Species-Specific Responses of Aquatic Macrophytes to Fish Exclusion in a Prairie Marsh: a Manipulative Experiment

WETLANDS, Vol. 26, No. 2, June 2006, pp. 430±437 ᭧ 2006, The Society of Wetland Scientists

SPECIES-SPECIFIC RESPONSES OF AQUATIC MACROPHYTES TO FISH EXCLUSION IN A PRAIRIE MARSH: A MANIPULATIVE EXPERIMENT

Vincent D. Evelsizer1 and Andrew M. Turner Department of Biology Clarion University Clarion, Pennsylvania, USA 16214

1Present address: Iowa Department of Natural Resources 109 Trowbridge Hall University of Iowa Iowa City, Iowa, USA 52242

Abstract: An exclosure experiment was carried out at two sites in Delta Marsh, Manitoba, Canada to investigate the role of ®sh in limiting the growth of submersed macrophytes. The experiment consisted of three treatments: (1) ®ne-mesh exclosures designed to exclude both planktivorous ®sh and carp, (2) coarse- mesh exclosures designed to exclude adult carp but admit smaller ®sh, and (3) reference plots marked with corner stakes but without sides. Treatments were established in mid-May, and macrophyte biomass was sampled from within the exclosures in late August to assess treatment effects. Exclosure treatments had strong effects on the macroalgae Chara, with biomass 11.9-fold greater in full-exclosure plots than in reference plots, and 3-fold greater in carp exclosures than in reference plots. Exclosure treatments had no effect on above-ground or below-ground biomass of Stuckenia pectinata, the most widespread and abundant macrophyte in Delta Marsh. Thus, ®sh appear to limit macrophyte growth in Delta Marsh, but the effect of ®sh exclusion was dependent on species composition of the macrophyte assemblage.

Key Words: macrophytes, biomanipulation, turbidity, wetland restoration, Chara, Stuckenia, Delta Marsh, carp

INTRODUCTION tal approaches are necessary to identify the underlying mechanisms. Shallow lakes and marshes tend to exist in one of One potential determinant of macrophyte abundance two alternative conditions: a clear water state charac- in wetlands is the abundance of planktivorous and ben- terized by high water transparency and abundant sub- thivorous ®sh. A number of studies have shown that mersed macrophytes, and a turbid state characterized high densities of zooplanktivorous ®sh are capable of by low water clarity and few submersed macrophytes depressing zooplankton standing crop, which in turn (Timms and Moss 1984, Jeppesen et al. 1990, Scheffer reduces phytoplankton grazing by zooplankton and 1998, Bayley and Prather 2003). Nutrient loading, leads to high phytoplankton standing crops and thus food web structure, herbivory, and wave exposure are low water clarity (Turner and Mittelbach 1992, Car- among the factors that in¯uence lake state. Many shal- penter and Kitchell 1993, Schriver et al. 1995, Jep- low lakes and marshes in North America and Europe pesen et al. 1997). Low water clarity usually limits the have recently experienced increases in turbidity and growth and species diversity of submersed aquatic decreases in the abundance of submersed macrophytes plants (e.g., Chambers and Kalff 1985, Duarte et al. (Chow-Fraser 1998, Scheffer 1998). Often, the decline 1986, Kantrud 1990). Benthivorous ®sh, such as com- of macrophytes is associated with human-induced dis- mon carp (Cyprinus carpio Linneaus) can contribute turbances such as the stabilization of water levels, in- to turbidity by resuspending sediments as they forage vasion of planktivorous and/or benthivorous ®sh, or (Meijer et al. 1990, Breukelaar et al. 1994). Carp may increased nutrient loading (Scheffer et al. 1993, Bouf- also limit the growth of aquatic macrophytes in a direct fard and Hanson 1997). However, because these dis- manner by uprooting plants during feeding or spawn- turbances often disrupt several mechanisms simulta- ing activities (Anderson 1950, Tryon 1954, Atton neously, the speci®c factors most responsible for mac- 1959, Robel 1961, King and Hunt 1967). Thus, a key rophyte decline are usually unknown, and experimen- to the restoration of submersed macrophytes in marsh-

