Download A comparative growth analysis between alien invader and native

12 (1): 35-43 (2005)
A comparative growth analysis between alien
invader and native Senecio species with
distinct distribution ranges1
Hèctor GARCIA-SERRANO2, Departament de Biologia Vegetal, Facultat de Biologia, Universitat de
Barcelona, Av. Diagonal 645, 08028 Barcelona, Catalunya, Spain, e-mail: [email protected]
Josep ESCARRÉ & Éric GARNIER, Centre d’Écologie Fonctionelle et Évolutive (CEFE) du
F.
Centre National de la Recherche Scientifique (CNRS), 1919 Route de Mende, 34293 Montpellier
Cedex 05, France.
Xavier SANS, Departament de Biologia Vegetal, Facultat de Biologia, Universitat de Barcelona,
Av. Diagonal 645, 08028 Barcelona, Catalunya, Spain.
Abstract: A good way to check hypotheses that explain the invasion of ecosystems by exotic plants is to compare congeneric
alien and native species. To test the hypothesis that alien invaders grow faster than natives, the maximum relative
growth rate and its components were compared in controlled growth conditions between four Senecio species, two aliens
introduced from southern Africa (S. inaequidens and S. pterophorus) and two European natives (S. malacitanus and S.
jacobaea). The four species colonize similar habitats, but the frequency and abundance of their populations and their
distribution ranges differ. The two aliens showed a higher relative growth rate than the natives, and although there were
differences between species for leaf area ratio, leaf dry matter content, and dry matter partition between stems, leaves,
and roots, no clear pattern was detected to explain the differences in growth rates: several combinations of the
components of the relative growth rate can give similar results. The higher relative growth rate of the alien species,
combined with other ecological and life-history traits, may enhance their invasive capacity.
Keywords: alien, interspecific comparisons, invasion, native, relative growth rate, Senecio.
Résumé : Une bonne façon de tester les hypothèses expliquant l’invasion des écosystèmes par des plantes exotiques est
de comparer les espèces étrangères et indigènes appartenant à un même genre. Nous avons utilisé le taux de croissance
relatif maximal afin de tester l’hypothèse que les espèces exotiques envahissantes croissent plus rapidement que les
espèces indigènes. Le taux de croissance relatif maximal et ses composantes ont été comparés en conditions contrôlées
chez quatre espèces de Senecio, soit deux espèces introduites provenant d’Afrique du Sud (S. inaequidens et S.
pterophorus) et deux espèces indigènes européennes (S. malacitanus et S. jacobaea). Les quatre espèces colonisent des
habitats similaires, mais la fréquence d’apparition et l’abondance de leurs populations ainsi que leur répartition sont
différentes. Les deux espèces exotiques montrent un taux de croissance relatif supérieur à celui des espèces indigènes. Il
existe des différences entre les espèces au niveau du rapport de la surface de la feuille, du contenu en matière sèche de
la feuille et du partage de la matière sèche entre les tiges, les feuilles et les racines, mais aucun patron bien défini ne semble
expliquer les différences dans les taux de croissance. Plusieurs combinaisons des composantes du taux de croissance relatif
peuvent donner des résultats similaires. Le plus haut taux de croissance relatif des espèces exotiques combiné à d’autres
caractéristiques écologiques ou du cycle vital peuvent favoriser ces espèces lorsqu’elles envahissent de nouveaux milieux.
Mots-clés : comparaisons interspécifiques, espèce exotique, espèce indigène, invasion, Senecio, taux de croissance
relatif.
Nomenclature: Bolòs & Vigo, 1995; Stace, 1997.
Introduction
Invasion by alien species can have both a detrimental
effect on ecosystems (Vitousek & Walker, 1987; Mack et
al., 2000) and a great economic impact (Pimentel et al.,
2000). Some alien species can outcompete and displace
native species or hinder their regeneration (Vitousek,
1990), thereby lowering the diversity of invaded ecosystems or modifying ecosystem characteristics and function
(Vitousek & Walker, 1987; Blank & Young, 2002).
