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Research Institute for the Environment and Livelihoods
Interactions between
Brolgas and Sarus Cranes in Australia
Timothy Donnelly NEVARD¹˒³ BSc Hons (Imperial College at Wye, University of London); MSc (Imperial College at Wye,
University of London).
Submission date 21st January 2019
For the degree of Doctor of Philosophy
Supervisors: Professor Stephen Garnett¹, Dr George Archibald CM²,
Professor Michael Lawes¹, succeeded by Dr Ian Leiper¹ July 2017.
¹Research Institute for the Environment and Livelihoods,
Charles Darwin University, Darwin, NT 0909
²International Crane Foundation, E11376 Shady Lane Road, Baraboo, WI 53913, United
States
³Forever Wild (formerly Wildlife Conservancy of Tropical Queensland), C/- PO Box 505,
Ravenshoe, QLD 4888
2
DEDICATION
This thesis is dedicated to my wife Gwyneth, who cautioned against starting and predicted I’d
never finish…so is as surprised as me.
3
TABLE OF CONTENTS
Page
DEDICATION 2
TABLE OF CONTENTS 3
ABSTRACT 7
CANDIDATE’S DECLARATION 9
AUTHOR CONTRIBUTIONS TO PUBLISHED PAPERS 10
ACKNOWLEDGEMENTS 13
LIST OF TABLES 15
LIST OF FIGURES 17
LIST OF ABBREVIATIONS 20
CHAPTER 1 – INTRODUCTION, LITERATURE REVIEW AND THESIS
STRUCTURE 21
1.1 Preamble 21
1.2 A Paleoenvironmental Context 22
1.3 Agriculture and Biodiversity 23
1.4 Agricultural Sustainability 26
1.5 Agriculture and Cranes 28
1.6 Australian Cranes 31
1.6.1 The Brolga 32
1.6.2 The Australian Sarus Crane 34
1.6.3 The ‘Sarolga’ 35
1.6.4 The Conservation Status of Australian Cranes 36
1.7 Research Questions and Thesis Structure 36
4
1.7.1 Research Questions 37
1.7.2 Thesis Structure 38
CHAPTER 2 – STUDY AREA AND METHODS 41
2.1 Study Area and Geographical Scope 41
2.2 Methodology 43
CHAPTER 3 - THE AUSTRALIAN SARUS CRANE 48
3.1 Abstract 48
3.2 Introduction 48
3.3 Methods 53
3.3.1 Samples 53
3.3.2 Extraction 56
3.3.2.1 Nuclear DNA 56
3.3.2.2 Mitochondrial DNA 57
3.3.3 Statistical Analysis 58
3.3.3.1 Nuclear DNA 58
3.3.3.2 Mitochondrial DNA 59
3.4 Results 59
3.5 Discussion 66
3.6 Conclusions and Recommendations 68
CHAPTER 4 – EXTENT AND TRAJECTORY OF INTROGRESSION 70
4.1 Abstract 70
4.2 Introduction 71
4.2.1 Background 71
4.2.2 The Brolga 75
4.2.3 The Australian Sarus Crane 76
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4.2.4 Aims 77
4.3 Methods 78
4.3.1 Field Observations and Sample Collection 78
4.3.2 Molecular Analysis 80
4.3.3 Lincoln Petersen Index 84
4.4 Results 84
4.4.1 Field Observations 84
4.4.2 Population Genetics 86
4.4.3 Lincoln Petersen Index 88
4.5 Discussion and Conclusions 89
CHAPTER 5 - RESOURCE PARTITIONING AND COMPETITION 94
5.1 Abstract 94
5.2 Introduction 95
5.3 Methods 97
5.3.1 Atherton Tablelands Study Area 97
5.3.2 Field Surveys 100
5.3.3 Data Analysis 100
5.4 Results 103
5.4.1 Temporal Patterns 103
5.4.2 Spatial Patterns 104
5.4.3 Habitat Use 107
5.4.4 Crop Seasonality 109
5.5 Discussion 110
5.6 Conservation Management 112
5.7 Conclusions and Recommendations 113
6
CHAPTER 6 - FARMER ATTITUDES 115
6.1 Abstract 115
6.2 Introduction 115
6.3 Study Area 119
6.4 Methods 121
6.5 Results 122
6.5.1 Primary Production on the Atherton Tablelands 122
6.5.2 Farmer Intentions and Attitudes 123
6.6 Discussion and Recommendations 127
6.6.1 Crane Management Options 130
6.6.2 Consequences of Failing to Conserve Cranes on the Atherton Tablelands 133
CHAPTER 7 –DISCUSSION 135
7.1 Introduction 135
7.2 Key Findings 137
7.3 Future Scenarios 142
CHAPTER 8 - CONCLUSIONS AND RECOMMENDATIONS 146
8.1 Conclusions 146
8.2 Recommendations 147
8.3 A Final Word 149
ACKNOWLEDGEMENT OF ASSISTANCE 150
APPENDIX – PERMITS, APPROVALS AND AUTHORITIES 152
BIBLIOGRAPHY 153
7
ABSTRACT
Brolgas and Sarus Cranes use agricultural lands on the Atherton Tablelands in Australia,
where they come into conflict with farmers. To help frame their conservation management,
this research investigates genetic, spatial, temporal and socioeconomic patterns.
Work on Brolga genetics (incorporating data from this research) which identifies only small
variation between northern and southern populations (exluding New Guinea) has recently
been published, so the genetic component of this thesis has focussed on the Australian Sarus
Crane. Analyses of 10 microsatellite loci and 49 mitochondrial control sequences have
established that it differs significantly from both South and South-east Asian subspecies. A
sample from the extinct Philippine subspecies also clustered with the Australian Sarus Crane,
hinting at its potential importance in relation to reintroduction to Luzon.
Early observations of suspected Brolga and Sarus Crane introgression coincided with
significantly increased opportunities for interaction when foraging on agricultural crops.
Bayesian clustering based on ten microsatellite loci has confirmed that Australian cranes
hybridise and that their hybrids are fertile. Genetic analyses have also provided definitive
evidence that Brolgas and Sarus cranes migrate between the Gulf Plains and Atherton
Tablelands.
Abundances of both species on the Atherton Tablelands were positively correlated, with
Sarus Cranes more abundant on fertile volcanic soils and Brolgas in outlying cropping areas,
closer to roost sites. Both occurred at their highest densities on cultivated land, as well as
harvested maize and peanut stubbles.
Farmers were interviewed to explore their current attitudes and future intentions towards
cranes. Most are beginning to reduce post-harvest crop residues and move to perennial crops;
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diminishing traditional crane foraging opportunities and increasing the potential for conflict
resulting from crane damage to new plantings. By creating specific foraging areas, crane
tourism could provide new feeding opportunities for cranes but as they are mobile and able to
take advantage of newly created cropping areas, abandonment of the Atherton Tablelands
Key Biodiversity Area is therefore also possible.
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CANDIDATE’S DECLARATION
I hereby warrant that this work contains no material which has been accepted for the award of
any other degree or diploma in any university or other tertiary institution and, to the best of
my knowledge and belief, contains no material previously published or written by another
person, except where due reference has been made in the text.
Whilst every reasonable effort has been made to gain permission and acknowledge the
owners of copyright material, I would be pleased to hear from any copyright owner who has
been omitted or incorrectly acknowledged.
I give consent to this copy of my thesis, when deposited in the University Library, being
made available for loan and photocopying online via the University’s Open Access repository
eSpace.
Signed by: Timothy Donnelly NEVARD Dated: 10th
August 2019
10
AUTHOR CONTRIBUTIONS TO PAPERS PUBLISHED AND
SUBMITTED FOR PUBLICATION
During the course of my research for this thesis, I led the preparation and submission of the
four papers for peer reviewed publication listed below. They respectively form the basis of
Chapters 3, 4, 5 and 6.
Publications:
1. Nevard, T.D., Haase, M., Archibald, G., M., Leiper, I., Van Zalinge, R., Purchkoon,
N., Siriaroonrat, B., Latt, T.N., Wink, M. and Garnett, S.T. (in press). Subspecies in
the Sarus Crane Antigone antigone revisited; with particular reference to the
Australian population. Submitted to PLOS ONE (26/17/2019).
2. Nevard, T., Haase, M., Archibald, G., Leiper, I. and Garnett, S.T. (2019). The
Sarolga: conservation implications of genetic and visual evidence for hybridization
between the Brolga Antigone rubicunda and the Australian Sarus Crane Antigone
antigone gillae. Oryx. doi:10.1017/S003060531800073X.
3. Nevard, T.D., Franklin D.C., Leiper, I., Archibald, G. and Stephen T. Garnett, S.T
(2019). Agriculture, Brolgas and Australian Sarus Cranes on the Atherton Tablelands,
Australia. Pacific Conservation Biology, doi:10.1071/PC18055.
4. Nevard, T., Leiper, I., Archibald, G and Garnett S (2018). Farming and cranes on the
Atherton Tablelands, Australia. Pacific Conservation Biology,
doi.org/10.1071/PC18055.
11
Nature and extent of the author’s intellectual contributions:
1. Nevard led the development of the research questions and collected/sourced samples
and data with the assistance of Haase, Archibald, Van Zalinge, Purchkoon,
Siriaroonrat, Latt and Wink. The University of Greifswald laboratory performed the
genetic analyses under the supervision of Haase. Nevard wrote the first draft of the
paper with input from Haase; revised with editorial input from Garnett, Archibald and
Leiper. Van Zalinge, Purchkoon, Siariaroonrat, Latt and Wink all provided minor
amendments. Nevard and Haase developed the tables. Nevard and Leiper developed
the maps.
2. Nevard led the development of the research questions and collected the data. Nevard
worked with Leiper on spatial data analyses. The University of Greifswald laboratory
performed the genetic analyses under the supervision of Haase. Nevard wrote the first
draft of the paper with input from Haase; revised with editorial input from Garnett,
Archibald and Leiper. Nevard and Haase developed the tables. Nevard and Leiper
developed the maps.
3. Nevard led the development of the research questions, collected the data and worked
with Franklin and Leiper on statistical analyses. Nevard wrote the first draft of the
paper with input from Franklin; revised with editorial input from Garnett, Archibald,
and Leiper. Nevard and Franklin developed the tables. Nevard and Leiper developed
the maps.
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4. Nevard led the development of the research questions, collected the data and worked
with Garnett and Leiper on data analyses. Nevard wrote the first draft of the paper
with input from Garnett; revised with editorial input from Garnett, Archibald and
Leiper. Nevard developed the tables. Nevard and Leiper developed the maps.
We confirm the candidate’s contribution to the abovementioned papers and consent to the
inclusion of these papers in this thesis.
Martin Haase Robert Van Zalinge
Stephen Garnett Nuchjaree Purchkoon
George Archibald Boripat Siriaroonrat
Ian Leiper Tin Nwe Latt
Don Franklin Michael Wink
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ACKNOWLEDGEMENTS
First and foremost, I would like to thank my supervisory team: Professor Stephen Garnett
(principal advisor), Dr George Archibald CM, Dr Ian Leiper and Professor Michael Lawes
(retired 2017). Without their dedicated professional and personal support, I would not have
been able to either envisage or complete this project. In this context, I would particularly like
to acknowledge Professor Garnett, who provided outstanding personal, academic and logistic
direction at every unforeseen turn in the road; and Dr Archibald, who has so generously
shared his unparalleled knowledge of cranes.
I would also like to especially thank Dr Martin Haase of the University of Greifswald, with
whom I have worked on cranes for many years and who, notwithstanding the ‘tyranny of
distance’, has provided unfailing insight and encouragement throughout. I would also like to
acknowledge Dr Don Franklin, who provided great support with statistical analyses.
There are so many other people with whom I have also shared my PhD journey. These
include: Elinor Scambler, Dr Graham Harrington, Ceinwen Edwards and Dr John Grant, who
have all generously shared their insights on cranes of the Atherton Tablelands and Gulf
Plains; Trevor Adil, who helped me break the ice with farmers on the Atherton Tablelands
Dr Barry Hartup, Yulia Momose, Dr Baz Hughes, Dr Geoff Hilton and Dr Inka Veltheim
who have all provided invaluable advice in relation to crane catching and banding techniques;
Yossi Leshem, who shared insights into crane-related tourism; Dr Adam Miller, who was a
great collaborator on Brolga genetics; Dr David Westcott and Adam McKeown of CSIRO,
who provided advice in relation to potential tracking; Silke Fregin, who has marvellously
managed a huge number of samples and complex lab work at the University of Greifswald;
Dr Annabelle Olsson, who facilitated veterinary health clearances; Robert Van Zalinge,
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Nuchjaree Purchkoon, Dr Boripat Sinaroonrat, Professor Michael Wink and Tin Nwe Latt
who gathered and contributed genetic samples from Sarus Cranes in S.E. Asia; Emily Imhoff
of Cincinnati Museum and Dr Chris Milensky, the Collections Manager of the Division of
Birds at the Smithsonian Institution, who single-mindedly tracked-down and sampled their
museum specimens; and U Win Naing Thaw (Director of the Myanmar Nature and Wildlife
Conservation Division) who facilitated the collection of Myanmar samples.
A big thank you also to Betsy Didrickson, who unfailingly sourced references and literature
from the International Crane Foundation library; Dr Kerryn Morrison, Dr Gopi Sundar,
Tanya Smith, Dr Claire Mirande, and other colleagues at the International Crane Foundation,
who provided fantastic advice on crane catching, sampling and counting techniques.
In relation to volunteer fieldworkers and landholders, I would like to thank Dr Ruairidh,
Harry and Bronwen Nevard, Stella and Jürgen Freund, Jess Harris, Baron Dominic and
Baroness Vera von Schwertzell, who good naturedly assisted with logistics and sample
collection, notwithstanding pre-dawn starts and cramped conditions in tiny hides; Hans
Rehme of Lemgo, who generously provided access to his outstanding global collection of
cranes; Tom and Tanya Arnold (Miranda Downs cattle station), the Waddell family
(Woodleigh cattle station), Terry Trantor and Nick Reynolds, Marg Atkinson and Greg
Jenkins, the Godfrey family and Fay Moller-Nielsen, who all provided unfettered access to
their farms and cattle properties; and Angela and Peter Freeman of Cairns Tropical Zoo and
the North Queensland Wildlife Trust, who generously provided access to their captive cranes,
as well as funding for laboratory analyses.
Last but not least my heartfelt thanks to the scores of other ‘craniacs’ who helped me to learn
more about these fantastic birds than I ever thought possible.
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LIST OF TABLES
Page
Chapter 3
Table 3.1: Sources of Sarus Crane DNA used in analyses 54
Table 3.2: Details of sample collections for Sarus Crane 54
Table 3.3: PCR specifications and diversity of microsatellite loci 60
Table 3.4: Cluster analyses 61
Chapter 4
Table 4.1: Reference birds 80
Table 4.2: PCR specifications and diversity of microsatellite loci 81
Table 4.3: The number (and percentage) of cranes observed across 46 sites on the
Atherton Tablelands 2013-2016 84
Table 4.4. Total number of cranes and proportion of juvenile cranes at sites dominated
by either Brolgas or Sarus Cranes 86
Chapter 5
Table 5.1: Area and value of agricultural production on the Atherton Tablelands,
Queensland 98
Table 5.2: Population and density of crane species by land use type 108
Table 5.3: Probabilities from modelling of crop preferences of two crane species 108
Table 5.4: Density of crane species in crop types on the Atherton Tablelands,
Queensland, during surveys from May to December from 2014-2016 109
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Chapter 6
Table 6.1: Agricultural production on the Atherton Tablelands, Queensland, in 2015;
sorted by area for and within each major type of agricultural activity and the intensity
of use by Brolgas and Sarus Cranes 122
Table 6.2: Returns from land on the Atherton Tablelands, Queensland; with different
intensities of dry season crane usage 123
Table 6.3: Landholder ranking of social issues 125
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LIST OF FIGURES
Page
Chapter 2
Fig. 2.1: Global distribution of Brolga Antigone rubicunda; Sarus Crane
Antigone antigone; and field data collection sites in northern Queensland 41
Fig. 2.2: Atherton Tablelands region; showing location, major settlements,
land use and Key Biodiversity Area 42
Chapter 3
Fig. 3.1: Global distribution of the Sarus Crane A. antigone; showing populations
and subspecies 50
Fig. 3.2: Extant Sarus Crane subspecies 52
Fig. 3.3: Bayesian cluster analyses of microsatellite data 62
Fig. 3.4: Phylogenetic tree for three subspecies of the Sarus Crane A. antigone;
based on mtDNA sequences resulting from Bayesian analysis 64
Fig. 3.5: TCS network for five populations of the Sarus Crane A. antigone;
based on mtDNA sequences compared to the Brolga A. rubicunda 65
Chapter 4
Fig. 4.1: Typical Brolga with unfledged chick (Gulf Plains); showing small
red skull-cap type comb, dark wattle and grey legs, with scalloped plumage 72
Fig. 4.2: Typical Australian Sarus Cranes with first year juvenile (Atherton
Tablelands); showing pink legs, red comb extending down the neck,
whitish crown and darker grey colour 73
Fig. 4.3: Global distribution of Brolga Antigone rubicunda; Sarus Crane
Antigone antigone; and field data collection sites in northern Queensland 74
18
Fig. 4.4: Heads and necks of typical species phenotypes and presumed hybrids 79
Fig. 4.5: Pie-charts showing general distribution and clustering of Brolga,
Sarus Crane and Sarolga; visually identified at 46 observation sites on the
Atherton Tablelands 2013-2016 85
Fig. 4.6: STRUCTURE plot with K = 2; showing admixture among a total
of 363 Brolgas and Sarus Cranes 87
Chapter 5
Fig. 5.1: Atherton Tablelands region; showing survey sites, irrigated
agriculture and the Atherton Tablelands Key Biodiversity Area 99
Fig. 5.2: Foraging site hotspot analysis; based on the percent of cranes that
were Brolgas or Sarus 105
Fig. 5.3: Species-specific crane densities at feeding sites; as a function of
distance to the nearest roost 106
Fig. 5.4: Mean density of Brolgas (a) and Sarus Cranes (b) at each survey site.
Roost locations are also presented, classified according to most prominent species
observed at each 106
Fig. 5.5: Regression tree habitat models for Sarus Crane and Brolga 107
Chapter 6
Fig 6.1: Brolgas feeding on volunteer peanuts in an irrigated winter wheat
crop at Innot Hot Springs, Atherton Tablelands, Queensland 117
Fig. 6.2: Pairs of Brolgas and Australian Sarus Cranes with cattle at Kaban,
Atherton Tablelands, Queensland 117
Fig. 6.3: Atherton Tablelands region; showing location, major settlements,
land use and Key Biodiversity Area 120
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Chapter 8
Fig. 8.1: Queensland Coat of Arms (with author endorsements) 149
20
LIST OF ABBREVIATIONS
ABBBS Australian Bird and Bat Banding Scheme
ACBPS Australian Customs and Border Protection Service
AMOVA Analysis of Molecular Variance
CDU Charles Darwin University
CYP Cape York Peninsula
GIS Geographic Information System
ICF International Crane Foundation
IUCN International Union for the Conservation of Nature
KBA Key Biodiversity Area
NMNH National Museum of Natural History
PCR Polymerase Chain Reaction
QP&WS Queensland Parks and Wildlife Service
RIEL Research Institute for the Environment and Livelihoods
USA United States of America
21
CHAPTER 1 – INTRODUCTION AND LITERATURE
REVIEW
1.1 Preamble
The 15 members of the bird family Gruidae - the cranes - are revered wherever they occur
through Asia, Africa, Europe and Australia (Von Treuenfels, 2006). Australia has two crane
species, the Brolga Antigone rubicunda and Australian Sarus Crane Antigone antigone gillae.
They are similar in appearance and sympatric, with the distribution of the Australian Sarus
Crane entirely overlapped by the much larger range of the Brolga (Menkhorst et al., 2017).
Both species breed in shallow swamps and feed in savanna grassland and on agricultural
lands, as well as occasionally interbreed. This raises questions about how they retain their
specific identities or whether they will continue to do so as the Australian environment
changes.
The Sarus Crane but not the Brolga also occurs in South and South-east Asia, where some
populations have been extirpated and others are declining. Globally the species is listed as
Vulnerable under the IUCN Red List (IUCN 2018). This means that the isolated Australian
population has substantial conservation significance. Not only might interactions with the
Brolga be affecting its prospects in Australia but so too might interactions with intensifying
agriculture. Most crane species have a close relationship with agriculture and the two
Australian cranes also used cultivated land when they encounter it.
In this thesis I throw light on some of these issues, including the relationship of the
Australian Sarus Crane to populations in Asia and its genetic relationship with the Brolga. I
analyse the interactions of both species with agriculture where they co-occur on the Atherton
Tablelands in north Queensland and explore the future of farming in the region through
22
interviews with farmers. On the basis of this research, I consider the long-term prospects for
cranes and provide recommendations for their conservation.
I explore below the paleoenvironmental context of northern Australia, as well as the global
development of agriculture and its increasing impact on wildlife. I then discuss increasing
research interest in sustainable agriculture and food security, before moving on to review the
impact of agriculture on cranes and providing an introduction to Australia’s cranes.
1.2 A Paleoenvironmental Context
Up until the arrival of European agriculture in the 19th
Century, Australia’s two cranes, the
Brolga Antigone rubicunda and Australian Sarus Crane Antigone antigone gillae, were
confined to savanna woodland and grassland and adapted to the wet-dry conditions of
Australia’s monsoonal north. At the time of lowest sea level during the last Ice Age
(Lambeck et al. 2002), a savanna corridor extended both north and south of the equator
across the Sunda Plain (Bird et al. 2005) a feature soon lost by rising sea levels and rainforest
expansion. This corridor ended not far north of the Pleistocene Lake Carpentaria, around
which there would have been savannas inhabited by megafauna including grazing and
browsing marsupials, fundamentally influencing the extent and quality of crane habitat across
the region.
The maximum extent of global ice caps between 18,000 and 15,000 years ago marked the
greatest extent of land in the Sunda and Sahul Shelves (White, 1997) and the high point of
continental aridity. Deglaciation was underway by 14,000 years ago and global sea levels
rose rapidly from 130 metres below current levels (at the 14,000 year glacial maximum) to 35
metres below current levels 10,000 years ago. During this approximately 4,000 year period,
hydrological stress declined, temperature variations were less limiting to biota and wind
23
regimes less forceful. The Carpentaria Basin was gradually invaded by rising seas between
12,000 and 8,000 years ago (Joseph et al. 2019), with full marine conditions established
about 8,000 years ago. The period 9,000 to 7,000 years ago was one of optimal rainfall and
temperature for the regional expansion of rainforest and diminishing wet savanna, with sea
levels peaking 5,500 to 5,000 years ago at between 1 and 2 metres above current levels.
Between 3,000 and 2,000 years ago a drier period, with reactivated hydrological stress,
characterised northern Australia (White, 1997). So, throughout the Holocene and the last half
of the Quaternary, Australia has been a land of drought-tolerant biota, which included
Australia’s two mobile and adaptable crane species.
These conditions would have especially determined the distribution of Brolgas, which
uniquely amongst cranes have a salt excreting gland (Hughes and Blackman, 1973); allowing
them to differentially exploit foraging opportunities in harsh brackish coastal environments
more hostile to Sarus Cranes, which do not posess salt glands. When observed in the same
area as Sarus Cranes, Brolgas favour deeper, generally coastal marshes (Walkinshaw, 1973).
Perhaps this is why the Australian population of Sarus Cranes, although long known to
Aboriginal people (Reardon, 2007), was not formally identified until 1964 (Gill, 1967) due to
their restricted distribution and small numbers. Perhaps recently expanding in numbers
because they had access to a suitably- modified savanna environment, biologically
engineered anew by a cattle-based grazing megafauna and the establishment of cultivation
and crops.
1.3 Agriculture and Biodiversity
The development of agriculture in Australia and its impact on biodiversity is recent and needs
to be considered against a global backdrop, with cultivation of domesticated cereal crops first
developing in Eurasia, Africa and North America from about 12,000 years ago (Roberts,
24
2017). In addition to providing food for humans, these crops also provided accessible and
energy-rich food for many bird species, including cranes. As well as the gradual development
of cropping, pastoralists actively managed the Eurasian steppe and African savannas for their
livestock; extensive natural grazing assemblages using prairie and arid grasslands in North
America and Australasia. The subsequent ‘Columbian exchange’ of crops and technology
between the Americas, Eurasia, Africa and Australasia (Nunn and Qian, 2010) introduced
crops such as maize and potatoes to Eurasian and African cranes and wheat, rice, millet,
sorghum and cattle grazing to cranes in North America. Australasian cranes were only
exposed to all of these cropping changes from the 19th
Century onwards.
The transition from agrarian to industrial economies had its origins in Britain and coincided
with rising human populations and rapid declines in natural habitats (Deane, 1979). By the
1930s the developing world was also gradually intensifying agricultural production, with
increases in cropped area, yields and mechanical harvesting increasing foraging opportunities
for cranes. However, this expansion also led to the loss both of wetland and grassland
habitats, contributing to the decline and sometimes the disappearance of crane populations
(Austin et al., 2018). Another consequence of industrialisation and intensification was a
concomitant change from nomadic to sedentary lifestyles in traditionally grassland areas such
as Mongolia, also fundamentally reshaping the landscape (Ilyashenko and King, 2018).
Notwithstanding that more intensive farming and higher yields may have prevented the
transformation of more than 80m ha of natural habitat to agriculture between 1960 and 2000
(Alexandratos and Bruinsma, 2012), expansion of cultivation has accelerated in the 21st
Century (Phalan et al., 2013). The main facilitators of this expansion have been advances in
technology, mechanisation and crop protection measures; contributing to the expansion of
arable agriculture onto formerly marginal and less fertile land. During the 20th
Century,
25
agriculture expanded globally by around 50%, from around 1,200m ha to around 1,800m ha
(Ramankutty et al. 2002). Alexandratos and Bruinsma (2012) estimated that 4m ha of arable
land were added to the global cultivated area each year between 1961 and 2007. Galluzzi et
al. (2011) estimated that by 2050 global arable land will have increased by around 70m ha.
Farming now depends less on the intrinsic capability and ecological function of farmland
than ever before and as urban growth and with other more intensive land uses encroaching on
regions with the best climate and soils for growing crops, agriculture is pushing into more
marginal areas and fragile wildlife habitat (Avery, 1997), accelerating an already substantial
decline in biodiversity (Bignal and McCracken, 2000). Moreover, notwithstanding
modification by transfer payments to agriculture from other sectors of the economy, the
inexorable impact of Engels Law (Timmer et al., 1983), is determining ongoing increases in
farm size, loss of small farm operations, crop specialisation, and increasingly concentrated
monocultures. All these factors lead to simplification of landscapes, reduction or elimination
of natural habitat patches or edges and hence the diversity and abundance of farmland
wildlife. Alongside this, more efficient harvesting equipment and intensive cultivation are
reducing the amount of waste grain and hence post-harvest food availability for wildlife
(Sherfy et al., 2011).
With recent advances in agronomic and harvesting efficiency leading to fewer post-harvest
foraging opportunities for cranes, the potential for feeding on newly-sown grain, uprooting
young plants, trampling vegetation or nest building increases conflict with farmers
(Ilyashenko and King 2018). Moreover, over-abstraction of water from rivers and
groundwater, interference and disturbance, collisions with powerlines (especially when
located between roost and feeding sites) and poisoning by agrochemicals also increase with
more intensive land use.
26
1.4 Agricultural Sustainability
Against this concerning backdrop, recent research effort has been deployed to identify ways
in which these trends can be mitigated or reversed. Food security is not only linked to an
increasing global population, it is also a function of rising personal income and changing diet,
which together suggest a growth in demand for food which would be extremely challenging
to meet through sustainable production (Benton, 2016). Ray et al. (2013) predict that global
crop production needs to double by 2050 to meet the projected demands from rising
population, diet shifts, and increasing biofuel consumption. Although maize, rice and wheat
yields have been respectively increasing at 1.6%, 1.0%, and 0.9% a year respectively;
significantly less than the 2.4% per year growth rate required to double global food
production by 2050.
The balancing of food security against biodiversity loss potentially involves one of the key
societal trade-offs of the 21st Century. Tscharntke et al. (2012) argue that smaller farms rather
than capital intensive, large-scale agri-businesses, are more likely to minimise these trade-
offs, without significant compromise. This is supported by Hanspach et al. (2017), who
conducted a multivariate analysis of social–ecological data from 110 landscapes and found
that either trade-offs or mutual benefits between food security and biodiversity were possible
but high degrees of food security in landscapes with developed infrastructure, market access
and capital came at the expense of biodiversity.
Benton (2016) notes that emissions from the food sector are significant contributors to
climate change, perhaps more so than any other sector; and yet, probably less than half the
27
world's calories are used directly for healthy diets (Kamp et al., 2015), with over half of
agricultural production lost or wasted, fed to animals or consumed in excess of healthy
requirements. It is this excess from which cranes have benefitted that will be explored in
section 1.5 below. Newell and Taylor (2018) argue that because of the corporate structure and
political influence of agribusiness, as well as its research focus on larger scale of enterprises,
‘Climate Smart Agriculture’ is extremely difficult to implement at the smallholder level.
Consistent with this, Mahon et al. (2018) noted that ‘Sustainable Intensification’ can be
criticised as being too narrow in scope; failing to address all aspects of sustainability and with
an overemphasis on environmental elements and insufficient weight given to social and
cultural dimensions. Whitfield et al. (2018) have sought to more clearly codify what Climate
Smart Agriculture could mean but believe that the firmly established paradigm of growing
more, cheaper food, without fundamentally changing the role of commodity-based trade and
markets, is a major hurdle.
Another thread in this debate is whether ‘land-sparing’, restricting farmland to smaller,
higher-yielding areas and strictly conserving natural capital elsewhere, can lead to better
biodiversity outcomes than ‘land sharing’. Based on modelling, Eisner et al. (2017) argue that
higher yielding agricultural production does not necessarily lead to higher environmental
impacts. Phalan et al. (2016) support this position, and Balmford et al. (2018) maintain that
field data suggest that impacts on wildlife would be greatly reduced through boosting
yields on existing farmland and sparing remaining natural habitats.
Although this debate continues, as yet no definitive position around ‘land sharing’ vs.
‘land sparing’ has emerged. In the meantime, as agriculture continues to change, the
significant agriculturally-related challenges faced by cranes are increasing.
28
1.5 Agriculture and Cranes
All of the world’s crane species make use of agricultural land (Harris and Mirande, 2013).
Some crane populations have benefitted significantly from agricultural expansion by foraging
on arable land; especially on grain spilt or remaining after harvest, when high energy forage
is sought for migration and wintering (Meine and Archibald, 1996). However, the emerging
technological and agronomic factors explored above are particularly impacting on some crane
species.
Anteau et al. (2011) found that changes in agricultural practice such as reduction in cropping
intervals, as well as the application of modern technology, can lead to a reduction of available
forage for cranes. Improved harvesting efficiency leads to dramatic reductions in post-harvest
waste grain, forcing cranes to seek new food sources at greater distances from roost sites,
resulting in lower reproductive success and increased crop damage through switching to
newly-sown and growing crops (Pearse et al., 2010). How cranes can adapt to agricultural
cropping and land use change is therefore a key conservation issue and management
consideration for farmers, conservation land managers and policy makers in crane range areas
(Harris and Mirande, 2013; Austin et al., 2018).
Crane populations exhibit a range of responses to agriculture, with some species’
relationships with agriculture severely impacted by the accelerating uptake of mechanisation
and improvements in agronomy (Wright et al., 2012). During the early 20th
Century Sandhill
Cranes Antigone canadensis became rare in many American states as a result of agricultural
expansion and intensification but have since recovered as a result of protection and
adaptation to modern agricultural practices. Following agricultural intensification, increased
grain production provided a number of crane species with forage at resting and wintering
sites, and high-energy combinable crops along their migration routes led to range expansion
29
and increased populations in many countries (Krapu et al., 2004; Nowald, 2012; Nowald and
Mewes, 2010; Prange, 2015; Salvi, 2015). However, intensification can lead also to fewer
roosting sites (Barzen et al., 2012). Under optimal conditions, cranes prefer to feed in fields
close to their roosts, with the distance between foraging and roost sites only rarely exceeding
30 km (Prange, 2010; Anteau et al., 2011, Nilsson et al. 2016, Nevard et al. 2019a). Limiting
accessibility to roosts may therefore lead cranes to concentrate on fewer and larger ones -
increasing conflict with farmers in close proximity (Bouffard et al., 2005; Nowald and
Mewes, 2010).
The political collapse of the former Soviet Union brought about a number of changes in crane
behaviour and distribution, and led to a westward shift in migration and dramatically
increased crane numbers along the two key European flyways (Prange, 2012; Prange, 2015).
In Ukraine, crane numbers at Askania-Nova Nature Reserve and in adjacent agricultural areas
increased from approximately 5,000 in the late 1980s to approximately 20,000 –45,000 in the
2010s; whilst numbers decreased markedly in areas of agricultural abandonment (Redchuk et
al., 2015).
In Western Europe, increased maize production has corresponded with increased numbers of
Eurasian Cranes at staging and resting areas and an increase in the migratory population from
about 40,000–45,000 in 1980s to 350,000 birds by the winter of 2014/2015 (Prange, 2015).
