Shifts in the Effects of Tuft-Weaving Midges on Filamentous Algae Author(S): Mary E

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Shifts in the Effects of Tuft-weaving Midges on Filamentous Algae Author(s): Mary E. Power Source: The American Midland Naturalist, Vol. 125, No. 2 (Apr., 1991), pp. 275-285 Published by: The University of Notre Dame Stable URL: http://www.jstor.org/stable/2426232 Accessed: 14-07-2016 00:48 UTC

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Shifts in the Effects of Tuft-weaving Midges on Filamentous Algae

MARY E. POWER Department of Integrative Biology, University of California, Berkeley, Berkeley 94720

ABSTRACT.-During summer low-flow periods massive growths of filamentous green algae (dominated by Cladophora glomerata) in the Eel River of Northern California become infested with chironomid larvae that weave the algae into retreats, or "tufts." Field experiments suggest that these midges (primarily Pseudochironomus richardsoni) have negative early effects, and positive later effects on the biomass of algae they inhabit. During initial colonization and tuft construction by midges, weight loss of Cladophora and associated epiphytes in stream enclosures increased with increasing midge densities. In an in situ incubation experiment, chlorophyll a content and final damp weight of Cladophora and epiphytes were higher with old, feces-filled tufts, or with nitrate fertilizer, and were lower in controls or with new midge tufts. These results suggest that tuft-weaving midges have complex effects on algae they inhabit that change with the ontogeny of midges and the age of the retreats they construct.

INTRODUCTION The strength and often the nature of species interactions change with ontogeny (Neill, 1975; Werner, 1986). Changes in the "ontogenetic niches" (sensu Werner and Gilliam, 1984) of holometabolous aquatic insects, which feed in fresh water as larvae and reproduce as aerial adults, are particularly pronounced. Even within the larval stage, early and late instars may differ in the foods and habitats that they use (Anderson and Cummins, 1979; Siegfried and Knight, 1976; Feminella and Stewart, 1986; Fuller and Stewart, 1977; Win- terbourn, 1974). These changes must alter the interactions of such species with other members of their communities, but we know little about the ecological consequences of ontogenetic shifts in aquatic insects. Here I discuss the effects of a guild of larval chironomids (dominated by Pseudochironomus richardsoni) on the filamentous algae (mainly Cladophora glomerata L.) that they inhabit. Midges weave the algae into retreats, or tufts, and feed mainly on diatoms epiphytic on Cladophora. Eventually, midge larvae fill their retreats with fecal material. Midges pupate within tufts and emerge as winged adults. During summer low-flow periods, these chironomid larvae are extremely dense in sunlit reaches of the Eel River in northern California, numerically dominating the insect fauna (Power, 1990a, b). Midges could benefit or harm the filamentous algae in which they live. If they removed harmful epiphytes, fertilized algae with their feces, or if their silk and weaving augmented tensile strength of algal filaments, they might prolong the persistence, and/or enhance the growth, of filamentous algae. On the other hand, midges might reduce algal biomass if, for example, they ingested significant amounts of Cladophora, or caused filaments to be frag- mented and exported. As a third alternative, midges might exert both positive and negative effects on algae, with the net outcome shifting over time. Here, I report field experiments that compare the effects of midges and their newly formed versus long occupied retreats on the condition and biomass of Cladophora. These results address the three alternative hypotheses that tuft-weaving midges have negative, positive, or changing effects on their algal host.

275

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STUDY SITE AND BIOTA

Midge-algae interactions were studied in a 3-km reach of the South Fork of the Eel River near Branscomb, in Mendocino Co., California (39?44'N, 123?31'W). The South Fork, with a gradient of 0.5-0.6% over the reach studied, drains sparsely settled forest and pastureland before entering the Northern California Coast Range Preserve, where the study reach was located. Here the South Fork is surrounded by a mature forest of coastal redwood (Sequoia sempervirens), Douglas fir (Pseudotsuga menziesii), and oak (Quercus spp.). Alder (Alnus rhombifolia), sedges (Carex nudata), and an introduced legume (Melilotus alba) line the active, boulder-filled channel of the river. Precipitation in coastal California falls mainly between October and April. Following winter floods, discharge drops steadily and water temperatures rise. During the low-flow months, the inundated channel is 3-15 m wide, and pools are 0.5-4.0 m deep. During this sunny warm period, the river bed stabilizes, the water clears and filamentous algae, largely Cladophora glomerata, proliferate. Attached strands of algae, or "turfs," proliferate in May. By June and early July, algal turfs up to 8-9 m long cover most bedrock and boulder substrata. Large amounts of algae detach in July, and accumulate as floating mats. From June through September, tuft-weaving midge larvae are extremely abundant, attaining densities of up to 60 individuals/g (damp weight) of algae, and of 12 individuals/cm2 of water surface (Power, 1990a).

