Cipollini and Schradin: Impacts of Ranunculus ficaria Guilty in the Court of Public Opinion: Testing Presumptive Impacts and Allelopathic Potential of Ranunculus ficaria Kendra A. Cipollini1 and Kelly D. Schradin
Wilmington College, Wilmington, Ohio 45177 Abstract.—Information about invasive species can be based primarily on anecdotal evidence, indicating the need for further information. Ranunculus ficaria is an ephemeral riparian plant species that is presumed invasive in the United States, despite the lack of any published information on its impacts. Mechanisms by which R. ficaria may affect native plant species include competition and allelopathy. We examined if R. ficaria negatively affected the growth and reproduction of the native Impatiens capensis and, if so, whether it is by allelopathy, nutrient competition or some combination thereof. We performed a fully-factorial field experiment in the field, manipulating the presence of R. ficaria, nutrients, and allelopathy with the use of activated carbon. The presence of R. ficaria tended to negatively affect survival of I. capensis. In the absence of carbon, R. ficaria significantly decreased seed production, illustrating the negative impact of R. ficaria. In the presence of carbon, there was no effect of R. ficaria, suggesting that carbon may have ameliorated the negative allelopathic effect of R. ficaria. Nutrient competition did not show strong effects. Despite its widespread identification as an invasive species, this is the first study to demonstrate the negative impact of R. ficaria on a native species and the possible role of allelopathy in its success. Further, the negative impacts of this ephemeral species persist well beyond its early growing season, which calls into question previous assumptions about R. ficaria exerting effects primarily on other ephemeral species.
Invasive species threaten biodiversity on a global scale (Wilcove et al., 1998; McGeoch et al., 2010) and are defined as those species that cause or have the potential to cause economic or environmental harm, weighed against their benefits (NISC, 2006). Most naturalized plants are introduced through the horticultural industry (Mack and Erneberg, 2002) and some can still be purchased in some instances despite their invasive status (Harris et al., 2009; Axtell et al., 2010). However, only a portion of naturalized species are actually categorized as invasive (Milbau and Stout, 2008). As a result, there is much interest in characterizing the species traits and introduction routes that make a species invasive (Lambdon et al., 2008; Milbau and Stout, 2008; van Kleunen et al., 2010). Yet, in many of these studies the methods by which species are identified as invasive are vague and based on expert opinion and anecdotal evidence, with little scientific evidence (Blossey, 1999). Further, even when there is some published information, the impacts of an invasive species can be overstated by the popular press (Lavoie, 2010), which may lead to inappropriate response strategies or undue focus. The lack of information on the impact of invasive species and on the possible mechanism of impact is an obstacle to effectively prioritizing the control of invasive species during a time of dwindling resources.
Invasive plant species can negatively impact native species through a variety of mechanisms (Levine et al., 2003). Invasive species can simply outcompete native species for above- and/or below-ground resources (e.g., Kueffer et al., 2007; Cipollini et al., 2008a; Galbraith-Kent and Handel, 2008). Enhanced nutrient acquisition can lead to invasive species success. For example, Centaurea maculosa acquired more phosphorus than surrounding native species which may have increased competitive success (Thorpe et al., 2006). Additionally, Leishman and Thomson (2005) found that invasive species had greater responses to nutrient addition than native species, thus outcompeting the natives in nutrient-rich environments. Another mechanism by which invasive species affect native communities is allelopathy (Hierro and Callaway, 2003; Ens et al. 2009). Most plants produce secondary compounds (Ehrenfeld, 2006) that can affect an adjacent plant either directly (Cipollini et al., 2008b) or indirectly through changing soil ecology (Stinson et al., 2006; Mangla et al., 2008). Some allelopathic chemicals that have no negative impact in their native environment may have negative effects in an invaded community, a mechanism coined the “novel weapons hypothesis” (Callaway and Aschehoug, 2000; Callaway and Ridenour, 2004; Callaway et al., 2008; Thorpe et al., 2009).
Discovering impacts due to allelopathy can be done with careful experimentation (Inderjit and Callaway, 2003). Allelopathic effects have been studied using activated carbon (e.g., Ridenhour and Callaway, 2001; Cipollini et al., 2008a). Activated carbon adsorbs organic compounds, including allelochemicals (Ridenour and Callaway, 2001). Addition of carbon can also has effects on soil properties and plant growth in potting soil (Lau et al., 2008; Weisshuhn and Prati, 2009). Addition of nutrients is thought to help ameliorate any fertilizing effects of the addition of activated carbon (Inderjit and Callaway, 2003). Activated carbon may also serve as a restoration tool to change soil conditions in invaded soils (Kulmatiski and Beard, 2006; Kulmatiski, 2010).