Sweden, Norway, Denmark and Estonia also saw dramatic increases in numbers (Sandvik,
2010; Lundgren, 2013; Tofft, 2013; Leito, 2014). In Germany the breeding range of Eurasian
cranes doubled in the thirty years to 2010 (Mewes, 2010). In France, cereal growing now
occurs over the majority of the country and has led to increases in the number of wintering
cranes to about 150,000 and a significant northward shift in crane wintering grounds (Salvi,
2015).
30
A similar response to agricultural expansion and intensification took place in the Western
Cape of South Africa, where the former extent of fynbos vegetation limited Blue Crane
Anthropoides paradisea distribution until the 1990s; when conversion to cereal production
created favourable breeding and feeding conditions (Scott and Scott, 1996). Although this
area only represented 7.6% of the Blue Crane’s range, by the early 2000s cereal-growing on
former fynbos areas supported 47.4% of the South African population (McCann et al., 2007).
As outlined above, contemporary agronomic practices, such as integrated pest management,
can induce high agricultural productivity from almost any marginal soil and land type and in
the past have led to greater availability of residual post-harvest grain for cranes. However,
improvements in agronomy and harvesting technology are now significantly reducing
leftover grain. Krapu et al. (2004) found that, largely due to improved harvesting efficiency,
whilst maize yields in central North America increased by 20% from 1978 to 1998, post-
harvest leftover grain averaged only 1.8% of production by 1998; representing a 47%
reduction in available forage for cranes.
In Western Europe during the 1970s and 1980s approximately 3–5% of wheat, barley and
oats, and 5–10% of maize was left on the ground post-harvest. More recently, only 1–2% of
other cereals and 0–1% of maize are typical levels of residual post-harvest grain, leading to
increased conflicts between cranes and farmers, with cranes foraging more intensively
amongst newly-sown crops (Nowald, 2012).
Krapu et al. (2004) also found that, as a result of shorter cropping intervals, between 77–97%
of post-harvest residual grain became unavailable to foraging birds. With the advent of pre-
emergent herbicides, new varieties of grain and intensification, farmers have begun to
cultivate immediately following harvest, to control weeds and bury residual crop stubbles,
31
leaving only a short time for cranes to feed (Prange, 2012). Cranes are hence moving to
newly-sown crops and coming into direct conflict with farmers at the critical time for crop
establishment (Nowald and Mewes, 2010).
Cropping changes can also negatively impact on crane breeding habitat. In India, replacement
of subsistence rice cropping with cash crops such as sugarcane, cotton and tobacco eliminated
crane breeding habitat in the areas where these crops are grown (Borad and Mukherjee,
2002). Some districts in Nepal have seen increased sugarcane production, with Indian Sarus
Cranes A. a. antigone no longer breeding in the Krishnagar region (Aryal et al., 2009).
1.6 Australian Cranes
Australia has two crane species. Although remaining relatively abundant in the north, the
Brolga Antigone rubicunda has disappeared from much of its range in southern Australia
(Arnol et al., 2004). The Sarus Crane Antigone antigone is primarily an Asian species (Indian
sub-continent, Myanmar, Thailand, Indochina and formerly the Philippines) and is declining
in significant parts of its range but the Australian Sarus Crane A. a. gillae is thought to have
increased significantly in numbers over the past 50 years (Archibald et al., 2003). Both
Australia’s crane species are iconic cultural symbols for both European and Aboriginal
people across Australia’s tropical north but are increasingly coming into conflict with the
agricultural sector.
The apparent population growth of the Australian Sarus Crane since its first formal
description in the 1960s (Gill, 1967) has occurred in the presence of the congeneric Brolga
and within the context of the establishment and more recent expansion of cropping in
northern Australia (Archibald et al. 2003). Not only is there now extensive Brolga-Sarus
sympatry and interaction on cropping lands, hybrids (‘Sarolgas’) have been recorded amongst
32
mixed flocks (Lofdahl, 1979; Archibald, 1981, Nevard et al. 2019b) and are known to be
fertile (Gray, 1958; Nevard et al., 2019b).
We do not yet know the drivers for this introgression but Templeton et al. (1990) identified
that changes in landscapes can be associated with genetic consequences and a hybrid zone
may be establishing in north Queensland. Imprinting studies suggest that hybrid young may
introgress with one or both parental species (Immelmann, 1972), eventually leading to
character convergence and displacement, or competitive exclusion. As agriculturally-driven
sympatry is so recent, adaptation is therefore still likely to be happening and may be
accompanied by evolutionary consequences.
1.6.1 The Brolga
The Brolga is an Australasian (Australia and New Guinea) endemic and autochthonous form.
Archibald’s (1976) work on unison calls found the Brolga call to be distinct from all other
cranes but most related morphologically and behaviourally to Sarus and White-naped cranes
Antigone vipio. Notwithstanding the c.100 year probable allopatry of northern and southern
Brolga populations, recent research by Miller et al. (2019) has identified only small genetic
differences (using materials gathered by this research).
Known to early European settlers as the ‘Native Companion’ due to its apparent propensity to
be seen in company with Aboriginal people, the Brolga has been recorded throughout the
State of Queensland (Marchant and Higgins, 1993) but is now only common and abundant in
the north. During the dry season, large flocks, sometimes numbering several thousand, can
gather at key sites such as the Cromarty Wetlands south of Townsville (Marchant and
Higgins, 1993). While breeding occurs in suitable areas throughout their Queensland range
33
(Marchant and Higgins 1993; Barrett et al. 2003), it appears to be focussed on the Gulf Plains
and Cape York Peninsula.
Brolgas have traditionally been identified as a species of freshwater and brackish wetlands;
widely dispersed when breeding but gathering in flocks during the dry season to feed on
sedge tubers in seasonally dry swamps (Herring, 2005; Chatto, 2006; Herring, 2007;
Franklin, 2008). In north Queensland they concentrate, to varying extents, on the Atherton
Tablelands and east coast marshes (such as near Cromarty, Giru, Townsville and Ingham).
Brolgas can use brackish waters, having a unique salt-gland (Hughes and Blackman, 1969)
and when observed with Australian Sarus Cranes near Normanton, Brolgas favoured deeper,
generally coastal marshes (Walkinshaw, 1973), also occurring in open habitats, forest and
woodland.
Despite early work on the ecology of the Brolga in Australia’s tropics, conducted by Lavery
and Blackman (1969), little is known about the details of key breeding and flocking sites,
although recent work by Sundar et al. (2018) has gone some way to clarify this in relation to
the Gulf Plains. In north Queensland, breeding sites are found at their highest densities in the
Normanton-Karumba area in the southeast of the Gulf of Carpentaria (G. Archibald pers.
comm.; Sundar et al., 2018) stretching inland and north to Dunbar and Kowanyama. Cape
York Peninsula is also thought to hold significant concentrations of breeding Brolgas
(Marchant and Higgins, 1993; Chatto, 2006).
Key known flocking sites in Queensland are the Gulf of Carpentaria coastal plain, Cape York
Peninsula, and coastal freshwater wetland areas along the east coast from south of Townsville
to inland areas of Cairns, including the Atherton Tablelands (Collins, 1995; Chatto, 2006).
Many of these areas have only been identified from casual observations and much of the
34
information (apart from the Atherton Tablelands) is based on occasional counts. The Brolga
population in northern Australia is thought to be stable and estimated to comprise of 20,000-
100,000 individuals (Meine and Archibald, 1996). A total of 51,969 Brolgas were recorded
by Kingsford et al., (2012), with all but 135 of these being from northern Australia.
The behaviour and biology of Brolgas in southern habitats is well documented, where their
wetland habitat requirements have also been studied (White 1987; Arnol et al. 1984; Harding
2001; Herring 2007; Myers 2001) but in Queensland these are poorly understood. Recent
work by Sundar et al. (2018) has identified that their diet in their Gulf Plain breeding areas is
less diverse than that of Australian Sarus Cranes.
1.6.2 The Australian Sarus Crane
Work by Archibald et al. (2003) and Jones et al. (2005) sought to clarify the taxonomic
position of the Sarus Crane and its subspecies. This has since been more thoroughly explored
as part of this research (Nevard et al., 2019b and in press), confirming that a distinct genetic
separation exists between the Australian subspecies A. a. gillae and the clinal Asian
subspecies A. a. antigone and A. a. sharpii.
As noted, the population of Australian Sarus Crane appears to have increased relatively
rapidly from what is thought to have been small numbers in northern Australia following its
formal identification in 1964 (Gill, 1967). G. Archibald (pers. comm.) estimates that the
population was c.200 in 1972 and current estimates suggest 5,000-10,000 individuals (E.
Scambler pers. comm.) but these are relatively loose. More specific and reliable counts
undertaken on the Atherton Tablelands indicate c.1,200-3,000 individuals flocking in the dry
season from 1997-2008 (as well as more recent counts to 2017) but it is currently not known
what proportion of the total Australian Sarus population these birds represent.
35
Sarus Cranes in Australia are almost entirely confined to Queensland, with known breeding
areas along the Gulf of Carpentaria coastal plain, at least as far north as New Mapoon and
central Cape York Peninsula (Marchant and Higgins, 1993; Sundar et al., 2018); Elinor
Scambler (pers.comm.); Lavery and Blackman (1969) and Author (pers. obs.) found that
Australian Sarus Cranes had a strong preference for ‘upland’ rather than wetland foraging
areas, where they appear to be confined to freshwater. Many feed in flocks during the dry
season on recently harvested cropping land on the Atherton Tablelands (in the company of
Brolgas), migrating to breed in wetlands on the Gulf Plains and Cape York Peninsula. Sundar
et al. (2018) found that Australian Sarus Cranes preferred Eucalyptus-dominated regional
ecosystems for breeding and had a more varied diet than sympatric Brolgas but fed across a
narrower range of trophic levels (Nevard et al. 2019a).
1.6.3 The ‘Sarolga’
Archibald (1976) has identified a common phylogenetic history between Brolgas and Sarus
cranes, diverging from a common ancestor c.3 million years ago, suggesting significant
behavioural and genetic divergence. However, with the apparent significant population
growth of Australian Sarus Cranes since the 1960s occurring in the presence of the
congeneric Brolga, one explanation put forward has been that the Australian Sarus Crane
population may have been augmented by Brolga genes. Hybrid ‘Sarolgas’ have been
recorded in the wild (Nevard et al., 2019b), and are known from captive observations to be
fertile (Gray, 1958). J. Grant, (pers. comm.) has noted that the majority of Sarolgas he has
observed appear to have been paired with Brolgas, in at least two instances accompanied by a
juvenile. Of the 44,554 cranes surveyed during this research, 2.58% were identified as
hybrids, which are backcrossing (Nevard et al., 2019b).
36
1.6.4 The Conservation Status of Australian Cranes
The IUCN Red List of Threatened Species lists the Brolga as being of Least Concern, as it
has a global population of more than 10,000 individuals and it is neither declining rapidly nor
restricted to a small range. The Brolga is not listed as threatened under the Australian
Environment Protection and Biodiversity Conservation Act 1999; however, its conservation
status varies from State to State and is listed as Threatened under the Victorian Flora and
Fauna Guarantee Act (1988). Under this Act, an Action Statement for recovery and future
management has been prepared. It is also included in the 2007 advisory list of threatened
vertebrate fauna in Victoria where it is listed as Vulnerable. The Sarus Crane is classified as
Vulnerable on the IUCN Red List on the basis of rates of decline in Asia (BirdLife
International, 2018c).
The current legal status of Brolgas and Australian Sarus Cranes affords a degree of
protection, but within their range in Queensland there are only a few protected areas used by
cranes, including Rinyirru (Lakefield) and Errk Oyangand (Staaten River) National Parks. On
the crane-critical Atherton Tablelands, only Hastie’s Swamp National Park and the Mareeba
Wetlands Nature Refuge have protected status.
1.7 Research Questions and Thesis Structure
Set against the background set out above, my thesis is framed to explore the distributional,
resource use, phylogenetic and agricultural relationships of Brolgas and Australian Sarus
Cranes. Its geographic focus is mainly on and around the Atherton Tablelands in north
Queensland but also extends to other parts of Australia and Asia. The key research questions
and the hypotheses I test are outlined below, followed by an explanation of the structure of
the thesis designed to address them.
37
1.7.1 Research questions
Question 1: What are the evolutionary relationships between Australian Sarus Cranes and
subspecies in Asia?
Null hypothesis: Australian Sarus Cranes are likely to have not divereged from Asian
subspecies and to form a cline with them. Under this null hypothesis I would expect genetic
differentiation to be minimal and not significant.
Alternative hypothesis: Australian Sarus Cranes form a genetically distinct subspecies. Under
this alternative hypothesis, I would expect Australian Sarus Cranes to have diverged
significantly from all Asian subspecies and that there would be a discontinuity in variation
coinciding geographically with phenological variation.
Question 2: What is the propensity for introgression between Sarus Cranes and Brolgas?
Null hypothesis: Given their long period of divergence from a common ancestor, there are
sufficient behavioural and genetic obstacles to prevent significant introgression. Under this
null hypothesis I would expect introgression to be minimal and not a significant evolutionary
pathway.
Alternative hypothesis: Introgression is occurring at a rate sufficient to influence the
evolutionary trajectory of both Australian crane species. Under this alternative hypothesis I
would expect introgression to be significant and have the potential to increase.
Question 3: What are the distribution and resource partitioning characteristics of cranes on
the Atherton Tablelands?
Null hypothesis: Crane distribution and resource partitioning are not determined by foraging
opportunities, crop stage and range of agricultural crops. Under this null hypothesis I would
expect no significant correlation between foraging opportunities, crop stage and cropping
patterns.
38
Alternative hypothesis: Crane distribution and resource partitioning are related to foraging
opportunities, cropping patterns and crop stage. Under this alternative hypothesis, I would
expect a strong relationship with foraging opportunities, cropping pattern, stage and crane
distribution.
Question 4: What are the attitudes of farmers and pastoralists towards cranes?
Null hypothesis: Farmers and pastoralists are not comfortable with cranes using their crops.
Under this null hypothesis I would expect farmers and pastoralists to take active measures to
exclude cranes.
Alternative hypothesis: Farmers and pastoralists tolerate cranes amongst some of their crops
but believe that forthcoming agronomic and cropping changes will reduce crane foraging
opportunities. Under this alternative hypothesis, I would expect farmers to be open to the
development of humane crane repellent measures and economic opportunities around crane-
based tourism.
1.7.2 Thesis Structure
To address these questions and associated hypotheses, my thesis is structured as follows:
Chapter 1 – Introduction, Literature Review and Thesis Structure: Paleoenvironmental
and agricultural contexts. In Chapter 1 I have described the evolutionary context of cranes
and their relationship with past, present and future agricultural development; including a brief
overview of the influence of the impacts of specific political, cultural, social and agronomic
changes on cranes. I have also presented an introduction to the biology, ecology and
conservation status of Brolgas and Australian Sarus Cranes.
Chapter 2 - Study Area and Methodology: I describe the region in which the research was
conducted (the Atherton Tablelands and Gulf Plains). I also describe the rationale for the
39
adoption of the methodological approaches used, providing an outline of the detailed methods
set out in each of Chapters 4, 5, 6 and 7.
Chapter 3 - The Australian Sarus Crane: Genetic and phylogenetic significance of
Australian Sarus Cranes. In this chapter, submitted for publication in PLOS ONE, I describe
the phylogenetic relationships between the Australian Sarus Crane and other extant Sarus
Crane subspecies. I provide a genetic analysis based on a large range of samples from most
Sarus Crane range areas, as well as from the extinct Philippine subspecies.
Chapter 4 – Extent and Potential Trajectory of Introgression: Genetic and visual
evidence for hybridisation between the Brolga and Australian Sarus Crane. In this chapter,
published online in Oryx (Nevard et al., 2019b), I confirm the level of introgression between
the Brolga and Australian Sarus Crane and confirm their migration between the Atherton
Tablelands and Gulf Plains; using a range of genetic sample sources, including a particularly
large sample of recently shed feathers gathered on the Atherton Tablelands and in the Gulf
Plains.
Chapter 5 - Resource Partitioning and Competition: Distribution and foraging of Brolgas
and Sarus Cranes on the Atherton Tablelands. In this chapter, published online in Pacific
Conservation Biology (Nevard et al., 2019a), I provide a statistical analysis of observational
data, gathered over a three year period on the Atherton Tablelands; with definitive results in
relation to species distribution, foraging preferences and population.
Chapter 6 – Farmer Attitudes: Relationships between cranes, farmers and pastoralists on
the Atherton Tablelands. In this chapter, published online in Pacific Conservation Biology
(Nevard et al., 2018), I provide an analysis of farmer attitudes towards cranes, as well as an
40
overview of their future cropping and agronomic intentions. I also explore the potential for
the development of a crane-based tourism sector.
Chapter 7 – Discussion: An exploration of research findings in relation to contemporary
issues and postulation of various potential future scenarios relating to cranes in north
Queensland.
Chapter 8 - Conclusions and Recommendations: In this final chapter I reiterate my
research conclusions and make recommendations for the conservation management of
Brolgas and Australian Sarus Cranes.
41
CHAPTER 2 – STUDY AREA AND METHODOLOGY
2.1 Study Area and Geographical Scope
This research was mainly conducted on the Atherton Tablelands in Far North Queensland but
also refers to other parts of Australia and Asia (see Fig. 2.1 below).
Fig 2.1 Global distribution of Brolga Antigone rubicunda and Sarus Crane Antigone antigone (A),
field data collection sites in northern Queensland (B, C and D). Distribution data derived from
BirdLife International and NatureServe Bird Species Distribution Maps of the World (2014) and the
Australian Bird Guide (2017). Gulf Plains Interim Biological Regionalisation Area (IBRA) derived
from Department of Environment and Energy (2012) and state roads from Department of Transport
and Main Roads (2016).
42
Brolgas and Sarus Cranes breed in the wet season on the Gulf Plains and in Cape York
Peninsula, and flock in the dry season on the Atherton Tablelands (see Fig. 2.2 below), which
was the principal location for this research.
Fig. 2.2 Atherton Tablelands region showing location, major settlements, land use and Key
Biodiversity Area (data from Queensland Globe and Department of Environment & Energy, 2012). .
The Atherton Tablelands extend from north of Mareeba and south of Innot Hot Springs, with
an area of approximately 6,000 km2 of which about 500 km
2 is intensively farmed. Elevation
ranges from 399 to 1,070 m above sea level, with a tropical mid-elevation to upland climate
and strongly seasonal rainfall, ranging from 900 to 2,200 mm. The Tablelands encompass
three main landscape elements: (i) rainforests (mainly part of the Wet Tropics World
Heritage Area); (ii) areas of dry sclerophyll savanna woodland; and (iii) some of Australia’s
most fertile and productive farmland (Department of Agriculture and Fisheries, 2015). Cranes
are absent from rainforest but occur in the latter two landscapes, mainly during the dry season
flocking months of May to December.
43
Typical agricultural soils in the northern and southernmost areas of the Atherton Tablelands
are derived from granite and metamorphics and have a slightly acid pH and low fertility,
compared to the well-drained soils in the central Tablelands derived from basalt (Department
of Agriculture and Fisheries, 2015). Water for the Mareeba-Dimbulah Irrigation Area is
supplied through an extensive network of channels and streams from a large water
impoundment on the Barron River, Tinaroo Dam. Farming enterprises in other parts of the
Tablelands (including intensive agricultural areas around Atherton, Malanda and Ravenshoe)
draw water from volcanic groundwater aquifers, natural watercourses and smaller dams
(Department of Agriculture and Fisheries, 2015).
The Atherton Tablelands provide a regionally important dry season refuge for both Brolgas
and Australian Sarus Cranes. In the case of Australian Sarus Cranes, the area is currently
their only formally-identified dry season site (Archibald and Swengel, 1987) and as the Sarus
Crane is listed as Vulnerable by the IUCN (Birdlife International, 2018a), these factors were
key reasons for the designation of the Atherton Tablelands Key Biodiversity Area (Birdlife
International, 2018b); where both crane species have been counted annually by local BirdLife
Australia members since 1996.
2.2 Methodology
In order to be useful in relation to the multifaceted conservation problems facing cranes in
northern Australia, a multidisciplinary approach is required. This thesis uses observational,
genetic, GIS, socioeconomic and statistical tools to address this. As detailed methodologies
are provided in each of Chapters 3, 4, 5, and 6 a précis is provided below, along with
reference to where published.
44
Chapter 3 - Subspecies in the Sarus Crane Antigone antigone revisited; with particular
reference to the Australian population. [Submitted for publication to PLOS ONE].
To thoroughly investigate the genetic relationships between Sarus Crane subspecies and
maximise the resolution of their genetic history, large numbers of blood and tissue samples
were assembled from most Sarus Crane range states and analysed using techniques
established in published genetic work on cranes. Ten amplified microsatellite loci were used
that had been developed for the Brolga (Miller et al., 2019), the Sarus Crane (Jones et al.,
2005) and other crane species (Hasegawa et al., 2000; Meares et al., 2009). Statistical
analyses used to calculate gene diversity (Nei, 1987) and allelic richness (Petit et al., 1998)
included FSTAT 2.9.3.2 (Goudet, 1995) and GenePop 4.2 (Raymond and Rousset, 1995;
Rousset, 2008). For population differentiation, microsatellite data were analysed by Bayesian
clustering, using STRUCTURE 2.3.4 (Pritchard et al., 2000; Falush et al., 2007). Structure
Harvester 0.6.94 (Earl et al., 2012) was used to analyse the data, following Evanno et al.
(2005). The most likely assignment of individuals to clusters was inferred in CLUMPAK
(Kopelman et al., 2015). K-means clustering was applied to validate the Bayesian approach
using GenoDive 2.0b23 (Meirmans and van Tienderen, 2004), as it is free of population
genetic assumptions (in contrast to STRUCTURE). Relationships among mitochondrial
haplotypes were analysed using statistical parsimony/TCS (Clement et al., 2002) and
implemented in PopART (Leigh and Bryant, 2015) and MrBayes 3.2.6 (Ronquist et al.,
2012).
Chapter 4 – Extent and Potential Trajectory of Introgression: The Sarolga: conservation
implications of genetic and visual evidence for hybridization between the Brolga Antigone
rubicunda and the Australian Sarus Crane Antigone antigone gillae. Oryx.
doi:10.1017/S003060531800073X.
45
In order to gain a clear understanding of the extent of Brolga and Australian Sarus Crane
introgression, both visual surveys and genetic sampling were conducted across their flocking
areas of the Atherton Tablelands (see Chapter 5). Large numbers of freshly-shed feathers
were also collected opportunistically from sites in the Gulf Plains and on the southern edge of
the Atherton Tablelands. Using techniques described in Chapter 4, microsatellite loci were
tested which had been successfully used in the Sarus Crane (Jones et al., 2005), Brolga
(Miller, 2016) and other species of crane (Hasegawa et al., 2000; Meares et al., 2009). As
there was the possibility that feathers of a particular bird were collected more than once,
identical genotypes were identified using Cervus 3.0.7 (Kalinowski et al., 2007). In order to
identify the number of genetic clusters and potential hybrid individuals, Bayesian clustering
was conducted using STRUCTURE 2.3.4 (Pritchard et al., 2000; Falush et al., 2007).
Structure Harvester 0.6.94 (Earl and von Holdt, 2012) was used to analyse the data, following
Evanno et al. (2005) and Structure Plot V2.0 (Ramasamy et al., 2014). More detailed
analyses were conducted based on the clusters identified by Bayesian clustering using
FSTAT 2.9.3.2 (Goudet, 1995), GenePop 4.2 (Raymond and Rousset, 1995; Rousset, 2008),
and Micro-Checker 2.2 (van Oosterhout et al., 2004). In order to test whether shed feathers
might have a wider application in monitoring crane populations, application of the Lincoln-
Petersen Index was also undertaken for ‘genetically re-trapped’ birds; based on the
methodology described by Southwood and Henderson (2000).
Chapter 5 - Resource Partitioning and Competition: Agriculture, brolgas and Australian
sarus cranes on the Atherton Tablelands, Australia. Pacific Conservation Biology,
doi:10.1071/PC18081.
An observational approach was used to investigate crane distribution and foraging on the
Atherton Tablelands. Forty-six crane feeding sites, along a 335 km driven traverse, were
46
surveyed on 44 occasions. The use of more resource-intensive techniques such as stable
isotope analysis was considered but rejected, as analyses of observational data were
considered to be capable of providing definitive findings in relation to differential numbers,
distribution, and foraging.
To evaluate whether species used the Atherton Tablelands differently over time, Permanova
was used and the Euclidean distance measure was employed to untransformed counts. To
determine whether crane species used different sites on the Atherton Tablelands, the rank
correlation between species was first examined (separately using each of abundance and
density). To measure spatial association of sites Moran’s I statistic was calculated, based on
the percentage of Brolgas at each site and using the Getis-Ord Gi* statistic to identify clusters
of sites with values higher (hotspot) or lower (coldspot) in magnitude than expected by
chance (Getis and Ord, 1992).
To consider the possibility that choice of feeding sites might be constrained by distance to
roosts, the distance between them was evaluated as a function of species. Effects of distance
class, species, and the distance class were then evaluated by species interaction in Permanova
with site as a random effect; using the Euclidean distance measure, a Type III Sum of
Squares model, and 9999 permutations. As the interaction term was statistically significant,
post-hoc pairwise comparisons of distances classes were conducted separately for each
species.
A regression tree analysis was run to examine species foraging preferences. To identify crop
type preferences, each crane species was considered in a separate model. The analysis was
performed in Permanova using the Euclidean distance measure, a Type III Sum of Squares
model, and 9999 permutations. To evaluate seasonal patterns of crop type availability,
47
observed frequencies were compared to expected frequencies across months (May to
December), the latter based on constant proportionality calculated across all site surveys and
evaluated using Chi-squared analysis.
Chapter 6 – Farmer Attitudes: Farming and cranes on the Atherton Tablelands, Australia.
Pacific Conservation Biology, doi:10.1071/PC18055. 2018.
Information on the relationship between cranes and agriculture on the Atherton Tablelands is
critical for conservation management. Attitudes and socioeconomic conditions under which
farmers and graziers operate were explored using an interview methodology established by
Garnett et al. (2016).
Forty-five farmers and graziers, whose land was known to be used by cranes, described their
farming experience; the composition of their enterprises; their views on nature conservation;
knowledge of and attitudes towards cranes; damage by cranes and other wildlife; potential
solutions for reducing crop damage; and attitudes towards crane tourism and crop damage
mitigation trials. They also expressed their intentions for their enterprises in the future. Two
forms of analysis were conducted based on the landholder survey: (i) descriptive statistics
based on ranking to summarise knowledge and attitudes; and (ii) textual sampling of
comments made by individual interviewees to convey the tone of the interviews and provide
context.
48
CHAPTER 3 - THE AUSTRALIAN SARUS CRANE
Subspecies in the Sarus Crane Antigone antigone revisited; with
particular reference to the Australian population. [Submitted for
publication to PLOS ONE 26/07/19].
3.1 Abstract
Subspecies are less well-defined than species but have become one of the basic units for
protection in law. Evidence for the erection or synonymy of subspecies therefore needs to be
based on the best science available. It is shown that there is clear genetic differentiation in the
Sarus Crane Antigone antigone where previously the variation had appeared to be clinal.
Based on a sample of 76 individuals, analysis of 10 microsatellite loci from 67 samples and
49 sequences from the mitochondrial control region, this research establishes that the
Australian Sarus Crane A. a. gillae differs significantly from both A. a. antigone (South Asia)
and A. a. sharpii (Myanmar and Indochina). A single sample from the extinct Philippine
subspecies A. a luzonica clustered with A. a. gillae, hinting at a more recent separation
between them than from A. a. antigone and A. a. sharpii even though A. a. sharpii is closer
geographically. The results demonstrate that failure to detect subspecies through initial
genetic profiling does not mean discontinuities are absent and has significance for other cases
where subspecies are dismissed on the basis of partial genetic evidence alone. It is also
potentially important for sourcing birds for reintroduction to the Philippines.
3.2 Introduction
Species are diagnosed along a continuum from phenotypically distinguishable but with
common ancestry, through to biological incompatibility (de Quieroz, 2007); with over 30
49
definitions currently in use (Zachos, 2018). Subspecies are even less well defined with
diagnoses applied unevenly among taxa. Broadly they represent geographically defined
populations that are potentially incipient species diagnosable by at least one heritable trait
(Wallin et al., 2017) but while there have been attempts to define subspecies mathematically
(Baker et al., 2002, Patten and Unitt, 2002), debate continues (Patten and Remsen, 2017).
The hope that genetic analysis would resolve ambiguities has not eventuated. For example,
while cetacean biologists are content to define subspecies quantitatively on the basis of
mitochondrial DNA control region sequence data alone (Martien et al., 2017), this approach
has been rejected for birds (McCormack and Maley, 2015), not least because there is often
discordance between mitochondrial and nuclear DNA (Toews and Brelsford, 2012).
The definitions matter. This leaves open the point at which the best scientific information is
reached. A failure to recognise subspecies can mean they are lost before being recognised as
warranting conservation attention (Gippoliti et al., 2017). On the other hand, over-splitting
increases the probability of genetic problems among the necessarily smaller populations
identified (Frankham et al., 2012). Moreover, subspecies have become, with species, the
common currency of threatened species conservation in most jurisdictions (Garnett and
Christidis, 2007) with erection or synonymy of subspecies having legal, financial and social
consequences. For example, had the US Fish and Wildlife Service followed Zink et al. (2013)
and decided that the California gnatcatcher (Polioptila c. californica) did not warrant
subspecies status, 80,000 ha of its critical coastal sage scrub habitat would have been released
for development (Frost, 2015). In the end they decided otherwise, on the basis that the best
available scientific information did not support synonymy (US Fish and Wildlife Service,
2016).
50
The Sarus Crane Antigone antigone [Linnaeus, 1758] exemplifies how further investigation
of variation has the potential to change both taxonomic treatment and the value given to
different populations, having geographically separate populations in southern Asia and
Australia (see Fig. 3.1).
Fig. 3.1 Global distribution of the Sarus Crane A. antigone, showing populations and subspecies
[Distribution data derived from BirdLife International and NatureServe Bird Species Distribution
Maps of the World (2014), the Australian Bird Guide (2017) and author contributions].
As it is extinct in the Philippines and declining in some of its Asian range, particularly in
Myanmar and Indochina (Meine and Archibald, 1996; Archibald et al., 2003), it is classed as
Vulnerable by the IUCN (BirdLife International, 2018c). Intraspecific variation within the
species has been the subject of ongoing debate. Blyth and Tegetmeier (1881) initially erected
the Indian and Myanmar birds as distinct species, based on plumage (the Indian Sarus Crane
has a white upper neck and tertials) and body size. Sharpe (1894) retained this distinction but
51
shortly afterwards Blanford (1895) combined them into one species with two sub-species,
Grus antigone antigone and Grus antigone sharpii respectively, a classification which has
since endured. Hachisuka (1941) described the (then extant) Philippine population as Grus
antigone luzonica and distinct from both G. a. antigone and G. a. sharpii. Although the
taxonomic nomenclature A. a. sharpii has been followed for the South-east Asian subspecies
adopted by del Hoyo and Collar (2014), it is noted that the latinisation of Sharpe’s name as A.
a. sharpii is not grammatically correct and is more properly A. a. sharpeii.
In 1966, Sarus Cranes were discovered in Australia (Gill, 1967). Initially assigned to G. a.
sharpei (sic) because of a lack of white in the plumage, they were subsequently described by
Schodde (1988) as a new sub-species G. a. gilliae (sic), on the basis of distinct plumage and a
larger ear patch. Archibald (personal observation) notes that A. a. gillae also has different
unison calls from both A. a. antigone and A. a. sharpii, helping to differentiate it from the
sympatric Brolga A. rubicunda. Although he did not separate it by plumage, Hachisuka’s
(1941) description of the Philippine Sarus Crane population as the subspecies A. a. luzonica
was made on the basis of its significantly smaller size (in a range of measurement parameters
compared to A. a. antigone and A. a. sharpii). However, most recently, del Hoyo and Collar
(2014) have recognised only three subspecies (see Fig. 3.2): A. a. antigone (India), A. a.
sharpii (South-east Asia) and A. a. gillae (Australia); considering A. a. luzonica to have been
indistinguishable from A. a. sharpii.
52
Fig. 3.2 Extant Sarus Crane subspecies: (a) antigone South Asia; (b) sharpii Myanmar and
Indochina; (c) gillae Australia. [Photographs T, Nevard (a) and (c); Robert van Zalinge (b)]
These relatively settled sub-specific arrangements, largely indicated by morphology, have not
hitherto been strongly supported by genetic analyses. Application of molecular techniques to
understand the subspecific arrangements of Sarus Cranes (Dessauer et al.,1992; Wood and
Krajewski, 1996; Jones et al., 2005) suggested that colonisation of Australia by Sarus Cranes
was relatively recent and that there had been little differentiation of populations across their
range (Jones et al., 2005).
The potential ancestral relationship with other populations is relevant for two reasons. The
first of these is as a contribution to the debate about using genetics as the sole basis for
synonymising or retaining subspecies; particularly whether the different subspecies should
continue to be treated as separate, valued management units - although urged regardless of
the taxonomy (Jones et al., 2005). Second, reintroduction of Sarus Cranes to the Philippines
is being considered (J. C. Gonzalez, pers. comm.), so an appropriate potential founding stock
needs to be identified.
