Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-19T01:40:44.114Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  08 April 2016

Julia Fritz
Affiliation:
Institute of Physiology, Physiological Chemistry and Animal Nutrition, Ludwig-Maximilians-University Munich, Schönleutnerstr. 8, 85764 Oberschleiβheim, Germany. E-mail: [email protected]
Jürgen Hummel
Affiliation:
Institute of Animal Science, Animal Nutrition Group, University of Bonn, Germany
Ellen Kienzle
Affiliation:
Institute of Physiology, Physiological Chemistry and Animal Nutrition, Ludwig-Maximilians-University Munich, Schönleutnerstr. 8, 85764 Oberschleiβheim, Germany
Oliver Wings
Affiliation:
Museum of Natural History, Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, Germany
W. Jürgen Streich
Affiliation:
Leibniz-Institute of Zoo and Wildlife Research Berlin, Germany
Marcus Clauss*
Affiliation:
Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Winterthurerstrasse 260, 8057 Zurich, Switzerland. E-mail: [email protected]
*
Corresponding author

Abstract

Particle size reduction is a primary means of improving efficiency in herbivores. The mode of food particle size reduction is one of the main differences between herbivorous birds (gizzard) and mammals (teeth). For a quantitative comparison of the efficiency of food comminution, we investigated mean fecal particle sizes (MPS) in 14 herbivorous bird species and compared these with a data set of 111 non-ruminant herbivorous mammal species. In general MPS increased with body mass, but there was no significant difference between birds and mammals, suggesting a comparable efficiency of food processing by gizzards and chewing teeth. The results lead to the intriguing question of why gizzard systems have evolved comparatively rarely among amniote herbivores. Advantages linked to one of the two food comminution systems must, however, be sought in different effects other than size reduction itself. In paleoecological scenarios, the evolution of “dental batteries,” for example in ornithopod dinosaurs, should be considered an advantage compared to absence of mastication, but not compared to gizzard-based herbivory.

Type
Articles
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Amat, J. A. 1995. Effects of wintering greylag geese Anser anser on their Scirpus food plants. Ecography 18:155163.Google Scholar
Amerah, A. M., Lentle, R. G., and Ravindran, V. 2007. Influence of feed form on gizzard morphology and particle size spectra of duodenal digesta in broiler chickens. Journal of Poultry Science 44:175181.Google Scholar
Bakker, R. 1986. The dinosaur heresies. Longman Scientific and Technical, Harlow, U.K.Google Scholar
Barboza, P. S., Parker, K. L., and Hume, I. D. 2009. Integrative wildlife nutrition. Springer, Berlin.Google Scholar
Benton, M. J. 1990. Phylogeny of the major tetrapod groups: morphological data and divergence dates. Journal of Molecular Evolution 30:409424.CrossRefGoogle ScholarPubMed
Benton, M. J., and Clark, J. M. 1988. Archosaur phylogeny and the relationships of the Crocodilia. Pp. 295338in Benton, M. J., ed. The phylogeny and classification of the tetrapods. Systematics Association, Oxford.Google Scholar
Bjorndal, K. A., and Bolten, A. B. 1992. Body size and digestive efficiency in a herbivorous freshwater turtle: advantages of small bite size. Physiological Zoology 65:10281039.Google Scholar
Bjorndal, K. A., Bolten, A. B., and Moore, J. E. 1990. Digestive fermentation in herbivores: effect of food particle size. Physiological Zoology 63:710721.Google Scholar
Brochu, C. A. 2001. Progress and future directions in archosaur phylogenetics. Paleontology 76:11851201.Google Scholar
Calvo, J. O. 1994. Jaw mechanics in sauropod dinosaurs. GAIA 10:183193.Google Scholar
Cerda, I. A. 2008. Gastroliths in an ornithopod dinosaur. Acta Palaeontologica Polonica 53:351355.Google Scholar
