Chapter 6 The Effect of Hypoxia on Fish Swimming Performance and Behaviour P. Domenici, N. A. Herbert, C. Lefrançois, J. F. Steffensen and D. J. McKenzie Abstract Oxygen depletion, hypoxia, can be a common stressor in aquatic hab- itats, including aquaculture. Hypoxia limits aerobic swimming performance in fish, by limiting their aerobic metabolic scope. Hypoxia also elicits changes in spon- taneous swimming activity, typically causing a decrease in swimming speed in sedentary species and an increase in active species. However, fish do have the capacity to avoid hypoxia and actively choose well-oxygenated areas. Hypoxia causes differences in fish behaviour in schools, it may reduce school density and size and influence activities such as shuffling within schools. Hypoxia also influ- ences predator–prey interactions, in particular by reducing fast-start performance. Thus, through effects on swimming, hypoxia can have profound effects on species distributions in the field. In aquaculture, effects of hypoxia may be particularly significant in sea cages. It is therefore important to understand the nature and thresholds of effects of hypoxia on swimming activity to extrapolate to potential impacts on fish in aquaculture. P. Domenici (&) CNR-IAMC Loc. Sa Mardini, Torregrande, Oristano, Italy e-mail: [email protected] N. A. Herbert Leigh Marine Laboratory, University of Auckland, PO Box 349, Warkworth 0941, New Zealand C. Lefrançois UMR 6250 LIENSS (CNRS-University of La Rochelle), 2 rue Olympe de Gouges, 17000 La Rochelle, France J. F. Steffensen Marine Biological Laboratory, Biological Institute, University of Copenhagen, Strandpromenaden 5, 3000 Helsingør, Denmark D. J. McKenzie UMR 5119 Ecologie des Systèmes Marins Côtiers, Université Montpellier II, Place Eugène Bataillon cc 093, Montpellier cedex 5, 34095 Montpellier, France A. P. Palstra and J. V. Planas (eds.), Swimming Physiology of Fish, 129 DOI: 10.1007/978-3-642-31049-2_6, Ó Springer-Verlag Berlin Heidelberg 2013 130 P. Domenici et al. 6.1 Introduction Water has a low capacitance for oxygen, air-saturated water only contains a few milligrams per litre of oxygen at normal atmospheric pressures. As a result, oxygen levels can be depleted quite easily by respiring organisms, especially in nutrient- rich environments with a large microbial biomass, or stagnant areas with poor vertical mixing. Oxygen depletion, hypoxia, is therefore a natural phenomenon. As such, fish have evolved to cope with hypoxia, although their relative tolerance depends on the species, its habitat and lifestyle. Hypoxia may occur over a variety of timescales, defined by Kemp et al. (2009) as (1) permanent, (2) persistent seasonal, both stratified and vertically mixed, (3) episodic and (4) diel. Hypoxia is also a common symptom of degraded water quality caused by nutrient pollution and eutrophication. Over the last few decades, eutrophication of coastal waters has been linked to increases in the frequency, duration and geographical extent of hypoxic events, which are recognised as important environmental problems globally (Diaz and Rosenberg 2008). Hypoxic events have the potential to significantly impact coastal fisheries (Diaz 2001). Shifts in spatial distribution and the structure of benthic and nekton assemblages can occur through direct mortality during extreme local events, especially of sluggish species, and through sublethal effects such as increased emigration of vagile species. Additionally, fish exposed to hypoxic conditions grow slower and produce fewer viable offspring (Petersen 1987; Plante et al. 1998; Dean and Richardson 1999; Smith and Able 2003; Taylor and Miller 2001). Changes in assemblage structure and loss of habitat can have bottom-up effects on food web structure such as losses in key prey species resulting in further ecological effects (Diaz 2001). Hypoxia may have profound effects on production efficiency of fish in culture, through its depressive effects on growth. Species differ greatly in their relative tolerance of hypoxia, as a function of the environment in which they have evolved. Thus, cyprinids that have evolved in slow-moving or static and warm waters, where hypoxia can develop, are known to be more tolerant of oxygen depletion than salmonids, which rarely encounter any hypoxia in their cool fast-flowing habitats. Oxygen levels are generally carefully monitored and controlled in modern commercial finfish aquaculture, except for some air-breathing species in south-east Asia (Lefevre et al. 2011). Hypoxia can, however, develop in sea cage aquaculture through oceanographic and eutrophic forces. Little is known about how it influences the behaviour of cultured fish (Oppedal et al. 2011). The current review therefore provides an opportunity to extrapolate what we know about