European Frogbit (Hydrocharis Morsus-Ranae) Invasion Facilitated by Non- Native Cattails (Typha) in the Laurentian Great Lakes

JGLR-01497; No. of pages: 9; 4C: Journal of Great Lakes Research xxx (xxxx) xxx

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European frogbit (Hydrocharis morsus-ranae) invasion facilitated by nonnative cattails (Typha) in the Laurentian Great Lakes

Andrew M. Monks a,⁎, Shane C. Lishawa a, Kathryn C. Wellons b, Dennis A. Albert b, Brad Mudrzynski c, Douglas A. Wilcox d a Institute of Environmental Sustainability, Loyola University Chicago, 1032 W. Sheridan Rd Chicago, IL 60660, USA b Department of Horticulture, Oregon State University, Agricultural and Life Sciences 4017, Corvallis, OR 97331, USA c Genesee County Soil and Water Conservation District, 29 Liberty St, Batavia, NY 14020, USA d Department of Environmental Science and Ecology, State University of New York: Brockport, Lennon Hall 108 B, Brockport, NY 14420, USA article info abstract

Article history: Plant-to-plant facilitation is important in structuring communities, particularly in ecosystems with high levels of Received 22 March 2019 natural disturbance, where a species may ameliorate an environmental stressor, allowing colonization by another Accepted 1 July 2019 species. Increasingly, facilitation is recognized as an important factor in invasion biology. In coastal wetlands, Available online xxxx non-native emergent macrophytes reduce wind and wave action, potentially facilitating invasion by floating plants. We tested this hypothesis with the aquatic invasive species European frogbit (Hydrocharis morsus- Communicated by Anett Trebitz ranae; EFB), a small floating plant, and invasive cattail (Typha spp.), a dominant emergent, by comparing logistic Keywords: models of Great Lakes-wide plant community data to determine which plant and environmental variables European frogbit exerted the greatest influence on EFB distribution at multiple scales. Second, we conducted a large-scale field ex- Facilitation periment to evaluate the effects of invasive Typha removal treatments on an extant EFB population. Invasive Hybrid cattail Typha was a significant predictor variable in all AIC-selected models, with wetland zone as the other most com- Invasive plants mon predictive factor of EFB occurrence. In the field experiment, we found a significant reduction of EFB in plots Laurentian Great Lakes where invasive Typha was removed. Our results support the hypothesis that invasive Typha facilitates EFB persis- Wetlands tence in Great Lakes coastal wetlands, likely by ameliorating wave action and wind energy. The potential future distribution of EFB in North America is vast due in part to the widespread and expanding distribution of invasive Typha and other invading macrophytes, and their capacity to facilitate EFB's expansion, posing significant risk to native species diversity in Great Lakes coastal wetlands. © 2019 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved.

