Genomic Underpinnings of Population Persistence in Isle Royale Moose.

Island ecosystems provide natural laboratories to assess the impacts of isolation on population persistence. However, most studies of persistence have focused on a single species, without comparisons to other organisms they interact with in the ecosystem. The case study of moose and gray wolves on Isle Royale allows for a direct contrast of genetic variation in isolated populations that have experienced dramatically differing population trajectories over the past decade. Whereas the Isle Royale wolf population recently declined nearly to extinction due to severe inbreeding depression, the moose population has thrived and continues to persist, despite having low genetic diversity and being isolated for ∼120 years. Here, we examine the patterns of genomic variation underlying the continued persistence of the Isle Royale moose population. We document high levels of inbreeding in the population, roughly as high as the wolf population at the time of its decline. However, inbreeding in the moose population manifests in the form of intermediate-length runs of homozygosity suggestive of historical inbreeding and purging, contrasting with the long runs of homozygosity observed in the smaller wolf population. Using simulations, we confirm that substantial purging has likely occurred in the moose population. However, we also document notable increases in genetic load, which could eventually threaten population viability over the long term. Overall, our results demonstrate a complex relationship between inbreeding, genetic diversity, and population viability that highlights the use of genomic datasets and computational simulation tools for understanding the factors enabling persistence in isolated populations.

Links between three chronic and age-related diseases, osteoarthritis, periodontitis, and osteoporosis, in a wild mammal (moose) population.

OBJECTIVE: Osteoarthritis, periodontitis and osteoporosis are chronic, age-related diseases which adversely impact millions of people worldwide. Because these diseases pose a major global public health challenge, there is an urgent need to better understand how these diseases are interrelated. Our objective was to document the age and sex-specific prevalence of each disease and assess interrelationships among the three diseases in a wild mammal (moose, Alces alces) population. METHODS: We examined the bones of moose dying from natural causes and recorded the severity of osteoarthritis (typically observed on the hip and lowest vertebrae), osteoporosis (osteoporotic lesions observed on the skull) and periodontitis (observed on maxilla and mandibles). RESULTS: Periodontitis was associated with a greater prevalence of both severe osteoarthritis and osteoporotic lesions in moose. We found no evidence to suggest that moose with osteoporotic lesions were more or less likely to exhibit signs of osteoarthritis or severe osteoarthritis. The prevalence of osteoarthritis, periodontitis and osteoporotic lesions was greater among males than for females. CONCLUSIONS: Our results were consistent with the hypothesis that bacterial pathogens causing periodontitis are a risk factor for osteoarthritis and osteoporosis. They are also consistent with the hypothesis that the inverse association between osteoarthritis and osteoporosis sometimes observed in humans may be influenced by shared risk factors, such as obesity, smoking or alcohol consumption, which are absent in moose. Together these results provide insights about three diseases which are expected to become more prevalent in the future and that cause substantial socio-economic burdens.

Demographic history shapes North American gray wolf genomic diversity and informs species' conservation.

Effective population size estimates are critical information needed for evolutionary predictions and conservation decisions. This is particularly true for species with social factors that restrict access to breeding or experience repeated fluctuations in population size across generations. We investigated the genomic estimates of effective population size along with diversity, subdivision, and inbreeding from 162,109 minimally filtered and 81,595 statistically neutral and unlinked SNPs genotyped in 437 grey wolf samples from North America collected between 1986 and 2021. We found genetic structure across North America, represented by three distinct demographic histories of western, central, and eastern regions of the continent. Further, grey wolves in the northern Rocky Mountains have lower genomic diversity than wolves of the western Great Lakes and have declined over time. Effective population size estimates revealed the historical signatures of continental efforts of predator extermination, despite a quarter century of recovery efforts. We are the first to provide molecular estimates of effective population size across distinct grey wolf populations in North America, which ranged between Ne ~ 275 and 3050 since early 1980s. We provide data that inform managers regarding the status and importance of effective population size estimates for grey wolf conservation, which are on average 5.2-9.3% of census estimates for this species. We show that while grey wolves fall above minimum effective population sizes needed to avoid extinction due to inbreeding depression in the short term, they are below sizes predicted to be necessary to avoid long-term risk of extinction.

