Integrative Behavioural Biology
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Our main research interest is the integrative study of social behaviour, which combines the study of proximate causes (gene modules, hormones, neural circuits, cognitive processes) and ultimate effects (evolutionary consequences). In particular we aim to understand how brain and behaviour can be shaped by social environment, and how the cognitive, neural and genetic mechanisms underlying plasticity in the expression of social behaviour have evolved. Current research questions centre on four topics: 1. Evolution of social cognition and of its neuromolecular mechanisms – we aim to understand if social plasticity is as an organismal performance trait that impacts Darwinian fitness and may itself be subject to selection; 2. Genomic and epigenomic mechanisms of social plasticity – we seek to understand how the same genome can produce different social phenotypes in response to key social cues in the environment; 3. Neuroendocrinology of social interactions and of social plasticity – this research aims to understand the role of hormones and neuropeptides as neuromodulators involved in the plasticity of social behaviour; 4. Fish cognition and welfare – we aim to use our knowledge in this field to improve fish husbandry and handling procedures towards better research and animal welfare.
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- Face Your Fears: Cleaning Gobies Inspect Predators despite Being Stressed by ThemPublication . Soares, Marta C.; Bshary, Redouan; Cardoso, Sónia C.; Côté, Isabelle M.; Oliveira, Rui F.social stressors typically elicit two distinct behavioural responses in vertebrates: an active response (i.e., "fight or flight") or behavioural inhibition (i.e., freezing). Here, we report an interesting exception to this dichotomy in a Caribbean cleaner fish, which interacts with a wide variety of reef fish clients, including predatory species. Cleaning gobies appraise predatory clients as potential threat and become stressed in their presence, as evidenced by their higher cortisol levels when exposed to predatory rather than to non-predatory clients. Nevertheless, cleaning gobies neither flee nor freeze in response to dangerous clients but instead approach predators faster (both in captivity and in the wild), and interact longer with these clients than with non-predatory clients (in the wild). We hypothesise that cleaners interrupt the potentially harmful physiological consequences elicited by predatory clients by becoming increasingly proactive and by reducing the time elapsed between client approach and the start of the interaction process. The activation of a stress response may therefore also be responsible for the longer cleaning service provided by these cleaners to predatory clients in the wild. Future experimental studies may reveal similar patterns in other social vertebrate species when, for instance, individuals approach an opponent for reconciliation after a conflict.
- Arginine vasotocin regulation of interspecific cooperative behaviour in a cleaner fishPublication . Soares, Marta C; Bshary, Redouan; Mendonça, Rute; Grutter, Alexandra S; Oliveira, Rui FIn an interspecific cooperative context, individuals must be prepared to tolerate close interactive proximity to other species but also need to be able to respond to relevant social stimuli in the most appropriate manner. The neuropeptides vasopressin and oxytocin and their non-mammalian homologues have been implicated in the evolution of sociality and in the regulation of social behaviour across vertebrates. However, little is known about the underlying physiological mechanisms of interspecific cooperative interactions. In interspecific cleaning mutualisms, interactions functionally resemble most intraspecific social interactions. Here we provide the first empirical evidence that arginine vasotocin (AVT), a non-mammalian homologue of arginine vasopressin (AVP), plays a critical role as moderator of interspecific behaviour in the best studied and ubiquitous marine cleaning mutualism involving the Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus. Exogenous administration of AVT caused a substantial decrease of most interspecific cleaning activities, without similarly affecting the expression of conspecific directed behaviour, which suggests a differential effect of AVT on cleaning behaviour and not a general effect on social behaviour. Furthermore, the AVP-V1a receptor antagonist (manning compound) induced a higher likelihood for cleaners to engage in cleaning interactions and also to increase their levels of dishonesty towards clients. The present findings extend the knowledge of neuropeptide effects on social interactions beyond the study of their influence on conspecific social behaviour. Our evidence demonstrates that AVT pathways might play a pivotal role in the regulation of interspecific cooperative behaviour and conspecific social behaviour among stabilized pairs of cleaner fish. Moreover, our results suggest that the role of AVT as a neurochemical regulator of social behaviour may have been co-opted in the evolution of cooperative behaviour in an interspecific context, a hypothesis that is amenable to further testing on the potential direct central mechanism involved.
- A Three-Dimensional Stereotaxic MRI Brain Atlas of the Cichlid Fish Oreochromis mossambicusPublication . Simões, José M.; Teles, Magda C.; Oliveira, Rui F.; Van der Linden, Annemie; Verhoye, MarleenThe African cichlid Oreochromis mossambicus (Mozambique tilapia) has been used as a model system in a wide range of behavioural and neurobiological studies. The increasing number of genetic tools available for this species, together with the emerging interest in its use for neurobiological studies, increased the need for an accurate hodological mapping of the tilapia brain to supplement the available histological data. The goal of our study was to elaborate a three-dimensional, high-resolution digital atlas using magnetic resonance imaging, supported by Nissl staining. Resulting images were viewed and analysed in all orientations (transverse, sagittal, and horizontal) and manually labelled to reveal structures in the olfactory bulb, telencephalon, diencephalon, optic tectum, and cerebellum. This high resolution tilapia brain atlas is expected to become a very useful tool for neuroscientists using this fish model and will certainly expand their use in future studies regarding the central nervous system.
