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Ecology |
Department of Ecology and Evolutionary Biology, Rice University, Houston, Texas 77005 USA
Received for publication March 5, 2002. Accepted for publication August 27, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: acute defoliation • Chinese tallow tree • chronic defoliation • compensatory plant growth • Euphorbiaceae • exotic invader • herbivory tolerance • nitrogen fertilization • shade tolerance • Sapium sebiferum • woody encroachment
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Mack et al., 2000
; Pimentel et al., 2000
). Although deliberately introduced perennial woody species are among the least common invasive plants (Baker, 1974
; Reichard and Hamilton, 1997
), they are frequently the most aggressive invaders of natural habitats (Vitousek and Walker, 1989
; Schierenbeck, Mack, and Sharitz, 1994
; Fleischmann, 1997
; Richardson, 1998
). Sapium sebiferum [(L.) Roxb., Euphorbiaceae, Chinese tallow tree] is a major woody invader in the southeastern United States (Bruce, Cameron, and Harcombe, 1995
; Jubinsky and Anderson, 1996
). Once established, it aggressively displaces native plants and forms monotypic woodland thickets (Bruce et al., 1997
; Grace, 1998
).
Phenotypic plasticity and differences in resource acquisition abilities have been identified as fundamental traits contributing to the invasiveness of introduced plants (Bazzaz, 1986
; Dukes and Mooney, 1999
; Alpert, Bone, and Holzapfel, 2000
; Davis, Grime, and Thompson, 2000
). The rapid decomposition of Sapium litter makes available nitrogen concentrations under Sapium trees nearly double those beneath native prairie vegetation (Cameron and Spencer, 1989
), which creates nutrient feedbacks that potentially contribute to the invasion of coastal grasslands. Also, the ability to grow efficiently in a wide range of light conditions may partially explain Sapium's successful invasion of a variety of different habitats (Jones and McLeod, 1989
; Rogers and Siemann, 2002
). Sapium seedlings are capable of rapid growth in full sunlight and sustained, moderate growth under low light levels, where their growth rates are frequently higher than many native, shade-tolerant tree species (Jones and McLeod, 1989
, 1990
).
Different resource availabilities also affect herbivore selectivity and the ability of plants to respond to herbivores (Bazzaz et al., 1987
; Trumble, Kolodny-Hirsch, and Ting, 1993
; Stowe et al., 2000
; Lill and Marquis, 2001
). Sapium's success as an invader is frequently attributed to a lack of pests and pathogens (Scheld and Cowles, 1981
; Harcombe, Cameron, and Glumac, 1993
; Jubinsky and Anderson, 1996
; Bruce et al., 1997
), and its leaves purportedly contain secondary metabolites that maintain resistance to both native vertebrate and invertebrate herbivores (Russell, Schwartz, and Dollahite, 1969
; Cameron and Spencer, 1989
; Jubinsky and Anderson, 1996
). Repeated observations confirm that Sapium experiences very low levels of herbivory in its introduced range (Scheld and Cowles, 1981
; Siemann and Rogers, 2001
). Ecological theory holds that a trade-off exists between herbivory resistance (i.e., mechanisms that reduce the probability of defoliation) and herbivory tolerance (i.e., mechanisms that facilitate regrowth following defoliation) (van der Meijden, Wijn, and Verkaar, 1988
; Herms and Mattson, 1992
; Simms, 1992
; Fineblum and Rausher, 1995
). Thus, herbivory-resistant plants invest resources and energy that would otherwise be used for growth or reproduction into producing and maintaining chemical or physical herbivore deterrents, while herbivory-tolerant plants rapidly regrow following defoliation and compensate for mass lost to herbivore damage via high growth rates.
