Fish-zooplankton interactions and their effects on water quality of a tropical Brazilian reservoir. M. S. Arcifal, T. G. Northcote2 & 0. Froehlich3. 1Departamento de ...
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Hydrobiologia 139 : 49-58, (1986) . © Dr W. Junk Publishers, Dordrecht - Printed in the Netherlands .
Fish-zooplankton interactions and their effects on water quality of a tropical Brazilian reservoir M . S . Arcifal, T. G. Northcote2 & 0. Froehlich 3 1Departamento de Biologia, FF.C.L ., Universidade de Sao Paulo, 14100 Ribeirdo Preto, Brasil; 2lnstitute of Animal Resource Ecology, The University of British Columbia, Vancouver, B.C., V6T IW5, Canada; 3 Departamento de Zoologia, Unicamp, Campinas SP, Brasil
Keywords : fish, zooplankton, eutrophication, biological control, tropical reservoir
Abstract The influence of zooplanktivorous fishes on the plankton community and water quality of Americana Reservoir, Brazil was studied experimentally in 4 floating enclosures during the dry seasons (July-September) of 1982 and 1983 . Tivo enclosures were stocked with adult fish (Astyanax bimaculatus in 1982; A . fasciatus in 1983) at near maximal densities measured in the reservoir upper surface waters (35 m -2 ) and two were fish-free during each experiment lasting about one month . Marked differences were evident between the fish and fish-free enclosures after a 2-3 week period in each experiment, particularly with respect to water transparency, phytoplankton biomass, and zooplankton abundance as well as species and size composition . By the end of each experiment water transparencies were lower and phytoplankton biomass higher in the fish enclosures compared to those without fish . Also at that time Rotifera were the prominent zooplankters in the fish enclosures and Cladocera in the fish-free ones . Larger or more conspicuous species of Cladocera as Daphnia gessneri, D. ambigua, and Moina micrura were present in the fish-free enclosures but not in the fish enclosures . The interactions between fish predation, zooplankton grazing, phytoplankton biomass and water quality conditions are discussed in relation to eutrophication of a tropical aquatic ecosystem .
Introduction Following the pioneering work of Hrbacek et al. (1961) and then Brooks & Dodson (1965) there has been over two decades of intensive work on predation by zooplanktivorous fishes and its influence on zooplankton community structure (see Hall et al., 1976 ; Nilsson, 1978 ; Zaret, 1980; for useful reviews) . More recently attention has shifted to the role of fish planktivory in eutrophication processes (Andersson et al., 1978 ; Leah et al., 1980; Lynch & Shapiro, 1981 ; Timms & Moss, 1984) and to biological control through trophic-level interactions (Shapiro, 1979, 1980 ; Langeland & Larsson, 1980) . All of these studies have involved temperate rather than tropical systems, so for this and other reasons we wished to examine experimentally the effects of intense fish zooplanktivory on water quality conditions of a very eutrophic Brazilian reservoir .
Americana Reservoir is a small (11 .5 km2 ), fairly shallow (maximum depth 19 m, mean depth 9 .2 m), polymictic reservoir some 120 km NNW of Sao Paulo City. Although surface temperatures in the summer wet season may reach 33'C and bottom minimum temperatures in the winter dry season may approach 16°C, there usually is no sharp thermal stratification . Particularly during high runoff periods Secchi transparency may be less than 0 .5 m but in the cool dry season may extend to 2 .5 m. This reservoir has been one of the more eutrophic in the region with surface oxygen supersaturations at times exceeding 150% and severe depletions frequent in bottom waters . In the late 1970's average euphotic zone concentrations of total phosphorus were 193 µgl -1 . Phytoplankton biomass and production were the highest of 10 reservoirs studied in southern Brazil (Arcifa et al., 1981) with zooplankton density being the second
50 highest (Arcifa, 1984) . Americana Reservoir frequently has had very dense blooms of blue-green algae, especially of Micro cyst is sp ., and periodically massive mortalities of fish have been reported . The first phase of our study began in August 1981 with a survey to determine the species composition, distribution and feeding habits of the fish fauna . Shortly thereafter the reservoir underwent a major drawdown which changed some of its characteristics (Northcote et al., 1985) . During the winters of 1982 and 1983 two sets of enclosure experiments were conducted with two of the most zooplanktivorous and abundant fishes in the system - the characins Astyanax fasciatus and A . bimaculatus - to examine their effect on the zooplankton community and concomitant changes in water quality conditions .
