Inflorescence architecture affects pollinator behaviour and mating success in Spiranthes sinensis (Orchidaceae)

Abstract

Summary• Despite the wide inflorescence diversity among angiosperms, the effects of inflorescence architecture (three-dimensional flower arrangement) on pollinator behaviour and mating success have not been sufficiently studied in natural plant populations.• Here, we investigated how inflorescence architecture affected inter-and intra-plant pollinator movements and consequent mating success in a field population of Spiranthes sinensis var. amoena (S. sinensis). In this species, the flowers are helically arranged around the stem, and the degree of twisting varies greatly among individuals. The large variation in inflorescence architecture in S. sinensis results from variation in a single structural parameter, the helical angle (the angular distance between neighbour-flower directions).• The numbers of visits per inflorescence and successive probes per visit by leaf-cutting bees decreased with helical angle, indicating that individual flowers of tightly twisted inflorescences received less visitations. As expected from pollinator behaviour, pollinia removal and fruit set of individual flowers decreased with helical angle. Meanwhile, geitonogamy decreased in tightly twisted inflorescences.• Our novel findings demonstrate that natural variation in inflorescence architecture significantly affects pollinator behaviour and reproductive success, suggesting that inflorescence architecture can evolve under pollinator-mediated natural selection in plant populations. We also discuss how diverse inflorescence architectures may have been maintained in S. sinensis populations.

The effect of different chiral morphs on visitation rates and fruit set in the orchid Spiranthes spiralis

“…The twisting of the inflorescence probably reduces the number of successive probes within inflorescence and the time length of foraging path. A similar pattern was found in Spiranthes sinensis where a negative correlation between the size of helical angle between two successive flowers and skip behaviour (number of skips of neighbouring flowers per visit) has been found and hypothesised as a potential mechanism for reducing geitonogamy (Iwata et al 2012). The probability of setting fruits for the different positions of flowers along the inflorescence suggests that frequency of pollinator probing differs between clockwise and anti-clockwise morphs, being shorter in the latter and, in particular, that the probability that a pollinator leaves the inflorescence (thus reducing the number of pollinated flowers) increases after the first 10 flowers (roughly corresponding to a first inflorescence turn).…”

“…However, many studies have highlighted how also the plant inflorescence is subject to strong pollinator-mediated selection as its shape strongly determines pollinator behaviour and duration of visits (Ohashi and Yahara 2001;Sletvold and Ågren 2010;Iwata et al 2012). Flower size and number, density of flowers on an inflorescence, three-dimensional arrangement of flowers on the inflorescence have all been found to be important for determining the attractiveness of individual plants, the movement of pollinators within the inflorescence and the overall mating success of the plant (Fishbein and Venable 1996;Harder et al 2004;Ishii et al 2008).…”

“…has flowers which are bilaterally symmetrical, but produces chiral inflorescences because the flowers coil around a central axis in a clockwise or anti-clockwise fashion, or, very rarely, uncoiled (Jacquemyn and Hutchings 2010;Iwata et al 2012). Often, chirality is a developmental consequence and stochastically determined.…”

The role of breeding system in community dynamics: Growth and mortality in forests of different successional stages

“…Ecological variables that are associated with resources available for pollinators (e.g., quantity of inflorescence) have a great impact on population structure through their effect on the pollinator behavior and plant mating (Case & Ashman, 2009; Gervasi & Schiestl, 2017; Iwata, Nagasaki, Ishii, & Ushimaru,2012). In addition, the sex ratio of species can vary considerably in response to tree size, density and stand age if the plants are growing in a stressful environment (Charlesworth, 2006; Lloyd & Bawa, 1984; Ortiz, Arista, & Talavera, 2002), which likely explains the frequency and role changing of hermaphrodite over succession.…”

The Floral Biology, Breeding System and Pollination Efficiency of Schima superba Gardn. et Champ. (Theaceae)

“…The reproductive success of plants is often limited by lack of pollination, mate availability and fecundity and mate limitation [3]. Flower arrangement and reward availability within plants are also important factors that influence mating success [4]. The timing of pollen presentation and stigma receptivity at both the individual and population levels may strongly correlate with mate availability, and species with long flowering periods may avoid pollination limitation and reproductive deficit as a consequence of an increased overlap with insect activity [5].…”