What the cognitive abilities of the cleaner fish "Labroides dimidiatus" may tell us about vertebrate brain evolution
Authors:   , Aellen Mélisande 
Published: January 2024

Explaining the great variation in relative brain size in comparison to body size among vertebrates has been a great scientific challenge. Scientists have tried to understand what factors triggered this relative difference, as well as what it implies to have a bigger brain, i.e. how is brain size linked to cognitive abilities? Various hypotheses such as the social brain hypothesis, the ecological intelligence hypothesis, as well as most recently the general intelligence hypothesis propose different factors that could explain this variation. However, current results can often be interpreted as supporting various hypotheses, showing that additional studies are needed in order to disentangle which selective factors are the main driver of brain evolution. Particularly intriguing is the observation that relative brain size differs on average by a factor 10 between endo- and ectotherms, i.e. an ectotherm of the same weight of an endotherm possesses a ten times smaller brain. Thus, while both ecto- and endotherms face social and environmental challenges, we need to understand what aspects are of such fundamental difference that a factor 10 emerges. Therefore, cognitive processes are studied in various animal species via ecological or abstract task to test their relationship to brain size, and whether cognitive processes are linked to general intelligence. My PhD thesis aimed to investigate whether cleaner fish Labroides dimidiatus, a species with a rather average ectotherm brain size, show advanced cognitive abilities. Cleaner fish engage in mutualistic interactions with so-called client fish. They remove the ectoparasites from their clients, constituting their food resources, and clients, in turn, get cleaned. However, cleaners prefer to eat mucus over ectoparasites constituting cheating. Because of this cheating behaviour, cleaners show great sophisticated strategies behaviour previously documented, such as audience effect, reputation management, and client type prioritization in order to retain their clients. First, cognitive processes were tested separately and with or without ecological relevance to the fish. With this first approach, I was able to disentangle whereas cleaner fish were also able to show cognitive abilities only in an ecological context or also in an abstract situation. Second, I was interested in testing the presence of general intelligence in ectotherms by testing this time different cognitive processes. Four cognitive tasks were lacking ecological relevance and one was related to cleaners’ ecology. In the first chapter, I tested fish in a delay of gratification paradigm. High performance in primates has been linked to high levels of self-control and low discounting of future benefits, proposing that the ability is cognitively demanding. I used two cleaner fish species (L. dimidiatus and L. bicolor), and noncleaner wrasse species (Halichoeres trimaculatus and H. hortulanus) were used. Cleaner fish species differ in their ecology as L. dimidiatus live at cleaning stations, allowing clients to decide whether to seek or avoid any particular cleaner. In contrast, L. bicolor are roving cleaners lacking cleaning stations. Such roving behaviour allows L. bicolor to cheat more towards their clients as these ones are not capable of following the cleaners bicolor individually. Both non-cleaner wrasses eat small crustaceans in the sand. I asked whether the special ecology of cleaners would increase their performance compared to non-cleaners which lack any ecological reason to perform well in this task. Fish species performed well at controlling their impulse toward food in order to get more. In contrast, only cleaners show an understanding of the task by making the decision early on to wait or not for a bigger food reward, showing the ability to anticipate. In the second chapter, L. dimidiatus were tested in an abstract experimental design of concept learning, a classic approach to test whether animals can learn without specific reinforcement (conditioning). The matching-to-sample task was used in the most general form compared to previous experiments. Cleaners overall performed above chance in this task, suggesting that they possess the cognitive process of concept learning, i.e. reasoning ability. Furthermore, one individual was tested in a delayed matching-to-sample experiment but did not succeed. As only one individual was tested, it is rather difficult to conclude that cleaners lack working memory cognitive process. Finally, in the third chapter, L. dimidiatus individuals were exposed to different tasks designed to test for general intelligence, and their performances in each task were ranked to check for the presence/absence of ‘g’. Interestingly, intraspecific variation in sophisticated strategies were linked to fish densities as a likely correlate of intra- and interspecific complexity. Since those strategies were related to cleaners' ecology, the main question was whether cleaners' performances vary depending on if the task was ecologically relevant or not. Therefore, half of the individuals were coming from a high fish density and the other half from a low fish density. Cleaners showed abilities in three out of four cognitive processes, i.e. learning-flexibility, inhibition, and quantitative reasoning. They failed in the working memory task. Even though cleaners performed well in the tasks, I found no evidence for general intelligence, i.e. the tasks were not positively loading on a single main principal component factor. Moreover, the complexity of the environment, i.e. fish density, did not affect cleaners' performance in any task. In conclusion, this thesis increases evidence that cleaner fish, as representatives of ectotherms with relatively smaller brains compared to endotherms, possess a variety of supposedly advanced cognitive processes, which they can also apply to non-ecologically relevant situations. Therefore, the results from this thesis refute the hypothesis that major differences in the cognitive tool set may explain the 10-fold difference in relative brain size between endotherm and ectotherm vertebrates. However, despite cleaners' advanced cognitive abilities, they lack general intelligence. This result raises the question of whether the absence of general intelligence is a common pattern in ectotherms. If this was confirmed, general intelligence may provide a new explanation for the endotherm-ectotherm divide in the encephalization index.