56 (1986) 59-68 Elsevier Science Publishers B.V., Amsterdam - Printed in The Netherlands
Aquaculture,
59
IMPACT OF SILVER AND BIGHEAD CARPS ON PLANKTON COMMUNITIES OF CHANNEL CATFISH PONDS
JOHN S. BURKE’, DAVID R. BAYNE* and HARRY REAa
Department of Fisheries and Allied Aquacultures, Alabamo Agricultural Experiment Station, Auburn University, AL 36849 (U&A.) *To whom correspondence should be addressed Present addresses: I 5345-C Dana Drive, Raleigh, NC 27606 (U.S.A.) ZVirginia Cooperative Extension Service, 106B Butler Road, Fredericksberg, VA 22401 (U.S.A.) (Accepted
17 March 1986)
ABSTRACT Burke, J.S., Bayne, D.R. and Rea, H., 1986. Impact of silver and bighead carps on plankton communities of channel catfish ponds. Aquaculture, 55: 59-68. Stocking of ponds with planktivorous carps in polyeulture with channel catfiih (Ictaand a hybrid) reduced the density of zooplankton when compared to controls. Bighead (Araktichthye nobilis) and silver carp (Hypophthalmichthys molitrix) similarly reduced zooplankton, though the mechanism of suppression may be different. Phytoplankton biomass was significantly higher in ponds containing bighead and silver carp. Ammonia and nitrite concentrations were similar in bighead and silver carp ponds and were significantly lower than in control ponds.
lurus punctatus
PRODUCTION
The planktivorous Chinese carps have received recent attention as promising polyc~t~e species and as possible movement tools of aquatic systems. Interest in these species as a means of controlling nuisance blooms of algae in catfish production ponds has developed among fish culturists in the United States. Opuszynski (1979) used dense stocking rates (4000-12 OOOf ha) of silver carp (Hypophfhalmichthys molitrix) to determine if planktonic algae could be controlled; however, these stocking densities increased phytoplankton biomass. Opuszynski gave the following reasons for the failure of silver carp to control algal blooms: (1) low efficiency of algal feeding due to feeding on detritus; (2) elimination of zooplankton; (3) more rapid circulation of plant nutrient; and (4) slower rate of weight increase of fish as stocking densities increased. Opuszynski (1981) showed that both silver and bighead carp in polyculture with common carp did not differ significantly in
0044-8436lS6i$O3.50
0 1986 Elsevier Science Publishers B.V.
60
their effect on the plankton but that bighead carp competed to a greater degree with common carp for natural food. The indirect effect of planktivorous carps on plant nutrients is of interest since both un-ionized ammonia and nitrite can cause fish disease and mortality (Boyd, 1979). Previous experiments with planktivorous fishes in polyculture with catfish have resulted in reduced problems associated with eutrophication while increasing total fish yield (Smith, 1971; Dunseth, 1977). The objectives of our study were to determine the impact of lower stocking rates of silver and bighead carp on zooplankton, phytoplankton and inorganic nitrogen compounds in catfish culture ponds. MATERIALS
AND METHODS
Twelve 0.04-ha ponds with a mean depth of 1 m were randomly assigned to one of three treatments (Table 1). All ponds were stocked with channel catfish (Ictalurus punctatus) and the hybrid, channel X blue catfish (I. punctutus X I. furcatus) in equal numbers to a combined rate of 7410 fish/ha. Grass carp (C~enop~a~~godon ~dell~) were stocked (124/ha) in all ponds to provide weed control. Four of the ponds were stocked with fingerling silver carp (2470/ha) and four ponds with fingerling bighead carp (2470/ha). Fish were fed daily with a floating feed containing 32% protein. Each pond received a total of 5126 kg feed/ha during the 203day culture period. TABLE 1 Treatments, fish species, stocking rates, dates and weights Treatment
Fish species
Stocking rate
Stocking date
Mean stocking weight (g/fish)
Control
Catfish Grass carp
741a/ha 124jha
7 March 9 March
12 119
Bighead carp
Catfish Grass carp Bighead carp
7410lha 124/ha 2470/ha
7 March 9 March 7 March
11 119 10
Silver carp
Catfish Grass carp Silver carp
74lOjha 124jha 2470/ha
7 March 9 March 7 March
12 119 15
Gut analysis
All ponds were seined monthly, May to August, to obtain fish for mean weight determinations. Two carp from each of the ponds were removed for intestinal examination and replaced by fish of similar size. A total of 32 big head and 32 silver carp were examined during the experiment. Digestive tracts were preserved in 10% formalin. Contents were removed from the anterior 5 cm of the gut and examined
