Secondary metabolites in a neotropical shrub: spatiotemporal allocation and role in fruit defense and dispersal

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Authors

Maynard, Lauren
Slinn, Heather
Glassmire, Andrea
Matarrita-Carranza, Bernal
Dodson, Craig
Nguyen, Trang
Burroughs, Megan
Dyer, Lee
Jeffrey, Christopher
Whitehead, Susan

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Wiley

Abstract

Deciphering the ecological roles of plant secondary metabolites requires integrative studies that assess both the occurrence patterns of compounds and their bioactivity in ecological interactions. Secondary metabolites have been primarily studied in leaves, but many are unique to fruits and can have numerous potential roles in interactions with both mutualists (seed dispersers) and antagonists (pathogens and predators). We described 10 secondary metabolites of the class alkenylphenols from the plant species Piper sancti-felicis, quantified their patterns of intraplant allocation across tissues and fruit development, and examined their ecological role in fruit interactions. We found that fruit pulp had the highest concentrations and diversity of alkenylphenols, followed by flowers; leaves and seeds had only a few compounds at detectable concentrations. We observed a nonlinear pattern of alkenylphenol allocation across fruit development—increasing as the flowers developed into unripe pulp then decreasing as the pulp ripened. This pattern is consistent with the hypothesis that alkenylphenols function to defend fruits from pre-dispersal antagonists and are allocated based on the contribution of the tissue to the plant’s fitness. To assess the impacts of alkenylphenols in interactions with antagonists and mutualists, we performed fungal bioassays, field observations, and feeding experiments with vertebrate dispersers. In fungal bioassays, we found that increasing concentrations of alkenylphenols had a negative effect on the growth of most fungal taxa. In field observations, nocturnal dispersers (bats) removed the majority of infructescences, and diurnal dispersers (birds) removed a larger proportion of unripe infructescences. In feeding experiments, bats had an aversion to alkenylphenols, but birds did not. This aversion observed in bats, combined with our results showing a decrease in alkenylphenols during ripening, suggests that alkenylphenols in fruits represent a trade-off (defending against pathogens but reducing disperser preference). Together, this research provides a broad overview of the ecological significance of a little studied class of secondary metabolites in seed dispersal and fruit defense. It can also serve as a roadmap for integrating the study of intraplant spatiotemporal allocation patterns with ecological experiments to further our understanding of the evolutionary ecology of plant chemical traits.

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Keywords

Antagonism, Alkenylphenols, Defense trade-off hypothesis, La Selva Biological Station, Mutualism, Optimal defense theory, Piper sancti-felicis, Specialized metabolites

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