Hydrologic and Trophic Controls of Seasonal Algal Blooms in Northern California Rivers

Arch. Hydrobiol. 125 I 4 385-410 I 1 Smrrgm, Okrober 1992

Hydrologic and trophic controls of seasonal algal blooms in northern California rivers

By MARYE. Po-, University of California at Berkeley’

With 15 figures and 1 table in the text

Abstract Ckzdophoru glomeruta L., a dominant macroalga in lakes and rivers worldwide, undergoes a marked bloom-detachment-senescencecycle in unregulated rivers of northern California with natural winter flood, summer drought flow regimes. In two regulated channels which probably did not experience scouring floods, however, low standing crops of attached Cladopboru turf persisted throughout the year. The contrast between Ckzdophora phenology in regulated and unregulated rivers suggests that Cla- dophoru cycles may be extrinsically driven by factors related to the hydrograph. Pre- liminary data on seasonal patterns of animal abundance in regulated and unregulated channels suggest that winter flooding promotes Cladophoru blooms in rivers by reducing consumer densities. A working hypothesis relating hydrologic regime, food chain length, and algal phenology in rivers is advanced. This hypothesis predicts that pronounced algal bloomdetachment-senescence cycles will occur in unregulated rivers in Mediterranean climates following winter flooding, and that blooms will not occur in the absence of flooding in regulated channels, or in natural rivers during prolonged drought.

Introduction In rivers which are sunlit, rock-bedded, and clear at low flow, attached algae are often dominant components of ecological communities. Cludophoru gfomerutaL., a filamentous green, may be the most common and cosmopolitan macroalga in temperate rivers throughout the world (BLIJM,1956; WHITTON, 1970; WHAFSEet al., 1984). In sunlit rivers of the western United States, Cla- dophoru provides much of the physical structure in the habitat during the low flow season, and plays a driving role in food web dynamics (LAMBERTI& RF.SH, 1983; Gw,1987; FEMINELUet al., 1989; POWER,1990 a, b). In these rivers and elsewhere (notably in the Laurentian Great Lakes), Cludophoru blooms create severe management problems (BLUM,1956, 1982; BELLIS, 1967; AUERet al., 1982; MILLNER& SWEENEY, 1982; GOLDMAN& HORNE, 1983). Despite their ecological and economic importance, factors regulating growth, detachment, and senescence cycles of Ckzdophoru are still not well understood (WHI-ITON, 1970; NEIL&JACKSON, 1982).

’ Author’s address: Dept. of Integrative Biology, University of California at Ber- keley, Berkeley, CA. 94707, USA.

25 jrchiv f. Hydrobiologie, Bd. 125 0003-9136/92/0125-0385$6.50 0 1992 E. Schwcizerbm’scbe Vcrlagsbuchhmdlung.DJDXI Stuttgm 1 386 Mary E. Power Hydrologic and trophic controls of seasonal algal blooms 387

This study addresses three questions about Ckdopbora in northern Cali- fornia rivers: 1. What is the seasonal cycle of Ckzdqhora in rivers with natural summer drought, winter flood hydrographs? 2. How does this cycle compare with Cladophoru phenology in regulated rivers with artificially stabilized flow? m Eureka 3. How do abundance patterns of invertebrates and smallvertebrates associated with Cladophoru change seasonally in regulated and unregulated chan- 2 nels? To develop hypotheses about factors governing timing, magnitude, and duration of algal blooms and mat detachment, I monitored Cludophora, physical factors, nutrients, and associated biota in four unregulated and two regulated rivers in northern California. Results from this survey complement ex- perimental studies on smaller spatial scales of controls on this dominant river dga (LAMBEXTI& ~SH, 1983; LIGON,1986; FEMINELLAet d., 1989; POWER,1990 a, b). \

Study Sites I monitored six rivers near sites gaged by the United States Geological Survey (USGS) (Fig. 1). These rivers differed in discharge, exposure to sun, and land use in their watersheds. Two rivers were regulated upstream of the monitored sites, either by a dam (Dry Creek) or by a water diversion (from the Eel River to the East Fork of the Russian River) and had artificially sustained summer baseflow (Fig. 2 e, f, Fig. 3). Dry Creek experienced stable low flow throughout the year. Dividing discharge by channel drainage area indicates that releases from the Warm Springs Dam above Dry Creek were considerably less than natura winter flows in channels of similar drainage area in this region (Fig. 4). Consequently, the bed of Dry Creek was stable throughout the period of study. To compare the relative intensity of bed movement for the remaining five rivers, I used two empirical generalizations about gravel bedded riven. First, bankfull discharge typically has a recurrence interval of about 1.5 years (e.g. DUNNE& LEOPOLD,1978). Sec- Fig. 1. Location of the six study reaches (numbers 1,2,4-7) and of a diversion from the ond, significant gravel bed mobility often does not occur until the flow is close to bank- Eel River to the Russian River (3) that stabilizes flow in the East Fork Russian River discharge (Pmmn, 1978). In the East Fork Russian River, elevated winter flows oc- full (site 2). Drainage areas above the six monitored sites are, for the two regulated channels: curred, but peak discharge in 1989 remained below bankfull discharge as estimated from (1) Dry Creek (USGS 11465000): 562km', and (2) East Fork Russian River (USGS flood frequency analyses (Fig. 5). Hence, it is likely that little bed movement occurred. 11461500): 239 km2. For the four unregulated channels, drainage areas are (4) Outlet This inference is consistent with visual observations that the bed of the East Fork Creek (USGS 11472200): 417kmz; (5) Middle Fork Eel (USGS 11473900): 1929 km2; (6) Russian River showed no evidence of scour over the period of study. In contrast, the South Fork Eel (USGS 11475500): 114km' and (7) Elder Creek (USGS 11475560): other four monitored rivers, which were unregulated (the South Fork Eel River, Elder 17km'. Creek, Outlet Creek, and the Middle Fork Eel River), experienced the natural summer drought, winter flood hydrograph typical of streams in regions with Mediterranean climates (Fig. 2 a-d). Each unregulated river experienced flows equal or greater than bankfull discharge during the 1988- 1989 study period (Fig. 5). Visual observations over the summer (Fig. 3). During October, the month of minimum discharge in natural chan- the winter confirmed that beds in these four rivers moved, and were subject to consid- nels, most monitored sites had current velocities slower than 5cms-'. In the two re- erable scour. gulated rivers, current velocities during October ranged from 0 to > 50cms-', and During the summer low flow season, from June through September, the four unre- were fairly evenly represented among the monitored sites (Fig. 6). Despite the large gulated rivers experienced low or no discharge (Fig. 3). In contrast, flows in Dry Creek variation in drainage areas and discharges of the six rivers (Fig. 1, legend), in summer and the East Fork Russian River were maintained at levels ranging from 2-4 m's-' over months they were all easily waded. Hydrologic and trophic controls of seasonal algal blooms 389 388 Mary E. Power

