Annals of Botany 78 : 591–598, 1996
Interactive Effects of Soil Nutrients, Moisture and Sand Burial on the
Development, Physiology, Biomass and Fitness of Cakile edentula
J I A N H U A Z H A N G*
Department of Biology, McGill UniŠersity, 1205 AŠe. Dr. Penfield, Montreal, Que., H3A 1B1, Canada
Received : 14 August 1995
Accepted : 9 May 1996
The relative importance and interactive effects of nutrient supply, soil moisture content and sand burial on the
development, physiology, biomass allocation and fitness of Cakile edentula were examined under controlled
greenhouse conditions. Plant traits were more frequently affected by nutrient supply than by soil moisture content or
sand burial. Measurements on most plant traits also varied depending on the two or three way interactions among
the three environmental factors. Plants partially buried by sand had higher leaf chlorophyll concentration than those
unburied at the early stages of development, especially under low soil moisture content. High nutrient supply tended
to lower the leaf chlorophyll concentration of mature plants, and this effect was more pronounced under high as
compared to low soil moisture content. High nutrient supply enhanced the photosynthetic capacity of plants when
they were water stressed. With adequate soil moisture, high nutrient supply increased}decreased the photosynthetic
capacity of plants with}without previous experience of water stress. High nutrient supply increased the biomass
allocation to the root system of plants, especially at low soil moisture content. Partial sand burial also promoted
biomass allocation to the root system of plants grown at low soil moisture content.
# 1996 Annals of Botany Company
Key words : Soil nutrition, water supply, sand accretion, multiple stresses, biomass allocation, Cakile edentula.
INTRODUCTION
Plants inhabiting lacustrine or coastal sand dune systems
usually encounter substantial variations in soil nutrients,
moisture content and sand accretion (Barbour, de Jong
and Pavlik, 1985 ; Maun, 1985 ; Tyndall, Teramura and
Douglass, 1986 ; Hawake and Maun, 1988). Such variations
may occur at small spatial as well as temporal scales.
Normally, sand dune systems are poor in nutrient supply.
The reported nitrogen concentration of dune soils ranges
from 0±006–0±02 % by weight in Britain (Willis et al., 1959 ;
Hassouna and Wareing, 1964), 0±001–0±003 % along the
Pacific coast (Holton, 1980) and only trace amounts in the
sand dune along Lake Huron (Maun, 1985) as compared to
0±02–0±5 % in cultivated soils (Brady, 1974). Often, dune
plants are flexible in their requirements for essential nutrients
as the result of adaptation to low soil fertility (Hawake and
Maun, 1988 ; Zhang, 1995). However, deposition of organic
debris through wave action may periodically raise the soil
nutrient content to higher levels (van der Valk, 1974),
resulting in increased biomass and shoot}root ratio of dune
plants (Pemadasa and Lovell, 1974 ; Holton, 1980 ; Hawake
and Maun, 1988). These responses of plants were observed
even with the addition of very small amounts of N, P and K
(Hawake and Maun, 1988). The degree of fluctuation in
nutrient level of dune soils depends on daily and seasonal
variations in wind speed, wind direction and rainfall (van
der Valk, 1974 ; Maun, 1985).
* Present address : Research Center, Agriculture and Agri-Food
Canada, Harrow, ON, Canada N0R 1G0.
0305-7364}96}110591­08 $25.00}0
Although the moisture content of dune soils remains
relatively stable at depths greater than 20 cm (van der Valk,
1974), substantial variation occurs at shallow depths
depending on wind direction and velocity, and the distance
from the wave line (Tyndall et al., 1986). The variation can
be rather high so that it was reported that the sand at some
locations on the foredune along Currituck Bank, North
Carolina, USA, became completely dry to a depth of at least
20 cm by late June (Tyndall et al., 1986). The surface sand
dries out quickly even after rainfalls due to the low water
holding capacity of sand. The drying out of surface sand
affects the survivorship of seedlings of dune plants (Payne
and Maun, 1984 ; Tyndall et al., 1986). The growth of
established plants may also be affected as low soil water
potential reduces the leaf water potential, stomatal conductance, and nutrient uptake of dune plants (Tyndall et al.,
1986), which in turn lower the productivities of plants.
