SEPTEMBER, 1977 199 THE ECOLOGY OF IN (A lecture presented to the S.A.O.A. on June 25, 1976) HUGH A. FORD Accepted September, 1976 I shall present this evening a summary .of the The 22 species of honeyeaters regularly found work which has been carried out on honey­ near Adelaide can be separated into two main eaters in the Department of Zoology at .groups; the short-beaked and. the long-beaked Adelaide University over the past three years honeyeaters. In a study of the feeding habits by myself, David Paton and Neville Forde. and food of these species in the sclerophyll The initial reason for my interest in honey­ forest and woodland habitats of the Mount eaters was that I was interested in the ecological Lofty Ranges, I have shown that the short­ phenomenon of interspecific competition. Inter­ beaked species feed more on insects than , specific competition can be defined as the en­ and the long-beaked ones more on nectar than deavour of two or more species to consume a insects. The short-beaked species belong to the common resource which is in short supply, or, genera Meliphaga (or Lichenostomus) and if it is not in short supply, then nevertheless to Melithreptus. The Yellow-faced harm each other in some other way, for Meliphaga chrysops is a of the forests and example by aggression. This is an important neighbouring woodland, and takes a lot of in­ concept in ecology, and has been extensively in­ sects by hawking and also by gleaning from vestigated theoretically, in plants and laboratory leaves and bark, whereas the White-plumed populations of ; but the impor­ Honeyeater M. peniciUata is a bird of wood­ tance of competition in natural populations of land, especially along red-gum creeks, and feeds vertebrates is not understood well. The honey­ by gleaning from leaves and bark, and by hawk­ eaters are a particularly suitable group for the ing. The White-naped Honeyeater Melithreptus study of competition, as there are frequently lunatus, Brown-headed Honeyeater M. breviros­ many species in one habitat, and they often use tris and Black-chinned Honeyeater M. gularis a series of common resources, i.e. nectar from all take small insects from both leaves and bark, a range of flower species. In addition this re­ and appear to occupy different habitats; tall source is relatively easy to measure and manipu­ forest, scrubby forest and drier woodland, and late. savannah woodland respectively. All of these Although I was initially interested in compe­ five species will visit flowers, especially of tition, my approach has broadened consider­ Eucalyptus, when they are available. ably; and our studies in Adelaide have become On the other hand the long-beaked species more concerned with exploring the importance appear to rely largely on nectar and move, at of honeyeaters in the community, that is the least locally, in search of flowering bushes and whole assemblage of living organisms and non­ trees. The Yellow-winged Honeyeater Phyli­ living entities in their environment. In any com­ donyris novaehollandiae visits a very broad munity the green plants capture the sun's array of flowers in forest, heath and woodland. energy and convert it into chemical energy, The Crescent Honeyeater P. pyrrhoptera and which is in turn consumed by . Honey­ Eastern Spinebill Acanthorhynchus tenuirostris eaters consume a large amount of this energy live mostly in forest, and feed rather more selec­ in a very simple form from the plants, nectar, tively on flowers of mistletoe, heaths ( which is a solution of sugars. In return honey­ and ) and , as 'Well as Eucalyptus. eaters effect pollination in the plants they visit. However these three species are frequently They also consume many herbivorous insects, found in the same area feeding on the same which feed on plants, and predatory insects species of flower. The Tawny-crowned Honey­ which consume mostly herbivorous insects. As eater P. melanops inhabits more heathy open well as competing amongst themselves for these areas, and feeds on flowers of low bushes such foods, they compete with a range of insects as and Grevillea. The Red Wattle­ which feed on nectar and an array of insecti­ bird carunculata inhabits wood­ vorous . Honeyeaters are themselves food land more than forest and feeds principally on for predatory birds, reptiles and mammals, and Eucalyptus flowers. All of the long-beaked are parasitised by a range of micro-organisms. species take most of their insects by hawking, Thus by studying honeyeaters we can start to except for the Tawny-crowned which takes in­ fill in a few pieces of the picture of a com­ sects from low shrubs and the ground. Although munity in an Australian environment. these species spend nearly as. long feeding on 200 SOUTH AUSTRALIAN ORNITHOLOGIST, 27

