124 PARKER, Birds as Pollina:ors Bird [ Watcher Birds as Pollinators by S. A. PARKER, Curator of Birds, South Australian Museum, North Terrace, Adelaide, South Australia, 5000. INTRODUCTION Ehrlich & Raven ( 1969) contended that gene flow in nature is much more resricted than is commonly thought. They discussed among other examples the case of wind-pollinated plants. In Zea mays (Poaceae) cross-pollination at distances greater that 18.3 m has been shown to be 1% ; in Beta vulgaris ( Chenopodiaceae) cross-pollination between plants 200 m apart is 0.3%. Studies on Pinus coulteri (Pinaceae) have shown that the bulk of the pollen is dispersed 3-9 m downwind of the parent, with very little beyond 46 m. Among insect-pollinated species similar very short distances for cross-pollination have been demonstrated, exceptions being such species as Oenothera organensis ( Onagraceae), which is pollinated by strong-flying hawkmoths. The authors concluded in plants there was considerable evidence that distances of from 15 m to a few miles may effectively isolate populations, and that there was no evidence of longer-range gene flow. In view of the fact that Raven & Curtis ( 1970) state that many species of birds serve as pollinators, it is noteworthy that Ehrlich & Raven ( op. cit. ) make no mention of this. Birds probe flowers for three reasons - to obtain nectar (a source of carbohydrates), pollen (a source of proteins) or insects. The rifling of the flower by the bird generally results in the dusting of the latter with pollen, often in large amounts. The pollen may adhere to the bird for a considerable time (indefinitely in museum skins), and cross­ pollination may occur when the bird visits another plant of the same species. The implications of birds as pollen-vectors are profound. The subject is a neglected one, however, a no-man's-land between botany and ornithology. In the systematic list of flower-visitors in volume 3 of Davis's (1909) translation of Knuth's Handbook of Flower Pollination, for instance, no mention is made of birds. Of several modern botanical texts consulted, some discussed bird­ pollination briefly, others treated wind- and insect-pollination only. Below I present some notes on nectar-feeding and the role of birds in pollination. ADAPTATIONS OF THE AVIAN TONGUE TO NECTAR-FEEDING Although curling, splitting and fraying of the tongue-tip occurs in many families of birds (Gardner, 1925), in eleven only are these conditions carried to an extreme for nectar-feeding, and even within these not all species have such modifications equally pro­ nounced. In nectar-feeders the tongue is usually fimbriated at the tip (the brush-tongue effect, as in most honeyeaters) or longi­ tudinally curled into a tube or pair of tubes (as in hummingbirds December J Birds as Pollinators 125 1977 and many sunbirds) or both (as in Myzornis and Chloropsis; see below). These adaptations increase by capillarity the amount of nectar absorbed onto the tongue, though in the tube-tongued species it may be that nectar is also actively drawn up. The three families in which these tongue adaptations are typical are the Trochilidae (hummingbirds, ca 320 spp.), Nectariniidae (sun birds, ca 116 spp.), Meliphagidae (honeyeaters ca 171 spp.) and Ephianuridae (Australian chats, 5 spp.). Other families in which they are present but less pronounced or less frequent include the Philepittidae (Neodrepanis only), Timaliidae (babblers; Myzor­ nis only), Chloropseidae (leafbirds), Fringillidae (tribes Parulini, Drepanini, Icterini, Coerebini), Dicruridae ( drongos), Artamidae (woods wallows), Dicaeidae ( flowerpeckers) and Zosteropidae (white-eyes). In addition several species of Sturnidae (starlings) are inveterate nectar-feeders but modification of the tongue has been demonstrated so far only for the aberrant South African Frame­ raps, which pollinates species of Prot ea. Some Oriolidae (orioles) also feed frequently on nectar but their tongues have not been examined. (See Rand, 1967; Ali & Ripley, 1972; Parker, 1973). SOME FLOWERS VISITED BY BIRDS Liliaceae: Xanthorrhoea. - The highly nectariferous flowers of this genus form dense upright spikes. The stamens are exserted and the tiny stigma protrudes a little beyond them. At least three species (including X. drummondii and X. preissii) are known to be visited by birds: Black-faced Woodswallow Artamus cinereus, White-browed Woodswallow A. superciliosus, Brown Honeyeater Lichmera indistincta, White-cheeked Honeyeater Phylidonyris nigra, Singing Honeyeater Lichenostomus virescens, Red Wattlebird Anthochaera carunculata, Blue-faced Honeyeater Entomyzon cyanotis and Noisy Friarbird Philemon corniculatus, (Sargent 1928, Ingram 1972). Amaryllidaceae: Anigosanthos (formerly Anigozanthos) .