Aquatic Invasions (2014) Volume 9, Issue 2: 157–166
doi: http://dx.doi.org/10.3391/ai.2014.9.2.04
© 2014 The Author(s). Journal compilation © 2014 REABIC
Open Access
Research Article
Effect of water column phosphorus reduction on competitive outcome and traits
of Ludwigia grandiflora and L. peploides, invasive species in Europe
Joëlle Gérard 1 * , Natacha Brion 2 and Ludwig Triest 1
1
2
Plant Biology and Nature Management (APNA), Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels, Belgium
Analytical and Environmental Geochemistry (AMGC), Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels, Belgium
E-mail: [email protected] (JG), [email protected] (NB), [email protected] (LT)
*Corresponding author
Received: 14 December 2013 / Accepted: 24 April 2014 / Published online: 14 May 2014
Handling editor: Vadim Panov
Abstract
The invasion of alien macrophytes in aquatic ecosystems has caused serious ecological and economic impacts. Their introduction often leads
to competition with natives and already established invasive species. Competition among invasive species is assumed to be greater than
among native and invasive species, especially for plants with similar growth form and position in the water column. Many freshwater bodies
are eutrophicated due to high phosphorus inputs, which have led to a competitive advantage for invasive macrophytes. A decrease in water
column phosphorus load might lead to a change in competitive performance and reveal apparent variation in those traits promoting
invasiveness. We investigated the effect of a water column phosphorus reduction on the growth, competitive outcome, traits and nutrient
uptake of two related invasive Ludwigia species, L. grandiflora a n d L. peploides. We performed indoor competition experiments in
eutrophic and mesotrophic conditions following a complete additive design. L. grandiflora always was the better competitor in both trophic
conditions and had higher trait values compared to L. peploides. Both species relative growth rates (RGR) and trait values were affected by
a P reduction, especially the number of branches and stem length. Although both species prefer higher water column phosphorus loadings,
they can also colonize habitats of lower mesotrophic phosphorus concentrations. L. peploides was able to store more P in its tissue compared
to L. grandiflora, thereby possibly outcompeting L. grandiflora in even lower P concentrations. Our results show a water column P
reduction to lower branch numbers, stem length and biomass, which could reduce mat formation and allow for more effective control of both
species.
Key words: macrophyte, alien, eutrophication, growth, freshwater, competition, RGR
Introduction
The invasion of alien plant species has become a
worldwide problem and is considered a severe
threat to biodiversity (Mack et al. 2000). During
the last few decades, a high number of macrophyte
species, especially ornamental plants, have been
introduced due to increases in travel and trade
(Brunel 2009; Hulme 2009). The presence of
invasive alien species often leads to competition
with native species, usually resulting in a partial
or complete loss of the latter. Competition among
invasive species will be higher, particularly
between related species with similar growth form
residing in the same position in the water column
(Gopal and Goel 1993; Cahill et al. 2008). Invasive
plants are characterized by higher growth rates
(Fogarty and Facelli 1999; Burns 2004; Funk and
Vitousek 2007; Grotkopp and Rejmanek 2007)
and other traits which enhance their invasiveness
and show plasticity with resource availability
(Hastwell et al. 2008; Fan et al. 2013). Many
studies have investigated traits associated with
invasiveness, however a universally applicable
set of predictive traits is still elusive, especially
for aquatic plants (Daehler 2003; Mony et al.
2006; Richardson and Pysek 2006). Trait studies
focusing on competition between related invasive
species with the same growth form are more
suitable to reveal which species will be a better
competitor and which traits promote invasiveness
(Pysek and Richardson 2007; Feng and Fu 2008).
