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Extending the limits of fish production in manured static-water ponds
27
Aquaculture, 89 (1990) 27-41 Elsevier Science Publishers B.V., Amsterdam
Extending the limits of fish production in manured static-water ponds*
John A. Colman’, Peter Edwards, Manoj Yomchinda Pacharaprakiti
and Chintana
Asian institute of Technology, Agricultural and Food Engineering Division, GPO Box 2754, Bangkok (Thailand) (Accepted 22 December
1989)
ABSTRACT
Colman, J.A., Edwards, P., Yomchinda, M. and Pacharaprakiti, C., 1990. Extending the limits of fish product [on in manured static-water ponds. Aquaculture, 89: 27-4 1. A working hypothesis was adopted that previously reported limits to fish productivity in manured static-water systems (2.5-3.5 g fish m-’ dd’) are derived from an imbalance between phytoplankton productivity and harvest by tish. The assumption that an improved balance would result in greater net generation of oxygen, and phytoplankton and fish productivities was tested in a series of outdoor fertilized concrete tanks in which phytoplankton harvesting was regulated by varying the stocking density (mnge 0.5-10 fish m-‘) of the phytophagous Nile tilapia (Oreochromis niloticus). The resulting patterns of fish growth rates and dissolved oxygen concentrations at various fish stocking densities supported the phytoplankton balance hypothesis. Oxygen concentrations at dawn and growth per fish were lowest at low fish stocking densities, 0.5 and 1.0 fish m-*, where presumably the large standing crop of algae was grazed too slowly to stimulate algal growth. The highest tank fish productivity measured, 8.8 g fish me2 at 5 fish m-*, was well above previously reported levels but was sustained for only 2 weeks. However, the two highest sustained tank fish productivities of 4.5 and 5.3 g fish m-’ dd’ averaged 63% higher than the average of previously reported-maxima. These results indicate that higher growth rates on an area1 basis are possible than have previously been reported. However, iachieving growth at the highest rate was not routine. The average growth of five tanks stocked with 5 fish m-’ was only 1.7 g m-’ dd’. Microcystis, the algal taxon that dominated all but one experimental tank, may have been important for high fish productivity. At the optimal fish stocking density of 5 fish m-‘, nitrite build-up may have limited fish productivity in some tanks. Feed conversion ratios based on phytoplankton as feed ranged from 4.0 to 0.9 at 5 fish m-‘; based on phytoplankton and organic fertilizer as feeds they ranged from 10.7 to 3.1. *ICLARM Contribution No. 237. Paper presented at the 2nd International Conference on Warm Water Aquaculture - Finfrsh, 5-8 February 1985, Brigham Young University, HI (U.S.A.). ‘Present address and correspondence: U.S. Geological Survey, 102 E. Main St., Urbana IL 61801 (U.S.A.).
0044-8486/90/$03.50
0 1990 -
Elsevier Science Publishers
B.V.
28
J.A. COLMAN ET AL.
INTRODUCTION
There appears to be a maximum fish yield of approximately 2.5-3.5 g m-’ d-’ (25-35 kg ha-’ dd’ or 9-l 3 tons ha-’ yr- ’ ) in manured static-water fish ponds from several countries with a range of fish species and types of manure (Schroeder, 1987a,b; Wohlfarth and Hulata, 1987 ). Extrapolated net fish yields of 5.5 g rnw2 dd’ were reported for a system in which Nile tilapia (0. niloticus) were fed phytoplankton, but the algae were pumped through concrete fish tanks from a sewage-fed high rate stabilization pond and were not produced in situ as in a manured fish pond (Edwards et al., 198 1). A working hypothesis of productivity-limiting factors in manured ponds, developed by Colman and Edwards ( 1987 ) , was adopted for the present investigation: that an imperfect balance between primary productivity and phytoplankton harvest by phytophagous fish limits net algal productivity and fish yield in current practice. Net algal productivity is important in phytophagous fish culture because it represents production of fish food and net production of oxygen. Both algal growth equations and experimentation with continuous algal biomass culture indicate that maximal net phytoplankton productivity in nutrient-sufficient, light-limited culture occurs when the algal standing crop size is maintained at an intermediate level (Goldman, 1979). Net primary productivity generally increases with increasing phytoplankton standing crop because of increased reproducing stock. However, at very high levels of phytoplankton standing crop, self-shading becomes important and continued standing crop increase leads to lower net primary productivity. The stocking density of phytophagous fish was varied in an initial experiment in a series of outdoor concrete tanks to provide different rates of phytoplankton harvest by fish. This investigation sought to find whether an optimal-sized phytoplankton standing crop could be approached by substituting fish cropping of algae for the mechanical harvesting used in continuous algal biomass culture. It was expected that grazing pressure would approach an optimal rate for phytoplankton productivity at one of the fish stocking densities used, with concomitant optimal fish yield. Phytoplankton productivity and rates of conversion of phytoplankton biomass and organic carbon inputs to fish were determined in tanks in a second experiment under stocking conditions which produced the highest fish yield in the first experiment. Methods to estimate net phytoplankton productivity, which is required for the calculation of food conversion ratios (FCR ), remain to be standardized. Even recent methodological comparisons of the measurement of gross primary productivity (GPP) in hyper-eutrophic systems revealed no agreement between methods (Bemer et al., 1986); the determination of net phytoplankton productivity (GPP less phytoplankton respiration) is still more problematical. The best available methods for primary productivity determination
29
FISH PRODLICTION IN MANURED STATIC-WATER PONDS
have been used in this study - oxygen change, appropriate for hypertrophia (Berner et al., 1986 ), in unconfined tanks to avoid bottle effects (McConnell, 1962; Hall and Moll, 1975). Although the net phytoplankton productivity values reported here have uncertain accuracy, they are useful for comparisons between tanks and experiments in which the same methodology is used; and they are a useful beginning in computing the FCR of phytoplankton produced in situ as a food source for phytophagous fish. MATERIALS AND METHODS
Experiment 1 - stocking density Fish were stocked in 4.8-m3 outdoor concrete tanks at six stocking densities in triplicate. Tank inputs were septage (slurry from septic tanks and cesspools) and inorganic fertilizers. Nets lined the insides of the tanks to facilitate fish samlpling. The tanks were tilled with water from a surface source (total alkalinity 300-400 mg CaC03 l- ’ ) to a depth of 1 m. A 28-day start-up period was begun on 23 January 1984 to allow phytoplankton to develop in the tanks. Four Nile tilapia (0. niloticus) of mean weight 44 g were added to each tank during the start-up period to condition the water and to control insect larvae. The fish were obtained from a local commercial hatchery. Fertilizers were applied in three doses per week, equivalent to the daily rates shown in Table 1. Inorganic fertilizers were dissolved in water before addition, except for iron, which was added as a slurry. The four fish in each tank were removed on 20 February and male tilapia of mean weight 77 g were stocked. Three replicates of the following stocking density treatments were used: 0, 0.5, 1, 2, 5, 10 fish m-‘. A random assignment of treatments to tanks was used. Tank fertilization was continued at approximately three doses per week after stocking fish. Water was not circuTABLE 1 Fertilizer input rates Fertilizer
Potassium
nitrate
Triple superphosphate FeSO,.7H,O Septage
Weight of fertilizer (g tank-’ dose-‘)
Nutrient equivalent (gm-‘d-l)
120
K -4.16 N - 1.50 P -0.22 Fe - 0.25” Organic C - 3b N - 0.42 P -0.13
12 14 5 (litres)
“Iron addition was reduced 10 fold in Experiment 2. bEstimated from measured chemical oxygen demand.
