124 PARKER, as Pollina:ors [ 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 ) 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 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 ) .­ 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 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. 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 , Hakea and 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. The pollen received by the bird may well be from the protostigma, the indications being that the anthers had passed maturity at this stage. At a later stage, possibly after pollination, the corolla lobes reflex completely. I have examined also the flowers of Amyema preissii and A . maidenii. They are similar to those of L. exocarpi except that the corolla lobes are free to the base. In these too the corolla is fairly tightly closed during nectar-flow. Sargent (op. cit.) reported A. preissii as being visited by the Silvereye, and both this species and Nuytsia floribunda by the Brown Honeyeater. In India the starling Sturnus malabaricus occasionally takes the nectar of Loranthus spp. (Ali. & Ripley, op. cit.). Papilionaceae.- In July and August 1970, I noted Brachysema chambersii flowering at many localities in the Tanami Desert, N.T. The sand round the base of each bush was marked by birds' feet. The birds involved turned out to be the Masked Woodswallow Artamus personatus and Crimson Chat Ephthianura tricolor, large numbers of which were on passage through the desert. Brachysema chambersii is a small spiny shrub whose flowers are borne almost at ground-level, in a cluster protected from above by the mass of spines. The corolla is red. The five petals are tight­ fitting but in many flowers there was a ventral slit that seemed to be along the commissure of the keel. Stamens and style are free and slightly longer than the corolla. I observed the woodswallows and chats probing these flowers, presumably for their copious nectar, but was never able to see precisely the details of the operation. Whitlock (in Sargent, op. cit.) noted the Masked Woodswallow and White-browed Woodswallow visiting the flowers of Brachy­ sema daviesioides on a sandplain 30 miles west of Wiluna, W.A. The birds were "flattening themselves on the ground and even lving on their sides to get at the nectar (and insects?) within the flowers . . . "/shot two (A. superciliosus) .. . Their foreheads were thick with pollen." December J 129 1977

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Sturt's Desert Pea Clianthus formosus is another species of the arid inland of Australia. The standard and keel of its large scarlet flowers diverge from each other and the wings are very short. The Brown Honeyeater has been observed visiting the flowers for their nectar, and the Red Wattlebird noted probing cultivated specimens (Sargent, op. cit.) I surmise that this species is also visited and pollinated by the Masked and White-browed Wood­ swallows and the Crimson Chat, desert nomads that regularly descend to the ground to feed (as they do on Brachysema). The New Zealand species C. puniceus is stated (Laing & Blackwell, op. cit.) to be pollinated by birds, though they gave no details. The manner in which pollination is effected in Clianthus may be like that found in the similar Templetonia retusa. In this species a narrow slit at the junction of standard and keel leads te> the nectary. The bird, in forcing its bill into the slit, causes the keel to open and expose the pollen-laden anthers, which dust the bird on the throat or crown (depending which way up the bird is.) In another pea discussed by Sargent, Crotalaria cunninghamii, the keel is conical with a tiny opening at the apex through which pollen is forced when a bird probes the nectary. Other legumes thought to be pollinated by birds include species of Butea, Acrocarpus, Erythrina, Sophora, * see POSTSCRIPT, and Swainsona. Mimosaceae.- Sargent recorded his own interesting observa­ tions on the pollination of Acacia celastrifolia. In this species the nectaries are extrafloral, being situated on the edge of the phyll­ odes. The distance between flower and nectary rules out pollination by the many insects that are attracted to the latter. Sargent observed, however, that Silvereyes feeding on the nectaries came into contact with the flowers at the same time. I have not covered all families in which bird-pollination is known or suspected to occur. Of the remainder perhaps the most important is the Myrtaceae, examples being known in , Angophora, Melaleuca, Beaufortia, Calothamnus, Metrosideros, Careya and Syncarpia. Other families include the Bombacaceae, Sterculiaceae, Capparidaceae, Bignoniaceae, Myoporaceae, Cacta­ ceae, Orchidaceae, Agavaceae, Musaceae, Passifloraceae, Cam­ panulaceae, Epacridaceae and Onagraceae. DISCUSSION Sargent ( op. cit.) speculated on the origin of bird-pollination. It is likely that birds were first led to probe flowers for insects and for nectar as water rather than as a sweet-tasting source of energy. As the birds tapped the nectar, the flowers were pollinated. Sub­ sequent adaptations in many birds and flowers have improved the efficiency of this relationship. The most successful nectar-feeding birds have long fine decurved bills and fimbriated or tubular tongues. Flowers pollinated mainly or solely by birds are pre­ dominantly red (also orange, yellow and cream), discharge copious nectar and are large or in large inflorescences. The nectar is often in a sealed corolla or nectary not very accessible to insects. Often December J Birds as Pollinators 131 1977 the outside of the perianth is bristly or hairy and the tube blocked inside by a zone of hairs, again presumably to discourage insects. The stigma is small and pollen and stigma are brought into contact with the bird as it feeds. The flowers have little scent and lack the special landing-stages found in some insect-pollinated plants. Pro­ tandry is common. The dependence of such flowers on birds has never, to my knowledge, been systematically studied, but I suspect that in many instances it is total. The botanist Sargent was in little doubt as to the situation in Eucalyptus: "The author has found no trace of pollen on the body of any insect-visitor of a "gum" blossom so far examined (his observations covered 25 years) ... if honey-eating birds became extinct the eucalyptus would probably speedily fo llow them." Nor could he conceive of kangaroo paws without honey­ eaters. Clianthus puniceus of New Zealand is dwindling to extinc­ tion on the main islands (Laing & Blackwell, op. cit.). If this pea is pollinated by the nectar-feeders Prosthemadera, Anthornis, Notiomystis and Creadion one might look no further for the reason beyond the fact that these birds too are now extinct in many areas, Notiomystis in particular being found only on Little Barrier Island.

