Chapter 2 The Evolutionary Ecology of Seed Size Michelle R. Leishman, Ian J. Wright, Angela T. Moles and Mark Westoby Department of Biological Sciences, Macquarie University, Sydney, New South Wales, Australia Introduction of seed mass. Unlike many other areas of comparative plant ecology, we have sub- Seed mass is a trait that occupies a pivotal stantial published information from several position in the ecology of a species. It links different scales and research styles. As well the ecology of reproduction and seedling as field experiments and demographic establishment with the ecology of vegeta- studies with a few species at a time, we tive growth, strategy sectors that are other- have simple experiments with larger num- wise largely disconnected (Grime et al., bers of species (ten to 50), quantification of 1988; Shipley et al., 1989; Leishman and seed mass and its correlates in whole-vege- Westoby, 1992). tation types (hundreds of species) and tests There is a startling diversity of shapes of consistency across different continents. and sizes of seeds among the plant species The wide-scale quantification began as of the world. Seeds range from the dust early as Salisbury (1942) and Baker (1972), seeds of the Orchidaceae and some sapro- but has been much added to and consoli- phytic and parasitic species (around 10Ϫ6 dated over the past 10 years (e.g. Mazer, g), across ten orders of magnitude to the 1989, 1990; Leishman and Westoby, 1994a; double coconut Lodoicea seychellarum Leishman et al., 1995; Eriksson and (104 g) (Harper et al., 1970). Within species, Jakobsson, 1998). The work spanning large seed size typically spans less than half an numbers of species is complementary to order of magnitude (about fourfold: detailed experiments involving only a few Michaels et al., 1988). Most within-species species, giving a stronger sense of how variation occurs within plant rather than widely the results from particular experi- among plants or populations (Michaels et ments can be generalized. al., 1988; Obeso, 1993; Vaughton and Much of the literature examines how Ramsey, 1998), indicating environmental natural selection on seed size might be effects during development rather than influenced by various environmental fac- genetic differences between mothers. This tors. In this context, it is at first glance sur- chapter is concerned with the differences prising that seed size varies within in seed size among species, and the conse- communities across a remarkable five to six quences for vegetation dynamics and com- orders of magnitude (Leishman et al., 1995; munity composition. Fig. 2.1). Further, there is strong overlap of During the last 10–15 years, there has seed-size distributions between quite dif- been considerable progress in the ecology ferent habitats. Within the temperate zone, © CAB International 2000. Seeds: The Ecology of Regeneration in Plant Communities, 2nd edition 31 (ed. M. Fenner) 32 M.R. Leishman et al. Fig. 2.1. Frequency histograms of seed dry mass from eight floras. The floras originate from four continents and include representatives from tropical and temperate biomes and a diversity of environmental condi- tions, vegetation types and phylogenetic histories. Data from western New South Wales, central Australia, Sydney (Leishman et al., 1995); Northern Territory, Nigeria (Lord et al., 1997); Californian chaparral (Keeley, 1991); Indiana dunes (Mazer, 1989); and Sheffield (Grime et al., 1988). Seed masses are grouped into half- log classes. differences between communities account Components and measurement of for only about 4% of the variation in seed seed size size between species (Leishman et al., 1995). Differences between the tropics and Seeds consist of an embryo plus the temperate zone are somewhat larger endosperm (sometimes termed the seed (Lord et al., 1995), but variation within a reserve), plus a protective seed-coat or habitat remains a very large component testa. Many seeds have distinctive disper- of overall between-species variation. sal appendages attached to the seed, such Alternative mechanisms that might shape as plumes and hairs for wind dispersal, this wide within-habitat variation have not hooks and barbs for adhesion dispersal, yet been fully formulated theoretically, elaiosomes for ant dispersal and arils or much less exposed to strong experimental flesh for vertebrate dispersal. These disper- hypothesis tests. sal appendages plus the seed are termed Evolutionary Ecology of Seed Size 33 the diaspore. The mass of dispersal struc- coat. For example, for the Sydney data set ture and the proportion of seed mass that is (Westoby et al., 1990) r 2 = 0.92, P < 0.0005, seed-coat can vary considerably between while the percentage of dry seed mass due species. to the seed-coat varied between 1.2 and There is no single measure of seed size 96%, with a mean value of 43%. In a that is ideal for all purposes. For dis- smaller data set