Consequently, biological invasion is a threat to biodiversity
1Rec.
2004-04-20; acc. 2004-09-01.
Editor: Gilles Houle.
2Author for correspondence.
1Associate
and an important agent of global change (Vitousek et al.,
1996; Chapin et al., 2000; Mack et al., 2000). Habitat
disturbance and nutrient enrichment of soils, often after a
disturbance, may favour the proliferation of alien invasive
species (Davis & Pelsor, 2001). Actually, most exotic
species grow in disturbed and nutrient-rich ecosystems
(Fox & Fox, 1986; Hobbs & Huenneke, 1992; Meiners,
Pickett & Cadenasso, 2002).
Although many studies have addressed this topic,
there is no clear consensus as to the traits that make a
species invasive (Roy, 1990; Alpert, Bone & Holzapfel,
2000). Since invasive alien species are usually released
from the pressure of their native herbivores and parasites
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GARCIA-SERRANO
ET AL.:
GROWTH
ANALYSIS OF ALIEN AND NATIVE CONGENERIC SPECIES
in the invaded region (Keane & Crawley, 2002), there is
an increased allocation of resources to growth because of
a reduction in allocation to herbivore defence (Blossey &
Nortzhold, 1995; Torchin et al., 2003). This increased
growth can confer a superior competitive capacity to
aliens relative to that of natives (Baker, 1965; Noble,
1989; Bakker & Wilson, 2001). The competitive ability
of seedlings is related to seedling size, which depends on
seed size and relative growth rate (Marañón & Grubb,
1993). Furthermore, for species or populations of comparable seed size, the time to reach a critical seedling size is
an important component of fitness because large seedlings
may capture a larger share of resources and can survive
better, since smaller seedlings are more susceptible to
environmental constraints (Solbrig & Solbrig, 1984; Pino,
Sans & Masalles, 1986). This has led numerous authors
(Grime, 1973; Baker, 1974; Grime & Hunt, 1975;
Bazzaz, 1986; Davis, Grime & Thompson, 2000; Davis
& Pelsor, 2001) to hypothesize that a high relative growth
rate (RGR) favours plant colonization, especially in
resource-rich and disturbed ecosystems.
Few studies have compared the growth of alien and
native species (Garnier et al., 1989; Pattison, Goldstein &
Ares, 1998; Baruch, Pattison & Goldstein, 2000;
Grotkopp, Rejmanek & Rost, 2002) and, except for the
study by Garnier et al. (1989) on two species of Bromus
and the studies reviewed by Maillet and López (2000) on
several American aliens invading France, they have usually
found higher growth rates in aliens than in natives. With
the exception of the studies by Garnier et al. (1989) and
Grotkopp, Rejmanek, and Rost (2002), comparisons were
made between species from different genera and even
families, and there can be a confounding effect of phylogeny on the traits analyzed. Therefore, it might be more
meaningful to study closely related species, which can
yield clearer results in the comparisons due to the minimization of differences due to phylogeny (Mack, 1996;
Radford & Cousens, 2000).
Here we compared the growth of two alien and two
native species within the same genus, and we tested the
hypothesis that the alien invasive species have higher
growth rates than the natives. Furthermore, we compared
the components of RGR (ULR, LAR, LMR, and SLA;
see Table I for abbreviations and measurement units) in
order to improve our understanding of the underlying
causes of differences in growth rates between aliens and
natives. Classically, RGR can be broken down into the
product of ULR ¥ LAR, and LAR can be further broken
down into LMR ¥ SLA (Hunt, 1982). To assess these
parameters, a growth analysis of congeneric species from
the genus Senecio present in Spain was conducted under
optimal growth-chamber conditions. Two of these species
(the aliens Senecio inaequidens and S. pterophorus) can
be classified as “novel, invasive colonizers” in Europe,
with invaded areas of distinct size. The other two (the
natives S. malacitanus and S. jacobaea) can be classified
as “successional colonizers” (Davis & Thompson, 2000),
although the latter is a “novel, invasive colonizer” type of
invader in Australia and New Zealand (Parsons &
Cuthbertson, 1992; Wilson et al., 1992). In previous
36
TABLE I. Abbreviations, name, and units of growth and morphological parameters.
