Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community

P>1. Plant defence theory provides a robust framework for understanding interactions between plants and antagonists, and for interpreting broad patterns in the functional-trait composition of plant communities. However, this framework has been built almost entirely on traits expressed by seedlings and mature plants. 2. No equivalent seed defence theory exists that recognizes the distinct suite of natural enemies that seeds encounter, and the unique constraints to their response. Furthermore, most attention has been paid to insect and vertebrate seed predators active above ground, whereas microbes in soil also have large effects on seed survival, particularly for plants that recruit from soil seed banks. 3. We suggest that concurrent selection on seed dormancy and resistance to microbial antagonists should result in distinct seed defence syndromes. We predict that species with physical seed dormancy will rely on physical defences to exclude predators and pathogens, and rapid seed germination to escape pathogens at the emergence stage. In contrast, species with physiological seed dormancy will deploy a continuum of physical and chemical defences, depending on soil pathogen pressure and duration of seed persistence. Finally, seeds of some species persist in the soil in a non-dormant, imbibed state, and lack obvious chemical and physical defences. These seeds may be especially dependent upon protection from beneficial seed-inhabiting microbes. 4. Framing a general 'seed defence theory' may help to account for the distribution of seed dormancy types across ecosystems. We predict that physiological dormancy will be favoured in dry or well-drained environments where pathogen pressure is relatively low, germination cues are most unpredictable, and seedling recruitment success is most variable. In contrast, physical dormancy should be favoured in warm and moist environments where pathogen pressure is high, and where germination cues are a stronger predictor of recruitment success. Persistent, non-dormant seeds are restricted to relatively aseasonal environments where favourable conditions for recruitment can occur over most of the year. 5. Synthesis. Integrating seed defence and dormancy traits can provide new insights into selection on dormancy types, and will help elucidate major trends in seed ecology and evolution. Understanding how seeds are defended also may improve our ability to predict plant regeneration and help develop innovative management strategies for weedy and invasive species.