{"title":"Outdoor noncontact respiratory measurements of unrestricted rhesus macaques (Macaca mulatta) using millimeter-wave radar","authors":"Toshiki Minami, Daisuke Sanematsu, Itsuki Iwata, Takuya Sakamoto, Masako Myowa","doi":"10.1002/ajp.23661","DOIUrl":"10.1002/ajp.23661","url":null,"abstract":"<p>Respiration is an invaluable signal that facilitates the real-time observation of physiological dynamics. In recent years, the advancement of noncontact measurement technology has gained momentum in capturing physiological activities in natural settings. This technology is anticipated to be found not only in humans but also in nonhuman primates. Currently, the predominant noncontact approach for nonhuman animals involves measuring vital signs through subtle variations in skin color. However, this approach is limited when addressing areas of the body covered with hair or when working in outdoor settings under fluctuating sunlight. To overcome this issue, we focused on noncontact respiratory measurements using millimeter-wave radar. Millimeter-wave radar systems, which employ millimeter waves that can penetrate animal fur and estimate respiration-derived periodic body motion, exhibit minimal susceptibility to sunlight interference. Thus, this method shows potential for conducting noncontact vital measurements in natural and outdoor settings. In this study, we validated a millimeter-wave radar methodology for capturing respiration in outdoor-housed rhesus macaques (<i>Macaca mulatta</i>). The radar was positioned beyond the captive enclosure and maintained at a distance >5 m from the target. Millimeter waves were transmitted to the target, and the reflected waves were used to estimate skin surface displacement associated with respiration. The results revealed periodic skin surface displacement, and the estimated respiratory rates weres within the reported range of respiratory rates for rhesus macaques. These results suggest the potential applicability of millimeter-wave radar for noncontact respiration monitoring in outdoor-living macaques without anesthesia or immobilization. The continued advancement of noncontact vital measurement technology will contribute to understanding primate mental and physical dynamics during their daily life.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":"86 9","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/ajp.23661","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141475741","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Evidence for female dominance in the Milne-Edwards' sportive lemur (Lepilemur edwardsi)","authors":"Solofonirina Rasoloharijaona, Blanchard Randrianambinina, Ute Radespiel","doi":"10.1002/ajp.23658","DOIUrl":"10.1002/ajp.23658","url":null,"abstract":"<p>Female dominance over males is more frequent in Malagasy lemurs than in other primate clades, but patterns of female–male dominance vary among species, and few data are available for one particularly species-rich genus, <i>Lepilemur</i>. We investigated the types, temporal distribution, and outcome of female–male agonistic conflicts in the Milne-Edwards' sportive lemur (<i>Lepilemur edwardsi</i>). Ten <i>L. edwardsi</i> belonging to five social units were equipped with radio collars and observed during 79 focal follows between May and November 1998. We quantified agonistic conflicts, monthly conflict rates, and documented the winner and context for all conflicts. Female–male agonistic conflicts (<i>N</i> = 162) occurred at a mean rate of 0.21 conflicts/hour within groups. Agonistic conflicts peaked during the birth season and occurred mostly in unknown or infant proximity contexts. Females won 96% of all decided agonistic conflicts (<i>N</i> = 154). Other outcomes occurred only when females were with infants during the birth season. In that context, one female sometimes withdrew from her pair partner, and another female withdrew or fled from an extra-group male whose attacks eventually led to infanticide. Our results suggest female dominance in pair-living <i>L. edwardsi</i>. We hypothesize that elevated female aggression may convey fitness benefits to female <i>Lepilemur</i> because it generally allows females to intervene quickly and efficiently on behalf of their infants against nonfather males who may approach the newborn infants when they are parked in vegetation.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":"86 9","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-06-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/ajp.23658","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141454660","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Eduardo A. Diaz, Carolina Sáenz, Francisco Cabrera, Javier Rodríguez, Mateo Carvajal, Verónica Barragán
