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.

Mental health and well-being in primatology: Breaking the taboos.

We hope to raise awareness of mental health and well-being among primatologists. With this aim in mind, we organized a workshop on mental health as part of the main program of the Winter meeting of the Primate Society of Great Britain in December 2021. The workshop was very well received. Here, we review the main issues raised in the workshop, and supplement them with our own observations, reflections, and reading. The information we gathered during the workshop reveals clear hazards to mental health and suggests that we must collectively acknowledge and better manage both the hazards themselves and our ability to cope with them if we are to avert disaster. We call on institutions and learned societies to lead in seeking solutions for the benefit of primatologists and primatology.

Successful acclimatization of mandrills (Mandrillus sphinx) translocated to Conkouati-Douli National Park, Republic of Congo, as measured by fecal glucocorticoid metabolites.

Translocation and reintroduction are common tools in conservation management and can be very successful. However, translocation can be stressful for the animals involved, and stress is implicated as a major cause of failure in release programs. Conservation managers should therefore seek to understand how the stages of translocation impact stress physiology in the animals involved. We quantified fecal glucocorticoid metabolites (fGCMs) as a noninvasive measure of response to potential stressors during a translocation of 15 mandrills (Mandrillus sphinx) into Conkouati-Douli National Park, Republic of Congo. The mandrills were initially housed in a sanctuary, transferred to a pre-release enclosure in the National Park and then released into the forest. We collected repeated fecal samples (n = 1101) from known individuals and quantified fGCMs using a previously validated enzyme immunoassay. Transfer from the sanctuary to the pre-release enclosure correlated with a significant 1.93-fold increase in fGCMs, suggesting that transfer was a stressor for the mandrills. fGCM values decreased over time in the pre-release enclosure, suggesting that the mandrills recovered from the transfer and acclimatized to the enclosure. Release to the forest was not linked to a significant increase in fGCMs over the final values in the enclosure. Following release, fGCMs continued to decrease, fell below sanctuary values after just over a month and were about half the sanctuary values after 1 year. Overall, our results suggest that the translocation, although initially presenting a physiological challenge to the animals, was not detrimental to the well-being of the animals over the timescale of the study and, in fact, may have been beneficial. Our findings show the value of non-invasive physiology in monitoring, evaluating and designing wildlife translocations and, ultimately, contributing to their success.

Identification of potentially zoonotic parasites in captive orangutans and semi-captive mandrills: Phylogeny and morphological comparison.

Cysts and trophozoites of vestibuliferid ciliates and larvae of Strongyloides were found in fecal samples from captive orangutans Pongo pygmaeus and P. abelii from Czech and Slovak zoological gardens. As comparative material, ciliates from semi-captive mandrills Mandrillus sphinx from Gabon were included in the study. Phylogenetic analysis of the detected vestibuliferid ciliates using ITS1-5.8s-rRNA-ITS2 and partial 18S ribosomal deoxyribonucleic acid (rDNA) revealed that the ciliates from orangutans are conspecific with Balantioides coli lineage A, while the ciliates from mandrills clustered with Buxtonella-like ciliates from other primates. Morphological examination of the cysts and trophozoites using light microscopy did not reveal differences robust enough to identify the genera of the ciliates. Phylogenetic analysis of detected L1 larvae of Strongyloides using partial cox1 revealed Strongyloides stercoralis clustering within the cox1 lineage A infecting dogs, humans, and other primates. The sequences of 18S rDNA support these results. As both B. coli and S. stercoralis are zoonotic parasites and the conditions in captive and semi-captive settings may facilitate transmission to humans, prophylactic measures should reflect the findings.

Chemical cues of identity and reproductive status in Japanese macaques.

Olfactory communication plays an important role in the regulation of socio-sexual interactions in mammals. There is growing evidence that both human and nonhuman primates rely on odors to inform their mating decisions. Nevertheless, studies of primate chemical ecology remain scarce due to the difficulty of obtaining and analyzing samples. We analyzed 67 urine samples from five captive female Japanese macaques (Macaca fuscata) and 30 vaginal swabs from three of these females using gas chromatography-mass spectrometry and examined the relationship between odor (compounds identified, richness, intensity, and diversity) and female identity as well as cycle phase. We found a total of 36 urine compounds of which we identified 31, and 68 vaginal compounds of which we identified 37. Our results suggest that urine and vaginal odor varied more between individuals than within cycle phases. However, we found that within a female cycle, urine samples from similar phases may cluster more than samples from different phases. Our results suggest that female odor may encode information about identity (vaginal and urine odor) and reproductive status (urine odor). The question of how conspecifics use female urine and vaginal odor remains open and could be tested using bioassays. Our results and their interpretation are constrained by our limited sample size and our study design. Nonetheless, our study provides insight into the potential signaling role of female odor in sexual communication in Japanese macaques and contributes to our understanding of how odors may influence mating strategies in primates.

