2008 NORTHEASTERN NATURALIST 15(2):177–188
Natural History of Heterophylly in Nymphaea odorata ssp.
tuberosa (Nymphaeaceae)
Philip J. Villani1,* and Shelley A. Etnier1
Abstract - Nymphaea odorata (American white water lily) is an aquatic plant
that displays pronounced heterophylly, the appearance of different leaf forms on a
single plant. Water lilies produce leaves that either float or are held above the water’s
surface. In this paper, we describe the natural history of water lily leaf forms
and examine some of the factors that stimulate heterophylly. Over the course of
a growing season, the predominant leaf form switches from surface leaves in the
early season to aerial leaves in the midseason and then back to surface leaves at
season’s end. While many factors are known to contribute to heterophylly, our
results suggest that changes in the light environment may be the controlling factor
in this system.
Introduction
Heterophylly, the appearance of different leaf forms on a single plant,
is a common feature of many plants (Arber 1920, Schlichting 1986,
Sculthorpe 1967). Some of the most dramatic examples of heterophylly occur
in the aquatic amphibious plants. In these plants, heterophylly occurs when a
single plant is growing in two physically dissimilar environments (i.e., aquatic
and terrestrial) that pose substantially different metabolic and mechanical
demands on separate parts of the organism. Leaf adaptations often reflect the
physical differences in these environments and typically include changes in
leaf morphology, anatomy, and/or the position of the lamina relative to the
water’s surface (for a general review see Sculthorpe 1967).
One example of a plant that changes the position of its leaves relative to
the water’s surface is Nymphaea odorata Ait ssp. tuberosa (Paine) Wiersma
& Hellquist (American white water lily). It is commonly found in still
or slow-moving waters in the northeastern parts of North America (Gleason
and Cronquist 1991). During growth of the white water lily, its shoot
system (i.e., a rhizome) remains buried in the sediment below the water’s
surface throughout the life of the plant. Immature leaves are produced from
the rhizome and mature into three leaf types: immersed, which remain submerged;
surface, which float on the water’s surface; and aerial, which are
held above the water (Sculthorpe 1967; Fig. 1). These three leaf forms do
not represent a growth continuum, as a developing leaf matures into one
form or the other. Immersed leaves occur early in the season (Sculthorpe
1967) and are never abundant (P.J. Villani, pers. observ.). In some populations,
the surface leaf is the predominant leaf form, while other populations
produce both surface and aerial leaf forms (S.A. Etnier, pers. observ.).
1Department of Biological Sciences, Butler University, Indianapolis, IN
46208. *Corresponding author - pvillani@butler.edu.
178 Northeastern Naturalist Vol. 15, No. 2
In a previous study, we characterized the differences in biomechanical
properties between surface and aerial petioles (Etnier and Villani 2007). We
found that an aerial leaf rises above the water’s surface due to increased
rigidity of its petiole. The increased rigidity is due to subtle changes in petiole
anatomy and morphology. There seem to be seasonal differences in the
abundance of these two leaf types (S.A. Etnier, pers. observ.), but little is
known about the causal factors determining their appearance.
Many heterophyllous aquatic species switch between a combination
of immersed, surface (floating), and aerial leaf forms, although the exact
mechanism for this switch varies (Minorsky 2003). In Nuphar lutea (L.) Sm.
(yellow cow lily), herbivory causes an increase in immersed leaf production
relative to aerial leaves (Kouki 1993). In other aquatic species, the switch
to aerial leaf forms was stimulated by changes in water depth (Horn 1988,
Nohara and Kimura 1997), composition of sediment type (Barko and Smart
1986), and changes in the concentration of dissolved carbon dioxide as the
shoots grow out of the aquatic into a terrestrial environment (Bristow and
Looi 1968, Titus and Sullivan 2001). The exogenous application of abscisic
acid, a well-known plant hormone produced in response to osmotic stress,
has also been shown to mediate the switch from immersed to aerial leaf
forms (Anderson 1978, Liu 1984, Ram and Rao 1982). In other species, features
of the light environment including fluency rates (Goliber 1989), light
quality (Bodkin et al. 1980, Lin and Yang 1999), and photoperiod (Cook
1969, Kane and Albert 1987, Schmidt and Millington 1968) influenced heterophylly.