Materials and methods Two sets of experiments were carried out, the first from 20 August to 24 September 1982, and the second from 9 July to 6 August 1983 . Four replicate clear polyethylene plastic enclosures, each I x 1 m in surface area and 2 .5 m deep (tied at the bottom), were hung in tandem pairs by plywood encased styrofoam collars . Similar materials had been used in British Columbia enclosure experiments without apparent toxic effects . No openings were made in the plastic to allow water exchange . The enclosures were anchored in Sugar Cane Bay (see Fig . I in Northcote et al., 1985) at depths of about 4 to 5 m . Their upper surface was covered by 2 cm mesh netting to prevent fish addition or loss and to discourage bird defecation . Each enclosure was filled by pumping nearby water and plankton from the reservoir with an electric pump delivering 30 lmin_ 1 . The inlet hose of the pump (30 mm ID) was lowered and raised regularly between the surface and 2 m to fill the enclosures equally with water and plankton drawn from that depth interval . Water for dissolved nutrient and phytoplankton biomass sampling was similarly collected at about weekly intervals from each enclosure as well as the reservoir to fill a 10 1 container . These bulk samples were thoroughly mixed and subsamples were withdrawn for analysis . At the same time the
enclosures and the reservoir were monitored for transparency (30 cm D Secchi disc), temperature (0 and 2 m depths), dissolved oxygen (same depths, Winkler method with azide modification), pH (Metrohm meter), conductivity (Hidrocean model Antar S/01 meter), N-NH 4 (Grasshoff, 1976) as well as N-NO 3 , P-P0 4 and Si0 3 (Golterman, 1969) . Phytoplankton biomass was estimated by chlorophyll a analysis using Millipore AP20 filtration, 90% acetone extraction, and spectrophotometric readings and calculations as given by Golterman (1969) . A 15 1 integrated sample from 0 to 2 m in the enclosure was pumped weekly about midday into a 68 µm mesh net to collect macrozooplankton which was preserved in 4% formaldehyde. At least 3 plankton subsamples (1 ml) were counted in a grided chamber ; whole samples were searched for less abundant species . Two enclosures (A, B) were each stocked with 35 adult Astyanax bimaculatus (76.8 mm average fork length, 9 .7 g average weight ; ca 3400 kg ha -1 ) and no fish were put into the remaining two enclosures (C, D) for the 1982 experiments . This stocking level although high was in the upper range of Astyanax spp . densities estimated by seining and surface tow netting in nearby regions of the reservoir . Similarly in the 1983 experiments two enclosures (A, B) were stocked with 35 similar-sized adult A . fasciatus while the other two (C, D) remained fishless . Only a few fish were found dead near or at the end of the 1982 experiments (A: 1 on 26 August ; B : 1 on 20, 26 August and 3 September) but many of them died about 3 weeks after the start of the second experiment (1983) and were replaced with fish of the same species and size . Virtually all of these were alive and in good condition at the end of the 1983 experiment .
Results A . Physical and chemical conditions
During the 1982 experiments water temperatures in the enclosures were near 20 ° C with little difference (often less than a degree) between enclosures, between surface and 2 m depths, or between the enclosures and the outside water (Table 1). Although surface waters in the enclosures usually were well saturated with oxygen, near
51 Table 1 . Average temperature and dissolved oxygen values in replicate enclosures with fish (+ F) and without fish (- F), as well as in Americana Reservoir immediately outside enclosures (0) at the start and end of the experiments in 1982 and 1983 . Time
1982 Start 20 Aug .
End 24 Sept .
1983 Start 9 July
End 6 Aug .
Depth (m)
Dissolved oxygen (%a sat .)
