Gross intestinal morphometry and allometry in Carnivora

Abstract

Although typical anatomical features of the digestive tract of carnivores are well known, such as the presence or absence of a caecum in various carnivore taxa, and although a large number of length measurements have been published, the body mass measurement of the corresponding specimens has mostly not been reported. Here, we add original mass and intestine length measurements for 36 carnivore species to literature data. Using Phylogenetic Generalized Least Squares, we demonstrate that marine Carnivora (pinnipeds and the sea otter Enhydra lutris) have significantly longer total and small intestines relative to body mass than terrestrial Carnivora, and both pinnipeds and mustelids in general have particularly long total intestines amongst terrestrial Carnivora. The natural diet explains little about variation in relative intestinal length measures. However, amongst species that do have a caecum, a higher proportion of plant material in the diet might be associated with a longer caecum. In particular, a diet with higher proportions of plant material provided by humans could have led to a particularly long caecum in the domestic dog.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

References

  1. Anderson M, Richardson P, Woodall P (1992) Functional analyses of the feeding apparatus and digestive tract anatomy of the aardwolf (Proteles cristatus). J Zool (Lond) 228:423–434

    Article  Google Scholar 

  2. Axelsson E, Ratnakumar A, Arendt ML, Maqbool K, Webster MT, Perloski M, Liberg O, Arnemo JM, Hedhammar Å, Lindblad-Toh K (2013) The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495:360–364

    CAS  Article  PubMed  Google Scholar 

  3. Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512

    CAS  Article  PubMed  Google Scholar 

  4. Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2008) Corrigendum: the delayed rise of present-day mammals. Nature 456:274

    CAS  Article  Google Scholar 

  5. Bryden MM, Erickson AW (1976) Body size and composition of crabeater seals (Lobodon carcinophagus), with observations on tissue and organ size in Ross seals (Ommatophoca rossi). J Zool 179:235–247

    Article  Google Scholar 

  6. Buddington RK, Chen JW, Diamond JM (1991) Dietary regulation of intestinal brush-border sugar and amino acid transport in carnivores. Am J Physiol 261:R793–R801

    CAS  PubMed  Google Scholar 

  7. 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  Article  PubMed  Google Scholar 

  8. Clauss M, Kleffner H, Kienzle E (2010) Carnivorous mammals: nutrient digestibility and energy evaluation. Zoo Biol 29:687–704

    Article  PubMed  Google Scholar 

  9. Davis DD (1962) Allometric relationships in lions vs. domestic cats. Evolution 16:505–514

    Article  Google Scholar 

  10. Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    CAS  Article  PubMed  Google Scholar 

  11. Iversen JA (1972) Basal energy metabolism of mustelids. J Comp Physiol B 81:341–344

    Article  Google Scholar 

  12. Kenyon KW (1969) The sea otter in the eastern Pacific Ocean. US Fish and Wildlife Service No. 68, Washington

  13. King JE (1969) Some aspects of the anatomy of the Ross seal Ommatophoca rossi (Pinnipedia: Phocidae). Br Antarctic Sci Rep 63:1–54

    Google Scholar 

  14. Kostanecki K (1926) Le caecum des vertébrés (y compris l’ “appendice vermiculaire”). Morphologie et signification fonctionnelle. Bulletin International de l’Académie Polonaise des Sciences et des Lettres, Classe des Sciences Methématiques et Naturelles Série B :1–295

  15. Lavin SR, Karasov WH, Ives AR, Middleton KM, Garland T (2008) Morphometrics of the avian small intestine compared with that of nonflying mammals: a phylogenetic approach. Physiol Biochem Zool 81:526–550

    Article  PubMed  Google Scholar 

  16. Lovegrove BG (2010) The allometry of rodent intestines. J Comp Physiol B 180:741–755

    Article  PubMed  Google Scholar 

  17. Mårtensson PE, Nordoy ES, Messelt EB, Blix AS (1998) Gut length, food transit time and diving habit in phocid seals. Polar Biol 20:213–217