Because Sapium leaves are believed to possess costly anti-herbivore defenses we expected artificially damaged seedlings to show significant decreases in growth while competing for resources with native vegetation. We also proposed that decreased Sapium growth due to leaf damage could be partially compensated for by increasing light and soil nutrients because fertile conditions are known to reduce the negative effects of herbivores (Coley, Bryant, and Chapin, 1985
; Mashinski and Whitham, 1989
; Louda, Keeler, and Holt, 1990
; Hunter and Price, 1992
). To test these predictions, we conducted paired greenhouse and field experiments designed to assess the effects of different types of defoliation at different levels of light and nitrogen on Sapium seedlings grown in the presence of native coastal prairie.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Jubinsky and Anderson, 1996
). It is monecious and has insect-pollinated flowers from April through June (Bruce et al., 1997
). Fruits ripen from August to November, and seeds are dispersed by many bird species (Barrow et al., 2000
; Renne, Gauthreaux, and Gresham, 2000
). It is a deciduous tree that loses its leaves in autumn and has range limits largely determined by winter temperatures and aridity (Bruce et al., 1997
). Rapid growth, colorful fall foliage, abundant flowers, and seeds rich in oils have encouraged extensive planting of Sapium for ornamental purposes, biomass production, industrial oils, and a nectar crop (Scheld and Cowles, 1981
). It readily escapes cultivation throughout the southeastern United States, and Sapium invasions seriously threaten many native ecosystems, including endangered coastal prairies (Bruce, Cameron, and Harcombe, 1995
; Grace, 1998
; Barrileaux and Grace, 2000
). Once established, it is capable of aggressively displacing native plants and transforming diverse habitats into biotically depauperate woodland thickets (Bruce et al., 1997
; Grace, 1998
).
Greenhouse experiment
In December 1999, 48 clonal bunches of Schizachyrium scoparium were excavated from the University of Houston Coastal Center, a research area located approximately 50 km southeast of Houston, Texas, USA (see below for site description). The excavated bunches were reduced to fit into 9-L pots (24-cm diameter) and transferred to an unheated greenhouse at Rice University. After the grasses senesced in January 2000 (typical for Texas Gulf Coast graminoids), we clipped the vegetation 2.5 cm above the soil surface. This material was dried and weighed. In the same greenhouse, we germinated Sapium seeds collected from trees at the Coastal Center in November and December 1999. Following 1 mo of Schizachyrium regrowth, we planted a single newly sprouted Sapium seed into the middle of each clonal bunch on 18 February 2000. Sapium seedlings all had true leaves after less than 1 mo of growth in the pots. Focusing on early life-history stages has a greater capacity for revealing mechanisms that regulate community dynamics because young seedlings are frequently more susceptible to environmental stress than older plants (Fenner, 1987
; Meiners and Handel, 2000
).
We initiated the 15-wk experiment on 15 March 2000 and recorded initial Sapium stem heights, diameters, and leaf numbers. We measured stem height of each seedling from the soil surface to the tip of the apical meristem and measured stem diameter at the soil surface with a digital caliper. Each pot was randomly assigned a full-factorial treatment combination involving shade, nitrogen fertilization, and simulated leaf herbivory on the Sapium seedlings (Table 1). Plants in the shade treatment were placed under a black polypropylene shade cloth that intercepted approximately 87% photosynthetically active radiation present in the greenhouse as measured by weekly readings with a Decagon Accupar Linear Ceptometer (Decagon Devices, Pullman, Washington, USA). Unshaded plants received ambient greenhouse light that was reduced to 75% outdoor sunlight due to attenuation by glass panes. We rotated plants within each shade treatment frequently. Plants in nitrogen fertilization treatments received 14 g/m2 of nitrogen added as ammonium nitrate in weeks 1, 3, 5, 7, 9, 11, and 13 (2 g N/m2 per addition).
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; Karban and Baldwin, 1997
; Agrawal, 1998
). However, this type of simulated leaf herbivory can provide an adequate representation of the decreased leaf area and mass loss experienced by herbivore-damaged tree seedlings (Hendrix, 1988
; Marquis, 1992
; Stowe, 1998
; Tiffin and Inouye, 2000
).
Hole punches were randomly and independently assigned to leaves. If possible, we did not punch midveins to prevent unintended magnification of the damage, and new leaves near the top of each seedling were excluded to protect apical meristems and avoid affecting branching dynamics (Marquis, 1992
). Because partial herbivory rarely leads directly to the mortality of a seedling (Fenner, 1987
), two types of simulated leaf herbivory treatments were used to defoliate Sapium seedlings to assess which caused the greatest reduction in competitive ability (Hendrix, 1988
). The first treatment was a low-intensity, chronic defoliation (LCD; Table 1). We punched six leaf holes per seedling during weeks 4, 6, 8, 10, and 12 for a cumulative total of 30 leaf punches. Approximately 20% leaf area was removed initially, but as the seedlings grew larger, subsequent defoliations removed less area. The second simulated herbivory treatment was a high-intensity, acute defoliation (HAD) designed to simulate an outbreaking insect (Table 1). For the HAD treatment we punched 30 leaf holes in the Sapium seedlings during week 8. This constituted a mean of >60% estimated leaf area removed. Although the same number of leaf holes were punched for LCD and HAD treatments, the tempo and potential effect of the damage differed considerably.
