D~cember J McCULLOCH, at Flowers 113 1977 Adaptation by Birds to Feed at Flowers, the of which is not readily Available. By ELLEN M. McCULLOCH, 6 Bullen Ave., Mitchum, Victoria, 3132. Drawing by ANTHEA FLEMING

My interest in studying the adaptation of birds benefiting from exotic flowers was first aroused by seeing Eastern Acanthorhynchus tenuirostris feeding from camellias. The birds' long slender bills seemed ill-adapted to collecting nectar from the open flat flowers, but they persisted at the Sasanqua camellias, an early-flowering variety blooming when there is little else out in my garden. I have also been told of Little Wattlebirds Anthochaera chrysoptera at camellia blossoms. Since then, I have noted various reactions of birds to flowers both Australian and exotic. It is generally assumed that Australian birds such as and the nectar-eating parrots which visit flowers for nectar and pollen invariably act as pollinators by transferring sticky pollen caught either on head, back, or throat. At times honeyeaters are seen with bright orange or yellow patches which on close inspection are seen to be thickly encrusted pollen. There are examples of what appear to be by Australian specifically for pollination by some birds species. G. F. Mees (1967) points to the pollination of the Western Australian Kangaroo Paw Anigosanthus manglesii by the Western A. superciliosus, where the 's back becomes powdered with pollen as nectar is collected from the base of the almost hori­ zontal flower. I have not seen birds at Kangaroo Paws here in the eastern States where the Western Australian floral emblem has been extensively planted in gardens. I have been told that a number of honeyeaters do visit them, and the well of nectar in the flower is apparent. I have seen flowers of a red 'paw' which seemed to face upwards almost vertically in bunches, both with holes pierced at the base, and slit to the base. Kangaroo Paws here would pre­ sumably be as alien to birds as a Chinese abutilon or a South African protea. In Melbourne gardens Silvereyes Zosterops lateralis and White­ plumed Honeyeaters Lichenostomus penicillatus are very common. Both species have learned to pierce the base of some of the tube­ shaped flowers, or make a slit from the lip down to the base to reach the nectar. Flowers found so damaged/utilised include Lachenalia, Correa, some , Kniphofia (Red-hot Pokers) , several aloes, and tecoma, many of which are very rich in nectar. I admire the birds' ingenuity but some of my more garden concious friends do not. 114 McCULLOCH Bird [ Watcher

One shrub which really attracts the birds at the Maranoa Gar­ dens in the Melbourne suburb of Balwyn is the Green Birdflower laburnifolia. The large yellow-green pea-shaped flowers are stripped right off, or are almost shredded, in the birds' eagerness to get to the nectar. I do not think this is due just to destructive curiosity, as seems to be the case with parrots nipp:ng off some garden flowers. Some Crotalaria are found pierced with a small, fairly neat hole. In these gardens Silvereyes, White-plumed Honeyeaters, Red Wattlebirds Anthochaera carunculata and Little Wattlebirds have all been seen at these shrubs. I have not been fortunate enough to see what I know to be a perfect flower pierced for the first time. I have now seen Crotalaria similarly treated in three other suburbs. Hive , ants and other insects all take adv<:mtage of the flower once it has been so opened. There are about 300 species in the genus Crotalaria, spread widely throughout the tropics and sub-tropics. Several species are found across central and northern . What the normal pollinating agent is I have not been able to discover. The genus propagates by setting seed, from which new plants grow. Many pea-shaped flowers are pollinated by insects, including bees. One example given me by Dr. D. Langridge (Pers. Comm.) is of lucerne flowers, on which the anthers fly upwards to hit the b;;e from underneath as it straddles the keel. (Some bees can get their nectar without pollinating the flower by intruding the tongue from the side.) In his paper "Reactions between Birds and Plants" ( 1928) O.H. Sergent states that although the majority of our numerous native pea family are probably pollinated by bees," ... Three certainly, and others probably, require and receive the attention of birds". The three species referred to were Cocky's Beak Templetonia retusa, Sturt's Desert Pea Clianthus formosus and Crotalaria cunninghamii. He includes the Brown Lichmera indistincta and Singing Honeyeater Lichenostomus virescens as visiting the Crotalaria on the record of F. L. Whitlock as observer, but unfortunately does not give details of how the birds behaved at the flowers. It would appear to be biologically disadvantageous (if not disastrous) for a flower to be usually destroyed or mangled while pollination is effected or nectar is being obtained. Therefore it seems to me that either Crotalaria is not a "bird-adapted" flower or the wrong birds are sometimes attracted. Simple slitting or piercing of the flower tube may not affect the pollination and subsequent seed-set. During discussions it was suggested to me that the suburban situation is so artificial that birds there have become opportune feeders almost by accident and that it was unlikely that such nectar collection would occur elsewhere. I have frequently seen correas in bush areas pierced at the base of the flower, and some­ times mistletoe flowers split or torn open. In July, 1975, for the first time I saw Crotalaria cunninghamii Ma..raJ'-Otl- {jan:lu1s, :Ba.t""f"' , lite. F!tr-iL 3, 191.<;.

