Male mastodon landscape use changed with maturation (late Pleistocene, North America).

Under harsh Pleistocene climates, migration and other forms of seasonally patterned landscape use were likely critical for reproductive success of mastodons (Mammut americanum) and other megafauna. However, little is known about how their geographic ranges and mobility fluctuated seasonally or changed with sexual maturity. We used a spatially explicit movement model that coupled strontium and oxygen isotopes from two serially sampled intervals (5+ adolescent years and 3+ adult years) in a male mastodon tusk to test for changes in landscape use associated with maturation and reproductive phenology. The mastodon's early adolescent home range was geographically restricted, with no evidence of seasonal preferences. Following inferred separation from the matriarchal herd (starting age 12 y), the adolescent male's mobility increased as landscape use expanded away from his natal home range (likely central Indiana). As an adult, the mastodon's monthly movements increased further. Landscape use also became seasonally structured, with some areas, including northeast Indiana, used only during the inferred mastodon mating season (spring/summer). The mastodon died in this area (>150 km from his core, nonsummer range) after sustaining a craniofacial injury consistent with a fatal blow from a competing male's tusk during a battle over access to mates. Northeast Indiana was likely a preferred mating area for this individual and may have been regionally significant for late Pleistocene mastodons. Similarities between mammutids and elephantids in herd structure, tusk dimorphism, tusk function, and the geographic component of male maturation indicate that these traits were likely inherited from a common ancestor.

Late Holocene spread of pastoralism coincides with endemic megafaunal extinction on Madagascar.

Recently expanded estimates for when humans arrived on Madagascar (up to approximately 10 000 years ago) highlight questions about the causes of the island's relatively late megafaunal extinctions (approximately 2000-500 years ago). Introduced domesticated animals could have contributed to extinctions, but the arrival times and past diets of exotic animals are poorly known. To conduct the first explicit test of the potential for competition between introduced livestock and extinct endemic megafauna in southern and western Madagascar, we generated new radiocarbon and stable carbon and nitrogen isotope data from the bone collagen of introduced ungulates (zebu cattle, ovicaprids and bushpigs, n = 66) and endemic megafauna (pygmy hippopotamuses, giant tortoises and elephant birds, n = 68), and combined these data with existing data from endemic megafauna (n = 282, including giant lemurs). Radiocarbon dates confirm that introduced and endemic herbivores briefly overlapped chronologically in this region between 1000 and 800 calibrated years before present (cal BP). Moreover, stable isotope data suggest that goats, tortoises and hippos had broadly similar diets or exploited similar habitats. These data support the potential for both direct and indirect forms of competition between introduced and endemic herbivores. We argue that competition with introduced herbivores, mediated by opportunistic hunting by humans and exacerbated by environmental change, contributed to the late extinction of endemic megafauna on Madagascar.

Evolutionary and phylogenetic insights from a nuclear genome sequence of the extinct, giant, "subfossil" koala lemur Megaladapis edwardsi.

No endemic Madagascar animal with body mass >10 kg survived a relatively recent wave of extinction on the island. From morphological and isotopic analyses of skeletal "subfossil" remains we can reconstruct some of the biology and behavioral ecology of giant lemurs (primates; up to ∼160 kg) and other extraordinary Malagasy megafauna that survived into the past millennium. Yet, much about the evolutionary biology of these now-extinct species remains unknown, along with persistent phylogenetic uncertainty in some cases. Thankfully, despite the challenges of DNA preservation in tropical and subtropical environments, technical advances have enabled the recovery of ancient DNA from some Malagasy subfossil specimens. Here, we present a nuclear genome sequence (∼2× coverage) for one of the largest extinct lemurs, the koala lemur Megaladapis edwardsi (∼85 kg). To support the testing of key phylogenetic and evolutionary hypotheses, we also generated high-coverage nuclear genomes for two extant lemurs, Eulemur rufifrons and Lepilemur mustelinus, and we aligned these sequences with previously published genomes for three other extant lemurs and 47 nonlemur vertebrates. Our phylogenetic results confirm that Megaladapis is most closely related to the extant Lemuridae (typified in our analysis by E. rufifrons) to the exclusion of L. mustelinus, which contradicts morphology-based phylogenies. Our evolutionary analyses identified significant convergent evolution between M. edwardsi and an extant folivore (a colobine monkey) and an herbivore (horse) in genes encoding proteins that function in plant toxin biodegradation and nutrient absorption. These results suggest that koala lemurs were highly adapted to a leaf-based diet, which may also explain their convergent craniodental morphology with the small-bodied folivore Lepilemur.

