Genetic architecture and evolution of color variation in American black bears.

Color variation is a frequent evolutionary substrate for camouflage in small mammals, but the underlying genetics and evolutionary forces that drive color variation in natural populations of large mammals are mostly unexplained. The American black bear, Ursus americanus (U. americanus), exhibits a range of colors including the cinnamon morph, which has a similar color to the brown bear, U. arctos, and is found at high frequency in the American southwest. Reflectance and chemical melanin measurements showed little distinction between U. arctos and cinnamon U. americanus individuals. We used a genome-wide association for hair color as a quantitative trait in 151 U. americanus individuals and identified a single major locus (p < 10-13). Additional genomic and functional studies identified a missense alteration (R153C) in Tyrosinase-related protein 1 (TYRP1) that likely affects binding of the zinc cofactor, impairs protein localization, and results in decreased pigment production. Population genetic analyses and demographic modeling indicated that the R153C variant arose 9.36 kya in a southwestern population where it likely provided a selective advantage, spreading both northwards and eastwards by gene flow. A different TYRP1 allele, R114C, contributes to the characteristic brown color of U. arctos but is not fixed across the range.

An engineering perspective on the development and evolution of implantable cardiac monitors in free-living animals.

The latest technologies associated with implantable physiological monitoring devices can record multiple channels of data (including: heart rates and rhythms, activity, temperature, impedance and posture), and coupled with powerful software applications, have provided novel insights into the physiology of animals in the wild. This perspective details past challenges and lessons learned from the uses and developments of implanted biologgers designed for human clinical application in our research on free-ranging American black bears (Ursus americanus). In addition, we reference other research by colleagues and collaborators who have leveraged these devices in their work, including: brown bears (Ursus arctos), grey wolves (Canis lupus), moose (Alces alces), maned wolves (Chrysocyon brachyurus) and southern elephant seals (Mirounga leonina). We also discuss the potentials for applications of such devices across a range of other species. To date, the devices described have been used in fifteen different wild species, with publications pending in many instances. We have focused our physiological research on the analyses of heart rates and rhythms and thus special attention will be paid to this topic. We then discuss some major expected step changes such as improvements in sensing algorithms, data storage, and the incorporation of next-generation short-range wireless telemetry. The latter provides new avenues for data transfer, and when combined with cloud-based computing, it not only provides means for big data storage but also the ability to readily leverage high-performance computing platforms using artificial intelligence and machine learning algorithms. These advances will dramatically increase both data quantity and quality and will facilitate the development of automated recognition of extreme physiological events or key behaviours of interest in a broad array of environments, thus further aiding wildlife monitoring and management. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

Artificial night light helps account for observer bias in citizen science monitoring of an expanding large mammal population.

The integration of citizen scientists into ecological research is transforming how, where, and when data are collected, and expanding the potential scales of ecological studies. Citizen-science projects can provide numerous benefits for participants while educating and connecting professionals with lay audiences, potentially increasing the acceptance of conservation and management actions. However, for all the benefits, collection of citizen-science data is often biased towards areas that are easily accessible (e.g. developments and roadways), and thus data are usually affected by issues typical of opportunistic surveys (e.g. uneven sampling effort). These areas are usually illuminated by artificial light at night (ALAN), a dynamic sensory stimulus that alters the perceptual world for both humans and wildlife. Our goal was to test whether satellite-based measures of ALAN could improve our understanding of the detection process of citizen-scientist-reported sightings of a large mammal. We collected observations of American black bears Ursus americanus (n = 1,315) outside their primary range in Minnesota, USA, as part of a study to gauge population expansion. Participants from the public provided sighting locations of bears on a website. We used an occupancy modelling framework to determine how well ALAN accounted for observer metrics compared to other commonly used metrics (e.g. housing density). Citizen scientists reported 17% of bear sightings were under artificially lit conditions and monthly ALAN estimates did the best job accounting for spatial bias in detection of all observations, based on AIC values and effect sizes ( ß^  = 0.81, 0.71-0.90 95% CI). Bear detection increased with elevated illuminance; relative abundance was positively associated with natural cover, proximity to primary bear range and lower road density. Although the highest counts of bear sightings occurred in the highly illuminated suburbs of the Minneapolis-St. Paul metropolitan region, we estimated substantially higher bear abundance in another region with plentiful natural cover and low ALAN (up to ~375% increased predicted relative abundance) where observations were sparse. We demonstrate the importance of considering ALAN radiance when analysing citizen-scientist-collected data, and we highlight the ways that ALAN data provide a dynamic snapshot of human activity.

