Flies and flowers: taxonomic diversity of anthophiles and pollinators

Flies and flowers: taxonomic diversity of anthophiles and pollinators

BMH Larson Department of Ecology, Evolution and Marine Biology, University of California - Santa

Barbara, Santa Barbara, California, United States of America 93106

PG Kevan' Department of Environmental Biology, University of Guelph, Guelph, Ontario,

Canada NlG 2W1

DW lnouye Department of Zoology, University of Maryland, College Park, Maryland,

United States of America 20742

The Canadian Entomologist 133: 439 - 465 (2001)

Abstract-The Diptera are the second most important order among flower-visiting (anthophilous) and flower-pollinating insects worldwide. Their taxonomic diversity ranges from Nematocera to Brachycera, including most families within the suborders. Especially important are Syrphidae, Bombyliidae, and Muscoidea. Other families, especially of small flies, are less appreciated and often overlooked for their associations with flowers. We have compiled records of their flower visitations to show that they may be more prevalent than usually thought. Our knowledge of anthophilous Diptera needs to be enhanced by future research concerning (i) the significance of nocturnal Nematocera and acalypterate muscoids as pollinators, (ii) the extent to which the relatively ineffective pollen-canying ability of some taxa can be compensated by the abundance of individuals, and (iii) the role of Diptera as pollinators of the first flowering plants (Angiospermae) by using phylogenetic and palaeontological evidence. Specializations in floral relationships involve the morphology of Diptera, especially of their mouthparts, nutritional requirements, and behaviour, as well as concomitant floral attributes. The South African flora has the most highly specialized relations with dipterous pollinators, but in arctic and alpine generalist fly-flower relations are important in pollination and fly nutrition.

Larson BMH, Kevan PG, Inouye DW. 2001. Des mouches et des fleurs : diversit6 taxonomique des anthophiles et des pollinisateurs. The Canadian Entomologist 133 : 439465.

R e s u m G L e s diptkres occupent le second rang au monde parmi les ordres d'insectes qui visitent les fleurs (anthophiles) et qui assurent la pollinisation. Leur diversit6 taxonomique va des nCmatockres aux brachyckres et inclut presque toutes les familles de ces sous-ordres, en particulier les Syrphidae, les Bombyliidae et les Muscoidea qui occupent une place prepondtrante. Les associations des autres familles avec les fleurs, particulikrement les familles de mouches de petite taille, passent souvent inaperpes. Nous avons compilC des donnees sur leurs visites aux fleurs dans le but de dCmontrer qu'elles sont probablement plus importantes qu'on ne le croit. Nos connaissances des diptkres anthophiles doivent &tre complCtCes par d'autres recherches (i) pour dkterminer l'importance des nematockres nocturnes et des muscoi'des acalyptkres comme pollinisateurs, (ii) pour Cvaluer jusqu'h quel point l'inefficacite relative de certains taxons comme transporteurs de pollen peut Ctre compensCe par I'abondance des individus et (iii) pour juger du r61e des diptkres comme pollinisateurs des premikres plantes B fleurs (Angiospermae) en utilisant des

' Author to whom all correspondence should be addressed (E-mail: [email protected]).

440 'WE CANADIAN EN~DMOLOGIST JulyIAugust 2001

donnCes phylogCnCtiques et palContologiques. Les spCcialisations de relations fleurs-insectes sont basCes sur des particularitCs morphologiques des diptbres, sur- tout de leurs pibces buccales, sur leurs besoins nutritifs et sur leur comportement, en meme temps que sur les attributs correspondants des fleurs. La flore de 1'Afrique du Sud est celle qui a les relations les plus spCcialisCes avec les diptbres pollinisateurs. Cependant, dans les rCgions arctiiues e; alpines, des relations app&emrnent non svCcialisCes entre les mouches et les fleurs sont im~ortantes Dour la vollinisation des fleurs et l'alimentation des mouches.

[Traduit par la RCdaction]

Introduction

Anthophilous (flower visiting) insects are diverse, ranging from Collembola to Hymenoptera (Kevan and Baker 1983, 1999). In flowers, insects seek food rewards such as nectar (such flies are designated nectarophagous), pollen (pollenophagous flies), floral tissues, or other rewards such as shelter, mates, and oviposition sites. Although bees (Hymenoptera: Apoidea) are widely recognized as the most important anthophiles and pollinators, flies (Diptera) certainly rank second and display all the above behaviours on flowers. The commonness of Diptera as flower visitors has been noted since the middle of the 19th century. The classic reviews of Muller (1883) and Knuth (1909-1912) list a diverse fauna of anthophilous Diptera. Willis and Burkhill (1895-1908) expanded on those records, and Drabble and Drabble (1917, 1927) recorded 123 species of flies as visitors to 35 species of British flowers. Parmenter (1958, 1961) also recorded the flies that visit flowers of many British plants and noted that about three quarters of the anthophiles observed by Willis and Burkhill were flies. More recently, Proctor and Yeo (1973) and Proctor et al. (1996) have summarized the lists of those earlier workers and, along with Kevan and Baker (1983, 1999), have briefly reviewed flower visitation by Diptera. Other authors have considered the importance of Diptera in the origins of the coevolutionary relationships of flowering plants (Angiospermae) and insects (Willemstein 1987; Labandeira 1997, 1998a, 1998b; Ren 1998). Nevertheless, a comprehensive review of the diversity of anthophilous Diptera, and their roles in pollination, hitherto has not been undertaken.

