Clever : Investigating behaviour and learning in wild Torresian crows ( orru) and related Cracticids in a suburban environment

Author Brown, Matthew Jonathan

Published 2016-08

Thesis Type Thesis (PhD Doctorate)

School Griffith School of Environment

DOI https://doi.org/10.25904/1912/3190

Copyright Statement The author owns the copyright in this thesis, unless stated otherwise.

Downloaded from http://hdl.handle.net/10072/370411

Griffith Research Online https://research-repository.griffith.edu.au

Clever crows: Investigating behaviour and learning in wild Torresian crows (Corvus orru) and related Cracticids in a suburban environment

Matthew Brown B.Sc. (Ecol. & Cons. Biol.), B.Sc (Hons)

Griffith School of Environment

Griffith Sciences

Griffith University

A thesis submitted in fulfilment of the requirements of the degree of Doctor of Philosophy

August 2016

Synopsis

Few scientific fields spark the imagination of the public quite like the study of intelligence. For centuries, humanity’s ability to think and to create have represented characteristics that many have cited as being “what separates us from the ”. However, through the careful studies of a number of key taxa, the basis for this view of human exceptionalism has been heavily eroded. Tool use, for example, was found in chimpanzees, while accounts of intelligent behaviours in dolphins were frequently reported. Humanity’s apparent uniqueness became just one end of a continuum of intelligent behaviours displayed by a wide range of . Nonetheless, it is only recently that certain groups of have been elevated to the realm of intelligent fauna. These investigations have been dominated by two taxa: the parrots (: Psittaciformes) and the corvids (Family: ).

Many facets of high cognition have been described in the corvids, including tool use, social learning and theory of mind. The knowledge garnered from studies of the corvid family has been promising, yet it remains limited by the small number of species. This study attempts to complement and expand current knowledge by undertaking carefully designed experiments on a little-studied but eminently suited Australian species, the Torresian (Corvus orru), in a suburban environment.

This thesis is comprised of four sections, detailing the research project conducted between 2012 and 2016 in . Within these four sections are nine chapters. The first two chapters provide an overview of the nature of the corvids and of the Superfamily , before detailing the potential consequences of conducting behavioural research entirely in a controlled setting, describing the environment in which the study was conducted as well as the study species and sites.

The third chapter provides an in-depth review of trends in the literature regarding cognition in the corvids. This review found that the research was heavily biased towards studies on animals held in captivity, whether they be hand-reared or wild-caught birds. The study also found that, although the corvids are a near-worldwide group of approximately 120 species, almost all of the scientific literature surrounding the group has been conducted on just 14

i species, almost entirely in Europe and North America. Based on the results of this review, it appeared that an intensive study into a species from a different region and conducted on wild animals would be beneficial to the field.

The fourth chapter documents the methods devised and tested in the suburban environment, and discusses their level of success. Conducting experiments originally designed for use in a controlled laboratory setting on free-living animals in the wild required significant modifications to apparatus and methods. The need to attract crows while minimising interference from the many other species present in the area was a constant concern, and required the trialling of several kinds of bait. Apparatus were significantly modified several times throughout the study. This chapter documents these modifications to provide an extensive list of what does and does not work when studying learning behaviours of wild birds.

The second section includes four chapters, each of which is a piece of original research written in the form of a publication. The first of these (already been published in the journal Ethology) investigated the extent to which Torresian crows displayed neophobic behaviours in the wild, compared with three other corvoid birds common in suburban Brisbane: the Australian ( tibicen), grey (Cracticus torquatus) and pied (Strepera graculina). It was found that Torresian crows, like overseas corvids, are highly neophobic, being both significantly delayed in attaining food and displaying more neophobic behaviours when a novel object was present. The was affected by the novel object far more than any of the other three species studied.

Associative learning and shape discrimination were tested on five wild Torresian crows, three of which were successful. Numerosity, a form of rule-learning, was then tested in two of the crows that succeeded in the shape discrimination task. No crows were successful in distinguishing between different quantities.

Crows and other urban species were also exposed to Mirror-Image Stimulation (MIS), in light of several other studies on MIS and Mirror Self-Recognition in corvid species. Crow behaviour was significantly affected by the presence of a reflective surface, and this behaviour was relatively consistent between individuals. Crows behaved in a similar fashion to two native Cracticids, the and , and two invasive

ii species common in urban areas, the common myna (Acridotheres tristis) and spotted dove (Spilopelia chinensis). Other native species studied acted in a dissimilar way. Both territorial crows and reacted in a very dissimilar way to their usual response to seeing a conspecific in their territory.

Finally, crows and pied (Cracticus nigrogularis) were tested for their ability to solve a horizontal string-pulling problem and to discriminate between two parallel and two crossed strings, only one of which would result in a food reward. Only one crow spontaneously solved the problem, but then went on to fail the string discrimination task. Only two Torresian crows were able to distinguish between the parallel strings and none were capable of solving the crossed string experiment, producing similar results to what has been recorded in New Caledonian crows (Corvus moneduloides). Results suggested that the majority of crows tested were simply pulling a string without considering whether it was attached to the food reward. Conversely, pied butcherbirds excelled in this task, not only solving both tasks to a much greater degree than crows but also doing so without training.

This thesis has attempted to complement the existing literature on corvid cognition by studying an Australian species intensively in the wild environment. In doing so it has established that the behaviour of Australian crows was similar to their overseas cousins in a number of ways, including neophobia, associative learning and string discrimination. However, it is likely that the uncontrolled nature of wild experimentation may have hampered crow performance, and more controlled investigations may yield better results. On the other hand, this thesis has unveiled the butcherbirds (Cracticus spp) as being a group performing particularly well in cognitive tasks. It is quite possible that this could provide a third group of highly-intelligent birds, in addition to the corvids and parrots, for experimentation. Further investigations into this group could prove particularly fruitful.

iii Table of Contents

Synopsis ...... i List of Figures ...... ix List of Tables ...... xii Acknowledgements ...... xiii Statement of originality ...... xiv Acknowledgement of papers included in this thesis ...... xv Section 1: Background and Approach ~

Cognition and Corvids: An overview ...... 17 Cognition and Corvids ...... 17 Studying animal minds ...... 17 Higher cognition in the corvids ...... 19 Australian species of interest: The Corvoidea ...... 20 Study species: Torresian crow (Corvus orru) ...... 27 The approaches adopted in this thesis ...... 29 Thesis structure ...... 32 Corvoids and captivity: Study species and study sites ...... 34 Comparative cognition in the lab and field ...... 34 A case for field work ...... 34 Stress and welfare in captivity ...... 35 Differences in results between lab and field studies ...... 37 Native birds in urban environments ...... 39 Brisbane: Birds in a sub-tropical urban jungle ...... 40 Non-corvid study species ...... 43 Study Sites ...... 47 Studies on corvid cognition: a review ...... 50 Introduction...... 50 Advantages and drawbacks of laboratory studies ...... 50 Corvids ...... 51 Methods ...... 51 Results ...... 53

iv Discussion ...... 57 Conducting field experiments on wild Torresian crows: Advantages and challenges 60 Introduction...... 60 On trapping, banding and keeping wild crows ...... 60 Targeting wild adults ...... 60 Case study: Notes on keeping a captive adult Corvus coronoides ...... 61 Stationary funnel trap...... 62 Ladder entrance trap ...... 63 Bal-chatri trap ...... 66 “Noose carpet” trap...... 66 Behaviour of banded crows ...... 68 Familiarisation and training ...... 69 Excluding and including heterospecfics ...... 70 Observing and recording behaviours ...... 71 Experimental methodology ...... 72 Testing neophobia on wild birds ...... 72 Shape discrimination and numerosity: attempting learning tasks with wild animals ..... 74 Documenting responses of wild urban birds to their own reflections ...... 76 String pulling: trial and error in assembling apparatus ...... 80 Section 2: Experimentation and Results ~ Cautious crows: Neophobia in Torresian crows (Corvus orru) compared with three other corvoids in suburban ...... 88 Abstract ...... 88 Introduction...... 88 Methodology ...... 93 Study area ...... 93 Experimental design ...... 93 Data analysis ...... 94 Results ...... 94 Neophobia in wild urban crows ...... 94 Comparison of neophobia in urban corvoids ...... 96

v Discussion ...... 98 References ...... 100 Shape and quantity discrimination in wild Torresian crows (Corvus orru) in an urban environment ...... 105 Abstract ...... 105 Introduction...... 105 Cognition in crows ...... 105 Associative learning, rule learning and shape discrimination ...... 106 Numerosity ...... 107 Learning in Australian birds ...... 108 Methods ...... 110 Study species ...... 110 Study sites and apparatus ...... 110 Shape discrimination ...... 112 Numerosity ...... 112 Data analysis ...... 113 Results ...... 114 Shape discrimination ...... 114 Numerosity ...... 115 Discussion ...... 115 Responses of wild Torresian crows (Corvus orru) and other corvoids to their own reflection in an urban environment...... 118 Abstract ...... 118 Introduction...... 118 Investigating Mirror-Image Stimulation ...... 118 Urbanisation ...... 119 Suburban adapters in Brisbane ...... 120 Aims ...... 121 Methods ...... 122 Study sites and field work ...... 122 Behaviour categorisation ...... 123 Testing for agreeability ...... 124 Data analysis ...... 124

vi Results ...... 125 Discussion ...... 129 Discriminatory string-pulling in wild Torresian crows (Corvus orru) and pied butcherbirds (Cracticus nigrogularis) in a suburban environment ...... 132 Abstract ...... 132 Introduction...... 132 String pulling and insight in birds ...... 132 Discriminatory string pulling ...... 134 Corvids ...... 135 Study site and species ...... 136 Aims ...... 136 Methodology ...... 137 Study sites and species ...... 137 Experimental procedure ...... 137 Results ...... 139 Discussion ...... 142 Section 3: Conclusions and Reflections ~

Clever crows; a general discussion ...... 145 Behavioural capabilities of the Torresian crow compared to conspecifics ...... 145 Surprising results: the behaviours of non-corvid native urban birds in Brisbane ...... 147 Conducting learning experiments in the wild ...... 147 Weaknesses in methodology ...... 149 Propositions for future research ...... 150 Section 4: References and Appendices ~ References ...... 153 Appendices ...... 168 Appendix I: EQ ratio of native study species ...... 168 Appendix II: Studies reviewed in Chapter 3 analysis ...... 169 Appendix III: Detailed description of study species ...... 176 Corvoids ...... 176 Other species ...... 179

vii Appendix IV: Scorer sheet used in trial categorisation ...... 181 Appendix V: Scorer sheets used in final mirror classification ...... 182 Appendix VI: Correlations between scorers ...... 183 Appendix VII: Results of ANOSIM ...... 188

viii List of Figures

Figure 1.1 Phylogeny of the Corvoidea ...... 22 Figure 1.2 Geographic distribution of the Australian corvids ...... 24 Figure 1.3 Suggested phylogeny of Australian corvids ...... 24 Figure 1.4 Age-related changes in eye colour of the Australian corvids ...... 25 Figure 1.5 Torresian crow utilising anthropogenic foods inside a convenience store in Brisbane's inner-suburbs ...... 29 Figure 2.1 Human population change in Queensland and Brisbane 2012-2013 by Statistical Area 2 ...... 41 Figure 2.2 Locations where neophobia experimentation was conducted on Torresian crows, Australian magpies, grey butcherbirds and pied ...... 47 Figure 2.3 Map of eight experimental sites used in this project...... 48 Figure 3.1 Captive status of subject birds used in published studies on cognition in corvids...... 53 Figure 3.2 Number of cognition papers published for each species of corvid...... 54 Figure 3.3 Sample sizes in the reviewed literature of corvid cognition are commonly small. 55 Figure 3.4 Contribution of research institutions to the literature on corvid cognition...... 56 Figure 3.5 Historical trends the publishing of studies on corvid cognition, showing a significant increase in papers published from the mid-1990’s...... 57 Figure 4.1 Australian crow trap...... 64 Figure 4.2 Ladder trap constructed at Griffith University ...... 65 Figure 4.3 Noose carpet trap visible on concrete...... 67 Figure 4.4 Noose carpet trap camouflaged in natural surface...... 67 Figure 4.5 Crow E, caught at Griffith University with the noose carpet trap...... 69 Figure 4.6 Diagram of study sites for study of neophobia. Interaction time began when crow crossed imaginary 1m radius circle surrounding the bait...... 73 Figure 4.7 Novel object used in the study of urban corvoid neophobia...... 73 Figure 4.8 Arrangement of shape discrimination apparatus. Bowls were placed at a 4m distance to punish crows that did not flip over the correct bowl...... 75

ix Figure 4.9 All six combinations of the four numerosity bowls. Bowls were placed at random to prevent any pattern other than the number of dots from informing crows of the location of bait...... 76 Figure 4.10 Mirror deployed in suburban backyard. Mirror was placed at wall to reduce impact of neophobia...... 77 Figure 4.11 Cumulative number of recordings of each species in front of a mirror, at a total of eight sites ...... 78 Figure 4.12 Distribution of 50 videos used in cross-referencing trial across different species...... 79 Figure 4.13 Process used by a bird in order to pull up a vertical string (Heinrich 1995)...... 80 Figure 4.14 Original vertical string pulling apparatus ...... 81 Figure 4.15 crawling down vertical string to obtain beef...... 82 Figure 4.16 Cage used for string discrimination experiment (a), set for parallel (b) and crossed (c) experiments...... 83 Figure 4.17 Diagram of final horizontal string pulling apparatus...... 85 Figure 5.1 Interaction time of Torresian crows in different novelty levels ...... 95 Figure 5.2 Frequency of jumping jacks displayed by Torresian crows in different novelty levels...... 96 Figure 5.3 Interaction time with novel treatment of four Corvoid species...... 97 Figure 5.4 Frequency of jumping jacks with the novel treatment in four Corvoid species. .... 97 Figure 6.1 Diagram of shape discrimination experimental apparatus ...... 111 Figure 6.2 Each of the 6 possible combinations of quantities that crows were presented with ...... 113 Figure 6.3 Success of subject crows in shape discrimination experiment...... 114 Figure 7.1 Behaviours of Torresian crows at Site A. The existence of a reflective surface results in a significant shift in behaviour...... 126 Figure 7.2 Principal Component Analysis of Torresian crows at Site A shows the existence of a reflective surface affects crow behaviour in a generally agreed-upon way...... 126 Figure 7.3 Principal Components Analysis of Torresian crow behaviours when presented with mirrors. With the exception of two sites, crow responses to the reflective were consistent with a similarity of 70%...... 127

x Figure 7.4 MDS ordination of behaviours of suburban Brisbane birds when presented with mirrors ...... 128 Figure 8.1 Diagram of string discrimination apparatus. Milk bottle caps (MBC) were connected to stick. As string is pulled, stick is moved once MBC exits box, allowing the lid to snap shut ...... 138 Figure 8.2 Cumulative success of birds subject to the parallel string test ...... 141 Figure 8.3 Cumulative success of birds subject to the crossed string experiment ...... 141

xi List of Tables

Table 1.1 Thesis structure...... 33 Table 2.1 Summary of study species...... 44 Table 2.2 Location and description of sites throughout southern suburban Brisbane...... 49 Table 6.1 Ratios between quantities presented to crows...... 113 Table 7.1 Social and territorial aspects of suburban bird species in Brisdbane relevant to this study ...... 120 Table 7.2 Examples of behavioural states typical of the four categories ...... 123 Table 7.3 Comparative table of R-statistics and p-values from ANOSIM test in Primer 6.. 128 Table 8.1 Performance of Torresian crows and pied butcherbirds with parallel strings .... 140 Table 8.2 Performance of Torresian crows and pied butcherbirds with crossed strings ... 140

xii Acknowledgements

I would like to firstly acknowledge the contributions of my primary supervisor, Professor Darryl Jones, in all aspects of this PhD project. Prof. Jones has provided invaluable advice on conducting this project, regarding research, experimental design and writing, as well as aiding in field work, particularly in the efforts to capture and band wild crows. More importantly he has supported this project and myself through turbulent times, and for that I am very thankful.

I’d also like to thank Dr Gurudeo Anand Tularam and Mr James McBroom for their advice regarding methods of determining agreement between scorers and in analysing data for the first experimental chapter respectively.

For assistance in categorising videos of bird behaviour, I would like to thank Glenys-Julie Harris, Scott Brown, Lyndall Brown, Michelle Brown, Chetan Hemmadi, Vikasini Hemmadi and Pranav Hemmadi. Finally, I would like to thank my fiancé Priyanka Hemmadi for not only her assistance in field work and editing but also for her persistent support over the course of the project.

This research was supported financially by an Australian Postgraduate Award from Griffith University as well as funds from the Griffith School of Environment. All research within this thesis was conducted with the approval of the Griffith University Animal Ethics Committee (GU Ref No: ENV/15/12/AEC) (GU Ref No: ENV/16/12/AEC).

For Blackie.

xiii Statement of originality

This work has not previously been submitted for a degree or diploma in any university. To the best of my knowledge and belief, the thesis contains no material previously published or written by another person except where due reference is made in the thesis itself.

(Signed)______

Matthew Brown

xiv Acknowledgement of papers included in this thesis

Included in this thesis is a paper in Chapter 5 which are co-authored with other researcher. My contribution to the co-authored paper is outlined at the front of the relevant chapter. The bibliographic details for this paper including all authors, are:

Chapter 5: Brown, M. J. and Jones, D. N. (2016), Cautious Crows: Neophobia in Torresian Crows (Corvus orru) Compared with Three Other Corvoids in Suburban Australia. Ethology, 122: 726– 733. doi:10.1111/eth.12517

Appropriate acknowledgements of those who contributed to the research but did not qualify as authors are included in each paper.

