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Seedling establishment and regeneration of Korean red pine (Pinus densiflora S. et Z.) forests in Korea in relation to soil moisture
Forest Ecology and Management 199 (2004) 423–432
Seedling establishment and regeneration of Korean red pine (Pinus densiflora S. et Z.) forests in Korea in relation to soil moisture Chang Seok Leea,*, Joon Ho Kimb, Hoonbok Yic, Young Han Youa a
Faculty of Environment and Life Sciences, Seoul Women’s University, Seoul 139-774, South Korea b School of Biological Sciences, Seoul National University, Seoul 151-742, South Korea c Department of Forest Science, Oregon State University, Corvallis, OR 97331, USA Received 1 December 2003; received in revised form 7 January 2004; accepted 25 May 2004
Abstract To identify limitations on the regeneration of Korean red pine (Pinus densiflora S. et Z.) in its native range, we evaluated seed production, dispersal, germination, and seedling establishment under a range of canopies that intercepted 0% (open ground, OG), 70% (canopy gap, CG), and 97% (closed canopy, CC) of the light. To evaluate the importance of drought we added a treatment, which supplemented soil depth and irrigated to the most open setting (IO) as a reference plot. Depletion in soil moisture content was measured gravimetrically over a range of depths in the laboratory as well as over the specified site conditions where seeds (100 per 90 cm2) had been sown. Seedling germination, survival, water potentials (c), and relative water contents (RWC) were also monitored. Seed production proved stable interannually, averaging 25–27 m2 year1 with 42–44% viability. Seed gravity dispersal fell off exponentially from the edge of a 70-year-old pine stand, approaching zero at a distance of 80 m based on the relationship equation developed between seed number and distance from the forest edge. With irrigation, 90% of the sown seed germinated; without irrigation <40% germinated. Subsequently, seedling survival following germination was 99% in the IO treatment, 0% on OG, 32% on CC, and 8% on CG. Differences in seedling mortality were attributed to the degree that they experienced water stress; seedling death was recorded at c < 5.0 MPa and RWC <50%. P. densiflora has advantages in being able to survive in its native habitat by adaptation to withstand a long season (November–June) of little precipitation and to take quick advantage of improved growing conditions following spring rains. # 2004 Elsevier B.V. All rights reserved. Keywords: Germination; Human disturbance; Pinus densiflora; Relative water content; Seed dispersal; Seed production; Seedling survival; Water potential
1. Introduction Pinus densiflora S. et Z. (Korean red pine) is distributed over the Korean Peninsula, the Japanese *
Corresponding author. Tel.: þ82 2 970 5666; fax: þ82 2 970 5822. E-mail address: [email protected] (C.S. Lee).
Archipelago, and in Shandong and Manchuria provinces of China (Critchfield and Little, 1966). The pine forests had occupied about half of the forested area in Korea several decades ago (KFS, 1971) and currently occupies one-third of the area (KFS, 2002). This pine produces pollen that is wind dispersed (Kang, 1999). It takes 3 years to complete its reproduction cycle (Singh, 1978): female bud formation is
0378-1127/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2004.05.053
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initiated in the summer, pollination occurs the following spring, and seeds maturate in the fall a year later. After 40–60 years, relative growth in diameter and height slows as a log-normal (Lee and Kim, 1989). Cone production may begin at 7 years in isolated tree; it is delayed to 11—18 years when trees form stands (Lee and Kim, 1989). On exposed rocky ridges, some trees survive to ages beyond 140 years (Lee, 1995a). According to pollen analysis, pine forests replaced deciduous broad-leaved forests about 2300 years ago in the southwestern part, and 1400 years ago in the eastern part of the Korean Peninsula (Kim, 1980; Choi, 1998). This range expansion was in response to an increase in fire frequency associated with rising temperatures and agricultural activities (Kim, 1980; Choi, 1998). The persistence of these temperate pine forests in Korea has been speculated to be a result of the pine’s adaptation to and dependence upon dry weather from fall through spring (Kim, 1980; Lee and Kim, 1987; Lee and Lee, 2003), the availability of large areas with coarse-textured soils (Lee and Kim, 1987; Lee and Lee, 2003), and frequent disturbance by human activities (Kim, 1980; Lee and Hong, 2001). Disturbances were envisioned as creating gaps in the forest canopy and exposing bare soil that favored seed germination while coarse-textured soils would induce drought sufficient to limit competition from oak and other species (Lee, 1995a, b; Lee and Lee, 2003). With a shift toward fossil fuels for heating homes, the kinds of disturbances that once perpetuated Korean red pine are now lacking (Lee and Hong, 1998, 2001). Whether clear felling, or other alternatives might serve the same role as fire is a question worth addressing. In areas where native forests have been highly fragmented, such as in Korea, it is useful to evaluate life history attributes of a species in reference to its competitors. The critical stages in a plant’s life cycle are those having to do with reproduction, seed dispersal, germination, and seedling establishment (Kavanagh and Carleton, 1990). If conditions for successful regeneration occur infrequently, then successful maintenance of a population is less assured because a favorable seed year must correspond with an appropriate disturbance. Knowledge of interannual variation in seed production and the distribution of age classes of trees can address the importance of synchronous events in perpetuating tree populations
(Grubb, 1977; Urbanska, 1997). Adequate dispersal is necessary to occupy new habitats and to expand a population (Angevine and Chabot, 1979; Solbrig, 1980; Brown et al., 1988). Although seeds may germinate, seedling establishment may occur only under specific microclimatic and edaphic conditions that provide adequate moisture, light, and nutrients, without harmful pathogens and herbivores (Harper et al., 1965; Urbanska, 1997). Although most species in the genus Pinus grow well under high radiation (Koyama, 1943; Shirley, 1945), the initial establishment stage is more sensitive to the availability of soil moisture than radiation (Koyama, 1943; Oosting and Kramer, 1946). Because the Korean Peninsula customarily experiences a long dry season from fall to spring (KMA, 2001), we shall place special emphasis on monitoring plant water stress and root growth at the time of germination and seedling establishment. Our specific objective in this study was to explore the establishment phase of Korean red pine forests by quantifying: (1) interannual variation in seed production and viability, (2) the distance that wind-blown seed travels from the edge of a forest, (3) how seed germination varies under different light and soil conditions, and (4) how variation in soil moisture content affects seedling water relations and mortality.