of woody perennials from cussing seedling establishment, seed a range of habitats in New South Wales reserve mass best reflects the resources (Wright and Westoby, 1999), seed mass and available to the seedling. For discussing reserve mass were again tightly correlated the size of the object that has to be moved (r 2 = 0.99, P < 0.0005), while % coat varied by a given dispersal mechanism, seed mass from 7 to 57%, with a mean of 30%. In nei- including the seed-coat is most relevant. ther data set was there a relationship For discussing costs to the mother per seed between % coat and seed mass. produced, mass of the whole diaspore is To the extent that mineral nutrients as better than seed mass, though still not a well as energy are decisive during seedling complete measure of all costs of reproduc- establishment, the mineral nutrient content tion. Westoby (1998) recommended dry of the seed would be just as informative as seed mass, including seed-coat but exclud- seed mass. The nutrient content is the ing dispersal structures, as an ecological product of the nutrient concentration and strategy axis, partly as a compromise seed mass, but, since there is much greater among alternative measures, partly because cross-species variation in seed mass than it is easiest to measure and partly to main- in nutrient concentration (e.g. 6.7 versus tain comparability with the majority of 1.7 orders of magnitude in the c. 1500 existing data. At the same time, increasing species of Barclay and Earle, 1974), in large numbers of studies go to the trouble to dis- data sets seed mass and nutrient content sect diaspores into components where it tend to be correlated (even if mass and seems relevant (e.g. Westoby et al., 1990; concentration themselves are not). Some Jurado and Westoby, 1992; Leishman and authors have reported a negative associa- Westoby, 1994b, c). Fortunately, in data tion between seed mass and nutrient con- sets spanning a wide range of seed mass, centration (e.g. Fenner (1983) for 24 the alternative measures will be strongly species of Asteraceae; Grubb and Burslem correlated. Suppose, for example, that two (1998) within species for the majority of 12 species have dispersal structure mass 0 and South-East Asian trees; Grubb et al. (1998) 300% of seed mass: this can only reverse for 194 species from lowland tropical diaspore-mass ranking, relative to seed- rainforest) while others have found no cor- mass ranking, for species whose seeds dif- relation (e.g. Kitajima (1996a) for 12 tropi- fer in mass by less than a factor of three. cal woody species of Bignoniaceae, Thus, in data sets spanning orders of mag- Bombacaceae, Leguminosae; Grubb and nitude of seed mass, there is a strong posi- Burslem (1998) across the 12 South-East tive relationship between log dry diaspore Asian tree species; Milberg et al. (1998) for mass and log dry seed mass: e.g. in western 21 Eucalyptus, Banksia and Hakea New South Wales, n = 243, r 2 = 0.71; species). Thus, no consistent relationship central Australia, n = 199, r 2 = 0.83; has emerged between seed mass and nutri- Sydney, n = 286, r 2 = 0.97. On the other ent concentration, although evidence is hand, among sets of species spanning only beginning to emerge that variation in these (say) three- to fourfold in seed mass, attributes should be considered simultane- diaspore-mass ranking could be substan- ously with measures of allocation to seed tially different from seed-mass ranking. defence structures, such as seed-coats Similarly, log seed mass and log seed (Grubb et al., 1998). reserve mass tend to be closely correlated, The seed size of a species represents even though substantial variation exists in the amount of maternal investment in an the proportion of mass due to the seed- individual offspring, or how much ‘packed 34 M.R. Leishman et al. lunch’ an embryo is provided with to start the model is that, if a mother plant is in a its journey in life. Seed size represents a position to allocate more resources to seed fundamental trade-off, within the strategy output, it should produce more seeds of of a species, between producing more the same size. The physiological machin- small seeds versus fewer larger seeds from ery of seed provisioning should have been a given quantity of resource allocated to selected to approximate this outcome, reproduction. The trade-off and its conse- rather than increasing the size of a fixed quences were formalized in the model by number of seeds. In order to generate this Smith and Fretwell (1974). There is always prediction, the exact shape of the selection pressure to produce more seeds, Smith–Fretwell function is not important. since more seeds represent more offspring All that is required is for there to be some (although there may be a lower limit to the minimum size for a seed to have any seed size that permits a functional seedling chance of establishing and for there to be to be produced (Raven, 1999)).