Evaluation of a decade of management of a North American aquatic invasive species (Nitellopsis obtusa) highlights scale-dependent effectiveness and monitoring gaps
Abstract
Nitellopsis obtusa (starry stonewort) is an invasive macroalga subject to substantial control efforts in the Midwestern United States; however, there has not been systematic evaluation of treatment effectiveness. We synthesized management approaches and outcomes using monitoring performed over a decade-long period across 38 lakes in Indiana, Wisconsin, and Minnesota. Copper-based algaecide treatments were the primary means of control, followed by physical removal methods or combination treatments. Control efforts and associated monitoring data varied by spatial scale, as did surveyors’ N. obtusa sampling methods. At the largest (whole-lake) scale, we found no evidence that algaecide treatments were slowing expansion or reducing abundance of N. obtusa within infested lakes. At smaller, within-lake scales, we found that algaecide and physical treatments could reduce N. obtusa frequency and biomass, but outcomes were highly variable. At the smallest scales, hand pulling was an effective containment strategy for small, localized populations that were detected early. These results highlight the need to set realistic goals for N. obtusa control and develop improved management techniques. There were also critical gaps in monitoring that limited our ability to evaluate treatment effectiveness. In particular, increased monitoring of unmanaged reference lakes and untreated areas within managed lakes is needed.
Introduction
Aquatic invasive plants are a major threat to freshwater ecosystems, where they negatively affect native aquatic plant and fish communities, disrupt food webs, interfere with recreation, and decrease property values (Zhang and Boyle 2010; Schultz and Dibble 2012; Olden and Tamayo 2014; Tasker et al. 2022; Carey et al. 2023). While preventing spread to new waterbodies is the best option for limiting negative impacts, controlling within-lake spread and abundance becomes the primary means of mitigating impacts once they have established within a waterbody (Simberloff et al. 2013). Thus, evaluating and improving control effectiveness is crucial for soundly investing limited resources for management.
The invasive macroalga, starry stonewort (Nitellopsis obtusa Desv. (J. Groves)), has been a challenge for lake managers for decades in the Midwestern United States (Pullman and Crawford 2010; Larkin et al. 2018). First discovered in the 1970s in Quebec, it has spread to the Laurentian Great Lakes and inland lakes in the U.S. and Canada (Geis et al. 1981; Karol and Sleith 2017). Its dense growth is associated with declines in native macrophytes (Brainard and Schulz 2017; Ginn et al. 2021), facilitation of invasive zebra mussels and cyanobacteria blooms (Harrow-Lyle and Kirkwood 2020), and alteration of benthic water chemistry (Harrow-Lyle and Kirkwood 2021). Dense N. obtusa growth can impair dock access, boating, fishing, and swimming. While control efforts have been ongoing in some areas for ca. 20 years, there were no published laboratory or mesocosm studies on the efficacy of commonly used algaecides for N. obtusa until recently (Pokrzywinski et al. 2021; Wersal 2022; Glisson et al. 2022a). Evaluation of effectiveness of in-situ treatments is similarly lacking, with published field studies limited to a single lake in Minnesota (Glisson et al. 2018; Carver et al. 2022). To advance N. obtusa management, there is a critical need to understand the effectiveness of ongoing management across a broader range of lakes.
Copper-based algaecides have been the primary means of attempting to control N. obtusa in the Midwestern U.S. (Pullman and Crawford 2010; Glisson et al. 2018; Larkin et al. 2018). Aquatic pesticide regulations are stricter in Canada (Anderson et al. 2021), where algaecides have not been used on N. obtusa to our knowledge. Copper has been used for nuisance algae control for decades (Lembi 2014) and can be effective for macroalgae control in small waterbodies (e.g., ponds, rice paddies, McIntosh 1974; Guha 1991). However, effectiveness against macroalgae in lakes has been less thoroughly studied. Evidence from laboratory and mesocosm trials shows modest control of N. obtusa at concentrations at or near maximum product-labeled rates of 1 mg Cu L−1 (Pokrzywinski et al. 2021; Wersal 2022; Glisson et al. 2022a). However, these concentrations are difficult to achieve and maintain under operational field settings. In addition, because copper algaecides are non-systemic (i.e., not translocated through plant tissues), repeat treatments are often needed throughout the growing season to keep up with substantial seasonal growth (Glisson et al. 2018; Glisson et al. 2022b). This has raised concerns about copper algaecide use for N. obtusa given copper's toxicity to aquatic organisms (e.g., Mastin and Rodgers 2000; Christenson et al. 2014; Closson and Paul 2014; Kang et al. 2022) and its persistence and accumulation in sediments (Han et al. 2001). Given known and potential impacts of copper to freshwater systems, the effectiveness of continued use of copper-based algaecides for N. obtusa should be evaluated. Ideally, this could support achievement of control objectives balanced with minimizing copper inputs into the natural environment.
As an alternative to, and sometimes in combination with copper algaecides, physical removal methods have been implemented for N. obtusa control. For example, mechanical harvesting has been used to manage N. obtusa in some lakes (Glisson et al. 2018). Other methods, such as hand-pulling, diver-assisted suction harvesting (DASH), and drawdowns have also been implemented. The outcomes of these treatment efforts are often not recorded, analyzed, or reported due to time constraints and other challenges. When reported, they have largely been confined to grey literature or presentations, and, importantly, not synthesized with other treatment attempts. To enable sound recommendations regarding non-chemical and combination management strategies, comprehensive assessment is needed.
State agencies, lake groups, and contractors in the Midwest U.S. routinely conduct systematic surveys of N. obtusa lakes concurrent with management. Leveraging these data would allow for large-scale analysis of treatment effectiveness. Such approaches have advanced science-based management for other invasive aquatic plants (e.g., Kujawa et al. 2017; Nault et al. 2018; Mikulyuk et al. 2020; Verhoeven et al. 2020) and are urgently needed for N. obtusa.
