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Flora 209 (2014) 279–284
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Morphological changes and resource allocation of Zizania latifolia
(Griseb.) Stapf in response to different submergence depth and duration
a,d a,b,d a c,e,∗
Qiulin Wang , Jingrui Chen , Fan Liu , Wei Li
a
Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, Hubei 430074, China
b
Institute of Soil and Fertilizer, Fujian Academy of Agricultural Sciences, Fuzhou, Fujian 350013, China
c
Hubei Key Laboratory of Wetland Evolution & Ecological Restoration, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, Hubei 430074, China
d
University of Chinese Academy of Sciences, Beijing 100039, China
e
Key Laboratory of Ecological Impacts of Hydraulic-Projects and Restoration of Aquatic Ecosystem of Ministry of Water Resources, Institute of
Hydroecology, Ministry of Water Resources and Chinese Academy of Sciences, Wuhan 430079, China
a r a
t i b s
c l e i n f o t r a c t
Article history: Plants around ponds, rivers and lakes are subjected to long-term partial or complete submergence. When
Received 1 June 2013
they are flooded, water level affects the plants simultaneously with duration of submergence. Separate
Accepted 8 March 2014
and interactive effects of water level and duration on the growth of the herbaceous perennial Zizania
Edited by R. Lösch
latifolia (Poaceae) were investigated by exposing the plants in greenhouse water tanks to submergence
Available online 27 March 2014
in different water depths and for different time-spans. The plants exhibited great shoot elongation upon
submergence and prolonged flood duration, and the basal tiller number of the species decreased with
Keywords:
higher water levels. Submergence treatment advanced the flowering date and increased the inflorescence
Growth elongation
number. Plant total biomass did not differ among all the treatments, while the root:shoot ratio decreased
Root:shoot ratio
with increased water level, prolonged duration of submergence and their interaction. The high plasticity
Submergence duration
Water level in morphology and shifts in reproductive strategy and biomass allocation enabled the Zizania plants
Zizania latifolia to survive the compound effect of flooding height and duration. This may explain the occurrence of this
Wetland plants species in habitats subjected to long-term flooding. The results obtained in this experiment will contribute
to understanding the impact of flooding dynamics on plants and the ways of adaptation responses to
prolonged waterlogging.
© 2014 Elsevier GmbH. All rights reserved.
Introduction (Carter Johnson, 2000), decreased vegetation cover (Siebel, 1998),
and eutrophication (Thoms, 2003).
An essential habitat parameter in aquatic and emergent plant Coping with the harsh environmental conditions related to
communities is the stress of flooding. High water level related to the flooding, wetland plant species are adapted to increase sur-
excessive rainfall or discharge of melting snow and ice, and poor vival and reproduction. Morphological responses of some species
land drainage can severely affect plant growth and survival (Blom to flooding are shoot elongation and formation of adventitious
et al., 1994; Blom and Voesenek, 1996). Direct effects of flood- roots (Busch et al., 2004; Cooling et al., 2001; Kende et al., 1998).
ing on plants include restricted oxygen exchange, hampered soil In contrast, other plants are able to tolerate complete submer-
water movement (Hughes et al., 2001), and burial of individuals gence enduring with reduced or no growth the time until water
by sediments (Karrenberg et al., 2003; Marigo et al., 2000). Indi- level drops (Bailey-Serres and Voesenek, 2008; Blom et al., 1994;
rect effects are creation of bare substrates due to sedimentation Parolin, 2009). Physiologically, fluctuations of water level influ-
ence the photosynthetic performance of the plants, leading to
altered resource-allocation patterns and subsequent change of
community productivity (Hogeland and Killingbeck, 1985; Junk and
∗ Piedade, 1993). Moreover, changes in reproductive strategies have
Corresponding author at: Wuhan Botanical Garden, Chinese Academy of Sci-
also been detected under flooding conditions, including increased
ences, Wuhan, Hubei 430074, China. Tel.: +86 27 87510140; fax: +86 27 87510251.
E-mail address: [email protected] (W. Li). flower number with prolonged inundation duration and decreased
http://dx.doi.org/10.1016/j.flora.2014.03.006
0367-2530/© 2014 Elsevier GmbH. All rights reserved.
