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Mammalian Biology

, Volume 97, Issue 1, pp 104–111 | Cite as

The rumen washes off abrasives before heavy-duty chewing in ruminants

  • Jean-Michel Hatt
  • Daryl Codron
  • Dennis W. H. Müller
  • Nicole L. Ackermans
  • Louise F. Martin
  • Patrick R. Kircher
  • Jürgen Hummel
  • Marcus ClaussEmail author
Original investigation

Abstract

Based on comparative mandibular anatomy, observations of chewing behaviour, chewing forces and dental microwear, it has been suggested that an additional effect of the ruminant digestive strategy could be a reduction of both the required chewing load and tooth wear ruminants are exposed to. This effect is hypothesized to be the result of digestion, mixing, and digesta sorting prior to regurgitation for rumination, which might both soften the material and wash off external abrasives such as sand, grit and dust. Putatively, these external abrasives would thus be trapped in the (fore)stomach and excreted via the faeces. We investigated the location of sand in the stomach of goats fed diets containing phytoliths and sand for several months. The contents of the stomach section from where rumination material is recruited were comparatively depleted of sand. Sand mainly accumulated in another stomach section, the abomasum, without causing clinical problems. A certain phytolith content should hence affect ruminants and non-ruminant herbivores somewhat alike; however, a certain external abrasives content should affect ruminants less than non-ruminants. Results from feeding experiments as well as tooth wear studies support this hypothesis, and caution against the default use of dental anatomy and wear as taxon-free environmental proxies in paleobiology.