30
J.A. COLMAN ET AL.
lated through the tanks. Evaporative losses were replaced by fertilizer inputs and by make-up water. Chemical monitoring of 12 tanks, two tanks per treatment, was initiated after stocking fish. Water samples were obtained by pumping from 30-cm depth. Sampling was at approximately 8 a.m., before water column mixing was inhibited by temperature stratification (temperature measurements indicated that tanks mixed vertically every night). Samples for analysis of solutes were collected first; then the tanks were stirred to suspend particulate matter evenly and samples for chlorophyll a analysis were taken. Standard chemical analytical procedures were used (American Public Health Association et al., 1980). Ammonia (phenate method), chlorophyll a (acetone extraction with tissue grinding) and dissolved oxygen (Winkler method with the azide modification) were measured twice weekly. Additional samples for dissolved oxygen were taken weekly at dawn (6 a.m.). Determinations of pH, alkalinity and nitrite (spectroscopic, diazotization method) were made in selected tanks towards the end of the experiment. Fish growth was determined by batched weighing of fish from each tank at 14-day intervals. Fish were anaesthetized with quinaldine during weighing. Dominant phytoplankton genera were monitored subjectively by a visual estimation of abundance in percent of total biomass by microscopic observation approximately every 2 weeks. Experiment 2 -feed conversion Only one stocking density, 5 fish rnp2, was used. The culture method was similar to the previous experiment but with more complete monitoring of tank conditions. The phytoplankton growth start-up period was begun on 4 April 1984 and continued for 28 days until 2 May when fish were stocked. Fertilizer additions were again made three times per week (Table 1 ), although the amount of iron was reduced to 10% of the amount given in the first experiment. Tilapia of mean weight 70 g were stocked in nine tanks, 25 fish per tank. Monitoring of phytoplankton genera and fish sampling was as for Experiment 1. Water was sampled and analyzed as for Experiment 2 but nitrite was included with the parameters measured twice weekly. Diurnal pH and chemical oxygen demand (COD) (macromethod with dichromate reflux) were measured once per week. Primary productivity In addition to measuring dissolved oxygen at 6 a.m. in Experiment 2, dissolved oxygen was measured at the surface at 10 a.m. and 2 p.m. and in depth profile ( IO-cm intervals) at 6 p.m. 5 days per week beginning 3 weeks after the fish were stocked. Die1 whole-tank oxygen changes were computed from
FISH PRODUCTION
IN MANURED
STATIC-WATER
PONDS
31
these measurements and were used to estimate primary productivity (in the manner of McConnell ( 1962 ) and Hall and Moll ( 1975 ) ) as follows: mean wind speeds at the times of the surface oxygen measurements were used to correct for oxygen transfer across the air-water interface according to Banks and Herrera ( 1977). The corrected values were converted to gross primary productivity (GPP, g C rnB2 d-l) by adding the 12-h night community respiration to the daylight oxygen increase and converting from oxygen to carbon GPP= (NWCP+NPR)K,/K, where NWCP= the corrected daylight oxygen change (g O2 me2 d-l), NPR= the corrected night oxygen change (g O2 rnw2 d-l), K, =0.38, grammolecular weight ratio (C/O,), and K2= 1.2, the photosynthetic quotient (0,/C: molar basis; Lewis, 1974). Net phytoplankton productivity (NAP, g C me2 b’ ) was calculated by subtracting phytoplankton respiration, estimated by the product of phytoplankton standing crop and respiration rate (AR) NAP = GPP - Chla*lil,* AR where Chla= standing crop of chlorophyll a (g m-‘), KS= 44 (g C g Chla- ‘; Algren: 1983, for Oscillutoria), and AR= 0.07, respiration rate (d- ’ ) (Bannister, 1979), Evaluation of standing crop by chlorophyll a measurement and conversion to carbon is undesirable because of variability of K3. The conversion is necessary because direct measurements of carbon would not be specific to phytoplankton carbon. A wide range for AR is reported in the literature (Berner et al., 1986). The decision to base AR on the value reported in the Bannister model ( 1979) for respiration of Chlorelluat 26 oC was in part arbitrary. However, a model using this value accurately predicted oxygen concentration in freshwater prawn tanks and ponds which also contained some tilapia in Hawaii (Laws and Malecha, 198 1). Feed conversionratios Orga.nic carbon loading of septage to the tanks was estimated from measured chemical oxygen demand of the septage. The conversion factor used, 2.7 g 0, per gram of organic carbon, assumed an average oxidation state of the septage carbon equivalent to carbohydrate. Possible values for the factor vary from 4.4 for hydrocarbon to 1.3 for organic acids. The accuracy of the estima-tion used is unknown. The organic carbon loading was summed with the appropriate net primary productivity value to give the organic carbon loading rate (Table 2 ) . Organic carbon was converted to dry weight organic matter using a factor of 2 ( Algren, 1983 ) to generate the FCR on a dry weight organic matter to fresh weight fish basis. The accounting of carbon supply and fish growth to estimate FCR was started 3 weeks after fish were stocked to
32
J.A. COLMAN ET AL.
TABLE 2 Primary productivity and feed conversion ratios (dry weight organic matter to wet weight fish basis); numbers in parentheses are standard deviations, where n=29 Parameter
Tank no. 2
Gross primary productivity (gCm-‘d-l) Net primary productivity (gCm-2d-‘)a Organic carbon loading (gCm-2d-‘) Phytoplankton to fish FCRb Septage to fish FCRb Phytoplankton and septage to fish FCRb
3 (61..23 ) (4p ) 7.9
-7.1 -4.4 -11.5
6
-
6.4
8
14 6.1 (2.1) 2.6 (2.6) 5.6
( 1.3)
(Z)
5.9 (1.5)
3.8 (1.4) 6.8
(S:;) 6.2
(Z, 6.9
3.1 2.5 5.6
7.1 6.7 13.8
1.8
“Assumes a phytoplankton respiration rate of 0.07 d-l, see Methods. bNegative values occurred when fish lost weight during the 42-day measurement
1.4 3.3
2.6 2.9 5.3
interval.
minimize the effect on the computation of fish feeding on food organisms which had developed in the tanks during the pre-stocking period. RESULTS
Experiment 1 The addition of organic and inorganic fertilizers caused dense phytoplankton blooms to develop in the tanks by the time fish were stocked. Chlorophyll a concentrations increased from 0.6-0.7 mg 1-r just before fish stocking to 1.O mg I- ’ in the week after stocking , There did not appear to be any pattern of chlorophyll a change after fish stocking, nor any correlation between fish stocking density and chlorophyll a concentration. The dominant genus of phytoplankton ( > 90%) found in all tanks on the four occasions of examination was Microcystis. Other genera present were Chlamydomonas, Chroococcus, Pandorina and at the beginning of the experiment, diatoms. Mean fish growth in terms of biomass increment per area and weight increment per individual fish as a function of time and stocking density are presented in Fig. 1. Mean growth rate at 5 fish me2 remained above 5 g m-’ d-’ for the fist month after stocking. One tank at this stocking density averaged 5.3 g m-2 d-r growth for the first 55 days after stocking; during the 14-28day interval after stocking, growth rate in this tank was 8.8 g me2 d-l. Data were not considered from tanks in which more than 20% fish mortality occurred because significant mortality altered the treatments by changing the stocking density. Initially, weight increments both per fish and on an area1
FISH PRODUCTION IN MANURED STATIC-WATER PONDS
(b)
(a) 7
0.51
fi
^ <
2.ot
f
-0 .? f
Growth
Period
Fig. 1. Fish growth during the stocking density experiment; (a) on an individual fish basis, and (b) for the fish population on an area1 basis. Each bar refers to growth during the previous 14 days (time interval 1, O-l 3 days; 2, 14-27 days; 3, 28-41 days). Data from tanks with more than 20% mortality are not displayed. Numbers in parentheses above the bars indicate the number of tanks averaged when less than 3. The vertical lines above or below the bars equal one-half standard error. The numbers below the bars indicate fish stocking density in number of fish me2.
basis increased with an increase in stocking density up to 5 fish mm2 and then decreased at the highest stocking level of 10 fish rne2. By the time of the last weighing at 6 weeks, the increment of the 1-fish mm2 treatment was the largest on a per fish basis, although the 5&h rnT2 treatment continued to produce the largest increment on an area1 basis. An mdication of fish mortality is also given in Fig. 1 where tanks in which more than 20% mortality occurred are not represented. This level was reached in the highest and lowest stocking density treatments. The 6 a.m. dissolved oxygen concentrations of individual tanks fluctuated over a 5-8 mg 1-l range, with a period of approximately 6 days. The total range alcross all treatments was O-10 mg l- ’ with some treatments tending towards the upper portion of this range and others towards the lower portion. These trends are expressed, by treatment, as means for the first 28 days after fish stocking (Fig. 2). After 28 days, dissolved oxygen data obtained by the Winkler method were not accurate because of chemical interference from the large arnounts of iron put in the tanks as a fertilizer. Ammonia levels also fluctuated within a given tank during the experiment, but more slowly than dissolved oxygen. Mean concentrations by treatment for the first 28 days after stocking were negatively correlated with oxygen {Fig. 2 ).
34
J.A.COLMAN ETAL. 18,
I 16
T
1.4 _I _- 1.2b z 9 1.0-O 9 c :08Q = 0.6'0 I040.2I
0
2
I
1
I
4
6
a
Fish
Stocking
0 Denwty
I
I
2
4
(number
6
t
/
8
IO
mm*)
Fig. 2. Average early morning dissolved oxygen and total ammonia during the first 28 days of the stocking density experiment. The number of observations averaged for each treatment was i4 and 44 for total ammonia and dissolved oxygen, respectively. Error bars represent one standard deviation above and below the mean.
