Pollen feeding in hover flies (Diptera: Syrphidae)
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1 New Zealand Journal of Zoology ISSN: (Print) (Online) Journal homepage: Pollen feeding in hover flies (Diptera: Syrphidae) Beverley A. Holloway To cite this article: Beverley A. Holloway (1976) Pollen feeding in hover flies (Diptera: Syrphidae), New Zealand Journal of Zoology, 3:4, , DOI: / To link to this article: Published online: 30 Mar Submit your article to this journal Article views: 783 View related articles Citing articles: 44 View citing articles Full Terms & Conditions of access and use can be found at
2 New Zealand Journal of Zoology, 1976, Vol. 3, Pollen-feeding in hover-flies (Diptera: Syrphidae) BEVERLEY A. HOLLOWAY Entomology Division, Department of Scientific and Industrial Research, Private Bag, Auckland, New Zealand Analyses of the pollen contents of the crop and intestine of 11 species of New Zealand Syrphidae. showed that small, sparsely haired hover-flies with unbranched hairs, short, simple bristles, and a short proboscis had ingested at least 99% anemophilous pollens, and that larger, more hairy hoverflies with pollen-collecting hairs, long, spirally grooved bristles, and elongate mouthparts had ingested pollens almost exclusively from nectar-bearing flowers. Pollen-feeding behaviour was studied in one hairy species, the drone-fly Eristalis tenax, and in one sparsely-haired species, Melanostoma fasciatum. Using granulated charcoal as a substitute for pollen, it was found that in E. tenax particles trapped among the body hairs are combed off by the front and hind tibiae and transferred to pollenretaining bristles on the front and hind tarsi respectively. Particles retained among the front tarsal bristles are ingested directly from the bristles. Those retained by the hind tarsi are transferred in flight by leg-scraping movements to the front tarsi, from which they are subsequently eaten. E. tenax also eats pollen directly from anthers. In M. fasciatum apparently all the pollen ingested is taken directly from anther lobes or stigmas. The few pollen grains that adhere to the body of this species are combed off by the front and hind tibiae and transferred to the front and hind tarsi, but are not retained there because the bristles are short and simple. The mouthparts, hairs, and bristles of E. tenax and M. fasciatum are illustrated. Drawings of leg movements associated with pollen collection and ingestion, and photographs showing leg scraping in E. tenax are included. Morphological similarities between drone-flies and honey-bees, previously regarded as the result of mimicry, can be explained by convergent evolution in response to similar food-gathering behaviour. Probably the majority of Syrphidae, and also the related Acroceridae, collect pollen by means of branched or curly-tipped hairs. INTRODUCTION Miiller (1883) reported that syrphids consume pollen grains as well as taking nectar from flowers. The uptake of pollen is essential to normal ovarial functioning (Schneider 1969). Although the pollen is digested as it passes through the gut (Grinfield 1955) the grains retain their shape, and can still be identified. Schneider (1958) found that the crops of some over-wintered females of Lasiopticus pyrastri (Linnaeus), one of the hairy hover-flies, collected in early spring contained as many as 20 species of pollen. Most were from early spring flowers, but there were also a few out-of-season grains which Schneider considered must have been ingested in the previous autumn. Crop analyses carried out by van der Goot & Grabandt (1970) on sparsely haired hover-flies belonging to Melanostoma and Platycheirus revealed that some species had ingested only anemophilous pollens, either of plantain (Plantago lanceolata L.) or of grasses, although entomophilous pollens were available in the feeding area. Van der Goot & Grabandt pointed out that whereas Schneider (1958) had concluded that hover-flies do not confine themselves to a specific kind of flower, their own analyses showed that some species have a clearly restricted host-plant range in pollen-feeding. The present paper investigates pollen-feeding in some New Zealand Syrphidae. Results from crop analyses carried out during 1975 confirmed to some extent what was apparent from the European work, viz that the large, very hairy syrphids were ingesting a wide variety of pollens, almost entirely from entomophilous species, and the small, least hairy syrphids were eating only one or two kinds of pollen, mostly anemophilous. Eristalis tenax Linnaeus and Melanostoma fasciatum (Macquart), representing the two extremes of pollen diet, were selected for morphological study. In early summer of 1975, when live material became abundant, behaviour relating to pollen-collecting and nectar-feeding of both species was observed in the field and in the laboratory. Experiments in which granulated charcoal was substituted for pollen were carried out to show how pollen grains and other particles are collected and eaten by E. tenax and how the ingestion of certain pollens and particles is avoided by M. fasciatum. The morphological and behavioural features which determine the pollen diet of these hover-flies are described and discussed. Received 22 April Published online 30 Mar 2010
