Big-seed, durable construction syndrome

"Across species, a negative correlation has commonly been found between the seed mass and the potential relative growth rate (RGR) of seedligns grown under favourable conditions (e.g., Grime and Hunt, 1975; Shipley and Peters, 1990, Jurado and Westoby, 1992; Maranon and Grubb, 1993; Rincon and Huante, 1993; Osunkoya et al., 1994). However, there is no known mechanism through which larger seed mass might directly cause lower potential RGR. Rather, low potential RGR and large seed mass appear to be part of a trait syndrome also involving sturdy tissue construction (low-SLA and specific root length) (Reich et al., 1998; Wright and Westoby, 1999...) and low rates of tissue turnover (Bonger and Popma, 1990; Seiwa and Kikuzawa, 1991). Conversely, smaller-seeded species generally have higher potential RGR under near-optimal conditions, which is due in part to the seedlings being constructed of thinner or lower-density tissue with higher turnover rates."

Westoby et al. (2000) [see full citation in previous post]

Uniform seed size predicted

The seed size/number trade-off concept formalized in the Smith-Fretwell model predicts that: "if a mother plan is in a position to allocate more resources to seed output, it should produce more seeds of the same size...[assuming] some minimum size for a seed to have any chance of establishing and...diminishing returns at some stage as seed mass increases further. The curvature of the Smith-Fretwell function ensures that, if resources are reallocated such that one seed has higher seed mass than the optimum while another has less, the gain in fitness in the augmented seed is smaller than the loss in fitness in the diminished seed."

The mother plant's "...physiological machinery of seed provisioning " should have been selected to produce the maximum number of uniform, optimally sized seed, rather than simply producing larger seeds.

However, seeds vary within a species and even within an individual plant. Explanation?

"The moderate observed variation in seed mass within a species can be attributed either to the machinery of seed provisioning having limited capacity to deliver a completely standardized seem mass or to variability in the Smith-Fretwell function that seedlings are exposed to."

Source: Leishman, M.R., Wright, I.J., Moles, A.T., Westoby, M. (2000) The evolutionary ecology of seed size. In Seeds: the ecology of regeneration in plant communities.Fenner, M., ed. CABI Publishing, Wallingford: p. 31-57.

Seed size/number tradeoff summarized

"Seed size represents a fundamental trade-off, within the strategy of a species, between producing more small seeds versus fewer larger seeds from a given quantity of resource allocated to reproduction. The trade-off and its consequences were formalized in the model by Smith and Fretwell (1974). There is always selection pressure to produce more seeds, since more seeds represent more offspring (although there may be a lower limit to the seed size that permits a functional seedling to be produced (Raven, 1999)). On the other hand, larger, better-provisioned offspring have a greater chance of successful establishment, described by the Smith-Fretwell function....The best outcome from the mother's point of view is to maximize the ratio of seedling establishment chance to provisions invested in each seed..."

Weak positive correlation in Aquilegia pyrenaica

"Correlation analysis showed that only a few pairs of variables were significantly correlated (Table 3). No trade-off seems to exist between the number of seeds per carpel and the mean seed weight in a fruit, as the two variables are, if anything, positively correlated (r = 0.22, P = 0.06)."

M.C. Castellanos, M. Medrano, and C.M. Herrera. (2008) Subindividual variation and genetic versus environmental effects on seed traits in a European Aquilegia.

No seed size-seed number tradeoff in Lupinus perennis

"Within plants, this study detected no relationship between maternal parents’ seed number and seed size (weighted linear regression, b 5 3.8 3 1026, t 5 1.04, P 5 0.304) or between seed number and the coefficient of variation in seed size (weighted linear regression, b 5 23.8 3 1025, t 5 1.06, P 5 0.295; Fig. 2). Therefore, this study did not detect a trade-off between seed size and seed number, or a change in seed size variation with increasing seed number."

STACEY L. HALPERN (2005) SOURCES AND CONSEQUENCES OF SEED SIZE VARIATIONIN LUPINUS PERENNIS (FABACEAE): ADAPTIVE ANDNON-ADAPTIVE HYPOTHESES. American Journal of Botany 92(2): 205–213.

The origin of the debate

Building on the ideas of Robert MacArther, E.O. Wilson (The Theory of Island Biogeography, 1967), Harper (1970) framed the seed yield tradeoff concept in 1970, drawing on Erik Pianka's r/K terminology:

Tradeoff 1: Reproductive effort vs. longevity; seeds vs. "persistent vegetative organs"

"There is evidence that plant species differ in the proportion of their net annual assimilated income which is devoted to reproductive effort (2, 3). Crude generalizations about the reproductive effort of different types of plant are summarized in Table 1.

