Morphological and functional flower characteristics of New and Old World Annonaceae with respect to their mode of pollination

Abstract

The Annonaceae show a broader flower biological radiation than originally thought, with flowers being pollinated not only by beetles, but also by thrips, flies and even bees. The majority of species have hermaphroditic protogynous flowers. Species with white or yellowish‐white, small, delicate, day‐active flowers, may be pollinated either solely by thrips, or by thrips and small beetles (e.g., species of Bocageopsis, Oxandra, Xylopia). Several of these thrips‐pollinated species have stamens with an elongated, tongue‐like connective. Pollination by flies is not well documented for American species, notwithstanding it appears to be more common in Old World species, e.g., in the genus Pseuduvaria. The mitriform flowers exhale an unpleasant smell, produce nectar in purple‐colored petal glands and have a sapromyiophilous syndrome. Flies enter the flower center through large openings between the inner petals. Beetle‐pollinated Annonaceae have flowers with comparatively thick and, often, fleshy petals, which, during anthesis frequently form a pollination chamber with the petals inclining over the flower center. The stamens usually have peltate connective shields, probably a device for protection against voracious beetles. Some cantharophilous species have flowers which are day‐active while others are night‐active. When they are in their pistillate phase, the beetles are attracted by characteristic odor components. They enter the pollination chamber and usually remain in the interior of the flower until the flower has changed to its staminate phase, when pollen is shed and afterwards petals and stamens detach. Two lines of cantharophilous Annonaceae are recognizable on the basis of present knowledge. Species with smaller and more delicate flowers are pollinated by small beetles (Nitidulidae, Curculionidae, Chrysomelidae and Staphylinidae), whereas species with large, more robust flowers in the Neotropics are pollinated by large beetles of the family Scarabaeidae, subfamily Dynastinae. Some species of the cantharophilous Annonaceae, especially the large‐flowered ones, but also some species with smaller flowers, produce heat during anthesis (thermogenesis). Food bodies, developed on the adaxial surfaces or sides of the petals, provide unique nourishment possibilities for beetles when they stay inside the flowers during the pistillate phase. In the staminate stage of the flower, after pollen is shed, beetles also feed on pollen. Apparently, no dynastid‐flower relationship has evolved in Asia and Australia. Pollination by bees was discovered recently in Unonopsis guatterioides in Amazonia and Uvaria concava in North Queensland: the first by scent‐collecting euglossine males and the second by pollen‐collecting Meliponinae. The general trends in morphological/functional floral characteristics in the family are discussed in a presumptive phylogenetic context.

First records of flower biology and pollination in African Annonaceae: Isolona, Piptostigma, Uvariodendron, Monodora and Uvariopsis

“…Another difference exhibited by the Uvariodendron species is their nocturnal anthesis and their warming-up (thermogenesis) of flowers during the evening and night hours. Similar phenomena occur in nocturnal dynastid-scarab-pollinated Annonaceae in the Neotropics (Gottsberger, 1989;Silberbauer-Gottsberger et al, 2003;Webber, 1996). In the New World Annonaceae pollinated by species of Cyclocephala and species of other genera of the Dynastinae (Scarabaeidae), temperature elevation above the surrounding air temperature usually is much higher than in Uvariodendron, reaching 10 • C or more as compared to 1-3 • C in Uvariodendron.…”

“…The petals of some Australian Annonaceae species, viz. in Goniothalamus or Haplostichanthus (Silberbauer- Gottsberger et al, 2003) are also connivent, but their petals are smaller at the base and so openings are left for pollinators to enter. In both cases the pollinators are well protected in the flowers' interior.…”

“…Staphylinidae beetles enter the pollination chamber formed by the elongated inner petals the morning of the first day of anthesis on and remain inside the pollination chamber until the end of the male stage in the morning of the second or third day of anthesis. Such a 2-day flower rhythm in which beetles remain inside the flower center during the whole anthesis is the most commonly observed floral rhythm in New World and Old World Annonaceae (Gottsberger, 1999;Ratnayake et al, 2006aRatnayake et al, , 2007Silberbauer-Gottsberger et al, 2003). Beetles that enter a flower during the female stage are perfect pollinators when carrying pollen because pollen is easily transferred to the sticky stigmatic exudates.…”

“…Studies during the last decades on New and Old World representatives of this group revealed, however, that they are unexpectedly more diversified with regard to pollination. Besides pollination by beetles (cantharophily), which is indeed the predominant mode of the majority of species worldwide, there is also pollination by thrips (Thysanoptera), flies (myiophily and sapromyiophily), cockroaches and even bees (melittophily) -for reviews see Gottsberger (1989Gottsberger ( , 1999, Webber and Gottsberger (1995), Silberbauer-Gottsberger et al (2003), Teichert et al (2009), Saunders (2010). Thus, a more differentiated picture of pollination modes in the Annonaceae has become apparent, revealing distinct adaptations of flowers to their particular flower-visiting insect group.…”

“…Thus, particular floral features, as well as color, scent or thermogenesis (warming during anthesis) of floral organs and the duration of anthesis are expressions of pollination events and a particular flower biology. Co-evolution with different insect groups has influenced and shaped the Annonaceae flower and accompanied the diversification of species and genera of this old angiosperm lineage (Gottsberger, 1999;Silberbauer-Gottsberger et al, 2003).…”