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Ecology |
Lamont-Doherty Earth Observatory, Department of Earth and Environmental Sciences, Columbia University, Palisades, New York 10964 USA
Received for publication November 16, 2000. Accepted for publication May 10, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: abundance • construction cost • energetics • invasive species • Lythraceae • Lythrum salicaria
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), such as fire regimes, nutrient cycling, and energy budgets (Mack et al., 2000)
. A recent Florida study, for example, concluded 44–77% of invasive plants studied in that state potentially altered plant communities and/or ecosystem geomorphological, hydrological, and biogeochemical processes (Gordon, 1998
). Given the many possible environmental and economic impacts of plant invasions, it is important to increase our understanding of the physiological and environmental factors that influence the invasive potential of plant species to facilitate preventative and remediation efforts.
Lythrum salicaria (purple loosestrife), a herbaceous perennial introduced from Europe and Asia, is thought to have arrived in North America during the early 1800s (Thompson, 1991
). Since its introduction, this species has become particularly widespread across wetland, marshy, and riparian habitats in the northern tier states and provinces of North America. The spread of this species, along with that of other invasive plants, has altered the vegetation of many North American wetlands (Galatowitsch, Anderson, and Ascher, 1999
), resulting in the decline of species diversity and the extinction of some rare species (Moore and Keddy, 1989
). Invasions of L. salicaria, in particular, have been linked with the displacement of native plant species, including Typha spp. (cattail) (Mal, Louvett-Doust, and Louvett-Doust, 1997
; Mullin, 1998
) and Scirpus spp. (bulrush) (Mullin, 1998
), as well as changes in ecosystem nitrogen cycling (Otto et al., 1999
), sediment chemistry (Templer, Findlay, and Wigand, 1998
), detrital input (Emery and Perry, 1996
; Grout, Levings, and Richardson, 1997
), and avian diversity (Whitt, Prince, and Cox, 1999
).
The increasing abundance of L. salicaria suggests a high competitive advantage over many co-occurring native plants, yet this competitive success is not completely understood. While prolific seed production, high germination rates, and easy dispersal of its small seeds have been hypothesized to facilitate the spread of this species (Mal et al., 1992
; Mullin, 1998
), the continued success of L. salicaria also depends on its successful growth following establishment. Though it has been widely hypothesized that a lack of natural herbivores has given this species (Thompson, Stuckey, and Thompson, 1987
; Rendall, 1989
; Galatowitsch, Anderson, and Ascher, 1999
) and other invasive species (Rejmánek, 1996;
Mack et al., 2000
) a competitive growth advantage over co-occurring native species, recent studies have indicated the vigor of L. salicaria cannot be explained entirely by either a lack of herbivory (Rachich and Reader, 1999
; Willis and Blossey, 1999
) or a reduced need for herbivory defense mechanisms (Willis, Thomas, and Lawton, 1999
).
Habitat disturbance also has been cited as a factor influencing invasions of L. salicaria (Thompson, Stuckey, and Thompson, 1987
; Mullin, 1998
), and collectively, many studies have indicated there are positive correlations between disturbance and other species invasions in environments ranging from wetlands (e.g., Detenbeck et al., 1999
) to grasslands (e.g., Rose, Platt, and Frampton, 1995
) to roadsides (e.g., Dietz, Fischer, and Schmid, 1999
). Based on these shared findings, it seems reasonable to conclude environmental disturbance does influence the invasiveness of L. salicaria and numerous other plant species; ecosystem modeling results support this conclusion (Zalba et al., 2000)
. Yet the invasive species and their neighboring noninvasive species sharing these disturbed environments are subject to the same environmental conditions, regardless of the nature of the disturbance. Some components of plant physiology and/or morphology may, therefore, also influence the invasive potential of plant species by enabling them to establish populations capable of outcompeting other species in disturbed environments.
As a quantifiable measurement of the energy invested by a plant to construct biomass, construction cost (CC) can be related to both resource-use efficiency (Williams et al., 1987
; Griffin, 1994
) and growth rates (Lambers and Poorter, 1992
; Poorter and Bergkotte, 1992
; Griffin, Thomas, and Strain, 1993
; Griffin, 1994
; Poorter and Villar, 1997
), with high CC typically being associated with slow-growing species (Lambers and Poorter, 1992
; Poorter and Bergkotte, 1992
; Griffin, Thomas, and Strain, 1993
; Griffin, 1994
; Poorter and Villar, 1997
). Since every plant species has a resource requirement below which it cannot perform the functions necessary to grow and spread (Tilman, 1982
), it has been hypothesized that a relatively low resource requirement could increase the competitive ability of plant species (Tilman, 1999
). As it relates to CC, the resource requirement of a species could be influenced by the amount of energy required to perform growth functions, such that a plant requiring less energy to construct biomass may require less resources to generate that energy than a plant with more energetically expensive functions. Since a quantitative understanding of how different plants gain and allocate resources likely will facilitate predictions of their success in any given environment (Mooney, 1972
) and plant energetics can be related to resource use, we consider CC as a general approach to evaluating invasive potential.
