Stray Feathers showcases some of the remarkable adaptations of Australian birds. A brief introduction wondrous variety of forms and functions shaped by evolution. For example, did you know that Barn Owls can hunt in absolute darkness and that cuckoos commence incubation before their egg is laid? Sections include anatomy and physiology; the senses; giving voice; tongues talking; plumage; getting around; finding and handling food; optimising foraging and feeding; reducing competition; using ‘tools’; communicating; quality vs quantity; courtship; nests;
Stray Feathers
describes how evolution shapes form and function, followed by a series of vignettes illustrating the
parental care; chicks; and living together.
Stray Feathers Reflections on the Structure, Behaviour and Evolution of Birds
The book is superbly illustrated with black and white drawings of a range of birds, making it a worthy addition to the bookshelves of bird
About the authors Penny Olsen is a research scientist and experienced author and editor, with a fascination for birds. She has written 14 books, four of which have won Whitley Awards, and over 200 papers in journals. An Associate Professor at the Australian National University, she sits on various conservation and natural resource management committees and hopes to keep writing about Australia’s wonderful wildlife until she drops off the perch. Leo Joseph is the Director of the Australian National Wildlife Collection, CSIRO, Canberra. He has been involved in ornithology as an amateur and research scientist for some 35 years and has published widely in national and international scientific journals. From 1997–2005, he was the Research Curator
Penny Olsen & Leo Joseph
lovers everywhere.
in the Department of Ornithology, Academy of Natural Sciences, Philadelphia. Passionate about the evolution of Australian birds, he sees this book as an opportunity to acquaint a broad audience with some spectacular results of evolution in Australian birds.
Penny Olsen & Leo Joseph
Stray Feathers Reflections on the Structure, Behaviour and Evolution of Birds
Penny Olsen, The Australian National University & Leo Joseph, Australian National Wildlife Collection, CSIRO
© Text: Penny Olsen and Leo Joseph 2011
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Stray feathers : reflections on the structure, behaviour
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and evolution of birds / by Penny Olsen and Leo Joseph.
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Front cover: Eastern Barn Owl. (Artist: Trisha Wright) Back cover: Apostlebirds. (Artist: Trisha Wright) Set in Adobe Caslon Pro 11/18 and Helvetica Neue Edited by Janet Walker Cover and text design by Andrew Weatherill Typeset by Andrew Weatherill Printed in China by 1010 Printing International Ltd. 2
Foreword
Foreword Knowledge of the what of Australia’s birdlife abounds. Over the last 50 years, field guides, checklists, handbooks and manuals have detailed and distilled an enormous amount of information on what the species of Australian birds are, where they live and what they do. Next to nothing is understood, however, about the how of Australian birds: how they move, how they feed, and, indeed, how they have evolved their life forms. Today, these are questions that assume greater importance than ever, not only for appreciating Australia’s birdlife for its own sake, but also for understanding how to help manage the survival of its members. Why? Because the molecular revolution of the last 30 years reveals that Australia’s birdlife has had different, and often earlier, origins and evolutionary histories from the birdlife of northern continents, yet in appearance and behaviour the two avifaunas are remarkably alike. Many species of Australian raptors, ducks, pigeons, parrots and night-birds, not to mention its babblers, wrens, warblers, robins and flycatchers, may look just like northern hemisphere birds with the same names but they are either unrelated to them or but distantly connected. Adaptation to equivalent niches is, of course, the simple theoretical explanation. We now need to trace the course and steps of these evolutionary journeys, information on which will be both fascinating in itself and vital for understanding the ecological needs of our birds for survival. It bids to usher in the next phase of ornithological endeavour in Australia. This book opens a door on this new phase. It is a kaleidoscope of vignettes covering the biology of Australian birds: their anatomy and physiology, senses, voice and communication, plumage, means of movement, food and feeding, and breeding in all its diverse aspects, from courtship to fledging young. Some of the vignettes are straightforwardly descriptive, others have an evolutionary twist; and adaptive evolution and its genetic base are the threads that tie the whole together. Supporting the text are a multitude of fine figures illustrating the biological characteristics of Australian birdlife. Originally planned for an avian volume in The Fauna of Australia, an uncompleted program sponsored by the Australian Biological Resources Study, these figures, fortunately, finally see the light of day here. But not just textual content is important in getting a ‘message’ across – the right style and pitch are essential too. As well as being leading Australian ornithologists, Penny Olsen and Leo Joseph are able writers and deeply concerned with the health and growth of Australian ornithology. Their text may be packed with information, but it is also lively to read and easy to assimilate, unencumbered by jargon and needless detail. It brings science to the people. Anyone interested in birds, from the beginner to the professional ornithologist, will find much of interest and value in this work – but those who will surely be enthused and inspired the most will be the student and experienced amateur, the very people upon which the future of ornithological enterprise in Australia depends. Dr. Richard Schodde, OAM 3
Stray Feathers
Contents Foreword . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 Introduction: watching birds
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
Anatomy and physiology
17
Light, compact skeleton: Budgerigar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18 Rigid yet flexible skulls: Budgerigar, Rainbow Lorikeet and Great Knot Interlude: Form reflects function, but can mislead about evolution
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
20
Monster-mouth insect trap: White-throated Nightjar. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21 Scoop bill: Australian Pelican . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22 A diversity of beaks: bowerbirds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23 Boy bills and girl bills: riflebirds and Trumpet Manucode . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24 Interlude: Evolution of birds’ bills
25
A loaded spring: Australasian Darter . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26 Complex respiratory system: Budgerigar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27 Efficient digestive system: Budgerigar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28 Water saver: Emu . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29 Oil powered: storm-petrels
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30
The salt shedder: White-faced Storm-Petrel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31 Brain power: goose . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
The senses
35
Sense organs: Budgerigar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36 Seeing double: Tawny Frogmouth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37 By the light of the moon: Letter-winged Kite
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
Silent night hunters: barn owls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41 Interlude: Evolution of many traits for one purpose
42
Sight and sonar: Australian Swiftlet . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43 Seeing through the mud: Great Knot
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44
The smell of the sea: shearwaters and storm-petrels
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45
Interlude: The sensory world of birds – more than meets the eye
4
46
Contents
Giving voice
49
Sophisticated syrinxes: Budgerigar, ducks and geese . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50 Built-in bagpipes: Magpie Goose and Trumpet Manucode . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53 The air drummer: Emu. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54 A sound-sensing helmet? Southern Cassowary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55 The roarer: the Australian Bustard . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56
Tongues talking
59
Nectar straws: honeyeaters, silvereyes and sunbirds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60 Brush tongued: Spiny-cheeked Honeyeater . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62 Sweet tongued: Rainbow and Scaly-breasted Lorikeets
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
Fork tongued: Rufous and Black-tailed Treecreepers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 Shelling seed: parrots. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66 A quick drink: Red-capped Parrot and Rainbow Lorikeet
Plumage Flexible feathers: Budgerigar
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
69 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
Featherlight: Crimson Rosella . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71 A diversity of feathers: Budgerigar
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
Feathers are better than fur: Emu. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74 Looking after feathers: Budgerigar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75 Hung out to dry: cormorants and darters
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76
Blending into the background: Spotted Nightjar and Tawny Frogmouth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78 Don’t mess with me! Australian Painted Snipe, Eastern Barn Owl and Spotted Nightjar . . . . . . . . . . . . . . . . . . 80 Creating a diversion: Bush Stone-curlew . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82 Pluck a duck: Pink-eared Duck. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83 The secrets of cryptic chicks: shorebirds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 84 Something in the silhouette: various parrots and raptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86
Getting around
89
No-flap flight: albatrosses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90 Water wings: Little Penguin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91 Going up, going down: Brown Treecreeper and Varied Sittella . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92
5
Stray Feathers
The marathon runner: Emu . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94 Swimming on land: Short-tailed Shearwater
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
A gripping tale: Purple Swamphen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96 What’s in a foot? stilts and avocet . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97 Furtive traveller: Buff-banded Rail . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98 Migration and speciation: Australian and Oriental Pratincoles. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
Finding and handling food
103
A built-in broom: Chowchilla . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .104 Vice-like grip: Wedge-tailed Eagle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .106 Tension and spin: Grey Phalarope . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .107 Stand-over merchants: Great Skua and Arctic Skua . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .108 Unsavoury habits: Black-faced Sheathbill . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .109 Burly burley seekers: albatrosses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .110 Variations on a theme: storm-petrels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .112 Interlude: Thinking about the oceans as environments – parallels with more familiar terrestrial habitats 113 Feeling food: Straw-necked Ibis and Royal Spoonbill . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .115 Striking stalker: Black-necked Stork . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .116 Multi-purpose snake charmer: Brown Falcon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .117 The twitchers: Spangled Drongo, Satin Flycatcher, Willie Wagtail and Magpie-lark
. . . . . . . . . . . . . . . . . . . . .118
A wagging tale: Willie Wagtail . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .119
Optimising foraging and feeding
123
Putting your best foot forward: Crimson Rosella . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .124 The big-billed, picky eater: Glossy Black-Cockatoo
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .125
Choosing carefully: Peregrine Falcon and Galah. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .126 Interlude: The evolutionary equilibrium of predators and prey
127
Optimal foraging: oystercatchers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .128
Reducing competition
131
Made to measure: shorebirds
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .132
The same but different: Australasian and Hoary-headed Grebes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .134 Different ways to make a living: Pacific Gull, South Polar Skua and Crested Tern . . . . . . . . . . . . . . . . . . . . . . . .136 Size matters: honeyeaters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .138
6
Contents
Using ‘tools’
141
Playing with fire: Black Kite . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .142 Stone tools: Black-breasted Buzzard
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .143
Hammer and anvil user: Noisy Pitta. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .144 The lumberjack: Yellow-tailed Black-Cockatoo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .145 The drummer: Palm Cockatoo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .146
Communicating
149
The bearded boaster: Australian Raven . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .150 Group chorister: Australian Logrunner . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .151 A cracking duo: Eastern Whipbird . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .152 Heard but not seen: Rufous and Noisy Scrub-birds
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .154
The song and dance man: Superb Lyrebird . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .156 Polygynous posers: Magnificent Riflebird, Trumpet Manucode and Victoria’s Riflebird . . . . . . . . . . . . . . . . . .158 Signaling maturity: Black-faced Sheathbill
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .160
Staking a claim: Black-faced Sheathbill . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .161
Quality vs quantity
163
Boom and bust shorebird style: Banded Stilt . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .164 Familiarity pays: Short-tailed Shearwater . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .166
Courtship
169
Boom box territoriality: Emu . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .170 Male–female dynamics: Great Crested Grebe
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .171
The scented powderpuff: Musk Duck . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .173 A long engagement: Wandering Albatross . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .174 Breeding seasons’ greetings: Australasian Gannet . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .175 You are my Valentine: Christmas Island Frigatebird . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .176 Do you think I’m sexy? Pied Cormorant . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .177 Mutual attraction: Red-tailed Tropicbirds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .178 The flap dancer: Black-necked Stork . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .179 The ballet dancer: Brolga . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .180 Brazenly barefaced: Royal Spoonbill
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .181
Bow coo: pigeon courtship . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .182
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Stray Feathers
True blue Lotharios: Variegated Fairy-wren
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .184
Playing hard to get: White-throated Treecreeper . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .185 The importance of ritual: Red-browed Finch. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .186 Life in the monogamy fast track: Black-throated Finch . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .187 Architects are smarter: bowerbirds
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .188
Why go to so much trouble? Great, Spotted and Fawn-breasted Bowerbirds. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .192 Look at me: Crimson Chat . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .194
Nests
197
Designed by the same architect: robins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .198 Topped and tailed: Yellow-bellied Sunbird . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .200 What nest? Spotted Quail-Thrush. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .201 The fancy stitcher: Golden-headed Cisticola . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .202 An insect’s nest: Buff-breasted Paradise-Kingfisher
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .203
The bottle-builder: Fairy Martin. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .204 Bees and burrows: Rainbow Bee-eater
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .205
Interlude: A cooperative migrant
207
Parental care
209
Hot-footed: Brown Booby . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .210 Saliva nests and egg-incubating chicks: Australian Swiftlet . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .211 A bun in the oven: Malleefowl, Australian Brush-turkey and Orange-footed Scrubfowl
. . . . . . . . . . . . . . . . .213
Is it a boy or girl? Australian Brush-turkey . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .215 A head start in the arms race: Horsfield’s Bronze-Cuckoo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .216 Helpless hatchlings: Major Mitchell’s Cockatoo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .217 Coping with extremes: Australian Pratincole and Masked Lapwing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .218 A crown of thorns or a larder? Crested Bellbirds. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .220 Taking them under his wing: Comb-crested Jacana
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .221
A parent’s love: Brolga . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .222 Cream of the crop: Emerald Dove . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .223 Toilet trained: the Golden-headed Cisticola . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .224 A face only a father could love: Pheasant Coucal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .225
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Contents
Chicks: behaving badly; behaving well Balanced begging: Singing Bushlark
227
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .228
Bright little beggars: Painted Finch. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .229 Cooperative killers: Australian Pelican . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .230 Killer babies and insurance eggs: Brown Booby . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .232 Cheaters versus cheated and odd couples: Eastern Koel, Australasian Figbird and Little Friarbird . . . . . . .233 Sticking together: Fairy Tern . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .235
Living together: same species
237
Sociality for survival: Apostlebird, White-winged Chough and Varied Sittella . . . . . . . . . . . . . . . . . . . . . . . . . . . .238 Lending a hand: Grey-crowned Babbler . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .241 Red-eyed kidnapper: White-winged Chough . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .243 Waiting in the wings: Laughing Kookaburra Ritualised aggression: Dusky Moorhen
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .244
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .245
Cold comfort: Black-faced Woodswallow . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .247 You scratch my back and I’ll scratch yours: Silvereye
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .249
Troop fishing: Australian Pelican . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .250 Cooperative spear-fisherman: Black-necked Stork ( Jabiru) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .251
Living together: different species
253
A one-sided affair? Azure Kingfisher and Platypus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .254 Lured into the shadows: Cattle Egret . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .255 Farming mistletoe? Mistletoebird . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .256 Pest control: Spotted Pardalote . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .258 Looking after trees? Bell Miner
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .259
Wrapping up . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .261 Further reading. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .263
9
Stray Feathers
Preface In the late 1980s the Australian Biological Resources Study (ABRS) planned a volume on birds in the Fauna of Australia series, which aimed to synthesise and publish all current zoological information for the region. By the early 1990s much of Volume 2B Aves was drafted, but events such as the publication of the Handbook of Australian, New Zealand and Antarctic Birds overtook the exercise and it was abandoned. Many of the illustrations gathered for that volume are richly informative of the biology of Australian birds as well as being attractive in their own right. They provide an opportunity to discuss some of the adaptations that make birds so interesting and some that make Australia’s birds unique. Opportunism has its limitations, as many Australian birds know. In writing the text, we used each illustration to trigger a riff, rather than the more usual reverse. Hence the subject matter is heterogeneous and the collection and treatment far from comprehensive. The uniting theme is evolutionary biology, which shapes birds’ lives as it does all life. Some illustrations inspired a mini-essay, others a few lines of observation. The musings often tackled more than one subject but, for the sake of order, they have been placed under the section heading to which they most relate. Inevitably, because we wanted each essay to stand alone, there is some repetition. There are many different ways of looking at birds. Stray Feathers is intended as a ‘taster’ for bird lovers or students who wish to gain some insight beyond a simple enjoyment of birds for their beauty, liveliness or rarity. Our hope is that the book brings greater interest, study and understanding. Much-needed research into birds in landscapes has become the norm, but arguably the pendulum has swung too far from the individual. There is still plenty to be learned about the great, continuing and changing forces of evolution, which have implications for us all, especially in these rapidly changing times. There is still plenty that we need to know about Australia’s birds if we are to conserve them. And, of course, we will continue to refine and consolidate our ideas about evolution, assisted by the knowledge gleaned from watching birds. NOTE: Nomenclature follows Systematics and Taxonomy of Australian Birds by L. Christidis and W. Boles (CSIRO Publishing, 2008).
10
Acknowledgements
Acknowledgements We are grateful to the artists for permission to use their inspirational drawings: Wendy Arthur; William Cooper; Nicholas Day; Ian Faulkner; Jon Fjeldsä; Peter Marsack; and, especially, Trisha Wright, who could not be located to seek her blessing for the use of her work. Thanks also to the authors of the original, abandoned ABRS volume who suggested and vetted the illustrations close to 20 years ago: Baker-Gabb, D.; Bamford, M.J.; Bock, W.; Boles, W.; Briggs, S.; Brown, E.D.; Brown, R.G.B.; Bruce, M.; Burger. A.E.; Calaby, J.; Christidis, L.; Collins, B.G.; Crome, F.; Donaghey, R.; Ferrier, S.; Fitzherbert, K.; Fjeldsa, J.; Ford, H.; Forshaw, J.M.; Frith, C.; Fullagar, P.; Gales, R.; Garnett, S.; Hockey, P.; Homberger, D.; Howell, T.; Jones, D.; Joseph, L.; Kentish, B.; Kikkawa, J.; Lanyon, S.M.; Lewis, M.; Lill, A.; Long, J.; Lowe, K.W.; Maddock, M.; Marchant, S.; McEvey, A.; McLean, G.; Menkhorst, P.; Murray, D.; Norman, I; Noske, R.; Olsen, P.; Paton, D.; Pettigrew, J.; Reid, N.; Rich, P.; Rowley, I; Schodde, R.; Tarburton, M.K.; Tomkins, R.; van Tets, G.; Warham, J.; Weinecke, B.; Whitehead, M.; Williams, K.; Woinarski, J.; Woodall, P.; and Wooller, R.; and to its editors, Chris Glasby and Graham Ross. Special thanks to Alice Wells, ABRS, and John Manger and the team at CSIRO Publishing – Tracey Millen and Pilar Aguilera – and editor Janet Walker for their enthusiasm for the project and, not least, to Naomi Langmore, Janet Gardner, Peter Marsack, Jim Reynolds and Alice Wells, who commented helpfully on all or part of the manuscript.
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Stray Feathers
Introduction: watching birds What do we really see when we look at a bird or, for that matter, at a flock of birds? What do we think about when we observe a bird? What I am getting at here is something that we hope this book will encourage all those who watch birds, not just academics, to think about when they observe birds. It is perhaps most simply summed up in the following question: which interesting corners of evolutionary biology might be illuminated by the birds we are watching? That is what has motivated us to write this book. We wanted to explore the notion that when we see a bird in the field, we are really looking at the results and actions of evolution. A bird’s appearance and behaviour, the sounds it makes as vocalisations or perhaps with a whirr of its wings, where it nests, how it builds its nest, and what its eggs look like, all reflect the current point at which a bird finds itself on an evolutionary lineage. That lineage is a path that its ancestors have travelled as the species has evolved. Evolutionary thinking can start even before you leave your front door on a birdwatching trip. Consider this example. Not so long ago, I found myself on a one-day birdwatching tour led by Phil Maher in Deniliquin, New South Wales. We hoped to see one of Australia’s most peculiar birds, the Plains-wanderer. Perhaps without realising, the thing that drives most birdwatchers to want to see this odd bird is its evolutionary uniqueness. Certainly, that is what drove me and my two colleagues and friends, Dave Winkler from Cornell University and Krystof Zyskowski from Yale University, who had travelled from the USA to see the bird. Our current understanding is that the Plains-wanderer is the sole representative of an evolutionary lineage of shorebirds, or waders, which evolved a quail-like form through its adaptation to life in arid and semi-arid Australia and which is most closely related to the South American seedsnipes. The night-time is the right time to see Plains-wanderers, so in the afternoon we were treated to some of the other birdwatching delights of the area. On a plain covered in saltbush, we spotted a spectacular male Whitewinged Fairy-wren. As the party hastened to see that single, stunning adult, I pondered what he and his species could tell us about evolution. The first question we might consider is: where does the White-winged Fairy-wren fit in the world of birds; that is, within the avian family tree? First of all, it is a passerine and among passerines there are two major groups, the oscines and the sub-oscines. This fairy-wren is an oscine. Oscines fall into two main groups, the Passerida and all the rest, which, remarkably enough, do not have a simple scientific name. The phylogenetic tree (see page 14) is an attempt to illustrate this odd situation. Phylogenetic trees show relationships that reflect evolutionary history. As this tree shows, the species we are concerned with belongs to that other group of oscines with no formal name. Within that group, however, it is part of a subgroup known as the superfamily Meliphagoidea. Within the Meliphagoidea, the White-winged Fairy-wren belongs in the family Maluridae along with other fairy-wrens, grasswrens and emu-wrens. Within the genus Malurus, it is most closely related to the Western Australian island populations that are black and 12
Introduction
white, and then to the Red-backed Fairy-wren, then to the Superb, Splendid and Purple-crowned Fairy-wrens, then to the chestnut-shouldered group of species. That is a very dry, taxonomic way of looking at things. But what we have learned about the evolution of passerine birds in recent years is that the Australia-New Guinea-New Zealand region has been, to use a hackneyed but useful term, a cradle of evolution. Most particularly, the Passerida, which are the dominant passerines of the northern hemisphere, appear to have evolved from a southern hemisphere lineage that ‘escaped’ out of the region. So, our humble Deniliquin fairy-wren on top of his saltbush clump could be considered to represent the ancestral group that gave rise to the spectacular radiations of northern hemisphere passerines. Still thinking about the fairy-wren’s deeper evolutionary history, let’s go forward in time to consider how it relates both to the Western Australian offshore island populations of the species that are black-and-white and to its mainland populations that are blue-and-white. It has been learned that the granules that contain melanin (a black pigment) in the feathers of the black-and-white populations are still present but empty in the blueand-white populations. A 2004 study showed that a gene that controls the deposition of melanin (the gene’s abbreviated name is MC1R) has five fixed differences in its DNA base sequence between the blue-and-white and black-and-white forms. A later study, published in 2010, produced more nuanced conclusions. It looked at MC1R variation in Malurus fairy-wrens more generally, not just the White-winged Fairy-wren. Viewed in that broader context it became clear that the blue-and-white mainland birds are the ones that are genetically unique. So, the MC1R gene is not directly or solely responsible for the black-and white plumage of the island birds. Finally, the black-and-white populations appear to have evolved from blue-and white ancestors because vestiges of the nanostructure required for the production of blue colouration exist within their black feathers. Pulling together all the data on genetics and feather structure, the authors concluded that there have been two independent evolutionary transitions from blue to black plumage. Next, we can consider what has been learned of the reproductive biology of the various populations and what role natural selection might have played in the evolution of the island birds. The mainland birds are typical of the fairy-wrens in being cooperative breeders, in which birds other than the socially dominant pair – usually their offspring from earlier breeding attempts – help to raise the young. The island birds accord with predictions that have been made concerning the evolution of cooperative breeding on island versus mainland areas. That is, cooperative breeding should be less common in island birds, which are expected to evolve pair breeding. This is exactly what is seen in the black-and-white island populations. Next, we have learned from mitochondrial DNA (mtDNA) that the Western Australian island populations of the blue-and-white birds are more closely related to one of the island black-and-white birds than they are to eastern Australian blue-and-white birds. At face value, this also means that the two black-and-white populations are not each other’s closest relatives. This is an example of what is increasingly seen when we probe 13
Stray Feathers
Other Old Australo-Papuan Oscines: lyrebirds, bowerbirds, treecreepers, logrunners
Core Corvoidea: birds-of-paradise, crow-like birds, cuckoo-shrikes, fantails, butcherbirds and relatives and others
Meliphagoidea includes fairy-wrens
Other Oscine Passerines
Australo-Papuan Robins
Oscine Passerines
To the Suboscines Simplified evolutionary tree showing the relationship of fairy-wrens to other passerines.
the DNA of populations and species: a discordance between the geographical patterns that are seen between birds’ plumages and general form on one hand and the history of their populations as indicated by mtDNA on the other. That, in turn, opens up the question of why both have evolved black-and-white plumage. Is there something about the environment on the islands that has favoured development of black? Of course, all of this evolution has been played out on the landscapes of continental Australia as it too has experienced its own geological and environmental evolution. So we might wonder whether the gorgeous male fairy-wren that we were admiring north of Deniliquin is at the eastern end of a historical journey of dispersal by the species across the continent from west to east? Or did its ancestors arrive in its present position in eastern Australia through a more complicated scenario of long-term movements across the landscape? These sorts of questions can be addressed from an understanding of the deeper evolutionary history or phylogeny of the fairy-wrens themselves. So much for the deeper history. Thinking about the here and now, we now realise that the male bird sitting on a clump of saltbush for us to admire has to deal with the rigours of simply being alive. In evolutionary terms, this amounts to dealing with the pressures of natural selection to which he is exposed. Parasites may live among his feathers, feeding on them and affecting the condition of his plumage and thus his ability to attract a mate and maintain his social status. Internal parasites may be threatening his daily health and nutrition. Predators may find him easy to pick off as he sits, brightly coloured and exposed. 14
Introduction
What of the females? They are less conspicuous to predators, but snakes may prey on them as they sit on their nests. Brood-parasitic cuckoos may remove fairy-wren eggs so that they can lay their own eggs to be hatched and reared by the fairy-wrens. How can birds like fairy-wrens evolve defences against these pressures, which we so often tend to term as ‘natural threats’ but which in this book we want to stress are ‘selection pressures’? It was late afternoon when I saw the White-winged Fairy-wren atop a chenopod bush, so perhaps it needed to secure some food before nightfall in order to maintain its high metabolic rate through the night. A warm summer night may not be much of a problem, but most nights of the year where this species lives present something of a metabolic challenge for a small warm-blooded insectivore. That is where the thermoregulatory properties of feathers in preventing heat loss come in, of course. The whole issue of food and its procurement is a major area of avian evolutionary biology. How is a bird’s form, particularly its bill, adapted to its foraging techniques and to the food it seeks? What of its legs and feet if it is a ground forager? What of its wings and olfactory system if it is a seabird? What of its eyes and its spectrum of visual acuity if it is an aerial hunter, either an insectivore or perhaps a raptor? What if it does not use its eyes much but mainly relies on touch and smell, as a shorebird or seabird might? If the bird lives in the tropics or indeed in particularly wet temperate areas, prolonged rainfall can be seen as a selection pressure. Many birds cannot forage for food during prolonged, heavy rain and the weaker individuals or those not so capable of sitting out the rain can be quickly eliminated by natural selection. A bird must attract a mate and in many species evolution has led to male birds being colourful, whereas in others they are able to use sounds made by their wings (e.g. birds-of-paradise, manakins) to attract females. Similarly, females impose selection pressures on males simply through their choice of males with which to mate. The selection they can impose can continue in their reproductive tract where they can store sperm from different males. The means by which sperm from a male finally reaches and fertilises an egg is another level of evolution altogether, but the very shape of a female reproductive tract can influence this process. What we hope to achieve in this book is not a recipe for how one can go out and answer the sorts of evolutionary questions posed or hinted at above. Instead, we simply hope to reinforce the point that almost everything a bird does, almost everything about how it exists in its environment and how it looks, sees, moves, hears, sounds, smells, feeds and reproduces, and how it manages internal and external parasites, are facets of its evolutionary biology. Looking at birds with this kind of evolutionary perspective has certainly enriched how we view birds and given us added appreciation of what makes birds among the more spectacular creatures with which we share the planet. Leo Joseph
15
Stray Feathers
16
Anatomy and physiology
17
Stray Feathers
Light, compact skeleton: Budgerigar The avian skeleton is a compact framework that provides points for muscle attachment, protection and support for the viscera, and stores minerals for activities such as egg production. Despite its strength, structural adaptations mean that the skeleton is remarkably light – constituting only about 5% of the total mass of the bird. Like most features of birds, the skeleton is honed for flight. The major bones are light yet strong, filled with air spaces and struts for structural support. Flightless birds have fewer pneumaticised bones than flighted birds, which have many air-filled cavities in their bones. In the Budgerigar, for example, the ribs and vertebrae, as well as several larger bones such as the humerus, pelvic bones and sternum, are pneumaticised. A unique type of bone in birds is the medullary bone, which is laid down in the medullary cavity of the long bones to provide calcium for eggshell formation and then after
Budgerigar skeleton. (Artist: Trisha Wright)
breeding is rapidly reabsorbed to minimise weight.
The skeleton, along with the muscles, is part of the biomechanics of the bird. Although a bird’s skeleton is articulated, many bones are fused together to provide stability, especially in species such as diving birds that must withstand high impacts. The pelvis is highly fused and provides a stable, lightweight attachment for the legs, tail and abdominal muscles; the powerful flight muscles attach to the sternum or keel. Several vertebrae are fused and each rib is braced by a bony overlap with the next rib to reinforce the entire rib cage. In contrast, several joints are highly flexible, particularly wing joints, which are the highly modified hand and wrist bone equivalents in the wing. The sclerotic rings, or eye bones, are unique to birds and reptiles; these rings of small overlapping plates help to retain the shape of the large eyeballs. Birds have between 11 and 15 such eye bones; the Budgerigar, as illustrated, has 12. Finally, birds are toothless and this further minimises weight. To compensate, however, some birds that eat hard food items also ingest grit that acts as sandpaper inside the gizzard.
18
Anatomy and physiology
Rigid yet flexible skulls: Budgerigar, Rainbow Lorikeet and Great Knot All birds have the same basic skull structure, modified to suit their way of life, particularly their diet and manner of gathering and processing food. As in the remainder of the skeleton, many of the bones of the bird skull are fused and, in several species, heavily pneumaticised, to produce lightness with rigidity. Despite this high level of fusion and apparent rigidity, parts of a bird’s skull are highly flexible, especially so in the parrots, which are capable of precise, refined manipulations of their food. The posterior end of the upper jaw is hinged to the brain case and the jaw has bending zones so the bird can widen its gape as well as close its bill quickly (see below). Forward movement of the pterygoid, zygomatic arch and palatine swings the upper jaw upward to open the beak (see arrows below). The movement is known as cranial kinesis and its extent varies between species. In the Rainbow Lorikeet (see page 20), the bones are less robust than in the Budgerigar, because it does not need to process hard seeds, but they are potentially more kinetic, to facilitate gathering of nectar and pollen. The lower jaw (palatine) is made up of six or seven bones which allow several bending zones if the species is one that must swallow large prey (see page 21). In birds like the Budgerigar these lower jawbones are so fused as to appear as one. Nonetheless, the Budgerigar’s lower jaw is somewhat loosely articulated to the quadrate, which allows considerable freedom of movement when the bird is shelling seeds. Some birds, such as sandpipers, snipe and the Great Knot (see page 20), also have additional bending points towards the tip of the mandibles, so that they can open just the end of the bill while probing in the ground. The linkages between bones, which allow bending, have another important function: they act as shock absorbers between the bill and skull, protecting the fragile brain.
➀
➂
➁
➃
➄
➅
➆
➇
➀ Orbit ➁ Hinge ➂ Nostril ➃ Premaxilla (upper mandible) ➄ Horny tips of the beak ➅ Palatine (lower mandible) ➆ Zygomatic arch ➇ Pterygoid ➈ Quadrate
➈
Budgerigar. (Artist: Trisha Wright) 19
Stray Feathers
Interlude: Form reflects function, but can mislead about evolution Birds are perhaps a more uniform group than other vertebrates. Their structural and functional similarities have evolved principally because of the strong selective demands associated with flight. Nevertheless, basic features of many birds have been modified in response to a variety of environmental demands. Almost all of these adaptations are related to locomotion, feeding and reproduction. Hence, form has usually evolved in response to selection relating to some function. But form can be misleading if it is taken as evidence of evolutionary relationships. Traditionally, morphological attributes were used as primary sources of information in attempts to chart the evolutionary history of birds. These efforts were often misled by the fact that form so often reflects function. A spectacular example of this is that we didn’t understand until the 1980s that many Australo-Papuan passerines are not closely related to their northern hemisphere namesakes even though they can look remarkably similar. The modern revolution in using DNA to chart the evolutionary history of birds, however, has revitalised the understanding of form in evolution.
Rainbow Lorikeet. (Artist: Trisha Wright)
Great Knot. (Artist: Trisha Wright) 20
Anatomy and physiology
Monster-mouth insect trap: White-throated Nightjar Nightjars hawk aerial insects by night, making short sallies from a perch or the ground to snap up prey. They catch prey ranging from moths to winged ants, often taking immense numbers, which they pack into their capacious gullet. The nightjar’s small neat bill belies its massive gape. When a nightjar opens its mouth to envelop insects, the lower jaw balloons from a V-shape to a semicircle, greatly increasing the catch area. Stiff tactile bristles (modified feathers) fringe the bill, funneling insects to the mouth and screening the eyes. Although the mandibles (jaws) of all birds appear to be rigid they are quite flexible – a characteristic known as cranial kinesis (also see previous section). Several joints and bending areas in the upper jaw allow a bird to widen its gape and close its jaws fast and also act as a shock absorber between beak and skull. The mandible (lower jaw) is made up of six bones. In nightjars and other specialist feeders, and birds such as owls and some fish-eaters that swallow large prey, the bending zones allow great expansion of the gape. Amazingly, the width of the lower gape in nightjars can expand more than threefold between the resting and active postures. Unlike most birds, nightjars do not have a bony palate. It has been suggested that their softer palate is sensitive to collisions with tiny insects, increasing catch rate and triggering the rapid snap-shut mechanism. Among nightjars’ closer relatives are the frogmouths. The Tawny Frogmouth sometimes sits during the day with its mouth open, snapping it shut when an insect enters. It has been suggested that its palate produces an insect-attracting scent – a fascinating proposal for further study.
The lower mandible of the White-throated Nightjar at rest (left) and active (right). (Artist: Trisha Wright) 21
Stray Feathers
Scoop bill: Australian Pelican A wonderful bird is the pelican, His beak can hold more than his belly can. He can hold in his beak, Enough food for a week … Contrary to Edward Lear’s famous limerick, the pelican’s pouch is not for storing fish. Rather it is used to net fish, which are swallowed almost immediately. The pelican’s long, narrow upper ‘jaw’ is matched by a lower ‘jaw’ composed of the two long, flexible bones that support the throat pouch. On spotting a fish the bird thrusts its bill quickly into the water and the pouch expands like a balloon, bowing the supporting bones outward to create a wide scoop. The upper jaw acts as a lid. As the bill snaps shut the lower bones return to resting position, Australian Pelican. (Artist: Trisha Wright)
the pelican lowers it head, water
drains slowly from the bill and prey is left trapped inside. The bird lifts its bill up and back to swallow. The pelican’s upper bill is also tipped with a sharp nail used for gripping larger fish, which are tossed in the air, caught and swallowed head first. The bill is highly sensitive and can detect fish in murky water by touch. Although the pelican has a small tongue, its tongue muscles control the pouch, helping to expel litres of water after a catch (almost 14 litres or over eight kilos of water recorded). The bird even exercises to keep the pouch skin supple, throwing its head back with its bill open and then tucking its head down and everting its pouch. Although it is highly adapted for scooping fish, the pelican also puts its impressive pouch to good use for other purposes. It spreads its lower bill to catch rainwater. During the courtship period, when the pouch reddens in colour, the bird lifts its head to show off the bag, or inflates it with air. Lastly, the pouch is well supplied with blood vessels and the bird dissipates heat and lowers its body temperature on hot days by gular fluttering – functionally similar to the respiratory panting of mammals. The gular pouch of the pelican is thus an example of an organ that has evolved in response to a range of different selection pressures relating to food and reproduction. 22
Anatomy and physiology
A diversity of beaks: bowerbirds The bowerbirds are typically fruit-eaters, with strong, stout bills. Nonetheless, their bills show a diversity of sizes and shapes, reflecting the birds’ dietary habits. Most species have generalised bills, mainly used for plucking fruit (supplemented with invertebrates, especially during the breeding season, and flowers and other plant matter). The most divergent bills within the group are the longer, more slender, bills of the Regent Bowerbird (and some other Sericulus species), somewhat modified for their partly nectarivorous diet, and the unique bill of the Tooth-billed Bowerbird, which is strongly ‘toothed’ like that of a falcon, but used for cutting and manipulating large leaves to eat (folivory) and is also displayed to attract females during courtship.
Satin Bowerbird, Green Catbird and Golden Bowerbird (top to bottom). (Artist: William Cooper)
Spotted Bowerbird, Tooth-billed Bowerbird, Regent Bowerbird (top to bottom). (Artist: William Cooper) 23
Stray Feathers
Boy bills and girl bills: riflebirds and Trumpet Manucode Within the family Paradisaeidae, the bills vary enormously, from stout and crow-like to fine and starling-like in omnivorous species such as the Trumpet Manucode, to the elongate, sickle-bills of several species, adapted for Trumpet Manucode. (Artist: William Cooper)
probing flowers. Uniquely among the family, the riflebirds
use their strong, chisel-like bills to chip and probe at wood and foliage and to extract, even spear, invertebrates, and with assistance from their strong feet, to hold and manipulate complex, difficult to handle, fruits. The manucodes, on the other hand, are weaker-footed and weaker-billed and have significantly wider gapes; they glean insects and eat simple fruits that merely require plucking and swallowing, but they are capable of holding larger soft fruits such as figs in their feet while they tear off manageable pieces. These differences equip each species to feed most efficiently in a particular niche and thereby help to reduce competition between species. In the riflebirds this division of resources extends to the sexes, which have differently sized and shaped bills that adapt them to somewhat different feeding niches. Female riflebirds have a significantly longer and more down-curved bill than males, despite being slightly smaller in body size. The differences suggest that males and females take significantly different foods (different-sized insects or fruits, and/or from different foraging sites), which would be particularly advantageous during harder times.
Victoria’s Riflebird male (top) and female (below). (Artist: William Cooper)
Magnificent Riflebird male (top) and female (below). (Artist: William Cooper) 24
Anatomy and physiology
Interlude: Evolution of birds’ bills In the previous accounts we have seen the remarkable diversity that has evolved in the bills of birds for capturing and manipulating different plant and animal foods. We have also seen how an organ such as the bill can be under selection pressures relating to different facets of avian biology such as feeding and reproduction. The quest to understand the evolution of bill morphology has a grand tradition in evolutionary biology. It was, of course, a central topic in Charles Darwin’s unlocking of the secrets of the theory of evolution by natural selection. Darwin famously was puzzled by the birds of the Galapagos, including the group known as Darwin’s finches. They are now thought not to be true finches. Instead, they are part of an impressive evolutionary radiation in the Americas of tanager-like birds. Many of these tanagers have evolved very finch-like bills and are known as tanager-finches. Darwin gave us the mechanism, the theory of evolution by natural selection, with which to understand how unrelated species such as tanager-finches and the true finches can come to resemble each other. What, then, do we know of the genetic machinery that underlies this evolution? For example, is evolution acting on one set of genes involved in generating all of the diversity we see in the bills of all birds? At present, we only have glimmers of understanding about the answers to these questions. One such glimmer has emerged from studies of the molecular basis of the diversity of bill morphology in Darwin’s Finches. The research has shown that two molecules, bone morphogenetic protein 4 (BMP4) and calmodulin, are expressed differentially during the embryonic development of finches, regulating the depth, width and length of the bill. Are the same genetic and biochemical mechanisms involved in the impressive evolutionary diversity of bill morphology in the Australian black-cockatoos? The advent in recent years of techniques to look at whole genomes promises still more insights into how many different genes and sets of genes are involved in the evolution of the great diversity of bird bills.
25
Stray Feathers
A loaded spring: Australasian Darter Paddling with its feet, the darter hunts through the water, moving slowly until it suddenly thrusts itself at a flighty, fishy target. Underlying its slender, S-shaped neck is a specially adapted vertebral column that enables the bird to strike at lightning speed. A hinge between the eighth and ninth cervical vertebrae allows the darter to draw its neck into an extra tight kink with even more potential energy, which is released when the bird shoots its head forward to spear a fish. The darter has other adaptations for its manner of fishing. The trachea (windpipe) and oesophagus (the first section of the digestive tract) cross over and run straight down, which places them behind the bones and protects them in that part of the neck most prone to sharp bumps when the bird is hunting. The sharp, swordlike bill, edged with fine inward directed barbs, is custom-made to spear and anchor slippery fish.
Australasian Darter. (Artist: Trisha Wright) 26
Anatomy and physiology
Complex respiratory system: Budgerigar The respiratory system of birds is unique in that it comprises a complex system of air sacs, lungs and interconnecting tubes. The system is honed for efficient, often high energy, flight. It is the most elaborate respiratory arrangement of any vertebrate group and maintains a continuous stream of air, unlike that of mammals, which have rhythmic inhalations and exhalations. The illustration shows the lateral view of lungs and respiratory passageways of the Budgerigar in relation to its skeleton. Air is inhaled and exhaled through the nostrils (or mouth), as in most vertebrates. In birds, however, the trachea generally links the throat directly to the lungs. The trachea evenly divides into two and then unevenly two more times, ending in parabronchi from which air capillaries arise. Oxygen and carbon dioxide are exchanged across these capillaries. Air is drawn into and out of the lung by muscles that expand and contract various air sacs, including those in the larger bones: the cranial, caudal, abdominal and clavicular air sacs.
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3a
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3b
Lung (enlarged)
➀ Trachea ➁ Syrinx ➂ Bronchi (a. primary and b. secondary) ➃ Cranial thoracic sac ➄ Caudal thoracic sac ➅ Abdominal sac ➆ Clavicular sac
➅ ➃
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Respiratory system of the Budgerigar. (Artist: Trisha Wright) 27
Stray Feathers
Efficient digestive system: Budgerigar The digestive tract of birds, like that of any animal group, has evolved to absorb water and nutrients from food, and void waste. Along its length a number of glands assist in this process. Its accessory organs ➀
include the beak, which grows constantly
and must be kept in trim by use. Food is swallowed ➈
and passes into the crop where it can be stored temporarily (not all birds need a crop, but it is present
➇
in raptors, parrots and pigeons, for example). From the
➁
crop it passes slowly to the ‘stomach’, which consists of the proventriculus, where enzymes start to break down the food,
➆
and the gizzard, where food is macerated. The food then moves to the relatively short intestines where caecae maximise the surface
➂
area for digestion, especially in birds that eat plant material. (The intestines are shortest in nectar-feeders.) The digestive tract
➅ ➃
then empties through the cloaca, a joint opening for the
➄
alimentary and reproductive systems. The function of Digestive system of the Budgerigar. (Artist: Trisha Wright)
the cloacal bursa of Fabricius, puzzled anatomists for many years but is now known to be part of the bird’s
➀ Oesophagus ➁ Crop ➂ Pancreas ➃ Supraduodenal loop ➄ Duodenal loop
immune system, producing antibodies. It is most prominent in the first year or less of a bird’s life. The digestive tract of the budgerigar sits neatly
➅ Cloaca ➆ Cloacal bursa ➇ Gizzard ➈ Proventriculus
within its compact skeleton. As in all birds, the tract is relatively simple but has evolved to high efficiency, processing heavy food quickly to minimise weight during flight and provide the high energy levels needed. Average times for the passage of food in birds are 15–60 minutes in fruit-eaters, to 30–50 minutes in nectar-eaters and 40–100 minutes in grain-eaters. Water is problematic for flight because it is particularly heavy and birds have evolved mechanisms to remove it from food about 10 times faster than mammals on similar diets. On the theme of water needs, Budgerigars and a few other arid-adapted species, such as the Zebra Finches, are remarkable in that they can process dry seeds for months without ever drinking, thereby liberating them from the need to find free-standing water regularly, provided ambient temperatures are not too high.