Preliminary assessment of gastrointestinal parasites of the sun-tailed monkey (Allochrocebus solatus) in a semi-free-ranging colony.

BACKGROUND: The occurrence of gastrointestinal parasites in the sun-tailed monkey (Allochrocebus solatus) at the CIRMF primatology center is unknown. We, therefore, assessed the presence and richness (number of different parasite taxa) of gastrointestinal parasites in a semi-free-ranging colony of A. solatus. METHODS: A total of 46 fecal samples were screened using a modified McMaster technique for fecal egg counts. RESULTS: In the 46 samples collected, seven taxa of gastrointestinal parasites, including protozoa and nematodes were identified. The most prevalent parasite was strongyles parasites (98%), followed by Trichuris spp. (72%), Strongyloides spp. (67%) and Entamoeba coli (65%). Balantioides coli (33%), Endolimax nana (25%), and Spirurid eggs (26%) were only found in a minority of the animals. CONCLUSIONS: This study contributes new host records of gastrointestinal parasites in semi-free-ranging A. solatus and highlights the need to investigate the health of this species and implement proper precautions in the management of this colony.

Seasonal variation in the behavioural ecology of samango monkeys (Cercopithecus albogularis schwarzi) in a southern latitude montane environment.

Samango monkeys (Cercopithecus albogularis schwarzi) in the Soutpansberg Mountains, South Africa, experience a highly seasonal climate, with relatively cold, dry winters. They must show behavioural flexibility to survive these difficult conditions near the southern limit of the species' distribution and maintain the minimum nutritional intake they require. Through environmental monitoring and behavioural observations of a habituated group of samango monkeys, we explored how they adapted to the highly seasonal climate they experienced in the mountains. Our results indicated that the monkeys varied their foraging behaviours to account for changes in climate and daylight availability. The samangos increased their food intake in colder months, specifically leaves, likely due to an increased need for calories during winter to maintain body temperature. Samango monkeys have anatomical and physiological adaptations for digesting leaves, and these are likely important in explaining their ability to adapt to the broad range of climatic conditions they experience.

Dental microstructure records life history events: A histological study of mandrills (Mandrillus sphinx) from Gabon.

Accentuated lines in dental microstructure are hypothesized to correlate with potentially stressful life history events, but our understanding of when, how and why such accentuated lines form in relation to stressful events is limited. We examined accentuated line formation and life history events in the teeth of three naturally deceased mandrills (Mandrillus sphinx, Cercopithecidae), for whom we had detailed life history information. We determined the ages at formation of accentuated lines in histological tooth sections and used dates of birth and death to calibrate dental histology to calendar time and individual age. We found accentuated lines that matched their mother's resumption of sexual cycles in two individuals, and possibly in the third individual. The subjects also formed lines when their mothers were mate-guarded by males or wounded. Accentuated lines matched the birth of the next sibling in one of two cases. Both females formed accentuated lines when they experienced their own sexual swelling cycles, but lines did not match all sexual swelling cycles. Mate-guarding matched an accentuated line in one case, but not in another. Lines matched all three parturitions in the two females. Changes in alpha male and captures did not consistently coincide with accentuated line formation, but repeated captures were associated with lines. Using simulated data, we show that the observed number of matches between lines and events would be very unlikely under a null hypothesis of random line formation. Our results support the hypothesis that some life history events are physiologically stressful enough to cause accentuated line formation in teeth. They contribute to our understanding of how primate life histories are recorded during dental development and enhance our ability to use teeth to reconstruct life history in the absence of direct observation.

Fecal glucocorticoids and gastrointestinal parasite infections in wild western lowland gorillas (Gorilla gorilla gorilla) involved in ecotourism.

