Gizzard vs. teeth, it's a tie: Food-processing efficiency in herbivorous birds and mammals and implications for dinosaur feeding strategies

Paleobiology

Volumn 37, Issue 4, 2011, Pages 577-586

  Fritz, Julia ^a   Jürgen, Hummel ^b   Kienzle, Ellen ^a   Wings, Oliver ^c   Streich, W Jürgen ^d   Clauss, Marcus ^e  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c HUMBOLDT UNIVERSITY   (Germany)

^d LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^e UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BIRD; BODY MASS; COMPARATIVE STUDY; DATA SET; DINOSAUR; FEEDING BEHAVIOR; FOOD; FUNCTIONAL MORPHOLOGY; HERBIVORY; MAMMAL; PALEOECOLOGY; PALEOENVIRONMENT; PARTICLE SIZE; QUANTITATIVE ANALYSIS;

AVES; BOVIDAE; DINOSAURIA; MAMMALIA; ORNITHOPODA;

EID: 80052578873     PISSN: 00948373     EISSN: None     Source Type: Journal    
DOI: 10.1666/10031.1     Document Type: Article

References (94)

1. Amat, J. A. 1995. Effects of wintering greylag geese Anser anser on their Scirpus food plants. Ecography 18:155-163.
2. Amerah, A. M., R. G. Lentle, and V. Ravindran. 2007. Influence of feed form on gizzard morphology and particle size spectra of duodenal digesta in broiler chickens. Journal of Poultry Science 44:175-181. (Pubitemid 46741911)
3. Bakker, R. 1986. The dinosaur heresies. Longman Scientific and Technical, Harlow, U.K
4. Barboza, P. S., K. L. Parker, and I. D. Hume. 2009. Integrative wildlife nutrition. Springer, Berlin.
5. Benton, M. J. 1990. Phylogeny of the major tetrapod groups: morphological data and divergence dates. Journal of Molecular Evolution 30:409-424. (Pubitemid 20167647)
6. Benton, M. J., and J. M. Clark. 1988. Archosaur phylogeny and the relationships of the Crocodilia. Pp. 295-338 in M. J. Benton, ed.
7. Bjorndal, K. A., and A. B. Bolten. 1992. Body size and digestive efficiency in a herbivorous freshwater turtle: advantages of small bite size. Physiological Zoology 65:1028-1039. (Pubitemid 24410501)
8. Bjorndal, K. A., A. B. Bolten, and J. E. Moore. 1990. Digestive fermentation in herbivores: effect of food particle size. Physiological Zoology 63:710-721.
9. Brochu, C. A. 2001. Progress and future directions in archosaur phylogenetics. Paleontology 76:1185-1201. (Pubitemid 34271194)
10. Calvo, J. O. 1994. Jaw mechanics in sauropod dinosaurs. GAIA 10:183-193.
11. Cerda, I. A. 2008. Gastroliths in an ornithopod dinosaur. Acta Palaeontologica Polonica 53:351-355.
12. Cherney, J. H., D. J. R. Cherney, and D. R. Mertens. 1988. Fiber composition and digestion kinetics in grass stem internodes as influenced by particle size. Journal of Dairy Science 71:2112-2122.
13. Christiansen, P. 1996. The evidence for implications of gastroliths in sauropods. GAIA 12:1-7.
14. Clauss, M., and J. Hummel. 2005. The digestive performance of mammalian herbivores: why big may not be that much better. Mammal Review 35:174-187. (Pubitemid 40900014)
15. Clauss, M., M. Lechner-Doll, and W. J. Streich. 2002. Faecal particle size distribution in captive wild ruminants: an approach to the browser/grazer-dichotomy from the other end. Oecologia 131:343-349. (Pubitemid 36064421)
16. Clauss, M., R. Frey, B. Kiefer, M. Lechner-Doll, W. Loehlein, C. Polster, G. E. Rössner, and W. J. Streich. 2003. The maximum attainable body size of herbivorous mammals: morphophysio-logical constraints on foregut, and adaptations of hindgut fermenters. Oecologia 136:14-27. (Pubitemid 36837257)
17. Clauss, M., R. R. Hofmann, W. J. Streich, J. Fickel, and J. Hummel. 2008. Higher masseter mass in grazing than in browsing ruminants. Oecologia 157:377-385.
