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.

News and Perspectives: Words matter in primatology.

Postings on social media on Twitter (now X), BioAnthropology News (Facebook), and other venues, as well as recent publications in prominent journals, show that primatologists, ecologists, and other researchers are questioning the terms "Old World" and "New World" due to their colonial implications and history. The terms are offensive if they result in erasing Indigenous voices and history, ignoring the fact that Indigenous peoples were in the Americas long before European colonization. Language use is not without context, but alternative terminology is not always obvious and available. In this perspective, we share opinions expressed by an international group of primatologists who considered questions about the use of these terms, whether primatologists should adjust language use, and how to move forward. The diversity of opinions provides insight into how conventional terms used in primatological research and conservation may impact our effectiveness in these domains.

Local Voices: Perspectives from the Local Community on the Primates of Kakamega Forest, Western Kenya.

From the perspective of a field research team comprising members of the local community near a rain forest in western Kenya, we describe the relationship between local people and local primates. Local people generally have little knowledge about the natural history of the monkeys living nearby, with people living closer to the forest knowing more. Most have a negative attitude toward monkeys because they occasionally forage on agricultural crops. A few people value monkey meat, which they believe to enhance human health. Participating in research on the behavioral ecology of blue monkeys allowed the author team to learn a great deal about these animals, including their role in the forest ecosystem and their behavioral similarities to humans. This experience differentiates their attitudes from most other members of their local community. However, the attitudes of local people are changing along with lifestyles. With more children in school and adults finding paid work, local people today generally have less experience of the forest than previous generations. A more tolerant attitude toward monkeys, recognizing their role in the forest ecosystem and their similarities to humans, is emerging among those who have been taught about biodiversity. This perspective is likely to contribute to their successful conservation.

The birth hour of mammals: insights from intra-specific variation in wild blue monkeys.

While most mammals show birth hour peaks at times of the 24-h cycle when they are less active, there are exceptions to this general pattern. Such exceptions have been little explored, but may clarify evolutionary reasons for the diel timing of births. We investigated intraspecific variation in birth hour in wild blue monkeys Cercopithecus mitis stuhlmanni, a diurnal primate, to identify factors that differentiated daytime versus nighttime births. Behavioral and life history data from 14 groups over 14 years revealed that 4% of 484 births occurred during the day. Probability of daytime birth varied with mother's age, peaking at 15.7 years. Births whose annual timing deviated most from the population's peak birth months were 5 times more likely to occur during daytime than those that deviated less. There was no evidence that mother's rank or infant sex influenced birth hour, and mixed evidence that daytime births were more probable in larger groups. Survivorship did not differ significantly for infants born during the day versus night. Prime-aged mothers may be able to handle the consequences of an unusual birth hour more successfully than mothers with less experience or those weakened by age. Daytime birth may be more advantageous in the off-season because nights are colder at that time of year. These findings are consistent with hypotheses relating birth hour to the risk of losing social protection in group-living animals, but are not consistent with those emphasizing risk of conspecific harassment. Patterns of within-species variation can help in evaluating evolutionary hypotheses for non-random birth hour.

Female reproductive aging in seven primate species: Patterns and consequences.

Age-related changes in fertility have increasingly been documented in wild animal populations: In many species the youngest and oldest reproducers are disadvantaged relative to prime adults. How do these effects evolve, and what explains their diversity across species? Tackling this question requires detailed data on patterns of age-related reproductive performance in multiple animal species. Here, we compare patterns and consequences of age-related changes in female reproductive performance in seven primate populations that have been subjects of long-term continuous study for 29 to 57 y. We document evidence of age effects on fertility and on offspring performance in most, but not all, of these primate species. Specifically, females of six species showed longer interbirth intervals in the oldest age classes, youngest age classes, or both, and the oldest females also showed relatively fewer completed interbirth intervals. In addition, five species showed markedly lower survival among offspring born to the oldest mothers, and two species showed reduced survival for offspring born to both the youngest and the oldest mothers. In contrast, we found mixed evidence that maternal age affects the age at which daughters first reproduce: Only in muriquis and to some extent in chimpanzees, the only two species with female-biased dispersal, did relatively young mothers produce daughters that tended to have earlier first reproduction. Our findings demonstrate shared patterns as well as contrasts in age-related changes in female fertility across species of nonhuman primates and highlight species-specific behavior and life-history patterns as possible explanations for species-level differences.

