Responses to flooding intensity in Leontodon taraxacoides

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New Phytol. (1999), 141, 119–128

Responses to flooding intensity in

Leontodon taraxacoides

A. A. GRIMOLDI*, P. INSAUSTI, G. G. ROITMAN A. SORIANO

Departamento de EcologıUa, Facultad de AgronomıUa, Universidad de Buenos Aires,

Avenida San MartıUn 4453, 1417 Buenos Aires, Argentina

Received 19 May 1998; accepted 11 September 1998

Natural flooding is one of the major factors affecting vegetation dynamics in many regions of the world. The

Flooding Pampa Grasslands (Argentina) are frequently exposed to flooding events of diverse intensity and

duration, some of which Leontodon taraxacoides, an exotic dicot. frequent in these grasslands, seems to

survive. Its responses to four different water depths (0, 1, 7 and 13 cm) were studied. The results indicate that

plants in conditions of total submergence (depth of 13 cm) did not survive. In less severe flood conditions,

increases in the leaf insertion angle resulted in the maintenance of a large proportion of the total leaf area above

the water. Differences in leaf length and a decrease in the width and the proportion of lobes per leaf were also found

under partial submergence conditions (depth of 7 cm). Root and leaf aerenchyma, present in unflooded

plants, showed a significant increase in flood conditions. In spite of the anatomical and morphological

responses, total biomass and leaf area were severely affected by water depth. Control plants allocated more biomass

to reproductive organs, while partly submerged plants allocated more to leaves and less to reproductive organs.

Mature L. taraxacoides plants presented a wide range of plastic adjustment as a survival strategy in soil

anaerobiosis, and appear to be able to survive short spring floods in a vegetative state; in contrast, they might not

tolerate total submergence conditions imposed by more intense and long-lasting floods.

Key words: flood, water depth, aerenchyma, leaf morphology, allocation, Leontodon taraxacoides, Flooding

Pampa Grasslands.

In certain types of grassland, natural flooding is a

major factor in the disturbance regime. In these

systems, plants have to cope with unpredictable

periods of flooding at different times of the year. The

interaction between plant responses and the charac-

teristics of the flooding event, such as duration,

seasonal timing, water depth and frequency,

influences floristic composition and plant community

dynamics (Menges & Waller, 1983; Voesenek et al.,

1992). Responses to increasing flooding intensity

vary widely among plant species and are generally

associated with anatomical and morphological

changes (Jackson & Drew, 1984; Blom & Voesenek,

1996). For example, it has been found that in the

genus Rumex, aerenchyma formation and leaf

elongation are important for the recovery of contact

with the aerial environment and allow oxygen

transport to the submerged tissues (Laan et al.,

*Author for correspondence (e-mail grimoldi!ifeva.edu.ar).

1990b; Van der Sman et al., 1991). In conditions of

high flooding, when the water surface is not reached

by plants, other responses such as underwater

photosynthesis (Laan & Blom, 1990a), and metabolic

adaptations or dormancy are critical for plant

survival (Armstrong et al., 1994). In some cases,

plant responses to flooding involve changes in

biomass allocation patterns, enabling tolerant plants

to remain vegetative during flooding periods (Van

der Sman, et al. 1993; Blom & Voesenek, 1996).

The Flooding Pampa Grassland (Argentina) is

currently exposed to cattle grazing and periodic

flooding events of diverse intensity and duration

(Chaneton et al., 1988; Soriano, 1991). Natural

floods cause most dicots in the lowland communities

to decrease their biomass formation or to die, while

native monocots generally increase their cover and

biomass (Chaneton et al., 1988; Insausti, 1996).

Recent studies in this grassland found that native

grasses present plastic responses to flooding, such as

aerenchyma tissue formation and increase in plant

height (Rubio et al., 1995; Loreti & Oesterheld,


120 A. A. Grimoldi et al.

1996). We have little information regarding the

effects of flooding on exotic dicot. species naturalized

in the region, but it is known that after floods some

exotic dicots such as Leontodon taraxacoides persist,

possibly representing 10% of the total biomass in

lowland communities (Insausti, 1996).