430 Evelsizer & Turner, FISH AND SUBMERSED MACROPHYTES 431 es may be the limitation of planktivorous and benthi- (Goldsborough 1995). Water pH ranges from 8.2 to vorous ®sh (e.g., biomanipulation; Shapiro and Wright 9.0, and total alkalinity averages 338 mg/l CaCO3, 1984, Benndorf 1987, Jeppesen et al. 1990). European largely as bicarbonate (Anderson and Jones 1976). investigators have repeatedly tested these ideas and Delta Marsh historically had greater water clarity have accumulated substantial evidence documenting and supported dense beds of submersed macrophytes the important roles of ®sh in in¯uencing submersed (Hinks and Fryer 1936, Walker 1959, 1965). Large macrophytes in shallow lakes and marshes (e.g., numbers of waterfowl used the marsh as a migratory Scheffer et al. 1993, Jeppesen et al. 1997), but the role stop-over and breeding site (Hochbaum 1944, 1955). of ®sh in North American wetlands has not been as However, the common carp invaded Lake Manitoba widely evaluated (but see Hanson and Butler 1994, and the marsh in 1948 (McCrimmon 1968), and Fair- Zimmer et al. 2001, 2002). ford Dam was built at the lake's outlet in 1961, which Here, we evaluate the effect of ®sh exclusion on stabilized the water level of Delta Marsh. Since that submersed macrophyte biomass in East Delta Marsh, time, water clarity in the marsh has decreased, the Manitoba, Canada. Delta Marsh is one of North Amer- abundance of submersed macrophytes has been re- ica's most prominent wetlands and has been the site duced, and waterfowl use of the marsh has declined of important research in wetland ecology (e.g., Murkin (Batt 2000). Fish, including common carp and fathead et al. 2000) but, like many wetlands, has experienced minnows (Pimephales promelas Ra®nesque), are now increased turbidity, a decrease in the abundance of extraordinarily abundant in the marsh (LaPointe 1986, submersed macrophytes, and a reduction in waterfowl Kiers and Hann 1995, Batt 2000, Evelsizer 2001). We use (deGeus 1987, Batt 2000). We experimentally ex- conducted the exclosure experiment at two sites, Di- cluded benthivorous ®sh and planktivorous ®sh from vision Bay and 22-Bay (Figure 1). These sites were plots within the marsh and monitored the response of chosen based on historical data showing that S. pec- submersed macrophytes. Our goal was to test potential tinata was present at these sites in 1973±74 (Anderson strategies for remediation at small scales to improve and Jones 1976) and 1997 (T. Arnold and D. Wrub- methods for subsequent ecosystem level manipula- leski, personal communication). tions. Exclosure Study METHODS The experiment consisted of three treatments: (1) a Study Sites ®ne-mesh exclosure designed to exclude all ®sh (hereafter, full exclosure), (2) a coarse mesh exclosure de- Delta Marsh, located in south central Manitoba, signed to exclude adult carp but admit smaller ®sh Canada (50Њ11Ј N, 98Њ19Ј W), is a large (ϳ22,000 ha) (hereafter, carp exclosure), and (3) reference plots lacustrine marsh bordering the southern shoreline of marked with corner stakes but without sides. Study Lake Manitoba (Figure 1). Nearby upland areas south plots were 3 ϫ 3 m square and were placed in open of the marsh are intensively farmed. East Delta Marsh, water areas of known macrophyte beds and spaced at the site of our studies, is a shallow (Ͻ 2.5 m depth) least 4 m apart. Full exclosures were built with sides network of bays, channels, and ponds bordered by hy- of 0.25-mm nylon mesh attached to a frame of welded brid cattail Typha X glauca Godr. and common reed wire fence and supported by corner posts. Carp exclo- (Phragmites australis (Cav.) Trin ex. Steud.) (deGeus sures were built with 5 ϫ 10 cm welded steel mesh 1987, Shay et al. 1999). Sago pondweed (Stuckenia fencing. In addition to excluding large carp, the mesh pectinata (L.) Borner) is the most abundant submersed fencing may have reduced access of other large ani- macrophyte in the marsh (Anderson and Low 1976, mals (e.g., turtles and muskrats) to the plots, but we Anderson 1978). Summer water clarity is generally never sighted either of these species during our regular low, with vertical extinction coef®cient values (kd, visits to the exclosures. For both treatments, exclosure photosynthetic active radiation) of 3.2±5.0 mϪ1 and sides extended at least 15 cm into the sediments, and turbidity values of 12±25 NTU (Evelsizer 2001). The exclosures were covered with poultry-wire mesh fenc- marsh is moderately brackish (classi®cation of Stewart ing. Reference plots were marked at all four corners and Kantrud 1972), with speci®c conductivity values with 2.1 m steel fence posts. that generally range between 1000 and 3000 ␮S/cm Each of the two study sites received seven full ex- and total dissolved solids concentrations ranging from closures, seven carp exclosures, and 14 reference plots. 519 to 3230 mg/l (Goldsborough 1995, Evelsizer Treatments were randomly assigned to plots, and plots 2001). The waters are nutrient-rich, with water-column were arranged parallel to shore and placed so as to nitrogen: phosphorus ratios generally Ͼ16 and total standardize water depth (mean depth within cages ϭ phosphorus concentrations generally Ͼ 50 ␮g/l 76 cm in Division Bay, 56 cm in 22-Bay) and maintain 432 WETLANDS, Volume 26, No. 2, 2006