18. Clauss, M., C. Nunn, J. Fritz, and J. Hummel. 2009. Evidence for a tradeoff between retention time and chewing efficiency in large mammalian herbivores. Comparative Biochemistry and Physiology A 154:376-382.
19. Coe, M. J., D. L. Dilcher, J. O. Farlow, D. M. Jarzen, and D. A. Russell. 1987. Dinosaurs and land plants. Pp. 225-258 in E. M. Friis, W. G. Chaloner, and R. Crane, eds. The origins of angiosperms and their biological consequences. Cambridge University Press, Cambridge.
20. Cope, D. R., M. J. J. E. Loonen, J. M. Rowcliffe, and R. A. Pettifor. 1995. Larger barnacle geese (Branta leucopsis) are more efficient feeders: a possible mechanism for observed body size-fitness relationships. Journal of Zoology 265:37-42.
21. Copes, L. E., and G. T. Schwartz. 2010. The scale of it all: postcanine tooth size, the taxon-level effect, and the universality of Gould's scaling law. Paleobiology 36:188-203.
22. Corbet, P. S. 1960. The food of a sample of crocodiles (Crocodilus niloticus) from Lake Victoria. Proceedings of the Zoological Society of London 133:561-572.
23. Coria, R. A., and J. O. Calvo. 2002. A new iguanodontian ornithopod from Neuquen Basin, Patagonia, Argentina. Journal of Vertebrate Paleontology 22:503-509. (Pubitemid 35206044)
24. Coria, R. A., and L. Salgado. 1996. A basal iguanodontian (Ornithischia: Ornithopoda) from the Late Cretaceous of South America. Journal of Vertebrate Paleontology 16:445-457.
25. Cott, H. B. 1961. Scientific results of an enquiry into the ecology and economic status of the Nile crocodile (Crocodylus niloticus) in Uganda and Northern Rhodesia. Transactions of the Zoological Society of London 29:211-356.
26. Creighton, G. K. 1980. Static allometry of mammalian teeth and the correlation of tooth size and body size in contemporary mammals. Journal of Zoology 191:435-443.
27. Delany, M. F., and C. L. Abercrombie. 1986. American alligator food habits in northcentral Florida. Journal of Wildlife Management 50:348-353. (Pubitemid 17250345)
28. Diefenbach, C. O. 1975. Gastric function in Caiman crocodilus. 1. Rate of gastric digestion and gastric motility as a function of temperature. Comparative Biochemistry and Physiology A 51:259-265.
29. Drobney, R. 1984. Effect of diet on visceral morphology of breeding wood ducks. Auk 101:93-98.
30. Duke, G. E. 1997. Gastrointestinal physiology and nutrition in wild birds. Proceedings of the Nutrition Society 56:1049-1056. (Pubitemid 127760014)
31. Durant, D., H. Fritz, S. Blais, and P. Duncan. 2003. The functional response in three species of herbivorous Anatidae: effects of sward height, body mass and bill size. Journal of Animal Ecology 72:220-231. (Pubitemid 36412984)
32. Durant, D., L. Desnouches, H. Fritz, M. Guillemain, and F. Mesléard. 2009. Size-related consumption of Scirpus maritimus tubers by greylag geese Anser anser explained by their functional response. Behavioural Processes 80:39-45.
33. Farlow, J. O. 1987. Speculations about the diet and digestive physiology of herbivorous dinosaurs. Paleobiology 13:60-72. (Pubitemid 17264200)
34. Fortelius, M. 1986. Isometric scaling of mammalian cheek teeth is also true metabolic scaling. Pp. in D. E. Russell, J.-P. Santoro, and D. Sigogneau-Russell, eds. Teeth revisited. Proceedings of the VIIth International Symposium on Dental Morphology. Mém-oires du Museum National d'Histoire Naturelle C 53:459-462.
35. -1987. A note on the scaling of dental wear. Evolutionary Theory 8:73-75.
36. Franz, R., J. Hummel, E. Kienzle, P. Kölle, H. C. Gunga, and M. Clauss. 2009. Allometry of visceral organs in living amniotes and its implications for sauropod dinosaurs. Proceedings of the Royal Society B 276:1731-1736.
37. Franz, R., J. Hummel, D. W. H. Mü ller, M. Bauert, J.-M. Hatt, and M. Clauss. 2011. Herbivorous reptiles and body mass: effects on food intake, digesta retention, digestibility and gut capacity, and a comparison with mammals. Comparative Biochemistry and Physiology A 158:94-101.
