Abstract
Petunia is endemic to South America grasslands; member of this genus exhibit variation in flower colour and shape, attracting bees, hawkmoths or hummingbirds. This group of plants is thus an excellent model system for evolutionary studies of diversification associated with pollinator shifts. Our aims were to identify the legitimate pollinator of Petunia secreta, a rare and endemic species, and to assess the importance of floral traits in pollinator attraction in this Petunia species. To determine the legitimate pollinator, field observations were conducted, and all floral visitors were recorded and evaluated. We also measured the nectar volume and sugar concentration. To characterize morphological cues for pollinators, we assessed the ultraviolet (UV)-light response in detached flowers, and characterized the floral pigments and pollen volatile scents for four different Petunia species that present different pollination syndromes. Petunia secreta shares the most recent ancestor with a white hawkmoth-pollinated species, P. axillaris, but presents flavonols and anthocyanin pigments responsible for the pink corolla colour and UV-light responses that are common to bee-pollinated Petunia species. Our study showed that a solitary bee in the genus Pseudagapostemon was the most frequent pollinator of P. secreta, and these bees collect only pollen as a reward. Despite being mainly bee-pollinated, different functional groups of pollinators visit P. secreta. Nectar volume, sugar concentration per flower, morphology and components of pollen scent would appear to be attractive to several different pollinator groups. Notably, the corolla includes a narrow tube with nectar at its base that cannot be reached by Pseudagapostemon, and flowers of P. secreta appear to follow an evolutionary transition, with traits attractive to several functional groups of pollinators. Additionally, the present study shows that differences in the volatiles of pollen scent are relevant for plant mutualistic and antagonist interactions in Petunia species and that pollen scent profile plays a key role in characterizing pollination syndromes.
Highlights
Pollination syndromes were first defined by Federico Delpino (Fenster et al 2004) as suites of floral traits associated with particular pollinator groups (Etcheverry and Alemán 2005)
We found that plant–pollinator interactions in P. secreta cannot be interpreted as a bee-pollination syndrome based only on UV-light response and corolla colour, and pollen volatiles can have an important effect on the legitimate pollinator, Pseudagapostemum sp., since volatile organic compounds (VOCs) in this species are associated with responses by bee antennae in other angiosperms that allow the bees to detect pollen from a distance before landing (Dötterl et al 2005; Dötterl and Vereecken 2010)
Our findings suggest that the interaction with Pseudagapostemon sp. bees has minimized the nectar volume and concentration of P. secreta compared to other sympatric Petunia species, while maximizing pollen scent emission, corolla colour and UV-light reflectance to improve the attraction of shorttongued bees, all characteristics that are ancestral conditions of the genus
Summary
Pollination syndromes were first defined by Federico Delpino (Fenster et al 2004) as suites of floral traits associated with particular pollinator groups (Etcheverry and Alemán 2005). Animal pollinators have acted as drivers of floral diversification and plant speciation (van der Niet and Johnson 2012; van der Niet et al 2014), and the pollinators that most frequently visit and efficiently pollinate the flowers select for a number of floral traits in the long term (Armbruster 2014). In this sense, it is expected that similar suites of floral traits can reflect convergent adaptation to a particular type of pollinator in distantly related taxa (Proctor et al 1996; Fenster et al 2004). Floral volatiles play an important role in attracting pollinators (Raguso 2001; Knudsen and Gershenzon 2006; Knudsen et al 2006); scent stimuli are learned more quickly than visual clues in bees (Arenas and Farina 2014) and may differentially attract certain pollinator species (Huber et al 2005; Klahre et al 2011)
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