"It appears that species occupying early phases in succession (colonizing species) have a high reproductive effort, usually in the form of a large number of seeds, and a correspondingly high intrinsic rate of natural in- crease. These would be r species in the sense of MacArthur & Wilson (4). Perennials, and particularly woody species with low values of reproductive effort, seem to fit into the category of K species, which have stable habitats in later phases of succession. A greater part of their available energy resource is devoted to persistent vegetative organs; this confers advantages in a long-term intensive struggle for existence in crowded, resource-limited stable environments.

Tradeoff 2: Average seed mass (size) vs. number of seeds per plant

"Just as the resources available to a plant during development are partitioned between seed production and other ends, so the allocation to seeds is itself partitioned between numbers and size. Thus, the number of seeds borne by a plant is determined by 1. the size of the annual assimilated income, 2. the proportion of this devoted to seeds, and 3. the size of the seed units in which it is invested. It is a central thesis of this essay that seed numbers and seed size represent alternative strategies in the disposition of reproductive resources.

Sources:
J. L. Harper, P. H. Lovell, K. G. Moore (1970) The Shapes and Sizes of Seeds Author(s): Source: Annual Review of Ecology and Systematics, Vol. 1 (1970), pp. 327-356
MacArthur, R. and Wilson, E.O. (1967). The Theory of Island Biogeography, Princeton University Press (2001 reprint), ISBN 0-691-08836-5M.
Pianka, E.R. (1970). On r and K selection. American Naturalist 104, 592-597.

Simplistic Tradeoffs

"The simplicityof the trade-off concept has made it very popular in consideration of the evolution of life histories (e.g. Smith and Fretwell, 1974) and examples have been found in some instances (e.g. among plants of Silene alba, D. Hanych, pers. comm.). However, it is apparent now that simplistic trade-offs between size and number are often not found (see also Primack, 1978; Hardin, 1984). This does not mean, necessarily, that trade-offs are not important, but it does mean that the scale or conditions in which they may occur need to be examined more thoroughly."

"We found little evidence of trade-offs between mean seed mass and seed numbers within fruits or within whole seed crops."

Michaels et al (1988) made these conclusions after examining average seed mass, total seed production (mass and numbers) and the variation in seed mass in individuals and populations of 39 species. Among-plant variation was significant within 37 of the 39 species. Interestingly, in 29 of these species, within-plant component exceeded the among-plant component of the variation in seeds' mass.

Explanation for lack of tradeoffs between seed size and resource availability?

1. Allometry ["The failure to detect evidence of trade-offs in most cases may be partially attributable to the effects of plant size, which may have such strong effects on seed number that trade-offs maybe evident only when confounding effects of maternal size variation are removed."]


2. A seed's size may respond more to transient signals than to maternal resource availability signals


• seasonal environmental signals--whether it was fertilized early or late in the season


• seeds formed on shaded plants or ramets vs. sunny ones [however, Michaels et al. found that shaded plants of one species produced more variably sized seeds, but found no general relationship between seed mass and the shadiness of the habitat]
  
• fluctuations in resources--was it fertilized during a dry or wet spell
  

Perennials and seed size

While the main Tradeoff Debate is concerned with the putative negative correlation between plant longevity and yearly seed yield, those familiar with grassland perennial species might be forgiven for suspecting that perennials generally also have smaller seeds than annuals. Certainly, domesticated grains--currently all annuals--have much larger seeds than wild herbaceous perennials. The annual ancestors of some of the annual grains also have relatively large seeds.

However, when hundreds of plant species are compared, perenniality is only a weak predictor of a species' seed size:

• "the difference between the means for annual and perennial herbaceous autotrophs is small enough that herbaceous plants will be treated as a single group for many purposes." [Baker, 1972]
• "In each of the four floras [databases of plants from three continents] , plant perenniality was not associated with significant seed size variation after the addition of plant height or growth form." [Leishman et al., 1988]

Height is a robust predictor of seed size (tall species, in general, produce larger seeds), as is plant form (trees and vines generally have larger seeds than forbs and graminoids), according to Leishman et al. (1988). Perenniality is only a weak predictor...and it is the perennial habit that is associated with larger seed size.

• "Seed size was significantly associated with plant perenniality in the five floras (Fig. 4), with seeds of annual species generally smaller than seeds of perennials." [Leishman et al., p. 525]
• Baker (1972) found significant differences (p<0.001)>

• Mean seed weight of 664 native annual herbs: 5.76

  Mean seed weight of 940 native perennial herbs: 6.35

  Mean seed weight of 441 native shrubs: 7.55

  Mean seed weight of 94 native trees: 9.60

Sources:

Leishman, M. R., Westoby, M., Jurado, E. (1995) Correlates of seed size variation: a comparison among five temperate floras. Journal of Ecology. 83: 517-530

H. G. Baker (1972) Seed Weight in Relation to Environmental Conditions in California. Ecology, Vol. 53, No. 6 (Nov., 1972), pp. 997-1010