Introduction climatic extremes (Franco and Nobel, 1989; Freestone, 2006; Lawrence and Barraclough, 2016; Ryser, 1993), as well as coastal envi- Invasion biology has tended to focus on competitive interactions be- ronments that face disturbance through wave and tidal action (Altieri tween introduced and native species with the diversity resistance hy- et al., 2007; Bertness and Leonard, 1997; Bruno, 2000; Wright et al., pothesis, suggesting that more diverse community assemblages are 2014). less prone to invasive species due to increased numbers of competitive The Laurentian Great Lakes have been a hotspot for biological inva- and predatory interactions with native species (Kennedy et al., 2002). sions, because of a history of commerce, industry, anthropogenic devel- Alternatively, numerous examples exist of synergistic effects among in- opment, and international shipping through the St. Lawrence Seaway vaders leading to the dominance of an invader, codominance of multiple (Ricciardi, 2006; Ricciardi and MacIsaac, 2000). The presence of numer- invaders, or cascading ecological disruptions across trophic levels ous concurrent invasions has created unique community assemblages (O'Dowd et al., 2003; Ricciardi, 2001; Simberloff and Von Holle, 1999). and species interactions among invasive and native species. Repeated Facilitative relationships between species, where one or multiple spe- introductions to the Great Lakes have led to large shifts in ecosystem cies moderate or buffer against stressful physical conditions and allow structure and function (Ricciardi, 2001), which has been cited as an ex- other species to establish or persist, are well-documented (Bertness ample of an invasional meltdown (sensu, Simberloff and Von Holle, and Callaway, 1994; Bruno et al., 2003; Stachowicz, 2001; Von Holle, 1999). Here, we focus on the interaction and apparent facilitative rela- 2013). Facilitation plays a role in terrestrial environments prone to tionship between two invasive taxa, Typha spp. and European frogbit (Hydrocharis morsus-ranae L.; EFB). ⁎ Corresponding author. In the Laurentian Great Lakes, both narrow leaf and hybrid cattail E-mail address: [email protected] (A.M. Monks). (Typha angustifolia L.; T. × glauca Godr.; hereafter invasive Typha) are

Please cite this article as: A.M. Monks, S.C. Lishawa, K.C. Wellons, et al., European frogbit (Hydrocharis morsus-ranae) invasion facilitated by nonnative cattails (Typha) in the Laurentian Great Lakes..., Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2019.07.005 2 A.M. Monks et al. / Journal of Great Lakes Research xxx (xxxx) xxx invasive aquatic macrophytes that began spreading in the early 1900s collected in 2011–2012 and 2014–2015. The GLCWMP sampled N500 along with expanding human populations and agricultural activity in GLCWs using a standardized methodology (Uzarski et al., 2017). In the region (Shih and Finkelstein, 2008). In the intervening century, in- each wetland, three transects were located parallel to the water-depth vasive Typha has become a common plant of coastal wetlands through- gradient, thereby bisecting the three typically occurring vegetation out all five Great Lakes and major connecting rivers, dominating 13.5% zones: wet meadow, emergent marsh, and submergent marsh. Along of total Great Lakes wetland area through 2013 (Carson et al., 2018). In- each transect, five evenly spaced 1-m2 sampling plots were located vasive Typha dominance is associated with well-documented reduc- within each vegetation zone (Uzarski et al., 2017). Transect lengths var- tions of plant diversity (Lishawa et al., 2010; Martina et al., 2014; ied depending on the width of vegetation zones. At each plot, vegetation Tuchman et al., 2009; Wilcox et al., 2008), reduced abundance of inver- sampling crews determined plant community composition by assigning tebrates (Lawrence et al., 2016)andfish (A. Schrank, University of Min- areal cover values (b1–100%) for each plant species, total vegetation, nesota, personal communication, 2018), reduced habitat complexity and standing dead vegetation. Additional environmental data were col- (Kantrud, 1986; Lawrence et al., 2016), and altered biogeochemical cy- lected from each vegetation plot including wetland zone (meadow, cling regimes (Larkin et al., 2012; Lawrence et al., 2017; Lishawa et al., emergent, submergent), water depth, and soil organic layer depth. Soil 2014). organic layer depth was measured by gently pushing a graduated pole EFB, a small free-floating perennial aquatic plant native