The bii4africa dataset of faunal and floral population intactness estimates across Africa's major land uses.

Sub-Saharan Africa is under-represented in global biodiversity datasets, particularly regarding the impact of land use on species' population abundances. Drawing on recent advances in expert elicitation to ensure data consistency, 200 experts were convened using a modified-Delphi process to estimate 'intactness scores': the remaining proportion of an 'intact' reference population of a species group in a particular land use, on a scale from 0 (no remaining individuals) to 1 (same abundance as the reference) and, in rare cases, to 2 (populations that thrive in human-modified landscapes). The resulting bii4africa dataset contains intactness scores representing terrestrial vertebrates (tetrapods: ±5,400 amphibians, reptiles, birds, mammals) and vascular plants (±45,000 forbs, graminoids, trees, shrubs) in sub-Saharan Africa across the region's major land uses (urban, cropland, rangeland, plantation, protected, etc.) and intensities (e.g., large-scale vs smallholder cropland). This dataset was co-produced as part of the Biodiversity Intactness Index for Africa Project. Additional uses include assessing ecosystem condition; rectifying geographic/taxonomic biases in global biodiversity indicators and maps; and informing the Red List of Ecosystems.

Lead exposure and its relationship with fecal cortisol levels in black howler monkeys (Alouatta pigra).

Efficiently detecting early environmental threats to wildlife is vital for conservation. Beyond obvious dangers like habitat loss or deforestation, our study focuses on one of the most hazardous toxic metals for wildlife: lead (Pb). Pb is a widespread, cumulative, and insidious environmental pollutant that can trigger a wide range of physiological, biochemical, and behavioral disorders. In fact, Pb can cause permanent dysfunction of the major stress system, the hypothalamic pituitary adrenal (HPA) axis. We analyzed Pb and cortisol concentrations in fecal samples from Alouatta pigra in southern Mexico. Fecal samples were collected across six sites categorized as free-ranging (n = 65; conserved and disturbed) and from captive animals (n = 58). Additionally, we collected soil samples (n = 35). We found that Pb was present in 28% of fecal samples and 83% of soil samples. There was a positive relation between fecal and soil Pb levels, and fecal Pb concentration was negatively associated with cortisol levels. However, the claim of Pb being a direct interference with HPA axis requires further investigation. Given our findings, assessing wildlife exposure can be a valuable tool for understanding potential Pb exposure levels in the environment and its possible implications for human health. It can also serve as an early warning system of these consequences.

Small apes adjust rhythms to facilitate song coordination.

Song coordination is a universal characteristic of human music. Many animals also produce well-coordinated duets or choruses that resemble human music. However, the mechanism and evolution of song coordination have only recently been studied in animals. Here, we studied the mechanism of song coordination in three closely related species of wild Nomascus gibbons that live in polygynous groups. In each species, song bouts were dominated by male solo sequences (referred to hereafter as male sequence), and females contributed stereotyped great calls to coordinate with males. Considering the function of rhythm in facilitating song coordination in human music and animal vocalizations, we predicted that adult males adjust their song rhythm to facilitate song coordination with females. In support of this prediction, we found that adult males produced significantly more isochronous rhythms with a faster tempo in male sequences that were followed by successful female great calls (a complete sequence with "introductory" and "wa" notes). The difference in isochrony and tempos between successful great call sequences and male sequences was smaller in N. concolor compared with the other two species, which may make it difficult for females to predict a male's precise temporal pattern. Consequently, adult females of N. concolor produced more failed great call (an incomplete sequence with only introductory notes) sequences. We propose that the high degree of rhythm change functions as an unambiguous signal that can be easily perceived by receivers. In this regard, gibbon vocalizations offer an instructive model to understand the origins and evolution of human music.

Fifty+ years of primate research illustrates complex drivers of abundance and increasing primate numbers.

