PHYSIOL. PLANTARUM 69: 35-48.
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Responses of red alder and black cottonwood seedlings to flooding
Constance A. Harrington
Harrington, C. A. 1987. Responses of red alder and black cottonwood seedlings to
flooding. - Physiol. Plantarum 69: 35-48.
Red alder (Alnus rubra Bong.) and black cottonwood (Populus trichocarpa Torr. &
Gray) seedlings were monitored to evaluate response during a 20-day period of artifi­
cial flooding and a 20-day recovery period following flooding. During the flooding
period, both species showed changes in nutrient uptake and transport, initiated stem­
derived adventitious roots that became aerenchymatous, and exhibited hypertro­
phied lenticels. Flooded red alder seedlings also showed reduced height and leaf area
growth and developed lower-stem hypertrophy. Flooded black cottonwood seedlings
exhibited root dieback, aerenchyma in below ground root tips, and changes in root
hydraulic conductance and xylem pressure potential. Contrary to expectations, how­
ever, stomatal closure following flooding was not observed in either species.
Flooded red alder seedlings increased growth rapidly when drained, and by the end of
the recovery period, formerly flooded and non-flooded red alder seedlings differed
only minimally in this respect. In contrast, several characteristics of black cottonwood
- including growth rate and nutrient content - still differed between formerly flooded
and non-flooded seedlings at the end of the recovery period. Based on observed
treatment differences at the end of the experiment, red alder seedlings were judged
to be more tolerant of flooding than black cottonwood.
Additional key words- Alnus rubra, biomass allocation, biomass increment, leaf con­
ductance, mineral nutrition, Populus trichocarpa, root hydraulic conductance, soil
waterlogging.
C. A. Harrington, U. S. Forest Service, Southern Forest Exp. Stn., Box 3516, Monti­
cello, AR 71655, USA.
Introduction
Plant responses to flooding or soil waterlogging have
been studied for many years. The ability of oxygen-re­
quiring organisms to survive and grow under anaerobic
soil conditions has been attributed to many factors,
these include physiological responses, morphological
adaptations and anatomical changes. Recent reviews
(Bradford and Yang 1981, Hook and Scholtens 1978,
Jackson and Drew 1984, Kozlowski and Pallardy 1984)
provide good synthesis of past research in this field.
Red alder (Alnus rubra Bong.) and black cottonwood
(Populus trichocarpa Torr. & Gray) are hardwood spe­
cies commonly found along rivers and streams in Ore­
gon and Washington in the U. S., and British Columbia
in Canada. Both species are tolerant of short-term
flooding but are not hydrophytes. They differ in their
ecological distribution (Powells 1965, Minore 1979),
with red alder growing in marshy areas or bogs as well
as adjacent to both slow and fast moving rivers and
streams and black cottonwood usually confined to the
flood plains of major rivers and streams. Although eco­
logical observations indicate that red alder may have
greater tolerance for poorly drained soil than black cot­
tonwood, no controlled experiments have been report­
ed that compare the responses of the two species to
flooding or soil waterlogging. The present study moni­
tored red alder and black cottonwood seedlings during
and following a 20-day period of artificial flooding.
Seedling growth, nutrition, water relations and morpho­
logy were assessed periodically during the experiment.
- AT , after treatment; BT , before treatment;
LA, leaf area; LW, leaf weight; PAR, photosynthetically active
radiation ; RW, root weight; T W , total weight; T , treatment.
Abbreviations
Received 21 January, 1986; revised 11 August, 1986
3'
Physiol. Plantarum 69, 1987
35
Materials and methods
Red alder and black cottonwood seedlings were grown
from May to September in a shadecloth-covered green­
house at Olympia, WA. The soil was subsampled for
mechanical analysis and chemical characteristics prior
to potting of the seedlings. Texture, determined by the
hydrometer method (Bouyoucos 1962), was loamy sand
(86% sand, 13% silt, 1% clay). Soil pH was 5.9 (in 1: 1
soil-water suspension; U.S. Dept Agriculture 1972).
Soil chemical characteristics as determined by the Co­
operative Chemical Analytical Laboratory, Corvallis
OR, were: 0.9 g kg-1 total N by Kjeldahl (Jackson
1958); 40 mg kg-1 extractable P by Bray No. 1 (Jackson
1958); 14 g kg-1 organic carbon (Walkely-Black in Al­
lison 1965); ammonium acetate cation exchange capac­
ity of 0.62 mol(p+) kg-1 (Jackson 1958); and exchange­
able cation values (ammonium acetate extraction,
atomic absorption spectrophotometry, North Central
Regional Soil Testing Commitee 1980) of 88 mmol(+)
kg-1 K, 57 1 mmol( +) kg-1 Ca, 49 mmol(+) kg-1 Mg, 1
mmol( +) kg-1 Fe and 6 mmol (+) kg-1 Mn.
About 1 month before the experiment began, 160
seedlings of each species were transplanted into 5.6 1
plastic pots (one seedling per pot). Pots were filled with
sufficient gravel (3 em) to cover the drainage holes be­
fore soil was added. After transplanting, the seedlings
were watered as necessary and fertilized weekly with a
dilute nutrient solution (Peters 20-20-20). All seedlings
appeared healthy at the beginning of the experiment.
Two days before the esperiment began, mean seedling
heights were 1 1.3 em for red alder and 6.9 em for black
cottonwood. This height difference was planned to
create the early growing season difference in height be­
tween the two species that is caused by differences in
seed germination time (Powells 1965, U. S. Dept of Ag­
riculture 1974).
On 31 July, 1982, half the pots were flooded by being
placed in individual plastic bags that were attached to
wooden support bars and slowly filled with deionized
water prewarmed to 15°C (mean soil temperature) until
the soil surface was saturated. The water table was kept
at the soil surface during the flooding period by the ad­
dition of deionized, prewarmed water as necessary. Af­
ter 20 days of flooding, holes were punched in the bags
to allow the water to drain off slowly. The bags were re­
moved the following day.
Air and soil temperatures were recorded regularly.
The reduction potential (EH) of the soil was measured
weekly using the ± 700 m V option on a Beckman Zero­
matic pH meter and 28 platinum electrodes ( 1 mm di­
ameter) permanently placed 7-10 em below the soil sur­
face in randomly selected pots. Electrodes were cali­
brated prior to use (Jackson 1956).
