Abstract
Serotonin or 5-hydroxytryptamine (5-HT) is a monoaminergic neurotransmitter that is known to influence behaviour in various animal species. Its actions, however, are complex and not well-understood yet. Here, we tested whether and how two 5-HT receptor agonists and a 5-HT receptor antagonist influence behaviour in common waxbills (Estrilda astrild), focusing on aggression, movement and feeding. We applied acute administration of either 8-OH-DPAT (a 5-HT1A receptor agonist), fluoxetine (a selective serotonin reuptake inhibitor; SSRI) or WAY 100,635 (a 5-HT1A receptor antagonist), and then quantified behaviour in the context of competition for food. Waxbills treated with the SSRI fluoxetine showed an overall decrease of aggressive behaviour, activity and feeding, while we found no significant effects of treatment with the other serotonergic enhancer (8-OH-DPAT) or with the antagonist WAY 100,635. Since both 8-OH-DPAT and WAY 100,635 act mainly on 5-HT1A receptor pathways, while fluoxetine more generally affects 5-HT pathways, our results suggest that receptors other than 5-HT1A are important for serotonergic modulation of waxbill behaviour.
Significance statement
The serotonergic system is of interest for current behavioural research due to its influence on a range of behaviours, including aggression, affiliative behaviour, feeding and locomotion in various species. There are, however, numerous discrepancies regarding the behavioural effects of serotonin across studies. We used acute pharmacological manipulations of the serotonergic system in common waxbills, using two serotonin enhancers (8-OH-DPAT and fluoxetine) and a serotonin blocker (WAY 100,635). Behavioural effects of these pharmacological manipulations on aggressiveness, movement and feeding, during tests of competition over food, indicated an anxiogenic-like effect of fluoxetine, but not of 8-OH-DPAT and WAY 100,635. This suggests a distinct role for different serotonergic pathways on waxbill behaviour.
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Introduction
The behaviour of social and gregarious animals is often adapted to access and compete for resources such as food and mates within the group (Dickinson and Koenig 2018), and to establish dominance hierarchies (Drews 1993; Chase and Lindquist 2009; Paull et al. 2010; Ziomkiewicz 2016; Theodoridi et al. 2017). In many animal species, the mechanisms underlying aspects of social behaviour, including aggressive and impulsive behaviours, involve serotonergic function (e.g., Brown et al. 1979; Popova et al. 1997; Duke et al. 2013), which is a critical neural circuitry mediating context-dependent modulation of behaviour (Oliveira 2009). Serotonergic modulation can, affect multiple aspects of behaviour, including aggressive responses, mood, impulsivity, locomotor activity, affiliation and feeding, in both invertebrates and vertebrates (e.g. Evenden and Ängeby-Möller 1990; Saadoun and Cabrera 2002; Tse and Bond 2002; Ögren et al. 2008; Schweighofer et al. 2008; Oliveira 2009; Crockett et al. 2010; Mennigen et al. 2010; Kiser et al. 2012; Maximino et al. 2013; Björklund Aksoy 2017; Stettler et al. 2021), including birds (Steffens et al. 1997; Sperry et al. 2003; Dennis et al. 2008, 2013; dos Santos et al. 2015).
The role of serotonin (5-HT) in aggression and its relation to other behavioural dimensions, such as affiliation, feeding or movement, can be complex, with responses often depending on species’ identity, dosages used, social status or context (Hillegaart and Hjorth 1989; Evenden and Ängeby-Möller 1990; Steffens et al. 1997; Kravitz 2000; Harrison and Markou 2001; Saadoun and Cabrera 2002; Sperry et al. 2003; Gaworecki and Klaine 2008; Mennigen et al. 2010; Barry 2013; dos Santos et al. 2015; Huntingford 2019). Key experimental evidence implicating 5-HT as mediator of aggression and other behaviours have come from studies with pharmacological manipulations, designed to selectively and/or generally facilitate or to inhibit the serotonergic pathways (Tse and Bond 2002; Sperry et al. 2003; Dennis et al. 2008; Lorenzi et al. 2009; Lillesaar 2011; Maximino et al. 2013; Björklund Aksoy 2017). For instance, enhancing serotonergic function has been found to diminish aggressiveness in mammals (Olivier et al. 1995; Adams et al. 1996, Lopez-Mendoza et al. 1998), birds (Fachinelli et al. 1996; Sperry et al. 2003), fish (Winberg et al. 2001; Clotfelter et al. 2007; Dzieweczynski et al. 2016; Stettler et al. 2021), reptiles (Deckel 1996) as well as in crustaceans (Huber et al. 1997; Kravitz 2000). Suppressing serotonergic action has revealed opposite effects, with treated individuals seemingly becoming more aggressive, in a variety of model systems that include humans (Crockett et al. 2008, 2009), rodents (Lopez-Mendoza et al. 1998; de Boer et al. 1999, 2000;), birds (i.e., Buchanan et al. 1994) and fish species (Clotfelter et al. 2007; Paula et al. 2015; Stettler et al. 2021). Unsurprisingly, some discrepancies have been found between study species, treatments, dosages used and experimental contexts, as seen in Stettler et al. (2021), for example, where the agonist 8-OH-DPAT increased aggression in a cooperatively breeding cichlid (Neolamprologus pulcher), and the antagonist WAY 100,635 decreased aggression.
Behaviours like foraging or locomotion can also be affected by 5-HT, for example with serotonergic function reducing feeding motivation (e.g., birds: Saadoun and Cabrera 2002; fish: Gaworecki and Klaine 2008; Mennigen et al. 2010), but here too some discrepant results have been found (Steffens et al. 1997; dos Santos et al. 2015). With serotonergic enhancers like 8-OH-DPAT (agonist) and fluoxetine (a selective serotonin reuptake inhibitor, SSRI) either increasing or decreasing locomotor behaviour, depending on the study species (e.g.: rodents: Hillegaart and Hjorth 1989; Evenden and Ängeby-Möller 1990; Harrison and Markou 2001; and fish: Kohlert et al. 2012; Barry 2013; Dzieweczynski et al. 2016).
5-HT activity is affected by a large family of receptors, with the 5-HT1A and 5-HT1B subtypes being particularly influential in the modulation of several behaviours, including aggressiveness (e.g., humans: Nelson and Chiavegatto 2001; rodents: Olivier et al. 1995; de Boer and Koolhaas 2005; birds: Dennis et al. 2008). The 5-HT1A-like receptors are divided into two distinct groups based on their neural location: i) autoreceptors, known to suppress firing of serotonergic neurons when activated, therefore reducing 5-HT activity (Sprouse and Aghajanian 1987; Polter and Li 2010; dos Santos et al. 2015); and ii) heteroreceptors, that, when activated, execute intracellular effects (Carey et al. 2004; Polter and Li 2010). However, in avian models, information on serotonergic mechanisms underlying behavioural mediation, receptors and specific pathways is yet sparse (Buchanan et al. 1994; Sperry et al. 2003; Dennis et al. 2008, 2013).
