Tree Physiology 21, 1327–1334
© 2001 Heron Publishing—Victoria, Canada
Carbon uptake, growth and resource-use efficiency in one invasive and
six native Hawaiian dry forest tree species
L. C. STRATTON1,2 and G. GOLDSTEIN1
1
Botany Department, University of Hawaii, 3190 Maile Way, Honolulu, HI 96822, USA
2
Present address: P.O. Box 752, Avalon, CA 90704, USA
Received March 21, 2001
Summary Photosynthetic gas exchange, nitrogen- and water-use efficiency, leaf water potential and seasonal patterns of
leaf production were studied in seven, dominant dry-forest
species from the island of Lana‘i, Hawaii, including the rapidly
colonizing, non-native Schinus terebinthifolius (Raddi). We
evaluated whether unique physiological characteristics of the
invasive species explain its capacity to rapidly invade dry forests throughout the Hawaiian Islands. Apparent anomalies in
stable carbon isotope data (δ13C) relative to other results led us
to study effects of environmental conditions and physiological
performance during leaf expansion on δ13C. Species that expanded all their foliage at the beginning of the wet season had
more negative leaf δ13C values during the dry season than species with continuous leaf expansion. Among species, S. terebinthifolius had a strong seasonal pattern of leaf production
and the most negative δ13C (–29 ‰). With respect to almost every trait measured, S. terebinthifolius fell at an end of the range
of values for the native species. Rapid growth of S. terebinthifolius in this ecosystem may be partially explained by its high
maximum CO2 assimilation rates (15 µmol m –2 s –1), low leaf
mass per area, high photosynthetic nitrogen-use efficiency per
unit leaf mass or area and large decrease in stomatal conductance during the dry season. Relative to the native species, the
invasive species exhibited striking phenotypic plasticity, including high rates of stem growth and water and CO2 uptake
during the wet season, and maintenance of leaves and high leaf
water potentials, as a result of reduced water loss, during the
dry season, enabling it to utilize available resources effectively.
Keywords: carbon assimilation, photosynthetic nitrogen-use
efficiency, plasticity, water relations, water-use efficiency.
Introduction
Studies on the ecophysiology of invasive and native species
have provided insight into the mechanisms underlying the success of invasive species (Baruch et al. 1985, Harrington et al.
1989a, 1989b, Schierenbeck et al. 1994, Williams and Black
1994, Pattison et al. 1998). Successful invasive plants tend to
have morphological and physiological traits that enable them
to acquire substantial amounts of resources at low rates of carbon investment (Bazzaz 1986, Vitousek 1986, Baruch and
Goldstein 1999). Environments characterized by temporal
variation in the availability of an important resource pose special problems for profligate use of resources during the unfavorable season. Plasticity in morphological and physiological
traits may allow plants to utilize resources when they are available, and to avoid stressful conditions during periods of scarcity (Grime 1994). We hypothesized that in a seasonal environment successful invading species adjust physiological activity to maximize use of seasonally limited resources when
they become available.
Tropical dry forests, including the Hawaiian dry forests, are
exposed to an extended dry season (Bullock et al. 1995). In addition to prolonged periods of low water availability, trees in
Hawaiian dry forests have to cope with nutrient-poor soils
(Stratton 1995). Although sclerophyllous leaves are generally
associated with dry, low-nutrient conditions, the benefits of
being able to withstand such environmental extremes may not
be competitive against physiologically plastic species with
lower leaf mass per unit area (LMA). In plants with similar life
forms, LMA is usually inversely related to growth rate, because thinner leaves increase the capacity of the plant to sequester CO2 per given mass of carbon invested in photosynthetic tissues (Lambers and Poorter 1992, Reich et al. 1997).
Furthermore, species with low LMA tend to have higher
photosynthetic rates than species with high LMA, because of a
greater density of photosynthetic apparatus per unit leaf area
and mass (Reich et al. 1997).
Hawaiian forest ecosystems are more vulnerable to invasion
by non-native plants than comparable continental ecosystems
(Vitousek 1986, Vitousek et al. 1987, Simberloff 1995).