The long lives of primates and the 'invariant rate of ageing' hypothesis.

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.

Maternal death and offspring fitness in multiple wild primates.

Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the life span. Here, we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.

Energy balance but not competitive environment corresponds with allostatic load during development in an Old World monkey.

Primates develop slowly relative to their body size, a pattern posited to result from ecological risk aversion. Little is known, however, about how energy balance contributes to allostatic load in juveniles. Using data collected over 8 consecutive months, we examined variation in energy balance (as measured by urinary C-peptide) and how energy balance, life history status, and social competition related to allostatic load (as measured by deviation from baseline fecal glucocorticoid metabolites, dfGCs) in 41 wild juvenile blue monkeys from 3 social groups. Juvenile energy balance was higher among females, older juveniles, when ripe fruit was more available, and when rainfall was lower. Energy balance, but not life history or competitive environments, predicted dfGC concentrations, such that juveniles generally had lower mean dfGCs when they had higher energy balance. An additional exploratory analysis of how dfGCs relate to social strategies revealed that subjects had lower dfGCs when they groomed less, and played more. Time spent grooming interacted with energy balance in predicting dfGC concentrations, so that individuals that groomed more actually had higher dfGCs when they had higher energy balance. Together these results reveal that energetic deficiencies are a true ecological risk factor in blue monkeys, and suggest that navigating the social environment via overt affiliative behavior is potentially both a stress-relieving and stress-inducing endeavor during development.

Early life maternal sociality predicts juvenile sociality in blue monkeys.

Maternal effects are widespread in living organisms though little is known about whether they shape individual affiliative social behavior in primates. Further, it remains a question whether maternal effects on affiliative behavior differ by offspring sex, as they do in other physiological systems, especially in species with high levels of adult sexual dimorphism and divergence in social niches. We explored how direct and indirect experiences of maternal affiliative behavior during infancy predicted affiliative behavior approximately 1-6 years later during the juvenile period, using behavioral data from 41 wild blue monkey juveniles and their 29 mothers, and controlling for individual age, sex, and maternal rank. Female juveniles spent less time grooming with any partner and with peers the more maternal grooming they received during infancy, whereas males groomed more with any partner and with peers. Similarly, the more that mothers groomed with other adult females during subjects' infancy, female subjects played less with peers, and male subjects played more as juveniles. Further, this maternal effect on social behavior appears specific to early life, as the same aspects of mothers' sociality measured throughout subjects' development did not predict juvenile behavior. Overall, our results suggest that both direct and indirect experience of mother's affiliative behavior during infancy influence an individual's affiliation later in life that sexes respond differently to the maternal affiliation, and that the first year of life is a critical window.

Dietary generalists and nutritional specialists: Feeding strategies of adult female blue monkeys (Cercopithecus mitis) in the Kakamega Forest, Kenya.

Generalist primates eat many food types and shift their diet with changes in food availability. Variation in foods eaten may not, however, match variation in nutrient intake. We examined dietary variation in a generalist-feeder, the blue monkey (Cercopithecus mitis), to see how dietary food intake related to variation in available food and nutrient intake. We used 371 all-day focal follows from 24 adult females (three groups) in a wild rainforest population to quantify daily diet over 9 months. We measured food availability using vegetation surveys and phenology monitoring. We analyzed >700 food and fecal samples for macronutrient content. Subjects included 445 food items (species-specific plant parts and insect morphotypes) in their diet. Variation in fruit consumption (percentage of diet and total kcal) tracked variation in availability, suggesting fruit was a preferred food type. Fruits also constituted the majority of the diet (by calories) and some fruit species were eaten more than expected based on relative availability. In contrast, few species of young leaves were eaten more than expected. Also, subjects ate fewer young leaves (based on calories consumed) when fruit or young leaves were more available, suggesting that young leaves served as fallback foods. Despite the broad range of foods in the diet, group differences in fiber digestibility, and variation that reflected food availability, subjects and groups converged on similar nutrient intakes (grand mean ± SD: 637.1 ± 104.7 kcal overall energy intake, 293.3 ± 46.9 kcal nonstructural carbohydrate, 147.8 ± 72.4 kcal lipid, 107.8 ± 12.9 kcal available protein, and 88.1 ± 17.5 kcal structural carbohydrate; N = 24 subjects). Thus, blue monkeys appear to be food composition generalists and nutrient intake specialists, using flexible feeding strategies to regulate nutrient intake. Findings highlight the importance of simultaneously examining dietary composition at both levels of foods and nutrients to understand primate feeding ecology.

