African savanna raptors show evidence of widespread population collapse and a growing dependence on protected areas.

The conversion of natural habitats to farmland is a major cause of biodiversity loss and poses the greatest extinction risk to birds worldwide. Tropical raptors are of particular concern, being relatively slow-breeding apex predators and scavengers, whose disappearance can trigger extensive cascading effects. Many of Africa's raptors are at considerable risk from habitat conversion, prey-base depletion and persecution, driven principally by human population expansion. Here we describe multiregional trends among 42 African raptor species, 88% of which have declined over a ca. 20-40-yr period, with 69% exceeding the International Union for Conservation of Nature criteria classifying species at risk of extinction. Large raptors had experienced significantly steeper declines than smaller species, and this disparity was more pronounced on unprotected land. Declines were greater in West Africa than elsewhere, and more than twice as severe outside of protected areas (PAs) than within. Worryingly, species suffering the steepest declines had become significantly more dependent on PAs, demonstrating the importance of expanding conservation areas to cover 30% of land by 2030-a key target agreed at the UN Convention on Biological Diversity COP15. Our findings also highlight the significance of a recent African-led proposal to strengthen PA management-initiatives considered fundamental to safeguarding global biodiversity, ecosystem functioning and climate resilience.

Value of combining transect counts and telemetry data to determine short-term population trends in a globally threatened species.

To evaluate conservation interventions, it is necessary to obtain reliable population trends for short (<10 years) time scales. Telemetry can be used to estimate short-term survival rates and is a common tool for assessing population trends, but it has limitations and can be biased toward specific behavioral traits of tagged individuals. Encounter rates calculated from transects can be useful for assessing changes across multiple species, but they can have large confidence intervals and be affected by variations in survey conditions. The decline of African vultures has been well-documented, but understanding of recent trends is lacking. To examine population trends, we used survival estimates from telemetry data collected over 6 years (primarily for white-backed vultures [Gyps africanus]) and transect counts conducted over 8 years (for 7 scavenging raptors) in 3 large protected areas in Tanzania. Population trends were estimated using survival analysis combined with the Leslie Lefkovitch matrix model from the telemetry data and using Bayesian mixed effects generalized linear regression models from the transect data. Both methods showed significant declines for white-backed vultures in Ruaha and Nyerere National Parks. Only telemetry estimates suggested significant declines in Katavi National Park. Encounter rates calculated from transects also showed declines in Nyerere National Park for lappet-faced vultures (38% annual declines) and Bateleurs (18%) and in Ruaha National Park for white-headed vultures (Trigonoceps occipitalis) (19%). Mortality rates recorded and inferred from telemetry suggested that poisoning is prevalent. However, only 6 mortalities of the 26 presumed mortalities were confirmed to be caused by poisoning, highlighting the challenges of determining the cause of death when working across large landscapes. Despite declines, our data provide evidence that southern Tanzania has higher current encounter rates of African vultures than elsewhere in East Africa. Preventing further declines will depend greatly on mitigating poisoning. Based on our results, we suggest that the use of multiple techniques improves understanding of population trends over the short term.

