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0 University of Louisiana-Lafayette, Biology Department, Lafayette, Louisiana 70504 USA; and United States Geological Survey-National Wetlands Research Center, 700 Cajundome Boulevard, Lafayette, Louisiana 70506 USA
Received for publication June 8, 1999. Accepted for publication October 11, 1999.
ABSTRACT
The introduced tree Sapium sebiferum (Euphorbiaceae) is considered a serious threat to the preservation of the coastal prairie region of Louisiana and Texas, although it is currently uncommon in the western part of the region. The objective of this study was to evaluate the potential effects of location, soils, and available moisture on the growth and survival of S. sebiferum in coastal prairie. In a field experiment, S. sebiferum mortality was significantly greater at a western site than at central and eastern sites. The greatest mortality and least growth of surviving plants occurred on a soil from the western region, regardless of site. A greenhouse study also found that S. sebiferum growth was lowest on the western soil. Watering frequency significantly affected S. sebiferum growth, except on the western soil. Sapium sebiferum growth responded to both nitrogen and phosphorus additions for all soils. Soil analyses revealed the highest sand, sodium, and phosphorus contents, and much higher electrical conductivity in the western soil. It is concluded that the soil examined from the western region is unfavorable for S. sebiferum growth, though not to the extent to preclude S. sebiferum completely. Evidence suggests that soil salinity may be the primary cause of the poor S. sebiferum growth at the western site.
Key Words: Chinese tallowtree • coastal prairie • Euphorbiaceae • invasions • moisture effects • salinity • Sapium sebiferum • soil effects
Sapium sebiferum (L.) Roxb. (also known as Chinese tallowtree) is an exotic, invasive species that is a serious threat to the preservation of the coastal prairie ecosystem (Grace, 1998
), which occurs along the Gulf of Mexico coast from south-central Louisiana to southern Texas. Within coastal prairie there exists a complex east-west gradient of conditions in rainfall, potential evapotranspiration, and soil properties (Smeins, Diamond, and Hanselka, 1989
). A humid climate and high clay content soils characterize the eastern portion, while a semiarid climate, very high potential evapotranspiration, and sandy soils are prevalent in the western portion (Johnston, 1963
; Diamond and Smeins, 1984
; Smeins, Diamond, and Hanselka, 1989
). Less than 1% of the original coastal prairie vegetation remains due to agricultural and urban development, and the remaining tracts are at considerable risk of being replaced by S. sebiferum woodlands (Diamond and Smeins, 1988
; Allen and Vidrine, 1989
; Smeins, Diamond, and Hanselka, 1989
).
Sapium sebiferum, imported from subtropical China, has become naturalized across the southeastern United States, including the coastal prairie region, since its introduction in 1772 (Schoepf, 1911
; Bell, 1966
; Scheld and Cowles, 1981
; Glumac and Cowles, 1989
; Jubinsky, 1993
; Bruce et al., 1997
). It exhibits many traits associated with good invaders such as rapid growth, high rates of reproduction (both vegetatively and by seed), long-term viability of seeds, and the ability to tolerate a wide range of soil and climate conditions (Lin et al., 1958
; Scheld and Cowles, 1981
; Tanimoto, 1981
; Jubinsky, 1993
; Pianka, 1994
). Sapium sebiferum also appears to be tolerant of short-duration saltwater flooding, continuous freshwater flooding, and shading to as little as 5% of full sunlight (Jones and McLeod, 1989, 1990
; Jones and Sharitz, 1990
; Conner and Askew, 1993
). Evidence indicates that invasion first occurs in areas of high soil moisture, whereas drier regions are invaded at a slower rate (Hsu, 1928
; Jamieson and McKinney, 1938
; Lin et al., 1958
; Khan, Khan, and Malik, 1973
; Scheld and Cowles, 1981
; Helm et al., 1991
; Kuldeep et al., 1993
). The primary factor limiting its range appears to be temperature, specifically freezing (Lin et al., 1958
; National Academy of Sciences, 1983
; Bruce et al., 1997
). The range of S. sebiferum is also limited by extremely arid conditions, although it is considered to be relatively drought tolerant, especially on clay soils (Bruce, 1993
). Salinity is another factor potentially limiting the range of S. sebiferum (Tsing, Yi-hsiung, and Wan-li, 1956
; Conner, 1994
).