53
3.3 Methods
3.3.1 Samples
In order to measure the degree of differentiation between Sarus Crane populations, material
was secured opportunistically from all four putative subspecies and most range countries (see
Tables 3.1and 3.2 below). Sample material varied from naturally shed and deliberately
plucked feathers, to blood taken from live birds (both wild and captive) and tissue harvested
from natural mortalities and museum specimens.
Only samples from captive birds in Germany and Australia (Lemgo Crane Collection and
Cairns Tropical Zoo) and feathers from crane flocking sites in Australia and museum
specimens in the United States were specifically collected for this project. All other samples
assembled were derived from sets previously collected as part of other projects in Myanmar
(captive zoo and monastery birds), Thailand (captive zoo birds), and Cambodia (wild-caught
birds).
The blood sample collection protocol for captive German and Australian birds was for a
three-person restraining team (all with significant experience in crane restraint and sampling)
to catch the bird using a landing net; followed by immediate hooding and drawing ≤1mm of
blood from the brachial vein (placing this immediately into 100% ethanol). In all cases
restraint lasted less than 2 minutes. In Myanmar and Thailand, although sample collection
was not part of this project, the collection protocol was consistent. In Cambodia, birds were
wild caught using alpha chloralose, as part of a previous project and sampled as above, with
an additional oral swab. One tissue (brain) sample from Cambodia was from a bird that had
died recently from natural causes.
54
Shed feathers visibly free of soil and/or faecal contamination were gathered from crane
flocking sites in Australia using tweezers and re-sealable plastic bags then refrigerated.
Lightly-plucked chest feathers (3 to 5, ≤ 25mm) were obtained from restrained captive birds
in Germany and Australia and refrigerated.
Table 3.1 Sources of Sarus Crane DNA used in analyses.
Subspecies Country
Sample
type
No. DNA samples
Nuclear Mitochondrial
antigone India Blood 5 3
Toe pad 3 1
gillae Australia Feather 25 20
luzonica Philippines Toe pad 1 -
sharpii Cambodia Brain 1 -
Blood 12 6
Oral swab 1 -
Myanmar Blood 11 11
Thailand Blood 8 8
Total 67 49
Table 3.2 Details of sample collections for Sarus Crane (Ssp: subspecies; M: microsatellites; S:
sequences)
Code Ssp Country Locality
Collection
number
DNA
source M/S Aus01 gillae Australia Gulf Plains B1974 feather M/S
Aus02 gillae Australia Gulf Plains B1976 feather M/--
Aus03 gillae Australia Gulf Plains B1980 feather M/S
Aus04 gillae Australia Gulf Plains B1986 feather M/--
Aus05 gillae Australia Gulf Plains B1989 feather M/--
Aus06 gillae Australia Gulf Plains B2168 feather M/--
Aus07 gillae Australia Gulf Plains B2216 feather M/S
Aus08 gillae Australia Gulf Plains B2220 feather M/--
Aus09 gillae Australia Gulf Plains B2225 feather M/--
Aus10 gillae Australia Gulf Plains B2228 feather M/--
Aus11 gillae Australia Gulf Plains B2233 feather M/--
Aus12 gillae Australia Gulf Plains B2234 feather M/--
Aus13 gillae Australia Gulf Plains B2239 feather M/--
Aus14 gillae Australia Gulf Plains B2241 feather M/S
Aus15 gillae Australia Gulf Plains B2243 feather M/--
Aus16 gillae Australia Gulf Plains B2245 feather M/--
Aus17 gillae Australia Gulf Plains B2247 feather M/--
Aus18 gillae Australia Gulf Plains B2248 feather M/--
Aus19 gillae Australia Gulf Plains B2249 feather M/--
Aus20 gillae Australia Gulf Plains B2254 feather M/S
Aus21 gillae Australia Gulf Plains B2255 feather M/--
Aus22 gillae Australia Gulf Plains B2258 feather M/S
55
Code Ssp Country Locality
Collection
number
DNA
source M/S Aus23 gillae Australia Gulf Plains B2261 feather M/--
Aus24 gillae Australia Gulf Plains B2352 feather M/--
Aus25 gillae Australia Gulf Plains B2380 feather M/--
Aus26 gillae Australia Gulf Plains B1922 feather --/S
Aus27 gillae Australia Gulf Plains B1926 feather --/S
Aus28 gillae Australia Gulf Plains B1927 feather --/S
Aus29 gillae Australia Gulf Plains B1983 feather --/S
Aus30 gillae Australia Gulf Plains B2008 feather --/S
Aus31 gillae Australia Gulf Plains B2009 feather --/S
Aus32 gillae Australia Gulf Plains B2015 feather --/S
Aus33 gillae Australia Gulf Plains B2196 feather --/S
Aus34 gillae Australia Gulf Plains B2198 feather --/S
Aus35 gillae Australia Gulf Plains B2218 feather --/S
Aus36 gillae Australia Gulf Plains B2224 feather --/S
Aus37 gillae Australia Gulf Plains B2250 feather --/S
Aus38 gillae Australia Gulf Plains B2251 feather --/S
Aus39 gillae Australia Gulf Plains B2327 feather --/S
Cam01 sharpii Cambodia
Siem Reap, Angkor Centre for
Conservation of Biodiversity KHL15-ACCB-
006-Br-RNA brain M/--
Cam02 sharpii Cambodia Tonle Sap floodplains
KHL16-
ZALINGE-002 blood M/--
Cam03 sharpii Cambodia Tonle Sap floodplains
KHL16-
ZALINGE-003 blood M/--
Cam04 sharpii Cambodia Mekong delta region
KHL16-
ZALINGE-005 blood M/--
Cam05 sharpii Cambodia Mekong delta region
KHL16-
ZALINGE-006 blood M/--
Cam06 sharpii Cambodia Tonle Sap floodplains
KHL16-
ZALINGE-008 blood M/S
Cam07 sharpii Cambodia Tonle Sap floodplains
KHL16-
ZALINGE-009 blood M/--
Cam08 sharpii Cambodia Tonle Sap floodplains
KHL16-
ZALINGE-011 blood M/S
Cam09 sharpii Cambodia
Siem Reap, Angkor Centre for
Conservation of Biodiversity
KHL16-
ZALINGE-KH003 blood M/S
Cam10 sharpii Cambodia Tonle Sap floodplains
KHL16-
ZALINGE-R/W blood M/S
Cam11 sharpii Cambodia Tonle Sap floodplains
KHL16-
ZALINGE-001 blood M/S
Cam12 sharpii Cambodia
Siem Reap, Angkor Centre for
Conservation of Biodiversity
KHL16-
ZALINGE-KH001 blood M/--
Cam13 sharpii Cambodia
Siem Reap, Angkor Centre for
Conservation of Biodiversity
KHL16-
ZALINGE-KH002 blood M/S
Cam14 sharpii Cambodia
Siem Reap, Angkor Centre for
Conservation of Biodiversity ACCB-A0058-1
oral
swab M/--
Ind01 antigone India
Private collection:
Lemgo/Germany B1920 blood M/--
Ind02 antigone India
Private collection:
Lemgo/Germany B1921 blood M/--
Ind03 antigone India
Private collection:
Lemgo/Germany B2192 blood M/S
Ind04 antigone India
Private collection:
Lemgo/Germany B2822 blood M/S
Ind05 antigone India
Private collection:
Lemgo/Germany B2823 blood M/S
56
Code Ssp Country Locality
Collection
number
DNA
source M/S Ind06 antigone India NMNH, Washington DC USNM64453 toe pad M/S
Ind07 antigone India Cincinnati Zoo CinB299851 toe pad M/--
Ind08 antigone India Cincinnati Zoo CinB299851 toe pad M/--
Mya01 sharpii Myanmar Minbya, Rakhine State IPMB64768 blood M/S
Mya02 sharpii Myanmar Maubin, Ayeyarwady Region IPMB64769 blood M/S
Mya03 sharpii Myanmar Maubin, Ayeyarwady Region IPMB64770 blood M/S
Mya04 sharpii Myanmar Maubin, Ayeyarwady Region IPMB64771 blood M/S
Mya05 sharpii Myanmar Einme, Ayeyarwady Region IPMB64772 blood M/S
Mya06 sharpii Myanmar Einme, Ayeyarwady Region IPMB64773 blood M/S
Mya07 sharpii Myanmar Nay Pyi Taw Zoo, IPMB64774 blood M/S
Mya08 sharpii Myanmar Nay Pyi Taw Zoo, IPMB64775 blood M/S
Mya09 sharpii Myanmar Yadanapon Zoo IPMB64776 blood M/S
Mya10 sharpii Myanmar Minbya, Rakaine State IPMB64780 blood M/S
Mya11 sharpii Myanmar Minbya, Rakaine State IPMB64781 blood M/S
Phi01 luzonica Philippines NMNH, Washington DC USNM256982 toe pad M/--
Tha01 sharpii Thailand Korat Zoo 275 blood M/S
Tha02 sharpii Thailand Korat Zoo 280 blood M/S
Tha03 sharpii Thailand Korat Zoo 282 blood M/S
Tha04 sharpii Thailand Korat Zoo 283 blood M/S
Tha05 sharpii Thailand Korat Zoo 288 blood M/S
Tha06 sharpii Thailand Korat Zoo 292 blood M/S
Tha07 sharpii Thailand Korat Zoo 294 blood M/S
Tha08 sharpii Thailand Korat Zoo 295 blood M/S
3.3.2 Extraction
3.3.2.1 Nuclear DNA
DNA was extracted using the SDS/salting-out protocol of Miller et al. (1988). Dithiothreitol
and Roti-PinkDNA (Carl Roth, Karlsruhe, Germany) were added in order to increase the
yield. For the Cambodian blood and tissue samples, QIAGEN’s RNeasy Mini Kit was used,
for an oral swab the QIAamp Viral RNA Kit. For the Thailand blood samples, DNA was
extracted by using QIAGEN’s RNeasy Mini Kit. We amplified the ten microsatellite loci
(Gamµ3, 18, 24,101b; GjM8, 13, 15, 48b; GR22, 25) used in our analysis of hybridization of
the Brolga (Antigone rubicunda) and Australian Sarus Crane (A. antigone gillae) (Nevard et
al., 2019b) which have been developed for other crane species (Hasegawa et al., 2000;
Meares et al., 2009), the Sarus Crane (Jones et al., 2005) and the Brolga (Miller et al., 2019),
respectively. PCRs conducted in a volume of 10 µl contained 1 µl DNA (10-25 ng), 1 µl of
10 x NH4-based Reaction Buffer, 1.5-2.25 mM MgCl2 Solution (Table 2), 0.25 mM of each
primer, 0.2 mM of dNTP, 0.04 µl of BioTaq DNA Polymerase (5 U/µl), 0.6 µl of 1 % BSA
57
and sterile ddH2O. If not successful with this first protocol, the MyTaq mix (all products from
BIOLINE, London, UK) was used. The PCR profile started with an initial denaturation at
94°C, followed by 36 cycles of denaturation at 94°C, primer specific annealing (Table 2) and
extension at 72°C each for 30 s, and a final elongation at 72°C for 30 min. Microsatellite
alleles were separated on a 3130xl Genetic Analyzer using the GeneScan 600 LIZ Size
Standard 2.0. Fragment sizes were determined manually in GeneMapper 4.0 (all three
products from Applied Biosystems, Waltham, USA) as automatic calling with arbitrarily
predefined bin width may give inconsistent results. In order to maximize accuracy of size
determination, we repeated PCRs of samples with initially weak signals or which had rare
variants. Eventually, PCR samples peculiar to different runs had to be loaded on the same
plate to improve comparability.
3.3.2.2 Mitochondrial DNA
Where DNA quality allowed, we also sequenced large parts of copy 2 of the mitochondrial
control region (Akiyama et al. 2017) using primers L16707 and H1247 (Krajewski et al.,
2010) spanning a fragment of c. 1000 bp in A. antigone and 1150 bp in three specimens of A.
rubicunda; one from the Gulf plains and two from the Atherton Tablelands (see Nevard et al.,
2019b), which we used as outgroup in the phylogenetic analyses. In some specimens we had
to target a shorter fragment using the forward primer L514 instead resulting in lengths of
c.610 bp. PCRs were conducted using the MyTaq mix. The temperature profile for the long
fragment comprised: 95°C for 3 min, 5 cycles of 95°C/15 s, 65°C/20 s and 72°C/25 s, 5
cycles 95°C/15 s, 60°C/20 s and 72°C/25 s, 30 cycles 95°C/15 s, 55°C/20 s and 72°C/25 s,
and a final extension at 72°C for 5 min. For the short fragment the profile was similar and
had 4, 4 and 32 cycles with respective annealing temperatures of 60°C, 55°C and 50°C. PCR
products were cleaned using an exonuclease I/shrimp alkaline phosphatase mix. Cycle
58
sequencing was then performed in 10 µl using the PCR primers and ABI’s Big Dye
Terminator Ready Reaction Mix 3.1 of which 50% were replaced by halfBD (Merck). The
thermal cycler profile followed the manufacturer’s suggestions except that the annealing
temperature was lowered to 48° C. HighPrep DTR magnetic beads (Biozym) were used for
purification of the sequencing reactions. The sequences were read on an ABI 3130xl Genetic
Analyzer (Thermo Fisher Scientific Inc., Waltham, MA, USA). Raw sequences were edited
in Geneious 10 (www.geneious.com) and BioEdit 7.0.5.3 (Hall, 1999), respectively, and
aligned using the web version of MAFFT 7 (Katoh et al., 2017).
3.3.3 Statistical analysis
3.3.3.1 Nuclear DNA
FSTAT 2.9.3.2 (Goudet, 1995) as well as GenePop 4.2 (Raymond & Rousset, 1995; Rousset,
2008) were used to test the microsatellite data for Hardy-Weinberg equilibrium and to
calculate gene diversity (Nei, 1987) and allelic richness (Petit et al., 1998) of subspecies. For
population differentiation, the microsatellite data were analysed in two ways, (i) in a divisive
approach without a priori designation of subspecies by Bayesian clustering using
STRUCTURE 2.3.4 (Pritchard et al., 2000; Falush et al., 2007); and (ii) by estimating
differentiation of the nominal subspecies (except the single individual of A. a. luzonica),
calculating pairwise FST values using FSTAT. STRUCTURE was run with K (number of
clusters) ranging from one to six and ten replicates assuming the admixture model since the
sequence analyses suggested that there had been admixture. We modelled both, uncorrelated
and correlated allele frequencies as it was unclear which approach provided a better fit for the
biological context. The Markov chains ran for 1 million generations after a burn in of
100,000. Structure Harvester 0.6.94 (Earl et al., 2012) was used to analyse the data following
Evanno et al. (2005). Integrating the results of the replicated runs in STRUCTURE, the most
59
likely assignment of individuals to clusters was inferred in CLUMPAK (Kopelman et al.,
2015). K-means clustering was applied to validate the Bayesian approach using GenoDive
2.0b23 (Meirmans and van Tienderen, 2004) because it is free of population genetic
assumptions in contrast to STRUCTURE. Individuals were clustered based on their allele
frequencies according to the pseudo-F-statistic of Calinski and Harabasz (1974) as described
in Meirmans (2012). Finally, we estimated gene flow among subspecies based on FST and the
private alleles approach of Barton and Slatkin (1986) using GenePop (see Slatkin and Barton,
1989; Whitlock and McCauley, 1999).
3.3.3.2 Mitochondrial DNA
Relationships among mitochondrial haplotypes were analysed using statistical
parsimony/TCS (Clement et al., 2002) implemented in PopART (Leigh and Bryant, 2015)
and MrBayes 3.2.6 (Ronquist et al., 2011), respectively. MrBayes was run using GTR+I+G
identified as best fitting substitution model by jModeltest 2.1.4 (Darriba et al., 2012) with
default settings over 2 million generations with a 25% burnin. Effective sample sizes were >
700, potential scale reduction factors equalled 1.000 or 1.001, and the standard deviation of
split frequencies was < 0.006 indicating convergence of parameter estimates and both parallel
runs.
3.4 Results
The nominate subspecies had the highest diversity despite the lowest sample size, while A. a.
gillae had comparatively lower diversity than the nominate subspecies (Table 3.3). A. a.
antigone had four private alleles, two of them rare (only in one individual each and only
heterozygous), A. a. gillae five, four of them rare (each in not more than 2 specimens and
only heterozygous), and A. a. sharpii eight.
60
Table 3.3 PCR specifications and diversity of microsatellite loci. The subspecies are abbreviated by
the first three letters (ant: A. a. Antigone; gil: A. a. gillae; sha: A, a. sharpii)
N alleles Gene diversity Allelic richness
Locus/dye
MgCl2
[mM]
T
[°C] ant gil sha ant gil sha ant gil sha
Gamµ3/FAM 1.5 59 5 2 5 0.839 0.115 0.768 4.741 1.570 4.364
Gamµ18/HEX 1.5 53 2 1 1 0.321 0.000 0.000 1.993 1.000 1.000
Gamµ24/HEX 2.25 60 7 5 5 0.567 0.227 0.534 4.000 2.290 3.291
Gamµ101b/HEX 2 59 8 2 7 0.821 0.393 0.799 5.399 1.985 5.048
GjM8/FAM 2 59 5 2 3 0.125 0.115 0.425 1.750 1.570 2.526
GjM13/HEX 2 60 5 2 4 0.875 0.488 0.591 4.849 1.999 3.209
GjM15/FAM 2 59 6 4 4 0.696 0.623 0.494 2.999 3.289 3.225
GjM48b/HEX 2 56 4 2 4 0.393 0.040 0.458 1.999 1.240 2.966
GR22/HEX na 60 5 2 4 0.491 0.487 0.412 2.749 1.999 2.980
GR25/Cyanine3 na 60 3 3 2 0.339 0.486 0.496 1.993 2.237 1.999
Mean 5.0 2.5 3.9 0.547 0.297 0.498 3.247 1.918 3.062
Of these, five were rare (each in not more than three individuals and four only heterozygous).
Three of the private alleles occurred only in Myanmar and another three in both Cambodia
and Thailand. The single A. a. luzonica sampled had one allele that did not occur in any other
subspecies. Deviations from the Hardy-Weinberg equilibrium at several loci in A. a. antigone
and A. a. sharpii suggested that these subspecies are probably not panmictic. The same was
true analysing the samples by country (data not shown). This was confirmed from the results
of analysis using STRUCTURE and K-means clustering.
According to Evanno et al.’s (2005) ΔK criterion and assuming correlated allele frequencies,
STRUCTURE identified three clusters, modelling independent allele frequencies only two
(Fig. 3.3; cluster composition as summarized by CLUMPAK Table 3.4).
61
Table 3.4 Cluster analyses (codes from Table 3.2 above).
Bayesian clustering assuming population admixture
k-means clustering Correlated allele frequencies
Independent allele
frequencies Aus01 Cam05 Cam01 Aus01 Cam01 Aus01 Aus08
Aus02 Cam06 Cam02 Aus02 Cam02 Aus02 Aus20
Aus03 Cam08 Cam03 Aus03 Cam03 Aus03 Cam01
Aus04 Cam13 Cam04 Aus04 Cam04 Aus04 Cam02
Aus05 Cam14 Cam07 Aus05 Cam05 Aus05 Cam03
Aus06 Ind01 Cam09 Aus06 Cam06 Aus06 Cam04
Aus07 Ind02 Cam10 Aus07 Cam07 Aus07 Cam05
Aus08 Ind03 Cam11 Aus08 Cam09 Aus09 Cam06
Aus09 Ind04 Cam12 Aus09 Cam10 Aus10 Cam07
Aus10 Ind05 Mya03 Aus10 Cam11 Aus11 Cam09
Aus11 Ind06 Mya06 Aus11 Cam12 Aus12 Cam10
Aus12 Ind07 Tha01 Aus12 Cam13 Aus13 Cam11
Aus13 Ind08 Tha03 Aus13 Cam14 Aus14 Cam12
Aus14 Mya01 Tha04 Aus14 Ind02 Aus15 Cam13
Aus15 Mya02 Tha05 Aus15 Ind04 Aus16 Cam14
Aus16 Mya04 Tha06 Aus16 Ind05 Aus17 Ind01
Aus17 Mya05 Aus17 Ind06 Aus18 Ind02
Aus18 Mya07 Aus18 Ind07 Aus19 Ind03
Aus19 Mya08 Aus19 Ind08 Aus21 Ind04
Aus20 Mya09 Aus20 Mya01 Aus22 Ind05
Aus21 Mya10 Aus21 Mya02 Aus23 Ind06
Aus22 Mya11 Aus22 Mya03 Aus24 Ind07
Aus23 Tha02 Aus23 Mya04 Aus25 Ind08
Aus24 Tha07 Aus24 Mya07 Cam08 Mya01
Aus25 Tha08 Aus25 Mya08 Phi01 Mya02
Phi01 Cam08 Mya09 Mya03
Ind01 Mya10 Mya04
Ind03 Mya11 Mya05
Mya05 Tha01 Mya06
Mya06 Tha02 Mya07
Phi01 Tha03 Mya08
Tha04 Mya09
Tha05 Mya10
Tha06 Mya11
Tha07 Tha01
Tha08 Tha02
Tha03
Tha04
Tha05
Tha06
Tha07
Tha08
62
Fig. 3.3 Bayesian cluster analyses of microsatellite data (STRUCTURE/CLUMPAK). A, B: assuming
admixture and correlated allele frequencies; y axis, membership coefficient from 0 (bottom) to 100
(top); in A, individuals are sorted by subspecies and country of origin; in B, samples are ordered by
cluster, subspecies within clusters and membership coefficient Q (y-axis). For A. a. sharpii, the
country of origin is indicated by the first letter (C = Cambodia, M = Myanmar, T = Thailand). C:
assuming admixture and independent allele frequencies, samples ordered by subspecies and country
of origin within A. a. sharpii. Cluster 1 consists of all A. a. gillae as well as specimens labelled with 1.
In both analyses, all A. a. gillae fell into one cluster together with the A. a. luzonica
specimen. Assuming independent allele frequencies, the cluster with these subspecies also
contained three specimens of A. a. sharpii and two Indian individuals. For both models, a
solution with four clusters had the highest likelihood but the composition of the clusters was
less meaningful, apart from grouping all Australian individuals together. K-means clustering
also divided the sample set into two clusters (Table 3.4), one consisting of 23 A. a. gillae, one
63
A. a. sharpii, and the single A. a. luzonica, and the other of two A. a. gillae, all A. a. antigone
from India, and the remaining A. a. sharpii. Both Bayesian clustering (assuming admixture
and independent allele frequencies) as well as K-means clustering converged to very similar
solutions. The STRUCTURE bar plots also reflect the higher genetic diversity in the Asian
subspecies as summarized by the standard population genetic parameters above and in Table
3.2.
Differentiation among subspecies based on FST estimates revealed that A. a. antigone and A.
a. sharpii were considerably closer to each other (FST = 0.086) than either were to A. a. gillae
(FST = 0.282 and 0.168, respectively). These FST values translated into gene flow estimates of
2.66 migrants per generation between A. a. antigone and A. a. sharpii, 0.64 between the
nominate subspecies and A. a. gillae, and 1.24 between A. a. sharpii and A. a. gillae. The
private alleles approach estimated 0.71, 0.44, and 0.53 migrants, respectively. This again
emphasises the somewhat isolated position of the Australian subspecies.
The alignment of the control region 2 sequences comprised 1155 positions. A major
difference between A. rubicunda and A. antigone were two indels comprising 46 and 95
positions, respectively, which were present in the former and absent in the latter species.
Apart from these, A. rubicunda differed by at least 28 mutations from A. antigone, rendering
the latter monophyletic in the Bayesian tree reconstruction (Fig. 3.4), which is also illustrated
by the TCS network (Fig. 3.5).
64
Fig. 3.4 Phylogenetic tree for three subspecies of the Sarus Crane A. Antigone; based on mtDNA
sequences resulting from Bayesian analysis. Posterior probabilities are given if > 0.70 (for sample
codes see Ch. III Table 2; outgroup (A. rubicunda) pruned off.).
65
Fig. 3.5 TCS network for five populations of the Sarus Crane A. antigone based on mtDNA sequences
compared to the Brolga A. rubicunda (for sample codes see Table 3.2)
However, both tree and network agreed that no subspecies of A. antigone was monophyletic.
Both reconstructions suggested an ancestral polymorphism and/or repeated introgression,
meaning that there had been at least limited gene flow among the subspecies. Given the
overall low differentiation across A. antigone, resulting in low posterior probabilities (i.e.
node support) and the low sample size of the nominate subspecies, inferring evolutionary
trajectories is not possible.
66
3.5 Discussion
Our analyses differ from earlier work (Woods and Krajewski, 1996; Jones et al., 2005) by
having a larger sample size and in sequencing a highly variable part of the mitochondrial
control region (Krajewski et al.,2010) instead of protein coding genes (Woods and
Krajewski, 1996), thereby providing better phylogenetic resolution. Similarly to Woods and
Krajewski (1996), we found that Sarus Crane subspecies and populations were not
monophyletic (probably due to an ancestral polymorphism and/or introgression) and
microsatellite variation in A. a. antigone and A. a. sharpii overlapped significantly (Jones et
al. 2005). However, we have established that A. a. gillae is far more distinct from A. a.
antigone and A. a. sharpii than previously thought, irrespective of the clustering method and
the model assumptions used in Bayesian clustering. This was also confirmed by F-statistics
and gene flow estimates. We have also shown that the single A. a. luzonica specimen we have
hitherto been able to sample was more similar to A. a. gillae than the geographically closer A.
a. sharpii. The first finding has potential implications for definitions of subspecies, the
second in relation to better understanding the phylogeography of the species and potential
sourcing of birds for any Philippine reintroduction. We are well aware how problematic any
conclusions based on a single specimen might be but given that Philippine Sarus Cranes are
extinct and the scarcity of museum material, no alternative approach is available.
Given there are now attempts to define subspecies under law (Mallett et al., 2018), there is a
need for far greater understanding of just how much weight should be given to genetic data,
particularly where genetic variation appears to be lacking. While patterns of crane
morphological variation have not been reflected in marked genetic differences between
populations (Rhymer et al., 2001; Haase and Ilyashenko, 2012; Mudrik et al., 2015), the
findings of Jones et al. (2005) could have been used to suggest that the variation in Sarus
67
Cranes is clinal without distinct breaks in genetic variability. Our results suggest that simply
by looking at a slightly different part of the genome with a larger sample size a different
conclusion would have been drawn. This is relevant for current Australian policy, which has
not been consistent. For example, Schodde and Mason (1999) diagnosed new subspecies of
Southern Emu-wren Stipiturus malachurus and Eastern Bristlebird Dasyornis brachypterus
on the basis of morphological discontinuities. Despite genetic differences in the emu-wren
failing to match morphology (Donellan et al., 2009), threatened subspecies continue to be
recognised under legislation (Department of Environment & Energy, 2018). A similar level
of variation in the Eastern Bristlebird (Roberts et al., 2011) has meant that there has been no
recognition of the northern form of Eastern Bristlebird D. b. monoides (Schodde and Mason,
1999), of which 40 individuals are thought to survive (Stone et al., 2018) but for which
conservation effort has been inconsistent (Guerrero et al., 2017). Were rigid definitions of
subspecies enforced by law, as now being argued in the USA (Mallett et al., 2018), with the
level of knowledge previously available from Jones et al.(2005), Sarus Crane subspecies
might not have been eligible for conservation as separate subspecies. Our results confirm the
position of Patten and Remsen (2017) that synonymising subspecies can be highly
problematic without testing hypotheses using multiple data sources, as advocated by
integrative taxonomy (Dayrat, 2005). We therefore wish to stress that our findings are not a
final verdict on phylogeographic differentiation in the Sarus Crane, which requires further
morphological and genetic work to complement our analyses.
Although first formally noted in Australia in the 1960s (Gill, 1967), Sarus Cranes have been
in the country long enough to have been given a Wik (Cape York Aboriginal language group)
name, meaning ‘the Brolga that dipped its head in blood’ (Reardon 2007). Wood and
Krajewski (1996) have suggested that Sarus Cranes first arrived in Australia 37,500 years
68
ago, when sea levels were 40 m lower than today (Zong et al., 2002), permitting development
of a savanna corridor that extended both north and south of the equator across the Sunda plain
(Bird et al., 2005), much of which would have been lost by rising sea levels at the start of the
Holocene (about 10,000 years ago). In an Australian context, this corridor (Joseph et al.,
2019) would have ended not far north of the Pleistocene Lake Carpentaria, around which it is
thought there would have been savannas structurally similar to those used by Sarus Cranes in
northern Australia. It is also true that lower sea levels would have narrowed the distance
between the Philippines, Borneo/Peninsula Malaya (via Palawan) and Indochina (Voris,
2000) and hence potentially also brought A. a luzonica and A. a. sharpii into closer
proximity. However, especially given the shifting of the courses of the Mekong (Attwood and
Johnston, 2001) it is likely that facing coastal regions of both Indochina and the Philippines
would have been mainly comprised of closed forest, making sub-specific contact more
difficult.
3.6 Conclusions and Recommendations
We have shown that A. a. gillae differs significantly from the A. a. antigone and A. a. sharpii
genetic cline described by others. Where once A. a gillae might have been considered part of
this cline, more detailed analysis has revealed greater structure. This has relevance to the
wider debate about subspecies, suggesting that the level of genetic analysis required before
subspecies are dismissed needs to be carefully considered, and wherever feasible triangulated
with information gleaned from other character traits.
That the single sample from A. a luzonica clustered with A. a. gillae hints at the potential for
a close evolutionary relationship. Should reintroduction of Sarus Cranes to the Philippines be
deemed desirable and viable, subject to further research on the genetic affinities of A. a.
luzonica, Australia might be an appropriate source of birds.
69
Whilst Hachisuka (1941) found that Philippine birds were significantly smaller than those on
the south-Asian mainland, the general case for insular dwarfism is equivocal (van der Geer et
al., 2010). As we had access to only one individual of A. a. luzonica, further genetic work on
samples from Philippine museum specimens could help to clarify the status of this subspecies
and its potential to shed further light on the phylogeography of Sarus Cranes.
70
CHAPTER 4 – THE EXTENT AND TRAJECTORY OF
INTROGRESSION
The Sarolga: conservation implications of genetic and visual
evidence for hybridization between the Brolga Antigone
rubicunda and the Australian Sarus Crane Antigone antigone
gillae. [Oryx, doi:10.1017/S003060531800073X].
4.1 Abstract
In order to investigate the extent of suspected hybridisation between the Brolga, Antigone
rubicunda, and Australian Sarus Crane, A. antigone gillae, first noted in the 1970s, the
genetic diversity of 389 feathers collected from breeding and flocking areas in north
Queensland, Australia was analysed. These were compared with 15 samples from birds of
known identity or which were phenotypically typical. Bayesian clustering based on ten
microsatellite loci identified nine admixed birds (Q = 0.1-0.9) confirming that Australian
cranes do hybridize in the wild. Four of these were backcrosses, also confirming that wild
Australian crane hybrids are fertile. Genetic analyses identified ten times more hybrids than
our accompanying visual field observations.
The analyses also provided the first definitive evidence that both Brolgas and Sarus Cranes
migrate between the Gulf Plains, the principal breeding area for Sarus Cranes, and major non-
breeding locations on the Atherton Tablelands. It is suggested that genetic analysis of shed
feathers might potentially provide a cost-effective means to provide ongoing monitoring of
this migration.
71
The first observations of hybrids coincided with significantly increased opportunities for
interaction when foraging on agricultural crops, which have developed significantly in the
Atherton Tablelands flocking area since the 1960s. As the Sarus Crane is declining in much
of its Asian range, challenges to the genetic integrity of Australian Sarus Crane populations
have international conservation significance.
4.2 Introduction
4.2.1 Background
Hybridisation between what would appear to be well differentiated species is a commonly
observed phenomenon and widely studied in the context of speciation and reproductive
isolation among species (Arnold, 1997; Pennisi, 2016). Hybridisation has a range of
evolutionary consequences depending on the fitness of the hybrids, which may range from
sterility and reduced fertility, to hybrid vigour or heterosis, where hybrid individuals perform
better and out-compete parental species (Burke and Arnold, 2001; Pennisi, 2016). As a
consequence, if species are rare and locally confined (Rhymer and Simberloff, 1996), genetic
mixing can lead to extinction of one or even both parental species (Todesco et al., 2016).
Eventually, hybridisation can lead to speciation where two parental species gives rise to a
new species (Dowling and Secor, 1997; Soltis and Soltis, 2009), highlighting the relevance of
studying hybridisation from the perspective of conservation biology. Allendorf et al. (2001)
noted that taxa which have arisen through natural hybridisation clearly warrant protection.
However, they also noted that increased anthropogenically-related hybridisation is causing
extinction of many taxa (species, subspecies and locally adapted populations) by both
replacement and genetic mixing; going on to argue that hybrid taxa resulting from
anthropogenic causes should therefore be protected only in exceptional circumstances. It is
not yet known if Brolga/Sarus Crane hybrids have arisen as a result of anthropogenic habitat
72
change nor if agricultural and conservation policy has the potential to curtail this; but it is
clearly an important matter for careful consideration. The starting point for this is gaining an
appreciation of its scale. Depending on the interaction of parental alleles and their dominance
patterns as well as epistatic effects, hybrid individuals need not be phenotypically
intermediate between their parents (Rieseberg et al., 1999). Introgression of alleles from one
species into the other also need not be symmetrical, as demonstrated in many cases of
mitochondrial introgression (Toews and Brelsford, 2012). On the nuclear level, genomic data
indicate that hybridisation and introgression interacting with recombination and selection
result in much more complex pictures of genetic diversity (Payseur and Rieseberg, 2016).