Researchers who recently studied 30 invasive and 34 native species in Hawaii found overall lower leaf CC for the invasive vs. native species (Baruch and Goldstein, 1999
). Comparing native and invasive C4 grasses in Venezuela, another study concluded a similar occurrence of low leaf CC in invasive plants when compared to their native counterparts (Baruch and Gomez, 1996
). Given these recent findings and the association of CC with resource-use efficiency and growth rates, we hypothesize the invasiveness of L. salicaria over co-occurring native plants may be facilitated by relatively low energy requirements for leaf construction. Thus, L. salicaria may produce more photosynthetic leaf surface area and/or grow faster with lower energy expense to outcompete co-occurring native species. We investigated our hypothesis by comparing the leaf CC and related resource characteristics of field-collected L. salicaria and the five most abundant co-occurring native species along disturbed, dammed areas of three man-made ponds located in the Black Rock Forest, Cornwall, New York, USA.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), stems rising from the same rootstock were counted as one individual plant. Species relative abundance levels were determined on a density basis as the total number of individuals of each species divided by the total number of quadrants (in individuals per square meter). We have chosen to use this measure of abundance because it attests to the growth success as well as the establishment success of species.
Young, fully expanded sun leaves from one observably healthy individual of L. salicaria and the five most abundant co-occurring native species were collected from every plot where the respective species was present. To ensure enough leaf material was obtained for our analyses, 
50 cm2 of leaf material was collected from each individual plant. Leaves were processed through a portable area meter (Model LI-3000A, LI-COR, Lincoln, Nebraska, USA) and then dried in a 60°C oven (Model 20 GC, Quincy Lab, Chicago, Illinois, USA) for 48 h and weighed to determine leaf mass per unit area (LMA) (in grams per square meter) for each individual. Following this measurement, all dried leaves were ground into a fine powder using a ball mill (Cianflone Scientific Instruments, Pittsburgh, Pennsylvania, USA) and stored with a desiccant to maintain dryness for construction cost analysis.
Leaf energy and resource investment
Organic nitrogen (N) (in grams per gram leaf dry mass) and carbon (C) (in grams per gram leaf dry mass) content of two 1–2 mg samples of leaf powder from each individual were determined using an elemental analyzer (ANCA-SL, ANCA, Crewe, UK). The duplicate samples for each individual were averaged. To calculate N and C per unit leaf area (in grams per square meter), these values were multiplied by the LMA for each individual.
Ash content (Ash) (in grams per gram leaf dry mass) was measured for each individual by burning preweighed leaf powder samples in a 400°C muffle furnace (Model 51844, Lindberg, Watertown, Wisconsin, USA) for 6 h to obtain ash and then dividing the ash mass by the sample mass. To obtain ash-free heats of combustion (HC) (in kilojoules per gram leaf dry mass), three 6–20 mg pellets were pressed of the leaf powder from each individual. The pellets were combusted using a modified Phillipson microbomb calorimeter (Phillipson, 1964
) (Gentry Instruments, Aiken, South Carolina, USA) calibrated with 6–20 mg benzoic acid standards of known energy values. The HC values obtained for the triplicate pellets for each plant were then averaged.
The simplest measurement of CC involves quantifying the amount of resources allocated to a given vegetative structure's formation, which can be estimated accurately from measurements of HC, Ash, and N content (Williams et al., 1987
). The following equation (from Williams et al., 1987
) was used to calculate CC as the amount of glucose required to synthesize plant biomass (equivalent to grams glucose per gram leaf dry mass): CC = [(0.06968
HC – 0.065)(1 – Ash) + 7.5(kN/14.0067)](1/EG), where k is the oxidation state of the nitrogen substrate and EG is the growth efficiency. In terms of its deviation from 100%, EG represents the fraction of cost required to provide reductant that is not incorporated into biomass (Penning de Vries, Brunsting, and van Laar, 1974
). Penning de Vries, Brunsting, and van Laar (1974)
calculated EG as 0.87. Since k is +5 for nitrate and –3 for ammonium and the form of N was not known in our samples, CC for each individual was calculated twice, once with k = 5 and once with k = –3, providing a range of possible N substrate-dependent CC values. To calculate leaf CC per unit leaf area (equivalent to grams glucose per square meter), these values were multiplied by the LMA for each individual. Species means were obtained for all measured factors by averaging the values of all individuals for each species.
