Abstract
An oft-cited nutritional advantage of large body size is that larger animals have lower relative energy requirements and that, due to their increased gastrointestinal tract (GIT) capacity, they achieve longer ingesta passage rates, which allows them to use forage of lower quality. However, the fermentation of plant material cannot be optimized endlessly; there is a time when plant fibre is totally fermented, and another when energy losses due to methanogenic bacteria become punitive. Therefore, very large herbivores would need to evolve adaptations for a comparative acceleration of ingesta passage. To our knowledge, this phenomenon has not been emphasized in the literature to date. We propose that, among the extant herbivores, elephants, with their comparatively fast passage rate and low digestibility coefficients, are indicators of a trend that allowed even larger hindgut fermenting mammals to exist. The limited existing anatomical data on large hindgut fermenters suggests that both a relative shortening of the GIT, an increase in GIT diameter, and a reduced caecum might contribute to relatively faster ingesta passage; however, more anatomical data is needed to verify these hypotheses. The digestive physiology of large foregut fermenters presents a unique problem: ruminant—and nonruminant—forestomachs were designed to delay ingesta passage, and they limit food intake as a side effect. Therefore, with increasing body size and increasing absolute energy requirements, their relative capacity has to increase in order to compensate for this intake limitation. It seems that the foregut fermenting ungulates did not evolve species in which the intake-limiting effect of the foregut could be reduced, e.g. by special bypass structures, and hence this digestive model imposed an intrinsic body size limit. This limit will be lower the more the natural diet enhances the ingesta retention and hence the intake-limiting effect. Therefore, due to the mechanical characteristics of grass, grazing ruminants cannot become as big as the largest browsing ruminant. Ruminants are not absent from the very large body size classes because their digestive physiology offers no particular advantage, but because their digestive physiology itself intrinsically imposes a body size limit. We suggest that the decreasing ability for colonic water absorption in large grazing ruminants and the largest extant foregut fermenter, the hippopotamus, are an indication of this limit, and are the outcome of the competition of organs for the available space within the abdominal cavity. Our hypotheses are supported by the fossil record on extinct ruminant/tylopod species which did not, with the possible exception of the Sivatheriinae, surpass extant species in maximum body size. In contrast to foregut fermentation, the GIT design of hindgut fermenters allows adaptations for relative passage acceleration, which explains why very large extinct mammalian herbivores are thought to have been hindgut fermenters.
Similar content being viewed by others
Notes
Regression lines were calculated and compared according to Sachs (1997) using the SSS software (Rubisoft software GmbH, Puchheim, Germany, 1998).
The proportionally largest forestomach occurs in sloths, in which its capacity can be up to 30% of body weight (Langer 1988). Sloths have, if at all, only rudimentary caeca and a short large intestine (Stevens and Hume 1995). These animals have very low metabolic rates (McNab 1978), a low food intake (Nagy and Montgomery 1980), long retention times, and defecate only about once per week (Montgomery and Sunquist 1978)—options obviously not available for large ungulates.
References
Alexander RM (1989) Dynamics of dinosaurs and other extinct giants. Columbia Univesity Press, New York
Altman SA (1987) The impact of locomotor energetics on mammalian foraging. J Zool (Lond) 211:215–225
Anonymous (1872) Bairds Tapir. Zool Garten 13:58–59
Barboza PS, Bowyer RT (2000) Sexual segregation in dimorphic deer: a new gastrocentric hypothesis. J Mammal 81:473–489
