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Water flow requirements in the intensive production of Atlantic salmon (Salmo salar L.) fry: growth and oxygen consumption
Aquacultural Engineering 20 (1999) 1 – 15
Water flow requirements in the intensive production of Atlantic salmon (Salmo salar L.) fry: growth and oxygen consumption Sveinung Fivelstad a,*, Asbjørn Bergheim b, Hilde Kløften a, Reidun Haugen c, Torild Lohne c, Anne Berit Olsen d a
Laboratory of En6ironment, Bergen College of Engineering, Nyga˚rdsgaten 112, PB 6030, N-5020 Bergen, Norway b Rogaland Research, P.O. Box 2503, Ullandhaug, N-4004 Sta6anger, Norway c Sæ6areid Fish Farm, 5674 Sæ6areid, Norway d National Veterinary Institute Bergen, Minde Alle, P.O. BOX 40, N-5032 Minde, Norway Received 2 July 1998; accepted 15 December 1998
Abstract Atlantic salmon (Salmo salar L.) fry (1– 10 g) were exposed to three water flow rates: 1.4 (control), 1.0 (medium) and 0.7 l kg − 1 min − 1 (low). There were four replicate tanks in each group. Alkalinity was low (0.03–0.04 mM). Oxygen was added to the inlet water to maintain discharge water oxygen concentration higher than 7 mg l − 1, at 16°C. The mean weight of fish in the low water flow group was significantly lower than in the control flow group after 2 months. No significant differences in mean fish length and condition factor between groups were found. There was no significant difference in the frequency of occurrence of gill lesions among the groups. Mortality was low in all groups (0.3 – 0.4%). In the majority of tanks (nine of 12), oxygen consumption rates decreased significantly as the mean fish size increased. An overall range of 5–12 mg O2 kg − 1 min − 1 was observed. There were no significant differences between the b-values (weight exponent: log oxygen consumption versus log body weight) of the three groups. The range of the weight exponents for the combined groups (between −0.19 and −0.23) was narrower than that of the individual tanks (between − 0.12 and −0.27). The wide range in the individual tanks may be a result of relatively few oxygen measurements. No significant differences were found in the oxygen consumption levels of the three groups. The oxygen consumption rate was however higher than predicted by earlier oxygen consumption models. The mathematical corrections of oxygen consump* Corresponding author. Tel.: +47-55587500; fax: +47-55587790. E-mail address: [email protected] (S. Fivelstad) 0144-8609/99/$ - see front matter © 1999 Elsevier Science B.V. All rights reserved. PII: S 0 1 4 4 - 8 6 0 9 ( 9 9 ) 0 0 0 0 2 - 3
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tion rates due to reaeration of oxygen were generally within 9 3% of the measured oxygen consumption rates (in all tanks). Further studies are needed both to quantify water flow requirements and oxygen consumption rates for Atlantic salmon fry. © 1999 Elsevier Science B.V. All rights reserved. Keywords: Atlantic salmon fry; Water flow; Oxygen consumption models; Oxygenation; Growth
1. Introduction
1.1. Water flow The water flow requirement is biologically and economically important in landbased systems since it is one of the limiting factors for fish production. In Norwegian hatcheries, elevated temperature is used to increase the growth rates of Atlantic salmon (Salmo salar L.), especially from startfeeding and until the fry reach 10 g. The oxygen consumption rate of the fry is high and oxygen gas is added to the inlet water to decrease the demand of heated water. Quantitatively the water flow requirement may be expressed as (Fivelstad, 1988): q0 =
M DOin −DOout
(1)
where q0 is the specific water flow requirement (l kg − 1 min − 1), M is the oxygen consumption rate (mg kg − 1 min − 1) and DOin and DOout is the oxygen concentration (mg l − 1) in the inlet water and at the discharge, respectively. The water flow requirement (q0) is the inverse of loading (kg of fish divided by flow to rearing unit in liters per min (kg l − 1 min − 1) (Colt and Orwics, 1991)). This equation can also be stated as: q0 =
M d
(2)
where d is the difference in dissolved oxygen between the inlet water and the discharge (DOin −DOout). The difference (d) expresses the relationship between the oxygen consumption rate and the specific water flow: d=
M q0
(3)
The difference (d) is a measure of the production intensity of a fish farm. The specific water flow can be reduced when the oxygen consumption rate is reduced to operate a fish farm under constant values for d. When the water flow is reduced there is a build up of both carbon dioxide and total ammonia, and pH is reduced. The increase in carbon dioxide and the reduction in pH is directly related to increased values for d (Colt and Orwics, 1991). The aim of the present experiment was to study limiting values for the water flow requirement for Atlantic salmon fry under intensive hatchery production. The difference (d) was considered to be an important parameter in the experiment.
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1.2. Oxygen consumption Intensification of production often influences the metabolism of the fish stock. Factors such as water temperature, feeding, photo-period, oxygen level and biological parameters such as stress, will influence the metabolic rate (Jobling, 1993). Oxygen consumption rate models have been developed for post-smolt Atlantic salmon in commercial-scale tanks (Fivelstad and Smith, 1991; Forsberg, 1994), and in a tunnel respirometer (Grøttum and Sigholt, 1998). Bergheim et al. (1991) have described the oxygen consumption of parr-smolt (individual size 27–67 g) in a commercial-scale hatchery. There is however a lack of knowledge regarding the oxygen consumption rates of Atlantic salmon fry under intensive hatchery conditions. This paper describes the oxygen consumption of Atlantic salmon fry and fingerlings (up to 10 g) at high water temperature and three different water flow rates (l kg − 1 min − 1). The specific oxygen consumption rate is one of the important parameters determining the water flow requirement for fish.
2. Materials and methods
2.1. Experimental protocol and equipment The experiment was performed in an indoor hatchery, at Sævareid Fish Farm, during a period of 2 months. The water was soft (conductivity 20–25 mS cm − 1; calcium 0.5 – 0.7 mg l − 1; total alkalinity 0.03–0.04 mM) and the aluminium concentration was low (less than 5 mg l − 1 labile aluminium). The experimental set-up comprised 12 fish tanks, representing four replicates of the control (high water flow) and two test groups (medium and low water flow) (Table 1). Table 1 Experimental conditions for the three groupsa Parameters
Control group
Medium water flow group
Low water flow group
Specific water flow (l kg−1 min−1)
1.4 9 0.48 (220) 0.4–2.3 12.6 91.0 (221) 6.2 91.9 (137) 2.5–11.0
1.090.31 (220) 0.4–1.5 11.3 91.0 (221) 7.6 9 2.0 (137) 2.7–12.6
0.7 9 0.24 (220) 0.3–1.2 8.290.7 (221) 10.4 9 2.6 (142) 4.3–15.6
5.6 (148) 5.0–6.0
5.5 (148) 4.9–5.9
5.5 (148) 4.8–5.9
Oxygen at the discharge (mg l−1) Difference in dissolved oxygen between the inlet water and the discharge (mg l−1) pH at the discharge
a Mean (9 S.D.) and ranges (number of measurements in parenthesis). Mean oxygen concentration in the inlet water was 19 mg l−1 for all groups.
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The freshwater influent was heated to 15–16°C by a heat pump, and then aerated in a packed column aerator system. Each tank (volume: 2000 l) was stocked with 12 000–16 000 fry acclimated to the hatchery conditions since the eyed-egg stage. The fry were exposed to continuous light (24 h day − 1) and were fed ‘dry’ food (‘Felleskjøpet’ nos. 1.2 and 2.0) by ‘Aquaprodukter’ automatic feeders every 8 min on a 24-h basis. Fish density at the start of the experiment was 6–8 kg m3 and at the end 60 – 80 kg m3. During the experiment water flow (l min − 1) and the oxygen level in the inlet water was adjusted to meet the increased oxygen consumption in the tanks. Oxygen was added to the inlet water by an ‘Oxygenator’ from Hydrogas.
