Culum Brown

In Situ Examination of Boldness–Shyness Traits in the Tropical Poeciliid, Brachyraphis episcopi

Explaining consistent variation in the behaviour of individuals in terms of personality differences is one of the cornerstones of understanding human behaviour but is seldom discussed in behavioural ecology for fear of invoking anthropomorphism. Recently, however, interest has begun to focus on identifying personality traits in animals and examining their possible evolutionary consequences. One major axis used to define personality traits is the shyness–boldness continuum. We examined boldness in an in situ experiment using fish from eight populations of the poeciliid Brachyraphis episcopi (also referred to as Brachyrhaphis episcopi). Fish from high- and low-predation regions within four streams that run independently into the Panama Canal were tested. Boldness scores were strongly influenced by standard length and the relative level of predation pressure in the rivers. In all four rivers, fish from high-predation areas were bolder than those from low-predation areas. Fish became increasingly shy as they grew.

Fish cognition and behavior

The field of animal cognition is the modern approach to understanding the mental capabilities of animals. The theories are largely an extension of early comparative psychology with a strong influence of behavioural ecology and ethology. Cognition has been variously defined in the literature. Some researchers confine cognition to higher order mental functions including awareness, reasoning and consciousness. However, a more general definition of cognition also includes perception, attention, memory formation and executive functions related to information processing such as learning and problem solving. The study of animal cognition has been largely confined to birds and mammals, particularly non-human primates. This bias in the literature is in part due to the approach taken in the 1950s when cognitive psychologists began to compare known human mental processes with other closely related species. This bias was reinforced by an underlying misconception that learning played little or no role in the development of behaviour in reptiles and fishes. Throughout scientific history fishes have largely been viewed as automatons. Their behaviour was thought to be almost exclusively controlled by unlearned predispositions. Ethologists characterised their behaviour as a series of fixed action patterns released on exposure to appropriate environmental cues (sign stimuli). Whilst there is no doubt that fishes are the most ancient form of vertebrates, they are only ‘primitive’ in the sense that they have been on earth for in excess of 500 million years and that all other vertebrates evolved from some common fish-like ancestor (around 360 million years ago). However, it is important to note that fishes have not been stuck in an evolutionary quagmire during this time. Their form and function have not remained stagnant over the ages. On the contrary, within this time frame they have diversified immensely to the point where there are more species of fish than all other vertebrates combined (currently over 32,000 described species) occupying nearly every imaginable aquatic niche. The erroneous view that both behavioural and neural sophistications are associated in a linear progression from fishes through reptiles and birds to mammals is largely due to a heady mix of outdated and unscientific thinking. Aristotle’s concept of Scala naturae

Size Matters: A Test of Boldness in Eight Populations of the Poeciliid Brachyraphis episcopi

Individual variation in behaviour within populations may be explained in part by demographics and long-term, stable individual psychological differences. We examined the relation between boldness (taken as the time to emerge from a shelter and explore a novel environment) and body size in eight populations of the poeciliid Brachyraphis episcopi originating from sites upstream and downstream of waterfalls in four rivers that run into the Panama Canal. The relation between body size and time to emerge from a shelter was positive, with larger fish taking longer to emerge. This relation differed between downstream and upstream sites, being significant in the upstream populations only. These results are best explained by a metabolic hypothesis whereby juvenile fish are compelled to emerge earlier in order to resume feeding. In the downstream sites this effect was slightly offset by the relatively greater predation threat for smaller fish, such that they delayed their emergence from cover. We discuss the underlying importance of variation in boldness and its effects on other behavioural and life history traits.

Familiarity Facilitates Social Learning of Foraging Behaviour in the Guppy

Previous studies have shown that guppies, Poecilia reticulata, can learn the route to a food source by shoaling with knowledgeable conspecifics, and prefer to shoal with experienced foragers and familiar fish. We tested the hypothesis that guppies would learn more effectively from (1) familiar than unfamiliar demonstrators and (2) well-trained than poorly trained demonstrators. Demonstrator fish were given experience in swimming a route to a food source and then introduced into shoals of untrained observer guppies; the spread of this foraging skill was recorded over 15 trials. The demonstrators were either familiar or unfamiliar to the observers and either well trained or poorly trained. Observers performed significantly better when the demonstrators were familiar. The training of the demonstrators made no overall difference to the performance of naive observers. However, whilst observers in shoals exposed to well-trained demonstrators did better initially than those with poorly trained ones, the latter learned the route to the feeder faster. Our results suggest that familiarity may generate a form of directed social learning in guppy shoals, in which fish learn more effectively from familiar conspecifics. An analysis of who follows whom suggests that well-trained demonstrators can provide a ‘tip-off’ as to the location of the hole but poorly trained demonstrators were more likely to be followed. The results suggest that while observers are able to shoal with poorly trained demonstrators, well-trained demonstrators swim the maze route too quickly to be followed, but may attract attention to the maze route.