Secondary contact of taxa which are well differentiated in allopatry may result in
hybridisation (Grant and Grant, 2016; Vijay et al., 2016), even among non-sister species
(Koch et al., 2017). Such a situation is encountered for the two Australian cranes Antigone
rubicunda, the Brolga (see Fig. 4.1) and A. antigone gillae, the Australian subspecies of the
Sarus Crane (see Fig 4.2).
Fig. 4.1 Typical Brolga with unfledged chick (Gulf Plains); showing small red skull-cap type comb,
dark wattle and grey legs; with scalloped plumage [Photograph: T. Nevard]
73
Fig. 4.2 Typical Australian Sarus Cranes with first year juvenile (Atherton Tablelands), showing pink
legs, red comb extending down the neck, whitish crown and darker grey colour. [Photograph: T.
Nevard]
Krajewski et al. (2010) calculated that the Brolga, which is endemic to Australasia (Australia,
New Guinea), probably split from a common ancestor with the Sarus Crane between 3.3 and
4.9 million years ago (mya). Sarus Cranes, which have a range that includes South and South-
east Asia (see Fig 4.3 below), were only noticed in Australia in the 1960s (Gill, 1967), but
were thought to have been isolated from Asian populations for up to 37,500 years (Wood and
Krajewski 1996); whereas Nevard et al. (2019b) calculate that this isolation was probably
closer to 28,000 years.
74
Fig. 4.3 Global distribution of Brolga Antigone rubicunda and Sarus Crane Antigone antigone (A),
field data collection sites in northern Queensland (B, C and D). Distribution data derived from
BirdLife International and NatureServe Bird Species Distribution Maps of the World (2014) and the
Australian Bird Guide (2017). Gulf Plains Interim Biological Regionalisation Area (IBRA) derived
from Department of Environment and Energy (2012) and state roads from Department of Transport
and Main Roads (2016).
Hybridisation between the Brolga and Sarus Crane was first noted in French aviculture in
1934 (Gray, 1958), when fertile hybrids between the Brolga and the Southeast Asian
subspecies of the Sarus Crane A. a. sharpii, were produced. In 1972, when observing flocking
behaviour of Brolgas and Sarus Cranes on the Atherton Tablelands in Queensland, Archibald
(1981) identified at least two and possibly six potential hybrids (for which he coined the
75
name ‘Sarolga’) and speculated that, if hybridisation were to increase, introgression could be
significant in the conservation of cranes in Australia. Similar concerns led Jones et al. (2005)
to recommend monitoring of the genetic integrity of Australian Sarus Cranes. This research is
the first to confirm and quantify the extent of natural hybridisation between the Brolga and
Australian Sarus Crane.
4.2.2 The Brolga
In Australia, Brolgas occur across northern Australia in Queensland, the Northern Territory
and Western Australia, and extend as far south as Victoria, where they are threatened
(Marchant and Higgins, 1993; Fig. 4.3A). In Queensland, they have been recorded
throughout the state (Marchant and Higgins, 1993) but are now only widespread and
abundant in the north. While breeding occurs throughout their Queensland range (Marchant
and Higgins, 1993; Barrett et al., 2003), it appears to be focused on the grasslands and open
savanna woodland of the Gulf Plains, south-east of the Gulf of Carpentaria and in Cape York
Peninsula. Scattered breeding occurs elsewhere, with flocking (non-breeding) regions
including the Atherton Tablelands and south of Townsville on the north-east coast of
Queensland (Lavery and Blackman 1969).
The Brolga population in northern Australia is generally considered stable and was estimated
to comprise of 20,000-100,000 individuals (Meine and Archibald 1996). A total of 51,969
Brolgas were recorded by Kingsford et al. (2012); all but 135 of these being in northern
Australia. This number should be treated with caution, as the count would also have included
Sarus Cranes and as cranes occur away from wetlands, these would not have been well-
counted. The only longitudinal counts are from north-east Queensland (Atherton Tablelands
and Townsville regions); with an annual average of approximately 800 individuals recorded
76
by community-based naturalists over 21 years between 1997 and 2017; with a peak of
approximately 2,000 in 2005. (E. Scambler, pers. comm.).
The dispersal patterns of Brolgas and movements across their range are poorly understood,
including Queensland (Marchant and Higgins, 1993). Brolgas undertake seasonal movements
between breeding and non-breeding (flocking) habitats in response to rain and flooding
(Marchant and Higgins, 1993). Flocks are formed during the dry season and pairs disperse to
breeding sites in the wet season. Although a body of work is beginning to build in the south
of its range, especially in Victoria (Harding, 2001; Herring, 2005, 2007), knowledge of the
behaviour and ecology of tropical Brolgas remain largely confined to earlier studies such as
those of Hughes and Blackman (1969). Brolgas can use brackish waters, having a unique salt-
gland, and when observed with sarus cranes near Normanton, Brolgas favoured deeper,
generally coastal marshes (Walkinshaw, 1973). However, they do also occur in open forest
and woodland, grassland and cultivated land (Lavery and Blackman, 1969).
4.2.3 The Australian Sarus Crane
While the Sarus Crane is primarily a south Asian species, it is extinct in the Philippines,
declining in much of its Asian range, particularly in Burma, Thailand and Indochina (Meine
and Archibald, 1996; Archibald et al., 2003) and is classed as Vulnerable by the IUCN. The
Australian Sarus Crane population is therefore of international conservation significance and
hybridisation with the Brolga could potentially be a threat to the genetic integrity of the
Australian subspecies.
Sarus Cranes in Australia are almost entirely confined to Queensland (Fig. 3A, with known
breeding areas along the Gulf Plains and on the Normanby River floodplains in Eastern Cape
York Peninsula (Marchant and Higgins, 1993; Barrett et al., 2003; Franklin, 2008). Most
breeding records are from the Gulf Plains and concentrated in the Gilbert and Norman River
77
catchments, where cranes make use of both natural and man-made wetlands on cattle
properties (Barrett et al., 2003). The only known major dry season flocking area for Sarus
Cranes is the Atherton Tablelands and its immediate vicinity. Counts of dry season flocks on
the Atherton Tablelands provide the only current estimates of Sarus Crane recruitment rates
available (Marchant and Higgins, 1993, Grant, 2005). An unknown proportion of the Sarus
Crane population remains on the Gulf Plains and the adjacent inland area in the dry season
and therefore utilizes different landscapes and food types during this period, as there are no
significant cropped areas. Migration routes followed by Sarus Cranes to the Atherton
Tablelands from their breeding areas and their habitat usage along the way are currently
unknown. The importance of migration routes is becoming increasingly understood, as
knowledge of breeding and non-breeding locations alone is insufficient to secure the
protection of migratory species (Runge et al. 2014).
Estimates of total numbers of Australian Sarus Cranes have varied from 5,000-10,000
individuals (E. Scambler, pers. comm.), but these have low reliability (Garnett and Crowley,
2000). Annual (unpublished) counts undertaken by local Birdlife Australia members on the
Atherton Tablelands (E. Scambler, pers. comm.) range between 800 and 1,500 individuals
flocking in dry seasons from 1997-2017 but it is currently not known what proportion of the
total Australian Sarus Crane population these birds represent. Estimates of current population
trends in Australia do not yet exist (E. Scambler, pers. comm.), but it is thought that Sarus
Crane numbers have risen from perhaps as few as 200 on the Atherton Tablelands in the late
1960s (G. Archibald, unpubl. obs.).
4.2.4 Aims
Although the presence of putative hybrid cranes on the Atherton Tablelands has been noted
by experienced observers for many years, it was hypothesised that it was possible that these
78
were non-hybrid birds; exhibiting intrinsic phenotypic variability. Testing the degree of
introgression (if any) in the crane population, as well as providing a benchmark for its future
measurement both visually and genetically was therefore important. To achieve this, it
needed to be understood whether birds with the visual characteristics that had drawn
observers to believe that they were hybrids (Sarolgas) supported this assumption.
Against this background, we aimed to: (i) establish the extent of hybridisation between
Australian Sarus Cranes and Brolgas using molecular methods; (ii) seek evidence from these
genetic data for the presumed connectivity of breeding and flocking areas in the Gulf Plains
and Atherton Tablelands; (iii) describe the distribution of individuals with hybrid
characteristics on the Atherton Tablelands; and (iv) discuss the results, primarily with respect
to their relevance to biological conservation of the two species in Australia.
4.3 Methods
4.3.1 Field observations and sample collection
Over a three year period from July 2013 to June 2016, observations of cranes were made on
fifty-one 334.7 km circuits that encompassed 46 foraging sites distributed across all known
crane flocking areas of the Atherton Tablelands (Fig. 4.3D and Fig. 4.5) and readily visible
from the road. At each site counts were made of adult and first year juvenile Brolgas and
Sarus Cranes, using a pair of 10x40 binoculars; with potential hybrids (see Fig. 4.4) visually
examined with a 50x magnification spotting scope. As individuals could not be distinguished,
birds were probably counted on multiple occasions and at different sites. However, enough
cranes were counted that there is no reason to suspect systematic bias in the estimate of the
proportion of visually distinguishable hybrids amongst the wider crane population.
79
Fig. 4.4 Heads and necks of typical species phenotypes and presumed hybrids. A: typical Brolga; B:
Sarolga (this bird was congruent with a typical Brolga, except that it had pink legs, slightly more red
on the nape of the comb than is typical of Brolgas, and a very small, almost non-existent wattle. This
combination of characters had not hitherto been recorded); C: typical Sarolga, with much shorter neck
comb and slight wattle; D: typical Australian Sarus Crane. [Photos A, C and D: T. Nevard; Photo B:
Brian Johnson].
The initial identification of hybrids was based on the presence of at least four readily-
observable characteristics (including at least two of (i), (iv) and (vi)) in Archibald’s (1981)
typology of Sarolgas: (i) larger and heavier than either parent species; (ii) an irregular border
to the comb; (iii) notches in the cap; (iv) intermediate or mixed-colour legs, (iv) a scalloped
mantle; (v) brighter yellow eyes than typical Sarus Cranes (which are more orange); and (vi)
a small wattle. Although Archibald’s (1981) Sarolga typology was helpful, in overall
appearance the Sarolgas he describes are more like atypical Sarus Cranes than atypical
Brolgas, whereas putative hybrids looking more like atypical Brolgas were also observed
(Fig. 4.4B).
80
In May 2014, freshly-shed feathers were collected opportunistically from Miranda Downs
cattle station (17°19.755’S/141°52.770’E, elevation 55 m) on the Gulf Plains and in
September 2015 from Innot Hot Springs (17°43.749’S/145°16.302’E, elevation 628 m) on
the southern edge of the Atherton Tablelands (Fig. 4.3C). Only feathers with minimal
contamination from soil and vegetation were selected and picked-up from dry ground with
forceps, then immediately placed in sealed plastic bags and refrigerated prior to analysis.
4.3.2 Molecular analysis
A total of 389 feathers were collected and prepared for genotyping. This included 187 from
the Gulf Plains, 202 from the Atherton Tablelands, and 15 samples (blood, feathers) from
reference birds, which were either phenotypically typical or for which a potential history of
contact with the other species could be excluded or minimised (3 A. a. antigone, 7 A. a.
gillae, 5 A. rubicunda (see Table 4.1); note that including the non-Australian A. a. antigone in
the reference collection makes no difference to the veracity of the comparison with Brolgas).
Table 4.1 Reference birds. Samples were either taken from living and recently dead wild birds which
were phenotypically typical or from birds whose lineages of descent were known not to have had
contact with the other species. N: number of specimens.
Species N Locality Notes
A. a. antigone 3
Lemgo Avicultural
Collection, Germany
Breeding records show no interbreeding
with other Sarus Crane subspecies since
their ancestors were collected from the wild
in the 1970s.
A. a. gillae 5 Lemgo Avicultural
Collection, Germany
Breeding records show no interbreeding
since their ancestors were collected from the
wild in the 1970s.
A. a. gillae 2 Kairi, Queensland
Wild birds; phenotypically typical Sarus
crane.
A. rubicunda 3 Cairns Tropical Zoo,
Queensland
Breeding records show no interbreeding
since collected from a wild population with
no history of contact with Sarus Cranes.
A. rubicunda 2 Herbert River, Atherton
Tablelands, Queensland Wild birds; phenotypically typical Brolga.
81
DNA was extracted using the slightly modified SDS/salting-out protocol of Miller et al. (in
press [accepted for publication in Avian Biology Research 21/08/2018]). In order to increase
the yield, dithiothreitol and Roti®-PinkDNA (Carl Roth®, Karlsruhe, Germany) were added.
Initially, the 22 microsatellite loci were tested which had been successfully used in other
species of crane (Hasegawa et al., 2000; Meares et al., 2009) as well as the Sarus Crane
(Jones, 2005) and the Brolga (Miller, 2016). Of these, ten could be consistently amplified and
scored (Table 4.2). PCRs were conducted in a volume of 10 µl and contained 1 µl DNA (10-
25 ng), 1 µl of 10 x NH4-based Reaction Buffer, 1.5-2.25 mM MgCl2 Solution (see Table 2
below), 0.25 mM of each primer, 0.2 mM of dNTP, 0.04 µl of BioTaq DNA Polymerase (5
U/µl), 0.6 µl of 1 % BSA and sterile ddH2O. For two loci, GR22 and GR25, we used the
MyTaqTM
mix (all products from BIOLINETM
, London, UK).
Table 4.2 PCR specifications and diversity of microsatellite loci. Dye, fluorophore at 5’-end
of forward primer; MgCl2, concentration of magnesium chloride (mM); N alleles, number of
alleles; T, annealing temperature (°C); gene diversity was estimated according to Nei (1987)
and allelic richness following Petit et al. (1998). Loci that could not be consistently amplified
or scored: Gamµ2, Gamµ5, Gamµ6, Gamµ7, Gamµ9, Gamµ12, Gamµ21, Gamµ102, GjM11,
GjM34, GjM40, GR17 (Hasegawa et al. 2000; Meares et al. 2009; Miller, 2016).
N alleles Brolga Sarus Brolga Sarus
Locus/dye
MgCl
2 T Brolga Sarus Gulf Table Gulf Table Gulf Table Gulf Table
Gamµ3/FAM 1.5 59 7 6 0.618 0.654 0.162 0.229 6.994 6.965 3.183 2.875
Gamµ18/HEX 1.5 53 3d 1 0.224 0.363 0.000 0.000 2.943 3.000 1.000 1.000
Gamµ24/HEX 2.25 60 5 5d 0.578 0.628 0.204 0.338 4.943 4.998 3.732 4.000
Gamµ101b/HEX 2 59 4 3 0.173 0.203 0.349 0.326 3.000 2.566 2.273 2.999
GjM8/FAM 2 59 3 3 0.159 0.265 0.157 0.125 2.996 2.910 2.254 2.000
GjM13/HEX 2 60 5d 3
d 0.722 0.557 0.498 0.042 5.000 3.815 2.276 1.875
GjM15/FAM 2 59 9 5 0.794 0.757 0.552 0.539 8.994 8.251 4.422 4.000
GjM48b/HEX 2 56 8d 6
d 0.559 0.571 0.160 0.362 6.999 7.853 3.039 3.862
GR22m/HEX na 60 11
d 5 0.625 0.566 0.448 0.434 7.937 8.430 2.575 2.875
GR25m/Cyanine3 na 60 5 3 0.727 0.741 0.512 0.442 5.000 5.000 2.996 2.000
d heterocygote deficiency;
m multiplexed
82
The PCR profile comprised an initial denaturation at 94 °C, 36 cycles including denaturation
at 94 °C, primer specific annealing (Table 4.2) and extension at 72 °C each for 30 s, and a
final elongation at 72 °C for 10 min. Microsatellite alleles were separated on a 3130xl
Genetic Analyzer, together with the GeneScanTM
600 LIZ® Size Standard 2.0. Fragment
sizes were determined manually in order to avoid the inconsistencies in automatic calling due
to the arbitrariness of bin width definitions using GeneMapper® 4.0 (all three products from
Applied Biosystems®, Waltham, USA). In order to control accuracy of size determination,
PCRs of samples were repeated which initially gave weak signals or had rare variants. In
other cases, problematic PCR samples that were initially typed in different runs, so possibly
difficult to calibrate, were loaded on the same plate to improve comparability.
As there was the possibility that feathers of a particular bird were collected more than once,
identical genotypes were identified using Cervus 3.0.7 (Kalinowski et al., 2007).
Consequently, 41 samples (16 Gulf Plains, 24 Atherton Tablelands, 1 captive reference A. a.
gillae that was identical to its sibling) were excluded from the following analyses. In eleven
of these cases, the same genotype was found in both localities. In these, the sample from the
Atherton Tablelands was arbitrarily excluded. As only 16.2% of the birds had missing data
and only two of the nine potential hybrids lacked data (at one locus each) this was not
considered problematic. Given the moderate number of markers, it was not possible to
distinguish siblings from non-siblings because genetic variance would be too large.
In order to identify the number of genetic clusters and potential hybrid individuals, Bayesian
clustering was conducted, using STRUCTURE 2.3.4 (Pritchard et al., 2000; Falush et al.,
2007) with K (number of clusters) ranging from one to five and ten replicates assuming the
admixture model and, in different runs, either uncorrelated or correlated allele frequencies.
The Markov chains ran for 550,000 generations including a burn in of 50,000. Pilot runs with
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longer Markov chains yielded identical results. Structure Harvester 0.6.94 (Earl and von
Holdt, 2012) was used to analyse the data following Evanno et al. (2005) and Structure Plot
V2.0 (Ramasamy et al., 2014) and Adobe Illustrator CS4 (Adobe Systems Inc., San José,
California) to render the graphical output. Individuals were defined with admixture Q
between 0.1 and 0.9 as hybrids following Devitt et al. (2011). These thresholds appear
considerably more conservative in the analysis, as ten loci were used and not only three as by
Devitt et al. (2011). However, this restriction was necessary, as the loci they used had species
specific alleles whereas the two species of cranes compared shared some of their alleles.
There was no attempt made to identify different classes of hybrids (F1, F2 and their
backcrosses) because this would have required genotyping at least 50 loci (Fitzpatrick, 2012),
whereas only 10 were available. The Bayesian clustering approach was validated by K-means
clustering, which, in contrast to STRUCTURE, is free of population genetic assumptions,
using GenoDive 2.0b23 (Meirmans and van Tienderen, 2004). Individuals were clustered
based on their allele frequencies according to the pseudo-F-statistic of Calinski and Harabasz
(1974; see Meirmans, 2012).
More detailed population genetic analyses were conducted based on the clusters identified by
Bayesian clustering including descriptive statistics, tests for Hardy-Weinberg-Equilibrium,
linkage disequilibrium, null-alleles and population differentiation, using FSTAT 2.9.3.2
(Goudet, 1995), GenePop 4.2 (Raymond and Rousset, 1995; Rousset, 2008), and Micro-
Checker 2.2 (van Oosterhout et al., 2004). Gene flow was estimated using the formula Nm =
[(1/FST)-1]/4 (Nm, number of effective migrants) as well as based on private alleles, i.e.
alleles occurring only in one subpopulation (Barton and Slatkin, 1986), the latter in GenePop.
Probabilities that two individuals were identical were calculated with Cervus, assuming either
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that the two birds were unrelated or, more conservatively, that they were full siblings (Waits
et al., 2001). In multiple tests, α was Bonferroni corrected.
4.3.3 Lincoln Petersen Index
The Lincoln-Petersen Index was applied to ‘genetically re-trapped’ birds (nGulf x
nTablelands/nboth), based on methodology described by Southwood and Henderson (2000).
4.4 Results
4.4.1 Field observations
Crane observations on the Atherton Tablelands are summarized in Table 4.3 and Fig 4.5.
Table 4.3 The number (and percentage) of cranes observed across 46 sites on the Atherton
Tablelands 2013-2016.
Life history
stage Brolga
Sarus
Crane Sarolga Unidentified¹
Total
cranes
Adults 24,870 (55.8) 12,245 (27.5) 84 (0.2) - 37,199 (83.5)
First year
juveniles 2,491 (5.6) 1,136 (2.5) 0 (0) - 3,627 (8.1)
Total 27,361 (61.4) 13,381 (30) 84 (0.2) 3,728 (8.4) 44,554 (100)
¹Due to poor weather/light conditions
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Fig. 4.5 Pie-charts showing general distribution and clustering of Brolga (blue), Sarus Crane (red) and
Sarolga (open yellow dots) visually identified at 46 observation sites on the Atherton Tablelands
2013-2016. Grey quadrants represent unidentifiable cranes due to poor light and weather conditions.
Out of 40,826 cranes identifiable to species level (out of a total of 44,554 observations), only
84 were classified as morphologically intermediate Sarolgas (0.205 %). Variation among
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these intermediate birds meant it was not possible to assess the extent of potential
hybridisation (see Fig. 4.4).
Observations of visually identifiable hybrids on the Atherton Tablelands were concentrated in
a relatively small number of areas (see Fig. 4.5), such as Innot Hot Springs, Tumoulin/Kaban,
Hastie’s Swamp and the Mareeba Wetlands. Figure 4.5 also demonstrates that although they
occur in mixed flocks, Brolgas and Sarus Cranes are differentially distributed across the
Atherton Tablelands; with higher Sarus Crane numbers focused on more fertile volcanic soils
closer to Atherton itself and both Brolgas and putative hybrids predominantly visually
identified on areas of lower intrinsic fertility.
At sites with higher Brolga or Sarus Crane counts, the species with the lesser numbers in the
flock tended to have proportionally more first year juveniles (Table 4.4; Chi2 tests: p <
0.0001 in both cases), potentially increasing opportunities for interactions between species,
whilst juveniles are at a critical age for pair-bonding.
Table 4.4 Proportion of juveniles at sites dominated by either Brolgas or Sarus Cranes.
Brolga Sarus Crane
Total no. % Juvenile Total no. % Juvenile
Brolga-dominated sites 25,510 8.8 2,273 14.5
Sarus-dominated sites 1,851 13.3 11,308 8.9
Total 27,361 9.1 13,581 9.8
4.4.2 Population genetics
In all STRUCTURE analyses, the highest ΔK resulted assuming two clusters and this was
confirmed by k-means clustering. These clusters corresponded well to the species Brolga and
Sarus crane, as indicated by the reference birds (Fig. 4.6) As allele frequencies apparently
differed considerably between the species, we based the subsequent analyses on the
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STRUCTURE model assuming uncorrelated frequencies. While the majority of birds were
either pure Brolga or pure Sarus Crane, some were admixed (Fig. 4.6).
Fig. 4.6 STRUCTURE plot with K = 2 showing admixture among a total of 363 Brolga (blue) and
Sarus Cranes (red) ordered along x-axis by decreasing Q (membership coefficient; y-axis) with Brolga
as reference. Black rectangle includes nine hybrids with Q ranging between 0.9 and 0.1. Bar
underneath indicates origin of birds and reference specimens (green, Atherton Tablelands; orange,
Gulf Plains; blue, A. rubicunda; magenta, A. a. antigone; red, A. a. gillae)
According to the criteria used, 239 samples belonged to Brolgas (90 Gulf Plains, 149
Atherton Tablelands) and 101 to Sarus Cranes (77 Gulf Plains, 24 Atherton Tablelands). Nine
individuals (2.58 %; four Gulf Plains, five Atherton Tablelands) had Q scores ranging from
0.125 to 0.888 (reference: Brolga) and were identified as hybrids (Fig. 6), a proportion about
ten times greater than in field observations. Four hybrids had alleles occurring only in
Brolgas at one or two loci indicating that hybrids are fertile and can interbreed at least with
Brolgas or other hybrids.
After exclusion of reference birds and hybrids, the species were analysed separately,
subdividing both into two subpopulations corresponding to the localities. Genetic diversity is
summarized in Table 4.2. Gene diversity and allelic richness were both considerably higher
in Brolgas. Brolgas also exhibited 26 private alleles, between one and six per locus, whereas
Sarus Cranes had only eight private alleles and four loci did not have any. This translates into
much lower probabilities in Brolgas that two individuals will carry the same genotype than in
Sarus Cranes. The probabilities to find two unrelated individuals with identical genotype
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were 7.1x10-7
for Brolgas and 0.0012 for Sarus Cranes. Assuming the individuals were full
siblings, these probabilities rose to 0.0023 and 0.0395, respectively. In both Brolgas and
Sarus Cranes respectively, four and three loci deviated from the Hardy-Weinberg-
Equilibrium and the same loci had indications of null-alleles. However, this was probably due
to a fairly high number of rare alleles (frequency < 5%) in both species and was therefore not
considered problematic for the analyses. In any case, the general results of the STRUCTURE
analysis did not change after exclusion of these loci. Linkage disequilibrium did not play a
role in either species. In both species, subpopulations were hardly differentiated with FST =
0.010 (confidence interval: 0.003 - 0.020) in Brolgas and 0.047 (-0.006 - 0.136) in Sarus
Cranes. Sample size limited the significance of the result for Brolgas and is probably not
biologically relevant. Estimates of migration based on the private allele method were high in
both species with 6.56 and 7.75 migrants per generation for Brolgas and Sarus Cranes,
respectively. Transforming FST into estimates of migration using the formula Nm = [(1/FST)-
1]/4, 24.75 and 5.07 migrants respectively were inferred.
4.4.3 Lincoln-Petersen Index
In eleven cases, the same genotypes were collected at both Miranda Downs in the Gulf Plains
and Innot Hot Springs in the southern Atherton Tablelands. Of these, nine were attributable to
Brolgas, and two to Sarus Cranes. According to the probabilities of encountering two
individuals carrying identical genotypes by chance with the sample sizes, only the two Sarus
Cranes might be cases of chance identity, provided the respective birds were siblings (see
above). Application of the Lincoln-Petersen Index (nGulf x nTablelands/nboth; Southwood and
Henderson, 2000) to these results implies that at least 1473 Brolgas and 923 Sarus Cranes
could have moved between the Gulf and Atherton Tablelands.
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4.5 Discussion and Conclusions
Since Archibald’s first observation of hybrids in 1972 (Archibald, 1981), local observers
have continued to note the presence of apparent hybrids amongst dry season, non-breeding
crane flocks on the Atherton Tablelands (Matthiessen, 2002), as well as elsewhere. This
research has shown that natural hybridisation between Brolgas and Sarus Cranes is happening
and occurs more widely than is visually detectable. As hybridisation is still relatively
uncommon and Brolgas and Sarus cranes are differentially distributed on the Atherton
Tablelands (Fig. 4.5), its evolutionary influence could potentially be relatively limited.
However, a closer look at the allele-combinations in the hybrids suggests that introgression
could become more widespread. Four of the birds had alleles that occur only in Brolgas at
one or two loci. While one of these birds had a membership index of 0.5, suggestive of being
an F1-hybrid, these pure Brolga combinations indicate that the birds are hybrids of a later
generation with a hybrid parent that back-crossed with a Brolga or another hybrid. Sarolgas
therefore appear to be fertile at several generational re-combinations.
Longitudinal research on Darwin’s Finches Geospiza spp. has shown that they evolved from
a common ancestor in the Galápagos archipelago in the last two million years (Grant and
Grant, 2008) with both natural selection and introgressive hybridisation key processes in their
evolution. At this stage it is not possible to predict the trajectory of Brolga/Sarus Crane
introgression but Lamichhaney et al. (2016) have demonstrated that introgression at only a
single locus may have important evolutionary consequences. Interaction of introgression and
selection may be complex and locality dependent, as shown for European Crows Corvus
corone (Vijay et al., 2016), where genetic and phenotypic differentiation varies significantly
across its range; with some boundaries firm and others mobile. Ongoing Brolga/Sarus Crane
introgression may provide alleles to either species that could allow them to adapt to
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environmental changes brought about by such stresses as climate change or agricultural
intensification. Whether the larger body size of hybrids identified by Archibald (1981)
confers a selective advantage over the parental species, potentially leading to their
displacement, cannot yet be determined.
The current Australian population of Sarus Cranes appears to have increased relatively
rapidly from what is thought to have been small numbers in northern Australia following its
formal identification in the 1960s (Gill, 1967). Archibald (1981) estimated the Sarus Crane
population was approximately 200 on the Atherton Tablelands in 1972, when he identified at
least two and possibly six potential hybrids between Brolgas and Sarus Cranes (Archibald,
1981). Crops have been grown in northern Australia since the late 19th Century and
expanded substantially on the Atherton Tablelands in the 1960s, soon after Gill’s first Sarus
Crane observation. Templeton et al. (1990) have identified that changes in landscapes can be
associated with genetic consequences, including introgression that threatens species integrity
(e.g. Kakariki Cyanorhamphus spp (Triggs and Daugherty, 1996), Black-eared Miners
Manorina malanotis Clarke et al., 2001). Landscape features and heterogeneity can also be
reflected in population genetic structure within and across species (Miller and Haig, 2010;
Safner et al., 2011) and often changes in landscape are associated with habitat loss,
contributing to population decline and possibly resulting in changes in the genetic diversity of
remaining populations (Keyghobadi, 2007; Templeton et al., 1990).
That the species with the lesser numbers in a mixed-species flock has proportionally more
first year juveniles means that young Brolgas and Sarus Cranes are more exposed to one
another other at a time when imprinting is important (Horwich, 1996). This may make pairing
with the other species more likely. The enduring pair bond and longevity in both species
(Johnsgard, 1983) suggests that, once formed, hybrid pairs could contribute numerous hybrid
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offspring to the population. Although we cannot yet predict the trajectory of crane
introgression in northern Australia, there are clear conservation implications. The Sarus
Crane is thought to be declining in much of its Asian range, particularly in Burma, Thailand
and Indochina (Meine and Archibald, 1996; Archibald et al., 2003). The maintenance of
Australian Sarus Crane populations and their genetic integrity may therefore provide security
for the species should populations continue to decline in Asia. However, there would appear
to be no practical way of eliminating Australian crane introgression in the wild, as: (i) hybrids
are not necessarily visually distinguishable in the field; (ii) Australian cranes occur in remote
and inaccessible areas; and (iii) the underlying behavioural stimuli are not yet understood. If
related to anthropogenically-driven land use change, Brolgas and Sarus Cranes may be
brought into ever-closer and more frequent foraging and flocking proximity, potentially
leading to more hybridisation opportunities. Therefore, should the maintenance of
genetically pure (screened) populations of Australian Sarus Cranes and northern Australian
Brolgas be considered desirable for conservation purposes, one or more well-managed
extralimital populations may need to be established. As far as is known, the only captive
flock of Australian Sarus Cranes is at Lemgo in Germany, whose ancestry dates from a wild
capture in the 1970s. This could potentially form a nucleus for a captive Australian Sarus
Crane captive metapopulation, spread across several institutions. Establishing a flock
managed to maintain its genetic variability at this stage could also serve as insurance against
climate change impacts should these eventuate – with some models predicting a potential
91% decline in climatic suitability for the Australian Sarus Crane by 2085 (Garnett et al.,
2013).
As feathers have been collected from what appear to be the same birds in both the Gulf Plains
and Atherton Tablelands, considering the low probabilities of encountering genetically
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identical individuals, this has confirmed what has hitherto only been assumed by
birdwatchers in North Queensland – that cranes migrate between breeding areas in the Gulf
Plains and the Atherton Tablelands, a distance of about 500 km. As one would expect, there
appears to be no material genetic difference between Gulf Plains and Atherton Tablelands
cranes, indicated by estimates of population differentiation and migration after exclusion of
the duplicate genotypes. The conservation implications of this are significant, as both areas
will need to be targeted with appropriate conservation measures to ensure the survival of
north Queensland’s Brolgas and Sarus cranes. There are currently no laws protecting species
that migrate within Australia (Runge et al., 2017).
The identification of identical birds in both the Gulf Plains and Atherton Tablelands using
shed feathers highlights the potential of genetic analyses to explore migration patterns and
potential trends, not only in Australian cranes but also in other species. Although collection
of feathers was opportunistic rather than deliberately random and estimates using the
Lincoln-Petersen Index therefore necessarily indicative, they are of the same order as other
estimates of crane populations on the Atherton Tablelands (Brolgas 800-2000 counted/1473
calculated; Sarus Cranes 800-1500 counted/973 calculated). Similarly to the use of non-
invasive genetic monitoring techniques elsewhere, such as for large carnivores in Europe
(Kaczensky et al., 2012), genetic analysis of feathers could contribute to the assessment of
population trends and movements of cranes within the Atherton Tablelands and between the
Atherton Tablelands and other locations where either species is found.
Although feathers have the advantage of being a non-invasive means of gathering genetic
data on individuals, as noted by Hou et al. (2018); the probability of detecting hybrids was
over 10 times greater using genetic analysis. However, the boundaries between pure and
hybridised birds are unclear and are probably indefinable, given that hybrids are fertile;
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meaning that introgression may have reached the point where it has no clear thresholds. A
subject of future research could therefore be the definition of the relationship between
genetics and phenological expression, using the feathers of known birds with hybrid
phenotypes; using data from more than the 10 loci available (Fitzpatrick, 2012). In addition,
genomic approaches targeting coding loci (Payseur and Rieseberg, 2016) would provide a
deeper insight into the evolutionary consequences of the hybridisation, as the example of
Darwin’s Finches has shown (Lamichhaney et al., 2016). However, to obtain DNA in the
necessary quantities and quality would require catching many more cranes to obtain tissue
and blood samples.