2.2. Water quality measurements The inlet and outlet oxygen concentrations were measured by an Oxyguard dissolved oxygen meter (Handy Mk 1), and pH was measured by Radiometer pH meter PHM-80. The conductivity was measured by a YSI S-C-T meter (Model 33), and the total gas pressure was measured by a Weiss saturometer Model ES-2. Oxygen concentrations and pH were measured at least once a day. Water flow was determined by measuring the time taken to fill a 10-l container. Water temperature, recorded daily, was 15 – 16°C.
2.3. Growth and oxygen consumption The weight and length of individual fish (75 in each tank, 300 in each group) were measured at the beginning of exposure (day 0) and after 28 and 56 days of exposure. In addition, mean weights of 100 fish were measured after 16 and 43 days. The condition factor, CF, was calculated from the formula: CF= 100 W/L 3
(4)
where W is the wet weight (g) of each fish and L is fish length (cm). The specific growth rate (SGR as% wt. day − 1) was calculated from the equation: SGR=(ln W2 −ln W1)/(t2 − t1) · 100
(5)
where W1 and W2 are mean fish weights at the sample times t1 and t2, respectively. Oxygen consumption rates (M% as mg kg − 1 min − 1) were initially calculated from measurements of oxygen concentrations in the inlet and discharge waters, and the total biomass in the tanks: M%= [(Cinlet −Cdischarge)]Q/B
(6) −1
−1
where C is oxygen concentrations (mg l ), Q is the flow (l min ) and B is fish biomass (kg). In order to correct for the oxygen diffusion across the water surface, the diffusion rate (rdiff) was estimated for all tanks (Metcalf and Eddy, Inc., 1991): rdiff =K(Csat −C)
(7)
where K is the surface reaeration rate, Csat is the saturation concentration of oxygen and C is the actual oxygen concentration in the tank.
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The corrected oxygen consumption rates (M as mg kg − 1 min − 1) were finally calculated: M = [(Cinlet −Cdischarge)Q]/B + rdiffV/B
(8)
where V is tank volume (l). The relationship between oxygen consumption rate (M as mg kg − 1 min − 1) and fish size was estimated using the function (Brett and Groves, 1979): M =a·BW b
(9)
where BW is the individual fish weight (g), a is a constant and b is the fish weight factor.
2.4. Histomorphological examination Tissue specimens for histomorphological examination were collected on days 0 and 56. A total of 12 fish from each group were killed by severance of the spinal cord just behind the opercula. Immediately after sacrifice, gill, mid and hind kidneys were fixed in 10% neutral buffered formalin. The tissues were embedded in paraffin wax. Sections were cut at 3 –5-mm thickness and routinely stained with haematoxylin and eosin (H&E). The sections were studied blind, i.e. with no knowledge of the group to which the fish belonged. Gills were examined for histomorphological lesions in general. Kidneys were examined for mineral deposits, i.e. nephrocalsinosis.
2.5. Statistical analyses Statistical analyses were performed using Statgraphics from STSC. Multiple comparisons among pairs of means were performed by one-way ANOVA combined with the Tukey test method (Sokal and Rohlf, 1981; Fowler and Cohen, 1990). The significance of differences between regression lines was examined by a t-test (Fowler and Cohen, 1990). The regression analyses (log M vs. log BW) were based on recorded data from fish sizes down to about 2 g (i.e. seven to nine initial values were excluded from each tank). The reason for excluding these data was that pH was in the range 4.8 – 5.5 during the first 9 days of the experiment. In addition all tanks were treated with formalin on day 3.
3. Results
3.1. Water flow, growth, histomorphological examination and mortality Fish growth results are shown in Table 2. No clear differences in the mean values of the growth parameters measured (weight, length and condition factor) were determined between the high (control) and medium water flow groups. Mean weight for the low water flow group was however slightly, and significantly reduced,
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Table 2 Weight, length and condition factor during the experimenta Parameters
Day
Control group
Medium group
Low group
Weight (g)
0 28 56 0–56
1.319 0.020 (300) 3.859 0.085 (300) 11.5490.306 (298) 3.89
1.44 90.023 (300) 4.01 90.089 (300) 12.0290.288 (295) 3.79
1.35 9 0.025 (300) 3.41 90.076 (300) 10.36 90.249* (298) 3.64
0 28 56 0 28 56 0–56
4.9490.024 6.71 9 0.043 9.2590.080 1.0790.006 1.22 9 0.005 1.3690.006 0.36
5.06 9 0.024 6.79 9 0.045 9.39 9 0.075 1.09 9 0.008 1.22 90.005 1.37 90.005 0.28
4.95 90.028 6.50 90.042 9.00 90.071 1.08 90.006 1.19 90.007 1.34 90.006 0.44
Specific growth rate (% day−1) Length (cm)
Condition factor
Mortality (%)
(300) (300) (298) (300) (300) (298)
(300) (300) (295) (300) (300) (295)
(300) (300) (298) (300) (300) (298)
Mean 9S.E., number of measurements in parenthesis. * PB0.05.
a
when compared to the control group at the end of the experiment. Mean length and condition factor of the low group was slightly, although not significantly, reduced compared to the control group. There was no significant difference in the prevalence and quality of gill lesions among the groups. Nephrocalsinosis was not observed in any of the groups. Mortality was low in all three groups during the study period, at 0.3 – 0.4%.
3.2. Oxygen consumption: daily 6ariation Oxygen consumption data covering the whole study period are shown from three fish tanks representing the three water flow levels (Fig. 1a,b,c). In all groups, high oxygen consumption rate fluctuations were observed during the first 2 weeks of recording. The high water flow group in particular demonstrated extreme variations at this stage. The lowest consumption rates observed during the first days coincided with reduced tank outlet pH levels (pH 4.8–5.5) due to acidification of the inlet water. Subsequently, consumption rates gradually decreased with increasing fish size (2–9 g). An overall range of 5 – 12 mg O2 kg − 1 min − 1 was observed.
3.3. Oxygen consumption models Table 3 shows the results from the linear regression analyses of oxygen consumption changes with fish weight, grouped in terms of both individual tanks and the three water flow groups.
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Fig. 1. Measured Atlantic salmon fry oxygen consumption rates in three representative tanks supplied with different levels of water flow. In each tank seven to nine initial values are excluded from statistical analysis (Table 2, Fig. 2). (a) ‘Control’ (high) flow: tank no. 233; (b) ‘medium’ flow: tank no. 230; (c) ‘low’ flow: tank no. 229.
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Fig. 1. (Continued)
3.3.1. Low water flow group No significant differences were found in a- or b-values between the four tanks (P\0.05). In the four tanks, the oxygen consumption rates decreased significantly (PB0.01) as the mean fish size increased. Oxygen consumption data for these tanks were therefore combined. 3.3.2. Medium water flow group In one tank, a significant positive relationship between oxygen consumption and mean fish weight (b = 0.17) was found. The a-value for this tank was significantly different from the other three tanks so these results were excluded from the combined data for the medium group. Oxygen consumption rates in the three other tanks decreased significantly (P B 0.01) with increased mean fish size. Oxygen consumption data from these three tanks were combined. 3.3.3. High water flow group (control) Oxygen consumption rates decreased significantly (PB 0.01) with increased mean fish size in only two of four tanks. The a and b-values from these two tanks were not significantly different from each other. The oxygen consumption data for these two tanks were therefore combined. 3.3.4. Among group comparisons No significant differences were found in the a- (oxygen consumption levels) or b-values (slopes) among the combined groups. Therefore, the oxygen consumption
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Table 3 The relationship between oxygen consumption (M, mg O2 kg−1 min−1) and fish size (BW, g) in 12 tanks stocked with salmon fry at Sævareid Fish Farma Tank no.