Energy balance but not competitive environment corresponds with allostatic load during development in an Old World monkey.

Primates develop slowly relative to their body size, a pattern posited to result from ecological risk aversion. Little is known, however, about how energy balance contributes to allostatic load in juveniles. Using data collected over 8 consecutive months, we examined variation in energy balance (as measured by urinary C-peptide) and how energy balance, life history status, and social competition related to allostatic load (as measured by deviation from baseline fecal glucocorticoid metabolites, dfGCs) in 41 wild juvenile blue monkeys from 3 social groups. Juvenile energy balance was higher among females, when ripe fruit was more available, and when rainfall was lower. Energy balance, but not life history or competitive environments, predicted dfGC concentrations, such that juveniles generally had lower mean dfGCs when they had higher energy balance. An additional exploratory analysis of how dfGCs relate to social strategies revealed that subjects had lower dfGCs when they groomed less, and played more. Time spent grooming interacted with energy balance in predicting dfGC concentrations, so that individuals that groomed more actually had higher dfGCs when they had higher energy balance. Together these results reveal that energetic deficiencies are a true ecological risk factor in blue monkeys, and suggest that navigating the social environment via overt affiliative behavior is potentially both a stress-relieving and stress-inducing endeavor during development.

Evidence for paternal kin bias in the social affiliation of adult female blue monkeys.

If animals increase inclusive fitness by cooperating with relatives, nepotism should involve maternal and paternal kin equally, all else being equal. Evidence of a behavioral bias toward paternal half-siblings in primates is both limited and mixed, with most positive reports from papionins. To expand knowledge of paternal kin recognition, particularly in cercopithecine monkeys, we examined evidence for paternal kin bias in wild blue monkeys (Cercopithecus mitis), a species living mostly in one-male groups. Seasonal breeding and the amount of male reproductive skew in blue monkeys suggests that opportunities to distinguish paternal kin are plentiful, and their social system would make such discrimination beneficial. We compared spatial association and social contact (grooming and contact-sitting) of 20 adult females with at least one paternal half-sibling and at least one non-relative that were present at the same time. We used two data sets, one in which social partners were other parous females, the other in which they were juveniles. Data came from a 7-year period. When interacting with other adult females, subjects groomed and sat in contact with paternal half-siblings significantly more than with known non-kin, and there was a similar trend for spatial association. We detected no paternal kin bias in interactions with juvenile partners. Kin-biased affiliative contact with adult female partners did not appear to be based on age proximity, measured by birth cohort. The study species' social system suggests phenotype matching as the most likely alternative mechanism, though we could not test it directly. Across both behaviors, there was no significant relationship between the number of matrilineal kin a subject had and the degree to which she preferred paternal half-siblings over non-kin as affiliative partners. These findings contribute to a comparative understanding of paternal kin recognition in primates.

Stronger social bonds do not always predict greater longevity in a gregarious primate.

In group-living species, individuals often have preferred affiliative social partners, with whom ties or bonds can confer advantages that correspond with greater fitness. For example, in adult female baboons and juvenile horses, individuals with stronger or more social ties experience greater survival. We used detailed behavioral and life history records to explore the relationship between tie quality and survival in a gregarious monkey (Cercopithecus mitis stuhlmanni), while controlling for dominance rank, group size, and life history strategy. We used Cox proportional hazards regressions to model the cumulative (multi-year) and current (single-year) relationships of social ties and the hazard of mortality in 83 wild adult females of known age, observed 2-8 years each (437 subject-years) in eight social groups. The strength of bonds with close partners was associated with increased mortality risk under certain conditions: Females that had strong bonds with close partners that were inconsistent over multiple years had a higher risk of mortality than females adopting any other social strategy. Within a given year, females had a higher risk of death if they were strongly bonded with partners that changed from the previous year versus with partners that remained consistent. Dominance rank, number of adult female groupmates, and age at first reproduction did not predict the risk of death. This study demonstrates that costs and benefits of strong social bonds can be context-dependent, relating to the consistency of social partners over time.