Sand movement represents another frequent environmental stress faced by dune plants. Maun (1985) monitored
sand accretion at three locations about 30–50 m apart on
the foredune along Lake Huron and observed about 6–10 cm
difference in depth of sand accretion between locations on
various dates of observation during a growth season.
Differences in sand accretion are more distinct between
dune systems. The annual sand accretion was 8±7 cm along
Lake Huron (Maun, 1985), 30 cm along Lake Michigan
(Olson, 1958) and 30 cm along the Atlantic coast of North
Carolina (van der Valk, 1974). Most dune plants show
increased growth when partially buried by sand (Maun and
Lapierre, 1984 ; Zhang and Maun, 1990, 1992 ; Yuan, Maun
and Hopkins, 1993 ; Zhang, 1995). For example, sand
# 1996 Annals of Botany Company
592
Zhang—EnŠironmental Response of Cakile edentula
accretion has been shown to increase the total chlorophyll
content of newly emerged leaves (Disraeli, 1984), number of
bundle sheath cells and photosynthetic rate (Yuan et al.,
1993), biomass (Wallen, 1980 ; Maun and Lapierre, 1984),
and seed production (Zhang and Maun, 1992) of various
dune species. In an artificial burial experiment, Zhang and
Maun (1992) observed enhanced shoot growth of young
seedlings of Cakile edentula (Bigel.) Hook within 1 week
after burial with both unwashed and washed sand. However,
the growth advantage of buried plants was maintained and
resulted in increased biomass and seed production for plants
buried with unwashed sand only. This result supports the
idea that the improved growth of buried plants is most likely
to result from a collective effect of sand burial and improved
soil nutrient and moisture status associated with sand
accretion (Olson, 1958 ; Marshall, 1965).
The effects of variations in the above three environmental
factors on the growth of dune plants have each been
investigated extensively, but few studies have examined
their integrative impact on plants. The lack of integration in
ecological studies has drawn criticisms from plant
physiologists. Green, Mitchell and Gjerstad (1994)
emphasized that results from a study examining the response
of plants to any environmental factor in isolation may not
be adaptable to a field situation because they only partially
reflect the norms of reaction of the plants in multiple
dimensions. Given that natural environments vary both
temporally and spatially at small as well as large scales (Bell
et al., 1986 ; Bell and Lechowicz, 1994), it would be more
relevant to study the response of plants to a set of major
environmental factors at varying levels. It is thus the
purpose of this study to investigate the relative importance
and combined effect of nutrient supply, soil moisture
content, and sand accretion on Cakile edentula, an annual
commonly found in the sand dune systems along the Great
Lakes (Maun, Boyd and Olson, 1990), with special emphasis
on the development, physiology, biomass allocation and
final fitness of the plant.
MATERIALS AND METHODS
Fruit of Cakile edentula were collected from plants growing
in a foredune area along Lake Huron at the Pinery Provincial
Park (43°15« N, 81°50« W) in southwestern Ontario, Canada
and stratified at 4 °C for 2 months before being set to
germinate in a greenhouse. On 27 Jan. 1993, 160 germinated
seeds (all germinated on that day) were individually
transplanted into 15 cm plastic pots filled with washed
commercial sand. The pots were randomly assigned to ten
blocks on two greenhouse benches with 16 plants within
each block. One or two weeks after transplanting (depending
on the treatment), eight different treatments were applied at
random to the 16 plants within each block (2 plants per
treatment). The eight treatments were a factorial combination of low and high levels of moisture, nutrient supply,
and sand burial. The low and high moisture treatments were
maintained by delivering 80 and 150 ml tap water per pot
(1 week after transplanting), respectively, at 2-d intervals
throughout the experiment. The low and high nutrient
treatments were maintained by weekly addition of 80 ml
and 150 ml of 20-20-20 (N-P-K) solution per pot (1 week
after transplanting) at 5 and 50 % of the recommended
doses, respectively. The low and high sand burial treatments
were maintained by burying the plants (2 weeks after
transplanting) with washed sand to 0 and 6 cm, respectively.