METHODS

I monitored algae during the low-flow season at 10 x 10-cm2 sites evenly spaced at 1-m intervals under five permanent cross-stream transects. At each site, the presence or absence of Cladophora was noted, as well as whether or not it was woven with midge tufts. The number of sites examined per date varied from 55 to 36, decreasing as receding water levels reduced the wetted area of the river. To assess ingestion of Cladophora and its epiphytes by midges, 21 individuals, 6 to 9-mm long, were removed from tufts, collected during June, July and August, and dissected for gut analyses. Gut contents were spread thinly over a microscope slide and examined at 400 x. Using a gridded ocular reticle as a two-dimensional transect, I scored items under at least 100 intersections per sample to obtain scores indicating the frequency of items as indexed by their projected area (Jones, 1968). I examined the relationship between Cladophora weight change and the density of new midge colonists by incubating Cladophora in small field enclosures with 1-mm mesh walls which permitted immigration by chironomid larvae. Uniform-appearing Cladophora was harvested from the river and carefully cleaned in enamel trays, so that most invertebrates > 1-mm long (except for cryptic ceratopogonid larvae similar to Cladophora in diameter and color) were removed. Cleaned algae were divided into 5-g (damp weight) aliquots. Damp weight was measured to the nearest 0.1 g after algae had been spun for 50 revolutions in a salad spinner lined with 0.3-mm mesh netting. Repeated measurements of damp weight differed by less than 2%. Damp weight measured this way correlated closely with dry weight of Cladophora dried to constant weight at 100 C:

Dry weight (g) = 0.09 [damp weight (g)] + 0.02, n = 44, r2 = 0.98.

Spinning and weighing had little conspicuous effect on the health of Cladophora. Each of 48 stream enclosures was stocked with 5 g of cleaned Cladophora. Enclosures were cylinders with walls 12-cm high of 1 mm-mesh plastic screen supported between two 9-cm diameter plastic petri dishes. Groups of six enclosures were mounted on hollow buoys

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with Velcro-covered metal brackets inserted into a hose clamp encircling the center of each buoy. Buoys were slipped over metal poles driven into the river bed, then filled with water until the enclosures were half submerged. Enclosures were set out in a 32-m wide, 200-m pool of the South Fork Eel, in water 30 to 60 cm deep. Here, flow was uniformly slow (<5 cm s-') and Cladophora covered boulders that emerged from the gravel bed. To examine the effects of midges on Cladophora at different stages during their occupation of algae, I incubated Cladophora with old and new midge tufts. Tuft age was inferred from tuft size and contents. Thicker (>0.5-cm wide) tufts filled with fine particulate matter were considered "old." "New" tufts were more slender (<2-mm wide), and lacked the accu- mulated detritus. Tufts that appeared old contained larger larvae and pupae, while new tuft residents were smaller earlier instars. Twenty, clear, open-topped plastic containers (10-cm top diameter, 7-cm bottom diameter, 16-cm high) were embedded along the sandy margin of the same large backwater pool where enclosures were placed. The bottom 4 cm of each container was buried in the sandy bed, and the top rim projected ca. 2 cm above the water surface. A clean stone was placed in each container to anchor it, and 800 ml of river water was added. Five g (damp weight) of cleaned Cladophora were placed in each container. Five containers with Cladophora only served as controls; five containers also each received 10 new midge tufts, and five others received 10 old midge tufts. The groups of ten tufts were weighed before addition, and these weights (0.25-0.60 g for new tufts, 1.0-2.3 g for old tufts) were subtracted from final Cladophora weights at the end of the experiment. To determine if nitrogen was limiting to Cladophora at the time of these experiments, I added 2 M Na2NO3 in the form of a sand- agar wafer in an open-topped 4 cm diameter petri lid (see Pringle and Bowers, 1984 for description of this method) to a fourth group of containers with Cladophora (n = 5). At the end of the 19-d incubation period, water from containers and from the river was collected and filtered through Whatman GF/C filters, then through Gelman Metricel GN-6, 0.45 ,Am filters and stored frozen until chemically analyzed. Nitrate concentrations were measured by a hydrazine reduction method (Kamphake et al., 1967), ammonia by a phenolhypochlorite method (Solarzano, 1969), and inorganic phosphate by a stannous chloride technique (APHA, 1985). In addition, three replicate subsamples of algae from each container were collected and frozen for determination of chlorophyll a and pheophytin. These pigments were measured 12 d after collection by the methanol extraction method of Marker (1972).