Plastic responses that could minimize environ-

mental constraints to ensure survival, as a solution to

temporally heterogeneous environments, have been

discussed previously (Bradshaw, 1965; Via et al.,

1995). These responses could be important for the

survival of such exotic dicots as L. taraxacoides in the

Flooding Pampa Grasslands. Our objective was to

identify the anatomical, morphological and allo-

metric responses of L. taraxacoides measured in

different depths of water, and to analyse the effects of

flooding intensity on the survival of the plant,

particularly relevant when one considers the natural

flooding of grasslands which are invaded by this

species.

Species characteristics and study site

Leontodon taraxacoides (Vill) Merat is a short-lived

European perennial herb from the Asteraceae family

(tribe: Cichorieae). In Europe it is a common plant in

poor and overgrazed grasslands (Rivas & Rivas,

1963) found in dry open sites and sand dunes as well

as in pond borders (Pignatti, 1982). In the Flooding

Pampa Grassland, it is present only in plant

communities in humid lowland (Burkart, et al.

1990); it is characterized by self-compatibility,

bractless scapes with solitary heads, lobate leaves

disposed in a rosette, and a short erect truncate

stock. The reproductive phase runs from the end of

spring until the beginning of autumn.

Plants used in this study were taken from a field

under continuous grazing in Pila, in the Province of

Buenos Aires, Argentina (36° 30« S, 58° 30« W).

Plants were collected from a stand of Piptochaetium

montevidense, Ambrosia tenuifolia, Eclipta bellidioides,

Mentha pulegium and Briza subaristata, one of the

most widespread communities of the Flooding

Pampa (Burkart et al., 1990); found in flat areas, it is

associated with typical Natraquoll soils, with fine

texture that causes imperfect drainage. Short-lived

(1 month) floods of 7 cm or less occur at the

beginning of almost every spring. In contrast, large

floods are unusual and cover grasslands with water

10–30 cm deep for 3–5 months (Chaneton et al., 1988;

Soriano, 1991). At the same site, field experiments

showed soil redox potential (Eh() (A1 horizon) values

of 223 mV in unflooded conditions and ®153 mV

in flooded (Taboada & Lavado, 1986). The reductive

status of the soil during flooding corresponds with

conditions that reduce growth of most flood-

intolerant species (Ponnamperuma, 1984).

Experimental design

By the end of winter, similarly sized individuals of L.

taraxacoides were extracted in rectangular soil blocks

0±08 m#¬0±2 m, in which the selected plant was

central. In the field, depth of the root system does

not exceed 0±2 m (data not shown). Blocks were

transported to the experimental garden and were put

in groups of three, separated by a plastic membrane,

in a plastic container 0±24 m#¬0±4 m, each of which

represented an experimental unit ; there were five

replications. By this method the difficulty of simu-

lating floods in the field or maintaining experimental

controls during a natural flood were avoided.

After 2 months of acclimatization, treatments

consisting of different flood levels were randomly

assigned and applied for 49 d: (1) control ; (2)

waterlogging; (3) partial submergence; and (4) total

submergence. Controls were well drained and were

watered daily up to field capacity. Waterlogging

consisted of a constant water depth above soil level of

1 cm. At the beginning of the experiment, the partial

submergence and total submergence treatments were

flooded to a depth of 7 cm, the plants remaining

totally submerged. Afterwards the water level was

maintained constant in the partial submergence

treatment and was gradually increased in the total

submergence treatment, according to the height of

the plants, up to 13–14 cm above soil level at the end

of the experiment. The containers were kept in the

open air and were rotated every 7 d. In the flooded

treatments, water was gradually replaced.

