Journal of Comparative Physiology B

, Volume 185, Issue 5, pp 559–573 | Cite as

Digesta retention patterns of solute and different-sized particles in camelids compared with ruminants and other foregut fermenters

  • Marie T. Dittmann
  • Ullrich Runge
  • Sylvia Ortmann
  • Richard A. Lang
  • Dario Moser
  • Cordula Galeffi
  • Angela Schwarm
  • Michael Kreuzer
  • Marcus Clauss
Original Paper


The mean retention times (MRT) of solute or particles in the gastrointestinal tract and the forestomach (FS) are crucial determinants of digestive physiology in herbivores. Besides ruminants, camelids are the only herbivores that have evolved rumination as an obligatory physiological process consisting of repeated mastication of large food particles, which requires a particle sorting mechanism in the FS. Differences between camelids and ruminants have hardly been investigated so far. In this study we measured MRTs of solute and differently sized particles (2, 10, and 20 mm) and the ratio of large-to-small particle MRT, i.e. the selectivity factors (SF10/2mm, SF20/2mm, SF20/10mm), in three camelid species: alpacas (Vicugna pacos), llamas (Llama glama), and Bactrian camels (Camelus bactrianus). The camelid data were compared with literature data from ruminants and non-ruminant foregut fermenters (NRFF). Camelids and ruminants both had higher SF10/2mmFS than NRFF, suggesting convergence in the function of the FS sorting mechanism in contrast to NRFF, in which such a sorting mechanism is absent. The SF20/10mmFS did not differ between ruminants and camelids, indicating that there is a particle size threshold of about 1 cm in both suborders above which particle retention is not increased. Camelids did not differ from ruminants in MRT2mmFS, MRTsoluteFS, and the ratio MRT2mmFS/MRTsoluteFS, but they were more similar to ‘cattle-’ than to ‘moose-type’ ruminants. Camelids had higher SF10/2mmFS and higher SF20/2mmFS than ruminants, indicating a potentially slower particle sorting in camelids than in ruminants, with larger particles being retained longer in relation to small particles.


Digesta kinetics Digesta passage Rumen Digesta washing Selectivity factor 



We thank Jörg Wick, Andreas Thalmann and the animal keeper team of Zurich Zoo and the entire team of the Kamelhof Olmerswil for their support during animal management. We are also grateful to Catharina Vendl and Walter Salzburger for their help during the sampling period, Simon Ineichen for sample preparation, and Heidrun Barleben, Carmen Kunz, Muna Merghani and Elisabeth Wenk for sample analysis. This study was part of project 310030_135252/1 funded by the Swiss National Science Foundation.


  1. AOAC (1995) Official methods of analysis of AOAC International. Association of Official Analytical Chemists, Arlington VAGoogle Scholar
  2. Barker S, Brown GD, Calaby JH (1963) Food regurgitation in the macropodidae. Aust J Sci 25:430–432Google Scholar
  3. Bärmann EV (2014) The evolution of body size, horn shape and social behaviour in crown Antilopini—an ancestral character state analysis. Zitteliana B 32:185–196Google Scholar
  4. Bauchop T, Martucci RW (1968) Ruminant-like digestion of the langur monkey. Science 161:698–700PubMedCrossRefGoogle Scholar
  5. Baumont R, Deswysen AG (1991) Mélange et propulsion du contenu du réticulo-rumen. Repr Nutr Dev 31:335–359CrossRefGoogle Scholar
  6. Blaxter KL, Graham NM, Wainman FW (1956) Some observations on the digestibility of food by sheep, and on related problems. Br J Nutr 10:69–91PubMedCrossRefGoogle Scholar