We used data from the first 5–10 years of N. obtusa management in three Midwestern states to evaluate the effectiveness of current management approaches. Specifically, our objectives were to: (1) document the state of N. obtusa management in the Midwestern U.S.; (2) assess whether common management approaches are reducing the extent and abundance of N. obtusa; (3) identify the most promising approaches for control; and (4) develop recommendations for improved monitoring of management effectiveness.
Methods
Survey data
Many lakes in the study region are monitored using point-intercept (PI) surveys to assess aquatic plant community condition and change over time. Whole-lake PI surveys are a standardized method wherein evenly spaced points are sampled for aquatic plants with a thrown or spun rake method (Hauxwell et al. 2010; Madsen and Wersal 2017; Perleberg et al. 2019). The presence of each species or higher taxon (e.g., Chara spp.) is recorded and, for most but not all surveys, their relative abundance is estimated using the rake density method (also known as the rake fullness method; Deppe and Lathrop 1992). Rake density is measured on an ordinal, often 1–3, scale, with 1 indicating small fragment(s) present, 3 indicating a fully covered rake-head, and 2 indicating an intermediate abundance level (Hauxwell et al. 2010). The PI survey method is additionally adapted for targeted monitoring of managed areas, with denser concentrations of points and additional metrics, such as biomass, measured (a “sub-PI” survey, e.g., Glisson et al. 2018).
We compiled all available PI survey data from lakes where N. obtusa was known to occur since the year the species was first discovered in each state (Indiana, 2008; Wisconsin, 2014; Minnesota, 2015) until 2018 (Indiana) and 2019 (Wisconsin and Minnesota) (Fig. 1; see Supplementary Materials Table S1 for general study lake information). These data comprised raw survey and summary data from whole-lake PI surveys, as well as targeted sub-PI surveys within managed areas. For surveys conducted in the first year N. obtusa was discovered in a lake, we only retained those performed on or after its discovery date. We standardized all data to account for differences in methodology, sampling, and data entry. Specifically, Indiana uses a rake density scale of 1, 3, and 5 (INDNR 2018); however, this is equivalent to the 1–2–3 scale used by Minnesota and Wisconsin (Deppe and Lathrop 1992; Hauxwell et al. 2010; Perleberg et al. 2019) and was adjusted accordingly. For sub-PI surveys, 1–4 or 1–5 scales were sometimes used. In these cases, values >3 were converted to 3; for the 1–5 scale, values of 3 were converted to 2. To account for differences in sampling methodology and states’ variable definitions of the littoral zone, we selected only data from points ≤4.57 m (15 ft.) deep, following previous analyses of PI data (e.g., Verhoeven et al. 2020). For Indiana, data were summarized by depth bands in 1.5 m (5 ft.) increments; we selected data from the 0–5, 5–10, and 10–15 ft. bands. Data lacking an associated water depth (or depth band) were excluded.
Fig. 1.
Management data
We compiled all available information on N. obtusa management for the time periods encompassing the survey data. Management data were collected from: (1) pesticide application records (PARs; Minnesota), (2) chemical treatment and mechanical harvesting records (Wisconsin), (3) aquatic vegetation management plans (AVMPs; Indiana), and (4) direct knowledge of known management events (all states). We compiled as much information as possible for each management action on each lake, including management type (e.g., chemical treatment, hand pull, etc.); date and duration; area, water depth, and acre-feet of the managed area; chemical product(s) used and their amounts/concentrations; and, for copper algaecide applications, the amount of elemental copper applied. For hand pulling, we additionally compiled all available data on the biomass of N. obtusa removed during each event; we included all such data through 2022. For compiling summary data on management actions, we defined a management event as a discrete action implemented at a given time and location on a lake. Where information was missing, we estimated values if feasible. For example, when an exact date was not provided, we used the midpoint of the month provided. When only general information on management timing was available (e.g., “early season” or “summer”), we inferred whether the management action occurred before or after a given survey that year.
We used information for copper algaecide treatments to estimate the amount of elemental copper used across the study area and time span. If the product and amount (gallons or lbs.) were available for a given treatment, we used this information along with the product label to calculate elemental copper applied. If the amount of product was not reported, we used application rates (e.g., gal./acre-ft.) and the volume (acre-ft.) of the treatment area to estimate elemental copper. If neither the product amount nor acre-feet were available, we estimated based on the application rate and treated surface area.
Data analysis
Whole-lake response to management
We used whole-lake PI data to evaluate the lake-wide response of N. obtusa to management in terms of frequency of occurrence and abundance. Frequency of occurrence is the proportion of survey points in the littoral zone where N. obtusa was found (i.e., occupied surveys points/total survey points). Changes in frequency of occurrence over time can be considered changes in population extent, e.g., indicators of expansion or contraction. While frequency of occurrence lacks information on the amount of N. obtusa at a given survey point, frequency of occurrence data are easy to collect, widely available, and have been used in similar retrospective analyses of invasive macrophyte management (Kujawa et al. 2017; Mikulyuk et al. 2020; Verhoeven et al. 2020). Notably, the ability to detect changes in frequency of occurrence is sensitive to the density of survey points and the initial frequency of the species of interest (Mikulyuk et al. 2010). For species that occur infrequently, or highly localized within a lake, as is often true early in N. obtusa invasions (Bajcz et al. 2024), whole-lake frequency of occurrence may be a less sensitive measure compared to other approaches (e.g., targeted sub-PI surveys, biomass measurements). Abundance data are sometimes collected during PI surveys and provide information on the amount of N. obtusa, where present. For abundance, we used mean rake density where N. obtusa was found (i.e., rake density where present, following Verhoeven et al. 2020). Rake density was not available for all surveys, hence, abundance-based analyses relied on fewer data points.
