The Effects of Dissolved Oxygen, Temperature, and Low Stream Flow on Fishes: a Literature Review

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THE EFFECTS OF DISSOLVED OXYGEN, TEMPERATURE, AND LOW STREAM FLOW ON FISHES: A LITERATURE REVIEW

Aquatic Biology Section Technical Report

D. C. Dowling and M. J. Wiley

Report to Springfield City Water, Light, and Power Company L -Aff NN )logy -opp--..A Technical Report 1986(2)

Illinois Natural History Survey Aquatic Biology Technical Report 1986(2)

THE EFFECTS OF DISSOLVED OXYGEN, TEMPERATURE, AND LOW STREAM FLOW ON FISHES: A LITERATURE REVIEW

by D. C. Dowling and M. J. Wiley

to Springfield City Water, Light, and Power Company

M. J. Wiley, Princip 1 Investigator Robert W. Gorden, Head Aquatic Biology Section

\ THE EFFECTS OF DISSOLVED OXYGEN, TEMPERATURE, AND LW STREAM FLOW ON FISHES: A LITERATURE REVIEW

The chemical composition of rivers is very variable, depending on season, time of day, place, and depth (Golterman 1975). Of all the chemical substances in natural waters, oxygen is one of the most significant. The annual cycle of oxygen in a stream is closely correlated with temperature. Studies of large rivers and small streams in warm southern regions of moderate temperature regimes and in northern climates of broad temperature fluctuations have shown that the oxygen content of flowing waters is generally highest in winter and lowest in late summer. In small, slow-flowing streams of northern latitudes, decreased day length and ice and snow cover may inhibit photosynthesis and prevent entry of oxygen from the air, thereby depressing the oxygen concentration. Sometimes this oxygen depression becomes quite severe, stressing the resident fish populations, as was documented in the River Ob in Siberia (Mosevich 1947, Mossewitsch 1961). They documented oxygen levels falling to 14% saturation; the fish left the affected regions and congregated in a few more tolerable areas.

The vernal decline of oxygen content in slow-flowing streams may be attributed to the action of spring floods in removing vegetation and to the increased rate of decay of organic material with increasing water temperature. Further decreases in oxygen content toward late summer are due to one or more factors. High temperature water, reaching a maxinum in late summer, holds less oxygen in solution; decreased discharge results in diminished physical mixing and reoxygenation; and greater decomposition of naturally produced organic material uses some of the available oxygen (Reid 1961). When rainfall is light, rivers are generally fed by groundwater. Often underground water is devoid of oxygen and contains large amounts of carbon dioxide, because of its exposure to organic matter and bacterial respiration in the soil; although in limestone strata, where underground water usually flows through large solution channels, oxygen content of the emerging water may be high.

In many streams there is also a diurnal variation in oxygen content. The diurnal pulse is largely a reflection of temperature fluctuations and photosynthesis-respiration relationships. This diurnal pulse may become exaggerated in streams where the discharge is low and algal populations large. In summer, the diurnal curve is characterized by oxygen production lagging behind rising temperature, often by 2 or 3 hours, thus imparting high saturation values even after sundown. Depending upon oxygen demand, the minimum, and possibly most critical, level usually occurs prior to the early-morning low temperature. In streams of this nature, the oxygen concentration may be actively affected by sunlight intensity.

Autumn leaf fall, in combination with low flow, has been shown to create seasonally low oxygen concentrations. In the U.S. Southeast and Mid- western regions, and doubtless in other areas with similar hot and dry summers, small streams are reduced to a series of disconnected pools with little more than seepage between them. During autumn, great quantities of leaves are shed by riparian trees into the pools. The water acquires an inky black color, because organic matter leaches from leaves; oxygen concentrations fall to low levels; and these conditions persist until it rains (Schneller 1955, Slack 1964). Any organism that survives in such streams must be either very resistant to low oxygen or have a life history that ensures that no specimens are active in the water during late summer and autumn (Hynes 1970).

Documented Effects of Drought

Organisms inhabiting small, warmwater streams of central North America are normally exposed to severe environmental fluctuations; during periods of deficient rainfall and reduced stream flow, they are subjected to extreme physical, chemical, and biological stresses. Constriction of the environment changes competition, predation, and survival among crowded, displaced organisms. Evaporation, stagnation, and organic decomposition alter the

2 dissolved salts and gases upon which aquatic life depends (Larimore et al. 1959). In Smiths Branch, a small warmwater stream in Vermilion County, Illinois, discontinuous flow in the summer of 1953 reduced the aquatic habitat and exposed fish and invertebrates to desiccation, stagnation, and predation. Larimore et al. (1959) determined that mid-summer impoundment of the stream waters was not as detrimental to fish as might be expected. Even though the supply of well oxygenated riffle waters ceased and extreme thermal stratification occurred, no fish mortality was seen in July or August of any year with discontinuous flow. Stagnation was more destruc- tive to aquatic animals during September and early October, as leaves and other dead plant materials accumulated in the pools, decomposed, and progressively increased oxygen demand.

Most fish withstood extreme drought conditions in at least a few parts of the stream. Re-establishment of the populations began as soon as the stream resumed its flow, and during the following 2 weeks, 21 of 29 regularly occurring species moved into most of the stream course (Larimore et al. 1959). Twenty-five of the regular species of fish entered Smiths Branch by the end of the first summer. Only three species were significantly absent. The longear sunfish (Lepomis megalotis) was not taken until fall of 1955, and the blackstripe topminnow (Fundulus notatus) and the hornyhead chub (Nocumis biguttatus) had not repopulated the stream when final collections were made in 1957. Invertebrates displayed remarkable adaptations to drought conditions and repopulated Smiths Branch soon after flow resumed.

Other researchers have also studied the impact of droughts on stream systems. Cowx et al. (1984) investigated the effects of the 1976 summer drought on both fish and invertebrate populations of the Afon Dulas stream in Wales. The most significant effect was the failure of the 1976 year class of salmon. They felt that salmon alevins of the 1976 year class, which are less tolerant than either trout or older salmon par to prolonged exposure to temperatures around their upper lethal limit, did not survive high water temperatures in June and July. Some compensation for this loss to the fish populations was indicated by enhanced recruitment in 1977,

3 i.e., the numbers of juvenile salmon surviving beyond fry stage was greater in 1977 than in 1975, a year of typical recruitment.

One of the major effects of drought on invertebrates was the overall decrease in potentially colonizable habitats due to reduced depth and width of the river (Cowx et al. 1984). A reduction in wetted bed area may also have long-term implications, because many adult insects lay eggs in fast-flowing or broken water (Sawyer 1950); if suitable areas are reduced, subsequent populations may be affected (Hynes 1958). Follow-up surveys in 1977 and 1978 indicated that invertebrate fauna in the Ob Dulas had fully recovered from the drought, both in terms of taxonomic diversity and abundance, suggesting that invertebrate fauna in rivers can recover quickly from the effects of drought, usually within several life cycles.

Hynes (1958), working on a small stream in Wales, found that several species of worms and small crustacea can survive prolonged drought and that, although most insect nymphs and larvae are killed, eggs may survive. The number surviving depends on whether the drought coincides, at least partly, with the normal hatching period. Wickliff (1945) indicated that crayfish that normally do not burrow, may follow the receding water table for several inches underground and survive for weeks if the chamber into which they retreat remains moist; in pool and riffle headwaters, small fish are able to exist for months in large numbers in greatly reduced volumes of suitable water, returning to the riffles when flow resumes.

In general, invertebrates are better able to withstand the effects of drought than are fish, because of egg, nymphal, or pupal diapauses, emer- gence, or burrowing (Canton et al. 1984). Recolonization is rapid following resumption of flow (Hynes 1975, Townsend and Hildrew 1976, Williams and Hynes 1976a, 1976b, 1977).

