Marcus Clauss

Biology of the sauropod dinosaurs: the evolution of gigantism

The herbivorous sauropod dinosaurs of the Jurassic and Cretaceous periods were the largest terrestrial animals ever, surpassing the largest herbivorous mammals by an order of magnitude in body mass. Several evolutionary lineages among Sauropoda produced giants with body masses in excess of 50 metric tonnes by conservative estimates. With body mass increase driven by the selective advantages of large body size, animal lineages will increase in body size until they reach the limit determined by the interplay of bauplan, biology, and resource availability. There is no evidence, however, that resource availability and global physicochemical parameters were different enough in the Mesozoic to have led to sauropod gigantism.

The maximum attainable body size of herbivorous mammals: morphophysiological constraints on foregut, and adaptations of hindgut fermenters

An oft-cited nutritional advantage of large body size is that larger animals have lower relative energy requirements and that, due to their increased gastrointestinal tract (GIT) capacity, they achieve longer ingesta passage rates, which allows them to use forage of lower quality. However, the fermentation of plant material cannot be optimized endlessly; there is a time when plant fibre is totally fermented, and another when energy losses due to methanogenic bacteria become punitive. Therefore, very large herbivores would need to evolve adaptations for a comparative acceleration of ingesta passage. To our knowledge, this phenomenon has not been emphasized in the literature to date. We propose that, among the extant herbivores, elephants, with their comparatively fast passage rate and low digestibility coefficients, are indicators of a trend that allowed even larger hindgut fermenting mammals to exist. The limited existing anatomical data on large hindgut fermenters suggests that both a relative shortening of the GIT, an increase in GIT diameter, and a reduced caecum might contribute to relatively faster ingesta passage; however, more anatomical data is needed to verify these hypotheses. The digestive physiology of large foregut fermenters presents a unique problem: ruminant—and nonruminant—forestomachs were designed to delay ingesta passage, and they limit food intake as a side effect. Therefore, with increasing body size and increasing absolute energy requirements, their relative capacity has to increase in order to compensate for this intake limitation. It seems that the foregut fermenting ungulates did not evolve species in which the intake-limiting effect of the foregut could be reduced, e.g. by special bypass structures, and hence this digestive model imposed an intrinsic body size limit. This limit will be lower the more the natural diet enhances the ingesta retention and hence the intake-limiting effect. Therefore, due to the mechanical characteristics of grass, grazing ruminants cannot become as big as the largest browsing ruminant. Ruminants are not absent from the very large body size classes because their digestive physiology offers no particular advantage, but because their digestive physiology itself intrinsically imposes a body size limit. We suggest that the decreasing ability for colonic water absorption in large grazing ruminants and the largest extant foregut fermenter, the hippopotamus, are an indication of this limit, and are the outcome of the competition of organs for the available space within the abdominal cavity. Our hypotheses are supported by the fossil record on extinct ruminant/tylopod species which did not, with the possible exception of the Sivatheriinae, surpass extant species in maximum body size. In contrast to foregut fermentation, the GIT design of hindgut fermenters allows adaptations for relative passage acceleration, which explains why very large extinct mammalian herbivores are thought to have been hindgut fermenters.

The Morphophysiological Adaptations of Browsing and Grazing Mammals

There has been a continous debate whether there are fundametal morphophysiological differences in the ingestive apparatus (head, teeth) and the digestive tract between browsing and grazing herbivores. A particular characteristic of this debate appears to be that while there is a wealth of publications on such potential differences, the supposed undelying differences between browse and grass have rarely been analysed quantitatively. In this chapter, we first review the actual state of knowledge on those properties of browse and grass that appear relevant for the ingestive and digestive process, and then deduct hypotheses as to how one would assume that browsers and grazers differ due to these characteristics. We address the methodological issues involved in actually testing these hypotheses, with emphasis on the influence of body mass and phylogenetic descent. Finally, we present a literature compilation of statistical tests of differences between the feeding-types. Although in general, the published tests support many hypothesized differences, there is still both a lack of comparative data, and a lack of analyses with phylogenetic control, on different taxonomic levels. However, the published material appears to indicate that convergent evolutionary adaptations of browsing and grazing herbivores to their diet represent a rewarding area of research.

