Invasive species management method impacts restoration of understory plants in the presence of an herbivore: a case study of Amur honeysuckle (Lonicera maackii) and white-tailed deer

Management methods for invasive species may vary in their restoration success in the presence or absence of herbivores. We investigated the performance of understory plants after management of the invasive shrub, Lonicera maackii, using two herbicide-based methods (cut/paint and basal application) in fenced and unfenced plots. The cut/paint method resulted in the removal of above-ground stems, while the basal application resulted in the dead stems remaining in place. Light level in the cut/paint treatment was higher than in the basal application treatment, which was higher than in the control (no management) treatment. Across fencing treatments, fruit production, height and subsequent recruitment of transplanted Impatiens capensis were greater in the cut/paint treatment. Across management treatments, Impatiens capensis were taller in the fenced treatment. Native species richness was generally higher in the cut/paint and basal application treatments than in the control treatment. There were more I. capensis recruits, more I. capensis fruits and greater species richness in the cut/paint treatment than in the basal application treatment in fenced plots, but I. capensis plants performed similarly in these management treatments in unfenced plots. Thus standing dead stems of L. maackii offered some protection from damage in the presence of herbivores, offsetting the overall advantage of the cut/paint method seen in the fenced plots. There were more invasive Alliaria petiolata and more L. maackii seedlings in the cut/paint treatment than in the control treatment. Our results illustrate the complexities involved in selecting appropriate conservation management techniques given herbivore pressure and presence of multiple invasive species.

Forest restoration

Herbivory

Invasive plants

Invasive plants can have major impacts on native plant populations, communities, and ecosystems around the world (Sakai et al., 2001; Pimentel et al., 2005). Invasive species have been implicated as a major cause of endangerment and extinction of native species (Pimental et al., 2000). Once an invasive plant has become established in an ecosystem, conservation practitioners frequently seek to reduce populations of the invasive species through a variety of restoration methods, from mechanical to chemical (e.g., Carlson and Gorchov, 2004; Hartman and McCarthy, 2004; Milligan et al., 2004, Krueger-Mangold et al., 2006). In deciduous forests around the world, woodland herbs make up the majority of vascular plant species diversity (Whigham, 2004) and thus are often of conservation interest in these ecosystems (e.g., Drayton and Primack, 2006, Roy and de Blois, 2008). A major challenge to conservation of forest understory plants is browsing or other forms of damage by herbivores. Sweeney and Czapka (2004) suggest that protecting seedlings from herbivory should be given higher priority than protection from competition during restoration. In Midwestern and eastern forests in the United States, a primary herbivore threatening understory plants is the white-tailed deer, Odocoileus virginiana Zimmermann, which is considered a keystone herbivore due to its direct and indirect effects on both plants and animals (Rooney, 2001; Rooney and Waller, 2003; Cote et al., 2004). Herbivores may not only have direct impacts but may also have indirect impacts; for example, forest areas where O. virginiana had been excluded had lower numbers of invasive species (Webster et al., 2005), thus implicating deer in the spread of invasive plants.

Control of L. maackii is a major focus of natural resource agencies and conservation organizations in order to conserve forest communities. Due to these efforts, much information has been gained on how to effectively kill L. maackii in natural environments (Nyboer, 1992; Conover and Geiger, 1993; Hartman and McCarthy, 2004). Management techniques include the cut-and-paint, or cut/paint, method, where L. maackii is cut at the base and removed; herbicide is subsequently applied to the cut stump (McDonnell et al., 2005). Two other herbicide-based methods, the foliar spray method and the injection method (Conover and Geiger, 1993, Hartman and McCarthy, 2004, respectively), result in the killing of L. maackii with the dead stems left standing in place.

Standing dead stems of L. maackii could affect restoration success in a number of ways. Standing stems may continue to shade the understory, which may delay the development of plant communities for as long as stems remain standing. Lonicera maackii produces allelopathic compounds in its tissues (Trisel, 1997; Dorning and Cipollini, 2006; Cipollini et al., 2008a, c) and thus standing dead stems could continue to contribute allelochemicals to the understory until they decompose completely. In contrast, the presence of standing dead stems may have some positive effects, analogous to the protection from herbivory offered by so-called “nurse plants” (Garcia and Obeso, 2003, Bakker et al., 2004). There is some evidence that standing dead stems of L. maackii may provide protection of transplanted plants from deer browsing (Gorchov and Trisel, 2003), but this effect has not been quantified adequately. Hartman and McCarthy (2004) followed survival of transplanted tree seedlings after different methods of L. maackii management, but deer impact was insufficient to examine for protective effects. The response of the native herb community to the presence of standing dead stems has not been examined.

