2012 NORTHEASTERN NATURALIST 19(2):267–278 Managing Marginal Populations of the Rare Wetland Plant Trollius laxus Salisbury (Spreading Globeflower): Consideration of Light Levels, Herbivory, and Pollination Kristina N. Jones1,* and Susan M. Klemetti1,2 Abstract - To address the question of how succession in protected habitats might be managed to favor rare understory plants in the Northeast, this study examined whether reducing shade might have negative impacts via increased herbivory or reduced pollination. We studied marginal populations of Trollius laxus Salisbury (Spreading Globeflower), a rare herbaceous plant of calcareous wetlands, making observations of natural variation in one population, and experimentally cutting back herbaceous neighboring plants in another. In a Trollius population under a mixed canopy, we quantified natural light levels at each plant and tested for correlations with measures of reproduction and herbivory. Flowering and fruit production were positively correlated with light level in one of the two years measured, while herbivore damage and plant growth were uncorrelated with light level. In another study population, where the woody canopy had been removed previously, experimental clipping of herbaceous neighbors did not increase herbivore damage to T. laxus, nor did it decrease flowering or fruit production. Also, the few potential pollinators observed were all small insects unlikely to be negatively affected by increased light. Our results suggest that management to reduce shade in these marginal T. laxus populations is unlikely to have a negative impact on these rare plants via their herbivores and pollinators. Introduction Habitat protection is a critical step towards conservation of rare species; however, it has become increasingly clear that this act alone is not sufficient for the long-term persistence of many species (Heywood and Iriondo 2003). With the suppression of disturbances such as fires and floods, species adapted to habitats formerly prone to these disturbances may be at risk. Even protected habitats often need active management of disturbance and succession to enable the persistence of rare species (Hobbs and Huenneke 1992, Oostermeijer 2003, Scanga 2009). Given the complexity of most biological communities, it can be difficult to predict whether the net effect on a target species will be positive or negative, yet management decisions often must be made before specific information on likely impacts is available. Studies of responses to management practices such as canopy thinning are urgently needed to inform these practices in a range of habitats. Trollius laxus Salisbury (Spreading Globeflower) is an early- to mid-successional plant species, which generally competes poorly with larger herbaceous and 1Department of Biological Sciences, Wellesley College, 106 Central Street, Wellesley, MA 02481. 2Current address - Department of Sociology and Anthropology, Denison University, Granville, OH 43023. *Corresponding author - kjones@wellesley.edu. 268 Northeastern Naturalist Vol. 19, No. 2 woody species (Mitchell and Sheviak 1981). It is a globally rare species found only in the northeastern United States, where it is the sole representative of its genus (Parfitt 1997). Despite growing well in cultivation under unspecialized garden conditions (K. Jones, pers. observ.), T. laxus is restricted in the wild to wetlands with cold, alkaline groundwater discharge (Bliss 1985, Jones 2001). Habitat destruction is primarily responsible for the overall decline of T. laxus over the last century (NatureServe 2008), but even within protected areas several populations have continued to dwindle, especially at the edges of the species’ range (Jones 2001). Thus, in many cases, it appears that active management is required to prevent local extirpation of this species. Current management practices at T. laxus sites primarily involve canopy manipulation to increase light, along with control of invasive species (Jones 2001, Scanga 2009). Previous studies have shown that T. laxus generally responds positively to decreasing shade (Leimanis 1994, Zielinski 1993), except perhaps in conditions with low water availability (Rhinehalt 1990). In a definitive multi-year study of canopy manipulation on scattered subpopulations of a robust T. laxus population in New York, T. laxus performance initially increased following experimental canopy gap formation and then declined over time (Scanga 2009). Other understory plant species also may respond to higher light conditions, so the net effect of canopy thinning or removal