28
Anatomy and physiology
Water saver: Emu All birds excrete nitrogenous waste as uric acid. This system required less water than that of mammals, which rid their waste as watery urea. An adaptation for flight, because water is heavy, this also means that birds need less water. In addition, the Emu has several adaptations to life in hot, dry environments, including large, multi-folded nasal passages that condense water from exhaled air and absorb it, helping to retain moisture on all except the hottest days. Another somewhat similar adaptation to aridity is a colon that extracts water from urinary and digestive waste. In the Emu, the mucosa of the colon-coprodaeum is particularly elaborate and organised into many densely spaced, deep folds with numerous villi. The villi extract water from ingested food, resulting in higher retention of water by reabsorption than loss by excretion. Rather than the adaptive changes to the structure of the kidneys seen in desert mammals, this structure is the Emu’s evolutionary response to the selection pressures to maximise the conservation of water. The evolutionary lesson here is that one selection pressure – the need to retain water – has led to different evolutionary responses in desert mammals than in birds. This highlights how the randomness of mutations can give evolution different options to solve one problem.
Cross-section of the Emu’s intestine showing numerous villi. (Artist: Martin Thompson)
29
Stray Feathers
Oil powered: storm-petrels Like most other members of the Order Procellariiformes (albatrosses, shearwaters, petrels and storm-petrels), storm-petrels have evolved mechanisms to store oil in their very large, distendable proventriculus (the horizontal sac to the right in the illustrations). The high-energy oil is extracted from food by the proventriculus and retained as a reserve of energy for the individual and to feed chicks. Oils are found in breeders and nonbreeders, adults and chicks and in birds captured at sea and at breeding colonies. Evolution has presumably led to more efficient biochemical means of extracting the oil than in other fish-eating animals. Long foraging distances mean that this ability to concentrate food into a high-energy oil that occupies a relatively small volume, and has a low osmotic load (by eliminating large volumes of water), probably has the benefit of reducing the costs of transport to the bird as well as providing high-energy meals when needed. The oil also helps to sustain the birds on land: 30% of the energy metabolised by incubating Leach’s StormPetrels has been shown to originate from stomach oils. The lipids also provide a rich diet to their plump, rapidly growing chicks, and tide them over between feeds. One study showed that nearly 80% of energy fed to the chicks of Wilson’s Storm-Petrel was provided by stomach oils, delivered in a thick, oily paste of partly digested fish.
➀ Oesophagus ➁ Cloaca ➂ Caecum ➃ Spleen ➄ Liver ➅ Cystic duct ➆ Gall bladder ➇ Bile duct ➈ Pancreas ➉ Pancreatic ducts Gizzard Proventriculus
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➁ ➅ ➆ ➇ ➈ ➉
Gastro-intestinal tract of Leach’s Storm-Petrel (opened out and in place, respectively). (Artist unknown)
30
Anatomy and physiology
The salt shedder: White-faced Storm-Petrel Storm-petrels are the smallest of the tubenoses Order Procellariiformes. They are so named for the horny, raised, tubular nostrils that sit atop the bill. The storm-petrels are characterised by their prominent fused nostrils with a single opening that is usually inclined upwards. The nostril or naricorn carries salt, secreted by the salt glands (see nasal gland, page 36), away from the body. The salt glands efficiently rid the body of excess salt ingested in food and seawater, beyond that which the kidneys can handle and which could even be toxic. The gland maintains normal salt levels in blood and tissue, an evolutionary solution to the problem of ridding the body of excess salt (sodium chloride). All bird species have paired nasal glands in the orbit of the eye (above the eye), but the glands are small and inactive in all but tubenoses and other birds that live in saline habitats. The glands concentrate salt and can shed up to 90% of the bird’s salt intake. The salty secretion flows through a duct, out the nostril and is channeled down the bill to drip from or be shaken off the tip. The glands are intensely active when needed, such as following feeding, or after drinking seawater, but are otherwise inactive. Their function is thought to be controlled by hormones produced by the adrenal gland. Hence, marine birds, with their relative large salt intake, have larger adrenals than landbirds.
White-faced Storm-Petrel. (Artist: Trisha Wright)
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Brain power: goose As in four-footed animals, the nervous systems of birds is made up of central (brain, spinal cord) and peripheral (spinal and cranial nerves, autonomic nerves, sense organs) components. The avian brain has a cerebrum that is larger than that of reptiles, mainly because of the development of higher centres associated with vision and hearing, but its outer surface is relatively smooth and lacks the complex convolutions that have evolved in mammals. The corpus callosum, which in mammals allows the two hemispheres to share memory and learning, is also absent in birds. The illustration shows the brain of a goose, not generally recognised as the smartest of creatures, but a useful example of a generalised avian brain. The structure and elements of birds’ brains were once thought to indicate that they had inferior cognitive powers to mammals, but their brains are now viewed as simply being organised differently: that is, different structures have evolved to perform similar functions. The smartest known birds, corvids and parrots, are equivalent to the apes in intelligence and have been shown to use deception, ‘read’ their peers (estimate what they are thinking or how they might react), plan for the future and recall incidents from the past. For example, among corvids, crows can build complex tools from elements that are new to them and scrub-jays later secretly move food caches that they think they may have been seen to hide. Avian sleep, which is thought to allow the brain to process memory and save energy, is also as complex in birds as it is in mammals, but sleep activity occurs in different areas of the avian and mammalian brain. Notably, birds can sleep in one hemisphere at a time, so that the other side (and its eye) remains alert for predators. A few mammals have also evolved ways for the brain to be ‘half asleep’ – such as dolphins, which might otherwise drown. These are cases of convergent evolution: similar adaptations have evolved from very different bases. ➅ ➄
➀ ➁ ➃
➂ The brain of a goose. (Artist unknown) 32
➀ Cerebrum ➁ Olfactory bulb ➂ Pituitary ➃ Optic lobe ➄ Corpus cerebelli ➅ Epiphysis
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34
The senses
35
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Sense organs: Budgerigar A bird’s brain fills the skull completely and can be easily damaged because the skull, like all the bird’s skeletal elements, has evolved to be relatively thin for lightness for flight. Most birds have a particularly well-developed sense of vision, so not surprisingly their visual apparatus, which includes the eye and the optic lobe, takes up a relatively large part of the brain case. This displaces the cerebellum caudally, that is, towards the bird’s tail. The cerebellum is part of the central nervous system and is largely concerned with the regulation of movement, particularly breathing and the complexities of flight. Other sense organs are located within the skull, including the auditory apparatus. As in mammals, the ear is the organ of hearing and balance. Birds do not have a fleshy outer ear to catch sounds (although some have modified feathers that perform a similar function; for example, the Barn Owl). Birds’ tympanic membranes transmit vibrations from the ear-opening and auditory canal to the inner ear. Various glands are also situated within the skull: the nasal gland to secrete salt; the gland of the nictitating membrane to lubricate and cleanse the cornea (see also page 144); and the lacrimal glands to moisten the eye and drain it. Inside the eyeball is the large pecten, a pleated fan that is assumed to nourish the retina but for which other functions have been proposed, including detection of movement. It has long been thought that in general the sense of smell is not particularly well developed in birds and that they are primarily visual and auditory in their perception of the world about them. Genetic, anatomical and behavioural evidence now suggest that odour detection is useful to a surprising number of birds. (See also page 45.) The size of the olfactory bulb, for instance, varies between species. The bulb is relatively small in the Budgerigar (below) and other seed-eaters, which have little need of smell to test their food for freshness or ripeness. It is relatively large in waterbirds (see page 32), including rails, cranes and grebes; and it is largest in birds such as the nocturnal kiwi, which by smell alone can detect prey underground or buried in kelp beds. ➀
➁
➂ ➃
➈ ➅ ➆ ➇
➄ Sense organs within the skull of the Budgerigar. (Artist: Trisha Wright) 36
➀ Nasal gland ➁ Gland of the nictitating membrane ➂ Eye ➃ Pecten ➄ Lacrimal gland ➅ Optic lobe ➆ Tympanic membrane ➇ Inner ear ➈ Cerebrum
The senses
Seeing double: Tawny Frogmouth The importance of vision to the large majority of bird species is indisputable. It is evidenced both by the large relative and absolute size of their eyes compared with other vertebrates, the importance of visually guided behaviours such as flight and feeding, and the gaudy plumages of many species. Birds’ colour vision is thought to surpass that of humans and many perceive colours in the ultraviolet range, which humans cannot see. Truly nocturnal birds, however, are thought to be colour-blind. In contrast to mammals, changes in the direction of the gaze of birds are mainly achieved by the turning of a relatively long and flexible neck and by relatively minor eye movements (albeit limited, given the snug fit of the eyeball within the skull). DIVERGENT POSITION
But not all species are the same: there are large
RVA
differences between them in the position of the eyes in the skull and the range of movement of the eye. Some
REVF
species can move each eye independently. Nightbirds
BF
such as owls and frogmouths have particularly large eyes that fill the sockets to such an extent that very little movement is possible. The trade-off is that the field of binocular vision is much greater in the owl, similar to that in humans. This allows it greater LEVF
accuracy in judging distance and detecting movement. An evolutionary compensation for their more-or-less
LVA
immobile eyeballs is that owls have particularly flexible necks that rotate or swivel through an arc of about 180 degrees. CONVERGENT POSITION BF RVA LEV
F
BINOCULAR OVERLAP F REV BF = Binocular fovea LEVF = Left extreme visual field REVF = Right extreme visual field LVA = Left visual axis RVA = Right visual axis
LVA
Tawny Frogmouth. (Artist: Trisha Wright) 37
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Because they are hunters, owls have eyes that are more forward directed than those of birds that have greater need to watch their backs. Hence the blind spot behind the head of an owl might extend through more than 30 degrees while a duck has no blind spot because its eyes are on the side of its head. Snipe, for example, have eyes that are even further back, enabling them to detect predators (and possibly to protect their eyes from splatters, splashes and vegetation) while they are probing for food; their binocular vision may be even greater behind than in front. An interesting consequence of largely lateral (monocular) vision is that the eyes move in counter directions, whereas in birds that are largely binocular the eyes tend to move in the same direction. The illustration shows a frogmouth with its eyes directed more laterally (at top) – for example while being watchful when at roost or on the nest – and directed forwards (at bottom) to create a binocular field for tasks such as hunting and perhaps for defence of territory. A binocular field allows stereopsis – the ability to perceive depth and detail from visual disparities between the two eyes – which is supported by specialised retinal areas and neural pathways. Interestingly, visual deprivation during a critical period early in the life of a chick prevents the development of the visual pathways and the ability to use stereopsis is lost. Birds of prey (owls and diurnal raptors) have also evolved binocular vision to varying degrees depending on their predatory habits, but nightjars have not. It has been argued that the frogmouth is a perch-and-pounce hunter that takes prey from the ground and therefore has need of binocular vision to break the camouflage of its prey, whereas the nightjars have no need of it because they take aerial insects that are easily seen silhouetted or highlighted against the sky. The frogmouth would therefore have greater chance of injury if it misjudged the position of its prey and hence may need more refined detection of distance than the nightjars.
38
The senses
By the light of the moon: Letter-winged Kite The Letter-winged Kite is the only Australian bird of prey uniquely specialised for life in the arid inland. Its core range appears to be along the ephemeral creeks and rivers of the Lake Eyre drainage, but at times it disperses widely across mainland Australia except its driest deserts. The kite has a typical boom and bust life cycle, populations intermittently building up spectacularly in numbers when conditions are favourable, then going bust. Following generous rains, when the kite’s main prey, the irruptive Long-haired Rat, has a boom in population, the kites breed in busy colonies. As the outbreak spreads, some kites follow its front. After months or, rarely, years, the tide of rats wanes and the kites cease breeding, even abandoning their last broods, and disperse in search of better conditions – a few arrive in more coastal areas where they usually perish. Between these brief appearances the kite is little known. Presumably, small populations survive around inland refugia, such as wetter areas of the Barkly Tableland and Lake Eyre Basin, breeding sporadically, until the next boom. Like many creatures of the hot, dry interior, the Letter-winged Kite has become mostly nocturnal. Although it is a capable daytime hunter, especially when night-active prey are scarce, it most often hunts at night. The kite hunts mainly by sight, and at night it depends on moonlight. Unlike some owls (see page 41), it cannot hunt in total darkness. In good times, the kite colony begins to stir an hour before moonrise, which shifts by about an hour a day, and the kites even time the hatching of eggs to coincide with a full moon. To avoid the kites, the Long-haired Rats generally curtail their activity when the moon is above the horizon, but during a plague there is so much activity that the kites have a feast. The Letter-winged Kite belongs to the genus Elanus, a group of small kites that are essentially diurnal but sometimes active around dusk. An evolutionary way to think about its vision would be to predict that adaptations to its eyes for night-time hunting have evolved from an ancestor with an eye suited to diurnal hunting. More importantly, this would mean that its nocturnal
Letter-winged Kite. (Artist: Peter Marsack) 39
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vision evolved secondarily, on the back of diurnal vision, and arose independently of that of owls, for example. Indeed, research shows that the kite’s eyes have evolved from those of a daytime hunter, as expected, and, further, that its specialisation for night hunting is relatively recent. The degree of adaptation of its eyes falls between the diurnal raptors and truly nocturnal birds such as owls. In reality the diurnal and nocturnal hunting birds span the spectrum of adaptation to day or night hunting, from broad daylight to deep darkness. The Letter-winged Kite’s closest relative in Australia, the Blackshouldered Kite, is crepuscular, often hunting at dawn and dusk, so the former’s shift to night hunting has been small but significant. One of the clearest evolutionary signs that the Letter-winged Kite has evolved its night vision secondarily from diurnally hunting ancestors lies in its having two foveas in each of its retinas. The fovea is a pit in the macula of the retina and it is the point of sharpest visual acuity. Further, the fovea refracts light to generate a larger image. More to the point, two foveas are typical of day-hunting birds of prey. Other birds with two foveas include terns, parrots, swallows, doves, kingfishers, swifts and hummingbirds. Birds with two foveas in each eye have them located such that they provide good acuity for coping with the visual challenges of maintaining clear eyesight at speed and the accurate judgement of distance. A few birds, such as some terns and swallows, even have a third fovea. Most, however, including a few birds of prey, have eyes with only one fovea (like humans), which allows them to focus in on particular objects but it also explains why their peripheral vision is mediocre. With their origins from diurnal hunters established, we can nonetheless look at the adaptations of both Letter-winged and Black-shouldered Kites to hunting in reduced light. These include larger eyes to maximise light gathering and an increase in the ratio of rod (night) photoreceptors to cone (day) photoreceptors, more so in the Letter-winged than the Black-shouldered Kite. The F-ratio (ratio of focal length to aperture) of both kites also falls towards the nocturnal end of the spectrum. In the Letter-winged Kite it measures 0.98, compared with 1.11 for the Black-shouldered Kite, which suggests that the Letter-winged Kite has gained a 20% increase in light-gathering ability, and the Black-shouldered Kite less than 10%, since the two lineages diverged from a common diurnal ancestor less than a million years ago.
40
The senses
Silent night hunters: barn owls Owls, especially those that hunt at night, have evolved mechanisms to locate the source of even faint sounds with remarkable accuracy. The best studied are the barn owls, which can locate and capture prey in total darkness, by sound alone. It has a specialised auditory system enhanced by a concave facial ruff of stiff feathers that channel sound to its ears (technically, its inner ears, because it has no external pinnae). Asymmetrically oriented ear openings, the left higher than the right, allow the owl to pinpoint the source of the sound to within 1.5 degrees in both horizontal and vertical planes by differences in the timing and pitch of sound reaching each ear. From the sounds received, the owl’s brain produces a spatial map of its prey’s location. The asymmetry of the skull of owls and cetacean mammals such as whales is an example of convergent evolution – the same response in unrelated groups to similar selection pressures. In fact, it appears to have evolved at least five different variants among all owls. That is, each variant is a slightly different evolutionary solution to the problem of locating prey in darkness by sound. Compared with many nocturnal birds, tytonid owls have small eyes, indicating that sound is more important to them than sight. Some of the other, bigger-eyed owls of the strigid family of hawk owls depend more on sight and an intimate knowledge of the perches and other elements of their territory.
Eastern Barn Owl. (Artist: Trisha Wright) 41
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Nocturnally hunting owls have evolved other traits in response to the selection pressure of needing to hunt efficiently at night. The leading edges of their primary feathers have stiff fringes that reduce noise. The trailing edges of their primaries have soft fringes (fimbriae) that help to reduce turbulence where air flows across both sides of the wings. These two traits variously lead to silent flight by breaking up the sound waves that would normally be generated by the flow of air around wings during flight. Downy surfaces of the primaries, secondaries and wing feathers absorb more sound than in most birds. Owls also have a zygodactylous toe arrangement, with two similar-sized toes directed forwards and two backwards. This extends the capture area and allows an even, two-pronged grasp compared with the more usual avian arrangement of three toes forward, one back (and variously sized toes) – obviously an advantage under conditions of poor visibility.
Interlude: Evolution of many traits for one purpose The evolution of owls reminds us of a salient point. The evolutionary response to one kind of selection pressure, in this case the need for efficient hunting at night, can lead to evolution of multiple traits that work together as a single adaptation: silent hunting in darkness. We could develop this kind of argument for many groups of birds and so we should remember that it is not unique to owls. Owls are so readily recognisable, however, that they help us make the argument clearly. First, a phylogenetic perspective informs us that owls are a distinct and cohesive part of the evolutionary tree of birds. In more concise, if technical, terms owls are a monophyletic group and form a strongly supported clade in the phylogenetic tree of birds. This is the basis for arguing that the traits they share evolved in their common ancestral lineages as it became more efficient for those ancestors to exploit a resource that other birds and predators could not. Yet, we have seen that even one of these traits, the asymmetry of auditory openings, is not the same across all owls and that too appears to have evolved a diversity of its own.
42
The senses
Sight and sonar: Australian Swiftlet The short-legs of swiftlets give the family its name, Apodidae, meaning ‘without feet’. Swiftlets spend much of their life on the wing, soaring and dipping erratically on stiff wings as they forage aerially. At night they often roost clinging to a rock wall rather than perching. The swiftlets have two ways of ‘seeing’: sight and sonar. They use echolocation to negotiate the dark cavities where they build their nest colonies and roost. The flock members make incessant, audible clicks and use the returning echo from rock walls to navigate. The darker it is, the shorter the interval between their metallic clicks. This is a form of sonar, but the birds do not use it for hunting as do many bats. Instead, the swiftlets feed by day, using vision, aided by their large eyes. The swifts specialise in hunting aerial swarms such as those of mayflies and the nuptial flights of termites but
Australian Swiflet. (Artist: Trisha Wright)
they also take a wide variety of spiders and other flighted or wind-borne invertebrates. Their extremely wide, short bill, surrounded by sensitive bristles, forms an effective insect trap for aerial capture and helps to shield the eye. Not all species of swift navigate using echolocation but this ability seems to have evolved several times within the family.
43
Stray Feathers
Seeing through the mud: Great Knot Many shorebirds probe mud or sand in search of prey. How do they sense when prey are present? Under the horny layer of the Great Knot’s bill, within pits in the bones of the upper and lower ‘jaws’, there are clusters of nerve endings that are thought to be capable of detecting pressure gradients in the
5 mm
substrate. These are known as Herbst’s corpuscles. The bird probes about half a centimetre into the substrate, compacting it and sending out a pressure wave. Changes to the wave reveal the presence, or absence, of food items deeper down. Herbst’s corpuscles also occur in other birds and in other parts of the body, such as the tongue and wings.
Upper and lower mandibles of the Great Knot. (Artist: Trisha Wright)
44
The senses
The smell of the sea: shearwaters and storm-petrels Unlike mammals, scent is not generally regarded as central to the lives of birds (see also page 36). Yet, stormpetrels and other procellarids (shearwaters, prions and petrels) use odours to find their nest burrow among hundreds of others in the dark; to distinguish their partner and chick; and to guide them across vast tracts of apparently featureless oceanscape. Marine trials have shown that, as well as sight, the storm-petrels use their highly developed sense of smell to locate food in daylight and at night, scanning the breeze for airborne scents and tracking scent gradients to oceanic areas rich in prey. Aromatic chemicals, such as dimethyl sulphide, which smells like rotting seaweed, are released when zooplankton consume phytoplankton. The plankton concentrate at upwellings, which are associated with seamounts and ridges on the ocean floor, and thus provide an olfactory map of the ocean – a way by which birds can navigate across the ocean. The scents of fish oil, krill and squid have also been shown to attract these seabirds from downwind. An impressive nostril (tubenose) and an exceptionally large olfactory bulb in the brain have evolved to assist the birds with this olfactory navigation and identification system. Albatrosses have recently been shown to have similar sensory abilities.
Shearwaters (far left) and storm-petrels. (Artists: Nicholas Day and Trisha Wright, respectively) 45
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Interlude: The sensory world of birds – more than meets the eye We humans are very visual animals. It is easy for us to see birds as also being predominantly visual organisms. For most birds, this is probably reasonable. Nonetheless, we should begin to suspect that evolution has led to more than just sight in the sensory world of birds when we remind ourselves that spectacular visual displays are often accompanied by just as impressive sounds. Birds make these sounds through their own vocalisations or occasionally through specially evolved adaptations of their wing feathers. Think again, for example, of the asymmetric skull of some owls that aids them in using sound to locate their prey. We can begin to appreciate that the evolution of birds, particularly how they forage and conduct their courtship displays, has seen them respond to pressures from their environment that have resulted in development of sensory mechanisms that are not so readily obvious to us. Consider the adaptation to the marine environment that was described in the previous section: seabirds’ ability to smell the dimethyl sulphide that results from the feeding activities of zooplankton. How would natural selection have led to this? We know from work on mammals that there are more than 1000 gene regions coding for the molecules that can detect odours; that is, they act as olfactory receptors. In humans specifically, we even know that there are population-level differences in the number of different genes that are actively expressed for these receptors, which implies different olfactory abilities between different populations. Birds would almost certainly have a similar diversity of genes, each of which is either active or inactive in the different groups, but nonetheless are present in the avian genome. This is essentially a testable hypothesis relating to avian evolution. The tactile sense is another that is more developed in birds than we often think, particularly in their fine adjustment during flight. Evolution’s capacity to adapt birds to more efficient ways of finding food with this sense rather than just sight would similarly have opened up the niche of feeding on invertebrates in mudflats. But think about what else has evolved. In order to forage in the mud of an estuary at low tide, a shorebird bird must be able to walk across mud without sinking into it. So the anatomy and structure of the legs need to respond to those needs. Estuarine mudflats support a great variety of invertebrates and the different morphologies of shorebird bills have evolved to partition out that resource according to size and behaviour of invertebrate prey. Further, some of the iconic birds of New Zealand, the various species of kiwi, feed by foraging for invertebrates in washed-up drifts of kelp and they do so at night. Vision clearly is not playing a great role here. Why is it that kiwis have their nostrils at the tip of the bill rather than its base? They too are probably detecting odours of metabolic byproducts of their prey.
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48
Giving voice
49
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Sophisticated syrinxes: Budgerigar, ducks and geese Birds have evolved a variety of ways to communicate aurally: •
via sounds from their syrinx, the equivalent of the voice box, or from their windpipe; and
•
via mechanical sounds such as wing rustling (birds of paradise in courtship) or whirring (some pigeons as a warning); bill clicking (owls, in warning) or clacking (storks in warning); and drumming with a stick held in the foot (Palm Cockatoo in display).
Despite some birds’ ability to mimic the human voice, they do not produce sounds from a larynx. Instead, uniquely, birds have a syrinx, located at the base of the neck, an expansion of the trachea (windpipe) just before it divides into two. Like the trachea, the syrinx is formed of rings and semi-rings operated by an overlying sheath of muscles. The syrinx is a more complex sound generator than the larynx, although both operate by the forcing of air through the trachea, which causes a system of membranes to vibrate and produce sounds. In birds, sounds are created in expiration using nearly all the air passing through the respiratory system, and the flow of air is almost continuous (see page 27), so that bird song can be prolonged and seamless. Humans, by contrast, use only about 2% of air to speak, during clearly separate exhalations. The syrinx is suspended in the clavicular air sac, one of the many air sacs that ventilate a bird’s lungs, and this suspension is vital for syringeal sound production. In songbirds, sound is produced by a pair of thin tympanic membranes inside the syrinx. Because the syrinx straddles two tracheal tubes, each with membranes, some birds (e.g. thrushes) can even self-duet, generating two different sounds at once. Other songbirds can breathe through one side of the syrinx while singing through the other.
Trachea and syrinx of the Pacific Black Duck. (Artist: Ian Faulkner) 50
Giving voice
Some non-songbirds lack tympanic membranes, instead having an external membrane on the side of the trachea (e.g. the Emu, page 54). Penguins have much reduced syringeal complexity and ducks have a modified syrinx. In some male ducks, for example the Pacific Black Duck, the syrinx is expanded asymmetrically on the left side to form a chamber that increases resonance (pages 50 and 52 with images showing the bulla: the bump on the right arising from the syrinx). The parrots, including the Budgerigar, have relatively simple vocal organs – see illustration below showing the ventral view of the cartilage (A) and overlying muscle of the syrinx (B). Parrots’ talking ability seems to stem mainly from the spoon-shaped tongue of the talking species, and not from a sophisticated vocal apparatus. The syrinx has been used as a key feature in the taxonomic classification of birds, especially the passerines. The non-passerines and the suboscines (‘primitive’ songbirds, mostly of the Southern Hemisphere) have a simpler syrinx than the modern songbirds (the oscines), especially differing in the complexity of the musculature. For example, the oscines have five to eight syringeal muscles, the sub-oscines four or fewer. Some birds, such as penguins, lack the intrinsic muscles altogether. Within these groups there is enormous variation in syringeal structure and the ability to produce sophisticated sounds. In songbirds the degree of development, with respect to the muscles and their attachments, is generally linked to the quality of the song repertoire.
A
B ➄
➀
➁
➂ ➃
➀ Trachea ➁ Syringeal box ➂ Tracheal membrane ➃ Tympaniform membrane ➄ Sternotracheal muscle ➅ Bronchotracheal muscle ➆ Bronchial muscle ➇ 4th bronchial semiring
Vocal organs of the Budgerigar. (Artist: Trisha Wright) 51
➅
➆
➇
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Even in the non-passerines, the structural variation between species is useful for discerning relationships and tracing evolutionary history. The Anatidae (ducks and geese), for instance, have several distinct syringeal arrangements, sometimes used, with other characters, to assign species to subfamilies, which in Australia include the:
(a)
•
whistling-ducks (represented by Plumed Whistling-Duck);
•
stiff-tailed ducks (represented by Musk Duck);
•
geese and swans (represented by Cape Barren Goose); and
•
shelducks (represented by Australian Shelduck).
(b)
(c)
(d)
10 mm Syrinxes (from above) of the males of (a) Australian Shelduck, (b) Cape Barren Goose, (c) Plumed Whistling-Duck and (d) Musk Duck. (Artist: Ian Faulkner) 52
Giving voice
Built-in bagpipes: Magpie Goose and Trumpet Manucode The length of the windpipe of most bird species matches the size of the bird. However, in a few species it is markedly lengthened or coiled. The extended trachea serves to amplify the birds’ calls, giving them a farcarrying, resonant quality, disproportionately loud for the size of bird. Similar acoustic adaptations have evolved several times in different bird groups, ranging from cranes to northern swans and the manucodes. The character can be sexually dimorphic. Male Magpie Geese and female Painted Snipe (i.e. the larger sex of each species and the one that does the most advertising and competing for mates) each have a single very long loop whereas their opposite sex has none. By comparison, both sexes of the monomorphic manucodes have a trachea with several loops. In the Magpie Goose the syrinx is small but the trachea of the adult male coils between the breast muscle and the skin, reaching a length of about 150 cm and extending the entire length of the bird’s body. His falsetto honking call is much louder and far-carrying than the female’s and his peaked bony crown may also act as a resonator. The trachea of the male develops from simple and straight to a long coil at about 2.5 years, when sexual maturity is reached. In the hand, adult males can be distinguished from females by feeling the enlarged windpipe. Uniquely
among
passerines, the
Trumpet Manucode, especially the male, has a highly convoluted trachea, much more so than that of the Magpie Goose. The male’s distinctive deep, mellow bugling call, made from a high branch, attracts females from afar. The manucode is not known to be territorial but its resonant call may also be useful for maintaining contact in its dense tropical habitat. Tracheas of the male Magpie Goose (left) and male Trumpet Manucode (right). (Artist: Ian Faulkner) 53
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The air drummer: Emu Adult emus produce a variety of sounds by resonance of air, which they can pass directly from the trachea to the cervical air sac through a fenestra. On the ventral side of the trachea (i.e. facing the front of the Emu’s neck), five to 20 ossicles of the fenestra are incomplete, leaving a slit-like opening into the air sac (see below). In chicks the opening lies a little above the base of the neck, and is covered with a membrane until the bird is six to 12 months old. When the membrane ruptures the Emu can make its typical booms, drums and grunts by reverberation in the cervical air sac. The cervical air sac wall is a membrane, but it is partly overlain by a muscle that apparently stretches the membrane against the pressure of the air forced into the sac and improves its quality as a drumskin.
Tracheal fenestra of the Emu. (Artist: Martin Thompson)
A pair of Emus, the female with fully extended throat sac and booming. (Artist: Martin Thompson) 54
Giving voice
A sound-sensing helmet? Southern Cassowary At up to 70 kg, the Southern Cassowary is the heaviest bird in Australia. This shaggy black, flightless rainforest giant has a double red wattle that hangs from its blue-skinned neck, while a horn-like casque adorns its head. Although it is often described as horny or bony, the casque has a core of firm foamy material, riddled with cells and canals, and covered by a spongy layer and a tough, keratinous, outer sheath. Its purpose is unknown, but one possibility is that it is for sexual attraction. Another is that it protects the skull as the bird bashes its way, head lowered, through the bush when running. Other suggestions are that it is used as a weapon in dominance disputes, or as a tool to push aside leaf litter during foraging. Observations of behaviour lend little support to any of these proposals. A more recent suggestion is that the casque is involved in sound reception. The cassowary makes a low booming call, the lowest known birdcall and so low in frequency that it is at the very bottom end of the range of human hearing and can be felt as well as heard. Low frequency sounds attenuate little over distance, so they are useful for long-range communication. If the casque aids in sensing these low booms, it may have a role in auditory communication between these solitary birds in the dense rainforest.
Southern Cassowary. (Artist: Trisha Wright) 55
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The roarer: the Australian Bustard The stately Australian Bustard is the heaviest of the country’s flying birds. Not surprisingly, it is largely terrestrial, with feet modified for walking (no hind toes), and it moves sedately across the grasslands and scrub-covered plains with bill raised aloofly. When conditions are right for breeding – springtime in the south, or after rain – the male selects a raised spot from which he courts females. He becomes a strutting show-off. Extending his inflated white-feathered breast sac almost to the ground, he cocks his tail forward over his back and tucks his neck and head back amongst the feathers. Marking time with his feet so that his sac swings and twists irresistibly, he points his bill skyward, balloons his throat and makes a boom like the distant roar of a lion. If females indicate interest his display becomes even more intense. Externally, the male’s plumage adds to the display. Internally, male bustards have evolved a modified oesophagus that they dilate to enhance their spectacular display and resonant call. Females may visit several males, each displaying on their own arena, and they are thought to tend to choose the largest male with the most elaborate display. This mating system is known as exploded lekking – exploded because at most leks males gather at particular
Tongue
sites and their arenas are within sight of each other, but advertising male bustards are spaced up to one kilometre apart.
Trachea
Distended oesophagus
Australian Bustard. (Artist: Trisha Wright) 56
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Tongues talking
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Nectar straws: honeyeaters, silvereyes and sunbirds Like bills, the tongues of birds come in many shapes and sizes, adapted mainly for their role in feeding. Tongues have many tactile sensors to identify foods and help position them for crushing and swallowing. Some birds have highly specialised tongues. Penguins’ tongues, for example, have backward-directed spines to grip fish and send them towards the throat. Shovellers’ tongues are fringed to sieve small prey from water. However, the tongues of birds such as owls and pelicans, which bolt food whole, are quite rudimentary. Different bird families have evolved similar ways to tackle nectar feeding. Many typical honeyeaters lap nectar with a brush-tipped tongue. Silvereyes and sunbirds have curling and fraying edges of the tip. All collect nectar by capillarity, down grooves or troughs in the tongue. The different bill and tongue shapes and lengths are adapted to best suit particular flower shapes or a more generalised nectar diet, and may even differ between the sexes in some species: all act to limit competition for resources. The famously brush-tongued honeyeaters use their bill and tongue to harvest a wide variety of foods. Fluids such as nectar and honeydew are collected with the tongue, while fruit, lerps (layers of crystallised honeydew secreted by the larvae of psyllid insects) and arthropods are gathered in the bill. Most insects, fruit and lerps are grasped near the tip of the bill and then transferred to the mouth by a series of gulping actions that involve the tongue. The typical honeyeaters (Meliphagidae) have a distinctive, elongate tongue that is divided distally into two, four or eight parts, each with a brush-like extremity composed of fine terminal and (sometimes) lateral bristles (see page 62). The number of bristles on the tip of the tongue varies, although most species have at least 50 and some of the larger ones have more than 100. Nectar and other fluids are drawn by capillarity along grooves in these bristles and into a broad dorsal trough that leads to the base of the tongue and the oesophagus. Despite their insectivorous diet, the chats and Gibberbird have similar tongues to those of the
The tongue of the Silvereye, viewed from the side (left) and from above (right). (Artist: Trisha Wright)
typical honeyeaters, but one species eats nectar and
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Tongues talking
some of the others probe flowers for insects. This feature (among others) adds weight to an evolutionary finding of molecular studies: that the chats are a highly modified group of honeyeaters. But variations of the brush-tongue have evolved independently several times. The Silvereye’s tongue is as specialised as that of nectar-dependent meliphagids, to which it is unrelated. Although nectar often forms a small portion of the Silvereye’s highly variable diet, its tongue (see page 60) splits into four sections with frayed ends, and a division at the tip links to a channel that rapidly sucks up nectar by capillary action. Even among parrots, the Swift Parrot has evolved a brushtipped tongue. For many years this led ornithologists to consider it a lorikeet but we now know from a range of morphological and molecular data that it is a member of the rosella-like group of parrots that has adapted to a nectarivorous diet. The extra-long tongues of sunbirds resemble those of their closest relatives, the shorter-tongued flowerpeckers, and the Mistletoebird, which eats berries. The distal two-thirds of the Yellow-bellied Sunbird’s tongue has upturned edges forming a tube that divides near the tip (see lower mandible and
Hyoid apparatus
Distal end of tongue
tongue tip at right), and the long horns of the bony hyoid apparatus of the lower mandible are adapted to guide insertion of the lengthy tongue into the deepest flowers.
The lower mandible (left) and tongue tip (right) of the Yellow-bellied Sunbird. (Artist: Trisha Wright)
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Brush tongued: Spiny-cheeked Honeyeater Birds’ tongues are rarely noticed but the broom-like tongues of honeyeaters came to the attention of the earliest of the European colonists, if only for their curiosity value. Honeyeaters’ long tongues divide into two, four or eight parts each of which further separates to form a brush tip of numerous fine, flexible bristles. The illustration shows the 25 mm long tongue of a Spiny-cheeked Honeyeater from above and in crosssection at various points along its length; it has about 60 bristles. Other species have between 50 and 100 bristles. The bristles are concave and empty into a trough that traverses the length of the tongue almost to the root. The honeyeater inserts its sickle-shaped bill into a flower, extends its tongue into the nectar chamber, and by rapid licking collects nectar, which travels up the tongue by capillary action (without need for sucking), and empties into the throat. The broad spread of the ‘broom’ is very effective for mopping up scattered honeydew, and for feeding at plants with a thin film of nectar distributed over a broad surface. Honeyeaters’ tongues are very efficient conveyors of nectar. They are easily extended five to 15 mm beyond the tip of the bill, and can lick at rates of six to 12 licks/second. Most honeyeaters studied harvest 90–100% of the nectar from a flower during a visit, but occasionally take only 70%. Their visits are rapid: they probe about 15 flowers per minute for some plants, but more than 100 flowers in a minute when visiting others. Of course, the rate at which honeyeaters harvest nectar is influenced by a variety of factors including the distribution of flowers and flowering plants, floral morphology, and nectar composition, concentration and volume (which decrease as the day progresses), and the size of the bird itself. ➀
➀ ➁
➂
25 mm
➁
➂
➃ ➃
The tongue of the Spiny-cheeked Honeyeater from the side (left), above (centre) and sections at various points along its length (right). (Artist: Trisha Wright) 62
Tongues talking
Sweet tongued: Rainbow and Scaly-breasted Lorikeets Trichoglossus, the Rainbow and Scaly-breasted Lorikeets’ generic name, means hairy tongue. To support the birds’ sweet habits, the tip of their tongue is like a stiff brush and highly specialised for efficient feeding on nectar and pollen inside blossoms and other flowers. All lorikeets and the Swift Parrot show a suite of dietary adaptations not found in seed and fruit-eating parrots. Their longer, thinner tongues allow them to probe and manipulate flowers more dexterously than other parrots. The surface of the lingual tip has small projections (papillae), which are arranged in concentric semicircles and can be raised and folded down. In contrast, the tongue tip of most parrots is smooth with radially arranged grooves and can be modified from spoon-like to flat in shape (hence the talking ability of these parrots). Typically, lorikeets take the whole flower in their bill and move their bristly tongue around the floral cup in a circular manner, gathering nectar and pollen in the process and leaving the blossoms intact so that they can produce more nectar. In comparison, the unspecialised rosellas chew and destroy eucalypt flowers to extract the pollen and nectar.
Rainbow Lorikeet. (Artist: Trisha Wright) 63
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The sugars in nectar require much less intestinal processing for absorption than most other foods. Pollen, on the other hand, is a rich source of protein but is not easily digested; much of it simply passes unchanged through the bird. Lorikeets’ reduced gizzards (less muscular than in other parrots) and short intestines may allow fast processing of the food ingested, allowing them to obtain a high nutrient return from pollen simply because of the large amount that can be processed in a given time. Indeed, the digestive systems of Swift Parrots and Musk Lorikeets have been shown to empty Eucalyptus pollen grains efficiently and to be adept at rapidly ingesting large quantities of pollen.
Scaly-breasted Lorikeet. (Artist: Trisha Wright) 64
Tongues talking
Fork tongued: Rufous and Black-tailed Treecreepers Treecreepers feed on a wide variety of arthropods found on or beneath the bark surface of trees, as well as on the ground. They eat large numbers of ants, but these appear to be a cheap staple and the birds eagerly seek other more nutritious prey. Treecreepers glean prey mainly by pecking at the bark or ground surface, often while still climbing or hopping; probing in fissures, under loose bark, and into curled strips of bark (eucalypts) or epiphytic lichen (in rainforest); or excavating bark by hammering and tugging at loose bark fibres or flakes. At certain times they pursue insects and hawk them in the air, and also feed on nectar. The treecreepers use their tongues to ‘sweep’ up insects, and its structure possibly aids uptake of nectar, although it is not as brush-like as the tongues of honeyeaters. The treecreeper tongue is quadrifid (divides into four sections), and fringed at the tip, most likely to facilitate the extraction of ants and other insects from deep cracks or holes in bark.
The tongues of Rufous (left) and Black-tailed (right) Treecreepers. (Artist: Trisha Wright) 65
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Shelling seed: parrots All parrots, except lorikeets and the Swift Parrot, eat at least some seeds and small nuts. They nimbly remove the shell of seeds small enough to fit within the bill, using a characteristic seed-shelling system. Seeds too small to be shelled may be swallowed whole. Essentially the same method is used to remove the fleshy part of berries or fruits to free the seed within – for example, when the Double-eyed Fig-Parrot extracts seeds from ripe figs – or to open small galls to remove the insect grub. The basic mechanism is shown in the illustrations below: from the left (1) the seed is held in place with the tongue while the cutting edge of the lower mandible pierces the seed shell and separates the kernel from the lower half of the shell; (2) the tongue rotates the seed; (3) the cutting edge of the lower mandible removes the remaining shell half. Parrots have extraordinary numbers of sensitive touch receptors on the dorsal side of the tongue, especially in the tip as well as in the mouth, which assist them with their complex feeding and seed-shelling behaviours.
A seed-eating parrot. (Artist: Trisha Wright)
Double-eyed Fig-Parrot. (Artist: Trisha Wright) 66
Tongues talking
A quick drink: Red-capped Parrot and Rainbow Lorikeet Acutely attuned by natural selection to their vulnerability when drinking, parrots first settle quietly on a tree or shrub near water, or circle overhead several times, checking for predators. If all is clear, they swoop down to the ground, walk or run quickly to the water’s edge and drink for a few seconds before flying off again. They may also climb down to the water on overhanging branches. Amidst the flurry of the flock, Budgerigars often alight on the water and drink while floating briefly. Parrots probably drink dew from foliage more often than has been observed, because of its advantage in arid regions and the reduced risk of predation. The Red-capped Parrot, in common with most parrots, drinks by scooping with its tongue, ladling water with the spoon-shaped tip of its tongue. By contrast, lorikeets drink by rapid lapping: repeatedly immersing their elongate brush-tipped tongue and retracting it quickly and completely into the mouth cavity.