  7. Bruining M, Bosch MW (1992) Ruminal passage rate as affected by CrNDF particle size. Anim Feed Sci Technol 37:193–200CrossRefGoogle Scholar
  8. Cahill LW, McBride BW (1995) Effect of level of intake on digestion, rate of passage and chewing dynamics in hay-fed Bactrian camels. Proc Nutr Adv Group 1:3–35Google Scholar
  9. Clauss M, Lechner-Doll M (2001) Differences in selective reticulo-ruminal particle retention as a key factor in ruminant diversification. Oecologia 129:321–327CrossRefGoogle Scholar
  10. Clauss M, Rössner GE (2014) Old world ruminant morphophysiology, life history, and fossil record: exploring key innovations of a diversification sequence. Ann Zool Fenn 51:80–94CrossRefGoogle Scholar
  11. Clauss M, Schwarm A, Ortmann S, Alber D, Flach EJ, Kühne R, Hummel J, Streich WJ, Hofer H (2004) Intake, ingesta retention, particle size distribution and digestibility in the hippopotamidae. Comp Biochem Physiol A 139:449–459CrossRefGoogle Scholar
  12. Clauss M, Hummel J, Streich WJ (2006) The dissociation of the fluid and particle phase in the forestomach as a physiological characteristic of large grazing ruminants: an evaluation of available, comparable ruminant passage data. Eur J Wildl Res 52:88–98CrossRefGoogle Scholar
  13. Clauss M, Fritz J, Bayer D, Hummel J, Streich WJ, Südekum K-H, Hatt J-M (2009a) Physical characteristics of rumen contents in two small ruminants of different feeding type, the mouflon (Ovis ammon musimon) and the roe deer (Capreolus capreolus). Zoology 112:195–205PubMedCrossRefGoogle Scholar
  14. Clauss M, Fritz J, Bayer D, Nygren K, Hammer S, Hatt J-M, Südekum K-H, Hummel J (2009b) Physical characteristics of rumen contents in four large ruminants of different feeding type, the addax (Addax nasomaculatus), bison (Bison bison), red deer (Cervus elaphus) and moose (Alces alces). Comp Biochem Physiol A 152:398–406CrossRefGoogle Scholar
  15. Clauss M, Nunn C, Fritz J, Hummel J (2009c) Evidence for a tradeoff between retention time and chewing efficiency in large mammalian herbivores. Comp Biochem Physiol A 154:376–382CrossRefGoogle Scholar
  16. Clauss M, Hume ID, Hummel J (2010) Evolutionary adaptations of ruminants and their potential relevance for modern production systems. Animal 4:979–992PubMedCrossRefGoogle Scholar
  17. Clauss M, Lunt N, Ortmann S, Plowman A, Codron D, Hummel J (2011) Fluid and particle passage in three duiker species. Eur J Wildl Res 57:143–148CrossRefGoogle Scholar
  18. Clauss M, Schiele K, Ortmann S, Fritz J, Codron D, Hummel J, Kienzle E (2014) The effect of very low food intake on digestive physiology and forage digestibility in horses. J Anim Physiol Anim Nutr 98:107–118CrossRefGoogle Scholar
  19. Codron D, Clauss M (2010) Rumen physiology constrains diet niche: linking digestive physiology and food selection across wild ruminant species. Can J Zool 88:1129–1138CrossRefGoogle Scholar
  20. Darlis NA, Liang JB, Ho YW (2012) Effects of diets of differing fiber contents on digestibility, passage rate of digesta and heat production in lesser mouse deer (Tragulus javanicus). Mamm Biol 77:385–390Google Scholar
  21. Development Core Team R (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  22. Dittmann MT, Hummel J, Runge U, Galeffi C, Kreuzer M, Clauss M (2014a) Characterising an artiodactyl family inhabiting arid habitats by its metabolism: low metabolism and maintenance requirements in camelids. J Arid Environ 107:41–48CrossRefGoogle Scholar
