Elsevier

Aquaculture

Volume 536, 15 April 2021, 736416
Aquaculture

Impact of pre-aggressive experience on behavior and physiology of black rockfish (Sebastes schlegelii)

https://doi.org/10.1016/j.aquaculture.2021.736416Get rights and content

Highlights

  • The aggressive interaction of black rockfish was characterized.

  • The aggression of black rockfish was impacted by pre-aggressive experience in a subsequent aggressive interaction.

  • Social defeat may play a role to suppress aggressive behavior in black rockfish.

Abstract

Social dominance can cause growth heterogeneity of fish in captivity, but little is known whether pre-aggressive history can change fish behavior and physiology after facing a new encounter. This study investigates the impact of the pre-aggressive experience of black rockfish (Sebastes schlegelii) on the outcome of a subsequent aggressive interaction in fish with four pre-aggression histories. After fighting with a different-sized opponent in a paired-fish arrangement, the manipulated winners demonstrated more pendulum attacks, while the manipulated losers reduced the winning rate, increased the latency period of the first attack, and had a higher level of cortisol when facing a new encounter. These results indicate that the aggression of black rockfish was impacted by pre-aggressive experience in a subsequent aggressive interaction. However, once encountered new opponents, the mirror fighters that were involved in aggressive interactions but did not experience either a victory or a defeat had similar behavioral and physiological characteristics to those in the control group. We conclude that social defeat may play a role to suppress aggressive behavior in black rockfish. Our results add to a new understanding of farmed fish aggression and could help the improvement of behavioral management in intensive fish farming.

Introduction

Aggressive behavior can cause physical damage among interactive individuals in many fish species (Blanchard et al., 2003; Singh et al., 2007). Aggressive interactions occur whenever the interests of two or more individuals conflict. The conflicts are likely in the context of competing for a limited resource such as territory, food, mates, and a nesting site (Vassos et al., 2013). In a natural population, aggressive interactions usually lead to some individuals gaining access to the limited resource via expelling and eliminating vulnerable individuals (Anholt and Mackay, 2012; Summers et al., 2005). In this case scenario, aggressive interactions are of ecological adaptation to enhance individual survival and population stabilization (Freudenberg et al., 2016; Nelson and Chiavegatto, 2000; Parker, 1974). While fish are in captivity, this ecological adaptation may significantly increase the frequency of aggressive interactions because the vulnerable fish are unlikely to avoid fighting via habitat segregation or migration, resulting in excessive aggression and growth heterogeneity (Dan et al., 2016; Guo et al., 2017; Humble and Berk, 2003). Thus, to achieve the goal of uniform growth of fish in captivity, the issue of aggressive interaction among individual fish has become critically important in managing behavior under a farming condition.

Aggressive interactions have been studied in model organisms, such as Mus musculus and Danio rerio, in the past decades, and two protocols are widely used to record behavioral performance in laboratory conditions (Gerlai, 2003; Norton and Bally-Cuif, 2010; Singh et al., 2007). Aggressive interactions of two fish in a tank can be recorded with the dyadic fight protocol (DF). Dyads of fish will compete for a limited resource (e.g., shelter, mate, and food) after a period of social isolation. The dyadic fight represents a naturalistic setting in which a fish fights with a real opponent and eventually experiences a win or a loss (Filby et al., 2010; Paull et al., 2010). The other protocol to record aggressive behavior in fish is via mirror image stimulation (MIS) (Freudenberg et al., 2016). Fish may falsely reckon their images as an intruder to attack, but there are no cues such as social status, submission behavior, strength, or exhaustion to assess the outcome of a conflict (e.g., win or loss) for fish (Oliveira et al., 2005; Rowland, 1999). Under these circumstances, several behavioral patterns of aggressive interaction have been identified in fish (Gerlai, 2003; Johnsson et al., 1996). However, little is known on the consequence of follow-up fighting among fish that had different previous histories of aggression in captivity. Therefore, it is necessary to characterize aggressive interactions before gaining a full understanding of fish interaction in a farming condition (Mitchem et al., 2019).

