Direct and indirect effects of marsupial browsing on a foundation tree species

Plant-mediated indirect effects can be important ecological drivers in plant communities, especially in systems where extended genetic effects of foundation species can shape communities and influence ecosystem dynamics. Here we investigate the direct and indirect effects of uncontrolled browsing by marsupial herbivores including the common brushtail possum Trichosurus vulpecula, Bennetts wallaby Macropus rufogriseus and the red-bellied pademelon Thylogale billardierii, in a Eucalyptus system known to have extended community and ecosystem genetic effects. In a common garden trial containing 525 full-sib families from an incomplete diallel crossing program located in northeastern Tasmania, Australia, we assessed the genetic basis to herbivore preferences, the impact of a single and repeated marsupial browsing event on tree fitness and morphological traits and the associated indirect plant-mediated effects on a subsequent herbivore, autumn gum moth Mnesampela privata. Marsupial browsing was not influenced by plant genetics, but spatial components instead affected the pattern of damage across the trial. Marsupial browsing had significant impacts on tree development, morphology and survival, resulting in reductions in survival, height and basal area, an increase proportion in multiple stems, delays in flowering as well as delays in phase change from juvenile to adult foliage. Fitness impacts were minimal in response to a once-off browsing event, but effects were exacerbated when trees suffered repeated browsing. We demonstrate clear plant-mediated indirect effects of marsupial browsing on subsequent tree use by an invertebrate herbivore, through induced changes in plant morphology. Such indirect effects have the potential to influence biotic community structure on a foundation species host-plant, and the evolutionary interactions that occur between organisms and the host-plant themselves.