Cherney, J. H., Cherney, D. J. R., and Mertens, D. R. 1988. Fiber composition and digestion kinetics in grass stem internodes as influenced by particle size. Journal of Dairy Science 71:21122122.Google Scholar
Christiansen, P. 1996. The evidence for implications of gastroliths in sauropods. GAIA 12:17.Google Scholar
Clauss, M., and Hummel, J. 2005. The digestive performance of mammalian herbivores: why big may not be that much better. Mammal Review 35:174187.Google Scholar
Clauss, M., Lechner-Doll, M., and Streich, W. J. 2002. Faecal particle size distribution in captive wild ruminants: an approach to the browser/grazer-dichotomy from the other end. Oecologia 131:343349.CrossRefGoogle Scholar
Clauss, M., Frey, R., Kiefer, B., Lechner-Doll, M., Loehlein, W., Polster, C., Rössner, G. E., and Streich, W. J. 2003. The maximum attainable body size of herbivorous mammals: morphophysiological constraints on foregut, and adaptations of hindgut fermenters. Oecologia 136:1427.Google Scholar
Clauss, M., Hofmann, R. R., Streich, W. J., Fickel, J., and Hummel, J. 2008. Higher masseter mass in grazing than in browsing ruminants. Oecologia 157:377385.Google Scholar
Clauss, M., Nunn, C., Fritz, J., and Hummel, J. 2009. Evidence for a tradeoff between retention time and chewing efficiency in large mammalian herbivores. Comparative Biochemistry and Physiology A 154:376382.Google Scholar
Coe, M. J., Dilcher, D. L., Farlow, J. O., Jarzen, D. M., and Russell, D. A. 1987. Dinosaurs and land plants. Pp. 225258in Friis, E. M., Chaloner, W. G., and Crane, R., eds. The origins of angiosperms and their biological consequences. Cambridge University Press, Cambridge.Google Scholar
Cope, D. R., Loonen, M. J. J. E., Rowcliffe, J. M., and Pettifor, R. A. 1995. Larger barnacle geese (Branta leucopsis) are more efficient feeders: a possible mechanism for observed body size-fitness relationships. Journal of Zoology 265:3742.Google Scholar
Copes, L. E., and Schwartz, G. T. 2010. The scale of it all: postcanine tooth size, the taxon-level effect, and the universality of Gould's scaling law. Paleobiology 36:188203.Google Scholar
Corbet, P. S. 1960. The food of a sample of crocodiles (Crocodilus niloticus) from Lake Victoria. Proceedings of the Zoological Society of London 133:561572.Google Scholar
Coria, R. A., and Calvo, J. O. 2002. A new iguanodontian ornithopod from Neuquen Basin, Patagonia, Argentina. Journal of Vertebrate Paleontology 22:503509.Google Scholar
Coria, R. A., and Salgado, L. 1996. A basal iguanodontian (Ornithischia: Ornithopoda) from the Late Cretaceous of South America. Journal of Vertebrate Paleontology 16:445457.CrossRefGoogle Scholar
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 29:211356.Google Scholar
Creighton, G. K. 1980. Static allometry of mammalian teeth and the correlation of tooth size and body size in contemporary mammals. Journal of Zoology 191:435443.Google Scholar
Delany, M. F., and Abercrombie, C. L. 1986. American alligator food habits in northcentral Florida. Journal of Wildlife Management 50:348353.Google Scholar
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 51:259265.Google Scholar
Drobney, R. 1984. Effect of diet on visceral morphology of breeding wood ducks. Auk 101:9398.Google Scholar
Duke, G. E. 1997. Gastrointestinal physiology and nutrition in wild birds. Proceedings of the Nutrition Society 56:10491056.Google Scholar
Durant, D., Fritz, H., Blais, S., and Duncan, P. 2003. The functional response in three species of herbivorous Anatidae: effects of sward height, body mass and bill size. Journal of Animal Ecology 72:220231.Google Scholar
Durant, D., Desnouches, L., Fritz, H., Guillemain, M., and Mesléard, F. 2009. Size-related consumption of Scirpus maritimus tubers by greylag geese Anser anser explained by their functional response. Behavioural Processes 80:3945.Google Scholar
Farlow, J. O. 1987. Speculations about the diet and digestive physiology of herbivorous dinosaurs. Paleobiology 13:6072.Google Scholar
