Hydmbiologia 511: 215-231,2004. 215 © 2004 Kluwer Academic Publishers. Printed in the Netherlands. Pathways of increased water clarity after fish removal from Ventura Marsh; a shallow, eutrophic wetland Laura J. Schrage1-2 & John A. Downing1'* 1 Ecology, Evolution, and Organismal Biology, Iowa State University, 353 Bessey Hall, Ames, IA 50011-1020, U.S.A. E-mail: downing@iastate.edu 1Present address: Environmental and Public Health Program, University of Wisconsin - Eau Claire, Eait Claire, WI54702, U.S.A. (*A uthorfor correspondence) Received 27 August 2001; in revised form 13 October 2003; accepted 30 October 2003 Key words: biomanipulation, carp, eutrophication, fish, macrophytes, phosphorus, water clarity, wetland Abstract We investigated the pathways by which water clarity increases following fish removal by evaluating the effects of a benthivorous fish reduction in a large, shallow, eutrophic, wetland in a predominately agricultural watershed in Iowa, U.S.A. Phytoplankton was phosphorus limited prior to manipulation. After a substantial fish removal was obtained, water clarity increased as a result of decreased suspended sediment and phytoplankton biomass. Trophic cascading, mitigated by release from fish predation and decreased physical interference from suspended sediments, appears to determine water clarity. Inorganic suspended solids declined immediately after fish were removed but the biomass of Daphnia and Ceriodaphnia did not increase until a few weeks after fish removal. High grazing by zooplankton likely reduced phytoplankton biomass during the height of the clear-water phase. Phytoplankton appeared to be limited by zooplankton grazing for approximately two months before reverting to bottom-up control. An increase in suspended sediment and/or increased predation pressure on zooplankton, due to the return of juvenile carp, appears to account for the decline of larger-bodied zooplankters and the switch back to bottom-up control. Macrophyte diversity and density increased substantially after the initiation of the clear-water phase. Introduction terest, especially in lakes receiving excessive nutrients (Lathrop et al., 2002). Biomanipulation is a well known ecological manage Despite much study, there remain discrepancies ment tool aimed at increasing water clarity by ma concerning the mechanisms of water clarity increase nipulating the biomass of fish (Hrbacek et al., 1961; following fish removal. The most commonly cited Perrow et al., 1997; review by Lathrop et al., 2002). mechanism is trophic cascading whereby decreased Biomanipulations have been conducted throughout fish abundance allows increased zooplankton grazing, Europe and North America during the past 50 years, leading to clear waters and regrowth of aquatic mac many of which have been successful in improving rophytes (Gliwicz, 2002). Implicit in this mechanism water clarity and/or lowering phytoplankton biomass is a shift in zooplankton from small- to large-bodied (Drenner & Hambright, 1999). The success of bio species (e.g., Daphnia) which reduce phytoplankton manipulation has been variable (Mehner et al., 2002), biomass and increase clarity, due to higher grazing ef thus ficiency (Brooks & Dodson, 1965; Shapiro & Wright, studies elaborating the mechanisms through which fish removals alter ecosystem function are of in 1984; Carpenter et al., 1985). However, benthivorous fish (e.g., carp in North America) can structure aquatic 216 systems through many processes and it is uncertain greater depths (Barko & Smart, 1981; Skubinna et al., which processes are prominent in the switch of spe 1995) and sustain significant biomass in the absence cific ecosystems to higher water clarity following fish of foraging benthivores that uproot vegetation (Criv- removal (Mehner et al., 2002). elli, 1983). Reestablishment of macrophytes following Several mechanisms may lead to changes in lentic fish removal can provide positive feedbacks, which ecology after fish removal from shallow ecosystems, help stabilize the clear-water phase. Macrophytes may including direct mechanical effects, direct and indir maintain high water clarity by competing with algae ect effects on the nutrient supply, and alterations to for nutrients and light (Van Donk et al., 1993; Per- food-web structure. For example, water clarity may row et al., 1997), providing refugia for zooplankton increase following benthic fish removal simply due to (Timms & Moss, a reduction in suspended sediment. Benthivores feed creasing sedimentation of suspended particles (James on invertebrates inhabiting the sediment by sucking in & Barko, 1990), and suppressing algal growth (Wium- sediment, catching the invertebrates in their gill rakers Anderson et al., 1982). 