Population reduction by hunting helps control human-wildlife conflicts for a species that is a conservation success story.

Among the world's large Carnivores, American black bears (Ursus americanus) are the foremost conservation success story. Populations have been expanding across North America because the species is adaptable and tolerant of living near people, and because management agencies in the U.S. and Canada controlled hunting and other human-sources of mortality. As a result, human-black bear conflicts (damage to property, general nuisance, threat to human safety) have dramatically increased in some areas, making it urgently important to develop and deploy a variety of mitigation tools. Previous studies claimed that legal hunting did not directly reduce conflicts, but they did not evaluate whether hunting controlled conflicts via management of population size. Here, we compared temporal patterns of phoned-in complaints about black bears (total ~63,500) in Minnesota, USA, over 4 decades to corresponding bear population estimates: both doubled during the first decade. We also quantified natural bear foods, and found that large year-to-year fluctuations affected numbers of complaints; however, since this variation is due largely to weather, this factor cannot be managed. Complaints fell sharply when the management agency (1) shifted more responsibility for preventing and mitigating conflicts to the public; and (2) increased hunting pressure to reduce the bear population. This population reduction was more extreme than intended, however, and after hunting pressure was curtailed, population regrowth was slower than anticipated; consequently both population size and complaints remained at relatively low levels statewide for 2 decades (although with local hotspots). These long-term data indicated that conflicts can be kept in tolerable bounds by managing population size through hunting; but due to the bluntness of this instrument and deficiencies and uncertainties in monitoring and manipulating populations, it is wiser to maintain a population at a level where conflicts are socially-acceptable than try to reduce it once it is well beyond that point.

Bears habituate to the repeated exposure of a novel stimulus, unmanned aircraft systems.

Unmanned aircraft systems (UAS; i.e. 'drones') provide new opportunities for data collection in ecology, wildlife biology and conservation. Yet, several studies have documented behavioral or physiological responses to close-proximity UAS flights. We experimentally tested whether American black bears (Ursus americanus) habituate to repeated UAS exposure and whether tolerance levels persist during an extended period without UAS flights. Using implanted cardiac biologgers, we measured heart rate (HR) of five captive bears before and after the first of five flights each day. Spikes in HR, a measure of stress, diminished across the five flights within each day and over the course of 4 weeks of twice-weekly exposure. We halted flights for 118 days, and when we resumed, HR responses were similar to that at the end of the previous trials. Our findings highlight the capacity of a large mammal to become and remain habituated to a novel anthropogenic stimulus in a relatively short time (3-4 weeks). However, such habituation to mechanical noises may reduce their wariness of other human threats. Also, whereas cardiac effects diminished, frequent UAS disturbances may have other chronic physiological effects that were not measured. We caution that the rate of habituation may differ between wild and captive animals: while the captive bears displayed large initial spikes in HR change (albeit not as large as wild bears), these animals were accustomed to regular exposure to humans and mechanical noises that may have hastened habituation to the UAS.

Six Years in the Life of a Mother Bear - The Longest Continuous Heart Rate Recordings from a Free-Ranging Mammal.