To our knowledge, no studies have examined the factors influencing
heterophylly in the white water lily, although Sculthorpe (1967) briefly
mentioned that crowding may induce the aerial leaf form.
Figure 1. Heterophylly in the American white water lily as shown in a leaf-removal
experiment showing the two different forms of the lily pad leaves: surface (A, center
of figure) and aerial (B). Figure 1A is an experimental plot in which leaf removal
occurred. Leaves were selectively removed from the experimental plots in order to
maintain a 50%-exposed water surface, and Figure 1B is a control plot in which there
was no leaf removal.
2008 P.J. Villani and S.A. Etnier 179
In this paper, we investigate the natural history of heterophylly in the
white water lily. First, we describe the seasonal distribution of surface and
aerial leaves throughout the growing season. Second, we examine some
of the factors that may be responsible for the stimulation of heterophylly
under natural conditions. Based on research on other heterophyllic plants,
we examine differences in life-history traits, including growth rates and
leaf longevity. We also examine physical and chemical aspects of the
pond, as well as the influence of crowding, on the appearance of surface
and aerial leaves.
Materials and Methods
Plant material
All measurements were taken on a population of American white
water lily growing in a half-acre ice-skating pond at Eagle Creek City Park,
Indianapolis, IN. Observations and experiments were completed during the
2005 growing season, with the exception of the longevity and crowding studies,
which were conducted during 2006.
The lily pad growing season started at the beginning of April, when
leaves first appeared in the pond, and continued until their disappearance
from the pond in late October and early November. In this study, we have
divided the growing season into three parts: early season was defined as
April and May, mid-season as June and July, and late season as August
through October.
Water chemistry
During the growing season of 2006, we measured water chemistry
parameters biweekly. Using a LaMotte aquaculture test kit (Chestertown,
MD), we determined water pH and dissolved oxygen (dO2), carbon dioxide
(dCO2), and ammonia concentrations.
Life-history characteristics
At the onset of the growing season (early April), six square plots (1 m2)
were demarcated within the pond using garden stakes. Three plots were
placed on both the east and west side of the pond at 5, 10, and 20 m distances
from the shore along a straight line. We counted the number of immature,
surface, and aerial leaf forms occurring within the plots two to three times
a week throughout the growing season. We also recorded water temperature
and depth.
We measured the growth rate during the period in which the lamina
extends rapidly up to the water’s surface, in both surface and aerial petioles.
In each of the plots described above, we selected a small immature
leaf close to the pond bottom, marked it by placing a colored twist-tie
loosely around its base, and placed a garden stake near the leaf to allow us
to relocate it easily. Two to three times a week, we measured petiole length
and diameter at the midpoint, lamina length and width, and also recorded
observations on the shape of the elongating lamina (e.g., tightly coiled,
180 Northeastern Naturalist Vol. 15, No. 2
loosely coiled, partially open, or fully open). Each marked leaf was monitored
until it reached the water’s surface, at which time we discontinued
growth measurements. We continued to observe the leaf until its final form
(i.e., surface or aerial) could be determined. As soon as we stopped taking
measurements on one leaf, we selected another immature leaf and repeated
the process. We monitored 75 leaves between April and October. Growth
rates (cm/day) were calculated from a simple linear regression of petiole
length against the number of days from the initial measurement using Excel
Sp-1. All comparisons between means were performed using one-way
analysis of variance (ANOVA) followed by Tukey’s post-hoc test (MiniTab
Version 13) for multiple comparisons.
To determine leaf longevity, we selected twenty immature leaves on May
12 and marked them with a garden stake, as before. Leaves were somewhat
evenly distributed within a 20- x 20-m2 area. As leaves matured, we classified each leaf as either an aerial or surface form. We then observed each
leaf biweekly and recorded the amount of green tissue remaining on it until
the leaf was determined to be dead. We defined a leaf as dead when 50% of
the lamina was either necrotic or significantly chlorotic. Missing leaf material
was included as dead tissue. Twenty additional leaves were marked on
both June 8 and July 3, so that we have longevity measures for 59 leaves
(one sample was lost) spanning a period of time from May to August. These
measures included 28 surface leaves and 31 aerial leaves.
