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A central tenet of life-history theory proposes a size–number trade-off for offspring (Smith & Fretwell 1974; Godfray & Parker 1991). Indeed, plant life-history theory has attempted to account for the five-order range of seed size found in many communities (Leishman et al. 2000) as a continuum of maternal investment, defined by the extreme cases of many small seeds, each with a low probability of establishment, vs. a few large seeds with high probability of establishment (Venable 1992; Westoby et al. 2002). However, recent evidence suggests that this scenario may be too simple. First, smaller-seeded species may not always have a fecundity advantage: although species with larger seeds do tend to produce fewer seeds per year (Shipley & Dion 1992; Jakobsson & Eriksson 2000), they may have equal or greater lifetime seed production owing to their greater canopy area and more reproductive years (Moles et al. 2004).
Second, larger-seeded species may not always have an establishment advantage. It is true that larger seeds have been observed to better survive stressful environmental conditions including shade (Foster & Janson 1985; Leishman & Westoby 1994b; Osunkoya et al. 1994), drought (Baker 1972; Leishman & Westoby 1994a), deep litter (Molofsky & Augspurger 1992; Vazquez-Yanes & Orozco-Segovia 1992) and damage (Harms & Dalling 1997; Green & Juniper 2004a). However, smaller-seeded species tend to have higher potential growth rates and thus may outgrow seedlings from larger seeds, especially when resources are not limiting (Grime & Hunt 1974; Gross 1984; Maranon & Grubb 1993; Swanborough & Westoby 1996; Bloor & Grubb 2003). Thus, a trade-off between survival and growth rate could result in similar establishment probabilities for seedlings from large vs. small seeds (Gross 1984; Kitajima 1994). Furthermore, because the conditions granting a performance advantage to smaller seeds (e.g. high resources, no stresses) differ from those favouring larger seeds (e.g. low resources, high stresses), seedling establishment probabilities among species differing in seed size are predicted to differ along microhabitat gradients (Grubb 1977, 1996; Westoby et al. 1996). Spatial heterogeneity in microhabitat occurrence would then promote coexistence among species differing in seed size (Geritz 1995; Chesson 2000; Kneitel & Chase 2004).
Recent attention has focused on the mechanisms that could account for such patterns of differential performance among seeds of varying size, with three potential mechanisms receiving significant attention. First, several authors have investigated the ‘reserve effect’ hypothesis, which proposes that larger seeds maintain a greater proportion of reserves in storage as the seedling develops (Westoby et al. 1996; Green & Juniper 2004a). The reserve effect is based on the observation that larger seeds tend to have hypogeal cotyledons with a primarily storage function and these could maintain seedlings under the carbon deficits imposed by shade or tissue loss and the nutrient deficits of impoverished soils (Kitajima 1994; Ibarra-Manriquez et al. 2001). However, Green & Juniper (2004b) found that larger-seeded hypogeal-type species did not invest disproportionately more biomass in resprouting after damage than did smaller-seeded hypogeal species, suggesting that the reserve effect alone cannot explain the influence of seed mass on seedling performance.
An alternative mechanism, referred to by Westoby et al. (1996) as the ‘metabolic effect’, proposes that correlations between seed mass and a suite of other traits are responsible for the observed patterns of performance with seed mass. The slow relative growth rate (RGR) typically associated with larger seed size is taken to indicate inherently lower metabolic rates that permit seedlings to maintain their carbon balance under deep shade or in response to herbivory (see also Green & Juniper 2004a). Because such a strategy of stress or hazard tolerance is associated with other traits correlated with larger seed mass, such as lower leaf-level assimilation rates, lower specific leaf area, greater leaf longevity and higher leaf toughness (Kitajima 1994; Poorter 1999; Reich et al. 1999; Rose & Poorter 2003), this mechanism has been referred to elsewhere as part of a shade-tolerance syndrome (e.g. Poorter & Rose 2005).
Tropical forest tree communities provide an appropriate setting in which to examine the consequences of seed mass for seedling establishment and the underlying mechanisms causing differences in establishment because they encompass the largest range of seed mass among vegetation types reported in the literature (Hammond & Brown 1995; Metcalfe & Grubb 1995). In addition, seed size can differ considerably within species; for example, almost 10% of species exhibit at least two-fold variation in seed size in at least one community (Baraloto 2001).
