First record of Cebidicola armatus (Phthiraptera: Trichodectidae) on the Brachyteles hypoxanthus (Primate: Atelidae) in Brazil.

This study reports for the first time the infestation of Cebidicola armatus in Brachyteles hypoxanthus. In total, 14 lice were recovered of an individual in Minas Gerais, Brazil. These were subjected to a microscopic analysis and the identification of C. armatus was carried out through its very characteristic morphology.

Variation in monthly and seasonal elevation use impacts behavioral and dietary flexibility in Rhinopithecus bieti.

Black-and-white snub-nosed monkeys (Rhinopithecus bieti) rely on behavioral and dietary flexibility to survive in temperate latitudes at high-elevation habitats characterized by climate and resource seasonality. However, little is known about how elevation influences their behavioral and dietary flexibility at monthly or seasonal scales. We studied an isolated R. bieti population at Mt. Lasha in the Yunling Provincial Nature Reserve, Yunnan, China, between May 2008 and August 2016 to assess the impacts of elevation on feeding behavior and diet. Across our sample, R. bieti occupied elevations between 3031 and 3637 m above mean sea level (amsl), with a 315.1 m amsl range across months and a 247.3 m amsl range across seasons. Contrary to expectations, individuals spent less time feeding when ranging across higher elevations. Lichen consumption correlated with elevation use across months and seasons, with individuals spending more time feeding on this important resource at higher elevations. Leaf consumption only correlated with elevation use during the spring. Our results suggest that R. bieti do not maximize their food intake at higher elevations and that monthly and seasonal changes in lichen and leaf consumption largely explain variation in elevation use. These findings shed light on the responses of R. bieti to environmental change and offer insight into strategies for conserving their habitats in the face of anthropogenic disturbance.

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.

Drivers of habitat availability for terrestrial mammals: Unravelling the role of livestock, land conversion and intrinsic traits in the past 50 years.

The global decline of terrestrial species is largely due to the degradation, loss and fragmentation of their habitats. The conversion of natural ecosystems for cropland, rangeland, forest products and human infrastructure are the primary causes of habitat deterioration. Due to the paucity of data on the past distribution of species and the scarcity of fine-scale habitat conversion maps, however, accurate assessment of the recent effects of habitat degradation, loss and fragmentation on the range of mammals has been near impossible. We aim to assess the proportions of available habitat within the lost and retained parts of mammals' distribution ranges, and to identify the drivers of habitat availability. We produced distribution maps for 475 terrestrial mammals for the range they occupied 50 years ago and compared them to current range maps. We then calculated the differences in the percentage of 'area of habitat' (habitat available to a species within its range) between the lost and retained range areas. Finally, we ran generalized linear mixed models to identify which variables were more influential in determining habitat availability in the lost and retained parts of the distribution ranges. We found that 59% of species had a lower proportion of available habitat in the lost range compared to the retained range, thus hypothesizing that habitat loss could have contributed to range declines. The most important factors negatively affecting habitat availability were the conversion of land to rangeland and high density of livestock. Significant intrinsic traits were those related to reproductive timing and output, habitat breadth and medium body size. Our findings emphasize the importance of implementing conservation strategies to mitigate the impacts caused by human activities on the habitats of mammals, and offer evidence indicating which species have the potential to reoccupy portions of their former range if other threats cease to occur.

Paternity data reveal high MHC diversity among sires in a polygynandrous, egalitarian primate.

Evidence from human and nonhuman primates suggests that females avoid breeding with close kin and may choose mates based on MHC diversity, which can improve offspring survival. In despotic societies, female mate choice may be hindered by male sexual coercion, but in egalitarian societies, females may be less constrained. Among northern muriquis-an egalitarian, polygynandrous primate with male philopatry-analyses of new data on paternity and variation at microsatellite and MHC loci, combined with behavioural and life-history data, revealed that sires showed higher MHC diversity than expected by chance and were never close kin of dams, consistent with predictions of female mate choice and close inbreeding avoidance. However, females did not differentially reproduce with males who were more distantly related to them or more dissimilar at the MHC than expected by chance, nor with those who had more MHC alleles distinct from their own. The lack of male dominance may permit females to identify and reproduce preferentially with non-offspring males and with males who are more diverse at the MHC. Nonetheless, the absence of disassortative mating at the MHC and neutral loci suggests that female mate choice may be limited by other factors impacting male fertilization success.

Reproductive inequality in humans and other mammals.