to Europe through the easily penetrable organic layer to the mineral sediment (Catling et al., 2003; Zhu et al., 2018), is a relatively recent invader to margin. Additionally, for each individual wetland site, we calculated the Great Lakes. The North American population has been traced back the fetch by measuring the distance from the upland edge of the wet- to the Dominion Arboretum in Ottawa, Canada in 1932 where it had land (at the center of the linear extent of the wetland's shoreline) to been introduced from the Zurich Botanical Garden, in Zurich, the longest distance across open water to the lake's opposite shore. Switzerland (Catling et al., 2003). EFB subsequently spread up the St. We modeled data at the plot-level, treating all vegetation plots indepen- Lawrence River to Lake Ontario, where it was observed in 1991 (D. dently, and at the site-level, by calculating the average for all numerical Wilcox, personal observation, 1991). By 2004 it was found in 75% of values within each site. wetlands sampled (Trebitz and Taylor, 2007; Zhu et al., 2018) to the west and north to Lakes Erie and Huron. EFB now extends as far north Munuscong Bay invasive Typha-removal study as the St. Marys River, the connecting channel between Lakes Huron and Superior, where it was first documented in 2010 (D. Albert, per- We conducted our invasive Typha-removal experiment at the sonal observation, 2010). With its dense, intertwined growth habit, Munuscong Bay in Chippewa County, Michigan (46.20 N, 84.25 W, EFB can effectively outcompete native wetland taxa, especially floating Fig. 1). Munuscong Bay is a connecting channel river delta marsh plants, leading to a marked reduction in plant diversity (Catling et al., (Albert et al., 2005) positioned at the outlet of the Munuscong River to 1988). EFB can also be a nuisance to recreational and commercial the St. Marys River, which connects Lake Superior to Lake Huron. boating (Catling et al., 2003). Seasonal die-offs of EFB in the fall and sub- Munuscong Bay harbors an extensive population of invasive Typha, sequent decomposition have caused reductions in dissolved oxygen the dominant emergent macrophyte, which has been abundant in the (Zhu et al., 2008), which can have detrimental impacts on invertebrate site for N30 years (Albert et al., 1987). EFB was first found at Munuscong and fish communities dependent on Great Lakes coastal wetlands Bay in 2010 (D. Albert, personal observation, 2010), but the EFB popula- (GLCW) (Jude et al., 2005). EFB's reproductive strategy, including pro- tion has since expanded, reaching areal cover values of over 50% in some duction of easily-dispersed vegetative propagules (turions) that can re- parts of the marsh and becoming a dominant species in the Typha main dormant for at least two years (Catling et al., 2003), make understory. eradication of EFB populations especially challenging. As a watch- To test facilitation of EFB by invasive Typha, we set up an invasive listed invasive species in U.S. states (Nault and Mikulyuk, 2009; Typha-removal experiment during July 2016 in Munuscong Bay. Using Weibert, 2015) and Canadian provinces surrounding the Great Lakes, a low ground pressure amphibious, tracked vehicle (Softrak Cut and understanding its ecological associations is critical to predicting its Collect, Loglogic, Devon, UK), we implemented two treatments: spread and managing invaded wetlands. 1) One-time above water harvest (TyHarvAW), where all invasive In GLCWs, EFB commonly co-occurs with invasive Typha (Johnston Typha biomass N20 cm above the water line was cut and removed and Brown, 2013; Lemein et al., 2017; Trebitz and Taylor, 2007), a co- from the marsh by the Softrak harvester's flail-style chopping mecha- occurrence also documented in their home ranges in Europe (Sager nism, and 2) One-time below water harvest (TyHarvBW), which in- and Clerc, 2006). GLCWs are highly dynamic ecosystems that are ex- volved harvesting above water biomass, then subsequently cutting all posed to physical stress from wind, wave action, and seiche activity remaining severed invasive Typha stems ~20 cm below the water sur- (Trebitz, 2006). To evaluate whether invasive Typha was facilitating face using a specialized sickle-bar mower attachment (Loglogic, Devon EFB in GLCWs, we tested their co-occurrence at two scales. At the re- England). Each management plot was 15 × 60 m in size, with the nar- gional Great Lakes scale, we used plant data from a Great Lakes-wide row part of the plot oriented towards the open-water edge of the