New Forests (2006) 32:33–49 DOI 10.1007/s11056-005-3391-1
Springer 2006
-1
The effects of seed mass on germination, seedling emergence, and early seedling growth of eastern white pine (Pinus strobus L.) WILLIAM C. PARKER1,*, THOMAS L. NOLAND1 and ANDRE´E E. MORNEAULT2 1
Ontario Ministry of Natural Resources, Ontario Forest Research Institute, 1235 Queen St. E., Sault Ste. Marie, Canada ON P6A 2E5; 2Ontario Ministry of Natural Resources, Forest Research and Development Section, 3301 Trout Lake Rd., North Bay, ON, Canada P1A 4L7; *Author for correspondence (e-mail:
[email protected]; phone: 705-946-7424; fax: 705-946-2030) Received 4 March 2004; accepted in revised form 22 September 2005
Key words: Natural regeneration, Biomass partitioning Abstract. Half-sib seed of several eastern white pine (Pinus strobus L.) families was used to examine seed mass effects on laboratory germination, and seedling emergence and growth under moderate and low light (47 and 13% full sunlight) in a greenhouse. Percent germination and speed of germination under laboratory conditions were not related to seed mass among half-sib families or multi-family seedlots bulked by seed mass. Percent seedling emergence in the greenhouse was not related to seed mass, but families with heavier seeds exhibited faster emergence. Both rate and percent emergence were significantly increased under low light. Family differences in leaf, stem, root, and total seedling dry mass, primary root length, and the number of first-order-lateral-roots were positively related to seed mass in both light environments. Low light diminished the absolute biomass increment per unit seed mass, but the proportional change in biomass with seed mass was similar between light environments. Rate of emergence also influenced seedling size within families, with earlier emergence increasing seedling dry mass from 7 to 58%, dependent on light environment. Biomass partitioning coefficients were influenced by light environment but largely independent of seed mass.
Introduction Intraspecific variation in seed mass is common in forest tree species (Baldwin 1942; Righter 1945; Bonner 1987). In conifers, seed mass varies 3–5-fold among and within individuals due to positional, environmental, internal, and genetic factors that influence seed development (Baldwin 1942; Ehrenberg et al. 1955; Sarvas 1962). Seed mass has a strong influence on seedling establishment, with heavier seeds often exhibiting more rapid emergence, larger initial seedling size, and/or a higher capacity for survival of environmental hazards (Righter 1945; Bonner 1987; Farmer 1997). Studies of several woody species indicate that heavier seeds may improve emergence through deep litter layers and increase seedling size and survival under low light, thereby favouring establishment in shaded, competitive microsites (Bonfil 1988; Tripathi and Khan 1990; Paz and Martı´ nez-Ramos 2003). Conversely, smaller seed of some species form
34 seedlings of lesser size but an initially higher relative growth rate, perhaps adaptive for establishment in more open, disturbed microsites with abundant growth resources (Tripathi and Khan 1990; Houssard and Escarre´e 1991; Paz and Martı´ nez-Ramos 2003). Because seedling establishment is dependent in part on the interaction between seed mass and microsite, it has been hypothesized that the formation of a ‘seed shadow’ with a wide range in seed mass may be an adaptation to maximize establishment within heterogeneous environments (Janzen 1977; McGinley et al. 1987). To date, the ecological role of seed mass on natural regeneration of tree species has received little attention, and few studies have been conducted in a field setting (Tripathi and Khan 1990; Jones et al. 1997; Seiwa 2000; Paz and Martı´ nez-Ramos 2003). However, several controlled environment studies have demonstrated that seed mass effects on germination and early seedling growth are modified by resource availability (Wrzeœniewski 1982; Wright et al. 1992; Surles et al. 1993; Khurana and Singh 2000), suggesting that microsite may influence the expression of seed mass effects on natural regeneration. Poor seedling recruitment in white pine-dominated forest ecosystems of the Great Lakes region of North America has resulted in successional displacement of white pine by more fire sensitive, shade tolerant species (Carleton et al. 1996; Frelich 2002). This is attributable in part to replacement of recurrent, low to moderate intensity surface fire by harvesting activities as the primary disturbance agent of these ecosystems (Heinselman 1981; Frelich 2002). Presently, the shelterwood silvicultural system in combination with some form of forest floor disturbance is commonly used both to emulate disturbance by wildfire, and to create an understory