how hypoxia affects fish swimming performance and behaviour to culture scenarios. The impact of hypoxia on aquatic ecosystems is modulated by the physiology and behaviour of the organisms (Kramer et al. 1997;Domenicietal.2007a, b;Chapman and McKenzie 2009). Knowledge of the processes that regulate the interactions between hypoxia and ecologically relevant variables, such as growth and survival, is fundamental for understanding and predicting the effects of such interactions, par- ticularly on fish in aquaculture. A number of physiological and behavioural effects are 6 The Effect of Hypoxia 131 observed at sublethal levels of hypoxia, which presumably mediate subsequent effects on fish activity and distribution (Domenici et al. 2007a, b; Chapman and McKenzie 2009). Fish can sense oxygen levels in the ventilatory water stream and in their blood and, when oxygen levels in these milieux decline, they engage a suite of physi- ological responses which, together, aim to improve oxygen uptake at the gills, transport in the blood and release at the tissues (Randall 1982; Burleson et al. 1992; Richards 2009). Nonetheless, the reduced oxygen availability in hypoxia limits the ability of fish to provide oxygen for metabolic activities, their aerobic metabolic scope (MS; Fry 1947, 1971; Claireaux et al. 2007). The effects of hypoxia on aerobic metabolism, and MS, can be modelled as shown in Fig. 6.1. The standard metabolic rate (SMR) is the minimal rate of oxygen uptake required to support essential maintenance functions in ectotherms. In hypoxia, fish can typically use physiological responses to maintain oxygen uptake at or above SMR down until a critical dissolved oxygen (DO) threshold, termed critical O2 partial pressure (Pcrit) or saturation (Scrit). Below this critical threshold, the fish is no longer able to support maintenance metabolism and its metabolic rate is dependent on the oxygen level in its external O2 environment (Fig. 6.1, Schurmann and Steffensen 1997). Whilst SMR provides for essential core function, all other activities such as growth, reproduction and swimming activities (the focus of this review), depend on an ability to increase oxygen uptake and delivery above and beyond SMR, and within the limits of aerobic metabolic scope (MS). MS was first defined by Fry (1947) as the difference between the maximum metabolic rate (MMR) and SMR (Chabot and Claireaux 2008; Claireaux et al. 2000). Maximum metabolic rate measured in fish swimming at the maximum sustained speed is also called active metabolic rate (AMR) by some authors (e.g. Schurmann and Steffensen 1997; Claireaux et al. 2000). Fish MMR is increasingly limited as hypoxia becomes progressively more severe (Fig. 6.1, Claireaux et al. 2000; Cook et al. 2011). Fish must balance multiple metabolic demands, and swimming is an energetically demanding process (Schurmann and Steffensen 1997). Thus, hypoxic limitations to MS may limit a fish’s ability to perform activities such as swimming. Such limitations to MS will also force the fish to make decisions about how to use the available oxygen. The manner by which fish use the available oxygen will become increasingly important as they approach Pcrit, because MS will eventually be exhausted (SMR = MMR at Pcrit, Fig. 6.1). Behavioural responses are, therefore, likely to be driven by the physiological effects of hypoxia (Lefrançois and Claireaux 2003; Fritsche and Nilsson 1989). It is essential that the fish exhibit a suitable behavioural response to an O2 restricted environment because this could have a profound effect on their survival. Hypoxia may therefore elicit changes in spontaneous activity, schooling and predator–prey interactions. These may differ depending upon the species and the severity of hypoxia. This chapter reviews the effects that hypoxia can have on fish swimming perfor- mance and swimming behaviours. We discuss aerobic swimming performance in which work under controlled (i.e. forced) speed tested the effect of hypoxia on sus- tained (aerobic) swimming using swim tunnel observations. The effect of hypoxia on 132 P. Domenici et al. Fig. 6.1 Conceptual overview of how hypoxia (low partial pressure of oxygen, PO2) affects the various rates of mass-specific O2 consumption (MO2) at set temperatures. SMR = standard metabolic rate; MMR = maximum metabolic rate; MS = metabolic scope; Pcrit = critical oxygen pressure where SMR = MMR. Concepts taken from Fry (1947), Claireaux et al. (2000), Schurmann and Steffensen (1997) and Cook et al. (2011) spontaneous activity, i.e. unforced aerobic activity, is discussed next. Effects on schooling are included because hypoxia may have effects on this behaviour, given that schooling and swimming performance are tightly linked from an energetic point of view (Weihs 1973; Herskin and