Low Flow Discharge S. Fk. Eel, 1988-1989

m -mwl P -0- SouthFkEel - ElderCreek - OutletCreek - Middle Fk. Eel East Fk. Russian

May Jun Jul Aug Sep outlet Creek. 1988-1989 Fig.3. Mean monthly discharge during the summer low flow season in the four unregulated (solid lines) and two regulated (dashed lines) channels. Note that in August and September, when there was little or not flow even in the large unregulated rivers, flow continued in the two regulated channels.

salmon hatchery just below Warm Springs Dam, upstream from monitored sites. Both sources contribute nutrients to the stream, and probably account for its relatively XpBi91Pp3~so elevated levels of nitrate (Fig. 8). The East Fork Russian River near Ukiah receives water diverted from the Eel River through the Potter Valley Diversion (Fig. 1). The East Fork Dry Creak, 1988-1989 E. Fk. Russlan RIver, 1988-1989 Russian does not receive agricultural runoff, but human habitations occur very close to the river just upstream from the monitored cross sections. This river had the second I\ -m :a highest measured level of nitrate of the six studied here (Fig. 8). Insolation of the E. Fk. Russian, however, was much less than at Dry Creek due to shading during mornings and afternoons by tall alder trees and narrow valley walls. Outlet Creek is not regulated, but is otherwise heavily impacted by humans. Many human dwellings occur along the creek, which also receives sewage effluent from the town of Willits (Fig. 1). Of the unregulated streams, Outlet Creek has the highest measured nitrate levels (Fig. 8). Outlet Creek is extremely open and sunlit, as the active, boulder-strewn channel kept open by winter floods is much wider than the wetted channel during the summer low flow period. This is also the case along the monitored Fig.2. Monthly discharge records (from the USGS) for the four natural (a-d) and two reaches of the Middle Fork Eel. The land around the Middle Fork Eel is sparsely settled regulated (e, f) channels. Records for the South Fork Eel are from a currently monitored by humans, and subject to light cattle grazing. Crystal-clear water and low nutrient station near Leggett, CA, where the drainage area is 642 km', 5.6 times larger than at the levels (Fig. 8) suggest little human impact on this river at the monitored site. The South study site near Branscomb, where USGS monitoring was discontinued. During Fork Eel River flows for 5 km through a 3200 hectare forest preserve (the Northern 1968 - 1970 when Branscomb and Leggett stations were both monitored by the USGS, California Coast Range Preserve) and is also relatively undisturbed by humans, al- discharges were highly correlated (0.93 < r < 1.00 for 18 of 24 consecutive months, though sparse settlements and a sawmill occur upstream from the monitored site. As in 0.27 < r < 0.78 during four transitional spring or fall months (May, June, August, and Outlet Creek and the Middle Fk., winter floods open a wider channel in the S. Fk. Eel September). Discharge at Leggett was 5-6 times greater than at Branscomb during this than is wetted during low flow, so much of the river bed is sunlit. However, much of period. the channel is shaded during early morning and late afternoon by a tall bordering forests of mature Douglas fir (Psedotsugu menziesii) and redwood (Sequoia semperuirens), and The two regulated rivers also had similar proportional size distributions of bed sedi- by valley walls. Elder Creek is the least disturbed of all the monitored rivers, with the largest undisturbed Douglas forested watershed remaining in California (TRUSH, ments (Fig. 7), but otherwise differed considerably in their physical and chemical con- fir 1991). Its watershed was sparsely settled by homesteaders at the beginning of the cen- ditions. Dry Creek is an open, sunlit stream bordered by scrubby willows (Sulzx spp.) and alders (Alnus rbombifoliu). The creek flows from the Warm Springs Dam impound- tury, but presently experiences minimal human impact. Elder Creek is shaded for most of its length by steep valley walls and oak (Lithocurpusdensifonrs and Quercus spp.) and ing Lake Sonorna through vineyards with little topographic relief, and joins the Russian Douglas fir-dominated forest. River (Fig. 1). Dry Creek receives, in addition to agricultural runoff, effluent from a 390 Mary E. Power Hydrologic and trophic controls of seasonal algal blooms 391

South Fork Eel Elder Crook 200 W 190 a 180 m I 70 g 1w 160 150 140

X 130 nm 120 110

'O0#.O 1.1 1.2 1.3 1.1 1.5 1.6 1.7 1.8 1.0 2.0

Recurrence Interval (years) Outlet Creek 150 C -m 1000 20 900 18 800 16 700 14 600 m 12 500 R 10 400 8 300 6 ra X 200 I 4 100 2

1.0 1.1 1.2 1.3 1.4 1.5 1.6 1.7 1.1 1.0 2.0 Dry Creek East Fork Ruaalan 4.0 1.1 1.2 1.3 1.4 1.5 1.6 1.7 1.8 1.0 2.0 W 150 2 150 Recurrence Interval (years) Recurrence Interval (Years) e -mean < f -mm -rma -mx

500 -min I ... 450 4 400 sa 350 m 300

.c 4 250 200 n.s X 150 Fig. 4. Monthly discharge from channels, divided by channel drainage area, to show the X nm 100 a amount of precipitation discharged as runoff, illustrating the effect of storage by the 50 Warm Springs dam in depleting runoff in Dry Creek. '1.0 1.1 1.2 1.3 1.4 1.5 1.8 1.7 1.1 1.9 2.0