Does faecal matter reflect location? An initial assessment of isotopic variability between consumed prey remains and faecal matter for wild jaguars.

Faecal isotopic analysis may complement other non-invasive wildlife survey tools for monitoring landscape use by carnivores, such as motion-detecting cameras and non-invasive genetic sampling. We analysed carbon, nitrogen, and strontium isotopes in faecal matter produced by jaguars (Panthera onca) as well as bones from consumed prey at the Mountain Pine Ridge Forest Reserve (MPR) in Belize, Central America. The MPR is ideally suited for a spatial isotope study as vegetation and geology both vary considerably. The isotopic composition of faecal matter should reflect the habitat and geology where consumed prey lived. We used bone from consumed prey recovered from jaguar scats as a proxy for diet. Faecal matter and bone showed comparable spatial isotopic trends, suggesting that the isotopic composition of jaguar faeces can be used to detect foraging in different habitats (pine forest versus broadleaf forest) or on different geologies (Mesozoic carbonates; Palaeozoic granite, contact metamorphics, and metasediments). This result is reassuring as bones are not always present in carnivore scats. Studying landscape use by cryptic and wide-ranging carnivore species like jaguars remains challenging. Isotopic analysis of faecal matter complements the existing array of non-invasive spatial monitoring tools.

A new interpretation of Madagascar's megafaunal decline: The "Subsistence Shift Hypothesis".

Fundamental disagreements remain regarding the relative importance of climate change and human activities as triggers for Madagascar's Holocene megafaunal extinction. We use stable isotope data from stalagmites from northwest Madagascar coupled with radiocarbon and butchery records from subfossil bones across the island to investigate relationships between megafaunal decline, climate change, and habitat modification. Archaeological and genetic evidence support human presence by 2000 years Before Common Era (BCE). Megafaunal decline was at first slow; it hastened at ∼700 Common Era (CE) and peaked between 750 and 850 CE, just before a dramatic vegetation transformation in the northwest that resulted in the replacement of C3 woodland habitat with C4 grasslands, during a period of heightened monsoonal activity. Cut and chop marks on subfossil lemur bones reveal a shift in primary hunting targets from larger, now-extinct species prior to ∼900 CE, to smaller, still-extant species afterwards. By 1050 CE, megafaunal populations had essentially collapsed. Neither the rapid megafaunal decline beginning ∼700 CE, nor the dramatic vegetation transformation in the northwest beginning ∼890 CE, was influenced by aridification. However, both roughly coincide with a major transition in human subsistence on the island from hunting/foraging to herding/farming. We offer a new hypothesis, which we call the "Subsistence Shift Hypothesis," to explain megafaunal decline and extinction in Madagascar. This hypothesis acknowledges the importance of wild-animal hunting by early hunter/foragers, but more critically highlights negative impacts of the shift from hunting/foraging to herding/farming, settlement by new immigrant groups, and the concomitant expansion of the island's human population. The interval between 700 and 900 CE, when the pace of megafaunal decline quickened and peaked, coincided with this economic transition. While early megafaunal decline through hunting may have helped to trigger the transition, there is strong evidence that the economic shift itself hastened the crash of megafaunal populations.

Isotopic evidence for oligotrophication of terrestrial ecosystems.