Impacts caused by invasive plants underline
the importance of understanding the factors that
influence a habitat’s invasibility (Chadwell and
Engelhardt 2008). Eutrophication of freshwater
ecosystems as a result of human activities has
facilitated such invasions and enhanced their
adverse effects (Dukes and Mooney 1999; Daehler
2003), and is currently viewed as the second
157
J. Gérard et al.
major threat to biodiversity (Van et al. 1999;
Daehler 2003). High water column nutrient loadings
favor invasives by leading to increased growth
and a change in competitive balance between
plant species (Smith et al. 1999). Several studies
have shown invasives to be able to take up more
nutrients at high nutrient levels, while natives
are likely to have adapted to low nutrient
conditions and show low growth (Fogarty and
Facelli 1999; Burns 2004; Funk and Vitousek 2007;
Grotkopp and Rejmanek 2007; Hastwell et al. 2008;
Fan et al. 2013). In freshwater ecosystems, P is
usually the main limiting element, and eutrophication is thus enhanced by P inputs (Schindler
1977; Sharpley et al. 2003). Several studies have
however shown N limitation to occur as frequent
as P limitation (Elser et al. 2007; Lewis and
Wurtsbaugh 2008). Nevertheless, even if N is
primarily limiting, controlling P levels will
generally be the most successful and low-cost
method for reducing algal populations (Lewis
and Wurtsbaugh 2008). Hence, a water column
phosphorus reduction might affect macrophyte
species’ P uptake, growth rate and change the
competitiveness of the invasive species, since
species might vary in their ability to cope with
low P (Koerselman and Meuleman 1996). A
reduction in nutrients may also affect the amount
of internally stored nutrient concentrations (Chapin
1991). Invasive species are often able to better
exploit high nutrients or compete by pre-empting
the supply of limited nutrients (Craine et al.
2005). Plants with high storage ability should
occur over a wide ecological range and are
consequently highly competitive (Garbey et al.
2004; Thiébaut 2005). We therefore hypothesize
that the better competitor will have the highest
tissue P concentration.
Ludwigia grandiflora ((Michaux) Greuter and
Burdet, 1987) and Ludwigia peploides ((Kunth)
P.H. Raven, 1963) are two related invasive
macrophyte species originating from North and
South America, and are now both present in
several European countries including Belgium
(Bauchau et al. 1984; Dandelot 2004; Hussner
2012). The distribution of the two species has been
intensely studied in France, where L. peploides has
extended more throughout the Mediterranean
area, while L. grandiflora has spread more to the
Eastern and Northern parts of France, however
the species are often found to co-occur (Ancrenaz
and Dutartre 2002; Dandelot et al. 2005b). In
Belgium and other European countries, the
distribution of L. peploides is still limited (EPPO
158
2011), but since the two species are able to exist
in a wide range of habitats (Haury et al. 2010;
Hussner 2010), they could ultimately co-occur in
invaded areas. The spread of the species could
also be underestimated since L. peploides and
L. grandiflora are two morphologically very similar
species that are difficult to distinguish and often
confused when not flowering (Dandelot et al. 2008).
Both Ludwigia species are able to spread
quickly due to their rapid growth and propagation by
fragments (Dandelot et al. 2005b; Verloove 2006).
They can laterally extend their shoots on top of
the water column, thereby producing dense mats,
which are known to reduce native biodiversity,
degrade water quality by reducing oxygen and
silt up ponds (Dutartre et al. 1997; Dandelot et al.
2005b; Dandelot et al. 2008; Stiers 2011). Both
species produce two types of roots: branched
downwards growing roots and spongy unbranched
upwards growing roots for aeration (Ellmore
1981). The species are very vigorous, since they
are able to grow in several sediment types and
can inhabit wet terrestrial habitats as well as
aquatic habitats (Matrat et al. 2006; Hussner 2010).
In this paper, we investigated the effect of a
water column phosphorus reduction on growth,
strategies and competition between two invasive
related species Ludwigia grandiflora and
Ludwigia peploides with similar growth form
and position in the water column. Both species
were grown in monocultures and mixtures in
water column P concentrations concurring with
eutrophic and mesotrophic conditions. Our goals
are to determine (1) the effects of a water column
phosphorus reduction on growth; (2) the better
competitor in eutrophic and mesotrophic conditions
and hence the effect of a phosphorus reduction
on competitive outcome; (3) whether the better
competitor exhibits different traits related to
nutrient acquisition and invasiveness; (4) whether
traits show trait plasticity with decreasing P; and
(5) whether the competitive strength of the
species is related to the amount of phosphorus
acquired.