In this paper we survey the large body of literature about flower visitation and pollination by families of Diptera. To provide an exhaustive review of records in the entomological, botanical, ecological, and other relevant literature would be a daunting task. We discuss the prevalence of flower visitation (and, when possible, feeding and pollination) by flies, with classification and common names following McAlpine et al. (1981) and Borror et al. (1989). One of us (DWI) is compiling an inclusive database of anthophilous flies: fly visitors to over 555 plant species have been compiled so far. Flower-visitation records are noteworthy and form the basis of much of our survey, but future workers should attempt to assess more critically the effectiveness of visitors as pollinators.

Pollination by Diptera, referred to generally as myophily (see Muller 1883; Knuth 1906-1912; Faegri and van der Pijl 1979), includes sapromyophily, or pollination by at- traction of carrion and dung-feeding flies. The immense diversity of Diptera as anthophiles and pollinators suggests that "myophily" is too broad a term to be useful in categorizing syndromes, or suites of characters of flowers with respect to their pollination relationships, and that even "sapromyophily" includes several suites of floral characters that show only a little functional overlap.

Flower visitation and the ability to carry pollen do not qualify an anthophile as a pollinator (Kevan and Baker 1983, 1999; Lindsey 1984). For an anthophile to be an effective pollinator, it must visit flowers in such a way as to transfer pollen regularly from

Volume 133 THECANAnlAN ENTOMOLOGIST 44 1

anthers to stigmata, whether between plants (xenogamy), between flowers on the same plant (gietenogamy), or within the same flower (autogamy) [see Richards (1986) for de- tails on plant breeding systems] within the period of viability of the pollen grains they carry (Kevan 1972). Many early works on the relationships between insects and flowers have simplistically equated flower visitation with pollination. Flower visitors that do not regularly transfer pollen serve little purpose in the reproduction of the plant, even though they may be variously specialized for flower feeding (Pont 1993). Although some anthophilous Diptera are not pollinators, or at best equivocally so, the significance of floral resources in the lives of flies is well known. Nectar, mostly solutions of sugars, is fuel for flight and other activities, and pollen is highly nutritious for its ni- trogenous, carbohydrate, lipid, vitamin, and mineral constituents and apparently is used in sexual maturation and bodily maintenance. Some flies bask in flowers, some mate there, and others oviposit on them. Demonstrating that an anthophile is a pollinator re- quires careful experimentation and observation and, recently, methods for assessing the efficacy of pollination by anthophiles have been developed (see Kearns and Inouye 1993). Throughout this review we have noted, whenever possible, Diptera proven as pollinators.

Our intent is to write a series of review articles. In this review, we document the taxonomic diversity of Diptera as anthophiles and pollinators and summarize their relationships with, and other activities on, flowers. With that as background, the second review will focus on the nature and diversity of floral attractants and rewards, and their importance in the lives and bionomics of flies. In the third review, we will describe how those attractants and rewards are used in the foraging of Diptera at flowers. We will synthesize, in the fourth review, the coevolutionary principles linking Diptera to Angio- sperms and redefine floral syndromes (suites of floral characters that indicate pollination relationships) as they relate to flies.

The long-horned flies (suborder Nematocera)

Most flies of these families are characterized by primitive suctorial and lapping mouthparts and a short proboscis, which generally restricts them to open flowers with exposed nectar and to flowers with short tubular corollas (e.g., Apiaceae, Euphorbiaceae, Rosaceae, Saxifragaceae, Brassicaceae, and some Asteraceae). In general, Nematocera are probably less important as pollinators than their visitation fre- quency might suggest, but the suborder contains many nocturnal species, and observations of flowers at night are needed because these may greatly increase our rec- ognition of their prevalence as anthophilous Nematocera (e.g., Willemstein 1987). Their ancient origins and need for nectar as a carbohydrate fuel for flight have placed them as contenders for early pollinators of primitive Angiospermae (Willemstein 1987).

Thirteen families of Nematocera are known, to some extent, as anthophiles (Ta- ble 1). Most are small nectarophages, but despite historical statements of their inefficiency as pollinators because of their small size and inconstancy, some families (e.g., Mycetophilidae and Culicidae) are often significant pollinators. Mycetophilidae are often in great abundance and are noted as having hairy bodies well suited to carrying pollen and as important pollinators of Aristolochiaceae in forests in Japan and California (Table 1). Pollination has been confirmed also in the families Bibionidae, Cecidomyiidae, Ceratopogonidae, and Psychodidae (Table 1). In Central America, some cecidomyids (e.g., genera Clinodiplosis and Mycodiplosis) are thought to be, with some Ceratopogonidae, natural pollinators of cacao [Theobroma cacao L. (Sterculiaceae)] because of their flower-visiting behaviour, elongate and functional mouthparts, pollen- trapping legs, and abdominal hairs (Young 1985). Among the Cecidomyiidae are those

142 TliECANAI>IAN ENTOMOLOGIST July/Aug~st 2001

which Feil (1992) describes as pollinators of dioecious species of the genus Siparuna (Monimiaceae). The specialized flowers are enclosed by a velum (floral roof) with a small pore, which is larger in the male flowers than in the female ones. Female gall midges can lay eggs through the pore in the male flowers (and their larvae develop on the floral tissues) but not in the female flowers because their abdomens usually cannot fit through the pore to lay eggs. Pollination is effected because the midges pick up pollen on their abdomens while laying eggs in male flowers and then transfer it to the exserted stigmas of the female flowers while attempting to lay eggs there.