on Trollius populations is likely to depend at least in part on interactions such as competition with other species (Scanga 2009). Management practices also may affect herbivores and pollinators of Trollius. In general, insects may be more frequent and/or more active in the sun and at warmer temperatures than in the shade. For example, caterpillars have been shown to eat more in warmer temperatures (Levesque et al. 2002). Removal of shade greatly increased insect herbivory on Cardamine cordifolia A. Gray (Heartleaf Bittercress), and there is evidence that this plant species is restricted to shade by herbivory (Louda and Rodman 1996). Higher light levels in canopy gaps also have been correlated with higher mammalian herbivory (Maschinski et al. 1997). Also, stem elongation in response to light competition may make some plants more palatable to herbivores (e.g., Cipollini and Bergelson 2002, Kurashige and Agrawal 2005). On the other hand, plants in high light may have more chemical or physical defenses than those growing in lower light (Henriksson et al. 2003, Wang and Lincoln 2004) or may be able to tolerate defoliation better under high-light conditions (Baraza et al. 2004, Gleason and Ares 2004). Evaluation of canopy manipulation as a management tool for plant populations should include consideration of its impacts on herbivory. Management to increase light should have more predictable effects on pollinators, especially insects, as greater activity is generally beneficial to the plants. Rare plants often have difficulty attracting and supporting pollinators, especially if flowering is sparse (Dauber et al. 2010, Kunin 1993). In early spring, when Trollius laxus blooms, the energetics of insect foraging are generally more favorable under warmer conditions (Heinrich 1979). Flowers receiving direct sun for longer periods may be more attractive if emission of attractive scent volatiles is 2012 K.N. Jones and S.M. Klemetti 269 correlated with flower temperature (e.g., Sagae et al. 2008), and pollinators may be capable of flying longer distances upon leaving warm flowers than cool ones (Heinrich 1979). Identifying pollinators is the first step toward determining how light manipulations are likely to influence pollination for a rare plant. This study examined implications for herbivory and pollination of Trollius laxus due to management practices to increase light in marginal populations at the eastern edge of the species’ range. Specifically, we tested for correlations between light and herbivory levels, as well as plant growth and reproduction, in a population with naturally variable canopy cover; evaluated the effects of clipping herbaceous neighbors on T. laxus growth, reproduction, and herbivory in a population whose woody canopy had been removed; and identified insect visitors that seemed likely to serve as effective pollinators for T. laxus flowers in these populations. Methods Species description Trollius laxus (Spreading Globeflower) is an herbaceous perennial with longpetioled basal leaves atop thick, fibrous roots (Fig.1). One or more stems, each with a terminal flower, continue to elongate as the flower and fruit mature. The flowers are quite showy, up to 5 cm in diameter, with five to seven cream or pale yellow petaloid sepals. The actual petals are much reduced (staminodes), with nectar glands at the base (Parfitt 1997). The plants are among the first species to emerge and flower in spring, typically from mid-April through early May in Connecticut. Figure 1. Trollius laxus not quite in bloom in an experimental plot with herbaceous neighbors clipped short, at the Sharon, CT study site. 270 Northeastern Naturalist Vol. 19, No. 2 The seeds ripen by mid-June and are believed to be dispersed passively by gravity plus wind, rain, and seasonally high water (Parsons and Yates 1984). Field-site description There are six known extant populations of T. laxus in New England, all of them in Litchfield County, CT at the eastern edge of the species’ range (Brumback et al. 1996). The center of the species’ range, in central New York state, has much larger populations with more robust plants. All of the Connecticut populations have declined in the last hundred years, in most cases despite protection of the immediate habitat, and almost all currently have fewer than 100 plants; three additional Connecticut occurrences documented in the early 1900s have since become extirpated (Jones 2001). Of the existing populations, three have a woody canopy cover and three do not have a canopy (including a cemetery and a power line right-of-way). We