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Pollination and Floral Ecology$

Pat Willmer

Print publication date: 2011

Print ISBN-13: 9780691128610

Published to Princeton Scholarship Online: October 2017

DOI: 10.23943/princeton/9780691128610.001.0001

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Pollination by Flies

Pollination by Flies

Chapter:
(p.304) Chapter 13 Pollination by Flies
Source:
Pollination and Floral Ecology
Author(s):

Pat Willmer

Publisher:
Princeton University Press
DOI:10.23943/princeton/9780691128610.003.0013

Abstract and Keywords

This chapter focuses on pollination by flies, a very diverse group of insects of the order Diptera. Many types of fly have the ability to regurgitate saliva onto potential foodstuffs, making the material more liquid and manageable, and some use “bubbling” behavior to speed evaporation of excessively dilute fluids. Many groups have a strong preference for sugary fluids, and therefore commonly take some nectar as part of their adult diet; others feed on pollen. The chapter first provides an overview of the fly’s feeding apparatus as well as its sensory and behavioral capacities before discussing generalist flowers that are favored by a multitude of flies. It then considers specialist flower types that attract nectar-feeding flies, hoverfly flower types, and carrion-fly flower types. It concludes with an analysis of some other specialist cases of fly pollination of flowers.

Keywords:   fly pollination, Diptera, nectar, flower, pollen, feeding apparatus, generalist flower, specialist flower, hoverfly, carrion fly

Outline

  1. 1. Feeding Apparatus

  2. 2. Sensory and Behavioral Capacities

  3. 3. Generalist Fly Flowers

  4. 4. Specialist Nectar-Feeding Fly Flower Types

  5. 5. Hoverfly Flower Types

  6. 6. Carrion-Fly Flower Types

  7. 7. Some Other Specialist Cases

  8. 8. Overview

The flies (order Diptera) constitute a very diverse group of insects, all characterized by just one pair of wings, the ancestral rear pair being modified as flight- and balance-control organs termed halteres. Hence flies are often very agile fliers, able to take off and land in any direction and often to hover (rare in other insects). Fly mouthparts are essentially suctorial, but can be either piercing and sucking (using either plant or animal fluids) or merely sucking and lapping without the ability to pierce tissues. Many types of fly have the ability to regurgitate saliva onto potential foodstuffs, making the material more liquid and manageable, and some use “bubbling” behavior to speed evaporation of excessively dilute fluids. The feeding habits of flies are therefore highly varied, and different taxa are able to suck, lap, chew, or bite, so that flies can be found taking advantage of almost all possible foodstuffs. A great many groups (from at least 45 fly families) have a strong preference for sugary fluids, and therefore commonly take some nectar as part of their adult diet, by sucking or lapping at flowers; quite a number also take pollen.

Some flies after visiting a flower will carry moderate amounts of pollen on their bodies, making them potentially useful as pollinators; but many of them do not move large distances between plants (the mean interplant distance is usually less than 1 m), reducing their value for effecting cross-pollen movements. However, a few taxa are more inclined to make long-range movements and thus are more useful. One family in particular, the hoverflies (Syrphidae), are specifically equipped for pollen feeding and rely almost entirely on flowers for their adult food intake; they also move much more regularly and systematically through flower patches and are well known as efficient and important pollen vectors in temperate zones.

Before going into further details on any particular flower-visiting flies, some basic fly taxonomy is necessary to make sense of this group as possible pollinators. An overview is shown in table 13.1. Formerly the flies were subdivided into three main parts, but molecular evidence has clarified matters and there are now just two suborders, the second divided into four main infra-orders (see Yeates and Wiegmann 1999; Wiegmann et al. 2003). The most primitive flies are in the suborder Nematocera (meaning “threadlike antenna”), mostly very small and with very short mouthparts, and commonly with aquatic larval stages. These are the midges, mosquitoes, gnats, and craneflies, all of which are poorly endowed with attributes that might make them good pollinators but which can nevertheless be quite common on flowers; and they may represent the earliest of all flower-visiting animals (see chapter 4 and Thien et al. 2009). They are especially abundant in arctic and montane habitats (see chapter 27) where other insects are rare. They take mainly nectar from flowers, although some bibionids, mycetophilids, and scatopsids also eat pollen according to (p.305)

Table 13.1 Dipteran Taxonomy, Showing Some of the Main Groups of Flies Potentially Found on Flowers; Those with Significant Flower-Visiting Habits Are Shown in Bold

Suborder

Infra-order

Families

Common name

Nematocera

Tipulidae

Crane flies

Psychodidae

Owl midges

Culicidae

Mosquitoes

Ceratopogonidae

Biting midges

Chironomidae

Nonbiting midges

Simuliidae

Black flies

Bibionidae

Fever flies, St Mark’s flies

Mycetophilidae

Fungus gnats

Cecidomyiidae

Gall midges

Scatopsidae

Brachycera

Xylophagomorpha

Xylophagidae

Stratiomyomorpha

Stratiomyidae

Soldier flies

Tabanomorpha

Tabanidae

Horse flies

Rhagionidae

Snipe flies

Muscomorpha

Heterodactyla

Nemestrinidae

Long-tongued flies

Apioceridae

Flower-loving flies

Bombyliidae

Bee-flies

Asilidae

Robber flies

Therevidae

Eremoneura

Empididae

Empids

Dolichopodidae

Dance flies, long-headed flies

Cyclorrhapha

Platypezidae

Phoridae

Scuttle flies

Syrphidae

Hoverflies

Schizophora

Conopidae

Tephritidae

Trypetidae

Sepsidae

Sciomyzidae

Coelopidae

Sphaeroceridae

Ephydridae

Drosophilidae

Fruit flies

Chloropidae

Scathophagidae

Dungflies

Anthomyiidae

Lesser house flies

Fanniidae

(House flies)

Muscidae

House flies

Calliphoridae

Blow flies, bluebottles

Sarcophagidae

Flesh flies

Tachinidae

Source: Taxonomy based on B. M. Wiegmann et al. 2003.

