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1. Data from: "Multiscale variability in nutrients and secondary metabolites in a bat-dispersed neotropical fruit"

   https://doi.org/10.5281/zenodo.8250520  

   Gelambi, Mariana ; Whitehead, Susan R. ( January 2023 , Zenodo)

   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.

    

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2. Fruit secondary metabolites alter the quantity and quality of a seed dispersal mutualism

   https://doi.org/10.1002/ecy.4032  

   Nelson, Annika S. ; Gelambi, Mariana ; Morales‐M., Estefania ; Whitehead, Susan R. ( March 2023 , Ecology)

   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 important 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 genusPiper(Piperaceae), on seed dispersal effectiveness (SDE) by ants, which are common secondary seed dispersers. We experimentally added amide extracts toPiperfruits 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 ants 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.

    

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3. Fruit secondary metabolites alter the quantity and quality of a seed dispersal mutualism

   https://doi.org/10.7280/D1R39K  

   Nelson, Annika S. ; Gelambi, Mariana ; Morales-M., Estefania ; Whitehead, Susan R. ( January 2023 , Dryad)

   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. 

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4. Ant seed removal in a non‐myrmecochorous Neotropical shrub: Implications for seed dispersal

   https://doi.org/10.1111/btp.12728  

   Clemente, Seanne R. ; Whitehead, Susan R. ( December 2019 , Biotropica)

   This study investigated ant seed removal ofPiper sancti‐felicis,an early successional Neotropical shrub. NeotropicalPiperare a classic example of bat‐dispersed plants, but we suggest that ants are underappreciated dispersal agents. We identified eleven ant species from the generaAphaenogaster,Ectatomma,Paratrechina,Pheidole,Trachymyrmex, andWasmanniarecruiting to and harvestingP. sancti‐felicisseeds in forest edge and secondary forest sites at La Selva, Costa Rica. We also tested for differences in ant recruitment to five states in which ants can commonly encounter seeds: unripe fruit, ripe fruit, overripe fruit, bat feces, and cleaned seeds. Overall, ants harvested more seeds from ripe and overripe fruits than other states, but this varied among species. To better understand the mechanisms behind ant preferences for ripe/overripe fruit, we also studied how alkenylphenols, secondary metabolites found in high concentrations inP. sancti‐felicisfruits, affected foraging behavior in one genus of potential ant dispersers,Ectatomma. We found no effects of alkenylphenols on recruitment ofEctatommato fruits, and thus, these compounds are unlikely to explain differences in ant recruitment among fruits of different maturity. Considering thatP. sancti‐felicisseeds have no apparent adaptations for ant dispersal, and few ants removed seeds that were cleaned of pulp, we hypothesize that most ants are harvesting its seeds for the nutritional rewards in the attached pulp. This study emphasizes the importance of ants as important additional dispersers ofP. sancti‐felicisand suggests that other non‐myrmecochorous, vertebrate‐dispersed plants may similarly benefit from the recruitment to fruit by ants.

    

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5. Exploring the links between secondary metabolites and leaf spectral reflectance in a diverse genus of Amazonian trees

   https://doi.org/10.1002/ecs2.3362  

   Fine, Paul V. A. ; Salazar, Diego ; Martin, Roberta E. ; Metz, Margaret R. ; Misiewicz, Tracy M. ; Asner, Gregory P. ( February 2021 , Ecosphere)

   Plant defense chemistry is often hypothesized to drive ecological and evolutionary success in diverse tropical forests, yet detailed characterizations of plant secondary metabolites in tropical plants are logistically challenging. Here, we explore a new integrative approach that combines visible‐to‐shortwave infrared (VSWIR) spectral reflectance data with detailed plant metabolomics data from 19Protium(Burseraceae) tree species. Building on the discovery that differentProtiumspecies have unique chemistries yet share many secondary metabolites, we devised a method to test for associations between metabolites and VSWIR spectral data. Given species‐level variation in metabolite abundance, we correlated the concentration of particular chemicals with the reflectance of the spectral bands in a wavelength band per secondary metabolite matrix. We included 45 metabolites that were shared by at least 5Protiumspecies and correlated their per‐species foliar abundances against each one of 210 wavelength bands of field‐measured VSWIR spectra. Finally, we tested whether classes of similar metabolites showed similar relationships with spectral patterns. We found that many secondary metabolites yielded strong correlations with VSWIR spectra ofProtium. Furthermore, importantProtiummetabolite classes such as procyanidins (condensed tannins) and phytosterols were grouped together in a hierarchical clustering analysis (Ward’s algorithm), confirming similarity in their associations with plant spectral patterns. We also found a significant correlation in the phenolics content between juvenile and canopy trees of the same species, suggesting that species‐level variation in defense chemistry is consistent across life stages and geographic distribution. We conclude that the integration of spectral and metabolic approaches could represent a powerful and economical method to characterize important aspects of tropical plant defense chemistry.

    

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