Recurrence Interval (years) Recurrence Interval (Years) Methods Fig. 5. Recurrence intervals for momentary peak discharge showing the 1989 peak dis- I established three permanent cross-stream transects along monitored reaches of charge in relation to that with a 1.5 year recurrence interval, which gives an estimation each river. At points at 0.5-m or 1.0-m intervals along each transect, I measured water of the bankfull flow (DUNNE& LEOPOLD,1978). Flood recurrence intervals were es- depth, current velocity (with a low velocity threshold rotary current meter (Roy timated from 40 years of record in the E. Fk. Russian River; from a 25 year record in the Olund, Dept. of Oceanography, Univ. Wash., Seattle Wa.)) and described substrate S. Fk. Eel; from a 23 year record in Elder Creek; from a 34 year record in Outlet Creek; composition (classified by median particle size according to the modified Wentworth and from a 25 year record in the Middle Fk. Eel. scale (HYNES,1970, p. 24)). Using a face mask for underwater observation, I visually estimated an area of 10 x 1Ocm' under each sampling point, and noted: the genera of measure modal height of filaments or maximum diameter of floating algal mats); and dominant and subdominant algae; their height (I used a meter-stick or a 15cm ruler to their density and condition, (categorized as indicated in Table 1; see POWERet al. (1985) 392 Mary E. Power Hydrologic and trophic controls of seasonal algal blooms 393

\\\\\\\\\....\.\\,,,,,,*,,,,##,,, \\\\\\\.\\.\\\\\\ South Fork Eel River Elder Creek \\\\\\.\\\\\\\\\\,,,,,,,,,,,,,,,, 31 40 31-50

21 40 21.30

11-20

5-10

<5 00L 0.1 0.2 0.3 0.4 0.6 0.6 0.7 0 0.0u 0 I 0.2 0.3 0 4 0 6 0.8 0.7 10 0.6 0.6 1.0 0.0 0.2 0.4 0.6 0 8 0.0 0.2 0.4

J -! Ylddle Fork Eel River

,., . I . ,. , . , . , . , . , e- ,',',','#',',','# .\..\\\\ ,,,,,,,,,,,*\\\\\.\.. ::!B P*L*...... \\\\\.\\.. Mu+S.rdD, , , , , , I e . '5 > <5 0.0 01 02 03 Ob 0.5 06 0.7 0.0 0.1 0.2 03 04 0.5 06 07 0 0

0.0 0.2 0.4 0.6 0 8 1 0 0.0 0.2 0.4 0 6 0.8 1.0 Boyld.r-B1rosk I East Fork Dry Creek Rusrlan Rlver I (Regulated) 1 > 50 >E4 (Regulated) ...... COMh .;\;.;.;.;.;.; . 31-y1 u 31.50 .E 21.30 \\\\\\\\\\\\\\ \\\\\\\\\\,\,,,,,,,,,,, u 21-30 : P.M.. \'\'\'\'\'\'\'\'\'\'.'.'.'.',,,,,,,,,,,,,, - \\\\\\\\\\\\\\ : Phbl" .\.....\\\\\...... , 11.20 * 11-20 11 I iB .- t4Ld-S.m '4' 5-10 -:: 5.10 , , . , J e D,, 0 0 0 I 0 2 0 3 0.4 0.3 0.6 0.7 0.0 01 02 03 04 0.3 06 07 <5 > <5

Praporllon 01 SII.. PrOpDrtlDn 01 SIl.. 0.0 0.2 0.4 0 6 0 8 1.0 00 0.2 0.4 0 6 0 8 1.0 Fig. 7. Proportional distribution of bed sediments in mud-sand (median diameter < Proportion of Sites Proportion of Sites 2mm), pebble (2-64mm), cobble (65-256mm) and boulder to bedrock (> 256mm) size classes. Sample sizes (numbers of sites sampled) were S. Fk. Eel: 66; Elder Creek: 38; Fig. 6. Proponional distributions of current velocities measured at sampling sites during Outlet Creek: 48; Middle Fk. Eel: 75; E. Fk. Russian: 52; and Dry Creek: 76. (Sample October, at the time of lowest stream flow during the study period. Sample sizes (num- sizes exceed those for current velocities because they include some sites too shallow for bers of sites sampled) were S. Fk. Eel: 49; Elder Creek: 32; Outlet Creek: 48; Middle Fk. current velocity measurement). Eel: 73; E. Fk. Russian: 50; and Dry Creek: 76. given sampling date. When low flow cut off marginal pools from the main channel, and POWER & STEWART(1987) for further methodological details). I also recorded the however, pool water was sampled separately. presence of macroscopically conspicuous animals within the observed area under each Water samples were filtered within 4-h of collection through Whatman GF/C, then point, and collected representative samples of unfamiliar algae, macrophytes, and ani- through Gelman Metricel GN-6 0.45 micron filters, to remove particulates and algal mals for identification. cells. Filtration with Nalgene hand pumps was done at pressures of less than 10- 12psi At each transect site, I collected water samples in acid-cleaned 1-liter polyethylene to avoid rupture of cells. Filtered samples were stored frozen until analyzed chemically. botrles. To assess spatial variarion in nutrient concenrrations, six water samples were in- Nitrate was analyzed using a hydrazine sulfate method (KAMPHAKEet al., 1967); am- itially collected at each cross-section, near the surface and near the bed at three cross- monia was analyzed by a phenolhypochlorite method (SOLORZANO,1969), and soluble channel positions. No cross-stream spatial variation was detected, even at low flow reactive phosphorus was measured with a stannous chloride technique (American (I)OWI.ILIwo~~), SO .Iitcr I'IXX WIIY (1111. t)r Iwt) s.III11dl.s pcr tr.i~lscl.t WCI'C COIIC~.IC~I OII .I hhlk 1 Ic.iltli Asvociiition, 1985). These thrcc tcchniqucs Iiwc Iowcr wmitivity 394 Mary E. Power Hydrologic and trophic controls of seasonal algal blooms 395

Results i. Seasonal changes in Cladophora and other primary producers 80 "4-N T Cycles of bloom, detachment, senescence, and decomposition of Cla- were observed in four unregulated rivers during the low flow pe- L N03-N I dophoia all riod, but were more pronounced in the three sunlit channels (Fig. 9a-d). In Elder Creek, the most shaded of the natural channels, less algae accumulated. The accrual of algae during the low flow period was visually striking in all three sunlit channels, and locally in sunlit patches within Elder Creek.