Fortelius, M. 1986. Isometric scaling of mammalian cheek teeth is also true metabolic scaling. Pp. in Russell, D. E., Santoro, J.-P., and Sigogneau-Russell, D., eds. Teeth revisited. Proceedings of the VIIth International Symposium on Dental Morphology. Mémoires du Museum National d'Histoire Naturelle C 53:459462.Google Scholar
Fortelius, M. 1987. A note on the scaling of dental wear. Evolutionary Theory 8:7375.Google Scholar
Franz, R., Hummel, J., Kienzle, E., Kölle, P., Gunga, H. C., and Clauss, M. 2009. Allometry of visceral organs in living amniotes and its implications for sauropod dinosaurs. Proceedings of the Royal Society B 276:17311736.CrossRefGoogle ScholarPubMed
Franz, R., Hummel, J., Müller, D. W. H., Bauert, M., Hatt, J.-M., and Clauss, M. 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 158:94101.CrossRefGoogle Scholar
Fritz, J., Hummel, J., Kienzle, E., Arnold, C., Nunn, C., and Clauss, M. 2009. Comparative chewing efficiency in mammalian herbivores. Oikos 118:16231632.CrossRefGoogle Scholar
Fritz, J., Hummel, J., Kienzle, E., Streich, W. J., and Clauss, M. 2010. To chew or not to chew: faecal particle size in herbivorous reptiles and mammals. Journal of Experimental Zoology A 313:579586.Google Scholar
Gauthier, J. 1986. Saurischian monophyly and the origin of birds. In Padian, K., ed. The origin of birds and the evolution of flight. California Academy of Sciences Memoir 8:155. San Francisco.Google Scholar
Gionfriddo, J. P., and Best, L. B. 1996. Grit-use patterns in North American birds: the influence of diet, body size, and gender. Wilson Bulletin 108:658696.Google Scholar
Gionfriddo, J. P., and Best, L. B. 1999. Grit use by birds—a review. Current Ornithology 15:89148.Google Scholar
Gould, S. J. 1975. On the scaling of tooth size in mammals. American Zoologist 15:351362.Google Scholar
Herd, R., and Dawson, T. 1984. Fibre digestion in the emu, Dromaius novaehollandiae, a large bird with a simple gut and high rates of passage. Physiological Zoology 57:7084.Google Scholar
Horner, J. R., de Ricqlès, A., and Padian, K. 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 20:115129.Google Scholar
Hummel, J., Fritz, J., Kienzle, E., Medici, E. P., Lang, S., Zimmermann, W., Streich, W. J., and Clauss, M. 2008. Differences in fecal particle size between free-ranging and captive individuals of two browser species. Zoo Biology 27:7077.Google Scholar
Hummel, J., and Clauss, M. 2011. Feeding and digestive physiology. Pp. 1133in Klein, N., Remes, K., Gee, C. T., and Sander, M., eds. Understanding the life of giants. The biology of the sauropod dinosaurs. Indiana University Press, Bloomington.Google Scholar
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 Russell, D. E., Santoro, J.-P., and Sigogneau-Russell, D., eds. Teeth revisited. Proceedings of the VIIth International Symposium on Dental Morphology. Mémoires du Museum National d'Histoire Naturelle C 53:367387.Google Scholar
Ji, Q., Currie, P. J., Norell, M. A., and Ji, S. A. 1998. Two feathered dinosaurs from northeastern China. Nature 393:753761.Google Scholar
Ji, Q., Norell, M. A., Makovicky, P. J., Gao, K. Q., Ji, S. A., and Yuan, C. 2003. An early ostrich dinosaur and implications for ornithomimosaur phylogeny. American Museum Novitates 3420:119.Google Scholar
Karasov, W. H., Petrossian, E., Rosenberg, L., and Diamond, J. M. 1986. How do food passage rate and assimilation differ between herbivorous lizards and nonruminant mammals? Journal of Comparative Physiology B 156:599609.Google Scholar
Kobayashi, Y., and , J. C. 2003. A new ornithomimid dinosaur with gregarious habits from the Late Cretaceous of China. Acta Palaeontologica Polonica 48:235259.Google Scholar
Lucas, P. W. 2004. Dental functional morphology: how teeth work. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Mackie, R. 2002. Mutualistic fermentative digestion in the gastrointestinal tract: diversity and evolution. Integrative and Comparative Biology 42:319326.Google Scholar