Figure 1. Map of east Delta Marsh, Manitoba, Canada showing location of study sites in 22-Bay and Division Bay. uniform sediment characteristics. Exclosures were Peak standing crop of S. pectinata foliage occurs by constructed on shore and transported to each site with mid-August to early September (Anderson and Low an airboat to minimize disturbance to the study site. 1976). Therefore, we sampled vegetation biomass in Placement of exclosures was completed on May 25, each exclosure between 15 and 22 August. Four ran- less than one month after ice-out and before signi®cant domly selected locations within the interior of each above-ground macrophyte growth had begun. Two exclosure (Ͼ 0.5 m from edge in order to minimize minnow traps were placed within each full-exclosure any edge effects) were sampled for estimation of plot to capture any ®sh that invaded as eggs or larvae, above-ground and below-ground biomass. At each lo- and all exclosures were inspected at least twice a week cation, a 50 ϫ 50 ϫ 65 cm sheet metal quadrant was to ensure that large ®sh had not jumped into or oth- pushed into the sediments. All foliage was removed erwise invaded the plots. from within the quadrant for estimation of above- Evelsizer & Turner, FISH AND SUBMERSED MACROPHYTES 433

Figure 2. Treatment effects on Chara biomass in 22-Bay. Bars denote mean plus one standard error, nϭ14 enclosures in reference treatment and 7 enclosures for carp and full-exclosure treatments. ground biomass. Below-ground biomass was estimated analysis of exclosure effects on S. pectinata biomass. by removing all sediment within the quadrant to a In cases where ANOVA found signi®cant exclosure depth of 15 cm. The sediment was rinsed and sieved effects, Tukey's post-hoc test was used to make pair- with a 1.6-mm screen to retain roots and tubers. Roots wise comparisons among exclosure treatments. The were harvested to a depth of 15 cm to maintain con- design is unbalanced, with more reference plots than sistency with the earlier studies of Anderson and Low full exclosure or carp exclosure plots, which can make (1976) and Anderson (1978). Vegetation was air-dried ANOVA less robust to violations of assumptions, par- for at least 10 d, then sorted by species, oven dried ticularly homogeneity of variances. Data were ana- (60Њ C for 24 h) to a constant mass, and weighed. lyzed with the General Linear Models routine of SPSS We evaluated treatment effects on water clarity by 12.0, using type III sums of squares. Type III sums of measuring light extinction and turbidity on four oc- squares are invariant with respect to cell frequencies casions during the summer. The vertical attenuation of and, thus, are useful for unbalanced designs. In addi- photosynthetic active radiation (PAR) was estimated tion, the treatment effects presented here are either using a Li-Cor LI-192 underwater quantum sensor to highly signi®cant or far from signi®cant, so the out- record light intensity at the surface and at a depth of come is unlikely to be affected by the unbalanced de- 20 cm within each exclosure. The extinction coef®- sign. Data were log-transformed when necessary in or- cient kd was estimated as the instantaneous rate of light der to promote