mise à jour du
15 février 2009
Physiol Biochem Zool
The Influence of Dissolved Oxygen on Winter Habitat Selection by Largemouth Bass: An Integration of Field Biotelemetry Studies and Laboratory Experiments
Hasler CT, Suski CD, Hanson KC, Cooke SJ, Tufts BL.
Department of Biology, Queen's University, Kingston, Ontario. Canada
Baillements des poissons - Fish's yawn


In this study, field biotelemetry and laboratory physiology approaches were coupled to allow understanding of the behavioral and physiological responses of fish to winter hypoxia. The biotelemetry study compared dissolved oxygen levels measured throughout the winter period with continually tracked locations of nine adult largemouth bass obtained from a whole-lake submerged telemetry array. Fish habitat usage was compared with habitat availability to assess whether fish were selecting for specific dissolved oxygen concentrations. The laboratory study examined behavioral and physiological responses to progressive hypoxia in juvenile largemouth bass acclimated to winter temperatures. Results from the dissolved oxygen measurements made during the biotelemetry study showed high variance in under-ice dissolved oxygen levels. Avoidance of water with dissolved oxygen <2.0 mg/L by telemetered fish was demonstrated, but significant use of water with intermediate dissolved oxygen levels was also found. Results from the lab experiments showed marked changes in behavior (i.e., yawning and vertical movement) at <2.0 mg/L of dissolved oxygen but no change in tissue lactate, an indicator of anaerobic metabolism. Combined results of the biotelemetry and laboratory studies demonstrate that a dissolved oxygen content of 2.0 mg/L may be a critical threshold that induces behavioral responses by largemouth bass during the winter. In addition, the use by fish of areas with intermediate levels of dissolved oxygen suggests that there are multiple environmental factors influencing winter behavior.
Aquatic systems are spatially heterogeneous for a number of variables across a range of scales. Environmental heterogeneity exists because of spatial and temporal variations of different abiotic (e.g., temperature, dissolved oxygen, wave action, sunlight, and salinity) and biotic (e.g., prey abundance, vegetation cover, and conspecific location) factors that result in patches of optimal habitat mixed with patches of suboptimal and intermediate habitat. For example, lakes have some patches that are warmer than others, and these temperatures change daily and seasonally for a variety of reasons. Thus, aquatic organisms must continually seek out and compete for habitats that optimize their requirement for a suite of environmental resources based on a lake's abiotic and biotic factors (Hutchinson 1957, 1965; Fretwell and Lucas 1970). One important environmental resource that influences fish habitat selection and many physiological processes is dissolved oxygen (Hughes 1973; Kramer 1987).
Fish respond to reduced levels of dissolved oxygen in a variety of ways. Typically, chemoreceptors sense a decrease in ambient oxygen, and some physiological responses occur (e.g., increases in ventilation rate and amplitude; Perry and Gilmour 2002). Next, a behavioral response occurs, which may include habitat shifts; it is followed by the use of air-breathing organs (if present) and an increased use of surface respiration (Kramer 1987). After these behavioral responses, fish often exhibit more physiological responses to reduced levels of dissolved oxygen, including a decrease in cardiac output (Furimsky et al. 2003). Finally, if no other response is adequate, fish will switch to relying on anaerobic metabolism to meet energy demands.
Anaerobic metabolism produces far less ATP relative to aerobic mechanisms, and negative consequences of anaerobic metabolism include the production of lactate and a decrease in blood pH, both of which must be actively cleared on return to an oxygenated environment (Bennett 1978; Wendelaar Bonga 1997; Furimsky et al. 2003; Martinez et al. 2006). The behavioral, physiological, and biochemical responses of fish to hypoxia during winter conditions are not fully understood, and cold temperature may be an important covariable that influences behavioral and/or physiological outcomes because of its importance in determining rates of reactions. During winter in lakes located at high latitudes, dissolved oxygen is often less abundant than in summer, and this reduction in dissolved oxygen can influence fish behavior and habitat selection (Suski and Ridgway 2009).
