Percorrer por autor "Carvalho, Susana"
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- A Home Range Approach to the Ecology of Site Selection in Wild Chimpanzee Nut-CrackingPublication . Almeida-Warren, Katarina; Matsuzawa, Tetsuro; Carvalho, Susana
- A missing piece of the Papio puzzle: Gorongosa baboon phenostructure and intrageneric relationshipsPublication . Martinez, Felipe I.; Capelli, Cristian; Ferreira da Silva, Maria J.; Aldeias, Vera; Alemseged, Zeresenay; Archer, William; Bamford, Marion; Biro, Dora; Bobe, Rene; Braun, David R.; Habermann, Jörg M.; Luedecke, Tina; Madiquida, Hilario; Mathe, Jacinto; Negash, Enquye; Paulo, Luis M.; Pinto, Maria; Stalmans, Marc; Tata, Frederico; Carvalho, SusanaMost authors recognize six baboon species: hamadryas (Papio hamadryas), Guinea (Papio papio), olive (Papio anubis), yellow (Papio cynocephalus), chacma (Papio ursinus), and Kinda (Papio kindae). However, there is still debate regarding the taxonomic status, phylogenetic relationships, and the amount of gene flow occurring between species. Here, we present ongoing research on baboon morphological diversity in Gorongosa National Park (GNP), located in central Mozambique, south of the Zambezi River, at the southern end of the East African Rift System. The park exhibits outstanding ecological diversity and hosts more than 200 baboon troops. Gorongosa National Park baboons have previously been classified as chacma baboons (P. ursinus). In accordance with this, two mtDNA samples from the park have been placed in the same mtDNA Glade as the northern chacma baboons. However, GNP baboons exhibit morphological features common in yellow baboons (e.g., yellow fur color), suggesting that parapatric gene flow between chacma and yellow baboons might have occurred in the past or could be ongoing. We investigated the phenostructure of the Gorongosa baboons using two approaches: 1) description of external phenotypic features, such as coloration and body size, and 2) 3D geometric morphometric analysis of 43 craniofacial landmarks on 11 specimens from Gorongosa compared to a pan-African sample of 352 baboons. The results show that Gorongosa baboons exhibit a mosaic of features shared with southern P. cynocephalus and P. ursinus griseipes. The GNP baboon phenotype fits within a geographic clinal pattern of replacing allotaxa. We put forward the hypothesis of either past and/or ongoing hybridization between the gray-footed chacma and southern yellow baboons in Gorongosa or an isolation-by-distance scenario in which the GNP baboons are geographically and morphologically intermediate. These two scenarios are not mutually exclusive. We highlight the potential of baboons as a useful model to understand speciation and hybridization in early human evolution. (C) 2019 Elsevier Ltd. All rights reserved.
- The adaptive role of bark in the diet of budongo chimpanzees (Pan troglodytes schweinfurthii)Publication . Freymann, E.; Badihi, G.; Hobaiter, C.; Huffman, M. A.; Muhumuza, G.; Orbell, S.; Sempebwa, D.; Robert Yikii, E.; Zuberbühler, K.; Carvalho, SusanaThe ingestion of bark has been observed across the animal kingdom and is well documented in free-ranging chimpanzees. Thus far, the best-supported hypothesis for the adaptive function of this behavior is the fallback food hypothesis, which asserts that chimpanzees consume bark and cambium when preferred foods are scarce. However, alternative explanations exist, including the essential nutrient and mineral hypothesis, the self-medication hypothesis, and the stressed-tree hypothesis. We tested whether the fallback food hypothesis can explain bark-feeding across two communities of Eastern chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda. We used 13 years of the site's long-term behavioral data, 5 years of food availability data, and 8 months of direct and indirect observations. We also conducted eight 400-m line transects to collect data on the distribution of tree species across community home ranges. We employed several analyses, including Pearson correlation tests, qualitative comparisons of descriptive data and heat maps, and interpretation of behavioral anecdotes. We found varying patterns of bark-feeding seasonality across tree species, with bark-feeding on several species showing no correlation with food scarcity. We also identified differences in the amounts of bark targeted between tree species and report anecdotal evidence of chimpanzees prioritizing bark over high-value foods. Lastly, we found that bark-feeding on certain species disproportionally occurs far from community core areas, despite relative abundance of these species within the home range. As a result, we argue that the fallback food hypothesis cannot explain bark-feeding across all tree species. Instead, we present supporting evidence for several alternative hypotheses, including self-medication, thereby challenging the widely accepted function of this behavior.