Nitrite measurements were made only for the Wish m-2 treatment and only on day 57, after other treatments had been terminated, and concentrations found in the three tanks were 0.58,0.62 and 1.49 mg N 1-l. Total alkalinity and pH measurements were also measured on day 57 for these three tanks, with means of 580 mg CaC03 l- ’ and pH 10.0. Experiment 2 A heavy ph~oplan~on bloom developed during the 28-day start-up period as in the first experiment. Chlorophyll a concentrations again ranged around 1.O mg 1-r. However, despite an equal stocking density of 5 fish mm2 in all tanks in this experiment, tank number 8 had a significantly lower mean chlorophyll a concentration, 0.75 mg l- ‘, than the mean of the other tanks, 1.10 mg I-‘. The phytoplankton dominance at the time of fish stocking in this experiment was ~~c~o~~~~~,70% of the total biomass of ph~oplan~on (mean for all tanks) but dropped to 45% Micrucystis-55% Chroococcusthe following week. There was a gradual return to Microcystis dominance, which by experiment day 49 was greater than 90%. An exception was tank number 2, not included in the above results, in which Scenedesmuspredominated from day 22 (90- 100%) until the end of the experiment.
FISH PRODlJCTlON IN MANURED STATIC-WATER PONDS
35
Mortality was a problem immediately after stocking fish in Experiment 2. Four of .the nine tanks stocked lost three or more fish by the ninth day after stocking and were dropped from the experiment. All observations and results refer to t.he five remaining tanks. Fish biomass (per meter squared and per fish basis) as a function of time is shown. in Fig. 3. A range of fish growth rates occurred from essentially zero during the last 40 days of the 62-day experiment (tank number 2) to a mean growth of 4.5 g m-* d-l over the entire 62-day period (tank number 8 ). Fish mortality accounts for differences between per fish and per area growth curves for a given tank. Final fish densities ranged from 3.8 to 4.4 fish mV2 with the exception of tank 2, which decreased from 4.0 to 3.1 fish m-’ during the last 2-week interval. Early morning dissolved oxygen and ammonia concentrations were in the same range in the two experiments, but large concentrations of nitrite were found in Experiment 2. Concentrations of nitrite were in the 1-4 mg N 1-l range before fish were stocked. Concentrations fell to below 0.5 mg N 1-l from day 15 through day 33 after stocking .Nitrite then increased again in some tanks to as much as 6 mg N l- ‘. The relationship between fish growth (per area) and average nitrite concentration is shown in Fig. 4. Net and gross primary productivities calculated from the measured daily changes in dissolved oxygen are summarized in Table 2. Twenty-nine separate determinations of each productivity parameter were made for each tank during the last 40 days of the experiment. Tank means in g C me2 d-l for gross primary productivity ranged from 5.9 to 6.7. Tank means for net primary productivity ranged from 2.6 to 4.9.
I-
0
IO
20
5o Days
40
50
‘2
60
J
70s
g
50
0
io
20
3O
40
50
60
Days
Fig. 3. Fish growth during the feed conversion experiment: (a) for the fish population on an area1 basis, and (b) on an individual fish basis. Numbers beside lines are tank numbers.
J.A. COLMAN ET AL.
36
cl
z
1
Mean
Nifrite
.a
(mg N 7’)
Fig. 4. Average fish productivity rates and nitrite concentrations over the 62-day period of the feed conversion experiment. Tank numbers are shown above the bars. Each bar represents the average of 18 nitrite observations.
The carbon presentation rates and feed conversion ratios (FCR) of phytoplankton to fish, septage to fish, and combined sources to fish are given in Table 2. A wide range of FCR values was observed, mainly reflecting variation in fish growth rather than in organic matter input. DISCUSSION
Sustained high fish productivity occurred in individual tanks in both experiments: 5.3 g m-2 d-l for 55 days, Experiment 1; and 4.5 g m-’ d-’ for 62 days, Experiment 2; both results at 5 fish m-2. These levels average 63% higher than the previously reported maximum rate of 2.5-3.5 g m-’ d-’ (Schroeder, 1987a, 1987b; Wohlfa~h and Hulata, 1987). A maximum fish biomass increase of 8.8 g m-’ d-’ was obtained in one tank (5 fish mm2) during Experiment 1 in the 14-28 day interval after fish were stocked. These experimental results indicate that there is no fundamental factor limiting fish production to the 3.5 g mm2 d- ’ level. However, achieving the high levels was not routine and the average production for the five tanks stocked at 5 fish mm2 was only 1.7 g m-2 d-‘. The poorest fish growth rate in Experiment 2 was obtained in tank number 2, which was also unique because of the predominance of the green alga Sce-
FISH PRODIJCTION IN MANURED ~ATIC-EATER
PONDS
37
nedesm&a during the latter 40 days of the 62-day experiment. Poor assimilation of Scenedesmus may have contributed to the low fish productivity of tank number 2. Substantially reduced assimilation rates of green algae compared to blue-green algae by tilapia have been reported (Moriarty and Moriarty, 1973; McDonald, 1985a). In fact, the Microcystis dominance that characterized all the other tanks in both experiments may have been instrumental in suppo’rting high fish growth rates. Other fertilized tank experiments involving green algae and tilapia have shown low fish productivity (Gaigher, 1982; Pierce, l983; McDonald, 1985b) or have even shown specifically that fish did not gain nutrition from green algae (Schroeder, 1983 ). The apparent grazing of ~~c~oc~~~~j~ by tilapia did not lead to species succession as reported previously in tank culture (Pierce, 1983). Factors that may have contributed to the persistance of Microcystis in the tanks in this study were the high fertilization rate of nitrogen and the high pH. Microcystis has an u:nusually high requirement for nitrogen and grows best at pH 10 (Gerloff et al., 1952; Gerloff and Skoog, 1954). Furthermore, experiments using translucent-sided tanks (Pierce, 1983) may have eliminated the competitive advanta:ge of blue-green algae which shade other phytoplankton by growth at the surface of the water which is mediated by bouyancy regulation (Reynolds, 1984). An unsuitable chemical environment also may have cont~buted to reduced fish growth in some tanks. Some previous attempts to grow fish (guppy, Poecilia retz’culatu,and common carp, Cyprinus carpio) in tanks optimized for blue-green algal culture met with 100% fish mortality a few days after stocking fish (Venkataraman, 1983). High pH and occasional low early morning dissolved oxygen found in the tanks of the present study may not be as severe a problem for tilapia as for some other fish species (Chervinski, 1982). Of the other parameters measured, only nitrite reached concentrations likely to slow growth or cause mortality. Colt et al. ( 198 I ) found that growth of juvenile catfish (~c~~~~~~spunctatus) was reduced by nitrite levels of 1.6 mg N 1-l and above, and that mortality increased significantly at levels of 3.7 mg N l- ’ and above, Indeed, a correlation appeared to exist between average nitrite concentration (up to 6 mg N l- ’ ) and decreased fish productivity in Experiment 2 in which nitrite concentration was monitored (Fig. 4). Tank number 2 was art outlier in this trend but low fish productivity may have been due to green algal dominance as discussed above. The case for growth inhibition by nitrite based on these data is not strong. The correlation between growth increment and average nitrite concentration during a growth measurement interval was actually slightly negative. If low fish productivity can be explained by the factors discussed above, the high fish productivity rates obtained may indicate that a balance of phytoplankton productivity and harvest can increase fish yield in manured ponds beyond previous limits as hypothesized. The hypothesis is strengthened by
38
J.A. COLMAN ET AL.
