acta oecologica 31 (2007) 69–78
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/actoec
Original article
Interspecific competition between alien and native
congeneric species
H. Garcia-Serranoa, F.X. Sansa,*, J. Escarréb
a
Departament de Biologia Vegetal (Unitat de Botànica), Facultat de Biologia, Universitat de Barcelona. Av. Diagonal 645,
08028 Barcelona, Catalunya, Spain
b
Centre d’Écologie Fonctionelle et Evolutive (CEFE) du Centre National de la Recherche Scientifique (CNRS), 1919 Route de Mende,
34293 Montpellier Cedex 05. France
article info
abstract
Article history:
A good way to check hypotheses explaining the invasion of ecosystems by exotic plants is
Received 26 April 2006
to compare alien and native congeneric species. To test the hypothesis that invasive alien
Accepted 26 September 2006
plants are more competitive than natives, we designed a replacement series experiment to
Published online 12 January 2007
evaluate interspecific competition between three Senecio species representing the same bushy life form: two alien species (S. inaequidens and S. pterophorus, both from South Africa)
Keywords:
and a native species from the south-east of the Iberian Peninsula and Maghreb (S. malaci-
Invasion
tanus). While S. inaequidens is widespread throughout western Europe and is expanding to-
Alien
wards the south of Spanish–French border, the geographical distribution of the recently
Native
introduced S. pterophorus is still limited to north-eastern Spain. Plants from each species
Competition
were grown in pure and in mixed cultures with one of their congeners, and water availabil-
Replacement series
ity was manipulated to evaluate the effects of water stress on competitive abilities. Our re-
Senecio
sults show that the alien S. inaequidens is the most competitive species for all water
conditions. The native S. malacitanus is more competitive that the alien S. pterophorus in water stress conditions, but this situation is reversed when water availability is not limiting.
ª 2006 Elsevier Masson SAS. All rights reserved.
1.
Introduction
The publication of ‘‘The Ecology of Invasions by Animals and
Plants’’ (Elton, 1958) led to an increased interest among researchers in the phenomenon of biological invasion, which
is defined as the introduction, naturalisation and expansion
of a species in an area where it had previously been absent
(Mack et al., 2000; Richardson et al., 2000). Whereas exchanges
of species between different biogeographical regions is
a natural phenomenon at geological timescales, present rates
of biological invasion are clearly a result of human intervention (Rejmánek, 1996) and represent both a real threat to biodiversity and an important agent of global change (Vitousek
et al., 1996; Chapin et al., 2000; Mack et al., 2000).
Recent research to evaluate the main factors affecting degree of invasion has focused largely on biological attributes
of invading species (invasiveness) (e.g. Noble, 1989; Lodge,
1993; Kolar and Lodge, 2001; Sakai et al., 2001) and on the
* Corresponding author. Fax: þ34 93 411 2842.
E-mail address: [email protected] (F.X. Sans).
1146-609X/$ – see front matter ª 2006 Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.actao.2006.09.005
70
acta oecologica 31 (2007) 69–78
characteristics of invaded habitats (invasibility) (e.g. Levine
and D’Antonio, 1999; Lonsdale, 1999; Davis et al., 2000;
Prieur-Richard and Lavorel, 2000).
Most studies that endeavour to answer the question of
‘‘what attributes make some species more invasive than
others?’’ are based on the classification of long lists of species
for a geographical area as invaders or non-invaders, in an attempt to correlate species attributes with invasive ability
(Baker, 1965; Mooney and Drake, 1986; Drake et al., 1989; Noble, 1989; Di Castri et al., 1990; Williamson and Fitter, 1996).
Such lists have been demonstrated to be poorly predictive
(Crawley, 1987; Mack, 1996); nonetheless, they have allowed
researchers to formulate hypotheses as the basis for experiments that have improved our knowledge of the life history
attributes of invasive species. One such hypothesis is that invading plants are better competitors than natives (Baker, 1965;
Noble, 1989; Bakker and Wilson, 2001; Vilà and Weiner, 2004),
and differences in competitive abilities between invaders and
non-invaders may explain the maintenance of existing plant
populations of invaders outside their native range (Daehler,
2003).
The relative competitive performance of native versus invasive species often depends on environmental conditions
(Daehler, 2003). Thus resources and the fluctuations in their
availability can also play an important role in the invasion
process (Davis et al., 2000; Davis and Pelsor, 2001). In Mediterranean type climates, summer drought can be severe, thus
posing important restrictions to the invasion by alien species
that may be not well adapted to water deficit. Environmental
stress, including abiotic (resources, disturbance, etc) and
biotic stresses (competition, predation, etc) has been demonstrated to be an important factor preventing successful invasions (Alpert et al., 2000).
