Aquatic Botany, 14 (1982) 295--307
295
Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands
FACTORS INFLUENCING POTENTIAL INTRALAKE COLONIZATION
BY M Y R I O P H Y L L U M S P I C A T U M L.
JEFFREY C. KIMBEL*
Department of Botany, University of Wisconsin, Madison, WI 53706 (U.S.A.)
(Accepted for publication 30 March 1982)
ABSTRACT
Kimbel, J.C., 1982. Factors influencing potential intralake colonization by Myriophyllum
spicatum L. Aquat. Bot., 14: 295--307.
A factorial experimental design was used to determine which of several factors influence Myriophyllum spicatum L. vegetative colonization success. Also, the relationship
between total nonstructural carbohydrate (TNC) content, a measure of propagule vigor,
and propagule success was detailed. Colonization success in terms of growth and mortality was best during late summer in shallow water on rich organic sediments. Light availability, temperature, and sediment nutrient levels were high during this period. The
poorest colonization conditions occurred during early autumn. During this period
mortality was highest in deep water in calcareous nutrient poor sediments. Also, naturally produced vegetative fragments grew better than artificially abscised meristems and had
higher TNC concentrations. Low TNC levels increased mortality, but they had no effect
on subsequent growth, suggesting that naturally produced fragments are more likely to
survive the winter than artificial fragments.
INTRODUCTION
M yr io p h yllu m spicatum L., Eurasian w a t e r milfoil, is a s u b m e r s e d aquatic
p l a n t o f t e n c o n s i d e r e d to be a weed in the U n i t e d States. It has spread rapidly f r o m its p o i n t o f i n t r o d u c t i o n in C h e s a p e a k e Bay (Nichols, 1 9 7 5 ) a n d can
d o m i n a t e s u b m e r s e d m a c r o p h y t e c o m m u n i t i e s f o r m a n y years (Carpenter,
1 9 8 0 a ) . R e p r o d u c t i o n is i m p o r t a n t in m a i n t a i n i n g d o m i n a n c e (Grace and
Wetzel, 1 9 7 8 ) t h r o u g h e s t a b l i s h m e n t and eventual o c c u p a t i o n o f space by
biomass p r o d u c t i o n , M. spicatum is a highly efficient c o l o n i s t (Patten, 1 9 5 6 ;
N i c h o l s o n and Clerman, 1 9 7 7 ) b u t seedling e s t a b l i s h m e n t is rare (Patten,
1 9 5 6 ; Davis et al., 1 9 7 3 ; Grace a n d Wetzel, 1 9 7 8 ; A i k e n et al., 1 9 7 9 ) . Little
is k n o w n a b o u t the variables i n f l u e n c i n g vegetative c o l o n i z a t i o n and t h e y
axe the f o c u s o f this s t u d y .
A factorial e x p e r i m e n t a l design was used t o test vegetative p r o p a g u l e success in t h e field. Success was m e a s u r e d as biomass a c c u m u l a t i o n and survival.
T i m e o f year, s e d i m e n t t y p e and d e p t h were regarded as i m p o r t a n t variables
*Present address: Department of Botany, University of Texas, Austin, TX 78712, U.S.A.
0304-3770/82/0000--0000/$02.75 © 1982 Elsevier Scientific Publishing Company
296
influencing success. Two different types of vegetative propagules were used;
autofragments, attached shoots that begin rooting and are released naturally
and allofragments, plant fragments with meristematic tissue but lacking preformed roots, released by artificial abscission (due to motorboat use or
mechanical harvesting).
Although growth and mortality are ultimately dictated by the physical
environment, this influence is buffered by a plant's ability to withstand
stress. The internal carbohydrate content (measured as total nonstructural
carbohydrate or TNC) is often used as an index of tolerance to environmental
variation (Smith, 1968; Titus and Adams, 1979). Vegetative propagules
with greater amounts of TNC should have greater success in establishment
and growth. Therefore, TNC levels were monitored and a field experiment
explored the relationship between initial propagule TNC content and success.