Does climate variability influence the demography of wild primates? Evidence from long-term life-history data in seven species.

Earth's rapidly changing climate creates a growing need to understand how demographic processes in natural populations are affected by climate variability, particularly among organisms threatened by extinction. Long-term, large-scale, and cross-taxon studies of vital rate variation in relation to climate variability can be particularly valuable because they can reveal environmental drivers that affect multiple species over extensive regions. Few such data exist for animals with slow life histories, particularly in the tropics, where climate variation over large-scale space is asynchronous. As our closest relatives, nonhuman primates are especially valuable as a resource to understand the roles of climate variability and climate change in human evolutionary history. Here, we provide the first comprehensive investigation of vital rate variation in relation to climate variability among wild primates. We ask whether primates are sensitive to global changes that are universal (e.g., higher temperature, large-scale climate oscillations) or whether they are more sensitive to global change effects that are local (e.g., more rain in some places), which would complicate predictions of how primates in general will respond to climate change. To address these questions, we use a database of long-term life-history data for natural populations of seven primate species that have been studied for 29-52 years to investigate associations between vital rate variation, local climate variability, and global climate oscillations. Associations between vital rates and climate variability varied among species and depended on the time windows considered, highlighting the importance of temporal scale in detection of such effects. We found strong climate signals in the fertility rates of three species. However, survival, which has a greater impact on population growth, was little affected by climate variability. Thus, we found evidence for demographic buffering of life histories, but also evidence of mechanisms by which climate change could affect the fates of wild primates.

Bat Predation by Cercopithecus Monkeys: Implications for Zoonotic Disease Transmission.

The relationship between bats and primates, which may contribute to zoonotic disease transmission, is poorly documented. We provide the first behavioral accounts of predation on bats by Cercopithecus monkeys, both of which are known to harbor zoonotic disease. We witnessed 13 bat predation events over 6.5 years in two forests in Kenya and Tanzania. Monkeys sometimes had prolonged contact with the bat carcass, consuming it entirely. All predation events occurred in forest-edge or plantation habitat. Predator-prey relations between bats and primates are little considered by disease ecologists, but may contribute to transmission of zoonotic disease, including Ebolavirus.

Female and male life tables for seven wild primate species.

We provide male and female census count data, age-specific survivorship, and female age-specific fertility estimates for populations of seven wild primates that have been continuously monitored for at least 29 years: sifaka (Propithecus verreauxi) in Madagascar; muriqui (Brachyteles hypoxanthus) in Brazil; capuchin (Cebus capucinus) in Costa Rica; baboon (Papio cynocephalus) and blue monkey (Cercopithecus mitis) in Kenya; chimpanzee (Pan troglodytes) in Tanzania; and gorilla (Gorilla beringei) in Rwanda. Using one-year age-class intervals, we computed point estimates of age-specific survival for both sexes. In all species, our survival estimates for the dispersing sex are affected by heavy censoring. We also calculated reproductive value, life expectancy, and mortality hazards for females. We used bootstrapping to place confidence intervals on life-table summary metrics (R0, the net reproductive rate; λ, the population growth rate; and G, the generation time). These data have high potential for reuse; they derive from continuous population monitoring of long-lived organisms and will be invaluable for addressing questions about comparative demography, primate conservation and human evolution.

Agonism and dominance in female blue monkeys.