­ Mees (1967) was the first to demonstrate that A. manglesii was pollinated by birds, though this had been hinted by Sargent ( op. cit.). The red perianth of this species (fig. 2) is a decurved tube ca 8 em long with a slit running the length of the undersurface in mature flowers. The six anthers are large, almost sessile, and arise near the mouth of the perianth. The style is entirely free and as long as or a little longer than the perianth. A bird seeking nectar usually inserts its bill into the ventral slit near the base, causing the tube to buckle in the middle. T his brings the stigma and anthers down to touch the bird on the dorsum, anywhere from the nape to the rump depending on the bird's size. Mees concluded that pollination of the species by insects was unlikely, and that it was effected solely by birds. Jenkins (1968) and Sedgwick ( 1969) supplemented Mees' observations. It is now known that at least four of the eight species of Anigosanthos (A. manglesii, A . bicolor, A. viridis, A . flavida) are visited by birds, those recorded being 126 B~ [ Wa~h er Meliphagidae : Ephthianura tricolor (afte£ Parker 19 73) Meliphagida e : Fringillidae , Drepanini Apalopteron famjliare Vestiaria coccinea ( a fter Rand 1967) (after Rand 1967) Artami dae : Artamus superciliosus (after McKean 1969) TONGUES OF SOME NECTAR - FEEDING BIRDS December ] Birds as Pollinators 127 1977 the Western Spinebill Acanthorhynchus superciliosus, Red Wattle­ bird, Brown Honeyeater, White-naped Honeyeater Melithreptus lunatus, New Holland Honeyeater Phylidonyris novaehollandiae and Silvereye Zosterops lateralis. Proteaceae.- Many species in this family are visited by birds for their copious nectar, and are well situated for bird-pollination. Banksia and related genera are protandrous: by the time the flower has opened the anthers have matured, shed their pollen on the protostigma, and withered. The protostigma deposits the pollen on visiting birds, who may subsequently rub it off onto a more mature stigma. Birds visiting the spikes of this group may, apart from receiving pollen on the head from the particular flower they are probing, also be dusted elsewhere as they brush against other parts of the inflorescence. Numerous species of Banksia have been recorded as being visited by birds, the latter including Brown Honeyeater, White-naped Honeyeater, White-cheeked Honeyeater, Western Spinebill, Red Wattlebird, White-eared Honeyeater Lichenostomus leucotis and Dusky Miner Manorina obscura. The New Zealand Rewa-rewa Knightia excelsa has a similar pollinating mechanism. It is much visited by the Tui Prosthe­ madera novaeseelandiae and the Bellbird Anthornis melanura (Meliphagidae), who, pushing their bills into the newly-opened flowers, receive pollen on their foreheads from the protostigma (Laing & Blackwell, 1964). Several species of Dryandra are visited by birds. In D. nivea the flowers are borne round the edge of a disc, giving the inflores­ cence a cup-like shape. A bird seeking the nectar that pours from the flowers to the bottom of the cup, brushes against many of the inturned stigmata, and small species like the Western Spinebill may quite immerse their heads in these blossoms (Sargent op. cit.; Robinson 1947). In Adenanthos, Hakea and Grevillea the style is finally much longer that the perianth, emerging between the lobes and curving round beyond the mouth with the stigmatic surface turned towards the axis of the flower. Presumably the anthers mature first and the pollen is shed upon the protostigma, which assumes an ideal position for brushing the throat or forehead of a probing bird. Species of these three genera were reported by Sargent ( op. cit.) as being visited by birds. In the southern Northern Territory I have seen the Black Honeyeater Certhionyx niger, Grey-headed Honeyeater Lichenostomus keartlandi and White-fronted Honey­ eater Phylidonyris albifrons probing the red flowers of Grevillea wickhamii (Fig. 3). · Loranthaceae.- It is fairly well known that some birds aid in the dispersal of mistletoe seeds. The Mistlethrush Turdus viscivorus feeds on the sticky berries of Viscum album, wiping the seeds off its bill onto branches. The Australian Mistletoe-Bird Dicaeum hirundinaceum eats mistletoe berries and passes the seeds through its body; when defaecating it obligingly sits along, not across, its perch so that the voided seeds become attached to the branch ·- 128 PARKER Bird [ Watcher (Serventy & Whittell1967: 371). It is less well known that birds serve as pollinators of some mistletoes. At Idracowra, southern N.T., in May 1970, I noted White-fronted Honeyeaters probing the red flowers of Lysiana exocarpi, which was growing in masses on Acacia victoriae and A . ligulata. Flowers examined were about one-third filled with nectar. One of the honeyeaters was collected and its crown found to be covered with pollen, subsequently identified as that of the mistletoe. The corolla of L. exocarpi (Fig. 1) is decurved and six-lobed, the ventral lobe being free for a greater distance than the rest, about half the length of the corolla. The anthers arise near the distal ends of the lobes. During nectar-flow the corolla is fairly tightly closed, possibly to keep insects out, but yields to the probing of a bird's bill. As the bill is inserted the lobes give outwards, the ventral lobe for half the length of the tube, which would encourage the bird to work the flower from below.