Physiological monitoring of free-ranging wild animals is providing new insights into their adaptations to a changing environment. American black bears (Ursus americanus) are highly adaptable mammals, spending up to half the year hibernating, and the remainder of the year attempting to gain weight on a landscape with foods that vary seasonally and year to year. We recorded heart rate (HR) and corresponding activity of an adult female black bear over the course of six years, using an implanted monitor. Despite yearly differences in food, and an every-other year reproductive cycle, this bear exhibited remarkable consistency in HR and activity. HR increased for 12 weeks in spring, from minimal hibernation levels (mean 20-25 beats/minute [bpm]; min 10 bpm) to summer active levels (July daytime: mean 95 bpm). Timing was delayed following one cold winter. In August the bear switched from primarily diurnal to nocturnal, coincident with the availability of baits set by legal hunters. Activity in autumn was higher when the bear was with cubs. Birthing of cubs in January was identified by a transient increase in HR and activity. Long-term physiological and behavioral monitoring is valuable for understanding adaptations of free-ranging animals to climate change, food availability, and human-related stressors.

Blood clotting behavior is innately modulated in Ursus americanus during early and late denning relative to summer months.

Remarkably, American black bears (Ursus americanus) are capable of varying their heart rates to coincide with their breathing, creating pauses of 30 s or more, yet they do not appear to suffer from embolic events. We evaluated some features of the clotting cascade of black bears, providing novel insights into the underlying mechanisms they evoke for embolic protection during hibernation. We measured activated clotting time, prothrombin time and activated partial thromboplastin time during early denning (December), late denning (March) and summer (August). Activated clotting time during early hibernation was ∼3 times longer than that observed among non-hibernating animals. Clotting time was reduced later in hibernation, when bears were within ∼1 month of emerging from dens. Prothrombin time was similar for each seasonal time point, whereas activated partial thromboplastin time was highest during early denning and decreased during late denning and summer. We also examined D-dimer concentration to assess whether the bears were likely to have experienced embolic events. None of the non-parturient bears exceeded a D-dimer concentration of 250 ng ml-1 (considered the clinical threshold for embolism in mammals). Our findings suggest there is unique expression of the clotting cascade in American black bears during hibernation, in which extrinsic pathways are maintained but intrinsic pathways are suppressed. This was evaluated by a significant difference between the activated clotting time and activated partial thromboplastin time during the denning and non-denning periods. These changes are likely adaptive, to avoid clotting events during states of immobilization and/or periods of asystole. However, an intact extrinsic pathway allows for healing of external injuries and/or foreign body responses.

Bears Show a Physiological but Limited Behavioral Response to Unmanned Aerial Vehicles.

Unmanned aerial vehicles (UAVs) have the potential to revolutionize the way research is conducted in many scientific fields. UAVs can access remote or difficult terrain, collect large amounts of data for lower cost than traditional aerial methods, and facilitate observations of species that are wary of human presence. Currently, despite large regulatory hurdles, UAVs are being deployed by researchers and conservationists to monitor threats to biodiversity, collect frequent aerial imagery, estimate population abundance, and deter poaching. Studies have examined the behavioral responses of wildlife to aircraft (including UAVs), but with the widespread increase in UAV flights, it is critical to understand whether UAVs act as stressors to wildlife and to quantify that impact. Biologger technology allows for the remote monitoring of stress responses in free-roaming individuals, and when linked to locational information, it can be used to determine events or components of an animal's environment that elicit a physiological response not apparent based on behavior alone. We assessed effects of UAV flights on movements and heart rate responses of free-roaming American black bears. We observed consistently strong physiological responses but infrequent behavioral changes. All bears, including an individual denned for hibernation, responded to UAV flights with elevated heart rates, rising as much as 123 beats per minute above the pre-flight baseline. It is important to consider the additional stress on wildlife from UAV flights when developing regulations and best scientific practices.

Big data in wildlife research: remote web-based monitoring of hibernating black bears.