Ruminant Rumen Tooth wear Chewing Rumination Hypsodonty 

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References

  1. Ackermans, N.L., Winkler, D.E., Schulz-Kornas, E., Kaiser, T.M., Müller, D.W.H., Kircher, P., Hummel, J., Clauss, M., Hatt, J.-M., 2018. Controlled feeding experiments with diets of different abrasiveness reveal slow development of mesowear signal in goats (Capra aegagrus hircus). J. Exp. Biol. 221, jeb186411.PubMedCrossRefGoogle Scholar
  2. Ackermans, N.L., Clauss, M., Winkler, D.E., Schulz-Kornas, E., Kaiser, T.M., Müller, D.W.H., Kircher, P.R., Hummel, J., Hatt, J.M., 2019. Root growth compensates for molar wear in adult goats (Capra aegagrus hircus). J. Exp. Zool. A, 331, 139–148.CrossRefGoogle Scholar
  3. Allritz, M., Tennie, C., Call, J., 2013. Food washing and placer mining in captive great apes. Primates, 54, 361–370.PubMedCrossRefGoogle Scholar
  4. Andrews, P., Hixson, S., 2014. Taxon-free methods of palaeoecology. Ann. Zool. Fenn., 51, 269–284.CrossRefGoogle Scholar
  5. AOAC., 1995. Official Methods of Analysis of AOAC International. Association of Official Analytical Chemists, Arlington, VA.Google Scholar
  6. Braun, U., Irmer, M., Augsburger, H., Jud, R., Olerth, S., 2011a. Computed tomography of the abdomen in Saanen goats: I. Reticulum, rumen, and omasum. Schweiz. Arch. Tierheilkd., 153, 307–313.PubMedCrossRefGoogle Scholar
  7. Braun, U., Irmer, M., Augsburger, H., Müller, U., Jud, R., Ohlerth, S., 2011b. Computed tomography of the abdomen in Saanen goats: II. Liver, spleen, abomasum, and intestine. Schweiz. Arch. Tierheilkd., 153, 314–320.PubMedCrossRefGoogle Scholar
  8. Braun, U., Irmer, M., Augsburger, H., Ohlerth, S., 2011c. Computed tomography of the abdomen in Saanen goats: III. Kidneys, ureters and urinary bladder. Schweiz. Arch. Tierheilkd., 153, 321–329.PubMedCrossRefGoogle Scholar
  9. Clauss, M., Hume, I.D., Hummel, J., 2010. Evolutionary adaptations of ruminants and their potential relevance for modern production systems. Animal, 4, 979–992.PubMedCrossRefPubMedCentralGoogle Scholar
  10. Clauss, M., Steuer, P., Erlinghagen-Lückerath, K., Kaandorp, J., Fritz, J., Südekum, K.H., Hummel, J., 2015. Faecal particle size: digestive physiology meets herbivore diversity. Comp. Biochem. Physiol. A, 179, 182–191.CrossRefGoogle Scholar
  11. Clauss, M., Stewart, M., Price, E., Peilon, A., Savage, T., Van Ekris, I., Munn, A., 2016. The effect of feed intake on digesta passage, digestive organ fill and mass, and digestadry matter content in sheep (Ovis aries): flexibility in digestion but not in water reabsorption. Small Rumin. Res., 138, 12–19.CrossRefGoogle Scholar
  12. Clauss, M., Fritz, J., Tschuor, A., Braun, U., Hummel, J., Codron, D., 2017. Dry matter and digesta particle size gradients along the goat digestive tract on grass and browse diets. J. Anim. Physiol. Anim. Nutr., 101, 61–69.CrossRefGoogle Scholar
  13. Clauss, M., Hummel, J., 2017. Physiological adaptations of ruminants and their potential relevance for production systems. Rev. Bras. Zootec., 46, 606–613.CrossRefGoogle Scholar
  14. Clauss, M., 2019. Phylogenetic signal in tooth wear? A question that can be answered - by testing. Ecol. Evol.,  https://doi.org/10.1002/ece3.5214, online.Google Scholar
  15. DeSantis, L., Fortelius, M., Grine, F.E., Janis, C., Kaiser, T.M., Merceron, G., Purnell, M.A., Schulz-Kornas, E., Saarinen, J., Teaford, M., Ungar, P.S., Žliobaitė, I., 2018. The phylogenetic signal in tooth wear: what does it mean? Ecol. Evol., 8, 11359–11362.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Dittmann, M.T., Hummel, J., Hammer, S., Arif, A., Hebel, C., Müller, D.W.H., Fritz, J., Steuer, P., Schwarm, A., Kreuzer, M., Clauss, M., 2015. Digesta retention in gazelles in comparison to other ruminants: evidence fortaxon-specific rumen fluid throughput to adjust digesta washing to the natural diet. Comp. Biochem. Physiol. A, 185, 58–68.CrossRefGoogle Scholar