Zhang (1996) provided detailed information on the experimental procedures and ecological relevance of the
treatments.
Each plant was measured at weekly intervals for the
number of leaves, chlorophyll content and width of the fifth
newly emerged leaf, and the number of lateral branches. The
fifth newly emerged leaf was chosen for chlorophyll
measurement because it was well developed in plants across
treatments. Leaf chlorophyll content was determined using
the Minolta dual-wavelength chlorophyll meter (SPAD502, Minolta 1989). The SPAD values were then converted
to chlorophyll concentration following Monje and Bugbee
(1992). When plants had attained the maximum height 6
weeks after transplanting, the photosynthetic rate and water
use efficiency (WUE) of plants were measured twice for each
plant using a Li-cor 6200 (Li-Cor Inc, Lincoln, Nebraska,
USA) system. The first measurement was taken within
12–24 h after watering and was referred to as normal
photosynthetic rate and WUE. The second measurement
was taken after various periods following watering when a
plant started to show slight water stress (onset of wilting of
the first leaf) and was thus referred to as stressed
photosynthetic rate and WUE. Each plant was harvested
when there was no sign of further growth and the youngest
fruit was well developed. At harvest, the total number of
T     1. Summary (F Šalues) of repeated-measures analysis of Šariance for the number of leaŠes, leaf chlorophyll content,
leaf width and number of lateral branches of plants measured at weekly interŠals. Within subject effects are not presented as
time of obserŠation and its interaction with the three enŠironmental factors are all significant
Source
Nutrient (N)
Moisture (M)
Burial (B)
N¬M
N¬B
M¬B
N¬M¬B
Number of leaves
1661±67***
57±98***
0±01NS
7±11**
0±15NS
0±54NS
0±02NS
Chlorophyll content
10±27**
33±09***
16±46***
5±99*
4±00*
4±97*
0±13NS
Leaf width
1007±89***
112±13***
1±88NS
4±53*
0±01NS
4±27*
0±63NS
Number of branches
170±78***
54±56***
2±87NS
0±96NS
0±56NS
0±80NS
0±08NS
*** Significant at P ! 0±001, ** significant at P ! 0±01, * significant at P ! 0±05 and NS not significant (P " 0±05).
Zhang—EnŠironmental Response of Cakile edentula
Number of leaves
200
A
B
C
D
E
F
G
H
150
100
50
Chlorophyll (mg m–2)
0
600
525
450
375
300
30
Leaf width (mm)
fruits (lower­upper) were counted and the dry weight
(50 °C for 52 h) of fruits, shoot­leaves, roots and total
biomass were measured. Dry matter allocation to each
component and root}shoot ratio were then calculated. The
mean fruit mass was estimated by dividing the total fruit
weight by fruit number. The abortion rate of flowers was
calculated based on measurements on the total number of
flowers and fruit segments.
The collected data were screened for outliers by identifying
data points that were apparently isolated from the main
cluster(s) of measurements on a given variable. The identified
outliers were double checked for potential mistakes made
during measurement or data entry. Uncorrectable data
points were then considered as outliers and eliminated from
analysis. Six measures on stressed photosynthesis and WUE
were excluded (Table 1). The six excluded measurements on
stressed photosynthesis and WUE were randomly distributed among different treatments. Each plant variable was
transformed (angular for proportional data and natural log
for the others) and then analysed using a three way
ANOVA (Proc GLM, SAS Institute Inc., 1985). The weekly
measurement data were analysed using repeated measures
analysis of variance (Proc GLM, SAS Institute Inc., 1985).