Abbreviation
Name
Units
RGRDM
RGRA
ULRDM
ULRA
LAR
LMR
SMR
RMR
SLA
LDMC
Relative growth rate (dry mass)
Relative growth rate (area)
Unit leaf rate (dry mass)
Unit leaf rate (area)
Leaf area ratio
Leaf mass ratio
Stem mass ratio
Root mass ratio
Specific leaf area
Leaf dry matter content
g·g-1 plant ·d-1
m2·m-2 total ·d-1
g·g-1 leaf ·d-1
g·m-2·d-1
m2·kg-1 plant
g leaf ·g-1 plant
g stem ·g-1 plant
g root ·g-1 plant
m2·kg-1 leaf
g dry mass ·g-1 fresh mass
studies comparing S. inaequidens, S. pterophorus, and S.
malacitanus, we have found that there were no differences in the ability to emerge and establish between the
native S. malacitanus and the alien S. inaequidens,
whereas S. pterophorus had a lower emergence but a
proportionally higher establishment (Garcia-Serrano,
Escarré & Sans, 2004). Furthermore, the competitive
abilities of the two aliens were higher than those of the
natives when resources were not limiting (H. GarciaSerrano, unpubl. data).
Methods
PLANT MATERIAL
Senecio inaequidens and S. pterophorus are dwarf
shrubs of south-African origin. The former was introduced accidentally in Europe at the end of the nineteenth
century (Ernst, 1998). Today, it is widespread throughout
Western Europe, where it forms dense populations in
recently abandoned fields and in road margins. It also
colonizes heavily grazed grasslands. First recorded in
1995 near Barcelona (Pino et al., 2000), S. pterophorus
was recently introduced in Europe, and its geographical
distribution is still small. It also forms very dense populations, mainly in disturbed riverbeds, and plants can grow
up to 2 m high. According to Davis and Thompson
(2000), these two species can be classified as “novel,
invasive colonizers”, although S. inaequidens is far more
widespread than S. pterophorus.
Senecio malacitanus (also named S. linifolius) is a
dwarf shrub native to southern Europe that forms sparse
populations in temporarily flooded rivers and other disturbed sites nearby. Its geographical distribution is limited
to the southeast of the Iberian Peninsula and the Maghreb,
in semi-arid climates (under 350 mm·y -1 ). Senecio
jacobaea is a biennial or short-lived perennial native to
Europe and is widespread throughout the entire continent.
It can form dense stands in damp pastures with a certain
degree of disturbance, and sometimes coexists with S.
inaequidens (Ernst, 1998). Both species are “successional
colonizers” (sensu Davis & Thompson, 2000) in Europe,
although S. jacobaea is an aggressive invader in Australia
and New Zealand (Parsons & Cuthbertson, 1992; Wilson
et al., 1992).
Seeds from all four species were collected from populations growing in the Iberian Peninsula. Seeds from
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S. inaequidens were collected from a recently abandoned
field in Cantallops, northern Catalonia, near the SpanishFrench border, while those from S. pterophorus were collected from a population growing on the riverside of the
Ripoll river, near Barcelona. Seeds from S. malacitanus
came from Rambla del Rambutjar, a seasonal Mediterranean river near Alacant, and those from S. jacobaea were
collected in a population growing in a disturbed site near
Burgos. The mass of five replicates of 10 seeds of each
species was determined and tested for differences by an
analysis of variance and LSD test.
