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Into the wild: developing field tests to examine the link between elasmobranch personality and laterality
Abstract
The field of animal personality has received considerable attention in past decades, yet few studies have examined personality in the wild. This study investigated docility, a measure of boldness, in two Port Jackson shark (Heterodontus portusjacksoni) populations using field tests, and if laterality differences explained docility levels. We developed a struggle test as an assay for docility, which is particularly amenable to field studies. The struggle test was effective, and repeatable inter-individual docility differences were observed. Sex, but not population, influenced docility scores, with male sharks being less docile than females. This difference is likely due to the contrasting role each sex plays during mating. We also found individualized lateralization. However, no individual-level relationship between lateralization and docility was detected. Despite reported links between laterality and some personality traits, the relationship between laterality and boldness remains inconclusive in sharks. Further studies will prove essential to clarify the mechanisms behind personality traits in vertebrates.
... Brain lateralization, i.e. asymmetry in hemispheric functions, has been hypothesized as one of the possible proximate neurophysiological mechanisms that maintain personality variation [12,13]. Brain lateralization is expressed as a preference for using the contralateral part of the body and is often measured either as a limb preference [14][15][16][17][18], eye dominance [19,20] or tail and body orientation [12,21,22]. Brain lateralization is present both in vertebrates and invertebrates (reviewed in [23,24]), and it provides various benefits in terms of enhanced cognition, social cohesion and better predator detection while foraging [25][26][27], thus directly affecting an individual's survival. ...
... The link between brain lateralization and personality might be species-, task-or trait-specific. For example, there was no correlation between the swimming direction and stress reactivity or docility in Port Jackson sharks [22,36]. Likewise, studies reported no association between limb preference and scores on personality dimensions in cats [32], dogs [34] or donkeys [16]. ...
... Contrary to our prediction, neither direction nor strength of hand preference in a food-reaching task were linked to personality, as found also in humans and other species [16,34,35,42]. For instance, Extraversion and Agreeableness were not associated with the direction of limb preference in donkeys [16], lateral bias did not correlate with docility in sharks [22], and most of the personality dimensions did not show a link with paw preference in dogs [34]. There are several possible explanations for this result. ...
The proximate mechanisms underlying animal personalities, i.e. consistent inter-individual differences in behaviour, are a matter of discussion. Brain lateralization, expressed as the preferred use of the contralateral limb, has been suggested as one of these mechanisms. In this study, we measured a proxy of brain lateralization in captive common marmosets ( N = 28) by testing hand preference in a simple food-reaching task and evaluated personality by coding a wide range of behaviours observed in daily situations. We explored the links between personality and both direction and strength of hand preference, as well as age and sex, using linear models. Principal component analysis revealed that the stable behavioural variables were organized in three personality dimensions: Agreeableness, Extraversion and Neuroticism. Regarding hand preference, 14 individuals were left-handed, seven were right-handed and seven were ambilateral. Contrary to our predictions, we did not find any relationship between personality scores and hand preference or sex. Instead, age was a significant predictor of personality scores, with older individuals being more agreeable and less extraverted. The link between brain lateralization and personality seems to be equivocal and dependent on personality and brain lateralization assessment methods. Further examinations of other proximate mechanisms, such as physiology or (epi)genetics, may elucidate what drives personality variation in common marmosets.
... It is reasonable to assume that subjects spending a large proportion of time swimming along the mirrors differed in the shyness-boldness continuum compared to those who tended to spend less time close to the mirrors (Brown & Bibost, 2014a, 2014b. Moreover, several studies have found links between personality and laterality (e.g., Brown & Bibost, 2014a, 2014bByrnes, Vila-Pouca, Chambers, & Brown, 2016;Irving & Brown, 2013). ...
... It would be would be valuable to investigate whether guppies show a preferential eye usewhich reflects the use of one hemisphere of the brain compared to the other -when observing stimuli that differ in numerosity, similarly to that described for a wide range of other categories of stimuli (e.g., Bisazza, De Santi, & Vallortigara, 1999;Facchin et al., 1999). Finally, it is worth investigating other potential sources of individual variation in laterality such as the apparent link with personality (Brown & Bibost, 2014a, 2014bByrnes et al., 2016;Irving & Brown, 2013). ...
A large number of studies showed that fish possess numerical abilities similar to those reported in mammals and birds. However, inter-individual differences in numerical performance are repeatedly found with different types of stimuli and methodological approaches. A recent study on guppies, Poecilia reticulata, suggested that strongly lateralized individuals, assayed for eye preference in a mirror test, were better than poorly lateralized ones when tested for numerical abilities in a natural shoal choice. This study, however, had a potential confound; both the mirror and the shoal choice tests exploit the higher sociality and schooling tendencies in guppies. It is therefore possible that sociality rather than lateralization per se may have been responsible for the observed differences. In the present study, guppies were selected for high or low lateralization using a non-social test, the detour test. Subjects preferentially turning rightward (RD) or leftward (LD) when facing a dummy predator visible behind a barrier proved better than those with no preference (NL) when required to choose the larger of two groups in a shoal choice test. Our study supports the notion that inter-individual differences in the numerical abilities of guppies are related to their degree of cerebral lateralization.
... To date, few behavioral studies have demon- strated personality differences in the wild (but see Byrnes et al. 2016, May et al. 2016); yet validating behavioral traits with ecological (and physiologi- cal) data is pivotal to understanding the evolution of personality variation in natural populations (R eale et al. 2007(R eale et al. , Blaszczyk 2017. Thus, to quan- tify links between individual variation in behavior and ecology, we need to study free-ranging animals (Archard and Braithwaite 2010); and to attain generality, we need research on taxa from a wide variety of phylogenetic lineages. ...
... We repeated these measures whenever the individuals were re- handled to record growth or replace transmitter batteries. For 14 individuals that were captured and handled on two occasions, we assessed repeatabil- ity of struggling scores (and see Byrnes et al. 2016, for a similar method for elasmobranchs). ...
In many animal populations, individuals exhibit repeatable behavioral traits across a range of contexts, and similarly, individuals differ in ecological traits such as habitat use, home range sizes, growth rates, and mating success. However, links between an individual's positions on behavioral vs. ecological axes of variation remain relatively unstudied in the wild. In the course of fieldwork on a remote floodplain in tropical Australia, we quantified boldness and ecological traits in 86 free-ranging (radio-tracked) monitor lizards (Varanus panoptes). These large (up to 7 kg) lizards exhibited a spectrum of boldness, as reflected in correlated scores of responses to approach, handling, and novel prey. Bolder lizards had larger core home ranges and higher mating success and spent more time in areas of high predator abundance, and their seasonal regimes of predation-induced mortality differed from those of shyer lizards. Thus, behav-ioral differences among lizards underpin much of the variation in ecological traits and individual fitness within this population. Analyses of ecology and microevolution in natural populations cannot afford to ignore the complex covariation between behavior, ecology, and evolution in the wild.
... [50][51][52] Here we used a single test to represent boldness and averaged two repetitions for most individuals to increase the reliability of our measure somewhat. The number of struggles in the hand of a captor has been used to represent boldness in animals (e.g., 53 ), though others interpret it as docility 54,55 or obstinacy (e.g., 56 ). In any case, struggle number (or struggle time) in restraint is typically correlated with boldness established by other measures (emergence, exploration, etc.; 24,55 ). ...
BACKGROUND
Behavioral mechanisms underlying avian deterrence by lasers in sweet corn are not known, and we evaluated them in a rigorous aviary experiment. Eighteen flocks of European starlings (Sturnus vulgaris) foraged on sweet corn for several days in control and laser treated plots with ripe sweet corn while data were collected on where birds were distributed and how long birds foraged on corn. In 16 trials, fresh ears were presented on wooden sticks, and in two trials birds foraged on natural corn grown from seed. Birds were sexed and boldness scores were obtained. We predicted that (a) birds would avoid foraging on ears in laser plots and (b) if they did feed, lasers would reduce foraging bout duration.
RESULTS
Laser treatments reduced the probability that birds would feed on sweet corn ears, and to a striking degree in Natural Trials. We did not detect direct effects of laser exposure on foraging bout duration, but when corn foliage was low, bolder birds foraged longer in laser plots.
CONCLUSION
We provide the first quantification of bird foraging behavior in laser treated corn. The central mechanism underlying the effectiveness of laser scarecrows at reducing sweet corn damage is the prevention of settlement of depredating birds onto ripe ears. © 2025 Society of Chemical Industry. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.
... These little transponders are available in sizes as small as a grain of rice and are injected under the skin, into the body cavity, or into the musculature. We have deployed PIT tags in long-term studies of shark behavior to help us identify individuals after recapture over multiple years (Byrnes et al. 2016). We have also used them to monitor fish movements in a simple maze where the tagged fish had to swim through a doorway fitted with an antenna to access a food reward (Raoult et al. 2017). ...