2. Study areas Three separate areas were utilized in this study. To assess seed production and dispersal, we chose mature Korean red pine forests at Tdantduk (site 1–1: 12682100 320 E, 3683000 140 N) and Butdugi (site 1–2: 12682000 240 E, 3683300 420 N) of Seungun-ri, Anmyuneup, Taean-gun located in the central western Korea. ‘‘Gun’’ is an administrative unit, which corresponds to a county, and ‘‘ri’’ is the smallest administrative unit, which corresponds to a village. Sites take locality names from the corresponding hamlets. The stand was composed of ca. 70-year-old trees, averaging 16 m in height with a stocking of 780 trees ha1. Canopy coverage averaged more than 80%. The soil has a loamy texture derived from a sedimentary metamorphic parent material (Millar and Turk, 1965). Soil profile was well developed with litter, A, and B horizons of 1.5, 2.1, and 25.5 cm thick,
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Fig. 1. Mean monthly trends in precipitation (P) and potential evapotranspiration (PE) for the Taean, Seoul, and Suwon regions show similar water balances with deficits in May and/or June of the year. Potential evapotranspiration was estimated using the Thornthwaite equation (Thornthwaite and Mather, 1957). Data were derived from meteorological summaries between 1950 and 1980 (KMA, 1984).
respectively. Organic matter content and field capacity were 5.5 and 23.7%, respectively. In another pine stand of similar age, structure, and site conditions, located 4 km distant from where seed production was studied, a clear cut provided an exposed edge of the forest, below which an open area was available for us to quantify seed dispersal. Germination and seedling survival were investigated on pine stands with different canopy conditions located at Mt. Kwanak, Seoul (site 2: 12685700 400 E, 3782700 180 N) and Imok-dong, Suwon (site 3: 12685900 360 E, 3781900 320 N). Trees at both sites were 30–40-years-old but those at site 2 grew more slowly than at site 3. The height of the stands on Mt. Kwanak averaged 8 m high with a stocking of 1150 trees ha1 where the height of stands at Imok-dong averaged 11 m with a stocking of 1230 trees ha1. Canopy coverage of both stands ranged between 75 and 80%. Although climatic conditions in regard to monthly water balances at the two sites appear similar (Fig. 1), the coarser textured sandy soil at site 2 is more dry prone than the loamy soil found at site 3 (Millar and Turk, 1965). These differences reflect the physicochemical properties of the slightly different parent materials, a granite at site 2, and a gneiss at site 3. The soil at Mt. Kwanak lacks an A horizon and is very shallow with the litter depth of only 1.3 cm and B horizon 16.5 cm thick. Organic matter content and field capacity were 2.5 and 21.5%, respectively. The soil at Imok-dong has a moderately well developed soil profile with litter, A, and B horizons of 2.1, 1.8, and 23.5 cm thick, respectively. Organic matter content and field capacity were 4.8 and 27.3%, respectively.
In addition to studies in canopy gaps under the forests on Mt. Kwanak, Seoul, we increased the range of microhabitats to include: (1) open ground, OG (100% light intensity) with a very shallow soil below 5 cm, (2) canopy gap, CG (30:2 5:9% light intensity) and (3) closed canopy, CC (3:5 1:7% light intensity). An irrigated treatment in the open (IO) was prepared by adding sandy loam soil, gathered from the nearby forest, to a depth of 30 cm, equivalent to that of the CG and CC plots. The IO treatment was watered at 2-day intervals throughout the experimental period and served as a reference to compare seed germination, and survival of seedlings in other treatments. The distribution of precipitation and seasonal patterns in evaporative demand were similar across three all study sites, showing modest water deficits in May and/or June with a significant surplus of water during July and August (Fig. 1; KMA, 2001).
3. Methods 3.1. Seed production and dispersal Seed production was tallied at site 1–1 by counting the number of seeds fallen into twelve 1 m2 seed traps made from nylon netting that were positioned 1 m above the soil surface. Seeds were collected over 3 years from 1 May 1985 to 30 April 1987. Seed dispersal was measured using five seed traps per point, set at 0, (beneath the seed source), 5, 10, 20, 30 and 40 m distance from the exposed edge of the 70years-old stand at Butdugi, Taean.
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3.2. Emergence and survival of seedlings on forest floor One hundred seeds were sown on the surface and at 1.0 cm depth at the 30–40-year-old stands at 3 cm 3 cm spacing on 6 April 1985. All seedbeds were covered with a 0.5 cm thick layer of pine litter and had five replicates. The survival of seedlings was measured by tallying the number of live seedlings at 1week intervals from the 5th week after sowing. The survival of seedlings occurred naturally was investigated by applying the same methods as the abovementioned case from early May when seed germination was completed to August at both Mt. Kwanak and Imok-dong. 3.3. Plant water potential and relative water content A greenhouse study was conducted at the Seoul National University to define critical soil moisture contents and corresponding plant water potentials (c) and relative water contents (RWC) that limit survival. A total of 1000 pine seeds were planted in 40 pots and allowed to germinate and grow for 3 months. At the end of 3 months, half of the pots received no additional water, while the other half continued to be irrigated. Water potentials were determined by the Shardakov dye method (Barrs, 1968). This method involved placing tissue samples into tubes with a range of solutions of known osmotic potential. Tissues that are not in equilibrium with the osmotic solution will change the concentration of the solution by losing or taking up water. A drop of dye extracted from a separate set of osmotic solutions will, when released by a pipette in the middle of a tube with tissue at equivalent water potential to the osmotic solution, remain suspended where released; when the tissue is not in equilibrium with the surround osmotic solution the dye will sink or rise. c measurements were taken between 7:00 and 8:00 a.m. on the first and second leaves of seedlings at periodic intervals thereafter until wilting was observed 46 days later. RWC was determined on first and second leaves by measuring the fresh weight of samples placed within a weighing bottle as soon as sampled, the turgid weight of samples suspended in natural water at 25 8C for 10 h under a 30 W incandescent lamp set at 30 cm
distance from the sample, and the dry weight of samples dried at 80 8C for 48 h. RWC was calculated as the difference between fresh and dry weight divided by the difference between turgid and dry weight, multiplied by 100 to convert to percent (Catsky, 1972). 3.4. Root length Root samples were attained by destructive sampling of five seedlings. Length of the taproot was measured with calipers to 0.05 mm precision. 3.5. Relative light intensity Light intensity was determined using a LICOR Model LI-185A photometer and a LI-190X quantum sensor. Relative light intensity for each site was calculated in reference to measurements made in the open. Each measurement was replicated five times along a transect at random distances. 3.6. Soil environmental factors The thickness of each soil horizon was determined after being exposed with a sharp flat-tipped spade. Soil samples were collected from mineral soil at a depth within 5 cm from the ground surface considering OG seedbed with the shallowest soil depth below 5 cm at 1-week intervals during June, the peak of dry season. Soil moisture contents (SM) were determined on the samples gravimetrically (n ¼ 5 at each depth) with a chemical balance (0.01 mg precision) and a forced air-drying oven set at 105 8C for 48 h. Organic matter content was determined from ash-free dry weight after ignition in muffle furnace of 600 8C for 4 h (Peters, 1973). Field capacity was determined following standard procedures (Broadbent, 1973). 3.7. Statistical analyses All statistical analyses were carried out using SAS (SAS Institute, 1989). Analysis of variance (ANOVA) was performed to compare soil moisture, and germination among plots. t-tests were made when making individual comparisons of germination rates at ground surface and 1 cm depth; Tukey’s honestly significant difference method was employed when making multiple comparisons among means. Regression analyses
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were used to describe the relation between seed dispersal and distance from seed source.