insects as on nectar, we have calculated that mallee with shrubs such as uncinata, when they are hawking they spend far more in southern Eyre and Yorke Peninsulas, Kanga­ energy in capturing insects than they gain from roo Island and the Murray Mallee. The Yel­ them. On the other hand, they usually gain low-plumed Honeyeater M. ornata is a bird of more energy from nectar than they use. Nectar drier more open mallee, often dominated by E. is therefore the major source of energy. This is gracilis and E. oleosa with a semi-succulent or especially true in winter when demands are grassy understorey. The Singing Honeyeater M. high, and insects are small and so would pro­ virescens occurs in a range of open habitats: vide little energy. Insects are the major source coastal heath, saltbush-bluebush shrubsteppe of protein and other essentials. Neville Forde and Acacia woodland; but it also overlaps with has been collecting information on the kinds of the previous two species in mallee-heath and insects eaten by honeyeaters at different times mallee. However it usually feeds lower down of the year. than these two species, in shrubs or near the Thus the short-beaked species partition their ground. It also takes berries from plants such as environment chiefly on the basis of habitat, the native cherry Exocarpos, or the saltbushes while the long-beaked species overlap far more, Rhagodia and Enchylaena. The White-eared yet differ slightly in their preferences for differ­ Honeyeater M. leucotis proves to be the excep­ ent flowers. The short-beaked M eliphaga tion to the rule as it lives in a wide range of was studied in more detail to see if this pattern semi-arid habitats, and also in forest and wood­ of separation by habitat was repeated in the land on and in the South­ drier parts of South Australia. East. It differs markedly in feeding behaviour On a broader scale the Yellow-faced Honey­ from the other species, as it feeds almost en­ eater is a bird of sclerophyll forest in the South­ tirely on insects from bark, and rarely visits East, Mount Lofty Ranges and Southern Flin­ flowers. ders Ranges, and the White-plumed Honeyeater Two other species, the Yellow-fronted M. is a bird of savanna woodland, and tall trees plumula and Grey-headed Honeyeater lvI. along creeks in more arid areas. The Purple­ keartlandii, live in rocky mallee-spinifex and gaped Honeyeater M. cratitia lives almost ex­ arid woodland, but their detailed habitat -re­ clusively in mallee-heath, dense usually low quirements merit further study. The only

300 ,Ie, , \ , \ , \ I\

l(---l( PARAWIRRA I \ I / "\ + HALE :' \ , \ 0--0 MT. LOFTY , \ I X , I : I , I Figure 1. The numbers I I I , I of Yellow-faced Honey­ ~ 200 , , I I eaters seen each month Z I I , I in fifteen hours of obser­ o I I vation at Para Wirra :2 , I I I and Hale, and in six ~ I I hours of observation in 0: ,! tI the Mount Lofty area. W , I co >( , :2 II 'I :J II X' Z 100 , .. , \ , \ , \ ,, ,, I \ , \ , \ , \ : x...... x ,I , , ,I , , , ~ --x _ • J FMAM J J ,A SON D SEPTEMBER, 1977 201 species of this genus on Kangaroo Island are the Mount Lofty Ranges would in time the White-eared and Purple-gaped Honeyeaters. provide very interesting information on the The former is found only in woodland, but the movements of these and other species. In the latter occurs in all habitats including forest and autumn of 1976 the arrival of Yellow-faced woodland occupied by the Yellow-faced and and White-naped Honeyeaters was more notice­ White-plumed Honeyeaters on the mainland. able than in previous years, as, they were seen in Before leaving the short-beaked species I reasonable numbers in the suburbs of Adelaide, should like to mention two species which are the far northern Mount Lofty Ranges and even apparently migratory in South Australia. The in the Murray Mallee. The most likely reason Yellow-faced and White-naped Honeyeaters for this was that the Mount Lofty Ranges were are almost absent from the Para Wirra area very dry, with little flowering except for E. (northern Mount Lofty Ranges) from October odorata on the lower slopes. Out-of-season to March, and are scarce in the Mount Lofty flowering, and a range of exotic plants in the area. (See Figs. 1 and 2.) Their numbers in­ Adelaide area, could well have been very im­ crease very markedly in April and reach a peak portant to the survival of these and other in May near Mount Lofty, and in June at Para species of honeyeaters during this time. Wirra, and fall gradually thereafter. Numbers For the rest of the talk I shall discuss the of most species of honeyeaters appear to in­ interactions between plants, the nectar they pro­ crease in autumn, partly owing to greater activ­ duce and their pollination systems, and honey­ ity by the birds; but the Yellow-faced Honey­ eaters, especially their use of nectar as a re­ eater changes almost overnight from a scarce source. First of all I shall start by running bird to the second most abundant species of through some of the plants which are important bird at Para Wirra. I do not know where these to birds in South Australia. species go during the summer; but as they are The most important genus is Eucalyptus, at almost restricted to sclerophyll forest the most least one species of which has been seen to be likely area is the South-East and western Vic­ visited by all the species of honeyeaters, three toria. Both species are large-scale migrants species of lorikeets, silvereyes and . along the east coast of Australia. More The most important species in the Mount Lofty extensive banding of birds of all species in Ranges are E. leucoxylon, the South Australian

