Serotonin blockade delays learning performance in a cooperative fish

Animals use learning and memorizing to gather information that will help them to make ecologically relevant decisions. Neuro-modulatory adjustments enable them to make associations between stimuli and appropriate behavior. A key candidate for the modulation of cooperative behavior is serotonin. Previous research has shown that modulation of the serotonergic system spontaneously affects the behavior of the cleaner wrasse Labroides dimidiatus during interactions with so-called ‘client’ reef fish. Here, we asked whether shifts in serotonin function affect the cleaners’ associative learning abilities when faced with the task to distinguish two artificial clients that differ in their value as a food source. We found that the administration of serotonin 1A receptor antagonist significantly slowed learning speed in comparison with saline treated fish. As reduced serotonergic signaling typically enhances fear, we discuss the possibility that serotonin may affect how cleaners appraise, acquire information and respond to client-derived stimuli via manipulation of the perception of danger.     

Comparing species decisions in a dichotomous choice task: adjusting task parameters improves performance in monkeys

In comparative psychology, both similarities and differences among species are studied to better understand the evolution of their behavior. To do so, we first test species in tasks using similar procedures, but if differences are found, it is important to determine their underlying cause(s) (e.g., are they due to ecology, cognitive ability, an artifact of the study, and/or some other factor?). In our previous work, primates performed unexpectedly poorly on an apparently simple two-choice discrimination task based on the natural behavior of cleaner fish, while the fish did quite well. In this task, if the subjects first chose one of the options (ephemeral) they received both food items, but if they chose the other (permanent) option first, the ephemeral option disappeared. Here, we test several proposed explanations for primates’ relatively poorer performance. In Study 1, we used a computerized paradigm that differed from the previous test by removing interaction with human experimenters, which may be distracting, and providing a more standardized testing environment. In Study 2, we adapted the computerized paradigm from Study 1 to be more relevant to primate ecology. Monkeys’ overall performance in these adapted tasks matched the performance of the fish in the original study, showing that with the appropriate modifications they can solve the task. We discuss these results in light of comparative research, which requires balancing procedural similarity with considerations of how the details of the task or the context may influence how different species perceive and solve tasks differently.     

Cleaner fish Labroides dimidiatus recognise familiar clients

Individual recognition has been attributed a crucial role in the evolution of complex social systems such as helping behaviour and cooperation. A classical example for interspecific cooperation is the mutualism between the cleaner fish Labroides dimidiatus and its client reef fish species. For stable cooperation to evolve, it is generally assumed that partners interact repeatedly and remember each other's past behaviour. Repeated interactions may be achieved by site fidelity or individual recognition. However, as some cleaner fish have more than 2,300 interactions per day with various individuals per species and various species of clients, basic assumptions of cooperation theory might be violated in this mutualism. We tested the cleaner L. dimidiatus and its herbivorous client, the surgeon fish Ctenochaetus striatus, for their ability to distinguish between a familiar and an unfamiliar partner in a choice experiment. Under natural conditions, cleaners and clients have to build up their relationship, which is probably costly for both. We therefore predicted that both clients and cleaners should prefer the familiar partner in our choice experiment. We found that cleaners spent significantly more time near the familiar than the unfamiliar clients in the first 2 minutes of the experiment. This indicates the ability for individual recognition in cleaners. In contrast, the client C. striatus showed no significant preference. This could be due to a sampling artefact, possibly due to a lack of sufficient motivation. Alternatively, clients may not need to recognise their cleaners but instead remember the defined territories of L. dimidiatus to achieve repeated interactions with the same individual. Electronic Publication     

Fish cognition: a primate's eye view

We provide selected examples from the fish literature of phenomena found in fish that are currently being examined in discussions of cognitive abilities and evolution of neocortex size in primates. In the context of social intelligence, we looked at living in individualised groups and corresponding social strategies, social learning and tradition, and co-operative hunting. Regarding environmental intelligence, we searched for examples concerning special foraging skills, tool use, cognitive maps, memory, anti-predator behaviour, and the manipulation of the environment. Most phenomena of interest for primatologists are found in fish as well. We therefore conclude that more detailed studies on decision rules and mechanisms are necessary to test for differences between the cognitive abilities of primates and other taxa. Cognitive research can benefit from future fish studies in three ways: first, as fish are highly variable in their ecology, they can be used to determine the specific ecological factors that select for the evolution of specific cognitive abilities. Second, for the same reason they can be used to investigate the link between cognitive abilities and the enlargement of specific brain areas. Third, decision rules used by fish could be used as 'null-hypotheses' for primatologists looking at how monkeys might make their decisions. Finally, we propose a variety of fish species that we think are most promising as study objects. Accepted after revision: 6 September 2001 Electronic Publication     

Do cleaner fish learn to feed against their preference in a reverse reward contingency task?