Bartocci S, Amici A, Verna M, Terramoccia S, Martillotti F (1997) Solid and fluid passage rate in buffalo, cattle and sheep fed diets with different forage to concentrate ratios. Livestock Prod Sci 52:201–208
Beddard FE (1887) A note on the visceral histology of ceratotherium. J R Microsc Soc 78:120–122
Behrend A (2000) Kinetik des Ingestaflusses bei Rehen und Mufflons im saisonalen Verlauf. Dissertation Thesis Biology, Humboldt-University of Berlin, Germany
Bell RHV (1969) The use of herbaceous layers by grazing ungulates in the Serengeti. In: Watson A (ed) Animal populations in relation to their food resources. Symp Br Ecol Soc. Blackwell, Oxford, pp 111–124
Bell RHV (1971) A grazing ecosystem in the Serengeti. Sci Am 225:86–93
Bourdelle E, Lavocat R (1955) Ordre des Périssodactyles. In: Grassé JP (ed) Traité de zoologie. Anatomie, systématique, biologie. Tome XVII vol I. Paris, pp 1002–1167
Brashares JS, Garland T, Arcese P (2000) Phylogenetic analysis of coadaptation in behavior, diet, and body size in the African antelope. Behav Ecol 4:452–463
Case TJ (1979) Optimal body size and an animal's diet. Acta Biotheor 28:54–69
Chivers DJ, Hladik CM (1980) Morphology of the gastrointestinal tract in primates: comparisons with other mammals in relation to diet. J Morphol 166:337–386
Clauss M, Lechner-Doll M (2001) Differences in selective reticulo-ruminal particle retention as a key factor in ruminant diversification. Oecologia 129:321–327
Clauss M, Deutsch A, Lechner-Doll M, Flach EJ, Tack C (1998) Passage rate of fluid and particle phase in captive giraffe. Adv Ethol [Suppl Ethol] 33:98
Clauss M, Fröschle T, Lechner-Doll M, Dierenfeld ES, Hatt JM (2002a) Fluid and particle passage rate in captive black rhinoceros. Abstract Book of the Joint Nutrition Conference, August 2002, Antwerp, p 88
Clauss M, Lechner-Doll M, Streich WJ (2002b) Ruminants: why browsers are non-grazers. Abstract Book of the Joint Nutrition Conference, August 2002, Antwerp, p 126
Clauss M, Lechner-Doll M, Streich WJ (2002c) Faecal dry matter content in captive wild ruminants: implications for the browser/grazer-dichotomy. Abstract Book of the Joint Nutrition Conference, August 2002, Antwerp, p 128
Clauss M, Loehlein W, Kienzle E, Wiesner H (2003) Studies on feed digestibilities in captive Asian elephants. J Anim Physiol Anim Nutr 87:1-14
Clemens ET, Maloiy GMO (1982) Digestive physiology of three East African herbivores, the elephant, rhinoceros and hippopotamus. J Zool (Lond) 198:141–156
Clemens ET, Maloiy GMO (1983) Digestive physiology of East African ruminants. Comp Biochem Physiol 76A:319–333
Clemens ET, Maloiy GMO (1984) Colonic absorption and secretion of fluids, electrolytes and organic acids in East African ruminants. Comp Biochem Physiol 77A:51–56
Coenen M, Meyer H, Stadermann B (1990) Amount and composition of the GIT content according to type of feed and exercise. In: Meyer H (ed) Contributions to water and mineral metabolism of the horse. Parey, Berlin; Adv Anim Physiol Anim Nutr 21:7-20
Colbert EH (1993) Feeding strategies and metabolism in elephants and sauropod dinosaurs. Am J Sci 293A:1–19
Damuth J, MacFadden BJ (eds) (1990) Body size in mammalian paleobiology: estimation and biological implications. Cambridge University Press, Cambridge
De Bouveignes O (1953) Sparrmann et les rhinoceros. Zooleo 21:85–97
Demment MW (1983) Feeding ecology and the evolution of body size of baboons. Afr J Ecol 21:219–233
Demment MW, Longhurst WH (1987) Browsers and grazers: constraints on feeding ecology imposed by gut morphology and body size. In: Santana OP, da Silva AG, Foote WC (eds) Proceedings of the 4th International Conference on Goats, Departamento de Difusao de Tecnologia, Brazil, pp 989–1004
Demment MW, Van Soest PJ (1985) A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am Nat 125:641–672
Economos AC (1981) The largest land mammal. J Theor Biol 89:211–215
Eloff AK, Van Hoven W (1980) Intestinal protozoa of the African elephant. S Afr J Zool 15:83–90
Endo H, Morigaki T, Fujisawa M, Yamagiwa D, Sasaki M, Kimura J (1999) Morphology of the intestinal tract in the White rhinoceros. Anat Hist Embryol 28:303–305