Materials and methods
Plant material
We studied two invasive species: Ludwigia grandiflora (Michaux) Greuter and Burdet and Ludwigia
peploides (Kunth) P.H. Raven. L. grandiflora was
collected from De Spicht – Goorbroek in Belgium.
L. peploides was obtained from the Plant
Effect of phosphorus reduction on competition and traits
Protection Service of the Netherlands (collected
from former polder Alblas, the Netherlands).
Experimental design
All plants were cut into 10±1 cm long apices and
placed into 100 L containers filled with rain
water, to allow for root growth. After 3 weeks,
all plants (average height 15.0 cm) had grown
roots and were planted in monocultures and
mixtures in 1L pots (height 10 cm) following a
complete additive design (Spitters 1983).
L. grandiflora : L. peploides planting densities
were 0:2, 2:0, 2:2, 2:4, 4:2, 4:4, 4:0, 0:4, each
combination replicated 5 times. Although we do
not have any data on field densities, the same
initial densities were used in Ludwigia competition
experiments performed by Njambuya and Triest
(2010) and Thouvenot et al. (2013). Pots were
filled with sand and KNO 3 mixture (1g KNO 3/l
sand) and covered with 3 cm of clay to reduce N
flow to the water column. Pots were then placed
into 12 l buckets (height 24,5 cm) filled with 10 l
solution, such that the plants were submerged
only a few centimeters below the water surface
and were able to emerge during the first week.
We used a 3x diluted Nitrogen lacking Hoagland
and Arnon (1950) solution. P concentrations
were adjusted to 30 (mesotrophic) and 100 µg/l
(eutrophic condition) with KH2PO4. All buckets
were placed randomly in a greenhouse under
12:12 hr day: night cycle with Photosynthetically
Active Radiation (PAR) ranging from 105 to 197
µmol m-2 s-1. All solutions were replenished and
thoroughly mixed once a week. At the end of the
experiment, various biological traits were measured
including stem length, number of leaves, number
of shoots, and length and width of the leaves
(leaf at 3 cm from the plant apex). The average
pH (average eutrophic 7.50, mesotrophic 7.44),
water temperature (23.8°C) and air temperature
(29.4°C) were recorded. After 8 weeks, all plants
were harvested and separated into roots and
shoots. All biomass was dried for 72 hours at
70°C and weighed. We calculated the root/shoot
ratio as root weight (g)/shoot weight (g).
Particulate organic nitrogen (PON) and carbon
(POC) concentrations in plant tissue were analyzed
simultaneously with a Flash EA 1112 (Thermo)
elemental analyzer (Nieuwenhuize et al. 1994). The
analysis combines conversion of PON and POC
into N 2 and CO 2, separation on a chromatographic
solid phase column and detection by thermal
conductivity (Pella 1990). Concentrations of PON
and POC were obtained by standardization with
acetanilide. Total phosphorus in plants was analyzed
using a modified digestion protocol (Johengen
1996) after which digestions were analyzed with
a segmented flow auto-analyzer QuAAtro (SEAL
Analytical).
Statistical analysis
The relative growth rate (RGR) of each species
was calculated according to the formula: RGR
ln Y/y /t , where y is the species’ initial
aboveground biomass or length and Y the species’
aboveground biomass or length at the end of the
experimental period t. We determined the relative
competitive strength as formulated by olde
Venterink and Güsewell (2010): in each treatment,
we calculated the ratio of a species’ biomass in a
mixed pot by the biomass in a monoculture pot.
