Time-Dependent Trapping of Pollinators Driven by the Alignment of Floral Phenology with Insect Circadian Rhythms

Abstract

Several evolutionary lineages in the early divergent angiosperm family Annonaceae possess flowers with a distinctive pollinator trapping mechanism, in which floral phenological events are very precisely timed in relation with pollinator activity patterns. This contrasts with previously described angiosperm pollinator traps, which predominantly function as pitfall traps. We assess the circadian rhythms of pollinators independently of their interactions with flowers, and correlate these data with detailed assessments of floral phenology. We reveal a close temporal alignment between patterns of pollinator activity and the floral phenology driving the trapping mechanism (termed ‘circadian trapping’ here). Non-trapping species with anthesis of standard duration (c. 48 h) cannot be pollinated effectively by pollinators with a morning-unimodal activity pattern; non-trapping species with abbreviated anthesis (23–27 h) face limitations in utilizing pollinators with a bimodal circadian activity; whereas species that trap pollinators (all with short anthesis) can utilize a broader range of potential pollinators, including those with both unimodal and bimodal circadian rhythms. In addition to broadening the range of potential pollinators based on their activity patterns, circadian trapping endows other selective advantages, including the possibility of an extended staminate phase to promote pollen deposition, and enhanced interfloral movement of pollinators. The relevance of the alignment of floral phenological changes with peaks in pollinator activity is furthermore evaluated for pitfall trap pollination systems.

Accelerated diversification correlated with functional traits shapes extant diversity of the early divergent angiosperm family Annonaceae

“…Although anthesis usually extends over 48 h in species of Annonaceae with hermaphroditic flowers [23,24], Artabotrys , Dasymaschalon , Friesodielsia , and Goniothalamus species, which all exhibit circadian trapping, also have an abbreviated anthesis of only 23–27 h [23,24,44]. A similarly brief anthesis ( c. 27 h) is reported for Desmos chinensis [22], although this species does not trap pollinators.…”

“…Most species of Annonaceae possess partially enclosed pollination chambers with apertures that remain open throughout anthesis, enabling pollinators to enter or leave the flowers freely during any phenological stage [20]. Tightly enclosed floral chambers that trap pollinators are rare in the family, but are reported in Dasymaschalon , Friesodielsia , Goniothalamus , and possibly also Artabotrys [23,24,44] (Supplementary Fig. S4B).…”

“…S4B). The opening and closing of the floral chambers are precisely aligned with the endogenous periodicities of the pollinating beetles: opening of the flowers coincides with an activity peak, but the floral chamber closes before the beetles enter their next circadian peak [24] (Fig. 6A, B).…”

“…6A, B). This timing broadens the range of potential pollinators to include those with circadian rhythms that are both unimodal (with a single daily activity peak) and bimodal (with twice-daily peaks) [24]. Circadian trapping also endows other selective advantages, including the possibility of an extended staminate phase to promote pollen deposition and enhanced inter-floral movement of pollinators.…”

“…DNA sequences of nearly 1,000 species have been generated, enabling a good understanding of phylogenetic relationships and generic delimitation in the family. Considerable progress has also been made in understanding the distribution of morphological characters across the family and their possible roles in diversification, especially floral and fruit traits of ecological importance such as floral chambers [20], the role of stigmatic exudate as an extragynoecial compitum [21], staminate/pistillate-phase floral synchrony [22], the circadian trapping of pollinators [23,24], and seed dispersal units (discussed below; [25]). These advances in both molecular and morphological data accumulation and new analytical methods provide excellent opportunities to use recent comprehensive phylogenies to date divergence times in the family and to study diversification patterns in relation to key functional traits.…”