Relationships among nectar‐dwelling yeasts, flowers and ants: patterns and incidence on nectar traits

Abstract

Nectar‐dwelling yeasts are emerging as widely distributed organisms playing a potentially significant and barely unexplored ecological role in plant pollinator mutualisms. Previous efforts at understanding nectar–pollinator–yeast interactions have focused on bee‐pollinated plants, while the importance of nectarivorous ants as vectors for yeast dispersal remains unexplored so far. Here we assess the abundance and composition of the nectar fungal microbiota of the ant‐pollinated plant Cytinus hypocistis, study whether yeast transmission is coupled with ant visitation, and discern whether ant‐ transported yeasts promote changes in nectar characteristics. Our results show that a high percentage of flowers (77%) and plants (94%) contained yeasts, with yeast cell density in nectar reaching up to 6.2 × 104 cells mm−3, being the highest densities associated with the presence of the nectar‐specialist yeast Metschnikowia reukaufii. The establishment of fungal microbiota in nectar required flower visitation by ants, with 70% of yeast species transported by them being also detected in nectar. Ant‐vectored yeasts diminished the nutritional quality of nectar, with flowers exposed to pollinators and yeasts containing significantly lower nectar sugar concentration than virgin flowers (13.4% and 22.8%, respectively). Nectar of flowers that harbored M. reukaufii showed the lowest quality, with nectar concentration declining significantly with increasing yeast density. Additionally, yeasts modified patterns of interpopulation variation in nectar traits, homo genizing differences between populations in some nectar attributes. We show for the first time that the outcome of the tripartite pollinator–flower–yeast interaction is highly dependent on the identity and inherent properties of the participants, even to the extent of influencing the species composition of this ternary system, and can be mediated by ecological characteristics of plant populations. Through their influence on plant functional traits, yeasts have the potential to alter nectar consumption, pollinator foraging behavior and ultimately plant reproduction.

Metschnikowia drakensbergensis sp. nov. and Metschnikowia caudata sp. nov., endemic yeasts associated with Protea flowers in South Africa

“…The dominant yeasts recovered in those plant species were the small-spored Metschnikowia clade species Candida rancensis, M. reukaufii and M. koreensis. These three species appear to be cosmopolitan, being commonly isolated worldwide from floral nectar in plants pollinated by a diverse array of pollinators, primarily bees, butterflies and birds (BryschHerzberg, 2004;Pozo et al, 2011;Belisle et al, 2012;de Vega & Herrera, 2012). As nectar yeasts are thought to be vectored by the main animal visitors, and the newly described species appear associated with a small set of plant species visited by beetles, our findings suggests that the novel species are highly selective in terms of host and habitat requirements.…”

“…This last strain, also a member of the Metschnikowia clade, was obtained from a specimen of Heterochelus sp. in one of the study populations, on Mount Gilboa, in 2010(de Vega et al, 2012. It was considered premature to describe a novel species from this single strain.…”

“…; Scarabaeidae) and a honeybee (Apis mellifera scutellata) in previous sampling carried out in 2008 from insects visiting Protea flowers. Collection details for the insect isolates were given by de Vega et al (2012).…”

“…Yeasts living in association with African plants and their beetles are only beginning to receive attention, even though their diversity may plausibly be as high as or even higher than that observed on other continents. Three beetle-associated Metschnikowia species have been described so far in Africa (Lachance et al, 2006a(Lachance et al, , 2008de Vega et al, 2012). In an effort to gain further insight into the yeast biota associated with plants visited by beetles in poorly studied areas, we conducted a survey in the KwaZulu-Natal region of South Africa.…”

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

“…It is also commonly found in the nectar of other plant species [24] and on bees, ants, hummingbirds and other pollinators [23,25,26]. We isolated M. reukaufii from M. aurantiacus flowers at JRBP in 2010 by plating diluted nectar samples on yeast-malt agar (YMA; Difco, Sparks, MD, USA).…”