  23. Dittmann MT, Runge U, Lang RA, Moser D, Galeffi C, Kreuzer M, Clauss M (2014b) Methane emission by camelids. PLoS ONE 9:e94363PubMedCentralPubMedCrossRefGoogle Scholar
  24. Dittmann MT, Hummel J, Hammer S, Arif A, Hebel C, Müller DHW, Fritz J, Steuer P, Schwarm A, Kreuzer M, Clauss M (2015) Digesta retention in gazelles in comparison to other ruminants: evidence for taxon-specific rumen fluid throughput to adjust digesta washing to the natural diet. Comp Biochem Physiol A 185:58–68CrossRefGoogle Scholar
  25. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  26. Frei S, Ortmann S, Reutlinger C, Kreuzer M, Hatt J-M, Clauss M (2015) Comparative digesta retention patterns in ratites. Auk Ornithol Adv 132:119–131Google Scholar
  27. Fritz J, Hummel J, Kienzle E, Arnold C, Nunn C, Clauss M (2009) Comparative chewing efficiency in mammalian herbivores. Oikos 118:1623–1632CrossRefGoogle Scholar
  28. Gordon JG (1968) Rumination and its significance. Wrld Rev Nutr Diet 9:251–273Google Scholar
  29. Grovum WL, Williams VJ (1973) Rate of passage of digesta in sheep: 4. Passage of marker through the alimentary tract and the biological relevance of rate-constants derived from the changes in concentration of marker in faeces. Br J Nutr 30:313–329PubMedCrossRefGoogle Scholar
  30. Hebel C, Ortmann S, Hammer S, Hammer C, Fritz J, Hummel J, Clauss M (2011) Solute and particle retention in the digestive tract of the Phillip’s dikdik (Madoqua saltiana phillipsi), a very small browsing ruminant: biological and methodological implications. Comp Biochem Physiol A 159:284–290CrossRefGoogle Scholar
  31. Heller R, Gregory PC, von Engelhardt W (1984) Pattern of motility and flow of digesta in the forestomach of the llama (Lama guanacoe f. glama). J Comp Physiol B 154:529–533CrossRefGoogle Scholar
  32. Heller R, Cercasov V, von Engelhardt W (1986a) Retention of fluid and particles in the digestive tract of the llama (Lama guanacoe f. glama). Comp Biochem Physiol A 83:687–691PubMedCrossRefGoogle Scholar
  33. Heller R, Lechner M, von Engelhardt W (1986b) Forestomach motility in the camel (Camelus dromedarius). Comp Biochem Physiol A 84:285–288PubMedCrossRefGoogle Scholar
  34. Heller R, Lechner M, Weyreter H, von Engelhardt W (1986c) Forestomach fluid volume and retention time of fluid and particles in the gastrointestinal tract of the camel (Camelus dromedarius). J Vet Med A 33:396–399CrossRefGoogle Scholar
  35. Hendrichs H (1965) Vergleichende Untersuchung des Wiederkauverhaltens. Biol Zentrbl 84:681–751Google Scholar
  36. Hinderer S, von Engelhardt W (1975) Urea metabolism in the llama. Comp Biochem Physiol A 52:619–622PubMedCrossRefGoogle Scholar
  37. Hintz HF, Schryver HF, Halbert M (1973) A note on the comparsion of digestion by new world camels, sheep and ponies. Anim Prod 16:303–305CrossRefGoogle Scholar
  38. Hofmann RR, Streich WJ, Fickel J, Hummel J, Clauss M (2008) Convergent evolution in feeding types: salivary gland mass differences in wild ruminant species. J Morphol 269:240–257PubMedCrossRefGoogle Scholar
  39. Hummel J, Clauss M, Zimmermann W, Johanson K, Norgaard C, Pfeffer E (2005) Fluid and particle retention in captive okapi (Okapia johnstoni). Comp Biochem Physiol A 140:436–444CrossRefGoogle Scholar
  40. Hummel J, Steuer P, Südekum K-H, Hammer S, Hammer C, Streich WJ, Clauss M (2008) Fluid and particle retention in the digestive tract of the addax antelope (Addax nasomaculatus)—adaptations of a grazing desert ruminant. Comp Biochem Physiol A 149:142–149CrossRefGoogle Scholar