Most studies testing the general hypothesis that invasive
plants outcompete natives have compared the life history
characteristics of native and exotic species from different genera and families (Goergen and Daehler, 2001; Katz et al., 2001;
Blicker et al., 2002; Goergen and Daehler, 2002; Morris et al.,
2002; Booth et al., 2003; Daehler, 2003; Gerlach and Rice,
2003). Nevertheless, such comparisons do not take into account phylogenetic background, which may restrict species
variability in terms of morphological or physiological traits.
For this reason, it may be more meaningful to compare life
history traits for phylogenetically-related invasive and native
taxa with similar habitats so as to locate differences in their
attributes (Mack, 1996; Radford and Cousens, 2000). Indeed,
several studies within genera have yielded clearer results
than those that involve entire floras (Perrins et al., 1993;
Rejmánek and Richardson, 1996; Thébaud et al., 1996; Radford
and Cousens, 2000; Grotkopp et al., 2002; Gerlach and Rice,
2003). As indicated in the review made by Vilà and Weiner
(2004) to generalise that aliens are superior competitors than
natives, one should pair alien and native species with the
same life form because some studies have demonstrated
that species with distinct life forms respond very differently
to competition (Gerry and Wilson, 1995).
In this study we compare the competitive abilities of three
related species from the Senecio genus. S. inaequidens D.C. and
S. pterophorus D.C. are both alien species from South Africa
that have been accidentally introduced in Europe, and
S. malacitanus Huter is native to the south-eastern part of the
Iberian Peninsula. Given that these species belong to the
same genus and have the same life form it is assumed that
they will share similarities in resource capture, and therefore
in our study, each species was placed in direct competition
with its congeners. It has been hypothesised that competition
between alien and native species of the same genus might be
stronger than between less closely related species; this could
explain the fact that most invasive species are from alien genera (Darwin, 1859; Elton, 1958; Rejmánek, 1996), although this
does not hold for all floras analysed (Daehler, 2001; Strauss
et al., 2006). This hypothesis, however, has only been tested
in studies of flora, and not experimentally placing alien and
native congeners in direct competition with each other.
As invasiveness has been correlated with ecological range
(Lodge, 1993; Rejmánek and Richardson, 1996), we also tested
the hypothesis that, of the three species studied, the widespread alien S. inaequidens would be the best competitor,
followed by the more geographically restricted alien
S. pterophorus and finally, by the native S. malacitanus as the
least competitive of the three.
A replacement series experiment was designed to answer
the following questions: (1) Are the two invaders more competitive than their native congener? (2) What role does water
stress (a key factor in Mediterranean climates) play in competition between the alien and native congeners? These questions will elucidate some of the causes of their current
distribution and their dominance in case of future coexistence.
2.
Material and methods
2.1.
Species studied
Senecio inaequidens D.C. and Senecio pterophorus D.C. are two perennial plants of South-African origin. The former was introduced accidentally with wool imports to Europe at the end of
the nineteenth century (Ernst, 1998), and today is widespread
throughout western Europe. In Spain, individuals of S. inaequidens of French origin are invading the eastern Spanish–French
border, where they form dense populations in old fields and
road margins. This species also colonises heavily grazed grasslands. The distribution range of S. inaequidens is expanding towards the south and in some localities it is found together with
S. pterophorus, the other invasive species included in this study.
S. pterophorus was recently introduced in north-eastern Spain
and its geographical distribution is still reduced. It was first
recorded in 1982 near Cambrils (Tarragona), 120 km south of
Barcelona (Casasayas, 1989; Chamorro et al., 2006) and in
1995 near Barcelona (Pino et al., 2000). Despite the short time
since its introduction, it colonises the riverbeds of the Catalonia country (Spain), where it forms very dense populations.
These two Senecio species can be classified as novel, invasive
colonisers according to Davis and Thompson (2000), although
the distribution area of S. inaequidens is far greater than that
of S. pterophorus. Senecio malacitanus Huter (S. linifolius auct.)
is a perennial plant native to southern Europe, a successional
coloniser (sensu Davis and Thompson, 2000), which forms
acta oecologica 31 (2007) 69–78
very sparse populations in disturbed temporal rivers
(‘‘rambles’’) and other disturbed sites nearby. Its geographical
distribution is limited to the south-eastern Iberian Peninsula
and the Maghreb, in semi-arid climate (under 350 mm/year;
INM, 2004).