... These little transponders are available in sizes as small as a grain of rice and are injected under the skin, into the body cavity, or into the musculature. We have deployed PIT tags in long-term studies of shark behavior to help us identify individuals after recapture over multiple years (Byrnes et al. 2016). We have also used them to monitor fish movements in a simple maze where the tagged fish had to swim through a doorway fitted with an antenna to access a food reward (Raoult et al. 2017). ...
Methods for Fish Biology, 2nd edition
Chapter 16: Behavior
Julianna P. Kadar, Catarina Vila Pouca, Robert Perryman, Joni Pini-Fitzsimmons, Sherrie Chambers, Connor Gervais, and Culum Brown
doi: https://doi.org/10.47886/9781934874615.ch16
Kadar, J. P., C. V. Pouca, R. Perryman, J. Pini-Fitzsimmons, S. Chambers, C. Gervais, and C. Brown. 2022. Pages 593–642 in S. Midway, C. Hasler, and P. Chakrabarty, editors. Methods for fish biology, 2nd edition. American Fisheries Society, Bethesda, Maryland.
Humans interact with fish in a wide variety of contexts. Fish are rapidly becoming the go-to model for medical research because of the conservative nature of vertebrate physiology. We catch and grow fish in captivity for human consumption and frequently rear fish for release into the wild either to supplement wild populations to enhance fisheries or as a conservation measure. In all cases, understanding fish behavior is vital whether you are interested in stock management, conservation biology, or animal welfare (Brown 2015).
Gone are the days when fish were viewed as mindless automata. We now know that fish behavior is highly flexible, providing the plasticity to allow individuals to adjust to prevailing conditions or contexts (Bshary and Brown 2014). Their level of cognitive and behavioral sophistication is on par with the rest of the vertebrates (Bshary and Schäffer 2002; Vila Pouca and Brown 2018a; 2018b). Unsurprisingly, a change in behavior is often the first sign that something has shifted in the environment; thus, behavioral studies are at the forefront of environmental and ecotoxicological research (Brown 2012; Oulton et al. 2014). The massive diversity of fishes (currently more than 32,000 described species), and the range of niches they occupy, means that generalization is nearly impossible. Thankfully, the approaches for studying fish behavior are also many and varied and rapidly developing with changes in technology.
Here we provide a brief overview of some of the emerging methods for studying fish behavior. We will not be reviewing fish behavior in general since this is the topic of multiple books (e.g., Magnhagen et al. 2008; Brown et al. 2011), nor will we be providing a general overview of how to study animal behavior. Such details can readily be found in any of the many excellent texts on animal behavior or behavioral ecology (Davies 1991; Dugatkin and Earley 2004; Alcock 2005; Goodenough et al. 2009). Many people study fish behavior under captive conditions where it is possible to control the environment and observe behaviors that can be attributed to specific cognitive processes. In most instances, it is simply a matter of refining the standard methods to suit the aquatic environment and the species of interest. The main difficulties of studying fish behavior arise when trying to observe them in their natural environment. The underwater world is not a place with which most people are comfortable or familiar. Humans can stay only so long in the watery world of fishes, so many of the methods we describe here attempt to overcome these problems by studying fish behavior remotely.
... Thus, more studies are needed to elucidate which collection techniques, and in which organisms, biased collection occurs. Furthermore, while there has been a call for more behavioral studies of populations in the wild to address concerns of lab acclimation (Adriaenssens & Johnsson, 2011;Dall & Griffith, 2014), few studies have attempted to experimentally measure behavioral types of fish directly in the field, especially compared with other taxa (but see Brown et al., 2005;Byrnes et al., 2016;Wong et al., 2017 for in situ studies). ...
It is well known that fishing is size-selective, but harvest may also inadvertently target certain behavioral types or personalities. Changes in the abundance of behavioral types within a population have implications for fisheries management, including affecting catch rates, individual growth, and food web dynamics. Using streamside behavioral assays, we quantified the repeatability of behaviors in a population of Baikal grayling (Thymallus baicalensis) in northern Mongolia, a popular sport fish and important local predator. We assessed whether different angling techniques (i.e., fly or spinning gear) collected different behavioral types and whether variation in behavior was associated with body condition or diet (i.e., using stable isotope analysis). Surprisingly, we found no evidence for consistent individual differences in several behaviors within this population. Furthermore, differences in mean behaviors were not predicted by angling gear, body condition, or carbon and nitrogen isotopic signatures. We suggest that since this is a fished population, the range of behavioral variability in the population may have been reduced through previous behaviorally selective harvest. This might explain both the lack of difference in mean behaviors between fish caught by both gear types and the lack of evidence for consistent individual differences in behavior within the sampled population.
... However, Bass et al. (2021) and the results of this study suggest that there may be some diel Byrnes et al. (2016) found differences in the docility of male and female H. portusjacksoni and suggest that these differences may be due to the contrasting roles that each sex plays during courtship. The extent to which docility and other personality traits, such as boldness or aggression, influence the high individual variation in residency, roaming and dispersion of sharks is a priority for future research. ...
Examining the movement ecology of mesopredators is fundamental to developing an understanding of their biology, ecology and behaviour, as well as the communities and ecosystems they influence. The limited research on the residency and movements of benthic marine mesopredators has primarily used visual tags, which do not allow for the efficient and accurate monitoring of individual space use. In this study, the authors investigated the residency and movement patterns of Port Jackson sharks Heterodontus portusjacksoni (Meyer 1793) at a breeding aggregation site in Jervis Bay, south‐eastern Australia, using passive acoustic telemetry to further our understanding of the movement ecology of these important mesopredators. Between 2012 and 2014, individuals were tagged with acoustic transmitters, and their residency and movements within the bay were monitored for up to 4 years. H. portusjacksoni showed strong preferences for particular reefs within and between breeding seasons. Males had significantly higher residency indices at their favoured sites relative to females, suggesting that males may be engaging in territorial behaviour. Conversely, female H. portusjacksoni exhibited higher roaming indices relative to males indicating that females may move between sites to assess males. Finally, H. portusjacksoni showed temporal variation in movements between reefs with individuals typically visiting more reefs at night relative to the day, dusk and dawn corresponding with their nocturnal habits.
... To measure the behavioral attributes of wild reptiles, researchers must adapt their scoring systems to the ecology of the species in question (Byrnes et al., 2016;Ward-Fear et al., 2018). The four behavioral measures listed below are appropriate for assaying lace monitors along a shyness/boldness axis (see Results). ...
Anthropogenic activities often create distinctive but discontinuously distributed habitat patches with abundant food but high risk of predation. Such sites can be most effectively utilized by individuals with specific behaviors and morphologies. Thus, a widespread species that contains a diversity of sizes and behavioral types may be pre‐adapted to exploiting such hotspots. In eastern Australia, the giant (to >2 m) lizard Varanus varius (lace monitor) utilizes both disturbed (campground) and undisturbed (bushland) habitats. Our surveys of 27 sites show that lizards found in campgrounds tended to be larger and bolder than those in adjacent bushland. This divergence became even more marked after the arrival of a toxic invasive species (the cane toad, Rhinella marina) caused high mortality in larger and bolder lizards. Some of the behavioral divergences between campground and bushland lizards may be secondary consequences of differences in body size, but other habitat‐associated divergences in behavior are due to habituation and/or nonrandom mortality. Lace monitors (Varanus varius) are keen exploiters of anthropogenically disturbed habitat; however, only a subset of morphological and behavioral phenotypes in this species favor these artificial environments (i.e., large, bold individuals). The arrival of a toxic invader (Rhinella marina) may further exacerbate phenotypic divergences.
... This reptile species can be aggressive when agitated; such that lower struggle scores represent a shyer response. Such behaviours have been used to quantify boldness in many taxa, including sheep (Réale et al., 2000;Murphy et al., 1994), foxes (Korhonen & Niemela, 1996), mink (Korhonen et al., 2002), pigs (Janczak et al., 2003); and sharks (Byrnes et al., 2016). These behaviours are repeatable within individual Varanus panoptes, are correlated, and can be combined to produce a measure of boldness with biological relevance (see Ward-Fear et al., 2018). ...
Within all wild populations, individuals vary in ways that affect their vulnerability to threatening processes. Understanding that variation may clarify mechanisms of population persistence and/or evolution. In Australia, Yellow-spotted Monitors (Varanus panoptes), decline by >90% when toxic Cane Toads (Rhinella marina) invade an area. Taste-aversion training (exposing animals to non-lethal toads) can buffer impacts; but does pre-existing behavioural variation also influence survival? An individual’s fate can be predicted from its behaviour during aversion-training trials. Lizards presented with small toads either consumed them, rejected them, or fled. When Cane Toads invaded our study site, mortality was lower in lizards that ‘consumed’ (aversion-trained) than in those that ‘fled’ (untrained), but even lower in lizards that ‘rejected’ toads outright. Thus, animals reluctant to consume toads in trials survived despite never being aversion-trained. In this system, lizard vulnerability is driven by boldness, behavioural responses to novel prey types, and the opportunity to learn aversion.