225 228 229 234 224 227 230 235 223 226 232 233 All All, T227 All (T223–T226) Total
Water flow groups
Low
Medium
Control (high)
Low Medium Control (high) Low+medium
Log M= log a+b log BW
Log a (S.E.)
b (S.E.)
1.04 0.98 1.02 1.02 1.00 0.80 1.07 0.99 1.00 0.98 1.04 1.07 1.02 1.03 1.06 1.02
−0.151 (0.070) −0.225 (0.043)** −0.266 (0.042)** −0.222 (0.042)** −0.191 (0.038)** 0.177 (0.072)** −0.256 (0.029)** −0.122 (0.054)* −0.076 (0.042) −0.049 (0.085) −0.159 (0.033)** −0.207 (0.068)** −0.222 (0.035)** −0.199 (0.025)** −0.187 (0.040)** −0.198 (0.021)**
(0.042)** (0.026)** (0.026)** (0.027)** (0.026)** (0.048)** (0.019)** (0.037)** (0.038)** (0.057)** (0.022)** (0.043)** (0.021)** (0.017)** (0.026)** (0.014)**
R2
P-level
0.18 (23) 0.60 (21) 0.64 (25) 0.61 (20) 0.57 (21) 0.24 (21) 0.79 (22) 0.21 (21) 0.07 (25) 0.06 (21) 0.61 (17) 0.33 (22) 0.32 (89) 0.50 (64) 0.37 (39) 0.31(192)
B0.05 B0.01 B0.01 B0.01 B0.01 B0.01 B0.01 B0.05 B0.01 B0.01 B0.01 B0.01 B0.01 B0.01
+ high a Stable temperature (15.5–16.5°C), three levels of water flow (low, medium, control). Function used: M =a·BW b (Brett and Groves, 1979), where a is a constant and b is the weight factor (S.E.= standard error). * PB0.05. ** PB0.01.
data were combined in a common model for the three groups. Fig. 2 shows the distributions of log M (oxygen consumption rate) with respect to log BW (fish size) for the combined groups. It should be noted that the mathematical corrections of oxygen consumption rates due to reaeration of oxygen, generally were within 9 3% of the measured oxygen consumption rates (in all tanks).
4. Discussion
4.1. Water quality Water temperature was constant, and the same in all tanks. Though pH was lower than the optimum level for salmonids, there was only a slight difference in mean pH between the three groups. The safe level for low pH for freshwater fish is 5.0 (Alabaster and Lloyd, 1982) assuming no other synergistic factors. The low mortality rate in all groups indicates that pH was nevertheless within acceptable
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limits. The aluminium concentration of the water supply to Sævareid Fish Farm is very low. Gills are sensitive to pH/Al stress (Smith and Haines, 1995; Jagoe and Haines, 1997), but no gill damage was observed during the study. Growth rates achieved in the present study (3.6 – 3.9% per day at 16°C) were slightly lower than rates reported in growth tables (Austreng et al., 1987) for Atlantic salmon between 0.6 and 10 g (4.1 – 4.2% per day at 16°C). The experiment was run as a part of the full-scale production and it was not possible to regulate the oxygen concentration in the inlet water independently for the three groups. As a consequence the mean oxygen saturation was 125, 112 and 83% for the control group, the medium group and the low group, respectively. In addition, there was day to day variation in the oxygen saturation for the different groups. As a result of the oxygen saturation, single sets of measurements showed total gas pressure to be 108% (15.5 mg l − 1 oxygen), 105% (13.1 mg l − 1 oxygen) and 100% (9.4 mg l − 1 oxygen) for the control group, the medium group and the low group, respectively. The percent saturation of nitrogen (+ argon) was 95, 98 and 100% for the control group, the medium group and the low group, respectively. There is not enough background information in the literature to decide whether these differences in oxygen saturation may influence the growth rate of Atlantic salmon fry. Periodic decreases of oxygen levels from saturation to levels below saturation had even in some experiments a positive effect on the growth of fish (Konstantinov et al., 1998). In the present experiment the dissolved oxygen concen-
Fig. 2. The relationship between oxygen consumption rates and fish size (log M versus log BW) applying the combined model (control flow + medium flow+ low flow) for Atlantic salmon fry (n =192). The two pairs of dotted lines represent the 95% confidence (closest to the regression line) and prediction limits (farthest away from the regression line). Model estimates in Table 2.
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tration in the effluent from all tanks was maintained above 7 mg l − 1 (71% air saturation) during the experimental period. At this level, oxygen concentration is generally not considered to be a growth limiting factor (Rosseland et al., 1990). It should be noted that no significant differences were found in the oxygen consumption rates of the three different groups. It has been shown that reduced water flow may have detrimental effects on Atlantic salmon smolts due to increased CO2 concentrations and reduced pH (Fivelstad and Binde, 1994), if the difference in dissolved oxygen concentration between the tank inlet and outlet water is in the range 6–10 mg l − 1. In the present experiment, fish in the low water flow group achieved a slightly, yet significantly, lower weight than the other groups. For this group, the difference in oxygen concentration between the inlet and outlet water was in the range 4–16 mg l − 1 (Table 1). The effects on smolts (growth reduction, gill damages, etc.) observed by Fivelstad and Binde (1994) were however more severe than the effects on fry in the present experiment. Using the model proposed by Colt and Orwics (1991) mean free carbon dioxide concentration for the low water flow group during the present experiment, was predicted to be about 15 mg l − 1. Results from experiments performed on Atlantic salmon smolts during spring 1996 and 1997, in neutral water (pH 6.5), indicated that the maximum safe level for carbon dioxide is lower than 20 mg l − 1 (Fivelstad et al., in prep.). Carbon dioxide is also more toxic at lower pH (Alabaster and Lloyd, 1982). Thus, higher carbon dioxide concentrations combined with low pH may have resulted in a slightly lower growth rate for the low water flow group compared with the other two groups. Generally, a higher alkalinity is favourable when the water flow is reduced since it determines the ability of the water to buffer changes in pH resulting from carbon dioxide accumulation (Colt and Orwics, 1991; Ewing et al., 1994). It should be noted that no negative effects were found on chinook salmon smolts (Oncorhynchus tshawytscha) when supplemental oxygen was used at higher water alkalinities (Ewing et al., 1994). The present investigation clearly indicated that water flow (l kg − 1 min − 1) influences the growth rate of Atlantic salmon fry at low alkalinity. Further studies are needed to quantify water flow requirements for Atlantic salmon fry at other alkalinity levels and at other temperatures than presented here.
