Bouncy versus idles: On the different role of pollinators in the generalist Gentiana lutea L.

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Abstract

Generalist flowers are visited by a broad variety of insects that function as pollinators, occasional visitors and as pollen and/or nectar robbers. Moreover, among legitimate pollinators the pollination efficiency can be different. Nectar greatly affects visitor behaviour and fidelity to a certain species, influencing plant reproductive effort. In this study we have investigated a generalist system (Gentiana lutea L.), examining the role of flower visitors and quantifying the contribution of each pollinating taxon in three natural populations. In order to verify the level of generalization, we introduce an index of Pollinator Performance (PoP), based on insect visitation rate and cross-pollen transport efficiency. Our results confirm the high degree of pollinator-generalization of the study species. Nevertheless, flower visitors show various degree of pollinating performance, mainly defined by their sedentary versus dynamic behaviour. Sedentary insects enhance geitonogamous pollen transfer, which results in reduced seed set and pollen limitation. In particular, an unusual sluggish behaviour was observed in bumblebees feeding on nectar. The hexose-rich abundant nectar offered by G. lutea flowers is remarkably rich in proline and β-alanine amino acids: this composition presumably influences feeding choice and insect dynamism, likely exerting a narcotic effect on pollinators. The consequences on plant fitness are discussed in an evolutionary perspective.

Introduction

Nowadays the study of plant–pollinator interactions and the degree of their specialization is among the most lively and debated issues in plant biology and ecology. In particular, plant pollination systems present a continuum between specialists that depend on a single pollinator species to generalists pollinated by many animals (Waser and Ollerton, 2006).

Generally, only a fraction of total visitors acts as effective pollinators, depending on flower morphology, phenology and rewards, and on behavioural responses of flower visitors (Fisogni et al., 2011, Waser et al., 1996, Watts et al., 2012). At one extreme, visitors can act as nectar robbers, without contacting anthers or stigma and thus not providing any service to plant reproduction (Navarro and Medel, 2009, Stein and Hensen, 2011). On the other hand, pollinators carrying abundant pollen on their bodies may not always be the most efficient at depositing this pollen on stigmas (Adler and Irwin, 2006). At the same time, floral traits affect resource exploitation by pollinators, influencing search and handling times, and pollen receipt and export determining fitness differences amongst plants; it follows that field observations are fundamental in order to distinguish true pollinators and analyse their role in the transport of the male gametophyte to a compatible stigma.

Plant communities are typically constituted by different species that vary in abundance and in floral and plant traits, including rewards offered to pollinators. When foraging, pollinators make choices based on quantity, quality and type of rewards, with different responses at the individual and population level. Amongst biotic agents, nectar can strongly influence individual behaviour and fidelity to a certain species (Waddington, 2001). Floral nectar is the primary reward directly consumed by floral visitors (Nicolson, 2007, Westerkamp, 1996), and its most important components are sugars. Dominant sugars are the disaccharide sucrose and its constituent monosaccharides fructose and glucose. The proportion of the three sugars tends to be constant within species (Nicolson and Thornburg, 2007), with some exceptions (e.g., Herrera et al., 2006). Among-species sugar composition of nectar is highly variable, but convergence can be found in plants visited by similar pollinator guilds (Petanidou, 2007).

Amino acids are the second most abundant category of nectar solutes (Nepi et al., 2012, Nicolson and Thornburg, 2007), representing an important alimentary resource that can determine insect choices (Bertazzini et al., 2010, Nicolson, 2007, Petanidou et al., 2006). Nectars of species pollinated by different groups of visitors differ more in their amino acid concentration than in composition (Baker and Baker, 1986, Gardener and Gillman, 2001). Moreover, pollinator choice can shape sugar and nectar amino-acidic composition in relation to stimuli and dietary preferences of different insect families (Nicolson and Thornburg, 2007, Petanidou et al., 2006, Petanidou, 2005). Amongst other nectar constituents, secondary compounds and alcohols may have toxic effects and induce behaviour alterations of taxonomically unrelated floral visitors (Adler, 2000, Clinch et al., 1972, Jakubska et al., 2005). Alcohols are usually of microbiological origin rather than produced by the plant itself: nectars contaminated by yeasts commonly produce ethanol, which in turn can induce narcotic effects on pollinators like bumblebees (Kevan et al., 1988), wasps (Ehlers and Olesen, 1997) and rodents (Wiens et al., 2008), acting on plant-pollinator interaction.

To investigate how floral traits affect pollinator guilds in a phenotypically generalist species, we studied insect visitation, pollen transfer and reproductive success in the perennial herb Gentiana lutea L., considering three natural populations across its distribution area. In particular our main purposes were (1) to describe the level of flower generalization, quantifying the relative importance of each pollinating taxon, and (2) to analyse pollinator behaviour in relation to nectar composition. Finally, we discuss our findings in an evolutionary perspective.

Section snippets

Study species

Gentiana lutea L. (Gentianaceae) is a long-lived species that mainly grows on calcareous (sub)-alpine pastures (800–2500 m a.s.l.), from the Pyrenees to Asia Minor (Anchisi et al., 2010). Fertile stems show yellow flowers grouped in pseudo-whorls; the inflorescence develops in basipetal direction and a pseudo-whorl blooms in centrifugal way (Kozuharova, 1994). Flowering occurs between June and July; flowers present a sessile ovary with nectar glands at the base, a bilamellate stigma and free

Flower visitors

Total time of insect observations was 13 h and 15 min (Table 1). Flower visitors belong to four orders: Hymenoptera are the most represented, followed by Coleoptera, Diptera, and Lepidoptera. Bumblebee species were clustered in two groups based on body-colour pattern, since the distinction at species level was not possible in the field, and taxonomic identification was performed on sampled specimens (Table 2). Bumblebees were the most represented group at Mt. Grande (more than 50% in total),

Discussion

Gentiana lutea flowers are phenotypically generalized: wide open corollas provide to insects of different size an open and easy access to the nectar reward secreted at the base of the gynoecium. There are no evident morphological or phenological constraints towards visitors, which are abundant through all flower lifespan. Our study shows that all insects which visit G. lutea flowers have the potential to be pollinators, indicating a significant level of functional generalization (Ollerton et

Acknowledgements

We thank Silvia Crema, Valentina Lucchetta, Michela Albertini and Valentina Manca for help during field-work, Nicola Sitta and Alessandro Alessandrini for helpful information on Mt. Grande population, Annalisa Managlia and Umberto Mossetti for technical assistance, and Giovanni Cristofolini for scientific support and valuable suggestions. We also thank the National Park “Parco Nazionale dei Monti Sibillini” for permitting field investigations. The research was supported by the Italian MIUR

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    Both authors contributed equally to this work, and should be considered co-first authors.

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