chose one population of each type, each with at least 50 T. laxus plants, for this study. Both populations are within 10 m of a pond edge and frequently include areas of standing water, particularly in spring. The population with a canopy is in the town of Canaan, and the open site is in Sharon. Confidentiality of the exact locations is mandated by the Connecticut Department of Environmental Protection. Observations under natural canopy At the Canaan site, we monitored 70 T. laxus plants in two adjacent seeps over the 2002 and 2003 growing seasons. The mixed coniferous and broadleaf canopy varied considerably over the site. We tested for correlations between light levels and measures of plant growth and reproduction as well as damage due to herbivory. There were eight additional plants present in 2002 that did not reappear in 2003, and several seedlings that appeared in 2003, but the 70 monitored plants were all that were present in both years at this site. Herbivory levels were low overall in 2003, so we returned the following spring to measure herbivory in 2004 on the same 70 plants. For each plant, we counted the number of basal leaves (representative of plant size), flowers, and developed carpels. The number of expanded carpels served as a nondestructive proxy for seed set; similar-sized plants in CT averaged 5.5 seeds per developed carpel (Zielinski 1993), and the number of developed carpels per flower was quite variable (range = 0 to 16 at the Canaan site). Leaf damage due to herbivory was assigned an index, ranging from 0 (no damage) to 3 (more than 50% of leaf tissue missing), through the month of May each year. We measured the amount of photosynthetically active radiation (PAR, in mmol m-2 s-1) reaching each of the 70 plants on 7 May 2003 at approximately midday (1200 h) and midafternoon (1430 h), using an EMS-7 Canopy Transmission Meter (PP Systems, Haverhill, MA). Light levels varied dramatically, from plants experiencing direct sun at noon (930 mmol m-2 s-1) to one mostly covered by Symplocarpus foetidus (L.) Salisb. ex W.P.C. Barton (Skunk Cabbage) leaves, and others under multiple canopy layers (mean PAR measured was 247, range = 12–930 mmol m-2 s-1). This measured variation most likely overestimated variation among the plants in total PAR received as sun flecks moved across the understory over the course 2012 K.N. Jones and S.M. Klemetti 271 of a day. Therefore, we used nonparametric correlations to compare the rank orders rather than actual values of these data. Spearman’s rank correlations tested whether plants receiving more light also had more herbivore damage, flowers, or developed carpels, or a greater increase in number of leaves from 2002 to 2003. All data analyses were performed using JMP 7.0 (SAS Institute 2007). Experimental clipping of herbaceous neighbors The site with no woody canopy (Sharon) had been cut with a weed trimmer once a year in the fall or early spring for at least four years prior to this study, maintaining it as a small wet meadow at the edge of a pond. Following Castor canadensis Kuhl (Beaver) disturbance to the area in 2001, the site was fenced to keep out large mammals. We divided the fenced area into 1-m2 plots, 13 of which contained T. laxus plants, with an average of 4.7 Trollius and a range of 1–18 plants per plot. Plots were randomly assigned either to have all non- Trollius vegetation within the plot hand clipped to approximately 3 cm above soil level (7 plots; see Fig. 1), or to remain unclipped (6 plots). Plots were clipped at the earliest date after the T. laxus plants had emerged and expanded their leaves, on 19 April 2002 and 27 April 2003, while “unclipped” plots on the same days had the vegetation handled but not clipped, so that all plots had similar amounts of trampling and disturbance aside from the actual clipping. Herbivory was quantified in 2002 and 2003 using the same index as in the observational study. Change in leaf number between years again served as a measure of growth. Because T. laxus blooms immediately after emergence, using resources stored from previous growing seasons, we tested for effects of clipping on flowering and carpel development the following year after clipping (2003 and 2004). Plots rather than individual plants were the experimental units; therefore values per plant were averaged to yield one data point per plot for each of the response variables. Two-tailed t-tests were used to evaluate whether response variables (number of flowers, number of developed carpels, level of herbivore damage, change in leaf number) in clipped and