Effects of fish grazing on nutrient release and ... - Wiley Online Library

Notes Lmnol. Oceanogr., 32(3), 1987, 723-729 0 1987, by the American Society of Limnology

and Oceanography,

Effects of fish grazing on nutrient succession of primary producers’

723

Inc.

release and

Abstract-Macrophytes (Anacharis canadensis) growing in aquaria were eliminated by the grazing activity of the omnivorous rudd (Scardinius erythrophthalmus). The phosphorus content in both the water column and periphyton was greater in those aquaria that contained fish. Grazing activity of rudd caused 33P0,3- that was injected into the sediment and taken up by A. canadensis through their roots to be released into the water phase. In a pond experiment, grazing rudd reduced the biomass ofA. canadensis, which in turn caused the biomass of epiphytic algae to increase. We suggest that nutrients, which are taken up by macrophytes from the sediments, are released by grazing fish. This nutrient pathway may thus promote a succession from submersed macrophytes to other primary producers and accelerate the eutrophication process.

Several studies have shown that planktivorous and benthivorous fish accelerate eutrophication by affecting lower trophic levels and the water chemistry of lakes (e.g. Hrbaeek 1962; Andersson et al. 1978; Henriksson et al. 1980; Fott et al. 1980). Two main pathways by which fish may affect the trophic conditions of lakes have been suggested: predation by planktivorous fish depresses zooplankton abundance, allowing phytoplankton biomass to increase; and the feeding activity of fish on the bottom causes nutrients to be released from the sediment (Lamarra 1974; Andersson 198 1). A generally observed phenomenon following eutrophication is a decrease in biomass of submersed macrophytes and an increase of phytoplankton primary productivity (Wetzel 1979; Sand-Jensen 1980). The decrease in submersed vegetation has been attributed to shading by phytoplankton (Sand-Jensen 1980; Jones et al. 1983) or epiphytes (Phillips et al. 1978). However, several cyprinid fish species that increase in ’ The study was partially supported by the National Swedish Environmental Protection Board. L. Persson was supported by a grant from the Swedish Natural Science Research Council.

biomass with eutrophication in European lakes (Persson 19833; Johansson and Persson 1986) consume large amounts of vegetation (Kennedy and Fitzmaurice 1974; Prej s and Jackowska 19 78; Niederholzer and Hofer 1980; Johansson and Persson 1983). Consequently, submersed macrophytes may be reduced by fish grazing. Fish grazing on macrophytes may affect the internal balance among autotrophic components by reducing the biomass of macrophytes, thereby reducing their ability to compete with algae for nutrients. Furthermore, since macrophytes incorporate nutrients from the sediment (Carignan and Kalff 1980), the nutrients may be remobilized to the water after being eaten and egested by fish, giving phytoplankton and epiphytes access to a new nutrient source. In a broader context, release of nutrients by the grazing activity of fish may accelerate eutrophication. The existence of this third pathway by which fish may affect the trophic conditions of lakes was tested in laboratory and field experiments. The specific hypotheses we put forward are that submersed macrophytes absorb nutrients from the sediment and that fish, by grazing on the macrophytes, will cause a release of these nutrients to the water and this release will cause an increase in biomass of primary producers other than macrophytes. Valuable comments on earlier drafts of this paper were given by L. A. Greenberg, K. Sand-Jensen, and A. Siidergren. We thank the staff at Sydvatten AB for help with the pond experiment. The experiments were performed in eight 40-liter aquaria, each of which contained 2.7 kg (wet wt) of sediment from a eutrophic lake. To prevent the fish from disturbing the sediment, we placed a plastic net (mesh size, 5 mm) over the sediment. In four of the aquaria 200 g wet wt (22 g dry wt) of Anacharis canadensis were planted and allowed to develop roots for 3 weeks before

