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- Agonistic behaviour and shoal composition of juvenile Diplodus sargus : First field observationsPublication . Gonçalves, Ana R.; Silva, Matheus Augusto Farias da; Vendrell, Catarina L.; Almada, Vítor CarvalhoBehavioural observations of juvenile Diplodus sargus in natural habitats were conducted to test whether agonistic interactions occur in natural circumstances and, if they do, in which context they happen. The level of aggression and the shoals composition were also compared between distinct natural habitats. Behavioural observations were also conducted in captivity, and the level of aggression was comparedwith the level recorded in natural conditions to investigate which factors may promote aggressive behaviours. The observations were performed at two sites in the Atlantic Portuguese shore: São Pedro do Estoril (38°41′N, 9°22′W) and Cabo Raso (38°42′N, 9°29′W) from early July to late August 2010 and from late July to early October 2011, respectively. In nature agonistic behaviours do occur, with a higher frequency in pools than in open areas. However, even the highest values observed in nature are significantly lower than those reported for captive conditions. Shoal composition also changed in different habitats, with more members and aggregates more compact in open areas.We suggested that the high levels of aggression observed in captive groups may be an artefact caused by very high densities in confined spaces and eventually by the accumulation of chemicals that are known to be released by stressed fish and can be detected by other conspecifics. The confinement imposed in captivity may also affect shoal composition limiting the number of members and inter-individual distances in each group.
- Agonistic interactions elicit rapid changes in brain nonapeptide levels in zebrafishPublication . Teles, Magda; Gozdowska, Magdalena; Kalamarz-Kubiak, Hanna; Kulczykowska, Ewa; Oliveira, Rui FilipeThe teleost fish nonapeptides, arginine vasotocin (AVT) and isotocin (IT), have been implicated in the regulation of social behavior. These peptides are expected to be involved in acute and transient changes in social context, in order to be efficient in modulating the expression of social behavior according to changes in the social environment. Here we tested the hypothesis that short-term social interactions are related to changes in the level of both nonapeptides across different brain regions. For this purpose we exposed male zebrafish to two types of social interactions: (1) real opponent interactions, from which a Winner and a Loser emerged; and (2) mirror-elicited interactions, that produced individuals that did not experience a change in social status despite expressing similar levels of aggressive behavior to those of participants in real-opponent fights. Non-interacting individuals were used as a reference group. Each social phenotype (i.e. Winners, Losers, Mirror-fighters) presented a specific brain profile of nonapeptides when compared to the reference group. Moreover, the comparison between the different social phenotypes allowed to address the specific aspects of the interaction (e.g. assessment of opponent aggressive behavior vs. self-assessment of expressed aggressive behavior) that are linked with neuropeptide responses. Overall, agonistic interactions seem to be more associated with the changes in brain AVT than IT, which highlights the preferential role of AVT in the regulation of aggressive behavior already described for other species.
- Anaesthesia and analgesia in laboratory adult zebrafish: A question of refinementPublication . Martins, Tânia D.; Valentim, Ana M.; Pereira, Nuno Marques; Antunes, Luis M.Anaesthesia is used daily in fish experimental procedures; however, the use of an inadequate anaesthetic protocol can compromise not only the animal’s welfare but also the reliability of results. The use of zebrafish (Danio rerio) in biomedical research has increased in the last decades, highlighting the importance of appropriate anaesthetic regimens for this species. This article reviews the main anaesthetic agents and protocols used in laboratory adult zebrafish, and some of the analgesic methods to be used in this species that still need more research. In addition, a systematized observation of signs is proposed to evaluate adult zebrafish welfare to reduce pain and distress.
- Androgen response to social competition in a shoaling fishPublication . Teles, Magda; Oliveira, Rui FilipeAndrogens respond to social challenges and this response has been interpreted as a way for males to adjust androgen-dependent behavior to social context. However, the androgen responsiveness to social challenges varies across species and a conceptual framework has been developed to explain this variation according to differences in the mating system and parental care type, which determines the regimen of challenges males are exposed to, and concomitantly the scope (defined as the difference between the physiological maximum and the baseline levels) of response to a social challenge. However, this framework has been focused on territorial species and no clear predictions have been made to gregarious species (e.g. shoaling fish), which although tolerating same-sex individuals may also exhibit intra-sexual competition. In this paper we extend the scope of this conceptual framework to shoaling fish by studying the endocrine response of zebrafish (Danio rerio) to social challenges. Male zebrafish exposed to real opponent agonistic interactions exhibited an increase in androgen levels (11-ketotestosterone both in Winners and Losers and testosterone in Losers). This response was absent in Mirror-fighters, that expressed similar levels of aggressive behavior to those of winners, suggesting that this response is not a mere reflex of heightened aggressive motivation. Cortisol levels were also measured and indicated an activation of the hypothalamic-pituitary-interrenal axis in Winners of real opponent fighters, but not Losers or in Mirror-fighters. These results confirm that gregarious species also exhibit an endocrine response to an acute social challenge.
