Elodie Freymann, João d'Oliveira Coelho, Catherine Hobaiter, Michael A. Huffman, Geresomu Muhumuza, Klaus Zuberbühler, Susana Carvalho
{"title":"Applying collocation and APRIORI analyses to chimpanzee diets: Methods for investigating nonrandom food combinations in primate self-medication","authors":"Elodie Freymann, João d'Oliveira Coelho, Catherine Hobaiter, Michael A. Huffman, Geresomu Muhumuza, Klaus Zuberbühler, Susana Carvalho","doi":"10.1002/ajp.23603","DOIUrl":"10.1002/ajp.23603","url":null,"abstract":"<p>Identifying novel medicinal resources in chimpanzee diets has historically presented challenges, requiring extensive behavioral data collection and health monitoring, accompanied by expensive pharmacological analyses. When putative therapeutic self-medicative behaviors are observed, these events are often considered isolated occurrences, with little attention paid to other resources ingested in combination. For chimpanzees, medicinal resource combinations could play an important role in maintaining well-being by tackling different symptoms of an illness, chemically strengthening efficacy of a treatment, or providing prophylactic compounds that prevent future ailments. We call this concept the self-medicative resource combination hypothesis. However, a dearth of methodological approaches for holistically investigating primate feeding ecology has limited our ability to identify nonrandom resource combinations and explore potential synergistic relationships between medicinal resource candidates. Here we present two analytical tools that test such a hypothesis and demonstrate these approaches on feeding data from the Sonso chimpanzee community in Budongo Forest, Uganda. Using 4 months of data, we establish that both collocation and APRIORI analyses are effective exploratory tools for identifying binary combinations, and that APRIORI is effective for multi-item rule associations. We then compare outputs from both methods, finding up to 60% agreement, and propose APRIORI as more effective for studies requiring control over confidence intervals and those investigating nonrandom associations between more than two resources. These analytical tools, which can be extrapolated across the animal kingdom, can provide a cost-effective and efficient method for targeting resources for further pharmacological investigation, potentially aiding in the discovery of novel medicines.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2024-01-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/ajp.23603","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139641452","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":"Scientific activism to protect the world's primates and their environments from extinction: Introduction to the special issue","authors":"Paul A. Garber, Francine Dolins, Susan Lappan","doi":"10.1002/ajp.23601","DOIUrl":"10.1002/ajp.23601","url":null,"abstract":"<p>Nonhuman primates and their habitats are facing an impending extinction crisis. Approximately 69% of primate species are listed by the International Union for Conservation of Nature as threatened and 93% have declining populations. Human population growth (expected to reach 10.9 billion by the year 2100), the unsustainable demands of a small number of consumer nations for forest-risk commodities, deforestation and habitat conversion, the expansion of roads and rail networks, cattle ranching, the hunting and trapping of wild primate populations, and the potential spread of infectious diseases are among the primary drivers of primate population decline. Climate change will only exacerbate the current situation. The time to act to protect primate populations is now! In this special issue of the <i>American Journal of Primatology</i>, we present a series of commentaries, formulated as “Action Letters.” These are designed to educate and inform primatologists, conservation biologists, wildlife ecologists, political leaders, and global citizens about the conservation challenges faced by particular primate taxa and particular world regions, and present examples of specific actions that one can take, individually and collectively, to promote the persistence of wild primate populations and environmental justice for local human populations and impacted ecological communities. As scientists, researchers, and educators, primatologists are in a unique position to lead local, national, and international efforts to protect biodiversity. In this special issue, we focus on primates of the Brazilian Amazon, lemurs of northeast Madagascar, Temminck's red colobus monkey (<i>Piliocolobus badius temminckii</i>), night monkeys (<i>Aotus spp</i>.), long-tailed macaques (<i>Macaca fascicularis</i>), the primate pet trade, and professional capacity building to foster conservation awareness and action. We encourage primatologists, regardless of their research focus, to engage in both advocacy and activism to protect wild primate populations worldwide.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2024-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139569472","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}
Juliane Damm, Filippo Aureli, Ariadna Rangel-Negrín, Miriam Barradas-Moctezuma, Pedro A. D. Dias