In a Colorado stream in 1978 and 1979, Canton et al. (1984) investigated the impacts of low flow in 1978. Brook trout (Salvelinus fontinalis) collected in 1978 were thin and moribund when handled. Average weights

4 for each age class were lower than expected on the basis of other North American studies (Carlander 1969), and as a result, the mean condition factor (K) was lower in 1978 than in 1979. Regenerated scales, which often indicate environmental stress, were found on many fish in 1979. In a few cases, especially on white suckers (Catostomus camersoni) and brook trout, only regenerated scales were found. Regenerated scales were not observed in 1978. Fish population densities were significantly reduced by the drought, with no fish collected in most of the study area. After resumption of normal discharge, fish were abundant throughout the study area, although the greater abundance of trout at the upper end of the study area suggested that migration from Manitou Lake into the study area occurred. This lake probably was a refuge for stream fish during the drought. The rapid recovery of fish populations from drought has also been noted in studies by Stehr and Branson (1938) and Starrett (1950).

Canton et al. (1984) discovered through functional feeding group analysis that collector-gatherers and collector-filterers were relatively more important during normal flow years, whereas shredders and predators had greater importance during low flow. The decreased importance of gatherers and filterers during a drought may be related to a combination of factors, such as loss of habitat, decreased suspended matter, and increased predation pressure. However, the large increase in total density in 1979 again indicated rapid recovery of stream invertebrates camnunities from drought. This recovery was probably a result of survival of eggs in moist substrate, subsequent oviposition by aerial adults, and invertebrate drift from the upstream reach when flow resumed (Gray and Fisher 1981, Fisher et al. 1982). Mayflies appeared to be most severely affected by reduced discharge and Diptera least affected. Low discharge seemed to affect invertebrates primarily through loss of habitat, because temperature was not significantly affected.

5 When faced with low dissolved oxygen, many fish species will migrate to more tolerable regions, dramatically altering the local fish community structure. Tsai (1970), studying the Little Patuxent River in Maryland, found that fish species sensitive to organic enrichment and low dissolved oxygen decreased in abundance or disappeared. They were replaced by species that were tolerant to organic enrichment and low dissolved oxygen. Adversely affected species included important game fishes, such as smallmouth bass (Micropterus dolmieui), largemouth bass (L salmoides, and black crappie (Pomoxis nigrmaculatus). Favorably affected species included less important game fish, such as sunfishes, and coarse fish, such as the American eel (Anmuilla rostrata) and the creek chubsucker (Er imyzon oblongs).

Garmmon and Reidy (1981) stressed the important role that tributaries play during episodes of low dissolved oxygen. They noted that, under normal or high flow conditions, fish commnunities in tributaries to the middle Wabash River, Indiana, tended to be smaller, less diverse, and of a different species composition than fish conmunities in the mainstem. In late July and early August 1977, dissolved oxygen concentrations declined to a low of 1.0 mg/liter in a 35-mile stretch of the river. During that period, pollution-sensitive fishes moved into the mouths of tributaries, increasing several caununity indices. Such movements to avoid stress conditions in the Wabash mainstem have been hypothesized by Gammon (1976) . Previous work by Cross (1950), Minckley (1963), and Krumholz and Minckley (1964) documented this phenomenon in other rivers.

Fish often seem to avoid lethal levels successfully when better oxygenated water is accessible (Doudoroff and Shumway 1970). Concentrations below 4- 5 mg/liter apparently interfere with upstream migration of adult salmonids (Sams and Conover 1969), but migration of these and other anadromous fish through waters of lower dissolved oxygen concentrations of 2-3 mag/liter has been observed. Tagatz (1961) observed that young American shad ceased schooling when the dissolved oxygen concentration was reduced slowly to 1.4 mg/liter or rapidly to 2.4 mg/liter. However, sublethal effects of hypoxia on young shad, indicated by refusal to eat, rapid gulping, and breaking up of schools, seemed to begin at an oxygen concentration of 4.5 mg/liter (Chittenden and Westman 1967).

Time of year may delay recolonization of streams, even if they are fully recovered in terms of water quality and flow. Larimore et al. (1959) found that fish moved back into Smiths Branch quickly during April and May, but re-invasion was slow for several weeks during late February and early March, after stream flow resumed. Katz and Gaufin (1953) also observed a delay in re-invasion during winter; fish in winter did not move into a previously unacceptable area of a polluted Ohio stream, even though it was judged to be free of harmful pollution.

As indicated previously, many different grades of tolerance to low dissolved oxygen exist between stream fishes. Matthews and Styron (1981) investigated the tolerance of headwater versus mainstream fishes to abrupt physicochemical changes. They found that the mountain redbelly dace (Phoxinus )ore),the most abundant cyprinid in the intermittent headwaters of Mason Creek, Virginia, to be significantly more tolerant of abrupt changes in dissolved oxygen concentration, temperature, and pH than were three cyprinid species characteristically found in the more physicochemically stable Roanoke River and its larger tributaries. Their results suggest a correspondence between physicochemical tolerances of fish species and the upstream limits of their distributions in a stream with environmentally unstable headwaters. Fishes in other physically harsh environments have wide physicochemical tolerance limits, which can be related to their distributional limits. Cross and Cavin (1971) found the red shiner (Notropis lutrensis), which is highly successful in intermittent prairie streams, to be more tolerant of low oxygen conditions that the bluntface shiner (L. camurus), which is restricted to permanently flowing upland streams.

7 Matthews and Styron (1981) also reported that a greater portion of headwater than mainstream fantail darters (Etheostma flabellare) survived brief periods of oxygen stress. Small intraspecific differences in tolerance could be important, if over time they resulted in ecotypes adapted to specific parts of a heterogeneous watershed. Intraspecific differences in physiological tolerances among populations in a single watershed could influence local distribution patterns and help isolate populations, comprising an initial step in the speciation process. Burdick et al. (1954) noted that smallmouth bass in Bebe Lake, New York, were less sensitive than populations in Deer River to dissolved oxygen (Table 1). Oxygen acclimatization in a lake might be to a lower level than that in a rapidly flowing, relatively unpolluted stream.

Matthews and Hill (1979) looked at age-specific differences in the distribution of red shiners over physicochemical ranges and found that juveniles occupied warmer water than did adults in February, May, and August, higher oxygen concentration in February and October, and higher pH conditions in February and August. Juveniles occupied shallower water than did adults in February and August, locations with less shade in May, and less shelter in February, May, August, and October. Both groups occupied locations with very slow current. The mean habitat breadth of adults changed more as environmental conditions changed than did that of juveniles. Stress on red shiners was probably greatest in October, near the end of a lengthy drought, and in December-January when it was unusually cold.

Temperature and oxygen tolerances of four cyprinid species in a southwestern river coincided with their relative success during drought (Matthews and Maness 1979). The emerald shiner (Notropis atherinoides), which was least tolerant of temperature and oxygen, decreased in abundance in the sumner and apparently failed to spawn in 1976. The Arkansas River shiner, which was highly tolerant of low oxygen, was more successful than the plains minnow (fHybonathus placitus) or the red shiner from August to October, although substantial algal blooms during that time caused low nocturnal oxygen concentrations. Oxygen probably exerted less selection pressure than did temperature. The critical thermal maxima (CTM), which

8 Table 1. Summary of data on lethal oxygen concentrations (in parts per million) for smallmouth bass (Burdick et al. 1954).

Oxygen concentrations Number ; Temperature found lethal Standard Standard of fish in degrees F. M axi- deviation ]imum m um error mum mum I Median I'Mean

Deer River

29 54.0 0.95 0.58 0.72 0.74 ±0.083 ±0.015

20 60.0 0.98 0.63 0.87 0.83 ±0.121 ±0.028

14 70.0 1.23 0.77 0.91 0.96 ±0.138 ±0.037

9 80.0 1.32 0.99 1.17 1.15 ±0.132 ±0 044

Beebe Lake

20 1 52.5 0.85 0.48 0.63 0.63 ±0.142 ±0.032 15 60.0 1.10 0.48 0.73 0.73 ±0.145 ±0.037

20 70 0 1.19 0.61 0.86 0.87 1 ±0.133 +0 030

20 80.0 1.56! 0.72 1.03 1.08 ±0.221 ±0 050

9 is the thermal point at which locomotry activity becomes disorganized and the animal loses its ability to escape from conditions that will cause its death (Mihurksy and Kennedy 1976), were more closely related to field success than was low oxygen tolerance. The red shiner and the plains minnow, with higher CT' s, exhibited greater population increases from May to October than did the other two species.