Since there is limited information on the influence of serotonergic mediation in avian behaviour, we chose to focus on its effects in the common waxbills (Estrilda astrild), a highly gregarious bird found in flocks year-round, roosting, allopreening and bathing communally (Clement et al. 1993; Payne 2010). The common waxbill is, therefore, ideal to study the influence of 5-HT on behaviour, as this neurotransmitter may affect the drive to be social (Young 2013). Groups of common waxbills (hereafter, waxbills) form dominance hierarchies with mildly steep slopes, meaning that dominant individuals may sometimes be displaced by lower ranked birds, and individual differences in aggressiveness can be studied with behavioural trials of competition for food (Funghi et al. 2015, 2018; Beltrão et al. 2021a). Although there are repeatable individual differences in aggressiveness and social dominance, male and female waxbills are on average similarly aggressive and dominant (Funghi et al. 2015, 2018; Beltrão et al. 2021a, b). In this study, we focused on 5-HT1A receptors due to their widespread distribution in the brain (e.g., humans: Saulin et al. 2012; pigeon, Columba livia: dos Santos et al. 2015). We treated waxbills with 8-OH-DPAT (a 5-HT1A receptor agonist), WAY 100,635 (a 5-HT1A receptor antagonist) and fluoxetine (a SSRI that prevents 5-HT reuptake) and observed their overall locomotor activity, feeding, aggressiveness and allopreening, to investigate serotonergic effects on behaviour. Following most existing studies, usually using non-avian models, we hypothesized that the agonist 8-OH-DPAT and the SSRI fluoxetine would decrease waxbill aggressiveness and increase affiliative interactions, while the antagonist WAY 100,635 would have opposite effects. Our study is one of the few done in birds and analysing both sexes.
Material and methods
Model species
We acquired 24 adult wild-type common waxbills (12 males and 12 females), aged approximately around 3–4 years, from certified breeders in September 2019 and housed them in a room with birdcages at CIBIO (Vairão, Portugal). The birds were ringed for individual identification and housed in six cages, in mixed-sex groups of 4 birds per cage (2 males and 2 females), remaining in each designated cage until the end of experiments. These metal cages (88.5 × 30 × 40 cm) had 4 perches and a gridded front (Fig. 1). The room had natural ventilation, temperature, and light, complemented with light from full spectrum lamps on the ceiling, on a cycle adjusted to the natural photoperiod (lights on ca. 30 min before sunrise, and off ca. 30 min after dawn). The birds were provided with ad libitum food (a commercial mix of seeds for exotics birds, Tropical Finches Prestige, Versele-Laga, composed by panicum yellow 42%, yellow millet 28%, japanese millet 11.5%, canary seed 8,5%, red millet 5%, panicum red 4%, niger seed 1%), water in two drinkers, mixed grit with crushed oyster shells (Grit with Coral Prestige, Versele-Laga) on the cage floor, to provide a calcium supplement, and bathtubs were made available twice a week.
Manipulation of the 5-HT system and experimental design
Experiments took place between September and November 2019, corresponding to the non-reproductive season of waxbills in the Iberian Peninsula (Sanz-Aguilar et al. 2015; Beltrão et al. 2021c). Also, for consistency, experiments took place during the morning, between 9:30am and 12:45 pm, since birds are generally more active during the morning, and to avoid hormonal variations that occur along the day. Two hours before each behavioural test, we food deprived birds by removing all feeders from a cage. After 1h40min of food deprivation, each bird of the same cage was briefly removed to receive an injection, with treatments scheduled in a balanced manner through time (see supplementary material Table A.1). Each bird was then returned to its cage after the injection, and after 20 min (completing 2 h of food deprivation) the behavioural test of competition for food started.
Each bird cage was tested once a week, with an interval of 7 days between tests on the same cage to prevent possible carry over effects of the treatments. There were seven rounds of tests, thus lasting 7 weeks in total, and the order of the treatments differed among cages in a balanced manner, so that date is not a confounding factor in the experiment (calendar in Table A.1). In one of the seven rounds, all 4 birds (2 males and 2 females) of the same cage received control treatment (PBS). In the other six remaining rounds, one male and one female in the cage received PBS, and the other male and female of the same cage received an injection with either 8-OH-DPAT, fluoxetine or WAY 100,635. Each individual received the 8-OH-DPAT, fluoxetine and WAY 100,635 treatments only once (Table A.1). This happened in all the six birdcages. All treatments (control, 8-OH-DPAT, fluoxetine and WAY 100,635) were administered by intramuscular injection on the right side of the chest, in the pectoral muscle. The volume of the injections was 20 µl, administered with insulin syringes of 0.5 ml (29G). Dosages were based on previous studies (song sparrows (Melospiza melodia morphna): Sperry et al. 2003; wild cleaner wrasses (Labroides dimidiatus): Paula et al. 2015), whose results indicated that the dosages were able to produce significant biological effects without causing harm to the individuals. These were as follow: 1 mg kg-1 of body mass of 5-HT1A receptor agonist 8-OH-DPAT (H8520 Sigma-Aldrich, Darmstadt, Germany); 10 mg kg-1 of the selective 5-HT reuptake inhibitor (SSRI) fluoxetine (F132 Sigma-Aldrich); 1.5 mg kg-1 of the 5-HT1A receptor antagonist WAY 100,635 (W108 Sigma-Aldrich). These were diluted in 20 µl of phosphate-buffered saline (PBS). Dosages were adjusted to the mean body weight of waxbills (9 g), which we measured before the onset of experiments. The control injections consisted only of 20 µl of PBS.
Competition for food test
We used a behavioural test involving the competition for food to assess social aggressiveness, following protocols developed earlier for the waxbills (Funghi et al. 2015, 2018). After 2 h of food deprivation, we placed a feeder attached to the front grid in the centre of the cage (Fig. 1), and video recorded the behaviour of the birds for 15 min with a video camera (Canon LEGRIA HF M306) placed on a grid wall ca. 1.5 m in front of the test cage. From the recorded videos, we quantified five behavioural variables (data in Table A.2), using separate focal observations for each of the four individuals in the cage: 1) total duration at the feeder: the total time, in seconds, that the focal individual spent on all its visits to the feeder. 2) latency to the feeder: the amount of time, in seconds, that the focal individual took to go to the feeder for the first time. 3) movements: the total number of changes in position between six different areas in the cage: each of the four perches, the feeder and the ground. Every movement to a different area, whether adjacent to the initial area or more distant, was counted as one movement, and movements within the same area were not counted. 4) allopreening: the total amount of time, in seconds, that an individual preened or groomed another individual. 5) aggressiveness: the total number of aggressive displays or attacks made by the focal individual (i.e., opening the beak towards another individual with stretched neck and spread wings, displacements, pecking, chasing). Behavioural quantification of the videos was always performed by the same observer (BCS), using The Observer XT 11 (Noldus Information Techonology b.v., Wageningen, the Netherlands) and blind to the experimental treatment (names of the video files were coded).