Assessing the Jarman–Bell Principle: scaling of intake, digestibility, retention time and gut fill with body mass in mammalian herbivores

Differences in allometric scaling of physiological characters have the appeal to explain species diversification and niche differentiation along a body mass (BM) gradient - because they lead to different combinations of physiological properties, and thus may facilitate different adaptive strategies. An important argument in physiological ecology is built on the allometries of gut fill (assumed to scale to BM(1.0)) and energy requirements/intake (assumed to scale to BM(0.75)) in mammalian herbivores. From the difference in exponents, it has been postulated that the mean retention time (MRT) of digesta should scale to BM(1.0-0.75)=BM(0.25). This has been used to argue that larger animals have an advantage in digestive efficiency and hence can tolerate lower-quality diets. However, empirical data does not support the BM(0.25) scaling of MRT, and the deduction of MRT scaling implies, according to physical principles, no scaling of digestibility; basing assumptions on digestive efficiency on the thus-derived MRT scaling amounts to circular reasoning. An alternative explanation considers a higher scaling exponent for food intake than for metabolism, allowing larger animals to eat more of a lower quality food without having to increase digestive efficiency; to date, this concept has only been explored in ruminants. Here, using data for 77 species in which intake, digestibility and MRT were measured (allowing the calculation of the dry matter gut contents (DMC)), we show that the unexpected shallow scaling of MRT is common in herbivores and may result from deviations of other scaling exponents from expectations. Notably, DMC have a lower scaling exponent than 1.0, and the 95% confidence intervals of the scaling exponents for intake and DMC generally overlap. Differences in the scaling of wet gut contents and dry matter gut contents confirm a previous finding that the dry matter concentration of gut contents decreases with body mass, possibly compensating for the less favorable volume-surface ratio in the guts of larger organisms. These findings suggest that traditional explanations for herbivore niche differentiation along a BM gradient should not be based on allometries of digestive physiology. In contrast, they support the recent interpretation that larger species can tolerate lower-quality diets because their intake has a higher allometric scaling than their basal metabolism, allowing them to eat relatively more of a lower quality food without having to increase digestive efficiency.

Dietary Abrasiveness Is Associated with Variability of Microwear and Dental Surface Texture in Rabbits

Dental microwear and 3D surface texture analyses are useful in reconstructing herbivore diets, with scratches usually interpreted as indicators of grass dominated diets and pits as indicators of browse. We conducted feeding experiments with four groups of rabbits (Oryctolagus cuniculus) each fed a different uniform, pelleted diet (lucerne, lucerne & oats, grass & oats, grass). The lowest silica content was measured in the lucerne and the highest in the grass diet. After 25 weeks of exposure to the diets, dental castings were made of the rabbits lower molars. Occlusal surfaces were then investigated using dental microwear and 3D areal surface texture analysis. In terms of traditional microwear, we found our hypothesis supported, as the grass group showed a high proportion of (long) “scratches” and the lucerne group a high proportion of “pits”. Regardless of the uniform diets, variability of microwear and surface textures was higher when silica content was low. A high variability in microwear and texture analysis thus need not represent dietary diversity, but can also be related to a uniform, low-abrasion diet. The uniformity or variability of microwear/texture analysis results thus might represent varying degrees of abrasion and attrition rather than a variety of diet items per se.

Faecal particle size distribution in captive wild ruminants: an approach to the browser/grazer dichotomy from the other end

We investigated the particle size distribution in 245 faecal samples of 81 species of captive ruminants by a wet-sieving procedure. As a comparative measure, the modulus of fineness (MOF; Poppi et al. 1980) was used. Species were classified as frugivores (n=5), browsers (BR, n=16), intermediate feeders (IM, n=35) and grazers (GR, n=25). BR generally had a higher proportion of large particles, i.e. higher MOF values, than IM or GR of comparable size. These findings are in accord with reported lower fibre digestibility and less selective particle retention in BR, and are indicative of a difference in reticulo-ruminal physiology between the main ruminant feeding types. Possible consequences of the escape of larger particles from a browsers reticulo-rumen for the feeding of captive BR are briefly discussed.

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.

Paleontology. Sauropod gigantism.

