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.

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.

Using Maize δ15N values to assess soil fertility in fifteenth- and sixteenth-century ad Iroquoian agricultural fields.

Native Americans developed agronomic practices throughout the Western Hemisphere adapted to regional climate, edaphic conditions, and the extent of dependence on agriculture for subsistence. These included the mounding or "corn hill" system in northeastern North America. Iroquoian language speakers of present-day New York, USA, and Ontario and Québec, Canada were among those who used this system. While well-known, there has been little archaeological documentation of the system. As a result, there is scant archaeological evidence on how Iroquoian farmers maintained soil fertility in their often-extensive agricultural fields. Using δ15N values obtained on fifteenth- and sixteenth-century AD maize kernels from archaeological sites in New York and Ontario, adjusted to take into account changes that result from charring as determined through experiments, we demonstrate that Iroquoian farmers were successful at maintaining nitrogen in their agricultural fields. These results add to our archaeological knowledge of Iroquoian agronomic practices. Our results also indicate the potential value of obtaining δ15N values on archaeological maize in the investigation of Native American agronomic practices.

Reply to Van Valkenburgh et al.

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

High variability within pet foods prevents the identification of native species in pet cats' diets using isotopic evaluation.

Domestic cats preying on wildlife is a frequent conservation concern but typical approaches for assessing impacts rely on owner reports of prey returned home, which can be biased by inaccurate reporting or by cats consuming prey instead of bringing it home. Isotopes offer an alternative way to quantify broad differences in animal diets. By obtaining samples of pet food from cat owners we predicted that we would have high power to identify cats feeding on wild birds or mammals, given that pet food is thought to have higher C isotope values, due to the pervasive use of corn and/or corn by-products as food ingredients, than native prey. We worked with citizen scientists to quantify the isotopes of 202 cat hair samples and 239 pet food samples from the US and UK. We also characterized the isotopes of 11 likely native prey species from the southeastern US and used mixing models to assess the diet of 47 cats from the same region. Variation in C and N isotope values for cat food was very high, even within the same brand/flavor, suggesting that pet food manufacturers use a wide range of ingredients, and that these may change over time. Cat food and cat hair from the UK had lower C values than the US, presumably reflecting differences in the amount of corn used in the food chains of the two countries. This high variation in pet food reduced our ability to classify cats as hunters of native prey, such that only 43% of the animals could be confidently assigned. If feral or free ranging cats were considered, this uncertainty would be even higher as pet food types would be unknown. Our results question the general assumption that anthropogenic foods always have high C isotope values, because of the high variability we documented within one product type (cat food) and between countries (US vs. UK), and emphasize the need to test a variety of standards before making conclusions from isotope ecology studies.

Fish and maize: Bayesian mixing models of fourteenth- through seventeenth-century AD ancestral Wendat diets, Ontario, Canada.

Freshwater and marine fish have been important components of human diets for millennia. The Great Lakes of North America, their tributaries and smaller regional freshwater bodies are important Native American fisheries. The ethnohistorical record, zooarchaeological remains, and isotopic values on human bone and tooth collagen indicate the importance of fish in fourteenth- through seventeenth-century ancestral Wendat diets in southern Ontario, which is bordered by three of the Great Lakes. Maize (Zea mays ssp. mays) was the primary grain of Native American agricultural systems in the centuries prior to and following sustained European presence. Here we report new Bayesian dietary mixing models using previously published δ13C and δ15N values on ancestral Wendat bone and tooth collagen and tooth enamel. The results confirm previous estimates from δ13C values that ancestral Wendat diets included high proportions of maize but indicate much higher proportions of fish than has previously been recognized. The results also suggest that terrestrial animals contributed less to ancestral Wendat diets than is typically interpreted based on zooarchaeological records.

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.

Freshwater reservoir offsets on radiocarbon-dated dog bone from the headwaters of the St. Lawrence River, USA.