BACKGROUND: Numerous innovations for the management and collection of "big data" have arisen in the field of medicine, including implantable computers and sensors, wireless data transmission, and web-based repositories for collecting and organizing information. Recently, human clinical devices have been deployed in captive and free-ranging wildlife to aid in the characterization of both normal physiology and the interaction of animals with their environment, including reactions to humans. Although these devices have had a significant impact on the types and quantities of information that can be collected, their utility has been limited by internal memory capacities, the efforts required to extract and analyze information, and by the necessity to handle the animals in order to retrieve stored data. RESULTS: We surgically implanted miniaturized cardiac monitors (1.2 cc, Reveal LINQ™, Medtronic Inc.), a newly developed human clinical system, into hibernating wild American black bears (N = 6). These devices include wireless capabilities, which enabled frequent transmissions of detailed physiological data from bears in their remote den sites to a web-based data storage and management system. Solar and battery powered telemetry stations transmitted detailed physiological data over the cellular network during the winter months. The system provided the transfer of large quantities of data in near-real time. Observations included changes in heart rhythms associated with birthing and caring for cubs, and in all bears, long periods without heart beats (up to 16 seconds) occurred during each respiratory cycle. CONCLUSIONS: For the first time, detailed physiological data were successfully transferred from an animal in the wild to a web-based data collection and management system, overcoming previous limitations on the quantities of data that could be transferred. The system provides an opportunity to detect unusual events as they are occurring, enabling investigation of the animal and site shortly afterwards. Although the current study was limited to bears in winter dens, we anticipate that future systems will transmit data from implantable monitors to wearable transmitters, allowing for big data transfer on non-stationary animals.

Fellatio in captive brown bears: evidence of long-term effects of suckling deprivation?

Sexually stimulating behaviors that are not linked to reproduction are rare among non-human (especially non-primate) mammals. Such behaviors may have a function in the hierarchy of social species. In solitary species, such behaviors are more enigmatic, and possibly indicative of something abnormal. Here, we report on a case of two male brown bears, raised in captivity since being orphaned as cubs, which engaged in recurrent fellatio multiple times per day until at least 10 years old. The roles of provider and receiver in the act remained unchanged, and the behavior itself became highly ritualized. The provider always initiated the contact involving vigorous penile sucking that appeared to result in ejaculation. We suggest that the behavior began as a result of early deprivation of maternal suckling, and persisted through life, possibly because it remained satisfying for both individuals. This constitutes the first descriptive report of fellatio in bears, and suggests that some bears may suffer lifelong behavioral consequences from being orphaned at an early age.

Prolonged recovery of sea otters from the Exxon Valdez oil spill? A re-examination of the evidence.

Sea otters (Enhydra lutris) suffered major mortality after the Exxon Valdez oil spill in Prince William Sound, Alaska, 1989. We evaluate the contention that their recovery spanned over two decades. A model based on the otter age-at-death distribution suggested a large, spill-related population sink, but this has never been found, and other model predictions failed to match empirical data. Studies focused on a previously-oiled area where otter numbers (~80) stagnated post-spill; nevertheless, post-spill abundance exceeded the most recent pre-spill count, and population trends paralleled an adjacent, unoiled-lightly-oiled area. Some investigators posited that otters suffered chronic effects by digging up buried oil residues while foraging, but an ecological risk assessment indicated that exposure levels via this pathway were well below thresholds for toxicological effects. Significant confounding factors, including killer whale predation, subsistence harvests, human disturbances, and environmental regime shifts made it impossible to judge recovery at such a small scale.

Wound healing during hibernation by black bears (Ursus americanus) in the wild: elicitation of reduced scar formation.

Even mildly hypothermic body or limb temperatures can retard healing processes in mammals. Despite this, we observed that hibernating American black bears (Ursus americanus Pallas, 1780) elicit profound abilities in mounting inflammatory responses to infection and/or foreign bodies. In addition, they resolve injuries during hibernation while maintaining mildly hypothermic states (30-35 °C) and without eating, drinking, urinating or defecating. We describe experimental studies on free-ranging bears that document their abilities to completely resolve cutaneous cuts and punctures incurred during or prior to hibernation. We induced small, full-thickness cutaneous wounds (biopsies or incisions) during early denning, and re-biopsied sites 2-3 months later (near the end of denning). Routine histological methods were used to characterize these skin samples. All biopsied sites with respect to secondary intention (open circular biopsies) and primary intention (sutured sites) healed, with evidence of initial eschar (scab) formation, completeness of healed epidermis and dermal layers, dyskeratosis (inclusion cysts), and abilities to produce hair follicles. These healing abilities of hibernating black bears are a clear survival advantage to animals injured before or during denning. Bears are known to have elevated levels of hibernation induction trigger (delta-opioid receptor agonist) and ursodeoxycholic acid (major bile acid within plasma, mostly conjugated with taurine) during hibernation, which may relate to these wound-healing abilities. Further research as to the underlying mechanisms of wound healing during hibernation could have applications in human medicine. Unique approaches may be found to improve healing for malnourished, hypothermic, diabetic and elderly patients or to reduce scarring associated with burns and traumatic injuries.