Many primate populations are threatened by human actions and a central tool used for their protection is establishing protected areas. However, even if populations in such areas are protected from hunting and deforestation, they still may be threatened by factors such as climate change and its cascading impacts on habitat quality and disease dynamics. Here we provide a long-term and geographically wide-spread population assessment of the five common diurnal primates of Kibale National Park, Uganda. Over 7 year-long or longer census efforts that spanned 52 years, our team walked 1466 km, and recorded 480 monkey groups. Populations were generally relatively stable with a few exceptions, for which no apparent causative factors could be identified. This stability is unexpected as many ecological changes documented over the last 34+ years (e.g., decreasing food abundance and quality) were predicted to have negative impacts. Populations of some species declined at some sites but increased at others. This highlights the need for large, protected areas so that declines in particular areas are countered by gains in others. Kibale has large areas of regenerating forest and this most recent survey revealed that after 20+ years, forest regeneration in many of these areas appears sufficient to sustain sizeable primate populations, except for blue monkeys that have not colonized these areas. Indeed, the average primate abundance in the regenerating forest was only 8.1% lower than in neighboring old-growth forest. Thus, park-wide primate abundance has likely increased, despite many pressures on the park having risen; however, some areas in the park remain to be assessed. Our study suggests that the restoration, patrolling, and community outreach efforts of the Uganda Wildlife Authority and their partners have contributed significantly to protecting the park and its animals.

Cycles of fusion and fission enabled rapid parallel adaptive radiations in African cichlids.

Although some lineages of animals and plants have made impressive adaptive radiations when provided with ecological opportunity, the propensities to radiate vary profoundly among lineages for unknown reasons. In Africa's Lake Victoria region, one cichlid lineage radiated in every lake, with the largest radiation taking place in a lake less than 16,000 years old. We show that all of its ecological guilds evolved in situ. Cycles of lineage fusion through admixture and lineage fission through speciation characterize the history of the radiation. It was jump-started when several swamp-dwelling refugial populations, each of which were of older hybrid descent, met in the newly forming lake, where they fused into a single population, resuspending old admixture variation. Each population contributed a different set of ancient alleles from which a new adaptive radiation assembled in record time, involving additional fusion-fission cycles. We argue that repeated fusion-fission cycles in the history of a lineage make adaptive radiation fast and predictable.

Primate population dynamics in Ngogo, Kibale National Park, Uganda, over nearly five decades.

Many anthropogenic-driven changes, such as hunting, have clear and immediate negative impacts on wild primate populations, but others, like climate change, may take generations to become evident. Thus, informed conservation plans will require decades of population monitoring. Here, we expand the duration of monitoring of the diurnal primates at Ngogo in Kibale National Park, Uganda, from 32.9 to 47 years. Over the 3531 censuses that covered 15,340 km, we encountered 2767 primate groups. Correlation analyses using blocks of 25 census walks indicate that encounters with groups of black and white colobus, blue monkeys, and baboons neither increased nor decreased significantly over time, while encounters with groups of redtail monkeys and chimpanzees marginally increased. Encounters with mangabeys and L'Hoesti monkeys increased significantly, while red colobus encounters dramatically decreased. Detailed studies of specific groups at Ngogo document changes in abundances that were not always well represented in the censuses because these groups expanded into areas away from the transect, such as nearby regenerating forest. For example, the chimpanzee population increased steadily over the last 2 + decades but this increase is not revealed by our census data because the chimpanzees expanded, mainly to the west of the transect. This highlights that extrapolating population trends to large areas based on censuses at single locations should be done with extreme caution, as forests change over time and space, and primates adapt to these changes in several ways.

Vertebrate environmental DNA from leaf swabs.

Terrestrial vertebrates are threatened by anthropogenic activities around the world. The rapid biodiversity loss that ensues is most intense in the tropics and affects ecosystem functions, such as seed dispersal, or may facilitate pathogen transmission1. Monitoring vertebrate distributions is essential for understanding changes in biodiversity and ecosystems and also for adaptive management strategies. Environmental DNA (eDNA) approaches have the potential to play a key role in such efforts. Here, we explore whether eDNA swabbed from terrestrial vegetation in a tropical biodiversity hotspot is a useful tool for vertebrate biomonitoring. By swabbing leaves, we collected eDNA from 24 swabs at three locations in Kibale National Park, Uganda and used two metabarcoding systems to catalog the vertebrate taxa in the samples. We detected 52 wild vertebrate genera, including 26 avian and 24 mammalian genera; 30 of these assignments could be refined to the species level. We detected an average of 7.6 genera per swab. This approach, with its inexpensive and simple collection and DNA extraction, opens the door for inexpensive large-scale vertebrate biomonitoring.