724

Notes

the experiment began. Six fluorescent tubes (40 PEinst me2 s-l) provided light on a L/D cycle of 14 : 10 h. The water was stirred by bubbling with air. Rudd (Scardinius erythrophthalmus), a fish known to consume macrophytes (Prejs and Jackowska 1978; Niederholzer and Hofer 1980; Johansson and Persson 1983), was used in both the laboratory and field experiments. Four experimental treatments, each replicated once, were used: A. canadensis + fish, A. canadensis + no fish, fish + no A. canadensis, and no A. canadensis + no fish. The experiment consisted of adding two rudd (11.3+ 1.4 g, mean + 1 SD) to the two combinations indicated. After 5 weeks, the numbers of fish were doubled in order to increase the grazing rate. The experiment lasted 10 weeks. Water was sampled every week and analyzed for molybdate reactive phosphorus (MRP), total phosphorus, and phytoplankton Chl a. Biomass and phosphorus content of periphyton were determined every week by sampling a specified area (120 cm2) from the walls of the aquaria. Phosphorus content of A. canadensis was determined at the start and the end of the experiment. The water level in each aquarium was held constant by replacing sampled and evaporated water with tapwater. In one experiment, a tracer (33P043-) was used to study the transport of phosphorus from sediment to water via macrophyte uptake and fish grazing. In an aquarium, we placed an acrylic plastic plate over the sediment to minimize the flux of phosphorus to the water. Anacharis canadensis (180 g wet wt) was anchored to the bottom with a plastic net (mesh size, 5 mm) and rooted into the sediment through 200 holes (1 -mm diam) in the plastic plate. Small pieces (2 X 3 cm) of nylon netting (200~pm mesh size) were placed on the walls of the aquarium to facilitate sampling of periphyton. Three weeks after the introduction of the plants, carrier-free 33P043- (100 PC1 diluted in 15 ml of water) was injected into the sediment via 12 serum bottle stoppers. Eight days after the tracer was injected, two rudd (12 g wet wt each) were introduced into the aquarium. Water samples were taken 5 d before and every second day for 12

d after the introduction of fish, of which the former period served as control. Two leaves from each of five different A. canadensis stems and one piece of nylon netting colonized by periphyton were sampled 4 d after the injection and at the end of the experiment. Fecal pellets from the fish were also sampled at the end of the experiment. Samples of plant material and fecal pellets were digested in 2 ml of Soluene. Isotope contents of the samples were determined by counting in a Packard Tri-Carb 460 C scintillator. The field experiment was performed in three isolated compartments (each compartment, 12 x 25 m) of a pond 0.7 m deep, the bottom of which was covered with A. canadensis and Chara sp. Three combinations of rudd and macrophytes were used: one with no fish, one with a low density of fish (150 kg ha-‘), and one with a high density of fish (300 kg ha-‘). The high density treatment had a cyprinid biomass normal for eutrophic, south Swedish lakes (Persson 1983a, 1986). The mean wet weight of the rudd was 18 g. The pond experiment was run from the end of June until the end of October 1984. Once a month, macrophytes, periphyton, and phytoplankton were sampled to estimate biomass, and water was sampled to determine total phosphorus and MRP. Macrophytes and periphyton were sampled by harvesting all plants within a randomly placed frame (30 x 30 cm, four samples per treatment). Filamentous algae were separated from the macrophytes in the laboratory by hand. This technique underestimated the actual biomass of epiphytic algae as all algae could not be completely separated from the macrophytes. To estimate the phytoplankton biomass, we filtered 1 liter of water (Whatman GFK) and measured the Chl a according to Lorenzen (1967). To determine periphyton biomass, we filtered the periphyton as above, then dried (65°C 24 h) and weighed it. We then used the periphyton in these filters to determine the total phosphorus of the periphyton. MRP was analyzed according to Murphy and Riley (1962). Total dissolved phosphorus was analyzed after digestion with potassium persulfate and the phosphorus