Ranunculus ficaria L. (Ranunculaceae), or lesser celandine, is a groundcover, native to Europe (Taylor and Markham, 1978; Sell, 1994), which appears to be affecting native plants in forested floodplains in many US states (Swearingen 2005). There are five known subspecies, all of which are found in the United States (Post et al., 2009). Ranunculus ficaria was first recorded naturalized in the United States in 1867 (Axtell et al., 2010). As it is still being marketed by the nursery industry (Axtell et al., 2010), it was likely imported for horticultural purposes. It was recognized as a naturalized species in the Midwest in the 1980’s (Rabeler and Crowder, 1985) and in southern states more recently (Krings et al., 2005, Nesom, 2008). Ranunculus ficaria is currently documented in at least 21 US states, the District of Columbia, and 4 Canadian provinces (USDA, 2010). It has been identified as invasive in 9 states and the District of Columbia and is banned in Massachusetts and Connecticut as a noxious weed (Axtel et al., 2010).
Ranunculus ficaria emerges before most native spring species, which may provide it with a competitive advantage. Once established, it spreads rapidly across the forest floor to form a dense monoculture, which native species seemingly cannot penetrate (Swearingen, 2005). Hammerschlag et al. (2002) reported that R. ficaria created a monoculture in the Rock Creek floodplain in Washington, DC and few native species re-colonized after its removal. It is thought that R. ficaria, as a spring ephemeral, has impacts primarily on other spring ephemerals (Swearingen, 2005). However, most all information on R. ficaria as an invasive species is primarily anecdotal in nature. Unpublished and preliminary data indicate that presence of R. ficaria is associated with reduced abundance and richness of native species (Hohman, 2005). Ranunculus ficaria exhibits direct allelopathic effects on germination of some native species (Cipollini, unpublished data), indicating that R. ficaria may have negative effects beyond the spring time period through lingering allelopathic effects.
For our study, we examined if R. ficaria negatively affects the growth and reproduction of the native annual Impatiens capensis and, if so, whether it is by allelopathy, nutrient competition or some combination thereof. In the field we performed a fully-factorial experiment with the treatments of R. ficaria (present and absent), carbon (present and absent), and nutrient addition (present and absent). We expected that the presence of R. ficaria would have an overall negative impact, that addition of nutrients would have an overall positive impact and that addition of carbon would have no overall effect on the performance of I. capensis. If allelopathy were important, we expected to see a significant carbon by R. ficaria interaction and, if nutrient competition were important, we expected to see a significant nutrient by R. ficaria interaction on I. capensis response variables.
We performed the study in 2009 at Hamilton County Park District’s Winton Woods in Cincinnati, Ohio in an area invaded by R. ficaria ssp. bulbifer, a subspecies that forms asexual bulbils (Post et al., 2009). The study area was found in a floodplain along Westfork Mill Creek. We set up the experiment on 24 April, choosing an area with a uniform coverage of R. ficaria. We fenced the entire site using deer fencing to prevent trampling and/or herbivory. We used a fully factorial design with the main factors of: presence/absence of R. ficaria, presence/absence of activated carbon and presence/absence of additional nutrients, replicated 8 times (2 R. ficaria levels x 2 carbon levels x 2 nutrient levels x 8 replicates = 64 experimental units). The treatment combinations were haphazardly assigned to each plot and each plot was located approximately 25 cm apart. We tested the effects of these treatment combinations on the target plant Impatiens capensis Meerb., jewelweed (Balsaminaceae). We chose I. capensis because of the overlap in habitat and distribution with R. ficaria. Another advantage is that reproduction can be measured in this annual species. Additionally, I. capensis has served as a model organism in previous studies of invasive species effects (e.g., Cipollini et al., 2008a; Cipollini et al., 2009; Cipollini and Hurley, 2009). All I. capensis seedlings were obtained in an immediately adjacent area free of R. ficaria.