Author's personal copy
280 Q. Wang et al. / Flora 209 (2014) 279–284
vegetative reproduction (Lowe et al., 2010; Mony et al., 2010). Such October 5th, 2010. All plants were designed to grow for 100 d and
ecophysiological responses lead to individual survival, continued divided into 7 groups. In the control group, the rooting substrate
growth and generative reproduction (Blom and Voesenek, 1996). was water-saturated to the soil surface of the pot during the entire
The flooding regime is a major determinant of plant community experimental period (June 25th–October 5th). Other submergence
development and of patterns of plant zonation in wetlands (Bunn treatments were as follows: (1) For the 100 d submergence treat-
et al., 1997). With a gradually rising water level in the field, plants ment, two groups of shoots were submerged to the fixed water
in the lower areas experience earlier, longer and deeper submer- level (50 cm, 100 cm) in a water tank during the entire experimen-
gence, and vice versa. Parameters of the water regime itself (water tal period (June 25th–October 5th). (2) For the 70 d submergence
depth, duration, timing, frequency, etc.) and its impact on the plants treatment, two groups of shoots were cultivated on soil water-
(flooding depth and duration) exert impact on plant growth. Thus, saturated up to the soil surface for 15 d (June 25th–July 10th),
plants in flood-prone habitats are interactively affected by water then submerged to the fixed water level (50 cm, 100 cm) from July
depth and submergence duration. Much attention has been paid to 10th to September 20th, and thereafter readjusted to be emerged,
the impact of water depth on the growth of plant species (Hussner growing on the water saturated substrate for another 15 d (Sep
and Meyer, 2009; Lowe et al., 2010; Mony et al., 2010; Voesenek 20th–October 5th). (3) For the 40 d submergence treatment, two
et al., 2006). Relatively little is known about plant survival and groups of shoots were cultivated on the water-saturated soil for
growth in response to the combined effect of water depth and flood 30 d (June 25th–July 25th), then submerged to the fixed water level
duration (Vreugdenhil et al., 2006). Relevant investigation may help (50 cm, 100 cm) between July 25th and September 5th, and read-
to further explore the adaptive responses of plants to flooding. justed to be emerged, growing on water saturated substrate for
In the present work, we investigated the combined effects of another 30 d (September 5th–October 5th).
water depth and flood duration on an important macrophyte, Ziza- Every treatment was performed with six replicates and neces-
nia latifolia, that is found at river banks and lake shore sites in East sary measures were taken to support the plants to prevent lodging
Asia to address the following questions: (1) Does water depth work upon readjustment after submergence. The tank was filled with
interactively with flood duration? (2) And if yes, how does the plant water from nearby Donghu Lake, and water level was monitored
respond to their interaction? every 2 days. Water was added to the tank to keep the water levels
constant.
During the experiment, the blooming date of each inflorescence
Materials and methods
was recorded at the first sign of flowering and the inflorescence
number of each plant was monitored till the end of the experi-
Plant species description
ment. After submergence treatment, plant height (from the soil
surface to the tip of the longest leaf) and basal tiller number per
Zizania latifolia (Griseb.) Stapf (Oryzeae/Poaceae), wild rice, is
pot were determined. At the end of the experimental treatments all
a perennial aquatic macrophyte with well-developed rhizomes.
plants were harvested immediately and gently washed free of soil.
The species is widely distributed in ponds, rivers and lakes of
The plant biomass was separated into above-ground and below-
the middle-lower reaches of the Yangtze River, China. In ponds ◦
ground parts and dried at 80 C for 48 h to constant weight. The
or on river banks, the species grows to about 150–300 cm and its
root:shoot ratio (below-ground biomass/above-ground biomass)
usual rooting depth is about 20–30 cm. It reproduces sexually from
was calculated for each plant.
seedlings and/or asexually by rhizomes producing new tillers (Li,
1995). Z. latifolia has been historically domesticated and cultivated
in China as an aquatic vegetable under infection by Ustilago escu- Statistical analysis
lenta P. Henn (Guo et al., 2007). Its many elite varieties with high
quality grain and resistance to sheath blight make it a potential Statistical analysis was conducted with SPSS (Version 13.0).
valuable source of genetic material to improve the germplasm for Plant height, tiller number, total biomass and root:shoot ratio
modern rice breeding (Shen et al., 2011). were analyzed with two-way analysis of variance (Brock and
Casanova, 1997). The inflorescence number per plant had a non-
normal distribution and was analyzed with the non-parametric
Experimental design
Dunn’s Q test. All other plant data were tested for normality and
homogeneity of variances to meet the assumption of ANOVA, and
The experiment was conducted by cultivating Z. latifolia plants
transformed if necessary. Significant differences were identified by
in water tanks in a greenhouse of Wuhan Botanical Garden (WBG),
◦ ◦ Student–Newman–Keuls (SNK) multiple comparisons. Significance
Wuhan, China (30 33 N, 114 24 E) in the summer of 2010. The
was set at the 0.05 probability level.