Wild gibbons plan their travel pattern according to food types of breakfast.

Planning for the future is a complex skill that is often considered uniquely human. This cognitive ability has never been investigated in wild gibbons (Hylobatidae). Here we evaluated the movement patterns from sleeping trees to out-of-sight breakfast trees in two groups of endangered skywalker gibbons (Hoolock tianxing). These Asian apes inhabit a cold seasonal montane forest in southwestern China. After controlling for possible confounding variables including group size, sleeping pattern (sleep alone or huddle together), rainfall and temperature, we found that food type (fruits or leaves) of the breakfast tree was the most important factor affecting gibbon movement patterns. Fruit breakfast trees were more distant from sleeping trees compared with leaf trees. Gibbons left sleeping trees and arrived at breakfast trees earlier when they fed on fruits compared with leaves. They travelled fast when breakfast trees were located further away from the sleeping trees. Our study suggests that gibbons had foraging goals in mind and plan their departure times accordingly. This ability may reflect a capacity for route-planning, which would enable them to effectively exploit highly dispersed fruit resources in high-altitude montane forests.

Associations between faecal chemical pollutants and hormones in primates inhabiting Kibale National Park, Uganda.

While anthropogenic pollutants are known to be a threat to primates, our understanding of exposure to pollutants in situ and their sub-lethal effects is still limited. We used non-invasive biomonitoring to examine associations between faecal concentrations of 97 chemical pollutants and faecal hormone metabolites of cortisol and oestradiol in four primate species inhabiting Kibale National Park, Uganda (chimpanzees-Pan troglodytes, olive baboons-Papio anubis, red colobus-Piliocolobus tephrosceles and red-tailed monkeys-Cercopithecus ascanius). Across all species (n = 71 samples), results demonstrated positive associations of organochlorine pesticides (OCPs) (ß = 0.143, p = 0.020) and organophosphate esters (ß = 0.112, p = 0.003) with cortisol in adult females. Additionally, we observed positive associations of OCPs (ß = 0.192, p = 0.013) and brominated flame retardants (ß = 0.176, p = 0.004) with cortisol in juveniles. Results suggest that cumulative pesticides and flame retardants are disruptive to endocrine function in these populations, which could have implications for development, metabolism and reproduction. Our study further demonstrates that faeces can be an important, non-invasive matrix for examining pollutant-hormone associations in wild primates and other critical wildlife populations.

Trait matching and sampling effort shape the structure of the frugivory network in Afrotropical forests.

Frugivory in tropical forests is a major ecological process as most tree species rely on frugivores to disperse their seeds. However, the underlying mechanisms driving frugivore-plant networks remain understudied. Here, we evaluate the data available on the Afrotropical frugivory network to identify structural properties, as well as assess knowledge gaps. We assembled a database of frugivory interactions from the literature with > 10 000 links, between 807 tree and 285 frugivore species. We analysed the network structure using a block model that groups species with similar interaction patterns and estimates interaction probabilities among them. We investigated the species traits related to this grouping structure. This frugivory network was simplified into 14 tree and 14 frugivore blocks. The block structure depended on the sampling effort among species: Large mammals were better-studied, while smaller frugivores were the least studied. Species traits related to frugivory were strong predictors of the species composition of blocks and interactions among them. Fruits from larger trees were consumed by most frugivores, and large frugivores had higher probabilities to consume larger fruits. To conclude, this large-scale frugivory network was mainly structured by species traits involved in frugivory, and as expected by the distribution areas of species, while still being limited by sampling incompleteness.

Estimating the impact of the illegal trade of primates in Mexico: a potential threat to wildlife.