- Arginine vasotocin modulates associative learning in a mutualistic cleaner fishPublication . Cardoso, Sónia C.; Bshary, Redouan; Mazzei, Renata; Paitio, José R.; Oliveira, Rui Filipe; Soares, Marta C.Social environmental complexity induces structural and biochemical changes in animals’ brains, which are linked to the improvement of animals’ learning abilities. The nonapeptides from the arginine vasopressin (AVP) family (arginine vasotocin, AVT, in non-mammals) play a significant role in the regulation of social behavior, particularly in the formation of social memories and individual recognition. Moreover, the role of AVT in the regulation of interspecific interactions has only recently started to be addressed in the context of cleaner fish mutualisms and learning. Variance in the distribution of AVP receptor expression, which is linked to distinct neural systems (related to the dorsolateral and the dorsomedial telencephalon), is known to be implicated in differences in individual learning processes. Here we asked if the associative learning performance of the Indo-Pacific bluestreak cleaner wrasse (Labroides dimidiatus) is regulated by AVT. We tested the influence of AVT upon the cleaners’ ability to solve two different problems (cue and place discrimination tasks) that in principle differ in ecological relevance and are associated with two different memory systems. We found that AVT affected the learning competence of cleaners differently between tasks, as individual performance showed distinct response selectivity to AVT dosage levels. However, only in the ecologically relevant task was their learning response improved by blocking AVT via treatment with the antagonist Manning compound. Our findings demonstrate that AVT pathways, which are implicated in the regulation of interspecific behavior (i.e., a cleaner’s willingness to seek interactions with clients), are also linked to individual learning ability in the context of mutualistic behavior, and in tune with socio-ecological demands.
- Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brainPublication . Oliveira, Rui Filipe; Simões, José Miguel; Teles, Magda; Oliveira, Catarina R.; Becker, Jorg D.; Lopes, João SollariGroup living animals must be able to express different behavior profiles depending on their social status. Therefore, the same genotype may translate into different behavioral phenotypes through socially driven differential gene expression. However, how social information is translated into a neurogenomic response and what are the specific cues in a social interaction that signal a change in social status are questions that have remained unanswered. Here, we show for the first time, to our knowledge, that the switch between status-specific neurogenomic states relies on the assessment of fight outcome rather than just on self- or opponent-only assessment of fighting ability. For this purpose, we manipulated the perception of fight outcome in male zebrafish and measured its impact on the brain transcriptome using a zebrafish whole genome gene chip. Males fought either a real opponent, and a winner and a loser were identified, or their own image on a mirror, in which case, despite expressing aggressive behavior, males did not experience either a victory or a defeat. Massive changes in the brain transcriptome were observed in real opponent fighters, with losers displaying both a higher number of differentially expressed genes and of coexpressed gene modules than winners. In contrast, mirror fighters expressed a neurogenomic state similar to that of noninteracting fish. The genes that responded to fight outcome included immediate early genes and genes involved in neuroplasticity and epigenetic modifications. These results indicate that, even in cognitively simple organisms such as zebrafish, neurogenomic responses underlying changes in social status rely on mutual assessment of fighting ability.
- Audience effects and aggressive priming in agonistic behaviour of male zebrafish, Danio rerioPublication . Cruz, Ana S.; Oliveira, Rui FilipeAnimals communicate through the exchange of signals. However, third-party individuals can detect and intercept signals not directly sent to them, a phenomenon known as eavesdropping, and the presence of bystanders can influence the signalling behaviour of interacting conspecifics, a phenomenon named the audience effect. So far, research done on audience effects and eavesdropping has been mainly focused on their function, rather than on their proximate mechanisms. For this reason, we were interested in testing the occurrence of audience effects on male zebrafish, a genetically tractable model organism that is emerging as a major candidate for the study of the neural basis of social behaviour. Here, pairs of males were exposed to a mixed-sex shoal, which was used as an audience, at two different times: (1) during a contest between them, to test for an audience effect and (2) before the contest, to test whether this prior exposure influences subsequent agonistic behaviour (i.e. aggressive priming). We analysed the pairs' aggressive signalling during the contest by measuring variables that characterize both the individuals' behaviour and the interaction, and found that pre-exposure to an audience induced a shorter latency to display, an increase in the time dominants spent chasing subordinates and a shorter time to resolve the agonistic interaction. Also, exposure to the audience during the interaction led to a higher number of interactions in which displays occurred, a higher number of resolved interactions with displays and a decrease in the escalation of aggression for resolved interactions. These results add zebrafish to the literature on the audience effect and, most importantly, open the way for the study of the neural mechanisms involved in the processing of social information in a model organism.