The difficulty of detecting inbreeding depression and its effect on conservation decisions.

Statistical inferences about inbreeding depression are often derived from analyses with low power and a high risk of failing to detect inbreeding depression. That risk is widely appreciated by scientists familiar with the relevant statistical and genetical theory, but may be overlooked and underappreciated by decision-makers. Consequently, there is value in demonstrating this risk using a real example. We use data from the wolf population on Isle Royale to demonstrate the difficulty of making reliable statistical inferences about inbreeding depression. This wolf population is known-by other methods-to have gone effectively extinct due to deleterious genetic processes associated with inbreeding. Beyond that demonstration, we use two case-studies-wolves on Isle Royale and vaquita (porpoises) from the Gulf of California, Mexico-to show how statistical inferences about inbreeding depression can affect conservation decisions. According to most decision theory, decisions depend importantly on: 1) probabilities that certain states exist (e.g. inbreeding depression is present) and 2) the utility assigned to various outcomes (e.g. the value of acting to mitigate inbreeding when it is present). The probabilities are provided by statistical inference; whereas utilities are almost entirely determined by normative values and judgements. Our analysis suggests that decisions to mitigate inbreeding depression are often driven more by utilities (normative values) than probabilities (statistical inferences). As such, advocates for mitigating inbreeding depression will benefit from better communicating to decision-makers the value of populations persisting and the extent to which decisions should depend on normative values.

The role of governance in rewilding the United States to stem the biodiversity crisis.

A critical but underattended feature of the biodiversity crisis is the contraction of geographic range experienced by most studied terrestrial vertebrates. In the United States, the primary policy tool for mitigating the biodiversity crisis is a federal law, the Endangered Species Act (ESA). For the past two decades, the federal agencies that administer the ESA have interpreted the act in a manner that precludes treating this geographic element of the crisis. Therefore, the burden of mitigating the biodiversity crisis largely falls on wildlife agencies within state government, which are obligated to operate on behalf of the interests of their constituents. We present survey research indicating that most constituents expect state agencies to prioritize species restoration over other activities, including hunting. This prioritization holds even among self-identified hunters, which is significant because state agencies often take the provisioning of hunting opportunity as their top priority. By prioritizing rewilding efforts that restore native species throughout portions of their historic range, state agencies could unify hunting and nonhunting constituents while simultaneously stemming the biodiversity crisis.

Territoriality drives preemptive habitat selection in recovering wolves: Implications for carnivore conservation.

According to the ideal-free distribution (IFD), individuals within a population are free to select habitats that maximize their chances of success. Assuming knowledge of habitat quality, the IFD predicts that average fitness will be approximately equal among individuals and between habitats, while density varies, implying that habitat selection will be density dependent. Populations are often assumed to follow an IFD, although this assumption is rarely tested with empirical data, and may be incorrect when territoriality indicates habitat selection tactics that deviate from the IFD (e.g. ideal-despotic distribution or ideal-preemptive distribution). When territoriality influences habitat selection, species' density will not directly reflect components of fitness such as reproductive success or survival. In such cases, assuming an IFD can lead to false conclusions about habitat quality. We tested theoretical models of density-dependent habitat selection on a species known to exhibit territorial behaviour in order to determine whether commonly applied habitat models are appropriate under these circumstances. We combined long-term radiotelemetry and census data from grey wolves Canis lupus in the Upper Peninsula of Michigan, USA to relate spatiotemporal variability in wolf density to underlying classifications of habitat within a hierarchical state-space modelling framework. We then iteratively applied isodar analysis to evaluate which distribution of habitat selection best described this recolonizing wolf population. The wolf population in our study expanded by >1,000% during our study (~50 to >600 individuals), and density-dependent habitat selection was most consistent with the ideal-preemptive distribution, as opposed to the ideal-free or ideal-despotic alternatives. Population density of terrestrial carnivores may not be positively correlated with the fitness value of their habitats, and density-dependent habitat selection patterns may help to explain complex predator-prey dynamics and cascading indirect effects. Source-sink population dynamics appear likely when species exhibit rapid growth and occupy interspersed habitats of contrasting quality. These conditions are likely and have implications for large carnivores in many systems, such as areas in North America and Europe where large predator species are currently recolonizing their former ranges.