Eighty-six of the 800 naturalized species are invasive and represent serious threats to native ecosystems (Smith 1985). Understanding the invasive potential of non-native tree species is
of particular concern on island ecosystems that are fragmented
or contain many endemic species, such as the Hawaiian dry
forests. We evaluated the role that physiological determinants
of growth, including net CO2 assimilation, water- and photosynthetic nitrogen-use efficiency, leaf water potential, leaf
mass per area and other leaf traits, play in explaining the recent
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STRATTON AND GOLDSTEIN
increase in abundance of the invasive Schinus terebinthifolius
(Raddi) relative to six dominant, native Hawaiian dry-forest
species.
Materials and methods
Study site and species
The study was carried out between 1994 and 1997 in The Nature Conservancy of Hawaii’s Kanepu’u Dry Forest Preserve
on the island of Lana‘i (20°51′ N, 156°54′ W), Hawaii. Four
discrete (fenced) units, ranging in size from 1 to 0.8 km2 located at a mean elevation of 500 m with a total elevation range
of less than 65 m were intensively studied.
The study area experiences a 5-month dry season from June
through October and a mean rainfall of 500 mm per year. The
maritime environment of the Hawaiian Islands reduces the
evaporative demand relative to continental dry forest sites.
Mean monthly temperatures range from 19.2 to 22.5 °C. The
forest stands, which experience frequent high winds, are
stunted with tree heights averaging 3 to 5 m. The forest is dominated by Nestegis sandwicensis A. Gray (Oleaceae) (65%
canopy cover) and Diospyros sandwicensis A. DC (Ebenaceae) (25% canopy cover). The remaining 10% of canopy
cover is divided among more than 10 other woody species, including the five study species: Pouteria sandwicensis A. Gray
(Sapotaceae), Nesoluma polynesicum Hillebrand (Sapotaceae), Myoporum sandwicense A. Gray (Myoporaceae), Metrosideros polymorpha Gaud. (Myrtaceae), and the non-native
Schinus terebinthifolius Raddi (Anacardiaceae). Schinus terebinthifolius was introduced in the mid-1900s to Lana‘i from
South America (Wester 1992) and is rapidly colonizing seasonally dry environments on all of the major Hawaiian Islands
(Tamimoto and Char 1992). This species is also a major threat
to southern Florida habitats (Ewel 1984). The actual cover of
S. terebinthifolius has been kept low through an active cut and
herbicide program underway since The Nature Conservancy
established the preserve in 1993.
Leaf water potential, photosynthetic gas exchange and stable
carbon isotope composition
Leaf water potential (Ψ) was measured with a pressure chamber (PMS, Corvallis, OR) on nine branches per species, three
each from three individuals in the same unit of the preserve
where gas exchange studies were conducted. Because there
were no statistical differences in Ψ between individuals of the
same species, the data were pooled by species. Samples were
collected before dawn and at midday seven times over the
course of 15 months (December 1994–March 1996), in both
the wet and dry seasons. The samples were placed in sealed
bags and kept in a cooler until balancing pressures were determined at a nearby field station within 1 h of collection.
A photosynthetic gas exchange system (LI-6200, Li-Cor,
Lincoln, NE) was used to measure net CO2 assimilation and
stomatal conductance during both the wet (April 1995) and the
dry season (October 1995) in the two most diverse units of the
preserve. New, fully expanded leaves from exposed areas of
the canopy were selected for measurement. A minimum of
four individuals per species and two leaves per individual
were sampled multiple times in each 3-day sampling period,
from 0900 to 1300 h. Maximum assimilation rates are reported
for photosynthetic photon flux densities (PPFD) above
800 µmol m –2 s –1. Statistical differences in photosynthetic gas
exchange between individuals versus leaves within the same
individual were not significant, so data were pooled by species. Care should be taken when patterns of water use are inferred from stomatal conductance measurements made in
well-stirred leaf chambers. If species differ in leaf size, extrapolations of water use from stomatal conductance could be
misleading. The leaves of the study species were similar in
size, although variable in thickness.
Each leaf whose gas exchange was measured during the dry
season was dried, ground and sent to the Duke Phytotron laboratory for δ13C analysis (n = 5). Natural abundances of 13C and
12
C were measured to an accuracy of ± 0.01% with an SIRA
Series II isotope ratio mass spectrometer (VG Isotech, Middlewich, U.K.). Data were corrected for the uncontrolled contribution of the O2 used in sample combustion (Craig 1957).
