Tyrone Lucon-Xiccato

Discrimination reversal learning reveals greater female behavioural flexibility in guppies

Behavioural flexibility allows an animal to adapt its behaviour in response to changes in the environment. Research conducted in primates, rodents and domestic fowl suggests greater behavioural persistence and reduced behavioural flexibility in males. We investigated sex differences in behavioural flexibility in fish by comparing male and female guppies (Poecilia reticulata) in a reversal learning task. Fish were first trained on a colour discrimination, which was learned equally rapidly by males and females. However, once the reward contingency was reversed, females were better at inhibiting the previous response and reached criterion twice as fast as males. When reward reversing was repeated, males gradually reduced the number of errors, and the two sexes had a comparable performance after four reversals. We suggest that sex differences in behavioural flexibility in guppies can be explained in terms of the different roles that males and females play in reproduction.

Extensive training extends numerical abilities of guppies

Recent studies on animal mathematical abilities suggest that all vertebrates show comparable abilities when they are given spontaneous preference tests, such as selecting the larger number of food items, but that mammals and birds generally achieve much better performance than fish when tested with training procedures. At least part of these differences might be due to the fact that fish are usually trained with only one or two dozen trials while extensive training, sometimes with thousands of trials, is normally performed in studies of mammals and birds. To test this hypothesis, female guppies were trained on four consecutive numerical discriminations of increasing difficulty (from 2 vs. 3 to 5 vs. 6 items), with up to 120 trials with each discrimination. Five out of eight subjects discriminated all contrasts up to 4 versus 5 objects at levels significantly better than chance, a much higher limit than the 2 versus 3 limit previously reported in studies that provided fish with only short training sequences. Our findings indicate that the difference in numerical cognition between teleosts and warm-blooded vertebrates might be smaller than previously supposed.

Guppies discriminate between two quantities of food items but prioritize item size over total amount

When two food patches are available, individuals of many animal species feed on the larger one, a preference frequently used to study numerical abilities in mammals and birds. We employed this method to investigate, for the first time, food quantity discrimination and its underlying mechanisms in a fish, the guppy, Poecilia reticulata. Guppies facing two sets of similar-sized food items successfully discriminated numerosity up to a 0.5 ratio (one versus four and two versus four items, but not two versus three or three versus four food items). A further experiment suggested that guppies attended to cumulative surface area of food items rather than number to select the larger quantity. Moreover, in a two versus four discrimination in which the cumulative surface area occupied by food was matched by using larger items in the set with fewer items, guppies unexpectedly showed a preference for the smaller numerosity. Since this result might be explained by assuming that guppies selected the larger food item, we performed additional experiments to test this hypothesis. Guppies were observed to be very accurate in estimating item size, being able to discriminate between two food items that differed by a ratio of 0.75 in surface area. The attraction to the larger food item was so strong that guppies preferred the set containing the largest item even when the other set contained a double quantity of food. Since guppies in the wild forage in groups and compete for food, we hypothesized that in this species natural selection has favoured cognitive mechanisms allowing a rapid and efficient choice of the most profitable food item within the patch.

Assessing memory in zebrafish using the one-trial test

Zebrafish represents a very promising model to study memory function and impairment in vertebrates. The one-trial memory test has proven to be a reliable method to assess memory in mammals without the need for an extensive training procedure or the learning of a rule. To investigate whether such a test is suitable for zebrafish we observed adult fish in a modification of the original one-trial memory test developed for rats. Subjects were allowed to familiarize themselves with a new object for 25 min (exposure phase) and were then required to discriminate between the familiar object and a novel object that differed in shape and color (test phase). In both phases zebrafish showed a clear tendency to explore a new object, can memorize the characteristics of this object and use this information when a second object was presented irrespective of the delay (2, 6 or 24h) that separated the two phases. These results suggest that memory performance in fish could be also assessed using this very simple test.

Use of ordinal information by fish

Mammals and birds can process ordinal numerical information which can be used, for instance, for recognising an object on the basis of its position in a sequence of similar objects. Recent studies have shown that teleost fish possess numerical abilities comparable to those of other vertebrates, but it is unknown if they can also learn ordinal numerical relations. Guppies (Poecilia reticulata) learned to recognise the 3rd feeder in a row of 8 identical ones even when inter-feeder distance and feeder positions were varied among trials to prevent the use of any spatial information. To assess whether guppies spontaneously use ordinal or spatial information when both are simultaneously available, fish were then trained with constant feeder positions and inter-feeder distance. In probe trials where these two sources of information were contrasted, the subjects selected the correct ordinal position significantly more often than the original spatial position, indicating that the former was preferentially encoded during training. Finally, a comparison between subjects trained on the 3rd and the 5th position revealed that guppies can also learn the latter discrimination, but the larger error rate observed in this case suggests that 5 is close to the upper limit of discrimination in guppies.

