Integrated global assessment of the natural forest carbon potential.

Forests are a substantial terrestrial carbon sink, but anthropogenic changes in land use and climate have considerably reduced the scale of this system1. Remote-sensing estimates to quantify carbon losses from global forests2-5 are characterized by considerable uncertainty and we lack a comprehensive ground-sourced evaluation to benchmark these estimates. Here we combine several ground-sourced6 and satellite-derived approaches2,7,8 to evaluate the scale of the global forest carbon potential outside agricultural and urban lands. Despite regional variation, the predictions demonstrated remarkable consistency at a global scale, with only a 12% difference between the ground-sourced and satellite-derived estimates. At present, global forest carbon storage is markedly under the natural potential, with a total deficit of 226 Gt (model range = 151-363 Gt) in areas with low human footprint. Most (61%, 139 Gt C) of this potential is in areas with existing forests, in which ecosystem protection can allow forests to recover to maturity. The remaining 39% (87 Gt C) of potential lies in regions in which forests have been removed or fragmented. Although forests cannot be a substitute for emissions reductions, our results support the idea2,3,9 that the conservation, restoration and sustainable management of diverse forests offer valuable contributions to meeting global climate and biodiversity targets.

The global biogeography of tree leaf form and habit.

Understanding what controls global leaf type variation in trees is crucial for comprehending their role in terrestrial ecosystems, including carbon, water and nutrient dynamics. Yet our understanding of the factors influencing forest leaf types remains incomplete, leaving us uncertain about the global proportions of needle-leaved, broadleaved, evergreen and deciduous trees. To address these gaps, we conducted a global, ground-sourced assessment of forest leaf-type variation by integrating forest inventory data with comprehensive leaf form (broadleaf vs needle-leaf) and habit (evergreen vs deciduous) records. We found that global variation in leaf habit is primarily driven by isothermality and soil characteristics, while leaf form is predominantly driven by temperature. Given these relationships, we estimate that 38% of global tree individuals are needle-leaved evergreen, 29% are broadleaved evergreen, 27% are broadleaved deciduous and 5% are needle-leaved deciduous. The aboveground biomass distribution among these tree types is approximately 21% (126.4 Gt), 54% (335.7 Gt), 22% (136.2 Gt) and 3% (18.7 Gt), respectively. We further project that, depending on future emissions pathways, 17-34% of forested areas will experience climate conditions by the end of the century that currently support a different forest type, highlighting the intensification of climatic stress on existing forests. By quantifying the distribution of tree leaf types and their corresponding biomass, and identifying regions where climate change will exert greatest pressure on current leaf types, our results can help improve predictions of future terrestrial ecosystem functioning and carbon cycling.

Native diversity buffers against severity of non-native tree invasions.

Determining the drivers of non-native plant invasions is critical for managing native ecosystems and limiting the spread of invasive species1,2. Tree invasions in particular have been relatively overlooked, even though they have the potential to transform ecosystems and economies3,4. Here, leveraging global tree databases5-7, we explore how the phylogenetic and functional diversity of native tree communities, human pressure and the environment influence the establishment of non-native tree species and the subsequent invasion severity. We find that anthropogenic factors are key to predicting whether a location is invaded, but that invasion severity is underpinned by native diversity, with higher diversity predicting lower invasion severity. Temperature and precipitation emerge as strong predictors of invasion strategy, with non-native species invading successfully when they are similar to the native community in cold or dry extremes. Yet, despite the influence of these ecological forces in determining invasion strategy, we find evidence that these patterns can be obscured by human activity, with lower ecological signal in areas with higher proximity to shipping ports. Our global perspective of non-native tree invasion highlights that human drivers influence non-native tree presence, and that native phylogenetic and functional diversity have a critical role in the establishment and spread of subsequent invasions.

Beyond Dimorphism: Body Size Variation Among Adult Orangutans Is Not Dichotomous by Sex.