4. Results 4.1. Seed production Annual seed production in the 70-year-old pine forest was consistent, ranging from 25 to 27 seeds/ m2 with a viability averaging between 42 and 44% (Table 1). Seed fall and seed viability varied seasonally, with the highest values recorded in both cases in October and November every year (Table 1). 4.2. Seed dispersal The number of seeds collected in traps set at varying distances from the seed source decreased exponentially out to 40 m (Fig. 2). The exponential relationship developed between seed number and distance from the edge of the forest indicates by extrapolation that the maximum seed gravity dispersal would be about 80 m.
Table 1 Interannual seed production recorded under a 70-year-old Korean red pine stand Period
1985 May–September October November December–April Subtotal 1986 May–September October November December–April Subtotal 1987 May–September October November December–April Subtotal
Seeds collected Germinated Germination from twelve seeds percentage 1 m2 seed traps 53 70 66 112 301
10 42 47 28 127
18.8 60.0 71.2 25.0 42.2
49 61 58 153 321
31 41 38 32 142
63.3 67.2 65.5 20.9 44.2
42 62 106 86 296
5 36 68 17 126
11.9 58.1 64.2 19.8 42.6
Fig. 2. Changes of the number of seeds fallen in seed traps installed by distances from seed source stand. Equation on graph indicates relationship between distance and the number of seeds collected at each distance.
4.3. Germination Germination of seeds sown on the soil surface varied from a high of 90% on the irrigated open (IO) treatment to a low of 19% on the OG treatment. Germination rates on the CG and CC seedbeds were, respectively, 30 and 42% in 6 weeks after sowing (Table 2). Germination rates of seeds placed at 1 cm depth followed a similar response on the different seedbeds with only the OG and CG showing a significant difference from that measured on the soil surface (Table 2).
Table 2 Mean (%) and S.D. of seed germination from 100 per 900 cm2 that were sown on the soil surface and at 1 cm depth across a range of selected seedbeds Seedbeds
Germination rate (%) Soil surface
Irrigation, full exposure Open ground Canopy gap Closed canopy
89.8 19.2 30.0 42.0
3.9 4.1 4.0 3.4
P
1 cm depth 90.2 29.6 40.0 42.4
4.4 5.3 5.0 3.6
0.88 0.0001 0.0005 0.88
Significance of differences between soil surface and 1 cm depth plots are indicated with P values based on t-tests.
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Fig. 3. Survivorship curves of seedlings germinated on the different seedbeds on forest floor of the Korean red pine stand. Irrigated and exposed with soil supplement (IO), open ground (OG), canopy gap (CG), and closed canopy (CC).
4.4. Seedling survival under a range of seedbed conditions Of those seeds that germinated, survival varied from 99% on IO treatment to 0% on open ground (OG) (Fig. 3). The best survival without irrigation was observed under the closed canopy (about 30%), although growth of seedlings (not shown) was higher for those that survived in canopy gaps. Seedling survival naturally occurred on the forest floor of the pine forests at Seoul abruptly decreased to <10% near the end of June, whereas those in Suwon decreased more slowly and remained >70% (Fig. 4). These differences in responses between the two locations are interpreted as responses to differences in soil texture rather than climatic condition.
Fig. 4. Survivorship curves of seedlings germinated on forest floor of 30–40-year-old the Korean red pine stand in Seoul and Suwon. The poorer survival at Seoul compared to Suwon region is associated with
4.6. Water potential and relative water content of seedlings Under full exposure with irrigation (IO), water potentials of first and second leaves remained above
4.5. Soil moisture contents under a range of seedbed conditions For all seedbeds but the irrigated treatment, soil moisture contents in the upper 5 cm fell below 5% at the peak of drought in June (Fig. 5). The small differences in moisture content, even if they were significant, probably do not represent real differences in minimum soil water potentials (Philip, 1957), as the organic matter content varied slightly, with the highest under the CC treatment.
Fig. 5. Comparison of soil water contents averaged for the upper 5 cm of soil during the peak of drought in June under seedbeds exposed to different radiation loads: open ground (OG), irrigated (IO), open ground with a soil depth supplement to 30 cm, canopy gap (CG), closed canopy (CC). The letters indicate significant differences among means (n ¼ 5) at P ¼ 0:05 using the Tukey’s honestly significant difference method.
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Fig. 6. Comparison of seasonal changes in averaged leaf water potentials (c) and relative water contents under irrigated and nonirrigated fully exposed conditions.
