Patrick Steuer

Herbivory and body size: allometries of diet quality and gastrointestinal physiology, and implications for herbivore ecology and dinosaur gigantism.

Digestive physiology has played a prominent role in explanations for terrestrial herbivore body size evolution and size-driven diversification and niche differentiation. This is based on the association of increasing body mass (BM) with diets of lower quality, and with putative mechanisms by which a higher BM could translate into a higher digestive efficiency. Such concepts, however, often do not match empirical data. Here, we review concepts and data on terrestrial herbivore BM, diet quality, digestive physiology and metabolism, and in doing so give examples for problems in using allometric analyses and extrapolations. A digestive advantage of larger BM is not corroborated by conceptual or empirical approaches. We suggest that explanatory models should shift from physiological to ecological scenarios based on the association of forage quality and biomass availability, and the association between BM and feeding selectivity. These associations mostly (but not exclusively) allow large herbivores to use low quality forage only, whereas they allow small herbivores the use of any forage they can physically manage. Examples of small herbivores able to subsist on lower quality diets are rare but exist. We speculate that this could be explained by evolutionary adaptations to the ecological opportunity of selective feeding in smaller animals, rather than by a physiologic or metabolic necessity linked to BM. For gigantic herbivores such as sauropod dinosaurs, other factors than digestive physiology appear more promising candidates to explain evolutionary drives towards extreme BM.

Is there an influence of body mass on digesta mean retention time in herbivores? A comparative study on ungulates

The relation between body mass (BM) and digesta mean retention time (MRT) in herbivores was the focus of several studies in recent years. It was assumed that MRT scaled with BM(0.25) based on the isometric scaling of gut capacity (BM(1.0)) and allometric scaling of energy intake (BM(0.75)). Literature studies that tested this hypothesis produced conflicting results, arriving sometimes at higher or lower exponents than the postulated 0.25. This study was conducted with 8 ruminants (n=2-6 per species) and 6 hindgut fermenting species/breeds (n=2-6, warthog n=1) with a BM range of 60-4000 kg. All animals received a ration of 100% grass hay with ad libitum access. Dry matter intake was measured and the MRT was estimated by the use of a solute and a particle (1-2 mm) marker. No significant scaling of MRT(particle) with BM was observed for all herbivores (32 BM(0.04), p=0.518) and hindgut fermenters (32 BM(0.00), p=1.00). The scaling exponent for ruminants only showed a tendency towards significance (29 BM(0.12), p=0.071). Ruminants on average had an MRT(particle) 1.61-fold longer than hindgut fermenters. Whereas an exponent of 0.25 is reasonable from theoretical considerations, much lower exponents were found in this and other studies. The energetic benefit of increasing MRT is by no means continuous, since the energy released from a given food unit via digestion decreases over time. The low and non-significant scaling factors for both digestion types suggest that in ungulates, MRT is less influenced by BM (maximal allometric exponent ≤0.1) than often reported.

Does body mass convey a digestive advantage for large herbivores

Summary 1. A key concept of body mass (BM) in niche separation of large herbivores assumes that the decrease in diet quality inherent to increasing BM (due to less selective feeding behaviour) is balanced by a simultaneous increase in digestive ability (due to longer retention times), resulting in no or less-than-expected reduction in digestibility (as measured in the animal as a result of diet quality and digestive ability). However, the second part of this concept has been challenged recently due to theoretical problems and mismatch with empirical data. 2. A proxy for digestibility, such as metabolic faecal nitrogen (MFN), will comprise both information on diet quality and digestive ability in free-ranging animals. In captive animals, if diet is kept constant, such a proxy can exclusively indicate digestive ability. Comparing freeranging and captive animals under such conditions, one would expect an increase in MFN with BM in captive animals and no relationship between these measures in free-ranging animals if BM was related to digestive ability. 3. We compared captive ungulates on a consistent grass hay diet (17 species; 30–4000 kg BM) to a sample of free-ranging East African ungulates (19 species; 12–4000 kg BM). MFN was used as the major proxy for digestibility. 4. In captive animals, there was no influence of BM on MFN (P =0 � 466); for free-ranging animals, a significant decreasing effect of body mass on MFN (P =0 � 002) and therefore diet quality was found at a scaling of BM � 0� 15 . 5. In conclusion, scenarios that assume a compensation of the evident decrease in diet quality with BM via an increased digestive ability are not supported by this study. This does not rule out other feeding-related factors in facilitating large BM, such as compensation by an increased diet intake.

Comparative investigations on digestion in grazing (Ceratotherium simum) and browsing (Diceros bicornis) rhinoceroses

Rhinoceroses represent the largest extant herbivores with extensive dietary specialization for plant groups like browse (black rhino Diceros bicornis) or grass (white rhino Ceratotherium simum). However, it is not clear to what extent such diet selection patterns are reflected in adaptations of digestive physiology of the respective feeding types. In this study, feeding trials with four black and five white rhinos were conducted in four zoos. The animals had ad libitum access to the same batch of grass hay (second cut; neutral detergent fiber (NDF) 63% dry matter (DM), crude protein 10.2% DM). Total intake, fecal N content, in vitro digestibility of NDF residues of feces, fecal particle size and mean retention time (MRT) of particles (Cr-mordanted fiber; 1-2mm) and fluid (Co-EDTA) were quantified. The average daily DM intake was 70+/-12 g/kg BW(0.75) for white and 73+/-10 g/kg BW(0.75) for black rhinos. In the in vitro fermentation test fecal NDF residues of black rhinos resulted in higher gas productions at fermentation times of 12 to 24h, indicating that white rhinos have a superior capacity to digest NDF. Average MRT for fluids and particles was 28+/-4h and 43+/-5h in white and 34+/-4h and 39+/-4h in black rhinos. The selectivity factor (SF=MRT(particle)/MRT(fluid)) was higher for white (1.5+/-0.2) than for black rhinos (1.2+/-0.1) (p=0.016). In a comparison of 12 ruminant and 3 rhino species, SF was correlated to percentage of grass in diet (R=0.75). Mean fecal particle size was higher in white (9.1+/-1.94 mm) than in black rhinos (6.1+/-0.79 mm) (p=0.016). The results demonstrate differences between white and black rhinos in terms of retention times and fiber digestibility. The more selective retention of particles by the white rhino corresponds with the higher digestion of fiber measured indirectly. Furthermore there is indication for a general pattern of high SF in grazing ruminants and rhinos. The difference in fecal particle size between both rhino species might be due to the considerable difference in body weight.

