Shoal Of Conspecifics Research Articles

Heterospecific sociability and foraging behaviour of an invasive livebearer fish

AbstractHeterospecific sociability could enhance invasion success in social species since social non‐natives usually belong to small founding populations during the early stages of invasion. The twospot livebearer (Pseudoxiphophorus bimaculatus) is native to Central America and southern Mexico and is recently recognised as invasive in the Mexican Central Plateau, where it poses a threat to native species. Here, we evaluated twospot livebearer sociability towards either a conspecific pair or a shoal of four fish with one of four possible compositions, all conspecifics or two conspecifics combined with either two guppies, two porthole livebearers or two twoline skiffias. In a second experiment, foraging time, latency to feed, first fish to begin foraging and aggressive interactions were recorded under the same social conditions used in the sociability experiment, with body size included as a covariate in both experiments. All focal twospot livebearers spent significantly more time with the given shoals rather than with the available space in the aquarium. They showed a higher tendency to associate with small shoals of conspecifics than with pairs. Larger twospot livebearers associated more, regardless of the social condition. Twospot livebearer fed more with porthole livebearers, less with guppies and similarly with twoline skiffias. Latency to forage did not vary significantly between social conditions. Twospot livebearers were involved in more aggressive interactions when with guppies or porthole livebearers than when with native twoline skiffias or conspecifics. Twospot livebearers could gain benefits from associating with natives and conspecifics, but not with other invasive poeciliids. Heterospecific shoaling behaviour with natives may enhance invasion success during early stages when conspecifics are scarce while associating with other invasive poeciliids could lead to increased competition. Further research is needed on heterospecific interactions of non‐natives to better understand their behavioural role in invasion likelihood.

Sex differences in social buffering and social contagion of alarm responses in zebrafish

The alarm substance in fish is a pheromone released by injured individuals after a predator attack. When detected by other fish, it triggers fear/defensive responses, such as freezing and erratic movement behaviours. Such responses can also help other fish in the shoal to modulate their own behaviours: decreasing a fear response if conspecifics have not detected the alarm substance (social buffering) or triggering a fear response if conspecifics detected the alarm substance (social contagion). Response variation to these social phenomena is likely to depend on sex. Because males have higher-risk life-history strategies than females, they may respond more to social buffering where they risk not responding to a real predator attack, while females should respond more to social contagion because they only risk responding to a false alarm. Using zebrafish, we explored how the response of males and females to the presence/absence of the alarm substance is modified by the alarmed/unalarmed behaviour of an adjacent shoal of conspecifics. We found that, in social buffering, males decreased freezing more than females as expected, but in social contagion males also responded more than females by freezing at a higher intensity. Males were, therefore, more sensitive to visual information, while females responded more to the alarm substance itself. Because visual information updates faster than chemical information, males took more risks but potentially more benefits as well, because a quicker adjustment of a fear response allows to save energy to other activities. These sex differences provide insight into the modifying effect of life-history strategies on the use of social information.

What drives mixed-species shoaling among wild zebrafish? Role of predators, food access, abundance of conspecifics and familiarity.

Mixed-species groups occur across a wide range of faunal communities and provide several benefits to members. While zebrafish have often been observed to form mixed-species shoals with coexisting species, the factors determining their occurrence are not yet fully understood. Shoals comprising zebrafish (Danio rerio), flying barbs (Esomus danricus), and whitespots (Aplocheilus panchax) were collected from a stagnant canal at Haringhata (West Bengal, India), and using laboratory-based experiments, we deciphered likely drivers of mixed-species shoaling among zebrafish. Experiments assessing foraging efficiency revealed that the amount of food consumed by zebrafish individuals in mixed shoals was comparable to the amount consumed by these individuals in conspecific shoals. Within mixed-species shoals, zebrafish individuals, despite being smaller than the other species, consumed a comparable amount of food as the other species. Shoal choice experiments revealed that under predator risk, zebrafish associate more with mixed shoals and showed comparable associations to shoals differing in the abundance of conspecifics. Furthermore, zebrafish preferred associating with familiar conspecifics over unfamiliar mixed and unfamiliar conspecific shoals. Therefore, equitable food consumption in mixed shoals, greater association with mixed shoals in the presence of predators, and familiarity were important in driving zebrafish towards mixed-species shoaling.