Human societies depend on an Earth system that operates within a constrained range of nutrient availability, yet the recent trajectory of terrestrial nitrogen (N) availability is uncertain. Examining patterns of foliar N concentrations and isotope ratios (δ15N) from more than 43,000 samples acquired over 37 years, here we show that foliar N concentration declined by 9% and foliar δ15N declined by 0.6-1.6‰. Examining patterns across different climate spaces, foliar δ15N declined across the entire range of mean annual temperature and mean annual precipitation tested. These results suggest declines in N supply relative to plant demand at the global scale. In all, there are now multiple lines of evidence of declining N availability in many unfertilized terrestrial ecosystems, including declines in δ15N of tree rings and leaves from herbarium samples over the past 75-150 years. These patterns are consistent with the proposed consequences of elevated atmospheric carbon dioxide and longer growing seasons. These declines will limit future terrestrial carbon uptake and increase nutritional stress for herbivores.

Soil analysis in discussions of agricultural feasibility for ancient civilizations: A critical review and reanalysis of the data and debate from Chaco Canyon, New Mexico.

Questions about how archaeological populations obtained basic food supplies are often difficult to answer. The application of specialist techniques from non-archaeological fields typically expands our knowledge base, but can be detrimental to cultural interpretations if employed incorrectly, resulting in problematic datasets and erroneous conclusions not easily caught by the recipient archaeological community. One area where this problem has failed to find resolution is Chaco Canyon, New Mexico, the center of one of the New World's most vibrant ancient civilizations. Discussions of agricultural feasibility and its impact on local population levels at Chaco Canyon have been heavily influenced by studies of soil salinity. A number of researchers have argued that salinized soils severely limited local agricultural production, instead suggesting food was imported from distant sources, specifically the Chuska Mountains. A careful reassessment of existing salinity data as measured by electrical conductivity reveals critical errors in data conversion and presentation that have misrepresented the character of the area's soil and its potential impact on crops. We combine all available electrical conductivity data, including our own, and apply multiple established conversion methods in order to estimate soil salinity values and evaluate their relationship to agricultural productivity potential. Our results show that Chacoan soils display the same salinity ranges and spatial variability as soils in other documented, productive fields in semi-arid areas. Additionally, the proposed large-scale importation of food from the Chuska Mountains region has serious social implications that have not been thoroughly explored. We consider these factors and conclude that the high cost and extreme inflexibility of such a system, in combination with material evidence for local agriculture within Chaco Canyon, make this scenario highly unlikely. Both the soil salinity and archaeological data suggest that there is no justification for precluding the practice of local agriculture within Chaco Canyon.

Organic and Inorganic Pollutant Concentrations Suggest Anthropogenic Contamination of Soils Along the Manali-Leh Highway, Northwestern Himalaya, India.

Most studies on roadside soil pollution have been performed in areas where petrol is the main fuel. Very little work has been conducted in regions where diesel predominates. We collected soil samples from four sites that span a precipitation gradient along the Manali-Leh Highway in northwestern Himalaya, India. This road traverses rough terrain and most of the vehicles that travel along it are diesel-driven. At each site, we collected samples at incremental distances from the highway (0, 2, 5, 10, 20, and 150 m), and at each distance we collected samples from three depths (3, 9, and 15 cm). We assessed the concentrations of 10 heavy metals (Al, Fe, Cr, Cu, Pb, Ni, Co, Zn, V, and Ba), total sulphur, and total organic carbon (TOC) at each distance, and we measured the concentration of 16 polycyclic aromatic hydrocarbons (PAHs) at 2 m from the highway. Overall, we found that metal concentrations are low and there is no relationship between concentrations and distance from the highway, or depth within the soil profile. Sulphur concentrations, on the other hand, are high in roadside soils and there is a negative relationship between concentration and distance from the highway. PAH concentrations are low, but the proportion of different ringed species suggests that their source is anthropogenic. Correlations between TOC and the various pollutants further suggest that diesel vehicles and potentially biomass combustion are starting to affect the roadside environment in remote northwestern India. We suggest that pollutant concentrations be regularly monitored.