Leaves for δ13C were collected during the dry season because
it is the most stressful period for plant growth. The most recently expanded leaves were collected. Depending on the seasonal pattern of leaf production, however, the leaves of some
species had expanded during the wet season and others during
the dry season.
Seasonal variation in leaf expansion, nitrogen use-efficiency
and growth
Leaf phenology was monitored in 10 individuals of each species at 3-week intervals from October 1994 through May 1996
as described by Borchert (1994). The percentages of leaves at
the different developmental stages (newly expanding, fully
mature, and senescing) were recorded every 3 weeks. An index was developed for assessing seasonal variability in leaf
expansion rates among species to compare species quantitatively. Leaf phenology data were analyzed by calculating the
standard deviation for the percent of new foliage measured
during a given 3-week period, with respect to the maximum
for the species over the entire study period. All plants had the
same potential range (0 to 100%) so the standard deviation is
not dependent on the magnitude of the data. Thus, species with
the largest seasonal variation in the proportion of newly expanded leaves, i.e., those that synchronously and rapidly lose
and expand a complete cohort of leaves, had a higher index of
variation (highest standard deviation) than those species that
expanded leaves more slowly and continuously during the
year. The higher the SD, the higher the proportion of leaves
expanded during the wet season (Stratton et al. 2000b). This
index is a quantitative species-specific proxy for the proportion of leaves produced during the wet season.
Leaf nitrogen (N) concentrations were determined concurrently with δ13C measurements. All values of N are expressed
on a mass basis, because N content expressed this way is usually a better predictor of net CO2 uptake and growth potential
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(Field and Mooney 1983, 1986), particularly across different
species, than N concentration expressed on an area basis.
Photosynthetic nitrogen-use efficiency (PNUE), a measure of
net CO2 assimilation per unit leaf N, was based on maximum
net CO2 assimilation rates during the dry season and the N
concentration of those leaves. Leaf mass per area was used to
transform CO2 assimilation from a leaf area to a leaf mass basis for PNUE calculations. A set of 30 randomly chosen fully
expanded leaves, from at least five individuals per species,
was used to estimate leaf mass per unit area (LMA). Leaf areas
were measured with a portable area meter (LI-3000A, Li-Cor),
after which leaves were dried at 60 °C to constant mass and
weighed.
Stem growth was measured with dendrometer bands, in the
four preserve units, on the main stems of 10 individuals per
species over 1.5 years (September1995–June 1997). Measurements were taken quarterly and the final year of data was used
to estimate annual growth in terms of increases in stem crosssectional area relative to initial stem size.
Results
1329
season than in the wet season for all species (Figure 1A).
Myoporum sandwicense exhibited high A during both the wet
and dry season (14.2 and 12 µmol m –2 s –1, respectively).
Among species, the invasive S. terebinthifolius had the highest
A in the wet season (15.4 µmol m –2 s –1), but among the lowest
values in the dry season (4.2 µmol m –2 s –1). The native dominant species, N. sandwicensis, had the lowest A in both the wet
and dry seasons (6 and 2.3 µmol m –2 s –1, respectively).
Stomatal conductance (g) was also lower in the dry season
than in the wet season in all species (Figure 1B). These data
are based on a single 3-day sampling period in each season.
The ratio of net CO2 assimilation to stomatal conductance
(A/g), an estimate of instantaneous intrinsic water-use efficiency (WUE), was substantially higher (> 40%) in the dry
season for all species except N. sandwicensis, which showed
little seasonal change in WUE, and D. sandwicensis, which
was just 35% higher in the dry season (Table 1). Among species, M. sandwicense had one of the lowest values of WUE in
both the wet and dry seasons. Although the invasive S. terebinthifolius had WUE values comparable with those of the native dominants, the increase in WUE in the dry season was
much larger (~75%).
Photosynthetic gas exchange
Maximum net CO2 assimilation rates (A) were lower in the dry
Figure 1. Maximum net CO2 assimilation (A) and stomatal conductance (g) in the wet (open bars) and dry seasons (hatched bars), for
seven dry forest species. Values are means + 1 SE (n > 8).
Carbon isotope composition, and seasonal variations in leaf
expansion and water potential
In leaves collected during the dry season, the most negative
δ13C values were found in the dominant N. sandwicensis and
the invasive S. terebinthifolius, whereas the least negative
δ13C value was in M. sandwicense (Table 1). A negative linear
relationship between δ13C and degree of seasonal variation in
leaf expansion rate was observed across all species (Figure 2).