Agonistic behavior features prominently in hypotheses that explain how social variation relates to ecological factors and phylogenetic constraints. Dominance systems vary along axes of despotism, tolerance, and nepotism, and comparative studies examine cross-species patterns in these classifications. To contribute to such studies, we present a comprehensive picture of agonistic behavior and dominance relationships in wild female blue monkeys (Cercopithecus mitis), an arboreal guenon, with data from 9 groups spanning 18 years. We assessed where blue monkeys fall along despotic, tolerant, and nepotistic spectra, how their dominance system compares to other primates, primarily cercopithecines, and whether their agonistic behavior matches socioecological model predictions. Blue monkeys showed low rates of mainly low-intensity agonism and little counter-aggression. Rates increased with rank and group size. Dominance asymmetry varied at different organizational levels, being more pronounced at the level of interactions than dyad or group. Hierarchies were quite stable, had moderate-to-high linearity and directional consistency and moderate steepness. There was clear maternal rank inheritance, but inconsistent adherence to Kawamura's rules. There was little between-group variation, although hierarchy metrics showed considerable variation across group-years. Overall, blue monkeys have moderately despotic, moderately tolerant, and nepotistic dominance hierarchies. They resemble other cercopithecines in having significantly linear and steep hierarchies with a generally stable, matriline-based structure, suggesting a phylogenetic basis to this aspect of their social system. Blue monkeys most closely match Sterck et al.'s [1997] Resident-Nepotistic-Tolerant dominance category, although they do not fully conform to predictions of any one socioecological model. Our results suggest that socioecological models might better predict variation within than across clades, thereby incorporating both ecological variables and phylogenetic constraints. Our findings also highlight the need for clearer definitions of socioecologically relevant dominance categories, which would ideally derive from quantitative measures of dominance behavior. Intraspecific and methodological variation may, however, be a challenge.

Life as a bachelor: quantifying the success of an alternative reproductive tactic in male blue monkeys.

In species that live in one-male groups, resident males monopolize access to a group of females and are assumed to have higher reproductive success than bachelors. We tested this assumption using genetic, demographic, and behavioral data from 8 groups of wild blue monkeys observed over 10 years to quantify reproduction by residents and bachelors and compare the success of the two tactics. We used maximum-likelihood methods to assign sires to 104 offspring born in the study groups, 36 of which were sired by extra-group males, i.e., residents of neighboring groups and bachelors. Among these extra-group males, high-ranking males (many of whom were neighboring residents) were more likely to sire offspring than low-ranking males, but the time these visiting males spent in the mother's group when she conceived (male presence) did not predict their relative success. When bachelors competed for reproduction with other bachelors, neither rank nor male presence during the mother's conceptive period affected the probability of siring an offspring, suggesting that highly opportunistic mating with conceptive females is important in bachelor reproduction. In a second analysis, we used long-term data to estimate resident and bachelor reproductive success over the long term, and particularly to determine if there are any circumstances in which a typical bachelor may sire as many offspring as a typical resident during one or two periods of residency. Our findings generally support the assumption of a resident reproductive advantage because in most circumstances, a lifelong bachelor would be unable to sire as many offspring as a resident. However, a bachelor who performs at the average rate in the average number of groups for several years may have similar lifetime reproductive success as a male whose reproduction is limited to one short period of residency, especially in a small group. Our findings suggest that one should not assume a resident reproductive advantage for males in one-male groups in all circumstances.

Social status and helminth infections in female forest guenons (Cercopithecus mitis).

OBJECTIVE: When resource competition within primate social groups is effective, high-ranking individuals generally gain fitness benefits. Contrary to expectations, female Cercopithecus mitis form linear dominance hierarchies without evidence for rank-related variation in fitness-relevant measures, raising questions about the evolution of guenon social structure. Here, we test whether social status predicts gastrointestinal helminth infections, known to influence health and morbidity in other mammalian hosts. In addition, we assess whether infections contribute to stress responses as indicated by fecal glucocorticoid (fGC) levels. METHODS: We quantified infections and hormone levels in 382 fecal samples from 11 adult female Sykes' monkeys (C. m. albogularis) over four months in one wild study group at Gede Ruins, Kenya. Using a generalized estimating equations technique, we modeled the odds of infection, relative infection intensity, and fGC variation. RESULTS: High-ranking females were less likely infected with Trichuris and Trichostrongylus, had lower fecal egg counts for both taxa, and overall lower helminth richness than low-ranking females. An inverse relationship between rank and Trichuris egg counts existed also in a study population of blue monkeys (C. m. stuhlmanni), where we collected comparable data over a shorter period. Regardless of rank, lactating females were more likely than non-lactating females to be infected with Trichuris, and had higher fecal egg counts for both Trichuris and Oesophagostomum. Lastly, we report evidence that Trichuris infections exacerbated energetic stress and that food supplementation by tourists increased infection levels. CONCLUSION: Our findings suggest that high-rank may provide long-term health and energetic benefits for female C. mitis, with potential fitness implications.