Early specialized maritime and maize economies on the north coast of Peru.

We assess diet and economies of middle Holocene (∼7,500 to 4,000 calibrated [cal] B.P.) humans at coexisting mound sites (Huaca Prieta and Paredones) in north coastal Peru and document regular consumption of maize by ∼6,500 to 6,000 cal B.P. and its earliest use as a staple food in this area of the Andes between 5,000 and 4,500 cal B.P. Stable isotope data from enamel carbonates and dentin collagen (childhood diet) and dental microwear texture analysis (adult diet) demonstrate dietary and economic specialization. Previous studies revealed maize and mixed-food refuse at both sites, but this study documents actual food consumption, showing that these communities situated a few hundred meters apart had significantly distinct diets in childhood and adulthood. Huaca Prieta focused on marine resources, although there are some contributions from terrestrial meat. Paredones individuals primarily consumed maize during childhood (up to 70% of the juvenile diet), as shown by δ13C values, apatite-collagen spacing, and discriminant analysis of δ13Ccoll, δ13Ccarb, and δ15N values. Maize was likely used as a weaning food (e.g., gruel and/or chicha-a maize beverage), hinting at the significant role of breastfeeding mothers, weanling infants, and children in the development of maize as a staple crop. Additionally, dental microwear data show Paredones adult diets are high in abrasives, potentially from maize processing. The distinct foodways at these neighboring sites result from and also reflect their social and political distinctions. These differences in food production, distribution, and consumption generated opportunities for exchange, an interaction that bound them together in mutual benefit.

Global long-term stability of individual dietary specialization in herbivorous mammals.

Dietary variation within species has important ecological and evolutionary implications. While theoreticians have debated the consequences of trait variance (including dietary specialization), empirical studies have yet to examine intraspecific dietary variability across the globe and through time. Here, we use new and published serial sampled δ13Cenamel values of herbivorous mammals from the Miocene to the present (318 individuals summarized, 4134 samples) to examine how dietary strategy (i.e. browser, mixed-feeder, grazer) affects individual isotopic variation. We find that almost all herbivores, regardless of dietary strategy, are composed of individual specialists. For example, Cormohipparion emsliei (Equidae) from the Pliocene of Florida (approx. 5 Ma) exhibits a δ13Cenamel range of 13.4‰, but all individuals sampled have δ13Cenamel ranges of less than or equal to 2‰ (mean = 1.1‰). Most notably, this pattern holds globally and through time, with almost all herbivorous mammal individuals exhibiting narrow δ13Cenamel ranges (less than or equal to 3‰), demonstrating that individuals are specialized and less representative of their overall species' dietary breadth. Individual specialization probably reduces intraspecific competition, increases carrying capacities, and may have stabilizing effects on species and communities over time. Individual specialization among species with both narrow and broad dietary niches is common over space and time-a phenomenon not previously well recognized or documented empirically.

Dietary plasticity of North American herbivores: a synthesis of stable isotope data over the past 7 million years.

Palaeoecological interpretations are based on our understanding of dietary and habitat preferences of fossil taxa. While morphology provides approximations of diets, stable isotope proxies provide insights into the realized diets of animals. We present a synthesis of the isotopic ecologies (δ13C from tooth enamel) of North American mammalian herbivores since approximately 7 Ma. We ask: (i) do morphological interpretations of dietary behaviour agree with stable isotope proxy data? (ii) are grazing taxa specialists, or is grazing a means to broaden the dietary niche? and (iii) how is dietary niche breadth attained in taxa at the local level? We demonstrate that while brachydont taxa are specialized as browsers, hypsodont taxa often have broader diets that included more browse consumption than previously anticipated. It has long been accepted that morphology imposes limits on the diet; this synthesis supports prior work that herbivores with 'grazing' adaptions, such as hypsodont teeth, have the ability to consume grass but are also able to eat other foods. Notably, localized dietary breadth of even generalist taxa can be narrow (approx. 30 to 60% of a taxon's overall breadth). This synthesis demonstrates that 'grazing-adapted' taxa are varied in their diets across space and time, and this flexibility may reduce competition among ancient herbivores.