The species that expanded most of their leaves during the wet
season and therefore had a high standard deviation in seasonal
rate of leaf expansion (N. sandwicensis and S. terebinthifolius)
had the lowest δ13C values. In contrast, M. sandwicense,
which developed leaves more or less continuously through the
year, had the lowest seasonal variation in leaf expansion and
high δ13C values. The remaining species had intermediate
standard deviations in seasonal rate of leaf expansion and intermediate values of δ13C.
There was a positive linear relationship between δ13C and
the percent increase in WUE from the wet to the dry season, in
all native species. The native species with least negative δ13C
had the largest increase in WUE (Figure 3). However, the invasive S. terebinthifolius with the lowest δ13C increased WUE
from wet to dry season by more than 70%. Seasonal changes in
WUE may be a result of leaf-level plasticity in WUE (e.g.,
variation in WUE within a cohort of leaves that flushed simultaneously) or plant- level plasticity in WUE (e.g., variation in
WUE among cohorts of leaves that flushed at different times).
Although the relationship depicted in Figure 3 does not provide a basis for distinguishing between these possibilities, it
suggests that S. terebinthifolius, which expands all its leaves at
the beginning of the wet season, adjusts physiologically to the
decrease in soil water availability more than do the native species with comparably low δ13C (e.g., N. sandwicensis).
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STRATTON AND GOLDSTEIN
Table 1. Stable carbon isotope ratios (δ13C; ‰), instantaneous intrinsic water-use efficiency (A/g; µmol CO2 mol –1 H2O) in wet and dry seasons,
leaf N concentration (nmol N g –1) and dry season photosynthetic nitrogen-use-efficiency (PNUE; µmol CO2 mol N –1 s –1) for seven dry forest
woody species, including the invasive Schinus terebinthifolius. Values of δ13C values, leaf N concentration and PNUE are means from leaf samples obtained during the dry season (n = 5). Values of A/g are the means of n > 8 repeated samples. Values in parentheses are standard errors (SE).
Species
δ13C
A/g
Wet
Dry
Leaf N
PNUE
Diospyros sandwicensis
–26.83
(0.29)
26.9
(1.7)
36.3
(0.5)
0.45
(0.024)
37.2
(0.9)
Metrosideros polymorpha
–25.74
(0.23)
28.2
(1.9)
58.3
(1.2)
0.57
(0.031)
46.5
(1.7)
Myoporum sandwicense
–24.94
(0.18)
13.9
(1.2)
34.3
(2.9)
0.98
(0.018)
87.3
(1.2)
Nesoluma polynesicum
–25.81
(0.15)
32.7
(2.9)
46.4
(1.0)
1.16
(0.10)
28.4
(1.6)
Nestegis sandwicensis
–28.55
(0.16)
24.9
(1.3)
26.5
(1.9)
0.56
(0.029)
22.6
(0.7)
Pouteria sandwicensis
–26.98
(0.28)
20.7
(1.2)
31.1
(1.7)
1.18
(0.030)
23.5
(0.3)
Schinus terebinthifolius
–29.03
(0.21)
21.9
(1.4)
38.2
(0.5)
0.71
(0.038)
75.3
(2.5)
Minimum midday Ψ values measured during the dry season
ranged from –4.1 to –1.5 MPa (Figure 4). Values of δ13C
tended to increase with increasing Ψ among the native species,
and those species with higher δ13C maintained higher mini-
Figure 2. Stable carbon isotope ratios (δ13C) as a function of the degree of seasonal variation (SD) in leaf expansion rates (high SD =
large wet season flush, low SD = continuous, slower leaf expansion).
Values of δ13C are means ± 1 SE (n = 5) from samples obtained during
the dry season. Line represents the linear regression fitted to all data
(r 2 = 0.65).
mum leaf Ψ during the dry season. For example,
M. polymorpha had a minimum leaf Ψ of –1.5 MPa and a δ13C
of –25.7 ‰, whereas N. sandwicensis had a minimum leaf Ψ
of –3.87 MPa and a δ13C of –28.55 ‰. Schinus terebinthifolius was an exception to this linear relationship; it exhibited
Figure 3. Stable carbon isotope ratios (δ13C) as a function of % increase in instantaneous intrinsic WUE (A/g) from the wet to dry season. The δ13C values are means ± 1 SE (n = 5) from samples obtained
during the dry season. Dashed line represents the linear regression fitted to the native species only. Symbols as in Figure 2.