Fish may use other mechanisms to avoid the stress of deoxygenated waters. Gee et al. (1978) studied the reactions of 26 species of Great Plains fishes from eight families to progressive hypoxia. He noted that when freshwaters become hypoxic some fishes respond by breathing air facul- tatively. Others remain aquatic breathers, rising to the surface where they irrigate their gills with relatively oxygen-rich surface film. All species were able to use oxygen in the surface film, except Salmonidae (three species) and the walleye (Stizostedion vitreum)i. The concentration of dissolved oxygen at which this reaction occurred was found to be strongly temperature dependent in the fathead minnow (Pimephales promelas). Lowe et al. (1967) stated that, on the whole, minnows are more advantageously adapted structurally and behaviorally than are suckers to competition for surface-layer oxygen.

Connell (1975), Wiens (1977), and Diamond (1978) suggest that competition or predation pressures may be less intense, or at least occur less fre- quently, in harsh, fluctuating environments and some species avoid competition or predation through evolution of wide physicochemical tolerance and use of rigorous environments. Whether this is true remains to be seen, but it is readily apparent that a fish is affected by numerous biological factors: through its senses, by its associates, its school, predators, prey, algae, and aquatic plants, in addition to the changing physical and chemical characteristics of the water, which vary with depth and season (Sondheimer and Simeone 1970). It is this array of factors that actually constitutes what chemical concentrations a fish will survive and where it will reside. However, the effects of the combined influence of current, oxygen, and temperature on lotic species has not been accu- rately assessed (Brown 1971). Individual laboratory experiments have

10 shown how some of these factors may impact fish in their lotic environment.

Physiological Responses

The rate of oxygen consumption in freshwater fishes is not constant (Clausen 1936); it varies in the same fish from hour to hour, and it varies between individuals of the same species. Daily fluctuations are probably part of larger rhythms that harmonize with the physiological cycles of the animal. Wells (1914) pointed out differences in the resistance of fishes during breeding and later in the summer. Beamish (1964) investigated the standard rate of oxygen consumption (when the fish is nearly or completely resting) and the active rate of oxygen consumption (when the fish is stimulated to continuous activity) for brook trout, carp, and goldfish. These data indicate that, over a range of relatively high partial pressures of oxygen, the standard rate of consumption remains constant while the active rate increases with increases in the partial pressure (Fig. 1). Basu (1959) found that, when the oxygen concentration of water falls below a critical level, the fish is unable to satisfy its need for oxygen and oxygen consumption becomes dependent on the oxygen concentration of the water. For many fish species, oxygen concentrations below which activity is limited have been determined (Fry and Hart 1948, Graham 1949, Gibson and Fry 1954, Job 1955).

The classical concepts of Fry (1957) are embodied in Fig. 2. The point at which available oxygen coincides with oxygen needs for bare maintenance is termed the incipient lethal tension. Below this level, organisms resist for a time but eventually die. Standard metabolic rate was defined by Brett (1962) as the minimal metabolic rate accompanying the energy cost of maintenance, measured under laboratory conditions. It is close to, but slightly higher than, the thermal basal metabolic rate used by others. The point at which metabolic rate ceases to be dependent on available oxygen is termed the incipient limiting tension, or also the no-effect oxygen threshold, which affords good protection for fish species. In animals tolerant of low oxygen, the curve in Fig. 2 shifts to the left,

11 E

cbC

0 E I ro 0 o - 280 c -

- o 200

120

40 0 19EON %d1 l , 20 60 100 140 180 Partial Pressure of Oxygen, mm Hg

Fig. 1. Relation between standard and active oxygen consumption for carp. Solid symbols represent values for fish acclimated to air saturation. The standard curves have been taken from Fig. 2. The broken line represents the results for carp acclimated to the various partial pressures of oxygen applied. The weight range of carp used at the active level was 36 to 750 g at 10 C and 140 to 540 g at 20 C (Beamish 1964). I .

12 ZONE OF I ZONE OF RESPIRATORY DEPENDENCE I RESPIRATORY REGULATION ZONE OF L RESISTANCE I4 ZONE OF TOLERANCE

hi 4 INCIPIENT LMITING TENSION B. z hi 0 K 0 Ii. 0 hi STANDARD METABOLIC RATE 4

INCPIET ETHL ENSION INCIPIENT LETH AL TENSION

ENVIRONMENTAL 0 2

Fig. 2. Relation between standard and active (Maximum) oxygen uptake rates at different environmental oxygen concentrations (from Hoar 1966).

13 while in animals requiring higher levels of oxygen the curve shifts to the right. Thus, the oxygen tension that produces respiratory dependence varies with species (Davis 1975).

Ventilatory and circulatory changes have been observed in a number of fish species in response to hypoxia. Rainbow trout (Salm~ gairdneri) (Holeton and Randall 1967a, 1967b) and carp (Cyprinus car.piQ) (Garey 1967) show elevations in both rate and amplitude of breathing and decreased heart rate in response to low oxygen. In trout, the stroke volume of the heart increases, thus maintaining cardiac output as the heart rate decreases. The gill transfer factor for oxygen (a measure of the ability of the gills to transfer oxygen per unit gradient) increases, water flow through the gills goes up, and venous oxygen tension drops. All of these factors operate to maintain oxygen uptake with reduced oxygen availability.

These responses of fish to hypoxia represent compensation or adjustment of bodily processes. Fish can only resist or tolerate reduced oxygen levels for short periods. The success of tolerance depends on species, oxygen levels, and environmental factors, particularly temperature. Davis (1975) summarized temperature and oxygen levels at which many fish species are affected and the degree to which they are affected (Table 2).

Effects n Growth and Fecudit

Use of regulatory or compensatory mechanisms requires energy expenditure and reduces energy reserves for swinming, feeding, predator avoidance, and other activities. Stewart et al. (1967) investigated the influence of oxygen concentrations of the growth of juvenile largemouth bass. Its growth and food consumption rates increased with increases in dissolved oxygen to levels near saturation and declined with further increases of oxygen concentration (Fig. 3 and 4). Gross food conversion efficiencies were reduced only at concentrations below 4 rag/liter (Fig. 5). Stewart et al. (1967) also noted that growth of bass subjected alternately to low and

14 Table 2. The incipient oxygen response thresholds for various fish groups and habitats gathered from the literature with emphasis on Canadian species. The ration- ales for choosing the reported response and its significance are reported in the following pages 2301-2311. In most instances, oxygen response thresholds were found in only one form of terminology (e.g. column 6--mg 02/liter)and the others in the table were calculated. Calculations for freshwater fish made use of the reported temperature and the 02 solubility data in Tables 1 and 2 while those for nonanadromous fish in sea water used the data in Table 3 and an assumed salinity of 28%. It is stressed that the response levels reported are incipient oxygen levels where effects first become apparent thus providing a "biological indication" of the onset of hypoxic stress. A) Freshwater species, B) Marine nonanadromous species, C) Anadromous species, D) Eggs and larvae (freshwater and marine species) (Davis 1975).