Monitoring the wild black bear's reaction to human and environmental stressors.

BACKGROUND: Bears are among the most physiologically remarkable mammals. They spend half their life in an active state and the other half in a state of dormancy without food or water, and without urinating, defecating, or physical activity, yet can rouse and defend themselves when disturbed. Although important data have been obtained in both captive and wild bears, long-term physiological monitoring of bears has not been possible until the recent advancement of implantable devices. RESULTS: Insertable cardiac monitors that were developed for use in human heart patients (Reveal® XT, Medtronic, Inc) were implanted in 15 hibernating bears. Data were recovered from 8, including 2 that were legally shot by hunters. Devices recorded low heart rates (pauses of over 14 seconds) and low respiration rates (1.5 breaths/min) during hibernation, dramatic respiratory sinus arrhythmias in the fall and winter months, and elevated heart rates in summer (up to 214 beats/min (bpm)) and during interactions with hunters (exceeding 250 bpm). The devices documented the first and last day of denning, a period of quiescence in two parturient females after birthing, and extraordinary variation in the amount of activity/day, ranging from 0 (winter) to 1084 minutes (summer). Data showed a transition toward greater nocturnal activity in the fall, preceding hibernation. The data-loggers also provided evidence of the physiological and behavioral responses of bears to our den visits to retrieve the data. CONCLUSIONS: Annual variations in heart rate and activity have been documented for the first time in wild black bears. This technique has broad applications to wildlife management and physiological research, enabling the impact of environmental stressors from humans, changing seasons, climate change, social interactions and predation to be directly monitored over multiple years.

Seasonal regulation of the growth hormone-insulin-like growth factor-I axis in the American black bear (Ursus americanus).

The American black bear maintains lean body mass for months without food during winter denning. We asked whether changes in the growth hormone/insulin-like growth factor-I (GH-IGF-I) axis may contribute to this remarkable adaptation to starvation. Serum IGF-I levels were measured by radioimmunoassay, and IGF-binding proteins (IGFBPs) were analyzed by ligand blotting. Initial studies in bears living in the wild showed that IGF-I levels are highest in summer and lowest in early winter denning. Detailed studies in captive bears showed that IGF-I levels decline in autumn when bears are hyperphagic, continue to decline in early denning, and later rise above predenning levels despite continued starvation in the den. IGFBP-2 increased and IGFBP-3 decreased in early denning, and these changes were also reversed in later denning. Treatment with GH (0.1 mg·kg(-1)·day(-1) × 6 days) during early denning increased serum levels of IGF-I and IGFBP-3 and lowered levels of IGFBP-2, indicating that denning bears remain responsive to GH. GH treatment lowered blood urea nitrogen levels, reflecting effects on protein metabolism. GH also accelerated weight loss and markedly increased serum levels of free fatty acids and ß-hydroxybutyrate, resulting in a ketoacidosis (bicarbonate decreased to 15 meq/l), which was reversed when GH was withdrawn. These results demonstrate seasonal regulation of GH/IGF-I axis activity in black bears. Diminished GH activity may promote fat storage in autumn in preparation for denning and prevent excessive mobilization and premature exhaustion of fat stores in early denning, whereas restoration of GH/IGF activity in later denning may prepare the bear for normal activity outside the den.

The shared preference niche of sympatric Asiatic black bears and sun bears in a tropical forest mosaic.