3 340 N.Z. Journal of Zoology, 1976, Vol. 3 MATERIALS AND METHODS All the syrphids, including dissected specimens, used in this study are in the New Zealand Arthropod Collection, Mt. Albert Research Centre, DSIR, Auckland. Analyses were made of the crop, intestinal, or faecal pellet (adhering to the end of the abdomen) pollen contents of 11 species, itemised below under Pollen Analyses. Pollen analyses for Helophilus trilineatus and H. hochstetteri were made from pinned specimens. All others were from specimens stored in ethanol, which are more convenient to use for internal pollen analyses since they require no softening before the crop and intestine can be removed. A further advantage is that the pollen grains are visible through the transparent areas of the abdominal cuticle, and specimens containing large amounts of pollen can therefore be selected easily. Pollen appears to be present in both sexes equally, but the crop and intestine are more easily removed from males, which have only a small amount of glandular material and fat body. The slides on which the pollen analyses are based are held by Botany Division, DSIR, Lincoln. Live material was observed in the cage shown in Fig. 4. This was made from a 23.5x23.5x27.5 cm plastic container to which a 60x45 cm lightweight plastic bag cut open at the bottom and tied shut at the top was taped. To allow space for the flies to hover, the bag was supported internally by a light wire framework fitted into the base. The cage was kept in an environmentally controlled room at around 20 c and 55-60% RH. Appropriate flowers were placed in a jar in the cage and, when necessary, the nectar supply was supplemented with drops of honey-water. Charcoal used for dusting the body surfaces of flies was finely ground but not powdered, and was applied with a small paint brush to specimens observed under a low-power microscope. Specimens of Eristalis tenax could be held between thumb and forefinger without being damaged, but Melanostoma fasciatum was too delicate to be handled directly and had to be lightly anaesthetised and held with fine forceps. The charcoal experiments performed on both species are described in the main part of the paper. Faecal droplets of Eristalis tenax were collected directly on to microscope slides. The samples were more easily collected from females, in which the anus is exposed at the apex of the abdomen. The flight photographs of Eristalis tenax were obtained from specimens confined in a 50x13x11 cm plastic-film tower. To ensure that leg-scraping would occur frequently the specimens were dusted with pollens of Eschscholtzia and Ranunculus. POLLEN ANALYSES In the pollen spectra below, each pollen type is given as a percentage of the total pollen count (tr, < 1 %; +, pollen noted in scan after count made). Eristalis tenax (Linnaeus): $, Lynfield, Auckland, 24 Apr. 1974, in garden, B. A. Holloway. Crop contents. Fungal spores (c.f. Tilletia) 53; Compositae Taraxacum type 16, Matricaria type 4, unidentified tr; Myrtaceae {Metrosideros sp.) 10; Rosaceae 5; unknown 5; Cruciferae 4; Leguminosae 1; Rhamnaceae (c.f. Pomaderris sp.) 1; Gramineae tr. S, Green Bay, Auckland, 6 Apr. 1975, feeding continuously for 15 min on fennel {Foeniculum vulgare) flowers, B. A. Holloway. Crop contents (total pollen grains counted, 464). Cruciferae 77; Compositae Taraxacum type 13, Achillea type 2; Rosaceae 4; Escalloniaceae {Quintin i a sp.) 3; Myrtaceae {Leptospermum sp.) tr. Helophilus hochstetteri Nowicki: $, Browns Bay, Auckland, 12 Dec. 1948, on flowers, K. Harrow. Crop contents. Compositae Taraxacum type 33, unidentified 10, Matricaria type 2; Cruciferae 31; Rosaceae 8; Umbelliferae 8; Ranunculaceae 6; Gramineae 1; Chenopodiaceae tr; Ericaceae tr; Fagaceae (Quercus sp.) tr; Papilionaceae (Trifolium sp.) tr. Helophilus trilineatus (Fabricius): $, Waiheke L, Auckland, 10 May 1957, M. Beard. Contents of mid gut. Myrtaceae {Leptospermum sp.) 90; Compositae unidentified 6, {Taraxacum sp.) 1; Scrophulariaceae {Hebe sp.) 3. Helophilus cantpbellicus Hutton:, Biological Station, Snares I., 13 Feb. 1972, on Hebe elliptica, H. A. Best. Faecal pellet. Only 6 grains of Hebe sp. (Scrophulariaceae) pollen noted. Melangyna (Austrosyrphus) ortas (Walker):, Hydro Village, Monowai, Southland, 10 Jan. 1970, beating Hebe