60 A attached 0 loose 40

0 Fig. 8. Average concentrations with 1 SE of nutrients in the six monitored reaches. Samples were collected on survey dates; no seasonal variation was detected. Middle Fork Eel

Table 1. Categories for density and condition ranking of algae. - Density: .- cQJ 20 0: none detected 401 P I1 , or (< \" 1: a few filaments small isolated patches 5 mm diameter) i, , , , , , , , , , 2: < 10% canopy cover 3: IO-25% canopy cover East Fork Russian 4: > 25% canopy cover, but can still see primary substrate (Regulated) (Regulated) 5: substrate completely obscured by algal canopy Condition (Cladophora): 40 detritus 0: 20 1: detritus with a few recognizable filaments 2: pale, weak, senescent in appearance 0 3: discolored green: yellow or rusty with epiphyte or silt loads S 0 N D J FMA M J J A S S OND JFMAM J J A S 4: more green, filaments more robust 5: deep, bright green with fresh-appearing growth Month Fig. 9. Averaged heights or lengths of attached or loose (floating or deposited) algae in encountered at monitored sites in the six study reaches. Algal assemblages were do- thresholds of 1 pgA, 5pgA and 1pgA, respectively. Nutrient absorbance readings were minated by Cladopboru from June-September in the four unregulated reaches, and at all measured in 5 or lOcm cuvette cells on a Bausch and Lomb Spectronic 21 spectro- sample dates in the two regulated channels. All sample points are averages from 15 to 41 photometer. Low concentration samples were spiked with known concentrations of measurements of loose or attached algae on a given sampling date. From November to standard solutions to bring absorbance into the best measurement range for the instru- March, when the four unregulated streams were too high to wade, visual inspection re- ment. vealed no conspicuous macroalgae. 396 Mary E. Power Hydrologic and trophic controls of seasonal algal blooms 397

In contrast, no massive bloom or seasonal die-off of Chbpbwa or other stable discharge of the two channels also permitted growth along their margins algae occurred in either the shaded or the sunlit regulated river (Fig. 9 e, f). In of vascular macrophytes including Potamogeton, Veronica, Nasturtium, Lemna, both the E. Fk. Russian River and Dry Creek, short but healthy-appearing and Elodea. (green, robust) Cladophora turfs dominated primary producer assemblages In the four unregulated rivers and creeks, November floods scoured all throughout the year (Fig. 10e, f), although more sites were dominated by bare macroscopically conspicuous algae from the channels. Macroscopically visible substrate or detritus in the more shaded E. Fk. Russian. Loose algae was not algal growths first appeared on rock substrates in March. By April and early encountered along transects in the E. Fk. Russian River, with the exception of May, diatoms, cyanobacteria (Rivularia Nostoc, and Odlatoria), and the fil- a single thin strand of drift algae, 20cm in length, in October. The relatively amentous green alga Zygnemi dominated producer assemblages in three of the four unregulated rivers (Fig. 10). (Algal abundance and composition in the Middle Fork Eel were not monitored until June, when the river became low enough to wade). Zygnema grew as bright chartreuse turfs 10-40 cm long. By late May Zygnema was intermingled with Cladophora at many sites. By June, Zygnema was replaced by Cladophora at most sites. For example, in Outlet Creek, there was a large bloom of attached algae dominated by attached Zyg nema mixed with CIadophora that covered 60% of the bed (Fig. 10). By June, floating mats and attached turfs of algae dominated by Cladophora covered al- most 80% of the channel (Fig. 10). Zygnema in the South Fork Eel persists through the summer only in fast-flowing riffles (M. POWER,personal observations from 1987- 1991). Cladophoru turfs first appeared in the South Fork only on bedrock and boulder (> 256 mm median diameter) substrates. After June, small attached Cladopbora filaments appeared on smaller cobbles and pebbles; these became abundant after late July (Fig. 11).

Substrates with Attached Cladophora

1: 40 ai v) 0 Cobbles, Pebbles c Boulders, Bedrock v).- H .c O 20 L 0) n - f 10 f z 0 Fig. 10. Proportion of monitored sites dominated on a given sampling date by various 0 100 200 producer taxa, or by bare space. Three transects were monitored per channel per survey; FMAMJ J AS0 the total numbers of sites under transects varied with river width and stage: Elder Creek: Fig. 11. Number of monitored sites in the South Fork Eel, separated by substrate size, 21-37 sites; South Fork Eel: 38-55 sites; Outlet Creek: 45-50 sites; Middle Fork Eel: with attached Cladapboru. Pebbles and cobbles range from 16-256mm median 63-78 sites; East Fork Russian: 52-55 sites; Dry Creek: 73-77 sites. diameter; boulders and bedrock substrates are > 256 mrn median diameter. 398 Mary E. Power Hydrologic and trophic controls of seasonal algal blooms 399

Standing crops of Cladophoru, indexed by height of attached turfs or length 0.8 a South Fork Eel of detached mats peaked in midsummer and decreased afterwards (Fig. 9). Most 0.6 A Mobile Drev filamentous green algae had disappeared or decomposed by early fall, before the onset of winter floods. In Outlet Creek, the warmest and most eutrophic of the unregulated rivers, fall senescence of Cladophoru was particularly pronounced. On Oct. 2, 1988, no living Cladophoru was found in the channel, although white Ckzdophoru “paper” was stranded along the shore. The bed of I- Outlet Creek at this time was covered with Cladophoru-derived detritus, with Middle Fork Eel adnate Rivulurk spots stones representing the only conspicuous living alga. .-Ia, 0.8 A Outlet Creek d on (I)

