Radioactive sulfate (35S04) was added to the overlying water of lake sediment microcosms to determine the effect of the burrowing mayfly nymph, Hexagenia, ...
Use of 3% to determine the influence of Hexagenia on sulfur cycling in lake sediments G. B. Lawrence’ & M. J. Mitchell2 1 Department of Civil Engineering, 152 Hinds Hall, Syracuse University, Syracuse, NY 13210, USA 2 Department of Environmental and Forest Biology, S0N.Y; College of Environmental Science and Forestry, Syracuse, NY 13210, USA Keywords: Hexagenia, Sulfur, Bioturbation,
Sediment
Abstract
Radioactive sulfate (35S04) was added to the overlying water of lake sediment microcosms to determine the effect of the burrowing mayfly nymph, Hexagenia, on sulfur transformations and fluxes. Hexagenia increased the rate of 35S04 incorporation into the sediment and the rate at which 35S04 was biologically assimilated. In addition, 3304 approached a steady-state condition with non-radioactive sulfur pools more rapidly in microcosms containing Hexagenia than in reference microcosms. Results indicate that Hexagenia enhance rates of sulfur cycling which may alter sediment acid-base chemistry and redox potential. Introduction
Research on the mechanisms of aquatic sulfur (S) cycling has concentrated primarily on chemical and microbiological processes. Substantial evidence has shown, however, that macro-invertebrates play an important role in the cycling of nutrients. Through bioturbation, tubificids can increase rates of sediment nitrification and denitrification (Chatarpaul et al., 1980) and increase sediment redox potential (Davis, 1974). Similarly chironomids can facilitate the transport of phosphorus (Gallep, 1970; Graneli, 1979) and silica (Graneli, 1979), from sediment to overlying water. The effect of macro-invertebrates on aquatic S cycling has received limited attention. Aller & Yingst (1978) found that the burrows of a marine polychaete were sites of increased sulfide oxidation. Lawrence et al. (1982) showed that the burrowing mayfly nymph, Hexagenia, increased sulfate concentrations and may have decreased organic S fractions in freshwater sediment, suggesting that S mineralization was enhanced. Hexagenia also increased sediment redox potential and the flux of ammonium, hydrogen ion and sulfate from the Hydrobiologia @ Dr W. Junk
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(1985). Dordrecht.
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sediment to the overlying water in this study. The objective of the present study was to assess specific pathways of S flux in the sediment-water environment in the presence of Hexagenia. Radioactive sulfate (35S04) was added to the overlying water of lake sediment microcosms to quantify the effects of Hexagenia on translocation and transformation of S. Methods
Microcosms were constructed by filling one liter glass containers with a homogeneous mixture of five parts sediment to three parts water, by volume, obtained from Dear Lake, New York. Information on limnological and sediment characteristics of Deer Lake is given elsewhere (Mitchell et al., 1981). The water-sediment mixture was sieved (2 mm) and allowed to settle ‘for seven days, after which the overlying water was gently aerated for the remainder of the experiment. The microcosms were covered with cheesecloth and deionized water was added each week to compensate for evaporation. The water and sediment of the microcosms were
92