Temperature ('Q +F
-F
0
+F
-F
0
0 2
20.2 20 .0
20 .9 20 .1
20 .8 20 .0
85 .6 60.6
99 .4 52 .3
77 .6 4 .7
0 2
21 .4 20.4
21 .2 20 .4
21 .3 20 .4
95 .7 58 .2
64 .2 52 .3
66 .6 15 .5
0 2
19 .4 18 .9
19 .2 18 .9
19 .1 19 .1
58 .2 58 .2
62 .9 60 .6
62.9 60.6
0 2
17 .5 17 .4
17 .2 17 .2
17 .7 17 .5
79 .5 72 .7
85 .1 83 .9
55 .9 52 .6
bottom waters consistently were lower in oxygen saturation and occasionally values close to half saturation were recorded . The outside reservoir water usually was lower than the enclosures in dissolved oxygen at the surface and more severely depleted at depths of 2 m . No consistent differences were evident in conductivity between the enclosures or outside with values ranging from about 140 to 150 tScm -1 . Determinations of pH were not available until the end of the first set of experiments when the fish enclosures both had higher pH's (7 .8, 8 .0) than did those without fish (both 7 .2) or the water outside (7 .1) . During the 1983 experiments temperatures were several degrees lower (17-19°C, Table 1), and with usually less than half a degree difference between enclosures, depths or inside and outside . Frequent heavy rains (unusual in the dry season), along with cold fronts destabilized thermal stratification . With little or no stratification occurring, dissolved oxygen saturations (56-80%) were moderate but nowhere were fully saturated or supersaturated waters found as in the previous year. Little difference was evident in pH between enclosures or within and outside enclosures . During the 1982 experiments Secchi disc transparency in the reservoir water adjacent to the enclosures ranged between 0.9 and 1 .4 m . In the
fish enclosures, water transparency approached but never exceeded 1 m . On the other hand, in both fish-free enclosures transparency exceeded I m after the first week and reached depths of 2 m or more by the fourth week. In the 1983 experiments water transparency initially was low in all enclosures (ca . 0.5 m) because of a heavy load of suspended inorganic sediment in the reservoir water . This sediment settled out in the enclosures during the first week so that transparency increased to slightly over 1 m (Fig. 1) . Although both fish enclosures showed a slight further increase in transparency near the end of the second week, in the fishless enclosures the increase was much more marked . In the following two weeks transparency declined again to levels below 1 m in the fish enclosures whereas in those without fish transparency continued to increase to nearly 2 m or more (Fig . 1). Initial nutrient concentrations in the reservoir and in the enclosures were markedly different between the experiments (Table 2) . In 1982, concentrations of ammonia N, phosphate and silicate were several times higher than in 1983, although the reverse was true for nitrate . There was no marked change in nutrient concentrations outside the enclosures over the 4-5 week study period, nor any consistent difference in
52 1982
U o • w •
30 µm) increased in all enclosures with fish in both years whereas in the fishless enclosures only a slight and variable change occurred . C. Zooplankton
0
1983
x
6 30
20
r
10
0
Fig. 2. Chlorophyll a concentration in enclosures with fish (A, B) and without fish (C, D), as well as in the reservoir immediately outside (0) during the course of experiments in Americana Reservoir, 1982 and 1983 .
The zooplankton species composition in the enclosures was essentially the same during the two experiments, except that Bosminopsis was not recorded in 1982 (Table 4) . Daphnia gessneri was the largest cladoceran in the community, followed by D. ambigua. Bosmina and Bosminopsis were the smallest cladocerans . Mesocyclops longisetus was the largest of the cyclopoid copepods and Tropocyclops prasinus the smallest . In both years total zooplankton densities in enclosures with fish increased greatly over the course of the experiments (Fig. 3). Although the initial zooplankton densities in 1983 were about
54 Table 3 . Phytoplankton abundance (thousands of cells per ml) in three cell-size ranges during the enclosure experiments . Treatment
A
Cell size µm
Experiment 1 (1982)
Experiment 2 (1983)
Start
End
Start
End
30
26 .5 20 .2 0 .4
65 .2 10 .5 0 .9
15 .8 0 .2