Sapium sebiferum is able to tolerate the periods of drought and fire associated with the coastal prairie ecosystem, allowing it to invade and alter succession in grass-dominated communities, even in the absence of disturbance (Callaway and Davis, 1993
). Sapium sebiferum exhibits the ability to reduce fuel loads and prevent the spread of fires that suppress woody vegetation and sustain prairie ecosystems through shading and the rapid decay of its leaves (Cameron and Spencer, 1989
). Typically, when woody species invade, S. sebiferum quickly becomes dominant, creating a nearly monospecific S. sebiferum woodland within 10 yr of invasion (Bruce, 1993
; Bruce, Cameron, and Harcombe, 1995
; Neyland and Meyer, 1997
). For these reasons, S. sebiferum constitutes perhaps the single greatest threat to the continued existence of coastal prairie (Grace, 1998
).
At present, S. sebiferum exhibits a differential distribution with a large extent of invasion in the eastern and central regions of the coastal prairie and little invasion in the western end. It is unknown at the present time whether this pattern of invasion by S. sebiferum reflects differential growth conditions or simply the history of invasion. The objective of this study was to gain insight into the factors controlling the distribution of S. sebiferum within the coastal prairie, specifically the effects of soils and moisture regime on growth and survival. To achieve this objective, three experiments were conducted: (1) a field experiment designed to examine the effects of soils and location, (2) a greenhouse experiment designed to study the interactive effects of watering regime and soils, and (3) a greenhouse fertilization study designed to determine the degree of nitrogen and phosphorus limitation for S. sebiferum growing in different soils.
MATERIALS AND METHODS
The conditions investigated in this study were chosen to represent the gradient in soil and moisture conditions found across the coastal prairie region. Three study sites were selected: the Lacassine National Wildlife Refuge in Louisiana, the Brazoria National Wildlife Refuge in southeastern Texas, and the Aransas National Wildlife Refuge in south-central Texas (Fig. 1). The Lacassine site was selected to represent the high clay content, wet end of the coastal prairie gradient; the Brazoria site to represent moderate clay content, moderate moisture conditions; and the Aransas site to represent low clay content, dry areas of the gradient. Soils for all experiments were collected from Lacassine, Brazoria, and Aransas National Wildlife Refuges to represent this gradient. Soil samples from a site were selected from the most common soil type at each site.
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). The Edna and Aris soils typically occur together as the Edna-Aris complex. The Aris soil occurs in the complex on convex knolls and within the circular mima mounds characteristic of the coastal prairie, whereas the Edna soil is restricted to the flats surrounding knolls and mounds. The Morey soil was collected from the eastern portion of the coastal prairie, and the Aris, Edna, and Lake Charles soils were obtained from the central portion. The Mustang soil represented the western portion of the prairie. All soil collections were made from the "A" horizon of each respective soil and were homogenized for uniformity prior to analysis and allocation to containers.
Sapium sebiferum seeds were collected from a provenance (Zobel and Talbert, 1991
) of less than ten trees in an area of 1.6 km2 at the Brazoria National Wildlife Refuge. Seeds were germinated in the spring of 1996 in the greenhouse in 3 cm diameter Ropak® Multi-Pots (Stuewe & Sons, Inc., Corvallis, Oregon, USA) after being stratified according to the methods of Bonner (1974)
. Seedlings were watered daily and fertilized periodically with a water-soluble fertilizer (Miracle GroTM 15-30-15, Sterns, Inc., Port Washington, New York, USA) until transplanting into experimental treatments. The field and main greenhouse experiments used S. sebiferum seedlings of uniform size in the range of 4–6 cm initial height.
Field experiment
By using a three by three factorial experiment with ten replicates, the field study examined the effects of soils and study area on seedling growth and survival. The study was conducted during the 1996 growing season at the Lacassine, Brazoria, and Aransas National Wildlife Refuges, which represent the eastern, central, and western portions of the coastal prairie, respectively. Three soils, one from each region of the prairie were used in the study: the Morey silt loam (eastern), the Edna sandy loam (central-intermound), and the Mustang sand (western). The experiment was conducted using a split-plot design with study areas representing the whole plot units and containers of the three soils representing the subplots within each whole plot.
The experiment used the phytometer concept, with pregerminated S. sebiferum seedlings being grown in 19-L plastic containers filled with each of the three field soils. Containers were placed into the soil at each site, with the rim of each pot at ground level, in order to simulate natural runoff patterns. Seedlings were transplanted into containers during the period 22–25 May 1996. Competition of S. sebiferum with other plant species in containers was controlled by physical removal of competing vegetation. Additionally, 39-m2 exclosures at field sites, 1.2 m in height with a 5 by 10 cm mesh size, were employed to prevent damage from animal disturbance or herbivory.
