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Are some sharks more social than others? Short- and long-term consistencies in the social behavior of juvenile lemon sharks

DOI:10.1007/s00265-017-2431-0
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J. S. Finger
J. S. Finger
J. S. Finger
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Tristan L Guttridge at Saving the Blue
Tristan L Guttridge
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Alexander D M Wilson at University of Plymouth
Alexander D M Wilson
Samuel Gruber at University of Miami
Samuel Gruber
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Abstract and Figures

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.
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ORIGINAL ARTICLE
Are some sharks more social than others? Short- and long-term
consistencies in the social behavior of juvenile lemon sharks
J. S. Finger
1,2,3
&T. L. Guttridge
2
&A. D. M. Wilson
4
&S. H. Gruber
2
&J. Krause
1,3
Received: 15 June 2017 /Revised: 14 December 2017 /A ccepted: 19 December 2017 / Published online: 29 December 2017
#Springer-Verlag GmbH Germany, part of Springer Nature 2017
Abstract
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 maintenanceof animal personality and dynamics of social groups
in animals. In addition, understanding social behavior at the group- and individual-level could improve conservation manage-
ment 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 person-
ality 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 investi-
gated animal and suggest personality as an important aspect of juvenile lemon sharks’everyday life over a relatively long-term
period.
Keywords Fission-fusion .Follower .Group phenotype .Leadership .Personality .Social dynamics
Communicated by L. M. Moller
*J. S. Finger
js.finger@yahoo.fr
1
Faculty of Life Sciences, Albrecht Daniel Thaer-Institut,
Humboldt-Universität zu Berlin, Berlin, Germany
2
Bimini Biological Field Station Foundation, South Bimini, Bahamas
3
Leibniz-Institute of Freshwater Ecology and Inland Fisheries,
Berlin, Germany
4
School of Life and Environmental Sciences, University of Sydney,
Sydney, NSW 2006, Australia
Behavioral Ecology and Sociobiology (2018) 72: 17
https://doi.org/10.1007/s00265-017-2431-0
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Sharks' rate of movements was found to be repeatable, and to represent exploration personality, as sharks were found to habituate with repeated exposures to the test (Finger et al., 2016). Finger, Guttridge, Wilson, Gruber, & Krause, (2018) further developed a sociability test, where six sharks were observed for 20minutes in a 10m diameter arena (Figure 2.) and their social interactions recorded. Each shark was given a score representing its willingness to follow a conspecific (i.e. ...
... Each shark was given a score representing its willingness to follow a conspecific (i.e. sociability score), and this score was found to be repeatable (Finger et al., 2018). In both studies, the authors were able to avoid handling the sharks using t-bar anchor tags (Floy Tag & Manufacturing Inc, WA, U.S.A., Figure 3.) attached to the dorsal fins in unique colour combinations to identify individual sharks (making the scanning of PIT tags, and the associated capture unnecessary) and channels to usher sharks between the housing arenas and testing arenas (see (Finger et al., 2016) and figure 2. for details). ...
... Additionally, juvenile lemon sharks from these subpopulations have been subject to a yearly mark-recapture programme providing us with long-term subpopulation demographic estimates that can be used as proxies for intraspecific competition . Finally, juvenile lemon sharks in our study site have been studied for personality since 2012, and their behaviour is repeatable in two separate behavioural assays (novel open-field assay (Finger et al., 2016) and sociability assay (Finger et al., 2018)). Here, we took advantage of this long-term personality data set to test (1) how stable behavioural syndromes (measured as phenotypic correlations) are across time and subpopulation. ...
What did we learn from six years of shark personality research?
Conference Paper
  • Oct 2022
In behavioural ecology, interest in the study of animal personality (i.e. consistent individual differences in behaviour) has increased in the last two decades as it is believed to have important ecological and evolutionary consequences. These consequences are especially pronounced when personality covaries with other behaviours (i.e. behavioural syndrome) or with life-history (i.e. pace-of-life syndrome). So far, studies of personality on behavioural, and pace-of-life-syndromes have produced ambiguous outcomes, and the prominence of studies on captive animals in the literature may be a reason for inconclusive results. To address this knowledge gap, we tested personality in wild juvenile lemon shark (Negaprion brevirostris) from 2012 to 2018 to investigate the emergence of behavioural and pace-of-life-syndromes under relevant ecological pressures. We first explored how to quantify meaningful personality traits in our study species. We then investigated (1) whether a behavioural syndrome existed between two consistent traits and whether the appearance of the syndrome was context dependent, (2) whether a growth-mortality trade-off was mediated by personality and (3) whether personality could predict the foraging habitat of sharks and whether this link was context-dependent. Overall, our research suggest that ecological conditions play a crucial role in the emergence and the shaping of personality and trait association. This work offers a possible explanation for the ambiguous results of previous studies and highlights the importance of increasing the focus on wild study systems in future animal personality research. Along with recent revisions of the personality research framework, this work may help paving the way for future shark-personality research.