To address claims of human exceptionalism, we determine where humans fit within the greater mammalian distribution of reproductive inequality. We show that humans exhibit lower reproductive skew (i.e., inequality in the number of surviving offspring) among males and smaller sex differences in reproductive skew than most other mammals, while nevertheless falling within the mammalian range. Additionally, female reproductive skew is higher in polygynous human populations than in polygynous nonhumans mammals on average. This patterning of skew can be attributed in part to the prevalence of monogamy in humans compared to the predominance of polygyny in nonhuman mammals, to the limited degree of polygyny in the human societies that practice it, and to the importance of unequally held rival resources to women's fitness. The muted reproductive inequality observed in humans appears to be linked to several unusual characteristics of our species-including high levels of cooperation among males, high dependence on unequally held rival resources, complementarities between maternal and paternal investment, as well as social and legal institutions that enforce monogamous norms.

Geographic, climatic, and phylogenetic drivers of variation in colobine activity budgets.

Folivorous primates are typically considered time minimizers because the constraints of their unique digestive systems require them to spend a large portion of their activity budgets resting. However, inter- and intraspecific behavioral variation in their activity budgets may be influenced by local geographic and climatic conditions and evolutionary history. We compiled 48 studies representing ten genera, 31 species, and 50 populations to assess geographic (elevation, latitude), climatic (precipitation, temperature), and phylogenetic correlates of colobine activity budgets. Time spent resting negatively correlated with time spent feeding, moving, and socializing. Except for time spent socializing, activity budgets were independent of phylogeny, with more time spent feeding and less time resting in higher-elevation habitats and at lower temperatures. Among the four most common genera in our sample, only in Rhinopithecus did time spent feeding increase with higher elevations (range, 950-3950 m above mean sea level) and lower temperatures (range, 0.9-25 ℃). Only in Trachypithecus did time spent resting decrease with lower temperatures (range, 19-25 ℃). Our findings suggest that there are no apparent effects of geographic or climatic gradients on colobine activity budgets except for Rhinopithecus and Trachypithecus, whose activities are biased in favor of energy maximization rather than time minimization. Compared with other colobines, the ability of Rhinopithecus to adapt their activity budget at high elevations may make them less vulnerable to climate change, while the greater sensitivity of Trachypithecus to heat may make them more vulnerable to climate change.

Demographic changes in an Atlantic Forest primate community following a yellow fever outbreak.

We investigated demographic changes in three primate species (Alouatta guariba, Sapajus nigritus, and Callithrix flaviceps) at the Reserva Particular do Patrimônio Natural-Feliciano Miguel Abdala, Caratinga, Minas Gerais, Brazil, following a yellow fever outbreak (YFO) by comparing their population sizes before (2015) and after the outbreak (2017-2018), and by monitoring the size, composition, and reproductive status of groups from 2017 to 2021. Comparisons of pre- and post-YFO census data indicate the A. guariba population declined by 86.6%, from an estimated minimum of 522 individuals to 70 individuals. However, by October 2021, the population had grown to at least 86 individuals, with an adult sex ratio (N = 53) that was female-biased (0.61). Eleven of the 13 groups being monitored systematically were reproductively active with high survivorship to 12 months of age. S. nigritus declined by 40%, from 377 to 226 individuals. The sex ratio of 33 adult S. nigritus is also female-biased (0.71), and at least 8 of 15 groups being monitored are reproductively active. C. flaviceps declined by 80%, from 85 individuals to the 15-17 individuals observed from 2017 to 2021. The female-biased adult sex ratio and presence of infants and juveniles in the A. guariba and S. nigritus groups are encouraging signs, but there is still great concern, especially for C. flaviceps. Continued monitoring of the demographics of these primates is needed as their persistence appears to still be at risk.

Thanatology in the northern muriqui (Brachyteles hypoxanthus).

Primate thanatology, or the study of primate responses to dying and death, has become increasingly relevant in recent years. However, the number of reports remains small and the quality of published records is highly variable. Here, we extend the literature on comparative thanatology with observations on a population of the northern muriqui (Brachyteles hypoxanthus). We compiled all seven cases of muriqui responses to dead, dying, or abandoned infants observed by trained researchers of the Muriqui Project of Caratinga between 1998 and 2020. Four different adult females were observed carrying their dead offspring (n = 4) and one of these females was also observed carrying her dead grand-offspring (n = 1). Five of the seven cases involved dead newborns, one involved a newborn abandoned by its mother on the forest floor, and one involved a 1.6-year-old infant that was visibly ill and died after its mother left it on the ground. Dead newborns were carried for 1-3 days, and all cases occurred during the dry season months. No other age-sex classes were observed to interact with the dead or dying immatures. Our observations are consistent with hypotheses concerning the predominance of dead-infant carrying in other primates, and with the effects of climate on rates of corpse disintegration. They also show the value of long-term studies for obtaining and understanding anecdotal records of rare behavior.