593
24
18
12
RESULTS
DeŠelopment
Seedlings used in this study had the same number of leaves
during the first 2 weeks after transplanting (Fig. 1). The
effect of treatments was seen 3 weeks after transplanting
or 1–2 weeks after treatment. Plants grown at high nutrient
supply produced significantly more leaves than those at low
nutrient supply under both moisture rich and poor
conditions (Table 1, Fig. 1). When plants reached their
maximum size about 6 weeks after transplanting, the
difference in leaf number between plants grown at high and
low nutrient supply could be three to four-fold. Higher soil
moisture content also corresponded to more leaves per
plant. However, its effect depends on the level of nutrient
supply (Table 1). Under nutrient rich conditions, plants
produced more leaves at high than low soil moisture
content. Under nutrient poor conditions, there was little
difference in the number of leaves between plants grown
under high and low soil moisture content. The number of
leaves per plant was not affected by sand accretion alone or
its interaction with the other two factors throughout the
experiment (Table 1, Fig. 1). Although the burial treatment
2 weeks after transplanting buried about 70 % of the above
ground part (including some older leaves) of the plants,
there was little difference in leaf number between the
unburied and buried plants 1 week later (3 weeks after
transplanting) apparently due to enhanced leaf production
of the latter.
The chlorophyll concentration of leaves varied significantly depending on the three environmental factors and
their two-way interactions (Table 1). Under moisture rich
conditions, unburied plants had a slightly higher leaf
chlorophyll concentration than buried ones in the first 4
weeks after transplanting (Fig. 1). Thereafter, there was a
Number of branches
6
14
11
8
5
2
0
1
2
3
4
5 6 7 0 1 2 3
Weeks after planting
4
5
6
7
F. 1. Number of leaves (A, B), chlorophyll content (C, D), leaf width
(E, F) and number of lateral branches (G, H) of Cakile edentula under
moisture rich (A, C, E, G) and moisture poor (B, D, F, H) treatments
on different dates of observation. (E) Nutrient rich ; (D) nutrient
poor ; (——), buried ; (– –) unburied.
substantial increase in leaf chlorophyll concentration of
plants grown at low nutrient supply so that they maintained
greater leaf chlorophyll concentrations than those grown at
high nutrient supply across burial depths. Under moisture
poor conditions, high leaf chlorophyll concentration was
observed in unburied plants during the first 5 weeks after
transplanting. Plants grown at high nutrient supply began
to show a lower leaf chlorophyll concentration than those at
low nutrient supply 6 weeks after transplanting as observed
in moisture rich conditions. Plants at given levels of nutrient
supply and sand burial had higher leaf chlorophyll concentrations under moisture poor than moisture rich
conditions at the early stages (e.g. the first 5 weeks after
planting) of development (Fig. 1).
Leaf width depended significantly on nutrient supply and
soil moisture content (Table 1) with plants grown at high
nutrient supply and soil moisture content having wider
leaves for both the buried and unburied plants (Fig. 1). The
effect of soil moisture content on leaf width was more
594
Zhang—EnŠironmental Response of Cakile edentula
T     2. Summary (F Šalues) of ANOVA for physiological traits of Cakile edentula measured 6 weeks after planting
Variable
Nutrient (N)
Normal photosynthesis
Normal WUE
Stressed photosynthesis
Stressed WUE
0±01NS
6±56*
97±87***
5±93*
Moisture (M)
Burial (B)
N¬M
N¬B
M¬B
N¬M¬B
0±79NS
0±30NS
5±84*
0±43NS
1±17NS
0±58NS
5±76*
0±71NS
6±34*
2±17NS
5±09*
0±35NS
1±18NS
0±08NS
0±01NS
4±20*
0±01NS
3±26NS
7±60**
0±41NS
0±89NS
0±01NS
0±20NS
1±18NS
*** Significant at P ! 0±001, ** significant at P ! 0±01, * significant at P ! 0±05 and NS not significant (P " 0±05).
A
B
Normal WUE (µmol mmol–1)
Normal photosynthesis
(µmol m–2 s–1)
22
19
16
13
10
E
F
11
8
5
2
C
D
G
H
2.4
2.0
1.6
1.2
Stressed WUE (µmol mmol–1)
Stressed photosynthesis
(µmol m–2 s–1)
14
2.8
0
6
0
6
5
4
3
2
0
6
Depth of sand accretion (cm)
6
0
6
F. 2. Bar charts showing the effect of nutrient supply (+, nutrient rich ; *, nutrient poor), soil moisture content (moisture rich, A, C, E, G and
moisture poor, B, D, F, H) and sand burial on normal photosynthesis (A, B), normal WUE (C, D), stressed photosynthesis (E, F) and stressed
WUE (G, H) of Cakile edentula. Vertical bars indicate the standard errors.
pronounced at high than low nutrient supply. Sand burial
alone did not affect plant leaf width significantly. Although
there was a significant interaction between sand burial and
soil moisture content (Table 1), the magnitude was too
small because it is difficult to depict any general trend
(Fig. 1).
