Browsing by Author "Oliveira, Rui F."
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- 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.
- Audience Effects in Territorial Defense of Male Cichlid Fish Are Associated with Differential Patterns of Activation of the Brain Social Decision-Making NetworkPublication . Roleira, António; Oliveira, Gonçalo A.; Lopes, João S.; Oliveira, Rui F.Animals communicate by exchanging signals frequently in the proximity of other conspecifics that may detect and intercept signals not directed to them. There is evidence that the presence of these bystanders modulates the signaling behavior of interacting individuals, a phenomenon that has been named audience effect. Research on the audience effect has predominantly focused on its function rather than on its proximate mechanisms. Here, we have investigated the physiological and neuromolecular correlates of the audience effect in a cichlid fish (Mozambique tilapia, Oreochromis mossambicus). A male was exposed to a territorial intrusion in the presence or absence of a female audience. Results showed that the presence of the female audience increased territorial defense, but elicited a lower androgen and cortisol response to the territorial intrusion. Furthermore, analysis of the expression of immediate early genes, used as markers of neuronal activity, in brain areas belonging to the social decision-making network (SDMN) revealed different patterns of network activity and connectivity across the different social contexts (i.e., audience × intrusion). Overall, these results suggest that socially driven plasticity in the expression of territorial behavior is accommodated in the central nervous system by rapid changes in functional connectivity between nodes of relevant networks (SDMN) rather than by localized changes of activity in specific brain nuclei.
- 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.
- Brain Transcriptomic Response to Social Eavesdropping in Zebrafish (Danio rerio)Publication . Lopes, João Sollari; Abril-de-Abreu, Rodrigo; Oliveira, Rui F.Public information is widely available at low cost to animals living in social groups. For instance, bystanders may eavesdrop on signaling interactions between conspecifics and use it to adapt their subsequent behavior towards the observed individuals. This social eavesdropping ability is expected to require specialized mechanisms such as social attention, which selects social information available for learning. To begin exploring the genetic basis of social eavesdropping, we used a previously established attention paradigm in the lab to study the brain gene expression profile of male zebrafish (Danio rerio) in relation to the attention they paid towards conspecifics involved or not involved in agonistic interactions. Microarray gene chips were used to characterize their brain transcriptomes based on differential expression of single genes and gene sets. These analyses were complemented by promoter region-based techniques. Using data from both approaches, we further drafted protein interaction networks. Our results suggest that attentiveness towards conspecifics, whether interacting or not, activates pathways linked to neuronal plasticity and memory formation. The network analyses suggested that fos and jun are key players on this response, and that npas4a, nr4a1 and egr4 may also play an important role. Furthermore, specifically observing fighting interactions further triggered pathways associated to a change in the alertness status (dnajb5) and to other genes related to memory formation (btg2, npas4b), which suggests that the acquisition of eavesdropped information about social relationships activates specific processes on top of those already activated just by observing conspecifics.
- Dear Enemies Elicit Lower Androgen Responses to Territorial Challenges than Unfamiliar Intruders in a Cichlid FishPublication . Aires, Rui F.; Oliveira, Gonçalo A.; Oliveira, Tânia F.; Ros, Albert F. H.; Oliveira, Rui F.In many territorial species androgen hormones are known to increase in response to territorial intrusions as a way to adjust the expression of androgen-dependent behaviour to social challenges. The dear enemy effect has also been described in territorial species and posits that resident individuals show a more aggressive response to intrusions by strangers than by other territorial neighbours. Therefore, we hypothesized that the dear enemy effect may also modulate the androgen response to a territorial intrusion. Here we tested this hypothesis in male cichlid fish (Mozambique tilapia, Oreochromis mossambicus) using a paradigm of four repeated territorial intrusions, either by the same neighbour or by four different unfamiliar intruders. Neighbour intruders elicited lower aggression and a weaker androgen response than strangers on the first intrusion of the experiment. With repeated intrusions, the agonistic behaviour of the resident males against familiar intruders was similar to that displayed towards strangers. By the fourth intrusion the androgen response was significantly reduced and there was no longer a difference between the responses to the two types of intruders. These results suggest that the dear enemy effect modulates the androgen response to territorial intrusions and that repeated intrusions lead to a habituation of the androgen response.
- 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.
- 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.
- Mechanisms of social buffering of fear in zebrafishPublication . Faustino, Ana I.; Tacão-Monteiro, André; Oliveira, Rui F.Some humans thrive whereas others resign when exposed to threatening situations throughout life. Social support has been identified as an important modulator of these discrepancies in human behaviour, and other social animals also exhibit phenomena in which individuals recover better from aversive events when conspecifics are present - aka social buffering. Here we studied social buffering in zebrafish, by exposing focal fish to an aversive stimulus (alarm substance - AS) either in the absence or presence of conspecific cues. When exposed to AS in the presence of both olfactory (shoal water) and visual (sight of shoal) conspecific cues, focal fish exhibited a lower fear response than when tested alone, demonstrating social buffering in zebrafish. When separately testing each cue's effectiveness, we verified that the visual cue was more effective than the olfactory in reducing freezing in a persistent threat scenario. Finally, we verified that social buffering was independent of shoal size and coincided with a distinct pattern of co-activation of brain regions known to be involved in mammalian social buffering. Thus, this study suggests a shared evolutionary origin for social buffering in vertebrates, bringing new evidence on the behavioural, sensory and neural mechanisms underlying this phenomenon.
- 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.
- Social dominance modulates eavesdropping in zebrafishPublication . Abril-de-Abreu, Rodrigo; Cruz, Ana S.; Oliveira, Rui F.Group living animals may eavesdrop on signalling interactions between conspecifics and integrate it with their own past social experience in order to optimize the use of relevant information from others. However, little is known about this interplay between public (eavesdropped) and private social information. To investigate it, we first manipulated the dominance status of bystander zebrafish. Next, we either allowed or prevented bystanders from observing a fight. Finally, we assessed their behaviour towards the winners and losers of the interaction, using a custom-made video-tracking system and directional analysis. We found that only dominant bystanders who had seen the fight revealed a significant increase in directional focus (a measure of attention) towards the losers of the fights. Furthermore, our results indicate that information about the fighters' acquired status was collected from the signalling interaction itself and not from post-interaction status cues, which implies the existence of individual recognition in zebrafish. Thus, we show for the first time that zebrafish, a highly social model organism, eavesdrop on conspecific agonistic interactions and that this process is modulated by the eavesdroppers' dominance status. We suggest that this type of integration of public and private information may be ubiquitous in social learning processes.