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Methods of Belowground Movement in Erythronium americanum
Jack T. Tessier

Northeastern Naturalist, Volume 19, Special Issue 6 (2012): 77–88

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Northeast Natural History Conference 2011: Selected Papers 2012 Northeastern Naturalist 19(Special Issue 6):77–88 Methods of Belowground Movement in Erythronium americanum Jack T. Tessier* Abstract - As the climate changes, plants will need to respond to new environmental scenarios to survive. Belowground movements are one way in which plants respond to lethal temperatures. Plants use various methods to control belowground movements, notably contractile roots and droppers. I monitored populations of Erythronium americanum (Trout Lily) for contractile roots and documented the capacity of both annual corm growth and droppers to move the corm deeper in the soil. There was no evidence of contractile roots. While both corm growth and droppers lowered the corms, droppers provided for greater movement. Shallower corms produced longer droppers, and the average depth of a new corm formed from a dropper was consistent among corms of various original depths. Erythronium americanum can, therefore, use droppers to control corm depth, thus providing it a mechanism with which to escape potentially dangerous soil temperatures. Introduction Global climate change, as influenced by human activity (Karoly et al. 2003, Tett et al. 1999), is affecting the planet and its species in a variety of ways, including changes in temperature and precipitation (IPCC 2007). One emergent property in these changes is a reduction in the size and duration of the snowpack (Campbell et al. 2007, Lawrence and Slater 2010, Monson et al. 2006, Mote et al. 2005, Regonda et al. 2005, Stewart et al. 2005). Early snowmelt in mountains results in increased frost damage to montane wildflowers (Inouye 2008) and a decrease in winter soil respiration (Monson et al. 2006). In a simulation of climate-change impacts, experimentally reduced snowpack increased soil frost (Hardy et al. 2001), fine root depth (Groffman et al. 2001), and nitrogen and phosphorus leaching (Groffman et al. 2001), while decreasing soil moisture (Hardy et al. 2001). The number of forest species that may be affected by these changes in snowpack, soil conditions, and biogeochemical cycling is unknown. Knowledge of species-specific capacities to respond to environmental cues is integral in predicting the full implications of climate change (Chapin 2003). Plant movements are critical to avoiding lethal temperatures in the soil and near the soil surface (Garrett et al. 2010), which may be increasingly common in association with climate change and a reduced snowpack (Hardy et al. 2001). Contractile roots and droppers are two common methods of belowground plant movement (Galil 1980). Contractile roots are those that exert a pulling force and provide a channel to move the plant up or down in the soil (Pütz 1992, *State University of New York at Delhi, 722 Evenden Tower, Delhi, NY 13753; tessiejt@ delhi.edu. 78 Northeastern Naturalist Vol. 19, Special Issue 6 1996a). These roots are observable via a wrinkling of the base of the root, which is visible to the naked eye (Rimbach 1902). Contractile roots have been found in over 90% of plant species examined for them (Leopold 2000). They are common in geophytes (plants whose perennating structures are located at or below the soil surface), particularly in new corms (Burstrom 1971; Galil 1980; Iziro and Hori 1983; Jernstedt 1984; Leopold 2000; Pütz 1993, 1994, 1996a, 1996b, 1998; Rimbach 1895, 1902; Smith 1930). Droppers are root material (Kurzweil et al. 1995) that extend from the bottom of a tuber, bulb, or corm and result in the formation of a new tuber, bulb, or corm at their terminus. They are present in some dicotyledonous carnivorous plant species (Adlassnig et al. 2005), but are more common among monocotyledonous plants species (Addai 2010, Buxton and Robertson 1953, McCollum 1939, Persson 1988). Like contractile roots, droppers may serve to adjust the depth of subterranean structures (J.M.C. 1907). Erythronium americanum Ker Gawler (Trout Lily) is a spring ephemeral geophyte (Tessier 2008) that is common to secondary forests (Rooney and Dress 1997) in the northeastern United States. It is self sterile (Harder et al. 1993), with a 40% seed germination rate and constant mortality rate among adults (Wein and Pickett 1989). Seed predation is reduced by ant dispersal of its seeds (Ruhren and Dudash 1996, Wein and Pickett 1989). It is not shade tolerant (Wein et al. 1988) and is resilient to defoliation (Rockwood and Lobstein 1994). Trout Lily is mycorrhizal (Lapointe and Molard 1997), absorbing most of its nutrients in spring (Lapointe and Lerat 2006). Ecologically, this vernal uptake of N and K is comparable to the amounts of N and K lost from the terrestrial setting to stream water and is therefore important to nutrient cycling and ecosystem-level retention of nutrients (Muller 1978, Muller and Bormann 1976). Reports in the literature regarding contractile roots in Trout Lily are limited. Blodgett (1910) briefly noted that Trout Lily does not have contractile roots, but did not describe his procedures for determining so. Droppers have been observed in Trout Lily by several authors (Blodgett 1894, 1895, 1900, 1910; Mathew 1992; Robertson 1906), but their capacity for depth control has not been determined (Blodgett 1910). The overarching question addressed in this paper is: how do corms of Trout Lily descend into the soil profile? First, because contractile roots are common among geophytes and the Liliaceae in particular (Jaffe and Leopold 2007, Jernstedt 1984, Rimbach 1902), I sought to document the presence or absence of contractile roots in Trout Lily. Because contractile roots are so common among geophytes, I hypothesized that Trout Lily uses contractile roots to adjust corm depth, and predicted that contractile roots would be evident in the form of wrinkles on the roots of Trout Lily in the spring. Second, based on the results of the first component of this project, I hypothesized that as corms reform after the leafing period, they grow deeper in the soil with a new set of roots at the bottom, and predicted that corms would re-form in the soil profile at a depth increment similar to the distance between the old and new roots. Third, I hypothesized that the size of droppers provides them an advantage over corm growth for corm descent into the soil, and predicted that the increment into the soil profile would be greater from droppers than from corm growth. Finally, I 2012 J.T. Tessier 79 hypothesized that corms can control their depth via the increment into the soil provided by the dropper, and predicted that deeper corms would have a smaller increment provided by the dropper than shallower corms. Methods Study site This study was conducted in the Delhi College Arboretum, in Delhi, NY (42°14'48°N, 74°55'24°W). The Arboretum contains a northern hardwood forest dominated by Acer saccharum Marshall (Sugar Maple), Fagus grandifolia Ehrh. (American Beech), and Betula alleghaniensis Britton (Yellow Birch). In summer, the understory is dominated by Dryopteris intermedia (Muhl.) A. Gray (Common Wood Fern), Dryopteris marginalis (L.) A. Gray (Marginal Wood Fern), Caulophyllum thalictroides (L.) Michx. (Blue Cohosh), and Polystichum acrostichoides (Michx.) Schott (Christmas Fern), with abundant populations of Trout Lily and Allium tricoccum Aiton (Wild Leek) in the spring. Soils are of the Lackawanna flaggy silt loam series (Natural Resource Conservation Service 2011). Annual mean temperature is 6.67 °C, mean January temperature is -6.17 °C, and mean July temperature is 19.44 °C (National Climatic Data Center 2011). Mean annual precipitation is 10,973 mm, mean January precipitation is 749 mm, and mean July precipitation is 980 mm (National Climatic Data Center 2011). Field and laboratory methods Contractile roots. In May 2008, I found three populations of Trout Lily that included at least 50 plants each in the Delhi College Arboretum. These populations were at least 20 m away from each other and were therefore far enough apart to most likely be the result of separate events of sexual reproduction. I outlined each population with a series of small flags for subsequent work when the plants were not visible above ground. On a monthly basis from April until November 2009, I dug from the perimeter of the populations until I had located at least ten total corms (at least three from each population). In the field, I gently removed as much soil as possible and placed the corms in a plastic bag for transport. The collected corms were transported to the lab and soaked in tap water to remove any residual soil. After cleaning, each corm was examined under a dissecting microscope at a magnification of 7x to determine if there was any wrinkling on the roots that would indicate the presence of contractile roots. Each corm was photographed under the dissecting microscope using a Kodak DC290 digital camera with the Kodak MDS290 microscope system. I also measured the corm diameter, distance from roots on the side of the corm (hereafter “old roots”) to roots at the bottom of the corm (hereafter “new roots”), and the number and length of both old and new roots. Corm growth. In June of 2010 (prior to the development of new roots), I collected 30 corms and replanted them at a depth of 10 cm on top of a layer of white sand and adjacent to a sheet of plexiglass buried to a depth of 20 cm. The plexiglass permitted easy relocation of the corms and minimal disturbance at the time of re-measurement. In November 2010, I relocated the corms and measured 80 Northeastern Naturalist Vol. 19, Special Issue 6 the distance from the top of the white sand to the bottom of the corm, indicative of the increment into the soil that the corm moved as a result of corm growth. Droppers. In May 2010 (while leaves were visible above ground), I collected 30 corms with droppers and 30 corms without droppers. For all corms, I measured corm diameter at their greatest width. For corms with droppers, I measured the distance from the soil surface to the bottom of the corm and the distance from the soil surface to the depth at which the new corm was forming at the end of the dropper. Data analyses All analyses were completed at α = 0.05 using Minitab version 15 (Minitab, Inc., State College, PA). I calculated the mean ± standard error of the distance between old and new roots for all corms containing both sets of roots in the contractile root component of the study, the depth increment provided by corm growth, and the depth of