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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

Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, Hubei 430074, China

Institute of Soil and Fertilizer, Fujian Academy of Agricultural Sciences, Fuzhou, Fujian 350013, China

Hubei Key Laboratory of Wetland Evolution & Ecological Restoration, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, Hubei 430074, China

University of Chinese Academy of Sciences, Beijing 100039, China

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.

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

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

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

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

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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