Marco Dadda

Do fish count? Spontaneous discrimination of quantity in female mosquitofish

The spontaneous tendency to join the largest social group was used to investigate quantity discrimination in fish. Fish discriminated between shoals that differed by one element when the paired numbers were 1vs2, 2vs3 and 3vs4, but not when 4vs5 or larger. Using large numerosities (>4), the ability to discriminate between two numbers improved as the numerical distance between them increased and a significant discrimination was found only with ratios of 1:2 or smaller (4vs8, 8vs16 and 4vs10). Experiments to control for non-numerical variables evidenced the role played by the total area of stimuli with both large and small numerosities; the total quantity of movement of the fish within a shoal appeared also important but only when large numerosities were involved. Even though the pattern of discrimination exhibited by female mosquitofish is not fully consistent with any of the existing models of quantity representation, our results seem to suggest two distinct mechanisms in fish, one used to compare small numbers of objects and one used when larger numerosities are involved.

Does brain asymmetry allow efficient performance of simultaneous tasks

Rogers (2000, Brain and Language, 73, 236–253) suggested that the ubiquity of cerebral lateralization could be explained by the advantages it provides to individuals in coping with two simultaneous tasks, because in lateralized individuals each task could be carried out by a different hemisphere. To test this hypothesis, we compared lateralized and nonlateralized fish, obtained through selective breeding, in a situation requiring the sharing of attention between two simultaneous tasks, prey capture and predator vigilance. Food-deprived individual Girardinus falcatus had to enter a compartment adjacent to the home tank to capture live brine shrimps either in the presence or in the absence of a live predator placed at some distance. When no hazard was present, lateralized and nonlateralized fish did not differ in rate of prey capture. However, when the predator was visible, lateralized fish were twice as fast at catching shrimps as were nonlateralized fish. A fine analysis of fish movements revealed that lateralized fish tended to monitor the predator with one eye and to use the other eye for catching prey, whereas nonlateralized fish swapped between tasks, using each eye for both functions.

Quantity discrimination in female mosquitofish

The ability in animals to count and represent different numbers of objects has received a great deal of attention in the past few decades. Cumulative evidence from comparative studies on number discriminations report obvious analogies among human babies, non-human primates and birds and are consistent with the hypothesis of two distinct and widespread mechanisms, one for counting small numbers (<4) precisely, and one for quantifying large numbers approximately. We investigated the ability to discriminate among different numerosities, in a distantly related species, the mosquitofish, by using the spontaneous choice of a gravid female to join large groups of females as protection from a sexually harassing male. In one experiment, we found that females were able to discriminate between two shoals with a 1:2 numerosity ratio (2 vs. 4, 4 vs. 8 and 8 vs. 16 fish) but failed to discriminate a 2:3 ratio (8 vs. 12 fish). In the second experiment, we studied the ability to discriminate between shoals that differed by one element; females were able to select the larger shoal when the paired numbers were 2 vs. 3 or 3 vs. 4 but not 4 vs. 5 or 5 vs. 6. Our study indicates that numerical abilities in fish are comparable with those of other non-verbal creatures studied; results are in agreement with the hypothesis of the existence of two distinct systems for quantity discrimination in vertebrates.

Use of Number by Fish

Background Research on human infants, mammals, birds and fish has demonstrated that rudimentary numerical abilities pre-date the evolution of human language. Yet there is controversy as to whether animals represent numbers mentally or rather base their judgments on non-numerical perceptual variables that co-vary with numerosity. To date, mental representation of number has been convincingly documented only for a few mammals. Methodology/Principal Findings Here we used a training procedure to investigate whether mosquitofish could learn to discriminate between two and three objects even when denied access to non-numerical information. In the first experiment, fish were trained to discriminate between two sets of geometric figures. These varied in shape, size, brightness and distance, but no control for non-numerical variables was made. Subjects were then re-tested while controlling for one non-numerical variable at a time. Total luminance of the stimuli and the sum of perimeter of figures appeared irrelevant, but performance dropped to chance level when stimuli were matched for the cumulative surface area or for the overall space occupied by the arrays, indicating that these latter cues had been spontaneously used by the fish during the learning process. In a second experiment, where the task consisted of discriminating 2 vs 3 elements with all non-numerical variables simultaneously controlled for, all subjects proved able to learn the discrimination, and interestingly they did not make more errors than the fish in Experiment 1 that could access non-numerical information in order to accomplish the task. Conclusions/Significance Mosquitofish can learn to discriminate small quantities, even when non-numerical indicators of quantity are unavailable, hence providing the first evidence that fish, like primates, can use numbers. As in humans and non-human primates, genuine counting appears to be a ‘last resort’ strategy in fish, when no other perceptual mechanism may suggest the quantity of the elements. However, our data suggest that, at least in fish, the priority of perceptual over numerical information is not related to a greater cognitive load imposed by direct numerical computation.

Copulation duration, insemination efficiency and male attractiveness in guppies

In polyandrous species, females may influence paternity by biasing sperm usage in favour of particular males. In the guppy, Poecilia reticulata , the number of sperm inseminated in a copulation depends on the females perception of male attractiveness. We videorecorded copulations in the laboratory to test the hypothesis that there is a positive correlation between the number of sperm inseminated and the duration of the copulation. Duration was positively correlated with the number of sperm retrieved from the females gonoduct. Once copulation duration was statistically controlled for, more sperm were retrieved from the gonoduct in courtship copulations than in coercive copulations, and in postpartum females than in virgin females. Copulation duration was positively correlated with the degree of carotenoid coloration of the male, suggesting that copulation duration might be the proximate mechanism of cryptic female choice in this species. The intensity of ‘jerking’, a postcopulatory behaviour of male guppies, was positively correlated with the number of sperm inseminated, suggesting a possible signalling function of this display.