coastal wetland monitoring study. At the local scale, we analyzed asso- marsh to maximize water-depth variability within plots. The experi- ciations between the two species using intensively collected data within ment consisted of three replicate blocks within which we randomly Munuscong Bay, a Great Lakes coastal wetland that harbors both spe- assigned each of our two treatments and an unmanipulated control. cies. Secondly, at Munuscong Bay, we tested the ability for invasive All blocks contained invasive Typha as the dominant emergent species, Typha to facilitate EFB directly by conducting a large-scale (60 × 15 m with EFB growing at the water's surface. Pre-treatment percent cover plots), multi-year invasive Typha-removal study. We hypothesize that data on invasive Typha and EFB revealed some variability between existing populations of invasive Typha facilitate and allow the emerging blocks in Typha and EFB cover (ranging from 11.0 to 13.5% and invader EFB to persist and spread throughout Great lakes coastal 4.1–11.6%, respectively), but differences were not statistically signifi- wetlands. cant as determined by ANOVA (p N 0.05). To monitor the vegetative response to our invasive Typha removal Methods experiment, we established four 1-m2 subplots in each treatment plot within each of our three blocks (4 subplots × 3 treatments × 3 blocks Regional co-occurrence analyses for n = 36 subplots). Subplots were evenly spaced along the central axis of each treatment plot. In each subplot, we collected data mirroring To evaluate regional occurrences, we used data from the Great Lakes the methods of the Great Lakes Coastal Wetland Monitoring Program: Coastal Wetland Monitoring Program (GLCWMP) (Uzarski et al., 2017) water depth, depth of the organic soil layer, and aerial percent cover

Fig. 1. Location of invasive Typha removal study, Munuscong Bay on the St. Marys River in the eastern Upper Peninsula of Michigan, USA (a). Layout of blocks and plots nested within blocks (b). values (b1–100%) for each of the following: total vegetative cover, emergent, or submergent), invasive Typha presence, Phragmites standing dead vegetation, detritus below the water surface, and cover australis presence, and Phalaris arundinacea presence. We aggregated for each vascular plant species (Uzarski et al., 2017). Percent cover data to the site level by calculating the mean value of continuous nu- was determined via visual inspection from multiple samplers standing merical variables across all plots within each wetland. above each plot. We sampled each subplot once per year in late July or early August in 2017 and 2018 to coincide with peak plant coverage and precede EFB's propagule production (Catling et al., 2003). Analysis: Munuscong Bay invasive Typha-removal study

Analyses: regional co-occurrence For our field experiment, we analyzed the effects of treatment and year on plant and environmental data using linear mixed-effects model- We analyzed the regional co-occurrence between EFB and environ- ing (LME; Bates et al., 2015). We accounted for the non-independence mental variables, plant community assemblage, and dominant invasive of measures collected over two separate years by including treatment plant presence using logistic regression and stepwise Akaike Informa- and year as factors. Because the treatment for each plot was randomly tion Criteria (AIC) model selection to identify the model with the assigned and subplot locations were approximated within each plot highest parsimony (Burnham and Anderson, 2004). Models with ΔAIC by GPS, each subplot was treated as a nested random effect within values b2 were considered to be significant when assessing EFB pres- plot and block in the LME model. To minimize type I errors, we fit ence/absence (Burnham and Anderson, 2004). We created models of models using restricted maximum likelihood method and generated EFB occurrence in established populations (Lake Ontario) and invading type-III ANOVAs using approximated degrees of freedom with populations (all other Great Lakes and Great Lake connecting channels), Satterthwaite's method (Kuznetsova et al., 2017; Luke, 2017). The as- at the plot and site levels, with data from all four sampling years sumption of normality of residuals was checked visually with QQ (2011–2012, 2014–2015). Continuous predictor variables in full models plots, and log+1 transformation was used on all response variables to included: fetch, water depth, standing dead cover, and organic depth. meet assumptions of normality and homogeneity of variance. When Discreet predictor variables included: wetland zone (meadow, overall models were significant (p ≤ 0.05), multiple contrasts were

