ABSTRACT

Herbivores face the dilemma that the level of feed intake is negatively related to factors that determine digestive efficiency, such as thoroughness of ingesta comminution by chewing, and retention of digesta in the digestive tract. Ruminants have evolved particular adaptations to solve this dilemma. Most ruminants share the characteristic of “digesta washing”: fluid moves through their digestive tract faster than particles, thus effectively washing very fine particles, such as bacteria, out of the digesta plug. As the forestomach is followed by auto-enzymatic digestion, this allows a continuous, increased harvest of microbes from the forestomach. True rumination only evolved twice, in the camelids and the true ruminants. These both evolved a density-dependent sorting mechanism based on physical separation of the digesta by the process of flotation and sedimentation, ensuring that the process of rumination is applied to large particles. Differences in this sorting mechanism might facilitate a faster digesta processing in true ruminants as compared with camelids. The hallmark of ruminant digestive anatomy is the omasum, in which the fluid required for both digesta washing and the reticular separation mechanism is re-absorbed. In ruminants of the tribe Bovini, the omasum has reached the largest size and this group has a particularly great forestomach fluid throughput. Increasing the degree of digesta washing even more should increase microbial harvest from the forestomach and reduce the susceptibility to acidosis. At the same time, it should result in a metabolic state of the microbiome more tuned towards biomass production and less towards methanogenesis. Enhancing the forestomach fluid throughput by selective breeding could represent a promising way to further advance the productivity of the ruminant digestive tract.

cattle; digesta washing; foregut fermenter; microbial harvest; microbiome

Introduction

Domestic ruminants are special. In contrast to domestic pigs, camelids, or horses, they belong to a family (Bovidae) that comprises an enormous extant variety of more than 100 species (Fritz et al., 2009bFritz, S. A.; Bininda-Emonds, O. R. and Purvis, A. 2009b. Geographical variation in predictors of mammalian extinction risk: big is bad, but only in the tropics. Ecology Letters 12:538-549.). This difference in species diversity between bovids on the one hand, and suids, camelids, or equids on the other hand, has been interpreted as a result of a displacement of previously more speciose large herbivore groups by ruminants (Janis et al., 1994Janis, C. M.; Gordon, I. J. and Illius, A. W. 1994. Modelling equid/ruminant competition in the fossil record. Historical Biology 8:15-29.). Ruminant species cover a large variety of ecological niches and hence display a large variety of morphophysiological adaptations (Hofmann, 1989Hofmann, R. R. 1989. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78:443-457.; Kay, 1989Kay, R. N. B. 1989. Adaptation of the ruminant digestive tract to diet. Acta Veterinaria Scandinavica 86(Suppl.):196-203.; Woodall and Skinner, 1993Woodall, P. F. and Skinner, J. D. 1993. Dimensions of the intestine, diet and faecal water loss in some African antelope. Journal of Zoology 229:457-471.; Beuchat, 1996Beuchat, C. A. 1996. Structure and concentrating ability of the mammalian kidney: correlations with habitat. American Journal of Physiology 271:R157-R179.; Cain et al., 2006Cain, J. W.; Krausman, P. R.; Rosenstock, S. S. and Turner, J. C. 2006. Mechanisms of thermoregulation and water balance in desert ungulates. Wildlife Society Bulletin 34:570-581.; Zerbe et al., 2012Zerbe, P.; Clauss, M.; Codron, D.; Bingaman Lackey, L.; Rensch, E.; Streich, W. J.; Hatt, J.-M. and Müller, D. W. H. 2012. Reproductive seasonality in captive wild ruminants: implications for biogeographical adaptation, photoperiodic control, and life history. Biological Reviews 87:965-990.). On the one hand, certain production systems, in particular more extensive systems, sometimes might benefit from employing this existing variety of ruminant species to increase the overall efficiency of resource use (Arsenault and Owen-Smith, 2002Arsenault, R. and Owen-Smith, N. 2002. Facilitation versus competition in grazing herbivore assemblages. Oikos 97:313-318.; Odadi et al., 2011Odadi, W. O.; Karachi, M. K.; Abdulrazak, S. A. and Young, T. P. 2011. African wild ungulates compete with or facilitate cattle depending on season. Science 333:1753-1755.; Riginos et al., 2012Riginos, C.; Porensky, L. M.; Veblen, K. E.; Odadi, W. O.; Sensenig, R. L.; Kimuyu, D.; Keesing, F.; Wilkerson, M. L. and Young, T. P. 2012. Lessons on the relationship between livestock husbandry and biodiversity from the Kenya Long-term Exclosure Experiment (KLEE). Pastoralism 2:1-22.), but not always (Prins and Fritz, 2008Prins, H. H. T. and Fritz, H. 2008. Species diversity of browsing and grazing ungulates: consequences for the structure and abundance of secondary production. p.179-200. In: The ecology of browsing and grazing. Gordon, I. J. and Prins, H. H. T., eds. Springer, Berlin Heidelberg.). On the other hand, one could consider the variety of existing ruminant morphophysiologies as a pool from which one might choose certain traits as targets for selective breeding in domestic ruminant breeding programs (Clauss et al., 2010bClauss, M.; Hume, I. D. and Hummel, J. 2010b. Evolutionary adaptations of ruminants and their potential relevance for modern production systems. Animal 4:979-992.). This short review is concerned with this latter option.