4.2. Oxygen consumption In the present study the method used to determine the weight exponent (b) was based on log-log transformation prior to linear regression. However, a so-called ‘non-linear iterative least-square fit’ (Glass, 1969) might in certain cases, especially when the number of measurements is low, represent a somewhat better fitness than the log-log transformation method. The residuals plots for each fish tank were found to be uniformally spread around zero (data exhibiting homoscedasticity) indicating an accurate description of the relationship between oxygen consumption and body weight (Zar, 1996). In intensive hatchery production, the oxygen consumption rate may be influenced by numerous parameters. Consequently, it was not surprising that three out of the 12 involved tanks did not conform to the expected
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trend regarding oxygen consumption versus fish size. When this relationship (oxygen consumption vs. fish size) is masked by environmental factors, it is not possible to include the data in further statistical analyses. As a result, mathematical models for the oxygen consumption rate may not always apply to hatchery conditions. In a review, Forsberg (1994) presented a weight exponent (b) range from −0.14 to −0.28 for post-smolt Atlantic salmon. No weight exponents for Atlantic salmon fingerlings have though been located in the literature. In most tanks the relationship between oxygen consumption and fish size (weight exponent, b, between − 0.12 and −0.27) was within the range reported for various salmonid species. The range of the weight exponents for the combined groups (between −0.19 and −0.23) was narrower than that of the individual tanks (between − 0.12 and − 0.27). The wide range in the individual tanks may be a result of relatively few oxygen measurements. The weight exponent for the combined groups (− 0.20) corresponds closely to the weight exponent found by Liao (1971), indicating that the weight exponent converges against given values when the number of measurements is high. The wide variation reported in the literature may partly be related to a low number of measurements. Despite the significant relationship between oxygen consumption rate and fish size, the presented models (Table 2) only explained 32–50% of the total variation in the data. In earlier studies, factors such as daily ration (Haskell, 1955; Willoughby, 1968; Brett, 1976), activity (Brett, 1962; Beamish and Dickie, 1967; Albrecht, 1974), and stress level (Smart, 1981) have been found to influence metabolic rate. Activity and feeding level (appetite; amount of food ingested) may be important parameters contributing to the total variation in the data. Stress associated with daily husbandry routines may also be important. The metabolic rate related to the activity level can be divided into expenditure components, such as swimming against a given current, feeding behaviour and random activity. Swimming against a given current velocity may be the most important and easy component to quantify, since it is related to the stream velocity. This velocity does however vary considerably within any tank (Cripps and Poxton, 1992), so defining an average value may be difficult or unrealistic. The sparse current speed measurements in the present study indicated a relatively stable current velocity in all tanks of 1 – 1.5 BL s − 1. The consumption of food by animals results in an increase in metabolic rate. This increase is known as the specific dynamic action (SDA) of the food (Warren and Davies, 1967). The relationship between the feeding level and metabolic rate is based on the SDA effect and is easy to quantify if all the food is ingested and the feeding rate corresponds closely to the specific growth rate of the fish. However, diurnal variation in appetite (and amount of food wastes) may mask such a direct relationship. By re-analysing published data on rainbow trout (Onchoryncus mykiss) fry, Post and Lee (1996) detected a biphasic metabolism relationship with respect to fish size, not unlike the progress of this relationship found over the whole growth period at Sævareid Fish Farm (Fig. 1). Post and Lee (1996) proposed that the metabolic
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Fig. 3. Comparison between oxygen consumption rates (mg kg − 1 min − 1) as a function of fish size (g) using the model of Liao (1971) and the combined model (control flow +medium flow +low flow) obtained in the present investigation.
ontogeny may be explained by physiological changes (development of muscle mass) and changes in the surface area to volume ratio of the respiratory organs during the early life stages. No measurements of oxygen consumption of Atlantic salmon fry at such a high, stable temperature have previously been reported. Oxygen consumption may not increase exponentially with increased temperature (Forsberg, 1994). The Q10 value, used to express the relative change in oxygen consumption with water temperature changes (relative to consumption at 10°C), was found to decrease with increasing temperature, for Atlantic salmon parr of 5–27 g (Maxime et al., 1989): 3.5 at 9–13°C; 2.9 at 13 – 15°C; and 1.5 at 15–19°C (routine metabolism). The oxygen consumption reported by Maxime et al. (1989), corrected for fish size and temperature (11.5 g, 14.3°C), was however about 50% lower than that measured at Sævareid Fish Farm. Our presented oxygen consumption rates were 1.5–1.6 times higher than calculated by the oxygen consumption model estimated by Liao (1971) for Pacific salmon (Fig. 3). Since the proposed model (M = a·BW b) does not account for the activity level or the feeding level, the residuals must be expected to be considerable. The model for the different water flow groups did however explain 32–50% of the total variation in the data, which may be considered as good for data obtained from a full-scale production unit. The combined model (low group+ medium group+ control group) explained 31% of the total variation in the data. Further studies are needed to study oxygen consumption rates for Atlantic salmon fry at other temperatures than presented here.
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Acknowledgements Appreciation is expressed to all the staff at Sævareid Fish Farm for their co-operation. The project was partly financed by the Norwegian Research Council. Dr Simon J. Cripps (Rogaland Research) kindly gave advice on language and structure of the manuscript.
References Alabaster, J.S., Lloyd, R., 1982. Water Quality Criteria for Freshwater Fish. Butterworths, London Food and Agriculture Organization of the United Nations. Albrecht, M.L., 1974. Der Sauerstoffverbrauch der Regenbogenforelle (Salmo gairdneri ). Z. Binnenfischerei DDR 21, 53–61. ˚ sga˚rd, T., 1987. Growth rate estimates for cultured Atlantic salmon and Austreng, E., Storebakken, S., A rainbow trout. Aquaculture 60, 157–160. Beamish, F.W.H., Dickie, L.M., 1967. Metabolism and biological production of fish. In: Gerking, S.D. (Ed.), The Biological Basis of Freshwater Fish Production. Blackwell, Oxford, pp. 215 – 242. Bergheim, A., Seymour, E.A., Sanni, S., Tyvold, T., Fivelstad, S., 1991. Measurements of oxygen consumption and ammonia excretion of Atlantic salmon (Salmo salar L.) in commercial-scale, single-pass freshwater and seawater landbased culture systems. Aquacult. Eng. 10, 251 – 267. Brett, J.R., 1962. The swimming energetics of salmon. Scientific Am. 2, 80 – 85. Brett, J.R., 1976. Feeding metabolic rates of young sockeye salmon, Onchorhynchus nerka, in relation to ration level and temperature. Fish. Mar. Serv. Tech. Rep. 675, 1 – 43. Brett, J.R., Groves, T.D.D., 1979. Physiological energetics. In: Hoar, W.S., Randall, D.J., Brett, J.R. (Eds.), Fish Physiology, vol. VIII. Academic Press, New York, pp. 279 – 352. Colt, J., Orwics, K., 1991. Modeling production capacity of aquatic culture systems under freshwater conditions. Aquacult. Eng. 10, 1–29. Cripps, S.J., Poxton, M.G., 1992. A review of the design and performance of tanks relevant to flatfish culture. Aquacult. Eng. 11, 71–91. Ewing, R.D., Ewing, S.K., Sheahan, J.E., 1994. Willamette oxygen consumption studies. US Department of Energy, Bonneville Power Administration Environment, Fish and Wildlife, P.O. Box 3621, Portland, OR, pp. 1–167. Fivelstad, S., 1988. Waterflow requirements for salmonids in single-pass and semi-closed land-based seawater and freshwater systems. Aquacult. Eng. 7, 183 – 200. Fivelstad, S., Smith, M.J., 1991. The oxygen consumption rate of Atlantic salmon (Salmo salar L.) reared in single pass landbased seawater system. Aquacult. Eng. 10, 227 – 235. Fivelstad, S., Binde, M., 1994. Effects of reduced waterflow (increased loading) in soft water on Atlantic salmon smolts (Salmo salar L.) while maintaining oxygen at constant level by oxygenation of the inlet water. Aquacult. Eng. 13, 211235. Fivelstad, S., Olsen, A.B., Kløften, H., Ski, H.N., Stefansson, S. Effects of carbon dioxide on Atlantic salmon smolts (Salmo salar L.) at constant pH in bicarbonate rich fresh water. In prep. Forsberg, O.I., 1994. Modelling oxygen consumption rates of post-smolt Atlantic salmon in commercialscale, land-based farms. Aquacult. Int. 2, 180 – 196. Fowler, J., Cohen, L., 1990. Practical Statistics for Field Biology. Wiley, New York 229 pp. Glass, N.R., 1969. Discussion of calculation of power function with special reference to respirometer metabolism in fish. J. Fish. Res. Board Can. 26, 2643 – 2650. Grøttum, J.A., Sigholt, T., 1998. A model for oxygen consumption of Atlantic salmon (Salmo salar L.) based on measurements of individual fish in a tunnel respirometer. Aquacult. Eng. 17 (4), 241 – 251. Haskell, D.C., 1955. Weight of fish per cubic foot of water in hatchery troughs and ponds. Prog. Fish. Cult. July, 117–118.