Regional co-occurrence frequent since 2002; D. Wilcox, personal observation, 2002; Trebitz and Taylor, 2007), invasive Typha was positively related and Phragmites Across all AIC-selected models of EFB occurrence in the Great Lakes australis was negatively related to EFB presence at the site-level (at the site-level, plot-level, established, and invading populations) in- (Table 1). Both relationships were significant (p b 0.05; Table 2). In a vasive Typha presence was the first or second most important predictor second substantially supported model (ΔAIC = 1.28; Burnham and variable (Table 1), and was significantly (p b 0.05) positively correlated Anderson, 2004), standing dead was also included as a positive predic- with EFB presence (Table 2). Within the range of well-established EFB tor of EFB presence (Table 1). At the plot-level in the established popu- populations (Fig. 2; i.e., Lake Ontario EFB first detected in 1991 and lation, meadow zone and standing dead were negatively related, while invasive Typha, emergent zone, and Phragmites australis were positively related to EFB presence (Table 1). All positive and negative correlations Table 1 Logistic regression models of Hydrocharis morsus-ranae (EFB) presence in Great Lakes were highly significant (p b 0.001) except for Phragmites australis pres- coastal wetlands across four years (2011–2012, 2014–2015) in the established population ence (Table 2). (Lake Ontario) and invading population (other lakes and connecting channels) at the site Within the EFB invading range (i.e. all other Great Lakes and Δ b and plot level. Substantially supported models, with AIC 2.0, as determined by stepwise connecting channels) at the site-level, invasive Typha, standing dead, AIC model selection (Burnham and Anderson, 2004), are displayed in decreasing order of support. Sign in parentheses following each variable indicates a negative influence on EFB organic depth, and Phalaris arundinacea were all positive predictors presence. (Table 1)thatsignificantly (p b 0.05) correlated with EFB presence (Table 2). The second supported model (ΔAIC = 0.12; Burnham and AIC ΔAIC Anderson, 2004) also included Phragmites australis as a positive predic- Site level tor of EFB presence (Table 1). At the plot-level, the AIC-selected model Established population (n = 102) included invasive Typha, Phragmites australis, and standing dead as pos- EFB presence ~ Invasive Typha + Phragmites (−) 89.44 0.00 itive predictor variables and meadow zone, fetch, and organic depth as Invasive Typha + Phragmites (−) + standing dead 90.72 1.28 negative predictor variables (Table 1). All positive and negative correla- NULL (intercept only) 97.06 7.62 tions were significant (p b 0.01; Table 2). Invading population (n = 419) EFB presence ~ Invasive Typha + standing dead + organic depth + 329.90 0.00 Munuscong Bay Typha removal study Phalaris Invasive Typha + standing dead + organic depth + 330.02 0.12 In our linear mixed effects model across 2017 and 2018 for our Phalaris + Phragmites harvest experiment we found significant effects of invasive Typha re- NULL (intercept only) 482.35 152.45 moval treatment but not year or the interaction of treatment and Plot level Established population (n = 3746) year on invasive Typha cover, EFB cover, standing dead vegetation, EFB presence ~ and total vegetation cover (Fig. 3; p = 0.005, p =0.041,p =0.030, Meadow zone (−) + invasive Typha + Emergent zone 3682.70 0.00 p =0.014,respectively).Inpairwisecomparisons,invasiveTypha − + standing dead ( )+Phragmites cover was significantly reduced in TyHarvBW treatments compared NULL (intercept only) 4276.50 593.80 Invading population (n = 12,901) to controls in both 2017 and 2018 (Fig. 3b; p = 0.001; p =0.003,re- EFB presence ~ spectively), as was EFB cover (Fig. 3a; p = 0.050; p = 0.036, respec- Invasive Typha + Meadow zone (−) + fetch (−)+ 1669.30 0.00 tively), standing dead vegetation (Fig. 3c; p = 0.041; p = 0.008, Phragmites + organic depth (−) + standing dead respectively), and total vegetation cover (Fig. 3d; p =0.007;p = NULL (intercept only) 2049.00 379.70 0.015, respectively).

Fig. 2. Distribution of Hydrocharis morsus-ranae (EFB) in the Laurentian Great Lakes during two sampling periods, 2011–2012 (a) and 2014–2015 (b). Many wetlands were not sampled in both 2011–2012 and 2014–2015, so locations are not identical between the two periods.