  41. Hummel J, Hammer S, Hammer C, Ruf J, Lechenne M, Clauss M (2015) Solute and particle retention in a small grazing antelope, the blackbuck (Antilope cervicapra). Comp Biochem Physiol A 182:22–26CrossRefGoogle Scholar
  42. Hungate RE (1966) The rumen and its microbes. Academic Press, LondonGoogle Scholar
  43. Iqbal A, Khan BB (2001) Feeding behaviour of camel, Review. Pakistan J Agric Sci 38:58–63Google Scholar
  44. Janis CM, Gordon IJ, Illius AW (1994) Modelling equid/ruminant competition in the fossil record. Hist Biol 8:15–29CrossRefGoogle Scholar
  45. Kaske M, Groth A (1997) Changes in factors affecting the rate of digesta passage through pregnancy and lactation in sheep fed on hay. Repr Nutr Dev 37:573–588CrossRefGoogle Scholar
  46. Langer P (1988) The mammalian herbivore stomach. Gustav Fischer, StuttgartGoogle Scholar
  47. Lauper M, Lechner I, Barboza P, Collins W, Hummel J, Codron D, Clauss M (2013) Rumination of different-sized particles in muskoxen (Ovibos moschatus) and moose (Alces alces) on grass and browse diets, and implications for rumination in different ruminant feeding types. Mamm Biol 78:142–152Google Scholar
  48. Lechner I, Barboza P, Collins W, Fritz J, Günther D, Hattendorf B, Hummel J, Südekum K-H, Clauss M (2010) Differential passage of fluids and different-sized particles in fistulated oxen (Bos primigenius f. taurus), muskoxen (Ovibos moschatus), reindeer (Rangifer tarandus) and moose (Alces alces): rumen particle size discrimination is independent from contents stratification. Comp Biochem Physiol A 155:211–222CrossRefGoogle Scholar
  49. Lechner-Doll M, von Engelhardt W (1989) Particle size and passage from the forestomach in camels compared to cattle and sheep fed a similar diet. J Anim Physiol Anim Nutr 61:120–128CrossRefGoogle Scholar
  50. Lechner-Doll M, Rutagwenda T, Schwartz HJ, Schultka W, von Engelhardt W (1990) Seasonal changes of ingesta mean retention time and forestomach fluid volume in indigenous camels, cattle, sheep and goats grazing in a thornbush savanna pasture in Kenya. J Agric Sci 115:409–420CrossRefGoogle Scholar
  51. 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, pp 455–482CrossRefGoogle Scholar
  52. Lechner-Doll M, von Engelhardt W, Abbas HM, Mousa L, Luciano L, Reale E (1995) Particularities in forestomach anatomy, physiology and biochemistry of camelids compared to ruminants. In: Tisserand JL (ed) Elevage et alimentation du dromadaire–Camel production and nutrition Options méditerranéennes, Serie B. Etudes et Recherches Nr. 13 CIHEAM, Paris, pp 19–32Google Scholar
  53. Lentle R, Hemar Y, Hall C (2006) Viscoelastic behaviour aids extrusion from and reabsorption of the liquid phase into the digesta plug: creep rheometry of hindgut digesta in the common brushtail possum Trichosurus vulpecula. J Comp Physiol B 176:469–475PubMedCrossRefGoogle Scholar
  54. Levey D, Martínez del Rio C (1999) Test, rejection and reformulation of a chemical reactor-based model of gut function in a fruit-eating bird. Physiol Biochem Zool 72:369–383PubMedCrossRefGoogle Scholar
  55. Lirette A, Milligan LP (1989) A quantitative model of reticulo-rumen particle degradation and passage. Br J Nutr 62:465–479PubMedCrossRefGoogle Scholar
  56. Logan M (2001) Evidence for the occurence of rumination-like behaviour, or merycism, in koalas (Phascolarctos cinereus). J Zool 255:83–87CrossRefGoogle Scholar
