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

Sophie Petit,Russell Schumann,Annette T Scanlon,Alivereti Naikatini,Tara Pukala,Renee M Borges

doi:10.1371/journal.pone.0262985

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.

Highlights

Chiropterophilous plants attract bat visitors with specialized traits such as bell-shaped flowers that facilitate acoustic detection [1], scent [2], UV reflectance [3], and abundant floral nectar [4]
Obligate corolla removal by bats for pollination of some Dilleniaceae chiropterophily, lists a series of flower characteristics that prevail in this syndrome: nocturnal anthesis and nectar secretion, flowers lasting one night on plants with long flowering times, large container-shaped flowers, flowers away from leaves, thick corolla wall, pale colours, strong scents, numerous stamens rich in pollen, large nectar volumes, large space between nectar and stigmas and anthers
Known to produce nectarless flowers [7, 8], the family Dilleniaceae with ~ 500 mostly pantropical species [9] contains the genus Dillenia, whose large and stout flowers are assumed to be pollinated principally by bees [10], yet have many of the characteristics highlighted by Willmer for bat flowers [5]

Summary

Introduction

Chiropterophilous plants attract bat visitors with specialized traits such as bell-shaped flowers that facilitate acoustic detection [1], scent [2], UV reflectance [3], and abundant floral nectar [4]. Obligate corolla removal by bats for pollination of some Dilleniaceae chiropterophily, lists a series of flower characteristics that prevail in this syndrome: nocturnal anthesis and nectar secretion, flowers lasting one night on plants with long flowering times, large container-shaped flowers (some brushes), flowers away from leaves, thick corolla wall, pale colours, strong scents, numerous stamens rich in pollen, large nectar volumes, large space between nectar and stigmas and anthers. Known to produce nectarless flowers [7, 8], the family Dilleniaceae with ~ 500 mostly pantropical species [9] contains the genus Dillenia, whose large and stout flowers are assumed to be pollinated principally by bees [10], yet have many of the characteristics highlighted by Willmer for bat flowers [5]. Conservation International [12] chose D. biflora as one of the key native species to use in reforestation in northern Viti Levu, Fiji. Its fruits and seeds are likely consumed by both birds and bats

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