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University of Zurich Posted at the Zurich Open Repository and Archive, University of Zurich Clauss, M; Hofmann, R R; Streich, W J; Fickel, J; Hummel, J (2010). 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(1):26-38. Postprint available at: http://www.zora.uzh.ch University of Zurich Posted at the Zurich Open Repository and Archive, University of Zurich. Zurich Open Repository and Archive http://www.zora.uzh.ch Originally published at: Journal of Zoology 2010, 281(1):26-38. Winterthurerstr. 190 CH-8057 Zurich http://www.zora.uzh.ch Year: 2010 Convergence in the macroscopic anatomy of the reticulum in wild ruminant species of different feeding types and a new resulting hypothesis on reticular function Clauss, M; Hofmann, R R; Streich, W J; Fickel, J; Hummel, J Clauss, M; Hofmann, R R; Streich, W J; Fickel, J; Hummel, J (2010). 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(1):26-38. Postprint available at: http://www.zora.uzh.ch Posted at the Zurich Open Repository and Archive, University of Zurich. http://www.zora.uzh.ch Originally published at: Journal of Zoology 2010, 281(1):26-38. 1 1 Convergence in the macroscopic anatomy of the reticulum in wild ruminant species of 2 different feeding types and a new resulting hypothesis on reticular function 3 4 Marcus Clauss1*, Reinold R. Hofmann2, W. Jürgen Streich3, Jörns Fickel3, Jürgen Hummel4 5 6 1Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, 7 Winterthurerstr. 260, 8057 Zurich, Switzerland 8 2formerly at the Leibniz Institute for Zoo and Wildlife Research (IZW), Berlin, Germany 9 (retired); present address: Trompeterhaus, 15837 Baruth/Mark, Germany 10 3Leibniz Institute for Zoo and Wildlife Research (IZW), Alfred-Kowalke-Str. 17, 10315 11 Berlin, Germany 12 4Institute of Animal Science, Animal Nutrition Group, Endenicher Allee 15, University of 13 Bonn, 53115 Bonn, Germany 14 15 16 17 18 *correspondence to: Marcus Clauss, Clinic for Zoo Animals, Exotic Pets and Wildlife, 19 Winterthurerstr. 260, 8057 Zurich, Switzerland, phone: ++41 44 635 83 76, fax: ++41 44 635 20 89 01, email: [email protected] 21 22 Running head: Reticulum anatomy in ruminants 23 24 2 24 Summary 25 The reticulum is the second part of the ruminant forestomach, located between the rumen and 26 the omasum and characterised by a honeycomb-like internal mucosa. With its fluid contents, 27 it plays a decisive role in particle separation. Differences among species have been linked to 28 feeding style. We investigated whether reticulum size (absolute and in relation to rumen size) 29 and size of the crests that form the mucosal honeycomb pattern differ among over 60 30 ruminant species of various body sizes and feeding type, controlling for phylogeny. Linear 31 dimensions generally scaled allometrically, i.e. to body mass0.33. With or without controlling 32 for phylogeny, species that ingest a higher proportion of grass in their natural diet had both 33 significantly larger (higher) rumens and higher reticular mucosa crests, but neither reticulum 34 height nor reticulum width varied with feeding type. The height of the reticular mucosa crests 35 represents a dietary adaptation in ruminants. We suggest that the reticular honeycomb 36 structures do not separate particles by acting as traps (neither for small nor for large particles), 37 but that the structures reduce the lumen of the reticulum during contractions – at varying 38 degrees of completeness in the different feeding types. In browsing species with rumen 39 contents that may be less fluid and more viscous than those of the reticulum, incomplete 40 closure of the lumen may allow the reticulum to retain the fluid necessary for particle 41 separation. In grazing species, whose rumen contents are more stratified with a larger distinct 42 fluid pool, a more complete closure of the reticular lumen due to higher crests may be 43 beneficial as the reticulum can quickly re-fill with fluid rumen contents that contain pre- 44 sorted particles. 45 Key words: rumen, grazer, browser, rumination, forestomach, anatomy, physiology 3 46 Introduction 47 The process of rumination and the complicated forestomach of ruminants have 48 fascinated scientists for centuries (Peyer 1685, Haubner 1837). Apart from fermenting plant 49 material, which the ruminant forestomach shares with the foregut or hindgut of many other 50 herbivores (Stevens & Hume 1998), the forestomachs of ruminants and camelids have a 51 unique sorting function (Schwarm et al. 2008, Schwarm et al. 2009a) which ensures that large 52 ingesta particles are regurgitated and re-masticated (Fritz et al. 2009). This sorting mechanism 53 facilitates a high digestive efficiency (Clauss et al. 2009d) at comparatively high intakes in 54 ruminants, especially when compared to other foregut fermenters (Schwarm et al. 2009b). 