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Flies –Pollinators on two wings

 by Axel Ssymank, Bonn & Carol Kearns, Santa Clara

see http://www.bfn.de/0502_skripten.html

1. Diptera as pollinators

Diptera, the true flies, are an important, but neglected group of pollinators. Diptera can be distinguished from other insects by their two membranous front wings and the highly reduced halteres that represent the remnants of the second pair of wings. They are an ancient group, and were probably among the first pollinators of early flowering plants.

The drone-fly, Eristalis tenax, a harmless flower fly pollinating a garden Aster. © Axel SsymankMany people think of flies as pests, and certainly there are many pest species. Fewer people realize the beneficial activities provided by flies, including pest control, as food for valued species such as birds and fish, as decomposers and soil conditioners, as water quality indicators, and as pollinators of many plants. 

At least seventy-one of the 150 (Evenhuis et al. 2008) Diptera families include flies that feed at flowers as adults. More than 550 species of flowering plants are regularly visited by Diptera (Larson et al. 2001) that are potential pollinations. Diptera have been documented to be primary pollinators for many plant species, both wild and cultivated. 

Flies live almost everywhere in terrestrial ecosystems and they are abundant in most habitats. With over 160,000 species, flies form an extremely large and diverse group, varying in mouth parts, tongue length, size and degree of pilosity. The diversity of flower-visiting flies is reflected in their effectiveness as pollinators. Some flies, such as long-tongued tabanids of South Africa, have specialized relationships with flowers, while other flies are generalists, feeding from a wide variety of flowers. In some habitats, such as the forest under-story where shrubs may produce small, inconspicuous, dioecious flowers, flies seem to be particularly important pollinators. In arctic and alpine environments, under conditions of reduced bee activity, flies are often the main pollinators of open, bowl-shaped flowers, with readily accessible pollen and nectar.

2. Why do flies visit flowers?

Flies visit flowers for a number of reasons. The most important is for food in the form of nectar and sometRhingia campestris, a flower fly with a long snout concealing a proboscis as long as its body sitting on a Geranium-flower. © Axel Ssymankimes pollen. Nectar, a sugary solution, provides energy. Pollen is rich in proteins, which is required by some adult flies before they can reproduce.  

Other flies visit flowers to lay eggs, and the larvae feed on the flower heads or the developing fruits and seeds. Plants with carrion flowers deceive flies into visiting and effecting pollination by providing a scent and appearance that mimics the carcasses where these types of flies normally lay their eggs. In cold, arctic and alpine habitats, some flowers attract flies by providing a warm shelter. Flies bask in the warmth, which can be more than 5 degrees C warmer than the ambient temperature (Luzar and Gottsberger 2001). This keeps their flight muscles warm, and allows them to fly at temperatures that would thwart most bees. Their movement between flowers results in pollination. Flowers can also serve as rendezvous sites for mating. Large numbers of flies will congregate at a particular type of flower, and the byproduct of their behavior can be pollination.

3. Cultivated plants pollinated by flies

More than 100 cultivated crops are regularly visited by flies and depend largely on fly pollination for abundant fruit set and see production (Ssymank at al. 2008). In addition a large number of wild relatives of food plants, numerous medicinal plants and cultivated garden plants benefit from fly pollination. Klein et al. (2007) reviewed the literature for crop pollination and concluded that 87 out of 115 leading global food crops are dependent on animal pollination. They present a table of pollinators for those crops where this information is known. For thirty crop species flies are listed as pollinators and visitors (with 14 cases referring to flower flies, Syrphidae). This result certainly underestimates the importance of fly pollination for two major reasons: first pollination studies focus mainly on bee pollination, second the literature and data on fly pollination are much more dispersed and often published in smaller journals with less complete indexing. From just my own non-systematic field data (Ssymank) we could add at least 12 crop species which are visited or partly pollinated by flower flies, such as Fagopyron esculentum (18), Mangifera indica (6), Prunus spinosa (35), and Sambucus nigra (24; number of fly species known to visit in brackets). 

A cocoa blossom (Theobroma cacao) in Togo, Africa. © Axel SsymankA cocoa fruit (Theobroma cacao) in Togo, Africa. © Axel Ssymank

Ornidia obesa, a large metallic green neotropic flower fly, now spreading in cocoa-plantations over the whole african continent. © Axel Ssymank

No chocolate without flies: For the cocoa tree (Theobroma cacao) fly pollination is essential for fruit production, with various levels of self-imcompatibility present in different cocoa varieties. Here very small midges of the families Ceratopogonidae and Cecidomyiidae pollinate the small white flowers emerging from the stems. In addition to these midges, Ornidia obesa (a flower fly) may visit the cocoa flowers, since it is widespread in tropical cocoa plantations and larvae live in organic waste in the moist environment.