In the past, most studies of fish behavior have focused on the effects of aggressive interactions on the outcome of a subsequent conflict (i.e., win and lose) (Oliveira et al., 2011; Rutte et al., 2006). The winner from a conflict interaction is more likely to win again and the loser from an interaction is more likely to lose again, even against a new opponent. The winner and loser effect has been reported in shrimp Alpheus heterochaelis (Obermeier and Schmitz, 2003), crayfish Orconectes rusticus (Bergman and Moore, 2001), rainbow trout Oncorhynchus mykiss (Johnsson and Åkerman, 1998), zebrafish Danio rerio (Oliveira et al., 2011), and beetle Bolitotherus cornutus (Mitchem et al., 2019). As aggressiveness is one of the important determinants of a conflict outcome (Freudenberg et al., 2016; Larson et al., 2006), we believe that the outcome of aggressive interaction is likely to be related to a recent fighting episode in fish. Nevertheless, the sole fighting outcome may not reveal the underlying cause that provokes fighting among fish. The physiological status of a fish can be the internal driving force that initiates fighting or aggression. Some studies have shown that neurotransmitters (e.g., AVT, dopamine, and serotonin) and steroids are involved in aggression or fighting in fish (Colman et al., 2009; Filby et al., 2010). However, little is known about whether the physiological indicators associated with growth, which are of concern in farmed fish, are involved in fighting episodes in fish. Growth hormone (GH) is vital in growth regulation (Björnsson, 1997) and can promote nutrient absorption and feeding motivation (Johnsson et al., 1996; Martin-Smith et al., 2004). After a period of social interactions, similar-sized black rockfish with growth variation, and changes in GH levels were detected (Gao et al., 2017). Therefore, GH is likely to be related to a fighting episode in fish. Cortisol is a glucocorticoid hormone and has the functions of metabolic regulation and the hypothalamo-pituitary-interrenal (HPI) axis activation (Kim and Kang, 2016a, Kim and Kang, 2016b, Kim et al., 2020). Fish generally react to external threats, including social stress, via the activation of HPI axis and secretion of cortisol (Guo et al., 2017; Kim et al., 2018). Besides, the stress hormone cortisol is associated with physiological status and growth performance in fish (Gilmour et al., 2005; Gregory and Wood, 1999; Kim et al., 2019). Therefore, cortisol may be a potential indicator of stress in fish exposed to a fighting experience. Thus, we hypothesize that the levels of growth hormone and cortisol concentration are associated with aggressive interactions of fish in captivity.

The black rockfish (Sebastes schlegelii) are naturally solitary teleost fish and widely inhabit the coastal waters of Korea, China, and Japan (Kim and Kang, 2015). The black rockfish is an economically important fish species in cage-aquaculture due to its commercial value (Kim and Kang, 2016a; Kim and Kang, 2016b). The black rockfish breeds via internal fertilization and females store sperm until the fertilization of eggs (Gao et al., 2017). Interestingly, a female can be fertilized by multiple males, resulting in offspring to be released at different times. Although a female can produce up to a million eggs during a breeding season, the progeny is released at different times, resulting in size heterogeneity and cannibalism over time. In a farming situation, juvenile black rockfish show excessive variation in growth, and aggressions are frequently observed (Dan et al., 2016; Guo et al., 2017). To reduce aggression of black rockfish in aquaculture, it is crucial to understand how aggressive interactions occur and the underlying physiological mechanism that drives aggressive behavior.

The main objectives of this study are: (i) to characterize the aggressive interaction of black rockfish by developing an aggressive behavioral ethogram through behavioral manipulation; and (ii) to investigate the differences in the aggressive behavioral expression and physiological status (cortisol and GH levels) of individual fish with different aggressive experiences during a new aggressive interaction. The results of the study contribute to the understanding of black rockfish aggression and the social mechanism regulating aggression of fish in captivity to help the improvement of behavioral management in intensive fish farming.

Section snippets

Materials and methods

All procedures in this study have complied with ethical protocols (ARRIVE guidelines; EU Directive 2010/63/EU for animal experiments) approved by the Institutional Animal Care and Use Committee of the Ocean University of China.

Aggressive interaction

Nine patterns of aggressive behavior were recorded in black rockfish during aggressive interactions (Table 1, the videos have been uploaded as supplementary files). Based on this conflict resolution point (one fish starting to win the conflict and another to lose), the aggressive interactions can be separated into two phases: 1) a pre-resolution phase and 2) a post-resolution phase. The behavioral patterns in the pre-resolution phase included approach, demonstration, circling, wrestling,

Discussion

In the present study, we have characterized the aggressive interaction of black rockfish with the dyadic fight protocol. All the aggressive behaviors constituted the complex and highly structured behavioral sequences. There was a latency period of about one minute before the aggressive interaction started after an intruder was present. Fish started to attack with an extension of the fins, approaching and demonstrating to show the competitive capability to each other. The interaction intensity

Auther statement

It is submitted to be considered for publication as an original article in your journal because neither the entire paper nor any part of its content has been published or accepted elsewhere. In addition, it is not being submitted to any other journal. We declare no competing or financial interests. All authors have read the manuscript and approved the submission. All procedures in this study were complied with ethical protocols (ARRIVE guidelines; EU Directive 2010/63/EU for animal experiments)

Declaration of Competing Interest

No conflict of interest exists in the submission of this manuscript, and the manuscript is approved by all authors for publication. The work described was original research that has not been published previously, and not under consideration for publication elsewhere, in whole or in part. All the authors listed have approved the manuscript that is enclosed.

Acknowledgements

This work was supported by funds from the National Natural Science Foundation of China (32072966; 41676153),the National Key R&D Program of China(2019YFD0901303) and the Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao) (2019-ZY-B02).

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