Many northern temperate lakes can experience hypoxia (or even anoxia) during winter; ice cover, low light intensity, reduction in photosynthetic biomass, benthic decomposition, and crowding of fish can combine to reduce dissolved oxygen concentrations in localized areas (Greenbank 1945; Cooper and Washburn 1949). Winter hypoxia has previously been shown to influence fish behavior, movement, activity, species richness, species ranges, and population structure (Shuter and Post 1990; Fox and Keast 1991; Gent et al. 1995; Nu¨ rnberg 1995; Raibley et al. 1997; Tonn and Magnuson 1982; Farwell et al. 2007). However, few studies have measured the impact of winter hypoxia on seasonal fish habitat selection or linked fieldand laboratory-based responses to winter hypoxia. To quantify the impacts of hypoxia on winter fish responses and populations, many past studies have used controlled laboratory settings to reproduce conditions that can occur in nature (e.g., Petrosky and Magnuson 1973; Furimsky et al. 2003).
Results obtained from these studies are valuable because they allow the isolation of individual environmental variables on habitat selection to be determined in a controlled setting; however, they do not consider the suite of factors that can influence habitat selection for free-swimming fish. Biotelemetry, or the remote monitoring of free-ranging individuals, provides clues about why fish choose particular habitats over others and allows for an assessment of environmentaland individual-level variables (Lucas and Baras 2000; Cooke et al. 2004). The goal of this study was to use a combined approach involving both biotelemetryand laboratory-based experiments to better understand the influence of winter hypoxia on the behavior, physiology, and ecology of temperate fishes. Largemouth bass (Micropterus salmoides) was chosen as the study species because it is abundant in northern lakes that frequently experience winter hypoxia and winterkill (Scott and Crossman 1973).
For the biotelemetry portion of the study, a whole-lake acoustic telemetry array was used to compare the locations of fish in the winter with lakewide dissolved oxygen concentrations. For the laboratory study, the behavioral and physiological responses of fish to progressive hypoxia at winter temperatures were quantified. The combined results from these two studies will improve our understanding of how environmental variables influence habitat selection in fishes and will also allow a direct coupling between fieldand laboratory-based observations.
Eastern Ontario's Warner Lake experiences considerable variation in concentrations of dissolved oxygen available to largemouth bass over the winter. During this study's sampling dates when ice was not present on the lake, mean dissolved oxygen concentrations ranged from 10.2 to 11.3 mg/L; the twenty-fifth and seventy-fifth percentiles for dissolved oxygen concentration on these dates were 10.1 and 11.4 mg/L, respectively. Hence, fish were exposed only to water with dissolved oxygen concentrations greater than 10 mg/L. In contrast, during the icecover sample dates, mean dissolved oxygen concentrations across all of Warner Lake ranged from 2.7 to 3.8 mg/L, with the twenty-fifth and seventy-fifth percentiles on these dates 0.6 and 6.5 mg/L, respectively. Consequently, fish had access to water with a greater range of concentrations of dissolved oxygen available at these times, and the mean dissolved oxygen concentration was lower than during ice-free periods.
In addition, there was significant variation in dissolved oxygen concentration laterally across different sampling sites in the lake, providing a patchwork of available oxygen concentrations for largemouth bass to inhabit. The variance across sample dates in dissolved oxygen, as well as the overall reduction in dissolved oxygen concentration during periods of ice cover, is a result of a variety of inherent characteristics of temperate lakes at high latitudes. These include ice cover, organic decomposition, and The combined results of the biotelemetry and the laboratory studies demonstrate that largemouth bass show behavioral changes when exposed to water with dissolved oxygen concentration below 2 mg/L during winter. Sites in Warner Lake that had dissolved oxygen concentrations !2 mg/L contained significantly fewer largemouth bass than would be expected if fish were uniformly distributed with respect to oxygen concentration, while significantly more largemouth bass than expected were found in areas with 12 and !6 mg/L of dissolved oxygen.