1984; Schriver et al., 1995), in and resuspending sediment (Scheffer, 1998). Benthi- The cause of increased water clarity following fish vorous fish can have substantial effects on turbidity removal is commonly attributed to trophic cascading due to sediment bioturbation (Meijer et al., 1990; Breukelaar et al., 1994; Lougheed et al., 1998). (McQueen, 1990) but conclusions may be confoun ded by changes in bioturbation and nutrient cycling Another mechanism that may increase water clar after fish removal (McQueen, 1990; Vanni & Find- ity following fish removal is a reduction in phyto- lay, 1990; McQueen et al., plankton biomass through a decreased supply of phos this study was therefore to examine the multiple im 1992). The purpose of phorus (Boers et al., 1991). Because benthivores can pacts of benthivorous fish removals in the temperate, increase phosphorus concentrations through the recyc eutrophic Ventura Marsh. Ventura Marsh is a large, ling of nutrients from the sediment as well as by direct shallow, windy system located in a predominately ag nutrient excretion (Lamarra, 1975; Brabrand et al., ricultural watershed. Prior to manipulation, the marsh 1990; Vanni & Findlay, 1990; Havens, 1991; Breuk had a large population of carp which are known to elaar et al., 1994), benthivore removal can result in increase phosphorus concentrations (Lamarra, 1975; direct reductions in ambient phosphorus concentra Brabrand et al., 1990; Vanni & Findlay, 1990; Havens, tions (Meijer et al., 1989; Van Donk et al., 1990; 1991; Breukelaar et al., 1994), increase phytoplank Hanson & Butler, 1994; Meijer & Hosper, 1997; cf., ton biomass (Tatrai et al., 1997), increase turbidity Bonneau, 1999; Lougheed, 2000). (Scheffer, 1998), and reduce submerged macrophytes Although shifts from small- to large-bodied zo- (Barko & Smart, 1981; Crivelli, 1983; Roberts et al., oplankters following fish removal can result from 1995; Skubinna et al., 1995). This paper describes reduced preferential predation pressure on large zo- the effectiveness of benthivorous fish removal in in oplankton (Lammens & Hoogenboezem, 1991; Dren- creasing water clarity of Ventura Marsh and examines ner & Hambright, aspects of water chemistry and community structure to 1999), there may be other ex planations. Because grazing by large zooplankton is elucidate the pathway through which biomanipulation hindered by suspended sediments (Hart, 1988; Kirk, functions. 1991), removal of benthivores may reduce turbidity, allowing larger zooplankton to dominate (Lougheed & Chow-Fraser, 1998; Bonneau, 1999). Even in Methods the absence of trophic cascading, decreased suspen ded sediment following removal of benthivores may Ventura Marsh is a shallow (mean depth 0.79 m), 76 ha shift the zooplankton community toward larger-bodied marsh located in Iowa, U.S.A. (Fig. 1). The marsh is zooplankton, fed by surface drainage that forms three concentrated reducing the phytoplankton biomass, leading to increased water clarity. Expansion of macrophyte beds following fish re inflows from the west, southwest, and south, with an outlet through a spillway to Clear Lake on the east moval may further stabilize clear water conditions ern end. The water level in the marsh is regulated by (Meijer et al., 1990; Ozimek et al., 1990; Hanson & the Iowa Department of Natural Resources (IDNR) by Butler, 1994; Meijer & Hosper, 1997). This may occur placing boards to the desired level across the outfall. because the higher water clarity following benthi This structure was installed approximately 50 years vore removal can allow macrophytes to expand to ago to reduce the movement of fish between Clear 217 Clear Lake. Iowa, USA Farm land Urban & residential Grass & pasture ■=> Wetland 133 Forest Figure 1. Map of Clear Lake watershed showing land use and the location of Ventura Marsh and the reference system. Land-use was determined using records from the United States Natural Resources Conservation Service, aerial photography and field surveys. Straight, dark lines are roads and the outside boundary on the map indicates the limit of the watershed determined by GIS from digital elevation maps. Lake and Ventura Marsh, but the fish barrier system has fallen into disrepair. Prior to treatment, the fish fauna of Ventura Marsh was primarily black bullhead Table I. Ecosystem and water quality conditions for Ventura Marsh and reference system (Little Clear Lake). Values are averages of data collected during the pre-manipulation period (12 April 1999-16 August 1999) (Ictalurus melas) and common carp (Cyprinus carVentura Marsh pio), which have colonized the marsh since the failure The western bay of Clear Lake (Little Clear Lake), to which Ventura Marsh is a tributary, was monitored Mean depth (m) Area (ha) as a reference site for this study (Fig. 1). The Little Secchi transparency (in) Lake is a suitable reference site because it is sim Total phosphorus (|tg 1~' as P) Total nitrogen (mg 1~' as N) Silica (mgl"1 asSiO2) NH++NH3(ngr' asN) Total suspended solids (mg I"') ilar to Ventura Marsh in nutrient regime, size, and depth (Table 1), and is exposed to the same seasonal variability. The IDNR conducted the fish removals via applic Reference system of the fish barrier. 0.79 76 0.26 391 5.45 1.13 127 0.32 228 4.70 81 62 1485 1262 86 68 ation of rotenone. To gauge the success of the rotenone treatments, gill net surveys were performed in con junction with the IDNR. Three gill nets, measuring 48.8 m long with 6.4 cm bar mesh, were placed for 24 hours in Ventura Marsh on four occasions (3 Au gust 1999, 10 September 1999, 12 April 2000 and and the lengths of the first 50 fish of each species were measured. We began studying Ventura Marsh in the spring of 21 June 2000). The fish captured were identified and 1999 and the fish removal was planned to occur at counted. During the last three gill net surveys, carp the end of the summer of 1999. The IDNR applied were counted by size category (< 1.8 kg or > 1.8 kg). rotenone aerially to Ventura Marsh on 17 August 1999 There was reason to believe that the carp population at the rate of 4 ppm (Fish Kill 1 = FK1). Gill net was becoming re-established in late summer of 2000, surveys following FK1 indicated a carp reduction of so electroshocking was conducted on 1 September 