  57. Logan M (2003) Effect of tooth wear on the rumination-like behavior, or merycism, of free-ranging koalas (Phascolarctos cinereus). J Mammal 84:897–902CrossRefGoogle Scholar
  58. Lord RD (1994) A descriptive account of capybara behavior. Stud Neotrop Fauna Environ 29:11–22CrossRefGoogle Scholar
  59. Mambrini M, Peyraud JL (1997) Retention time of feed particles and liquids in the stomachs and intestines of dairy cows. Direct measurement and calculation based on fecal collection. Repr Nutr Dev 37:427–442CrossRefGoogle Scholar
  60. Matsuda I, Murai T, Clauss M, Yamada T, Tuuga A, Bernard H, Higashi S (2011) Regurgitation and remastication in the foregut-fermenting proboscis monkey (Nasalis larvatus). Biol Lett 7:786–789PubMedCentralPubMedCrossRefGoogle Scholar
  61. Matsuda I, Tuuga A, Hashimoto C, Bernard H, Yamagiwa J, Fritz J, Tsubokawa K, Yayota M, Murai T, Iwata Y, Clauss M (2014) Faecal particle size in free-ranging primates supports ‘rumination’ strategy in the proboscis monkey (Nasalis larvatus). Oecologia 174:1127–1137PubMedCrossRefGoogle Scholar
  62. Meyer K, Hummel J, Clauss M (2010) The relationship between forage cell wall content and voluntary food intake in mammalian herbivores. Mammal Rev 40:221–245Google Scholar
  63. Moir RJ, Somers M, Sharman G, Waring H (1954) Ruminant-like digestion in a marsupial. Nature 173:269–270PubMedCrossRefGoogle Scholar
  64. Moir RJ, Somers M, Waring H (1956) Studies on marsupial nutrition. I. Ruminant-like digestion in a herbivorous marsupial. Aust J Biol Sci 9:293–304Google Scholar
  65. Mollison BC (1960) Food regurgitation in Bennett’s wallaby and the scrub wallaby. CSIRO Wildl Res 5:87–88CrossRefGoogle Scholar
  66. Müller DWH, Caton J, Codron D, Schwarm A, Lentle R, Streich WJ, Hummel J, Clauss M (2011) Phylogenetic constraints on digesta separation: variation in fluid throughput in the digestive tract in mammalian herbivores. Comp Biochem Physiol A 160:207–220CrossRefGoogle Scholar
  67. Müller DWH, Codron D, Meloro C, Munn A, Schwarm A, Hummel J, Clauss M (2013) Assessing the Jarman-Bell Principle: scaling of intake, digestibility, retention time and gut fill with body mass in mammalian herbivores. Comp Biochem Physiol A 164:129–140CrossRefGoogle Scholar
  68. Schwarm A, Ortmann S, Wolf C, Streich WJ, Clauss M (2008) Excretion patterns of fluids and particle passage markers of different size in banteng (Bos javanicus) and pygmy hippopotamus (Hexaprotodon liberiensis): two functionally different foregut fermenters. Comp Biochem Physiol A 150:32–39CrossRefGoogle Scholar
  69. Schwarm A, Ortmann S, Wolf C, Clauss M (2009a) No distinct difference in the excretion of large particles of varying size in a wild ruminant, the banteng (Bos javanicus). Eur J Wildl Res 55:531–533CrossRefGoogle Scholar
  70. Schwarm A, Ortmann S, Wolf C, Streich WJ, Clauss M (2009b) More efficient mastication allows increasing intake without compromising digestibility or necessitating a larger gut: comparative feeding trials in banteng (Bos javanicus) and pygmy hippopotamus (Hexaprotodon liberiensis). Comp Biochem Physiol A 152:504–512CrossRefGoogle Scholar
  71. Schwarm A, Ortmann S, Wolf C, Streich WJ, Clauss M (2009c) Passage marker excretion in red kangaroo (Macropus rufus), collared peccary (Pecari tajacu) and colobine monkeys (Colobus angolensis, C. polykomos, Trachypithecus johnii). J Exp Zool A 311:647–661CrossRefGoogle Scholar