flowers, J. I. Townsend. Contents of mid gut. Scrophulariaceae {Hebe sp.) 100. c?, S. Borland R. flats, Westland, 12 Jan. 1970, beating flowers of Olearia virgata, J. I. Townsend. Contents of mid gut. Compositae (not Olearia type) 96; Scrophulariaceae {Hebe sp.) 4. Melangyna (Austrosyrphus) ropalus (Walker): g, Hydro Village, Monowai, Southland, 10 Jan. 1970, beating Hebe flowers, J. I. Townsend. Contents of mid gut. Compositae unidentified 93, Taraxacum type 1; Scrophulariaceae {Hebe sp.) 6. Melangyna (Austrosyrphus) novaezealandiae (Macquart): $, Rock and Pillar Ra., Otago, snow patch 1.6 km S of Summit Rock Ski Hut, 1372 m, 19 Dec. 1968, J. Child. Crop contents. Unknown 54; Liliaceae {Bulbinella sp.) 37; Ranunculaceae {Ranunculus sp.) 6; Caryophyllaceae {Stellaria sp.) 1; Fagaceae {Nothofagus sp.) tr; Podocarpaceae {Phyllocladus sp.) tr. Zelima montana (Miller) {= Xylota montana Miller): $, Arthurs Pass, mid Canterbury, 31 Jan. 1958, on Celmisia, L. J. Dumbleton. Contents of mid gut. Compositae (c.f. Celmisia sp.) 99; Ranunculaceae {Ranunculus sp.) tr; Scrophulariaceae {Hebe sp.) tr. Paragussp.: $, Mt. Barber, 1158 m, Wilmot Pass, Otago, 19 Jan. 1970, J. I. Townsend. Crop contents. Compositae 32; Stylidiaceae {Forstera sp.) 30; Gentianaceae (c.f. Sebaea sp.) 15; Plantaginaceae {Plantago lanceolata) 2; Cruciferae 1; Scrophulaciaceae {Hebe sp.) tr; unknown 19; Droseraceae {Drosera c.f. binatd) +.
4 Platycheirus sp.: $, Rock and Pillar Ra., Otago, 0.8 km N of Summit Rock, 1372 m, swept over stream, 19 Jan. 1968, J. Child. Crop contents. Ranunculaceae {Ranunculus gracilipes group) 81, {Ranunculus sp.) 19. Melanostoma fasciatum (Macquart): '$, Arthurs Pass, mid Canterbury, 28 Mar. 1920, Anon. Crop contents. Plantaginaceae {Plantago lanceolata) 100. <?, Lynfield, Auckland, 29 Oct. 1974, in garden, B. A. Holloway. Crop contents. Plantaginaceae {Plantago lanceolata) 99; Compositae unidentified tr, Taraxacum type +; unknown tr; Portulacaceae +. c?, Riverhead, Auckland, 31 Dec. 1974, pasture sweep, N. A. Martin. Contents of mid gut. Gramineae 77; Plantaginaceae {Plantago sp.) 23. These pollen spectra are brought together for comparison in Table 1. Pollens belonging to 23 plant families were identified. In addition unknown pollens occurred in 4 of the samples, and a high percentage of fungal spores, probably of Tilletia sp., was present in one specimen of Eristalis tenax. The greatest variety of pollens was found in Helophilus trilineatus, which had 12 species belonging to 10 different families. Only one species of pollen was present in H. campbellicus (Scrophulariaceae), Platycheirus sp. (Ranunculaceae), and the female of Melanostoma fasciatum (Plantaginaceae). It should be noted that the only analysis available for H. campbellicus was from a small faecal pellet containing 6 grains of Hebe pollen. Compositae pollen had been ingested by 8 of the 11 species, and Scrophulariaceae pollen occurred in 6 species. Apart from traces of Compositae, Portulacaceae, and an unknown pollen in one specimen, M. fasciatum contained only anemophilous pollen either of Plantago alone or of Plantago plus Gramineae. Plantago pollen was present in only one other fly, Paragus sp., in which it contributed 2 % of the total count. Grass pollen made up 77 % of the count in one specimen of M. fasciatum, whereas only 1 % was found in H. hochstetteri and a trace in the female E. tenax. The pollen spectra show that the largest (11-19 mm) and most hairy flies {Eristalis and Helophilus) had consumed the widest range of pollens per individual, and almost exclusively from nectar-producing flowers. The smallest (5-7 mm) and sparsely haired hover-flies {Melanostoma) had ingested at least 99 % anemophilous pollens, belonging to no more than 2 families. These findings agree closely with those recorded for comparable European hover-flies by Schneider (1958) {Lasiopticus pyrastri) and van der Goot & Grabandt (1970) {Melanostoma, Platycheirus). The remaining New Zealand species investigated, with a size range of 6-11 mm and not very hairy, had ingested one pollen or a variety, but never more than 2 % of anemophilous pollen. There appears to be no relationship between pollen grain size and the size of the insect (N.T. Moar, pers. Hollo way: Ho ver-fly Pollen-feeding 341 comm.). The smallest grains, Leptospermum, 17/xm, were predominant in the gut of Helophilus trilineatus, at 18 mm one of the larger hover-flies; whereas the largest grains, Gramineae, up to 50 /xm, were predominant in Melanostoma fasciatum, one of the smallest species (6 mm). In Melangyna {A.) novaezealandiae pollen grain size ranged from 19 /xm to 47 / x m, and a similar size range occurred in the pollens from the female Eristalis tenax. MORPHOLOGY AND BEHAVIOUR RELATING TO POLLEN INGESTION The pollen analysis results