Anatomical analysis

Root and leaf porosity were determined using the

pycnometer method (Sojka, 1988), based on the

weight increase which occurs when root or leaf air

volume is replaced by water after maceration. This

analysis was performed using young leaves and

lateral roots. The lateral roots used were produced

from the tap root and were 8–10 cm long, extracted

from a soil depth of 0–5 cm. In addition, some roots

and leaves were fixed and preserved in formalin-

acetic-alcohol. Segments of lateral roots from at least

2 cm from the tip, and leaves from 1 cm from the

plant stock were dehydrated in a series of increasing

ethanol concentrations and embedded in paraffin

wax. Sections 15–20 µm thick were cut, stained with

safranin and fast green and mounted in Canada

balsam. The percentage of root aerenchyma per total

cross-sectional area was calculated with a Minimop

Digitizer Prov. attached to an ocular microscope

(Sojka, 1988). These variables were measured in five

randomly selected plants at the beginning of the

experiment and 15 d after the first measurement, and

at the end of the study in one plant of each

replication. Root aerenchyma and root and leaf

porosity were also measured in five plants grown for

18 months in drained conditions.


Flooding intensity and Leontodon taraxacoides 121

L

Lb

La

Lc

1 cm

7 cm

HAa

α

Figure 1. Description of morphological analysis. Leaf

lengths (L) present in three layers were calculated for all

treatments: (La) 0–1 cm, (Lb) 1–7 cm and (Lc) above 7 cm

depth. Leaf height (H), leaf insertion angle in relation to

soil surface (£), maximal (A) and minimal (a) leaf width at

the mid-point of the leaf.

Morphological analysis

Leaf length and insertion angle in relation to the soil

surface were periodically measured. Leaf height was

calculated by: H ¯ sin (£)¬L (Fig. 1). Analyses

were performed by calculating the averages of all

adult leaves and the three maximum values of each

plant. Since results were the same for both analyses,

only the results from adult leaves are presented.

After the plant harvest, length (L), area, mid-rib

diameter, maximal (A) and minimal (a) width at the

mid-point of the leaf were measured in all adult leaves

(Fig. 1). The outlines of 10 randomly selected leaves

were copied onto white paper, the extremes of each

lobe were joined with straight lines and the leaf

dissection index was calculated as the quotient of leaf

area and the area of the empty space surface between

the lobes. All areas were measured with a Li-3000

leaf area meter (Li-Cor, Inc. Lincoln, NE, USA).

The vertical arrangement of leaf area was quantified

by an arbitrary division into three height layers, in

accordance with the imposed experimental water

depths. For all treatments the leaf length per layer

was determined by: La (0–1 cm) ¯ 1 cm}sin (£),

Lb (1–7 cm) ¯ (7 cm}sin £)®La and Lc ("7 cm)

¯ L®Lb®La (Fig. 1). For each individual, the

relationship between leaf length and leaf area was

estimated by linear regression (P!0±0001; r#"0±8)

and the leaf area present in each layer was calculated.

The number of leaves extending beyond each layer

was also calculated at the last measurement.

Biomass and survival

At the end of the experiment, two plants of each

replication were harvested and separated into three

different parts: heads and scapes; leaves; and stock

and roots. After maintaining soil blocks in 0±4%

sodium pyrophosphate solution for 48 h, they were

washed carefully and stock-roots material separated

as completely as possible. The material was weighed

after oven-drying for 72 h at 70°C. The biomass

allocation was analysed as the ratio of each part to the

total plant biomass. The total leaf length:leaf

biomass ratio was also calculated.

Statistical analysis

Morphological variables were analysed by repeated

measures ANOVA (n ¯ 5), with water level as the

between-subject main effect and time as the within-

subject factor. Greenhouse-Geyser adjustment was

used when mild violations of the hypothesis of

sphericity of the covariance matrices occurred. The

analysis was performed in two different ways: all

treatments within four measurement days (5, 10, 19,

25) and excluding the submerged treatment; within

six measurement days (5, 10, 19, 25, 32, 46).

Individual contrasts were made by the Bonferroni

test at a probability level of 0±05 (Von Ende, 1993).