Plants grown at high nutrient supply or soil moisture
content produced significantly more lateral branches regardless of sand accretion (Table 1, Fig. 1).
Physiology
The photosynthetic rate of plants shortly after watering
(normal photosynthetic rate) depended on the joint effect of
nutrient supply and soil moisture content (Table 2). Plants
that had been continuously grown in moisture rich
conditions had higher photosynthetic rates at high than low
nutrient supply (Fig. 2). Conversely, plants that had been
grown continuously in moisture poor conditions had a
higher photosynthetic rate at low than high nutrient supply.
The water use efficiency of plants shortly after watering
(normal WUE) varied with nutrient supply only (Table 2)
with those under nutrient rich conditions being significantly
more efficient in using water for photosynthesis than those
under nutrient poor conditions, especially when soil moisture content is low (Fig. 2).
The three environmental factors and their interactions
affected the photosynthetic rate of plants more when there
was a water stress (Table 2). In general, plants had a
significantly higher rate of photosynthesis (stressed photosynthetic rate) under nutrient rich than poor conditions
(Fig. 2). However, the difference between plants grown at
high Šs. low nutrient supply was smaller under moisture
poor than moisture rich conditions. This is because plants
that had been grown under moisture poor conditions were
able to maintain higher rates of photosynthesis at low
nutrient supply than plants that had been grown under
moisture rich conditions. Sand burial reduced the photo-
Zhang—EnŠironmental Response of Cakile edentula
595
T     3. Summary (F Šalues) of ANOVA for biomass and fitness traits of Cakile edentula measured at harŠest
Variable
Nutrient (N)
Total biomass
Allocation to shoot
Allocation to root
Root}shoot ratio
Allocation to fruits
Number of fruits
Abortion rate
Weight of fruits
Mean fruit weight
Moisture (M)
8875±61***
3±26NS
8±34**
11±82***
1±27NS
7083±71***
2±75NS
8016±22***
5±58*
27±14***
7±74**
0±34NS
0±49NS
3±09NS
30±28***
8±03**
23±38***
3±23NS
Burial (B)
6±74**
12±46***
29±36***
1±51NS
4±94*
5±63*
10±55**
0±29NS
2±41NS
N¬M
N¬B
M¬B
N¬M¬B
23±96***
0±12NS
2±69NS
2±57NS
4±68NS
84±17***
0±34NS
39±78***
13±02***
2±63NS
0±27NS
1±69NS
0±09NS
0±36NS
18±94***
0±08NS
0±89NS
28±46***
6±87**
0±27NS
7±93**
7±81*
10±73**
1±87NS
0±02NS
0±01NS
1±61NS
5±79*
10±56**
0±22NS
0±51NS
4±91*
0±01NS
0±01NS
0±51***
0±63NS
A
B
0.22
Root/shoot ratio
12
8
4
G
H
17
14
11
8
M
N
525
350
175
0
0.16
0.13
50
I
J
47
44
41
0
6
0
6
6.0
O
P
4.5
3.0
1.5
0
44
E
F
K
L
Q
R
41
38
35
32
38
Total weight of fruits (g)
Number of fruits
700
0.19
0
6
0
6
Depth of sand accretion (cm)
Abortion rate of flowers (%)
20
D
0.10
Allocation to fruits (%)
Allocation to roots (%)
0
C
Mean fruit weight (mg)
Plant biomass (g)
16
Allocation to shoot (%)
*** Significant at P ! 0±001, ** significant at P ! 0±01, * significant at P ! 0±05 and NS not significant (P " 0±05).
44
38
32
26
20
12
9
6
3
0
0
6
0
6
F. 3. Bar charts showing the effect of nutrient supply (+, nutrient rich ; *, nutrient poor), soil moisture content (moisture rich, A, C, E, G,
I, K, M, O, Q and moisture poor, B, D, F, H, J, L, N, P, R) and sand burial on biomass and fitness traits of Cakile edentula. Vertical bars indicate
the standard errors.