(Signed) ______(Date)______

Matthew Brown

(Countersigned) ______(Date)______

Supervisor: Prof. Darryl Jones

xv

Section 1: Background and Approach

͠

16 Cognition and Corvids: An overview

Cognition and Corvids

Studying animal minds

Over the past millennium, scientific discoveries have significantly changed society’s view of the world and of itself. The once self-evident belief in biological human exceptionalism have slowly been reassessed, our apparent disconnection with the rest of the animal kingdom being altered, initially through the acceptance of Darwin’s (1859, 1871) theory of evolution by natural selection (Hauser et al. 2002). More recently, discoveries such as Jane Goodall’s (1971) uncovering of apparently human-like culture in the behaviour of chimpanzees has been influential in changing the way we view our place in the Animal Kingdom in regards to intelligence and cognitive abilities. While human exceptionalism remains a prevalent viewpoint, the discovery of such anthropomorphic behaviours as tool-use in a non-human species engages the public consciousness in a way that does not often occur in other fields (Angell and Marzluff 2005, Marzluff and Angell 2013).

Cognition is arguably the ultimate trait that defines the anthropocentric view, even giving our species, Homo sapiens, its scientific name. Cognition is defined by Shettleworth (1998, p5) as “the mechanisms by which animals acquire, process, store and act on information from the environment”. Previous models of animal minds, such as that proposed by Descartes in the 17th Century, saw animals as simple machines acting purely through instinct and behaving in a predictable pre-programmed way to certain activities: the stimulus- response paradigm (Shettleworth 1998, Kaplan 2015). This belief persisted within science and the general public until the 20th Century, but is now generally regarded to be either overly simplistic or outright incorrect for a large number of species (Kaplan 2015). In the 1970’s, scientific studies of animal cognition, predominantly based on studies of associated learning in rats and pigeons in captivity, investigated processes that had already been established in humans such as memory and problem solving (Reviewed in Shettleworth 1998).

Cognition cannot be measured as a single phenomenon; instead its study must rely on measurements of a number of parameters (Kaplan 2015). Attempting to understand the

17 extent of an organism’s ability in a number of tasks, such as memory, conceptualisation and discrimination, is necessary to attempt an estimate of the species’ overall cognitive capacity. This concept was expanded upon by the advent of the field of cognitive ethology, whose advocates claimed that animals were actually conscious beings capable of intentions, thoughts and planning for the future (Shettleworth 1998). While animal consciousness is difficult to demonstrate empirically (Dawkins 1993), its proponents gained significant public attention with the 2012 Cambridge Declaration on Consciousness (Low et al. 2012), which states:

“The absence of a neocortex does not appear to preclude an organism from experiencing affective states. Convergent evidence indicates that non-human animals have the neuroanatomical, neurochemical, and neurophysiological substrates of conscious states along with the capacity to exhibit intentional behaviours. Consequently, the weight of evidence indicates that humans are not unique in possessing the neurological substrates that generate consciousness. Nonhuman animals, including all mammals and birds, and many other creatures, including octopuses, also possess these neurological substrates.”

While the question of animal consciousness remains controversial, with many cognition researchers still agnostic to the idea (Shettleworth 1998), the existence of complex cognitive mechanisms in non-human animals is now well-established and is broadening (Kaplan 2015, Angell and Marzluff 2005, Marzluff and Angell 2013, Zentall and Wasserman 2012). Traits normally associated with higher intelligence, such as tool use, were first recognised in non- human great apes, before being discovered in other primates and then non-primate mammals such as dolphins and elephants (Emery 2006, Cornell Laboratory of Ornithology 2009). In recent decades, the topic of higher intelligence in birds has gained greater recognition.

“It is everywhere recognized that birds possess highly complex instinctive endowments and that their intelligence is very limited” - (Herrick 1924). Birds have historically been regarded by modern science and culture as creatures of instinct due to lacking a neocortex, the part of the mammalian brain thought to be the source of cognition, language and spatial reasoning (Emery 2006). These animals were therefore

18 generally thought of as being incapable of higher thought (Emery 2006). Recent studies have, however, changed the modern understanding about avian intelligence, showing that some groups possess enlarged forebrains, thought to be an indicator of higher intelligence (Humphrey 1976, Whiten and Byrne 1988). This hippocampus, now known to be the avian equivalent of the mammalian neocortex, is most enlarged in two groups: the corvids (crows and ravens) and the psittids (parrots) (Emery 2006). Low et al. (2012) describe the similarities in function between the neocortex and hippocampus as “a striking case of parallel evolution of consciousness”. Many species in these groups also partake in significantly complex societies (Angel and Marzluff 2005). The need to keep track of the status of and relationships with conspecifics requires significant brainpower and is generally agreed upon to be a predominant selecting driver for intelligence, a theory known as the Social Intelligence Hypothesis (Humphrey 1976). Such characteristics have lead crows to be described as “feathered apes” (Emery 2004); Emery adds: “there is something very special about the cognitive abilities of crows and parrots” (Emery 2006, p23).

Higher cognition in the corvids

While reports of higher-level “thinking” among animals has generated great public interest, this appears to be enhanced when the species involved is particularly familiar and one with which people interact regularly. In no other group is this combination of cognition and human interaction more prevalent than in the corvids. As evidenced daily, corvids around the globe are among the most abundant and successful taxa of wild species to have colonised the urban environment (Marzluff et al. 2001, Goodwin 1976). Indeed, it is in the cities of the world where corvid intelligence is on conspicuous display. Despite this, studies of the behaviour of urban corvids are remarkably few.

The word ‘corvid’ is often used to refer to either of two taxonomic groupings: a member of the Genus Corvus, which includes the crows, ravens and rooks, or more broadly, members of the Corvidae Family, extending the definition to include other groups such as magpies and jays (Goodwin 1976, Madge and Burn 1999, Angell and Marzluff 2005). In discussions of intelligence, ‘corvid’ has come to refer more often to the latter, due to the comparative cognitive abilities of magpies and jays (Balda and Kamil 2002, Angell and Marzluff 2005). Members of the Corvus genus are often referred collectively as ‘crows’, regardless of whether they are a crow, raven or (Goodwin 1976). There are 40 Corvus species

19 worldwide and over 120 Corvidae, which range in size from the 40g dwarf ( nana) of Mexico to the 2kg thick-billed raven (Corvus crassirostris) of Ethiopia (Goodwin 1976, Madge and Burn 1999). Despite their infamous harsh calls and most mundane , corvids are, in fact, and are widely regarded as the peak of avian intelligence (Goodwin 1976, Debus 1996, Angell and Marzluff 2005).

Corvids are of particular interest to those who study behaviour because of their unusual and impressive cognitive abilities (Angell and Marzluff 2005). Recent studies are beginning to extend our knowledge of these very intelligent birds with the following features being investigated: self-recognition (Kusayama et al. 2000, Prior et al. 2008, Medina et al. 2011), tool-use (Montevecchi 1978, Hunt 2000a, b, Caffrey 2000, 2001, Weir et al. 2002, Bluff et al. 2007, Balda 2007, Bird and Emery 2009a, Wimpenny et al. 2009, Mehlhorn et al. 2010), social learning (Templeton et al. 1999b, Holzhaider et al. 2010), cultural evolution (Marzluff and Angell 2005, Marzluff et al. 2010), imagination (Heinrich 1995a, Bird and Emery 2009a), cooperation (Bossema and Benus 1985, Seed et al. 2008) and memory (Kamil and Balda 1990, Balda and Kamil 2002, Clayton et al. 2007, Marzluff et al. 2010). Emery (2004, 2006) suggestions that corvids should be considered “feathered apes” is due to their impressive cognitive ability and that the recent reappraisal to our fellow apes for their intelligence should also be extended to these birds. The recent practise of designing experiments testing intelligence to be suited to the species’ own natural history, as opposed to anthropocentric tests, has played no small part in the these advances in our understanding of corvids (Emery 2004, 2006, Clayton and Emery 2005). In the Northern Hemisphere, extending corvid research to the jays and true magpies is reasonable, as these species are readily available and exhibit many of the behaviours that have made the crows and ravens of such interest (Goodwin 1976). On the other hand, in Australia the Corvidae are represented by only five species scattered across the continent (Rowley 1970). Any comparative work in the Australian context should therefore should be refocussed on the superfamily Corvoidea. This superfamily, including a wide range of species from the birds of paradise to the butcherbirds, is a dominant group of birds found throughout the continent (Kaplan 2015).

Australian species of interest: The Corvoidea

The Aves class originated in Eastern Gondwana (now Australia), surviving the Cretacious- Tertiary event that wiped out their dinosaur cousins. Somewhat similar to the situation of

20 Africa in the origin of hominids, Australia has played a special role in the evolution of songbirds (Order: Passeriformes) (Kaplan 2015, Low 2014). Barker et al. (2004) showed conclusively that originated in Gondwana, not in Asia. This argument, however, was being made by Australian scientists decades earlier but was often dismissed due to Australia’s relatively low count of bird species and the possibly bias on part of the scientific community towards the Northern Hemisphere (Kaplan 2015, Low 2014).

The parvorder (now defunct) is notable as the vast majority of species for which cognitive traits have been noted come from this group (Sibley and Ahlquist 1985). In the Corvida, behaviours such as cooperative breeding, thieving and cheating, innovation and tool use, complexity in communication and sociality and mobbing are particularly prominent (Kaplan 2015). Along with large brains, many species in this group also partake in play, which Montgomery (2014) suggests is strongly correlated with intelligence. The similarities between this group and the behaviours observed specifically in the Northern Hemisphere Corvidae suggest that a broader sweep of species may yield results showing a more extensive occurrence of these features. Within this parvorder, the Corvoidea are a monophyletic group, with groups such as , and excluded.

The Corvoidea is a superfamily of some 800 species of passerine birds that are found world- wide (Jønsson et al. 2016). The group originated in the proto-Papuan region (now and West Papua) approximately 30 million years ago, an area that has acted as a ‘species pump’ resulting in a large diversification of species early in the group’s evolution (Jønsson et al. 2016). Jønsson et al. (2016) formulated a comprehensive genetic analysis of the Corvoidea, establishing the relationships between these diverse groups of birds (Fig. 1.1). Of most interest to this study is the phylogenic distance between the two families that contain the species studied: the Corvids and the Cracticids. These two groups are quite distantly related, diverging approximately 27 million years ago (Jønsson et al. 2016).

The exact of the Cracticids is heavily disputed. Some authors consider the Cracticidae and as two separate families (e.g., Nguyen et al. 2013, Dickinson 2003, Johnstone and Storr 2006), the butcherbirds and currawongs in the first and the in the latter. Another group (e.g., Higgins et al. 2006a, Christidis and Boles 2008, Jønsson et al. 2016) consider these groups to be subfamilies of a unified Artamidae. Depending on any final agreement on the family taxa, the species of interest lie in either the

21 ‘Cracticidae’ or ‘Cracticinae’, whose relationship to Corvidae as determined in Jønsson et al. (2016) remains undisputed. For simplicity, this thesis will refer to the group as the Cracticidae.

Figure 1.1 Phylogeny of the Corvoidea (Jønsson et al. 2016).

22 There are an abundance of ecological and physiological similarities between crows and Cracticids (Brown and Veltman 1987). Both groups have relatively long lifespans (>15 years) and do not achieve sexual maturity for at least a year (Kaplan 2004). Juveniles are dependent on their parents for a long period of time, begging for food from their parents for three months after fledgling and staying with their parents for longer, while these juveniles will often take part in play (Ficken 1977, Pellis 1981a, b, Heinrich and Smolker 1998, Kaplan 2008, 2015, Angell and Marzluff 2005, Marzluff and Angell 2013). Long-term relationships are common in each taxa, with obligate monogamy in corvids and stable pairing in cracticids (Higgins et al. 2006a). Both groups have also been documented bonding with human companions (Angell and Marzluff 2005, Haupt 2009, Kaplan 2004) and readily kill adult birds and small mammals (Kaplan 2004, Higgins et al. 2006a). Crows (Corvus spp), butcherbirds (Cracticus spp) and currawongs (Septera spp) in Australia all cache food (Chapman 1978, Walters 1980, Rollinson 2002, Lewis 2016, Leonard 2016, Prawiradilaga 2016), though there have been no experimental studies conducted that would allow comparison to the plentiful empirical studies conducted in the Northern Hemisphere (Chapter 3; Kaplan 2004, e.g., Stafford et al. 2006, Clayton et al. 2007, Dally et al. 2010, Shaw and Clayton 2013). As is commonly the case in Australia, knowledge of this behaviour is based largely on anecdotal observation in the absence of intensive study. Butcherbirds are known to store their food above ground, wedged between branches (Higgins et al. 2006a); Torresian crows (Corvus orru) have been noted doing this only once (Chapman 1978), though all other reports of Australian corvid caching (Chapman 1978, Leonard 2016, Lewis 2016, Walters 1979, Secomb 2005) are of ground-based caches. This abundant similarity between species that are moderately related and inhabit similar niches, as well as their abundance in the study area, makes the Cracticids a logical point of comparison with corvids.

Introduction to Australian Corvids The Family Corvidae is represented in Australia by five species of Corvus, the Australian raven (C. coronoides), (C. mellori), (C. tasmanicus), (C. bennetti) and Torresian crow (Rowley 1970, Debus 1996, Christidis and Boles 2008). Due to their similarity in morphology, behaviour and vocalisations are regarded as the best field identifiers for these species (Rowley 1970, Debus 1980, 1995, 1996). Australian corvids are

23 divided phylogenically into the ‘ravens’ (predominantly in the south of the continent) and the ‘crows’ (predominant in the north) (Fig. 1.2) (Rowley 1970, 1973d, Debus 1980, 1996) and form a monophyletic (Fig. 1.3). Their most striking feature is their unusual eye colour, a white iris with a blue inner ring around the , a trait shared only with the Moluccan long-billed crow (C. validus) and some species from Papua New Guinea and surrounding islands (Rowley 1970, Debus 1996). Eye colour is an effective indicator of age in the field as the colour gradually changes over the young crow’s lifetime (Fig. 1.4) (Rowley 1970).

Figure 1.2 Geographic distribution of the Australian corvids (Rowley 1973d).

Figure 1.3 Suggested phylogeny of Australian corvids (Rowley 1973d).

24

Figure 1.4 Age-related changes in eye colour of the Australian corvids (Rowley 1970).

Three of the five Australian corvid species (C. coronoides, C. tasmanicus, and C. orru) are sedentary, settling down into permanent defended territories once they have paired. The other, smaller species (C. mellori and C. bennetti) live mainly nomadic lives, enabling them to inhabit the more inhospitable parts of the continent (Rowley 1970, Debus 1980, 1996), though more recent literature has noted sedentariness in suburban little ravens (Whisson et al. 2015). All five species form nomadic flocks at some point in their life history with the sedentary species typically settling down after having found a mate. Once the pair has mated the pair-bond normally persists until one of the pair dies and they appear to cooperate in every facet of daily life, not just while breeding (Rowley 1973a, Rowley et al. 1973, Debus 1996). Kaplan (2015) notes that there has been no systematic cognitive study on the Australian corvids.

It must not be presumed that Australian corvids are highly intelligent, although the cognitive abilities of Northern Hemisphere and New Caledonian corvids, as well as numerous anecdotes from Australia, suggest that there is likely a benefit to assessing these species

25 (Kaplan 2015). The similar behaviour of corvids and the Cracticids, including caching, makes these species of interest as well. The well-known example of learning shown by an Australian corvid is that of Torresian crows and pied currawongs predating upon poisonous cane toads (Bufo marinus), the only native Australian species to do so (Donato and Potts 2004). This method, which involves flipping toads over to avoid the poisonous glands on their back, is now widespread in these species where cane toads are common.

Human-crow interactions in Australia In Australia, interactions between humans and corvids mirror that which has occurred elsewhere. Corvids are thought to have used the waste associated with Aboriginal activities as a food source for thousands of years, an interaction which persists in some Aboriginal societies today (Goodwin 1976). With the arrival of European settlers, corvids were often poisoned in large numbers as they were thought “likely to be troublesome” (Sinden 2002). The landmark series of studies on the Australian corvids undertaken by CSIRO ornithologist Ian Rowley (Rowley 1967, 1969, 1970, 1973a, b, c, d, Rowley et al. 1973) was initially carried out to investigate whether Australian ravens were killing lambs. Although the studies disproved any link between ravens and lamb deaths, the myth and associated hatred of corvids has continued in rural Australia (Sinden 2002, e.g. Lownds 2011).

In recent decades, corvids have come to be associated with the urban environment where they are provided with a reliable food source and are protected by law from shooting that can still occur in rural areas (Everding 1995, Marzluff et al. 2001, Angell and Marzluff 2005, Marzluff and Angell 2005, Marzluff and Neatherlin 2006). The urbanisation of Australian corvids has been documented in a number of sources (Everding 1995, Stewart 1997, Department of Environment 1998, Veerman 2002, Woodall 2004, Department of Environment and Conservation 2007, Whisson et al. 2015), although of particular interest is the phenomenon of communal roosting by Torresian Crows in suburban Brisbane, a practise more similar to foreign corvid species than their Australian relatives (Rowley 1973a, Everding 1995, Marzluff et al. 2001, Sinden 2002, Angell and Marzluff 2005, Everding and Jones 2006, Marzluff and Neatherlin 2006).

26 Study species: Torresian crow (Corvus orru)

The Torresian crow, one of five species of corvid in Australia, is all-black and approximately 550g in weight with subtle throat hackles (Coates 1990, Rowley 1970, 1973a, d). While mainly granivorous, its diet also includes invertebrates, and the young of other bird species. The bill, feet, , mouth and tongue of adults are black, while the mouth gape is pink in juveniles (Rowley 1970). They are the dominant corvid species for much of the northern half of the continent, extending from New England in along the coast to the Pilbara of .