Whilst acknowledging that the proportion of apparent hybrids identifiable by observers is
likely to be an order of magnitude lower than are actually present in the crane population,
both visual observation and analysis of shed feathers could provide valuable data to help
monitor the trajectory of Australian crane introgression.
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CHAPTER 5 – RESOURCE PARTITIONING AND
COMPETITION
Agriculture, Brolgas and Australian Sarus Cranes on the
Atherton Tablelands.
[Accepted for publication in Pacific Conservation Biology 24/12/2018]
5.1 Abstract
Flocks of Brolgas Antigone rubicunda and Australian Sarus Cranes A. antigone gillae
congregate in cropping areas of the Atherton Tablelands in north Queensland, Australia,
during the non-breeding months of May to December each year and sometimes come into
conflict with farmers. The central part of the region has been declared a Key Biodiversity
Area, largely because it is the only well-known non-breeding area for the Australian Sarus
Crane. The spatial and temporal patterns of use of this landscape were investigated for
foraging by the two species to determine how they might be affected by changes in cropping.
Abundances of the species were positively correlated with each other over both time and
space. Sarus Cranes were nevertheless markedly more abundant on the fertile volcanic soils
of the central Tablelands, whilst Brolgas were more abundant on a variety of soils in outlying
cropping areas close to roost sites, especially in the south-west of the region. Both species
used a wide variety of crops and pastures but occurred at highest densities on ploughed land
and areas from which crops (esp. maize) had been harvested. In addition, Brolgas were also
strongly associated with early-stage winter cereals with volunteer peanuts from the previous
crop. We conclude that maize and peanut crops are important as foraging sites for both
species during the non-breeding season, a situation that requires management in the interest
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of both cranes and farmers, especially as cropping patterns intensify and agricultural
technology changes. However, the mobility and adaptability to agricultural change of most
crane species suggests that Brolgas and Sarus Cranes are also likely to be able to take
advantage of newly created cropping areas.
5.2 Introduction
Most crane species make use of agricultural land for foraging (Harris and Mirande, 2013).
As global food production has expanded to meet rising demand from a growing human
population and increasing personal wealth, some crane populations have benefitted
significantly from the expansion of mechanical harvesting, by foraging on arable land,
especially on grain spilt or remaining after harvest (Meine and Archibald, 1996). However,
emerging technological and agronomic factors are likely to have an impact on some of the
crane species that have adapted to contemporary agricultural practices, potentially leading to
changes in their population, distribution, migration patterns, flocking and breeding success.
Changes in agricultural practice, such as reduction in cropping intervals and improved
harvesting efficiency can lead to dramatic reductions in post-harvest waste grain (Anteau et
al. 2011). In some sites cranes have been forced to seek new food sources at greater distances
from roost sites, resulting in lower reproductive success and increased crop damage (Pearse et
al., 2010, Austin, 2012, Barzen and Ballinger, 2017). Birdlife International (2018a) have
identified that agriculture is the biggest threat to globally threatened birds, with cranes having
a Red List Index (RLI) of 0.71 in 2016; significantly below the 0.91 RLI for threatened birds
as a whole. How cranes adapt to agricultural change is therefore a key conservation issue and
a management consideration for farmers and policy makers in crane range areas (Harris and
Mirande 2013).
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Both Australian crane species interact with agriculture. The Brolga Antigone rubicunda has
disappeared from much of its historical range in southern Australia as a result of agricultural
development and persecution (Arnol et al., 1984) but remains relatively common in
Australia’s tropics (Kingsford et al., 2012) where it has come into conflict with the
agricultural sector in north Queensland since at least the 1930s (Townsville Daily Bulletin,
1935). The Australian Sarus Crane A. antigone gillae breeds primarily on remote pastoral
areas in north Queensland but, along with the Brolga, migrates 500 km to spend the dry, non-
breeding season on the Atherton Tablelands (Archibald and Swengel, 1987; Nevard et al.
(2019b), one of Australia’s most intensively farmed areas. Because the Atherton Tablelands
are so important for the Sarus Crane, which is listed as Vulnerable by the IUCN (Birdlife
International, 2018b), they were a key factor in designation of the Atherton Tablelands Key
Biodiversity Area (Birdlife International, 2018c).
Ecologically Brolgas have traditionally been characterised as a species of freshwater and
brackish wetlands; widely dispersed when breeding but gathering in flocks during the dry
season to feed on sedge tubers in seasonally dry swamps (Herring, 2005; Chatto, 2006;
Herring, 2007; Franklin, 2008). In north Queensland they concentrate, to varying degrees, on
the Atherton Tablelands and east coast marshes (such as near Cromarty, Giru, Townsville and
Ingham), with their unique salt-gland (Hughes and Blackman, 1973) allowing them to exploit
brackish waters. Australian Sarus Cranes tend to avoid coastal wetlands, appearing to prefer
well-drained rather than wetland foraging areas (Lavery and Blackman, 1969). Where the
breeding ranges overlap, Brolgas favoured deeper, generally more coastal, marshes than
Sarus Cranes (Walkinshaw, 1973). However, both species also occur in open forest and
woodland, grassland and cultivation (Lavery and Blackman, 1969).
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Of 51,969 Brolgas recorded nationally by Kingsford et al. (2012), all but 135 were in
northern Australia. Since 1997 between 800 to 1500 Sarus Cranes have been counted
annually on the Atherton Tablelands (E, Scambler, pers. comm.), a number that may have
risen from a comparatively low base in the late 1960s (G. Archibald, pers. comm.), possibly
because arable agricultural development and changing crop patterns increased the availability
of residual unharvested crops.
Based on the experience of other crane ranges, the future of cranes on the Atherton
Tablelands is likely to be influenced by two key elements: a) land use change - through
expansion of cultivation and perennial crops and intensification of cultivation and water
management (Nevard et al. 2019); and b) technological development - through increased
mechanization, automation and agronomic sophistication. Both have the potential to affect
the availability of forage for cranes, especially as they recover from migration to dry
season/wintering habitats and prepare for the following breeding season.
This research seeks to build a platform from which to develop appropriate crane conservation
measures under conditions of changing agronomic practice. The spatial and temporal patterns
of occurrence of cranes are reported at their feeding sites over three non-breeding seasons to
answer three main questions: (i) what are the key habitat parameters, including crop
associations, of crane species; (ii) how do crane species differ in their usage of the study area;
and (iii) what are the implications for crane conservation management?
5.3 Methods
5.3.1 Atherton Tablelands Study Area
The study area encompassed known crane foraging habitat on the Atherton Tablelands (see
Fig. 5.1 below) from north of Mareeba south to Innot Hot Springs. Elevation of the surveyed
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area ranged from 399 to 1,070 m above sea level and with a tropical mid-elevation to upland
climate and strongly seasonal rainfall, ranging from 900 to 2,200 mm. The underlying
geology is granitic and metamorphic in the north and west and volcanic in the centre and
south, with patches of alluvial loam associated with major river systems and peat in dormant
volcanic craters.
Fig. 5.1 Atherton Tablelands region, showing survey sites, irrigated agriculture (Queensland
Government 2016) and the Atherton Tablelands Key Biodiversity Area. Inset shows location of study
region and general distribution of Brolgas and Sarus Cranes in Australia.
As a result of this topographic, climatic and geological variation, as well as its tropical
location, the Atherton Tablelands supports one of Australia’s most diverse biotas (Nix and
Switzer, 1991). It also sustains one of Australia’s largest ranges of both irrigated and non-
irrigated crops (see Table 5.1), contributing gross revenue of over AU$552 million to the
regional economy. Tree crops, are the largest component of the agricultural sector by value,
followed by field crops, animal industries and horticulture (Department of Agriculture and
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Fisheries 2015, Nevard et al., 2018). There is extensive public and private sector irrigation
infrastructure and a relatively dense rural population, many small family farms and a high
diversity of cropping.
Table 5.1 Area and value of agricultural production on the Atherton Tablelands, Queensland
(Department of Agriculture and Fisheries (2015) and Nevard et al. (2018).
Agricultural activity Area (ha)
Gross revenue per hectare
per year (AU$ '000)
Livestock 558,872 0.2 Beef cattle 550,000 0.1
Dairy cattle 8,800 3.9
Pigs and poultry 72 550.4
Field Crops and Horticulture 23,427 4.6
Sugar cane 10,956 3.6
Maize 4,719 2.4
Hay 3,020 1.2
Grass seed 1,195 4.0
Potato 972 16.2
Legume seed 968 3.1
Peanut 874 5.5
Minor field crops 723 35.2
Tree crops and forestry 11,297 27.8
Forestry plantations 3,600 5.6
Minor tree crops 2,497 34.5
Mango 2,400 21.1
Banana 1,850 49.2
Avocado 950 87.3
Miscellaneous 151 577.2
Total 593,747
Water for the Mareeba-Dimbulah Irrigation Area within the Atherton Tablelands region is
supplied from Tinaroo Dam (which has important crane roosting sites along its shoreline)
through an extensive network of channels and streams. Farming enterprises in other parts of
the Tablelands (including intensive agricultural areas around Atherton, Malanda and
Ravenshoe) draw water from natural watercourses, bores and small dams, many of which
provide drinking and roosting opportunities for cranes.
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5.3.2 Field surveys
A 335 km driven traverse, with 46 readily visible crane feeding sites spread widely across the
Atherton Tablelands, was established and data recorded from 44 traverses between July 2013
and December 2015. Traverses were undertaken in the months of May to December
inclusive, encompassing the time cranes are present on the Atherton Tablelands. A mean of
43.0 sites were assessed per traverse, a total of 1,892 site surveys, some site surveys being
missed or curtailed due to weather and the need to vary the timing of site visits. At each site
survey, cranes were counted and identified as Sarus Crane, Brolga, a hybrid of the two
species (Nevard et al. 2019a) or unidentified crane, using 10x40 binoculars and a 50x
spotting scope; with land use recorded as one of 32 crop classes, including current state (e.g.
ploughed, growing, harvested). On a one-off basis for each site, the following parameters
were recorded: area at each site visible from the road and used by cranes, elevation, distance
from dwellings or other buildings with human activity (3 classes), surface geology
(Cainozoic volcanic, metamorphic or alluvial), land use class (cropping, grazing, wetland)
and irrigation status (irrigated or not). All known roosts, identified during annual counts
conducted by Birdlife North Queensland (E. Scambler, pers. comm.), were visited, cranes
counted and then classified as either Brolga or Sarus Crane-dominated. Classification was by
simple majority but most roosts were strongly skewed to one species.
5.3.3 Data analysis
Most cranes were identified to species level but those that were unidentified were attributed
to a species in proportion to the sum of identified cranes counted at that site. The very few
hybrids identified visually (<0.3% of cranes counted) were ignored.
Sites were characterised by slope, distance from the nearest known crane roost and mean
annual rainfall. Slope was identified in three classes (<2%, 2–9%, >9%). Distances from the
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nearest roost to each feeding site were calculated to 0.1 km using a Geographic Information
System (GIS). Mean annual rainfall was determined by interpolation in three classes (<1,000
mm, 1,000–1,200 mm, 1,200–1,600 mm) from the records of the Bureau of Meteorology
(www.bom.gov.au). Field observations of site usage were converted to area measurements in
a GIS, and the density of each crane species calculated for each site survey.
Correlations and MARSpline and regression tree analyses were performed in Statistica 13.2
(Dell Inc. 1984-2016). Complex models were evaluated with the Permanova module in the
Permanova+ add-on to Primer 6 (Anderson et al., 2008). Permanova+ is permutational
software, meaning that probabilities are calculated by permutation rather than based on the
normal distribution. This is particularly appropriate where there are frequent zeroes in the
dataset, as was the case in this study. Spatial analyses were undertaken with ArcGIS v10.4.1
(ESRI, 2016).
To evaluate whether crane species used the Atherton Tablelands differently over time,
Permanova was used to model crane numbers using crane species and traverse number as
fixed effects, site as a random effect included to reflect the repeated measures structure of the
dataset, and the species by traverse interaction. A significant interaction term would provide
evidence of different frequencies across time. A total of 29 complete traverses for 43 sites
were used in this analysis. The Euclidean distance measure was employed to untransformed
count totals, a Type III Sum of Squares model, and 9999 permutations. Additionally, counts
were summed for each traverse and examined the temporal correlation between Sarus Crane
and Brolga numbers (log (n+1)-transformed).
To determine whether crane species use different sites on the Atherton Tablelands, the rank
correlation between species was first examined (separately using each of abundance and
density) for the 46 sites averaged across all site surveys. To measure spatial association of
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sites Moran’s I statistic was calculated, based on the percentage of Brolgas at each site and
the Getis-Ord Gi* statistic used to identify clusters of sites with values higher (hotspot) or
lower (coldspot) in magnitude than expected by chance (Getis and Ord, 1992).
To consider the possibility that choice of feeding sites might be constrained by distance to
roosts, the distance between them was evaluated as a function of species. Distances to the
nearest roost were categorised into four classes with approximately equal number of foraging
sites (0-1.5 km, n=10; 1.5-4.0 km, n=10; 4.0-8.0 km, n=13; 8.0-18 km, n=13). Site usage was
quantified as the fourth-root of species-specific mean crane density. Effects of distance class
were then evaluated by species interaction in Permanova with site as a random effect, using
the Euclidean distance measure, a Type III Sum of Squares model, and 9999 permutations.
As the interaction term was statistically significant, post-hoc pairwise comparisons of
distances classes were conducted for each species separately.
To examine foraging habitat preferences of the species based on fixed attributes of feeding
sites (i.e. not including crop type, which changed over time at many sites), a regression tree
analysis was run for each species mean site density after first culling variables using
MARSplines (non-parametric multiple regression models) on mean site density, to avoid
serious overfitting. For the regression trees, only groups containing at least 10 sites were
split, and the final trees pruned to remove incoherent or uninterpretable lower branches.
To identify crop type preferences, each crane species was considered in a separate model,
using the 31 feeding sites at which cropping was a frequent occurrence. The 32 crop
classes/states were aggregated into ten with similar characteristics. The response variable was
the density of the crane species during each site survey, with aggregated crop type as the key
predictor and site and traverse as random effects to control for non-independence of
individual surveys in space and time. The analysis was performed in Permanova using the
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Euclidean distance measure, a Type III Sum of Squares model, and 9999 permutations. Given
significant effects of crop type, preferences were then evaluated by post-hoc pair-wise
comparisons.
To evaluate seasonal patterns of crop type availability, the 10 crop classes were further
aggregated into four based on similar characteristics: ploughed land, growing grains,
harvested grains and others. Observed frequencies were compared to expected frequencies
across months (May to December), the latter based on constant proportionality calculated
across all site surveys and evaluated using Chi-squared analysis.
5.4 Results
In total, 28,548 crane observations were used in analyses, a mean of 649 per traverse, 15.1
per site survey and 50.4 per site at the 569 (30.1%) site surveys at which one or more cranes
were present. These were 62.1% Brolgas, 37.7% Sarus Cranes and <0.3% hybrids. When
cranes were present, site surveys yielded from one to 880 cranes and densities from 0.008 to
23.7 ha-1
(mean 1.6 ha-1
). Both species were present in 241 site surveys, Brolgas alone in 159
site surveys, Sarus Cranes alone in 166 site surveys and hybrids alone (one individual on each
occasion) in three surveys. Cranes were present from 2.4% to 90.3% of the times that a
particular site was surveyed (mean 30.6%). Twelve roosts were dominated by Brolgas and
30 by Sarus Cranes.
5.4.1 Temporal patterns
Though the number of cranes varied significantly between species (P = 0.002) and site (P <
0.001), the difference between traverses was not significant (P = 0.09) and there was no
significant interaction between species and traverse (P > 0.99). Furthermore, the abundance
of Sarus Cranes and Brolgas was strongly correlated across traverses (r = 0.84, n = 29, P
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<0.001). There is therefore no evidence of differential temporal patterns of use at a whole-of-
Tablelands scale for the months studied (May to December).
5.4.2 Spatial patterns
Among sites averaged across traverses, both the rank abundance and rank density of Brolgas
were positively but weakly correlated with those of Sarus Cranes (both tests, Spearman’s R =
0.39, n = 46, P = 0.007). There was significant clustering of sites based on the % of cranes
that were Brolgas (Moran's I = 0.84, Z = 9.1, P<<0.001), as well as significant hotspots for
each species (see Fig. 2 below). Brolga hotspots were located in the south (near Tumoulin
and Innot Hot Springs) and Sarus Crane hotspots were located in the central Tablelands (near
Atherton and Tinaroo Dam), with no significant clustering in the north (near Chewko and the
Mareeba Wetlands).
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Fig. 5.2 Foraging site hotspot analysis based on the percent of cranes that were Brolgas or Sarus.
Non-significant sites had an admixture of the two. Roost locations are also presented, classified
according to most prominent species observed at each.
Mean density of cranes did not differ between either distance to nearest roost class nor
species (P = 0.53 and 0.58 respectively) but the distance class by species interaction was
significant (P = 0.038). Post-hoc pair-wise analysis revealed no significant difference
between distance classes for Sarus Cranes (P all > 0.27) but for Brolgas there was one with a
significant difference (P = 0.01) and three with differences of P < 0.06. Brolgas were at much
higher density at feeding sites close to roosts than far from them (see Fig. 5.3 below). The
non-significant apparent reverse trend for Sarus Cranes is largely a product of a single high-
density feeding site 14.9 km from the nearest known roost (see Figs. 5.4 a and b below).
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Fig. 5.3 Species-specific crane densities at feeding sites as a function of distance to the nearest roost.
Fig. 5.4 Mean density of Brolgas (a) and Sarus Cranes (b) at each survey site. Roost locations are also
presented, classified according to most prominent species observed at each.
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5.4.3 Habitat use
For Sarus Cranes, MARSpline analysis (model R2 = 0.39) identified a positive association of
crane density with volcanic soils, negative association with elevation, and a preference for
moderate slopes. The positive association with higher fertility volcanic soils and strongly
diminishing density with increased elevation was also evident in the regression tree analysis
(Fig. 5.5A), but an effect of slope was not supported. For Brolgas, MARSpline analysis
(model R2 = 0.27) identified that Brolgas were negatively associated with distance from roost
(i.e. fed at sites closer to roosts) and were negatively associated with disturbance. Regression
tree analysis illustrates the effect of distance from roost on Brolga density (see Fig. 5.5B
below) but did not provide support for a directional effect of disturbance.
Fig. 5.5 Regression tree habitat models for Sarus Crane and Brolga. Values in boxes are the number
of sites and mean density of the crane species in the group, while values outside boxes are habitat
parameters. Higher densities are shown to the left.
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Brolgas were more often present at grazing and wetland sites than cropping sites but at higher
numbers and densities at cropping and grazing sites (see Table 5.2 below). Sarus Cranes were
more often present at wetlands, but most abundant and at highest densities at cropping sites.
Table 5.2 Population and density of crane species by land use type. Data are for site surveys. Sample
sizes: cropping – 1,300 site surveys across 31 sites; grazing – 423 site surveys across 11 sites; wetland
169 site surveys across 4 sites, with ‘% presence’ being the percentage of site surveys at which the
species was recorded.
Median (quartiles) when present
Species Land use % presence Population Density (ha-1
)
Brolga cropping 16.5 15 (4–51) 0.5 (0.1–1.6)
grazing 31.7 14 (4–27) 0.6 (0.1–1.4)
wetland 30.2 4 (3–9) 0.3 (0.1–0.3)
Sarus Crane cropping 20.8 19 (7–49) 0.7 (0.2–2.0)
grazing 20.3 4 (3–13) 0.1 (0.1–0.4)
wetland 30.2 3 (2–4) 0.1 (0.05–0.2)
The density of both crane species varied significantly among crop types after controlling for
the confounding effects of Site and Traverse. The effect of crop type was stronger for Sarus
Cranes than Brolgas (see Table 5.3).
Table 5.3 Probabilities from modelling of crop preferences of two crane species.
Pair-wise tests suggested three broad classes of crop preference for each species (see Table
5.4), with both species at highest densities where grain had been harvested and on ploughed
land with Brolgas also at high densities where grain was growing. This result was because the
Brolgas favoured a newly-sown site where they could feed on self-sown peanuts from the
previous crop.
Explanator Sarus Crane model Brolga model
Crop type <0.0001 0.003
Site (random effect) <0.0001 <0.0001
Traverse (random effect) <0.0001 0.017
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Table 5.4 Density of crane species in crop types on the Atherton Tablelands, Queensland, during
surveys from May to December from 2014-2016.
Mean crane density (birds/ha)
Crop (field) type Sarus Cranes Brolgas
Grains – harvested 0.95 0.66
Ploughed land 0.53 0.26
Maize – sown 0.33 0.09
Peanuts 0.25 0.03
Grains – growing 0.20 0.77
Potatoes 0.07 <0.01
Grazing and hay 0.05 0.01
Miscellaneous 0.02 0.00
Sugarcane 0.02 0.02
Maize – ripe <0.01 0.03
5.4.4 Crop seasonality
All four aggregated crop types (ploughed fields, growing grains, harvested grains, other)
were available in all months (May to December). Although relative crop frequency varied
significantly across months (Chi-square = 83.9, d.f. = 21, P << 0.001), there was no clear
seasonal trend in availability.
5.5 Discussion
Mixed flocks of crane species occur on all continents during the non-breeding season
(Johnsgard, 1983); although co-occurrence may mask minor differences in ecology between
species (Watanabe, 2006). On the Atherton Tablelands the differences in habitat use between
co-occurring Brolga and Sarus Crane were similarly subtle. There was no temporal separation
between species, both occurred at their highest densities and numbers where grain had been
harvested and on ploughed land and both species were found most frequently at wetland sites
to which they retreated when no cropping land suitable for crane foraging was available.
However, Brolgas (not Sarus Cranes) were most common close to their roost sites and were
found most commonly on grazing areas, while Sarus Cranes favoured the intrinsically more
fertile volcanic soils of the central Tablelands. The reasons the Sarus Cranes favoured this
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habitat and most Brolgas did not cannot be determined from a correlative analysis but the
differences are most readily explained by some form of low level competition between the
two species. In a captive feeding situation, Brownsmith (1978) found that Sarus Cranes
dominated Brolgas. While in the wild the reverse may be true in at least some circumstances
(T. Nevard, unpublished data), the largest Australian Sarus Cranes are larger than the largest
Brolgas (Marchant and Higgins, 1993), so there could be active exclusion if resources are
limiting, especially as Sarus Cranes, being larger, may then have higher nutritional
requirements. This could also explain not only the selection of the better soils by Sarus
Cranes but also differences in roost site proximity. While, for neither species, is the distance
travelled from the roost site unusual compared to other cranes (e.g. Eurasian Crane Grus
grus; Alonso et al., 2004), Brolgas may nevertheless be able to obtain their dietary
requirements more readily within a short distance of roost sites than Sarus Cranes, which
could be willing to travel further to feed. More speculatively, nutritional limitations may also
help explain the restricted distribution of Sarus Cranes in Australia where most soils have
intrinsic low fertility (Flannery, 1994) and more fertile soils until recently tend to have been
heavily vegetated. Grasslands on seasonally flooded alluvial soils near the Gulf of
Carpentaria, to which Sarus Cranes had been confined until the advent of arable cropping,
would have been an exception to this.
There are two main consequences for the choice of favoured agricultural habitat by
Australian Sarus Cranes: (i) the vulnerability of this habitat to agronomic trends; and (ii) the
novelty of the habitat.
Interviews with Atherton Tablelands farmers on whose land cranes have been recorded
(Nevard et al., 2018) indicate that there is a strong intention to shift towards tree crops that
give a return on investment an order of magnitude greater than the field crops favoured by the
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cranes. As has happened in India (Borad and Mukherjee, 2002) and Nepal (Aryal et al.,
2009), such shifts in crop preference can cause rapid declines in crane populations. Even for
those farmers intending to continue with field crops, some gains in yield are likely to arise
from reducing losses during harvesting, leaving little leftover grain available for cranes. This
would be consistent with findings in north America, where maize yield in the central Great
Plains increased by 20% from 1978 to 1998 by reducing post-harvest leftover grain to only
1.8% of production; a 47% reduction in the amount available for cranes (Krapu et al., 2004).
Similarly, in Western Europe, the amount of grain left behind dropped from 5–10% of maize
and 3–5% of wheat, barley and oats in the 1970s and 1980s to only 0–1% of maize and 1–2%
of other cereals today (Nowald, 2012). Further reductions in grain availability for cranes have
arisen as a result of adopting pre-emergent herbicides and new varieties and shortening
cropping intervals (Krapu et al., 2004; Prange, 2012).
The consequence of habitat loss is that cranes are likely to concentrate their foraging on the
small areas of suitable habitat remaining and potentially shift from foraging from waste food
to newly-sown seed. In North America and Europe this has resulted in conflict with farmers
(Nowald and Mewes, 2010). The results of farmer interviews carried out on the Atherton
Tablelands by Nevard et al., (2018) indicate that cranes can already cause economically
significant crop damage, especially where they forage in large numbers close to their roosts.
This has sometimes resulted in unlawful killing of cranes (Australian Broadcasting
Corporation, 2013).
The second conclusion to be drawn from the preference of Sarus Cranes for the better soils is
that this preferred habitat is almost entirely relatively new. The tropical savanna woodland
preferred by Brolgas, and most of the swamps beside which they roost, were present at the
time of European arrival in the area in the 1880s (albeit partially modified since by cattle
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grazing) and probably for thousands of years, given the environmental history of the area
under Indigenous occupation (Mooney et al., 2017). The fertile volcanic soils, however, were
almost entirely covered with rainforest until the first half of the 20th
Century. Such habitat
would have been unsuitable for cranes. As it is, Sarus Cranes were only observed on the
Atherton Tablelands for the first time in 1967, at which time numbers overall were thought to
be far lower than today (G. Archibald pers. obs.). This implies that the migration to the
Tablelands has been occurring for just a few generations, given that cranes commonly live for
several decades (Johnsgard, 1983).
In ungulates, migratory pathways established through social processes take 8-9 generations to
become fully established among naïve animals, even when they are joining an established
migration pathway (Jesmer et al., 2018). The rapidity with which Australian Sarus Cranes
have been able to locate and exploit the newly formed habitat on the Atherton Tablelands
suggests that, spatially, they are highly adaptable and opportunistic. This would be consistent
with our own observations of Brolgas and Sarus Cranes foraging in grain crops grown on
newly-developed arable areas in Cape York Peninsula (250 km north if the Atherton
Tablelands) and near Georgetown (300 km west) in May 2018; as well as near Emerald in
2014-5, some 900 km south (W. Cooper, pers. comm.).
5.6 Conservation Management
In areas with economically significant crop damage on the Atherton Tablelands, Nevard et al.
(2018) found that the majority of farmers interviewed were prepared to adopt appropriate
agronomic practices, such as crane repellents, to avoid damage. While encouraging, the
consequence of this could be similar to a progressive change in agronomic practice, i.e.
concentration of cranes on fewer and fewer farms, where the damage they would cause would
become increasingly severe. However, as detailed in Nevard et al. (2018), this may provide
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positive opportunities for ecotourism on the Atherton Tablelands, where an Annual Crane
Week celebrates the presence of large numbers of the birds. To succeed, this as yet immature
initiative needs coordination with agronomic practices in surrounding farmland, particularly
the spread of benefits so that farmers incurring economic damage from cranes receive
adequate compensation.
To achieve this would require detailed evaluation of the crane-related financial losses of a
representative sample of farming businesses, ideally in partnership with farming
organisations and local conservation organisations. This could then provide the basis for the
development of a package of measures for discussion with all levels of government and
potential sponsors. Nevard et al. (2018) identified that due to its proximity to the Cairns
tourism market, about AU$125,000 of annual gross regional product could potentially be
generated from crane watching on the Atherton Tablelands. However, the temporal window
for this opportunity could be curtailed if cranes adapt to habitat constrictions on the Atherton
Tablelands by moving to more remote newly-developing agricultural lands.
5.7 Conclusions and Recommendations
Arable cereal crops (especially maize) and peanuts are important to dry season crane flocks
on the Atherton Tablelands. While we have not established whether the area suitable for
crane foraging is currently limiting their abundance, constrictions are likely if changes to
arable cropping on the Atherton Tablelands reflect global agronomic trends towards
increased efficiency in harvesting and agronomy of field crops or their replacement with
higher value perennial crops.
However, the relative novelty of crane migration to the Tablelands, particularly for Sarus
Cranes, suggests that they may seek out and exploit other agricultural lands if, as appears to
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be happening, these are created elsewhere in north Queensland. If not, there are opportunities
for adaptation by combining the adoption of crane repellent techniques with the provision of
food or sacrifice crops in association with an expansion in crane-related tourism.
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CHAPTER 6 - FARMER ATTITUDES
Farming and Cranes on the Atherton Tablelands, Australia
[Accepted for publication in Pacific Conservation Biology 01/07/2018]
6.1 Abstract
Brolgas Antigone rubicunda and Australian Sarus Cranes A. antigone gillae, form dry season
flocks on the Atherton Tablelands in north Queensland, Australia; where they forage almost
exclusively amongst planted crops or intensively managed grassland. The long-term
relationship between cranes and farmers is therefore critical to their conservation, especially
as cranes can sometimes cause significant economic damage to crops. Farmers were
interviewed to explore their current attitudes to cranes and their intentions for land use that
might affect the birds. Most farmers were found to tolerate cranes, particularly when they fed
amongst stubble. Most, however, are increasing the efficiency of their agronomic practices,
harvesting combinable crops such as maize and peanuts in ways that are beginning to reduce
post-harvest crop residues. There is also a rapid trend away from field crops to perennial and
tree crops that have a higher return per unit area. Both trends may reduce foraging
opportunities for the cranes and, unless managed effectively, are likely to increase the
potential for damage and conflict with farmers in the field crops that remain.
6.2 Introduction
When the importance of agricultural lands for biodiversity is discussed, it is usually the
complexity of the matrix that is emphasised (Fahrig et al., 2011). Relatively few bird species
become synanthropic and benefit from agricultural land. In Australia, where agriculture has
been a dominant part of the landscape for little over 100 years (Garnett and Crowley, 2008),
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there are particularly few synanthropic native species. Among birds, for example, 60 native
species are recorded as localised pests of fruit crops (Tracey et al., 2007) and just eight
species in grain crops (Bomford and Sinclair, 2002); all with extensive ranges outside the
crops in which they cause problems.
Internationally, agricultural specialists are highly susceptible to changes in agronomic
practice. This has been most apparent in Eurasia, where a broad suite of farmland birds has
been disadvantaged by both intensification of cultivation systems and shifts from cultivation
to pasture (Robinson et al., 2001). In both Eurasia and North America, however, a small
number of large granivorous and herbivorous species have flourished in cultivated landscapes
on which they are increasingly dependent (Amano et al., 2008; Le Roy, 2010; Sugden et al.,
1988). Such is their abundance that they cause significant economic losses (Heinrich and
Craven, 1992; Lane et al., 1998; Lorenzen and Madsen, 1986).
Agricultural opportunists include members of the crane family (Gruidae), with nearly all of
the 15 species relying on agricultural lands during at least part of the year (Harris, 2010). The
extent to which the two crane species that occur in Australia, the Sarus Crane Antigone
antigone and the Brolga A. rubicunda (see Figure. 6.1 and Figure 6.2), rely on agriculture is
not fully understood but both species do use agricultural lands extensively during the non-
breeding season on the Atherton Tablelands in north Queensland, consuming grain, insects
and even small vertebrates (Meine and Archibald, 1996).
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Fig 6.1 Brolgas feeding on volunteer peanuts in an irrigated winter wheat crop at Innot Hot Springs,
Atherton Tablelands, Queensland. [Photograph: T. Nevard]
Fig. 6.2 Pairs of Brolgas and Australian Sarus Cranes with cattle at Kaban, Atherton Tablelands,
Queensland. [Photograph: T. Nevard]
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The Brolga population in northern Australia is generally considered stable and has been
estimated to comprise of 20,000-100,000 individuals (Meine and Archibald, 1996). Of 51,969
Brolgas recorded during a national census of waterbirds, all but 135 were in northern
Australia (Kingsford et al., 2012). The only longitudinal counts of Brolgas in tropical
Australia have been from north-east Queensland (Atherton Tablelands and Townsville
regions); with an annual average of approximately 800 individuals recorded by community-
based naturalists over 21 years between 1997 and 2017 (E. Scambler pers. comm. and Nevard
et al., 2019a and 2019b).
The 800-1,500 Sarus Cranes (sources as above) counted annually on the Atherton Tablelands
are globally important for a species classified as Vulnerable in the IUCN Red List (BirdLife
International, 2018c) and are the reason the Atherton Tablelands are registered as a Key
Biodiversity Area (BirdLife International, 2018b). A substantial proportion of the total
population of the endemic Australian subspecies A.a.gilliae migrates annually to the
Tablelands from their breeding grounds 400 km north-west near the Gulf of Carpentaria
(Nevard et al., 2019b). As with cranes in Eurasia, Africa and North America
(Andryuschenko, 2011; Prange, 2012 and Nowald and Mewes, 2010), foraging among crops
has caused damage on the Atherton Tablelands. There has also been one case where a
farming company was found guilty of poisoning (Australian Broadcasting Corporation,
2013).