View
... Sharks' rate of movements was found to be repeatable, and to represent exploration personality, as sharks were found to habituate with repeated exposures to the test (Finger et al., 2016). Finger, Guttridge, Wilson, Gruber, & Krause, (2018) further developed a sociability test, where six sharks were observed for 20minutes in a 10m diameter arena (Figure 2.) and their social interactions recorded. Each shark was given a score representing its willingness to follow a conspecific (i.e. ...
... Each shark was given a score representing its willingness to follow a conspecific (i.e. sociability score), and this score was found to be repeatable (Finger et al., 2018). In both studies, the authors were able to avoid handling the sharks using t-bar anchor tags (Floy Tag & Manufacturing Inc, WA, U.S.A., Figure 3.) attached to the dorsal fins in unique colour combinations to identify individual sharks (making the scanning of PIT tags, and the associated capture unnecessary) and channels to usher sharks between the housing arenas and testing arenas (see (Finger et al., 2016) and figure 2. for details). ...
... Additionally, juvenile lemon sharks from these subpopulations have been subject to a yearly mark-recapture programme providing us with long-term subpopulation demographic estimates that can be used as proxies for intraspecific competition . Finally, juvenile lemon sharks in our study site have been studied for personality since 2012, and their behaviour is repeatable in two separate behavioural assays (novel open-field assay (Finger et al., 2016) and sociability assay (Finger et al., 2018)). Here, we took advantage of this long-term personality data set to test (1) how stable behavioural syndromes (measured as phenotypic correlations) are across time and subpopulation. ...
Ecological consequences of personality in sharks
Thesis
  • Dec 2021
In behavioural ecology, interest in the study of animal personality (i.e. consistent individual differences in behaviour across time and/or context) has increased in the last two decades as it is believed to have important ecological and evolutionary consequences. These consequences are especially pronounced when a behaviour that is consistent covaries with other consistent behaviours (i.e. behavioural syndrome) or with life-history traits (i.e. pace-of-life syndrome). So far, studies of behavioural and pace-of-life-syndromes have produced ambiguous outcomes (e.g. hypotheses are sometimes verified and others not), and the prominence of studies on captive animals (i.e. as opposed to wild animals) in the literature may be a reason for inconclusive results as trait covariation has been hypothesized to be environmentally driven. To address this knowledge gap, I investigated the emergence of behavioural and pace-of-life-syndromes in a wild population of juvenile sharks subject to relevant ecological pressures (e.g. predation risk, inter-individual competition). I explored (1) whether a behavioural syndrome existed between two consistent traits (exploration and sociability) and whether the appearance of the syndrome was context dependent, (2) whether a growth-mortality trade-off was mediated by exploration personality and (3) whether personality could predict the foraging habitat of sharks and whether this link was context-dependent. First, I observed a behavioural syndrome between sociability and exploration personality which was inconsistent across years and locations and was dependent on inter-individual competition. Then, I found the association between exploration personality and a growth-mortality trade-off to only be observable in low predation risk. Similarly, I found that exploration personality only predicted wild foraging habitat when predation risk was low. Overall, these results suggest that ecological conditions play a crucial role in the emergence and the shaping of personality and trait association. This thesis offers a possible explanation for the ambiguous results of previous studies and highlights the importance of increasing the focus on wild study systems that are subject to relevant ecological pressures in future animal personality research.
View
... Our finding that gregariousness was variable between individuals, and consistent within individuals across years, is consistent with the wider pattern shown by many other species, namely that behavioural patterns such as social network positions remain stable across the lifespan (Aplin, Firth, et al., 2015;Blaszczyk, 2017;Finger et al., 2017;Jacoby et al., 2014;Wuerz & Krüger, 2015). ...