Chemical treatments were by far the most common, and thus data-rich, management approach; therefore, these were the focus of our analysis of whole-lake response to management. Because chemical treatments were targeted for control of N. obtusa—a macroalga—we use the term “algaecide” sensu lato to describe these products and treatments, even though this includes some products that were formulated to control vascular plants (i.e., herbicides). The dataset was not sufficient to compare different products and product combinations (but see Pokrzywinski et al. 2021; Glisson et al. 2022a). We categorized any lake having received ≥1 algaecide treatment prior to a whole-lake survey as having been “managed” for that year. Other management actions were sometimes performed alongside algaecide treatments (e.g., mechanical harvesting, hand-pulling), but these non-chemical treatments were secondary and applied to smaller areas. To ensure that sufficient area was treated for a lake-level impact to be detectable, we included surveys for which at least 0.4 ha (1 acre) of the lake was treated with algaecide (PI surveys are typically spaced for a minimum of one point per acre, Perleberg et al. 2019). To account for the late-season phenology of N. obtusa (Glisson et al. 2022b), i.e., to avoid surveys conducted before peak frequency and abundance, we selected surveys performed after 30 June of each year.
In addition to management status, we included explanatory variables that were widely available and likely to affect management outcomes: survey day of the year, years since the lake was known to be infested (i.e., there was a verified report of N. obtusa presence), proportion of lake area managed with algaecide, and an interaction between management status and years since infested. We included survey day of the year to account for N. obtusa phenological differences among survey dates (Glisson et al. 2022b), and years since infested to account for within-lake expansion of N. obtusa over time (Ginn et al. 2021). To account for extent and intensity of treatment—and given that multiple treatments were commonly conducted prior to a PI survey—we summed the acreage of all within-year algaecide treatments before a PI survey and divided this amount by total lake acreage; this value was used as the proportion of the lake area managed with algaecide. We did not have information on the total N. obtusa infested area for all lakes; however, consistent with prevailing practice, we assumed that management extent generally scaled with infestation extent, up to any state restrictions on treatment area. Finally, we included the interaction between management status and years since infested to account for potential effects of natural increases in N. obtusa over time on treatment outcomes.
All analyses were performed using R statistical software (R Development Core Team 2020). For N. obtusa frequency of occurrence, we fit a generalized linear mixed-effects model (GLMM) using the glmmTMB package, with binomial errors and logit link (Brooks et al. 2017). For this analysis, our sample was 103 surveys from 34 lakes over 10 years. Of the 103 surveys, 65 were conducted following management, and 38 were conducted prior to management or in an unmanaged year. We used frequency of occurrence as the response and management status (yes/no), proportion of the lake area managed with algaecide, years since infested, and survey day of the year as fixed-effect explanatory variables. We included a random-effect intercept for survey year to account for annual variability in N. obtusa populations. Additionally, we included a random slope for years since infested that varied with a random intercept for lake; this was to account for differences among lakes and accommodate different trajectories of population change over time.
Prior to analysis, we examined correlations among explanatory variables for multicollinearity. No variables were highly correlated (Pearson correlation coefficient [r] ≤ |0.6|). To improve model convergence and enable direct comparisons among explanatory variables, we scaled all explanatory variables to mean 0 and standard deviation 1. After running the model, we again assessed multicollinearity using variance inflation factors for each variable; none had a variance inflation factor >3, indicating only low correlation among variables. We confirmed model fit by visually examining residual plots and plotting observed versus fitted values. We additionally examined model fit and diagnostic tests for models using the DHARMa package (Hartig 2020) and determined that all models were acceptable.
For N. obtusa abundance (rake density), we fit a GLMM with gamma errors and log link. For this analysis, our sample was 77 surveys from 23 lakes over 9 years. Of the 77 PI surveys, 54 were conducted following management, and 23 were conducted prior to management or in an unmanaged year. We used the same fixed and random effects as for frequency of occurrence, except for proportion of the lake area managed with algaecide, which was excluded because we did not expect the areal extent of treatments to affect local abundance (where N. obtusa occurred). Additionally, we had fewer data points for this model and wanted to avoid overfitting. No explanatory variables were highly correlated (r ≤ |0.6|). Years since infested and the management status × years since infested interaction had variance inflation factors of 6.0 and 5.1, respectively, indicating moderate correlation and corresponding increase in standard errors of these variables, which we retained. We employed the same methods and tests to confirm model fit as for frequency of occurrence.
Response to management within treated areas: Before-after analysis
Effects of management should be most pronounced within discrete areas undergoing treatment. Hence, we separately analyzed more intensive sub-PI data from within managed areas. For most lakes, surveys were conducted both before and after treatment within these managed areas, allowing for direct evaluation of treatment outcomes and accounting for within-lake heterogeneity. Because many lakes received multiple treatments during the growing season and surveys were conducted inconsistently after follow-up treatments, we focused on the initial treatments conducted in a lake within a given year and used the before-after surveys of these initial treatments in our analysis. As with the whole-lake analyses, we focused on algaecide treatments, but in contrast to the whole-lake analyses, these treatments consisted exclusively of copper-based products. As with the whole-lake analysis, we treated algaecide treatment of any kind as a binary (yes/no). Other management approaches were also applied in discrete treatment areas, including hand pulling, DASH, and drawdown. Given limited data for these approaches, we assessed them individually as before-after case studies (see below). For lakes for which N. obtusa biomass data from hand pulling was available, we visually examined plots of biomass removed over time.