WHITE NAPED

300

v---v PARAWIRRA + HALE -MT. LOFTY Figure 2. The numbers of White-naped Honey­ ~ 200 eaters seen each month z in fifteen hours of obser­ o vation at Para Wirra and Hale, and in six ~ hours of·· observation in CC the Moun,t Lofty area. w en 2 :Jz 100

J FMAM JJ A S 0 N'D 202 SOUTH AUSTRALIAN ORNITHOLOGIST, 27

Blue Gum, E. cosmophylla, Cup Gum, E. against the feathers of the head and underside fasciculosa, Pink Gum, and E. odorata, Pepper­ of birds. The Scarlet Bottlebrush Callistemon is mint Gum. Several of the mallees such as E. popular, especially with the Yellow-winged incrassata are also visited frequently by birds; Honeyeater. The B. ornata and B. and many of the introduced species grown in marginata are visited by a wide range of species, Adelaide are also popular. The flowers are open including the Little Wattlebird whose distribu­ and cup-shaped with a ring of stamens, and the tion is closely linked with the Banksias. The nectar is easily accessible to birds and insects. extreme example of a brush inflorescence is Any of these visitors are likely to brush against shown by Xanthorrhoea, the Yacca, Blackboy the stamens and stigma and bring about polli­ or Grasstree, which has a flowering spike up to nation. a metre in length, with as many as 2,000 indivi­ The heaths, from the forest, dual flowers. Astroloma conostephioides from more scrubby Although it is well known that birds visit forests and heaths, and Brachyloma ericoides these flowers for nectar there has been until re­ from drier heaths, are visited by birds. Astro­ cently very little information on pollination by loma provides one of the most important birds in Australia. This subject has been sources of nectar in winter in the Para Wirra pioneered in Adelaide by David Paton, who has area. The flowers are tubular with the stamens collected and identified pollen from about 500 inside the tube, and the pollen is sticky, adher­ birds, most of them honeyeaters, The pollen can ing to the of visiting birds. The mistle­ be dusted from the and feathers with a toes spp. and Lysiana exocarpi are mascara brush. His results show that birds carry frequently visited by birds in summer, and pollen, frequently in very large amounts, from Correa is another popular tubular flower in late the flowers they visit. He has also carried out summer and autumn. The stamens of Correa experiments with stuffed birds and shown that, protrude beyond the corolla, and deposit pollen when they are probed into a series of flowers of on the forehead, face and throat of visiting one species they almost always deposit pollen on birds. Several species of Grevillea and Adenan­ the stigmata of these flowers. Another interest­ tho'S an~ frequently visited by birds, and here ing finding relating to pollen and birds was the mechanism of pollination is very precise: made by Neville Forde, who discovered that the the style is long and curved and the protostigma droppings of honeyeaters and lorikeets fre­ deposits pollen on the forehead of a bird, and quently contain large amounts of pollen. He has then becomes receptive to pollen from another not discovered yet whether the contents have flower. been digested: the outer shell is indigestible, but In the more arid parts of South Australia the it is possible that the pollen grains germinate most important flowers, in addition to Eucalyp­ inside the bird as they are mixed with the nec­ tus, are the Eremophilas, for instance Eremo­ tar. Pollen could be a supplementary source of phila oppositifolia and E. maculata, the Spotted protein for honeyeaters and other birds. Emu Bush. In wet years the latter flowers very I collected information on the availability of prolifically in a few localities, and each flower nectar throughout the year in two main areas, produces a large amount of nectar: in fact we Para Wirra and Hale National Parks, and have estimated that the smaller honeyeaters Braendler's Scrub, Monarto, which are could gain their daily energy requirements in sclerophyll forest - woodland and mallee heath about ten minutes of feeding on these flowers. habitats respectively. I also gained additional Brachyzema, a member of the pea family is also data from a few other places in the Mount visited by birds, as is the Sturt's Desert Pea Lofty Ranges and Murray Mallee. The inten­ Clianthus formosus (see Mack, S.A. Orn. 26, sity of flowering of each important plant was 90) although we have not seen birds feeding on estimated superficially on a scale of 0-5. it. An exotic, the Tobacco Bush Nicotiana Samples of about 50 flowers were collected in glauca has spread through disturbed semi-arid the early morning and late afternoon from the habitats and is also visited by birds, and may most abundant species. Some of the bushes, or be an important source of nectar in summer. branches of a tree, were covered with chicken It is perhaps one of the few introductions which wire to exclude birds, and insect-netting to ex­ could have had a positive effect on wildlife in clude birds and insects. Samples of flowers Australia, and for this reason should be were also collected morning and evening from tolerated. these covered plants. The volume of nectar in A different group of plants visited by birds each flower and the sugar concentration for are those with brush-like inflorescences. In