Western and interior populations of this species are restricted by the presence of water and have not been recorded in large flocks, unlike eastern birds, which are far less restricted due to the higher rainfall in the region (Rowley 1970). In Western Australia, Curry (1978) described the normal social unit of the Torresian crow as consisting of one to three birds and that large groups are rare. This contrasts to birds from the East Coast, where large murders of crows are common (Everding 1995; M. Brown unpub. data). The preferred habitat of Torresian crows is uncertain due to inconsistencies in the literature (Sinden 2002) although it has come to be associated with urban environments in many coastal areas (Jones and Everding 1993, Everding 1995, Sinden 2002, Woodall 2004, Schlacher et al. 2013).

Torresian crow numbers have exploded due to anthropogenic changes to the environment (Higgins et al. 2006a), particularly urbanisation. In the subtropical city of Brisbane, crows have gone from being a relatively rare and wary bird in the early twentieth century (Jack 1938) to being extremely common throughout the city by the 1980s (Sinden 2002). Torresian crows spend much of their early life in nomadic juvenile ‘gangs’, which in Brisbane congregate around areas with high levels of anthropogenic waste such as shopping centres and popular parks (Sinden 2002; M. Brown unpub. data). After mating, crows pair for life in socially and spatially close relationships, settling down into a defended territory (Rowley 1973a).

The literature on Torresian crows is relatively sparse, with the vast majority of information coming from either Rowley’s foundational series on Australian corvids (1973a, 1970, 1969, 1973b, d, c, Rowley et al. 1973, Rowley 1967) or several studies of the ecology and

27 behaviour of the species within the urban environments of Brisbane (Brown 2011, Everding and Montgomerie 2000, Everding 1995, Everding and Jones 2006, Sinden 2002, Studer 2010, McCaig et al. 2015, FitzGibbon and Jones 2006, Jones and Everding 1993, Brown and Jones 2016). No studies as of yet have been conducted on learning behaviours in any species of Australian corvid.

While their behaviours are not as thoroughly documented in the literature as their Northern-Hemisphere cousins, Torresian crows have been noted by members of the public to take part in a number of behaviours that are indicative of higher thinking. These anecdotes together paint a picture of a species that could produce interesting results if studied empirically. Torresian crows have been noted by school administrators to unzip school children’s backpacks in order to steal lunches, doing so during classes when the bags are left unattended (R. Schablom pers. comm.). Additionally, crows have been reported stealing lunches from Griffith University field workers, who would leave their lunches unattended in sealed containers while working. The crows opened the containers and were seen flying off with the researchers’ biscuits in their (S. Pell pers. comm.). One member of the public reported several Torreisan crows cooperating to pull a carcass off of a rural road in the Sunshine Coast hinterland. One crow was seen perched on a high tree and cawed when vehicles approached, at which point the crows on the road would fly to safety. Crows were witnessed repeating this process for a period of ten minutes when the carcass was pulled safely to the side of the road (T. Benbrook pers. comm.). Finally, in the inner-city suburb of West End in Brisbane, a crow was witnessed walking along the footpath outside shops and cafes. The bird then walked into a convenience store and opened a packet of food, out of sight of the attendant (Fig. 1.5). Twenty minutes later, a crow (most likely the same individual) was chased out of an adjacent restaurant (M. Brown pers. obs.).

28

Figure 1.5 Torresian crow utilising anthropogenic foods inside a convenience store in Brisbane's inner- suburbs (Photo: M. Brown). The approaches adopted in this thesis

The field of avian cognition has grown substantially over the past few decades and undoubtedly at the heart of this field are the corvids (Emery and Clayton 2004, Clayton and Emery 2005). The literature on this topic has grown at a rapid rate recently, although it remains constrained to captive individuals from a small number of species (See Chapter 3). There are arguments (e.g., Cunningham 2013 as cited in Kaplan 2015) that there is no longer a need to simply catalogue tool use or other cognitive abilities in species, but instead what is required is a move to more intensive investigations. Behaviours such as tool use being found

29 in a non-human species (Goodall 1971), and then a bird (Hunt 2000a, b), were remarkable findings at the time but have now become commonplace as more and more species have been investigated. Kaplan (2015), however, argues that this view has a distinctly Northern Hemisphere bias, accepting a gross extrapolation from a small number of Northern species, often in captive environments, onto a broad and diverse group of animals. This is particularly true in the study of corvids, where the only Southern Hemisphere species sufficiently studied in the literature has been the New Caledonian crow (Corvus moneduloides), which by all accounts is exceptional in its cognitive abilities compared to the rest of its Family. Kaplan (2015) highlights the large gaps in our knowledge regarding Southern Hemisphere bird species, comparing this view to trying to fit the monotremes into a Northern Hemisphere understanding of mammalian biology, or attempting to fit the extraordinary song of the Australian magpie (Cracticus tibecin) into a model derived from small, migratory, sexually dimorphic songbirds.

Therefore, this present suite of studies will investigate learning behaviours in wild Torresian crows, one of the five corvid species that inhabit the Australian continent. The study was conducted on banded and unbanded wild crows in a suburban setting, with each question involving multiple individuals in several geographically separate sites to ensure independence and minimise biases.

Investigations into learning behaviours and cognition in animals are most frequently undertaken by presenting subject animals with an artificial problem-solving apparatus for which a certain kind of thinking is required. Typically, the animals must interact with the apparatus to obtain a reward. These devices, when first presented to the animal, are by- definition novel, as they would not have encountered it before. All mammals and birds are, to some extent, neophobic, where they are wary of novel things (Corey 1979). When held in captivity, the subject can be persuaded to eventually interact with the apparatus, but in the wild they are most likely to simply avoid the study in favour of food elsewhere in their territory. It is therefore of interest to understand the extent to which the study species expresses neophobia in the wild. Corvids worldwide are generally considered to be highly neophobic (Heinrich 1988a, Kijne and Kotrschal 2002), though this trait has not yet been studied in Australian taxa. This is discussed further in more detail in Chapter 5.

30 Many studies into animal learning and cognition focus upon rule learning. One of the more basic forms of learning is for a subject to learn, recognise and distinguish between arbitrarily drawn shapes (Wilson et al. 1985, Cook et al. 1997). Additionally, a number of species have been tested in their ability to distinguish between greater and lesser quantities. Assessing whether these skills can be adequately and reliably tested in the field would be informative of whether a systematic and detailed investigation into rule learning in wild crows is feasible.

One facet of cognition that birds have not performed particularly well in is mirror self- recognition (Prior et al. 2008), considered by some to be an indicator of self-consciousness or and understanding of self (Marino et al. 1994, Heyes 1995, De Veer and Van den Bos 1999). The trait can be investigated by confronting an animal with its own reflection via a mirror and documenting the resulting behaviours. A mark only visible by looking at a reflection is often placed on the subject, with behaviours directed towards the mark considered indicative of the animal understanding that the mirror image is of itself. Only one study on Eurasian magpies ( pica) has produced positive results for the mirror mark test (Prior et al. 2008), despite the Class’ otherwise impressive performance in recent decades.

One problem-solving experiment that is often used on birds is the string-pulling experiment, where birds are required to pull a vertical or horizontal string that is attached to a food reward (Heinrich 1995a). One aspect of these tests is discriminatory string-pulling, where birds are offered a choice between two available strings, one of which will result in a food reward (e.g., Taylor et al. 2010b, 2012b). This discriminatory string-pulling is used to test a number of cognitive traits, including an understanding of causality (Werdenich and Huber 2006).

In light of these variety of tests that have been conducted on corvids overseas, the current thesis will seek to answer the following research questions:

1. Do Torresian crows display high levels of neophobia? 2. How does the extent of neophobia in Torresian crows compare to related corvoids in the same environment?

31 3. Are Torresian crows capable of learning, remembering and recognising arbitrary shapes and associating them with a food reward? 4. Are Torresian crows capable of distinguishing between greater and lesser quantities based on a rule? 5. How do Torresian crows react when exposed to their own reflection? 6. Are the behaviours Torresian crows display when exposed to a mirror consistent and predictable between individuals? 7. How do Torresian crows’ reactions to encountering their own reflections differ from other urban birds? 8. Can Torreisan crows spontaneously solve a horizontal string pulling problem? 9. Can Torresian crows discriminate between two parallel or crossed strings to determine which will result in a food reward? 10. How does the performance of Torresian crows’ compare to that of another common urban corvoid: the ? 11. Can experiments generally used in controlled laboratory environments be utilised to study learning and cognition in a wild, uncontrolled environment with high bird diversity and abundance?

The detailed observational and experimental research to be undertaken in the present study will attempt to add to our understanding of corvid behaviour by conducting studies on a relatively unstudied Australian species, the Torresian crow in the wild. This new information will complement the growing body of knowledge on cognition in the corvids and birds generally. Additionally, noting intelligent behaviours in an animal that many Australians regularly interact with may potentially assist in fostering a greater interest on part of these people in the natural world around them.

Thesis structure

This thesis is a collection of published and unpublished works (Table 1.1). Chapters 1 and 2 document previous research in this field as synthetised from the literature, showing areas where the research base is strong and where further research would be beneficial. Chapter 3 critically reviews the literature on corvid cognition and summarises trends in species studied, sample sizes and whether studies were conducted on captive or wild individuals.

32 Chapter 4 outlines the trials that were encountered studying these birds in the wild and solutions that were utilised to overcome them. Chapters 5 to 8 are original individual experimental studies conducted on Torresian crows between 2012 and 2016, while Chapter 9 summarises and critically analyses both the results and the process of undertaking these works in the context of what has been done before.

Table 1.1 Thesis structure.

Ch1: Cognition and Corvids: An overview Ch2: Corvids and corvoids in suburban Brisbane: Study species

Section 1: Background and Approach and study sites Ch3: Studies of corvid cognition: A review Ch4: Conducting field experiments on wild Torresian crows Ch5: Cautious crows: Neophobia in Torresian crows (Corvus orru) compared with three other corvoids in suburban Australia Ch6: Shape and quantity discrimination in wild Torresian crows (Corvus orru) in an urban environment

Section 2: Experimentation and Results Ch7: Responses of wild Torresian crows (Corvus orru) and other corvoids to their own reflection in an urban environment Ch8: Discriminatory string-pulling in wild Torresian crows (Corvus orru) and pied butcherbirds (Cracticus nigrogularis) in suburban Brisbane

Section 3: Conclusions and Reflections Ch9: Summary of results, correlations and general conclusions References Appendix I: EQ of native study species Appendix II: Studies cited in Chapter 3 review Appendix III: Detailed description of study species Section 4: References and Appendices Appendix IV: Scorer sheet used in trial categorisation Appendix V: Sheets used in final classification Appendix VI: Correlations between scorers Appendix VII: Results of ANOSIM

33 Corvoids and captivity: Study species and study sites

Comparative cognition in the lab and field

A case for field work

When studying the behaviour of animals, it has become standard practice to perform experiments on captive individuals, typically hand-reared, in a carefully controlled laboratory environment (Calisi and Bentley 2009, Byrne and Bates 2011). This has allowed researchers to conduct a wide array of experiments that produce “clean” data, free of the noise that comes with environmental variation, while also allowing for environmental manipulation to test a variety of hypotheses (Calisi and Bentley 2009, Byrne and Bates 2011). While some researchers have been able to obtain a large amount of data from captive birds (Bossema and Benus 1985, Bugnyar and Heinrich 2006, Bugnyar and Kotrschal 2002a, Chappell and Kacelnik 2004, Heinrich 1995a, b), Mason (2010) has stressed that even closely-related species can react very differently to captivity, making the impact of the animal’s well-being on results an unpredictable factor. Consequently, while using captive animals is the general norm in the study of animal cognition, it may not necessarily be the best or only way to investigate animal minds (Byrne and Bates 2011). In most scientific fields, data from the field is regularly used to assess and compliment models and theories (Byrne and Bates 2011). As an evolutionary product of their environment, the behaviour of animals removed from the complex influences and stimuli of the natural world may not necessarily be representative of that of their wild counterparts (Calisi and Bentley 2009, Byrne and Bates 2011). By focussing predominantly on data from captive and hand-reared subjects, the field of comparative cognition may be missing or neglecting numerous sources of context and insight into the workings of animal minds (Byrne and Bates 2011). Wild studies can also overhaul previously-held theories of animal culture and behaviour, such as in Connor et al. (2010's)’s studies of wild bottlenose dolphins (Tursiops spp). Eric Pianka (in Calisi and Bentley 2009) states:

34 “(animals) only make sense when they are living in the natural environments in which they evolved and to which they have become adapted.”

Corvids have become of great interest to students of animal cognition and our understanding of these birds has greatly improved since the mid-1990’s. Marzluff et al. (2010), for example, was able to show that wild American crows (Corcus brachyrhynchos) were able to remember the faces of individual humans for at least three years, and that this information was able to be passed both from one individual to another and from one generation to another (Cornell et al. 2012). This study, if performed on captive birds, would not have enabled the researchers to make the ambitious claims of cognition and memory. Earlier, Marzluff et al. (1996) demonstrated through elegant field experiments that raven roosts act as information centres regarding the location of food. Each of these studies provides evidence, not only that these species are capable of communication and social learning, but also that these abilities are being utilised by these species in the wild to achieve adaptive goals.

The process of removing an animal from its natural environment can, as a consequence, have significant impacts upon its physiology and psychology (Calisi and Bentley 2009, Byrne and Bates 2011), creating the potential for differences between data obtained in captivity and that from the field. These differences can be extreme, subtle or non-existent, depending on the species in question.

Stress and welfare in captivity

"There is about as much educational benefit to be gained in studying dolphins in captivity as there would be studying mankind by only observing prisoners held in solitary confinement" - Jacques Cousteau (as cited in Dougherty 2013)

While captive animals may be of better physical health than their wild counterparts, their constrained and contrived surroundings can result in adverse psychological and behavioural effects (Calisi and Bentley 2009). Moving adult animals from a natural environment to captivity can have far-reaching impacts upon an organism’s psychology and physiology, predominantly through stress (Mason 2010). Changes in an animal’s social situation may

35 also change the level of testosterone in their system, with captive birds generally having lower testosterone levels than their wild counterparts, though this is far from universal (Calisi and Bentley 2009). Such changes in hormonal levels, thought to be initiated by changes to social stability (Wingfield et al. 1997), impact upon behavioural traits such as boldness and aggression and may have significant influences on observed behaviours (Mason 2010). Even changes from a natural to a captive diet can have significant impacts on behaviour (Calisi and Bentley 2009).

The field of animal welfare science has developed due to increased concern for and appreciation of the psychological capacity of non-human animals, and increasingly prevalent societal views that animals should be treated in a more humane fashion (Mason 2010). Controversies associated with the direct measurement of fear, distress, anxiety and pain in animals, have lead welfare scientists to seek more quantifiable indices to infer their psychological wellbeing (Mason 2010). These indices include (but are not limited to) hormonal and corticosteroid responses to stress, compromised growth, immunosuppression and stereotypic behaviour (Mason 2010, Wingfield et al. 1997) (Table 2.1). While some animals benefit physically from captivity, being protected from predators and provided with plentiful food, others, such as elephants and giraffes, experience shorter life spans; similar psychological impacts have also been documented in several other species (Bashaw et al. 2001, Clubb et al. 2008, Mason et al. 2009, Mason and Veasey 2010). Stereotypic behaviour, the act of performing the same behaviours repeatedly, can vary from excessive scratching, licking and pacing to acts that can result in physical harm to the animal and is considered an indicator of poor mental health (Mason 2010, Wingfield et al. 1997). Any changes to hormones or corticosteroids inevitably influence an animal’s behaviour (Adkins-Regan 2005), making stress in captive animals of particular interest not only from an animal welfare point of view but also regarding the impact it may have on subjects’ behaviour and performance during experimentation.

Holding animals in captivity inevitably has physiological and psychological impacts on an animal’s wellbeing, although the reaction may differ markedly between species (Mason 2010). Some workers hypothesise that there is a correlation between the ability to thrive in human proximity and ability to flourish in captivity (Mason 2010). While the myriad of studies involving captive corvids (See Chapter 3) and their synanthropy indicate that crows

36 should, at least theoretically, take well to captivity, prior research appears to indicate that phylogenic relationships are not good indicators of a species ability to cope with captivity (Mason 2010). Standard procedures for reducing stress include allowing animals to acclimatise to their captive surroundings (Archard and Braithwaite 2010), although the duration of time required and whether long term effects actually subside completely, varies between species (Mason 2010). Mason (2010) has stressed that even closely-related species can react very differently to captivity.

Keeping animals in captivity can induce both acute (Teixeira et al. 2007, Gregory et al. 1996, Omsjoe et al. 2009) and chronic stress levels (Dickens et al. 2009). Both types of stress can have significant and differing impacts upon the behaviour and psychological function of the animal (Wingfield et al. 1997). For example, Bradshaw (2011) cites symptoms of Complex Post-Traumatic Stress Disorder, a mental illness arising from being “held in a state of captivity, physically or emotionally” (Whealin and Slone 2001) in captive parrots that had been mistreated or neglected. Individuals suffering from Complex PTSD have sustained a prolonged period (months to years) of total control by another (Whealin and Slone 2001).