0.9 MPa, with RWC at 91% throughout the greenhouse experiment. Without irrigation, water potentials began to drop within 30 days and reached a lethal point (5.1 Mpa) with a RWC of 54% by 45 days without irrigation (Fig. 6). 4.7. Root growth and vertical distribution of soil moisture Under closed canopy forests, current year seedlings extended their roots on average to a depth of 3.7 cm by
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Fig. 7. Seasonal pattern in root growth of current year seedlings germinated on the forest floor under a closed canopy of 30–40year-old Korean red pine.
May, with a further extension to below 7 cm by the peak of drought in June (Fig. 7). To avoid lethal water stresses, seedlings must reach more moist soil conditions than available in the upper 7 cm of soil, as was shown by those seedlings that survived drought stress in all non-irrigated experimental seedbeds. In fact, soil moisture contents measured at 1-week intervals during June were getting moisten as soil depth increased and exceeded 6%, which can be assumed as above critical level of water potential and RWC, from 9 cm depth (Fig. 8; Newman, 1966).
Fig. 8. Vertical distribution of soil moisture contents measured at 1-week intervals during June, the peak of dry season under a closed canopy of 30–40-year-old Korean red pine.
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5. Discussion 5.1. Seed production and dispersal Our observations over 3 years indicate minimum variation in seed production year to year (Table 1). It is possible that variation might still be encountered with a longer record of observation but from our limited study we conclude that a fair seed fall could be expected every year. This assumption is shared by foresters in their general reliance on seed trees following harvest activities (Lee and Kim, 1989; Bae, 1994; Kang et al., 2004). With distance from the seed source, the number of seeds caught in traps decreased rapidly with >50% recorded not more than 5 m from the stand edge and none expected to be wind-blown beyond a distance of 80 m (Fig. 2). Mean distance among seed trees in a silvicultural treatment, which have practiced in Korea, was 10–15 m. The further the distance among seed trees, the longer the time was required for recruitment of seedlings (Lee et al., 2004). The results from this study suggest that the distance should be reduced to shorten the period required to reach the optimal density in the silvicultural practice and further, to get satisfactory timber production. Seed dispersal may be affected by several variables: (1) the height of the seed tree, (2) the aerodynamic characteristics of the seed such as its weight, possession of wings, plumes, etc., (3) the effectiveness of distribution, a function of wind direction and velocity for pine seeds, as well as the presence and activities of animal vectors (Harper, 1977; Augspurger, 1986; Kang, 1999). 5.2. Environmental factors affecting germination and seedling survival Field experiments carried out on the forest floor under pine stands with different canopy conditions indicate that germination and seedling survival depend on the water content of each seedbed (Table 2; Figs. 3 and 5). In addition, germination percentages at 1 cm depth were somewhat higher than those on the soil surface in the OG and CG treatments (Table 2). No differences were observed with the IO treatment where the surface conditions did not dry out, or with the CC treatment where the
dense forest canopy reduced surface evaporation by intercepting >97% of the short-wave radiation and by reducing wind velocity to a minimum (Brandle et al., 1988). Further, seedling survival in Suwon with fine textured loamy soil was higher than that in Seoul of coarser textured sandy soil. In this respect, differences in germination and seedling survival among seedbeds in Seoul and between Seoul and Suwon would be attributed to the degree of water stress that they experienced. 5.3. Relationship between water deficits and seedling mortality The lethal water potentials of Korean red pine seedlings, 5.1 MPa, were far lower than those of other species of pine (1.0 to 1.9 MPa) or Picea spp. (1.8 to 2.2 MPa) (Richter, 1976). The lethal c of P. densiflora was nearly as low as that of Juniperus spp. (5.9 MPa) adapted to semi-desert environment (Richter, 1976). Korean red pine seedlings have been shown to survive drought for 45 days longer than competing oak species (Kim, 1990). The result resembles the former results that conifers usually have stronger drought resistance than broad-leaved trees (Jarvis and Jarvis, 1963; Hellkvist et al., 1974; Waring and Running, 1976). Although pine seedlings can tolerate considerable drought, their survival still requires that roots extend into the deeper soil below 9.0 cm to attain sufficient water or, alternatively, that cuticular transpiration is minimized once drought is imposed so that seedlings do not reach lethal relative water contents and water potentials. Korean red pine exhibits rapid root growth and a tolerance for drought that makes this species adapted to survival on coarsetextured soils throughout its native range. Even so, under similar climatic conditions (Fig. 1), survival can differ from region to region based on differences in soil texture (Fig. 4). In summary, water deficit in the spring appears to be the dominant cause of mortality of pine seedlings (Figs. 3 and 4). Differences in tolerance to desiccation among competing species govern the distribution and dominance of Korean red pine (Lee and Lee, 2003). Without a drought period and coarse-textured soils, most areas of the Korean Peninsula would be forested with deciduous broad-leaved species. With a shift in use of forest for fuel, the disturbance pattern has been
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altered (Lee and Hong, 1998, 2001). Clear cutting is not conducive to successful natural regeneration of the pine, although bare-rooted stock, if properly prepared and planted, might survive adequately. To achieve natural regeneration, our research indicates that a light to moderate partial cut would favor establishment because the seedbed conditions created would be less extreme than those encountered in more open, exposed seedbeds (Bae, 1994).
Acknowledgements We would like to thank Dr. R.H. Waring and Miss S.J. Wessell of the Oregon State University for a critical review of an earlier draft of this paper.