new corms formed at the end of droppers. I used a ttest to make the following comparisons: the diameter of corms having one set of roots versus two sets of roots, the number of old roots versus the number of new roots on corms with both sets of roots, the length of old roots versus the length of new roots for corms with both sets of roots, depth increment provided by corm growth versus the mean distance between old and new roots, the depth increment provided by corm growth versus that provided by droppers, and the diameter of corms with versus without droppers. Linear regression was used to compare the original depth of the corm to the depth increment provided by the droppers. Results One hundred six corms were observed during the contractile root component of the study, including at least 10 corms in each month of the study. In April, no contractile roots were evident and some corms were beginning to form droppers (Fig. 1a). One seedling was also observed in April (Fig. 1b). In May, no contractile roots were observed, and some but not all corms had well developed droppers (Fig. 1c, d). In June through September, no contractile roots were present, droppers were not evident, and corms had either one set of roots or no roots (Fig. 1e and f). Corms with no roots were likely those that had formed at the end of droppers earlier in the year (Fig. 1f). In October and November, there was no evidence of contractile roots and some corms had two sets of roots (one on the side [old roots] and another at the bottom [new roots] of the corm, Fig. 1g) and other corms had one set of roots (Fig. 1h). The old roots earned this name because they were visually darker and softer (indicative of senescence) than the new roots. The distance between the centers of the old and new roots was 3.85 ± 0.27 mm (mean ± standard error). The diameter of corms with two sets of roots (13 corms) was significantly greater than that for corms with one set of roots (t = 7.10, P < 0.0001, comparing data from 13 randomly selected corms with one set of roots; Fig. 2a). On corms with both old and new roots, there were significantly more new roots than old roots (t = 4.27, P = 0.0001, Fig. 2b), and the length of new roots was significantly greater than that of old roots (t = 2.23, P = 0.046; Fig. 2c). 2012 J.T. Tessier 81 F i g u r e 1 . Representative corms of Erythronium americanum observed at the Delhi College Arboretum (Delhi, NY, USA) in April (a and b), May (c and d), June– September (e and f), and October and November (g and h) 2009. Labels: dr = dropper, or = old root, nr = new root. 82 Northeastern Naturalist Vol. 19, Special Issue 6 The depth increment provided by corm growth (distance into the layer of white sand) was 3.40 ± 0.12 mm (n = 30). This increment was not significantly different from the 3.85 ± 0.27 mm (n = 13) of distance seen previously between the old and new roots (t = 1.49, P = 0.156). The depth increment provided by droppers was significantly greater than that provided by corm growth (t = -7.60, P < 0.0001; Fig. 3a). The average diameter of corms with droppers was significantly less than that of corms without droppers (t = -2.89, P = 0.005; Fig. 3b). There was a significant negative relationship between the depth of the original corm and the depth increment provided by the droppers (P = 0.004, r2 = 0.272; Fig. 3c). The average depth of corms formed at the bottom of droppers was 8.80 ± 0.42 cm. Figure 2. Diameter of corms with one vs. two sets of roots (a), number of old and new roots per corm (b), and mean length of old vs. new roots (c) in Erythronium americanum at the Delhi College Arboretum (Delhi, NY) in 2009. Error bars represent one standard error above the mean. 2012 J.T. Tessier 83 Discussion The results of this study reject the first hypothesis that Trout Lily uses contractile roots to control corm depth, providing visual evidence in support of the vague note made by Blodgett (1910). At no time during the year were contractile roots evident in the corms observed (Fig. 1). Droppers were routinely seen during the spring supporting observations made by Blodgett (1900, 1910). These structures have been proposed as a method of both vegetative reproduction (Blodgett 1894, 1895; Gray 1871; Mathew 1992) and control of corm depth in Trout Lily (Blodgett 1900, 1910; Galil 1980; Osborn 1919). Figure 3. Increment of downward movement provided by corm vs. dropper growth (a), diameter of corms with vs. without droppers (b), and the relationship between original corm depth and increment of downward movement provided by droppers (c) in Erythronium americanum at the Delhi College Arboretum (Delhi, NY) in 2010. Error bars represent one standard error above the mean. 84 Northeastern Naturalist Vol. 19, Special Issue 6 The second hypothesis, that corm growth can provide depth increment, is supported because the depth increment provided by corm growth is not signifi- cantly different from the distance between the old and new roots. Because the new corms that develop at the end of the droppers do not seem to develop roots until the fall (Figs. 1h, 2a; Brundrett and Kendrick 1990), this method of depth increment is likely to only be effective in second year or older corms. This result provides a mechanism for the development of new corms from below old corms as noted by Blodgett (1910). The third hypothesis, that droppers