55 The second section of the ruminant forestomach, the reticulum, has long been 56 recognised in domestic ruminants as the site of particle sorting (Reid 1985, Mathison et al. 57 1995, Okine et al. 1998). In wild ruminants, empirical evidence also points towards the 58 reticulum as the major site of particle sorting (Clauss et al. 2009a, Clauss et al. 2009b). The 59 bisphasic contractions of the reticulum in domestic ruminants lead to a re-jection of larger, 60 floating particles into the rumen, while the opening of the reticulo-omasal orifice allows the 61 passage of fluids and finer, denser particles; in the second contraction phase, the reticulum 62 contracts completely in cattle so that its lumen disappears, and the then empty reticulum 63 relaxes and re-fills again with contents from the ventral rumen with a high proportion of 64 fluids. An important precondition for the sorting function, apart from the precise timing of 65 contractions and opening of the reticulo-omasal orifice, is the correlation between density and 66 size of reticuloruminal contents – smaller particles are usually more dense, and are hence 67 passed on to the omasum by the reticulum (Sutherland 1988, Beaumont & Deswysen 1991, 68 Lechner-Doll, Kaske & Engelhardt 1991, Allen 1996, Hristov et al. 2003). This function of 4 69 the reticulum has been investigated in numerous studies and is, to date, undisputed (Okine, 70 Mathison & Hardin 1990, Kaske & Midasch 1997). 71 How the anatomy of the reticulum - especially the peculiar shape of its internal mucosa 72 which is arranged in net-like ridges (hence the name “reticulum”) or “honeycomb cells” (Fig. 73 1) – accomplishes its function is unclear. Historically, the reticular crests and honeycomb 74 cells have been suspected to play a role in water storage, to help grind coarse food during 75 contractions, or to be directly involved in the particle separation mechanism – either by acting 76 as traps that hold larger food particles and prevent their passage toward the omasum 77 (Hofmann & Schnorr 1982) or by acting as sedimentation traps that catch small dense 78 particles and direct them towards the omasum during contractions (Grau 1955, Reid 1985). 79 However, empirical data supporting either mechanism is lacking. 80 The height of the reticular crests and the respective depth of the honeycomb structures 81 vary greatly across species (Fig. 1 & 2). Würfel (1908) described respective differences 82 between cattle and sheep. Reticular crests are shallow in okapi (Okapia johnstoni), giraffe 83 (Giraffa camelopardalis) and deer, and higher in chamois (Rupicapra rupicapra), sheep and 84 cattle (Burne 1917, Neuville & Derscheid 1929). Grazing ruminants have in general higher 85 reticular crests than browsers, and more pronounced secondary, tertiary and even quaternary 86 crests (Hofmann 1969, Hofmann 1973, Langer 1988). Appropriate statistical treatments of 87 this observation, however, are lacking. Additionally, Hofmann (1973, 1989) suggested that 88 browsing ruminants have generally larger reticula than grazers – a suggestion that Langer 89 (1988) confirmed statistically using Hofmann’s (1973) data. The suggested functional reason 90 for this latter observation is that the whole reticulo-rumen might be involved in the particle 91 separation in grazers, in which rumen contents are prominently stratified, whereas in browsers 5 92 the sorting mechanism might be spatially limited to the reticulum only, which might therefore 93 need to be of a larger size (Clauss et al. 2009b, Clauss et al. 2009c, Hummel et al. 2009). 94 Here, we report comparative analyses of the reticulum size and the height of the 95 reticular crests from more than 60 ruminant species of different feeding types. We predicted 96 that 97 1. as linear measurements, the height and width of the reticulum, and the 98 height of the reticular crests, would scale allometrically to body mass (BM) with an 99 exponent of 0.33 (based on simple geometry, volumes should scale to BM1.00, 100 areas/surfaces should scale to BM0.67, and linear dimensions to BM0.33); 101 2. species with a higher proportion of grass in their natural diet (grazers) 102 would have a smaller reticulum, both in absolute terms and in relation to rumen size, 103 than similar-sized species with a lower proportion of grass in their natural diet 104 (browsers); 105 3. species with a higher proportion of grass in their natural diet would 106 have higher (taller) reticular crests than similar-sized species with a lower proportion 107 of grass in their natural diet. 108 In interpreting the results, we offer a potentially novel explanation of the functional 109 significance of reticular crests. 110 111 Methods 112 The core of the data originated from the second author and was supplemented with data 113 from other sources (Table 1). Additional animals were obtained over years from from hunts in 114 Germany, Austria, Switzerland, Finland, Canada, Botswana, Namibia and South Africa, and 115 from European zoological gardens; because studies that document and influence of diet on the 6 116 size of reticular crests are lacking, captive animals were also included (but marked in Table 117 1).
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