In this paper we present data from a 5-year field experiment with eight tropical tree species grown from seed, to address both the general hypotheses for coexistence among species differing in seed mass and the mechanistic hypotheses underlying patterns of performance. First, we test for the survival advantage and growth disadvantage of larger seeds predicted by the survival–RGR trade-off hypothesis. Second, we test whether relationships between seed mass and seedling performance (survival, RGR) change along environmental gradients, as predicted by the spatial heterogeneity hypothesis. Finally, we examine the mechanisms underlying correlations between seed mass and seedling performance. In particular, we test the seedling size effect mechanism both among the eight species and within two of the larger-seeded species that each exhibits 10-fold variation in dry seed mass. We discuss the implications for the evolution and maintenance of tree diversity and seed mass variation in tropical forests.
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The experiment was conducted within the Paracou Reserve, near Sinnamary, French Guiana (5°18′ N, 52°55′ W), a seasonal lowland tropical forest with annual precipitation of 3160 mm ± 161 SE. In 1998, we established 120 plots along 12 100-m × 10-m belt transects that were arranged perpendicular to topographic contours to maximize representation of edaphic variability. Plots were established along transects in a random-stratified design; every 10 m along each transect, one square-metre site among the 100 possibilities was chosen using random number tables. No attempt was made either to traverse or to avoid any treefall gaps.
In March 1998, three soil sampling points were established at the points of an equilateral triangle with sides of 50 cm centred within each plot. At each point, litter depth was estimated to the nearest 0.5 cm (Molofsky & Augspurger 1992) and soil surface compaction was estimated using a pocket penetrometer (Forestry Suppliers, Jackson, MS, USA); mean values of the three measures were reported for each plot. One 5-cm-diameter by 10-cm-deep soil core was extracted from beneath the litter layer at each sampling point and then bulked for each plot. Soil moisture content was determined after drying the sample at 60 °C to constant mass. A 50-g subsample of each dried core was transported to the University of Michigan where total carbon, total nitrogen and extractable phosphorus were estimated as described in Baraloto & Goldberg (2004). A principal components analysis (PCA) of variables describing soil properties defined two factors representing 65.1% of the variance: a soil softness factor, with strong contributions from litter depth (correlation = 0.882) and soil surface compaction (−0.847), and a soil richness factor, with strong contributions from soil carbon (0.787), soil nitrogen (0.764), soil phosphate availability (0.727) and soil moisture fraction (0.561). Light availability, estimated as the global site factor (GSF; HemiView software, Delta-T Instruments, UK) using hemispherical photographs at 50 cm height centred within each plot, was orthogonal to other environmental measures, with most sites under closed canopy (Table 1).
Table 1. Summary of environmental characteristics of the 120 plots in the experiment. Plots were selected in a random-stratified design, with one randomly chosen plot each 10 m along 1210 × 100-m belt transects. Shown for each variable is the mean and range (values at 5% and 95%), for measurements made at the initiation of the experiment in March 1998
|Light (% full sun)|| 1.3|| 0.5|| 4.1|
|Litter depth (cm)|| 2.2|| 0.5|| 4.5|
|Soil compaction (MPa)|| 0.11|| 0.03|| 0.20|
|Soil moisture (%)||20.0||13.8||26.6|
|Soil PO4-P (mg kg−1)|| 3.2|| 0.9||10.4|
|Soil C (%)|| 2.61|| 1.43|| 5.46|
|Soil N (%)|| 0.16|| 0.10|| 0.31|
Environmental measures were repeated in March 2000 for six points along six of the 12 transects, and these were used to construct PCA axes describing soil conditions, using the same weightings as those in 1998. We observed no significant change between years in environmental characterizations of these sampling points (Hotellings T2 = 2.19, F3,68 = 0.71, P = 0.551), although overall soil moisture was slightly higher and litter depth was slightly lower in 2000 than in 1998.
Eight focal species were chosen that represent the range of seed mass in the Paracou tree community (Table 2). Seedlings of all eight species have been observed to survive in shaded conditions with less than 1% photosynthetically active radiation (PAR) (Baraloto & Goldberg 2004). In April 1998, seeds of the focal species were collected from at least five adults per species within the reserve. We measured the wet mass of all seeds planted for the three species exhibiting high variation in seed mass (Carapa procera, Vouacapoua americana and Eperua grandifora). Wet seed mass was standardized to dry seed mass using polynomial regression equations (for which r2 varied from 0.87 to 0.94) calculated from at least 30 individuals per species dried to constant mass at 60 °C. For the other five species, the mean dry seed mass of 50 seeds (50 groups of 20 seeds for Jacaranda copaia) was determined.