Negative frequency-dependent foraging behaviour in a generalist herbivore (Alces alces) and its stabilizing influence on food web dynamics.

Resource selection is widely appreciated to be context-dependent and shaped by both biological and abiotic factors. However, few studies have empirically assessed the extent to which selective foraging behaviour is dynamic and varies in response to environmental conditions for free-ranging animal populations. Here, we assessed the extent that forage selection fluctuated in response to different environmental conditions for a free-ranging herbivore, moose (Alces alces), in Isle Royale National Park, over a 10-year period. More precisely, we assessed how moose selection for coniferous versus deciduous forage in winter varied between geographic regions and in relation to (a) the relative frequency of forage types in the environment (e.g. frequency-dependent foraging behaviour), (b) moose abundance, (c) predation rate (by grey wolves) and (d) snow depth. These factors are potentially important for their influence on the energetics of foraging. We also built a series of food-chain models to assess the influence of dynamic foraging strategies on the stability of food webs. Our analysis indicates that moose exhibited negative frequency dependence, by selectively exploiting rare resources. Frequency-dependent foraging was further mediated by density-dependent processes, which are likely to be predation, moose abundance or some combination of both. In particular, frequency dependence was weaker in years when predation risk was high (i.e. when the ratio of moose to wolves was relatively low). Selection for conifers was also slightly weaker during deep snow years. The food-chain analysis indicates that the type of frequency-dependent foraging strategy exhibited by herbivores had important consequences for the stability of ecological communities. In particular, the dynamic foraging strategy that we observed in the empirical analysis (i.e. negative frequency dependence being mediated by density-dependent processes) was associated with more stable food web dynamics compared to fixed foraging strategies. The results of this study indicated that forage selection is a complex ecological process, varying in response to both biological (predation and moose density) and abiotic factors (snow depth) and over relatively small spatial scales (between regions). This study also provides a useful framework for assessing the influence of other aspects of foraging behaviour on the stability of food web dynamics.

Climate warming is associated with smaller body size and shorter lifespans in moose near their southern range limit.

Despite the importance of body size for individual fitness, population dynamics and community dynamics, the influence of climate change on growth and body size is inadequately understood, particularly for long-lived vertebrates. Although temporal trends in body size have been documented, it remains unclear whether these changes represent the adverse impact of climate change (environmental stress constraining phenotypes) or its mitigation (via phenotypic plasticity or evolution). Concerns have also been raised about whether climate change is indeed the causal agent of these phenotypic shifts, given the length of time-series analysed and that studies often do not evaluate - and thereby sufficiently rule out - other potential causes. Here, we evaluate evidence for climate-related changes in adult body size (indexed by skull size) over a 4-decade period for a population of moose (Alces alces) near the southern limit of their range whilst also considering changes in density, predation, and human activities. In particular, we document: (i) a trend of increasing winter temperatures and concurrent decline in skull size (decline of 19% for males and 13% for females) and (ii) evidence of a negative relationship between skull size and winter temperatures during the first year of life. These patterns could be plausibly interpreted as an adaptive phenotypic response to climate warming given that latitudinal/temperature clines are often accepted as evidence of adaptation to local climate. However, we also observed: (iii) that moose with smaller skulls had shorter lifespans, (iv) a reduction in lifespan over the 4-decade study period, and (v) a negative relationship between lifespan and winter temperatures during the first year of life. Those observations indicate that this phenotypic change is not an adaptive response to climate change. However, this decline in lifespan was not accompanied by an obvious change in population dynamics, suggesting that climate change may affect population dynamics and life-histories differently.