The three species were chosen due to the following reasons: they are from the same genus, they are ecologically similar, they are perennials and they have the same growth form
(dwarf shrubs). Moreover, S. malacitanus can be easily confounded with S. inaequidens such that the first authors that
found S. inaequidens in Europe identified it as S. malacitanus.
In addition, if S. inaequidens and S. pterophorus continue their
progression towards the south of Spain, they may cross the
range of S. malacitanus and eventually threaten the populations of this species because the species colonise similar habitats. It would have been interesting to use at least another
native species in the study, but we found no other species
with appropriate characters.
2.2.
Design of the experiment
Our replacement series experiment was carried out in the experimental fields of the Centre d’Écologie Fonctionelle et Evolutive (CEFE-CNRS) at Montpellier, France. To avoid the
expansion of both exotic species, which are not yet very widespread in Spain and France, the experiences were made in
controlled conditions and only during the vegetative period.
The experiment was stopped when several plants entered
the flowering period.
Seeds were planted at the end of March 2002 directly in
pots measuring 20 20 cm on the surface and 27 cm in depth,
filled with a mixture of commercial compost and sterilised
calcareous soil from the CEFE-CNRS fields. Each species was
grown in pure culture and in combination with one of the
other two species, thus, Senecio malacitanus (SM):Senecio inaequidens (SI), SM:Senecio pterophorus (SP) and SI:SP. For the
SM:SI pair five proportions were studied: 0:1, 1:2, 1:1, 2:1 and
1:0. For the other combinations, only the combination 1:1
and the pure cultures (0:1 and 1:0) were studied, as not
enough seedlings were obtained at the beginning of the experiment due to the high rate of non-viable seeds for S. pterophorus. To avoid the replacement series experiment problem
of initial size bias (Connolly et al., 2001), care was taken that
all seedlings were of similar size. Therefore, non germinated
seeds were replaced by a seedling of a similar size as the
others present in the pot. Additional pots were sown for this
purpose. Total density was 1225 plants/m2, or 48 plants per
pot, regardless of the proportion of seedlings per species,
but to avoid any border effect only the 24 individuals from
the middle were analysed. Results from replacement series
can be density-dependent (Cousens and O’Neil, 1993; Sackville Hamilton, 1994), although the competitive hierarchy of
two species can usually be maintained when density of the
mixture is sufficiently high (Taylor and Aarssen, 1989). For
this reason, the density used for our experiment was the
highest seedling density found for populations of S. inaequidens in Catalonia (Afán, 2000).
Thus, we obtained eight cultures (3 species in pure cultures, 3 proportions of SM:SI, and 1 culture each of SM:SP
and SP:SI). Each culture was replicated in eight pots, four of
71
which were randomly assigned to water stress treatment,
and the remaining four assigned to the control treatment
(unlimited water availability). Seedlings remained 2 months
in a heated greenhouse, after which the pots were placed
outdoors and the plants were acclimatised for 10 days prior
to commencing the period of stress treatment to simulate
the growing conditions at the beginning of the summer in
Mediterranean region. Stress treatment started on the 4th of
June 2002, and all plants were harvested, dried and weighed
on the 1st of July. At the moment of the harvest most of the
plants of S. inaequidens were in the initial phases of flowering
and individuals of S. pterophorus were in bolting stage. Because
of the difficulty of isolating the roots of individual plants in
each pot, only aboveground dry mass was analysed.
Throughout the experiment, a water sensor triggered an
electric motor to automatically position a light glasshousetype roof over the plants when rain fell and remove it after
some minutes without rain. Ten randomly selected pots per
treatment were weighed daily in order to establish the mean
water status for each treatment. Control pots were watered
daily to field capacity, to a soil weight/soil dry weight ratio
of 1.58–1.77. Water-stress pots were maintained at a 1.19–
1.29 soil weight/soil dry weight ratio; some plants undergoing
this treatment wilted daily prior to watering. The stress level
was determined by a preliminary experiment with irrigated
and non-irrigated Helianthus annuus plants to establish the
relationship between pre-dawn water potential and pot water
content, since Helianthus annuus shows good equilibrium with
soil water potential in the root zone. Pre-dawn water potential
was measured for each pot using the mean of three leaves
(one per plant) and correlated to the pot soil weight (corrected
for plant weight). Measured potential (in MPa) was plotted
against the ratio of soil weight/dry soil weight, and the
resulting curve was used to monitor drought stress and to
define the stress level (more details are available in Cheptou
et al., 2000).