{"title":"Analytical and biological validation of a noninvasive measurement of glucocorticoid metabolites in feces of Geoffroy's spider monkeys (Ateles geoffroyi)","authors":"Juliane Damm, Filippo Aureli, Ariadna Rangel-Negrín, Miriam Barradas-Moctezuma, Pedro A. D. Dias","doi":"10.1002/ajp.23598","DOIUrl":"10.1002/ajp.23598","url":null,"abstract":"<p>We report on an analytical and biological validation of a commercial cortisol enzyme immunoassay (EIA) to measure glucocorticoids (GC) in feces of Geoffroy's spider monkeys (<i>Ateles geoffroyi</i>). Validation of endocrinological methods for each sample matrix and study species is crucial to establish that the methods produce reliable results. For the analytical validation of the EIA, we assessed parallelism, accuracy, and precision. We carried out a biological validation based on three well-studied GC patterns with the following predictions: (1) increased fecal GC metabolite (fGCM) concentrations after veterinary intervention; (2) increased fGCM concentrations during early morning hours; and (3) higher fGCM concentrations during gestation than in other female reproductive states. For the first prediction, we sampled feces of two zoo-housed females 2 days before, the day of, and 2 days after a veterinary intervention. For the second prediction, we analyzed 284 fecal samples collected from 12 wild males using a linear mixed model (LMM). For the third prediction, we analyzed 269 fecal samples of eight wild females using an LMM. Analytical validation revealed that the EIA showed parallelism, was accurate, and precise within each assay. However, there was elevated variation in between-assay precision. The biological validation supported all predictions: (1) the two zoo-housed females showed a substantial increase in fGCM concentrations 2.5 and 11 h after veterinary intervention; (2) there was a negative effect of sample collection time on fGCM concentrations (i.e., higher concentrations during early morning); (3) gestating females had significantly higher fGCM concentrations than lactating females. Thus, we analytically validated the commercial EIA and, despite between-assay variation, we were able to find three biologically relevant GC signals in captive and wild settings, and in males and females. We are therefore confident that the method can be used to noninvasively address behavioral endocrinology questions in Geoffroy's spider monkeys.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2024-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139519590","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}
María Fernanda Alvarez-Velazquez, Mauricio González-Jáuregui, Sergio Albino Miranda, Genoveva Rosano-Ortega, Colin A. Chapman, Juan Carlos Serio-Silva
{"title":"Lead exposure and its relationship with fecal cortisol levels in black howler monkeys (Alouatta pigra)","authors":"María Fernanda Alvarez-Velazquez, Mauricio González-Jáuregui, Sergio Albino Miranda, Genoveva Rosano-Ortega, Colin A. Chapman, Juan Carlos Serio-Silva","doi":"10.1002/ajp.23600","DOIUrl":"10.1002/ajp.23600","url":null,"abstract":"<p>Efficiently detecting early environmental threats to wildlife is vital for conservation. Beyond obvious dangers like habitat loss or deforestation, our study focuses on one of the most hazardous toxic metals for wildlife: lead (Pb). Pb is a widespread, cumulative, and insidious environmental pollutant that can trigger a wide range of physiological, biochemical, and behavioral disorders. In fact, Pb can cause permanent dysfunction of the major stress system, the hypothalamic pituitary adrenal (HPA) axis. We analyzed Pb and cortisol concentrations in fecal samples from <i>Alouatta pigra</i> in southern Mexico. Fecal samples were collected across six sites categorized as free-ranging (<i>n</i> = 65; conserved and disturbed) and from captive animals (<i>n</i> = 58). Additionally, we collected soil samples (<i>n</i> = 35). We found that Pb was present in 28% of fecal samples and 83% of soil samples. There was a positive relation between fecal and soil Pb levels, and fecal Pb concentration was negatively associated with cortisol levels. However, the claim of Pb being a direct interference with HPA axis requires further investigation. Given our findings, assessing wildlife exposure can be a valuable tool for understanding potential Pb exposure levels in the environment and its possible implications for human health. It can also serve as an early warning system of these consequences.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2024-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139541071","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}
Kathelijne Koops, Walter Akankwasa, Henry Didier Camara, Maegan Fitzgerald, Alex Keir, Gnan Mamy, Tetsuro Matsuzawa, Hella Péter, Kizza Vicent, Klaus Zuberbühler, Catherine Hobaiter
{"title":"Flexible grouping patterns in a western and eastern chimpanzee community","authors":"Kathelijne Koops, Walter Akankwasa, Henry Didier Camara, Maegan Fitzgerald, Alex Keir, Gnan Mamy, Tetsuro Matsuzawa, Hella Péter, Kizza Vicent, Klaus Zuberbühler, Catherine Hobaiter","doi":"10.1002/ajp.23593","DOIUrl":"10.1002/ajp.23593","url":null,"abstract":"<p>Primate social organizations, or grouping patterns, vary significantly across species. Behavioral strategies that allow for flexibility in grouping patterns offer a means to reduce the costs of group living. Chimpanzees (<i>Pan troglodytes</i>) have a fission-fusion social system in which temporary subgroups (“parties”) change in composition because of local socio-ecological conditions. Notably, western chimpanzees (<i>P. t. verus</i>) are described as showing a higher degree of bisexual bonding and association than eastern chimpanzees, and eastern female chimpanzees (<i>P. t. schweinfurthii</i>) are thought to be more solitary than western female chimpanzees. However, reported comparisons in sociality currently depend on a small number of study groups, particularly in western chimpanzees, and variation in methods. The inclusion of additional communities and direct comparison using the same methods are essential