Mammal pollinators lured by the scent of a parasitic plant

Abstract

To communicate with animals, plants use signals that are distinct from their surroundings. Animals generally learn to use these signals through associative conditioning; however, signals are most effective when they elicit innate behavioural responses. Many plant species have flowers specialized for pollination by ground-dwelling mammals, but the signals used to attract these pollinators have not been elucidated. Here, we demonstrate the chemical basis for attraction of mammal pollinators to flowers of the dioecious parasitic plant Cytinus visseri (Cytinaceae). Two aliphatic ketones dominate the scent of this species; 3-hexanone, which elicits strong innate attraction in rodents, and 1-hexen-3-one, which repels them in isolation, but not in combination with 3-hexanone. The aliphatic ketone-dominated scent of C. visseri contrasts with those of insect-pollinated plants, which are typically dominated by terpenoids, aromatic or non-ketone aliphatic compounds. 3-hexanone is also known from some bat-pollinated species, suggesting independent evolution of plant signals in derived, highly specialized mammal-pollination systems.

Figure 1.

Habitat, morphology and pollinators of C. visseri. (a) Habitat on the summit of the Long Tom Pass, South Africa. (b) Male inflorescence. scale bar, 10 mm. (c) Cross section of male flower. A = androecium, N = nectar chamber. Scale bar, 5 mm. (d) Cross section of female flower. S = stigma. Scale bar, 5 mm. (e) A short-snouted elephant shrew E. brachyrhynchus feeding on nectar in C. visseri flowers. The tongue entering the flower is visible below the snout. Scale bar, 10 mm. (f) A striped field mouse R. pumilio feeding on nectar in male C. visseri flowers. Scale bar, 10 mm.

Figure 2.

Major volatile compounds, arranged according to biosynthetic origins, present in the scents of female and male C. visseri flowers and their nectar. Bars represent mean (± s.e.) percentages. A detailed list of compounds is given in electronic supplementary material, table S3. Black bars, nectar; grey bars, whole flower.

Figure 3.

Mean (±95% CI) behaviour of striped field mice (R. pumilio) during choice trials involving the dominant volatile compounds in the scent of C. visseri flowers, 1-hexen-3-one and 3-hexanone, and a mixture of both compounds. (a) Proportions of trials during which mice entered a y-maze olfactometer from a holding tank. (b) Proportions of trials during which mice chose the scented arm of the y-maze olfactometer, rather than the unscented arm. (c) The latency period before mice made a choice. Statistics are back-transformations of least-squares means from two-factor repeated-measures analyses, hence the asymmetrical confidence intervals. White circles, females; grey circles, males.