Wildlife ecotourism can offer a source of revenue which benefits local development and conservation simultaneously. However, habituation of wildlife for ecotourism can cause long-term elevation of glucocorticoid hormones, which may suppress immune function and increase an animal's vulnerability to disease. We have previously shown that western lowland gorillas (Gorilla gorilla gorilla) undergoing habituation in Dzanga-Sangha Protected Areas, Central African Republic, have higher fecal glucocorticoid metabolite (FGCM) levels than both habituated and unhabituated gorillas. Here, we tested the relationship between FGCM levels and strongylid infections in the same gorillas. If high FGCM levels suppress the immune system, we predicted that FGCM levels will be positively associated with strongylid egg counts and that gorillas undergoing habituation will have the highest strongylid egg counts, relative to both habituated and unhabituated gorillas. We collected fecal samples over 12 months in two habituated gorilla groups, one group undergoing habituation and completely unhabituated gorillas. We established FGCM levels and fecal egg counts of Necator/Oesophagostomum spp. and Mammomonogamus sp. Controlling for seasonal variation and age-sex category in strongylid infections we found no significant relationship between FGCMs and Nectator/Oesophagostomum spp. or Mammomonogamus sp. egg counts in a within group comparison in either a habituated group or a group undergoing habituation. However, across groups, egg counts of Nectator/Oesophagostomum spp. were lowest in unhabituated animals and highest in the group undergoing habituation, matching the differences in FGCM levels among these gorilla groups. Our findings partially support the hypothesis that elevated glucocorticoids reduce a host's ability to control the extent of parasitic infections, and show the importance of non-invasive monitoring of endocrine function and parasite infection in individuals exposed to human pressure including habituation process and ecotourism.

Olfactory signals and fertility in olive baboons.

Female primates signal impending ovulation with a suite of sexual signals. Studies of these signals have focussed on visual, and to a lesser extent, acoustic signals, neglecting olfactory signals. We aimed to investigate the information content of female olfactory signals in captive olive baboons (Papio anubis) and relate these to the female fertile period. We studied eight adult females living in four groups at the CNRS Station de Primatologie, Rousset-sur-Arc, France. We used vaginal cytology to detect ovulation. We investigated the volatile component of odour signals using solid-phase microextraction and gas chromatography-mass spectrometry. We found a total of 74 volatile compounds, of which we tentatively identified 25, including several ketones, alcohols, aldehydes, terpenes, volatile fatty acids and hydrocarbons that have been identified in odour profiles of other primates. Our results show that vaginal odour intensity differs with sexual cycle stage suggesting that odour might play a role in signalling female baboon fertility. We found differences in vaginal odour between females living in all-female and in mixed sex groups but we could not distinguish the effects of group composition, female age and identity. This study of olfactory signalling improves our understanding of how female primates advertise their sexual receptivity.

Corrigendum: A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

[This corrects the article DOI: 10.1093/biosci/biaa082.].

Acceptability of neonatal sickle cell disease screening among parturient women at the Paul Moukambi Regional Hospital in rural Eastern Gabon, Central Africa.

Neonatal screening and the effective management of sickle cell disease (SCD) are now well established in urban areas in some sub-Saharan African countries. The high rate of sickle cell trait in Koula-Moutou, Gabon, prompted an assessment of the psycho-clinical context of the introduction of neonatal screening in this rural area in eastern Gabon. Interviews were conducted with 215 women from February to June 2016 in Maternity and Maternal Child Protection services at the Paul Moukambi Regional Hospital Center in Koula-Moutou. Few childbearing women knew about SCD (24%), very few (6%) knew their hemoglobin status and only 30% of parturient women authorized sampling for neonatal SCD screening. Young mothers aged 16-28 years (p=0.018) and those who were educated (p=0.002) were more likely to authorize neonatal blood screening. There was no association between acceptance of blood sampling and knowledge of SCD or the parturient woman's hemoglobin status. The barriers to acceptance for SCD neonatal diagnosis are related to the education and culture rather than the knowledge of this disease. Introduction of diagnosis in rural areas requires a team comprising a psychosocial worker and health workers known to the rural population, to remove inhibitions related to blood collection from newborn infants.

The occurrence of the red-handed howler monkey (Alouatta belzebul) in amazonian savannas is related to forest patch area and density of flooded area palms.

All Neotropical primates are arboreal and thus depend on forests for their survival. Arboreality puts many Neotropical primates at risk of extinction due to the high rates of deforestation in the tropics. We assessed the influence of vegetation structure and forest patch attributes on the occurrence of the threatened red-handed howler monkey (Alouatta belzebul) in an Amazonian savanna. Using a sample of 38 forest patches in a region of approximately 2000 km2 in the state of Amapá, northern Brazil, we used logistic regression to find the best predictors of the occurrence of A. belzebul. We assessed patch area, patch isolation, the proportion of seasonally flooded forest in the patch, the density of flooded area palms, forest height, canopy cover, and diameter at breast height of trees. Patch area and palm density were the best predictors of the occurrence of A. belzebul in forest patches, both having a positive effect on the probability of occurrence. Our results indicate that areas of flooded forest in forest patches may be keystone habitats for A. belzebul living in Amazonian savannas. The observed effect of palm density on A. belzebul suggests that this variable is useful for planning conservation actions, including the selection of areas for protection and management strategies for areas inhabited by this primate.