suggested that pollencollecting methods used by large, hairy hover-flies differed from those of the smaller, less hairy species, so the morphology and behaviour associated with feeding were investigated in representatives of both groups Eristalis tenax and Melanostoma fasciatum respectively. Eristalis tenax This is the cosmopolitan drone-fly, generally regarded as a mimic of the honey-bee (Fig. 2, 5). Most of the body, including the front of the eyes, is covered with hairs, many of which are long, curlytipped, plumose or branched (Fig. 8), and palynophilic (pollen-attracting). The black hairs on the legs are simple. Long, spirally grooved pollen-retaining bristles (Fig. 9) are abundant on the ventral surface of the tarsi and at the apex of the tibiae, and a row of these bristles along the distal ventral edge of each tibia forms a distinct comb. Pollen grains and other particles adhere to most of the body hairs, and may be several layers deep among the spirally grooved bristles. The proboscis is long, about 5.7 mm when fully extended in the specimen illustrated (Fig. 6) but up to 7 mm in some specimens (Proctor & Yeo 1973). There are pseudotracheal canals on each labellar lobe (Fig. 7). LEG MOVEMENTS IN NON-FLYING E. tenax. Droneflies spend a lot of time combing particles from the body surface and wings. Only the front and hind legs perform these cleaning movements. The front legs comb one another, the head and its appendages, and the middle legs; all other surfaces, and also the middle legs, are combed by the hind legs. The leg positions of a resting drone-fly are shown in Fig. 14. Fig show the main cleaning movements involving the hind legs. In Fig. 15 the pollencollecting combs at the concave distal edge of the hind tibiae are removing particles from the upper surface of the abdomen. The hind tarsi do not touch the body surface during combing. From time to time combing is interrupted by pollen-concentrating movements (Fig. 16), during which the hind legs extend backwards, free of the substrate, and the
5 342 N.Z. Journal of Zoology, 1976, Vol. 3 Table 1. Pollen spectra of crop, intestinal, or faecal contents of some New Zealand Syrphidae, as percentages of total pollen count for each specimen (tr, <1 %; +, noted in scan after count was made) Eristalis tenax $ Helophilus hochstetteri $ < < < 8 g u u 0 u tr < 0 s s ter tr tr < Q H R Ir u <p- < u c Q < J a: Z O < O S 5 S o * z if. trilineatus $ //. campbellicus $ 100 Melangyna {Austrosyrphus) ortas S o M. (y4.) ropalus $ M. (A.) novaezealandiae $ 1 tr Zelima ( = Xylota) montana $ 99 tr tr Paragus sp. $ tr Platycheirus sp. c? 100 Melanostoma fasciatum $ <? to tr tibial apex and tarsi of one leg scrape with a slight spiralling action against those of the other. Pollenconcentrating, which lasts about 3 s, allows particles which are caught by the comb to be transferred to the pollen-retaining bristles of the tarsi. It is followed by one or two rapid leg-tapping movements (Fig. 17) during which the hind tarsi extend obliquely to the sides of the body before being brought downwards and inwards for a short distance across the substrate. Leg-tapping dislodges outsize particles as well as a few pollen grains which are not trapped among the retaining bristles. The transport of particles just described was studied by applying finely ground charcoal to hairs on the upper surface of the abdomen, then observing the specimens in cages and examining bristles and hairs under a low-power microscope. It should be noted that the hind legs never come into contact with the mouthparts. The sequence of movements involving the front legs of non-flying drone-flies is shown in Fig The first 3 movements, combing (Fig. 18), pollenconcentrating (Fig. 19), and tarsal tapping (Fig. 20), are similar to those performed by the hind legs. During combing the head may be rotated through 90, and the proboscis is often everted. The front legs are extended anteroventrally for pollen-concentrating, and do not touch the substrate. Tarsal tapping occurs frequently in specimens which have had the head dusted with charcoal granules, but may be omitted when specimens are dusted only with pollen. In the fourth activity, pollen ingestion (Fig. 21), the front legs are directed anteroventrally and sharply elbowed between femur and tibia, the mouthparts are extruded for a short distance, and the fly eats the pollen and other particles caught among the tarsal bristles. As the particles are being ingested the labellum moves rapidly over the retaining bristles of the slightly rotated tarsi. The abdomen does not pulsate during pollen ingestion. The pathway of particles from head to gut was shown as follows. Specimens previously maintained on Ranunculus sardous flowers were fed on honeywater for 24 h, then, at hourly intervals from 9 a.m.