  17. Dittmann, M.T., Kreuzer, M., Runge, U., Clauss, M., 2017. Ingestive mastication in horses resembles rumination but not ingestive mastication in cattle and camels. J. Exp. Zool. A327, 98–109.CrossRefGoogle Scholar
  18. Erickson, N., Hendrick, S., 2011. Sand impactions in a Saskatchewan beef cow-calf herd. Can. Vet. J., 52, 74–76.PubMedPubMedCentralGoogle Scholar
  19. Fletcher, T.M., Janis, CM., Rayfield, E.J., 2010. Finite element analysis of ungulate jaws: can mode of digestive physiology be determined? Palaeontol. Electron. 13, 21A.Google Scholar
  20. Fraser, D., Haupt, R.J., Barr, W.A., 2018. Phylogenetic signal in tooth wear dietary niche proxies. Ecol. Evol., 8, 5355–5368.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Hummel, J., Findeisen, E., Südekum, K.H., Ruf, I., Kaiser, T.M., Bucher, M., Clauss, M., Codron, D., 2011. Another one bites the dust: faecal silica levels in large herbivores correlate with high-crowned teeth. Proc. R. Soc. B, 278, 1742–1747.PubMedCrossRefPubMedCentralGoogle Scholar
  22. Ito, M., Macdonald, A.A., Leus, K., Atmaja, I., Balik, I.W., 2017. Food preparation behaviour of babirusa (Babyrousa celebensis). J. Zoo Aquar. Res., 5, 97–103.Google Scholar
  23. Janis, CM., Constable, E.C., Houpt, K.A., Streich, W.J., Clauss, M., 2010. Comparative ingestive mastication in domestic horses and cattle: a pilot investigation. J. Anim. Physiol. Anim. Nutr. 94, e402–e409.CrossRefGoogle Scholar
  24. Kaiser, T.M., Müller, D.W.H., Fortelius, M., Schulz, E., Codron, D., Clauss, M., 2013. Hypsodonty and tooth facet development in relation to diet and habitat in herbivorous ungulates: implications for understanding tooth wear. Mammal Rev., 43, 34–46.CrossRefGoogle Scholar
  25. Karme, A., Rannikko, J., Kallonen, A., Clauss, M., Fortelius, M., 2016. Mechanical modelling of tooth wear. J. Roy. Soc. Int. 13, 20160399.CrossRefGoogle Scholar
  26. Kubo, M.O., Yamada, E., 2014. The inter-relationship between dietary and environmental properties and tooth wear: comparisons of mesowear, molar wear rate, and hypsodonty index of extant sika deer populations. PLoS One 9, e90745.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Lechner-Doll, M., Kaske, M., von Engelhardt, W., 1991. Factors affecting the mean retention time of particles in the forestomach of ruminants and camelids. In: Tsuda, T., Sasaki, Y., Kawashima, R. (Eds.), Physiological Aspects of Digestion and Metabolism in Ruminants. Academic Press, San Diego, CA, pp. 455–482.CrossRefGoogle Scholar
  28. McLeod, M.N., Minson, D.J., 1988. Large particle breakdown by cattle eating ryegrass and alfalfa. J. Anim. Sci., 66, 992–999.PubMedCrossRefPubMedCentralGoogle Scholar
  29. Melendez, P., Krueger, T., Benzaquen, M., Risco, C., 2007. An outbreak of sand impaction in postpartum dairy cows. Can. Vet. J., 48, 1067–1070.PubMedPubMedCentralGoogle Scholar
  30. Merceron, G., Ramdarshan, A., Blondel, C., Boisserie, J.R., Brunetiere, N., Francisco, A., Gautier, D., Milhet, X., Novello, A., Pret, D., 2016. Untangling the environmental from the dietary: dust does not matter. Proc. R. Soc. B 283, 20161032.PubMedCrossRefGoogle Scholar
  31. Mihlbachler, M.C., Campbell, D., Ayoub, M., Chen, C., Ghani, I., 2016. Comparative dental microwear of ruminant and perissodactyl molars: implications for paleodietary analysis of rare and extinct ungulate clades. Paleobiology, 42, 98–116.CrossRefGoogle Scholar
  32. Müller, J., Clauss, M., Codron, D., Schulz, E., Hummel, J., Fortelius, M., Kircher, P., Hatt, J.M., 2014. Growth and wear of incisor and cheekteeth in domestic rabbits (Oryctolagus cuniculus) fed diets of different abrasiveness. J. Exp. Zool. A, 321, 283–298.CrossRefGoogle Scholar
  33. Müller, J., Clauss, M., Codron, D., Schulz, E., Hummel, J., Kircher, P., Hatt, J.M., 2015. Tooth length and incisal wear and growth in guinea pigs (Cavia porcellus) fed diets of different abrasiveness. J. Anim. Physiol. Anim. Nutr., 99, 591–604.CrossRefGoogle Scholar
  34. Nakamichi, M., Kato, E., Kojima, Y., Itoigawa, N., 1998. Carrying and washing of grass roots by free-ranging Japanese macaques at Katsuyama. Folia Primatol., 69, 35–40.PubMedCrossRefGoogle Scholar
