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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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J. S. Finger
J. S. Finger
J. S. Finger
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Tristan L Guttridge at Saving the Blue
Tristan L Guttridge
  • Saving the Blue
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.
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... 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 ecosystems, sharks can be predators, competitors, facilitators, nutrient transporters, and food. However, overfishing and other threats have greatly reduced shark populations, altering their roles and effects on ecosystems. We review these changes and implications for ecosystem function and management. Macropredatory sharks are often disproportionately affected by humans but can influence prey and coastal ecosystems, including facilitating carbon sequestration. Like terrestrial predators, sharks may be crucial to ecosystem functioning under climate change. However, large ecosystem effects of sharks are not ubiquitous. Increasing human uses of oceans are changing shark roles, necessitating management consideration. Rebuilding key populations and incorporating shark ecological roles, including less obvious ones, into management efforts are critical for retaining sharks’ functional value. Coupled social-ecological frameworks can facilitate these efforts.
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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. ...
Movements and habitat use of a nursery area by a widely distributed species of shark in the Southern Caribbean
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  • May 2024
  • MAR BIOL
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.
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... 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). ...
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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.
View
... 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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