Genomic Variation of Inbreeding and Ancestry in the Remaining Two Isle Royale Wolves.

Inbreeding, relatedness, and ancestry have traditionally been estimated with pedigree information, however, molecular genomic data can provide more detailed examination of these properties. For example, pedigree information provides estimation of the expected value of these measures but molecular genomic data can estimate the realized values of these measures in individuals. Here, we generate the theoretical distribution of inbreeding, relatedness, and ancestry for the individuals in the pedigree of the Isle Royale wolves, the first examination of such variation in a wild population with a known pedigree. We use the 38 autosomes of the dog genome and their estimated map lengths in our genomic analysis. Although it is known that the remaining wolves are highly inbred, closely related, and descend from only 3 ancestors, our analyses suggest that there is significant variation in the realized inbreeding and relatedness around pedigree expectations. For example, the expected inbreeding in a hypothetical offspring from the 2 remaining wolves is 0.438 but the realized 95% genomic confidence interval is from 0.311 to 0.565. For individual chromosomes, a substantial proportion of the whole chromosomes are completely identical by descent. This examination provides a background to use when analyzing molecular genomic data for individual levels of inbreeding, relatedness, and ancestry. The level of variation in these measures is a function of the time to the common ancestor(s), the number of chromosomes, and the rate of recombination. In the Isle Royale wolf population, the few generations to a common ancestor results in the high variance in genomic inbreeding.

Interannual variability: a crucial component of space use at the territory level.

Interannual variability in space use and how that variation is influenced by density-dependent and density-independent factors are important processes in population ecology. Nevertheless, interannual variability has been neglected by the majority of space use studies. We assessed that variation for wolves living in 15 different packs within Yellowstone National Park during a 13-year period (1996-2008). We estimated utilization distributions to quantify the intensity of space use within each pack's territory each year in summer and winter. Then, we used the volume of intersection index (VI) to quantify the extent to which space use varied from year to year. This index accounts for both the area of overlap and differences in the intensity of use throughout a territory and ranges between 0 and 1. The mean VI index was 0.49, and varied considerably, with approximately 20% of observations (n = 230) being <0.3 or >0.7. In summer, 42% of the variation was attributable to differences between packs. These differences can be attributable to learned behaviors and had never been thought to have such an influence on space use. In winter, 34% of the variation in overlap between years was attributable to interannual differences in precipitation and pack size. This result reveals the strong influence of climate on predator space use and underlies the importance of understanding how climatic factors are going to affect predator populations in the occurrence of climate change. We did not find any significant association between overlap and variables representing density-dependent processes (elk and wolf densities) or intraspecific competition (ratio of wolves to elk). This last result poses a challenge to the classic view of predator-prey systems. On a small spatial scale, predator space use may be driven by factors other than prey distribution.

Evaluating whether nature's intrinsic value is an axiom of or anathema to conservation.

That at least some aspects of nature possess intrinsic value is considered by some an axiom of conservation. Others consider nature's intrinsic value superfluous or anathema. This range of views among mainstream conservation professionals potentially threatens the foundation of conservation. One challenge in resolving this disparity is that disparaging portrayals of nature's intrinsic value appear rooted in misconceptions and unfounded presumptions about what it means to acknowledge nature's intrinsic value. That acknowledgment has been characterized as vacuous, misanthropic, of little practical consequence to conservation, adequately accommodated by economic valuation, and not widely accepted in society. We reviewed the philosophical basis for nature's intrinsic value and the implications for acknowledging that value. Our analysis is rooted to the notion that when something possesses intrinsic value it deserves to be treated with respect for what it is, with concern for its welfare or in a just manner. From this basis, one can only conclude that nature's intrinsic value is not a vacuous concept or adequately accommodated by economic valuation. Acknowledging nature's intrinsic value is not misanthropic because concern for nature's welfare (aside from its influence on human welfare) does not in any way preclude also being concerned for human welfare. The practical import of acknowledging nature's intrinsic value rises from recognizing all the objects of conservation concern (e.g., many endangered species) that offer little benefit to human welfare. Sociological and cultural evidence indicates the belief that at least some elements of nature possess intrinsic value is widespread in society. Our reasoning suggests the appropriateness of rejecting the assertion that nature's intrinsic value is anathema to conservation and accepting its role as an axiom.

