Dissolved oxygen variability in a commercial sea-cage exposes farmed Atlantic salmon to growth limiting conditions
Introduction
The environment within marine aquaculture cages can be highly variable (reviewed by: Oppedal et al., 2011b), and is a critical determinant of growth rate in farmed fish. Two of the most important external factors directing fish metabolism are temperature (reviewed by: Eliason and Farrell, 2016), and oxygen availability (Richards et al., 2009). Temperature determines metabolic rate, and thus the pace of growth, while dissolved O2 is the primary limiting factor for aerobic metabolism (Claireaux and Chabot, 2016).
Recent work on Atlantic salmon (Salmo salar) post-smolts has demonstrated that, in this species, aerobic scope (Hvas et al., 2017a) and feed intake (Remen et al., 2016) increase throughout ecologically and farm relevant temperatures (3–23 C and 7–19 C, respectively). In parallel, the metabolic rate and amount of O2 required for fish to survive and grow also increase. As a consequence, salmon post-smolt have increasing O2 requirements with temperature, and the limiting oxygen saturation (LOS) below which they switch to anaerobic glycolysis rises from 30% at 6 C to 55% at 19 C (Remen et al., 2013). In less extreme hypoxia, as high as 76% dissolved O2 saturation, feed intake declines (Remen et al., 2016). Even in cyclic hypoxia with salmon kept and fed in normoxic conditions but subjected to 1 h of 50% dissolved O2 saturation every 6 h, specific growth rates were reduced by 13% compared to normoxic controls (Remen et al., 2014). In a similar trial, when salmon were fed during hypoxic conditions, growth rates were reduced even further (Burt et al., 2013).
Given its physiological importance, understanding how dissolved O2 varies within marine cages, and what conditions salmon experience as a result of such variation, is paramount to maximizing salmon production performance and welfare. Temperature, current velocity, salinity and dissolved O2 have all been observed to vary vertically in marine cages (e.g. Johansson et al., 2006, Johansson et al., 2007, Oppedal et al., 2011b, Burt et al., 2012, Stien et al., 2012, Dempster et al., 2016), with mean dissolved O2 as much as 20 percentage points different between the surface and cage bottom (Johansson et al., 2006). But fish in marine cages are not only moving up and down through a 2-dimensional environment, they are faced with the far more complex challenge of moving, constantly, through an ever changing 3-dimensional environment.
Little is known about how dissolved O2 varies horizontally within marine cages. Studies of water movement horizontally across cages have found that current speed and direction are highly variable (Johansson et al., 2007, Stien et al., 2012, Frank et al., 2015), and strongly affected by fish behaviour (Klebert et al., 2013, Gansel et al., 2014). Given that physical transport mechanisms such as currents and wave action are the primary means through which oxygen is replenished in marine cages (Edwards and Edelsten, 1976, Wildish et al., 1993, Johansson et al., 2007), and that fish do not distribute themselves evenly throughout the cage (Oppedal et al., 2011a, Oppedal et al., 2011b, Johansson et al., 2014), it is expected that dissolved O2 will also vary horizontally.
Observations of salmon group behaviour have recorded changes in vertical distribution in response to a wide variety of environmental stimulus including light (Oppedal et al., 2007, Wright et al., 2015), temperature, salinity, feeding (Oppedal et al., 2011a), water current velocity (Johansson et al., 2014), sound (Bui et al., 2013) and sea lice infestation level (Bui et al., 2016). Avoidance of sub-optimal dissolved O2 conditions, however, is inconsistent (Johansson et al., 2006, Johansson et al., 2007, Burt et al., 2012), and in heterogeneous environments can be superseded by other factors (Stien et al., 2012, Dempster et al., 2016, Oldham et al., 2017).
A great deal of inter-individual variation in swimming depth has also been observed within groups of caged salmon (Juell and Westerberg, 1993, Johansson et al., 2009, Korsøen et al., 2012, Nilsson et al., 2013). And while group observations provide information on average behaviour and general trends, observations of the environment as experienced by individuals can provide a deeper understanding of the physiological implications of cage variability as well as the coping mechanisms employed by individuals facing heterogeneous conditions (Juell, 1995).
To improve understanding of dissolved O2 variation within the cage environment, and how salmon respond to and experience such variation, in this case study we, a) tracked the dissolved O2 experience of multiple individual salmon, and b) mapped the 3-dimensional marine cage environment with respect to salinity, temperature and dissolved O2.
Section snippets
Study site
Observations were collected in two case study periods from 8 to 12 October (period 1) and 2–7 November (period 2) 2012 at a commercial marine cage farm in Storeneset, a small branch of Fensfjorden, western Norway (60.5° N), Fig. 1. Measurements were collected from 1 of the 5 cages at the site which measured 20 m deep and 50 m in diameter. The depth below the cages varied from 50 to 120 m. According to farm data, the observed cage was stocked with 170, 300 Atlantic salmon with an average weight of
Results
Of the 8 individual fish fitted with dissolved O2 loggers, 3 were excluded from final data analysis due to excessive measurement drift (> 5%) between study periods, and a 4th was lost. The remaining 4 individuals equipped with transmitters experienced large variation in dissolved O2, from 30 to 90% saturation, spanning the full extent of observed variation within the cage (Fig. 2, Table 3). Dissolved O2 experience varied significantly between individuals (F = 458, p < 0.001), with average dissolved O
Discussion
Using a combination of individually tagged salmon and 3-dimensional water quality measurements, this data reveals important and novel insights about the cage environment. Extreme temporal and spatial variation in dissolved O2 distribution within the cage led to salmon experiencing suboptimal conditions known to negatively impact growth. Each of the tagged individuals experienced the full range of dissolved O2 conditions present within the cage, and though partially relieved by behaviour in some
Conclusion
The extreme variability of dissolved O2 conditions observed throughout the cage, ranging from 30 to 90% saturation, was mirrored in the experiences of individually tagged fish. All tagged individuals were exposed to dissolved O2 conditions limiting to growth and production performance. Additionally, the 3-dimensional mapping of environmental conditions within the cage documented a novel and complex pattern of dissolved O2 variability across the cage width, with hotspots of poor oxygen
Conflicts of interest
None.
Acknowledgements
The authors are greatly indebted to the personnel at the salmon farm and Jan Erik Fosseidengen for their kind assistance. The work was funded by the Norwegian Research Council project “Salmon Dynamics” (206968), as well as an Australian Government Research Training Program Scholarship.
Author contributions
Conceived and designed the experiments: DS FO PK FS TV. Performed the experiments: DS TV PK. Analyzed the data: DS TO LS PK. Wrote the paper: DS TO FO. All authors contributed to manuscript editing and revision, and have approved the final article.
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2023, AquacultureCitation Excerpt :Moreover, in a changing environment, due to climate change, the elevated sea water temperature may set new challenges for respiration (Pörtner et al., 2017; Pörtner and Knust, 2007). These challenges can be even greater for animals reared under extensive aquaculture conditions, since during the warm months of the year, a combination of reduced oxygen capacity of the warm water with the reduced circulation of water through the net of the cage due to fouling and the increased oxygen demand by the fish can make oxygen scarce (Johansson et al., 2006; Makridis et al., 2018; Solstorm et al., 2018). Hypoxia is a shortage of oxygen, usually defined as dissolved oxygen concentrations below 2–3 mg O2 l−1 (Farrell and Richards, 2009).
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