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. On the development of the bulb of the Adder’s-tongue. Botanical
Gazette 20:172–175.
Blodgett, F.H. 1900. Vegetative reproduction and multiplication in Erythronium. Bulletin
of the Torrey Botanical Club 27:305–315.
Blodgett, F.H. 1910. The origin and development of bulbs in the genus Erythronium.
Botanical gazette 50:340–373.
Brundrett, M.C., and B. Kendrick. 1990. The roots and mycorrhizas of herbaceous woodland
plants. I. Quantitative aspects of morphology. New Phytologist 114:457–468.
Burstrom, H.G. 1971. Tissue tensions during cell elongation in Wheat roots and a comparison
with contractile roots. Physiologia Plantarum 25:509–513.
86 Northeastern Naturalist Vol. 19, Special Issue 6
Buxton, E.W., and N.F. Robertson. 1953. The fusarium yellows disease of Gladiolus.
Plant Pathology 2:61–64.
Campbell, J.L., C.T. Driscoll, C. Eager, G.E. Likens, T.G. Siccama, C.E. Johnson, T.J.
Fahey, S.P. Hamburg, R.T. Holmes, A.S. Bailey, and D.C. Buso. 2007. Long-term
trends from ecosystem research at the Hubbard Brook Experimental Forest. USDA
Forest Service Northeast Research Station General Technical Report NRS-17. Newton
Square, PA.
Chapin, F.S., III. 2003. Effects of plant traits on ecosystem and regional processes: A
conceptual framework for predicting the consequences of global change. Annals of
Botany 91:455–463.
Dixon, K., and R.L. Tremblay. 2009. Biology and natural history of Caladenia. Australian
Journal of Botany 57:247–258.
Galil, J. 1958. Physiological studies on the development of contractile roots in geophytes.
Bulletin of the Research Council of Israel. 6D:221–236.
Galil, J. 1980. Kinetics of bulbous plants. Endeavor 5:15–20.
Gray, A. 1871. A new species of Erythronium. The American Naturalist 5:298–300.
Garrett, T.Y., C.-V. Huynh, and G.B. North. 2010. Root contraction helps protect the “living
rock” cactus Ariocarpus fissuratus from lethal high temperatures when growing in
rocky soil. American Journal of Botany 97:1951–1960.
Groffman, P.M. C.T. Driscoll, T.J. Fahey, J.P. Hardy, R.D. Fitzhugh, and G.L. Tierney.
2001. Colder soils in a warmer world: A snow-manipulation study in a northern hardwood
forest ecosystem. Biogeochemistry 56:135–150.
Halevy, A.H. 1986. The induction of contractile roots in Gladiolus grandiflorus. Planta
167:94–100.
Harder, L.D., M.B. Cruzan, and J.D. Thomson. 1993. Unilateral incompatibility and the
effects of interspecific pollination for Erythronium americanum and Erythronium
albidum (Liliaceae). Canadian Journal of Botany 71:353–358.
Hardy, J.P., P.M. Groffman, R.D. Fitzhugh, K.S. Henry, A.T. Welman, J.D. Demers, T.J.
Fahey, C.T. Driscoll, G.L. Tierney, and S. Nolan. 2001. Snow depth manipulation and
its influence on soil frost and water dynamics in a northern hardwood forest. Biogeochemistry
56:151–174.
Heithaus, E.R. 1981. Seed predation by rodents on three ant-dispersed plants. Ecology
62:136–145.
Inouye, D.W. 2000. The ecological and evolutionary significance of frost in the context
of climate change. Ecology Letters 3:457–463.
Inouye, D.W. 2008. Effects of climate change on phenology, frost damage, and floral
abundance of montane wildflowers. Ecology 89:353–362.
Intergovernmental Panel on Climate Change (IPCC). 2007. Climate change 2007: Synthesis
report. Contribution of Working Groups I, II, and III to the Fourth Assessment
Report of the Intergovernmental Panel on Climate Change [Core Writing Team,
Pachauri, R.K., and A. Reisinger (Eds.)]. IPCC, Geneva, Switzerland, 104 pp.
Iziro, Y., and Y. Hori. 1983. Effect of planting depth in the growth of contractile root(s)
and daughter corm or bulbs in Gladiolus and Oxalis bowieana. Journal of the Japanese
Society of Horticultural Science 52:51–55.