Moth flies (Psychodidae) are well known as pollinators of "Lords and Ladies" (Arum maculatum L.) in Britain (Table 1). In particular, females of Psychoda phalaenoides L. are attracted by the stench emitted by the spadix. Landing on the spathe, they crawl down into a basal chamber where they are trapped by downward- projecting hairs. The plant is protogynous, so the stigmas on the basal portion of the spadix are mature at this time, and they receive any pollen from the arriving midges. The next day, the stench abates, the stigmas wither and secrete a small drop of nectar, and the anthers mature and shed pollen onto the midges. Withering of the trap hairs al- lows the midges to escape and possibly repeat the process at another flower to effect cross-pollination. It is probable that psychodids and other Nematocera are pollen vectors for other aroids and sapromyophilous "trap" flowers, such as some orchids (e.g., van der Pijl and Dodson 1966).

In the Culicomorpha, the sometimes highly elongate biting mouthparts of mosquitoes, black flies (Simuliidae), and biting midges (Ceratopogonidae) are hypothesized to have first arisen as a means of reaching nectar at the base of tubular corollas (e.g., Willemstein 1987). Mosquitoes (Culicidae) are common flower visitors, mostly recorded as nectarophages, but they have been invoked as pollinators, especially in Arctic regions (Table 1). There is a comprehensive literature concerning the transfer of pollinia of the nearctic boreal orchid Platanthera (Habenaria) obtusata (Banks ex Pursh) Lindley by attachment of the viscidium to the eyes of females of various species of Aedes as they probe for nectar (Table 1). In all the aforementioned cases, the abundance of the mosquitoes may compensate for their low effectiveness as individuals.

Although many midges (Chironomidae) do not feed as adults, some species feed on exposed nectar (Table 1). There is little information on flower relations of midges. Smittia velutina (Lundbeck) is an abundant High Arctic species that can carry pollen, but its effectiveness as a pollinator is unknown. Kevan (1970) suggested that, although they move around, apparently following the warmth of the sun or sheltering beneath flowers in rain (Kevan 1970, 1989, 1990), they may visit only one inflorescence or plant in their short lifetimes and so be insignificant as pollinators on obligately out- crossing plants, such as Saxifraga oppositijolia L. and Salix spp. (Kevan 1972).

The short-horned flies (suborder Brachycera)

In addition to unspecialized flies able to exploit only exposed nectar and small, tubular flowers, the Brachycera contains additional families with elongate proboscides and the ability to exploit flowers with deep tubes and hidden nectar. The Brachycera: Orthorrhapha have been invoked as having had important pollination relationships with Angiospermae since their origins in Jurassic time (Ren 1998; Labandeira 1998a, 19983; Grimaldi 1999).

Horse and deer flies (Tabanidae) often visit flowers (Table 1). Blood feeding in the females may have arisen secondarily after the evolution of longer mouthparts for nectar feeding, but this is debatable (e.g., Downes 1958; Oldroyd 1964; La11 and Davies

Volume 133 THE CANADIAN ENTOMOLOGIST 443

1971). Tabanidae are important flower visitors in pollination sytems in South Africa (Goldblatt and Manning 1999, 2000; Goldblatt et al. 2000, 2001).

Snipe flies (Rhagionidae), athericid flies (Athericidae), soldier flies (Stratiomyidae), robber flies (Asilidae), flower-loving flies (Apioceridae), stiletto flies (Therevidae), and mydas flies (Mydidae) are all known to be anthophiles. The endan- gered species Rhaphiomidas terminatus abdominalis Cazier is known as the Delhi Sands flower-loving fly, even though it is a mydid, but little is known of the importance of flowers in its life (see Kingsley 1996). Their relationships with flowers may be more important than the sparse literature suggests, especially when the Stratiomyidae and Apioceridae (Toft and Kimsey 1982) are considered (Table 1). Some small-headed flies (Acroceridae or Cyrtidae), a family characterized as having long proboscides, are known to be sometimes nectarophagous and even bee mimics (Goldblatt et al. 1997) (Table 1). Some may be pollenophagous, as Holloway (1976) inferred from the yellow faeces of Ogcodes brunneus (Hutton). This species' palynophilic hairs suggests that it can effect pollination, as indicated for other species of Acroceridae (Table 1).

Descriptions of anthophily and pollination by tangle-veined flies (Nemestrinidae), with their strong similarities to long-tongued tabanids, bombyliids, and some syrphids, come especially from southern Africa (Table 1) (Goldblatt and Manning 1999, 2000; Goldblatt et al. 2000, 2001). This pollinator assemblage of long-tongued flies led Vogel (1954, pp 68-75) to cast it within the parallel context of the floral syndromes, psychophily (butterfly pollination), and sphingophily (pollination by sphinx moths).