The primates of Mexico, Ateles geoffroyi, Alouatta palliata, and Alouatta pigra, are seriously threatened by habitat loss, fragmentation, and illegal hunting and trade. Very little is known about the extent of illegal trade and its impacts on declining primate populations. Our study proposes a potential method based on estimating the number of individuals that die in the trade before being detected and those that probably cannot be detected. This facilitates estimating the number of animals extracted and allows an assessment of how trafficking impacts their populations. We derive estimates from seizure data of primates in Mexico between 2010 and 2019. To do this, we created wildlife detection rates and mortality rates from the existing literature (scientific articles, journalistic articles, and notes) to estimate the number of primates that die during capture, transport, and sale and the number of trafficked primates that were not detected by Mexican authorities. We estimate that 946 primates were removed from the wild for the pet trade each year (spider monkey Ateles geoffroyi = 854; black howler monkeys Alouatta pigra = 38, mantled howler monkey Alouatta palliata = 54). The annual reduction in population size caused by trafficking was greatest for Ateles geoffroyi (2.2%), followed by Alouatta pigra (1.3%), and Alouatta palliata (0.4%). Our estimates show the percentage of impacts that trafficking has on Mexican primate populations. Nevertheless, trade has the potential to impact declining populations and still must be addressed.

Factors influencing terrestriality in primates of the Americas and Madagascar.

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs.

Chimpanzees (Pan troglodytes) harbor rich assemblages of malaria parasites, including three species closely related to P. falciparum (sub-genus Laverania), the most malignant human malaria parasite. Here, we characterize the ecology and epidemiology of malaria infection in wild chimpanzee reservoirs. We used molecular assays to screen chimpanzee fecal samples, collected longitudinally and cross-sectionally from wild populations, for malaria parasite mitochondrial DNA. We found that chimpanzee malaria parasitism has an early age of onset and varies seasonally in prevalence. A subset of samples revealed Hepatocystis mitochondrial DNA, with phylogenetic analyses suggesting that Hepatocystis appears to cross species barriers more easily than Laverania. Longitudinal and cross-sectional sampling independently support the hypothesis that mean ambient temperature drives spatiotemporal variation in chimpanzee Laverania infection. Infection probability peaked at ~24.5 °C, consistent with the empirical transmission optimum of P. falciparum in humans. Forest cover was also positively correlated with spatial variation in Laverania prevalence, consistent with the observation that forest-dwelling Anophelines are the primary vectors. Extrapolating these relationships across equatorial Africa, we map spatiotemporal variation in the suitability of chimpanzee habitat for Laverania transmission, offering a hypothetical baseline indicator of human exposure risk.

How individual, social, and ecological conditions influence dispersal decisions in male vervet monkeys.

Dispersal between social groups reduces the risk of inbreeding and can improve individuals' reproductive opportunities. However, this movement has costs, such as increased risk of predation and starvation, loss of allies and kin support, and increased aggression associated with entering the new group. Dispersal strategies, such as the timing of movement and decisions on whether to transfer alone or in parallel with a peer, involve different costs and benefits. We used demographic, behavioral, hormonal, and ecological data to examine the causes and consequences of 36 dispersal events from 29 male vervet monkeys (Chlorocebus pygerythrus) at Lake Nabugabo, Uganda. Adult males' secondary dispersal coincided with the conception season in females, and males improved their potential access to females by moving to groups with higher female-to-male sex ratios and/or by increasing their dominance rank. Males that dispersed with a peer had lower fecal glucocorticoid and androgen metabolite levels than lone dispersers. Subadult males were not more likely to engage in parallel dispersals compared to adult males. Dispersal was also used as a mechanism to avoid inbreeding, but changes in hormone levels did not seem to be a trigger of dispersal in our population. Our findings illustrate the complex individual strategies used during dispersal, how many factors can influence movement decisions, as well as the value of dominance and hormone analyses for understanding these strategies.

The cost of living in larger primate groups includes higher fly densities.

Flies are implicated in carrying and mechanically transmitting many primate pathogens. We investigated how fly associations vary across six monkey species (Cercopithecus ascanius, Cercopithecus mitis, Colobus guereza, Lophocebus albigena, Papio anubis, and Piliocolobus tephrosceles) and whether monkey group size impacts fly densities. Fly densities were generally higher inside groups than outside them, and considering data from these primate species together revealed that larger groups harbored more flies. Within species, this pattern was strongest for colobine monkeys, and we speculate this might be due to their smaller home ranges, suggesting that movement patterns may influence fly-primate associations. Fly associations increase with group sizes and may thus represent a cost to sociality.

Disassociation of social and sexual partner relationships in a gibbon population with stable one-male two-female groups.