the pattern of growth as a function of tank stocking density which occurred in Experiment 1 (Fig. 1). Highest fish growth rates occurred at an inte~ediate stocking density (5 fish mm2) as predicted by the hypothesis, possibly when an optimal balance of phytoplankton productivity and harvest of phytoplankton biomass by fish occurred. A notable feature of the dissolved oxygen and ammonia concentrations in Experiment 1 was their optimal values for fish culture, high oxygen and low ammonia, in the tanks with highest fish productivity and presumed highest phytoplankton productivity. This again supports the working hypothesis because it can be shown from the stoichiometry of the photosynthesis reaction that a balance, one that produces maximum phytoplankton productivity, would also be optimal for oxygen generation (Colman and Edwards, 1987 ). When photosynthesis was measured in Experiment 2, the lowest mean gross and highest mean net phytoplankton productivities (excluding the Scene&smus tank, No. 2 ) were observed in tank 8 (Table 2 ), in which the largest fish biomass increase occurred. Chlorophyll a standing crop was also lowest in tank 8. Apparently, the smallest standing crop of phytoplankton had the largest net productivity, and presumably the largest fish biomass increase was supported by the largest consumption of ph~oplankton biomass by fish. Primary productivity measurements enabled a comparison to be made with those typical of mass algal culture. Assuming that net phytoplankton productivity in g C per time can be converted to dry weight ph~oplankton biomass gain by multiplying by 2 (factor found by Algren ( 1983 ) for conversion of g C to biomass for blue-green algae), the mean tank phytoplankton productivity rates obtained during Experiment 2 ranged from 5.1 to 9.8 g dry weight m-* d- ‘, or only about one-third of the 15-25 g m-* d- ’ productivity that is routine in mass algal culture (Goldman, 1979). However, mass algal culture involves carefully controlled and mechanically mixed cultures of green algae. Algal culture systems using the blue-green alga Spirulina are closer to the tank conditions reported in this study and result in similar algal yields. Venkataraman ( 1983) reported Spirulina yields of 8-12 g m-2 d-’ at the Central Food Technolgical Research Institute (CFTRI), Mysore, India, and at the commercial algal production unit of Sosa Texcoco, Mexico. Highly efficient conversion of phytoplankton biomass to fish occurred in some tanks as indicated by low FCR for algae to fish (Table 2). However, this interpretation is confounded by the septage fertilizer which represented an additional source of organic carbon that may have supplemented the fish diet. The second highest net primary productivity occurred in tank number 8 in which the highest sustained fish productivity was found. Relatively efficient conversion of both algal and septage carbon must have occurred in this tank because the combined FCR of phytoplankton and septage was only 3.1 f even with the poor nitritional values of most waste-carbon sources. A waste input must first be converted to bacterial carbon to contribute to fish nutri-
FISH PRODU(~lON
IN MANURED STATIC-WATER PONDS
39
tion, a process which is about 35% efficient on a carbon-to-carbon basis (Schroeder, 1978). The rat her low adjusted FCR of 2.4 for the sustained high productivity tank indicates that both phytoplankton and bacteria were efficiently converted to fish biomass. Although different experimental systems may not be strictly comparable, the fish productivity at the optimal fish stocking density was substantially higher than that previously reported for manured ponds. The dependency of fish growth rate and oxygen supply on stocking treatment was in accord with the hypothesis of optimal balance between ph~oplan~on standing crop and productivity, and harvesting. Management to achieve the highest possible rate of phytoplankton productivity goes against most conventional advice in which excessive phytoplankton growth is viewed as a problem (Laws and Malecha, 198 1; Boyd, 1982; Smith, 1985 ). The dominance of the tanks by Microcystis, an exceptionally assimilable alga for tilapia, may account in part for the new findings. Fish culture systems dominated by either relatively indigestible algae and/or devoted to non-phytophagous fish species may be expected to develop algal standing crops in excess of the optimum. However, for optimal growth of phytophagous fish, not only must phytoplankton generation and consumption be balanced, but water quality must be suitable for fish growth. It has been demonstrated that previously reported limits to fish productivity in manured ponds may not be absolute and that higher rates may depend on a balance between productivity and harvesting of the readily assimilable Microcystis by phytophagous Nile tilapia. However, relatively sophisticated pond management relating to algal species dominance, adjustment of the rapidly growing fish population to the desirable range for algal harvesting, and control of concentrations of growth-slowing metabolic products, may also be required to realize such improved yields. ACKNOWLEDGEMENTS
This research was supported by the Asian Institute of Technology, The International Center for Living Aquatic Resources Management, and a Rockefeller Foundation Fellowship to John A. Colman. Peter Edwards is seconded to the Asian Institute of Technology by the Overseas Development Administration, U.K.
REFERENCES Algren, G., 1983. Comparison of methods for estimation of phytoplankton carbon. Arch. Hydrobiol., 9%:489-508. American Public Health Association, American Water Works Association and Water Pollution
40
J.A. COLMAN ET AL.
Control Federation, 1980. Standard Methods for the Examination of Water and Wastewater, 15th edition. American Public Health Association, Washington, DC, 1260 pp. Banks, R.B. and Herrera, F.F., 1977. Effect of wind and rain on surface reaeration. J. Environ. Eng. Div., Am. Sot. Civ. Eng., 103: 489-504. Bannister, T.T., 1979. Quantitative description of steady state, nut~ent-saturated algal growth, including adaptation. Limnol. Oceanogr., 24: 76-96. Berner, T., Dubinsky, Z., Schanz, F., Grobbelar, J.U., Rai, H., Uelinger, U. and Falkowski, P.G., 1986. The measurement of primary productivity in a high-rate oxidation pond (HROP). J. Plankton Res., 8: 659-672. Boyd, C.E., 1982. Water Quality Management for Pond Fish Culture. Elsevier Science Publishers, New York, NY, 3 18 pp. Chervinski, J., 1982. Environmental physiology of tilapias. In: R.S.V. Pullin and R.H. LoweMcConnell (Editors), The Biology and Culture of Tilapias. ICLARM Conference Proceedings 7, International Center for Living Aquatic Resources Management, Manila, Philippines, pp. 119-128. Colman, J.A. and Edwards, P., 1987. Feeding pathways and environmental constraints in wastefed aquaculture: balance and optimization. In: D.J.W. Moriarty and R.S.V. Pullin (Editors), Detritus and Microbial EcoIogy in Aquaculture. ICLARM Conference Proceedings 14, International Center for Living Aquatic Resources Management, Manila, Philippines, pp. 240281. Colt, J., Ludwig, R., Tchobanoglous, G. and Cech, J.J., Jr., 1981. The effects of nutrite on the short-term growth and survival of channel cattish, Ictaluruspunctatus.Aquaculture, 24: 1I l122. Edwards, P., Sinchumpasak, O.A. and Tabucanon, M., I98 1. The harvest of microalgae from the effluent of a sewage fed high rate stabilization pond by Tilapia nilotica. Part 2: Studies of the fish ponds. Aquaculture, 23: 107- 147. Gaigber, I.G., 1982. The growth and production of Mozambique tilapia (O~eoc~ro~~s mossumbicus) fed on aigae in small tanks. Water South Africa, 8: 142-I 44. Gerloff, G.C. and Skoog, F., 1954. Cell contents of N and P as a measure of their availability for growth of %crocystis aeruginosa. Ecology, 35: 348-353. Gerloff, G.C., Fitzgerald, G.P. and Skoog, F., 1952. The minimal nutrition of Microcystisaeruginosa. Am. J. Bot., 39: 26-32. Goldman, J.C., 1979. Outdoor algal mass cultures. II. Photosynthetic yield limitations. Water Res., 13: 119-136. Hall, C.A.S. and Mall, R., 1975. Methods of assessing aquatic primary productivity. In: H. Lieth and R.H. Whittaker (Editors), Primary Productivity ofthe Biosphere. Springer-Verlag, New York, NY, pp. 19-53. Laws, E.A. and MaIecha, S.R., 1981. Application of a nutrient-saturated growth model to phytoplankton management in freshwater prawn (Macrobrachbm rusenbergii) ponds in Hawaii. Aquaculture, 24: 91-101. Lewis, W.M., 1974. Primary production in the plankton immunity of a tropical lake. Ecol. Monogr., 44: 377-409. McConnell, W.J., l962. Productivity relations in carboy microcosms. Limnol. Oceanogr., 7: 335-343. McDonald, M.E., 1985a. Carbon budgets for a phytoplanktivorous fish fed three different unialgal populations. Oecologia (Berlin), 67: 246-249. McDonald, M.E., 198513.Growth of a grazing phytoplanktivorous fish and growth enhancement of the grazed algae. Oecologia (Berlin), 67: 132-l 36. Moriarty, C.W. and Moriarty, D.J.W., 1973. The assimilation of carbon from phytoplankton by two herbivorous fishes: Tiahpianiloticusand Haplochromis nigripinnus.J. Zool., 17 1: 4 l55.
FISH PRODUCTION IN MANURED STATIC-WATER PONDS
41
Pierce, B.A., 1983. Biotic effects of grazing by tilapia (Oreochromis aureus) on phytoplankton populations in solar silos. J. Freshwater Ecol., 2: 293-304. Reynolds, C.S., 1984. The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridlge, 384 pp. Schroeder, G.L., 1978. Autotrophic and heterotrophic production of microorganisms in intensely manured fish ponds and related fish yields. Aquaculture, 14: 303-325. Schroeder, (G.L., 1983. Stable isotope ratios as naturally occurring tracers in the aquaculture food web. Aquaculture, 30: 203-210. Schroeder, G.L., I987a. Carbon pathways in aquatic detrital systems. In: D.J.W. Moriarty and R.S.V. Pullin (Editors), Detritus and Microbial Ecology in Aquaculture. ICLARM Conference Proceedings 14. International Center for Living .4quatic Resources Management, Manila, Philippines, pp. 2 17-236. Schroeder, G.L., 1987b. Carbon and nitrogen budgets in manured fish ponds on Israel’s coastal plain. Aquaculture, 62: 259-279. Smith, D.W., 1985. Biological control of excessive phytoplankton growth and the enhancement of aquacultural production. Can. J. Fish. Aquat. Sci., 42: 1940-1945. Venkataraman, L.V., 1983. A Monograph on Spirulina platensis - Biotechnology and Application. Department of Science and Technology, New Delhi, India, 100 pp. Wohlfarth, G.W. and Hulata, G., 1987. Use of manures in aquaculture. In: D.J.W. Moriarty and R.S.V. Pulhn (Editors), Detritus and Microbial Ecology in Aquaculture. ICLARM Conference Proceedings 14, International Center for Living Aquatic Resources Management, Manila, Philippines, pp. 353-367.