In addition, during the laboratory study, largemouth bass significantly increased yawning (or gill flaring) and vertical movement behaviors when exposed to water with dissolved oxygen concentrations of 1.99 mg/L or less. Previous laboratory studies with yellow perch (Perca flavescens) and bluegill (Lepomis macrochirus) have shown that activity levels increase when fish are exposed to less than 2 mg/L of dissolved oxygen, presumably as they attempt to seek out habitat that is more oxygenated (Scherer 1971; Petrosky and Magnuson 1973). In our laboratory study, yawning activity (or gill flaring) increased at 1.99 mg/L, probably in order to increase water flow across gill lamellae in an effort to increase the amount of dissolved oxygen entering the bloodstream (Hughes 1973; Randall 1982; Perry and Gilmour 2002).
In winter field studies, Raibley et al. (1997) measured the dissolved oxygen at specific locations for multiple telemetered largemouth bass and found the fish to be consistently in water with dissolved oxygen concentrations 12 mg/L; however, they did not consistently record the dissolved oxygen concentrations at fish locations, and they did not quantify dissolved oxygen throughout the river system. Largemouth bass avoiding water with poor levels of dissolved oxygen would be advantageous because prolonged exposure to these waters could lead to costly, inefficient anaerobic metabolism, suffocation, and even death (Greenbank 1945; Cooper and Washburn 1949).
The combined results of our biotelemetry and laboratory studies suggest that a minimal level of dissolved oxygen near 2 mg/ L is a threshold below which behavioral changes in overwintering largemouth bass are induced. Interestingly, even though telemetered largemouth bass in our study showed an aversion to water that contained less than 2 mg/L dissolved oxygen, they did not choose to inhabit the most oxygenated water available. Specifically, during the entire period of ice cover, fish were found to inhabit sites with intermediate levels of dissolved oxygen (concentrations between 6 and 2 mg/L), even though water with 7, 8, and 9 mg/L of dissolved oxygen was available.
Previous studies have documented an animal's niche to be a combination of physical and biotic interactions, with the two types of interaction not always acting independently in space and time (Hutchinson 1957, 1965; Chapman 1966; Tracy and Christian 1986). Fry (1971) suggested that there are at least seven important factors in a fish's niche (temperature, dissolved oxygen, toxicity, metabolites, food, salinity, and carbon dioxide), while more recent work suggests that other physical and biotic characteristics (such as cover, water velocity, depth, territories, and aggregations) are equally important to niche generation (Stott and Cross 1973; Suthers and Gee 1986; Kramer 1987; Spoor 1990; Heggenes et al. 1999; Hasler et al. 2007). If some or all of these parameters are assessed by fish in Warner Lake when they make habitat decisions, the choice of intermediate oxygen patches must have benefits that outweigh the advantages associated with inhabiting more oxygenated water.
Specifically, in addition to oxygen, factors such as proximity to conspecifics (Breder and Nigrelli 1935; Hasler et al. 2007), proximity to cover, and/or prey abundance may affect selection of habitat by largemouth bass. Fish in this study chose not to inhabit areas with the highest dissolved oxygen concentrations and selected areas with lower amounts of dissolved oxygen, which suggest that fish are using other environmental variables in conjunction with dissolved oxygen to make habitat choices. Although there was an avoidance of areas with dissolved oxygen !2 mg/L, two of nine fish spent some time in such water during the March sampling period (although only for a few hours per day).
Moreover, during the laboratory study, fish did not exhibit increased lactate concentrations in white muscle, despite 1 h exposure to dissolved oxygen concentrations !2 mg/L, indicating that they were still respiring aerobically, despite this low oxygen concentration. It is important to consider, however, that oxygen requirements in winter will be low; two separate studies have concluded that the metabolic rate of largemouth bass during the winter months is greatly reduced and that fish are essentially dormant at that time (Beamish 1970; Crawshaw 1984; Lemons and Crawshaw 1985). In our study, the use of intermediate areas by largemouth bass is not unexpected, since previous studies have shown that hypoxia is not an absolute barrier to fish movements and that fish will use hypoxic zones for opportunistic feeding (Pihl et al. 1992; Rahel and Nutzman 1994).