(p.306) early records (Willis and Burkill, 1895–1908, UK flower-visiting records). Gnats, midges and mosquitoes of both sexes may take floral nectar as fuel, although for the females it is blood meals that provide the main fluid intake. Many of these insects, of either sex, are particularly active on flowers toward dusk, when their flights in search of their vertebrate hosts tend to reach a peak.

The second and much larger suborder is the Brachycera, usually stouter and with shorter antennae. The more ancestral parts of this taxon (see table 13.1) include a few moderately important flower-visiting groups, notably soldier flies (stratiomyids), which are brightly or metallically colored flies that occur reasonably commonly on flowers with exposed nectar, such as umbellifers. Rhagionids can also be quite common on such flowers; relatively large, with elongate pointed abdomens, they take some nectar but use flowers more commonly as encounter sites for prey or for mates. The same could be said of apiocerids, therevids, and asilids, in the slightly more advanced Muscomorpha/Heterodactyla grouping; also here are the acrocerids, where the genus Eulonchus contains some flower visitors selecting geraniums and similar forms with good floral constancy (Borkent and Schilinger 2008). But this taxon above all contains two key flower-visiting families, the bee-flies (Bombyliidae) and the nemestrinids. Bombyliids are long tongued (commonly 8–12 mm, but occasionally much longer than this) and are reasonably common in temperate habitats but especially abundant in Mediterranean and semiarid habitats. The Nemestrinidae are also long tongued, some species having exceptionally long probosces up to 70 mm, and are important in southern Africa, sometimes exclusive to particular long-corolla flowers. These two families originated around 210–180 MYA (Wiegmann et al. 2003), before the evolution of angiosperm flowers, so the earliest forms may have fed on Jurassic gnetaleans and other preflower structures.

The cyclorrhaphan and schizophoran subgroupings are enormous and within the former the key group is the specialist flower-feeding hoverflies (Syrphidae), which are rather like bees in their reward needs and floral preferences; they commonly have tongue lengths of 2–8 mm. The scuttle flies (Phoridae) are also potential pollinators of certain flowers, including Araceae and some of the elaborate Aristolochiaceae (Rulik et al. 2008). The Schizophora encompasses the higher flies, taxonomically difficult and with a host of small families. The drosophilids—fruit flies—are sufficiently familiar to have a common name; beyond them, the familiar house flies, blowflies, bluebottles, and botflies, as well as most of the dung- and carrion-visiting fly types, are the most recently evolved families (Calyptratae), many with flower-visiting propensities.

1. Feeding Apparatus

Flies are endowed with a proboscis (fig. 13.1) made up from a basal rostrum, plus the ancestral unpaired labrum and hypopharynx, which together normally form a short tube that lies on the labium. The labium forms the ventral wall of the food canal, and its tip is expanded into a pair of conspicuous flat pads termed the labella, each labellum bearing grooves known as pseudotracheae (Gilbert and Jervis 1998; see also Krenn et al. 2005). Where the proboscis is relatively short, flies can exploit many exposed fluids with a dabbing or lapping action, drawing fluid onto the pads (the pseudotracheal grooves often have hydrophilic inner linings to aid fluid uptake) and then upward into the mouth; but they can also use quite solid materials by first suspending the particles in saliva regurgitated through the hypopharynx.

In a few of the families, where there are flies with a more elongate proboscis, feeding from long tubular corollas becomes possible, as well as from the generalist open flowers repeatedly mentioned in the previous chapter. For example, in bombyliid flies the ventral part of the proboscis base is extended, and the suctorial mechanism is also more powerful, giving a tongue that can penetrate and suck fluid from quite deep corolla tubes. The labellar musculature is also altered, and these flies can feed from laterally opening flowers as well as those with frontal and dorsal openings (Szusich and Krenn 2002).

Where substantial pollen is taken in (suspended in nectar, especially in syrphids) the mouthparts tend to be shorter and the labella are broader with more pseudotracheae, the width of the furrows perhaps reflecting the preferred sizes of pollen grains (Gilbert and Jervis 1998).

2. Sensory and Behavioral Capacities

It has usually been noted that flies use visual cues for longer-range flower-seeking and then cue in to olfactory signals at closer range. The eyes of day-flying (p.307)

Pollination by Flies

Figure 13.1 The basic fly proboscis, with views of the labellar surface and pseudotracheae, and a transverse section showing the food channel at X. Dark areas are underlying sclerites.

(Largely modified from Gilbert and Jervis 1998.)

flies are large and sophisticated by insect standards, and all groups of flies so far tested have good trichromatic color vision. Flower foragers in at least some families (syrphids, calliphorids, anthomyids, tephritids) have an apparently innate preference for yellow, closely aligned with the wavelengths reflected from pollen in the centers of most of the generalist flowers; an innate response was clearly demonstrated in a syrphid by Sutherland et al. (1999). However, some of the more specialized flower-visiting bombyliid bee-flies prefer pinks, mauves, and blues, associated with particular radial flower forms (Johnson and Dafni 1998).

Flies have long-range chemosensors (sited on the antennae) that are abundant and receptive to many floral odors, plus taste receptors (contact chemosensors, on the mouthparts and on the feet) that are highly attuned to detection of sucrose and/or glucose.

Various taxa show associative learning, linking color or odor to reward, although some have innate preferences that persist despite training (e.g., syrphids retain their strong preference for yellow; Lunau 1992c). For Lucilia (the common greenbottle calliphorid) this kind of associative learning can occur with just one trial (Fukushi 1989), as shown in figure 13.2. Some flies can learn and use spatial landmarks, and various male syrphids use this ability to become territorial, managing to hover in one site reliably over successive days using visual cues, and chasing off intruders with considerable targeted accuracy (Collett and Land 1975). With sugar-seeking habits plus sophisticated sensory abilities and behavioral repertoires, a whole range of flies are therefore important components of the flower-visiting fauna in many habitats.