Another challenge to forest conservation is the response of invasive plants to restoration efforts (Loh and Daehler 2007). Although poorly replicated, McConnell et al. (2005) found an increase in species richness after management of L. maackii using the cut/paint method, but L. maackii seedlings and other invasive species also increased in abundance in the cut/paint treatment. Runkle et al. (2007) also found an increase in species richness eight years after removal of L. maackii; however, this increase was primarily the result in the increase of species with high dispersal ability, such as vines and other weedy species. Luken et al. (1997) found the vine Vitus vulpina responded positively to L. maackii management. No comparisons of the effects of honeysuckle management method on invasive plant responses have been published, but the presence of standing dead stems may slow the response of invasive plants.

The objectives of this study were to determine the effect of the presence or absence of standing dead L. maackii, the presence or absence of deer, and their interaction on understory plants. We followed the success of transplanted Impatiens capensis Meerb. (jewelweed), and transplanted Asarum canadense L. (wild ginger) in basal application and cut/paint management treatments. We also followed the natural recruitment of species in basal application, cut/paint and control treatments. We predicted that in the absence of deer, the cut/paint management method would best benefit plant performance, due to the increase in light and the removal of potentially allelopathic stem and leaf material. We predicted that in the presence of deer, the basal application method, which leaves the dead stems standing, would best benefit plant performance due to the protection conferred by the stems against deer damage.
2. Materials and Methods

We established experimental plots during the first week of April in 2005 in Hamilton County Park District’s Sharon Woods, located in Sharonville, Ohio, USA (39°16'40” N, 84°23'56”W). We chose two sites impacted by L. maackii approximately 0.75 km apart from each other. Each site is located in mixed oak-maple-ash forest community with a relatively large amount of L. maackii, yet still contained some degree of native understory vegetation. Deer density at Sharon Woods was approximately eight deer/km², which is the management goal at this site (J. Klein, Hamilton County Park District, personal communication). Within each site, we selected three subsites, with paired 8 x 6-m experimental plots at each subsite, for a total of 12 paired plots. Within each subsite, we used a split-split plot experimental design, with the split plot factor of deer exclusion and the split-split plot factor of L. maackii management method (see Fig. 1). We fenced one plot of each pair at each subsite, placing metal fence posts into the ground and attaching plastic deer fencing (1.8m-tall with five-cm mesh) to the posts. Within each paired plot (fenced and unfenced), we created eight 2x3 m subplots. For three of the adjacent subplots, we removed L. maackii using the cut/paint method, i.e. cutting off the L. maackii with a handsaw approximately 10 cm from the soil surface, removing the L. maackii, and painting the stump with the herbicide triclopyr (Pathfinder II, 13.6% triclopyr, Dow Agrosciences, Indianapolis, IN) to prevent resprouting. For three of the adjacent subplots, we removed L. maackii using the basal application method, i.e. applying triclopyr in a band around the entire circumference of the base of each stem. On subsequent visits, we controlled the minimal amount of living or sprouting L. maackii with the same method as the rest of the subplot. We did not remove any L. maackii in the remaining two adjacent subplots and these served as our controls. For two of the three management method subplots (i.e., basal application and cut/paint), one subplot was designated as the “transplant subplot” and one was designated as the “natural recruitment subplot” for further treatment and measurements. No further measurements were made on the third management method subplot.

On May 5, 2005, we transplanted four two-leaved rhizomes of the perennial A. canadense and six seedlings of the annual I. capensis into our “transplant subplots.” Transplants were collected locally. Asarum canadense is a shade-tolerant rhizomatous perennial that typically expands into a large clump through asexual reproduction. Asarum canadense has been shown to be impacted by L. maackii (Dorning, 2004), and appears to be largely resistant to deer browsing (D. Cipollini, personal observation). Plants were collected by first excavating rhizomes, which were often several internodes in length with a pair of leaves at each node. Single transplants, each containing one leaf pair, were then created by clipping the rhizome several cm on each side of a node. Impatiens capensis is an annual herb that is found in a range of light conditions, from forest clearings to closed woodlands (von Wettberg and Schmidt, 2005) and reproduces exclusively by seed. Impatiens capensis is sensitive to deer browsing (Williams et al., 2000; Asnani et al., 2006). Seedlings were transplanted from local populations when they were approximately 5-10 cm tall. Transplants were not placed in the control treatment, since we expected survival to be low (see Cipollini et al., 2008b). In 2005, we measured survival and fruit number of transplanted I. capensis on 2 June and 30 June, and both height and fruit number on 21 July. We measured survival and leaf number of each A. canadense clump on 25 April 2006 and 4 May 2007. On 4 May 2007, we measured the width of the largest leaf in each A. canadense clump.