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Richter, H., 1976. The water status in the plant experimental evidence. In: Lange, O.L., Kappen, L., Schulze, E.P. (Eds.), Water and Plant Life. Springer-Verlag, New York, pp. 42– 58. SAS Institute, 1989. SAS/STAT User’s Guide, Version 6. SAS Institute, Cary, NC, USA. Shirley, H.L., 1945. Reproduction of upland conifers in the lake status as affected by root competition and light. Am. Midl. Nat. 33, 537–612. Singh, H., 1978. Embryology of Gymnosperms. Gebruder Borntraeger, Berlin, pp. 1–302. Solbrig, O., 1980. Demography and natural selection. In: Solbrig, O. (Ed.), Demography and Evolution in Plant Populations. University of California Press, Berkeley, pp. 1–20. Thornthwaite, C.W., Mather, J.R., 1957. Introductions and tables for computing potential evapotranspiration and water balance. Publ. Climatol. 10, 182–311. Urbanska, K.M., 1997. Safe sites-interface of plant population ecology and restoration ecology. In: Urbanska, K.M., Webb, N.R., Edwards, P.E. (Eds.), Restoration Ecology and Sustainable Development. Cambridge University Press, Cambridge, pp. 81–109. Waring, R.H., Running, S.W., 1976. Water uptake, storage and transpiration by conifers: a physiological model. In: Lange, O.L., Kappen, L., Schulze, E.D. (Eds.), Water and Plant Life— Problems and Modern Approaches—Ecological Studies, Vol. 19, Springer, New York. pp. 189–202.
Seedling establishment and regeneration of Korean red pine (Pinus densiflora S. et Z.) forests in Korea in relation to soil moisture Chang Seok Leea,*, Joon Ho Kimb, Hoonbok Yic, Young Han Youa a
Faculty of Environment and Life Sciences, Seoul Women’s University, Seoul 139-774, South Korea b School of Biological Sciences, Seoul National University, Seoul 151-742, South Korea c Department of Forest Science, Oregon State University, Corvallis, OR 97331, USA Received 1 December 2003; received in revised form 7 January 2004; accepted 25 May 2004
Abstract To identify limitations on the regeneration of Korean red pine (Pinus densiflora S. et Z.) in its native range, we evaluated seed production, dispersal, germination, and seedling establishment under a range of canopies that intercepted 0% (open ground, OG), 70% (canopy gap, CG), and 97% (closed canopy, CC) of the light. To evaluate the importance of drought we added a treatment, which supplemented soil depth and irrigated to the most open setting (IO) as a reference plot. Depletion in soil moisture content was measured gravimetrically over a range of depths in the laboratory as well as over the specified site conditions where seeds (100 per 90 cm2) had been sown. Seedling germination, survival, water potentials (c), and relative water contents (RWC) were also monitored. Seed production proved stable interannually, averaging 25–27 m2 year1 with 42–44% viability. Seed gravity dispersal fell off exponentially from the edge of a 70-year-old pine stand, approaching zero at a distance of 80 m based on the relationship equation developed between seed number and distance from the forest edge. With irrigation, 90% of the sown seed germinated; without irrigation <40% germinated. Subsequently, seedling survival following germination was 99% in the IO treatment, 0% on OG, 32% on CC, and 8% on CG. Differences in seedling mortality were attributed to the degree that they experienced water stress; seedling death was recorded at c < 5.0 MPa and RWC <50%. P. densiflora has advantages in being able to survive in its native habitat by adaptation to withstand a long season (November–June) of little precipitation and to take quick advantage of improved growing conditions following spring rains. # 2004 Elsevier B.V. All rights reserved. Keywords: Germination; Human disturbance; Pinus densiflora; Relative water content; Seed dispersal; Seed production; Seedling survival; Water potential
1. Introduction Pinus densiflora S. et Z. (Korean red pine) is distributed over the Korean Peninsula, the Japanese *
Corresponding author. Tel.: þ82 2 970 5666; fax: þ82 2 970 5822. E-mail address: [email protected] (C.S. Lee).
Archipelago, and in Shandong and Manchuria provinces of China (Critchfield and Little, 1966). The pine forests had occupied about half of the forested area in Korea several decades ago (KFS, 1971) and currently occupies one-third of the area (KFS, 2002). This pine produces pollen that is wind dispersed (Kang, 1999). It takes 3 years to complete its reproduction cycle (Singh, 1978): female bud formation is
0378-1127/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2004.05.053
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initiated in the summer, pollination occurs the following spring, and seeds maturate in the fall a year later. After 40–60 years, relative growth in diameter and height slows as a log-normal (Lee and Kim, 1989). Cone production may begin at 7 years in isolated tree; it is delayed to 11—18 years when trees form stands (Lee and Kim, 1989). On exposed rocky ridges, some trees survive to ages beyond 140 years (Lee, 1995a). According to pollen analysis, pine forests replaced deciduous broad-leaved forests about 2300 years ago in the southwestern part, and 1400 years ago in the eastern part of the Korean Peninsula (Kim, 1980; Choi, 1998). This range expansion was in response to an increase in fire frequency associated with rising temperatures and agricultural activities (Kim, 1980; Choi, 1998). The persistence of these temperate pine forests in Korea has been speculated to be a result of the pine’s adaptation to and dependence upon dry weather from fall through spring (Kim, 1980; Lee and Kim, 1987; Lee and Lee, 2003), the availability of large areas with coarse-textured soils (Lee and Kim, 1987; Lee and Lee, 2003), and frequent disturbance by human activities (Kim, 1980; Lee and Hong, 2001). Disturbances were envisioned as creating gaps in the forest canopy and exposing bare soil that favored seed germination while coarse-textured soils would induce drought sufficient to limit competition from oak and other species (Lee, 1995a, b; Lee and Lee, 2003). With a shift toward fossil fuels for heating homes, the kinds of disturbances that once perpetuated Korean red pine are now lacking (Lee and Hong, 1998, 2001). Whether clear felling, or other alternatives might serve the same role as fire is a question worth addressing. In areas where native forests have been highly fragmented, such as in Korea, it is useful to evaluate life history attributes of a species in reference to its competitors. The critical stages in a plant’s life cycle are those having to do with reproduction, seed dispersal, germination, and seedling establishment (Kavanagh and Carleton, 1990). If conditions for successful regeneration occur infrequently, then successful maintenance of a population is less assured because a favorable seed year must correspond with an appropriate disturbance. Knowledge of interannual variation in seed production and the distribution of age classes of trees can address the importance of synchronous events in perpetuating tree populations
(Grubb, 1977; Urbanska, 1997). Adequate dispersal is necessary to occupy new habitats and to expand a population (Angevine and Chabot, 1979; Solbrig, 1980; Brown et al., 1988). Although seeds may germinate, seedling establishment may occur only under specific microclimatic and edaphic conditions that provide adequate moisture, light, and nutrients, without harmful pathogens and herbivores (Harper et al., 1965; Urbanska, 1997). Although most species in the genus Pinus grow well under high radiation (Koyama, 1943; Shirley, 1945), the initial establishment stage is more sensitive to the availability of soil moisture than radiation (Koyama, 1943; Oosting and Kramer, 1946). Because the Korean Peninsula customarily experiences a long dry season from fall to spring (KMA, 2001), we shall place special emphasis on monitoring plant water stress and root growth at the time of germination and seedling establishment. Our specific objective in this study was to explore the establishment phase of Korean red pine forests by quantifying: (1) interannual variation in seed production and viability, (2) the distance that wind-blown seed travels from the edge of a forest, (3) how seed germination varies under different light and soil conditions, and (4) how variation in soil moisture content affects seedling water relations and mortality.
