Victoria A. Braithwaite

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.

Do fishes have nociceptors? Evidence for the evolution of a vertebrate sensory system.

Nociception is the detection of a noxious tissue–damaging stimulus and is sometimes accompanied by a reflex response such as withdrawal. Pain perception, as distinct from nociception, has been demonstrated in birds and mammals but has not been systematically studied in lower vertebrates. We assessed whether a fish possessed cutaneous nociceptors capable of detecting noxious stimuli and whether its behaviour was sufficiently adversely affected by the administration of a noxious stimulus. Electrophysiological recordings from trigeminal nerves identified polymodal nociceptors on the head of the trout with physiological properties similar to those described in higher vertebrates. These receptors responded to mechanical pressure, temperatures in the noxious range (more than 40°C) and 1% acetic acid, a noxious substance. In higher vertebrates nociceptive nerves are either A–delta or C fibres with C fibres being the predominating fibre type. However, in the rainbow trout A–delta fibres were most common, and this offers insights into the evolution of nociceptive systems. Administration of noxious substances to the lips of the trout affected both the physiology and the behaviour of the animal and resulted in a significant increase in opercular beat rate and the time taken to resume feeding, as well as anomalous behaviours. This study provides significant evidence of nociception in teleost fishes and furthermore demonstrates that behaviour and physiology are affected over a prolonged period of time, suggesting discomfort.

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.

Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections

‘Good genes’ models of sexual selection suggest that elaborate male sexual ornaments have evolved as reliable signals of male quality because only males of high genetic viability are able to develop and maintain them. Females benefit from choosing such individuals if quality is heritable. A key prediction is that the offspring of males with elaborate mating displays will perform better than those of less elaborate males, but it has proved difficult to demonstrate such an effect independently of the effects of differences in parental investment. We tested for ‘good genes’ linked to male ornamentation in the three–spined stickleback Gasterosteus aculeatus using in vitro fertilization to generate maternal half–siblings, which were raised without parental care. Maternal half–siblings sired by brightly coloured males grew less quickly than half–siblings sired by dull males but were more resistant to a controlled disease challenge. Among the offspring that became infected, those with brighter fathers had higher white blood cell counts. This suggests that highly ornamented males confer disease resistance on their offspring. The association with reduced growth suggests a mechanism for the maintenance of heritable variation in both disease resistance and male sexual coloration.

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.

The evolution of sex differences in spatial ability.

It is widely believed that male mammals have better spatial ability than females. A large number of evolutionary hypotheses have been proposed to explain these differences, but few species have been tested. The authors critically review the proposed evolutionary explanations for sex differences in spatial cognition and conclude that most of the hypotheses are either logically flawed or, as yet, have no substantial support. Few of the data exclusively support or exclude any current hypotheses. The hypothesis with the strongest support proposes that range size was the selection pressure that acted to increase spatial ability. The authors suggest ways in which these hypotheses could be tested by presenting explicit predictions and suggesting suitable test species or conditions.

Novel object test: examining nociception and fear in the rainbow trout.

This study aimed to assess fear responses to a novel object while experiencing a noxious event to determine whether nociception or fear will dominate attention in a fish in novel object testing paradigm. This experimentally tractable animal model was used to investigate (1) the degree of neophobia to a novel object while experiencing noxious stimulation, (2) the response of the fish after removing the fear-causing event by using a familiar object, and (3) the effects of removing the nociceptive response by morphine administration and examining the response to a novel object. Control animals displayed a classic fear response to the novel objects and spent most of their time moving away from this stimulus, as well as showing an increase in respiration rate when the novel object was presented. In contrast, noxiously stimulated animals spent most of their time in close proximity to the novel object and showed no additional increase in respiration rate to novel object presentation. There was evidence of a slight hypoalgesia in noxiously stimulated animals. The responses to familiar objects demonstrated that by familiarizing the animal with the object, fear was removed from the experiment. Both control and noxiously treated animals responded in similar ways to a novel object by spending the majority of their time in close proximity. Treatment with morphine reduced effects of noxious stimulation and appears to be an effective analgesic. After morphine administration, the acid-injected animals showed a neophobic response to a novel object and this was similar to the response of the control fish, with a similar amount of time spent moving away from the object and an increase in ventilation in response to the novel object. Morphine affected the fear response because both groups approached the novel object more quickly than the non-morphine controls. These results suggest that nociception captures the animals attention with only a relatively small amount of attention directed at responding to the fear of the novel object.

The Long-Term Benefits of Human Generosity in Indirect Reciprocity

Among the theories that have been proposed to explain the evolution of altruism are direct reciprocity and indirect reciprocity. The idea of the latter is that helping someone or refusing to do so has an impact on ones reputation within a group. This reputation is constantly assessed and reassessed by others and is taken into account by them in future social interactions. Generosity in indirect reciprocity can evolve if and only if it eventually leads to a net benefit in the long term. Here, we show that this key assumption is met. We let 114 students play for money in an indirect and a subsequent direct reciprocity game. We found that although being generous, i.e., giving something of value to others, had the obvious short-term costs, it paid in the long run because it builds up a reputation that is rewarded by third parties (who thereby themselves increase their reputation). A reputation of being generous also provided an advantage in the subsequent direct reciprocity game, probably because it builds up trust that can lead to more stable cooperation.

Environmental variability in the early rearing environment generates behaviourally flexible cod: implications for rehabilitating wild populations

The release of hatchery-reared fishes for restoring threatened and endangered populations is one of the most controversial issues in applied ecology. A central issue has been to determine whether releases cause extinction of local wild populations. This may arise either through domesticated or non-local fishes hybridizing with wild fishes, or through inappropriate behavioural interactions; for example, many hatchery fishes show exaggerated aggressive and competitive behaviour and out-compete wild counterparts. The impact of the impoverished hatchery environment in shaping behaviour is only now receiving attention. Attempts to counteract hatchery-related behavioural deficiencies have utilized intensive training programmes shortly before the fishes are released. However, we show here that simple exposure to variable spatial and foraging cues in the standard hatchery environment generates fishes with enhanced behavioural traits that are probably associated with improved survival in the wild. It appears that fishes need to experience a varying and changeable environment to learn and develop flexible behaviour. Using variable hatchery rearing environments to generate suitable phenotypes in combination with a knowledge of appropriate local genotypes, rehabilitation of wild fishes is likely to succeed, where to date it has largely failed.

The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback

The capacity to learn enables animals to match their phenotypic response to a changing environment on the basis of experience but learning is likely to incur costs such as the cost of making mistakes or the energetic cost of processing information. Little is known about how animals optimize the use of learned behaviour within their natural environments such that potential costs are minimized. We investigated whether the use of local landmarks in learning orientation routes by the three-spined stickleback, Gasterosteus aculeatus, varied in response to the visual stability of their natural habitats. Sticklebacks collected from five fast-flowing rivers and five ponds were trained to locate a hidden reward in a T-maze. Locating the reward required the fish to learn a body-centred algorithmic behaviour (turn left or right) or to follow plant landmarks. Probe trials, in which these cues conflicted, revealed which spatial cue the fish was using. Pond fish appeared to rely more than river fish on visual landmarks, which is consistent with the suggestion that even within a species, learned behaviour is fine-tuned in response to local environmental conditions. Landmarks may be reliable indicators of location only in stable pond habitats. In rivers, turbulence and flow may continually disrupt the visual landscape such that river fish may benefit from learning orientation routes only if learning is constrained so that unreliable visual cues are ignored. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.