Dietary ecology of Alaskan polar bears (Ursus maritimus) through time and in response to Arctic climate change.

Arctic climate change poses serious threats to polar bears (Ursus maritimus) as reduced sea ice makes seal prey inaccessible and marine ecosystems undergo bottom-up reorganization. Polar bears' elongated skulls and reduced molar dentition, as compared to their sister species the grizzly bear (Ursus arctos), are adaptations associated with hunting seals on sea ice and a soft, lipid-rich diet of blubber and meat. With significant declines in sea ice, it is unclear if and how polar bears may be altering their diets. Clarifying polar bear dietary responses to changing climates, both today and in the past, is critical to proper conservation and management of this apex predator. This is particularly important when a dietary strategy may be maladaptive. Here, we test the hypothesis that hard-food consumption (i.e., less preferred foods including bone), inferred from dental microwear texture analysis, increased with Arctic warming. We find that polar bears demonstrate a conserved absence of hard-object feeding in Alaska through time (including approximately 1000 years ago), until the 21st century, consistent with a highly conserved and specialized diet of soft blubber and flesh. Notably, our results also suggest that some 21st-century polar bears may be consuming harder foods (e.g., increased carcass utilization, terrestrial foods including garbage), despite having skulls and metabolisms poorly suited for such a diet. Prior to the 21st century, only polar bears with larger mandibles demonstrated increased hard-object feeding, though to a much lower degree than closely related grizzly bears which regularly consume mechanically challenging foods. Polar bears, being morphologically specialized, have biomechanical constraints which may limit their ability to consume mechanically challenging diets, with dietary shifts occurring only under the most extreme scenarios. Collectively, the highly specialized diets and cranial morphology of polar bears may severely limit their ability to adapt to a warming Arctic.

Ecosystem engineering in the Quaternary of the West Coast of South Africa.

Despite advances in our understanding of the geographic and temporal scope of the Paleolithic record, we know remarkably little about the evolutionary and ecological consequences of changes in human behavior. Recent inquiries suggest that human evolution reflects a long history of interconnections between the behavior of humans and their surrounding ecosystems (e.g., niche construction). Developing expectations to identify such phenomena is remarkably difficult because it requires understanding the multi-generational impacts of changes in behavior. These long-term dynamics require insights into the emergent phenomena that alter selective pressures over longer time periods which are not possible to observe, and are also not intuitive based on observations derived from ethnographic time scales. Generative models show promise for probing these potentially unexpected consequences of human-environment interaction. Changes in the uses of landscapes may have long term implications for the environments that hominins occupied. We explore other potential proxies of behavior and examine how modeling may provide expectations for a variety of phenomena.

Cougars' key to survival through the Late Pleistocene extinction: insights from dental microwear texture analysis.

Cougars (Puma concolor) are one of only two large cats in North America to have survived the Late Pleistocene extinction (LPE), yet the specific key(s) to their relative success remains unknown. Here, we compare the dental microwear textures of Pleistocene cougars with sympatric felids from the La Brea Tar Pits in southern California that went extinct at the LPE (Panthera atrox and Smilodon fatalis), to clarify potential dietary factors that led to the cougar's persistence through the LPE. We further assess whether the physical properties of food consumed have changed over time when compared with modern cougars in southern California. Using dental microwear texture analysis (DMTA), which quantifies surface features in three dimensions, we find that modern and Pleistocene cougars are not significantly different from modern African lions in any DMTA attributes, suggesting moderate durophagy (i.e. bone processing). Pleistocene cougars from La Brea have significantly greater complexity and textural fill volume than Panthera atrox (inferred to have primarily consumed flesh from fresh kills) and significantly greater variance in complexity values than S. fatalis. Ultimately, these results suggest that cougars already used or adopted a more generalized dietary strategy during the Pleistocene that may have been key to their subsequent success.