RM F. 116 McCULLOCH Bird [ Watcher

growing in a natural state in the Macdonnell Ranges west of Alice Springs, N.T. There were only five blooms on the rather straggly specimen, but I found (much to my satisfaction, I admit) that four of these had been pierced on the keel. White-plumed Honeyeaters were recorded in the area, and it would be hard to find a situation less like suburban Melbourne. Charles McCubbin (Pers. Comm.) states that on a visit to the Simpson Desert, N.T., when there were many Crotalaria sp. bushes in bloom he did not notice any birds at the blooms. Additionally, the flowering Crotalaria bushes were spread out across the desert far away from the fringe areas where any honeyeaters were seen. It is not only tubular or pea-shaped flowers which birds learn to utilize. Some flowers have wide open petals, but have the nectar hidden, for example Hibiscus and the orange-flowered Chinese Abutilon Abutilon darwinii. White-plumed Honeyeaters and Red Wattlebirds find that though they cannot reach the nectar from the front of the pendant flower of the Abutilon, by perching on the back of it and inserting the beak between and behind the over­ lapping petals they can reach into the sweet reservoir. Similarly Little Wattlebirds have been recorded on Hibiscus (A. Swan, Pers. Comm.). Sometimes the tough green calyx is split during these attempts. In November 197 6 on the property of C. Barraclough at Heales­ ville, Victoria, I saw hundreds of naturalized Foxgloves Digitalis purpurea in bloom. Several groups of the flowers, particularly those growing near the creek, contained blooms all the way up the stem which had been slit or pierced at the base. Yellow-faced Honeyeaters Lichenostomus chrysops, Eastern Spinebills and Lewin Honeyeaters Meliphaga lewinii were recorded on the flowers. Honeybees flew straight to the base of the pierced blooms and went in through the perforation instead of crawling in through the opened end of the trumpet. Some individual birds never seem to be inquisitive enough to explore and exploit, though I have seen birds in a flock one after the other search the Abutilon. In another area Abutilon may not be touched at all. My limited search of the literature shows that in many areas of the world nectar is taken from flowers by both birds and insects which pierce the flower from the outside, thereby by-passing the evolved pollination mechanism (disadvantageous botanically and biologically as this may be). References come from South Ameri­ ca, South Africa, Asia, England and several areas in Australia, and there are undoubtedly many more unknown to me. V. B. Wigglesworth (1964) states (p. 272) "In Europe where we have no humming-birds, the Tropaeolum (Nasturtium) is attractive particularly to bumble-bees. But the short-tongued bumble-bees cannot reach the nectar by the normal route; they bite into the wall of the spur and rob the nectar from outside without effecting pollination. Indeed the short-tongued bees have learned to rob many flowers this way." In their native Peru, Nasturtium are normally pollinated by humming-birds. December ] 117 !977

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W. W. Howells, (1971) states (p. 108) (re Coppery Sunblrd N ectarinia cuprea of South Africa) - "Although de­ cidedly an insect-eater, both male and female were seen on several occasions to be feeding from nectar-bearing flowers. The birds use both common methods of obtaining nectar from flowers, i. e. puncturing the base of the flower and p<:ssing the bill down the flower tubes." E. Thomas Gilliard (1958; p. 351) states "To obtain nectar some species such as the Oriental White-eye peck holes in the calyx (basal part of the flower) of such flowers as Hibiscus. In southern Asia at certain seasons hardly a flower can be found that has not been pierced." C. J. Skead (1967; p. 50) .states "re Burchellia bubalima . .. to the human tongue its nectar is sweetest of all. So heavily are the flowers drawn on by the birds that it is possible to examine the many dozens of florets on a single bush without finding any nectar in them. And where Collared Sunbirds and White­ eyes occur near Burchellia, scarcely a flower-tube is entire, Each is ripped down the length of its side with a clean slit, the gate­ way to a nectar supply otherwise denied the birds because their short bill-length cannot reach the full depth of the corolla tubes." 118 McCULLOCH Bird [ Watcher