McNab, B. K. 2008. An analysis of the factors that influence the level and scaling of mammalian BMR. Comparative Biochemistry and Physiology A 151:528.Google Scholar
McNab, B. K. 2009. Ecological factors affect the level and scaling of avian BMR. Comparative Biochemistry and Physiology A 152:2245.CrossRefGoogle ScholarPubMed
Moore, S. J. 1998a. The comparative functional gizzard morphology of several species of birds. Australian Journal of Zoology 46:359368.Google Scholar
Moore, S. J. 1998b. Use of an artificial gizzard to investigate the effect of grit on the breakdown of grass. Journal of Zoology 246:119124.Google Scholar
Moore, S. J. 1999. Food breakdown in an avian herbivore: who needs teeth? Australian Journal of Zoology 47:625632.Google Scholar
Pauwels, O. S. G., Barr, B., Sanchez, M. L., and Burger, M. 2007. Diet records for the dwarf crocodile (Osteolaemus tetraspis tetraspis) in Rabi Oil Fields and Loango National Park, Southwestern Gabon. Hamadryad 31:258264.Google Scholar
Pendergast, B., and Boag, D. 1973. Seasonal changes in the internal anatomy of spruce grouse in Alberta. Auk 90:307317.Google Scholar
Piersma, T., Koolhaas, A., and Dekinga, A. 1993. Interactions between stomach structure and diet choice in shorebirds. Auk 110:552564.Google Scholar
Platt, S. G., Rainwater, T. R., Finger, A. G., Thorbjarnarson, J. B., Anderson, T. A., and McMurry, S. T. 2006. Food habits, ontogenetic dietary partitioning and observations of foraging behaviour of Morelet's crocodile (Crocodylus moreletti) in northern Belize. Herpetological Journal 16:281290.Google Scholar
Popowics, T. E., and Fortelius, M. 1997. On the cutting edge: tooth blade sharpness in herbivorous and faunivorous mammals. Annales Zoologici Fennici 34:7388.Google Scholar
Potter, M. A., Lentle, R. G., Minson, C. J., Birtles, M. J., Thomas, D., and Hendriks, W. H. 2006. Gastrointestinal tract of the brown kiwi (Apteryx mantelli). Journal of Zoology 270:429436.Google Scholar
Redelstorff, R., and Sander, P. M. 2009. Long and girdle bone histology of Stegosaurus: implications for growth and life history. Journal of Vertebrate Paleontology 29:10871099.Google Scholar
Reilly, S. M., McBrayer, L. D., and White, T. D. 2001. Prey processing in amniotes: biomechanical and behavioral patterns of food reduction. Comparative Biochemistry and Physiology A 128:397415.Google Scholar
Sander, P. M., Christian, A., Clauss, M., Fechner, R., Gee, C. T., Griebeler, E. M., Gunga, H. C., Hummel, J., Mallison, H., Perry, S. F., Preuschoft, H., Rauhut, O. W. M., Remes, K., Tütken, T., Wings, O., and Witzel, U. 2011. Biology of the sauropod dinosaurs: the evolution of gigantism. Biological Reviews 86:117155.Google Scholar
Schwarz, D., Ikejiri, T., Breithaupt, B. H., Sander, P. M., and Klein, N. 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 sauropods. Historical Biology 19:225253.CrossRefGoogle Scholar
Schwenk, K., and Rubega, M. 2005. Diversity of vertebrate feeding systems. Pp. 141in Starck, J. M. and Wang, T., eds. Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, N.H.Google Scholar
Sereno, P. C., Xijin, Z., and Lin, T. 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 277:199209.Google Scholar
Skoczylas, R. 1978. Physiology of the digestive tract. Pp. 589717in Gans, C., and Gans, K. A., eds. Biology of the Reptilia. Academic Press, London.Google Scholar
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 202:775785.Google Scholar
Stein, M., and Sander, M. 2009. Long bone histology and growth patterns in ankylosaurs. Journal of Vertebrate Paleontology 29:185A.Google Scholar
Stevens, C. E., and Hume, I. D. 1995. Comparative physiology of the vertebrate digestive system. Cambridge University Press, Cambridge.Google Scholar
