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The Enemy Release Hypothesis (ERH) proposes that non-native plants escape their co-evolved herbivores and benefit from reduced herbivory in their introduced ranges. Numerous studies have tested this hypothesis, with conflicting results, but previous studies focus on average levels of herbivory and overlook the substantial within-population variability in herbivory, which may provide unique insights into the ERH. We tested differences in mean herbivory and added a novel approach to the ERH by comparing within-population variability in herbivory between native and non-native plant populations. We include several covariates that might mask an effect of enemy release, including latitude, regional plant richness, plant growth form and plant cover. We use leaf herbivory data collected by the Herbivory Variability Network for 788 plant populations (616 native range populations and 172 introduced range populations) of 503 different native and non-native species distributed worldwide. We found no overall differences in mean herbivory or herbivory variability between native and non-native plant populations. Taken together, our results indicate no evidence of enemy release for non-native plants, suggesting that enemy release is not a generalized mechanism favoring the success of non-native species. 

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. 

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. 

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. 

Plants and herbivores are remarkably variable in space and time, and variability has been considered a defining feature of their interactions. Empirical research, however, has traditionally focused on understanding differences in means and overlooked the theoretically significant ecological and evolutionary roles of variability itself. We review the literature with the goal of showing how variability-explicit research expands our perspective on plant–herbivore ecology and evolution. We first clarify terminology for describing variation and then review patterns, causes, and consequences of variation in herbivory across scales of space, time, and biological organization. We consider how incorporating variability improves existing hypotheses and leads to new ones. We conclude by suggesting future work that reports full distributions, integrates effects of variation across scales, describes nonlinearities, and considers how stochastic and deterministic variation combine to determine herbivory distributions. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 54 is November 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates. 

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. 

Plant secondary metabolites are key mechanistic drivers of species interactions. These metabolites have primarily been studied for their role in defense, but they can also have complex consequences for mutualisms, including seed dispersal. Although the primary function of fleshy fruits is to attract seed-dispersing animals, fruits often contain complex mixtures of toxic or deterrent secondary metabolites that can reduce the quantity or quality of seed dispersal mutualisms. Furthermore, because seeds are often dispersed across multiple stages by several dispersers, the net consequences of fruit secondary metabolites for the effectiveness of seed dispersal and ultimately plant fitness are poorly understood. Here, we tested the effects of amides, nitrogen-based defensive compounds common in fruits of the neotropical plant genus Piper (Piperaceae), on seed dispersal effectiveness (SDE) by ants, which are common secondary seed dispersers. We experimentally added amide extracts to Piper fruits both in the field and lab, finding that amides reduced the quantity of secondary seed dispersal by reducing ant recruitment (87%) and fruit removal rates (58% and 66% in the field and lab, respectively). Moreover, amides not only reduced dispersal quantity but also altered seed dispersal quality by shifting the community composition of recruiting ants (notably by reducing the recruitment of the most effective disperser by 90% but having no detectable effect on the recruitment of a cheater species that removes fruit pulp without dispersing seeds). Although amides did not affect the distance ants initially carried seeds, they altered the quality of seed dispersal by reducing the likelihood of ants cleaning seeds (67%) and increasing their likelihood of redispersing seeds outside of the nest (200%). Overall, these results demonstrate that secondary metabolites can alter the effectiveness of plant mutualisms, by both reducing mutualism quantity and altering mutualism quality through multiple mechanisms. These findings present a critical step in understanding the factors mediating the outcomes of seed dispersal and, more broadly, demonstrate the importance of considering how defensive secondary metabolites influence the outcomes of mutualisms surrounding plants. 

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 inPiper sancti‐felicisripe 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.