environment conducive to the establishment and growth of white pine regeneration (Wendel and Smith 1990; Pinto 1992). Moderate light (50% full sunlight) beneath partial overstory canopies promotes the establishment and height growth of white pine natural regeneration, but the ecological relevance of the interaction between light and seed mass is unknown. This relationship may be particularly important to seedling recruitment since initial seedling size has a prominent influence on the outcome of competition under light limited conditions (Wilson 1988). In an effort to better understand the factors that limit regeneration of white pine, we examined the influence of variation in seed mass on natural regeneration. Because of inconsistencies in results and differences in sample size and methods of previous examinations of white pine (Mitchell 1939; Spurr 1944; Wright 1945; Pauley et al. 1955; Genys 1968; Demeritt and Hocker 1975; Sayward 1975) we conducted a comprehensive re-examination of seed mass effects in this species in a series of laboratory, greenhouse, and field experiments (Parker et al. 2004; Noland et al. 2005). In this report, we present the results of studies that examined the influence of seed mass on: (1) laboratory germination and (2) seedling emergence, growth, and biomass partitioning under moderate (47% sunlight) and low (13% sunlight) light conditions
35 selected to represent the understory of uniform shelterwoods and closed canopy stands, respectively, of white pine-dominated forests.
Materials and methods Seed source and processing White pine seed was collected from 195 trees in two second-growth, mixed pine-hardwood stands in central Ontario to assess sources of variation in seed characteristics of this species (Noland et al. 2005). Seed was extracted from cones and X-rayed to identify sound, fully developed seed (Simak 1980). Average seed mass per parent tree was determined by bulk measurement of a known amount (‡100) of sound seed. Seven half-sib families with bulk averaged seed mass that ranged from 13.6 to 26.6 mg were selected for study. Mean seed mass for each family was determined by weighing individual, sound seeds (n = 50–100). A limited amount of seed from two families necessitated the use of a different subset of five families for the laboratory and greenhouse components of this experiment.
Laboratory seed germination The effect of seed mass on germination under laboratory conditions was examined using 400 sound seeds from each of five families. Seed was soaked in deionized water for 24 h, drained, transferred to plastic bags, and stored at 2 C for 75 days (Schopmeyer 1974). After stratification, eight groups of 50 seeds of each family were sealed in plastic Petri dishes containing filter paper moistened with deionized water. Dishes were placed in a controlled environment chamber programmed to provide 75% relative humidity, a 16/8 h light/ dark photoperiod, and an 8/16 h, 30 C/20 C air temperature regime. A 16/ 8 h light/dark photoperiod was used instead of the conventional 8 h light period, since this longer photoperiod promotes seed germination of eastern white pine (Farmer 1997). Lighting was provided by both cool, white fluorescent and incandescent bulbs. Germination, defined as radicle protrusion and geotropic curvature, was assessed every 3–4 days for 28 days. To minimize any genetic effects on laboratory germination characteristics, a second laboratory assessment was conducted using composite seedlots. Three bulked seedlots were created by combining cleaned seed (n = 520) from 10 trees with small (12–16 mg), medium (17–20 mg), and large (21–25 mg) seed. Only trees with >80% sound seeds as determined by X-radiography of seed subsamples were selected. Forced-air gravity separation was used to remove empty and immature (i.e., seed with 98% of immature seed were removed by this
36 method. After cleaning, 100 seeds of each composite seedlot were individually weighed. The mean (±standard deviation) seed mass of the small, medium, and large seedlots was 15.4 ± 0.2, 19.3 ± 0.2, and 23.8 ± 0.2 mg, respectively. Seedlots were stratified and laboratory germination tests conducted as described above. For all laboratory germination tests, mean percent final germination was calculated from cumulative values on the final day of assessment (i.e., day 28). The speed of germination was estimated using the peak value (PV) and germination value (GV) of Czabator (1962), and the number of days until 50% germination of viable seeds occurred (R¢50) (Thomson and El-Kassaby 1993). Peak value is the maximum quotient of percent cumulative germination and day during a germination test. Germination value is the product of PV and the mean number of germinants observed per day (i.e., final percent germination/ 28 days).