Variables measured once were analysed using one-

way (n ¯ 5) and a posteriori means-

comparison were performed with Tukey tests at a

probability level of 0±05. Leaf area, biomass, leaf

number and scape number data were transformed

(log x) to comply with the assumptions of the

ANOVA. Porosity (%), biomass allocation (%), leaf

area (%) and leaf number (%) per layer data were

(arcsin ox)-transformed. All results are presented as

mean³SE.

Anatomical analysis

Roots and leaves of plants growing for 18 month

under conditions of free drainage showed porosity

values, determined by pycnometry, of 10±5³2±1%

and 11±7³1±8% respectively. The porosity of the

plants growing under field conditions was 20±93³1±7% in roots and 15±87³1±5% in leaves. After 15 d

of flooding, no differences were found in leaf

porosity among treatments (P ¯ 0±2954), but

root porosity decreased in conditions of total sub-

mergence (P ¯ 0±0342) (Fig. 2). After 49 d,

considerable increases in leaf (P ¯ 0±0008) and root

porosity (P ¯ 0±0009) were recorded in plants in the

waterlogging and partial submergence treatments

compared with the controls (Fig. 2). In drained

conditions, porosity values were lower than those

measured at the beginning of the experiment (Fig.

2). Root porosity values, based on pycnometer

measurements, did not differ from those found by

visual cross-sectional area analysis. However, on day

15, the root aerenchyma of totally submerged plants,

calculated by visual analysis, was greater

(31±94³1±58%) than the value obtained by the

pycnometer method (Fig. 2).



(a)40

30

20

10

0

a

a a a

Leaf

po

rosi

ty (

%)

b

a a

(b)40

30

20

10

0

a

ab

b

Ro

ot

po

rosi

ty (

%)

b

aa

Day 15 Day 49

ab

Figure 2. (a) leaf and (b) root porosity of Leontodontaraxacoides plants grown at different water depths (w.d.) :

control (*), waterlogging (w.d. 1 cm) (8), partial

submergence (w.d. 7 cm) (7) and total submergence (w.d.

13 cm) (+). Values are means³SE of five replicates and

different letters indicate significant differences (P!0±05)

among treatments within the day of measurement based on

the Tukey test.

(a)(a)(a) (b)(b)(b) (c)(c)(c)

LLLLLL

LLL

Figure 3. Transverse sections of roots on Leontodon taraxacoides plants grown at different water depths (w.d.).

(a) Control. (b) Waterlogging (w.d. 1 cm). (c) Partial submergence (w.d. 7 cm). Lysigenous aerenchyma (L).

Bar, 150 µm.

Aerenchyma production involved different

degrees of cell dissolution until the formation of

larger lysigenous lacunae (Figs 3, 4). In the roots,

each lacuna was separated by a variable number of

intact cells, stretching radially from the inner to the

outer cortex. After 15 d, the radius of the control

plants contained several rows of intact cells (Fig. 3a),

the number of rows decreasing with increasing water

depth. A single row remained in waterlogging

conditions (Fig. 3b) and an incomplete row of cells,

or only the remains of cell walls persisted in partial

(Fig. 3c) and total submergence (not shown). Mean-

while, the number of cortical radial cells involved in

the lacunae increased similarly (Fig. 3). The trans-

verse sections also showed that only lateral roots of

control plants developed secondary tissues (Fig. 3a).

Leaves presented constitutive schizogenous

aerenchyma (Fig. 4a–c) and lysogenous aerenchyma

development was limited to the mid-rib leaf blade

(Fig. 4b,c). Transverse sections of tissue from the

leaf base revealed that lacunae were produced in

flooding conditions (Fig. 4b,c) but no lysigenus

aerenchyma was formed in the control plants

(Fig. 4a).

Morphological analysis

Repeated measures ANOVA indicated significant

treatment (P!0±0001) and time effects (P!0±0001)

for the variables analysed. The interaction

treatment-time was significant (P ¯ 0±01), showing

that water level effects differed through time. The

first response registered was the change in the leaf



(a)(a)(a) (b)(b)(b) (c)(c)(c)

LLL

LLL

Figure 4. Transverse sections of leaves of Leontodon taraxacoides plants grown at different water depths (w.d.).

