Effects of habitat, burial, age and passage through birds on germination and establishment of chinese tallow tree in coastal South Carolina
Renne, Ian J
Effects of habitat, burial, age and passage through birds on germination and establishment of Chinese tallow tree in coastal South Carolina1
RENNE, I. J., T. P SPIRA (Department of Biological Sciences, Clemson University, Clemson, South Carolina 29634) AND W. C. BRIDGES, JR. (Department of Experimental Statistics, Clemson University, Clemson, South Carolina 29634). Effects of habitat, burial, age and passage through birds on germination and establishment of Chinese tallow tree in coastal South Carolina. J. Torrey Bot. Soc. 128:000-000. 2001.-Factors affecting germination and seedling establishment of the nonindigenous, invasive Chinese tallow tree (Sapium sebiferum (L.) Roxb.) were investigated under greenhouse and field conditions. In greenhouse experiments, buried seeds had higher germination rates and percentages than surface seeds, and simulated and actual seed passage through the avian gut enhanced germination. One year of aging reduced germination and seed viability, particularly for seeds unhandled by birds. In the field, seedling emergence and survival were greater in mixed pine-hardwood forest than in pine-turkey oak forest or spoil areas. Planting date did not affect overall seedling emergence or survival. Seeds sown in March 1998 and 1999 in five coastal forests that contained established tallow trees emerged throughout the growing season. While seedling emergence rates varied, final seedling numbers were similar across habitats in 1998, but were lower and differed across habitats in 1999. Recruitment was thus spatially and temporally variable. Viability of seeds buried for one and two years ranged from 16 to 69% in the five habitats, but did not differ among habitats or length of burial time. Because habitat type did not affect seed dormancy (both years) and final seedling number (1998 only), we conclude that other factors influence the differential success of tallow trees among coastal forests in South Carolina. Management strategies (e.g., fire) should consider the seedling phenology and seed bank capability of tallow tree.
Key words: Sapium sebiferum, exotic plant, invasion, avian seed dispersal, germination, dormancy, seedling establishment.
Chinese tallow tree (Sapium sebiferum (L.) Roxb.) is a nonnative, aggressive plant that has colonized coastal prairie and other habitats along the Gulf Coast (Bruce et al. 1995; Neyland and Meyer 1997; Wall and Darwin 1999) as well as several forest types along the southeastern coastal plain (Helm et al. 1991). In South Carolina, not all habitats are equally susceptible to tallow tree invasion (Renne, unpubl. data). Spoil dredge areas and other highly disturbed sites generally harbor the highest density of large reproductive trees, whereas many less disturbed forest types have smaller, more widely spaced individuals. In particular, longleaf pine-turkey oak and pine flatwood communities contain almost no tallow trees. These habitats may not receive sufficient numbers of seeds to successfully establish populations (i.e., seed-limited) and/or conditions may be unsuitable for seed germination and seedling establishment (i.e., microsite– limited; Klinkhamer and de Jong 1989; Eriksson and Ehrlen 1992).
Determining the factors) limiting tallow tree population growth among habitats can be useful for predicting its future local and regional success. If seed input is high, for example, seed– limited areas would likely become invaded, whereas microsite-limited areas may be more resistant, depending on the spatial and temporal availability of `safe sites’ (Harper 1977) and other environmental factors affecting adult growth, survival and fecundity.
Renne et al. (2000) found that tallow tree seeds are consumed in large numbers by many bird species, but the fate of these propagules is unknown (see Renne 1996). Birds may digest the seeds or they may defecate viable seeds in inappropriate sites for establishment. Viable seeds could also be deposited in suitable areas where they do not immediately germinate. Seed banks can be important to the growth and persistence of plant populations by spreading the risk of propagule mortality in a spatially and temporally variable environment (Cohen 1966; Brown and Venable 1986; Kalisz and McPeek 1993).