Aquaculture, 89 (1990) 27-41 Elsevier Science Publishers B.V., Amsterdam
Extending the limits of fish production in manured static-water ponds*
John A. Colman’, Peter Edwards, Manoj Yomchinda Pacharaprakiti
and Chintana
Asian institute of Technology, Agricultural and Food Engineering Division, GPO Box 2754, Bangkok (Thailand) (Accepted 22 December
1989)
ABSTRACT
Colman, J.A., Edwards, P., Yomchinda, M. and Pacharaprakiti, C., 1990. Extending the limits of fish product [on in manured static-water ponds. Aquaculture, 89: 27-4 1. A working hypothesis was adopted that previously reported limits to fish productivity in manured static-water systems (2.5-3.5 g fish m-’ dd’) are derived from an imbalance between phytoplankton productivity and harvest by tish. The assumption that an improved balance would result in greater net generation of oxygen, and phytoplankton and fish productivities was tested in a series of outdoor fertilized concrete tanks in which phytoplankton harvesting was regulated by varying the stocking density (mnge 0.5-10 fish m-‘) of the phytophagous Nile tilapia (Oreochromis niloticus). The resulting patterns of fish growth rates and dissolved oxygen concentrations at various fish stocking densities supported the phytoplankton balance hypothesis. Oxygen concentrations at dawn and growth per fish were lowest at low fish stocking densities, 0.5 and 1.0 fish m-*, where presumably the large standing crop of algae was grazed too slowly to stimulate algal growth. The highest tank fish productivity measured, 8.8 g fish me2 at 5 fish m-*, was well above previously reported levels but was sustained for only 2 weeks. However, the two highest sustained tank fish productivities of 4.5 and 5.3 g fish m-’ dd’ averaged 63% higher than the average of previously reported-maxima. These results indicate that higher growth rates on an area1 basis are possible than have previously been reported. However, iachieving growth at the highest rate was not routine. The average growth of five tanks stocked with 5 fish m-’ was only 1.7 g m-’ dd’. Microcystis, the algal taxon that dominated all but one experimental tank, may have been important for high fish productivity. At the optimal fish stocking density of 5 fish m-‘, nitrite build-up may have limited fish productivity in some tanks. Feed conversion ratios based on phytoplankton as feed ranged from 4.0 to 0.9 at 5 fish m-‘; based on phytoplankton and organic fertilizer as feeds they ranged from 10.7 to 3.1. *ICLARM Contribution No. 237. Paper presented at the 2nd International Conference on Warm Water Aquaculture - Finfrsh, 5-8 February 1985, Brigham Young University, HI (U.S.A.). ‘Present address and correspondence: U.S. Geological Survey, 102 E. Main St., Urbana IL 61801 (U.S.A.).
0044-8486/90/$03.50
0 1990 -
Elsevier Science Publishers
B.V.
28
J.A. COLMAN ET AL.
INTRODUCTION
There appears to be a maximum fish yield of approximately 2.5-3.5 g m-’ d-’ (25-35 kg ha-’ dd’ or 9-l 3 tons ha-’ yr- ’ ) in manured static-water fish ponds from several countries with a range of fish species and types of manure (Schroeder, 1987a,b; Wohlfarth and Hulata, 1987 ). Extrapolated net fish yields of 5.5 g rnw2 dd’ were reported for a system in which Nile tilapia (0. niloticus) were fed phytoplankton, but the algae were pumped through concrete fish tanks from a sewage-fed high rate stabilization pond and were not produced in situ as in a manured fish pond (Edwards et al., 198 1). A working hypothesis of productivity-limiting factors in manured ponds, developed by Colman and Edwards ( 1987 ) , was adopted for the present investigation: that an imperfect balance between primary productivity and phytoplankton harvest by phytophagous fish limits net algal productivity and fish yield in current practice. Net algal productivity is important in phytophagous fish culture because it represents production of fish food and net production of oxygen. Both algal growth equations and experimentation with continuous algal biomass culture indicate that maximal net phytoplankton productivity in nutrient-sufficient, light-limited culture occurs when the algal standing crop size is maintained at an intermediate level (Goldman, 1979). Net primary productivity generally increases with increasing phytoplankton standing crop because of increased reproducing stock. However, at very high levels of phytoplankton standing crop, self-shading becomes important and continued standing crop increase leads to lower net primary productivity. The stocking density of phytophagous fish was varied in an initial experiment in a series of outdoor concrete tanks to provide different rates of phytoplankton harvest by fish. This investigation sought to find whether an optimal-sized phytoplankton standing crop could be approached by substituting fish cropping of algae for the mechanical harvesting used in continuous algal biomass culture. It was expected that grazing pressure would approach an optimal rate for phytoplankton productivity at one of the fish stocking densities used, with concomitant optimal fish yield. Phytoplankton productivity and rates of conversion of phytoplankton biomass and organic carbon inputs to fish were determined in tanks in a second experiment under stocking conditions which produced the highest fish yield in the first experiment. Methods to estimate net phytoplankton productivity, which is required for the calculation of food conversion ratios (FCR ), remain to be standardized. Even recent methodological comparisons of the measurement of gross primary productivity (GPP) in hyper-eutrophic systems revealed no agreement between methods (Bemer et al., 1986); the determination of net phytoplankton productivity (GPP less phytoplankton respiration) is still more problematical. The best available methods for primary productivity determination
29
FISH PRODLICTION IN MANURED STATIC-WATER PONDS
have been used in this study - oxygen change, appropriate for hypertrophia (Berner et al., 1986 ), in unconfined tanks to avoid bottle effects (McConnell, 1962; Hall and Moll, 1975). Although the net phytoplankton productivity values reported here have uncertain accuracy, they are useful for comparisons between tanks and experiments in which the same methodology is used; and they are a useful beginning in computing the FCR of phytoplankton produced in situ as a food source for phytophagous fish. MATERIALS AND METHODS
Experiment 1 - stocking density Fish were stocked in 4.8-m3 outdoor concrete tanks at six stocking densities in triplicate. Tank inputs were septage (slurry from septic tanks and cesspools) and inorganic fertilizers. Nets lined the insides of the tanks to facilitate fish samlpling. The tanks were tilled with water from a surface source (total alkalinity 300-400 mg CaC03 l- ’ ) to a depth of 1 m. A 28-day start-up period was begun on 23 January 1984 to allow phytoplankton to develop in the tanks. Four Nile tilapia (0. niloticus) of mean weight 44 g were added to each tank during the start-up period to condition the water and to control insect larvae. The fish were obtained from a local commercial hatchery. Fertilizers were applied in three doses per week, equivalent to the daily rates shown in Table 1. Inorganic fertilizers were dissolved in water before addition, except for iron, which was added as a slurry. The four fish in each tank were removed on 20 February and male tilapia of mean weight 77 g were stocked. Three replicates of the following stocking density treatments were used: 0, 0.5, 1, 2, 5, 10 fish m-‘. A random assignment of treatments to tanks was used. Tank fertilization was continued at approximately three doses per week after stocking fish. Water was not circuTABLE 1 Fertilizer input rates Fertilizer
Potassium
nitrate
Triple superphosphate FeSO,.7H,O Septage
Weight of fertilizer (g tank-’ dose-‘)
Nutrient equivalent (gm-‘d-l)
120
K -4.16 N - 1.50 P -0.22 Fe - 0.25” Organic C - 3b N - 0.42 P -0.13
12 14 5 (litres)
“Iron addition was reduced 10 fold in Experiment 2. bEstimated from measured chemical oxygen demand.