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Jagoe, C.H., Haines, T.A., 1997. Changes in gill morphology of Atlantic salmon (Salmo salar) smolts due to addition of acid and aluminum to stream water. Environ. Pollut. 97, 137 – 146. Jobling, M., 1993. Bioenergetics: feed intake and energy partitioning. In: Rankin, J.C., Jensen, F.B. (Eds.), Fish Ecophysiology. Chapman and Hall, London, pp. 1 – 44. Konstantinov, A.S., Zadanovich, V.V., Pushkar, V.Y., Soloveva, E.A., 1998. Effects of oxygen fluctuations in water on growth and energetics of fishes. J. Ichtyol. 38 (5), 386 – 392. Liao, P.B., 1971. Water requirements for salmonids. Progressive Fish-Culturist 33, 210 – 215. Maxime, V., Boeuf, G., Pennec, J.P., Peyraud, C., 1989. Comparative study of energetic metabolism of Atlantic salmon (Salmo salar) parr and smolt. Aquaculture 82, 163 – 171. Metcalf and Eddy, Inc., 1991. Wastewater Engineering Treatment, Disposal, and Reuse. McGraw-Hill, New York 1334 pp. Post, J.R., Lee, J.A., 1996. Metabolic ontogeny of teleost fishes. Can. J. Fish. Aquat. Sci. 53, 910 – 923. Rosseland, B.O., Jacobsen, P., Grande, M., 1990. Miljørelaterte tilstander. In: Poppe, T.T. (Ed.), Fiskehelse. Grieg Forlag, Bergen, Norway, pp. 279 – 287 (in Norwegian). Smart, G.R., 1981. Aspects of water quality producing stress in intensive fish culture. In: Pickering, A.D. (Ed.), Stress and Fish. Academic Press, New York, pp. 277 – 293. Smith, T.R., Haines, T.A., 1995. Mortality, growth, swimming activity and gill morphology of brook trout (Sal6elinus fontinalis) and Atlantic salmon (Salmo salar) exposed to low pH with and without aluminum. Environ. Pollut. 90, 33–40. Sokal, R.R., Rohlf, F.J., 1981. Biometry. The Principles and Practice of Statistics in Biological Research, 2nd ed. W.H. Freeman, San Francisco 859 pp. Warren, C.E., Davies, G.E., 1967. Laboratory studies on the feeding, bioenergetics, and growth of fish. In: Gerking, S.D. (Ed.), The Biological Basis of Freshwater Fish Production. Blackwell, Oxford, pp. 175 – 214. Willoughby, H., 1968. A method for calculating carrying capacities of hatchery troughs and ponds. Prog. Fish. Cult. July, 173–174. Zar, J.H., 1996. Biostatistical Analyses, 3rd ed. Prentice Hall, Englewood Cliffs, NJ 662 pp.
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Water flow requirements in the intensive production of Atlantic salmon (Salmo salar L.) fry: growth and oxygen consumption Sveinung Fivelstad a,*, Asbjørn Bergheim b, Hilde Kløften a, Reidun Haugen c, Torild Lohne c, Anne Berit Olsen d a
Laboratory of En6ironment, Bergen College of Engineering, Nyga˚rdsgaten 112, PB 6030, N-5020 Bergen, Norway b Rogaland Research, P.O. Box 2503, Ullandhaug, N-4004 Sta6anger, Norway c Sæ6areid Fish Farm, 5674 Sæ6areid, Norway d National Veterinary Institute Bergen, Minde Alle, P.O. BOX 40, N-5032 Minde, Norway Received 2 July 1998; accepted 15 December 1998
Abstract Atlantic salmon (Salmo salar L.) fry (1– 10 g) were exposed to three water flow rates: 1.4 (control), 1.0 (medium) and 0.7 l kg − 1 min − 1 (low). There were four replicate tanks in each group. Alkalinity was low (0.03–0.04 mM). Oxygen was added to the inlet water to maintain discharge water oxygen concentration higher than 7 mg l − 1, at 16°C. The mean weight of fish in the low water flow group was significantly lower than in the control flow group after 2 months. No significant differences in mean fish length and condition factor between groups were found. There was no significant difference in the frequency of occurrence of gill lesions among the groups. Mortality was low in all groups (0.3 – 0.4%). In the majority of tanks (nine of 12), oxygen consumption rates decreased significantly as the mean fish size increased. An overall range of 5–12 mg O2 kg − 1 min − 1 was observed. There were no significant differences between the b-values (weight exponent: log oxygen consumption versus log body weight) of the three groups. The range of the weight exponents for the combined groups (between −0.19 and −0.23) was narrower than that of the individual tanks (between − 0.12 and −0.27). The wide range in the individual tanks may be a result of relatively few oxygen measurements. No significant differences were found in the oxygen consumption levels of the three groups. The oxygen consumption rate was however higher than predicted by earlier oxygen consumption models. The mathematical corrections of oxygen consump* Corresponding author. Tel.: +47-55587500; fax: +47-55587790. E-mail address: [email protected] (S. Fivelstad) 0144-8609/99/$ - see front matter © 1999 Elsevier Science B.V. All rights reserved. PII: S 0 1 4 4 - 8 6 0 9 ( 9 9 ) 0 0 0 0 2 - 3
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tion rates due to reaeration of oxygen were generally within 9 3% of the measured oxygen consumption rates (in all tanks). Further studies are needed both to quantify water flow requirements and oxygen consumption rates for Atlantic salmon fry. © 1999 Elsevier Science B.V. All rights reserved. Keywords: Atlantic salmon fry; Water flow; Oxygen consumption models; Oxygenation; Growth
1. Introduction
1.1. Water flow The water flow requirement is biologically and economically important in landbased systems since it is one of the limiting factors for fish production. In Norwegian hatcheries, elevated temperature is used to increase the growth rates of Atlantic salmon (Salmo salar L.), especially from startfeeding and until the fry reach 10 g. The oxygen consumption rate of the fry is high and oxygen gas is added to the inlet water to decrease the demand of heated water. Quantitatively the water flow requirement may be expressed as (Fivelstad, 1988): q0 =
M DOin −DOout
(1)
where q0 is the specific water flow requirement (l kg − 1 min − 1), M is the oxygen consumption rate (mg kg − 1 min − 1) and DOin and DOout is the oxygen concentration (mg l − 1) in the inlet water and at the discharge, respectively. The water flow requirement (q0) is the inverse of loading (kg of fish divided by flow to rearing unit in liters per min (kg l − 1 min − 1) (Colt and Orwics, 1991)). This equation can also be stated as: q0 =
M d
(2)
where d is the difference in dissolved oxygen between the inlet water and the discharge (DOin −DOout). The difference (d) expresses the relationship between the oxygen consumption rate and the specific water flow: d=
M q0
(3)
The difference (d) is a measure of the production intensity of a fish farm. The specific water flow can be reduced when the oxygen consumption rate is reduced to operate a fish farm under constant values for d. When the water flow is reduced there is a build up of both carbon dioxide and total ammonia, and pH is reduced. The increase in carbon dioxide and the reduction in pH is directly related to increased values for d (Colt and Orwics, 1991). The aim of the present experiment was to study limiting values for the water flow requirement for Atlantic salmon fry under intensive hatchery production. The difference (d) was considered to be an important parameter in the experiment.