The ability to control impulsive behaviour has been studied in animals with a standard test in which subjects need to choose the smaller of two food items in order to receive the larger one (reverse reward contingency). As a variety of mammals that have been tested so far (mostly primates) have great difficulties to solve the task, it has been proposed that it is generally cognitively demanding. However, according to an ecological approach to cognition, a species’ ability to solve the task should not depend on its general cognitive abilities but on whether its ecology causes selective pressure on the ability to restrain foraging behaviour. We tested this hypothesis using the cleaner wrasse (Labroides dimidiatus), a fish species that feeds against its preference in nature when engaging in cleaning interactions with so called ‘client fish’. None of the eight tested individuals learned to choose a non-preferred item after 200 trials. In a subsequent test, one subject learned to respond correctly in a large or none contingency task (only the choice of the small food was rewarded). After a short re-experience treatment, this individual learned to solve the reverse reward task after 30 trials. In conclusion, we did not find support for the general idea that interactions with clients prepared cleaners to quickly solve a reverse reward test. However, the results suggest that the potential to solve a reverse reward contingency may not be restricted to mammals but could be present also in a fish species in which the problem of choosing a non-preferred food over a preferred one is an ever present challenge in nature.     

Cleaner fish <Emphasis Type="Italic">Labroides dimidiatus</Emphasis> discriminate numbers but fail a mental number line test

Several species of primates, including humans, possess a spontaneous spatial mental arrangement (i.e. mental number line MNL) of increasing numbers or continuous quantities from left to right. This cognitive process has recently been documented in domestic chicken in a spatial–numerical task, opening the possibility that MNL is a cognitive capacity that has been conserved across vertebrate taxa. In this scenario, fish might possess the MNL as well. Here we investigated whether cleaner fish Labroides dimidiatus show evidence for MNL in two experiments. In Experiment I, we tested fish’s abilities in number discrimination, presenting simultaneously either small (2 vs 5) or large (5 vs 8) continuous quantities where one quantity was systematically rewarded. Experiment II used a protocol of an MNL task similar to the study on chickens. We trained cleaners with a target number (i.e. 5 elements), then we presented them with an identical pair of panels depicting either 2 elements or 8 elements, and we recorded their spontaneous choice for the left or right panel on each presentation. Cleaner fish showed high abilities in discriminating small and large numbers in Experiment I. Importantly, cleaners achieved this discrimination using numerical cues instead of non-numerical cues such as the cumulative surface area, density, and overall space. In contrast, cleaners did not allocate continuous quantities to space in Experiment II. Our findings suggest that cleaner fish possess numbering skills but they do not have an MNL. While similar studies on animals from various clades are needed to trace the evolution of MNL within vertebrates, our results suggest that this cognitive process might not be a capacity conserved across all vertebrate taxa.     

Ravens (Corvus corax) are indifferent to the gains of conspecific recipients or human partners in experimental tasks

Although cooperative behaviours are common in animals, the cognitive processes underpinning such behaviours are very likely to differ between species. In humans, other-regarding preferences have been proposed to sustain long-term cooperation between individuals. The extent to which such psychological capacities exist in other animals is still under investigation. Five hand-reared ravens were first tested in an experiment where they could provide food to a conspecific at no cost to themselves. We offered them two behavioural options that provided identical amounts of food to the actor and where one of the two options additionally delivered a reward to a recipient. Subsequently, we made the ravens play a no-cost cooperation game with an experimenter. The experimenter had the same options as the animals and matched the ravens’ choices, making the prosocial choice the more profitable option. In both conditions, ravens were indifferent to the effects of their choices and hence failed to help conspecifics and to cooperate with the experimenter. While our negative results should be interpreted with care, overall, our findings suggest that the ravens had no understanding of the consequences of their actions for a potential recipient. This study adds to several others that have used a similar set-up and have reported negative results on other-regarding preferences in animals.     

Generalized rule application in bluestreak cleaner wrasse (<Emphasis Type="Italic">Labroides dimidiatus</Emphasis>): using predator species as social tools to reduce punishment

Generalized rule application promotes flexible behavior by allowing individuals to adjust quickly to environmental changes through generalization of previous learning. Here, we show that bluestreak ‘cleaner’ wrasse (Labroides dimidiatus) uses generalized rule application in their use of predators as social tools against punishing reef fish clients. Punishment occurs as cleaners do not only remove ectoparasites from clients, but prefer to feed on client mucus (constituting cheating). We tested for generalized rule application in a series of experiments, starting by training cleaners to approach one of two fish models in order to evade punishment (by chasing) from a ‘cheated’ client model. Cleaners learned this task only if the safe haven was a predator model. During consecutive exposure to pairs of novel species, including exotic models, cleaners demonstrated generalization of the ‘predators-are-safe-havens’ rule by rapidly satisfying learning criteria. However, cleaners were not able to generalize to a ‘one-of-two-stimuli-presents-a-safe-haven’ rule, as they failed to solve the task when confronted with either two harmless fish models or two predator models. Our results emphasize the importance of ecologically relevant experiments to uncover complex cognitive processes in non-human animals, like generalized rule learning in the context of social tool use in a fish.