Red-capped Parrot (left) and Rainbow Lorikeet (right). (Artist: Trisha Wright) 67
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68
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Flexible feathers: Budgerigar Birds’ feathers are their single most evolutionarily distinctive trait. Highly complex structures, they are derived from the integument, that is, the skin. They are remarkably light and strong, with high tensile strength. As the illustration shows, feathers provide streamlining, forming an outer shell that evens out a bird’s surprisingly scrawny, bumpy contours so that it slips more easily through the air. They also provide insulation and waterproofing, sensory input, articles of display and, not least, a means of flight. Feathers have freed birds to take to the air and certainly aided in their dispersal across the globe. The great diversity that has evolved in the amount, colouration and patterning of feathers helps distinguish individuals, gender, age classes and, of course, species. Individuals can use and manipulate their feathers to signal threat, alarm, and even fear and lust.
Body contours of the Budgerigar. (Artist: Trisha Wright) 70
Plumage
Featherlight: Crimson Rosella Despite appearances, most birds are not uniformly covered in feathers; instead, their feathers are attached in rows or tracts interspersed with bare areas of skin. In the early 19th century, a whole science, pterylography, ptilology or pterylology, grew up around the study of feather tracts, or pterylae. This was based around the fact that the pattern of distribution of the feathers over the body (pterylosis) varies among bird families, potentially making it a trait that can be used to study evolutionary history. The ratites (e.g. Emu and cassowary in Australia) are an exception to the general pattern: their bodies are uniformly covered with feathers; even the apparently bare areas of skin on the neck are actually clothed in tiny feathers. The penguins are a close second: they are almost completely uniformly coated in feathers. The other birds have extensive featherless areas hidden from view by overlying feathers. One notable peculiarity of some use in classification of birds is the distinction between eutaxy and diastataxy: the distinction of whether the fifth secondary flight feather is present or absent, respectively. Passerines for example are eutaxic but non-passerines are more generally diastataxic, with some groups such as pigeons being
Feather tracts of the Crimson Rosella. (Artist: Trisha Wright) 71
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variable. It remains unclear whether eutaxy and diastataxy serve any adaptive role in avian biology or whether they mainly help us with Scrabble and crosswords. Even though feathers are ‘light as a feather’, the entire plumage makes up 15–20% of a bird’s weight, and a feather’s pulpy base is its heaviest part. Hence in flighted (or volant) birds, arranging the feathers in tracts interspersed with naked areas has evolved as a way to minimise the number of feathers, which in turn reduces weight.
Crimson Rosella. (Artist: Trisha Wright) 72
Plumage
A diversity of feathers: Budgerigar Birds have several kinds of feathers. The main structural types are: large stiff remiges and rectrices (the flight feathers of the wing and tail, respectively); the small to moderately sized, basic, vaned firm feathers of the body and wing-coverts (contour feathers); small, fluffy down feathers (which form a warm undercoat); hair-like filoplumes and tiny, occasionally long, bristles on the face. In reality there are all sorts of gradations between the general types, and not all species have every type of feather. Variations of the typical contour feather of a Budgerigar (illustrated) sheath a bird’s body. In many species the feather Contour feather
has an aftershaft, the barbs of which are fluffy and do not lock together to form a flat sheet, or vane, as on the main feather. Viewed under the microscope, as shown in the lower drawing, these plumulaceous barbules have nodes, which are different shapes in different bird
Aftershaft
families. The size of the aftershaft varies considerably, and can be as large as the contour feather itself in the Emu and cassowaries. Of course, birds’ plumage has evolved to suit them to their particular environmental and individual needs.
Macroscopic (above) and microscopic (below) views of the structure of a contour feather from a Budgerigar. (Artist: Trisha Wright) 73
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Feathers are better than fur: Emu Among many functions, feathers and fur protect their wearers from overheating and solar radiation. Lighter colours generally reflect more solar radiation, yet the Emu has shaggy brown to grey-brown feathers with black tips. A comparison of heat regulation with that of another prominent denizen of the arid zone, the Red Kangaroo, showed that as expected, the Emu’s coat absorbs 83% of the solar radiation, much more than the kangaroo’s lighter-coloured fur at 61%. But colour and absorptivity are only part of the story – coat depth and density (and wind speed) also play a role. Even though the Emu’s plumage absorbs a high proportion of the sun’s heat, it is captured in the surface layers then shed back to the environment. The Emu’s dense, loosely packed inner feathers prevent much of the heat reaching the skin. How does this compare with the kangaroo? In the shade, the kangaroo’s heat load is minimal, but in the sun as much as 25% of incident radiation is transferred to the skin. On the other hand, the Emu’s plumage provides almost complete protection from solar radiation even in full sun, which explains why on hot days the kangaroo often lolls in the shade while the Emu can feed in the open. The Emu and Red Kangaroo have evolved different combinations of behavioural, morphological and physiological mechanisms to cope with the stresses of a hot, arid environment. One such trait is that the Emu is more diurnal whereas the kangaroo tends to be more active at night. (See also page 29.)
Emus. (Artist: Martin Thompson) 74
Plumage
Looking after feathers: Budgerigar Feathers need maintenance through grooming. They are made from keratin, as are reptilian scales and human fingernails. Once grown, they are not capable of further growth and over time they wear and become brittle, and need to be replaced. Some species replace feathers from all the tracts over a relatively short time (a complete moult), others replace only some tracts or parts of tracts in any one period (partial moult). Annual moulting of flight feathers, especially, is a major energy cost, and for species that become flightless temporarily, it can make them more vulnerable to predation. There is therefore much biological interest in studying the timing and sequence in which different birds moult their feathers and relating this to the environment in which they live. In birds, apart from glands in the skin, which produce oil, and in the ear, which produce wax, the most obvious gland is the preen gland, or uropygial gland, a pair of which are situated on the top of the tail-bone (the pygostyle). A few birds, including the Emu, Bustard and pigeons and many parrots, do not have a preen gland; instead they may have powder down (they have special down which fragments and soaks up oil and dirt) or a dust bath to cleanse the feathers. Conversely, the gland is especially well developed in ducks, petrels and pelicans. The Budgerigar, however, is among the parrots and many other birds, that do have the gland, and it is tipped with a tuft of eight small feathers that act like a wick. When touched, the gland releases an oily secretion (mainly diester waxes called uropygiols), which the bird strips from the wick with its bill or by rubbing its head against it and distributes through the feathers. Not only does the oil stop the feathers from becoming brittle, but it contains chemicals that protect the feathers from fungi and bacteria and may deter feather lice and mites. There has been considerable debate about the waterproofing function of the uropygiols. They are hydrophobic, but recent experiments suggest that they primarily function to condition the feathers and maintain feather microstructure, but that the microstructure itself has a more important role in keeping the plumage waterproof.
The preen gland of the Budgerigar: atop the spinal column (left) and in cross-section (right). (Artist: Trisha Wright) 75
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Hung out to dry: cormorants and darters Cormorants and darters are closely related diving birds. Both regularly stop foraging to perch with their wings and tail spread in a characteristic cruciform pose. The explanation for this peculiar habit is generally thought to be that the birds are drying their plumage. Evidence for this is found in the observation that the birds hold the posture longer when the breeze is low and that they face the wind and adjust their orientation to the direction of flow. But why do they need to dry their feathers when other diving birds do not? Like most animals, birds are naturally buoyant. Cormorants and darters decrease their buoyancy by having easily saturated plumage. Their plumage does not lack waterproofing oils; instead, the feathers have a microstructure that lets water into tiny spaces in them. With so much water onboard, the cormorants and darters cannot bob on the surface of the water; instead they swim with their body submerged and head and upper neck above water. Herein lies the answer to the question of to dry or not to dry. Evolution has resulted in different strategies that enable different diving birds to submerge efficiently. These differences in buoyancy also suit them to fishing at different depths from each other, thereby reducing competition for food. Yet reducing buoyancy by increasing the wettability of feathers compromises insulation. Cormorants have a thin layer of waterproof feathers that helps to keep them warm. Darters’ plumage provides particularly poor insulation and the birds must warm themselves in the sun after a dive, hence they have mostly black, heatabsorbing plumage. That is also why darters tend to keep their wings outspread even after they dry: to maximise the area that is exposed to the sun. By contrast, the deep-diving cold-water penguins, which stay submerged longer and have an even greater challenge to keep warm, do not get wet because their feather structure is not as open. They reduce buoyancy by moving their feathers to release air from the plumage, without allowing water to penetrate. That is why penguins have no need to hang their feathers out to dry. Again, these examples show how evolution draws on different mechanisms generated from the randomness of mutation to respond to similar environmental pressures.
Australasian Darter in the water. (Artist: Trisha Wright) 76
Plumage
Little Pied Cormorant (top) and Australasian Darter. (Artist: Trisha Wright) 77
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Blending into the background: Spotted Nightjar and Tawny Frogmouth Many ground-birds rely on camouflage for protection. Blending into the background is an effective defence against predators. When disturbed, the ground-nesting Spotted Nightjar closes its eyes to slits and remains immobile. Its dead leaf and mottled bark colours blend seamlessly with the litter of the woodland floor. If a predator approaches too close the nightjar may creep away unnoticed, then at a safe distance burst into flight, distracting the predator away from the nest. Cryptic plumage and behaviour are characteristic of the caprimulgiforms (frogmouths, nightjars and owletnightjars). The Tawny Frogmouth uses a similar defence, freezing into the form of a broken off branch, its tree-trunk plumage and whiskery face adding to the effect. When threatened, the adults of both species make an alarm call that signals to the chicks to remain quiet and immobile until the coast is clear. Immobility ensures that the camouflage provided by their feather colours and patterns is not broken.
Spotted Nightjar. (Artist: Trisha Wright) 78
Plumage
Tawny Frogmouth with nestling. (Artist: Trisha Wright) 79
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Don’t mess with me! Australian Painted Snipe, Eastern Barn Owl and Spotted Nightjar When threatened, many birds make themselves look as big, bold and formidable as possible, hoping to deter and, for some, to confuse predators visually. Feathers play a big role in this subterfuge, by helping to create the illusion of size or through startling colours and patterns. The female Australian Painted Snipe, for example, makes a frontal (pictured) or lateral display. It holds its head low and looks the predator in the eye, with wings fully extended and tail fanned. If pressed it may charge, give a hissing threat call and jab with bill. In the lateral display the bird crouches with the near wing folded or drooped to the ground, and the far wing raised high and fully fanned. When cornered, the Eastern Barn Owl fixes its intense dark eyes, framed in a heart-shaped ruff, on potential predators, droops its wings and sways from side to side, making a clicking sound. It may also fully extend and fan its wings. At rest Spotted Nightjars are cryptic, their earthy colours blending with their surroundings, but they use their brilliant patterning to great effect when threatened, showing their white throat and white wing patches and hissing.
Australian Painted Snipe. (Artist: Trisha Wright) 80
Plumage
Eastern Barn Owl (top) and Spotted Nightjar. (Artist: Trisha Wright) 81
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Creating a diversion: Bush Stone-curlew To divert attention from their young or nest, the ground-nesting stone-curlews make a superficially similar display to their warning display. If disturbed at the nest, the bird feigns surprise, makes an alarm call and flops around with one or both wings hanging. Using this ‘broken-wing act’ the bird lures the predator, which is feeling assured of an easy meal, well away from the nest, then makes a miraculous recovery.
Bush Stone-curlew. (Artist: Trisha Wright) 82
Plumage
Pluck a duck: Pink-eared Duck A bird of temporary saline or brackish inland lakes, the Pink-eared Duck has a bill fringed with fine lamellae that filter out microscopic organisms (crustaceans, molluscs, insects, algae and small seeds) from the water. The duck breeds when this food is abundant. The female nests in a hollow spout, on a log, or in the old nest of a coot or native-hen, usually over water. To line the nest, she plucks feather down from her body and buries her eggs in a mound of down when she leaves to feed. This habit is thought to keep the eggs warm in the case of ducks in cooler climates but it seems more likely that in this species it would stop the eggs from over-heating or drying out, and may make them less conspicuous to potential predators. By removing her breast feathers she also exposes the bare skin or brood patch, which becomes heavily vascularised to transmit heat readily to the eggs.
A Pink-eared Duck on the nest. (Artist: Trisha Wright) 83
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The secrets of cryptic chicks: shorebirds Feathers give clues to evolutionary origins but also to immediate environmental concerns. In the 1960s and ’70s the distinctive feather patterning of shorebird chicks was used in attempts to track the evolution of patterns and elucidate phylogenetic relationships. The chicks are nidifugous and precocial: they leave the nest after one to three days and feed themselves thereafter. Although the youngsters may stay with their parents, they are vulnerable to a raft of predators, both terrestrial and aerial. Yet, if the chicks remain still, they are often safe, going undetected by hungry eyes. To foil predators, they have evolved cryptic downy plumage, strikingly marked on the back with stripes, spots and stipples that match their often coastal nesting and feeding substrates of sand, seaweed and pebbles, or the inland equivalents. This is also known as disruptive colouration, because it breaks up the outline of the chick.
Black-fronted Dotterel
JACANIDAE
CHARADRIIDAE
Hooded Plover
Double-banded Plover
Red-capped Plover
ROSTRATULIDAE PEDIONOMIDAE GLAREOLIDAE
Comb-crested Jacana
Australian Painted Snipe
Plainswanderer
Australian Pratincole
Patterning of Australian shorebird chicks mapped onto a conservative summary of their relationships. 84
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These downy patterns can be placed on a scaffold provided by an evolutionary tree of shorebird relationships. That scaffold, or phylogeny, will have been derived from other traits such as DNA and skeletal anatomy. Suddenly, we see that natural selection has moulded camouflage from a different template or starting point in each of the major groups of shorebirds shown. It has successfully produced cryptic patterns in each group but each pattern nonetheless retains some signal of relationships within the different groups. Note, for example, how jacana and Painted Snipe nestlings resemble each other more than either does any other group. Similarly, the patterns within and between various dotterels, plovers and lapwing groups set them apart from all other groups.
Inland Dotterel
Red-kneed Dotterel
Masked Lapwing
Banded Lapwing
RECURVIROSTRIDAE BURHINIDAE
Banded Stilt
Red-necked Avocet
Beach Stone-curlew
(Artist: Jon Fjeldsä) 85
Bush Stone-curlew
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Something in the silhouette: various parrots and raptors Form reflects function and the flight feathers of birds are no exception. Among birds the variety of wing (and tail) shapes seems myriad and reflects a bird’s long-term evolutionary history as well as its presentday natural history. Species that live in open habitats tend to have relatively longer wings than species that inhabit woodlands. So, for instance, the woodland-dwelling Crimson Rosella (see below) has a shorter, rounder wing than the swift-flying Regent Parrot, which lives in more open situations. Bourke’s Parrot is somewhat intermediate. There is even variation within species: for example, a resident Peregrine Falcon (opposite), as in Australia, has broader, less tapered wings than a migratory subspecies of the falcon. Wing shape is often described by two measures: wing loading and aspect ratio: •
Wing loading is total body weight per unit wing area. A high wing loading indicates that the species is heavy for its wing size and either makes short flights and works relatively hard or must
(a)
fly swiftly to stay in the air; conversely, a light wing loading indicates a buoyant flier or a glider that can stay airborne relatively effortlessly. The Regent Parrot, Brown Goshawk and Wedgetailed Eagle have relatively light wing loadings (see opposite) and all have relatively long tails that also provide lift. Conversely, the Peregrine Falcon and Osprey have relatively heavy wing loadings and short tails. •
(b)
Aspect ratio is a comparison of wing length to breadth. Long, narrow wings have a high aspect ratio, which provides plenty of lift and little drag once the bird is airborne. Such wings work well at speed (Peregrine Falcon, Regent Parrot), in high winds, or for hovering species (Osprey). A low aspect ratio (Crimson Rosella and Brown Goshawk) provides good lift (without stalling) at take-off or low speeds.
(c) (a) Regent Parrot, (b) Bourke’s Parrot and (c) Crimson Rosella. (Artist: Trisha Wright) 86
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Birds with a heavy wing loading and/or a low aspect ratio must flap their wings frequently, whereas birds with a light wing loading and high aspect ratio tend to flap infrequently. Tail characteristics also relate to flight performance. For instance, broad tails provide lift and long narrow tails assist agility. So too does feather shape. Some species have some wing feathers that narrow suddenly. The narrowing creates slots that allow air to slip through the wing. For example, the greater slotting of the expanded wing of the Crimson Rosella allows the bird easily to rise steeply from the ground, whereas the less slotted wings of the Regent and Bourke’s Parrots perform better taking off in level flight from trees than from the ground. Other flight-related feather characteristics include firmer body feathers on fast fliers and looser feathers on more leisurely fliers. Natural selection can operate much faster than once believed. Darwin’s famous finches again provided the model, revealing that characters such as beak and body size can change rapidly, through natural selection, in response to changes in the food supply. In a similar vein, a recent study of the wing shapes of North American birds detected a shift in several songbird species towards a pointed wing shape more suited to life in open habitats than in forests. The results suggest that habitat change, in this case felling and fragmenting of forests, is driving evolutionary change.
(a)
(c)
(b)
(d)
(a) Peregrine Falcon, (b) Osprey, (c) Brown Goshawk, (d) Wedge-tailed Eagle (not to scale). (Artist: Trisha Wright) 87
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88
Getting around
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No-flap flight: albatrosses Albatrosses remain at sea except when breeding. They are highly adapted to gliding or soaring, minimising energy use when travelling great distances. The Wandering Albatross, for example, with the longest wings of all oceanic birds, has been tracked covering 9500 km over 30 days. A Southern Royal Albatross was tracked from Campbell Island and covered 13 000 km in two weeks; distances of up to 190 000 km in one year have been recorded. The albatrosses soar most frequently less than 20–30 m above the sea surface, where wind velocity gradients are greatest. Their vertically circular soaring flight pattern, which is looping when viewed head-on, allows long journeys to be made with reasonable speed and minimal energy expenditure. If a bird gliding close to the surface banks into the wind, it is forced up rapidly to 15–20 m above the waves. At this height, downwind progress requires only a simple turn, followed by a shallow glide. To progress upwind, the bird turns and dives steeply to gain speed, followed by a rapid turn to glide upwind close to the water where wind speed is least (approximately a metre above the water), until its airspeed drops off and it repeats the cycle. Albatrosses not only ride the prevailing wind, but use cyclonic and anticyclonic wind patterns associated with passing weather systems to search for food. In strong winds they use ‘dynamic soaring’, and can also ‘slope soar’ on the updraft created as a wave moves forward, forcing up the air ahead of it. But in the doldrums, albatrosses can’t fly so they settle on the ocean until the wind rises, rather than using flapping flight for extended periods. They also need wind to help them take off, easily becoming airborne at sea in windspeeds in excess of 27 km/hr. The high aspect ratio of albatrosses’ wings (very long and narrow) allows them to soar effortlessly under most conditions. Because they make limited use of flapping flight, they have been able to reduce flight muscle development, which lightens their load. However, there are trade-offs. To stay aloft, they must maintain fast gliding speeds, which means that they have sacrificed manoeuvrability and, consequently, must feed while bobbing on the sea surface rather than in flight.
Flight pattern of an albatross according to wind direction (arrow). (Artist: Nicholas Day) 90
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Water wings: Little Penguin Penguins are flightless, yet they fly through the water on small, stiff flippers, which are derived from ancestral wings. Unlike nearly all truly volant birds, they use muscular force on the upstroke as well as the downstroke. Together with the tail, their webbed feet serve as a rudder and a brake. Because the feet are set so well back on the body, the bird must waddle upright on land, a characteristic that makes the penguin so endearing. Their formal livery, so fetching on land, in the water renders them inconspicuous to potential predators and prey: from above their black backs blend with the ocean depths and from below their white bellies meld with the bright sky (see also page 112). To insulate them from the chilly ocean, penguins’ short, tight feathers cover their body almost completely. The feathers are not arranged in well-spaced tracts as in all other birds but are packed to a density approximately four times that of landbirds and totally exclude water. The Little Penguin, the only resident Australian penguin, is one of the smaller species. It occurs in more temperate waters compared with species that frequent Antarctic waters, where larger bodies are more advantageous for retaining heat. But small penguins are particularly vulnerable to predators, so each evening as dusk descends Little Penguins gather in large offshore rafts (safety in numbers) before splitting into smaller groups to make a beeline for the beach and into the safety of their burrows. By day, the Little Penguin hunts mainly small shoaling fish and squid by pursuit and diving, encircling shoals and plunging through them. It is capable of rapid turns and even though it looks neckless, it swims with its neck pulled in and extends it considerably to capture prey without turning the entire body. Indeed, the flexibility of its neck compensates for the rigidity of the spine. Little Penguins can swim on the surface but experience drag less when submerged. They have been measured travelling at a mean speed of 1.5 km/hr on short trips and 0.7 km/hr on long trips; swimming speeds that are at least as fast as those of their prey. Although typically they dive two metres or so, the greatest depth a Little Penguin is known to have achieved is 67 m in 90 seconds, which matches the theoretical limit for its one kilogram body size. Little Penguins work hard for their supper, swimming as much as 100 km/day to catch 250 grams of fish. In the breeding season they must catch nearly a kilogram within 12 km of the colony, on average making 500 dives during 18 hours at sea, 11 of them swimming actively. Little Penguin. (Artist: Trisha Wright) 91
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Going up, going down: Brown Treecreeper and Varied Sittella Treecreepers and sittellas are arboreal climbers that tend to traverse the trunks of trees in opposite directions: the treecreepers work from bottom to top; the sittellas spiral head first from top to bottom. Both have physical adaptations that allow them to forage over the vertical substrate. The six Australian species of treecreeper resemble their European namesakes, the creepers, and the Varied Sittella resembles the nuthatches. Nevertheless, the Australian birds are unrelated to their more northern counterparts, so their similarities are examples of convergent evolution. Tree-feeding treecreepers work their way vertically up the trunks and out along the branches of trees, before planing down in a glide to the base of the next tree. They climb briskly, with a shuffling gait, one foot ahead of the other. When climbing vertically, the axis of a treecreeper’s body is oriented parallel to that of the trunk, but its legs are held obliquely and widely separated, with the forward leg under tension and the back one compressed. During movement the lower foot is released and brought up to the level of the upper, then the upper foot is moved higher. This process has been described as ‘inching’ to distinguish it from the ‘hitching’ technique of the non-Australian creepers (the certhiids). At intervals the placement of the feet is changed so that the other foot leads. Occasionally, for short distances treecreepers hop downwards backwards, but they never assume the headdown vertical postures of the sittellas. Because one foot always grips the bark they can even climb upsidedown along the underside of limbs, making them the only birds in Australia to have access to this feeding niche. The treecreepers have strong legs, large feet and long claws for clinging to the tree. They do not use their tail as a prop as do many non-Australian climbing birds, such as the woodpeckers and certhiid creepers. Elements of treecreepers’ skeleton and musculature of the syrinx, jaws, femur and hind toe are unique. For example, they have a peculiar extensor system that allows greater rotation of the hallux (hind toe) than in most birds, and facilitates fine adjustments to irregularities on the substrate as they move. The other great Australian climbing birds are the various subspecies of Varied Sittella. They live in groups of five or more and feed mainly in the canopy, working their way downwards, then flying high into the next tree, constantly communicating by chittering. The birds zig-zag actively up and down the trunk and along branches with a rocking horse motion, probing and levering the bark with their upturned bills and occasionally flickering one wing, probably to flush cryptic prey. The Varied Sittella, like its northern ecological counterparts, the nuthatches, is a ‘reverse hopper’. It holds its body axis at an oblique angle to the trunk or branch, and its feet parallel and widely spread. When climbing the bird proceeds in a series of hops, both feet lifted simultaneously. Because its body is angled across the substrate, the bird spirals down the trunk or limb, although it can move up by reversing the body axis at each hop (zig-zagging).
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In contrast to treecreepers, the sittella’s feet show little structural modification for climbing. The toes and claws are relatively short, and the hind-toe is curved as in most perching birds, not somewhat straightened as is typical in climbers. The sittella’s tail, however, clearly aids climbing, keeping it out of the way as the bird rocks its way around the tree.
Varied Sittella (left) and Brown Treecreeper (right). (Artist: Ian Faulkner)
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The marathon runner: Emu Australians tend to take the Emu for granted but it is an extraordinary bird – giant, flightless and capable of sustained high-speed running. It is built like a marathoner, with puny forelimbs and mighty legs. Its legs are long and robust, armoured with heavy-duty but light scales, and its feet are modified from the usual four toes to three, all facing forward; the hind toe has been lost. Its leg muscles have evolved to provide great power during short bursts and endurance running. The largest muscle in the shank is uniquely equipped with four muscle bellies rather than the usual three. Perhaps not surprisingly, the relative muscle mass of the Emu’s legs is equivalent to that of the breast and wing muscles of flying birds: that is, the centre of greatest muscular power has been redistributed to its legs. The Emu is nomadic – although in Western Australia it shows a regular movement north in summer and south in winter – and may travel long distances to find plant and insect food. It is believed to use distant clouds and storm activity to guide it. Its marathoner’s legs enable it to cover these great distances at a fast, economical trot and, if necessary, sprint at 50 km/h for some distance. In many ways it is the avian equivalent of the hoofed mammals. Yet it is worth remembering that the Emu is the sole surviving species of a group that also occurred until recently on southern Australian offshore islands, such as Tasmania and King and Kangaroo Islands. Anatomical studies of the few remaining bones of these other species of Emu may reveal something of how they lived in their more forested environments.
Emu. (Artist: Trisha Wright) 94
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Swimming on land: Short-tailed Shearwater On the ground most procellariids shuffle along on their tarsi (legs). Walking is particularly awkward for the shearwaters, which have backwardly placed legs, adapted for swimming. They seldom walk except during courtship, and to shuffle from landing place to nest, when they hold their bodies low and thrust forward with their webbed feet. If necessary, they clamber clumsily over rocks and tree trunks to reach a nest or launching site, using the tail and bill to help them along. If they are in a hurry they raise themselves onto their toes and, with the help of beating wings, travel quite rapidly, half running and half flying. Because they come ashore in the evening, their poor mobility does not become a handicap unless they are out of their nest burrows after dawn, when they are likely to be killed by gulls or other avian predators. Hence, their evolutionary trade-off, between legs and feet that function well in water and those that operate well on land, works for them.
Short-tailed Shearwater. (Artist: Trisha Wright) 95
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A gripping tale: Purple Swamphen The Purple Swamphen lives on the margins of wetlands. Although it can swim, it prefers to walk, jerking its stubby tail up and down as it searches for young reeds to eat. The swamphen’s extraordinarily long toes – three forward and one backward-facing – help it walk over mud without sinking and support it by gripping ‘handfuls’ of reeds as it climbs through them. The swamphen feeds on young reed stems, herbs, seeds, fruit, insects, spiders, molluscs, frogs, snails, eggs and young ducklings. Most often it pulls up reeds, or bites them off at the base, grasping them with its huge foot as it eats the soft part of the stem. Despite appearances, its ungainly feet are as adept at grasping as those of parrots.
Purple Swamphen feeding. (Artist: Trisha Wright) 96
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What’s in a foot? stilts and avocet Recurvirostrids are large shorebirds with very long, slender bills and legs. Their feet are partially or fully webbed, and the hind toe, which is of little use on mud, is small or missing, as in the other shorebirds. The three Australian species all forage whilst wading in shallow wetlands. The Banded Stilt and Red-necked Avocet also bob for food, upending like ducks, but the Black-necked Stilt swims infrequently. In line with birds’ evolutionary quest to lighten their load for flight, the Black-winged Stilt, which has little need for flippers, has very little webbing between its toes. This and the pattern of scales suggests that the Banded Stilt and Rednecked Avocet, which are both Australian endemics, are more closely related to each other than to the Blackwinged Stilt, which is currently regarded as a cosmopolitan species.
(a)
(b)
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The feet of the (a) Red-necked Avocet, (b) Black-winged Stilt and (c) Banded Stilt. (Artist unknown) 97
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Furtive traveller: Buff-banded Rail The shy, secretive Buff-banded Rail is a typical rallid (rails, crakes and gallinules), with a strong, deliberate walking gait and a preference for running instead of flying. When it does take to the air, its flight appears laboured, with legs trailing and much rapid flapping. Yet the bird can travel long distances to short-lived ephemeral habitats, such as along drier parts of the coast and inland wetlands briefly inundated by rain or floodwaters. The rail’s capacity for dispersal by way of nocturnal flights has also allowed it to populate many remote oceanic islands, including Norfolk, Lord Howe and other Pacific islands, New Zealand, Cocos-Keeling (Indian Ocean) and from New Guinea to the Philippines. Given this mobility, it is hardly surprising that the Rallidae are among the most widespread of bird families, occurring on all continents outside the Arctic and Antarctic Circles. Although all appear to be feeble fliers, it is ironic that they have a particular facility for colonising remote islands. Indeed their weak flight may enhance the likelihood of wide, somewhat random dispersal because they may easily be blown off course and, once landed, be more inclined to stay. Once an island is colonised, speciation, often accompanied by the evolution of flightlessness, can occur rapidly. Flightless rails were once even more ubiquitous: over 1000 species are estimated to have evolved on islands by speciation from repeated colonisation events by flighted species, most to become extinct after the arrival of man in the last 2000 years.
Buff-banded Rail. (Artist: Trisha Wright) 98
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Migration and speciation: Australian and Oriental Pratincoles Only two of the 18 species of the family Glareolidae occur in Australia: the Australian and the Oriental Pratincoles. Both are insectivores that occupy a similar ecological niche: they favour open plains, shorelines of lakes and saltpans, mudflats and even airfields as feeding habitats, usually within two kilometres of open water, where they forage and drink, especially in hot weather. There are some differences. On the ground the Oriental Pratincole runs well, but its short legs do not allow great speed. The Australian Pratincole, on the other hand, is an exceptionally good runner, catching much of its invertebrate food on the ground, pursuing it on foot and preventing its escape at the last moment by flashing out a wing and swinging its body around to block the prey’s path – a method of capture unique in birds. Both pratincoles are strong graceful fliers whose long wings enable them to cover great distances. They are somewhat segregated geographically, never breeding together in the same area. The Australian Pratincole nests on gibber plains or open shorelines mainly in inland Australia and to a smaller extent in the north of the continent, usually from September to December or even January. Outside the breeding season it migrates to the more northern parts of Australia and to New Guinea and Indonesia, like all of the few AustraloPapuan migrants. The Oriental Pratincole, on the other hand, breeds in southern and eastern Asia, migrating southwards in its non-breeding season (October to May) to the Philippines, the Greater Sunda Islands and Australia, and occasionally beyond. How did these patterns of distribution and opposite routes of migration evolve? Migration is thought of as a current but not necessarily fixed end-point of an evolutionary process that results in the unhinging of breeding from non-breeding grounds. This can occur when conditions are favourable for a species only seasonally. Natural selection can drive this process as long as reproductive success is enhanced by migrating rather than staying put. It has been suggested that natural selection can also drive non-migration by enhancing survivorship over productivity. So, a balance of different evolutionary pathways among different species can result whereby some species become migratory and others stay put and maximise survivorship with, of course, enough reproduction for replacement. Speciation typically is thought to be driven by various isolating mechanisms, notably geographic isolation during past events such as sea level changes and changes in climate that bring habitat change. These mechanisms split an ancestral population into units that over time evolved into species with their own unique features. If there was ample, geographically scattered habitat, the ancestral species could diversify into several species, even adapting to new habitats. Nevertheless, migration can play a role: indeed migrants are probably finetuned by natural selection to be better than sedentary species at colonising new areas with suitable habitat, where there is potential to speciate. So, for a species to diversify, it probably helps to be highly mobile, like the pratincoles (and rails, see page 98).
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nonbreeding range of the Australian Pratincole breeding range
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nonbreeding range of the Oriental Pratincole breeding range
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A built-in broom: Chowchilla The three logrunners – the Chowchilla of the Wet Tropics and its close relatives the Australian Logrunner of eastern Australia and the New Guinean Logrunner – are part of an ancient Australo-Papuan lineage of passerines that have foraged on rainforest floors for millions of years. With their robust legs and feet, they make an unusual sideways sweeping motion to sift through leaf litter in search of invertebrate food. This distinctive foraging process is clearly audible and is often the first indication that a logrunner is nearby. Propped on one leg and its tail, the bird flings the litter away with a vigorous sideways sweeping arc of the other leg. After a while it changes legs and repeats the process. Despite the busy activity below, the bird’s head remains steady to watch for movement of prey. The spray of leaves and debris may rise above the bird itself. After clearing away the litter, it scratches from front to back to uncover its invertebrate prey and, still using its tail as a brace, briefly inspects the cleared area, feeds if food items are detected, then repeats the process. It may almost disappear from view as it gets lower and lower in the humus of the forest floor, before moving to a new patch, leaving a soup-bowl depression in its wake. Logrunners have evolved a unique structure of the pelvis, femur, and associated musculature that allows this strange motion, which often begins with the foot forward beneath the throat and extends through an arc of up to 90 degrees. Other adaptations that support this sweeping of the forest floor include a uniquely elongate outer toe comparable in length to the middle toe and a resilient, spine-tipped tail so that wear of the barbs as the birds constantly balance on the tail is not an issue.
Chowchilla. (Artist: Trisha Wright) 104
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Among ground-foraging birds worldwide, the most common methods of foraging among leaf-litter are backwards and forwards scratching with the feet or flicking with the bill. The rarity of adaptations that allow sideways sweeping motions of the feet suggests that they are in some way more difficult for evolution to bring together. Nonetheless, a few other birds are known with similar, if not as pronounced, pelvic structure – from Hawaii, the extinct honeycreeper Ciridops, and from New Zealand the Fernbird, Whitehead, Yellowhead and extinct wren Pachyplichas. However, it seems that logrunners are truly unique in the swivelling movement of their legs while foraging.
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Vice-like grip: Wedge-tailed Eagle The term raptor is derived from ‘rapere’ – to seize by force – which is exactly how most birds of prey make their living. A raptor’s style of hunting and its selection of prey are reflected in the form of the structures of its hind limb, as well as in its general form and its beak. Hence the short, robust tarsi (legs) and toes, and the long, robust claws of the Wedge-tailed Eagle reveal that it takes large prey on the ground. Its hind or killer talon is particularly sharp, robust and deeply curved. Despite appearances the eagle’s impressive beak is used to tear prey secured by the feet, not to kill. The eagle’s limbs must be short and thick to withstand the blow as it hits its large prey. The whole hind limb, including bones, muscles and tendons, must be powerful to subdue prey quickly, which is usually done by a rhythmic squeezing of the thorax. In eagles and other accipitrids (but not falcons, which kill by a swift bite to the spinal column or brain), it is usually this compression of the prey’s lungs and organs that kills. The eagle’s active grip is said to be over ten times more powerful than that of the human hand, even though the raptor weighs only three or four kilos. Its grip is assisted by a specialised ratchet mechanism of the tendons of the foot that locks the vice-like grip so that the bird can hold prey without muscular effort. This locking mechanism is also present in perching birds, enabling them to perch effortlessly for long periods, but is modified and more robust in both nocturnal and diurnal raptors, and it is particularly heavy-duty in eagles.
Wedge-tailed Eagle. (Artist: Trisha Wright) 106
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Tension and spin: Grey Phalarope Phalaropes and other wading birds (shorebirds) effortlessly transport small prey along their bill using the surface tension of water. The Grey Phalarope captures prey in a water droplet and then opens its jaws repeatedly with a tweezer-like motion so that the drop is drawn stepwise from the bill tip towards the mouth, taking the food with it. When the drop reaches the mouth the bird closes its jaws, shakes the water away and swallows the food item. This all happens fast: the bird can detect, seize, transport and swallow prey in less than half a second and glean food items at a rate of 180 pecks per minute. Experiments on the bill of a dead bird demonstrate that surface tension is sufficient to explain prey transport in phalaropes without the use of suction or tongue motions. Uniquely, when surface prey are scarce, phalaropes often hunt by spinning in tight circles to create an upwelling of water, which carries small invertebrates towards the surface where the bird can reach them. Individual phalaropes show a preference either for right or left-handed spinning. At sea, the phalaropes do not spin, but forage around eddies and currents which perform the same function. Phalaropes are the only vertebrates that forage by spinning. Their paddling legs drive the spinning and produce a flow below the surface that concentrates and draws prey upwards. Each one-second spin requires seven to eight kicks, with the bird’s lobed toes spread for thrust and folded for recovery. The bird leans inwards so that its bill is above the core of the vortex. It moves its head in discrete 45-degree snaps, separated by brief pauses, while its body circles continuously.
Grey Phalarope. (Artist: Trisha Wright) 107
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Stand-over merchants: Great Skua and Arctic Skua Five species of skuas (or jaeger) hunt over Australian waters but none breed there. All are persistent and powerful predators, swift and agile in flight, but also scavenge. The smaller, lighter jaegers are particularly fast and falcon-like in flight, with pointed wings and distinctively elongate central tail feathers. They frequently harry gulls and terns, forcing them to regurgitate or drop their meal. The Arctic Jaeger is especially singleminded and makes more of its living from kleptoparasitism (theft) than the other species. The larger skuas, such as the Great Skua, steal food from birds even larger than themselves, such as gannets and even albatrosses; they hurtle ferociously after the victim, silently twisting and tailing it closely, even tweaking its tail or wing. When not thieving or scavenging, they are formidable hunters – the raptors of the ocean. All the skuas are migratory. The southern subspecies of the Great Skua breeds on sub-Antarctic islands and visit Australia in winter. The Arctic Skua breeds throughout the Arctic and arrives offshore around Australia’s coasts in October–November staying until April. Hence, the two species do not often interact in Australian territory. When they do, the hefty Great Skua usually prevails – in fact it is one of the few predators of its feisty smaller cousin.
Great Skua pursuing an Arctic Skua. (Artist: Nicholas Day) 108
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Unsavoury habits: Black-faced Sheathbill Across most of its range the sheathbill is the only wholly terrestrial bird. Unlike all the other Antarctic birds, it does not have webbed or strongly taloned feet, so it cannot fish. Instead, it forages along the coastlines and intertidal zones of sub-Antarctic islands, surviving in the relatively barren environment by being highly adaptable. The sheathbill uses its robust beak to scrape algae off rocks, uproot vegetation in search of prey, and peck, probe and pull flesh off carcasses, which may be held down with the feet. A quarrelsome bird, several sheathbills will often squabble over scraps. Most of its food is gathered at penguin colonies and includes eggs and small chicks, carrion, ectoparasites, spilled food and excreta. Ever opportunistic, the sheathbill uses a unique method of kleptoparasitism, flying against penguins as they regurgitate to their chicks, causing them to spill food, which it snatches. It also eats the placentas of seals and picks at their wounds and sips milk from nursing seals. During winter, when few seabirds or seals are ashore, the sheathbill ekes out a living by eating kelp-fly larvae, molluscs, crustaceans and algae along the shoreline and spiders and insects from vegetated areas.
Black-faced Sheathbill about to steal food from a Rockhopper Penguin. (Artist: Trisha Wright) 109
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Burly burley seekers: albatrosses Most albatrosses have a varied diet of fish and krill, and floating dead or moribund cuttlefish and squid, among other carrion. The composition of the diet varies with location and season. Although albatrosses are opportunistic feeders and scavengers, they regularly attend predictable feeding grounds throughout the southern hemisphere, such as oceanic waters over prominent submarine ridges or at the edge of continental shelves, and coastal areas of upwelling where primary production attracts abundant prey. These rich offshore feeding areas, especially to the south and south-east of Tasmania and in the mid-Tasman sea, are also the targets for fisheries, and albatrosses have learned to keep an eye on the boats for discards and offal, burley used to attract fish and the baited hooks used by longline fishermen. In the frenzied feeding activity behind a fishing boat the larger species (Wandering, Royal and Shy Albatrosses) usually win contests against smaller albatross such as the Black-browed Albatross, but some smaller seabirds (e.g. Short-tailed Shearwater) compete successfully because they are nimble, or dive. There are also feeding hierarchies within species, according to age, with older birds prevailing.
In flight: Wandering Albatross (centre) and Short-tailed Shearwater (at right). On water: Shy Albatross (at left) and Wandering Albatross with wings extended; Black-browed Albatross with wings folded. (Artist: Nicholas Day) 110
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Longline fishing boats set fishing lines over 100 km long, each with thousands of baited hooks. The baits do not sink immediately, and albatrosses and other seabirds try to seize them. If a bird takes a bait it usually drowns, and many thousands are killed this way each year. Because albatrosses are long-lived and do not replace themselves rapidly, many populations cannot sustain these losses. Thus, the inclination to scavenge and to visit profitable fishing spots, behaviour that evolved over millions of years, threatens albatrosses’ existence because it brings them into conflict with humans in competition for the same resource. Changing fishing practices (e.g. night setting and use of bait-throwing machines so that bait sinks faster) has reduced some of this by-catch. The development and implementation of new equipment (e.g. underwater setting and hauling in of longlines) should reduce incidental seabird deaths even further.
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Variations on a theme: storm-petrels Storm-petrels are the smallest of seabirds, weighing 20 to 70 grams. They feed on the wing by plucking tiny animals such as crustaceans from the sea surface. This requires an almost incessant effort, day and night, over even the stormiest seas, to collect sufficient food. Southern hemisphere breeding storm-petrels have longer legs and shorter wings than their northern counterparts. This relates to their foraging and flight styles. Several of the southern species foot-patter on the ocean with their partially webbed feet, which may help them hold their position ever so slightly aloft above the sea surface, and attract or flush prey. Wilson’s Storm-Petrels often hover and patter with their feet while their wings are raised in a V; Leach’s Storm-Petrels patter, but rarely; moth-like Grey-backed Storm-Petrels leap from side to side pushing off the surface with their feet; whereas Black-bellied Storm-Petrels zig-zag low, smacking the water with their breast every few moments. All the storm-petrels are countershaded, darker dorsally than ventrally, which breaks up their outline and masks their presence from above and below (in part by reducing their shadow). This is common in marine animals like sharks and penguins, as well as some land animals, and is thought to make them harder for predators to see and/or allows them to approach prey undetected. A moment’s reflection suggests how impressive it has been that the evolutionary process has produced the same pattern in such unrelated animals for one very specific purpose. That in turn makes one realise the strength of the selective pressures operating in the marine environment to generate that pattern.