Taggart, R. E., and Cross, A. T. 1997. The relationship between land plant diversity and productivity and patterns of dinosaur herbivory. Pp. 403416in Wolberg, D. L., Stump, E., and Rosenberg, G., eds. Dinofest International: proceedings of a symposium held at Arizona State University. National Academy of Natural Sciences, Philadelphia.Google Scholar
Throckmorton, G. S. 1976. Oral food processing in two herbivorous lizards, Iguana iguana (Iguanidae) and Uromastix aegypticus (Agamidae). Journal of Morphology 148:363390.Google Scholar
Upchurch, P., and Barrett, P. M. 2000. The evolution of sauropod feeding mechanisms. Pp. 79122in Sues, H. D., ed. Evolution of herbivory in terrestrial vertebrates: perspectives from the fossil record. Cambridge University Press, Cambridge.Google Scholar
Van der Graaf, A. J., Coehoorn, P., and Stahl, J. 2006. Sward height and bite size affect the functional response of barnacle geese Branta leucopsis. Journal of Ornithology 147:479484.Google Scholar
Varricchio, D. J. 2001. Gut contents from a cretaceous tyrannosaurid: implications for theropod dinosaur digestive tracts. Journal of Paleontology 75:401406.Google Scholar
Veiberg, V., Mysterud, A., Gaillard, J. M., Delorme, D., Van Laere, G., and Klein, F. 2007. Bigger teeth for longer life? Longevity and molar height in two roe deer populations. Biology Letters 3:268270.Google Scholar
Wallace, K. M., and Leslie, A. J. 2008. Diet of the Nile crocodile (Crocodylus niloticus) in the Okavango Delta, Botswana. Journal of Herpetology 42:361368.Google Scholar
Weishampel, D. B., and Norman, D. B. 1989. Vertebrate herbivory in the Mesozoic; jaws, plants, and evolutionary metrics. In Farlow, J. O., ed. Paleobiology of the dinosaurs. Geological Society of America Special Paper 238:87100.Google Scholar
Western, D., and Ssemakula, J. 1982. Life history patterns in birds and mammals and their evolutionary interpretation. Oecologia 54:281290.Google Scholar
Williams, S. H., and Kay, R. F. 2001. A comparative test of adaptive explanations for hypsodonty in ungulates and rodents. Journal of Mammalian Evolution 8:207229.Google Scholar
Wing, S. L., Sues, H. D., Tiffney, B. H., Stucky, R. K., Weishampel, D. B., Spicer, R. A., Jablonski, D., Badgley, C. E., Wilson, M. V. H., and Kovach, W. L. 1992. Mesozoic and early Cenozoic terrestrial ecosystems. Pp. 327416in Behrensmeyer, A. K., Damuth, J. D., DiMichele, W. A., Potts, R., Sues, H. D., and Wing, S. L., eds. Terrestrial ecosystems through time: evolutionary paleoecology of plants and animals. University of Chicago Press, Chicago.Google Scholar
Wings, O. 2004. Identification, distribution, and function of gastroliths in dinosaurs and extant birds with emphasis on ostriches (Struthio camelus). , University of Bonn, Germany.Google Scholar
Wings, O. 2007. A review of gastrolith function with implications for fossil vertebrates and a revised classification. Acta Palaeontologica Polonica 52:116.Google Scholar
Wings, O., and Sander, P. M. 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 274:635640.Google Scholar
Worthy, T. H., and Holdaway, R. N. 2002. The lost world of the moa: prehistoric life of New Zealand. Indiana University Press, Bloomington.Google Scholar
Xu, X., Forster, C., Clark, J., and Mo, J. 2006. A basal ceratopsian with transitional features from the Late Jurassic of northwestern China. Proceedings of the Royal Society B 273:21352140.Google Scholar
Xu, X., Clark, J. M., Mo, J., Choiniere, J., Forster, C. A., Erickson, G. M., Hone, D. W. E., Sullivan, C., Eberth, D. A., Nesbitt, S., Zhao, Q., Hernandez, R., Jia, C. K., Han, F. I., and Guo, Y. 2009. A Jurassic ceratosaur from China helps clarify avian digital homologies. Nature 459:940944.CrossRefGoogle ScholarPubMed
You, H. L., and Dodson, P. 2004. Basal Ceratopsia. Pp. 478493in Weishampel, D. B., Dodson, P., and Osmólska, H., eds. The Dinosauria. University of California Press, Berkeley.Google Scholar
Zhou, Z.-H., and Wang, X.-L. 2000. A new species of Caudipteryx from the Yixian Formation of Liaoning, northeast China. Vertebrata PalAsiatica 38:111127.Google Scholar