Multivariate analyses of plant communities one and two years Discussion after treatments showed a significant shift in vegetation. When considering both years' species community data in a This study sought to clarify the relationship of an emergent invasive, PERMANOVA, treatment effects led to a significant shift in vegeta- Typha, and a floating invader, EFB, across multiple scales in GLCWs. We tion community (F = 4.093, p = 0.01), while year and the interac- found evidence that not only are the two species associated, but that in- tion of treatment and year did not, so we analyzed plant vasive Typha may provide structural facilitation for EFB, most likely by community data together for both 2017 and 2018 datasets. In ameliorating common stressors in GL coastal wetlands, including pairwise PERMANOVA analyses, plant communities varied signifi- waves, wind, and seiches (Keough et al., 1999; Trebitz, 2006). cantly between TyHarvBW and control treatments (F = 6.853, p Our Great Lakes-wide analysis revealed that invasive Typha is an im- = 0.01), and TyHarvAW and TyHarvBW treatments (F = 4.777, p portant predictor of the presence of EFB across multiple spatial scales. In = 0.02). both established (Lake Ontario) and invading (all other Great Lakes and NMDS plots visually illustrate differences in plant community Great Lake connecting channels) populations at the site and plot level, assemblages between treatments in two-dimensional space across invasive Typha presence was the first or second factor in all AIC- both years (Fig. 4). Our NMDS showed a good fittothedata,with selected models (Table 1). astressof0.059(Clarke, 1993). Across both years, TyHarvBW Environmental variables in this study's models provide insights into treatments tended to diverge from control and TyHarvAW treat- EFB's niche in GLCWs. EFB requires standing water to persist, is naturally ments, while TyHarvAW treatments and controls tended to over- associated with emergent and submergent plant communities (Catling lap. Fitted vectors to the NMDS showed the significant vector for et al., 2003), and would be unlikely to occur in meadow zones with little % cover unvegetated correlated positively with TyHarvBW treat- to no standing water or in shallow water zones that are often ments, while control and TyHarvAW treatments were correlated dewatered. As such, wetland zonation appeared in both plot-level positively with % cover EFB and % cover total vegetation. Percent models with emergent zone positively predictive of EFB presence in cover invasive Typha and % cover standing dead also varied to- the established population and meadow zone negatively associated gether in the direction of TyHarvAW and control plots. with EFB in the invading and established populations (Table 1). Further,

Fig. 3. Results from facilitation experiment in Munuscong Bay showing mean percent areal coverage by year and treatment for: live Hydrocharis morsus-ranae (EFB; a), live invasive Typha (b), standing dead vegetation (c), and total of all live vegetation (d). Error bars represent standard error. Control = unmanipulated plots; TyHarvAW=abovewaterTypha harvest only; TyHarvBW = above water Typha harvest with subsequent below water cutting. Indicators of a statistically significant result in within-year pairwise comparisons between controls and treatments as determined by linear mixed effects models: * p b 0.05, ** p b 0.01, ***, p b 0.001. wind and wave exposure, as quantified by fetch (the farthest distance contrasting relationships between EFB, standing dead vegetation, and from the center of a wetland across open water, and a useful proxy for organic matter that may point to thresholds of EFB tolerance associated exposure to wind, waves, and seiche activity [Burton et al., 2004]) was with old and highly established invasive Typha. Standing dead cover had a negative predictor of EFB presence in the invading population. Because contrasting relationships with EFB; it was negatively associated with EFB is a free floating species, vulnerable to disturbances from wave and EFB at the plot-level in established populations (Lake Ontario) and pos- wind activity (Catling et al., 2003), it follows that more exposed wet- itively associated in established populations at the site-level and invad- lands, with greater fetch, would be less suitable