Bee flies (Bombyliidae) are one of the best known families of anthophiles. With specialized, elongate (but nonretractable) proboscides, they are conspicuous nectarophages. Some species have special adaptations for eating pollen (Table 1). In their hovering and penchant for flowers they resemble bees and hover flies, and they are likewise eminent pollinators.

Of the Empidoidea, the dance flies (Empididae) are more frequently recorded as flower visitors than are long-legged flies (Dolichopodidae), which infrequently visit flowers. With long, piercing mouthparts, the predaceous dance flies are well equipped for nectarophagy (Table 1). Their roles as pollinators have not been well investigated (Table l), but Kevan (1972, 1973) records species of Rhamphomyia Meigen foraging in two positions that would cause pollination. On flowers, especially of Dryas integrifolia Vahl (Rosaceae) in the Arctic, the flies dip to imbibe nectar such that their bodies are between the stamens and pistils and their nota touch the anthers and become dusted with pollen while their venters rub on the stigmata. In the other position, they dip such that their nota touch the stigmata and their venters touch the anthers and become dusted with pollen. Pollination is thus effected. The long-legged flies are also predators, but have short and rarely tubular mouthparts, so they can forage only from flowers with exposed nectar (Table 1).

Of the Diptera: Cyclorrapha, recent reviews indicate that flower visiting by hump- backed flies (Phoridae) has been underestimated in the past (Baumann 1978; Disney 1980) (Table 1). In fact, they are becoming more commonly reported as pollinators of a wide variety of plants and it is hypothesized that they are essential to pollination of plants in tropical forest understories (Baumann 1978; Young 1984b) (Table 1).

The flower flies or hover flies (Syrphidae) are probably the most significant anthophilous Diptera, and their abundance at flowers is well known (Table 1). They commonly hover about flowers, from which they collect nectar or pollen or both. Syr- phids with relatively short proboscides can obtain nectar from the open flowers of various families of plants, and species with longer mouthparts also feed on deep tubular flowers (Table 1). Pollen is required by female syrphids for normal ovarian development (Schneider 1948, 1969; Maier 1978) and possibly by males to initiate sperm production (e.g., Kevan 1970), and there have been numerous studies concerning pollen

444 THE CANADIAN ENTOMOLOGIST J u ~ Y / A u ~ u s ~ 2001

foraging by syrphids (Holloway 1976; Haslett and Entwistle 1980; Gilbert 1981; Haslett 1989; Arruda and Sazima 1996). Although some syrphids eat pollen directly, others clean pollen attained while foraging for nectar from palynophilic hairs on their bodies (Holloway 1976). Pollen-foraging hover flies are common on purported anemophiles (wind-pollinated plants) (Table 1).

Although Robertson (1924) felt that the importance of syrphids as pollinators was greatly exaggerated, recent studies from the tropics to High Arctic and alpine barrens have shown otherwise (Table 1).

Acalyptrate muscoid flies

Most of the 50 or so acalyptrate families are rarely recorded visiting flowers, and the few anthophilous families have simple, lapping mouthparts that restrict them to exposed nectar sources (Table 1); however, it is likely that these tiny insects are overlooked (Oldroyd 1964) and that they may be more common as flower visitors and more significant as pollinators than presently thought. In many cases, the feeding habits of the adults are not well known (e.g., Willemstein 1987). Lauxaniid flies (Lauxaniidae) and pomace flies (Drosophilidae) have been reported as pollinators of primitive angiosperms (Table I), indicating that acalypterates may have been involved in pollination of the first angiosperms (Thien 1980; Lorence 1985; Kato et al. 1995; Ren 1998; Labandeira 1998a, 1998b). Drosophilidae have been associated with pollination of Genoplesium (Orchidaceae) in Australia (Bishop 1996 and see Chloropidae). In three- kingdom symbioses, Drosophilidae and sympatric Nitidulidae (Coleoptera) are also known to vector yeasts between flowers of many Convolvulaceae, Hibiscus, and other plants that possess campanulate flowers in the Nearctic, Neotropical, and Australo- Pacific regions (Lachance et al. 2001). The nature of the ecological interactions is probably quite complex.

Deceptive trap flowers are often pollinated by acalyptrate families that normally oviposit in dung, carrion, and other decaying matter (Table 1).

Calyptrate muscoid flies

The calyptrates are generally larger and hairier than the acalyptrates, so they are more effective as pollen vectors and pollinators, although they are not as specialized for nectar and pollen feeding as the bee flies and hover flies. They generally have lapping labella suited for obtaining nectar from open flowers and capitula.

Although most anthomyiid flies (Anthomyiidae) are generalist flower visitors, the group contains highly specialized, even exclusively, myophilic relationships (Table 1). The four species of the seed parasite of the genus Chiastocheta Pokorny which are the exclusive pollinators of their obligate host, the globeflower (Trollius europaeus L.), are being studied as presenting parallel phylogenies and mutualism with a view to elucidat- ing basic coevolutionary principles (Pellmyr 1989, 1992). Some anthomyiids are pollenophagous, and this activity may relate to ovarian maturation (see also Syrphidae) (Kevan 1970). Also, in feeding on nectar they assume the same paired positions on the flowers as do Rhamphomyia spp. (Empididae) (see earlier in the paper) and would effect pollination (Kevan 1970, 1972, 1973).