Statistical analysis
Since two of the behavioural measures (e.g., ‘total duration at the feeder’ and ‘latency to the feeder’) both relate to feeding and were correlated (-0.583, p < 0.001), we summarized them with a principal component analysis (PCA) from the correlation matrix. The first principal component (hereafter ‘FeedingPC ‘) from this PCA explained 77.4% of variance and had a strong positive loading for ‘Total duration at the feeder’ (0.890) and a strong negative loading for ‘Latency to the feeder’ (-0.890). High scores indicate more time spent at the feeder and a lower latency to go there for the first time. The remaining behavioural variables were not strongly mutually correlated (all |r|≤ 0.55, using data from the control treatments; see Table A.3) and, since they refer to different behaviours and hypotheses, they were analysed separately. Inspection of histograms showed positively skewed distributions for ‘allopreening’ and ‘aggressiveness’, so they were log(x + 1) transformed to approach normality. The variables ‘movements’ and ‘FeedingPC’ showed approximately normal distributions. Data for ‘FeedingPC’ can also be found in Table A.2.
We ran general linear mixed models (GLMMs), separately for each of the four behavioural variables (‘FeedingPC’, ‘movements’, ‘allopreening’ and ‘aggressiveness’) to test for within-individual differences between the control treatment and any of the serotonergic treatments, using the lmer() function in the R package “lme4” (v.1.1–23; Bates et al. 2014). In each GLMM, a behavioural trait was the dependent variable, treatment (control, 8-OH-DPAT, fluoxetine or WAY 100,635) was included as a fixed factor, cage identity was included as a random factor, to account for possible non-independence of data from within the same cage, and individual identity was included as a random factor nested within cages, to control for between-individual differences in behaviour. As controls, we only used the data from tests where all four individuals in a cage received PBS injection. We report the GLMM contrasts (i.e., the simple coefficients, without having run an ANOVA on the GLMM), which tests for differences between the reference level of the treatment (the control treatment) and each of the remaining levels (8-OH-DPAT, fluoxetine or WAY 100,635). We examined residuals using the command check_model() in the R package “performance” (v 0.7.0; Lüdecke et al. 2020), and in all models residuals were approximately normally distributed, homoscedastic and with homogeneous variance in relation to fitted values. Since we tested three different compounds, we only consider an effect statistically significant when P is smaller than the Bonferroni-adjusted criterion for statistical of 0.05/3 = 0.017. All analyses were conducted in R v. 4.0.0 (R Core Team 2020). Since male and female waxbills had very similar responses to our experimental treatments (supplementary Fig. A.1) we report analyses for the two sexes together.
Results
Compared to the control treatment, treatment with the SSRI fluoxetine was associated with a lower FeedingPC score (i.e., longer latency to go to the feeder for the first time, and less time at the feeder; t69 = -2.726; p = 0.008, Fig. 2A; Table 1). FeedingPC scores when treated with 8-OH-DPAT or WAY 100,635 did not differ significantly from the control treatment (Table 1).
Treatment with the SSRI fluoxetine decreased movements compared to the control (t69 = -3.428; p = 0.001, Table 1, Fig. 2B). The number of movements when treated with 8-OH-DPAT or WAY 100,635 did not differ significantly from the control treatment (Table 1, Fig. 2B).
Compared to the control, fluoxetine significantly decreased aggressive behaviour (t69 = -2.819; p = 0.006, Table 1, Fig. 2C), while treatments with 8-OH-DPAT and WAY 100,635 did not change aggressive behaviour (Table 1, Fig. 2C). Finally, the amount of allopreening was not significantly affected by any of the treatments (Table 1, Fig. 2D).
Discussion
We tested if short term changes in 5-HT activity influenced waxbills aggression, feeding, movements and allopreening. As predicted, we found that treatment with fluoxetine, a selective 5-HT reuptake inhibitor (SSRI), resulted in an overall decrease of waxbill’s aggressive behaviour, activity and feeding. However, treatment with 8-OH-DPAT, a selective 5-HT1A receptor agonist, and WAY 100,635, a 5-HT1A receptor antagonist, did not show discernible effects on waxbill behaviour. In what follows, we discuss serotonergic effects for the studied behaviours separately.
Fluoxetine-treated waxbills decreased activity levels compared to controls. Similar effects have been demonstrated in some fish species, in which short-term exposure to fluoxetine suppressed activity (Beulig and Fowler 2008; Kohlert et al. 2012; Barry 2013; Dzieweczynski et al. 2016). These instances of hypoactivity may be interpreted as anxiety-like behaviour because fluoxetine is not usually described as sedative. Anxiety is a secondary response to stress, which may take many forms, occurring when the stressor is absent or not clearly identified (reviewed in Fossat et al. 2014; Bacqué-Cazenave et al. 2020). In our case, perhaps the test of competition for food (including the food deprivation period and handling) is a stressor whose effect serotonin action may intensify. Several studies in fish and rodent species, have also reported anxiogenic-like effects following acute treatment with SSRIs (Griebel et al. 1994; Sánchez and Meier 1997; Maximino et al. 2013; Theodoridi et al. 2017). Acute rises in 5-HT can either increase (Griebel et al. 1994; Bagdy et al. 2001) or decrease (Inoue et al. 1996, 2004; Sánchez and Meier 1997) anxiety-like responses (Grillon et al. 2007), because 5-HT affects multiple brain structures that mediate anxiety via different pathways and receptors (Graeff et al. 1997; Grillon et al. 2007). Fluoxetine, as a SSRI, does not act specifically on receptors but rather on 5-HT overall availability, thus it may, in theory, interact with all 5-HT receptors (Shirayama et al. 1993; Sánchez and Meier 1997). For instance, Bagdy et al. (2001) suggested that the anxiogenic-like responses after a single dose of SSRIs, like fluoxetine, could be attributable to the activation of 5-HT2C receptors in the amygdala (Westenberg and den Boer 1988; Griebel et al. 1994; Burghardt et al. 2004, 2007; Grillon et al. 2007) as the SSRI fluoxetine has been noted to be related with these receptor subtypes (Jenck et al. 1994; Pälvimäki et al. 1996; Bonhaus et al. 1997). Other studies support the affinity of the SSRI for the 5-HT2 receptor family (Hyttel 1994; Sánchez and Meier 1997; Peng et al. 2014), implying that it acts as an antagonist for the 5-HT2C receptors (Sánchez 1996; Sánchez and Meier 1997). Thus, our results might be attributable to pathways other than that involving the 5-HT1A receptor, as the SSRI fluoxetine may also present high affinity for 5-HT2C receptors. While at this point we cannot empirically demonstrate an influence of the 5-HT2C pathways in waxbill activity levels, we may nonetheless suggest that this hypothesis merits future additional research. Perhaps this link between 5-HT shifts and anxiety response enhances animals’ defence mechanisms, which may serve to protect them from numerous sources of dangers and inform other conspecifics of possible risks (Dickinson and Koenig 2018).