In a 1-m² area of each of the transplant subplots (where I. capensis and A. canadense had been transplanted in 2005), we counted the number of seedlings of I. capensis on 26 April 2006 and on 24 April 2007. We were confident that most, if not all, of the seedlings of I. capensis were from fruits of plants that we had transplanted the previous year as there were almost no I. capensis in the plots except for the ones we transplanted. On 26 April 2006 and 24 April 2007, in one haphazardly-chosen control subplot and in both natural recruitment subplots, we counted the number of plants of each species in a 1-m² area of the subplot and species richness was determined. In all the subplots, we measured light levels at 1 m height on July 6 2006, which was a bright and mostly cloudless day (Li-Cor Quantum Sensor, Lincoln, NB). All light measurements were made within 65 min of each other.

For all analyses, we used a nested split-split plot Analysis of Variance (ANOVA) or Multivariate Analysis of Variance (MANOVA) with site as a fixed factor, subsite as the main plot factor (nested within site), fencing as the split plot factor and management method as the split-split plot factor (SAS, 1999). For MANOVAs, when significance was found using Wilk’s λ, separate univariate analyses of variance were performed on each separate date, followed by Tukey’s test to determine significance between treatment levels. We analyzed I. capensis fruit production in 2005 and number of seedlings in 2006-7, and number of A. canadense leaves using separate MANOVAs, with each date as a separate variable in the model (von Ende, 1993). We analyzed I. capensis height, I. capensis survival, A. canadense leaf width and A. canadense survival separately using ANOVA. We analyzed native species richness and number of A. petiolata plants using separate MANOVAs, using each date as a separate variable in the model. We analyzed number of L. maackii seedlings in spring 2007 using ANOVA. Data were transformed as necessary to meet model assumptions. For light levels, data could not be transformed to meet model assumptions of normality, and a Kruskal-Wallis Rank Sum test was then used. The α-level used for all tests was 0.05.
3. Results

Light levels were significantly affected by management treatment (F _{2, 76} = 47.10, p < 0.001); light levels in the cut/paint treatment was significantly higher than the light levels in the basal application treatment which were in turn significantly higher than the light levels in the control treatment (Fig. 2).

In the MANOVA for transplanted I. capensis fruit production across three dates, there was a significant effect of management treatment (F_3,42 = 4.19, p = 0.0111) and the interaction of fencing and management treatment (F_{3, 42} = 3.34, p = 0.0280). On 30 June, there were significantly more fruits on plants in the cut/paint treatment than on plants in the basal application treatment (F_1,44 = 11.77, p = 0.0013). On 30 June, there was a significant interaction between management method and fencing (F_1,44 = 9.58, p = 0.0034), with a more strongly positive effect of fencing on what fruit number for plants in the cut/paint treatment than for plants in the basal application treatment (Fig. 3). On 21 July 2007 transplanted I. capensis were significantly taller when they were fenced (F_1,3 = 10.25, p = 0.0493; Fig. 4). Likewise, plants were taller in the cut/paint treatment than in the basal application treatment on the same date (F_1,55 = 21.53, p < 0.0001; Fig. 4). There were no significant treatment effects on survival in the ANOVA.

In the MANOVA for the number of I. capensis seedlings, there was a significant effect of management method (F_2,9 = 4.86, p = 0.0370) and of the interaction of fencing and management method (F_2,9 = 9.09, p = 0.0069). In both years, there were more I. capensis seedlings in the cut/paint treatment than in the basal application treatment across fencing treatments (F_1,10 = 4.97, p = 0.0499 and F_1,10 = 10.58, p = 0.0087, respectively). In 2007, there was a significant interaction between fencing and management (F_1,10 = 7.91, p = 0.0184), with a more strongly positive effect of fencing on seedling number in the cut/paint treatment than in the basal application treatment. In basal application plots, seedling number was similar whether they were fenced or not (Fig. 5).

In the MANOVA for A. canadense leaf number, there were no significant treatment effects, yet the effect of management method approached significance (F_2,44 = 2.83, p = 0.070). We performed ANOVAs for each separate date to determine the nature of this non-significant trend. On 25 April 2006, there were leaves on plants in the basal application treatment (3.28 ± 0.27, mean ± SE) than in the cut/paint treatment (2.53 ± 0.15, mean ± SE; F_1,45 = 5.68, p = 0.0214). In the ANOVAs for A. canadense leaf width and survival, there were no significant effects.