Bradshaw (2011) argues that behaviours displayed by captive parrots closely mirrors those shown by humans suffering from Complex PTSD, such as self-mutilation, pacing, insomnia and becoming aggressive when touched (Bradshaw et al. 2009). In fact, two umbrella cockatoos (Cacatua alba) in Bradshaw’s (2011) investigation were diagnosed with Complex PTSD, showing symptoms including an inability to socialise, fits of rage, aggression, low self- esteem, anxiety and depression (Bradshaw et al. 2009). While the conditions in which these two individuals lived were far worse than what would be permitted in scientific research, they provide an example of the impact that captivity can on the psychology of wild animals.

Differences in results between lab and field studies

Data from animal welfare studies have shown that captivity often impacts upon the animal’s behaviour and that this must be taken into consideration when using captive animals in behavioural and cognitive studies (Mason 2010). Differences in results between studies on captive and wild animals can be extreme, subtle or even non-existent, depending on factors such as the species in question, the behaviours tested and the housing conditions of captive animals (Calisi and Bentley 2009). An example of discrepancies in the results between wild

37 and captive animals are evident in studies of functional and intrinsic neophobia, the suite of behaviours that relate to ‘fear of new or unfamiliar object’ (Greenberg and Mettke- Hofmann 2001, Greenberg 2003). Intrinsic neophobia is the potential extent of these behaviours while functional neophobia is the actual expression of this trait and is influenced by the organism’s prior experiences (Greenberg 2003). An animal raised in a captive environment will have experienced a significantly smaller range of stimuli and items than one that has lived in the wild. Thus, one would expect levels of intrinsic neophobia to be similar between animals in captivity or in the wild, while expressed functional neophobia to be quite different. Experiments undertaken by Greenberg (1989, 1992), for example, comparing neophobia in swamp sparrows (Melospiza georgiana) and song sparrows (Melospiza melodia), produced contradictory results among wild and captive birds. Discrepancies in results between studies on captive and wild animals of the same species can be found in numerous taxa. Calisi and Bentley (2009) produced a detailed assessment of studies that have produced differing and even contradictory results. For both birds and mammals, these discrepancies vary from steroid levels to parameters as basic as whether the animal is diurnal or nocturnal. Wingfield et al. (1990) documented opposite effects of social instability on testosterone levels in wild and captive birds from several species. The effect of day-night cycles on Black-capped chickadee (Poecile atricallus) neurochemistry also appeared to differ between wild and captive animals (Smulders et al. 2006, MacDougall- Shackleton et al. 2003). The varying results between captive and wild subjects suggests that the act of keeping an animal in an enclosed environment has impacted upon the animal’s physiology or behaviour, producing results that are not representative of the animal’s wild state (Calisi and Bentley 2009).

Selectively breeding captive animals may, either intentionally or not, also have a significant impact on behaviour and therefore results from experimentation (Huntingford et al. 2006, MacDougall-Shackleton et al. 2003, Archard and Braithwaite 2010). As well as selective breeding, long-held captive animals are subject to a lack of diversity when choosing a mate, depriving the population of sexual selection that may be present in wild populations (Archard and Braithwaite 2010).

By focussing predominantly on studies of captive animals, the study of animal cognition runs the risk of ignoring or dismissing important environmental context and may even draw

38 erroneous conclusions. Holding animals in captivity can have a significant impact upon that animal’s psychological health, affecting its behaviour and potentially producing results that are not representative of its natural capacity. Therefore, there is a necessity for studies of wild individuals in their natural environment in the field of animal cognition to compliment and expand those of captive animals.

While there is obviously a place for studies of wild animals, these are by no means straightforward or simple to undertake. Logistical constraints exist for any study but apply particularly to wild studies. Data collection is significantly more time consuming than for laboratory studies, and the quality of the data can be significantly undermined by environmental, individual or temporal variation (Archard and Braithwaite 2010). Archard and Braithwaite (2010) note that the complexity of an organism’s natural environment, while being what makes wild studies of greater interest, also make these studies substantially more difficult to conduct. However, while notably less efficient than studies of captive animals in producing data, these studies provide a “reality check” to those that exclude their subjects from their natural stimuli and context. These studies, if conducted in an environment within which people live, can have the effect of peaking the interest of the public in the natural world around them. Nowhere does this apply more than in the world’s cities.

Native birds in urban environments

Urbanisation is a major factor in environmental change in the 21st century, with an estimated 5.9 million km² of land to become part of the global urban environment by 2030 (Millennium Ecosystem Millennium Ecosystem Assessment 2005, Seto et al. 2012, Secretariat of the Convention on Biological Secretariat of the Convention on Biological Diversity 2012). Urbanisation degrades habitats through a number of ways, including loss of habitat through clearing, increased impact of edge effects, invasive species and reduced connectivity between remaining habitats, as well as increased light and noise (McDonnell and Hahs 2015). This degradation creates new urban ecosystems, with their own properties and challenges for organisms attempting to inhabit them (Hobbs and Cramer 2008, Kowarik 2011).

39 While the predominant ecological commentary on urban sprawl focuses on the loss of biodiversity due to habitat loss (Marzluff et al. 2001), of equal interest are the species that remain and often flourish in urban environments (Catterall 2004, Bonier et al. 2007a). The species that flourish in urban environments are often invasive generalists, such as pigeons and rats (Warne et al. 2010). There is, however, an increasing appreciation that many native species have been remarkably successful in urban environments throughout the world (Marzluff 2014) including Australia (Jones 2003). The study of the adaptation organisms must undergo to thrive in this novel environment has become of significant interest in ecology circles (McDonnell and Hahs 2015).

If a native organism is to adapt and exist within an urban environment, some properties of that organism’s niche must be maintained in the urban environment for long enough for the organism to adapt to the new properties of the environment (McDonnell and Hahs 2015, Ashley et al. 2003). Organisms that naturally flourish on edge habitats and open forest with grassy groundcover are highly likely to persist in the urban environment, due to the strong resemblance of suburban yards and parks to these habitats (McDonnell and Hahs 2015).

Brisbane: Birds in a sub-tropical urban jungle

The city of Brisbane lies in the South-Eastern corner of the state of Queensland and is the third largest city in Australia and by far the largest city in the northern half of the continent, with a population of 2.45 million people (ABS 2015). The Greater Brisbane Region (Fig. 2.1) is one of the fastest-growing urban areas in Australia with a population increase by 1.7% (38,500 people) between 2013 and 2014 (ABS 2015). For much of the 2000’s, around 1000 people settled in the area each week (Ryan 2007). Brisbane has a wide variety of native fauna, ranging from water dragons (Intellagama lesueurii) and (Family: Cicadidae) to flying foxes (Pteropus spp) and carpet pythons (Morelia spilota) (Ryan 2007), with the Queensland Museum (Poole 1996) noting that a bird watcher is able to see more than 50 individual bird species within 15km of the Brisbane CBD on any given morning. Although, as is common in urban areas, this biodiversity is under threat, with 67,500ha of forest cleared over a period of 10 years in the 2000’s (Ryan 2007). It is predicted that within a few decades there will be continuous urban sprawl from Noosa to Murwillumbah to form a “200km city” (Spearritt 2009), an extraordinarily large area dominated by urban fauna and flora (Poole 1996). Continued deforestation to account for Brisbane’s growing population have put a

40 number of these species, such as the squirrel glider (Petaurus norfolcensis), spotted-tail (Dasyurus maculatus) and koala (Phascolarctos cinereus), at risk in an area in which they have been historically common (Ryan 2007).

Figure 2.1 Human population change in Queensland and Brisbane 2012-2013 by Statistical Area 2 (insert) (ABS 2015). The urbanisation of South East Queensland has converted large forested areas into suburbia.

A number of national parks were declared around the Greater Brisbane area in the early 1900’s, predominantly in the Gold Coast and Sunshine Coast hinterlands (Poole 1996). Brisbane ticks many of the boxes for high biodiversity as proposed in the literature: being young, subtropical and sprawling, it contains a wide variety of habitats and resources, contains a strong link to the coastline, and is surrounded by large areas of remnant vegetation (McDonnell and Hahs 2015, Poole 1996, Sewell and Catterall 1998, Catterall 2004, Catterall et al. 2010). These rainforests of South East Queensland are of national significance, hosting a vast diversity of flora and fauna, including Gondwanian remnants such as the Antarctic Beech (Lophozonia moorei) (Poole 1996). Brisbane itself is home to a number of dry forests, with shrubby understories dominated by grass trees (Xanthorrhoea johnsonii), banksias (Banksia spp) and wattles (Acacia spp), under a eucalypt

41 canopy (Poole 1996). As the population has grown, many bushland areas have been converted into urban sprawl, producing large areas of suburban lawns interspersed with trees (Sewell and Catterall 1998).

Lawn is popular in suburban environments worldwide due to their aesthetic (Uhl 1998) and durability (Adams 1994). This expansive resource also supports many species of arthropods and worms that inhabit the soil just beneath the surface (Falk 1976). Brisbane’s lawns, excepting times of drought, are generally well-watered, allowing these invertebrate populations to increase far beyond what would naturally occur in native bushland (Gerard 1967, Edwards and Bohlen 1996, Falk 1976, Heppner 1965, Rollinson et al. 2003), creating a food supply that can support unnaturally large bird populations (O'Leary 2002, Jones 2002). For avian species that forage on the ground for invertebrate prey, a suburban environment hosting significant expanses of well-watered grass can dramatically increase food availability and, therefore, abundance (Jones 2002, O'Leary 2002).

Crows in Brisbane: growth and conflict Brisbane, like many cities worldwide, has seen an explosion in the urban densities of corvids over the past few decades (Marzluff et al. 2001, Sinden 2002, Woodall 2004). Once considered rare and extremely difficult to locate in South East Queensland (Jack 1938), Torresian crows are now one of the most common bird species in Brisbane (Sinden 2002, Woodall 2004) and are spread widely over the northern half of the Australian continent. Torresian crows populations in Brisbane have increased significantly between 1980 and 2000 (Woodall 2004), which Sinden (2002) suggests is due to the abundance of invertebrate food.

The rapidly increasing crow population has led to an escalation in conflicts between the birds and human residents (Jones and Everding 1993, Sinden 2002). A significant minority of people in urban areas are disturbed by crow roosts, mostly due to their excessive noise in the early morning (Jones and Everding 1993). Despite this, surveys have shown the majority of people in Brisbane either like or are indifferent to crows and that the vast majority do not want them to be harmed (Everding and Jones 2006). This conflict is accentuated by crows’ preference to roost in trees located close to suburban homes, making the issue of excessive crow noise a constant problem for residents (Jones and Everding 1993, Sinden 2002).

42 Notably, only Torresian crows in Brisbane and little ravens in are known to form large-scale communal roosts in urban areas in Australia (Whisson et al. 2015, Ekanayake et al. 2016 D. Jones pers. comm.). These roosts, located throughout Brisbane, are comprised of adult and juvenile crows from surrounding territories. While information travels quickly within crow populations, there appears to be very little movement between populations; as members of juvenile gangs may move between roosts, while mated adults appear to be relatively sedentary to their territories (Everding 1995; M. Brown pers. obs.; D. Jones pers. comm.). This suggests that there is likely to be a lag in information from the population in one area reaching another.

Non-corvid study species

The Family Cracticidae consists of 12 species of bird in Australia, separated into two Genera: Cracticus and Septera. These birds are diurnal generalists with a black and white, and sometimes grey, plumage (Kaplan 2004). This thesis investigates primarily four of these species: the pied currawong (Septera graculina), pied butcherbird (Cracticus nigrogularis), (Cracticus torquatus) and Australian magpie. Additionally, several non- corvoid species that also inhabit the suburbs of Brisbane were included in an investigation into Mirror-Image Stimulation (MIS). The Encephalisation Quotients for all native study species have been provided in Appendix I.

43 Table 2.1 Summary of study species (Marchant and Higgins 1993, Higgins and Davies 1996, Higgins et al. 2006b, a, Jones 1990a, 1990b, 1992, 2003, 1999, Jones and Everding 1991, Everding 1995, Jones and Thomas 1999, Sinden 2002, O'Leary and Jones 2002, Johnson 2003, Warne and Jones 2003, Goth and Jones 2003, Rollinson et al. 2003, Jones and Nealson 2003, Everding and Jones 2006, Jones and Goth 2008, Warne et al. 2010, Pizzey and Knight 2012, Cousins and Jones 2013, Brown 2016). Images retrieved from Birdlife Australia (2017). For more information, see Appendix III.

Species Size Habitat Food Behaviour Torresian crow 53cm, Edge of eucalypt forests and Primarily granivorous, Exist in social groups while (Corvus orru) 550g grasslands, extremely common also eats invertebrates, young, sedentary pairs during in cities. carrion, fledglings and adulthood. Territorial and will anthropogenic foods. defend against conspecifics.

Australian 44cm, Variety of habitats: dry open Forage exclusively on the Territorial, can live in pairs or in magpie 350g forests, grasslands, residential ground, feed on large flocks. Highly aggressive, (Cracticus areas, shrublands and invertebrates, fledglings will attack heterospecifics while tibicen) occasionally in wet closed and other birds. foraging and passing humans forests during breeding season.

Grey 24cm, Forest margins, parks and Generalist. Easts birds, Can be found alone, in pairs or butcherbird 100g gardens. lizards and , also small family groups. No (Cracticus fruit and seeds. Can hunt cooperative breeding. torquatus) on ground but also kill birds in flight.

44 Species Size Habitat Food Behaviour Pied 36cm, Dry woodlands, farmlands, Small reptiles, mammals, Often in large groups of 3-4 butcherbird 120g urban parks and gardens. frogs and birds, also large adults with additional young. (Cracticus insects. Partake in cooperative breeding. nigrogularis)

Pied 50cm, Found in forests and Small lizards, insects, Highly social, found in large currawong 290g woodlands, common in berries, small fledglings groups during winter. Becoming (Strepera forested suburban areas. and mammals. more permanent in Brisbane. graculina)

Magpie-lark 30cm, Open grasslands and eucalypt Insectivorous. Prey on Sedentary, usually found in (Gralina 85g forests, built up areas. food in canopies or in the pairs. Aggressively territorial. cyanoleuca) Sedentary in most of Northern air. Australia

45 Species Size Habitat Food Behaviour Australian 70cm, Common in rainforests and dry Insects, seeds and fruit. Males defend mounds of dirt brush-turkey 2300g sclerophyll forests. Very Predominantly feed on and debris for incubation. (Alectura common in East coast cities. food under leaf litter lathami) exposed after raking.

Crested pigeon 34cm, Found throughout Australian Feeds on seed, Unusually aggressive, will kill (Ocyphaps 270g continent. Common in pastoral predominantly native other birds on sight. lophotes) lands, paddocks, sports seeds but also grounds and urban areas. introduced crops.

Spotted dove 32cm, Invasive, native to South and Seeds and waste food. Poorly-known (Spilopelia 160g South-East Asia. Rarely found chinensis) away from developed landscapes.

Common myna 24cm Invasive, native to Indian Generalist scavengers. Social, compete with native (cridotheres 110g Subcontinent. Synanthropic, noisy miner for territory. tristis) flourishes in urban areas. Complex song.

46 Study Sites

The study sites used in this project varied between the different experiments conducted. During the study of neophobia, there was no familiarisation or training process and the experimentation time did not exceed 15 minutes. This was in contrast to the other experiments where this process often took several weeks or months. Therefore, sites for the neophobia experiment (Fig. 2.7) were numerous, short-term and ad hoc while the others were undertaken at seven permanent sites throughout Brisbane’s southern suburbs (Fig. 2.8). Attempts were also made to gather data at ten additional permanent sites but these were abandoned due to a number of reasons including crows not interacting with the apparatus, ceasing interactions partway through the experiment and displacement and exclusion by other species.

Figure 2.2 Locations where neophobia experimentation was conducted on Torresian crows (Red), Australian magpies (Purple), grey butcherbirds (Blue) and pied currawongs (Green).

47

Figure 2.3 Map of eight experimental sites used in this project. Sites F and G were used for MIS (Yellow), E and D for MIS and Learning (Green), B for Learning and String Discrimination (Purple), and A and C for all three (Red).

Birds were studied at a total of eight sites within the suburbs of Brisbane (Table 2.4), dependent on accessibility to private land to minimise the risk of theft or interference of apparatus. Three of these were located in suburbs surrounding the Mount Gravatt Central district, with the final site in the bayside suburb of Manly West, 30km to the North-East. All suburbs were low-density residential area with readily-available trees and lawn.

The remaining sites were located throughout Griffith University’s Nathan Campus (Table 2.4), situated within Toohey Forest Park (Wallace and Catterall 1987). While crows are less common within the forest itself, around the campus, with its plentiful lawns, cafes, bins and general food waste, the population has become relatively large, inhabiting the area year- round. Unlike most areas with high densities of crows such as shopping centres, school ground and other university campuses, the Nathan Campus crow population appears to consist almost entirely of territorial adult pairs, instead of the more common flocks of juveniles (M. Brown, pers. obs.). From extensive observations of behaviour of banded and

48 unbanded crows, this area was found to support many small and aggressively defended crow territories, some measuring only 50m across (M. Brown pers. obs).

Table 2.2 Location and description of sites throughout southern suburban Brisbane.