Flesh flies (Sarcophagidae) and dung flies (Scathophagidae) are occasionally reported as anthophilous, but may be more prevalent than presently thought. Some sarcophagids and scathophagids may be pollinators, but their true roles have not been well elucidated (Table 1). Flies of the genus Scathophaga are often recorded on flowers where they seek prey and feed on floral resources (Kevan 1970; Proctor et al. 1996).

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Blowflies (Calliphoridae) are well known as anthophiles (Table 1) and nectarophages. They are important as pollinators in various and special settings. For ex- ample, they are readily attracted to the decaying smell of many sapromyophilous flowers [such as Raflesia (Rafflesiaceae)] in Malaysia (Beaman et al. 1988; Bbziger 1991) which they pollinate, and they are one of the groups of Diptera considered responsible for pollination of understory palms (Arecaceae) in the tropics (Henderson 1986). Along with muscid flies (Muscidae), they frequent the flowers of mangrove, Avicennia oficinalis L. (Avicenniaceae), in India (Raju 1990). They are natural and important pollinators of various crops, especially mango [Mangifera indica L. (Anacardiaceae)] in Thailand (Suvamayathipat 1984), Israel (Dag et al. 1998), and elsewhere (Roubik 1995) and may be managed for pollination for seed production of various horticultural crops (Table 1). Given the medical and potential pollination importance of this group, much remains to be learned about, and potentially gained from, the relations of blowflies and flowers (see Dethier 1976).

Tachinid or bristle flies (Tachinidae) are abundant and conspicuous nectarophagous anthophiles. Their setiferous bodies may enhance their pollen-carrying ability. Despite the conspicuousness of some species as anthophiles, and the potential value of these flies as biocontrol agents, the importance of flower relations to their bionomics is poorly known.

Muscidae (including Fanniidae) are often considered the most significant anthophiles after syrphids (Speight 1978; Proctor et al. 1996). In arctic and alpine regions they seem especially important as pollinators (Table 1). On some flowers, they forage for pollen while standing on the gynoecium or androecium, which dusts the dor- sum or venter with pollen, respectively, allowing later transfer to stigmas (Kevan 1970).

The dominance of calyptrates as flower visitors and pollinators in arctic and alpine biomes is more pronounced when other families in this group, such as tachinids, anthomyiids, and calliphorids, are included (e.g., Hocking 1953; Chernov 1966; Mosquin and Martin 1967; Kevan 1970, 1972; Arroyo et al. 1982; Philipp et al. 1990). In montane New Zealand, tachinids are the most abundant flower visitors, with muscids close behind (Primack 1978, 1983). Over 80% of the insect visitors to Minuartia groenlandica (Retz.) Ostenfeld (Caryophyllaceae) on Mount Washington, New Hamp- shire, were muscids and anthomyiids [Delia platura (Meigen) and Nupedia aestiva (Meigen)] (Levesque and Burger 1982). Although the calyptrates do not carry as much pollen as the less frequent syrphids, their numbers and higher activity levels under ad- verse conditions offset their inefficiency (Levesque and Burger 1982; Pont 1993). The systematics of many of these fly groups is incomplete (SA Marshall, personal communication), and this has hampered some studies of pollination (e.g., Primack 1983).

Numerous lower plants, fungi, and angiosperms have convergently developed chemical mimicry to attract carrion- and dung-loving calyptrates, which act as spore dispersers. Rust fungi (Uredinales) and macrofungi such as Phallus impudicus L. emit carrion odours for this reason (Stowe 1988). ~ h o i b i a phrenione Seguy (Anthomyiidae) is an essential conidial vector for the ascomycete Epichloe typhina (Fr.) Tul. (Bultman and White 1988), and anthomyiids are the primary visitors to pseudoflowers of the rust fungus Puccinia monoica (Pk.) Arth., transferring rust gametes between mating types on infected plants (Roy 1994). Similarly, various flies including Scatophaga furcata (Say) (Scathophagidae), Pyrellia cyanicolor Zetterstedt, Myospila metida (Muscidae), Delia platura (Anthomyiidae), and calliphorids are attracted to several genera of the moss family Splachnaceae, whose spores they disperse (Troilo and Cameron 1981; Cameron and Troilo 1982; Koponen 1990). The complex three-kingdom relations between insects (including Diptera), flowers, and fungi are likely to provide exciting new avenues for research in community ecology and coevolution (see Lachance et al. 2001).

Table 1. Summary of Diptera by suborder and family with respect to their activities on flowers.

Taxon Activity Comments References

Anisopodidae Nectarophagous Bibionidae Anthophilous

Nectarophagous

Pollinator

Blephariceridae Nectarophagous Cecidomyiidae Anthophilous

Pollinator

Other Ceratopogonidae Nectarophagous and

pollenophagous

Pollinator

On flowers with exposed neclar Early in the year. because mating swarms often forage on nearhy flowering

plants for sustenance On Flowers with exposed lspccies with short prnhoscides (about 2 mm

long)] and hidden (species with elongate ~nouthpms) nectar rrom tubular flowers

Nemophilrr ntomnrin Fisch. and Mey. (Hydrophyllaceae) is pollinated by two species of Rihio Geoffroy (I): adults of many more species may be important as pollinators. but their effectiveness needs to be quantified (2)

