Chemical ecology of fruit defence: synergistic and antagonistic interactions among amides from Piper

Abstract

Summary1. Although ripe, fleshy fruits function primarily to attract seed dispersers, they must also be defended against diverse communities of seed predators and pathogens. For some plants, the concentration and diversity of secondary metabolites in fruits can exceed that of leaves and other plant parts, but little is known about the functional significance of the suites of compounds found in fruits. Fruit secondary metabolites may function in defence, or they may play a variety of other roles in seed development and dispersal. 2. In this study, we conducted a series of experiments to test the effects of amides, a highly diverse class of secondary metabolites found in Piper fruits, on a variety of antagonistic fruit pests, including an insect seed predator (Sibaria englemani, Pentatomidae) and three unidentified species of fungi isolated from ripe Piper reticulatum (Piperaceae) fruits. We tested the effects of amide-rich extracts from unripe and ripe fruits of P. reticulatum and the effects of two pure compounds, piperine and piplartine, presented alone and in combination. 3. Amide-rich extracts from unripe and ripe fruits had no effect on insect feeding preferences, but strong negative effects on fungal growth rates. A comparison of the relative bioactivity of unripe and ripe fruit extracts, controlling for concentration, showed that the specific composition of compounds in unripe fruits provides a more effective defence than that of ripe fruits against two of the three fungal species tested. 4. Pure amides had variable effects on insect feeding preferences and strong negative effects on fungal growth rates. Tests of the bioactivity of two pure amides, presented alone and in combination, showed that the same two compounds can interact either synergistically or antagonistically in mixtures depending on the particular consumer involved. 5. Together, these results suggest that the secondary metabolites in fruits may be a key characteristic contributing to fruit defence and plant reproductive success. Specifically, our results emphasize: (i) the potential for slight changes in the composition of mixtures to alter the efficacy of defence; and (ii) the potential for complex interactions among compounds in mixtures that can alter the bioactivity of secondary metabolites differentially among different consumers.

Defensive fruit metabolites obstruct seed dispersal by altering bat behavior and physiology at multiple temporal scales

“…In this scenario, fruit pulp secondary compounds deter seed predators, detrimental bacteria or fungi (Cipollini and Levey 1997). There is increasing support for the defensive trade-off hypothesis (Cipollini and Levey 1997, Izhaki 2002, Cazetta et al 2008, Whitehead and Bowers 2014, Whitehead et al 2016), but tests of this hypothesis have focused on the costs of fruit secondary metabolites in terms of reductions in the number of seeds that are removed and transported from the parent plant (i.e., the "quantity" of seed dispersal effectiveness, sensu Schupp et al 2010). There is increasing support for the defensive trade-off hypothesis (Cipollini and Levey 1997, Izhaki 2002, Cazetta et al 2008, Whitehead and Bowers 2014, Whitehead et al 2016), but tests of this hypothesis have focused on the costs of fruit secondary metabolites in terms of reductions in the number of seeds that are removed and transported from the parent plant (i.e., the "quantity" of seed dispersal effectiveness, sensu Schupp et al 2010).…”

Defence syndromes in lodgepole – whitebark pine ecosystems relate to degree of historical exposure to mountain pine beetles

“…These mechanisms include both constitutive defences and induced traits elicited by the attacking agents (Karban et al 1999;Underwood & Rausher 2002;Bonello et al 2006;Heil & Bueno 2007;Pieterse et al 2013). While some plants appear to rely on one or two defence compounds to resist attack, most species deploy mixtures of allelochemicals, which challenge the abilities of herbivores and their symbionts to tolerate or adapt to them (Whitehead & Bowers 2014, Raguso et al 2015. Suites of traits that collectively minimize herbivory are termed 'plant defence syndromes' (Agrawal & Fishbein 2006).…”

Chemical tradeoffs in seed dispersal: defensive metabolites in fruits deter consumption by mutualist bats

“…The occurrence of toxic secondary metabolites in a tissue meant to attract mutualists is puzzling, but a number of different adaptive hypotheses have been proposed to explain how these compounds may increase plant fitness (Cipollini and Levey ). Perhaps the most well‐supported of these is the defense tradeoff hypothesis, which suggests that fruit secondary metabolites function primarily to defend against non‐dispersing insect and microbial fruit pests (Herrera , Cipollini and Levey , Izhaki , Tewksbury et al , Whitehead and Bowers , ). However, because the same secondary metabolites that defend against pests could also affect interactions with mutualists, understanding the overall ecological and evolutionary consequences of fruit chemical defense requires a broad view of the possible effects of defense traits on the foraging and feeding behavior of seed‐dispersing animals.…”