725

Notes Table 1. Mean levels (? 1 SD) of MRP (Fg liter’) period. Replicate

in aquarium

water averaged over the entire experimental Replicate

1

2

Treatment

Mean

SD

n

Mean

SD

n

A. canadensis + fish A. canadensis + no fish Fish + no A. canadensis No A. canadensis or fish

22.1 4.5 12.1 5.3

14.3 5.0 5.4 2.5

11 10 11 3

37.5 12.1 17.8 6.7

33.4 3.3 13.9 2.1

10 9 11 3

content of A. canadensis and periphyton after digestion with HClO, + HNO, (1 + 4). The biomasses of macrophytes and periphyton in the field experiment were calculated as dry weight (drying at 65°C to constant weight). Concentrations of MRP in the water were highest in the aquaria with macrophytes and fish together (Table 1). The aquaria with only fish showed intermediate concentrations of MRP, while concentrations of MRP were lowest in the aquaria with macrophytes alone and those with neither macrophytes nor fish (Table 1). Concentrations of MRP in the aquaria without fish showed very little variation over time. Concentrations of phytoplankton Chl a never exceeded 5 pg liter-’ in any aquarium. In aquaria without fish they were lower (mean, 0.8 pg n = 17) than in aquaria with fish liter’, (mean, 2.1 pg liter-‘, n = 39). No differences in phytoplankton Chl a were observed between the treatments with fish. All macrophytes in the aquaria with fish and macrophytes were consumed 8 weeks after the fish were added. In the aquaria with A. canadensis alone, the biomass and phosphorus content of the macrophytes increased (Table 2). Periphyton biomass in treatments with fish increased markedly about 20 d after the experiment began. Thereafter, the biomasses were relatively constant (0.16-O-25 mg DW cm-2). The Table 2. Initial (I) and final (F) biomass (g wet wt aquarium-‘) and total phosphorus content (mg aquarium-‘) of Anacharis canadensis in aquaria containing only A. canadensis. Biomass

P content

I

F

Increase P/o)

200 200

241 255

21 28

I

F

39.5 39.5

102.4 86.9

Increase W)

159 120

amount of periphyton phosphorus per surface area was twice as high in aquaria with fish and macrophytes compared to aquaria with fish only (Fig. 1). No periphyton was ever observed in the aquaria with macrophytes only. Only macrophytes contained significant amounts of 33P0 43- before the introduction of fish (Table 3). After fish were introduced, the 33P043p content increased by 100 times in the water and 30 times in the periphytic algae (Table 3). 33P043- was also detected in the fecal pellets of the fish. That the increase in 33P0 3- content was a result of the introduced fish and not a time effect is supported by the controls (Table 1). At the start of the field experiment, the mean concentrations of MRP and total P in the water were 93 and 113 pg liter l. Later in the growing season, the concentrations in all compartments decreased to < 10 pg liter’ MRP and ~40 pg liter’ total P. Phytoplankton Chl a was ~6 pg liter’ in all compartments during the entire season. The initial biomass of A. canadensis was 0.20

1

0’

^

21

28

0 35

42

49

56

63

70

days

Fig. 1. Total phosphorus content in periphyton per sample (120 cm2) during the laboratory experiment. Solid lines-aquaria with fish and Anacharis canadensis; broken lines-aquaria with fish only. In aquaria with A. canadensis only, no periphytic growth was observed.

Notes

726

Table 3. Activity (cpm) of 33P043min macrophyte leaves, water, and periphyton before and after the introduction of fish. Activity of 33P0,3- in fish feces is also given.

Leaves (cpm leaf-l) Water (cpm ml-l) Periphyton (cpm cm-*) Fish feces (cpm mm-‘)

Before

After

1,450 5 24 -

740 460 650 400

not significantly different among the three compartments (Mann-Whitney U-test, P > 0.17) (Fig. 2). The macrophyte biomass increased markedly in the fish-free compartment during the experiment and was significantly higher than in any of the compartments containing fish on all sampling occasions except 14 August (MannWhitney U-test, P I 0.05). The macrophyte biomass in the compartment with the low density of fish (150 kg ha-‘) increased somewhat during the vegetation period, while the biomass did not increase in the compartment with the high density of fish (300 kg ha-‘) (Fig. 2). The macrophyte biomass in the compartment with low fish density was significantly higher than that in the com-

partment with high fish density only on 24 September (Mann-Whitney U-test, P < 0.014). No filamentous algae were observed in any of the compartments at the beginning of the experiment. In the middle of August, filamentous algae (mainly Spirogyra sp.) began to appear in the compartment with high fish density (Fig. 3). About 1 month later, filamentous algae appeared in the compartment with low fish density.There was a high variance in Spirogyra biomass in the same compartment within sampling occasions (Fig. 3), indicating a patchy distribution. A similar patchiness in macrophyte distribution was observed in the compartments containing fish, which is reflected in an increased C.V. at the end of the experiment (Table 4). In the fish-free compartment, no filamentous algae were observed, and the C.V. of macrophytes did not increase (Table 4). Biomass of macrophytes was negatively correlated to the biomass of Spirogyra (r, =

