Evidence for social agency in fish

Back to: A Model of social agency in fish *** SUMMARY of Conclusions reached References

Dr. Redouan Bashary specialises in mutualism in cleaner fish.
Picture courtesy of the Behavioural Ecology Department, Max Planck Institute for Behavioral Physiology, Seewiesen, Germany.

In my model of social agency in fish, I outlined a proposed set of sufficient criteria for agency in a social context, looked at the rationale for social learning, and noted its widespread occurrence across vertebrate species.

I shall now examine my proposed set of sufficient criteria for agency in a social context, one by one, discussing evidence of their occurrence amongst fish. Bshary, Wickler and Fricke (2002) caution that the evidence is assembled from different species of fish. Further research is needed to determine whether one species satisfies all of the requisite criteria.

Goals or end-states

Brown and Laland (2003) mention four general categories of goals, in relation to which social learning is known to take place amongst fish: predator avoidance; migration and orientation; foraging for food; and mate choice. There is an ever-growing body of evidence that juvenile fish engage in extensive social learning of skills relating to all of these goals (Laland, Brown and Krause, 2003).

Behaviour modelled on that of a knowledgeable individual

Individuals (especially juveniles) learn to model their behaviour on that of experienced adults, mainly by accompanying them and observing how they behave (Bshary, Wickler and Fricke, 2002).

Sensory discrimination between individuals and/or categories of individuals

There is abundant evidence in the literature of individual recognition in fish:

Individual recognition based primarily on optical cues ... has been demonstrated experimentally in a variety of species... There is even evidence that in damselfish, individuals can recognise one another on purely acoustical cues... In summary, individual recognition can safely be assumed to be widespread across fish families (Bshary, Wickler and Fricke, 2002).

In addition to individual recognition, cleaning symbiosis provides an example of a case where the ability to categorise individuals on the basis of their observed characteristics is especially useful:

In cleaning symbiosis, so-called client fish trade the removal of parasites and dead or infected tissue against an easy meal for so-called cleaner fish... Cleaning symbiosis is particularly promising for comparative studies as cleaner fish are found in many different fish families and can differ markedly in the degree to which they depend on interactions with clients for their diet... Full-time cleaners like the cleaner wrasse (Labroides dimidiatus) may have about 2,300 interactions per day with clients belonging to over 100 different species... There is strong evidence that cleaners can categorise their 100-or-so client species into resident species that have access to their local cleaner only, due to their small territory or home range, and other species that have home ranges that cover several cleaning stations. As predicted by biological market theory (Noe et al. 1991), clients with choice options between cleaners almost invariably have priority of access over clients without choice at cleaning stations (Bshary, Wickler and Fricke, 2002).

Memory for individuals and their track record

The ability to remember individuals over long periods of time is of fundamental importance for social learning. Bshary, Wickler and Fricke (2002) cite evidence that an anemonefish can recognise an individual that it has not seen for 30 days. (So much for the myth that fish have only a 3-second memory!)

According to Bshary, Wickler and Fricke (2002), some fish can also monitor changes in the status of individuals and track relationships within their groups.

Bshary, Wickler and Fricke (2002) describe experiments showing that some fish species are capable of engaging in book-keeping (remembering their partners' behaviour during past interations) with several partners at once:

The most famous example of co-operation in fish is probably the inspection of nearby predators by one or several fish that leave the relative safety of their school to do so (Pitcher et al. 1986). During inspection, pairs of sticklebacks, Gasterosteus aculeatus, and guppies, Poecilia reticulata, among others, approach the predator in alternating moves. A series of experiments led to the conclusion that these fish solve a so-called "prisoner's dilemma" (Luce and Raiffa 1957). In a prisoner's dilemma, two players have the option of either co-operating with or cheating their partner. Cheating the partner yields a higher benefit than co-operation irrespective of what the partner does, but if both partners co-operate then they receive a higher benefit than if both cheat, hence the dilemma. Milinski (1987) and Dugatkin (1988) proposed that fish solve the prisoner's dilemma by playing a "tit-for-tat" strategy, which states that a player starts co-operatively and does in all further rounds what the partner did in the previous round (Axelrod and Hamilton 1981). This interpretation is not yet entirely resolved (see review in Dugatkin 1997) but discussions about the interpretation led to a few experiments with very interesting additional results. Milinski et al. (1990a) could show that individual sticklebacks prefer specific partners to others, which implies that school members recognise each other. In addition, partners build up trust in each other during repeated inspections, that is, they hesitate less in approaching a predator when accompanied by a partner that co-operated in the past (Milinski et al. 1990b). Similar results have been found in guppies (see review in Dugatkin 1997). These data imply that these fish species are capable of book-keeping (remembering their partners' behaviour during past interactions) with several partners simultaneously (2002).

Flexible behaviour (acquiring new practices)

Juvenile fish learn what to eat by observing conspecifics:

There is some evidence that young fish learn what to eat by observing adults. Fish definitely learn horizontally from conspecifics what to eat under lab conditions. Templeton ... found that juvenile rock bass ... that saw a trained conspecific eating a novel food item would readily consume that food later when, alone, they were tested for the first time. Without prior observations, these juveniles did not attack the prey... (Bshary, Wickler and Fricke, 2002).

Hatchery-reared Atlantic salmon acquire new kinds of feeding behaviour and learn to target new kinds of prey, simply by observing knowledgeable conspecifics. Salmon raised in hatcheries tend to prefer taking prey from the surface, because of long-term conditioning in the hatchery environment. This can cause high mortality rates from starvation when they are released into the wild, because their choice of prey near the surface is restricted and energetically costly. However, after six days of watching "demonstrators" through a clear perspex partition, naive salmon changed their feeding habits and were able to feed from the bottom (Brown, Markula and Laland, 2003).