2000. Two transects were shocked for 7 min each. The fish captured during electroshocking were identified less than 50%. Perrow et al. (1997) suggests a con servative target of 75% fish reduction, so a second attempt to reduce the fish population was conducted in 218 7 be 2 11 be 10 abc 12 c 1 abc 13 be 9 B c _2 Kilometers Figure 2. Map ot Ventura Marsh showing the water quality, plankton, and benthic sampling sites. Points where plankton, benthic samples, and water samples are indicated by lower case letters. the winter of 1999/2000. The water level of the marsh We assessed water quality variables at three sites was lowered to 51.8 cm below crest and rotenone was in Ventura Marsh (Fig. 2) and at the deepest point in applied under the ice on 13 February 2000 to induce the Little Lake. Dissolved oxygen, temperature, pH, a winterkill (FK2). Following the second rotenone ap and conductivity were measured at each half-meter in plication, approximately 50% of the carp population terval in the water column. We also collected water had been eradicated. A third attempt to reduce the fish samples for analysis of total nitrogen, nitrate, ammo population occurred in the spring of 2000 (FK3). The nia, total phosphorus, silica, and total, inorganic, and water among the cattails surrounding the marsh may volatile (by combustion at 550 °C for 1 hour) suspen have provided a refuge for fish during FK1. To re ded solids at these depths. Total nitrogen and nitrate duce this possibility, the water level of the marsh was were analyzed using the second derivative method lowered to 61 cm below crest in June 2000, reducing (Crumpton et al., 1992). The remaining analyses were the amount of water in the cattail beds. Rotenone was conducted according to standard methods (American aerially applied at the rate of 8 ppm on 7 June 2000. Public Health Association, 1998). Secchi disk read A gill net survey indicated that the fish population ings were also taken at these three sites. had been reduced by at least 75% following the third rotenone application. We could not reliably estimate Plankton and benthos samples were collected in excess to make sure that sufficient sampling preci the size distribution of fish after FK3 since we were sion was obtained. In August of 1999 we expanded only able to catch a few fish in nets after these three our sampling of plankton and benthos from three rotenone treatments. replicate samples to 13 replicate plankton samples To determine the mechanism(s) by which benthi- and seven replicate benthic samples (Fig. 2). Fewer vorous fish removal influenced Ventura Marsh, we benthic samples were taken because we felt that the studied water quality, plankton, benthos, and macro- distribution of benthos was more homogeneous than phytes before and after this series of fish kills (i.e., that of the plankton community. We counted a num FK1-FK3). Water quality, plankton, and benthic com ber of randomly chosen samples from each date that munities were sampled every 2 weeks from April was sufficient to yield an inter-replicate standard er through October of 1999 and every 2 weeks from ror of <20% of the mean (Downing, 1979). After March through September of 2000, with a higher fre counting many of the 1999 plankton samples, it was quency of sampling employed following summer fish noticed that four phytoplankton and three zooplankton removals. Water quality and phytoplankton samples samples were sufficient for most dates. We therefore were collected from the reference system (Little Clear reduced the number of samples collected in 2000 to Lake) every two weeks on the same days as we six phytoplankton and five zooplankton samples. We sampled Ventura Marsh. 219 continued to collect seven replicate benthic samples were identified to genus and Copepoda to subor on each date in 2000. der using the keys of Pennak (1989). We estimated The phytoplankton samples were comprised of zooplankton dry biomass by applying length-weight equal volumes of water taken from each half-meter equations (Dumont et al., 1975; Rosen, 1981) with interval and were preserved with Lugol's solution the exception of Keratella spp. The biomasses of Ker- (American Public Health Association, 1998). Samples atella spp. were estimated from biovolume (Ruttner- were concentrated and sub-sampled with a Hensen- Kolisko, 1977) assuming a specific gravity of 1.0 and Stempel pipette. a wet to dry weight ratio of 0.05 (Schindler & Noven, The volume of each sub-sample varied between 2-5 ml depending on cell density. Us ing an inverted microscope, we identified, counted, 1971). The grazing rate potential of cladocerans and ro and measured phytoplankton. Samples were counted tifers were approximated using abundance data and until the most abundant species reached 125 except estimated clearance rates from the literature (Haney, when Oscillatoria was most abundant. OsciUatoria 1973; was often present in very high densities, so when Lacroix, 1990; Grosselain et al., 1996). The analyses Bogdan & Gilbert, 1982; Mourelatos & Oscillatoria was most abundant, samples were coun of Peters & Downing (1984) were not used because ted until Oscillatoria counts reached 1000. Fifty cells those authors note the potential impact of container of each taxon were measured for each sample, ex effects and other laboratory artifacts on predictions cept Oscillatoria, for which 250 cells were measured. from their models. Copepods were not included in the Phytoplankton were identified to genus, with the ex estimation