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1.2. Oxygen consumption Intensification of production often influences the metabolism of the fish stock. Factors such as water temperature, feeding, photo-period, oxygen level and biological parameters such as stress, will influence the metabolic rate (Jobling, 1993). Oxygen consumption rate models have been developed for post-smolt Atlantic salmon in commercial-scale tanks (Fivelstad and Smith, 1991; Forsberg, 1994), and in a tunnel respirometer (Grøttum and Sigholt, 1998). Bergheim et al. (1991) have described the oxygen consumption of parr-smolt (individual size 27–67 g) in a commercial-scale hatchery. There is however a lack of knowledge regarding the oxygen consumption rates of Atlantic salmon fry under intensive hatchery conditions. This paper describes the oxygen consumption of Atlantic salmon fry and fingerlings (up to 10 g) at high water temperature and three different water flow rates (l kg − 1 min − 1). The specific oxygen consumption rate is one of the important parameters determining the water flow requirement for fish.
2. Materials and methods
2.1. Experimental protocol and equipment The experiment was performed in an indoor hatchery, at Sævareid Fish Farm, during a period of 2 months. The water was soft (conductivity 20–25 mS cm − 1; calcium 0.5 – 0.7 mg l − 1; total alkalinity 0.03–0.04 mM) and the aluminium concentration was low (less than 5 mg l − 1 labile aluminium). The experimental set-up comprised 12 fish tanks, representing four replicates of the control (high water flow) and two test groups (medium and low water flow) (Table 1). Table 1 Experimental conditions for the three groupsa Parameters
Control group
Medium water flow group
Low water flow group
Specific water flow (l kg−1 min−1)
1.4 9 0.48 (220) 0.4–2.3 12.6 91.0 (221) 6.2 91.9 (137) 2.5–11.0
1.090.31 (220) 0.4–1.5 11.3 91.0 (221) 7.6 9 2.0 (137) 2.7–12.6
0.7 9 0.24 (220) 0.3–1.2 8.290.7 (221) 10.4 9 2.6 (142) 4.3–15.6
5.6 (148) 5.0–6.0
5.5 (148) 4.9–5.9
5.5 (148) 4.8–5.9
Oxygen at the discharge (mg l−1) Difference in dissolved oxygen between the inlet water and the discharge (mg l−1) pH at the discharge
a Mean (9 S.D.) and ranges (number of measurements in parenthesis). Mean oxygen concentration in the inlet water was 19 mg l−1 for all groups.
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The freshwater influent was heated to 15–16°C by a heat pump, and then aerated in a packed column aerator system. Each tank (volume: 2000 l) was stocked with 12 000–16 000 fry acclimated to the hatchery conditions since the eyed-egg stage. The fry were exposed to continuous light (24 h day − 1) and were fed ‘dry’ food (‘Felleskjøpet’ nos. 1.2 and 2.0) by ‘Aquaprodukter’ automatic feeders every 8 min on a 24-h basis. Fish density at the start of the experiment was 6–8 kg m3 and at the end 60 – 80 kg m3. During the experiment water flow (l min − 1) and the oxygen level in the inlet water was adjusted to meet the increased oxygen consumption in the tanks. Oxygen was added to the inlet water by an ‘Oxygenator’ from Hydrogas.
2.2. Water quality measurements The inlet and outlet oxygen concentrations were measured by an Oxyguard dissolved oxygen meter (Handy Mk 1), and pH was measured by Radiometer pH meter PHM-80. The conductivity was measured by a YSI S-C-T meter (Model 33), and the total gas pressure was measured by a Weiss saturometer Model ES-2. Oxygen concentrations and pH were measured at least once a day. Water flow was determined by measuring the time taken to fill a 10-l container. Water temperature, recorded daily, was 15 – 16°C.
2.3. Growth and oxygen consumption The weight and length of individual fish (75 in each tank, 300 in each group) were measured at the beginning of exposure (day 0) and after 28 and 56 days of exposure. In addition, mean weights of 100 fish were measured after 16 and 43 days. The condition factor, CF, was calculated from the formula: CF= 100 W/L 3
(4)
where W is the wet weight (g) of each fish and L is fish length (cm). The specific growth rate (SGR as% wt. day − 1) was calculated from the equation: SGR=(ln W2 −ln W1)/(t2 − t1) · 100
(5)
where W1 and W2 are mean fish weights at the sample times t1 and t2, respectively. Oxygen consumption rates (M% as mg kg − 1 min − 1) were initially calculated from measurements of oxygen concentrations in the inlet and discharge waters, and the total biomass in the tanks: M%= [(Cinlet −Cdischarge)]Q/B
(6) −1
−1
where C is oxygen concentrations (mg l ), Q is the flow (l min ) and B is fish biomass (kg). In order to correct for the oxygen diffusion across the water surface, the diffusion rate (rdiff) was estimated for all tanks (Metcalf and Eddy, Inc., 1991): rdiff =K(Csat −C)
(7)
where K is the surface reaeration rate, Csat is the saturation concentration of oxygen and C is the actual oxygen concentration in the tank.
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The corrected oxygen consumption rates (M as mg kg − 1 min − 1) were finally calculated: M = [(Cinlet −Cdischarge)Q]/B + rdiffV/B
(8)
where V is tank volume (l). The relationship between oxygen consumption rate (M as mg kg − 1 min − 1) and fish size was estimated using the function (Brett and Groves, 1979): M =a·BW b
(9)
where BW is the individual fish weight (g), a is a constant and b is the fish weight factor.
2.4. Histomorphological examination Tissue specimens for histomorphological examination were collected on days 0 and 56. A total of 12 fish from each group were killed by severance of the spinal cord just behind the opercula. Immediately after sacrifice, gill, mid and hind kidneys were fixed in 10% neutral buffered formalin. The tissues were embedded in paraffin wax. Sections were cut at 3 –5-mm thickness and routinely stained with haematoxylin and eosin (H&E). The sections were studied blind, i.e. with no knowledge of the group to which the fish belonged. Gills were examined for histomorphological lesions in general. Kidneys were examined for mineral deposits, i.e. nephrocalsinosis.
2.5. Statistical analyses Statistical analyses were performed using Statgraphics from STSC. Multiple comparisons among pairs of means were performed by one-way ANOVA combined with the Tukey test method (Sokal and Rohlf, 1981; Fowler and Cohen, 1990). The significance of differences between regression lines was examined by a t-test (Fowler and Cohen, 1990). The regression analyses (log M vs. log BW) were based on recorded data from fish sizes down to about 2 g (i.e. seven to nine initial values were excluded from each tank). The reason for excluding these data was that pH was in the range 4.8 – 5.5 during the first 9 days of the experiment. In addition all tanks were treated with formalin on day 3.