- Automated audiovisual behavior recognition in wild primatesPublication . Bain, Max; Nagrani, Arsha; Schofield, Daniel; Berdugo, Sophie; Bessa, Joana; Owen, Jake; Hockings, Kimberley J.; Matsuzawa, Tetsuro; Hayashi, Misato; Biro, Dora; Carvalho, Susana; Zisserman, AndrewThe field of ethology seeks to understand animal behavior from both mechanistic and functional perspectives and to identify the various genetic, developmental, ecological, and social drivers of behavioral variation in the wild (1). It is increasingly becoming a data-rich science: Technological advances in data collection, including biologgers, camera traps, and audio recorders, now allow us to capture animal behavior in an unprecedented level of detail (2). In particular, large data archives including both audio and visual information have immense potential to measure individual- and population-level variation as well as ontogenetic and cultural changes in behavior that may span large temporal and spatial scales. However, this potential often goes untapped: The training and human effort required to process large volumes of video data continue to limit the scale and depth at which behavior can be analyzed. Automating the measurement of behavior can transform ethological research, open up large-scale video archives for detailed interrogation, and be a powerful tool to monitor and protect threatened species in the wild. With rapid advances in deep learning, the novel field of computational ethology is quickly emerging at the intersection of computer science, engineering, and biology, using computer vision algorithms to process large volumes of data (3).
- Automated face recognition using deep neural networks produces robust primate social networks and sociality measuresPublication . Schofield, Daniel P.; Albery, Gregory F.; Firth, Josh A.; Mielke, Alexander; Hayashi, Misato; Matsuzawa, Tetsuro; Biro, Dora; Carvalho, SusanaLongitudinal video archives of behaviour are crucial for examining how sociality shifts over the lifespan in wild animals. New approaches adopting computer vision technology hold serious potential to capture interactions and associations between individuals in video at large scale; however, such approaches need a priori validation, as methods of sampling and defining edges for social networks can substantially impact results.Here, we apply a deep learning face recognition model to generate association networks of wild chimpanzees using 17 years of a video archive from Bossou, Guinea. Using 7 million detections from 100 h of video footage, we examined how varying the size of fixed temporal windows (i.e. aggregation rates) for defining edges impact individual-level gregariousness scores.The highest and lowest aggregation rates produced divergent values, indicating that different rates of aggregation capture different association patterns. To avoid any potential bias from false positives and negatives from automated detection, an intermediate aggregation rate should be used to reduce error across multiple variables. Individual-level network-derived traits were highly repeatable, indicating strong inter-individual variation in association patterns across years and highlighting the reliability of the method to capture consistent individual-level patterns of sociality over time. We found no reliable effects of age and sex on social behaviour and despite a significant drop in population size over the study period, individual estimates of gregariousness remained stable over time.We believe that our automated framework will be of broad utility to ethology and conservation, enabling the investigation of animal social behaviour from video footage at large scale, low cost and high reproducibility. We explore the implications of our findings for understanding variation in sociality patterns in wild ape populations. Furthermore, we examine the trade-offs involved in using face recognition technology to generate social networks and sociality measures. Finally, we outline the steps for the broader deployment of this technology for analysis of large-scale datasets in ecology and evolution.
- Carbon, nitrogen, and oxygen stable isotopes in modern tooth enamel: A case study from Gorongosa National Park, central MozambiquePublication . Lüdecke, Tina; Leichliter, Jennifer N.; Aldeias, Vera; Bamford, Marion K.; Biro, Dora; Braun, David R.; Capelli, Cristian; Cybulski, Jonathan D.; Duprey, Nicolas N.; Ferreira da Silva, Maria J.; Foreman, Alan D.; Habermann, Jörg M.; Haug, Gerald H.; Martínez, Felipe I.; Mathe, Jacinto; Mulch, Andreas; Sigman, Daniel M.; Vonhof, Hubert; Bobe, Rene; Carvalho, Susana; Martínez-García, AlfredoThe analyses of the stable isotope ratios of carbon (delta C-13), nitrogen (delta N-15), and oxygen (delta O-18) in animal tissues are powerful tools for reconstructing the feeding behavior of individual animals and characterizing trophic interactions in food webs. Of these biomaterials, tooth enamel is the hardest, most mineralized vertebrate tissue and therefore least likely to be affected by chemical alteration (i.e., its isotopic composition can be preserved over millions of years), making it an important and widely available archive for biologists and paleontologists. Here, we present the first combined measurements of delta C-13, delta N-15, and delta O-18 in enamel from the teeth of modern fauna (herbivores, carnivores, and omnivores) from the well-studied ecosystem of Gorongosa National Park (GNP) in central Mozambique. We use two novel methods to produce high-precision stable isotope enamel data: (i) the "oxidation-denitrification method," which permits the measurement of mineral-bound organic nitrogen in tooth enamel (delta N-15(enamel)), which until now, has not been possible due to enamel's low organic content, and (ii) the "cold trap method," which greatly reduces the sample size required for traditional measurements of inorganic delta C-13(enamel) and delta O-18(enamel) (from >= 0.5 to <= 0.1 mg), permitting analysis of small or valuable teeth and high-resolution serial sampling of enamel. The stable isotope results for GNP fauna reveal important ecological information about the trophic level, dietary niche, and resource consumption. delta N-15(enamel) values clearly differentiate trophic level (i.e., carnivore delta N-15(enamel) values are 4.0 parts per thousand higher, on average, than herbivores), delta C-13(enamel) values distinguish C-3 and/or C-4 biomass consumption, and delta O-18(enamel) values reflect local meteoric water (delta O-18(water)) in the park. Analysis of combined carbon, nitrogen, and oxygen stable isotope data permits geochemical separation of grazers, browsers, omnivores, and carnivores according to their isotopic niche, while mixed-feeding herbivores cannot be clearly distinguished from other dietary groups. These results confirm that combined C, N, and O isotope analyses of a single aliquot of tooth enamel can be used to reconstruct diet and trophic niches. Given its resistance to chemical alteration, the analysis of these three isotopes in tooth enamel has a high potential to open new avenues of research in (paleo)ecology and paleontology.