of grazing rates because only harpacticoid ception of small Cyanobacteria, using the keys of and cyclopoid copepods were present in this study, Ward & Whipple (1959) and Whitford & Schumacher neither of which are substantial suspension feeders (1984). Phytoplankton cells were measured and wet (Pennak, 1989). biomass estimated by applying basic geometric formu The sediment of Ventura Marsh is organic mud so lae (Findenegg, 1974). From this information, we cal we were able to obtain benthic samples with an Ekman culated the biomass of edible (<30 |im) and inedible grab and filled a one liter bottle with this sediment. We (>30 \im) phytoplankton (Watson et al., 1992). filtered the sediment samples through a 600-fxm sieve, We used a 30-1 Schindler-Patalas trap with a 61- and the portion remaining in the sieve was preserved in |xm mesh net to collect zooplankton samples from 5% Formalin solution with sucrose and 100 mg I"1 of the onset of the study until 23 May 2000, at which rose bengal (Mason & Yevich, 1967). We counted and time we began sampling using a 61-jJim mesh Wis identified all benthic organisms in the samples using consin net. We switched to a Wisconsin net because the keys of Pennak (1989) and Merritt & Cummins we were unable to submerge the Schindler-Patalas (1996). The first 25 chironomids and 30 oligochaetes trap without disturbing the sediment during periods in each sample were measured. Dry masses of Diptera of low water in 2000. To determine the difference in and Gastropoda were estimated using length-weight efficiency between these two sampling devices, both equations (Eckblad, 1970; Benke et al., 1999). We collection methods were used simultaneously on three estimated oligochaete dry mass based on biovolume sampling dates. In terms of biomass, the Schindler- (Smit et al., 1993). The standing density of benthos Patalas trap was found to be approximately 5% more was estimated on a per unit volume basis to simu efficient than the Wisconsin net. Therefore, zooplank late availability to benthivorous fish. Densities were ton biomass values from Wisconsin net samples were therefore determined by dividing total dry mass by the corrected such that they express the expected biomass, volume of the collection bottle. had the Schindler-Patalas trap been used. Zooplank In order to evaluate the impact offish manipulation ton samples were preserved in 5% Formalin solution on submerged macrophytes, we conducted macro- with sucrose (Haney & Hall, 1973) for a minimum of phyte surveys in July 1999 and August 2000. Twelve two weeks and were later transferred to 70% ethanol. north-south transects were evenly spread throughout Samples were sub-sampled using a Hensen-Stempel the open water and surveyed in 1999. We recorded pipette to obtain a volume with a minimum of 60 or the species present along these transects. In 2000, ganisms (McCauley, 1984). We identified, counted, the open water of the marsh was surveyed for sub and measured zooplankton using a stereomicroscope merged macrophytes with 27 north-south transects with 50 x magnification. Twenty-five individuals of located 50 m apart. A one-meter square quadrat was each taxon were measured. Rotifera and Cladocera placed approximately every 20 m along these tran- 220 0.0B == a> 0.06 0.04 — Q. CO ZJ CO g id 'c 0.02 — CO £> o c — o.oo i July 0.2 i r August September 2000 Figure 3. Inorganic suspended solids and Secchi disk transparency for Ventura Marsh during the clear water phase (7 June 2000-27 September 2000), alter the third fish removal (FK3). sects. We identified the species in the quadrats and 1 September 2000 (a few months after FK3), two tran visually estimated the percent cover of each species. sects in the marsh were electroshocked. A total of 73 Direct comparisons of water quality values fishes (68 common carp, 4 buffalo, and 1 bullhead) between the four time periods (pre-manipulation, post- were captured in transect one. Only seven fishes (6 FKl, post-FK2, and post-FK3) could be confounded common carp and 1 buffalo) were captured in transect by seasonal variability. To reduce this likelihood, the 2. The carp were primarily small fish with an average before-after-control-impact (BACI) method of ana length of 15.7 cm and a range of 11.9-26.7 cm. lysis (Smith et al., 1993) was used to determine whether differences in nutrient concentrations, sus Secchi disk transparency was generally quite low in the marsh (~0.35 m) but was significantly higher pended solids, Secchi disk transparency, and phyto- following FK3 (BACI, p < 0.05). The highest Secchi plankton biomass were statistically significant among disk transparency of 1.0 m was recorded on 13 July the four time periods. Little Clear Lake was used as 2000 (Fig. 3), 6 weeks after FK3. The Secchi disk the reference system in these analyses. transparencies from 10 May 2000 to 19 July 2000 were slightly underestimated since the Secchi disk reached the marsh bottom at one or more of the sites without Results Prior to disappearing from view. The period following FK3 is rotenone applications, gill nets placed overnight in Ventura Marsh collected 170 common carp (Cyprimis carpio) (Table 2). After FK1 and FK2, 113 and 84 common carp were collected respectively. Of the carp captured following FK1, 54% were very large fish (>1.8 kg), while only 11% of the carp cap tured following FK2 were large. Despite lengthy gill net sets, only 2 common carp, both less than 1.8 kg in weight were collected following FK3 in June of 2000, indicating that