Wilson’s Storm-Petrel (at left), Black-bellied Storm-Petrel (centre below), Leach’s Storm-Petrel (centre top) and Grey-back Storm-Petrel (at right). (Artist: Nicholas Day) 112
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Interlude: Thinking about the oceans as environments – parallels with more familiar terrestrial habitats We have now seen that seabirds use their sense of smell to locate food. We have seen specialised foraging methods such as foot-pattering on the sea surface to disturb prey items. We have also seen adaptive plumage patterning, albeit simple and widespread among pelagic vertebrates, to aid in camouflage. Perhaps the bigger message here is that oceans are evolutionary landscapes just as are terrestrial environments. The intricacies of albatross and seabird biology, as they gradually emerge through some of the most remarkable research programs in ornithology, help us to see this. Have you ever looked across an extensive landscape such as a rainforest canopy, or a saltbush plain, and been tempted to think how homogeneous it is? Of course, when we take a closer look we quickly learn that the species of tree may vary, or there may be variation in underlying soils from one area to another, slight variation in topography, and so on. The marine environment is similarly far from homogeneous. There is the more obvious partitioning between continental shelf and deep water, pelagic areas, for example, but the presence of varying concentrations of dimethyl sulphide help us understand that the marine environment is broken up as surely as different species of tree are scattered across a rainforest. We now know that different albatross species forage in completely different parts of the ocean. This ecological partitioning parallels what we may be more familiar with in how closely related land birds and shorebirds partition their foraging environments. But the separation is not confined to the species level. Even the different sexes and age groups of albatrosses forage in different parts of the ocean. It has been shown from satellite tracking studies that older male albatrosses forage only in remote Antarctic waters whereas younger males never go so far south. Furthermore, the older birds travel greater distances but have less contact with the sea surface and return to land with elevated levels of the stress hormone, corticosterone, reflecting their lower foraging efficiency. Different sexes forage in widely differing parts of the oceans too and this has implications for our understanding of their evolution and their conservation. These different foraging patterns mean that the different sexes interact to differing degrees with longline fisheries. Males appear to be affected by them more often, but in one case, the Wandering Albatrosses of the Crozet Islands, the females experience higher mortality rates as they forage in areas where long-line fishing occurs. Regardless of which sex is suffering heaviest losses, any level of mortality of such long-lived, low reproductive-rate birds, due to long-line fishing must be of concern. It is pleasing to know that efforts to reduce this mortality have been having some success. Continued on page 114 113
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How and why have different sexes of one species evolved different patterns of foraging? Is it even evolutionary? In a comparative morphometric study of Black-browed and Grey-headed Albatrosses, considerable differences between the species and the sexes were found in wing area and wing loading. These corresponded, both within and between species, to broad-scale differences in habitat preferences relating to wind strength. At the time of year when they are breeding, the two species and the two sexes of each forage in different parts of the ocean. Clearly, this minimises any potential for competition for food at the time of year when it is most needed. This recalls the famous example of the extinct New Zealand Huia, in which the two sexes had different bill morphologies reflecting differences in how and where they foraged on trees. In the albatross example we see differences in morphology adapting the sexes to foraging in the different environments provided by different parts of the oceans. Such sexual segregation may also have implications for conservation in relation to sex-specific overlap with commercial fisheries.
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Feeling food: Straw-necked Ibis and Royal Spoonbill Modifications to the bill, legs and feet usually relate to a bird’s food catching and manipulation. In the illustration a young Straw-necked Ibis probes mud for dung beetles while a Royal Spoonbill dabbles in a pool. The two are close relatives, members of the Family Threskiornithidae, and often feed together. Both are bare faced, stately birds with long legs and feet adapted for wading or striding in search of animal food. They forage by walking forward through shallow water, mud or short vegetation, with the head and neck bent forward and downward, and the bill either poked at the substrate (ibises) or through it (spoonbills), diagnostic features that can be seen from a distance. Both species inhabit marine intertidal and inland areas, preferring standing or slow-flowing fresh water, marshes, floodlands and tidal flats. They eat a similar variety of invertebrates, especially insects and their larvae, molluscs and crustaceans, and small vertebrates, particularly fish, reptiles and amphibians. The ibis, however, will also feed in drier habitats and scavenge at garbage tips, sewage farms and in public areas such as parks and zoos. The two have lengthy bills. That of the ibis is sickle-shaped for probing, fossicking or seizing prey in water and on land. The spoonbill’s is flattened and wide-tipped. It is used to locate prey as the bird sweeps the open, submerged bill from side to side in an arc, creating swirls that flush prey from the mud and water. Whereas tactile detection of food by the wide, spatulate bill allows the spoonbill to feed both day and night, the ibis is strictly diurnal, probably finding food more by sight than touch. Even though similarities in habitat and prey might create competition between the two species, they have evolved enough differences to keep it minimal. From a common ancestor, the spoonbills and ibises (five species in Australia, 31 worldwide) have diversified to fill a range of slightly different niches offered by the relatively resource-rich habitats they occupy.
Straw-necked Ibis (at left) and Royal Spoonbill. (Artist: Trisha Wright)
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Striking stalker: Black-necked Stork The Black-necked Stork or Jabiru is Australia’s only stork. It occupies most types of wetlands, where it feeds by wading and probing in shallow waters for fish, crustaceans, amphibians, lizards, snakes and insects. In a distinctive hunched pose, the stork strides through the water, sweeping or probing methodically with its bill slightly open. The sensitive bill detects prey even in muddy conditions and the bird snaps it shut. The stork also runs excitedly after fish with wings raised and simply jabs. Speared fish are then manipulated so that they can be swallowed head first (see also page 251). The storks share many of these foraging behaviours with the ibises and herons, which are currently considered their closest relatives. The alternative view that storks may be closely related to the New World (American) vultures appears now to have been solidly rejected.
Black-necked Stork. (Artist: Trisha Wright) 116
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Multi-purpose snake charmer: Brown Falcon Compared with the Wedge-tailed Eagle, and most other falcons, the Brown Falcon has long legs and relatively short, thick toes. These come in handy when it stalks prey on the ground, or handles snakes. Try gripping a hose and you will quickly discover that stumpy fingers are an advantage. The Brown Falcon is the only falcon that takes snakes in any numbers. It sometimes fronts them, standing high on its long legs, with body feathers raised, making a fluffy target above the snake, occasionally leaping to a new position to try to grab the snake and immobilise its head. The falcon’s skull is relatively highly kinetic which may allow it the bill movement and flexibility to swallow snakes whole, at the expense of an extremely powerful bite (as in the Peregrine Falcon). The Brown Falcon is a generalist, taking anything from reptiles to invertebrates, birds and mammals. Individual pairs specialise, concentrating on whatever is most available in their territory, but readily switching prey type. The falcon hunts using a wide variety of techniques, including pursuit on the wing, but it mostly takes prey from the ground, either dropping on it from the air or running or walking across the ground and pouncing. It often hunts from a perch and can even hover, rather laboriously, where there are no convenient vantage points from which to look for prey. Brown Falcons will also gather in numbers to feed at fires, rodent plagues and termite irruptions.They will snatch insects from vegetation and scratch at litter to expose prey. They will even feed on carrion and their large eyes allow them to hunt at lower light intensities than most other Australian falcons, as well as by day. Altogether, a multi-purpose falcon.
Brown Falcon. (Artist: Trisha Wright) 117
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The twitchers: Spangled Drongo, Satin Flycatcher, Willie Wagtail and Magpie-lark What has been called the avian family Dicruridae includes a mix of large and small insectivorous birds, not immediately obviously related. Most have broad bills, well fringed by rictal bristles that help them capture insects and protect their eyes. Several are pied or black and all are bold, active birds, rarely motionless, inclined to skirmishing with neighbours, and not noted for their songs. Although all these birds prey on insects and spiders, each has a typical feeding strategy. Most often, they capture prey by direct pursuit in flight (the Drongo and fantails such as the Willie Wagtail), by gleaning from foliage and bark (most flycatchers) and/or from the ground (fantails and Magpie-lark). Drongos, fantails and monarchs are acrobatic fliers and make energetic, twisting sallies from a perch in pursuit of aerial insects. The Magpie-lark walks strongly, with a backward and forward movement of its head. Most of these species are chronic twitchers: they make jerky movements of the tail and wings while foraging. The Drongo shrugs it shoulders and flicks its tail before dashing erratically through the foliage. When perched, the flycatchers show a characteristic rapid tail-quivering, mostly vertically but sometimes sideways, and they raise their crown into an angled peak and dart from branch to branch. The fantails, as their name suggests, constantly fan or wag their tail and may flick open their wings suddenly; they also raise their crown to make good use of their eyebrows. The movements may help to startle insects (see also page 119). The Magpie-larks, however, seem to direct their twitches – flashing their wings and flicking their tail – solely at each other.
Clockwise from top left: Spangled Drongo in aerial pursuit; Satin Flycatcher gleaning; Willie Wagtail in flying pursuit; Magpie-lark foraging on the ground. (Artist: Nicholas Day) 118
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A wagging tale: Willie Wagtail The bold little Willie Wagtail is contrastingly coloured with almost entirely black upper parts and white underparts, and only a pair of white eyebrows break the pattern. The wagtail uses these brows to great effect, raising its crown to flare them when it is aroused in sexual interest, territorial defence or displays of dominance. When the bird is relaxed or submissive they form thin white lines. In immatures they are duller so that they send a milder signal. The brows are even recognised in the bird’s specific name leucophrys, derived from the Ancient Greek words for white eyebrows. The common name is also based on a characteristic trait of the Willie Wagtails and some other open country insect-eaters that wag their tail as they hop about feeding on insects. In fact, they jerk their bodies and the movement is exaggerated in their tails. Why do they incessantly wag? There are various possibilities: the Willie Wagtail may move its tail to help it balance as it darts about, to signal to other wagtails, or to flush hidden insects. The last possibility has been cleverly demonstrated to be so by observing foraging wagtails in bright sunshine and shade. In sunlight, the moving tail throws a shadow obvious to insects, whereas on an overcast day, or in the shade, no shadow is cast. If the tail is wagged to startle insects, it should be more effective and therefore wagged less often in bright sunlight. Indeed in sunlight, the wagtail wags about 10 times a minute, but under dull conditions it doubles the number of wags. It remains unknown whether their rate of tail-wagging is directly correlated with the probability of flushing insects and, perhaps most importantly from ecological and evolutionary viewpoints, with prey-capture rates. There are other evolutionary twists to the Willie Wagtail’s story. Its leg bones are longer and its pelvis slightly longer and narrower than other Australian fantails. These traits too are almost certainly correlated with its terrestrial foraging habits. A phylogenetic study based on DNA sequences found that its closest relatives are three species that occur outside Australia – Rhipidura javanica, R. aureola and R. albicollis. All have been recorded foraging on or close to the ground but the uniqueness and function of wagging behaviour among the fantail group has not been studied.
Willie Wagtail. (Artist: Trisha Wright) 119
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Futhermore, just to render the evolutionary picture of Willie Wagtails incomplete, we do not know why they call so fulsomely on warm, summer nights. Summertime is their breeding season, but why would they continue to call into the night, long after other day-active birds have gone to roost? A correlation between this nocturnal calling and bright lights, either the moon or artificial lights in urban environments, seems real enough although there are no data on the subject. Why do the birds advertise their presence to predators so prominently? Is there a trade-off and what is it? Do the Willie Wagtail’s close relatives call at night? Some of them are migratory and may call at night on migration. Is there an evolutionary connection there?
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Putting your best foot forward: Crimson Rosella A preference for one foot over the other in certain birds was first noticed in the 17th century. Parrots that use their feet to manipulate food are particularly dexterous, and often prefer to use one foot over the other. The favoured foot may be used to handle larger or complex food items – such as large insects and flowers, leaves bearing several lerps or galls, or multi-seeded fruits – and to raise them towards the bill. Less frequently, the foot is used to clamp or tether a food item and stabilise it on the ground or perch. Only a few parrots, including the Budgerigar and Ground Parrot, never seem to use their feet for feeding. Many parrots use the left foot more frequently, although the rosellas appear to be predominantly right-footed. A strong preference for one side or the other has been shown to improve parrots’ problem-solving performance; species showing strong footedness are quicker to find a solution to a foraging problem than those that are ambidextrous (use either foot without a preference). Individual parrots that show a strong preference for one foot over the other have also been demonstrated to perform better at foraging tasks. Cerebral lateralisation is common in vertebrates and insects. This brain asymmetry, in which one hemisphere specialises in certain tasks (such as handedness in humans, footedness in birds, and speech), is the subject of much debate, but is thought to enhance performance and facilitate multi-tasking.
Crimson Rosella. (Artist: Trisha Wright) 124
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The big-billed, picky eater: Glossy Black-Cockatoo A cockatoo perches in a casuarina holding a cone in its left foot. This simple observation is the current end point of evolution in the birds’ morphology and behaviour as well as the still incompletely understood evolution of the interaction between the birds and their food plants, the casuarinas. Black-cockatoos show variation in bill morphology to rival anything that Darwin’s finches have evolved. Not only is there variation between the species but also within the species. The Glossy Black-Cockatoo’s broad bill is ideally suited to the systematic method with which they extract seeds from casuarina cones. The other black-cockatoos also have bills matched, in size and shape, to their main food. Of all the black-cockatoos bills, the Glossy Black-Cockatoo’s takes the prize for the largest proportionally. Glossy Black-Cockatoos prefer to feed from the seeds of mature casuarina trees, but very occasionally eat the seeds of eucalypts, angophoras, acacias and hakeas, and insect larvae. A layer of cracked cones and fragments accumulates under favoured food trees, offering a clue to the cockatoo’s preferences. How the birds select trees for their prolonged bouts of feeding – at least 88% of their day – is linked to the extent of the crop of cones on the trees and their quality: cones produced the previous year are preferred because they have the highest nutrient content. Birds check the cones for quality before settling in a tree to feed and younger birds appear to learn the whereabouts of productive trees from more experienced members of the flock. As the birds are effectively seed predators, the patchiness of suitable trees may well be an evolutionary response from the trees to such efficient seed predators dining out on them daily!
Glossy Black-Cockatoo. (Artist: Trisha Wright) 125
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Choosing carefully: Peregrine Falcon and Galah The Peregrine Falcon is justifiably renowned for the ferocious speed of its stoop, or dive, which has been clocked at as much as 160–440 km per hour (even its level flying speed is an impressive 80 km per hour or more), depending on starting height and wind speed as well as the posture of the bird. It hits its prey with tremendous force. For relatively large, dangerous prey such as the Galah it is important that the falcon stuns or kills it outright, rather than risk losing a toe from the Galah’s powerful bite. The Galah also has other defences. It is typically in a flock, which would make the peregrine likely to be spotted early in its attack, and flocks have a number of aerial strategies to avoid predators, such as tightly wheeling in formation or trying to out climb the attacker. The falcon, on the other hand, can survey flocks to identify any weaker members to target, using such tactics as diving below the flock and swinging up to split it. The falcon may use the element of surprise – for example, attacking with the sun behind it; waiting at height to ambush a flock seen coming from a distance as it rounds a blind bend; or attacking from a concealed perch. The members of a peregrine pair will also hunt cooperatively, one splitting the flock while the other follows up from behind. The peregrine is an aerial hunter that specialises on flocking species such as parrots, pigeons and starlings, although occasionally it will tackle lone birds, and other aerial and non-aerial prey such as bats, rabbits and insects. As with most things in nature, overall the falcon makes a trade-off, in this case between size and
Peregrine Falcon in pursuit of a Galah. (Artist: Trisha Wright) 126
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difficulty, or reward and risk. Some small prey may be easier to catch but provide a small meal, whereas some larger prey will be harder to kill and present greater risk of injury but provide a generous meal. The Peregrine Falcon is a silent hunter but may use auditory cues to locate its prey and decide whether it is vulnerable or not. Another falcon, the Merlin, has been shown to use the singing powers of its prey to judge whether pursuit is likely to be worthwhile. If its prey sings robustly and competently, it is probably very fit and not worth the effort of the chase.
Interlude: The evolutionary equilibrium of predators and prey Evolution has clearly moulded predators for the physical ways in which they hunt, whether their morphology is suited for high-speed surprise attacks or searching by soaring, for example. But if the predators have to trade-off the ease of catching prey with the energetic costs and benefits of doing so, prey species must also make trade-offs. They must be conspicuous enough to go about their biological business of communicating with their conspecifics and attracting mates and so on, but not be so obvious that they are picked off by the first passing raptor. Natural selection is constantly shaping the lives of birds.
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Optimal foraging: oystercatchers The techniques that individual oystercatchers use to break open mollusc shells – from hammering to prising with their long, robust, chisel-shaped bill – vary greatly and are thought to be learned during the period when they are fed by their parents. Indeed, they are one of the few waders that feed their young, probably because they use such a difficult, specialised foraging technique that takes time to master. Oystercatchers are highly selective feeders, choosing prey and foraging sites that provide them with the greatest food intake per unit effort. Their sensitivity to the characteristics of their prey is fine-tuned. They prefer thinner shelled mussels and those less crusted with barnacles. They select mussels with lower moisture content by colour, so that they can ingest more during a feeding bout. In northern NSW they favour beaches where pipis are on average longest and at greatest density. With larger prey, such as mussels, they pick mediumsized shells until they are depleted, and then they take larger, thicker animals (more of a meal but more effort to open). Why do oystercatchers need to find and open prey so quickly and efficiently? It is thought that they maximise their relatively short opportunities for feeding when mussels are exposed (sometimes seasonally) and perhaps try to lessen the time that they themselves are exposed to predators and interference from other individual oystercatchers.
Pied Oystercatcher. (Artist: Trisha Wright) 128
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The two Australian oystercatchers eat similar prey but avoid competition by partitioning the coastal strip and largely sticking to their own particular foraging habitats. The Pied Oystercatcher prefers the soft substrates of mudflats, sandbanks and sandy ocean beaches and is less common along rocky or shingle coastlines. It hammers open bivalve molluscs, but it will also eat other invertebrates such as worms, crustaceans and insects. On rocky shores, the Sooty Oystercatcher prises apart limpets and mussels. During winter, it forages along the driftline of sandy beaches, eating small prey such as sandhoppers. Most overlap between the two oystercatchers occurs on estuarine mudflats.
Sooty Oystercatcher (at left) and Pied Oystercatcher. (Artist: Trisha Wright) 129
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Made to measure: shorebirds The Scolopacidae is a large family of shorebirds with longish, slender bills. Their necks and legs vary in length but are often long. Their plumages are mottled or patterned browns, greys and white, picking up more colourful reds and oranges in the breeding season. Just under 50 species spend the spring and summer in Australia and return to their breeding grounds in the northern hemisphere by the austral autumn. In Australia, shorebirds typically feed at low tide, each species specialised for a particular foraging niche or period. Nonetheless, their habitats range from tidal mudflats to beaches, reefs and freshwater bodies. Shorebird bills give clues to food and feeding strategies; they range from decurved through to recurved, straight to spatulate, and some species have a sensitive tip used when probing for food. Shorebirds employ two main feeding strategies. The first is a slow methodical walk with occasional probing into prey burrows, hunting blind, sometimes with the mouth open to increase the sensory surface, used by knots, godwits, sandpipers and curlews. The second is a more active run–stop–search, pausing to use visual cues and then pecking, as used by turnstones. Most species (e.g. godwits and Eastern Curlew) use a combination of both techniques to varying degrees. The straight-billed species tend to pick prey off the surface or make rapid thrusts into soft mud or sand – the firmer the substrate, the straighter the bill. Specialisations include that used by the turnstone, which actually turns over stones and debris, and the spinning of phalaropes (see also page 107). The larger-eyed species such as snipe forage and travel more by night than the others. Larger species such as the Eastern Curlew, the largest shorebird in the world, tend to catch larger prey and therefore do not have to spend as much of the day foraging as do smaller species. Smaller species such as Red-necked Stint and Curlew Sandpiper, however, must continue to feed during high tide, when they move to adjacent saltmarsh and claypan habitats. Shorebird flocks often include several species that distribute themselves across the tidal zone, from the drier portion, through mudflats to deepish water: each species tends to segregate in a zone where it can find food optimally. The species illustrated in the shorebird parade represent a range of sizes and shapes, all adapted to slightly different niches:
From left to right: Red-necked Stint; Curlew Sandpiper; Ruddy Turnstone; Terek Sandpiper; and Great Knot. (Artist: Mike Bamford) 132
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(1) The Red-necked Stint (very small) has a short straight bill that is very slightly swollen at the tip; it is an active hunter at low and high tides. (2) The Curlew Sandpiper has a long, tapering evenly down-curved bill; it forages on exposed intertidal mudflats and, less often, inland freshwater wetlands, often in deepish water. (3) The Ruddy Turnstone has a wedge-shaped bill and short legs; it frequents rocky coastlines, coral and sand islands and, less often, inter-tidal mudflats, scavenging by turning over debris. (4) The Terek Sandpiper has a long upcurved bill and is a very active forager in the seagrass beds of estuaries and bays and on inter-tidal mudflats fringed by mangroves. (5) The Great Knot has a slender bill, slightly downcurved towards the tip; it is a specialist hunter of bivalves on inter-tidal mudflats and, less so, on sandflats. (6) Latham’s Snipe (also known as Japanese Snipe) is a cryptic species with a long, straight bill; it forages in tussock grass and sedge surrounding freshwater wetlands. (7) The Bar-tailed Godwit has a long tapering, slightly upturned bill; it feeds mainly in shallow water on inter-tidal mudflats, sewage ponds and saline inland lakes, where it probes deep into the mud. (8) The Eastern Curlew has a disproportionately long, downcurved bill to reach deep into the burrows of worms and crustaceans; it forages across exposed seagrass beds or inter-tidal mudflats. The shorebirds are a textbook example of adaptive radiation. The evolution of a wide variety of shorebird types allows the group to share and exploit the prey-rich tidal zone and other similar habitats with minimal competition. Some shorebirds, such as oystercatchers, can even shift to feeding at night, when few other shorebirds are active.
From left to right: Latham’s Snipe; Bar-tailed Godwit; and Eastern Curlew. (Artist: Mike Bamford) 133
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The same but different: Australasian and Hoary-headed Grebes Grebes are highly specialised swimmers and divers that spend most of their lives in water, except when nesting. Their anatomical specialisations include bodies that are streamlined and nearly tail-less, and short, curved wings that hug their body contour. Their strongly compressed legs are situated posteriorly (the family name Podicipedidae means ‘rump foot’), and have separate, peculiar swimming lobes on each toe. There are three Australian species. The Australasian Grebe and Hoary-headed Grebe are quite similar in size. Both species are gregarious and often coexist, sometimes in large numbers. Both prefer shallow, softbottomed waterbodies, with plentiful submerged vegetation and aquatic arthropods and small fish, and forage more by searching than by pursuit. The third member of the trio, the Great Crested Grebe, is a larger, solitary hunter that actively pursues fish. On a landscape scale, the two prefer different habitats: the Australasian Grebe is often sedentary at permanent deep clear ponds, swamps and farm dams and tends to stay near cover; whereas the Hoary-headed Grebe is nomadic, seeking out larger, more open waterbodies and even turbid floodwaters. When they occur together it is often in open water where they hunt in different micro-habitats. At one study site, Lake Bathurst in NSW, the foraging habitats of the two species were almost entirely separate: the Australasian Grebe foraged in dense floating-leaf vegetation and along aquatic ecotones (where two habitat or vegetation types meet) and the Hoary-headed Grebe favoured areas one to two metres deep, where the weeds were fine-leaved and quite uniform, and they had easy access to the muddy bottom.
Australasian Grebe (at left) and Hoary-headed Grebe. (Artist: Jon Fjeldsä) 134
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As is typical in such situations, the two potentially competing species have evolved differences in feeding methods that minimise competition for prey resources. The Australasian Grebe is an unspecialised feeder, with a broad diet. One study showed that it dived during about 50% of hunting attempts, many of them brief, and gleaned invertebrates from foliage, from the bottom and the surface and by reaching up into overhanging branches, and pursued small fish. The Hoary-headed Grebe, in contrast, made repeated stationary dives (up and back in virtually the same place), to search for small, slow insect larvae and also macrozooplankton (e.g. water beetles and their larvae), which it picked from sediment and submerged foliage. Over 90% of foraging events were dives to explore small patches of bottom, where they pecked at the substrate and rarely pursued prey. The diet of the two species overlapped by 28% if prey type was considered but only 9% by prey weight, the Australasian Grebe taking considerably larger prey on average. Other differences between the two also affect their potential to compete. The Australasian Grebe is loosely social, whereas the Hoary-headed Grebe is highly gregarious – a habit that may facilitate capture of prey by flushing and the detection of concentrated prey in turbid water. The two even hunt at different times: the Australasian Grebe feeds mostly in the morning and evening twilight, and perhaps into the night, and the Hoary-headed forages more during the day. So, while the two species are superficially similar, close inspection reveals that, as a result of interspecific competition, they have evolved ways of reinforcing differences. ➂
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➆ Australasian Grebe
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Composition of the diet of two species of grebe at Lake Bathurst. (Artist: Jon Fjeldsä) 135
➀ Zooplankton ➁ Damselfly larvae ➂ Bugs ➃ Larvae of water beetle ➄ Water beetles ➅ Larvae of water moth ➆ Larvae of caddisfly ➇ Larvae of midge ➈ Midges ➉ Snails Fish Other items
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Different ways to make a living: Pacific Gull, South Polar Skua and Crested Tern The Laridae, terns, gulls and their relatives, provide a good example of a group of species that have radiated to fill a variety of different ecological niches. In this way the widespread group makes use of a number of coastal and oceanic zones and its members avoid competing with each other (see also page 132). Aside from skimmers and two species of gulls (none of which occur in the Australian region), most are active during the day. The illustration shows three representative species: a Pacific Gull dropping a mollusc; a determined-looking South Polar Skua arriving to see what can be pirated; and two Crested Terns, one hovering while it scans the ocean below for prey, the other having succeeded in catching a small fish. The gulls are opportunists and generalists that eat a wide variety of foods. Many scavenge and catch fish and invertebrates along the seashore. Some species of gull take advantage of human garbage or handouts. They have a wide variety of methods for obtaining food, including walking on the ground, searching in the water, and diving. They also drop molluscs and other hard-shelled animals from height to crack them open. The Pacific Gull generally avoids human habitation but is occasionally seen on rubbish tips not far inland. It forages along the coasts between the high-water mark and shallow water on sandy beaches. It drops turban shells and other molluscs, especially limpets and mussels, from height onto a rock in order to break the shells.
Pacific Gull, South Polar Skua and Crested Tern. (Artist: Nicholas Day) 136
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Terns are more specialised; they usually dive into the ocean for fish. Some species are plunge feeders whereas others feed from the surface, some feed inshore while others are pelagic. The Crested Tern is coastal and feeds mainly on small surface fish five to eight centimetres long. It hovers about five to 15 m above the sea surface, on rapidly beating wings with its bill pointing downwards, then plunges at angles of 60 to almost 90 degrees, with wings held in a steep V-shape before entering the water, rising again after a few seconds. It grabs the fish behind the head and swallows it headfirst. While the other larids are most often in flocks, the skuas are frequently solitary. They are coastal and oceanic and are the most aggressive and predatory species in the group, reflected in their unusual feet which are both sharply taloned and webbed. The South Polar Skua is an opportunistic scavenger and predator and also steals food from other birds. It takes a wide range of food, including eggs, young and adult seabirds, crustaceans, molluscs, fish and small mammals (rabbits and rats), carrion, garbage, seal milk, faeces and offal. Occasionally two skuas cooperate to hunt live prey. Despite this catholic approach to foraging, the skua often fishes for itself, revealing its commonality with the other larids by forming foraging flocks over schools of fish. Fishermen often look for these congregations to locate shoals of fish.
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Size matters: honeyeaters Closely related species that overlap in distribution usually show ecological separation by habitat. For example, among its close relatives, the Tawny-crowned Honeyeater tends to occupy low shrubby coastal heathlands; the White-cheeked Honeyeater and the New Holland Honeyeater occur in taller heaths, woodlands and forests with shrubby understoreys; the Crescent Honeyeater prefers wetter woodlands and forests; and the Whitefronted Honeyeater inhabits arid shrublands and mallee. Where species coexist, they often partition resources (plant-associated carbohydrates such as nectar and lerps) along a gradient. Larger honeyeaters tend to use the richest and most profitable patches and aggressively exclude smaller species if food is limiting. Smaller species require fewer resources and can live where food is scarce or available less of the time. Further partitioning of resources may also occur within a species. Males of most species are larger than females (with correspondingly higher energy needs), and dominant males usually monopolise the best available resources, often forcing subordinate females, juveniles and other males to use less profitable sources. The longer bills of males also allow them to take nectar that females cannot reach. Honeyeaters adjust their territory size to ensure that sufficient flowers are defended to meet the energy requirements of the individual or group: smaller territories are needed when the plants concerned have high floral density and high nectar production. For example, various species of Eucalyptus, Banksia, Grevillea and Eremophila have high floral densities and nectar production, and are often defended for weeks or months. These plants quickly replenish nectar and honeyeaters visit their individual flowers or inflorescences as frequently as 10 to 20 times per day. Conversely, plants such as Epacris, Correa and Adenanthos, which have low rates of nectar production and occur at low densities, are rarely defended. Typically, their flowers are visited by honeyeaters fewer than five times per day, and sometimes they are simply not worth the effort.
Tawny-crowned Honeyeater. (Artist: Martin Thompson) 138
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Playing with fire: Black Kite A northern Australian bushfire invariably attracts kites and other birds of prey. The smoke brings them from miles away. Large numbers of Black Kites circle on the thermals created above burning grasslands, keeping a sharp lookout for animals fleeing the flames. Reptiles, mammals, birds, insects and other invertebrates are all great tucker. So useful are fires to Black Kites that some individuals drop smouldering sticks to extend the fire. Their fire-lighting has been dismissed as unintentional, but there are too many accounts of both the Black Kite and the less gregarious Whistling Kite repeatedly carrying and dropping smoking sticks across tracks and other breaks ahead of fires to discount the behaviour so readily. Northern indigenous peoples have long held that the hawks are pyromaniacs. The kites are clever, opportunistic hunters and scavengers. They have a wide range of ways of garnering food. A Black Kite has even been observed to drop bread scraps into a river to attract fish to the surface (as do some gulls, herons and egrets). Hence, it is hardly surprising that they haunt the frequent northern fires – an easy way to feed a whole flock of kites. Nor is it a large behavioural step to learn to use sticks – firesticks – as a tool to spread fire.
Black Kite. (Artist: Trisha Wright) 142
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Stone tools: Black-breasted Buzzard Like its close relative the Square-tailed Kite, the Black-breasted Buzzard is a nest robber – it preys on nestlings and the eggs of ground-nesting birds. Although it also eats carrion and actively hunts, it can be regarded as an egg-eating specialist with associated unique behaviours. Since the shells of large, nutritious Emu eggs are too hard to break open by simply pecking, the buzzard uses rocks to assist. It searches the area surrounding its prize to find an appropriate smashing tool, usually an egg-shaped stone. Its aim is imperfect and it often takes several attempts to breach the shell. Interestingly, the forward jerking movement of the buzzard’s head when it is throwing a stone is very similar to the movement used when the bird simply pecks to break open an egg. How did the behaviour evolve – did buzzards originally throw eggs to crack them and then progress to throwing stones? The skill is innate, not learned. Young buzzards reared away from adults throw stones. However, they may need to recognise eggs as a rewarding source of food before they begin cracking them with rocks. The use of inanimate objects to achieve a goal is regarded as tool use: sticks or stones are most often employed. Like the Black-breasted Buzzard, the Egyptian Vulture also hurls stones at eggs, and some crows are even more ingenious, actually fashioning tools themselves to gain access to food. These species are far from each other’s closest relatives so the trait would appear to have arisen independently in each of them.
Black-breasted Buzzard and Emu egg. (Artist: Trisha Wright) 143
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Hammer and anvil user: Noisy Pitta Pittas are long-legged, stubby-tailed birds of the forest floor. Despite their electric colours, they are surprisingly hard to see amongst the busy foliage. They hop about singly or in pairs, upturning leaves and tossing litter aside with their stout, pointed bills and scratching and pecking at the soil like domestic hens. Like most of its family, the Noisy Pitta eats mainly snails and insects, but also woodlice, worms, spiders and other small animals and, occasionally, berries and fruit. Snails are held in the pitta’s beak and struck repeatedly against a stone or stump until the shell is broken. The bird holds the snail in its bill and batters it repeatedly against the anvil until all but the inner whorl is broken away, then extracts the rich flesh intact. Other small invertebrates are also often bashed, against a log, to soften them before swallowing. To protect the eye from shattered shell and other debris, the bird draws its nictitating membrane across the eye horizontally from the inner corner. This translucent third eyelid (see illustration) allows the hammering bird some visibility while protecting and moistening the eye. The anvil is often worn smooth from re-use and is surrounded by a midden of empty snail shells. These and the sound of hammering can be giveaways to the pitta’s presence. Still, the pitta is hardly quiet at other times, living up to its name by shouting ‘walk to work’ and rustling noisily through the litter.
Noisy Pitta. (Artist: Trisha Wright) 144
Using ‘tools’
The lumberjack: Yellow-tailed Black-Cockatoo To varying degrees all the black-cockatoos eat insects and their larvae. In eastern Australia, the wood-boring larvae of insects, notably of cossid moths and cerambycid beetles, are probably the staple diet of the Yellow-tailed BlackCockatoo, although it also feeds on seed capsules and very occasionally on fungi and slime mould. Generally, the Yellow-tailed Black-Cockatoo feeds in flocks, stripping the sapwood of eucalypts, acacias, casuarinas and grasstrees to expose larval tunnels. Its powerful bill is adapted for gouging out wood and extracting the grubs. Moving down the trunk tail first, using its bill and claws to cling and tail for balance, it searches the trees for frass holes, listening and testing them by biting, then using its long upper mandible to enlarge the opening if it seems promising. Birds in some populations have learned to strip a 2–3 cm chunk of bark from above the frass hole and use their weight to pull it out and down. When the hinged strip is at about 50 degrees just below the frass hole, they perch on it to achieve a better angle for prising open the larval gallery and extracting and eating the plump grub. The preparation of a ‘chopping board’, as was once used by lumberjacks, is time-consuming and takes young birds a long time to learn, but the reward is a sizeable, high-protein meal.
Yellow-tailed Black-Cockatoo. (Artist: Trisha Wright) 145
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The drummer: Palm Cockatoo Among cockatoos, the display of the Palm Cockatoo may be the most complex. Perched near the entrance to a tree hole, the male stands tall with wings outstretched, raises his crest and blushes. Blood rushes in to deepen his reddish cheek patches, which he reveals fully by moving his feathers. He exaggeratedly acts out the dropping of slivers of wood into the nest. But to really impress the object of his desire he has evolved an even more remarkable behaviour: he loudly stamps his feet and drums against a hollow branch or trunk with a sturdy piece of wood held in one foot. The female signals interest by displaying her cheek patches and blushing, or disinterest by keeping them covered. The whole process is accompanied by the male outstretching his wings, leaning forward and uttering a whistle – a most unexpected call for such a bird. Palm Cockatoos visit and maintain several nest holes in their territory; on Cape York Peninsula these are typically in woodland eucalypts, or, occasionally, a rainforest tree. Competition for large tree holes is fierce, although Palm Cockatoos use near-vertical chimneys, open to the sky, and construct a platform of splintered sticks to keep the eggs and nestlings above any flooding, whereas the other large cockatoos generally choose enclosed holes with a side opening and do not build up the floor.
Palm Cockatoo. (Artist: Trisha Wright) 146
Using ‘tools’
Whereas other cockatoos sometimes use tools to extract food, the Palm Cockatoo seems to use sticks only for percussion, most likely as a territorial message. Another possibility is that it is a sexual attractant – the sound issued may indicate to females the quality of the tree hole or that it is available. The drumming carries for some distance so it could indeed carry a message of ownership to neighbours or would-be usurpers. Interestingly, in New Guinea the Palm Cockatoos are not percussionists. Perhaps the dense forest there blankets the sound too much to make it worthwhile, competition for tree holes is less intense, or the drumming habit simply developed only in Australia.
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The bearded boaster: Australian Raven Many birds use calls or song to advertise their territory. The calls indicate that the territory is occupied and serve as a warning to intruders. One of the most distinctive sounds of the Australian bush is the territorial call of the Australian Raven, a loud wailing ‘aah-aah-aah-aaaaaahhh,’ drawn out and descending in tone. Pairs of Australian Ravens hold territories year round and typically advertise at dawn and anytime they need to assert ownership. They make the call from a prominent perch, assuming a stereotypic display posture with body held horizontal, head and neck stretched forward and bill open. They fan the hackles of their throat into a shaggy beard and may also depress their tail as they pump out each note. The territorial call may also be made in flight, accompanied by aggravated wing flicking. If the warning fails and a confrontation escalates (for example, between pairs at a boundary), the male and female alternate their calls in a frenzied, angry duet. However, being smart and sometimes social birds, ravens communicate using a sophisticated repertoire of calls and postures. They have an extensive vocabulary beyond the discordant territorial call, including a ‘song’: a medley of calls sometimes including vocal mimicry, usually made rather quietly. The two native crows and three ravens can be distinguished by their territorial calls, as well as by physical features such as hackles. The Australian Raven and Torresian Crow have been described as tenors, Little Raven and Little Crow as baritones and the Forest Raven as bass. They separate ecologically and geographically, but there are broad areas of overlap, and where two species co-exist their calls are said to become even less alike.
Australian Raven. (Artist: Peter Marsack) 150
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Group chorister: Australian Logrunner The stout-legged, robust-voiced Logrunner is a bird of the forest floor. Hidden in the dense undergrowth, it communicates using calls of extraordinary volume. Other members of the family also have strong, distinctive voices, including the Chowchilla with its deafening ‘chow, chowchilla’. The calls tend to be ventriloqual, appearing to originate from a different location to the caller – a foil to would-be predators. All year round, but more often in the breeding season, several neighbouring pairs gather at first light and perch facing each other on a vine, stone or log about 40 cm above the ground. With their heads held high, wings drooped and tail fanned, they sing forcefully with open bills: a loud, resonant, rapidly repeated ‘be-kweek-kweek-kweek-kweek’. Some birds continue the chorus while others chase each other, chattering excitedly, through the understorey. They may then rejoin the event, which continues for some 15 minutes before subsiding gradually. They are so engrossed in the performance that they can be approached closely. The function of this intense behaviour is unknown, but it may be some form of group defence and perhaps a chance to assess the competition or to compare potential mates (perhaps a form of lek?). Males make similar calls, with a downward inflection, as they face each other across their territorial boundary in the early morning or late afternoon; but in this situation the females do not join the vocal challenge.
Australian Logrunner. (Artist: Nicholas Day) 151
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A cracking duo: Eastern Whipbird Birdcalls are generally simple, short and stereotyped – such as alarm calls and contact calls to keep pairs and flocks together – used in particular situations. Bird songs, however, tend to be complex and learned, or partially so. The oscine passerines, or songbirds, have developed some extraordinarily complex songs and for some species evolution has favoured their development via the assistance of a partner. Instead of the male singing alone the female contributes a song component that is so seamlessly integrated with the male’s song that it sounds like a solo. The Eastern Whipbird is a consummate duetist. More often heard than seen, it hops along the ground and through understorey vegetation, foraging actively on the forest floor, probing and turning over leaf litter with its bill but apparently never with its feet. Every now and then the male sings and the female answers. This antiphonal duet is tightly coordinated: the male gives a long musical introduction followed by a penetrating crack to which female the responds with two or three sharp notes. The whipbirds’ duet is one of the most distinctive contributors to the dawn chorus. The humming effect of the male’s introduction, and the well-placed retorts from the female, emerge from the general clamour. Where whipbirds are abundant, their chorus is a highly musical affair: neighbouring pairs sing together, each in a different key. The sonogram opposite shows an example of a duet, which is so well coordinated that it sounds as if one bird produces it. The male whistle of 2.25 kHz lasts for about 1.5 seconds, followed by a whip crack rapidly rising from 1 to 5 kHz, made for 0.06 of a second; the song concludes with two sharp notes given by the female. Pairs sing together all year but there is a peak in the breeding season. Their duet has variously been suggested to function as cooperative defence of territory, to assist pair formation and pair-bond maintenance, and to be an acoustic form of mate-guarding. In reality it may serve several of these functions.
Eastern Whipbird. (Artist: Trisha Wright) 152
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Although their content and intent are difficult for researchers to untangle, the whipbird’s complex songs contain a wealth of information. It could be that males with a rich repertoire are more attractive to females: a wide range of song variations may be a good indicator of quality, revealing a male’s age, experience or ability. As well as advertisement of territory, the duets may also reveal to outsiders the strength of coalitions and tensions within the territory.
6– 5 kHz 4–
2–
–
20
25
}
–
1 kHz –
kHz
15
0.06 Seconds
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Heard but not seen: Rufous and Noisy Scrub-birds If ever a distribution pattern looked relictual, that of the scrub-birds is it. The two extant species occur on opposite sides of the continent: the Noisy Scrub-bird in a pocket of far south-western Western Australia and the Rufous Scrub-bird in a short strip of the central eastern Australian coast. Late Pleistocene fossils have been identified as scrub-birds from Pyramids Cave in eastern Victoria, further pointing to a much wider former distribution. Molecular and morphological evidence suggests that the scrub-birds are most closely related to the lyrebirds and that the group they form is closest to the treecreepers and bowerbirds. So intense has been the level of interest in the phylogenetic relationships of the scrub-birds that in 1985 an entire issue of the Records of the Australian Museum was devoted to a collection of papers reporting on a series of dissections and examinations of just one specimen of the Noisy Scrub-bird.