Is Rapoport's rule a recent phenomenon? A deep time perspective on potential causal mechanisms.

Macroecology strives to identify ecological patterns on broad spatial and temporal scales. One such pattern, Rapoport's rule, describes the tendency of species' latitudinal ranges to increase with increasing latitude. Several mechanisms have been proposed to explain this rule. Some invoke climate, either through glaciation driving differential extinction of northern species or through increased seasonal variability at higher latitudes causing higher thermal tolerances and subsequently larger ranges. Alternatively, continental tapering or higher interspecific competition at lower latitudes may be responsible. Assessing the incidence of Rapoport's rule through deep time can help to distinguish between competing explanations. Using fossil occurrence data from the Palaeobiology Database, we test these hypotheses by evaluating mammalian compliance with the rule throughout the Caenozoic of North America. Adherence to Rapoport's rule primarily coincides with periods of intense cooling and increased seasonality, suggesting that extinctions caused by changing climate may have played an important role in erecting the latitudinal gradients in range sizes seen today.

Pre-Younger Dryas megafaunal extirpation at Rancho La Brea linked to fire-driven state shift.

The cause, or causes, of the Pleistocene megafaunal extinctions have been difficult to establish, in part because poor spatiotemporal resolution in the fossil record hinders alignment of species disappearances with archeological and environmental data. We obtained 172 new radiocarbon dates on megafauna from Rancho La Brea in California spanning 15.6 to 10.0 thousand calendar years before present (ka). Seven species of extinct megafauna disappeared by 12.9 ka, before the onset of the Younger Dryas. Comparison with high-resolution regional datasets revealed that these disappearances coincided with an ecological state shift that followed aridification and vegetation changes during the Bølling-Allerød (14.69 to 12.89 ka). Time-series modeling implicates large-scale fires as the primary cause of the extirpations, and the catalyst of this state shift may have been mounting human impacts in a drying, warming, and increasingly fire-prone ecosystem.

Extinction implications of a chenopod browse diet for a giant Pleistocene kangaroo.

Kangaroos are the world's most diverse group of herbivorous marsupials. Following late-Miocene intensification of aridity and seasonality, they radiated across Australia, becoming the continent's ecological equivalents of the artiodactyl ungulates elsewhere. Their diversity peaked during the Pleistocene, but by approximately 45,000 years ago, 90% of larger kangaroos were extinct, along with a range of other giant species. Resolving whether climate change or human arrival was the principal extinction cause remains highly contentious. Here we combine craniodental morphology, stable-isotopic, and dental microwear data to reveal that the largest-ever kangaroo, Procoptodon goliah, was a chenopod browse specialist, which may have had a preference for Atriplex (saltbushes), one of a few dicots using the C(4) photosynthetic pathway. Furthermore, oxygen isotope signatures of P. goliah tooth enamel show that it drank more in low-rainfall areas than its grazing contemporaries, similar to modern saltbush feeders. Saltbushes and chenopod shrublands in general are poorly flammable, so landscape burning by humans is unlikely to have caused a reduction in fodder driving the species to extinction. Aridity is discounted as a primary cause because P. goliah evolved in response to increased aridity and disappeared during an interval wetter than many it survived earlier. Hunting by humans, who were also bound to water, may have been a more decisive factor in the extinction of this giant marsupial.

Dietary ecology of the scimitar-toothed cat Homotherium serum.