The results of both the factorial and TNC experiments were used to predict
the fate of overwintering propagules.
SPECIES AND SITE CHARACTERISTICS
Myriophyllum spicatum is a herbaceous, submersed plant with long flexuous
stems and thin dissected leaves. It is a perennial, overwintering under the ice
cover as a group of bright green stems. In the spring, these stems begin to
elongate and by early June have reached the water surface. At this time 75%
of the plant's biomass is concentrated in the top 30 cm of the water column
(Titus, 1977). Typically, flowering is from mid to late June.
After flowering, standing crop biomass declines due to fragmentation.
Autofragrnents develop adventitious roots before abscission, settle to the
bottom and grow. Further growth of both established plants and autofragments during the midsummer months results in maximum biomass
(Gustafson and Adams, 1973} and a second flowering period in mid-August.
Fragmentation occurs again and plants die back by early November.
This study was conducted in Lake Wingra, a small, shallow (mean depth
2.4 m}, hardwater, eutrophic lake in suburban Madison, Wisconsin. One-third
of the lake's area is littoral zone (Gustafson and Adams, 1973) which until
recently was dominated by M. spicatum.
METHODS
Experimental design and independent variable analysis
A factorial design of two levels for each of four variables was employed for
the first portion of the project. Substrate, depth, time of year and propagule
type were used as variables. A quantitative description of these categorical
factors was made as follows.
297
Sediment
Two substrates, eastern and western, were selected from different parts
of the lake. Sediments were analyzed for ammonium (NH4-N), nitrate
(NO3-N) and potassium (K) by the Soil and Plant Analysis Laboratory, University of Wisconsin, Madison; total phosphorus (TP) and total inorganic
phosphorus (TIP), using a modified Mehta procedure (Prentki, 1979); percentage organic matter (%OM), by combusting samples (550 ° C, 4 h) and
weighing the residue; hydrogen ion content (pH), using a Corning pH meter;
and percentage calcium carbonate (%CaCO3), by combusting samples
(950°C, 4 h) and weighing.
Depth
The experiment was conducted using 0.5 m and 1.0 m depths to simulate
different light intensities. Water temperature did not vary with depth. Photosynthetically-active radiation was measured using a Lambda Instruments
quantum meter equipped with an underwater probe.
Time of year
A portion of the 1978 growing season was divided into approximately two
four-week parts, from 1 August until 31 August (late summer), and from 5
September until 10 October (early autumn). The second period coincided
with the time of maximum autofragment release. Water temperature (0.2 m
depth), pH and alkalinity were periodically monitored. Alkalinity was calculated as CaCO3 using an acid titration (APHA, 1971). Hydrogen ion content was measured using a Beckman portable pH meter.
Propagule type
Allofragments (20 cm M. spicatum meristematic tips) and autofragments
(segments with preformed roots) were sampled twice during the summer of
1978. Both types were assayed by the Soil and Plant Analysis Laboratory,
University of Wisconsin, Madison for total nitrogen (TotN), phosphorus (P)
and potassium (K). The first autofragment collection came from University
Bay, Lake Mendota, Wisconsin. University Bay's size and characteristics are
similar to Lake Wingra's (see Lind and Cottam, 1969; Titus, 1977).
Field and laboratory methods
Sediments were contained in plastic pans (31 × 23 × 13 cm) held in a
wooden frame. Depth was controlled by adjusting a cord running between the
frame and an anchor. Fragments were collected a few hours before insertion
into the sediment. They were fastened in place by passing the stem base and
a set of lower leaves through wire screening (6.4 mm mesh) attached to the
frame. Fifty propagules per pan were planted (7 propagules dm -2) and the
frame lowered to either 0.5 m or 1.0 m from the water surface. The two
frames were located within 15 m of each other near the east shore.
298
After 4 weeks stem material was collected, dried (70°C) and weighed.