Rufous Scrub-bird. (Artist: Trisha Wright) 154
Communicating
The two contemporary species of scrub-bird live in thickets and tangled undergrowth and are seldom seen. They are spotted briefly running rodent-like across small openings in the dense vegetation. Strongly territorial, their most overt, distinctive feature is the loud, penetrating territorial call of the males. Scrub-bird pairs live together all year. The female incubates the eggs and raises the chicks unassisted. The male’s job is to maintain the territory. This he does by regularly singing and displaying, most intensely in the breeding season, from a low branch or on the ground. He raises his bill up and puffs out his chest, making his throat markings more obvious. He droops his wings, cocks and fans his tail, and vibrates his body, as do the lyrebirds and treecreepers. The male’s voice is astonishingly sharp and far-carrying. His song is a descending ‘cheep, cheep, cheep, cheep’ accelerating into an ear-splitting crescendo and is very occasionally enlivened by mimicry of a wide range of other bird species. The female is usually a silent partner, but occasionally sings with the male. The westernmost of the two scrub-birds, the Noisy Scrub-bird, long thought extinct, was rediscovered in 1961 at Two Peoples Bay near Albany in Western Australia. A proposed town site was cancelled and in 1966 the 4700 ha Two Peoples Bay Nature Reserve was created primarily for the scrub-bird’s conservation. The current management program for the species involves habitat management by exclusion of fire and translocations aimed at increasing the number of sub-populations as well as the total population size. A regular census of singing males is the only practical way to monitor the population.
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The song and dance man: Superb Lyrebird The male lyrebird is justifiably renowned for its splendid tail plumes, displayed to great effect at courts scattered across its large territory. He constructs and displays on earth mounds up to 10 cm high and a metre in diameter, energetically scraping together 20 or more (as many as 83 recorded) in a territory of 0.9 to 35 ha which overlaps with the smaller territories of up to six females. The Superb Lyrebird is polygamous and the males associate only briefly with females during the breeding season for courtship and copulation. Females may visit several males. When a male first encounters a visiting female he seduces her with subdued ‘whisper song’ before inducing her to follow him to a nearby mound. On the mound, he holds his tail feathers horizontally so that they drape over his back and spread to form a shimmering, white fan in front of his head. As he shivers his tail he jumps and circles rapidly. When the female approaches closely, he half closes his tail and vibrates it at her madly.
Superb Lyrebird. (Artist: Trisha Wright) 156
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This famous visual courtship display is accompanied by loud, protracted singing, for as much as half the day at the height of the breeding season. The content of the singing varies regionally (there are local dialects) and may include signals such as a territorial song, warning of a predator and the presence of an intruding conspecific. Up to 80% of song comprises a stream of extremely accurate mimicry, mainly of the calls and sounds produced by co-habiting bird species, including the chatters and wing-beats of parrot flocks, the antiphonal duets of kookaburras, magpies and whipbirds, and occasionally mammals, such as dogs, and inanimate objects, such as musical instruments. The mimicry can be learned entirely from the parent or neighbouring male lyrebirds rather than from the original songster, as evidenced by the long-term retention of mimicked calls of strictly mainland bird species among the introduced Tasmanian lyrebirds. This complex singing probably functions mainly to attract females, but may also be territorial proclamation to other males. Exactly why interspecific mimicry might attract females is unresolved. Possibly it is simply a way of achieving vocal complexity, driven by a preference among female lyrebirds for males with complex song and/or who are accurate mimics. If this is the case, it is likely that male vocal performance improves with age and condition, as well as ability, giving females a basis for mate choice. Lyrebirds have a mating system that is sometimes called an exploded lek. A typical lek is a site where multiple males of what are usually visually striking birds gather to spar with each other and competitively display en masse to females. In species such as the lyrebird, evolution seems to have driven a more dispersed, or exploded, lek. In this system individual males are not necessarily within sight of each other but they are certainly within earshot. (See also page 56.)
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Polygynous posers: Magnificent Riflebird, Trumpet Manucode and Victoria’s Riflebird All birds have courtships displays, some more modest than others. The displays of the birds of paradise are perhaps the most famous and extravagant, exuberantly combining costume, high drama and sound. Two of the three main lineages of birds of paradise are found in Australia: the manucodes, represented by the Trumpet Manucode, and the riflebirds, with three species. The remaining group, with the most elaborate plumages, is found in New Guinea. The Trumpet Manucodes are monogamous and the riflebirds are polygynous. The riflebirds have long been thought to provide textbook examples of sexual selection: female choice has driven males to evolve ever more flamboyant performances and plumage. If a male avoids being eaten by a predator and maintains his finery, he is likely to have good genes and be desirable to females. The best-dressed males mate with several females and father more offspring. The females, in the meantime, stay safely and cryptically coloured.
Left to right: Magnificent Riflebird; Trumpet Manucode; and Victoria’s Riflebird. (Artist: Nicholas Day) 158
Communicating
The male riflebird has spectacularly glossy black plumage, trimmed across the breast and on the head with iridescent blue and green, velvety on the head. The Magnificent Riflebird has elongate flank plumes. The male manucode, on the other hand, only needs to impress one female and differs from her only in having slightly more richly coloured black feathers. The displays of all birds of paradise are ritualised and have evolved to show off the plumage. Adult male riflebirds are solitary and territorial; during courtship they defend an area that includes display boughs. The Magnificent Riflebird selects high branches and Victoria’s Riflebird chooses stumps or horizontal limbs. At the arrival of a female, males perform an open-wing display. They make sudden, swinging side-to-side head and neck movements between raised wings that accentuate the iridescent breast shield and crown, sometimes accompanied by gaping to expose their coloured mouth lining. They fan and shimmer their wings to produce a loud sharp rustling sound and bob up and down or bounce along a branch. A displaying male may even ‘embrace’ a female between his wings. The manucode’s displays are less elaborate but have similar elements. The male fans his wings and throws back his head to show off his long, wild head plumes, shivers his feathers and lunges at the female. Male riflebirds need more experience than male manucodes to compete for females. It takes four or five years for a riflebird to become fully mature but less than two for the manucode, one indication that sexual selection is stronger in the riflebird.
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Signaling maturity: Black-faced Sheathbill Few of us are familiar with sheathbills – odd shorebirds, plump, dumpy and pigeon-like. There are just two species of sheathbill, both Antarctic in distribution, and one, the hardy Black-faced Sheathbill (sometimes known as the Lesser Sheathbill or Paddy), occurs on sub-Antarctic islands, including the Australian territories of Heard and McDonald Islands. Sheathbills are named for the horny covering across the top of the stout bills of the adults (the sheath). In the Black-faced Sheathbill, the sheath, bill and bare, wart-like wattles are purple-black, and contrast with the snowy white plumage. Between the ages of one and two years, the sheaths, caruncles and pink eye ring increase in size and complexity, signaling impending sexual maturity. Among non-breeding flocks of sheathbills, the importance of facial ornamentation is demonstrated in dominance hierarchies, based on age and bill size.
Black-faced Sheathbill: juvenile (at top) and adult. (Artist: Trisha Wright) 160
Communicating
Staking a claim: Black-faced Sheathbill Patrolling sub-Antarctic shorelines, the sturdy Black-faced Sheathbill stands its ground when confronted, using its facial ‘mask’ to great effect. In the breeding season, territory holders, principally the males, threaten same-species intruders by lowering their head, giving a strident ‘kek, kek, kek’ call and bill-wiping. They frequently chase the intruder, but serious fights are rare and most border disputes consist of ritualised beak jabbing and wiping.
Black-faced Sheathbill. (Artist: Trisha Wright) 161
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Boom and bust shorebird style: Banded Stilt A clutch of eggs sits exposed on the ground at the shore of a desert salt lake. Inside the egg is an evolutionary history that runs the gamut of arid zone ecology, influencing debates on subjects as diverse as phylogenetic history, migration biology and conservation of Australia’s waterways. The Banded Stilt, an Australian resident shorebird, breeds in hypersaline environments: inland terrestrial wetlands with more than twice the salt content of seawater (and sometimes highly acidic). A highly gregarious species, the stilt is famous for breeding in vast flocks, but only occasionally. Immediately after rain, when salinity and acidity levels change appropriately, a surge of prey ensues, and the stilts gather to nest in dense colonies, each nest a simple ‘scrape’ or slight depression made in the ground, eventually containing three to four eggs. During floods, nests with eggs may be raised as much as 50 cm by gathered debris, including corpses of dead birds that did not survive the boom. New nests are constructed in the centre of the breeding colony, where chicks have already left older nests. These central nests are less prone to predation, and may enhance the breeding success of the population, helping to make best use of an ephemeral flush of resources.
Banded Stilt. (Artist: Trisha Wright) 164
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In recent years the stilt has even bred on the Coorong of South Australia. The 2006 mass breeding at the Coorong, when high salinity and rain produced an abundance of brine shrimps, was the first coastal breeding record for the species. This tells us something of the remarkably high levels of salinity that the Coorong reached after a series of drought years and decades of overextraction of water. After breeding, the population disperses to wetter coastal areas of eastern and western Australia, to habitats such as salt marshes, saltworks and sewage farms. There may not be another major breeding event for years. The environmental controls and determinants of the stilt’s intermittent breeding events are not fully understood. What do we know about its breeding, if any, in intervening years? The nesting colonies experience high levels of predation by gulls and other predators. Natural selection, although often summarised by the maxim survival of the fittest can also alternatively and just as appropriately be summed up with nothing succeeds like excess. Here is a case in point. If predation is excessive, as it was in 1989 at Lake Torrens, the breeding event will largely fail. Individuals die but the population survives. If the breeding attempt is successful overall, the population expands many-fold. The similarity of the breeding biology of the Banded Stilt to that of flamingos projected the stilt into the centre of a stormy evolutionary debate. Also shared with flamingos was the presence of a muscle otherwise unknown in birds. On these grounds, in the 1980s, an evolutionary link between flamingos and shorebirds was suggested. The idea was not that Banded Stilts are small flamingos or that flamingos are big stilts, but that flamingos had evolved from an ancestor of stilt-like shorebirds. However, as the idea was explored it was realised that these similarities were just that – similarities. They had not been analysed in an appropriate context. What it comes down to is the meaning of the word ‘shared’ in relation to biological attributes such as the presence of an unusual leg muscle or breeding biology. There can indeed be a case for arguing a close relationship if two species share that trait because they inherited it from their most recent common ancestor. There is no case for arguing a close relationship, however, if they share it for either of the following two reasons. The first is that a trait evolved independently in the two very different evolutionary lineages. The second is that they inherited a trait from a much more distant ancestor. To illustrate, extreme examples of each possibility are: (1) parrots and hornbills share the habit of nesting in hollows but data suggest that the trait arose independently in these two groups, not that the they are particularly closely related; (2) Emus and thornbills both have feathers, but this does not suggest that they are closely related because feathers have been retained in all birds from a very distant ancestor. It is now accepted that Banded Stilts are stilts, and flamingos are most closely related to grebes! The surprising flamingo–grebe relationship is turning out to be one of the most strongly supported groupings in ornithology.
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Familiarity pays: Short-tailed Shearwater The Short-tailed Shearwater is one of the better-studied seabirds. It is a K-selected species: it is long-lived, with low fecundity, and inhabits relatively stable and predictable environments. It is at the opposite end of the spectrum to the boom and bust life cycles (often referred to as r-selected) of several typical inland Australian species such as the Banded Stilt and Budgerigar that have traded off the quality of their offspring for quantity. K-selected species form long-term pair bonds and invest carefully in just a few offspring, giving them a high likelihood of surviving to live a long life, as opposed to r-selected species which need to pump out as many young as they can when an opportunity presents itself in expectation that their likelihood of survival is low. The shearwater is capable of reproducing at five years of age, but most individuals do not breed until reaching seven years of age when they are experienced foragers. Established pairs mostly breed annually – at one colony only 10% of breeding pairs were absent on ‘sabbatical’ in any one year – and lay just one egg per year. Barring death, most pairs stay together and ‘divorce’ is most frequent amongst younger birds. The benefit of faithfulness and experience is increased reproductive success, which is greatest among long-term partners. The shearwaters are philopatric: when they are ready, young birds return to breed in their natal colony. As has been discovered for many bird species, only a small core of pairs is responsible for producing most of the young that survive to return to nest in the colony. Many birds produce no young during the whole of their lives. Although this may seem surprising, it means that only the fittest of birds are likely to contribute to future generations.
Short-tailed Shearwater. (Artist: Trisha Wright) 166
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Boom box territoriality: Emu Emus communicate by voice and gesture. Although both sexes can give the full range of calls, females grunt rarely and boom or drum frequently, whereas the reverse is true for the smaller sex, the males. The booming, drumming, and grunting can be heard up to 2 km away. The female courts the male and, as the breeding season approaches, she becomes more attractive. Her plumage darkens slightly and the small patches of bare skin below her eyes and near her bill turns brighter blue. She strides around confidently, puffing out her feathers, inflating her cervical air sac until it is almost touching the ground (see below), and making a low, monosyllabic drumming sound (see also page 54). Females compete vigorously for males. If the male is single, females may fight over him, kicking and chasing and calling intensely for some hours. If he is paired, they may challenge but the incumbent usually has a clear advantage. If a male is interested, he will stretch his neck, erect his feathers (below at right), then bend over and peck at the ground. Next, he sidles up to the female, swaying his body and neck from side to side, and rubbing his breast against his partner’s rump, usually without calling out. The female accepts by sitting down and raising her rump. The pair mates every day or two, and every second or third day the female lays an egg, until the nest contains an average of 11 (and as many as 20) large, thick-shelled, dark green eggs.
Emus. (Artist: Martin Thompson) 170
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Male–female dynamics: Great Crested Grebe Grebes are pugnacious in the courtship period: paired birds violently attack advertising birds of their own sex and keenly defend breeding territories. Courtship includes many elements of attack behaviour and varies from simple rituals in Hoary-headed and Australasian Grebes to complex sequences in the Great Crested Grebe. The sexes look alike, and most courtship displays are mutual (carried out by both sexes), but in some species even the roles are reversible, including ‘copulation’. Great Crested Grebes perform an elegant mutual courtship dance to establish the pair bond. Both partners perform head-wagging and reed-holding displays and other rituals. In the most common display the individuals in a pair face one another in the water. They make excited gurgling chattering sounds and raise the ruff of feathers about the throat and head. When the excitement reaches a higher pitch the pair rise almost vertically in the water, like a mirror image, breast to breast and bill to bill. They mate on a reed platform near their floating nest, which is usually well hidden amongst reeds. Although all birds have internal fertilisation, the males of most species, including the grebes, do not have a penis. Instead, the male’s cloaca everts and deposits sperm in the cloaca of the female. Some waterfowl and the large flightless birds are the only exceptions.
Great Crested Grebe. (Artist: Trisha Wright) 171
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Among some of the birds that are so equipped – ducks and geese – the length of the male phallus and elaboration in its shape (e.g. an anti-clockwise spiral) and the ‘vaginas’ of the females are evolving in a sort of arms race. Forced copulation is common and to counter it females have evolved structures, such as vaginas coiling in a clockwise direction and dead-end sacs, which prevent intromission without their cooperation. This provides a possible clue to why all mammals have a penis and so few birds. One possible explanation is that the penis may become important when males can force unwilling females to copulate. In most birds a penis would be unnecessary because males cannot grasp and copulate with unwilling females. Furthermore, losing the phallus may reduce the costs of flight.
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The scented powderpuff: Musk Duck Uniquely among waterfowl, the male Musk Duck has a leathery black flap or dewlap under its bill, which increases in size and in the strength of its musky odour in the breeding season. Normally, the male floats low in the water with his stiff little tail of 24 pointed feathers (most ducks have 18 or fewer), spread like a fan. But in display he transforms himself, cocking his tail forward over his back and spreading his under-tail feathers into a powderpuff. To complete the performance he raises his head and with bill-flap turgid, puffs out his cheeks, and rotates slowly in the water, sending jets of water sideways and backwards with his large feet, splashing and plonking and making as much noise as he can. He completes the performance with a sharp, far-carrying whistle. His aim is to attract females to his territory, from which he vigorously excludes other males. The male Musk Duck is three times heavier than the female, making it one of the most sexually dimorphic of bird species. Larger males, with larger lobes and which display most frequently seem to be preferred by females, hence they father the most young. The larger, more successful males also produce the most musk. The females raise the ducklings alone, even feeding them bill-to-bill.
Musk Duck (left and above). (Artist: Trisha Wright) 173
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A long engagement: Wandering Albatross Courtship is all about getting to know each other. Two or more birds use a series of gestures and responses to overcome aggression and hesitation, and to establish familiarity. In albatrosses, courtship is an intense affair that creates and later reinforces a life-long bond between a pair of birds. Wandering Albatrosses fly leisurely in line formation one behind the other over the nesting colony, interacting and calling, possibly to establish a male hierarchy. Sky-pointing is often the first obvious communication between a bird on the ground and another flying low over it. A courting male will stand on his ‘display’ nest, stretch his neck and bill skywards and call a quiet, penetrating gurgle to an approaching bird. This sky-call may be attractive to a mate-seeking female, but may be interpreted by a male, especially a non-breeder, as a territorial threat. An interested female will land near an eligible, sky-calling male, and initiate the courtship dance, which may be repeated several times. The dance includes touching bills, turning the head away, preening, calling, and circling or walking towards and away from each other. It climaxes in passionate sky-calls by both birds. Alternately, or occasionally in unison, each performs this spectacular dance; sometimes both birds climax simultaneously. After dancing, the birds may sit together and allopreen, or walk away from each other. Gatherings of five or more dancing birds are not uncommon. Onlookers are often forced away by aggressive snapping, although sometimes they may be allowed to participate in the dance. It takes newly widowed, experienced adults one or two seasons of these courtship activities to bond with a new partner, but young birds must watch, learn and practise courtship etiquette for many more seasons before they are successful in their quest. By then they have enough foraging experience to support a breeding attempt. Such careful lifetime commitment after a bird’s experience has been honed is a strategy that works well for long-lived birds like albatrosses.
A Wandering Albatross colony. (Artist: Nicholas Day) 174
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Breeding seasons’ greetings: Australasian Gannet Among the family Sulidae, the gannets and boobies, sky-pointing is a male advertising display in some species and a greeting in others. The commonality of the posture reflects the group’s ancestral connections but has been adopted for use in somewhat different social situations. Abbott’s Booby, perhaps closest to the ancestral sulid, is alone among living members of the family in that it does not sky-point at all. Whereas male boobies, with the exception of Abbott’s Booby, use sky-pointing to advertise territory, in the Australasian Gannet it is a greeting to the nest-attending bird on arrival or departure of its partner. The pair greet each other facing breast to breast, stretching their necks and bills skywards and gently fencing with their bills. Neither of the pair leaves until the other has stopped the ceremony, so the eggs or young chicks remain covered. The departing bird turns and performs an exaggerated waddle to display the strikingly outlined webs of its feet, with neck stretched vertically, eyes straining down and forward, before running or launching into flight. On return to the colony, alighting birds may also sky-point solo at the edge of the colony before bounding to the nest. Pair formation begins months before egg-laying, and long-term pairs reunite with excited courtship dances and displays. Males sometimes present females with gifts of a nest building material such as seaweed or feathers, and females may reciprocate.
Australasian Gannet. (Artist: Ian Faulkner) 175
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You are my Valentine: Christmas Island Frigatebird The oceanic frigatebirds are represented in Australia by three species: the Great and Lesser Frigatebirds and endemic Christmas Island Frigatebird (pictured). The adult males of all three have inflatable, heart-shaped, scarlet throat pouches that they put to spectacular use to woo females. At sea, frigatebirds are the pirates of the ocean, making a living stealing food from other seabirds (a behaviour known as kleptoparasitism). A favourite tactic is to soar over seabird nesting colonies and ambush birds returning from fishing trips. Frigatebirds’ flight is powerful and very agile, with speeds of about 100 km/hr and an ability to make stall-turns, which are used to great effect outmanoeuvring other frigatebirds, terrorising other seabirds so that they regurgitate food or drop nest material, and snatching chicks from nests and live prey and food scraps from the sea. However, at the nest frigatebirds are pictures of gentle domestic bliss. The males select and claim a nest site, where their advertising for a mate includes display flights and dramatic ballooning of their red throats, which not only make a dazzling visual display but also act as a resonator for their calls. The females select a mate and, if accepted, they snuggle together and the male continues his colourful courtship. The sac is the gular pouch that pelicans and their relatives have under their tongue, which holds food – it would have been a small evolutionary step for it to become adapted in frigatebirds for an additional purpose.
Christmas Island Frigatebird: male at left. (Artist: Trisha Wright) 176
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Do you think I’m sexy? Pied Cormorant During the breeding season the Pied Cormorant’s bare facial skin brightens, turning from pale yellow to bright orange-yellow between its eye and bill, reddish on the chin, and blue around the eye. The male selects a nest site and displays to attract females. He raises and lowers both wings together, with the primaries oddly tucked behind the secondaries, and the wingtips pointing up. Between wing-waves he raises his head in an arc – to point his open bill up and display his white chin with its red skin – then lowers it. When his head is back he depresses his tongue and enlarges his gular pouch (known as kink-throating) and may make a low guttural call often referred to as gargling. The display ends when a female lands beside him and the pair perform a greeting display, which includes kink-throating. With the ceremonials over, she guards the site while he sets about collecting nesting material.
Male Pied Cormorant. (Artist: Trisha Wright) 177
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Mutual attraction: Red-tailed Tropicbirds Tropicbirds intent on breeding display spectacularly over their cliffside or island nest sites. A pair or a group made up of several pairs hover with tails depressed and black webbed feet extended prominently, contrasting with their white bellies. They call raucously while one of the pair makes a shallow glide below and in front of its partner, who hovers by rotating the wings through a large circle while backpedalling the legs and feet. Then they change places. Perhaps most conspicuously of all, they twitch their tail from side to side to show-off the two ribbon-like central streamers, which reach impressive lengths, occasionally exceeding the length of an individual’s head and body. On reaching adulthood both male and female acquire long, red, stiff streamers as their badge of maturity. Even though the other feathers are moulted outside the breeding season, the streamers are replaced continuously so that a new one is always growing beside an old one. There has been much speculation about the function of such mutual ornamentation. More typically one sex is adorned, usually the male, which is clearly driven by sexual selection. Various theories have been tested for the tropicbird but none were supported. Streamer length and asymmetry are unrelated to age, body condition or various measures of reproductive success. Nor do the streamers appear to have any aerodynamic function, but given that the lengths of the tails of members of a pair are correlated, they might signal the social status of the pair.
Red-tailed Frigatebird. (Artist: Nicholas Day) 178
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The flap dancer: Black-necked Stork The ‘flap-dash’ display of the Black-necked Stork is performed on the feeding grounds, while walking or in shallow water. It is thought to strengthen the pair bond. One of the pair rushes through the water with wings outstretched, flapping its wings forcefully before stopping in front of its mate exposing the extensive white feathers of its underwing. This is presumably a ‘turn-on’ if you happen to be a stork.
Black-necked Stork. (Artist: Nick Day) 179
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The ballet dancer: Brolga Like all cranes, the Brolga has an exuberant ‘dance’ display that involves synchronised leaping, flapping, strutting, head swinging and bowing. The elegant dance is accompanied by wild bugling calls: pairs point their bills skyward to whoop and trumpet an antiphonal duet that ends in a cacophony. Occasionally, a dancer plucks a bunch of vegetation and hurls it in the air, sometimes catching it as it falls. The display is an important component of courtship. Sub-adults are the most avid dancers in their quest for a partner. Older birds retain their mates from year to year, perhaps feeling less need to dance. Although its primary purpose is to attract and keep a partner, the ritualised dance seems to serve a wider role in social bonding. Now and then elements of aggression are incorporated into the choreography, in defence of a breeding or feeding territory. The dance mood can spread contagiously through a flock, resulting in an impressive semi-synchronised mass display, perhaps more reminiscent of a modern dance company than a traditional ballet.
Aspects of the courtship display of the Brolga. (Artist: Nicholas Day) 180
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Brazenly barefaced: Royal Spoonbill The spoonbills’ face is devoid of feathers as in all members of their family, including the ibises, some of which have totally bald heads. This avoids getting their feathers dirty when foraging and opens an evolutionary pathway to a palette for bright facial skin colours that can be used to attract a mate. The Royal Spoonbill has an unusual, almost comical head, with a black bill and face set in a white-feathered head, and highlighted by two vivid yellow ‘eyebrow’ patches and a red streak across the top of the forehead. When breeding, the effect is further enhanced by the brightening of facial skin and the addition of a crest of long plumes and bib of pale yellow feathers. At the start of breeding, often following flood, the males usually claim a nest territory in the crown of a tree or dense vegetation, almost invariably over water, and frequently on small islands in marshes. A pair may nest solitarily but typically join colonies, which consist of loose associations of breeding ibises and spoonbills, occasionally in the company of herons, egrets, cormorants and a range of waterfowl. With the arrival of the females, spoonbill pairs perform courtship flights and displays at or near the nest that include raising and tossing their extravagant plumes and bowing to display the colours and patterns to full effect. They preen each other, rub their heads together and entwine their necks while grasping vegetation with their beaks and shaking their heads. The nests are large platforms of interwoven vegetation, usually of sticks and rushes, built largely by the female using material brought by the male, who presents the building material to her, with an accompanying performance of bowing, head tossing and grunting.
Royal Spoonbill. (Artist: Trisha Wright) 181
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Bow coo: pigeon courtship Most pigeons perform a number of types of displays during courtship, commonly bowing, puffing and strutting in front of a potential mate. Their aggressive display is similar. In sexual situations, the male faces the female of interest and quickly bows, lowering his head to point the bill down and cooing before lifting his head again. There are variations on this common pattern. For example, at the low point of the display, members of the genus Geophaps (e.g. Squatter Pigeon) bow the breast low, and spread the wings and tail; Macropygia (e.g. Brown Cuckoo-Dove) perform a simple sedate lowering of the head and breast bringing the body horizontal; Ptilinopus (e.g. Superb Fruit-Dove) puff up the neck, tuck the bill in tight and lean forward to show the crown patch; and Columba (e.g. White-headed Pigeon) lower the body but keep it angled. The cuckoo-doves and White-headed Pigeon, the most closely related of the four pigeons depicted, also perform courtship flights whereas the other two genera aren’t known to do so. In the aerial display the bird rises high with exaggeratedly beating wings and at the apex opens the wings and tail and glides back down. Especially in the days before the molecular genetics revolution, differences and similarities in such stereotypic behaviours were studied to help define phylogenetic relationships. Because displays are conservative, it is often the case that similarity in characters among species is due to common ancestry.
Squatter Pigeon (left) and White-headed Pigeon. (Artist: Trisha Wright) 182
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Fascination with the distinctive, highly ritualised displays of pigeons goes way back. Ethology, the study of the evolutionary and functional significance of behaviour, is generally considered to have originated in the 1800s with C.O. Whitman, who studied displays in pigeons. This reminds us that work from more than 100 years ago still influences modern research.
Superb Fruit-Dove (at top) and Brown Cuckoo-Dove. (Artist: Trisha Wright) 183
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True blue Lotharios: Variegated Fairy-wren A jaunty male Variegated Fairy-wren in full nuptial plumage carries a grub to feed to a nestling. His brilliant blue nuptial plumage acts as a signal to other fairy-wrens. As in other species of fairy-wren, males advertise and defend territories by perching prominently and singing (females and subordinate males often sing as well), and rivals engage in song battles. In more direct confrontations, males chase one another, flattening their body feathering and flaring their bright blue cheek patches. Physical fighting, however, is rare and retreating males puff out their backs, flaring patches of dorsal black and hiding their challenging blue plumage as an appeasement signal. Females find blue plumage attractive, which, of course, is the reason males find it threatening. In contrast to competitive interactions, courtship is quiet and unobtrusive, even furtive. In paired birds, courtship display leading to copulation may follow little else than a brief chase of the female by the male. Typically, males spend more time courting females other than their partner. Courting males, particularly those encroaching on to neighbouring territories, sometimes carry flower petals in their bills and execute prominent ‘sea-horse’ flights over shrubbery. The petals are often yellow, a spectrally complementary colour to the blue patches of plumage. Pre-dawn, males sing in the gloom and some paired females leave their territory to dally with the chosen male. Females apparently select males on the length of time they wear their ‘blues’ – the full nuptial plumage. Some brave males even wear blue all winter and these are the most successful breeders, siring many young by different females. Because their brilliant blues make them so visible to predators, their survival over the hardest time of year is apparently a better indication (i.e. a more honest signal) of their fitness than simply donning full blues in springtime. The blue story even applies across species. Crossspecies comparison shows that species with a greater area of blue plumage are those in which there is more cuckoldry. Thus, in populations of the brazenly blue Superb and Splendid Fairy-wrens as few as 20% of young are fathered by the attending males. In contrast, the Purple-crowned Fairy-wrens can be much more assured of their paternity, which averages over 95%. Nor do the faithful male Purple-crowned Fairy-wrens bother with flowers. (The extent of blue plumage is also associated with larger testes – useful to inseminate more females.) The Variegated Fairy-wren with an intermediate amount of blue plumage is predicted to fall somewhere between the two extremes but has yet to be studied.
Variegated Fairy-wren. (Artist: Trisha Wright) 184
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Playing hard to get: White-throated Treecreeper The White-throated Treecreeper has a more elaborate pre-copulation display than the other treecreepers. In the month leading up to egg-laying, the male gives crescendo calls for five minutes or more over several consecutive days from a selected site. Facing the female, he shivers his outstretched wings, raises his tail until it is almost vertical, and may rock his body from side to side. The female, in contrast, merely watches until he advances towards her. Males of all six species of treecreeper indulge in ‘courtship’ feeding of their females prior to nesting. The male trills as he arrives, often with a white-winged moth in his mouth. He approaches the female from below, displaying to her by raising his crown feathers and sometimes
drooping
and
shivering his wings. She may repeatedly reject his offering, even taking it and tossing it aside, but usually he persists. Once she accepts, he flies off. Although the feeding ceremony is part of the bonding process it serves the very practical purpose of fattening the female so that she has enough reserves to lay eggs. It can provide useful feedback: if the female is not sufficiently supported – if the male or territory are low quality, or the season is meagre – she will be unable to lay or will lay only a small clutch.
White-throated Treecreeper. (Artist: Nicholas Day) 185
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The importance of ritual: Red-browed Finch During the first stage of courtship, the males of several grassfinch species posture by holding a blade of grass or a feather, perhaps as a symbol of nesting. Each species has its own variations. For example, the Red-browed Finch has a particularly vigorous courtship dance and makes a symbolic show with a blade of grass nipped off and grasped at its base (see illustration) whereas the male Double-barred Finch skips the courtship dance and does not bother with a nesting token. When searching for a nest site, the male leads and indicates suitable localities to the female by performing a display and uttering special nesting calls. The female makes the final choice of site. The nest is a domed structure with a side entrance or tunnel. Green or dried grass is used and some species line the interior with softer plant material or feathers. The male chooses the nesting material, making a ritualised performance as he does so. He tests each piece of grass in his bill by chewing (opening and closing his bill around it). He sometimes manipulates the blade between his bill and foot. Most species use standing grass, which the male bites off at ground level and carries by the thick end to the nest, an unusual way of carrying nest material. After this show he gives the grass to the female, who actually builds the nest by herself.
Red-browed Finch. (Artist: Trisha Wright) 186
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Life in the monogamy fast track: Black-throated Finch Pair formation in the grassfinches appears to be low-key. A male begins with singing and low-intensity courtship directed at a number of females and even some males. In finch societies it seems that it can be of benefit for an individual to conceal its sex to avoid harassment from more dominant individuals, sometimes leading to misdirected courtship displays (the sexual indistinguishability hypothesis, which can apply in species in which males and females look alike). Once bonded, grassfinch pairs stay close and even outside the breeding season members of a pair maintain close proximity and synchronise their activities. The duo exchange frequent displays and greetings, including the characteristic, cheerful head-bobbing. Unlike many other supposedly monogamous birds, ‘divorce’ is rare and so too is extra-pair mating. This perpetual closeness is considered to be an adaptation to the finch’s opportunistic breeding: a readiness to breed quickly when rains induce good growth of grasses. The courtship display is very elaborate, stereotyped and three-staged, typified by the Black-throated Finch (see illustrated sequence): the initiation of courtship, which may include mandibulation (rapid opening and closing of the beak) by the male directed at the female, and (1) a long sequence in which both birds hop between two branches with heads and tails twisted towards one another; (2) immediately after the pair cease their hopping and the male performs his courtship dance; and (3) finally the female solicits copulation by a tail-quivering display. Recent research has identified an area of the brain that controls this behaviour and may even determine whether an individual functions as a stud or a dud.
Black-throated Finch. (Artist: Trisha Wright) 187
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Architects are smarter: bowerbirds Many bird species build an intricately constructed nest, and the males of some birds build or clear a courting ground (e.g. lyrebirds), but only among the bowerbirds do males construct an elaborately decorated structure to stage their wooing of females. The 20 species comprising the bowerbird family show a range of bower-building skills, from none to highly elaborate. The inclination to build is tied up with a suite of other traits including song and dance, mating strategy, territorial behaviour and brain size. The catbirds do not build a bower and are monogamous and defend an all-purpose territory. All the other species are polygynous and defend only their bower(s). These promiscuous males create a courting arena which, if successful, helps to win them several females. Their ‘bowers’ range from cleared ground courts, to mats of ferns or mosses, and highly decorated structures of sticks, grasses or orchid stems. The Tooth-billed Bowerbird is the only species that builds a stage without the opera house behind. It clears an area of forest floor of leaf litter and then decorates the bare earth with large, fresh green leaves, placed with their contrastingly paler undersides uppermost. This is thought to represent the ancestral condition, the first step towards bower building.
Court of the Tooth-billed Bowerbird. (Artist: Nicholas Day) 188
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Archbold’s Bowerbird of highland New Guinea is the only ‘mat’ builder. It accumulates a thick pad of fern fronds on the floor of upland moss forest beneath several low horizontal perches that it drapes with epiphytic orchid stems and other plants. The mat is decorated with snail shells, beetle wing cases (elytra), fruits, fungi, pieces of charcoal, tree exudate, and other choice items, including the unique head plumes of the King of Saxony Bird of Paradise. The Golden Bowerbird is Australia’s only maypole builder. It accumulates sticks into one or two conical towers, up to three metres high, beside or either side of a display perch. Finer sticks are placed neatly immediately either side of the perch and decorated with lichen, flowers and seedpods. The four other maypole-making species are New Guinean (Amblyornis spp.) and build more elaborate structures, some resembling small huts. The other actual bower builders make avenues of vertically placed sticks. Avenue bowers are built by Ptilonorhynchus, Chlamydera and Sericulus species: the basic form is two parallel walls of sticks and/or grasses placed upright into a foundation platform of the same materials. Modifications include the bower of the Fawnbreasted Bowerbird which has enlarged the foundation into a substantial high platform (see also page 192).
Mat of Archbold’s Bowerbird of New Guinea. (Artist: Nicholas Day) 189
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The males decorate in and around the true bowers with shells, leaves, flowers, stones, berries and manmade materials such as plastic, glass and metal items including nails, coins and rifle shells. The various species favour objects of a certain colour, shape, texture and size, which are often rare in the immediate environment: the Golden Bowerbird favours pale green lichen and delicate cream flowers; the Satin Bowerbird vibrant blue or yellow berries and shells; the Fawn-breasted Bowerbird uses green and white objects; and the Great Bowerbird likes grey and white with a dash of red. Males gather, inherit, or loot these precious decorations from neighbours and even destroy rivals’ bowers in the process. Decoration of avenue bowers even extends to painting of the interior walls. Males paint parts of the walls with a mixture of masticated plant matter, charcoal and saliva, leaving a dark-stained band. Females visit multiple bowers to inspect the structure, and sometimes taste the paint, often returning for a second evaluation. Males make a considerable investment in time and effort in bower construction, defence and maintenance. The Great Bowerbird, for example, with the largest avenue of all, up to a metre long, gathers 4000–5000 sticks and hundreds to thousands of decorations. As well as their attentiveness to the actual structure, males take care with bower placement. They site bowers strategically, according to the landscape, vegetation and ambient light. Some sites have been in use by males for more than 50 years (and are seemingly well known to local females), and some have even been suggested to be resistant to fire.
Avenue bower of the Regent Bowerbird. (Artist: Nicholas Day) 190
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With no child-rearing duties, male bowerbirds devote 80% of their day to bower construction and maintenance. If they get it right, the reward is likely to be enhanced breeding success. Thus, sexual selection has driven the evolution of these various complex behaviours and traits. From the local talent, a female will choose a male who is an accomplished builder and decorator (i.e. longer-lived, more experienced and perhaps more talented). Selection has also operated on another related trait: brain size. Among the various species, the more complex the bower, the larger the brain, especially in males, but also in females. Non-builders have the smallest brains of all.
Maypole bower of the Golden Bowerbird. (Artist: Nicholas Day) 191
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Why go to so much trouble? Great, Spotted and Fawn-breasted Bowerbirds Female bowerbirds usually arrive at a bower escorted by its owner. Once a female is at or within the bower, where mating mostly takes place, the male performs ritualised postures in front of her, on his court or stage, including presentation of his nape (see illustrations), sometimes with a bower decoration held in his bill and/ or dancing steps accompanied by vocalisations that often incorporate avian mimicry. A number of hypotheses have been proposed that attempt to explain the evolution of such complex bowerbuilding and associated behaviours, beyond their obvious role of enticement of females. The ‘transferral effect’ was popular for a time. It proposed that males with the less colourful, less ornamented (e.g. crested) plumages build the most elaborate bowers. The idea was that the colourfulness or showiness of the male is transferred to the bower (making him less vulnerable to predators). This holds in some groups, such as the grey bowerbirds (the Great, Spotted and Fawn-breasted Bowerbirds) in which a correlation between bower complexity and extent of colourful male plumage has been observed. Males adorned with a lilac nuchal crest (Spotted and Great Bowerbirds) build simple avenue bowers whilst males lacking a crest (Fawn-breasted Bowerbird; see illustrations) build complex ones. However, broader analysis suggests that this explanation does not apply universally. Among the more recent hypotheses is a proposition that the bower functions as protection from the unwanted or more frenzied attentions of the male. From the bower, the female can watch his display or be coy without feeling threatened. Alternatively, the male can position himself so that the female in the bower does not fully see his display
Males of Chlamydera bowerbirds in Australia at their respective avenue bowers performing the nape presentation display to a female within the bower. Great Bowerbird (above), Spotted Bowerbird (far right above) and Fawn-breasted Bowerbird (far right). (Artist: Nicholas Day) 192
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until he feels the moment is right. If the female is receptive she crouches in the bower and the male makes his way from his display area to enter the bower from the back and mount her. This gives her time to escape or change her mind. As for the colours (including those in the ultraviolet range) and items chosen for decoration, they are often rare in the local environment, and/or contrast with the bower and its surroundings, focusing the eye. Recent evidence suggests that the males carefully order the bower ornaments to create an optical illusion to fool females. It was noticed that the size and position of ornaments displayed on all of over 30 different Great Bowerbird courts had been ordered according to size. The further the objects were placed from the entrance to the bower, the larger they were, along a gently increasing gradient. From the female’s perspective this would probably make the male look large relative to the court and also make him stand out from the regular pattern of his stage.
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Look at me: Crimson Chat Chats nest during the cooler part of the year, usually after rain has stimulated a flush of vegetation and insects. Flocks break up and pair bonds and territories are established. Unusually among Australian passerines, male chats moult into brilliant nuptial plumage. For the duration of the breeding season, the black, red, orange or yellow plumage pigments of the head, throat and breast of the males are very bright. Males advertise breeding territories from the tops of bushes, posturing to display these vibrant hues and striking patterns on their head, throat, breast, rump and tail. In the Crimson Chat, for example, the male alights near the female and erects his scarlet crown feathers, exaggerating the area of red and highlighting his pale, blazing eyes. He also performs a display flight, swooping at the female with wings spread widely, flapping slowly and deliberately, with tail spread (illustrated at left). The intensity of melanin saturation of the plumage of male chats is related to increasing aridity of habitat, in accordance with Gloger’s Rule, a near-universal phenomenon referring to the common observation that within a species, the races or subspecies in warm and humid areas are apt to be more heavily pigmented than those in cool and dry areas. Eumelanins – dark brown to black – predominate in hot and humid regions, and, phaeomelanins – reddish to sandy colour – in arid regions, providing crypsis. An additional benefit may be the increased resistance of dark feathers to breakdown by humidity and bacteria. The chats range from the White-fronted Chat, with the deepest and most extensive amount of black plumage, through the Crimson Chat, Orange Chat and Yellow Chat to the desert-dwelling Gibberbird, with the least.
Crimson Chat. (Artist: Nicholas Day) 194
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196
Nests
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Designed by the same architect: robins Nests are a way of controlling the environment and making it safer for reproduction. It has been argued that the construction of a small nest, in a place of choice, was one of the factors that assisted the rapid radiation of the passerines in the Tertiary period (65 or 66 million to 1.6 or 1.8 million years ago). It has also been suggested that a small change – a change in behaviour using the same nest material, or the same behaviour using a novel nest material – is all that is necessary for the huge variety of nest types to have evolved. New technologies such as the adoption of mud and, in particular, spiders’ webs, with their high tensile strength, were taken up at some point in certain lineages with great success. The huge variety of nests (location, size, shape, colour, intricacy, materials) point to different selection pressures on their builders for successful nesting, including the protection of eggs and young from predators and the elements. Even the seemingly jumbled handful-of-twigs nests of some doves are constructed so that they do not fall apart with the birds’ comings and goings. Hence a nest’s materials and mode of construction can be explored for their utility as characters with evolutionary significance. Alternatively, nest characteristics can be mapped on to trees of relationships that have been constructed independently using other sources of data, just as other characteristics of birds such as plumage or voice can be so mapped. For example, the habit of building mud nests must have arisen twice in Australo-Papuan passerines. This is argued because the Australian Magpie-lark and New Guinean Torrent-lark are in one branch of the passerine tree whereas White-winged Choughs and Apostlebirds are each other’s closest relatives in another part of the tree altogether. So, two origins of the mud-nesting habit are necessary to explain the evolution of building nests of mud. The Australo-Papuan robins of the family Petroicidae all build small, cup-shaped nests.