Many other examples are given in this interesting book, including the one of Lesser Double-collared Sunbirds dying from what was diagnosed as "an accumulation of coagulated latex. This had been ingested incidentally, bit by bit, whenever the bird pricked the petals of the introduced rubber tree Manihot galziovii in order to get at the nectar. Each prick had allowed latex from the petals to exude . . . " The South American Flower-piercers (genus Dig/ossa); Family Ceorebidae: (Honeycreepers) are referred to by many authors. These birds have a hook on the upper mandible with which they hold the flower. Ed. Peter Scott "The World Atlas of Birds" (1974; p. 93) re Masked Flower-piercer Dig/ossa nyanea "The Masked Flower-piercer alights near the head of a mountain flower and, holding the base of the bloom with the finely hooked tip of its upper bill, drives the sharp lower mandible through the petals. In a raid lasting only a second, the bird extracts the flower's store of nectar through the tiny hole with darting movements of its slender, brush-like tongue." Rodger Elliot (Pers. Comm.) told me that on a visit to the Grampians in Victoria in 1974, it was difficult to find one bloom of Correa lawrenciana which was entire. At Jumping Creek Reserve, Warrandyte State Park at Warran­ dyte, Victoria, on June 15, 1976, of 39 green flowered bushes growing along the river bank, only 9 bushes had 100% whole blooms. These nine bushes were close together, in heavy cover and were sparsely flowered (two plants had only three flowers on each of them). On each of the other 30 vigorously flowering bushes some of the flowers had been pierced or slit. Some had only two or three flowers damaged; on others, groups of six or seven flowers close together were affected. Buds on a number had been pierced before opening. Presumably nectar is not at its peak then, if it is present at all. On this date the Correa flowering was at various stages on the same bush from tight small buds, to longer buds, open flowers and dying spent flowers. Obviously if nectar is at its peak with pollen when the flower first opens fully, as seems to be assumed/sugges­ ted in most literature, good nectar flow is available from a Correa bush over its long flowering period, and this applies to many other species. On that visit honeyeaters heard or seen in the vicinity were White-plumed, White-eared Lichenostomus leucotis, Bell-Miners, Manorina melanophrys and , though the area list contains others. No birds were recorded on the bushes. Mrs. B. Armstrong (Pers. Comm.) reports of a Western Aust­ ralian wildflower Balaustion pulcherrimum (Native Pomegranate) that in one area in 1975, a large proportion of the small orange trumpet-shaped flowers of this prostrate had been pierced. Blossoms of Correa mannii in a garden in the Little Desert area, Victoria, are sometimes found littering the ground and the White­ eared Honeyeater is suspected. Bees find the freshly picked blos­ soms on the ground. December J ] 19 1977

Slit

1

G. Ambrose (in Litt.) found that of 117 green flowers of Correa sp. examined at La Trobe University Wildlife Reserve on July 5, 1975, 64 were intact (those nearest the ground tended to be intact) and 53 were pierced or slit. On June 6, 1976, when visiting the B.O.C. Centre at Yellingbo, Victoria, I inspected flowering bushes of garden varieties of Correa and planted there. On every bush in flower there were samples of the piercing of bloorns, some 20 bushes having flowers fully out. In some cases the tube corollas of the were so 120 McCULLOCH Bird [ Watcher

narrow and small, even at the basal swelling, that it was difficult to see the hole readily. Striated Thornbills Acanthiza lineata are common in the area, and were actually seen to drink from the holes, or at least to put the tip of the beak to the hole, but whether they pierced the holes originally I do not know. I suspect they did, from the tiny size of the opening made. Previously McCulloch ( 197 5) found that under magnification the tip of the tongue of this species is seen to be very slightly grooved and frayed, and this would facilitate nectar feeding. On July 7, 1976, in the Grampians, Victoria, many hundreds of low bushes of Flame Heath Styphelia behrii were in bloom. Some carried only tight unopened buds, others both buds and flowers, others spent flowers. Even when the flower is fully out there is only a very small opening at the end of the corolla, and when looking at this it is difficult to imagine which if any bird would readily pollinate them. On watching, we saw White-plumed Honeyeaters, Eastern Spine­ bills and Fuscous Honeyeaters Lichenostomus fuscus visiting the flowers. The birds sometimes stood on the ground and reached upwards, sometimes on stems of the bush reaching down, but always appeared to be reaching in through the small open end of the corolla. They did not attempt to pierce the tough calyx. There were also Eastern and Crimson Rosella Platycercus elegans and P. eximius standing on the ground and reaching into the bushes, sometimes with head reaching right into the centre of the bushes. Unfortunately we could not see exactly what the birds were doing, but many complete flowers were found on the ground. The calyx of each was complete so it is difficult to see how the parrots could have taken any nectar as the flowers were not chewed or damaged. In several areas in the Grampians on this visit Correa flowers which had been slit or pierced were seen, more particularly if the flowers were large and orange or red. H . A. Ford & D. C. Paton ( 1976) note that the average amount of nectar recorded in flowers varied from two microlitres in Epacris to twenty microlitres in Correa. Ford & Paton also state that at its maximum nectar flow in August, Flame Heath offers nectar at a higher calorific value than in any other flower that they measured. Certainly the birds found the blossoms very attractive, even the short-beaked White-plumed and Fuscous Honeyeaters. The tongue of the bird can of course be extended well beyond the beak. It may be that some Correas and heaths compare with some of the South African plants such as Aloe and Tecomarea which attract so many birds because of their heavy nectar flow. Perhaps Crotalaria also hold a disproportionately large amount of nectar. One reads rather contradictory statements about Australian honeyeaters. For example S. & K. Breeden (1972: p. 192) state (as caption of photo) "Honev Flower or Mountain Devil Lam­ bertia formosa. Tall shrubs of this species grow on the Hawkesbury or Sydney Sandstone. The long tubular flowers are full of nectar. 121 ,_

