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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.
... 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) 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.
... There are virtually no data to address the importance of sharks in deep sea and polar ecosystems (137), for smaller-bodied species, and for smaller age classes of large species in most ecosystems. Furthermore, sharks can exhibit marked and persistent individual behavioral variation within populations (41,138), resulting in considerable differences in the ecological roles and threats that individuals face. Understanding the prevalence, magnitude, and nature of individual specialization is important for understanding the importance of sharks in ecosystems and developing adequate management strategies. ...
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... In the Caribbean and adjacent waters, lemon sharks are common at several groups of islands with suitable coral reef and mangrove habitat, such as Bimini and Eleuthera, The Bahamas (Gruber 1982;Feldheim et al. 2002;Murchie et al. 2010), Atol das Rocas, Brazil , US Virgin Islands (DeAngelis et al. 2008), Turks and Caicos, British West Indies (Henderson et al. 2010), and Las Aves and Los Roques archipelagos, Venezuela (Tavares 2005;Tavares et al. 2016). Most of the knowledge about spatial ecology of lemon sharks within nursery areas has been obtained from studies conducted in Bimini (Gruber et al. 1988;Gruber 1993a, 1993b;Sundström et al. 2001;Guttridge et al. 2012;Hussey et al. 2017;Finger et al. 2018;Dhellemmes et al. 2020;Heinrich et al. 2021). Although lemon shark can be considered a well-studied species, they occupy a range of nurseries of variable size and habitat characteristics throughout their distribution. ...
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Use of a small tropical nursery in the Los Roques Archipelago by lemon sharks (Negaprion brevirostris) was investigated using acoustic telemetry. Twelve juvenile lemon sharks of three size classes were tracked between February 2014 and August 2015 in the Sebastopol Lagoon. Sharks were strongly site attached and remained in the lagoon for the duration of the study. Individuals in the smallest size class exhibited restricted movements within the innermost area of the lagoon in shallow water (< 1 m), over muddy substrate and along mangrove-lined shores. Sharks in the two larger size classes ranged further, in deeper water, over a wider range of substrates and more frequently near the lagoon entrance. Activity space varied among size classes, with home range (95% kernel utilization densities–KUD) of 0.42 km² and core area (50% KUD) of 0.13 km² for individuals in the smallest size class. For the medium and large size classes home ranges were 1.11 and 1.15 km² and core areas were 0.33 and 0.35 km² respectively. Space use as Minimum Convex Polygons differed among size classes, with overlap between the two largest size classes of 89%, compared with 40% between medium and smallest and 43% for largest and smallest size classes. Space use of lemon sharks in the Los Roques nursery illustrates variable use of habitat with varying environmental characteristics, likely reflecting a balance between predator avoidance and prey acquisition. Greater understanding of the use of nursery habitats for species such as lemon sharks, which use small, discrete nurseries over a broad geographical range can enhance our understanding of relationships between life history traits and environmental variability and management of populations.
... 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). ...
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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). ...
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