Since the percentage of M. spicatum ash does n o t vary significantly in Lake
Wingra (Carpenter, 1980b), dry weight was used in growth calculations. Propagule mortality was measured by counting survivors after 4 weeks. It was
assumed that any losses n o t due to mortality were constant between treatments.
TNC levels were monitored during the summer and early autumn of 1978.
Allofragments were sampled on four dates; autofragments were collected on
two dates. Samples were divided into groups of five, dried at 70°C and ground
to pass through a 40 mesh screen. TNC was then assayed in duplicate 100
mg subsamples by iodometric titration as reducing sugars after enzymatic
digestion (Smith, 1969).
In early October 1978 allofragments were collected and placed in a dark,
aerated chamber for 3 or 7-day periods. This effectively reduced TNC content
to two different levels. These fragments, along with freshly collected ones,
were planted in plastic pans containing western sediment (Table I). Thirty
fragments per pan (4.2 plants dm -2) were planted on 2 October and anchored
at 0.5 m from the water surface. Collections were made after 7 and 15 days.
Plants were then counted, dried (70°C), weighed and assayed for TNC.
TABLE I
Eastern and western sediment physio-chemical characteristics
(Each confidence interval is one standard error (s/x/n) for 6 replicates. Differences
were detected using a t-test.)
Component
East
West
NH4--N (rag I-' )*
NO3--N (rag I-')
K(mg]-')**
18 +2
5.3 +1.9
25 +0
116 -+23
9.3 -+2.3
78 +15
'rP (~g 1-1)
TIP (ug 1-1)**
pH**
OM (%)
CaC03 (%)*
208
56
7.49
9.2
53
+74
-+12
-+0.03
+0.6
-+1
584
336
7.29
12.1
47
+129
+40
-+0.06
+1.5
-+3
*0.05 > P > 0.01.
* ' 0 . 0 1 > P > 0.001,
Calculations
Growth was determined by taking the difference between an average initial
dry weight and that of the sample and dividing by the number of growing
days. In some cases growth was negative.
Analysis of variance (ANOVA) was used on both dependent variables
(growth and mortality). In the analyses involving mortality measurements,
three and four-factor interaction mean squares were averaged and used as
measure of residual error (Sokal and Rohlf, 1969; Box et al., 1978).
299
RESULTS
Independent variable analysis
A t-test showed that eastern and western sediments differed @gnificantly
except for NO3-N concentration (Table I). Qualitatively, eastern sediments
were more consolidated and had a larger particle size. Western sediments appeared to be more conducive to plant growth, having greater amounts of
available N and P fractions.
Average light intensity was ~ 3 . 9 times greater at 0.5 m than at 1.0 m. Light
availability was also greater during late summer than in early autumn (Table
II; and Duffie and Beckman, 1974). Alkalinity and pH were a b o u t the same
during the two time periods (Table II).
TABLE II
Average environmental characteristics during the late summer and early a u t u m n
growing periods
Late summer
1--31 August
Water temperature (°C)
Surface light*
(Langley/day)
Light extinction
coefficient**
pH
Alkalinity
(mg 1-1 as CaCO3)
26.4
Early autumn
5 September-10 October
18.9
463
365
-0.026
8.4
-0.028
8.3
140
156
*Duffie and Beckman (1974; average for Madison, Wisconsin).
**R.C. Jones (personal communication, 1979).
TABLE III
Analysis of allo- and autofragments during the two study periods
(Differences were detected using a t-test)
3 August
Allofragment
Autofragment
Total N (%)
P (%)
K (%)
1.84 -+0.31
0.17 -+0.01
0.41 -+0.08
1.47 +-0.25
0.16 +-0.01
1.01 +-0.10
1.69 +-0.09
0.22 -+0.02
0.80 -+0.16
1.72 +-0.06
0.13 +-0.01"
0.80 -+0.12
6 September
Total N (%)
P (%)
K (%)
*0.05 > P > 0.01.
300
Allofragments and autofragments had similar N, P and K concentrations
in early August (Table III). Phosphorus levels were higher in allofragments in
early September.