61
with a dissecting microscope to determine gross characteristics. ,A l-ml aliquot was diluted to 100 ml with water and a portion examined in a Sedgwick-Rafter cell with the aid of a compound microscope. Twenty-five randomly selected fields were examined to estimate the volume that each food category contributed to the gut contents. The mean volume percentage that each food category contributed to the total volume of food for that sample date was then calculated (Wallace, 1981). Gut contents from the posterior end of the intestine were examined qualitatively to determine extent of digestion. P~anktun and water quality A composite water sample from each pond was obtained weekly with a column sampler (Boyd, 1979). Ten water column samples were taken from representative areas of each pond and pooled. For a zooplankton sample, 10 1 of pond water were passed through an 80~pm mesh, Wi~on~ style plankton net and the concentrate preserved in 5% formalin. Zooplankton were counted in a Sedgwick-Rafter cell with the aid of a compound microscope (Lind, 1979). Cladocerans and rotifers were identified to species and copepods to suborder using current and standard taxonomic references. All samples were examined qu~itatively. Zoopl~~on counts were made at monthly intervals in all treatments; however, weekly counts were made during periods when qualitative examination indicated the need for closer inspection. Temperature and dissolved oxygen were determined, chlorophyll-a was extracted with acetone and measured sp~t~pho~rn~~c~y (APHA et al., 1980), and ph~ph~~~orr~ted chlorophy~ values were reported. Total ammonia nitrogen was determined by the phenate method (Boyd, 1979) and nitrite concentration was determined by the calorimetric method (APHA et al., 1980). Data analy so Seasonal means of chemical and biological variables were compared using analysis of variance with preplanned treatment mean contrasts. The contrasts were made between the control and silver carp treatment and the control and bighead carp treatment. The Statistical Analysis System package (H&wig and Council, 1979) was used and statements of significant differences were based on an a = 0.05. RESULTS
standing stock o~~~up~a~kton and water quality Overall treatment means for zooplankton and water quality variables are presented in Table 2. Results of the preplanned contrast tests appear in Ta-
ble 3. Comparisons of seasonal trends in zooplankton standing stocks for the control and two carp treatment are presented in Fig. 1. Mean standing stocks of all zooplankton groups were significantly lower in the bighead and silver carp treatments than in the control. Water temperature in culture ponds increased during May to a summer TABLE 2 Treatment means for chlorophyll-a (CL-a), zooplankton groups, total ammonia nitrogen (TAN) and nitrite measured in three experimental fish culture treatments in 1983. The number of samples appears in parentheses Treatment
CL-a Copepods (pug/l)
Copepod nauplii
Cladocerans
Rotifers
297 (32) t3”2”,
302 (32) (a421,
1,600 (32) 406 (32) 456 (32)
Tan (mg/l)
Nitrite (r&l)
0.393 (112) 0.123 (112) 0.082 (111)
9.19 (108) 3.43 (108) 2.69 (107)
(liter-’ ) Control Silver carp Bigheadcarp
38.17 (112) 80.19 (112) 80.50 (110)
137 (32) 14 (32) 11 (32)
TABLE 3 Results of preplanned contrasts of treatment means of the control (C) and silver carp (SC) treatments and the control and bighead carp (BHC) treatments Contrast
Difference
Chiorophy~-a (rgfl) SC-C 42.02 BHC-C 42.33 Nitrite (p&l) SC-C 5.76 BHC-C 6.60 Total ammonia nitrogen (mg/l) SC-C 0.26 BHC-C 0.30 Cladocerans (liter-l ) SC-C 261.62 BHC-C 284.80 Copepods (liter-‘) SC-C 123.82 BHC-C 126.44 Copepod nauplii (liter-‘) SC-C 238.23 BHC-C 240.76 Rotifers (liter-‘) SC-C 1193.60 BHC-C 1144.10
Probability
SE
12.14 12.19
0.003 0.004
2.50 2.53
0.04 0.02
0.14 0.14
0.07 0.04
51.76 51.76
0.0001 0.0001.
13.37 13.37
0.0001 0.0001
26.67 26.67
0.0001 0.0001
229.24 229.24
0.0001 0.0001
63
high. During this month chlorophyll-a concentration in the carp treatments began to rise from a seasonal low (Fig. 2). Chlorophyll-u concentrations in the control remained comparatively low and stable, and were significantly lower than in the carp treatment (Table 3). Ammonia levels rose rapidly in the control and remained high throughout the season (Fig. 3). Levels in the carp treatments remained low through June after which they fluctuated widely. Nitrite concentrations followed this same general pattern (Fig. 3). This pattern of reduced dissolved nitrogen in
----..-_
Mar.