Importancia de combinar los conteos de transectos y los datos de telemetría para determinar las tendencias poblacionales a corto plazo de especies amenazadas a nivel mundial Resumen Para evaluar las intervenciones de conservación es necesario obtener tendencias poblacionales confiables para escalas temporales cortas (<10 años). La telemetría puede usarse para estimar las tasas de supervivencia a corto plazo, además de que es una herramienta común para analizar las tendencias poblacionales, pero tiene limitantes y puede sesgarse con el comportamiento específico de los individuos marcados. Las tasas de encuentro calculadas a partir de transectos pueden ser útiles para analizar cambios en varias especies, aunque pueden tener intervalos grandes de confianza y verse afectadas por las variantes en las condiciones del censo. La declinación de los buitres africanos está bien documentada, pero hace falta el conocimiento sobre las tendencias recientes. Usamos las estimaciones de supervivencia tomadas de datos telemétricos recolectados durante seis años (principalmente del buitre Gyps africanus) y los conteos de transecto de siete especies carroñeras realizados durante ocho años en tres áreas protegidas en Tanzania. Estimamos las tendencias poblacionales con la combinación de análisis de supervivencia y el modelo de matriz Leslie Lefkovitch hecho con los datos telemétricos y usando modelos bayesianos de regresión lineal generalizada de efectos mixtos hechos con los datos de los transectos. Ambos métodos indicaron declinaciones significativas de Gyps africanus en los Parques Nacionales Ruaha y Nyerere. Sólo las estimaciones telemétricas sugirieron una declinación significativa en el Parque Nacional Katavi. Las tasas de encuentro calculadas a partir de los transectos también indicaron declinaciones de Torgos tracheliotos (38% de declinaciones anuales) y de Terathopius ecaudutus (18%) en el Parque Nacional Nyerere y de Trigonoceps occipitalis (19%) en el Parque Nacional Ruaha. Las muertes registradas e inferidas a partir de la telemetría sugieren que el envenenamiento es prevalente. Sin embargo, sólo se confirmaron seis muertes por envenenamiento de las 26 supuestas, lo que resalta los obstáculos para determinar la causa de muerte cuando se trabaja en paisajes amplios. A pesar de las declinaciones, nuestros datos proporcionan evidencia de que el sur de Tanzania tiene tasas actuales de encuentro con buitres africanos más altas que en cualquier otra parte del occidente de África. La prevención de declinaciones en el futuro dependerá principalmente de evitar el envenenamiento. Con base en nuestros resultados, sugerimos que el uso de técnicas múltiples incrementa el conocimiento sobre las tendencias poblacionales a corto plazo.

We are what we eat, plus some per mill: Using stable isotopes to estimate diet composition in Gyps vultures over space and time.

Dietary studies in birds of prey involve direct observation and examination of food remains at resting and nesting sites. Although these methods accurately identify diet in raptors, they are time-consuming, resource-intensive, and associated with biases from the feeding ecology of raptors like Gyps vultures. Our study set out to estimate diet composition in Gyps vultures informed by stable isotopes that provide a good representation of assimilated diet from local systems.We hypothesized that differences in Gyps vulture diet composition is a function of sampling location and that these vultures move between Serengeti National Park and Selous Game Reserve to forage. We also theorized that grazing ungulates are the principal items in Gyps vulture diet.Through combined linear and Bayesian modeling, diet derived from δ13C in Gyps vultures consisted of grazing herbivores across sites, with those in Serengeti National Park consuming higher proportions of grazing herbivores (>87%). δ13C differences in vulture feather subsets did not indicate shifts in vulture diet and combined with blood δ13C, vultures fed largely on grazers for ~159 days before they were sampled. Similarly, δ15N values indicated Gyps vultures fed largely on herbivores. δ34S ratios separated where vultures fed when the two sites were compared. δ34S variation in vultures across sites resulted from baseline differences in plant δ34S values, though it is not possible to match δ34S to specific locations.Our findings highlight the relevance of repeated sampling that considers tissues with varying isotopic turnover and emerging Bayesian techniques for dietary studies using stable isotopes. Findings also suggested limited vulture movement between the two local systems. However, more sampling coupled with environmental data is required to fully comprehend this observation and its implications to Gyps vulture ecology and conservation.

A Global Review of Causes of Morbidity and Mortality in Free-Living Vultures.

Vulture species worldwide play a key role in ecosystems as obligate scavengers, and several populations have had precipitous declines. Research on vulture health is critical to conservation efforts including free-living vultures and captive breeding programs, but is limited to date. In this systematic review, we determined the reported causes of free-living vulture species morbidity and mortality worldwide. The most commonly reported cause of mortality was from toxins (60%), especially lead and pesticides, followed by traumatic injury (49%), including collisions with urban infrastructure and gunshot. Neglected areas of research in free-living vulture health include infectious diseases (16%), endocrine and nutritional disorders (6%), and neoplasia (< 1%). Almost half of the studies included in the review were conducted in either Spain or the USA, with a paucity of studies conducted in South America and sub-Saharan Africa. The highest number of studies was on Griffon (Gyps fulvus) (24%) and Egyptian vultures (Neophron percnopterus) (19%), while half of all vulture species had five or fewer studies. Future investigations on free-living vulture health should focus on neglected areas of research, such as infectious diseases, and areas with gaps in the current literature, such as South America, sub-Saharan Africa, and under-studied vulture species.

