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

Abstract

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.

Figure 1. The link between body size and availability of prey in sufficient amounts/packages in terrestrial vertebrates.

Modified from Hiiemae . Note that large body size is linked to prey (package) abundance and accessibility, not necessarily to low diet quality per se.

Figure 2. Relationship between herbivore body mass (BM) and characteristics of the natural diet that are indicators of diet quality from comparative studies in African mammals.

a) BM and nitrogen concentration in (fore)stomach contents or the measured diet ; note that large herbivores (giraffe, rhinos, hippo, elephant) oppose the trend in the smaller species; b) BM (estimated from other sources) and the crude fibre concentration in rumen contents (data on ruminants only) ; c) BM and the proportion of non-stem material in the rumen , , , –; note that browsing ruminants of very small (dikdik), small (duiker, steenbok), intermediate (bongo) and large size (giraffe) show less systematic variation with BM, but their selective inclusion/exclusion will influence the data set; note also that the African buffalo (and also the hippo) do not follow the clear negative trend seen in smaller grazers.

Figure 3. Relationship between herbivore body mass (BM) and characteristics of the natural diet that are indicators of diet quality/degradability from comparative studies in African mammals.

a) BM and the preference for newly burned savanna patches from Sensenig et al. (note that the study did not include rhinos or hippos); b) BM and in vitro fermentation rates (a proxy of microbial digestion) in rumen, forestomach (hippo) or caecum (elephant) contents ; c) BM and the concentration of short-chain fatty acids (SCFA, which represent products of microbial digestion) , ; d) BM and the ratio of the SCFA propionate (C3) to acetate (C2) (a proxy of the proportion of easily fermentable carbohydrates in the diet) , ; e) BM and nitrogen content of faeces (a proxy for diet digestibility; – organic matter OM basis, - OM basis, – dry matter DM basis); f) BM and the neutral detergent fibre (NDF) content of faeces , .

Figure 4. Schematic explanation of circular reasoning in the traditional approach of explaining a positive effect of body mass on digestibility.

a) The difference in the scaling of gut capacity (measured as wet or dry gut contents; BM^1.0) and daily dry matter intake (BM^0.75), or actual dry matter gut fill rate, results in more gut available per unit digesta at higher BM, and should hence lead to increased mean retention times at higher BM (BM^0.25). If these increased retention times are used to postulate a higher digestibility at higher BM, the situation in b) occurs: The increasing digestibility reduces the actual gut fill rate, hence increases the difference in the scaling of gut capacity and gut fill rate even more, which should translate into even longer retention times.

Figure 5. Relationships of body mass (BM) and aspects of the digestive physiology of herbivorous vertebrates.

a) BM and faecal particle size in mammal, reptile and avian herbivores –; b) BM and methane production in ruminant and nonruminant mammal herbivores and tortoises (herbivorous reptiles) –; c) BM and particle mean retention time in herbivorous mammals, reptiles and birds , , (note little increase above BM of 1 kg); d) BM and particle mean retention time in three independent datasets on large herbivorous mammals , , (note the absence of relevant scaling); e) BM and organic matter digestibility in mammalian hindgut fermenters (note that there is no clear scaling pattern); f) BM and NDF digestibility on two different forages and in vitro faecal NDF gas production (an inverse proxy for fibre digestibility) in mammal hindgut fermenters and g) ruminants (note that there are no clear scaling patterns).

Figure 6. Relationships between body mass (BM) and aspects of the digestive physiology of herbivorous vertebrates.

a) wet gut contents , ; note the similarity in all three vertebrae clades, with a duck species (a flying bird) as a notable outlier; b) dry matter gut contents as calculated from simultaneous passage and digestion studies , , ; note the similarity in the scaling of both measures of gut fill in all three vertebrate clades, with herbivorous birds falling into two categories (flying birds with lower gut fills; flightless or flight-reduced birds such as hoatzin and ostrich with gut fill as in mammals); c) dry matter intake in feeding studies in captivity , , ; note the generally lower intake in reptiles as compared to mammals and birds; a curvature in mammals is evident with a lower scaling in smaller and a steeper scaling in larger species; d) dry matter intake (DMI, on a variety of diets) or organic matter intake (OMI, on a consistent diet) in mammal herbivores >100 kg (no smaller species included in the Foose dataset); note a tendency for a lower scaling in the Foose dataset (see text) that is not significant, raising the question whether the steeper intake scaling in larger herbivores in the Müller et al. dataset is a reaction to a putative decreasing diet quality with increasing BM.

Figure 7. Relationships between aspects of the digestive physiology of herbivorous vertebrates.

a) the relative food intake (per unit metabolic body weight) and the passage of digesta through the gastrointestinal trat (measured as mean retention time MRT or, in the case of some reptiles, as transit time TT) , ; note that species/individuals with a higher food intake have shorter retention times; note that flying birds show a similar relationship on a lower level, potentially due to their smaller gut capacity (cf. Fig. 6b); b) body mass and foraging time for hindgut fermenters and ruminants (regression given for hindgut fermenters; extrapolation to 100% of the day yields an upper BM limit of app. 18 tons).