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.
- Applying collocation and APRIORI analyses to chimpanzee diets: methods for investigating nonrandom food combinations in primate self‐medicationPublication . Freymann, Elodie; Coelho, João d'Oliveira; Hobaiter, Catherine; Huffman, Michael A.; Muhumuza, Geresomu; Zuberbühler, Klaus; Carvalho, SusanaIdentifying 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.
- 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.
- Baboon route repetition in a seasonal environmentPublication . Lewis-Bevan, Lynn Catrin; Hammond, Philippa; Carvalho, Susana; Biro, DoraIntroduction: Route-based navigation is a common movement strategy for a variety of taxa, wherein animals repeatedly re-use familiar paths during travel. However, this type of navigation is understudied in wild animals that experience regular displacement, raising questions about the robustness and longevity of such routes and route memories. The seasonal flooding of Gorongosa National Park, Mozambique, provides an opportunity to test multiple facets of route-based navigation in wild primates, due to its high seasonality and annual flooding.Methods: Data was collected from GPS collars placed on four chacma baboons in two troops in Gorongosa National Park. Using GPS points taken every 15 minutes, we use nearest-neighbour analysis to compare daily paths across the year, to identify high-use paths. We then look at the identified high-use paths to see if they are used across the entire study period, with a focus on areas that were vacated for more than two months of the study period.Results: We find that the baboons do have vacated areas, but return to the same areas after displacement. We did not find high-use routes in these areas used both before and after displacement, although high-use routes did exist that were used across the study period in different areas.Discussion: Our results indicate that routes may not be maintained in long-term memory spanning several months, or that route reuse is in part dependant on seasonal resources or navigational aids. Although the study period did not span a full year, this study presents a replicable method of analysing route reuse and identifying high-use routes without traditional methods of manually overlaying and analysing daily paths.
- The behavioural ecology of hominin locomotion: what can we learn from landscapes of fear and primate terrestriality?Publication . Hammond, Philippa; Bobe, René; Carvalho, SusanaA defining feature of the hominin clade is bipedality, often parcelled together with terrestriality. However, there is increasing evidence of locomotor diversity, both within the hominin clade and amongst the Miocene apes that came before them. There is also growing recognition that bipedalism might have arboreal origins and that arboreality persisted in several hominin taxa, including our own genus Homo. Furthermore, the difference between terms like “habitual” and “obligate” bipedality is not clearly defined and is often inferred from fossil features, rather than a description of each behaviour in vivo. Combining fossil and palaeoecological evidence with insights from behavioural ecology facilitates new interpretations of evolutionary pathways and highlights the importance of considering convergent evolution in the emergence of locomotor traits and characteristics. Taking such an approach also moves away from assumptions of a straight-line trajectory towards modern human locomotion and explores the likelihood that independent forms of bipedality and terrestriality arose at different times and in different combinations with other features of ape morphology and behaviour. Evidence from extant primate species can broaden our understanding of the correlates, causes, and consequences of terrestriality and can be used to generate hypotheses which are then explored further using paleontological methods. In this paper, we explore the evolutionary origins of hominin locomotion, but extend our review to include broader timescales, a wider range of primate taxa, and an integrated set of methods and disciplines for generating and testing hypotheses about locomotion. Perceived risk (or, the “landscape of fear”) is a key pressure that has selected for primate arboreality – particularly nocturnal arboreality. We propose that shifts in Plio-Pleistocene landscapes of fear – caused by declining carnivoran abundance and diversity – might also have been a key selection pressure in changes to primate locomotion, particularly papionin and hominid terrestriality. We discuss this hypothesis and propose future research avenues to explore it further. Not only will such research provide a more nuanced view of the causes and consequences of a rare behavioural trait in primates, but it could ultimately help us explain how one group of African apes came to spend all their time on the ground, and how that made them human.
- 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.