are a more effective method of increasing depth than corm growth, is supported because droppers provide more than 8 times the increment provided by corm growth (Fig. 3a). The large number of Erythronium species that have droppers (Robertson 1966) may be explained by this distinct mobility advantage provided by them. Developing a dropper appears to require significant energy mobilization, as evidenced by the small diameter of corms with droppers relative to those without droppers (Fig. 3b). Visible shriveling of the outer covering of corms with droppers suggests that they had been larger prior to dropper development. Because droppers only form in older corms of Trout Lily (Addai 2010), younger corms may be relegated to depth increment via corm growth until they can acquire sufficient resources to support dropper development. This result addresses the need identified by J.M.C. (1907) to document the capacity of droppers to increase the depth of the corm. The fourth hypothesis, that Trout Lily can control its depth with droppers, is also supported because shallower corms produced droppers that descended a greater increment into the soil than those of deeper corms (Fig. 3c). This trend suggests that corms can detect their depth and adjust their droppers based on it, which is a trait typical of other bulbous plants (Massart 1903). The depth increment provided by contractile roots in other species is cued by temperature and/ or light (Galil 1958, 1980; Halevy 1986; Iziro and Hori 1983; Jacoby and Halevy 1970; Jaffe and Leopold 2007; Pütz 1996c; Pütz et al. 1997), and these environmental cues may determine the depth increment provided by droppers in Trout Lily. Further, this trend suggests that there is an advantage to the corm from being sufficiently deep in the soil. The average depth of new corms formed at the end of droppers (8.80 ± 0.42 cm) is remarkably consistent among corms and is similar to the deepest existing corm observed in this part of the study (8.0 cm). Blodgett (1910) noted that droppers descend a maximum of 4–5 cm into the soil, which may have been predicated by his use of corms planted in window boxes for his observations. The data from the current study are from a forested ecosystem, and are more likely to be representative of corm behavior in the wild. The depth increment provided by droppers is comparable to the 6–10-cm increment reported for contractile roots in other species (Pütz and Sukkau 1995). These results lead to new questions regarding the ecological significance of corm depth and movement, particularly in the face of climate change. First, how important is corm depth to winter survival and how will a reduced snowpack associated with climate change affect winter survival of corms (Inouye 2000, Kapnick and Hall 2010, Lawrence and Slater 2010, Simons et al. 2010)? Younger 2012 J.T. Tessier 85 corms that develop from fall-germinating seeds (Blodgett 1910) may be especially susceptible to freezing with a reduced snowpack, unless ants bury them at a sufficient depth (Heithaus 1981, Ruhren and Dudash 1996). If seedlings are not capable of descending fast enough to survive the first winter under a scenario of reduced snowpack, then the capacity for sexual reproduction and thus genetic diversity of the population would be compromised in Trout Lily (Inouye 2000). This eventuality is particularly concerning because the results of this study show that young corms have limited capacity to control their own depth. Second, at what depth do seedlings form? Surface germination would leave the seedlings vulnerable to freezing, but ants may bury seeds at a sufficient depth to minimize this risk (Heithaus 1981, Ruhren and Dudash 1996). Third, what environmental cues does E. americanum use to determine its corm depth? Other species use droppers to avoid predation and dangerous temperatures, but the driving force behind this movement is unknown (Dixon and Tremblay 2009). Fourth, what is the exact developmental progression of corms in Trout Lily? For example, Blodgett (1910) reports that droppers are a seedling trait, but Addai (2010) reports that they occur in mature corms. Future research should address these questions and help to determine the capacity of Trout Lily to establish seedlings and move its corms under novel conditions associated with climate change. Acknowledgments I thank Mark Jaffe and Carl Leopold for their presentation on contractile roots at the Boyce Thompson Institute Root and Soil Conference that introduced me to contractile roots, Karen Teitelbaum and Donna Doherty for assistance with the microscope and camera, Lisa Tessier for assistance with Figure 1, Benjamin McGraw and two anonymous reviewers for constructive comments on iterations of the manuscript, and the SUNY Delhi Dean’s Council for the Professional Development Grant that supported travel. Literature Cited Addai, I.K. 2010. Growth and biochemistry of the Common Hyacinth (Hyacinthus orientalis L.) and the lily (Lilium longiflorum L.). Ph.D. Dissertation. University of Sussex, Brighton, UK. 285 pp. Adlassnig, W., M. Peroutka, H. Lambers, and I.K. Lichtscheidl. 2005. The roots of carnivorous plants. Plant and Soil 274:127–140. Blodgett, F.H. 1894. On the development of the bulb of the Adder’s-tongue. Botanical Gazette 19:61–65. Blodgett, F.H. 1895. 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