Level of dissolved oxygen Temp Response to oxygen Species Size (C) P0 2-mm Hg ml O 2 liter mg O 2 /liter 7, Satn. level Itrema

A. Freshwater species Arctic char, - 2±.05 25 1.53 2.18 15.8 "signs of asphyxia Holetm Salvelinus and loss of equilibrium" (1973) alpinus brown bullhead, 43-127 9-10 60 4.87-4.76 6.95-6.80 38.0 onset of oxygen - Ictalurus nebulosus g dependent oxygen uptake (196) Rainbow trout, 682-1136 20 78 3.20 4.59 50 below this level blood Irving et . Salmo gairdneri g is not fully saturated (1941) with oxygen 120-250 8.5-15 80-100 3.63-5.14 5.18-7.34 50.7-63.7 circulatory changes Randsd g occur, including a andSIta slowing of heart carp, 77-350 g 10 50 2.51 3.59 31.7 standard oxygen up- Beamilh Cyprinus carpio take elevated (de- (1964) 30-600 g 20 80 3.29 4.71 51.3 pressed at lower levels) 235-785g 13.3-25 80 2.74-3.04 5.39-4.34 50.9-51.6 blood ceased to be Itazaw fully saturated with (1970) 02 below this level Walleye, 2 yr-old 22 35.2-70.4 2.8-1.4 4-2.0 45.3-22.7 loss of negative pho- ScShr Stizostedion vitreum totaxis (light avoid- (1971) ance behavior) 70.4-96.8 3.85-2.8 5.5-4.0 45.3-62.3 increased mobility, "darting" behavior Largemouth bass, 5-9 - - 3.15 4.5 - some indication of Whitmort Micropterus cm avoidance behavior et al. salmonides I.I 1.5 - marked avoidance (190) Brook trout 682-1136 20 77.95 3.21 4.59 50 blood ceases to be Irvialgetid. (speckled trout) g fully satd. with 02 (1941) Salvelinus below this level fontinalis 17-65 5 100 5.66 8.09 63.2 onset of Or-dependent Graham g metabolism (1949) 8 80 4.19 5.99 50.7 reduced cruising speed 20 154 6.34 9.06 98.8 onset of Or depen. dent metabolism 5-20 116.9-118.7 6.72-4.82 9.6-6.88 75 reduced activity, all temps. 56-140 10,15 80 4.03-3.63 5.75-5.18 50.7-51.0 standard oxygen up- Beamish g take reduced below (1964) this level Brown trout, 682-1136 20 77.95 3.21 4.59 50 blood ceases to be Irving et aL Salmo trutta g fully satd. with O (1941) below this level Rainbow trout, 13.3±1.4 17± .5 156.6 6.82 9.74 100 any reduction in Downing Salmo gairdnerl cm oxygen led to more (1954) rapid death in cyanide 20 mos old 8-10 78.85-79.95 4.16-3.97 5.94-5.67 50 43% reduction in Jones maximum swimming (1971b) speed 21-23 77.85-77.6 3.15-3.04 4.50-4.34 50 30% reduction in maximum swimming speed 235-510 2.3-13 100 6.11-4.71 8.73-6.74 63.1-63.6 blood is not fully Itazawa g satd. with oxygen (1970) below this level - 15 78.45 3.55 5.08 50 altered respiratory Kutty quotient, little capacity (1968a) for anaerobic metabolism below this level - 15 80-100 3.63-4.53 5.18-6.47 51.0-63.7 changes in oxygen Randall transfer factor and et al. (1967) effectiveins of O exchange occur

15 Table 2 (continued).

Level of dissolved oxygen Temp Response to oxygen Species Size (C) POa-mm Hg ml O0/liter mg O/liter 7%SaIa. level Reference

t t 400-600 13.5 80 3.74 5.35 51.0 breathing amplitude Hughes and g and buccal pressure Saunders elevated (1970) . t approx. 300 10,15, 80 3.30-4.03 4.71-5.75 50.7-51.3 below this level blood Cameron g 20 is not fully satd. with (1971) oxygen 1-11 17.5 93.8 4.05 5.78 60 toxicity of zinc, lead, Lloyd g copper, phenols in- (1961) Screased markedly below this level Largemouth bass, juvenile 25 92.3-110.7 3.5-4.2 5-6 59.7-71.6 final (maximum sus- Dahlberg Mkropterus tained) swimming et al. (1968) salmoldes speed reduced below this level Ulvuell, 5-9 - - 2.1 3.0 - some avoidance Whitmore L/pomis cm behavior et al. (1960) macrochirus 1.1 1.5 - strong avoidance B. Marine nonanadromous species -4it perch, adults 11 80 3.19 4.56 50.8 blood ceases to be Webb and Macochilus vacca fully 02 saturated Brett below this level (1972) Dofish, 2.5-6.0 10 115 4.68 6.69 72.92 blood ceases to be Lenfant and Sq"as suckleyl kg fully 0O saturated Johansen below this level (1966) Dogtish, 150-600 12-14 80 3.12-2.95 4.46-4.20 50.8-51.0 Oxygen-dependent Hughes and Scylo inus g metabolism begins Umezawa caniculas below this level (1968a) Dragonet, 70-140 11-12 125 4.98-4.88 7.12-6.97 79.4 Oxygen-dependent Hughes and Cutieymus lyra" g metabolism below Umezawa this level (1968b) 100 3.97-3.90 5.67-5.58 63.5 altered heart rate Dragnet, 80-120 - 80 - - - increased ventilatory Hughes and Ca•Meymus lyrea muscle activity below Ballintijn this level (1968) a1sh5 - 11 150 5.98 8.54 95.2 blood ceases to be Hanson Ndretegus colliei fully Oa saturated (1967) below this level Atlantic cod, 1.14-2.33 5 158.2 7.14 10.20 100 any reduction in Saunders Gdus morsua kg ambient O0 level (1963) produces rise in ventilatory water flow C. Anadromous species Seilbead, Selsm gairdnert - see freshwater species Sockeyesalmon, 50 g 20-24 15$5.9-154.9 6.42-5.97 9.17-8.53 100 available oxygen level Brett Owerkynchus nerka appears to limit active (1964) metabolism and maximum swimming speed 1579 g 13 100 4.72 6.74 63.6 blood ceases to be Davis fully 0O saturated (1973) below this level 1.5-1.7 15 78.45 3.55 5.07 50 elevated blood and Randall kg buccal pressure and and Smith breathing rate increased (1967) Caoe salmon, 6.3-11 "summer - 3.15 4.5 - erratic avoidance Whitmore oerwhynchus cm tempera- behavior et al. (1960) kisutch tures" 5.1-14.8 12±1 130.8 6.3 9.0 83.1 below this level acute Hicks and cm mortality in kraft DeWitt pulpmill effluent (1971) mincreased to . Juvenile 10-20 1 57.7-155.9 7.93-6.42 11.33-9.17 100 reduction of 02 below Davis et al. saturation produced (1963) some lowering of maximum sustained swimming speed to t "9 20 155.9 6.42 9.17 100 as above Dahlberg 90 ot to 10 et al. (1968) 136-67.9 5.6-2.8 8.0-4.0 87.2-43.6 growth rate propor- Hermann tional to oxygen level (1958) with best growth at 8.0 ms/liter, lowest at 4.0 mg/liter

16 Table 2 (continued).

Level of dissolved oxygen Temp Response to oxygen Species Size (C) PO-mm Hg ml O/liter mg Oa/liter %7Satn. level Refermw