3. Results
3.1. Water flow, growth, histomorphological examination and mortality Fish growth results are shown in Table 2. No clear differences in the mean values of the growth parameters measured (weight, length and condition factor) were determined between the high (control) and medium water flow groups. Mean weight for the low water flow group was however slightly, and significantly reduced,
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Table 2 Weight, length and condition factor during the experimenta Parameters
Day
Control group
Medium group
Low group
Weight (g)
0 28 56 0–56
1.319 0.020 (300) 3.859 0.085 (300) 11.5490.306 (298) 3.89
1.44 90.023 (300) 4.01 90.089 (300) 12.0290.288 (295) 3.79
1.35 9 0.025 (300) 3.41 90.076 (300) 10.36 90.249* (298) 3.64
0 28 56 0 28 56 0–56
4.9490.024 6.71 9 0.043 9.2590.080 1.0790.006 1.22 9 0.005 1.3690.006 0.36
5.06 9 0.024 6.79 9 0.045 9.39 9 0.075 1.09 9 0.008 1.22 90.005 1.37 90.005 0.28
4.95 90.028 6.50 90.042 9.00 90.071 1.08 90.006 1.19 90.007 1.34 90.006 0.44
Specific growth rate (% day−1) Length (cm)
Condition factor
Mortality (%)
(300) (300) (298) (300) (300) (298)
(300) (300) (295) (300) (300) (295)
(300) (300) (298) (300) (300) (298)
Mean 9S.E., number of measurements in parenthesis. * PB0.05.
a
when compared to the control group at the end of the experiment. Mean length and condition factor of the low group was slightly, although not significantly, reduced compared to the control group. There was no significant difference in the prevalence and quality of gill lesions among the groups. Nephrocalsinosis was not observed in any of the groups. Mortality was low in all three groups during the study period, at 0.3 – 0.4%.
3.2. Oxygen consumption: daily 6ariation Oxygen consumption data covering the whole study period are shown from three fish tanks representing the three water flow levels (Fig. 1a,b,c). In all groups, high oxygen consumption rate fluctuations were observed during the first 2 weeks of recording. The high water flow group in particular demonstrated extreme variations at this stage. The lowest consumption rates observed during the first days coincided with reduced tank outlet pH levels (pH 4.8–5.5) due to acidification of the inlet water. Subsequently, consumption rates gradually decreased with increasing fish size (2–9 g). An overall range of 5 – 12 mg O2 kg − 1 min − 1 was observed.
3.3. Oxygen consumption models Table 3 shows the results from the linear regression analyses of oxygen consumption changes with fish weight, grouped in terms of both individual tanks and the three water flow groups.
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Fig. 1. Measured Atlantic salmon fry oxygen consumption rates in three representative tanks supplied with different levels of water flow. In each tank seven to nine initial values are excluded from statistical analysis (Table 2, Fig. 2). (a) ‘Control’ (high) flow: tank no. 233; (b) ‘medium’ flow: tank no. 230; (c) ‘low’ flow: tank no. 229.
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Fig. 1. (Continued)
3.3.1. Low water flow group No significant differences were found in a- or b-values between the four tanks (P\0.05). In the four tanks, the oxygen consumption rates decreased significantly (PB0.01) as the mean fish size increased. Oxygen consumption data for these tanks were therefore combined. 3.3.2. Medium water flow group In one tank, a significant positive relationship between oxygen consumption and mean fish weight (b = 0.17) was found. The a-value for this tank was significantly different from the other three tanks so these results were excluded from the combined data for the medium group. Oxygen consumption rates in the three other tanks decreased significantly (P B 0.01) with increased mean fish size. Oxygen consumption data from these three tanks were combined. 3.3.3. High water flow group (control) Oxygen consumption rates decreased significantly (PB 0.01) with increased mean fish size in only two of four tanks. The a and b-values from these two tanks were not significantly different from each other. The oxygen consumption data for these two tanks were therefore combined. 3.3.4. Among group comparisons No significant differences were found in the a- (oxygen consumption levels) or b-values (slopes) among the combined groups. Therefore, the oxygen consumption
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Table 3 The relationship between oxygen consumption (M, mg O2 kg−1 min−1) and fish size (BW, g) in 12 tanks stocked with salmon fry at Sævareid Fish Farma Tank no.
225 228 229 234 224 227 230 235 223 226 232 233 All All, T227 All (T223–T226) Total
Water flow groups
Low
Medium
Control (high)
Low Medium Control (high) Low+medium
Log M= log a+b log BW
Log a (S.E.)
b (S.E.)
1.04 0.98 1.02 1.02 1.00 0.80 1.07 0.99 1.00 0.98 1.04 1.07 1.02 1.03 1.06 1.02
−0.151 (0.070) −0.225 (0.043)** −0.266 (0.042)** −0.222 (0.042)** −0.191 (0.038)** 0.177 (0.072)** −0.256 (0.029)** −0.122 (0.054)* −0.076 (0.042) −0.049 (0.085) −0.159 (0.033)** −0.207 (0.068)** −0.222 (0.035)** −0.199 (0.025)** −0.187 (0.040)** −0.198 (0.021)**
(0.042)** (0.026)** (0.026)** (0.027)** (0.026)** (0.048)** (0.019)** (0.037)** (0.038)** (0.057)** (0.022)** (0.043)** (0.021)** (0.017)** (0.026)** (0.014)**
R2
P-level
0.18 (23) 0.60 (21) 0.64 (25) 0.61 (20) 0.57 (21) 0.24 (21) 0.79 (22) 0.21 (21) 0.07 (25) 0.06 (21) 0.61 (17) 0.33 (22) 0.32 (89) 0.50 (64) 0.37 (39) 0.31(192)
B0.05 B0.01 B0.01 B0.01 B0.01 B0.01 B0.01 B0.05 B0.01 B0.01 B0.01 B0.01 B0.01 B0.01
+ high a Stable temperature (15.5–16.5°C), three levels of water flow (low, medium, control). Function used: M =a·BW b (Brett and Groves, 1979), where a is a constant and b is the weight factor (S.E.= standard error). * PB0.05. ** PB0.01.
data were combined in a common model for the three groups. Fig. 2 shows the distributions of log M (oxygen consumption rate) with respect to log BW (fish size) for the combined groups. It should be noted that the mathematical corrections of oxygen consumption rates due to reaeration of oxygen, generally were within 9 3% of the measured oxygen consumption rates (in all tanks).
4. Discussion
4.1. Water quality Water temperature was constant, and the same in all tanks. Though pH was lower than the optimum level for salmonids, there was only a slight difference in mean pH between the three groups. The safe level for low pH for freshwater fish is 5.0 (Alabaster and Lloyd, 1982) assuming no other synergistic factors. The low mortality rate in all groups indicates that pH was nevertheless within acceptable
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limits. The aluminium concentration of the water supply to Sævareid Fish Farm is very low. Gills are sensitive to pH/Al stress (Smith and Haines, 1995; Jagoe and Haines, 1997), but no gill damage was observed during the study. Growth rates achieved in the present study (3.6 – 3.9% per day at 16°C) were slightly lower than rates reported in growth tables (Austreng et al., 1987) for Atlantic salmon between 0.6 and 10 g (4.1 – 4.2% per day at 16°C). The experiment was run as a part of the full-scale production and it was not possible to regulate the oxygen concentration in the inlet water independently for the three groups. As a consequence the mean oxygen saturation was 125, 112 and 83% for the control group, the medium group and the low group, respectively. In addition, there was day to day variation in the oxygen saturation for the different groups. As a result of the oxygen saturation, single sets of measurements showed total gas pressure to be 108% (15.5 mg l − 1 oxygen), 105% (13.1 mg l − 1 oxygen) and 100% (9.4 mg l − 1 oxygen) for the control group, the medium group and the low group, respectively. The percent saturation of nitrogen (+ argon) was 95, 98 and 100% for the control group, the medium group and the low group, respectively. There is not enough background information in the literature to decide whether these differences in oxygen saturation may influence the growth rate of Atlantic salmon fry. Periodic decreases of oxygen levels from saturation to levels below saturation had even in some experiments a positive effect on the growth of fish (Konstantinov et al., 1998). In the present experiment the dissolved oxygen concen-
Fig. 2. The relationship between oxygen consumption rates and fish size (log M versus log BW) applying the combined model (control flow + medium flow+ low flow) for Atlantic salmon fry (n =192). The two pairs of dotted lines represent the 95% confidence (closest to the regression line) and prediction limits (farthest away from the regression line). Model estimates in Table 2.