30
J.A. COLMAN ET AL.
lated through the tanks. Evaporative losses were replaced by fertilizer inputs and by make-up water. Chemical monitoring of 12 tanks, two tanks per treatment, was initiated after stocking fish. Water samples were obtained by pumping from 30-cm depth. Sampling was at approximately 8 a.m., before water column mixing was inhibited by temperature stratification (temperature measurements indicated that tanks mixed vertically every night). Samples for analysis of solutes were collected first; then the tanks were stirred to suspend particulate matter evenly and samples for chlorophyll a analysis were taken. Standard chemical analytical procedures were used (American Public Health Association et al., 1980). Ammonia (phenate method), chlorophyll a (acetone extraction with tissue grinding) and dissolved oxygen (Winkler method with the azide modification) were measured twice weekly. Additional samples for dissolved oxygen were taken weekly at dawn (6 a.m.). Determinations of pH, alkalinity and nitrite (spectroscopic, diazotization method) were made in selected tanks towards the end of the experiment. Fish growth was determined by batched weighing of fish from each tank at 14-day intervals. Fish were anaesthetized with quinaldine during weighing. Dominant phytoplankton genera were monitored subjectively by a visual estimation of abundance in percent of total biomass by microscopic observation approximately every 2 weeks. Experiment 2 -feed conversion Only one stocking density, 5 fish rnp2, was used. The culture method was similar to the previous experiment but with more complete monitoring of tank conditions. The phytoplankton growth start-up period was begun on 4 April 1984 and continued for 28 days until 2 May when fish were stocked. Fertilizer additions were again made three times per week (Table 1 ), although the amount of iron was reduced to 10% of the amount given in the first experiment. Tilapia of mean weight 70 g were stocked in nine tanks, 25 fish per tank. Monitoring of phytoplankton genera and fish sampling was as for Experiment 1. Water was sampled and analyzed as for Experiment 2 but nitrite was included with the parameters measured twice weekly. Diurnal pH and chemical oxygen demand (COD) (macromethod with dichromate reflux) were measured once per week. Primary productivity In addition to measuring dissolved oxygen at 6 a.m. in Experiment 2, dissolved oxygen was measured at the surface at 10 a.m. and 2 p.m. and in depth profile ( IO-cm intervals) at 6 p.m. 5 days per week beginning 3 weeks after the fish were stocked. Die1 whole-tank oxygen changes were computed from
FISH PRODUCTION
IN MANURED
STATIC-WATER
PONDS
31
these measurements and were used to estimate primary productivity (in the manner of McConnell ( 1962 ) and Hall and Moll ( 1975 ) ) as follows: mean wind speeds at the times of the surface oxygen measurements were used to correct for oxygen transfer across the air-water interface according to Banks and Herrera ( 1977). The corrected values were converted to gross primary productivity (GPP, g C rnB2 d-l) by adding the 12-h night community respiration to the daylight oxygen increase and converting from oxygen to carbon GPP= (NWCP+NPR)K,/K, where NWCP= the corrected daylight oxygen change (g O2 me2 d-l), NPR= the corrected night oxygen change (g O2 rnw2 d-l), K, =0.38, grammolecular weight ratio (C/O,), and K2= 1.2, the photosynthetic quotient (0,/C: molar basis; Lewis, 1974). Net phytoplankton productivity (NAP, g C me2 b’ ) was calculated by subtracting phytoplankton respiration, estimated by the product of phytoplankton standing crop and respiration rate (AR) NAP = GPP - Chla*lil,* AR where Chla= standing crop of chlorophyll a (g m-‘), KS= 44 (g C g Chla- ‘; Algren: 1983, for Oscillutoria), and AR= 0.07, respiration rate (d- ’ ) (Bannister, 1979), Evaluation of standing crop by chlorophyll a measurement and conversion to carbon is undesirable because of variability of K3. The conversion is necessary because direct measurements of carbon would not be specific to phytoplankton carbon. A wide range for AR is reported in the literature (Berner et al., 1986). The decision to base AR on the value reported in the Bannister model ( 1979) for respiration of Chlorelluat 26 oC was in part arbitrary. However, a model using this value accurately predicted oxygen concentration in freshwater prawn tanks and ponds which also contained some tilapia in Hawaii (Laws and Malecha, 198 1). Feed conversionratios Orga.nic carbon loading of septage to the tanks was estimated from measured chemical oxygen demand of the septage. The conversion factor used, 2.7 g 0, per gram of organic carbon, assumed an average oxidation state of the septage carbon equivalent to carbohydrate. Possible values for the factor vary from 4.4 for hydrocarbon to 1.3 for organic acids. The accuracy of the estima-tion used is unknown. The organic carbon loading was summed with the appropriate net primary productivity value to give the organic carbon loading rate (Table 2 ) . Organic carbon was converted to dry weight organic matter using a factor of 2 ( Algren, 1983 ) to generate the FCR on a dry weight organic matter to fresh weight fish basis. The accounting of carbon supply and fish growth to estimate FCR was started 3 weeks after fish were stocked to
32
J.A. COLMAN ET AL.
TABLE 2 Primary productivity and feed conversion ratios (dry weight organic matter to wet weight fish basis); numbers in parentheses are standard deviations, where n=29 Parameter
Tank no. 2
Gross primary productivity (gCm-‘d-l) Net primary productivity (gCm-2d-‘)a Organic carbon loading (gCm-2d-‘) Phytoplankton to fish FCRb Septage to fish FCRb Phytoplankton and septage to fish FCRb
3 (61..23 ) (4p ) 7.9
-7.1 -4.4 -11.5
6
-
6.4
8
14 6.1 (2.1) 2.6 (2.6) 5.6
( 1.3)
(Z)
5.9 (1.5)
3.8 (1.4) 6.8
(S:;) 6.2
(Z, 6.9
3.1 2.5 5.6
7.1 6.7 13.8
1.8
“Assumes a phytoplankton respiration rate of 0.07 d-l, see Methods. bNegative values occurred when fish lost weight during the 42-day measurement
1.4 3.3
2.6 2.9 5.3
interval.
minimize the effect on the computation of fish feeding on food organisms which had developed in the tanks during the pre-stocking period. RESULTS
Experiment 1 The addition of organic and inorganic fertilizers caused dense phytoplankton blooms to develop in the tanks by the time fish were stocked. Chlorophyll a concentrations increased from 0.6-0.7 mg 1-r just before fish stocking to 1.O mg I- ’ in the week after stocking , There did not appear to be any pattern of chlorophyll a change after fish stocking, nor any correlation between fish stocking density and chlorophyll a concentration. The dominant genus of phytoplankton ( > 90%) found in all tanks on the four occasions of examination was Microcystis. Other genera present were Chlamydomonas, Chroococcus, Pandorina and at the beginning of the experiment, diatoms. Mean fish growth in terms of biomass increment per area and weight increment per individual fish as a function of time and stocking density are presented in Fig. 1. Mean growth rate at 5 fish me2 remained above 5 g m-’ d-’ for the fist month after stocking. One tank at this stocking density averaged 5.3 g m-2 d-r growth for the first 55 days after stocking; during the 14-28day interval after stocking, growth rate in this tank was 8.8 g me2 d-l. Data were not considered from tanks in which more than 20% fish mortality occurred because significant mortality altered the treatments by changing the stocking density. Initially, weight increments both per fish and on an area1
FISH PRODUCTION IN MANURED STATIC-WATER PONDS
(b)
(a) 7
0.51
fi
^ <
2.ot
f
-0 .? f
Growth
Period
Fig. 1. Fish growth during the stocking density experiment; (a) on an individual fish basis, and (b) for the fish population on an area1 basis. Each bar refers to growth during the previous 14 days (time interval 1, O-l 3 days; 2, 14-27 days; 3, 28-41 days). Data from tanks with more than 20% mortality are not displayed. Numbers in parentheses above the bars indicate the number of tanks averaged when less than 3. The vertical lines above or below the bars equal one-half standard error. The numbers below the bars indicate fish stocking density in number of fish me2.
basis increased with an increase in stocking density up to 5 fish mm2 and then decreased at the highest stocking level of 10 fish rne2. By the time of the last weighing at 6 weeks, the increment of the 1-fish mm2 treatment was the largest on a per fish basis, although the 5&h rnT2 treatment continued to produce the largest increment on an area1 basis. An mdication of fish mortality is also given in Fig. 1 where tanks in which more than 20% mortality occurred are not represented. This level was reached in the highest and lowest stocking density treatments. The 6 a.m. dissolved oxygen concentrations of individual tanks fluctuated over a 5-8 mg 1-l range, with a period of approximately 6 days. The total range alcross all treatments was O-10 mg l- ’ with some treatments tending towards the upper portion of this range and others towards the lower portion. These trends are expressed, by treatment, as means for the first 28 days after fish stocking (Fig. 2). After 28 days, dissolved oxygen data obtained by the Winkler method were not accurate because of chemical interference from the large arnounts of iron put in the tanks as a fertilizer. Ammonia levels also fluctuated within a given tank during the experiment, but more slowly than dissolved oxygen. Mean concentrations by treatment for the first 28 days after stocking were negatively correlated with oxygen {Fig. 2 ).
34
J.A.COLMAN ETAL. 18,
I 16
T
1.4 _I _- 1.2b z 9 1.0-O 9 c :08Q = 0.6'0 I040.2I
0
2
I
1
I
4
6
a
Fish
Stocking
0 Denwty
I
I
2
4
(number
6
t
/
8
IO
mm*)
Fig. 2. Average early morning dissolved oxygen and total ammonia during the first 28 days of the stocking density experiment. The number of observations averaged for each treatment was i4 and 44 for total ammonia and dissolved oxygen, respectively. Error bars represent one standard deviation above and below the mean.