Isotopic analysis of dog (Canis lupus familiaris) bone recovered from archaeological sites as proxies for human bone is becoming common in North America. Chronological placement of the dogs is often determined through radiocarbon dating of dog bone. The Great Lakes, their tributaries, and nearby lakes and streams were important fisheries for Native Americans prior to and after sustained European presence in the region. Carbon entering the food web in freshwater systems is often not in full isotopic equilibrium with the atmosphere, giving rise to spuriously old radiocarbon ages in fish, other aquatic organisms, and their consumers. These freshwater reservoir offsets (FROs) have been noted on human and dog bone in several areas of the world. Here we report the results of multi-tracer Bayesian dietary modeling using δ15N and δ13C values on dog bone collagen from mid-fifteenth to mid-sixteenth-century Iroquoian village sites at the headwaters of the St. Lawrence River, New York, USA. Results indicate that fish was an important component of dog diets. A comparison of radiocarbon dates on dog bone with dates on deer bone or maize from the same sites indicate FROs ranging from 97 ± 24 to 220 ± 39 14Cyr with a weighted mean of 132 ± 8 14Cyr. These results suggest that dog bone should not be used for radiocarbon dating in the absence of modeling to determine fish consumption and that previously reported radiocarbon dates on human bone from the larger region are likely to have FROs given the known importance of fish in regional human diets.

Peptide sequences from the first Castoroides ohioensis skull and the utility of old museum collections for palaeoproteomics.

Vertebrate fossils have been collected for hundreds of years and are stored in museum collections around the world. These remains provide a readily available resource to search for preserved proteins; however, the vast majority of palaeoproteomic studies have focused on relatively recently collected bones with a well-known handling history. Here, we characterize proteins from the nasal turbinates of the first Castoroides ohioensis skull ever discovered. Collected in 1845, this is the oldest museum-curated specimen characterized using palaeoproteomic tools. Our mass spectrometry analysis detected many collagen I peptides, a peptide from haemoglobin beta, and in vivo and diagenetic post-translational modifications. Additionally, the identified collagen I sequences provide enough resolution to place C. ohioensis within Rodentia. This study illustrates the utility of archived museum specimens for both the recovery of preserved proteins and phylogenetic analyses.

Exploring the Potential of Laser Ablation Carbon Isotope Analysis for Examining Ecology during the Ontogeny of Middle Pleistocene Hominins from Sima de los Huesos (Northern Spain).

Laser ablation of tooth enamel was used to analyze stable carbon isotope compositions of teeth of hominins, red deer, and bears from middle Pleistocene sites in the Sierra de Atapuerca in northern Spain, to investigate the possibility that this technique could be used as an additional tool to identify periods of physiological change that are not detectable as changes in tooth morphology. Most of the specimens were found to have minimal intra-tooth variation in carbon isotopes (< 2.3‰), suggesting isotopically uniform diets through time and revealing no obvious periods of physiological change. However, one of the two sampled hominin teeth displayed a temporal carbon isotope shift (3.2‰) that was significantly greater than observed for co-occurring specimens. The δ13C value of this individual averaged about -16‰ early in life, and -13‰ later in life. This isotopic change occurred on the canine crown about 4.2 mm from the root, which corresponds to an approximate age of two to four years old in modern humans. Our dataset is perforce small owing to the precious nature of hominid teeth, but it demonstrates the potential utility of the intra-tooth isotope profile method for extracting ontogenetic histories of human ancestors.

Using a Novel Absolute Ontogenetic Age Determination Technique to Calculate the Timing of Tooth Eruption in the Saber-Toothed Cat, Smilodon fatalis.

Despite the superb fossil record of the saber-toothed cat, Smilodon fatalis, ontogenetic age determination for this and other ancient species remains a challenge. The present study utilizes a new technique, a combination of data from stable oxygen isotope analyses and micro-computed tomography, to establish the eruption rate for the permanent upper canines in Smilodon fatalis. The results imply an eruption rate of 6.0 millimeters per month, which is similar to a previously published average enamel growth rate of the S. fatalis upper canines (5.8 millimeters per month). Utilizing the upper canine growth rate, the upper canine eruption rate, and a previously published tooth replacement sequence, this study calculates absolute ontogenetic age ranges of tooth development and eruption in S. fatalis. The timing of tooth eruption is compared between S. fatalis and several extant conical-toothed felids, such as the African lion (Panthera leo). Results suggest that the permanent dentition of S. fatalis, except for the upper canines, was fully erupted by 14 to 22 months, and that the upper canines finished erupting at about 34 to 41 months. Based on these developmental age calculations, S. fatalis individuals less than 4 to 7 months of age were not typically preserved at Rancho La Brea. On the whole, S. fatalis appears to have had delayed dental development compared to dental development in similar-sized extant felids. This technique for absolute ontogenetic age determination can be replicated in other ancient species, including non-saber-toothed taxa, as long as the timing of growth initiation and growth rate can be determined for a specific feature, such as a tooth, and that growth period overlaps with the development of the other features under investigation.

Brooktrout Lake case study: biotic recovery from acid deposition 20 years after the 1990 Clean Air Act Amendments.

