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- 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.
- 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.
- 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.
- 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.
- Genomic variation in baboons from central Mozambique unveils complex evolutionary relationships with other Papio speciesPublication . Santander, Cindy; Molinaro, Ludovica; Mutti, Giacomo; Martínez, Felipe I.; Mathe, Jacinto; Ferreira da Silva, Maria J.; Caldon, Matteo; Oteo-Garcia, Gonzalo; Aldeias, Vera; Archer, Will; Bamford, Marion; Biro, Dora; Bobe, René; Braun, David R.; Hammond, Philippa; Lüdecke, Tina; Pinto, Maria J.; Meira Paulo, Luis; Stalmans, Marc; Regala, Frederico; Bertolini, Francesco; Moltke, Ida; Raveane, Alessandro; Pagani, Luca; Carvalho, Susana; Capelli, CristianBackground Gorongosa National Park in Mozambique hosts a large population of baboons, numbering over 200 troops. Gorongosa baboons have been tentatively identified as part of Papio ursinus on the basis of previous limited morphological analysis and a handful of mitochondrial DNA sequences. However, a recent morphological and morphometric analysis of Gorongosa baboons pinpointed the occurrence of several traits intermediate between P. ursinus and P. cynocephalus, leaving open the possibility of past and/or ongoing gene flow in the baboon population of Gorongosa National Park. In order to investigate the evolutionary history of baboons in Gorongosa, we generated high and low coverage whole genome sequence data of Gorongosa baboons and compared it to available Papio genomes. Results We confirmed that P. ursinus is the species closest to Gorongosa baboons. However, the Gorongosa baboon genomes share more derived alleles with P. cynocephalus than P. ursinus does, but no recent gene flow between P. ursinus and P. cynocephalus was detected when available Papio genomes were analyzed. Our results, based on the analysis of autosomal, mitochondrial and Y chromosome data, suggest complex, possibly male-biased, gene flow between Gorongosa baboons and P. cynocephalus, hinting to direct or indirect contributions from baboons belonging to the “northern” Papio clade, and signal the presence of population structure within P. ursinus. Conclusions The analysis of genome data generated from baboon samples collected in central Mozambique highlighted a complex set of evolutionary relationships with other baboons. Our results provided new insights in the population dynamics that have shaped baboon diversity.
- Gorongosa by the sea: First Miocene fossil sites from the Urema Rift, central Mozambique, and their coastal paleoenvironmental and paleoecological contextsPublication . Habermann, Jörg M.; Alberti, Matthias; Aldeias, Vera; Alemseged, Zeresenay; Archer, Will; Bamford, Marion; Biro, Dora; Braun, David R.; Capelli, Cristian; Cunha, Eugenia; da Silva, Maria Ferreira; Luedecke, Tina; Madiquida, Hilario; Martinez, Felipe I.; Mathe, Jacinto; Negash, Enquye; Paulo, Luis M.; Pinto, Maria; Stalmans, Marc; Regala, Frederico Tata; Wynn, Jonathan G.; Bobe, Rene; Carvalho, SusanaThe East African Rift System (EARS) has played a central role in our understanding of human origins and vertebrate evolution in the late Cenozoic of Africa. However, the distribution of fossil sites along the rift is highly biased towards its northern extent, and the types of paleoenvironments are primarily restricted to fluvial and lacustrine settings. Here we report the discovery of the first fossil sites from the Urema Rift at Gorongosa National Park (central Mozambique) at the southern end of the EARS, and reconstruct environmental contexts of the fossils. In situ and surface fossils from the lower member of the Mazamba Formation, estimated to be of Miocene age, comprise mammals, reptiles, fishes, invertebrates, palms, and dicot trees. Fossil and geological evidence indicates a coastal-plain paleoenvironmental mosaic of riverine forest/woodland and estuarine habitats that represent the first coastal biomes identified in the Neogene EARS context. Receiving continental sediment from source terranes west of today's Urema Graben, estuarine sequences accumulated prior to rifting as compound incised-valley fills on a low-gradient coastal plain following transgression. Modern environmental analogues are extremely productive habitats for marine and terrestrial fauna, including primates. Thus, our discoveries raise the possibility that the Miocene coastal landscapes of Gorongosa were ecologically-favorable habitats for primates, providing relatively stable maritime climate and ecosystem conditions, year-round freshwater availability, and food both from terrestrial and marine sources. The emerging fossil record from Gorongosa is beginning to fill an important gap in the paleobiogeography of Africa as no fossil sites of Neogene age have previously been reported from the southernmost part of the EARS. Furthermore, this unique window into past continental-margin ecosystems of central Mozambique may allow us to test key paleobiogeographic hypotheses during critical periods of primate evolution.
- Landscape‐scale effects of season and predation risk on the terrestrial behavior of chacma baboons (Papio ursinus)Publication . Hammond, Philippa; Gaynor, Kaitlyn; Easter, Tara; Biro, Dora; Carvalho, SusanaObjectives: “Terrestrial” primates are not common nor well defined across the order. In those species that do use the ground, terrestriality is rarely documented outside daylight hours. Predation risk is thought to have shaped conserved behaviors like primates' selection of arboreal sleep sites, but it is less clear—particularly at the landscape scale—how predation risk interacts with other ecological and seasonal variables to drive terrestriality. This camera trapping study investigates patterns in terrestrial behavior both spatially and temporally across neighboring populations of chacma baboons. Materials and Methods: We use camera trap data from two terrestrial grids, one established within and one outside the boundaries of Gorongosa National Park, Mozambique. We model how baboon terrestrial activity varies with woody cover, proximity to water, season, anthropogenic variables, as well as predation risk. We also model how terrestrial activity varies across the diel cycle and use overlap analyses to explore differences in the baboon populations' activity patterns. Results: We find no significant predictors of geospatial variation in the terrestrial activity of baboons across each grid but do find evidence of higher terrestrial activity in the late dry season. We also find significantly different diel patterns of baboon activity detected across each grid. Discussion: Baboons likely use the ground more in the dry season for accessing water and resources when arboreal foods are less abundant. Diel variation between the two populations suggests that baboons might utilize the ground more during “riskier” crepuscular and nocturnal hours where leopards are not present.