6 until noon, had finely ground charcoal applied to hairs on the head. After each application the specimens were returned to the cage, where they fed on honey-water and carried out the particle collecting and ingesting movements described above. By noon the flies were producing black faeces containing large quantities of charcoal. The specimens were killed 1 h later, and were found to have charcoal granules distributed throughout the gut. During the 6 weeks that drone-flies were kept in the cage on flowers of Ranunculus sardous they were not seen to eat pollen directly from stamens, but they continually produced yellow faeces containing large numbers of Ranunculus pollen grains. Specimens in the field were not observed to eat Ranunculus pollen directly, but some were seen ingesting pollen from anthers of Raphanus maritimus and R. sativa. LEG MOVEMENTS IN HOVERING E. tenax. The usual positions of the legs of a hovering drone-fly are shown in Fig. 22. The front and middle tarsi are directed forwards, approximately parallel to the ventral surface of the thorax; the hind tarsi are held parallel to the obliquely tilted abdomen. Two different scraping movements were seen to occur during hovering. The first involves only the hind legs, and is similar in appearance and probably also in function to the pollen-concentrating movements of the non-flying insect. The second involves all 3 pairs of legs, and takes place as they dangle at 90 to the body. Fig. 23 shows an early stage of leg dangling in which only the middle and hind legs have been brought together. In Fig. 24 all the legs are in close contact with one another and the left front tarsi are touching the right hind tarsi. Movement of the legs from the normal flight position to dangling and back to flight position can be completed within 2 s. In laboratory specimens leg dangling began most frequently within 3 s of takeoff. In the field, drone-flies were seen to dangle the legs up to 5 times before settling again to feed or groom. That leg dangling allows pollen grains and other particles caught in the hind tarsal bristles to be transferred to the front tarsi for ingestion was shown by the following experiment. Charcoal granules were pushed down among the hairs on the posterior half of the mesonotum of a specimen (Fig. 14), which was then placed in the observation cage and provided with honey-water but no pollen or charcoal. After 24 h, during which the fly was frequently observed to comb the thorax, dangle the legs, and eat particles from the front tarsi, the gut was examined and found to contain charcoal granules throughout its length. Charcoal was also present among the retaining bristles of the front and hind tarsi, and a few granules remained among the Holloway: Hover-fly Pollen-feeding 343 thoracic hairs. The mesonotum is combed only by the hind tibiae and particles are consumed only from the front tarsi, so for charcoal applied to the mesonotum to reach the mouth the granules had to pass from the hind tarsi to the front tarsi; this contact is possible only during leg dangling. Leg movements similar to all those described above for E. tenax have been observed in the field in Melangyna (Austrosyrphus) novaezealandiae and Merodon equestris (Fabricius). Melanostoma fasciatum This small, shiny syrphid (Fig. 1, 3) is abundant in pastures and wastelands throughout New Zealand. The whole body is sparsely haired, but the eyes are bare. The hairs are short, stiff, apparently palynophobic, and never plumose, curly, or branched. A simple hair from the upper surface of the hind femur, and typical of all the body hairs, is shown in Fig. 13. Short, simple bristles (Fig. 12) which have fine, oblique surface striae but are never spirally grooved are numerous on the apex of the tibiae and on the ventral surface of all tarsi. A coronet of these bristles at the distal end of the tibia forms a cleaning comb. Pollen grains are rarely present among the vestiture, and it is difficult to get charcoal granules to adhere to any part of the body, particularly the wings. The proboscis is short, about 1.4 mm when fully extended (Fig. 10). There are pseudotracheal canals on each labellar lobe (Fig. 11). LEG MOVEMENTS IN NON-FLYING M. fasciatum. Although in the field and in the laboratory specimens of M. fasciatum rest for long periods on the stems of grasses and weeds, they groom very little. Most of these specimens are engorged with pollen, and probably are inactive while digestion is taking place. The feeding and cleaning activities of specimens kept on various types of anthers or dusted with charcoal granules or pollen were studied in the observation cage and in glass tubes at low magnifications. Specimens were also observed in the field. It was found that, as in E. tenax, the front legs clean one another, the head, and the middle legs, and the hind legs clean the remainder of the body and also the middle legs. The grooming sequence involving the hind legs was similar to that shown in Fig , but because the tarsal bristles are short, and do not have deep spiral grooves, very few particles or none at all were retained on the tarsi after leg tapping. Similarly movements involving the front legs were like those shown in Fig , but the few particles concentrated on the front tarsi dropped off during leg tapping. The mouthparts were not seen to be applied to the front tarsi for feeding as they are in E. tenax. Rather, M. fasciatum assumed a position closely resembling that shown