In the MANOVA, species richness was significantly affected by management method (F_4,38 = 3.70, p = 0.0122) and by the interaction between fencing and management method (F_4,38 = 2.87, p = 0.0358). The effect of management method on species richness approached significance in 2006 (F_2,20 = 3.11, p = 0.0667) and was significant in 2007 (F_2,20 = 7.62, p = 0.0035), with greater richness in the cut/paint and basal application treatment compared to the control treatment (Fig. 6). The interaction of fencing and management was significant in 2007 (F_2,20 = 5.61, p = 0.0116). When fenced, species richness was higher in the cut/paint treatment than the basal application treatment. In contrast, when unfenced, there was similar to lower species richness in cut/paint treatment than in basal application treatment (Fig. 6).

There was a significant effect of management method on number of A. petiolata in the MANOVA (F_4,38 = 3.34, p = 0.0194). In both years, there were significantly more A. petiolata in cut/paint treatment than in control treatment, with the number of A. petiolata in basal application treatment intermediate between the two (F_{2, 20} = 4.29, p = 0.0282; F_{2, 20} = 4.99= 0.0174 respectively; Fig. 7). The effects of management method on L. maackii seedlings in 2007 were significant (F_{2, 20} = 4.11, p = 0.0319) and similar to the effects seen for A. petiolata (Fig. 8).
4. Discussion

When removing invasive species such as L. maackii, the management method should be carefully considered in light of the results of this study. Previous studies have found that L. maackii exerts strong aboveground effects on native species (Gorchov and Trisel, 2003; Miller and Gorchov, 2004; Cipollini et al., 2008b). Controlling L. maackii, whether using the cut/paint method or a method that leaves the dead stems in place, increases the light reaching the forest floor. We found that controlling L. maackii and leaving the dead stems in place did increase light levels over eight times of light levels in the control. In comparison, the cut/paint treatment increased light levels over 24 times of the light levels in the control. Smaller (~10 times) increases in light after L. maackii removal were reported in previous studies (Luken et al., 1997). Species richness increased in both the cut/paint and basal application methods. We found a benefit to I. capensis fruit production, height and recruitment by using the cut/paint method, likely due to the increased light intensity. However, alleviation of allelopathy by removal of L. maackii stems may have contributed to the beneficial effects of this treatment (Trisel, 1997; Dorning and Cipollini, 2006; Cipollini et al., 2008c). Regardless of mechanism, native plants benefited from control of L. maackii, with a trend for greater success using the cut/paint method.

Light conditions and allelopathy are not the only consideration during restoration, as deer can greatly impact restoration success (e.g., Ruhren and Handel, 2003, Sweeney and Czapka, 2004). Deer damage observed in this study included not only herbivory, but also physical damage by trampling. Although our fences excluded other herbivores aside from deer, we observed that deer were responsible for the majority of damage observed in unfenced plots. The density of deer at this site was high enough to have statistically significant main effects on I. capensis height only. Due to the nature of our statistical split-split plot design, small differences in the split-plot factor of fencing can not be easily detected (Neter et al., 1996). The experimental design does allow better detection of differences between the split-split plot factor of management method and its interaction with fencing, which was of primary interest in this study. We found that leaving the dead stems standing provided some protection from deer damage. This is inferred from the less positive effect of fencing on I. capensis fruit production and recruitment and native species richness in the basal application treatment than in the cut/paint treatment. For example, in plots protected from herbivores, I. capensis recruitment in 2007 was twice as high in cut/paint treatments compared to basal the basal application treatment. In plots exposed to herbivores, I. capensis recruitment was nearly identical in the two management treatments (Fig. 5). Thus, the general advantage of using the cut/paint treatment was not seen in the presence of deer. Interestingly, we found that species richness was higher in our unmanaged control plots when they were not fenced. However, the overall interaction of fencing and management method on species richness was significant even if the control treatment was removed from the statistical analysis. It is important to note that although differences in species richness were statistically significant, differences were small in scale, as illustrated in Fig. 6.