Unlike the case for the SSRI fluoxetine, we found that neither treatment with 8-OH-DPAT, a 5-HT1A receptor agonist, nor with the antagonist WAY 100,635 affected movement. 5-HT can modulate activity in a rather complex manner, with similar dosages or similar exposure times sometimes exerting distinct behavioural responses (reviewed in Bacqué-Cazenave et al. 2020; Flaive et al. 2020), which may explain why in our results only some 5-HT pathways but not all affected movement. For instance, in rodents, the activation of the 5-HT1A receptor usually produces anxiolytic-like effects (stimulate locomotor behaviour), depending on the site of injection and the type of 1A receptors being activated (Hillegaart and Hjorth 1989; Evenden and Ängeby-Möller 1990; Harrison and Markou 2001).
Regarding feeding behaviour, waxbills treated with the SSRI fluoxetine took longer to reach and spent less time at the feeder, similarly to previous results from studies in fish species (Gaworecki and Klaine 2008; Mennigen et al. 2010; Weinberger and Klaper 2014; Dzieweczynski et al. 2016). Similarly, to the results with movement, no other treatment (8-OH-DPAT and WAY 100,635) changed the feeding behaviour of waxbills. The absence of significant effects by WAY 100,635 on feeding response has been reported before, for example with pigeons (dos Santos et al. 2009).
In some species, treatment with 8-OH-DPAT decreased food intake (pigs: Ebenezer et al. 1999; chickens: Saadoun and Cabrera 2002), while it was also seen to increase food intake (pigeons: Steffens et al. 1997; dos Santos et al. 2015). 5-HT has been associated with an overall inhibitory effect of feeding (Denbow et al. 1982; Blundell 1984; Baranyiová 1990; Ebenezer et al. 1999; De Vry and Schreiber 2000; Saadoun and Cabrera 2002), but with little evidence for a relevant participation of the 5-HT1A receptor (but see Reis and Marinho 2005, for effects on quails Coturnix japonica, and Mancilla-Diaz et al. 2005, for brain region-specific effects on rats Rattus novergicus), thus explaining the absence of effects in waxbills’ feeding behaviour, for both the 5-HT1A receptor agonist and antagonist (8-OH-DPAT and WAY 100,635, respectively).
None of our experimental treatments affected the amount of allopreening but increasing serotonergic availability with fluoxetine resulted in fewer aggressive interactions. This latter result agrees with the meta-analysis of Carrillo et al. (2009), regarding the effects of pharmacological increases in 5-HT levels (with either SSRIs, 5-hydroxytryptophan, L-tryptophan, or 5-HT) on aggressive behaviour across vertebrates (birds, dogs, fish, hamsters, mice, rats, and monkeys), showing the overall inhibitory effect of higher levels of 5-HT on aggression. Since we found that fluoxetine also inhibited waxbill general activity and feeding, besides their aggressiveness, we cannot discard a general sedative effect of this drug in our birds. For example, in gerbils (Meriones unguicalatus), the effects of fluoxetine on social behaviour are influenced by previous housing conditions, with prosocial effects observed in individuals that were previously housed singly and sedative effects in individual previously maintained in groups (Hendrie et al. 2003). An alternative explanation is that fluoxetine produced anxiogenic effects, and in this way inhibited ongoing behaviours. In several species, acute SSRIs usually produce an anxiogenic-like effects in different behavioural paradigms (e.g., mouse: Mombereau et al. 2010; rat: Greenwood et al. 2008; fish: Maximino et al. 2013).
The inhibitory effect of acute fluoxetine on aggression has been most often attributed to the activation of both 5-HT1A and 5-HT1B autoreceptors, in several species (Piñeyro and Blier 1999; Sperry et al. 2003; Grillon et al. 2007; Beulig and Fowler 2008; Dennis et al. 2008; Gaworecki and Klaine 2008; Mennigen et al. 2010; Homberg 2012; Kohlert et al. 2012; Barry 2013), leading to a reduction of the firing rate of serotonergic neurons (Piñeyro and Blier 1999; Grillon et al. 2007; Homberg 2012), but also to its influence on the 5-HT2C pathway (de Moura et al. 2022). The activation of 5-HT1A receptors by treatment with a 5-HT1A receptor agonist has been shown to decrease aggression in some species (hamsters: Joppa et al. 1997; song sparrows: Sperry et al. 2003; fighting fish: Clotfelter et al. 2007;), although there are also studies where it increased aggression (chickens: Dennis et al. 2008; cichlid fish: Stettler et al. 2021). Also, the 5-HT1A receptor antagonist was shown to increase aggressiveness of treated bluestreak cleaner wrass females (Labroides dimidiatus) towards same-sex conspecifics (Paula et al. 2015), although other reports did not find similar effects (Sánchez 1997; Lopez-Mendoza et al. 1998; Bell et al. 1999; Clotfelter et al. 2007). In our experiments with waxbills, both 8-OH-DPAT and WAY 100,635 (5-HT1A receptor agonist and antagonist, respectively) did not affect aggression. In general, the lack of an effect for both treatments could be due to species differences (i.e., no participation of the 5-HT1A receptor on aggression in waxbills, 5-HT baseline levels), dose effects, or procedural differences.
In conclusion, fluoxetine treatment had a consistent effect in decreasing activity, feeding and aggressiveness in waxbills, producing an overall anxiogenic-like effect. No significant effects of 8-OH-DPAT and WAY 100,635 were found. Since 8-OH-DPAT and WAY 100,635 affect mainly 5-HT1A receptor pathways, it is possible that the effects of fluoxetine that we found were due to its action on the 5-HT2C receptor pathways instead. Our results may also be partially dependent on the dosage applied, resulting in hypoactivity under the effect of fluoxetine (Dagh 2013). Future studies should investigate potential effects when using different dosages, distinct time action frames, and other receptors that may also share a role in waxbills’ aggressive-like response, specifically on 5-HT2C receptor family.
Data availability
All data generated or analysed during this study are included in this published article (and its supplementary information files).