2. Study areas Three separate areas were utilized in this study. To assess seed production and dispersal, we chose mature Korean red pine forests at Tdantduk (site 1–1: 12682100 320 E, 3683000 140 N) and Butdugi (site 1–2: 12682000 240 E, 3683300 420 N) of Seungun-ri, Anmyuneup, Taean-gun located in the central western Korea. ‘‘Gun’’ is an administrative unit, which corresponds to a county, and ‘‘ri’’ is the smallest administrative unit, which corresponds to a village. Sites take locality names from the corresponding hamlets. The stand was composed of ca. 70-year-old trees, averaging 16 m in height with a stocking of 780 trees ha1. Canopy coverage averaged more than 80%. The soil has a loamy texture derived from a sedimentary metamorphic parent material (Millar and Turk, 1965). Soil profile was well developed with litter, A, and B horizons of 1.5, 2.1, and 25.5 cm thick,
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Fig. 1. Mean monthly trends in precipitation (P) and potential evapotranspiration (PE) for the Taean, Seoul, and Suwon regions show similar water balances with deficits in May and/or June of the year. Potential evapotranspiration was estimated using the Thornthwaite equation (Thornthwaite and Mather, 1957). Data were derived from meteorological summaries between 1950 and 1980 (KMA, 1984).
respectively. Organic matter content and field capacity were 5.5 and 23.7%, respectively. In another pine stand of similar age, structure, and site conditions, located 4 km distant from where seed production was studied, a clear cut provided an exposed edge of the forest, below which an open area was available for us to quantify seed dispersal. Germination and seedling survival were investigated on pine stands with different canopy conditions located at Mt. Kwanak, Seoul (site 2: 12685700 400 E, 3782700 180 N) and Imok-dong, Suwon (site 3: 12685900 360 E, 3781900 320 N). Trees at both sites were 30–40-years-old but those at site 2 grew more slowly than at site 3. The height of the stands on Mt. Kwanak averaged 8 m high with a stocking of 1150 trees ha1 where the height of stands at Imok-dong averaged 11 m with a stocking of 1230 trees ha1. Canopy coverage of both stands ranged between 75 and 80%. Although climatic conditions in regard to monthly water balances at the two sites appear similar (Fig. 1), the coarser textured sandy soil at site 2 is more dry prone than the loamy soil found at site 3 (Millar and Turk, 1965). These differences reflect the physicochemical properties of the slightly different parent materials, a granite at site 2, and a gneiss at site 3. The soil at Mt. Kwanak lacks an A horizon and is very shallow with the litter depth of only 1.3 cm and B horizon 16.5 cm thick. Organic matter content and field capacity were 2.5 and 21.5%, respectively. The soil at Imok-dong has a moderately well developed soil profile with litter, A, and B horizons of 2.1, 1.8, and 23.5 cm thick, respectively. Organic matter content and field capacity were 4.8 and 27.3%, respectively.
In addition to studies in canopy gaps under the forests on Mt. Kwanak, Seoul, we increased the range of microhabitats to include: (1) open ground, OG (100% light intensity) with a very shallow soil below 5 cm, (2) canopy gap, CG (30:2 5:9% light intensity) and (3) closed canopy, CC (3:5 1:7% light intensity). An irrigated treatment in the open (IO) was prepared by adding sandy loam soil, gathered from the nearby forest, to a depth of 30 cm, equivalent to that of the CG and CC plots. The IO treatment was watered at 2-day intervals throughout the experimental period and served as a reference to compare seed germination, and survival of seedlings in other treatments. The distribution of precipitation and seasonal patterns in evaporative demand were similar across three all study sites, showing modest water deficits in May and/or June with a significant surplus of water during July and August (Fig. 1; KMA, 2001).
3. Methods 3.1. Seed production and dispersal Seed production was tallied at site 1–1 by counting the number of seeds fallen into twelve 1 m2 seed traps made from nylon netting that were positioned 1 m above the soil surface. Seeds were collected over 3 years from 1 May 1985 to 30 April 1987. Seed dispersal was measured using five seed traps per point, set at 0, (beneath the seed source), 5, 10, 20, 30 and 40 m distance from the exposed edge of the 70years-old stand at Butdugi, Taean.