Apisromia c*legans (Rig00 feeds on Asteraceae On small tubular flowers of Saxifragaceae and Asteraceae. which have

exposed nectar (I) : adlilts of the genus Cka~rliodonrr~n~yiu are common in the inflorescence.; of the neotropical bambucoid gracc genus Pnriana Aubl. (Poaceae) (2)

Cacao. Tl~robromn cacao L. (Sterculiaceae), is pollinated by species of Clino(1iplosis Keiffer and M~rocfiplosis Riibs,unlen pollinate (I); also pollinated hy Cecidomyiidae are species of Siparrrnu Aubl. (Monimiaceae) in the tropical Americas (2)

Oviposition and brood site Female and male commonly visit flowers with exposed nectar, r.8.. adults

of the genus C!rlic.oides Latreille are abundant as nectar feeders on flowers of Heraclertm L. and Cicrrra L. (Apiaceae). among others (I): female Atrirlropo~orr polliniror~~s Downes feed on pollen to obtain proreinaceous and other nutrients that are, by other Ceratopogonidae. found in blood meals (2)

The protogynous flowers of the arum lily. Pinellirr Ten. (Aracaeae), in Japan and the pipevine, Ari.stnlorhia nwrsonii Wooton and Standley (Aristolochiaceae). in the American southwest are pollinated in a trap manner similar lo that described h r psychotlids pollinating Arrtrn rnacrrlai~rm L. (Araceae) (I ): the genus Fr~rripnn~yiu Meigen, and especially its suhgentis EtrprJonnnisiu, contains numerous species essential Tor the pollination of cacao in the tropics (2)

Proctor ei ril. 1996: and Speight 1978 Primack 1978; Speight 1978: and Shaw and

Taylor 1986 Beattie 1971, 1972

( I ) Cruden 1972; (2) D'Arcy-Burl and Blackshaw 1991

Downes 1958 ( 1 ) Proctor and Yeo 1973: and Proctor et al.

1996: (2) Soderstrom and Caldemn 1971

(1) Young 1985: (21 Feil 1992: and C Vergara, V Meltndez, and PG Kevan, personal observations from Veracruz. Mexico

Feil 1992 (1) Hocking 1953. 1968; Downes 1958; and

Proctor and Yeo 1973: (2) Downes 1955

(1) Meeuse and Moms 1984; and Crosswhite and Crosswhite 1984; (2) Entwistle 1972; Byswak and Wirth 1978; Young 1984a, 1986; and Wirth 1991

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448 THE CANADIAN ENTOMOLOGIST

Bombyliidae Anthophilous

Pollinator

Apioceridae Anthophilous Despite these flies having the common name of "flower-loving Bes" tl~ere is little know about the flower relations. They are invoked as being among the Brachycen associated with Cretaceous and pre-Cretaceous angosperms

Asilidae Nectarophagous R m l y found on flowers. adults may f e d from the flowers of Apiaceae and other families with shon tubes and possibly deeper-tubed flowers. as in C'crccirri~~n?

Other Adults have elongate mouthparts used primarily for predation: some species may await prey at flowers

Athericidae Anthophilous Occasional visitors to those Asteraceae and Apiacew with flowers with exposed nectar. although they are rarely mentioned as anthophiles: probably relatively insigificant as pollinators. hut their relationships with flowers need more investigation

They commonly forage a! phloxes (Polemoniaceae). Scrophulariaceae. and other long-rubed ilowers such as species of Prinrrrlu L. (Primulaceae) m d Cnrdornin~ L. (Brassicaceae). Ailcgu rcptons L., and Glecqhnmo hrrferulc.ru L. (Lamiaceae), although they can forage a1 flowers with open nectar (1): they are comnion visitors of boreal forest herbs (2): large floral displays of Asteraceae in South Africa are visited extensively ( 3 )

Nectarophagous Best known families of anthophilous Dipten with an elongate (up to 1.2 cm), specialized proboscis adapted for obtaining nectar from nectaries hidden deep within tubular flowers: however, some species. such as Anrfrrcw spp.. have short mouthparts that restrict them to lapping at open flowers with exposed nectar and flowers with shon corolla tubes (1): bee flies cannot fold or coil their long proboscis, so they often hover in front of flowers to reach the nectar within (2); some species such as Pocrik(~~no~lrrrs pkrrrctipcwnis (Walker) eat pollen that is gathered with the front tarsi (3)

Bomhylir~s ngit)r L. is a dominant menlber of the guild of eastern North American spring wildflo\n.er pollinators (1); in northern Aushalin. species of Li,qyra Newman are important pollinators of cashew. Anarar~lilrm ocridt-ntulr L. (Anacardinceae) (2)

Dolichopodidae Anthophilous Infrequent visitors oi flowers

Ren 1998; Labandeira 1998a. 1998b; Grimaldi 1999

Proctor et al. 1996

Downes 1958; Oldroyd 1964; Spipht 1978; Proctor and Yco 1973: and Proctor er al. 1996

(1) Simer 1946: Grant and Griint 1965: Straw 1963 for Pe~lsrcnlnn: Knight 1967: Proctor and Yeo 1973: and Proctor t.1 (11. 1996: (2) Barren and Helenunn 1087: (3) Vogel 1054