unclipped plots were the same. Pollination While performing weekly surveys of herbivory and flowering in April and May of 2002 and 2003, we noted any potential pollinators visiting T. laxus flowers. With so few flowers in the populations (the 70 plants at the Canaan site had a combined total of 32 flowers over the 2002 blooming season and 47 in 2003, and the Sharon site had only nine flowers in 2002 and 47 in 2003), there was not enough pollinator activity to warrant pollinator behavior observations, but we did observe a few small bees, flies, and ants in the flowers, and captured and identifi ed a sample of them. Results Observations under natural canopy We found no significant correlations between herbivore damage and natural light levels (PAR) at each plant’s location within the Canaan site (Table 1, Fig. 2). 272 Northeastern Naturalist Vol. 19, No. 2 There was a weakly positive correlation between light levels and the number of flowers per plant, and between light and the number of developed carpels in 2002 (Table 1, Fig. 3). In 2003, the only significant correlation between light levels and Table 1. Spearman rank correlations (r) between May light levels (PAR received at the location of each T. laxus plant at 1200 h and 1430 h, and the mean of these two values) and numbers of flowers and developed carpels per plant, growth in leaf number from one year to the next, and levels of herbivory. * indicates significant correlation at 0.01 < P < 0.05. # flowers # carpels Growth Herbivory 2002 2003 2002 2003 2002–03 2002 2003 2004 PAR 1200 h 0.262* 0.164 0.244* -0.033 0.007 -0.077 -0.133 -0.004 PAR 1430h 0.294* 0.261* 0.234* 0.173 0.064 -0.102 0.016 0.044 PAR mean 0.273* 0.198 0.257* 0.002 0.028 -0.092 -0.122 -0.002 Figure 2. Relationships between amount of herbivore damage and light levels (PAR, in mmol m-2 s-1) measured at each plant under a mixed canopy, in years of relatively high (2002) and low (2003) herbivore damage. Neither correlation is significantly different from zero. 2012 K.N. Jones and S.M. Klemetti 273 measures of reproduction was a weakly positive one between PAR at 1430 h and number of flowers per plant (Table 1). Growth in leaf number from 2002 to 2003 was uncorrelated with light levels (Table 1). Experimental clipping of herbaceous neighbors The increased exposure of T. laxus plants in plots where neighboring vegetation was clipped had no negative effects on any of the measured response variables (Table 2). Sample sizes were too small to detect significant effects, but all measures of growth and reproduction, but not herbivory, had larger average values in clipped plots than in unclipped plots in both years. Trollius plants in plots clipped in 2002 emerged significantly earlier in 2003 (by 2.7 days; t = 2.31, P = 0.042) than did the Trollius in unclipped plots. Figure 3. Relationships between components of r e p r o d u c t i o n (A: number of flowers per plant; B: number of developed carpels per plant) and light levels (PAR, in mmol m-2 s-1) measured at each plant under a mixed canopy. The line in each graph represents the best linear fit for these signifi- cantly positive correlations. 274 Northeastern Naturalist Vol. 19, No. 2 Pollination Visits by potential pollinators to T. laxus flowers at the two sites were rare, but we did capture a few, including two kinds of bees and a fly that may be effective pollinators. These were: a Sweat bee—Lasioglossum (Dialictus) sp. female with pollen in her scopa (family Halictidae); a Cuckoo bee—Nomada sp. female (family Apidae), and a fly in the family Tachinidae—a parasitic fly with long mouthparts that probably feeds on nectar as an adult. There were also several unidentified ants, only one of which had any Trollius pollen (a single grain) on its body. Discussion The primary concern motivating this study was that management to increase light in marginal Trollius laxus populations may have some detrimental effects on these rare plants, primarily via increased herbivory. Increasing light by cutting back woody or herbaceous competitors may have the unintended consequence of making Trollius plants more apparent to herbivores, or of creating abiotic conditions more favorable to herbivore activity. However, our results do not substantiate these concerns, at least for the two populations studied. There was no correlation between light and herbivory levels in the population under a variable woody canopy, and herbivory was not greater in plots where all non-Trollius herbaceous plants were clipped short, compared to unclipped plots. There was considerably more leaf damage