In particular, our approach focuses on digestive physiology. Evidently, any characteristic could be chosen as a target for selective breeding. For example, given the variety of dental traits (Archer and Sanson, 2002Archer, D. and Sanson, G. 2002. Form and function of the selenodont molar in southern African ruminants in relation to their feeding habits. Journal of Zoology 257:13-26.; Heywood, 2010Heywood, J. J. N. 2010. Functional anatomy of bovid upper molar occlusal surfaces with respect to diet. Journal of Zoology 281:1-11.; Kaiser et al., 2010Kaiser, T. M.; Fickel, J.; Streich, W. J.; Hummel, J. and Clauss, M. 2010. Enamel ridge alignment in upper molars of ruminants in relation to their natural diet. Journal of Zoology 281:12-25.) and hypsodonty (Mendoza et al., 2002Mendoza, M.; Janis, C. M. and Palmqvist, P. 2002. Characterizing complex craniodental patterns related to feeding behaviour in ungulates: a multivariate approach. Journal of Zoology 258:223-246.; Damuth and Janis, 2011Damuth, J. and Janis, C. M. 2011. On the relationship between hypsodonty and feeding ecology in ungulate mammals, and its utility in palaeoecology. Biological Reviews 86:733-758.; Jordana et al., 2012Jordana, X.; Marín-Moratalla, N.; DeMiguel, D.; Kaiser, T. M. and Köhler, M. 2012. Evidence of correlated evolution of hypsodonty and exceptional longevity in endemic insular mammals. Proceedings of the Royal Society B 279:3339-3346.) in ruminants, one could consider breeding domestic ruminants for more complex and higher-crowned teeth, if there was evidence that the production potential of domestic ruminants was constrained by the durability of their teeth. Given the variety of muzzle width (Gordon and Illius, 1988Gordon, I. J. and Illius, A. W. 1988. Incisor arcade structure and diet selection in ruminants. Functional Ecology 2:15-22.; Janis and Ehrhardt, 1988Janis, C. M. and Ehrhardt, D. 1988. Correlation of the relative muzzle width and relative incisor width with dietary preferences in ungulates. Zoological Journal of the Linnean Society 92:267-284.; Tennant and MacLeod, 2014Tennant, J. P. and MacLeod, N. 2014. Snout shape in extant ruminants. PLoS One 9:e112035.) in ruminants, one could consider breeding domestic ruminants for wider muzzles to enhance their foraging efficiency, if muzzle width was identified as a constraint. The focus we place herein on digestive physiology is, at the moment, a subjective one.

Basic ruminant digestive physiology

Herbivore digestive physiology can be conceptualized as the dilemma to maximize feed intake while also maximizing diet quality and diet digestibility (Hume, 2005Hume, I. D. 2005. Concepts of digestive efficiency. p.43-58. In: Physiological and ecological adaptations to feeding in vertebrates. Starck, J. M. and Wang, T., eds. Science Publishers, Enfield NH.). The level of feed intake is typically negatively related with digesta mean retention time (Müller et al., 2013Müller, D. W. H.; Codron, D.; Meloro, C.; Munn, A.; Schwarm, A.; Hummel, J. and Clauss, M. 2013. Assessing the Jarman-Bell Principle: scaling of intake, digestibility, retention time and gut fill with body mass in mammalian herbivores. Comparative Biochemistry and Physiology A 164:129-140.), a major determinant of digestibility. The intake-retention time relationship can be modulated by gut capacity (Clauss et al., 2007Clauss, M.; Streich, W. J.; Schwarm, A.; Ortmann, S. and Hummel, J. 2007. The relationship of food intake and ingesta passage predicts feeding ecology in two different megaherbivore groups. Oikos 116:209-216.) and the retention time-digestibility relationship can be modulated by particle size reduction (i.e., chewing efficiency; Clauss et al., 2009dClauss, M.; Nunn, C.; Fritz, J. and Hummel, J. 2009d. Evidence for a tradeoff between retention time and chewing efficiency in large mammalian herbivores. Comparative Biochemistry and Physiology A 154:376-382.).

The exceptional reduction of ingesta particle size that functional ruminants achieve is the hallmark of ruminant digestive physiology (Fritz et al., 2009aFritz, J.; Hummel, J.; Kienzle, E.; Arnold, C.; Nunn, C. and Clauss, M. 2009a. Comparative chewing efficiency in mammalian herbivores. Oikos 118:1623-1632.), which allows them to increase intake (as compared with non-ruminant foregut fermenters) without compromising digestibility (Schwarm et al., 2009Schwarm, A.; Ortmann, S.; Wolf, C.; Streich, W. J. and Clauss, M. 2009. 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). Comparative Biochemistry and Physiology A 152:504-512.; Clauss et al., 2015Clauss, M.; Steuer, P.; Erlinghagen-Lückerath, K.; Kaandorp, J.; Fritz, J.; Südekum, K.-H. and Hummel, J. 2015. Faecal particle size: digestive physiology meets herbivore diversity. Comparative Biochemistry and Physiology A 179:182-191.). This increased chewing efficiency is not achieved by a particular dental design, but by a density-depending sorting mechanism in the forestomach, which separates the small particles from the large ones that are then regurgitated to be masticated again (i.e., rumination) (Lechner-Doll et al., 1991Lechner-Doll, M.; Kaske, M. and von Engelhardt, W. 1991. Factors affecting the mean retention time of particles in the forestomach of ruminants and camelids. p.455-482. In: Physiological aspects of digestion and metabolism in ruminants. Tsuda, T.; Sasaki, Y. and Kawashima, R., eds. Academic Press, San Diego CA.). Although merycism (i.e., regurgitation and re-mastication) and the presence of comparatively fine digesta particles have been reported in non-ruminant foregut fermenters such as kangaroos (Schwarm et al., 2013Schwarm, A.; Ortmann, S.; Fritz, J.; Rietschel, W.; Flach, E. J. and 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. Mammalian Biology 78:412-421.; Vendl et al., 2017Vendl, C.; Munn, A.; Leggett, K. and Clauss, M. 2017. Merycism in western grey (Macropus fuliginosus) and red kangaroos (Macropus rufus). Mammalian Biology 86:21-26.) and proboscic monkeys (Nasalis larvatus) (Matsuda et al., 2011Matsuda, I.; Murai, T.; Clauss, M.; Yamada, T.; Tuuga, A.; Bernard, H. and Higashi, S. 2011. Regurgitation and remastication in the foregut-fermenting proboscis monkey (Nasalis larvatus). Biology Letters 7:786-789.; Matsuda et al., 2014Matsuda, I.; Tuuga, A.; Hashimoto, C.; Bernard, H.; Yamagiwa, J.; Fritz, J.; Tsubokawa, K.; Yayota, M.; Murai, T.; Iwata, Y. and Clauss, M. 2014. Faecal particle size in free-ranging primates supports ‘rumination’ strategy in the proboscis monkey (Nasalis larvatus). Oecologia 174:1127-1137.), true rumination linked to a sorting mechanism and with a physiologically fixed motor sequence (Gordon, 1968Gordon, J. G. 1968. Rumination and its significance. World Review of Nutrition and Dietetics 9:251-273.) only evolved twice, in the camelids and the taxonomic ruminants. While there appears to be no functional difference in the forestomach particle sorting mechanism between these two functional ruminant groups (Dittmann et al., 2015bDittmann, M. T.; Runge, U.; Ortmann, S.; Lang, R. A.; Moser, D.; Galeffi, C.; Schwarm, A.; Kreuzer, M. and Clauss, M. 2015b. Digesta retention patterns of solutes and different-sized particles in camelids compared with ruminants and other foregut fermenters. Journal of Comparative Physiology B 185:559-573.), a major difference between them is the generally lower metabolism and lower feed intake in camelids (Dittmann et al., 2014Dittmann, M. T.; Hummel, J.; Runge, U.; Galeffi, C.; Kreuzer, M. and Clauss, M. 2014. Characterising an artiodactyl family inhabiting arid habitats by its metabolism: low metabolism and maintenance requirements in camelids. Journal of Arid Environments 107:41-48.). This may be linked to a less efficient morphophysiological design of their sorting mechanism (Dittmann et al., 2014Dittmann, M. T.; Hummel, J.; Runge, U.; Galeffi, C.; Kreuzer, M. and Clauss, M. 2014. Characterising an artiodactyl family inhabiting arid habitats by its metabolism: low metabolism and maintenance requirements in camelids. Journal of Arid Environments 107:41-48.; Dittmann et al., 2015bDittmann, M. T.; Runge, U.; Ortmann, S.; Lang, R. A.; Moser, D.; Galeffi, C.; Schwarm, A.; Kreuzer, M. and Clauss, M. 2015b. Digesta retention patterns of solutes and different-sized particles in camelids compared with ruminants and other foregut fermenters. Journal of Comparative Physiology B 185:559-573.; Pérez et al., 2016Pérez, W.; König, H. E.; Jerbi, H. and Clauss, M. 2016. Macroanatomical aspects of the gastrointestinal tract of the alpaca (Vicugna pacos) and dromedary (Camelus dromedarius). Vertebrate Zoology 66:419-425.); however, conclusive physiological studies are lacking.

