Pollination of Trichosalpinx (Orchidaceae: Pleurothallidinae) by biting midges (Diptera: Ceratopogonidae)

Abstract

Pleurothallidinae (Epidendreae) are a megadiverse Neotropical orchid subtribe comprising > 5100 species, most of which are probably pollinated by Diptera. The role of pollinators as drivers of species diversity is largely unknown because knowledge of pollination systems in Pleurothallidinae is still scarce. Here, we addressed the pollination of Trichosalpinx s.s. through study of floral anatomy, pollinator behaviour and floral traits shared with other angiosperms to elucidate its pollination mechanisms. We identified midge specimens with DNA barcoding and morphology, documented pollination with video recordings, studied the anatomy of flowers by combining microscopy (light microscopy, scanning electron microscopy and transmission electron microscopy) and histochemistry and analysed floral scents with gas chromatography-mass spectrometry. We found that two Trichosalpinx spp. are pollinated exclusively by female biting midges of a Forcipomyia (Euprojoannisia) sp. (Ceratopogonidae). The midges land on the motile lip and appear to suck substances from its papillose surface. We detected secretion of carbohydrates and proteins on the lip and sepals, and thus, Trichosalpinx might stimulate a protein collection instinct in female biting midges. The well-developed mandibles and poorly developed laciniae of the pollinators indicate that they mainly feed on invertebrate hosts from which they draw haemolymph. Thus, Trichosalpinx flowers offer small quantities of proteins and carbohydrates that may act as flavour teases and together with the colour, fragrances, trichomes and movement of the lip, they probably form part of a complex deceptive system. Some other angiosperms that are also pollinated by biting midges possess similar dark purple flowers with ciliate ornamentation and use myophily, sapromyophily or kleptomyiophily as strategies to exploit different families of Diptera as pollinators. One Forcipomyia sp. (Euprojoannisia) is kleptoparasitic, suggesting that kleptomyiophily may have evolved in Trichosalpinx. The similar floral morphology among members of Trichosalpinx and some species of the closely related genera Anathallis and Lankesteriana suggests that they are also pollinated by biting midges.

Orchid conservation: how can we meet the challenges in the twenty-first century?

“…Recent papers have investigated birds (e.g. Micheneau et al 2006 ; van der Niet et al 2015 ), crickets (Micheneau et al 2010 ), fungus gnats (Phillips et al 2014 ) and biting midges (Bogarín et al 2018 ) as specialized pollinators. Many orchid species attract pollinators by deceipt, with the forms of deception including food deception, brood-site imitation, shelter imitation, rendezvous attraction and sexual deception (Jersáková et al 2006 ), and recent discoveries of dual deceipt (pseudopollen lacking food value; Davies et al 2013 ), carrion mimicry (van der Niet et al 2011 ) and production of fruitfly aggregation pheromones (Karremans et al 2015 ) demonstrate that we are far from understanding the full complexities of orchid pollination.…”

A new species of Pleurothallis (Orchidaceae: Pleurothallidinae) in subsection Macrophyllae-Fasciculatae with a unique, highly reduced, morphologically distinct labellum

“…(Borba & Semir 2001); Andinia (Luer) Luer (Álvarez 2011); Dracula Luer (Endara et al 2010, Policha et al 2016; Lepanthes Sw. (Blanco & Barboza 2005, Blanco & Vieira 2011, Calderón-Sáenz 2012; Restrepia Kunth (Millner & Baldwin 2016); Specklinia Lindl. (Karremans et al 2015); and Trichosalpinx Luer (Bogarín et al 2018). In comparison to these other Pleurothallidinae much less is known about pollination strategies in Pleurothallis, with only a few careful studies having been published (Calderón-Sáenz 2011, Damon & Salas-Roblero 2007, Díaz-Morales & Karremans 2015, Duque-Buitrago et al 2014 and only one of these being of a species in subsection Macrophyllae-Fasciculatae (Duque-Buitrago et al 2014).…”

Don’t forget the flies: dipteran diversity and its consequences for floral ecology and evolution

“…The convergent evolution of a volatile-mediated kettle trap in chloropid-pollinated Ceropegia dolichophylla (Apocynaceae; Heiduk et al 2015) suggests that an important pollination niche has been overlooked. Bogarín et al (2018) describe a similar case of convergent evolution for pollination by biting midges (Ceratopogonidae), including species of Trichosalpinx and Bulbophyllum orchids, different species of Aristolochia and Ceropegia, as well as Theobroma cacao (Malvaceae), the natural source of chocolate. In this case, attraction of female flies appears to involve the provision of small amounts of floral protein, dark, hirsute floral structures and cuticular chemistry recalling animal skin or sebaceous gland secretions.…”