Enhanced schooling performance in lateralized fishes

The occurrence of functional left–right cerebral asymmetries has been documented in a wide range of animals, suggesting that the lateralization of cognitive functions enjoys some kind of selective advantage over the bilateral control of the same functions. Here, we compared schooling performance of fishes with high or low degree of lateralization, which were obtained through selective breeding. Schools of lateralized fishes moving in a novel environment showed significantly more cohesion and coordination than schools of non-lateralized (NL) fishes. Pairs of fishes lateralized in opposite directions were as efficient as pairs of same laterality, suggesting that the performance of lateralized fishes derives from a computational advantage rather than being the consequence of a behavioural similarity among schoolmates. In schools composed of both lateralized and NL fishes, the latter were more often at the periphery of the school while lateralized fishes occupied the core, a position normally safer and energetically less expensive.

Behavioural asymmetry affects escape performance in a teleost fish

Escape performance is fundamental for survival in fish and most other animals. While previous work has shown that both intrinsic (e.g. size, shape) and extrinsic (e.g. temperature, hypoxia) factors can affect escape performance, the possibility that behavioural asymmetry may affect timing and locomotor performance in startled fish is largely unexplored. Numerous studies have found a relationship between brain lateralization and performance in several cognitive tasks. Here, we tested the hypothesis that behavioural lateralization may affect escape performance in a teleost, the shiner perch Cymatogaster aggregata. Escape responses were elicited by mechanical stimulation and recorded using high-speed video (250 Hz). A number of performance variables were analysed, including directionality, escape latency, turning rate and distance travelled within a fixed time. A lateralization index was obtained by testing the turning preference of each subject in a detour test. While lateralization had no effect on escape directionality, strongly lateralized fish showed higher escape reactivity, i.e. shorter latencies, which were associated with higher turning rates and longer distances travelled. Therefore, lateralization is likely to result in superior ability to escape from predator attacks, since previous work has shown that escape timing, turning rate and distance travelled are among the main determinants of escape success.

Early differences in epithalamic left-right asymmetry influence lateralization and personality of adult zebrafish

The habenulae are part of an evolutionary conserved conduction system that connects the limbic forebrain areas with midbrain structures and is implicated in important functions such as feeding, mating, avoidance learning, and hormonal response to stress. Very early during zebrafish neurogenesis the parapineal organ migrates near to one habenula, commonly the left, inducing wide left-right habenular asymmetries in gene expression and connectivity. It was posited that this initial symmetry-breaking event determines the development of lateralized brain functions and early differences in epithalamic left-right asymmetry give rise to individual variation in coping styles and personality. We tested these two hypotheses by sorting zebrafish with left or right parapineal at birth using a foxD3:GFP marker and by measuring visual and motor laterality and three personality dimensions as they become adults. Significant differences between fish with opposite parapineal position were found in all laterality tests while the influence of asymmetry of the habenulae on personality was more complex. Fish with atypical right parapineal position, tended to be bolder when inspecting a predator, spent less time in the peripheral portion of an open field and covered a shorter distance when released in the dark. Activity in the open field was not associated to anatomical asymmetry but correlated with laterality of predator inspection that in turn was influenced by parapineal position. One personality dimension, sociality, appeared uncorrelated to both anatomical and functional asymmetries and was instead influenced by the sex of the fish, thus suggesting that other factors, i.e. hormonal, may be implicated in its development.

Male sexual harassment and female schooling behaviour in the eastern mosquitofish

Among poeciliid fish, male sexual harassment is often intense and is costly for females. In Gambusia holbrooki, sexual harassment can greatly reduce female foraging efficiency when an isolated female is harassed by a single male and these costs are negatively correlated with male length. However, when females are in groups, male harassment is diluted and female foraging efficiency increases. When several males compete for the same female, mating attempts are monopolized by the dominant male and female foraging efficiency also increases. We tested whether females actively vary their schooling behaviour with conspecifics according to the presence of a harassing male. Consistent with the predictions, we found that females swam closer to each other when a male was visible. When chased by a male, females approached a group of males, and when males of different size were available, they preferred to stay close to large males. These results suggest that female schooling behaviour is a flexible strategy and that male sexual harassment may represent an important factor influencing social aggregation in poeciliids.

The costs of hemispheric specialization in a fish

Laboratory and field studies have documented better cognitive performance associated with marked hemispheric specialization in organisms as diverse as chimpanzees, domestic chicks and topminnows. While providing an evolutionary explanation for the emergence of cerebral lateralization, this evidence represents a paradox because a large proportion of non-lateralized (NL) individuals is commonly observed in animal populations. Hemispheric specialization often determines large left–right differences in perceiving and responding to stimuli. Using topminnows selected for a high or low degree of lateralization, we tested the hypothesis that individuals with greater functional asymmetry pay a higher performance cost in situations requiring matching information from the two eyes. When trained to use the middle door in a row of a nine, NL fish correctly chose the central door in most cases, while lateralized fish showed systematic leftward or rightward biases. When choosing between two shoals, each seen with a different eye, NL fish chose the high-quality shoal significantly more often than the lateralized fish, whose performance was affected by eye preference for analysing social stimuli. These findings suggest the existence of a trade-off between computational advantages of hemispheric specialization and the ecological cost of making suboptimal decisions whenever relevant information is located on both sides of the body.