The Adirondack Mountain region is an extensive geographic area (26,305 km(2)) in upstate New York where acid deposition has negatively affected water resources for decades and caused the extirpation of local fish populations. The water quality decline and loss of an established brook trout (Salvelinus fontinalis [Mitchill]) population in Brooktrout Lake were reconstructed from historical information dating back to the late 1880s. Water quality and biotic recovery were documented in Brooktrout Lake in response to reductions of S deposition during the 1980s, 1990s, and 2000s and provided a unique scientific opportunity to re-introduce fish in 2005 and examine their critical role in the recovery of food webs affected by acid deposition. Using C and N isotope analysis of fish collagen and state hatchery feed as well as Bayesian assignment tests of microsatellite genotypes, we document in situ brook trout reproduction, which is the initial phase in the restoration of a preacidification food web structure in Brooktrout Lake. Combined with sulfur dioxide emissions reductions promulgated by the 1990 Clean Air Act Amendments, our results suggest that other acid-affected Adirondack waters could benefit from careful fish re-introduction protocols to initiate the ecosystem reconstruction of important components of food web dimensionality and functionality.

Effects of global warming on ancient mammalian communities and their environments.

BACKGROUND: Current global warming affects the composition and dynamics of mammalian communities and can increase extinction risk; however, long-term effects of warming on mammals are less understood. Dietary reconstructions inferred from stable isotopes of fossil herbivorous mammalian tooth enamel document environmental and climatic changes in ancient ecosystems, including C(3)/C(4) transitions and relative seasonality. METHODOLOGY/PRINCIPAL FINDINGS: Here, we use stable carbon and oxygen isotopes preserved in fossil teeth to document the magnitude of mammalian dietary shifts and ancient floral change during geologically documented glacial and interglacial periods during the Pliocene (approximately 1.9 million years ago) and Pleistocene (approximately 1.3 million years ago) in Florida. Stable isotope data demonstrate increased aridity, increased C(4) grass consumption, inter-faunal dietary partitioning, increased isotopic niche breadth of mixed feeders, niche partitioning of phylogenetically similar taxa, and differences in relative seasonality with warming. CONCLUSION/SIGNIFICANCE: Our data show that global warming resulted in dramatic vegetation and dietary changes even at lower latitudes (approximately 28 degrees N). Our results also question the use of models that predict the long term decline and extinction of species based on the assumption that niches are conserved over time. These findings have immediate relevance to clarifying possible biotic responses to current global warming in modern ecosystems.

Determining landscape use of Holocene mammals using strontium isotopes.

The use of the landscape by animals is predicted to be a function of their body size. However, empirical data relating these two variables from an array of body sizes within a single mammalian community are scarce. We tested this prediction by assessing landscape use of mammals by analyzing strontium (Sr) isotope signatures found in mammalian hard tissues representing a 3,000-year record. We examined: (1) the Sr-determined landscape area of small (approximately 100 g), medium (approximately 1,500 g) and large (approximately 100,000 g) mammals, and; (2) whether the area used by these mammals varied during periods of environmental change. Strontium isotope values were obtained from 46 specimens from the Holocene paleontological deposits of Lamar Cave and Waterfall Locality in Wyoming, USA, as well as from 13 modern ungulate specimens from the same area. Our data indicate that medium- and large-sized species use larger percentages of the landscape than do species of small body size. The isotope values for specimens from each of the paleontological sites are similar across all stratigraphic levels, suggesting no change in home range over the last 3,000 years, even though climate is known to have fluctuated at these sites over this time period. Further, our study verifies that the fossil localities represent the local community. Where bedrock geology is appropriate, the use of strontium isotope analyses provides a valuable tool for discerning landscape use by vertebrate communities, an important though generally difficult aspect of an ancient species niche to identify.

Assessing the causes of late Pleistocene extinctions on the continents.

One of the great debates about extinction is whether humans or climatic change caused the demise of the Pleistocene megafauna. Evidence from paleontology, climatology, archaeology, and ecology now supports the idea that humans contributed to extinction on some continents, but human hunting was not solely responsible for the pattern of extinction everywhere. Instead, evidence suggests that the intersection of human impacts with pronounced climatic change drove the precise timing and geography of extinction in the Northern Hemisphere. The story from the Southern Hemisphere is still unfolding. New evidence from Australia supports the view that humans helped cause extinctions there, but the correlation with climate is weak or contested. Firmer chronologies, more realistic ecological models, and regional paleoecological insights still are needed to understand details of the worldwide extinction pattern and the population dynamics of the species involved.