Dr%20Susana%20Carvalho: List of publications

1. Longitudinal 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.<br> 2. 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.<br> 3. 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.<br> 4.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.

Social 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.

Leave taking is a common, possibly universal, feature of human social behaviour that has undergone very little empirical research. Although the importance remains unknown, it has been suggested to play an important role in managing separations, mitigating the risk, and increasing social bonding beyond the interaction itself. In nonhuman species, the literature is virtually absent, but identifying leave taking beyond humans may provide unique insights into the evolutionary history of this behaviour and shed light onto its proximate and ultimate function(s). Methods to study leave taking are not well-established, and the variation in definitions, measures, and control variables presented in past studies poses additional challenges. Baboons are a valuable model for investigating human behavioural evolution: as a flexible, highly adaptable, and social primate whose radiation is, similarly to humans, associated with the emergence of the African savannah biome. Using the framework and definition proposed by Baehren, we investigated the presence of leave taking in a wild, generalist primate and tested a range of candidate behaviours on prerecorded video footage: (1) self-scratching, (2) eye gaze, and (3) orientation in the direction of parting. Using multivariate analysis, controlling for interaction duration and individual variation, our results show that orientation in the direction of parting occurs predominantly before social separation events. These results indicate evidence of leave taking in a wild nonhuman population and contrast with previous ideas that this is a uniquely human behaviour. The presence of leave taking in baboons suggests a deep evolutionary history of this behaviour, warranting further investigation into its function and presence across other nonhuman primate species.

<strong>Background<br></strong> Gorongosa National Park in Mozambique hosts a large population of baboons, numbering over 200 troops. Gorongosa baboons have been tentatively identified as part of <i>Papio ursinus</i> 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 <i>P. ursinus</i> and <i>P. cynocephalus</i>, 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 <i>Papio</i> genomes. <br><strong> Results<br></strong> We confirmed that <i>P. ursinus</i> is the species closest to Gorongosa baboons. However, the Gorongosa baboon genomes share more derived alleles with <i>P. cynocephalus</i> than <i>P. ursinus</i> does, but no recent gene flow between <i>P. ursinus</i> and <i>P. cynocephalus</i> was detected when available <i>Papio</i> 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 <i>P. cynocephalus</i>, hinting to direct or indirect contributions from baboons belonging to the “northern” <i>Papio</i> clade, and signal the presence of population structure within <i>P. ursinus</i>. <br><strong> Conclusions<br></strong> 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.

Discussions of how animal culture can aid the conservation crisis are burgeoning. As scientists and conservationists working to protect endangered species, we call for reflection on how the culture concept may be applied in practice. Here, we discuss both the potential benefits and potential shortcomings of applying the animal culture concept, and propose a set of achievable milestones that will help guide and ensure its effective integration existing conservation frameworks, such as Adaptive Management cycles or Open Standards.

Large video datasets of wild animal behavior are crucial to produce longitudinal research and accelerate conservation efforts; however, large-scale behavior analyses continue to be severely constrained by time and resources. We present a deep convolutional neural network approach and fully automated pipeline to detect and track two audiovisually distinctive actions in wild chimpanzees: buttress drumming and nut cracking. Using camera trap and direct video recordings, we train action recognition models using audio and visual signatures of both behaviors, attaining high average precision (buttress drumming: 0.87 and nut cracking: 0.85), and demonstrate the potential for behavioral analysis using the automatically parsed video. Our approach produces the first automated audiovisual action recognition of wild primate behavior, setting a milestone for exploiting large datasets in ethology and conservation.

Spatial information is crucial to archaeological field research. From the plane-table to the total station, recent technological advances have enabled data collection to become fully digital and highly accurate. Nevertheless, the recent expansion of archaeological expeditions to novel environments often incompatible with modern mapping equipment, e.g. tropical forests or ephemeral shorelines, calls for further methodological innovations. Such projects, as well as those under logistic or financial limitations, are still largely reliant on more time consuming, less accurate, traditional approaches, e.g. offset or tape and compass methods. The DistoX2 is a digital, highly portable, and versatile hand-held instrument originally developed for speleological surveys where total stations and DGPSs are not feasible. However, the potential of the DistoX2 system as a spatial mapping tool in above-ground contexts has been surprisingly overlooked. Here, we present a first assessment of the applicability of the DistoX2 for archaeological mapping in non-speleological environments. We investigate precision and accuracy in controlled above-ground settings relative to two common methods of data collection – total station, and tape and compass. We test the relative precision of the DistoX2 when mounted on a tripod or operated in hand-held mode and discuss its applicability, and potential combined used, in the context of other increasingly popular methods – GNSS and SfM photogrammetry. With a mean error of ≈5.00 cm for horizontal readings and ≈2.00 cm for vertical readings, the DistoX2 is considerably more accurate than the tape and compass method (µ ≈ 67.00 cm horizontal; µ ≈ 3.00 cm vertical). While the DistoX2 exceeds the error thresholds of projects that require high spatial sensitivity (e.g. Palaeolithic excavations), it provides a reliable, low-cost and more accurate alternative to many projects that resort to more traditional methods. This fills an existent methodological and financial gap amongst the growing diversity of archaeological expeditions.