Chinook salmon, 6.3-11 "summer - 3.15 4.5 - marked avoidance of Whitmen Oncorhynchus cm temps" this level in summer et al. (11 Ishawytscha "fall - - 4.5 - little avoidance of temps" this level in fall " "* J uveniles 10-20 157.7-155.9 7.93-6.42 11.33-9.17 100 reduction of O Davis etd. below saturation pro- (1963) duced some lowering of maximal sustained swimming speed Atlantic salmon, 87-135 15 69.6 3.15 4.5 44.33 Salmon stop swimming Kuttysad Salmo salar g at a speed of 55 Saunden cm/s at 02 levels (1973) below this. Faster swimming requires more oxygen American shad, - - - 1.75-2.1 2.5-3.0 - threshold for migra- Chittenda Alosa sapidissima tion through (1973) polluted areas 2.8 4.0 - necessary for spawning areas D. Eggs and larvae Rainbow trout, 1+8 10+1 100 5.03 7.18 63.4 elevated heart and Holetoa larvae, day breathing rates below (1971) Salmo gairdnerl old this level. Brady- larvae cardia (heart rate slows) sets in at lower O0 levels Chum salmon eggs, early 10 13.9 .7 1 8.8 retarded development, Alderdice Oncorhynchus keta stage deformities, mortal- et al. (1953) eggs ity, respiratory Oa- dependence pre-hatch 10 >97.4 >4.9 > 7.0 > 61.8 oxygen level required eggs for normal development and non O2- dependent metabolism 5 day 8.0-8.2 22.2 1.17 1.67 14.07 critical oxygen level Wickett eggs for supply of oxygen (1954) demand and non 02- denendent metabhlism b (eyed) 3.6-4.9 > 60.3 > 3.5b > 5.0 > 38.1 b 85 day eggs Atlantic salmon, early 5.5 9.62 .53 0.76 6.09 As above Lindroth Salmo salar eggs (1942) near (from hatching 5 71.7 4.06 5.80 45.31 Wickett hatching 17 160.8 7.0 10.0 102.67 1954)) Atlantic salmon, eyed 10 43.14 2.17 3.1 27.36 critical 02 level for Hayes et al. Salmo salar hatching 10 98.83 4.97 7.1 62.67 supply of 02 demand (1951)(from and non O2 -depen- Wickett, dent metabolism 1954) Northern pike, from 15,19 > 5.18-5.66 > 2.16-2.35 > 3.35-3.09 > 33.0 necessary O2 level for Siefert Esox lucius fertilization proper hatching, et al. to survival and (1973) feeding development larvae MummichogL fertilization 20 101.2 3.15 4.5 64.9 reduced hatching at Voyer and Fundulus to this level compared Hennekey heteroclltus hatching to 7.5 mg/liter 0O (1972) Pacific cod, fertilization 3-5 > 2-3 oxygen level required Alderdica Gadus to for qptimal hatching and macrocephalus hatching at 157,o salinity Forresmt (1971) *European species - representatives of this family found in Canadian Atlantic waters. bCalculations based on 4 C. *Estuarine fish- calculations based on salinity of 30%,.

17 0 w II Zsc z s-

at4 VS)r5) I< ri) ys)NTS) hn)WkJ)

*E - iii, -, 1 4 a 7 a 9 -i WD -- DISSOLVED OXYGEN CONCENTRATION IN MILLIGRAMS PER LITER

Fig. 3. Growth of largemouth bass in relation to dissolved oxygen concentration (Stewart et al. (1967).

18 0%Ad%^ - U.500 r-

4 0.400 - aJI

>o--

3t 0.300 -

a W 0.200

F MENT-I MENT-2 oz o 0.100 MENT-4 MENT-5 41- MENT-6

l I & .,, I I . . . . I O= •.vvv ...... MA I 2 3 4 5 6 7 8 910 20 30 DISSOLVED OXYGEN CONCENTRATION IN MILLIGRAMS PER LITER

Fig. 4. Food consumption rate in relation to dissolved oxygen concentration (Stewart et al. 1967).

0 0 4 £ I 9 £ hI

O--- -O EXPERIMENT- I ------A EXPERIMENT- 2 0---0 EXPERIMENT-3 ----- Q EXPERIMENT-4 --- -0 EXPERIMENT-5 EXPERIMENT-6

DISSOLVED OXYGEN CONCENTRATION IN MILLIGRAMS PER LITER

Fig. 5. Food conversion ratio in relation to dissolved oxygen concentration. The food conversion ration of those fish that lost weight was considered to be 0, regardless of the weight loss (Stewart et al. 1967).

19 high concentrations of dissolved oxygen for either equal or unequal portions of 24 hours was markedly impaired.

Andrews et al. (1973) studied the influence of dissolved oxygen on the growth of channel catfish (Ictalurus punctatus). Growth rates of fish maintained at 36% air saturation were approximately half that of fish maintained at 60 and 100% (Table 3). Food conversion ratios were substantially poorer for groups maintained at the lower oxygen level. Blood hematocrit (the packed volume of red blood cells) , hemoglobin levels, and survival rates (100% in all groups) were not influenced by oxygen levels. Fish maintained at the two higher oxygen levels were active and fed vigorously, while those maintained at 36% saturation swam lethargically, fed poorly, and had reduced response to loud noises. Under ad libutum feeding, dissolved oxygen concentrations influenced catfish growth more than when a constant daily rate of 3% biomass was fed (Table 4). Herrmann et al. (1962) and Stewart et al. (1967) postulated that food efficiency was not substantially reduced until the oxygen level was low enough to reduce food consumption to a level where most of the nutrients were used to maintain the animal. Stress due to hypoxic conditions did not appear to enhance disease or parasite problems, because no mortalities occurred in either experiment.

Chronic effects of low dissolved oxygen concentrations on the fathead minnow were studied by Brungs (1971a). Fathead minnows were exposed to constant dissolved oxygen concentrations (1.0-5.0 rag/liter) for 11 months. The number of eggs produced per female was reduced at 2.0 mg/liter and no spawning occurred at 1.0 mg/liter (Table 5) . Fry growth was reduced significantly at all concentrations below the control (7.9 mg/liter). Fry survival was reduced at 4.0 ramg/liter and lower dissolved oxygen concentrations (Table 6). Eighteen percent of the survivors at 4.0 mg/liter were deformed. The time required for hatching was increased at succes- sively lower oxygen concentrations by as much as 50%, from 5.0 days under control conditions to 7.8 days at 2.0 rag/liter. No effect on percent hatch was observed. Fry growth, therefore, was the most sensitive indi-

20 Table 3. Experiment 1--Groups of catfish were maintained at three oxygen levels and fed at a constant rate of 3% of their biomass daily (Andrews et al. 1973).

Dissolved oxygen Feed level con- (% of air Average version Hema- Hemo- satu- gains (g feed/ tocrita globin" ration) (g) g gain) (%) (g/100 ml)

100 294a 1.23 33a 8.7a 60 287a 1.30 35a 9.9a 36 151b 1.78 32a 8.4a a Values within a given column followed by the same letter are not statistically different (P > 0.01, Duncan, 1965). b Feed conversion was calculated on the basis of the total amount of feed offered the fish during the experimental period. No attempt was made to determine what portion was actually consumed by the fish.

Table 4. Experiment 2--Groups of catfish were maintained at three oxygen levels and fed three times a day ad libitum (Andrews et al. 1973).

Feed Dissolved con- oxygen sumption Feed level (% of Conver- (% of air Average bio- sion Hema- satu- gaina mass/ (g feed/ tocrit" ration) (g) day) g gain) (%) 100 159a 3.3 1.12 37a 60 124b 2.9 1.18 34a 36 65c 2.1 1.47 35a * Values within a given column followed by the same letter are not statistically different (P > 0.01, Duncan, 1965).

21 Table 5. Spawning and egg production in the fathead minnow reared from fry at various oxygen concentrations (Brungs 1971a),

No. of Mean measured dissolved oxygen spawnings/ eggs/ eggs/ (mg/liter) females males female spawning female

1.06 4" 3' 0 0 0 1.99 5 6 5.4 171 925 3.00 6 4 10.0 176 1763 3.94 4 5 13.3 150 1992 4.91 7 5 16.3 146 2377 7.92 (Control) 8 6 10.6 127 1349

*Three of the females and two of the males were immature at the end of the test.

Table 6. Survival and growth during 30 days of fathead minnow fry spawned and reared at various dissolved oxygen concentrations (Brungs 1971a).

Mean measured Mean length dissolved oxygen No. No. fry Survival after 30 days* (mg/liter) replicates at start (%) (mm)b

2.02 3 70,38,65 0,0,0 - 3.08 4 70,42,94,91 10,5,3,5 8.7.9.3a 4.02 2 70,96 30,20 9.0,9.3 5.01 2 70,73 64,68 9.0,10.3 7.26 (Control) 2 70,70 50,50 12.2,11.1

*Thirty-day period includes the time required for hatching. bMean length of 143 newly hatched fry from a control dissolved oxygen concentration was 5.3 mm. eOnly two of the four replicates were continued for 30 days.

