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.
Highlights
Polyalthia suberosa was selected as an exemplar small-beetle pollinated Annonaceae species exhibiting a standard anthesis duration (c. 48 h)
The beetles subsequently remain relatively immobile in the flower until their activity peak the following morning (06:00–09:00 h of Day 2); this coincides with the end of the pistillate phase, at which point the dissipation of floral scent encourages pollinator departure
A new cohort of beetles is attracted during their activity peak, which coincides with the onset of the staminate phase when the flowers again emit a scent
Summary
Pollinator traps—defined as structures of a flower or inflorescence that prevent floral visitors from leaving until pollination has been achieved (Kugler, 1955)—have evolved independently in numerous angiosperm lineages, including basal angiosperms (Bolin et al, 2009; Oelschlägel et al, 2009), monocots (Vogel and Martens, 2000; Singer, 2002) and eudicots (Masinde, 2004; Heiduk et al, 2010). Most function as pitfall traps, in which floral visitors (generally insects) enter or fall into the flower or inflorescence and are trapped, often due to specialized trichomes and slippery surfaces that lack anchor points (Cammerloher, 1923, 1933; Daumann, 1971; Lack and Diaz, 1991; Vogel and Martens, 2000; Singer, 2002; Bolin et al, 2009; Oelschlägel et al, 2009; Heiduk et al, 2010), a more complex trap mechanism operates in some sexually. Petals in Dasymaschalon are inferred to be homologous with the outer petals of other Annonaceae (Saunders, 2010), they are apically connivent and morphologically similar to the inner petals of the sister genus Friesodielsia; trapping operates by lateral petal expansion that closes the apertures between contiguous petals (Pang and Saunders, 2014)
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