Greenhouse environment White pine seedlings were grown in two adjacent, environmentally controlled greenhouse cubicles, each containing two benches. Greenhouse lighting was provided by natural sunlight and high pressure, sodium vapour lamps suspended 1.5 m above the benches. Blackout curtains were used to provide a 14 h photoperiod. Each bench was divided into a moderate and low light environment. The moderate light treatment consisted of ambient light conditions in the cubicle. The low light environment was created using a wood frame structure covered with spectrally neutral shadecloth that reduced transmittance of ambient photon flux density (PFD) by 50%. Mean daily PFD as a percent of full sunlight for each light environment, estimated using a model LI-191SA Line Quantum Sensor (LI-COR Inc, Lincoln, NE, USA) and the method of Messier and Puttonen (1995), averaged 47.2% in the moderate and 12.6% in the low light environment, very similar to that reported for shelterwood and undisturbed white pine stands, respectively (O’Connell and Kelty 1994, Burgess and Wetzel 2000). Maximum height growth of white pine, an intermediately shade tolerant species, occurs at about 50% of full sunlight (Logan 1966, Groninger et al. 1996). Seedling height growth is significantly reduced as PFD falls below 25%, with mortality increasing as PFD drops below 5–10% sunlight (Kobe et al. 1995, Canham et al. 1996, Groninger et al. 1996).
Seedling emergence, growth, and morphology Seed mass and light effects on seedling emergence and growth were examined using sound seed from five families. Stratified seed (n = 23–33) from each family were sown to a depth of 1 cm (one seed per cell) in six, multi-celled planting containers filled with fine sand. Two containers per family were
37 randomly arranged in the moderate and low light environments on each of three adjacent greenhouse benches. Emergence was recorded daily for 28 days and PV, GV, R¢50, mean day of emergence, and percent final emergence calculated for each planting container. Seedlings were grown for 8 weeks and irrigated as needed to maintain the soil moisture content near field capacity. Air temperature in the light/dark period was maintained at 25 C/15 C. After 8 weeks of growth, seedlings were removed from the planting cells. Root systems were gently washed free of sand, and primary root length (maximum vertical extension of the root system) and the number of first-orderlateral-roots ‡ 1 cm in length (FOLR) were measured. Seedlings were then separated into roots, stems, and foliage and dried at 65 C for 48 h to determine the dry mass of these seedling biomass components. A significant linear relationship was exhibited between seedling dry mass and leaf, root, and stem dry mass for each light and family combination. The relative partitioning of seedling biomass was estimated by the ratio of organ to total seedling biomass (g g1) and reported as leaf mass ratio (LMR), stem mass ratio (SMR), and root mass ratio (RMR).
Statistical analysis Laboratory seed germination data of single tree and bulked seedlots were analyzed using the General Linear Model (GLM) procedure of SAS and oneway analysis of variance (ANOVA), with family (F) as a fixed factor (SAS Institute, v. 8.0, Cary, NC, USA). Seedling emergence data were analyzed using the GLM procedure, ANOVA, and a split-plot experimental design, with light treatment representing the whole plot, and family being the subplot (Anderson and McLean 1974). A mixed general linear model Yijkl ¼ l þ Bi þ LJ þ BLij þ Fk þ BFik þ LFjk þ BLFijk þ eðijkÞl
ð1Þ
with family and light environment (L) classified as fixed factors, and block (B) (i.e., bench) as a random factor. Percent final emergence was transformed to the arcsine of its square root prior to ANOVA to stabilize variance. This model accounted for 50% of the variation in percent emergence and >70% of the variation in PV, GV, R¢50, and mean day of emergence. Mean comparisons of family and light effects on seedling emergence were performed using a Fisher’s Least Significant Difference (LSD) test and type III sums of squares where ANOVA indicated main treatment effects were significant (p < 0.05). The effects of family and light environment on seedling biomass components, primary root length, and biomass partitioning coefficients were analyzed using the GLM procedure, ANOVA, and the same general linear model. This model accounted for about 46% of the variation in LMR and ‡76% of variation in remaining variables. A LSD test was used for mean comparisons as described above. Because descriptive statistics indicated FOLR data were not
38 normally distributed, seedling ranks by block, ANOVA and Freidman’s test were used to assess treatment effects (Glantz 1992). Linear regression analysis and the REG procedure of SAS (SAS Institute, v 8.0, Cary, NC, USA) were used to quantify the effect of light on the relationship of seed mass with seedling traits. The effect of light environment on the absolute and proportional change in biomass, root length, and FOLR with seed mass was examined by comparing the slopes of separately fitted regression lines of the two light treatments using the method presented by Neter and Wasserman (1974). The comparative influence of seed mass and rate of emergence on seedling biomass were examined using linear regression analysis and the REG procedure of SAS. Regression equations were generated to define the relationship between the mean values for seedling dry mass and day of emergence for each light by family treatment combination. Values of seedling dry mass associated solely with differences in seed mass were predicted for each family using regression equations and the highest mean day of emergence (i.e., slowest rate of emergence) observed within the low (16.9 d) and moderate (18.1 d) light treatment as the independent variable. The combined influence of seed mass and rate of emergence on seedling dry mass for each family was estimated using regression equations and mean day of emergence observed for each light by family combination as the independent variable. The percent difference between these two predicted values was used as a relative measure of the influence of different rates of emergence on seedling dry mass for a given family.
