Roleira, António; Oliveira, Gonçalo A.; Lopes, João Sollari; Oliveira, Rui Filipe
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...
Madeira, Natália; Oliveira, Rui Filipe
In species in which individuals live in stable social groups, individual recognition is expected to evolve to allow individuals to remember past interactions with different individuals and adjust future behavior toward them accordingly. Thus, social memory is expected to be a ubiquitous component of social cognition of social species. However, few studies have investigated the occurrence of social memory in non-mammals. Here we evaluated the ability of zebrafish (Danio rerio) to recognize different conspecifics and to retain this information in long lasting (i.e. 24 h) memories. We used a social discrimination paradigm, adapted from mouse studies, in which the focal individual...
Faustino, Ana Isabel Soares; Tacão-Monteiro, André; Oliveira, Rui Filipe
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...
Wircer, Einav; Blechman, Janna; Borodovsky, Nataliya; Tsoory, Michael; Nunes, Ana Rita; Oliveira, Rui Filipe; Levkowitz, Gil
Proper response to stress and social stimuli depends on orchestrated development of hypothalamic neuronal circuits. Here we address the effects of the developmental transcription factor orthopedia (Otp) on hypothalamic development and function. We show that developmental mutations in the zebrafish paralogous gene otpa but not otpb affect both stress response and social preference. These behavioral phenotypes were associated with developmental alterations in oxytocinergic (OXT) neurons. Thus, otpa and otpb differentially regulate neuropeptide switching in a newly identified subset of OXT neurons that co-express the corticotropin-releasing hormone (CRH). Single-cell analysis revealed that these neurons project mostly to the hindbrain and spinal...
Cardoso, Sara D.; Faustino, Ana Isabel Soares; Costa, Silvia S.; Valério, Fábio; Gonçalves, David; Oliveira, Rui Filipe
Material suplementar está disponível online em doi: 10.1007/s10211-016-0249-9, disponibilizado a todos os utilizadores autorizados.
Martins, Tânia; 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.
Abril-de-Abreu, Rodrigo; Cruz, Ana S.; Oliveira, Rui Filipe
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...
Teles, Magda; Gozdowska, Magdalena; Kalamarz-Kubiak, Hanna; Kulczykowska, Ewa; Oliveira, Rui Filipe
The 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...
Borges, Ana C.; Pereira, Nuno Marques; Franco, Maysa; Vale, Liliana; Pereira, Margarida; Cunha, Mónica V.; Amaro, Ana; Albuquerque, Teresa; Rebelo, Manuel
In the past two decades, zebrafish (Danio rerio)-based research has contributed to significant scientific advances. Still, husbandry and health programs did not evolve at the same pace, as evidenced by the absence of general guidelines. Health monitoring is essential to animal welfare, to permit animal exchanges across facilities, to contribute to robust experimental results, and for data reproducibility. In this study, we report a health program implemented in a zebrafish research facility to prevent, monitor, and control pathogen, and disease dissemination. This program includes quarantine, routine health screening of sentinels, and nonroutine screenings of retired animals and sick/moribund individuals. An...
Oliveira, Rui Filipe; Simões, José Miguel; Teles, Magda; Oliveira, Catarina R.; Becker, Jorg D.; Lopes, João Sollari
Group 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....
Teles, Magda; Oliveira, Rui Filipe
Androgens 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...
Fagundes, Teresa; Simões, Mariana G.; Saraiva, João Luis Vargas de Almeida; Ros, Albert F. H.; Gonçalves, David; Oliveira, Rui Filipe
1. In species with plastic expression of alternative reproductive tactics (ARTs), individuals of
the same sex, usually males, can adopt different reproductive tactics depending on factors such
as body size.
2. The ‘birth date hypothesis’ proposes that condition-dependent expression of ARTs may
ultimately depend on birth date, because individuals born at different times of the year may
achieve different sizes and express different reproductive tactics accordingly. However, this has
rarely been tested.
3. Here, we tested this hypothesis in a fish with ARTs, the peacock blenny (Salaria pavo). A
long-term (6 years) mark–recapture study demonstrated that ARTs in the peacock blenny were
sequential and that males may follow at...
Lopes, João Sollari; Abril-de-Abreu, Rodrigo; Oliveira, Rui Filipe
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...
Teles, Magda; Almeida, Olinda; Lopes, João Sollari; Oliveira, Rui Filipe
According to the social decision-making (SDM) network hypothesis, SDM is encoded in a network of forebrain and midbrain structures in a distributed and dynamic fashion, such that the expression of a given social behaviour is better reflected by the overall profile of activation across the different loci rather than by the activity of a single node. This proposal has the implicit assumption that SDM relies on integration across brain regions, rather than on regional specialization. Here we tested the occurrence of functional localization and of functional connectivity in the SDM network. For this purpose we used zebrafish to map different...
Cruz, Ana S.; Oliveira, Rui Filipe
Animals 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...
Abril-de-Abreu, Rodrigo; Cruz, José; Oliveira, Rui Filipe
Group living animals may eavesdrop on signalling interactions between conspecifics in order to
collect adaptively relevant information obtained from others, without incurring in the costs of firsthand
information acquisition. This ability (aka social eavesdropping) is expected to impact Darwinian
fitness, and hence predicts the evolution of cognitive processes that enable social animals to use
public information available in the environment. These adaptive specializations in cognition may have
evolved both at the level of learning and memory mechanisms, and at the level of input mechanisms,
such as attention, which select the information that is available for learning. Here we used zebrafish
to test if attention in a social...
Penteriani, Vincenzo; Delgado, Maria del Mar; Campioni, Letizia
To date, animal movement studies have mostly
analysed the movement behaviours of individuals at specific
times of their lives, but we lack detailed information on how
individual movements may be affected by the various and
different changes that individuals experience throughout their
life (e.g. life history phases, experience, age). Here, we attempt
to identify differences in home range and movement
behaviour between two different statuses, disperser vs. breeder,
of a long-lived species (the eagle owl Bubo bubo).
Information on home range and movement behaviour between
different stages of an individual life are crucial for species
conservation and management, as well as for basic
knowledge on space use and rhythm of activity. Does...
Faustino, Ana Isabel Soares; Oliveira, Gonçalo A.; Oliveira, Rui Filipe
In fluctuating environments, organisms require mechanisms enabling the rapid
expression of context-dependent behaviors. Here, we approach behavioral flexibility from
a perspective rooted in appraisal theory, aiming to provide a better understanding on
how animals adjust their internal state to environmental context. Appraisal has been
defined as a multi-component and interactive process between the individual and the
environment, in which the individual must evaluate the significance of a stimulus to
generate an adaptive response. Within this framework, we review and reframe the
existing evidence for the appraisal components in animal literature, in an attempt to reveal
the common ground of appraisal mechanisms between species. Furthermore, cognitive
biases may occur in...
Cardoso, Sónia C.; Grutter, Alexandra S.; Paula, José R.; André, Gonçalo I.; Messias, João P.; Gozdowska, Magdalena; Kulczykowska, Ewa; Soares, Marta C.
Animals establish privileged relationships with specific partners, which are treated differently from other conspecifics, and contribute to behavioral variation. However, there is limited information on the underlying physiological mechanisms involved in the establishment of these privileged ties and their relationship to individual cooperation levels. The Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus often forages in mixed-sex pairs when cleaning fish clients. Intra-couple conflicts often arise during a joint client inspection, which may alter the overall quality of cleaning service provided. Here we tested two hypotheses: a) whether intra-pair association (i.e. association index), measured with joint interspecific cleaning and intraspecific behavior, is...
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