Table 2. Seed mass for the focal species. Values are the mean dry mass of 50 seeds for Recordoxylon, Dicorynia, Sextonia and Virola, the mean dry mass of 50 groups of 20 seeds for Jacaranda, and the mean of the 720 seeds used in the experiment estimated from polynomial regressions between fresh and dry seed mass for Carapa, Vouacapoua and Eperua
|Species*||Family||Dry seed mass (g) ± SE|
|Jacaranda copaia||Bignoniaceae||0.038 ± 0.003|
|Recordoxylon speciosum||Caesalpiniaceae||0.178 ± 0.024|
|Dicorynia guianensis||Caesalpiniaceae||0.349 ± 0.017|
|Sextonia rubra||Lauraceae|| 1.17 ± 0.04|
|Virola michelii||Myristicaceae|| 1.25 ± 0.11|
|Carapa procera||Meliaceae|| 6.58 ± 0.23|
|Vouacapoua americana||Caesalpiniaceae||12.39 ± 0.37|
|Eperua grandiflora||Caesalpiniaceae||27.61 ± 0.86|
In April 1998, six seeds of each focal species were planted into each of the 120 plots. A 1-m-high wire cage exclosure with 2-cm mesh was installed around each plot, doubled at the base to 20 cm height, to deter mammalian predators from removing seeds. Exclosures were used to avoid the false attribution of mortality to missing seeds that may have been removed by mammalian dispersal agents including Myoprocta acouchi and Dasyprocta leporina. Toothpicks were placed adjacent to smaller seeds to mark their location, and missing seeds were eliminated from subsequent analyses.
All individuals were censused monthly until 4 months from the first planting date, with seven subsequent censuses up to 5 years after planting. Survival was scored only for seeds that had been observed to germinate at a prior census date. In the case of Jacaranda, a species with tegument dormancy, all ungerminated seeds were censused until 8 months from planting, the first date when germinability tests conducted in growth chambers on a subset of 50 of the remaining seeds resulted in no germination. We did not observe field germination of remaining planted seeds after this time.
Seedling RGR for height growth was calculated to permit comparisons with other published field studies (e.g. Clark & Clark 1992) as
- RGR = (ln(height at date 2) − ln(height at date 1))/time interval.
Although height RGR provides a crude estimate for biomass RGR, height and biomass have been found to be well correlated among these eight species in a complementary shadehouse experiment (r = 0.94, P < 0.001; C. Baraloto, D. Bonal & D.E. Goldberg, unpublished data).
For seedling RGR, we performed analyses of covariance on RGR from initial size post-germination (4 months since planting) to 1 and 5 years age, for all individuals surviving to each census date. Individuals were assigned the microhabitat conditions (March 1998 measures) of the plot in which they were planted, as well as their estimated seed dry mass (ln-transformed to meet normality assumptions), as continuous independent variables.
For survival data, we performed logistic regressions with the binary dependent variable of survival at the 60-month census date and the microhabitat principal components and seed size as independent variables. The significance of regression coefficients for independent variables and their interactions was tested using Wald's statistic compared against the chi-squared distribution. We also performed regressions following Cox's proportional hazards model to test the effects of species, seed mass and microhabitat on the dependent variable of time surviving, calculated using the last census date at which an individual was observed to be alive (surviving individuals at the 60-month census were thus censored). These results were concordant with those for the logistic regression; here we present the results of logistic regression because they were also used in the path analysis described below.
To examine the relative contributions of direct vs. indirect effects of seed mass to seedling performance, we performed path analyses. Path analysis is useful for separating the effects of correlated independent variables, such as seed mass and initial seedling size, for which a multiple regression analysis may be inappropriate (Li 1981). We constructed a simple path diagram based on our understanding of causal relationships between seed mass, initial seedling size, survival and RGR. Path coefficients were calculated as the standardized partial regression coefficients for simple and multiple regressions: initial seedling height (at 4 months of age) regressed on seed mass, survival regressed on seed mass and initial seedling height, and RGR regressed on seed mass and initial seedling height. To determine whether these relationships changed during the course of the experiment, we calculated these coefficients using datasets at the 12-month and 60-month censuses. To determine if these relationships were consistent within as well as among species, we also calculated these coefficients for all eight species combined as well as within two species, Eperua and Vouacapoua, for which seed mass varied more than 10-fold and a sufficient number of seedlings survived to permit comparisons.
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Across all species, high mortality occurred during the first 8 months following planting (Fig. 1). However, 5-year mortality rates differed widely among species (Table 3), with more than 99% of Jacaranda seedlings but fewer than 42% of Eperua seedlings dying over 5 years (Fig. 1). Overall, larger-seeded species had higher survival rates throughout the experiment (Fig. 2). All species survived better with increasing light availability, but no other microhabitat factor had a significant effect on survival (Table 3). Furthermore, the effect of increasing light availability on survival was not significantly different between species (Table 3).
