Dormancy-defense syndromes and tradeoffs between physical and chemical defenses in seeds of pioneer species

Authors: ZALAMEA, P - SMITHSONIAN TROPICAL RESEARCH; DALLING, J - UNIVERSITY OF ILLINOIS; SARMIENTO, C - SMITHSONIAN TROPICAL RESEARCH; ARNOLD, A - UNIVERSITY OF ARIZONA; DELEVICH, C - SMITHSONIAN TROPICAL RESEARCH; BERHOW, MARK; NDOBEGANG, A - UNIVERSITY OF ARIZONA; GRIPENBERG, S - UNIVERSITY OF ARIZONA; DAVIS, ADAM

Submitted to: Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/14/2018
Publication Date: 8/4/2018
Citation: Zalamea, P.C., Dalling, J.W., Sarmiento, C., Arnold, A.E., Delevich, C., Berhow, M.A., Ndobegang, A., Gripenberg, S., Davis, A.S. 2018. Dormancy-defense syndromes and tradeoffs between physical and chemical defenses in seeds of pioneer species. Ecology. 99(9):1988-1998. https://doi.org/10.1002/ecy.2419.
DOI: https://doi.org/10.1002/ecy.2419

Interpretive Summary: Pioneer plants are found in a wide range of highly disturbed environments, from agricultural fields to clearings in tropical forests. Seedlings of pioneer species rapidly colonize newly-disturbed areas, but to do so, they rely on seeds buried within the soil seedbank. Understanding what causes pioneer seeds to survive in the soil has many practical applications, from managing weeds in agricultural systems to conserving tropical plants. Using 16 pioneer plant species, we investigated relationships among four physical (i.e., seed fracture resistance, seed coat thickness, seed permeability, and seed mass) and two chemical (i.e., number of phenolic compounds and phenolic peak area) defense traits, and their association with seed persistence. We found that seed permeability – a trait that distinguishes physical dormancy from other dormancy types – was positively associated with chemical defense traits and negatively associated with physical defense traits. These results provide a frame of reference for future investigations into reducing the persistence of weed seeds, indicating that management tactics should be developed within dormancy and seed defense classes.

Technical Abstract: Seeds of pioneer plant species have chemical and physical characteristics that determine their propensity to persist in the soil seed bank. These defense traits allow seeds to survive in the soil despite diverse predators and pathogens, and to germinate and recruit even decades after dispersal. Defenses in seedlings and adult plants often are described in terms of trade-offs between chemical and physical defense, but the interplay of such defensive strategies has not been evaluated for seeds, which are the most important component of reproduction for trees. Here we evaluated whether different classes of seed defenses were negatively correlated across species (consistent with trade-offs in defense strategies), or whether groups of traits formed associations across species (consistent with seed defense syndromes). Using 16 of the most common pioneer tree species in a neotropical lowland forest we investigated relationships among four physical (i.e., seed fracture resistance, seed coat thickness, seed permeability, and seed mass) and two chemical (i.e., number of phenolic compounds and phenolic peak area) defense traits, and their association with seed persistence. We complemented trait analyses with seed bioassays to evaluate activity of seed extracts against fungal pathogens and a model invertebrate. We did not find a univariate trade-off between chemical and physical defenses. Instead, we found that seed permeability – a trait that distinguishes physical dormancy from other dormancy types – was positively associated with chemical defense traits and negatively associated with physical defense traits. Using a linear discriminant analysis and a hierarchical cluster analysis we found empirical evidence to distinguish among three distinctive seed defense syndromes that correspond directly with seed dormancy classes (i.e., quiescent, physical, and physiological). Our data suggest that short and long-term persistence of seeds can be achieved via two distinct strategies: having permeable seeds that are well defended chemically, or impermeable seeds that are well defended physically. Overall, our results do not support the existence of clear trade-offs between physical and chemical defenses in seeds per se. Instead, we find that seed defense and seed dormancy are linked, suggesting that environmental and evolutionary pressures on seed persistence and for delayed germination can select for trait combinations defining distinct dormancy-defense syndromes.