Video playback versus live stimuli to assess quantity discrimination in angelfish (Pterophyllum scalare)

Video playback is a widely used technique for presentation of visual stimuli in animal behavior research. In the analysis of behavioral responses to social cues, presentation of video recordings of live conspecifics represents a consistently reproducible stimulus. However, video-recordings do not interact with the experimental subject, and thus this stimulus may be inferior in the social context. Here, we evaluated how angelfish (Pterophyllum scalare) respond to a video playback of conspecifics versus a live shoal of conspecifics. Using binary choice tests, subjects were presented different stimuli. Time spent close to one versus the other stimulus was considered an index of preference. We found angelfish to prefer a live shoal of conspecifics to an empty tank, and also the video playback of a shoal of conspecifics to a blank screen, although the level of preference in the latter was lower than in the former. These results indicate that video-playback of live conspecifics may be appropriate in angelfish, thus allowing manipulation of specific cues that angelfish may use in quantity discrimination. However, when we directly contrasted a live and a video recorded shoal, both having the same number of members, experimental fish preferred the live shoal. When the choice consisted of a live shoal of four conspecifics versus a video playback of a shoal of nine conspecifics no clear preference emerged. These results imply that video-playback has disadvantages in quantity discrimination studies with angelfish. Exploring procedural and/or technological parameters will verify the suitability of video-recording-based stimulus presentation for future use in angelfish.

Dynamic visual noise promotes social attraction, but does not affect group size preference, in a shoaling fish

Gathering information from the environment allows animals to make informed behavioural decisions, with individuals sampling information either privately or via social cues from group members. Environmental noise, however, may disrupt the ability of animals to gather information in their environment. Therefore, social interactions could be disrupted by environmental noise, or adapted to mitigate the costs associated with compromised perception in noisy environments. Here we tested whether the presence of water caustics, a natural form of visual noise prevalent within shallow aquatic habitats, affects the social decisions of shoaling fish. In a classic experimental paradigm, individual three-spined sticklebacks, Gasterosteus aculeatus, were given a choice between two conspecific shoals differing in size while immersed in different levels of visual noise. Fish showed greater social attraction towards conspecifics as noise levels increased, measured by a reduction in the distance they maintained from others. While sticklebacks only showed clear preferences for groups that had at least four more members than another group, there was no evidence that visual noise level influenced fish's preference to associate with these larger shoals, nor did it change the preferences for other shoal sizes. Our findings suggest that, at the group sizes tested, visual noise increases individual stickleback's social attraction towards conspecifics, but does not affect their decision to associate with the larger of two groups. Such changes to social behaviour may reflect the consequences of having a reduced ability to sample private, but not social, information in noisy environments.

The Three-Chamber Choice Behavioral Task using Zebrafish as a Model System.

Neurodegenerative diseases are age-dependent, debilitating, and incurable. Recent reports have also correlated hyperglycemia with changes in memory and/or cognitive impairment. We have modified and developed a three-chamber choice cognitive task similar to that used with rodents for use with hyperglycemic zebrafish. The testing chamber consists of a centrally located starting chamber and two choice compartments on either side, with a shoal of conspecifics used as the reward. We provide data showing that once acquired, zebrafish remember the task at least 8 weeks later. Our data indicate that zebrafish respond robustly to this reward, and we have identified cognitive deficits in hyperglycemic fish after 4 weeks of treatment. This behavioral assay may also be applicable to other studies related to cognition and memory.

Juvenile bonefish (Albula vulpes) show a preference to shoal with mojarra (Eucinostomus spp.) in the presence of conspecifics and another gregarious co-occurring species