References
Adams CF, Liley NR, Gorzalka BB (1996) PCPA increases aggression in male firemouth cichlids. Pharmacology 53:328–330. https://doi.org/10.1159/000139446
Bacqué-Cazenave J, Bharatiya R, Barrière G, Delbecque J-P, Bouguiyoud N, Di Giovanni G, Cattaert D, De Deurwaerdère P (2020) Serotonin in animal cognition and behavior. Int J Mol Sci 21:1649. https://doi.org/10.3390/ijms21051649
Bagdy G, Graf M, Anheuer ZE, Modos EA, Kantor S (2001) Anxiety-like effects induced by acute fluoxetine, sertraline or m-CPP treatment are reversed by pretreatment with the 5-HT2C receptor antagonist SB-242084 but not the 5-HT1A receptor antagonist WAY-100635. Int J Neuropsychopharmacol 4:399–408. https://doi.org/10.1017/S1461145701002632
Baranyiová E (1990) Effects of serotonin on the food intake in chickens in the early post-hatching period. Acta Vet Brno 59:23–33. https://doi.org/10.2754/avb199059010023
Barry MJ (2013) Effects of fluoxetine on the swimming and behavioural responses of the Arabian killifish. Ecotoxicology 22:425–432. https://doi.org/10.1007/s10646-012-1036-7
Bates D, Maechler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using 482 lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bell R, Lynch K, Mitchell P (1999) Lack of effect of the 5-HT(1A) receptor antagonist WAY-100635 on murine agonistic behaviour. Pharmacol Biochem Behav 64:549–554. https://doi.org/10.1016/s0091-3057(99)00105-7
Beltrão P, Gomes ACR, Marques CI, Guerra S, Batalha HR, Cardoso GC (2021a) European breeding phenology of the invasive common waxbill, a sub-Saharan opportunistic breeder. Acta Ethol 24:197–203. https://doi.org/10.1007/s10211-021-00376-9
Beltrão P, Marques CIJ, Cardoso GC, Gomes ACR (2021b) Plumage colour saturation predicts long-term, cross-seasonal dominance in a social bird. Anim Behav 182:239–250. https://doi.org/10.1016/j.anbehav.2021.09.011
Beltrão P, Silva PA, Soares MC, Cardoso GC, Trigo S (2021c) Testosterone treatment produces sex-dependent effects in social dominance. Anim Behav 179:307–315. https://doi.org/10.1016/j.anbehav.2021.07.016
Beulig A, Fowler J (2008) Fish on prozac: effect of serotonin reuptake inhibitors on cognition in goldfish. Behav Neurosci 122:426–432. https://doi.org/10.1037/0735-7044.122.2.426
Björklund Aksoy S (2017) Effects of serotonin on personality in field crickets (Gryllus bimaculatus) Dissertation Linköping University
Blundell JE (1984) Serotonin and appetite. Neuropharmacology 23:1537–1551. https://doi.org/10.1016/0028-3908(84)90098-4
Bonhaus DW, Weinhardt KK, Taylor M et al (1997) RS102221: a novel high affinity and selective, 5-HT2C receptor antagonist. Neuropharmacology 36:621–629. https://doi.org/10.1016/S0028-3908(97)00049-X
Brown GL, Goodwin FK, Ballenger JC, Goyer PF, Major LF (1979) Aggression in humans correlates with cerebrospinal fluid amine metabolites. Psychiat Res 1:131–139. https://doi.org/10.1016/0165-1781(79)90053-2
Buchanan CP, Shrier EM, Hill WL (1994) Time-dependent effects of PCPA on social aggression in chicks. Pharmacol Biochem Behav 49:483–488. https://doi.org/10.1016/0091-3057(94)90059-0
Burghardt NS, Sullivan GM, McEwen BS, Gorman JM, LeDoux JE (2004) The selective serotonin reuptake inhibitor citalopram increases fear after acute treatment but reduces fear with chronic treatment: a comparison with tianeptine. Biol Psychiat 55:1171–1178. https://doi.org/10.1016/j.biopsych.2004.02.029
Burghardt NS, Bush DE, McEwen BS, LeDoux JE (2007) Acute selective serotonin reuptake inhibitors increase conditioned fear expression: blockade with a 5- HT(2C) receptor antagonist. Biol Psychiat 62:1111–1118. https://doi.org/10.1016/j.biopsych.2006.11.023
Carey RJ, Depalma G, Damianopoulos E, Müller CP, Huston JP (2004) The 5-HT1A receptor and behavioral stimulation in the rat: effects of 8-OHDPAT on spontaneous and cocaine-induced behavior. Psychopharmacology 177:46–54. https://doi.org/10.1007/s00213-004-1917-4
Carrillo M, Ricci LA, Coppersmith GA, Melloni RH Jr (2009) The effect of increased serotonergic neurotransmission on aggression: a critical meta-analytical review of preclinical studies. Psychopharmacology 205:349–368. https://doi.org/10.1007/s00213-009-1543-2
Chase I, Lindquist WB (2009) Dominance hierarchies. In: Hedström P, Bearman P (eds) The Oxford Handbook of Analytical Sociology. Oxford University Press, Oxford, UK, pp 566–591
Clement P, Harris A, Davis J (1993) Finches and sparrows. Princeton University Press, Princeton
Clotfelter ED, O’Hare EP, McNitt MM, Carpenter RE, Summers CH (2007) Serotonin decreases aggression via 5-HT1A receptors in the fighting fish Betta splendens. Pharmacol Biochem Behav 87:222–231. https://doi.org/10.1016/j.pbb.2007.04.018
Crockett MJ, Clark L, Tabibnia G, Lieberman MD, Robbins TW (2008) Serotonin modulates behavioral reactions to unfairness supplementary material. Science 320:1739. https://doi.org/10.1126/science.1155577
Crockett MJ, Clark L, Robbins TW (2009) Reconciling the role of serotonin in behavioural inhibition and aversion: Acute tryptophan depletion abolishes punishment-induced inhibition in humans. J Neurosci 29:11993–11999. https://doi.org/10.1523/JNEUROSCI.2513-09.2009
Crockett MJ, Clark L, Hauser MD, Robbins TW (2010) Serotonin selectively influences moral judgment and behavior through effects on harm aversion. P Natl Acad Sci USA 107:17433–17438. https://doi.org/10.1073/pnas.1009396107
Dagh J (2013) Zebrafish as a behavioral model acute fluoxetine effects on behavior and influence of sex Student report
de Boer SF, Koolhaas JM (2005) 5-HT1A and 5-HT1B receptor agonists and aggression: a pharmacological challenge of the serotonin deficiency hypothesis. Eur J Pharmacol 526:125–139. https://doi.org/10.1016/j.ejphar.2005.09.065
de Boer SF, Lesourd M, Mocaer E, Koolhaas JM (1999) Selective antiaggressive effects of alnespirone in resident–intruder test are mediated via 5-hydroxytryptamine1A receptors: a comparative pharmacological study with 8-hydroxy-2-dipropylaminotetralin, ipsapirone, buspirone, eltoprazine, and WAY-100635. J Pharmacol Exp Ther 288:1125–1133