Bird-pollination was not considered (Ehrlich & Raven ( op. cit.) when they wrote: "In tropical rainforest, trees of a given species are often separated by considerable distances. Here it would appear that either strong-flying selective pollinators must actively seek out individuals or self-pollination must be prevalent." Oliver ( 1930) considered that Prosthemadera and A nthornis were im­ portant in the pollination of forest trees in New Zealand. One wonders how the remaining forest trees of the Hawaiian group are faring; for most species of their chief pollinators, the Hawaiin honeycreepers (Fringillidae, Drepanini) and the mohos (Melipha­ gidae), have been wiped out by introduced diseases and rats (Greenway, 1967). The prevalence of bird-pollination in tropical forests and its decreasing incidence towards the higher latitudes may, I suggest, be due to the fact that species-diversity decreases away from the tropics, resulting in more homogeneous forests in higher latitudes in which trees of a given species are closer to­ gether, rendering wind- and insect-pollination adequate (i.e., no selection-pressure for long-range vectors). Recher & Abbott ( 1970) comment on the large numbers of honeyeaters wintering in the Hawkesbury Sandstone area, N.S.W., compared with the small number of strictly insectivorous birds then present: "Possibly insects are not sufficiently abundant ... to support a diverse population of insectivorous birds, but the large assemblage of many species of honeyeaters occur because honeyeaters obtain their energy requirements from nectar and need insects only as a source of protein." This is probably the situation with nomadic nectar-feeders in much of the arid zone of Australia. 132 PARKER Bird [ Watcher