S auropod dinosaurs were the largest animals ever to inhabit the land (see the figure). At estimated maximum body masses of 50 to 80 metric tons, they surpassed the largest terrestrial mammals and nonsauropod dinosaurs by an order of magnitude. With body lengths of more than 40 m and heights of more than 17 m, their linear dimensions also remain unique in the animal kingdom. From their beginnings in the Late Triassic (about 210 million years ago), sauropods diversified into about 120 known genera. They dominated ecosystems for more than 100 million years from the Middle Jurassic to the end of the Cretaceous, setting a record that mammalian herbivores will only match if they can double their current geological survival time. Thus, sauropods were not only gigantic but also, in evolutionary terms, very successful. Recent advances bring us closer to understanding the enigma of their gigantism (1–3). Extrinsic causes have repeatedly been advanced to explain the success of sauropod dinosaurs and the gigantism seen in the dinosaur era. However, physical and chemical conditions in the Mesozoic (250 to 65 million years ago) were probably less favorable for plant and animal life than they are today; for example, atmospheric O 2 concentrations were much lower (4). The variation of other factors (such as land mass size, ambient temperature, and atmospheric CO 2 concentrations) through time is not tracked by variations in sauropod body size (2,5). Thus, the clue to sauropod gigantism must lie in their unusual biology (see the figure). Sauropods had an elephantine body supported by four columnar legs and ending in a long tail. From the body arose a long neck bearing a small skull. Sauropods exhibit diverse oral, dental, and neck designs, indicating dietary niche differentiation; this variety makes reliance on any particular food source (6) as the reason for gigantism unlikely. However, one evolutionarily primitive character truly sets sauropods apart: In contrast to mammals and advanced bird-hipped dinosaurs (duck-billed and horned dinosaurs), they did not masticate their food; nor did they grind it in a gastric mill, as did some other herbivorous dinosaurs (7). Because gut capacity increases with body mass (8), the enormous gut capacity of sauropods would have guaranteed the long digestion times (6) necessary for degrading unchewed plant parts, even at a relatively high food intake. The lack of a masticatory apparatus allowed sauropod heads to remain small and was one prerequisite for their long neck to How did sauropod dinosaurs reach body sizes that remain unsurpassed in land-living animals? Sauropod Gigantism

Evidence for a tradeoff between retention time and chewing efficiency in large mammalian herbivores.

Large body size is thought to produce a digestive advantage through different scaling effects of gut capacity and food intake, with supposedly longer digesta retention times in larger animals. However, empirical tests of this framework have remained equivocal, which we hypothesize is because previous comparative studies have not included digesta particle size. Larger particles require more time for digestion, and if digesta particle size increases with body mass, it could explain the lack of digestive advantage in larger herbivores. We combine data on body mass, food intake, digesta retention and digestibility with data on faecal particle size (as a proxy for digesta particle size) in 21 mammalian herbivore species. Multiple regression shows that fibre digestibility is independent of body mass but dependent on digesta retention and particle size; the resulting equation indicates that retention time and particle size can compensate for each other. Similarly, digestible food intake is independent of body mass, but dependent on food intake, digesta retention, and particle size. For mammalian herbivores, increasing digesta retention and decreasing digesta particle size are viable strategies to enhance digestive performance and energy intake. Because the strategy of increased digesta retention is usually linked to reduced food intake, the high selective pressure to evolve a more efficient dentition or a physiological particle separation mechanism that facilitates repeated mastication of digesta (rumination) becomes understandable.

In vitro digestibility of fern and gymnosperm foliage: implications for sauropod feeding ecology and diet selection

Sauropod dinosaurs, the dominant herbivores throughout the Jurassic, challenge general rules of large vertebrate herbivory. With body weights surpassing those of any other megaherbivore, they relied almost exclusively on pre-angiosperm plants such as gymnosperms, ferns and fern allies as food sources, plant groups that are generally believed to be of very low nutritional quality. However, the nutritive value of these taxa is virtually unknown, despite their importance in the reconstruction of the ecology of Mesozoic herbivores. Using a feed evaluation test for extant herbivores, we show that the energy content of horsetails and of certain conifers and ferns is at a level comparable to extant browse. Based on our experimental results, plants such as Equisetum, Araucaria, Ginkgo and Angiopteris would have formed a major part of sauropod diets, while cycads, tree ferns and podocarp conifers would have been poor sources of energy. Energy-rich but slow-fermenting Araucaria, which was globally distributed in the Jurassic, was probably targeted by giant, high-browsing sauropods with their presumably very long ingesta retention times. Our data make possible a more realistic calculation of the daily food intake of an individual sauropod and improve our understanding of how large herbivorous dinosaurs could have flourished in pre-angiosperm ecosystems.