiological implications of Tenontosaurus-Deinonychus associations. Journal of Vertebrate Paleontology, 15, 707-712.
  • Meng, Q. J., Grossnickle, D., Liu, D., Zhang, Y. G., Neander, A. I., Ji, Q., & Luo, Z. X. (2017). New gliding mammaliaforms from the Jurassic. Nature, 548, 291-296.
  • Meri, S. (2010). Length-weight allometries in lizards. Journal of Zoology, 281, 218-226.
  • Messel, H. & Vorlicek, G. C. (1989). Ecology of Crocodylus porosus in northern Australia. In Crocodiles: their ecology, management and conservation (pp.164-183). IUCN.
  • Morse, D. R., Lawton, J. H., Dodson, M. M., & Williamson, M. H. (1985). Fractal dimension of vegetation and the distribution of arthropod body lengths. Nature, 314, 731-733.
  • Mrykalo, R. J., Grigione, M. M., & Sarno, R. J. (2009). A comparison of available prey and diet of Florida Burrowing Owls in urban and rural environments: a first study. The Condor, 111, 556-559.
  • Naish, D. (2000). Theropod dinosaurs in the trees: a historical review of arboreal habits amongst nonavian theropods. Archaeopteryx, 18, 35-41.
  • Nesbitt, S. J., Turner, A. H., Erickson, G. M., & Norell, M. A. (2006). Prey choice and cannibalistic behaviour in the theropod Coelophysis. Biology Letters, 2, 611-614.
  • Nielsen, J. M., Clare, E. L., Hayden, B., Brett, M. T., & Kratina, P. (2018). Diet tracing in ecology: Method comparison and selection. Methods in Ecology and Evolution, 9, 278-291.
  • Norell, M. A., Clark, J. M., Turner, A. H., Makovicky, P. J., Barsbold, R., & Rowe, T. (2006). A new dromaeosaurid theropod from Ukhaa Tolgod (Omnogov, Mongolia). American Museum Novitates, 3545, 1-51.
  • O' Connor, J., Zheng, X., Dong, L., Wang, X., Wang, Y., Zhang, X., & Zhou, Z. (2019). Microraptor with ingested lizard suggests nonspecialized digestive function. Current Biology, 29, 2423-2429.
  • O' Connor, J., Zhou, Z., & Xu, X. (2011). Additional specimen of Microraptor provides unique evidence of dinosaurs preying on birds. Proceedings of the National Academy of Sciences, 108, 19662-19665.
  • O' Gorman, E. J., & Hone, D. W. (2012). Body size distribution of the dinosaurs. PloS ONE, 7, e51925.
  • Ostrom, J. H. (1964). A functional analysis of jaw mechanics in the dinosaur Triceratops. Postilla, 88, 1-35.
  • Ostrom, J. H. (1978). The osteology of Compsognathus longipes Wagner. Zitteliana, 4, 73-118.
  • Pei, R., Li, Q., Meng, Q., Gao, K. Q., & Norell, M. A. (2014). A new specimen of Microraptor (Theropoda: Dromaeosauridae) from the Lower Cretaceous of western Liaoning, China. American Museum Novitates, 3821, 1-28.
  • Pei, R., Pittman, M., Goloboff, P. A., Dececchi, T. A., Habib, M. B., Kaye, T. G., Larsson, H. C. E., Norell, M. A., Brusatte, S. L., & Xu, X. (2020). Potential for powered flight neared by most close avialan relatives, but few crossed its thresholds. Current Biology, 30, 4033-4046.
  • Powers, M. J., Sullivan, C., & Currie, P. J. (2020). Re-examining ratio based premaxillary and maxillary characters in Eudromaeosauria (Dinosauria: Theropoda): Divergent trends in snout morphology between Asian and North American taxa. Palaeogeography, Palaeoclimatology, Palaeoecology, 547, 109704.
  • Preuschoft, H., & Witzel, U. (2002). Biomechanical investigations on the skulls of reptiles and mammals. Senckenbergiana Lethaea, 82, 207-222.
  • Radloff, F. G. & Du Toit, J. T. (2004). Large predators and their prey in a southern African savanna: a predator' s size determines its prey size range. Journal of Animal Ecology, 73, 410-423.
  • Roach, B. T., & Brinkman, D. L. (2007). A reevaluation of cooperative pack hunting and gregariousness in Deinonychus antirrhopus and other nonavian theropod dinosaurs. Bulletin of the Peabody Museum of Natural History, 48, 103-138.
  • Sakamoto, M., Lloyd, G. T., & Benton, M. J. (2010). Phylogenetically structured variance in felid bite force: the role of phylogeny in the evolution of biting performance. Journal of Evolutionary Biology, 23, 463-478.