In taxonomic ruminants, the particle sorting mechanism is based on a flotation-sedimentation mechanism in the reticulum (Sutherland, 1988Sutherland, T. M. 1988. Particle separation in the forestomach of sheep. p.43-73. In: Aspects of digestive physiology in ruminants. Dobson, A. and Dobson, M. J., eds. Cornell University Press, Ithaca, NY.; Baumont and Deswysen, 1991Baumont, R. and Deswysen, A. G. 1991. Mélange et propulsion du contenu du réticulo-rumen. Reproduction Nutrition Development 31:335-359.), for which a high moisture content is an important prerogative (Clauss et al., 2009bClauss, M.; Fritz, J.; Bayer, D.; Nygren, K.; Hammer, S.; Hatt, J.-M.; Südekum, K.-H. and 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). Comparative Biochemistry and Physiology A 152:398-406.; Hummel et al., 2009Hummel, J.; Südekum, K.-H.; Bayer, D.; Ortmann, S.; Hatt, J.-M.; Streich, W. J. and Clauss, M. 2009. Physical characteristics of reticuloruminal contents of cattle in relation to forage type and time after feeding. Journal of Animal Physiology and Animal Nutrition 93:209-220.; Clauss et al., 2017Clauss, M.; Fritz, J.; Tschuor, A.; Braun, U.; Hummel, J. and Codron, D. 2017. Dry matter and digesta particle size gradients along the goat digestive tract on grass and browse diets. Journal of Animal Physiology and Animal Nutrition 101:61-69.). The sorting mechanism automatically leads to the outflow of the fluid from the reticulum together with small particles. This fluid could represent a burden on the enzyme-secreting function of the abomasum and small intestine (that would have to compensate for the dilution effect with increased secretion rates). The omasum has been interpreted as the organ that reabsorbs this fluid and hence facilitates an efficient sorting mechanism and a great fluid throughput linked to high feed intake (Clauss and Rössner, 2014Clauss, M. and Rössner, G. E. 2014. Old world ruminant morphophysiology, life history, and fossil record: exploring key innovations of a diversification sequence. Annales Zoologici Fennici 51:80-94.).

With this great fluid throughput, the ruminant forestomach displays a similar characteristic to most other foregut fermenters (with the exception of primates): a relatively faster movement of fluid vs. particles, (i.e., a “washing” or “flushing” of the forestomach contents; Müller et al., 2011Müller, D. W. H.; Caton, J.; Codron, D.; Schwarm, A.; Lentle, R.; Streich, W. J.; Hummel, J. and Clauss, M. 2011. Phylogenetic constraints on digesta separation: variation in fluid throughput in the digestive tract in mammalian herbivores. Comparative Biochemistry and Physiology A 160:207-220.). It has been claimed that an important effect of such a “digesta washing” is the efficient harvest of microbes from the forestomach (Hummel et al., 2008bHummel, J.; Steuer, P.; Südekum, K.-H.; Hammer, S.; Hammer, C.; Streich, W. J. and Clauss, M. 2008b. Fluid and particle retention in the digestive tract of the addax antelope (Addax nasomaculatus) – adaptations of a grazing desert ruminant. Comparative Biochemistry and Physiology A 149:142-149.; Müller et al., 2011Müller, D. W. H.; Caton, J.; Codron, D.; Schwarm, A.; Lentle, R.; Streich, W. J.; Hummel, J. and Clauss, M. 2011. Phylogenetic constraints on digesta separation: variation in fluid throughput in the digestive tract in mammalian herbivores. Comparative Biochemistry and Physiology A 160:207-220.; Hummel et al., 2015Hummel, J.; Hammer, S.; Hammer, C.; Ruf, J.; Lechenne, M. and Clauss, M. 2015. Solute and particle retention in a small grazing antelope, the blackbuck (Antilope cervicapra). Comparative Biochemistry and Physiology A 182:22-26.).