homoscedasticity. attenuation (Wetzel and Likens 2000). We sampled turbidity using a 5.5-cm-diameter clear tube, which ex- RESULTS tended through the entire water column. Water was allowed to mix inside the tube before ®lling 500-ml Two species of submersed macrophytes were abun- sample bottles, which were then read by a turbidime- dant in the study plots. Chara sp., a green macroalgae ter. We randomly selected 7 of the 14 reference plots (Chlorophyta: Charophyceae), composed 63% of the for water clarity measurements (n ϭ 21 measurements above-ground biomass in 22-Bay (reference plot per site). Water clarity measurements were averaged mean) but comprised less than 2% of macrophyte bio- across the summer for each plot, and plot means were mass in Division Bay. Stuckenia pectinata comprised the unit of analysis. most of the remaining macrophyte biomass at the two The effects of exclosure treatment and site on mac- sites. Myriophyllum sibiricum (Komarov), Utricularia rophyte biomass variables (above-ground biomass, be- macrorhiza (LeConte), and Vallisneria americana low-ground biomass, root/shoot allocation) and water (Michx.) were present in a few plots but comprised clarity (turbidity, extinction coef®cient) were analyzed less than 1% of macrophyte biomass in all treatments. with two-way ANOVA, with plot means as the unit of Because these species were not present in most plots, observation. One abundant macrophyte, Chara sp., statistical analysis of treatment effects on their abun- was present at just one site, so the analysis of treatment dances was not possible, and they are not considered effects on Chara was a simple one-way ANOVA. We further. also tested whether Chara suppressed S. pectinata at There was a strong effect of exclosure treatment on ϭ Ͻ this site by using Chara biomass as a covariate in the Chara biomass in 22-Bay (Figure 2; F2,25 29.2; P 434 WETLANDS, Volume 26, No. 2, 2006

Table 1. Biomass of Stuckenia pectinata and water quality parameters within exclosure plots in 22-Bay and Division Bay. There is a signi®cant effect of site on above- and below-ground biomass of S. pectinata. All other treatment and site effects are not signi®cant. Standard errors of means are shown in parentheses. For vegetation variables, n ϭ 14 for reference pots, 7 for carp and full exclosure plots. For water transparency variables, n ϭ 7 for all three treatments.

22-Bay Division Bay Carp Full Carp Full Reference Exclosure Exclosure Reference Exclosure Exclosure Above-ground biomass (g/m2) 19.4 (4.5) 18.7 (5.3) 6.8 (1.1) 12.5 (3.1) 2.2 (0.8) 9.4 (3.6) Below-ground biomass (g/m2) 3.6 (0.5) 3.3 (0.6) 2.3 (0.3) 2.4 (0.5) 1.1 (0.4) 2.0 (0.7) Root/shoot ratio 4.9 (0.7) 5.7 (1.1) 2.9 (0.3) 4.9 (0.6) 2.5 (0.5) 4.0 (0.8) Extinction coef®cient (mϪ1) 4.3 (0.1) 4.2 (0.1) 4.4 (0.1) 4.4 (0.1) 4.5 (0.1) 4.5 (0.1) Turbidity (NTU) 12.6 (0.2) 12.8 (0.3) 12.8 (0.3) 12.7 (0.4) 12.2 (0.4) 12.5 (0.3)

0.001). Full-exclusion plots had the greatest Chara of exclosure treatment on light extinction or turbidity biomass, followed by the carp exclosure and reference (P Ͼ 0.10 for all treatment effects; Table 1). There plots (Figure 2). Full-exclusion treatment means were was no signi®cant site effect on light extinction, al-