The influence of winter severity, predation and senescence on moose habitat use.

Habitat use is widely known to be influenced by abiotic and biotic factors, such as climate, population density, foraging opportunity and predation risk. The influence of the life-history state of an individual organism on habitat use is less well understood, especially for terrestrial mammals. There is good reason to expect that life-history state would affect habitat use. For example, organisms exhibiting poor condition associated with senescence have an increased vulnerability to predation and that vulnerability is known to alter habitat use strategies. We assessed the influence of life-history stage on habitat use for 732 moose (Alces alces) killed by wolves (Canis lupus) over a 50-year period in Isle Royale National Park, an island ecosystem in Lake Superior, USA. We developed regression models to assess how location of death was associated with a moose's life-history stage (prime-aged or senescent), presence or absence of senescent-associated pathology (osteoarthritis and jaw necrosis), and annual variation in winter severity, moose density and ratio of moose to wolves, which is an index of predation risk. Compared to senescent moose, prime-aged moose tend to make greater use of habitat farther from the shoreline of Isle Royale. That result is ecologically relevant because shoreline habitat on Isle Royale tends to provide better foraging opportunities for moose but is also associated with increased predation risk. During severe winters prime-aged moose tend to make greater use of habitat that is closer to shore in relation to senescent-aged moose. Furthermore, moose of both age classes were more likely to die in riskier, shoreline habitat during years when predation risk was lower in the preceding year. Our results highlight a complicated connection between life history, age-structured population dynamics and habitat-related behaviour. Our analysis also illustrates why intraspecific competition should not be the presumed mechanism underlying density-dependent habitat use, if predation risk is related to density, as it is expected to be in many systems.

The far-reaching effects of genetic process in a keystone predator species, grey wolves.

Although detrimental genetic processes are known to adversely affect the viability of populations, little is known about how detrimental genetic processes in a keystone species can affect the functioning of ecosystems. Here, we assessed how changes in the genetic characteristics of a keystone predator, grey wolves, affected the ecosystem of Isle Royale National Park over two decades. Changes in the genetic characteristic of the wolf population associated with a genetic rescue event, followed by high levels of inbreeding, led to a rise and then fall in predation rates on moose, the primary prey of wolves and dominant mammalian herbivore in this system. Those changes in predation rate led to large fluctuations in moose abundance, which in turn affected browse rates on balsam fir, the dominant forage for moose during winter and an important boreal forest species. Thus, forest dynamics can be traced back to changes in the genetic characteristics of a predator population.

Seasonal patterns of predation for gray wolves in the multi-prey system of Yellowstone National Park.

1. For large predators living in seasonal environments, patterns of predation are likely to vary among seasons because of related changes in prey vulnerability. Variation in prey vulnerability underlies the influence of predators on prey populations and the response of predators to seasonal variation in rates of biomass acquisition. Despite its importance, seasonal variation in predation is poorly understood. 2. We assessed seasonal variation in prey composition and kill rate for wolves Canis lupus living on the Northern Range (NR) of Yellowstone National Park. Our assessment was based on data collected over 14 winters (1995-2009) and five spring-summers between 2004 and 2009. 3. The species composition of wolf-killed prey and the age and sex composition of wolf-killed elk Cervus elaphus (the primary prey for NR wolves) varied among seasons. 4. One's understanding of predation depends critically on the metric used to quantify kill rate. For example, kill rate was greatest in summer when quantified as the number of ungulates acquired per wolf per day, and least during summer when kill rate was quantified as the biomass acquired per wolf per day. This finding contradicts previous research that suggests that rates of biomass acquisition for large terrestrial carnivores tend not to vary among seasons. 5. Kill rates were not well correlated among seasons. For example, knowing that early-winter kill rate is higher than average (compared with other early winters) provides little basis for anticipating whether kill rates a few months later during late winter will be higher or lower than average (compared with other late winters). This observation indicates how observing, for example, higher-than-average kill rates throughout any particular season is an unreliable basis for inferring that the year-round average kill rate would be higher than average. 6. Our work shows how a large carnivore living in a seasonal environment displays marked seasonal variation in predation because of changes in prey vulnerability. Patterns of wolf predation were influenced by the nutritional condition of adult elk and the availability of smaller prey (i.e. elk calves, deer). We discuss how these patterns affect our overall understanding of predator and prey population dynamics.