in 2002 and 2004 than in 2003, but whether herbivory levels were high or low, there was no relationship to light levels under the natural canopy at the Canaan site in any of the three years. We did not observe much herbivore activity, despite spending over 100 hours in these populations. Either herbivores were active mostly from dusk to dawn, or our presence suppressed their activity. Although nocturnal activity seems unlikely to depend on small-scale daytime light levels, clipping the surrounding vegetation nonetheless may make the remaining Trollius plants easier to find. On the other hand, this practice also reduces cover for animals Table 2. Effects of clipping neighboring herbaceous vegetation in 2002 and 2003 on T. laxus production of flowers and developed carpels per plant in 2003 and 2004, growth in leaf number from 2002 to 2003, maximum leaf size (cm2), and herbivory levels in 2002 and 2003. n = 7 clipped plots and 6 unclipped plots, all at the Sharon site. Data shown are mean ± standard error of these plot values. Clipped Unclipped t P # flowers 2003 1.20 ± 0.29 0.46 ± 0.32 1.79 0.107 # carpels 2003 6.54 ± 1.90 2.47 ± 2.05 1.55 0.159 # flowers 2004 0.87 ± 0.27 0.48 ± 0.29 1.03 0.326 # carpels 2004 5.32 ± 1.55 2.67 ± 1.68 1.20 0.258 Increase in leaf # 1.91 ± 0.51 0.61 ± 0.55 1.72 0.113 Largest leaf size 36.2 ± 3.6 34.5 ± 3.9 0.30 >0.5 Herbivory 2002 0.75 ± 0.18 0.89 ± 0.20 0.52 >0.5 Herbivory 2003 0.12 ± 0.05 0.13 ± 0.05 0.14 >0.5 2012 K.N. Jones and S.M. Klemetti 275 such as slugs and caterpillars and may therefore reduce herbivore presence in the general area. During night censuses at a California old-field site, Strauss et al. (2009) found that herbivorous mollusks (slugs and snails) were more abundant in areas of taller herbaceous vegetation. We did observe occasional slugs on Trollius leaves, and the most common leaf damage was consistent with the type of damage resulting from slugs. Slugs are introduced generalist herbivores that can impact both the biomass and diversity of plant communities (Bruelheide and Scheidel 1999, Buschmann et al. 2005). Slugs also can have a strong impact on seedling establishment (Joe and Daehler 2008), which we did not quantify. In a study of Trollius europeaus in Scotland, slug predation had a dramatic impact on seedling survival, and this predation was significantly greater in unmowed compared to mowed wet meadow areas (Hitchmough 2003). In T. laxus populations with ample flowering but low seedling recruitment, it may be fruitful to examine nocturnal seedling herbivory. It is important to note that the clipping experiment was carried out in a population that was fenced, keeping out deer and other mammals that may browse the plants, particularly the fruits that are held considerably above the rest of the plant. More than 90% of fruits were browsed in a Colorado population of Trollius albifl orus (K.N. Jones and S.M. Klemetti, unpubl. data), a similar and closely related species found in western North America (Parfitt 1997). It is possible that clipping the surrounding vegetation may exacerbate such browsing, but our experiment did not address this issue. Reduced competition for light may be accomplished by clipping a much smaller area, such as a 10-cm radius around each Trollius plant, to minimize changes in plant apparency to browsers. In addition to suggesting that foliar herbivory is not an increased concern with management to reduce competition for light in Trollius laxus populations, our results indicate that such management is likely to provide an overall benefit to T. laxus plants in these marginal populations. Correlations with higher light levels were either positive or insignificant for measures of plant growth and reproduction, with the most positive effects on flowering. These results from a marginal population are consistent with those from another observational study in what is probably the largest extant T. laxus population, in a New York forested fen, in which higher light levels were positively correlated with Trollius reproductive performance (Scanga and Leopold 2010). Also, data from the clipping experiment suggest that cutting back neighboring plants may increase Trollius growth and reproduction, although the sample sizes were too small to conclude such benefits with much confidence. There was no hint of negative effects of neighbor clipping on any measured aspect of growth and reproduction in this Trollius population. In contrast, a parallel experiment using the same methods in a subalpine population of Trollius albiflorus in Colorado resulted in lower numbers