Automated face recognition using deep neural networks produces robust primate social networks and sociality measures
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Full-text available
Longitudinal video archives of behaviour are crucial for examining how sociality shifts over the lifespan in wild animals. New approaches adopting computer vision technology hold serious potential to capture interactions and associations between individuals in video at large scale; however, such approaches need a priori validation, as methods of sampling and defining edges for social networks can substantially impact results. Here, we apply a deep learning face recognition model to generate association networks of wild chimpanzees using 17 years of a video archive from Bossou, Guinea. Using 7 million detections from 100 h of video footage, we examined how varying the size of fixed temporal windows (i.e. aggregation rates) for defining edges impact individual‐level gregariousness scores. The highest and lowest aggregation rates produced divergent values, indicating that different rates of aggregation capture different association patterns. To avoid any potential bias from false positives and negatives from automated detection, an intermediate aggregation rate should be used to reduce error across multiple variables. Individual‐level network‐derived traits were highly repeatable, indicating strong inter‐individual variation in association patterns across years and highlighting the reliability of the method to capture consistent individual‐level patterns of sociality over time. We found no reliable effects of age and sex on social behaviour and despite a significant drop in population size over the study period, individual estimates of gregariousness remained stable over time. We believe that our automated framework will be of broad utility to ethology and conservation, enabling the investigation of animal social behaviour from video footage at large scale, low cost and high reproducibility. We explore the implications of our findings for understanding variation in sociality patterns in wild ape populations. Furthermore, we examine the trade‐offs involved in using face recognition technology to generate social networks and sociality measures. Finally, we outline the steps for the broader deployment of this technology for analysis of large‐scale datasets in ecology and evolution.
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... Like social birds and mammals, elasmobranchs maintain social preferences between individuals (Guttridge et al., 2009;Perryman et al., 2019), and their social interactions can have adaptive functions (e.g. in learning or information transfer; Guttridge et al., 2011;Keller et al., 2017;Vila Pouca et al., 2020;Papastamatiou et al., 2020) that contribute to emergent population structuring (Mourier & Planes, 2021;Papastamatiou et al., 2020). Sharks are known to have highly variable behavioural phenotypes relating to exploration and movement, sufficient to comprise individual personalities (Jacoby et al., 2014;Byrnes & Brown, 2016;Finger et al., 2017Finger et al., , 2018. Differences in movement behaviour and sociability are often linked and may covary in the form of a behavioural syndrome (Burns, 2016). ...
Reef manta ray social dynamics depend on individual differences in behaviour
Article
Knowledge of the drivers of fine-scale spatial ecology in wide-ranging marine species is vital to understand population structuring and conserve threatened species. Movements and habitat use are likely to be strongly influenced by social relationships between individuals, and social units within animal populations may be subject to distinct selective pressures. Here we used passive acoustic telemetry and network-based analyses to investigate the site visit patterns and social affiliations of reef manta rays, Mobula alfredi, in Raja Ampat, West Papua. Acoustic transmitters were externally deployed on 27 rays that were tracked for up to 110 days. Visit profiles were retrieved from nine acoustic receivers positioned in clusters at known aggregation sites, enabling analysis of movement behaviour and social processes at various spatial scales. We utilized Bayesian inference and a double permutation method to address issues in sampling and hypothesis testing on social networks constructed from automated telemetry data. We found that social affiliations were assorted into spatially defined communities which remained stable over several weeks to months, although many affiliations were short lived. Interindividual variability in detection profiles was correlated with social network metrics. Individuals with high levels of site attachment had stronger social affiliations, while individuals that regularly attended different receiver clusters were more central to the overall social network. These results suggest that reef manta ray movements, habitat preferences and social relationships should be understood as linked behavioural processes for which variability between individuals and groups may drive emergent population structure. Future research and local management of manta rays will likely benefit from identifying how, where and why social gatherings occur.
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... However, a growing number of studies have demonstrated that some elasmobranch species could form social communities characterized by non-random and long-term associations, despite opportunities for social relationships to develop between different communities (Mourier et al. 2012, Perryman et al. 2019. The reasons for such social structures in sharks are not yet completely clear, but familiarity (Keller et al. 2017), phenotypic assortment (Mourier et al. 2012;Perryman et al. 2019), foraging efficiency (Labourgade et al. 2020, dominance hierarchy (Brena et al., 2018), leadership , personality, and individuality (Jacoby et al. 2014;Finger et al. 2018) are all aspects of sociality observed in elasmobranchs, although kinship has not been found to drive social behavior . Even large, solitary sharks that are characterized by cross-national boundary movements have been shown to non-randomly aggregate at specific areas (Schilds et al. 2019). ...