five and eight cm deep, respectively, with a surface area of 50 cmz. Microcosms were maintained in the dark at 20 “C. The experiment was initiated by the addition of two Hexagenia (c. 0.1 g wet; H. limbata Seville or H. bilineata Say) nymphs to each of two microcosms (designated Hexagenia microcosms). Nymphs were obtained from Deer Lake, where both species co-exist in the same habitat. Differentiation between the two species at this stage in their development was not possible without risk of injury. Two additional microcosms served as references. After allowing 24 hours for the nymphs to establish burrows, 2.3 x 10’ dpm of ‘YS04 was added to the overlying water of each of the four microcosms. The microcosms were destructively sampled six days after addition of the 35S04. Sediment samples were separated into O-4 and 4- 8 cm layers and stored at 1 “C in polyethylene bags until completion of the analyses. All sediment analyses were performed on wet samples. Water samples were stored at 1 “C in polyethylene bottles. The top sediment (O-4 cm) layer was analyzed for Eh, moisture content, and five S fractions; HCl reducible S (acid soluble S, primarily sulfide), Zn-HCl reducible S (inorganic non-sulfate S), HI reducible S (non-pyritic inorganci S + ester sulfate), sulfate and total S. From these fractions non-HI reducible S (total S-HI S), inorganic S (Zn-HCl S+sulfate), ester sulfate (HI S-inorganic S) and organic S (non-HI reducible S+ester sulfate) were calculated. Non-HI reducible S includes carbonbonded S plus pyritic S. A previous study, however, indicated that the total sulfur pool in Deer Lake sediments was comprised of only 6% pyritic S (Mitchell et al., 1984) so that the sum of non-HI reducible S and ester sulfate is assumed to be the organic S pool. 35S was also determined for the same five sulfur fractions in the top sediment layer and total 35Swas determined from the bottom sediment depth (4-8 cm). In addition, total 3% was measured from overlying water samples collected 4 h after adding the 3sS04, and on days two, three, four and five. All sulfur analyses were performed using the techniques of Landers et al. (1983) and all sediment sulfur concentrations were expressed on a dry mass basis. The number of replicate microcosms was limited by time consuming procedures required for the decontamination of glassware used in the ana-
Fig. 1. Overlying reference (solid n=2.
water total 3’s in Hexugeniu (dashed line) and line) microcosms. Means with standard errors;
lytical procedures. Statistical analysis of the data was peformed by analysis of variance, regression and student’s t-test. Results
The initial 35S04 concentration in the overlying water decreased rapidly during the first two days in both Hexagenia and reference microcosms (Fig. 1). After this period the 35S04 concentration in the reference microcosms no longer decreased (p>O.O5), while in the Hexagenia microcosms, 35S04 continued to decrease (~~0.01) through the duration of the experiment (day 2 to day 5) at a rate of 577k62.1 dpm+$ * . d- * (degrees of freedom = 6). The decrease in overlying water 3sS04 appeared to result in an accumulation of 3% in the sediment.
1
TOP
BOTTOM
TOP
BOTTOM
Fig. 2. Total 35S in top (O-4 cm) and bottom (4-8 cm) sediment layers, 6 days after adding 35S04 to the overlying water of Hexugeniu (crossed bars), and reference (open bars), microcosms. Means with standard errors; n=6.
93 Table 1. Mean sediment Hexagenia and reference
S constituents microcosms.
Sulfur
Hexagenia
fraction
Mean f SE. YS04 (lo6 dpm.g-I) 35S04 (070 of total %) SO4 (070 of total S) Organic 35S (lo6 dpm.g-I) Organic 35S (Vo of total YS)
in microcosms
with
Table 2. Sediment (P >0.05)
(N)
Reference Mean + S.E.
Sulfur
between
)% fractions which showed no difference microcosm types as a percentage of total 3sS.
fraction
Mean
+ S.E.