Throughout the experiment, non-Schizachyrium plants (mostly forbs and sedges) that germinated in the pots were removed. In order to prevent uncontrolled background herbivory, we periodically sprayed esfenvalerate (tradename Asana XL, DuPont Agricultural Products, Wilmington, Delaware, USA) on the plants. We have conducted separate phytotoxicity tests and found no negative effects of this insecticide on Sapium or Schizachyrium plant mass (E. Siemann, unpublished data). All pots were watered daily or as needed.
At the end of 15 wk (105 d) we measured final Sapium stem heights, diameters, leaf numbers, and leaf area. Leaf area was estimated from the length and width of three leaves systematically selected near the top, middle, and bottom of each seedling. This measure strongly correlates with computerized leaf scans due to the obovate shape of Sapium leaves (W. E. Rogers, unpublished data). Sapium stems and Schizachyrium shoots were clipped at the soil base, Sapium leaves were removed from the stems, and roots were gently washed from the soil. Sapium and Schizachyrium roots were visually distinguishable and carefully separated. Sapium root growth did not reach the bottom of any pot; thus, none of the tree seedlings appeared to be growth-limited by rooting space. Leaves, stems, and roots of Sapium and shoots and roots of Schizachyrium were dried at 60°C for at least 72 h and weighed separately.
Field experiment
A companion field study was designed to complement the greenhouse study. This experiment was conducted in a Schizachyrium-dominated coastal prairie at the University of Houston Coastal Center that was last mowed in May 1999. The regional climate is semitropical with 1200-mm mean rainfall and a 250-d growing season (Scheld and Cowles, 1981
; Harcombe, Cameron, and Glumac, 1993
). Soils are Lake Charles clay (fine, montmorillonitic, thermic Typic Pelludert) containing a 40–60% clay content (Anonymous, 1988
). The annually mowed coastal grassland areas primarily consist of perennial grasses (75% of mass) with vegetation cover dominated by Schizachyrium scoparium (34%), Paspalum plicatum (10%), and Tripsacum dactyloides (6%) (Harcombe, Cameron, and Glumac, 1993
). A diverse assemblage of graminoids, perennial forbs, and shrubs comprise the remaining plant cover except unmowed or unburned areas are predominantly monospecific Sapium woodlands (Harcombe, Cameron, and Glumac, 1993
; Bruce, Cameron, and Harcombe, 1995
).
Sapium seeds were individually germinated in an unheated greenhouse in single-celled, 100-mL conetainers (Stuewe and Sons, Corvallis, Oregon, USA) containing surface soil collected from the Coastal Center. After growing in the greenhouse for approximately 1 mo, the seedlings were transferred outdoors, placed beneath a 50% shade cloth for 2 wk, and watered daily.
We established a grid of 1-m2 plots in the prairie and transplanted a Sapium seedling in the center of alternating plots so that all seedlings were a minimum of 2 m apart. A total of 48 Sapium seedlings were transplanted. The plots were watered periodically to minimize transplant mortality. One seedling died and was replaced the first week after transplanting. We initiated the 15-wk experiment on 17 May 2000, 2 wk after transplanting Sapium seedlings into the field, and recorded initial Sapium stem heights, diameters, and leaf numbers. Experimental treatments were analogous to the greenhouse experiment, but field contingencies required some changes in the manipulations (Table 1). In particular, rather than erecting shade cloths over plots in the field we manipulated light by pulling back the herbaceous prairie vegetation using wire tomato cages (S0). This increased light to the Sapium seedling by approximately 58.6% compared with the shaded conditions beneath the undisturbed prairie canopy (S1). Nitrogen additions were similar to the greenhouse experiment, except the ammonium nitrate was dissolved in approximately 8 L of water and applied equally to the entire 1-m2 plot. Control plots received equal amounts of water. Simulated herbivory treatments were administered in the same way as in the greenhouse experiment.