Grouping behavior occurs across a wide variety of taxa, both within and between species. While members are thought to obtain foraging and antipredator advantages, they can also experience costs in the forms of competition or increased conspicuity to predators. The mechanisms behind these costs and benefits can vary depending on group composition, ultimately influencing the choice of which groups to join. Mixed-species fish shoals are common in shallow nearshore habitats, where research has shown that juvenile bonefish (Albula vulpes) occur among similarly-sized mojarras (Eucinostomus spp.) at a rate far exceeding that predicted given the fishes overlapping habitat use, suggesting that bonefish may actively select to join mojarras. To evaluate this hypothesis experimentally, we assessed the shoaling preferences of bonefish when presented with shoals of conspecifics, mojarras, or another gregarious co-occurring fish (pilchard; Harengula jaguana) in a laboratory setting. Focal juvenile bonefish (n = 25) were given the choice between: (i) conspecifics or mojarra, and (ii) conspecifics or pilchard, tested in shoal sizes of one, two, four, and eight. Bonefish were also given the choice between a mixed shoal (two conspecifics, two mojarra) as an alternative to single species shoals of either: (iii) four conspecifics, or (iv) four mojarra. Juvenile bonefish exhibited a strong association with mojarra, spending significantly more time with them than conspecifics in all but one treatment. Moreover, focal fish showed no detectable preference between conspecifics or pilchard, regardless of shoal size. In mixed shoal treatments, focal fish spent significantly more time wherever there was a higher proportion of mojarra. These findings imply that the co-occurrence of bonefish and mojarra in nature is largely a product of bonefish shoal choice behavior, and likewise that any costs that bonefish might incur by joining mojarras (i.e., oddity effects) are likely outweighed by the putative benefits of doing so, which potentially include access to social information and/or reduced intraspecific competition.

Oxytocin receptor signalling modulates novelty recognition but not social preference in zebrafish.

Sociality is a complex phenomenon that involves the individual´s motivation to approach their conspecifics, along with social cognitive functions that enable individuals to interact and survive. The nonapeptide oxytocin (OXT) is known to regulate sociality in many species. However, the role of OXT in specific aspects of sociality is still not well understood. In the present study, we investigated the contribution of the OXT receptor (OXTR) signalling in two different aspects of zebrafish social behaviour: social preference, by measuring their motivation to approach a shoal of conspecifics, and social recognition, by measuring their ability to discriminate between a novel and familiar fish, using a mutant zebrafish lacking a functional OXTR. Although oxtr mutant zebrafish displayed normal attraction to a shoal of conspecifics, they exhibited reduced social recognition. We further investigated whether this effect would be social-domain specific by replacing conspecific fish by objects. Although no differences were observed in object approach, oxtr mutant fish also exhibited impaired object recognition. Our findings suggest that OXTR signalling regulates a more general memory recognition of familiar vs novel entities, not only in social but also in a non-social domain, in zebrafish.

Boldness is affected by recent experience with predation cues and body size in mosquitofish

Adjusting behaviour can be crucial to prey surviving a predator encounter. How any one individual modifies their behaviour in response to predation risk might be affected by their previous experience with danger and their own vulnerability. Using western mosquitofish, we examined how boldness in different contexts was affected by an individual’s recent experience with predation risk. Individuals were repeatedly chased by a largemouth bass model and encountered alarm cue to mimic conditions of high risk (cues twice on 2 days), low risk (cues twice on 1 day), or no risk (water only). We then measured boldness and avoidance behaviour under three different contexts: in a novel tank, with a shoal of conspecifics, and with alarm cues and a model predator. We found that how recent experiences influenced boldness in a novel tank depended on body size. Smaller fish from the no and low risk treatments were more likely to emerge from a shelter into a novel environment than larger individuals. When individuals had recently experienced high levels of risk however, this pattern was reversed. We also found that individuals who had experienced any recent risk (low and high) were more likely to leave the safety of a shoal and approach a novel object compared to individuals who had not experienced any recent danger. Avoidance behaviour across the three assays was not affected by recent experiences but was affected by body size to varying degrees. For example, larger fish were more likely to stay in the plants, away from the cues of predation compared to smaller fish. Overall, our results suggest that how recent experiences with risk influence subsequent behaviour can depend on a variety of interacting factors including the intensity of recent experiences, the particular behaviour examined, and an individual’s body size.