{"title":"COVID-19 in a common woolly monkey (Lagothrix lagothricha): First evidence of fatal outcome in a nonhuman primate after natural SARS-CoV-2 infection","authors":"Eduardo A. Diaz, Carolina Sáenz, Francisco Cabrera, Javier Rodríguez, Mateo Carvajal, Verónica Barragán","doi":"10.1002/ajp.23654","DOIUrl":"10.1002/ajp.23654","url":null,"abstract":"<p>Coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), was declared a pandemic by the World Health Organization in March 2020. Since then, viral spread from humans to animals has occurred worldwide. Nonhuman primates (NHPs) have been found to be susceptible to reverse-zoonosis transmission of SARS-CoV-2, but initial research suggested that platyrrhine primates are less susceptible than catarrhine primates. Here we report the natural SARS-CoV-2 infection of a common woolly monkey (<i>Lagothrix lagothricha</i>) from a wildlife rehabilitation center in Ecuador. The course of the disease, the eventual death of the specimen, and the pathological findings are described. Our results show the susceptibility of a new platyrrhine species to SARS-CoV-2 and provide evidence for the first time of a COVID-19-associated death in a naturally infected NHP. The putative route of transmission from humans, and implications for captive NHPs management, are also discussed. Given that common woolly monkeys are at risk of extinction in Ecuador, further understanding of the potential threat of SARS-CoV-2 to their health should be a conservation priority. A One Health approach is the best way to protect NHPs from a new virus in the same way that we would protect the human population.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":"86 8","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-06-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141454659","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Himani Nautiyal, Valéria Romano, Hiroyuki Tanaka, Michael A. Huffman
{"title":"Female social dynamics as viewed from grooming networks in the Central Himalayan Langur (Semnopithecus schistaceus)","authors":"Himani Nautiyal, Valéria Romano, Hiroyuki Tanaka, Michael A. Huffman","doi":"10.1002/ajp.23655","DOIUrl":"10.1002/ajp.23655","url":null,"abstract":"<p>Enhanced survival and reproduction are associated with an individual's direct and indirect social connections with members of a group. Yet, the role of these connections is little known in a vast range of primate species. We studied female Central Himalayan Langur (CHL) to investigate the link between four specific attributes (dominance rank, age, genetic relatedness, and the presence of females carrying infants) and a female's direct and indirect social relationships. By analyzing grooming networks, we revealed different behavioral strategies: high-ranking females form relationships with many females (high degree), whereas females with dependent infants have strong relationships (high strength and eigenvector). Subadult females are important individuals that hold the social network together (high betweenness), while an immigrant female strategy is to integrate herself into the group by forming strong bonds with females who themselves have strong bonds (high eigenvector). Our study sheds light on how behavioral strategies shape female CHL grooming networks, which may help them to secure fitness and survival advantages.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":"86 8","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-06-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141454661","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Laura Grieneisen, Allison Hays, Erica Cook, Ran Blekhman, Stacey Tecot
{"title":"Temporal patterns of gut microbiota in lemurs (Eulemur rubriventer) living in intact and disturbed habitats in a novel sample type","authors":"Laura Grieneisen, Allison Hays, Erica Cook, Ran Blekhman, Stacey Tecot","doi":"10.1002/ajp.23656","DOIUrl":"10.1002/ajp.23656","url":null,"abstract":"<p>The gut microbiome is a plastic phenotype; gut microbial composition is highly variable across an individual host's lifetime and between host social groups, and this variation has consequences for host health. However, we do not yet fully understand how longitudinal microbial dynamics and their social drivers may be influenced by ecological stressors, such as habitat degradation. Answering these questions is difficult in most wild animal systems, as it requires long-term collections of matched host, microbiome, and environmental trait data. To test if temporal and social influences on microbiome composition differ by the history of human disturbance, we leveraged banked, desiccated fecal samples collected over 5 months in 2004 from two ecologically distinct populations of wild, red-bellied lemurs (<i>Eulemur rubriventer</i>) that are part of a long-term study system. We found that social group explained more variation in microbiome composition than host population membership did, and that temporal variation in common microbial taxa was similar between populations, despite differences in history of human disturbance. Furthermore, we found that social group membership and collection month were both more important than individual lemur identity. Taken together, our results suggest that synchronized environments use can lead to synchronized microbial dynamics over time, even between habitats of varying quality, and that desiccated samples could become a viable approach for studying primate gut microbiota. Our work opens the door for other projects to utilize historic biological sample data sets to answer novel temporal microbiome questions in an ecological context.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":"87 1","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-06-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/ajp.23656","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141316576","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pu-Zhen Xie, Yu-Xuan Fan, Colin Chapman, Chi Ma, Cheng-Feng Wu, Ping Hu, Liu-Liu Hu, Peng-Fei Fan