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 influence of seasonality, anthropogenic disturbances, and cyclonic activity on the behavior of northern sportive lemurs (Lepilemur septentrionalis) at Montagne des Français, Madagascar.

Anthropogenic tropical deforestation and degradation imminently threaten primates today. Primates living in these disturbed habitats may also be subjected to increasingly severe tropical storms such as cyclones or hurricanes. These disturbances pose an immediate risk to their livelihood and can dramatically alter their habitats, in turn potentially shifting behavioral patterns. We had the unique opportunity to study the effects of seasonality, anthropogenic disturbances, and the immediate effects of a cyclone on the behavior of the critically endangered northern sportive lemur (NSL) in an anthropogenically disturbed forest in Madagascar. Cyclone Enawo made landfall on March 7, 2017 in northeast Madagascar with sustained wind speeds of 230 km/h. We collected behavioral data on nine individual NSLs during both wet and dry seasons, before and after Cyclone Enawo, and in areas of differing human activity, using scan sampling at 5-min intervals. We ran generalized linear mixed models to test the effects of seasonality and disturbances on behavior. We found that NSLs spent more time feeding in dry months compared with wet (Z = -4.21, p < 0.001). More specifically, they spent more time-consuming leaves and vine species in the dry season (Z = -2.26, p = 0.02; Z = -2.3; p = 0.02). We also found that NSLs were observed at lower heights in trees after the cyclone (Z = -2.45; p = 0.016) and spent more time in the interior portions of trees (Z = 3.44; p < 0.001), perhaps due to extensive limb damage of emergent trees documented after the cyclone. Our analyses show that seasonality affected most aspects of NSL behavior, followed by the effects of Cyclone Enawo, with anthropogenic disturbances having little effect. Our data suggest that the behavioral flexibility of NSLs in response to predictable seasonality may enable them to respond similarly to stochastic climatic disturbances. However, their generalist diet may allow them to persist in anthropogenically disturbed landscapes without the need to greatly alter their behavior.

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.

Degree of Frugivory Predicts Rates of Food-Related Agonism and Intragroup Proximity in Wild Gray Woolly Monkeys (Lagothrix lagotricha cana).

The main factors influencing feeding competition among members of diurnal primate groups are the distribution, availability, and quality of food resources. Socioecological models predict that temporal availability of preferred resources, such as fruit, can influence intragroup feeding competition, which is expected to affect rates of agonism and intragroup spatial patterns. We evaluated the effects of temporal variation in fruit availability on the degree of frugivory (i.e., the proportion of time spent feeding on fruit in relation to total food consumption) and the effects of fruit availability and degree of frugivory on rates of agonistic interactions, and intragroup proximity in two wild groups of gray woolly monkeys (Lagothrix lagotricha cana) in southwestern Brazilian Amazonia. We recorded 227 agonistic interactions via the all occurrences method and 3549 records of spacing via scan sampling during an 8-mo field study from March to October 2017. We found that fruit availability showed a positive relationship with the woolly monkeys' degree of frugivory, which in turn showed a positive relationship with the rates of agonism. We also found that degree of frugivory positively affected intragroup proximity in periods of lower fruit availability, and that agonistic interactions and proximity covaried positively. Conversely, as the degree of frugivory increased, monkeys exhibited greater interindividual distances and, consequently, lower rates of agonism, consistent with lower levels of feeding competition in periods of higher fruit availability. Therefore, we suggest that intragroup contest competition for fruits is an important cost of group living even for generalized, opportunistic frugivorous primates, such as woolly monkeys.

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.

Phylogeographic evidence for two species of muriqui (genus Brachyteles).