Conflict between cranes and agriculture outside Australia has been managed in four ways that
do not entail lethal control: (i) compensation to farmers, an approach adopted in Europe and
North America with some success although the cost is rising (Nilsson et al., 2016). Surveys
suggest that there is guarded support for such programs among farmers in north Queensland
(Greiner, 2015); (ii) a crane repellent which makes cranes nauseous is available in the United
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States, but has not yet been tested in Australia; (iii) cranes can be diverted from farms by
providing grain elsewhere in the landscape near their major roost sites such as Lake
Hornborgasjön in Sweden and Lac du Der in France (Lundgren, 2013; Salvi, 2015); (iv)
cranes can become an economic asset as a focus for tourism, such as at Tsurui in Japan and
Lac du Der in France. The Wildlife Conservancy of Tropical Queensland and the Tablelands
Regional Council have established Atherton Tablelands Crane Week (www.craneweek.org)
to raise the profile of cranes in north Queensland and explore potential farm-based crane-
viewing opportunities for both domestic and international visitors. However, none of these
solutions can be implemented without first understanding farm practice, farmer attitudes and
their intentions (Manfredo, 1989). Such research has not been conducted in Australia. The
aim of this research was therefore to provide an insight into the views of Atherton
Tablelands’ farmers and the interaction of cranes with their livelihoods as a prelude to
identification of crane management options for the Atherton Tablelands.
6.3 Study Area
The study was conducted in agricultural lands on the Atherton Tablelands, an area of
approximately 6,000 km2 of which about 500 km
2 is under intensive agricultural production.
The region is highly diverse with three main landscape elements: (i) rainforests, which are
mainly part of the Wet Tropics World Heritage Area; (ii) areas of dry sclerophyll savanna
woodland; and (iii) some of Australia’s most fertile and productive farmland. Cranes are
absent from rainforest but occur in the latter two land types, mainly during the dry season
flocking months of May to December (see Fig. 6.3).
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Fig. 6.3 Atherton Tablelands region showing location, major settlements, land use and Key
Biodiversity Area (data from Queensland Globe and Department of Environment & Energy, 2012).
Typical agricultural soils in the northern and southernmost areas are derived from granite and
metamorphics and have a slightly acid pH and low fertility, compared to the well-drained
soils in the central Tablelands derived from basalt. The latter areas contain some of the most
expensive arable land in Queensland, with land and associated water allocations in 2018
being sold for up to AUD80,000/ha (J. Suffield, Elders Real Estate, pers.comm.)
Water for the Mareeba-Dimbulah Irrigation Area is supplied from a large water impoundment
on the Barron River, Tinaroo Dam, through an extensive network of channels and streams.
Farming enterprises in other parts of the Tablelands (including intensive agricultural areas
around Atherton, Malanda and Ravenshoe) draw water from volcanic groundwater aquifers,
natural watercourses and small dams.
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6.4 Methods
Information on the relationship between cranes and agriculture on the Atherton Tablelands
was obtained from two main sources.
1. Data on agricultural systems in the study area were obtained from Queensland
Department of Agriculture and Fisheries (Department of Agriculture and Fisheries,
2015). Based on this cropping data and farmers’ experience, we have rated the
intensity of use by cranes as low, moderate or high.
2. Attitudes and socioeconomic conditions under which farmers and graziers operate on
the Atherton Tablelands were explored using informal landholder interviews
(approved by the Charles Darwin Univerity Human Ethics Committee), similar to the
methodology previously used successfully by Garnett et al. (2016) to test landholder
support for Night Parrot Pezoporus occidentalis conservation.
All forty-five of the 260 farmers and graziers listed in the Yellow Pages from the Atherton
Tablelands (Sensis, 2015) on whose land identified as being used by cranes were contacted
for interview. Each of those 31 who agreed to be interviewed (14 declined or did not respond)
described their farming experience, the composition of their enterprises, their views on nature
conservation, knowledge of and attitudes towards cranes, damage by cranes and other
wildlife, potential solutions for reducing crop damage and attitudes towards crane tourism
and crop damage mitigation trials. They also expressed their intentions for their enterprises in
the future.
Interviews based on questions approved by the Charles Darwin University Human Ethics
Committee took place between February 2015 and March 2016. Before commencing, each
interviewee was first assured of the anonymity of their responses and location of their land.
Each interview was conducted in person and transcribed during the interview, with transcripts
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read back at the end of each interview and opportunity given for additional comments or
correction.
Two forms of analysis were conducted based on the landholder survey: (i) descriptive
statistics based on ranking to summarise knowledge and attitudes; and (ii) textual sampling of
comments made by individual interviewees to convey the tone of the interviews and provide
context.
6.5 Results
6.5.1 Primary Production on the Atherton Tablelands
The Queensland Department of Agriculture and Fisheries (2015) identified 40 agricultural
land uses in the Atherton Tablelands region (see Tables 6.1 and 6.2).
Table 6.1 Agricultural production on the Atherton Tablelands, Queensland, in 2015 sorted by area for
each major type of agricultural activity and the intensity of use by Brolga and Sarus Cranes [Source:
Department of Agriculture and Fisheries (2015) and this research].
Agricultural activity Area (ha)
Gross revenue
per hectare/yr
(AUD '000)
Crane use
intensity
Livestock 558,872 0.2
Beef cattle 550,000 0.1 Low
Dairy cattle 8,800 3.9 Moderate
Pigs and poultry 72 550.4 Low
Field Crops and Horticulture 23,427 4.6
Sugar cane 10,956 3.6 Moderate
Maize 4,719 2.4 High
Hay 3,020 1.2 Moderate
Grass seed 1,195 4.0 Moderate
Potato 972 16.2 Moderate
Legume seed 968 3.1 Moderate
Peanut 874 5.5 High
Minor field crops 723 35.2 Low
Tree crops and forestry 11,297 27.8
Forestry plantations 3,600 5.6 Low
Minor tree crops 2,497 34.5 Low
Mango 2,400 21.1 Low
Banana 1,850 49.2 Low
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Agricultural activity Area (ha)
Gross revenue
per hectare/yr
(AUD '000)
Crane use
intensity
Avocado 950 87.3 Low
Miscellaneous 151 577.2 Low
Total 593,747 910.4
Table 6.2 Returns from land on the Atherton Tablelands, Queensland, with different intensities of dry
season crane usage [Source: Department of Agriculture and Fisheries (2015)]
Potential for crane usage Area (ha)
Gross revenue per
hectare (AUD '000)
High (maize and peanuts) 5,593 2.9
Moderate 25,911 3.9
Low (intensive use) 12,243 31.8
Low (beef cattle) 550,000 0.1
Beef cattle production was the dominant agricultural land use over the wider region,
accounting for 93% of the total agricultural area; largely on low fertility savanna woodlands.
The main agricultural use in areas of high fertility soils was cropping (e.g. sugar cane, maize
and hay), which accounted for more than half of the intensely farmed areas; followed by
dairy cattle and tree crops (e.g. forest plantations, minor tree crops, mango and banana).
Returns per hectare on tree crops, were an order of magnitude higher than for field crops or
dairy cattle.
6.5.2 Farmer intentions and attitudes
Of the 45 landholders within the areas of the Atherton Tablelands visited by cranes in the dry
season, 31 participated in interviews. This sample represents approximately 12% of all
farmers in the region.
The properties that interviewees managed were widely distributed across the Atherton
Tablelands and ranged from c. 30 to c. 13,500 ha. They were located on irrigated and non-
irrigated land and engaged in farming livestock (dairy and beef), cropping (sugar cane, maize,
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sorghum, peanut, potato, soya, canola, Rhodes grass, wheat, barley, oats, pumpkin) and/or
tree crops (avocado, banana, lychee, coffee). Many were mixed enterprises.
Interviewees had a median of 38 years of experience in primary industry (20-69 years) with a
median of 25 years on their property (9-55 years). Thirteen interviewees indicated that they
thought their children would be likely to take on the property and 18 owned or managed more
than one property. Nineteen were partnerships or sole traders with 12 having a company
structure. The median percentage of income derived from farming was 80%, with the average
contribution of primary industry to total income being 68%.
All interviewees were questioned about their cropping and livestock husbandry practices.
Eighteen were involved in annual cropping, 13 had livestock, nine had tree crops and ten
grew sugar cane. When asked to speculate on the future of farming on the Atherton
Tablelands, all interviewees felt that more tree and perennial crops would be planted and nine
indicated that more efficient crop management, harvesting and sowing was already being
adopted. Two quotes from the interviews underline this: “High value crops such as
avocadoes, bananas and sugar are increasing, and we’re almost the only large-scale maize
and peanut growers left in our area” and “As cropping is becoming specialised and needs new
efficient equipment to be profitable, there’s a general move towards avocadoes, sugar and
bananas on the better crop land and we’re planting avocadoes”.
To provide a context for opinions, all interviewees were asked to rank the following six
socioeconomic issues in order of importance to themselves: economic growth; nature
conservation; healthcare; education; employment; and immigration. The majority of
respondents ranked economic growth as the most important. Education was second, with
health care and employment joint third, and immigration and nature conservation least
important (see Table 6.3).
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Table 6.3 Landholder ranks of social issues (ranked from 1 (highest) – 6 (lowest); n=30)
Policy issue Average rank No. ranking highest No. ranking last
Economic growth 2.1 18 0
Education 1.9 11 0
Conservation 4.7 0 8
Healthcare 2.8 2 6
Employment 3.2 0 5
Immigration 5.0 1 15
Most interviewees (23) felt that landholders should generally look after wildlife but a quarter
did not. A typical response was: “Society in general has a responsibility for wildlife, not just
farmers and government. Consumers should be paying an ‘environmental premium’ for food,
as we have to get the marketplace to pay”. Some financial responsibility for managing
wildlife was conceded by 21 interviewees, with ten disagreeing “Landholders should bear
some burden in the sense that profitable businesses pay more tax but it is essentially a
taxpayer responsibility”. Only six interviewees thought that government was looking after
threatened species well in or off National Parks. One interviewee said: “They’re making a
mess of it and sitting in offices rather than spending time in the bush”.
Interviewees were roughly equally split on whether the local Council should play a bigger
role in helping to conserve wildlife on private land (15 for and 16 against). Typical responses
from both sides were: “Council could (play a bigger role) but it doesn’t have the resources,
especially when our roads are falling apart” and “it’s not their job”.
Nearly all (27) interviewees could distinguish between Brolga and Sarus Crane species, with
11 demonstrating knowledge of their breeding and foraging habits. The median length of time
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that interviewees judged that they’d had cranes on their property was 25 years (10-50 years),
for example one respondent indicated that they’d had cranes “since the Mareeba Wetlands
was created around 20 years ago”.
Twenty-eight interviewees said that cranes first arrived each year in May and June (12 and 16
respondents respectively) and 26 said that the cranes left in November and December (6 and
20 respectively). A smaller number of interviewees (5), all of whom had predominantly
Brolgas on their land, said that the cranes left in January and February.
Twenty-four respondents indicated that cranes foraged on their land and six that they both
foraged and roosted. Only one indicated that fewer cranes foraged on their land due to
cropping changes: “They feed on our farm but don’t roost. As our agronomy and harvesting
gear has got more efficient, we get less Brolgas and Sarus Cranes than we used to a few years
ago”. When asked if their stock interacted with Brolgas and Sarus Cranes, 13 indicated that
this happened, for example “The cranes seem to like the company of stock and will spend a
lot of time walking among them”.
When interviewees were asked to describe how Brolgas and Sarus Cranes used their land, 11
indicated that a mix of maize, peanuts and recently cultivated land had the highest number of
crane visits, followed by a mix of maize and peanuts (eight respondents); a mix of livestock
and grass, sugar cane, and cultivations were each nominated by three respondents. Just over
half (16 respondents) reported no damage from cranes with 14 reporting damage to peanuts
and 11 to maize. When asked about the critical time for damage, 20 nominated after sowing,
two pre-harvest and nine had no damage so offered no opinion.
When asked to nominate other animals causing damage, 19 interviewees grouped Magpie
Geese, Whistling Ducks and Cockatoos together as causing damage, six indicated only
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Magpie Geese, three (all graziers) named dingoes and two feral pigs. Twelve respondents
took no measures to prevent damage, eight concentrated on human intervention such as riding
a motorbike in the paddock, five combined mechanical measures such as bird scarers with
human intervention, for example “scaring-off by driving a ute and beeping the horn and gas
guns” and four graziers poisoned dingoes and feral dogs. Agronomic measures, such as
repellent seed coatings, and human intervention were considered potentially effective in
reducing bird damage by seven and six interviewees respectively, one comment being:
“We’ve heard that they use a repellent for seed corn and potatoes to stop cranes and geese in
the US”. Eleven interviewees thought that no measures are effective in reducing damage.
Nineteen indicated that they would be interested in participating in trialling measures to
reduce crop damage by Brolgas and Sarus Cranes, a typical comment being: “yes but we
don’t have much time”.
Interviewees were asked about their knowledge of or involvement in crane conservation or
research activities, to ascertain regional interest in cranes amongst both farmers and graziers.
Twenty-four said that they had heard of the annual Atherton Tablelands crane count and 23
said that they had heard of Crane Week, a local celebration of crane abundance. Six
interviewees felt that crane-based tourism could potentially provide a source of income for
their property, including one individual with a degree in hospitality and tourism. Twenty said
they would not welcome birdwatchers on their property: “we’d rather not have them”.
6.6 Discussion and Recommendations
Established global trends to reduce harvesting losses through machinery and agronomic
efficiency improvements and minimise fallow periods tend to reduce crane foraging
opportunities (Prange, 2012). During the dry season, cranes on the Atherton Tablelands were
observed to feed primarily on unharvested grain and nuts in the stubble of maize and peanut
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crops, and to a lesser extent on insects extracted from among hay crops, potatoes, legumes,
seed crops and, post-harvest in sugar cane, grass crop and dairy fields. As agronomic and
harvesting efficiencies are taken-up, these opportunities are likely to become far fewer.
Alongside agronomic and harvesting efficiencies, in many areas where production costs are
high, perennial and tree crops are replacing combinable crops eaten by cranes (grains,
oilseeds and peanuts), which have significantly lower returns per hectare than those with low
crane suitability (see Table 6.2). This is illustrated on the Atherton Tablelands by the banana
industry, which had the highest gross income for any crop in 2015 (AUD90.9 million)
followed by avocadoes (AUD82.9 million). The area under both crops has therefore
expanded substantially in recent years (Department of Agriculture and Fisheries, 2015), as
have other high return crops such as citrus (AUD31.3 million) and pawpaw (AUD15.1
million).
The pattern of cropping is also potentially likely to shift as, in cooperation with the
Queensland State Government, the Tablelands Regional Council is investigating the
establishment of further irrigated cropping areas (10-15,000 ha) in the southern Atherton
Tablelands; south and west of Ravenshoe (Dr Hurriyet Babacan, CEO of Tablelands
Regional Council, pers. comm.). Although it is anticipated that annual crops will continue to
be grown in this area, rises in the price of water could have the potential to tip the balance in
favour of higher value tree crops.
Given this background, the results highlight three concerning factors for the future of cranes
on the Atherton Tablelands:
(i) Gross returns per hectare from crops that cranes use frequently (e.g. maize and
peanuts) are an order of magnitude lower than crops such bananas and avocadoes,
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with low intensity cranes use. As anticipated by the farmers interviewed, with
rising labour, land, machinery, input and irrigation costs there will be substantial
economic pressure to convert many areas of combinable crops to higher value
agricultural activities that tend to be unsuitable for crane foraging.
(ii) There are growing economic imperatives to increase harvest and agronomic
efficiency in combinable crops. Many farmers commented that cranes favoured
post-harvest and cultivated fields because maize and peanuts are lost in the
harvesting process and remain available to the cranes. More efficient farming
techniques and changing cropping patterns will reduce the availability of this post-
harvest grain residue (Krapu et al., 2004; Austin, 2012; Prange, 2015; Nilsson et
al., 2016). Indeed one farmer from the Atherton Tablelands commented that his
increased efficiency had meant cranes no longer visited his property. Increased
harvest efficiency has been linked to a reduction in food availability and
population declines/range shifts for cranes in many countries (Andryuschenko,
2011; Prange, 2012; and Nowald and Mewes, 2010).
(iii) Although the scale of poisoning remains unknown on the Atherton Tablelands,
van Velden et al. (2016) found that farmers who had experienced large flocks on
their farms and farmers who ranked cranes as more problematic than other bird
pests were more likely to perceive cranes to be damaging their livelihoods.
Biographical variables and crop profiles were not correlated with perceptions of
damage, indicating the complexity of this human-wildlife conflict. However,
farmers’ need for management alternatives was related to the perceived severity of
damage. For ethical reasons, poisoning was not discussed during interviews
because it is illegal and could have either implicated the interviewee or made the
interviewer complicit in the illegal activity. Nevertheless, many farmers
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mentioned that their crops had been damaged by cranes immediately after sowing
and that they felt crop losses to be severe. They were also well-informed about the
recent prosecution for poisoning cranes.
The interview process found that farmers on the Atherton Tablelands are well aware of
cranes, with every interviewee having some knowledge of the timing of arrival and departure
on their properties. Importantly, some interviewees valued the cranes in their own right
beyond economic and financial considerations. For example, one believed that “as
landholders, farmers should recognise their responsibility for the wildlife on their farms and
contribute”. However there was also a general undercurrent of caution amongst farmers (less
obvious amongst graziers, who do not suffer damage) in relation to talking to outsiders about
cranes on their land. Given the potentially adverse trajectory of cropping change for cranes
on the Atherton Tablelands, there is a need for well-considered management options
developed cooperatively with farmers. However, farmer intentions revealed through
interviews suggest that changes in crop selection and agronomic practice do not auger well
for the populations of Brolga and Sarus Cranes on the Atherton Tablelands Key Biodiversity
Area, notwithstanding the differences between stated intentions and actual action (Fishbein
and Ajzen, 2011).
6.6.1 Crane management options
All of the following four options for managing conflict between cranes and agriculture could
be relevant to the Atherton Tablelands:
(i) Compensation to farmers. While compensation paid for damage caused by cranes
would be unlikely to overcome the discrepancy in returns between tree and
combinable crops, it could reduce the market incentive to switch out of maize and
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peanuts. However, because neither Brolga nor Sarus Cranes are listed as
threatened under Commonwealth or State legislation, compensation may not be
available from government, as funding tends to be given only to listed taxa.
Compensation funds would therefore have to be drawn from private philanthropic
funds.
(ii) Crane repellents. The State and Commonwealth Governments could facilitate
research to test commercially available crane repellents in Australia, especially as
they are already licensed for use in the United States, South Africa and parts of
Europe. The repellents protect newly emerging grain (Barzen and Ballinger, 2017)
which farmers noted was the most susceptible to damage by foraging cranes.
Attempts by private individuals to import the repellent for trial over the last ten
years have been thwarted by Commonwealth agrochemical regulations that
require expensive Australian trials prior to approval for release (G. Harrington
pers. comm.).
(iii) Diversion to alternate foraging areas. Active feeding of cranes at particular sites
could divert cranes and reduce damage on valuable agricultural land, and sites
could be selected to coincide with tourism opportunities. Such schemes exist in
Europe with annual contributions of up to 100,000€ towards the cost of
supplementary food and site management being provided by regional government
authorities (Le Roy, 2004; Nowald, 2012; Nilsson et al., 2016). The Tablelands
wintering population of cranes (Brolga and Sarus) is currently about 3,000
individuals. Blackwell et al. (2002) found that in captive situations, a pair of
Sandhill Cranes Antigone canadensis consumed 231.4g of maize a day. The
average weight of male and female Sandhill Cranes is 3,550 g, Brolgas 6,359 and
Australian Sarus Cranes 7,800 g (Johnsgard, 1983). This equates to an
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approximate Australian crane/Sandhill Crane weight ratio of approximately 2:1
(7,078g/3,550g). As food consumption is unlikely to be directly related to weight
and Blackwell’s findings are not from a wild situation (where other food sources
are available), for the purposes of calculating an order of magnitude of maize that
could be required to replace crane crop raiding on the Atherton Tablelands, a wild
Australian crane/captive Sandhill Crane maize consumption ratio of 1:1 has been
adopted. Assuming that the approximately 3,000 wintering cranes (1,500 ‘pair
equivalents’) remain on the Atherton Tablelands for an average of 180 days (June-
November) they would consume about 62,000 kg of maize a year. At current
prices this would cost AUD 22,000 p.a.
(iv) Ecotourism. Birding is a growing sector in the Australian tourism market (Steven
et al. 2015) and, in the absence of government-sponsored agri-environmental
measures, nature-based tourism has been identified as a potential ecosystem
service for which transfer payments can be made to assist with conservation
(Balmford et al. 2009). Whilst most interviewees were not interested in having
birdwatchers on their land, there was some interest in using cranes to generate
income from tourism among interviewees, especially by those landholders close
enough to Cairns to benefit from day visitors. The Atherton Tablelands Crane
Week aims particularly to take advantage of the large numbers of Japanese and
Chinese tourists who visit north Queensland. In both countries cranes are
venerated and have a number of crane-led visitor destinations (e.g. Tsurui in
northeast Hokkaido, Japan) with numerous farm-based/council-funded crane-
viewing opportunities (Y. Momose, pers. comm. and Matthiessen, 2014). Other
important north Queensland tourism markets, such as the United States, France
and Germany, also have well-developed crane-based tourism (Nowald, 2012),
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potentially creating the opportunity for a global network of crane viewing
opportunities. In the Hula Valley of northern Israel, large wetland areas have been
drained for agricultural expansion and the land used for grain crops. Migratory
Eurasian Cranes Grus grus started wintering, with numbers building to 100,000
and crop damage becoming substantial. Feeding stations were established to draw
cranes away from growing crops, to which visitors were transported in portable
viewing stations. Funds generated by current visitor numbers of up to 400,000 a
year contribute to crane food and on-site management. (Shanni et al., 2012 and
Yossi Leshem, pers. comm.). On the Atherton Tablelands returns to the local
economy from, for example, an extra 5,000 tourists p.a. could exceed the cost of
paying to feed visiting cranes by an order of magnitude (e.g. a local restaurant
meal of AUD25 per head could equate to AUD125,000 of additional gross
regional product).
6.6.2 Consequences of failing to conserve cranes on the Atherton Tablelands
For Sarus Cranes at least, there is some evidence that numbers have greatly increased since
the 1960s, possibly because of the abundance of food in the dry season provided by
agriculture (Archibald, 1987). Given that the population of Sarus Cranes using the Atherton
Tablelands is thought to be only 1,500 at the most (Elinor Scambler, pers. comm.), the loss of
this population would mean that the only birds remaining would be those that do not migrate
to the Atherton Tablelands from their breeding grounds on the Gulf Plains, 500 km to the
west. The size of the non-migratory population is unknown but is likely to be much smaller
than the Tablelands population, meaning that the subspecies of Sarus Crane in Australia
could be likely to meet IUCN Red List Criteria as vulnerable.
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However, were habitat no longer available on the Atherton Tablelands, the situation could
revert to that which occurred before the land was cleared, the tree crops keeping cranes off
fertile regional soils, just as rainforest once did.
Should this transpire, the cranes of the Atherton Tablelands, which could potentially be
globally significant for conservation and form the basis of an incipient tourism industry,
might not endure. This research provides the basis for discussions between primary producers
and government, conservation and tourism interests about potential measures for retaining
cranes by reducing crop damage and expanding opportunities for tourism. Identification of
sources of funding for physical measures and compensatory payments would need to be part
of these discussions.
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CHAPTER 7 – DISCUSSION
7.1 Introduction
Cranes are iconic birds and have close cultural relationships with people, forged over
thousands of years. Eulogised in storytelling (such as the Australian Aboriginal Buralga
myth), dance, poetry and song; depicted in art; celebrated in traditional cultures; used as
contemporary symbols of trust and fidelity; they are prominent flagships for wetland
ecosystems and unsurpassed symbols of natural heritage. However, they are becoming
increasingly dependent upon modified agricultural and pastoral landscapes, requiring a
sustainable balance to be struck between the needs of cranes and those of farming.
A key challenge to achieve this is that landscapes important for cranes are also generally
those most suitable for farming. Global agriculture is intensifying rapidly, with its trajectory
set towards feeding a burgeoning global human population, which, with the accelerants of
increasing personal wealth and dietary change (explored in Chapter 1), may need 50% more
food by 2030, doubling by 2050. As a result, especially where unmoderated by cultural
values or viable economic alternatives, farmers and cranes are coming into conflict.
Balmford et al. (2019) argue that whilst land-sparing approaches to meeting human
agricultural demand remain the least detrimental to biodiversity, practical difficulties in
implementing land sparing could still have significant impacts on biodiversity. Bull et al.
(2017) have also explored this in the context of offsets, raising concerns about potential gaps
between their theoretical and practical effectiveness. As cranes are synanthropic, with most
species having at least some level of dependency on agriculture, practical crane-specific land-
sharing measures are required within the landscapes they share with farmers. Strategies
which explicitly link yield increases could therefore be extremely valuable in helping to
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offset increased crane damage, brought about by agronomic change and increased
efficiencies.
Notwithstanding recent progress in the debate around ‘sustainable intensification’ it is not yet
seen as mature enough at either policy or agronomic levels to more than marginally affect the
focus of commercial agricultural development; which remains firmly production-oriented.
Whilst increasing yields once underpinned significant increases in the populations of some
crane species (Nowald, 2012), harvesting efficiencies are now inexorably increasing pressure
on crane populations (Krapu, et al., 2004) and practical measures to protect cranes within
agricultural landscapes are urgently required.
Against this backdrop, the ICF (Austin et al., 2018) has identified inter alia a range of
research that should be undertaken to support the complex decision-making required to
address the changes at the agriculture/crane interface. This includes: (i) understanding the
crane-related dietary and bioenergetic characteristics of grains and other crops; (ii) formal
delineation and protection of flyways and important stopover areas; (iii) understanding
habitat connectivity and patterns of habitat loss; (iv) identifying spatial and temporal risks
from factors such as drought, fire, crop protection, power lines and avian diseases; and (v)
better understanding the key socioeconomic factors at the agriculture/crane conservation
interface. To create workable models across such a complex matrix of issues requires
adaptive, multidisciplinary approaches; founded on sound research and monitoring, and
generating high quality data to underpin appropriate practical and policy-related conservation
interventions.
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7.2 Key Findings
The global backdrop against which my research findings and their implications have been
discussed is set out in each of Chapters 1, 3, 4, 5, and 6 above. For completeness, the
following summary discusses five key findings of the research and goes on to postulate a set
of potential future scenarios that could affect cranes in tropical Australia.
Key Finding 1: The Australian Sarus Crane is a distinct subspecies; significantly different
from Asian mainland subspecies, underlining the conservation importance of the Australian
population. It also seems likely that the Australian and extinct Philippine subspecies share a
close evolutionary relationship.
For the formulation of robust and durable crane conservation strategies and framing of
appropriate supporting legislation, it is first essential to confirm the taxonomic status of
Australia’s cranes. Miller et al. (in press) have done this for the Brolga; finding that the large
northern population is slightly different genetically from the small and potentially threatened
southern population but not differentiated sufficiently for subspecies status. This research
(see Chapter 3) has explored the genetic differences between the Australian Sarus Crane and
extant Asian subspecies; finding that it differs substantially and potentially clusters
genetically with the extinct Philippine subspecies.
Typically, genetic drift occurs in small populations, where rare alleles are more likely to be
lost. The result of this process is reduced genetic diversity and increased genetic
differentiation (Hedrick, 2011). Compared to the two extant Asian subspecies, the genetic
diversity of Australian Sarus Cranes is significantly lower, as it may have passed through a
genetic bottleneck around 28,000 years ago, soon after its colonisation of Australia (Jones et
al. 2005). The implications of this for any captive breeding program are significant. Should it
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be deemed appropriate to assemble a representative captive group of Australian Sarus Cranes
to ensure that its unique genetic characteristics can be preserved from ongoing introgression
(see Chapter 4 and below), it would be important to ensure that the founders of the group had
the broadest diversity possible. This would help to avoid problems such as those encountered
with existing captive populations of the White-headed Duck Oxyura leucocephala, which
were found genetically unsuitable for reintroduction; requiring the re-building of a more
diverse captive population, based on birds taken from different areas of their range (Munoz-
Fuentes et al., 2008).
As cranes are large charismatic birds, they have been the subject of a number of ‘flagship’
reintroduction projects, such as the ‘Great Crane Project’ in England
(www.thegreatcraneproject.org.uk); creating significant media focus and fostering cross-
community interest in nature conservation. The potentially close relationship between the
Australian Sarus Crane and its Philippine relative suggests that should a flagship Sarus Crane
reintroduction to its former range in Luzon be promulgated (J. C. Gonzalez, pers. comm.),
Australian birds could (subject to further genetic investigation) provide the founding stock.
Key Finding 2: Introgression between Australian Sarus Cranes and Brolgas has been
confirmed. Although introgression is still relatively low, it is occurring at a significantly
higher rate than previously realised. Migration of both species between the Atherton
Tablelands and Gulf Plains has been confirmed, using genetic evidence from shed feathers.
As discussed in relation to Key Finding 1 above, the Australian Sarus Crane is significantly
different from the two other extant Sarus Crane subspecies. Although the current rate of
Brolga/Australian Sarus Crane introgression (2.58%) does not yet appear to be putting the
genetic integrity of either Brolgas or Australian Sarus Cranes at risk, as discussed in Chapter
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4, Lamichhaney et al. (2016) have demonstrated that introgression at only a single locus may
have important evolutionary consequences. Whether the larger body size of hybrids identified
by Archibald (1981) confers a selective advantage over the parental species cannot yet be
determined but ongoing Brolga/Sarus Crane introgression may differentially favour alleles
which promote adaptation to environmental changes brought about by such stresses as
climate change or agricultural intensification. This suggests that there is sufficient
uncertainty about introgression stimulated by anthropogenic influences to lend weight to the
potential value of establishing a viable captive ‘insurance group’ of Australian Sarus Cranes;
as well as (possibly) a group representative of the northern Brolga population.
The use of shed feathers in this research has confirmed that movement/migration occurs
between the Atherton Tablelands and Gulf Plains and suggests an opportunity for ‘citizen
science’. Subject to the appropriate permitting and training, shed feathers from various
locations in crane breeding and flocking habitat could be collected by members of birding
NGOs and Indigenous rangers, using simple easy-to-follow instructions and minimal
equipment (forceps, plastic gloves and bags, and pre-paid postal bags). The preparation and
genetic analyses of these feathers could, if funded sufficiently, provide extremely valuable
data for strategic decisions on crane conservation.
Key Finding 3: Brolgas and Sarus Cranes are synanthropic on the Atherton Tablelands,
having taken full advantage of combinable crops such as maize and artificial roost sites such
as irrigation storages. This may explain the rapid rise in Australian Sarus Crane numbers
since its formal discovery in the 1960s; as well as the propensity for mixing between Brolgas
and Sarus Cranes, and their consequent introgression.
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The sometimes intimate dependence of cranes on agriculture has been described in Chapters
1, 4, 5 and 6 of this thesis. The growth in the area and farmed intensity of combinable crops
(e.g. maize and peanuts) on the Atherton Tablelands appears to have coincided with an
increase in both Brolga and Australian Sarus Crane numbers; with records of crop usage by
Brolgas going back to at least the 1930s. This mirrors the growth in crane numbers in
response to agricultural expansion and intensification in other countries (see Chapter 1).
In relation to the propensity for introgression, a finding of this research is that at sites with
higher Brolga or Australian Sarus Crane counts, the species with lesser numbers in a mixed
flock tended to have proportionally more first year juveniles (see Chapter 4). This puzzling
differential distribution of juveniles of one species amongst flocks of the other, which could
be related to differing species-specific flocking propensity amongst individuals, potentially
increases opportunities for inter-species interactions. As juvenile experience can override
imprinting (Gallagher, 1976), this could significantly affect the number of hybridisation
opportunities created when juveniles are at the critical age for pair-bonding.
Key Finding 4: Brolgas and Sarus Cranes are differentially distributed across the Atherton
Tablelands, with Sarus Cranes favouring intrinsically more fertile volcanic soils and Brolgas
concentrated on poorer metamorphic and granitic soils, closer to roosts. Both favour
cultivated land and post-harvest combinable crops such as maize and peanuts.
The apparent differential distribution of Brolgas and Australian Sarus Cranes on the Atherton
Tablelands, with the latter concentrated on areas of intrinsically higher fertility, may be a
consequence of competition. Although similar in size, the largest Australian Sarus Cranes are
larger than the largest Brolgas (Marchant and Higgins, 1993), so if resources are limiting
there could be active exclusion, especially as Sarus Cranes, being larger, may have higher
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nutritional requirements. This could also explain not only the selection of the better soils by
Sarus Cranes but also differences in roost site proximity. While, for neither species, is the
distance travelled from the roost site unusual compared to other cranes (Alonso et al., 2004),
Brolgas may be able to obtain their apparently broader dietary requirements (Sundar et al.,
2018) more readily within a shorter distance of roost sites than Sarus Cranes, which could be
willing to travel further to feed. More speculatively, nutritional limitations may also help
explain the restricted distribution of Sarus Cranes in Australia, where most soils have
intrinsically low fertility (Flannery, 1994), the Atherton Tablelands being a rare exception to
this.
An issue arising from the choice of more fertile agricultural land by Australian Sarus Cranes
is their potential greater vulnerability to agronomic trends. Interviews with Atherton
Tablelands farmers have confirmed a strong intention to shift towards higher value tree crops
(which do not provide foraging opportunities for cranes) on more fertile, higher-yielding
land, likely bringing a decrease in foraging opportunities earlier to Australian Sarus Cranes
than to Brolgas.