There is little evidence for different kinds of foraging behaviors in different fly groups; for example, on Clematis ligustifolia Borkent and Harder (2007) recorded similar visit and revisit frequencies across a range of culicids and small to large muscids, and on Shepherdia they found no differences between syrphid and empid behaviors.

3. Generalist Fly Flowers

A wide range of small open flowers with exposed nectaries, occurring either singly or in clustered umbels or capitula (see fig. 2.11) are accessible to, and favored by, a multitude of flies. This includes both the more primitive midges and mosquitoes and the advanced syrphid and muscid types. The flies operate using the “spit and lap” technique that allows feeding on nectar of almost any concentration, but which is especially useful when exposed nectar becomes more concentrated on warmer and drier days. Muscids in particular can take nectar that is effectively crystalline, in excess of 75% concentration, when virtually all other flower (p.308)

Pollination by Flies

Figure 13.2 Substantial associative learning occurs in a single trial in the calliphorid fly Lucilia cuprina, trained on either blue or yellow paper circles mimicking flowers.

(Drawn from data in Fukushi 1989.)

visitors are unable to use this; they can be seen actively feeding on a range of familiar umbellifers—such as hogweed (Heracleum), carrot (Daucus), and parsnip (Pastinaca)—on the hottest summer days.

These kinds of flowers are traditionally referred to as myophilous, and the generalist fly flower syndrome as myophily. The typical flowers have the following properties:

  1. 1.They are small and open, flat or shallow bowl shaped, radially symmetrical

  2. 2. They are often clustered into inflorescences

  3. 3. They are white or cream, or sometimes greenish-yellow, in color

  4. 4. They have mild, sweet or musty, but usually not unpleasant smells

  5. 5. They open in the daytime, often producing nectar throughout the middle of the day

  6. 6. The nectar is exposed, high concentration and low volume.

There is an evident overlap here with the generalist syndrome described in the last chapter, and it is quite reasonable to merge these all into one syndrome, encompassing flowers visited by all the beetles, wasps, and short-tongued flies.

Similar floral designs can be found on a larger plant framework on many familiar temperate trees that have open accessible flowers—lime (Tilia), sycamore (Acer), rowan (Sorbus), and hawthorn (Crataegus), as well as some fruit trees (Malus and Prunus). Not surprisingly, all of these too are frequented by many of the fly groups, and the plants could be included as exemplifying the myophily syndrome. In fact the reality of “generalist fly flowers” can readily be tested by enthusiastic observers in their own gardens: a single sunny day spent watching the flowers of Tilia, Heracleum, or Crataegus can easily yield records of ten or more fly families, and hundreds of individual dipteran visits (although visits from beetles and wasps may also occur, and activity from at least a few bees is also likely). Examples of such records can be found in Corbet, Unwin et al. (1979), Willmer (1983), and Zych (2002, 2007).

Small flies from the lower taxonomic groups also visit plants that are low growing and so produce their flowers close to the ground, where the microclimate may be more equable and humid, suited to a small flying ectothermic animal. Some alpine plants with tiny clustered flowers exemplify this scenario—saxifrages and sedums, among others. Climbers with flowers growing close to surfaces have similar properties, and flies are common at ivy flowers in autumn. Flies also visit a range of somewhat taller fairly generalist plants with bowl flowers, such as meadowsweet (Filipendula), rock-rose (Potentilla), and other Rosaceae, or certain kinds of Clematis (Ranunculaceae); or those with very short tubular corollas growing in masses, for example some asters and scabious, valerians (Valeriana), (p.309) mints (Mentha), and some spurges (Euphorbia). Again, white and rather pale pinks or yellows tend to dominate, and the individual flowers are radial or nearly so, usually close enough together for a fly to walk between them across the inflorescence surface (see plate 1B,G).

A few of the lower Brachycera fly families should also be picked out for mention here. The stratiomyids or soldier flies, with conspicuously colored and somewhat flattened bodies, are reasonably frequently seen on flowers, especially in waterside habitats; their tongues are quite short but spread out at the tip into large labella that lap up medium-concentrated nectars very effectively. They visit Apiaceae regularly, and some of the shorter-tubed Asteraceae. Empids are also regular flower visitors, although primarily predatory; their mouthparts look relatively well suited for nectar feeding, being designed for piercing, but the proboscis is rather rigid and inflexible (suited to its role of stabbing into prey) so in practice works best when probing into shorter corollas than one might predict on tongue length alone. Empids occur quite commonly on daisy-type flowers with medium corolla lengths, such as knapweeds and thistles (Centaurea and Cirsium), which hold nectar at the base of tubes several millimeters in length.

Within the Schizophora, flies from several families are generalist flower visitors, all having short tongues that merely mop up nectar. Sepsids are small ant-like flies, often common on umbels. Some of the tephritids and trypetids are brood-site parasites of flowers, laying their eggs in flower heads of various composites; they may transfer some pollen between plants, but any benefit to the plant is probably outweighed by the subsequent loss of flowers or seeds to the feeding larvae. The same may be true of the fruit flies (Drosophilidae), which are often attracted to nectar and sometimes lay eggs in flower heads (Miyake and Yafuso 2003, 2005), particularly of flowers in the family Araceae with rather fruity scents. Chloropids are small, often yellow-colored flies that again visit Apiaceae and Asteraceae but are additionally regularly recorded on forget-me-nots (Myosotis); the family also includes the frit flies (Oscinella) which are serious pests of cereals where they lay their eggs.