{"title":"Determinants of macaques' space use: A test for the ecological constraints model using GPS collars","authors":"Pu-Zhen Xie, Yu-Xuan Fan, Colin Chapman, Chi Ma, Cheng-Feng Wu, Ping Hu, Liu-Liu Hu, Peng-Fei Fan","doi":"10.1002/ajp.23636","DOIUrl":"10.1002/ajp.23636","url":null,"abstract":"<p>As a central topic in Behavioral Ecology, animal space use involves dynamic responses to social and ecological factors. We collared 22 rhesus macaques (<i>Macaca mulatta</i>) from six groups on Neilingding Island, China, and collected 80,625 hourly fixes over a year. Using this high-resolution location data set, we quantified the macaques' space use at the individual level and tested the ecological constraints model while considering various environmental and human interfering factors. As predicted by the ecological constraints model, macaques in larger groups had longer daily path lengths (DPLs) and larger home ranges. We found an inverted U-shape relationship between mean daily temperatures and DPLs, indicating that macaques traveled farther on mild temperature days, while they decreased DPLs when temperatures were too high or too low. Anthropogenic food subsidies were positively correlated to DPLs, while the effect of rainfall was negative. Macaques decreased their DPLs and core areas when more flowers and less leaves were available, suggesting that macaques shifted their space use patterns to adapt to the seasonal differences in food resources. By applying GPS collars on a large number of individuals living on a small island, we gained valuable insights into within-group exploitation competition in wild rhesus macaques.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":"86 8","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-06-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141198455","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Aylén D. Giannetti-Domínguez, Ariadna Rangel-Negrín, Alejandro Coyohua-Fuentes, Pedro A. D. Dias
{"title":"Leadership and the finder's advantage in mantled howler monkeys","authors":"Aylén D. Giannetti-Domínguez, Ariadna Rangel-Negrín, Alejandro Coyohua-Fuentes, Pedro A. D. Dias","doi":"10.1002/ajp.23651","DOIUrl":"10.1002/ajp.23651","url":null,"abstract":"<p>Leading collective movements and arriving first at feeding sites may improve food acquisition. Specifically, the first individual to discover and exploit a feeding site may gain a feeding advantage known as the “finder's advantage.” The aim of this research was to verify if the probability of leading group movements to feeding sites in mantled howler monkeys (<i>Alouatta palliata</i>) varied by sex and reproductive status, and whether finders had higher foraging success than followers. We studied 18 adult individuals from two groups in La Flor de Catemaco over a year (978 h), and sampled group movements (<i>n</i> = 211) and foraging behavior (<i>n</i> = 215 feeding episodes). Gestating females were leaders and finders of group movements to feeding sites more often than expected but were also replaced in the leading position more frequently than individuals of other sex/reproductive states. Feeding behavior was not influenced by the order of arrival at feeding sites per se, but gestating females had higher food intake rate, bite rate, and feeding time when arriving earlier (i.e., occupying front group positions) than later. Therefore, leadership and the finder's advantage occur in this species and are probably employed by gestating females to maintain their energetic condition.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":"86 8","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-05-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141157378","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jenny E. Jaffe, Sonja Metzger, Kerstin Mätz-Rensing, Alexis Ribas, Roman M. Wittig, Fabian H. Leendertz
{"title":"Oesophagostomum stephanostomum causing parasitic granulomas in wild chimpanzees (Pan troglodytes verus) of Taï National Park, Côte d'Ivoire","authors":"Jenny E. Jaffe, Sonja Metzger, Kerstin Mätz-Rensing, Alexis Ribas, Roman M. Wittig, Fabian H. Leendertz","doi":"10.1002/ajp.23652","DOIUrl":"10.1002/ajp.23652","url":null,"abstract":"<p>Nematodes belonging to the genus <i>Oesophagostomum</i> frequently infect wild chimpanzees (<i>Pan troglodytes</i>) across widely separated field sites. Nodular lesions (granulomas) containing <i>Oesophagostomum</i> are commonly seen in the abdomen of infected chimpanzees post-mortem. At Taï National Park, Côte d'Ivoire, previous studies have identified larvae of a variety of <i>Oesophagostomum</i> spp. in wild chimpanzee stool, based on sequencing of larval DNA, and nodular lesions associated with <i>Oesophagostomum</i>, identified morphologically to the genus level but not sequenced. Here we present three recent cases of parasitic granulomas found post-mortem in chimpanzees at Taï. We complement descriptions of gross pathology, histopathology and parasitology with PCR and sequencing of DNA isolated from the parasitic nodules and from adult worms found inside the nodules. In all three cases, we identify <i>Oesophagostomum stephanostomum</i> as the causative agent. The sequences from this study were identical to the only other published sequences from nodules in nonhuman primates—those from the wild chimpanzees of Gombe, Tanzania.