In order to minimize the effects of a prolonged drought in East Texas and improve comparisons with the daily watered greenhouse experiment, we erected sprinklers on site and watered the plots once weekly. Again, we periodically sprayed esfenvalerate on the vegetation to prevent uncontrolled background herbivory.
At the end of 15 wk (105 d) we measured final Sapium stem heights, diameters, leaf numbers, and leaf area. Sapium stems were clipped at the soil base, and leaves were clipped from stems. A 0.1-m2 frame was used to clip aboveground prairie vegetation in each plot. Leaves and stems of Sapium and clipped prairie mass were dried at 60°C for 72 h and weighed separately.
Data analyses
For both experiments, Sapium growth rates [ln(final measurement/initial measurement)] were calculated for stem height and stem diameter. New Sapium leaves added were calculated by subtracting final leaf numbers from initial leaf numbers. We examined the data for normality and used analysis of variance to compare among experimental treatments (StatView 5.0, SAS Institute, Cary, North Carolina, USA). Sapium seedlings that died in the greenhouse experiment were included as zeros for mass but excluded from growth rate analyses.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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At the end of 15 wk, Sapium height growth rate was significantly increased by nitrogen additions (F1,31 = 5.56; P = 0.025), but not affected by shade, simulated leaf herbivory, or any interactions among experimental variables (Fig. 1A). Sapium diameter growth rate was not significantly affected by any experimental variables (not shown). Only shade significantly increased the number of new Sapium leaves added (F1,31 = 6.11; P = 0.019; Fig. 2A) and mean leaf area (F1,31 = 22.09; P < 0.0001; Fig. 2B). Sapium shoot (leaves + stem) mass was not significantly affected by any experimental variables as main effects or in interaction, although there was a trend for additional nitrogen to increase shoot mass (F1,31 = 3.10; P = 0.087; Fig. 3A). Shade significantly decreased both Sapium root mass (F1,36 = 5.48; P = 0.025; Fig. 3B) and Sapium root : shoot mass ratio (F1,36 = 53.4; P < 0.0001). A significant nitrogen by herbivory interaction also revealed that simulated herbivory increased Sapium root : shoot mass without nitrogen, but simulated herbivory decreased root : shoot mass with additional nitrogen (F2,36 = 5.78; P = 0.007). Shade significantly decreased Schizachyrium shoot mass (F1,36 = 11.38; P = 0.002; Fig. 3C), root mass (F1,36 = 11.66; P = 0.002; Fig. 3D), and root : shoot mass ratio (F1,36 = 9.41; P = 0.004). The ratio of Sapium mass : total plant mass (Sapium + Schizachyrium), a measure of post-invasion success, was significantly increased by nitrogen additions (Table 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Jubinsky and Anderson, 1996
; Bruce et al., 1997
; Siemann and Rogers, 2001
). However, while previous assertions regarding the lack of herbivore regulation imply that herbivores are deterred by costly herbivory resistance (Russell, Schwartz, and Dollahite, 1969
; Cameron and Spencer, 1989
; Jubinsky and Anderson, 1996
), our current studies suggest that herbivory tolerance, expressed as phenotypic plasticity and rapid compensatory regrowth, is an additional explanation for Sapium's success. Phenotypic plasticity has been identified as a fundamental trait contributing to the invasiveness of many non-native plants (Bazzaz, 1986
; Alpert, Bone, and Holzapfel, 2000
), hence Sapium's resilience is likely a key factor in its success.