de Boer SF, Lesourd M, Mocaer E, Koolhaas JM (2000) Somatodendritic 5-HT(1A) autoreceptors mediate the anti-aggressive actions of 5-HT(1A) receptor agonists in rats: an ethopharmacological study with S-15535, alnespirone, and WAY-100635. Neuropsychopharmacology 23:20–33. https://doi.org/10.1016/S0893-133X(00)00092-0
De Vry J, Schreiber R (2000) Effects of selected serotonin 5HT1 and 5HT2 receptor agonists on feeding behavior: possible mechanisms of action. Neurosci Biobehav Rev 24:341–353. https://doi.org/10.1016/S0149-7634(99)00083-4
Deckel AW (1996) Behavioral changes in Anolis carolinensis following injection with fluoxetine. Behav Brain Res 78:175–182. https://doi.org/10.1016/0166-4328(95)00246-4
Denbow DM, Van Krey HP, Cherry JA (1982) Feeding and drinking response of young chicks to injections of serotonin into the lateral ventricle of the brain. Poult Sci J 61:150–155. https://doi.org/10.3382/ps.0610150
Dennis RL, Chen ZQ, Cheng HW (2008) Serotonergic mediation of aggression in high and low aggressive chicken strains. Poultry Sci J 87:612–620. https://doi.org/10.3382/ps.2007-00389
Dennis RL, Lay DC, Cheng HW (2013) Effects of early serotonin programming on behavior and central monoamine concentrations in an avian model. Behav Brain Res 253:290–296. https://doi.org/10.1016/j.bbr.2013.07.043
Dickinson J, Koenig W (2018) Animal social behaviour In Encyclopedia Britannica Chicago
dos Santos M, Hoeller A, Santos T, Felisbino M, Herdt M, Simão da Silva E, Paschoalini M, Marino-Neto J (2009) Behavioural and electroencephalographic effects of systemic injections of 8-OH-DPAT in the pigeon (Columba livia). Behav Brain Res 201:244–256. https://doi.org/10.1016/j.bbr.2009.02.017
dos Santos TS, Krüger J, Melleu FF, Herold C, Zilles K, Poli A, Güntürkün O, Marino-Neto J (2015) Distribution of serotonin 5-HT1A-binding sites in the brainstem and the hypothalamus, and their roles in 5-HT-induced sleep and ingestive behaviors in rock pigeons (Columba livia). Behav Brain Res 295:45–63. https://doi.org/10.1016/j.bbr.2015.03.059
Drews C (1993) The concept and definition of dominance in animal behaviour. Behaviour 125:283–313
Duke AA, Bègue L, Bell R, Eisenlohr-Moul T (2013) Revisiting the serotonin-aggression relation in humans: a meta-analysis. Psychol Bull 139:1148–1172. https://doi.org/10.1037/a0031544
Dzieweczynski TL, Campbell BA, Kane JL (2016) Dose-dependent fluoxetine effects on boldness in male Siamese fighting fish. J Exp Biol 219:797–804. https://doi.org/10.1242/jeb.132761
Ebenezer IS, Parrot RF, Velluci SV (1999) Effects of the 5-HT1A receptor agonists 8-OH-DPAT on operant food intake in food-deprived pigs. Physiol Behav 67:213–217. https://doi.org/10.1016/s0031-9384(99)00050-5
Evenden JL, Ängeby-Möller K (1990) Effects of 8-hydroxy-2-(di-n-propylamino) tetralin (8-OH-DPAT) on locomotor activity and rearing of mice and rats. Psychopharmacology 102:485–491. https://doi.org/10.1007/BF02247129
Fachinelli C, Ison M, Rodríguez Echandía EL (1996) Effect of subchronic and chronic exposure to 5-hydroxytryptophan (5-HTP) on the aggressive behavior induced by food competition in undernourished dominant and submissive pigeons (Columba livia). Behav Brain Res 75:113–118. https://doi.org/10.1016/0166-4328(96)00178-7
Flaive A, Fougère M, van der Zouwen CI, Ryczko D (2020) Serotonergic modulation of locomotor activity from basal vertebrates to mammals. Front Neural Circuit 14:590299. https://doi.org/10.3389/fncir.2020.590299
Fossat P, Bacqué-Cazenave J, De Deurwaerdère P, Delbecque JP, Cattaert D (2014) Comparative behavior. Anxiety-like behavior in crayfish is controlled by serotonin. Science 344:1293–1297. https://doi.org/10.1126/science.1248811
Funghi C, Leitão AV, Ferreira AC, Mota PG, Cardoso GC (2015) Social dominance in a gregarious bird is related to body size but not to standard personality assays. Ethology 121:84–93. https://doi.org/10.1111/eth.12318
Funghi C, Trigo S, Gomes ACR, Soares MC, Cardoso GC (2018) Release from ecological constraint erases sex difference in social ornamentation. Behav Ecol Sociobiol 72:67. https://doi.org/10.1007/s00265-018-2486-6
Gaworecki KM, Klaine SJ (2008) Behavioral and biochemical responses of hybrid striped bass during and after fluoxetine exposure. Aquat Toxicol 88:207–213. https://doi.org/10.1016/j.aquatox.2008.04.011
Graeff FG, Viana MB, Mora PO (1997) Dual role of 5-HT in defense and anxiety. Neurosci Biobehav Rev 21:791–799. https://doi.org/10.1016/s0149-7634(96)00059-0
Greenwood BN, Strong PV, Brooks L, Fleshner M (2008) Anxiety-like behaviors produced by acute fluoxetine administration in male Fischer 344 rats are prevented by prior exercise. Psychopharmacology 199:209–222. https://doi.org/10.1007/s00213-008-1167-y
Griebel G, Moreau JL, Jenck F, Misslin R, Martin JR (1994) Acute and chronic treatment with 5-HT reuptake inhibitors differentially modulate emotional responses in anxiety models in rodents. Psychopharmacology 113:463–470. https://doi.org/10.1007/BF02245224
Grillon C, Levenson J, Pine DS (2007) A single dose of the selective serotonin reuptake inhibitor citalopram exacerbates anxiety in humans: A fear-potentiated startle study. Neuropsychopharmacology 32:225–231. https://doi.org/10.1038/sj.npp.1301204
Harrison AA, Markou A (2001) Serotonergic manipulations both potentiate and reduce brain stimulation reward in rats: involvement of serotonin-1A receptors. J Pharmacol Exp Ther 297:316–325
Hendrie CA, Pickles AR, Duxon MS, Riley G, Hagan JJ (2003) Effects of fluoxetine on social behaviour and plasma corticosteroid levels in female Mongolian gerbils. Behav Pharmacol 14:545–550. https://doi.org/10.1097/00008877-200311000-00007
Hillegaart V, Hjorth S (1989) Median raphe, but not dorsal raphe, application of the 5HT1A agonist 8-OH-DPAT stimulates rat motor activity. Eur J Pharmacol 160:303–307. https://doi.org/10.1016/0014-2999(89)90505-0