7 344 N.Z. Journal of Zoology, 1976, Vol. 3 Fig Syrphidae, adults: 1, Melanostoma fasciatum on Raphanus maritimus; 2, Eristalis tenax on Picris echioides; 3, M. fasciatum S (right), $ (left); 4, observation cage; 5, E. tenax S (right) cf. worker honey-bee (left). in Fig. 21 when it held the anthers of plants such as grasses, Plantago, and Raphanus maritimus with the front tarsi and ate pollen directly from the anther lobes. Specimens were also seen to grasp the stigmas of Plantago in a similar way while consuming the adhering pollen grains. LEG MOVEMENTS IN FLYING M. fasciatum. Flight movements were difficult to observe because of the fly's small size. In hovering specimens the legs were normally held close to the body, but the actual positions could not be determined. On a few occasions the legs were seen to dangle and scrape, apparently in a manner similar to that observed and photographed in E. tenax (Fig. 23, 24). Hind leg scraping (pollen-concentrating) in flight probably occurs, but was not observed with certainty. POLLEN INGESTION IN M. fasciatum. During the weeks that M. fasciatum was observed in the field
8 Holloway: Hover-fly Pollen-feeding 345 palp_3, hypophary Fig Morphology of adult Eristalis tenax (6-9) and Melanostoma fasciatum (10-13): 6, 10, mouthparts (vestiture omitted); 7, 11, labellar lobe; 8, 13, seta from hind femur (apical half only in 8); 9, 12, bristle from hind metatarsus (7, 10, 11 and 8, 9, 12, 13 each to same scale). 13 and the laboratory it was not seen to eat particles from its tarsi. In nature, all the pollen ingested is apparently taken directly from stamens (and also stigmas in Plantago). Some specimens in the laboratory ate pollen grains from the surface of the glass tube, but all other pollen eaten was taken directly from anthers. M. fasciatum visits a variety of flowers for nectar (e.g., Daucus, Taraxacum, Leptospermum), but the analyses showed that pollen was rarely consumed from these species. When consuming Plantago and grass pollens the fly grips the anther between the front tarsi, inserts
9 N s J*3fl\ g Fig Movements involving hind legs of resting Eristalis tenax: 14, resting position (indicating area dusted with charcoal for experimental purposes); 15, abdominal combing; 16, concentrating particles among tarsal bristles; 17, tarsal tapping to dislodge large particles. Fig Movements involving front legs of resting Eristalis tenax: 18, head combing; 19, concentrating particles among tarsal bristles; 20, tarsal tapping to dislodge large particles; 21, eating particles caught among tarsal bristles.
10 Holloway: Hover-fly Pollen-feeding $41 Fig In-flight movements involving legs of Eristalis tenax: 22, normal flight position; 23, 24, leg dangling and scraping during which particles are transferred from hind tarsi to front tarsi (all 1/5000 s exposure) both labellar lobes into a pollen-filled anther lobe, and eats all the pollen that is present, repeating this systematically on the adjacent anther lobes. The large, abundant, elongate anther lobes of Plantago and grasses (Fig. 25) allow considerable amounts of pollen to be ingested within a short period. To determine whether pollens other than anemophilous ones would be eaten, specimens deprived of pollen for 24 h were provided with a single pollen source: Raphanus maritimus (Cruciferae: sea radish); Ranunculus sardous (Ranunculaceae: buttercup); Eschscholtzia californica (Papaveraceae: Californian poppy); or Daucus carota (Umbelliferae: wild carrot). Specimens isolated on the first 3 species were seen to eat pollen, and subsequent analysis confirmed that their crops contained an abundance of each of the pollens. The specimens kept for 24 h on 24 Daucus carota were seen to take nectar but not pollen from the flowers, and analysis showed that their crops indeed contained no pollen at all. the surface of the tube, in nature they probably Raphanus, Ranunculus, and Eschscholtzia all have select pollen from anther lobes that are large enough large, elongate anther lobes comparable to those of to accommodate the mouthparts. Depending on the Plantago and grasses, and with large quantities of plant species, total engorgement with pollen can pollen. The Iabellum of Melanostoma can be inserted occur on a single flower and within a very short time. into the anther lobes of all these species. In Daucus For instance, a specimen of M. fasciatum in the (Fig. 27, 28), however, the anther lobes are circular, laboratory systematically emptied the contents of contain relatively little pollen, and are too small to the 6 erect stamens of a newly opened flower of allow insertion of the Iabellum. Although Melanostoma in the laboratory were seen to eat pollen from Single flowers of umbelliferous plants such as Raphanus maritimus (Fig. 26) in less than 15 min. Daucus