Total height and leaf area of all seedlings were meas­
ured weekly beginning 8 days prior to flooding. The
number of leaves per seedling in each of five size classes
was counted weekly, and average leaf areas for each
36
species, leaf size class and treatment period were deter­
mined by running a subsample of leaves from each
group through an area meter (Li-Cor 3 100). Then the
number of leaves in each size class was multiplied by the
appropriate area factor and the results added to deter­
mine total leaf area for each seedling. Changes in indi­
vidual seedling heights and leaf areas were calculated
for each weekly period and for the flooding and re­
covery periods.
Two replications of 10 seedlings were randomly se­
lected from each species and treatment group 10 and 20
days after flooding began and 20 days after its conclu­
sion. The seedlings were cleaned, physically separated
into various categories, dried at 65°C for 48 h and then
weighed. On the first measurement date, seedlings were
divided into roots, stems and leaves. At the time of the
second measurement, leaves were subdivided into be­
fore-treatment and treatment categories. On the last
measurement date, an after-treatment leaf category was
added to include those leaves that developed during re­
covery.
The same seedlings used for growth measurements
were also used for chemical analysis. Tissue separations
were as described above except that at the first harvest,
roots and stems were combined for chemical analysis.
For all analyses, there were two replications of each
component by species and treatment; each was a com­
posite of 10 seedlings. After 10 days of flooding and at
the end of both flooding and recovery periods, plant tis­
sues were analyzed for nitrate-N, water extraction
(Thomas and Chamberlain 1974) and total P (perchloric
acid digestion; Jackson 1958) by OSU-PNW Cooper­
ative Chemical Analysis Lab., Corvallis, OR. Plant tis­
sues collected at the end of the flooding period were
also analyzed for total K, Ca, Mg, Fe and Mn (per­
chloric acid digestion, atomic absorption spectropho­
tometry; Perkin-Elmer Corporation 1976).
Six randomly chosen seedlings from each treatment
were monitored for their diurnal patterns of leaf con­
ductance 1, 2, 5, 10 and 20 days after flooding began
and 1, 2, 5, 10 and 24 days after it ended. Both species
are hypostomatous (Pezeshki and Hinckley 1982); thus,
conductance was measured only on the underside of
fully developed, healthy, upper-stem leaves. Measure­
ments were made every 2 h each day from 04 00 to 22 00
h using a steady-state porometer (Li-Cor 1600) with a 2
cm2 sampling aperture. The porometer also measured
relative humidity, leaf and air temperature, and pho­
tosynthetically active radiation (PAR). On the final
measurement date, a null balance porometer (Interface
Instrument Company) was used because the Li-Cor was
not functioning properly. The two instruments were la­
ter calibrated against each other.
Five plants of each species and treatment were meas­
ured for root hydraulic conductance and xylem pressure
potential on five dates during the flooding period. Sam­
ple plants were removed from both flooded and non­
flooded pots by placing each pot in a bucket of water
Physiol. Plantarum 69, 1987
and gently agitating the resulting soil-water suspension.
Root systems were washed free of soil and the plants
were placed in beakers of water to keep the root sys­
tems wet. Plants were processed one at a time as needed
to minimize the time between removal of the plant from
the pot and measurement. This proceedure resulted in
minimal root damage but , unavoidably , would have
changed the root environment just prior to measuring
xylem pressure potential and root hydraulic conduct­
ance.
The terminal 10-15 em of each seedling (containing
the upper leaves) was placed in a large-capacity pres­
sure chamber (Plant Moisture Stress, Inc.) with the cut
end protruding. Xylem pressure potential of the stem
was then measured using standard methodology
(Ritchie and Hinckley 1975). After the terminal portion
of the stem was removed , the seedling root system was
placed in a water-filled container inside the pressure
chamber so that just the stem was above water and pro­
truding out of the chamber. A pressure gradient of 0.4
MPa was applied for 12 min. The amount of liquid
forced through the root system was determined using
preweighed wicks placed over the end of the plant stem.
Root length was determined by tracing with an electri­
fied grid system. Root hydraulic resistance (Ramos and
Kaufmann 1979) and then root conductance (Kramer
1969) were calculated using root length and flow rate.
Paired measurements of xylem pressure potential and
root conductance were taken beginning at predawn and
continuing through the day until all designated trees had
been sampled. A flooded and non-flooded tree of each
species were measured within ca 15 min of each other.
Seedlings were regularly examined for morphological
changes especially the occurrence and development of
adventitious roots , lenticels and stem hypertrophy.
Notes and sketches were made on the appearance of all
seedlings destructively sampled during the experiment.
At the end of both the treatment and recovery periods ,
10 lateral root tips were cut from 10 seedlings of each
species and treatment and placed in formalin acetic acid
alcohol or Craf III fixative (Berlyn and Miksche 1976).
Adventitious roots from each species were also sampled
and placed in fixative. The samples were dehydrated via
an isopropyl and t-butyl alcohol series (Berlyn and
Miksche 1976), embedded in paraffin , serially sectioned
on a rotary microtome (American Optical) at 12 [.till,
mounted on glass slides and stained with saffranin and
fast green.
Statistical differences between treatments were tested
using a standard , two-sample t-test; analyses were done
separately for each species. When data had been col­
lected by plant component, each component was ana­
lyzed separately. Paired t-tests were used to analyze the
xylem pressure potential and root conductance meas­
urements.
Physiol. Plantarum 69, 1987
Results
Survival and growth
Seedling survival was 100% but growth responses varied
by treatment and species. After 10 days of flooding ,
stem and root weight and mean total seedling weight
were greater for red alder in the flooded treatment than
in the non-flooded one. Twenty days after flooding be­
gan, its effects on total dry matter accumulation of
either species were minor , with only the stem weight of
red alder significantly greater in the flooded treatment
(Fig. 1). This increase in stem weight was probably due
primarily to the observed occurrence of lower-stem hy­
pertrophy. For both species , weight of leaves in the be­
fore-treatment category appeared to be greater for
flooded than non-flooded seedlings although the differ­
ences were not significant. Non-flooded seedlings , es­
pecially black cottonwood , abscised some lower leaves
during the flooding period , but flooded seedlings did
not experience any leaf abcission. Flooding may also
have resulted in increased expansion of some younger
0.8
0.7
0.6
0.5
0.4
0.3
B
OD
K co
AT LEAVES
IBJT LEAVES
§llj B T LEAVES
[ml STEMS
IBJ ROOTS
-**-
0 .2
0.1
0
\!)