Key Finding 5: Global changes in agronomy, harvesting technology and cropping are
combining to reduce food availability for cranes on agricultural land. There is no reason to
expect Australia will be different and interviews with farmers on the Atherton Tablelands
have confirmed this.
Interviews with farmers on the Atherton Tablelands have confirmed that globally increasing
efficiencies in agronomy and harvesting of combinable crops (both resulting in less post-
harvest waste) are being rapidly adopted. Not only will this affect the availability of both
crane species to forage on the Atherton Tablelands, it is also relevant in relation to the
142
development of new agricultural areas in Cape York Peninsula, as well as the Gulf Plans and
other locations where these new technologies may be deployed as part of cropping
development. Whether this will lead to overall decreases in crane numbers as less dry season
food resource is available or increased raiding of establishing crops (or both), is not yet clear
in Australia but experience from elsewhere (see Chapter 1) suggests that both are plausible
outcomes, for which farmers and conservation managers should already be actively planning.
7.3 Future Scenarios
It is a time of rapid land use change in Australia’s tropical north. To explore what this might
mean for Brolgas and Australian Sarus Cranes, a set of future scenarios and associated
potential land management practices are postulated below. These have been formulated
based on the most frequent issues aired by farmers, conservationists, policy-makers and the
wider community during this research.
Scenario 1: Waste grain reduces from combinable crops, due to improvements in agronomy
and harvesting efficiency – cranes begin to focus on newly-planted crops; negative farmer
attitudes intensify; cranes are persecuted; numbers decline. This could be tested by: (i)
monitoring of crane distribution and numbers on the Atherton Tablelands through late dry
season counts; and (ii) farmer attitude surveys.
Scenario 2: As a result of commercial and policy shifts in irrigation water use towards
higher value agriculture dominated by tree and other high value perennial crops on the
Atherton Tablelands – cranes concentrate on remaining properties; damage is caused to
newly-planted combinable crops, as large numbers of hungry cranes look for food; cranes are
persecuted and their numbers decline. This could be tested by: (i) monitoring of crane
143
distribution and numbers on the Atherton Tablelands through late dry season counts; and (ii)
farmer attitude surveys.
Scenario 3: Combinable crops expand into new areas such as CYP and the Gulf Plains -
cranes move to newly-cultivated areas; crane populations increase but with less waste grain
the potential for crop damage and persecution increases. This could be tested by: (i)
monitoring of crane distribution and numbers in late dry season counts; and (ii) shed feather
sampling at new sites and the Atherton Tablelands (confirming trajectories of crane
movements).
Scenario 4: Crane-based tourism – cranes are deliberately fed; farmers are compensated by
tourism operators/local government; crane numbers rise: potentially more hybridisation
occurs due to closer sympatry of juveniles. This could be tested by: (i) monitoring of
distribution and numbers in late dry season counts; and (ii) genetic sampling of shed feathers.
Scenario 5: Changes in cattle grazing regimes alter breeding area suitability – technological
and husbandry changes alter the way in which cattle use crane breeding habitat in the Gulf
Plains and CYP. This could be tested by monitoring of crane distribution and numbers in late
breeding season counts.
Scenario 6: De-stocking of significant areas of crane breeding habitat occurs following
purchase of cattle properties by nature conservation NGOs (this is already happening
extensively in northern CYP) and the widespread uptake of plant-based meat products - cattle
are removed at a large scale; leading to changes in land management practices and the
structure of vegetation; with as yet unknown outcomes for cranes. This could be tested by:
monitoring of crane distribution and numbers in late breeding season counts.
144
Scenario 7: Significant increase in mining adjacent to key breeding season habitat – leading
to greater disturbance adjacent to significant areas of crane breeding habitat in CYP and
elsewhere. This could be tested by: monitoring of crane distribution and numbers in late
breeding season counts.
Scenario 8: The Philippine government decides to reintroduce Sarus Cranes as a flagship
agri-conservation project and seeks suitable founding stock and expertise. This could be
tested/investigated by: (i) further genetic analyses of Philippine Sarus Crane museum
specimens; (ii) surveys of suitability of sites for potential reintroduction to Luzon; and (iii)
surveys of local Luzon communities to test their preparedness to accept a reintroduction
project.
Although these scenarios are speculative, 1, 2, 3 and 4 are potentially critical in the short
term, with Scenario 4 potentially offering a solution for 1, 2 and 3; retaining cranes within the
Atherton Tablelands KBA and providing financial benefits to facilitate ongoing crane
management. For scenario 4 to have the best chance of working, early, comprehensive and
durable engagement between the Cairns-based regional tourism industry, landholders, local
and State government is essential, assisted by community-based initiates such as the Atherton
Tablelands Crane Week (www.craneweek.org) and Birdlife Australia’s annual Crane Count.
Scenarios 5 and 6 are generated by different but related objectives, bringing about significant
ecological change within crane habitat. Some observers (the author and G. Archibald pers.
obs.) believe that there may be synergistic relationships between cattle grazing and crane
foraging, roosting and breeding habitat, making this important to investigate. The
development of Scenario 8 would require a formal approach from a Philippine agency and
facilitation by an organisation such as the ICF.
145
The debate around crane conservation in agricultural landscapes is becoming more intense.
The ICF have seen this and responded by bringing available knowledge together in its
landmark report ‘Cranes and Agriculture: A Global Guide for Sharing the Landscape’ (Austin
et al., 2018). This does a comprehensive job of bringing together research from almost all
crane states. However, due to the dearth of Australian research here it necessarily only makes
relatively small mention of our continent. A key role for this thesis is therefore to stimulate
research that can fill the gaps in relation to the interface between agriculture, Brolgas and
Australian Sarus Cranes.
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CHAPTER 8 - CONCLUSIONS AND RECOMMENDATIONS
8.1 Conclusions
Based on a multidisciplinary perspective to crane conservation recommended by the ICF, this
thesis has reached four conclusions in areas of key importance to crane conservation:
1. Confirmation of the Australian Sarus Crane as a distinct subspecies. The
Australian Sarus Crane has unique genetic traits and is distinct from the two clinal
Asian Sarus Crane subspecies; underpinning its retention as a separate conservation
management unit. Although based on only one individual and subject to further
investigation, a closer genetic relationship is likely to exist between Australian and
Philippine Sarus Cranes; re-confirming the distinct status of the extinct Philippine
subspecies.
2. Confirmation of introgression between Brolgas and Australian Sarus Cranes:
This research has confirmed introgression between Brolgas and Australian Sarus
Cranes, and although currently of relatively low incidence (2.58%), research in other
taxa suggests that this may be evolutionarily significant. Migration between flocking
areas on the Atherton Tablelands and breeding areas in the Gulf Plains has also been
confirmed.
3. Definition of the relationship between agriculture and cranes on the Atherton
Tablelands: This research has established the differential distribution of cranes on the
Atherton Tablelands and that both harvested maize and cultivated land are critical to
crane usage of the Atherton Tablelands. It has also established that Australian Sarus
Cranes make differential use of intrinsically more fertile land than Brolgas, probably
as a result of competitive exclusion; and that the proximity of roosts to foraging areas
is of greater significance for Brolgas, possibly related to a broader dietary base.
147
4. Determination of the attitudes of farmers towards cranes: Interviews with farmers
have confirmed visual observations that maize, cultivated land and other combinable
crops are of significant importance to cranes. The interviews also confirmed that
farmers intend to radically reduce waste grain at harvest through improved efficiency,
as well as move to higher value perennial crops which provide no foraging
opportunities for cranes. Both changes could potentially lead to higher levels of
damage to remaining areas of early stage combinable crops on the Atherton
Tablelands, similarly in newly-developed cropping areas. Farmer interest in crane-
related tourism has also been confirmed.
8.2 Recommendations
Cranes are charismatic, long-lived and readily observable. They are used to epitomise prized
societal values in cultures ranging from the Australian Aboriginal ‘Buralga’ to Indian Hindu
‘Ramayana’ myths, both of which continue to help protect cranes in contemporary
landscapes. Cranes also provide globally-recognised commercial emblems, such as those
displayed on the tailplanes of Japanese and German airlines, on Chinese credit cards and
Australian wines. This combination of charisma, cultural significance and commercial
recognition makes them ideal ambassadors for conservation in agricultural and pastoral
landscapes.
The cranes and landscape of the Atherton Tablelands could provide a fulcrum around which
to reconnect farmers and communities with nature. Cranes readily lend themselves to
outreach programmes designed to foster greater awareness, understanding, and appreciation
of the landscapes that farmers share with nature, as has been done in England with the Great
Crane Project. Crane-based tourism and community-based events could further reinforce
148
these relationships, providing opportunities to demonstrate the value of nature to the broader
community.
Based on the research findings and issues explored in this thesis, to ensure that cranes can to
continue to prosper in Australia’s rapidly-changing agricultural and pastoral landscapes I
make the following recommendations; capable of implementation either as individual
measures or as components of multi-measure integrated programmes:
Recommendation 1: Framing and adoption of policies and regulations by all levels of
government, designed to sustain biodiversity within agricultural and pastoral landscapes;
including formal protection of wetlands and other crane habitat.
Recommendation2: Fostering of longitudinal working relationships between farmers,
conservation practitioners, agricultural experts, government and other key stakeholders to
explore effective mitigation measures for farming/crane conflicts.
Recommendation 3: Development of a farmer-friendly crane management handbook (in an
appropriate range of media), setting-out practical measures to reduce conflicts between cranes
and farmers, and build a long-term relationship; including damage avoidance and protection
measures, habitat creation techniques and supplementary feeding opportunities.
Recommendation 4: Fostering of research which identifies practices that can enhance both
agricultural sustainability and biodiversity, whilst meeting demands for increased agricultural
output and efficiencies. For example, trialling crane-repellent seed coatings.
Recommendation 5: Fostering and development of partnerships between tourism operators,
farmers and local government (with the assistance of State government) to identify
opportunities for crane-based tourism.
149
Recommendation 6: Investigation of the relationship between cattle grazing and cranes,
especially in wet season breeding and dry season foraging habitat, as well as in the vicinity of
roost sites.
Recommendation 7: Investigation of the feasibility of establishing a genetically-balanced
captive group of Australian Sarus Cranes at a well-resourced institution, with appropriate
avian management skills; safeguarding birds free from admixture of Brolga genes (NB – It
may also be appropriate to investigate the establishment of a representative captive group
from the northern population of the Brolga).
I also recommend that further work be undertaken on the genetic relationships between the
Philippine Sarus Crane and other subspecies. Should this confirm that the Philippine and
Australian subspecies are closely-related, and subject to agreement by Philippine agencies, a
flagship reintroduction project similar to the UK’s Great Crane Project may be feasible and
would benefit from the outputs of all of the above seven recommendations above.
8.3 A Final Word
The Brolga is Queensland’s official bird emblem and supports the right hand side of its coat
of arms, a sheaf of grain occupying the bottom left hand quadrant. With agricultural
intensification inevitable, we must ensure cranes are not put in jeopardy of disappearing from
either Queensland’s coat of arms or its rural landscapes by insensitive land use change.
Fig. 8.1 Queensland Coat of Arms (with author endorsements).
150
ACKNOWLEDGEMENT OF ASSISTANCE
Supervisory team
• Professor Stephen Garnett, Research Institute for the Environment and Livelihoods (RIEL),
CDU (Principal Supervisor).
• Dr George Archibald, International Crane Foundation.
• Dr Ian Leiper, RIEL, CDU (from 2017).
• Professor Michael Lawes, formerly at RIEL, CDU (until 2017).
Financial support
• Charles Darwin University (CDU) Postgraduate Research Scholarship (2013-16).
• North Queensland Wildlife Trust.
• Norman Wettenhall Foundation.
• CDU travel and accommodation support grants.
• CDU supplementary research funding grants.
• BirdLife Australia.
Technical assistance
• Genetic analyses: Dr Martin Haase of the University of Greifswald.
• Statistical design and analyses: Dr Don Franklin of RIEL, CDU and Ecological
Communications.
• Spatial analysis: Dr Ian Leiper of RIEL, CDU.
• Veterinary clearances: Dr Annabelle Olsson of Boongarry Veterinary Clinic.
• Additional genetic samples: Nuchjaree Purchkoon and Dr Boripat Siriaroonrat of Korat
Zoo, Thailand; Robert van Zalinge of RIEL, CDU; Professor Michael Wink of the University
of Heidelberg, Germany; Tin Nwe Latt of Mahidol University, Thailand; Dr Chris Milensky
151
of the Division of Birds at the Smithsonian Institution, Washington; and Emily Imhoff of
Cincinnati Museum.
Editorial support
• Manuscript editing: Supervisory team.
Fieldwork
• Volunteers: Harry Nevard, Bronwen Nevard, Dr Ruairidh Nevard, Baroness Vera von
Schwertzell zu Willingshausen, Baron Dominic von Schwertzell zu Willingshausen, Stella
Freund, Jürgen Freund, Dr John Grant, Trevor Adil and Jess Harris.
• Technical assistance: Dr David Westcott, Adam McKeown and Dr Inka Veltheim.
Laboratory work
• Technical support: Silke Fregin, University of Greifswald.
152
APPENDIX – PERMITS, APPROVALS AND AUTHORITIES
Permit number: WISP13984714 – QP&WS Scientific Purposes Permit.
Permit number: 545 – ABBBS Banding Project Permit.
Permit number: ACLTE47K – ACBPS Export Permit
Approval number: A13019 – CDU Ethics Approval for Animal Based Research.
Approval number: H15003 – CDU Ethics Approval for Human Based Research.
Authority number: 000002/FD-2011 – CITES approval.
Authority number: PWS2014-AU-001240 – CITES approval.
Authority number: PWS2015-AU-000119 – CITES approval.
Authority number: KH1108 – CITES approval.
153
BIBLIOGRAPHY
Akiyama, T., Nishida, C., Momose, K., Onuma, M., Takami, K. and Masuda, R. (2017).
Gene duplication and concerted evolution of mitochondrial DNA in crane species. Mol
Phylogen Evol, 106: 158-163.
Alexandratos, N. Bruinsma, J. (2012). World agriculture towards 2030/2050: the 2012
andrevision. ESA Working Paper No. 12-03. Food and Agriculture Organization, Rome.
Allendorf, F.W., Leary, R.F., Spruell, P. and Wenburg, J.K. (2001) The problems with
hybrids: setting conservation guidelines. Trends in Ecology and Evolution, 16: 613–622.
Alonso, J.C., Bautista, L.M. and Alonso, J.A. (2004). Family‐based territoriality vs flocking
in wintering common cranes Grus grus. Journal of Avian Biology, 35(5): 434-444.
Amano, T., Ushiyama, K. and Higuchi, H. (2008). Methods of predicting risks of wheat
damage by white-fronted geese Journal of Wildlife Management, 72: 1845-1852.
Anderson, M.J., Gorley, R.N. and Clarke, K.R. (2008). PERMANOVA+ for PRIMER: Guide
to Software and Statistical Methods. PRIMER-E: Plymouth, UK. 214 pp.
Andryuschenko, Y. A. (2011). The Demoiselle Crane on Agricultural Lands in the Ukraine.
In: (Eds E. Ilyashenko, S. Winter) Cranes of Eurasia (biology, distribution, migrations,
management). Issue 4. Moscow: Crane Working Group of Eurasia. pp. 476–483.
Anteau, M.J., Sherey, M.H. and Bishop. A.A. (2011). Location and agricultural practices
influence spring use of harvested cornfields by cranes and geese in Nebraska. Journal of
Wildlife Management, 75: 1004–1011.
154
Archibald, G.W. (1975). Introducing the ‘Sarolga’. Unpublished note; International Crane
Foundation, Wisconsin (ICF library ref: 08-028).
Archibald, G.W. (1976). The Unison Call of Cranes as a Useful Taxonomic Tool. PhD
Thesis, Faculty of Cornell University Graduate School. December 1976.
Archibald, G.W. (1976) Crane taxonomy as revealed by the unison call. In Proceedings of the
International Crane Workshop (ed J.C. Lewis), pp. 225-251. Oklahoma State University.
Archibald, G.W. (1981) Introducing the Sarolga. In Crane Research around the World.
Proceedings of the International Crane Symposium at Sapporo, Japan in 1980 and Papers
from the World Working Group on Cranes. (eds J.C. Lewis, H. Masatomi), pp. 213-215.
International Council for Bird Preservation.
Archibald, G.W. and Swengel, S.R. (1987). Comparative ecology and behaviour of eastern
sarus cranes and brolgas in Australia. In ‘Proceedings of the 1985 Crane Workshop.
International Crane Foundation’. (Ed. J. C. Lewis.) pp. 107–116. (Platte River Whooping
Crane Habitat Maintenance Trust, and US Fish and Wildlife Service: Grand Island, NB.)
Archibald, G.W., Sundar, K. S. G. and Barzen, J. (2003). A review of the three subspecies of
Sarus Cranes Grus antigone. Journal of the Ecological Society (India), 16:5-15.
Arnol, J. D., White, D. M. and Hastings, I. (1984). Management of the brolga (Grus
rubicundus) in Victoria. Department of Conservation, Forests and Lands, Fisheries and
Wildlife Service.
Arnold, M.L. (1997) Natural hybridization and evolution. Oxford University Press.
155
Aryal, A., Shrestha, T.K., Sen, D.S., Upreti, B. and Gautam, N. (2009). Conservation regime
and local population ecology of Sarus Crane (Grus antigone antigone) in west-central region
of Nepal. Journal of Wetlands Ecology, 3:1–11.
Attwood, S.W. and Johnston, D.A. (2001). Nucleotide sequence differences reveal genetic
variation in Neotricula aperta (Gastropoda: Pomatiopsidae), the snail host of schistosomiasis
in the Lower Mekong Basin. Biological Journal of the Linnean Society, 73:23-41.
Austin, J.E. (2012). Conflicts between Sandhill Cranes and farmers in the Western United
states: evolving issues and solutions. In: Harris J, (ed.). Proceedings of the Cranes,
Agriculture, and Climate Change Workshop, 28 May-3 June 2010, 132–140 International
Crane Foundation.
Austin, J.E., Morrison, K.L. and Harris, J.T., eds. (2018). Cranes and Agriculture: A Global
Guide for Sharing the Landscape: International Crane Foundation. Baraboo, Wisconsin,
USA.
Australian Broadcasting Corporation (2013). www.abc.net.au/news/2013-08-14/queensland-
protected...brolgas-poison/4887360
Avery, D.T. (1997). Saving the planet with pesticides, biotechnology and European farm
reform, Global Food Issues, Vol 1. Hudson Institute, Indianapolis.
Baker, A.N., Smith, A.N.H. and Pichler, F.B. (2002). Geographical variation in Hector’s
dolphin: recognition of new subspecies of Cephalorhynchus hectori. ,Journal of the Royal
Society of New Zealand, 32:713–727.
156
Balmford, B., Green, R.E., Onial, M, Phalan, B. and Balmford, A. (2019). How imperfect can
land-sparing be before land-sharing is more favourable for wild species? Journal of Applied,
Ecology, 59:73-84.
Balmford, A., Amano, T., Bartlett, H., Chadwick, D., Collins, A., Edwards, D., Field, R.,
Garnsworthy, P., Green, R., Smith, P., Waters, H., Whitmore, A., Broom, D., Chara, J.,
Finch, T., Garnett, E., Gathorne-Hardy, A., Hernandez-Medrano, J., Herrero, M., Hua,
F., Latawiec, A., Misselbrook, T., Phalan, B., Simmons, B., Takahashi, T., Vause, J., zu
Ermgassen, E. and Eisner, R. (2018). The environmental costs and benefits of high-yield
farming. Nature Sustainability, 1: 477–485.
Balmford, A., Beresford, J., Green, J., Naidoo, R., Walpole, M. and Manica, A. (2009). A
global perspective on trends in nature-based tourism. PLoS Biology, 7(6): e1000144.
Ban, N.C., Mills, M., Tam, J., Hicks, C.C., Klain, S., Stoeckl, N., Bottrill, M.C., Levine, J.,
Pressey, R.L., Satterfield, T. and Chan, K.M. (2013). A social-ecological approach to
conservation planning: embedding social considerations. Frontiers in Ecology and the
Environment, 11:194–202.
Barrett, G., Silcocks, A., Barry, S. and Poulter, R. (2003) The new atlas of Australian birds.
Royal Australasian Ornithological Union, Melbourne.
Barton, N.H. and Slatkin, M. (1986) A quasi-equilibrium theory of the distribution of rare
alleles in a subdivided population. Heredity, 56:409-415.
Barzen, J. and Ballinger, K. (2017) Sandhill and Whooping Cranes. Wildlife Damage
Management Technical Series. US Department of Agriculture, Animal and Plant Inspection
Service.
157
Barzen, J., Lacy, A. and Harris, J. (2012). Developing solutions to Sandhill Crane damage to
seedling corn in the upper Midwest, USA. In: Harris J, editor. Proceedings of the Cranes,
Agriculture, and Climate Change Workshop at Muraviovka Park, 28 May–3 June, 2010.
International Crane Foundation, Baraboo, Wisconsin, USA.
Benton, T (2016). The many faces of food security. International Affairs, 6:1505-15
Bignal, E.M. and McCracken, D.I. (2000). The nature conservation value of European
traditional farming systems. Environmental Review, 8:149–171.
Bird, M.I., Taylor, D. and Hunt, C. (2005). Palaeoenvironments of insular Southeast Asia
during the Last Glacial Period: a savanna corridor in Sundaland? Quaternary Science
Reviews, 24(20-21):2228-2242.
BirdLife International (2018a) State of the world’s birds: taking the pulse of the planet.
Cambridge, UK: BirdLife International.
BirdLife International (2018b). Important Bird Areas factsheet: Atherton Tablelands.
Downloaded from: http://www.birdlife.org [accessed 15 February 2018]
BirdLife International. (2018c). Antigone antigone. The IUCN Red List of Threatened
Species 2016: e.T22692064A93335364. http://dx.doi.org/10.2305/IUCN.UK.2016-
3.RLTS.T22692064A93335364.en. [accessed 27 September 2018].
Blackwell. B. F., Helon, D. A. and Dolbeer, R. A. (2002). Repelling sandhill cranes from
corn: whole-kernel experiments with captive birds. Crop Protection, 20:65-68.
Blanford, W. (1895) Grus (antigone) sharpei. Bulletin of the British Ornithologists’ Club, 5:7.
158
Blyth, E. and Tegetmeier, W. G. (1881) The Natural History of the Cranes. Horace Cox,
London.
Bomford, M. and Sinclair, R., (2002). Australian research on bird pests: impact, management
and future directions. Emu, 102(1):29-45.
Borad, C.K. and Mukherjee, A. (2002). Cranes in agricultural ecosystem. China Crane News,
6 (supplement):24–25.
Bouffard, S.H., Cornely, J.E. and Goroshko. O.A. (2005). Crop depredation by cranes at
Daursky State Biosphere Reserve, Siberia. Proceedings of the North American Crane
Workshop, 9:145–150. International Crane Foundation.
Brownsmith, C. B. (1978). Sarus Cranes dominant over Brolgas in captivity. Emu, 78:98.
Bull, J.W., Lloyd, S.P. and Strange, N. (2017). Implementation gap between the theory and
practice of biodiversity offset multipliers. Conservation Letters, 10:656–669.
Burke, J.M. and Arnold M.L. (2001) Genetics and the fitness of hybrids. Annual Review of
Genetics, 35:31-52.
Calinski, R.B. and Harabasz, J. (1974) A dendrite method for cluster analysis.
Communications in Statistics, 3:1-27.
Chatto, R. (2006). The distribution and status of waterbirds around the coast and coastal
wetlands of the Northern Territory. Technical report no. 76, Parks and Wildlife Commission
of the Northern Territory, Northern Territory, Australia.
159
Clarke, R.H., Gordon, I.R. and Clarke, M.F., (2001). Intraspecific phenotypic variability in
the black-eared miner (Manorina melanotis); human-facilitated introgression and the
consequences for an endangered taxon. Biological Conservation, 99(2):145-155.
Clement, M., Snell, Q., Walke, P., Posada, D. and Crandall, K. (2002). TCS: estimating gene
genealogies. Proc. 16th International Parallel Distribution Process Symposium, 2:184.
Collins, P. (1995). The birds of Broome. Broome Bird Observatory, Broome, Western
Australia.
Darriba, D., Taboada, G.L., Doallo, R. and Posada, D. (2012). jModelTest 2: more models,
new heuristics and parallel computing. Nature Methods, 9(8):772.
Dayrat, B. (2005). Towards Integrative Taxonomy. Biol. J. Linnean Soc, 83(3): 407-415
Deane, P.M. (1979). The First Industrial Revolution. Cambridge University Press, New York
Dell Inc. (1984-2016). Statistica 13.2. Dell Inc.: Round Rock, Texas.
del Hoyo, J. and Collar, N. J. (2014). HBW and BirdLife International Illustrated Checklist of
Birds of the World (Volume 1 Non-Passerines). Lynx Edicions, in association with BirdLife
International. Barcelona.
Dessauer, H.C., Gee, G.F. and Rogers, J.S. (1992). Allozyme evidence for crane systematics
and polymorphisms within populations of Sandhill, Sarus, Siberian, and Whooping cranes.
Molecular Phylogenetics and Evolution, 1:279-288.
Department of Agriculture and Fisheries (2015). Tablelands Agricultural Profile. Department
of Agriculture and Fisheries, Mareeba, Queensland.
160
Department of the Environment and Energy (2012) Interim Biogeographic Regionalisation
for Australia, Version 7 and Sub-regions. Commonwealth of Australia, Canberra.
Department of Environment and Energy (2018). EPBC Act List of Threatened Fauna.
http://www.environment.gov.au/cgi-bin/sprat/public/publicthreatenedlist.pl#birds_extinct
[Accessed 9/27/2018].
Department of Transport and Main Roads (2016) State controlled roads – Queensland. State
of Queensland (Department of Transport and Main Roads).
de Quieroz, K. (2007) Species concepts and species delimitation. Systematic Biology 56:879–
886.
Dessauer, H.C., Gee, G.F. and Rogers, J.S. (1992). Allozyme evidence for crane systematics
and polymorphisms within populations of Sandhill, Sarus, Siberian, and Whooping cranes.
Molecular Phylogenetics and Evolution, 1(4): 279-288.
Devitt, T.J., Baird, S.J.E. and Moritz, C. (2011). Asymmetric reproductive isolation between
terminal forms of the salamander ring species Ensatina eschscholtzii revealed by fine-scale
genetic analysis of a hybrid zone. BMC Evolution Biology, 11: 245.
Donnellan, S.C., Armstrong, J., Pickett, M., Milne, T., Baulderstone, J., Hollfelder, T. and
Bertozzi, T. (2009). Systematic and conservation implications of mitochondrial DNA
diversity in emu-wrens, Stipiturus (Aves: Maluridae). Emu, 109(2): 143-152.
Dowling, T.E. and Secor, C.L. (1997) The role of hybridization and introgression in the
diversification of animals. Annual Review of Ecology and Systematics, 28:593-619.
161
Earl D.A. and von Holdt B.M. (2012). STRUCTURE HARVESTER: a website and program
for visualizing STRUCTURE output and implementing the Evanno method. Conservation
Genetics Resources, 4:359-361.
Eisner, R., Waters, H.S., Green, R., Edwards, D., Field, R., Fenuik, C. and Balmford, A.
(2017). Does higher-yielding agriculture mean more environmental harm? Aspects of
Applied Biology, 136:63–70.
ESRI 2016. ArcGIS Desktop: Release 10.4.1. Redlands, CA: Environmental Systems
Research Institute.
Evanno, G., Regnaut, S. and Goudet, J. (2005). Detecting the number of clusters of
individuals using the software STRUCTURE: a simulation study. Molecular Ecology,
14:2611-2620
Fahrig, L., Baudry, J., Brotons, L., Burel, F.G., Crist, T.O., Fuller, R.J., Sirami, C.,
Siriwardena, G.M. and Martin, J.L., (2011). Functional landscape heterogeneity and animal
biodiversity in agricultural landscapes. Ecology Letters, 14 (2):101-112.
Falush, D., Stephens, M. and Pritchard, J.K. (2007). Inference of population structure using
multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes,
7:574-578.
Fishbein, M. and Ajzen, I. (2011). ‘Predicting and changing behaviour: the reasoned action
approach’. (Taylor and Francis: New York.)
Fitzpatrick, B.M. (2012) Estimating ancestry and heterozygosity of hybrids using molecular
markers. BMC Evolutionary Biology, 12:131.
162
Flannery, T.F. (1994). The Future Eaters: An ecological history of the Australasian lands and
people. Reed, Melbourne.
Frankham, R., Ballou, J.D., Dudash, M.R., Eldridge, M.D., Fenster, C.B., Lacy, R.C.,
Mendelson III, J.R., Porton, I.J., Ralls, K. and Ryder, O.A. (2012). Implications of different
species concepts for conserving biodiversity. Biological Conservation, 153:25-31.
Franklin, D.C. (2008). Report 9: The waterbirds of Australian tropical rivers and wetlands.
In: Lukacs, G.P. and Finlayson, C.M. (Eds.) A Compendium of Ecological Information on
Australia’s Northern Tropical Rivers. Sub-project 1 of Australia’s Tropical Rivers - an
Integrated Data Assessment and Analyses (DET18). A report to Land and Water Australia.
National Centre for Tropical Wetland Research, Townsville, Queensland.
Frost, G. (2015). Rare coastal sage scrub habitat provides a home for threatened gnatcatcher
and many other species. http://ca.audubon.org/news/rare-coastal-sage-scrub-habitat-provides-
home-threatened-gnatcatcher-and-many-other-species.
Gallagher, J. (1976). Sexual imprinting: effects of various regimens of social experience on
mate preference in Japanese Quail (Coturnix coturnix japonica). Behaviour, 57:91-115.
Galluzzi, G., Van Duijvendijk, C., Collette, L., Azzu, N. and Hodgkin, T. (2011).
Biodiversity for food and agriculture. Contributing to food security and sustainability in a
changing world. PAR platform. Food and Agriculture Organisation, Rome.
Garnett, S. T., Woinarski, J. C. Z., Crowley, G. M. and Kutt, A. S. (2010). Biodiversity
conservation in Australian tropical rangelands. In ‘Can rangelands be wildlands?: wildlife
and livestock in semi-arid ecosystems’. (Eds J. du Toit, R. Kock, and J. Deutsch.) 191–234.
Blackwell Publishing, Oxford.
163
Garnett, S.T and Christidis, L, (2007). Implications of changing species definitions for
conservation purposes. Bird Conservation International, 17:187-195.
Garnett, S.T. and Christidis, L. (2017). Taxonomy anarchy hampers conservation. Nature,
546:25-27.
Garnett, S.T. and Crowley, G.M. (2000) The Action Plan for Australian Birds 2000.
Environment Australia, Canberra.
Garnett, S.T. and Crowley, G.M. (2008). The history of threatened birds in Australia and its
offshore islands. Pp. 353-401 in Davis, W.E., Recher, H.F. and Boles, W.E. (eds.)
Contributions to the History of Australasian Ornithology. Nuttall Ornithological Club,
Harvard, Massachusetts.
Garnett, S.T., Franklin, D.C., Ehmke, G., VanDerWal, J.J., Hodgson, L., Pavey, C., Reside,
A.E., Welbergen, J.A., Butchart, S.H.M., Perkins, G.C. and Williams, S.E. (2013) Climate
change adaptation strategies for Australian birds. National Climate Change Adaptation
Research Facility, Gold Coast
Garnett, S.T., Kleinschmidt, M., Jackson, M.V., Zander, K.K. and Murphy, S.A. (2016).
Social landscape of the Night Parrot in western Queensland, Australia. Pacific Conservation
Biology, 22:360-366.
Gavrilets, S. (2003). Models of speciation: what have we learned in 40 years? Evolution,
57:2197-2215.
Gill HB. The first record of the Sarus Crane in Australia. Emu. 1967;69: 49-52.
164
Gippoliti S, Cotterill FP, Zinner D, Groves CP. Impacts of taxonomic inertia for the
conservation of African ungulate diversity: an overview. Biological Reviews. 2018;93(1):
115-130.
Goudet J. FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of
Heredity. 1995;86: 485-486.
Getis, A. and Ord, J.K. (1992). The analysis of spatial association by use of distance
statistics. Geographical Analysis, 24(3):189-206.
Gill, H.B. (1967). The first record of the Sarus Crane in Australia. Emu, 69: 49-52.
Gippoliti, S., Cotterill, F.P., Zinner, D. and Groves, C.P. (2018). Impacts of taxonomic inertia
for the conservation of African ungulate diversity: an overview. Biological Reviews, 93(1):
115-130.
Goudet, J. (1995). FSTAT (version 1.2): a computer program to calculate F-statistics. Journal
of Heredity, 86:485-486.
Grant, J.D.A. (2005). Recruitment rate of Sarus Cranes (Grus antigone) in northern
Queensland. Emu, 105:311-315.
Grant, P.R. and Grant, B.R. (2008). How and Why Species Multiply – The Radiation of
Darwin’s Finches. Princeton University Press, Princeton and Oxford.
Grant, P.R. and Grant, B.R. (2016). Introgressive hybridization and natural selection in
Darwin’s finches. Biological Journal of the Linnean Society, 117:812-822.
165
Gray, A.P. (1958). Bird Hybrids. Commonwealth Agricultural Bureau, Farnham Royal,
Bucks, England.
Greiner, R. (2015). Motivations and attitudes influence farmers' willingness to participate in
biodiversity conservation contracts. Agricultural Systems, 137:154–165.