Farlow JO (1987) Speculations about the diet and digestive physiology of herbivorous dinosaurs. Paleobiology 13:60–72
Field CE (1976) Palatability factors and nutritive value of the food of buffalo (Syncerus caffer) in Uganda. E Afr Wildl J 14:181–201
Foose TJ (1982) Trophic strategies of ruminant versus nonruminant ungulates. PhD thesis, University of Chicago, Chicago, Ill., USA
Fortelius M, Kappelman J (1993) The largest land mammal ever imagined. Zool J Linn Soc 107:85–101
Frade F, Vanfrey R (1955) Ordre de Proboscidiens. In: Grassé JP (ed) Traité de zoologie. Anatomie, systématique, biologie. Tome 17, vol 1. Paris, pp 715–875
Freeland WJ (1991) Plant secondary metabolites: biochemical coevolution with herbivores. In: Palo RT, Robbins CT (eds) Plant defenses against mammalian herbivory. CRC Press, Boca Raton, pp 61–81
Frewein J, Gasse H, Leiser R, Roos H, Thomé H, Vollmerhaus B, Waibl H (eds) (1999) Lehrbuch der Anatomie der Haustiere, vol 2. Eingeweide, 8th edn. Parey, Berlin
Fritz H, Duncan P, Gordon IJ, Illius AW (2002) Megaherbivores influence trophic guilds structure in African ungulate communities. Oecologia 131:620–625
Gagnon M, Chew AE (2000) Dietary preferences in extant African bovidae. J Mammal 81:490–511
Garrod AH (1873) On the visceral anatomy of the Sumatran rhinoceros. Proc Zool Soc Lond, pp 92–104
Garrod AH (1877) On some points in the visceral anatomy of the rhinoceros of the Sunderbunds (Rhinoceros sondaicus). Proc Zool Soc Lond, pp 707–711
Gaulin SJC (1979) A Jarman/Ball model for primate feeding niches. Hum Ecol 7:1-20
Geist V (1974) On the relationship of social evolution and ecology in ungulates. Am Zool 14:205–220
Gentry AW (1967) Pelovoris oldowayensis Reck, an extinct bovid from East Africa. Bull Br Mus Nat Hist Geol Ser 14:243–299
Gentry AW, Gentry A (1978) Fossil Bovidae of Olduvai Gorge, Tanzania. Bull Br Mus Nat Hist Geol Ser 29:289–446; 30:1-83
Geraads D (1996) Le Sivatherium du Pliocène final d'Ahl al Oughlam et l'évolution du genre en Afrique. Paläont Z 70:623–629
Giesecke D, Van Gylswyk NO (1975) A study of feeding types and certain rumen functions in six species of South African wild ruminants. J Agric Sci (Camb) 85:75–83
Gordon IJ, Illius AW (1994) The functional significance of the browser-grazer dichotomy in African ruminants. Oecologia 98:167–175
Guthrie RD (1984) Mosaics, allelochemics and nutrients. In: Martin PS, Klein RG (eds) Quaternary extinctions. A prehistoric evolution. University of Arizona Press, Tucson, pp 259–298
Gutmann WF (1989) Die Evolution hydraulischer Konstruktionen: Organismische Wandlung statt altdarwinistischer Anpassung. Kramer, Frankfurt/Main, Germany
Hackenberger MK (1987) Diet digestibilities and ingesta transit times of captive Asian and African elephants. MS thesis, University of Guelph, Canada
Harris JM (1991) Giraffidae. In: Harris JM (ed) Koobi Fora research project 3. Clarendon Press, Oxford, pp 93–138
Hofmann RR (1988) Morphophysiological evolutionary adaptations of the ruminant digestive system. In: Dobson A, Dobson MJ (eds) Aspects of digestive physiology in ruminants. Cornell University Press, Ithaca, N.Y., USA, pp 1–20
Home E (1821) An account of the skeletons of the dugong, two-horned rhinoceros, and tapir of Sumatra. Philos Trans R Soc Lond 11:268–274
Hoppe PP (1977) Rumen fermentation and body weight in African ruminants. In: Peterle TJ (ed) 13th Congress of Game Biology. The Wildlife Society, Washington, DC, pp 141–150
Hume ID (1999) Marsupial nutrition. Cambridge University Press, Cambridge
Illius AW, Gordon IJ (1992) Modelling the nutritional ecology of ungulate herbivores: evolution of body size and competitive interactions. Oecologia 89:428–434
Janis CM (1990) Correlation of cranial and dental variables with body size in ungulates and macropodoids. In: Damuth J, MacFadden BJ (eds) Body size in mammalian paleobiology: estimation and biological implications. Cambridge University Press, Cambridge, pp 255–299
Janis CM, Carrano M (1992) Scaling of reproductive turnover in archosaurs and mammals: why are large terrestrial mammals so rare? Ann Zool Fenn 28:201–216
