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1. 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)

   Abstract 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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2. 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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3. Tomato fruit quality is more strongly affected by scion type and planting season than by rootstock type

   https://doi.org/10.3389/fpls.2022.948556  

   Gong, Tian; Brecht, Jeffrey K.; Hutton, Samuel F.; Koch, Karen E.; Zhao, Xin (December 2022, Frontiers in Plant Science)

   Previous studies of tomato rootstock effects on fruit quality have yielded mixed results, and few attempts have been made to systematically examine the association between rootstock characteristics and tomato fruit quality. In this study, grape tomato (‘BHN 1022’) and beefsteak tomato (‘Skyway’) were grafted onto four rootstocks [‘Estamino’ (vigorous and “generative”), ‘DR0141TX’ (vigorous and “vegetative”), ‘RST-04-106-T’ (uncharacterized), and ‘SHIELD RZ F1 (61–802)’ (mid-vigor, uncharacterized)] and compared to non-grafted scion controls for two growing seasons (Spring and Fall in Florida) in organically managed high tunnels. In both seasons and for both scions, the two vigorous rootstocks, regardless of their designation as “vegetative” (‘DR0141TX’) or “generative” (‘Estamino’), exhibited negative impacts on dry matter content, soluble solids content (SSC), SSC/titratable acidity (TA), lycopene, and ascorbic acid contents. Similar effects on fruit dry matter content and SSC were also observed with the ‘RST-04-106-T’ rootstock, although little to no change was seen with grafting onto ‘SHIELD RZ F1 (61–802)’. Further studies are needed to elucidate the impact of rootstock vigor on tomato volatile profiles and consumer sensory acceptability in order to better determine whether any of the documented effects are of practical importance. On the other hand, the evident effects of scion cultivar and planting season on fruit quality were observed in most of the measurements. The scion by rootstock interaction affected fruit length, firmness, pH, and total phenolic content, while the planting season by rootstock interaction impacted fruit firmness, pH, total antioxidant capacity, and ascorbic acid and lycopene contents. The multivariate separation pattern of planting season, scion, and rootstock treatments as revealed by the canonical discriminant analysis further indicated that the influence of scion cultivar and planting season on tomato fruit quality could be much more pronounced than the rootstock effects. The fruit color ( C * and H °), length and width, SSC, pH, total antioxidant capacity, ascorbic acid, and lycopene contents were the main attributes distinguishing different scion-planting season groups. 

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4. Untargeted Metabolomics Reveals Fruit Secondary Metabolites Alter Bat Nutrient Absorption

   https://doi.org/10.1007/s10886-024-01503-z  

   Gelambi, Mariana; Whitehead, Susan_R (May 2024, Journal of Chemical Ecology)

   Abstract 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 (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. 

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5. Comparative Metabolomics of Fruits and Leaves in a Hyperdiverse Lineage Suggests Fruits Are a Key Incubator of Phytochemical Diversification

   https://doi.org/10.3389/fpls.2021.693739  

   Schneider, Gerald F.; Salazar, Diego; Hildreth, Sherry B.; Helm, Richard F.; Whitehead, Susan R. (August 2021, Frontiers in Plant Science)

   Interactions between plants and leaf herbivores have long been implicated as the major driver of plant secondary metabolite diversity. However, other plant-animal interactions, such as those between fruits and frugivores, may also be involved in phytochemical diversification. Using 12 species of Piper , we conducted untargeted metabolomics and molecular networking with extracts of fruits and leaves. We evaluated organ-specific secondary metabolite composition and compared multiple dimensions of phytochemical diversity across organs, including richness, structural complexity, and variability across samples at multiple scales within and across species. Plant organ identity, species identity, and the interaction between the two all significantly influenced secondary metabolite composition. Leaves and fruit shared a majority of compounds, but fruits contained more unique compounds and had higher total estimated chemical richness. While the relative levels of chemical richness and structural complexity across organs varied substantially across species, fruit diversity exceeded leaf diversity in more species than the reverse. Furthermore, the variance in chemical composition across samples was higher for fruits than leaves. By documenting a broad pattern of high phytochemical diversity in fruits relative to leaves, this study lays groundwork for incorporating fruit into a comprehensive and integrative understanding of the ecological and evolutionary factors shaping secondary metabolite composition at the whole-plant level. 

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