    Article  Google Scholar 

  18. McNab BK (2008) An analysis of the factors that influence the level and scaling of mammalian BMR. Comp Biochem Physiol A 151:5–28

    Article  Google Scholar 

  19. Mitchell PC (1903–6) On the intestinal tract of mammals. Transactions of the Zoological Society of London 17:437–536

  20. Mitchell PC (1916) Further observations on the intestinal tract of mammals. Proc Zool Soc London 86:183–252

    Article  Google Scholar 

  21. Navarrete A, van Schaik CP, Isler K (2011) Energetics and the evolution of human brain size. Nature 480:91–93

    CAS  Article  PubMed  Google Scholar 

  22. Okamoto M, Tanaka K, Tsunokawa M, Kasamatsu M, Yokota H, Tanida K, Kawasako K, Komine M, Akihara Y, Shimoyama Y, Hirayama K (2006) Small intestinal volvulus in a captive Steller sea lion (Eumetopias jubatus). Vet Rec 159:21

    CAS  Article  PubMed  Google Scholar 

  23. Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N (2010) Caper: comparative analyses of phylogenetics and evolution in R. R package version 04/r71 See http://caperrforgerproject.org/

  24. Orr RT (1976) Vertebrate biology. WB Saunders, Philadelphia

    Google Scholar 

  25. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    CAS  Article  PubMed  Google Scholar 

  26. Raven HC (1936) Notes on the anatomy of the viscera of the giant panda (Ailuropoda melanoleuca). Am Mus Novit 877:1–23

    Google Scholar 

  27. Revell LJ (2010) Phylogenetic signal and linear regression on species data. Methods Ecol Evol 1:319–329

    Article  Google Scholar 

  28. Richardson KC, Gales NJ (1987) Functional morphology of the alimentary tract of the Australian sea-lion Neophoca cinerea. Aust J Zool 35:219–226

    Article  Google Scholar 

  29. Schiek JO, Millar JS (1985) Alimentary tract measurements as indicators of diets of small mammals. Mammalia 49:93–104

    Google Scholar 

  30. Snipes RL, Snipes H (1997) Quantitative investigation of the intestine in eight species of domestic mammals. Mamm Biol 62:359–371

    Google Scholar 

  31. Sparling CE, Fedak MA, Thompson D (2007) Eat now, pay later? Evidence of deferred food-processing costs in diving seals. Biol Lett 3:95–99

    Article  Google Scholar 

  32. Stark R, Roper TJ, MacLarnon AM, Chivers DJ (1987) Gastrointestinal anatomy of the European badger Meles meles. A comparative study. Mamm Biol 52:88–96

    Google Scholar 

  33. Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system. Cambridge University Press, New York

    Google Scholar 

  34. Team RDC (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria ISBN 3-900051-07-0, URL http://www.R-project.org/

  35. Williams TM, Haun J, Davis RW, Fuiman LA, Kohin S (2001) A killer appetite: metabolic consequences of carnivory in marine mammals. Comp Biochem Physiol A 129:785–796

    CAS  Article  Google Scholar 

  36. Wilman H, Belmaker J, Simpson J, de la Rosa C, Rivadeneira MM, Jetz W (2014) Elton traits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95:2027

    Article  Google Scholar 

Download references

Acknowledgments

The collection of the specimens by AN was supported by the Swiss National Science Foundation (grant number 3100A0-117789), the A.H. Schultz-Stiftung and the European Integrated Activities grant SYNTHESYS (grant application number HU-TAF-4916). We thank Jeanne Peters for the work on the digital images.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Marcus Clauss.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

McGrosky, A., Navarrete, A., Isler, K. et al. Gross intestinal morphometry and allometry in Carnivora. Eur J Wildl Res 62, 395–405 (2016). https://doi.org/10.1007/s10344-016-1011-3

Download citation

Keywords

  • Canid
  • Felid
  • Ursid
  • Viverrid
  • Jejunum
  • Colon