Matt Sponheimer

The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds

We tested the competing hypotheses that (1) nitrogen discrimination in mammals and birds increases with dietary nitrogen concentration or decreasing C:N ratios and, therefore, discrimination will increase with trophic level as carnivores ingest more protein than herbivores and omnivores or (2) nitrogen discrimination increases as dietary protein quality decreases and, therefore, discrimination will decrease with trophic level as carnivores ingest higher quality protein than do herbivores. Discrimination factors were summarized for five major diet groupings and 21 different species of birds and mammals. Discrimination did not differ between mammals and birds and decreased as protein quality (expressed as biological value) increased with trophic level (i.e., herbivores to carnivores). Relationships between discrimination factors and dietary nitrogen concentration or C:N ratios were either the opposite of what was hypothesized or non-significant. Dietary protein quality accounted for 72% of the variation in discrimination factors across diet groupings. We concluded that protein quality established the baseline for discrimination between dietary groupings, while other variables, such as dietary protein intake relative to animal requirements, created within-group variation. We caution about the care needed in developing studies to understand variation in discrimination and subsequently applying those discrimination factors to estimate assimilated diets of wild animals.

Three case studies used to reassess the reliability of fossil bone and enamel isotope signals for paleodietary studies

Abstract The emphasis on tooth enamel for extraction of stable light isotope signals from the mineral phase of archaeological and paleontological calcified tissues is based on the widespread understanding that enamel remains a relatively closed system, while bone does not. Twenty years ago, however, Sullivan and Krueger’s groundbreaking study demonstrating the potential of stable carbon isotopes from the mineral phase relied entirely on bone apatite samples from archaeological sites. Further effort to test whether diagenetic effects in bone mineral may be circumvented remains important because bone apatite yields dietary information about adult life-stages beyond the discrete snapshots obtainable from enamel. In this paper we re-examine the grounds for exclusion of bone apatite as sample material, using case studies drawn from three sites which differ in age and depositional conditions. We use 13C/12C, 18O/16O, 87Sr/86Sr, and Fourier transform infrared (FTIR) spectroscopy data from three sites (Reunion Rocks, Border Cave, and Makapansgat Limeworks) to show that, while enamel is not a closed system, it nevertheless retains biogenic isotopic signals. In addition, bone signals may be surprisingly well preserved where fossilisation pathways have induced ‘enamel-like’ crystallisation changes.

DIETS OF SOUTHERN AFRICAN BOVIDAE: STABLE ISOTOPE EVIDENCE

Abstract Although bovids have been studied for decades, debate still exists about their diets. To address this problem, we examined bovid dietary ecology through analysis of stable carbon isotopes. We analyzed tooth enamel, bone collagen, and hair from 312 individual bovids, representing 27 species from southern Africa. Although dietary information from the literature is usually supported by this technique, our results and the literature are sometimes highly divergent. For instance, our results indicate that Taurotragus oryx and Raphicerus campestris eat less grass than is widely believed. Furthermore, contrary to most theoretical expectations, our data indicate no relationship between body size and percentage of monocots consumed by southern African Bovidae. Although many researchers have abandoned the idea that bovid soft-tissue anatomy is strongly indicative of diet, we demonstrate a strong relationship between the percentage of grass in a bovid’s diet and several hard-tissue craniodental indices.

Diet of Paranthropus boisei in the early Pleistocene of East Africa

The East African hominin Paranthropus boisei was characterized by a suite of craniodental features that have been widely interpreted as adaptations to a diet that consisted of hard objects that required powerful peak masticatory loads. These morphological adaptations represent the culmination of an evolutionary trend that began in earlier taxa such as Australopithecus afarensis, and presumably facilitated utilization of open habitats in the Plio-Pleistocene. Here, we use stable isotopes to show that P. boisei had a diet that was dominated by C4 biomass such as grasses or sedges. Its diet included more C4 biomass than any other hominin studied to date, including its congener Paranthropus robustus from South Africa. These results, coupled with recent evidence from dental microwear, may indicate that the remarkable craniodental morphology of this taxon represents an adaptation for processing large quantities of low-quality vegetation rather than hard objects.

The Diets of Early Hominins

Diet changes are considered key events in human evolution. Most studies of early hominin diets focused on tooth size, shape, and craniomandibular morphology, as well as stone tools and butchered animal bones. However, in recent years, dental microwear and stable isotope analyses have hinted at unexpected diversity and complexity in early hominin diets. Some traditional ideas have held; others, such as an increasing reliance on hard-object feeding and a dichotomy between Australopithecus and Paranthropus, have been challenged. The first known evidence of C4 plant (tropical grasses and sedges) and hard-object (e.g., seeds and nuts) consumption dates to millions of years after the appearance of the earliest probable hominins, and there are no consistent trends in diet change among these species through time.

Isotopic evidence of early hominin diets

Carbon isotope studies of early hominins from southern Africa showed that their diets differed markedly from the diets of extant apes. Only recently, however, has a major influx of isotopic data from eastern Africa allowed for broad taxonomic, temporal, and regional comparisons among hominins. Before 4 Ma, hominins had diets that were dominated by C3 resources and were, in that sense, similar to extant chimpanzees. By about 3.5 Ma, multiple hominin taxa began incorporating 13C-enriched [C4 or crassulacean acid metabolism (CAM)] foods in their diets and had highly variable carbon isotope compositions which are atypical for African mammals. By about 2.5 Ma, Paranthropus in eastern Africa diverged toward C4/CAM specialization and occupied an isotopic niche unknown in catarrhine primates, except in the fossil relations of grass-eating geladas (Theropithecus gelada). At the same time, other taxa (e.g., Australopithecus africanus) continued to have highly mixed and varied C3/C4 diets. Overall, there is a trend toward greater consumption of 13C-enriched foods in early hominins over time, although this trend varies by region. Hominin carbon isotope ratios also increase with postcanine tooth area and mandibular cross-sectional area, which could indicate that these foods played a role in the evolution of australopith masticatory robusticity. The 13C-enriched resources that hominins ate remain unknown and must await additional integration of existing paleodietary proxy data and new research on the distribution, abundance, nutrition, and mechanical properties of C4 (and CAM) plants.