Seed dispersal and seedling establishment represent an important demographic link in the life history of plants (Harper 1977; Herrera et al. 1994; Houle 1995). Environmental factors affecting germination, seedling establishment and other life history phases such as adult survival, growth and fecundity may be positively correlated. However, spatial and temporal fluctuations in microsite differences (e.g., local variation in predation, competition, edaphic conditions, etc.) can cause considerable discordance between seed bank longevity, germination and subsequent seedling recruitment (Herrera et al. 1994; Houle 1995, 1998; Schupp 1995). This in turn can lead to weak correlations between seed rain pattern and adult plant distribution.
In this study, we investigated factors affecting germination and seedling establishment of Chinese tallow tree. The effects of seed passage through a bird’s gut, seed burial and seed age on germination were assessed in a greenhouse. In a series of field experiments, we investigated whether seedling emergence and survival differed among planting dates, years and forest types in coastal South Carolina. The potential for a two-year soil seed bank was also assessed. By studying the germination behavior and establishment of this invasive plant, a better understanding of its demography and management may be achieved.
Methods. STUDY SPECIES. Chinese tallow tree is a semitropical, deciduous tree that can grow to 20 rn or more. It is monoecious and the inflorescence is a spikelike thyrse that forms by the end of May in coastal South Carolina. Three– lobed green capsules that contain up to three seeds develop by mid-July. Upon maturation in October through November, the outer husk dehisces, exposing white arillate seeds. The outer layer of tallow is about 25% of the seed weight, and contains lipids and proteins (Potts and Bolley 1946; Huoran and Pengxin 1991). A hard black seed is located below the aril. Seed viability is between 90 and 95% (Bonner 1974; Bruce 1993), germinability is high after five years of storage (Cameron et al. 2000) and 50% of seeds can remain viable in Louisiana soil for more than one year (Harper 1995). The seedlings are tolerant of shade (Jones and McLeod 1989, 1990) and flooding by fresh and saltwater (Jones and Sharitz 1990; Conner and Askew 1993; Conner 1994). Along the Gulf Coast, seedling growth and survival depend on watering frequency and soil type (Bruce 1993; Barrilleaux and Grace 2000). Jubinsky (1993), Bruce et al. (1997) and Renne et al. (2000) review other aspects of tallow tree biology.
GREENHOUSE EXPERIMENTS. The effects of seed passage through the gut of a bird and depth of burial on percent and rate of germination were studied in a greenhouse. Seeds defecated by birds were collected below reproductive tallow trees in the field. No seeds were identified to particular birds, but many were surrounded with feces containing ant exoskeletons, indicating they were defecated by northern flickers (Colaptes auratus L.). Seeds with no visible beak marks were collected directly from tallow trees (‘unhandled’ seeds hereafter).
Experimental design was a 2 X 2 balanced factorial with two seed types (defecated and unhandled), two burial depths (0 and 1 cm) and 100 seeds per treatment. On 4 March 1996, seeds were evenly sown either 1 cm deep or on the surface (‘buried’ and ‘surface’ seeds hereafter) of vermiculite in four, 55 X 30 X 5 cm trays, which were watered to field capacity with tap water five times a week. When seeds germinated or seedlings emerged in surface and buried treatments, respectively, they were marked with a toothpick with dated masking tape. Germination occurred when the seed coat split and the radicle began to grow and seedling emergence occurred when the hypocotyl emerged from the vermiculite. The time taken for germinated surface seeds to reach a seedling height of 1 cm was recorded. This length of time was subtracted from the length of time taken for seedlings to emerge from buried seeds so that their germination time could be approximated. Due to greenhouse construction, the 87-day experiment was ended on 29 May 1996.