(!j'
NF
.2
F
"
t..j
""
[!}
Q_
h.
1.4
RED ALDER
1.2
1.0
0.8
>..
ll::
c::,
NF
F
0.4
0.6
Fig. 1. Mean DW by species, treatment and plant component.
Treatment differences between components or for the total
seedling indicated by the symbol connecting or above the bars.
*, P :S 0.10; **, P < 0.05; 20F, 20 days of flooding; 20R, 20
days of recovery following 20F; NF, non-flooded; F, flooded;
AT , after treatment; T , treatment; BT , before treatment. Note
difference in Y-axis scale between species.
37
50 r----.
45
40
::;;
::;;
­
I);
"'
::;;
0
•
NON- FLOODED
FLOODED
35
30
25
20
15
0 ��----�----�
30 r----.
25
"'
BLACK COTTONWOOD
RED ALDER
0
NON-FLOODED
20
15
10
-1
TRE
3
NT +--T
NT
WEEK
+---R--
y
Fig. 2. Mean weekly height growth per seedling by species,
treatment and date. Shown are means ± SE, n 40.
=
leaves in this category. At the end of the flooding
period , flooded black cottonwood seedlings had lower
root weights than non-flooded seedlings but the differ­
ence was not significant. At the end of the recovery
period , however , formerly flooded cottonwood seed­
lings had significantly less total biomass , root biomass
and biomass in leaves formed during the recovery
period (AT leaves) than non-flooded seedlings (Fig. 1).
Red alder seedlings exhibited no differences between
treatments in total biomass. However , formerly flooded
red alder seedlings had significantly less biomass in AT
leaves and more in BT leaves than non-flooded seed­
lings. There was considerable increase in weight of ear­
lier formed (BT) red alder leaves during the recovery
period.
During the flooding period , black cottonwood seed­
lings exhibited no treatment differences in weekly
height increments , but flooded red alder seedlings
showed significantly reduced height growth during the
second and third weeks of flooding (Fig. 2). During the
recovery period , weekly height growth of formerly
flooded black cottonwood seedlings was significantly
less than that of non-flooded seedlings during all 3
weeks of measurement. Growth of formerly flooded red
alder seedlings was initially less than that attained by
non-flooded seedlings; however , the growth difference
between treatments decreased over time. This narrow­
ing of red alder treatment differences during the re­
covery period can be attributed to increased growth of
formerly flooded seedlings and to photoperiod-induced
38
decreased growth of non-flooded seedlings. The total
reduction in height due to flooding during the 6-week
experimental period was 18% for alder and 17% for cot­
tonwood.
Seedling response to flooding in weekly leaf area
(LA) growth was similar to that in height growth (Fig.
3). There were no significant differences between treat­
ments in weekly LA increase of black cottonwood seed­
lings during the flooding period. However , LA incre­
ment was significantly lower for the formerly flooded
cottonwood seedlings during all 3 weeks of the recovery
period. Flooded red alder seedlings showed significantly
lower LA increments than non-flooded seedlings during
the second and third weeks of flooding and the first and
second weeks of recovery. During the last week of the
recovery period , there was no significant difference in
LA growth between red alder treatments.
The ratio of LA to total plant weight (TW) decreased
during the growing season for red alder and was consist­
ently lower for flooded seedlings (Tab. 1). Thus , seed­
lings used less LA to support each unit of biomass as the
growing season progressed , and flooded red alder seed­
lings were presumably more efficient than non-flooded
seedlings in accumulating biomass per unit of LA. In
contrast , LAffW for black cottonwood did not change
much over the experimental period and was unaffected
by flooding. Specific leaf area (LA/LW) decreased over
the experimental period for red alder; that is , leaves be­
came heavier per unit area. This morphological leaf
change in red alder was increased by flooding. Black
cottonwood seedlings , however , exhibited very little
change in specific leaf area either over time or as a func­
tion of treatment.
The LA/RW ratio decreased for red alder during the
600 ,-------�
BLACK COTTONWOOD
o
•
<\j
500
NON-FLOODED
FLOODED
RED ALDER
0
e
-I
NON-FLOODED
FLOQ[)EO
3
WEEK
Fig. 3. Mean weekly change in leaf area per seedling by spe­
cies, treatment and date. Shown are means ± SE, n 40.
=
Physiol. Plantarum 69, 1987
Tab. 1. Ratios of leaf area to tissue weights by species, time and treatment. 10F, 10 days of flooding; TW, total seedling weight;
LA, leaf area; LW, leaf weight; RW, root weight; see Fig. 1 for other abbreviations.
Time
Black cottonwood
lOF
20F
20R
Red alder
lOF
20F
20R
Treatment
LA
TW
em' g-1
LA
LW
em' g-1
LA
RW
em' g-1
Non-flooded
Flooded
Non-flooded
Flooded
Non-flooded
Flooded
2243
2195
2380
1550
1368
1447
3692
3788
3774
2534
2460
2648
12632
11364
15384
12500
9380
9570
Non-flooded
Flooded
Non-flooded
Flooded
Non-flooded
Flooded
2647
1847
1921
1298
1320
881
4412
3522
3356
2353
3144
2438
14750
12430
9620
7570
3900
2540
experiment and was consistently lower for flooded red
alder seedlings than for non-flooded seedlings (Tab. 1).
In contrast, LA/RW did not change as much over time
for black cottonwood, and changes in the ratio differed
between treatments. During the recovery period,
LA/RW increased by 80 cm2 g-1 for non-flooded black
cottonwood seedlings and decreased by 2150 cm2 g-1 for
formerly flooded seedlings. T hus, formerly flooded cot­
tonwood seedlings diverted a greater proportion of their
plant resources to their root systems than was the case
for non-flooded seedlings.