the majority of the carp population had been eradicated by the three rotenone applications. Thirty-one bullheads (Ictalurus melas) were collected after FK1, but none were captured on the other collec tion dates. The gill net surveys conducted may not be an accurate indicator of the bullhead population since the nets had a large mesh size (6.4 cm bar mesh). On therefore referred to the 'clear-water phase' and all prior periods as the 'turbid phase'. Total phosphorus concentrations were somewhat reduced in the period following FK3 compared to the pre-manipulation and the post-FKl periods (BACI, /; < 0.058). In the pre-manipulation and the post-FKl periods, the total phosphorus of Ventura Marsh was, on average, 147 and 216 |ig I"1, respectively, higher than the total phosphorus concentration of the refer ence system, whereas in the clear-water phase, the average difference was only 32 \ig I"1. By inference, therefore, carp removal resulted in a 115-184 [ig I"1 reduction in total phosphorus concentration in the marsh. In the turbid phase, total phosphorus and phytoplankton biomass were strongly correlated (r2 = 0.73; p < 0.001) but were not strongly correlated 221 200 400 600 BOO Total Phosphorus (/yg M) Figure 4. The relationship between total phosphorus and phyloplankton biomass (A) during the 'turbid' phase (12 April 1999-6 June 2000) and (B) during the 'clear water' phase (7 June 2000-27 September 2000). Phytoplankton biomass and total phosphorus were strongly positively correlated during the turbid phase (r2 = 0.73; p < 0.001), but were not signUicantly correlated in the clear water phase (r2 = 0.23; p > 0.05). during the clear-water phase (r2 = 0.23; p > 0.05) silica showed no significant changes in concentrations (Fig. 4). among the four treatment periods (BACI, p > 0.05). Ammonia concentrations following FK3 were sig Inorganic suspended solids (ISS) concentrations in nificantly different from the pre-manipulation and the the water column did not differ significantly among the first post-manipulation period (BACI, p 0.05). four treatment periods (BACI, p < 0.05), although the On average, the ammonia concentrations of Ventura lowest concentration of ISS occurred during the clear- < Marsh were 198 and 234 [xg I"1 higher than the ref water phase (Fig. 3). Linear regression of ISS and erence system during the pre-manipulation and the Secchi disk depth in the clear-water and turbid phases post-FKl periods, respectively. Following FK3, am showed an overall negative correlation (r2 = 0.51; monia concentrations in the marsh were, on average, /; < 0.001) (Fig. 5), however. 387 fig I"1 lower than the reference system. By infer ence therefore, carp removal resulted in a >600 |xg 1~' nificantly lower than during the other three treat reduction in ammonia. Total nitrogen, nitrate, and ment periods (BACI, p Volatile suspended solids following FK3 were sig < 0.05). During the pre- manipulation and the post-FKl periods, volatile sus- 222 1.2 — 1.0 — o spare ranj • Turbid Phase o Clear Waler Phase D _ O 0.8 — 0.6 — \- _ Uish i 0.4 — 0.2 — i 1 0.00 0.02 i i i 0.04 . 0.06 0.08 Inorganic Suspended Solids (g M) Figure 5. Relationship between Secchi disk transparency and inorganic suspended solids (/-2 = 0.51; p < 0.001). Solid circles indicate data from the turbid phase (12 April 1999-6 June 2000) and open circles indicate data from the clear water phase (7 June 2000-27 September 2000). Table 2. Fish captured during gill net surveys on Ventura Marsh using three 48.8 m long nets with 6.4 cm bar mesh. Gill nets were placed for 24 hours in Ventura Marsh on four occasions: 3 August 1999, 10 September 1999, 12 April 2000, and 21 June 2000. The fish captured were identified and counted. Common carp (Cyprinus carpio), black bullhead (lctaluras melas), and channel catfish {Ictalums punciatus) were captured. Common carp were categorized as either < 1.8 kg or > 1.8 kg. Asterisk (*) indicates that the captured carp were not categorized. The large mesh size may account for the absence of bullheads on three of the four sampling dates Date Common carp Carp Bullhead Channel catfish size class Pre-manipulation Post-FKl 3 August 1999 10 September 1999 170 * 113 61 (> 1.8 kg) 0 2 31 1 0 0 0 0 52 (< 1.8 kg) Post-FK2 12 April 2000 84 9(> 1.8 kg) 75 (< 1.8 kg) Post-FK3 21 June 2000 2 0(> 1.8 kg) 2 (< 1.8 kg) pended solids of Ventura Marsh were, on average, chi disk transparency showed a strong negative linear 2 and 7 mg I"1 greater than the reference system, relationship with phytoplankton biomass across the respectively. Volatile suspended solids during the post- FK2 period were, on average, 2 mg I"1 less than the turbid and clear phases (r2 = 0.55,0.74; p < 0.001). Phytoplankton biomass steadily increased through reference system, while during the post-FK3 period, out 1999 and a similar trend began in 2000 (Fig. 6). volatile suspended solids were 22 mg I"1 lower than After FK3, however, the phytoplankton biomass de the reference system. Volatile suspended solids in creased from 23 mg I"1 to 2 mg I"1. Total phyto clude both phytoplankton and organic detritus, and plankton biomass and cyanobacteri a biomass appeared were thus reduced by nearly 30 mg I"1. No signific to be slightly higher in 1999 than in 2000. Oscillat- ant difference in phytoplankton biomass was detected oria, Actinastrum, and small cyanobacteria were more among the four periods (BACI, p = 0.05). However, a prominent in 1999, while Closterium, Merismopedia, > 20-fold decrease in phytoplankton biomass