greenhouse had several big windows and was well-ventilated to
make sure that inside temperatures equaled more or less out-
side temperatures. Vegetative shoots with few adventitious roots Results
were collected from ponds in WBG and planted into the plastic
pots (25 cm diameter × 15 cm height), one shoot per pot, culti- Plant height and tiller number
vated under natural temperatures and watered periodically. The
pots were filled with fertile sediment from the site wherefrom All experimental plants survived the treatments, and there was
the plants were collected (organic matter: 0.15% ± 0.02%; total no interaction between water level and duration affecting plant
nitrogen: 2.4% ± 0.06%; total phosphorus: 0.08% ± 0.005%; sand: height and tiller number (Table 1). The internode number of Z. lat-
10.2% ± 0.2%; silt: 78.8% ± 3.3%; clay: 11.1% ± 3.1%). After approxi- ifolia is about 5–8, the number of nodes and internodes did not
mately two-month growth, plants of uniform height (109 ± 5.4 cm) differ among groups. Plant height was promoted by water depth
were selected for experiment. and submergence duration. Compared to the control (average
To simulate the habitat conditions of concern, the experiment height: 135 cm), a significant stimulation of water level treat-
was set up as a two-way fixed factor experiment (Shen et al., ment on Z. latifolia plant height was observed (P < 0.001, Table 1).
2011). The two factors were water level (50 cm, 100 cm, water Plant height increased significantly after the water level was raised
surface above the soil surface of pot) and submergence duration (Fig. 1), reaching a maximum height in the 100 cm water depth-
(40, 70, 100 d). The experiment started on June 25th and ended on 100 d submergence duration treatment (maximal total height:
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Q. Wang et al. / Flora 209 (2014) 279–284 281
Table 1
Results (F value) of two-way ANOVA on the effect of water level (W), submergence duration (D) and their interaction on shoot height, tiller number, total biomass and
root:shoot ratio.
Source of variation Plant height Tiller number Total biomass Root:shoot ratio
ns
W 47.777*** 16.153*** 2.114 15.726***
ns ns
D 4.699* 1.964 0.091 27.026***
ns ns ns
W × D 0.103 0.546 0.358 4.387*
***, P < 0.001; **, P < 0.01; *, P < 0.05; ns, P > 0.05.
Contr ol 50cm 100cm
300 a a 260
b 220 c
ight (cm) c he 180 cd
Plant d 140
100 Control 40 70 100
Duration (d)
Fig. 1. Plant height of Zizania latifolia in response to varying water depth and submergence duration, means ± S.E.
255.3 ± 14.3 cm). A significant effect of submergence duration on no significant difference from the control, and tiller number of both
plant height was also found (P < 0.05, Table 1). Plant height did not were significantly higher than that of the 100 cm water level treat-
differ significantly between 70 d and 100 d duration of submer- ment (P < 0.001).
gence, but was greater than that of 40 d under the same water
level and distinctly higher than the control. Tiller number was Flowering
significantly affected by high water levels and decreased under
submerged conditions. No significant differences between plant
Flowers were produced under all the treatments. Flowering in
groups were found with respect to submergence duration (Fig. 2
the control treatment began on the 80th day after initiation of
and Table 1). Tiller number of the 50 cm water level group showed
the experiment. In both 50 cm and 100 cm water level treatments,
1.1 Control 50cm 100cm
0.9 a a a ab a 0.7
Tiller number b 0.5 b
0.3 Control 40 70 100
Duration (d)
Fig. 2. Tiller number (log 10 transformed) of Zizania latifolia in response to varying water depth and submergence duration, means ± S.E.
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282 Q. Wang et al. / Flora 209 (2014) 279–284
Control
50 cm-40 d
50 cm-70 d
50 cm-100 d
100 cm-40 d
100 cm-70 d
100 cm-100 d
0 5 0 5 0 5 0 5 0 6 6 7 7 8 8 9 9 10
Days since start of experiment (d)
Fig. 3. Flowering days since start of experiment for each treatment.
flowering started significantly earlier than in the control plants Discussion
(Fig. 3). The water level gradient significantly affected the inflo-
rescence number (P = 0.005) whereas submergence duration did Flooding is one of the most common and widespread natural
not (P = 0.561). Multiple comparisons showed that both 50 cm and stresses to plants. There can be an increase in negative effect on
100 cm water depths significantly increased the inflorescence num- plant survival and growth as the length of inundation time increases
ber of the plants (Fig. 4). (Blom and Voesenek, 1996; He et al., 1999). Adaptive responses in
morphology and reproductive strategy are developed in wetland
plants to minimize the effects of this stress.