-0.56, P < 0.002, n = 36). Besides the other mechanisms by which fish may accelerate eutrophication, i.e. heavy predation on zooplankton and feeding activity on the bottom (Lamarra 1974; An-

800

r

1

I JUL

AUG

I SEP

f

I OCT

MONTH

Fig. 2. Biomass development of Anacharis canadensis (means k 1 SD) in the field experiment in the compartment with no fish (O), low density of fish (0), and high density of fish (0). Arrows indicate first appearance of filamentous algae in the compartment with high (solid) and low fish density (open). (n = 4 on each sampling occasion.)

727

Notes 80-

T

~

r-

_j, J”L , :L;:,:::v, SEP

AUG

OCT

MONTH

Fig. 3. Biomass of filamentous algae (means t 1 SD) on different occasions in the field experiment compartments with low (0) and high density of fish (a). (n = 4 on each sampling occasion.)

dersson et al. 1978; Henriksson et al. 1980; Fott et al. 1980), our study adds a third pathway. Fish grazing on macrophytes involves a transport of nutrients from the sediment to the water phase via macrophyte uptake of nutrients from the sediment. That submersed macrophytes absorb large amounts of phosphorus from the sediment has been shown in many studies (e.g. DeMarte and Hartman 1974; Carignan and Kalff 1980; Carpenter 198 l), and this was also the case in our study, wherein A. canadensis significantly increased its phosphorus content by uptake from the sediment (Tables 2, 3). Grazing caused higher dissolved phosphorus concentrations (Tables 1, 3); phosphorus absorbed by macrophytes was released to the water by grazing. Release of phosphorus was probably due both to

in

breakdown of fish feces (Table 3) and leakage from macrophyte tissue injured by grazing fish. Phosphorus released from the macrophytes was absorbed by periphytic algae in the laboratory study (Fig. 1, Table 3), and in the field experiment periphytic algae showed an increased biomass (Fig. 3). Hence grazing by fish causes a release of nutrients from macrophytes to other primary producers such as filamentous algae, which respond with an increase in biomass. Earlier studies on the effects of fish grazing on macrophytes have mainly been restricted to studies of the grass carp (Ctenopharyngedon idella). Although increased water turbidity from grass carp feeding has been reported, the results have been inconsistent and contradictory (Lewis et al. 1978; Richard et al. 1984). For example, Lembi

Table 4. Coefficients of variation, (s*/T) 100, of macrophyte biomasses in the pond compartments before and after colonization of filamentous algae. In the fish-free compartment where filamentous algae were never observed, the first three sampling dates have been categorized as “before” and the last three as “after” to serve as an internal control. Fish density

Before After

(kg ha-l)

150

0

300

Mean

Range

n

Mean

Range

n

Mean

22 12

7-36 5-25

3 3

19 45

4-27 11-53

4 2

12 49

Range

n

4-27 1 l-55

2 4

728

Notes

et al. (1978) showed that grass carp feeding on macrophytes caused increased turbidity and phosphorus content in the water, while Mitzner ( 19 7 8) found decreased nitrogen levels and turbidity, with no effects on phosphorus. None of these studies indicated any effects on phytoplankton. In our field experiment, we found no effect on phytoplankton, but there was an increase in the biomass of periphytic algae. We suggest that algae directly attached to the macrophytes have first access to nutrients leaking from them. The degree to which macrophytes leak nutrients is debated (Carignan and Kalff 1982; Wetzel 1983), but grazing by fish, injuring the macrophytes, should increase that leakage (DeMarte and Hartman 1974). Previously, cyprinid fishes in the temperate region were thought to inhibit the growth of submersed macrophytes by feeding on zooplankton, which results in increased phytoplankton biomass and reduced light transparency (Andersson 19 8 1). Direct grazing was considered to be of minor importance, but our study demonstrates that this may not always be the case. In our field study, the two abundances of fish gave corresponding levels of response in macrophyte biomass. The highest cyprinid abundance corresponded to that normally found in eutrophic lakes (Persson 1983a, 1986). Hence the results suggest that cyprinids could potentially regulate macrophyte biomass by direct grazing in natural systems also. Since fish also feed on filamentous algae (Niederholzer and Hofer 1980), higher grazing impact in terms of intensity or duration may promote the succession from macrophytes and periphytic algae to a situation where primary production is dominated by phytoplankton. This successional pattern is basically the same as that which follows increased nutrient loading (Wetzel 1979; Sand-Jensen 1980). Carpenter (1980, 198 1) showed that large amounts of nutrients were released by macrophytes, accelerating the internal eutrophication and the aging of lakes. Our study suggests that fish grazing intensifies the turnover and mineralization rates of macrophyte biomass. Even though the effects of grazing on nutrient dynamics have not been examined in detail, our study shows that