On 26 March 1998, the experiment was repeated with modifications. To determine if tallow tree seeds were germinable after one year of storage, defecated and unhandled seeds from the 1996-97 and 1997-98 seed crop were sown. 1996-97 seeds were stored in a paper bag and kept outside in a sheltered location in Clemson, South Carolina for one year. We also simulated seed passage through the avian gut by soaking freshly collected 1997-98 unhandled seeds in concentrated hydrochloric acid for 40 minutes and rubbing the aril off with cloth. Similar procedures and design were used except this experiment lasted 244 days and all seeds were sown at a depth of 1 cm in vermiculite. Eight months after sowing, ungerminated seeds were split open and intact embryos were cut in half and placed in 1% tetrazolium chloride (TC) for 24 hours to test for living tissue (Moore 1985). Embryos that turned red were considered viable.
STUDY SITE. Field studies were conducted from 1995-1996 and 1998-2000 in the 3077 ha Hobcaw Forest (33 deg 20’N, 79 deg 15’W) located on the outer Coastal Plain in Georgetown County, South Carolina. Mean annual precipitation was 1315 rum and mean January and August air temperatures were 9 deg C and 27 deg C, respectively, from 1930-1996 (Clemson Forestry Department, Georgetown County). In the plot study (see below), mixed pine-hardwood stands (MPH) were sampled. Common canopy species included loblolly pine (Pinus taeda L.), live oak (Quercus virginiana Mill.), and sweetgum (Liquidambar styraciflua L.). Soils ranged from moderately well to poorly drained. Two spoil areas (SA) separated by about five km were also sampled. The latter were highly disturbed areas with fine– textured soil dikes enclosing a settling pond for dredged material. Tallow trees were the most common large woody plant on these dikes (pers. obs.). Lastly, we worked in longleaf pine-turkey oak forests (PTO). These dry areas had sandy, excessively drained soil and contained few tallow trees (pers. obs.).
In the transect study (see below), five common coastal forest types that contained established tallow tree populations were sampled. The maritime evergreen forest (MAR) had a relatively open 25 m tall canopy of loblolly pine and live oak, high shrub and vine density, and moderate to poorly drained dark gray sandy soil. The loblolly pine forest (LP) contained a continuous 20 m tall canopy, poorly developed shrub and herb layers, a 5-10 cm litter layer of pine needles and moderately well drained grayish brown sand. Grasses, wingstem (Verbesina occidentalis Walt.) and tallow trees dominated a recent mixed pine-hardwood forest clearcut (CC). Soil was moderately well drained gray brown loamy sand. The young mixed pine-hardwood forest (YMPH) had a 7-11 m tall canopy of loblolly pine, water oak (Q. nigra L.) and tallow trees; wax myrtle (Myrica cerifera L.) was the dominant shrub, and a dark gray well to moderately poorly drained sandy soil was present. A welldeveloped bottomland hardwood forest (BLH; blackwater type) had a diverse 25-30 m tall canopy, a thick shrub layer dominated by dwarf palmetto (Sabal minor (Jacq.) Persoon) and a poorly drained black loam that was intermittently flooded. Community and soil descriptions follow Schafale and Weakley (1990) and Stuckey (1982), respectively, and nomenclature follows Radford et al. (1968).
FIELD PLOT STUDY. The effects of habitat type and planting date were tested on seedling emergence and survival by using an unbalanced 3 X 2 factorial, with three habitat types (MPH, SA and PTO), two planting dates (19 December 1995, 23 February 1996) and five replications. Dates correspond to times when tallow tree seeds are dispersed by birds (Renne et al. 2000). On each date, 50 seeds with no aril damage were collected from 30 widely separated trees and mixed in a bag. Seeds were then sown at 5 cm intervals in a 10 by 10 grid (n = 100 seeds per plot) and covered with ca. 0.5 cm of soil to decrease the chance of seed removal by animals, gravity or water. The 0.25 m^sup 2^ plots were fenced with chicken wire to deter feral hogs (Sus scrofa L.) from rooting in them. To standardize local microsite differences and test the effect of soil type among habitats on germination and seedling survival, vegetation and litter were removed from plots before seeds were sown. On 23 February 1996, a fenced 0.25 m^sup 2^ plot was constructed adjacent to each of the 15 plots and seeds were similarly sown. One pair of plots in SA was destroyed by feral hogs, thus data from 28 plots were analyzed (n = 2800 seeds). As a negative control, a 0.25 m^sup 2^ area next to each set of plots was randomly chosen so that emergence from a soil seed bank could be estimated.
