Bradysia sp. (Diptera: Sciaridae), a pollinator that can die in flowers of Ditassa banksii Schult. (Apocynaceae, Asclepiadoideae)

Bradysia sp. (Diptera: Sciaridae), um polinizador que pode morrer em flores de Ditassa banksii Schult. (Apocynaceae, Asclepiadoideae)

ABSTRACT

This is the first record of Bradysia sp. as a pollinator of Ditassa banksii Schult.. This fly usually becomes trapped in the flower and die, but it carries out the pollination too. It is common to find fragments of insects bodies or dead individuals trapped in flowers of Asclepiadoideae. However, this is the first report of Bradysia sp. inserting pollinia.

Keywords:
fly; pollination; pollinium

RESUMO

Este é o primeiro registro de Bradysia sp. como polinizador de Ditassa banksii Schult.. Este díptero geralmente fica preso nas flores e morre, mas também pode realizar a polinização. É comum, em flores de Asclepiadoideae, encontrar partes do corpo de insetos ou até indivíduos já mortos presos nas flores, entretanto, este é o primeiro registro de Bradysia sp. inserindo polínias.

Palavras-chave:
mosca; polínia; polinização

Introduction

The Asclepiadoideae (Apocynaceae) present peculiar flowers, with the five anthers fused around the gynoecium and the pollen transferred in pollinium, two per pollinarium. A narrow space called guide rail is formed between adjacent anthers; the pollinarium brought by the pollinator is inserted in there (Endress 1996). In general, the inner part of the guide rail is covered with nectariferous tissue and the nectar accumulates below of guide rail, inducing the insects to look for this place (Demarco 2017).

For an insect to remove a pollinarium from the flower it must be strong enough, otherwise, it may become trapped and will die or may lose part of the body to be free from the flower (Corry 1884). There are several records of insects parts, or individuals, trapped in flowers of Asclepiadoideae (Corry 1884, Pant et al. 1982) and eventually mutilated insects may themselves be pollinators (Morse 1981, Shuttleworth & Johnson 2009).

Flies with pollinaria attached to the mouthparts are commonly treated as pollinators of Asclepiadoideae (Medeiros et al. 2008, Nihei & Schwarz 2011). However, this evidence does not guarantee that these insects can properly insert pollinia in the guide rail, assuming that visitors who can withdraw and transport pollinaria may be able to deposit them, and thus pollinate the plant (Ollerton & Liede 1997).

Studying the floral biology of Ditassa banksii Schult., several flowers with trapped insects were observed. This work, therefore, aimed to verify which groups of insects were trapped in the guide rail.

Material and methods

The fieldwork was carried out in the restinga (sandbank coastal vegetation) of Environmental Protection Area of Maricá (22°96'46”S, 42°89'47”W), Rio de Janeiro State, Brazil. Ditassa banksii is a climbing plant generally supported on bushes and produces many flowers in umbelliform inflorescences. The flowers are white, laterally inclined or facedown. The corolla is subcampanulate to urceolate. The lobes remain erect during anthesis. The corona is double, with five external subulate white lobe longer than the five internal oval-lanceolate white lobes, they are basally connected to each other and cover part of the chamber entrance below the guide rail, where the pollinia are inserted by pollinators (figure 1a). The flowers measure in average 4.21 mm ± 0.39 (3.31-5.08 mm; n = 30) in length by 2.86 mm ± 0.72 (1.37-4.28 mm; n = 30) in width. They remain open 7-8 days, produce a honey smell and the nectar has an average sugar concentration of 21.8% ± 3.28 (16-23%, n = 6). In the same area, Musca domestica (Linnaeus, 1758) and another unidentified species of Diptera were also considered effective pollinators (Koschnitzke 2015). In November 2008, 68 flowers were collected and later, in the stereomicroscope, they were observed the insects trapped and dead in the guide rails.

Figure 1
Ditassa banksii L. a. Pollinarium inserted in the guide rail. b. Ant with one leg trapped and another with an attached pollinarium; c. Bradysia sp. trapped by legs and a pollinarium attached to the mouthparts. d. Bradysia sp. with the mouthparts trapped in guide rail, with the pollinarium inserted by him just below.

Results

Ants and flies were found dead in flowers of Ditassa banksii, trapped in guide rails or attached to the pollinaria, mainly by the mouthparts, but also by legs and antennas. An ant, caught by one of front legs, had two pollinaria attached to the other front leg (figure 1b).

Bradysia sp. was found dead in 76% of the collected flowers. Of these, four individuals had one to two pollinaria attached to the mouthparts and were trapped by legs in the guide rail (Figure 1c). It was also observed a pollinarium inserted in the guide rail just below an arrested individual of Bradysia sp. (figure 1d).

Discussion

The pollinarium inserted just below an arrested individual of Bradysia sp. indicate that the pollinarium was brought by that fly. Therefore, these flies, besides being able to remove pollinaria, may also carry out pollination, even though most of the time they become trapped and die by doing this.

In Asclepiadoideae, there is only one record of pollination by Sciaridae, genus Sciara Meigen, in Marsdenia cymulosa Benth in Australia (Forster 1992). According to the author, these insects were numerous and active, carrying pollinaria attached to the body moving to flowers of different plants, demonstrating that these small flies are capable of cross-pollinating.