For the before-after algaecide treatment analysis, we fit GLMMs with N. obtusa frequency of occurrence and abundance as response variables. For both models, we included a single fixed-effect explanatory variable for treatment (two levels: before treatment, after treatment). We included random-effect intercepts for lake, year, and a unique identifier for each before-after comparison. Hence, this analysis is similar to a paired t-test of before vs. after data, but with random effects to account for the non-independence of surveys conducted within the same lakes and survey years. For the frequency of occurrence model, we used a binomial distribution and logit link, and examined 21 before-after comparisons (42 data points) from 5 Minnesota and 4 Wisconsin lakes across 4 years. For abundance, we used a gamma distribution and log link, and examined 19 before-after comparisons (38 data points) from the same lakes and years. We examined and confirmed fit for both models as described for whole-lake analyses.
For before-after case studies, we conducted individual χ2 tests using frequency of occurrence of N. obtusa before vs. after treatment. Due to small sample sizes and infrequent presences for N. obtusa in the case study data, we computed P-values using Monte Carlo simulation with 10 000 permutations. We examined 9 case studies (18 data points) from 4 Minnesota and 3 Wisconsin lakes across 5 years; treatments included DASH (n = 3), hand pull + algaecide (n = 2), and hand pull, dredge, drawdown, and suction dredge (n = 1 for each).
Response to management within treated areas: Before-after-control-impact analysis
For some lakes and years, surveyors compared treated areas to untreated reference areas over time. This before-after-control-impact (BACI) design enables treatment effects to be distinguished from natural variability over time (Stewart-Oaten and Bence 2001). Despite its inferential strengths, this design is not typically used for non-research monitoring of treatment effectiveness because it requires areas to be left untreated, additional monitoring, and more complex analyses. However, it outperforms simpler control-impact and before-after study designs for assessing environmental change (Christie et al. 2019).
We compiled all available data from lakes and years where a BACI design was implemented, selecting situations where: (1) before and after survey dates were known, (2) treatment details were known, (3) N. obtusa was found in both treated and reference sites before treatment, and (4) before-surveys did not follow any substantial treatments (e.g., an earlier algaecide treatment). For some lakes and years, unique treatments were implemented in different sites simultaneously or at different times; we examined each treatment action independently. Criteria for BACI analyses were met for seven analyses of treatment effectiveness across three lakes and 4 years: Big Muskego Lake (Wisconsin) in 2015 (n = 2), Little Muskego Lake (Wisconsin) in 2016 (1), and Lake Koronis (Minnesota) in 2016 (1), 2017 (2), and 2018 (1). The 2016 Lake Koronis data were analyzed previously (Glisson et al. 2018), but included here for comparison to other lakes and years. As with the before-after analysis, we examined surveys directly preceding and following the first treatment in each year to ensure that subsequent management did not impact results. See Supplementary Materials (Table S2) for information about BACI data.
For Big Muskego Lake and Lake Koronis, N. obtusa biomass was measured before and after treatments, and was used as the response variable in our models. We natural-log transformed biomass data (as ln[x + 1]) when the transformation improved normality of data, as determined by a Shapiro–Wilk normality test. For each lake, we fit a linear mixed-effects model (LME) with biomass as the response variable and treatment time (before/after), treatment type (treated/untreated), and a treatment time × treatment type interaction as explanatory variables. Because the same survey points were sampled before and after treatment, we included a random intercept for survey point. We examined the significance of the interaction term with type III analysis of variance (ANOVA) using the Anova function in the car package (Fox and Weisberg 2019), with a significant interaction term indicating a significant effect of treatment.
For Little Muskego Lake, we used the same modeling approach, but with frequency of occurrence as the response variable in a GLMM with binomial errors and logit link implemented with the glmmTMB package.
Results
Management approaches
We identified eight N. obtusa management strategies (Table 1). Algaecide treatment was the most common approach (90% of all management events), distantly followed by hand pulling (5%). The remaining approaches combined accounted for <5% of all management events. Algaecide treatments had a mean size of 5.5 ± 0.5 ha (1 S.E.) and comprised 33 unique products or product combinations (Supplementary Materials Table S3). The most common algaecide treatment was a combination of Cutrine®-Ultra and Hydrothol® 191 (41% of algaecide treatment events), followed by Cutrine®-Plus (19%), and Clipper™ (9%). Most algaecide treatments (88%) included at least one copper-based product, and an estimated total of 18 234 kg (20 tons) of elemental copper were applied across all treatments.
Table 1.
| Management approach | Frequency |
|---|---|
| Algaecide | 89.9% |
| Hand pull | 5.3% |
| Mechanical harvest | 2.0% |
| Diver-assisted suction harvest (DASH) | 1.3% |
| DASH + hand pull | 0.5% |
| Suction dredge | 0.5% |
| Dredge | 0.3% |
| Drawdown | 0.3% |
Whole-lake response to management
We found no evidence that within-year management reduced whole-lake N. obtusa frequency of occurrence (P = 0.139; Table 2). In fact, there was a non-significant positive association between management and N. obtusa frequency of occurrence. Surveys not associated with management had an estimated marginal mean frequency of occurrence of 0.080 (8% of surveyed points), whereas surveys following management had an estimated marginal mean of 0.108 (11% of points). The only significant predictor of N. obtusa frequency of occurrence was a positive relationship with years since infested (P < 0.001; Fig. 2). There was no evidence that N. obtusa frequency of occurrence was affected by an interaction between years since infested and management status, the proportion of lake area managed with algaecide, or survey day of the year (Table 2).