We selected these four species because 1) they differ
in origin and extent of distribution area; 2) they are of the
same genus, thereby reducing phylogenetic biases in the
comparison; 3) they colonize similar habitats, disturbed and
nutrient-rich sites (disturbed riverbeds and riversides of
temporary watercourses, roadsides, recently abandoned
fields, and waste ground); 4) they are all perennials; three
of them are dwarf shrubs (S. malacitanus, S. inaequidens
and S. pterophorus) and one is a hemicryptophyte (S. jacobaea), which does not usually flower during the first
growing season (Bolòs & Vigo, 1995); and 5) their current
distribution areas nearly overlap in Europe. Senecio malacitanus can easily be mistaken for S. inaequidens, to the point
that the first authors to find S. inaequidens in Europe identified it as S. linifolius (a synonym of S. malacitanus). Both
exotic species are extending their respective ranges
towards the south of the Iberian Peninsula and may, in
the future, interact competitively with the native S. malacitanus. Although the growth form of S. jacobea is not the
same as that of the other three species, it was included in
this study because it already coexists with S. inaequidens
in Central Europe and is also invasive in other regions of
the world.
GROWTH TECHNIQUE
Seeds were germinated on moist filter paper placed
vertically in plastic folders, with a 12:12 h photoperiod
and temperatures of 22 °C (day) and 19 °C (night). All
seeds were germinated in deionized water. Twenty-five
plants were transplanted into a water culture system when
their cotyledons were fully expanded and before the formation of any true leaves, when their size was between 2
and 5 cm length, including the radicle (day 0). Plants
were grown hydroponically in a growth room, as described
in Garnier (1992), with the nutritive solution described by
Koch et al. (1987), and artificial light was provided by
four metal halide lamps (Osram HQI-T 400 W, Berlin,
Germany). The photoperiod was set at 16:8 h (day:night),
the air temperature was 22:18 °C and relative humidity
was maintained above 60%. The mean (± SE) photosynthetically active radiation (PAR) at seedling height was
515 ± 8 mmol·m-2·s-1 (n = 100).
HARVESTS AND GROWTH ANALYSIS
Four to five plants per species were harvested at days
10, 15, 18, 22, and 25 after transplantation into the culture system. Each plant was divided into roots, stems,
and leaves. Cotyledons and the hypocotyl were included
in the leaf and in the stem, respectively. The leaf area of
each plant was determined with a Delta-T area meter
VOL.
12 (1), 2005
(MK2, Cambridge, United Kingdom). Fresh mass was
measured for each organ, and dry mass was measured
after drying at 60 °C for 48 h.
Relative growth rates expressed on a total dry mass
(RGRDM: unit of dry mass increment per day and per unit
of total dry mass of plant) and on a leaf area basis (RGRA:
unit of leaf area increment per day and per unit of leaf
area) and unit leaf rates (ULRA: plant dry mass increment
per day per unit leaf area or ULRDM: per unit leaf dry
mass) were calculated following the functional approach
described by Hunt (1982), using a Fortran version of the
HPcurves program written by Hunt and Parsons (1974).
Differences in RGR between species were tested with an
ANCOVA on the natural logarithm of total dry mass or
leaf area, with number of days after transplanting into the
culture system as covariate, and were considered significantly different when the interaction species ¥ time was
significant. As only one value for each species and harvest is obtained for ULR from Hunt’s program, it is not
possible to perform an analysis of variance and multiple
comparisons of means for this parameter.
As some growth parameters are size dependent, these
were calculated for one harvest for each species such that
the mean total dry mass of the four species ranged
between 0.165 g and 0.242 g (Table II) and did not differ
significantly between them (F3, 15 = 1.00, P > 0.05). This
corresponded to harvests on day 15 for S. inaequidens
and S. pterophorus and on day 18 for S. malacitanus and
S. jacobaea. All comparisons for growth parameters were
performed on data from these harvests, except RGR (see
above paragraph). Specific leaf area (SLA: unit of leaf
area per unit of leaf dry mass), leaf area ratio (LAR: unit
leaf area per unit total mass), leaf, stem, and root mass
ratios (LMR, SMR, RMR: unit organ mass per unit total
mass), and leaf dry matter content (LDMC: leaf dry mass
per unit of leaf fresh mass) were calculated and compared
among species by means of a one-way ANOVA. When
differences were found, a least significant difference test
(LSD) was performed to check for differences between
specific means. Analyses were performed with SAS
Version 8 (SAS Institute, Cary, North Carolina, USA).