22 cator of sublethal effects of dissolved oxygen with fry survival nearly as sensitive. Reproduction was least sensitive.

A continuous 12-month exposure of fathead minnows to elevated water temperatures (26-34 C) showed that reproduction was more sensitive than survival (Table 7), growth, or egg hatchability in assessing the effect of temperature (Brungs 1971b). The number of eggs produced per female, the number of eggs per spawning, and the number of spawnings per female were each gradually reduced at successive temperatures above the control (23.5 C) (Table 8). No spawning or mortality occurred at 32 C, which was the lowest temperature where growth was apparently reduced. Male secondary sexual characteristics were less developed at 30 C than at lower temperatures. Brett (1944) demonstrated that acclimation to higher temperatures for the fathead minnow increased the upper lethal temperatures. He reported a maximum lethal temperature of 34 C. Hart (1947) estimated the upper incipient lethal temperatures to be 28.2 C after 2000 minutes for fish acclimated at 10 C, 31.7 C after 1800 minutes with acclimation at 20 C, and 33.2 C after 9000 minutes when fish were acclimated at 30 C.

Andrews and Stockney (1972) studied the interactions of feeding rates and environmental temperature on growth, food conversion, and body composition of channel catfish. Daily feeding rates were 2, 4, and 6% of total biomass of fish in each aquarium. The resulting data indicated that greater growth and lower conversions were obtained at 30 C than at either 26 or 34 C (Fig. 6 and 7), which agrees with West (1966) who found that the optimal temperature for growth was between 29-30 C, with the maximum food conversion efficiency at 28.9 C. Shrable et al. (1969) also suggested that the most rapid rate of digestion was at 26.6-29.4 C and Kilambi et al. (1970) found that the optimum condition for raising channel catfish was 32 C with a 14-hour photoperiod.

23 Table 7. Fry survival and length at three temperatures (90 days) 1 (Brungs 1971b).

Male Female Mean Number measured of fry Mean Mean- temperature at 45 Survival length Standard Range length Standard Range Chamber (C) days (%) (mm) deviation (mm) (mm) deviation ( mm)

4C 27.3 40 98 43(23)2 3.4 37-50 39(16) 2.5 35-43 5C 25.9 40 100 46(19) 2.9 40-51 41(21) 2.3 36-44 6C (Control) 21.5 40 100 44(26) 3.0 39-51 39(14) 2.1 35-43 I Spawning in 30 C chamber ceased before the fry survival and growth studies were initiated. 2.Numbers in parentheses indicate number of fish.

Table 8. Egg production data and percent of hatch at six temperatures (Brungs 1971b).

Mean measured Mean Mean Mean temperature Number of Number of spawnings/ Number eggs/ eggs/ Percentage Chamber (C) spawnings females female of eggs spawning female hatch

1A 33.7 0 0 0 0 0 0 0 1B 34.0 0 0 0 0 0 0 0 2A 31.9 0 7 0 0 0 0 0 2B 31.8 0 3 0 0 0 0 0 3A 29.8 21 7 3.0 1,414 67 202 67 3B 30.0 24 7 3.4 1,064 44 152 80 4A 27.8 109 7 15.6 13,209 121 1,887 90 4B 27.9 67 7 9.6 7,942 119 1,135 88 5A 26.1 150 8 18.8 25,131 168 3,590 95 5B 26.2 89 6 14.9 14,199 160 2,367 96 6A (Control) 23.5 155 6 25.8 29,570 191 4,928 87 6B ( Control) 23.5 144 8 18.0 26,983 187 3,373 94 1 All eggs were hatched in the "A" side of the test chambers.

24 FEEDING RATES 800 A 6 percent

* 4 percent 2 600

w0I- 4cqc 400 - 'U

I' 200

0 .

18 22 26 30 34

TEMPERATURE (C)

Fig. 6. The relationship between environmental temperature and average percentage gain in 12 weeks of channel batfish fingerlings fed at three feeding rates. Each point represents average values from duplicate aquaria each containing twenty fish (Andrews and Stickney 1972).

2 I-. 10

2 0 8

6 IU 0 0 0 4 Is.

"18 22 26 30 34

TEMPERATURE MC)

Fig. 7. The relationship between environmental temperature and food conversion ratio (g feed/g gain) for channel catfish fed at three feeding rates. Each point represents combined data from duplicate aquaria each containing twenty fish (Andrews and Stockney 1972).

25 Accliation

The phenomenon of acclimation may change the point at which a fish is affected by dissolved oxygen or temperature. A clear shift in the lethal level of oxygen in relation to acclimation was shown by Shepard (1955) for the eastern brook trout and for three warmwater species by Moss and Scott (1961). Shepard (1955) suggested that adjustments might be made in the oxygen carrying capacity of the blood, thus increasing its ability to extract oxygen from the water. Prosser et al. (1957) found this to be true for goldfish. MacLeod and Smith (1966) found that fathead minnows increased their hematocrit in response to low oxygen, thus making more hemlobin available for oxygen transport in the blood.

As well as resulting in blood oxygen capacity changes, acclimation can be behavioral in nature (Davis 1975). Considerable energy can be expended by a nonacclimated fish reacting behaviorally to low oxygen conditions. Acclimation lowers the magnitude of these reactions and enables energy conservation during oxygen stress. Any such ability to adapt to low oxygen should be useful, especially if the transition to a low oxygen regime is slow enough to enable acclimation to occur without severe physiological stress. However, this mechanism would be of little help to fish suddenly encountering low levels of oxygen. The ability to acclimate can be considered as a built-in safety factor for species encountering low oxygen conditions.

Acclimation temperature has a direct positive effect upon avoidance temperatures of species tested (Mathur et al. 1983). Fishes avoided temperatures higher than their acclimation temperatures (Fig. 8). The differences between avoidance and acclimation temperatures decreased as acclimation temperatures increased. Strong evidence of similarities rather than differences between populations and among species within a family was demonstrated. Moss and Scott (1961) studied the differences in survival between fish exposed to rapid drops in dissolved oxygen to a critically low point from near saturation (shock test) and fish exposed to dissolved oxygen declines gradually over a period of time (acclimation

26 L OU %MO

0. E 4)

#VI

0 > <

Acclimation Temp.(C)

Fig. 8. Plot of the published data on the relationship between avoidance temperature and acclimation temperatures of fishes within a family. The 90% confidence intervals of the individual predicted values are shown. 'Cherry et al. (1975, 1977); -, Muddy Run-Cono- wingo (Mathur et al. 1983).

27 test). The minimal dissolved oxygen survived by fish in acclimation tests was lower than that survived in shock tests at any given temperature (Table 9). The metabolic mechanisms of the species considered appear to be highly adaptive. In addition, data from the starved and obese groups of channel catfish used in shock tests at 30 C suggest that excessively fat fish are more sensitive to low levels of dissolved oxygen than are fish that have been normally fed.

Allen and Strawn (1971) noted that juvenile channel catfish, changed from lower to higher temperatures, were nearly reacclimated in 1-3 days, measured in terms of change in heat resistance. However, fish changed from high to low temperatures required 4-14 days to approach acclimation. In both changes, complete reacclimation required at least 12 days, indicating that tempering for a few hours would increase heat tolerance to same extent, but almost 1 day would be required to significantly increase it. Channel catfish could be held in cold water for 1-2 days with only a partial loss of heat tolerance. Fish exposed to fluctuating temperature should retain a relatively high heat tolerance.

Diana (1983) found that largemouth bass acclimated to a thermocycle exhibited no stress during rapid temperature changes, and the metabolic rate at each end point in temperature was similar to fish acclimated to that temperature. A major reason for stress responses to altered temperature found in earlier studies may be that the fish had been exposed only to constant temperatures in the lab. Diana's (1983) results make sense in that largemouth bass are considered temperature eurytherms (Magnuson et al. 1979) and regularly undergo seasonal temperature extremes from 1 to 32 C. Their response to temperature fluctuations is more variable than stenotherms. Venables et al. (1977) determined that bass were meta- bolically acclimated to a new constant temperature after only 3 days, much less than the usual 2-week acclimation period recommended for most fish (Beamish 1964).