Independent variable effects
Under the range of variables studied, time of year ("season" in
Table IV) had a significant effect on mortality. The depth X season interaction was also significant (Table IV). Mortality was about 24% higher
during early autumn but increased with depth during late summer while it
decreased with depth during early autumn (Fig. 1).
Average growth was 4.6 times greater during late summer than in early
TABLE IV
Analysis of variance for propagule mortalities as a function of sediment type, depth,
time of year (season) and propagule type
Factor
Degrees of
freedom
Mean
square
F Ratio
Sediment (Sd)
Depth (D)
Season (Se)
Propagule (P)
Sd x D
Sd × Se
Sd x P
D X Se
DXP
Sex P
Error
1
1
1
1
1
1
1
1
1
1
5
30.25
24.01
2410.81
764.52
203.06
150.06
30.25
2910.60
21.16
424.36
191.73
0.16
0.13
12.57"
3,99
1.06
0.78
0.16
15.18"
0.11
2,21
*0.05 > P > 0.01.
80
60
66.9
F-
%MORTALITY 40
I
38.3
20
SEASON
e
~
O.5m
1.0m
DEPTH
Fig. 1. Propagule mortality during late summer (l.s.) and early a u t u m n (e.f.) at 0.5 and
1.0 m depth.
301
autumn. The magnitude of this effect clouded the analysis. In order to
further clarify h o w independent variables were functioning, the design was
divided into t w o factorials, each representing a time period. During late
summer, sediment and depth had significant main effects and a significant
interaction (Table V). Growth was a b o u t 10 times greater at 0.5 m in western
sediment than at an:- other contingency (Fig. 2). The lowest growth response
occurred in eastern sediments at 1.0 m. The early autumn results had a highly significant three-factor interaction (Table VI). Fastest (least negative) growth
occurred for allofragments in eastern sediment at 0.5 m depth (Fig. 3). However, under the same conditions at 1.0 m depth the slowest growth occurred.
Overall, autofragments grew twice as well as allofragments.
TABLE V
A n a l y s i s o f variance for p r o p a g u l e g r o w t h r a t e s d u r i n g late s u m m e r
Factor
Degrees o f
freedom
S e d i m e n t (Sd)
D e p t h (D)
P r o p a g u l e (P)
Sd × D
Sd x P
D x P
Sd X D X P
Error
1
1
1
1
I
1
1
23
Mean square
(× 10 -4)
F Ratio
4.15
4.84
0.07
1.27
0.00
0.14
0.33
0.17
24.31"*
28.39**
0.42
7.42*
0.00
0.84
1.95
* 0 . 0 5 > P > 0.01.
**0.01 > P > 0.001.
1.2
1.0
1.15
--
0.8
GROWTH
i
I
0.6
(g d r y w t da -1)
0.4
o.2
West
SED
I
~ __--~ ~
0.Sin
DEPTH
1.Ore
0.0
-0.2
[~
"0.23
Fig. 2. P r o p a g u l e g r o w t h r a t e s d u r i n g late s u m m e r in e a s t e r n a n d w e s t e r n s e d i m e n t s a t
0.5 a n d 1.0 m d e p t h .
302
TABLE VI
Analysis of variance for propagule growth rates during early autumn
Factor
Degrees of
freedom
Mean square
(× 10 -4)
F ratio
Sediment (Sd)
Depth (D)
Propagule (P)
Sd X D
Sd X P
D XP
Sd x D × P
Error
1
1
1
1
1
1
1
23
0.02
0.04
1.14
1.02
0.01
0.27
1.03
0.04
4.25*
0.93
26.23**
23.50**
0.16
6.20*
23.07**
*0.05 > P > 0.01.
* ' 0 . 0 1 > P > 0.001.
0.000
SED.
West~i,
East
//
r-i
r---:
0.Sm
~-~..__ ~ 3 J
"~
°°05
'
,oo, ,/
:o~'.:=;
:,
GROWTH
(gdrywtda 4)
Auto,
-.003
1.0m
DEPTH
West
East
o.ooo
//•r--]
.ooo,;
.ooo
,
~
i
I
'
-o.oo5
"
,'~ -.0~0~
-0.Srn 1.OreLJ,I I
AIIo.