Adult males living in a one-male multi-female social group are expected to try to monopolize copulations with resident females to increase reproductive fitness. Gibbons have traditionally been described as living in monogamous groups, with the sole resident adult male assumed to sire all of the group's offspring. Here, we used microsatellite analyses and behavioral observations to examine rates of extra-group paternity (EGP) over 16 years in a population of crested gibbons (Nomascus concolor) that form stable and long-term one-male two-female social units. Forty percent of offspring (N = 14) were sired by extra-group males. To understand this high level of EGP, we tested whether inbreeding avoidance was related to EGP. Females who engaged in EGP did not show larger pairwise relatedness with their resident male compared to females who did not engage in EGP. Nevertheless, the standardized heterozygosity of EGP offspring was significantly higher than for offspring sired by the group's resident male. These results provide partial support for the inbreeding avoidance hypothesis. It appears that resident male crested gibbons are unable to monopolize resident females' matings. Our results indicate that long-term social partners are often distinct from sexual partners in this population. Clearly, the breeding system of crested gibbons is more flexible than previously thought, indicating a need for integrating long-term behavioral data and genetic research to re-evaluate gibbon social and sexual relationships derived from concepts of monogamy and pair-bonding.

Identifying monitoring information needs that support the management of fish in large rivers.

Management actions intended to benefit fish in large rivers can directly or indirectly affect multiple ecosystem components. Without consideration of the effects of management on non-target ecosystem components, unintended consequences may limit management efficacy. Monitoring can help clarify the effects of management actions, including on non-target ecosystem components, but only if data are collected to characterize key ecosystem processes that could affect the outcome. Scientists from across the U.S. convened to develop a conceptual model that would help identify monitoring information needed to better understand how natural and anthropogenic factors affect large river fishes. We applied the conceptual model to case studies in four large U.S. rivers. The application of the conceptual model indicates the model is flexible and relevant to large rivers in different geographic settings and with different management challenges. By visualizing how natural and anthropogenic drivers directly or indirectly affect cascading ecosystem tiers, our model identified critical information gaps and uncertainties that, if resolved, could inform how to best meet management objectives. Despite large differences in the physical and ecological contexts of the river systems, the case studies also demonstrated substantial commonalities in the data needed to better understand how stressors affect fish in these systems. For example, in most systems information on river discharge and water temperature were needed and available. Conversely, information regarding trophic relationships and the habitat requirements of larval fishes were generally lacking. This result suggests that there is a need to better understand a set of common factors across large-river systems. We provide a stepwise procedure to facilitate the application of our conceptual model to other river systems and management goals.

Specialized digestive adaptations within the hindgut of a colobine monkey.

In mammal herbivores, fiber digestion usually occurs predominantly in either the foregut or the hindgut. Reports of mechanisms showing synergistic function in both gut regions for the digestion of fiber and other nutrients in wild mammals are rare because it requires integrative study of anatomy, physiology, and gut microbiome. Colobine monkeys (Colobinae) are folivorous, with high-fiber foods fermented primarily in their foreguts. A few colobine species live in temperate regions, so obtaining energy from fiber during the winter is essential. However, the mechanisms enabling this remain largely unknown. We hypothesized that such species possess specialized mechanisms to enhance fiber digestion in the hindgut and studied microbial and morphological digestive adaptations of golden snub-nosed monkeys (GSMs), Rhinopithecus roxellana. which is a temperate forest colobine from central China that experiences high-thermal-energy demands while restricted to a fibrous, low-energy winter diet. We tested for synergistic foregut and hindgut fiber digestion using comparisons of morphology, microbiome composition and function, and digestive efficiency. We found that the GSM colon has a significantly greater volume than that of other foregut-fermenting colobines. The microbiomes of the foregut and hindgut differed significantly in composition and abundance. However, while digestive efficiency and the expression of microbial gene functions for fiber digestion were higher in the foregut than in the hindgut, both gut regions were dominated by microbial taxa producing enzymes to enable active digestion of complex carbohydrates. Our data suggest that both the GSM foregut and hindgut facilitate fiber digestion and that an enlarged colon is likely an adaptation to accommodate high throughput of fiber-rich food during winter.