Results Laboratory germination Laboratory germination began after 7 days in the incubator, was ‡50% complete within 11–14 days, and essentially finished within 21–24 days. Final germination was uniformly high (‡95%) for all families (Table 1). Family had a significant effect on percent germination, PV, and GV, but not R¢50 (Table 1a). Family differences in laboratory germination parameters were not significantly correlated with seed mass. Germination characteristics did not differ significantly among the three seedlots bulked by mean seed mass (Table 1b).
Seedling emergence, growth, and morphology Seedling emergence under greenhouse conditions began 11–13 days after sowing. Light environment had a significant effect on PV, GV, and percent final emergence, with values being higher under low light (Table 2). Family had
39 Table 1. Mean PV, GV, R¢50 and percent final germination under laboratory conditions for (a) five white pine families and (b) three bulked seedlots differing in mean seed mass. Seed mass (mg) (a) Family 13.6a 16.1b 21.8c 24.8d 26.6e (b) Seedlot 15.4c 19.3b 23.8a
PV
GV
R¢50
Germination (%)
5.9ab 6.1a 5.2c 5.8b 5.7b
20.2b 21.7a 17.9c 20.5b 20.3b
12.5a 13.3a 14.0a 12.5a 11.8a
95.5c 99.0b 96.5c 99.3ab 99.8a
5.2a 4.7a 4.6a
18.0a 16.1a 15.6a
14.0a 14.0a 14.8a
96.3a 96.5a 94.8a
Mean values followed by the same letter are not significantly different (p < 0.05).
a significant effect on PV, GV, R¢50, mean day of emergence, and percent final emergence that was independent of light environment (Table 2). Percent final emergence was not related to seed mass in either light environment, but family differences in the speed of emergence were strongly influenced by seed mass, particularly in the low light treatment. Families with larger mean seed mass exhibited more rapid emergence under low light, with seed mass being significantly correlated with PV (r = 0.98, p < 0.01), GV (r = 0.94, p < 0.05), R¢50 (r = 0.92, p < 0.05), and mean day of emergence (r = 0.96, p < 0.01). Strong trends were also exhibited between seed mass and PV (r = 0.86, p < 0.06), GV (r = 0.83, p < 0.08), R¢50 (r = 0.87, p < 0.06) and mean day of emergence (r = 0.83, p < 0.08) under moderate light. Table 2. Mean PV, GV, R¢50, day of emergence, and percent final emergence for five white pine families differing in mean seed mass grown under (a) low and (b) moderate light, and (c) by light treatment for all families combined. Seed mass (mg) (a) Low light 13.6 16.1 20.7 24.8 25.6 (b) Moderate light 13.6 16.1 20.7 24.8 25.6 (c) All families Low light Moderate light
PV
GV
R¢50
Day of emergence
Emergence(%)
4.7d 5.1cd 5.5bc 6.3a 6.0ab
16.5c 17.6bc 19.2abc 22.3a 20.4ab
16.7a 14.5b 14.0bc 13.0c 13.2c
16.9a 15.2b 14.2bc 13.2d 13.5cd
98.0a 97.1a 96.9a 100.0a 95.8a
3.8c 4.7b 4.9ab 5.6a 5.0ab
12.0c 16.2ab 15.4bc 19.5a 17.2ab
18.0a 16.8b 14.3cd 13.5d 15.2c
18.2a 16.8b 14.6d 13.8d 15.6c
85.3b 96.5ab 85.2b 97.0a 95.7a
5.5a 4.8b
19.2a 16.0b
14.3a 16.6a
14.6a 15.8a
97.6a 91.9b
Mean values followed by the same letter are not significantly different (p < 0.05) within (a,b) or between (c) light treatments.