In the R. ficaria-present treatments, we removed R. ficaria and planted them back in place while transplanting I. capensis seedlings. In R. ficaria-absent treatments, we removed the R. ficaria completely before transplanting I. capensis. In activated carbon-present treatments, we worked 10 ml of activated carbon (Aquarium Pharmaceuticals Black Magic Activated Carbon, Chalfont, Pennsylvania) into the top 8 cm of soil of each plot. This ratio of activated carbon to soil volume has been shown to mitigate allelopathic effects in previous research (Cipollini et al., 2008a; Ridenour and Callaway, 2001). In nutrient-addition treatments, we worked the manufacturer-recommended amount of 1.5 teaspoons of slow-release fertilizer (Scotts Osmocote, Scotts-Sierra Horticultural Product Co., Marysville, Ohio) into the top 8 cm of soil in each plot. We disturbed the soil in each subplot regardless of treatment combination to control for soil disturbance effects. On May 1 we replaced any I. capensistransplants that did not survive, presumably due to transplant shock. We measured the height of each seedling when transplanted. The number of fruits, number of seeds and survival (days to death) of the seedlings were recorded once each week. Height and stem diameter (measured directly beneath bottom node with a digital caliper) was measured. Ranunculus ficaria had lost all of its foliage by 2 June (week 6) and the leaf litter had decomposed by 12 June (week 8), leaving the bulbils exposed on the soil surface. Measurements began on 5 May and ended on 28 August (week 18).
We performed a series of Analysis of Variances (ANOVAs) on the I. capensis response variables, using the full model with fixed factors of nutrients (+/-), R. ficaria (+/-) and carbon (+/-). We were unable to include all of the variables in a single MANOVA model due to the missing values generated as plants died. For survival, we analyzed the number of days to death for all plants. For total number of seeds, we included starting height as a significant covariate. We removed those plants that had died within 8 weeks of transplant, as seed production was essentially non-existent up to that time. For final height and stem diameter, we used a MANOVA with starting height as a significant covariate for the 32 surviving plants. When significance was found in the MANOVA using Wilk’s λ, we ran separate univariate Analyses of Variance (ANOVAs) for each variable. For all statistical tests, model assumptions of normality and heteroskedasticity were verified prior to analysis and transformed where appropriate.
For survival, there was a near-significant effect of R. ficaria (F1,55 = 3.75, p = 0.058), with I. capensis tending to die sooner when R. ficaria was present (Fig. 1). For the total number of seeds produced, there was a significant effect of nutrients (F1,47 = 20.53, p < 0.001) and a significant interactive effect between R. ficaria-presence and carbon (F1,47 = 5.03, p = 0.030). The presence of nutrients nearly tripled seed production (Fig. 2). When carbon was absent, the presence of R. ficaria reduced seed production. When carbon was present, seed production was similar whether R. ficaria was present or absent (Fig. 3). In the MANOVA, there was a significant effect of nutrients on final height and stem diameter (F2, 22 = 14.904, p = 0.000). In the univariate ANOVA, nutrients increased both height (F1, 23 = 7.28, p = 0.013) and stem diameter (F1, 31 = 30.34, p < 0.001) (Fig. 2).
We wanted to know if the putative invasive R. ficaria negatively affected the growth and reproduction of the native I. capensis, and if it did, whether allelopathy or nutrient competition played a causative role. Because R. ficaria has been identified as invasive (Axtell et al., 2010) and has been associated with reduced native abundance and diversity (Homann, 2005), we expected that the presence of R. ficaria would have a negative impact on the performance of I. capensis. Our results show that R. ficaria does indeed negatively affect I. capensis providing confirmatory evidence of its assumed impact on native species. Ranunculus ficaria showed a tendency to have a negative overall impact on the survival of I. capensis with plants dying ~10 days earlier in the presence of R. ficaria. In the absence of carbon, R. ficaria decreased seed production by ~50%. As expected, nutrients showed a significant effect on growth (in terms of height and stem diameter) and seed production. If nutrient competition were a key factor in inhibition of I. capensis by R. ficaria, we would have expected I. capensis to exhibit a release from competition in the presence of added nutrients. There was no significant interaction between nutrient addition and presence of R. ficaria, suggesting that nutrient competition was most likely not the primary mechanism of impact of R. ficaria. We do however acknowledge that our study does not rule out other forms of resource competition, such as competition for light or water.