NAME LOCATION DESCRIPTION SITE A Nathan Campus • Limited fragmented grassed area • Plentiful eucalypt trees • Many buildings SITE B Coopers Plains • Fragmented grassed areas • Available eucalypt trees • Many buildings SITE C Manly West • Fragmented grassed areas • Small invasive trees • Many buildings SITE D Eight Mile Plains • Extensive grassed area • Available eucalypt trees • Few buildings SITE E Nathan Campus • Limited fragmented grassed area • Plentiful eucalypt trees • Many buildings SITE F Nathan Campus • Plentiful grassed area • Plentiful eucalypt trees • Few buildings SITE G Holland Park West • Limited fragmented grassed area • Available eucalypt trees • Many buildings SITE H Nathan Campus • No available grassed area • Plentiful eucalypt trees • Few buildings

49 Studies on corvid cognition: a review

Introduction

Advantages and drawbacks of laboratory studies

The field of animal cognition and behaviour has historically been dominated by studies of captive animals, either raised in captivity or caught in the wild (Byrne and Bates 2011). These studies are advantageous as they allow researchers to eliminate environmental factors to clear away the ‘noise’, allowing the distinct signal to be more easily recognised (Calisi and Bentley 2009). These studies can also allow the researcher to compel the subject animal to partake in the study, allowing them to accumulate a sufficiently large dataset of this clean data in a relatively short amount of time (Byrne and Bates 2011). However, such studies often do not take into account the environmental context in which an animal has evolved, and animals removed from this environment and placed in captivity can experience substantial changes in behaviour due to immediate and chronic stress (Calisi and Bentley 2009, Mason 2010).

The extent of this stress varies significantly between species and can be influenced by the captive environment of the animal and its treatment by its keepers (Mason 2010). Animals kept in low quality environments have been found to show signs of Complex Post-Traumatic Stress Disorder (Bradshaw et al. 2009) and chronic stress can be detected by observing a number of behaviours including but not limited to compromised growth, immunosuppression and stereotypic behaviour (Mason 2010). These changes in behaviour have been shown to alter the results of studies of animal behaviour, in some cases even producing contradictory conclusions to what is observed by the same species in the wild.

Studies of animal cognition are often conducted in captive environments, due to the necessity to test and re-test individuals over time to assess learning ability, memory and other factors. The study of animal minds has been greatly progressed by studies of captive primates in zoos and laboratories. One group that has become synonymous with animal cognition is the corvids, the crows, ravens and jays.

50 Corvids

Corvids (Family: Corvidae) are a group of some 120 species of generalist passerine birds that are found on every continent bar Antarctica and include the crows and ravens (Genus: Corvus), jays and true magpies (Goodwin 1976, Madge and Burn 1999, Angell and Marzluff 2005). Corvids are highly encephalised (Emery 2006) and commonly display behaviours consistent with high intelligence, such as self-recognition (Kusayama et al. 2000, Prior et al. 2008, Medina et al. 2011), tool-use (Montevecchi 1978, Hunt 2000b, a, Caffrey 2000, 2001, Weir et al. 2002, Bluff et al. 2007, Balda 2007, Bird and Emery 2009a, Wimpenny et al. 2009, Mehlhorn et al. 2010), social learning (Templeton et al. 1999b, Holzhaider et al. 2010), cultural evolution (Marzluff and Angell 2005, Marzluff et al. 2010), imagination (Heinrich 1995a, Bird and Emery 2009a), cooperation (Bossema and Benus 1985, Seed et al. 2008) and memory (Kamil and Balda 1990, Balda and Kamil 2002, Clayton et al. 2007, Marzluff et al. 2010). This, combined with the evolutionary independence of the avian brain from the mammalian brain, has resulted in considerable interest in corvid cognition from both researchers and the general public (Angell and Marzluff 2005, Marzluff and Angell 2013).

Corvids have become the flagship taxa for avian cognition. Until recently thought to be organisms of almost pure instinct, birds are now subject to a healthy and ever-growing catalogue of studies regarding learning and higher cognition. This field has extended to parrots (Wood 1984, Auersperg et al. 2012, Pepperberg et al. 1995), starlings (Marcus 2006) and even pigeons (Cook et al. 1997). For such an important group as corvids, it is worthwhile investigating the properties of the studies that make up this collection. This can be used to inform future studies of which areas to target in order to most effectively complement the existing literature.

This review therefore aims to assess the current state of the literature on corvid cognition, ranging from the contributions made by various species, institutions and what proportion of these studies are based on wild species.

Methods

In order to discern the features associated with research in this field, a review was conducted on the literature of corvid cognition. Published literature was discovered through use of Google Scholar and Web of Science using key words commonly found in cognitive

51 works. These terms included but were not restricted to “corvus, corvid, jay, crow, raven, problem solving, cognition, cognitive, string, memory, tool, learning and behaviour”. Websites of known authors were also used in order to attain a large number of studies efficiently. Reference lists were then checked which, in addition to use of the “cited in” feature of Google Scholar, allowed relevant papers both before and after its publication date to be added to the dataset. This process was then repeated several times until no new studies were discovered.

A total of 149 individual peer-reviewed papers on 16 corvid species were catalogued and examined for their experimental methods and sample size (Appendix II). Literature reviews and field observations were excluded so that the dataset consisted entirely of experimental studies, cutting the sample size to 114 publications in total. Only papers investigating cognition through behavioural experimentation were included, thus excluding assessments of neuroanatomy, population distribution, general behaviour or pathology. Studies were categorised by whether they used wild, captive wild, or hand-reared birds and the species that the study investigated. If an individual study included experiments on more than one species, or both wild and captive birds, the experiment on each species or state was counted individually. The number of individuals used in each study was also noted, as a way to determine the most common sample sizes in the field. Finally, in order to assess broader patterns in the literature, the institution with which the researchers were associated was recorded. If authors from more than one university were involved in the study, the university where the experimentation took place was noted.

52 Results

A total of 83% of all 114 studies examined were conducted on corvids held in captivity, with the majority being hand-reared birds that had had no experience of their natural environment (Fig. 3.1). Approximately three quarters of wild studies were either conducted exclusively on banded birds or included banded birds. Many of these were part of a long- term study of a particular population, such as the common raven (Corvus corax) population at the Konrad Lorenz Research Station in Austria or the American crow (Corvus brachyrhynchos) population at the University of Washington Seattle campus in the United States. The previous work of these research groups meant that the subject birds did not have to be banded as part of each individual experiment, reducing the work required for each individual investigation. Additionally, there were several instances of captive birds being used for several experiments during their time in captivity, whether that be years in the case of Kamil and Balda’s prolonged studies of pinyon jays (Gymnorhinus cyanocephalus) or just a few months in the case of the University of Auckland’s New Caledonian crow (Corvus moneduloides) population.

Captive

Wild

0 20 40 60 80 100 120

Banded for identification Not banded Hatched and reared in captivity Wild-caugght and tested in captivity

Figure 3.1 Captive status of subject birds used in published studies on cognition in corvids. Many subjects had not experienced life outside captivity at the time of experimentation.

53 The literature was also dominated by three species: the common raven, New Caledonian crow (both Corvus spp), and the Clark’s (Nucifraga columbiana) (Fig. 3.2). These three species made up more than 50% of all studies. With the exception of the New Caledonian crow and the jungle crow (Corvus macrorhynchos), all of the species reviewed were Holarctic birds: seven from North America and five from Eurasia. Studies on New Caledonian crows were, unsurprisingly, dominated by investigations into the animal’s use of tools while studies on caching and memory made up the majority of studies on jays and nutcrackers. Wild studies tended to be conducted on American crows, common ravens and to a lesser extent New Caledonian crows and blue jays ( cristata).

30

25

20

15

10

5 Frequency in literature in Frequency 0

Species

Hatched and reared in captivity Wild-caugght and tested in captivity Wild and banded for identification Wild and unbanded

Figure 3.2 Number of cognition papers published for each species of corvid. Almost all the information available on all but three species is derived from captive animals, and subsequently may be lacking context.

54 Small sample sizes were unsurprisingly common, with a large proportion of studies only utilising four animals, and a majority using fewer than eight (Fig. 3.3). Wild studies were over-represented in the large sample size studies, including 100% of those with more than 100 individuals and approximately one third of those with 50 to 100. These publications tended to focus on roosting, foraging, facial recognition and caching.

>200 101-200 51-100 26-50 25 24 23 22 21 20 19 18 17 16 15 14 13

Frequency in literature in Frequency 12 11 10 9 8 7 6 5 4 3 2 1

0 5 10 15 20 25 # of individuals in study

Hatched and reared in captivity Wild-caugght and tested in captivity Wild and banded for identification Wild and unbanded

Figure 3.3 Sample sizes in the reviewed literature of corvid cognition are commonly small. Additionally, many studies produced by research groups tend to either test the same individuals for multiple studies, or use their previous subjects’ offspring in new papers.

55 The field of corvid cognition was found to be dominated by a small number of research teams, which have contributed the majority of publications found in the literature (Fig. 3.4). Of the six most frequently noted institutions, two are in the United States, two in the United Kingdom, one in Austria and one in New Zealand, though the latter’s research is predominantly conducted at field stations in New Caledonia.

25

20

15

10 Frequency in Literature in Frequency 5

0

Institution

Hatched and reared in captivity Wild-caugght and tested in captivity Wild and banded for identification Wild and unbanded

Figure 3.4 Contribution of research institutions to the literature on corvid cognition. The information pertaining to this clade has been constructed by a small number of individuals.

56 The frequency of publications on corvid cognition has increased markedly over the past twenty years, with 2006 marking a high point after which the frequency of publication has remained relatively stable (Fig. 3.5). The field appeared to become more mainstream in the mid-1990’s, with publications before that time being sparse.

12

10

8

6

4 Frequency in literature in Frequency 2

0

Year published

Hatched and reared in captivity Wild-caugght and tested in captivity Wild and banded for identification Wild and unbanded

Figure 3.5 Historical trends the publishing of studies on corvid cognition, showing a significant increase in papers published from the mid-1990’s. Discussion

Calisi and Bentley (2009) state that the majority of work on vertebrates has been conducted on captive animals and this appears to be the case in the field of corvid cognition. Most of the knowledge in this field has been derived from individuals in a captive environment. Most of which were raised in captivity and would not have life experiences representative of those encountered by wild individuals.

Of 120 species of corvid, only 16 were found to have had their cognition investigated scientifically and only three have been subject to more than ten studies over 45 years. While there are undoubtedly some papers that were not found during research, the number of publications involving additional species would likely be minimal. This small number was dominated by studies of the common raven and the New Caledonian crow, as well as a small number of jay species. The seven Corvus species found in the dataset represent six of the

57 eight described in (Jønsson et al. 2016), representing a good coverage of the genus. Jønsson et al. (2016) also described a single large clade of species from Australia, the Sundas and Pacific Islands. Of these, only the New Caledonian crow has been studied (Fig. 2.6).

In corvid cognition, as is likely the case for many scientific fields, both the institutions producing research and the species they are studying are heavily biased towards the Holarctic realm, particularly the United States and United Kingdom. The University of Auckland is the only institution responsible for a significant number of the publications noted that resides outside North America or Europe, and the New Caledonian crow is the only non-Holarctic species subject to more than five publications in the reviewed literature. Keio University’s publications on jungle crows provide information on a species that inhabits other realms, but only two studies have been noted in this review.

The frequency of papers published on corvid cognition experienced a significant rise in the late 1990’s and early 2000’s. At first glance, a possible explanation for this increase is the discovery of tool use in New Caledonian crows in the late 1990s (Hunt 2000a, b), which resulted in a series of investigations into a species that was, until then, unstudied. This species has now become the second most-studied corvid with 25 papers noted in this survey. Nonetheless, the publications during this period are by no means dominated by this species but instead include a large number of studies on caching and rule-learning in jays and Clark’s nutcrackers by researchers from the University of Nebraska and University of Cambridge. The dominance of the New Caledonian crow is a much more recent phenomenon, undoubtedly due to the establishment of research stations in the mid-2000’s on Mare Island and in Farino in 2012 by the University of Auckland (2016). This relatively recent discovery of complex behaviours in a species that has since contributed so much to our understanding of animal intelligence makes a strong case for further investigation into species that have not as of yet been thoroughly studied.

While this review has been substantial, it is by no means exhaustive and bias may have been introduced through the method of review. Those studies that published in non-English language journals would be less likely to be detected, and would likely have only been identified if their title contained Latin word “Corvus”, or if they had been cited by or had cited a publication that had already been noted. This bias is by no means restricted to this study, as language barriers reduce detectability in most scientific fields, a reality caused by

58 the adoption of the English language by a large number of international journals. The dominance of institutions from the United States and United Kingdom may also have been exaggerated by this effect.

Additionally, publications were found online through electronic methods. Publications that were produced before the introduction of the internet and had not been digitised would not be found through the majority of the methods used here. This may explain, to some extent, the relative absence of papers produced before 1995. However, if this absence was entirely due to the influence of the internet, these studies should have been detected in the reference lists of those papers that were surveyed. As this was not the case, the change in frequency of publications before and after 1995 may be attributed to changes in the scientific community, rather than a weakness in the reviewing methodology. Alternatively, part of this increase may have been influenced by the inclusion of non-ISI publications in the Web of Science, though this would be difficult to confirm.

There are definite advantages to conducting experiments in controlled environments on captive individuals. While in captivity, the individuals may be compelled to partake in the study, environmental factors could be controlled and individuals could be kept track of. Potential for discernible intelligence is not always expressed, as organisms subject to environmental factors can be influenced behaviourally. Motivation can increase an organism’s apparent intelligence, while stress or chronic fear can reduce it (Kaplan 2015). Birds in the wild have less motivation to interact with any apparatus laid out as they can obtain food elsewhere, while the presence of heterospecifics or fledglings can increase stress. Include neophobic fear of the apparatus and of humans and there is the potential for intelligence to not be fully expressed. Nonetheless, this over-reliance on captive studies is a weakness in the literature that could be addressed by further research in the field. While the knowledge accumulated is impressive and has greatly furthered our understanding of these birds in a short period of time, some balance is surely required.

59 Conducting field experiments on wild Torresian crows: Advantages and challenges

Introduction

Thus far, this thesis has provided a comprehensive summary of the current state of the literature on learning behaviours in corvid birds. This literature, while extensive, is significantly biased towards only a small subset of the Corvidae family and is dominated by studies of captive individuals, whether they be captured or raised in captivity (See Chapter 3). By relying on captive individuals to understand the group, the field runs the risk of ignoring significant context, both environmental and social, and potentially making incorrect or incomplete conclusions (Reviewed in Calisi and Bentley 2009). Such studies should be complimented by an array of investigations into cognitive traits of birds in their natural environment, with the experiences of having lived in a complex natural environment. However, this context comes at a cost; wild studies may be influenced by environmental factors that cannot be accounted for, fail to recognise signals that would be clearer in clean data from a controlled environment, or simply be more difficult to conduct due to the inability to control or individually identify the subjects. This chapter documents the process of studying wild Australian crows and other birds in the suburban environment of the subtropical city of Brisbane, Australia. Many approaches and field techniques were attempted but did not have the desired result, requiring new techniques to be formulated in response to challenges that arose during the study. The methods used and discussed in Chapters 5, 6, 7 and 8 of this thesis evolved over time through thorough experimentation in the field. It is intended that this paper assist in future research by describing how successful various techniques were when utilised in a suburban environment.

On trapping, banding and keeping wild crows

Targeting wild adults

In line with a number of similar studies (Auersperg et al. 2011, Bogale et al. 2011, Bogale and Sugita 2014, Chappell and Kacelnik 2004, Izawa and Watanabe 2008, Jelbert et al. 2014, Medina et al. 2011, Taylor et al. 2010b), the possibility of capturing wild crows, either adult

60 or juvenile, and holding them in captivity was carefully investigated. The crows were to be housed in a large aviary at Griffith University’s Nathan Campus, which had previously been used for a variety of avian species in behaviours studies. After consultation with BIRO (Birds Injured, Rehabilitated and Orphaned), a local bird rehabilitation organisation, the aviary was deemed not to be suitable for housing crows due to a variety of factors including exposure to the sun and lack of access to unroofed areas. Furthermore, advice from a series of authorities with experience of keeping wild-caught Australian crows (D. Jones pers. comm.) suggested strongly that these birds tend not to settle well, even after extended periods, and would therefore be unlikely to act as useful subjects in behavioural experiments. Torresian crow territories can measure up to several hundred metres across and crows can fly at a speed of up to 60km/hr (Rowley 1973a). Any kind of captivity would likely have significantly impacted upon the crows psychologically, potentially yielding results unrepresentative of what would be attained in studies conducted upon wild birds (Calisi and Bentley 2009).

Case study: Notes on keeping a captive adult Australian raven Corvus coronoides

During the early 1970s, an Australian raven was found by a local farmer trapped in a chicken house near Wagga Wagga, NSW and subsequently held captive for observations by D Jones (unpubl. data). The size and eye colour indicated that the bird was a fully- grown adult, though the bird’s age was not certain. The bird was kept alone in moderately large (4m x 2m x 5m) aviary and fed twice daily on beef mince, wet dog food and periodically supplemented with dead mice and chicken chicks.

Significantly, although kept for almost two years, and with daily gentle contact – including long periods of the observer sitting quietly beside the enclosure with food, the bird did not become in anyway calm or quiet. It never came to the ground to feed if anyone was present anywhere in the house or yard, and always flapped alarmingly when anyone entered the enclosure.

Despite concerted attempts to gain its confidents, this never eventuated and the bird was eventually released.

61 While it is difficult to predict how any individual animal will react to captivity based on the responses to closely-related species, the problems encountered by D. Jones (unpubl. data), along with the other issues raised by students of animal welfare science (Mason 2010, Calisi and Bentley 2009) raise concerns regarding holding Torresian crows in captivity.

Therefore, the decision was made to concentrate entirely on wild crows. Studies would be based on observations of either entirely undisturbed, free-living birds or preferably on individually marked birds. This necessitated the catching and banding of adult Torresian crows. Territorial mated pairs were targeted as their home ranges are relatively stable (M. Brown pers. obs.) and, excepting easily-identifiable fledglings, typically only two individual adult crows are ever present in each territory (M. Brown pers. obs.; Rowley 1973a). These territories were aggressively defended against conspecifics, and territorial borders may be inferred by observing bouts and conflicts between neighbours (M. Brown pers. obs.). This territoriality allowed researchers to correctly identify both individuals with the need to capture and tag only one of the pair, thus minimising disturbance. Captured birds were banded with a coloured band on the left leg and metal identification band on the right as advised by Lowe (1989). The capture of Torresian crows was attempted using a number of devices with mixed success.