122 McCULLOCH Bird [ Watcher

Those honeyeaters with too short to dip in from the top will puncture the flower at the base and drain it from underneath ..."; and on p. 194 "But things are not as haphazard as they appear. Not every bird and every insect can get nectar from just any flower. The flowers have developed in such a way that they attract and make their nectar available only to those visitors which are best suited to pollinate them . . ." For some plants such as this latter statement may be true, as birds with short beaks just cannot penetrate them. In some areas it may also be true, in the sense that individual birds have not learned to do otherwise, but it does not seem to be so everywhere, given the combination of long-belled flowers and short-beaked and tongued birds. It is possibly another example of the adaptability of members of the Honeyeater family Meliphagidae, which with 69 species, is often quoted as one of the most successful of Australian groups. Some Australian writers have already raised some of the points mentioned above: Sargent ( op. cit.) in 1928 noted that some flowers were destroyed by birds, and in 1945 a picture was published in Wild Life magazine showing Fuchsia blossoms pierced by White-plumed Honeyeaters. Paton D. C. & Ford H. A (1977) "Pollination by birds of native plants in South Australia" Emu 77: 73-85 found that honeyeaters rarely damage flowers, and that a frame-by-frame analysis of a movie made at feeding areas showed that the length of bill and extended tongue of the species studied was greater than the longest floral tube, a Correa sp. Thus honeyeaters did not need to destroy flowers to obtain nectar, but that the tongues of Silvereyes did not extend far beyond their short bills. It is probable that the learning situation varies between birds in different areas, whether they are in a natural habitat or in sub­ urban gardens. Flowers are pollinated by wind, insects and including many birds, but it is still not known in Australia how many of even the most common plants are pollinated. Merely recording an insect or a bird at a flower does not mean it is the chief or most important pollinator, nor do the examples recorded in the above text imply that the majority of the species of plants mentioned are ill-adapted to birds as pollinators. It does indicate that in this area we still have a lot to learn. REFERENCES Breeden, S. & K. 1972. Australia's South East. A natural History of Australia: 2. Collins. Ford, Hugh A & Paton, David C. 1976. The value of insects and nectar to honeyeaters. Emu 76: 83-84. Gilliard, E. Thomas, 1958. Living Birds of the World. Hamish Hamilton, London. Howells, W. W., 1971. Breeding of the Coppery Sunbird at Salis­ bury, Rhodesia. Ostrich 42 (2): 99-109. McCulloch, Ellen M., Tongues of Some Birds. Australian Bird Watcher 6 (1): 1-3. December J 123 1977

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Mees, G. F ., 1967. A Note of the pollination of the Kangaroo Paw. W.A. Nat. 10: 149-151. Sargent, 0. H., 1928. Reactions Between Birds and Plants. Emu 27: 185-192. Scott, Peter (Ed.) 1974. The World Atlas of Birds. Random House, New York. Skead, C. J., 1967. Sunbirds of South Africa: also Sugarbirds, White-eyes and the Spotted Creeper. S.A. Bird Book Fund. Wigglesworth, V. B., 1964. The Life of Insects. Weidenfeld and Nicolson, London. [See also (i) Ford, H.A. & N. Ford, 1976. Birds as possible polli­ nators of Acacia pycnanther. Aust. J. Bot. 24: 793-5. (ii) ParkerS. A., 1977. Birds as pollinators. Aust. Birdwatcher, 7 ( 4) : 124-1 3 3. (iii) Paton, D. C. & H. A., Ford, 1977. Pollination by birds of native plants in South Australia. Emu 77: 73-85. Hon. Editor]