Despite a protective effect from deer, the benefit of using the basal application method in the presence of deer was not great enough to fully recommend its use over the cut/paint method in terms of benefits to native plant performance; in our study, even in unfenced plots, native plants generally performed better or the same with the cut/paint method. Due to deer management efforts, the deer density at our study site is only slightly above the carrying capacity of 4-6 deer/km² recommended from studies in Wisconsin and Illinois (Alverson et al., 1988; Anderson, 1994; Balgooyen and Waller, 1995). In areas where deer density is high, a method that leaves the dead stems standing may be more beneficial than the cut/paint method. Since dead stems start to fall after approximately 2-3 years (K. Cipollini, personal observation), it is unclear how long the protective effect will persist. At the very least, the short-term protection from deer damage allows time for a deer management program to be implemented before deer can impact restoration efforts after L. maackii control. Additionally, the costs of each management method in terms of labor and materials must be weighed during consideration of restoration strategy. Clearly, relying on dead stems for protection from herbivores is more cost effective than the installation of deer fencing, though admittedly the conservation benefits may be not as great. The injection method, which leaves the dead stems in place, is faster and therefore cheaper than the cut/paint method for larger stems (Hartman and McCarthy, 2004). Similarly, the foliar spray method is cost effective (T. Borgman, Hamilton County Park District, personal communication).

We found few treatment effects on A. canadense, which would be expected based on its relative resistance to deer damage and its shade tolerance. On the other hand, the study may have been too short to detect responses in this perennial species. We did find a trend for greater leaf number in the basal application treatment, which could be due to the propensity of this species to perform better in later successional habitats that have lower light levels (Damman and Cain, 1998). We found that A. canadense is a good candidate for restoration, as rhizome fragments are easy to collect and transplant and they survived (75% survival on average) and grew well (5 leaves on average after two years) during our study, consistent with the transplant success found by Mottl et al. (2006). Ruhren and Handel (2003) found that A. canadense had poor transplant success; since their transplants were grown from seed, they may have been much smaller than the rhizome fragments that we transplanted.

When L. maackii was controlled, the number of A. petiolata and L. maackii seedlings was significantly higher in the cut/paint compared to the control, with the basal application intermediate in number. Luken et al. (1997) found that one of the most important species in L. maackii thickets was A. petiolata, yet it did not respond positively to gap formation. Runkle et al. (2007) found a slight but significant increase in A. petiolata on one sampling date after L. maackii management. In comparison, we found strong responses of A. petiolata to L. maackii management, as there were seven times more A. petiolata plants in cut/paint treatments than in control treatments in the second year after L. maackii management. We also found increases in L. maackii seedlings with control of L. maackii, similar to the results of McConnell et al. (2005). Therefore, the benefits of using the cut/paint method are diminished when other invasive species are present.

Our results indicated that in determining the best method for restoration success, conservation practitioners need to take into account deer populations and the presence of other invasive species. The cut/paint method increases light and facilitates greater target plant performance but it can contribute to the reinvasion of other invasive species. The cut/paint method is not as successful when deer are present. Methods that leave the dead stems standing may provide temporary protection from browsing and may delay the expansion of invasive species, allowing native species to have higher growth, survival and reproduction. Our results indicate that there are differences between conservation management methods in successful understory restoration and that the management method, the effect of deer and the presence of invasive species must be weighed together in devising conservation strategies.

Acknowledgments

We thank the Hamilton County Park District for providing funding for this project and permission to perform the research at Sharon Woods. We thank Tom Borgman of the Hamilton County Park District in particular for all his assistance. We thank Jim Rosenberger for statistical advice. We thank Elizabeth Cipollini, Emmett Cipollini, Caitlin Combs, Georgette McClain, Rob Murphy, Jana Reser, Adam Roe and Yvonne Vadeboncoeur for assisting with field research. Doug Burks, Don Troike, Doug Woodmansee, and the WC students of BIO 440/441 provided valuable comments throughout this experiment.

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FIGURE LEGENDS

Fig. 1 – Diagram of experimental set-up of one paired plot. Fenced plots were fenced along the entire 8 x 6 m perimeter of the plot.

Fig. 5 - Mean (± SE) number of seedlings of I. capensis in 2006 and 2007 in fenced and unfenced treatments, with L. maackii removed using either the cut/paint method or the basal application method. Letters indicate significant differences between management treatments using Tukey’s test at p < 0.05. The effect of the interaction between fencing and management treatments on fruit number was significant in 2007 (p = 0.0184).

Fig. 8 - Mean (± SE) number of L. maackii seedlings in treatments where L. maackii was not removed and where L. maackii was removed using either the cut/paint method or the basal application method. Management treatments with different letters are significantly different from each other based on Tukey’s test at p < 0.05.