All capture and handling protocols were approved by the Griffith University Animal Ethics Committee (aec/16/12/env).

Stationary funnel trap

Previous attempts at capturing crows in Brisbane had been conducted by Everding (1995) using a funnel trap. The trap was approximately 2m x 1.5m x 1.2m with a small mesh funnel facing inwards on one end and another facing outwards on the other. The method requires weeks of baiting with mince to encourage crows to enter the trap and allowing them to leave through the outward-facing funnel. On the day of capture, the exit was closed and crows entering were unable to escape. In 1995, this method caught 46 crows following prolonged baiting near a large roost (Everding 1995). After the successful catch, all subsequent attempts at this location failed to attract any crows, most probably due to the local population learning to avoid the trap (Everding 1995).

62 For the present study, this trap was utilised at the same location 19 years later for a period in excess of two months, with the trap being baited and checked daily. Unfortunately, this was not successful as crows did not engage with the trap. This may have been due to changes in crow densities in the area, though crows were regularly sighted in the area, an aversion of the resident crows to large novel objects or even, unlikely, memories in the local crow population of the trap.

Ladder entrance trap

A second attempt at trapping was made using a Ladder Entrance Trap, used predominantly for hunters to catch crows (Bub 1991). The Ladder Entrance Trap, also known as the Australian Crow Trap (Johnson 1994) or Norwegian Large-scale crow trap (Tsachalidis et al. 2006), is a commonly-used device to capture crows in areas where they are abundant (Tsachalidis et al. 2006) and has been used to reduce pest bird numbers in California’s wine region for decades (Gadd 1996) and were successfully implemented to catch little ravens in Australia (Shannon et al. 2014). Tsachalidis et al. (2006) attempted to use the ladder entrance to trap hooded crows (Corvus cornix) and Eurasian magpies in an agricultural area of Greece, due to their perception as an agricultural pest.

This trap was constructed for use in the present study. It was 2m x 1.5m x 1.5m in size, and contained a ladder on the roof, through which birds could drop down but were unable to exit the trap (Figs. 4.1 & 4.2). The trap was placed in two locations at the edge of a dry sclerophyll forest and a built-up area, areas inhabited by a pair of sedentary adult crows. During a period of familiarisation, the roof of the trap was entirely removed to allow birds to enter and exit unimpeded. This was followed by a trapping period of one month. The ladder trap was again unsuccessful. A single crow was caught accidentally when the roof was attached but with the ladder rungs removed. This bird, showing distress, was released by a concerned member of the public. This may be considered to be a design flaw, as crows should have been able to enter and exit the trap in a form very similar to that of the set trap, namely the roof being attached, to maximise the chance of trapping. Camera traps set on the cage wall confirmed that a variety of species including Australian brush-turkeys, butcherbirds, laughing kookaburras and pied currawongs regularly entered the unset trap, with very occasional visits from crows. In spite of this, the fully constructed trap was only ever entered by grey butcherbirds, which were small enough to easily enter and leave the

63 trap via the ladder roof. No crows were detected entering the set trap and none were captured. The trap was tested in two separate locations with similar success.

Figure 4.1 Australian crow trap (Johnson 1994).

64

Figure 4.2 Ladder trap constructed at Griffith University as per the instructions in Rowley (1968). This trap was deployed for a number of weeks without success.

The ladder entrance trap’s success appears to depend on construction, location, the time of year and bait (Moran 1991, Tsachalidis et al. 2006, Johnson 1994) and is most effective in areas where crows gather in large numbers (Tsachalidis et al. 2006, Johnson 1994, Shannon et al. 2014). This situation is quite different to the territorial pairs that were targeted in this study, as the likelihood of catching any crows increases drastically with a larger number of birds in the vicinity (Johnson 1994). In a large group of crows there are not only likely to be bold individuals but also juveniles, which have been shown to be far more neophillic than adults and far less wary of novel or anthropogenic objects (Heinrich 1995b). When there are only two birds in the entire area, the probability of either of them entering a large conspicuous trap drops, the length of time devoted to familiarisation and trapping sharply increases and the potential benefit of trapping (the number of crows likely to be caught) is much lower, making large-scale traps such as the ladder entrance tap and stationary funnel trap unsuitable.

65 Bal-chatri trap

After several months of failed trapping, it was determined that the size of the ladder entrance trap and funnel trap, and the long familiarisation processes required for these traps, was the predominant factor causing failure in catching crows in a sedentary territorial environment. In an attempt to capture birds of prey, Berger and Mueller (1959), after experimenting with trapping techniques for almost a decade, concluded that the Bal-Chatri trap was the most effective method. A significantly smaller (80cm x 80cm x 20cm) bal-chatri trap design was therefore appropriated as an alternative method for catching crows. This trap consists of a flat metal mesh cage upon the upper surface of which a large number of hand-knotted fishing line snares are tied. A live bait, typically a mouse, is placed in the cage to attract raptors. When the birds land talons-first, their legs enter the snares, which tighten and trap the bird as it attempts to fly away (Berger and Mueller 1959).

In the execution of this trap for the present study, a bird carcass was placed on top of the trap instead of the live bait commonly used for raptors. During several days of trialling the crows reacted extremely cautiously to the trap. A single crow was trapped once but escaped when the knot on the fishing line became detached. While from that point onwards the trap was largely ignored, it remained the most successful of the three designs attempted. The biggest weakness of the trap appeared to be its conspicuousness, which was addressed with design changes.

“Noose carpet” trap

In order to solve the problem of reliably trapping crows, a new trap was designed in an attempt to minimise the neophobic reaction of the birds to the trap and to maximise the chance that crows would continue to approach it, even if they had been trapped before or seen another bird trapped. The solution was to create a modified bal-chatri trap using a flat metal grate that would effectively merge with the ground layer of grass and leaf litter (Figs. 4.3 & 4.4). The grate was spray painted black and forest green for extra camouflage and nooses of fishing line (>0.5mm thick to avoid any harm to the birds’ legs) were tied directly onto the grate, in a design similar to the “noose carpet” trap described in Bub (1991). The trap was used throughout the Griffith University’s Nathan Campus in areas with either grass or leaf litter, with approximately 250g of beef mince placed in the middle of the trap. Crows,

66 landing next to the trap, would walk onto it to attain the mince and be snared by the loops attached to the grate. The grate was not secured to the ground as it was heavy enough to prevent crows from flying off. Researchers observed from less than 20m away from the trap, often hiding inside or behind buildings as crows would not generally approach a trap with humans nearby. Once crows were caught, they were quickly restrained and placed in a cloth sack before measurements of beak, foot and body length were taken.

Figure 4.3 Noose carpet trap visible on concrete.

Figure 4.4 Noose carpet trap camouflaged in natural surface.

67 This design proved to be by far the most effective trap design employed, eventually catching five crows over the period of two months. Several more crows were caught but escaped before they were able to be handled by researchers. Any currawongs, magpies, butcherbirds and kookaburras that were inadvertently caught with the trap were quickly released by researchers. If a crow witnessed another species being trapped, they were extremely reluctant to approach the trap for a number of days.

Behaviour of banded crows

Of the five crows captured and banded, three remained in their territories for the duration of the study. One pair’s territory shifted substantially (~300m) and one disappeared altogether (Fig. 4.5), possibly due to predation of one or both birds. Regardless, all five pairs, including the individuals not handled, became significantly more wary of any experimental apparatus after being caught. This wariness was evident to such an extent that only one individual of the five was able to be used in subsequent studies, and all were exceptionally cautious of both the researcher and any apparatus. Dozens of attempts over several weeks proved fruitless as the banded crow and its mate would either flee at the sight of the researcher or follow at a distance, rarely if ever interacting with any novel apparatus placed in their territory. This wariness prevented bands from being used for their intended purpose of distinguishing between individuals. In order to account for this scenario, pseudoreplication was prevented by treating pairs as subjects, and sites were instead placed in geographically separate crow territories.

68

Figure 4.5 Crow E, caught at Griffith University with the noose carpet trap. Familiarisation and training

Crows are broadly recognised as being a highly-neophobic group (Greenberg 2003, Greenberg and Mettke-Hofmann 2001, Kijne and Kotrschal 2002), meaning that they will often react with fear or wariness to an object that they have not yet encountered previously. By definition, apparatus for testing aspects of an animal’s cognition, whether it be the puzzle box (Auersperg et al. 2011), Aesop’s fable device (Jelbert et al. 2014) or a mirror test (Medina et al. 2011), all involve exhibiting novel stimuli. Due to the neophobic nature of crows, any apparatus that is introduced into the environment is likely to be met with a fearful reaction. It may take days to months for crows to sufficiently explore experimental apparatus to the point where experiments can be undertaken (Angell and Marzluff 2005).

In the present study, crows seemed to react with a greater level of fear to objects that were larger and more obvious, particularly if the object was larger than themselves (M. Brown pers. obs.). Objects that were below a crow’s eye level while on the ground appeared to elicit far shorter latency times than those that stood >20cm high. Through preliminary trials, it was found that crow’s wariness could also be lessened by placing the object near a wall,

69 fence or log, as opposed to in an open field as crows appeared to assume that the object was part of the vertical surface, with which they were already familiar, and be more willing to approach it. This is contrary to many other urban birds, which displayed little to no fear of humans or human-related objects (M. Brown per. obs). When putting out apparatus for experimentation, this resulted in non-corvid birds often interrupting experiments before the

crows would overcome their neophobia.

Excluding and including heterospecfics

Torresian crows are a generalist species that consume a wide variety of natural and anthropogenic foods (Rowley 1973c). Experimental study sites were initially baited with dry dog food, as this was a cheap and readily available food that did not easily perish in the hot and sunny environment of Brisbane. This bait was not particularly successful, as although crows would readily eat it, they appeared to prefer other sources of food available to them in their natural environment. Canned dog food was likewise trialled, with similar results.

From observations, crows appeared to prefer carrion over other food sources, often risking road traffic in order to access a road-killed common brushtail possum (Trichosurus vulpecula) (M. Brown pers. obs.). It was considered that the red colour of raw carrion may act as an enticement to crows, standing out visually against the green and brown background. Therefore, raw beef mince was trialled as a bait, with considerable success. Crows readily flew more than 50m at the sight of raw mince being left out. While this bait perished within a day, it was usually entirely consumed or cached within hours, negating spoiling as a problem. Furthermore, it is possible that these crows were receiving mince from humans feeding the local wildlife (Rollinson et al. 2003).

Unsurprisingly, crows were far from the only urban species in Brisbane that are attracted to the mince used for baits. Many other common species, including magpies, currawongs, butcherbirds, kookaburras, brush-turkeys and white ibis (Threskiornis moluccus) were also attracted to the mince, as well as reptiles such as lace monitors (Varanus varius) and Eastern water dragons (Intellagama lesueurii lesueurii). Furthermore, all of these other species were far more inclined to interact with novel objects than were crows, meaning that baits were frequently entirely consumed before any crows had approached the apparatus. Brush- turkeys and lizards could easily be excluded by holding experiments in sites away from their

70 incubation mounds or in areas not readily accessible without flying (e.g., median strips, backyards and fenced in areas). For other birds, this problem was addressed in a number of different ways.

In some instances, mince was either replaced or supplemented with chicken , which reduced the stealing of bait by butcherbirds, kookaburras and currawongs as they were unable to consume unbroken eggs (M. Brown pers. obs.). Eggs dyed red were also trialled to test the hypothesis that crows were more attracted to the colour red. However, crows reacted with far less enthusiasm to eggs, both dyed and undyed, than they did to the mince. As such, eggs were predominantly used in conjunction with mince. Crows did not appear to approach red eggs with any more enthusiasm than they did natural eggs, though this may be due to the fact that red eggs represented some kind of novelty as an object that they would not have come across in the wild.

Alternatively, the interruption of experiments by other species was soon perceived as an important opportunity to expand the scope of the study. The intervention of these species provided the chance to compare other common urban bird species with Torresian crows. The investigations into neophobia, mirror responses and connectivity all became comparative studies of some of the common corvoids of Brisbane, while maintaining a core focus on the Torresian crow. Most prominent of these were the Australian magpie, pied butcherbird, grey butcherbird and pied currawong, all common cracticids that were related to the Torresian crow via the Corvoidea. Additionally, the investigation into behavioural reactions to mirrors was broadly expanded to include non-corvoid species such as megapodes, columbolids and the invasive common myna.

Observing and recording behaviours

Due to their wariness of humans and heightened level of neophobia, crows rarely interacted with experimental apparatus while the researcher was still in the vicinity. With rare exceptions, behaviours were recorded by either an Acorn Ltl-5210A motion camera tied to a tree or fence, or fixed upon a tripod. These cameras filmed either 30 second or 60 second videos, depending on the experiment in question, when triggered by movement near the apparatus. In some experiments, cameras were left in the field for weeks on end, with the SD card and batteries being changed regularly. Other investigations only required recording

71 apparatus to be deployed for short intervals. These cameras allowed the researcher to leave the area, increasing the probability of birds interacting with the apparatus. Finally, the urban nature of the study resulted in some study sites being too exposed to leave the expensive motion cameras unsupervised without fear of theft. At these sites, the observer would retreat to a hide to view the site.

Experimental methodology

Testing neophobia on wild birds

Neophobia in crows and related birds was tested by placing a ball of raw beef mince in view of the bird. In this case, the first method trailed was successful in producing results, so little modification was deemed necessary. Crows, currawongs, grey butcherbirds and magpies readily came to the food to eat. These birds inhabit similar niches, being primarily carnivorous generalists that are very common the urban environment (Higgins et al. 2006a). Crows were exposed to unaccompanied meat, meat placed next to a common background object (a stick) and a novel artificial object (pipe cleaners) (Figs. 4.6, 4.7). Pseudoreplication was prevented by testing crows throughout Brisbane at a large variety of sites separated by territorial borders. While crows frequently interacted with the apparatus, the distance between subjects and the apparatus as well as distractions such as the cawing of rival crows were found to have a significant effect on the time crows took to approach the meat. In order to account for this variation, an additional variable called ‘approach time’ was adopted, which began once crows were 1m away from the bait (Fig. 4.6). This method ensured that the variation in time to approach the bait was due to an interaction with the apparatus and not random distance from the bait when experimentation began.

72 1m

Control

1m

Background

1m

Novel

Figure 4.6 Diagram of study sites for study of neophobia. Interaction time began when crow crossed imaginary 1m radius circle surrounding the bait.

Figure 4.7 Novel object used in the study of urban corvoid neophobia.

73 Shape discrimination and numerosity: attempting learning tasks with wild animals

In order to test crows’ abilities to learn, recognise and distinguish between shapes and numbers, wooden bowls were painted and set at sites around Brisbane in a similar experiment to that by Bogale and Sugita (2014) but altered for the wild environment. The experiment relied on crows foraging by sight and not scent, which was consistent with observations (M. Brown unpubl. data) and studies on foraging in the closely-related little raven (Ekanayake et al. 2015, Ekanayake 2015, Ekanayake et al. 2016). Wooden bowls were chosen to be light enough for crows to easily lift but remained stable during gusts of wind. Familiarisation for the shape recognition experiment involved a number of steps. Bowls were painted with a triangle, circle or cross (Fig. 4.8) and meat was placed in the crossed bowl. Firstly, crows were presented with three bowls upside down (open side up) to familiarise crows with the presence of bowls and to train them to approach the experimental site for food. Step two involved bowls being put the right side up with mince on the edge of the crossed bowl. This required crows to lift up the bowl to access the food while the bait remained visible to passing birds. Afterwards, the meat was placed completely under the crossed bowl in full view of the crows, allowing the crows to see which bowl the food was placed under, but once it was placed, the mince was hidden. This step required crows to completely flip over the bowl in order to retrieve the mince. In the final and experimental stage, an opaque fitted sheet was placed over each of the bowls as the researcher reached under the sheet, pretending to place the meat under each bowl so as to not provide additional cues that crows may use to solve the problem. This sheet was removed before experimentation began. Crows in this stage were not able to tell which bowl the meat was under without mentally linking the cross with the reward. Before meat was placed, all three bowls were picked up, shuffled and placed back in the same three places, ensuring that the correct bowl was not always in the same place. This entire process took a period of 3-7 weeks.

Bowls were initially placed at a distance of 50cm from each other to allow all three bowls to be covered with the opaque sheet when baiting. However, crows tested in this method only chose the correct bowl in 10 of 20 trials, not significantly more than the 33% that would be achieved through randomly choosing bowls (Z = 1.1180, n.s.). It was hypothesised from this

74 and from observations made during trials, that crows were simply choosing their first bowl at random before flipping over all bowls. As observers had to retreat to a significant distance, there was no ability to remove the baited bowl if crows chose incorrectly, meaning crows were able to receive the same reward by flipping random bowls until they found the meat with little additional cost, therefore there was little advantage to learning the correct shape. The randomness of crows’ choices at this distance also suggests that crows were not able to smell the reward and were instead relying on sight. In order to create a cost for an incorrect choice, the distance between bowls was increased to 4m, requiring the crows to walk this distance if they chose incorrectly. Each bowl was covered with the sheet one at a time in random order, with the same motion of baiting the bowl made for each.

4m

Figure 4.8 Arrangement of shape discrimination apparatus. Bowls were placed at a 4m distance to punish crows that did not flip over the correct bowl.