Monoculture and mixture pots were randomly
coupled. The superior competitor was the species
which produced significantly more biomass in
mixture than in monoculture (competitive response
> 1) and/or caused the other species to produce
significantly less biomass in mixture than in
monoculture (CR<1) (olde Venterink and Güsewell
2010). By calculating the L. grandiflora / L.
peploides biomass ratio, we examined the relative
dominance of the two species in competition (olde
Venterink and Güsewell 2010). We analyzed the
differences in biomass, weight RGR and length
RGR between separate initial planting densities
using non-parametric Mann-Whitney U-tests for
monocultures and Kruskall-Wallis tests for mixtures
due to the non-normal distribution of the data.
For all the parameters, there was no significant
difference between the initial planting densities
in monocultures or in mixtures and therefore the
different densities of monocultures and mixtures
were pooled. The differences in RGR between
species and between nutrient levels were analyzed
with parametric t-tests. Differences in other
traits, biomass, competitive response, biomass
ratio and tissue nutrient concentrations did not
pass the assumptions of normality or equal
variances and were therefore analyzed with nonparametric Mann-Whitney U-tests.
Results
Species biomass and competitive strength
We found L. grandiflora to produce more biomass
than L. peploides at the end of each trophic
experiment, both in monocultures and in mixtures
(Eutrophic: monoculture p<0.001, mixed culture
p<0.0001; Mesotrophic: monoculture p<0.05, mixed
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J. Gérard et al.
Figure 1. Effect of phosphorus reduction
on L. grandiflora and L. peploides total
biomass production in monocultures
(grey boxes) and mixtures (white boxes).
□ represents the median, the box the
interquartile range and the vertical lines the
minimum and the maximum non-outlier
values. Outliers are represented by ○.
Significant differences are indicated
as ** p < 0.01, * p < 0.05.
culture p<0.0001). For both nutrient levels, the
biomass of L. grandiflora remained similar in
monocultures and in mixtures. The biomass of
L. peploides however was reduced in mixed
cultures compared to monocultures in both trophic
conditions, indicating that L. grandiflora was the
superior competitor in the tested conditions (Figure
1). The relative competitive strength of both
species and biomass ratio of L. grandiflora /
L. peploides in mixtures was not affected by a
phosphorus reduction, confirming the superiority
of L. grandiflora under the conditions of this study.
Strategy
Relative growth rate
In both trophic conditions, Ludwigia grandiflora
generally had a higher biomass relative growth
rate (RGR) than L. peploides, in monocultures
and in mixtures (Figure 2A). The length RGR was
higher for L. grandiflora in monocultures and
mixtures in eutrophic condition, but in mesotrophic
condition both species performed similarly (Figure
2B). When compared between monocultures and
mixtures in eutrophic condition, both species’
weight RGR was higher in monocultures than in
mixtures. In mesotrophic condition however, the
two species performed similarly in monocultures
and mixtures. A comparison of the length RGR
indicated that both species performed similar in
mixtures and monocultures for both trophic
conditions. Growing in nutrient reduced conditions
had a negative effect on both species length and
weight RGR, except for L. grandiflora weight
RGR in mixtures.
160
Plant traits
Six plant traits were measured during the
experiment (Table 1). When compared between
species, we found that in both trophic conditions,
values of traits of L. grandiflora were almost
always higher than the ones of L. peploides.
L. grandiflora produced longer stems (Eutrophic
U= 790.5, p<0.0001; Mesotrophic: U= 732.0,
p<0.001) and more leaves per stem (Eutrophic
U= 443.5, p<0.0001; Mesotrophic U= 486.5,
p<0.0001). The average number of branches
produced was higher for L. grandiflora in eutrophic
conditions, however in mesotrophic conditions
both species produced similar amounts (Eutrophic
U=1119.5, p<0.01; Mesotrophic U=1339.5, p>0.05).
Leaf length was the highest for L. grandiflora, in
both nutrient conditions (Eutrophic U= 200.0,
p<0.0001; Mesotrophic U= 188.0, p< 0.0001).
The same results were found for leaf width
(Eutrophic: U= 481.0, p<0.0001; Mesotrophic
U= 655.0, p<0.001). The root/shoot ratio was
higher for L. grandiflora in both nutrient conditions
(Eutrophic U=385.5, p<0.0001; Mesotrophic
U=1500.0, p<0.0001).