- Threat perception and familiarity moderate the androgen response to competition in womenPublication . Oliveira, Gonçalo A.; Uceda, Sara; Oliveira, Tânia; Fernandes, Alexandre; Garcia-Marques, Teresa; Oliveira, Rui F.Social interactions elicit androgen responses whose function has been posited to be the adjustment of androgen-dependent behaviors to social context. The activation of this androgen response is known to be mediated and moderated by psychological factors. In this study we tested the hypothesis that the testosterone (T) changes after a competition are not simply related to its outcome, but rather to the way the subject evaluates the event. In particular we tested two evaluative dimensions of a social interaction: familiarity with the opponent and the subjective evaluation of the outcome as threat or challenge. Challenge/threat occurs in goal relevant situations and represent different motivational states arising from the individuals' subjective evaluation of the interplay between the task demands and coping resources possessed. For challenge the coping resources exceed the task demands, while threat represents a state where coping resources are insufficient to meet the task demands. In this experiment women competed in pairs, against a same sex opponent using the number tracking test as a competitive task. Losers appraised the competition outcome as more threatening than winners, and displayed higher post-competition T levels than winners. No differences were found either for cortisol (C) or for dehydroepiandrosterone. Threat, familiarity with the opponent and T response were associated only in the loser condition. Moderation analysis suggests that for the women that lost the competition the effect of threat on T is moderated by familiarity with the opponent.
- Mind the fish: zebrafish as a model in cognitive social neurosciencePublication . Oliveira, Rui F.Understanding how the brain implements social behavior on one hand, and how social processes feedback on the brain to promote fine-tuning of behavioral output according to changes in the social environment is a major challenge in contemporary neuroscience. A critical step to take this challenge successfully is finding the appropriate level of analysis when relating social to biological phenomena. Given the enormous complexity of both the neural networks of the brain and social systems, the use of a cognitive level of analysis (in an information processing perspective) is proposed here as an explanatory interface between brain and behavior. A conceptual framework for a cognitive approach to comparative social neuroscience is proposed, consisting of the following steps to be taken across different species with varying social systems: (1) identification of the functional building blocks of social skills; (2) identification of the cognitive mechanisms underlying the previously identified social skills; and (3) mapping these information processing mechanisms onto the brain. Teleost fish are presented here as a group of choice to develop this approach, given the diversity of social systems present in closely related species that allows for planned phylogenetic comparisons, and the availability of neurogenetic tools that allows the visualization and manipulation of selected neural circuits in model species such as the zebrafish. Finally, the state-of-the art of zebrafish social cognition and of the tools available to map social cognitive abilities to neural circuits in zebrafish are reviewed.
- Androgen modulation of social decision-making mechanisms in the brain: an integrative and embodied perspectivePublication . Oliveira, Gonçalo A.; Oliveira, Rui F.Apart from their role in reproduction androgens also respond to social challenges and this response has been seen as a way to regulate the expression of behavior according to the perceived social environment (Challenge hypothesis, Wingfield et al., 1990). This hypothesis implies that social decision-making mechanisms localized in the central nervous system (CNS) are open to the influence of peripheral hormones that ultimately are under the control of the CNS through the hypothalamic-pituitary-gonadal axis. Therefore, two puzzling questions emerge at two different levels of biological analysis: (1) Why does the brain, which perceives the social environment and regulates androgen production in the gonad, need feedback information from the gonad to adjust its social decision-making processes? (2) How does the brain regulate gonadal androgen responses to social challenges and how do these feedback into the brain? In this paper, we will address these two questions using the integrative approach proposed by Niko Tinbergen, who proposed that a full understanding of behavior requires its analysis at both proximate (physiology, ontogeny) and ultimate (ecology, evolution) levels.
- Androgen responsiveness to competition in humans: the role of cognitive variablesPublication . Oliveira, Rui; Oliveira, GonçaloAlthough androgens are commonly seen as male sex hormones, it has been established over the years that in both sexes, androgens also respond to social challenges. To explain the socially driven changes in androgens, two theoretical models have been proposed: the biosocial model and the challenge hypothesis. These models are typically seen as partly overlapping; however, they generate different predictions that are clarified here. In humans, sports competition and nonmetabolic competitive tasks have been used in the laboratory setting, as a proxy for agonistic interactions in animals. The results reviewed here show that the testosterone (T) response to competition in humans is highly variable – the studies present postcompetition T levels and changes in T that depend on the contest outcome and that cannot be predicted by the current theoretical models. These conflicting results bring to the foreground the importance of considering cognitive factors that could moderate the androgen response to competition. Among these variables, we elect cognitive appraisal and its components as a key candidate modulating factor. It is known that T also modulates the cognitive processes that are relevant to performance in competition. In this article, we reviewed the evidence arising from studies investigating the effect of administering exogenous T and compare those results with the findings from studies that measured endogenous T levels. Finally, we summarized the importance of also considering the interaction between androgens and other hormones, such as cortisol, when investigating the social modulation of T, as proposed by the dual-hormone hypothesis.
