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
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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- 10472026
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- Zenodo
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- National Science Foundation
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Abstract 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. -
Orangutan habitats are characterized by fluctuations in the availability of ripe fruits. During non-fruiting periods orangutans typically incorporate more lower-quality foods such as pith and bark in their diet. Condensed tannins (CT) are secondary plant compounds that bind to proteins, thus impeding the digestibility of proteins, and tending to make foods bitter or unpalatable. We analyzed condensed tannin content in 129 plant samples collected from Gunung Palung National Park in Borneo, Indonesia between 1994 and 2001. We predicted that CT concentrations would be highest in bark, and that there would be a correlation between protein and condensed tannin content. We used ANOVA with Bonferonni’s method for post-hoc comparisons to test for differences in tannin content between plant parts, and Pearson’s correlation to test for relationships between tannin concentrations and other nutrients. There were significant differences in condensed tannin content (F(4)=2.70, p=0.03) but no differences after adjusting the alpha-level for post-hoc comparisons. Whole fruit (including the skin) tended to have the highest CT concentration. However, we found no correlation between CT and concentration of nutrients including crude protein (R=0.12, p=0.19, N=127), free simple sugars (R=-0.09, p=0.40, N=100), or fiber (R=-0.38, p=0.67, N=128). This underscores that plants rich in desirable nutrients may also be rich in antifeedants, posing challenges for orangutan consumption and digestion even as they provide a source of high-quality energy. Additionally, for some food categories where high tannin content is predicted, such as bark, orangutans may be choosing to eat species that are lower in these compounds.more » « less
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Orangutan habitats are characterized by fluctuations in the availability of ripe fruits. During non-fruiting periods orangutans typically incorporate more lower-quality foods such as pith and bark in their diet. Condensed tannins (CT) are secondary plant compounds that bind to proteins, thus impeding the digestibility of proteins, and tending to make foods bitter or unpalatable. We analyzed condensed tannin content in 129 plant samples collected from Gunung Palung National Park in Borneo, Indonesia between 1994 and 2001. We predicted that CT concentrations would be highest in bark, and that there would be a correlation between protein and condensed tannin content. We used ANOVA with Bonferonni’s method for post-hoc comparisons to test for differences in 11tannin content between plant parts, and Pearson’s correlation to test for relationships between tannin concentrations and other nutrients. There were significant differences in condensed tannin content (F(¬4)=2.70, p=0.03) but no differences after adjusting the alpha-level for post-hoc comparisons. Whole fruit (including the skin) tended to have the highest CT concentration. However, we found no correlation between CT and concentration of nutrients including crude protein (R=0.12, p=0.19, N=127), free simple sugars (R=-0.09, p=0.40, N=100), or fiber (R=-0.38, p=0.67, N=128). This underscores that plants rich in desirable nutrients may also be rich in antifeedants, posing challenges for orangutan consumption and digestion even as they provide a source of high-quality energy. Additionally, for some food categories where high tannin content is predicted, such as bark, orangutans may be choosing to eat species that are lower in these compounds. Funders: Boston University Undergraduate Research Opportunities Program, NSF (BCS-1638823, BCS-0936199); National Geographic; USFish/Wildlife (F18AP00898, F15AP00812, F13AP00920, 96200-0-G249, 96200-9-G110, 9414388); Leakey; Disney Wildlife Conservation; Wenner-Gren; Nacey-Maggioncalda; Orangutan Conservancy; Conservation, Food, and Health Foundation.more » « less
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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 genus
Piper (Piperaceae), on seed dispersal effectiveness (SDE) by ants, which are common secondary seed dispersers. We experimentally added amide extracts toPiper 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 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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Abstract This study investigated ant seed removal of
Piper sancti‐felicis, an early successional Neotropical shrub. NeotropicalPiper are 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 , andWasmannia recruiting to and harvestingP. sancti‐felicis seeds 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‐felicis fruits, affected foraging behavior in one genus of potential ant dispersers,Ectatomma . We found no effects of alkenylphenols on recruitment ofEctatomma to fruits, and thus, these compounds are unlikely to explain differences in ant recruitment among fruits of different maturity. Considering thatP. sancti‐felicis seeds 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‐felicis and suggests that other non‐myrmecochorous, vertebrate‐dispersed plants may similarly benefit from the recruitment to fruit by ants.