Strontium isotopes (87 Sr/86 Sr) in terrestrial ecological and palaeoecological research: empirical efforts and recent advances in continental-scale models.

Strontium (Sr) isotope analysis can provide detailed biogeographical and ecological information about modern and ancient organisms. Because Sr isotope ratios (87 Sr/86 Sr) in biologically relevant materials such as water, soil, vegetation, and animal tissues predominantly reflect local geology, they can be used to distinguish geologically distinct regions as well as identify highly mobile individuals or populations. While the application of Sr isotope analysis to biological research has been steadily increasing, high analytical costs have prohibited more widespread use. Additionally, accessibility of this geochemical tool has been hampered due to limited understanding of (i) the degree to which biologically relevant materials differ in their spatial averaging of 87 Sr/86 Sr ratios, and (ii) how these differences may be affected by lithologic complexity. A recently developed continental-scale model that accounts for variability in bedrock weathering rates and predicts Sr isotope ratios of surface water could help resolve these questions. In addition, if this 'local water' model can accurately predict 87 Sr/86 Sr ratios for other biologically relevant materials, there would be reduced need for researchers to assess regional Sr isotope patterns empirically. Here, we compile 87 Sr/86 Sr data for surface water, soil, vegetation, and mammalian and fish skeletal tissues from the literature and compare the accuracy with which the local water model predicts Sr isotope data among these five materials across the contiguous USA. We find that measured Sr isotope ratios for all five materials are generally close to those predicted by the local water model, although not with uniform accuracy. Mammal skeletal tissues are most accurately predicted, particularly in regions with low variability in 87 Sr/86 Sr predicted by the local water model. Increasing regional geologic heterogeneity increases both the offset and variance between modelled and empirical Sr isotope ratios, but its effects are broadly similar across materials. The local water model thus provides a readily available source of background data for predicting 87 Sr/86 Sr for biologically relevant materials in places where empirical data are lacking. The availability of increasingly high-quality modelled Sr data will dramatically expand the accessibility of this geochemical tool to ecological applications.

Variation in carbon isotope values among chimpanzee foods at Ngogo, Kibale National Park and Bwindi Impenetrable National Park, Uganda.

Stable isotope values in primate tissues can be used to reconstruct diet in the absence of direct observation. However, in order to make dietary inferences, one must first establish isotopic variability for potential food sources. In this study we examine stable carbon isotope (δ(13) C) values for chimpanzee (Pan troglodytes) food resources from two Ugandan forests: Ngogo (Kibale National Park), and Bwindi Impenetrable National Park. Mean δ(13) C values for plant samples are equivalent at both sites. Plant δ(13) C values are best explained by a multivariate linear model including plant part (leaves, pith, flowers, and fruit), vertical position within the canopy (canopy vs. ground), and taxon (R(2) = 0.6992). At both sites, leaves had the lowest δ(13) C values followed by pith and fruit. Canopy resources have comparable δ(13) C values at the two sites but ground resources have lower δ(13) C values at Ngogo than Bwindi (-30.7 vs. -28.6‰). Consequently, isotopic differences between ground and canopy resources (4.2 vs. 2.2‰), and among plant parts are more pronounced at Ngogo. These results demonstrate that underlying environmental differences between sites can produce variable δ(13) C signatures among primate food resources. In the absence of observation data or isotope values for local vegetation, caution must be taken when interpreting isotopic differences among geographically or temporally separated populations or species. Am. J. Primatol. 78:1031-1040, 2016. © 2016 Wiley Periodicals, Inc.

What did Hadropithecus eat, and why should paleoanthropologists care?