Results
SEED SIZE
Seed mass was significantly different among species
(Table II), with the two aliens having smaller seeds than
the two natives. The species with the smallest seed mass
was S. pterophorus, followed by S. inaequidens, S. malacitanus, and S. jacobaea.
DRY
MATTER ALLOCATION
The proportion of dry matter allocated to leaves,
stems, and roots differed significantly among species
(Table II) and remained almost constant over time
(Figure 1). Senecio jacobaea was the species that allocated
the highest proportion of biomass to roots (RMR), whereas it devoted the least to stems (SMR). Senecio pterophorus allocated significantly more biomass to leaves (LMR)
and was the species that directed the least to roots (RMR).
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GARCIA-SERRANO
ET AL.:
GROWTH
ANALYSIS OF ALIEN AND NATIVE CONGENERIC SPECIES
TABLE II. Mean (± SE) growth parameters calculated at comparable total masses of the four species (day 18 for Senecio inaequidens
and S. pterophorus and day 22 for S. malacitanus and S. jacobaea). Different letters indicate significant differences among species
for each variable (protected LSD tests). Numbers in parentheses apply to growth analysis parameters.
Species
Mass of 10 seeds (mg)
Total mass (g)
Proportion of mass
Root mass ratio (RMR)A
Stem mass ratio (SMR)
Leaf mass ratio (LMR)
Leaf area (cm2) A
Leaf area ratio (LAR)
Specific leaf area (SLA)
Leaf dry matter content (LDMC)
Unit leaf rate (ULR) B
ULR area
ULR dry mass
Senecio inaequidens
(n = 4)
Senecio pterophorus
(n = 5)
Senecio malacitanus
(n = 5)
Senecio jacobaea
(n = 4)
F3, 14
6.88 ± 0.19c
0.242 ± 0.035ns
3.98 ± 0.22d
0.165 ± 0.016ns
8.50 ± 0.05b
0.182 ± 0.033ns
9.94 ± 0.59a
0.235 ± 0.039ns
147.64***
1.57 ns
0.247
0.113
0.640
31.6
13.0
20.3
0.130
±
±
±
±
±
±
±
0.019ab
0.006b
0.019b
4.8a
0.2ab
0.4ns
0.015b
25.3 ± 1.6
0.537 ± 0.030
A ANOVA performed on data transformed with natural
B ULR calculated following Hunt and Parsons (1974).
* P < 0.05; ** P < 0.01; *** P < 0.001; ns P > 0.05.
0.192
0.109
0.699
25.2
15.3
22.0
0.223
±
±
±
±
±
±
±
25.2 ± 2.0
0.542 ± 0.029
0.244
0.176
0.580
18.9
10.9
18.6
0.128
±
±
±
±
±
±
±
0.014b
0.006a
0.010c
2.6b
1.0b
1.4ns
0.013b
25.8 ± 1.7
0.527 ± 0.030
0.308
0.079
0.613
32.9
13.8
22.6
0.111
±
±
±
±
±
±
±
0.035a
0.009c
0.033bc
6.7a
0.6a
0.7ns
0.019b
7.14
47.89
8.94
3.50
6.04
2.37
10.10
**
***
**
*
**
ns
***
20.2 ± 1.3
0.449 ± 0.03
logarithms.
GROWTH PARAMETERS
RGR differed significantly among species, expressed
both on dry mass and leaf area, as shown by results of
analysis of covariance (RGRDM: F3, 89 = 5.65, P < 0.01
and RGRA: F3, 89 = 4.25, P < 0.001). The two aliens
showed a significantly higher RGR than the natives
(Table III).
RGRDM was analyzed from the product of ULRA ¥
LAR (Hunt, 1982), and LAR was further broken down
into LMR ¥ SLA. Taking the values from harvests of
equal sizes for the four species (Table II), significant differences in LAR were detected due to the lower value in
S. malacitanus. The values of SLA were not significantly
different among the four species, whereas LMR was significantly smaller in S. malacitanus. Finally, LDMC was
significantly higher in S. pterophorus.