Functional traits driving species role in the structure of terrestrial vertebrate scavenger networks.

Species assemblages often have a non-random nested organization, which in vertebrate scavenger (carrion-consuming) assemblages is thought to be driven by facilitation in competitive environments. However, not all scavenger species play the same role in maintaining assemblage structure, as some species are obligate scavengers (i.e., vultures) and others are facultative, scavenging opportunistically. We used a database with 177 vertebrate scavenger species from 53 assemblages in 22 countries across five continents to identify which functional traits of scavenger species are key to maintaining the scavenging network structure. We used network analyses to relate ten traits hypothesized to affect assemblage structure with the "role" of each species in the scavenging assemblage in which it appeared. We characterized the role of a species in terms of both the proportion of monitored carcasses on which that species scavenged, or scavenging breadth (i.e., the species "normalized degree"), and the role of that species in the nested structure of the assemblage (i.e., the species "paired nested degree"), therefore identifying possible facilitative interactions among species. We found that species with high olfactory acuity, social foragers, and obligate scavengers had the widest scavenging breadth. We also found that social foragers had a large paired nested degree in scavenger assemblages, probably because their presence is easier to detect by other species to signal carcass occurrence. Our study highlights differences in the functional roles of scavenger species and can be used to identify key species for targeted conservation to maintain the ecological function of scavenger assemblages.

Teacher training as a means to sustained and multiplicative behavior change: An example using fuel-efficient stoves.

Chimpanzee conservation is dependent on addressing key threats such as habitat degradation, which is fueled by collection of firewood in Uganda's Kibale National Park. To address this threat, sustained behavior change that reduces dependence on fuelwood is needed. One of the greatest challenges for conservation education programs and behavior change campaigns is to have long-term and consistent effects on communities. Teacher trainings have potential to influence a large number of students over an extended period of time. In this study, we tested if teacher training on an activity designed to reduce community impact on the environment and thus reduce habitat encroachment in a critical chimpanzee habitat-construction of fuel-efficient stoves (FES)-could lead to retained knowledge and attitude improvements for students as well as sustained behavioral change in communities around Kibale National Park up to 2 years after initial training on the topic. We consistently found improvements in student knowledge and attitude change between the beginning and end of the year for third- and sixth-grade students in 11 program schools, but not in four control schools. In addition, the number of FES built by 120 teachers engaged in the program and their students continued to average over 150 stoves per year across 4 years. Our study suggests that teacher training can lead to sustained and multiplicative behavior change, which may mitigate threats to chimpanzees and other wildlife threatened by habitat encroachment in the park over time.

Increasing browse and social complexity can improve zoo elephant welfare.

While recent work has assessed how environmental and managerial changes influence elephant welfare across multiple zoos, few studies have addressed the effects of management changes within a single institution. In this paper, we examine how management changes related to social structure and diet affect the behavior of a group of zoo elephants over a 23-month period while also considering underlying factors, such as time of day, hormonal cycle, and individual differences. We recorded individual behaviors using 2-min scan samples during 60-min sessions. We analyzed behavioral changes across several study variables using generalized linear mixed models. We found that increasing browse can improve opportunities for foraging throughout the day but may not be sufficient to reduce repetitive behaviors. We observed that increasing group size and integration of bulls with cows can lead to increased social interaction in African elephants. Our results highlight the importance of using multiple management alterations to address elephant welfare, and considering environmental factors, when making management decisions.

Circulating nutrients and hematological parameters in managed African elephants (Loxodonta Africana) over a 1-year period.