An experimental study of nitrogen flux in llamas: is 14N preferentially excreted?

Nitrogen isotope analysis is now commonly used to investigate the diets, and to a lesser extent, the environments of ancient populations. These studies assume that mammals are predictably enriched in 15 N over their food, and concomitantly, that 15 N becomes increasingly concentrated as one moves up the food chain. The literature commonly states that this 15 N-enrichment of mammalian tissues is due to preferential excretion of light nitrogen ( 14 N), but there are few data to support this assertion. To address the gap, we conducted two nitrogen flux trials in which four llamas (Lama glama) were fed high- and low-protein diets. The ratios of fecal nitrogen loss to urinary nitrogen loss were 0.30 and 0.88 on the high- and low-protein diets respectively. Feces were enriched in 15 N by approximately +3‰ on both diets, whereas urinary nitrogen was depleted in 15 N( 2.1‰) on the low-protein diet, but not significantly different from intake 15 N on the high-protein diet. Most importantly, there was no statistically significant difference between dietary and total excreta 15 N on either diet. Given these data and theoretical considerations, we argue that the nitrogen influx and efflux of adult mammals at steady state should be isotopically commensurate. However, during growth, diet change, thermal or nutritional stress, animals may not be at steady state and fractionation between intake and excreta 15 Nm ay occur.

Strontium isotope evidence for landscape use by early hominins

Ranging and residence patterns among early hominins have been indirectly inferred from morphology, stone-tool sourcing, referential models and phylogenetic models. However, the highly uncertain nature of such reconstructions limits our understanding of early hominin ecology, biology, social structure and evolution. We investigated landscape use in Australopithecus africanus and Paranthropus robustus from the Sterkfontein and Swartkrans cave sites in South Africa using strontium isotope analysis, a method that can help to identify the geological substrate on which an animal lived during tooth mineralization. Here we show that a higher proportion of small hominins than large hominins had non-local strontium isotope compositions. Given the relatively high levels of sexual dimorphism in early hominins, the smaller teeth are likely to represent female individuals, thus indicating that females were more likely than males to disperse from their natal groups. This is similar to the dispersal pattern found in chimpanzees, bonobos and many human groups, but dissimilar from that of most gorillas and other primates. The small proportion of demonstrably non-local large hominin individuals could indicate that male australopiths had relatively small home ranges, or that they preferred dolomitic landscapes.

The diet of Australopithecus sediba

Specimens of Australopithecus sediba from the site of Malapa, South Africa (dating from approximately 2 million years (Myr) ago) present a mix of primitive and derived traits that align the taxon with other Australopithecus species and with early Homo. Although much of the available cranial and postcranial material of Au. sediba has been described, its feeding ecology has not been investigated. Here we present results from the first extraction of plant phytoliths from dental calculus of an early hominin. We also consider stable carbon isotope and dental microwear texture data for Au. sediba in light of new palaeoenvironmental evidence. The two individuals examined consumed an almost exclusive C3 diet that probably included harder foods, and both dicotyledons (for example, tree leaves, fruits, wood and bark) and monocotyledons (for example, grasses and sedges). Like Ardipithecus ramidus (approximately 4.4 Myr ago) and modern savanna chimpanzees, Au. sediba consumed C3 foods in preference to widely available C4 resources. The inferred consumption of C3 monocotyledons, and wood or bark, increases the known variety of early hominin foods. The overall dietary pattern of these two individuals contrasts with available data for other hominins in the region and elsewhere.

Stable isotopes in fossil hominin tooth enamel suggest a fundamental dietary shift in the Pliocene.

Accumulating isotopic evidence from fossil hominin tooth enamel has provided unexpected insights into early hominin dietary ecology. Among the South African australopiths, these data demonstrate significant contributions to the diet of carbon originally fixed by C4 photosynthesis, consisting of C4 tropical/savannah grasses and certain sedges, and/or animals eating C4 foods. Moreover, high-resolution analysis of tooth enamel reveals strong intra-tooth variability in many cases, suggesting seasonal-scale dietary shifts. This pattern is quite unlike that seen in any great apes, even ‘savannah’ chimpanzees. The overall proportions of C4 input persisted for well over a million years, even while environments shifted from relatively closed (ca 3 Ma) to open conditions after ca 1.8 Ma. Data from East Africa suggest a more extreme scenario, where results for Paranthropus boisei indicate a diet dominated (approx. 80%) by C4 plants, in spite of indications from their powerful ‘nutcracker’ morphology for diets of hard objects. We argue that such evidence for engagement with C4 food resources may mark a fundamental transition in the evolution of hominin lineages, and that the pattern had antecedents prior to the emergence of Australopithecus africanus. Since new isotopic evidence from Aramis suggests that it was not present in Ardipithecus ramidus at 4.4 Ma, we suggest that the origins lie in the period between 3 and 4 Myr ago.