38. Fritz, J., J. Hummel, E. Kienzle, C. Arnold, C. Nunn, and M. Clauss. 2009. Comparative chewing efficiency in mammalian herbivores. Oikos 118:1623-1632.
39. Fritz, J., J. Hummel, E. Kienzle, W. J. Streich, and M. Clauss. 2010. To chew or not to chew: faecal particle size in herbivorous reptiles and mammals. Journal of Experimental Zoology A 313:579-586.
40. Gauthier, J. 1986. Saurischian monophyly and the origin of birds. In K. Padian, ed. The origin of birds and the evolution of flight. California Academy of Sciences Memoir 8:1-55. San Francisco.
41. Gionfriddo, J. P., and L. B. Best. 1996. Grit-use patterns in North American birds: the influence of diet, body size, and gender. Wilson Bulletin 108:658-696.
42. -1999. Grit use by birds-a review. Current Ornithology 15:89-148.
43. Gould, S. J. 1975. On the scaling of tooth size in mammals. American Zoologist 15:351-362.
44. Herd, R., and T. Dawson. 1984. Fibre digestion in the emu, Dromaius novaehollandiae, a large bird with a simple gut and high rates of passage. Physiological Zoology 57:70-84.
45. Horner, J. R., A. de Ricqlès, and K. Padian. 2000. Long bone histology of the hadrosaurid dinosaur Maiasaura peeblesorum: growth dynamics and physiology based on an ontogenetic series of skeletal elements. Journal of Vertebrate Paleontology 20:115-129.
46. Hummel, J., J. Fritz, E. Kienzle, E. P. Medici, S. Lang, W. Zimmermann, W. J. Streich, and M. Clauss. 2008. Differences in fecal particle size between free-ranging and captive individuals of two browser species. Zoo Biology 27:70-77. (Pubitemid 351405402)
47. Hummel, J., and M. Clauss. 2011. Feeding and digestive physiology. Pp. 11-33 in N. Klein, K. Remes, C. T. Gee, and M. Sander, eds. Understanding the life of giants. The biologyofthe sauropod dinosaurs. Indiana University Press, Bloomington.
48. Janis, C. M. 1988. An estimation of tooth volume and hypsodonty indices in ungulate mammals and the correlation of these factors with dietary preferences. In D. E. Russell, J.-P. Santoro, and D. Sigogneau-Russell, eds. Teeth revisited. Proceedings of the VIIth International Symposium on Dental Morphology. Mémoires du Muséum National d'Histoire Naturelle C 53:367-387.
49. Ji, Q., P. J. Currie, M. A. Norell, and S. A. Ji. 1998. Two feathered dinosaurs from northeastern China. Nature 393:753-761. (Pubitemid 28299479)
50. Ji, Q., M.A. Norell, P.J. Makovicky, K. Q. Gao, S. A.Ji, andC. Yuan. 2003. An early ostrich dinosaur and implications for ornithomi-mosaur phylogeny. American Museum Novitates 3420:1-19.
51. Karasov, W. H., E. Petrossian, L. Rosenberg, and J. M. Diamond. 1986. How do food passage rate and assimilation differ between herbivorous lizards and nonruminant mammals? Journal of Comparative Physiology B 156:599-609.
52. Kobayashi, Y., and J. C. Lü. 2003. A new ornithomimid dinosaur with gregarious habits from the Late Cretaceous of China. Acta Palaeontologica Polonica 48:235-259. (Pubitemid 36906194)
53. Lucas, P. W. 2004. Dental functional morphology: how teeth work. Cambridge University Press, Cambridge.
54. Mackie, R. 2002. Mutualistic fermentative digestion in the gastrointestinal tract: diversity and evolution. Integrative and Comparative Biology 42:319-326.
55. McNab, B. K. 2008. An analysis of the factors that influence the level and scaling of mammalian BMR. Comparative Biochemistry and Physiology A 151:5-28.
56. -2009. Ecological factors affect the level and scaling of avian BMR. Comparative Biochemistry and Physiology A 152:22-45.
57. Moore, S. J. 1998a. The comparative functional gizzard morphology of several species of birds. Australian Journal of Zoology 46:359-368. (Pubitemid 29073129)
58. -1998b. Use ofan artificial gizzardtoinvestigate the effect of grit on the breakdown of grass. Journal of Zoology 246:119-124. (Pubitemid 28486086)
59. -1999. Food breakdown in an avian herbivore: who needs teeth? Australian Journal of Zoology 47:625-632. (Pubitemid 30028166)
60. Pauwels, O. S. G., B. Barr, M. L. Sanchez, and M. Burger. 2007. Diet records for the dwarf crocodile (Osteolaemus tetraspis tetraspis) in Rabi Oil Fields and Loango National Park, Southwestern Gabon. Hamadryad 31:258-264.