Higher schizophorans include most of the flies familiar to the layman and irritatingly present in urban situations. They are generally quite large and round bodied, and many are rather bristly in appearance (especially the tachinids). A number of the families are important, albeit rather generalist, flower visitors, and they are probably more use as pollinators than the lower muscomorphs, primarily because of their larger size. All the groups commonly termed “house flies” (muscids in the broad sense, including anthomyiids and fanniids) are generalists flower foragers (plate 1D), and because they are so numerous and so enamored of sugars they are probably the second most important kind of flower-visiting flies after the hoverflies. They can be found intermittently on almost any open flower offering access to sugary fluids. They therefore fit fully into the generalist myophily syndrome, although there are indications that they are more attracted to sweet-smelling flowers (such as meadowsweet (Filipendula), rowan (Sorbus), and mignonette (Reseda)) than some other flies. Lucilia (greenbottles) and Calliphora (bluebottles; see plate 1G) have similar habits to the muscids and can be particularly effective as pollinators of various Allium species such as leeks and onions (Clement et al. 2007), although the bluebottles also like to visit carrion (and so can be particularly problematic in spreading unwanted bacteria onto sugary foodstuffs). The same is true of the common yellow dungfly Scathophaga, which obviously frequents various kinds of dung but also visits flowers to find prey and to feed on both nectar and pollen; it can be common in late spring on buttercups and hawthorn, and in autumn on brambles and various umbels. The broad grouping of higher flies together contributes a substantial generalist flower-visiting cohort in most habitats. In northern parts of Europe and North America, and in mountain habitats, they may be more numerous than either bees or beetles; and with the generalist nematoceran flies added on they strongly dominate in the really cold alpine, taiga, and tundra zones.

Figure 13.3 shows distributions of various generalist myophilous flower visitors along a humidity or rainfall gradient in Patagonia (Devoto et al. 2005), with flies common in the wetter habitats and decreasing in areas of low rainfall; this may again be partly associated with temperature differences.

4. Specialist Nectar-Feeding Fly Flower Types

Those families of flies endowed with a longer slender proboscis may visit all the flower types referred to (p.310)

Pollination by Flies

Figure 13.3 Relative composition of flower-visiting fauna at eight sites in Patagonia, ordered from left to right along a decreasing humidity gradient; flies decrease in abundance in the drier sites.

(Redrawn from Devoto et al. 2005.)

above, but can in addition visit a substantially broader spectrum of floral morphologies, inserting their mouthparts into elongate corollas. Such flies tend to be more specifically seeking nectar and may show quite specialist relationships with particular flowers. The two classic examples are the bombyliids (bee-flies), common in many parts of the world, and the nemestrinids, which are largely restricted to southern Africa.

Bombyliids are unusual in having a long forward-pointing tongue that is not retractable, so they are easily recognized in flight and when hovering above flowers. However, in other respects they are confusing to an observer because (as the name implies) they appear very bee-like, having unusually rounded and furry bodies (plate 23H). When sitting on or hovering over flowers probing for nectar, they are very easily mistaken for small bees. In Europe, species of Bombylius reach the size of smaller bumble bees, and have tongues (fig. 13.4) that can be 10–12 mm in length; in Africa their diversity is greater and their tongues can be even longer.

The bombyliids are highly specialized nectar feeders, working systematically through floral communities, while selecting their preferred species carefully primarily by sight; and since they can carry substantial pollen on their body hairs they are clearly effective pollinators (although some may also eat a little pollen).

Kastinger and Weber (2001) indicated that their importance has usually been underestimated. They visit moderately small tubular flowers, which in temperate habitats are mainly white, blue, and purple (more rarely yellow). They are especially active in spring in temperate habitats, preferring sunlit sites, but visit flowers all year round in the tropics. Familiar preferred temperate flowers include violets (Viola), grape hyacinths (Muscari), stitchworts (Cerastium), various small-flowered Labiatae such as bugle (Ajuga) and ground ivy (Glechoma), and Boraginaceae such as forget-menots (Myosotis) and lungwort (Pulmonaria). Some also visit primroses and cowslips (Primula).

The bee-flies have a semiparasitic relationship with bees in their reproductive habits, since they lay eggs at or in the entrances of solitary bee nests, and their larvae develop by feeding on the stored provisions within; this habit has presumably led to selection for resemblance to bees.

The extreme case of long-tongued flower-visiting hovering flies is the family Nemestrinidae. All representatives have tongues more than 15 mm long and sometimes up to 70 mm (more than four times the body length; see fig 13.4C). In the same southern African habitats, and exploiting many of the same flowers, there are some very long-tongued bombyliids and (oddly) also some members of the family Tabanidae (p.311)

Pollination by Flies

Figure 13.4 (A) and (B) Bombylius tongue structure, and transverse section of the food channel formed by labrum and hypopharynx (modified from Gilbert 1981). (C) The extremely long tongue of a southern African nemestrinid fly, Megistorhynchus (redrawn from Barth 1985).

with tongues of up to 47 mm (plate 23G), although tabanids in other habitats are typically endowed with short stabbing mouthparts that can inflict painful bites on vertebrates. This unusual dipteran community interacts with a whole range of apparently specialized floral species (Johnson and Steiner 1995, 1997; Goldblatt and Manning 1999, 2000), some of the flowers perhaps forming mimicry rings (Johnson et al. 2003). These flowers are from several plant families, including Geraniaceae (pelargoniums), Iridaceae (iris/gladioli), and Orchidaceae; and they have many shared features, especially zygomorphic deep tubular morphology, often with additional nectar spurs and conspicuous nectar guides, and copious nectar at 20%–30% concentration. The various authors familiar with these interactions propose the recognition of a specific long-tongued fly syndrome to reflect both their importance in these ecosystems (see chapter 27), and the close match of morphological traits of insects and flowers. Johnson (2006) showed the functional synergy of fly and plant types here, and the convergent evolution in both partners, although he also noted that the flies and plants occur in “guilds,” lacking obligate one-to-one relationships, a particular plant species potentially being visited by more than one type of fly that in turn visits several plant species.

As well as the bombyliids and nemestrinids, there are other families of fly with less extreme elongate tongues that link to flower-visiting behaviours.