Statistical analyses
After homogeneity of sample variances was verified using a Levene statistic test, a one-way analysis of variance (ANOVA) model adjusted for unbalanced experimental design (in which species was defined as the fixed independent variable) was used to compare means between species for all measured leaf variables (SPSS for Windows, release 7.5.1, 1996, SPSS, Chicago, Illinois, USA). Mean values were considered significantly different if P 
0.05. When ANOVA results were significant, least significant difference (LSD) post-hoc analysis was performed to further compare species means. Linear regressions were made to determine the relationship between mean leaf CC and other leaf variables for all species. The average of the leaf CC values considering ammonium and nitrate each as the primary source of leaf N were used in regression analysis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Area-based leaf CC estimates provide information on processes influenced by leaf surface area, such as those driven by light interception or those limited by diffusion to the plant surface (Griffin, 1994
). The stronger association of species relative abundance with area-based leaf CC than mass-based leaf CC in this study suggests processes dependent on leaf surface area may influence competitive success of these species to some extent. In fact, we found LMA to be slightly more strongly correlated with species relative abundance than is area-based leaf CC in this study (r2 = 0.81). However, because LMA is not a cause but rather the result of a change in physiology, while leaf CC may be considered a more mechanistic approach to understanding plant growth, we emphasize leaf CC and related factors.
Here, a positive correlation between LMA and area-based mean leaf CC (Fig. 4A) illustrates the association of leaf CC and leaf thickness or cell density. Typically, plants with a high LMA have been found to contain more lignin (Austin and Vitousek, 1998
; Groeneveld, Bergkotte, and Lambers, 1998
) and cell-wall components (Groeneveld, Bergkotte, and Lambers, 1998
), which tend to be energetically expensive. In our study, this association seemed characteristic of two of the less abundant species, A. syriaca and Solidago graminifolia, which exhibited relatively high mean LMA values associated with both high mass- and area-based leaf CC, while both P. quinquefolia and L. salicara exhibited the opposite characteristics.
The relatively low mean LMA of the most abundant sampled species in this study (Table 2) could indicate these species have a higher capacity for light interception and carbon assimilation with a limited amount of energetic expense, while relatively higher mean LMA could have the opposite effect in co-occurring species. Though photosynthesis was not measured in our study, researchers who examined photosynthesis of invasive plants with lower LMA and leaf CC than co-occurring native plants concluded the invasive species had overall higher average rates of mass-based photosynthesis (Baruch and Goldstein, 1999
).
Nitrogen, which is contained in many of the more expensive biochemical plant compounds (Penning de Vries, Brunsting, and van Laar, 1974
) such as proteins and amino acids (Williams et al., 1987
), typically exhibits a positive correlation with leaf CC (Miller, Eddleman, and Kramer, 1990
; Sims and Pearcy, 1991
; Griffin, Thomas, and Strain, 1993
; Griffin, Winner, and Strain, 1996
). The relatively high mass-based leaf N and low mass-based leaf CC in both L. salicaria and P. quinquefolia in this study suggests these species have a low energetic expense per unit N, which could increase photosynthetic capacity at minimal cost. Yet the strong positive correlation between area-based leaf N and CC (Fig. 4C) reflects the influence of interspecific differences in LMA. Like area-based leaf N, leaf C also seemed to be influenced by LMA (Fig. 4B). Relating both N and C content, the significantly low leaf C : N of L. salicaria could indicate reduced herbivory defense in the form of low amounts of structural carbon compounds, such as cellulose and lignin (Herms and Mattson, 1992
), which have an energetic cost.
In L. salicaria, low leaf CC may be indicative of high resource-use efficiency and growth rates, both of which could facilitate its invasiveness. As it correlates with species abundance in this study, leaf CC could provide a useful evaluation of invasive potential that may be applicable in other settings. While past research has suggested there may be little interspecific variation in this factor (e.g., Merino, 1987
; Chapin, 1989
; Williams, Field, and Mooney, 1989
), a more recent review has found a twofold range in mass-based leaf CC and an even greater range in area-based leaf CC between species (Griffin, 1994
). Our findings, while contributing only a small piece to the complex puzzle of species invasions, support those of a very limited number of other studies examining leaf CC and species invasiveness (e.g., Baruch and Gomez, 1996
; Baruch and Goldstein, 1999
).
While more specific physiological and morphological characteristics may contribute to the relative competitive ability of a species, it often is difficult to draw conclusions regarding the influence of these specific characteristics on invasive potential due to a lack of commonality. For example, while some invasive species may have high seed production or the ability to fix nitrogen, other invasive species may not share these characteristics. However, since every growth strategy has an energy consequence, energy can be considered a basic unit of comparison between organisms (Griffin, 1994
). As such, CC measurements reflect specific growth strategies, while allowing for a more general comparison of resource-use efficiency between species. We propose examining leaf CC of native and invasive species in other settings to further evaluate the application of this factor for assessing invasive potential. Furthermore, we suggest evaluating CC measurements for other plant structures, such as roots, stems, and seeds, to gain insight into patterns of energy use and resource allocation within invasive and co-occurring native plants.
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FOOTNOTES |
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2 Author for reprint requests (Lamont-Doherty Earth Observatory, Route 9W, Palisades New York 10964 USA; jenn{at}ldeo.columbia.edu
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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= Parthenocissus quinquefolia; 
= Lythrum salicaria; 
= Erigeron philadelphicus; 
= Spirea latifolia; 
= Solidago graminifolia. Error bars represent 1 SE of the mean