We monitored seedling emergence on 21 March, 5 April, 19 April, 13 May, 22 June, 8 August and 20 September 1996 (n = 7 dates) by marking newly emerged seedlings with a toothpick with dated masking tape. On 20 September 1996, the number of surviving seedlings was counted and differences in emergence and survival rate were tested as a function of habitat and planting date. Seedling survival for each plot was calculated by dividing the number of surviving seedlings by the total number of seedlings that emerged. A seedling was considered a survivor if it had at least one fully expanded leaf and a living shoot apex.
FIELD TRANSECT STUDY. Tallow tree population growth rates differ in the five coastal forest types described above (Renne, unpubl. data), so we investigated whether seedling emergence and survival were different in these habitats. Because herbivory, trampling by mammals and microsite differences can create spatial and temporal differences in seed germination and seedling survival (Howe et al. 1985; Oswald and Neuenschwander 1993), seeds were sown along unfenced transects where no litter or vegetation was removed.
On 15 March 1998, 6000 seeds were collected from ca. 100 tallow trees. Seeds were sown 0.5 cm deep at 20 cm intervals along five randomly placed 20 m transects in all five habitats (n = 100 seeds per transect and 500 seeds per habitat). On 23 May, 23 June and 31 July 1998, newly emerged seedlings were marked with a plastic straw and their transect position was recorded so that emergence and survival history could be determined for each seedling. Because seedlings may emerge from a seed bank, seedling emergence was also monitored along transects without sown seeds. These were located I m away from those with sown seeds. Final seedling number was estimated by subtracting numbers of surviving seedlings from transects without sown seeds from ones with sown seeds on 9 October 1998. This experiment was repeated on 18 March 1999, but freshly collected seeds were sown at 40 cm intervals along 20 rn transects located 1 rn away from those used the previous year (n = 50 seeds per transect and 250 seeds per habitat). Numbers of surviving seedlings were recorded on 10 October 1999 only.
SEED BANK STUDY. On 15 March 1998, the potential for a one- and two-year soil seed bank was assessed by burying two packs of 100 tallow tree seeds at a depth of 4 cm in each of three randomly selected, fenced locations in each of the five forest types (n = 3000 seeds). Seeds were placed in panty hose pouches surrounded with 0.5 cm mesh hardware cloth to prevent seed predation by rodents. One seed pack was recovered from each plot after one and two years. We assumed seeds with split seed coats had germinated. Ungerminated seeds were tested for viability with 1% TC. Actual sampling of the soil seed bank did not occur.
Six thousand seeds from one collection event were used in the seed bank, 1998 transect and second greenhouse experiment (1997-1998 seeds only). To obtain a baseline for initial seed viability, we split 101 of these seeds, counted the number of intact embryos, and placed cut embryos in 1% TC before any experiments were done.
Discussion. GREENHOUSE EXPERIMENTS. Although an avian gastrointestinal treatment is not a germination requirement, defecated and acid– treated seeds had higher percent germination and reduced germination time relative to unhandled seeds (also see Glyphis et al. 1981; Barnea et al. 1991). If early emergence leads to greater biomass accumulation during the growing season relative to later-emerging seedlings (Ross and Harper 1972; Fowler 1988), then the seedling survival advantage conferred by seed passage through birds may contribute to the northward spread of tallow tree by reducing germination time. Indeed, Draper (1982) and Jubinsky and Anderson (1996) report frost damage is a limitation to its distribution, and Renne (unpubl. data) found plant size is a strong determinant affecting tallow tree overwintering survival. Early emergence can also confer a competitive advantage over late-emerging conspecifics or other plants (Ross and Harper 1972; Weaver and Cavers 1979), but this advantage may vary in space and time (Fowler 1984; Kalisz 1986; Jones and Sharitz 1989).
