Behavioral Flexibility and the Evolution of Primate Social States

Comparative approaches to the evolution of primate social behavior have typically involved two distinct lines of inquiry. One has focused on phylogenetic analyses that treat social traits as static, species-specific characteristics; the other has focused on understanding the behavioral flexibility of particular populations or species in response to local ecological or demographic variables. Here, we combine these approaches by distinguishing between constraining traits such as dispersal regimes (male, female, or bi-sexual), which are relatively invariant, and responding traits such as grouping patterns (stable, fission-fusion, sometimes fission-fusion), which can reflect rapid adjustments to current conditions. Using long-term and cross-sectional data from 29 studies of 22 species of wild primates, we confirm that dispersal regime exhibits a strong phylogenetic signal in our sample. We then show that primate species with high variation in group size and adult sex ratios exhibit variability in grouping pattern (i.e., sometimes fission-fusion) with dispersal regime constraining the grouping response. When assessing demographic variation, we found a strong positive relationship between the variability in group size over time and the number of observation years, which further illustrates the importance of long-term demographic data to interpretations of social behavior. Our approach complements other comparative efforts to understand the role of behavioral flexibility by distinguishing between constraining and responding traits, and incorporating these distinctions into analyses of social states over evolutionary and ecological time

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

Genetic Diversity and Population History of a Critically Endangered Primate, the Northern Muriqui (Brachyteles hypoxanthus)

Social, ecological, and historical processes affect the genetic structure of primate populations, and therefore have key implications for the conservation of endangered species. The northern muriqui (Brachyteles hypoxanthus) is a critically endangered New World monkey and a flagship species for the conservation of the Atlantic Forest hotspot. Yet, like other neotropical primates, little is known about its population history and the genetic structure of remnant populations. We analyzed the mitochondrial DNA control region of 152 northern muriquis, or 17.6% of the 864 northern muriquis from 8 of the 12 known extant populations and found no evidence of phylogeographic partitions or past population shrinkage/expansion. Bayesian and classic analyses show that this finding may be attributed to the joint contribution of female-biased dispersal, demographic stability, and a relatively large historic population size. Past population stability is consistent with a central Atlantic Forest Pleistocene refuge. In addition, the best scenario supported by an Approximate Bayesian Computation analysis, significant fixation indices (ΦST = 0.49, ΦCT = 0.24), and population-specific haplotypes, coupled with the extirpation of intermediate populations, are indicative of a recent geographic structuring of genetic diversity during the Holocene. Genetic diversity is higher in populations living in larger areas (>2,000 hectares), but it is remarkably low in the species overall (θ = 0.018). Three populations occurring in protected reserves and one fragmented population inhabiting private lands harbor 22 out of 23 haplotypes, most of which are population-exclusive, and therefore represent patchy repositories of the species' genetic diversity. We suggest that these populations be treated as discrete units for conservation management purposes

Effects of local habitat variation on the behavioral ecology of two sympatric groups of brown howler monkey (alouatta clamitans)

Although the brown howler monkey (Alouatta clamitans) is a relatively well-studied Neotropical primate, its behavioral and dietary flexibility at the intra-population level remains poorly documented. This study presents data collected on the behavior and ecology of two closely located groups of brown howlers during the same period at the RPPN Feliciano Miguel Abdala in southeastern Brazil. One group occupied a primary valley habitat, henceforth the Valley Group (VG), and the other group occupied a regenerating hillside habitat, the Hill Group (HG). We hypothesized differences in the behavior and ecological parameters between these sympatric groups due to the predicted harsher conditions on the hillside, compared to the valley. We measured several habitat parameters within the home range of both groups and collected data on the activity budget, diet and day range lengths, from August to November 2005, between dawn and dusk. In total, behavioral data were collected for 26 (318 h) and 28 (308 h) sampling days for VG and HG, respectively. As we predicted, HG spent significantly more time feeding and consumed less fruit and more leaves than VG, consistent with our finding that the hillside habitat was of lower quality. However, HG also spent less time resting and more time travelling than VG, suggesting that the monkeys had to expend more time and energy to obtain high-energy foods, such as fruits and flowers that were more widely spaced in their hill habitat. Our results revealed that different locations in this forest vary in quality and raise the question of how different groups secure their home ranges. Fine-grained comparisons such as this are important to prioritize conservation and management areas within a reserve