Growth and survival data for the S. sebiferum seedlings, including plant height, basal diameter, and number of leaves, were collected both initially and during harvest. The experiment was harvested 1 mo after planting during the period between 25 June and 3 July 1996. The duration of the experiment was shortened due to animal disturbance, which occurred following the first monthly data collection. The data were examined for homogeneity and normality of residuals and then normalized to meet parametric assumptions using a linear ranks transformation. The General Linear Model (GLM) ANOVA and Tukey's HSD multiple comparisons procedures were then performed using SAS (SAS, 1989
) with 
= 0.05. Survival analysis was performed using a categorical model procedure and contrast analysis.
Greenhouse experiment
A greenhouse study was performed to investigate the interactive effects of soils and watering regime on S. sebiferum seedlings using a five by five factorial design with six replicates. In this experiment, five soils were used including the same three from the field experiment plus two additional soils, the Aris fine sandy loam (central-mound) and the Lake Charles clay (central-clay), both from the central site, Brazoria. Sapium sebiferum seedlings were transplanted into each of the five soils in identical 19-L plastic containers on 13 July 1996. Watering regime was determined by the frequency of watering. Five watering frequencies were employed consisting of daily, semiweekly, weekly, every 2 wk, and monthly watering. At each watering, soils were watered to saturation. An additional treatment, using the Morey silt loam (eastern) soil with a daily watering frequency, was included in 38-L plastic containers (twice the volume of the other containers) to determine whether container size limited plant growth in this study (Hanson, Dixon, and Dickson, 1987
; Beeson, 1993
; Oddiraju et al., 1994
). Competition between S. sebiferum and other plant species in containers was controlled by physical removal.
Plant height, basal diameter, and survival were monitored initially and every 2 wk during the experiment. All plants were harvested after 3 mo on 21 October 1996, oven dried at 80°C for 72 h, and total, leaf, stem, and root masses were determined. The data were examined for homogeneity and normality of residuals. Collected data were normalized to meet parametric assumptions by using a linear ranks transformation and analyzed with the GLM MANOVA procedure and Tukey's HSD multiple comparisons analysis using SAS (SAS, 1989
) and = 0.05, to determine whether soil, watering regime, or an interaction of the two significantly affected plant growth.
Fertilization experiment
In the fertilization experiment, conducted during the 1997 growing season, the five soils were investigated to determine whether any were limited in nitrogen or phosphorus for S. sebiferum growth. The design consisted of a randomized complete block with six replicates as a five by three factorial experiment. The fertilization study used uniform field-collected seedlings from the Brazoria National Wildlife Refuge, ~10 cm in height, because of poor germination rates in the 1997 season. The addition of nitrogen at 60 mg/kg of soil, phosphorus at 60 mg/kg of soil, and a control formed the fertilization treatments (Duryea and Landis, 1984
).
Collected seedlings were planted in 90, 100-mL plastic containers on 17 June 1997 and placed in the greenhouse. Initial plant height data were collected, and height growth was monitored at 10-d intervals. After 45 d, all seedlings were harvested, oven dried at 80°C for 72 h, and total, leaf, stem, and root biomasses determined. All data were examined for homogeneity and normality of residuals. All data were analyzed with the GLM MANOVA procedure and Tukey's HSD multiple comparisons analysis using SAS (SAS, 1989
) and = 0.05, to determine whether any of the soils used in the research were resource limited due to nitrogen or phosphorus.
Soil analyses
Five samples from each field soil were analyzed for texture, bulk density, pH (in water), cation exchange capacity, and extractable nutrient concentrations. Extractable nutrients were determined using Mehlich-1 extraction and Inductively Coupled Plasma Spectrography, including phosphorus, potassium, calcium, magnesium, zinc, and sodium (Mehlich, 1953
; Baker and Shur, 1982
). Total soil carbon and nitrogen concentrations were determined using a Leeman Labs CE-440 C-H-N elemental analyzer (Leeman Labs, Inc., Lowell, Massachusetts, USA). Additionally, electrical conductivity was determined for all soils using a YSI Model 75 handheld conductivity probe (YSI, Inc., Yellow Springs, Ohio, USA).