occurred and Synedra were predominant in 2000. between 23 May 2000 and 27 June 2000 (Fig. 6). Sec ED D Dinophyceae Chrysophyceae Bacillariophyceae Chlorophyceae i\Cyanobacteria 2000 223 in early June and an increase in biomass of Chydorus pre-manipulation period. There was a peak of Bosmina at which time the biomass of Daphnia, Ceriodaphnia, nus. Brachionus began to decrease in late June 2000, zooplankter to increase following FK3 was Brachio zooplankton biomass composition (Fig. 7). The first Following FK3, there were substantial changes to the rest of the post-FK2 period. nia were present, but remained very low throughout Temporal trends in phytoplankton biomass and percent composition of the phytoplankton community in Ventura Marsh from 13 May 1999-27 September 2000. Arrows indicate dates of rotenone applications. Changes were observed in the zooplankton com munity across the fish manipulations (Fig. 7). The during August that remained high until FKL Biomass zooplankton biomass composition changed during the of cyclopoid copepods and Keratella was constant Approximately one month later, the biomass of Bos cyclopoid copepods, and nauplii began to increase. mina increased. In early August, Daplmia and Ceriod during this period. Zooplankton biomass was low fol toxicity (Beal & Anderson, 1993). There was a small lowing FK1, which may be attributed to the rotenone and September of 2000, the zooplankton community aphnia populations began to decline. By mid-August consisted mainly of Brachionus, Bosmina, cyclopoid peak of the rotifer Brachionus, followed by a steady and nauplii during the post-FKl period. Chydorus biomass of Keratella, Chydorus, cyclopoid copepods, copepods, and nauplii. throughout the post-FK2 period. The zooplankton bio cladocerans was between 0.2-0.3 mm, whereas, in cladoceran taxa (Fig. 8). In 1999, the length of most during this study reflect changes in the prominent Changes in the size distribution of cladocerans was very abundant during this period. The biomass mass in the post-FK2 period was primarily cyclopoid composition of zooplankton remained fairly similar copepods. In the spring, cyclopoid nauplii and Daph- 224 ■ H □ U O O) 1 I ] Si Q Copepod Nauplii Q Cyclopoidea 1lA 2 — D ■ 2 c 2 IS Q. O O Ceriodaphnia Daphnia Bosmina Chydorus Harpacticoida 1 — Brachionus Keratellat N I I I I I I I I I I f Figure 7. Temporal trends in zooplankton biomass and percent composition of the zooplankton community in Ventura Marsh from 12 April 1999-27 September 2000. Arrows indicate dates of rotenone applications. Data are as dry mass. 2000, a larger range of cladoceran lengths was ob Oligochaetes and non-predaceous chironomids served (0.14-2.06 mm). In 1999, Chydorus was the were the primary benthic organisms in Ventura Marsh primary cladoceran while larger cladocerans, such as (Fig. 10). The composition of the benthic community Daphnia and Ceriodaphnia, were more prominent in remained similar throughout the study but the biomass 2000. The distribution of copepod lengths remained changed considerably. In the pre-manipulation and the fairly constant throughout the study with a median post-FK 1 periods, the average biomass of benthos was length of approximately 0.6 mm (Fig. 8). 22 and 32 mg I"1 of sediment respectively, whereas Although the estimated grazing rates of cladocer ans and rotifers peaked a few times before FK3 (i.e., in the post-FK2 and FK3 periods, the average biomass was 95 and 116 mg I"1 of sediment. The length dis September 1999, June 2000), by far the highest peak tribution of oligochaetes remained similar throughout grazing rate potential occurred in July 2000 (Fig. 9), the study while the median length of chironomids in some weeks after the fish removal. The July 2000 creased in the post-FK3 period (Fig. 11). The increase peak in grazing was very high; with nearly 140% of in size of chironomids in 2000 is likely associated the marsh water likely filtered each day. During the with reduced predation from benthivores and not a turbid phase, grazing rate and phytoplankton biomass were positively correlated (r2 = 0.42; p < 0.001). After FK3, however, phytoplankton biomass declined seasonal trend since an increase in abundance of larger chironomids was not observed in 1999. Throughout this study, cattails (Typha) surroun precipitiously as the abundance of grazers with high ded the shoreline of Ventura Marsh and clumps of grazing rates increased (Fig. 9). Lemna were present throughout the open water. In 225 PreManipulation FigureS. Box-whisker plot of cladoceran and copepod lengths during pre-manipulalion (12 April 1999-16 August 1999), post-manipulation 1 (17 August 1999-15 October 1999), post-manipulation 2 (14 March 2000-6 June 2000), and post-manipulation 3 (7 June 2000-27 September 2000) periods. Copepod nauplii were not included in these plots. The box represents the middle 50% of the data and the lines represent the lower and upper quartile. The open star indicates that the mean cladoceran length during post-manipulation 2 was significantly greater than the mean length during the other three periods. The closed star indicates that the mean cladoceran length in post-manipulation 3 was significantly greater than during post-manipulation 1. Mean copepod length during post-manipulation 3 was significantly lower than the pre-manipulation and post-manipulation 2 periods as indicated by the asterisk. 