... Many elasmobranchs have developmental shifts in habitat and diet (Wetherbee et al. 2004) that may drive assortment in size-or sex-segregated groups (Wearmouth and Sims 2008). Recently, ex situ studies have shown that some species exhibit complex sociality, including social structure (Jacoby et al. 2010;Mourier et al. 2012), social learning (Guttridge et al. 2013;Thonhauser et al. 2013), and individual personalities (Jacoby et al. 2014;Byrnes et al. 2016). Due to the difficulty in observing multiple interactions between wild elasmobranchs, however, quantitative analysis of the importance of social relations to the structure of their populations is lacking (but see Guttridge et al. 2011;Mourier et al. 2012). ...
Understanding how individual behavior shapes the structure and ecology of populations is key to species conservation and management. Like many elasmobranchs, manta rays are highly mobile and wide-ranging species threatened by anthropogenic impacts. In shallow water environments, these pelagic rays often form groups and perform several apparently socially mediated behaviors. Group structures may result from active choices of individual rays to interact or passive processes. Social behavior is known to affect spatial ecology in other elasmobranchs, but this is the first study providing quantitative evidence for structured social relationships in manta rays. To construct social networks, we collected data from more than 500 groups of reef manta rays (Mobula alfredi) over 5 years in the Raja Ampat Regency of West Papua. We used generalized affiliation indices to isolate social preferences from non-social associations, the first study on elasmobranchs to use this method. Longer lasting social preferences were detected mostly between female rays. We detected assortment of social relations by phenotype and variation in social strategies, with the overall social network divided into two main communities. Overall network structure was characteristic of a dynamic fission-fusion society, with differentiated relationships linked to strong fidelity to cleaning station sites. Our results suggest that fine-scale conservation measures will be useful in protecting social groups of M. alfredi in their natural habitats and that a more complete understanding of the social nature of manta rays will help predict population responses to anthropogenic pressures, such as increasing disturbance from dive tourism.
Significance statement
In social animals, relationships between individuals have important implications for species conservation. Like many other sharks and rays, manta rays are threatened species, and little is known about their natural behavior or how their populations are structured. This study provides evidence of social structure in a wild, free-ranging population of reef manta rays. We show for the first time that individual manta rays have preferred relationships with others that are maintained over time, and structured societies. This study extends our knowledge of elasmobranch ecology and population structuring. Results suggest that understanding social relationships in manta rays will be important in protecting populations from human impacts and developing sustainable, localized conservation and management initiatives.
... Repeatable individual behavioural traits such as boldness, activity, or sociability, for example, have now been widely demonstrated in teleosts (Budaev & Brown, 2011) and more recently in sharks (Byrnes et al., 2016b;Finger et al., 2017;Jacoby et al., 2014). Personality traits have been linked to the way individuals make decisions, which includes social behaviour decision-making (Raoult et al., 2017;Sih & Del Giudice, 2012;Trompf and Brown, 2014). ...
This study investigated whether captive‐reared juvenile Port Jackson sharks Heterodontus portusjacksoni choose to aggregate and if familiarity is one of the mechanisms driving social preference. In a controlled binary‐choice experiment, juvenile sharks were given the option to associate or not with unfamiliar conspecifics, or to associate or not with familiar conspecifics. In neither group did juvenile H. portusjacksoni actively choose to associate with conspecifics, but familiarity decreased the proportion of time spent near a conspecific only during the initial phase of the experiment. Treatment (1 or 3 shoal mates), sex and size had no effect on aggregation behaviour. These findings suggest that familiarity is not a driver of social preferences in juvenile H. portusjacksoni, contrary to results in another shark species. Additionally, adult H. portusjacksoni form large aggregations during the breeding season and actively associate with familiar sex and size‐matched individuals, thus our results suggest the species undergoes an ontogenetic shift in social behaviour.
... Gummy sharks (Mustelus antarcticus) caught on longlines in the field rested throughout most of the capture event, whereas animals caught on experimental gear in the laboratory were nearly continuously active (Frick et al., 2010;Guida et al., 2016Guida et al., , 2017a. Intra-specific variation in responses to capture have received far less attention, although recent evidence of personality in sharks suggests that individuals exhibit unique, repeatable behaviours, including responses to capture and handling (Wilson et al., 2015;Byrnes et al., 2016aByrnes et al., , 2016bFinger et al., 2018). Laboratory studies have been instrumental in providing preliminary insights into species-specific responses to capture, but there is a need for field-based studies to define intra-and inter-specific differences in exercise intensity of sharks during longline capture, especially given apparent contradictory responses between wild and captive studies. ...
Some shark populations face declines owing to targeted capture and by-catch in longline fisheries. Exercise intensity during longline capture and physiological status may be associated, which could inform management strategies aimed at reducing the impacts of longline capture on sharks. The purpose of this study was to characterize relationships between exercise intensity and physiological status of longline-captured nurse sharks (Ginglymostoma cirratum) and Caribbean reef sharks (Carcharhinus perezi). Exercise intensity of longline-captured sharks was quantified with digital cameras and accelerometers, which was paired with blood-based physiological metrics from samples obtained immediately post-capture. Exercise intensity was associated with physiological status following longline capture. For nurse sharks, blood pH increased with capture duration and the proportion of time exhibiting low-intensity exercise. Nurse sharks also had higher blood glucose and plasma potassium concentrations at higher sea surface temperatures. Associations between exercise intensity and physiological status for Caribbean reef sharks were equivocal; capture duration had a positive relation with blood lactate concentrations and a negative relationship with plasma chloride concentrations. Because Caribbean reef sharks did not appear able to influence blood pH through exercise intensity, this species was considered more vulnerable to physiological impairment. While both species appear quite resilient to longline capture, it remains to be determined if exercise intensity during capture is a useful tool for predicting mortality or tertiary sub-lethal consequences. Fisheries management should consider exercise during capture for sharks when developing techniques to avoid by-catch or reduce physiological stress associated with capture.
... To date, only a handful of studies have investigated shark personality (see Finger et al., 2017). In Port Jackson sharks, individuals vary greatly and reliably in terms of boldness and stress reactivity (Byrnes and Brown, 2016), with differences between males and females (Byrnes et al., 2016b). They also show individual and sex-biased variation in laterality (i.e. the tendency for some neural functions of cognitive processes to be more dominant in one brain hemisphere than the other), which may be linked to stress reactivity (Byrnes et al., 2016a). ...
... Evidence for personality was recently demonstrated in a study that involved capturing and testing Port Jackson sharks in the field (Byrnes et al. 2016a). The researchers used a docility test that measured the shark's response to human handling (e.g., Martin and Réale 2008), and a lateralization test that recorded if and which side a shark rolled onto once it landed on a boat. ...
Because of its impact on our understanding of evolution and ecology, animal personality has become an important area of research within behavioral ecology. Indeed, individual variation is no longer considered random noise but as a consistent phenomenon that impacts animal biology. However, research on animal personality and individual differences has largely focused on small-bodied species, which means that sharks and other elasmobranchs are dramatically underrepresented. The aim of this chapter is to illustrate, using existing studies, the opportunities and challenges involved in studying Elasmobranchs in captivity and in the field. While doing so, we discuss how this work informs the fields of animal personality and elasmobranch conservation. Although the lack of data necessitates a focus on sharks with only a mention of rays, we hope that this chapter will stimulate further research on personality in this underrepresented group.
The notion that men are more variable than women has become embedded into scientific thinking. For mental traits like personality, greater male variability has been partly attributed to biology, underpinned by claims that there is generally greater variation among males than females in non-human animals due to stronger sexual selection on males. However, evidence for greater male variability is limited to morphological traits, and there is little information regarding sex differences in personality-like behaviours for non-human animals. Here, we meta-analysed sex differences in means and variances for over 2100 effects (204 studies) from 220 species (covering five broad taxonomic groups) across five personality traits: boldness, aggression, activity, sociality and exploration. We also tested if sexual size dimorphism, a proxy for sex-specific sexual selection, explains variation in the magnitude of sex differences in personality. We found no significant differences in personality between the sexes. In addition, sexual size dimorphism did not explain variation in the magnitude of the observed sex differences in the mean or variance in personality for any taxonomic group. In sum, we find no evidence for widespread sex differences in variability in non-human animal personality.