Growing the plants in nutrient reduced conditions
(mesotrophic) had a significant negative impact,
compared to eutrophic conditions, on almost all
plant traits (Table 1). Both species’ stem length
and number of branches were reduced, however
the number of leaves per stem increased. Leaves
in eutrophic condition were longer for both species
and wider for L. grandiflora. The root/shoot ratio
was also higher for both species in eutrophic
compared to mesotrophic condition.
Effect of phosphorus reduction on competition and traits
Effect of a heterospecific neighbor
L. peploides always showed similar tissue P% in
monocultures and mixtures. L. grandiflora had
higher tissue concentrations in mixtures in eutrophic
condition (p<0.01) but not in mesotrophic condition.
Both species showed similar N% and C% in monocultures and mixtures in both nutrient conditions,
except for L. peploides C%, which was higher in
mesotrophic monocultures versus mixtures (p<0.05).
Effect of a phosphorus reduction
The overall tissue P% was similar for L. peploides
in both trophic conditions, in mixtures and in
monocultures. L. grandiflora however showed a
decrease in tissue concentration with decreasing
nutrient level (mono p<0.01, mix p<0.0001). In
both species the tissue N% was significantly lower
when phosphorus concentration was reduced from
eutrophic to mesotrophic condition, except for
L. peploides mixtures (L. grandiflora mono p<0.05,
mix p<0.001; L. peploides mono p<0.05). L.
peploides tissue C% was similar in eutrophic and
mesotrophic condition, while L. grandiflora
acquired more C in mixtures (p<0.01), but not in
monocultures.
Figure 2. Above-ground weight and length RGR (mean ± SE) of
L. peploides and L. grandiflora in monocultures (grey bars) and
mixtures (white bars) in eutrophic and mesotrophic condition. The
letters a and b represent differences between trophic conditions
for L. peploides or L. grandiflora in monocultures or mixtures, X
and Y represent differences between monocultures and mixtures
for the same species grown at similar phosphorus concentration, +
and * represent differences between L. peploides and L.
grandiflora in respectively monocultures and mixtures at similar
phosphorus concentration.
Tissue nutrient content
Difference between species
The two species always showed similar tissue
P% in monocultures (Figure 3A) in both eutrophic
and mesotrophic condition. In mixtures however,
P% was significantly different. An important
observation was that L. grandiflora had higher
concentrations than L. peploides in eutrophic
condition, while the reverse was true in mesotrophic
condition. The N% was significantly higher for
L. grandiflora than L. peploides in eutrophic
conditions (Figure 3B). In mesotrophic conditions
however, both species acquired similar amounts
of N. The overall tissue C% was always similar
for both species except in mesotrophic conditions,
which was significantly higher for L. grandiflora
mixtures (Figure 3C).
Discussion
Ludwigia grandiflora and L. peploides were both
affected by a phosphorus reduction and showed a
reduction in relative growth rates based on both
biomass and length. The average RGRs found in
this study are quite low compared to ranges in
literature (approximately 0.03–0.06 g g -1 day-1)
(Rejmankova 1992; Hussner 2009; Hussner 2010).
Our results concur with Lowe et al. (2003), stating
that not all invasives show high growth in high
nutrient levels. Our results are related to field
conditions since several ponds and lakes in Belgium
show P concentrations concurring with eutrophic
condition (Teissier et al. 2011; Van Onsem et al.
2012). However the overall average phosphorus
concentration in Belgian surface waters is higher,
being 0.39 mg P/L (VMM 2013). The observed
lower growth rates could therefore be explained
by the relatively ‘low’ phosphorus concentrations
applied in this study compared to these average
field concentrations. Both Ludwigia species have
also been shown to grow well on substrate with
high nutrient availabilities and show reduced growth
on nutrient limited soil (Hussner 2009). Hence the
lack of P in our incubation soil will probably
have resulted in the observed lower growth.