For the past two centuries, non‐human primates have been reported to inspect, protect, retrieve, carry or drag the dead bodies of their conspecifics and, for nearly the same amount of time, sparse scientific attention has been paid to such behaviours. Given that there exists a considerable gap in the fossil and archaeological record concerning how early hominins might have interacted with their dead, extant primates may provide valuable insight into how and in which contexts thanatological behaviours would have occurred. First, we outline a comprehensive history of comparative thanatology in non‐human primates, from the earliest accounts to the present, uncovering the interpretations of previous researchers and their contributions to the field of primate thanatology. Many of the typical behavioural patterns towards the dead seen in the past are consistent with those observed today. Second, we review recent evidence of thanatological responses and organise it into distinct terminologies: direct interactions (physical contact with the corpse) and secondary interactions (guarding the corpse, vigils and visitations). Third, we provide a critical evaluation regarding the form and function of the behavioural and emotional aspects of these responses towards infants and adults, also comparing them with non‐conspecifics. We suggest that thanatological interactions: promote a faster re‐categorisation from living to dead, decrease costly vigilant/caregiving behaviours, are crucial to the management of grieving responses, update position in the group's hierarchy, and accelerate the formation of new social bonds. Fourth, we propose an integrated model of Life‐Death Awareness, whereupon neural circuitry dedicated towards detecting life, i.e. the agency system (animate agency, intentional agency, mentalistic agency) works with a corresponding system that interacts with it on a decision‐making level (animate/inanimate distinction, living/dead discrimination, death awareness). Theoretically, both systems are governed by specific cognitive mechanisms (perceptual categories, associative concepts and high‐order reasoning, respectively). Fifth, we present an evolutionary timeline from rudimentary thanatological responses likely occurring in earlier non‐human primates during the Eocene to the more elaborate mortuary practices attributed to genus Homo throughout the Pleistocene. Finally, we discuss the importance of detailed reports on primate thanatology and propose several empirical avenues to shed further light on this topic. This review expands and builds upon previous attempts to evaluate the body of knowledge on this subject, providing an integrative perspective and bringing together different fields of research to detail the evolutionary, sensory/cognitive, developmental and historical/archaeological aspects of primate thanatology. Considering all these findings and given their cognitive abilities, we argue that non‐human primates are capable of an implicit awareness of death.

<p>The origin of technology is believed to have marked a major adaptive shift in human evolution. Understanding the evolutionary process(es) underlying the first human adaptation to tool use, and the subsequent process(es) that led <em>Homo sapiens</em> to become the only extant primate fully dependent on technology, is one of the most stimulating topics of research of present-day archaeology. New fields of research have been founded (e.g. primate archaeology, Pliocene archaeology) during the quest to find out <em>how</em> old technology is, <em>where</em> it originated, and <em>who</em> were the first tool users. Historically, the vast majority of the information on this topic comes from the study of lithic (stone) tools, tools whose manufacture was generally believed to be a uniquely human characteristic until well into the 1960s. The production of lithic technology was linked first to the origin of the earliest hominins (the taxonomic group comprising modern humans, extinct human species, and all immediate human ancestors), being thought to have co-evolved with traits such as bipedalism or hunting/scavenging, and later to the evolution of the genus <em>Homo</em> and accompanying increases in brain size. As a result of breakthroughs in the field of primatology, and greater interdisciplinary work between archaeologists and primatologists, a paradigm shift in beliefs surrounding the uniqueness of human technology is underway. Following discoveries from the second half of the 20th century and the early 21st century, habitual tool use, tool manufacture, and the production of flakes are now known to occur in extant non-human species, firmly decoupling brain size expansion, bipedalism, and the origins of technology. Knapped stone tools and cut-marked bones have been discovered dating to ca. half a million years before the earliest evidence of <em>Homo</em>, giving rise to the possibility that earlier, previously unconsidered hominins, or even other extinct non-human primates, could have been responsible for the inception of tool use and manufacture. Following these advances, it is reasonable to hypothesize that the origins of technology may lie much further back in time than the earliest discovered modified stone tools—perhaps as far back as the late Miocene with the last common ancestor of <em>Homo</em> and <em>Pan</em>. Moreover, discoveries of lithic technology in more distantly related species, where convergent evolution is the most parsimonious explanation, strongly suggest the existence of multiple evolutionary pathways for technological emergence. While there is still much to unearth, the extension of the antiquity of modified stone tools, combined with the increased focus on interdisciplinary studies between archaeologists, primatologists, and paleoanthropologists, has gone a long way in overturning outdated beliefs by demonstrating that the development of technology is unlikely to have been a simple, linear process resulting from a single event or factor in the evolutionary history of humans.</p>