(1) Graenicher 1910: Robertson 1928: and Gilbert and Jervis 1998; (2) Rarth 1985: (3) Knoll 1921: Prnctor and Yeo 1973: and Deyrup 1988

(1) Beattie 197 1 and 1976 for Iriolo rostruta Pursh and other violels: Motten PI 01. 1981; Mutten 1986; and Grimaldi 1988 for Hedyntis cuurrtl~o (L.) Hook (Rubiaceae); (2) Heard er art. 1'300

Willis and Burkill 1895-1908: and Hobby and Smith 1961

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'saimi~au pasodua-llam qi!m sJamoU woq p a s Lluo uvn La111 os +lvlnqnI lam^ pm? uoi[s a.ln st~sdqinotu ~ ! a q l 'slolspa~d am sa!lj av3qi qiSnotlily Sn0%8yd0Jt?l3a~

sluaururo3 iil!h!13~ u o x e ~

Pelworl~ynchidae Anfhophilous

Rhagionidae Anthophilous Stratiomyidae Anthophilous

Males and females of the genus P~lccorhynchrrs have been recorded on the flowers of Lepr~~spermum J.R. Forst. and G. Forst (Myrtaceae)

See Athericidae See Athericidae: adults have been recorded from the flowers of 22 plant

families, but the visitation records are sparse ( 1 ) : they were observed in low numbers but often on the flowers of the dioecious treelet P t ~ l e n trifnliotn L. (Rutaceae) on the Ontario shore of Lake Erie (2)

Tn banidae Anthophilous Often visit flowers

Nectarophagous Nectar feeding well known, but subfamilies vary greatly in their ability to procure nectar from flowers with corollas of different Lengths: illthough the broad proboscis of tabanines ( e . ~ . . genera H~honiitru Enderlein and Tuhunrts L.) is best suited for flowen with exposed nectar that are clumped in pseudanthia and umbels (such as Apiaceae, some Ericaceae, and Asteraceae). chrysopine tabanids ( e . ~ . . genus Ch,lvsops Meigen) and tropical pangoniines ( c . ~ . , genus Pnngonia) have longer mouthparts that enable them to feed from the longer-mhed flowers of Lamiacei~e. Leguminosae. and Scrophulariacetre ( I ) ; hoth males and females collect nectar from flowers. hut the latter switch to blood meals after mating. when protein is required for egg development ( 2 )

Long-tongued tabanids of the genus Philolich~ are pollinators of several Inng-tuhed lridaceae (especially Glncliliolrts) and Orchidaceae in soutliern Africa

Few recorck on flowers that have exposed or partly concealed nectar

Pollinator

Therevidae Anthophilous

Brachpcera: Cpclormpha: Aschiza Lonchopteridae Nectarophagous Some Lonclloptcru spp. feed on exposed nectar Pipunculidae Nectarophagous Some records of nectarophagy from open flowers Phoridae Anthophilous In Europe. 77 species of phorids visit 60 species of plants (I) : in the

British Isle-3. records indicate 41 species from 45 flowers (2): in both cases. they Frequent species of RonrmtLrrlrrs. Pornossiu. Sulis. Potenrillu, Apiaceae (c-g., Angelir*o syhrstris L. and Heroclrtini sphondylitim L.), and Asteraceae with relatively exposed nectar

Willemstein 1487 5 E

- w

(1) Knuth 19061912; (2) Amhmse a! RI. 1985 W

combined under "other"

Hocking 1953: Pratt and Pratt 1972: Wilqon and Licux 1972: and Maparelli er 01. 1970

( 1 ) Hocking 1953: Vogel 19.54 and Lall and Davie9 1971; (2) Speiphr 1978

Manning and Goldhlatt 1996: Johnson and Steiner 1997: C;oldhlatt and Manning 2000; and Goldblatt et a!. ?Wl

Proctor er 01. 1996: Proctor and Yeo 1973; and Williams 1995

Proctor er al. 1996: and Speight 1978 Proctor el al. 1996: and Speight 1978 ( 1 ) Baumann 1978: (7) Disney 1980

Nectarophagous See Anthophilous

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.(panu!zuo3) 1 alqeJ

Lauxanidae

Milichiidae

Otitidae

Piophilidae Sciomyzidae Sepsidae Sphaeroceridae Tephritidae

Other See Drosophilidae

and Milichiidae Anthophilous

Pollination

Other Pollination

Other

Nectarophagous See Otitidae Nectarophagous Anthophilous Other

Calliphoridae Anthophilous

Sparse records of sapromyophily 2 6

Adults have been reported from the hap flowers of Ahroma ougusta L. f. (Sterculiaccae) in Indonesia and Cerr)p~gia albisepfu Jum., and H . Perr. (Asclepiadaceae) in Madagascar, and the genus DL-srnomeropn Loew is sometimes numerous at flowers (I); Parrrmyia nirens (Loew) can be found abundantly on flowers, especially of some Asteraceae. in Ontario (2)

Together with chloropids and lawraniids (predominantly females). adults have been reported in Aristolochirr L. spp., which they may pollinate ( 1 )

Sparse records of sapromyophily Invoked as pollinators (with Muscidea) of Arisfolochio ~randiflom Swanz