Crowding study
We examined the influence of vegetational shading (leaf crowding) on
the production of aerial leaf forms in summer 2006. In May, we set up six
plots in an open area of the pond. Each plot consisted of two concentric
circles, one meter and two meters in diameter, that were marked with garden
stakes and string. Three of the plots were designated as control plots
and were left undisturbed during the course of the experiment. In the other
three plots, leaves were selectively removed from the outer ring in an effort
to maintain a 50% open water surface throughout the experiment. Laminae
were removed by hand at the water’s surface. We were careful not to enter
the plots during the pruning process so that we would not cause injury to
the rhizomes of the study plants. Twice a week, we recorded the number of
surface and aerial leaves appearing within the inner circle for both control
and experimental plots.
Results
Water conditions
Temperature, dO2, and dCO2, although highly variable from day to day,
consistently oscillated above and below a central mean value during the
growing season (Table 1). In contrast, pond depth decreased from approximately
82 cm in May to 14.5 cm in October, whereas ammonia concentration
and water pH remained nearly constant.
2008 P.J. Villani and S.A. Etnier 181
Life-history characteristics
Across the growing season, immature leaves were produced rapidly at
the beginning of the season, but their numbers gradually decreased over
the summer (Fig. 2). As leaves matured, they became surface (floating)
leaves early in the season, aerial leaves in mid-season, and surface leaves
in late season (Fig. 3). Thus, there were two changes in the predominant
leaf form during the growing season, from surface to aerial leaves in
May–June and from aerial to surface in August–September. Regardless of
form, the number of leaves present on a day-to-day basis was fairly stable
until late August, when it began to decrease until the end of the growing
season (Fig. 2).
Immature surface and aerial leaf forms differed in their appearance
underwater. When submerged, the laminae of surface leaves were initially
tightly curled, but then began to unfold under water until they were
Table 1. Pond water quality parameters measured biweekly during the course of the 2006 summer.
S.D. = standard deviation, N = sample size.
Parameter Seasonal average Range S.D. N
Temperature (°C) 22.7 17–28 2.25 28
Depth (cm) 50.1 14.5–82 17.9 73
Dissolved O2 (ppm) 56.9 10–78 23.8 29
Dissolved CO2 (ppm) 62.5 21–94 20.9 29
Ammonia (ppm) 0.23 0.2–0.8 0.02 28
pH 6.55 6.5–7.5 0.20 29
Figure 2. Total numbers of mature (both surface and aerial) and immature water lily
leaves produced over the growing season. Six plots (1 m2) were monitored for leaf
production two to three times weekly during the 2005 growing season.
182 Northeastern Naturalist Vol. 15, No. 2
completely open as they reached the water’s surface. The laminae of
aerial leaves also started tightly curled, but they remained curled as they
approached the surface and only opened after they were completely out of
the water.
Figure 3. Total numbers of aerial and surface leaves produced over the growing
season. Six plots (1 m2) were monitored two to three times per week during the 2005
growing season.
Figure 4. Growth rates of water lily leaf types over the growing season. Forty-one
leaves produced across the growing season were monitored to determine the growth
rate of petioles.
2008 P.J. Villani and S.A. Etnier 183
Petiole growth rate was highly variable at a given time during the
season; however, the growth rates of all petioles decreased as the season
progressed (Fig 4). Since immature leaves mature almost exclusively into
surface leaves in the early and late season and into aerial leaves in the
mid-season, we compared growth rates of petioles among the different
times of the seasons. Early season surface petioles had a mean growth
rate of 53 ± 19.5 mm/day (n = 17), while mid-season aerial petioles had
a mean growth rate of 37.8 ± 22.5 mm/day (n = 13). Late season surface
petioles had a mean growth rate of 21.6 ± 10.5 mm/day (n = 11). Early
and late season surface petioles differed significantly in their growth rates
(F2, 38 = 9.59, P < 0.005).
To determine whether immature petiole form could be used to predict
final leaf form, we compared the maximum diameter of immature petioles
on the first measurement date for all leaves. The leaf form of a measured immature
petiole was determined retrospectively by following an elongating
petiole to maturity. Immature aerial leaf forms had a mean petiole diameter
that was larger than surface forms (Table 2).
Overall, mature surface and aerial leaves were similar in shape. However,
the laminae of surface leaves tend to have a smaller surface area compared
to aerial leaves (Table 2; F1, 28 = 2.8, P = 0.11). In addition, the mean longevity
of surface leaves was significantly less than the mean longevity of aerial
leaves (Table 2).