Typical nests of the Eastern Yellow Robin (left) and Rose Robin. (Artist: Trisha Wright) 198
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Each genus of those robins, however, has its own characteristic cup disguised to blend with its surroundings. The nests range in size from the tiny neat nests of flycatchers to the larger relatively bulky nests of the White-browed Robin and scrub-robins. The Lemon-bellied Flycatcher builds the smallest nest of any Australian bird. Cup nests are constructed from an initial platform and shaped by tucking loose strands down into the cup. The female bird also presses into the nest with her breast and pushes back hard with each leg alternately, turning now and then to help compact the inside. As nest Hooded or Dusky Robins’ nest. (Artist: Trisha Wright)
building progresses, more soft lining is added, which is light and springy with good insulatory properties. The ability to build a particular type of nest is innate, but
individuals improve with experience. Scrub-robin (genus Drymodes) nests are unique in that they are built from fine grass, rootlets, twigs and bark in a shady hollow scraped into the ground, and surrounded by larger sticks or leaves heaped up to the rim to form a barricade and blend the nest with its surroundings. Most other Australian robins bind their nests with spiders’ webs and place their nests in forks of trees and shrubs, but Dusky and Hooded Robins (Melanodryas spp.), and also the Flame and Rose Robins (Petroica spp.), build nests in sheltered sites such as crevices and cavities. Robins that build in exposed situations decorate (or disguise) the nest on the outside with lichen, moss or bark. The Eastern Yellow Robin, for example, festoons its nest externally with lichen and hanging strips of bark. The Pink and Rose Robins build neat, exquisite nests decorated externally with a patchwork of moss and lichen.
Nests of the Lemon-bellied Flycatcher (left) and Southern or Northern Scrub-robins (above). (Artist: Trisha Wright) 199
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Topped and tailed: Yellow-bellied Sunbird The Yellow-bellied Sunbird, like other sunbirds outside Australia, constructs a beautiful hanging nest, loosely woven from small pieces of bark, plant fibre, grass and lichen, bound with spiders’ webs and further decorated with insects and caterpillar casings. The whole structure forms a spindle shape 30–60 cm long, suspended from a sapling, vine, low branch or building or other artificial structure such as a clothesline. The actual nest section is domed and more densely constructed, neatly lined with soft plant fibre and feathers, with an upper side entrance topped with an overhanging lip, and finished with a streamer-like tail. It has been suggested that the tail helps to keep the nest dry by channeling water like a chain. The hood over the nest entrance presumably performs a similar function. The female usually builds the nest and incubates the eggs, but both sexes feed the young on dismembered insects and spiders and nectar of flowers, particularly tubular species. As with many honeyeaters, the young receive the same diet as the adults but with the balance tipped towards the higher protein components (i.e. invertebrates) that promote growth.
Yellow-bellied Sunbird. (Artist: Trisha Wright) 200
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What nest? Spotted Quail-Thrush Nests built on the ground are particularly vulnerable to predation. The ground-dwelling Spotted Quail-Thrush builds a well-disguised nest in a hollow in the ground beside a sheltering rock, tree or tussock. The loose cup nest is usually finished with a platform of leaves at the entrance, which helps to blend it perfectly with its surroundings. Ground nesters are thought to have shorter nestling periods and more broods than birds that nest in more protected locations. The cost is greater loss of adults to predators. That is, there is a trade-off between fecundity and survival.
Spotted Quail-Thrush. (Artist: Trisha Wright) 201
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The fancy stitcher: Golden-headed Cisticola The Golden-headed Cisticola makes a beautifully woven, domed nest in rank grasses or reeds, less than 50 cm from the ground and with a large side entrance near the top. The birds gather green and dry grasses, reeds or broad-leaved herbs near the nest and weave them together with generous amounts of spiders’ web. Usually, one or more large green leaves are stitched around the outside of the nest, with web threaded through holes pecked around the outer edge of the leaf. These seem to anchor the plants to the nest, limiting distortion as the supporting plants grow. The cisticola is polygynous, with as many as 14 different females nesting within the territory of one male. The breeding season commences in early spring. Males hold small grassland territories which they vigorously defend until the following autumn. The males build courtship nests that are completed before egg-laying by the females. Once this courtship nest is completed the male plays no further part in reproductive activity. The female completes the nest by lining the cavity with fine grasses and then lays a clutch of three to five eggs that she incubates for about 16 days. She alone feeds the chicks for the 12 to 14 days that they are in the nest and for a few weeks after fledging. In the meantime the male has commenced building another courtship nest for his next mate. As with other polygamists, polygyny is thought to be possible because of the productive habitat occupied by the cisticola, where the males can hold a small territory that will sometimes support several nesting females and the females do not need assistance to raise a brood.
Golden-headed Cisticola. (Artist: Trisha Wright) 202
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An insect’s nest: Buff-breasted Paradise-Kingfisher Buff-breasted Paradise-Kingfishers migrate between New Guinea and Cape York Peninsula, breeding in the latter area. Their appearance in Australia to breed appears to bring together a suite of life-history attributes that have been attuned by selection. Records over many years show that they often arrive there after the first rains of the wet season, probably to take advantage of increases in the abundance of leaf litter invertebrates. At this time of year the termite mounds – into which they tunnel to form a nest – are soft and active. Buff-breasted Kingfishers always nest in terrestrial termite mounds. This behaviour may have arisen from competition with the Yellow-billed Kingfisher, which not only uses arboreal termitaria but also establishes its territories earlier as well. Returning birds almost always settle on the same territory with the same partner as the previous year. No nesting material is used, and the white eggs are laid on decayed wood dust or earth on the floor of the chamber.
Buff-breasted Paradise-Kingfisher. (Artist: Trisha Wright) 203
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The bottle-builder: Fairy Martin The Fairy Martin is the only Australian bird species to construct an enclosed bottle-shaped mud nest. The nests, built in colonies of dozens, are often fused together, and clustered on the walls or ceiling of a cave or overhung bank, in a cavernous tree, or under a large road culvert, bridge or the eaves of a building. Each mud-pot apartment is shaped like a swollen gourd with a drooping, narrower entrance spout. It is built by six or so birds, of both sexes: one inside receiving deliveries of mud and the others visiting a nearby source to scoop up a beakful, possibly the only time these birds ever stand on the ground. The nest is often finished with a lining of fine grass and feathers. The birds often return to these colonial nests each breeding season, but old nests can be taken over by bats, pardalotes, House Sparrows, Tree Martins, Zebra Finches and Budgerigars. For Fairy Martins the nest is the focus for courtship – the male advertises by calling from the nest. Copulation apparently takes place in the nest. Socially monogamous adult pairs defend their nest sites as well as the approach to the nest and both members of the pair help care for the eggs and young. Males are often promiscuous, however, and females sometimes lay in another bird’s nest (a behaviour known as egg dumping and a form of nest parasitism within a species). The intensity with which males guard their mates varies according to the risk of loss of paternity. Hence, the more closely synchronised the reproduction of members of the colony is, the more intensely the Fairy Martin. (Artist: Trisha Wright) 204
males guard.
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Bees and burrows: Rainbow Bee-eater Bee-eater nests are usually concealed on flat ground, gravel slopes, low banks, sides of ridges or ruts, and placed up to two metres above ground level. The female is the main excavator and often loses her tail wires, or racquets, in the process. Balancing on her wings and feet, she digs with her beak and transfers some of her weight to her bill while she pushes loose soil backwards with her feet and out the end of the burrow. She digs about seven or eight centimetres a day until the tunnel is about a metre long (between 40 cm to two metres and often curved) and finishes it with the nest chamber. The male contributes by feeding her insects. When the nest is completed, the female lays three to seven eggs and the pair shares incubation duties. After about 24 days the eggs hatch. For a while the nestlings are naked and blind and appear spiny from the retention of their feather sheaths, and they have ankle pads to facilitate their movement about the nest burrow. The young fledge after 30 days and in the meantime there is no nest sanitation. It is thought that because the nest tunnel is so narrow, and the birds’ bodies press so closely against the walls when they enter and exit, that their movements might act like a piston, sucking in fresh air and pushing out stale air. Some breeding pairs are assisted by one or more helpers, most often a son from a previous breeding season, who may help in all tasks from excavating to feeding the young. Bee-eaters have a real taste for bees and can eat several hundred a day, especially when they have hungry youngsters to feed, but they also take other winged insects such as locusts, hornets and wasps. They snatch insects from the air and carry them back to a perch to consume, first knocking their catch against the perch to subdue it. A little further probing of this habit suggests some fascinating aspects of evolution are waiting to be clarified by further work. Bee-eaters nearly always catch worker bees: the stinging sterile-female caste. The bird’s de-venomisation behaviour appears to be learned and involves a process of first incapacitating the bee by thumping the insect’s head against a perch. It then rubs the insect’s sting against the perch to rupture and inactivate it. During this step, the bee-eater holds its bill tightly shut and closes it eyes to avoid being squirted by the ruptured poison sac.
Rainbow Bee-eater. (Artist: Trisha Wright) 205
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Although there is some evidence that this so-called bee-rubbing behaviour is innate, it is clearly no guarantee that a young bee-eater will not experience a few stings. The birds quickly learn to avoid being stung, however. It has even been suggested that bee-eaters have evolved physiological immunity to stings, but this has not been tested rigorously. Certainly, some bee-eaters have been recorded to have survived several stings in quick succession or to have numerous stings in their oesophagus and stomach.
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Interlude: A cooperative migrant An adult Rainbow Bee-eater brings food to nestlings in a burrow. To reach this stage of its life cycle, the adult can be thought of as being at the end-point of a geographical corner of bee-eater evolution. To begin with, it is the only species in Australia of an otherwise mainly Afro-Asian group. Its very presence in Australia is of evolutionary interest. Then, as a member of the Australian avifauna, it has evolved to be one of the relatively few Australian species that undergo a temperate–tropical migration that is so prevalent elsewhere in the world such as the Americas. Furthermore, unusually, it combines migration and coloniality with cooperative breeding. That is, it nests in colonies, several pairs within a short distance of each other, and lives in flocks the rest of the year, and its breeding pairs are often assisted by one or more helpers. Yet, in general, cooperatively breeding bird species are much more likely to be resident than migratory. Remarkably, individual bee-eaters show great fidelity to their nesting areas, often returning to nest in burrows within tens of metres or less of their burrows from previous years. Before arrival at its nest burrow, the little bird has migrated into southern Australia from the north of the continent and beyond. Did its ancestors evolve in the area where it now breeds or elsewhere? What environmental factors have driven the evolution of its migration? How does it navigate? Why does it breed cooperatively?
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Hot-footed: Brown Booby Incubation in most birds involves transfer of heat from parent to egg through a highly vascularised and bareskinned brood patch. Boobies are an exception: they don’t have brood patches, but instead curl their large fleshy feet over the eggs to keep them warm. Just as most birds develop brood patches in the breeding season, the feet of incubating boobies become more vascularised, with an enhanced network of blood vessels circulating heat from the body through the foot, particularly in the females. Hence, booby feet are surrogate brood patches and function in the same way during incubation. Brown Boobies lay their eggs on the ground of cliff edges or small clearings on islands and the parents take turns to incubate them for about 42 days. In tropical regions overheating of the eggs (and chicks) can be a risk and the parents shade them with their body.
Brown Booby. (Artist: Trisha Wright) 210
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Saliva nests and egg-incubating chicks: Australian Swiftlet Australian Swiftlets nest in colonies of hundreds, their tightly packed, scoop-shaped bracket nests glued to the dark wall of a cave or overhang between boulders. The tiny, unlined nests are made from plant material and feathers cemented together with saliva. The edible nests of some Asian swiflets, famously used in bird’s nest soup, are built entirely of this gummy saliva. Both members of a pair help to build the nest and have a pair of lobed salivary glands beneath the tongue, which enlarge many-fold during nest building and come to fill the entire floor of the mouth. The glands produce gummy saliva, a glycoprotein that hardens on contact with air. The saliva is also used to consolidate food boluses carried in the parent’s throat to feed the chicks. The swiftlets feed their young about twice a day, but may take hours to regurgitate each gummy feed. Each pair lays one egg in the shallow cup. The incubation period is about 27 days and the chicks fledge at about 46 days in good seasons and 51 days in poor seasons – lengthy periods for such small birds but typical of swifts in general. Why do these birds have such long nestling periods? Is it genetic or a more physiologically plastic response to the environment? One hypothesis is that breeding in large colonies forced birds to forage further afield and hence to feed nestlings less frequently. This might be predicted to apply to many colonial birds, especially aerial insectivores. However, it has not been tested. A study of a New Guinean swiftlet suggested that low temperatures in its nesting caves may prolong the incubation and nestling periods. Clearly, this topic warrants closer study. Salivary glands of the Australian Swiftlet. (Artist: Trisha Wright) 211
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The slow-growing swiftlet chicks hatch naked and do not have a downy stage. The wing primaries emerge first, 16 to 24 days after hatching. The feet, however, develop relatively early, so that the chick can cling to the nest. Many still tumble to their deaths, providing a strong selection pressure that drives early maturation of the feet. After their first egg has hatched, Australian Swiftlet parents often lay a second egg (about 59 days after the first egg is laid), which the first chick incubates. The nestling even develops a brood patch. When the surrogate incubator fledges the parents resume incubation duties. No other bird species is known to use such a strategy.
Nests of Australian Swiftlet. (Artist: Trisha Wright) 212
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A bun in the oven: Malleefowl, Australian Brush-turkey and Orange-footed Scrubfowl Among birds, six main categories of parental care have been recognised: use of environmental heat to incubate eggs; brood parasitism; male-only care; female-only care (8% of species); biparental care and cooperative breeding (9%). The most common is biparental care by a male and female, which is characteristic of about 80% of the world’s species. Male-only care, brood parasitism and the use of thermal heat are the least common (each less than 1%). Thus, the megapodes, large-footed, ground-living fowl of Australasia, are unusual among birds in their use of environmental heat for incubation. The three Australian species – Malleefowl, Australian Brush-turkey, Orange-footed Scrubfowl – scrape vegetation into mounds and cover it with soil or sand. Microbes decompose the vegetation, releasing considerable heat. The female lays eggs singly over days or months in a hole made and refilled by the male. After about seven weeks of incubation the chicks have passed through the downy stage in the egg and hatch fully feathered. They dig to the surface unassisted, ready to run and soon to fly, and often never even see their parents. As a base to the mound, the southern, dry country Malleefowl digs a crater, whereas the other two species, the tropical scrubfowl and east coast brush-turkey, tend to build on a natural mound or slope, perhaps for drainage purposes.
Distributional ranges of the Malleefowl (spots), Orange-footed Scrubfowl (light hatching) and Australian Brush-turkey (diagonal stripes). (Artist: Wendy Arthur) 213
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The scrubfowl makes greatest use of heat from the sun. On Dunk Island it even lays its eggs in leaf-filled fissures among warm rocks. Where there is less natural heat, as in dense forest, they build a mound. Pairs or several birds may work on the same mound, which will have more vegetation in it where the environs are cooler. The largest mounds reach about 12 m in diameter and three metres high, but are usually smaller, and contain six to 12 eggs. The eggs are laid where the temperature is appropriate within the mound, but the scrubfowls do not manage the temperature of the mound. By contrast, the male Malleefowl and brush-turkey carefully regulate the temperature, humidity and aeration of the mound by opening it, turning it over or further covering it, and testing the heat by picking up material or probing. When the temperature is stable (about 33–35°C), they allow the female to lay. The brush-turkey’s mound, commonly about four metres across and one or two metres high, is mostly plant material, which ferments readily. The female lays 10–16 eggs over the winter. The Malleefowl has the most highly complex mound-tending routine to cope with the scanty dry litter and dry climate, under temperatures that fluctuate widely. Over the winter the solitary male excavates a shallow crater then fills it with litter swept from a radius of some 45 m. When it rains he covers his collection with sandy soil to a depth of 50 cm. He digs through the soil so that the female deposits her eggs close together in the most climatically stable part of the mound. She may lay over a long period from spring to autumn and produce up to 30 or so eggs depending on her nutritional status. The eggs begin incubation straight away so the chicks hatch over a long period. The male insists on tending the mound alone and in summer he must keep it from overheating. Thus, he spends much of the year minding the mound and protecting any eggs from predation. In evolutionary terms, the habit of using environmental heat to incubate eggs is of course not unique to birds. It is well-known in turtles and crocodilians. Most likely it evolved independently in birds given how few species use the technique and the diversity of processes involved.
From the top: Malleefowl; Australian Brush-turkey; and Orange-footed Scrubfowl. (Artist: Wendy Arthur) 214
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Is it a boy or girl? Australian Brush-turkey An Aboriginal elder told a researcher that more male Australian Brush-Turkeys emerge from mounds in cold nesting seasons, and more females in hot years. It was well accepted that incubation temperatures influence sex ratios in reptiles (known as temperature-dependent sex determination or TSD), but this had not previously been reported for birds. The researcher investigated, using brush-turkey mounds on the central coast of New South Wales, and did indeed find biases: at the ‘normal’ temperature of 34 degrees Celsius there were equal numbers of each sex, but at 31 degrees about two-thirds were male and at 36 degrees about two-thirds were female. Megapodes are similar to many reptiles in that they use environmental heat to incubate their eggs, but they differ in having heteromorphic sex chromosomes, which make TSD an unlikely mechanism in birds. Differential mortality of male and female eggs within the mound is the most likely explanation for the biases, although other explanations such as temperature-dependent sex reversal (which is yet to be demonstrated in birds) are possible. The finding raises the possibility that male megapodes, the keepers of the mound, can manipulate the sex ratio of their offspring by managing the temperature of the mound or the placement of eggs within it. It also raises several other questions. Is sex ratio altered according to prevailing environmental conditions – the smaller sex favoured in poor conditions, the larger sex predominating in times of plenty – as has been demonstrated for some other species?
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A head start in the arms race: Horsfield’s Bronze-Cuckoo Horsfield’s Bronze-Cuckoos are brood parasites that lay their eggs into the nests of small thornbills, fairy-wrens, robins and chats. The female cuckoo lurks nearby while the nest is being built and removes, and sometimes eats, an egg before replacing it with one of her own. After a two-day interval she may lay again in another nest that she has also had under observation. The female cuckoo may even lay a partly incubated egg (with a developing embryo). By initiating incubation through egg retention in her oviduct, she shortens the length of extrabody incubation and advances hatching by a day or two, which may give her chick an advantage over the host’s. However, the cuckoo’s incubation period is generally slightly shorter than that of the host’s eggs, so egg retention does not directly appear to be a strategy for brood parasitism. Instead it may happen simply because the female carries the egg in her oviduct while she searches for a suitable nest. Selection could still favour egg retention, however, if the net effect is a consistent reduction in the host’s incubation time. Cuckoos make the perfect subjects for studying the arms race between host and brood parasite. Over evolutionary time, cuckoos need to evolve better subterfuge continually while the hosts evolve to prevent or minimise the effects of cuckoo parasitism on their own breeding performance. It was once thought that host’s main line of defence was rejection of eggs and that if the cuckoo chick hatched it was raised. However, hosts do sometimes detect and reject chicks: Superb Fairy-wrens, for example, often abandon a lone chick and are even more likely to desert it if cuckoos are apparent in the area. The cuckoo chick counters by imitating the begging calls of an entire brood and the adult cuckoos counter heightened nest vigilance by minimising the time they spend in a particular area (to avoid being seen) and by targeting naive host pairs. 216
Horsfield’s Bronze-Cuckoo. (Artist: Nicolas Day)
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Helpless hatchlings: Major Mitchell’s Cockatoo Major Mitchell Cockatoos lay up to five eggs at intervals of two to three days, which hatch at similar intervals (i.e. asynchronously) after about 25 days of incubation. Hence, brood members may vary markedly in age and size. Like all cockatoos, the eggs are small and the chicks are relatively undeveloped at hatching. The hatchlings are blind because their eyelids are sealed shut until they begin to open at about 12 to 13 days of age. The chicks respond to the calls and sounds of their parents and reach upwards, blindly gaping automatically to be fed. At first they are heavy-headed, all beak, and their necks are weak, allowing them to feed only briefly before collapsing exhausted. Both parents feed them a regurgitated gruel of partly digested food – seeds, fruits, nuts and tubers from a wide variety of plants – gathered on the ground and in the canopy of trees and shrubs. The nestlings hatch in wispy, beige down. Their eyes have fully opened by 17 days, and the primary (wing) pin-feathers have emerged. Around three weeks of age rows of pink, sheathed quills cover the natal down (as in the illustration). By four weeks nestlings probably have a sufficient covering of feathers to regulate their own body temperature and no longer need to be brooded and the pin-feathers of their distinctive crest have begun to emerge. They fledge at about 57 days and their parents continue to feed and care for them for perhaps a further two to three months. Like many long-lived species, the cockatoos make a relatively small initial investment in each potential offspring: they put relatively little energy into egg production (i.e. they lay small eggs) and asynchronous hatching ensures that the weakest chicks die early if seasonal conditions are poor. The strong nestlings are most likely to survive and they are then given a long period of care and education.
Major Mitchell’s Cockatoo. (Artist: Trisha Wright) 217
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Coping with extremes: Australian Pratincole and Masked Lapwing From September to December, or any time following good rains, Australian Pratincoles return to their inland breeding grounds. They nest in loose colonies on gibber plains or claypans within about a kilometre of water. Despite the harsh conditions, they lay their eggs on the ground and generally avoid nesting near any vegetation or other sources of shade. How do they cope with soaring daytime temperatures and exposure to the sun while protecting their eggs and young? A few minutes of exposure to high temperatures (40 degrees Celsius or more) and solar radiation can destroy a clutch of eggs. In pratincoles, both parents incubate and care for the young and relieve each other at the nest every hour and a half or so. They appear to be able to maintain the temperature of their eggs below lethal levels during the heat of the day through a combination of biparental care, of 100% attentiveness, minimum exposure of eggs during changeover at the nest, and belly-soaking. Regulation of the body temperature of the incubating birds below damaging levels is more complex. Even after the young have hatched, although they lead them to a refuge under a nearby shrub or grass tuft, the adults themselves do not seek shade in hot weather. The incubating bird copes by: frequent changeovers with their mate at the nest, allowing the relieved bird to go and drink and stand in water; panting or gular fluttering to dissipate heat; raising the feathers of the crown and back to release heat or increase insulation from insolation; orientation on the nest with respect to the sun (back facing the sun to minimise heat gain) and wind (maximise convective cooling); sitting loosely; and belly-soaking.
Masked Lapwing. (Artist: Trisha Wright) 218
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As solar radiation and temperature increase so too do these protective behaviours. For example, as the bird heats up, it increases the intensity of its panting, opens its bill wider, salivates more copiously, and holds its wings a little away from the body. Wherever possible, off-duty birds often stand on raised objects (larger stones, cairns, graded ridges along roads) probably primarily for better visibility but with the added benefit of slightly cooler temperatures (in one case, the ground temperature was 45 degrees Celsius while just 20 cm up at the top of a cairn on which an offduty parent stood it was 4 degrees cooler). Belly-soaking is unique to some members of the Charadriiformes (pratincoles, sandgrouse, lapwings, plovers, terns and allies). When breeding in hot, dry conditions, they must drink regularly. After drinking they may wade into the shallows and perform strange rocking or bobbing actions to thoroughly soak their uniquely adapted, dense belly feathers (which hold more water than most feathers) before returning to the young or nest. Thus, belly-soaking may function in cooling the incubating bird exposed to intense solar radiation, cooling the eggs and chicks, and increasing nest humidity. Chicks even drink from the sodden breast which the adult puffs out to water them.
Australian Pratincole. (Artist: Trisha Wright) 219
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A crown of thorns or a larder? Crested Bellbirds Why do Crested Bellbirds ring their nests with hairy caterpillars? The bellbird places as many as 14 living caterpillars of various species in and on its nest, but especially around the rim. The birds nip the neck of the grub to immobilise it. Perhaps the caterpillars are gathered in times of plenty and ‘cached’ alive to provide fresh food for the parents and nestlings. An alternative explanation is that the bristly caterpillars provide a measure of protection to the nestlings. Nearly a century since this unique behaviour was first recorded its function is yet to be established: it may in fact serve both purposes.
Crested Bellbirds. (Artist: Trisha Wright) 220
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Taking them under his wing: Comb-crested Jacana Jacanas have enormously long-toed, long-clawed feet that spread their weight over a large area, allowing them to walk and run over floating waterplants without sinking. Hence, their alternative names are lotus-bird, lilytrotter and Jesus-bird. When they fly their spindly legs and feet dangle behind them like streamers. Australia’s Comb-crested Jacana is polyandrous – as are the other Jacana species elsewhere in the world – which is rare amongst birds. The female is larger and more aggressive and may mate with several males (up to three recorded). The male cares for the eggs and young, freeing the female to lay a clutch with another male. Polyandry seems to have evolved where resources are concentrated spatially, such as at the permanent wetlands jacanas favour and when the rate of breeding failure is typically high. Females lay as many clutches as possible to compensate. The male builds a nest on a mat of floating vegetation. If the vegetation starts to break up or predators threaten he may scoop up the eggs or chicks and carry them elsewhere tucked under his wings. Only the spidery limbs of the chicks give them away. At the heart of evolutionary understanding of this unusual mating system is the theory that increased investment in care of the offspring by one of the sexes involves a cost in terms of decreased availability of that sex for additional reproductive activity. That sex then becomes a ‘limiting resource’ and the other sex competes for access to them. Most commonly, it is female birds that invest that effort, but when it is males the opportunity arises for the mating system and the skewed sex ratio in jacanas to evolve. An intermediate step in the evolution of male care in the jacanas may be seen in the Wattled Jacana of Panama. Wattled Jacana females do not incubate eggs but they retain the ability to perform all aspects of chick care. They do this only under exceptionally rare circumstances when their mates are physically unable to perform these behaviours themselves, such as when they are taken by a predator. Also, these females have an important role in predator defence, responding to threats when alerted by the male. Hence, Wattled Jacanas benefit from a system that has flexibility – exclusively male care or biparental care, as required.
Comb-crested Jacana. (Artist: Trisha Wright) 221
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A parent’s love: Brolga A Brolga chick shelters under the warmth of its parent’s wing as the parent preens and keeps a watchful eye for predators. Brolgas have at most one brood a year, with one or two chicks. The chicks hatch in a coat of down and within hours of hatching can leave the nest to follow the parents on foot. By four to five weeks the youngsters are clothed in body feathers and at about three months they are fully feathered. They continue to solicit food from their parents but increasingly are capable of feeding themselves. They stay in the family group, often until the next time the parents begin to breed (i.e. when the fledglings are aged either about 11 months or nearly two years). The young mature at about two years but rarely breed successfully until they are older. The Brolga is a typical K-selected species, investing heavily in each individual offspring (see also pages 164 and 166).
Brolga. (Artist: Trisha Wright) 222
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Cream of the crop: Emerald Dove Like mammals, some birds have evolved physiological mechanisms to make special secretions to feed their young, but unlike mammals, both sexes produce it. To cope with the challenges they face raising young, three very different types of bird have evolved the capacity to produce this ‘milk’. Each produces a different form of milk in a different way. For about two months while their special filter-feeding apparatus develops, young flamingos are fed exclusively on milk produced by glands lining the entire upper digestive tract of the parents. For the male Emperor Penguin milk is a back-up; if the female has not returned from foraging at sea by the time the chick has hatched he can feed it for a few days on milk secreted by his oesophagus. The best known of these secretions is the crop milk that all pigeons feed to their squabs. Pigeons eat hard seeds or fruit, which are low in protein. Growing birds need a high protein diet so, instead of providing protein in the form of insects, as do many seed-eaters, pigeons produce a nutritious milk, higher in protein and fat than cow or human milk. Made of sloughed off, fluid-filled cells from the lining of the crop – the thin-walled, sac-like food-storage chamber that projects outward from the base of the oesophagus – it does not resemble mammalian milk but rather cottage cheese. Pigeons begin to produce milk a couple of days before their eggs are due to hatch. They may stop eating so that the milk is uncontaminated by seeds. The squabs are fed on this pure crop milk for the first week or so of life. Then, the parents begin to introduce a proportion of seed, softened from time in their moist crop, until by the end of the second week the squabs are fed entirely on softened adult food. Usually, pigeons lay two eggs. If one fails to hatch, the single squab enjoys the benefits of a supply of crop milk sufficient for two, and by the end of the first week it is almost as big as two normal squabs would be. The built-in milk bar can be a limitation because even if food is plentiful, pigeons can only produce sufficient milk to feed two chicks.
Emerald Dove. (Artist: Trisha Wright) 223
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Toilet trained: the Golden-headed Cisticola Most nesting birds routinely remove or eat the eggshells after their chicks have hatched. This is thought to reduce the risk of predation. But what about smelly faeces that might attract predators and certainly attract insects? The nestlings of many species turn around, point their posteriors away from the nest and fire away. Depending on the aim, their success in keeping the nest clean is variable. Pigeon chicks simply soil their nest. The cleanest nests belong to species such as the Golden-headed Cisticola pictured, which dispose of the faeces. During the first few days after the nestlings hatch, the parents may eat the faeces. At this stage, the droppings are rich in partially digested food and worth recycling, and the parents are reluctant to stray too far from the nest. As the chicks mature they extract more of the nutrients and produce larger faecal sacs, which the parents start to carry away and discard. Disposal of the nestlings’ faeces, either by ingesting them or carrying them away, is largely confined to the passerines and their close relatives. The waste is excreted in a tough mucilaginous sac, shed from the lining of the gut. The nestlings often void after a feed as the parent waits. If the chick is tardy the parent may even poke its bottom to hurry it up. The neat sac is easy to carry and dump, leaving no extraneous sign or scent that might alert predators to the nest. This fastidiousness may also lessen the chance of disease and infestation by nest parasites and prevent tiny chicks from fouling themselves and becoming chilled. Some species wipe the bag onto a bough, while others drop it at some distance from the nest site. Lyrebirds bury it or place it in a stream. In fruit-eaters such as the Mistletoebird, the sacs are full of seeds, which easily germinate to produce more food plants for the bird – an integral part of the partnership that has evolved between the two.
Golden-headed Cisticola. (Artist: Trisha Wright) 224
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A face only a father could love: Pheasant Coucal Despite cuckoos’ notoriety as brood parasites that escape from parental duties by leaving their eggs to be raised by other species, many cuckoos, including the Pheasant Coucal, raise their own offspring. Nevertheless, the Pheasant Coucal is unusual in that care of the offspring is predominantly by the male. Males are the primary carers in about 1% of bird species (see also page 213). Coucal males build the nest and incubate the eggs alone. They also defend the nestlings and deliver about 80% of the food items – large insects, frogs, reptiles, eggs and young of birds and, sometimes, small mammals – to the young. The female assists with feeding but typically makes a minor contribution. The chicks’ fronds of white, hair-like feathers, glossy black skin and red gapes displaying prominent papillae and patterning on the palate create an arresting visual display. Like many passerine nestlings they make creative use of the complexity of colours their parents can see, including vivid mouth colours with high ultraviolet reflectance. This reflectance is likely to improve their conspicuousness since contrast with the nest background is greatest in the ultraviolet and is especially effective in dark nests. The various colour-pattern combinations probably function to stimulate and guide the parent to the open mouths. There is also evidence that the gapes of begging nestlings brighten with the intensity of hunger of the chick – an honest signal of need – so that parents can adjust the amount they feed accordingly. As to the function of the nestlings’ unusual feather tufts, they are on the upper surface only and, provided chicks keep their mouths shut, may help the chicks to look like an empty nest when the father leaves them uncovered while he forages. They certainly function that way when chicks as young as six days old leap from the nest in response to a warning call from their father and huddle together by a tussock or log, where they blend with the pale grass and black soil of the floodplain. The father soon has an empty nest as the young fledge at about 13 days of age, and before they are fully grown. This short stay may have evolved to lessen the chances of predation but it is a feature of all cuckoos, whether parasitic or not. Coucal chicks begging. (Artist: Trisha Wright) 225
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Balanced begging: Singing Bushlark The Singing Bushlark builds a flimsy domed nest in a depression near a tussock. As in all ground-nesters the nestlings are vulnerable to both terrestrial and aerial predators. The chicks’ begging calls can alert predators to the presence of a nest, so chicks remain silent until they see a parent or some other sign of its return, such as movement of the nest or a shadow at the entrance. However, the chicks cannot remain totally silent because their begging also stimulates parents to gather food and can also reveal a chick’s hunger levels, so that the parent can decide which mouth to feed. Hence, a balance has evolved such that communication between parents and offspring occurs and predation is kept to a manageable level at the population level. One way this happens is through the evolution of chick calls: species most at risk of predation have begging calls that are of higher frequency (pitch) and lower amplitude (loudness), which makes them hard to locate. As in all natural systems, there is a complexity of pressures and influences to balance. At the individual brood level, very hungry chicks may beg too frequently and reveal themselves to a predator – this is natural selection in action and is an example of the old maxim survival of the fittest. In fact, a recent study that swapped eggs between parents revealed that begging by chicks was matched to the provisioning capabilities of their biological, not their surrogate, parents. The chicks of parents that were in the best body condition were more robust beggers, regardless of who was feeding them.
Bushlark. (Artist: Trisha Wright) 228
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Bright little beggars: Painted Finch All Australian grassfinch species make a special effort to protect their nests from predators: some hang the nests on twigs above water, some favour the vicinity of wasps’ nests, or the nests of birds of prey, and some build in prickly trees. The Painted Finch usually nests in a small cavity in a dense clump of spinifex grass. Before the nest is started, the birds construct a platform of bark, small stones, clods of earth and sticks, which serves to prevent the sharp spinifex stalks from penetrating the nest. The young beg to be fed by quivering their wings. Within days of hatching they assume a distinctive pose: a prone posture with neck twisted to one side and beak directed upwards. Like all finches, the nestlings’ begging gapes have ‘runway lights’ that stimulate and guide the parent in the dim nest. The edge of the mouth and tongue are highlighted or ringed by dark markings, some brightly coloured, luminescent or in the ultraviolet range, which gives the highest contrast with the background. Changes in their contrasting colours may also indicate chick health or hunger. Each grassfinch species has a different pattern so the gapes also reveal the species to which the nestling belongs (see also page 225).
Painted Finch feeding youngster. (Artist: Trisha Wright) 229
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Cooperative killers: Australian Pelican Like all pelicans, the Australian Pelican is a colonial breeder and needs predator-free nesting places close to super-rich foraging ground to breed. In Australia, major breeding sites are rare and unpredictable and the birds flock to them in their thousands when conditions are right, such as when Lake Eyre floods. Smaller colonies breed on bare coastal islands. Pair formation starts in flocks, with several males following a female on land and water and in the air. Eventually a female retains one follower, who leads her to a nest site. There he uses displays to encourage her to remain while he goes away to gather nest material. The nest, built mainly by the female, consists of a scrape, augmented by a variety of sticks and debris including cattle dung. Territorial defence is limited to the nest site. The pair takes turns guarding the nest site, incubating the eggs and caring for small chicks. They coordinate their hunting: females are away from the nest during the morning and males during the afternoon, with a change-over during the middle of the day. The parents warm the eggs or chicks with their webbed feet (see also page 210). When it is hot and dry, they shade eggs and small chicks with their bodies and wings and may bring them water soaked into their plumage.
Australian Pelican colony. (Artist: Trisha Wright) 230
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Newly hatched chicks are fed a gastric fish soup, from the tip of the upper bill. Older chicks take regurgitated fish from their parent’s throat and often step right into the pouch to do so. Strangely, large chicks sometimes go into convulsions after receiving a large meal, perhaps because of gullet pressure on the single carotid artery. The Australian Pelican usually lays two eggs which hatch asynchronously, about two days apart, so that there is a size difference between the chicks. When the fishing is poor the younger chick starves because the older, dominant chick monopolises the food, kills its sibling or expels it from the nest. It is evolution’s brutal but efficient way of ensuring that when food is short it is not wasted on substandard chicks. In larger colonies, after about a month, when chicks can regulate their own body temperature, they gather into friendly crèches of mixed-aged chicks for protection while their parents are absent hunting.
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Killer babies and insurance eggs: Brown Booby Brown Boobies usually lay two chalky blue or blue-green eggs, five or so days apart. Because the parents start to incubate immediately, the chicks hatch days apart. If both eggs hatch, the second and much smaller chick is outcompeted for food or is killed by its sibling without interference from the parents, which only ever raise a single chick. Hence, the second egg is often regarded as an insurance against the failure of the first egg to hatch. Masked Boobies, egrets, bee-eaters, some eagles and several other birds also have killer hatchlings. In some species, such as Brown Boobies, siblicide is obligate while in others, such as some non-Australian boobies, it is facultative and only occurs when food is scarce. Not only is the oldest chick likely to be larger than its sibling but it may have also been exposed to higher levels of hormones such as testosterone while it is still in the egg and this can trigger aggressive behaviour after hatching. Reproduction is costly and, unsavoury as it sounds, nurturing murderous siblings is an effective way for some birds to maximise the chance of raising a chick and a healthy one at that.
Brown Booby. (Artist: Trisha Wright) 232
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Cheaters versus cheated and odd couples: Eastern Koel, Australasian Figbird and Little Friarbird Eastern Koels are also known as Rainbirds because their annual return to their Australian breeding grounds from a winter spent in Papua-New Guinea signals the arrival of spring rains. Given that most birds vocalise on most days of the year, perhaps the name Rainbird, applied as it is to many species, says more about human observers’ propensities to notice birds prior to rain than about birds’ undoubted sensitivity to imminent rain. Courting male koels call noisily and make short, energetic flight chases of females and rivals. Over weeks, the females lay a single egg in several nests of figbirds, Olive-backed Orioles, Magpie-larks, riflebirds or honeyeaters, such as the Little Friarbird. These are all very different hosts and this visual trickery only works for koels if the cuckoo’s egg is not too much bigger or not too differently coloured from its hosts’, otherwise the egg is rejected. Hence, individual female Eastern Koels specialise on a particular species, laying eggs that match those of their preferred host. The trickery is more likely to work if the koel can quickly lay its egg undetected, so it is probably more likely to parasitise successfully inattentive or inexperienced host pairs. The nestling koel hatches and within 48–72 hours takes over the host’s nest. With its broad flattened back it pushes the host’s nestlings or eggs to the nest rim and shovels them over. After that, if any unfortunate nestlings remain the koel is larger and outcompetes them for food. The cuckoo chick grows rapidly, fledging about seven days earlier from the nests of insect-eaters (diets high in protein) than from those of fruit-eaters. The hapless hosts continue to feed the monster chick for another three to four weeks, during which time it may eat more than a normal, full brood of host chicks, The hosts are apparently tricked into feeding the mammoth impostor by its rapid calls that imitate a whole brood of begging chicks and stimulate the foster parents to deliver enough food for a crowd. Animal behaviourists call this phenomenon super-stimulus. Eastern Koel chick removing an Australasian Figbird hatchling from its nest. (Artist: Trisha Wright) 233
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Cuckoos are viewed as virulent avian brood parasites, both as adults and nestlings, because they reduce the ability of their hosts to produce offspring. The extent of virulence varies widely, both within and between species. In India, for example, the koel’s larger host has nestlings that tolerate some nest mates, perhaps because of the larger nest or the greater capacity of the host to provide food. Traditionally, studies have focused on the benefits of parasitic intolerance to host chicks, but it has been recognised recently that not only are there physical and other constraints on the evolution of chick-killing strategies, but that there are likely to be costs. By killing its host’s offspring, the cuckoo nestling avoids sharing or competing for parental care, but it might cause desertion or lessen parental attentiveness by removing ‘helpers’ in the soliciting of parental care. Hence, the nestling brood parasite must ‘decide’ whether or not to kill all the young of its host by weighing up the benefits of reduced competition in the nest against the risk of desertion or inattention by host parents. The outcome of this trade-off will vary within and between species.
Little Friarbird and Eastern Koel chick. (Artist: Trisha Wright) 234
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Sticking together: Fairy Tern The Fairy Tern produces a single brood per season and both sexes share incubation of the eggs and care of the young. Their nests may be as little as 30 cm apart within a colony of from two to 400 pairs. To some extent, the colony provides the protection (safety in numbers) that might otherwise be afforded by a nest built off the ground or hidden in a bush. The tern’s strategy is to invest relatively heavily in just a few young. They usually lay one or two eggs and incubate for 28 days. The chicks are fed until well after fledging, perhaps even after the family has dispersed from the breeding grounds. When they leave the nest, the downy young group together to form crèches. The camouflage patterning and secretive behaviour of the chicks confer some protection from natural predators, but introduced animals (cats, dogs and foxes) take their toll.
Fairy Terns. (Artist: Trisha Wright) 235
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Sociality for survival: Apostlebird, White-winged Chough and Varied Sittella Some birds are solitary, others flock all or part of the year and there is all sorts of variation between these extremes. Sociable behaviour can have high survival value for some bird species and so it is maintained as part of their interactions. The benefits may include a decreased risk of predation for individuals within the group, increased foraging efficiency and thermoregulatory benefits (see, for example, Black-faced Woodswallows, page 247). Such groups have evolved a complex social structure and the accompanying behaviours to maintain it. Apostlebirds are so called because they often seem to hang around in groups of 12 (typically six to 10 birds, but occasionally in a simple pair or a group of over 20). The group is close knit and its members feed, preen, play, sleep, build a mud nest and raise offspring together. The male is the linchpin that holds the group together, there are one or two dominant females, and the remainder tend to be offspring retained from previous years. The group members feed in close proximity and at night they roost together, touching, and facing the prevailing wind, in the highest part of dense shrub.
Apostlebirds. (Artist: Trisha Wright) 238
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Apostlebirds eke out a living from dry litter and their insect food is often hard to find. Probably, as in Whitewinged Choughs, smaller groups are inefficient reproductive units, and so helpers (previous years’ offspring) are essential for successful breeding. It takes four years for individuals to become sufficiently efficient foragers that they have spare capacity available to feed young and really assist with the breeding attempt. Hence, helper choughs may offer food to the current breeding attempt but then gulp it down themselves. Experiments have shown that helpers seldom monopolise food when it is abundant and that they rarely withhold food from a nestling in the presence of other choughs that might witness the selfish act; that is, when food is scarce, helpers seem to behave deceptively, presumably to avoid punishment by the dominant members of the group (see also page 243).