of developed carpels and smaller leaf sizes in plots with clipped neighbors than in unclipped plots (S.M. Klemetti and K.N. Jones, unpubl. data). We had hoped that this closely related and much more abundant species might serve as a useful 276 Northeastern Naturalist Vol. 19, No. 2 model for T. laxus for further experimental purposes, but found that their habitats are notably distinct, as T. albiflorus occurs in more acidic, montane to alpine wetlands rather than the alkaline seeps and fens of T. laxus (Parfitt 1997), and ecologically the two species seem quite different from each other. Increasing light is also unlikely to have negative impacts on pollination of T. laxus. The small bees and flies that we observed in T. laxus flowers in April and early May can probably forage better in direct sun than in shade, especially under cool spring temperatures. When sunlight and temperature conditions permit longer flight distances, such pollinators are more likely to be able to visit sequential rewarding Trollius flowers, even if they are widely separated relative to more common flowers. Lack of “constancy” by generalist pollinators is a problem for rare plants, as it can severely limit the efficiency of pollen transfer (e.g., Peter and Johnson 2009). The presence of seedlings in both study populations in 2003 and 2004 indicated at least some successful reproduction in these sites. In summary, this study did not substantiate concerns that manipulations to increase light might be detrimental to Trollius laxus plants in marginal populations. Such management may provide direct benefits to the plants without increasing risk of herbivory. With the reduction of natural disturbance, such as flooding, and limited dispersal ability in fragmented landscapes, active management probably is required for the persistence of a significant proportion of the remaining T. laxus populations. Acknowledgments We thank Jason Jannot for assistance with fieldwork, Sara Scanga and Alden Griffith for helpful comments on the manuscript, and William Brumback, Michael Dudek, and Rose Walsh for permission to work at the sites. Dr. Robbin Thorp kindly identified the insect visitors we collected from T. laxus flowers. This study was funded in part by a National Science Foundation/New England Wild Flower Society Fellowship in Conservation Biology (to S.M. Klemetti). Literature Cited Baraza, E., J. Gomez, J. Hodar, and R. Zamora. 2004. Herbivory has a greater impact in shade than in sun: Response of Quercus pyrenaica seedlings to multifactorial environmental variation. Canadian Journal of Botany 82:357–364. Bliss, P. 1985. Element steward abstract for Trollius laxus ssp. laxus—Spreading Globefl ower. The Nature Conservancy, Boston, MA. Bruelheide, H., and U. Scheidel. 1999. Slug herbivory as a limiting factor for the geographical range of Arnica montana. Journal of Ecology 87:839–848. Brumback, W.E., L.J. Mehrhoff, R.W. Enser, S.C. Gawler, R.G. Popp, P. Somers, D.D. Sperduto, W.E. Countryman, and C.B. Hellquist. 1996. Flora conservanda: New England. Rhodora 98:233–361. Buschmann, H., M. Keller, N. Porret, H. Dietz, and P.J. Edwards. 2005. The effect of slug grazing on vegetation development and plant species diversity in an experimental grassland. Functional Ecology 19:291–298. Cipollini, D.F., and J. Bergelson. 2002. Interspecific competition affects growth and herbivore damage of Brassica napus in the field. Plant Ecology 162:227–231. 2012 K.N. Jones and S.M. Klemetti 277 Dauber, J., J.C. Biesmeijer, D. Gabriel, W.E. Kunin, E. Lamborn, B. Meyer, A. Nielsen, S.G. Potts, S.P.M. Roberts, V. Sõber, J. Settele, I. Steffan-Dewenter, J.C. Stout, T. Teder, T. Tscheulin, D. Vivarelli, and T. Petanidou. 2010. Effects of patch size and density on flower visitation and seed set of wild plants: A pan-European approach. Journal of Ecology 98:188–196. Gleason, S.M., and A. Ares. 2004. Photosynthesis, carbohydrate storage, and survival of a native and an introduced tree species in relation to light and defoliation. Tree Physiology 24:1087–1097. Heinrich, B. 1979. Bumblebee Economics. Harvard University Press, Cambridge, MA. 245 pp. Henriksson, J., E. Haukioja, V. Ossipov, S. Ossipova, S. Sillanpaa, L. Kapari, and K. Pihlaja. 2003. Effects of host shading on consumption and growth of the geometrid Epirrita autumnata: Interactive roles of water, primary, and secondary compounds. Oikos 103:3–16. Heywood, V.H., and J.M. Iriondo. 2003. Plant conservation: Old problems, new perspectives. Biological Conservation 113:321–335. Hitchmough, J.D. 2003. Effects of sward height, gap size, and slug grazing on emergence and establishment of Trollius europaeus (Globeflower). Restoration Ecology 11:20–28. Hobbs, R.J., and L.F. Huenneke. 