Reduction potential and plant nutrient relations
Reduction potential (EH) in non-flooded pots was usu­
ally between 500 and 600 m V with little variation among
pots. Variation in EH values among flooded pots was
much greater than among non-flooded pots; sos were
at least three times higher in the flooded treatments. EH
in flooded pots decreased steadily, falling to 300 m V in
a week and to below 200 mV at 3 weeks. Surprisingly,
EH continued to decrease linearly for 2 weeks after
drainage, reaching a low value of 50 mV. After 20 days
of drainage, EH in flooded pots had increased again to
275 mV. Even though the soil in the pots was coarse­
textured, formerly flooded pots were slow to dry out
due to the low ratio of plant size to soil volume and the
fairly cloudy and cool weather conditions. Based on the
observed EH values in the flooded pots, soil oxygen
would have been depleted and nitrate, manganic man­
ganese and ferric iron ions reduced (Gambrell and Pa­
trick 1978, Mcintyre 1970). Depending on the variabil­
ity within and between pots, sulfate, carbon dioxide and
organic acids may also have been reduced.
Tab. 2. Concentration ( tmol kg-1 ) of nitrate nitrogen by species, treatment, time and plant component. Significant differences be­
tween treatments are indicated by a symbol after the value for the non-flooded treatment. Comparisons are valid only for a given
species, plant component and date. On the lOF sampling date, roots and stems were combined for analysis and leaves were not
separated into categories. 0, not detectable; ***, Ps 0.01; see Fig. 1 for other abbreviations and symbols.
Time
Treatment
Roots
Stems
Leaves
BT
Black cottonwood lOF
Non-flooded
Flooded
20F
Non-flooded
Flooded
20R
Non-flooded
Flooded
Red alder
lOF
Non-flooded
Flooded
20F
Non-flooded
Flooded
20F
Non-flooded
Flooded
Physiol. Plantarum 69, 1987
284***
93
177*
106
127**
23
21*
7
12*
4
6
6
179**
6
124*
19
215** 51
136***
2
98**
3
0
0
2
1
2*
5
0
0
2
1
T
AT
200**
5
105*
4
86**
7
0.2
0
2
1
39
Levels of N03-N were significantly reduced in all
components of flooded cottonwood seedlings during the
flooding period (Tab. 2) and were still significantly
lower in the formerly flooded cottonwood seedlings 20
days after flooding had ended. Red alder had much
lower levels of N03-N than black cottonwood, with less
variability. Ten days after flooding began, N03-N levels
were significantly lower in flooded red alder seedlings
than in non-flooded seedlings. At the end of the flood­
ing period, flooded red alder seedlings had lower
NO,-N concentrations in roots than non-flooded seed­
lings. However, by the end of the recovery period,
treatment-associated differences in root concentrations
were no longer present.
After 10 days of flooding, there were no significant
differences between P levels in black cottonwood seed­
lings, but significantly lower levels of P were present in
the leaves of flooded red alder seedlings. At the end of
the flooding period, flooded black cottonwood seed­
lings had lower concentrations of P in leaves that devel­
oped during the treatment period than non-flooded
seedlings, but by the end of the recovery period they
had significantly higher levels of P in roots and in leaves
formed during and after flooding. Twenty days of flood­
ing reduced P concentrations in all red alder compo­
nents, but by the end of the recovery period there were
no treatment differences in P levels for any of the red al­
der components.
T he total amount of P per black cottonwood seedling
did not differ significantly by treatment (Tab. 3). How­
ever, flooded or formerly flooded seedlings had a higher
proportion of total P per seedling in their root systems
than non-flooded seedlings. After 10 days of flooding,
flooded red alder seedlings had a greater proportion of
total P in root and stem tissues than did non-flooded
seedlings. At the end of the flooding period, there was
only 62% as much P in flooded red alder seedlings as in
non-flooded seedlings. T he total amount of P in leaves,
especially leaves formed during the flooding period, was
much less in flooded seedlings. By the end of the re­
covery period, seedlings in the two treatments again had
equal amounts of total P per seedling, but formerly
flooded seedlings had less P in leaves formed during the
recovery period and more in stems than non-flooded
seedlings.
Non-flooded red alder seedlings had higher levels of
Ca2+ and Mg2+ in all above-ground plant components
than flooded seedlings (Tab. 4). Total uptake of Ca2+
and Mg2+ by red alder was reduced with flooding, but
allocation between plant tissues was unaffected.
Flooded black cottonwood seedlings had much higher
concentrations of K+ in roots than non-flooded seed­
lings. However, K+ concentrations in above ground tis­
sues were lower in flooded than in non-flooded seed­
lings (Tab. 4). Flooding reduced the total amount of K+
per seedling in both species. Reductions in K+ uptake
were particularly striking for red alder: flooded red al­
der seedlings had only half as much total K+ per seed­
ling as non-flooded seedlings at the end of the flooding
period.
Concentrations of Fe in above-ground tissues were
unaffected by treatment for either species. Significant
treatment differences in Fe concentrations were ob­
served in root tissues, however, with black cottonwood
seedlings having lower Fe concentrations in roots when
flooded, whereas flooded red alder seedlings had higher
concentrations. Amount of Fe in roots and total Fe per
seedling were increased with flooding for red alder and
decreased for black cottonwood. For both species, dif­
ferences between treatments in concentrations and total
amount of Mg2+ per seedling were small, but generally
followed the same trends observed with Fe.