African elephants (Loxodonta Africana) are currently considered a vulnerable species. One key to improving methods of species management is to better monitor and understand elephant nutrition. Analyzing circulating nutrients is one of the best and least invasive methods of monitoring managed elephant nutrition, but limited reference values are available. This study examined the circulating basic hematology concentrations, minerals, vitamins A, D, and E, and fatty acids of six African elephants (two males and four females) at the North Carolina Zoo collected monthly from March 2016 to April 2017 and compared levels among seasons. Creatinine (CRE) and albumin had seasonal differences (p ≤ .05). Calcium, magnesium, phosphorus, potassium, selenium, zinc, cobalt, manganese, and molybdenum displayed seasonal differences (p ≤ .05). Retinol and 25-hydroxyvitamin D2 had seasonal differences (p ≤ .05). Linoleic acid, α-linolenic acid, arachidonic acid, total omega-3 fatty acids, total omega-6 fatty acids, and the omega-6 to omega-3 ratio showed seasonal differences (p ≤ .05). Findings suggest that exogenous vitamin E supplements may not be necessary with a mixed feedstuff diet (hay, fortified concentrate pellet, browse, and produce) based on circulating values. This data offer updated information on circulating reference values and novel circulating concentrations of nutrients for Southeastern US managed African elephants that can be used to inform nutritional and health management in all similar habitats.

Analyses of African elephant (Loxodonta africana) diet with various browse and pellet inclusion levels.

To more closely simulate the diet of free-ranging elephants, the diet of six (2.4) African elephants (Loxodonta africana) was altered to include more browse and less pelleted complete feed (5% total diet). Dietary proximate compounds, minerals, vitamins A (and carotenoids), D and E, and fatty acids were analyzed on pelleted diet items and forages including hay, grass, and browse. A total of 42 browse species were offered over 1 year with an average total diet inclusion of 5.2% (dry matter basis) per day. Dietary Na and Se were low while Fe and Mn were high compared to published intake levels for elephants. Analyzed nutrients within browse varied widely among seasons and species. Ingredient analyses were used to create predicted elephant nutrient intake for (a) the current diet, (b) a diet excluding pellets, and (c) a diet excluding pellets and providing browse at doubled levels. Formulated diets excluding pellets had lower mineral levels than the current diet and doubled browse did not alter mineral inclusions of concern. This study provides seasonal data on the nutrient levels of Southeastern browse species important for various pachyderm and herbivorous species. Predicted nutrient intake with new diet scenarios does not support the exclusion of pellets in the diets of African elephants without greater browse quantity availability, strict diet management, or additional supplements.

Air temperature and diet influence body composition and water turnover in zoo-living African elephants (Loxodonta africana).

African elephants, the largest land animal, face particular physiological challenges in captivity and the wild. Captive elephants can become over- or under-conditioned with inadequate exercise and diet management. Few studies have quantified body composition or water turnover in elephants, and none to date have examined longitudinal responses to changes in diet or air temperature. Using the stable isotope deuterium oxide (2H2O), we investigated changes in body mass, estimated fat-free mass (FFM, including fat-free gut content) and body fat in response to a multi-year intervention that reduced dietary energy density for adult African elephants housed at the North Carolina Zoo. We also examined the relationship between air temperature and water turnover. Deuterium dilution and depletion rates were assayed via blood samples and used to calculate body composition and water turnover in two male and three female African elephants at six intervals over a 3-year period. Within the first year after the dietary intervention, there was an increase in overall body mass, a reduction in body fat percentage and an increase in FFM. However, final values of both body fat percentage and FFM were similar to initial values. Water turnover (males: 359 ± 9 l d-1; females: 241 ± 28 l d-1) was consistent with the allometric scaling of water use in other terrestrial mammals. Water turnover increased with outdoor air temperature. Our study highlights the physiological water dependence of elephants and shows that individuals have to drink every 2-3 days to avoid critical water loss of approximately 10% body mass in hot conditions.

