Crane flies and microlepidoptera also function as pollinators in Epidendrum (Orchidaceae: Laeliinae): the reproductive biology of E. avicula

Abstract

Crane flies and microlepidoptera have been recorded as pollinators in unrelated orchid groups, but these insects have never been recorded in Epidendroideae, the most species‐rich orchid subfamily, which includes one of the most diverse genera among Orchidaceae, Epidendrum. Based on data on phenology, floral morpho‐anatomy, pollinators, pollination mechanisms and breeding system, the reproductive biology of E. avicula was studied in south‐eastern Brazil. Epidendrum avicula possess osmophores that produce a citric fragrance at night. The flowers attract Tipulidae flies and several families of microlepidoptera that drink the nectar produced in a tube formed by the adnation of the labellum and column. As is common in Epidendrum, after removing the pollinarium, both crane flies and micro‐moths get trapped by the proboscis, which frightens the insects and inhibits any possible intent to immediately visit another flower. The behavior of the pollinators on flowers, plus the retention of the anther cap by the pollinarium, results in a reduction in the occurrence of geitonogamy. Because E. avicula is self‐incompatible, the consequence of pollinator behavior and the floral mechanisms tend to reduce the pollen loss. As far as we know, this is the first study to report the reproductive biology of a species of Epidendroideae pollinated by crane flies and microlepidoptera. Based on more recent concepts of plant–pollinator interactions, although E. avicula is pollinated by several species belonging to two distinct orders, suggesting an unspecialized pollination system is involved, nectar‐seeking microlepidoptera and Tipulidae flies can be recognized as a single functional group.

Nectar-Secreting and Nectarless Epidendrum: Structure of the Inner Floral Spur

“…It is distributed from the southeastern United States of America to northern Argentina ( Hágsater and Soto-Arenas, 2005 ). It comprises both food-rewarding and food-deceptive species ( Pansarin, 2003 ; Pansarin and Amaral, 2008b ; Pansarin and Pansarin, 2014 , 2017 ). Although its flowers are visited by a wide range of pollinators, moths and butterflies are the most frequently recorded, and according to Pinheiro and Cozzolino (2013) , this kind of specialization (together with certain novel vegetative characters) may represent key innovations that led to the enormous degree of speciation found in this genus.…”

“…Orange-red or yellow flowers are attributed to butterfly-pollinated species, whereas whitish to pale green, highly fragrant flowers are predominantly moth-pollinated ( van der Pijl and Dodson, 1969 ; van der Cingel, 2001 ). In some moth-pollinated species, scent is produced by osmophores ( Pansarin and Pansarin, 2017 ). Epidendrum densiflorum (= E. paniculatum ) is pollinated by both butterflies and Arctiidae moths ( Pansarin, 2003 ), whereas E. avicula , is pollinated by several species of micro-moths, as well as Tipulidae or crane flies ( Pansarin and Pansarin, 2017 ).…”

“…In some moth-pollinated species, scent is produced by osmophores ( Pansarin and Pansarin, 2017 ). Epidendrum densiflorum (= E. paniculatum ) is pollinated by both butterflies and Arctiidae moths ( Pansarin, 2003 ), whereas E. avicula , is pollinated by several species of micro-moths, as well as Tipulidae or crane flies ( Pansarin and Pansarin, 2017 ). In fact, many Epidendrum species have a long cuniculus and are thus adapted for pollination by Lepidoptera ( Pansarin, 2003 ; Pansarin and Amaral, 2008b ; Fuhro et al, 2010 ; Pansarin and Pansarin, 2017 ).…”

“…Epidendrum densiflorum (= E. paniculatum ) is pollinated by both butterflies and Arctiidae moths ( Pansarin, 2003 ), whereas E. avicula , is pollinated by several species of micro-moths, as well as Tipulidae or crane flies ( Pansarin and Pansarin, 2017 ). In fact, many Epidendrum species have a long cuniculus and are thus adapted for pollination by Lepidoptera ( Pansarin, 2003 ; Pansarin and Amaral, 2008b ; Fuhro et al, 2010 ; Pansarin and Pansarin, 2017 ). Conversely, although other members of Laeliinae have also long been considered to possess a cuniculus (e.g., Dressler, 1993 ), some taxa, such as Amblostoma and Lanium , both currently included in Epidendrum sensu lato , lack this character ( Pansarin and Pansarin, 2014 , 2017 ).…”

“…In fact, many Epidendrum species have a long cuniculus and are thus adapted for pollination by Lepidoptera ( Pansarin, 2003 ; Pansarin and Amaral, 2008b ; Fuhro et al, 2010 ; Pansarin and Pansarin, 2017 ). Conversely, although other members of Laeliinae have also long been considered to possess a cuniculus (e.g., Dressler, 1993 ), some taxa, such as Amblostoma and Lanium , both currently included in Epidendrum sensu lato , lack this character ( Pansarin and Pansarin, 2014 , 2017 ). Study of the reproductive biology of E. tridactylum , a member of the Amblostoma group, demonstrated that this species produces fragrant and rewardless flowers, and attracts dipterans that drink the extra-floral nectar produced at the base of the floral bracts ( Pansarin and Pansarin, 2014 ).…”