Table 2.
| Response variable | Explanatory variable | Estimate | SE | z | P-value |
|---|---|---|---|---|---|
| Freq. of occurrence | |||||
| Management (managed) | 0.331 | 0.224 | 1.479 | 0.139 | |
| Proportion of lake area managed with algaecide | 0.059 | 0.058 | 1.016 | 0.310 | |
| Years since infested | 1.251 | 0.275 | 4.544 | < 0.001 | |
| Survey day of the year | 0.040 | 0.034 | 1.169 | 0.242 | |
| Management (managed) × years since infested | 0.420 | 0.217 | 0.194 | 0.846 | |
| Rake density | |||||
| Management (managed) | 0.232 | 0.102 | 2.285 | 0.022 | |
| Years since infested | −0.174 | 0.094 | −1.855 | 0.064 | |
| Survey day of the year | −0.014 | 0.023 | −0.614 | 0.539 | |
| Management (managed) × years since infested | 0.199 | 0.114 | 1.754 | 0.080 |
Note: Parameter estimates are untransformed (logit scale for frequency of occurrence and log scale for rake density). All explanatory variables were scaled to mean 0 and standard deviation 1 prior to analysis. Bold text highlights significant or marginally significant explanatory variables.
Fig. 2.
For whole-lake abundance (rake density where N. obtusa occurred), there was a significant, positive association with management (P = 0.022; Table 2), i.e., N. obtusa abundance was greater following management. Surveys following management and those not associated with management had estimated marginal mean rake densities of 1.86 and 1.48 (out of 3), respectively. There was weak evidence of a negative relationship between years since infested and N. obtusa abundance (P = 0.064). There was similarly weak evidence that the relationship between abundance and management was affected by years since infestation (interaction: P = 0.08); abundance of N. obtusa among managed lake-years increased more with years since infestation than unmanaged lake-years. Lastly, there was no evidence of a relationship between N. obtusa abundance and survey day of the year (Table 2).
Response to management within treated areas
Frequency of N. obtusa occurrence within copper algaecide-treated areas significantly decreased following treatment (P = 0.014, d.f. = 37). Estimated marginal mean frequency of occurrence before and after treatment was 0.44 and 0.38, respectively—a mean reduction of 0.06 (6%). However, there was high heterogeneity in responses, with N. obtusa frequency also substantially increasing in some treated areas and remaining stable in others (Fig. 3; Supplementary Materials Table S4). Abundance of N. obtusa did not differ before vs. after treatment (P = 0.566, d.f. = 32). Estimated marginal mean rake density before and after treatment was 1.40 and 1.36 (out of 3), respectively.
Fig. 3.
Of the nine case studies examined, only two resulted in significant changes to N. obtusa: a whole-lake drawdown and dredging were associated with significant increases in N. obtusa frequency of occurrence (Table 3). The remaining management approaches resulted in non-significant changes in N. obtusa frequency of occurrence within treated areas. Nonetheless, hand pulling, alone or in combination with copper algaecide treatment, resulted in consistent reductions of N. obtusa frequency of occurrence (Table 3). These same types of hand-pull treatments depleted N. obtusa biomass down to sustained, low levels, in three Minnesota lakes (Fig. 4).
Table 3.
| Before management | After management | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| State | Lake | Year(s) | Management action | Survey date | Present points/survey points | F.O. (SE) | Survey date | Present points/survey points | F.O. (SE) | Χ2 | P-value |
| MN | Grand | 2019 | Hand pull | 30-Jul | 2/20 | 10% (7%) | 22-Aug | 1/22 | 5% (4%) | 0.47 | 0.60 |
| Pleasant | 2018 | Hand pull + algaecide | 31-Aug | 1/23 | 4% (4%) | 1-Nov | 0/23 | 0% (0%) | 1.02 | 1 | |
| Pleasant | 2019 | Hand pull + algaecide | 28-Jun | 1/23 | 4% (4%) | 30-Jul | 0/21 | 0% (0%) | 0.93 | 1 | |
| Rice | 2016 | Suction dredge | 11-Oct | 2/14 | 14% (9%) | 20-Oct | 1/14 | 7% (7%) | 0.37 | 1 | |
| Sylvia | 2016 | DASH | 11-Oct | 2/15 | 13% (9%) | 28-Oct | 5/16 | 31% (12%) | 1.42 | 0.39 | |
| WI | Little Cedar | 2019 | DASH | 14-Aug | 6/30 | 20% (7%) | 7-Oct | 10/45 | 22% (6%) | 0.05 | 1 |
| Little Muskego | 2015 | DASH | 1-Jul | 168/282 | 60% (3%) | 14-Sep | 170/290 | 59% (3%) | 0.05 | 0.86 | |
| Little Muskego | 2017-2018 | Whole-lake drawdown | 24-Aug | 65/534 | 12% (1%) | 4-Sep | 124/472 | 26% (2%) | 32.64 | < 0.001 | |
| Silver | 2019 | Dredge | 17-Jun | 5/128 | 4% (2%) | 10-Sep | 18/87 | 21% (4%) | 15.27 | < 0.001 | |
Note: MN = Minnesota; WI = Wisconsin. DASH = diver-assisted suction harvest.
Fig. 4.
Of the seven BACI analyses performed, three indicated significant treatment benefits, i.e., reduction of N. obtusa in treated relative to untreated reference plots over time (Fig. 5). Notably, all of these significant effects were from treatments conducted in a single lake (Lake Koronis; Figs. 5c, 5e, 5f). Other analyses indicated no significant treatment × time interaction (Figs. 5a, 5b, 5g) or a marginally significant increase with treatment (Fig. 5d).
Fig. 5.