The habitual consumption of large-animal resources (e.g., similar sized or larger than the consumer) separates human and nonhuman primate behavior. Flaked stone tool use, another important hominin behavior, is often portrayed as being functionally related to this by the necessity of a sharp edge for cutting animal tissue. However, most research on both issues emphasizes sites that postdate ca. 2.0 million years ago. This paper critically examines the theoretical significance of the earlier origins of these two behaviors, their proposed interrelationship, and the nature of the empirical record. We argue that concepts of meat-eating and tool use are too loosely defined: outside-bone nutrients (e.g., meat) and inside-bone nutrients (e.g., marrow and brains) have different macronutrient characteristics (protein vs. fat), mechanical requirements for access (cutting vs. percussion), search, handling and competitive costs, encounter rates, and net returns. Thus, they would have demanded distinct technological and behavioral solutions. We propose that the regular exploitation of large-animal resources—the “human predatory pattern”—began with an emphasis on percussion-based scavenging of inside-bone nutrients, independent of the emergence of flaked stone tool use. This leads to a series of empirical test implications that differ from previous “meat-eating” origins scenarios.

The 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.

African apes and humans share a genetic mutation that enables them to effectively metabolize ethanol. However, voluntary ethanol consumption in this evolutionary radiation is documented only in modern humans. Here, we report evidence of the long-term and recurrent ingestion of ethanol from the raffia palm (Raphia hookeri, Arecaceae) by wild chimpanzees (Pan troglodytes verus) at Bossou in Guinea, West Africa, from 1995 to 2012. Chimpanzees at Bossou ingest this alcoholic beverage, often in large quantities, despite an average presence of ethanol of 3.1% alcohol by volume (ABV) and up to 6.9% ABV. Local people tap raffia palms and the sap collects in plastic containers, and chimpanzees use elementary technology—a leafy tool—to obtain this fermenting sap. These data show that ethanol does not act as a deterrent to feeding in this community of wild apes, supporting the idea that the last common ancestor of living African apes and modern humans was not averse to ingesting foods containing ethanol.

Stone tool use by wild chimpanzees of West Africa offers a unique opportunity to explore the evolutionary roots of technology during human evolution. However, detailed analyses of chimpanzee stone artifacts are still lacking, thus precluding a comparison with the earliest archaeological record. This paper presents the first systematic study of stone tools used by wild chimpanzees to crack open nuts in Bossou (Guinea-Conakry), and applies pioneering analytical techniques to such artifacts. Automatic morphometric GIS classification enabled to create maps of use wear over the stone tools (anvils, hammers, and hammers/ anvils), which were blind tested with GIS spatial analysis of damage patterns identified visually. Our analysis shows that chimpanzee stone tool use wear can be systematized and specific damage patterns discerned, allowing to discriminate between active and passive pounders in lithic assemblages. In summary, our results demonstrate the heuristic potential of combined suites of GIS techniques for the analysis of battered artifacts, and have enabled creating a referential framework of analysis in which wild chimpanzee battered tools can for the first time be directly compared to the early archaeological record.

Percussive technology continues to play an increasingly important role in understanding the evolution of tool use. Comparing the archaeological record with extractive foraging behaviors in nonhuman primates has focused on percussive implements as a key to investigating the origins of lithic technology. Despite this, archaeological approaches towards percussive tools have been obscured by a lack of standardized methodologies. Central to this issue have been the use of qualitative, non-diagnostic techniques to identify percussive tools from archaeological contexts. Here we describe a new morphometric method for distinguishing anthropogenically-generated damage patterns on percussive tools from naturally damaged river cobbles. We employ a geomatic approach through the use of three-dimensional scanning and geographical information systems software to statistically quantify the identification process in percussive technology research. This will strengthen current technological analyses of percussive tools in archaeological frameworks and open new avenues for translating behavioral inferences of early hominins from percussive damage patterns.