White-winged Choughs. (Artist: Trisha Wright) 239
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The Varied Sittella is another highly social species. Typically, it lives in groups of between five and seven birds (ranging from a pair up to 20) that forage and roost together. In spring–summer (autumn in the north), all group members contribute to nest construction, feeding of the breeding female and caring for the young. As in Apostlebirds, this cooperation enhances breeding success because it increases group foraging efficiency and decreases vulnerability to predation. Although there are clear reproductive benefits in grouping, the adaptive value of group roosting has not been studied in either species. It can be expected to include a decreased risk of predation. Sittella groups roost along branch, all individuals facing the same way and huddled together, and the dominant males sit at each end. In one group, the outermost, most dominant male went to sleep last, suggesting that he was on guard duty.
Varied Sitellas. (Artist: Trisha Wright) 240
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Lending a hand: Grey-crowned Babbler In general, cooperative breeding is relatively rare in birds and biparental care is far and away the norm. That said, close to one-quarter of Australian endemic passerines breed with the assistance of a group. This might be explained by the Australian climate that can be harsh and unpredictable, thereby providing strong selection pressure for a system where assistance promotes the success of a breeding attempt, especially when times are tough. In some cases it may even evolve to be essential to the success of nesting attempts. Consider the Grey-crowned Babbler that lives and breeds in cooperative territorial groups of two to 15 birds. Groups forage for insects amongst litter and from the bark of trees and shrubs. Groups normally consist of a primary breeding pair and several non-breeders (occasionally groups contain two breeding pairs or two dominant females that both breed) . Most members of the group help to build nests, but the primary female contributes most. They construct two types of nest: roost-nests, usually larger and used by the whole group, and brood-nests for the breeding females. Often old nest sites are renovated and reused in successive years. The nests are large and domed, placed in a tree fork four to seven metres high, and made of thick sticks, with projections that form a covered landing platform for the entrance tunnel.
Grey-crowned Babblers at nest with young. (Artist: Trisha Wright) 241
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The babbler is a facultative cooperative breeder, unlike the White-winged Chough, which is unable to breed in groups of less than four adults. That is, babbler pairs can breed successfully without helpers, but most are assisted by some of their offspring from previous breeding attempts, or by unrelated helpers. Breeding females lay up to four clutches (usually three eggs per clutch) per season and are fed by the other group members, and all help to feed the nestlings. Larger groups tend to raise more young, and it is the assistance of male, but not female, helpers that increases the number of young fledged from individual nests and the likelihood of re-nesting, resulting in higher seasonal fledgling production. Helpers enhance reproduction more in poor conditions, demonstrating the interaction between social and ecological influences on reproductive success. Why would an individual bird give up its own chance to breed to help raise offspring that are not its own? Among the possible benefits are that, because most helpers are relatives, they gain indirect fitness benefits through helping to raise kin. Unrelated helpers, on the other hand, stand to gain a breeding vacancy should it arise. Another benefit is that helpers learn skills and gain experience that are crucial when they themselves breed. Breeding vacancies are usually filled by the oldest unrelated helper or by an immigrant if all the helpers are related to the surviving breeder. Like most things in nature there are potential costs to breeding cooperatively and these include a high risk of inbreeding. Grey-crowned Babblers appear to circumvent this problem because related helpers disperse when their same-sex dominant dies, rather than staying in the hope of inheriting the breeding position.
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Red-eyed kidnapper: White-winged Chough The White-winged Chough is a highly sociable species that performs most of its activities in a family group. Its most visible behaviour is intra-group communication, both auditory – by piping and whistling – and visual, by displays. As in other birds, choughs’ visual displays are often associated with distinctive plumage colours or patterns and the postures are highly stereotyped; they help to defuse aggression and rarely lead to combat. The most prevalent White-winged Chough displays are variations on the ‘Wing-Wag, Tail-Wave’ (WWTW), during which a chough flashes its white wing-patch: it fans and waves its wings and tail in turn, every second or so, and bobs its head. At the same time its eyes become engorged with blood, turning bright red and protruding, making them seem larger. Often one group member starts such a display and soon another follows suit until several perform, presumably achieving group-bonding. The WWTW varies in intensity with circumstance. A noisy, full-blown WWTW might occur in a rare encounter with a neighbouring group when the dominant male leads the group in a mass WWTW display which might be accompanied by displacement behaviour (displaced aggression) such as pecking the ground or pulling out vegetation. Most often the WWTW is used as a greeting between group members, but it can also occur in situations suggestive of punishment or admonishment; for example, it is seen when a youngster has lagged behind the feeding group and rejoins it, or in appeasement by the individual being challenged. Chough groups occasionally raid other group territories and kidnap a fledgling, presumably to bolster their own group size (choughs are obligate cooperative breeders that need a group to breed successfully) and perhaps to introduce ‘new blood’. In these situations, the WWTW is used to entice a fledgling away during an inter-group scuffle. For the adoption to be successful, the fledgling must be under four weeks old – presumably before it develops a sense of identity and place.
WWTW display of the White-winged Chough. (Artist: Trisha Wright) 243
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Waiting in the wings: Laughing Kookaburra Kookaburras live in family groups marked by extreme social behaviour. Their chicks fight for dominance and food so aggressively that the smallest is often killed. In contrast, many adult kookaburras delay their own breeding in order to help their relatives raise young. The helpers are usually young from previous years and, as non-breeding adults, they remain with their parents to aid in territory defence, incubation of eggs, and care of chicks. Helpers take a subordinate position within the family hierarchy, and some individuals are known to remain helpers for up to four years before securing a chance to breed, usually on the death of members of dominant breeding pairs in the same or in neighbouring territories. The kookaburra’s iconic laughing call is far-carrying. It is usually given by the dominant pair, taken up by the group and answered by neighbouring groups. The full laughing call – a staccato ‘kook-kook-kook’ rising to a shout of ‘kook-kook-kook-ka-ka-ka’ before falling to a chuckle – has three primary functions: territorial defence; mate guarding; and establishing and maintaining the dominance of breeding adults over their helpers. It is given rarely when one or both breeding adults are absent, and laughter by helpers, especially during the daytime, indicates a challenge to the dominance of a breeding adult.
Laughing Kookaburra. (Artist: Trisha Wright) 244
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Ritualised aggression: Dusky Moorhen Dusky Moorhens are noisy, aggressive rails that are frequently seen fighting and chasing each other. Like most rails, they are highly territorial and their aggressive (or agonistic) displays are stereotyped and ritualised to avoid serious combat. During the spring and summer moorhen kin groups hold a territory and repel trespassers from their stretch of water. Their displays during these encounters are conspicuous and visual and accompanied by a chorus of resonant ‘koks’, ‘kerks’ and screeches. Typically, when an intruder is first spotted, the resident bird extends its head and neck upwards, holding them rigidly for a few seconds. It then swims towards the trespasser with its neck extended forward and tail lowered. As it approaches the intruder, the defender lowers its head and neck further to a fraction above the water and depresses its tail completely so that motion through the water becomes smooth and swift and the scarlet head shield is prominent. The trespasser then retreats, holding its tail up and frequently flicking it and turning its head. Finally, the resident flaps its wings and runs across the water towards the intruder, slapping the surface with its feet as the trespasser also takes flight.
The Dusky Moorhen’s threat display (foreground left); retreat (foreground right); pursuit across the water (midground); and fighting with feet (background). (Artist: Nicholas Day) 245
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In most such encounters the intruder is driven off and the resident begins to relax, often pecking at the water to release aggression. Very occasionally both parties retreat, each keeping a low profile, with neck extended low, wings partly raised and white undertail feathers fluffed out. In this submissive attitude, the threatening head shield is obscured. If the meeting display fails to thwart the intruder, a ritualised fight may ensue. The birds attack each other with their bills, biting at their opponent’s neck and attempting to drag its head underwater. If one is successful it holds its opponent underwater for 30 seconds, which causes it to retreat. If neither gets a grip, they begin to grapple and strike with their feet, flapping to stay aloft, and then both retreat. As in most species, evolution has ensured that these battles are more ritual than actual bloody combat.
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Cold comfort: Black-faced Woodswallow Compared with mammals of a similar body size, birds maintain a high body temperature; typically 40–44 degrees Celsius. This supports a very active existence including extraordinary feats such as long distance migration. A lot of energy is required to maintain high body temperatures and birds have developed various structural (e.g. circulatory system), metabolic and behavioural ways to manage energy use efficiently both when active and at rest.
Black-faced Woodswallows. (Artist: Trisha Wright) 247
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Feathers are even better insulators than fur and birds can increase insulation by fluffing up their feathers to create warm pockets of air. For small birds, however, feathers are not always enough. Small animals have a relatively large surface area across which to lose heat. One way to counter this is by huddling with neighbours or partners. At low temperatures, huddling reduces the surface area exposed to the cold. The highly social Black-faced Woodswallow often roosts in packed rows and forms clusters of hundreds of individuals on sheltered vertical trunks, like swarms of bees. While such behaviour can conserve heat when it is cold, clustering has often been noted at high temperatures and in full sun, which might suggest that its function is not only to conserve heat. However, woodswallows also use another strategy to cope with the energy cost of maintaining a high body temperature: they do not maintain it; that is, they let their body temperature fall. Dusky Woodswallows have been tracked spending as long as 12 hours of the day in torpor, particularly in autumn–winter when their energy sources (e.g. food or fat reserves) may be scarce and the cost of keeping warm high. Their body temperature may fall as low as 29 degrees Celsius, greatly reduced from an average of 39–40 degrees, and in this state they are immobile and cold to the touch. This ability to go into torpor, with a lower metabolic rate and lower body temperature, can be employed not only in poor weather but also when food is short or as part of the daily routine. The reason that woodswallows huddle together even when it is not cold may simply be that they are using the sun to warm their torpid bodies, thereby conserving energy. The energy savings made by clustering are a major benefit of sociality in these small birds. Savings will vary with conditions, flock size and other factors, but in overseas studies the overnight energy use of grouproosting individuals was only 50–79% of that of loners. In addition, inner birds in the huddle, which were often dominants, burned less energy than those on the edge. All of these benefits may drive selection for huddling behaviour.
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You scratch my back and I’ll scratch yours: Silvereye Feather care is one of the most important aspects of birds’ lives. Well-kept feathers provide insulation, waterproofing, and the means of flight and successful social communication. Maintaining feather health, dealing with the emergence of new feathers and removing ectoparasites, is a complex and time-consuming task, so it is not surprising that some species share the load by grooming their partners or neighbours. This mutual grooming, or allopreening, is usually concentrated in hard-to-reach places such as the back of the neck; occasionally, it is directed at other body feathers, but not flight feathers. Typically, the individuals involved take turns to groom each other. In Silvereyes, allopreening is very common and occurs between sexual pairs, parent–offspring, young siblings, and prospective partners in pair formation, which starts as early as one month of age. It is thought to strengthen pair bonds which are (quite unusually among passerines) monogamous and last year round. Allopreening is one of several behaviours that are both altruistic and selfish. Not only does it have benefits for an individual’s feather health, but it helps to maintain bonds between pairs or flock members and to ease stress in relations between neighbours. Studies of several species have shown that dominant individuals receive the most grooming. Among pairs, allopreening is thought to improve long-term fitness (i.e. dedicated allopreeners raise more offspring over their lifetimes). In flock-nesting species the benefits may be more immediate: fewer conflicts and a greater chance of nesting success. All in all, a well-groomed bird is likely to be a fit bird in the evolutionary sense.
Silvereyes. (Artist: Trisha Wright) 249
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Troop fishing: Australian Pelican The Australian Pelican is one of seven pelican species around the world, all primarily fish-eaters and very similar anatomically, but each slightly different in its foraging strategy. The Australian species is one of several that hunt in cooperative groups. It rarely uses the other main pelican foraging strategy, plunge-diving, and then only makes shallow dives. The Australian Pelican prefers to hunt socially and, provided there are sufficient fish, several birds band together in a fish drive. The group swims slowly forward, thrusting their beaks into the water ahead of them, sometimes in synchrony, or with bills open in the water, leaving little room for fish to escape. Occasionally, two groups form and drive fish towards each other to trap them between. Flocks also form chains of ‘beaters’, scaring the fish by vigorous wing beats and blocking off large areas of the water surface. More often the team swims in linear formation or a semi-circle to herd fish towards the shore, where they can be more easily caught. Thus, they move slowly from deeper to shallower water until they merely have to scoop up their prey. Not surprisingly this group effort is more successful for individuals than solo fishing and presumably has been favoured by evolution.
Australian Pelicans. (Artist: Nick Day) 250
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Cooperative spear-fisherman: Black-necked Stork ( Jabiru) The Black-necked Stork feeds in shallow margins of lakes, mudflats and rivers, but less often in grassland and open woodland. Typically the birds walk busily about searching, or dash around in pursuit of prey, jabbing with their bulky, dagger-like bill, which is used to spear fish up to about 500 grams in weight, young crocodiles, snakes and turtles. The storks hunt solo, in pairs, family groups and mixed species flocks. Family groups hunt in close formation through the water, sometimes stirring with their feet, or flashing open their wings, to flush prey ahead of them. Occasionally the storks get together with other similar species – several birds walking together side by side toward shore, herding fish into shallower water. The storks are not to be trusted, however, because they will also steal fish from other birds.
Black-necked Stork. (Artist: Trisha Wright) 251
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A one-sided affair? Azure Kingfisher and Platypus The ‘fishing’ kingfishers (Family Alcedinidae) can dive up to two metres below the surface of the water to catch prey, although none feeds exclusively on fish. One member of the family, the Azure Kingfisher, follows Platypuses to catch the animals they disturb. The bird, or pair of birds, hovers above the mammal, perhaps intentionally disturbing it, although the Platypus appears to be unperturbed. Often, immediately after the Platypus dives to search the bottom, so too does a bird. One mammal–bird pair was observed to dive together seven times in an hour, the bird invariably surfacing from the disturbed area with a fish. The Azure Kingfisher is among the few members of the kingfisher family that occasionally hunt by following other animals, including otters, cormorants, egrets, cattle and army ants, to catch the small animals that they scatter. Some species also attend grassfires and catch prey flushed by the flames. These behaviours are all very similar and, in an evolutionary sense, could be related
Azure Kingfisher and Platypus. (Artist: Trisha Wright)
to kleptoparasitism (one species steals from another). Theft has been reported among several of the world’s kingfishers; the victims include birds, water shrews, hawks and tree snakes.
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Lured into the shadows: Cattle Egret The pasture-feeding Cattle Egret forages primarily for insects, particularly crickets and grasshoppers, in association with grazing stock, but it can also catch prey in water like more typical herons. Over water it sometimes extends one or both wings umbrella-like to shade the surface, which reduces glare and may attract shade-loving fish and aquatic invertebrates. It may also stir the water with one foot to disturb prey. Although it is an adaptable forager, the Cattle Egret is named for its most obvious habit of following large co-occurring native mammals and, in more recent times, cattle, all of which flush small animals and invertebrates as they wander and graze. The relationship is far from passive. The egrets may defend individual cattle and provoke them to move. Studies have shown that egrets associated with cattle capture many more insects per unit time than when foraging alone. The egrets also use the cattle as a perch or vantage point and remove and eat external parasites from them. From Africa, the egret followed the human transport of livestock through Asia and to Australia, arriving about a century after the cattle, in the mid-twentieth century; it also reached North and then South America. The relationship evolved in Africa has equipped the egret to spread across the world.
Cattle Egret. (Artist: Trisha Wright) 255
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Farming mistletoe? Mistletoebird Many birds depend to a greater or lesser extent on a particular plant or animal for their livelihood or reproduction, but reciprocal relationships are less common. The partnership between the Mistletoebird and mistletoes is a good example of reciprocity: their association is obligatory – each species depends on the other to reproduce successfully. Hence, the relationship is usually considered to be symbiotic, an extreme form of mutualism. Although mistletoe berries are the main food of the Mistletoebird it also eats insects, spiders, nectar, pollen and berries from other plants, all gleaned from the canopy. However, the bird’s nesting season is tied to the fruiting of the mistletoe and begins after the first mistletoe berries become available. Mistletoes fruit for many months and the birds can be seen flitting between clumps. At firm-fruited mistletoes, the bird pecks the unattached end of the seed case then extracts the pulp and seed before ingesting them, leaving the empty skin hanging; with softer-skinned mistletoes the bird chews the fruit then spits out the skin.
Mistletoebird. (Artist: Nicholas Day) 256
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Numerous backward-pointing projections on the dorsal surface of the Mistletoebird’s tongue assist in chewing and swallowing fruits. Even the bird’s digestive system is specially adapted to process the berries and it easily separates the seed from the nutrients in its sweet sticky pulp. The bird’s gut is modified to form a simple tube that allows the seeds to bypass the small gizzard, which is attached as a blind sac. The pulp is digested and nutrients extracted while the seeds pass directly through and are voided intact, with a sticky coating – the remnants of the pulp. The droppings (faeces) stick to branches and in time the seeds germinate. The Mistletoebird’s voiding method also helps it to keep its end of the bargain. It voids a string of mistletoe seeds, jerking its abdomen against the branch to deposit the gluey strand. The birds may raise up to three broods in a season. In the meantime, the nest tree and lookout trees, which may not be infected, are particular recipients of a new crop of mistletoes seeded during this time. The bird and plant are co-adapted: the mistletoe supplies the bird with a reliable source of food and, in return, the parasitic plant has its seeds disseminated to suitable arboreal germinating places. The birds also help to cross-fertilise the plants, by dispersing pollen as they forage. The Mistletoebird is an Australian member of the southern Asian-Australasian family of flowerpeckers, several species of which have evolved close relationships with plants, particularly mistletoes. The evolutionary relationship between several Australian birds and mistletoes has been a productive area of study and no doubt more remains to be learned.
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Pest control: Spotted Pardalote Pardalotes, honeyeaters and thornbills are among several birds that feed on carbohydrate-rich sugars from trees: manna, the crystalline sap which oozes from injuries to trees made by insects or other animals; honeydew, the exudate of sap-sucking coccids and aphids; and lerps, the protective sugary coating of psyllid larvae. Pardalotes have intimate relationships with eucalypts, feeding on the nymphs of eucalypt leaf-eating insects, and their sugary exudate, or lerp. They have morphological and behavioural adaptations for foliage gleaning, including a stubby bill adapted for removing the lerp coating and the psyllid, and other insects from the surface of leaves. Pardalotes, such as the Spotted Pardalote illustrated, usually nest in tree hollows or in burrows tunnelled into the ground, where they build a loose domed nest of bark strips lined with grass. Both sexes participate in tunnel construction, nest building, incubation and feeding young. They feed their young on a range of invertebrates, and even occasionally small vertebrates. However the main year-round food item, at least for mainland species, is lerps, preferably varieties with high levels of soluble sugars. In Tasmania, in contrast, pardalotes feed more extensively on manna. The birds are thought to perform a service for the plants by keeping these damaging insect pests at a level that the tree can sustain, and preventing outbreaks. One long-term study, for example, found that predation of nymphs and adults by pardalotes, especially the Striated Pardalote, and other lerp eaters, played a dominant role in protecting Eucalyptus blakelyi from overpopulation by the psyllid Cardiaspina albitextura.
Spotted Pardalote feeding chicks. (Artist: Trisha Wright) 258
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Looking after trees? Bell Miner The variety, widespread distribution and abundance of honeyeaters in Australia are explained by the group’s ability to exploit the abundance and diversity of carbohydrate-rich foods provided by nectar-producing trees and shrubs; and manna, honeydew and lerps from the foliage and bark of eucalypts, often at times of year when nectar is less abundant. The trees and shrubs benefit by the cross-pollination and pest-control services provided by the birds. Indeed, some plants depend almost entirely on honeyeaters for pollination and maximum seed production, and set fewer seeds in their absence or when visited less frequently. Honeyeaters forage mainly in trees and shrubs, probing flowers for nectar, consuming fruit, or searching bark and foliage for arthropods, manna, honeydew or lerps. Tall forests, rainforests, mangroves, arid shrublands and non-heathy coastal shrublands often support honeyeaters throughout the year with a succession of flowers, fruit, manna, honeydew or lerps, all providing carbohydrate that is easily digested by the honeyeaters. Insects and pollen provide protein. This high-energy diet supports honeyeaters’ intensely active and aggressive behaviours. Individuals and groups of many honeyeaters, particularly large species, vigorously defend of patches of blossom, nectar and other vital sources of carbohydrate, excluding other birds. They actively probe flowers and glean insects in the foliage, and sally out to snap up airborne insects as the day progresses and nectar flow decreases. Like many honeyeaters, Bell Miners eat psyllid larvae and their sugary protective coating (lerp). The miners establish dense colonies near eucalypts that are already infested with abundances of lerps, and the whole miner community pugnaciously excludes most other birds,
Bell Miner with psyllid larvae. (Artist: Trisha Wright) 259
Stray Feathers
especially smaller, more efficient foliage gleaners. There has even been a suggestion that the miners ‘farm’ lerps but it has not been substantiated. Regardless, the resulting lower predation pressure promotes higher psyllid densities and contributes to eucalypt death (die-back). The miners are behaving naturally but habitat change, particularly fragmentation into small easily monopolised patches, and poor forest health, are thought to contribute to this imbalance. The miner-enhanced psyllid plague may simply be the last straw for the trees.
260
Wrapping up
Wrapping up Towards the end of writing this book, Leo found himself giving a brief talk to a small group of enthusiasts on the subject of bird migration. He couldn’t resist telling his audience about some recent discoveries concerning the truly spectacular, mind-boggling feats that are accomplished by migratory shorebirds. Using geolocators and satellite telemetry, researchers around the world have been learning that birds such as Bar-tailed Godwits make non-stop flights of 14 000 km across the Pacific Ocean from Alaska to New Zealand. And that a Red Knot has been recorded flying 8 000 km in six days non-stop across South America, the West Indies and much of North America before landing near Philadelphia to refuel for the last leg of its migration on the energyrich eggs of horseshoe crabs. He spoke also of research showing that godwits undergo a reduction in the size of many of their internal organs during these global migrations, except, remarkably enough, in the size of the brain. This points to the relative importance of the brain in accomplishing these migrations. It is tempting just to marvel at these phenomena and think of them as among nature’s great mysteries. Yet they typify what this book has set out to achieve. The success with which these birds can breed in response to the great, fleeting, summer productivity of their northern hemisphere breeding grounds underlies the migration, at least in part. Evolution has driven and moulded the birds’ navigation mechanisms and their physiology to enable them to accomplish these migrations while it is worth doing so. We started this book by thinking about the evolution wrapped up in a beautiful male White-winged Fairywren perched atop a chenopod bush. He may never move more than a few hundred metres from that bush in his lifetime. Although finishing the book with birds that move across the globe twice a year for most of their lives is a marvellous contrast, the message of the evolution underlying it all is the same. We do not want to peddle the old notion that evolution has made every bird into a magnificently efficient biological machine, because evolution often does not result in the most efficient way of doing things. Instead, it is a mechanism that sculpts organisms to their environments and there are many ways that evolution can deal with one given selection pressure from the environment. Examples include how an organism copes with thermal stress, whether it be extreme heat or cold. There might be behavioural adaptations such as evolving a fossorial (burrowing) habit. There may be morphological adaptations such as feathers with highly efficient insulation. Physiological adaptations such as aestivation or water economy may evolve. Or natural selection may even drive migration, where the birds go somewhere else for part of the year. Often more than one pressure will be involved and we have tried to convey something of the range of these evolutionary pressures and responses in birds. These pressures and responses may not be mentioned in every section, but they are implied.
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Birds have evolved much overt diversity that we, as similarly visual creatures, can often (but not always) easily detect. We need to remember that any group of organisms, and birds are certainly no exception, is the result of different evolutionary forces acting on different parts of their life history and biology and on different senses. Yet birds have been one of nature’s more successful evolutionary experiments, resulting in their tremendous diversity. How lucky we are to be able to see and enjoy that rich diversity.
262
Further reading
Further reading NOTE: The ‘Further reading’ section is not comprehensive; rather, it contains the main references that were sourced. Much of the basic information in this book was gleaned from or corroborated by the Handbook of Australian, New Zealand and Antarctic Birds (Oxford University Press, Melbourne) and references therein.
Page 12: Introduction
Paton, T. and Baker, A. (2006) Sequences from 14 mitochondrial genes provide a well-supported phylogeny of the Charadriiform birds congruent with the nuclear RAG-1 tree. Molecular Phylogenetics and Evolution 39: 657–667.
Barker, F.K., Barrowclough, G.F. and Groth, J.G. (2002) A phylogenetic hypothesis for passerine birds: taxonomic and biogeographic implications of an analysis of nuclear DNA sequence data. Proceedings of the Royal Society London B 269(1488): 296–308.
Paton, T., Baker, A.J., Groth, J.G. and Barrowclough, G.F. (2003) RAG-1 sequences resolve phylogenetic relationships within Charadriiform birds. Molecular Phylogenetics and Evolution 29: 268–278.
Barker, F.K., Cibois, A., Schikler, P.A., Feinstein, J. and Cracraft, J. (2004) Phylogeny and diversification of the largest avian radiation. PNAS 101: 11040–11045. Brennan, P.L.R., Prum, R.O., McCracken, K.G., Sorenson, M.D., Wilson, R.E. and Birkhead, T.R. (2007) Coevolution of male and female genital morphology in waterfowl. PLoS ONE 2(5): e418. Doucet, S.M., Shawkey, M.D., Rathburn, M.K., Mays, Jr. H.L. and Montgomerie, R. (2004) Concordant evolution of plumage colour, feather microstructure and a melanocortin receptor gene between mainland and island populations of a fairy-wren. Proceedings of the Royal Zoological Society of London B 271: 1663–1670. Driskell, A.C., Prum, R.O. and Pruett-Jones, S. (2010) The evolution of black plumage from blue in Australian fairy-wrens (Maluridae): genetic and structural evidence. Journal of Avian Biology 41: 505–514.
Rathburn, M. and Montgomerie, R. (2003) Breeding biology and social structure of White-winged Fairywrens (Malurus leucopterus): comparison between island and mainland subspecies having different plumage phenotypes. Emu 103: 295–306.
Page 18: Light, compact skeleton Brooke, M. and Birkhead, T. (1991) The Cambridge Encyclopedia of Ornithology. Cambridge University Press, Cambridge. Evans, H.E. (1982) Anatomy of the Budgerigar. In Diseases of Cage and Aviary Birds. Second edition. (Ed. M. Petrak) pp. 111–187. Lea and Febiger, Philadelphia. Gionfriddo, J.P. and Best, L.B. 1999. Grit use by birds: a review. Current Ornithology 15: 89–148.
Ericson, P.G.P. and Johansson, U.S. (2003) Phylogeny of the Passerida (Aves: Passeriformes) based on nuclear and mitochondrial sequence data. Molecular Phylogenetics and Evolution 29: 126–138.
Reynolds, S.J. and Perrins, C.M. (2010) Dietary calcium availability and reproduction in birds. Current Ornithology 17: 31–74.
Garnett, S. and Growley, G. (1995) Feeding ecology of Hooded Parrots Psephotus dissimilis during the early wet season. Emu 95: 54–61.
Page 19: Rigid yet flexible skulls Bock, W.J. (1964) Kinetics of the avian skull. Journal of Morphology 114: 1–42.
Olsen, P. and Olsen, J. (1992) Does rain hamper raptors’ hunting? Emu 92: 184–187. 263
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Brooke, M. and Birkhead, T. (1991) The Cambridge Encyclopedia of Ornithology. Cambridge University Press, Cambridge.
Patel, N.H. (2006) How to build a longer beak. Science 442: 5125–516. Weiner, J. (1995) The Beak of the Finch: A Story of Evolution in Our Time. Vintage, London.
Burton, P.J.K. (1974) Feeding and the Feeding Apparatus in Waders: A Study of Anatomy and Adaptations in the Charadrii. British Museum of Natural History, London.
Page 26: A loaded spring Proctor, N.S. and Lynch, P.J. (1998) Manual of Ornithology: Avian Structure and Function. Yale University Press, New Haven.
Burton, P.J.K. (1974) Jaw and tongue features in Psittaciformes and other orders with special reference to the anatomy of the Tooth-billed Pigeon (Didunculus strigirostris). Journal of Zoology 174: 255–276. Evans, H.E. (1982) Anatomy of the Budgerigar. In Diseases of Cage and Aviary Birds. Second edition. (Ed. M. Petrak) pp. 111–187. Lea and Febiger, Philadelphia.
Page 21: Monster-mouth insect trap
Page 27: Complex respiratory system Proctor, N.S. and Lynch, P.J. (1998) Manual of Ornithology: Avian Structure and Function. Yale University Press, New Haven.
Page 28: Efficient digestive system
Cleere, N. (2010) Nightjars of the World: Potoos, Frogmouths, Oilbird and Owlet-Nightjars. WILDGuides, Hampshire.
Evans, H.E. (1982) Anatomy of the Budgerigar. In Diseases of Cage and Aviary Birds. Second edition. (Ed. M. Petrak) pp. 111–187. Lea and Febiger, Philadelphia.
Diamond, J. (1994) Nature’s infinite book: Stinking birds and burning books. Natural History 103: 4–12.
Karsov, W.H. (1990) Digestion in birds: chemical and physiological determinants and ecological implications. Studies in Avian Biology 13: 391–415.
Page 23: A diversity of beaks Frith, C.B. and Frith, D.W. (2004) The Bowerbirds: Ptilonorhynchidae. Oxford University Press, Melbourne.
Page 24: Boy bills and girl bills
Stevens, C.E. and Hume, I.D. (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiological Reviews 78: 393–427.
Frith, C.B. and Beehler, B.M. (1998) The Birds of Paradise: Paradisaeidae. Oxford University Press, Melbourne.
Wyndham, E. (1980) Diurnal changes in crop contents and total body lipids of Budgerigars Melopsittacus undulatus. Ibis 122: 229–234.
Page 25: Interlude
Wyndham, E. (1980) Diurnal cycle, behaviour and social organization of the Budgerigar. Emu 80: 25–30.
Abzhanov, A., Protas, M., Grant, R.B., Grant, P.R. and Tabin, C.J. (2004) Bmp4 and morphological variation of beaks in Darwin’s finches. Science 305: 1462–1465.
Zann, R. (1996) The Zebra Finch: A Synthesis of Field and Laboratory Studies. Oxford University Press: Oxford, UK.
Abzhanov, A., Kuo, W.P., Hartmann, C., Grant, R.B. and Grant, P.R. (2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin’s finches. Science 442: 563–567.
Page 29: Water saver Johnson, O.W. and Skadhauge, E. (1975) Structuralfunctional correlations in kidneys and observations of 264
Further reading
colon and cloacal morphology in certain Australian birds. Journal of Anatomy 120: 495–505.
Hagelin, J. (2007) The citrus-like scent of crested auklets: reviewing the evidence for an avian olfactory ornament. Journal of Ornithology 148(Suppl 2): S195–S201.
Maloney, S.K. and Dawson, T.J. (1998) Ventilatory accommodation of oxygen demand and respiratory water loss in a large bird, the Emu (Dromaius novaehollandiae), and a re-examination of ventilatory allometry for birds. Physiological Zoology 71: 712–719.
Hagelin, J. and Jones, I.J. (2007) Bird odors and other chemical substances: a defense mechanism or overlooked mode of intraspecific communication. The Auk 124: 741–761. Steiger, S.S., Fidler, A.E., Vaclu, M. and Kempenaers, B. (2008) Avian olfactory gene repertoires: evidence for a well-developed sense of smell in birds? Proceedings of the Royal Society of London B 275: 2309–2317.
Page 30: Oil powered Jacob, J. (1982) Stomach oils. In Avian Biology. Vol. 6. (Eds D.S. Farner, J. King and K.C. Parkes) pp. 325– 340. Academic Press, London.
Page 37: Seeing double
Place, A.R., Stoyan, N.C., Ricklefs, R.E. and Butler, R.G. (1989) Physiological basis of stomach oil formation in Leach’s Storm-Petrel (Oceanodroma leucorhoa). Auk 106: 687–699.
Doucette, L. (2009) The adaptable owlet-nightjar. Wingspan 19(2): 38–41. Martin, G.R. (1978) Through an owl’s eye. New Scientist 77: 72–74.
Ricklefs, R.E., Roby, D.D. and Williams, J.B. (1986) Daily energy expenditure of adult Leach’s StormPetrels during the nesting cycle. Physiological Zoology 59: 649–660.
Martin, G.R. (1985) Eye. In Form and Function in Birds, Vol III. (Eds. A.S. King and J. McLelland) pp. 311– 371. Academic Press, London. Martin, G.R. (2007) Visual fields and their functions in birds. Journal of Ornithology 148(Suppl 2): S547–562.
Page 31: The salt shedder Peaker, M. and Linzell, J.L. (1975) Salt Glands in Birds and Reptiles. Cambridge University Press, Cambridge.
Pettigrew, J.D. (1986) The evolution of binocular vision. In Visual Neuroscience. (Eds J.D. Pettigrew, K.J. Sanderson and W.R. Levick) pp. 208–222. Cambridge University Press, Cambridge.
Page 32: Brain power Low, P.S., Shank, S.S., Sejnowski, T.J. and Margoliash, D. (2008) Mammalian-like features of sleep in Zebra Finches. Proceedings of the National Academy of Sciences 105: 9081–9086.
Schwab, I.R. and Hart, N.S. (2003) In the search for stereopsis. British Journal of Ophthalmology 87: 1205.
Page 39: By the light of the moon
Romer, A.S. (1970) The Vertebrate Body. W.B. Saunders, London.
Carstairs, J.L. (1974) The distribution of Rattus villosissimus (Waite) during plague and non-plague years. Australian Wildlife Research 1: 95–106.
Seed, A.M., Emery, N.J. and Clayton, N.S. (2009) Intelligence in corvids and apes: a case of convergent evolution? Ethology 115: 401–420.
Page 36: Sense organs
Husband, S. and Shimizu, T. (2001) Evolution of the avian visual system. In Avian Visual Cognition. (Ed. R.G. Cook), http://www.pigeon.psy.tufts.edu/avc/ husband/
Evans, H.E. (1982) Anatomy of the Budgerigar. In Diseases of Cage and Aviary Birds. Second edition. (Ed. M. Petrak) pp. 111–187. Lea and Febiger, Philadelphia.
Jackson, S.W. (1919) Haunts of the Letter-winged Kite (Elanus scriptus) with an account of its breeding habits, and notes on other species. Emu 18: 160–172.
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paleognathous and neognathous birds. Journal of Anatomy 211: 493–502.
Klapske, J. (1979) Field notes on the Letter-winged Kite Elanus scriptus at Werribee, Victoria, 1977. Australian Bird Watcher 8: 19–26. Pettigrew, J.D. (1982) A note on the eyes of the Letterwinged Kite Elanus scriptus. Emu 82 (Suppl.): 305–308. Proctor, N.S. and Lynch, P.J. (1993) Manual of Ornithology. Avian Structure and Function. Yale University Press, New Haven.
Piersma, T., van Aelst, R., Kurk, K., Berkhoudt, H. and Maas, L.R.M. (1998) A new pressure sensory mechanism for prey detection in birds: the use of principles of seabird dynamics? Proceedings of the Royal Society: Biological Sciences 265: 1377–1383.
Page 45: The smell of the sea
Page 41: Silent night hunters
Bang, B.G. and Cobb, S. (1968) The size of the olfactory bulb in 108 species of birds. Auk 85: 55–61.
del Hoyo, J., Elliott, A and Sargatal, J. (Eds) (1999) Handbook of the Birds of the World. Vol. 5. Barn-Owls to Hummingbirds. Lynx Edicions, Barcelona.
Grubb, T.C. (1972) Smell and foraging in shearwaters and petrels. Nature 237: 404–405.
Knudsen, E.I. and Konishi, M. (1979) Mechanisms of sound localisation in the Barn Owl (Tyto alba). Journal of Comparative Physiology A 13: 13–21.
Grubb, T.C. (1974) Olfactory navigation to the nesting burrow in Leach’s Petrel (Oceanodroma leucorhoa). Animal Behaviour 22: 192–202.
Konig, C., Weick, F. and Becking, J.-H. (1999) Owls. A Guide to the Owls of the World. Pica Press, Sussex.
Mardon, J., Nesterova, A.P., Traugott, J., Saunders, S.M. and Bonadonna, F. (2010) Insight of scent: experimental evidence of olfactory capabilities in the Wandering Albatross (Diomedea exulans). Journal of Experimental Biology 213: 558–563.
Konishi, M. (1973) How the owl tracks its prey. American Scientist 61: 414–424. Norberg, R.Å. (1977) Occurrence and independent evolution of bilateral ear asymmetry in owls and implications on owl taxonomy. Philosophical Transactions of the Royal Society of London B 280: 375–408.
Nevitt, G.A. (1999) Foraging by seabirds in an olfactory landscape. American Scientist 87: 46–53. Nevitt, G.A. and Bonadonna, F. (2005) Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds. Biology Letters 1: 303–305.
Payne, R.S. (1971) Acoustic location of prey by Barn Owls (Tyto alba). Journal of Experimental Biology 54: 535–573.
Simpson, K. and Day, N. (1984) The Birds of Australia. Currey O’Neil, South Yarra.
Page 43: Sight and sonar
Page 46: Interlude
Thomassen, H.A. and Povel, G.D.E. (2006) Comparative and phylogenetic analysis of the echo clicks and social vocalisations of swiftlets (Aves: Apodidae). Biological Journal of the Linnean Society 88: 631–643.
Menashe, I., Man, O., Lancet, D. and Gilad, Y. (2003) Different noses for different people. Nature Genetics 34: 143–144.
Page 50: Sophisticated syrinxes
Page 44: Seeing through the mud
Brackenbury, J.H. (1989) Functions of the syrinx and the control of sound production. In Form and Function in Birds. Vol. 4. (Eds A.S. King and J. McLelland) pp. 193–220. Academic Press, London.
Cunningham, S., Castro, I. and Alley, M. (2007) A new prey-detection mechanism for kiwi (Apteryx spp.) suggests convergent evolution between 266
Further reading
Evans, H.E. (1982) Anatomy of the Budgerigar. In Diseases of Cage and Aviary Birds. Second edition. (Ed. M. Petrak) pp. 111–187. Lea and Febiger, Philadelphia. Johnsgard, P.A. (1961) The tracheal anatomy of the Anatidae and its taxonomic significance. Wildfowl Trust Annual Report 12: 58–69.
Page 60: Nectar straws Christidis, L., Schodde, R., Shaw, D.D. and Maynes, S.F. (1991) Relationships among the Australo-Papuan parrots, lorikeets and cockatoos (Aves: Psittaciformes): Protein evidence. Condor 93: 302–317. Collins, B.G., Newland, C. and Briffa, P. (1984) Nectar utilisation and pollination by Australian honeyeaters and insects visiting Calothamnus quadrifidus (Myrtaceae). Australian Journal of Ecology 9: 353–365.
King, A.S. (1989) Functional anatomy of the syrinx. In Form and Function in Birds. Vol. 4. (Eds A.S. King and J. McLelland) pp. 105–192. Academic Press, London.
Moreau, R.E., Perrins, M. and Hughes, J.T. (1969) Tongues of the Zosteropidae (White-eyes). Ardea 57: 29–47.
Page 53: Built-in bagpipes Fitch, W.T. (1999) Acoustic exaggeration of size in birds via tracheal elongation: comparative and theoretical analyses. Journal of Zoology 248: 31–48.
Parker, S.A. (1973) The tongues of Ephthianura and Ashbyia. Emu 73: 19–20.
Frith, C.B. (1984) Adaptive significance of tracheal elongation in manucodes (Paradisaeidae). Condor 9: 552–555.
Paton, D.C. and Collins, G.B. (1989) Bills and tongues of nectar-feeding birds: a review of morphology, function and performance, with intercontinental comparisons. Australian Journal of Ecology 14: 473–506.
Page 54: The air drummer
Scharnke, H. (1932). Ueber der Bau der Zunge der Nectariniidae, Promeropidae und Drepanididae nebst Bemerkungen zur Systematik fur blütenbesuchenden Passeres. Journal für Ornithologie 80: 114–123.
Murie, J. (1867) On the tracheal pouch of the Emu (Dromaeus novae-hollandiae, Vieill.). Proceedings of the Zoological Society of London 35: 405–415.
Schlamowitz, R., Hainsworth, F.R. and Wolf, L.L. (1976). On the tongues of sunbirds. Condor 78: 104–107.
Page 55: A sound-sensing helmet? Crome, F. and Moore, L. (1988) The cassowary’s casque. Emu 88: 123–124.
Page 62: Brush tongued
Mack, A.L. and Jones, J. (2003) Low-frequency vocalizations by cassowaries (Casuarius spp.) Auk 120: 1062–1068.
Collins, B.G. (1985) Energetics of foraging and resource selection by honeyeaters in forest and woodland habitats of Western Australia. New Zealand Journal of Zoology 12: 577–587.
Richardson, K.C. (1991) The bony casque of the Southern Cassowary Casuarius casuarius. Emu 91: 56–58.
Page 56: The roarer Marchant, S. and Higgins, P. J. (Eds) (1993) Handbook of Australian, New Zealand and Antarctic Birds. Vol. 2. Raptors to Lapwings. Oxford University Press, Melbourne.
Collins, B.G., Newland, C. and Briffa, P. (1984) Nectar utilization and pollination by Australian honeyeaters and insects visiting Calothamnus quadrifidus (Myrtaceae). Australian Journal of Ecology 9: 353–365. Ford, H.A. (1979) Interspecific competition in Australian honeyeaters – depletion of common resources. Australian Journal of Ecology 4: 145–164. Ford, H.A. and Paton, D.C. (1986) (Eds) The Dynamic Partnership: Birds and Plants in Southern Australia. South Australian Government Printer, Adelaide.
Ziembicki, M. (2010) Australian Bustard. CSIRO Publishing, Collingwood. 267
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trinkmethoden der papageien (Psittaci). Bonner Zoologische Monographien 13: 1–192.
Paton, D.C. and Collins, B.G. (1989) Bills and tongues of nectar-feeding birds: a review of morphology, function and performance, with intercontinental comparisons. Australian Journal of Ecology 14: 473–506.
Page 67: A quick drink
Paton, D.C. and Ford, H.A. (1983) The influence of plant characteristics and honeyeater size on levels of pollination in Australian plants. In Handbook of Experimental Pollination Biology. (Eds C.E. Jones and R.J. Little) pp. 235–248. Van Nostrand Reinhold, New York.