(a) Control. (b) Waterlogging (w.d. 1 cm). (c) Partial submergence (w.d. 7 cm). Arrows point to schizogenous

aerenchyma; lysigenous aerenchyma (L). Bar, 150 µm.

angle and height from a prostrate to a more erect

position in flood conditions. The differences were

observed within 24 h of the beginning of the flood

treatments and corresponded with the water height

imposed in each one of them (Fig. 5). Leaf angle and

height in partially and totally submerged conditions

showed a marked initial change, but little subsequent

change (Fig. 5a,c). The morphology of plants under

total submergence changed steadily until death (Fig.

5). The angle measurements differed significantly

after 10 d (Fig. 5a), as did the height measurements

after 30 d (Fig. 5c), among all treatments. After 10 d,

length of mature leaves were significantly shorter in

plants in waterlogged conditions than in those in the

rest of the treatments (Fig. 5b). After 19 d the leaves

of the controls were longer than those under partial

and total submergence (Fig. 5b).

At the end of the experiment, a great proportion of

the leaves were above the height of 7 cm under

partial submergence conditions (P!0±0001); under

waterlogged conditions, most leaves were positioned

within the 1–7-cm layer (P!0±0001), and in control

conditions the proportion present in the lower layer

was significantly greater than in the rest of the

treatments (P ¯ 0±0094) (Table 1). At harvest, plants

under partial submergence had a graminoid-like

morphology (Fig. 6). Narrowness of blades and

absence of lobes were indicated by the differences

between the maximal (P!0±0001) and minimal (P ¯0±0073) width and in the leaf dissection index

(P!0±0001) (Table 1). Leaves of the waterlogged

plants were narrower but had the same lobe

proportion as the control plants (Fig. 6; Table 1).

Under partial submergence, the diameter of the leaf

mid-rib was larger than in the rest of the treatments

(P ¯ 0±0052), and the area of the mature leaf was

greater in the control plants than in the rest of the

treatments (P ¯ 0±0004) (Table 1).

Biomass and survival

At the beginning of the experiment, the total number

of leaves per plant was 14±2³0±4. Plants continued

producing leaves, except under total submergence,

which caused the death of 50% of individuals after

25 d and of 100% after 40 d of treatment. At the final

measurement the control plants had more leaves and

flower scapes than the plants in the rest of the

treatments. The numbers of leaves and scapes were

greater in the waterlogged plants than in those under

partial submergence (P!0±0001) (Table 2).

The total leaf area per plant was higher in control

plants (P!0±0001), and differences were not found

between the two flood treatments (Table 2). At the

same time, leaf area of the top layer ("7 cm) was

greater under partial submergence than in water-

logged conditions (P ¯ 0±0002). Shallow water

depth corresponded to higher values of plant biomass

(P!0±0001) and higher allocation to reproductive

organs (P ¯ 0±0002) (Table 2). Accordingly, partly

submerged plants allocated more biomass to leaves



(a)90

80

70

60

0

(b)14

12

10

8

12

Mea

n le

af h

eig

ht

(cm

)

Days

50

40

30

20

10

6

9

6

3

00 10 20 4030 50

Mea

n le

af le

ng

th (

cm)

Mea

n le

af a

ng

le (

°)

(c)

Figure 5. Adult leaves of Leontodon taraxacoides plants grown under different water depths (w.d.) : control (+),

waterlogging (w.d. 1 cm) (E), partial submergence (w.d. 7 cm) (*), total submergence (w.d. 13 cm) (D).

(a) Mean leaf insertion angle (°) in relation to soil surface (b) Length (cm). (c) height (cm). Values are

means³SE of five replications.

(P ¯ 0±0297) and stock-root organs (P ¯ 0±0103)

than plants in the rest of the treatments. The total

leaf length:leaves biomass ratio was smaller in the

control plants than in those in conditions of partial

submergence (P ¯ 0±0094) (Table 2).