<p style="text-align:justify;">Why did our earliest hominin ancestors begin to walk bipedally as their main form of terrestrial travel? The lack of sufficient fossils and differing interpretations of existing ones leave unresolved the debate about what constitutes the earliest evidence of habitual bipedality. Compelling evidence shows that this shift coincided with climatic changes that reduced forested areas, probably forcing the earliest hominins to range in more open settings [1]. While environmental shifts may have prompted the origins of bipedality in the hominin clade, it remains unknown exactly which selective pressures led hominins to modify their postural repertoire to include a larger component of bipedality [2]. Here, we report new experimental results showing that wild chimpanzees walk bipedally more often and carry more items when transporting valuable, unpredictable resources to less–competitive places.</p>

To model or not to model? A recent search of the internet using three key words, “chimpanzees model humans,” yielded 27,200,200 pages of results, in less than half a second. Recently, chimpanzees (Pan troglodytes) have been labeled as unsatisfactory models in understanding human evolution (Sayers and Lovejoy 2008; White et al. 2009). Highlighted differences between the anatomy of Ardipithecus ramidus (a hominin species living in East Africa at 4.4 Ma) and of the extant African apes suggest that the last common ancestor (LCA) of humans and African apes was morphologically more primitive than previously assumed (Pilbeam and Young 2004). This suggests that several primitive traits common to extant African apes and early hominins might have been a result of convergent adaptations rather than phylogeny (Stern and Orgogozo 2009). The reconstructed paleobiology of Ardi emphasizes behavioral (e.g., facultative bipedality) and morphological (e.g., reduced canine teeth) divergences from the extant chimpanzee. According to Lovejoy et al. (2010, p. 410), these conclusions “were based on intensive review of homologous traits in other primates,” using a method known as strategic modeling (cf. Whiten et al. 2010). The aim of our paper is not to seek to prove that the chimpanzee is the best or only model for human evolution, compared with other living nonhuman species. Nor do we argue about the implications of vague behavioral terms, such as facultative bipedalism (e.g., how much bipedal locomotion does a facultative bipedal perform?), or broadly omnivorous (e.g., how much fruit needs to be in the diet for a species to be classed as a ripe fruit specialist, given that diets vary considerably with ecological context?), or terrestrial and arboreal feeder (e.g., what percentage of food must come from the ground versus above it?). Chimpanzees are insufficient models, if they are presented as the only useful species for reconstructing the hominin fossil record, nor are they time machines, whereby chimpanzee behavior precisely mimics LCA or hominin behavior. As we share various features with all primates (Fleagle 1998; Martin 1990), different research topics are better approached with a comparative approach, using pertinent species as models. Research that uses comparative primate modeling covers a wide range of human behavioral patterns, from tool use to contagious disease (Boyd and Silk 2009; Chapman et al. 2005).

Springer, Tokyo Matsuzawa T (2005) Book review of the cultured chimpanzee: reflections on cultural primatology. Nature 434:21–22 Matsuzawa T (2006a) Bossou: 30 years. Pan Africa News 13:16–19 Matsuzawa T (2006b) Sociocognitive&nbsp;...

Chimpanzees rarely capture an animal without eating it, but this puzzling pattern occurs in both nature and captivity, mostly by youngsters1-6. At Bossou in Guinea, chimpanzees rarely hunt for meat; their home range presents few suitable prey7. From 1976 to 2008, only one bird (West African wood-owl, Ciccaba woodfordi) capture was recorded, and it was consumed7. In 2009, we saw two captures of this species, which were not followed by consumption. Instead, both raptors were used as toys, as previously observed at Bossou with tree hyrax, Dendrohyrax dorsalis3. Here we describe the captures and discuss the implications of this behavior from an evolutionary perspective.

All modern humans use tools to overcome limitations of our anatomy and to make difficult tasks easier. However, if tool use is such an advantage, we may ask why it is not evolved to the same degree in other species. To answer this question, we need to bring a long-term perspective to the material record of other members of our own order, the Primates.

Recent etho-archaeological studies of stone-tool use by wild chimpanzees have contributed valuable data towards elucidating the variables that influenced the emergence and development of the first lithic industries among Plio-Pleistocene hominins. Such data help to identify potential behaviours entailed in the first percussive technologies that are invisible in archaeological records. The long-term research site of Bossou in Guinea features a unique chimpanzee community whose members systematically use portable stones as hammers and anvils to crack open nuts in natural as well as in field experimental settings. Here we present the first analysis of repeated reuse of the same tool-composites in wild chimpanzees. Data collected over 5 years of experimental nut-cracking sessions at an "outdoor laboratory" site were assessed for the existence of systematic patterns in the selection of tool-composites, at group and at individual levels. Chimpanzees combined certain stones as hammer and anvil more often than expected by chance, even when taking into account preferences for individual stones by themselves. This may reflect an ability to recognise the nut-cracker as a single tool (composed of two elements, but functional only as a whole), as well as discrimination of tool quality-effectiveness. Through repeatedly combining the same pairs of stones-whether due to preferences for particular composites or for the two elements independently-tool-users may amplify use-wear traces and increase the likelihood of fracturing the stones, and thus of detaching pieces by battering. © 2009 Springer-Verlag.