J.M.C. 1907. “Droppers” of Tulipia and Erythronium. Botanical Gazette 43:75.
Jacoby, B., and A.H. Halevy. 1970. Participation of light and temperature fluctuation in
the induction of contractile roots of Gladiolus. Botanical Gazette 131:74–77.
Jaffe, M.J., and A.C. Leopold. 2007. Light activation of contractile roots of Easter Lily.
Journal of the American Society for Horticultural Science 132:575–582.
Jernstedt, J.A. 1984. Seedling growth and root contraction in the soap plant, Chlorogalum
pomeridianum (Liliacae). American Journal of Botany 71:69–75.
2012 J.T. Tessier 87
Kapnick, S., and A. Hall. 2010. Observed climate-snowpack relationships in California
and their implications for the future. Journal of Climate 23:3446–3456.
Karoly, D.J., K. Braganza, P.A. Stott, J.M. Arblaster, G.A. Meehl, A.J. Broccoli, and
K.W. Dixon. 2003. Detection of a human influence on North American climate. Science
302:1200–1203.
Kurzweil, H., H.P. Linder, W.L. Stern, and A.M. Pridgeon. 1995. Comparative vegetative
anatomy and classification of Disease (Orchidaceae). Botanical Journal of the Linnean
Society 117:171–220.
Lapointe, L., and S. Lerat. 2006. Annual growth of the spring ephemeral Erythronium
americanum as a function of temperature and mycorrhizal status. Canadian Journal
of Botany 84:39–48.
Lapointe, L., and J. Molard. 1997. Costs and benefits of mycorrhizal infection in a spring
ephemeral, Erythronium americanum. New Phytologist 135:491–500.
Lawrence, D.M., and A.G. Slater. 2010. The contribution of snow condition trends to
future ground climate. Climate Dynamics 34:969–981.
Leopold, A.C. 2000. Many modes of movement. Science 288:2131–2132.
Massart, J. 1903. Comment les plantes vivaces maintiennent leur niveau souterrain. Bulletin
de Jardin Botanique de L’etat a Bruxelles 1:113–141.
Mathew, B. 1992. A taxonomic and horticultural review of Erythronium L. (Liliaceae).
Botanical Journal of the Linnean Society 109:453–471.
McCollum, R.L. 1939. The development of the embryo sac and the seed of Commelina
angustifolia Michx. Bulletin of the Torrey Botanical Club 66:539–548.
Monson, R.K., D.L. Lipson, S.P. Burns, A.A. Turnipseed, A.C. Delany, M.K. Williams,
and S.K. Schmidt. 2006. Winter forest soil respiration controlled by climate and microbial
community composition. Nature 439:711–714.
Mote, P.W., A.F. Hamlet, M.P. Clark, and D.T. Lettenmaier. 2005. Declining mountain
snow pack in Western North America. Bulletin of the American Meteorological Society
86:39–49.
Muller, R.N. 1978. The phenology, growth, and ecosystem dynamics of Erythronium
americanum in the northern hardwood forest. Ecological Monographs 48:1–20.
Muller, R.N., and F.H. Bormann. 1976. Role of Erythronium americanum Ker. in energy
flow and nutrient dynamics of a northern hardwood forest ecosystem. Science
193:1126–1128.
National Climatic Data center (NCDC). 2011. Monthly station normal of temperature,
precipitation, and heating and cooling degree days 1971–2000. Available online at
http://cdo.ncdc.noaa.gov/cgi-bin/climatenormals/climatenormals.pl. Accessed 21
February 2011.
Natural Resource Conservation Service (NRCS). 2011. Web soil survey. Available online
at http://websoilsurvey.nrcs.usda.gov/app/WebSoilSurvey.aspx. Accessed 21 February
2011.
Osborn, T.G.B. 1919. Some observations on the tuber of Phylloglossum. Annals of
Botany 33:485–516.
Persson, K. 1988. New species of Colchicum (Colchicaceae) from the Greek mountains.
Willdenowia 18:29–46.
Pütz, N. 1992. Measurement of the pulling force of a single contractile root. Canadian
Journal of Botany 70:1433–1439.