DEPTH
--
'
I
Ii
-0.010
I
-,011
Fig. 3. Autofragment (Auto.) and ailofragment (Allo.) growth during early autumn in
eastern and western sediments at 0.5 and 1.0 m depth.
Non-structural carbohydrate effects
Allofragment TNC values remained a b o u t the same for most of the sampling period, decreasing during autumn {Fig. 4). Autofragment TNC levels
increased 17% from late summer to early autumn (Fig. 4) on the 6 September
samplings were a b o u t twice those of allofragments (t-test, P < 0.02).
The importance of high TNC levels to fragment survival and growth was
determined b y altering TNC content and measuring growth and survival. Darkness effectively reduced initial TNC levels, b u t recovery was rapid once propagules were placed in the field (Fig. 5). After 8 days there was no difference
303
2°I
15
(D
ae
z lo
~\\\\
~
[
J
I
A
1978
I
S
0
]
Fig. 4. Allofragment (e) and autofragment (o) TNC concentrations during summer 1978.
Each confidence interval is -+ o n e s t a n d a r d e r r o r f o r 4 replicates.
7
6
0
2
4
6
8
10
TIME(days)
12
14
16
Fig. 5. Time course of allofragment TNC concentrations after placement in the field.
in TNC c o n t e n t b e t w e e n plants initially having highest and m i d d l e range TNC
c o n c e n t r a t i o n s . A f t e r 15 days all c o n c e n t r a t i o n s were virtually the same.
Initial T N C c o n c e n t r a t i o n altered i m m e d i a t e g r o w t h b u t had n o lasting
effect. Most p r o p a g u l e s lost weight w h e n placed in situ (Fig. 6). Propagules
with the highest i n i t i a L T ~ C c o n t e n t lost the m o s t weight (and T N C ) b u t had
the m o s t rapid r e c o v e r y (Fig. 6). T h e r e was n o d i f f e r e n c e b e t w e e n g r o w t h
rates over t h e last 8-day interval and overall ( A N O V A , P > 0.05).
304
80
0.02
70
60
"~ 0.01
>- 5 0
I-._l
,<
I- 40
I
~
0
30
0.00
a
b
20
10
-0.01
a
8 days
15 d a y s
0
Fig. 6. Allofragment growth rates after 8 and 15 days in the field. Initial TNC concentrations were 0.0% (a), 0.3% (b), and 5.4% (c).
Fig. 7. Allofragment mortality after 15 days in the field. The letters a, b, and c are the
same as in Fig. 6. The vertical bar is -+ one standard-error for 20 b i n o m i a l l y distributed
variates. Mortality difference b e t w e e n b and c is significant (z = 2.34, P < 0.05) 'as is the
difference b e t w e e n a and c (z = 3.15, P < 0.001).
Initial TNC content was inversely related to mortality (Fig. 7). However,
a 95% reduction in TNC resulted in only a 23% increase in mortality.
DISCUSSION
A favorable colonization environment shifted with depth and time. Low
mortality occurred during late summer in shallow water then during early
autumn in deep water. Substrate and propagule type did not affect mortality.
Several observers (Pearsall, 1920; Misra, 1938; Hutchinson, 1975} have noted
changes in aquatic plant distribution with substrate changes. Patten (1955)
comments that M. spicatum was not found on the sandy sediments in the
lake he studied. Nicholson et al. (1975) found an interaction of macrophyte
abundance with depth. However, Giesy and Tessier (1979) found that
M. spicatum interlake colonization was not limited by substrate composition.
In Lake Wingra M. spicatum has been observed to grow luxuriantly over the
entire littoral zone, regardless of substrate type. Sediment type may not show
an effect when nutrients are in excess of basic needs (Barko and Smart, 1981).