Crows able to successfully discriminate between shapes were then tested in their ability to distinguish between quantities by being presented with the same bowls with a number of dots between ‘2’ and ‘5’ (Fig. 4.9), with only two presented at any one time. Raw mince was placed under the larger number, with two to three days of familiarisation. Pairs of crows were tested in five trials per combination, a total of 30 trials, with the sequence of combinations randomised.

75

4m 4m 4m 4m 4m 4m

Figure 4.9 All six combinations of the four numerosity bowls. Bowls were placed at random to prevent any pattern other than the number of dots from informing crows of the location of bait.

Documenting responses of wild urban birds to their own reflections

Field work Birds from throughout Brisbane were exposed to a mirror over a course of several weeks. Birds were attracted to the mirror with a combination of frozen beef mince, chicken eggs and bird seed. The mince was frozen to prevent crows from moving the entire bait away from the mirror in very few visits, instead requiring them to pick off small bits over a longer period. Eggs were hard-boiled, which, along with the freezing of meat, prolonged the period of time bait could be deployed before perishing due to heat. Mirrors were originally placed in the open to allow birds to view behind the mirror but this had a significant neophobic effect on crows. Therefore, mirrors were placed along vertical walls and logs (e.g., Fig. 4.10), which reduced the impact of neophobia. Birds were recorded by an Acorn Ltl-5210A motion camera at a maximum of 3m distance.

76

Figure 4.10 Mirror deployed in suburban backyard. Mirror was placed at wall to reduce impact of neophobia.

While this experiment was directed at crows, there was no ability to prevent other urban birds from either eating the bait or interacting with the mirror, and therefore being recorded. This was particularly significant as the bait used, while very attractive for crows, also attracted a number of the many carnivorous bird species that are common in Brisbane. These recordings of other birds totalled to 25% of all recordings that contained a bird. Instead of discarding such a large portion of the available data (Fig. 4.11), these videos were incorporated into the study, with videos of species from all sites to be merged into one dataset, with the exception of Torresian crows.

77 1400

1200

1000

800

600 Total # videos 400

200

0

Species

A C D E F G H

Figure 4.11 Cumulative number of recordings of each species in front of a mirror, at a total of eight sites (A, C-H) (See Fig. 2.8). Videos were 30 seconds in length.

Classification and cross-referencing After behaviour was recorded, it must then be categorised in a way that can be quantified. Categorisation of behaviour is highly subjective and open to interpretation and bias. Methods of classification were trialled with a small sample of fifty 30sec videos (Fig. 4.12) that were categorised by seven independent scorers using a scorer sheet shown in Appendix IV. Individual behaviours were categorised by scorers into one of several behavioural categories, before being determined whether or not the bird was interacting with the mirror, and whether the behaviour was socially directed, self-directed, or neither.

After this was conducted, the scoring of individual behaviours was found to be of little use as birds would change behaviours frequently while performing a certain task (e.g., continually looking out for predators while eating). The high frequency of behaviour changes and the large variety of possible behaviour created a significant amount of noise, through which it was impossible to find correlations between scorers or patterns within or between species. Additionally, redundancy was found in repetitive behaviours such as

78 looking to swallow food or aggressively pecking the mirror, resulting in several notations of the same behaviour repeated. In light of this trial, a far more general classification method was devised, focussing on states of bird behaviour.

6

5

4

3

2

# videos used in sample in used videos # 1

0

Figure 4.12 Distribution of 50 videos used in cross-referencing trial across different species. Five videos were chosen for crows from each site, while samples for other species were proportionate to their frequency in the dataset. See Fig. 2.8 for site locations.

Mirror Self Recognition and Mirror Image Stimulation Experimentation began with the intention of conducting Gallup’s (1970) mirror and mirror mark tests on wild Torresian crows. While the mirror test relied on interpretations of animal behaviour directed to its mirror image, the mirror mark test involves placing an out-of-sight mark on the animal that can only be seen with the mirror. In this test, mark-directed behaviours are believed to be indicative of an understanding by the animal that the mirror image is a reflection of itself (Gallup 1970). Unfortunately, the inability to account for the multitude of outside factors in the wild environment made accurately distinguishing self- directed behaviours extremely difficult. Additionally, captured crows were observed to avidly avoid anthropogenic apparatus after capture (M. Brown pers. obs.), which would have made conducting the mirror mark test impossible. Crows simply would not have approached the mirror readily while the mark was still fixed. Therefore, the experiment instead focussed on describing the behaviours crows and other suburban birds exhibited when subject to Mirror-Image Stimulation, particularly aggression.

79 String pulling: trial and error in assembling apparatus

String pulling experiments have often been undertaken on captive birds, and with a vertical hanging string (Heinrich 1995a). These setups required birds to complete a complex series of movements in order to pull up the sting, repeating six distinct steps (Fig. 4.13). Some researchers have built upon these experiments by changing the orientation of strings in relation to the reward (e.g. crossing strings over) in order to investigate the cognitive processes used to solve the problem (Taylor et al. 2010b). A vertical string apparatus was built with the intention of setting it up in the wild for crows and other species (Fig. 4.14). The apparatus consisted of a natural branch mounted upon camping tent posts at a possible height of 2.5m, sufficient height to dissuade crows from attempting to attain the bait by jumping from the ground. This apparatus was set up at the Site D. Due to the size of the apparatus, there was a significant neophobic impact upon subject crows and they did not come near the site.

Figure 4.13 Process used by a bird in order to pull up a vertical string (Heinrich 1995).

80

Figure 4.14 Original vertical string pulling apparatus. Artificial branch could be deployed anywhere, allowing flexibility. Apparatus was discarded due to significant neophobic reactions from crows and dominance of the area surrounding the apparatus by other urban birds.

After three weeks, the apparatus was removed and a string was tied from a real tree branch, in the hope that the lack of artificial apparatus would make the birds more willing to interact with the experiment. Unfortunately, the openness of the apparatus resulted in other birds attempting to attain the meat, including noisy miners (Manorina melanocephala), laughing kookaburras and grey butcherbirds. Grey butcherbirds would repeatedly fly up to the meat from the ground, and attempt to rip it free of the string, with occasional success. Noisy miners, a small species of , crawled down the vertical string to peck at the meat (Fig. 4.15). Kookaburras would simply wait until another bird had attained the meat, then attempt to steal it. No birds attempted to pull up the string, which is consistent with previous documentation that only crows (Heinrich 1995a) and parrots (Pepperberg 2004) have been able to spontaneously solve the vertical string pulling problem. The presence of kookaburras kept crows away from the experiment, and did not attempt to attain the meat once. After three weeks of this trial, including attempts to discourage unwanted birds, the vertical string pulling apparatus was abandoned.

81

Figure 4.15 Noisy miner crawling down vertical string to obtain beef.

A horizontal string pulling apparatus was created, using a small 60cm x 50cm x 20cm cage (Fig. 4.16a). In order to prevent birds swallowing the meat with string still attached, the string was tied to milk bottle caps, within which the meat was placed. The experiment consisted of four stages: a single string with a meat reward, in order to familiarise crows with pulling the string; then a second string was added, with the milk bottle cap empty (Fig. 4.16b); and in stage 3 the strings were to be crossed over as in Taylor et al. (2010b) (Fig. 4.16c).

82 a)

b) c)

Figure 4.16 Cage used for string discrimination experiment (a), set for parallel (b) and crossed (c) experiments.

The cage string apparatus was tested in a site with an unusually bold pair of breeding adult crows, which reacted in a highly neophobic fashion to the apparatus. Any successful attempts by the adult crows resulted in them being attacked by butcherbirds, magpies and

83 kookaburras, attempting to gain the meat. This high neophobia in bold individuals, along with the inability of crows to experience a reward for completing the experiment, led to its abandonment in favour of a much smaller and less intimidating apparatus.

The final apparatus for the string experiment was designed with the primary aim of reducing neophobia as much as possible. The apparatus was smaller, less than 1/8th the size of the previous apparatus, and low enough that the crows could easily stand over and look down upon it. The material was also changed from cast iron to transparent plastic. The new apparatus was trialled at two sites, at which crows readily interacted. Even so, after several trials, it became apparent that crows were not learning which string they should pull. It was determined that the lack of learning came from a lack of disincentive to pull the wrong string. As both strings could be freely pulled, a crow that had pulled the wrong string would only have to move 20cm and pull the only remaining string to receive the same reward they would have received for pulling the correct string in the first place. Attempts to interrupt unsuccessful crows before they could attain the meat only resulted in subjects quickly pulling both strings without investigating the apparatus, in order to ensure they gained the food reward before being interrupted.

A way of denying food to unsuccessful subjects involving a pulley system was devised in a way that did not significantly increase the neopbobic reactions of crows, and did not have to be manually triggered by an observing human, as some subjects would not interact with apparatus if a human was nearby (Fig. 4.17). Fishing line was attached to both milk bottle lids and was threaded throughout the apparatus to a small stick holding up a piece of Perspex large enough to cover the opening of the apparatus. This meant that the pulling of either string would cause the stick to be pulled into the apparatus, allowing the Perspex to drop to the ground, covering the opening and blocking access to the remaining milk bottle cap.

84

Figure 4.17 Diagram of final horizontal string pulling apparatus.

85

Section 2: Experimentation and Results

͠

86 STATEMENT OF CONTRIBUTION TO CO-AUTHORED PUBLISHED PAPER

This chapter includes a co-authored paper. The bibliographic details of the co-authored paper, including all authors, are:

Brown, M. J. and Jones, D. N. (2016), Cautious Crows: Neophobia in Torresian Crows (Corvus orru) Compared with Three Other Corvoids in Suburban Australia. Ethology, 122: 726–733. doi:10.1111/eth.12517

My contribution to the paper involved:

Reviewing of the literature, designing and conducting of experiments, recording and statistical analysis of data, and writing.

(Signed) ______(Date)______

Matthew Brown

(Countersigned) ______(Date)______

Corresponding author of paper: Prof. Darryl Jones

87 Cautious crows: Neophobia in Torresian crows (Corvus orru) compared with three other corvoids in suburban Australia

Abstract

Corvids (Family: CORVIDAE) are a clade of some 120 species widespread throughout much of the world that have attracted the interest of researchers due to their impressive cognitive abilities. The group is, however, also generally described as neophobic, a trait that increases the difficulty of undertaking such research. In Australia, Torresian crows (Corvus orru), like corvid species worldwide, thrived in urban environments, sharing this habitat with a number of other corvoid (Superfamily: Corvoidea) species. While each of these species has successfully colonised urban areas, the extent to which neophobia is present is not known. This study empirically tested the extent to which neophobia is exhibited in wild urban Torresian crows by measuring the delaying effect of a novel object to obtaining food and any changes in neophobic behaviours displayed. This was then compared to the other urban corvoid species that inhabit similar niches. This study confirmed that Torresian crows are significantly wary of a novel objects, displaying more neophobic behaviours and taking longer to attain the food. Crow behaviour provided evidence in support of both the Dangerous Niche Hypothesis and the two-factor model of neophobia and neophilia. Crows also displayed these behaviours to a significantly greater extent than the three other corvoids studied. However, the individual variation in crow behaviours when exposed to a novel object was extensive. This variation may be attributed to differing behavioural types between individuals, or different experiences with novel objects or humans in the bird’s past.

Introduction

Corvids are a highly intelligent clade of birds that include crows, ravens, jays and magpies (Madge and Burn 1999). This intelligence, including displays of problem solving (Heinrich and Bugnyar 2005, Taylor et al. 2010b), social learning (Templeton et al. 1999a, Holzhaider et al. 2010) and tool-use (Hunt 2000b, Caffrey 2000, Bluff et al. 2007, Mehlhorn et al. 2010)

88 has lead these birds to be of considerable interest for cognitive and behavioural studies. Some aspects of these attributes, however, can make corvids particularly challenging to study (1995b, 1988a). For example, investigating animal cognition often requires exposing captive or wild subjects to artificial experimental apparatus (Emery 2004, Emery and Clayton 2004, Seed et al. 2009). In what is known as the ‘Oz Fallacy’ (Greenberg and Mettke- Hofmann 2001, p121), researchers run the risk of “mistaking courage for brains” as less- wary subjects are more likely to interact with the apparatus and solve it more quickly. Alternatively, researchers may mistake a reluctance to interact with experimental apparatus as an inability to solve the task or activity.

Such wary behaviours are at least, in part, associated with neophobia, which is thought to be common in adult corvids (Kijne and Kotrschal 2002, Heinrich 1988a). Neophobia is predominantly defined as the avoidance by an individual of an unfamiliar object that has not been encountered before (Greenberg and Mettke-Hofmann 2001) and is considered to be present to some extent in all species of mammals and birds (Corey 1979). Neophobia may be demonstrated by placing a novel object near familiar food and measuring the latency of a focal bird to commence foraging (Greenberg 2003). A longer time taken to initiate feeding can, generally, be attributed to the presence of the novel object. It is also commonly typified in birds exhibiting apparently fearful behaviours such as ‘jumping jacks’, where the animal approaches the object before hopping back suddenly (Heinrich 1988a, Greenberg 2003). While neophobia may be adaptively advantageous in reducing the possibility of exposure to unfamiliar objects and attendant risks, it may also limit the exploration of novel foods and objects, and can be detrimental to innovation (Stöwe et al. 2006a).

Greenberg (2003) describes neophobia in two discrete categories: functional and intrinsic. Functional neophobia refers to the extent to which neophobia is expressed by wild adult animals, and is subject to the experiences of individuals throughout their lifetime. Innate neophobia, in contrast, excludes the influence of prior experiences in order to assess its inherent expression. Thus, tests of wild animals attempt to discern functional neophobia, while those on hand-reared individuals are aimed at describing innate neophobia. Neophobia has been comprehensively studied in captive passerines (Boogert et al. 2006, Coleman and Mellgren 1994, Greenberg 1984, Mettke‐Hofmann et al. 2009), while fewer have been conducted on wild animals (Vernelli 2013, Mettke-Hofmann et al. 2013).

89 Experiments undertaken by Greenberg (1989, 1992) comparing neophobia in swamp (Melospiza georgiana) and song sparrows (Melospiza melodia) produced contradictory results among wild and captive birds, suggesting that certain experiences in the lives of young wild swamp sparrows increased their neophobia while this was not the case in song sparrows. This discrepancy suggests that relying on studies of hand-reared animals may provide an incomplete or even contradictory assessment of various species’ expression of neophobia.

Neophobia is often associated with a specialist diet, with highly neophobic species considered to be more likely to be specialised as their exploration of new food sources is limited, an idea central to the Neophobia Threshold Hypothesis (Greenberg 1983). This concept contrasts with the more traditional view of neophobia exemplified by the Dangerous Niche Hypothesis, where the behaviour is associated with avoidance of potential dangers (Greenberg 2003, Greenberg and Mettke-Hofmann 2001). According to the Dangerous Niche Hypothesis, birds that eat a wide variety of foods are more likely to encounter dangerous foods and objects and a heightened level of wariness is an evolutionarily advantageous trait (Greenberg 2003). This hypothesis explains to some extent the detection of neophobia in generalist species such as house sparrows, rats and ravens (Barnett 1958, Heinrich 1988a, Echeverría and Vassallo 2008, Brunton et al. 1993) and has been supported by investigations into wild birds by Mettke-Hofmann et al. (2013). Corvids have been frequently recorded as being wary of unfamiliar items or food types new to the bird’s experience (Heinrich 1988a), with Kijne and Kotrschal (2002, p13) stating that common ravens (Corvus corax) often take “minutes to months” before they become familiar with a novel object. This prevalence of neophobia in a generalist that so often interacts with humans seems to favour the Dangerous Niche Hypothesis over the Neophobia Threshold Hypothesis (Vernelli 2013). While neophobia in corvids is generally accepted (Greenberg and Mettke-Hofmann 2001), quantitative studies have generally been restricted to investigations into the effect of social context and sex in common ravens (Stöwe et al. 2006a, 2006b, 2007, Range et al. 2006).

In their review of neophobia in birds, Greenberg and Mettke-Hofmann (2001) describe corvids as displaying, in addition to neophobia, high levels of neophilia, a heightened attraction to novel objects. This apparent contradiction, first proposed by Montgomery

90 (1955) as the two-factor model, decouples neophobia from neophilia and asserts that an animal may be both curious and cautious of novel objects. Such conflicting motivations may result in the animal approaching and retreating from the object repeatedly (Vernelli 2013). While most adult corvids are generally thought to be highly neophobic, young may exhibit neophilia to an extreme extent; Heinrich (1995b) determined that juvenile ravens were up to 24,000 times more likely to touch novel objects than those with which they were familiar. Heinrich (1988a) also noted that neophobic tendencies were prominent in adolescent ravens, but ceased after three or four exposures to the object. These adolescent ravens also appeared curious of novel objects, even while displaying neophobic reactions (Heinrich 1988a).

Neophobia in wild adult corvids may have significant adaptive drawbacks, being thought to constrain exploration, learning and innovation (Stöwe et al. 2006a, Stöwe et al. 2006b). Corvids are often scavengers, especially in urban environments, where they exploit a large variety of foods, including road kill, refuse, and discarded food scraps (Range et al. 2006). Given the large variety of food available in urban settings, restrictions on innovation could potentially hamper the birds’ ability to take advantage of the relative abundance of anthropogenic foods (Kijne and Kotrschal 2002, Range et al. 2006). However, more recent studies have challenged this notion, suggesting that innovation may not be hampered by neophobia (Griffin et al. 2014, Liker and Bókony 2009, e.g., Coleman and Mellgren 1994). Neophobia also provides protection against potential risks associated with foods, such as apparent carcasses that may actually be living, lures of predators such as those used by the -tailed horn viper (Pseudocerastes urarachnoides), or baits or traps placed by humans (Heinrich 1988).