1992. Disturbance, diversity, and invasion: Implications for conservation. Conservation Biology 6:324–337. Joe, S.M., and C.C. Daehler. 2008. Invasive slugs as under-appreciated obstacles to rare plant restoration: Evidence from the Hawaiian Islands. Biological Invasions 10:245–255. Jones, K.N. 2001. Trollius laxus (Spreading Globeflower) Conservation and Research Plan. New England Plant Conservation Program, Framingham, MA. 28 pp. Kunin, W.E. 1993. Sex and the single mustard: Population-density and pollinator-behavior effects on seed set. Ecology 74:2145–2160. Kurashige, N.S., and A.A. Agrawal. 2005. Phenotypic plasticity to light competition and herbivory in Chenopodium album (Chenopodiaceae). American Journal of Botany 92:21–26. Leimanis, A.A. 1994. Habitat characteristics of Trollius laxus spp. laxus (Spreading Globeflower) in a minerotrophic forested peatland in central New York. M.Sc. Thesis. College of Environmental Science and Forestry, SUNY, Syracuse, NY. Levesque, K.R., M. Fortin, and Y. Mauffette. 2002. Temperature and food-quality effects on growth, consumption, and post-ingestive utilization efficiencies of the Forest Tent Caterpillar Malacosoma disstria (Lepidoptera: Lasiocampidae). Bulletin of Entomological Research 92:127–136. Louda, S.M., and J.E. Rodman. 1996. Insect herbivory as a major factor in the shade distribution of a native crucifer (Cardamine cordifolia A. Gray, Bittercress). Journal of Ecology 84:229–237. Maschinski, J., T.E. Kolb, E. Smith, and B. Phillips. 1997. Potential impacts of timber harvesting on a rare understory plant, Clematis hirsutissima var. arizonica. Biological Conservation 80:49–61. Mitchell, R.S., and C.J. Sheviak. 1981. Rare plants of New York State. The University of the State of New York, State Education Department, Albany, NY. NatureServe. 2008. NatureServe Explorer: An online encyclopedia of life. Version 7.0. NatureServe, Arlington, VA. Available online at http://www.natureserve.org/explorer. Accessed: 23 October 2008. 278 Northeastern Naturalist Vol. 19, No. 2 Oostermeijer, J.G.B. 2003. Threats to rare plant persistence. In Population viability in plants: Conservation, management, and modeling of rare plants. C.A. Brigham and M.W. Schwartz (Eds.). Springer, Berlin, Germany. Parfitt, B. 1997. Trollius. Pp. 189–190, In Flora of North America Editorial Committee, Flora of North America. Vol. 3. Oxford University Press, NY. 590 pp. Parsons, B.C., and T.A. Yates. 1984. The cultural requirements of Trollius laxus Salisb. ssp. laxus. Report for the Ohio Department of Natural Resources and the Ohio Biological Survey, Holden Arboretum, 9500 Sperry Road, Kirtland, OH 44094. Peter, C.I., and S.D. Johnson. 2009. Reproductive biology of Acrolophia cochlearis (Orchidaceae): Estimating rates of cross-pollination in epidendroid orchids. Annals of Botany 104:573–581. Rhinehalt, G.A. 1990. Ecology of Trollius laxus, an endangered species in Ohio. M.Sc. Thesis. Ohio University, Athens, OH. Sagae, M., N. Oyama-Okubo, T. Ando, E. Marchesi, and M. Nakayama. 2008. Effect of temperature on the floral scent emission and endogenous volatile profile of Petunia axillaris. Bioscience Biotechnology and Biochemistry 72:110–115. SAS Institute. 2007. JMP version 7.0.2. SAS Institute, Inc., Cary, NC. Scanga, S.E. 2009. Population ecology of the rare wetland plant Trollius laxus (Ranunculaceae). Ph.D. Dissertation. State University of New York, College of Environmental Science and Forestry, Syracuse, NY. Scanga, S.E., and D.J. Leopold. 2010. Population vigor of a rare, wetland, understory herb in relation to light and hydrology. Journal of the Torrey Botanical Society 137:297-311. Strauss, S.Y., M.L. Stanton, N.C. Emery, C.A. Bradley, A. Carleton, D.R. Dittrich-Reed, O.A. Ervin, L.N. Gray, A.M. Hamilton, J. Harrington Rogge, S.D. Harper, K. Cook Law, V.Q. Pham, M.E. Putnam, T.M. Roth, J.H. Theil, L.M. Wells, and E.M. Yoshizuka. 2009. Cryptic seedling herbivory by nocturnal introduced generalists impacts survival, performance of native and exotic plants. Ecology 90:419–429. Wang, M., and D.E. Lincoln. 2004. Effects of light intensity and artificial wounding on monoterpene production in Myrica cerifera from two different ecological habitats. Canadian Journal of Botany 82:1501–1508. Zielinski, M.L. 1993. Demography, genetic diversity, and light requirements of the rare plant species Trollius laxus ssp. laxus. M.Sc. Thesis. University of Connecticut, Storrs, CT.