Comparative ruminant digestive morphophysiology

Although morphological differences of the digestive tract between ruminant species had been known for a long time (Garrod, 1877Garrod, A. H. 1877. Notes on the visceral anatomy and osteology of the ruminants, with a suggestion regarding a method of expressing the relations of species by means of formulae. Proceedings of the Zoological Society of London:2-18.; Neuville and Derscheid, 1929Neuville, H. and Derscheid, J. M. 1929. Recherches anatomiques sur l’okapi (Okapia johnstoni). IV. L’estomac. Revue de Zoologie et de Botanique Africaine 16:373-419.; Langer, 1973Langer, P. 1973. Vergleichend-anatomische Untersuchungen am Magen der Artiodactyla. II. Untersuchungen am Magen der Tylopoda und Ruminantia. Gegenbaurs Morphologisches Jahrbuch 119:633-695.), it was the seminal, comparative works of Hofmann (1973Hofmann, R. R. 1973. The ruminant stomach. East African Literature Bureau, Nairobi.; 1988; 1989) and, to a less well-known extent, of Kay (1989)Kay, R. N. B. 1989. Adaptation of the ruminant digestive tract to diet. Acta Veterinaria Scandinavica 86(Suppl.):196-203., that placed these differences in a comprehensive ecological framework. This framework suggested convergences between feeding types (browser, intermediate feeder, grazer). Many of the resulting hypotheses were later corroborated by statistical evaluations (Pérez-Barbería et al., 2004Pérez-Barbería, F. J.; Elston, D. A.; Gordon, I. J. and Illius, A. W. 2004. The evolution of phylogenetic differences in the efficiency of digestion in ruminants. Proceedings of the Royal Society B 271:1081-1090.; Clauss et al., 2008aClauss, M.; Hofmann, R. R.; Streich, W. J.; Fickel, J. and Hummel, J. 2008a. Higher masseter mass in grazing than in browsing ruminants. Oecologia 157:377-385.; Meier et al., 2016Meier, A. R.; Schmuck, U.; Meloro, C.; Clauss, M. and Hofmann, R. R. 2016. Convergence of macroscopic tongue anatomy in ruminants and scaling relationships with body mass or tongue length. Journal of Morphology 277:351-362.). However, in many cases, correlations of investigated characteristics with the percentage of grass in the natural diet included substantial scatter, though being significant. The major challenge in these studies was not the statistical evaluation, but the development of an explanatory concept of biological validity.

Explanatory approach I: fibre content of forages

In the initial concept, Hofmann (1989)Hofmann, R. R. 1989. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78:443-457. considered the major difference between grass and browse to be the general fibre concentration, with lower values in browse. However, empirical data on the fibre concentration in rumen contents in specimens of different feeding types did not support this hypothesis (Woodall, 1992Woodall, P. F. 1992. An evaluation of a rapid method for estimating digestibility. African Journal of Ecology 30:181-185.). Instead, the proportions of different fibre types (hemicellulose, cellulose, lignin) were demonstrated to differ between grass and browse forages, as well as the fermentation behaviour of these forages (Hummel et al., 2006Hummel, J.; Südekum, K.-H.; Streich, W. J. and Clauss, M. 2006. Forage fermentation patterns and their implications for herbivore ingesta retention times. Functional Ecology 20:989-1002.). This in turn links to hypotheses of grazers requiring longer digesta retention times and hence a larger rumen (Clauss et al., 2003Clauss, M.; Lechner-Doll, M. and Streich, W. J. 2003. Ruminant diversification as an adaptation to the physicomechanical characteristics of forage. A reevaluation of an old debate and a new hypothesis. Oikos 102:253-262.; Clauss et al., 2010aClauss, M.; Hofmann, R. R.; Streich, W. J.; Fickel, J. and Hummel, J. 2010a. Convergence in the macroscopic anatomy of the reticulum in wild ruminant species of different feeding types and a new resulting hypothesis on reticular function. Journal of Zoology 281:26-38.). However, many other differences between grazers and browsers cannot be logically linked to fibre characteristics. For example, there is no logical concept why a high-fibre diet should be linked to small salivary glands or why a low-fibre diet should be linked to a more voluminous large intestine, as proposed in Hofmann (1989)Hofmann, R. R. 1989. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78:443-457..

Explanatory approach II: various characteristics of forages and different niche characteristics

Various differences between forages might be linked to differences characterising the anatomy and physiology of browsers and grazers. Among these properties of forages might be their growth form, their spatial arrangement, the heterogeneity of their harvestable units, their physical resistance to mastication, and their content of phytoliths and secondary plant compounds (reviewed in Clauss et al., 2008bClauss, M.; Kaiser, T. and Hummel, J. 2008b. The morphophysiological adaptations of browsing and grazing mammals. p.47-88. In: The ecology of browsing and grazing. Gordon, I. J. and Prins, H. H. T., eds. Springer, Heidelberg.). Corresponding adaptations of ruminants include those related to oral and dental processing (Archer and Sanson, 2002Archer, D. and Sanson, G. 2002. Form and function of the selenodont molar in southern African ruminants in relation to their feeding habits. Journal of Zoology 257:13-26.; Clauss et al., 2008aClauss, M.; Hofmann, R. R.; Streich, W. J.; Fickel, J. and Hummel, J. 2008a. Higher masseter mass in grazing than in browsing ruminants. Oecologia 157:377-385.; Heywood, 2010Heywood, J. J. N. 2010. Functional anatomy of bovid upper molar occlusal surfaces with respect to diet. Journal of Zoology 281:1-11.; Kaiser et al., 2010Kaiser, T. M.; Fickel, J.; Streich, W. J.; Hummel, J. and Clauss, M. 2010. Enamel ridge alignment in upper molars of ruminants in relation to their natural diet. Journal of Zoology 281:12-25.; Meier et al., 2016Meier, A. R.; Schmuck, U.; Meloro, C.; Clauss, M. and Hofmann, R. R. 2016. Convergence of macroscopic tongue anatomy in ruminants and scaling relationships with body mass or tongue length. Journal of Morphology 277:351-362.) or behavioural foraging strategies (Searle and Shipley, 2008Searle, K. R. and Shipley, L. A. 2008. The comparative feeding bahaviour of large browsing and grazing herbivores. p.117-148. In: The ecology of browsing and grazing mammals. Gordon, I. J. and Prins, H. H. T., eds. Springer, Heidelberg.). Other components of observed differences that had also been originally linked to the feeding type differences, such as the length of intestinal sections (Hofmann, 1989Hofmann, R. R. 1989. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78:443-457.), were probably best explained by concepts completely unrelated to feeding types (Woodall and Skinner, 1993Woodall, P. F. and Skinner, J. D. 1993. Dimensions of the intestine, diet and faecal water loss in some African antelope. Journal of Zoology 229:457-471.).