Janis CM, Gordon IJ, Illius AW (1994) Modelling equid/ruminant competition in the fossil record. Hist Biol 8:15–29
Janis CM, Damuth J, Theodor JM (2000) Miocene ungulates and terrestrial primary productivity: where have all the browsers gone? Proc Natl Acad Sci 97:7899–7904
Jarman PJ (1968) The effect of the creation of Lake Kariba upon the terrestrial ecology of the middle Zambezi valley. PhD thesis, University of Manchester
Jarman PJ (1974) The social organization of antelope in relation to their ecology. Behaviour 48:215–267
Justice KE, Smith FA (1992) A model of dietary fiber utilization by small mammalian herbivores, with empirical results for Neotoma. Am Nat 139:398–416
Kiefer B (2002) Quality and digestibility of white rhinoceros food—a comparison of field and experimental studies. Diss thesis, University of Munich, Germany
Kingdon J (1979) East African mammals, vol 3, part B. Large mammals. Academic Press, London
Langer P (1976) Functional anatomy of the stomach of Hippopotamus amphibius. S Afr J Sci 72:12–16
Langer P (1988) The mammalian herbivore stomach. Fischer, Stuttgart
Langer P (1991) Evolution of the digestive tract in mammals. Verh Dtsch Zool Ges 84:169–193
Langer P (1994) Food and digestion of Cenozoic mammals in Europe. In: Chivers DJ, Langer P (eds) The digestive system of mammals: food, form, and function. Cambridge University Press, Cambridge, pp 9–24
Loehlein W, Kienzle E, Wiesner H, Clauss M (2003) Investigations on the use of chromium oxide as an inert external marker in captive Asian elephants (Elephas maximus): passage and recovery rates. In: Fidgett A, et al. (eds) Zoo animal nutrition, vol 2. Filander, Fürth, Germany (in press)
MacFadden BJ, Hulbert, RC (1990) Body size estimates and size distribution of ungulate mammals from the Late Miocene Love Bone Bed of Florida. In: Damuth J, MacFadden BJ (eds) Body size in mammalian paleobiology: estimation and biological implications. Cambridge University Press, Cambridge, pp 337–363
Maloiy GMO, Clemens CT (1980) Colonic absorption and secretion of electrolytes as seen in five species of East African herbivorous mammals. Comp Biochem Physiol 67A: 21–25
Maloiy GMO, Clemens ET, Kamau JMZ (1982) Aspects of digestion and in vitro rumen fermentation rate in six species of East African wild ruminants. J Zool (Lond) 197:345–353
McNab B (1978) Energetics of arboreal folivores: physiological problems and ecological consequences of feeding on an ubiquitous food supply. In: Montgomery GG (ed) Ecology of arboreal folivores. Smithsonian Institution Press, Washington, DC, pp 153–162
Meyer H, Stadermann B, Radicke S, Kienzle E, Nyari A (1993) Investigations on amount and composition of the gastrointestinal tract and postprandial parameters in blood and urine according to type of feed. Pferdeheilkunde 9:15–25
Mitchell PC (1903/6) On the intestinal tract of mammals. Trans Zool Soc Lond 17:437–536
Montgomery GG, Sunquist ME (1978) Habitat selection and use by two-toed and three-toed sloths. In: Montgomery GG (ed) Ecology of arboreal folivores. Smithsonian Institution Press, Washington, DC, pp 329–359
Mullen A (1682) An anatomical account of the elephant accidentally burnt in Dublin on Fryday, June 17. in the year 1681. Smith, London
Nagy KA, Montgomery GG (1980) Field metabolic rate, water flux and food consumption in three-toed sloths. J Mammal 61:465–472
Naples VL (1987) Reconstruction of cranial morphology and analysis of function in the Pleistocene ground sloth Nothrotheriops shastense. Nat Hist Mus Los Angeles Cty Contrib Sci 389:1-21
Naples VL (1989) The feeding mechanism in the Pleistocene ground sloth, Glossotherium. Nat Hist Mus Los Angeles Cty Contrib Sci 415:1-23
NOW (2002) Neogene of the Old World. http://www.helsinki.fi/science/now. Cited June 2002
Owen TR (1862) On the anatomy of the Indian rhinoceros. Trans Zool Soc Lond 4:31–58
Owen-Smith N (1982) Factors influencing the consumption of plant products by large herbivores. In: Huntley BJ, Walker BH (eds) Ecology of tropical savannas, Springer, Berlin Heidelberg New York, pp 359–404