Discussion
This study provides the first quantitative synthesis of N. obtusa management outcomes. At the largest spatial scale evaluated, current algaecide treatments were not effective for reducing the extent of N. obtusa within infested lakes (Table 2, Fig. 2), and there was evidence of increased abundance following such treatments (Table 2). At a finer scale, within individual treatment areas, there was significant reduction in N. obtusa frequency of occurrence following algaecide treatments overall (Fig. 3a), but outcomes were highly variable (Fig. 3b–3d) and there was not concomitant reduction in N. obtusa abundance. The most robust survey data available, from BACI sampling, showed that local N. obtusa biomass was consistently reduced with algaecide treatment in one lake, but biomass and frequency of occurrence were not reduced in two others (Fig. 5). The paucity of such robust data are a critical gap in monitoring that impedes assessment of management effectiveness. Similarly, it appears likely that N. obtusa will continue to spread within treated lakes, but whether such expansion would markedly differ in the absence of treatment is difficult to assess given a lack of monitoring of untreated reference lakes. Encouragingly, hand pulling of small infestations, alone or in combination with algaecide treatments, depleted N. obtusa to nearly undetectable levels (Fig. 4)
On a whole-lake scale, we expected to see declines in N. obtusa frequency and abundance with algaecide treatments, especially over time, given patterns observed for other invasive macrophytes. For example, Eurasian watermilfoil (Myriophyllum spicatum) significantly decreased in lakes over time with continued treatment (Kujawa et al. 2017), as did curly-leaf pondweed (Potamogeton crispus) (Verhoeven et al. 2020). The lack of lake-wide N. obtusa control with algaecides could be interpreted in several ways. One possible explanation is that these algaecide treatments may simply not slow the spread and reduce the abundance of N. obtusa within a lake; if so, then alternative approaches need to be developed, and continued treatments should be evaluated in light of limited resources for lake management and potential non-target impacts of algaecides (e.g., Mikulyuk et al. 2020).
Native Characean macroalgae such as Chara spp., which often co-occur with N. obtusa (Ginn et al. 2021; Harrow-Lyle and Kirkwood 2022), are sensitive to copper algaecides (McIntosh 1974; Guha 1991). Reduction of native Characeae following N. obtusa algaecide treatment has not been evaluated in the scientific literature to our knowledge, but if substantial, could consequently reduce competition for N. obtusa and thereby exacerbate its expansion. Native Characeae occupy a distinct niche in the macrophyte community, fostering fish and invertebrate communities that differ from those associated with vascular macrophytes (Blindow et al. 2014; Schneider et al. 2015). The extent to which N. obtusa may perform a similar role as native Characeae in North America is unclear. Thus, potential harm to native Characean macroalgae should be considered when deciding whether to treat N. obtusa. Complicating matters, however, is evidence that native Characeae may be particularly susceptible to displacement by N. obtusa (Wagner 2021), so there is also potential risk to native Characeae from unabated N. obtusa spread. Additionally, field and lab studies suggest that copper-based algaecide treatment could foster asexual reproduction of N. obtusa via increased bulbil production and/or sprouting (Glisson et al. 2018; Glisson et al. 2022a). In sum, sustained application of copper algaecides may negatively impact native Characeae while not effectively controlling N. obtusa spread; but native Characeae could also be negatively impacted by N. obtusa dominance. These complexities require careful consideration given the amount of copper being added to lakes for N. obtusa control (ca. 20 tons for study lakes during this monitoring period), paired with uncertainty about the long-term ecological impacts of N. obtusa invasion.
Interestingly, the only two lakes where N. obtusa was not managed, and surveys spanned ≥2 year(s) (Pike Lake, Wisconsin; Like Winnibigoshish, Minnesota), exhibited decreasing and minimally increasing N. obtusa frequency, respectively, contrasting with other lakes in the region that were regularly managed and showed consistent N. obtusa expansion (Fig. 2). These patterns may be due to sub-optimal conditions for N. obtusa growth in these lakes compared to others; nonetheless, these patterns, combined with disappointing control outcomes and concerns about toxicity risks with repeated copper use, have led the Wisconsin Department of Natural Resources to substantially limit permits for chemical control of N. obtusa. The generally decreasing N. obtusa frequency of occurrence over time in Pike Lake is particularly compelling. This pattern demonstrates the value of monitoring some infested lakes while refraining from management, and further suggests the possibility of this approach being as or more beneficial than algaecide treatment—at least at a whole-lake scale. Along with management status, other factors in a waterbody, such as water clarity, water chemistry, and sediment composition, should also be monitored in infested lakes to determine how they may impact N. obtusa abundance and management effectiveness. Similar to the case of Eurasian watermilfoil, a lack of N. obtusa management does not seem to condemn a lake to be fully overtaken (Kujawa et al. 2017).
A second potential explanation of the lack of whole-lake response of N. obtusa to algaecide treatment could be that there has been insufficient treatment effort in terms of extent or concentrations, or use of poor-performing products and product combinations. In terms of extent, we did not have complete information on the area of each N. obtusa infestation, but entire populations were not always targeted for treatment, especially in lakes where populations covered most of the littoral zone, such as Lake Koronis (Minnesota). Treatment of greater proportions of N. obtusa populations could lead to greater lake-wide reductions. However, most states have regulations that restrict how much of the littoral zone can be treated, so this is not always possible. Regarding the most effective products and concentrations for N. obtusa control, only a handful of comparative studies have been performed (Pokrzywinski et al. 2021; Carver et al. 2022; Wersal 2022; Glisson et al. 2022a). While some products appear slightly more effective than others, to date there is little evidence of a specific product or combination (Table S3) substantially outperforming others. For copper algaecides, higher copper concentrations, up to the U.S. limit of 1 mg Cu L−1, generally perform better for N. obtusa control (Glisson et al. 2022a). Difficulty maintaining these concentrations for sufficient durations in the field (i.e., achieving adequate concentration-exposure time, or CET) and delivering algaecides to N. obtusa beds, however, may have led to poor treatment outcomes. Hence, strategies such as in-water barriers, cooled-water algaecide mixtures, and drop-hose applications could result in greater treatment effectiveness with currently used products. We cannot rule out that larger-scale treatments, new chemicals/combinations, novel application methods, and greater CETs would increase effectiveness; however, our analysis demonstrates that current algaecide approaches are not reducing N. obtusa on a whole-lake scale.