2. Seasonal changes in conspicuous fauna

Abundances of visually conspicuous animals in the water column or on the surface of the river bed under monitored sites were estimated semi-quantita- tively with presence/absence observations. These observations suggest that the densities of particular guilds differed among the six rivers. Sessile primary consumers (eating primarily plants or detritus (LAMBERII& MOORE,1984)) were abundant in the two regulated rivers on all sampling dates, while their frequency of occurrence rose, then declined in the two frequently monitored unregulated 0.4 rivers (S. Fk. Eel and Elder Creek) over the low flow season (Fig. 12a, b). -11 1 114I Mobile taxa initially dominated the primary consumer guilds in both of these rivers. Subsequently, in the South Fork Eel, predators increased, mobile 0.0 SONDJFMAMJ JAS S N DJ FM A MJ J A S primary consumers decreased, and sessile primary consumers increased. In the o.2uJUJ0 darker Elder Creek, similar trends occurred, but were seasonally delayed. Pre- dators and omnivores (animals eating both animal and plant-detrital foods) Month were less frequently observed in regulated than in unregulated channels (Fig. 12). Fig. 12. Seasonal changes in abundance estimates of members of three consumer guilds. More different taxa of conspicuous surface fauna in all trophic levels were ob “Mobile Prim” - mobile primary consumers (e.g., mayflies, mobile caddisflies, snails, tadpoles, sphenid beetle larvae); “Sessile Prim” attached or retreat-dwelling primary served in the unregulated rivers (Fig. All the trends suggested here require - 13). consumers (e.g., sessile caddisflies and tube- or tuft-dwelling chironomids); “Preds and more observations with more rigorous sampling methods before they can be Omnivs” are taxa that eat live animal tissue (e.g., roach (minnows), steelhead parr, confirmed. mites, stoneflies, naucorids (hemipterans), crayfish, flatworms). Lines are drawn between October and August observations in the East Fork Russian because during a Discussion January census of algae when fauna not recorded, the presence of large numbers of hydropsychids was noted qualitatively. In the four unregulated channels, winter flows The seasonal cycle of growth, detachment, and senescence of Ckzdophoru precluded wading transects, but from the bank, the absence of fauna and algae on in unregulated rivers of northern California resembles its cycle in the Lau- scoured bed material could be detected. rentian Great Lakes (BLUM,1982) where in recent decades, massive Cludophoru blooms have occurred (AUER,1982; MILLNER& SWZENEY, 1982; NEIL& JACK- (MILLNFX& SWEENEY,1982; POWER,unpublished data). In winter, Cludophoru is SON, 1982). In both northern California rivers and the Great Lakes, Cladophoru eliminated from shoreline habitats in the Great Lakes by ice scour and from initiates growth in the late spring, covering large portions of the bed where river beds by scouring floods. In Lake Michigan, perennating basal rhizoidal suitable stable substrates occur (AUER,1982; DUFFet al., 1984; POWER,1990 b). holdfasts on deeper substrates overwinter and vegetatively produce the first re- Cladophoru in both the lakes and in unregulated rivers attains its maximum growth in the spring (BLWM,1982). A similar pattern has been described for biomass in mid-summer, then detaches to form floating mats. Senescence in Cladophoru in the Baltic Sea by WAERN(1952, cited in BLUM(1982)), who dis- late summer or fall is sometimes followed by a limited resurgence of growth tinguished populations of “perennial Cladopbora” in deep habitats from 400 Mary E. Power Hydrologic and trophic controls of seasonal algal blooms 401

South Fork Eel River Elder Creek Middle Fork Eel River Outlet Creek

"" Mobile Primary Consumers { ' Mobile Primary Consumers 0.8 0.0- 08 0- 0- 0.0- 8nU 08 8 0 1, 0.4

00 M O 8 2

.n I ." Sessile Primary Consumers ""PSggSile primary Consumers Sessile Primly Consumers 0.8-

0.6 - 0.6 o'81 n 0.4- 0.4

0.2j 02

0.0 O

1 .O I." .." Predators and Omnivores Predators and Omnivores Predatocs and Omnivores Predators and Omnivores I 0.8' 0.0- GI wauln. mwm?a H mW 0 a- 0.6- 0 0.8 0.8- N- o'81 8 mb 8 M.d 0.4 0.4- 0.4 - 0.4 I3 -dl 1 0.2 0.2- 0.2 1

0.0 0.0 O s 1M D 2 i? $ Fig. 13/1 Fig. 1312 summer "hydrolittoral Cfudopboru" at the waterline. Shoreline Cludopboru ap 1987). From March through August of 1989, Cfudophoru in the South Fork Eel pears to recruit from spores released by the deeper summer populations, and did not develop on unglazed tiles placed above the bed where they were inac- does not overwinter. Spring regrowth of Cludopboru in California rivers also cessible to most grazers, despite luxuriant growth of the alga on bedrock im- appears to be from vegetative regrowth by basal holdfasts that overwinter on mediately beneath tiles. This observation also suggests limited recruitment boulder or bedrock substrates. Attached Cladopboru first occurs in late spring from zoospores during that year. only on large boulder and bedrock substrates (Fig. 11), which experience less The annual bloom-detachment-decomposition cycle of Cludophoru in the scour and overturn during bed movement (SOLISA, 1979; POWER& STEWART, Great Lakes and in unregulated California rivers contrasts with the constant

26 dchiv f. Hydrobiologie, Bd. 125 402 Mary E. Power Hydrologic and trophic controls of seasonal algal blooms 403

East Fork Russian River (Regulated) Dry Creek (Regulated) Most physicc-chemical factors were probably more favorable for Cfa- dophoru growth in the regulated rivers. Their more constant hydrographs 1 .o two Mobile Primary Consumers would reduce mortality from scour in winter and from stranding and desiccation in summer. Temperature was more constant in these channels (between 9- 18 "C (data from the USGS and POWER,unpublished data)). This tempera- 0.6 ture interval is close to that yielding maximum production of Lake Michigan Cludophoru: 10-23 OC; above temperatures of 23 "C, standing crops declined (GRAHAMet al., 1982). During summer low flow, shallow stagnant areas of the unregulated rivers in this study could warm to 28-30 "C on a daily basis. The sustained flow in regulated channels during summer (Figs. 3, 6) would also maintain higher fluxes of nutrients known to favor growth of filamentous green algae (WHITFORD& SCHUMAKER,1964); in addition, measured nitrate concentrations were higher in the regulated than in the unregulated rivers (Fig. 8). Sessile Prhry Consumers In North America, phosphorus is more often limiting in eastern and mid- western regions (SCHMLER, 1978), while nitrogen limitation often occurs in imuiium hyhop.* n 0.6 western regions (GOLDMAN,1981). In northern California, N: P ratios are low (typically around 2 (Fig. 8)), and nitrogen can limit algal growth (HILL& KNIGHT,1988; POWER,1991). Despite apparently more favorable physico-chemical conditions, Clu- dophoru blooms were not observed in regulated channels as they were in the rivers with natural hydrographs. Instead, low but viable standing crops of Clu- dophoru were maintained throughout the year. These observations suggest that interaction of the hydrograph with biotic factors: consumers, self-limitation, 1.o and/or epiphytes, may determine whether or not Cludophoru cycles in rivers. Predators and Omnivores Predators and Omnivores o.8/ A working hypothesis 0.6 0.6' 0- Although grazing has been considered unimportant as a potential control 0.4 m .- 0.4- 0 IMCh on Cladophoru in the Great Lakes (AUER& CANALE,1982), grazing by ver-