Scavenging in the Anthropocene: Human impact drives vertebrate scavenger species richness at a global scale.

Understanding the distribution of biodiversity across the Earth is one of the most challenging questions in biology. Much research has been directed at explaining the species latitudinal pattern showing that communities are richer in tropical areas; however, despite decades of research, a general consensus has not yet emerged. In addition, global biodiversity patterns are being rapidly altered by human activities. Here, we aim to describe large-scale patterns of species richness and diversity in terrestrial vertebrate scavenger (carrion-consuming) assemblages, which provide key ecosystem functions and services. We used a worldwide dataset comprising 43 sites, where vertebrate scavenger assemblages were identified using 2,485 carcasses monitored between 1991 and 2018. First, we evaluated how scavenger richness (number of species) and diversity (Shannon diversity index) varied among seasons (cold vs. warm, wet vs. dry). Then, we studied the potential effects of human impact and a set of macroecological variables related to climatic conditions on the scavenger assemblages. Vertebrate scavenger richness ranged from species-poor to species rich assemblages (4-30 species). Both scavenger richness and diversity also showed some seasonal variation. However, in general, climatic variables did not drive latitudinal patterns, as scavenger richness and diversity were not affected by temperature or rainfall. Rainfall seasonality slightly increased the number of species in the community, but its effect was weak. Instead, the human impact index included in our study was the main predictor of scavenger richness. Scavenger assemblages in highly human-impacted areas sustained the smallest number of scavenger species, suggesting human activity may be overriding other macroecological processes in shaping scavenger communities. Our results highlight the effect of human impact at a global scale. As species-rich assemblages tend to be more functional, we warn about possible reductions in ecosystem functions and the services provided by scavengers in human-dominated landscapes in the Anthropocene.

Patterns of wounding in hamadryas baboons (Papio hamadryas) in North American zoos.

In North American zoos, hamadryas baboons (Papio hamadryas) have traditionally been housed as single one-male units (single male groups). In recent years, efforts have been made to house hamadryas in groups composed of multiple one-male units (multi-male groups) to more closely mirror their natural social structure, in addition to all-male or bachelor groups to manage surplus males. Given that the majority of social conflict in hamadryas occurs between males during the acquisition and defense of females, it was thought that managing hamadryas in these multi-male groups would result in increased rates of wounding. To assess this, incidences of wounding were recorded over one year across seven zoos (10 social groups, 59 individuals). Overall, we found no difference in wounding rates between group types, or by sex, and group type. These data provide evidence that managing hamadryas in multi-male and bachelor groups is an effective husbandry practice that does not negatively impact the welfare of the individuals, in addition to providing a more species-appropriate social setting for hamadryas in zoos. As the management of hamadryas in multi-male and bachelor groups continues and expands, additional research will be needed to understand what factors contribute to optimal cohesion, and welfare of groups and if wounding rates change as group size continues to increase.

Evaluating the effect of a year-long film focused environmental education program on Ugandan student knowledge of and attitudes toward great apes.

Films, as part of a larger environmental education program, have the potential to influence the knowledge and attitudes of viewers. However, to date, no evaluations have been published reporting the effectiveness of films, when used within primate range countries as part of a conservation themed program. The Great Ape Education Project was a year-long environmental education program implemented in Uganda for primary school students living adjacent to Kibale National Park (KNP) and Bwindi Impenetrable National Park (BINP). Students viewed a trilogy of conservation films about great apes, produced specifically for this audience, and participated in complementary extra-curricular activities. The knowledge and attitudes of students participating in the program from KNP, but not BINP were assessed using questionnaires prior to (N = 1271) and following (N = 872) the completion of the program. Following the program, students demonstrated a significant increase in their knowledge of threats to great apes and an increase in their knowledge of ways that villagers and students can help conserve great apes. Additionally, student attitudes toward great apes improved following the program. For example, students showed an increase in agreement with liking great apes and viewing them as important to the environment. These data provide evidence that conservation films made specifically to address regional threats and using local actors and settings can positively influence knowledge of and attitudes toward great apes among students living in a primate range country.