Explanatory approach III: a cohesive set of observations

Evident relationships between plant properties and the oral and dental processing apparatus notwithstanding, the observed differences between species in the anatomy and physiology of the forestomach and related structures still begged for a coherent explanation. In terms of anatomy, these included drastic differences in salivary gland size (Hofmann et al., 2008Hofmann, R. R.; Streich, W. J.; Fickel, J.; Hummel, J. and Clauss, M. 2008. Convergent evolution in feeding types: salivary gland mass differences in wild ruminant species. Journal of Morphology 269:240-257.), intraruminal papillae distribution (Clauss et al., 2009cClauss, M.; Hofmann, R. R.; Fickel, J.; Streich, W. J. and Hummel, J. 2009c. The intraruminal papillation gradient in wild ruminants of different feeding types: implications for rumen physiology. Journal of Morphology 270:929-942.), height of the reticular crests (Clauss et al., 2010aClauss, M.; Hofmann, R. R.; Streich, W. J.; Fickel, J. and Hummel, J. 2010a. Convergence in the macroscopic anatomy of the reticulum in wild ruminant species of different feeding types and a new resulting hypothesis on reticular function. Journal of Zoology 281:26-38.), or omasum size (Clauss et al., 2006aClauss, M.; Hofmann, R. R.; Hummel, J.; Adamczewski, J.; Nygren, K.; Pitra, C.; Streich, W. J. and Reese, S. 2006a. The macroscopic anatomy of the omasum of free-ranging moose (Alces alces) and muskoxen (Ovibos moschatus) and a comparison of the omasal laminal surface area in 34 ruminant species. Journal of Zoology 270:346-358.). In terms of physiology, these related mainly to distinct differences in the relative retention times of fluids and particles in the reticulorumen (Hummel et al., 2005Hummel, J.; Clauss, M.; Zimmermann, W.; Johanson, K.; Norgaard, C. and Pfeffer, E. 2005. Fluid and particle retention in captive okapi (Okapia johnstoni). Comparative Biochemistry and Physiology A 140:436-444.; Clauss et al., 2006bClauss, M.; Hummel, J. and Streich, W. J. 2006b. 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. European Journal of Wildlife Research 52:88-98.; Dittmann et al., 2015aDittmann, M. T.; Hummel, J.; Hammer, S.; Arif, A.; Hebel, C.; Müller, D. H. W.; Fritz, J.; Steuer, P.; Schwarm, A.; Kreuzer, M. and Clauss, M. 2015a. Digesta retention in gazelles in comparison to other ruminants: Evidence for taxon-specific rumen fluid throughput to adjust digesta washing to the natural diet. Comparative Biochemistry and Physiology A 185:58-68.). In the analyses of the adaptive values of these characteristics, we recently introduced the terms “moose-type” and “cattle-type” ruminants. Moose-type species are characterised by a low throughput of relatively viscous fluid (produced by large salivary glands) and a corresponding lack of stratification of rumen contents and intraruminal papillae gradient, low reticular crests, and small omasa. Cattle-type ruminants are characterised by a high throughput of a non-viscous fluid (produced by small salivary glands) and corresponding well-stratified rumen contents and an intraruminal papillae gradient, higher reticular crests, and larger omasa (to absorb the higher amount of fluid passing through the reticulorumen; cattle-type) (Clauss et al., 2010bClauss, M.; Hume, I. D. and Hummel, J. 2010b. Evolutionary adaptations of ruminants and their potential relevance for modern production systems. Animal 4:979-992.). We chose this terminology to avoid circular reasoning when comparing the botanical composition of the diet (“browser-grazer diet”) with the adaptations of the species (“browser-grazer anatomy/physiology”).

Explanatory approach IIIa: maximizing stratification?