Senecio jacobaea showed the lowest ULR values,
while the three other species had comparable values for
this parameter (differences in ULR cannot be formally
tested: see Methods section).
TRENDS OF GROWTH PARAMETERS OVER TIME
LAR decreased over time in all species; given a constant RGR, this produced an increase in ULRA over time
(Figures 2a and 2b). As stated above, ULRA was lower in
S. jacobaea than in the other species, which explains its
lower RGR given its high LAR (Table II). Moreover,
LAR and ULRA in this species were nearly constant over
time. In contrast, ULRA in S. malacitanus was similar to
that of the two aliens, but its LAR was significantly lower
because of its significantly smaller LMR, which explains
its lower RGR.
Discussion
GROWTH PARAMETERS AND DRY MATTER ALLOCATION
The RGRs of the four species are among the highest
values found in studies performed on European herbaceous species (Grime & Hunt, 1975; Poorter & Remkes,
1990; Ryser & Wahl, 2001). In the same growth system,
38
0.009c
0.004b
0.007a
2.7ab
0.9a
1.5ns
0.018a
Garnier (1992) found a mean value of 0.21 g·g-1plant·d-1
for annual and perennial grasses, and Meerts and Garnier
(1996) found values between 0.381 and 0.432 g·g-1plant·d-1
in several ecotypes of Polygonum aviculare. Marañón and
Grubb (1993) found values of RGR between 0.239 and
0.333 g·g-1·d-1 for seven annual Asteraceae. High values
of RGR are usually related to high values of LAR, and
this is usually related to high values of SLA (Poorter &
van der Werf, 1998; Poorter & Garnier, 1999). However,
the LAR values in our study were small compared to those
obtained for other species with similar RGRs (Poorter &
Remkes, 1990). The fastest growing species, S. pterophorus, had a high value of LAR compared to S. malacitanus,
but it did not differ from that of S. jacobaea, which
showed a lower RGR. Analyzing the components of LAR
we found that the four species had smaller SLAs and similar LMRs compared to the values reported by Poorter
and Remkes (1990) and to the values for seven annual
Asteraceae reported by Marañón and Grubb (1993).
However, a comparison of the four species shows that
SLA did not differ among them, whereas LMR was the
only parameter that was higher in the fast-growing S. pterophorus and smaller in the slow-growing S. malacitanus.
Nevertheless, our observations do not explain the differences in the RGR of S. inaequidens and S. jacobaea,
whose RGRs differed but whose values of LAR and its
components were similar. Thinner leaves should compensate the higher value of LDMC in S. pterophorus,
because SLA (1/[LDMC ¥ leaf thickness]) did not differ
between species.
The values of ULR calculated for the four Senecio
species were higher than those reported for several perennial plants by Poorter and Remkes (1990) and for seven
annual Asteraceae by Marañón and Grubb (1993), indicating that the high RGRs in the Senecio species are not
related to LAR and its components but to ULR.
Comparison of ULR values among the four species
showed that the lower RGR of S. jacobaea was related to
its lower ULR. In fact, the growth form of this species
differs considerably from that of the other three, as it
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FIGURE 1. Total biomass and its allocation to stems, leaves, and roots during the course of the experiment. On the total mass plots, the continuous
line is the biomass estimate from the RGR function calculated by Hunt and Parsons’ (1974) program, with the first-order polynomial function, and
dots are measured mean biomasses (± SE).
TABLE III. Relative growth rates (mean ± SE) and classification of the four Senecio species. Different letters indicate significant differences among species for each variable (protected LSD tests).
Colonizer type
(Davis & Thompson, 2000)
S.
S.
S.
S.
inaequidens
pterophorus
malacitanus
jacobaea
novel, invasive
novel, invasive
successional colonizer
successional colonizer
RGRDM
(g·g-1 plant ·d-1)
Status
alien/widespread
alien/restricted
native/restricted/arid
native/widespread/humid
0.343
0.365
0.298
0.274
±
±
±
±
0.019b
0.019a
0.018c
0.014c
RGRA
(m2·m-2 total ·d -1)
0.317
0.349
0.279
0.268
±
±
±
±
0.019b
0.019a
0.016d
0.015c
RGRDM: Relative growth rate calculated from dry matter increase.
