Personality counts: the effect of boldness on shoal choice in three-spined sticklebacks

doi:10.1016/j.anbehav.2009.03.004

Animal Behaviour

Volume 77, Issue 6, June 2009, Pages 1501-1505

https://doi.org/10.1016/j.anbehav.2009.03.004 Get rights and content

The grouping behaviour of fish is a widespread phenomenon of high biological significance but little is known as to how consistent individual behavioural differences may affect group joining preferences. When given the option to join either a shy or a bold shoal of three-spined sticklebacks, Gasterosteus aculeatus, both shy and bold individuals showed a strong preference for associating with bold fish. Personality type interacted with individual hunger levels to affect the extent of association, suggesting important strategy variation by focal fish in a competitive foraging environment. Furthermore, shoals modified their behaviour in relation to the focal individual. Individual behavioural differences were shown to have a complex role in influencing association preferences as well as driving previously unrecognized behavioural modifications in foraging groups.

Section snippets

Study Organism and Equipment

Stocks of three-spined sticklebacks were collected with sweep nets from the Histon and Swaffham Bulbeck areas of the River Cam, U.K. during 2007. They were transported to the laboratory in large buckets and immediately transferred to large glass aquaria where they were kept at 17 ± 1 °C on a 10:14 h light:dark regime for at least 1 month before being used in experiments. This study is part of a series of experiments that were approved under a nonregulatory procedures framework by the Animal Users

Results

Focal fish, irrespective of their personality and hunger status, showed a preference for spending time with the bold shoal (test for intercept of GLM being different from the expected value for no preference, that is, c ≠ arcsine (sqrt(0.5)): t₂₀₈ = 2.459, P = 0.015). There was also a significant interaction between personality of focal fish and hunger level influencing the amount of time spent in the zone nearest the bold shoal (GLM: F_1,208 = 4.81, P = 0.029; Fig. 2), mostly caused by a decrease in the

Discussion

Regardless of personality or hunger state, focal fish preferred to associate with groups of bold individuals rather than shy shoals. This result is somewhat surprising, as it suggests that matching one's own phenotype is not a major factor in choosing with which shoal to associate. On the other hand, recent work on guppies, Poecilia reticulata, by Dyer et al. (2009) found that bold shoals have higher foraging success than shy shoals, so focal fish might be trying to associate with the shoal

Acknowledgments

We are grateful to two anonymous referees for their helpful comments on the manuscript. This work was funded by a grant from the Association for the Study of Animal Behaviour to A.M. and a NERC studentship to J.H. We thank I. Goldstone for assisting with care of the fish and for building the equipment used in the experiments.

References (39)

C. Brown et al.
In situ examination of boldness-shyness traits in the tropical poeciliid, Brachyraphis episcopi
Animal Behaviour
(2005)
S.R. Evans et al.
Shoaling preferences in decapod crustacea
Animal Behaviour
(2007)
J.L. Harcourt et al.
Social feedback and the emergence of leaders and followers
Current Biology
(2009)
E.M.A. Hensor et al.
Effects of nutritional state on the shoaling tendency of banded killifish, Fundulus diaphanus, in the field
Animal Behaviour
(2003)
D.J. Hoare et al.
Context-dependent group size choice in fish
Animal Behaviour
(2004)
F.A. Huntingford
The relationship between anti-predator behaviour and aggression among conspecifics in the three-spined stickleback, Gasterosteus aculeatus
Animal Behaviour
(1976)
J. Krause et al.
The influence of nutritional state on shoal choice in zebrafish, Danio rerio
Animal Behaviour
(1999)
V.L. Pritchard et al.
Shoal choice in zebrafish, Danio rerio: the influence of shoal size and activity
Animal Behaviour
(2001)
E. Ranta et al.
Size matters when three-spined sticklebacks go to school
Animal Behaviour
(1992)
G.G. Rosenthal et al.
Assortative preferences for stripes in danios
Animal Behaviour
(2005)

C. Theodorakis

Size segregation and the effects of oddity on predation risk in minnow schools

Animal Behaviour

(1989)

M.E.M. Verbeek et al.

Consistent individual differences in early exploratory behaviour of male great tits

Animal Behaviour

(1994)

A.M. Bell

Future directions in behavioural syndromes research

Proceedings of the Royal Society of London, Series B

(2007)

B. Borg et al.

Mechanisms in the photoperiodic control of reproduction in the stickleback

Behaviour

(2004)

C. Brown et al.

Correlation between boldness and body mass in natural populations of the poeciliid Brachyrhaphis episcopi

Journal of Fish Biology

(2007)

J. Buckingham et al.

Shoaling decisions in female swordtails: how do fish gauge group size?