these each sample were measured and converted into the stamens of many flowers at one time brush energetic terms (the number of calories per SEPTEMBER, 1977 203 flower). If nectar was produced or reabsorbed nate them. Probably the reason why so many through the day this would be shown by honeyeaters can coexist in one area and use the changes in the net-covered flowers. The amount same species of flower is that the intensity of of nectar taken by insects could be calculated flowering varies greatly by locality and from from differences between net-covered and wire­ year to year, and also that birds move around, covered flowers, and that taken by birds from particularly during the summer. In addition the differences between wire-covered and un­ smaller species are more efficient than the larger covered flowers. ones as they require less energy; but the larger There were always some plants in flower in species could aggressively exclude the smaller most areas throughout the year, but they were ones from the most concentrated and rich more abundant in winter and spring. The sources of nectar. Thus the system is a dynamic amounts of nectar available in the morning one, with no single species favoured for long were highest in spring in all areas, dropped enough or in a large enough area to become through the summer and rose again in winter. dominant. The numbers of all species vary In autumn 1975, after rain in March, nectar greatly through the year and from year to year, was abundant by early May; whereas in at least locally and perhaps over a wider area. autumn 1976, which was dry, nectar was scarce Details of movements and population changes until late June. Nectar probably accumulates for all of these species are scanty at present, and in the flower from day to day, unless it is taken; need to be collected over a period of many so that the reason for the low level of nectar in years. the early morning in summer could be either In conclusion, the short-beaked honeyeaters that little is being produced, or that most has are mainly insectivorous and are separated from been taken by birds or insects. On some days in their congeners by habitat. They breed mostly summer and early autumn, over 90% of the in spring and early summer when insects are nectar was taken by mid-morning. In winter perhaps at their most abundant. The long­ and spring usually only an insignificant propor­ beaked honeyeaters are mostly nectarivorous, tion of nectar was taken during the day. It was but take insects for protein and other essentials. hard to separate the effects of the insects from They overlap in habitat and in the flowers they those of the birds, because birds fed very visit, and compete for nectar when it is scarce rapidly in the first few hours of the day in in summer and autumn. They breed in late summer, while insects started feeding later and winter and early spring when nectar is most reached their greatest activity around the abundant, and in some years also in autumn. middle of the day. Insects probably took what Our studies at Adelaide University over the last the birds left, and this included the nectar from three years have allowed us to construct a flowers covered by chicken-wire from which the superficial picture of the comparative ecology of birds were excluded. Thus although the results honeyeaters in South Australia; but many more indicated that most of the nectar was taken by longer term studies are necessary to see if this insects, the real story is much more complex. picture is a realistic and accurate one. So, to summarise the relationship between honeyeaters and this important resource, nee­ List of papers .which present more substantial tar;- (1) different species of honeyeater fre­ data on our studies on honeyeaters. quently overlap in habitat and in the species of H. A. Ford and D. C. Paton. 1976. The value of Insects and nectar to honeyeaters. Emu. 76. 83-84. flower they visit, at least in the year I studied D. C. Paton and H. A. Ford. 1977. Pollination by birds of native plants in South Australia. Emu. 77. 73-85. them; (2) nectar is superabundant in winter and H. A. Ford and D. C. 'Paton. 1976. Resource partioning and spring but scarce in summer; and (3) the birds competition in honeyeaters of the genus Meliphaga. Anst. J. Eco!. 1, 281-287. are probably forced to feed on the same species H. A. Ford and N. Forde. 1976. Birds as possible pollina­ during summer, and, as a large proportion of tors of Acacia. Aust, J. Bot. 24, 793-5. H. A. Ford. The honeyeaters of Kangaroo Island, 1976. the nectar is taken, they are therefore likely to S.A. Om. 27: 134-8. In preparation: undergo strong interspecific competition for H. A. Ford and D. C. Paton. The comparative ecology of their major source of energy. ten species of honeyeaters in South Australia. H.A. Ford. Competition for resources in 'South Australian Some theoretical ecologists believe that high honeyeaters. H. A. Ford. The Black Honeyeater in South Australia. levels of overlap in the use of scarce resources H. A. Ford. The timing of moult and breeding in South such as food should prevent the coexistence of Australian honeveaters, species. One species should be more efficient Dept. of Zoology, University of New England, overall than the others and so should extermi- Armidale, N.S.W.