Social enhancement of foraging has been reported in species as different as salmon, rock bass, Alaska pollack and brown trout (Brown and Laland, 2003).

Fish can also learn novel techniques for obtaining food from observation of knowledgeable conspecifics. Juvenile European sea bass learned to press a lever to get food, simply by watching other fish that had been previously trained to do this (Brown and Laland, 2003).

Learning (group traditions)

Schools of fish have their own "traditions" relating to their choice of sites for resting sites, migration routes and food sources, and this knowledge is transmitted through social learning (Bshary, Wickler and Fricke, 2002). For instance, juvenile French grunts learn the migration route from their resting grounds to feeding sites by following older individuals, and bluehead wrasse have prefrred mating sites that stay the same over many generations (Brown and Laland 2003).

Bshary, Wickler and Fricke describe the mechanism by which traditions are perpetuated in guppies:

Laland and Williams ... conducted laboratory experiments and showed experimentally that guppies learn the way to hidden food sourced from knowledgeable conspecifics. The conspecifics had been trained to use only one of two ways to the food source. Naive fish were added and learned the way to the food source by schooling with the others. Members of the original school could be replaced successively and the school still preferentially took the originally learned way to the food source. The fish thus built up a tradition. Using principally the same experimental set up, Laland and Williams ... went one step further and showed that even maladaptive behaviour can spread through a population due to social learning. In their study, a longer and therefore more costly way to a foraging site was still preferred over a short way 3 days after all original trainers had been removed" (Bshary, Wickler and Fricke, 2002).

Fine-tuning (controlled, modulated activity):

Individuals carefully tailor their own social behaviour towards an individual, in accordance with their observations of that individual's past interactions with other individuals.

Male Siamese fighting fish ... monitor aggressive interactions between neighbouring conspecifics and use the information on relative fighting ability in subsequent aggressive interactions with the males they have observed...(Brown and Laland, 2003, p. 285).

Individuals also adjust their behaviour towards a specific individual on the basis of their own previous interactions with that individual - a practice known as book-keeping. Cleaner fish engage in book-keeping: they provide better than average service to dissatisfied clients that "punished" (aggressively chased) them during their last interaction. As Bshary, Wickler and Fricke (2002) point out, punishment can only work if there is individual recognition. This means that cleaner fish must be able to keep track of the behaviour of each their clients (up to 100 individuals), and modulate their behaviour towards each of them.

Cleaner fish also provide tactile stimulation to predatory clients, possibly as a form of pre-conflict management, or towards clients it has cheated in the past (Bshary, Wickler and Fricke, 2002).

Additionally, cleaner fish behave much more attentively (or "altruistically") towards their clients if they are being watched by bystanders who have the option of switching to another cleaning station. The reason is that an observer will copy the behaviour of the previous client, and either invite for inspection if it witnessed a positive interaction, or flee the approaching cleaner if it saw the last client run away as well. The true rationale for cleaner "altruism" is a selfish one: the opportunity to recruit a new customer and get access to more food (Bshary, Wickler and Fricke, 2002).

Representation

The mechanisms by which fish represent their social interactions with other individuals are not known, but fish are certainly able to form internal representations of the status and fighting ability of other individuals in their group, as well as the reliability of former partners (Bshary, Wickler and Fricke, 2002). Presumably, when copying the goal-oriented behaviour of a knowledgeable individual, they must be able to represent the activity of following the role model's example as a means of attaining its own ends, which are (qualitatively) the same as its own. Alternatively, in simpler cases (e.g finding hidden food by following a knowledgeable individual), the observer may simply represent the model itself as a kind of "moving signpost" pointing to its goal (i.e. the model itself is viewed as a means to the individual's end).

Self-correction

Fish are certainly capable of altering their social behaviour when their expectations of another individual are disappointed. As we saw above, Bshary, Wickler and Fricke (2002) cited evidence that sticklebacks and guppies adopt a tit-for-tat strategy towards their partners: a partner that fails to co-operate is punished the next time round. Clients of cleaner fish who cheat them by removing extra food (healthy tissue) as well as dead or infected tissue, are "punished" (chased aggressively).

Addendum: other examples of intelligent behaviour in fish:

According to Bshary et al. (2002):

there is an array of behaviours found in a variety of fish families (categorisation, cheating, punishment, manipulation of individuals and altruism) which are usually thought of as unique to primates;

there are instances of interspecific cooperative hunting between giant moray eels and red sea coral groupers;

co-operative hunting between conspecific predators is widespread in fish, and different individuals play different roles;

some fish appear to be able to use cognitive maps of their environment. For instance, inter-tidal gobies acquire an effective memory of the topography of its home pool as well as that of surrounding pools, because at low tide, it often has to jump into these pools without being able to see where it is going. Other fish appear to use landmarks for homing;

some fish use advanced foraging techniques - e.g. removing obstacles to reach hidden prey, and using their spatial intelligence to gain access to prey;

a few fish are capable of tool-using behaviour in the strict sense of the word (Beck, 1980), where an animal directly handles an object in order to obtain a goal. South American cichlids are a case in point;

some fish also build complex nests and bowers (Laland, Brown and Krause, 2003).

Finally, contrary to claims by Varner (1998), fish are indeed capable of progressive adjustments in multiple reversal trials - as long as olfactory stimuli are used (Mackintosh and Cauty, 1971, cited by Wakelin, 2003). Earlier, we examined arguments that creatures which show improvements in serial reversal learning were capable of meta-learning, insofar as they had to develop primitive hypotheses about changes in their surroundings. We tentatively concluded that this was the most reasonable interpretation of the experimental evidence, and that the behaviour should be described using an agent-centred intentional stance.