Pütz, N. 1993. Underground plant movement I. The bulb of Nothoscordum inodorum
(Alliaceae). Botanica Acta 106:338–343.
Pütz, N. 1994. Vegetative spread of Oxalis pes-caprae (Oxalidaceae). Plant Systematics
and Evolution 191:57–67.
88 Northeastern Naturalist Vol. 19, Special Issue 6
Pütz, N. 1996a. Development and function of contractile roots. Pp. 895–874, In Y. Waisel,
A. Eshel, and U. Kafkafi(Eds.). Plant Roots: The Hidden Half. 2nd Edition. Marcel
Dekker, Inc. New York, NY. 1002 pp.
Pütz, N. 1996b. Underground plant movement. III. The corm of Sauromatum guttatum
(Wall.) Schott (Araceae). Flora 191:275–282.
Pütz, N. 1996c. Underground plant movement. IV. Observance of the behavior of some
bulbs with special regard to the induction of root contraction. Flora 191:313–319.
Pütz, N. 1998. Underground plant movement. V. Contractile root tubers and their importance
to the mobility of Hemerocallis fulva L. (Hemerocallidaceae). International
Journal of Plant Science 159:23–30.
Pütz, N., and I. Sukkau. 1995. Comparative examination of the moving process in monocot
and dicot seedlings using the example Lapeirousia laxa (Iridaceae) and Foeniculum
vulgare (Apiaceae). Feddes Repertorium 106:5–8.
Pütz, N., J. Pieper, and H.A. Froebe. 1997. The induction of contractile root activity in
Sauromatum guttatum (Araceae). Botanica Acta 110:49–54.
Regonda, S.K., B. Rajagopalan, M. Clark, and J. Pitlick. 2005. Seasonal cycle shifts in
hydroclimatology over the western United States. Journal of Climate 18:372–384.
Rimbach, A. 1895. Zur biologie der pflanzen mit unterirdishem spross. Deutsche Botanische
Gesellschaft 13:141–155.
Rimbach, A. 1902. Physiological observations on the subterranean organs of some Californian
Liliacae. Botanical Gazette 33:401–420.
Robertson, A. 1906. The “droppers” of Tulipia and Erythronium. Annals of Botany
20:429–440.
Robertson, K.R. 1966. The genus Erythronium (Liliaceae) in Kansas. Annals of the Missouri
Botanical Garden 53:197–204.
Rockwood, L.L., and M.B. Lobstein. 1994. The effects of experimental defoliation on
reproduction in four species of herbaceous perennials from northern Virginia. Castanea
59:41–50.
Rooney, T.P., and W.J. Dress. 1997. Patterns of plant diversity in overbrowsed primary
and mature secondary hemlock-northern hardwood forest stands. Bulletin of the Torrey
Botanical Society 124:43–51.
Ruhren, S., and M.R. Dudash. 1996. Consequences of the timing of seed release of Erythronium
americanum (Liliaceae), a deciduous forest myrmecochore. American Journal
of Botany 83:633–640.
Simons, A.M., J.M. Goulet, and K.F. Bellehumeur. 2010. The effect of snow depth on
overwinter survival in Lobelia inflata. Oikos 119:1685–1689.
Smith, F.H. 1930. The corm and contractile roots of Brodiaea lactea. American Journal
of Botany 17:916–927.
Stewart, I.T., D.R. Cayan, and M.D. Dettinger. 2005. Changes toward earlier streamflow
timing across western North America. Journal of Climate 18:1136–1155.
Tessier, J.T. 2008. Leaf habit, phenology, and longevity of eleven forest understory plant
species in Algonquin State Forest, northwest Connecticut, USA. Botany 86:457–465.
Tett, S.F.B., P.A. Stott, M.R. Allen, W.J. Ingram, and J.F.B. Mitchell. 1999. Causes of
twentieth century temperature change near the Earth's surface. Nature 399:569–572.
Wein, G.R., and S.T.A. Pickett. 1989. Dispersal, establishment, and survivorship of a cohort
of Erythronium americanum. Bulletin of the Torrey Botanical Club 116:240–246.
Wein, G.R., S.T.A. Pickett, and B.S. Collins. 1988. Biomass allocation of Erythronium
americanum populations in different irradiance levels. Annals of Botany 61:717–722.