RGRA: Relative growth rate calculated from leaf area increase.
forms a rosette of leaves, which may cause more leaf
overlapping and shading. A comparison of the ULR
between S. pterophorus, S. malacitanus, and S. inaequidens, which have the same growth form, showed that
the species with the higher RGR, S. pterophorus, had a
slightly lower ULR, whereas the more slowly growing S.
malacitanus had a slightly higher ULR. Although a negative relation between RGR and ULR is not usually detected in interspecific studies, other studies that compared
genotypes within a species or closely related species also
reported this negative trend (Gottlieb, 1978; Meerts &
Garnier, 1996). The lack of clear relationships between
RGR and its parameters across the species studied can be
explained by the fact that we analyzed only four species
and all four are within a narrow range of RGR values.
Senecio jacobaea is a biennial or short-lived perennial, and it forms a basal rosette of leaves and a taproot
during its first growing season in order to store energy to
elongate the reproductive stem in the second year. This is
consistent with its higher RMR. In contrast, S. malaci-
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39
GARCIA-SERRANO
ET AL.:
GROWTH
ANALYSIS OF ALIEN AND NATIVE CONGENERIC SPECIES
1993). Moreover, seedling size can be critical for resisting environmental constraints (Solbrig & Solbrig, 1984).
Our results show that although there are differences in
seed mass among species, differences in the final seedling
size of the four species studied are related to RGR and
not to seed size. The growth potential of the two alien
species is higher than that of the two natives. Other studies have reported that alien species are able to exploit
resources better than natives (Burke & Grime, 1996;
Baruch & Goldstein, 1999; Milberg, Lamont & PerezFernandez, 1999; Alpert, Bone & Holzapfel, 2000;
Blicker, Olson & Engel, 2002; Kolb et al., 2002; Morris,
Walck & Hidayati, 2002; Gerlach & Rice, 2003; Leger &
Rice, 2003). For example, the growth of S. madagascarensis, a South African invader in Australia that is the
diploid form of S. inaequidens (Lafuma et al., 2003), was
enhanced by nitrogen and phosphorus addition in
Australian pastures more than coexisting native grassland
species (Sindel & Michael, 1996). Moreover, S. madagascarensis was found to grow faster than its native Australian
congener S. lautus (Radford & Cousens, 2000).
As stated previously, our results show that there is no
clear relation between RGR and LAR, and even less
between RGR and SLA. Although some explanation for
the higher values of the RGR of aliens can be found in
LMR, ULR also plays an important role in explaining differences among the four species. Grotkopp, Rejmanek,
and Rost (2002) compared the RGR of 29 invasive and
non-invasive Pinus species and found that the RGR of
invader pines was higher than that of non-invaders, and
that this was strictly related to differences in SLA.
Garnier et al. (1989) compared the growth of two Bromus
species, one invader and one non-invader, but found no
differences in RGR or its components. Pattison, Goldstein,
and Ares (1998) compared the growth and biomass allocation of four native and five alien species in Hawaii
grown under a range of irradiance. Only one pair of congeneric species, from the genus Bidens, were compared in
their study; they reported that the higher RGR of the
invader was mainly due to a higher LAR, especially
under shade conditions. On the basis of those studies, it is
surprising that differences in the invasive behaviour of the
species included in our study were not clearly related to
these parameters.
FIGURE 2. LAR, ULRA, and LMR values during the course of the
experiment. For LAR and LMR, dots are the parameters measured and
lines are the estimates from Hunt and Parsons’ (1974) program. For
ULRA we show only estimated parameters. SLA is not shown because
there are no differences among species.
tanus allocated significantly less biomass to leaves, and
this may be due to an adaptation to the dry habitats that it
inhabits in southern Spain. This hypothesis is supported
by a lower LAR value.