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Figure 4. Stable carbon isotope ratios (δ13C) as a function of minimum annual leaf water potential (Ψ). Values are means ± 1 SE (n = 9
for Ψ, and n = 5 for δ13C obtained from samples collected during the
dry season). Line represents the linear regression fitted to native species. Symbols as in Figure 2.
Figure 5. Stem growth (% annual increase in stem cross-sectional
area) as a function of leaf mass per area (LMA). Values are means ± 1
SE; n = 10 for growth, and n = 30 for LMA. Line represents the exponential decay function fit to all data (R2 = 0.97). Symbols as in Figure 2.
the most negative δ13C (–29.03 ‰) but had a relatively high
leaf Ψ (–1.7 MPa).
Discussion
Stem growth and leaf nitrogen concentration
Among species, S. terebinthifolius had the highest annual relative stem growth rate (21%) followed by M. sandwicense
(9.8%, Figure 5). The remaining species had substantially
lower annual stem growth rates (~4%). Stem growth rate decreased asymptotically with increasing leaf mass per area
(LMA) (Figure 5). Species with low LMA had larger increases
in stem growth rate than species with thicker, more sclerophyllous, leaves. Stem growth rate increased exponentially
with increasing net CO2 assimilation (Figure 6). Relative to
the native species, S. terebinthifolius had the largest stem
growth rate for comparable assimilation rates.
Leaf N concentration, on a mass basis, ranged from 0.45 to
1.2 mmol g –1 (Table 1) and was not strongly correlated with
net CO2 uptake. The poor correlation was probably because
the two latex-bearing species in the family Sapotaceae
(N. polynesicum and P. sandwicensis) had high N concentrations relative to their photosynthetic rates. During the dry season, PNUE ranged from 20 to 90 µmol CO2 mol N –1 s –1 (Table 1). The species with the highest PNUE were M. sandwicense, (87 µmol CO2 mol N –1 s –1) followed by S. terebinthifolius (75 µmol CO2 mol N –1 s –1). The native dominants and
Sapotaceous species had the lowest PNUE. We present PNUE
data for the dry season because this is the period when conflicting demands on water and nutrients resources are likely to
occur for species that retain photosynthetically active leaves.
Stable carbon isotope ratio and water- versus nitrogen-use
efficiency
Stable carbon isotope ratios of leaves collected during the dry
season were linearly related to the seasonal pattern of leaf production, with species producing all their leaves at the beginning of the wet season having the most negative δ13C and
therefore being the least water-use efficient. In general, δ13C
values reflect the photosynthetic characteristics of leaves during the period of leaf expansion; therefore, its use as a comparative indicator of long-term or integrated WUE may be misleading unless the seasonal pattern of leaf production for each
species is taken into consideration. Good agreement across
species was observed between δ13C and the percent increase in
instantaneous intrinsic WUE (A/g) from wet to dry season
when S. terebinthifolius was removed from the regression
analysis. Schinus terebinthifolius, which had low δ13C values
and expanded most of its leaves during the wet season, was
able to adjust WUE by more than 70%, whereas N. sandwicensis, with similar δ13C values and leaf expansion patterns,
was more constrained in its ability to adjust its WUE.
With the exception of the invasive S. terebinthifolius, a positive relationship was observed between δ13C and minimum Ψ
in the dry season, indicating that the native plants were subjected to larger water deficits and were less efficient in conserving water resources than the invasive species. The native
species with high Ψ and δ13C values (M. sandwicense and
M. polymorpha) expand leaves continuously into the dry season, so leaf carbon may have been formed under conditions
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STRATTON AND GOLDSTEIN
Figure 6. Stem growth (% annual increase in stem cross-sectional
area) as a function of net CO2 assimilation. Values of net CO2 assimilation are means ± 1 SE (n ≥ 8). Line describes the modified single exponential function fitted to all data (R2 = 0.88). Symbols as in
Figure 2.
that would result in high WUE. In contrast, S. terebinthifolius
expands all its leaves in a single flush immediately after the
first winter rains, and its δ13C values reflect the more humid
conditions under which leaves expanded. Schinus terebinthifolius also had relatively high leaf specific conductivity
(18.8 mmol m –1 s –1 MPa –1), which may partially explain the
maintenance of high leaf water potentials (Stratton et al.