  35. Neadle, D., Allritz, M., Tennie, C., 2017. Food cleaning in gorillas: social learning is a possibility but not a necessity. PLoS One 12, e0188866.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Nickel, R., Schummer, A., Seiferle, E., 2004. Eingeweide. In: Lehrbuch der Anatomie der Säugetiere 2, Parey, Stuttgart, Germany.Google Scholar
  37. Ohlert, S., Becker-Birck, M., Augsburger, H., Jud, R., Makara, M., Braun, U., 2012. Computed tomography measurements of thoracic structures in 26 clinically normal goats. Res. Vet. Sci., 92, 7–12.CrossRefGoogle Scholar
  38. Core_Team., 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria https://doi.org/www.R-project.org/.Google Scholar
  39. Sauer, C., Clauss, M., Bertelsen, M.F., Weisbjerg, M.R., Lund, P., 2017. Rumen content stratification in the giraffe (Giraffa camelopardalis). Comp. Biochem. Physiol. A, 203, 69–76.CrossRefGoogle Scholar
  40. Schwarm, A., Ortmann, S., Rietschel, W., Kühne, R., Wibbelt, G., Clauss, M., 2010. Function, size and form of the gastrointestinal tract of the collared Pecari tajacu and white-lipped peccary Tayassu pecari. Eur.J. Wildl. Res., 56, 569–576.CrossRefGoogle Scholar
  41. Sommer, V., Lowe, A., Dietrich, T., 2016. Not eating like a pig: European wild boar wash their food. Anim. Cogn., 19, 245–249.PubMedCrossRefPubMedCentralGoogle Scholar
  42. Staaland, H., Hove, K., White, R.G., 1986. Mineral absorption in relation to nutritional ecology of reindeer. Rangifer 6, 279–287.CrossRefGoogle Scholar
  43. Staaland, H., Thing, H., 1991. Distribution of nutrients and minerals in the alimentary tract of muskoxen (Ovibos maschatus). Comp. Biochem. Physiol. A, 98, 543–549.CrossRefGoogle Scholar
  44. Trudell-Moore, J., White, R.G., 1983. Physical breakdown of food during eating and rumination in reindeer. Acta Zool. Fenn., 175, 47–49.Google Scholar
  45. van de Waal, E., Krützen, M., Hula, J., Goudet, J., Bshary, R., 2012v. Similarity in food cleaning techniques within matrilines in wild vervet monkeys. PLoS One 7, e35694.Google Scholar
  46. Van Soest, P.J., 1994. Nutritional Ecology of the Ruminant, 2nd edn. Cornell University Press, Ithaca.Google Scholar
  47. Williams, S.H., Stover, K.K., Davis, J.S., Montuelle, S.J., 2011. Mandibular corpus bone strains during mastication in goats (Capra hircus): a comparison of ingestive and rumination chewing. Arch. Oral Biol., 56, 960–971.PubMedCrossRefPubMedCentralGoogle Scholar
  48. Wings, O., Hatt, J.M., Schwarm, A., Clauss, M., 2008. Gastroliths in a pygmy hippopotamus (Hexaprotodon liberiensis). Senck. Biol., 88, 345–348.Google Scholar
  49. Zeitz, J.O., Ineichen, S., Soliva, CR., Leiber, F., Tschuor, A., Braun, U., Kreuzer, M., Clauss, M., 2016. Variability in microbial population and fermentation traits at various sites within the forestomach and along the digestive tract as assessed in goats fed either grass or browse. Small Rumin. Res., 136, 7–17.CrossRefGoogle Scholar
  50. Zhou, Z., Winkler, D.E., Fortuny, J., Kaiser, T.M., Marcé-Nogué, J., 2019. Why ruminating ungulates chew sloppily: biomechanics discern a phylogenetic pattern. PLoS One 14, e0214510.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde, e. V. DGS 2019

Authors and Affiliations

  • Jean-Michel Hatt
    • 1
  • Daryl Codron
    • 2
  • Dennis W. H. Müller
    • 1
  • Nicole L. Ackermans
    • 1
  • Louise F. Martin
    • 1
  • Patrick R. Kircher
    • 3
  • Jürgen Hummel
    • 4
  • Marcus Clauss
    • 1
    Email author
  1. 1.Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse FacultyUniversity of ZurichZurichSwitzerland
  2. 2.Department of Zoology and EntomologyUniversity of the Free StateBloemfonteinSouth Africa
  3. 3.Clinic for Diagnostic Imaging, Vetsuisse FacultyUniversity of ZurichZurichSwitzerland
  4. 4.Ruminant Nutrition, Department of Animal SciencesUniversity of GoettingenGoettingenGermany

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