Nitrite measurements were made only for the Wish m-2 treatment and only on day 57, after other treatments had been terminated, and concentrations found in the three tanks were 0.58,0.62 and 1.49 mg N 1-l. Total alkalinity and pH measurements were also measured on day 57 for these three tanks, with means of 580 mg CaC03 l- ’ and pH 10.0. Experiment 2 A heavy ph~oplan~on bloom developed during the 28-day start-up period as in the first experiment. Chlorophyll a concentrations again ranged around 1.O mg 1-r. However, despite an equal stocking density of 5 fish mm2 in all tanks in this experiment, tank number 8 had a significantly lower mean chlorophyll a concentration, 0.75 mg l- ‘, than the mean of the other tanks, 1.10 mg I-‘. The phytoplankton dominance at the time of fish stocking in this experiment was ~~c~o~~~~~,70% of the total biomass of ph~oplan~on (mean for all tanks) but dropped to 45% Micrucystis-55% Chroococcusthe following week. There was a gradual return to Microcystis dominance, which by experiment day 49 was greater than 90%. An exception was tank number 2, not included in the above results, in which Scenedesmuspredominated from day 22 (90- 100%) until the end of the experiment.
FISH PRODlJCTlON IN MANURED STATIC-WATER PONDS
35
Mortality was a problem immediately after stocking fish in Experiment 2. Four of .the nine tanks stocked lost three or more fish by the ninth day after stocking and were dropped from the experiment. All observations and results refer to t.he five remaining tanks. Fish biomass (per meter squared and per fish basis) as a function of time is shown. in Fig. 3. A range of fish growth rates occurred from essentially zero during the last 40 days of the 62-day experiment (tank number 2) to a mean growth of 4.5 g m-* d-l over the entire 62-day period (tank number 8 ). Fish mortality accounts for differences between per fish and per area growth curves for a given tank. Final fish densities ranged from 3.8 to 4.4 fish mV2 with the exception of tank 2, which decreased from 4.0 to 3.1 fish m-’ during the last 2-week interval. Early morning dissolved oxygen and ammonia concentrations were in the same range in the two experiments, but large concentrations of nitrite were found in Experiment 2. Concentrations of nitrite were in the 1-4 mg N 1-l range before fish were stocked. Concentrations fell to below 0.5 mg N 1-l from day 15 through day 33 after stocking .Nitrite then increased again in some tanks to as much as 6 mg N l- ‘. The relationship between fish growth (per area) and average nitrite concentration is shown in Fig. 4. Net and gross primary productivities calculated from the measured daily changes in dissolved oxygen are summarized in Table 2. Twenty-nine separate determinations of each productivity parameter were made for each tank during the last 40 days of the experiment. Tank means in g C me2 d-l for gross primary productivity ranged from 5.9 to 6.7. Tank means for net primary productivity ranged from 2.6 to 4.9.
I-
0
IO
20
5o Days
40
50
‘2
60
J
70s
g
50
0
io
20
3O
40
50
60
Days
Fig. 3. Fish growth during the feed conversion experiment: (a) for the fish population on an area1 basis, and (b) on an individual fish basis. Numbers beside lines are tank numbers.
J.A. COLMAN ET AL.
36
cl
z
1
Mean
Nifrite
.a
(mg N 7’)
Fig. 4. Average fish productivity rates and nitrite concentrations over the 62-day period of the feed conversion experiment. Tank numbers are shown above the bars. Each bar represents the average of 18 nitrite observations.
The carbon presentation rates and feed conversion ratios (FCR) of phytoplankton to fish, septage to fish, and combined sources to fish are given in Table 2. A wide range of FCR values was observed, mainly reflecting variation in fish growth rather than in organic matter input. DISCUSSION
Sustained high fish productivity occurred in individual tanks in both experiments: 5.3 g m-2 d-l for 55 days, Experiment 1; and 4.5 g m-’ d-’ for 62 days, Experiment 2; both results at 5 fish m-2. These levels average 63% higher than the previously reported maximum rate of 2.5-3.5 g m-’ d-’ (Schroeder, 1987a, 1987b; Wohlfa~h and Hulata, 1987). A maximum fish biomass increase of 8.8 g m-’ d-’ was obtained in one tank (5 fish mm2) during Experiment 1 in the 14-28 day interval after fish were stocked. These experimental results indicate that there is no fundamental factor limiting fish production to the 3.5 g mm2 d- ’ level. However, achieving the high levels was not routine and the average production for the five tanks stocked at 5 fish mm2 was only 1.7 g m-2 d-‘. The poorest fish growth rate in Experiment 2 was obtained in tank number 2, which was also unique because of the predominance of the green alga Sce-
FISH PRODIJCTION IN MANURED ~ATIC-EATER
PONDS
37
nedesm&a during the latter 40 days of the 62-day experiment. Poor assimilation of Scenedesmus may have contributed to the low fish productivity of tank number 2. Substantially reduced assimilation rates of green algae compared to blue-green algae by tilapia have been reported (Moriarty and Moriarty, 1973; McDonald, 1985a). In fact, the Microcystis dominance that characterized all the other tanks in both experiments may have been instrumental in suppo’rting high fish growth rates. Other fertilized tank experiments involving green algae and tilapia have shown low fish productivity (Gaigher, 1982; Pierce, l983; McDonald, 1985b) or have even shown specifically that fish did not gain nutrition from green algae (Schroeder, 1983 ). The apparent grazing of ~~c~oc~~~~j~ by tilapia did not lead to species succession as reported previously in tank culture (Pierce, 1983). Factors that may have contributed to the persistance of Microcystis in the tanks in this study were the high fertilization rate of nitrogen and the high pH. Microcystis has an u:nusually high requirement for nitrogen and grows best at pH 10 (Gerloff et al., 1952; Gerloff and Skoog, 1954). Furthermore, experiments using translucent-sided tanks (Pierce, 1983) may have eliminated the competitive advanta:ge of blue-green algae which shade other phytoplankton by growth at the surface of the water which is mediated by bouyancy regulation (Reynolds, 1984). An unsuitable chemical environment also may have cont~buted to reduced fish growth in some tanks. Some previous attempts to grow fish (guppy, Poecilia retz’culatu,and common carp, Cyprinus carpio) in tanks optimized for blue-green algal culture met with 100% fish mortality a few days after stocking fish (Venkataraman, 1983). High pH and occasional low early morning dissolved oxygen found in the tanks of the present study may not be as severe a problem for tilapia as for some other fish species (Chervinski, 1982). Of the other parameters measured, only nitrite reached concentrations likely to slow growth or cause mortality. Colt et al. ( 198 I ) found that growth of juvenile catfish (~c~~~~~~spunctatus) was reduced by nitrite levels of 1.6 mg N 1-l and above, and that mortality increased significantly at levels of 3.7 mg N l- ’ and above, Indeed, a correlation appeared to exist between average nitrite concentration (up to 6 mg N l- ’ ) and decreased fish productivity in Experiment 2 in which nitrite concentration was monitored (Fig. 4). Tank number 2 was art outlier in this trend but low fish productivity may have been due to green algal dominance as discussed above. The case for growth inhibition by nitrite based on these data is not strong. The correlation between growth increment and average nitrite concentration during a growth measurement interval was actually slightly negative. If low fish productivity can be explained by the factors discussed above, the high fish productivity rates obtained may indicate that a balance of phytoplankton productivity and harvest can increase fish yield in manured ponds beyond previous limits as hypothesized. The hypothesis is strengthened by
38
J.A. COLMAN ET AL.
