Disruption of pollination by herbivores is rescued by nectar yeasts

Abstract

Abstract Attracting pollinators to achieve successful reproduction is a key challenge for wild plants that may be disturbed by complex multispecies interactions in nature. Pairwise plant–pollinator interactions have traditionally been studied for decades, while ignoring other ecological players may obscure a comprehensive understanding on how plants recruit partners or combat enemies in the pollination process. Hence, integrated studies considering the inherent complexity of ecological interactions are needed, which may open up new perspectives for deciphering intricate systems and predicting ecological consequences. We examined the presence of nectar yeasts using a combination of high‐throughput sequencing, cultivation and microscopy and quantified floral herbivory by evaluating the incidence of flowers with visible holes in 13 natural populations of Iris bulleyana in the Hengduan Mountains of southwest China during 2017–2022. We combined yeast inoculation and herbivore manipulation treatments to illustrate the isolated and combined impacts of two contrasting nectarivorous organisms, the ascomycetous yeast Metschnikowia reukaufii and adult sawflies, on pollinator visitation and plant reproductive success in two populations. In the lab, we first employed gas chromatography–mass spectrometry to profile the volatile metabolites of yeast‐inoculated nectar relative to control, followed by a behavioural bioassay to test the preference of honeybees for these microbial volatiles. Yeasts commonly inhabited floral nectar and insect herbivores frequently bit holes in the perianth tube to consume nectar and nectaries. Nectar yeasts indirectly facilitated plant reproduction through increased pollinator visits, probably because of microbial metabolism as honeybees preferred nectar volatiles produced by yeasts in behavioural bioassays. Insect herbivores increased total floral visits but reduced legitimate visits by inducing legitimate‐to‐robbing behavioural changes of honeybees, thus leading to lower seed production. The detrimental effect of herbivory was mitigated by the presence of yeasts, which diminished the relative proportion of robbing visits and thereby ‘rescued’ flowers from reproductive failure. Synthesis: Overall, we found contrasting effects of non‐pollinator species, including both micro‐ and macro‐organisms, on plant–pollinator interactions in a biodiversity hotspot, where pollination deficit may be a ubiquitous phenomenon. Our findings suggest that both microbial and herbivory effects are likely to be important in explaining the exact causes of pollen limitation in species‐rich areas, highlighting the biological context dependence of species interactions in natural ecosystems.