Sexual dimorphism in floral scents of the neotropical orchid Catasetum arietinum and its possible ecological and evolutionary significance

Abstract

Dioecy in angiosperms is often associated with sexual dimorphism in floral traits other than the sexual organs. Species of the neotropical orchid genus Catasetum produce unisexual flowers characterized by a remarkable morphological sexual dimorphism. Catasetum species emit strong floral perfumes that act as both signal and reward for male euglossine bee pollinators. Although the role of floral perfumes of Catasetum in attracting euglossine pollinators is well investigated, little is known about whether perfumes differ between floral sexes and, if they do, whether this chemical dimorphism influences the pollination ecology of the plants. Taking Catasetum arietinum as a model species, our aim was to observe the behaviour of pollinators on male and female flowers and to compare scent properties (i.e. chemical composition, total amount and temporal fluctuation) of male and female flowers. Floral scent samples were collected by using dynamic headspace methods and were analysed via gas chromatography coupled with mass spectroscopy (GC-MS). Catasetum arietinum is pollinated by males of two Euglossa species (i.e. E. nanomelanotricha and E. securigera). Bees approached male and female inflorescences of C. arietinum in similar proportions but landed significantly more often and spent more time on female flowers, which emitted more scent than male flowers. Furthermore, the amount of scent emitted varied across the different times of sampling, corresponding to the pattern of the diel foraging activity of pollinating bees on male and female flowers. The chemical composition of scents differed significantly between sexes. The two major compounds (Z)-methyl-p-methoxycinnamate and (E)-geranyl geraniol contributed most to this difference. This is the first case of sexual dimorphism reported in orchid floral perfumes. We discuss the influence of sex-specific floral scents on the behaviour of euglossine pollinators and offer new insights into the ecological and evolutionary significance of divergence in floral scents among dioecious plants.

Reproductive Ecology of Euglossine Bee-pollinated Orchid Catasetum Integerrimum Hook (Ochidaceae)

“…Whilst, the forced launching of pollinaria towards bees during its oral visitation contributed to explain the early departure and low visitation frequency of bees to staminate plants. The aversive behavior of bees caused by the forced attachment of pollinaria is coincident with the reported for several Catasetum species (Janzen 1981;Romero and Nelson 1986;Milet-Pinheiro et al 2015;Nunes et al 2017;Brandt et al 2020).…”

“…Hence, highly specialized pollination systems may be less prone to pollen limitation in presence of suitable pollinators (Romero and Nelson 1986;Tremblay 1992). Despite specialized pollination in Catasetum, several studies have documented a low fruit set under natural pollination regime (Janzen 1981;Milet-Pinheiro et al 2015;Brandt et al 2020).…”

Unraveling the Olfactory Biases of Male Euglossine Bees: Species-Specific Antennal Responses and Their Evolutionary Significance for Perfume Flowers

“…In agreement to these patterns, the chemical composition of floral scents of perfume-rewarding orchids has been shown to differ among Euglossa-and Eulaema-pollinated species. Several chemical compounds which seem to be typically found in the floral scent bouquets of either Euglossa-(i.e., ipsdienol and myrcene; Milet-Pinheiro and Gerlach, 2017;Brandt et al, 2020) or Eulaema-pollinated species (e.g., α-pinene and (−)-(E)-carvone epoxide; Whitten et al, 1986;Milet-Pinheiro and Gerlach, 2017) coincide with the compounds most responsible for the separation of antennal response profiles among tested euglossine genera in our study. Altogether, these findings underline the finding of Ramírez et al (2011) suggesting that distinct sensory biases between euglossine bee lineages have shaped the evolution of floral scents in perfume-rewarding plants.…”

Pollination of the strongly scented Sarcoglottis acaulis (Orchidaceae) by male orchid bees: nectar as resource instead of perfume

“…2015; Brandt et al . 2020). By synchronizing the emission of scent with periods of higher pollinator activity (and reducing the emission during their low‐activity periods), the high energetic costs associated with scent production can be minimized.…”