Larger flies such as carrion and dung flies visit and pollinate pawpaw (Asimina triloba). Many Rosaceous flowers in the northern hemisphere are visited and at least partly pollinated by flower flies (Syrphidae): Apple (Malus domestica) and Pear (Pyrus communis) trees, strawberries (Fragaria vesca, F. x ananassa), Prunus species (cherries, plums, apricot and peach), Sorbus species (e.g. Rowanberry) and most of the Rubus-species (Raspberry, Blackberry, Cloudberry etc.) as well as the wild rose Rosa canina.

Flower flies are among the most important pollinating insect groups other than bees (Apidae), pollinating and visiting a number of tropical fruits such as Mango (Mangifera indica), Capsicum annuum and Piper nigrum. They also visit a number of spices and vegetable plants of the family Apiaceae like fennel (Foeniculum vulgare), coriander (Coriandrum sativum), caraway (Carum carvi), kitchen onions (Allium cepa), parsley (Petroselinum crispum) and carrots (Daucus carota). Most people are aware that bees are vital for the pollination of flowers. Fewer people realize that flies are second in importance to bees as pollinating insects. Compared to bees, which must provision a nest with floral food, adult flies have low energy requirements. Although this makes flies less devoted to the task of moving quickly between flowers, it also frees them to bask in flowers and remain active at low temperatures. 
Mango trees (Mangifera indica) represent an important tropical crop on local markets with a complex pollinator system involving many flower flies. © Axel SsymankThe flower fly Asarkina madecassa is an endemic flower fly visiting Mango-flowers in Madagascar. © Axel Ssymank

Conditions affecting bee populations can be quite different from those affecting fly populations due to the great difference in larval requirements. Most entomophilous flowers are visited by multiple types of insects. Since insect populations fluctuate temporally, the relative importance of a particular pollinator to a flower is likely to vary with time. Many types of flies have few hairs when compared to bees, and pollen is less likely to adhere to the body surface. But under conditions when bees are scarce, an inefficient pollinator is better than none. Higher flight activities of flies may well compensate lower pollen carrying capacity. Even in cases where honeybees are abundant on flowers and specialised bees like Megachile lapponica on Epilobium angustifolium are foraging, flower flies (Syrphidae) can be the most effective pollinators producing the highest seed set (Kühn et al. 2006). 

4. Flowers flies (Syrphidae) as pollinators and in biocontrol

Flower flies (Syrphidae) represent a large family of flies with a double role in ecosystems: adults are mostly flower visitors and of high importance for pollination services, while about 40 % of the world's species have zoophagous larvae contributing to biocontrol in agriculture and forestry.

The family of flower flies has approximately 6000 named species in 200 genera worldwide. They occur in almost every terrestrial habitat, from dunes, salt marsh, heath lands, bogs, all grassland ecosystems, scrub and forest-ecosystems, from low altitudes up to glacial moraine fields. They are represented in all zoogeographic regions of the worlds. Flower flies as pollinators have a wide range of adaptations for visiting different flower types, including proboscis lengths from 1mm to almost body length (with 11 mm for example in Rhingia, Ssymank 1991), enabling them to exploit deep corollas of zygomorphic flowers. Flower flies visit large numbers of different plant species. For example in Germany more than 600 plant species are visited (Ssymank unpubl. data) and in Belgium more than 700 plant species (De Buck 1990, 1993). Regional studies in Europe (Ssymank 2001) showed that up to 80% of the regional flora may be visited by flower flies. Preferences for certain colours, flower types, flight height and phenology of simultaneously flowering plants usually ensure a high flower constancy of flower flies. With their high flight and flower-visiting activity they can be quite effective pollinators. Even long distance pollen transport is possible by migrating species like Eristalis tenax or Helophilus species. Many flower fly larvae play an important role in biocontrol. About 40% of the species have zoophagous larvae, mainly eating crop-damaging aphids. Some species, such as Episyrphus balteatus in Europe can reproduce rapidly, producing large numbers of eggs and up to five generations per year. Females can smell aphid colonies and and use olfactory cues to oviposit directly in or in the vicinity of the colonies. Provided semi-natural structures are present in a habitat, rapid population growth and effective biocontrol preventing aphid outbreaks is possible.