RESULTS Gut contents of midge larvae. -Frequencies of empty diatom frustrules, the most common identifiable item in guts, did not vary among months (P > 0.52 from a Kruskal-Wallis test). Empty epiphytic diatoms (predominantly Epithemia sp. and Cocconeis sp.) were the most abundant item in the guts of each of the 21 larvae examined, followed by empty filaments of Cladophora and coccoid unicells ca. 2 microns in diameter (Table 1). With the exception of the latter, few cells in midge guts retained their contents (Table 1). Phenology of midges and Cladophora.-Cladophora was not macroscopically detectable in the channel during February and March, following scouring winter floods, but began to appear in April (Fig. la). It increased through June when the peak of attached biomass occurred. In July, much Cladophora had detached from the bed and floated as mats in slack water in pools or along channel margins. Biomass of both attached turfs and floating mats of algae decreased in late July and August, although the proportion of monitored sites with these algae remained high until September when most Cladophora was reduced to detritus (Fig. la). More description of Cladophora phenology in the South Fork Eel is reported in Power (1990a, b).

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TABLE 1.-Composition of recognizable items in guts of Pseudochironomus richardsoni

Mean proportion (SE)

Cladophora, fulla 0.01 (0.02) Cladophora, emptya 0.13 (0.08) Other filamentous green algae, full 0.01 (0.01) Other filamentous green algae, empty 0.03 (0.03) Diatoms, full 0.00 (0.00) Diatoms, empty 0.72 (0.11) Coccoid unicells 0.08 (0.09) Other 0.03 (0.03)

a "full" - cell contents cover 225% of projected cell area; "empty" = cell contents cover <25% of projected cell area

Retreats of tuft-weaving midges were not apparent in Cladophora until late June but increased markedly thereafter until late July. A second increase in the proportion of algae infested occurred in October, because the small amount of algae that remained in the channel at this time had midge retreats (Fig lb). This proportion of all sites monitored that had tufted algae peaked in July, when 40% of all sites monitored had algae woven by midges (Fig. lc). During this peak infestation period, 80-95% of the biomass of sampled Cladophora mats was incorporated into chironomid retreats, as indicated by the lumpy appearance of these mats (Fig. 2). Effects of colonizing midges on Cladophora. -When Cladophora was retrieved from the field enclosures after 20 d of incubation in the river, clumps had been colonized by up to 21 larval chironomids. Only a few individuals of other insect taxa colonized Cladophora clumps (28/354 individuals counted); these were largely early instar hydrophilid and naucoriid larvae. Their abundance was uncorrelated with abundance of chironomids or the final weight of Cladophora. There was, however, a significant negative relationship between damp weight of stocked algae and the number of chironomids which had colonized an enclosure (Fig. 3), suggesting that midge larvae had a negative effect on algal biomass over the first 20 days of their colonization and occupation of Cladophora. Effect of midges and old and new retreats.-The incubation of Cladophora with nitrate fertilizer and with old and newly constructed midge tufts allowed comparison of the effects of recent colonists and older larvae nearing pupation. The latter had filled their tufts with fine particulate material which was hypothesized to be a potential nitrogen source. After the 19-day incubation, nitrogen levels, algal pigments and damp weights of the incubated Cladophora all differed among treatments (Table 2-4). Significant experimentwise effects for nitrate and ammonia were detected (P = 0.008 and P = 0.009, respectively from Kruskal- Wallis tests). Not suprisingly, nitrate levels were highest in the Na2NO3 addition treatment and lowest in the controls. This contrast in nitrate concentration was the only significant one (P < 0.01) revealed by a nonparameteric multiple comparison test (Dunn's Q for unequal sample sizes, Zar, 1984: p. 200). For ammonia concentrations, the only significant difference was between the nitrate addition treatment (highest ammonia) and the old tuft treatment (lowest ammonia) (P < 0.01 from Dunn's Q test). Concentrations of both nitrogen and ammonia were much higher in the enclosed containers than in the ambient water of the flowing stream, even in controls (Table 2). This was probably due to the release of nitrogen compounds from senescing and decaying organic matter into small volumes (initially 800 ml, evaporating to ca. 500 ml in all treatments) of water. Phosphate levels did not differ