Behaviour

(2007)

J. Cote et al.

Social personalities influence natal dispersal in a lizard

Proceedings of the Royal Society of London, Series B

(2007)

M. Crawley

Statistical Computing: an Introduction to Data Analysis Using S-PLUS

(2002)

J.R.G. Dyer et al.

Shoal composition determines foraging success in the guppy

Behavioral Ecology

(2009)

Cited by (90)

Life-history evolution in response to foraging risk, modelled for Northeast Arctic cod (Gadus morhua)
2023, Ecological Modelling
Foraging behaviour is known to be a key element in ecology and evolution. Increased foraging intensity increases energy intake, which is useful for growth and reproduction but comes at the cost of higher mortality risk due to increased exposure to predators. Here, we investigate these trade-offs through an individual-based, mechanistic modelling framework adapted to the Northeast Arctic Cod. The model incorporates a series of life-history traits, survival trade-offs, and heritability, which allow evolution to occur and optimal strategies to emerge due to individual trait combinations and their fitness consequences. By altering the relationship between foraging intensity and mortality risk, we find that increased risk causes evolution towards lower foraging effort leading to lower growth and in turn, earlier maturation and a faster pace of life. These results build on previous studies by demonstrating behavioural evolution without direct anthropogenic stressors. Natural mortality among fish is poorly understood, and these results highlight an interesting point of further research that could help future modelling approaches make more accurate assumptions about natural mortality and its components.
Social behaviour at the beginning of life: the role of quality signals and family size
2023, Animal Behaviour
Social interactions facilitate information exchange for, among others, decision making and conflict resolution in animal societies. A central component of social interactions is the expression of signals of quality, and the role of signals can be expected to become more relevant in densely populated environments, in which social interactions are more frequent and the degree of conflict is probably stronger. We tested this hypothesis using the family context to explore whether a signal of quality expressed by the offspring modulates intrafamily interactions and whether it plays a more prominent role when the social density is increased. To this aim, we experimentally blocked a signalling trait, the ultraviolet (UV)/yellow reflectance of breast feathers and used brood size as a proxy of social density in a small passerine, the blue tit, Cyanistes caeruleus. We found that UV-blocked offspring were involved in fewer social interactions than control nestlings, suggesting that the expression of quality signals might affect the position within the family social network. Interestingly, this effect was independent of brood size. Moreover, we detected an overall preference to be in physical contact with nestmates of a different UV colour phenotype, which was stronger in small broods. Our results suggest that quality signals expressed by the offspring can influence the intrafamily social structure and that this effect is modulated by social density and, presumably, by the degree of conflict.
Familiarity, personality, and foraging performance in three-spined sticklebacks
2022, Behavioural Processes
Animals can gain large benefits from living in groups but must coordinate with their groupmates in order to do so. Social interactions between groupmates drive overall group coordination and are influenced by the characteristics of individual group members. In particular, consistent inter-individual differences in behaviour (e.g. boldness) and familiarity between individuals in groups profoundly affect the individual interactions that mediate group coordination. However, the effects of boldness and familiarity have mostly been studied in isolation. Here we describe how familiarity and boldness interact to affect individual performance, leadership, and group coordination in small shoals of three-spined sticklebacks (Gasterosteus aculeatus) solving a novel foraging task. Groups of higher average boldness were less cohesive, but only when group members were familiar with one another. Familiarity affected shy and bold individuals’ foraging performance and leadership tendencies differently depending on group characteristics: the shyest group member experienced declining foraging success and leadership with increased group boldness in familiar groups, but experienced the opposite effect on foraging and no effect on leadership in unfamiliar groups. The boldest group member, in contrast, exhibited the opposite pattern: leading and eating more with increasing group boldness in familiar groups, but eating less with increasing group boldness in unfamiliar groups. These results suggest that both boldness and familiarity are important for establishing group behaviour and coordination, and that consistent inter-individual differences in behaviour may primarily impact group coordination once familiarity has been established.
The effect of idiosyncrasy on aggregation in group-living organisms
2022, Journal of Theoretical Biology
Citation Excerpt :
Interindividual behavioural differences can also be associated with leadership (Petit and Bon, 2010; Couzin et al., 2005; Pettit et al., 2015), hierarchy (Goessmann et al., 2000; Abe et al., 2021), the influence of informed or naïve individuals on the group behaviour (Kadak and Miller, 2020) or personality/ idiosyncrasy (Aplin et al., 2014; Planas-Sitjà and Deneubourg, 2018; Michelena et al., 2010). For this latter case, it has been shown that the classical shy-bold axis affects the frequency of initiations and contributes to coordination during foraging, where bold individuals emerge as leaders and shy individuals as followers (Harcourt et al., 2009). The expression of interindividual differences occurs at many different time scales, as they may be the result from social life and from individual’s histories.