Growth was influenced by several non-additive effects. Grace and Wetzel
(1978) review influences on M. spicatum production and conclude that
growth is governed by a large set of interacting variables. Recent studies
(Best and Mantai, 1978; Bole and Allan, 1978; Smith, 1978; Barko and
Smart, 1979; Aiken and Picard, 1980; Carigan and Kalff, 1980) have shown
that the mineral nutrition ofM. spicatum is greatly dependent upon sub-
305
strate chemistry. For example, Smith {1978) found that 73% of M. spicatum
phosphorus uptake is by the roots. In the present study, the substrate effect
on propagule growth was significant. However, depth (light intensity) also
was significant. Estimating from Adams et al. (1974), M. spicatum net photosynthesis at 1.0 m depth is 27% of that at 0.5 m. Furthermore, temperature
is a strong influence on aquatic plant biomass production (e.g. Grace and
Tilly, 1976; Haag and Gorham, 1977; Barko and Smart, 1981). The large
effect of season was probably the synergistic result of changes in all of these
environmental factors. For example, in early autumn average light availability was 79% less and temperature was somewhat lower than that of late
summer {Table II), but the average early autumn weight was only 45% that of
late summer. It is notable that fragment t y p e influenced growth during
autumn, but n o t during late summer. During early autumn allofragment P
concentrations were higher than autofragment concentrations {Table III).
However, TNC levels were higher in autofragments {Fig. 4, although I found
no relationship between TNC c o n t e n t and growth). H o w sensitivity to variables
changed is open to question.
The presence of a large TNC pool is indicative of high plant plasticity
and resistance to adverse environmental conditions (Smith, 1969; Titus
and Adams, 1979). Kimbel and Carpenter (1981) found no relationship between autumnal TNC content and subsequent summer biomass production
but here a reduction in TNC c o n t e n t was linked to an increase in propagule
mortality {Fig. 7) and changes in growth response. However, high TNC-level
plants did n o t grow significantly better than low TNC-level plants. This may
have been due to a rapid recovery of TNC levels (Fig. 5).
Autofragment TNC levels were similar to shoot levels obtained by Titus
and Adams (1979), b u t allofragment TNC patterns differed between studies.
Since high TNC c o n t e n t increases survival, TNC allocation to reproductive
structures may be a tactic for enhancing overwintering survival. After biomass
breakup, many allofragments are formed. Allofragment (shoot) concentrations were high during 1974 and 1975 (Titus and Adams, 1979) preceding
years of high biomass production (Carpenter, 1980a), while concentrations
were low in 1978 (Fig. 4) preceding a year of low biomass production (Jones,
1980). Low TNC concentrations in 1978 may have resulted in increased allofragment overwintering mortality, reduced colonization and low 1979 biomass.
CONCLUSIONS
Few investigators have related aquatic plant propagule success to environmental variables. Propagules of M. spicatum are most successful during
August in shallow water on rich organic sediments. Also, propagule TNC
levels are high at this time meaning mortality is low. Propagules are least
successful during the early autumn period, b u t the response to other factors
is more complex. Generally, during September, in shallow water autofrag-
306
ments have highest mortality but grow faster there than at greater depths.
In deeper water mortality is reduced but so is growth. September TNC content is probably an important influence when carbohydrates are needed to
support basal metabolism for overwintering.
ACKNOWLEDGMENTS
This study was supported by National Science Foundation grants DEB-7519777 and DEB-78-10640 to the Institute for Environmental Studies, Center
for Biotic Systems, University of Wisconsin, Madison. The author thanks: J.
Eberhart, A. Gurevitch, P.S. Johnsen and D. Pay for field and laboratory
assistance; M.S. Adams, S. Aiken, R.C. Jones, R.T. Prentki, C.S. Smith and
especially S.R. Carpenter, who made helpful suggestions during the course of
this project, and M.S. Adams, R.C. Jones, S.R. Carpenter and C.D. Schlichting
who commented on an earlier version of this manuscript. The Madison Academic Computing Center and the University of Texas provided computing
support.
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