2000a). Efficient long-distance water transport would probably buffer S. terebinthifolius leaves against transient water
deficits. During the dry season S. terebinthifolius was able to
adjust instantaneous intrinsic WUE and maintain high leaf Ψ
in leaves expanded at the beginning of the wet season, whereas
the adjustment in instantaneous intrinsic WUE in native species occurred in leaves expanded under dry conditions.
Foliar N concentration is an important determinant of
growth and photosynthetic capacity, mainly because of the
large allocation of N to carboxylating enzymes (Field and
Mooney 1986, Reich et al. 1997). We found that net CO2 assimilation in the wet season increased linearly with increasing
leaf N concentration across four of the seven species studied
(M. polymorpha, D. sandwicensis, N. sandwicensis and
M. sandwicense) (Table 1), but S. terebinthifolius had the
highest photosynthetic rates relative to foliar N concentrations. Leaves of S. terebinthifolius had low LMA and most of
the foliar N may be allocated to photosynthetic enzymes rather
than to latex or structural components. Species that have relatively large amounts of leaf N compounds that are used for
non-photosynthetic activities may not fit within this positive
linear relationship between photosynthesis and foliar N, such
as the two latex-bearing species (N. polynesicum and P. sandwicensis) whose N concentrations were relatively high.
The combination of a seasonally dry environment and oligotrophic soils in Hawaiian dry forests may generate conflicting demands on limiting resources, resulting in a trade-off between PNUE and WUE (Field and Mooney 1983). The decrease in carbon assimilation associated with decreases in
stomatal conductance during the dry season would have the effect of reducing PNUE and increasing WUE. Based on δ13C as
a measure of integrated WUE, the invasive S. terebinthifolius
exhibited low WUE and high PNUE, whereas the native species showed no trade-off. In water-limited environments,
DeLucia and Schlesinger (1991) also observed that fast-growing plants had low integrated WUE (based on δ13C) and high
PNUE. However, conclusions about a trade-off between
PNUE and integrated WUE based on δ13C alone may not necessarily reflect a plant’s ability to adjust its physiological activity during the unfavorable season unless they are based on
the status of the plant when the leaves are expanded. When we
used the percent change in A/g from wet to dry season as an estimate of WUE during the unfavorable season, no trade-off between WUE and PNUE was apparent for any of the study species, including the invasive S. terebinthifolius.
Growth, photosynthesis and resource utilization
Although plants with higher photosynthetic capacity generally
exhibit higher growth rates, the relationship does not hold for
all species because of differences in the pattern of resource allocation (e.g., Givnish 1978, Poorter and Remkes 1990). We
observed a positive correlation between growth rate and photosynthetic rate, suggesting that the pattern of carbon allocation was similar in the studied species. During the wet season,
S. terebinthifolius had the highest growth rate and the highest
CO2 assimilation rate among the species studied.
Leaf mass per area (LMA) is usually inversely related to
growth rate (Lambers and Poorter 1992, Reich et al. 1997). A
low LMA may increase the capacity of a plant to assimilate
CO2 because more leaves are produced for a given mass of carbon invested in photosynthetic tissues. Low leaf construction
costs have been associated with high relative growth rates
(Lambers and Poorter 1992). In a survey of 64 species in Hawaii, a positive relationship was observed between LMA and
leaf construction costs measured by combustion of free ash
leaf samples (Baruch and Goldstein 1999). We found that,
across species, stem growth increased exponentially with decreasing LMA. Therefore, if the positive relationship between
LMA and cost of construction holds for tree species in Hawaiian dry forests, tree species with low LMA (lower leaf construction costs) will assimilate more CO2 per unit of carbon
invested in photosynthetic tissues than tree species with high
LMA. This increased efficiency could partially explain the
higher growth rates observed in species with thin leaves, particularly those of S. terebinthifolius (Lambers and Poorter
1992, Reich et al. 1997).