RGR AND INVASIVE ABILITY
It has been hypothesized that alien invaders are more
competitive than natives (Baker, 1965; Noble, 1989;
Bakker & Wilson, 2001). Competitive ability can be
related to size, and the size of a seedling depends on its
RGR and on the size of the seed (Marañón & Grubb,
40
HOW
DO OUR
RGR
RESULTS HELP TO IMPROVE KNOWLEDGE
OF THE INVASIVE ABILITY OF THE SPECIES STUDIED?
The two alien species analyzed in this study, S. inaequidens and S. pterophorus, displayed the highest RGR of
all four species. A high RGR can be a valuable trait in a
colonization event, as plants with this trait can grow fast
after germination, thereby avoiding competition from
other plants. However, our experiment was performed
under optimal nutrient conditions, and results may differ
depending on the availability of soil resources.
In field conditions, S. pterophorus, which had the
highest RGR in our experiment, grows preferentially in
areas with abundant resources and seems to be sensitive
to water stress. Well-established populations of this
species are restricted to places with high resource avail-
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ability, where it can grow to its high RGR potential.
Senecio inaequidens populations are more widespread,
colonizing old fields and road margins. Both species
might benefit from the availability of sufficient resources
to reach their highest RGR potential in order to establish
and compete with pioneer species. A high initial growth
rate and a perennial life-history make a good life-history
trait combination that favours establishment after a disturbance and allows the maintenance of a stock of adult
plants when establishment is difficult because of a scarcity
of suitable sites.
On the other hand, field and controlled experiments
with the two aliens S. inaequidens and S. pterophorus and
the native S. malacitanus (Sans, Garcia-Serrano & Afán,
2004; H. Garcia-Serrano, F. X. Sans & J. Escarré, unpubl.
data) have shown that the two aliens are more competitive
than the native S. malacitanus, especially S. inaequidens,
which out competes the other two species even under water
stress. In addition, the two alien species start flowering very
early in their life, particularly S. inaequidens. An early flowering can confer a high invasive potential on these species,
as they can establish populations that are a crucial source of
seeds for the colonization of nearby sites.
The two natives also displayed high RGRs, which is
to be expected since they colonize disturbed and nutrientrich environments. However, their maximum potential
RGR is lower than that of the aliens, and this may explain
their lower invasive potential. Nevertheless, the case of S.
jacobaea differs, since it is an alien invader in other parts
of the world. Because of its distinct growth form (an initial basal rosette) and life cycle (hemicryptophyte), our
results for this species are not strictly comparable with
the other three species analyzed. The strategy of growing
a rosette of leaves and storing nutrients in a root might
reduce RGR because of shading among leaves in the
rosette, but it may be a good strategy for pre-empting the
space available. However, flowering does not occur until
the next growing season, and compared to the two alien
species, this may reduce its invasive potential.
Finally, S. malacitanus showed the lowest RGR
among the species analyzed, although it is rather high
compared to other species; this high RGR may be an
adaptation for colonizing disturbed habitats. The distribution area of this species is located in zones with considerable periodic water restrictions, and this may explain its
lower LAR and, therefore, its lower RGR. A lower LAR,
related to a low LMR, may be an adaptive response to
prevent water loss in arid environments. Moreover, this
species starts flowering later than the two aliens (H. GarciaSerrano, unpubl. data), thus reducing its invasive ability.
A high RGR appears to be a favourable trait for a
colonizing species, as shown by the high values found in
the four species analyzed, although in this case different
combinations of RGR components yielded similar RGRs.
The alien species in our study showed higher RGRs than
the natives, and this, combined with other ecological and
life-history traits, such as enhanced competitive abilities,
early flowering, and a high reproductive output, can
enhance their ability to invade new habitats.
VOL.
12 (1), 2005
Acknowledgements
The authors thank G. Laurent for help during the experiment. We would also thank G. Houle and two anonymous
reviewers for their helpful comments on previous versions of the
manuscript. 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
Science and Technology Department of the Spanish Government
(project REN2001-2837/GLO), and by the Laboratoire
Européen Associé “Mediterranean Ecosystems in a changing
world” (Centre National de la Recherche Scientifique).
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43