1999, only six of the twelve transects were found Discussion to contain any submerged macrophytes. Three taxa of submerged and floating leafed macrophytes were The 2-year study of Ventura Marsh provided the op observed: sago pondweed {Stuckenia pectinata), coon- portunity to study the effects of a series of benthi- tail {Ceratophyllum), and water lily (Nymphaea sp.). vorous fish removals. FK1 eradicated approximately Potamogeton pectinatus and Ceratophyllum were the a third of the fish population. Following FK2, the fish primary submerged macrophytes with only one occur population had been reduced to about half of the pre- rence of Nymphaea. All submerged macrophytes in manipulation level. A greater than 75% reduction in 1999 were found within 5 m of the shoreline. In the fish abundance was achieved by FK3 in early summer 2000 survey, macrophytes were present along all 27 of 2000. Little change in water clarity or community transects with over 80% of transects having submerged structure could be discerned until fish removal was > macrophytes extending 60 m from shore. Of the 492 75%. By late summer 2000, however, juvenile fish quadrats sampled, over a fourth had 35% or more cov became re-established in Ventura Marsh. erage from submerged macrophytes (Fig. 12). A total Benthivorous fish removal appears associated with of 6 genera of submerged macrophytes were found a reduction in water column phosphorus concentration in 2000 {Stuckenia pectinata, Elodea, Ceratophyllum, that may arise through one or both of two mechanisms. Vallisneria americana, Although phosphorus did not decline to mesotrophic Zannichellia palustris, and Sagittaria) with Potamogeton pectinatus and Elodea levels due to substantial nutrient inputs to this eco being the most prevalent. system, phosphorus concentrations were reduced in 226 weeks following FK3 and then remained low during July and August of 2000, indicating a reduced amount of sediment in the water column possibly due to de creased benthic fish foraging. An increase in benthos biomass during the clear-water phase supports the thesis that fish foraging was low during the clear-water phase. The high water clarity following FK3 may be partially due to lower amounts of suspended sediment as a consequence of reduced fish foraging. Simil arly, Meijer et al. (1990) attributed increased water clarity in Lakes Bleiswijkse Zoom and Noorddiep fol lowing fish removal partially to decreased suspended sediment due to reduced bioturbation by fish. 1 0 I^l 40 ■ I 80 ' The increased water clarity of Ventura Marsh ap I 120 160 Calculated Grazing Rate (%/day) Figure 9. Covariation of grazing rates and phytoplankton biomass following the third fish removal in Ventura Marsh (FK3). The third rotenone application came at the beginning of the time period plotted. Point labels refer to dates samples were taken. peared to also result from reduced phytoplankton bio mass in the water column. Secchi disk transparency showed a strong negative relationship with phyto plankton biomass throughout both the turbid and clear- water phases (r2 = 0.55,0.74; p < 0.001), indicating that water clarity increased as phytoplankton biomass declined. Phytoplankton biomass showed large fluctu ations in 1999 but overall steadily increased through Ventura Marsh during the clear-water phase follow out the summer (Fig. 6). A similar trend began to ing FK3 compared to the pre-manipulation and the develop in 2000 with a ten-fold increase in phyto post-FKl periods (BACI, p = 0.058). Sediment re- plankton biomass from March to early June. However, suspension was low during portions of the clear-water following FK3 in June, phytoplankton biomass de phase perhaps leading to reduced nutrient recycling creased to low levels, similar to those observed in 2000 and thus lower phosphorus concentrations. Similarly, following ice out, for approximately one month. Havens (1991) observed lower phosphorus concentra Although the evidence is circumstantial, the re tions in experimental ponds where fish were prevented duction in phytoplankton biomass following the third access to the sediment versus ponds in which fish had fish removal appears to be due to zooplankton graz access to the sediment (Havens, 1991). In addition, the ing. Shortly after FK3, estimated zooplankton grazing fish removal may have led to lower total phosphorus rates peaked at 55% of the marsh water per day fol concentrations due to reduced fish excretion. In Lake lowed a month later by another peak of around 140% Gjersj0en, phosphorus released from the roach pop of the marsh water per day (Fig. 9). The first peak ulation has been calculated to be on the same order was due solely to rotifers since cladocerans had not of magnitude as external phosphorus loading from the yet become established. During the second peak in watershed (Brabrand et al., 1990). grazing, zooplankton biomass was not notably higher, A short-term clear-water phase was obtained fol but approximately half of the zooplankton biomass lowing FK3, involving elements of trophic cascading was comprised of Daphnia and Ceriodaphnia, which and changes in physical disturbance. One factor in were rarely observed on other occasions (Fig. 7). Of volved in the immediate increase in water clarity in the cladocerans and rotifers identified in this study, Ventura Marsh was suspended sediment. This is indic Daphnia and Ceriodaphnia were the genera with the ated by the immediate decline in ISS following FK3 highest clearance rates. Phytoplankton biomass re (Fig. 3) as well as by the strong negative correlation mained low during these peaks in grazing, suggesting