Tab. 3. Concentrations (mmol kg-1 ) and amounts (mg per seeding) of total phosphorus by species, treatment, date and plant com­
ponent. Amounts, given in parentheses, were calculated by multiplying concentrations by the appropriate dry weight. Significant
differences between treatments are indicated by a symbol after the value for the non-flooded treatment. Comparisons are valid
only for a given plant component and date. On the lOF sampling date, roots and stems were combined for analysis, and leaves
were not separated into categories. See Fig. 1 for abbreviations and symbols
Time
Treatment
Stems
Roots
Leaves
BT
Black cottonwood
lOF
Non-flooded
Flooded
20F
Non-flooded
Flooded
20R
Non-flooded
Flooded
Red alder
lOF
Non-flooded
Flooded
20F
Non-flooded
Flooded
20R
Non-flooded
Flooded
40
39
41
51
65
43***
102
30
30
37
35
39
42
(0.05)
(0.06)
(0.05)
(0.06)
(0.13***)
(0.22)
(0.13)
(0.20)
(0.18)
(0.16)
(0.79)
(0.86)
32
27
30
37
31***
16
34
40
(0.04)
(0.05)
(0.19)
(0.16)
70
59
20
27
38
28
(0.14)
(0.12)
(0.02*)
(0.06)
(0.06)
(0.03)
(0.17**)
(0.12)
(0.49)
(0.69)
47**
30
35
17
36
31
(0.30)
(0.23)
(0.23*)
(0.15)
(0.22)
(0.33)
T
63**
44
31**
43
56
30
34
39
(0.15)
(0.11)
(0.07)
(0.11)
(0.40*)
(0.18)
(0.30)
(0.22)
AT
Total
seedling
64* (0.50)
97 (0.41)
(0.19)
(0.18)
(0.26)
(0.28)
(0.95)
(0.93)
63 (0.65)
76 (0.39)
(0.43)
(0.43)
(0.99***)
(0.61)
(2.45)
(2.49)
Physiol. Plantarum 69, 1987
Tab. 4. Concentrations (mmol kg-1) and amounts (mg per plant component) of selected nutrients by species, treatment and plant
component at the end of the 20-day flooding period. Amounts given in parentheses were calculated by multiplying concentration
(in g kg-1) by the appropriate dry weight. Significant differences between treatments are indicated by a symbol after the value for
the non-flooded treatment. Comparisons are valid only for a given species, element and plant component. ***, P < 0.01; see Fig.
1 for other abbreviations and symbols.
Elements
and plant part
l(+
Roots
Stems
BT leaves
T leaves
Black cottonwood
Non-flooded
191**
421**
609*
596**
150***
234***
554**
266*
125
67***
165**
111***
105**
3
8
3
Total seedling
(0.08)
(0.10)
(0.12)
(0.21)
(0.15**)
(0.01)
(0.01)
(0.01)
4
2
1
1**
(0.005)
(0.006)
(0.002)
(0.005)
(0.018)
Water relations
T he two species had distinctly different diurnal patterns
of leaf conductance but, with some exceptions, flooding
had no major or consistent effect on leaf conductance of
either species (Fig. 4). During the first few days of
flooding, flooded black cottonwood seedlings generally
had higher levels of leaf conductance t han non-flooded
seedlings, and by day 5, the differences between treat­
ments were significant. T he increase in conductance was
greatest at noon when flooded seedlings had 50%
greater leaf conductance than non-flooded seedlings
( 1.38 versus 0.89 em s-1). Flooded seedlings also had
more variable maximum conductances; sos during mid­
day were three times higher for flooded than for non­
flooded seedlings. On the last day of flooding and the
second day of recovery, values for leaf conductance
Physiol. Plantarum 69, 1987
115
158
283
229
324
135**
553**
445*
(0.14)
(0.39)
(0.73)
(0.73)
202
355**
344*
227**
(1.99)
100
31
70
79
(0.07)
(0.05)
(0.11)
(0.16)
39
3
8
4
(0.07)
(0.01)
(0.03)
(0.02)
85
60***
124***
98**
(0.005)
(0.004)
(0.007)
(0.011)
(0.027)
(1.26)
(0.81)
(1.78)
(1.59)
(11.62***)
(5.44)
(1.25)
(2.48)
(2.82)
(2.11 **)
156
184
227
109
(0.33)
(0.26)
(0.63)
(0.57*)
46*
3
4
2
(0.40*)
(0.04)
(0.04)
(0.03)
92
43
82
59
(0.025)
(0.027)
(0.092)
(0.064)
(0.208)
(0.33)
(0.25)
(0.56)
(0.28)
(1.42)
82
4
4
2
(0.67)
(0.05)
(0.06)
(0.02)
(0.80)
(0.51*)
3
3
8
5
(0.89)
(1.84)
(2.48)
(0.83)
(6.04)
(1.79**)
(0.13)
3
1
2
2
220
(2.00)
87
(0.94**)
(4.54**) 164
(4.14***) 208
(8.66*)
(0.39)
(0.18*)
Total seedling
Manganese
Roots
Stems
BT leaves
T leaves
(0.15)
(0.58)
(0.51)
(0.80)
(0.47)
(0.44)
(0.91)
(1.38)
Flooded
Non-flooded
(3.20)
(0.51)
Total seedling
Iron
Roots
Stems
BT leaves
T leaves
398
177
352
430
(2.04)
Total seedling
Mg2+
Roots
Stems
BT leaves
T leaves
Flooded
(3.72*)
Total seedling
Ca2+
Roots
Stems
BT leaves
T leaves
(0.19*)
(1.05)
(0.69)
(1.79*)
Red alder
5
5
5
3
(0.039)
(0.064)
(0.075)
(0.035)
(0.213)
were lower during the afternoon in flooded black cot­
tonwood seedlings. On day 5 of recovery, formerly
flooded black cottonwood seedlings had significantly
lower conductance at 16 00 h than non-flooded seed­
lings. During the other days of the recovery period,
there were no treatment differences for black cotton­
wood.
During the flooding period, the only apparent treat­
ment effects on leaf conductance in red alder occurred
on the last day when it was significantly lower and more
variable in flooded seedlings at 12 00 and 14 00 h than
in non-flooded seedlings. On the first 2 days of the re­
covery period, non-flooded red alder seedlings had
higher leaf conductance values at 08 00 and 10 00 h than
flooded seedlings; however, midday maximums were
similar between treatments. On day 5 of recovery, non­
41
BLACK COTTONWOOD
NON- FLOODED
• FLOODED
D
o
RED ALDER
Fig. 4. Mean leaf conductance
by species, treatment and time
of day: (A) day 1 of flooding
(flooding began at 09 00 h), (B)
day 5 of flooding, (C) day 10
of flooding, (D) day 2 of re­
covery, (E) day 5 of recovery,
(F) day 10 of recovery. X on
time axes indicates when
photosynthetically active
radiation exceeded 150 tmol m-2 s-1• n 6. =
E
XXXXXX xxxxxxxxxxxxx
F
XX)(XXX XXXXXX
1200
1600
0800
1200
1 6 00
2000
tonwood seedlings were significantly lower than those in
non-flooded seedlings. By the end of the flooding
period, there were no treatment differences in root con­
ductance for black cottonwood seedlings.