Crowding
Among the three control plots with no leaf removal, the mean number of
aerial leaves over the course of the study increased steadily, to a maximum
of 24. In contrast, only a single aerial leaf was observed during the entire
study period in the three experimental plots (Fig. 5).
Discussion
The natural history of aerial and surface leaves varies with respect to a
number of different parameters. Aerial and surface leaves appear at different
times during the growing season. While their growth rates are similar, their
patterns of growth differ, both during maturation and in their final morphology.
We suggest that these differences are due to changing functional and
Table 2. Comparison of surface and aerial leaf characteristics in the white water lily. Values
are means and standard deviations are given in parentheses. An asterisk denotes a significant
difference of P < 0.05.
Immature
Petiole petiole Lamina
Leaf form length (cm) diameter (mm) area (cm2) Longevity (days)
Surface 66.95 (11.3) 5.8* (1.4) 339.3 (186.6) 34.6* (7.3)
N = 15 N = 12 N = 15 N = 28
Aerial 63.13 (10.4) 7.6* (1.1) 436.6 (126.2) 48.0* (11.1)
N =15 N = 32 N = 15 N = 31
184 Northeastern Naturalist Vol. 15, No. 2
physiological demands on the leaf. Lily pads maintain high leaf productivity
during most of the growing season (Fig. 2, immature leaves), suggesting
that they continually develop new organs that are well suited for the current
environmental conditions. The heterophyllic nature of the white lily pad may
allow it to optimize its photosynthetic opportunities as natural conditions
change with the season.
Immature surface and aerial leaves differ in form as they grow. Surface
leaves open while still underwater, while aerial leaves remain coiled until
they extend into the air. We suggest that the coiled aerial leaves more easily
penetrate the canopy of surface leaves already present at the water’s surface.
The final morphology of surface and aerial leaves also differs. Compared to
surface leaves, aerial leaves have a larger petiole diameter (Etnier and Villani
2007) and tend to have a greater lamina surface area (Table 2). Since
aerial leaves occur during mid-season, a larger lamina surface area may
allow for greater photosynthetic productivity during the long duration and
high-intensity light of summer days.
The steady decrease in petiole growth rates across the growing season
suggests factors other than leaf type may influence growth. For example,
pond depth decreased over the course of our study, thus the amount of
petiole growth required to bring a lamina to the surface decreased. Once
mature, aerial leaves persist for about 13 days longer than surface leaves
Figure 5. The influence of leaf removal on aerial-leaf production in water lily. The
production of aerial leaf forms were monitored in six plots, three of which did not
have leaves removed from them and three of which had leaves removed randomly to
maintain 50% exposure of the water surface.
2008 P.J. Villani and S.A. Etnier 185
(Fig. 3), potentially influencing the seasonal patterns observed in our
study. We suggest that aerial leaves are more costly to produce because
they require more material, so increased longevity may balance the cost
of leaf production.
During the growing season, there were two major switches in the predominant
leaf form. The switch in the developmental pathway leading to
surface or aerial leaves must occur early in leaf maturation. Early in development,
when petioles are approximately one-third their final length,
immature aerial petioles are already larger in diameter than surface
petioles (Table 2). The first switch, from surface to aerial, was relatively
gradual and occurred early in the season. The second switch, from aerial
back to surface, occurred later in the growing season and was much more
abrupt, with a rapid decrease in aerial-leaf abundance. The difference in
the rate of these two switching events suggests that the plants may be responding
to different stimuli.
Factors influencing heterophylly
A number of different stimuli have been shown to influence heterophylly
in other aquatic species, but these factors are unlikely to be responsible for
causing it in the white water lily. Marsilea quadrifolia L. (European waterclover)
produces aerial leaf forms when submerged shoots grow out of the
water into dry air, a desiccation response mediated by abscisic acid (Lin and
Yang 1999, Liu 1984). Desiccation is not likely a stimulus in white water lily
because the shoot system remains submerged in persistent ponds or lakes,
and both leaf forms are always exposed, at least partially, to the atmosphere.
In other species, decreasing water depth favors a switch from submerged
to aerial leaf forms (Nohara and Kimura 1997, Titus and Sullivan 2001).
In our study, water depth decreased over the course of the growing season.