Fish do not appear to handle fluctuations in oxygen as well as they do those in temperature. Exposure to cycling oxygen levels appeared to

28 Table 9. Critical levels of dissolved oxygen (p.p.m.) as determined in shock and acclimation tests (Moss and Scott 1961). Temperature (degrees centigrade) Type of test and species (degrees centigrade) 25 30 35

Shock tests Bluegill 0.75 1.00 1.23 Largemouth bass 0.92 1.19 1.40 Channel catfish 0.95 1.03 1.08 Acclimation tests Bluegill 0.70 0.80 0.90 Largemouth bass 0.83 0.83 1.23 Channel catfish 0.76 0.89 0.92

29 reduce the growth of largemouth bass juveniles at 26 C (Stewart et al. 1967). Similarly, Whitworth (1968) observed weight loss in brook trout exposed to daily fluctuations in oxygen.

Behavioral Responses

A number of other behavioral responses to hypoxia have been reported. Scherer (1971) described loss of normal avoidance of high light inten- sities (negative phototaxis) in walleye when dissolved oxygen fell to 2-4 mg/liter. It has also been shown that fish generally become more active in hypoxic water and attempt to move away from the low oxygen region (Randall 1970). Avoidance behavior has been reported for a number of species, although the reported dissolved oxygen threshold for a given response often varies considerably. It is not clear whether avoidance behavior in response to low oxygen constitutes a highly directed form of behavior. It may result simply from increased locomotor activity with more random movement, which is satisfied by discovery of improved oxygen conditions. Avoidance behavior in low oxygen would have survival value and the presence of this behavioral pattern suggests that fish periodi- cally may benefit from it. Implicit in a behavioral response to low oxygen would be sane means of detecting low oxygen concentrations. The physiological responses to hypoxia are rapid, consisting of circulatory and ventilatory changes in trout and tench within a few seconds of the onset of hypoxia (Eclancher 1972, Randall and Smith 1967). Such rapid responses suggest the presence of an oxygen receptor system on or near the gills.

Whitmore et al. (1960) investigated the avoidance reactions of salmonid and centrarchid fishes to low oxygen concentrations. Largemouth bass and bluegill (Lepomis macrochirus) markedly avoided concentrations near 1.5 mg/liter, but they showed little or no avoidance of the higher concentrations. Only bass showed any avoidance of concentrations near 4.5 mg/ liter. Avoidance by fish of water with low dissolved oxygen concentrations was shown not only by shorter excursions in distance and time into the experimental channels but also by fewer entries into the low oxygen

30 channels. Avoidance revealed by periodic counts of fish in the channels could be the result of gradually produced discomfort and stimulation at reduced oxygen concentrations. Shelford and Allee (1913) found that several fish species avoided water with low oxygen content in a gradient tank by turning back into water with more favorable concentrations.

Ironically, the mechanism necessary to move fish fran hypoxic areas, the locomotory system, is also influenced by low dissolved oxygen. Katz et al. (1959) reported that 6-cn bass could resist a water current of 25 cm/ second at 25 C in September at 2.0 mg/liter oxygen. However, in December at 15-17 C, they were unable to do so even when oxygen levels were 5.0 mg/ liter. Dahlburg et al. (1968) studied the influence of dissolved oxygen and carbon dioxide on the swimming performance of largemouth bass and coho salmon (Oncorhynchus kisutch). They concluded that concentrations of free carbon dioxide even above 40 mg/liter, which is rarely found in nature, had virtually no adverse effect on the swimning performance of largemouth bass (Fig. 9). The swimming speed of largemouth bass at low carbon dioxide concentrations decreased with dissolved oxygen concentrations below 5-6 mg/liter (Fig. 10). At concentrations above 6.0 mg/liter, the performance of bass apparently was independent of oxygen concentration.

Effects on Reproductive Success

The adult life stage of fish is not the only portion of their life cycle impacted by low dissolved oxygen. Developing fish eggs and larvae have a number of responses to low oxygen, including respiratory dependence, retarded growth, reduced yolk sac absorption, developmental deformities, and mortality. As developnent proceeds, oxygen requirements of eggs and larvae increase. Brungs (1971a) found larvae to be the most sensitive stage in the life cycle of the fathead minnow, when exposed to reduced oxygen levels of 1.0-5.0 mg/liter.

Carlson et al. (1974) studied the effects of lowered dissolved oxygen concentrations on channel catfish embryos and larvae. The effects of low oxygen concentrations on embryos and larvae were evident at all reduced

31 U w

w cc0 .J z

w nON) RE) TION) z I

DISSOLVED OXYGEN CONCENTRATION IN MG PER LITER Fig. 9. Mean final swimming speeds, expressed in L/sec, of largemouth bass at various concentrations of dissolved oxygen and carbon dioxide. The curve relating swimming speed -to oxygen concentration is the curve that was fitted to all data from tests at the low concentration of free carbon dioxide (probably <3 mg/liter) only, most of which (those from early tests) have not been plotted here. The stated free carbon dioxide levels of 48, 21, and 38 mg/liter are means of observed values for individual tests ranging from 44 to 55 mg/liter, 17 to 23 mg/liter, and 24 to 38 mg/liter, respectively (Dahlburg et al. 1968).

U 'M w6

9) ILw 5 -J Z 4 Q hiw w 3

z 2

ii 0A Ln DISSOLVED OXYGEN CONCENTRATION IN MG PER LITER Fig. 10. Relationship between the mean final swimming speed of largemouth bass, expressed in L/sec, and the dissolved oxygen concentration at nearly natural, low concentrations of carbon dioxide (<3 mg/liter) and temperatures near 25 C (Dahlburg et al. 1968).

32 concentrations tested at 25 C. Embryo pigmentation was progressively lighter as the oxygen concentration decreased. At reduced oxygen concentrations, hatching was prolonged by 0.5-2.0 days and feeding was delayed by 1-3 days. Growth of survivors was reduced at all lowered concentrations so that average lengths attained were 0.9-2.8 mm less than those of controls. Survival was also significantly less at 30 and 50% saturation. No hatching occurred at 20% saturation at 25 C. Only three fish survived at 30% saturation and 28 C. Channel catfish embryos and larvae were sensitive to all reductions in dissolved oxygen, although survival was only slightly affected at 60 and 70% saturation. Siefert and Spoor (1974), using similar testing methods, found that early-stage white suckers and walleye were not harmed at 50% saturation.

Dudley and Eipper al. (1975) investigated the survival of largemouth bass embryos at low dissolved oxygen concentrations. Oxygen concentrations that caused mortalities during hatching were 2.0, 2.1, and 2.8 mg/liter at incubation temperatures of 15, 20, and 25 C, respectively (Fig. 11), although some embryos developed and hatched at oxygen concentrations as low as 1.0, 1.1, and 1.3 mg/liter. The increasing embryo biomass requires more oxygen as it develops to the hatching point. Laurence (1969) reported that oxygen consumption of largemouth bass embryos incubated at 20 C increased from 0.06 microliters during the first 24 hours to 1.92 microliters during the last 24 hours of the 96-hour prehatching period. During hatching, largerouth bass embryos move vigorously (Carr 1942) . Laurence (1969) noted a possible peak in oxygen consumption during hatching. The increased oxygen consumption coincident with hatching of largemouth bass embryos undoubtedly increases oxygen needs above that which some conditions can supply.