signi®cantly different from both carp exclosure and though 22-Bay had slightly higher water clarity (F1,36 reference means (Tukey's Test, P Ͻ 0.001), but carp ϭ 3.72; P ϭ0.06) and no site effect on turbidity (Table exclosure means were not signi®cantly different from 1). reference means (P ϭ 0.38). The relative abundance of Chara was also greatest DISCUSSION in the full-exclusion treatment, where it comprised 96.4% of the total plant biomass, and lowest in ref- Marshes worldwide have been altered by human ac- erence plots, where it accounted for 62.6 % of the tivities from a clear-water state with abundant sub- plant biomass. Exclosure effects on relative abundance mersed vegetation to a turbid state with little or no ϭ ϭ were signi®cant (F2,25 3.6; P 0.04), with full-ex- vegetation (Jeppesen et al. 1998b, Scheffer 1998). In closure means different from reference means (P ϭ order to restore these systems, it is essential to identify 0.03), but other pairwise comparisons were not signif- the mechanisms responsible for the state transition. icant (P Ͼ 0.10). Field experiments can be an effective means of iden- Stuckenia pectinata biomass was relatively low, tifying such mechanisms (Dunham and Beaupre 1998). with above-ground biomass in reference plots aver- Here, we showed that a local reduction in ®sh abun- aging just 15.9 g mϪ2 and below-ground biomass 3.0 dance can induce increased plant growth, but this re- gmϪ2. Exclosure treatments had no effect on above- sponse depends on the initial state of the system. At a ground biomass of S. pectinata, below-ground bio- site with Chara present, ®sh exclusion had a strong mass, or shoot/root allocation (P Ͼ 0.10; Table 1). positive effect on overall abundance of submerged There was a signi®cant effect of study site on S. pec- macrophytes, but at a site dominated by S. pectinata, tinata biomass, with average above-ground biomass in ®sh exclusion had no effect on macrophyte biomass. reference plots 1.76-fold higher in 22-Bay than in Di- The failure of S. pectinata growth rates to respond ϭ ϭ vision Bay (F1,50 4.17; P 0.05), and below-ground to either of the ®sh exclosure treatments was contrary biomass 1.66-fold higher in 22-Bay than in Division to our expectations, but a review of the literature sug- ϭ Ͻ Bay (F1,50 7.33; P 0.01; Table 1). There was no gests that this result is consistent with other studies of site effect on root/shoot allocation (P Ͼ 0.10) and no submersed macrophytes in wetlands. Studies conduct- nonadditive effects of exclosure treatment and site on ed in wetlands dominated by S. pectinata have found any of the variables (P Ͼ 0.10 for all interaction that the abundance of this species is often unrelated to terms). An analysis of co-variance (ANCOVA) testing water clarity (Bales et al. 1993, Jeppesen et al. 1994, for the joint effects of Chara biomass and exclosure Moss 1994, Jeppesen et al. 1998a). Stuckenia pectinata treatments on above-ground biomass of S. pectinata is relatively tolerant of high turbidity because of its showed that the biomass of S. pectinata was not re- growth habit of forming a canopy of foliage near the ϭ lated to Chara biomass (ANCOVA; F1,24 0.181; P water's surface (Kantrud 1990). We found that the rel- ϭ0.20). ative abundance of S. pectinata in 22-Bay decreased Averaged across the summer, there were no effects in ®sh exclosure plots. Similarly, Anderson (1950) and Evelsizer & Turner, FISH AND SUBMERSED MACROPHYTES 435