40 Light, family, and light * family generally had significant effects on seedling biomass components and root characteristics (Table 3). Family differences in seedling biomass were strongly related to seed mass under both low and moderate light, with significant positive linear relationships exhibited between seed mass and leaf, root, stem, and total seedling dry mass (Figure 1). Seed mass generally had less comparative influence on root than shoot development, but significant linear relationships were observed between seed mass and root length under low light, and with FOLR in both light environments (Figure 1). Low light reduced the absolute change in leaf, root, and seedling dry mass, and FOLR per unit seed mass, but the relationship of stem dry mass and root length with seed mass was unaffected by light. However, the relative expression of seed mass effects on seedling traits did not differ between light treatments. Seedling biomass was also influenced by the rate of seedling emergence, with significant linear relationships (p < 0.05) between seedling dry mass and day of emergence exhibited in 9 of 10 light by family treatment combinations (Table 4). The daily dry mass increment (i.e., slope value) ranged from 1.9 to 5.9 mg under moderate light and 0.17–1.8 mg under low light. This translates to a 1–9% and 7–10% reduction in mean seedling dry mass for each day emergence is delayed under moderate and low light, respectively, dependent on family. Therefore, larger seedling dry mass of white pine families with higher seed mass was associated, in part, with more rapid seedling emergence of these families. Seedling dry mass normalized to the slowest family mean rate of emergence observed under each light treatment indicate that more rapid emergence accounted for about 7–58% of the difference among families in seedling dry mass (Table 4). Biomass partitioning coefficients did not differ among families but SMR was higher, and RMR slightly lower (p < 0.07) under low light (Table 3, Figure 2). Biomass partitioning coefficients were not related with seed mass under moderate light, but seedlings grown under low light showed a trend toward higher LMR (r = 0.84, p < 0.07) and lower RMR (r = 0.85, p < 0.07) with increasing seed mass. Biomass partitioning coefficients did not vary with day of emergence.
Table 3. Significance probability (p > F) values for light (L), family (F) and light * family (L * F) treatment effects on biomass components, root development, and biomass partitioning coefficients for 8-week-old white pine seedlings. Treatment
Dry mass Leaf
L F L*F a
£ 0.001 £ 0.001 £ 0.001
Primary root length.
Stem £ 0.001 £ 0.001 £ 0.001
Root 0.054 £ 0.001 £ 0.001
RLa
FOLR
LMR
SMR
RMR
0.155 0.048 0.400
£ 0.001 £ 0.001 0.044
0.353 0.632 0.630
0.005 0.820 0.039
0.061 0.489 0.110
Total £ 0.001 £ 0.001 £ 0.001
41
Figure 1. The relationship of seed mass with mean (±SE) leaf dry mass (a), stem dry mass (b), root dry mass (c), total seedling dry mass (d), primary root length (e) and number of first-orderlateral roots (f) for seedlings grown under moderate (solid symbols) and low light (open symbols). Linear regression equations and coefficients of determination (r2) are presented for relationships under moderate (M) and low (L) light. Asterisk following regression equation denotes a significant difference (p < 0.05) in slope between light treatments for a given seedling variable.