In the Tanami and Simpson deserts, insects and strictly insec­ tivorous birds are low in numbers. When rains cause the blossom­ ing of nectariferous Grevillea, Hakea, etc., great numbers of wood­ swallows, honeyeaters and crimson chats move into the area. Presumably they can subsist on the low populations of insects because they exploit the nectar for energy. In turn the desert flowers are pollinated, a task for which the insect numbers may not be sufficient. It is worth considering too the probability that these highly mobile and nomadic birds carry pollen hundreds of miles in a very short time, distances that far exceed Ehrlich and Raven's theoretical limits for gene-flow. REFERENCES Ali, S. & S.D. Ripley, 1972. Handbook of the Birds of India and Pakistan, 5. OUP. Ehrlich, P. R. & P. H. Raven, 1969. Differentiation of populations. Science 165: 1228-1232. Gardner, L. L., 1925. The adaptive modifications and the taxo­ nomic value of the tongue in birds. Proc. U.S. nat. Mus. 67 (19): 1-49. Greenway, J. C., 1967. Extinct and Vanishing Birds of the World. 2nd rev. ed. New York: Dover Pubis. Ingram, G., 1972. Notes on the feeding of White-browed Wood­ swallows (Artamus superciliosus). Sunbird 3: 64-65. Jenkins, C. F. H., 1968. Pollination of Kangaroo Paws. W. Aust. Nat. 11: 19. Knuth, P., Handbook of Flower Pollination. Trans. J. R. Ains­ worth Davis. Vol. 3 (1909). Oxford: Clarendon Press. Laing, R. M. & E . W. Blackwell, 1964. Plants of New Zealand. 7th ed. rev. E . J. Godley. Whitcombe and Tombs. McKean, J. L., 1969. The brush tongue of Artamidae. Bull. Brit. Om. Club 89: 129-130. Mees, G. F., 1967. A note on the pollination of the Kangaroo Paw Anigozanthos manglesii. W. Aust. Nat. 10: 149-151. Oliver, W. R. B., 1930. New Zealand Birds. Wellington: Fine Arts (N.Z.) Parker, S. A., 1973. The tongues of Ephthianura and Ashbyia. Emu73 : 19-20. Rand, A. L., 1967. The flower-adapted tongue of a timaliine bird and its implications. Fieldiana, Zool. 51: 53-61. Raven, P. H . & H. Curtis, 1970. Biology of Plants. New York: Worth. Recher, H. F. & I. J. Abbott, 1970. The possible significance of hawking by honeyeaters and its relation to nectar feeding. Emu 70: 90. Recher, H. F. & I. J . Abbott, 1970. Some differences in use of habitat by White-eared and White-cheeked Honeyeaters. Emu 70: 117-25. Robinson, A. H., 1947. Spinebill Honeyeaters and Dryandra nivea. W. Aust. Nat. 1: 67. December J Birds as Pollinators 133 1977

Sargent, 0. H., 1928. Reactions between birds and plants. Emu 27: 185-92. Sedgwick, E. H., 1969. Birds and Kangaroo Paws. W. Aust. Nat. 11: 65-66. Serventy, D. L. & H. M. Whittell, 1967. Birds of Western Aust­ ralia. 4th ed. Perth: Lamb.

POSTSCRIPT August 21 1973: I observed Red Wattlebirds probing the odourless red flowers of an introduced Erythrina tree (Papilion­ aceae) and picked flowers for examination. The nectar is contained between the keel petals, and flows after the flower has opened. The style is eventually longer than the stamens, and the stigma is turned upwards. Possibly the species is protandrous; for the anthers of the opened flowers were nearly all withered. Not a trace of pollen was found on any of the structures. The flower is ideally suited to pollination by birds standing in the centre of the inflorescence and inserting their bills from behind and above: their crowns would be touched by the stigma. T he Red Wattlebirds were seen feeding in this position, and also from below and in front of the flower, in which case they would not come into contact with the stigma. Considering the distance between the nectar and the stigma, pollination by insects is pre­ sumably impossible. [See also(i) Ford, H . A. & N. Ford, 1976. Birds as possible polli­ nators of A cacia pyenantha. Aust. J. Bot. 24: 793-5. (ii) McCulloch, E., 1977. Adaptations by birds to feed at flowers, the nectar of which is not readily available. Aust. Bird Watcher7 (4): 113-123. (iii) Paton, D. C. & H . A. Ford, 1977. Pollination by birds of native plants in South Australia. Emu 77: 73-85. Hon. Editor]