- 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 Sollari; Oliveira, Rui FilipeAnimals 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.
- Autism-associated gene shank3 is necessary for social contagion in zebrafishPublication . Kareklas, Kyriacos; Teles, Magda C; Dreosti, Elena; Oliveira, Rui F.Background Animal models enable targeting autism-associated genes, such as the shank3 gene, to assess their impact on behavioural phenotypes. However, this is often limited to simple behaviours relevant for social interaction. Social contagion is a complex phenotype forming the basis of human empathic behaviour and involves attention to the behaviour of others for recognizing and sharing their emotional or affective state. Thus, it is a form of social communication, which constitutes the most common developmental impairment across autism spectrum disorders (ASD). Methods Here we describe the development of a zebrafish model that identifies the neurocognitive mechanisms by which shank3 mutation drives deficits in social contagion. We used a CRISPR-Cas9 technique to generate mutations to the shank3a gene, a zebrafish paralogue found to present greater orthology and functional conservation relative to the human gene. Mutants were first compared to wild types during a two-phase protocol that involves the observation of two conflicting states, distress and neutral, and the later recall and discrimination of others when no longer presenting such differences. Then, the whole-brain expression of different neuroplasticity markers was compared between genotypes and their contribution to cluster-specific phenotypic variation was assessed. Results The shank3 mutation markedly reduced social contagion via deficits in attention contributing to difficulties in recognising affective states. Also, the mutation changed the expression of neuronal plasticity genes. However, only downregulated neuroligins clustered with shank3a expression under a combined synaptogenesis component that contributed specifically to variation in attention. Limitations While zebrafish are extremely useful in identifying the role of shank3 mutations to composite social behaviour, they are unlikely to represent the full complexity of socio-cognitive and communication deficits presented by human ASD pathology. Moreover, zebrafish cannot represent the scaling up of these deficits to higher-order empathic and prosocial phenotypes seen in humans. Conclusions We demonstrate a causal link between the zebrafish orthologue of an ASD-associated gene and the attentional control of affect recognition and consequent social contagion. This models autistic affect-communication pathology in zebrafish and reveals a genetic attention-deficit mechanism, addressing the ongoing debate for such mechanisms accounting for emotion recognition difficulties in autistic individuals.
- A behavioral perspective on the biophysics of the light-dependent magnetic compass: a link between directional and spatial perception?Publication . Phillips, John B.; Muheim, R.; Jorge, P. E.In terrestrial organisms, sensitivity to the Earth's magnetic field is mediated by at least two different magnetoreception mechanisms, one involving biogenic ferromagnetic crystals (magnetite/maghemite) and the second involving a photo-induced biochemical reaction that forms long-lasting, spin-coordinated, radical pair intermediates. In some vertebrate groups (amphibians and birds), both mechanisms are present; a light-dependent mechanism provides a directional sense or 'compass', and a non-light-dependent mechanism underlies a geographical-position sense or 'map'. Evidence that both magnetite- and radical pair-based mechanisms are present in the same organisms raises a number of interesting questions. Why has natural selection produced magnetic sensors utilizing two distinct biophysical mechanisms? And, in particular, why has natural selection produced a compass mechanism based on a light-dependent radical pair mechanism (RPM) when a magnetite-based receptor is well suited to perform this function? Answers to these questions depend, to a large degree, on how the properties of the RPM, viewed from a neuroethological rather than a biophysical perspective, differ from those of a magnetite-based magnetic compass. The RPM is expected to produce a light-dependent, 3-D pattern of response that is axially symmetrical and, in some groups of animals, may be perceived as a pattern of light intensity and/or color superimposed on the visual surroundings. We suggest that the light-dependent magnetic compass may serve not only as a source of directional information but also provide a spherical coordinate system that helps to interface metrics of distance, direction and spatial position.