Genomic sweep and potential genetic rescue during limiting environmental conditions in an isolated wolf population.

Genetic rescue, in which the introduction of one or more unrelated individuals into an inbred population results in the reduction of detrimental genetic effects and an increase in one or more vital rates, is a potentially important management tool for mitigating adverse effects of inbreeding. We used molecular techniques to document the consequences of a male wolf (Canis lupus) that immigrated, on its own, across Lake Superior ice to the small, inbred wolf population in Isle Royale National Park. The immigrant's fitness so exceeded that of native wolves that within 2.5 generations, he was related to every individual in the population and his ancestry constituted 56 per cent of the population, resulting in a selective sweep of the total genome. In other words, all the male ancestry (50% of the total ancestry) descended from this immigrant, plus 6 per cent owing to the success of some of his inbred offspring. The immigration event occurred in an environment where space was limiting (i.e. packs occupied all available territories) and during a time when environmental conditions had deteriorated (i.e. wolves' prey declined). These conditions probably explain why the immigration event did not obviously improve the population's demography (e.g. increased population numbers or growth rate). Our results show that the beneficial effects of gene flow may be substantial and quickly manifest, short-lived under some circumstances, and how the demographic benefits of genetic rescue might be masked by environmental conditions.

Predicting prey population dynamics from kill rate, predation rate and predator-prey ratios in three wolf-ungulate systems.

1. Predation rate (PR) and kill rate are both fundamental statistics for understanding predation. However, relatively little is known about how these statistics relate to one another and how they relate to prey population dynamics. We assess these relationships across three systems where wolf-prey dynamics have been observed for 41 years (Isle Royale), 19 years (Banff) and 12 years (Yellowstone). 2. To provide context for this empirical assessment, we developed theoretical predictions of the relationship between kill rate and PR under a broad range of predator-prey models including predator-dependent, ratio-dependent and Lotka-Volterra dynamics. 3. The theoretical predictions indicate that kill rate can be related to PR in a variety of diverse ways (e.g. positive, negative, unrelated) that depend on the nature of predator-prey dynamics (e.g. structure of the functional response). These simulations also suggested that the ratio of predator-to-prey is a good predictor of prey growth rate. That result motivated us to assess the empirical relationship between the ratio and prey growth rate for each of the three study sites. 4. The empirical relationships indicate that PR is not well predicted by kill rate, but is better predicted by the ratio of predator-to-prey. Kill rate is also a poor predictor of prey growth rate. However, PR and ratio of predator-to-prey each explained significant portions of variation in prey growth rate for two of the three study sites. 5. Our analyses offer two general insights. First, Isle Royale, Banff and Yellowstone are similar insomuch as they all include wolves preying on large ungulates. However, they also differ in species diversity of predator and prey communities, exploitation by humans and the role of dispersal. Even with the benefit of our analysis, it remains difficult to judge whether to be more impressed by the similarities or differences. This difficulty nicely illustrates a fundamental property of ecological communities. Second, kill rate is the primary statistic for many traditional models of predation. However, our work suggests that kill rate and PR are similarly important for understanding why predation is such a complex process.