In the presence of carbon, there was no effect of R. ficaria; carbon therefore ameliorated the negative effect of R. ficaria on I. capensis. In previous research, application of carbon to soils has mitigated the effects of invasive species (Cipollini et al., 2008a; Ridenour and Callaway, 2001). Ridenour and Callaway (2001) found that the competitive ability of Eurasian grass species was greatly reduced by activated carbon and suggested that the advantage of this species, at least in part, was due to allelopathy. Similarly, one possible conclusion from our study is that the addition of carbon may have attenuated the allelopathic effect of R. ficaria. However, when using activated carbon as an experimental tool to test allelopathy, caution must be used in interpreting results. The addition of activated carbon itself can change soil conditions in potting soil (Lau et al., 2008; Weisshuhn and Prati, 2009), though it is important to note that these studies used twice as much activated carbon compared to the amount used in our study. Activated carbon itself can have a direct fertilizing effect (Lau et al., 2008). In our study, the mitigating effect of carbon was significant even in nutrient-addition treatments, suggesting that direct addition of nutrients by the activated carbon was most likely not the mechanism through which carbon exerted its effects. Ranunculus ficaria is purported to have medicinal uses in herbal medicine as a treatment for hemorrhoids and as an astringent (Chevallier, 1996) and contains a number of secondary chemicals (Texier et al., 1984; Tomcysk et al., 2002). The presence of secondary compounds may be a good predictor of invasive species impacts, including allelopathy (Ehrenfeld, 2006). Further, because R. ficaria exhibits direct allelopathy on some species in the laboratory and greenhouse (Cipollini, unpublished data), allelopathy is a likely mechanism in the field, though clearly further study is needed (see Blair et al., 2009). Whatever the exact mechanism of its effect, activated carbon nevertheless was clearly able to negate the negative effect of R. ficaria, suggesting that, at the very least, it may serve as an effective restoration tool to modify soil conditions in the field to the benefit of native species (Kulmataski and Beard, 2006; Kulmatiski, 2010),.
Interestingly, we found that R. ficaria had lasting effects beyond its brief growing season. We expected that effects on I. capensis would not be particularly strong, as it is thought that the negative effects of this species are exerted primarily on spring ephemeral species (Swearingen, 2005). Further studies using spring ephemeral species are obviously needed to clarify the comparative effect on this set of species presumed most sensitive. Even though R. ficaria had completely senesced by week 6 of the experiment, it still significantly negatively impacted I. capensis, which lived without the presence of R. ficaria for about two-thirds of its life span. Other invasive species can have residual effects on native species, even after the removal of the invasive species (Conser and Conner, 2009). The effect of R. ficaria well past its growing season may be due to lingering effects, such as those due to allelochemicals or to other modification of soil conditions. An alternative explanation may be that the seedling stage is the most vulnerable stage of I. capensis, similar to the findings in Barto et al. (2010).
This is the first study to show the negative impact of R. ficaria on I. capensis and to point towards a possible mechanism of success – allelopathy or other modification of soil conditions. It is surprising that this is the first published study to investigate the invasive potential of R. ficaria, given that natural resource agencies have recognized it as a species important to control in natural areas since at least the year 2000 (Hammerschlag et al., 2002). Ranunculus ficaria has already been banned in two states (Axtell et al., 2010) since the year 2006. Admittedly, there is a balance between taking immediate action against an invasive species and waiting for time-consuming scientific studies (Blossey, 1999). Indeed, we support the use of the “precautionary principle” (e.g., Blossey, 2001) in assessing invasive species. Since R. ficaria can form dense monocultures, the assumption that it is an invasive species is most likely a valid one. However, in the ten or more years it has been identified as a concern, there is not a single published paper documenting its impact. It is entirely possible that the impact of R. ficaria has been overblown in the eyes of the public (Lavoie, 2010), causing larger-than-needed economic losses to the horticultural industry and redirection of resources away from more important invaders. This research provides an example of the need for more basic research into invasive species impacts and mechanisms of impacts on native species for use in effective invasive species targeting, control and management.
Acknowledgments.—We would like to thank Kyle Titus and Sara Moore for assisting in field research. We also thank Doug Burks, Don Troike, and Doug Woodmansee who provided guidance throughout this project. We thank Don Cipollini for his insight and support. We thank the Hamilton County Park District for providing funding for this project and Tom Borgman in particular for all his assistance. We are especially thankful for their understanding when the first experiment was destroyed by flooding.
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Figure captions Fig. 1─Mean (± SE) life span of Impatiens capensis grown with and without Ranunculus ficaria, across nutrient and carbon treatments
Fig. 2─Mean (± SE) number of seeds, height and stem diameter of Impatiens capensis grown with and without nutrients, across Ranunculus ficaria and carbon treatments.
Fig. 3─Mean (± SE) number of seeds for Impatiens capensis grown with and without Ranunuculus ficaria in the presence and absence of carbon, across nutrient treatments