42 Table 4. Linear regression equations and coefficients of determination (r2) for the relationship between mean seedling dry mass (Y) and day of emergence (X) for five white pine families differing in mean seed mass and grown under low (a) and moderate (b) light. Seed mass (mg)
Regression equation
(a) Low light 13.6 Y = 21.6 0.17X 16.1 Y = 44.3 1.22X 20.7 Y = 55.7 1.63X 24.8 Y = 62.8 1.77X 25.6 Y = 60.1 1.49X (b) Moderate light 13.6 Y = 63.0 1.91X 16.1 Y = 69.0 1.90X 20.7 Y = 143.6 5.94X 24.8 Y = 107.3 2.79X 25.6 Y = 138.8 4.70X
r2
Observed dry mass (mg)
Normalized dry mass (mg)
Rate of emergence effecta
0.20b 0.81 0.83 0.71 0.73
18.86 25.76 32.55 39.44 40.00
18.86 23.68 28.15 32.89 34.92
0.0 8.8 15.6 19.9 14.5
0.62 0.78 0.93 0.88 0.85
28.43 37.08 56.88 68.80 65.48
28.43 34.61 36.09 56.80 53.73
0.0 7.1 57.6 21.1 21.9
a Rate of emergence effects on seedling dry mass was estimated as the ratio of observed to normalized seedling dry mass expressed as a percentage increase. b p < 0.10.
Discussion The results of this study indicate that although laboratory seed germination characteristics vary among families, seed mass effects on the percent and speed of germination of white pine are minimal under near optimal conditions. Germination of seedlots bulked to diminish any genetic influence also exhibited no relation to seed mass. A previous study of white pine reported that percent germination under laboratory conditions was higher in larger as compared with smaller seed mass within ten single-tree seedlots (Spurr 1944). However, since only empty seed were removed in that study, it is possible that some of the smaller mass seed used may not have had fully mature female gametophytes and/or embryos. The presence of morphologically immature seed with reduced germinability could have depressed mean germination performance of this smaller mass seedlot (Edwards 1980). A higher percent germination in medium mass, as compared with small and large mass seedlots, was reported by Wright (1945), but the methods used are unclear and the seed was not stratified. The absence of empty and immature seed and adequate stratification in the half-sib and bulked seedlots tested in the present study should have minimized the potentially confounding influence of the above-mentioned factors on our results. Percent seedling emergence of white pine in the greenhouse was also unrelated to seed mass, but contrary to the results of our laboratory germination tests, the speed of emergence in the greenhouse was positively influenced by seed mass under low and perhaps moderate light. These conflicting results are not unexpected given the enhanced expression of seed mass effects on
43
Figure 2. Relationship of seed mass with mean (±SE) LMR (a), SMR (b), and RMR (c) for white pine seedlings grown under moderate and low light.
44 germination exhibited under sub-optimal environmental conditions (Dunlap and Barnett 1983; Bonner 1987). Previous nursery bed studies of white pine have reported the absence of (Genys 1968) or positive seed mass effects on the rate of seedling emergence (Spurr 1944; Demeritt and Hocker 1975). Seedling emergence was also favoured under low as compared with moderate light. This agrees with results of field and greenhouse studies where some level of shelter from direct sunlight increased emergence and establishment of white pine seedlings due to improved soil moisture retention and seedling water status (Thomas and Wein 1985, Herr et al. 1999). The strong positive influence of seed mass on family differences in early growth of white pine seedlings observed in the present study was the combined result of larger embryo and energy reserves, the efficient mobilization and use of these reserves, and more rapid emergence of heavier seeds. Other studies of white pine have reported significant seed mass effects on seedling size and biomass components being attributable to larger reserve tissues, earlier emergence of larger seeds, or both (Mitchell 1939; Spurr 1944; Pauley et al. 1955; Genys 1968; Demeritt and Hocker 1975; Parker et al. 2004). Where seed mass effects on speed of emergence of other forest tree species have been reported, the relative contribution of faster emergence to early seedling size varied from negligible (Griffin 1972; Dumroese and Wenny 1987) to substantial (Dunlap and Barnett 1983). Our estimates suggest earlier emergence accounted for an average of 15 and 27% of total dry mass of 8-week-old white pine seedlings grown under low and moderate light, respectively. Seed coat induced dormancy in conifers delays germination and emergence by impeding the expansion and water absorption of megagametophyte and embryo tissues, but can be overcome by stratification for an appropriate period (Barnett 1976, 1997; Campbell and Ritland 1982; Hoff 1987). In the present study, seed were stratified about 2 weeks longer than the 60 days recommended for maximum germination of white pine (Schopmeyer 1974). This extended stratification and the relatively high seed viability (‡95%) observed in our study suggest that differential seed dormancy among families