grazing by fish on macrophytes has the potential to promote succession from macrophytes to other primary producers, thus accelerating eutrophication.

Lars-Anders Hansson Lars Johansson Lennart Persson Institute of Limnology University of Lund P-0. Box 65 S-221 00 Lund, Sweden

References G. 198 1. Influence of fish on waterfowl and lakes [in Swedish with English summary]. Anser 20: 21-34. -. 1984. The role of fish in lake ecosystemsand in Limnology, p. 63-76. Zn S. Bosheim and M. Nichols [eds.], Interactions between trophic levels in freshwaters. Norsk Limnologforening. -, H. BERGGREN, G. CRONBERG, AND C. GELIN. 1978. Effects of planktivorous and benthivorous fish on organisms and water chemistry in eutrophic lakes. Hydrobiologia 59: 9-l 5. CARIGNAN, R., AND J. KALFF. 1980. Phosphorus sources for aquatic weeds: Water or sediments? Science 207: 987-989. -, AND -. 1982. Phosphorus release by submerged macrophytes: Significance to epiphyton and phytoplankton. Limnol. Oceanogr. 27: 419-427. CARPENTER, S. R. 1980. Enrichment of Lake Wingra, Wisconsin, by submersed macrophyte decay. Ecology 61: 1145-l 155. -. 198 1. Submersed vegetation: An internal factor in the lake ecosystem succession. Am. Nat. ANDERSSON,

118: 372-383. J. A., AND R.T. HARTMAN. 1974. Studies on absorption of 32P, 59Fe and 45Ca by water-milfoil (Myriophyllum exalbescens Fernald). Ecology 55: 188-194. FOTT, J.,L. PECHAR,AND M. PRAZAKOVA. 1980. Fish as a factor controlling water quality in ponds, p. 255-261. In J. Barica and L. R. Mur [eds.], Hyper-trophic ecosystems. Develop. Hydrobiol. 2. Junk. HENRIKSSON, L.,H.G. NYMAN, H.G. OSCARSSON,AND J. A. E. STENSON. 1980. Trophic changes, without changes in the external nutrient loading. Hydrobiologia 68: 257-263. HRBAEEK, J. 1962. Species composition and the amount of zooplankton in relation to the fish stock. Rozpr. Cesk. Akad. Ved Rada Mat. Prir. Ved 72: l-l 17. JOHANSSON, L., AND A.-C. PERSSON. 1983. Niche relations between rudd and roach in lake Siivdeborgssjijn [in Swedish with English summary]. Inform. Inst. Freshwater Res. Drottningholm 3. AND L. PERSSON. 1986. The fish community of’temperate eutrophic lakes, p. 601-630. In B. DEMARTE,