A first hypothesis developed to explain these patterns was based on the finding that rumen contents of a browser did not seem to stratify in vivo as previously reported for grazers (Clauss et al., 2001Clauss, M.; Lechner-Doll, M.; Behrend, A.; Lason, K.; Lang, D. and Streich, W. J. 2001. Particle retention in the forestomach of a browsing ruminant, the roe deer (Capreolus capreolus). Acta Theriologica 46:103-107.) and that, in captivity, browsing ruminants had larger faecal particles (i.e. a lesser particle size reduction efficiency) than grazing ruminants (Clauss et al., 2002Clauss, M.; Lechner-Doll, M. and Streich, W. J. 2002. Faecal particle size distribution in captive wild ruminants: an approach to the browser/grazer dichotomy from the other end. Oecologia 131:343-349.). We note that both findings have been corrected since (Hummel et al., 2008aHummel, J.; Fritz, J.; Kienzle, E.; Medici, E. P.; Lang, S.; Zimmermann, W.; Streich, W. J. and Clauss, M. 2008a. Differences in fecal particle size between free-ranging and captive individuals of two browser species. Zoo Biology 27:70-77.; Clauss et al., 2009aClauss, M.; Fritz, J.; Bayer, D.; Hummel, J.; Streich, W. J.; Südekum, K.-H. and 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 112:195-205.; Clauss et al., 2009bClauss, M.; Fritz, J.; Bayer, D.; Nygren, K.; Hammer, S.; Hatt, J.-M.; Südekum, K.-H. and 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). Comparative Biochemistry and Physiology A 152:398-406.). Based on those early observations, a theory was developed that linked the throughput of great amounts of a low-viscosity fluid in cattle-type ruminants to adaptations whose ultimate objective was considered to be the enhancement of the natural tendency of grass forage to stratify in the rumen, thus facilitating a more efficient selective particle retention, size reduction via rumination, and hence digestibility (Clauss et al., 2003Clauss, M.; Lechner-Doll, M. and Streich, W. J. 2003. Ruminant diversification as an adaptation to the physicomechanical characteristics of forage. A reevaluation of an old debate and a new hypothesis. Oikos 102:253-262.; Clauss et al., 2008bClauss, M.; Kaiser, T. and Hummel, J. 2008b. The morphophysiological adaptations of browsing and grazing mammals. p.47-88. In: The ecology of browsing and grazing. Gordon, I. J. and Prins, H. H. T., eds. Springer, Heidelberg.). When this theory was tested experimentally, however, results indicated that the particle retention and sorting mechanism did not differ fundamentally between a moose-type and a cattle-type species, even though differences in rumen content stratification, rumen fluid viscosity, and the relative rumen fluid throughput could be demonstrated (Lechner et al., 2010Lechner, I.; Barboza, P.; Collins, W.; Fritz, J.; Günther, D.; Hattendorf, B.; Hummel, J.; Südekum, K.-H. and 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. Comparative Biochemistry and Physiology A 155:211-222.; Clauss et al., 2011Clauss, M.; Lechner, I.; Barboza, P.; Collins, W.; Tervoort, T.; Südekum, K.-H.; Codron, D. and Hummel, J. 2011. The effect of size and density on the mean retention time of particles in the reticulorumen of cattle (Bos primigenius f. taurus), muskoxen (Ovibos moschatus) and moose (Alces alces). British Journal of Nutrition 105:634-644.; Lauper et al., 2013Lauper, M.; Lechner, I.; Barboza, P.; Collins, W.; Hummel, J.; Codron, D. and 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. Mammalian Biology 78:142-152.).

Explanatory approach IIIb: optimizing microbial harvest

Since then, our explanatory focus for the observed differences in fluid throughput and stratification has been on an optimization of digesta washing and hence harvest of microbes from the forestomach. This idea was first proposed by Hummel et al. (2008b)Hummel, J.; Steuer, P.; Südekum, K.-H.; Hammer, S.; Hammer, C.; Streich, W. J. and Clauss, M. 2008b. Fluid and particle retention in the digestive tract of the addax antelope (Addax nasomaculatus) – adaptations of a grazing desert ruminant. Comparative Biochemistry and Physiology A 149:142-149. and has been elaborated since (Clauss et al., 2010bClauss, M.; Hume, I. D. and Hummel, J. 2010b. Evolutionary adaptations of ruminants and their potential relevance for modern production systems. Animal 4:979-992.; Müller et al., 2011Müller, D. W. H.; Caton, J.; Codron, D.; Schwarm, A.; Lentle, R.; Streich, W. J.; Hummel, J. and Clauss, M. 2011. Phylogenetic constraints on digesta separation: variation in fluid throughput in the digestive tract in mammalian herbivores. Comparative Biochemistry and Physiology A 160:207-220.; Dittmann et al., 2015aDittmann, M. T.; Hummel, J.; Hammer, S.; Arif, A.; Hebel, C.; Müller, D. H. W.; Fritz, J.; Steuer, P.; Schwarm, A.; Kreuzer, M. and Clauss, M. 2015a. Digesta retention in gazelles in comparison to other ruminants: Evidence for taxon-specific rumen fluid throughput to adjust digesta washing to the natural diet. Comparative Biochemistry and Physiology A 185:58-68.). Hummel et al. (2015)Hummel, J.; Hammer, S.; Hammer, C.; Ruf, J.; Lechenne, M. and Clauss, M. 2015. Solute and particle retention in a small grazing antelope, the blackbuck (Antilope cervicapra). Comparative Biochemistry and Physiology A 182:22-26. demonstrated with an example calculation that because of the digesta washing effect, cattle-type ruminants could have a 10% higher microbial efficiency, quantified as the amount of microbial nitrogen produced in the rumen per unit of fermented organic matter.

The concept suggests that moose-type ruminants have adopted a strategy of defending themselves against secondary plant compounds by salivary tannin-binding proteins, which render the saliva comparatively viscous. Because the production of these proteins becomes the limiting step in saliva release, they have large salivary glands; yet, they do not achieve great amounts of saliva output. Lower amounts of saliva in combination with a high saliva viscosity reduce the tendency of rumen contents to stratify. Therefore, they lead to a homogenous intraruminal papillae formation pattern, make lower reticular crests understandable (to avoid complete emptying during reticular contractions that would cause a slow refilling of the reticulum because of the small amount of viscous saliva available), and do not require considerable omasal tissue for re-absorption (Clauss et al., 2010bClauss, M.; Hume, I. D. and Hummel, J. 2010b. Evolutionary adaptations of ruminants and their potential relevance for modern production systems. Animal 4:979-992.).