Hjorth S, Bengtsson HJ, Kullberg A, Carlzon D, Peilot H, Auerbach SB (2000) Serotonin autoreceptor function and antidepressant drug action. J Psychopharmacol 14:177–185. https://doi.org/10.1177/026988110001400208
Homberg JR (2012) Serotonergic modulation of conditioned fear. Scientifica 821549. https://doi.org/10.6064/2012/821549
Huber R, Smith K, Delago A, Isaksson K, Kravitz EA (1997) Serotonin and aggressive motivation in crustaceans: altering the decision to retreat. P Natl Acad Sci USA 94:5939–5942. https://doi.org/10.1073/pnas.94.11.5939
Huntingford FA (2019) Aggressive behaviour In Encyclopedia Britannica Chicago
Hyttel J (1994) Pharmacological characterization of selective serotonin reuptake inhibitors (SSRIs). Int Clin Psychopharmacol 9:19–26. https://doi.org/10.1097/00004850-199403001-00004
Inoue T, Tsuchiya K, Koyama T (1996) Serotonergic activation reduces defensive freezing in the conditioned fear paradigm. Pharmacol Biochem Behav 53:825–831. https://doi.org/10.1016/0091-3057(95)02084-5
Inoue T, Li XB, Abekawa T, Kitaichi Y, Izumi T, Nakagawa S, Koyama T (2004) Selective serotonin reuptake inhibitor reduces conditioned fear through its effect in the amygdala. Eur J Pharmacol 497:311–316. https://doi.org/10.1016/j.ejphar.2004.06.061
Jenck F, Moreau JL, Mutel V, Martin JR (1994) Brain 5-HT1C receptors and antidepressants. Prog Neuro-Psychoph 18:563–574. https://doi.org/10.1016/0278-5846(94)90013-2
Joppa MA, Rowe RK, Meisel RL (1997) Effects of serotonin 1A or 1B receptor agonists on social aggression in male and female Syrian Hamsters. Pharmacol Biochem Behav 58:349–353. https://doi.org/10.1016/s0091-3057(97)00277-3
Kiser D, Steemers B, Branchi I, Homberg JR (2012) The reciprocal interaction between serotonin and social behaviour. Neurosci Biobehav Rev 36:786–798. https://doi.org/10.1016/j.neubiorev.2011.12.009
Kohlert JG, Mangan BP, Kodra C, Drako L, Long E, Simpson H (2012) Decreased aggressive and locomotor behaviours in Betta splendens after exposure to fluoxetine. Psychol Rep 110:51–62. https://doi.org/10.2466/02.13.PR0.110.1.51-62
Kravitz EA (2000) Serotonin and aggression: Insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior. J Comp Physiol A 186:221–238. https://doi.org/10.1007/s003590050423
Lillesaar C (2011) The serotonergic system in fish. J Chem Neuroanat 41:294–308. https://doi.org/10.1016/j.jchemneu.2011.05.009
Lopez-Mendoza D, Aguilar-Bravo H, Swanson HH (1998) Combined effects of Gepirone and (+) WAY 100135 on territorial aggression in mice. Pharmacol Biochem Behav 61:1–8. https://doi.org/10.1016/s0091-3057(97)00563-7
Lorenzi V, Carpenter RE, Summers CH, Earley RL, Grober MS (2009) Serotonin, social status and sex change in the bluebanded goby Lythrypnus dalli. Physiol Behav 97:476–483. https://doi.org/10.1016/j.physbeh.2009.03.026
Lüdecke D, Makowski D, Waggoner P, Patil I, Ben-Shachar MS (2020) performance assessment of regression models performance R package version 0 7 0
Mancilla-Diaz JM, Escartin-Perez RE, Lopez-Alonso VE, Floran-Garduño B, Romano-Camacho JB (2005) Role of 5-HT1A and 5-HT1B receptors in the hypophagic effect of 5-HT on the structure of feeding behavior. Med Sci Monit 11:74–79
Maximino C, Puty B, Benzecry R, Araújo J, Lima MG, de Jesus Oliveira Batista E, Renata de Matos Oliveira K, Crespo-Lopez ME, Herculano AM, (2013) Role of serotonin in zebrafish (Danio rerio) anxiety: relationship with serotonin levels and effect of buspirone, WAY 100635, SB 224289, fluoxetine and para-chlorophenylalanine (pCPA) in two behavioral models. Neuropharmacology 71:83–97. https://doi.org/10.1016/j.neuropharm.2013.03.006
Mennigen JA, Sassine J, Trudeau VL, Moon TW (2010) Waterborne fluoxetine disrupts feeding and energy metabolism in the goldfish Carassius auratus. Aquat Toxicol 100:128–137. https://doi.org/10.1016/j.aquatox.2010.07.022
Mombereau C, Gur TL, Onksen J, Blendy JA (2010) Differential effects of acute and repeated citalopram in mouse models of anxiety and depression. Int J Neuropsychopharmacol 13:321–334. https://doi.org/10.1017/S1461145709990630
de Moura LA, Pyterson MP, Pimentel AFN, Araújo F, de Souza LVXB, Mendes CHM, Costa BPD, de Siqueira-Silva DH, Lima-Maximino M, Maximino C (2022) Roles of the 5-HT2C receptor on zebrafish sociality. bioRvix 09(12):507567. https://doi.org/10.1101/2022.09.12.507567
Nelson RJ, Chiavegatto S (2001) Molecular basis of aggression. Trends Neurosci 24:713–719. https://doi.org/10.1016/s0166-2236(00)01996-2
Ögren SO, Eriksson TM, Elvander-Tottie E, D’Addario C, Ekström JC, Svenningsson P, Meister B, Kehr J, Stiedl O (2008) The role of 5-HT(1A) receptors in learning and memory. Behav Brain Res 195:54–77. https://doi.org/10.1016/j.bbr.2008.02.023
Oliveira RF (2009) Social behavior in context: Hormonal modulation of behavioral plasticity and social competence. Integr Comp Biol 49:423–440. https://doi.org/10.1093/icb/icp055
Olivier B, Mos J, van Oorschot R, Hen R (1995) Serotonin receptors and animal models of aggressive behaviour. Pharmacopsychiatry 28:80–90. https://doi.org/10.1055/s-2007-979624
Pälvimäki EP, Roth BL, Majasuo H, Laakso A, Kuoppamäki M, Syvälahti E, Hietala J (1996) Interactions of selective serotonin reuptake inhibitors with the serotonin 5-HT2C receptor. Psychopharmacology 126:234–240. https://doi.org/10.1007/BF02246453
Paula JR, Messias JP, Grutter AS, Bshary R, Soares MC (2015) The role of serotonin in the modulation of cooperative behavior. Behav Ecol 26:1005–1012. https://doi.org/10.1093/beheco/arv039
Paull GC, Filby AL, Giddins HG, Coe TS, Hamilton PB, Tyler CR (2010) Dominance hierarchies in zebrafish (Danio rerio) and their relationship with reproductive success. Zebrafish 7:109–117. https://doi.org/10.1089/zeb.2009.0618
Payne RB (2010) Family Estrildidae (Waxbills). In: del Hoyo J, Elliott A, Christie DA (eds) Handbook of the Birds of the World-weavers to new world warblers, vol 15. Lynx Edicions, Barcelona, pp 234–377