Understanding how mammalian scavengers use information from avian scavengers: cue from above.

Interspecific social information transfer can play a key role in many aspects of animal ecology from foraging to habitat selection to predator avoidance. Within scavenging communities, avian scavengers often act as producers and mammalian scavengers act as scroungers, but we predict that species-specific cueing will allow for mammalian scavengers to utilize particular avian scavenger species using preferred food sources similar to their own preferences. We use empirical and theoretic approaches to assess interactions between mammalian and avian scavengers in one of the most diverse scavenging guilds in Masai Mara National Reserve, Kenya. Using a spatially explicit model and data from experimental carcasses, we found evidence that mammals benefit from local enhancement provided by vultures and that mammalian-avian following patterns are consistent with the idea that species-specific cueing is occurring. Results suggest that ongoing population declines in avian scavengers may have significant impacts on mammalian scavengers and potentially create trophic cascades.

The crouching of the shrew: Mechanical consequences of limb posture in small mammals.

An important trend in the early evolution of mammals was the shift from a sprawling stance, whereby the legs are held in a more abducted position, to a parasagittal one, in which the legs extend more downward. After that transition, many mammals shifted from a crouching stance to a more upright one. It is hypothesized that one consequence of these transitions was a decrease in the total mechanical power required for locomotion, because side-to-side accelerations of the body have become smaller, and thus less costly with changes in limb orientation. To test this hypothesis we compared the kinetics of locomotion in two mammals of body size close to those of early mammals (< 40 g), both with parasagittally oriented limbs: a crouching shrew (Blarina brevicauda; 5 animals, 17 trials) and a more upright vole (Microtus pennsylvanicus; 4 animals, 22 trials). As predicted, voles used less mechanical power per unit body mass to perform steady locomotion than shrews did (P = 0.03). However, while lateral forces were indeed smaller in voles (15.6 ± 2.0% body weight) than in shrews (26.4 ± 10.9%; P = 0.046), the power used to move the body from side-to-side was negligible, making up less than 5% of total power in both shrews and voles. The most power consumed for both species was that used to accelerate the body in the direction of travel, and this was much larger for shrews than for voles (P = 0.01). We conclude that side-to-side accelerations are negligible for small mammals-whether crouching or more upright-compared to their sprawling ancestors, and that a more upright posture further decreases the cost of locomotion compared to crouching by helping to maintain the body's momentum in the direction of travel.

African vultures don't follow migratory herds: scavenger habitat use is not mediated by prey abundance.

The ongoing global decline in vulture populations raises major conservation concerns, but little is known about the factors that mediate scavenger habitat use, in particular the importance of abundance of live prey versus prey mortality. We test this using data from the Serengeti-Mara ecosystem in East Africa. The two hypotheses that prey abundance or prey mortality are the main drivers of vulture habitat use provide alternative predictions. If vultures select areas based only on prey abundance, we expect tracked vultures to remain close to herds of migratory wildebeest regardless of season. However, if vultures select areas where mortality rates are greatest then we expect vultures to select the driest regions, where animals are more likely to die of starvation, and to be attracted to migratory wildebeest only during the dry season when wildebeest mortality is greatest. We used data from GSM-GPS transmitters to assess the relationship between three vulture species and migratory wildebeest in the Mara-Serengeti ecosystem. Results indicate that vultures preferentially cluster around migratory herds only during the dry season, when herds experience their highest mortality. Additionally during the wet season, Ruppell's and Lappet-faced vultures select relatively dry areas, based on Normalized Difference Vegetation Index, whereas White-backed vultures preferred wetter areas during the wet season. Differences in habitat use among species may mediate coexistence in this scavenger guild. In general, our results suggest that prey abundance is not the primary driver of avian scavenger habitat use. The apparent reliance of vultures on non-migratory ungulates during the wet season has important conservation implications for vultures in light of on-going declines in non-migratory ungulate species and use of poisons in unprotected areas.