The ecological interaction between fleshy fruits and frugivores is influenced by diverse mixtures of secondary metabolites that naturally occur in the fruit pulp. Although some fruit secondary metabolites have a primary role in defending the pulp against antagonistic frugivores, these metabolites also potentially affect mutualistic interactions. The physiological impact of these secondary metabolites on mutualistic frugivores remains largely unexplored. Using a mutualistic fruit bat (
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Abstract Carollia perspicillata ), we showed that ingesting four secondary metabolites commonly found in plant tissues affects bat foraging behavior and induces changes in the fecal metabolome. Our behavioral trials showed that the metabolites tested typically deter bats. Our metabolomic surveys suggest that secondary metabolites alter, either by increasing or decreasing, the absorption of essential macronutrients. These behavioral and physiological effects vary based on the specific identity and concentration of the metabolite tested. Our results also suggest that a portion of the secondary metabolites consumed is excreted by the bat intact or slightly modified. By identifying key shifts in the fecal metabolome of a mutualistic frugivore caused by secondary metabolite consumption, this study improves our understanding of the effects of fruit chemistry on frugivore physiology. -
Abstract Frugivore foraging behavior is largely influenced by two key groups of chemical traits: nutrients and secondary metabolites. Many secondary metabolites function in plant defense, but their consumption can negatively impact both mutualistic and antagonistic frugivores, often due to toxic properties of the metabolites or through nutrient absorption interference. Frugivores are assumed to maximize nutrient acquisition while avoiding or minimizing toxic metabolite intake, but the relative roles of co‐occurring nutrients and secondary metabolites in foraging behavior are not well understood. Here, we used a neotropical fruit bat to investigate the interactive effects of nutrients and a broadly bioactive fruit secondary metabolite, piperine, on two essential processes in nutrient acquisition, namely foraging behavior and nutrient absorption. Through the manipulation of nutrient and piperine concentrations in artificial diets, we showed that captive fruit bats prioritize nutrient concentrations regardless of the levels of piperine, even though piperine is a strong deterrent on its own. Furthermore, our findings reveal that while piperine has no detectable influence on total sugar absorption, it reduces protein absorption, which is a crucial and limited nutrient in the frugivore diet. Overall, our results demonstrate the importance of considering the interaction between co‐occurring chemical traits in fruit pulp to better understand frugivore foraging and physiology.
Free, publicly-accessible full text available April 1, 2025 -
Abstract Ripe fleshy fruits contain not only nutrients but also a diverse array of secondary metabolites. Nutrients serve as a reward for mutualists, whereas defensive metabolites protect the fruit against pests and predators. The composition of these chemical traits is highly variable, both across different plants and even within repeating structures on the same individual plant. This intraspecific and intraindividual variation has important fitness consequences for both plants and animals, yet patterns of variation and covariation in nutrients and secondary metabolites are not well understood, especially at smaller scales. Here, we investigate the multiscale variation and covariation between nutrients and defensive metabolites in
Piper sancti‐felicis ripe fruits. Means and measures of variation of sugars, proteins, phenolics, and alkenylphenols vary greatly among plants, and at least 50% of the trait variation occurs at the intraindividual level. Also, we found that proteins, but not sugars, were correlated with phenolics and alkenylphenols at multiple scales, suggesting trait variation in protein content may be more constrained than sugars. Our findings emphasize the importance of examining patterns across scales and provide the groundwork to better understand how complex patterns of variation and covariation in nutrients and defensive metabolites shape ecological interactions surrounding fruits. -
Data from: Interactions between nutrients and fruit secondary metabolites shape bat foraging behavior and nutrient absorption; by Gelambi, M., Morales-M. E., & Whitehead, S. R. Published in Ecosphere, 2024. The study was conducted at La Selva Biological Station, Costa Rica during June-July 2021. We employed neotropical fruit bats (Carollia perspicilla) as a model to investigate how nutrients and a broadly bioactive fruit secondary metabolite, piperine (Sigma-Aldrich), interact and influence two critical aspects of nutrient acquisition: foraging behavior and nutrient absorption. By manipulating nutrient and piperine concentrations in artificial diets, we reveal that captive fruit bats prioritize nutrient concentrations, even in the presence of piperine's potent deterrent effects. Additionally, our findings indicate that while piperine exerts no detectable influence on total sugar absorption, it significantly reduces protein absorption.more » « less
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Data from: Untargeted Metabolomics Reveals Fruit Secondary Metabolites Alter Bat Nutrient Absorption; by Gelambi, M. & Whitehead, S. R. Published in the Journal of Chemical Ecology, 2024. Using a mutualistic fruit bat (Carollia perspicillata), our research explores how four secondary metabolites (piperine, tannin acid, eugenol, and phytol) commonly found in plant tissues affect the foraging behavior and induce changes in the fecal metabolome. In this study, bats were captured and housed in flight cages. Nightly trials exposed them to varying concentrations of secondary metabolites. Objective 1 involved non-choice trials to measure food consumption, while Objective 2 evaluated the impact of metabolite consumption on the bat fecal metabolome. Fecal samples were collected, stored, and later analyzed to understand how secondary metabolites influence bat behavior and metabolism. All the analyses were performed in R v. 4.2.1.more » « less
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Interactions between plants and herbivores are central in most ecosystems, but their strength is highly variable. The amount of variability within a system is thought to influence most aspects of plant-herbivore biology, from ecological stability to plant defense evolution. Our understanding of what influences variability, however, is limited by sparse data. We collected standardized surveys of herbivory for 503 plant species at 790 sites across 116° of latitude. With these data, we show that within-population variability in herbivory increases with latitude, decreases with plant size, and is phylogenetically structured. Differences in the magnitude of variability are thus central to how plant-herbivore biology varies across macroscale gradients. We argue that increased focus on interaction variability will advance understanding of patterns of life on Earth.
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Original data and R code accompanying our paper in Ecology & Evolution by Gelambi M. & Whitehead, S. R. (2023).
Ripe fleshy fruits contain not only nutrients but also a diverse array of many secondary metabolites. Nutrients serve as a reward for mutualists, whereas defensive metabolites protect the fruit against pests and predators. The composition of these chemical traits is highly variable, both across different plants and even within repeating structures on the same individual plant. This intraspecific and intraindividual variation has important fitness consequences for both plants and animals, yet patterns of variation and covariation in nutrients and secondary metabolites are not well understood, especially at smaller scales. Here, we investigate the multiscale variation and covariation between nutrients and defensive metabolites in Piper sancti-felicis ripe fruits. Means and variances of sugars, proteins, phenolics, and alkenylphenols vary greatly among plants, and at least 50% of the trait variation occurs at the intraindividual level. Also, we found that proteins, but not sugars, were correlated with phenolics and alkenylphenols at multiple scales, suggesting trait variation in protein content may be more constrained than sugars. Our findings emphasize the importance of examining patterns across scales and provide the groundwork to better understand how complex patterns of variation and covariation in nutrients and defensive metabolites shape ecological interactions surrounding fruits.