Size and Life History Theory. Size of Dispersal Units

Size of Dispersal Units.Salisbury (1942) developed an influential proposition about seed size in flowering plants and nutritional resources that was extended by Garrett (1973) to plant pathogenic fungi. The idea in Garrett’s words (p. 3) is that “the average size of a reproductive propagule is determined by the nutritional needs for establishment of a new young individual of the species in its typical habitat”. Salisbury’s thesis was that seed size is determined by the length of time during which a seedling must be self-supporting before it can supply its own needs by photosynthesis. Salisbury’s generalization was based on data on seed and fruit production by 240 species of British flowering plants.

He found that the spectrum in seed size could be correlated with habitat type: Species with the smallest seeds were characteristic of open habitats (early successional); at the other extreme were the heaviest seeds from shade- adapted woodland flora (later successional). By evolutionary adjustment of seed size to habitat type, it was argued, any plant species could efficiently allocate resources, providing the appropriate level of reserve in each instance. This story is analogous to Lack’s (1947) and Cody’s (1966) famous work on allocation of resources and clutch size in birds.

Though Salisbury’s logic is appealing (perhaps deceptively so), subsequent studies on the evolution of seed size have shown the issue to be considerably more complicated and related to many attributes, among them plant size and longevity, and not only survival through the juvenile phase but through reproduction (e.g., Chap. 21 in Harper 1977; Moles and Westoby 2006; Rees and Venable 2007). An important caveat must also be added in how this logic is worded and interpreted. Ultimately at issue here is what compromise strategy maximizes fitness. Reproductive capacity does not evolve to match the hazards of the environment because as Harper says (1977, p. 648) ..."it is impossible for an organism to evolve to a state in which it leaves enough offspring to replace itself from a condition in which it did not leave enough". Rather, the interpretation (and obviously that of Garrett, below) needs to be made from the standpoint of natural selection favoring those individuals that contribute more descendants than their competitors to subsequent generations (see comments Chap. 1).

Garrett (1973) proposed that the fungi Botrytis and Fusarium illustrated the principle that the level of endogenous reserves in fungal spores appears to be adjusted to take advantage of supplementary exogenous nutrients supplied in plant exudates. B. fabae produces spores about nine times the size of (and with proportionately more nutrient reserves than) those of B. cinerea. The former pathogen is able to overcome the resistance of healthy, vigorous leaves. In contrast, B. cinerea does not preferentially infect healthy leaves, except under extreme conditions of inoculum pressure or in the presence of additional nutrients (e.g., as may be leached from pollen deposited on leaf surfaces).

This species is well known to be an opportunistic parasite of senescing, wounded, or weakened plants. Its typical infection courts are debilitated leaves, floral organs, overripe fruit—all of which are predisposed to infection by virtue of nutrient leakage or reduced resistance or both (Ngugi and Scherm 2006). So Haldane’s (1956) maxim “on being the right size” for Botrytis may mean one of two strategies: The organism could produce numerous small propagules of limited infectiv- ity that rely on nutrients from a conducive host structure or condition to compensate for their small nutrient reserve (analogous to Salisbury’s theme of smaller but more abundant seeds characteristic of plants from open habitats).

Alternatively, fewer but large, well-supplied spores could be produced, capable of overcoming highly resistant host organs. The benefit would be a propagule of higher infectivity, less subject to certain external conditions; the cost is reduced output. Both strategies are evidently successful, but it is interesting that B. cinerea is the more abundant and widespread of the two species (Garrett 1973), suggesting that it may be ecologically more successful. Among Botrytis species, B. cinerea is considered to be a polyphagous generalist attacking over 200 eudicot species, whereas B. fabae is a specialist restricted to certain hosts in the Fabaceae (pea family) (Elad et al. 2004; Staats et al. 2005), although human influences on host manipulation complicate the interpretation somewhat.

Salisbury (1942) extended his seed size hypothesis to encompass vegetative propagules such as rhizomes and stolons, insofar as these were another means of nutritional support from the parent plant. Analogously, Garrett (1973) recognized the striking visual and functional parallel presented by certain structures of root-infecting fungi such as species of Fomes, Armillaria, and Phymatotrichum. Mycelial strands and rhizomorphs differ in detail but all are basically subterranean, macroscopic (often several mm in diameter), multistranded cables of hyphae that may extend for dozens of meters. In Armillaria, clones extending at least 450 m have been documented (Anderson et al. 1979) and the maximum size of a single clonal population can be immense (Smith et al. 1992).

All such strands or rhizomorphs function in translocating nutrients from a food base to the growing apex, ultimately to the point of infection. Why does an essentially microscopic organism consisting of fine mycelial threads allocate biomass to produce such a massive, elaborate structure? In part, these are effective organs for resource exploration (Boddy et al. 2009). Furthermore, unlike the roots of herbaceous plants that are relatively vulnerable to infection by single spores, those of undamaged, woody hosts resist invasion by physical and chemical defenses. By aggregating multiple hyphae as a rhizomorph, the pathogen can breach the defenses of a mature tree that would be impenetrable by a single hypha. Rhizomorphs also offer the fungus some insularity from adverse environments or nutrient leakage while the organism is in an exploratory mode.

Harper (1977, pp. 672-673) makes some most interesting points relating to plants with very small seeds that complement Salisbury’s story. This pertains to certain symbiotic plants, such as the saprophytic Monotropa and the parasitic Orobanche. Unlike some of the larger seeded symbionts (dodder and mistletoes, which must either grow to locate a host or penetrate its bark, respectively), these small-seeded plants germinate only when triggered to do so by a host chemical. They are thus assured of an external food source immediately upon germination. In evolutionary terms, this removed the need for an internal food reserve and natural selection acted to increase seed number rather than size.

The species have acted opportunistically, seizing on “an alternative mode of embryo nutrition to reduce seed size to tiny dried bags of DNA and expand their reproductive capacity to a new limit” (p. 673). This is in contrast to the conventional interpretation that they “need” to produce more seeds to “find” a host—an explanation which, as Harper points out, is wrong, for reasons noted above. In this context it is also important to recall that number of progeny (i.e., seeds in the present context) is not the same thing as number of descendants, and that the currency of natural selection is the latter (Chap. 1).