0.2- tebrates and invertebrates can limit Cludophoru accrual in California rivers "'1 and streams (LAMBERTI& RESH, 1983; FFMINELLAet al., 1989; POWER,1990 b). 0.01 - 1 x '" Spring blooms of Ckzdophora in unregulated rivers may occur because the alga d Fig. 13/3 3 s recovers from winter scour before the densities of grazers build up. Severe winter floods reduce stream invertebrates, many of which overwinter as larvae (FEMINELJA& 1990; et al., 1989). Following winter flooding, Fig. 13. Frequencies of occurrence of taxa (numbers of sightings per number of sites RESH, RESH Cla- monitored) in the three consumer guilds in the six monitored rivers. dophoru enjoys a window of time in late spring and early summer with favorable growth conditions in a community with only one functionally significant (sensu FRETWELL,1977) trophic level: producers unchecked by her- bivory (Fig. 14). Subsequently, as river levels drop and consumer densities low standing crops of the alga maintained in the two rivers with artificially re- build up, Cludophoru biomass will be grazed down where rivers have two or gulated flow. The contrast suggests that Cladophoru cycles in rivers may be ex- four functional trophic levels (unrestrained grazers, or where predators of pre- trinsically driven by factors related to the hydrograph. dators release grazers (POWER,1990 b)). The alga will persist longer where it is 404 Mary E. Power Hydrologic and trophic controls of seasonal algal blooms 405

et al., manuscript) can groom Cfudophoru, removing epiphytes from host filaments. In the regulated rivers, where constant, low, viable standing crops of Cfudophoru persisted throughout the year, densities of primary consumers, particularly sessile taxa, also remained high year round (Fig. 12e, f and M. POWER,personal observations). Potential predators were less frequently observed in regulated than in unregulated rivers during the low flow season (Fig. 12). One explanation for this observation is that some predatory taxa such as stoneflies or salmonids may require natural hydrologic fluctuation and/or natural seasonal thermal regimes to complete their life cycles (WARD& STANFORD, 1979). However, salmonids and stoneflies were observed in the regulated channels surveyed here, (Dry Creek was the release stream for a salmon hatchery), suggesting that physical factors did not exclude these predators. Another hypothesis to explain low JFMAMJJASOND predator abundances in the regulated channels is that under prolonged stable scouring spring grazing, scouring flow regimes, primary consumers with effective defenses against predators, floods bloom senescence floods such as sessile taxa protected by cases or retreats, come to dominate (Fig. 15), Fig. 14. Predicted patterns of seasonal fluctuation in algal biomass produced by interac- and provide an inadequate food base for predators. Thus, sessile primary con- tions of hydrologic and trophic regimes in regulated and unregulated river channels. sumers with attached cases or retreats (shown for one of the common Eel River taxa to enhance resistance to predators (POWERet al., 1992, see also Jo- HANSSON,1991 and references therein) were usually more abundant than ungrazed (one trophic level), or where third-level predators hold grazers in mobile primary consumers in both regulated channels (Figs. 12, 13)). In the check (Fig. 14, POWER,1990 b). most frequently surveyed unregulated channel, the South Fork Eel, mobile If large growths of Cladophoru accrue, they will eventually slough and se- primary consumers initially dominated following winter floods, but were nesce, whether grazed or not. Cldophoru cells near basal portions of filaments eventually outnumbered by sessile primary consumers as predators built up under massive growths are in dark, stagnant environments, and are likely to (Fig. 12 a). A similar but weaker, and seasonally delayed, trend occurred in the weaken, detaching the colony (STEVENSON& STOERMER, 1982 a). In addition, more shaded, less productive Elder Creek (Fig. 12 b). Less algae accrued in Cludophoru, especially when near or at the water surface, accrues heavy loads Elder Creek than in other unregulated channels (Fig. 9), probably because it of epiphytic diatoms (the rough surfaces of its cell walls make good settling was the most shaded of all the monitored channels. In addition, of the four un- substrates (LOWEet al., 1982)). Heavy epiphyte overgrowth in late summer has regulated channels, Elder Creek had the smallest peak flood relative to its been attributed to the leakage of nutrients by senescing Cludophoru (FITZGE- bankfull discharge (Fig. 5), so Overwintering grazers might have suffered less RALD, 1969). Epiphytes may also induce senescence, however, as they can shade from scour. Mobile, but not sessile grazers were relatively high during the first host filaments, block nutrient uptake, or damage cell walls (STEVENSON& sample date in Elder Creek (Fig. 12 b). Further study is needed to determine STOERMER,1982 a, b). In unregulated rivers, these interactions among macro- the relative importance and possible interplay of productivity and disturbance algae and epiphytes occur under increasingly unfavorable flow, nutrient, and thermal regimes as flows decline over the summer. A combination of physico- regimes in limiting algal accrual in these channels. chemical and biotic stresses may account for the senescence and decomposition An implicit assumption underlying the hypothesis presented above is that of Cladophoru before the onset of winter floods. Higher trophic levels may ac- stream invertebrates that are more resistant (or faster to recover from) scouring floods are less resistant to predators. channels with frequent, large dis- celerate or retard the detachment and senescence of algae following blooms In (Fig. 14), but they probably cannot prevent it. charge fluctuations, disturbance-resistant taxa with traits like high mobility, short life histories, and high intrinsic rates of increase should dominate (GRAY If chronically grazed, however, Cfudophoru may never build up sufficient & FISHER,1981). In channels with prolonged stable flow, taxa protected from biomass to become self-limited. Low standing crops, well beneath the water predators by traits like heavy cases, retreats, or sessile or sedentary habits surface, will also be slower to accrue epiphytes. In addition, algivores such as which make potential prey inconspicuous and keep them in or near refuges, midges (POWER,1991), mayflies (DUDLEY,in press), and tadpoles (KUPFERBERG 406 Mary E. Power Hydrologic and trophic controls of seasonal algal blooms 407

