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.

Exceptional avian herbivores: multiple transitions toward herbivory in the bird order Anseriformes and its correlation with body mass

“…2013). Such a hypothesis invokes a physiological mechanism whereby differential scaling of digestive parameters, such as food intake rate, causes larger herbivores to outcompete smaller herbivores or increase the herbivorous portion of their diet.…”

“…The “abundance‐packet size” hypothesis proposes an ecological mechanism whereby increases in body mass, for reasons perhaps unrelated to dietary shifts, causes animals to shift toward diets composed of foods that are available in increasingly abundant or large packets (Hiiemae 2000; Clauss et al. 2013). In the spectrum of food abundance and packet size, it is supposed that leaves of plants and large animals lie at the extremes of abundance and packet size, respectively.…”

“…A second hypothesis proposes an ecological mechanism whereby body size is not positively associated with herbivory, per se, but rather with diets that provide sufficiently abundant and large packets of food (Hiiemae 2000; Clauss et al. 2013). This hypothesis, referred to here as the “abundance‐packet size” hypothesis, predicts that as a lineage increases in body mass, selection will act to shift the diet toward foods that are available in larger or more abundant packets, such as leaves of plants, resulting in an observed positive correlation between herbivory and body mass.…”

Ontogenetic and life history trait changes associated with convergent ecological specializations in extinct ungulate mammals

“…Pending more precise environmental data, it seems at least reasonable to assume that the acquisition of a more durable and rapidly efficient dentition allowed notoungulates to widen the spectrum of plants consumed (19,40,41) in being more tolerant toward abrasives, which partly led to their subsequent specializations. These innovations may also have allowed juvenile notoungulates to exploit more rapidly an abundant and readily available food type, which contributed to reducing the energetic cost of foraging (42). This is the case of many extant fast-growing herbivores, such as ruminants and horses (2,3), and may be assumed to be the case for notoungulates.…”

Comparative digesta retention patterns in ratites

“…A thorough microbial digestion of plant material, which necessitates a voluminous gut with long digesta retention times (Clauss et al 2013), is usually considered incompatible with anatomic adaptations of flight. Avian herbivores that rely heavily on microbial plant fiber fermentation are therefore thought to be obligatorily flightless (e.g., Morton 1978).…”