161
J. Gérard et al.
Figure 3. Tissue P, N and C concentration (mg/g dry weight) of
L. peploides (white boxes) and L. grandiflora (black boxes) in
monocultures and mixtures in eutrophic and mesotrophic
condition. □ represents the median, the box the interquartile range
and the vertical lines the minimum and the maximum non-outlier
values. Outliers are represented by ○, extremes by x. Significant
differences between species are indicated as *** p < 0.001, ** p <
0.01, * p < 0.05, ns non significant.
162
The search for traits associated with invasiveness
is crucial since a common set of traits is elusive,
particularly for aquatic plants (Daehler 2003;
Mony et al. 2006; Richardson and Pysek 2006).
Although this approach is mainly used for
explaining differences between natives and
invasives, we believe it is also valid for explaining
different degrees of alien species’ invasiveness. Ludwigia grandiflora and Ludwigia peploides are
two very similar species which are hard to
distinguish in the absence of flowers (Dandelot et
al. 2005b). Even though being almost identical
species, we showed that once placed in
competition, both species performed differently.
Under the conditions of this study, L. grandiflora
was the overall better competitor, in high
phosphorus concentration as well as in lower
concentration. Several studies have investigated
traits in native and invasive species and found
invaders to have higher growth rates, leaf area,
leaf mass ratio, nutrient uptake rates and other
traits (Barrat-Segretain et al. 2002; Feng et al. 2007;
van Kleunen et al. 2010; Matzek 2012). Our results
support that Ludwigia species possess several of
these traits which might explain their excessive
spread in such a large range of countries
(Aboucaya 1999; Cronk and Fuller 1995). When
compared between species, L. grandiflora exhibited
higher values of traits compared to L. peploides. L. grandiflora stems were longer, and produced
more branches and leaves. Leaves were also larger,
thereby having a larger photosynthetic surface.
To predict future invasions and to control invasive
species that are already present, it is important to
study trait responses under changing conditions
(Drenovsky et al. 2012) such as nutrient loading
to surface water, since it is of great relevance to
water quality standards (Wersal and Madsen 2011).
We found that reduced phosphorus inputs in the
water column affected not only species RGR but
also other traits. Especially the smaller number
of branches and stem length was highly reduced.
This was also observed by Mony et al. (2006),
who found Ranunculus peltatus traits to depend
on P-availability.
When growing in high P, L. grandiflora had
higher tissue P in mixture than in monoculture,
even though biomass remained similar, indicating
that L. grandiflora had an enhanced phosphorus
accumulation capacity in the presence of L. peploides. Additionally, L. grandiflora had
higher P% than L. peploides in eutrophic conditions,
probably by having superior competitive ability for
nutrient uptake (Aerts et al. 1999). L. peploides
Effect of phosphorus reduction on competition and traits
Table 1. Effect of a water column phosphorus reduction on L. grandiflora and L. peploides traits. Species are indicated by G= L. grandiflora
and P= L. peploides .Values given are average values. Significant differences between nutrient levels are shown as **** p < 0.0001, *** p <
0.001, ** p < 0.01, * p < 0.05, ns non significant.
Trait
Final length (cm)
Number of branches
Number of leaves
Leaf length (cm)
Leaf width (cm)
Biomass (g)
Root:shoot ratio
Species
Eutrophic condition
Mesotrophic condition
p
U
G
P
G
P
G
P
G
P
G
P
G
P
G
P
39.87
29.48
6.12
3.19
19.29
14.07
2.92
1.52
1.97
1.28
0.32
0.12
0.25
0.08
28.23
24.24
2.68
2.13
21.50
16.09
2.28
1.24
1.46
1.07
0.25
0.08
0.14
0.07
****
****
***
**
*
*
****
**
****
ns
ns
**
**
*
790.5
732.0
1030.5
1114.5
1135.5
899.0
746.0
735.0
799.5
685.5
3340.5
2575.0
2660.5
2480.5
on the other hand always had similar P accumulation
in monocultures and mixtures, whatever the P
levels, even though biomass was always reduced due
to the presence of L. grandiflora. In mesotrophic
conditions, L. peploides even had higher internal
P compared to L. grandiflora in mixtures.