Figure 1. Changes in survival and seedling height over 5 years for the eight species planted in the field experiment. Data are the means (± standard error) of six germinating seeds and the corresponding proportion of surviving seedlings planted into each of 120 plots. Species are identified by genus names adjacent to the axes, with rankings of seed mass indicated in parentheses (see Table 2).
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Table 3. Summary of the effects of species, seed mass and microhabitat variables (see text for complete descriptions) on seedling performance. Six seeds of each of eight species were planted across 120 planting sites in which environmental conditions were measured in March 1998. Dry seed mass for each seed (ln-transformed) was entered into the models as a covariate. Survival data were analysed using logistic regression for the 3830 seeds that had germinated within 8 months of planting. Shown is Wald's statistic and corresponding probability values, for species effects and interactions with microhabitat descriptors. Seedling relative growth rates (RGR) for height from 4 to 60 months age were analysed using ancova for the 808 seedlings that survived until the final census date. Shown is the F-statistic with corresponding probability values
|Dry seed mass||1|| 7.46|| 0.006||4.53||0.034|
|Soil softness||1|| 1.22|| 0.27||0.54||0.46|
|Soil richness||1|| 0.45|| 0.50||0.92||0.34|
|Species × Light||7||13.0|| 0.08||1.03||0.41|
|Species × Soil softness||7|| 4.50|| 0.72||0.46||0.86|
|Species × Soil richness||7|| 4.85|| 0.68||0.32||0.95|
Figure 2. Among- and within-species effects of seed size on measures of seedling performance. Dry seed mass was estimated from fresh mass using species-specific regressions from 50 seeds dried at the initiation of the experiment. The leftmost panels compare means (± standard errors) for eight species identified by specific epithet initials. The centre and right panels present within-species effects for Vouacapoua (161 seedlings at 1 year, 84 seedlings at 5 years) and Eperua (413, 251). For survival comparisons within species, individuals were orientated by dry seed mass and grouped into bins of 10 for which the mean dry seed mass and proportion surviving were calculated. Correlation coefficients and probability values for linear or loglinear relationships are indicated for each panel at early (solid symbols and curves) and later (grey or open symbols and dashed curves) seedling stages.
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Although species grew at significantly different rates (Fig. 2), seed mass was a less significant predictor of RGR than it was for survival (Table 3). Among species, initial seedling RGR was not correlated with seed mass, but smaller-seeded species did grow faster from 1 to 5 years of age (Fig. 2). Microhabitat effects on growth were similar to those for survival. All species grew much faster in plots with greater light availability, but no other microhabitat factor influenced RGR, nor did we observe any species × microhabitat interactions for RGR (Table 3).
We used path analysis to quantify simultaneously the direct and indirect (via initial seedling size) contributions of seed mass to survival and RGR. Path diagrams are illustrated in Fig. 3 for all species grouped together, as well as within Eperua and Vouacapoua. In each diagram, the strength of the path is depicted by the width of each arrow and indicated by the standardized partial regression coefficient. The total contribution of seed mass to each measure of performance can be estimated as the sum of the direct effect and the product of the two paths describing the indirect effect. For example, across all species larger seeds survived better initially because of a slight indirect effect but survived better later because of a direct effect (and despite a negative indirect effect). Seed mass explained almost half of the variation in initial seedling height across all species, and indirect effects of seed mass on performance mediated by initial seedling height were common both within and among species. However, the magnitude and direction of direct vs. indirect effects varied among vs. within species as well as between the two census datasets. Vouacapoua exhibited no direct or indirect influence of seed mass on survival at either census date. By contrast, larger seeds of Eperua were less likely to survive initially because they made taller seedlings that appear to have been more vulnerable to stem browsing or branchfall. Both between and within species, seedlings that were larger initially grew more slowly, and this effect persisted through the 5-year census date. Seed mass thus showed a consistent negative indirect effect on RGR that nevertheless did not offset the early (all species, Eperua) and later (Vouacapoua) positive direct effects of seed mass on RGR.
Figure 3. Path analyses illustrating the direct and indirect effects of seed size, and the effects of plot-level light availability, on seedling performance. In each diagram, the strength of the path is depicted by the width of each arrow and indicated by the standardized partial regression coefficient. The total contribution of seed mass to each measure of performance can be estimated as the sum of the direct effect and the product of the two paths describing the indirect effect. The top panels present analyses for all species combined, whereas the others represent analyses for the single species Vouacapoua or Eperua. Left- and right-hand panels represent datasets from the 1-year and 5-year census dates. Although it is not noted in the figure, a significant amount of variance in both RGR and survival was not explained by the three variables (light, seed mass or initial seedling height) in all cases.
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