Bombylius major, Linnaeus, 1758

Leins, Claudia Erbar Peter, 2013, Nectar production in the pollen flower of Anemone nemorosa in comparison with other Ranunculaceae and Magnolia (Magnoliaceae), Organisms Diversity & Evolution (New York, N. Y.) 13 (3), pp. 287-300 : 288-292

Bombylius major

In spring 2010 (19 April), between 12.30 noon and 2.30 pm, in a beech forest near Heidelberg (Reilingen) we observed the major bee-fly, Bombylius major , visiting flowers of Anemone nemorosa (Figs. 1–4). Several individuals of Bombylius moved rapidly from flower to flower in the relatively dense population of Anemone nemorosa . Bombylius usually hovers next to the plant, then approaches the flower and rests with its legs on the flower to stabilize its hovering when feeding (Figs. 3–4). When the insect holds onto the flower, it buzzes more or less constantly with its wings. Only occasionally, when flower-visits last some time, is the buzzing briefly interrupted (Fig. 1). The insects visited the white, proterogynous flowers in the female and the early male as well as in the late male phase of anthesis. In between, Bombylius visited the blue-violet flowering Vinca minor ( Apocynaceae ; Fig. 6) and Viola riviniana ( Violaceae ). In both, the insect is rewarded by copious nectar. The long mouthparts of the bee-flies reach deep into the corolla tube of Vinca and the spur of Viola . During the period of observation (between noon and early afternoon) no liquid nectar could be observed in the Anemone flowers. Nevertheless, occasionally glistening of nectar drops (in limited quantity) was visible (Fig. 5, arrow), which may occur when flowers have not been visited by insects for some time.

The bee-flies visiting Anemone nemorosa at our study site did not consume pollen out of the anthers. Instead, after probing at the bottom of the flower they spread the labella and, in doing so, they presumably dissolve solidified nectar in saliva (Figs. 1–2).

nectar. Fig. 6 B. major visiting Vinca minor ( Apocynaceae ). Fig. 7 Tip of the proboscis of B. major , spreading labella make the hypopharynx visible. Figs. 8–9 Nectar in a just-opened flower of A. nemorosa . Hyp Hypopharynx, La labellum

The rigid, needle-like proboscis (ca. 10 mm long, formed by labrum, labium and hypopharynx) is adapted for sucking nectar deep in flowers. It is projected forwards more or less horizontally and cannot be retracted. The paired labella, however, are flexible (Fig. 7) and make initial contact with substances to be ingested. If the labella are pressed tightly together, the proboscis is used to suck up liquid nectar (Fig. 10). If the slender labella are spread at right angles to the axis of the proboscis as observed during the visits of Anemone flowers (Figs. 1–2), the labella are also involved in food uptake but, at the bottom of the Anemone flower, they come into contact only with dried up nectar. Each labellum is traversed on its inner side by three pseudotracheae, i.e. canals that extend in the longitudinal axis of the proboscis (Figs. 7, 11–14). These tube-like structures have openings for the discharge of saliva. The outflowing saliva can dissolve the solidified nectar. The fluid is then conducted along furrows that are formed by interpseudotracheal folds ( Figs. 13 –15).

Flower of Anemone nemorosa and nectar secretion

Anemone nemorosa , the wood anemone or windflower, is a long-lived perennial, and is a common, often dominant, understorey spring herb of European (and also Asian) deciduous woodland, and naturalised in parts of North America. Its creeping rhizomes can make wide-spreading carpets. The solitary flowers are 2 cm in diameter, with mostly six (or seven) tepals with many stamens (mostly about 45) and a choricarpous gynoecium (about 10–20 carpels). The sepals are usually white inside, sometimes slightly tinged with pink outside. The flower is held erect during the day, but closes and droops at night and in bad weather.

Looking for nectar in the field may yield only limited success. At midday or in the afternoon, one may sometimes see some glistening of nectar at the base of the carpels (Fig. 5, arrow). Only with a dissecting microscope could we detect copious nectar in flowers that had just opened (Figs. 8–9; flowers collected on 13 April 2012, early in the morning).