It is considered preferable to assess competition
experiments not only in terms of biomass (or growth) but
also in terms of other Darwinian fitness parameters, such as
survival and reproduction (Aarssen and Keogh, 2002). For the
purposes of our experiment, growth and survival were analysed. However, it was not possible to analyse reproduction
as the experiment had to be ended when the S. pterophorus
plants started showing capitula, in order to avoid the invasion
of this species in the Montpellier area (where it is not currently
present). Although a complete picture of interspecific
competition between these dwarf shrubs has not been
possible for ethical reasons, competition at the seedling stage
is ecologically relevant because small differences in height are
determinant for the access to the light and therefore to
survival of the individuals. Indeed, after Grime (1979) the
most important effects of dominance are found during the
seedling stage.
2.3.
Data analysis and interpretation
2.3.1.
Survival and growth
Survival was calculated as the proportion of individuals surviving to the end of the experiment divided by the initial
72
acta oecologica 31 (2007) 69–78
number of individuals per pot. Individual biomass was calculated as the total aboveground biomass per pot divided by the
number of individuals surviving to the end of the experiment.
Individual aboveground biomass data, after being log-transformed to comply with assumptions of normality and homoscedasticity of residuals, was analysed using ANOVA (Sokal
and Rohlf, 1981). Given that survival is a binomial response,
this was analysed using a generalised linear model with a logit
link, specifying binomial errors (SAS, 1999).
Two separate analyses were performed, the first one to test
the effect of culture and water stress in each species pair (replacement series) and the second one to test the effect of water stress between the three species in pure cultures. For the
first analysis, three factors were considered: (1) ‘water treatment’ at two levels (stressed or well-watered); (2) ‘culture’ at
four levels (puredproportion 1:0dor mixeddproportions 2:1,
1:1 and 1:2) or at two levels for the mixed cultures with S. pterophorus (1:0 and 1:1); and (3) ‘species’ at two levels. For the second analysis, a complete two factorial design with only data
from the pure cultures was used, with factor ‘species’ at three
levels and factor ‘water treatment’ at two levels. Means were
compared using least-squares means tests (SAS, 1999).
in a mixed culture; i.e. i experiences more competition from
individuals of species j than from individuals of its own species i, implying that i is an inferior competitor to j (Snyder
et al., 1994).
RYT is the weighted sum of Relative Yields for the mixed
culture components. An RYT of 1.00 means that both species
are competing for the same resources, and one is potentially
capable of excluding the other; an RYT of greater than 1.00
means that the two species exploit different resources and
therefore do not compete (e.g. due to different root depths); finally, an RYT of less than 1.00 implies that the two species are
mutually antagonistic, with both having a detrimental effect
on the other (Harper, 1977; Fowler, 1982).
RY and RYT from each mixed culture were compared to the
value of 1.00 using t-tests (P ¼ 0.05), for both water stress and
control conditions.
2.3.2.
RSIi ¼
Competitive interactions
Relative Yield per plant (RY) and Relative Yield Total (RYT)
were calculated from final aboveground biomass (dry weight)
for each species in each pot, following Fowler (1982). These
measures provide information on competitive interaction between species in a mixed culture by the comparison of growth
in mixed and pure cultures.
Relative Yield per plant of species i in a mixed culture with
species j was calculated as:
RYij ¼
Yij
ðp$YiÞ
and for species j in a mixed culture with species i as:
RYji ¼
Yji
ðq$YjÞ
Finally, Relative Yield Total was calculated as:
RYT ¼ p$RYij þ q$RYji
where Yij is the yield for species i growing with j (g/individual),
Yji is the yield for species j growing with i, Yi is the yield for
species i growing in pure culture (g/individual), Yj is the yield
for species j growing in pure culture, p is the initial proportion
of species i in the mixed culture and q the initial proportion of
species j in the mixed culture, with ( p þ q) ¼ 1.
RY measures the average performance of individuals in
mixed cultures compared to that of individuals in pure cultures. A RYij of 1.00 indicates that species i performs as well
in a mixed culture with species j as it does in a pure culture,
thereby indicating that species i and j are both equal in terms
of competitive ability (i.e. species i is as good competing with
itself as with j). A RYij greater than 1.00 means that species i
performs better in mixed rather than pure cultures; i.e. species i experiences more competition from individuals of the
same species than from individuals of species j, and therefore,
i is a superior competitor to j. Finally, a RYij of less than 1.00
means that species i performs better in a pure culture than
2.3.3.