Such moose-type ruminants are typically browsers. However, among the cattle-type ruminants, there is no clear association between the degree by which their characteristics are expressed and the percentage of grass in their natural diet (Codron and Clauss, 2010Codron, D. and Clauss, M. 2010. Rumen physiology constrains diet niche: linking digestive physiology and food selection across wild ruminant species. Canadian Journal of Zoology 88:1129-1138.). In other words, the most extreme grazers are not necessarily the most extreme cattle-type ruminants. This was exemplified by Clauss and Hofmann (2014)Clauss, M. and Hofmann, R. R., 2014. The digestive system of ruminants, and peculiarities of (wild) cattle. p.57-62. In: Ecology, evolution and behaviour of wild cattle: implications for conservation. Melletti, M.; Burton, J., eds. Cambridge University Press, Cambridge UK. listing a series of species from the taxonomic group of cattle, which have the most prominent cattle-type characteristics, yet consume higher amounts of browse (i.e., more “intermediate-type” diets) than strict grazers. This seeming contradiction could be resolved if the focus is no longer placed on adaptations to properties of the respective forages (grass or browse). Rather, we think that it is more promising to put the focus on an optimization of microbial harvest, which may be beneficial on any kind of forage. This new concept considers the different cattle-type ruminants as different stages in an evolution towards optimized microbial harvest from the forestomach.

Digesta washing, microbial harvest, microbial metabolism

A variety of in vitro assays (Isaacson et al., 1975Isaacson, H. R.; Hinds, F. C.; Bryant, M. P. and Owens, F. N. 1975. Efficiency of energy utilization by mixed rumen bacteria in continuous culture. Journal of Dairy Science 58:1645-1659.; Meng et al., 1999Meng, Q.; Kerley, M. S.; Ludden, P. A. and Belyea, R. L. 1999. Fermentation substrate and dilution rate interact to affect microbial growth and efficiency. Journal of Animal Science 77:206-214.; Fondevila and Pérez-Espés, 2008Fondevila, M. and Pérez-Espés, B. 2008. A new in vitro system to study the effect of liquid phase turnover and pH on microbial fermentation of concentrate diets for ruminants. Animal Feed Science and Technology 144:196-211.) and in vivo experiments with domestic ruminants (Harrison et al., 1975Harrison, D. G.; Beever, D. E.; Thomson, D. J. and Osbourn, D. F. 1975. Manipulation of rumen fermentation in sheep by increasing the rate of flow of water from the rumen. Journal of Agricultural Science, Cambridge 85:93-101.; Wiedmeier et al., 1987bWiedmeier, R. D.; Arambel, M. J. and Walters, J. L. 1987b. Effect of orally administered pilocarpine on ruminal characteristics and nutrient digestibility in cattle. Journal of Dairy Science 70:284-289.; Froetschel et al., 1989Froetschel, M. A.; Amos, H. E.; Evans, J. J.; Croom, W. J. and Hagler, W. M. 1989. Effects of a salivary stimulant, slaframine, on ruminal fermentation, bacterial protein synthesis and digestion in frequently fed steers. Journal of Animal Science 67:827-834.; Bird et al., 1993Bird, A. R.; Croom, W. J.; Bailey, J. V.; O’Sullivan, B. M.; Hagler, W. M.; Gordon, G. L. and Martin, P. R. 1993. Tropical pasture hay utilization with slaframine and cottonseed meal: ruminal characteristics and digesta passage in wethers. Journal of Animal Science 71:1634-1640.) support the concept that an increased fluid throughput through the rumen, in other words, an increase in the relative passage of fluid (as compared with particles) or an enhanced “digesta washing”, increases the microbial yield from the rumen system (Figure 1). This is probably due to an increased microbial flow to the lower digestive tract. Additionally, the metabolic state of the ruminal microflora is most likely tuned to faster growth rates probably fuelled by a higher digestive capacity of the microbes, with the majority of microbial cells in the growth and reproductive stages (Isaacson et al., 1975Isaacson, H. R.; Hinds, F. C.; Bryant, M. P. and Owens, F. N. 1975. Efficiency of energy utilization by mixed rumen bacteria in continuous culture. Journal of Dairy Science 58:1645-1659.; Hummel et al., 2015Hummel, J.; Hammer, S.; Hammer, C.; Ruf, J.; Lechenne, M. and Clauss, M. 2015. Solute and particle retention in a small grazing antelope, the blackbuck (Antilope cervicapra). Comparative Biochemistry and Physiology A 182:22-26.). Such a shift in microbial metabolism (Shi et al., 2014Shi, W.; Moon, C. D.; Leahy, S. C.; Kang, D.; Froula, J.; Kittelmann, S.; Fan, C.; Deutsch, S.; Gagic, D.; Seedorf, H.; Kelly, W. J.; Atua, R.; Sang, C.; Soni, P.; Li, D.; Pinares-Patiño, C. S.; McEwan, J. C.; Janssen, P. H.; Chen, F.; Visel, A.; Wang, Z.; Attwood, G. T. and Rubin, E. M. 2014. Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome. Genome Research 24:1517-1525.) might also lead to a decrease in methane yield (Isaacson et al., 1975Isaacson, H. R.; Hinds, F. C.; Bryant, M. P. and Owens, F. N. 1975. Efficiency of energy utilization by mixed rumen bacteria in continuous culture. Journal of Dairy Science 58:1645-1659.; Van Nevel and Demeyer, 1979Van Nevel, C. J. and Demeyer, D. I. 1979. Stoichiometry of carbohydrate fermentation and microbial growth efficiency in a continous culture of mixed rumen bacteria. European Journal of Applied Microbiology and Biotechnology 7:111-120.). This shift might occur because of an effect similar to the “partitioning factor” of feeds, that is, the degree by which they trigger energy transfer into microbial growth or into short-chain fatty acid and hence also CH₄ production (Blümmel et al., 1997Blümmel, M.; Steingass, H. and Becker, K. 1997. The relationship between in vitro gas production, in vitro microbial biomass yield and N incorporation and its implications for the prediction of voluntary feed intake of roughages. British Journal of Nutrition 77:911-921.; Moss and Newbold, 2000Moss, A. R. and Newbold, C. J. 2000. The impact of hexose partitioning on methane production in vitro. Reproduction Nutrition Development 40:211-212.). A higher fluid throughput due to a higher saliva production should also be protective against acidosis. Carefully designed experiments are warranted to test the effect of differentially increasing rumen fluid throughput, by infusion of artificial saliva via fistula (Rogers et al., 1979Rogers, J. A.; Marks, B. C.; Davis, C. L. and Clark, J. H. 1979. Alteration of rumen fermentation in steers by increasing rumen fluid dilution rate with mineral salts. Journal of Dairy Science 62:1599-1605.), or by pharmacologically enhancing saliva production (Wiedmeier et al., 1987aWiedmeier, R. D.; Arambel, M. J.; Lamb, R. C. and Marcinkowski, D. P. 1987a. Effect of mineral salts, carbachol, and pilocarpine on nutrient digestibility and ruminal characteristics in cattle. Journal of Dairy Science 70:592-600.; Wiedmeier et al., 1987bWiedmeier, R. D.; Arambel, M. J. and Walters, J. L. 1987b. Effect of orally administered pilocarpine on ruminal characteristics and nutrient digestibility in cattle. Journal of Dairy Science 70:284-289.; Froetschel et al., 1989Froetschel, M. A.; Amos, H. E.; Evans, J. J.; Croom, W. J. and Hagler, W. M. 1989. Effects of a salivary stimulant, slaframine, on ruminal fermentation, bacterial protein synthesis and digestion in frequently fed steers. Journal of Animal Science 67:827-834.; Bird et al., 1993Bird, A. R.; Croom, W. J.; Bailey, J. V.; O’Sullivan, B. M.; Hagler, W. M.; Gordon, G. L. and Martin, P. R. 1993. Tropical pasture hay utilization with slaframine and cottonseed meal: ruminal characteristics and digesta passage in wethers. Journal of Animal Science 71:1634-1640.), not only on measures of digestive efficiency, pH, and microbial and methane yield, but also on the metabolic state (Shi et al., 2014Shi, W.; Moon, C. D.; Leahy, S. C.; Kang, D.; Froula, J.; Kittelmann, S.; Fan, C.; Deutsch, S.; Gagic, D.; Seedorf, H.; Kelly, W. J.; Atua, R.; Sang, C.; Soni, P.; Li, D.; Pinares-Patiño, C. S.; McEwan, J. C.; Janssen, P. H.; Chen, F.; Visel, A.; Wang, Z.; Attwood, G. T. and Rubin, E. M. 2014. Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome. Genome Research 24:1517-1525.) of the microbiome itself.