There was marked similarity between results for the greenhouse and field experiments. Although there were some statistical differences, the majority of measured variables in both studies observed commensurate responses to experimental treatments. For instance, Sapium seedlings grew quite well without supplemental nutrients, but nitrogen fertilization significantly increased height growth rate in both greenhouse and field studies. Similarly, additional nitrogen significantly increased Sapium shoot mass in the field experiment and tended to increase shoot mass in the greenhouse study. Nitrogen did not affect the number of Sapium leaves or mean leaf surface area in the greenhouse study. However, in the field experiment nitrogen fertilization significantly decreased the number of Sapium leaves while significantly increasing mean leaf surface area possibly suggesting an allocation trade-off. Our study also revealed that elevated nitrogen levels in both experiments significantly increased Sapium mass relative to grassland vegetation, thereby suggesting coastal prairie sites are more susceptible to Sapium invasion with increased fertility. Davis, Grime, and Thompson (2000)
provide an alternative explanation for the increased severity of invasion caused by additional nitrogen. Their theory suggests an invader need not be a better competitor for resources, but rather an increase in resource availability causes a temporary reduction in competitive interactions and provides opportunities for new species to become established (Davis, Grime, and Thompson, 2000
; Davis and Pelsor, 2001
). Additional studies are underway to determine the role resource fluctuations play in Sapium invasions.
Experimental light manipulations in the field experiment did not significantly affect any aspect of Sapium growth. Sapium seedlings grew equally well beneath the undisturbed prairie vegetation and with canopy tiebacks that increased light availability. Other research has shown that Sapium grows vigorously in a variety of light environments (Jones and McLeod, 1989
, 1990
; Rogers and Siemann, 2002
). However, markedly lower light levels beneath the greenhouse shade cloth significantly affected both Sapium and Schizachyrium growth. Shade significantly increased both number and mean surface area of Sapium leaves in the greenhouse study. Accordingly, increased shade decreased Sapium root mass and root : shoot mass. Increased shade also decreased Schizachyrium shoot mass, root mass, and root : shoot mass.
While Sapium's various responses to different resource conditions provide interesting new insights into its competitive ability, the most striking result from these combined studies is the absence of any appreciable effects of either defoliation treatment on Sapium growth. Despite the removal of considerable leaf area and mass, neither low-intensity, chronic defoliation nor high-intensity, acute defoliation had any statistically significant effects on Sapium height or diameter growth rates, new leaves added, average leaf surface area, or any measure of shoot or root mass. Sapium fully compensated for both types of simulated leaf herbivory in all conditions.
Previous studies have shown Sapium is able to tolerate different levels of chronic leaf herbivory when grown without competition for resources (Rogers et al., 2000
; Rogers and Siemann, 2002
). However, we predicted that Sapium would not be able to fully compensate for lost leaf tissue while concurrently competing with native vegetation for limited resources, particularly if defoliation was severe (e.g., Coley, Bryant, and Chapin, 1985
; Maschinski and Whitham, 1989
; Louda, Keeler, and Holt, 1990
). This was not the case. Rather, these experiments revealed that Sapium is remarkably tolerant of intense defoliation levels and able to fully compensate for lost leaf mass under a variety of resource levels in competitive conditions. The morphological plasticity of Sapium is exhibited in the greenhouse study, where root : shoot mass was significantly affected by a nitrogen and herbivory interaction. In these conditions, Sapium invested more mass in roots in the absence of herbivory, but defoliation shifted allocation toward rebuilding lost leaf mass with added soil nitrogen. Regardless of its effect on allocation patterns, defoliation did not negatively impact Sapium growth in any resource condition.
In a previous study, Siemann and Rogers (2001)
demonstrated that the increased competitive ability and invasive success of introduced Sapium is likely due to a genetically determined reallocation away from costly anti-herbivore defenses toward increased rapid growth and reproduction. In other words, in a relatively brief period Sapium has evolved from an herbivore-resistant into a rapidly growing, herbivore-tolerant tree. Further, because it does not have an appreciable herbivore load like other herbivore-tolerant native plants, it is not experiencing the typical trade-off between these strategies (Herms and Mattson, 1992
). Other researchers have suggested that an isolated population of introduced plants may lose adaptations to herbivory over time (Blossey and Nötzold, 1995
; Daehler and Strong, 1997
; Mack et al., 2000
; Willis, Memmott, and Forrester, 2000
; Mooney and Cleland, 2001
). This explanation for the success of Sapium as an exotic invader remains consistent with our current results and suggests that the ability to thrive in a variety of environmental conditions, low herbivory damage, and rapid compensatory regrowth are all likely to contribute to Sapium's invasion of the endangered coastal prairie ecosystem and will complicate the development of a management strategy for controlling this aggressive invader.
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FOOTNOTES |
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2 Author for reprint requests (wer{at}rice.edu
)
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