Red alder exhibited no significant differences in xy­
lem pressure potential between flooded and non­
flooded seedlings (Tab. 6). Black cottonwood had signi­
ficantly more negative potentials in the flooded seed­
lings from the beginning of flooding (first measurements
taken after 12 h) up through day 13. By the end of the
treatment period, however, there were no treatment
differences in the xylem pressure potential of black cot­
tonwood seedlings.
flooded seedlings again had higher values for leaf con­
ductance from 08 00 to 14 00 h (when the midday peak
in conductance occurred), but only the difference at the
12 00 h reading was statistically significant. There were
no other treatment-associated differences in red alder
leaf conductance during the recovery period.
Hydraulic root conductance increased in red alder
seedlings during the measurement period, but did not
differ between treatments (Tab. 5). Black cottonwood
seedlings did not exhibit a consistent trend of increasing
or decreasing root conductance during the treatment
period. During the first half of the flooding period,
however, root conductance values in flooded black cot-
Tab. 5. Hydraulic root conductance of seedling root systems by species, treatment and time since flooding. Significance of treat­
ment differences is indicated by the symbol after the value for the non-flooded treatment. Comparisons are valid only for a given
species and plant component. See Fig. 1 for symbols.
Days since
flooding began
Root conductance 10-11 MPa-ts-1
Non-flooded
1-2
4--5
10
20
42
Red alder
Black cottonwood
4.4**
5.1**
5.0**
4.5
Flooded
Non-flooded
Flooded
3.0
2.9
3.1
4.4
4.1
4.0
4.3
6.8
3.5
3.4
5.0
6.7
Physiol. Plantarum 69, 1987
Tab. 6. Xylem pressure potential of upper stem leaves by species, treatment and date. Paired measurements (non-flooded and
flooded) taken at various times during the day and analyzed using a paired /-test. Significance of treatment differences is indicated
by the symbol after the value for the non-flooded treatment. Comparisons are valid only for a given species and plant component.
***' p :S 0.01.
Days in flooding (F)
or
recovery (R) period
-XPP (MPa)
Non-flooded
F1-3
F12-13
F20
R1
R12
Red alder
Black cottonwood
0.30***
0.50***
0.68
0.70
0.76
Flooded
Non-flooded
Flooded
0.81
0.61
0.63
0.80
0.74
0.33
0.55
0.51
0.32
0.33
0.33
0.60
0.55
0.44
0.36
Morphology and anatomy
Flooded red alder seedlings exhibited pronounced
lower-stem hypertrophy, enlarged lenticels, and adven­
titious roots. After 20 days of flooding, most flooded
red alder seedlings had several short (1G-50 mm)
cream-colored adventitious roots that only emerged
from the stem at or just above the root collar. After
flooded pots were allowed to drain, the adventitious
roots darkened and began growing downward into the
soil. Some seedlings exhibited chlorosis during the latter
half of the flooding period, but this gradually disappear­
ed during the recovery period. By the end of the flood­
ing period, most red alder nodules in flooded pots were
covered with numerous tiny roots. These nodule roots
did not grow appreciably during the recovery period,
and by its end, they had darkened in color and were in­
conspicuous.
Red alder root tips from non-flooded pots exhibited
greater endodermal thickening or suberization than
those from flooded pots. Adventitious roots (but not
below ground roots) of flooded red alder seedlings exhi­
bited many large thin-walled aerenchyma that were ir­
regular in shape and appeared to be randomly distri­
buted throughout the cortical parenchyma.
Lenticels on flooded black cottonwood seedlings be­
came hypertrophied, and several short adventitious
roots emerged at or just above the root collar. By the
end of the flooding period, many of the black cotton­
wood seedlings had experienced extensive root mor­
tality. In particular, fine lateral roots died back, and
many long, unbranched lateral roots shed all tissues ex­
terior to the cambium, leaving the woody stele exposed.
Roots close to the soil surface appeared more normal
than those deeper in the soil. In contrast to observations
of red alder seedlings, flooded black cottonwood seed­
lings exhibited only minor stem hypertrophy. Some
flooded black cottonwood seedlings had chlorotic
foliage and a few exhibited pronounced red or purple
veinal coloration. During the recovery period, foliage
with abnormal coloration regained normal color and
newly formed leaves were normal in appearance.
Physiol. Plantarum 69, 1987
Fig. 5. Radially-oriented aerenchyma in root tip of black cot­
tonwood seedling after 20 days of flooding (bar 50 [1m).
Both adventitious roots and root tips from lateral
roots of flooded black cottonwood had more layers of
cortical parenchyma than those of non-flooded seed­
lings (5-8 vs 2-3). In addition, within 10G-200 tm of the
root tips, the cortical tissues of adventitious roots and
flooded lateral roots became aerenchymatous. The lysi­
genous aerenchyma radiated outward symmetrically
from the stele (Fig. 5). Root tips from flooded pots ex­
hibited less epidermal suberization than those from
non-flooded pots.
Discussion
Survival and growth
Both red alder and black cottonwood are generally con­
sidered to be fairly tolerant of excess soil moisture (Mi­
nore 1979). However, 100% survival was better than
anticipated for this study. Minore (1968) artificially
flooded red alder seedlings and recorded 100% survival
in his non-flooded and winter-flooded treatments but
only 50 and 65% in his 4- and 8-week summer flooding
treatments. No similar experiments have been reported
43
for black cottonwood, although lack of soil aeration is
known to reduce its growth (Smith 1957).
