The symbiosis with beneficial soil microbiota critically affects plant physiology, growth and community structure. Recent findings further suggest that these effects translate into changes in aboveground plant-herbivore interactions. However, virtually unknown is whether or not variation in the microbially-mediated defensive plant phenotype actually results in differential responses of plant consumers and ultimately plant fitness in nature. In a field study in Costa Rica (Osa Peninsula) we screened a large population of wild lima bean (Phaseolus lunatus L.) for spatial variation in direct (HCNp, cyanogenic potential) and indirect (EFN; extrafloral nectar) defense against herbivores, rhizobial strains, as well as type and abundance of herbivores. In subsequent transplanting experiments using either plants, rhizobia, or both from different locations (coastal and inland sites), we studied changes in chemical defensive plant phenotypes, plant performance, and survival at the native and introduced sites.
Results/Conclusions
Comparing cyanogenic potential (HCNp) and extrafloral nectar (EFN) among individual plants in the population (N= 80 plants) revealed significant differences in both traits depending on location. Plants near the coastline showed significantly higher HCNp than plants on nearby inland slopes (71±12 vs. 27±8 µmol HCN g-1 fw). Quantitative EFN secretion showed the opposite pattern with significantly higher EFN production in inland compared to coastal plants (6.2±1.1 vs. 3.9±0.8 mg sugar g-1 dw 12h-1). Comparing rhizobial strains (16S rDNA, nifH) colonizing individual plants at the coastal and more inland locations revealed distinct distribution patterns which were significantly correlated with both location and chemical phenotypes of host plants. Experiments with sterile cuttings in combination with inoculation and transplanting experiments showed that both plant traits (HCNp and EFN) were genetically controlled but that colonization by different rhizobial strains further enhanced the expression of either defense trait. Surveys of herbivore communities revealed differences in herbivore species composition with specialist lepidopteran herbivores being dominant at inland locations whereas herbivory by generalist iguanas was observed mostly at the coastal locations. We conclude that small-scale variation in plant defense traits as well as defense-mediating effects of specific rhizobial strains are adaptive under natural conditions.