Bradysia species are exclusive pollinators of two species of Orchidaceae, Lindellia crassifolia Lindl. (Barbosa et al. 2009) and Lepanthes glicensteinii Luer (Blanco & Barboza 2005). They are also pollinators of Pleurothallis marthae (Luer & Escobar) Luer, an Orchidaceae endemic to Colombia (Duque-Buitrago et al. 2014), and of Rheum nobile Hook.f. & Thomson (Polygonaceae) (Song et al. 2013).

The floral complexity of Asclepiadoideae is often interpreted as a highly specialized pollinating system, but in fact their flowers are functionally but not ecologically specialized (Wolff et al. 2008); that is, only a few insects can pollinate them, but the nectar can be easily accessed by numerous other insects with short mouthparts. The pollination system of asclepiad flowers can only be considered highly specialized at the functional group level (Shuttleworth & Johnson 2008) when the mutilation of pollinator is not taken into account. When pollinators lose part of their body or die trapped in flowers, the relationship is probably more antagonistic than mutualistic, because the amount of pollinated flowers decreases (Morse 1981) and the pollinators become less efficient (Shuttleworth & Johnson 2009).

Acknowledgment

The author thanks Dalton S. Amorim for identifying the Sciaridae and the Fundação de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ) for the financial support.

Literature cited

• Blanco, M.A. & Barboza, G. 2005. Pseudocopulatory Pollination in Lepanthes (Orchidaceae: Pleurothallidinae) by Fungus Gnats. Annals of Botany 95: 763-772.
• Barbosa, A.R., Melo, M.C. & Borba, E.L. 2009. Self-incompatibility and myophily in Octomeria (Orchidaceae, Pleurothallidinae) species. Plant Systematics and Evolution 283: 1-8.
• Corry, T.H. 1884. On the Structure and Development of the Gynostegium, and the Mode of Fertilization in Asclepias cornuti Descaisne (A. syriaca L.). Transactions of the Linnean Society of London 2: 173-207.
• Demarco, D. 2017. Staminal wing and a novel secretory structure of asclepiads. Botany 95: 763-772.
• Duque-Buitrago, C.A, Alzate-Quintero, N.F. & Otero, J.T. 2014. Nocturnal Pollination by Fungus Gnats of the Colombian Endemic Species, Pleurothallis marthae (Orchidaceae: Pleurothallidinae). Lankesteriana 13: 407-417.
• Endress, P.K. 1996. Diversity and evolutionary biology of tropical flowers. 2 ed. Cambridge University Press, Cambridge.
• Forster, P.I. 1992. Insects associated with the flowers of Marsdenia cymulosa Benth (Asclepiadaceae) and their possible role in pollination. Australian Entomological Society 19: 45-47.
• Koschnitzke, C. 2015. Polinizadores e visitantes florais de três táxons de Asclepiadoideae (Apocynaceae) na restinga de Maricá, Rio de Janeiro, Brasil. Natureza online 13: 165-176.
• Medeiros, J.F., Rapini, A., Barbosa, U.C., Py-Daniel, V. & Braga, P.I.S. 2008. Primeiro registro de Simuliidae (Diptera) com polinários de Asclepiadoideae (Apocynaceae). Neotropical Entomology 37: 338-341.
• Morse, D.H. 1981. Modification of bumblebee foraging: The effect of milkweed pollinia. Ecology 62: 89-97.
• Nihei, S.S. & Schwarz, E.A. 2011. On the first tachinid fly (Diptera, Tachinidae) carrying Asclepiadoideae pollinaria in the Neotropical Region. Revista Brasileira de Entomologia 55: 441-444.
• Ollerton, J. & Liede, S. 1997. Pollination systems in the Asclepiadaceae: a survey and preliminary analysis. Biological Journal of the Linnean Society 62: 593-610.
• Pant, D.D., Nautiyal, D.D., Chaturcedi, S.K. 1982. Pollination ecology of some Indian asclepiads. Phytomorphology 32: 302-313.
• Shuttleworth, A. & Johnson, S.D. 2008. Bimodal pollination by wasps and beetles in the African milkweed Xysmalobium undulatum Biotropica 40: 568-574.
• Shuttleworth, A. & Johnson, S.D. 2009. Palp-faction: an African milkweed dismembers its wasps pollinators. Environmental Entomology 38: 741-747.
• Song, B., Zhang, Z., Stöcklin, J., Yang, Y., Niu, Y., Chen, J. & Sun, H. 2013. Multifunctional bracts enhance plant fitness during flowering and seed development in Rheum nobile (Polygonaceae), a giant herb endemic to the high Himalayas. Oecologia 172: 359-370.
• Wolff, D., Meve, U. & Liede-Schumann, S. 2008. Pollination ecology of Ecuadorian Asclepiadoideae (Apocynaceae): How generalized are morphologically specialized flowers? Basic and Applied Ecology 9: 24-34.

Publication Dates

• Publication in this collection
  Mar 2018

History

• Received
  15 Sept 2017
• Accepted
  03 Jan 2018