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

Abstract

Although fl eshy fruits function primarily to attract seed dispersers, many animal-dispersed fruits contain potentially toxic secondary metabolites. Th ese metabolites can provide defense against seed predators and pathogens, but their eff ects on dispersers are still poorly understood. In some cases plants may experience a tradeoff , where the metabolites that provide fruit defense also reduce seed disperser preferences. In other cases the bioactivity of fruit secondary metabolites may be directed primarily at pests with no negative eff ects on seed-dispersing vertebrates. We tested the eff ects of amides, a group of nitrogen-based defensive compounds common in the plant genus Piper (Piperaceae), in interactions with the primary seed dispersers of Piper in the neotropics -fruit-feeding bats in the genus Carollia (Phyllostomidae). In a series of fl ight cage experiments, pure amides and amide-rich fruit extracts reduced the preferences of bats for Piper fruit, aff ecting both the bats ' initial choices to remove Piper infructescences and the proportion of fruit consumed from individual infructescences once they were removed. However, the eff ects of amides varied considerably among three species of Carollia and among the specifi c individual amides and extracts tested. Overall, our results support the hypothesis that plants experience a tradeoff between seed dispersal and fruit defense, but the strength of this tradeoff and the overall fi tness consequences may depend strongly on ecological context.

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

“…For detailed experimental procedures, see Whitehead et al (2016). For detailed experimental procedures, see Whitehead et al (2016).…”

“…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).…”

“…1) from a Neotropical bat-plant dispersal system involving pepper plants in the genus Piper (Piperaceae) and fruit bats in the genus Carollia (Phyllostomidae). Second, fruit secondary compounds have been shown to reduce fruit removal rates in Carollia (Whitehead et al 2016) and we mined the raw data sources of that paper to extract fruit removal times of natural and amide-supplemented fruits. Second, fruit secondary compounds have been shown to reduce fruit removal rates in Carollia (Whitehead et al 2016) and we mined the raw data sources of that paper to extract fruit removal times of natural and amide-supplemented fruits.…”

“…1; Whitehead et al 2015;Baldwin et al 2019a;Baldwin et al 2019b), we tested the following hypotheses: (H1) fruit secondary compounds delay time of fruit removal, (H2) high GRT confers high-speed dispersal distances, and (H3) dispersal distances vary with time of fruit removal. 1; Whitehead et al 2015;Baldwin et al 2019a;Baldwin et al 2019b), we tested the following hypotheses: (H1) fruit secondary compounds delay time of fruit removal, (H2) high GRT confers high-speed dispersal distances, and (H3) dispersal distances vary with time of fruit removal.…”

Plant Antiherbivore Defense in Diverse Environments

“…The most bioactive compounds reported by Piper are amides, a group nitrogen-based compounds stored at leaves and fruits to defend that genera against herbivores [80]. In Piper, prenylated benzonic acid, chromene, and dimeric chromane at concentrations higher than 10% of dry weight of leaf material that compounds have synergistic or additive effect against herbivore attack also have been reported.…”