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3.2. Emergence and survival of seedlings on forest floor One hundred seeds were sown on the surface and at 1.0 cm depth at the 30–40-year-old stands at 3 cm 3 cm spacing on 6 April 1985. All seedbeds were covered with a 0.5 cm thick layer of pine litter and had five replicates. The survival of seedlings was measured by tallying the number of live seedlings at 1week intervals from the 5th week after sowing. The survival of seedlings occurred naturally was investigated by applying the same methods as the abovementioned case from early May when seed germination was completed to August at both Mt. Kwanak and Imok-dong. 3.3. Plant water potential and relative water content A greenhouse study was conducted at the Seoul National University to define critical soil moisture contents and corresponding plant water potentials (c) and relative water contents (RWC) that limit survival. A total of 1000 pine seeds were planted in 40 pots and allowed to germinate and grow for 3 months. At the end of 3 months, half of the pots received no additional water, while the other half continued to be irrigated. Water potentials were determined by the Shardakov dye method (Barrs, 1968). This method involved placing tissue samples into tubes with a range of solutions of known osmotic potential. Tissues that are not in equilibrium with the osmotic solution will change the concentration of the solution by losing or taking up water. A drop of dye extracted from a separate set of osmotic solutions will, when released by a pipette in the middle of a tube with tissue at equivalent water potential to the osmotic solution, remain suspended where released; when the tissue is not in equilibrium with the surround osmotic solution the dye will sink or rise. c measurements were taken between 7:00 and 8:00 a.m. on the first and second leaves of seedlings at periodic intervals thereafter until wilting was observed 46 days later. RWC was determined on first and second leaves by measuring the fresh weight of samples placed within a weighing bottle as soon as sampled, the turgid weight of samples suspended in natural water at 25 8C for 10 h under a 30 W incandescent lamp set at 30 cm
distance from the sample, and the dry weight of samples dried at 80 8C for 48 h. RWC was calculated as the difference between fresh and dry weight divided by the difference between turgid and dry weight, multiplied by 100 to convert to percent (Catsky, 1972). 3.4. Root length Root samples were attained by destructive sampling of five seedlings. Length of the taproot was measured with calipers to 0.05 mm precision. 3.5. Relative light intensity Light intensity was determined using a LICOR Model LI-185A photometer and a LI-190X quantum sensor. Relative light intensity for each site was calculated in reference to measurements made in the open. Each measurement was replicated five times along a transect at random distances. 3.6. Soil environmental factors The thickness of each soil horizon was determined after being exposed with a sharp flat-tipped spade. Soil samples were collected from mineral soil at a depth within 5 cm from the ground surface considering OG seedbed with the shallowest soil depth below 5 cm at 1-week intervals during June, the peak of dry season. Soil moisture contents (SM) were determined on the samples gravimetrically (n ¼ 5 at each depth) with a chemical balance (0.01 mg precision) and a forced air-drying oven set at 105 8C for 48 h. Organic matter content was determined from ash-free dry weight after ignition in muffle furnace of 600 8C for 4 h (Peters, 1973). Field capacity was determined following standard procedures (Broadbent, 1973). 3.7. Statistical analyses All statistical analyses were carried out using SAS (SAS Institute, 1989). Analysis of variance (ANOVA) was performed to compare soil moisture, and germination among plots. t-tests were made when making individual comparisons of germination rates at ground surface and 1 cm depth; Tukey’s honestly significant difference method was employed when making multiple comparisons among means. Regression analyses
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were used to describe the relation between seed dispersal and distance from seed source.
4. Results 4.1. Seed production Annual seed production in the 70-year-old pine forest was consistent, ranging from 25 to 27 seeds/ m2 with a viability averaging between 42 and 44% (Table 1). Seed fall and seed viability varied seasonally, with the highest values recorded in both cases in October and November every year (Table 1). 4.2. Seed dispersal The number of seeds collected in traps set at varying distances from the seed source decreased exponentially out to 40 m (Fig. 2). The exponential relationship developed between seed number and distance from the edge of the forest indicates by extrapolation that the maximum seed gravity dispersal would be about 80 m.
Table 1 Interannual seed production recorded under a 70-year-old Korean red pine stand Period
1985 May–September October November December–April Subtotal 1986 May–September October November December–April Subtotal 1987 May–September October November December–April Subtotal
Seeds collected Germinated Germination from twelve seeds percentage 1 m2 seed traps 53 70 66 112 301
10 42 47 28 127
18.8 60.0 71.2 25.0 42.2
49 61 58 153 321
31 41 38 32 142
63.3 67.2 65.5 20.9 44.2
42 62 106 86 296
5 36 68 17 126
11.9 58.1 64.2 19.8 42.6
Fig. 2. Changes of the number of seeds fallen in seed traps installed by distances from seed source stand. Equation on graph indicates relationship between distance and the number of seeds collected at each distance.
4.3. Germination Germination of seeds sown on the soil surface varied from a high of 90% on the irrigated open (IO) treatment to a low of 19% on the OG treatment. Germination rates on the CG and CC seedbeds were, respectively, 30 and 42% in 6 weeks after sowing (Table 2). Germination rates of seeds placed at 1 cm depth followed a similar response on the different seedbeds with only the OG and CG showing a significant difference from that measured on the soil surface (Table 2).
Table 2 Mean (%) and S.D. of seed germination from 100 per 900 cm2 that were sown on the soil surface and at 1 cm depth across a range of selected seedbeds Seedbeds
Germination rate (%) Soil surface
Irrigation, full exposure Open ground Canopy gap Closed canopy
89.8 19.2 30.0 42.0
3.9 4.1 4.0 3.4
P
1 cm depth 90.2 29.6 40.0 42.4
4.4 5.3 5.0 3.6
0.88 0.0001 0.0005 0.88
Significance of differences between soil surface and 1 cm depth plots are indicated with P values based on t-tests.
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Fig. 3. Survivorship curves of seedlings germinated on the different seedbeds on forest floor of the Korean red pine stand. Irrigated and exposed with soil supplement (IO), open ground (OG), canopy gap (CG), and closed canopy (CC).
4.4. Seedling survival under a range of seedbed conditions Of those seeds that germinated, survival varied from 99% on IO treatment to 0% on open ground (OG) (Fig. 3). The best survival without irrigation was observed under the closed canopy (about 30%), although growth of seedlings (not shown) was higher for those that survived in canopy gaps. Seedling survival naturally occurred on the forest floor of the pine forests at Seoul abruptly decreased to <10% near the end of June, whereas those in Suwon decreased more slowly and remained >70% (Fig. 4). These differences in responses between the two locations are interpreted as responses to differences in soil texture rather than climatic condition.
Fig. 4. Survivorship curves of seedlings germinated on forest floor of 30–40-year-old the Korean red pine stand in Seoul and Suwon. The poorer survival at Seoul compared to Suwon region is associated with
4.6. Water potential and relative water content of seedlings Under full exposure with irrigation (IO), water potentials of first and second leaves remained above
4.5. Soil moisture contents under a range of seedbed conditions For all seedbeds but the irrigated treatment, soil moisture contents in the upper 5 cm fell below 5% at the peak of drought in June (Fig. 5). The small differences in moisture content, even if they were significant, probably do not represent real differences in minimum soil water potentials (Philip, 1957), as the organic matter content varied slightly, with the highest under the CC treatment.