spring and early summer before densities of animals build up. Initially, Sessile midges, primary consumer guilds should be dominated by mobile, fast-growing species pyralids, caddis like mayflies. Such taxa will be replaced by predator-resistant consumers as E 0 predator densities build up following disturbance. The hypothesis predicts that cm Retreat-dwelling D caddis, midges heavy winter rains associated with El Nino events will trigger particularly pro- 2 a nounced algal bloom-sloughing-senescence cycles in unregulated rivers. In the g Heavy-cased absence of winter flooding, predator-resistant primary consumers will come to W mobile caddis 0 L dominate, producing food webs with two functional trophic levels: herbivores cm .-VI Thin-cased snails unrestrained by predators. Under this trophic regime, Cladophora should not VI and mobile caddis a: attain sufficient biomass to undergo the bloom-detachment-senescence cycle. Mobile non-armored Tests of this working hypothesis will require long-term monitoring, closer taxa (e.g. mayflies) study of the performance of invertebrates with various traits exposed to discharge fluctuations and predation, and more rigorous faunal surveys of differ- Resistance to Scour or Dessication 3 ent types of channels. The visual scanning and coarse taxonomic resolution I used in field surveys yield only a superficial impression of faunal distributions. Fig. 15. Diagram of a working hypothesis concerning adaptations that may represent tradeoffs for aquatic invertebrates between resistance to discharge fluctuation and re- These methods were applied consistently among the six rivers studied, how- sistance to predation. Sessile and sedentary habits are hypothesized to decrease the abil- ever, and provide a preliminary basis for comparison. These observations ity of individuals to avoid areas of scour or desiccation. In addition, these traits, as well motivate more careful study, because comparisons of communities and com- as allocation to armor, would slow food acquisition by individuals, reducing the growth munity assembly in rivers that differ in size, productivity, and discharge-me- rates of their populations that would permit recovery from floods or desiccation. Mobile, non-armored taxa should permit individual mobility and high population diated disturbance regime may provide insights about key processes that struc- growth and recovery rates, at the expense of vulnerability to fish and other predators. In ture river communities. The cyclical accrual of large standing crops of the surveyed northern California rivers surveyed in this study, Petrophila (Paragyrac- macroalgae is not only one possible outcome of these processes, it is also a re- tidae: Lepidoptera) and hydropsychid caddis larvae (Trichoptera) would be representa- gulator of interactions among higher trophic levels, and of exchange between tive sessile retreat dwellers; Dicosmoecw gzfvipes (Limnephilidae: Trichoptera) would re- rivers and their watersheds (FISHERet al., 1982; POWER,1990 a). present heavycased species; Physel(a (Gastropoda) would represent thin-cased species; and a variety of mayfly species (Ephemeroptera) would represent mobile, non-armored taxa. Acknowledgement

I would like to thank BILLRNNEY and HABTEKIFLE for help with field work, HEATH should dominate. (The tendency for beds of rivers experiencing low stable dis- CARNEYand RHEA WILLIAMSONfor help with chemical analyses, KENNETHMARKHAM and JOHN PALXIERof the USGS for providing hydrologic records, BILLDIETRICH for help charge to become choked with fine sediments should enhance the advantages with flood frequency analyses, MICHAELPARKER for valuable discussion and comments of sessile or cased invertebrates over mobile invertebrates, whose spatial ref- on the manuscript, and the California State Water Resources Center (W-726) and the uges from predators dwindle as pore spaces in the bed fill up.) Because many National Science Foundation (Ru-8600411, BSR-9106881) for financial support. traits conferring predator-resistance are likely to reduce both mobility and allocation to growth and reproduction which allow taxa to escape or recover References from disturbance, resistance to one of these major sources of mortality for stream invertebrates should often increase vulnerability to the other (Fig. 15). American Public Health Association, Amerian Waterworks Association and Water To the extent that these tradeoffs involve energy allocations, transitions from Pollution Control Federation (1980): Standard Methods for the Examination of Water and Wastewater. APHA, Washington, D.C. dominance by disturbance-resistant to predator-resistant primary consumers - AUER,M. T. (1982): Preface, Ecology of Filamentous Algae. - J. Great Lakes Res. 8: should occur earlier in channels with higher primary productivity. 1-2. In summary, hydrologic and trophic controls of Cludophoru in northern AUER,M. T. & CANALE,R. P. (1982): Ecological studies and mathematical modeling of California rivers are hypothesized to interact. Winter floods that reduce pop- Cladophora in Lake Huron: III. The dependence of growth rates on internal phos- ulations of invertebrates permit river algae to accrue large standing crops in phorus pool size. - J. Great Lakes Res. 8: 93-99. 408 Mary E. Power Hydrologic and trophic controls of seasonal algal blooms 409