Notes Riemann and M. Sondergaard [eds.], Carbon dynamics in temperate eutrophic lakes; The structure and function of the pelagic system. Elsevier. JONES, R. C., K. WALTI, AND M. S. ADAMS. 198 3. Phytoplankton as a factor in the decline of the submersed macrophyte Myriophyllum spicatum L. in lake Wingra, Wisconsin, U.S.A. Hydrobiologia 107: 2 13-2 19. KENNEDY, M., AND P. FITZMAURICE. 1974. Biology of the rudd Scardinius erythrophthalmus (L.) in Irish waters. Proc. R. Irish Acad. 74B: 245-305. LAMARRA, A. V., JR. 1974. Digestive activities ofcarp as a major factor contributing to the nutrient loading of lakes. Proc. Int. Assoc. Theor. Appl. Limnol. 19: 246 l-2468. LEMBI, C. A., B. G. RITENOUR, E. M. IVERSON, AND E. C. FORSS. 1978. The effects of vegetation removal by grass carp on water chemistry and phytoplankton in Indiana ponds. Trans. Am. Fish. Sot. 107: 161-171. LEWIS, W. M., R. C. HEIDINGER, AND R. 0. ANDERSON. 1978. Summary and evaluation. Trans. Am. Fish.

Soc.107:223-224. C. J. 1967. Determination of chlorophyll and pheopigments: Spectrophotometric equations. Limnol. Oceanogr. 12: 343-346. MITZNER, L. 1978. Evaluation of biological control of nuisance aquatic vegetation by grass carp. Trans. Am. Fish. Sot. 107: 135-145. MURPHY, J., AND J. P. RILEY. 1962. A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta 27: 3 l36. NIEDERHOLZER, R., AND R. HOFER. 1980. The feeding of roach (Rutilus rutilus L.) and rudd (Scardinius erythrophthalmus L.). 1. Studies on natural populations. Ekol. Pol. 28: 45-59. PERSSON, L. 1983a. Food consumption and compeLORENZEN,

Lmnol. Oceanogr., 32(3), 1987, 729-735 0 1987, by the American Society of Limnology

and Oceanography,

729

tition between age classes in a perch Percafluviatilis population in a shallow eutrophic lake. Oikos 40: 197-207. -. 1983b. Food consumption and the significance of detritus and algae to intraspecific competition in roach Rutilus rutilus in a shallow eutrophic lake. Oikos 41: 118-126. . 1986. Effects of reduced interspecific competition on resource utilization in perch (Perca fluviatilis). Ecology 67: 355-364. PHILLIPS, G. L., D. EMINSON, AND B. Moss. 1978. A mechanism to account for macrophyte decline in progressively eutrophicated waters. Aquat. Bot. 4: 103-l 26. PREJS, A., AND H. JACKOWSKA. 1978. Lake macrophytes as the food of roach (Rut&s rutilus L.) and rudd (Scardinius erythrophthalmus L.). 1. Species composition and dominance relations in the lake and food. Ekol. Pol. 26: 429-438. RICHARD, D. I., J. W. SMALL JR., AND J. A. OSBORNE. 1984. Phytoplankton responses to reduction and elimination of submerged vegetation by herbicides and grass carp in four Florida lakes. Aquat. Bot. 20: 307-3 19. SAND-JENSEN, K. 1980. The balance between autotrophic components in temperate lakes with different nutrient loading [in Danish with English summary]. Vatten 2/80: 104-l 15. WETZEL, R. G. 1979. The role of the littoral zone and detritus in lake metabolism. Ergeb. Limnol. 13: 145-161. ~ 198 3. Attached algae-substrata interactions: Fact or myth, and when and how?, p. 207-2 15. Zn R. G. Wetzel [ed.], Periphyton of freshwater ecosystems. Develop. Hydrobiol. 17. Junk.

Submitted: 15 April 1986 Accepted: 20 December 1986

Inc.

Determination of phosphorus in natural water using hydride generation and gas chromatography’ Abstract-A new hydride-generation method was applied to the determination of phosphorus in seawater and pond water. A sample solution containing phosphate was mixed with a 6% sodium borohydride solution in a quartz vessel and dried under an incandescent light at 40°C for 2 h. Phosphine was reproducibly generated from phosphate by heating this vessel at 460°C. Total phosphorus and total dissolved phosphorus were

’ Research supported by grant 60030028 from the Ministry of Culture, Science, and Education.

determined by this method with small sample volume (about 100 ~1) without any digestion procedure. Good agreement was found between the hydride-generation method and ordinary colorimetry with sample digestion.

At present, phosphorus is usually determined calorimetrically for the phosphomolybdenum heteropoly-blue complex. This method has become especially popular since Murphy and Riley ( 1962) proposed it for determining soluble phosphate in sea-