Among extant great apes, orangutans are considered the most sexually dimorphic in body size. However, the expression of sexual dimorphism in orangutans is more complex than simply males being larger than females. At sexual maturity, some male orangutans develop cheek pads (flanges), while other males remain unflanged even after becoming reproductively capable. Sometimes flange development is delayed in otherwise sexually mature males for a few years. In other cases, flange development is delayed for many years or decades, with some males even spending their entire lifespan as unflanged adults. Thus, unflanged males of various chronological ages can be mistakenly identified as "subadults." Unflanged adult males are typically described as "female-sized," but this may simply reflect the fact that unflanged male body size has only ever been measured in peri-pubescent individuals. In this study, we measured the skeletons of 111 wild adult orangutans (Pongo spp.), including 20 unflanged males, 45 flanged males, and 46 females, resulting in the largest skeletal sample of unflanged males yet studied. We assessed long bone lengths (as a proxy for stature) for all 111 individuals and recorded weights-at-death, femoral head diameters, bi-iliac breadths, and long bone cross-sectional areas (CSA) (as proxies for mass) for 27 of these individuals, including seven flanged males, three adult confirmed-unflanged males, and three young adult likely-unflanged males. ANOVA and Kruskal-Wallis tests with Tukey and Dunn post-hoc pairwise comparisons, respectively, showed that body sizes for young adult unflanged males are similar to those of the adult females in the sample (all P ≥ 0.09 except bi-iliac breadth), whereas body sizes for adult unflanged males ranged between those of adult flanged males and adult females for several measurements (all P < 0.001). Thus, sexually mature male orangutans exhibit body sizes that range from the female end of the spectrum to the flanged male end of the spectrum. These results exemplify that the term "sexual dimorphism" fails to capture the full range of variation in adult orangutan body size. By including adult unflanged males in analyses of body size and other aspects of morphology, not as aberrations but as an expected part of orangutan variation, we may begin to shift the way that we think about features typically considered dichotomous according to biological sex.

Co-limitation towards lower latitudes shapes global forest diversity gradients.

The latitudinal diversity gradient (LDG) is one of the most recognized global patterns of species richness exhibited across a wide range of taxa. Numerous hypotheses have been proposed in the past two centuries to explain LDG, but rigorous tests of the drivers of LDGs have been limited by a lack of high-quality global species richness data. Here we produce a high-resolution (0.025° × 0.025°) map of local tree species richness using a global forest inventory database with individual tree information and local biophysical characteristics from ~1.3 million sample plots. We then quantify drivers of local tree species richness patterns across latitudes. Generally, annual mean temperature was a dominant predictor of tree species richness, which is most consistent with the metabolic theory of biodiversity (MTB). However, MTB underestimated LDG in the tropics, where high species richness was also moderated by topographic, soil and anthropogenic factors operating at local scales. Given that local landscape variables operate synergistically with bioclimatic factors in shaping the global LDG pattern, we suggest that MTB be extended to account for co-limitation by subordinate drivers.

The number of tree species on Earth.

One of the most fundamental questions in ecology is how many species inhabit the Earth. However, due to massive logistical and financial challenges and taxonomic difficulties connected to the species concept definition, the global numbers of species, including those of important and well-studied life forms such as trees, still remain largely unknown. Here, based on global ground-sourced data, we estimate the total tree species richness at global, continental, and biome levels. Our results indicate that there are ∼73,000 tree species globally, among which ∼9,000 tree species are yet to be discovered. Roughly 40% of undiscovered tree species are in South America. Moreover, almost one-third of all tree species to be discovered may be rare, with very low populations and limited spatial distribution (likely in remote tropical lowlands and mountains). These findings highlight the vulnerability of global forest biodiversity to anthropogenic changes in land use and climate, which disproportionately threaten rare species and thus, global tree richness.

Effects of a recurring late-night event on the behavior and welfare of a population of zoo-housed gorillas.

The impact of visitors on the well-being of captive animals presents both positive and potentially negative consequences. While some amount of novelty through visitor stimulation offers the opportunity for a more complex captive environment, anecdotal evidence from primate staff observations at the Smithsonian's National Zoo and Conservation Biology Institute suggested that gorillas exhibited increased restlessness during the annual month-long late night ZooLights (ZL) event than before it. The current study compared activity budgets, aggression (interactions involving contact between conspecifics and displays toward visitors), and abnormal behaviors in two groups of socially housed gorillas for 1-month periods before, during, and after the 2015 ZL event. We also compared the fecal glucocorticoid metabolite profiles of all six gorillas across these same observation periods. Physiologically, most individuals appeared to cope appropriately with the increased visitor presence during the event. We saw little difference in contact aggression; however, abnormal behavior was observed in some gorillas during and after the event, which highlights the importance of individual analysis and data interpretation. As predicted, we found that the majority of gorillas rested less during ZL than during other observation periods, particularly adult females in the mixed sex troop. Preliminary results of this study aided the decision of zoo management to close initially the Great Ape House and subsequently most animal buildings during future ZL events to avoid the potential disruption of normal activity patterns. While the findings of this study were mixed as to the impact of the event on these gorillas, the results suggest that zoos should carefully consider the possible ramifications of keeping great ape buildings open for lengthy multi-night events.

Phylogenetic classification of the world's tropical forests.