The proportion of leaf area and biomass positioned

in higher layers increased with higher water levels.

The total leaf area above 7 cm was 2±7³1% in

control, 1±8³0±5% in waterlogged, and, significantly

different from these, 19±0³3% in partly submerged

plants. Waterlogged and partly submerged plants

had greater total leaf area in the 1–7 cm layer

(66³3%) than the controls (47±6³3±9%, P!0±0001).

All treatments differed significantly in the pro-

portion of the leaf area in the 0–1 cm layer

(P!0±0001), control plants had the highest,

49±7³4±5%, and partially submerged plants the

lowest, 14±1³0±7%, (P!0±0001). Under partial

submergence, leaf area in the upper layer

corresponded to 11% of the aboveground biomass,

whereas in the rest of the treatments the proportion

represented 1% (P!0±0001).

The results show a strong negative relationship

between water depth and growth and survival of L.

taraxacoides. In waterlogged and conditions of

partial submergence, plant growth and biomass were

severely affected and, under totally submerged



Table 1. Leaf morphological traits of Leontodon taraxacoides plants

grown at different water depths (w.d.): control, waterlogging (w.d. 1 cm)

and partial submergence (w.d. 7 cm)

Variable Control Waterlogging

Partial

submergence

Maximal leaf width (cm) 1±67³0±10 a 0±91³0±03 b 0±64³0±09 c

Minimal leaf width (cm) 0±54³0±04 a 0±35³0±01 b 0±41³0±05 ab

Leaf dissection index 1±41³0±16 b 1±95³0±26 b 6±49³0±53 a

Leaf area (cm#) 7±90³0±94 a 3±60³0±13 b 3±90³0±65 b

Mid-rib diameter (cm) 0±13³0±01 b 0±12³0±01 b 0±15³0±01 a

Leaves per layer (%)

0–1 cm 32±8³4±6 a 13±8³2±9 b 14±9³4±5 b

1–7 cm 54±8³2±4 b 73±4³4±2 a 24±8³5±5 c

"7 cm 12±4³3±5 b 12±8³4±8 b 60±2³3±3 a

Values are means³SE of five plants harvested at the end of the experiment.

Different letters indicate significant differences (P!0±05) between treatments

based on Tukey test.

(a) (b)

(c)

Figure 6. Shape of leaves of Leontodon taraxacoidesplants grown for 49 d at different water depths (w.d.).

(a) Control. (b) waterlogging (w.d. 1 cm). (c) partial

submergence (w.d. 7 cm). Bar, 1 cm.

conditions, plants could not survive. The anatomical,

morphological and allometric traits of plants growing

in flooded conditions show a wide range of plastic

adjustment, associated with survival under anaerobic

conditions (Blom & Voesenek, 1996).

Anatomical and morphological plastic responses

to flooding in herbaceous plants have been widely

studied (Jackson & Drew, 1984; Armstrong et al.,

1994). Hormones play a central role in the expression

of these traits (Voesenek et al., 1992). Some studies

have found that, in conditions of flooding, the

internal ethylene concentration influences lysigenous

aerenchyma tissue production (Drew et al., 1979),

epinastic curvature of the leaves (Jackson & Drew,

1984) and shoot elongation (Van der Sman et al.,

1991). Accordingly, the vital contribution of

increased leaf height to better aerated and

illuminated zones above or close to the water surface,

and the presence of aerenchyma tissue, which

reduces the resistance to oxygen transport and the

oxygen demand of the plant tissues, has been

demonstrated by various authors (Armstrong, 1979;

Laan & Blom 1990a; Laan et al., 1990b).

In L. taraxacoides, increase of root porosity in

conditions of flooding and root aerenchyma type are

similar to those found in wetland species (Smirnoff

& Crawford, 1983; Justin & Armstrong, 1987). In

some cases, shoot aerenchyma increased significantly

and was apparently accompanied by an increase in

the diameter of the organs involved, such as the

increment of the mid-rib diameter in L. taraxacoides

in conditions of partial submergence (Moon et al.,

1993; Coops et al., 1996). The contrast between the

low root-porosity values found by the pycnometer

method under submergence conditions with those

found by the visual cross-sectional technique sug-

gests a possible collapse of the root radius cells.