Over 40 years ago, Clifford Jolly noted different ways in which Hadropithecus stenognathus converged in its craniodental anatomy with basal hominins and with geladas. The Malagasy subfossil lemur Hadropithecus departs from its sister taxon, Archaeolemur, in that it displays comparatively large molars, reduced incisors and canines, a shortened rostrum, and thickened mandibular corpus. Its molars, however, look nothing like those of basal hominins; rather, they much more closely resemble molars of grazers such as Theropithecus. A number of tools have been used to interpret these traits, including dental microwear and texture analysis, molar internal and external morphology, and finite element analysis of crania. These tools, however, have failed to provide support for a simple dietary interpretation; whereas there is some consistency in the inferences they support, dietary inferences (e.g., that it was graminivorous, or that it specialized on hard objects) have been downright contradictory. Cranial shape may correlate poorly with diet. But a fundamental question remains unresolved: why do the various cranial and dental convergences exemplified by Hadropithecus, basal hominins, and Theropithecus exist? In this paper we review prior hypotheses regarding the diet of Hadropithecus. We then use stable carbon and nitrogen isotope data to elucidate this species' diet, summarizing earlier stable isotope analyses and presenting new data for lemurs from the central highlands of Madagascar, where Hadropithecus exhibits an isotopic signature strikingly different from that seen in other parts of the island. We offer a dietary explanation for these differences. Hadropithecus likely specialized neither on grasses nor hard objects; its staples were probably the succulent leaves of CAM plants. Nevertheless, aspects of prior hypotheses regarding the ecological significance of its morphology can be supported. Am. J. Primatol. 78:1098-1112, 2016. © 2015 Wiley Periodicals, Inc.

Advances in primate stable isotope ecology-Achievements and future prospects.

Stable isotope biogeochemistry has been used to investigate foraging ecology in non-human primates for nearly 30 years. Whereas early studies focused on diet, more recently, isotopic analysis has been used to address a diversity of ecological questions ranging from niche partitioning to nutritional status to variability in life history traits. With this increasing array of applications, stable isotope analysis stands to make major contributions to our understanding of primate behavior and biology. Most notably, isotopic data provide novel insights into primate feeding behaviors that may not otherwise be detectable. This special issue brings together some of the recent advances in this relatively new field. In this introduction to the special issue, we review the state of isotopic applications in primatology and its origins and describe some developing methodological issues, including techniques for analyzing different tissue types, statistical approaches, and isotopic baselines. We then discuss the future directions we envision for the field of primate isotope ecology. Am. J. Primatol. 78:995-1003, 2016. © 2015 Wiley Periodicals, Inc.

Comparative and population mitogenomic analyses of Madagascar's extinct, giant 'subfossil' lemurs.

Humans first arrived on Madagascar only a few thousand years ago. Subsequent habitat destruction and hunting activities have had significant impacts on the island's biodiversity, including the extinction of megafauna. For example, we know of 17 recently extinct 'subfossil' lemur species, all of which were substantially larger (body mass ∼11-160 kg) than any living population of the ∼100 extant lemur species (largest body mass ∼6.8 kg). We used ancient DNA and genomic methods to study subfossil lemur extinction biology and update our understanding of extant lemur conservation risk factors by i) reconstructing a comprehensive phylogeny of extinct and extant lemurs, and ii) testing whether low genetic diversity is associated with body size and extinction risk. We recovered complete or near-complete mitochondrial genomes from five subfossil lemur taxa, and generated sequence data from population samples of two extinct and eight extant lemur species. Phylogenetic comparisons resolved prior taxonomic uncertainties and confirmed that the extinct subfossil species did not comprise a single clade. Genetic diversity estimates for the two sampled extinct species were relatively low, suggesting small historical population sizes. Low genetic diversity and small population sizes are both risk factors that would have rendered giant lemurs especially susceptible to extinction. Surprisingly, among the extant lemurs, we did not observe a relationship between body size and genetic diversity. The decoupling of these variables suggests that risk factors other than body size may have as much or more meaning for establishing future lemur conservation priorities.

Quantifying inter-laboratory variability in stable isotope analysis of ancient skeletal remains.