The taxonomy of muriquis, the largest extant primates in the New World, is controversial. While some specialists argue for a monotypic genus (Brachyteles arachnoides), others favor a two-species classification, splitting northern muriquis (Brachyteles hypoxanthus) from southern muriquis (B. arachnoides). This uncertainty affects how we study the differences between these highly endangered and charismatic primates, as well as the design of more effective conservation programs. To address this issue, between 2003 and 2017 we collected over 230 muriqui fecal samples across the genus' distribution in the Brazilian Atlantic Forest, extracted DNA from these samples, and sequenced 423 base pairs of the mitochondrial DNA (mtDNA) control region. Phylogenetic and species delimitation analyses of our sequence dataset robustly support two reciprocally monophyletic groups corresponding to northern and southern muriquis separated by an average 12.7% genetic distance. The phylogeographic break between these lineages seems to be associated with the Paraíba do Sul River and coincides with the transition between the north and south Atlantic Forest biogeographic zones. Published divergence estimates from whole mitochondrial genomes and nuclear loci date the split between northern and southern muriquis to the Early Pleistocene (ca. 2.0 mya), and our new mtDNA dataset places the coalescence time for each of these two clades near the last interglacial (ca. 120-80 kya). Our results, together with both phenotypic and ecological differences, support recognizing northern and southern muriquis as sister species that should be managed as distinct evolutionarily significant units. Given that only a few thousand muriquis remain in nature, it is imperative that conservation strategies are tailored to protect both species from extinction.

From the field to the lab: Muriqui endocrinology from a collaborative perspective.

The northern muriqui (Brachyteles hypoxanthus) is a critically endangered species endemic to the Atlantic Forest of southeastern Brazil. Long-term observational studies of wild muriquis have provided many insights into the behavioral ecology and life history of this species. However, nearly everything that is currently known about the northern muriqui's behavioral endocrinology has come from combining our respective expertise in noninvasive field and laboratory research. Here, we reflect on the history of our collaboration, focusing on major challenges, key scientific findings, and factors that contributed to its success. Challenges included insuring the reliable collection of frequent fecal samples from a large enough number of known individuals over extended periods of time, preserving the steroids in the field and transporting them, developing and validating the fecal steroid assays, and interpreting the hormonal profiles within the behavioral and ecological contexts of the study subjects. Major findings included our thorough description of the fecal progesterone and estradiol profiles associated with muriqui ovarian cycling and gestation, the seasonal resumption of cycling, its onset during puberty of dispersing females, and the differences between fertile and infertile cycles. We also documented the relationship between fecal cortisol and testosterone in sexually active males across breeding and nonbreeding seasons, and sex differences in cortisol levels across the mating and conception seasons. We attribute the success of our collaboration to a number of factors including our mutual appreciation for one another's high standards for ethics, data quality, and data interpretation.

Status of the northern muriqui (Brachyteles hypoxanthus) in the time of yellow fever.

Understanding the impact of zoonotic diseases on wild primate populations is important for assessing local extinction risks and for evaluating potential mitigating factors. Comparative data on demographic changes in two isolated populations of the northern muriqui (Brachyteles hypoxanthus) during a severe yellow fever outbreak in southeastern Brazil provide unique insights into the potential effects of this disease in this Critically Endangered species. From October 2016 to April 2017, the muriqui population at the Reserva Particular do Patrimônio Natural-Feliciano Miguel Abdala (Caratinga) lost 31 of its 324 members, or nearly 10%, whereas the population at the Reserva Particular do Patrimônio Natural-Mata do Sossego (Sossego) declined from 34 to 25 individuals, or 26%. Greater per-capita risks to muriquis in the Sossego population could be related to ecological and anthropogenic differences, including a wetter climate and an absence of sympatric howler monkeys (Alouatta guariba), which may have directly or indirectly buffered the Caratinga muriquis. Although we lack definitive confirmation that the muriqui population declines were caused by yellow fever, the timing and magnitude of the losses strongly implicate the disease. We highlight the risks of catastrophic population declines in small populations and emphasize the value of long-term demographic monitoring studies.

Demographic monitoring of wild muriqui populations: Criteria for defining priority areas and monitoring intensity.

Demographic data are essential to assessments of the status of endangered species. However, establishing an integrated monitoring program to obtain useful data on contemporary and future population trends requires both the identification of priority areas and populations and realistic evaluations of the kinds of data that can be obtained under different monitoring regimes. We analyzed all known populations of a critically endangered primate, the muriqui (genus: Brachyteles) using population size, genetic uniqueness, geographic importance (including potential importance in corridor programs) and implementability scores to define monitoring priorities. Our analyses revealed nine priority populations for the northern muriqui (B. hypoxanthus) and nine for the southern muriqui (B. arachnoides). In addition, we employed knowledge of muriqui developmental and life history characteristics to define the minimum monitoring intensity needed to evaluate demographic trends along a continuum ranging from simple descriptive changes in population size to predictions of population changes derived from individual based life histories. Our study, stimulated by the Brazilian government's National Action Plan for the Conservation of Muriquis, is fundamental to meeting the conservation goals for this genus, and also provides a model for defining priorities and methods for the implementation of integrated demographic monitoring programs for other endangered and critically endangered species of primates.