Water stress
In order to compare the effects of water stress on the growth
of the target species, a Relative Stress Index (RSI) was also calculated for each pure culture. RSI for species i was calculated
as:
ðYic YisÞ
Yic
where Yic is the yield for species i growing in a pure culture in
control conditions and Yis is the yield for species i growing in
a pure culture in water stress conditions.
The RSI reflects the relative reduction in biomass as a consequence of water stress. If the RSI equals 0.00, growth is unaffected by water stress; if the RSI is between 0.00 and 1.00,
growth is negatively affected by water stress (the closer to
1.00, the greater the effect); finally, if the RSI is between less
than 0.00, the plants experiencing water stress produce
greater biomass than the control plants.
RSI was compared between species with a one-way
ANOVA with factor ‘species’ at three levels. Multiple comparisons of means were performed with a Tukey test. Independent t-tests were applied to check if the RSI was different
from 0.00 (P ¼ 0.05). All statistical analyses were performed
using SAS software (SAS, 1999).
3.
Results
3.1.
Pure cultures
Although survival for each of the three species growing in pure
cultures was unaffected by water stress (c2 ¼ 0.38; df ¼ 1;
P ¼ 0.54), significant differences were found between species
(c2 ¼ 9.01; df ¼ 2; P ¼ 0.01). Thus, survival for S. malacitanus
was significantly lower than for the other two species
(survival ¼ 0.74 0.06), although no significant differences in
survival were detected for S. inaequidens and S. pterophorus
(0.86 0.04 and 0.94 0.02, respectively; LS-means at P ¼ 0.05).
There was no difference in individual aboveground biomass for the three species growing in non-limiting water conditions (LS-means P > 0.05), although biomass was strongly
reduced by water stress in all species (F ¼ 51.85; df ¼ 1, 18;
P < 0.001), and this was confirmed by the Relative Stress Index
73
acta oecologica 31 (2007) 69–78
S. inaequidens
vs
S. malacitanus
1.0
0.8
SURVIVAL
(RSI), which was above zero for all three species (independent
t-tests at P ¼ 0.05). In the water stress treatment, the individual
biomass for S. pterophorus was statistically lower than the
individual biomass for the other two species (LS-means
P < 0.001, interaction species treatment F ¼ 3.71; df ¼ 2, 18;
P ¼ 0.04). Results of RSI (Mean S.E.) show that the species
that suffered least and most from water stress were S. malacitanus (0.25 0.17) and S. pterophorus (0.62 0.04), respectively.
While RSI of S, pterophorus was significantly higher than
S. malacitanus, no significant differences were found between
S. inaequidens (0.50 0.02) and the other two congeners.
0.6
0.4
0.2
0.0
3.2.
Competitive interactions
1:0
1:1
1:0
Water stress
3.2.1. Growth and survival for the S. inaequidens–
S. malacitanus pair (SI:SM)
S. inaequidens
vs
S. pterophorus
1.0
0.8
SURVIVAL
Survival of S. inaequidens was significantly higher than that of
S. malacitanus, and was unaffected by water treatment or culture (Table 1, Fig. 1). Individual aboveground biomass of S. malacitanus was significantly reduced in the mixed culture with
S. inaequidens, and that of S. inaequidens was significantly
1:1
Control
0.6
0.4
0.2
Table 1 – ANOVAs for survival and individual biomass for
combinations of Senecio inaequidens (SI), S. malacitanus
(SM) and S. pterophorus (SP)
df
Survival
Chi-square
Mean
square
F value
(a) SI–SM
Water treatment (T)
Proportion (P)
TP
Species (S)
TS
PS
TPS
Residual
1
3
3
1
1
3
3
48
0.00
10.32**
2.61
12.40***
0.00
2.75
0.94
48.08
7.66144
1.12107
0.05539
21.44206
0.04081
4.22207
0.04326
0.14358
53.36***
7.81***
0.39
149.34***
0.28
29.41***
0.30
(b) SI–SP
Water treatment (T)
Proportion (P)
TP
Species (S)
TS
PS
TPS
Residual
1
1
1
1
1
1
1
24
0.13
0.20
0.34
6.90**
0.00
26.62**
0.03
22.237
4.52057
3.95314
0.04610
18.23038
0.03194
10.33996
0.33958
0.05492
82.31***
71.97***
0.84
331.92***
0.58
188.25***
6.18
(c) SM–SP
Water treatment (T)
Proportion (P)
TP
Species (S)
TS
PS
TPS
Residual
1
1
1
1
1
1
1
24
0.30
1.62
0.01
3.62
4.32*
1.26
1.74
24.46
3.21274
0.01156
0.00589
0.65192
3.73427
0.12961
1.11664
0.08516
37.73***
0.14
0.07
7.66*
43.85***
1.52
13.11**
1:0
1:1
1:0
Water stress
Biomass
1:1
Control
S. malacitanus
vs
S. pterophorus
1.0
0.8
SURVIVAL
Source
0.0
0.6
0.4
0.2
Survival was analysed with binomial error and logit link. *P < 0.05;