Plants with the ability of high nutrient storage
are highly competitive (Garbey et al. 2004; Thiébaut
2005). Internal nutrient concentrations can be used
to compare aggressiveness and competitiveness
in nutrient uptake at different nutrient concentrations, and are even recommended over nutrient
uptake studies for evaluating nutrient competitiveness (Gerloff 1975). P thresholds have to be
accounted for (Demars and Edwards 2007), since
they indicate interesting variations in the nutritional
requirements of organisms, even within species
belonging to the same taxonomic group (Gerloff
1975). For aquatic species, estimated critical P
nutrient concentrations in tissues having 95% of
the maximum yield (= final standing biomass)
and 95% of the maximum growth are 0.10 (±0.03
SD) % DW and 0.16 (±0.05 SD) % DW,
respectively (Gerloff 1975; Demars and Edwards
2007). Our results showed both species to always
contain P levels above the maximum biomass
threshold. However, in mesotrophic condition 50%
of the L. grandiflora internal P concentration
was lower than the maximum growth threshold,
indicating that P could have been growth-limiting.
However this value needs to be interpreted with
care since P thresholds are species-specific
(Gerloff 1975). Demars and Edwards (2007) also
found external nutrient availability for aquatic
vascular plants to influence tissue nutrient
concentrations. Additionally, a low P availability
has often been found to reduce tissue P
concentrations of other aquatic plants (Xu et al. 2006; Rejmankova and Snyder 2008; Zhang and
Liu 2011).
L. grandiflora was probably able to take up more
nutrients than L. peploides due to the production of
more and longer roots. Both species produced
branched downwards growing roots and unbranched
spongy upwards growing roots. An important
observation in our study was that in both trophic
conditions, L. peploides showed red leaves and
reddish downward growing roots not embedded
in the soil. The coloration of the roots is often
found in both Ludwigia species (Ellmore 1981;
Hussner 2010; van Valkenburg pers. comm.).
This could be caused by an accumulation of
anthocyanin, a pigment with a wide range of
functions associated to UV absorption and nutrient
stress (Stewart et al. 2001; Kliebenstein 2004).
Anthocyanin is known to accumulate in plants
when P is limiting (Jiang et al. 2007). Anthocyanin
can also accumulate to protect the plant from
high-light damage by absorbing light (ChalkerScott 1999). Since roots were only colored
above-ground and individuals in field conditions
growing out of the water have also shown pink
roots (van Valkenburg pers. comm.), this
explanation seems more appropriate. Additionally,
Ellmore (1981) found the nodes of L. peploides
plants to show red pigmentation on the dorsal
sides illuminated by the sun, while the shaded
ventral sides remained green.
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J. Gérard et al.
Both species also produced spongy white
upwards growing roots, known as pneumatophores,
which improve gas exchange during anoxic
conditions, occurring mostly in summer (Ellmore
1981; Dandelot et al. 2005a). These roots were
frequently observed for L. grandiflora, but not
often for L. peploides. Both species have also
been found to release allelopathic chemicals in
the environment (Dandelot et al. 2008), which
may have played a role in the competitive
outcome. Other studies also mention complex
interactions with bacteria that produce toxic
compounds (Ahmed et al. 2005; Dandelot et al.
2005a; Dandelot et al. 2008). However this toxicity
due to the proliferation of bacteria, has been found
to be higher in L. grandiflora compared to L.
peploides stands (Dandelot et al. 2005a).
Acknowledgements
We would like to thank D. Maes, J. Appah and J. van Valkenburg
for supplying L. peploides. We are grateful to the anonymous
reviewers for their comments on the manuscript. This PhD
research is funded by a scholarship provided by the government
agency for Innovation by Science and Technology and by the
Vrije Universiteit Brussel (BAS42).
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