Reproductive resource partitioning in two sympatric Goniothalamus species (Annonaceae) from Borneo: floral biology, pollinator trapping and plant breeding system

Abstract

The floral phenology, pollination ecology and breeding systems of two sympatric early-divergent angiosperms, Goniothalamus tapisoides and G. suaveolens (Annonaceae) are compared. The flowers are protogynous and morphologically similar, with anthesis over 23–25 h. Both species are predominantly xenogamous and pollinated by small beetles: G. tapisoides mainly by Curculionidae and G. suaveolens mainly by Nitidulidae. Coevolution and reproductive resource partitioning, reducing interspecific pollen transfer, is achieved by temporal isolation, due to contrasting floral phenologies; and ethological isolation, due to contrasting floral scents that contain attractants specific to the two beetle families. Analysis of floral scents revealed three volatiles (3-methylbutyl acetate, ethyl hexanoate and 2-phenylethanol) that are known to be nitidulid attractants in the floral scent of G. suaveolens, but absent from that of G. tapisoides. An effective pollinator trapping mechanism is demonstrated for both species, representing the first such report for the family. Trapping is achieved by the compression of the outer petals against the apertures between the inner petals. This trapping mechanism is likely to be a key evolutionary innovation for Goniothalamus, increasing pollination efficiency by increasing pollen loading on beetles during the staminate phase, promoting effective interfloral pollinator movements, and increasing seed-set by enabling rapid turn-over of flowers.

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).…”

“…Annonaceae species with abbreviated anthesis often display pistillate/staminate-phase floral synchrony, in which pistillate-phase and staminate-phase flowers are not borne concurrently on an individual, thereby minimizing opportunities for geitonogamy [22,23,24,44]. Lau et al [23] hypothesized that shortening of anthesis in species with this type of floral synchrony reduces the proportion of non-flowering days and hence increases seedset. Abbreviated anthesis and pistillate/staminate-phase floral synchrony might therefore be prerequisites for circadian pollinator trapping.…”

“…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.…”

Stigmatic exudate in the Annonaceae: Pollinator reward, pollen germination medium or extragynoecial compitum?

“…Goniothalamus tapisoides is pollinated by small curculionid beetles and is predominantly xenogamous (Lau et al ). The flowers are protogynous, with anthesis extending over c. 23 h, from the early morning (c. 06:00 hours) of the first day of anthesis until early morning (c. 05:00 hours) the next day, and with the pistillate phase (c. 13 h duration) followed by a non‐sexual interim phase (c. 3 h) prior to the onset of the staminate phase (c. 7 h) (Lau et al ). Corresponding phenological data is not available for G. parallelivenius , although field observations indicate that it is also protogynous and pollinated by small beetles (J.Y.Y.…”