habitat for EFB, and it ing populations in all cases (Table 1). Standing dead litter can provide adds additional support for the proposed mechanism of invasive important structure for EFB, protecting it from wind, wave, and seiche Typha facilitating EFB by providing physical shelter in high energy activity. However, beyond a certain cover threshold, dense standing GLCWs. dead material may exclude EFB by preventing adequate light penetra- Over time, Typha invasion is associated with organic sediment depo- tion to the water surface; EFB is vulnerable to shading levels above sition and increased detritus and standing dead cover (Lishawa et al., 70% (Zhu et al., 2014), which are common in the understory of 2013; Lishawa et al., 2014; Mitchell et al., 2011), which confers compet- established invasive Typha stands (Lishawa et al., 2015). In the well- itive dominance over native plants (Larkin et al., 2012; Vaccaro et al., established population of EFB (Lake Ontario) the negative relationship 2009). Our Great Lakes-wide models identify some interesting and between standing dead cover and EFB may be indicative of this

Fig. 4. Non-metric multidimensional scaling ordination of plant community data from 2017 and 2018 across treatments in Munuscong Bay. Points represent plant community data (percent cover of all species present) aggregated at the plot-level. Fitted vector arrows are significant (p b 0.05) with a length proportional to explanatory strength. Significant vectors are: Total_Veg (percent cover of live vegetation), R2 =0.85,p b 0.001; Unveg (percent cover unvegetated), R2 =0.85,p b 0.001; Standing_dead (percent cover standing dead vegetation), R2 =0.38,p = 0.027; Typha (percent cover invasive Typha), R2 =0.86,p b 0.001; and EFB (percent cover Hydrocharis morsus-ranae), R2 =0.60,p = 0.001. Control = unmanipulated plots; TyHarvAW = above water Typha harvest only; TyHarvBW = above water Typha harvest with subsequent below water cutting. threshold at the plot-level. At the site-level, however, wetlands contain- competitive exclusion or the tendency of Phragmites to grow in drier ing standing dead were positively associated with EFB presence, possi- and shallower conditions than Typha (Asaeda et al., 2005) which are un- bly due to the increased prevalence of standing dead material in sites suitable for EFB. It is also important to note that native emergent species invaded by Typha,(Mitchell et al., 2011), where less dense Typha stands in GLCWs have the potential to facilitate EFB populations by providing in the emergent zone may provide structural support for EFB (Table 1). structural support and shelter from wind, wave, and seiche activity in Organic soil depth had contrasting relationships with EFB in the invad- GLCWs. This study focused on the most abundant and dominant plants ing population, with a negative effect at the plot-level. In part, this may in the region, and thus did not directly test facilitative relationships be- be explained by the preference of EFB for the emergent and submergent tween EFB and native species, which merits further investigation. marsh zones, which tend to have shallower organic soils than the While results of Great Lakes-wide models reveal a close association meadow zone (Albert et al., 2005). In contrast, at the site-level, organic between invasive Typha and EFB, the facilitative relationship between soil depth was positively correlated with EFB, which may be due to the the two plants is further illuminated in the invasive Typha-removal ex- association of structure-providing invasive Typha with rapid accumula- periment. Invasive Typha was effectively removed and killed in the tion of organic matter (Lishawa et al., 2013; Mitchell et al., 2011). TyHarvBW treatments, where both Typha and EFB cover dropped pre- Interestingly, both Phragmites australis and Phalaris arundinacea,two cipitously (Fig. 3). The TyHarvAW treatments, however, did not reduce common invasive grasses in the Great Lakes, were also positively asso- invasive Typha or EFB cover. This is due to the fact that Typha,aperen- ciated with EFB in some cases of Great Lakes-wide modeling, although nial plant, has a robust system of underground rhizomes that can in fewer models and with lesser predictive strength than invasive allow the plant to rebound quickly from cutting (Keyport