Knowledge about the biogeographic affinities of the world's tropical forests helps to better understand regional differences in forest structure, diversity, composition, and dynamics. Such understanding will enable anticipation of region-specific responses to global environmental change. Modern phylogenies, in combination with broad coverage of species inventory data, now allow for global biogeographic analyses that take species evolutionary distance into account. Here we present a classification of the world's tropical forests based on their phylogenetic similarity. We identify five principal floristic regions and their floristic relationships: (i) Indo-Pacific, (ii) Subtropical, (iii) African, (iv) American, and (v) Dry forests. Our results do not support the traditional neo- versus paleotropical forest division but instead separate the combined American and African forests from their Indo-Pacific counterparts. We also find indications for the existence of a global dry forest region, with representatives in America, Africa, Madagascar, and India. Additionally, a northern-hemisphere Subtropical forest region was identified with representatives in Asia and America, providing support for a link between Asian and American northern-hemisphere forests.

Maximum ingested food size in captive anthropoids.

OBJECTIVES: Maximum ingested food size (Vb ) is an empirically tested performance variable that can shed light on feeding energetics and adaptation in the masticatory system. Until now, this variable had been tested in strepsirrhines alone among primates. Here, we present the first data on Vb in a broad sample of anthropoid primates and describe scaling patterns. MATERIALS AND METHODS: Vb data on anthropoids were collected under captive conditions at the Philadelphia Zoo and compared with published data on strepsirrhines. Data on Vb were scaled against individual body mass and were compared with experimentally determined toughness and stiffness values for the test foods. RESULTS: Unlike in strepsirrhines, where essentially Vb scales isometrically with body mass, Vb in anthropoids scales with negative allometry. There is a significant effect of food material properties on Vb , although bite size in anthropoids varies less based on food properties than in strepsirrhines. Large folivorous strepsirrhines follow the anthropoid trend in bite size scaling, but large frugivorous ones take especially large bites. DISCUSSION: Negative scaling of bite size in the anthropoids sampled could be due to reduced adaptation for gape. Some early anthropoids likely evolved adaptations for maximizing mechanical advantage and fatigue resistance in the chewing muscles, resulting in reduced gape. This might have channeled them toward smaller bites of more-resistant foods and away from taking large bites. This might also be the case for some folivorous strepsirrhines.

An estimate of the number of tropical tree species.

The high species richness of tropical forests has long been recognized, yet there remains substantial uncertainty regarding the actual number of tropical tree species. Using a pantropical tree inventory database from closed canopy forests, consisting of 657,630 trees belonging to 11,371 species, we use a fitted value of Fisher's alpha and an approximate pantropical stem total to estimate the minimum number of tropical forest tree species to fall between ∼ 40,000 and ∼ 53,000, i.e., at the high end of previous estimates. Contrary to common assumption, the Indo-Pacific region was found to be as species-rich as the Neotropics, with both regions having a minimum of ∼ 19,000-25,000 tree species. Continental Africa is relatively depauperate with a minimum of ∼ 4,500-6,000 tree species. Very few species are shared among the African, American, and the Indo-Pacific regions. We provide a methodological framework for estimating species richness in trees that may help refine species richness estimates of tree-dependent taxa.

Call cultures in orang-utans?

BACKGROUND: Several studies suggested great ape cultures, arguing that human cumulative culture presumably evolved from such a foundation. These focused on conspicuous behaviours, and showed rich geographic variation, which could not be attributed to known ecological or genetic differences. Although geographic variation within call types (accents) has previously been reported for orang-utans and other primate species, we examine geographic variation in the presence/absence of discrete call types (dialects). Because orang-utans have been shown to have geographic variation that is not completely explicable by genetic or ecological factors we hypothesized that this will be similar in the call domain and predict that discrete call type variation between populations will be found. METHODOLOGY/PRINCIPAL FINDINGS: We examined long-term behavioural data from five orang-utan populations and collected fecal samples for genetic analyses. We show that there is geographic variation in the presence of discrete types of calls. In exactly the same behavioural context (nest building and infant retrieval), individuals in different wild populations customarily emit either qualitatively different calls or calls in some but not in others. By comparing patterns in call-type and genetic similarity, we suggest that the observed variation is not likely to be explained by genetic or ecological differences. CONCLUSION/SIGNIFICANCE: These results are consistent with the potential presence of 'call cultures' and suggest that wild orang-utans possess the ability to invent arbitrary calls, which spread through social learning. These findings differ substantially from those that have been reported for primates before. First, the results reported here are on dialect and not on accent. Second, this study presents cases of production learning whereas most primate studies on vocal learning were cases of contextual learning. We conclude with speculating on how these findings might assist in bridging the gap between vocal communication in non-human primates and human speech.