  72. Schwarm A, Ortmann S, Fritz J, Rietschel W, Flach EJ, Clauss M (2013) No distinct stratification of ingesta particles and no distinct moisture gradient in the forestomach of nonruminants: the wallaby, peccary, hippopotamus, and sloth. Mamm Biol 78:412–421Google Scholar
  73. Silanikove N (1994) The struggle to maintain hydration and osmoregulation in animals experiencing severe dehydration and rapid rehydration: the story of ruminants. Exp Physiol 79:281–300PubMedCrossRefGoogle Scholar
  74. Sponheimer M, Robinson T, Roeder B, Hammer J, Ayliffe L, Passey B, Cerling T, Dearing D, Ehleringer J (2003) Digestion and passage rates of grass hay by llamas, alpacas, goats, rabbits and horses. Small Rum Res 48:149–154CrossRefGoogle Scholar
  75. Steuer P, Südekum K-H, Müller DWH, Kaandorp J, Clauss M, Hummel J (2013) Fibre digestibility in large herbivores as related to digestion type and body mass - an in vitro approach. Comp Biochem Physiol A 164:319–326CrossRefGoogle Scholar
  76. Sutherland TM (1988) Particle separation in the forestomach of sheep. In: Dobson A, Dobson MJ (eds) Aspects of digestive physiology in ruminants. Cornell University Press, Ithaca, pp 43–73Google Scholar
  77. Thielemans MF, Francois E, Bodart C, Thewis A (1978) Mesure du transit gastrointestinal chez le porc a l’aide des radiolanthanides. Comparaison avec le mouton. Ann Biol Anim Biochim Biophys 18:237–247CrossRefGoogle Scholar
  78. Udén P, Colucci PE, Van Soest PJ (1980) Investigation of chromium, cerium and cobalt as markers in digesta. Rate of passage studies. J Sci Food Agric 31:625–632PubMedCrossRefGoogle Scholar
  79. Vallenas A, Cummings JF, Munnell JF (1971) A gross study of the compartmentalized stomach of two New-World camelids, the llama and guanaco. J Morphol 134:399–424PubMedCrossRefGoogle Scholar
  80. Van Weyenberg S, Sales J, Janssens GPJ (2006) Passage rate of digesta through the equine gastrointestinal tract: a review. Livestock Sci 99:3–12CrossRefGoogle Scholar
  81. von Engelhardt W, Schneider W (1977) Energy and nitrogen metabolism in the llama. Anim Res Dev 5:68–72Google Scholar
  82. von Engelhardt W, Haarmeyer P, Kaske M, Lechner-Doll M (2006a) Chewing activities and oesophageal motility during feed intake, rumination and eructuation in camels. J Comp Physiol B 176:117–124CrossRefGoogle Scholar
  83. von Engelhardt W, Haarmeyer P, Lechner-Doll M (2006b) Feed intake, forestomach fluid volume, dilution rate and mean retention of fluid in the forestomach during water deprivation and rehydration in camels (Camelus sp.). Comp Biochem Physiol A 143:504–507CrossRefGoogle Scholar
  84. Warner ACI (1981) Rate of passage through the gut of mammals and birds. Nutr Abstr Rev B 51:789–820Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Marie T. Dittmann
    • 1
    • 2
  • Ullrich Runge
    • 3
  • Sylvia Ortmann
    • 4
  • Richard A. Lang
    • 5
  • Dario Moser
    • 6
  • Cordula Galeffi
    • 7
  • Angela Schwarm
    • 2
  • Michael Kreuzer
    • 2
  • Marcus Clauss
    • 1
  1. 1.Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty ZurichUniversity of ZurichZurichSwitzerland
  2. 2.ETH ZurichInstitute of Agricultural SciencesZurichSwitzerland
  3. 3.Kamelhof OlmerswilNeukirch/ThurSwitzerland
  4. 4.Leibniz Institute for Zoo and Wildlife Research (IZW)BerlinGermany
  5. 5.Cochranton Veterinary HospitalCochrantonUSA
  6. 6.Zoological InstituteUniversity of BaselBaselSwitzerland
  7. 7.Zurich ZooZurichSwitzerland

Personalised recommendations