In contrast, at the scale of individual treatment areas, copper algaecide treatments were generally effective at reducing N. obtusa frequency of occurrence (before-after analysis) and showed mixed results based on biomass (BACI analysis). Most notable were the substantial biomass reductions within most treated areas on Lake Koronis relative to untreated control areas (Figs. 5c, 5e, 5f). The areas targeted for control on Lake Koronis were generally those with the greatest N. obtusa biomass, and biomass reductions were consistently achieved in these areas on a yearly basis. Thus, at a smaller scale, control of N. obtusa can be achieved with currently available algaecides, as has been observed in other recent field studies (also from Lake Koronis: Glisson et al. 2018; Carver et al. 2022). Reductions in N. obtusa frequency of occurrence and biomass, however, were not observed across all lakes and treatments. For frequency of occurrence, N. obtusa stayed stable or increased (Figs. 3c, 3d; Fig. 5g) in nearly as many cases as it decreased (Fig. 3b), and we did not observe reduced N. obtusa abundance based on before-after analysis of rake density. Even on Lake Koronis, N. obtusa biomass significantly increased following an early-summer treatment in 2017 (Fig. 4d, Supplementary Materials Table S2). In general, the BACI results suggest that later-season treatments and higher copper concentrations might be more effective. Nonetheless, without being able to account for other potentially influential factors (e.g., product applied, water depth, time of year), or the luxury of larger data sets encompassing many treatments varying across these factors, we cannot determine why some treatments were more successful than others. Future BACI studies could also examine effectiveness across multiple treatments within a year (e.g., Glisson et al. 2018), and across years.
Contrasting results of algaecide treatment outcomes at whole-lake versus finer scales highlight different scenarios for management of N. obtusa moving forward. For populations that are already widespread and established, large reductions in extent are unlikely using current management options, and control should be focused on high-priority areas, be those areas of greatest impacts to recreation (e.g., docks and accesses) or the environment (e.g., ecologically sensitive areas, those with rare native species). Within these smaller areas, reductions in N. obtusa frequency and biomass may be achievable. For small, localized populations, containing N. obtusa and deterring within-lake spread is feasible using algaecides and some of the case-study approaches described below. The success of these containment efforts is evidenced by the lack of spread in lakes where populations were quite small, and presumably detected early (e.g., Grand, Pleasant, Carnelian, and Sylvia Lakes in Minnesota).
Before-after-control-impact studies allow rigorous inference of treatment effectiveness (Christie et al. 2019). But a challenge for lake managers and decision makers is choosing to leave infested areas within lakes—or at a larger spatial scale, entire lakes—untreated. This is particularly difficult to do with high-concern emerging invaders like N. obtusa, where there is strong, justified motivation to intervene. Nonetheless, monitoring untreated areas/lakes is essential for evaluating treatment effectiveness, and thereby guiding and improving future management. Where populations are small and eradication is the goal, leaving an area untreated is not realistic. However, it is fairly common that N. obtusa is already extensive when discovered in a waterbody (see Fig. 2), and treatment of the entire population is not feasible (e.g., due to insufficient funds, regulations, or presence of sensitive species). In these situations, areas of similar environmental conditions and N. obtusa establishment could be paired as treatment and untreated reference site(s)—ideally with random assignment of management status. Because PI surveys are routinely conducted on numerous infested lakes, points could also be assigned as control areas without any additional work, i.e., points can simply be categorized as reference locations for subsequent analyses. With sufficient infestation extent, multiple treatment and reference sites could be monitored to increase the power of BACI analysis to detect treatment impacts (Underwood 1991). This framework could further be scaled up to examine entire lakes as treated and untreated. Lakes such as Pike Lake (Wisconsin), where eradication is unlikely and a robust native plant community is still intact, are particularly good candidates to remain untreated for BACI analysis. In addition to elucidating treatment effectiveness, untreated reference lakes are also vital for investigations of N. obtusa ecology and impacts, e.g., potential competition with native macrophytes (e.g., Glisson et al. 2022b).
Case studies, which included physical removal methods, suggested that some approaches are poor candidates for N. obtusa management (Table 3). Namely, a whole-lake winter drawdown on Little Muskego Lake (Wisconsin) resulted in a significant increase in N. obtusa frequency, with the proportion of occupied points doubling the year following the drawdown (2017: 12%, 2018: 26%). Desired sediment freeze and compaction were not achieved during this treatment, which likely limited its effectiveness. Such issues are common among drawdown treatments for macrophyte control (e.g., Dugdale et al. 2012). Bottom dredging was also ineffective for N. obtusa control: in Silver Lake (Wisconsin), frequency of N. obtusa significantly increased within the managed area. Both dredging and drawdown are major disturbances of the lake bottom. In its native range, N. obtusa was shown to be susceptible to disturbance caused by lakebed drying (Boissezon et al. 2018). However, in its invaded range in the Midwestern U.S., we have frequently observed N. obtusa in disturbed environments (e.g., near boat launches subject to prop wash) and consider it to at least tolerate if not outright benefit from disturbance. The drawdown and dredging in Little Muskego and Silver Lakes did lead to declines in co-dominant macrophytes, including Myriophyllum spicatum (WDNR, unpublished data). Thus, these treatments appear to have opened up habitat that N. obtusa was then able to colonize. These poor results, paired with the substantial cost and time commitment of whole-lake drawdown and dredging, caution against these approaches for N. obtusa management.
