Digestive physiology of the plains viscacha ( Lagostomus maximus ): A large herbivorous hystricomorph rodentby Katharina B. Hagen, Dorothea Besselmann, Ulrike Cyrus-Eulenberger, Catharina Vendl, Sylvia Ortmann, Robert Zingg, Ellen Kienzle, Michael Kreuzer, Jean-Michel Hatt, Marcus Clauss

Zoo Biology

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Year
2015
DOI
10.1002/zoo.21216
Subject
Animal Science and Zoology

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RESEARCH ARTICLE

Digestive Physiology of the Plains Viscacha (Lagostomus maximus): A Large Herbivorous

Hystricomorph Rodent

Katharina B. Hagen,1 Dorothea Besselmann,1 Ulrike Cyrus-Eulenberger,1 Catharina Vendl,1

Sylvia Ortmann,2 Robert Zingg,3 Ellen Kienzle,4 Michael Kreuzer,5 Jean-Michel Hatt,1 and Marcus Clauss1* 1Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland 2Leibniz Institute for Zoo and Wildlife Research (IZW), Berlin, Germany 3Zoo Zurich, Zurich, Switzerland 4Chair of Animal Nutrition and Dietetics, Ludwig-Maximilians-University of Munich, Munich, Germany 5Institute of Agricultural Sciences, ETH Zurich, Zurich, Switzerland

Plains viscachas (Lagostomus maximus) are large South American, fossorial rodents susceptible to diabetic cataracts.

Various aspects of their digestive physiology were studied in three different experiments with nine male and seven female adult animals and six different diets (total n of feeding trials¼ 35). Viscachas achieved mean retention times of 23–31 hr, which is of a magnitude also recorded in horses; these did not differ for solute or small particle (<2mm) markers. Secondary marker excretion peaks indicated coprophagy, and were rarer on high-protein as compared to grass hay-only diets. Mean resting metabolic rate was, at 229 kJ/kg0.75/day, lower than expected for a mammal of this size.

Digestible energy requirement for maintenance was 445 kJ/kg0.75/day. At 1.6–2.7 L/day, viscachas produced more methane than expected for a hindgut fermenter of their size. On diets that included concentrate feeds, viscachas excreted glucose in their urine, corroborating reports on the susceptibility of this species for diabetes when kept on energy-dense food. Viscachas had a similar apparent digestibility of protein, lipids, and macrominerals as other rodents, rabbits, or domestic horses. This suggests that whether or not a species practices coprophagy does not have a major influence on these measures. Viscachas resemble other hindgut fermenters in their high apparent calcium digestibility. With respect to a digestibility-reducing effect of dietary fiber, viscachas differed from rabbits and guinea pigs but were similar to horses, suggesting that small body size needs not necessarily be linked to lower digestive efficiency on high-fiber diets. Zoo Biol. XX:1–15, 2015. © 2015 Wiley Periodicals, Inc.

Keywords: herbivory; nutrition; colonic separation mechanism; coprophagy; obesity

INTRODUCTION

In the debate on the influence of body size on digestive physiology, niche differentiation, and species diversification, the traditional focus has been on large ungulate herbivores with well-documented differences in diet type and diet quality [Clauss et al., 2013]. Efficient herbivory has long been considered a privilege of large-bodied mammals [Demment and Van Soest, 1985; Foley and Cork, 1992], and herbivorous small mammals such as rodents appear less intensively studied [Smith, 1995]. However, many rodent species are true herbivores [Wilman et al., 2014] and have developed a variety of corresponding morphological and physiological adaptations [Gorgas, 1966; Cork et al., 1999;

Sakaguchi, 2003] that need to be understood for a full assessment of strategies facilitating herbivory. These adaptive mechanisms comprise selective feeding [Justice

Grant sponsor: National Science Foundation; grant number: 310030_135252/1.

Conflicts of interest: None. Correspondence to:MarcusClauss,Clinic forZooAnimals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Winterthurerstr. 260, 8057 Zurich, Switzerland. E-mail: mclauss@vetclinics.uzh.ch

Received 16 February 2015; Revised 07April 2015; Accepted 08April 2015

DOI: 10.1002/zoo.21216

Published online XX Month Year in Wiley Online Library (wileyonlinelibrary.com). © 2015 Wiley Periodicals, Inc.

Zoo Biology 9999 : 1–15 (2015) and Smith, 1992]; a strategy of compensatory high food intake as diet quality declines [Meyer et al., 2010]; large relative gut capacities similar to those of larger mammals; digesta retention times that are similar to, or lower than, those of larger mammals [M€uller et al., 2013]; different strategies with respect to the movement of fluids and particles in the colonic separation mechanism that facilitates the strategy of coprophagy [Hume and Sakaguchi, 1991; Franz et al., 2011a]; microbial fiber fermentation [Stevens and Hume, 1998]; a strategy to absorb more calcium than required from the intestinal tract and excrete the surplus via urine [Hagen et al., 2015]; and a relative methane production similar to other nonruminant mammals [Franz et al., 2011b].

Plains viscachas (Lagostomus maximus) are hystricomorph South American rodents that occur in a variety of arid, semiarid or humid habitats; they are colonial and live in a communal burrow system [Jackson et al., 1996]. Plains viscachas have a colonic furrow typical for hystricomorph rodents [Gorgas, 1966], practice coprophagy [Jackson et al., 1996; Clauss et al., 2007] and are able to concentrate urine similar to desert rodents [Kohl, 1980]. They are herbivorous [Campos et al., 2001], with an apparent preference for grasses [Giulietti and Jackson, 1986; Branch et al., 1994; Puig et al., 1998; Bontti et al., 1999; Pereira et al., 2003], and have been reported to have a low metabolic rate [Kohl, 1980]. Nevertheless, their diet in captivity has traditionally contained varied amounts of energy dense feeds, which may trigger diet-induced diabetes mellitus with cataract formation, similar to degus (Octodon degus) [R€ubel et al., 1989; Gull et al., 2009;

Wenker et al., 2009].

In the course of investigating the nutritional requirements of this species, the various experiments reported in the present study were performed. The overall aim was to facilitate a comparison of the plains viscacha with other herbivores, to assess convergence or homology in digestive function. In particular, we aimed to test, in a comparison with domestic horses, whether differences in the digestive efficiency can be demonstrated that are either putatively related to (i) body mass (the influence of dietary fiber on digestive efficiency) or (ii) to digestive strategy (assuming higher apparent digestive efficiency for protein and lipids in a coprophageous vs. a noncoprophagoues herbivore).