The study of laterality (i.e. asymmetries of brain and behaviour) is a potential non-invasive approach to gain insights into the common neural mechanisms underpinning both personality and emotions in animals. The hypotheses underlying this thesis state that the left (respectively the right) hemisphere regulates approach or positive (respectively avoidance or negative) emotions. The goal of this thesis was to study lateralized motor functions (Study 1) and their associations with personality indices (Study 2), and the effect of monocular viewing on emotional reactions (Study 3) in pigs.
Open access: https://doi.org/10.18453/rosdok_id00002791
The development of adaptive responses to novel situations via learning has been demonstrated in a wide variety of animal taxa. However, knowledge on the learning abilities of one of the oldest extant vertebrate groups, Chondrichthyes, remains limited. With the increasing interest in global wildlife tourism and shark feeding operations, it is important to understand the capacities of these animals to form associations between human activities and food. We used an operant conditioning regime with a simple spatial cognitive task to investigate the effects of reinforcement frequency and reward magnitude on the learning performance and memory retention of Port Jackson sharks (Heterodontus portusjacksoni). Twenty-four Port Jackson sharks were assigned one of four treatments differing in reward magnitude and reinforcement frequency (large magnitude–high frequency; large magnitude–low frequency; small magnitude–high frequency; small magnitude–low frequency). The sharks were trained over a 21-day period to compare the number of days that it took to learn to pass an assigned door to feed. Sharks trained at a high reinforcement frequency demonstrated faster learning rates and a higher number of passes through the correct door at the end of the trials, while reward magnitude had limited effects on learning rate. This suggests that a reduction in reinforcement frequency during tourism-related feeding operations is likely to be more effective in reducing the risk of sharks making associations with food than limiting the amount of food provided.
In dieser Doktorarbeit behandle ich verschiedene Persönlichkeitsaspekte von jugendlichen Zitronenhaien (Negaprion brevirostris). Ich habe wiederholt Individuen in einem neuartigen Testfeld untersucht. Diese Experimente zeigten, dass jugendliche Zitronenhaie sich konstant verschieden verhalten. Außerdem konnte ich durch eine wiederkehrende Exposition in dem neuartigen Testfeld ein Gewöhnungsverhalten aufzeigen. Gewöhnung war ein Indikator, dass dieser Test es möglich macht, Reaktionen auf Veränderungen zu erforschen. Und endlich zeigte dieses Experiment dass Individuen verschiedene Gewöhnungsraten besitzen. Zweitens testete ich konsistente individuelle Verschiedenheiten in einigen der sozialen Verhaltensweisen über Zeiträume von einigen Tagen bis Perioden von vier Monaten. Während des neuerlichen Tests von Individuen wurde die Zusammensetzung der Gruppen geändert, um sicher zu gehen, dass die Wiederholbarkeit nicht vom gleichen sozialen Umfeld zwischen den wiederholten Versuchen kam. Hier wiederum fand ich, dass jugendliche Zitronenhaie Persönlichkeitsdifferenzen in ihrem sozialen Umfeld besaßen und dies trotz der veränderten Gruppen und einer viermonatigen Periode zwischen den Tests. Drittens testete ich die Präsenz eines Verhaltenssyndroms zwischen der Sozialisierung und der Reaktion auf ein neues Testfeld unter Berücksichtigung einer möglichen Variation dieses Syndroms durch Ontogenese und den Fangplatz. Dazu untersuchte ich noch die Dauerhaftigkeit von individuellen Unterschieden in verschiedenen Altersklassen und von verschiedenen Fangplätzen. Ich fand eine starke negative Korrelation zwischen der Soziabilität und der Reaktion auf Ungewohntes bei den Haien, in einer von zwei getesteten Kinderstuben, aber nur wenn sie älter als ein Jahr waren. Dazu fand ich, dass Haie, die weniger als ein Jahr alt waren, keine langdauernde Verhaltenskonsistenz zum Gegensatz zu älteren Haien zeigten.
The marine environment is filled with biotic and abiotic sounds. Some of these sounds predict important events that influence fitness while others are unimportant. Individuals can learn specific sound cues and ‘soundscapes’ and use them for vital activities such as foraging, predator avoidance, communication and orientation. Most research with sounds in elasmobranchs has focused on hearing thresholds and attractiveness to sound sources, but very little is known about their abilities to learn about sounds, especially in benthic species. Here we investigated if juvenile Port Jackson sharks could learn to associate a musical stimulus with a food reward, discriminate between two distinct musical stimuli, and whether individual personality traits were linked to cognitive performance. Five out of eight sharks were successfully conditioned to associate a jazz song with a food reward delivered in a specific corner of the tank. We observed repeatable individual differences in activity and boldness in all eight sharks, but these personality traits were not linked to the learning performance assays we examined. These sharks were later trained in a discrimination task, where they had to distinguish between the same jazz and a novel classical music song, and swim to opposite corners of the tank according to the stimulus played. The sharks’ performance to the jazz stimulus declined to chance levels in the discrimination task. Interestingly, some sharks developed a strong side bias to the right, which in some cases was not the correct side for the jazz stimulus.
Despite substantial research interest in understanding individual-level consistency in behavioral attributes, significant knowledge gaps remain across traits and taxa. For example, relatively few studies have looked at social personality in large marine species such as elasmobranchs and whether or not individual differences in behavior are maintained in unstable social groups (i.e., fission-fusion dynamics). However, it is important to investigate this topic in other model species than the usually small species with short generation times typically investigated in these areas of behavioral ecology. Indeed, studies on ecologically diverse taxa could provide mechanistic insights into the emergence and maintenance of animal personality and dynamics of social groups in animals. In addition, understanding social behavior at the group- and individual-level could improve conservation management of these large animals with long generation times (e.g., removal of particular behavioral types by fisheries practices). Here, we investigated consistent individual differences in sociability in wild juvenile lemon sharks (Negaprion brevirostris) over both short- (4 to 18 days) and long-term (4 months) sampling periods. Individual sharks were observed in social groups and scored according to the number of social interactions performed during observations. Despite variable individual group compositions between repeated trials, sharks showed consistent individual differences in their social behavior over both time scales. These results suggest reduced plasticity and highlight individuality as an important explanatory variable for the social dynamics of juvenile lemon sharks. In addition, long-term stability observed in this wild population demonstrates the importance of personality in the daily behavioral repertoire of juvenile lemon sharks. Our results are discussed in the context of other shark studies and taxonomic groups and potential avenues for future research are proposed.
Significance statement
This study investigated the social personality axis in a wild population of juvenile lemon sharks. First, we demonstrated consistent individual differences in their tendency to socialize. Second, we showed that individuals maintained their differences over a four-month period in the wild. Finally, we found that individual social behaviors were maintained despite being tested in variable group compositions. These results highlight the importance of individuality in the social dynamic of a poorly investigated animal and suggest personality as an important aspect of juvenile lemon sharks’ everyday life over a relatively long-term period.
The shy–bold continuum is recognized as a fundamental axis of behavioral variation in humans, but 3 major issues have not been addressed. First, the taxonomic distribution of shyness and boldness is unknown. Second, the ecological consequences of shyness and boldness have not been studied in natural populations. Third, no one has tried to predict and test patterns of shyness and boldness that might result from natural selection. We show that a shy–bold continuum, which influences diet, predator risk, and parasite fauna, exists in juvenile pumpkinseed sunfish (Lepomis gibbosus). Individual differences are relatively stable in nature but seem to disappear when the fish are held in social and ecological isolation in the laboratory. Thus, phenotypic stability may not reflect innate tendencies to be shy or bold but rather environmental conditions that maintain differences between phenotypically plastic individuals.
Emotions such as fear in vertebrates are often strongly lateralised, that is, a single cerebral hemisphere tends to be dominant when processing emotive stimuli. Boldness is a measure of an individual’s propensity to take risks and it has obvious connections with fear responses. Given the emotive nature of this well-studied personality trait, there is good reason to suspect that it is also likely to be expressed in a single hemisphere. Here, we examined the link between laterality and boldness in wild and captive-reared rainbowfish, Melanotaenia nigrans. We found that fish from the wild were bolder than those from captivity, which might be a reflection of the differences in the level of predation pressure experienced by the two populations. Secondly, we found that non-lateralised fish were bolder than strongly lateralised fish. In addition, differences in boldness scores between left- and right-biased fish were revealed. We suggest that variation in cerebral lateralisation contributes to the persistence of individual differences in boldness scores in animal populations.