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FIG. la.-Proportions of monitored sites with Cladophora. b. Proportion of sites with Cladophora where algae was woven into tufts by midges. c. Proportion of all sites monitored with midge-woven Cladophora (c = a x b)

among treatments (P = 0.489) and were not greatly elevated above ambient levels in the river (Table 2). Chlorophyll a content differed among the four treatments (P < 0.007, two-tailed Kruskal- Wallis test) and was higher for old tuft additions and nitrate additions and lower for new tuft additions and controls (Table 3). A nonparametric Tukey-type multiple comparisons test (Zar, 1984: p. 199-200) showed that chlorophyll a in algae with added nitrate was significantly higher than chlorophyll a in controls or in algae with new midge tufts (P < 0.01 and P < 0.05, respectively), but not higher than in algae with old midge tufts. Pheophytin, a breakdown product of chlorophyll, differed among the four treatments (P < 0.03, two-tailed Kruskal-Wallis test). The multiple comparisons test showed significant differences between the nitrate treatment (least pheophytin) and the new midge treatment (most pheophytin) (P < 0.05). Chlorophyll to pheophytin ratios, reflecting algal condition (Wetzel, 1983), were <1 in controls and new tuft treatments, and >1 in nitrate and old tuft treatments (Table 3). Cladophora weight change at the end of the 1 9-d experiment was significantly different among the four treatments (Table 4, P = 0.01 5, two-tailed Kruskal-Wallis). Controls and treatments with new midge tufts each had lower final weights than either nitrate treatments or treatments with old tufts (P < 0.001, Dunn's nonparametric multiple comparisons test

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FIG. 2.-Photograph of midge-infested Cladophora taken in July in the South Fork Eel. Each lump is a tuft ca. 1 cm long, containing one or more chironomid larvae or pupae

for each of these four pairwise comparisons, Zar, 1984: p. 200-201). No other pairwise comparison was statistically different.

DISCUSSION

Grazers exert both harmful and beneficial effects on plants (Porter, 1977; Harper, 1977; D'Antonio, 1985; Cattaneo, 1983; Belsky, 1986; Sterner, 1986; Brawley and Adey, 1981a, b). Results from this study suggest that negative and positive effects of tuft-weaving midges inhabiting Cladophora shift in relative importance over time. Initially, when larvae first colonize and weave algae into tufts, effects of midges on algal biomass are negative. Later, when tufts are filled with feces and occupied by older, less active larvae or pupae, there may be positive effects on algae, as suggested by higher chlorophyll a content and biomass. Various mechanisms could account for early negative effects of midges on Cladophora. Midges ingested some Cladophora, but fed more heavily upon epiphytic diatoms. In some studies, epiphyte grazing has been reported to benefit host algae (e.g., Brawley and Adey, 1981a, b). Epiphytes can shade host plants (Sand-Jensen, 1977; Stevenson and Stoermer, 1982), compete with them for nutrients (Fitzgerald, 1969), increase drag and the probability of host detachment (D'Antonio, 1985; Black, 1976; Menge, 1975), and damage cell surfaces (Rogers and Breen, 1981; Howard-Williams et al., 1978), increasing chances of invasions by pathogens. Grazers of epiphytes may incidentally damage host surfaces with similar results (D'Antonio, 1985; Goff and Cole, 1976). Relationships among epiphytes, host plants and micrograzers are variable and complex (Hay et al., 1987; D'Antonio, 1985). In this study, any potential benefits of epiphyte grooming are outweighed by negative effects on filamentous host algae of young chironomids during their period of active tuft construction. Fragmentation of algae during tuft construction would increase export of Cladophora. In experimental channels, chironomids increased drift of attached algae 5-7-fold (Eichenberger