  1. 1.Conopidae often have moderately long tongues that are extended further by elongated labella. Various species can reach nectar in corollas 4–7 mm deep, but in practice they tend to visit open exposed nectaries in the Apiaceae, Asteraceae, and Rosaceae, and in the autumn they are fairly common on ivy flowers. However, they spend rather longer just “sitting around” on a wider variety of flowers than is required for their feeding, because they use flowers as encounter sites for their prey (bees and other hymenopterans). Hence they may be recorded as visitors on flowers where they are not feeding, and are making almost no contact with anthers.

  2. 2.A few species of tachinid fly (beyond those already mentioned in southern Africa) are moderately long tongued. For example, Siphonia and Prosena both visit small tubular flowers such as Mentha in Europe. Some exceptionally bristly tachinids such as Dejeania also occur on Acacia inflorescences in Africa, apparently probing for both nectar and pollen (pers. obs.).

5. Hoverfly Flower Types

Syrphidae, the hoverflies (or sometimes simply called “flower flies”), are by far the most important flies to be properly equipped for pollen feeding and specifically deriving all or nearly all of their food (as adults and as larvae) from flowers. As such they often rival the bees in importance as pollinators in particular habitats or for particular crops, and they have been better studied than most other flower-feeding flies. They are particularly important in north temperate habitats and on relatively nonspecialist flowers (once again the Apiaceae, the Rosaceae, and many Asteraceae and Brassicaceae); (p.312)

Pollination by Flies

Figure 13.5 Syrphid venation, easily recognized by the false vein and the apparent outer margin formed by the outer cross veins.

thus they are very good pollinators of crops such as rape (Jauker and Wolters 2008). They may take nectar or pollen or both (Gilbert 1981, 1985), in part depending on the flower type and their needs at the time. They show good floral constancy in mixed-array tests and in the field (for example, Melanostoma had on average just 2.7 pollen types in its gut when caught; Hickman et al. 1995), so they have all the key attributes of good pollinators.

Syrphids come in a wide range of sizes, many of the tiny ones being elongate and shiny black or metallic, while the medium to large species are often black and yellow (plate 23B,D,E) or black and red and so are regularly mistaken for wasps. A few are specific mimics of bees: the drone flies in the genus Eristalis (plate 23C) can be remarkably like male honeybees, while the genus Volucella contains excellent bumblebee mimics and can even have morphs within one species, each morph having color bands appropriate to mimic a particular bumblebee type. All syrphids have some covering of hair, which can be branched or even plumose, but these bee-mimic species are especially hairy (in part no doubt to keep up the resemblance) and therefore become particularly good pollen carriers. The mimicry is assumed to be effective in deterring predators, and several hoverflies are readily able to deceive birds into ignoring them as potential prey (Bain et al. 2007). But for human observers it is relatively easy to distinguish hoverflies once they are at rest, as they have just one pair of wings like all dipterans and have extremely standard and rather unusual wing venation (fig. 13.5; plate 23D).

The mouthparts of hoverflies are variable in length (usually 2–4 mm, but up to 5–8 mm in Eristalis and Volucella and 12 mm in Rhingia), but they are reasonably consistent in design, with a more or less elongate rostrum from which emerges a more or less elongate proboscis (made up from the labrum and the hypopharynx) (fig. 13.6). In species with very long tongues, such as Rhingia in Europe (fig. 13.6C), both rostrum and labrum are elongated (unlike most other longer-tongued flies, where the rostrum remains short). The tip of the proboscis expands into a pair of bristly labella, which are used to dab at a flower and pick up superficial pollen (Gilbert 1981). Alternatively, pollen is gathered either by rubbing anthers between the labella, or by inserting the labella into larger anthers and scraping out the pollen. The face and tongue are regularly cleaned with the legs, allowing pollen to be transferred to the mouth and eaten. The labella can be closed together almost as a tube when feeding on nectar in tubular flowers, or spread out over a wider liquid surface in more open flowers. This allows the syrphids to feed on a particularly wide range of flower types.

Gilbert (1981; see also Gilbert and Jervis 1998) analyzed feeding behavior in common European hoverflies. All species took pollen as their main protein source (more so in females, as they have to provision their eggs with substantial protein), and the proportion of pollen taken was roughly reflected in the recorded density of the ridges (pseudotracheae) on the labella surfaces. The more polyphagous genera visiting several sources for pollen (such as Platycheirus, Episyrphus, Sphaerophoria) were shown to be commoner in open habitats, compared with more forest-loving oligophagous types (Branquart and Hemptinne 2000).

Not all hoverflies take in nectar. The smaller types, often with shorter tongues, are mainly pollen feeders (e.g., Syrphus, Episyrphus, and Melanostoma), although others of similar body size have longer tongues with smaller labella and take both nectar and pollen (e.g., Metasyrphus, Platycheirus, and Syritta). Varying amounts of nectar were used in the diets of some medium and all larger species tested (Sphaerophoria, Rhingia, and Eristalis), presumably reflecting their higher energy needs. The largest hoverflies such as Eristalis could fill their crop with nectar in 75–220 minutes depending on the flowers chosen (Gilbert 1983).

As might be expected, hoverfly flowers include a multitude of designs. There is a good correlation between proboscis length and flower depth (Gilbert 1981; fig. 13.7), even though flies with longer tongues can also exploit shallower open flowers. The most favored (p.313)

Pollination by Flies

Figure 13.6 (A) and (B) General syrphid proboscis types in Episyrphus and Platycheirus, and (C) elongated pointed proboscis in the genus Rhingia.

(All modified from Gilbert 1981.)

families are Apiaceae, Asteraceae, Ranunculaceae, Brassicaceae, Caryophyllaceae, and Rosaceae, many of these corresponding with the generalist fly flowers discussed in section 2, Sensory and Behavioral Capacities, above. The range of Asteraceae used is certainly extended for the hoverflies, with more of the longer-corolla flower species coming into the frame; syrphids regularly visit hawkbit (Leontodon), hawkweed (Hieracium), and dandelion (Taraxacum). Gilbert and others have also reported a strong propensity to visit the (normally wind-pollinated) flowers of grasses (Poaceae) and of plantains (Plantago), especially for two very common genera, Melanostoma and Platycheirus. On open flowers such as these, the timing of hoverfly foraging depends in part on size and coloration as discussed in chapter 10 (figs. 10.9 and 10.10), with a particular tendency to activity in cooler weather in the large and hairy drone flies (Eristalis), as these have some endothermic ability.