Homberger, D. (1980) Funkionell-morphologische untersuchungen zur radion der ernahrungs-und trinkmethoden der papageien (Psittaci). Bonner Zoologische Monographien 13: 1–192. Forshaw, J. (2003) Australian Parrots. Alexander Editions, Robina.
Page 63: Sweet tongued
Page 71: Featherlight
Gartrell, B.D. and Jones, S.M. (2001) Eucalyptus pollen grain emptying by two Australian nectarivorous psittacines. Journal of Avian Biology 32: 224–230.
Grubb, T.C. (2006) Ptilochronology: Feather Time and the Biology of Birds. Oxford University Press, Oxford.
Gartrell, B.D., Jones, S.M., Brereton, R.N. and Astheimer, L.B. (2000) Morphological adaptations to nectarivory of the alimentary tract of the swift parrot Lathamus discolor. Emu 100: 274–279. Richardson, K.C. and Wooler, R.D. (1990) Adaptations of the alimentary tracts of some Australian lorikeets to a diet of pollen and nectar. Australian Journal of Zoology 38: 581–586.
Jenni, L. and Winkler, R. (1994) Moult and Aging of European Passerines. Academic Press, London. Lucas, A.M. and Stettenheim, P.R. (1972) Avian Anatomy: Integument, Part I. Agriculture Handbook 362, Washington. Proctor, N.S. and Lynch, P.J. (1993) Manual of Ornithology. Avian Structure and Function. Yale University Press, New Haven.
Wyndham, E. and Cannon, C.E. (1985) Parrots of eastern Australian forests and woodlands: the genera Platycercus and Trichoglossus. In Birds of Eucalypt Forests and Woodlands: Ecology, Conservation and Management. (Eds A. Keast, H.F. Recher, H. Ford and D. Saunders) pp. 141–150. Surrey Beatty, Melbourne.
Page 73: A diversity of feathers Evans, H.E. (1982) Anatomy of the Budgerigar. In Diseases of Cage and Aviary Birds. Second edition. (Ed. M. Petrak) pp. 111–187. Lea and Febiger, Philadelphia. Lucas, A.M. and Stettenheim, P.R. (1972) Avian Anatomy: Integument, Part I. Agriculture Handbook 362, Washington.
Page 65: Fork tongued Parker, S.A. (1982) The relationships of the AustraloPapuan treecreepers and sittellas. South Australian Omithologist 28: 197–200.
Page 74: Feathers are better than fur
Schodde, R. and Mason, I. (1999) The Directory of Australian Birds. CSIRO Publishing: Melbourne.
Page 66: Shelling seed
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characterisation of the muscles used to power running in the Emu (Dromaius novaehollandiae), a giant flightless bird. Journal of Experimental Biology 175: 233–249. Patak, A.E. and Baldwin, J. (1998) Pelvic limb musculature in the Emu Dromaius novaehollandiae
Irwin, D.E. and Irwin, J.H. (2005) Siberian migratory divides: the role of seasonal migration in speciation. In Birds of Two Worlds: The Evolution of Migration. (Eds R. Greenberg and P. Marr) pp. 27–40. Johns Hopkins University, Baltimore.
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Tuck, G.N., Polacheck, T., Croxall, J.P., Weimerskirch, H., Prince, P.A. and Wotherspoon, S. (1999) The potential of archival tags to provide long-term movement and behaviour data for seabirds: first results from Wandering Albatross Diomedea exulans of South Georgia and the Crozet Islands. Emu 99: 60–68.
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Lowe, K.W. (1982) Feeding behaviour and diet of the Royal spoonbill (Platalea regia) in Westernport Bay. Emu 82: 163–168.
Olsen, P. (1995) Australian Birds of Prey. University of New South Wales Press: Sydney.
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Avise, J.J., Nelson, W.S. and Sibley, C.G. (1994) DNA sequence support for close phylogenetic relationship between some storks and New World vultures. Proceedings of the National Academy of Science USA 91: 5173–5177.
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Barker, R.D. and Vestjens, W.J.M. (1989) The Food of Australian Birds. 1. Non-Passerines. CSIRO Division of Wildlife and Ecology, Canberra.
Schodde, R. and Mason, I. (1999) The Directory of Australian Birds. CSIRO Publishing: Melbourne.
Cracraft, J., Barker, F.K., Braun, M., Harshman, J., Dyke, G.J., Feinstein, J., Stanley, S., Cibois, A., Schikler, P., Beresford, P., García-Moreno, J., Sorenson, M.D., Yuri, T. and Mindell, D.P. (2004) Phylogenetic relationships among modern birds (Neornithes): toward an avian tree of life. In Assembling the Tree of Life. (Eds J. Cracraft and M.J. Donoghue) pp. 468–489. Oxford University Press, Oxford. Ericson, P.G.P., Anderson, C.L., Britton, T., Elzanowski, A., Johansson, U.S., Kallerrsjo, M., Ohlson, J.I., Parsons, T.J., Zuccon, D. and Mayr, G. (2006) Diversification of Neoaves: integration of
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Joseph, L. (1989) Food-holding behaviour of some Australian parrots. Corella 13: 143–144.
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Cameron, M. (2005) Group size and feeding rates of Glossy Black-cockatoos in central New South Wales. Emu 105: 299–304.
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Cresswell, W. (1994) Song as a pursuit-deterrent signal, and its occurrence relative to other anti-predator behaviours of skylark (Alauda arvensis) and Merlin (Falco columbarius). Behavioural Ecology and Sociobiology 34: 217–223.
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Fjeldså, J. (1988) Comparative ecology of the Australasian Grebes (Aves: Podicipedidae). RAOU Report 54: 1–30.
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Aumann, T. (1990) Use of stones by the Black-breasted Buzzard Hamirostra melanosternon to gain access to egg contents for food. Emu 90: 141–144.
Hulsman, K. (1976) The robbing behaviour of terns and gulls. Emu 76: 143–149.
Debus, S. (1991) Further observations on the Blackbreasted Buzzard Hamirostra melanosternon using stones to break eggs. Australian Bird Watcher 14: 138–143.
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Hunt, G.R., Rutledge, R.B. and Gray, R.D. (2006) The right tool for the job: what strategy do wild New Caledonian crows use? Animal Cognition 9: 307–316.
Collins, B.G. and McNee, S. (1991) Resource partitioning within Australian nectarivorous bird communities. Acta XX Congressus Internationalis Ornithologica 2: 1166–1174. Ford, H.A. and Paton, D.C. (1982) Partitioning of nectar sources in an Australian honeyeater community. Australian Journal of Ecology 7: 149–159.
Thouless, C.R., Fanshawe, J.H. and Bertram, B.C.R. (1989) Egyptian vultures Neophron percnopterus and Ostrich Struthio camelus eggs – the origins of stonethrowing behaviour. Ibis 13: 9–15.
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Lambert, F. and Woodcock, M. (1996) Pittas, Broadbills and Asities. Pica Press, Sussex.
Watson, D.M. (1997) The importance of Mistletoe to the White-fronted Honeyeater Phylidonyris albifrons in Western Victoria. Emu 97: 174–177.
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Watson, M. (1969) Significance of antiphonal song in the Eastern Whipbird, Psophodes olivaceus. Behaviour 35: 157–178. White F.W.G. (1987) A comparison of the whip-crack calls of the Olive Whistler and Eastern Whipbird. Australian Bird Watcher 12: 28–29.
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Bock, W.J. and Clench, M. H. (1985) Morphology of the Noisy Scrub-bird, Atrichornis clamosus (Passeriformes: Atrichornithidae): systematic relationships and summary. Records of the Australian Museum 37: 243–254.
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Smith, G.T. (1976) Ecological and behavioural comparisons between the Atrichornithidae and the Menuridae. In Proceedings of the 16th International Ornithological Congress. (Eds H.J. Frith and J.H. Calaby) pp. 125–136. Australia Academy of Sciences, Canberra.
Rowley, I. (1973) The comparative ecology of Australian corvids. VI. Why five species? CSIRO Wildlife Research 18: 157–169.
Page 151: Group chorister
Smith, G.T. (1977) The effect of environmental change on six rare birds. Emu 77: 173–179.
Boles, W.E. (1977) Aggressive display in two species of chowchillas (logrunners). Corella 1: 38. Hindwood, K.A. (1934) The Spine-tailed Log-runner (Orthonyx temminckii). Emu 33: 257–267.
Page 156: The song and dance man Marshall, A.J. (1950) Function of vocal mimicry in birds. Emu 50: 5–16.
McNamara, E. (1934) Observations on the habits of the Spine-tailed Log-runner. Emu 34: 177–180.
Powys, V. (1995) Regional variation in the territorial songs of superb lyrebirds in the central tablelands of New South Wales. Emu 95: 280–289.
Page 152: A cracking duo Hall, M.L. (2009) A review of vocal duetting in birds. Advances in the Study of Behaviour 40: 47–121.
Putland, D.A., Nicholls, J.A., Noad, M.J. and Goldizen, A.W. (2006) Imitating the neighbours: vocal dialect matching in a mimic-model system. Biology Letters 2: 367–370.
Pizzey, G. and Knight, F. (1997) Field Guide to the Birds of Australia. Angus and Robertson, Sydney. 276
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Page 166: Familiarity pays
Robinson, F.N. and Curtis, H.S. (1996) The vocal displays of the lyrebirds (Menuridae). Emu 96: 258–275.
Bradley, J.S., Wooller, R.D. and Skira, I.J. (1995) The relationship of pair-bond formation and duration to reproductive success in Short-tailed Shearwaters Puffinus tenuirostris. Journal of Animal Ecology 64: 31–38.
Page 158: Polygynous posers Frith, C.B. and Beehler, B.M. (1998) The Birds of Paradise: Paradisaeidae. Oxford University Press, Melbourne. Irestedt, M., Jønsson, K.A., Fjeldså, J., Christidis, L. and Ericson, P.G.P. (2009) An unexpectedly long history of sexual selection in birds-of-paradise. BMC Evolutionary Biology 9: 235–246.
Bradley, J.S., Wooller, R.D., Skira, I.J. and Serventy, D.L. (1990) The influence of mate retention and divorce upon reproductive success in Short-tailed Shearwaters Puffinus tenuirostris. Journal of Animal Ecology 59: 487–496.
Page 160: Signaling maturity
Wooller, R.D., Bradley, J.S., Skira, I.J. and Serventy, D.L. (1989) Short-tailed Shearwater. In Lifetime Reproduction in Birds. (Ed. I. Newton) pp. 405–411. Academic Press, London.
Burger, A.E. (1980) Sexual size dimorphism and aging characters in the Lesser Sheathbill at Marion Island. Ostrich 51: 39–43. Shaw, P. (1986) The relationship between dominance behaviour, bill size and age group in Greater Sheathbills Chionis alba. Ibis 128: 48–56.
Page 170: Boom box territoriality Coddington, C.L. and Cockburn, A. (1995) The mating system of free-living Emus. Australian Journal of Zoology 43: 365–372.
Page 161: Staking a claim Burger, A.E. (1980) An analysis of the displays of Lesser Sheathbills Chionis minor. Zeitschrift für Tierpsychologie 52: 381–396.
Page 171: Male–female dynamics Brennan, P.L.R., Clark, C.J. and Prum, R.O. (2010) Explosive eversion and functional morphology of the duck penis supports sexual conflict in waterfowl genitalia. Proceedings of Royal Society of London B 277: 1309–1314.
Page 164: Boom and bust shorebird style Goodsell, J.T. (1990) Distribution of waterbird broods in relation to the wetland salinity and pH in southwestern Australia. Australian Wildlife Research 17: 219–229.
Brennan, P.L.R., Prum, R.O., McCracken, K.G., Sorenson, M.D., Wilson, R.E. and Birkhead, T.R. (2007) Coevolution of male and female genital morphology in waterfowl. PLoS ONE 2(5): e418.
Mayr, G. (2004) Morphological evidence for sister group relationship between flamingos (Aves: Phoenicopteridae) and grebes (Podicipedidae). Zoological Journal of the Linnean Society 140: 157–169.
Briskie, J.V. and Montgomerie, R. (1997) Sexual selection and the intromittent organ of birds. Journal of Avian Biology 28: 73–86.
Olson, S. and Feduccia, A. (1980) Relationships and evolution of flamingos (Aves: Phoenicopteridae). Smithsonian Contributions to Zoology 316: 1–73.
Caizergues, A. and Lambrechts, M.M. (2001) Male ‘macho’ mammals exploiting females versus male ‘Don Juan’ birds exploited by females: the oppositesex exploitation (OSEX) theory. Ecology Letters 2: 204–206.
Storer, R.W. (2006) The grebe–flamingo connection: A rebuttal. Auk 123: 1183–1184. 277
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Page 173: The scented powderpuff
Tropicbirds (Phaethon rubricauda) as inferred from patterns of variation. Auk 120: 1033–1043.
Guay, P.-J. and Mulder, R.A. (2007) Skewed paternity distribution in the extremely size dimorphic Musk Duck (Biziura lobata) Emu 107: 190–195.
Kraaijeveld, K., Kraaijeveld-Smit, F.J.L. and Komdeur, J. (2007) The evolution of mutual ornamentation. Animal Behaviour 74: 657–677.
McCracken, K.G., Paton, D.C. and Afton, A.D. (2000) Sexual size dimorphism in the Musk Duck. Wilson Bulletin 112: 457–466.
Veit, A.C. and Jones, I.L. (2004) Patterns of growth of Red-tailed Tropicbird Phaethon rubricauda tail streamer ornaments. Ibis 146: 355–359.
Page 174: A long engagement
Page 180: The ballet dancer
Jouventin, P., Lequette, B. and Dobson, S. (1999) Agerelated mate choice in the wandering albatross. Animal Behaviour 57: 1099–1106.
Johnsgard, P.A (1983) Cranes of the World. Indiana University Press, Bloomington.
Lequette, B. and Jouventin, P. (1991) The dance of the Wandering Albatross II: acoustic signals. Emu 91: 172–178.
Page 182: Bow coo Frith, H.J. (1977) Some display postures of Australian pigeons. Ibis 119: 167–182.
Lequette, B. and Weimerskirch, H. (1990) Influence of parental experience on the growth of Wandering Albatross chicks. Condor 92: 726–731.
Frith, H. (1982) Pigeons and Doves of Australia. Rigby Publishers, Adelaide. Higgins, P.J. and Davies, S.J.J.F. (Eds) (1996) Handbook of Australian, New Zealand and Antarctic Birds. Vol. 3: Snipe to Pigeons. Cambridge University Press, Melbourne.
Tomkins, R.J. (1984) It’s great to be alive, especially on Macquarie Island. Tasmanian Naturalist 79: 24–32.
Page 175: Breeding seasons’ greetings
Whitman, C. O. and Riddle, O. (Eds) (1919) The Posthumous Works of Charles Otis Whitman. Carnegie Institution, Washington.
Nelson, J.B. (2005) Pelicans, Cormorants, and Their Relatives: The Pelecaniformes. Bird Families of the World, 17. Oxford University Press, Oxford.
Page 184: True blue Lotharios
Page 176: You are my Valentine
Dunn, P.O. and Cockburn, A. (1999) Extra-pair mate choice and honest signalling in cooperatively breeding Superb Fairy-wren. Evolution 53: 938–946.
Nelson, J.B. (2005) Pelicans, Cormorants, and Their Relatives: The Pelecaniformes. Bird Families of the World, 17. Oxford University Press, Oxford.
Green, D.G., Osmond, H.L., Double, M.C. and Cockburn, A. (2000) Display rate by male fairy-wrens (Malurus cyaneus) during the fertile period of females. Behavioural Ecology and Sociobiology 48: 438–446.
Page 177: Do you think I’m sexy? Nelson, J.B. (2005) Pelicans, Cormorants, and Their Relatives: The Pelecaniformes. Bird Families of the World, 17. Oxford University Press, Oxford.
Kingma, S.A., Hall, M.L., Segelbacher, G. and Peters, A. (2009) Radical loss of an extreme extra-pair mating system. BMC Ecology 9: 15.
Page 178: Mutual attraction
Rowley, I. (1991) Petal-carrying by fairy-wrens of the genus Malurus. Australian Bird Watcher 14: 75–81.
Jones, I.L. (2003) Function of tail streamers of Red-tailed 278
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Page 188: Architects are smarter
Rowley, I. and Russell, E. (1990) ‘Philandering’ – a mixed mating strategy in the Splendid Fairy-wren Malurus splendens. Behavioural Ecology and Sociobiology 27: 431–437.
Borgia, G. and Mueller, U. (1992) Bower destruction, decoration stealing and female choice in the Spotted Bowerbird Chlamydera maculata. Emu 92: 11–18. Day, L.B., Westcott, D.A. and Olster, D.H. (2005) Evolution of bower complexity and cerebellum size in bowerbirds. Brain, Behaviour and Evolution 66: 62–72.
Page 185: Playing hard to get Doerr, E.D. and Doerr,V.A.J. (2007) Positive effects of helpers on reproductive success in the brown treecreeper and the general importance of future benefits. Journal of Animal Ecology 76: 966–976.
Frith, C.B. and Frith D.W. (2004) The Bowerbirds: Ptilorhynchidae. Oxford University Press, Oxford. Gilliard, E.T. (1959) A comparative analysis of courtship movements in closely affiliated bowerbirds of the genus Chlamydera. American Museum Novitates 1936: 1–7.
Doerr, E.D. and Doerr,V.A.J. (2006) Comparative demography of treecreepers: evaluating hypotheses for the evolution and maintenance of cooperative breeding. Animal Behavior 72: 147–159.
Gilliard, E.T. (1969) Birds of Paradise and Bower Birds. Weidenfeld and Nicolson, London. Madden, J. (2001) Sex, bowers and brains. Proceedings of the Royal Society of London 268: 833–838.
Page 186: The importance of ritual Zann, R. (1976) Inter- and intraspecific variation in the courtship of three species of grassfinches of the subgenus Poephila (Gould) (Estrildidae). Zeitschrift für Tierpsychologie 41: 409–433.
Madden, J. (2003) Preference for coloured bower decorations can be explained in a nonsexual context. Animal Behaviour 64: 1077–1083. Mikami, O.K., Katsumo, Y., Yamashita, D.M., Noske, R. and Eguchi, K. (2010) Bowers of Great Bowerbird (Chlamydera nuchalis) remained unburned after fire: is this an adaptation to fire? Journal of Ethology 28: 15–20.
Zann, R. (1977) Pair-bond and bonding behaviour in three species of grassfinches of the genus Poephila (Gould). Emu 77: 97–106.
Page 187: Life in the monogamy fast track Adkins-Regan, E. and Tomaszycki, M. (2007) Monogamy on the fast track. Biology Letters 3: 617–619. Goodson, J.L., Kabiluk, D., Kelly, A.M., Rinaldi, J. and Klatt, J.D. (2002) Midbrain dopamine neurons reflect affiliation phenotypes in finches and are tightly coupled to courtship. Proceedings of the National Academy of Sciences 106: 8737–8742.
Miles, A.J. and Madden, J.R. (2002) Bower location by the Spotted Bowerbird (Chlamydera maculata). Emu 102: 187–193.
Page 192: Why go to so much trouble? Borgia, G. (1997) Comparative behavioural and biochemical studies of bowerbirds, and the evolution of bower-building. In Understanding and Protecting Our Biological Resource. (Eds M.L. Reaka-Kudla, D.E. Wilson and E.O. Wilson) pp. 263–276. Joseph Henry Press, Washington.
Langmore, N.E. and Bennett, A.T.P. (1999) Strategic concealment of sexual identity in an estrildid finch. Proceedings of the Royal Society of London B 266: 543–550.
Borgia, G., Coyle, B. and Zwiers, P.B. (2007) Evolution of colourful display. Evolution 61: 708–712.
Zann, R. (1976) Distribution, status and breeding of Black-tailed finches Poephila cincta in northern Queensland. Emu 76: 201–206.
Endler, J.A., Endler, L.C. and Doer, N.R. (2010) Great Bowerbirds create theaters with forced perspective 279
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when seen by their audience. Current Biology 20: 1679–1684.
Page 200: Topped and tailed
Endler, J.A., Westcott, D.A., Madden, J.R. and Robson, T. (2005) Processing illuminates signal evolution animal visual systems and the evolution of colour patterns: sensory processing illuminates signal evolution. Evolution 59: 1795–1818. Frith, C.B. and Frith D.W. (2004) The Bowerbirds: Ptilorhynchidae. Oxford University Press, Melbourne. Gilliard, E.T. (1959) A comparative analysis of courtship movements in closely affiliated bowerbirds of the genus Chlamydera. American Museum Novitates 1936: 1–7. Gilliard, E.T. (1969) Birds of Paradise and Bower Birds. Weidenfeld and Nicolson, London.
Beruldsen, G. (2003) Australian Birds: Their Nests and Eggs. G. And E. Bruldsen, Kenmore Hills.
Page 201: What nest? Martin, T. (1995) Avian life history evolution in relation to nest sites, nest predation, and food. Ecological Monographs 65: 101–127.
Page 202: The fancy stitcher Bennett, P.M. and Owens, I.P.F. (2002) Evolutionary Ecology of Birds: Life Histories, Mating Systems, and Extinction. Oxford University Press, Oxford.
Page 203: An insect’s nest Page 194: Look at me
Legge, S. and Heinsohn, R. (2001) Kingfisher in paradise: the breeding biology of Tanysiptera sylvia at the Iron Range National Park, Cape York. Australian Journal of Zoology 49: 85–98.
Driskell, A.C. and Christidis, L. (2004) Phylogeny and evolution of the Australo-Papuan honeyeaters (Passeriformes, Meliphagidae). Molecular Phylogenetics and Evolution 31: 943–960.
Page 204: The bottle-builder
Goodwin, D. (1967) Notes on behaviour of some Australian birds. Emu 66: 237–251.
Gould, J. (1865) Handbook to the Birds of Australia. Vol. 1. The Author, London.
Williams, C.K. and Main, A.R. (1979) Ecology of Australian chats (Epthianura Gould). Australian
Page 198: Designed by the same architect
Hammers, M., von Engelhardt, N., Langmore, N.E., Komdeur, J., Griffith, S.C. and Magrath, M.J.L. (2009) Mate-guarding intensity increases with breeding synchrony in the Fairy Martin, Petrochelidon ariel. Animal Behaviour 78: 661–669.
Collias, N.E. (1997) On the origin and evolution of nest building by passerine birds. Condor 99: 253–270.
Hyett, J. (1980) Squatters in the nests of Fairy Martins. Australian Bird Watcher 8: 247–248.
Hansell, M.H. (2000) Bird Nests and Construction Behaviour. Cambridge University Press, Cambridge.
Manwell, C. and Baker, C.M.A. (1975) Molecular genetics of avian proteins. XIII. Protein polymorphism in three species of Australian passerines. Australian Journal of Biological Science 28: 545–557.
Journal of Zoology 27: 213–229.
Winkler, D.W. and Sheldon, F.H. (1993) Evolution of nest construction in swallows (Hirundinidae): a molecular phylogenetic perspective. Proceedings of the National Academy of Sciences USA 90: 5705–5707.
Tarburton, M.K. (1991) Breeding biology of Fairy Martins at Murwillumbah. Emu 91: 93–99.
Zyskowski, K. and Prum, R. (1999) Phylogenetic analysis of the nest architecture of Neotropical ovenbirds (Furnariidae). Auk 116: 891–911.
Page 205: Bees and burrows Boland, C.R.J. (2004) Breeding biology of Rainbow 280
Further reading
Bee-eaters (Merops ornatus): a migratory, colonial, cooperative bird. Auk 121: 811–823.
Cockburn, A. (2006) Prevalence of different modes of parental care in birds. Proceedings of the Royal Society of London B 273: 1375–1383.
Fry, C.H. (1984) The Bee-Eaters. Buteo Books, South Dakota. Fry, C.H., Fry, K. and Harris, A. (1999) Kingfishers, Beeeaters and Rollers. Christopher Helm, London.
Frith, H.J. (1985) Megapode. In A Dictionary of Birds. (Eds B. Campbell and E. Lack) pp. 344–345. Poyser, Calton.
Page 207: Interlude
Jones, D. and Göth, A. (2008) Mound-builders. CSIRO Publishing, Collingwood.
Cockburn, A. (2003) Cooperative breeding in oscine passerines: does sociality inhibit speciation? Proceedings of the Royal Society of London B 270: 2207–2214.
Page 215: Is it a boy or girl? Goth, A. and Booth, D.T. (2005) Temperature-dependent sex ratio in a bird. Biological Letters 1: 31–33.
Page 210: Hot-footed
Komdeur, J. (2003) Daughters on request: about helpers and egg-sex in the Seychelles warbler. Proceedings of the Royal Society of London B 270(1510): 3–11.
Morgan, S.M., Ashley-Ross, M.A. and Anderson, D.J. (2003) Foot-mediated incubation: Nazca Booby (Sula granti) feet as surrogate brood patches. Physiological and Biochemical Zoology 76: 360–366.
Page 216: A head start in the arms race Brooker, M.G. and Brooker, L.C. (1989) The comparative breeding behaviour of two sympatric cuckoos, Horsfield’s Bronze-Cuckoo Chrysococcyx basalis and the Shining Bronze-Cuckoo C. lucidus, in Western Australia: a new model for the evolution of egg morphology and host specificity in avian brood parasites. Ibis 131: 528–547.
Page 211: Saliva nests and egg-incubating chicks del Hoyo, J., Elliott, A and Sargatal, J. (Eds) (1999) Handbook of the Birds of the World. Vol. 5. Barn-Owls to Hummingbirds. Lynx Edicions, Barcelona. Johnston, D.W. (1958) Sex and age characters and salivary glands of the Chimney Swift. Condor 60: 73–84. Marshall, A.J. and Folley, S.J. (1956) The origin of nest-cement in edible-nest swiftlets (Collocalia spp.). Proceedings of the Zoological Society of London 126: 383–389.
Brooker, M.G. and Brooker, L.C. (1996) Acceptance by the Splendid Fairy-wren of parasitism by Horsfield’s Bronze-cuckoos: further evidence for evolutionary equilibrium in brood parasitism. Behavioural Ecology 7: 395–407.
Tarburton, M. (1986) Breeding of the White-rumped Swiflet in Fiji. Emu 86: 214–227.
Davies, N.B. (2000) Cuckoos, Cowbirds and Other Cheats. Poyser, London.
Tarburton, M. (2003) The breeding biology of the Mountain Swiftlet (Aerodramus hirundinaceus) in Irian Jaya. Emu 103: 177–182.
Langmore, N.E. and Kilner, R.M. (2010) The coevolutionary arms race between Horsfield’s BronzeCuckoos and Superb Fairy-wrens. Emu 110: 32–38.
Page 213: A bun in the oven
Liversidge, G. (1961) Pre-incubation development of Clamator jacobinus.Ibis 103: 624.
Clutton-Brock, T. H. (1991) The Evolution of Parental Care. Princeton University Press, New Jersey.
Payne, R.B. (1977) The ecology of brood parasitism in birds. Annual Review of Ecology and Systematics 8: 1–28. 281
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Page 217: Helpless hatchlings
Page 221: Taking them under his wing
Cameron, M. (2007) Cockatoos. CSIRO Publishing, Collingwood.
Emlen, S. and Wrege, P. (2004) Size dimorphism, intrasexual competition, and sexual selection in Wattled Jacana (Jacana jacana), a sex-role-reversed shorebird in Panama. Auk 121: 391–403.
Krebs, E. (2002) Sibling competition and parental control: patterns of begging in parrots. In The Evolution of Begging: Competition, Cooperation and Communication. (Eds J. Wright and M.L. Leonard) pp. 319–336. Springer, Netherlands.
Emlen, S. and Wrege, P. (2004) Division of labour in parental care behaviour of a sex-role-reversed shorebird, the wattled jacana. Animal Behavior 68: 847–855.
Rowley, I. and Chapman, G. (1991) The breeding biology, food, social organisation, demography and conservation of the Major Mitchell or Pink Cockatoo, Cacatua leadbeateri, on the margin of the Western Australian wheatbelt. Australian Journal of Zoology 39: 211–261.
Garul, W.D., Derrickson, S.R. and Mock, D.W. (1977) The evolution of avian polyandry. The American Naturalist 111: 812–816. Gowatry, P.A. (1981) An extension of the Orians-VernerWillson model to account for mating systems other than polygyny. The American Naturalist 118: 851–859.
Sindell, S. and Lynn, R. (1989) Australian Cockatoos: Experiences in the Field and Aviary. Singil Press, Sydney.
Mace, T. (2000) Time budget and pair-bond dynamics in the Comb-crested Jacana Irediparra gallinacea: a test of hypotheses. Emu 100: 31–41.
Page 218: Coping with extremes
Page 223: Cream of the crop
Amat, J.A. and Maero, J.A. (2007) The functions of bellysoaking in Kentish Plovers Charadrius alexandrinus. Ibis 149: 91–97.
Blockstein, D.E. (1989) Crop milk and clutch size in Mourning Doves. Wilson Bulletin 101(l): 11–25.
Grant, G.S. (1982) Avian incubation: temperature, nest humidity, and behavioural thermoregulation in a hot environment. Ornithological Monographs 30. American Ornithologists’ Union,Washington.
Horseman, N.D. and Buntin, J.D. (1995) Regulation of pigeon cropmilk secretion and parental behaviors by prolactin. Annual Review of Nutrition 15: 213–238. Klasing, K.C. (1998) Comparative Avian Nutrition. CAB International, Wallingford.
Maclean, G.L. (1975) Belly-soaking in the Charadriiformes. Bombay Natural History Society 72: 74–82.
Page 224: Toilet trained
Maclean, G. L. (1976) A field study of the Australian Pratincole. Emu 76: 171–182.
Dell’Omo, G., Alleva, E. and Carere, C. (1998) Parental recycling of nestling faeces in the common swift. Animal Behaviour 56: 631–637.
Page 220: A crown of thorns or a larder?
McGowan, K.J. (1995) A test of whether economy or nutrition determines fecal sac ingestion in nesting corvids. Condor 97: 50–56.
Chisholm, A.H. (1918) Birds and caterpillars. Emu 18: 75–76. Chisholm, A.H. (1919) Bell-birds and caterpillars. Emu 18: 295–297.
Petit, K.E., Petit, L. J. and Petit, D.R. (1989) Fecal sac removal: do the pattern and distance of dispersal affect the chance of nest predation? Condor 91: 479–482.
Ross, J.A. (1930) Crested Bell-bird. Emu 29: 174. 282
Further reading
Skutch, A.F. (1976) Parent Birds and Their Young. University of Texas Press, Austin.
Redondo, T. and Castro, F. (1992) The increase in risk of predation with begging activity in broods of magpies Pica pica. Ibis 134: 180–187.
Welty, J.C. and Baptista, L. (1988) The Life of Birds. Saunders College, New York.
Page 229: Bright little beggars
Page 225: A face only a father could love
Hunt, S., Kilner, R.M., Langmore, N.E. and Bennett, A.T.D. (2003) Conspicuous, ultraviolet-rich mouth colours in begging chicks. Proceedings of the Royal Society of London B Supplement 270: s25–s28.
Higgins, P.J. (Ed.) (1999) Handbook of Australian, New Zealand and Antarctic Birds, Volume 4. Parrots to Dollarbird. Oxford University Press, Melbourne.
Immelmann, K. (1965) Australian Finches. Angus and Robertson, Sydney.
Kilner, R.M. (2006) Function and evolution of color in young birds. In Bird Coloration: Function and Evolution, Vol. 2. (Eds G.E. Hill and K.J. McGaw) pp. 201–232. Harvard University Press, Cambridge.
Page 230: Cooperative killers
Maurer, G. (2008) Who cares? Males provide most parental care in a monogamous nesting cuckoo. Ethology 114: 540–547.
Pinson, D. and Drummond, H. (1993) Brown Pelican siblicide and the prey-size hypothesis. Behavioral Ecology and Sociobiology 32: 111–118.
Tanner, M. and Richner, H. (2008) Ultraviolet reflectance of plumage for parent-offspring communication in the Great Tit (Parus major). Behavioral Ecology 19: 369–373.
Vestjens, J.W.M. (1977) Breeding behaviour of the Australian Pelican, Pelecanus conspicillatus in New South Wales. Australian Wildlife Research 4: 37–58.
Taplin, A. and Beurteaux, Y. (1992) Aspects of the breeding biology of the Pheasant Coucal Centropus phasianinus. Emu 92: 141–146.
Page 232: Killer babies and insurance eggs Mazuc, J., Bonneaud, C., Chastel, O. and Sorci, G. (2003) Social environment affects female and egg testosterone levels in the House Sparrow. Ecology Letters 6: 1084–1090.
Page 228: Balanced begging Briskie, J.V., Martin, P.R. and Martin, T.E. (1999) Nest predation and the evolution of nestling begging calls. Proceedings of the Royal Society of London B 266: 2153–2159.
Page 233: Cheaters versus cheated and odd couples Brooker, L.C. and Brooker, M.G. (1990) Why are cuckoos host specific? Oikos 57: 301–309.
Haskell, D. (1994) Experimental evidence that nestling begging incurs a cost due to nest predation. Proceedings of the Royal Society of London B 1349: 161–164.
Davies, N.B. (2000) Cuckoos, Cowbirds and Other Cheats. Poyser, London. Grim, T. (2006) Low virulence of brood parasitic chicks: adaptation or constraint? Ornithological Science 5: 237–242.
Haskell, D. G. (2002) Begging behaviour and nest predation. In The Evolution of Begging. (Eds J. Wright and M.L. Leonardo) pp. 162–172. Springer, The Netherlands.
Kilner, R.M. (2005) The evolution of virulence in brood parasites Ornithological Science 4(1): 55–64.
Hinde, C.A., Buchanan, K.L. and Kilner, R.M. (2009) Prenatal environmental effects match offspring begging to parental provisioning. Proceedings of the Royal Society of London B 276: 2787–2794.
Kilner, R.M., Madden, J.R. and Hauber, M.E. (2004) Brood parasitic cowbird nestlings use host young to procure resources. Science 305: 877–879. 283
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Langmore, N.E., Hunt, S. and Kilner, R.M. (2003) Escalation of a co-evolutionary arms race through host rejection of brood parasitic young. Nature 422: 157–160.
Brown, J.L., Dow, D.D., Brown, E.R. and Brown, S.D. (1978) Effects of helpers on feeding of nestlings in the Grey-crowned Babbler (Pomatostomus temporalis). Behavioural Ecology and Sociobiology 4: 43–59.
Page 238: Sociality for survival
Page 243: Red-eyed kidnapper
Boland, C.R.J., Heinsohn, R. and Cockburn, A. (1997) Deception by helpers in cooperatively breeding Whitewinged Choughs and its experimental manipulation. Behavioral Ecology and Sociobiology 41: 251–256.
Baldwin, M. (1971) Group movements of the Whitewinged Chough. Australian Bird Watcher 4: 69–76.
Chapman, G. (1998) The social life of the Apostlebird. Emu 98: 178–183.
Heinsohn R. (1991) Kidnapping and reciprocity in cooperatively breeding White-winged Choughs. Animal Behaviour 41: 1097–1100. Rowley, I. (1978) Communal activities among Whitewinged Chough Corcorax melanocephalus. Ibis 120: 178–197.
Noske, R. (1985) Huddle-roosting behaviour of the Varied Sittella Daphoenositta chrysoptera in relation to social status. Emu 85: 188–194.
Page 244: Waiting in the wings
Noske, R. (1998) Social organization and nesting biology of the cooperative-breeding Varied Sittella Daphoenositta chrysoptera in north-eastern New South Wales. Emu 98: 85–96.
Legge, S. (2004) Kookaburra: King of the Bush. CSIRO Publishing, Collingwood. Parry, V.A. (1970) Kookaburras. Lansdowne Press, Melbourne.
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Reyer, H.-U. and Schmidl, D. (1988) Helpers have little to laugh about: group structure and vocalisation in the Laughing Kookaburra Dacelo novaeguineae. Emu 88: 150–160.
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Blackmore, C.J. and Heinsohn, R. (2007) Reproductive success and helper effects in the cooperatively breeding Grey-crowned Babbler. Journal of Zoology 273: 326–332.
Garnett, S.T. (1978) The behaviour patterns of the Dusky Moorhen, Gallinula tenebrosa Gould (Aves: Rallidae). Australian Wildlife Research 5: 363–384. Garnett, S.T. (1980) The social organisation of the Dusky Moorhen Gallinula tenebrosa Gould (Aves: Rallidae). Australian Wildlife Research 7: 103–112.
Blackmore, C.J. and Heinsohn, R. (2008) Variable mating strategies and incest avoidance in cooperatively breeding grey-crowned babblers. Animal Behaviour 75: 63–70.
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Brown, J.L. and Balda, R.P. (1977) The relationship of habitat quality to group size in Hall’s Babbler (Pomatostomus halli). Condor 79: 312–320.
Geiser, F., Körtner, G. and Maddocks, T.A. (2006) Torpor in Australian birds. Acta Zoologica Sinica 52: 405–408.
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Reid, N. (1991) Coevolution of mistletoes and frugivorous birds? Australian Journal of Ecology 16: 457–469.
Kikkawa, J. (1987) Social relations and fitness in silvereyes. In Animal Societies: Theories and Facts. (Eds Y. Ito, J.L. Brown and J. Kikkawa) pp. 253–256. Japan Scientific Society, Tokyo.
Richardson, K.C. and Wooller, R.D. (1988) The alimentary tract of a specialist frugivore, the Mistletoebird, Dicaeum hirundinaceum, in relation to its diet. Australian Journal of Zoology 36: 373–382.
Lewis, S., Roberts, G., Harris, M., Prigmore, C. and Wanless, S (2007) Fitness increases with partner and neighbour allopreeening. Biology Letters 3: 386–389.
Watson, D.M. (2002) Effects of mistletoe on diversity: a case-study from New South Wales. Emu 102: 275–281. Watson, D.M. (2011) Mistletoes of Southern Australia. CSIRO Publishing, Collingwood.
Page 250: Troop fishing Anderson, J.G.T. (1991) Fishing behaviour of the American White Pelican (Pelecanus erythrorhynchos) in western Nevada. Colonial Waterbirds 14: 166–172.
Page 258: Pest control Clark, L.R. (1964) The population dynamics of Cardiaspina albitextura (Psyllidae). Australian Journal of Zoology 12: 362–380.
Page 254: A one-sided affair? Hickey, G. (1995) The platypus and the kingfisher. Nature Australia 25(2): 18. Troughton, G.J. and Wray, S. (1994) An apparent feeding association between the Azure Kingfisher Ceyx azurea and the Platypus Ornithorhynchus anatinus. Sunbird 24: 45.
Page 255: Lured into the shadows
Paton, D.C. (1980) The importance of manna, honeydew and lerp in the diet of honeyeaters. Emu 80: 213–226. Woinarski, J.C.Z. (1983) Small birds, lerp-feeding and the problem of honeyeaters. Emu 84: 137–141. Woinarski, J.C.Z. (1983) Patterns of ecological segregation among forest and woodland birds in south-eastern Australia. Ornithological Science 1: 7–27. Woinarski, J.C.Z. (1989) Some life history comparisons of small leaf-gleaning birds of south-eastern Australia. Corella 13: 73–80.
Brown, L.H., Urban, E.K. and Newman, K. (1980) The Birds of Africa. Volume 1. Academic Press, London. Grubb, T.C. (1976) Adaptiveness of foraging in the Cattle Egret. Wilson Bulletin 88: 145–148.
Page 259: Looking after trees?
Heatwole, H. (1965) Some aspects of the association of Cattle Egrets with cattle. Animal Behaviour 13: 79–83.
Clarke, M.F. and Schedvin, N. (1999) Removal of Bell Miners Manorina melanophrys from Eucalyptus radiata forest and its effects on avian diversity, psyllids and tree health. Biological Conservation 88: 110–120.
McKilligan, N.G. (1984) The food and ecology of the Cattle Egret, Ardea ibis, when nesting in south-east Queensland. Australian Wildlife Research 11: 133–144.
Clarke, M., Taylor, R., Oldland, J., Grey, M.G. and Dare, A. (2006) Dealing with indigenous despots. The State of Australia’s Birds report. Supplement to Wingspan 16(4): 26.
Page 256: Farming mistletoe? Reid, N. (1990) Mutualistic interdependence between mistletoes (Amyema quandang), and Spiny-cheeked Honeyeaters and Mistletoebirds in an arid woodland. Australian Journal of Ecology 15: 175–190.
Collins, B.G. and Spice, J. (1986) Honeyeaters and the pollination biology of Banksia prionotes (Protaeceae). Australian Journal of Botany 34: 175–185. 285
Stray Feathers
Collins, B.G., Newland, C. and Briffa, P. (1984) Nectar utilization and pollination by Australian honeyeaters and insects visiting Calothamnus quadrifidus (Myrtaceae). Australian Journal of Ecology 9: 353–365. Ford, H.A. and Paton, D.C. (1986) The Dynamic Partnership: Birds and plants in Southern Australia. Government Printer, Adelaide. Loyn, R.H. (1995). Bell Miners and the farming hypothesis – a comment. Emu 95: 145–146. Loyn, R.H., Runnals, R.G., Forward, G.Y. and Tyers, J. (1983) Territorial Bell Miners and other birds affecting populations of insect prey. Science 221: 1411–1413. Poiani, A. (1993). Bell Miners: what kind of farmers are they? Emu 93: 188–194. Stone, C. (2005) Bell-miner-associated dieback at the tree crown scale: a multi-trophic process. Australian Forestry 68: 237–241.
Page 261: Wrapping up Battley, P.F., Piersma, T., Dietz, M.W., Tang, S., Dekinga, A. and Hulsman, K. (2000) Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proceedings of the Zoological Society of London B 267: 191–195. Gill, R.E., Tibbitts, T.L., Douglas, D.C., Handel, C.M., Mulcahy, D.M., Gottschalck, J.C., Warnock, N., McCaffery, B.J., Battley, P.F. and Piersma, T. (2009) Extreme endurance flights by landbirds crossing the Pacific Ocean: ecological corridor rather than barrier? Proceedings of the Zoological Society of London B 276: 447–457.
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