Biomass partitioning The height of Zizania latifolia increased with increasing water
level. Strong elongation growth of shoots documented great sen-
Total biomass of the plant was not affected by either water level sitivity of wild rice to the rise of water level. Elongation growth
or submergence duration (Fig. 5 and Table 1). Significant differences enabled the plant upper parts to escape the flooding stress, expos-
of root:shoot ratio resulted from different water levels (P < 0.001), ing leaf blades to the atmosphere so that gas exchange could
submergence duration (P < 0.001) and their interaction (P < 0.05) continue (Kende et al., 1998). Like the submergence-induced peti-
(Fig. 6 and Table 1). The root:shoot ratio decreased significantly as ole elongation (escape strategy) in Rumex palustris, the physiology
the submergence duration prolonged and water depth increased. of submergence-induced shoot elongation in Z. latifolia may be
linked to entrapment of the gaseous plant hormone ethylene and
mediated by the interaction of ethylene and gibberellin (Musgrave
et al., 1972; Voesenek et al., 2004). According to Kende and co-
workers ethylene concentration inside submerged internodes may 3.0
−1
C ontrol increase 50-fold, from approximately 0.02 to 1 l l , and applica-
50cm tion of ethylene to non-submerged plants has resulted in promotion
of internodal growth (Kende et al., 1998; Metraux and Kende, 1983).
2.4 100cm
Both the great morphogenetic plasticity and the escape strategy
mber
may explain that Z. latifolia grows well in flood-prone habitats (Li,
nu 1.8 1995).
Besides plant elongation, vegetative reproduction is also a
nce
common growth strategy for herbaceous species in habitats
ce
1.2 where inundation occurs (Amoros and Bornette, 1999; Brock and
Casanova, 1997). Zizania latifolia reproduces asexually by produc-
Inflores
ing new tillers from underground rhizomes, but in the experiments
0.6
an elevated water level decreased tiller number of the plants. These
results conform with previous work which demonstrated that an
increased water level inhibits basal tiller emergence of deepwa-
0.0
ter rice varieties (Datta and Banerji, 1979), and that submergence
generally reduces or inhibits ramet production of wetland species
Con trol 40 70 100
(Wang et al., 2009). Under submergence, production of tillers may
Duration (d) be inhibited for the shortage of light, oxygen and nutrient sup-
ply, as energy reserves and structural carbohydrates apparently are
Fig. 4. The inflorescence number of Zizania latifolia in response to varying water
invested by priority into growth of the mature shoot (Manzur et al.,
depth and submergence duration (clustered boxplot by SPSS). Data points outside
2009).
this range are extremes (*). Dark bars inside this range are medians (—).
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Q. Wang et al. / Flora 209 (2014) 279–284 283
60 Control 50cm 100cm
50
40
Total biomass (g) 30
20 Control 40 70 100
Duration (d)
Fig. 5. Total biomass of Zizania latifolia in response to varying water depth and submergence duration; means ± S.E.
Flowering of Zizania latifolia showed substantial variation in Shifts in resource allocation is a ubiquitous response to inun-
response to water depth. The timing of flowering was advanced dation in riparian species (Mommer et al., 2006; Voesenek et al.,
and the inflorescence number was found to increase with increas- 2006). Negative effects on plant growth may become prevailing
ing water depth, which indicates that water depth treatments will when water level increases and inundation time are extended
favor sexual reproduction of Z. latifolia. Also in Scirpus maritimus (He et al., 1999; Mahelka, 2005). In Z. latifolia, no influence was
allocation of biomass to flowering and seed production increase found of water level and submergence duration on total biomass.
with increasing water depth, and a shift from vegetative reproduc- This shows that growth of flood-adapted Z. latifolia is actually not
tion in shallow water to sexual reproduction in deep water was negatively affected by submergence, which conforms with simi-
observed correspondingly (Lieffers and Shay, 1981). In perennial lar observations in other emergent wetland plants (Coops et al.,
species, prolonged inundation may promote the development of 1996). However, Z. latifolia exhibited a highly significant decrease
taller flowering shoots or lead to an increase in the proportion of in root:shoot ratio with increasing water level and prolonged sub-
flowering tillers and hence mass allocation to sexual reproduction mergence duration. This may indicate that submergence triggers a
(Merril and Collberg, 2003; Naidoo and Mundree, 1993). This may biomass allocation response preferably from roots to the shoots in
promote higher seed production and subsequent higher probability this species. The organ of Z. latifolia resisting submergence is the
of regenerating new individuals (Mony et al., 2010), suggesting that shoot which elongates, escaping inundation. It can be generalized
flooding is an important selection pressure on genetic variation, that plants occurring in frequently disturbed habitats allocate more
favoring plant sexual reproduction. biomass to organs that resist the disturbance (Barrat-Segretain,
1.2 a Control 50cm 100cm
b b b o
i 0.9
c c
0.6 d Root:shoot rat
0.3 Control 40 70 100
Duration (d)
Fig. 6. Root:shoot ratio (square-root transformed) of Zizania latifolia in response to varying water depth and submergence duration; means ± S.E.
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284 Q. Wang et al. / Flora 209 (2014) 279–284
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