BELLIS,V. J. & MCLARTY,D. A. (1967): Ecology of Cfudophorugfomeruta (L.) KUTZ.in LIGON,F. K. (1986): The response of algal communities in streams to timber harvest ac- southern Ontario. - J. Phycol. 3: 57-63. tivities. - M.S. thesis, Univ. Cali., Berkeley. BLUM,J. L. (1956): The ecology of river algae. - Bot. Rev. 22: 291-341. Lomz, R. C. & HERDENDOW,C. E. (1982): Growth dynamics of Cfudopboruglomerura - (1982) Colonization and growth of attached algae at the Lake Michigan water in Western Lake Erie in relation to some environmental factors. - J. Great Lakes line. - J. Great Lakes Res. 8: 10- 15. Res. 8: 42-53. DUDLEY,T. L. (1992): Beneficial effects of herbivores on stream macroalgae via epiphyte LOWE,R. L., ROSEN,B. H. & KINGSTON,J. C. (1982): A comparison of epiphytes on removal. - Oikos (in press). Bungia urropurpurea (Rhodophyta) and Ckzdophoru gfomeruru (Chlorophyta) from Northern Lake Michigan. J. Great Lakes Res. DUFF,J. H., TRISKA,F. J. & Omurn, R. S. (1984): Denitrification associated with - 8: 164- 168. stream periphyton: chamber estimates from undisrupted communities. - J. En- MILLNER,G. C. & SWEENEY,R. A. (1982): Lake Erie Ckzdophoru in perspective. - J. viron. Qual. 13: 514-518. Great Lakes Res. 8: 27-29. MILLNER,G. C., SWEENEY,R. A. & FREDERICK,V. R. Biomass and distribution of DUNNE,T. & LEOPOLD,L. B. (1978): Water in Environmental Planning. - Freeman and (1982): Company, San Francisco, CA. Cladophoru glomerura in relation to some physical-chemical variables at two sites in Lake Erie. - J. Great Lakes Res. 8: 35-41. FEMMELLA,J. W. & RESH,V. H. (1990): Hydrologic influences, disturbance, and intra- NEIL, H. &JACKSON,M. B. Monitoring Cladophoru growth conditions and the specific competition in a stream caddisfly population. - Ecology 71: 2083 -2094. J. (1982): effect of phosphorus additions at a shoreline site in Northeastern Lake Erie. - J. FEMINELLA,J. W., Poum, M. E. & %H, V. H. Periphyton responses to inver- (1989): Great Lakes Res. tebrate grazing and riparian canopy in three northern California coastal streams. 8: 30-34. PARKER,G. (1978): Self-formed straight rivers with equilibrium banks and mobile bed. - Freshw. Biol. 22: 445-457. Part 2. The gravel river. - J. Fluid Mechanics 89: 127- 146. FISHER,S. G., GRAY,L. J., GRIMM,N. B. & BUSCH,D. E. (1982): Temporal succession in POWER,M. E. (1990a): Benthic turfs vs. floating mats of algae in river food webs. - a desen stream ecosystem following flash flooding. - Ecol. Monogr. 52: 93- 110. Oikos 58: 67-79. FITZGERALD,G. P. Some factors in the competition or antagonism among bac- (1969): - (1990b): Effects of fish in river food webs. - Science 250: 411-415. teria, algae, and aquatic weeds. - J. Phycol. 5: 351-359. - (1990 c): Seasonal and hydrologic controls of algal blooms in northern California FRETWELL, D. The regulation of plant communities by food chains exploiting S. (1977): rivers. - Tech. Compl. Rep., Water Res. Ctr., Univ. Calif., Riverside, Riverside, them. - Persp. Biol. Med. 20: 169-185. CA. GOLDMAN,C. R. (1981):Lake Tahoe: two decades of change in a nitrogen deficient oligo- - (1991): Shifts in the effects of tuft-weaving midges on filamentous algae. - Am. trophic lake. - Verh. Internat. Verein. Limnol. 21: 45-70. Midl. Nat. 125: 275-285. GOLDMAN,C. R. & HORNE, J. (1983): Limnology. - McGraw-Hill, New York, N.Y. A. Po-, M. E., hms,J. C. & PARICER,M. S. (1992): Variation in the vulnerability of GRAHAM,J. M., Am,M. T., CANALE,R. P. & HOFFMAN,J. P. (1982): Ecological studies prey to predators: community-level consequences. - Ecology (in press). and mathematical modeling of Cladophoru in Lake Huron. Photosynthesis and IV. POWER,M. E., hmws,W. J. & STEWART,A. J. (1985): Grazing minnows, piscivorous respiration functions of light and temperature. - J. Great Lakes Res. 8 as bass and stream algae: dynamics of a strong interaction. - Ecology 66: 100- 11 1. 1448 - 1456. GRAY,J, J. & FISHER,S. G. (1981): Postflood recolonization pathways of macroinver- Pomn, M. E. & STEWART,A. J. (1987): Disturbance and recovery of an algal assemblage tebrates in a lowland Sonoran Desert stream. - Am. Midl. Nat. 94: 421 -424. following flooding in an Oklahoma stream. - Am. Midl. Nat. 117: 333-345. GRIMM,N. B. (1987): Nitrogen dynamics during succession in a desen stream. - Ecol- RESH, V. H., JACKSON,J. K. & MCELRAVY,E. P. (1989): Disturbance, annual variability, ogy 68: 1157-1170. and lotic benthos: examples from a California stream influenced by a Mediter- HILL,W. R. & KNIGHT,A. W. (1988): Nutrient and light limitation of algae in two ranean climate. - Mem. 1st. Idrobiol. 47: 297-317. northern California streams. - J. Phycol. 24: 125- 132. SCHINDLER,D. W. (1978): Factors regulating phytoplankton production and standing HYNES,H. B. N. (1970): The Ecology of Running Waters. - Univ. of Toronto Press, crop in the world’s freshwaters. - Limnol. Oceanogr. 23: 478-486. Toronto. SOLORZANO,L. (1969): Determination of ammonia in natural waters by the phenol- JOHANSSON,A. (1991): Caddis larvae cases (Trichoptera, Limnephilidae)as antipredatory hypochlorite method. - Limnol. Oceanogr. 14: 799-801. devices against brown trout and sculpin. - Hydrobiologia 211: 185- 194. SOIJSA,W. P. (1979): Disturbance in marine intertidal boulder fields: the nonequilibrium KAMPHAKE,L. S., HANNAH,S. A. & COHEN,J. M. (1967): An automated analysis for ni- maintenance of species diversity. - Ecology 60 1225- 1239. trate by hydrazine reduction. - Wat. Res. l: 205-216. STEVENSON,R. J. & STOERMER,E. F. (1982a): Abundance patterns of diatoms on Cla- KUPFERBERG,S. J., Msas, J. C. & Po=, M. E.: Variation in natural algal and detrital dophoru in Lake Huron with respect to a point source of wastewater treatment diets: Effects on larval anuran life history. Manuscript. plant effluent. - J. Great Lakes Res. 8: 184- 195. LAMBERTI,G. A. & RESH,V. H. (1983):Stream periphyton and insect herbivores: An ex- - - (1982b): Seasonal abundance patterns of diatoms on Cfudopboru in Lake perimental study of grazing by a caddisfly population. - Ecology 64: 1124- 1135. Huron. - J. Great Lakes Res. 8: 169- 183. LmBEnn, G. A. & MOORE,J. W.(1984): Aquatic insects as primary consumers. - In: TRUSH,W. J. (1991): The influence of channel morphology and hydrology on spawning RESH,V. H. & ROSENBERG,D. M. The Ecology of Aquatic Insects, pp. 164- 194. populations of steelhead trout in South Fork Eel tributaries. - Ph. D. disserta- - Plenum, New York, N.Y. tion, Univ. Calif., Berkeley. 410 Mary E. Power, Seasonal algal blooms

WARD,J. V. &STANFORD,J. W. (1979): Ecological factors controlling stream zoobenthos with emphasis on thermal modification of regulated streams. - In: WARD,1. V. & STANFORD,J. W.: The Ecology of Regulated &earns, pp. 35-55. - Plenum, New York, N.Y. WHARFE,J. R., TAYLOR,K. S. & MONTGOMERY,H. A. C. (1984): The growth of Clu- dophom glomeruzu in a river receiving sewage effluent. - War. Res. 18: 971 -979. WHITFORD,L. A. & SCHUMACHER, G. J. (1961): Effect of current on mineral uptake and respiration by a freshwater alga. - Limnol. Oceanogr. 6: 423 -425. WHITTON,B. A. (1970): Biology of Cladopboru in freshwaters. - Water Res. 4: 457 -476.

Submitted: 29 August 1991; accepted: 21 April 1992.