**P < 0.01; ***P < 0.001.
0.0
1:0
1:1
Water stress
1:0
1:1
Control
Fig. 1 – Mean survival ( ± S.E.) for studied species grown
in pure and mixed cultures in water stress and control
conditions. For the sake of clarity, 2:1 and 1:2 proportions
are not shown. (a) Senecio inaequidens vs. S. malacitanus; (b)
Senecio inaequidens vs. S. pterophorus; (c) Senecio malacitanus
vs. S. pterophorus.
enhanced in the mixed culture (interaction proportion x species: Table 1a). Water stress produced a significant reduction
in the final individual biomass for both species (Fig. 2).
3.2.2. Growth and survival for the S. inaequidens–S.
pterophorus pair (SI:SP)
Survival of S. pterophorus was significantly reduced when it
grew in mixed culture with S. inaequidens (Fig. 1), whereas
74
acta oecologica 31 (2007) 69–78
proportion species, Table 1b). This effect was stronger in
the control pots than in water-stressed pots (interaction treatment proportion species, Table 1b), where S. inaequidens
growth was greater, unlike S. pterophorus, whose growth
remained the same.
S. inaequidens
vs
S. malacitanus
5
(g/plant)
BIOMASS
4
3
3.2.3. Growth and survival for the S. malacitanus–
S. pterophorus pair (SM:SP)
2
1
0
1:0
1:1
Water stress
1:0
1:1
Control
S. inaequidens
vs
S. pterophorus
5
(g/plant)
BIOMASS
4
3
2
When grown in mixed cultures, S. malacitanus and S. pterophorus survival was not significantly affected, althoughdas already indicateddthat of S. malacitanus was significantly
reduced in water stress conditions in the pure culture (Fig. 1;
interaction treatment species, Table 1c). The individual biomass for any of the three species was not affected when
grown together in water stress conditions. However, growth
in the control mixed cultures varied between species: thus,
S. pterophorus showed better growth with S. malacitanus whilst
the latter showed better growth in pure culture (interaction
treatment species and treatment proportion species;
Table 1c, Fig. 2).
Overall, the species that showed best growth was S. inaequidens; for the other two species growth depended on treatment
and culture proportions.
1
3.3.
0
1:0
1:1
Water stress
1:0
1:1
Control
S. malacitanus
vs
S. pterophorus
5
(g/plant)
BIOMASS
4
3
2
1
0
1:0
1:1
Water stress
1:0
1:1
Control
Fig. 2 – Mean individual biomass ( ± S.E.) for studied species
grown in pure and mixed cultures in water stress and
control conditions. For the sake of clarity, 2:1 and 1:2 proportions are not shown. (a) S. inaequidens vs. S. malacitanus;
(b) S. inaequidens vs. S. pterophorus; (c) S. malacitanus vs.
S. pterophorus.
The RY for S. inaequidens was significantly greater than 1.00
when grown with S. malacitanus in mixed cultures at 1:2
(SI:SM) in water stress conditions, and at 1:1 and 2:1 in control
conditions, but was not significantly different from 1.00 for
the other proportions. When grown with S. pterophorus, the
RY for S. inaequidens was greater than 1.00 regardless of water
treatment (Table 2).
When grown with S. inaequidens, the RY for S. malacitanus
was significantly less than 1.00 for all proportions and for
both water stress and control conditions. When grown with
S. pterophorus, the RY was significantly greater than 1.00 in water stress conditions but less than 1.00 in control conditions.
The RY for S. pterophorus was always lower than 1.00 when
grown with S. inaequidens. In mixed cultures with S. malacitanus, the RY was not significantly different from 1.00 in water
stress conditions but was greater than 1.00 for the control
treatment.
The RYT was not different from 1.00 except in the case of S.
inaequidens and S. pterophorus growing in water stress conditions, a fact which can be attributed to the biomass reduction
in S. pterophorus (Table 2).