(Aristolochiaceae) in Costa Rica Feeding habits of these adults are not well known, but flower visiting by

this predacious family may be for the location of prey On tundra flowers, but not likely pollinators

Feed on nectar at umhels of Apiaceae, b u ~ not likely pollinators Found in trap flowers and the spathes of Araceae; sparse records of anthophily Visit Aweraceae to oviposit, but normally they neither visit enough flowers

nor carry enough pollen to be effective pollinators. and their parasitic offspring consume the developing ovules

Rrachycera: Schizophora: Calppterate Muscoidea Common visitors to flowers of Asclepiau spp. (Asclepiadaceae) in

northeastern North America (1) and are recorded as the most common Diptera visiting flowers of h e dioecious hop wee, Preleu n$o/iam, on the north shore or Lake Erie (2); in arctic and alpine tundra blowflies overwinter as adults, so they are among the first anthophiles after the winter, and are sometimes prevalent visitors to members of the Saxifngaceae and Salicaceae (3): along with muscid flies (Muscidae), they are consistent and frequent visitors to the mangtovc, Auicennia ofl~cina1i.v L. (Avicenniaceae), in India (4): they are readily attracted to the decaying smell of many saprornyophilo~is flowers (such as Rafle.~ia (Rafflesiaceae) in the Malay archipelago ( 5 )

L W

(1) van der Pijl 1953: and Sabrosky 1983, 1987; w

(2) SA Marshall. personnl communication

Brantjes 1980: and Wolda and Sabrosky 1986

Hilje 1984 1

Willemstein 1987 3 0

z Chernov 1966: McAlpine 1965: and Kevan 1970

k

Proctor et crl. 1996 3 Grensted 1947; Prime 1960; and Yafuso 1993 Proctor er at. 1996 g g

(1) Punchihewa 1984; (2) Ambrose rf al. 1985; (3) McAlpine 1965; Chemov 19hh; and Kevan 1970. 1973: (4) Raju 1990: (5) Beaman et al. 1988: and Bdnziger 1991

456 THE CANADIAN WOMOLOGIST July/August 2001

Nectarophagous Adults are abundant flower visitors in many regions, where they feed Karczewski 1967; Speight 1978; Proctor et al. predominately on nectar, and their hairiness may enhance their pollen- 1996; and Gilbert and Jervis 1998 F

el carrying ability; dexiine and siphoniine tachinirk, such as Siphona ,qeniruknu (DeGeer) and species oC Calirrhoe. have relatively long and slender proboscides that allow them to exploit the nectar in the tubular corollas of some legames. Asteraceae. and species of Mcntha L.

Sarcophagidae Anthophilous Pollinator

Scathophagidae Anthophilous

(Lamiaceae) Occasionally reported from flowers Blaesu.ripho jlerclteri (Aid.) may pollinate Sorracenin prrrpltreo L. Thomas 1986

(Sarraceniaceae) Reported occaqionally as flower visitors: Hjvfrornyza lh~ens Fall. is common (1) van der Velde et al. 1978; (2) SA Marshall,

in the flowers of Nlrphar Irrtea (L.) Sm. (Nymphaeaceae) in Holland and personal communication is presumably a pollen vector (1 ): the same may be true of Hydromvm c o n f l ~ ~ n s h e w , a miner on water lilies (Nymphaea) in eastern North America where it can be found abundantly on the flowers (2)

Necbrophligous and Flies of the genus Scathoplpka~a Meigen are often recorded at Rosaceae. Proctor et al. 1996 pollenuphagous Ranunculaceae, Rrassicaceae. Apiaceae, and Asteraceae, where they feed

on pollen and nectar - 55

Other In the Canadian High Arctic. Scuthopha.~a apicalis Curtis uses flowers, Kevan 1970 2 especially Sa- ifr raga f>ppo.sirifolicl. as sites for ambushing prey, mostly I

Syrphidae g Note: Taxonomic arrangement is first by suborder: Nematocera then Brachycera split into Orthorrapha and Cyclorrhapha. Within Cyclorrapha, the Schizophora and Aschiza are separated, and within Aschiza, Acalypterate and Calypterate Muscoidea are listed separately. Within those larger taxa, families are listed alphabetically, The schema follows that of the Manual of nearctic Diptera (McAlpine et al. 1981).

TVFTAKADIAN ENTOMOLOGIST

Acknowledgements

Thanks to Steve Marshall for comments and the Natural Sciences and Engi- neering Research Council of Canada (NSERC) for a research grant to PG Kevan that al- lowed completion and publication of this paper. Anonymous reviewers have helped with critical comments and observations.

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Botany 66: 820-4 Addicott JF. 1986. Variation in the costs and benefits of mutualism: the interaction between yuccas and

yucca moths. Oecologia 70: 486-94 Agnew JD. 1976. A case of myophily involving Drosophilidae (Diptera). Journal of South African Botany

42: 85-95 Ambrose JD, Kevan PC, Gadawski RM. 1985. Hop tree (Ptelea trifoliata) in Canada: population and repro-

ductive biology of a rare species. Canadian Journal of Botany 63: 1928-35 Arroyo MTK, Primack R, Armesto J. 1982. Community studies in pollination ecology in the high temperate

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(Received: 30 November 1999; accepted: 16 March 2001)

Documents

Flies and flowers: taxonomic diversity of anthophiles and pollinators