May
JUIY
Sept.
Mar.
Control Btthead Carp Silver Carp
M6Y
.-..-I_July
Fig. 1. Mean standing stocks of four zooplankton culture treatments, 1983.
Sept.
groupe for the three experimental fish
---- Control
_
-BtgheadCsrP ----Silver
. Iyla.
Carp
. Apr.
May
Jim idy A& 6&f.
Fig. 2. Mean chlorophyll-a ments, 1983.
con~nt~tions
for the three experimental
fish culture treat-
64
----
Control
-.--.
Bighead Carp Silver Carp
Fig. 3. Mean concentrations treatments, 1983.
of ammonia and nitrite in the three experimental fish cufture
the carp treatments may be the result of phytoplankton die-offs, which are followed by a rapid increase of dissolved nitrogen (Boyd, 1979). With the exception of the silver carp-control comparison for ammonia, nitrite and ammonia concentrations were significantly higher in the control than in either carp treatment (Table 3). Gut contents
Results of gut analyses are presented in Table 4. Individual silver carp gut contents ranged from about 90% detritus to 99% algae. The highest estimate for zooplankton was 5% in one fish in the May sample which was composed almost entirely of rotifers. ~os~~n~, ostracods and remains of copepods were observed in silver carp intestines but always as isolated occurrences. Individual bighead carp intestinal contents ranged from 90% zooplankton to predominantly algae or detritus. High percentages of zooplankton oc-
65 TABLE 4 Gut contents of silver and biihead carp sampled at monthly Value& represent estimates of mean volume par cent Month
Algae
Detritus
intervals (May-August),
Zooplankton Rotifers
May June July August
45 60 50 50
40 40 50 50
Silver carp 5 T T T
May June July August
10 25 60 50
40 60 35 40
Bighead carp 10 5 5 10
copepods
TE T T T
30 T T T
Cladocerans
T -
10 10 T T
aT = trace amounts.
cur-red in the May and June samples. Subsequent samples had greatly reduced zooplankton volume. July and August samples were dominated by colonial algae. DISCUSSION
The impact of silver and bighead carp on plankton communities appears related to the feeding habits of these fishes. Although both carp species consumed algae, a significant increase in algal biomass occurred in carp treatments. Similar results were reported by Opuszynski (1979,198l) who cited diets high in detritus, elimination of zooplankton and rapid circulation of nutrients as reasons for failure of the silver carp to control algae. In our study, reduction in zooplankton numbers seems to have been a key factor in the failure of the carp to control algae. Control ponds had the highest zooplankton densities and dissolved nitrogen levels, indicating high algal mortality. In the carp treatments dissolved nitrogen was generally lower and algal biomass accumulated, indicating low mortality (Tilman et al., 1982). It appears that by reducing zooplankton numbers, the carp removed a factor important in regulating phytoplankton biomass in catfish ponds. Literature on feeding of the pl~ktivo~us carps is extensive and contradictory, apparently due to the variety of physical and biological conditions under which investigations have been conducted. Bighead carp have been reported to feed primarily on zooplankton and detritus (Lazareva et al., 1977; Cremer and Smitherman, 1980; Opuszynski, 1981). In our study, bighead carp fed primarily on zooplankton and detritus during May and June and switched to colonial algae in July and August. Lazareva et al. (1977) found
66
that while phytoplankton usually remained a small percentage of the diet of the bighead carp, “bloom” conditions could result in increased consumption of algae amounting to 70% of the food bolus. In the present study, July and August standing stocks of algae were very high and standing stocks of zooplankton low. Algae may be filtered incident~y as bighead carp forage for scarce zooplankton. Much of the algae consumed appeared to pass through the gut unchanged. Results of silver carp feeding habit studies are also quite variable. Silver carp are generally considered as phytophagous fish (Chiang, 1971; Cremer and Smitherman, 1980; Spataru et al., 1983), although several authors stressed the importance of detritus and bacterioplankton (Omarov and Lazareva, 1974; Kuznetsov, 1977; Spataru, 1977; Opuszynski, 1979,198l). Workers who have studied silver carp feeding in fish ponds are in general agreement that zooplankton does not represent a large part of the gut contents; however, Spataru and Gophen (1985) found significant amounts of zooplankton in guts of silver carp from a reservoir. Bitterlich and Gnaiger (1984) found that rotifers and copepod nauplii were rapidly decomposed in gut fluid from silver carp and suggested that this was a factor in the scarcity of zooplankton in silver carp feeding studies. In our study, the main components of silver carp gut contents were ph~opl~~on and detritus, both of which were found in high volumes throughout the growing