Sociable bluegill, Lepomis macrochirus, are selectively captured via recreational angling

Individuals often show considerable variance in social behaviour and aggression, leading to defined social roles. Removal of individuals with particular roles from groups may have impacts on group function, leaving those groups less able to locate critical resources and avoid danger. In recreational fisheries, capture by humans constitutes a mortality risk, and therefore angling has the potential to fundamentally alter social structure in exploited populations if individuals with defined social roles are disproportionately captured. However, little work has examined the linkage between social behaviour and angling vulnerability. To address this gap, we conducted a study on bluegill, Lepomis macrochirus, a freshwater fish known to be socially gregarious, and a common target of recreational anglers in North America. Fish were angled in a naturalistic pond setting, and a subset of captured and uncaptured fish was then assessed for sociability in a shoaling assay and aggression/dominance in paired dyadic contests. Results showed a significant effect of time spent in the social zone on capture status, with captured individuals spending significantly more time near a transparent divider separating it from a shoal of conspecifics compared to uncaptured fish. Dominance was not associated with angling vulnerability, and sociability was not linked with dominance. Collectively, these results show that more social bluegill are more likely to be captured by anglers. This could in turn lead to decreased social functionality in exploited populations as a result of the removal of particularly social individuals, as well as possible evolution of social behaviour in exploited populations due to this selection.

Quantity discrimination in angelfish (Pterophyllum scalare) is maintained after a 30-s retention interval in the large but not in the small number range.

The ability to discriminate between sets that differ in the number of elements can be useful in different contexts and may have survival and fitness consequences. As such, numerical/quantity discrimination has been demonstrated in a diversity of animal species. In the laboratory, this ability has been analyzed, for example, using binary choice tests. Furthermore, when the different number of items first presented to the subjects are subsequently obscured, i.e., are not visible at the moment of making a choice, the task requires memory for the size of the sets. In previous work, angelfish (Pterophyllum scalare) have been found to be able to discriminate shoals differing in the number of shoal members both in the small (less than 4) and the large (4 or more) number range, and they were able to perform well even when a short memory retention interval (2-15s) was imposed. In the current study, we increased the retention interval to 30s during which the shoals to choose between were obscured, and investigated whether angelfish could show preference for the larger shoal they saw before this interval. Subjects were faced with a discrimination between numerically small shoals (≤4 fish) and also between numerically large (≥4 fish) shoals of conspecifics. We found angelfish not to be able to remember the location of larger versus smaller shoals in the small number range, but to exhibit significant memory for the larger shoal in the large number range as long as the ratio between these shoals was at least 2:1. These results, together with prior findings, suggest the existence of two separate quantity estimation systems, the object file system for small number of items that does not work with the longer retention interval and the analogue magnitude system for larger number of items that does.

Zebrafish prefer larger to smaller shoals: analysis of quantity estimation in a genetically tractable model organism.

Numerical abilities have been demonstrated in a variety of non-human vertebrates. However, underlying biological mechanisms have been difficult to study due to a paucity of experimental tools. Powerful genetic and neurobiological tools already exist for the zebrafish, but numerical abilities remain scarcely explored with this species. Here, we investigate the choice made by single experimental zebrafish between numerically different shoals of conspecifics presented concurrently on opposite sides of the experimental tank. We examined this choice using the AB strain and pet store zebrafish. We found zebrafish of both populations to generally prefer the numerically larger shoal to the smaller one. This preference was significant for contrasted ratios above or equalling 2:1 (i.e. 4 vs. 0, 4 vs. 1, 8 vs. 2, 6 vs. 2 and 6 vs. 3). Interestingly, zebrafish showed no significant preference when each of the two contrasted shoals had at least 4 members, e.g. in a contrast 8 versus 4. These results confirm that zebrafish possess the ability to distinguish larger numbers of items from smaller number of items, in a shoaling context, with a potential limit above 4. Our findings confirm the utility of the zebrafish for the exploration of both the behavioural and the biological mechanisms underlying numerical abilities in vertebrates.

Individual guppies differ in quantity discrimination performance across antipredator and foraging contexts