Selective breeding for digesta washing?

It has been suggested that domestic ruminants could be selected for increased digestive efficiency, based on phenotypic characteristics of the way digesta moves through their digestive tract (Hegarty, 2004Hegarty, R. S. 2004. Genotype differences and their impact on digestive tract function of ruminants: a review. Australian Journal of Experimental Agriculture 44:459-467.). Ruminants can actually be bred to differ in the mean retention time of digesta (Thompson et al., 1989Thompson, B. C.; Dellow, D. W. and Barry, T. N. 1989. The effect of selection for fleece weight upon urea metabolism and digestive function in Romney sheep. Australian Journal of Agricultural Research 40:1065-1074.; Smuts et al., 1995Smuts, M.; Meissner, H. H. and Cronje, P. B. 1995. Retention time of digesta in the rumen: its repeatability and relationship with wool production of Merino rams. Journal of Animal Science 73:206-210.; Goopy et al., 2014Goopy, J. P.; Donaldson, A.; Hegarty, R.; Vercoe, P. E.; Haynes, F.; Barnett, M. and Oddy, V. H. 2014. Low-methane yield sheep have smaller rumens and shorter rumen retention time. British Journal of Nutrition 111:578-585.). Variation in ruminal digesta retention time is currently considered the most likely explanation for the inherited differences in methane emissions (Pinares-Patiño et al., 2013Pinares-Patiño, C. S.; Hickey, S. M.; Young, E. A.; Dodds, K. G.; MacLean, S.; Molano, G.; Sandoval, E.; Kjestrup, H.; Harland, R.; Hunt, C.; Pickering, N. K. and McEwan, J. C. 2013. Heritability estimates of methane emissions from sheep. Animal 7:316-321.). Frothy bloat in cattle is associated with decreased saliva production (Gurnsey et al., 1980Gurnsey, M. P.; Jones, W. T. and Reid, C. S. W. 1980. A method for investigating salivation in cattle using pilocarpine as a sialagogue. New Zealand Journal of Agricultural Research 23:33-41.) and decreased ruminal fluid passage rates (Okine et al., 1989Okine, E. K.; Mathison, G. W. and Hardin, R. T. 1989. Relations between passage rates of rumen fluid and particulate matter and foam production in rumen contents of cattle fed on different diets ad lib. British Journal of Nutrition 61:387-395.). A report of a successful breeding program to reduce bloat susceptibility (Morris et al., 1997Morris, C. A.; Cullen, N. G. and Geertsema, H. G. 1997. Genetic studies of bloat susceptibility in cattle. Proceedings of the New Zealand Society of Animal Production 57:19-21.) therefore suggests that increased saliva flows can be achieved. Given the evidence from wild ruminants that not only retention time in general, but the difference between fluid and particle retention in the rumen is a species-specific and hence genetic/heritable characteristic, selective breeding for this measure would theoretically be feasible, if appropriate proxies could be found to evaluate phenotypes.

Conclusions

The diversity of ruminant species can be considered a catalogue of genetically fixed, morphophysiological characteristics that could, in theory, be exploited in domestic species by selective breeding. Some characteristics of that catalogue have most likely been selected indirectly during the process of breeding for phenotypes of high production value. For example, although reticulorumen volume is not a direct selection criterion, a particularly voluminous reticulorumen most likely results as an effect of breeding for phenotypes with a high intake capacity for a high milk yield. Other characteristics, such as those related to dental anatomy and durability, could be interesting in respect to intentions to prolong domestic ruminant lifespan. We propose that the characteristic of pronounced digesta washing and the associated microbial harvest and change of the microbial metabolism could represent a target for selective breeding that could further improve the efficiency of domestic ruminants.

Acknowledgments

MC thanks Izabelle Auxiliadora Molina de Almeida Teixeira for the invitation to contribute to the 1st International Meeting of Advances in Animal Science in Jaboticabal, São Paulo, Brazil, in June 2016.

References

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