On the adaptive value of large seeds for tropical moist forest trees: a review and synthesis

In moist temperate and tropical environments species that typically become established in closed, shaded habitats tend to have larger seeds than those that regenerate in open, secondary habitats. Despite this common pattern and the frequency with which benefits of small seed size for early successional species (large number, enhanced dispersal potential) have been discussed, little attention has focused on the advantages of large seeds for species that regenerate in closed, late successional associations. It is generally considered that large seeds enhance seedling survivorship at low light intensities. However, light intensity is only one of several factors that differ between shaded and sunlit habitats. This review examines microclimatic and biotic differences between shaded subcanopy habitats in mature tropical forests and those in sunlit, light gap habitats in which the early stages of tropical forest succession occur. Each factor is examined as a possible selective agent responsible for maintaining seed size differences between two guilds of tropical rainforest trees; the pioneer species that have small seeds and typically become established in large, sunlit gaps in the forest canopy and the persistent, relatively shade-tolerant species that have larger seeds and produce seedlings that survive for variable periods of time in the shade beneath the forest canopy. Three microclimatic factors that differ in subcanopy and gap habitats are examined; temperature, moisture, and light intensity. It is unlikely that temperature has been an important selective agent in maintaining the differences in seed sizes observed between the pioneer and persistent tree guilds. However, greater desiccation stress in light gaps might prevent successful regeneration of larger seeds in this habitat and thus might impose the smaller mean seed sizes of pioneer species. Reduced light intensities in subcanopy habitats also could favor larger seeds in the persistent guild because large seed reserves might 1) enhance the abilities of seeds to persist until suitable light (or moisture) conditions arise by providing for metabolic requirements of seeds during quiescent periods, 2) provide secondary compounds for defense of persistent seedlings against pathogens and predators during periods of low energy availability, 3) provide energy for construction of large amounts of photosynthetic tissue needed to maintain a positive net energy balance when light conditions are just above the leaf light compensation point of the plant, 4) provide energy for growth into higher light intensity strata, and 5) provide nutrients for replacement of lost or damaged tissues in persistent seedlings. Differences between soils in light gaps and subcanopy habitats are considered briefly. It is concluded that too little is known for predictions to be made regarding the probable effects of soil differences on the sizes of seeds able to survive in each habitat. Finally, differences between the two habitats in four biotic factors (competition, predation, pathogens, and mycorrhizal availability) are considered. Of these, greater competition for nutrients in the subcanopy habitat, and competition among co-germinating seedlings for light could have been important in favoring large seeds in the guild of persistent species. Pathogens are known to be more effective in shaded habitats, but data on seedling resistance to pathogens do not provide support for a role of seed size in enhancing resistance. Although differences in predation intensity and in mycorrhizal abundance in the two habitats have not been evaluated in the field, potential roles of these two factors in maintaining the seed size differential between these two guilds of forest trees are discussed. Despite the existence of numerous potential benefits of large seed reserves, seed sizes often must reflect compromises between conflicting selective pressures. Environmental conditions (e.g., moisture availability) can impose upper limits on seed size. Enhanced dispersal potential and greater total propagule numbers from maternal energy reserves are benefits of small seed size that can counterbalance selection for large seed reserves. The interactions between selective forces in molding seed sizes are discussed in a final section.