For the medium- and long-tongued syrphids, a further range of plants beyond these generalist families are exploited. Some of the smaller zygomorphic flowers from the families Lamiaceae and Scrophulariaceae (such as Stachys, Glechoma, and Ajuga) are especially valued by such flies, which feed on them much more efficiently than can other flies; they approach in an appropriate direction and handle the relatively complex morphology of the flower rather easily, unlike muscids and calliphorids, which seem to visit more randomly. Other preferred flowers include smaller legumes such as melilot (Melilotus) and clover (Trifolium), and varieties of scabious (Knautia and Scabiosa). Extraordinarily, members of the genera Volucella and Eristalis that mimic bees also manage to mimic their habits of buzz pollination on some of the classically sonicated flowers (see chapter 7).

A few plants are sometimes regarded as having more specialist hoverfly flowers (Kugler 1938). Many of these share a particular arrangement of paired sideways-spreading stamens set at a slightly higher level than the central and slightly downwardly directed stigma (fig. 13.8), as seen in some species of Veronica (speedwell), and in enchanter’s nightshade (Circaea). When a hoverfly grasps the stamens to feed, they droop slightly under the weight, and the underside of the insect body contacts the stigma. Both these plants are (p.314)

Pollination by Flies

Figure 13.7 Correlations of syrphid tongue lengths with average corolla depth of flowers visited for nectar (A), and with percentage of nectar taken in the diet (B). 1, Syrphus ribesii; 2, Metasyrphus corollae; 3, Episyrphus balteatus; 4, Melanostoma; 5, Platycheirus; 6, Syritta; 7–9, Eristalis spp; 10–11, Sphaerophoria spp.

(Redrawn from Gilbert 1981.)

common in the shady moist habitats of woodland, where appropriate smaller-bodied hoverflies such as Melanostoma, Baccha, and Syritta also occur (and where similarly sized bees that could also work the flowers are rather uncommon). Another rather specialist example is the slipper orchid Paphiopedilum villosum, which is almost exclusively visited by syrphids, lured in by glistening staminodes and an apparent perch to land on, as well as a urine-like scent; this is pollination by deceit, as in attempting to land the flies slide off into a trough and can only escape (unrewarded) by squeezing out past the pollinia (Bänzinger 1996). (p.315)

Pollination by Flies

Figure 13.8 Flower forms said to be typical for hoverflies, with paired high stamens and a downward-pointing stigma.

(Drawn from photographs.)

For the really long-tongued hoverflies, favored flowers include red campion (Silene), some geraniums, common bluebells (Hyacinthoides), the bindweeds (Convolvulus spp.), and some of the small to medium balsams (Impatiens). Rhingia is particularly adept at feeding on nectar from common bindweed in hedges and extending its attention to ornamental forms growing in gardens and is also a regular visitor to forget-me-nots and lungworts.

It should be evident from this discussion that hoverfly flowers overlap very substantially with any listing of bee flowers. It is reasonably common to find hoverflies as main pollinators on bee flowers in regions or at times where bees are relatively scarce, as in the moist woodlands mentioned above, or in winter in grasslands of the subtropics, where hoverflies have been reported to take over as pollinators of flowers such as Sisyrinchium (Freitas and Sazima 2003). In recent years, with a scarcity of honeybees in many areas (see chapter 29), there have been marked increases in hoverfly numbers, especially of the ubiquitous and almost worldwide Episyrphus balteatus.

Hoverflies also have sensory and behavioral attributes that are rather bee-like and accentuate their importance as pollinators. Their color and shape preferences are attuned to their being flower visitors; in laboratory trials several showed a clear preference for yellow flowers, or yellow centers, and smaller types such as Episyrphus chose smaller rather than larger flower models (Sutherland et al. 1999). A strong bias for yellow is accompanied by poor discrimination of either blues or deep reds from grays. Additionally they are “clever” flower visitors, with good associative learning. Many have an excellent ability to learn spatial landmarks, which links to male territoriality, one individual returning to hover in the same sunny patch or woodland edge day after day. Hoverflies can handle complex flower morphologies with considerably more facility than most other insects and can deal with zygomorphic corollas quickly and easily. In addition, they can work systematically around the florets of composite flowers (fig. 13.9), “counting off” a full circuit and then leaving (Gilbert 1983). Crucially, the hoverflies also tend to show a high degree of flower constancy. Studies with mixed floral communities showed very different but highly consistent flower choices made by Eristalis and Helophilus (Parmenter 1958), while Kugler (1950) revealed that individual constancy occurred, different individuals of Eristalis tenax being faithful to quite different flower species on a given day.

6. Carrion-Fly Flower Types

These flowers practise deceit pollination, and flies are very commonly involved. In essence this is a form of brood-site mimicry, covered more generally in chapter 23. The flowers mimic animal carcases and carrion, the preferred egg-laying site of various kinds of fly whose larvae require dead or decaying flesh as food; they attract in the adult flies but usually offer no rewards. The technical term for this syndrome is sapromyophily (p.316)

Pollination by Flies

Figure 13.9 The hoverfly Eristalis tenax appears able to “count” a circuit when foraging on Aster flower heads, with the majority of individuals completing a 360° turn and then leaving the flowers.

(Redrawn from Gilbert 1983.)

(although something similar also occurs with dung beetles, when it is termed coprocantharophily; chapter 12). A closely related brood-site mimicry is found in some flowers that resemble the gills of fungi, attracting visits by egg-laying flies, and termed mycetophily; here the best-known examples involve fungus gnats (very small nematoceran flies in the family Mycetophilidae). Within the Saxifragaceae, a fungus-gnat pollination syndrome with unusual saucer-shaped flowers has evolved repeatedly (Okuyama et al. 2008).