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Number of Midges per Enclosure

FIG. 3.-Final Cladophora damp weight versus larval midge density after 20 days in enclosures. The regression fit to the data is: Final damp weight (g) = -0.23 (number of midge larvae) + 4.89; r2= 0.18, n = 48, P < 0.005

and Schlatter, 1978). Weaving may reduce Cladophora growth if it reduces light reception. These hypotheses have not yet been evaluated in our system. Chironomids that construct retreats benefit local algae by creating micropatches of nutrients (Pringle, 1985). The importance of nutrient micropatches has been shown in lakes (Lehman and Scavia, 1982). In the present study, beneficial effects of older midge tufts on Cladophora or its epiphytes were suggested by the second field experiment. Algal growth and condition were better with old tufts or fertilizer than when algae were incubated alone or with new tufts. Field incubations were carried out under natural light and temperature regimes, and density of midges (2 individuals per g damp weight of algae) were within ranges commonly observed in the South Fork (Power, 1990a). Flow and chemical conditions

TABLE 2.-Nutrient levels in containers and in ambient river water following Cladophora incubation with new and old midge tufts

NO3-N (,ug/liter) NH3-N (,ug/liter) P04-P (,ug/liter) Treatment R (SE) R (SE) R (SE)

Cladophora (n = 4%)* 477 (349) 248 (21) 26 (10) Cladophora and Na2NO3 (n = 5) 5735 (154) 729 (60) 14 (9) Cladophora and new tufts (n = 4)* 1786 (828) 246 (25) 22 (6) Cladophora and old tufts (n = 4)* 1546 (1262) 172 (45) 12 (3) South Fork river water Sept. 10, end of experiment (n = 3) 8 (5) 24 (8) 7 (4) South Fork river water Aug. 22, beginning of experiment (n = 3) 6 (2) 9 (0.3) 6 (2)

* One sample spilled in the field

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TABLE 3.-Chlorophyll a and Pheophytin a (,tg/g dry weight) in Cladophora following field incubation with Na2NO3 and old and new midge tufts

Chlorophyll a Pheophytin a Treatment Mean (SE) Mean (SE) Chl a/Pheo a ratio

Cladophora (n = 5) 172 (43) 220 (26) 0.78 Cladophora and Na2NO3 (n = 5) 1140 (42) 69 (14) 16.52 Cladophora and new tufts (n = 5) 165 (25) 233 (27) 0.71 Cladophora and old tufts (n = 5) 280 (69) 193 (42) 1.45

in the in situ enclosures were artificial, due to the lack of exchange with ambient river water. At the end of these experiments, levels of N03-N and NH3-N were much higher in experimental containers than in ambient river water. Given these conditions, responses of algae to treatments, insofar as they depend on nutrient levels or concentrations of other chemicals, must be extrapolated with caution to predict responses of algae in the open river. Extrapolation is not altogether unwarranted, however, as algal mats infested with tuft- weaving chironomids are often situated in still or stagnant water and flow within the mat is much reduced.- Because of the intimate contact of algae with fecal accumulations in tufts, the local availability of released nutrients could be quite high. Nitrogen is sometimes limiting for algae in the South Fork (Power, 1990b). In experimental containers, levels of nitrate in ambient water were highest with the nitrate fertilizer, similar with old and new tufts, and lowest in midge-free controls (Table 2). Ammonia levels were highest in fertilized treatments and significantly lower only in old tuft treatments (Table 2). Phosphate levels did not differ among treatments. At first glance, these results might suggest that new tufts were better sources of ammonia nitrogen than old tufts. For example, midge excretion may have contributed to ammonia pools. Nitrogen concentrations of the water, however, are lowered by uptake by healthy algae, and raised by leakage from damaged algal cells. In new tuft treatments, algae damaged by activities of midges may have leaked ammonia, and damaged cells may have had slower uptake rates. The second interpretation is supported by the differences in levels of chlorophyll a among treatments. Chlorophyll a levels were highest for fertilized algae, next highest for Cladophora with old tufts, lower for controls, and lowest for Cladophora with new tufts (Table 3). Pheophytin, a breakdown product of chlorophyll often associated with grazing (Wetzel, 1983), was highest in Cladophora with new tufts, second in controls, third in Cladophora with old midge tufts, and lowest in fertilized Cladophora. Together, these pigment concentrations suggest that