Preliminary insights of a mixed-species shark aggregation: a case study of two carcharhinids from the Mediterranean Sea
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Full-text available
Social and non-social animals can aggregate at a specific site for various reasons such as reproduction, feeding, or other synchronized patterns of movements. While shark aggregations are well documented, mixed-species aggregations are less studied and therefore poorly understood. To overcome this, a combination of acoustic telemetry and social network analysis was used to investigate population structure and behavior based on the temporal overlap of 22 individuals of 57 tagged sharks of two species, the sandbar (Carcharhinus plumbeus) and the dusky (Carcharhinus obscurus) sharks, that form a winter mixed-species aggregation in front of an Israeli coastal power plant. The results suggested that if both species co-occurred and share the study site, their finer-scale associations revealed temporal partitioning between species and species assortment in sandbar sharks. The multi-species network was also structured by sex. The difference between species may indicate separate strategies and temporal niche partitioning at the aggregation site. The particularly warmer temperatures (~ 5–10 °C warmer) caused by the electric power plant suggest that female dusky sharks follow the thermal niche–fecundity hypothesis by selecting warmer waters to optimize gestation, while male sandbar sharks socialize at the site. This study represents the first attempt to examine the fine-scale structure of a mixed-species aggregation of sharks and provides new insights into the shark’s social structures through tolerance of each other and social-niche partitioning in this mixed-species aggregation.
View
... For example, Jacoby and colleagues [92] summarized some research studies on social behaviors in different shark species, e.g. group foraging and social facilitation (Sevengill Shark, Notorynchus cepedianus) or social organization (Lemon Shark, Negaprion brevirostris), aside from their well-known reproductive aggregations. Guttridge and colleagues [93] found Lemon Sharks to be able to use socially derived information to learn about novel features in their environment. In a more recent study, Finger and colleagues [94] found that juvenile Lemon Sharks showed social behaviors, such as following and paralleling partners, with consistent individual differences. ...
Social representations of sharks, perceived communality, and attitudinal and behavioral tendencies towards their conservation: An exploratory sequential mixed approach
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Sharks are crucial to the marine ecosystem, but they are critically declining. Their bad public image explains, to some extent, the lesser concern for their conservation compared to other marine species. Extending previous research which has mainly focused on the study of attitudes towards sharks, we propose a two studies sequence, first by exploring the shark’s social representation, followed by an exploration of some stereotypical traits that may affect attitudes toward shark conservation. Study 1 specifically exploreed the social representation of sharks in a sample of zoo goers (N = 979). Main results showed that the representation was ambivalent and participants considered sharks as human predators. Surprisingly, findings showed that sharks were also seen as highly agentic and little communal animals. Consequently, Study 2 (N = 60) was designed to more thoroughly explore this gendered view as well as its implications in the attitudes and behavioral intention towards shark conservation. Results showed that, although sharks were again perceived as highly agentic, it was the perception of the sharks’ communality that was associated with more positive attitudes towards their conservation and a higher tendency to choose a shark conservation trust as first choice. Implications of studies 1 and 2 results for sharks’ conservation communication strategies and policies are discussed.
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Personality differences are widespread throughout the animal kingdom and can have important ecological and evolutionary consequences. Despite a rapidly increasing body of literature, large (marine) vertebrates remain underrepresented in personality research. Given their unique life history traits (e.g. slow growth rate, slow reproduction rate, long life span) and their pivotal role in ecosystem processes, this is an important gap in our current knowledge. Here we investigated consistency and plasticity in movement behaviour of wild juvenile lemon sharks, Negaprion brevirostris, by repeatedly subjecting sharks to open field tests. First, we investigated the presence of interindividual differences in movement behaviour in a novel open field. Second, we investigated the effect of trial repetition on movement behaviour to understand whether movement in a novel open field reflects a reaction to novelty, or general activity. Third, we estimated individual differences in habituation/sensitization rates over trial repetition and studied how the habituation rate was predicted by the initial movement rate. We found consistent individual differences in movement behaviour during the open field tests. Sharks showed habituation in movement behaviour (i.e. decrease) over repeated trials indicating that the movement behaviour during the first trials is a reaction to novelty, and not general activity. Individuals, however, differed in their rate of habituation (i.e. plasticity) and this rate was negatively related to an individual's movement behaviour in the first open field trial. In addition to showing individual differences in consistency and plasticity in juvenile lemon sharks, our study emphasizes the importance of examining the validity of personality tests when adapting them to new species.
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Personality in Elasmobranchs with a Focus on Sharks: Early Evidence, Challenges, and Future Directions
Chapter
  • Jul 2017
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.
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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.
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