Some of the lacunae might be filled with water, which

would affect the pycnometer analysis and root

survival (Sojka, 1988). L. taraxacoides has con-

stitutive schizogenous leaf aerenchyma and develops

lysogenous leaf aerenchyma in response to flooding.

The results showed that lateral roots present

lysogenous aerenchyma that showed a significant

increase in flood conditions; and that root porosity

might gradually decrease in drained-soil conditions.

In this case, the presence of secondary tissues

and less porous organs would probably confer more

resistance to soil mechanical constraints (Engelaar

& Blom, 1995), especially in the dry summer season

when trampling by cattle produces greater increases

in soil bulk density (Taboada & Lavado, 1993). This

fluctuation pattern contrasts with the data available

for Paspalum dilatatum (Rubio et al., 1995; Loreti

& Oesterheld, 1996), a native grass with high flood

tolerance that contains large proportions of aeren-

chyma throughout the year. In this species, the

presence of a sclerenchymatous sheath in the outer

layers of the cortex (Rubio et al., 1995) might provide



Table 2. Leaf area and biomass traits of Leontodon taraxacoides plants

grown at different water depths (w.d.): control, waterlogging (w.d. 1 cm)

and partial submergence (w.d. 7 cm)

Variable Control Waterlogging

Partial

submergence

Scape number 77³5 a 7³1 b 3³1 c

Leaf number 137³12 a 24³2 b 17³2 c

Plant leaf area (cm#)

0–1 cm 479³62 a 23³4 b 7³1 c

1–7 cm 485³94 a 47³4 b 35³2 b

"7 cm 26³11 a 2³1 b 11³2 a

Total 990³150 a 72³7 b 53³3 b

Plant biomass (g)

Heads and scapes 5±57³0±89 a 0±44³0±09 b 0±08³0±04 c

Leaves 4±89³0±75 a 0±51³0±07 b 0±29³0±04 c

Stock and roots 1±95³0±18 a 0±34³0±05 b 0±19³0±07 c

Total 12±41³1±44 a 1±29³0±16 b 0±56³0±09 c

Leaf length}leaf biomass

(cm}g)

246±1³21±2 b 321±4³37±2 ab 474±7³95±0 a

Values are means³SE of five plants harvested at the end of the experiment.

Different letters indicate significant differences (P!0±05) between treatments

based on Tukey test.

a stronger root structure which protects the lacunae

from collapse, which occurs in many flood-tolerant

monocotyledons (Smirnoff & Crawford, 1983).

Several traits of leaf morphology responded to

water depth and, as a result, a high proportion of the

leaf area was positioned relative to the water height

in each treatment. The short reaction time indicates

that plastic changes in epinasty and leaf length

occurred in response to flooding (Van der Sman et

al., 1991). The leaf insertion angle appears to be the

principal factor enabling leaves to emerge above the

water surface. In addition, between flooded treat-

ments leaf elongation was promoted only in those

plants in conditions of partial or total submergence.

Like those for Rumex maritimus, our experimental

data showed complete survival only of the plants

whose leaf tips emerged above the water surface,

showing the vital importance of recovering air–shoot

contact to flood-survival ability (Laan & Blom,

1990a; Van der Sman et al., 1991). Furthermore, in

L. taraxacoides, these responses were followed by a

complete change of leaf shape, involving leaf width

reduction and total absence of lobes under conditions

of partial submergence. Leaf shape responses have

also been documented, especially in aquatic species

in relation to water depth (Bostrack & Millington,

1962; Wooten, 1986). These results show that the

intensity of the stimulus determines the degree and

the number of the morphological responses to

flooding, increasing with environmental stress.