A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

Threats to biodiversity are well documented. However, to effectively conserve species and their habitats, we need to know which conservation interventions do (or do not) work. Evidence-based conservation evaluates interventions within a scientific framework. The Conservation Evidence project has summarized thousands of studies testing conservation interventions and compiled these as synopses for various habitats and taxa. In the present article, we analyzed the interventions assessed in the primate synopsis and compared these with other taxa. We found that despite intensive efforts to study primates and the extensive threats they face, less than 1% of primate studies evaluated conservation effectiveness. The studies often lacked quantitative data, failed to undertake postimplementation monitoring of populations or individuals, or implemented several interventions at once. Furthermore, the studies were biased toward specific taxa, geographic regions, and interventions. We describe barriers for testing primate conservation interventions and propose actions to improve the conservation evidence base to protect this endangered and globally important taxon.

Aegean monkeys and the importance of cross-disciplinary collaboration in archaeoprimatology: a reply to Urbani and Youlatos.

In their reply to our article "A new identification of the monkeys depicted in a Bronze Age wall painting from Akrotiri, Thera" [Primates 61(3), 2019], Urbani and Youlatos (Primates https://doi.org/10.1007/s10329-020-00825-2 , 2020) argue for the traditional identification of the monkeys depicted on the north and west walls of Room 6 of Building Complex Beta at Akrotiri, Thera, as vervet monkeys (Fig. 1). Their argument is based largely on previous scholarship and their analysis of monkey morphology as it appears in this Bronze Age artwork. Here, after clarifying some misconceptions and misquotations, we thoroughly contextualize the wall painting in question, emphasizing the importance of collaboration between disparate disciplines for a multifaceted and rigorous approach. The nature of the item in question is key in this reply: it is an artwork. Because the artwork in question is a cultural representation of monkeys rather than a study of live primates or preserved specimens, consideration of artistic choice, color conventions, and the agency of the artist, which are important facets of material culture, is important when answering the questions raised by Urbani and Youlatos, and should stimulate further cross-disciplinary discussions.

Odontochronologies in male and female mandrills (Mandrillus sphinx) and the development of dental sexual dimorphism.

OBJECTIVES: We examine how dental sexual dimorphism develops in mandrills, an extremely sexually dimorphic primate. We aimed to (a) establish the chronology of dental development (odontochronology) in male and female mandrills, (b) understand interindividual and intersex variation in odontochronologies, and (c) determine how dental sexual dimorphism is achieved. MATERIALS AND METHODS: We prepared histological ground sections from the permanent teeth of four female and four male mandrills from the semi-free ranging colony at the Centre International de Recherches Médicales, Franceville, Gabon. We used the microscopic growth increments in the sections to create odontochronologies. We compared ages at crown initiation, crown formation times (CFT) and crown extension rates (CER) between individuals and sexes to assess interindividual and intersex variation. RESULTS: All mandrill teeth are sexually dimorphic in size. Dental sexual dimorphism in mandrills is achieved via sex differences in the duration of growth (bimaturism) and in growth rates. We also found interindividual and intersex variation in the ages at initiation and completion of crown formation. DISCUSSION: Our results show that the rate of ameloblast differentiation varies between individuals and that selection for both the age at tooth initiation and CER has occurred independently in males and females to ensure that the teeth develop at appropriate times relative to the growth of the sexually dimorphic jaws. They also show that canine dimorphism is achieved through differences in both CER and CFT, unlike extant great apes or Cantius. Given at least three mechanisms for achieving canine dimorphism, we need more information to trace the evolution of this trait in primates.

A New Species of Sucking Louse from the Mandrill from Gabon with a Review of Host Associations and Geographical Distributions, and Identification Keys to Members of the Genus pedicinus (Phthiraptera: Anoplura: Pedicinidae).

Members of the sucking louse genus Pedicinus are ectoparasites of cercopithecid primates in Africa, Asia, and Gibraltar. Pedicinus gabonensis n. sp. is described on the basis of adult male and female specimens collected from the mandrill (Mandrillus sphinx) in Gabon. The new species is compared morphologically with other members of the genus Pedicinus, and a nuclear elongation factor 1 alpha gene sequence is provided. Host associations and geographical distributions of the 18 previously recognized species of the genus and of P. gabonensis n. sp. are reviewed. Updated identification keys are provided for males and females of all known valid species of Pedicinus.