The shy–bold continuum is recognized as a fundamental axis of behavioral variation in humans, but 3 major issues have not been addressed. First, the taxonomic distribution of shyness and boldness is unknown. Second, the ecological consequences of shyness and boldness have not been studied in natural populations. Third, no one has tried to predict and test patterns of shyness and boldness that might result from natural selection. The authors show that a shy–bold continuum, which influences diet, predator risk, and parasite fauna, exists in juvenile pumpkinseed sunfish. Individual differences are relatively stable in nature but seem to disappear when the fish are held in social and ecological isolation in the laboratory. Thus, phenotypic stability may not reflect innate tendencies to be shy or bold but rather environmental conditions that maintain differences between phenotypically plastic individuals. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
When several personality traits covary, they form a behavioral syndrome. Understanding the evolutionary dynamics of a behavioral syndrome requires knowledge of its genetic underpinning. At present, our understanding of the genetic basis of behavioral syndromes is largely restricted to domestic and laboratory animals. Wild behavioral syndromes are mostly inferred on the basis of phenotypic correlations, and thus make the "phenotypic gambit" of assuming that these phenotypic correlations capture the underlying genetic correlations. On the basis of 3 years of reciprocal cross-fostering of 2896 nestlings of 271 families within a pedigreed population, we show that the nestling personality traits handling aggression, breathing rate, and docility are heritable (h(2) = 16-29%), and often have a pronounced "nest-of-rearing" variance component (10-15%), but a relatively small "nest-of-origin" variance component (0-7%). The three nestling personality traits form a behavioral syndrome on the phenotypic and genetic level. Overall, the phenotypic correlations provide a satisfactory description of the genetic ones, but significantly underestimate the magnitude of one of the pairwise genetic correlations, which mirrors the conclusion based on domestic and laboratory studies.
There is a growing interest in animal person-ality because individual variation is the substrate of the evolutionary process. Despite revelations that personality traits affect key fitness variables, little is known about the proximate mechanisms generating consistent behavioural differences between individuals. Boldness, the propensity to take risks, is one of the most widely studied aspects of personality in fishes. We assessed the position of juvenile Argyosomus japonicus on the ''boldness–shyness'' contin-uum by repeatedly recording the time taken to exit a refuge and explore a novel environment. Stress-related hormone concentrations after exposure to a mild stressor were ana-lysed 1 month before behavioural assays and found to be significantly linked to boldness scores. Shy fish had sig-nificantly higher plasma cortisol concentrations in response to handling stress than bold fish. Spontaneous switching between personality categories occurred between trials, highlighting the importance of repeated testing of person-ality traits over time to correctly attribute personality.
A behavioral syndrome is a suite of correlated behaviors expressed either within a given behavioral context (e.g., correlations between foraging behaviors in different habitats) or across different contexts (e.g., correlations among feeding, antipredator mating, aggressive, and dispersal behaviors). For example, some individuals (and genotypes) might be generally more aggressive, more active or bold, while others are generally less aggressive, active or bold. This phenomenon has been studied in detail in humans, some primates, laboratory rodents, and some domesticated animals, but has rarely been studied in other organisms, and rarely examined from an evolutionary or ecological perspective. Here, we present an integrative overview on the potential importance of behavioral syndromes in evolution and ecology. A central idea is that behavioral correlations generate tradeoffs; for example, an aggressive genotype might do well in situations where high aggression is favored, but might be inappropriately aggr
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 striking ability of territory owners to repel intruders has generated a number of theoretical explanations as well as
experimental studies in many animal species. However, effects of individual habitat preferences on territorial defence have
rarely been studied. From the territory value hypothesis, we predicted that owners of preferred habitats should invest more
resources in defence than owners of non-preferred habitats. We tested this prediction with young territorial brown trout in
a two-stage experiment. First, trout were allowed to choose individually between gravel and a uniform bright substrate. As
expected, they showed a significant (79%) preference for gravel. However, there was considerable variation between individuals
in substrate preference, with a few fish preferring the bright substrate. Half of the tested fish were then transferred to
a gravel substrate and the rest to a bright substrate, manipulating habitat type in relation to preference. Territory owners
were then staged against size-matched intruders whereupon contest aggression was observed and the winner of each contest determined.
Overall, owners won most of the contests. Satisfied owners won 86% and owners of less preferred territories, 74% of the contests.
Furthermore, more satisfied owners attacked sooner and were more aggressive relative to the intruders. We conclude that brown
trout show individual variation in habitat preference, which appears to be linked with their investment in territorial defence.
These results suggest that understanding and modelling of animal contests could benefit from considering how territorial defence
is influenced by individual habitat preference and specialisation.
Orientational asymmetries of male gelada baboons were assessed to determine visual field preferences during agonistic and post-conflict behaviour using photographic sequences of aggressive interactions and records of facial injuries. Both opponents used their left visual field significantly more frequently than their right during fights, threats and approaches; the degree of left visual field preference varied with the level of negative emotion. During post-conflict behaviour, only the non-retreating animal showed a significant left visual field preference. The observed left visual field preferences appear to indicate a right hemisphere dominance in the processing of emotional information. Other possible causes of the baboons' observed visual field preference (including processing of auditory cues and visuospatial information, lateralised control of the brain over facial expression, and the asymmetrical signalling capacity of the face) are discussed.
Individual differences in temperament may affect how animals react to novel situations, avoid predation, invest in reproduction and behave in a variety of social contexts. Little information is available, however, about individual differences in temperament for wild animals. For bighorn sheep, Ovis canadensis, ewes captured as part of a long-term study, we compared behaviour during handling to behaviour in the field and reproductive history. We considered ‘bold’ ewes those that were frequently trapped during the summer, and assigned to each ewe a docility index based on her behaviour during handling. Measurements of temperament for the same individual at different captures were highly consistent. Temperament was not affected by reproductive status or age, nor was it related to body mass. Correlations between behaviour at the trap and in the field were weak and mostly nonsignificant, suggesting that temperament is domain specific rather than domain general. Bold ewes tended to start reproducing earlier and have higher weaning success than shy ewes. Variability in temperamental traits in the study population could be maintained by life-history trade-offs and by yearly changes in selective pressures.
In human and non-human animals the steroid hormones cortisol and testosterone are involved in social aggression and recent studies suggest that these steroids might jointly regulate this behavior. It has been hypothesized that the imbalance between cortisol and testosterone levels is predictive for aggressive psychopathology, with high testosterone to cortisol ratio predisposing to a socially aggressive behavioral style. In this review, we focus on the effects of cortisol and testosterone on human social aggression, as well as on how they might modulate the aggression circuitry of the human brain. Recently, serotonin is hypothesized to differentiate between impulsive and instrumental aggression, and we will briefly review evidence on this hypothesis. The aim of this article is to provide a theoretical framework for the role of steroids and serotonin in impulsive social aggression in humans.
Consistent individual differences in behaviour, and behavioural correlations within and across contexts, are referred to as animal personalities. These patterns of variation have been identified in many animal taxa and are likely to have important ecological and evolutionary consequences. Despite their importance, genetic and environmental sources of variation in personalities have rarely been characterized in wild populations. We used a Bayesian animal model approach to estimate genetic parameters for aggression, activity and docility in North American red squirrels (Tamiasciurus hudsonicus). We found support for low heritabilities (0.08-0.12), and cohort effects (0.07-0.09), as well as low to moderate maternal effects (0.07-0.15) and permanent environmental effects (0.08-0.16). Finally, we found evidence of a substantial positive genetic correlation (0.68) and maternal effects correlation (0.58) between activity and aggression providing evidence of genetically based behavioural correlations in red squirrels. These results provide evidence for the presence of heritable variation in red squirrel behaviour, but also emphasize the role of other sources of variation, including maternal effects, in shaping patterns of variation and covariation in behavioural traits.
Behavioral syndromes are suites of two or more behaviors that correlate across environmental contexts. The aggression-boldness syndrome links aggression, boldness, and exploratory activity in a novel environment. Although aggression-boldness has been described in many animals, the mechanism linking its behavioral components is not known. Here we show that mutation of the gene encoding fibroblast growth factor receptor 1a (fgfr1a) simultaneously increases aggression, boldness, and exploration in adult zebrafish. We demonstrate that altered Fgf signaling also results in reduced brain histamine levels in mutants. Pharmacological increase of histamine signaling is sufficient to rescue the behavioral phenotype of fgfr1a mutants. Together, we show that a single genetic locus can underlie the aggression-boldness behavioral syndrome. We also identify one of the neurotransmitter pathways that may mediate clustering of these behaviors.
Cerebral lateralization is an evolutionarily ancient adaptation, apparently ubiquitous among vertebrates. Despite demonstrated advantages of having a more lateralized brain, substantial variability in the strength of lateralization exists within most species. The underlying reasons for the maintenance of this variation are largely unknown. Here, we present evidence that the strength of lateralization is linked to a behavioural trait, aggressiveness, in the convict cichlid (Archocentrus nigrofasciatus), and that this relationship depends on the sex of the fish. This finding suggests that individual variation in behaviour may be linked to variation in cerebral lateralization, and must be studied with regard to the sex of the animal.