Digesta kinetics in gazelles in comparison to other ruminants: Evidence for taxon-specific rumen fluid throughput to adjust digesta washing to the natural diet

Digesta flow plays an important role in ruminant digestive physiology. We measured the mean retention time (MRT) of a solute and a particle marker in the gastrointestinal tract (GIT) and the reticulorumen (RR) of five gazelles and one dikdik species. Species-specific differences were independent from body mass (BM) or food intake. Comparative evaluations (including up to 31 other ruminant species) indicate that MRT GIT relate positively to BM, and are less related to feeding type (the percentage of grass in the natural diet, %grass) than MRT RR. The MRTparticleRR is related to BM and (as a trend) %grass, matching a higher RR capacity with increasing BM in grazers compared to browsers. MRTsoluteRR is neither linked to BM nor to %grass but shows a consistent phylogenetic signal. Selectivity factors (SF; MRTparticle/MRTsolute, proxies for the degree of digesta washing) are positively related to %grass, with a threshold effect, where species with >20% grass have higher SF. These findings suggest that in different ruminant taxa, morphophysiological adaptations controlling MRTsoluteRR evolved to achieve a similar SF RR in relation to a %grass threshold. A high SF could facilitate an increased microbial yield from the forestomach. Reasons for variation in SF above the %grass threshold might represent important drivers of ruminant diversification and await closer investigation.

Fibre digestibility in large herbivores as related to digestion type and body mass — An in vitro approach

The coexistence of different ungulate species in a given ecosystem has been the focus of many studies. Differences between ruminant foregut fermenters and hindgut fermenters were remarkable for example in the way they ingest and digest high fibre diets. Digestion trials based on total collections are difficult to conduct or are sometimes even not possible for wild animals in the field or in zoos. To gain information on the fibre digestion achieved by these animals and the influence of body mass (BM) thereon, a method using spot sampling is desirable. In this study, in vitro fermentation of faecal neutral detergent fibre (NDF) was used as a measure of fibre digestion in large ungulates. Food and faecal samples of 10 ruminant foregut fermenting and 7 hindgut fermenting species/breeds were collected. All animals received 100% grass hay with ad libitum access. The NDF of food and faeces was fermented in vitro in a Hohenheim gas test (HGT) for 96 h. The digestion type generally had an effect on the gas production (GP) of faecal NDF in the HGT with hindgut fermenters showing higher values than ruminant foregut fermenters. At any time interval of incubation, BM had no influence on GP. The results are in accordance with both findings that ruminant foregut fermenters have longer mean retention times and more comprehensive particle reduction and findings of a lack of influence of BM on digesta mean retention time. It can be stated that the HGT (96 h) is a useful and quick method to show also small differences within groups in fibre digestion.

An isthmus at the caecocolical junction is an anatomical feature of domestic and wild equids

The isthmus at the caecocolical junction in domestic equids is well described. Like another isthmus between the ansa proximalis coli (the colonic fermentation chamber or ‘large colon’) and the colon transversum (the distal or ‘small’ colon), this spot represents not only a potential anatomical feature contributing to particle ingesta retention but also an explicit predilection site for intestinal obstructions. The question whether this anatomical feature also occurs in wild equids is therefore of both physiological and medical interest but has not been addressed so far. In this paper, we report dissections of the large intestine of a domestic pony (Equus caballus f. dom.), a Przewalski horse (Equus przewalski) and a plains zebra (Equus burchelli). The intestinal tract section of all three animals were similar in length; each species displayed the caecocolical isthmus as well as the abrupt narrowing of the intestinal tract between the ‘large’ and the ‘small’ colon. Graphical descriptions of wild equid gastrointestinal anatomy should include these features.

Food intake rates of herbivorous mammals and birds and the influence of body mass

The bite size and bite rate of an animal determines its food intake rate. Because of the importance of ingesting food, this behaviour makes up a large part of the daily routine of mammalian and avian herbivores, since they have to ingest large amounts of fibrous forage to meet their daily energy demands. Hence, they have to solve the dilemma of conflicting interests in their daily activities between foraging, social behaviour, sleep or predator avoidance. In this study, the role that body mass (BM) plays in this context was quantified and mammals and birds were compared regarding the influence of BM on instantaneous food intake rate (IFIR) (the first minutes of a meal), bite size (BS) and bite rate (BR). Because birds do not chew their food, it was hypothesised that they can increase their IFIR above the upper limit of similar-sized mammals which chew their food. Combining our own findings with literature, results showed that there is no difference between mammals and birds regarding IFIR, BS and BR. It was shown that IFIR (mammals BM0.95, birds BM0.82) and BS (mammals BM0.83, birds BM0.87) increase with increasing BM. Moreover, the factor ‘non-chewing’ does not increase the IFIR of birds.