Skip to main content

Advertisement

Log in

The maximum attainable body size of herbivorous mammals: morphophysiological constraints on foregut, and adaptations of hindgut fermenters

Oecologia Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2A, B.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

Notes

  1. Regression lines were calculated and compared according to Sachs (1997) using the SSS software (Rubisoft software GmbH, Puchheim, Germany, 1998).

  2. 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

    Google Scholar 

  • Anonymous (1872) Bairds Tapir. Zool Garten 13:58–59

    Google Scholar 

  • Barboza PS, Bowyer RT (2000) Sexual segregation in dimorphic deer: a new gastrocentric hypothesis. J Mammal 81:473–489

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Beddard FE (1887) A note on the visceral histology of ceratotherium. J R Microsc Soc 78:120–122

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Case TJ (1979) Optimal body size and an animal's diet. Acta Biotheor 28:54–69

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Clauss M, Lechner-Doll M (2001) Differences in selective reticulo-ruminal particle retention as a key factor in ruminant diversification. Oecologia 129:321–327

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Clemens ET, Maloiy GMO (1982) Digestive physiology of three East African herbivores, the elephant, rhinoceros and hippopotamus. J Zool (Lond) 198:141–156

    Google Scholar 

  • Clemens ET, Maloiy GMO (1983) Digestive physiology of East African ruminants. Comp Biochem Physiol 76A:319–333

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Damuth J, MacFadden BJ (eds) (1990) Body size in mammalian paleobiology: estimation and biological implications. Cambridge University Press, Cambridge

    Google Scholar 

  • De Bouveignes O (1953) Sparrmann et les rhinoceros. Zooleo 21:85–97

    Google Scholar 

  • Demment MW (1983) Feeding ecology and the evolution of body size of baboons. Afr J Ecol 21:219–233

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Economos AC (1981) The largest land mammal. J Theor Biol 89:211–215

    Google Scholar 

  • Eloff AK, Van Hoven W (1980) Intestinal protozoa of the African elephant. S Afr J Zool 15:83–90

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Farlow JO (1987) Speculations about the diet and digestive physiology of herbivorous dinosaurs. Paleobiology 13:60–72

    Google Scholar 

  • Field CE (1976) Palatability factors and nutritive value of the food of buffalo (Syncerus caffer) in Uganda. E Afr Wildl J 14:181–201

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gagnon M, Chew AE (2000) Dietary preferences in extant African bovidae. J Mammal 81:490–511

    Google Scholar 

  • 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

    Google Scholar 

  • Geist V (1974) On the relationship of social evolution and ecology in ungulates. Am Zool 14:205–220

    Google Scholar 

  • Gentry AW (1967) Pelovoris oldowayensis Reck, an extinct bovid from East Africa. Bull Br Mus Nat Hist Geol Ser 14:243–299

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Gordon IJ, Illius AW (1994) The functional significance of the browser-grazer dichotomy in African ruminants. Oecologia 98:167–175

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Janis CM, Gordon IJ, Illius AW (1994) Modelling equid/ruminant competition in the fossil record. Hist Biol 8:15–29

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Mitchell PC (1903/6) On the intestinal tract of mammals. Trans Zool Soc Lond 17:437–536

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Naples VL (1989) The feeding mechanism in the Pleistocene ground sloth, Glossotherium. Nat Hist Mus Los Angeles Cty Contrib Sci 415:1-23

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Persson L (1985) Asymmetrical competition: are larger animals competitively superior? Am Nat 126:261–266

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Singer R, Boné E (1960) Modern giraffes and the fossil giraffids of Africa. Ann S Afr Mus 45:375–548

    Google Scholar 

  • Smith FA (1995) Scaling of digestive efficiency with body mass in Neotoma. Funct Ecol 9:299–305

    Google Scholar 

  • 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

    Google Scholar 

  • Van Hoven W, Prins RA, Lankhorst A (1981) Fermentative digestion in the African elephant. S Afr J Wildl Res 11:78–86

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Woodall PF, Skinner JD (1993) Dimensions of the intestine, diet and faecal water loss in some African antelope. J Zool (Lond) 229:457–471

    Google Scholar 

  • 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

    Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to M. Clauss.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-003-1254-z

Keywords

Navigation