et al., 2018; Typha (Table 1). Both species share physical and ecological similarities Lishawa et al., 2015). Cutting below the water surface with sustained with invasive Typha: they are tall, perennial, rhizomatous graminoids flooding, however, severs the atmospheric connection between Typha that form dense, low-diversity clones (Zedler and Kercher, 2004)that stems and their underground rhizomes. Typha, like all plants, requires can provide structural support for EFB. However, Phragmites australis oxygen to metabolize sugars, and relies on a system of hollow plant tis- also appeared as a negative predictor of EFB presence in the established sue, called aerenchyma, to conduct oxygen down to rhizomes. population (Lake Ontario) at the site-level, which may be indicative of TyHarvBW cutting severed this connection and effectively killed plants,

Please cite this article as: A.M. Monks, S.C. Lishawa, K.C. Wellons, et al., European frogbit (Hydrocharis morsus-ranae) invasion facilitated by nonnative cattails (Typha) in the Laurentian Great Lakes..., Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2019.07.005 8 A.M. Monks et al. / Journal of Great Lakes Research xxx (xxxx) xxx leading to a more open vegetation structure than the pre-treatment implications for the early detection and rapid response to EFB in the emergent marsh (Lishawa et al., 2017). Creation of these openings Great Lakes. was accompanied by a drastic (five-fold) decrease in EFB coverage (Fig. 3a), as the plant was now exposed to wind and seiche activity in the treatment plots. This reduction was also accompanied by a reduc- Acknowledgements tion in standing dead material, which otherwise provides structural shelter for EFB plants and reproductive turions. The appearance of This study was made possible through financial support from the standing dead as a positive indicator in regression models mirrors the Michigan Department of Natural Resources Grants IS17-2006 and effects seen in the removal experiment, where EFB cover is higher in IS15-2003. Special thanks to B. Ohsowski for help with data analysis treatments containing higher standing dead cover, except for the and B. Carson, K. Berke, G. Habeeb, C. Rutkowski, D. Sugino, N. Spehn, TyHarvAW treatment in 2017 (Fig. 3). The negative impacts of standing M. Majszak, O. Niosi, M. O'Brien, and R. Belleville for help sampling in dead cover via shading or competitive exclusion were not tested in this the field. experiment due to EFB's co-dominance with invasive Typha at this site. NMDS results further emphasize the shift in vegetative community References from control to TyHarvBW, where the environmental vector “unvegetated” correlates with the TyHarvBW treatment, while EFB Albert, D.A., Crispin, S.R., Reese, G., Wilsmann, L.A., Ouwinga, S.J., 1987. A survey of Great Lakes marshes in Michigan's Upper Peninsula. Michigan Natural Features Inventory, cover, invasive Typha cover, and standing dead cover correlated with Lansing, Technical Report 73 (CZM Contract 9C-10). the plots containing EFB after treatment (Fig. 4; Control and Albert, D. A., Wilcox, D. A., Ingram, J., Thompson, T. A., 2005. Hydrogeomorphic classifica- TyHarvAW). NMDS vectors reflect important factors in the regression tion for Great Lakes coastal wetlands. J. Great Lakes Res., (Suppl. 1), 129-146. Altieri, A.H., Silliman, B.R., Bertness, M.D., 2007. Hierarchical organization via a facilitation models, with invasive Typha and EFB tending to vary together along cascade in intertidal cordgrass bed communities. Am. Nat. 169 (2), 195–206. with standing dead cover. Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of variance. The fact that EFB cover was lower over two years in TyHarvBW treat- Aust. J. Ecol. 26, 32–46. Anderson, M.J., Walsh, D.C.I., 2013. PERMANOVA, ANOSIM, and the mantel test in the face ments where invasive Typha had been removed suggests a facilitative of heterogeneous dispersions: what null hypothesis are you testing? Ecol. Monogr. relationship not unlike that of the rooted invasive plant, alligator 83, 557–574. weed (Alternanthera philoxeroides), and a secondary invader, the float- Asaeda, T., Fujino, T., Manatunge, J., 2005. Morphological adaptations of emergent plants fl ing plant, water hyacinth (Eichhornia crassipes). 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