4.
there was no significant difference in S. inaequidens survival
between pure cultures and mixed cultures with S. pterophorus
(interaction proportion x species, Table 1b). Water stress treatment significantly reduced growth (Fig. 2) but not survival
(Table 1b) in both species. When grown in a mixed culture
with S. pterophorus, S. inaequidens produced significantly
more individual biomass than in pure culture (Fig. 2), while
S. pterophorus produced less individual biomass in mixed
culture with S. inaequidens than in pure culture (interaction
RY and RYT
Discussion
Our replacement series experiment showed that the widespread alien Senecio inaequidensdwhich we hypothesised to
be a more successful competitor than the geographically restricted alien S. pterophorus and the native S. malacitanusdwas
the best performer both in water stress and control conditions. Overall, the results showed that biomass production
per plant for S. inaequidens was greater in mixed rather than
in pure cultures, which would indicate that S. inaequidens is
75
acta oecologica 31 (2007) 69–78
Table 2 – Mean Relative Yield (RY) and mean Relative Yield Total (RYT) for each pair of species
Treatment
Proportion
S. inaequidens and S. malacitanus
Stress
Control
2:1
1:1
1:2
2:1
1:1
1:2
S. inaequidens
Mean RY S.E.
S. malacitanus
Mean RY S.E.
Mean RYT S.E.
1.19 0.08
1.33 0.20
2.27 0.29*
1.28 0.09*
1.63 0.15*
2.04 0.31*
0.19 0.06***
0.33 0.09**
0.41 0.10*
0.28 0.08**
0.50 0.08**
0.58 0.09*
0.86 0.05
0.83 0.13
1.02 0.08
0.95 0.03
1.06 0.09
1.07 0.10
S. inaequidens
Mean RY S.E.
S. pterophorus
Mean RY S.E.
Mean RYT S.E.
1.58 0.08**
1.95 0.18*
0.14 0.01***
0.07 0.08***
0.86 0.04*
1.01 0.09
S. malacitanus
Mean RY S.E.
S. pterophorus
Mean RY S.E.
Mean RYT S.E.
S. inaequidens and S. pterophorus
Stress
Control
1:1
1:1
S. malacitanus and S. pterophorus
Stress
Control
1:1
1:1
1.70 0.14*
0.66 0.05**
0.74 0.16
1.57 0.09*
1.22 0.10
1.12 0.06
Means (S.E.) are significantly different from 1 at P < 0.05 (*); P < 0.01 (**) or P < 0.001 (***) by the t-test.
a successful competitor. This conclusion is supported by the
fact that its RY was greater than 1.0 for almost all proportions
with the other two species and for both water treatments.
Moreover, when cultivated with S. malacitanus, survival was
also higher than in pure culture, a fact that would also indicate
its greater competitiveness. Similar results were obtained for
S. madagascariensisdthe invasive diploid taxon of S. inaequidens in Australia (Scott et al., 1998)dwhich also grew and
reproduced more rapidly than the closely related native congener S. lautus (Radford and Cousens, 2000).
When grown in interspecific competition in our pots,
S. inaequidens also showed a broad tolerance to water stress
that was higher than the tolerance exhibited by S. malacitanus,
a species adapted to the semi-arid conditions of southern
Spain.
Unlike S. inaequidens, S. pterophorus performed poorly in water stress conditions (as shown by the RSI results) and was
outcompeted by both S. inaequidens and S. malacitanus in terms
of biomass (confirmed by an RY of less than one). However, in
the case of S. malacitanus, water stress conditions appear to
play a more significant role than competition, which would
explain why the RY in this case is not different from one. In
contrast, in non-limiting water conditions, S. pterophorus was
clearly more competitive than S. malacitanus, although it was
unable to overcome competition from S. inaequidens. The
larger leaves and leaf area ratio (LAR) of S. pterophorus compared to both S. inaequidens and S. malacitanus (Garcia-Serrano
et al., 2005) probably make it more sensitive to drought. Differences in competitive ability between the closely related Solidago canadensis and S. juncea (Potvin and Werner, 1983) and
Conyza canadensis and C. sumarensis (Thébaud et al., 1996)
were also related to differences in total leaf area. The RYT of
less than one for the S. inaequidens–S. pterophorus combination
in water stress conditions can be explained by interference between these species in terms of obtaining water; the fact that
S. inaequidens is more able to exploit this resource may have
had a detrimental effect on the growth of S. pterophorus. We
would have predicted that S. pterophorus, with its higher LAR,
would have the fastest growth rate and therefore, under well
watered conditions, it would outcompete S. inaequidens. In
fact, a study by Garcia-Serrano et al. (2005) shows that, in optimal growth chamber conditions, S. pterophorus is the fastest
growing species; however, in other experiments in sub-optimal conditions (with potted plants), S. pterophorus showed
a lower growth rate than S. inaequidens due to a lower photosynthetic rate per unit leaf area (unpublished results).