to assess whether reported subspecies differences in sociality hold in this behaviorally heterogeneous species. We explored whether sociality differs between two communities of chimpanzees using the same motion-triggered camera technology and definitions of social measures. We compare party size and composition (party type, sex ratio) between the western Gahtoy community in the Nimba Mountains (Guinea) and the eastern Waibira community in the Budongo Forest (Uganda). Once potential competition for resources such as food and mating opportunities were controlled for, subspecies did not substantially influence the number of individuals in a party. We found a higher sex-ratio, indicating more males in a party, in Waibira; this pattern was driven by a greater likelihood in Gahtoy to be in all-female parties. This finding is the opposite of what was expected for eastern chimpanzees, where female-only parties are predicted to be more common. Our results highlight the flexibility in chimpanzee sociality, and caution against subspecies level generalizations.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2024-01-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/ajp.23593","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139511618","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}
Carly H. Batist, Emmanuel Dufourq, Lorène Jeantet, Mendrika N. Razafindraibe, Francois Randriamanantena, Andrea L. Baden
{"title":"An integrated passive acoustic monitoring and deep learning pipeline for black-and-white ruffed lemurs (Varecia variegata) in Ranomafana National Park, Madagascar","authors":"Carly H. Batist, Emmanuel Dufourq, Lorène Jeantet, Mendrika N. Razafindraibe, Francois Randriamanantena, Andrea L. Baden","doi":"10.1002/ajp.23599","DOIUrl":"10.1002/ajp.23599","url":null,"abstract":"<p>The urgent need for effective wildlife monitoring solutions in the face of global biodiversity loss has resulted in the emergence of conservation technologies such as passive acoustic monitoring (PAM). While PAM has been extensively used for marine mammals, birds, and bats, its application to primates is limited. Black-and-white ruffed lemurs (<i>Varecia variegata</i>) are a promising species to test PAM with due to their distinctive and loud roar-shrieks. Furthermore, these lemurs are challenging to monitor via traditional methods due to their fragmented and often unpredictable distribution in Madagascar's dense eastern rainforests. Our goal in this study was to develop a machine learning pipeline for automated call detection from PAM data, compare the effectiveness of PAM versus in-person observations, and investigate diel patterns in lemur vocal behavior. We did this study at Mangevo, Ranomafana National Park by concurrently conducting focal follows and deploying autonomous recorders in May–July 2019. We used transfer learning to build a convolutional neural network (optimized for recall) that automated the detection of lemur calls (57-h runtime; recall = 0.94, F1 = 0.70). We found that PAM outperformed in-person observations, saving time, money, and labor while also providing re-analyzable data. Using PAM yielded novel insights into <i>V. variegata</i> diel vocal patterns; we present the first published evidence of nocturnal calling. We developed a graphic user interface and open-sourced data and code, to serve as a resource for primatologists interested in implementing PAM and machine learning. By leveraging the potential of this pipeline, we can address the urgent need for effective primate population surveys to inform conservation strategies.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2024-01-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/ajp.23599","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139510191","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":"Cortisol levels across the lifespan in common marmosets (Callithrix jacchus)","authors":"Matthew Lopez, Amaya Seidl, Kimberley A. Phillips","doi":"10.1002/ajp.23597","DOIUrl":"10.1002/ajp.23597","url":null,"abstract":"<p>Human aging is associated with senescence of the hypothalamic–pituitary–adrenal (HPA) axis, leading to progressive dysregulation characterized by increased cortisol exposure. This key hormone is implicated in the pathogenesis of many age-related diseases. Common marmosets <i>(Callithrix jacchus)</i> display a wide spectrum of naturally occurring age-related pathologies that compare similarly to humans and are increasingly used as translational models of aging and age-related disease. Whether the marmoset HPA axis also shows senescence with increasing age is unknown. We analyzed hair cortisol concentration (HCC) across the lifespan of 50 captive common marmosets, ranging in age from approximately 2 months–14.5 years, via a cross-sectional design. Samples were processed and analyzed for cortisol using enzyme immunoassay. HCC ranged from 1416 to 15,343 pg/mg and was negatively correlated with age. We found significant main effects of age group (infant, adolescent, adult, aged, very aged) and sex on HCC, and no interaction effects. Infants had significantly higher levels of HCC compared with all other age groups. Females had higher HCC than males. There was no interaction between age and sex. These results suggest marmosets do not show dysregulation of the HPA axis with increasing age, as measured via HCC.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2024-01-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139490441","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}
Tiago Falótico, Tatiane Valença, Michele P. Verderane, Beatriz C. Santana, Giulia Sirianni