The scimitar-toothed cat Homotherium was one of the most cosmopolitan cats of the Pleistocene, present throughout Eurasia, Africa, and the Americas until at least ~28 thousand years ago.1-3 Friesenhahn Cave (Bexar County, Texas) contains some of the best-preserved specimens of Homotherium serum alongside an abundance of juvenile mammoths, leading some to argue that H. serum preferentially hunted juvenile mammoths.1,4 Dietary data of Homotherium are rare, with their ecology inferred from morphological, taphonomic, and genetic data.1,3-10 Here, we use a multi-proxy approach to clarify the dietary ecology of H. serum as compared to extinct and extant cats and their relatives. Dental microwear texture analysis (DMTA) reveals that H. serum consumed soft and tough foods, similar to the extant cheetah, which actively avoids bone,11,12 but in stark contrast to extant lions and hyenas, which are observed to engage in durophagy (i.e., bone processing).11-14 DMTA data are consistent with taphonomic evidence of bone defleshing and the absence of bone-crunching behavior in H. serum. Stable carbon isotope values of H. serum indicate a clear preference for C4 grazers including juvenile mammoths, in agreement with taphonomic evidence suggestive of a "Homotherium den"1,4 and morphological data indicative of a relatively cursorial lifestyle.6-8 Notably, the inferred diet of H. serum contrasts with the extinct dirk-tooth sabertooth cat Smilodon fatalis, which preferred forest/woodland prey and engaged in bone processing.15-19Homotherium serum exhibited a novel combination of morphological adaptations for acquiring open-country prey, consuming their soft and tough flesh-including the tough flesh of juvenile mammoths. VIDEO ABSTRACT.

Clarifying relationships between cranial form and function in tapirs, with implications for the dietary ecology of early hominins.

Paleontologists and paleoanthropologists have long debated relationships between cranial morphology and diet in a broad diversity of organisms. While the presence of larger temporalis muscle attachment area (via the presence of sagittal crests) in carnivorans is correlated with durophagy (i.e. hard-object feeding), many primates with similar morphologies consume an array of tough and hard foods-complicating dietary inferences of early hominins. We posit that tapirs, large herbivorous mammals showing variable sagittal crest development across species, are ideal models for examining correlations between textural properties of food and sagittal crest morphology. Here, we integrate dietary data, dental microwear texture analysis, and finite element analysis to clarify the functional significance of the sagittal crest in tapirs. Most notably, pronounced sagittal crests are negatively correlated with hard-object feeding in extant, and several extinct, tapirs and can actually increase stress and strain energy. Collectively, these data suggest that musculature associated with pronounced sagittal crests-and accompanied increases in muscle volume-assists with the processing of tough food items in tapirs and may yield similar benefits in other mammals including early hominins.

Reply to Van Valkenburgh et al.

DeSantis et al. respond to the concerns raised by Van Valkenburgh et al. on their original study.

A year in the life of a giant ground sloth during the Last Glacial Maximum in Belize.

Stable isotope analysis of the first fossilized Eremotherium laurillardi remains from Belize offers valuable insights into the conditions within which this individual lived and its ability to adapt to the increasing aridity of the Last Glacial Maximum (LGM). Cathodoluminescence (CL) microscopy was used to identify chemical alteration of the tooth during fossilization. Results demonstrate that the inner orthodentin resists diagenesis, yielding potentially unaltered values. Using an intensive "vacuum milling" technique, the inner orthodentin produced an accelerator mass spectrometry (AMS) date of 26,975 ± 120 calibrated years before the present. The stable carbon and oxygen isotope analysis of this layer shows that the tooth recorded two wet seasons separated by one longer dry season and that this sloth was able to adapt its diet to the marked seasonality of the LGM. This study offers new insights into obtaining reliable isotope data from fossilized remains and suggests that this individual adapted to climate shifts, contributing to the conversation surrounding megafauna extinction.

Causes and Consequences of Pleistocene Megafaunal Extinctions as Revealed from Rancho La Brea Mammals.