- Impact of ecotourism on the fish fauna of Bonito region (Mato Grosso do Sul State, Brazil): ecological, behavioural and physiological measuresPublication . Lima, Ana Carolina; Assis, Jorge; Sayanda, Diogo; Sabino, José; Oliveira, Rui F.Bonito, in Mato Grosso do Sul State, is an important destination for ecotourism in Brazil and the main challenge of sustainable ecotourism here has been to accommodate and adjust the increase of tourism without compromising the ecological integrity of the local ecosystems. In this study we aimed to assess the environmental impact of ecotourism on the fish fauna of Sucuri River in Bonito by integrating ecological, behaviour and physiological criteria and using the fish species Crenicichla lepidota and Moenkhausia bonita as indicators. Two distinct sites were defined to collect data: (1) affected daily by ecotourism (Tourism) and (2) undisturbed (No Tourism). The "stationary point count" method was performed to assess variations in ecological parameters and "ad libitum" and focal animal methods were used to collect behaviour data. The cortisol response of M. bonita to a stress protocol was measured from holding-water. Results showed a significantly increase in species richness, density and diversity at the Tourism site. Nevertheless, behaviour patterns indicated a higher stress at the Tourism site for both species as well higher cortisol levels for M. bonita. In opposition to the ecological measures, the behaviour and physiological ones may be interpreted as an early sign of negative impact caused by ecotourism, prior to changes at community level.
- Behavioural Stress Responses Predict Environmental Perception in European Sea Bass (Dicentrarchus labrax)Publication . Millot, Sandie; Cerqueira, Marco; Castanheira, Maria-Filipa; Øverli, Øyvind; Oliveira, Rui F.; Martins, Catarina I. M.Individual variation in the response to environmental challenges depends partly on innate reaction norms, partly on experience-based cognitive/emotional evaluations that individuals make of the situation. The goal of this study was to investigate whether pre-existing differences in behaviour predict the outcome of such assessment of environmental cues, using a conditioned place preference/avoidance (CPP/CPA) paradigm. A comparative vertebrate model (European sea bass, Dicentrarchus labrax) was used, and ninety juvenile individuals were initially screened for behavioural reactivity using a net restraining test. Thereafter each individual was tested in a choice tank using net chasing as aversive stimulus or exposure to familiar conspecifics as appetitive stimulus in the preferred or non preferred side respectively (called hereafter stimulation side). Locomotor behaviour (i.e. time spent, distance travelled and swimming speed in each tank side) of each individual was recorded and analysed with video software. The results showed that fish which were previously exposed to appetitive stimulus increased significantly the time spent on the stimulation side, while aversive stimulus led to a strong decrease in time spent on the stimulation side. Moreover, this study showed clearly that proactive fish were characterised by a stronger preference for the social stimulus and when placed in a putative aversive environment showed a lower physiological stress responses than reactive fish. In conclusion, this study showed for the first time in sea bass, that the CPP/CPA paradigm can be used to assess the valence (positive vs. negative) that fish attribute to different stimuli and that individual behavioural traits is predictive of how stimuli are perceived and thus of the magnitude of preference or avoidance behaviour.
- Testosterone response to competition in males is unrelated to opponent familiarity or threat appraisalPublication . Oliveira, Gonçalo A.; Uceda, Sara; Oliveira, Tânia F.; Fernandes, Alexandre C.; Garcia-Marques, Teresa; Oliveira, Rui F.It has been proposed in the literature that the testosterone (T) response to competition in humans may be modulated by cognitive variables. In a previous experiment with a female sample we have reported that opponent familiarity and threat appraisal moderated the T response to competition in women. With this experiment we aim to investigate if these variables have the same impact on males T response to competition, extending the previous findings in our lab. Forty male participants (20 dyads) were recruited to engage in a same sex, face to face competition using the Number Tracking Test as a competitive task. Levels of T, cortisol (C) and dehydroepiandrosterone (DHEA) were measured before and 20 min after the competition. Results show that losers report higher levels of threat than winners and increased their T levels after the competition, however this T change was not predicted by opponent familiarity or threat appraisal. No variation was detected for C and DHEA levels. These findings suggest that there could be sex differences for the moderators/mediators of the T response to competition in humans.
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