Beetle pollination and flowering rhythm of Annona coriacea Mart. (Annonaceae) in Brazilian cerrado: Behavioral features of its principal pollinators

Abstract

The conservation and sustainable management of Annona coriacea requires knowledge of its floral and reproductive biology, and of its main pollinators and their life cycles. In this work, we analyzed these aspects in detail. Floral biology was assessed by observing flowers from the beginning of anthesis to senescence. The visiting hours and behavior of floral visitors in the floral chamber were recorded, as were the sites of oviposition. Excavations were undertaken around specimens of A. coriacea to determine the location of immature pollinators. Anthesis was nocturnal, starting at sunset, and lasted for 52–56 h. The flowers were bisexual, protogynous and emitted a strong scent similar to the plant´s own ripe fruit. There was pronounced synchrony among all floral events (the period and duration of stigmatic receptivity, release of odor, pollen release and drooping flowers) in different individuals, but no synchrony in the same individuals. All of the flowers monitored were visited by beetle species of the genera Cyclocephala and Arriguttia. Beetles arrived at the flowers with their bodies covered in pollen and these pollen grains were transferred to the stigmata while foraging on nutritious tissues at the base of the petals. With dehiscence of the stamens and retention within the floral chamber, the bodies of the floral visitors were again covered with pollen which they carried to newly opened flowers, thus promoting the cycle of pollination. After leaving the flowers, female beetles often excavated holes in the soil to lay eggs. Larvae were found between the leaf litter and the first layer of soil under specimens of A. coriacea. Cyclocephala beetles were the main pollinators of A. coriacea, but Arriguttia brevissima was also considered a pollinator and is the first species of this genus to be observed in Annonaceae flowers. Annona coriacea was found to be self-compatible with a low reproductive efficiency in the area studied. The results of this investigation provide ecological data that should contribute to the conservation and economic exploitation of A. coriacea.

Synopsis of the cyclocephaline scarab beetles (Coleoptera, Scarabaeidae, Dynastinae)

“…Cyclocephala cribrata Burmeister larvae reportedly eat the roots of bromeliads in Brazil (Luederwaldt 1926). Cyclocephala atricapilla Mannerheim adults and larvae were found beneath litter near their Annona host plants, and the larvae were observed feeding on decaying material (Costa et al 2017). …”

“…Cyclocephaline scarab beetles have been observed to mate within the inflorescences or flowers of many families: 1) Nymphaeaceae (Prance and Arias 1975; Hirthe and Porembski 2003); 2) Annonaceae (Gottsberger 1990, Murray 1993, Costa et al 2017); 3) Magnoliaceae (Gibbs et al 1977, Dieringer and Espinosa 1994, Dieringer et al 1999); 4) Cyclanthaceae (Beach 1982); 5) Araceae (Young 1986, 1988a, b, Maia and Schlindwein 2006, Grimm 2009, Seymour et al 2009, Moore 2012); 5) Arecaceae (Beach 1984, Rickson et al 1990, Voeks 2002); 6) Solanaceae (Ratcliffe and Cave 2017); and possibly 7) Cactaceae (B. Schlumpberger in litt . 2011).…”

“…Floral food rewards for these scarab beetles are diverse and include sterile staminate or staminode tissue (Prance 1976, 1980, Young 1986, Maia et al 2010, Maldonado et al 2015), carpellary appendages (Prance and Arias 1975, Hirthe and Porembski 2003), stamens (Dieringer and Espinosa 1994, Hirthe and Porembski 2003, Costa et al 2017), petal tissue (Gibbs et al 1977, Gottsberger 1989, Dieringer and Espinosa 1994, Dieringer et al 1999, Voeks 1992), specialized adaxial food tissue of bracts (Beach 1982), and pollen (Rickson et al 1990). Cyclocephala amazona was observed consuming epidermal trichomes from the stalk of Bactris gasipaes Kunth (Arecaceae) inflorescences before feeding on pollen (Rickson et al 1990).…”

“…Detailed studies on Dieffenbachia Schott (Araceae) indicate that among a group of cyclocephaline floral visitors, some species are relatively more effective pollinators (Young 1988a). Seasonal abundance of cyclocephalines at a specific locality, along with floral phenology, may also determine which species are primary or secondary pollinators (Maia et al 2010, Costa et al 2017). …”

“…In Brazilian cerrado habitat, A. brevissima are floral visitors of Annona coriacea Mart. and are likely late-season, secondary pollinators of this species (Costa et al 2017). Specimens of A. brevissima have been collected at lights at night (Martínez 1968a).…”