In spite of the reported mechanisms of flood

resistance, reduction in leaf growth rate and plant

biomass indicates a stress condition in flooding

treatments (Chapin, 1980). In L. taraxacoides,

anaerobic and reductive soil conditions seem to

produce metabolic constraints that severely affect

root and shoot growth (Jackson & Drew, 1984). Leaf

growth rate is extremely sensitive to a variety of

stresses (Chapin, 1980), including flooding (Jackson

& Drew, 1984). Leaves of waterlogged plants were

shorter, but changes in leaf angle were sufficient to

raise them above the water level. By contrast, partly

and totally submerged plants elongated their leaves

in a magnitude similar to controls but with less

biomass, as demonstrated by higher leaf length:leaf

biomass ratio. This response indicated that leaf

elongation is the priority for recovery of contact with

the air and survival in conditions of partial sub-

mergence.

Biomass allocation was markedly affected by the

different experimental treatments. Control plants

allocated a great proportion of biomass to repro-

ductive structures; in contrast, flooded plants

increased leaf or stock-root biomass. The greater leaf

biomass proportion in conditions of partial sub-

mergence could be part of a homeostatic strategy to

maximize the acquisition of oxygen, the most

limiting resource under these conditions (Bloom

et al., 1985). It is known that perennial plants com-

monly respond to stress by reducing allocation

to reproductive structures, and do the reverse in

conditions of high resource availability (Chapin,

1980; Bloom et al., 1985). In the Netherlands River

Forelands, it has been found that some perennial

species delay or postpone flowering to the next year

in flooding conditions (Van der Sman et al., 1993).

This strategy was described as stress-tolerant-

ruderal (S-R) (sensu Grime, 1979; Van der Sman

et al., 1993) and corresponds with the established

secondary strategy proposed for L. taraxacoides in



the functional approach to common British species

(Grime et al., 1988). At a greater scale of analysis, it

was proposed that stress-tolerant species have

morphologically fixed traits under stress conditions

(Grime, 1979), but in the case of L. taraxacoides,

phenotypic plasticity might play a central role in

reducing adverse environmental effects (Bradshaw,

1965; Via et al., 1995), especially in conditions of

partial flooding (Laan & Blom, 1990a; Laan et al.,

1990b).

It has been shown that plastic responses could

influence the process of species invasion (Meerts,

1992; Williams et al. 1995). L. taraxacoides occurs in

dry and humid open sites of European grasslands

(Rivas & Rivas, 1963; Pignatti, 1982, Grime et al.,

1988), but in the Flooding Pampa Grassland it is

present only in humid-lowland plant communities

(Burkart et al., 1990). The constitutive and plastic

features related to flood-survival could indicate an

adjustment of this species to the characteristics of

those invaded communities (Noble, 1989). Grazing

facilitates invasion and subsequent dominance of

alien dicots, such as L. taraxacoides in the Flooding

Pampa Grasslands (Oesterheld & Sala, 1990).

However, after flooding, native monocots generally

increase their presence and exotic dicots suffer

significant decreases in biomass and abundance

(Chaneton et al., 1988; Insausti, 1996). Adult

L. taraxacoides plants, nevertheless, can survive

slight spring floods, through a certain ability to

survive under root anaerobiosis. In contrast, L.

taraxacoides does not endure intense and long-lasting

floods when totally submerged. The flooding stress

effects that were detected in this study corroborate

the results found in experiments at the community

scale (Chaneton et al., 1988; Insausti, 1996) and

show that flooding intensity strongly influences the

demography of this species.

We especially thank Dorita Grimoldi for her technical

assistance in all phases of this work. We thank Professor

Mo! nica Tourn, who helped with the anatomical analysis,

and P. Quinos, J. Loreti, M. Omacini, M. Nogue! s Loza

and two anonymous reviewers, who helped to improve the

manuscript. We also thank the Bordeau family, owners of

Estancia Las Chilcas, who facilitated our work on their

land. Agustı!n Grimoldi was supported by a fellowship

from CONICET.

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Responses to flooding intensity in Leontodon taraxacoides

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