We use a minimalistic mathematical model with a limited number of parameters to evaluate the impact of interindividual differences in the collective decision-making of a group. As it turns out, in most cases, heterogeneous groups are more efficient in their decision-making than homogenous ones, especially when considering small group sizes. In reality, being different disfavours the emergence of an hysteresis and a collective threshold which are characteristics of such cooperative species while keeping inter-attractions the same between individuals. Finally, when the cooperativity becomes very large, we observe an explosion of accessible stable states.
Activity, boldness and schooling in freshwater fish are affected by river salinization
2022, Science of the Total Environment
Rivers are experiencing increasing anthropogenic pressures and salinity has shown to affect freshwater fish behaviour, potentially disrupting ecological processes. In this study, the aim was to determine the sub-lethal effects of salinization on freshwater fish behaviour, using a widespread native cyprinid species, the Iberian barbel (Luciobarbus bocagei) as the model species. Behavioural trials in a mesocosms setting were performed to assess the effects of three levels of a salinity gradient – control (no salt added to the water, 0.8 mS/cm), low (9 mS/cm), and high concentration (18 mS/cm) – on fish routine activity, shoal cohesion and boldness. Upon increasing the salinity levels in the flume-channels, fish showed a significant reduction on their i) swimming activity (76% of searching behaviour in the control vs. 57% in high salinity), and ii) shoal cohesion (0.95 shoal cohesion ratio in the control vs. 0.76 in high salinity), while iii) an increase of bolder individuals, measured by a higher number of attempts to escape the altered environment (106 total jumps in the control vs. 262 in high salinity), was simultaneously observed. Behavioural changes in fish can reflect shifts in ecological condition. Thus, the behavioural responses of fish caused by salinization stress should be further researched, in addition to the interaction with other environmental stressors, in order to understand the true scope of the consequences of salinization for fish species.
“How not to judge a deer by its cover”: A personality assessment study on captive adult red deer males (Cervus elaphus)
2021, Behavioural Processes
Personality is not a uniquely human characteristic and it has been documented in a wide range of organisms, from mammals to birds, reptiles, fish, and invertebrates. However, personality is still poorly understood in Cervids. Therefore, our study aimed to fill this gap by i) investigating personality and ii) exploring its links to dominance hierarchy, assessed by behavioral observations in 11 captive and tame male red deer (Cervus elaphus). Using questionnaires to assess personality, three trained volunteers rated these animals in 15 behaviorally composed adjectives with detailed descriptions, based on their overall impression at the end of the observation period. Behavioral data from animals were collected across three different situations, namely “feeding” (i.e., high competition for a scarce resource), “normal” (i.e., no external stimuli) in a group setting, and “handling” (i.e., stressful situation due to human manipulation) in an individual setting. We estimated dominance hierarchies between the individuals based on situations of average and high competition (i.e., “normal” and “feeding”) via the Clutton-Brock Index (CBI). Using Fleiss’ Kappa for inter-rater reliability, only five of our 15 behavioral adjectives showed acceptable reliability. Using principal component analysis, four of these adjectives formed one personality component labelled “Confidence/Aggressiveness”. We found that although “Confidence/Aggressiveness” did not correlate with CBI, ratings of two adjectives loading onto this component, namely “Confident” and “Submissive”, significantly correlated with the CBI, indicating that the questionnaire ratings reflect real behavioral variation in red deer males. Our study provides the first assessment of personality in male red deer and adds to the growing literature on Cervid personality, offering the basis for future personality research in ungulates.

View all citing articles on Scopus

View full text

Personality counts: the effect of boldness on shoal choice in three-spined sticklebacks

Section snippets

Study Organism and Equipment

Results

Discussion

Acknowledgments

Animal Behaviour

Animal Behaviour

Current Biology

Animal Behaviour

Animal Behaviour

Animal Behaviour

Animal Behaviour

Animal Behaviour

Animal Behaviour

Animal Behaviour

Animal Behaviour

Animal Behaviour

Future directions in behavioural syndromes research

Proceedings of the Royal Society of London, Series B

Mechanisms in the photoperiodic control of reproduction in the stickleback

Behaviour

Correlation between boldness and body mass in natural populations of the poeciliid Brachyrhaphis episcopi

Journal of Fish Biology

Shoaling decisions in female swordtails: how do fish gauge group size?

Behaviour

Social personalities influence natal dispersal in a lizard

Proceedings of the Royal Society of London, Series B

Statistical Computing: an Introduction to Data Analysis Using S-PLUS

Shoal composition determines foraging success in the guppy

Behavioral Ecology