Heritable and experiential effects on boldness in a tropical poeciliid

Consistent differences in human behaviour are often explained with reference to personality traits. Recent evidence suggests that similar traits are widespread across the entire animal kingdom and that they may have substantial fitness consequences. One of the major components of personality is the shyness–boldness continuum. Little is known about the relative contributions of genes and the environment in the development of boldness in wild animal populations. Here, we bred wild-caught fish (Brachyraphis episcopi) collected from regions of high- and low-predation pressure, reared their offspring in the laboratory under varying conditions and tested boldness utilising an open-field paradigm. First-generation laboratory-reared fish showed similar behaviour to their wild parents suggesting that boldness has a heritable component. In addition, repeated chasing with a net increased boldness in both high- and low-predation offspring, showing that boldness is also heavily influenced by life experiences. Differences between males and females were also sustained in the laboratory-reared generation indicating that sex differences in boldness are also heritable. We discuss these results with reference to the potential underlying genetic and hormonal mechanisms as well as the environmental influences that may be responsible for expression of boldness in wild animals.

Interactions between shoal size and conformity in guppy social foraging

Previous experimental studies have established that shoaling fish forage more effectively in large than small groups. We investigated how shoal size affects the foraging efficiency of laboratory populations of the guppy, Poecilia reticulata, exposed to different foraging tasks. Experiment 1 confirmed the prediction that in open water the first fish and focal fish of larger shoals locate food faster than in smaller shoals. However, a second experiment, in which shoals of fish were required to swim through a hole in an opaque partition to locate food, found the reverse pattern: smaller shoals learned to complete the task faster than large shoals. Experiment 3, in which shoals of various sizes were exposed to a transparent maze partition, clarified the apparent contradictory results of the first two experiments, with larger shoals again learning to complete the task faster than small shoals. The findings of experiments 2 and 3 can be explained in terms of positive frequency-dependent social learning, or conformity. This facilitated social learning in large groups in experiment 3 where visual contact could be maintained through the partition, but hindered it in experiment 2 where visual contact was lost once a fish had passed through the partition. The findings raise the possibility that novel behavioural innovations, particularly those that require individuals to break contact with the group, may be more likely to spread in smaller than larger groups of animals.

Laterality enhances cognition in Australian parrots

Cerebral lateralization refers to the division of information processing in either hemisphere of the brain and is a ubiquitous trait among vertebrates and invertebrates. Given its widespread occurrence, it is likely that cerebral lateralization confers a fitness advantage. It has been hypothesized that this advantage takes the form of enhanced cognitive function, potentially via a dual processing mechanism whereby each hemisphere can be used to process specific types of information without contralateral interference. Here, we examined the influence of lateralization on problem solving by Australian parrots. The first task, a pebble-seed discrimination test, was designed for small parrot species that feed predominately on small seeds, which do not require any significant manipulation with the foot prior to ingestion. The second task, a string-pull problem, was designed for larger bodied species that regularly use their feet to manipulate food objects. In both cases, strongly lateralized individuals (those showing significant foot and eye biases) outperformed less strongly lateralized individuals, and this relationship was substantially stronger in the more demanding task. These results suggest that cerebral lateralization is a ubiquitous trait among Australian parrots and conveys a significant foraging advantage. Our results provide strong support for the enhanced cognitive function hypothesis.

Differential stress responses in fish from areas of high- and low-predation pressure

We subjected fish from regions of high and low levels of predation pressure in four independent streams to a mild stressor and recorded their opercular beat rates. Fish from low-predation areas showed higher maximum, minimum and mean opercular beat frequencies than fish from high-predation regions. The change in opercular beat frequency (scope) was also significantly greater in fish from low- than in fish from high-predation regions. Under normal activity levels, however, low predation fish showed a reduced opercular beat frequency, which may be indicative of reduced activity levels or metabolic rate. Opercular beat frequency was negatively correlated with standard length as one would expect based on higher metabolic rates in smaller fish. We suggest that these contrasting stress responses are most likely the result of differential exposure to predators in fish from high- and low-predation areas. We argue that reduced stress responses in high-predation areas evolved to prevent excessive energy expenditure by modulating the fright response.

Personality traits predict hierarchy rank in male rainbowfish social groups

Personality traits are becoming increasingly important in explaining adaptive individual differences in animal behaviour and probably represent a leading edge of the evolutionary process. Despite the new-found interest in animal personality among behavioural ecologists, few studies have investigated the link between personality traits and fitness measures. We examined this link using male rainbowfish, Melanotaenia duboulayi, as a model species and found that a range of personality traits (aggression, activity and boldness) covaried with a male’s position in a hierarchy, which is directly related to reproductive success in this and many other species. Dominant fish were more aggressive, active, bold and also significantly larger than subordinate fish. Moreover, we found strong correlations between activity levels and boldness suggesting that selection may act on a suite of traits in concert (sensu behavioural syndromes). When taken together with previous research, our results suggest that the activity–boldness syndrome is likely to be domain specific. We suggest that multiple trait correlations may be generated by high levels of competition (e.g. sexual selection) in addition to predation pressure as identified by previous studies.

Population variation in lateralized eye use in the poeciliid Brachyraphis episcopi

Differential use of each hemisphere of the brain for specific tasks is a widespread phenomenon that appears to have arisen in the early history of tetrapod lineage. Despite a high degree of conformity in the development of lateralization among the tetrapods, some variation exists. The mechanisms underlying this variation remain largely unresolved. We exposed fish from regions of high and low predation pressure to a series of visual experiences, including viewing an empty compartment, a novel object and a live predator. Fish from each region differed in their preferential use of each eye to view the scenes. For example, fish from high predation regions viewed a live predator by using their right eye, whereas fish from low predation sites showed no eye preference. These results suggest that the degree of lateralization varies between populations of the same species that have been exposed to different ecological/evolutionary pressures.