synthetic rate of plants under moisture poor but not
moisture rich conditions. The stressed water use efficiency of
plants varied significantly with soil nutrition and the level of
sand burial (Table 2). High soil nutrient supply significantly
enhanced the stressed water use efficiency of unburied but
not buried plants under both low and high moisture
conditions (Fig. 2).
Biomass and fitness
Measurements on the biomass and fitness of plants varied
significantly with the three environmental factors and their
interactions (Table 3). In general, the total biomass of
plants increased significantly with nutrient supply under
both moisture rich and moisture poor conditions (Fig. 3).
At high nutrient supply, plants under moisture rich
conditions also had significantly greater biomass than those
under moisture poor conditions. Sand burial did not have
apparent effects on plant biomass except at low soil nutrient
level under moisture poor conditions, where a slight increase
was observed in the buried plants. Plants grown at high
nutrient supply had greater root}shoot ratios than those at
596
Zhang—EnŠironmental Response of Cakile edentula
low nutrient supply only under moisture poor conditions.
Buried plants, at a given level of soil nutrients, also had
significantly greater root}shoot ratio, than unburied ones
under moisture poor but not moisture rich conditions (Fig.
3). Dry matter allocation to shoots and fruits of plants did
not show any clear trend of variation with any of the three
environmental factors. A substantial increase in the amount
of dry matter allocated to the root systems was observed in
plants grown at a given level of soil nutrients under moisture
poor conditions as a result of sand burial (Fig. 3).
Under moisture poor conditions, the abortion rate of
flowers was significantly higher for unburied plants or those
grown at high soil nutrient level (Fig. 3). Under moisture
rich conditions, variations in the abortion rate of flowers
appeared to be independent of the three environmental
factors. The number of fruits produced by a plant increased
significantly with nutrient supply under both moisture rich
and poor conditions. While plants grown under nutrient
poor conditions had a similar number of fruit regardless of
soil moisture content and sand burial, those grown in
nutrient rich conditions produced more fruit at high rather
than low levels of soil moisture or sand burial. The total
weight of fruits increased with soil nutrient level under both
moisture rich and poor conditions, and with soil moisture
level under nutrient rich conditions. Sand burial did not
have any significant effect on the total weight of fruits.
Plants tended to produce small fruits when buried under
nutrient rich conditions within a given soil moisture regime,
or grown at moisture rich conditions at a given depth of
sand burial. Buried plants grown at low soil nutrient levels,
however, tended to produce larger fruits than unburied ones
under both moisture rich and poor conditions (Fig. 3).
DISCUSSION
Temporal and spatial environmental variations are expected
to occur in almost any ecosystem (Bell et al., 1986). To
understand the impact of a given environmental factor on
plants, it would be most relevant to study its effects relative
to other abiotic or biotic factors. Although sand dune
systems undergo drastic environmental changes even on a
daily basis (Barbour et al., 1985 ; Maun, 1985), and it has
been recognized that plant growth may be affected by a
group of interacting factors (Olson, 1958 ; Marshall, 1965 ;
Zhang and Maun, 1992), few studies have examined the
relative importance and integrative effect of these environmental factors on dune plants. Among the 17 (a total
of traits listed in Tables 1, 2, and 3) plant variables
measured in this study, 13 were significantly affected by
nutrient supply, ten by soil moisture content and eight by
sand accretion as main factors. At P ¯ 0±05, the chance of
mistakenly identifying a non-significant response of plant is
about 1 out of 17 variables. Thus, the differences between 13
out of 17 and 10 or 8 out of 17 variables are not likely to
result from chance alone, suggesting that nutrient supply is
a significantly more important factor than soil moisture
content or sand burial on the growth of Cakile edentula
under field conditions where variations in multiple factors
occur.
