An official website of the United States government
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.
more »
« less
Fruit secondary metabolites alter the quantity and quality of a seed dispersal mutualism
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.
more »
« less
- Award ID(s):
- 1856776
- PAR ID:
- 10410185
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology
- Volume:
- 104
- Issue:
- 5
- ISSN:
- 0012-9658
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract 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.more » « less
-
This study investigated ant seed removal of Piper sancti-felicis, an early successional Neotropical shrub. Neotropical Piper are a classic example of bat-dispersed plants, but we suggest that ants are underappreciated dispersal agents. We identified eleven ant species from the genera Aphaenogaster, Ectatomma, Paratrechina, Pheidole, Trachymyrmex, and Wasmannia recruiting to and harvesting P. 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 in P. sancti-felicis fruits, affected foraging behavior in one genus of potential ant dispersers, Ectatomma. We found no effects of alkenyl- phenols on recruitment of Ectatomma to fruits, and thus, these compounds are un- likely to explain differences in ant recruitment among fruits of different maturity. Considering that P. sancti-felicis seeds have no apparent adaptations for ant disper- sal, 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 of P. sancti-felicis and suggests that other non-myrmecochorous, vertebrate-dispersed plants may similarly benefit from the recruitment to fruit by ants.more » « less
-
Orangutans are large-bodied frugivores predicted to be effective seed dispersers. We studied Bornean orangutan (Pongo pygmaeus wurmbii) seed dispersal effectiveness, by measuring the quantity of seeds dispersed and the quality of dispersal in Gunung Palung National Park, Borneo, Indonesia (August 2018 to August 2019). For dispersal quality we conducted germination experiments, measured germination rates, and modeled dispersal distances. We systematically collected orangutan fecal samples, feeding behavior, and GPS tracks during focal follows. We sieved 549 fecal samples collected from 36 orangutans and identified the seeds, and of the fecal samples collected 75.2% contained seeds. A total of 24 genera were dispersed via endozoochory. Germination experiments were conducted with orangutan defecated seeds and seeds from fruits. A significantly higher percent of orangutan defecated seeds germinated for 5 out of 6 genera than control seeds with pulp (p<0.01). A significantly higher percent of orangutan defecated seeds germinated for 3 out of 6 genera compared to control seeds without pulp (p<0.01). Gut transit times in wild orangutans ranged from 39.5 to 87 hours. Finally, we modeled seed dispersal distances using orangutan movement tracks (n= 30) with gut passage durations of 45 and 60 hours. Gut retention times of 45 hours resulted in a mean dispersal distance of 507 ± 123m, and 60 hours resulted in a mean distances of 592 ± 115m. We conclude orangutans are effective seed dispersers, as orangutans disperse a wide variety of genera over medium to long distances and defecated seeds exhibit high germinability. Orangutans are large-bodied frugivores predicted to be effective seed dispersers. We studied Bornean orangutan (Pongo pygmaeus wurmbii) seed dispersal effectiveness, by measuring the quantity of seeds dispersed and the quality of dispersal in Gunung Palung National Park, Borneo, Indonesia (August 2018 to August 2019). For dispersal quality we conducted germination experiments, measured germination rates, and modeled dispersal distances. We systematically collected orangutan fecal samples, feeding behavior, and GPS tracks during focal follows. We sieved 549 fecal samples collected from 36 orangutans and identified the seeds, and of the fecal samples collected 75.2% contained seeds. A total of 24 genera were dispersed via endozoochory. Germination experiments were conducted with orangutan defecated seeds and seeds from fruits. A significantly higher percent of orangutan defecated seeds germinated for 5 out of 6 genera than control seeds with pulp (p<0.01). A significantly higher percent of orangutan defecated seeds germinated for 3 out of 6 genera compared to control seeds without pulp (p<0.01). Gut transit times in wild orangutans ranged from 39.5 to 87 hours. Finally, we modeled seed dispersal distances using orangutan movement tracks (n= 30) with gut passage durations of 45 and 60 hours. Gut retention times of 45 hours resulted in a mean dispersal distance of 507 ± 123m, and 60 hours resulted in a mean distances of 592 ± 115m. We conclude orangutans are effective seed dispersers, as orangutans disperse a wide variety of genera over medium to long distances and defecated seeds exhibit high germinability. Funders: National Science Foundation (BCS-1638823); National Geographic Society; US Fish and Wildlife Services (F19AP00798; F18AP00898); Disney Wildlife Conservation Fundmore » « less
-
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.more » « less
