Jürgen Hummel

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 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.

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.

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.

The intraruminal papillation gradient in wild ruminants of different feeding types: implications for rumen physiology

Browsing and grazing ruminants are thought to differ in the degree their rumen contents are stratified—which may be due to different characteristics of their respective forages, to particular adaptations of the animals, or both. However, this stratification is difficult to measure in live animals. The papillation of the rumen has been suggested as an anatomical proxy for stratification—with even papillation indicating homogenous contents, and uneven papillation (with few and small dorsal and ventral papillae, and prominent papillae in the atrium ruminis) stratified contents. Using the surface enlargement factor (SEF, indicating how basal mucosa surface is increased by papillae) of over 55 ruminant species, we demonstrate that differences between the SEFdorsal or SEFventral and the SEFatrium are significantly related to the percentage of grass in the natural diet. The more a species is adapted to grass, the more distinct this difference, with extreme grazers having unpapillated dorsal and ventral mucosa. The relative SEFdorsal as anatomical proxy for stratification, and the difference in particle and fluid retention in the rumen as physiological proxy for stratification, are highly correlated in species (n = 9) for which both kind of data are available. The results support the concept that the stratification of rumen contents varies among ruminants, with more homogenous contents in the more browsing and more stratified contents in the more grazing species. J. Morphol., 2009.

Another one bites the dust: faecal silica levels in large herbivores correlate with high-crowned teeth

The circumstances of the evolution of hypsodonty (= high-crowned teeth) are a bone of contention. Hypsodonty is usually linked to diet abrasiveness, either from siliceous phytoliths (monocotyledons) or from grit (dusty environments). However, any empirical quantitative approach testing the relation of ingested silica and hypsodonty is lacking. In this study, faecal silica content was quantified as acid detergent insoluble ash and used as proxy for silica ingested by large African herbivores of different digestive types, feeding strategies and hypsodonty levels. Separate sample sets were used for the dry (n = 15 species) and wet (n = 13 species) season. Average faecal silica contents were 17–46 g kg−1 dry matter (DM) for browsing and 52–163 g kg−1 DM for grazing herbivores. No difference was detected between the wet (97.5 ± 14.4 g kg−1 DM) and dry season (93.5 ± 13.7 g kg−1 DM) faecal silica. In a phylogenetically controlled analysis, a strong positive correlation (dry season r = 0.80, p < 0.0005; wet season r = 0.74, p < 0.005) was found between hypsodonty index and faecal silica levels. While surprisingly our results do not indicate major seasonal changes in silica ingested, the correlation of faecal silica and hypsodonty supports a scenario of a dominant role of abrasive silica in the evolution of high-crowned teeth.

Differential passage of fluids and different-sized particles in fistulated oxen (Bos primigenius f. taurus), muskoxen (Ovibos moschatus), reindeer (Rangifer tarandus) and moose (Alces alces): Rumen particle size discrimination is independent from contents stratification

Ruminant species differ in the degree that their rumen contents are stratified but are similar insofar that only very fine particles are passed from the forestomach to the lower digestive tract. We investigated the passage kinetics of fluid and particle markers (2, 10 and 20 mm) in fistulated cattle (Bos primigenius f. taurus), muskoxen (Ovibos moschatus), reindeer (Rangifer tarandus) and moose (Alces alces) on different diets. The distribution of dry matter in the rumen and the viscosity of rumen fluids suggested that the rumen contents were more stratified in muskoxen than moose. Correspondingly, as in previous studies, the species differed in the ratio of mean retention times of small particles to fluids in the reticulorumen, which was highest in cattle (2.03) and muskoxen (1.97-1.98), intermediate in reindeer (1.70) and lowest in moose (0.98-1.29). However, the ratio of large to small particle retention did not differ between the species, indicating similarity in the efficiency of the particle sorting mechanism. Passage kinetics of the two largest particle classes did not differ, indicating that particle retention is not a continuous function of particle size but rather threshold-dependent. Overall, the results suggest that fluid flow through the forestomach differs between ruminant species. A lower relative fluid passage, such as in moose, might limit species to a browse-based dietary niche, whereas a higher relative fluid passage broadens the dietary niche options and facilitates the inclusion of, or specialization on, grass. The function of fluid flow in the ruminant forestomach should be further investigated.

Physical characteristics of rumen contents in four large ruminants of different feeding type, the addax (Addax nasomaculatus), bison (Bison bison), red deer (Cervus elaphus) and moose (Alces alces).

Based on morphological and physiological observations, it has been suggested that differences exist in the degree that reticuloruminal (RR) contents are stratified between various ruminant species. However, the occurrence of stratification has hardly been measured in non-domestic species. Forestomach contents of free-ranging moose (n=22) and red deer (24) shot during regular hunting procedures, and of captive (but 100% forage fed) addax (6) and bison (10) culled for commercial or management purposes were investigated. There was no difference between the species in the degree by which RR ingesta separated according to size due to buoyancy characteristics in vitro. However, RR fluid of moose was more viscous than that of the other species, and no difference in moisture content was evident between the dorsal and the ventral rumen in moose, in contrast to the other species. Hence, the RR milieu in moose appears less favourable for gas or particle separation due to buoyancy characteristics. These findings are in accord with notable differences in RR papillation between the species. In moose, particle separation is most likely restricted to the reticulum, whereas in the other species, the whole rumen may pre-sort particles in varying degrees; a possible explanation for this pattern is a hypothetically lesser saliva production and fluid throughput in moose. The results suggest that differences in RR physiology may occur across ruminant species. The RR sorting mechanism should be considered a dynamic process that is better measured by its result--the significantly smaller particle size in the distal digestive tract when compared to the RR--than by regional differences in particle size within the RR.