Two or three way interactions between the three environmental factors are often observed (14 out of 17) and
some of the results are useful to explain divided opinions
between researchers. For example, it was reported by
Disraeli (1984) that the concentration of chlorophyll in
leaves of Ammophila breŠiligulata increased exponentially
with increased sand accretion. Using the same species, Yuan
(1991) observed a decrease in leaf chlorophyll concentration
with increasing depth of sand burial. According to the
current study, both increased and decreased leaf chlorophyll
may occur as one of the possible responses of plants to sand
accretion under different regimes of environmental
conditions (Fig. 1). It is thus reasonable to assume that
differences in the combination of environmental factors
may be responsible for the contradicting results obtained in
these two previous studies. Buried plants of C. edentula
generally had lower leaf chlorophyll concentrations than
unburied ones at earlier stages of development of the plants
(Fig. 1), which may be a direct effect of compensatory
growth commonly found in plants. Increased biomass and
fitness of plants in response to moderate defoliation are
typical examples of compensatory growth (Belskey, 1986,
1987 ; Oba, 1994). Sand burial also reduces the total amount
of photosynthetic area or the above ground part of plants
and thus may practically have a similar effect as defoliation
that initiates a process of compensatory growth of the target
plants. Zhang and Maun (1992) provided indirect support
for this hypothesis by showing that the improved shoot
growth within one week after the burial of C. edentula
seedlings was not triggered by nutrient addition or the
response of plants to the dark condition imposed by the
deposited sand. While the compensatory growth of plants
may make up the reduced photosynthetic area and balance
the carbon and nutrition requirements of plants, overcompensation in some species or under a certain set of
circumstances (Oba, 1994) may result in deficient supply in
growth materials and, in the case of buried plants of C.
edentula, low chlorophyll concentration of the newly
developed leaves.
The majority of the evidence showing improved growth
of buried plants is based on biomass and final fitness, while
far fewer studies have examined the physiological response
of plants to sand burial. A recent study by Yuan et al. (1993)
showed that buried plants of A. breŠiligulata and
CalamoŠilfa longifolia generally had higher net photosynthetic rates than unburied ones. This result is probably
not due to improved moisture conditions in the root zones
because the water potential of leaves of both buried and
unburied plants did not differ significantly. Yuan et al.
(1993) attributed the increased photosynthetic rate of buried
plants to thicker leaves and a great total area of mesophyll
cells exposed to intercellular spaces per unit leaf area
(Ames}A). A larger Ames}A value has been observed to
increase CO absorbtion (Nobel and Walker, 1985). This
#
hypothesis is relevant because Yuan et al. (1993) used
established adult plants in their study. The well developed
root system of established plants may minimize the limiting
effect of soil nutrients and moisture on photosynthesis. For
young seedlings or annual plants, however, the nutrition
and moisture status of the microhabitat may be crucial to
Zhang—EnŠironmental Response of Cakile edentula
their photosynthetic abilities. In the current study, the
photosynthetic rate of plants was measured shortly after
watering, which mimics the soil conditions after rainfall or
big wave action, and when plants had just started to show
a sign of water stress, which mimics the soil conditions on
dry and hot summer days. The results showed that the
photosynthetic capacity of a plant depended on sand burial,
soil nutrition, and the current as well as the history of soil
moisture conditions. Sand burial affected the photosynthesis
of plants mainly under conditions where water stress was a
recurrent event (stressed photosynthesis). This may occur
during the summer or before the majority of the root system
of a plant reaches the 20 cm depth. In these cases, however,
buried plants tend to have a lower rather than higher
photosynthetic rate than unburied ones (Fig. 2). It then
follows that sand burial alone is not likely to enhance the
photosynthetic capacity of plants. Zhang and Maun (1992)
also suggested that sand burial generally did not stimulate
long term positive responses of plants unless the deposited
sand contained a certain amount of nutrients. Even so,
variations may occur depending on soil moisture status.
