Herbivore specificity and the chemical basis of plant-plant communication in Baccharis salicifolia (Asteraceae).

It is well known that plant damage by leaf-chewing herbivores can induce resistance in neighbouring plants. It is unknown whether such communication occurs in response to sap-feeding herbivores, whether communication is specific to herbivore identity, and the chemical basis of communication, including specificity. We carried out glasshouse experiments using the California-native shrub Baccharis salicifolia and two ecologically distinct aphid species (one a dietary generalist and the other a specialist) to test for specificity of plant-plant communication and to document the underlying volatile organic compounds (VOCs). We show specificity of plant-plant communication to herbivore identity, as each aphid-damaged plant only induced resistance in neighbours against the same aphid species. The amount and composition of induced VOCs were markedly different between plants attacked by the two aphid species, providing a putative chemical mechanism for this specificity. Furthermore, a synthetic blend of the five major aphid-induced VOCs (ethanone, limonene, methyl salicylate, myrcene, ocimene) triggered resistance in receiving plants of comparable magnitude to aphid damage of neighbours, and the effects of the blend exceeded those of individual compounds. This study significantly advances our understanding of plant-plant communication by demonstrating the importance of sap-feeding herbivores and herbivore identity, as well as the chemical basis for such effects.

Ecological convergence in phytochemistry and flower-insect visitor interactions along an Andean elevation gradient.

The diversity of specialized molecules produced by plants radiating along ecological gradients is thought to arise from plants' adaptations to local conditions. Therefore, closely related species growing in similar habitats should phylogenetically converge, or diverge, in response to similar climates, or similar interacting animal communities. We here asked whether closely related species in the genus Haplopappus (Asteraceae) growing within the same elevation bands in the Andes, converged to produce similar floral odors. To do so, we combine untargeted analysis of floral volatile organic compounds with insect olfactory bioassay in congeneric Haplopappus (Asteraceae) species growing within the same elevation bands along the Andean elevational gradient. We then asked whether the outcome of biotic interactions (i.e., pollination vs. seed predation) would also converge across species within the same elevation. We found that flower odors grouped according to their elevational band and that the main floral visitor preferred floral heads from low-elevation band species. Furthermore, the cost-benefit ratio of predated versus fertilized seeds was consistent within elevation bands, but increased with elevation, from 6:1 at low to 8:1 at high elevations. In the light of our findings, we propose that climate and insect community changes along elevation molded a common floral odor blend, best adapted for the local conditions. Moreover, we suggest that at low elevation where floral resources are abundant, the per capita cost of attracting seed predators is diluted, while at high elevation, sparse plants incur a higher herbivory cost per capita. Together, our results suggest that phytochemical convergence may be an important factor driving plant-insect interactions and their ecological outcomes along ecological gradients.

La gran diversidad de moléculas especializadas producidas por plantas a lo largo de gradientes ecológicos se atribuye a la adaptación de plantas a sus condiciones locales. Por tanto, especies de plantas estrechamente relacionadas que crecen en hábitats similares deberían de converger en la producción de fitoquímicos similares, en respuesta a climas similares o comunidades de animales con las que interactúan. En este estudio exploramos esta hipótesis caracterizando la metabolómica no dirigida de compuestos orgánicos volátiles florales y conduciendo bioensayos olfativos de insectos en especies cogenéticas del género Haplopappus (Asteraceae) que crecen dentro de las mismas bandas altitudinales a lo largo de un gradiente altitudinal andino. Conjuntamente investigamos si el resultado de las interacciones bióticas (ej. polinización versus depredación) también convergen entre especies que crecen dentro de la misma banda altitudinal. Encontramos que los olores de las flores se agrupan de acuerdo con su banda altitudinal, y que el visitante floral más común prefiere los capítulos florales de las especies de bandas de baja elevación. Además, la relación entre el costo (depredación) y beneficio (polinización) es consistente dentro de las bandas de elevación pero incrementa con elevación, de 6:1 en elevaciones bajas a 8:1 en elevaciones altas. Por lo tanto, proponemos que los cambios climáticos y la comunidad de insectos a lo largo de la elevación resultaron en una mezcla común de olores de flores, mejor adaptada a las condiciones locales. Asimismo, sugerimos que a baja altura donde los recursos florales son abundantes, el costo per cápita de atraer a los depredadores de semillas se diluye, mientras que en sitios altos, las plantas escasas incurren en un costo per cápita de herbivoría más alto. Nuestros resultados sugieren que la convergencia fitoquímica puede ser un factor importante que impulsa las interacciones planta­insecto y sus resultados ecológicos a lo largo de gradientes ecológicos.

Herbivore Diet Breadth and Host Plant Defense Mediate the Tri-Trophic Effects of Plant Toxins on Multiple Coccinellid Predators.

Host plant defenses are known to cascade up food chains to influence herbivores and their natural enemies, but how herbivore and predator traits and identity mediate such tri-trophic dynamics is largely unknown. We assessed the influence of plant defense on aphid and coccinellid performance in laboratory trials with low- vs. high-glucosinolate varieties of Brassica napus, a dietary specialist (Brevicoryne brassicae) and generalist (Myzus persicae) aphid, and five species of aphidophagous coccinellids. The performance of the specialist and generalist aphids was similar and unaffected by variation in plant defense. Aphid glucosinolate concentration and resistance to predators differed by aphid species and host plant defense, and these effects acted independently. With respect to aphid species, the dietary generalist aphid (vs. specialist) had 14% lower glucosinolate concentration and coccinellid predators ate three-fold more aphids. With respect to host plant variety, the high-glucosinolate plants (vs. low) increased aphid glucosinolate concentration by 21%, but had relatively weak effects on predation by coccinellids and these effects varied among coccinellid species. In turn, coccinellid performance was influenced by the interactive effects of plant defense and aphid species, as the cascading, indirect effect of plant defense was greater when feeding upon the specialist than generalist aphid. When feeding upon specialist aphids, low- (vs. high-) glucosinolate plants increased coccinellid mass gain by 78% and accelerated development by 14%. In contrast, when feeding upon generalist aphids, low- (vs. high-) glucosinolate plants increased coccinellid mass gain by only 11% and had no detectable effect on development time. These interactive effects of plant defense and aphid diet breadth on predator performance also varied among coccinellid species; the indirect negative effects of plant defenses on predator performance was consistent among the five predators when transmitted via the dietary specialist aphid, but these effects varied substantially among predators-in both the magnitude and direction-when transmitted via the dietary generalist aphid. Accordingly, the cascading effect of plant defense on predators was stronger in magnitude and more consistent among predator taxa when transmitted by the specialist than generalist herbivore. Overall, these findings support a central role of herbivore diet breadth in mediating both the strength and contingency of tri-trophic interactions.