King and Hunt (1967) found that ®sh removal will However, it is important to consider the extent to allow other species to re-establish themselves in the which our results can be extrapolated to large-scale plant community and eventually lead to a lower abun- manipulations (Dunham and Beaupre 1998). Our ex- dance of S. pectinata. These other species presumably closures permitted water exchange with the surround- compete with S. pectinata and reduce its dominance ing marsh, so treatment effects on water clarity may in the plant assemblage. If S. pectinata is less sensitive have been diluted. In addition, propagule limitation to turbidity than other taxa, the results of experimental may slow the invasion of new species (van der Valk studies examining the effects of improved water clarity and Davis 1978) and thus inhibit the response of the on the overall abundance of submersed plants will de- macrophyte community to short-term improvements in pend on the availability of propagules for these other, water clarity. These particular processes would tend to less tolerant taxa. make restoration of macrophytes more dif®cult at Exclusion of all ®sh in 22-Bay resulted in a 11.9- small scales than at larger scales, and we expect that fold increase in Chara standing crop, but carp exclu- exclosures like ours may underestimate the potential sion resulted in just a 3-fold increase. This difference for recovery of submerged macrophytes. suggests that small, planktivorous ®sh play an impor- Anderson (1978, see also Anderson and Low 1976) tant role in regulating water clarity and growth of sub- also studied factors limiting the growth of S. pectinata merged macrophytes. Planktivore exclusion can have in Delta Marsh. Their study focused on spatial varia- a positive effect on macrophytes via a trophic cascade tion in growth and found that sediment characteristics, that results in higher zooplankton abundance, lower exposure to wave action (fetch), and mean water depth phytoplankton abundance, and improved water clarity were the most important factors in determining the (Turner and Mittelbach 1992, Carpenter and Kitchell biomass of S. pectinata at a particular site. These data 1993, Schriver et al. 1995, Jeppesen et al. 1997). An also provided a valuable benchmark that, when con- important role of planktivorous ®sh is certainly plau- trasted with more recent surveys, show that production sible, as small ®sh were very abundant in the marsh of S. pectinata in Delta Marsh has decreased by ap- (Kiers and Hann 1995). Overnight sets of Beamish proximately 40% over the past 30 years (Wrubleski minnow traps (Evelsizer 2001) showed that fathead 1998, Evelsizer 2001). The factors identi®ed by An- minnows (a planktivore) were very abundant at both derson (1978) as responsible for driving patterns of study sites (catches Ͼ 800 per set). Spottail shiners spatial variation within Delta Marsh fail to account for (Notropis hudsonius Clinton) and Iowa darters (Eth- the recent decline of submersed macrophytes, as there eostoma exile Girard) were moderately abundant is no evidence that sediment characteristics, wave ac- (catches Ͼ 30 per set), and other zooplanktivorous ®sh tion, and water depth changed appreciably between including brook stickleback (Culaea inconstans) and 1970 and 2000. However, there is evidence that the yellow perch (Perca ¯avescens Mitchell) were also abundance of planktivorous and benthivorous ®sh in present. Delta Marsh has increased (Wrubleski 1998), probably Despite the circumstantial evidence implicating because of stabilized water levels associated with com- small ®sh and trophic cascades in the suppression of pletion of Fairford Dam (Batt 2000). submerged macrophytes, our measurements of water The experimental results presented here show that clarity (turbidity and light attenuation) failed to detect ®sh exclusion can increase the biomass of submersed consistent treatment effects. This is not entirely sur- macrophytes and induce a shift in species composition. prising, as the mesh walls of the exclosures permitted They further suggest that it is not the direct action of some water exchange with the surrounding marsh. It carp uprooting plants that is responsible for macro- is possible that any shifts in water clarity were tran- phyte suppression, but rather some other yet uniden- sitory and largely missed by our snapshot samples, or ti®ed mechanism associated with the presence of ®sh. that they were small in magnitude but important to the Taken together with earlier studies of Delta Marsh, it plants. It is also possible that some factor other than seems likely that recent changes in the ®sh dynamics light availability limited plant growth, but water clarity of Delta Marsh may have played a key role in the in 22-Bay was greater than in Division Bay, which is decline of submersed macrophytes and that the success consistent with the greater plant biomass and presence of restoration efforts may well hinge on the ability to of Chara in 22-Bay. Thus, the results of the exclosure reduce ®sh abundance in the marsh. study support the hypothesis that ®sh contribute to the suppression of vegetation in Delta Marsh, but the ACKNOWLEDGMENTS mechanism of suppression remains unclear. Large-scale manipulations of Delta Marsh are being We thank the Delta Waterfowl Foundation for pro- considered, and our work was designed to provide data viding the ®nancial and logistical support necessary to regarding the potential success of such manipulations. conduct this work. Todd Arnold was particularly in- 436 WETLANDS, Volume 26, No. 2, 2006 strumental in the design and execution of this project. Manitoba, Winnipeg, MB, Canada. University Field Station (Delta Marsh) Annual Report 29:11±19. Luke Naylor, Chris and John DeRuyke, Faye Babi- Hanson, M. A. and M. G. Butler. 1994. 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