The ability to discriminate between different quantities is useful to an animal since it allows adaptive decisions in several contexts. In humans, some individuals are generally better at solving different numerical and mathematical problems, but we currently ignore whether other species also show individual differences in quantitative abilities across different contexts. Aiming to investigate this possibility, we observed the performances of individual guppies (Poecilia reticulata) in an antipredator task that required the discrimination between shoals made of a different number of conspecifics (4 versus 6 fish) and, successively, in two foraging tasks that required the discrimination between different numbers of food items (4 versus 6 items) and food items with different sizes (0.67 ratio between the two surface areas). Overall, guppies achieved comparable performances in the discrimination of shoal size and food item size, but showed reduced accuracy in the discrimination between different numbers of food items. Performances of guppies were correlated between the discrimination of shoal size and food item size, suggesting the existence of individual differences in quantity discrimination abilities in different contexts in this species. Unexpectedly, this relationship was negative, and some guppies were better in the antipredator task, while others were better in the foraging task. Our results agree with the general trend of the literature on animals that suggests the existence of multiple cognitive functions whose activation are task specific, and also introduce the possibility that some of these functions are subject to constraints. In this work, we provided the first clear evidence of individual differences in the ability to solve quantity discriminations in a fish. Guppies were observed in three quantity discrimination tasks: recognising and joining the larger shoal of conspecifics among two options, a behaviour that confers protection from predators; selecting the larger number of food items between two sets; and selecting the food item with larger size. Guppies that were more accurate in the shoal size discrimination achieved lower scores in the food item size discrimination. Some individuals gain advantage from cognitive abilities that confer defence against predators, while other individuals from those abilities that improve foraging success.

Zebrafish response to 3D printed shoals of conspecifics: the effect of body size

Recent progress in three-dimensional (3D) printing technology has enabled rapid prototyping of complex models at a limited cost. Virtually every research laboratory has access to a 3D printer, which can assist in the design and implementation of hypothesis-driven studies on animal behavior. In this study, we explore the possibility of using 3D printing technology to understand the role of body size in the social behavior of the zebrafish model organism. In a dichotomous preference test, we study the behavioral response of zebrafish to shoals of 3D printed replicas of varying size. We systematically vary the size of each replica without altering the coloration, aspect ratio, and stripe patterns, which are all selected to closely mimic zebrafish morphophysiology. The replicas are actuated through a robotic manipulator, mimicking the natural motion of live subjects. Zebrafish preference is assessed by scoring the time spent in the vicinity of the shoal of replicas, and the information theoretic construct of transfer entropy is used to further elucidate the influence of the replicas on zebrafish motion. Our results demonstrate that zebrafish adjust their behavior in response to variations in the size of the replicas. Subjects exhibit an avoidance reaction for larger replicas, and they are attracted toward and influenced by smaller replicas. The approach presented in this study, integrating 3D printing technology, robotics, and information theory, is expected to significantly aid preclinical research on zebrafish behavior.

Sensory cues employed for the acquisition of familiarity-dependent recognition of a shoal of conspecifics by climbing perch (Anabas testudineus Bloch).

In this study we showed that a freshwater fish, the climbing perch (Anabas testudineus) is incapable of using chemical communication but employs visual cues to acquire familiarity and distinguish a familiar group of conspecifics from an unfamiliar one. Moreover, the isolation of olfactory signals from visual cues did not affect the recognition and preference for a familiar shoal in this species.

Acute caffeine administration affects zebrafish response to a robotic stimulus

Zebrafish has been recently proposed as a valid animal model to investigate the fundamental mechanisms regulating emotional behavior and evaluate the modulatory effects exerted by psychoactive compounds. In this study, we propose a novel methodological framework based on robotics and information theory to investigate the behavioral response of zebrafish exposed to acute caffeine treatment. In a binary preference test, we studied the response of caffeine-treated zebrafish to a replica of a shoal of conspecifics moving in the tank. A purely data-driven information theoretic approach was used to infer the influence of the replica on zebrafish behavior as a function of caffeine concentration. Our results demonstrate that acute caffeine administration modulates both the average speed and the interaction with the replica. Specifically, zebrafish exposed to elevated doses of caffeine show reduced locomotion and increased sensitivity to the motion of the replica. The methodology developed in this study may complement traditional experimental paradigms developed in the field of behavioral pharmacology.

Angelfish (Pterophyllum scalare) discriminate between small quantities: a role of memory.