Finding Purpose in the Conservation of Biodiversity by the Commingling of Science and Ethics.

Averting the biodiversity crisis requires closing a gap between how humans tend to behave, individually and collectively, and how we ought to behave-"ought to" in the sense of behaviors required to avert the biodiversity crisis. Closing that gap requires synthesizing insight from ethics with insights from social and behavioral sciences. This article contributes to that synthesis, which presents in several provocative hypotheses: (i) Lessening the biodiversity crisis requires promoting pro-conservation behavior among humans. Doing so requires better scientific understanding of how one's sense of purpose in life affects conservation-relevant behaviors. Psychology and virtue-focused ethics indicate that behavior is importantly influenced by one's purpose. However, conservation psychology has neglected inquiries on (a) the influence of one's purpose (both the content and strength of one's purpose) on conservation-related behaviors and (b) how to foster pro-conservation purposes; (ii) lessening the biodiversity crisis requires governance-the regulation of behavior by governments, markets or other organization through various means, including laws, norms, and power-to explicitly take conservation as one of its fundamental purposes and to do so across scales of human behaviors, from local communities to nations and corporations; (iii) lessening the biodiversity crisis requires intervention via governance to nudge human behavior in line with the purpose of conservation without undue infringement on other basic values. Aligning human behavior with conservation is inhibited by the underlying purpose of conservation being underspecified. Adequate specification of conservation's purpose will require additional interdisciplinary research involving insights from ethics, social and behavioral sciences, and conservation biology.

Ecology of arthritis.

Osteoarthritis (OA) is a widespread degenerative disease of skeletal joints and is often associated with senescence in vertebrates. OA commonly results from excessive or abnormal mechanical loading of weight-bearing joints ('wear-and-tear'), arising from heavy long-term use or specific injuries; yet, in the absence of injury, the aetiology of OA remains obscure. We show that poor nutritional conditions experienced by moose (Alces alces) early in life are linked to greater prevalence of OA during senescence as well as reduced life expectancy. Moreover, we also found a negative relationship between kill rate by wolves (Canis lupus) and prevalence of OA, suggesting a potential connection between senescence of prey and the population ecology of predator-prey systems. This association between OA and early malnutrition also provides a basis for explaining the observation in anthropology that OA became more prevalent in native Americans as their diet become poorer - the result of relying more on corn and agriculture and less on hunting and gathering.

Geography and recovery under the U.S. Endangered Species Act.

The U.S. Endangered Species Act (ESA) defines an endangered species as one "at risk of extinction throughout all or a significant portion of its range." The prevailing interpretation of this phrase, which focuses exclusively on the overall viability of listed species without regard to their geographic distribution, has led to development of listing and recovery criteria with fundamental conceptual, legal, and practical shortcomings. The ESA's concept of endangerment is broader than the biological concept of extinction risk in that the "esthetic, ecological, educational, historical, recreational, and scientific" values provided by species are not necessarily furthered by a species mere existence, but rather by a species presence across much of its former range. The concept of "significant portion of range" thus implies an additional geographic component to recovery that may enhance viability, but also offers independent benefits that Congress intended the act to achieve. Although the ESA differs from other major endangered-species protection laws because it acknowledges the distinct contribution of geography to recovery, it resembles the "representation, resiliency, and redundancy" conservation-planning framework commonly referenced in recovery plans. To address representation, listing and recovery standards should consider not only what proportion of its former range a species inhabits, but the types of habitats a species occupies and the ecological role it plays there. Recovery planning for formerly widely distributed species (e.g., the gray wolf [Canis lupus]) exemplifies how the geographic component implicit in the ESA's definition of endangerment should be considered in determining recovery goals through identification of ecologically significant types or niche variation within the extent of listed species, subspecies, or "distinct population segments." By linking listing and recovery standards to niche and ecosystem concepts, the concept of ecologically significant type offers a scientific framework that promotes more coherent dialogue concerning the societal decisions surrounding recovery of endangered species.