Potential advantages of rapid aril removal by acid treatment or digestion by birds include increased imbibition and gas exchange of seeds, two requirements for germination (Baskin and Baskin 1998). Gas exchange of surface seeds was at least as great as those that were buried, whereas imbibition was likely greater for buried seeds because more seed surface was in direct contact with soil. The higher germination of buried seeds suggests increased imbibition efficiency was the primary mechanism influencing their germination (also see Bruce 1993).
Defecated and freshly collected seeds had higher seed viability than unhandled and one– year old seeds, respectively, and one-year old unhandled seeds had the lowest viability of any treatment. Loss of viability occurred under our outdoor storage conditions, but was slower for seeds that passed through the avian gut. Reduction in seed moisture (Harrington 1973) due to removal of the waxy aril may have prolonged longevity, but it is not clear if bird-dispersed seeds have greater longevity than unhandled seeds under field conditions.
FIELD SEEDLING ESTABLISHMENT. Tallow tree is seed-limited in many habitats in coastal South Carolina because sowing seed along transects and in plots resulted in higher seedling establishment rates relative to control areas with no sown seeds (Louda 1982; Shaw and Antonovics 1986). Disturbance was not simulated along transects (i.e., no vegetation was removed), thus the possibility of microsite limitation within habitats cannot be excluded (Eriksson and Ehrlen 1992). In 1998, microsite differences for germination and initial establishment existed among habitats, but because seedling survival did not differ, the transition probability from seed to established seedling was not different among habitats.
In 1999, however, final seedling number differed among habitats (Fig. 4b). If conditions affecting adult growth and survival are similar to those affecting seedling establishment, then many of the coastal forests we sampled will continue to be invaded, albeit at different rates, by tallow tree. Renne (unpubl. data) found that tallow tree population growth rates differed among the five forest types, but all were positive from 1997-1999. Moreover, population growth corresponded well with our seedling emergence and survival data, with the slowest (BLH) and most rapidly increasing (CC) populations having the lowest and highest establishment rates, respectively. As these populations continue to grow and age, they will likely become microsite-limited as available sites become colonized.
Fewer seedlings were also found in 1999 than in 1998, thus recruitment was variable in both space and time. Horvitz and Schemske (1995) found considerable spatial and temporal variation in nearly all life history stages of a tropical understory herb, but particularly so for the seedling stage. They concluded that heterogeneous selective pressure can vary such that the relative importance of specific life history stages to overall population growth (i.e., elasticity values) may change across populations, years and populations within years. This spatiotemporal variation can complicate management efforts but is necessary to estimate when implementing the most effective conservation strategy(ies). Current studies using population projection matrices may elucidate the consequences of early life history spatiotemporal variation to local and regional tallow tree population growth.
From January through March, there was 68% less rainfall in 1999 compared to 1998 (22.9 and 70.8 cm, respectively; Clemson Forestry Department, Georgetown County), and the soils, many of which are located at or below sea level, were likely wetter when seeds were sown in 1998 than in 1999. From April through August, however, 29% more rain fell in 1999 than in 1998 (76.9 and 59.5 cm, respectively), the period when most seedlings emerged. It remains unclear why recruitment was lower in 1999, but heavy rains in the beginning of 1998 may have caused the observed higher seedling establishment patterns by increasing early seed imbibition and promoting germination. No other meteorological factors were examined.
Plot and transect data show that tallow tree seeds germinated throughout the growing season, with a peak occurring from late April to mid June in most habitats (Figs. 3 and 4a). This pattern is consistent with the germination phenology of other shade-tolerant species, which typically exhibit temporally broad germination relative to shade-intolerant species (Garwood 1982). Germination spread over time can buffer against complete seedling cohort loss due to fire, herbivory, drought or late frost (Rice 1987; Kalisz and McPeek, 1993) and should be considered when implementing management strategies (see below).