Fig. 5. Comparison of soil water contents averaged for the upper 5 cm of soil during the peak of drought in June under seedbeds exposed to different radiation loads: open ground (OG), irrigated (IO), open ground with a soil depth supplement to 30 cm, canopy gap (CG), closed canopy (CC). The letters indicate significant differences among means (n ¼ 5) at P ¼ 0:05 using the Tukey’s honestly significant difference method.
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Fig. 6. Comparison of seasonal changes in averaged leaf water potentials (c) and relative water contents under irrigated and nonirrigated fully exposed conditions.
0.9 MPa, with RWC at 91% throughout the greenhouse experiment. Without irrigation, water potentials began to drop within 30 days and reached a lethal point (5.1 Mpa) with a RWC of 54% by 45 days without irrigation (Fig. 6). 4.7. Root growth and vertical distribution of soil moisture Under closed canopy forests, current year seedlings extended their roots on average to a depth of 3.7 cm by
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Fig. 7. Seasonal pattern in root growth of current year seedlings germinated on the forest floor under a closed canopy of 30–40year-old Korean red pine.
May, with a further extension to below 7 cm by the peak of drought in June (Fig. 7). To avoid lethal water stresses, seedlings must reach more moist soil conditions than available in the upper 7 cm of soil, as was shown by those seedlings that survived drought stress in all non-irrigated experimental seedbeds. In fact, soil moisture contents measured at 1-week intervals during June were getting moisten as soil depth increased and exceeded 6%, which can be assumed as above critical level of water potential and RWC, from 9 cm depth (Fig. 8; Newman, 1966).
Fig. 8. Vertical distribution of soil moisture contents measured at 1-week intervals during June, the peak of dry season under a closed canopy of 30–40-year-old Korean red pine.
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5. Discussion 5.1. Seed production and dispersal Our observations over 3 years indicate minimum variation in seed production year to year (Table 1). It is possible that variation might still be encountered with a longer record of observation but from our limited study we conclude that a fair seed fall could be expected every year. This assumption is shared by foresters in their general reliance on seed trees following harvest activities (Lee and Kim, 1989; Bae, 1994; Kang et al., 2004). With distance from the seed source, the number of seeds caught in traps decreased rapidly with >50% recorded not more than 5 m from the stand edge and none expected to be wind-blown beyond a distance of 80 m (Fig. 2). Mean distance among seed trees in a silvicultural treatment, which have practiced in Korea, was 10–15 m. The further the distance among seed trees, the longer the time was required for recruitment of seedlings (Lee et al., 2004). The results from this study suggest that the distance should be reduced to shorten the period required to reach the optimal density in the silvicultural practice and further, to get satisfactory timber production. Seed dispersal may be affected by several variables: (1) the height of the seed tree, (2) the aerodynamic characteristics of the seed such as its weight, possession of wings, plumes, etc., (3) the effectiveness of distribution, a function of wind direction and velocity for pine seeds, as well as the presence and activities of animal vectors (Harper, 1977; Augspurger, 1986; Kang, 1999). 5.2. Environmental factors affecting germination and seedling survival Field experiments carried out on the forest floor under pine stands with different canopy conditions indicate that germination and seedling survival depend on the water content of each seedbed (Table 2; Figs. 3 and 5). In addition, germination percentages at 1 cm depth were somewhat higher than those on the soil surface in the OG and CG treatments (Table 2). No differences were observed with the IO treatment where the surface conditions did not dry out, or with the CC treatment where the
dense forest canopy reduced surface evaporation by intercepting >97% of the short-wave radiation and by reducing wind velocity to a minimum (Brandle et al., 1988). Further, seedling survival in Suwon with fine textured loamy soil was higher than that in Seoul of coarser textured sandy soil. In this respect, differences in germination and seedling survival among seedbeds in Seoul and between Seoul and Suwon would be attributed to the degree of water stress that they experienced. 5.3. Relationship between water deficits and seedling mortality The lethal water potentials of Korean red pine seedlings, 5.1 MPa, were far lower than those of other species of pine (1.0 to 1.9 MPa) or Picea spp. (1.8 to 2.2 MPa) (Richter, 1976). The lethal c of P. densiflora was nearly as low as that of Juniperus spp. (5.9 MPa) adapted to semi-desert environment (Richter, 1976). Korean red pine seedlings have been shown to survive drought for 45 days longer than competing oak species (Kim, 1990). The result resembles the former results that conifers usually have stronger drought resistance than broad-leaved trees (Jarvis and Jarvis, 1963; Hellkvist et al., 1974; Waring and Running, 1976). Although pine seedlings can tolerate considerable drought, their survival still requires that roots extend into the deeper soil below 9.0 cm to attain sufficient water or, alternatively, that cuticular transpiration is minimized once drought is imposed so that seedlings do not reach lethal relative water contents and water potentials. Korean red pine exhibits rapid root growth and a tolerance for drought that makes this species adapted to survival on coarsetextured soils throughout its native range. Even so, under similar climatic conditions (Fig. 1), survival can differ from region to region based on differences in soil texture (Fig. 4). In summary, water deficit in the spring appears to be the dominant cause of mortality of pine seedlings (Figs. 3 and 4). Differences in tolerance to desiccation among competing species govern the distribution and dominance of Korean red pine (Lee and Lee, 2003). Without a drought period and coarse-textured soils, most areas of the Korean Peninsula would be forested with deciduous broad-leaved species. With a shift in use of forest for fuel, the disturbance pattern has been
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altered (Lee and Hong, 1998, 2001). Clear cutting is not conducive to successful natural regeneration of the pine, although bare-rooted stock, if properly prepared and planted, might survive adequately. To achieve natural regeneration, our research indicates that a light to moderate partial cut would favor establishment because the seedbed conditions created would be less extreme than those encountered in more open, exposed seedbeds (Bae, 1994).
Acknowledgements We would like to thank Dr. R.H. Waring and Miss S.J. Wessell of the Oregon State University for a critical review of an earlier draft of this paper.
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