61. Pendergast, B., and D. Boag. 1973. Seasonal changes in the internal anatomy of spruce grouse in Alberta. Auk 90:307-317.
62. Piersma, T., A. Koolhaas, and A. Dekinga. 1993. Interactions between stomach structure and diet choice in shorebirds. Auk 110:552-564.
63. Platt, S. G., T. R. Rainwater, A. G. Finger, J. B. Thorbjarnarson, T. A. Anderson, and S. T. McMurry. 2006. Food habits, ontogenetic dietary partitioning and observations of foraging behaviour of Morelet's crocodile (Crocodylus moreletti) in northern Belize. Herpetological Journal 16:281-290. (Pubitemid 46524284)
64. Popowics, T. E., and M. Fortelius. 1997. On the cutting edge: tooth blade sharpness in herbivorous and faunivorous mammals. Annales Zoologici Fennici 34:73-88. (Pubitemid 27389485)
65. Potter, M. A., R. G. Lentle, C. J. Minson, M. J. Birtles, D. Thomas, and W. H. Hendriks. 2006. Gastrointestinal tract of the brown kiwi (Apteryx mantelli). Journal of Zoology 270:429-436. (Pubitemid 44581603)
66. Redelstorff, R., and P. M. Sander. 2009. Long and girdle bone histology of Stegosaurus: implications for growth and life history. Journal of Vertebrate Paleontology 29:1087-1099.
67. Reilly, S. M., L. D. McBrayer, and T. D. White. 2001. Prey processing in amniotes: biomechanical and behavioral patterns of food reduction. Comparative Biochemistry and Physiology A 128:397-415. (Pubitemid 32200400)
68. Sander, P. M., A. Christian, M. Clauss, R. Fechner, C. T. Gee, E. M. Griebeler, H. C. Gunga, J. Hummel, H. Mallison, S. F. Perry, H. Preuschoft, O. W. M. Rauhut, K. Remes, T. Tütken, O. Wings, and U. Witzel. 2011. Biology of the sauropod dinosaurs: the evolution of gigantism. Biological Reviews 86:117-155.
69. Schwarz, D., T. Ikejiri, B. H. Breithaupt, P. M. Sander, and N. Klein. 2007. A nearly complete skeleton of an early juvenile diplodocid (Dinosauria: Sauropoda) from the Lower Morrison Formation (Late Jurassic) of north central Wyoming and its implications for early ontogeny and pneumaticity in sauro-pods. Historical Biology 19:225-253. (Pubitemid 46930221)
70. Schwenk, K., and M. Rubega. 2005. Diversity of vertebrate feeding systems. Pp. 1-41 in J. M. Starck and T. Wang, eds. Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, N.H.
71. Sereno, P. C., Z. Xijin, and T. Lin. 2010. A new psittacosaur from Inner Mongolia and the parrot-like structure and function of the psittacosaur skull. Proceedings of the Royal Society of London B 277:199-209.
72. Skoczylas, R. 1978. Physiology of the digestive tract. Pp. 589-717 in C. Gans, and K. A. Gans, eds. Biology of the Reptilia. Academic Press, London.
73. Starck, J. M. 1999. Phenotypic flexibility of the avian gizzard: rapid, reversible and repeated changes of organ size in response to changes in dietary fibre content. Journal of Experimental Biology 202:775-785.
74. Stein, M., and M. Sander. 2009. Long bone histology and growth patterns in ankylosaurs. Journal of Vertebrate Paleontology 29:185A.
75. Stevens, C. E., and I. D. Hume. 1995. Comparative physiology of the vertebrate digestive system. Cambridge University Press, Cambridge.
76. Taggart, R. E., and A. T. Cross. 1997. The relationship between land plant diversity and productivity and patterns of dinosaur herbivory. Pp. 403-416 in D. L. Wolberg, E. Stump, and G. Rosenberg, eds. Dinofest International: proceedings of a symposium held at Arizona State University. National Academy of Natural Sciences, Philadelphia.
77. Throckmorton, G. S. 1976. Oral food processing in two herbivorous lizards, Iguana iguana (Iguanidae) and Uromastix aegypti-cus (Agamidae). Journal of Morphology 148:363-390.