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":"86 8","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-05-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/ajp.23652","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141160844","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"First noncontact millimeter-wave radar measurement of heart rate in great apes: Validation in chimpanzees (Pan troglodytes)","authors":"Takuya Matsumoto, Itsuki Iwata, Takuya Sakamoto, Satoshi Hirata","doi":"10.1002/ajp.23633","DOIUrl":"10.1002/ajp.23633","url":null,"abstract":"<p>Heart rate is a crucial vital sign and a valuable indicator for assessing the physical and psychological condition of a target animal. Heart rate contributes to (1) fundamental information for cognitive research, (2) an indicator of psychological and physical stress, and (3) improving the animal welfare of captive animals, especially in nonhuman primate studies. Heart rate has been measured using a contact-type device; however, the device burdens the target animals and that there are risks associated with anesthesia during installation. This study explores the application of heartbeat measurement techniques using millimeter-wave radar, primarily developed for humans, as a remote and noninvasive method for measuring the heart rate of nonhuman primates. Through a measurement test conducted on two chimpanzees, we observed a remarkable correspondence between the peak frequency spectrum of heart rate estimated using millimeter-wave radar and the mean value obtained from electrocardiograph data, thereby validating the accuracy of the method. To the best of our knowledge, this is the first demonstration of the precise measurement of great apes' heart rate using millimeter-wave radar technology. Compared to heart rate measurement using video analysis, the method using millimeter-wave radar has the advantage that it is less susceptible to weather and lighting conditions and that measurement techniques for multiple individuals have been developed for human subjects, while its disadvantage is that validation of measurement from long distances has not been completed. Another disadvantage common to both methods is that measurement becomes difficult when the movement of the target individual is large. The possibility of noncontact measurement of heart rate in wild and captive primates will undoubtedly open up a new research area while taking animal welfare into consideration.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":"86 8","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-05-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/ajp.23633","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141075303","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Correcting the record: Phonetic potential of primate vocal tracts and the legacy of Philip Lieberman (1934−2022)","authors":"Axel G. Ekström","doi":"10.1002/ajp.23637","DOIUrl":"10.1002/ajp.23637","url":null,"abstract":"<p>The phonetic potential of nonhuman primate vocal tracts has been the subject of considerable contention in recent literature. Here, the work of Philip Lieberman (1934−2022) is considered at length, and two research papers—both purported challenges to Lieberman's theoretical work—and a review of Lieberman's scientific legacy are critically examined. I argue that various aspects of Lieberman's research have been consistently misinterpreted in the literature. A paper by Fitch et al. overestimates the would-be “speech-ready” capacities of a rhesus macaque, and the data presented nonetheless supports Lieberman's principal position—that nonhuman primates cannot articulate the full extent of human speech sounds. The suggestion that no vocal anatomical evolution was necessary for the evolution of human speech (as spoken by all normally developing humans) is not supported by phonetic or anatomical data. The second challenge, by Boë et al., attributes vowel-like qualities of baboon calls to articulatory capacities based on audio data; I argue that such “protovocalic” properties likely result from disparate articulatory maneuvers compared to human speakers. A review of Lieberman's scientific legacy by Boë et al. ascribes a view of speech evolution (which the authors term “laryngeal descent theory”) to Lieberman, which contradicts his writings. The present article documents a pattern of incorrect interpretations of Lieberman's theoretical work in recent literature. Finally, the apparent trend of vowel-like formant dispersions in great ape vocalization literature is discussed with regard to Lieberman's theoretical work. The review concludes that the “Lieberman account” of primate vocal tract phonetic capacities remains supported by research: the ready articulation of fully human speech reflects species-unique anatomy.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":"86 8","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-05-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/ajp.23637","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140915594","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}