09
9.45 0.89
0.99 0.06
(4) (4)
54.7 21.7
2.68 4.09
(4) (4)
45.3
2.62
(4)
(N)
7.78 *0.075 21.0 kO.40 2.21 + 0.009
(2) (2) (2)
7.35 zto.o.5 26.3 kO.01 2.61+ 0.056
(2) (2) (2)
26.3
kO.430
(2)
17.7
*0.09
(2)
71.0
kO.85
(2)
63.3
kO.76
(2)
Total 35S (Fig. 2) in the top depth of the sediment in the reference microcosms was greater (p < 0.05) than in the bottom depth, while in the Hexagenia microcosms, the bottom depth showed greater total 35S concentrations than the upper portion of the sediment. Total 3sS in both depths of the Hexagenia microcosms was greater (~~0.05) than either depth in controls. Sediment s5S04 as a percentage of total.3sS, however was greater (~~0.05) in the reference microcosms (Table 1) than in the Hexagenia microcosms, although there was no difference (p c 0.05) in the absolute amount of ?S04 between microcosm types (Table 1). By the sixth day (Fig. 3) the majority of 35S04 in
Zn-HCl (inorganic non-sulfate S) HCl (sulfide) HI (non-pyritic inorganic S + ester sulfate) Ester sulfate Non-HI reducible S (carbon-bonded S plus pyritic S)
the sediment had become incorporated into organic S in both microcosm types, although the organic fraction of 35S was smaller than the same fraction of non-radioactive sulfur. In addition, both the absolute amount of organic 3% and the organic fraction of 39 was higher in Hexagenia than in the reference microcosms (Table 1). A statistical difference in organic fraction of 35S could not be shown however, due to small sample sizes (N =2). Mean values of 35S fractions which were not different between microcosm types (p>O.O5) are given in Table 2. Discussion
Sulfur translocation
TOTAL
“SULFUR
Fig. 3. Comparison of the distribution of total S and total 3JS between non-HI reducible S (crossed section), ester sulfate (solid section) and inorganic sulfur (open section) fractions on day 6. Each circle represents the mean of 4 microcosms (2 Hexagenia, 2 reference); numbers represent S fractions as a percentage of total S.
The results of this experiment indicated that the activities of Hexagenia increased the translocation of dissolved sulfate from the water column to the sediment. In its nymphal stage, Hexagenia builds U-shaped burrows in the sediment through which water is transported for gas exchange. The circulation of water generated by Hexagenia increased the transport of overlying water into the sediment. By this process Hexagenia enhanced the incorporation of dissolved 35S04 into the sediment. The higher concentration of 35S in the lower sediment of the Hexagenia microcosms may have been caused by the position of the nymph assumes in its burrow, since it was generally in the deepest portion and increased turbulence in this region. Sulfur transformation Hexagenia increased the rate at which inorganic 35S was incorporated into organic matter due to
94
was not unrealistic since densities have been reported to exceed 700 nymphs per m* in shallow Michigan lakes (Hunt, 1953). Hexagenia populations are often major components of benthos and can exist at depths of up to 18 m (Edmunds et al., 1976). Hexagenia nymphs were found throughout the basin of Deer Lake, where they comprised 66% of the production and 80% of the biomass in the benthic community (Uutala, 1982). Conclusion
Fig. 4. Comparison
of 35S cycling rates between Hexagenia and reference microcosms. I equals initial (day 0) values; F equals final (day 6) values. Initial and final values for water total ?S are given in dpm.pl-I. Sediment 35S04 and organic YS initial and final values are given in 106 dpm.dry g-l. The rates of 35S translocation (circled values) are given in dpm pl- ’ .d - I. Rates of 35S0, transformation into organic YS (values in hexagons) are given in 106 dpm .dry g- I & I.