78. Upchurch, P., and P. M. Barrett. 2000. The evolution of sauropod feeding mechanisms. Pp. 79-122 in H. D. Sues, ed. Evolution of herbivory in terrestrial vertebrates: perspectives from the fossil record. Cambridge University Press, Cambridge.
79. Van der Graaf, A. J., P. Coehoorn, and J. Stahl. 2006. Sward height and bite size affect the functional response of barnacle geese Branta leucopsis. Journal of Ornithology 147:479-484. (Pubitemid 44288448)
80. Varricchio, D. J. 2001. Gut contents from a cretaceous tyranno-saurid: implications for theropod dinosaur digestive tracts. Journal of Paleontology 75:401-406. (Pubitemid 32382847)
81. Veiberg, V., A. Mysterud, J. M. Gaillard, D. Delorme, G. Van Laere, and F. Klein. 2007. Bigger teeth for longer life? Longevity and molar height in two roe deer populations. Biology Letters 3:268-270.
82. Wallace, K. M., and A. J. Leslie. 2008. Diet of the Nile crocodile (Crocodylus niloticus) in the Okavango Delta, Botswana. Journal of Herpetology 42:361-368. (Pubitemid 351786806)
83. Weishampel, D. B., and D. B. Norman. 1989. Vertebrate herbivory in the Mesozoic; jaws, plants, and evolutionary metrics. In J. O. Farlow, ed. Paleobiology of the dinosaurs. Geological Society of America Special Paper 238:87-100.
84. Western, D., and J. Ssemakula. 1982. Life history patterns in birds and mammals and their evolutionary interpretation. Oecologia 54:281-290. (Pubitemid 13285497)
85. Williams, S. H., and R. F. Kay. 2001. A comparative test of adaptive explanations for hypsodonty in ungulates and rodents. Journal of Mammalian Evolution 8:207-229. (Pubitemid 33815230)
86. Wing, S. L., H. D. Sues, B. H. Tiffney, R. K. Stucky, D. B. Weishampel, R. A. Spicer, D. Jablonski, C. E. Badgley, M. V. H. Wilson, and W. L. Kovach. 1992. Mesozoic and early Cenozoic terrestrial ecosystems. Pp. 327-416 in A. K. Behrensmeyer, J. D. Damuth, W. A. DiMichele, R. Potts, H. D. Sues, and S. L. Wing, eds. Terrestrial ecosystems through time: evolutionary paleo-ecology of plants and animals. University of Chicago Press, Chicago.
87. Wings, O. 2004. Identification, distribution, and function of gastroliths in dinosaurs and extant birds with emphasis on ostriches (Struthio camelus). Dissertation thesis, University of Bonn, Germany.
88. -2007. A review of gastrolith function with implications for fossil vertebrates and a revised classification. Acta Palaeonto-logica Polonica 52:1-16. (Pubitemid 46510666)
89. Wings, O., and P. M. Sander. 2007. No gastric mill in sauropod dinosaurs: new evidence from analysis of gastrolith mass and function in ostriches. Proceedings of the Royal Society of London B 274:635-640. (Pubitemid 47056778)
90. Worthy, T. H., and R. N. Holdaway. 2002. The lost world of the moa: prehistoric life of New Zealand. Indiana University Press, Bloomington.
91. Xu, X., C. Forster, J. Clark, and J. Mo. 2006. A basal ceratopsian with transitional features from the Late Jurassic of northwestern China. Proceedings of the Royal Society B 273:2135-2140. (Pubitemid 44318302)
92. Xu, X., J. M. Clark, J. Mo, J. Choiniere, C. A. Forster, G. M. Erickson, D. W. E. Hone, C. Sullivan, D. A. Eberth, S. Nesbitt, Q. Zhao, R. Hernandez, C. K. Jia, F. I. Han, and Y. Guo. 2009. A Jurassic ceratosaur from China helps clarify avian digital homologies. Nature 459:940-944.
93. You, H. L., and P. Dodson. 2004. Basal Ceratopsia. Pp. 478-493 in D. B. Weishampel, P. Dodson, and H. Osmólska, eds. The Dinosauria. University of California Press, Berkeley.
94. Zhou, Z.-H., and X.-L. Wang. 2000. A new species of Caudipteryx from the Yixian Formation of Liaoning, northeast China. Vertebrata PalAsiatica 38:111-127.