Like fish, eggs also show respiratory dependence (Fry 1957). Alderdice and Brett (1957) reported a gradual increase in the dissolved oxygen requirements of chum salmon (Qncorhynchus kA) eggs as development progressed. Eggs at early stages of incubation required about 1 mg/liter oxygen, while those about to hatch required over 7 rag/liter. Eggs held at low oxygen tensions experienced reduced growth and retarded development. Deformities

33 EXPNM EXPE

--. 5 c a Survival at 90% --- * 20 C 0 Oxygen Saturation

--- 25C A

6 m.-- (I)

0 as_- SO- uc

f / / /0 / / / A / nA° / AA/ An A

Oxygen Concentration (mg/I)

Fig. 11. Relationships between embryo survival and oxygen concentration at three incubation temperatures. Each point represents the percent of 40 embryos (Experiment II) or 150 embryos (Experiment III) which survived to completion of hatching. Curves were fitted by eye to Experiment III data, Although at 20 C survival in Experiment II agreed with that found in Experi' ment III, survival was higher in Experiment III than in Experiment II at both 15 C and 25 C (Dudley and Eipper 1975).

34 in embryos exposed to hypoxia were observed, with mortality occurring at the stage when the circulatory system develops. Others have reported similar increased oxygen requirements of eggs as development proceeds (Lindroth 1942, Hayes 1949, Wickett 1954, Guilidov 1969).

Minimum Oxen Standard

Setting a minimum allowable summer dissolved oxygen concentration for water quality standards in warmwater systems would be extremely difficult. In his classic work, Ellis (1937) concluded that a minimum summer dissolved oxygen concentration of 5 mg/liter was necessary to support good, mixed fish faunas. Coble (1982) looked at fish populations in a Wisconsin river in relation to dissolved oxygen and found sport fishes and a variety of other species in water with less than 5 mg/liter oxygen. However, the quantitative measure, percent sport fish 2100 mn in samples, revealed that the proportion of a fish community composed of sport fishes was larger in waters, with higher levels of dissolved oxygen. Moreover, with a measure of dissolved oxygen concentration of daytime or averaged values, the level of 5 mg/liter could be identified as a point of departure between good and poor fish populations. Davis (1975) established critical oxygen and temperature criteria for Canadian aquatic life (Fig. 12). His criteria contained three levels to assess potential risk: Level A provides a high safeguard for very important aquatic populations; with Level B, there is a possibility of moderate risk to aquatic organisms with depressed oxygen concentrations; and with Level C, a large portion of a given population or community may be severely affected by low oxygen levels, especially on a chronic exposure basis.

35 A

4 100

0o- a

0 60

40 I ... Ow---*O -AA-I*0O SA. I 20-

a 5 10 15 20 ZS

SLASONAL TEMPERAITU€ MAXIMUM - C

**9091"eI **eg **~.*fP*.Oao s«O MI*CMI* N hi 0 O

* J 0*° S o * * e.. A

a W N mmm--- *

K a- 0 - - A A,-• Ft a 1% aA 4 f I S 1 Ti I 1 U 0L I StASONAL TIMPEOATULI MAXIMUM - C

Fig. 12. A, Oxygen criteria, expressed as seasonal minima in percent saturation, at various seasonal temperature maxima. Three levels of protection, A, B, and C, are given as defined in the text. Values used in derivation of the criteria are summarized in Table 10; B, Oxygen criteria, expressed as oxygen minima in mg 02/liter (ppm), at various seasonal temperature maxima. Three levels of protection, A, B, and C, are given as defined in the text. These values were calculated from the percentage saturation values illus- trated in (A) and summf4xrzed in Table 10 (Davis 1975),

36 LITERATURE CITED Alderdice, D. F., and J. R. Brett. 1957.. Some effects of kraft mill effluent on young Pacific salmon. J. Fish. Res. Board Can. 14:783- 795. Allen, K. O., and K. Strawn. 1971. Rate of acclimation of juvenile channel catfish, Ictalurus punctatus, to high temperatures. Trans. Am. Fish Soc. 100:665-671. *Andrews, J. W., T. Murai, and G. Gibbons. 1973. The influence of dissolved oxygen on the growth of channel catfish. Trans. Am. Fish. Soc. 102:835-838. *Andrews, J. W., and R. R. Stickney. 1972. Interactions of feeding rates and environmental temperature on growth, food conversion, and body composition of channel catfish. Trans. Am. Fish. Soc. 101:94-99. *Basu, S. P. 1959. Active respiration of fish in relation to ambient concentrations of oxygen and carbon dioxide. J. Fish. Res. Board Can. 16:175-212. *Beamish, F. W. H. 1964. Respiration of fishes with special emphasis on standard oxygen consumption. III. Influence of oxygen. Can. J. Zool. 42:355-366. Brett, J. R. 1944. Same lethal temperature relations of Algonquin Park fishes. Univ. Toronto Stud. Biol. Ser. 52. Publ. Ont. Fish. Res. Lab. 63:1-49. Brett, J. R. 1962. Sanme considerations in the study of respiratory metabolism in fish, particularly salmon. J. Fish. Res. Boad Can. 19: 1025-1038. Brown, A. L. 1971. Ecology of fresh water. Harvard Univ. Press, Cambridge, MA. *Brungs, W. A. 1971a. Chronic effects of low dissolved oxygen concentrations on the fathead minnow (Pimephales promelas). J. Fish. Res. Board Can. 28:1119-1123. *Brungs, W. A. 1971b. Chronic effects of constant elevated temperature on the fathead minnow (Pimephales promelas Rafinesque). Trans. Am. Fish. Soc. 100:659-664. Burdick, G. E., M. Lipschuitz, H. F. Dean, and E. F. Harris. 1954. Lethal oxygen concentrations for trout and smallmouth bass. N. Y. Fish. Game J. 1:84-97. Canton, S. P., L. D. Cline, R. A. Short, and J. V. Ward. 1984. The macroinvertebrates and fish of a Colorado stream during a period of fluctuating discharge. Freshw. Biol. 14:311-316.

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41 Mosevich, N. A. 1947. Winter ice conditions in the rivers of the Ob-Irtysh basin (Russian). Szv. vses. Inst. Ozern. rechn. ryb. Khoz. 25:1-56. Moss, D. D., and D. C. Scott. 1961. Dissolved oxygen requirements of three species of fish. Trans. Am. Fish. Soc. 90:377-393. Mossewitsch, N. A. 1961. Sauerstoffdefizit inder Flussen des West- sibirischen Tieflandes, seine Ursachen un Einflusse auf die aquatische Fauna. Verh. int. Verin. theor. Angew. Limnol. 14:447- 450. Prosser, C. L., J. M. Barr, C. Y. Lauer, and R. D. Pinc. 1957. Acclima- tion of goldfish to low concentrations of oxygen. Physiol. Zool. 30:137-141. Randall, D. J. 1970. Gas exchange in fish. Pages 253-292 in W. S. Hoar and D. J. Randall, eds. Fish physiology, vol. IV. Academic Press, New York, NY. Randall, D. J., and J. C. Smith. 1967. The regulation of cardiac activity in fish in a hypoxic environment. Physiol. Zool. 40:104-113. Reid, G. K. 1961. Ecology of inland waters and estuaries. Reinhold Publ. Corp., New York, NY. Sams, R. E., and K. R. Conover. 1969. Water quality and the migration of fall salmon in the lower Willamette River. Final Rep. Oregon Fish Comn. 58 p. Sawyer, F. E. 1950. Studies of the Skerry spinner. Salmon Trout Mag. 129:110-114. Scherer, E. 1971. Effects of oxygen depletion and of carbon dioxide buildup on the photic behavior of the walleye (Stizostedion vitreum). J. Fish. Res. Board Can. 28:1303-1307. *Schneller, M. V. 1955. Oxygen depletion in Salt Creek, Indiana. Invest. Ind. Lakes Streams 4:163-175. Shelford, V. E., and W. C. Allee. 1913. The reactions of fishes to gradients of dissolved atmospheric gases. J. Exp. Zool. 14:207-266. Shepard, M. P. 1955. Resistance and tolerance of young speckled trout (Salvelinus fontinalis) to oxygen lack, with special reference to low oxygen acclimation. J. Fish. Res. Board Can. 12:387-446. Shrable, J. B., 0. W. Tiemeier, and C. W. Deyae. 1969. Effects of temperature on rate of digestion by channel catfish. Prog. Fish-Cult. 31:131-138.

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