The fossils preserved in the Rancho La Brea "tar" seeps in southern California span the past ∼50,000 years and provide a rare opportunity to assess the ecology of predators (e.g., the American lion, sabertooth cats, cougars, dire wolves, gray wolves, and coyotes), including clarifying the causes and consequences of the terminal Pleistocene extinction event. Here, a multi-proxy approach elucidates dietary responses of carnivorans to changing climates and megafaunal extinctions. Using sample sizes that are unavailable anywhere else in the world, including hundreds of carnivoran and herbivore specimens, we clarify the paleobiology of the extinct sabertooth cats and dire wolves-overturning the idea that they heavily competed for similar prey. Canids (especially the dire wolf) consumed prey from more open environments than felids, demonstrating minimal competition for prey throughout the latest Pleistocene and largely irrespective of changing climates, including just prior to their extinction. Coyotes experienced a dramatic shift in dietary behavior toward increased carcass utilization and the consumption of forest resources (prey and/or plant resources) after the terminal Pleistocene megafaunal extinction. Extant predators' ability to effectively hunt smaller prey and/or utilize carcasses may have been a key to their survival, especially after a significant reduction in megafaunal prey resources. Collectively, these data suggest that dietary niches of carnivorans are not always static and can instead be substantially affected by the removal of top predators and abundant prey resources.

Effects of climate on dental mesowear of extant koalas and two broadly distributed kangaroos throughout their geographic range.

Dental mesowear analysis can classify the diets of extant herbivores into general categories such as grazers, mixed-feeders, and browsers by using the gross wear patterns found on individual teeth. This wear presumably results from both abrasion (food-on-tooth wear) and attrition (tooth-on-tooth wear) of individual teeth. Mesowear analyses on extinct ungulates have helped generate hypotheses regarding the dietary ecology of mammals across space and time, and recent developments have expanded the use of dental mesowear analysis to herbivorous marsupial taxa including kangaroos, wombats, possums, koalas, and relatives. However, the diet of some of the most ubiquitous kangaroos (e.g., Macropus giganteus) along with numerous other species cannot be successfully classified by dental mesowear analysis. Further, it is not well understood whether climate variables (including precipitation, relative humidity, and temperature) are correlated with dental mesowear variables including various measures of shape and relief. Here, we examine the relationship between dental mesowear variables (including traditional methods scoring the sharpest cusp and a new potential assessment of multiple cusps) and climate variables in the grazers/mixed feeders Macropus giganteus and Macropus fuliginosus, and the obligate browser Phascolarctos cinereus. We find that dental mesowear of mandibular teeth is capable of differentiating the dietary habits of koalas and the kangaroo species. Furthermore, both Macropus giganteus and Phascolarctos cinereus exhibit mesowear correlated with mean minimum temperature, while Macropus fuliginosus dental mesowear is unaffected by temperature, despite significant differences in mean minimum and mean maximum temperature across their distribution (and in the specimens examined here). Contrary to expectations that individuals from drier regions would have blunter and lower relief teeth, dental mesowear is unrelated to proxies of relative aridity-including mean annual precipitation and relative humidity. Collectively, dental mesowear in these marsupials is related to feeding behavior with increased wear in cooler regions (in Macropus giganteus and Phascolarctos cinereus) potentially related to more or different food resources consumed.

Dietary behaviour of man-eating lions as revealed by dental microwear textures.

Lions (Panthera leo) feed on diverse prey species, a range that is broadened by their cooperative hunting. Although humans are not typical prey, habitual man-eating by lions is well documented. Fathoming the motivations of the Tsavo and Mfuwe man-eaters (killed in 1898 in Kenya and 1991 in Zambia, respectively) may be elusive, but we can clarify aspects of their behaviour using dental microwear texture analysis. Specifically, we analysed the surface textures of lion teeth to assess whether these notorious man-eating lions scavenged carcasses during their depredations. Compared to wild-caught lions elsewhere in Africa and other large feliforms, including cheetahs and hyenas, dental microwear textures of the man-eaters do not suggest extreme durophagy (e.g. bone processing) shortly before death. Dental injuries to two of the three man-eaters examined may have induced shifts in feeding onto softer foods. Further, prompt carcass reclamation by humans likely limited the man-eaters' access to bones. Man-eating was likely a viable alternative to hunting and/or scavenging ungulates due to dental disease and/or limited prey availability.