We investigated turning responses in 16 species of fish faced with a vertical-bar barrier through which a learned dummy predator was visible. Ten of these species showed a consistent lateral bias to turn preferentially to the right or to the left. Species belonging to the same family showed similar directions of lateral biases. We performed an independent test of shoaling tendency and found that all gregarious species showed population lateralisation, whereas only 40% of the non-gregarious species did so. The results provide some support to the Rogers (1989) hypothesis that population lateralisation might have been developed in relation to the need to maintain coordination among individuals in behaviours associated with social life.
Consistent individual differences (CIDs) in behavior are a widespread phenomenon in animals, but the proximate reasons for them are unresolved. We discuss evidence for the hypothesis that CIDs in energy metabolism, as reflected by resting metabolic rate (RMR), promote CIDs in behavior patterns that either provide net energy (e.g. foraging activity), and/or consume energy (e.g. courtship activity). In doing so, we provide a framework for linking together RMR, behavior, and life-history productivity. Empirical studies suggest that RMR is (a) related to the capacity to generate energy, (b) repeatable, and (c) correlated with behavioral output (e.g. aggressiveness) and productivity (e.g. growth). We conclude by discussing future research directions to clarify linkages between behavior and energy metabolism in this emerging research area.
Levels of reproductively-related steroids were determined in captive male sand tiger sharks, Carcharias
taurus, maintained at two institutions: SeaWorld Adventure Park Orlando and the National Aquarium in Baltimore. Sexual conflicts were absent at the former, but were documented at the latter. Serum titers of 17β-estradiol, progesterone, testosterone, and 5α-dihydrotestosterone were determined via radioimmunoassay in adult male sharks from 1988 to 2000. Sampling overlap between the two institutions occurred for 3 months of the year, but steroid concentrations were compared only for April due to the occurrence of sexual conflicts in the sharks at the National Aquarium in Baltimore in that month. For April, testosterone and dihydrotestosterone were significantly higher in the SeaWorld males, and progesterone was significantly higher in the National Aquarium in Baltimore males, while estradiol was not significantly different. Steroid levels were also determined from serial samples taken monthly over 17 months from three male sharks and one female shark at the National Aquarium in Baltimore in 2001–2002 and were compared with corresponding observed sexual conflicts. The steroid levels obtained showed distinct annual hormonal cycles in the male sharks and corroborated a biennial cycle for the single serially-sampled female shark. Furthermore, the steroid levels for individual males correlated with sexual conflicts as well as their position within the male dominance hierarchy. As this species is depleted in some regions globally, insight into the steroid profile of mature sand tiger sharks is important for a greater understanding of the relationship between their reproductive physiology and behavior, and may aid in captive management and reproduction.
New technologies have vastly increased the available data on animal movement and behaviour. Consequently, new methods deciphering the spatial and temporal interactions between individuals and their environments are vital. Network analyses offer a powerful suite of tools to disentangle the complexity within these dynamic systems, and we review these tools, their application, and how they have generated new ecological and behavioural insights. We suggest that network theory can be used to model and predict the influence of ecological and environmental parameters on animal movement, focusing on spatial and social connectivity, with fundamental implications for conservation. Refining how we construct and randomise spatial networks at different temporal scales will help to establish network theory as a prominent, hypothesis-generating tool in movement ecology.
New technologies have vastly increased the available data on animal movement and behaviour. Consequently, new methods deciphering the spatial and temporal interactions between individuals and their environments are vital. Network analyses offer a powerful suite of tools to disentangle the complexity within these dynamic systems and we review these tools, their application, and how they have generated new ecological and behavioural insights. We suggest that network theory can be used to model and predict the influence of ecological and environmental parameters on animal movement, focusing on spatial and social connectivity, with fundamental implications for conservation. Refining how we construct and randomise spatial networks at different temporal scales will help establish network theory as a prominent, hypothesis-generating tool in movement ecology.
Model building and data analysis in the biological sciences somewhat presupposes that the person has some advanced education in the quantitative sciences, and statistics in particular. This requirement also implies that a person has substantial knowledge of statistical hypothesis-testing approaches. Such people, including ourselves over the past several years, often find it difficult to understand the information-theoretic approach, only because it is conceptually so very different from the testing approach that is so familiar. Relatively speaking, the concepts and practical use of the information-theoretic approach are much simpler than those of statistical hypothesis testing, and very much simpler than some of the various Bayesian approaches to data analysis (e.g., Laud and Ibrahim 1995 and Carlin and Chib 1995).
Ontogenetic niche shifts are common among animals, yet most studies only investigate niche shifts at the population level, which may overlook considerable differences among individuals in the timing and dynamics of these shifts. Such divergent behaviors within size-/age-classes have important implications for the roles a population-and specific age-classes-play in their respective ecosystem(s). Using acoustic telemetry, we tracked the movements of juvenile bull sharks in the Shark River Estuary of Everglades National Park, Florida, and found that sharks increased their use of marine microhabitats with age to take advantage of more abundant resources, but continued to use freshwater and estuarine microhabitats as refuges from marine predators. Within this population-level ontogenetic niche shift, however, movement patterns varied among individual sharks, with 47 % of sharks exhibiting condition-dependent habitat use and 53 % appearing risk-averse regardless of body condition. Among sharks older than age 0, fifty percent made regular movements between adjacent regions of the estuary, while the other half made less predictable movements that often featured long-term residence in specific regions. Individual differences were apparently shaped by both intrinsic and extrinsic factors, including individual responses to food-risk trade-offs and body condition. These differences appear to develop early in the lives of bull sharks, and persist throughout their residencies in nursery habitats. The widespread occurrence of intraspecific variation in behavior among mobile taxa suggests it is important in shaping population dynamics of at least some species, and elucidating the contexts and timing in which it develops and persists is important for understanding its role within communities.
1. The relationships between dominance status and individual differences in foraging behaviour, habitat use, growth and emigration were examined for fluvial red-spotted masu salmon, Oncorhynchus masou ishikawai, in a mountain stream. 2. Size-structured linear dominance hierarchies were recognized among individuals inhabiting the same stream pools. Observations on space utilization and foraging behaviour revealed fish to be either territorial or nonterritorial. Within each local pool, dominant fish exclusively occupied the mid or surface layer of the pools as foraging territories, whereas subordinates adopted nonterritorial tactics, primarily utilizing the bottom layer. 3. Of the territorial fish, more dominant individuals tended to occupy focal points nearer the pool inlet, where they had priority of access to drifting food items. These fish showed higher actual foraging rates, feeding upon larger prey than their subordinates. This foraging advantage resulted in their having larger daily growth increments. 4. The more dominant fish in each pool exhibited a more sedentary tendency than their subordinates. Population densities in the pools did not fluctuate appreciably owing to both emigration of nonterritorial subordinates and immigration. 5. These results support the hypothesis that unequal resource partitioning among individuals subject to a dominance hierarchy plays an important role in their density-dependent population regulation.
The central nervous system, and the brain in particular, is one of the most remarkable products of evolution. This system allows an individual to acquire, process, store and act on information gathered from the environment. The resulting flexibility in behavior beyond genetically coded strategies is a prime adaptation in animals. The field of animal cognition examines the underlying processes and mechanisms. Fishes are a particularly interesting group of vertebrates to study cognition for two reasons (Figure 1). First, they occupy a key position in the vertebrate phylogenetic tree: the common ancestor of the tetrapods was a bony fish. Thus, all vertebrates share key genetic features that code for the body structure, including the vertebrate brain. Similarities in brain structure and function are hence likely to be due to common ancestry. A second reason to study fish cognition is that fish have had their own independent evolution/radiation since they split from tetrapods. Bony fishes are by far the most species-rich vertebrate group. As a consequence, they provide the best options for a comparative approach that aims to link the evolution of cognition to a species’ ecology. Therefore, the study of fishes may reveal general principles of ecological effects on cognitive abilities in vertebrates.
Elasmobranch reproductive behavior has been inferred from freshly caught specimens, laboratory examinations of reproductive structures and function, or determined from direct observations of captive or free swimming wild animals. Several general behaviors have been described including seasonal sexual segregation, courtship and copulation. Courtship behavior was inferred for many species from the presence of scars and tooth cuts on the female's body, and noted in more detail from underwater observations. Copulation has been directly observed in captive settings for several species of elasmobranchs in large aquaria, and in the wild for three species of urolophids and for Triaenodon obesus and Ginglymostoma cirratum. A detailed ‘case history’ of nurse shark reproductive behavior is presented that may be used as a template for future work on shark reproductive behavior of other species. Our studies, using diver identifiable tags and in situ behavioral observations, provide unprecedented information on social structure and mating behavior in this species. Since 1993, 115 G. cirratum, 45 adults and 70 juveniles have been tagged in the Dry Tortugas, Florida. Observations show that adult males visit the study site every year with three males dominant. Individual adult females visit the study area to mate in alternate years. Polygyny and polyandry are common. Future research on reproductive behavior of elasmobranchs should address questions on male access to females, sexual selection and dominance hierarchies.