Over the past forty years, stable isotope analysis of bone (and tooth) collagen and hydroxyapatite has become a mainstay of archaeological and paleoanthropological reconstructions of paleodiet and paleoenvironment. Despite this method's frequent use across anthropological subdisciplines (and beyond), the present work represents the first attempt at gauging the effects of inter-laboratory variability engendered by differences in a) sample preparation, and b) analysis (instrumentation, working standards, and data calibration). Replicate analyses of a 14C-dated ancient human bone by twenty-one archaeological and paleoecological stable isotope laboratories revealed significant inter-laboratory isotopic variation for both collagen and carbonate. For bone collagen, we found a sizeable range of 1.8‰ for δ13Ccol and 1.9‰ for δ15Ncol among laboratories, but an interpretatively insignificant average pairwise difference of 0.2‰ and 0.4‰ for δ13Ccol and δ15Ncol respectively. For bone hydroxyapatite the observed range increased to a troublingly large 3.5‰ for δ13Cap and 6.7‰ for δ18Oap, with average pairwise differences of 0.6‰ for δ13Cap and a disquieting 2.0‰ for δ18Oap. In order to assess the effects of preparation versus analysis on isotopic variability among laboratories, a subset of the samples prepared by the participating laboratories were analyzed a second time on the same instrument. Based on this duplicate analysis, it was determined that roughly half of the isotopic variability among laboratories could be attributed to differences in sample preparation, with the other half resulting from differences in analysis (instrumentation, working standards, and data calibration). These findings have serious implications for choices made in the preparation and extraction of target biomolecules, the comparison of results obtained from different laboratories, and the interpretation of small differences in bone collagen and hydroxyapatite isotope values. To address the issues arising from inter-laboratory comparisons, we devise a novel measure we term the Minimum Meaningful Difference (MMD), and demonstrate its application.

Stable isotopes complement focal individual observations and confirm dietary variability in reddish-gray mouse lemurs (Microcebus griseorufus) from southwestern Madagascar.

We examine the ecology of reddish-gray mouse lemurs from three habitats at Beza Mahafaly Special Reserve using focal follows and stable carbon and nitrogen isotope data. Focal observations indicate dietary differences among habitats as well as sexes and seasons. Both sexes consume more arthropods during the rainy season but overall, females consume more sugar-rich exudates and fruit than males, and individuals from riparian forest consume fewer arthropods and more fruit than those in xeric or dry forest. We ask whether these observations are isotopically detectable. Isotope data support differences between seasons and sexes. Nitrogen isotope values are higher during the rainy season when lemurs consume more arthropods, and higher in males than females, particularly during the dry season. However, differences among populations inferred from focal observations are not fully supported. Lemurs from riparian forest have lower isotope values than those in xeric scrub, but isotope data suggest that lemurs from the dry forest eat the least animal matter and that focal observations overestimated dry forest arthropod consumption. Overall, our results suggest that observational and isotopic data are complementary. Isotope data can be obtained from a larger number of individuals and can quantify ingestion of animal matter, but they apparently cannot quantify the relative consumption of different sugar-rich foods. Combined focal and isotope data provide valuable insight into the dietary constraints of reddish-grey mouse lemurs, with implications for their vulnerability to future habitat change.

Technical Note: Calcium and carbon stable isotope ratios as paleodietary indicators.

Calcium stable isotope ratios are hypothesized to vary as a function of trophic level. This premise raises the possibility of using calcium stable isotope ratios to study the dietary behaviors of fossil taxa and to test competing hypotheses on the adaptive origins of euprimates. To explore this concept, we measured the stable isotope composition of contemporary mammals in northern Borneo and northwestern Costa Rica, two communities with functional or phylogenetic relevance to primate origins. We found that bone collagen δ(13) C and δ(15) N values could differentiate trophic levels in each assemblage, a result that justifies the use of these systems to test the predicted inverse relationship between bioapatite δ(13) C and δ(44) Ca values. As expected, taxonomic carnivores (felids) showed a combination of high δ(13) C and low δ(44) Ca values; however, the δ(44) Ca values of other faunivores were indistinguishable from those of primary consumers. We suggest that the trophic insensitivity of most bioapatite δ(44) Ca values is attributable to the negligible calcium content of arthropod prey. Although the present results are inconclusive, the tandem analysis of δ(44) Ca and δ(13) C values in fossils continues to hold promise for informing paleodietary studies and we highlight this potential by drawing attention to the stable isotope composition of the Early Eocene primate Cantius.