TABLE 4.-Weight of Cladophora after incubation with Na2NO3, new midge tufts, or old midge tufts

Damp weight (g) Treatment Mean (SE)

Cladophora (n = 5) 3.5 (0.1) Cladophora and Na2NO3 (n = 5) 4.2 (0.1) Cladophora and new tufts (n = 5) 3.5 (0.3) Cladophora and old tufts (n = 4)* 5.3 (0.7)

* One replicate spilled

This content downloaded from 136.152.142.49 on Thu, 14 Jul 2016 00:48:08 UTC All use subject to http://about.jstor.org/terms 1991 POWER: TUFT-WEAVING MIDGES 283 chlorophyll a synthesis increased with nitrogen, and that algae were in better condition [as suggested by chlorophyll: pheophytin ratios (Table 3)] in the presence of old tufts than with new tufts, or with no tufts. This interpretation is further supported by the finding that final weights of algae were higher in old-tuft and fertilized treatments than in controls and new- tuft treatments. This study indicates that effects of tuft-weaving midges on Cladophora are complex and change as midges and their tuft retreats age. Their ecosystem-level effects will depend on the duration of negative versus positive effects and the timing of these impacts relative to other seasonal influences on algae. For example, the importance of nutrients leached from midge feces would depend on ambient nutrient availability, which changes seasonally. In addition, epiphyte loads on Cladophora increase over the summer period (personal obser- vations in the Eel River, Stevenson and Stoermer, 1982), and nutrients cycled late in the summer may benefit these epiphytes to the detriment of their filamentous hosts (Fitzgerald, 1969). Another study in which densities of tuft-weaving midges were altered on a large spatial scale by manipulation of predators indicated that, over a six-week period, the overall effect of midges on algal biomass was negative (Power, 1990b). In treatments which reduced densities of midges 8.5-fold, the biomass of attached algae was six times higher than in treatments with higher midge densities, and that of algae which detached to float on the water surface was 69 times higher. In treatments with low midge densities, Cladophora became heavily overgrown by nitrogen-fixing epiphytes (Power, 1990b). The Cladophora stubble that remained in treatments with high midge densities had lighter epiphyte loads and was visibly greener. Thus, although midges had negative effects on the macroalga over the six-week experimental study, they may have had positive longer term effects. If groomed free of epiphytes, Cladophora, rather than its epiphytes, could capitalize on release from grazing pressure as water temperatures and activities of micrograzers like larval midges drop during late summer. The stage would be set for the secondary, late summer or early autumn Cladophora blooms observed during some years in Northern California rivers (Pow- er, 1990c) and during most years in the Great Lakes (Blum, 1982). While large grazers such as crayfish (Lodge and Lorman, 1987) or algivorous fish (Power et al., 1985) exert clearly negative effects on freshwater algae, interactions of macroalgae with small grazers are more complex (Bronmark, 1989; Hay et al., 1987). Cironomids (Oliver, 1971) and Cladophora (Whitton, 1970) dominate the biotas of littoral freshwater habitats worldwide. Their abundance points to the need for more studies on a variety of temporal and spatial scales (Frost et al., 1988), to assess mechanisms, controls and impacts of their interactions.

Acknowledgments. -I would like to thank Habte Kifle, Jennifer Nielsen, Lisa Palermo, Wilson Power, Karen Treacher and Rhea Williamson for assistance in the field and the laboratory, Lisa Palermo for help with data reduction, Peter Steel and The Nature Conservancy for access to the site, and Mike Winnell and Leonard Ferrington for identification of chironomids. Jack Feminella, Bill Rainey, Bill Dietrich and Walter Dodds made comments on the manuscript. I am especially indebted to Rex Lowe and Phycology Night (Department of Biological Sciences, Bowling Green State University for their comments and encouragement. This study was supported by the California State Water Resources Center (W-726) and the National Science Foundation (RII-8600411).

LITERATURE CITED

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SUBMITTED 21 MAY 1990 ACCEPTED 11 FEBRUARY 1991

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