Guerrero, A.M., McKenna, R., Woinarski, J.C.Z., Pannell, D.J, Wilson, K.A. and Garnett,
S.T. (2017). Threatened species recovery planning in Australia: Learning from two case
studies. National Environmental Science Programme, Threatened Species Recovery Hub.
Haase, M. and Ilyashenko, V. (2012). A Glimpse on Mitochondrial Differentiation among
four Currently Recognized Subspecies of the Common Crane Grus grus. Ardeola, 59(1):131-
135.
Hachisuka, M. (1941). Further contributions to the ornithology of the Philippine Island. Tori,
11:61–89.
Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis
program for Windows 95/ 98/NT. Nucleic Acids Symposium Series, 41:95–98.
Hanspach, J.A., Collier, D.J., French, N., Dorresteijn, I., Schultner, J. and Fischer, J. (2017).
From trade‐offs to synergies in food security and biodiversity conservation. Frontiers in
Ecology and the Environment. doi.org/10.1002/fee.1632.
Harding, C. (2001) Use of remote sensing and geographic information systems to predict
suitable breeding habitat for the Brolga Grus rubicundus in south-west Victoria. Diss. Centre
for Environmental Management, University of Ballarat, Victoria, Australia.
166
Harris, J. and Mirande, C. (2013). A global overview of cranes: status, threats and
conservation priorities. Chinese Birds 4:189–209.
Harris, J. (2010). Introduction: Cranes, Agriculture and Climate Change pp1-14. in “Cranes,
Agriculture, and Climate Change. Proceedings of a workshop organized by the International
Crane Foundation and Muraviovka Park for Sustainable Land Use”. Ed. J.Harris.
International Crane Foundation, Baraboo.
Hasegawa, O., Ishibashi, Y. and Abe, S. (2000). Isolation and characterisation of
microsatellite loci in the red-crowned crane Grus japonensis. Molecular Ecology, 9:1677-
1678.
Heinrich, J.W. and Craven, S.R (1992). The economic-impact of Canada Geese at the
Horicon Marsh, Wisconsin. Wildlife Society Bulletin, 20:364-371.
Hedrick, P.W. (2011). Genetics of Populations. Jones and Bartlett Publishers, Sudbury, MA,
USA.
Herring, M.W. (2005). Threatened species and farming. Brolga: management of breeding
wetlands in northern Victoria. Arthur Rylah Institute for Ecological Research, Heidelberg,
Australia.
Herring, M.W. (2007) Brolga breeding habitat: managing wetlands on your farm. Murray
Catchment Management Authority, Australia.
Horwich, R.H. (1996) Imprinting, attachment, and behavioral development in cranes. In
Cranes: Their biology, husbandry and conservation (eds Ellis, D.H., Gee, G.F. and Mirande,
C.M.), pp. 117-22. Washington, D.C.: Department of the Interior, National Biological
Service/International Crane Foundation.
167
Hou, X., Xu, P., Lin, Z., d'Urban-Jackson, J., Dixon, A., Bold, B., Xu, J., Zhan, X. and Hou,
A. (2018). An integrated tool for microsatellite isolation and validation from the reference
genome and their application in the study of breeding turnover in an endangered avian
population. Integr Zool. 2018 Jan 9. doi: 10.1111/1749-4877.12305
Hughes, M. R. and Blackman, J. G. (1973). Cation content of salt gland secretion and tears in
the Brolga Grus rubicundus (Perry) (Aves: Gruidae). Australian Journal of Zoology, 21:515-
518.
Ilyashenko, E. and King, S. (2018). Crane responses to changes in agriculture. In Austin, J.E.,
Morrison K. and Harris, J.T., eds. Cranes and Agriculture: A Global Guide for Sharing the
Landscape. Baraboo, International Crane Foundation, Wisconsin, USA.
Immelmann, K. (1972). Sexual and other long-term aspects of imprinting in birds and other
species. Advances in the Study of Behaviour, 4:147-174.
Jesmer, B.R., Merkle, J.A., Goheen, J.R., Aikens, E.O., Beck, J.L., Courtemanch, A.B.,
Hurley, M.N., McWhirter, D.E., Miyasaki, H.M., Monteith, K.L. and Kauffman, M.J. (2018).
Is ungulate migration culturally transmitted? Evidence of social learning from translocated
animals. Science, 361:1023-1025.
Johnsgard, P. A. (1983) Cranes of the World. Indiana University Press, Bloomington
Jones, K.L., Barzen, J.A. and Ashley, M.V. (2005) Geographical partitioning of
microsatellite variation in the Sarus Crane. Animal Conservation, 8:1-8.
Joseph, L., Bishop, K.D., Wilson, A.C., Edwards, S.V, Iova B, and Campbell, C.D. (2019).
Review of evolutionary research on birds of the New Guinean savannas and closely
168
associated habitats of riparian rainforests, mangroves and grasslands. Emu. DOI:
10.1080/01584197.2019.1615844
Kaczensky, P., Guillaume, C., Huber, D., Andrén, H. and Linnell, J. (2012). Status,
management and distribution of large carnivores – bear, lynx, wolf and wolverine in Europe.
European Commission
Kalinowski, S.T., Taper, M.L. and Marshall, T.C. (2007). Revising how the computer
program CERVUS accommodates genotyping error increases success in paternity
assignment. Molecular Ecology, 16:1099-1106.
Kamp, J., Urazaliev, R., Balmford, A., Donald, P.F., Green, R.E., Lamb, A.J. and Phalan, B.
(2015). Agricultural development and the conservation of avian biodiversity on the Eurasian
steppes: a comparison of land-sparing and land-sharing approaches. Journal of Applied
Ecology, 52:1578–1587.
Katoh, K., Rozewick, J. and Yamada, K.D. (2017). MAFFT online service: multiple
sequence alignment, interactive sequence choice and visualization. Briefings in
Bioinformatics: https://doi.org/10.1093/bib/bbx108.
Keyghobadi, N. (2007). The genetic implications of habitat fragmentation for animals.
Canadian Journal of Zoology, 85:1049-1064.
Kingsford, R.T., Porter, J.L. and Halse, S.A. (2012). National waterbird assessment.
Waterlines report, National Water Commission, Canberra.
169
Koch, E.L., Neiber, M., Walther, F. and Hausdorf, B. (2017). High gene flow despite
opposite chirality in hybrid zones between enantiomorphic door-snails. Molecular Ecology,
26:3998-4012.
Kopelman, N.M., Mayzel, J., Jakobsson, M., Rosenberg, N.A. and Mayrose, I. (2015).
CLUMPAK: a program for identifying clustering modes and packaging population structure
inferences across K. Molecular Ecology Resources,15:1179-1191.
Krajewski, C., Sipiorski, J.T. and Anderson, F.E. (2010). Complete Mitochondrial Genome
Sequences and the Phylogeny of Cranes (Gruiformes: Gruidae). The Auk, 127:440-452.
Krapu, G.L., Brandt D.A. and Cox, R.R. (2004). Less waste corn, more land in soybeans and
the switch to genetically modified crops: trends with important implications to wildlife
management. Wildlife Society Bulletin, 32:127–136.
Lambeck, K., Yokoyama, Y. and Purcell, T. (2002). Into and out of the Last Glacial
Maximum: sea-level change during Oxygen Isotope Stages 3 and 2. Quaternary Science
Reviews, 21(1-3):343-360.
Lamichhaney, S., Berglund, J., Wang, C., Almén, M.S., Webster, M.T., Grant, R.B., Grant,
P.R. and Andersson, L. (2016) A beak size locus in Darwin’s Finches facilitated character
displacement during a drought. Science, 352:62-84.
Lane, S. J., Azuma, A. and Higuchi H (1998). Wildfowl damage to agriculture in Japan.
Agric. Ecosyst. Environ., 70: 69-77.
Lavery, H.J. and Blackman J.G. (1969). The cranes of Australia. Queensland Agricultural
Journal, 95:156-162.
170
Leigh, J.W. and Bryant, D. (2015). PopART: Full-feature software for haplotype network
construction. Methods in Ecology & Evolution, 6(9):1110–1116.
Le Roy, E. (2010). What has been done in the Champagne-Ardenne to prevent crane damages
on farmlands since 2004. In Nowald, G., Alexander, W., Fanke, J., Weinhardt, E. and
Donner, N. (Eds.), Proceedings of the VIIth European crane conference breeding, resting,
migration and biology, Stralsund, Germany (2010), pp. 53-56
Leito, A. (2014). Current situation of the Eurasian Crane in France and recent evolutions.
Scientific abstracts of VIII European Crane Conference (10–14 November 2014, Gallocanta,
Spain.
Lofdahl, K. (1979). Sympatry and Speciation in Australian Cranes. Unpublished research
proposal; International Crane Foundation, Wisconsin (ICF library Ref 04-053).
Lorenzen, B. and Madsen, J. (1986). Feeding by geese in the Filsø farmland, Denmark, and
the effect of grazing on yield structure of spring barley. Holarctic Ecology, 9:305-311.
Lundgren, S. (2013). Current status of the Common Crane in Sweden. Breeding, resting, and
colour banding. In: Nowald G, Weber A, Fanke J, Weinhardt E, and Donner N, editors.
Proceedings of the 7th European Crane Workshop. 16–18. Kranichschutz Deutschland. Groß
Mohrdorf.
Mahon, N., Crute, I and di Bonito, M. (2018). Towards a broad based and holistic framework
for Sustainable Intensification. Land Use Policy, 77:576-597.
Mallet, J., Ehrlich, P., Gill, F., McCormack, J. and Raven, P. (2018). In Comments on
Petition of Pacific Legal Foundation, et al., for Rule-Making Under the Administrative
Procedure Act (Which Aimed to Promulgate New Regulatory Definitions of “Species” and
171
“Subspecies” Under the Endangered Species Act). http://nrs.harvard.edu/urn-
3:HUL.InstRepos:37568375.
Manfredo, M.J. (1989). Human dimensions of wildlife management. Wildlife Society
Bulletin, 17: 447-449.
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.
Martien, K.K., Leslie, M.S., Taylor, B.L., Morin, P.A., Archer, F.I., Hancock‐Hanser, B.L.,
Rosel, P.E., Vollmer, N.L., Viricel, A. and Cipriano, F. (2017). Analytical approaches to
subspecies delimitation with genetic data. Marine Mammal Science, 33:27-55.
Mattheissen, P. (2002). Birds of Heaven. The Harvill Press, London.
Matthiessen, P. (2014). From the Archives: The Cranes of Hokkaido, by Peter Matthiessen,
Audubon (7 April 2014) 165.
McCann, K.I., Thero, L.J and Morrison, K. (2007). Conservation priorities for the Blue Crane
(Anthropoides paradiseus) in South Africa - the effects of habitat changes on distribution and
numbers. Ostrich: Journal of African Ornithology, 78:205–211.
McCormack, J.E. and Maley, J.M. (2015). Interpreting negative results with taxonomic and
conservation implications: Another look at the distinctness of coastal California
Gnatcatchers. The Auk, 132(2):380-388.
Meares, K., Dawson, D.A., Horsburgh, G.J., Glenn, T.C., Jones, K.L., Braun, M.J., Perrin,
M.R. and Taylor, T.D. (2009). Microsatellite loci characterized in three African crane species
(Gruidae, Aves). Molecular Ecology Research, 9:308-311.
172
Meine, C. D. and Archibald, G. W. (eds). (1996). The Cranes: Status survey and conservation
action plan. IUCN, Gland, Switzerland and Cambridge, UK.
Meirmans P.G. (2012). AMOVA-based clustering of population genetic data. Journal of
Heredity, 103:744-750.
Meirmans, P.G. and Van Tienderen, P.H. (2004). GENOTYPE and GENODIVE: two
programs for the analysis of genetic diversity of asexual organisms, Molecular Ecology
Notes, 4:792-794.
Meirmans, P.G. (2013). AMOVA-based clustering of population genetic data. Journal of
Heredity,103:744-750.
Menkhorst, P., Rogers, D., Clarke, R., Davies, J., Marsack, P. and Franklin, K. (2017). The
Australian Bird Guide. CSIRO Publishing, Clayton South, Australia.
Mewes, W. (2010). Population development, range of distribution and population density of
Common Cranes Grus grus in Germany and its federal states. Vogelwelt, 131:75–92.
Mewes W. (2012). Why are breeding populations of Eurasian Cranes increasing and
spreading in Germany? Abstracts of the International Workshop Management of Common
Cranes at the Hula Valley, Israel: Past, Present and Future (16–18 December 2012).
Miller, A. (2016). The development of microsatellite loci through next generation
sequencing, and a preliminary assessment of population genetic structure for the iconic
Australian crane, Brolga (Antigone rubicunda). Nature Glenelg Trust, Warrnambool,
Victoria.
173
Miller, A., Veltheim. I., Nevard, T.D., Gan, H.M. and Haase, M. (2019). Microsatellite loci
and the complete mitochondrial DNA sequence characterized through next generation
sequencing and de novo genome assembly, and a preliminary assessment of population
genetic structure for the Australian crane, Antigone rubicunda. Avian Biology Research,
doi/10.1177/1758155919832142.
Miller, M.P. and Haig, S.M. (2010). Identifying shared genetic structure patterns among
Pacific Northwest forest taxa: insights from use of visualization tools and computer
simulations. PLoS One, 5, e13683.
Miller, S.A., Dykes, D.D. and Polesky, H.F. (1988). A simple salting out procedure for
extracting DNA from human nucleated cells. Nucleic Acids Research, 16:1215.
Mooney, S. D., Sniderman, J. M., Kershaw, P., Haberle, S. G. and Roe, J. (2017). Quaternary
Vegetation in Australia. In D. A. Keith (Ed.), Australian Vegetation (3rd ed., pp. 63-88).
Cambridge, United Kingdom: Cambridge University Press.
Mudrik, E.A., Kashentseva, T.A., Redchuk, P.S. and Politov, D.V. (2015). Microsatellite
variability data confirm low genetic differentiation of western and eastern subspecies of
common crane Grus grus L. (Gruidae, Aves). Molecular Biology, 49(2):260–266.
Munoz-Fuentes, V., Green, A.J. and Sorenson, M.D. (2008). Comparing the genetics of wild
and captive populations of White-headed Ducks Oxyura leucocephala: consequences for
recovery programmes. Ibis, 150:807-815.
Myers, A. (2001). Factors influencing the nesting success of Brolgas, Grus rubicundus, in
Western Victoria. Honours thesis. School of Ecology and Environment, Deakin University,
Victoria, Australia.
174
Nei, M. (1987). Molecular evolutionary genetics. Columbia University Press, New York.
Nevard, T.D., Haase, M., Archibald, G., M., Leiper, I., Van Zalinge, R., Purchkoon, N.,
Siriaroonrat, B., Latt, T.N., Wink, M. and Garnett, S.T. (in press). Subspecies in the Sarus
Crane Antigone antigone revisited; with particular reference to the Australian population.
[Submitted for publication to PLOS ONE 26.07.2019].
Nevard, T.D., Leiper, I., Archibald, G. and Garnett, S.T. (2018). Farming and cranes on the
Atherton Tablelands, Australia. Pacific Conservation Biology, doi:10.1071/PC18055.
Nevard, T.D., Franklin, D.C., Leiper, I., Archibald, G., Garnett, S.T. (2019a). Agriculture,
Brolgas and Australian Sarus Cranes on the Atherton Tablelands, Australia. Pacific
Conservation Biology, doi:10.1071/PC18081.
Nevard, T.D., Haase, M., Archibald, G., Leiper, I. and Garnett, S.T. (2019b). The Sarolga:
conservation implications of genetic and visual evidence for hybridization between the
Brolga Antigone rubicunda and the Australian Sarus Crane Antigone antigone gillae. Oryx,
doi:10.1017/S003060531800073X.
Newell, P. and Taylor, O. (2018). Contested landscapes: the global political economy of
climate-smart agriculture. Journal of Peasant Studies, 45:108–129.
Nilsson, L., Bunnefeld, N., Persson, J. and Månsson J. (2016). Large grazing birds and
agriculture — predicting field use of common cranes and implications for crop damage
prevention. Agriculture, Ecosystems and Environment, 219:163–170.
Nix, H.A. and Switzer, M.A. (1991). Rainforest Animals. Atlas of Vertebrates Endemic to
Australia’s Tropics. Australian Parks and Wildlife Service. Canberra.
175
Nowald, G. (2010). Cranes and People: Agriculture and Tourism. pp.60-65. in Cranes,
Agriculture, and Climate Change. Proceedings of a workshop organized by the International
Crane Foundation and Muraviovka Park for Sustainable Land Use. Ed. Harris J. International
Crane Foundation, Baraboo.
Nowald, G. (2012). Cranes and people: agriculture and tourism. In: Harris, J., editor.
Proceedings of the Cranes, Agriculture, and Climate Change Workshop at Muraviovka Park.
Russia, 28 May-3 June 2010. 60–64. International Crane Foundation.
Nowald, G. and Mewes, W. (2010). Cranes and people. In: Koga, K., Hu, D. and Momose,
K., editors. Cranes and people: prologue to a new approach for conservation of the Red-
crowned Crane. 13–14, Kushiro, Japan.
Nunn, N. and Qian, N. (2010). The Columbian exchange: A history of disease, food, and
ideas. Journal of Economic Perspectives 24:163–188.
Patten, M.A. and Remsen J.V. Jr (2017). Complementary roles of phenotype and genotype in
subspecies delimitation. Journal of Heredity, 108(4): 462-464.
Patten, M.A. and Unitt, P. (2002). Diagnosability versus mean differences of Sage Sparrow
subspecies. The Auk, 119:26–35.
Payseur, B.A. and Rieseberg, L.H. (2016) A genomic perspective on hybridization and
speciation. Molecular Ecology, 25:2337-2360.
Pearse, A.T., Krapu, G.L., Brandt, D.A. and Kinzel, P.J. (2010). Changes in agriculture and
abundance of snow geese affect carrying capacity of Sandhill cranes in Nebraska. Journal of
Wildlife Management 74:479–488.
176
Pennisi, E. (2016). Shaking up the Tree of Life. Science, 354:817-821.
Petit, R.J., el Mousadik, A. and Pons, O. (1998). Identifying populations for conservation on
the basis of genetic markers. Conservation Biology,12:844-855.
Phalan, B., Bertzky, M., Stuart, H. M., Donald, P.F., Scharlemann, J.P.W., Stattersfield, A.J.
and Balmford A. (2013). Crop expansion and conservation priorities in tropical countries.
PLOS ONE, 8(1).
Phalan, B., Green, R.E., Dicks, L.V., Dotta, G., Feniuk, C., Lamb, A., Strassburg, B.B.N.,
Williams, D.R., zu Ermgassen, E.K.H.J. and Balmford, A. (2016). How can higher-yield
farming help to spare nature? Science, 351:450–451.
Prange, H. (2010). Migration and resting of the Common Crane Grus grus and changes in
four decades. Vogelwelt, 2:155–168.
Prange, H. (2012). Reasons for changes in crane migration patterns along the West-European
Flyway. In: Harris, J, editor. Proceedings of the Cranes, Agriculture and Climate Change
Workshop, 28 May – 3 June 2010, 35–48. International Crane Foundation.
Prange, H. (2015). Distribution and migration of the Eurasian Crane on the West-European
route. In: Ilyashenko, E.I. and Winter, S.V. (eds). Cranes of Eurasia (biology, distribution,
captive breeding). 5:287-312. Moscow: Crane Working Group.
Pritchard, J.K., Stephens, M. and Donnelly, P. (2000). Inference of population structure using
multilocus genotype data. Genetics,155:945–959.
Queensland Government (2016). Land use mapping – 1999 to 2015 – Wet Tropics and
Northern Gulf NRM regions.
177
Ramankutty, N., Foley, J.A. and Olejniczak, N.J. (2002). People on the land: changes in
population and global croplands during the 20th century. Ambio, 31:251−257.
Ramasamy, R.K., Ramasamy, S., Bindroo, B.B. and Naik, V.G. (2014) STRUCTURE PLOT:
a program for drawing elegant STRUCTURE bar plots in user friendly interface.
SpringerPlus, 3:431.
Ray, D.K., Mueller, N.D., West, P.C. and Foley, J.A. (2013). Yield Trends Are Insufficient to
Double Global Crop Production by 2050.PLOS ONE, 19:8(6)
Raymond, M. and Rousset, F. (1995). GENEPOP (version 1.2): population genetics software
for exact tests and ecumenicism. Journal of Heredity, 86:248-249.
Reardon, M. (2007). Brolga Country: Travels in Wild Australia. Allen and Unwin. Crows
Nest, Australia.
Redchuk, P., Fesenko, G.V. and Slyusar, N.V. (2015). Migration Routes of the Eurasian
Crane in Ukraine. In: Ilyashenko EI, Winter SV, editors. Cranes of Eurasia (biology,
distribution, captive breeding) 5. Proceedings of International Scientific Conference “Cranes
of Eurasia: biology, conservation, management,” p 313–334. Trans-Baikalia, Russia, 1‒4
September 2015. Moscow, Russia: Crane Working Group of Eurasia.
Rhymer, J.M. and Simberloff, D. (1996). Extinction by hybridization and introgression.
Annual Review of Ecology and Systematics, 27:83–109.
Rieseberg, L.H., Archer, M.A. and Wayne, R.K. (1999). Transgressive segregation,
adaptation and speciation. Heredity, 83:363-372.
Roberts, A. (2017). Tamed. Ten Species that Changed Our World. Windmill Books, London.
178
Roberts, D.G., Baker, J. and Perrin, C. (2011). Population genetic structure of the endangered
Eastern Bristlebird, Dasyornis brachypterus; implications for conservation. Conservation
Genetics, 12(4)1075-1085.
Robinson, R.A., Wilson, J.D. and Crick, H.Q. (2001). The importance of arable habitat for
farmland birds in grassland landscapes. Journal of Applied Ecology, 38(5):1059-1069.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L/, Darling, A., Höhna, S., Larget, B.,
Liu, L., Suchard, M.A. and Huelsenbeck, J.P. (2012). MrBayes 3.2: efficient Bayesian
phylogenetic inference and model choice across a large model space. Systema Biologica,
61:539-542.
Rousset, F. (2008). Genepop'007: a complete reimplementation of the Genepop software for
Windows and Linux. Molecular Ecology Resources, 8:103-106.
Runge, C.A., Gallo‐Cajiao, E., Carey, M.J., Garnett, S.T., Fuller, R.A. and McCormack, P.C.,
(2017). Coordinating domestic legislation and international agreements to conserve migratory
species: A case study from Australia. Conservation Letters, 10:765-772.
Runge, C.A., Martin, T.G., Possingham, H.P., Willis, S.G. and Fuller, R.A., (2014).
Conserving mobile species. Frontiers in Ecology and the Environment, 12:395-402.
Safner, T., Miller, M.P., McRae, B., Fortin, M.J. and Manel, S. (2011). Comparison of
Bayesian clustering and edge detection methods for inferring boundaries in landscape
genetics. International Journal of Molecular Science, 12:865-889.
179
Salvi, A. (2015). The Eurasian Crane in France: evolutions in the last four decades In:
Ilyashenko, E.I. and Winter, S.V. (eds). Cranes of Eurasia (biology, distribution, captive
breeding). 5:191–205. Moscow: Crane Working Group.
Sankhom, R., Warrit, N., Pimpakan, T. and Wiwegweaw. (2018). A Genetic Diversity of
Captive Eastern Sarus Crane in Thailand. Inferred from Mitochondrial Control Region
Sequence and Microsatellite DNA markers. Tropical Natural History.18(2):84-96.
Sankhom, R., Warrit, N. and Wiwegweaw, A. (2018). Screening and application of
microsatellite markers for genetic diversity analysis of captive eastern sarus crane Grus
antigone sharpie (Blanford 1895) in Thailand. Zoo Biology, 37(5):310-319.
Sandvik, J. (2010). Results of the colour ringing of cranes in Norway. Abstracts of the VIIth
European Crane Conference, Oct. 14-17, Stralsund, Germany.
Schodde, R. (1988). New sub-species of Australian birds. Canberra Bird Notes, 13:1
Schodde, R. and Mason, I. J. (1999). Directory of Australian Birds: Passerines. CSIRO
Publishing, Melbourne.
Scott, H.A. and Scott R.M. (1996). A conservation program for the Blue Crane in the
Overberg, Southern Cape, South Africa. In: Beilfuss, R.D., Tarboton, R.W. and Gichuki,
N.N. (eds). Proceedings of the 1993 African Crane and Wetland Training Workshop, 8-15
August 1993. p395–402. International Crane Foundation.
Sensis, (2015). Cairns District and Atherton Tablelands Yellow Pages 2014/15.
Shanni, I., Labinger, Z. and Alon. D. (2012). A review of the crane-agriculture conflict, Hula
Valley, Israel. In: Harris J, editor. Proceedings of the Cranes, Agriculture, and Climate
180
Change Workshop at Muraviovka Park. Russia, 28 May-3 June 2010. pp101–105.
International Crane Foundation.
Sharpe, R.B. (1894). Catalogue of Birds in the British Museum, vol. 23. British Museum of
Natural History, London.
Sherfy, M.H., Anteau, M.J. and Bishop, A.A. (2011). Agricultural practices and residual corn
during spring crane and waterfowl migration in Nebraska. Journal of Wildlife Management,
75:995–1003.
Slatkin, M. and Barton, N.H. (1989). A comparison of three indirect methods for estimating
average levels of gene flow. Evolution 43:1349-1368.
Soltis, P. and Soltis, D.E. (2009). The role of hybridization in plant speciation. Annual
Review of Plant Biology, 60:561-588.
Southwood, T.R.E. and Henderson, A. (2000). Ecological Methods (3rd
Edition). Blackwell
Science Ltd, Oxford
Steven, R., Morrison, C., Arthur, J.M., and Castley, J.G. (2015). Avitourism and Australian
Important Bird and Biodiversity Areas. PLOS ONE 10:e0144445.
Stone, Z.L., Tasker, E. and Maron, M. (2018). Grassy patch size and structure are important
for northern Eastern Bristlebird persistence in a dynamic ecosystem. Emu, 118:269-280.
Sugden, L. G., Clark, R. G., Woodsworth, E. J and Greenwood H. (1988). Use of cereal fields
by foraging Sandhill Cranes in Saskatchewan. Journal of Appied Ecology, 25:111-124.
181
Sundar, K.S.G., Grant, J.D.A., Veltheim, I., Kittur, S., Brandis. K., McCarthy, M.A. and
Scambler, E.C. (2018). Sympatric cranes in northern Australia: abundance, breeding success,
habitat preference and diet. Emu, doi: 10.1080/01584197.2018.1537673.
Szabo, J.K., Khwaja, N., Garnett, S.T. and Butchart, S.H.M. (2012). Global patterns and
drivers of avian extinctions at the species and subspecies level. PLOS ONE 7:e47080.
Van Velden, J.L., Smith, T. and Ryan, P.G. (2016). Cranes and Crops: Investigating farmer
tolerances toward crop damage by threatened blue cranes (Anthropoides paradiseus) in the
Western Cape, South Africa. Environmental Management, 58(6):972-983.
Templeton, A.R, Shaw, K., Routman, E. and Davis, S.K. (1990). The genetic consequences
of habitat fragmentation. Annals of the Missouri Botanical Garden, 77:13-27.
Timmer, C.P., Falcon, W.P. and Pearson, S.R. (1983). Food policy Analysis. Johns Hopkins
University Press, Baltimore.
Tobias, J. A., Seddon, N., Spottiswoode, N., Pilgrim, J.D., Fishpool, L.D.C. and Collar, N.J.
(2010). Quantitative criteria for species delimitation. Ibis, 152:724–746.
Todesco, M., Pascual, M.A., Owens, G.L., Ostevik, K.L., Moyers, B.T., Hübner, S., Heredia,
S.M., Hahn, M.A., Caseys, C., Bock, D.G. and Rieseberg, L.H. (2016). Hybridization and
extinction. Evolutionary Applications, 9:892-908.
Toews, D.P.L and Brelsford, A. (2012). The biogeography of mitochondrial and nuclear
discordance in animals. Molecular Ecology, 16:3907-3930.
182
Tofft, J. (2013). Current status of the Common Crane (Grus grus) in Denmark. In: Nowald G,
Weber A, Fanke J, Weinhardt E and Donner N, eds. Proceedings of the 7th European Crane
Workshop. pp19–21. Kranichschutz Deutschland.
Townsville Daily Bulletin (1935). Atherton Tableland Notes, page 5, Friday 20 September
1935. National Library of Australia http://nla.gov.au/nla.news-article62410202
Tracey, J, Bomford, M, Hart, Q, Saunders, G. and Sinclair, R (2007). Managing Bird Damage
to Fruit and Other Horticultural Crops.
http://www.dpi.nsw.gov.au/agriculture/horticulture/pestsdiseases-hort/multiple/managing-
bird-damage
Triggs, S.J. and Daugherty, C.H. (1996). Conservation and genetics of New Zealand
parakeets. Bird Conservation International, 6:89-101.
Tscharntke, T., Clough, Y., Wanger, T.C., Jackson, L., Motzke, I., Perfecto, I., Vandermeer,
J. and Whitbread, A. (2012). Global food security, biodiversity conservation and the future of
agricultural intensification. Biological Conservation, 151:53-9.
US Fish & Wildlife Service. Service Determines Coastal California Gnatcatcher is a
Subspecies and Remains Threatened under Endangered Species Act.
https://www.fws.gov/news/ShowNews.cfm?ref=service-determines-coastal-california-
gnatcatcher-is-a-subspecies-and-&_ID=35782. 2016 [Cited 14 May 2019].
Van der Geer, A., Lyras, G., de Vos, J. and Dermitzakis, M (2010). Evolution of Island
Mammals, Adaption and Extinction of Placental Mammals on Islands. Wiley-Blackwell,
Oxford.
183
Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. and Shipley, P. (2004). MICRO-
CHECKER: software for identifying and correcting genotyping errors in microsatellite data.
Molecular Ecology Notes, 4:535-538.
Von Treuenfels, C-A. (2006). The Magic of Cranes. Abrams, New York.
Voris, H.K. (2000). Maps of Pleistocene sea levels in Southeast Asia: Shorelines, river
systems and time durations. Journal of Biogeography, 27:1153-1167.
Vijay, N., Bossu, C.M., Poelstra, J.W., Weissensteiner, M.H., Suh, A., Kryukov, A.P. and
Wolf, J.B.W. (2016). Evolution of heterogeneous genome differences across multiple contact
zones in a crow species complex. Nature Communications, 7:13195.
Waits, L.P., Luikart, G. and Taberlet, P. (2001). Estimating the probability of identity among
genotypes in natural populations: cautions and guidelines. Molecular Ecology, 10, 249-256.
Walkinshaw, L. H. (1973). Cranes of the World. Winchester Press, New York.
Wallin, H., Kvamme, T. and Bergsten, J. (2017). To be or not to be a subspecies: description
of Saperda populnea lapponica ssp. (Coleoptera, Cerambycidae) developing in Downy
Willow (Salix lapponum L.). ZooKeys, 69:103-148
Watanabe, T (2006). Comparative breeding ecology of Lesser Sandhill Cranes (Grus
canadensis canadensis) and Siberian Cranes (G. leucogeranus) in Eastern Siberia. A
dissertation by Tsuyoshi Watanabe submitted to the Office of Graduate Studies of Texas
A&M University in partial fulfilment of the requirements for the degree of Doctor of
Philosophy. December 2006.
184
White, D. M. (1987). The status and distribution of the Brolga in Victoria, Australia. In:
Proceedings of the 1983 International Crane Workshop. Baraboo, Wisconsin, USA:
International Crane Foundation. Based on the proceedings of the workshop held in Bharatpur,
India, February 1983. (eds G. Archibald and R. F. Pasquier) pp. 115-31.
White, M. E. (1997). After The Greening. Kangaroo Press, Kenthurst.
Whitfield, S., Challinor, A.J. and Rees, R.M. (2018). Frontiers in climate smart food systems:
outlining the research space. Frontiers in Sustainable Food Systems, 2:2.
Whitlock, M.C., McCauley, D.E. (1999). Indirect measures of gene flow and migration: FST ≠
1/(4 Nm + 1). Heredity, 82: 117-125.
Wilson, E.O. and Brown, W.L. Jr (1953). The subspecies concept and its taxonomic
application. Systema Zoologica, 2:97–111.
Winker, K. (2009). Reuniting phenotype and genotype in biodiversity research. BioScience,
59:657-665.
Wood, T.C. and Krajewski, C. (1996). Mitochondrial sequence variation among the
subspecies of Sarus Crane (Grus antigone). The Auk, 113:655-633.
Wright, H.L., Lake, I.R. and Dolman, P.M. (2012). Agriculture - a key element for
conservation in the developing world. Conservation Letters, 5:11–19.
Zachos, F.E. (2018). Species Concepts in Biology: Historical Development, Theoretical
Foundations and Practical Relevance. Switzerland, Springer Nature.
Zink, R.M., Groth, J.G., Vázquez-Miranda, H. and Barrowclough, G.F. (2013).
Phylogeography of the California Gnatcatcher (Polioptila californica) using multilocus DNA
185
sequences and ecological niche modelling: Implications for conservation. The Auk,
130(3):449-458.
Zong, Y., Huang, G., Li, X.Y. and Sun, Y.Y. (2016). Late Quaternary tectonics, sea-level
change and lithostratigraphy along the northern coast of the South China Sea. Geological
Society of London, Special Publications, 429(1):123-136.