BACKGROUND: Ecologically similar species often coexist by partitioning use of habitats or resources. Such partitioning can occur through divergent or shared niches. We investigated overlap in habitat use and spatial co-occurrence by sympatric Asiatic black bears and sun bears in three habitats in Thailand, and thereby assessed which niche model best accounts for their coexistence. METHODS/PRINCIPAL FINDINGS: We used density of species-specific signs to assess habitat use. Signs of both bear species occurred in all three habitats, and on >60% of sampling transects. Both species fed mostly on fruit; insect feeding signs were uncommon, and were mostly from sun bears. Significant differences in habitat use occurred only in montane forest, the habitat in which fruit was most abundant; incidence of black bear sign there was six times higher than that of sun bears. Habitat use was similar between the two species in the other habitats, which comprised 85% of the area. Of 10 habitat attributes examined, fruiting tree density was the best predictor of occurrence for both species. Models that included interspecific competition (fresh foraging activity of the other species) were less supported than the top models without competition. CONCLUSIONS/SIGNIFICANCE: Bear species co-occurrence at both coarse and fine spatial scales and use of the same resources (fruit trees) indicated common niche preferences. However, their habitat use differed in ways expected from their physical differences: larger black bears dominated in the most fruit-rich habitat, and smaller sun bears used less-preferred insects. These results indicate broadly overlapping fundamental niches combined with asymmetric competition-features consistent with the concept of shared preference niches. This model of the niche has received little attention in ecology, but appears to be relatively common in nature.

A Quantitative Ecological Risk Assessment of the Toxicological Risks from Exxon Valdez Subsurface Oil Residues to Sea Otters at Northern Knight Island, Prince William Sound, Alaska.

A comprehensive, quantitative risk assessment is presented of the toxicological risks from buried Exxon Valdez subsurface oil residues (SSOR) to a subpopulation of sea otters (Enhydra lutris) at Northern Knight Island (NKI) in Prince William Sound, Alaska, as it has been asserted that this subpopulation of sea otters may be experiencing adverse effects from the SSOR. The central questions in this study are: could the risk to NKI sea otters from exposure to polycyclic aromatic hydrocarbons (PAHs) in SSOR, as characterized in 2001-2003, result in individual health effects, and, if so, could that exposure cause subpopulation-level effects? We follow the U.S. Environmental Protection Agency (USEPA) risk paradigm by: (a) identifying potential routes of exposure to PAHs from SSOR; (b) developing a quantitative simulation model of exposures using the best available scientific information; (c) developing scenarios based on calculated probabilities of sea otter exposures to SSOR; (d) simulating exposures for 500,000 modeled sea otters and extracting the 99.9% quantile most highly exposed individuals; and (e) comparing projected exposures to chronic toxicity reference values. Results indicate that, even under conservative assumptions in the model, maximum-exposed sea otters would not receive a dose of PAHs sufficient to cause any health effects; consequently, no plausible toxicological risk exists from SSOR to the sea otter subpopulation at NKI.

Integrated population modeling of black bears in Minnesota: implications for monitoring and management.

BACKGROUND: Wildlife populations are difficult to monitor directly because of costs and logistical challenges associated with collecting informative abundance data from live animals. By contrast, data on harvested individuals (e.g., age and sex) are often readily available. Increasingly, integrated population models are used for natural resource management because they synthesize various relevant data into a single analysis. METHODOLOGY/PRINCIPAL FINDINGS: We investigated the performance of integrated population models applied to black bears (Ursus americanus) in Minnesota, USA. Models were constructed using sex-specific age-at-harvest matrices (1980-2008), data on hunting effort and natural food supplies (which affects hunting success), and statewide mark-recapture estimates of abundance (1991, 1997, 2002). We compared this approach to Downing reconstruction, a commonly used population monitoring method that utilizes only age-at-harvest data. We first conducted a large-scale simulation study, in which our integrated models provided more accurate estimates of population trends than did Downing reconstruction. Estimates of trends were robust to various forms of model misspecification, including incorrectly specified cub and yearling survival parameters, age-related reporting biases in harvest data, and unmodeled temporal variability in survival and harvest rates. When applied to actual data on Minnesota black bears, the model predicted that harvest rates were negatively correlated with food availability and positively correlated with hunting effort, consistent with independent telemetry data. With no direct data on fertility, the model also correctly predicted 2-point cycles in cub production. Model-derived estimates of abundance for the most recent years provided a reasonable match to an empirical population estimate obtained after modeling efforts were completed. CONCLUSIONS/SIGNIFICANCE: Integrated population modeling provided a reasonable framework for synthesizing age-at-harvest data, periodic large-scale abundance estimates, and measured covariates thought to affect harvest rates of black bears in Minnesota. Collection and analysis of these data appear to form the basis of a robust and viable population monitoring program.

