Functional floral traits and the evolution of pollination systems in Annonaceae : reproductive resource partitioning, pollinator trapping and stigmatic exudate

Abstract

A detailed study of functional floral traits and the evolution of pollination systems in the early divergent angiosperm family Annonaceae is conducted. The study focuses on nine species, viz. Dasymaschalon trichophorum, Desmos chinensis, Fissistigma oldhamii, Friesodielsia borneensis, Goniothalamus tapisoides, Goniothalamus suaveolens, Polyalthia suberosa, Uvaria grandiflora and Uvaria macrophylla in Brunei Darussalam, Singapore, Hainan, Guandong and Hong Kong.

Coevolution and reproductive resource partitioning in the sympatric species Goniothalamus tapisoides and G. suaveolens with overlapping flowering periods is shown to be achieved by temporal isolation (by varying floral phenologies) and ethological isolation (by differing floral scent attractants that are specific for different pollinators, viz. Curculionidae and Nitidulidae), thereby reducing interspecific pollen transfer. This represents the first study of this phenomenon in early divergent angiosperms.

A ‘circadian’ pollinator trapping mechanism is reported in Goniothalamus tapisoides and G. suaveolens, in contrast with ‘pitfall’ trapping, which is observed in other angiosperm families that trap pollinators. Pollinator trapping in Goniothalamus operates by the movement of the outer petals, which compress against the basal apertures located between the apically connivent inner petals. An extended flange on the inner petal ‘claws’, together with growth of the outer petals increase trapping efficiency in G. tapisoides. This mechanism is likely to be a key evolutionary innovation in this genus to enhance pollination efficiency.

This pollinator trapping mechanism, together with pollinator selection, is further demonstrated to be driven by the alignment of floral phenology and the circadian rhythms of the beetle pollinators, based on studies of several species in disparate genera in the family, viz. Desmos chinensis, Dasymaschalon trichophorum, Friesodielsia borneensis, Goniothalamus tapisoides and Polyalthia suberosa. I hypothesise that pollinator trapping in the Annonaceae may be advantageous for promoting pollination efficiency as it enhances pollen loading on the pollinator’s body due to the extended staminate floral phase, increases the turn-over rate of flowers and thus increases seedset, facilitates interfloral pollinator movement, and utilises a broader range of potential pollinators with contrasting circadian rhythms (bimodal, morning unimodal and evening unimodal activity patterns). This hypothesis is likely to be relevant to other angiosperms with ‘pitfall’ pollinator traps.

A detailed study of the role of stigmatic exudate in the Annonaceae is also undertaken. Sugar concentration of the exudate during the pistillate floral phase is shown to provide the optimal condition for pollen germination in Uvaria macrophylla. In addition to sucrose, the detection of the amino acids γ-aminobutyric acid (GABA) and arginine further support the hypothesised role of exudate for optimising pollen germination. The presence of sugars in the exudate of Uvaria grandiflora and U. macrophylla, together with many different essential amino acids, and other amino acids that are sugar-sensitive cell stimulants and/or have phagostimulatory effects for insect pollinators further suggests that stigmatic exudate may function as a nutritive reward to insect pollinators. The stigmatic exudate of Goniothalamus tapisoides and G. parallelivenius is furthermore demonstrated to function as an extragynoecial compitum, enabling intercarpellary growth of pollen tubes. This is hypothesised to be a key evolutionary innovation in apocarpous species, enhancing pollination efficiency and increasing seedset.