Two case-study approaches that were promising were hand-pulling and DASH (Table 3, Fig. 4). While DASH did not significantly reduce N. obtusa frequency of occurrence in Little Muskego and Little Cedar Lakes (Wisconsin; in 2015 and 2019, respectively), these treatments may have helped contain further spread, with frequency of occurrence largely unchanged two months following treatment, during time periods when N. obtusa biomass is expected to still be seasonally increasing (Table 3; Glisson et al. 2022b). Frequency of N. obtusa occurrence did increase following DASH on Lake Sylvia (Minnesota); however, this increase was not significant and was based on relatively few survey points. This approach warrants further research as an N. obtusa control strategy, particularly in situations where algaecides are not permitted or pose unacceptable risk to native macrophytes.
Hand pulling, alone or in combination with algaecide, did not result in statistically significant reductions of N. obtusa frequency of occurrence in our case study analysis (however, combination treatments did reduce N. obtusa frequency to zero occurrences in Pleasant Lake, Minnesota; Table 3). Presence-absence measures from PI sampling grids likely underestimate the effectiveness of hand pulling given the clumped, patchy distribution of nascent N. obtusa infestations—the context in which hand-pulling has been used. In contrast, measures of biomass removal illustrate the consistent effectiveness across lakes and over time of repeated, sustained hand pulling (Fig. 4). Sustained hand pulling resulted in similar reductions of Eurasian watermilfoil over a comparable time period (Gagné and Lavoie 2023). Along with DASH, hand pulling is a targeted method for directly removing N. obtusa while minimizing damage to native macrophytes. However, due to the time and effort needed to conduct hand pulls, this strategy is most feasible for small infestations in shallow areas with low turbidity.
Conclusion
Our analysis of N. obtusa treatments in three U.S. states provides a status update on N. obtusa management and a foundation for follow-up work. We close with four main conclusions related to treatment effectiveness, setting realistic goals for management, and needs for future monitoring:
1.
At the largest (whole-lake) scale, we found no evidence that algaecide treatments were containing or slowing expansion of N. obtusa within infested lakes. Long-term reduction of whole-lake extent and abundance is a reasonable management goal for other invasive macrophytes in the study region, but this is not (yet) a feasible target for N. obtusa control, i.e., with currently available tools and strategies that have been employed to date.
2.
At smaller, within-lake scales, we found that chemical and physical treatment methods can reduce N. obtusa biomass and frequency. Local control for recreational and other benefits may be a reasonable management goal. We also note high heterogeneity in outcomes across study lakes and treatment events, and encourage applied research to better understand the factors contributing to control effectiveness (or lack thereof).
3.
At the smallest scales, for new populations detected early, hand pulling (alone, or combined with algaecides) can be a highly effective containment strategy. Increased surveillance efforts to identify new populations are encouraged, as are technical and logistical support for lake groups and other organizations engaged in grassroots hand-removal efforts.
4.
We are grateful for the time-consuming monitoring performed by coauthors and their colleagues that enabled this analysis of management effectiveness. But there are limitations to the inferences we could make due to gaps in monitoring. In particular, it would be of tremendous value for advancing N. obtusa management to increase monitoring of untreated reference areas where and when it is feasible. These should include both (1) untreated locations within lakes that are undergoing management, to enable more BACI analyses; and (2) unmanaged reference lakes, to better characterize outcomes of the no-management alternative. Monitoring of this type would also increase understanding of the impacts of management on native plant communities, i.e., whether there are net benefits for native vegetation from N. obtusa reduction, net harm due to non-target impacts, or species-specific responses.
Acknowledgements
Funding for this project was provided by the Minnesota Environment and Natural Resources Trust Fund as recommended by the Minnesota Aquatic Invasive Species Research Center and the Legislative-Citizen Commission on Minnesota Resources. We thank Wendy Crowell of the Minnesota Department of Natural Resources and Justin Valenty of Three Rivers Park District for their help with this project. We thank all those who collected the field data that made this project possible.
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FACETS
Volume 10 • 2025
Pages: 1 - 14
Editor: Jacob Brownscombe
History
Received: 27 May 2024
Accepted: 9 January 2025
Version of record online: 28 February 2025
Copyright
© 2025 The Author(s). This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
Data Availability Statement
Data analyzed for this study are publicly available in the Data Repository for the University of Minnesota (DRUM) at https://doi.org/10.13020/vjxh-5p45.
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Author Contributions
Conceptualization: WJG, DJL
Data curation: WJG, MN, CJ, EF, KL, KBC, AL, NK, EHJ, RE, SM, EF
Formal analysis: WJG
Funding acquisition: DJL
Investigation: WJG
Methodology: WJG, DJL
Project administration: WJG, DJL
Supervision: DJL
Visualization: WJG, DJL
Writing – original draft: WJG, DJL
Writing – review & editing: WJG, MN, CJ, EF, KL, KBC, AL, NK, EHJ, RE, SM, EF, DJL
Competing Interests
The authors declare there are no competing interests.
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Minnesota Aquatic Invasive Species Research Center
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Wesley J. Glisson, Michelle Nault, Chris Jurek, Eric Fischer, Keegan Lund, Kylie Bloodsworth Cattoor, April Londo, Nicole Kovar, Emelia Hauck-Jacobs, Rod Egdell, Steve McComas, Eric Fieldseth, and Daniel J. Larkin. 2025. Evaluation of a decade of management of a North American aquatic invasive species (Nitellopsis obtusa) highlights scale-dependent effectiveness and monitoring gaps. FACETS.
10: 1-14.
https://doi.org/10.1139/facets-2024-0104
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