  • Samuels, J.X., & Van Valkenburgh, B. (2008). Skeletal indicators of locomotor adaptations in living and extinct rodents. Journal of Morphology, 269, 1387-1411.
  • Schmitz, L., & Motani, R. (2011). Nocturnality in dinosaurs inferred from scleral ring and orbit morphology. Science, 332, 705-708.
  • Slater, G. J., Dumont, E. R., & Van Valkenburgh, B. (2009). Implications of predatory specialization for cranial form and function in canids. Journal of Zoology, 278, 181-188.
  • Therrien, F. (2005). Mandibular force profiles of extant carnivorans and implications for the feeding behaviour of extinct predators. Journal of Zoology, 267, 249-270.
  • Therrien, F., Henderson, D. M., & Ruff, C. B. (2005). Bite me: biomechanical models of theropod mandibles and implications for feeding behavior. In K. Carpenter (Ed.), The Carnivorous Dinosaurs (pp. 179- 237). Indiana University Press.
  • Therrien, F., Zelenitsky, D. K., Voris, J. T., & Tanaka, K. (2021). Mandibular force profiles and tooth morphology in growth series of Albertosaurus sarcophagus and Gorgosaurus libratus (Tyrannosauridae: Albertosaurinae) provide evidence for an ontogenetic dietary shift in tyrannosaurids. Canadian Journal of Earth Sciences, 58, 812-828.
  • Thomason, J. J. (1991). Cranial strength in relation to estimated biting forces in some mammals. Canadian Journal of Zoology, 69, 2326- 2333.
  • Varricchio, D. J., (2001). Gut contents from a Cretaceous tyrannosaurid: implications for theropod dinosaur digestive tracts. Journal of Paleontology, 75, 401-406.
  • Vezina, A. F. (1985). Empirical relationships between predator and prey size among terrestrial vertebrate predators. Oecologia, 67, 555-565.
  • Walmsley, C. W., Smits, P. D., Quayle, M. R., McCurry, M. R., Richards, H. S., Oldfield, C. C., Wroe, S., Clausen, P. D., & McHenry, C. R. (2013). Why the long face? The mechanics of mandibular symphysis proportions in crocodiles. PLoS ONE, 8, e53873.
  • Wang, M., O' Connor, J. K., Xu, X., & Zhou, Z. (2019). A new Jurassic scansoriopterygid and the loss of membranous wings in theropod dinosaurs. Nature, 569, 256-259.
  • Wilson, J. P., Woodruff, D. C., Gardner, J. D., Flora, H. M., Horner, J. R., & Organ, C. L., (2016). Vertebral adaptations to large body size in theropod dinosaurs. PLoS ONE, 11, e0158962.
  • Woodroffe, R., Lindsey, P. A., Romanach, S. S., & Ranah S. M. O. (2007). African wild dogs (Lycaon pictus) can subsist on small prey: implications for conservation. Journal of Mammalogy, 88, 181- 193.
  • Xing, L., Bell, P. R., Persons IV, W. S., Ji, S., Miyashita, T., Burns, M. E., Ji, Q., & Currie, P. J. (2012). Abdominal contents from two large Early Cretaceous compsognathids (Dinosauria: Theropoda) demonstrate feeding on confuciusornithids and dromaeosaurids. PLoS ONE, 7, e44012.
  • Xing, L., Persons IV, W. S., Bell, P. R., Xu, X., Zhang, J., Miyashita, T., Wang, F., & Currie, P. J., (2013). Piscivory in the feathered dinosaur Microraptor. Evolution, 67, 2441-2445.
  • Xu, X., Choiniere, J. N., Pittman, M., Tan, Q., Xiao, D., Li, Z., Tan, L., Clark, J. M., Norell, M. A., Hone, D. W. E., & Sullivan, C. (2010). A new dromaeosaurid (Dinosauria: Theropoda) from the Upper Cretaceous Wulansuhai Formation of Inner Mongolia, China. Zootaxa, 2403, 1-9.
  • Xu, X., Zhou, Z., & Wang, X. (2000). The smallest known non-avian theropod dinosaur. Nature, 408, 705-708.
  • Xu, X., Zhou, Z., Wang, X., Kuang, X., Zhang, F., & Du, X. (2003). Fourwinged dinosaurs from China. Nature, 421, 335-340.
  • Zheng, X., Wang, X., Sullivan, C., Zhang, X., Zhang, F., Wang, Y., Li, F., & Xu, X. (2018). Exceptional dinosaur fossils reveal early origin of avian-style digestion. Scientific Reports, 8, 14217.