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

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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 sharkseveryday 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.
... Consistent individual differences in social behaviour, whether measured as spatial association patterns or rates of direct physical interactions such as grooming and aggression, have been identified across various animal taxa [1][2][3][4][5][6][7][8]. Repeatability, the statistical metric by which such stable differences are quantified, is defined as the proportion of variation in trait expression attributable to between-individual differences relative to the overall variation in trait expression [9]. ...
... The repeatability of social behaviour has been well explored in relatively short-lived species, both in the wild [1,4,5,7] and in more controlled captive settings [6,8]. In such studies, the comparatively short lifespans of the study species allow for monitoring the stability of social tendencies across different socioecological settings, such as across breeding seasons [1], different life-history stages [8], or even across generations [5]. ...
... In such studies, the comparatively short lifespans of the study species allow for monitoring the stability of social tendencies across different socioecological settings, such as across breeding seasons [1], different life-history stages [8], or even across generations [5]. However, quantifying social tendencies in these animals is often limited to quantifying patterns of spatial association [1,4,6,7], either due to the practical challenges of monitoring directed social interactions, or due to such social behaviour being comparatively rare in a species. While studies of patterns of association are clearly important for understanding the evolution of social phenotypes, for many species, navigating the social environment requires a diverse range of affiliative and agonistic behaviours. ...
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... 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. ...
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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.
... 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). ...
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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.
... 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. ...
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... Matich and Heithaus (2015) suggested that intraspecific variation in the habitat use of juvenile bull sharks could be caused by intrinsic factors such as habitat-use preferences, foraging strategies or even personalities. Although there has been limited research on personality in sharks (Jacoby et al. 2014;Byrnes and Brown 2016), variation in personality traits could drive variation in the residency, habitat use, movement patterns and social behaviour of individuals (Finger et al. 2016;Finger et al. 2018;Dhellemmes et al. 2020). In other taxa, personality traits, such as aggression and boldness, have been shown to drive intraspecific variation in the foraging behaviour, intraspecific niche variation, habitat preferences, home range utilisation and dispersal in individuals (Bergmüller and Taborsky 2010;Cote et al. 2010;Brown and Irving 2014;Spiegel et al. 2017). ...
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... Researchers have identified several important axes of animal personality in which individuals can be placed in a wide range of organisms, from mammals to birds, reptiles, fish and invertebrates (Gosling, 2001;Carere and Maestripieri, 2013). These axes are usually labelled shynessboldness, explorationavoidance, aggressiveness, activity, sociability and proactivereactive stress coping styles (Bergmuller and Taborsky, 2010;Finger et al., 2018;Koolhaas et al., 1999;Réale et al., 2007). Some of these axes, such as boldness-shyness (Dahlbom et al., 2011), aggressiveness (Drent et al., 1996;Rodriguez-Santiago et al., 2020) and exploration-avoidance (Verbeek et al., 1999), have been associated with a higher position in the hierarchy or with changes in the dominance status (Rudin et al., 2016). ...
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... Those differences are also present on shorter time scales in wild guppies Poecilia reticulata (Krause et al. 2017). What is more, this consistent between-individual variation has been shown to be maintained in different habitats including field and laboratory in vampire bats Desmodus rotundus (Ripperger et al., 2019), or across social environments in captive sharks like the small-spotted catshark Scyliorhinus canicula (Jacoby et al. 2014), the lemon shark Negaprion brevirostris (Finger et al. 2018), and in captive forked fungus beetles like Bolitotherus cornutus (Formica et al. 2017) and wild Emei music frogs Babina daunchina (Deng & Cui 2019). Yet, it remains unclear, and if so, in which circumstances, those patterns in behaviors measured in captivity can be translated into the wild within the same species (Bell et al., 2009, Osborn & Briffa 2017, Herborn et al., 2010. ...
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... Sharks were then individually subjected to the novel open-field assay. Data on sociability is not presented here as the sample size was significantly lower than on the novel open-field assay due to difficulties with the observations (but see Finger et al. (2018) for repeatability of Sociability). The sociability and exploration tests could not be conducted on separate TA B L E 1 Overview of sample sizes. ...
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Chapter
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.