Not all species in a community have equal access to limiting
resources. Differential access to available resources may in-
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fluence a plant’s ecological performance (Goldstein and Sarmiento 1986). Myoporum sandwicense differed from the other
species in being spatially more isolated (7.8 m from its nearest
neighbors versus 2.5 m for the other species (Stratton et al.
2000b)) and having relatively high growth rates during both
the wet and dry seasons. This spatial isolation may allow
M. sandwicense trees access to a larger volume of soil water
during the dry season than trees of the other species, resulting
in year-round high net CO2 assimilation rates. Alternatively,
M. sandwicenses’s high water-use rates may competitively exclude other species from its root zone.
Invasive species and phenotypic plasticity
Several traits have been linked to the success of invasive species. For example, differences in reproductive efforts, seed
dispersal, seedling performance and susceptibility to herbivory and pathogens can all be important predictors of invasive
ability (Bazzaz 1986, Rejmanek 1996, Williamson and Fitter
1996, Pysek 1997). In cases where such life-history characteristics as growth form and overall reproductive potential are
similar between invasive and native species, successful invaders in seasonal environments usually exhibit higher rates of resource utilization when resources are available, and also
exhibit a greater ability to adjust their physiological performance during unfavorable periods. Schinus terebinthifolius
has many traits considered to be typical of successful invasive
species including rapid leaf expansion and a high growth rate
achieved at a relatively low cost (low LMA), high photosynthetic rates and high stomatal conductance during the wet season. Fischer and Turner (1978) hypothesized that, in dry
habitats, natural selection should favor plants with high WUE;
however, S. terebinthifolius, exhibited low WUE when soil
water was not limiting. High WUE can be a disadvantage in
environments with seasonal variation of soil water availability
(DeLucia and Heckathorn 1989). A combination of profligate
use of water and the ability to avoid water deficits was found
to be a successful combination of physiological characteristics
in certain water-limited environments (DeLucia et al. 1988).
An important factor in the success of invasive species is
phenotypic plasticity (Williams and Black 1994, Williams et
al. 1995). For example, the invasive grass Agropyron desertorum (Fisch.) Schult., showed greater plasticity in response to
herbivory and to soil nutrient availability than its native congener A. spichatum (Pursh) Scribn. & J. G. Sm. (Caldwell et
al. 1981). In a recent study of species from wet Hawaiian forests, invasive species exhibited a greater ability to adjust leaf
area ratios (the ratio of total leaf surface to plant dry weight)
and photosynthetic rates across a wide range of light environments than native species (Pattison et al. 1998). In our study,
S. terebinthifolius showed a striking ability to decrease
stomatal conductance, and therefore to reduce the rate of water
loss, during the dry season in leaves expanded during the wet
season. In contrast, N. sandwicensis, which also expanded the
majority of its leaves in the wet season, showed little adjustment of WUE or leaf water potential in the dry season. These
different responses to seasonal changes in soil water availabil-
1333
ity provide evidence that physiological plasticity is an important component in the success of invasive species (Baker
1974, Williams et al. 1995). Recently, Davis et al. (2000)
advanced the theory that fluctuation in resource availability is
the key factor controlling the rate of invasion by non-resident
species. The observed changes in physiological traits exhibited by S. terebinthifolius in response to seasonal fluctuations
in resource availability are consistent with this theory and can
account for its high rate of invasion in a seasonally dry environment.
In conclusion, S. terebinthifolius differed substantially from
co-occurring native dry forest tree species in several physiological traits considered to be characteristic of invasive species. Schinus terebinthifolius had high net CO2 assimilation
rates and was able to adjust its level of physiological activity
within a single cohort of leaves according to seasonal changes
in the abundance of soil water resources. This plasticity, in
combination with a low LMA and the maintenance of photosynthetic leaves and high leaf Ψs during the dry season, enabled S. terebinthifolius to direct relatively large amounts of
assimilate toward stem growth and leaf production.
Acknowledgments
Partial financial support was received from the U.S. Geological Survey, Biological Resources Division, Pacific Island Ecosystem Center,
Pacific Cooperative Studies Unit and the National Park Service, Hawaii Audubon Society, Ecology, Evolution and Conservation Biology Program at the University of Hawaii-Manoa and The Nature
Conservancy of Hawaii. We thank Darren Sandquist for earlier reviews of the manuscript.
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