Balancing the competing requirements of air-breathing and display behaviour during male–male interactions in Siamese fighting fish Betta splendens

Abstract

Air-breathing fish of the Anabantoidei group meet their metabolic requirements for oxygen through both aerial and aquatic gas exchange. Siamese fighting fish Betta splendens are anabantoids that frequently engage in aggressive male–male interactions which cause significant increases in metabolic rate and oxygen requirements. These interactions involve opercular flaring behaviour that is thought to limit aquatic oxygen uptake, and combines with the increase in metabolic rate to cause an increase in air-breathing behaviour. Air-breathing events interrupt display behaviour and increase risk of predation, raising the question of how Siamese fighting fish manage their oxygen requirements during agonistic encounters. Using open-flow respirometry, we measured rate of oxygen consumption in displaying fish to determine if males increase oxygen uptake per breath to minimise visits to the surface, or increase their reliance on aquatic oxygen uptake. We found that the increased oxygen requirements of Siamese fighting fish during display behaviour were met by increased oxygen uptake from the air with no significant changes in aquatic oxygen uptake. The increased aerial oxygen uptake was achieved almost entirely by an increase in air-breathing frequency. We conclude that limitations imposed by the reduced gill surface area of air-breathing fish restrict the ability of Siamese fighting fish to increase aquatic uptake, and limitations of the air-breathing organ of anabantoids largely restrict their capacity to increase oxygen uptake per breath. The resulting need to increase surfacing frequency during metabolically demanding agonistic encounters has presumably contributed to the evolution of the stereotyped surfacing behaviour seen during male–male interactions, during which one of the fish will lead the other to the surface, and each will take a breath of air.

Introduction

Animals use display behaviour for many different purposes, including courtship and territory defence. These display behaviours are influenced by physiological indicators of fitness, and are necessary for beneficial rewards such as access to territory, resources and mates. Animals exhibiting such display behaviours must balance the time spent displaying against time spent foraging and their own energetic requirements. Siamese fighting fish Betta splendens are a facultatively air-breathing freshwater fish belonging to the Anabantoidei group (Graham, 1997, Mendez Sanchez and Burggren, 2012), possessing an air breathing labyrinth organ that enables them to obtain oxygen from the air to supplement aquatic oxygen uptake via the gills and skin (Peters, 1978). During both aggressive territorial encounters and courtship displays, male Siamese fighting fish engage in fin and opercular flare behaviour (Simpson, 1968). Such displays are intense, causing significant changes in muscle metabolites (Haller, 1991a, Haller, 1991b) and resulting in significantly increased rates of oxygen uptake (Castro et al., 2006). The extent to which display behaviour is supported by anaerobic metabolism has not been determined, but Haller (1992) suggests that glycolysis is the major energy source during aggressive behaviour in Siamese fighting fish, and the observation that rates of oxygen uptake remain elevated following an agonistic encounter (Castro et al., 2006) supports the view that anaerobic metabolism is likely to be important. Indeed, opercular flaring is also hypothesised to decrease gill ventilation because it inhibits action of the opercular pump (Abrahams et al., 2005), which acts to move water over the gills (Hughes and Shelton, 1958, Hughes, 1960). Thus, while holding the opercular spread during agonistic encounters, Siamese fighting fish are unable to rise to the surface to breathe air, and are unable to effectively exchange respiratory gases with water (Abrahams et al., 2005).

The duration of opercular flare displays is a significant predictor of success in agonistic encounters (Evans, 1985), rather than morphological features such as fin size (Allen and Nicoletto, 1997). Moreover, exposure to hypoxia causes individuals to reduce opercular displays (Abrahams et al., 2005), suggesting that opercular displays are a reliable signal of body condition. Individuals in better physical condition are physiologically more able to cope with the reduction in respiratory gas exchange that occurs during opercular flaring, and thus are able to continue to display more vigorously, for longer periods of time, under challenging conditions.

During fights, air breathing frequency is positively correlated with the frequency and duration of opercular flaring and with tail beating (Dore et al., 1978, Meliska et al., 1980). This suggests that these activities increase metabolic rate or compromise aquatic gas exchange, or both, thereby necessitating an increased reliance on aerial gas exchange to support aerobic metabolism. Given that opercular display rate is a significant predictor of success in male–male interactions (Simpson, 1968, Evans, 1985), and that air breathing during an agonistic encounter could potentially compromise display behaviour, it seems reasonable to suggest that individuals would benefit from minimising the time engaged in air-breathing behaviour in order to maximise the time engaged in display behaviour. However, empirical data are lacking for males during fights where gas exchange and air breathing behaviour are measured simultaneously. Therefore, through continuous measuring of aerial and aquatic gas exchange during male–male interactions, we tested two non-exclusive hypotheses for how male Siamese fighting fish balance the need for metabolically demanding aggressive displaying against the need to obtain oxygen from air and water: (1) during display behaviour, Siamese fighting fish will increase the their oxygen uptake per breath relative to routine activity in order to minimise the time engaged in air-breathing behaviour, or (2) during display behaviour, Siamese fighting fish will increase their reliance on aquatic oxygen uptake, in order to minimise air-breathing behaviour.