Nutrient addition increases the photosynthetic capacity of
water stressed plants no matter if they have or have not
experienced any water stress previously (stressed photosynthesis in Fig. 2). Provided with adequate water (e.g.
after rainfall or big waves), nutrient addition tends to
increase or decrease the photosynthetic capacity of plants
that have not or have experienced water stress previously
(normal photosynthesis in Fig. 2). Therefore, nutrient
addition due to sand accretion or deposition of organic
debris may affect the growth of dune plants to various
degrees depending not only on the current but also the
history of soil moisture status.
The pattern of biomass allocation of plants is one of the
major focuses of contemporary ecological studies. Evidence
from a large body of literature shows that plants under
nutrient or moisture poor conditions often have a large root
to shoot ratio (Sultan and Bazzaz, 1993 a, b ; Green et al.,
1994). The response of C. edentula to soil nutrient and
moisture content contradicted this generalization in that
plants tended to have a greater root to shoot ratio in
nutrient rich than in nutrient poor conditions, especially
when soil moisture content had been continuously low (Fig.
3). It is recognized that the root-bound growth of plants
that commonly occurs in greenhouse experiments may have
caused abnormal distribution of biomass between the above
and below ground parts of the plants in this study. If this
was really the case then plants grown under nutrient rich
conditions would be more likely to be root-bound and thus
tend to have a small root to shoot ratio, especially at high
soil moisture content without sand accretion. This is not
supported by the results from this study. According to
Zhang (1993), the root to shoot ratio of C. edentula grown
under a single testing environment is negatively related to
overall biomass regardless of the age of plants. This
correlation does not explain the results of the current study
either because high nutrient supply resulted in large plants
associated with higher root to shoot ratios. Green et al.
(1994) reported that nitrogen nutrition and drought
interacted to determine the root to shoot ratio of Pinus
597
taeda L. seedlings. While high nitrogen supply decreased
the root to shoot ratio of P. taeda seedlings, the effect of
nitrogen decreased with the length of drought treatment and
was no longer observable after 10 d water stress (Green et
al., 1994). It was also observed that starch metabolism to
support growth was fast in water stressed plants under high
nitrogen supply, but was limited under low nitrogen supply
(Green et al., 1994). Perhaps efficient starch metabolism of
C. edentula plants at high nutrient supply may have enabled
them to maintain a greater root biomass than plants at low
nutrient supply under water stressed condition. Biomass
allocation to roots was also observed to increase with sand
burial under moisture poor but not moisture rich conditions
(Fig. 3). Although the underlying mechanisms are as yet
unknown, the result demonstrates that the effect of an
environmental factor on biomass allocation of plants may
be altered by variation in another factor. In fact, the
interaction between environmental factors on plant biomass
allocation is an important but poorly addressed question
(Green et al., 1994).
Although sand accretion affected the total biomass of
plants (P ! 0±01) according to the analysis of variance, the
effect was perhaps not substantial biologically (Fig. 3).
However, buried plants did produce significantly more
fruits than unburied ones, especially at high soil nutrition.
A similar result has also been reported by Zhang and Maun
(1992). This was partially achieved through a more
economical reproductive strategy of the buried plants, as
they tended to have a lower abortion rate of flowers than
the unburied ones, and through a trade off between fruit
number and weight (Fig. 3). Compensatory growth following sand burial would be another option, as it is
commonly observed that defoliated plants tend to increase
their final fitness (Belskey, 1986, 1987).
Because plants are generally subjected to multiple stresses
under field conditions, they would possess the ability (as the
result of natural selection) to adjust their growth according
to the levels of all the major environmental factors involved.
Interactions between abiotic and}or biotic factors may
activate plant responses that are not normally observed
under a single testing environment. These responses perhaps
have significant ecological and evolutionary values and
should receive more attention.
A C K N O W L E D G E M E N TS
I thank the Natural Sciences and Engineering Research
Council of Canada for a post-doctoral fellowship and Dr
M. J. Lechowicz at the Department of Biology, McGill
University for helpful discussions on the project. Comments
by Dr I. A. Ungar and an anonymous reviewer on an early
draft of the manuscript are highly appreciated.
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