between ISS and Secchi disk transparency (r2 = 0.51; that the control of phytoplankton was by zooplankton p < 0.001) (Fig. 5). Patterns in ISS and Secchi disk grazing. transparency tend to mirror one another (Fig. 3). Over Fish manipulation in Ventura Marsh switched the all, ISS concentrations were not significantly lower factor limiting phytoplankton biomass from nutrients during the clear-water phase (BACI, p = 0.05), how to zooplankton grazing. The phytoplankton biomass ever, ISS concentrations steadily decreased for three seemed to vary with the phosphorus concentration dur- 227 Hirudinea Ceratopogonidae Chaoboridae Gastropoda Olichochaeta Chrionomidae 1999 2000 F/^'H/f 70. Temporal trends in benthic hiomass and percent composition for Ventura Marsh from 12 April 1999-27 September 2000. Arrows indicate dates of rotenone applications. ing the turbid phase (Fig. 4). Following FK3, however, (Fig. 1; Arbuckle & Downing, 2001). Overall, phyto Daphnia and Ceriodaphnia became abundant and the plankton in Ventura Marsh were correlated with phos phytoplankton was limited by zooplankton grazing phorus concentrations until FK3 appeared to switch (Fig. 9). Zooplankton grazing rates quickly decreased them to top-down control by herbivorous zooplankton. from the high peak of 140% in July 2000 to less Two months later, the system had apparently reverted than 25% per day. After the decline in grazing in late back to bottom-up control. July 2000, phytoplankton biomass began to increase The maintenance of top-down control is essential again. Grazing rates remained low (<35% per day) to a successful fish biomanipulation. It is therefore during August and September while phytoplankton important to discern the factors limiting the abundance continued to grow until limited by nutrient availabil of large-bodied filter feeding cladocerans. Top-down ity. The trends in standing phytoplankton biomass in control occurred following FK3 for approximately two August and September were similar to the trends in months when there was a substantial biomass of Daph total phosphorus, suggesting that the phytoplankton nia and Ceriodaphnia. Although we were not able was once again related to phosphorus concentrations. to collect data on fish diets before manipulation, the Phosphorus limitation of phytoplankton growth is not reduction in fish predation by small carp, and lower uncommon in high nutrient lakes in this region be suspended sediment in the clear-water phase prob cause N:P is often quite high due to large amounts ably accounts for the increase in biomass of these of fertilizer nitrogen in these agricultural watersheds larger-bodied cladocerans. The biomass of Daphnia 228 I Figure Pre- Post- Post- Post- Manipulation FK1 FK2 FK3 11. Box-whisker plot of chironomid and oligochaete lengths during pre-manipulation (12 April 1999-16 August 1999). post-manipulation I (17 August 1999-15 October 1999). post-manipulation 2 (14 March 2000-6 June 2000). and post-manipulation 3 (7 June 2000-27 September 2000). The box represents the middle 50% of the data and the lines represent the lower and upper quartile. The star indicates that mean chironomid length during that period (post-manipulation 3) was significantly greater than the mean chironomid length during pre-manipualtion and post-manipulation 1. 90% coverage 80% coverage 70% coverage 60% coverage 50% coverage 40% coverage 30% coverage 20% coverage 10% coverage 200m 400m 600m 0% coverage Figure 12. Map of Ventura Marsh showing the percent coverage of submerged macrophytes during the summer of 2000. Map was constructed based on data from (he August 2000 macrophyte survey. The inverse distance to a power gridding method was used. 229 and Ceriodaphnia began to decline in late July and macrophytes (Scheffer et al., 1993). The expansion remained low for the remainder of the study. The of submerged macrophytes in Ventura Marsh suggests decline in biomass of larger-bodied cladocerans did that the higher water clarity may persist in subsequent not correspond to changes in dissolved oxygen or years if fish removal could be sustained. Benthivorous temperature. An increase in juvenile carp and suspen fish biomanipulations may alter aquatic ecosystems ded sediment, perhaps due to wind, likely inhibited through multiple pathways involving trophic cascad the dominance of larger-bodied cladocerans in late ing and changes in physical disturbance. summer. Even over the short post-manipulation clear-water phase, the increase in water clarity was sufficient to Acknowledgements promote a dramatic increase in macrophyte diversity and abundance. The higher water clarity and reduced We are grateful to N. Eckles and B. Cordes for their uprooting of vegetation may have allowed macro help in field sampling and lab work. D. Knoll created phytes to become established at greater depths and at maps of Clear Lake and Ventura Marsh. We also grate higher densities. The presence of macrophytes is also fully acknowledge the Iowa Department of Natural helpful to the maintenance of high water clarity be Resources, especially Don Bonneau, Jim Wahl and the cause they help sustain lower suspended sediment and crew at the Clear Lake Fish Hatchery, for their sup lower phytoplankton biomass (James & Barko, 1990; port assistance and use of equipment. We also thank Van Donk et al., 1993; Perrow et al., 1997). two anonymous reviewers who offered constructive criticisms on the first edition of this manuscript. 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