Biodiversity and Topographic Complexity: Modern and Geohistorical Perspectives.

Topographically complex regions on land and in the oceans feature hotspots of biodiversity that reflect geological influences on ecological and evolutionary processes. Over geologic time, topographic diversity gradients wax and wane over millions of years, tracking tectonic or climatic history. Topographic diversity gradients from the present day and the past can result from the generation of species by vicariance or from the accumulation of species from dispersal into a region with strong environmental gradients. Biological and geological approaches must be integrated to test alternative models of diversification along topographic gradients. Reciprocal illumination among phylogenetic, phylogeographic, ecological, paleontological, tectonic, and climatic perspectives is an emerging frontier of biogeographic research.

Was the giant short-faced bear a hyper-scavenger? A new approach to the dietary study of ursids using dental microwear textures.

Dramatic environmental changes associated with global cooling since the late Miocene, and the onset of glacial-interglacial cycles in the Pleistocene served as a backdrop to the evolutionary radiation of modern bears (family Ursidae). These environmental changes likely prompted changes in food availability, and triggered dietary adaptations that served as motive forces in ursid evolution. Here, we assess correspondence of dental microwear textures of first and second lower molars with diet in extant ursids. We use the resulting baseline data to evaluate the hypothesis that the Pleistocene giant short-faced bear, Arctodus simus, was a bone consumer and hyper-scavenger at Rancho La Brea, California, USA. Significant variation along the tooth row is consistent with functional differentiation, with the second molar serving as a better dietary recorder than the first. Results evince significant variation among species: carnivorous and omnivorous ursids (Ursus maritimus, U. americanus) have significantly higher and more variable complexity (Asfc) than more herbivorous ones (Ailuropoda melanoleuca, Tremarctos ornatus, U. malayanus), and A. melanoleuca is differentiated from U. maritimus and U. americanus by significantly higher and more variable anisotropy (epLsar) values. Arctodus simus from Rancho La Brea exhibits wear attributes most comparable to its closest living relative (T. ornatus), which is inconsistent with hard-object (e.g., bone) consumption, and the hypothesis that short-faced bears were bone consuming hyper-scavengers across their range.

Direct comparisons of 2D and 3D dental microwear proxies in extant herbivorous and carnivorous mammals.

The analysis of dental microwear is commonly used by paleontologists and anthropologists to clarify the diets of extinct species, including herbivorous and carnivorous mammals. Currently, there are numerous methods employed to quantify dental microwear, varying in the types of microscopes used, magnifications, and the characterization of wear in both two dimensions and three dimensions. Results from dental microwear studies utilizing different methods are not directly comparable and human quantification of wear features (e.g., pits and scratches) introduces interobserver error, with higher error being produced by less experienced individuals. Dental microwear texture analysis (DMTA), which analyzes microwear features in three dimensions, alleviates some of the problems surrounding two-dimensional microwear methods by reducing observer bias. Here, we assess the accuracy and comparability within and between 2D and 3D dental microwear analyses in herbivorous and carnivorous mammals at the same magnification. Specifically, we compare observer-generated 2D microwear data from photosimulations of the identical scanned areas of DMTA in extant African bovids and carnivorans using a scanning white light confocal microscope at 100x magnification. Using this magnification, dental microwear features quantified in 2D were able to separate grazing and frugivorous bovids using scratch frequency; however, DMTA variables were better able to discriminate between disparate dietary niches in both carnivorous and herbivorous mammals. Further, results demonstrate significant interobserver differences in 2D microwear data, with the microwear index remaining the least variable between experienced observers, consistent with prior research. Overall, our results highlight the importance of reducing observer error and analyzing dental microwear in three dimensions in order to consistently interpret diets accurately.