A new identification of the monkeys depicted in a Bronze Age wall painting from Akrotiri, Thera.

Bronze Age Aegean (ca. 3500-1100 B.C.) wall paintings from the islands of Crete and Thera depict monkeys in a variety of roles such as running wild in nature, possibly following (trained) commands, and participating in sacred activities. These images, while stylistically Aegean, are traditionally considered closely related to-and descendant from-Egyptian, Near Eastern, and Mesopotamian monkey imagery. While monkey depictions in the latter regions may provide species-specific characteristics, Aegean wall paintings typically lack this level of detail. In an attempt to better understand the relationships between the monkeys depicted in Aegean wall paintings and the species that were encountered by the Aegean, Mesopotamian, and Egyptian peoples, a collaborative team of primatologists, a taxonomic illustrator, and an art historian/archaeologist identified species-indicative visual characteristics. This collaborative approach led us to identify a new region that serves as a source for monkey iconography: the Indus River Valley. With an emphasis on the primatological aspect and the growing corpus of possible Indus goods and possible species found in the Aegean, a broader iconographic and socioreligious sphere of interaction emerges. In this expanded system, Mesopotamia functions as an intermediary that enables the movement of goods, raw materials, people, and iconography between the east and west. Mesopotamia may have even afforded an opportunity for Aegean peoples to encounter the creatures themselves, first-hand. Of primary importance to the methodology employed for this project is the cooperation of scholars from disparate disciplines-the stitching together of various projects and experiences in attempt to answer both new and previously unanswerable questions. This type of interdisciplinary approach can be applied to other species, sites, paintings, and objects to hone our understanding of period, place, animal, movement, and trade.

Biochemical and biological validations of a faecal glucocorticoid metabolite assay in mandrills (Mandrillus sphinx).

Stress is a major factor in determining success when releasing endangered species into the wild but is often overlooked. Mandrills (Mandrills sphinx) are vulnerable to extinction due to habitat loss and demand for bush meat and the pet trade. To help bolster in situ populations, rehabilitated rescued mandrills recently were released into a protected area in the Republic of Congo. The goal of this study was to validate the use of faecal glucocorticoid metabolite enzyme immunoassays (EIAs) in mandrills and test field-friendly faecal hormone extraction techniques that can subsequently be used to monitor the stress physiology and welfare of mandrills throughout the release process. Using faecal samples collected from ex situ mandrills, we tested cortisol, corticosterone, 11ß-hydroxyetiocholanolone (69a), and 11-oxoetiocholanolone EIAs. Absolute concentrations, hormone profiles following medical procedures or translocation, and high-performance liquid chromatography fraction immunoreactivity showed that the 69a assay was the best choice to monitor the stress response in this species. Samples with delayed extraction or drying times had 40-80% lower 69a concentrations than samples extracted immediately post-collection and frozen. The 69a EIA is an appropriate assay for monitoring welfare in this species in situ or ex situ, and results indicated that consistent extraction methods are important for accurate comparisons.

Group and kin recognition via olfactory cues in chimpanzees (Pan troglodytes).

Primates were traditionally thought to have a reduced sense of smell. Although there is now evidence that olfaction plays a greater role in primate social life than previously assumed, research on the sense of smell in non-human apes is scarce. Chimpanzees sniff the ground and vegetation on boundary patrols, but the function of this behaviour is unclear. Since chimpanzees are highly territorial and can kill individuals that do not belong to their own community, sniffing might function to gather information about conspecifics, particularly concerning group membership and kinship. To investigate whether chimpanzees recognize group members and kin via olfactory cues, we conducted behavioural bioassays on two groups of chimpanzees at Leipzig Zoo. In a pilot study, we found that chimpanzees responded more strongly to urine than to faeces or body odour. We then presented urine from group members, outgroup individuals and an unscented control in aerated boxes using a simultaneous discrimination task. The first behaviour after a chimpanzee first approached a box was related to olfaction (sniffing, nose within 20 cm, licking) in 83% of cases, highlighting the importance of olfaction as a general investigation mechanism in this species. Chimpanzees sniffed significantly longer at urine stimuli than the control and significantly longer at odours from outgroup individuals than those from group members. Furthermore, the duration of sniffing was positively correlated with relatedness. Our results suggest that chimpanzees use olfactory cues to obtain information about social relationships and fill a gap in our understanding of primate chemical communication.