11 348 N.Z. Journal of Zoology, 1976, Vol. 3 Fig Food sources for adult Syrphidae: 25, large, abundant, elongate anthers of Plantago lanceolata (left) and Dactylis glomerata (middle) cf. fewer, smaller anthers of Cotoneaster horizontalis (right); 26, elongate anther lobes of Raphanus maritimus held erect by water storage cells; 27, 28, flowers of Daucus carota showing large, nectar-covered disc and small, widely spaced anthers in various stages of development and dehiscence. and Foeniculum vulgare (fennel) can produce copious quantities of nectar, but the amount of pollen available at any one time varies considerably because the stamens do not all open simultaneously (Fig. 27, 28). DISCUSSION Syrphids require both nectar and pollen in their diet. Proboscis length will determine to a large extent the nectar sources exploited by various species. Hoverflies with a short proboscis (Melanostoma fasciatum) obtain nectar from disc flowers such as those of Umbelliferae, from Compositae in which the nectar wells up in the flower, and from cruciferous flowers which have separated petals. In M. fasciatum the labellar surface is small and the pseudotracheal canals responsible for nectar intake are few in number. Most syrphids have a long, flexible proboscis which in addition to taking exposed nectar can reach into the tubular flowers of Scrophulariaceae and Verbenaceae and can probe the concealed nectaries of Ranunculaceae. Some species belonging to this group have a greatly increased labellar surface with as many as 40 pseudotracheal canals. Pollen is obtained in two very different ways. The short-mouthed M. fasciatum eats pollen directly from anthers, apparently selecting species in which the anther lobes are large enough to accommodate both labellar lobes during feeding. The anther lobes of anemophilous plants belong in this category, and those of some entomophilous species can also be used. In Eristalis tenax and probably the majority of syrphids direct pollen feeding has been supplemented, and in some species probably replaced, by
12 a pollen-collecting system which operates as the flies collect nectar. Some of the body hairs are branched, plumose, or curly-tipped, and collect pollen grains which are later removed by the front and hind tibial combs and concentrated in the spirally grooved retaining bristles on the front and hind tarsi. Particles retained among the front tarsal bristles are eaten from the tarsi. Those trapped in the hind tarsal bristles are transferred by in-flight scraping movements to the front tarsi. Pollen-combing, pollenconcentrating, leg-tapping, and leg-scraping movements in E. tenax are identical with the leg movements used solely for cleaning in M. fasciatum. The presence of pollen-retaining tarsal bristles in E. tenax has changed the cleaning process to one of pollen collection. In general the crop contents of syrphids with pollen-collecting vestiture have complex pollen spectra, and these indicate fairly accurately the sorts of flowers that have been visited for nectar. The head is probably the most important pollen-collecting surface in E. tenax. In the laboratory, the large quantities of pollen picked up by the facial hairs as drone-flies probed the nectaries of Ranunculus sardous were constantly being removed and eaten. Pollen adhering to the wings was also removed frequently, but pollen on the thorax and abdomen may be left for several days (? weeks) before it is removed. This became apparent when specimens which had been kept on Ranunculus flowers for a week and were producing yellow faeces containing 100% Ranunculus pollen (plus a large flagellate protozoan) were deprived of pollen. For 24 h after pollen starvation began the faeces continued to be yellow, and contained large but decreasing amounts of Ranunculus pollen. After a further 24 h, continued pollen combing and ingestion of particles resulted in fungal hyphae and spores, at least 8 pollens besides Ranunculus, some body hairs, and some small crystals being present in the faeces. This finding probably explains why a few out-of-season pollens were among the early spring grains in the overwintered Lasiopticus pyrastri examined by Schneider (1958). It is obvious from the charcoal experiments carried out on Eristalis that particles trapped in the front tarsal bristles have to be eaten regardless of whether they are nutritive. The 53% of fungal spores in the crop of the E. tenax female were probably acquired by accidental contamination of the body hairs during nectar feeding. Pollen analysis of body surfaces and gut will not necessarily indicate all the plant species that have been visited by syrphids. Because of the arrangement of stamens or their irregular maturation or early dehiscence, pollens of some species, especially Umbelliferae {Foeniculum vulgare, Daucus), visited frequently for nectar may Holloway: Hover-fly Pollen-feeding 349 never be picked up by the pollen-collecting hairs. Whether in-flight scraping movements occur in Diptera other than Syrphidae is not known, but the cleaning movements of M. fasciatum are comparable with those of Drosophilidae, Ephydridae, Muscidae, and Calliphoridae. Increased vestiture, pollencollecting hairs, pollen-retaining bristles, and elongate mouthparts are apomorphic (derived) characters in Syrphidae, and species possessing these characters are able to gather food from a wide range of plant species. The combining of pollen- and nectargathering considerably reduces the time required for foraging, and pollen grains consumed some days after being collected, although no longer viable, would still have nutritive value. The move from direct to indirect pollen feeding in adults has been parallelled to some extent in the larvae by a change from carnivorous feeding to scavenging. Intermediate stages and various combinations between the extreme forms of larvae and adults occur. In Melangyna (Austrosyrphus) novaezealandiae (Table 1), for example, the body is slender and has a small number of curly-tipped pollencollecting hairs, the proboscis is elongate, with 33 pseudotracheal canals on each labellar lobe, and the larva is aphidophagous. The specimen of Platycheirus included in Table 1 is small, slender, shiny, and sparsely haired, with pollen-collecting hairs restricted to the sides of the thorax and with ornate legs bearing several huge pollen-retaining bristles. The proboscis is elongate and slender, with only 13 pseudotracheal canals on each labellar lobe. The larva of this species is unknown. It is very likely that in some species substantial amounts of pollen are collected by the wing membranes, and that some of the tubercles and groups of bristles on the hind legs, e.g., in Helophilus trilineatus and Merodon equestris, are involved in removing this pollen. Eristalis and some of the other large syrphids rest and feed with the wings slightly opened (Fig. 2), perhaps providing a greater collecting surface for pollen, whereas Melanostoma rests and feeds with the wings folded over the abdomen (Fig. 1), and is less likely to be contaminated with pollen grains. Although the pollen-conveying vestitute of some syrphids has been remarked upon by various authors (e.g., Kendall & Solomon 1973, Proctor & Yeo 1973) its importance as a food-collecting surface appears to have been completely overlooked. In the past it has been assumed that all the pollen ingested by Syrphidae is eaten directly from stamens. The discovery that E. tenax is using palynophilic hairs to collect pollen for its own consumption may provide a simple explanation of the apparent mimicry of honey-bees by this species and others in the genus. Brower & Brower (1965) have pointed out that in size, form, and colour-pattern the Old and
13 350 N.Z. Journal of Zoology, 1976, Vol. 3 New World species of Eristalis are all very similar, yet some of the species have evolved in regions in which honey-bees did not occur. In trying to explain how the apparent mimicry could have taken place in the absence of a specific model they concluded that "a general bee-like appearance of the genus {Eristalis) preceded the sympatry of the drone-flies and honey-bees in North America. But once the honey-bee was introduced into areas where Eristalis occurred it seems likely that the general resemblance, evolved in isolation, could then become enhanced through selection for mimicry." There can be little doubt that the morphological and behavioural similarities between E. tenax and the honey-bee are mainly the result of convergent evolution in response to similar food-gathering requirements. In both species branched hairs and spirally grooved bristles function as collectors and retainers of pollen, and leg-scraping during hovering allows transfer of pollen to take place, from hind legs to front legs in drone-flies and in the reverse direction in honey-bees. The significance, if any, of the brown and yellow colour-pattern in both species is not clear at present, but it possibly plays a part in controlling body temperature during long periods of foraging. Coloration in honey-bees is not obviously protective because it neither provides camouflage on flowers nor exhibits the typical hymenopterous warning pattern. Within the Diptera, pollen gathering by means of a specialised vestiture is probably not confined to Syrphidae. All the New Zealand species of the closely related Acroceridae have palynophilic hairs, and furthermore Oncodes brunneus (Hutton) produces yellowish faeces which could well contain pollen. ACKNOWLEDG MENTS I thank Dr N. T. Moar, Botany Division, DSIR, for carrying out the pollen analyses and for providing information about various pollens; Messrs A. P. Underhill and B. E. Eykel, Mt Albert Research Centre, DSIR, Auckland, for their patience and skill in obtaining the photographs used here, especially those of Eristalis tenax in flight (A.P.U.); also at MARC Dr N. A. Martin for collecting live material, Mr A. E. Esler for providing botanical information, and Dr R. A. Cumber for lending equipment. REFERENCES BROWER, J. V. Z.; BROWER, L. P. 1965: Experimental studies of mimicry. 8. Further investigations of honey bees (Apis mellifera) and their drone fly mimics (Eristalis spp.). The American Naturalist 99: GRINFELD, E. K. 1955: Feeding of hover-flies (Diptera: Syrphidae) and their part in pollination of plants. [In Russian.] Entomologicheskoe Obozrenie 13: KENDALL, D. A.; SOLOMON, M. E. 1973: Quantities of pollen on bodies of insects visiting apple blossom. Journal of Applied Ecology 10: MULLER, H. 1883: Diptera and Thysanoptera. Pp in The Fertilisation of Flowers (transl. D'Arcy W. Thompson). Macmillan, London. PROCTOR, M.; YEO, P. 1973: The Pollination of Flowers. New Naturalist Series, No. 54. Collins, London. SCHNEIDER, F. 1958: Kimstliche Blumen zum Nachweis von Winterquartieren, Futterpflanzen und Tageswanderungen von Lasiopticus pyrastri (L.) und anderen Schwebfliegen (Syrphidae, Dipt.). Mitteilungen der Schweizerischen Entomologische Geseltschaft 31: : Bionomics and physiology of aphidophagous Syrphidae. Annual Review of Entomology 14: VAN DER GOOT, V. S.; GRABANDT, R. A. J. 1970: Some species of the genera Melanostoma, Platycheirus and Pyrophaena (Dipt., Syrphidae) and their relation to flowers. Entomologische Berichten 30:
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