Crawford ( 1971) distinguished flood-tolerant species
from intolerant species by their growth rates after flood­
ing ended. In this experiment, total biomass accumula­
tion, biomass distribution, height growth and leaf area
increment for black cottonwood were all unaffected by
treatment during the flooding period but were reduced
or altered during recovery. In contrast, flooded red al­
der exhibited reduced height growth, reduced leaf area
increment, and changes in biomass distribution during
flooding, but total biomass per seedling did not differ
between treatments at the end of recovery. Formerly
flooded red alder seedlings initially showed reduced
height growth and leaf area increment; however, differ­
ences between treatments diminished over time. Thus,
based on Crawford's criterion, red alder demonstrated
greater flood tolerance than black cottonwood. This
finding is consistent with the ecological distribution of
the two species; i.e., red alder is more common than
black cottonwood on sites where internal soil drainage
is restricted and it is considered to be more tolerant of
soil waterlogging (Walters et al. 1980).
Plant nutrient relations
In the present study, concentrations of NO:; were lower
in all plant tissues of both species when flooded (Tab.
2). Based on the observed soil reduction potential,
much of the soil nitrate would have been reduced to gas­
eous compounds (N2, N20) and thus be unavailable for
root uptake. Drew and Sisworo ( 1977, 1979) reported
that soil waterlogging resulted in sharp decreases in ni­
trogen uptake and concentrations in above ground tissues
of barley; nitrate-N levels were more sensitive to change
than total N. They found that N was transported from
older leaves to younger leaves under flooded condi­
tions. However, in the present experiment, differences
in NO,-N concentrations between leaf ages were similar
for both flooded and non-flooded seedlings at the end of
the flooding period. By the end of the recovery period,
though, non-flooded black cottonwood seedlings had
fairly uniform N03-N levels for the leaf categories,
whereas formerly flooded seedlings had the highest con­
centrations in the youngest leaves (AT).
Effects of flooding or waterlogging on uptake and al­
location of P have not been consistent in previous re­
ports (Drew and Sisworo 1979, Hook et al. 1983, Jack­
son 1979, Keeley 1979). During the flooding period in
the present study, P concentrations were significantly
reduced in aboveground tissues of both species but
changes in belowground tissues were non-significant
(Tab. 3). Based on foliar symptoms and concentrations
observed in P-deficient eastern cottonwood by Hac­
skaylo et al. ( 1969), flooding probably induced a tem­
porary P deficiency in the leaves of at least some
flooded black cottonwood seedlings. However, for­
merly flooded black cottonwood seedlings had higher I?
44
concentrations in roots and leaves (T and AT) at the end
of the recovery period and a much greater proportion of
total P per seedling in their root systems than non­
flooded seedlings.
K+ uptake has been consistently reported to decline
under flooding (Drew and Sisworo 1979, Jackson 1969,
John et al. 1974). K+ concentrations in tissues, how­
ever, have increased or decreased depending on the
relative amount of plant growth. In the present study,
flooded red alder seedlings had lower concentrations of
K+ in all tissues than non-flooded seedlings (Tab. 4). In
both species, flooding reduced total K+ uptake and
probably caused an increase in net translocation of K+
from older leaves to the newly expanding leaves. Foliar
K+ concentrations in flooded red alder were above def­
iciency levels (Hughes and Gessel 1968), but may have
been low enough to have caused the slower postdawn
stomatal opening observed at the end of flooding and
the beginning of recovery. K+ concentrations were in­
creased in roots of flooded black cottonwood, but de­
creased in all aboveground tissues. Reductions in K+
transport to aboveground tissues and in root hydraulic
conductivity in flooded black cottonwood may both
have been caused by the effects of abscisic acid (ABA)
on membrane permeability (Addicott and Van Steve­
ninck 1983, Pitman and Cram 1977, Van Steveninck and
Van Steveninck 1983). Foliar ABA levels have been
found to increase with flooding in some species (Shay­
bany and Martin 1977, Wright 1978) and inhibition of
ion transport to the xylem without inhibition of ion up­
take can be caused by changes in ABA levels (Cram and
Pitman 1972, Pitman and Cram 1977, Pitman and Well­
fare 1978).
In previous studies (Hook et al. 1983, Jackson 1979,
Keeley 1979), Ca2+ and Mg2+ concentrations have de­
creased under flooding for some species and tissues but
not for others. In the present experiment, Ca2+ and
Mg2+ concentrations in aboveground tissues of both spe­
cies were generally reduced with flooding (Tab. 4).
Lower Ca2+ concentrations in roots of flooded black
cottonwood may have resulted from sloughing of older,
more woody roots.
Both Fe and Mn become more soluble under an­
aerobic soil conditions, and their concentrations (par­
ticularly in root tissues) have been reported to increase
with flooding (Hook et al. 1983, Jones 1970, Keeley
1979). As with previous studies, flooded red alder seed­
lings had higher root system concentrations of Fe and
Mn than non-flooded seedlings. In contrast, flooded
black cottonwood seedlings had lower concentrations of
Fe and Mn in their root systems than non-flooded seed­
lings. Black cottonwood seedlings may possibly have
had increased uptake of Fe and Mn when flooded, but
the seedlings did not retain these elements. For exam­
ple, Fe and Mn may have accumulated in the cortical
free space of the root system. Large amounts of these
outer root tissues were sloughed off in flooded black
cottonwood pots. In addition, older roots that had accuPhysiol. Plantarum 69, 1987
mulated high Fe and Mn concentrations may have died
and also have sloughed off. Since black cottonwood
seedlings formed root aerenchyma when flooded, it is
also possible that these aerenchymatous channels were
efficient enough in gas transport to have resulted in suf­
ficient rhizosphere oxidation (Bartlett 1961) to have re­
duced Fe and Mn uptake.
Water relations
Leaf conductance in this experiment was basically unaf­
fected by flooding. This is in contrast to the stomatal
closure under flooding observed in many herbaceous
species (Bradford and Yang 1981) and in several woody
plants (Blake and Reid 1981, Coutts 1981, Kozlowski
and Pallardy 1979, Pezeshki and Chambers 1985, Re­
gehr et al. 1975, Serra Gomes and Kozlowski 1980a,b,
Tang and Kozlowski 1982). The only species previously
reported not to close their stomata when flooded are
sunflower (Thorton and Wample 1980) and loblolly pine
(Kramer 1951). In addition, a recent report indicated
that flooding had no effect on photosynthesis of Scots
pine (Zaerr 1983); thus, presumably stomatal closure
did not occur. Stomatal reopening following flooding­
induced closure has been suggested as indicating flood
tolerance (Serra Gomes and Kozlowski 1980a). How­
ever, whether or not stomatal closure occurs with flood­
ing has not been shown to be related to flood tolerance
(present study; Blake and Reid 1981).