Androgens are classically thought of as the sex steroids controlling male reproduction. However, in recent years evidence has accumulated showing that androgens can also be affected by the interactions between conspecifics, suggesting reciprocal interactions between androgens and behaviour. These results have been interpreted as an adaptation for individuals to adjust their agonistic motivation and to cope with changes in their social environment. Thus, male– male interactions would stimulate the production of androgens, and the levels of androgens would be a function of the stability of its social environment w'challenge hypothesis', Gen. Comp. Endocrinol. 56 (1984) 417x. Here the available data on social modulation of androgen levels in male teleosts are reviewed and some predictions of the challenge hypothesis are addressed using teleosts as a study model. We investigate the causal link between social status, territoriality and elevated androgen levels and the available evidence suggests that the social environment indeed modulates the endocrine axis of teleosts. The association between higher androgen levels and social rank emerges mainly in periods of social instability. As reported in the avian literature, in teleosts the trade-off between androgens and parental care is indicated by the fact that during the parental phase breeding males decreased their androgen levels. A comparison of androgen responsiveness between teleost species with different mating and parenting systems also reveals that parenting explains the variation observed in androgen responsiveness to a higher degree than the mating strategy. Finally, the adaptive value of social modulation of androgens and some of its evolutionary consequences are discussed.
This study examined whether variation in the strength and direction of lateralization in a detour task was linked with variation in three common personality measurements: boldness, activity and sociability, in a population of wild guppies Poecilia reticulata. Additionally, the aim was to determine whether any consistent correlations between these behavioural traits, known as behavioural syndromes, were present in the study population. The results revealed that all three personality traits were highly repeatable over time in both sexes. Evidence of a complex syndrome in the form of a correlation between boldness, sociability and activity was found; however, this relationship was only present in males. Males that were more active in a familiar environment emerged more quickly from shelter into a novel environment and were more social. In general, male P. reticulata were bold, active and antisocial compared to females, with these differences probably a reflection of opposing life-history strategies. Only a weak link between the strength of cerebral lateralisation and personality was discovered and this was mediated by sex.
Predation is a strong selective force in most natural systems, potentially fueling evolutionary changes in prey morphology, life history and behaviour. Recent work has suggested that contrasting predation pressures may lead to population differentiation in personality traits. However, there are indications that these personality traits also differ between sexes and not necessarily in a consistent way between populations. We used an integrative approach to quantify boldness (latency to emerge from a shelter) in wild-caught guppies in relation to predation pressure, population origin, sex and size. In addition we quantified the repeatability of these personality traits. We show that predation regime had significant effects on emergence time. In general, fish from high predation localities emerged sooner from the shelter compared to those from low predation localities. We found strong sex differences; males were significantly bolder than females. The relationship between emergence time and body size was non-significant in all populations. We discuss what responses to expect from predator-naïve versus predator-experienced individuals and how this can be linked to the shyness–boldness continuum.
The role of female choice as a potential mechanism influencing male reproductive success in non-human primates is unclear. Few systematic studies have explicitly evaluated how female reproductive tactics modify male mating success. A 19-month field study of savanna baboons,Papio cynocephalus, was undertaken in Kenya in order to document patterns of mate choice and mate competition. Neither size dimorphism nor female competition hindered the expression of female choice. Female mating preferences affected the identity of mating partner and the probability of an escalated confrontation over access to a female. Reproductive tactics that diminished consortship duration included hiding from a male and approaching other males, whereas maintaining proximity to a male partner when he was aggressively challenged prolonged consortship duration. Non-cooperation in the form of mount rejection had no negative repercussions on male ejaculatory success and did not increase the chances of male abandonment. Male mating success depended more upon male than female reproductive tactics, and female tactics seemed to be based upon a propensity to mate with multiple males.
Behavioural traits related to temperament were studied and the genetic variability estimated in German Angus (Aberdeen Angus×German dual purpose breeds) and Simmental cattle. Temperament was defined as the behavioural response of the animal to handling. Five progeny groups of both breeds (Simmental cattle, n=206; German Angus cattle, n=249) were tested in 2 consecutive years, 2 and 3 weeks after weaning. The animals were tested individually with a combination of a non-restrained and a restrained test. Each animal was separated from a group of 10 (separation yard, 100m2) into a smaller area then confined in a corner of the restraint yard (25m2). Behaviour was recorded and temperament scores were given by three different observers. The parameters of separation time, time spent running, number of escapes, aggression, vocalisation and time spent in the corner directed by the handler were recorded. Analysis of variance was performed with a model including breed, year, handler and sex as fixed effects. The model for estimating heritability included the sire as a random effect and sex, year and handler as fixed effects. In both models a regression on the age of the calf was included. The estimated heritability (±S.E.) for the different characteristics of temperament were between 0.0 and 0.61 (±0.17) for German Angus and, 0.0 and 0.59 (±0.41) for Simmental cattle with highest values for temperament scores. These were negatively correlated with daily weight gain. Simmental cattle were more difficult to handle than German Angus when considering the different parameters. The estimated heritability of some behavioural traits open a way of selection for temperament in German Angus and Simmental cattle assuming the high standard errors of the estimated values were caused primarily by the limited number of animals.
Nine commerical herds were observed on three separate occasion for flight distance, i.e., how close a human can come before a stationary cow moves away, and approach distance, i.e., how close a cow will come to a stationary human. Herdsmen from each herd scored their cows on parlor behavior using a scoring system that ranged from 1 (the most docile) to 5 (the most aggressive). These three behavior factors were compared with milk production. Both mean flight distance and mean approach distance were 1.6 m. Mean parlor score was 2.2 and mean production was 9153 kg. These were significant inter-herd correlations between flight distance and approach distance (r=0.30), flight distance and parlor score (r=0.20), and parlor score and milk production (r=0.08); however, only flight distance and approach distance (r=0.18), and flight distance and parlor score (r=0.12) were significantly correlated within herds. There was no significant intraherd correlation between milk production and any of the behavioral factors considered. These findings indicate that while parlor score is associated with milk production across herds, flight distance and approach distance are not useful indicators of milk production.
Cerebral lateralization refers to the lateralized partitioning of cognitive function in either hemisphere of the brain. Using a standard detour test, we investigated lateralized behaviour in wild-caught, female poeciliid fish, Brachyraphis (=Brachyrhaphis) episcopi, from high- and low-predation areas. Wild fish were bred and their offspring reared under controlled laboratory conditions. These laboratory-reared fish were screened in the same laterality assays as their parents. We observed differences between wild-caught females and their laboratory-reared female offspring in the pattern of lateralization (tendency to use one hemisphere over the other to process information). Conversely, the strength of lateralization (consistency of hemispherical bias) was largely conserved between generations, consistent with it being a heritable character. Both wild-caught females from high-predation sites and their laboratory-reared offspring showed stronger lateralized behaviour than their counterparts from low-predation sites. This difference in strength of lateralization is likely to provide fitness benefits to fish that occur in high-predation areas by enabling them to school and watch for predators simultaneously (dual processing). We hypothesized that the differences in the pattern of lateralization observed between species, and populations within species, are due to the manner in which they perceive and classify stimuli in the world around them. In particular, the perceived emotive content or context of a scene is likely to vary between individuals that have had different life experiences.
A small but taxonomically diverse number of vertebrates have a left-eye preference for aggression, but this has been shown only in males. Here we present data consistent with a left-eye preference for aggressive rejection display in females of the striped plateau lizard, Sceloporus virgatus. Already-mated females perform this display, which contains key elements of male–male aggressive displays, to courting males. Lateral eye placement reduces binocular vision of such displays. In a field study, we recorded the responses of individual gravid females to one of three possible stimulus presentations: a tethered conspecific male presented so the female viewed him (1) from a head-on (HO) position, (2) with her left visual field (LVF) or (3) with her right visual field (RVF). Although a small proportion of all trials yielded no response, females were significantly less likely to show any response in RVF presentations compared with HO or LVF presentations. In a large majority of trials, females responded to males, and almost all responding females displayed aggressively. When females displayed after RVF presentations, a female was equally likely to use her LVF or RVF to view the male when she first performed an aggressive rejection display. In contrast, in LVF and HO presentations where females displayed, females were significantly more likely than expected by chance to use their LVF to view the males when they displayed. Charge, a very aggressive act, also was significantly more likely to occur when females were viewing males with their LVF than their RVF or HO. Finally, in a small number of unmanipulated natural encounters we observed, all females used their LVF to display to courting males. Our results suggest that, as in males of several vertebrate species, females show a left-eye bias for conspecific aggression.