Third stage larvae of Syrphus eating aphids. © Axel SsymankFlower fly pup before hatching (Syrphus). © Axel SsymankNewly emerged Episyrphus balteatus, male. © Axel SsymankThe life cycle of an aphidophagous flower fly like e.g. Episyrphus balteatus can be completed within only 15-20 days under optimal conditions. Eggs are laid in aphid colonies, larvae hatch immediately, first larvae mould after 1 day, the second larvae mould after 2-3 days and larval stage 3 is devouring up to 300 aphids per night until it pupates. The newly emerged adult is after a short time ready for mating and giving rise to a new generation. 

5. Plant-pollinator interactions

Pollinators have a keystone function in ecosystems. Without pollination many wild plants could not reproduce and survive. Animals, too, are indirectly dependent on pollination services, as they feed on fruit or plants that would not exist without pollinators. Pollination is an ecosystem service that maintains wild plant and crop diversity, guarantees food safety and is a cornerstone of animal diversity. Flies and bees are the most important pollinator groups. Over 71 families of Diptera are known to visit and pollinate flowers, linking the fate of plants and animals. Depending on the region, the time of the day, the flowering phenology and weather conditions, flies may be the main or exclusive pollinators, or share pollination services with bees and other pollinator groups.

The flower fly Chrysotoxum “intermedium (aggregate) pollinating the flowers of the tree spurge (Euphorbia dendroides) on the Maltese islands. © Axel SsymankWhile some flower - pollinator relationships are highly specialised, many pollinator interactions are complex systems usually involving several pollinators. Daily and seasonal changes in pollinator communities are frequent, especially in plants with long flowering periods. Plant species with large ranges or cultivated in large areas may have a significant regional or geographical variation in pollinator communities, and the surrounding landscape with its features and habitat requisites can play an important role. Many pollinator assemblages are not well understood or even known, a fact not only true for wild plants but also for many crops and cultivated plant species. 

6. Pollinator decline and research needs

Our understanding of pollination services is considerably hampered by a lack of some very basic knowledge. Although some types of fly pollinators have been well studied, as a group, fly pollination deserves far more research. It is striking how large the gaps in species knowledge are: probably less than 10% of all Diptera species are named worldwide; considerable gaps exist even in Europe, where the fauna is generally well documented. For many groups, even the existing knowledge is not easy to use, as identification keys are missing. 

Monoceromyia is a flower fly genus with many afrotropical species, mimicking wasps, and visiting tropical trees. © Axel SsymankPollination services of flies are underestimated and functional relations poorly understood. In the past, much pollination research has focused on bees, leaving a wide opportunity open for the study of other pollinator assemblages. A systematic look at ecosystems without bees (e.g. on some islands, in high mountains, nordic or arctic environments) could provide insight into functional replacements, and into the evolution of plant and fly adaptations. The review by Klein et al. (2007) makes it apparent that even crop plant - pollinator systems are incompletely studied. Many cases of "unknown" pollinators or order-level indications of "Diptera" indicate the need for more research.

Today, ecologists are concerned that climate change may decouple the synchrony of inter-dependent organisms. For the majority of flies, we do not have baseline phenology information. For flower flies (Syrphidae) the data are better than for many other small Diptera groups. Examples of changes in range and phenology of flower flies exist - however possible desynchronisation of flowering plants and their pollinators have not yet been studied. There is evidence of parallel pollinator and insect-pollinated plant decline for flower flies and bees in UK and NL (Biesmeijer et al. 2006). The factors threatening the species are mostly unknown. Data from other countries is largely absent. Many pollinating Diptera groups are not even assessed in Red-data-Books as no data or no fly specialists exist.

What consequences can we expect from the loss of pollinators? To what extent can any one pollinator be replaced by another? The answers to these questions are unknown and urgently need investigation. The loss of honeybees to Colony Collapse Disorder has led to severe declines of bee colonies in the U.S. Unwise application of pesticides has caused honeybee losses again and again. The loss of honeybees has not only beekeepers and ecologists, but the general public alarmed. And yet loss of natural pollinator communities may cause dramatic changes in ecosystems and biodiversity. Our current knowledge is too limited to extend to natural systems. There is an urgent need for networking among researchers, and for more fundamental and applied research toward improving our knowledge of pollination services. A new and better understanding will allow for active, effective management of pollinators for crop production and for the conservation and maintenance of biodiversity of terrestrial ecosystems worldwide. 

