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  1. 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. 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. Abstract

    1. Although associative learning is widespread across animals, its ecological importance is difficult to assess because learning is rarely studied in the field, where informative cues are juxtaposed against complex backgrounds of uninformative noise.

    2. Ants rely heavily on chemical cues for foraging and engage in many ecologically important interactions with plants. Nevertheless, little is known about the role of associative learning of plant chemicals in ant foraging for carbohydrates.

    3. In a field setting, the present study investigated whether the distantly related ant speciesFormica podzolica(Formicinae subfamily) andTapinoma sessile(Dolichoderinae subfamily) exhibited associative learning of the chemical cues from two co‐occurring plant species that are taxonomically and chemically distinct (Asteraceae:Helianthella quinquenervisand Apiaceae:Ligusticum porteri).

    4. For two consecutive summers, ants were trained to forage from artificial sugar‐rich baits associated with the leaf chemicals from eitherH. quinquenervisorL. porterifor 24 h, after which a two‐choice test was deployed to assess whether ants would be more likely to select baits associated with the same (versus different) plant chemicals on which they had been trained.

    5. The present study demonstrates associative learning of chemicals from both plant species, and these effects were consistent between ant species and years; training increased bait occupancy from 42% on the untrained scent to 66% on the trained scent. These results indicate that associative odour‐learning may be widespread across ants and serve as an important mechanism mediating ant selection of resources.

     
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  5. Abstract

    The abiotic environment drives species abundances and distributions both directly and indirectly through effects on multi‐trophic species interactions. However, few studies have documented the individual and combined consequences of these direct and indirect effects.

    We studied an ant‐tended aphid along an elevational gradient, where lower elevations were more arid. Hypotheses of stronger species interactions at lower elevations and a greater sensitivity of higher trophic levels to climate led us to predict increased top‐down control of aphids by natural enemies (third trophic level) but even stronger protection from mutualist ants (fourth trophic level) with increasing aridity. As a result, we predicted that mutualism strength and aphid abundance would increase with aridity.

    We documented patterns of aphid abundance and tested for both the direct and multi‐trophic indirect effects of aridity on aphid performance. To do so, we used both observational and manipulative methods across two years in replicate high‐ and low‐elevation valleys, where summer temperatures decreased by 3.7°C and precipitation increased by 27 mm/mo from low to high elevations.

    Aphid colonies were 75% larger in the most (vs. least) arid sites, and this was best explained by changes in interactions with predators and ants. Aphids were unaffected by the direct effects of the abiotic environment or its indirect effects via host plant quality. In contrast, natural enemy effects increased with aridity; under ant exclusion, natural enemies had no effect on aphids in the least arid sites but depressed colony growth by 252% in the most arid sites. Ant activity also increased with aridity, with ants discovering more aphid colonies and experimental baits and allocating more foragers per aphid, although there was no effect of aridity on ant abundance or community composition. Correspondingly, the mutualist services provided by ants increased with aridity; ants provided no benefits to aphids in the least arid sites but doubled colony growth in the most arid sites.

    In summary, an elevational cline in herbivore abundance was driven by a monotonic increase in trophic‐level sensitivity to aridity. These findings illustrate that predicting species responses to climate change will require a multi‐trophic perspective.

     
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