Diet traditions in wild orangutans.

This study explores diet differences between two populations of wild Bornean orangutans (Pongo pygmaeus wurmbii) to assess whether a signal of social learning can be detected in the observed patterns. The populations live in close proximity and in similar habitats but are separated by a river barrier that is impassable to orangutans in the study region. We found a 60% between-site difference in diet at the level of plant food items (plant species-organ combinations). We also found that individuals at the same site were more likely to eat the same food items than expected by chance. These results suggest the presence of diet (food selection) traditions. Detailed tests of three predictions of three models of diet acquisition allowed us to reject a model based on exclusive social learning but could not clearly distinguish between the remaining two models: one positing individual exploration and learning of food item selection and the other one positing preferential social learning followed by individual fine tuning. We know that maturing orangutans acquire their initial diet through social learning and then supplement it by years of low-level, individual sampling. We, therefore, conclude that the preferential social learning model produces the best fit to the geographic patterns observed in this study. However, the very same taxa that socially acquire their diets as infants and show evidence for innovation-based traditions in the wild paradoxically may have diets that are not easily distinguished from those acquired exclusively through individual learning.

Life history costs and benefits of encephalization: a comparative test using data from long-term studies of primates in the wild.

The correlation between brain size and life history has been investigated in many previous studies, and several viable explanations have been proposed. However, the results of these studies are often at odds, causing uncertainties about whether these two character complexes underwent correlated evolution. These disparities could arise from the mixture of wild and captive values in the datasets, potentially obscuring real relationships, and from differences in the methods of controlling for phylogenetic non independence of species values. This paper seeks to resolve these difficulties by (1) proposing an overarching hypothesis that encompasses many of the previously proposed hypotheses, and (2) testing the predictions of this hypothesis using rigorously compiled data and utilizing multiple methods of analysis. We hypothesize that the adaptive benefit of increased encephalization is an increase in reproductive lifespan or efficiency, which must be sufficient to outweigh the costs due to growing and maturing the larger brain. These costs and benefits are directly reflected in the length of life history stages. We tested this hypothesis on a wide range of primate species. Our results demonstrate that encephalization is significantly correlated with prolongation of all stages of developmental life history except the lactational period, and is significantly correlated with an extension of the reproductive lifespan. These results support the contention that the link between brain size and life history is caused by a balance between the costs of growing a brain and the survival benefits the brain provides. Thus, our results suggest that the evolution of prolonged life history during human evolution is caused by increased encephalization.

Animal innovation defined and operationalized.

Innovation is a key component of most definitions of culture and intelligence. Additionally, innovations may affect a species' ecology and evolution. Nonetheless, conceptual and empirical work on innovation has only recently begun. In particular, largely because the existing operational definition (first occurrence in a population) requires long-term studies of populations, there has been no systematic study of innovation in wild animals. To facilitate such study, we have produced a new definition of innovation: Innovation is the process that generates in an individual a novel learned behavior that is not simply a consequence of social learning or environmental induction. Using this definition, we propose a new operational approach for distinguishing innovations in the field. The operational criteria employ information from the following sources: (1) the behavior's geographic and local prevalence and individual frequency; (2) properties of the behavior, such as the social role of the behavior, the context in which the behavior is exhibited, and its similarity to other behaviors; (3) changes in the occurrence of the behavior over time; and (4) knowledge of spontaneous or experimentally induced behavior in captivity. These criteria do not require long-term studies at a single site, but information from multiple populations of a species will generally be needed. These criteria are systematized into a dichotomous key that can be used to assess whether a behavior observed in the field is likely to be an innovation.

Long-term effects of infant rearing condition on the acquisition of dominance rank in juvenile and adult rhesus macaques (Macaca mulatta).

We examined the effects of early rearing experience on the development of dominance status in 53 juvenile (age 3) and then in 38 adult (ages 5-8) rhesus macaques. Based on previous research investigating the behavioral outcomes of nursery-rearing, we predicted that mother-reared (MR) monkeys would outrank peer-only reared (PR) monkeys, which would in turn outrank surrogate/peer-reared (SPR) subjects. Juvenile MR and PR subjects did not differ in ranks, but monkeys from both rearing backgrounds outranked SPR cage-mates at age 3. Independent of rearing condition, high-ranking juveniles gained the most weight between ages 1-3, suggesting that low status may be associated with decreases in early weight gain. Adult MR subjects outranked both PR and SPR subjects, with PR animals occupying intermediate ranks. These results indicate that impoverished early experiences, such as adult absence and limited social interaction, are useful predictors of future social success in rhesus macaques.