The commonly observed decrease in leaf conduct­
ance with flooding has historically been assumed to be
caused by a decrease in root hydraulic conductance fol­
lowed by a decrease in leaf water potential, which, in
turn, causes stomatal closure (Biron and Wright 1973,
Kramer 1983). This apparently logical chain of events
has only been illustrated once (Syvertsen et al. 1983),
and other studies indicate that additional mechanisms
are involved. Leaf water potential (or the rate of change
in leaf water potential) has been shown to be correlated
with leaf conductance under non-flooded conditions
(e.g. Cohen and Cohen 1983, Cowan and Farquhar
1977, Jarvis 1976), but since the response of leaf water
potential to flooding has not been consistent (Bradford
and Yang 1981) and stomatal closure in flooded plants
has been shown to occur in the absence of water deficit
(Blake and Reid 1981, Jackson et al. 1978, Pereira and
Kozlowski 1977), factors other than decreased leaf wa­
ter potential must be involved in triggering stomatal clo­
sure.
Sojka and Stolzy ( 1980) concluded that low soil oxy­
gen does not have a consistent effect on plant water po­
tential, and stomatal closure at low soil oxygen levels
"may not be entirely a passive mechanical response" to
decreases in plant water potential. Most studies have re­
ported flooding to have either no effect or to increase
leaf water potential (Bradford and Yang 1981), but de­
creases have also been reported (Syvertsen et al. 1983,
Zaerr 1983). In the present study, leaf water potential
Physiol. Plantarum 69, 1987
was unaffected by flooding in red alder but was initially
decreased in black cottonwood.
Morphology and anatomy
The role of adventitious roots in plant response to
flooding is not clear. Flooding has been shown to reduce
gibberellin and cytokinin levels (Burrows and Carr
1969, Reid et al. 1969), and adventitious roots may be
important because they produce gibberellins and cytoki­
nins necessary for function and growth of aboveground
tissues (Gill 1975, Reid and Crozier 1971). Reid and
Crozier ( 1971) reported an increase in gibberellin con­
tent in tomato shoots on the third day of flooding when
gibberellin content in roots was still decreasing, and ob­
served that this increase coincided with the appearance
of adventitious roots. Serra Gomes and Kozlowski
( 1980b) concluded that stomatal opening following floo­
ding-induced closure was closely associated with the for­
mation and production of adventitious roots. The link
between stomatal function and production of adventit­
ious roots has not been identified. Stomatal regulation
has been linked with abscisic acid levels, and other plant
growth substances were not thought to be involved in
stomatal regulation (Mansfield and Heath 1962, Wright
1972, 1978). A recent report (K. J. Bradford unpub­
lished, cited in Zeiger 1983), however, documents an ef­
fect of root cytokinins on stomatal conductance of
flooded tomato plants. Levels of plant growth sub­
stances associated with flooding have not been reported
for species that do not exhibit flooding-induced stom­
atal closure.
Reductions in root hydraulic conductivity can be
caused by changes in the water-absorbing surface (such
as suberization) or by changes in membrane permeab­
ility (Ramos and Kaufmann 1979). In the present study,
cottonwood seedlings exhibited reduced root conduc­
tivity and more negative xylem pressure potentials
within a day of flooding. The decreased root conduct­
ance occurred too rapidly to be attributed to treatment­
caused differential root growth or development. In ad­
dition, anatomical investigation showed suberization of
root tips to be decreased with flooding rather than in­
creased as would be required if the length of unsub­
erized root tips were to be decreased. Thus, root con­
ductivity in cottonwood seedlings was probably de­
creased due to reduced membrane permeability. Root
conductivity in flooded black cottonwood seedlings in­
creased to the level of non-flooded seedlings before the
end of the flooding period, possibly due to higher con­
ductivity associated with roots which have recently died
(Kramer 1933) or changes in seedling root systems. For
example, aerenchyma development may increase inter­
nal root aeration sufficiently to reverse the anaerobic­
caused reduction in membrane permeability to water.
Another possibility is that new roots formed during
flooding may be more conductive than those formed
prior to flooding.
45
In mesophytes, flooding-induced formation of aeren­
chyma in the roots is generally considered to be a bene­
ficial adaptation to flooding (Armstrong 1972, Coutts
and Armstrong 1976, Kawase 1981, Kawase and Whit­
moyer 1980), although the degree of aerenchyma devel­
opment does not indicate the relative flood tolerance of
a species (Hook and Scholtens 1978 , Smirnoff and
Crawford 1983). Aerenchyma formation cannot reverse
all the negative effects of flooding, and prolonged flood­
ing will result in t he death of any non-hydrophytic spe­
cies.
It has been suggested that morphological and phys­
iological root adaptations are critical in determining
relative flood tolerance (Hook and Brown 1973).
Changes in physiological root characteristics were not
assessed in the present study. T he anatomical and mor­
phological changes in root systems of flooded black cot­
tonwood apparently adapted seedlings to the anaerobic
environment successfully enough that aboveground
growth was basically unaffected during flooding. How­
ever, the changes in black cottonwood root systems in
reponse to flooding may also have made the root system
less functional under the better aerated conditions of
the recovery period. On the other hand, red alder ­
which exhibited few anatomical and morphological
changes in its root system when flooded - was judged to
be the more flood tolerant species based on its growth
during the combined treatment and recovery periods.
Assessing several plant characteristics, both during and
following flooding, is recommended to accurately rank
species as to their relative flood tolerance and to under­
stand the various plant strategies used in dealing with
such stress.
Acknowledgements- The author thanks H. M. Culliton, R. L.
Deal, J. E. Wilcox, B. M. Casson and W. C. Carlson for tech­
nical assistance and T. M. Hinckley, D. S. DeBell, D. D.
Hook, E. L. Stone, and two anonymous reviewers for their
helpful comments on earlier versions of the manuscript.
The use of trade, firm or corporation names in this article is
for the information and convenience of the reader. Such use
does not constitute official endorsement or approval by the
U.S. Dept of Agriculture of any product or service to the ex­
clusion of others that may be suitable.
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