One possible reason is that during winter conditions, slightly higher temperatures that are present in areas with low amounts of dissolved oxygen (because of decomposition of organic material) would allow for increased metabolism and activity (Fry 1971; Gee et al. 1978; Burleson et al. 2001). In winter, it may be beneficial for fish to tolerate lower dissolved oxygen concentrations that might be lethal during warmer periods, when the oxygen requirements are relatively higher (Fry 1971). However, our laboratory study did not find a physiological change when fish were exposed to hypoxia: tissue lactate, an indicator of anaerobic respiration, did not change. It is evident from the current biotelemetry and laboratory studies that largemouth bass tolerate low levels of dissolved oxygen during winter.
In addition, short-term laboratory exposure to low amounts of dissolved oxygen did not facilitate a metabolic change, suggesting that the physiological consequence of winter habitat selection is minimal. Age and size differences among fish of the same species may influence behavioral and physiological responses to stressors such as exhaustive exercise or low dissolved oxygen (Cech et al. 1979; Petersen and Petersen 1990; Kieffer et al. 1996; Burleson et al. 2001). For example, Kieffer et al. (1996) found a significant positive relationship between the accumulation of muscle lactate, metabolic protons, and body size in brook trout (Salvelinus fontinalis ) that were exhaustively exercised (exercise that essentially results in hypoxic conditions in the swimming muscle; Kieffer et al. 1996) but did not find a difference in the anaerobic response to exercise between large and small largemouth bass. In our study, larger fish were used in the biotelemetry study than in the laboratory study because of size limitations related to transmitter implantation.
However, regardless of this size difference, both experiments revealed a similar threshold at which a response to hypoxia was generated&emdash;approximately 2 mg/L. Specifically, in our laboratory study, yawning and vertical movement began to happen at 1.99 mg/L, while in the telemetry study, fish were rarely found in water with less than 2 mg/L of dissolved oxygen. In a similar result, Burleson et al. (2001) found that regardless of fish size, largemouth bass typically avoided water below 2.4 mg/L during laboratory experiments. Also, they did not find differences in short-term selection for particular areas; larger fish were equally as likely to venture for brief periods of time to areas of low dissolved oxygen concentration when compared to smaller fish (Burleson et al. 2001).
Thus, results from previous studies have not documented a size-specific response to anaerobic stressors for largemouth bass (Kieffer et al. 1996; Burleson et al. 2001). Likewise, fish in our biotelemetry and laboratory studies, although different in size, demonstrated similar avoidance responses to cold water with approximately 2 mg/L of dissolved oxygen.
Biotelemetry and laboratory studies conducted to determine the factors affecting behavior and physiology are most often performed independently. In this study, these two approaches were used synergistically to quantify the effect of hypoxia on the behavior and physiology of overwintering largemouth bass. Ambient dissolved oxygen concentration was found to influence not only individual behavioral responses such as increased surface breathing but also habitat selection in the wild.
More specifically, largemouth bass telemetered in the field tended to avoid areas with dissolved oxygen concentrations !2.0 mg/L, and laboratory-tested largemouth bass exhibited behavioral responses, such as yawning and vertical movement, when exposed to water with dissolved oxygen levels near 2.0 mg/L.
Large-mouth bass tended to choose water with intermediate concentrations of dissolved oxygen over the most oxygenated water available, possibly because of multiple abiotic and biotic variables. Overwintering largemouth bass appear to avoid water with less than 2.0 mg/L of dissolved oxygen, but further research is needed to understand the extent to which prolonged exposure to low amounts of dissolved oxygen affects physiological processes.