Boldness, activity, and aggression: Insights from a large-scale study in Baltic salmon (Salmo salar L)

PLOS ONE RESEARCH ARTICLE Boldness, activity, and aggression: Insights from a large-scale study in Baltic salmon (Salmo salar L) Johanna Axling1,2, Laura E. Vossen3, Erik Peterson4, Svante Winberg ID1,2,3* 1 Behavioural Neuroendocrinology, Department of Medical Cell Biology, Uppsala University, Uppsala, Sweden, 2 Behavioural Neuroendocrinology, Department of Neuroscience, Uppsala University, Uppsala, Sweden, 3 Division of Anatomy and Physiology, Department of Anatomy, Physiology and Biochemistry, Swedish University of Agricultural Sciences, Uppsala, Sweden, 4 Department of Aquatic Resources, Swedish University of Agriculture, Uppsala, Sweden a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Axling J, Vossen LE, Peterson E, Winberg S (2023) Boldness, activity, and aggression: Insights from a large-scale study in Baltic salmon (Salmo salar L). PLoS ONE 18(7): e0287836. https://doi.org/10.1371/journal.pone.0287836 Editor: Pierluigi Carbonara, COISPA Tecnologia & Ricerca - Stazione Sperimentale per lo Studio delle Risorse del Mare, ITALY Received: June 10, 2022 Accepted: June 14, 2023 Published: July 20, 2023 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0287836 Copyright: © 2023 Axling et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. * Abstract Atlantic salmon (Salmo salar) display high levels of agonistic behavior in aquaculture farms, resulting in fin damage and chronic stress. Aggression affects fish growth and performance negatively, and presents a serious welfare problem. Indeed, it would be beneficial to identify, separate or exclude overly aggressive individuals. Research on behavioral syndromes suggests that aggressive behavior may correlate with other behavioral traits, such as boldness and locomotory activity. We aimed to develop a high-throughput method to quantify and predict aggressive behavior of individual parr in hatchery-reared Baltic salmon (Salmo salar L.). We screened approximately 2000 parr in open field (OF) and mirror image stimulation (MIS) tests. We extracted seven variables from video tracking software for each minute of the tests; distance moved and duration moving (activity), the duration in and number of entries to the center of the arena (boldness), the distance moved in and duration spent in the area adjacent to the mirror during the MIS test (aggressiveness) and head direction (lateralization). To investigate the relationship between activity, boldness and aggression we first correlated the first six variables to one another. Second, we assigned individuals to high, medium, low or zero aggression groups based on the MIS test and quantified activity and boldness in each group. Third, we analyzed whether the fish viewed the mirror with the left or right eye. Our results show that medium and low aggressive fish were the most active, while highly aggressive fish showed average activity. Aggressive groups did not differ in boldness. Activity and boldness were positively correlated. Finally, we detected a preference for fish to view the mirror with the left eye. We conclude that aggressiveness cannot be predicted from the results of the OF test alone but that the MIS test can be used for largescale individual aggression profiling of juvenile salmon. Data Availability Statement: Data has been uploaded to https://figshare.com/; DOI 10.6084/ m9.figshare.23611272. PLOS ONE | https://doi.org/10.1371/journal.pone.0287836 July 20, 2023 1 / 20 PLOS ONE Funding: Formas (ANIHWA 2014-01842 to SW) website: https://formas.se/en/start-page.html The Swedish Research Council (VR 2017-03779 to SW) website: https://www.vr.se/english.html FACIAS foundation (to SW and JA) website:https:// stiftelsemedel.se/stiftelsen-facias/ The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Boldness, activity and aggression in Baltic salmon Introduction The health and welfare of fish in aquaculture systems is of growing concern to consumers [1, 2]. In aquatic species such as fish, health and welfare are tightly linked to water quality, stocking density and disease control [3, 4]. In addition, aggression between individuals is a major cause of stress and fin damage [5], which often leads to bacterial or fungal infections commonly seen in hatcheries [6]. Considering that teleost fish possess nociceptors and show withdrawal from potentially painful stimuli [7], it is likely that fish perceive fin damage as painful, which raises ethical concerns. Furthermore, secondary effects of fin damage on fish health may comprise production efficiency, quality and quantity [8]. Atlantic salmon (Salmo salar L) is an important aquaculture species [9] which shows high levels of aggression in hatcheries. In Sweden and Norway, Baltic populations of Atlantic salmon are also bred in hatcheries to compensate for loss of access to their natural spawning areas due to hydroelectric power plants [10]. During the freshwater phase juvenile salmon are territorial and the level of agonistic behavior is high [6, 11–13]. These agonistic responses can include indirect interaction such as displays, color changes, threatening postures as well as overt aggressive acts, such as chasing and biting [9, 14, 15]. There is evidence that the aggressive display of salmon is lateralized. Fish may view their opponent with a particular eye, although both a right eye and left eye bias have been reported [16]. Displays, both lateral and frontal [17, 18] are aggressive signals that challenge and reinforce dominance without direct physical interactions. During an initial encounter with a conspecific, the fish may switch back and forth between direct attack (overt aggression) and display (passive aggression) [19] before a stable dominance hierarchy is established. Subordinate fish tend to show a stress-induced behavioral inhibition [20] and if possible will try to escape [21, 22]. It has becoming increasingly clear that salmonids and other teleosts display intraspecific divergence in behavioral and physiological responses to challenge [23]. Behavioral responses is often described as personalities, which include boldness, exploration, activity, aggression, and sociability [24]. Physiological responses are often called stress coping and includes physiological traits, such as sympathetic reactivity and post-stress plasma cortisol [25]. Animals displaying a proactive coping style (...truncated)