Edge effects on foliar stable isotope values in a Madagascan tropical dry forest.

Edge effects represent an inevitable and important consequence of habitat loss and fragmentation. These effects include changes in microclimate, solar radiation, or temperature. Such abiotic effects can, in turn, impact biotic factors. They can have a substantial impact on species, communities, and ecosystems. Here we examine clinal variations in stable carbon and nitrogen isotope values for trees along an edge-interior gradient in the dry deciduous forest at Ankarafantsika National Park. We predicted that soil respiration and differences in solar irradiance would result in stratified δ¹³C values where leaves collected close to the forest floor would have lower δ¹³C values than those growing higher up in the canopy. We also anticipated that plants growing at the savannah-forest boundary would have higher δ¹³C and δ¹5N values than plants growing in the forest interior. As expected, we detected a small but significant canopy effect. Leaves growing below 2 m from the forest floor exhibit δ¹³C values that are, on average, 1.1‰ lower than those growing above this threshold. We did not, however, find any relationship between foliar δ¹³C and distance from the edge. Unpredictably, we detected a striking positive relationship between foliar δ¹5N values and increasing distance into the forest interior. Variability in physiology among species, anthropogenic influence, organic input, and rooting depth cannot adequately explain this trend. Instead, this unexpected relationship most likely reflects decreasing nutrient or water availability, or a shift in N-sources with increasing distance from the savannah. Unlike most forest communities, the trees at Ampijoroa are growing in nutrient-limited sands. In addition to being nutrient poor, these well-drained soils likely decrease the amount of soil water available to forest vegetation. Continued research on plant responses to edge effects will improve our understanding of the conservation biology of forest ecosystems in Madagascar.

Extinction and ecological retreat in a community of primates.

The lemurs of Madagascar represent a prodigious adaptive radiation. At least 17 species ranging from 11 to 160 kg have become extinct during the past 2000 years. The effect of this loss on contemporary lemurs is unknown. The concept of competitive release favours the expansion of living species into vacant niches. Alternatively, factors that triggered the extinction of some species could have also reduced community-wide niche breadth. Here, we use radiocarbon and stable isotope data to examine temporal shifts in the niches of extant lemur species following the extinction of eight large-bodied species. We focus on southwestern Madagascar and report profound isotopic shifts, both from the time when now-extinct lemurs abounded and from the time immediately following their decline to the present. Unexpectedly, the past environments exploited by lemurs were drier than the protected (albeit often degraded) riparian habitats assumed to be ideal for lemurs today. Neither competitive release nor niche contraction can explain these observed trends. We develop an alternative hypothesis: ecological retreat, which suggests that factors surrounding extinction may force surviving species into marginal or previously unfilled niches.

Bornean orangutans on the brink of protein bankruptcy.

Protein is a limiting resource that is essential to the growth, maintenance and reproduction of tropical frugivores, yet few studies have examined how wild animals maintain protein balance. During chronic periods of fruit scarcity, Bornean orangutans (Pongo pygmaeus) often catabolize their own fat reserves despite unusually low metabolic requirements. Such energy deficits suggest a marginal existence, and raise the possibility that orangutans also endure periods of negative protein balance. To test this hypothesis, we conducted the first study of protein cycling in a wild primate. Our five year analysis of urinary metabolites revealed evidence of protein recycling when fruit was scarce. During these periods, orangutans consumed more leaves and bark, proteinaceous but tough foods that yielded a mean daily intake of 1.4 g protein kg(-1) metabolic mass. Such an amount is inadequate for humans and one-tenth the intake of mountain gorillas, but sufficient to avert, perhaps narrowly, a severe protein deficit. Our findings highlight the functional and adaptive value of traits that maximize protein assimilation during periods of ecological exigency.