due to insufficient cold storage likely had little influence on speed of emergence. Stronger seed dormancy and delayed germination in some conifers is also related to a higher percentage of total seed mass contained in seed coat tissues (Barnett 1976, 1997). However, variation among white pine families in percent seed coat mass as a factor in the present study is also unlikely since this proportion apparently varies little with seed mass in this species (Mitchell 1939). Instead, more rapid emergence was likely due to higher germinative vigor associated with larger reserve tissues and embryos in heavier seeds. Positive effects of earlier emergence on first-year seedling growth and survival of several temperate woody species were attributed to the competitive advantage accrued from enhanced capture of ephemerally available resources and growing space by earlier germinants (Trimble and Tryon 1969; Tripathi and Khan 1990; Jones et al. 1997; Seiwa 1998). Early emergence may also decrease the vulnerability of seedlings to mortality from some forms of abiotic
45 stress (Larson 1963; Graber 1968; Jones et al. 1997) or from pathogens that are less active in cooler, spring weather (Seiwa 1997, 1998). However, faster emergence may predispose seedlings to damage and mortality by late spring frosts or biotic agents more prevalent early in the growing season (Campbell and Ritland 1982, Barnett 1997). Genetic variation in seed dormancy within species may optimize the timing and speed of speed of germination and emergence to avoid growing season hazards and improve seedling establishment (Levins 1969; Campbell and Ritland 1982; Barnett 1997). The larger absolute increase in seedling biomass per unit seed mass under moderate light conditions likely resulted from the positive influence of higher PFD on the relative growth rate of white pine seedlings (Reich et al. 1998; Parker et al. 2004). As a result, seed mass may have a greater influence on initial size of white pine natural regeneration under the more favourable understory light environment beneath shelterwoods or the more open canopies of shade intolerant northern hardwood species, i.e., paper birch (Betula papyrifera Marsh.) and aspen (Populus sp.) (Frelich 2002; Dovcˇiak et al. 2003). However, the relative expression of seed mass effects on growth, measured as the proportional increase in seedling traits with seed mass, was unaffected by light conditions. This suggests that manifestation of seed mass effects on the size of white pine regeneration is not increased by low light availability. This finding differs from results for several species where low resource availability or competition accentuated seed mass effects on seedling size and survival (Dolan 1984; Wulff 1986; Houssard and Escarre´ 1991; Vaughton and Ramsey 2001). Biomass allocation patterns of white pine seedlings varied only slightly with light environment and seed mass. Stem production was favoured over root production under low light, in agreement with the preferential investment in shoot production in white pine under low light observed previously (Canham et al. 1996; Groninger et al. 1996). A trend toward greater biomass partitioning to leaf over root tissues under low light was exhibited, but seed mass effects on allocation patterns were not as strong as observed for biomass components. Whether this weak relationship is representative of temperate tree species is unclear, as studies of seed mass have examined effects on biomass partitioning only infrequently. Biomass allocation patterns varied with seed mass within some tree species (Wright et al. 1992; Khurana and Singh 2000) while not in others (Reich et al. 1994, Wang et al. 1995), perhaps reflective of the lesser influence of seed mass on partitioning.
Conclusions The mass of sound seed produced by white pine varies 3–5-fold among individuals (Noland et al. 2005) but the influence of seed mass on natural regeneration of this species is unknown. The results of our greenhouse study suggests that white pine germinants arising from larger seeds may exhibit more rapid emergence, larger initial size, and comparatively higher investment in
46 stem relative to root biomass than individuals formed by smaller seeds. Although seedling size was diminished under low light conditions, larger seeds always formed seedlings of higher dry mass, perhaps adaptive for establishment in the moderate shade of partial conifer overstory canopies, or stands of young birch and aspen with relatively open crowns.
Acknowledgements We thank Dianne Othmer, Chris Lyons, Brian Brown, Jeff Kokes, Wanda Nott, Stew Blake, Marc Boudreau, Nick Seymour, Nadia Kucherepa, and Jane Nicholson, Ontario Ministry of Natural Resources, for their assistance, Mike Adams, Canadian Forest Service, for use of the X-ray machine, and Lisa Buse, Ontario Ministry of Natural Resources, for her editorial input. Dr Ben Wang, Canadian Forest Service (retired), and three of four anonymous reviewers provided many helpful comments on earlier versions of this manuscript.
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