A novel bat pollination system involving obligate flower corolla removal has implications for global Dillenia conservation

Abstract

The Dilleniaceae is known to produce nectarless flowers pollinated by bees, but the fact that bats ingest Dillenia biflora pollen led us to question pollination assumptions for these trees. We aimed to identify the pollinators of D. biflora, check for nectar presence, and investigate potential for cleistogamy and global prevalence of this pollination system. We examined aspects of the pollination of D. biflora on two Fijian islands using video recordings, direct observations, hand pollination, measurements (flowers, bite marks, nectar), and monitoring. The flowers, receptive for one night, contained copious nectar and had permanently closed globose corollas that required removal by bats for pollination. All the 101 flowers that retained their corolla died and did not produce seeds by cleistogamy. The bat Notopteris macdonaldi was well adapted to corolla removal. Keeping corollas closed until bats manipulate the nectar-rich flowers is a beneficial strategy in high-rainfall environments with many flower parasites. We propose to name a pollination system reliant exclusively on bats “chiropteropisteusis.” From clues in the literature, other species in the geographical range of Dillenia are probably chiropteropisunous. Chiropteropisteusis should be investigated in the Old-World range of Dillenia, many species of which are threatened. The remarkable “fall” of the entire corolla observed by an earlier botanist for several species in the genus is most likely attributable to bats. This discovery has important implications for the conservation of bat-dependent trees and their associated fauna, particularly considering the high level of threat faced by flying-foxes globally.

Dillenia (Dilleniaceae) pollen heteromorphy and presentation, and implications for pollination by bats

“…The feeding behaviour of bats at D. biflora presented in Petit et al. (2022, 2021), which involves perching and approaching the flower from the top with the tip of the muzzle, is obviously compatible with pollen dispensing via apical pores.…”

“…The non‐seasonal cream to yellow and pink flowers have permanently closed globose corollas (16–20 mm measurements on average; Figure 1) that must be removed by bats with their teeth for pollination to take place. They contain nectar and some are lightly scented (Petit et al., 2022). Seeds are available for dispersal when the sepals curve back as the fruit opens upon maturity (Smith, 1981).…”

“…For example, perching bats are more effective pollinators than are hovering bats in the New World palm Calyptrogyne ghiesbreghtiana (Tschapka, 2003). The feeding behaviour of bats at D. biflora presented in Petit et al (2022Petit et al ( , 2021, which involves perching and approaching the flower from the top with the tip of the muzzle, is obviously compatible with pollen dispensing via apical pores.…”

“…Conservation of chiropteropisunous (bat-dependent) species is concerning considering the high level of threat facing island bats (Vincenot et al, 2017), including in Fiji, where D. biflora occurs, and where cave-dwelling blossom bat pollinators (Notopteris macdonaldi) are disturbed and hunted (Scanlon, Petit, & Bottroff, 2014). Several potential Dillenia bat pollinators identified by Petit et al (2022) have declining populations. The dependence of bats on Dillenia spp.…”

“…Several potential Dillenia bat pollinators identified by Petit et al. (2022) have declining populations. The dependence of bats on Dillenia spp.…”