The carpels are hairy all around their lower part (Fig. 16). The hairs are unicellular with a somewhat dilated base (Figs. 17–18). The epidermal cells between the hairs are striking. Sometimes they form a group around the base of the hair (Fig. 18). The epidermal cells in the area of the hairy part differ from those of the upper part of the carpel; they are smaller, more papillate and stain (with toluidine blue) deeper due to their dense protoplasm (Figs. 20–23). Nectar should be secreted by the epidermis in the ovarian part of the carpel; however, there is no underlying nectar tissue. We were unable to determine whether the hairs also secrete nectar. In any case, they hold the nectar. Stomata could be found only in the stylar region above the ovary (Figs. 19, 22), where they may serve in gas exchange. In some cases we found crystallized nectar in the SEM preparations due to nectar rising above the hairy region in flowers where much nectar was produced (Fig. 19). We obtained identical results in flowers of Anemone nemorosa sampled at four different sites in Germany (see Material and methods).

Nectaries in other Ranunculaceae

Flowers of many members of the Ranunculaceae offer nectar besides pollen. As examples, the different sites of nectar secretion were demonstrated in selected species ( Ranunculus aconitifolius , Pulsatilla turczaninovii , Clematis alpina , Caltha palustris ) and for comparison in Magnolia stellata ( Magnoliaceae ).

In many genera, nectar is secreted in special nectary organs, which are formed between perianth and androecium. These variously shaped nectary organs are often showy and take over petal function, as for example in Ranunculus (Fig. 24). In Ranunculus acris , like in most species of this genus, a scale covers a nectar-secreting pit, at the base of which nectar tissue can be found. In the white-flowering Ranunculus aconitifolius the scale is not a flat structure but tubular (Fig. 30). At the time when the stamen primordia have already differentiated into anthers and short filaments, the primordia of the nectary organs in Ranunculus aconitifolius are small and flat. The primordia may exhibit slight depressions (Figs. 31–32) due to pressure from contiguous stamens. Differentiation of the nectary organs starts with the formation of a horseshoe-shaped bulge at the ventral base of the young nectary organ (Figs. 31–32). Soon afterwards the upwards pointing ends come into contact, forming a ring-like structure (Fig. 33). By further unequal upgrowth the bowl-shaped structure changes into a obliquely tube-shaped scale whose longer part may be entire or slightly two-lobed (Fig. 30). A massive nectar-secreting tissue of small, plasma-rich cells lies at the base of the tubular scale (Figs. 34–35). Nectary slits could not be detected.

In the Siberian pasque flower, Pulsatilla turczaninovii , plenty of nectar is secreted, mainly during the early female phase of anthesis (flowers are proterogynous; Fig. 25). The nectar is secreted by the outer short, club-shaped sterile stamens (staminodes), either from the filament or from the entire staminode (Figs. 36–37).

Clematis alpina has outer spatulate staminodes (Figs. 26, 38). However, it is not these staminodes, but rather the fertile inner stamens that are the site of the nectary—strictly speaking the ventral side of their filaments (Fig. 39). Nectar is secreted by the epidermis in an oval area (Figs. 40–42). In this area the epidermis differs from that of the surrounding area: there are deep longitudinal furrows between the secreting cells (Fig. 41), perhaps capillary nectar holders.

Caltha palustris —the kingcup or marsh marigold (Fig. 27)—exhibits a carpellary nectary. At anthesis, flowers of Caltha have droplets of nectar between the carpels (Fig. 28). On either side of each carpel, there is a basal group of approximately 100 unicellular, clavate trichomes that are responsible for nectar secretion (Figs. 43–46).

In Magnolia stellata , nectar secretion is found only at the beginning of anthesis (the flowers are proterogynous; Fig. 29). Small droplets are produced in the region of the style and the ovary. There is no localised nectary tissue below the epidermis (Figs. 50–51), but the epithelial nectary covers the whole carpel from style (Fig. 52) to ovary (Fig. 53). In objects prepared for SEM investigation, the surfaces of the carpels are coated by a granular material, presumably solidified nectar (Figs. 47–49). Nectar secretion is through the epidermal cell wall. Stomata (Fig. 48) may only serve in gas exchange.

stylar area; arrow transition area of both parts. Fig. 20 Transition area at higher magnification. Fig. 22 Cross section through the style; note the large, ± unstained epidermal cells; arrow stoma. Fig. 23 Cross section through the ovary; note the cytoplasm-rich and thus more intensively stained epidermal cells (carpellary epidermal nectary). O Ovary, Ov ovule, Sty style