more rapid transport of 3sSO4 into the sediment. The larger organic fraction of 35S in the Hexagenia microcosms, however, indicated that Hexagenia may also have increased the assimilation of sulfate into organic matter (Fig. 4). This conclusion is further supported by the smaller sediment “SO4 fraction of total 35S in the Hexagenia microcosms, since the small HCl S pool (Table 1) indicated that sulfate reduction was not a major process. Although the 3sS04 fraction of total ‘5 was less in the Hexagenia microcosms than reference microcosms, this value was considerably greater than the non-radioactive sulfate fraction of total S in the same microcosms (Table 1). This suggests that the length of the experiment (6 days) was not sufficient for the 35S to become equilibrated with the S constituents within the sediment. The surplus of 35S04 in the sediment showed that the rate of 3sS04 translocation into the sediment exceeded the rate of transformation into organic forms. The smaller 3sS04 and larger 35S fractions, of total 35S in Hexagenia microcosms, however, indicated that the 35S04 was more rapidly approaching a steady state with non-radioactive S due to increased cycling in the presence of Hexagenia (Fig. 4). It is important to note that the density of Hexagenia used in this experiment (400 nymphs per m*)
The results of this experiment show that Hexagenia can play an important role in the biogeochemical cycle of S. The presence of Hexagenia increased the transformation of sulfate into organic S and the flux of S into the sediment, while a previous study (Lawrence et al., 1982) showed that Hexagenia increased S mineralization, S flux from the sediment to the overlying water and sediment redox potential. The combined results of these studies indicate that Hexagenia increased the cycling rate of S, thereby influencing the chemical and biological environment of the sediment. Mineralization of organic forms of S, followed by oxidation to sulfate generates hydrogen ions, while assimilatory reduction of sulfate neutralizes hydrogen ions. The relative rates of these processes therefore influences the proton cycle within sediments. Due to increased sediment redox potential in the presence of Hexagenia, inorganic precipitates, such as pyrite, accumulate in the sediment at a lower rate. Proton cycling and redox potential both influence the cycling of limiting nutrients such as phosphorus which control production in aquatic ecosystems. Further investigation into the effect of increased S cycling on transformations and fluxes of growth limiting nutrients is needed to more completely assess the effect of Hexagenia on sediment dynamics. Acknowledgements
We gratefully acknowledge Dr. Charles Driscoll’s careful review of this manuscript. This work was supported by a grant from the United States Office of Water Research and Technology.
95 References Aller, R. C. & J. Y. Yingst, 1978. Biogeochemistry of tubedwellings: a study of the sedentary polychaete Amphritrite ornota. J. mar. Res. 36: 201-254. Chatarpaul, L., J. B. Robinson & N. K. Kaushik, 1980. Effects of tubificid worms on denitrification and nitrification in stream sediment. Can. J. Fish. aquat. Sci. 37: 656-663. Davis, R. B., 1974. lubificids alter profiles of redox potential and pH in profundal lake sediment. Limnol. Oceanogr. 19: 342- 346. Edmunds, G. F., S. L. Jensen & L. Berner, 1976. The mayflies of North and Central America. University of Minnesota Press, Minneapolis, 330 pp. Gallep, G. W., 1979. Chironomid influence on phosphorus release in sediment-water microcosms. Ecology 60: 547 - 556. Graneli, G. W., 1979. The influence of Chironomus plumosus larvae on the exchange of dissolved substances between sediment and water. Hydrobiologia 66: 149-159. Hunt, B. P., 1953. The life history and economic importance of a burrowing mayfly, Hexageniu limbata, in southern Michigan lakes. Bull. Inst. Fish. Res. No. 4, Mich. Dept. of Cons., 151 pp.
Landers, D. H., M. J. Mitchell & M. B. David, 1983. Analysis of organic and inorganic sulfur constituents in sediments, soils and water. Int. J. envir. Anal. Chem. 14: 245-256. Lawrence, G. B., M. J. Mitchell & D. H. Landers, 1982. Effects of the burrowing mayfly, Hexagenia, on nitrogen and sulfur fractions in lake sediment microcosms. Hydrobiologia 87: 273-283. Mitchell, M. J., D. H. Landers & D. F. Brodowski, 1981. Sulfur constituents of sediment and their relationship to lake acidification. Wat. Air Soil Pollut. 16: 177-186. Mitchell, M. J., D. H. Landers, D. F. Brodowski, G. B. Lawrence & M. B. David, 1984. Organic and inorganic sulfur constituents of the sediments of three New York Lakes: effect of site, sediment depth and season. Wat. Air. Soil. Pollut. 21: 231-245. Uutala, A., 1982. Composition and production of the zoobenthos community in three New York lakes, with emphasis on Chironomidae (Diptera). M. Sci. Thesis, St. Univ., N.Y. Coll. envir. Sci. For. 131 pp. Received 21 February 1985; in revised form 11 June 1985; accepted 11 June 1985.