Further suggested reading:

KEARNS, C. A. 2001. North American dipteran pollinators: assessing their value and conservation status. Conservation Ecology 5(1): 5. [online] URL: http://www.consecol.org/vol5/iss1/art5/

Special COP9-issue of Tropical Conservancy on Agrobiodiversity:

SSYMANK, A., KEARNS, C.A., PAPE, TH. & F.C. THOMSON: Pollinating Flies (Diptera): A major contribution to plant diversity and agricultural production. - Tropical Conservancy 9 (1 & 2): 86-89.

Introduction to flower flies:

GILBERT, F.S. (1986): Hoverflies. Naturalists' Handbooks. - Cambridge, 66 pp.

SCHMID, U. (1996): Auf gläsernen Schwingen. Stuttgarter Beiträge zur Naturkunde, Serie C 40: 1-81, Stuttgart. [in German]

Citations 

BIESMEIJER, J. C., ROBERTS, S. P. M., REEMER, M., OHLEMÜLLER, R., EDWARDS, M., PEETERS, T., SCHAFFERS, A. P., POTTS, S. G., KLEUKERS, R., THOMAS, C. D., SETTELE, J., AND W. E. KUNIN, W. E. 2006. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313 (5785): 351-354.

DE BUCK, N. 1990. Bloembezoek en bestuivingsecologie van Zweefvliegen (Diptera, Syrphidae) in het bijzonder voor Belgie. - Studiendocumenten Royal Belgian Institute of Natural Sciences. 60: 1-167, Brussels. 

DE BUCK, N. 1993. Bloembezoek en bestuivingsecologie van zweefvliegen (Diptera, Syrphidae) in het bijzonder voor Belgie. Appendix to working document '60' of the Royal Belgian Institute of Natural Sciences. – unpublished, 56. pp.

EVENHUIS, N. L., T. PAPE, A.C. PONTAND, F.C. THOMPSON (Eds.). 2008. Biosystematic Database of World Diptera, Version 10. http://www.diptera.org/biosys.htm, accessed on 20 January 2008.

KLEIN, A.-M., VAISSIÈRE, B.E., CANE, J.H., STEFFAN-DEWENTER, I., CUNNINGHAM, S.A., KREMEN, C. & T. TSCHARNTKE (2007): Importance of pollinators in changing landscapes for world crops. - Proc. R. Soc. B (2007) 274, 303–313, Published online 27 October 2006.

KÜHN, J., A. HAMM, M. SCHINDLER, D.WITTMANN (2006): Ressourcenaufteilung zwischen der oligolektischen Blattschneiderbiene Megachile lapponica L. (Hym., Apiformes) und anderen Blütenbesuchern am schmablättrigen Weidenröschen (Epilobium angustifolium, Onagrarceae). Mitt. Dtsch. Ges. Allg. Angew. Ent., 15: 389-391.

LARSON, B. M. H., P. G. KEVAN AND D. W. INOUYE. 2001. Flies and flowers: The taxonomic diversity of anthophiles and pollinators. Canadian Entomologist 133(4): 439-465.

LUZAR, N. AND G. GOTTSBERGER 2001. Flower Heliotropism and Floral Heating of Five Alpine Plant Species and the Effect on Flower Visiting in Ranunculus montanus in the Austrian Alps. Arctic, Antarctic, and Alpine Research, Vol. 33, No. 1 (Feb., 2001), pp. 93-99

SSYMANK, A. (1991): Rüssel- und Körperlängen von Schwebfliegen (Diptera, Syrphidae) unter Berücksichtigung der Verwendung von Alkoholmaterial. – Mitt. Schweizer. Entom. Gesellschaft 64: 67 – 80.

SSYMANK, A. 2001. Vegetation und blütenbesuchende Insekten in der Kulturlandschaft [Vegetation and flower-visiting insects in cultivated landscapes] - Schriftenreihe Landschaftspflege und Naturschutz 64, 513 pp., Bonn-Bad Godesberg.

SSYMANK, A., KEARNS, C.A., PAPE, TH. & F.C. Thomson: Pollinating Flies (Diptera): A major contribution to plant diversity and agricultural production. - Tropical Conservancy 9 (1 & 2): 86-89.

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