Members of the family Araceae (the aroids) are best known as carrion flowers, but examples also occur in Aristolochiaceae, Apocynaceae/Ascelpiadaceae, Taccaceae, and Orchidaceae. Some examples are relatively simple, while others involve complex trapping mechanisms. Various asclepiads use simple brood-site mimicry, a well-known example being Stapelia: the large flowers have reddish or purplish corollas and distinctive patterns of hair on the petals, increasing the resemblance (both visual and tactile) to dead animal surfaces. Most strikingly, the flowers are strongly and unpleasantly scented; volatile profiles were shown in table 6.2 (Jürgens et al. 2006). They attract a range of muscid and calliphorid flies, which lay eggs on the flowers and in the process get the typical asclepiad pollinaria (chapter 7) stuck on their feet. Some other asclepiads (e.g., Tavaresia) enhance their attraction to flies by incorporating motile structures inside (or at the mouth of) their flowers, such as hairs or filamentous tissues that constantly move or vibrate in the slightest breeze; similar oscillating structures occur in some Ceropegia species and in a few orchids.

Rafflesia, a genus including the world’s largest flower, also fits in here. Like its close relative Rhizanthes, the Rafflesia plant occurs in the shaded under-story of Asian forests, growing as a parasite on tree roots and with only its enormous reddish-brown flowers visible above ground level (plate 22G,H). Both genera emit volatiles and some carbon dioxide and have a degree of thermogenesis (Patino et al. 2002), all helping to attract the blowflies such as Lucilia that act as pollinators (Beaman et al. 1988). Flies seek to access the enticing “flesh” by entering anther grooves with hair-lined ridges that guide them precisely, so that the viscous pollen matrix is deposited on their backs; then the flies squeeze into female flowers under a ring of stigmatic tissue where pollen is rubbed off. Figure 13.10 shows the architectural features involved.

The genus Tacca is also worth mentioning; again it occurs in Asian forests. Widely referred to as the “bat flower” from its shape, but nectarless and with elaborate filiform appendages in dark purple or almost black colors and strong decaying odors, this is again fly visited (albeit at low frequency, with selfing being common; Zhang et al. 2005; and see Fenster and Martén-Rodriguez 2007).

Examples of trapping systems in carrion flowers are described in chapter 23, so here we concentrate only on the floral features linked to fly attraction. Examples include Aristolochia, where the corollas are (p.317)

Pollination by Flies

Figure 13.10 Rafflesia structures: (A) general cutaway view; (B) blowfly feeding on male structures under the rim of the diaphragm; (C) closeup of male structures, with channels leading to the anthers dispensing a viscous pollen mix.

(Modified from Endress 1994, based on earlier sources.)

typically tubular but strongly protogynous so that they depend on attracting flies already covered in pollen (Brantjes 1980). The flowers have expanded petal lobes, often greenish or mottled with purple and white, and with a long tail (or sometimes several shorter tails around the edge of the petals), all providing visual attraction (fig. 13.11 and plate 22A). They emit strong carrion smells, often intensely over just a few hours, and these are sometimes localized into the petal tails which act as osmophores. The base of the corolla (containing a central cone of stout styles and anthers) secretes a little nectar with a high amino acid content and is also transparent so it appears as a window, attracting the flies down to the reproductive organs in pursuit of food and a way out. For the small Eurasian species, the pollinators are mainly small nematoceran flies, especially biting midges or, in the case of A. pallida, male phorids (scuttle flies) (Rulik et al. 2008). For the larger and more complex South American Aristolochia flowers, a whole variety of fly genera are attracted, although only a small range (usually sepsids, muscids, and calliphorids) are actually trapped by any one species. There is rather good specificity (and little overlap) between flower species and fly genera. These New World Aristolochia species often have a U-shaped corolla, and are called “Dutchman’s pipes” because of their form (fig. 13.11B).

In the Asclepiadaceae the highly variable genus Ceropegia, occurring throughout the southern continents, provides all the major examples of carrion fly flowers (Vogel 1961). Here again the corolla is long and tubular, commonly green/grey, with the petal lobes converging and usually uniting at their tips to produce a lanternlike structure (fig. 13.12 and plate 22B,C). The flower may also have a paler window area basally, around the sexual organs and nectaries. Ceropegia species usually lack the purple fleshy external appearance and the strong decaying scents of other carrion flowers, instead having quite delicate scents. They attract a range of small flies with fairly good specificity. The flies pick up pollinia on the underside of their heads or mouthparts while drinking nectar and may deposit them into grooves adjacent to the nectaries in a subsequent flower. (p.318)

Pollination by Flies

Figure 13.11 (A) Various Aristolochia flower structures (redrawn from Endress 1994). (B) New World Dutchman’s pipe type, in front view and transverse slice (redrawn from Proctor et al. 1996 and from flowers).

Pollination by Flies

Figure 13.12 A variety of floral forms in Ceropegia species: (A) C. ampliata; (B) C. distincta haygarthii; (C) C. sandersonii; (D) C. robynsiana; (E) C. stapeliiformis. Scent-producing areas are black, and waxy or slippery surfaces are stippled.

(Redrawn, not to scale, from Vogel 1961.)

(p.319)

Pollination by Flies

Figure 13.13 Structures of typical saprophytic aroid inflorescences: (A) and (B) external view and transverse section of Cryptocoryne; (C) internal view of spadix of Arum (A–C redrawn from Proctor et al. 1996); (D) the main volatiles emitted by common Arum species.