Extreme respiratory sinus arrhythmia enables overwintering black bear survival--physiological insights and applications to human medicine.

American black bears survive winter months without food and water while in a mildly hypothermic, hypometabolic, and inactive state, yet they appear to be able to return to near-normal systemic function within minutes of arousal. This study's goal was to characterize the cardiovascular performance of overwintering black bears and elicit the underlying mechanisms enabling survival. Mid-winter cardiac electrophysiology was assessed in four wild black bears using implanted data recorders. Paired data from early and late winter were collected from 37 wild bears, which were anesthetized and temporarily removed from their dens to record cardiac electrophysiological parameters (12-lead electrocardiograms) and cardiac dimensional changes (echocardiography). Left ventricular thickness, primary cardiac electrophysiological parameters, and cardiovascular response to threats ("fight or flight" response) were preserved throughout winter. Dramatic respiratory sinus arrhythmias were recorded (cardiac cycle length variations up to 865%) with long sinus pauses between breaths (up to 13 s). The accelerated heart rate during breathing efficiently transports oxygen, with the heart "resting" between breaths to minimize energy usage. This adaptive cardiac physiology may have broad implications for human medicine.

Distribution and abundance of sacred monkeys in Igboland, southern Nigeria.

Although primates are hunted on a global scale, some species are protected against harassment and killing by taboos or religious doctrines. Sites where the killing of sacred monkeys or the destruction of sacred groves is forbidden may be integral to the conservation of certain species. In 2004, as part of a distribution survey of Sclater's guenon (Cercopithecus sclateri) in southern Nigeria, we investigated reports of sacred monkeys in the Igbo-speaking region of Nigeria. We confirmed nine new sites where primates are protected as sacred: four with tantalus monkeys (Chlorocebus tantalus) and five with mona monkeys (Cercopithecus mona). During 2004-2006, we visited two communities (Akpugoeze and Lagwa) previously known to harbor sacred populations of Ce. sclateri to estimate population abundance and trends. We directly counted all groups and compared our estimates with previous counts when available. We also estimated the size of sacred groves and compared these with grove sizes reported in the literature. The mean size of the sacred groves in Akpugoeze (2.06 ha, n = 10) was similar to others in Africa south of the Sahel, but larger than the average grove in Lagwa (0.49 ha, n = 15). We estimated a total population of 124 Sclater's monkeys in 15 groups in Lagwa and 193 monkeys in 20 groups in Akpugoeze. The Akpugoeze population was relatively stable over two decades, although the proportion of infants declined, and the number of groups increased. As Sclater's monkey does not occur in any official protected areas, sacred populations are important to the species' long-term conservation. Despite the monkeys' destruction of human crops, most local people still adhere to the custom of not killing monkeys. These sites represent ideal locations in which to study the ecology of Sclater's monkey and human-wildlife interactions.

The status of the world's land and marine mammals: diversity, threat, and knowledge.

Knowledge of mammalian diversity is still surprisingly disparate, both regionally and taxonomically. Here, we present a comprehensive assessment of the conservation status and distribution of the world's mammals. Data, compiled by 1700+ experts, cover all 5487 species, including marine mammals. Global macroecological patterns are very different for land and marine species but suggest common mechanisms driving diversity and endemism across systems. Compared with land species, threat levels are higher among marine mammals, driven by different processes (accidental mortality and pollution, rather than habitat loss), and are spatially distinct (peaking in northern oceans, rather than in Southeast Asia). Marine mammals are also disproportionately poorly known. These data are made freely available to support further scientific developments and conservation action.