RESULTS
Field experiment
Site and soil significantly affected planted S. sebiferum seedling mortality, with no significant interaction (Table 1). Across all soils, S. sebiferum mortality was significantly greater at the western site (37%) compared to the central and eastern sites (20%). Across all sites, mortality was 73% in the western soil, while mortalities were 3% for the central soil and 0% for the eastern soil.
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The results presented in this study clearly show that the growth of Sapium sebiferum is strongly affected by differences in soil characteristics within the coastal prairie. In the field experiment, mortality was greater and height of survivors lower for seedlings grown in the western soil. Effects of soils on mortality were particularly strong. In field conditions, seedlings suffered 73% mortality when grown on the western soil compared to only 3 and 0% mortality when grown on central and eastern soils, respectively. Effects of soil on plant height were also dramatic, with plants grown in the western soil under field conditions producing <20% of the height of plants grown in central or eastern soils. Greenhouse studies using a greater number of soils and more controlled conditions confirmed that the western soil supported substantially less growth for S. sebiferum seedlings (Fig. 4). Thus, all available evidence indicates that the western soil had adverse effects on S. sebiferum growth compared to the other soils examined, which had roughly equivalent effects on plant growth and survival.
The results of soil property analysis suggest possible reasons why plant growth and survival were lower on the western soil compared to the other soils studied. Although the western soil had considerably higher sand content than the other soils, it was also distinctive in other ways. Compared to the other soils, the western soil had the lowest carbon and nitrogen contents, higher sodium and phosphorus, and by far the highest electrical conductivity. Of all these properties, the one that may be of greatest significance is electrical conductivity, which averaged 3070 µS for the western soil compared to 140–634 µS for the other soils. High electrical conductivity values are indicative of high soil salinity (Job, Tabbagh, and Hachicha, 1995
; Lopez-Bruna and Herrero, 1996
; Hanson and Kaita, 1997
), a factor believed to strongly limit the growth of S. sebiferum (Conner, 1994
).
Several studies suggest that S. sebiferum is only modestly tolerant of saline conditions. Conner (1994)
confirmed this relatively low tolerance to salinity, based on studies that found S. sebiferum mortality to be significantly higher in plants watered with 10 g/L saltwater than in plants watered with freshwater. Sapium sebiferum growth was not reduced by watering plants with 2 g/L saltwater. This is consistent with findings by Tsing, Yi-hsiung, and Wan-li (1956)
. Plants continuously flooded with saltwater exhibited significantly reduced growth as compared to treatments watered to saturation daily. Plants flooded with 10 g/L saltwater exhibited 100% mortality within 6 wk of initiating the treatments.
The tolerance of S. sebiferum to saltwater flooding with polyhaline (27 g/L) water was examined by Conner and Askew (1993)
to determine its potential response to storm-surge flooding of coastal wetland forests. Subject plants were flooded continuously for 5 d with saltwater, after which they were thoroughly rinsed to simulate rainfall following a hurricane. Plants were then watered daily for 8 wk before being harvested. It was found that S. sebiferum exhibited 40% mortality following saltwater flooding. Thus, S. sebiferum appears to be able to tolerate short, infrequent periods of saltwater flooding in coastal forests.
The salinity values in saline soils and saltwater are not directly comparable when assessing their negative impacts on plant growth (Marschner, 1986
). Salinity levels in soil can increase tremendously as soil moisture levels decrease below field capacity. The actual salt concentration can also be much greater at root surfaces than in the surrounding soil. Salinity measurements are also limited in the fact that they indicate total salt concentrations in soil or water, not salt composition or the combinations of salts present, which may be different for soils and saltwater. Thus, earlier studies of the effects of saltwater on S. sebiferum have not established a critical salinity value that can be applied to soils.
While it is not possible to eliminate all other explanations for the deleterious effects of the western soil on S. sebiferum growth, the effects of sand content on the retention of soil moisture does not appear to be a contributing factor. One might reasonably expect that the sandy nature of the western soil would result in a more rapid rate of water loss (Brady, 1990
; Smettem and Gregory, 1996
). The results of the greenhouse study, however, showed that watering frequency had no effect on plant growth on the western soil, unlike the results observed for the other soils (Fig. 5). Stated in a different way, growth of seedlings on the western soil was substantially and equally impaired regardless of watering regime, indicating that counter to expectations, plants growing on this soil did not suffer greater drought stress with less frequent water supply. From this it is concluded that the deleterious effects of the western soil observed in this study do not result from a greater tendency for water stress.