The ability to discriminate between sets of items differing in quantity has shown a growing interest in comparative studies as a diversity of animal species exhibit such quantitative competence. Previous studies with angelfish (Pterophyllum scalare) have demonstrated that this species is capable of spontaneously discriminating between fully visible groups (shoals) of conspecifics of different numerical size. In the present study, we investigated quantity discrimination in angelfish adopting a new procedure that we expected to make the task more difficult for the fish. During a pretest period, angelfish were allowed to fully see shoals of conspecifics of different numerical size, subsequently all fish but 1 in each stimulus shoal were hidden behind opaque barriers. Thus, during testing, experimental fish had to rely on their working memory, which implies a certain level of mental representation of the quantities or numbers discriminated. Angelfish chose the larger shoal with similar accuracy when 1 versus 2, 1 versus 3, 1 versus 4, 2 versus 3, and 2 versus 4 stimulus fish were contrasted, but failed to distinguish shoals when 3 versus 4, 4 versus 5, and 4 versus 6 fish were contrasted. Strong similarities were observed in relation with our previous procedure indicating the robustness of the quantity discrimination abilities of this species. Our results imply that angelfish form internal representations and demonstrate that these fish can make comparisons between small quantities of items while relying on their working memory alone.

Exotic invaders gain foraging benefits by shoaling with native fish.

Freshwater habitats are under increasing threat due to invasions of exotic fish. These invasions typically begin with the introduction of small numbers of individuals unfamiliar with the new habitat. One way in which the invaders might overcome this disadvantage is by associating with native taxa occupying a similar ecological niche. Here we used guppies (Poecilia reticulata) from a feral population in Mexico to test the prediction that exotic shoaling fish can associate with heterospecifics, and that they improve their foraging efficiency by doing so. Guppies have invaded the Mexican High Plateau and are implicated in the declines of many native topminnow (Goodeinae) species. We show that heterospecific associations between guppies and topminnows can deliver the same foraging benefits as conspecific shoals, and that variation in foraging gains is linked to differences in association tendency. These results uncover a mechanism enabling founding individuals to survive during the most vulnerable phase of an invasion and help explain why guppies have established viable populations in many parts of Mexico as well in every continent except Antarctica.

Activity counts: the effect of swimming activity on quantity discrimination in fish.

Human infants and non-human animals can discriminate the larger of two sets of discrete items. This quantity discrimination may be based upon the number of items, or upon non-numerical variables of the sets that co-vary with number. We have demonstrated that angelfish select the larger of two shoals of conspecifics without using inter-fish distance or space occupied by the stimuli as cues. However, density appeared to influence the choice between large shoals. Here, we examine the role of another non-numerical cue, swimming activity of the stimulus fish, in quantity discrimination by angelfish. To control this variable, we varied the water temperature of the stimulus aquaria or restricted the space occupied by each fish in the stimulus shoals. We used the previously successfully discriminated contrasts consisting of large (10 vs. 5) and small (3 vs. 2) shoals. We also studied whether more active or less active shoals are preferred in case of equally sized shoals (10 vs. 10, 5 vs. 5, and 3 vs. 3). When differences in stimulus fish activity were minimized by temperature manipulation we found angelfish to prefer the larger shoal in the 3 vs. 2 comparison, but not in the 10 vs. 5 comparison. When activity was controlled by space restriction, angelfish preferred the larger shoal in both numerical contrasts. These results imply that the overall activity level of the contrasted shoals is not a necessary condition for small shoals discrimination in angelfish. On the other hand, the results obtained for the large shoals, together with results obtained in the control treatments (equal numerical contrasts and differing activity levels), suggest that activity is a sufficient condition for discrimination when large shoals are involved. Further experiments are needed to evaluate the influence of other continuous variables, and to assess whether the mechanisms underlying performance are comparable to those suggested for other animals.

Behavioural syndromes and shoaling: connections between aggression, boldness and social behaviour in three different Danios

While many behavioural syndrome studies focus on individual-level correlations of behaviors across various contexts, it is also possible to examine these syndromes on a population level, comparing various species or groups. In this study we tested wild type zebrafish (Danio rerio), longfin zebrafish (Danio rerio lof mutants) and the closely related pearl danio (Danio albolineatus) to determine whether aggression and boldness varied and whether population-level differences in these behavioural types were linked to differences in shoaling preferences among the three Danio types. We found significant differences in overall levels of boldness and aggression between the three Danio groups. Pearl danios were the most ‘aggressive’ type, and wildtype zebrafish were relatively ‘passive’. In contrast, wildtype zebrafish showed the most ‘boldness’ while longfin zebrafish were comparatively ‘shy’. We also found subsequent differences in social behaviour, with pearl danios showing significant preferences for conspecific shoals. Our results indicate that fish may not only be making social decisions based on the behaviour, health and appearance of potential shoal mates, but their own temperament may be important in mediating social interactions as well.