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1. 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)

   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. 

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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. 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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4. Fruit odorants mediate co-specialization in a multispecies plant–animal mutualism

   https://doi.org/10.1098/rspb.2021.0312  

   Santana, Sharlene E.; Kaliszewska, Zofia A.; Leiser-Miller, Leith B.; Lauterbur, M. Elise; Arbour, Jessica H.; Dávalos, Liliana M.; Riffell, Jeffrey A. (August 2021, Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Despite the widespread notion that animal-mediated seed dispersal led to the evolution of fruit traits that attract mutualistic frugivores, the dispersal syndrome hypothesis remains controversial, particularly for complex traits such as fruit scent. Here, we test this hypothesis in a community of mutualistic, ecologically important neotropical bats ( Carollia spp.) and plants ( Piper spp.) that communicate primarily via chemical signals. We found greater bat consumption is significantly associated with scent chemical diversity and presence of specific compounds, which fit multi-peak selective regime models in Piper . Through behavioural assays, we found Carollia prefer certain compounds, particularly 2-heptanol, which evolved as a unique feature of two Piper species highly consumed by these bats. Thus, we demonstrate that volatile compounds emitted by neotropical Piper fruits evolved in tandem with seed dispersal by scent-oriented Carollia bats. Specifically, fruit scent chemistry in some Piper species fits adaptive evolutionary scenarios consistent with a dispersal syndrome hypothesis. While other abiotic and biotic processes likely shaped the chemical composition of ripe fruit scent in Piper , our results provide some of the first evidence of the effect of bat frugivory on plant chemical diversity. 

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5. Frugivory, seed dispersal, and seed predation by Bornean orangutans (Pongo pygmaeus wurmbii)

   Blackburn, A; Susanto, TW; Knott, CD (January 2020, 6th Annual Meeting of the Northeastern Evolutionary Primatologists)

   null (Ed.)

   Seed dispersal is important for forest growth, maintenance, and regeneration. Orangutans are large-bodied frugivores with ecological roles as seed predators and seed dispersers. However, little is known about orangutans’ ecological roles and how they relate to orangutans’ patterns of frugivory. We investigated Bornean orangutans’ (Pongo pygmaeus wurmbii) ecological roles at the Cabang Panti Research Station in Gunung Palung National Park, Indonesian Borneo. We collected orangutan feces (n=401) and analyzed them for intact seeds (August 2018 to March 2020). We observed orangutan fruit handling behavior for 306 feeding bouts for 53 fruit genera to measure how often orangutans swallow, spit, or predate seeds. We used Ivlev’s Electivity Index to analyze fruit preference using long-term feeding data and phenology data (2014-2019). Lastly, we combined fruit preference with fruit handling behavior using the seed dispersal effectiveness framework to identify which fruit taxa were most effectively dispersed. Orangutans dispersed seeds in 71.8% of fecal samples with a mean of 27.9 ±4.5 (SD=0.95) seeds (>2mm) per fecal sample. Orangutans predated seeds more often than spitting or swallowing seeds (predating= 42.1% of fruit feeding time; spitting= 21.8%; swallowing= 12.5%; mixed behaviors= 10.6%, not observed=12.0%). Additionally, the top five preferred fruit genera, (Dialium, Sindora, Scaphium, Magnifera, and Spatholobus) were highly predated (0 to 5% of seeds dispersed). We identified Alangium and Tetramerista as the most effectively dispersed genera, orangutans frequently dispersed and preferred these fruits. We found orangutans are frequent seed predators, but this overlaps with their seed dispersal role, and we describe orangutans’ seed dispersal contribution. Funders: NSF (9414388, BCS-1638823, BCS-0936199); National Geographic; USFish/Wildlife (F18AP00898, F15AP00812, F13AP00920, 96200-0-G249, 96200-9-G110); Leakey; Disney Conservation Fund; Wenner-Gren; Nacey-Maggioncalda; Conservation-Food-Health; Orangutan Conservancy; Woodland Park Zoo; Boston University GRAF 

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