One other factor that could be responsible for poor plant growth on a soil is low nutrient content. Elemental analysis indicated that the western soil was low in total carbon and nitrogen. In this case, however, nutrient addition failed to show that the western soil was limited to a greater degree by available nitrogen or phosphorus. Instead, the response of seedling growth to nutrient addition followed the same pattern for the western soil as for all the other soils, though it again supported only modest growth (regardless of fertilization treatment). It is not possible to completely rule out the possibility that nutrient availability or other fertility factors contribute to the poor growth of S. sebiferum seedlings on the western soil. However, the results from this study provide no evidence to support such an interpretation. For this reason, we believe that the most likely explanation for the observed deleterious effects of the western soil on plant growth is elevated soil salinity.
There are at least two possible reasons why the soil from the western study site was high in electrical conductivity, and therefore, salinity. First, soil salinity is strongly linked to high ratios of evapotranspiration to precipitation, as is commonly found in arid regions (Savenije and Pages, 1992
; Benasher, 1994
). The western site has a long-term precipitation average of 732 mm compared to 1224 and 1437 mm for the central and eastern study areas, respectively. According to Smeins, Diamond, and Hanselka (1989)
, the western area of the coastal prairie region has a substantially greater evapotranspiration to precipitation ratio than the eastern portion, and this could contribute to a generally higher conductivity in the soil. A second factor that could contribute to the higher salinity at the western site is greater coastal influence. While all three study areas are in the coastal zone, the western site was physically closer to the coast and could be subjected to greater influence from salt spray or saltwater inputs. It is well documented that distance from the coast is not a simple predictor of soil salinity (Mitsch and Gosselink, 1993
). Small topographic influences are known to play a major role in soil salinities in coastal areas (Bertness, Gough, and Shumway, 1992
; Shumway and Bertness, 1992
). Because of this, further examination of the extent of salinity at all three sites might contribute to a better understanding of the degree to which salinity could limit S. sebiferum growth in the coastal prairie.
Aside from soil effects, when plants were grown in field conditions, study site location had effects on both survival and growth regardless of soil. Across all soils, plants grown at the western site had greater mortality (37%) compared to those grown at the central and eastern sites (20%). In addition, the height of survivors grown at the western site averaged ~6 cm, while those grown at central and eastern sites averaged ~8 and 12 cm, respectively. These results indicate, therefore, that growing conditions at the western site were less favorable for S. sebiferum seedlings than at the central and eastern sites.
The importance of available moisture for S. sebiferum growth was also demonstrated in this study. For most soils, growth was substantially greater with frequent watering. As other studies have indicated (Lin et al., 1958
; National Academy of Sciences, 1983
), S. sebiferum grows most rapidly in wet conditions. Despite this, it appears to have substantial tolerance to drought conditions (Bruce, 1993
), and in this study, plants limited to monthly watering survived and grew, though at slower rates.
Overall, the results of this study support the hypothesis that conditions in the western portion of the coastal prairie are generally poor for S. sebiferum growth. It is further proposed that elevated salinity is a major factor reducing growth on the western soil. This effect, although strong, may not completely prevent invasion by this species. Future work is recommended to determine the degree to which soil salinity can prevent the invasion of S. sebiferum into the coastal prairie and other ecosystems.
FOOTNOTES
1 The authors thank the management and staff of the University of Louisiana-Lafayette Biology Department and the United States Geological Survey-National Wetlands Research Center for their assistance and suggestions; the staff of the United States Fish and Wildlife Service at the Aransas, Brazoria, and Lacassine National Wildlife Refuges for their cooperation, and Editor-in-Chief Karl Niklas, Tammy Charron, Dr. Paul Harcombe, and an anonymous reviewer whose comments and suggestions improved the quality of this manuscript. 
2 Author for correspondence, current address: Louisiana Department of Natural Resources, Coastal Restoration Division, P. O. Box 639, Abbeville, Louisiana 70511 USA (troyb{at}dnr.state.la.us
).
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  W. E. Rogers and E. Siemann Effects of simulated herbivory and resources on Chinese tallow tree (Sapium sebiferum, Euphorbiaceae) invasion of native coastal prairie Am. J. Botany, February 1, 2003; 90(2): 243 - 249. [Abstract] [Full Text] [PDF]
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 M. PIGLIUCCI and A. KOLODYNSKA Phenotypic Plasticity and Integration in Response to Flooded Conditions in Natural Accessions of Arabidopsis thaliana (L.) Heynh (Brassicaceae) Ann. Bot., August 1, 2002; 90(2): 199 - 207. [Abstract] [Full Text] [PDF]
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