the pattern of growth as a function of tank stocking density which occurred in Experiment 1 (Fig. 1). Highest fish growth rates occurred at an inte~ediate stocking density (5 fish mm2) as predicted by the hypothesis, possibly when an optimal balance of phytoplankton productivity and harvest of phytoplankton biomass by fish occurred. A notable feature of the dissolved oxygen and ammonia concentrations in Experiment 1 was their optimal values for fish culture, high oxygen and low ammonia, in the tanks with highest fish productivity and presumed highest phytoplankton productivity. This again supports the working hypothesis because it can be shown from the stoichiometry of the photosynthesis reaction that a balance, one that produces maximum phytoplankton productivity, would also be optimal for oxygen generation (Colman and Edwards, 1987 ). When photosynthesis was measured in Experiment 2, the lowest mean gross and highest mean net phytoplankton productivities (excluding the Scene&smus tank, No. 2 ) were observed in tank 8 (Table 2 ), in which the largest fish biomass increase occurred. Chlorophyll a standing crop was also lowest in tank 8. Apparently, the smallest standing crop of phytoplankton had the largest net productivity, and presumably the largest fish biomass increase was supported by the largest consumption of ph~oplankton biomass by fish. Primary productivity measurements enabled a comparison to be made with those typical of mass algal culture. Assuming that net phytoplankton productivity in g C per time can be converted to dry weight ph~oplankton biomass gain by multiplying by 2 (factor found by Algren ( 1983 ) for conversion of g C to biomass for blue-green algae), the mean tank phytoplankton productivity rates obtained during Experiment 2 ranged from 5.1 to 9.8 g dry weight m-* d- ‘, or only about one-third of the 15-25 g m-* d- ’ productivity that is routine in mass algal culture (Goldman, 1979). However, mass algal culture involves carefully controlled and mechanically mixed cultures of green algae. Algal culture systems using the blue-green alga Spirulina are closer to the tank conditions reported in this study and result in similar algal yields. Venkataraman ( 1983) reported Spirulina yields of 8-12 g m-2 d-’ at the Central Food Technolgical Research Institute (CFTRI), Mysore, India, and at the commercial algal production unit of Sosa Texcoco, Mexico. Highly efficient conversion of phytoplankton biomass to fish occurred in some tanks as indicated by low FCR for algae to fish (Table 2). However, this interpretation is confounded by the septage fertilizer which represented an additional source of organic carbon that may have supplemented the fish diet. The second highest net primary productivity occurred in tank number 8 in which the highest sustained fish productivity was found. Relatively efficient conversion of both algal and septage carbon must have occurred in this tank because the combined FCR of phytoplankton and septage was only 3.1 f even with the poor nitritional values of most waste-carbon sources. A waste input must first be converted to bacterial carbon to contribute to fish nutri-
FISH PRODU(~lON
IN MANURED STATIC-WATER PONDS
39
tion, a process which is about 35% efficient on a carbon-to-carbon basis (Schroeder, 1978). The rat her low adjusted FCR of 2.4 for the sustained high productivity tank indicates that both phytoplankton and bacteria were efficiently converted to fish biomass. Although different experimental systems may not be strictly comparable, the fish productivity at the optimal fish stocking density was substantially higher than that previously reported for manured ponds. The dependency of fish growth rate and oxygen supply on stocking treatment was in accord with the hypothesis of optimal balance between ph~oplan~on standing crop and productivity, and harvesting. Management to achieve the highest possible rate of phytoplankton productivity goes against most conventional advice in which excessive phytoplankton growth is viewed as a problem (Laws and Malecha, 198 1; Boyd, 1982; Smith, 1985 ). The dominance of the tanks by Microcystis, an exceptionally assimilable alga for tilapia, may account in part for the new findings. Fish culture systems dominated by either relatively indigestible algae and/or devoted to non-phytophagous fish species may be expected to develop algal standing crops in excess of the optimum. However, for optimal growth of phytophagous fish, not only must phytoplankton generation and consumption be balanced, but water quality must be suitable for fish growth. It has been demonstrated that previously reported limits to fish productivity in manured ponds may not be absolute and that higher rates may depend on a balance between productivity and harvesting of the readily assimilable Microcystis by phytophagous Nile tilapia. However, relatively sophisticated pond management relating to algal species dominance, adjustment of the rapidly growing fish population to the desirable range for algal harvesting, and control of concentrations of growth-slowing metabolic products, may also be required to realize such improved yields. ACKNOWLEDGEMENTS
This research was supported by the Asian Institute of Technology, The International Center for Living Aquatic Resources Management, and a Rockefeller Foundation Fellowship to John A. Colman. Peter Edwards is seconded to the Asian Institute of Technology by the Overseas Development Administration, U.K.
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Control Federation, 1980. Standard Methods for the Examination of Water and Wastewater, 15th edition. American Public Health Association, Washington, DC, 1260 pp. Banks, R.B. and Herrera, F.F., 1977. Effect of wind and rain on surface reaeration. J. Environ. Eng. Div., Am. Sot. Civ. Eng., 103: 489-504. Bannister, T.T., 1979. Quantitative description of steady state, nut~ent-saturated algal growth, including adaptation. Limnol. Oceanogr., 24: 76-96. Berner, T., Dubinsky, Z., Schanz, F., Grobbelar, J.U., Rai, H., Uelinger, U. and Falkowski, P.G., 1986. The measurement of primary productivity in a high-rate oxidation pond (HROP). J. Plankton Res., 8: 659-672. Boyd, C.E., 1982. Water Quality Management for Pond Fish Culture. Elsevier Science Publishers, New York, NY, 3 18 pp. Chervinski, J., 1982. Environmental physiology of tilapias. In: R.S.V. Pullin and R.H. LoweMcConnell (Editors), The Biology and Culture of Tilapias. ICLARM Conference Proceedings 7, International Center for Living Aquatic Resources Management, Manila, Philippines, pp. 119-128. Colman, J.A. and Edwards, P., 1987. Feeding pathways and environmental constraints in wastefed aquaculture: balance and optimization. In: D.J.W. Moriarty and R.S.V. Pullin (Editors), Detritus and Microbial EcoIogy in Aquaculture. ICLARM Conference Proceedings 14, International Center for Living Aquatic Resources Management, Manila, Philippines, pp. 240281. Colt, J., Ludwig, R., Tchobanoglous, G. and Cech, J.J., Jr., 1981. The effects of nutrite on the short-term growth and survival of channel cattish, Ictaluruspunctatus.Aquaculture, 24: 1I l122. Edwards, P., Sinchumpasak, O.A. and Tabucanon, M., I98 1. The harvest of microalgae from the effluent of a sewage fed high rate stabilization pond by Tilapia nilotica. Part 2: Studies of the fish ponds. Aquaculture, 23: 107- 147. Gaigber, I.G., 1982. The growth and production of Mozambique tilapia (O~eoc~ro~~s mossumbicus) fed on aigae in small tanks. Water South Africa, 8: 142-I 44. Gerloff, G.C. and Skoog, F., 1954. Cell contents of N and P as a measure of their availability for growth of %crocystis aeruginosa. Ecology, 35: 348-353. Gerloff, G.C., Fitzgerald, G.P. and Skoog, F., 1952. The minimal nutrition of Microcystisaeruginosa. Am. J. Bot., 39: 26-32. Goldman, J.C., 1979. Outdoor algal mass cultures. II. Photosynthetic yield limitations. Water Res., 13: 119-136. Hall, C.A.S. and Mall, R., 1975. Methods of assessing aquatic primary productivity. In: H. Lieth and R.H. Whittaker (Editors), Primary Productivity ofthe Biosphere. Springer-Verlag, New York, NY, pp. 19-53. Laws, E.A. and MaIecha, S.R., 1981. Application of a nutrient-saturated growth model to phytoplankton management in freshwater prawn (Macrobrachbm rusenbergii) ponds in Hawaii. Aquaculture, 24: 91-101. Lewis, W.M., 1974. Primary production in the plankton immunity of a tropical lake. Ecol. Monogr., 44: 377-409. McConnell, W.J., l962. Productivity relations in carboy microcosms. Limnol. Oceanogr., 7: 335-343. McDonald, M.E., 1985a. Carbon budgets for a phytoplanktivorous fish fed three different unialgal populations. Oecologia (Berlin), 67: 246-249. McDonald, M.E., 198513.Growth of a grazing phytoplanktivorous fish and growth enhancement of the grazed algae. Oecologia (Berlin), 67: 132-l 36. Moriarty, C.W. and Moriarty, D.J.W., 1973. The assimilation of carbon from phytoplankton by two herbivorous fishes: Tiahpianiloticusand Haplochromis nigripinnus.J. Zool., 17 1: 4 l55.
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Pierce, B.A., 1983. Biotic effects of grazing by tilapia (Oreochromis aureus) on phytoplankton populations in solar silos. J. Freshwater Ecol., 2: 293-304. Reynolds, C.S., 1984. The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridlge, 384 pp. Schroeder, G.L., 1978. Autotrophic and heterotrophic production of microorganisms in intensely manured fish ponds and related fish yields. Aquaculture, 14: 303-325. Schroeder, (G.L., 1983. Stable isotope ratios as naturally occurring tracers in the aquaculture food web. Aquaculture, 30: 203-210. Schroeder, G.L., I987a. Carbon pathways in aquatic detrital systems. In: D.J.W. Moriarty and R.S.V. Pullin (Editors), Detritus and Microbial Ecology in Aquaculture. ICLARM Conference Proceedings 14. International Center for Living .4quatic Resources Management, Manila, Philippines, pp. 2 17-236. Schroeder, G.L., 1987b. Carbon and nitrogen budgets in manured fish ponds on Israel’s coastal plain. Aquaculture, 62: 259-279. Smith, D.W., 1985. Biological control of excessive phytoplankton growth and the enhancement of aquacultural production. Can. J. Fish. Aquat. Sci., 42: 1940-1945. Venkataraman, L.V., 1983. A Monograph on Spirulina platensis - Biotechnology and Application. Department of Science and Technology, New Delhi, India, 100 pp. Wohlfarth, G.W. and Hulata, G., 1987. Use of manures in aquaculture. In: D.J.W. Moriarty and R.S.V. Pulhn (Editors), Detritus and Microbial Ecology in Aquaculture. ICLARM Conference Proceedings 14, International Center for Living Aquatic Resources Management, Manila, Philippines, pp. 353-367.