season. Zooplankters were infrequently encountered and appeared in significant numbers only in the spring sample. At this time guts of bighead carp, from ponds which had similar standing stocks of zooplankton, contained as much as 90% zooplankton. The varied reports on feeding habits suggest that silver carp should be considered versatile omnivores (Bitterlich and Gnaiger, 1984). It appears that bighead carp exert significant predation pressure on zooplankton. Though evidence is lacking that silver carp exert similar pressure on zooplankton in fish culture ponds, the quantitative reduction of zooplankton by the two carp species was similar in this and a previous investigation (Opuszynski, 1981). An alternative to the hypothesis that silver carp reduce zooplankton standing stock through predation might be competition. Competition for food is not restricted to animals of similar size or physiology. Brown and Davidson (1977) discussed competition between seed-eating rodents and ants. If pop~tions of animals are essentially similar in their diets then they are similar ecologically and the presumption of intense competition upon co-association is warranted (Hansen and Uekert, 1970). Data on feeding habits indicate considerable overlap in the particle size filtered by zooplankton (Allan, 1976); rotifers (l-20 pm), cladocerans (l-50 pm) and copepods (5-100 pm) and silver carp (8-100 (urn) (Cremer and Smitherman, 1980). Kuznetsov (1977) reported that particles smaller than this may be concentrated on the slime secreted by the laby~nthyfo~ organ of the silver carp. One would expect competition to function to reduce a pop~ation only if resources are limiting; the reported increase in phytoplankton in the silver carp ponds suggests that they were not. However, despite the reported in-
67
crease in algal biomass it is possible that resources were hmited. This could occur if, as algal biomass increased, the p~po~ion of algal forms Apache to filter-feeding zooplankters and the silver carp decreased. Opuszynski (1979) reported that the composition of the phytoplankton community changed to a dominance of larger species under the influence of silver carp. These forms may be unavailable to zooplankton because of their large size (Lynch and Shapiro, 1981), gelatinous sheath or tough cell wall which prevents digestion (Porter, 1973; Wetzel, 1975). Some algal species, notably blue-greens, may be toxic (Lambert, 19Sl). These same factors may affect utilization of algae by silver carp as well as zooplankton. Blooms of certain blue-greem algae may be rejected by silver carp as a food source (Umarov and Lazareva, 1974) and many species of algae are not digested by silver carp (Spataru, 1977). When algae in fish ponds are of poor quality, detritus and bacteria may be of considerable importance to zooplankton and silver carp. Studies of silver carp diet in ponds fertilized with fluid manure have suggested that the flocculent manure or colonizing microflora was the source of nut~tion for silver carp (Schroeder, 1983; Shan et al., 1985). A number of investigators have stressed the importance of the detrital food chain to zooplankton (Taub and Dollar, 1968; Wetzel, 1975; Geiger, 1983). The detrital food chain may become of critical importance during summer months when colonial green and bluegreen algae become dominant in catfish ponds (Boyd, 1973). The carp stocking rates used in this study were apparently too high, resulting in reduced ~oop~~ton numbers and increased phy~p~k~n biomass. F~her research is needed to determine if fower carp stocking rates would have a more desirable effect. Another approach would be to evaluate within-pond zooplankton refuges that would permit coexistence of large numbers of zooplankton with planktivorous fish. Smith (1985) reported success with this technique when it was tested in 1000-l fiberglass tanks. RBFERENCBS ABan, J.D., 1976. Life history patterns in zooplankton. Am. Nat,, 110: X66---189. American Public Health Association, American Water Works hociation, and Water Polhrtion Control Federation, 1980. Standard Methods for the Examination of Water and Wastewater, 15th ed. APHA, Washington, DC, $134 pp. Bitterlich, G. and Gnaiger, A., 1934. Phytoplanktivorous or omnivorous fiih? Digestibility of zooplankton by silver carp, Hypophthalmichthys molitrix (Val.). Aquaculture, 40: 261-263. Boyd, C.E., 1973. Summer algal communities and primary productivity in fish ponds. Hy~bio~~ia, 41: 367-390. Boyd, C.E., 1979. Water Quality in W~mwater Fi~~nds. Alabama ~~cultur~ Experiment Station, Auburn University, AL, 369 pp. Brown, J.H. and Davidson, D.W., 1977. Competition between seed-eating rodente’and ants in desert ecosy&ems. Science, 196: 880-332. Chiang, W., 1971. Studies on feeding and protein digestibility of silver carp, ~ypophtha~michthys molitrix (C. + V.). Joint Comm~~on for Rural R~o~~~ion Fish Series, 11: 96-114.