S. malacitanus performed very well under drought conditions, as demonstrated by its low RSI in pure cultures. It
should be pointed out that since its distribution area is in
semi-arid Mediterranean regions (rainfall under 350 mm/
year), it is likely to be adapted to stressful water conditions.
Nonetheless, it was outcompeted by S. inaequidens in the water
stress treatment, and it is also strongly outcompeted by both
non-natives in non-limiting water conditions. The competitive performance comparisons reviewed by Daehler (2003)
suggest that the relative performance of invaders and co-occurring natives often depends on growing conditions. In this
sense, many studies have shown that alien species use resources more efficiently than native species in favourable
conditions or disturbed habitats (Kotanen, 1995; Burke and
Grime, 1996; Baruch and Goldstein, 1999; Milberg et al., 1999;
Alpert et al., 2000; Blicker et al., 2002; Kolb et al., 2002; Morris
et al., 2002; Gerlach and Rice, 2003; Leger and Rice, 2003). For
instance, growth of the alien S. madagascariensis in Australia
was shown to increase in response to the addition of nitrogen
and phosphorus to pastures. Moreover, S. madagascariensis
76
acta oecologica 31 (2007) 69–78
allocated a higher percentage of dry matter to stems and capitula than to leaves, thereby enhancing its invasive potential
by increasing its reproductive ability (Sindel and Michael,
1992).
S. pterophorus is a successful competitordand therefore
a successful invaderdin areas with no water restrictions (indeed, its populations are mainly located along river banks
without strong water limitations). This conclusion concurs
with other studies which show that invasion by alien species
is easier in habitats with some degree of disturbance (Alpert
et al., 2000) that increases the level of resources such as nitrogen, light and temperature fluctuations (D’Antonio and
Meyerson, 2002).
The competitive differences between the two alien species
were also demonstrated in another experiment in field conditions (Sans et al., 2004). In that experiment, the same three
species were not directly in competition, but were transplanted into separate plots with established herbaceous vegetation (mostly annuals). Resource availabilitydmainly water
but also nutrientsdwas manipulated in order to observe plasticity in response to competition. It was found that the two
alien species competed more successfully than the native species in non-limiting water conditions. In water-limited plots,
however, the competitive ability of S. pterophorus, but not
that of S. inaequidens, was greatly reduced. Indeed, the latter,
in contrast with the two other species, seems to have a broader
range of environmental tolerance and can competedand
therefore invadedsuccessfully in more stressful conditions.
This finding also concurs with our field observations, as we
have found this species in both wet and dry habitats and at altitudes ranging from sea level to 2000 m. Moreover, our results
have shown that in the case of future coexistence, it is likely to
be able to displace S. malacitanus; in environments with a moderate summer stress conditions as in northern parts of the
range of this species. However, it remains to be tested whether
S. inaequidens is adapted to resist severe drought stress as it occurs in the south of the Mediterranean region.
In conclusion, the results of the present study based on
closely pair-wise experiments in contrasting water regimes
strengthen the hypothesis that the competitiveness of aliens
varies depending on performance of target native species. In
addition, the hypothesis that the more widespread alien is
more competitive has been confirmed for both stressful and
non-stressful conditions, but the response of the more restricted alien to competition from its native congener will
vary depending on water availability. This suggests that invasion by alien plants is highly dependent on the characteristics
of both species and habitat.
Acknowledgements
We would like to thank C. Collin and all people at the experimental fields at the CEFE for assistance with the mechanism
for avoiding rain and irrigation of the pots. We thank J. Shykoff
and two anonymous reviewers for valuable comments on
a previous version of the paper. This research was partially
funded by the Catalan Government Department for Universities, Research and the Information Society with a fellowship
to the first author, by the GDRE between France and Spain
‘‘Ecosystèmes méditerranéens et montagnards dans un
monde changeant’’ (Centre National de la Recherche Scientifique) and by the Science and Technology Department of the
Spanish Government (project REN2001-2837/GLO).
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