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tration in the effluent from all tanks was maintained above 7 mg l − 1 (71% air saturation) during the experimental period. At this level, oxygen concentration is generally not considered to be a growth limiting factor (Rosseland et al., 1990). It should be noted that no significant differences were found in the oxygen consumption rates of the three different groups. It has been shown that reduced water flow may have detrimental effects on Atlantic salmon smolts due to increased CO2 concentrations and reduced pH (Fivelstad and Binde, 1994), if the difference in dissolved oxygen concentration between the tank inlet and outlet water is in the range 6–10 mg l − 1. In the present experiment, fish in the low water flow group achieved a slightly, yet significantly, lower weight than the other groups. For this group, the difference in oxygen concentration between the inlet and outlet water was in the range 4–16 mg l − 1 (Table 1). The effects on smolts (growth reduction, gill damages, etc.) observed by Fivelstad and Binde (1994) were however more severe than the effects on fry in the present experiment. Using the model proposed by Colt and Orwics (1991) mean free carbon dioxide concentration for the low water flow group during the present experiment, was predicted to be about 15 mg l − 1. Results from experiments performed on Atlantic salmon smolts during spring 1996 and 1997, in neutral water (pH 6.5), indicated that the maximum safe level for carbon dioxide is lower than 20 mg l − 1 (Fivelstad et al., in prep.). Carbon dioxide is also more toxic at lower pH (Alabaster and Lloyd, 1982). Thus, higher carbon dioxide concentrations combined with low pH may have resulted in a slightly lower growth rate for the low water flow group compared with the other two groups. Generally, a higher alkalinity is favourable when the water flow is reduced since it determines the ability of the water to buffer changes in pH resulting from carbon dioxide accumulation (Colt and Orwics, 1991; Ewing et al., 1994). It should be noted that no negative effects were found on chinook salmon smolts (Oncorhynchus tshawytscha) when supplemental oxygen was used at higher water alkalinities (Ewing et al., 1994). The present investigation clearly indicated that water flow (l kg − 1 min − 1) influences the growth rate of Atlantic salmon fry at low alkalinity. Further studies are needed to quantify water flow requirements for Atlantic salmon fry at other alkalinity levels and at other temperatures than presented here.
4.2. Oxygen consumption In the present study the method used to determine the weight exponent (b) was based on log-log transformation prior to linear regression. However, a so-called ‘non-linear iterative least-square fit’ (Glass, 1969) might in certain cases, especially when the number of measurements is low, represent a somewhat better fitness than the log-log transformation method. The residuals plots for each fish tank were found to be uniformally spread around zero (data exhibiting homoscedasticity) indicating an accurate description of the relationship between oxygen consumption and body weight (Zar, 1996). In intensive hatchery production, the oxygen consumption rate may be influenced by numerous parameters. Consequently, it was not surprising that three out of the 12 involved tanks did not conform to the expected
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trend regarding oxygen consumption versus fish size. When this relationship (oxygen consumption vs. fish size) is masked by environmental factors, it is not possible to include the data in further statistical analyses. As a result, mathematical models for the oxygen consumption rate may not always apply to hatchery conditions. In a review, Forsberg (1994) presented a weight exponent (b) range from −0.14 to −0.28 for post-smolt Atlantic salmon. No weight exponents for Atlantic salmon fingerlings have though been located in the literature. In most tanks the relationship between oxygen consumption and fish size (weight exponent, b, between − 0.12 and −0.27) was within the range reported for various salmonid species. The range of the weight exponents for the combined groups (between −0.19 and −0.23) was narrower than that of the individual tanks (between − 0.12 and − 0.27). The wide range in the individual tanks may be a result of relatively few oxygen measurements. The weight exponent for the combined groups (− 0.20) corresponds closely to the weight exponent found by Liao (1971), indicating that the weight exponent converges against given values when the number of measurements is high. The wide variation reported in the literature may partly be related to a low number of measurements. Despite the significant relationship between oxygen consumption rate and fish size, the presented models (Table 2) only explained 32–50% of the total variation in the data. In earlier studies, factors such as daily ration (Haskell, 1955; Willoughby, 1968; Brett, 1976), activity (Brett, 1962; Beamish and Dickie, 1967; Albrecht, 1974), and stress level (Smart, 1981) have been found to influence metabolic rate. Activity and feeding level (appetite; amount of food ingested) may be important parameters contributing to the total variation in the data. Stress associated with daily husbandry routines may also be important. The metabolic rate related to the activity level can be divided into expenditure components, such as swimming against a given current, feeding behaviour and random activity. Swimming against a given current velocity may be the most important and easy component to quantify, since it is related to the stream velocity. This velocity does however vary considerably within any tank (Cripps and Poxton, 1992), so defining an average value may be difficult or unrealistic. The sparse current speed measurements in the present study indicated a relatively stable current velocity in all tanks of 1 – 1.5 BL s − 1. The consumption of food by animals results in an increase in metabolic rate. This increase is known as the specific dynamic action (SDA) of the food (Warren and Davies, 1967). The relationship between the feeding level and metabolic rate is based on the SDA effect and is easy to quantify if all the food is ingested and the feeding rate corresponds closely to the specific growth rate of the fish. However, diurnal variation in appetite (and amount of food wastes) may mask such a direct relationship. By re-analysing published data on rainbow trout (Onchoryncus mykiss) fry, Post and Lee (1996) detected a biphasic metabolism relationship with respect to fish size, not unlike the progress of this relationship found over the whole growth period at Sævareid Fish Farm (Fig. 1). Post and Lee (1996) proposed that the metabolic
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Fig. 3. Comparison between oxygen consumption rates (mg kg − 1 min − 1) as a function of fish size (g) using the model of Liao (1971) and the combined model (control flow +medium flow +low flow) obtained in the present investigation.
ontogeny may be explained by physiological changes (development of muscle mass) and changes in the surface area to volume ratio of the respiratory organs during the early life stages. No measurements of oxygen consumption of Atlantic salmon fry at such a high, stable temperature have previously been reported. Oxygen consumption may not increase exponentially with increased temperature (Forsberg, 1994). The Q10 value, used to express the relative change in oxygen consumption with water temperature changes (relative to consumption at 10°C), was found to decrease with increasing temperature, for Atlantic salmon parr of 5–27 g (Maxime et al., 1989): 3.5 at 9–13°C; 2.9 at 13 – 15°C; and 1.5 at 15–19°C (routine metabolism). The oxygen consumption reported by Maxime et al. (1989), corrected for fish size and temperature (11.5 g, 14.3°C), was however about 50% lower than that measured at Sævareid Fish Farm. Our presented oxygen consumption rates were 1.5–1.6 times higher than calculated by the oxygen consumption model estimated by Liao (1971) for Pacific salmon (Fig. 3). Since the proposed model (M = a·BW b) does not account for the activity level or the feeding level, the residuals must be expected to be considerable. The model for the different water flow groups did however explain 32–50% of the total variation in the data, which may be considered as good for data obtained from a full-scale production unit. The combined model (low group+ medium group+ control group) explained 31% of the total variation in the data. Further studies are needed to study oxygen consumption rates for Atlantic salmon fry at other temperatures than presented here.
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Acknowledgements Appreciation is expressed to all the staff at Sævareid Fish Farm for their co-operation. The project was partly financed by the Norwegian Research Council. Dr Simon J. Cripps (Rogaland Research) kindly gave advice on language and structure of the manuscript.
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