In Europe it is primarily the Araceae, and specifically the genus Arum, that provide carrion fly-trap examples (Meeuse and Morris 1984). Many of these aroids smell strongly of decaying meat, with dark purplish-brown and often hairy surfaces. They have unusual inflorescences with a central club-shaped spadix and an outer leafy spathe (fig. 13.13) that together take over all the attractive functions, and either of these structures may be expanded into long tails. Inside the resulting upright inflorescence tube, the flowers exist in single-sex arrays, the females (little more than an ovary with a flattened stigma on top) being at the base of the spadix and the male flowers (merely paired stamens) in a ring just above this, both protected deep within the spathe cavity. In the familiar European Arum maculatum (lords and ladies or cuckoo pint), and the similar Mediterranean Arum nigrum, the spathe opens during the night, the stigmas mature, and the spadix emits a strong fecal odor from dawn onward, composed of ammonia, ethylamine and diethylamine, putrescine, indoles, and skatole (fig. 13.13D; and see chapter 6). Dung and flesh flies and varied small nematoceran flies may arrive in considerable numbers over the next few hours, drawn in from a distance by the scent and at closer range by the colors and sometimes by the waving tails. In A. maculatum a high proportion of the insects that effect pollination are small flies in the owl-midge family (Psychodidae) (Lack and Diaz 1991), while in Asian species a range of biting midges (Ceratopogonidae) and blackflies (Simuliidae) have been recorded.

One odd feature of most kinds of aroid is their (p.320) substantial heat generation during flowering. This was at one time thought to be an attractant, inducing flies to enter the spadix voluntarily; but in practice there is no doubt that the flies fall in accidentally, and are not attracted to warmth per se. It seems likely that the heat produced in the spadix by chemical thermogenesis is mainly helpful in rapidly vaporizing the volatile scents as they are secreted from the plant’s tissues (Meeuse 1966). Similar high levels of heat production have been reported in various Ceropegia and Aristolochia species.

From these descriptions of examples from three key families, it is not difficult to identify key convergent features of these flowers.

The Sapromyophilous Syndrome

  1. 1.Large tubular flowers with spreading upper corolla, often growing close to the ground

  2. 2. Dull red, purple, brown, or sometimes greenish coloration, often with mottling

  3. 3. Petal surfaces with hairs and often with longer tail-like structures

  4. 4. Strong unpleasant scents, mimicking dead or decaying flesh or excreta, with vaporization sometimes aided by thermogenesis

  5. 5. Window effects from translucent corolla bases

  6. 6. Abundant pollen, little or no nectar (amino-acid-rich where present, perhaps to sustain the fly until it meets and is trapped by its next flower)

  7. 7. May have trapping mechanisms (downward-pointing hairs, slippery papillate surfaces, rings of protective bristles, constrictions, overhangs; chapter 23 gives details)

  8. 8. May have release mechanisms (withering of hairs, relaxation of constrictions, or change of floral orientation from pendant to horizontal)

  9. 9. Strongly protogynous 10. Relatively short lived, often 2–4 days

Orchids can readily be found that fit within this same syndrome, in both Old and New World floras. Red or brown flowers and foul odors occur in various Bulbophyllum species, on which flies alight and crawl toward the middle, finding themselves tipped rapidly toward the central column when they try to grip the orchid labellum, which is a finely balanced spring mechanism. Different species of Bulbophyllum exploit different flies, each being “sprung” by a different weight of visitor. Similar mechanisms occur in some Neotropical Masdevallia, which lure in flesh flies by color and odor and offer no reward (Dodson 1962).

7. Some Other Specialist Cases

Various gall midges are known to have relatively specialist interactions with flowers. For example, Schisandra is pollinated specifically by female Megommata midges (Cecidomyidae), the females unusually eating the pollen as a major part of their diet (Yuan et al. 2007). Cocoa flowers (Theobroma) are also routinely pollinated by cecidomyid midges (Young 1985; chapter 28). More unusually, the monoecious tree Artocarpus integer is pollinated by gall midges, but here a fungus that infects the male flowers is crucial to the interaction (Sakai et al. 2000), as the midges eat the fungal mycelium while ovipositing on the flower and picking up pollen, then transfer this to (uninfected) females presumably because of an odor-based sexual mimicry.

Fungus gnats, as well as engaging in deceit pollination with flowers that resemble their oviposition sites, have rather specialist interactions with a range of spring-flowering woodland plants such as Tolmeia (Saxifragaceae), where larger flies and bees are ineffective and act merely as pollen robbers on male-phase plants (Goldblatt et al. 2004).

Orchid pollination is also sometimes effected by flies other than carrion types. Male mosquitoes visit Habenaria in North America (Thien 1969), and various nematoceran flies work the flowers of the genus Pterostylis. Tachinid flies pollinate an Andean orchid, Trichoceros antennifera.

8. Overview

From a worldwide perspective, flies are second only to bees in their importance as flower visitors, often making up for their relatively poor pollen-carrying capacities by their sheer abundance (Larson et al. 2001). They may also be less rigorous visitors and make visits to fewer flowers per plant, so producing less geitonogamy, and they show reduced grooming so that less pollen may be wasted from the plants’ point of view. Anthophilous flies probably do not get their fair share (p.321) of attention in the pollination literature. They may be at least as important as bees in some tropical and semiarid zones and are often more important on some islands where bees are uncommon (including large islands such as New Zealand), and especially in the cold high-latitude and high-altitude habitats considered in chapter 27.

However, the details given in this chapter should make it evident that there is not one fly pollination syndrome (myophily) but several. Most flies could best be included within the generalist syndrome described in chapter 12, and it is these for which the term “myophily” is most often used (and see table 11.1). But there could also be grounds for regarding the long-tongued flies of southern Africa, and perhaps even more so the carrion flies, as representing additional syndromes in their own right. Furthermore, the hoverflies (and a few other groups) are distinctly more specialist than the majority of flies, and in many respects their flower-visiting choices are allied closely with the characteristics of bee pollination discussed in chapter 18. In these last three syndromes—long-tongued flies, carrion flies, and hoverflies—quite specialist and efficient pollination relationships have developed, with good constancy, good pollen carriage, and potentially rather high pollination efficiencies.