Some community types are more resistant to tallow tree invasion than others. In our plot study, seedling emergence and survivorship were lower in SA and PTO relative to MPH. Tallow trees are the dominant plant of SA, particularly on the lower banks of dikes, but seeds were sown high on the banks so that seeds were not removed or added by flooding or seed fall from reproductive trees. It is unknown whether an establishment gradient exists along SA banks, but high seed input and/or establishment rate have contributed to high tallow tree density in this locale. In PTO, lack of tallow trees is the result of poor seedling emergence and survival. Low moisture availability due to porous sandy soils and a high relative elevation may also reduce adult growth and survival in this habitat.
SEED BANK DYNAMICS. Numbers of buried seeds remaining viable did not differ among habitats, but differed among replicate plots in four of five habitats. A locally variable, but regionally constant, multiyear soil seed bank can therefore develop. The relatively high seedling emergence along transects without sown seeds also indicates a persistent seed bank.
Seed bank evolution is a consequence of unpredictable spatial and temporal events that affect seedling establishment (Cohen 1966; Templeton and Levin 1979; Venable and Brown 1988). Tallow tree seedlings (and adults) are relatively shade-tolerant (Jones and McLeod 1989, 1990) and persist under a well-developed canopy, but the creation of canopy gaps increases growth and reduces mortality of seedlings (Renne, unpubl. data). Hurricanes, for example, are a major structuring force of Southeastern coastal forests, but the magnitude and frequency of their effects are inherently variable in space and time. Under these circumstances, colonization of ephemeral safe sites would be maximized with a persistent seed bank (Horvitz and Schemske 1986; Cipollini et al. 1993).
MANAGEMENT CONSIDERATIONS. Fire can kill tallow tree seedlings and reduce adult growth, but an intense, growing season bum may be required (Grace 1998). Because seedling emergence was temporally broad and buried seeds remained viable in the Southeast (this study) and Gulf Coast (Harper 1995), late season annual bums may be most effective in killing the most individuals, particularly in recently invaded areas because larger individuals often resprout when top killed (Grace 1998). No data exist on how fire affects tallow tree seed survival.
CONCLUSIONS. Our data suggest that susceptibility of forest types to tallow tree invasion differs greatly, but effective avian seed dispersal (Renne et al. 2000), a regionally persistent seed bank and consistently successful seedling establishment contribute to its current invasion of many coastal forests in South Carolina. Because seed dormancy (both years) and seedling establishment (1998 only) were not affected by forest type, differences in seed dispersal and adult growth, survival and fecundity are other probable factors influencing its differential success among forests. Populations will likely become less seed-limited, and more microsite-limited, as available sites become colonized, but clearcuts and other canopy disturbances may reverse this trend. Future studies on tallow tree demographics can be used to identify important life history stages so that effective control efforts for this species may be achieved.
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Ian J. Renne2 and Timothy P. Spira
Department of Biological Sciences, Clemson University, Clemson, South Carolina 29634-0326
W. C. Bridges, Jr.
Department of Experimental Statistics, Clemson University, Clemson, South Carolina 29634
Received for publication October 26, 2000, and in revised form February 14, 2001.
1 We thank Wylie Barrow and the National Wetlands Research Center in Lafayette, Louisiana for partial funding of this project. Paul E Renne also provided financial support, and he, JoAnne and Don Lightner, Paul John, Jennifer, Paul A. and Eileen Renne, and John and Flo Ference deserve thanks for other forms of support. We thank Chuck Gresham and staff members at the Baruch Forest Science Institute in Georgetown County, SC for providing helpful suggestions and transportation.
2 Author for correspondence. E-mail: irenne@ clemson.edu
Copyright Torrey Botanical Society Apr-Jun 2001
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