It is not known whether sharksuckers have positive or negative effects on their hosts, partly because this association is difficult to study in free-ranging fish. I observed the behaviour of sharks with and without sharksuckers, to determine whether the hosts actively avoid sharksuckers. Wild blacktip sharks, Carcharhinus limbatus, took evasive actions when sharksuckers, Echeneis naucrates, attached to them, presumably to escape from skin irritation or hydrodynamical drag caused by the sharksuckers. Sharksuckers were most often attached to the belly or back of the shark, and sharks reacted most strongly to sharksuckers on their heads, sides, and dorsal fins. Observations of two captive bull sharks, Carcharhinus leucas, indicated that swimming speed increased when sharksuckers were attached. This paper supports the hypothesis that sharksucker attachment irritates sharks, and that the relationship between the two is best viewed as a subtle host–parasite interaction.
Animal temperament describes behavioural differences between individuals that are consistent across time and contexts. Variation in animal temperament is rapidly gaining interest and attention within behavioural and evolutionary ecology. If we are to understand the causes and consequences of temperament variation within and between populations we need to determine the selection pressures that affect temperament in natural environments. To date, however, the vast majority of temperament studies have been carried out on captive-bred individuals. This review highlights potential problems that arise from using captive animals to elucidate the ecological and evolutionary functions of temperament in wild populations. For example, development, learning and environmental variability can all affect behaviour. Thus, both environment and gene-by environment interactions can affect the fitness functions of different temperaments, and hence selection. We stress the need for measurements of repeatability and heritability, and the importance of biological and ecological validation of temperament tests in wild animals. We describe the limited evidence from wild populations of the fitness consequences of temperament variation, and the use of intra- and inter-specific comparisons to prove adaptation. To identify multiple axes of behavioural variation, and how these interact with environments that vary spatially and temporally, we need long-term studies on wild populations – yet few studies of this nature currently exist. Finally, and perhaps counter-intuitively, we suggest that there is much to be gained from incorporating some of the approaches and statistics employed in the much longer established field of human personality.
A pattern of hemispheric specialization common to all vertebrates has been presented (summarized in Fig. 6). It has been considered, as far as possible, in terms of behavior patterns that are important in the natural environment. Responses in foraging and prey capture are typical specializations of the left hemisphere and they are often apparent as rightward-directed responses. Responses to novel stimuli and potential predators are specializations of the right hemisphere and responses to these stimuli are directed preferentially to the animal's left side. The right hemisphere is also specialized for the expression of fear and aggression, and to process and memorize topographical information, essential in association with predator-escape responses. The baseline differences between the hemispheres are (1) rapid and species-typical responses being under the control of the right hemisphere and (2) responses requiring considered decision making being under control of the left hemisphere.
Similarly to other vertebrates, the androgen testosterone (T) is present in teleost fishes. In addition, 11-oxygenated androgens, especially 11-ketotestosterone (11KT) are present. 11KT is found in higher levels in the plasma of males than in females, whereas this is usually not the case for T. 11-Oxygenated androgens are generally more effective than T in stimulating secondary sexual characters, reproductive behaviour and spermatogenesis. Nevertheless, receptor-like binding has only reported for T and not for 11KT.
To investigate the ecological significance of personality, researchers generally measure behavioural traits in captivity. Whether behaviour in captivity is analogous to behaviour in the wild, however, is seldom tested. We compared individual behaviour between captivity and the wild in blue tits, Cyanistes caeruleus. Over two winters, 125 blue tits were briefly brought into captivity to measure exploratory tendency and neophobia using variants of standard personality assays. Each was then released, fitted with a passive integrated transponder. Using an electronic monitoring system, we then recorded individuals' use of feeders as they foraged in the wild. We used variation in the discovery of new feeders to score 91 birds for exploratory tendency in the wild. At eight permanent feeding stations, 78 birds were assayed for neophobia in the wild. Behavioural variation in the captive personality trials was independent of permanent (e.g. sex) and nonpermanent (e.g. condition or weather) sources of between-individual variation at capture. Individual exploratory tendency and neophobia were consistent and repeatable in captivity, and analogous traits were repeatable in the wild; thus all constituted personality traits in the blue tit. Exploratory tendency and neophobia were not correlated with each other, in either the captive or the wild context. Therefore they are independent traits in blue tits, in contrast to many species. Finally, exploratory tendency and neophobia measured in captivity positively predicted the analogous traits measured in the wild. Reflecting differences in the use of feeding opportunities, personality in captivity therefore revealed relevant differences in foraging behaviour between individuals.
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.
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.
Cerebral lateralization, the preferential use of one hemisphere of the brain to perform certain cognitive functions, is a widespread and evolutionarily ancient adaptation. Lateralization appears to enhance cognitive capacity, yet substantial individual variation in the strength cerebral lateralization is apparent in all species studied so far. It is puzzling that cerebral lateralization, a seemingly advantageous trait, has not been driven to fixation. It has been suggested that variation in lateralization may be linked to individual variation in behaviour, which itself may be subject to disruptive selection. We examined the relation between cerebral lateralization and individual variation in boldness in the convict cichlid, Archocentrus nigrofasciatus. We show that convict cichlids that are more strongly lateralized when exploring a familiar environment, but not a novel one, are quicker to emerge from a shelter in a test for boldness. The possibility that cerebral lateralization is linked to life history strategy is discussed.
Previous work has shown that predator inspection in mosquitofish, Gambusia holbrooki, is more likely to occur when a mirror image of the test fish is visible on its left rather than on its right side. We investigated whether this is due to a preference for using the right eye when fixating the predator or the left eye when fixating the mirror image, or a combination of both eye preferences. We found that mosquitofish preferentially used the left eye during sustained scrutiny of their mirror image when tested in the absence of any predator. On the other hand, when tested in a swimway for predator inspection responses in the absence of any mirror image (or other social stimuli), mosquitofish explored the environment with the left eye when at a distance and the right eye when near the predator.
Repeatability (more precisely the common measure of repeatability, the intra-class correlation coefficient, ICC) is an important index for quantifying the accuracy of measurements and the constancy of phenotypes. It is the proportion of phenotypic variation that can be attributed to between-subject (or between-group) variation. As a consequence, the non-repeatable fraction of phenotypic variation is the sum of measurement error and phenotypic flexibility. There are several ways to estimate repeatability for Gaussian data, but there are no formal agreements on how repeatability should be calculated for non-Gaussian data (e.g. binary, proportion and count data). In addition to point estimates, appropriate uncertainty estimates (standard errors and confidence intervals) and statistical significance for repeatability estimates are required regardless of the types of data. We review the methods for calculating repeatability and the associated statistics for Gaussian and non-Gaussian data. For Gaussian data, we present three common approaches for estimating repeatability: correlation-based, analysis of variance (ANOVA)-based and linear mixed-effects model (LMM)-based methods, while for non-Gaussian data, we focus on generalised linear mixed-effects models (GLMM) that allow the estimation of repeatability on the original and on the underlying latent scale. We also address a number of methods for calculating standard errors, confidence intervals and statistical significance; the most accurate and recommended methods are parametric bootstrapping, randomisation tests and Bayesian approaches. We advocate the use of LMM- and GLMM-based approaches mainly because of the ease with which confounding variables can be controlled for. Furthermore, we compare two types of repeatability (ordinary repeatability and extrapolated repeatability) in relation to narrow-sense heritability. This review serves as a collection of guidelines and recommendations for biologists to calculate repeatability and heritability from both Gaussian and non-Gaussian data.
The habenulae are part of an evolutionary conserved conduction system that connects the limbic forebrain areas with midbrain structures and is implicated in important functions such as feeding, mating, avoidance learning, and hormonal response to stress. Very early during zebrafish neurogenesis the parapineal organ migrates near to one habenula, commonly the left, inducing wide left-right habenular asymmetries in gene expression and connectivity. It was posited that this initial symmetry-breaking event determines the development of lateralized brain functions and early differences in epithalamic left-right asymmetry give rise to individual variation in coping styles and personality. We tested these two hypotheses by sorting zebrafish with left or right parapineal at birth using a foxD3:GFP marker and by measuring visual and motor laterality and three personality dimensions as they become adults. Significant differences between fish with opposite parapineal position were found in all laterality tests while the influence of asymmetry of the habenulae on personality was more complex. Fish with atypical right parapineal position, tended to be bolder when inspecting a predator, spent less time in the peripheral portion of an open field and covered a shorter distance when released in the dark. Activity in the open field was not associated to anatomical asymmetry but correlated with laterality of predator inspection that in turn was influenced by parapineal position. One personality dimension, sociality, appeared uncorrelated to both anatomical and functional asymmetries and was instead influenced by the sex of the fish, thus suggesting that other factors, i.e. hormonal, may be implicated in its development.