The early switch from surface to aerial leaves occurred while water depth
was deepest, while the late season switch from aerial to surface leaves occurred
when water depth was shallowest. Therefore, water depth is unlikely
the stimulus for heterophylly in lily pads. Low dissolved carbon dioxide
and oxygen stimulate a switch from submerged to floating leaves in Nuphar
variegata Dur. (Titus and Sullivan 2001). Although the shoot in water lily is
under water throughout the growing season, the mature leaf forms of water
lily are always exposed to the atmosphere. Furthermore, lily pads have a
ventilation system which forces air through the leaves down to the rhizome
and roots (Dacey 1981); thus, dCO2 and dO2 are probably not limiting factors
in this species.
Based on the results of the leaf-removal experiment, we hypothesize
that changes in the underwater light environment may stimulate the production
of aerial leaf forms. The appearance of aerial leaves coincided with
the time of maximum surface-leaf production, when surface leaves completely
covered the pond surface. The leaf canopy in terrestrial systems has
been shown to alter the quality of the irradiance below the canopy and affect
plant growth (Leyser and Day 2003, Smith and Whitelam 1997). With
186 Northeastern Naturalist Vol. 15, No. 2
respect to water lily, a canopy of surface leaves at the water’s surface may
affect two aquatic light parameters, namely light intensity (fluence rate)
and quality, and both have been shown to influence heterophylly in other
species (Goliber 1989, Leyser and Day 2003, Lin and Yang 1999, Schmidt
and Millington 1968). The results of our leaf-removal study suggest that
maintaining a degree of open water surface, thus potentially allowing
natural light irradiance to penetrate down to the rhizomes, significantly
repressed the appearance of aerial leaf forms (Figs. 1 and 5). This observation
also indicates that the site of stimulus perception is likely the shoot
and/or developing leaves. The slow gradual stimulation of aerial leaf forms
is likely associated with the increasing pond coverage by surface leaves,
which may affect the red/far-red ratio of light (Bodkin et al. 1980). This
mechanism, which is likely a phytochrome-mediated response, would produce
an adaptive leaf form irrespective of what is causing the change in the
light quality, either self shading or shading from other species (e.g., other
floating aquatic organisms such as algae or aquatic ferns).
The above hypothesis addresses the first switch in leaf form from surface
to aerial leaves. However, the second abrupt switch, when aerial leaf production
reverted back to surface leaf production, suggests that the plants are
responding to a different stimulus. Changes in seasonal photoperiods induce
changes in leaf form in some aquatic species (Cook 1969, Kane and Albert
1987, Wallenstein and Albert 1962). Therefore, we hypothesize that the second
change in leaf form, which occurred during the long days of summer, is
a response to changing seasonal photoperiods.
Future studies on heterophylly in white water lily should include the direct
manipulation of light parameters under controlled conditions and further
study of the effect of photoperiods. While our studies suggests that crowding
changes the light environment and thus influences aerial leaf production,
crowding may also influence other environmental parameters affecting leaf
development. To our knowledge, these parameters have not been addressed
in white water lily.
Heterophylly in the white water lily may be a response to changes in the
light environment. We suggest that the switch from surface to aerial leaf
forms early in the season allows the plant to maintain a high photosynthetic
rate by placing aerial leaves above the existing leaf canopy. Interestingly,
this response is not necessarily simple competition for light between different
plants, as a given shoot can be shaded by its own leaves, other lily pad
leaves, or even other vegetation. Potentially, this heterophyllic response
allows a given plant to maximize its photosynthetic capabilities at a given
time in the season regardless of the source of shading. As the surface leaves
reach senescence, they are replaced by aerial leaves that are fully exposed
to the sun. Late in the growing season, the ambient light levels begin to
decrease and the shoot switches back to producing surface leaves. One
potential benefit of reverting back to surface leaves is to allow the plant to
2008 P.J. Villani and S.A. Etnier 187
prolong the growing season. The warm water may protect the leaves from
frost by insulating them from large temperature fluctuations of the fall air,
although this remains to be studied.
Acknowledgments
The authors thank Eric Holm, Kyle Keller, Aster Gebrekidan, and Maisy the dog
for their assistance in data collection. Butler University’s Institute for Research and
Scholarship provided funding for this study, and Eagle Creek City Park generously
allowed us access to their ice-skating pond.
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