- Chimpanzee face recognition from videos in the wild using deep learningPublication . Schofield, Daniel; Nagrani, Arsha; Zisserman, Andrew; Hayashi, Misato; Matsuzawa, Tetsuro; Biro, Dora; Carvalho, SusanaVideo recording is now ubiquitous in the study of animal behavior, but its analysis on a large scale is prohibited by the time and resources needed to manually process large volumes of data. We present a deep convolutional neural network (CNN) approach that provides a fully automated pipeline for face detection, tracking, and recognition of wild chimpanzees from long-term video records. In a 14-year dataset yielding 10 million face images from 23 individuals over 50 hours of footage, we obtained an overall accuracy of 92.5% for identity recognition and 96.2% for sex recognition. Using the identified faces, we generated co-occurrence matrices to trace changes in the social network structure of an aging population. The tools we developed enable easy processing and annotation of video datasets, including those from other species. Such automated analysis unveils the future potential of large-scale longitudinal video archives to address fundamental questions in behavior and conservation.
- Chimpanzee play sequences are structured hierarchically as gamesPublication . Mielke, Alexander; Carvalho, SusanaSocial play is ubiquitous in the development of many animal species and involves players adapting actions flexibly to their own previous actions and partner responses. Play differs from other behavioural contexts for which fine-scale analyses of action sequences are available, such as tool use and communication, in that its form is not defined by its function, making it potentially more unpredictable. In humans, play is often organised in games, where players know context-appropriate actions but string them together unpredictably. Here, we use the sequential nature of play elements to explore whether play elements in chimpanzees are structured hierarchically and follow predictable game -like patterns. Based on 5,711 play elements from 143 bouts, we extracted individual-level play sequences of 11 Western chimpanzees (Pan troglodytes verus) of different ages from the Bossou community. We detected transition probabilities between play elements that exceeded expected levels and show that play elements form hierarchically clustered and interchangeable groups, indicative of at least six games that can be identified from transition networks, some with different roles for different players. We also show that increased information about preceding play elements improved predictability of subsequent elements, further indicating that play elements are not strung together randomly but that flexible action rules underlie their usage. Thus, chimpanzee play is hierarchically structured in short games which limit acceptable play elements and allow players to predict and adapt to partners' actions. This "grammar of action"approach to social interactions can be valuable in understanding cognitive and communicative abilities within and across species.
- Chimpanzee wooden tool analysis advances the identification of percussive technologyPublication . Luncz, Lydia V.; Braun, David R.; Marreiros, Joao; Bamford, Marion; Zeng, Chen; Pacome, Serge Soiret; Junghenn, Patrick; Buckley, Zachary; Yao, Xinyu; Carvalho, SusanaThe ability of humans to mediate environmental variation through tool use is likely the key to our success. However, our current knowledge of early cultural evolution derives almost exclusively from studies of stone tools and fossil bones found in the archaeological record. Tools made of plants are intrinsically perishable, and as such are almost entirely absent in the early record of human material culture. Modern human societies as well as nonhuman primate species use plant materials for tools far more often than stone, suggesting that current archaeological data are missing a substantial component of ancient technology. Here, we develop methods that quantify internal and external damage pattern in percussive wooden tools of living primates. Our work shows that the inflicted damage is irreversible, potentially persisting throughout fossilization processes. This research presents opportunities to investigate organic artifacts, a significant and highly neglected aspect of technological evolution within the Primate order.
- Could it be culture? An inter-troop comparison of baboon behaviour in Gorongosa National Park, MozambiquePublication . Muschinski, Jana; Lewis-Bevan, Lynn; Biro, Dora; Carvalho, SusanaBaboons in Gorongosa National Park have been observed to strip bark off Acacia robusta trees, chew the fibres underneath the bark, and spit out wadges. These actions leave identifiable marks on trees. Work conducted during 2018 indicates regional variation exists within the park1. Some trees exhibit stripping on the trunk, likely by elephants, in addition to (or instead of) on upper branches. We resurveyed all sites for bark stripping in 2019 and tested several ecological hypotheses following the method of exclusion2, 3.