68 Cremer, M.C. and Smitherman, R.O., 1980. Food habits and growth of silver and bighead carp in cages and ponds. Aquaculture, 20: 67-64. Dunseth, D.R., 1977. Polyculture of channel catfish, ZctaZurus punctotus, silver carp, Hypophthalmichthys molitrix, and three all male tilapias, Sarotherodon spp. Doctoral Dissertation, Auburn University, AL. Geiger, J.G., 1983. A review of pond zooplankton production and fertilization for the culture of larval and fingering striped bass. Aquaculture, 35: 353-369. Hansen, R.M. and Uekert, D.N., 1970. Dietary similarity of some primary consumers. Ecology, 51: 640-647. Helwig, J.T. and Council, K.A., 1979. SAS User’s Guide. SAS Institute Inc., Gary, NC, 494 pp. Kuznetsov, Y.A., 1977. Consumption of bacteria by silver carp (Hypophthalmichthys molitrix). J. Ichthyol., 17: 398-403. Lambert, W., 1981. Inhibitory and toxic effects of blue green algae on Daphnia. Int. Rev. Ges. Hydrobiol., 66(3): 286-298. Lazareva, L-P., Omarov, M.O. and Lezina, A.N., 1977. Feeding and growth of the bigbead, Ari8~ichthys nobilis, in the waters of Dagestan. J. Ichthyol., 17(l): 65-75. Lind, O-T., 1979. Handbook of Common Methods in Limnology. C.V. Mosby, St. Louis, MO, 199 pp. Lynch, M. and Shapiro, J., 1981. Predation, enrichment and phytoplankton community structure. Limnol. Oceanogr., 26: 86-102. Omarov, M.O. and Lazareva, L.P., 1974. The food of the silver carp in Dagestan ponds and lakes. Gidrobiol, Zh., lO(4): 100-104. Opuszynski, K., 1979. Silver carp ~ypophfhaimich~hys molitrix (Val.) in carp ponds. III. Influence on ecosystem. Ekol. Pol., 27: 117-133. Opuszynski, K., 1981. Comparison of the usefulness of the silver carp and the bighead carp as additional fish in carp ponde. Aquaculture, 26: 223-233. Porter, K.G., 1973. Selective grazing and differential digestion of algae by zooplankton. Nature, 244 : 179-180. Schroeder, G.L., 1983. Natural food web contributions to fish growth in manured ponds as indicated by stable carbon isotopes. J. World Maricult. Sot., 14: 505-509. Shan, J., Chang, L., Gua, X., Fang, Y., Zhu, Y., Chou, X., Zhou, F. and Schroeder, G.L., 1985. Obsenrations on feeding habits of fish in ponds receiving green and animal manures in Wuxi, Peoples Republic of China. Aquaculture, 46: 111-117. Smith, D.W., 1985. Biological control of excessive phy~pl~kton growth and the enhancement of aquacultural production. Can. J. Fish. Aquat. Sci., 42: 1940-1945. Smith, P.L., 1971. Effects of Tilapia aurea (Steindachner), cage culture, and aeration on channel catfish Zctalurus punctatus (Rafinesque) production in ponds. Doctoral Dissertation, Auburn University, AL. Spataru, P., 1977. Gut contents of silver carp Hypophthalmichthys molitrix (Val.) and some trophic relations to other fish species in a polyculture system. Aquaculture, 11: 137-146. Spataru, P. and Gophen, M., 1986. Feeding behavior of silver carp ~y~ph~halmich~hy8 rno~i~~ Val. and its impact on the food web in Lake Kinneret, Israel. Hyd~biologia, 120: 53-61. Spataru, P., Wohlfarth, G.W. and Hulata, G., 1983. Studies on the natural food of different fish species in intensively manured polyculture ponds. Aquaculture, 35: 283298. Taub, F.B. and Dollar, A.M., 1968. The nutritional inadequacy of Chlorella and Chlamydomonas as food for Daphniapulex. Limnol. Oceanogr., 13: 60’7-617. Tilman, D., Kilham, S.S. and Kilham, P., 1982. Phytoplankton community ecology: the role of limiting nutrients. Annu. Rev. Ecol. Systems, 13: 349-372. Wallace, R.K., 1981. An assessment of diet-overlap indexes. Trans. Am. Fish. Sot., 110: 72-76. Wetzel, R.G., 1975. Limnology. W.B. Saunders Co., Philadelphia, London, Toronto, 743 pp.