Elevational cline in herbivore abundance driven by a monotonic increase in trophic-level sensitivity to aridity.

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.

Relative effects of genetic variation sensu lato and sexual dimorphism on plant traits and associated arthropod communities.

Intraspecific plant trait variation can have cascading effects on plant-associated biotic communities. Sexual dimorphism is an important axis of genetic variation in dioecious plants, but the strength of such effects and the underlying mechanisms relative to genetic variation are unknown. We established a common garden with 39 genotypes of Baccharis salicifolia sampled from a single population that included male and female genotypes and measured plant traits and quantified associated arthropod communities. Genetic variation sensu lato (genotypic variation) had strong effects on most plant traits (flower number, relative growth rate, specific leaf area, percent water content, carbon-nitrogen ratio, monoterpene but not sesquiterpene concentrations) and on herbivore and predator density, and on arthropod community composition (relative abundance of 14 orders). In contrast, sexual dimorphism had weaker effects on only a few plant traits (flower number and relative growth rate), on predator density, and on arthropod community composition, but had no effect on herbivore density. Variation in flower number drove genetic variation sensu lato and sex dimorphism in predator density and arthropod community composition. There was unique genetic variation sensu lato in herbivore density (positively) associated with monoterpene concentration and in arthropod community composition associated with specific leaf area and carbon-nitrogen ratio. There was unique sexual dimorphism in arthropod community composition associated with plant relative growth rate. Together, these results demonstrate that genetic variation sensu lato and sexual dimorphism can shape plant-associated arthropod communities via both parallel and unique mechanisms, with greater overall effects of the former.

Abiotic mediation of a mutualism drives herbivore abundance.

Species abundance is typically determined by the abiotic environment, but the extent to which such effects occur through the mediation of biotic interactions, including mutualisms, is unknown. We explored how light environment (open meadow vs. shaded understory) mediates the abundance and ant tending of the aphid Aphis helianthi feeding on the herb Ligusticum porteri. Yearly surveys consistently found aphids to be more than 17-fold more abundant on open meadow plants than on shaded understory plants. Manipulations demonstrated that this abundance pattern was not due to the direct effects of light environment on aphid performance, or indirectly through host plant quality or the effects of predators. Instead, open meadows had higher ant abundance and per capita rates of aphid tending and, accordingly, ants increased aphid population growth in meadow but not understory environments. The abiotic environment thus drives the abundance of this herbivore exclusively through the mediation of a protection mutualism.

Fruit secondary metabolites alter the quantity and quality of a seed dispersal mutualism.

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 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 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.

Fruit secondary metabolites shape seed dispersal effectiveness.

Plant secondary metabolites (PSMs) play a central role in seed dispersal and fruit defense, with potential for large impacts on plant fitness and demography. Yet because PSMs can have multiple interactive functions across seed dispersal stages, we must systematically study their effects to determine the net consequences for plant fitness. To tackle this issue, we integrate the role of fruit PSMs into the seed dispersal effectiveness (SDE) framework. We describe PSM effects on the quantity and quality of animal-mediated seed dispersal, both in pairwise interactions and diverse disperser communities, as well as trade-offs that occur across dispersal stages. By doing so, this review provides structure to a rapidly growing field and yields insights into a critical process shaping plant populations.

Plant chemical mediation of ant behavior.

Ants are ecologically dominant members of terrestrial communities. Ant foraging is often strongly associated with plants and depends upon associative learning of chemicals in the environment. As a result, plant chemicals can affect ant behaviors and, in so doing, have strong multi-trophic indirect effects. Plant chemicals mediate ant behaviors in the contexts of floral visitation, seed dispersal and predation, leaf cutting, interactions with ant-mutualist host plants, interactions with mutualist and prey insects in plant canopies, and plant predation of ants by carnivorous plants. Here, we review what is known about these differing contexts in which plant chemicals influence ant behavior, the mechanisms by which ants are affected by plant chemicals, and future directions within these topics.