Inhospitable sweetness: nectar filtering of pollinator-borne inocula leads to impoverished, phylogenetically clustered yeast communities

Abstract

Identifying the rules and mechanisms that determine the composition and diversity of naturally co-occurring species assemblages is a central topic in community ecology. Although micro-organisms represent the 'unseen majority' of species, individuals and biomass in many ecosystems and play pivotal roles in community development and function, the study of the factors influencing the assembly of microbial communities has lagged behind that of plant and animal communities. In this paper, we investigate experimentally the mechanisms accounting for the low species richness of yeast communities inhabiting the nectar of the bumble-bee-pollinated Helleborus foetidus (Ranunculaceae), and explore the relationships between community assembly rules and phylogenetic relatedness. By comparing yeast communities on the glossae of foraging bumble-bees (the potential species pool) with those eventually establishing in virgin nectar probed with bee glossae (the realized community), we address the questions: (i) does nectar filter yeast inocula, so that the communities eventually established there are not random subsamples of species on bumble-bee glossae? and (ii) do yeast communities establishing in H. foetidus nectar exhibit some phylogenetic bias relative to the species pool on bumble-bee glossae? Results show that nectar filtering leads to species-poor, phylogenetically clustered yeast communities that are a predictable subset of pollinator-borne inocula. Such strong habitat filtering is probably due to H. foetidus nectar representing a harsh environment for most yeasts, where only a few phylogenetically related nectar specialists physiologically endowed to tolerate a combination of high osmotic pressure and fungicidal compounds are able to develop.

Phylogenetic relatedness predicts priority effects in nectar yeast communities

“…New flowers are initially sterile and yeasts are thought to colonize mainly via pollinators [24]. While pollinators vector a wide array of fungi, nectar presents a strong habitat filter and only a small subset of these species are able to colonize [44]. This filter probably acts in two ways.…”

“…This filter probably acts in two ways. First, species must have high osmotolerance to grow in approximately 20-50% sugar concentrations found in nectar [44]. In addition, nectar often contains strong anti-microbial chemicals that may require specific adaptations to tolerate [45,46].…”

Nectar bacteria, but not yeast, weaken a plant–pollinator mutualism

“…It has been pointed out that the community ecology of nectar microbes cannot be understood without considering plantpollinator interactions [11,19]. This is because many nectar rspb.royalsocietypublishing.org Proc R Soc B 280: 20122601 microbes depend on pollinators to disperse between flowers [11,26].…”

“…This is because microbial species vary in their effects on pollination, as we have shown here. As a consequence, factors affecting microbial community assembly in nectar, including habitat filtering [19], niche breadth [48], dispersal [23,25] and competition and priority effects [22] should no longer be of interest only to microbial ecologists, but also to pollination biologists. Our findings suggest several directions of future research on plant -pollinator -microbe interactions.…”

“…sugar consumption) and other ecological traits (e.g. tolerance to high osmotic pressure, hydrogen peroxide and oxygen limitation) that allow them to thrive in the rather unique habitat [11,19,20]. Nonetheless, given the physiological and metabolic diversity of microbial species, their effects on plant-pollinator mutualisms may still differ.…”