Male and female guppies differ in speed but not in accuracy in visual discrimination learning

In many species, males and females have different reproductive roles and/or differ in their ecological niche. Since in these cases the two sexes often face different cognitive challenges, selection may promote some degree of cognitive differentiation, an issue that has received relatively little attention so far. We investigated the existence of sex differences in visual discrimination learning in the guppy, Poecilia reticulata, a fish species in which females show complex mate choice based on male colour pattern. We tested males and females for their ability to learn a discrimination between two different shapes (experiment 1) and between two identical figures with a different orientation (experiment 2). In experiment 3, guppies were required to select an object of the odd colour in a group of five objects. Colours changed daily, and therefore, the solution for this task was facilitated by concept learning. We found males’ and females’ accuracy practically overlapped in the three experiments, suggesting that the two sexes have similar discrimination learning abilities. Yet, males showed faster decision time than females without any evident speed–accuracy trade-off. This result indicates the existence of consistent between-sex differences in decision speed perhaps due to impulsivity rather than speed in information processing. Our results align with previous literature, indicating that sex differences in cognitive abilities are the exception rather than the rule, while sex differences in cognitive style, i.e. the way in which an individual faces a cognitive task, are much more common.

Individual differences in cognition among teleost fishes

Individual differences in cognitive abilities have been thoroughly investigated in humans and to a lesser extent in other mammals. Despite the growing interest in studying cognition in other taxonomic groups, data on individual differences are scarce for non-mammalian species. Here, we review the literature on individual differences in cognitive abilities in teleost fishes. Relatively few studies have directly addressed this topic and have provided evidence of consistent and heritable individual variation in cognitive abilities in fish. We found much more evidence of individual cognitive differences in other research areas, namely sex differences, personality differences, cerebral lateralisation and comparison between populations. Altogether, these studies suggest that individual differences in cognition are as common in fish as in warm-blooded vertebrates. Based on the example of research on mammals, we suggest directions for future investigation in fish.

Sex differences in spatial abilities and cognitive flexibility in the guppy

When males and females differ in their spatial ecology, selection is expected to promote sex differences in spatial abilities. Although this prediction applies to many species, few studies have looked at sex differences in spatial abilities outside mammals. Here, we addressed this hypothesis in the guppy, Poecilia reticulata, a polygynous fish in which males disperse more than females and inhabit more spatially complex environments. We compared the performance of male and female guppies in two spatial tasks to test whether males have been selected for enhanced spatial abilities. In a detour task (experiment 1), the two sexes showed similar ability to navigate around an obstacle to reach a target. However, males were more persistent in trying to pass through the transparent obstacle, an effect that is likely to be related to sex differences in cognitive flexibility rather than to spatial abilities. In the second experiment, with a more complex maze in which guppies had to choose between alternative routes to reach the target, males learned the task after only one presentation, whereas females did not show any evidence of learning after five trials. The direction of these differences is the same as that observed in most polygynous species investigated, suggesting a common pattern of cognitive sex differences across vertebrates.

Guppies Show Behavioural but Not Cognitive Sex Differences in a Novel Object Recognition Test

The novel object recognition (NOR) test is a widely-used paradigm to study learning and memory in rodents. NOR performance is typically measured as the preference to interact with a novel object over a familiar object based on spontaneous exploratory behaviour. In rats and mice, females usually have greater NOR ability than males. The NOR test is now available for a large number of species, including fish, but sex differences have not been properly tested outside of rodents. We compared male and female guppies (Poecilia reticulata) in a NOR test to study whether sex differences exist also for fish. We focused on sex differences in both performance and behaviour of guppies during the test. In our experiment, adult guppies expressed a preference for the novel object as most rodents and other species do. When we looked at sex differences, we found the two sexes showed a similar preference for the novel object over the familiar object, suggesting that male and female guppies have similar NOR performances. Analysis of behaviour revealed that males were more inclined to swim in the proximity of the two objects than females. Further, males explored the novel object at the beginning of the experiment while females did so afterwards. These two behavioural differences are possibly due to sex differences in exploration. Even though NOR performance is not different between male and female guppies, the behavioural sex differences we found could affect the results of the experiments and should be carefully considered when assessing fish memory with the NOR test.

Prenatal exposure to predation affects predator recognition learning via lateralization plasticity

Prey with cerebral lateralization often shows a bias in escape direction and asymmetrical use of eyes for scanning. Such asymmetries are likely to cause ecological disadvantages when, for example, predators attack from the side in which the prey is more susceptible. However, lateralized individuals are diffuse in many species and, paradoxically, their frequency increases via developmental plasticity in environments with high-predation risk. Using wood frog tadpoles, Lithobates sylvaticus, we tested the hypothesis that cerebral lateralization enhances predator recognition learning and thus overcomes the costs of behavioral asymmetries in high predation risk environments. In the first experiment, we found tadpoles exposed to risk as embryos developed more intense lateralization in a rotational test compared to predator-naive controls. Risk exposure led to the more frequent development of clockwise swimming preference. In the second experiment, we found that tadpoles exhibiting no behavioral lateralization and tadpoles with marked clockwise swimming preference learned to recognize the novel predator odor, with the latter showing a better performance as predicted. Tadpoles with anticlockwise swimming preference did not learn to associate the predator with risk. Exposure to a high-risk environment during early ontogeny appears to favor the development of either a lateralization phenotype with refined predator recognition learning skills, or, to a lesser extent, a lateralization phenotype with poor predator recognition learning skills. Such individuals likely cope with predation using mechanisms other than learning.