Peng L, Gu L, Li B, Hertz L (2014) Fluoxetine and all other SSRIs are 5-HT2B agonists - importance for their therapeutic effects. Curr Neuropharmacol 12:365–379. https://doi.org/10.2174/1570159X12666140828221720
Piñeyro G, Blier P (1999) Autoregulation of serotonin neurons: role in antidepressant drug action. Pharmacol Rev 51:533–591
Polter AM, Li X (2010) 5-HT1A receptor-regulated signal transduction pathways in brain. Cell Signal 22:1406–1412. https://doi.org/10.1016/j.cellsig.2010.03.019
Popova NK, Kulikov AV, Avgustinovich DF, Voĭtenko NN, Trut LN (1997) Effect of domestication of the silver fox on the main enzymes of serotonin metabolism and serotonin receptor. Genetika 33:370–374
R Core Team (2020) R: A language and environment for statistical computing version 4 0 0 R Foundation for Statistical Computing Vienna Austria
Reis LC, Marinho VR (2005) Influence of 5-HT1A agonist on the feeding behavior of Coturnix japonica (Galliformes: Aves). Braz J Biol 65:675–681. https://doi.org/10.1590/s1519-69842005000400015
Saadoun A, Cabrera MC (2002) Effect of the 5-HT1A receptor agonist 8-OH-DPAT on food and water intake in chickens. Physiol Behav 75:271–275. https://doi.org/10.1016/s0031-9384(01)00665-5
Sánchez C (1996) 5-HT(1A) receptors play an important role in modulation of behavior of rats in a two-compartment black and white box. Behav Pharmacol 7:788–797
Sánchez C (1997) Interaction studies of 5-HT1A receptor antagonists and selective 5-HT reuptake inhibitors in isolated aggressive mice. Eur J Pharmacol 334:127–132. https://doi.org/10.1007/s002130050181
Sánchez C, Meier E (1997) Behavioral profiles of SSRIs in animal models of depression, anxiety and aggression. Are they all alike? Psychopharmacology 129:197–205. https://doi.org/10.1016/s0014-2999(97)01199-0
Sanz-Aguilar A, Carrete M, Edelaar P, Potti J, Tella J (2015) The empty temporal niche: breeding phenology differs between coexisting native and invasive birds. Biol Invasions 17:3275–3288. https://doi.org/10.1007/s10530-015-0952-x
Saulin A, Savli M, Lazenberger R (2012) Serotonin and molecular neuroimaging in humans using PET. Amino Acids 42:2039–2057. https://doi.org/10.1007/s00726-011-1078-9
Schweighofer N, Bertin M, Shishida K, Okamoto Y, Tanaka SC, Yamawaki S, Doya K (2008) Low-serotonin levels increase delayed reward discounting in humans. J Neurosci 28:4528–4532. https://doi.org/10.1523/JNEUROSCI.4982-07.2008
Shirayama Y, Nishikawa T, Umino A, Takahashi K (1993) p-chlorophenylalanine-reversible reduction of sigma binding sites by chronic imipramine treatment in rat brain. Eur J Pharmacol 237:117–126. https://doi.org/10.1016/0014-2999(93)90100-v
Sperry TS, Thompson CK, Wingfield JC (2003) Effects of acute treatment with 8-OH-DPAT and fluoxetine on aggressive behaviour in male song sparrows (Melospiza melodia morphna). J Neuroendocrinol 15:150–160. https://doi.org/10.1046/j.1365-2826.2003.00968.x
Sprouse JS, Aghajanian GK (1987) Electrophysiological responses of serotoninergic dorsal raphe neurons to 5-HT1A and 5-HT1B agonists. Synapse 1:3–9. https://doi.org/10.1002/syn.890010103
Steffens SM, Casas DC, Milanez BC, Freitas GC, Paschoalini MA, MarinoNeto J (1997) Hypophagic and dipsogenic effect of central 5-HT injections in pigeons. Brain Res Bull 44:681–688. https://doi.org/10.1016/s0361-9230(97)00199-8
Stettler PR, Antunes DF, Taborsky B (2021) The serotonin 1A receptor modulates the social behaviour within groups of a cooperatively-breeding cichlid. Horm Behav 129:104918. https://doi.org/10.1016/j.yhbeh.2020.104918
Theodoridi A, Tsalafouta A, Pavlidis M (2017) Acute exposure to fluoxetine alters aggressive behavior of zebrafish and expression of genes involved in serotonergic system regulation. Front Neurosci 11:223. https://doi.org/10.3389/fnins.2017.00223
Tse WS, Bond AJ (2002) Serotonergic intervention affects both social dominance and affiliative behaviour. Psychopharmacology 161:324–330. https://doi.org/10.1007/s00213-002-1049-7
Weinberger J, Klaper R (2014) Environmental concentrations of the selective serotonin reuptake inhibitor fluoxetine impact specific behaviors involved in reproduction, feeding and predator avoidance in the fish Pimephales promelas (fathead minnow). Aquat Toxicol 151:77–83. https://doi.org/10.1016/j.aquatox.2013.10.012
Westenberg HG, den Boer JA (1988) Clinical and biochemical effects of selective serotonin uptake inhibitors in anxiety disorders. Adv Biol P 17:84–99. https://doi.org/10.1159/000416220
Winberg S, Øverli Ø, Lepage O (2001) Supression of aggression in rainbow trout (Oncorhynchus mykiss) by dietary L-tryptophan. J Exp Biol 204:3867–3876. https://doi.org/10.1242/jeb.204.22.3867
Young SN (2013) The effect of raising and lowering tryptophan levels on human mood and social behaviour. Phil Trans R Soc B 368:20110375. https://doi.org/10.1098/rstb.2011.0375
Ziomkiewicz A (2016) Serotonin and dominance. In Weekes-Shackelford V, Shackelford T, Weekes-Shackelford V (eds) Encyclopedia of Evolutionary Psychological Science. Springer Cham, Switzerland, pp 1–4. https://doi.org/10.1007/978-3-319-16999-6_1440-1
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We thank the reviewers and editors for their helpful comments and suggestions. We also thank Ana Cristina Gomes and Patrícia Beltrão for helping with the script of the statistical analyses.
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Open access funding provided by FCT|FCCN (b-on). This work was supported by Portuguese National Funds through the Fundação para a Ciência e Tecnologia (grant numbers PTDC/BIA-ECO/32210/2017, PTDC/BIA-COM/2644/2020, DL57/2016/CP1440/CT0011, DL57/2013/CP1440/CT0019), and FEDER funds under COMPETE 2020 (CEEC Individual – 2021.01458.CEECIND/CP1668/CT0003).
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Saldanha, B.C., Silva, P.A., Maximino, C. et al. The role of serotonin in modulating common waxbill behaviour. Behav Ecol Sociobiol 77, 39 (2023). https://doi.org/10.1007/s00265-023-03316-8
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DOI: https://doi.org/10.1007/s00265-023-03316-8