Owen-Smith N (1988) Megaherbivores. The influence of very large body size on ecology. Cambridge University Press, Cambridge
Parra R (1978) Comparison of foregut and hindgut fermentation in herbivores. In: Montgomery, GG (ed) The ecology of arboreal folivores. Smithsonian Institution Press, Washington, DC, pp 205–230
Pérez-Barberìa FJ, Gordon IJ, Nores C (2001) Evolutionary transitions among feeding styles and habitats in ungulates. Evol Ecol Res 3:221–230
Persson L (1985) Asymmetrical competition: are larger animals competitively superior? Am Nat 126:261–266
Peters RH (1983) The ecological implications of body size. Cambridge UniversityPress, Cambridge
Prins RA, Kreulen DA (1991) Comparative aspects of plant cell wall digestion in mammals. In: Hoshino S, Onodera R, Minoto H, Itabashi H (eds) The rumen ecosystem: the microbial metabolism and its regulation. Japan Scientific Soc Press, Tokyo, pp 109–121
Renecker LA, Hudson RJ (1992) Thermoregulatory and behavioral response of moose: is large body size an adaptation or constraint? Alces [Suppl] 1:52–64
Roux W (1881) Der Kampf der Theile im Organismus. Engelmann, Leipzig, Germany
Sachs L (1997) Angewandte Statistik, vol 8. Springer, Berlin Heidelberg New York
Schmidt-Nielsen K (1984) Scaling. Why is animal size so important? Cambridge UniversityPress, Cambridge
Scott KM (1990) Postcranial dimensions of ungulates as predictors of body mass. In: Damuth J, MacFadden BJ (eds) Body size in mammalian paleobiology: estimation and biological implications. Cambridge UniversityPress, Cambridge, pp 301–335
Sikes SK (1971) The natural history of the African elephant. Weidenfeld and Nicolson, London, UK
Silva M, Downing JA (1995) CRC handbook of mammalian body masses. CRC Press, Boca Raton, Fla.
Sinclair ARE (1974) The natural regulation of buffalo population in East Africa. IV. The food supply as a regulating factor and competition. E Afr Wildl J 10:77–89
Singer R, Boné E (1960) Modern giraffes and the fossil giraffids of Africa. Ann S Afr Mus 45:375–548
Smith FA (1995) Scaling of digestive efficiency with body mass in Neotoma. Funct Ecol 9:299–305
Solounias N, McGraw WS, Hayek LA, Werdelin L (2000) The paleodiet of the Giraffidae. In: Vrba ES, Schaller GB (eds) Antelopes, deer, and relatives. Fossil record, behavioral ecology, systematics, and conservation. Yale University Press, New Haven
Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system. Cambridge UniversityPress, Cambridge
Van Hoven W (1978) Digestion physiology in the stomach complex and hindgut of the hippopotamus. S Afr J Wildl Res 8:59–64
Van Hoven W, Prins RA, Lankhorst A (1981) Fermentative digestion in the African elephant. S Afr J Wildl Res 11:78–86
Van Soest PJ (1994) Nutritional ecology of the ruminant, 2nd edn. Cornell UniversityPress, Ithaca
Van Soest PJ (1996) Allometry and ecology of feeding behavior and digestive capacity in herbivores: a review. Zoo Biol 15:455–479
Van Wieren SE (1996) Browsers and grazers: foraging strategies in ruminants. In: Van Wieren SE (ed) Digestive strategies in ruminants and nonruminants. Thesis, Landbouw Universiteit, Wageningen, pp 119–145
Wilson VJ, Edwards PW (1965) Data from a female rhinoceros and foetus from the Fr. Jameson district. Puku 3:179–180
Woodall PF, Skinner JD (1993) Dimensions of the intestine, diet and faecal water loss in some African antelope. J Zool (Lond) 229:457–471
Woolnough AP, du Toit JT (2001) Vertical zonation of browse quality in tree canopies exposed to a size-structured guild of African browsing ungulates. Oecologia 129:585–590
Acknowledgements
We thank M. Clauss and V. Margerie for support in literature acquisition, and A.W. Milewski and T.J. Foose for comments upon the manuscript. A.W. Milewski provided the spark for this review.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Clauss, M., Frey, R., Kiefer, B. et al. The maximum attainable body size of herbivorous mammals: morphophysiological constraints on foregut, and adaptations of hindgut fermenters. Oecologia 136, 14–27 (2003). https://doi.org/10.1007/s00442-003-1254-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-003-1254-z