{"title":"Mapping nut-cracking in a new population of wild capuchin monkeys (Sapajus libidinosus) at Ubajara National Park, Brazil","authors":"Tiago Falótico, Tatiane Valença, Michele P. Verderane, Beatriz C. Santana, Giulia Sirianni","doi":"10.1002/ajp.23595","DOIUrl":"10.1002/ajp.23595","url":null,"abstract":"<p>Populations of bearded capuchin monkeys (<i>Sapajus libidinosus</i>) vary in their tool use behaviors, with some of this divergence regarded as culturally determined. The use of stone tools, primarily to crack open encased foods, is widespread among bearded capuchins living in dry habitats (<i>Caatinga</i> and <i>Cerrado</i>). Significant diversity in targets, processed foods, material, and size of tools is observed across populations. However, so far, only a few sites have been systematically studied, and we are still distant from a representative picture of the range of variation in capuchins’ culture. In this study, we did a systematic assessment of stone tool use sites in the Ubajara National Park (UNP), in the <i>Caatinga</i> region of Ceará, Brazil, recording and measuring stone tools, processed foods, and available lithic resources as part of an extensive comparative research, the CapCult project. We found indirect and direct evidence that capuchin monkeys at UNP customarily use hammerstones and anvils to process at least two species of palm nuts, macauba (<i>Acrocomia aculeata</i>) and the harder babaçu (<i>Attalea speciosa</i>). Most of the anvils were rock surfaces and had leftovers of only one palm nut species. The hammerstones used to process both palm nuts were not significantly different in weight, although the ones used for <i>Ac. aculeata</i> were longer. We found a higher frequency of nut-cracking sites in the drier lowland area of the park, reflecting differences in the density of the most common palm species, <i>Ac. aculeata</i>, and availability of raw stone material. The stone tool use observed in UNP is within the scope of previously reported in savannah capuchin populations. Our study widens the knowledge of stone tool-use diversity in wild capuchin monkeys, which could contribute to shaping conservation policy, including cultural traits.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2024-01-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/ajp.23595","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139465577","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}
Sylvia Atsalis, Marlene Gravenberch, Marilyn A. Norconk
{"title":"Mentorship and professional growth for conservationists in primate-range countries","authors":"Sylvia Atsalis, Marlene Gravenberch, Marilyn A. Norconk","doi":"10.1002/ajp.23592","DOIUrl":"10.1002/ajp.23592","url":null,"abstract":"<p>Ways to support professional capacity of emerging conservation leadership in primate range countries.\u0000 <figure>\u0000 <div><picture>\u0000 <source></source></picture><p></p>\u0000 </div>\u0000 </figure></p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2024-01-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139416112","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}
Alexander J. Pritchard, John P. Capitanio, Laura Del Rosso, Brenda McCowan, Jessica J. Vandeleest
{"title":"Repeatability of measures of behavioral organization over two years in captive infant rhesus macaques, Macaca mulatta","authors":"Alexander J. Pritchard, John P. Capitanio, Laura Del Rosso, Brenda McCowan, Jessica J. Vandeleest","doi":"10.1002/ajp.23591","DOIUrl":"10.1002/ajp.23591","url":null,"abstract":"<p>Individual differences of infant temperament have been associated with future health outcomes that provide explanatory power beyond adult personality. Despite the importance of such a metric, our developmental understanding of personality-like traits is poor. Therefore, we examined whether young primates show consistency in personality traits throughout development. We replicated a Biobehavioral Assessment (BBA) at three time periods: 3–4 months, 1 year, and 2 years of age in 47 rhesus macaque (<i>Macaca mulatta</i>) subjects from large mixed-sex outdoor social housing units at the California National Primate Research Center. We report results for tests focused on responses and adaptation to the temporary separation and relocation, responses to a threatening stimulus, and ratings of overall temperament. We found consistently repeatable associations in measures of Emotionality; these associations were stronger in males, but also present in females, and broadly consistent between Years 1 and 2. We also explored whether behavioral responses to this experimental relocation might be influenced by their experience being relocated for other reasons (i.e., hospitalizations) as individuals' responses might be influenced by similar experiences to the BBA procedure. Only locomotion, during one of the assessments, was associated with past hospitalization events. Overall, repeatability in Emotionality-associated behaviors was evident across the 2 years, in both sexes. We did, however, find evidence of the emergence of sex differences via differentiated expression of behavioral responses during the BBA. We emphasize that there is likely contextual nuance in the use of these BBA factor-associated behaviors. Further research is required to determine whether and how shifts occur in underlying factor structure and the expression of associated behaviors.</p>","PeriodicalId":7662,"journal":{"name":"American Journal of Primatology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2024-01-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/ajp.23591","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139428845","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}