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

Tropical field stations yield high conservation return on investment

Conservation funding is currently limited; cost-effective conservation solutions are essential. We suggest that the thousands of field stations worldwide can play key roles at the frontline of biodiversity conservation and have high intrinsic value. We assessed field stations’ conservation return on investment and explored the impact of COVID-19. We surveyed leaders of field stations across tropical regions that host primate research; 157 field stations in 56 countries responded. Respondents reported improved habitat quality and reduced hunting rates at over 80% of field stations and lower operational costs per km2 than protected areas, yet half of those surveyed have less funding now than in 2019. Spatial analyses support field station presence as reducing deforestation. These “earth observatories” provide a high return on investment; we advocate for increased support of field station programs and for governments to support their vital conservation efforts by investing accordingly.Additional co-authors: Ekwoge Abwe, Tanvir Ahmed, Marc Ancrenaz, Raphali R. Andriantsimanarilafy, Andie Ang, Filippo Aureli, Louise Barrett, Jacinta C. Beehner, Marcela E. Benítez, Bruna M. Bezerra, Júlio César Bicca-Marques, Dominique Bikaba, Robert Bitariho, Christophe Boesch, Laura M. Bolt, Ramesh Boonratana, Thomas M. Butynski, Gustavo R. Canale, Susana Carvalho, Colin A. Chapman, Dilip Chetry, Susan M. Cheyne, Marina Cords, Fanny M. Cornejo, Liliana Cortés-Ortiz, Camille N. Z. Coudrat, Margaret C. Crofoot, Drew T. Cronin, Alvine Dadjo, S. Chrystelle Dakpogan, Emmanuel Danquah, Tim R. B. Davenport, Yvonne A. de Jong, Stella de la Torre, Andrea Dempsey, Judeline C. Dimalibot, Rainer Dolch, Giuseppe Donati, Alejandro Estrada, Rassina A. Farassi, Peter J. Fashing, Eduardo Fernandez-Duque, Maria J. Ferreira da Silva, Julia Fischer, César F. Flores-Negrón, Barbara Fruth, Terence Fuh Neba, Lief Erikson Gamalo, Jörg U. Ganzhorn, Paul A. Garber, Smitha D. Gnanaolivu, Mary Katherine Gonder, Sery Ernest Gonedelé Bi, Benoit Goossens, Marcelo Gordo, Juan M. Guayasamin, Diana C. Guzmán-Caro, Andrew R. Halloran, Jessica A. Hartel, Eckhard W. Heymann, Russell A. Hill, Kimberley J. Hockings, Gottfried Hohmann, Naven Hon, Mariano G. Houngbédji, Michael A. Huffman, Rachel A. Ikemeh, Inaoyom Imong, Mitchell T. Irwin, Patrícia Izar, Leandro Jerusalinsky, Gladys Kalema-Zikusoka, Beth A. Kaplin, Peter M. Kappeler, Stanislaus M. Kivai, Cheryl D. Knott, Intanon Kolasartsanee, Kathelijne Koops, Martin M. Kowalewski, Deo Kujirakwinja, Ajith Kumar, Quyet K. Le, Rebecca J. Lewis, Aung Ko Lin, Andrés Link, Luz I. Loría, Menladi M. Lormie, Edward E. Louis Jr., Ngwe Lwin, Suchinda Malaivijitnond, Lesley Marisa, Gráinne M. McCabe, W. Scott McGraw, Addisu Mekonnen, Pedro G. Méndez-Carvajal, Tânia Minhós, David M. Montgomery, Citlalli Morelos-Juárez, David Morgan, Amancio Motove Etingüe, Papa Ibnou Ndiaye, K. Anne-Isola Nekaris, Nga Nguyen, Vincent Nijman, Radar Nishuli, Marilyn A. Norconk, Luciana I. Oklander, Rahayu Oktaviani, Julia Ostner, Emily Otali, Susan E. Perry, Eduardo J. Pinel Ramos, Leila M. Porter, Jill D. Pruetz, Anne E. Pusey, Helder L. Queiroz, Mónica A. Ramírez, Guy Hermas Randriatahina, Hoby Rasoanaivo, Jonah Ratsimbazafy, Joelisoa Ratsirarson, Josia Razafindramanana, Onja H. Razafindratsima, Vernon Reynolds, Rizaldi Rizaldi, Martha M. Robbins, Melissa E. Rodríguez, Marleny Rosales-Meda, Crickette M. Sanz, Dipto Sarkar, Anne Savage, Amy L. Schreier, Oliver Schülke, Gabriel H. Segniagbeto, Juan Carlos Serio-Silva, Arif Setiawan, John Seyjagat, Felipe E. Silva, Elizabeth M. Sinclair, Rebecca L. Smith, Denise Spaan, Fiona A. Stewart, Shirley C. Strum, Martin Surbeck, Magdalena S. Svensson, Mauricio Talebi, Luc Roscelin Tédonzong, Bernardo Urbani, João Valsecchi, Natalie Vasey, Erin R. Vogel, Robert B. Wallace, Janette Wallis, Siân Waters, Roman M. Wittig, Richard W. Wrangham, Patricia C. Wright, Russell A. Mittermeie

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.This study investigates the impact of habitat degradation on terrestrial mammal species. By comparing historic and current distribution maps for 475 species, we found that 59% of them have less available habitat in their lost ranges, suggesting habitat loss contributed to range declines. Factors like land conversion to rangeland and high livestock density negatively affected habitat availability. Intrinsic traits such as reproductive timing, habitat breadth and medium body size also played a role. The study underscores the need for conservation efforts to mitigate human-induced habitat threats and identifies species that could potentially reclaim lost range if threats are addressed.imag

The long lives of primates and the ‘invariant rate of ageing’ hypothesis

This work was supported by NIA P01AG031719 to J.W.V. and S.C.A., with additional support provided by the Max Planck Institute of Demographic Research and the Duke University Population Research Institute.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.Publisher PDFPeer reviewe

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 (bodymass, 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