A recent intensive investigation of neophobia in wild Eurasian magpies (Pica pica) by Vernelli (2013) noted that this species displayed both high neophobia and neophilia, supporting Montgomery’s (1955) two-factor model. This was most evident in the subjects’ tendency to approach and retreat from and circle around novel objects (Vernelli 2013). Previous studies into neophobia in corvids have also noted considerable variation in both latency and likelihood of exploratory behaviours among individual ravens (Heinrich 1988a, 1995b, Stöwe et al. 2006a, Stöwe et al. 2006b, Stöwe and Kotrschal 2007). Stöwe et al.

(2006b) investigated the effect of social context on latency to approach novel objects, while

91 Range et al. (2006) also found individual and sex variation in learning abilities and explorative behaviours in common ravens, citing ‘behavioural syndromes’ as a possible explanation for the variance.

A number of studies have linked neophobia with animal personalities (Van Oers et al. 2004), due to its negative correlation with exploratory behaviour and aggression (e.g., Van Oers et al. 2004, Dall 2004, Frost et al. 2007, Sloan Wilson et al. 1994, Sneddon 2003, Wilson and Godin 2009). Carere and Locurto (2011) assert that individual behavioural traits impact on an individual’s willingness to interact with novel objects and environments, and that neophobia may also increase an animal’s ability to detect slight changes in familiar habitats. Heinrich (1988a) also noted that hungry ravens were less likely to display neophobic behaviours than well-fed ones.

Like many cities worldwide (Marzluff et al. 2001), the city of Brisbane, Australia, has seen a massive increase in the densities of urban corvids over the past few decades (Sinden 2002, Woodall 2004). Once considered to be rare and extremely wary (Jack 1938), the native Torresian crow (Corvus orru) is now abundant and visible in modified environments like Brisbane (Higgins et al. 2006a, Ryan 2007), possibly due to the abundance of invertebrate and anthropogenic food (Woodall 2004, Sinden 2002). While urban Torresian crows are more habituated to humans than their rural counterparts (D. Jones unpubl. data), they appear to be more reluctant than other urban birds (such as Australian magpies (Cracticus tibicen), butcherbirds (Cracticus spp.) and laughing kookaburras (Dacelo novaeguineae)) to take food provided by a human at close proximity (M. Brown pers. obs.)

Brisbane is also inhabited by a variety of corvoids (Superfamily: Corvoidea), including the Australian magpie, grey butcherbird (Cracticus torquatus) and the pied currawong (Strepera graculina). These species (Family: Artamidae) are distantly related to the Torresian crow (Kearns 2011) and occupy similar niches. All four species inhabit the edge habitat between forest and open grass, a prominent feature of suburban landscapes, all have similar generalist diets, are highly social, and all have flourished in the urban environment (Peter et al. 2006). In their analysis of bird feeding in suburban Brisbane, Rollinson et al. (2003) noted that Australian magpies, butcherbirds and Torresian crows were among the most commonly-fed birds, with magpies and butcherbirds often being specifically targeted by bird feeders.

92 While corvids as a group are generally considered to be neophobic, this has not been assessed empirically in the Australian corvids and no such generalisations exist for the Artamidae. In this study we investigated whether urban Torresian crows exhibit quantifiable functional neophobia, and examined whether it is more pronounced compared to similar corvoid species in the same environment.

Methodology

Study area

The subtropical Australian city of Brisbane (27.4679° S, 153.0278° E), population 2.45 million (ABS 2015), is typified by low-density suburban housing with expansive lawns and an abundance of large trees (Sushinsky et al. 2013). Experiments were undertaken using wild adult birds found at numerous environmentally-similar locations throughout Brisbane’s southern suburbs between the months of November and February in 2013/14. Studies took place from dawn to 10:00 and from 15:00 to dusk on clear days. Each of the species investigated were distinctly territorial and sedentary during this time, allowing relative certainty that all of the birds included in the observations were different individuals. Sites were, on average 1km apart, although several closer sites 100-300m apart were separated by obscuring man-made structures. Torresian crows were tested at 25 sites, while 11 Australian magpies, 10 grey butcherbirds and 5 pied currawongs were also tested.

Experimental design

Free-ranging birds (Torresian crow, Australian magpie, grey butcherbird and pied currawong) were presented with a ball of raw beef mince ~2.5cm in diameter in three experimental scenarios: ‘control’, ‘background’ and ‘novel’. In the control tests, the bait was provided alone on the ground within 10m of a perched bird. In the background and novel tests, an object was placed next to the bait. These were either a three-stemmed natural dead twig (background) (15 x 15 x 15 cm) or a similarly-shaped object made of multi- coloured pipe cleaners (novel). The experimental design was similar to that used by Echeverría and Vassallo (2008), with the addition of the background treatment to ensure that any observed changes in the bird’s responses were due to the novelty of the object and not simply the presence of the object or its association with a human. Due to the foraging

93 nature of the species, and in an effort to minimise unnecessary neophobia, placing the sites on the ground was deemed preferable to using artificial bird feeders.

Once the apparatus was in place, the observer retreated to a distance of no less than 7m and recorded the behaviours manually. The first bird to approach the meat was considered the ‘focal bird, and only its behaviour was noted. ‘Latency time’, the time between the bait being deployed and the bird subsequently making contact with it, was measured with a stop-watch. A second timer was started when the bird had approached to within 1m of the bait. This second measurement, referred to as ‘approach time’, was a more accurate determination of the delaying influence of the novel object as it accounted for distractions, distance and other variables that may have delayed the bird from approaching the bait. The number of ‘jumping jacks’ displayed by the focal bird was also recorded, as were the number of birds present during the experiment. The experiment ceased once the bird’s beak made contact with the bait. Crows were subjected to the ‘control’, ‘background’ and ‘novel’ experiments in a random order on separate occasions between one and four days apart, while other species were only subjected to the novel test for comparison.

Data analysis

Similar to studies such as (Schiestl 2013), the data was non-normal, requiring non- parametric tests to determine significant effects. The presence of unequal sample sizes also prevented the use of more traditional analyses. The effect of novelty on ‘approach time’ and the frequency of jumping jacks was analysed by two separate Kruskal-Wallis tests by ranks in SAS 9.4, as were the differences of these two variables between the four corvoid species. Differences between individual treatments were determined through use of Wilcoxon Normal Approximations in SAS 9.4.

These experiments were approved by the Griffith University Animal Ethics Committee (ENV/16/12/AEC and ENV/16/13/AEC)

Results

Neophobia in wild urban crows

A total of 65 tests were conducted on crows, comprising 25 control, 19 background and 21 novel tests. In crows, 85% of tests were conducted in the presence of an individual’s mate

94 only, with 15% undertaken in the presence of one bird or a pair with a juvenile. Novelty was found to have a significant effect on approach time (df = 2, χ²=27.8045, p<0.0001) (Fig. 5.1) and frequency of jumping jacks (df=2, χ²= 27.0535, p<0.0001) (Fig. 5.2). Individual Wilcoxon tests found that the novel state induced longer approach times than both the control (Z=- 5.003, p<0.0001) and background (Z=-2.1501, p<0.05) states, while approach times in the background state were also longer than in the control (Z=3.257, p<0.001). A similar trend occurred with jumping jacks, with more of these reactions occurring in novel experiments than in background (Z=-2.3088, p<0.05) or control (Z=-4.0339, p<0.0001) scenarios. However, the background object did not induce a significantly larger frequency of jumping jacks than the control (Z=1.3964, p<0.08).

Figure 5.1 Interaction time of Torresian crows in different novelty levels. Box plot represents interquartile range (box), median (line within box) mean (◊), maximum and minimum values within 1.5IQR fences (whiskers) and values outside 1.5 Interquartile Range (IQR) fences (o).

95

Figure 5.2 Frequency of jumping jacks displayed by Torresian crows in different novelty levels.

Comparison of neophobia in urban corvoids

Totals of 21 crows, 11 magpies, 10 grey butcherbirds and 5 pied currawongs were exposed to the novel stimuli. Both approach time (df=3, χ²=8.69991, p<0.05) (Fig. 5.3) and the frequency of jumping jacks (df=3, χ²=17.3530, p<0.001) (Fig. 5.4) were found to differ between the tested species of corvoid. Torresian crows were delayed by the presence of a novel object for longer than magpies (Z=-2.1425, p<0.05), grey butcherbirds (Z=-2.3453, p<0.01) and currawongs (Z=-1.9518, p<0.05). Crows also displayed a significantly higher frequency of jumping jacks than the three other species; magpies (Z=-34671, p<0.0005), butcherbirds (Z=-2.6861, p<0.01), and currawongs (Z=-1.9061, p<0.05).

96

Figure 5.3 Interaction time with novel treatment of four Corvoid species.

Figure 5.4 Frequency of jumping jacks with the novel treatment in four Corvoid species.

97 Discussion

Wild Torresian crows were shown to display neophobia through both increased latency time and frequency of neophobic behaviours. Surprisingly, crows were found to respond to the simple presence of an object, even though the object (a dead twig) was a common part of its habitat. This may suggest that crows were cautious of the twig because it had been associated with a human (possibly witnessed during the setup), or that the crows experienced a neophobic reaction to the stick being placed in a novel position. However, neophobia was greater in all measures for the object with additional novelty than for the one without. Crows interacted with the novel apparatus in a way similar to Vernelli’s (2013) description of Eurasian magpies by repeatedly approaching and retreating from the object, behaviour that was in that study deemed indicative of the two-factor model of neophobia and neophilia.

The difference in means between treatments, however, appears to be only part of the story. The considerable variation within treatments suggests that neophobia and wariness varies significantly between individual crows. This supports Kijne and Kotrschal’s (2002) statement that crows can take “months to minutes” to become familiarised with novel stimuli. It is possible that these differences can be explained by different behaviour types, such as varying levels of boldness, between individuals. Alternatively, varying levels of hunger between individuals may have influenced the study, though all crows existed in a similar environment. A third explanation may be that crows at different sites may have had different life experiences involving humans or novel objects in general. Social context appears to be an unlikely candidate, as crows tested were sedentary mated pairs, not living in large social groups.

Crows also responded to the novel stimuli in a far more exaggerated fashion compared to other urban corvoids. Latency for magpies, butcherbirds and currawongs also more closely resembled that which crows displayed for the background object, suggesting this may be simply a reaction to an object as opposed to neophobia. While all species measured have been extremely successful in the urban environment and fill similar niches as generalist carnivorous edge species, crows appear to be unique in the extent of their neophobia. This

98 disparity in results between generalists appears not to support the Neophobia Threshold Hypothesis.

Prior interactions with humans may explain this disparity to some extent (Jones and Everding 1993). Rollinson et al. (2003) noted that Torresian crows, Australian magpies and pied butcherbirds were all regularly fed by bird feeders, although only the latter two were fed intentionally. The similarity in results of pied currawongs to magpies and butcherbirds suggests human feeding may not be a driving factor. Human persecution may provide an alternative explanation, as even though all four species are protected by Queensland law, Torresian crows are occaisionally targetted by residents with poisonous bait (D. Jones unpubl. data). Such an effect of human persecution could be considered supportive of the Dangerous Niche Hypothesis. While (Echeverría and Vassallo 2008) suggested that some neophobic species benefit from foraging with more explorative species, it seems unlikely that Torresian crows utilise these less neophobic species in this way as they are rarely seen in their company and are easily intimidated in confrontations in which they do not outnumber the heterospecifics (M. Brown pers. obs.).

While all studies were undertaken in relatively similar suburban environments, interactions with the human inhabitants of the sites, either negative or positive, could not be accounted for. Additionally, Greenberg and Mettke-Hofmann (2001) suggest that highly intelligent birds, such as crows (Emery et al. 2007), are more likely to be neophobic. This heightened neophobia in crows but not in other related species may be interpreted as evidence in support of Greenberg and Mettke-Hofmann’s (2001) statement.

In this study we have quantifiably demonstrated that, despite living in a highly complex and dynamic urban environment, Torresian crows have maintained the fear of novel stimuli that is commonly associated with their Genus. The extent of this neophobia, however, varied substantially between individuals, for which there are number of possible explanations. Both this heightened neophobia and its unpredictable nature raise obstacles regarding the study of these birds in the wild. Any experimental apparatus novel to the crow would require a significant familiarisation process, the length of which would vary wildly between individuals. Closely-related birds that inhabit a similar niche did not display neophobia approaching that displayed by crows. This difference raises questions of the process of urbanisation and source of neophobia in these otherwise similar species.

99 References

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104 Shape and quantity discrimination in wild Torresian crows (Corvus orru) in an urban environment

Abstract

The family Corvidae is a particularly well-studied group by students of animal intelligence and learning, yet the vast majority of work on this group is focused on a few Holarctic species, with only one exception. In Australia, the family is represented by five Corvus species. Corvids have been tested in both associative learning and rule learning in controlled laboratory environments. Both hooded crows (Corvus cornix) and jungle crows (Corvus macrorhynchos) are capable of learning to associate arbitrarily drawn shapes with a food reward, distinguish between this and another shape, and between pairs of same and different shapes. Additionally, many species including corvids have been tested for numerosity, particularly in a concept of greater and lesser quantities. In this study, wild Torresian crows were tested for their ability to associate a shape with food and to distinguish between this and other shapes. Successful crows were then presented with two quantities of marks, the largest of which resulted in a food reward. Three of the five crows tested were able to discriminate between shapes, though none significantly preferred the larger quantity over the lesser. It is possible that this latter failure was due to the less- controlled conditions in conducting experiments in the wild, or Torresian crows have numerosity capabilities of other corvid species. This study highlights the possibility of investigating more complex processes such as same-difference and oddity-learning in both Australian corvids and in other wild birds.

Introduction

Cognition in crows

Corvids (Family: Corvidae) are a group of some 120 species of highly-encephalised songbirds (Goodwin 1976) that are now of significant interest to students of animal cognition due, in part, to their exemplary results in cognitive experiments (Angell and Marzluff 2005, Emery

105 2004, Emery and Clayton 2004). Recent studies of self-recognition (Kusayama et al. 2000, Prior et al. 2008, Medina et al. 2011), tool-use (Montevecchi 1978, Hunt 2000b, a, Caffrey 2000, 2001, Weir et al. 2002, Bluff et al. 2007, Balda 2007, Bird and Emery 2009a, Wimpenny et al. 2009, Mehlhorn et al. 2010), social learning (Templeton et al. 1999b, Holzhaider et al. 2010), cultural evolution (Marzluff and Angell 2005, Marzluff et al. 2010), imagination (Heinrich 1995a, Bird and Emery 2009a), cooperation (Bossema and Benus 1985, Seed et al. 2008) and memory (Kamil and Balda 1990, Balda and Kamil 2002, Clayton et al. 2007, Marzluff et al. 2010) have made the corvids a poster group for avian cognition both in the scientific community and the general public.

Much of the cognitive research conducted on corvids over the past 30 years has been focussed on animals either raised in captivity or subject to a captive environment during experimentation (Chapter 3). Animals kept in captivity can exhibit both immediate and chronic stress, reduced testosterone, and other impacts, all of which have the capacity to alter the subject’s behaviour (Calisi and Bentley 2009). Excessive reliance on data from captive animals runs the risk of negating the environmental context in which the animal has evolved, particularly in cases where generations of subjects have been raised in captivity (Calisi and Bentley 2009).

Associative learning, rule learning and shape discrimination

Animals can be trained to associate certain stimuli with a food reward, the most famous example of which are so-called ‘Pavlov’s dogs’ experiments, where dogs learned to associate a ringing bell with a food reward (Dugatkin 2004). This classical conditioning process, as well as stimulus-response techniques that train animals to push a button or pull a lever, have been historically used frequently in the ethological literature (Pearce and Bouton 2001). These are examples of associative learning, where subjects associate objects, colours or shapes with a food reward, have become standard approaches in investigations of cognition that involve training (Review in Shettleworth 1998). Other approaches test the ability of animals to understand rules and concepts, such as that of a triangle with all its variations, as opposed to a particular shape that is always the same (Bogale and Sugita 2014), or a greater or lesser quantity of objects or shapes (Bogale et al. 2011).

106 Little is known about concept formulation in corvids, particularly wild corvids (Bogale and Sugita 2014), with notable exceptions being studies of the ability of hooded crows to transfer a ‘same-different’ concept from colour to numerals (Smirnova et al. 2000) and colour to shapes (Wilson et al. 1985). Bogale and Sugita (2014) attempted to investigate concept learning relating to artificial stimuli in jungle crows, presenting captive birds with triangles and non-triangles, with subjects trained to select triangles over the alternative for a food reward. Cups were covered with a card, upon which a shape was printed, with the crow being rewarded if it selected the triangle and the cups removed if it selected the wrong shape. These authors obtained highly successful learning for this task, with the subjects selecting the correct shape in over 80% of trials. After changing colours and orientation, the majority of the trained crows continued to pass the test, only failing when the researchers altered the shape of the triangle to a substantially different form, suggesting that the crows were generally able to transfer their concept learning to novel situations.

Smirnova et al. (2000) demonstrated that hooded crows are able to distinguish oddity on the basis of shape, colour and the number of elements, indicating an ability to discriminate among arbitrary symbols as well as differing quantity. These birds were also able to assimilate this ability as a general rule and apply it to novel stimuli. Transferring such matching stimuli to novel situations is unusual in other animals (Wright et al. 1988), with the exception of chimpanzees (Oden et al. 1988).

Numerosity

Numerosity, the ability to understand and distinguish quantities, has been tested for and detected in a number of taxa (Smirnova et al. 2000, Pepperberg and Gordon 2005, Honig and Stewart 1989). Several authorities are of the opinion that animals prioritise quantity below other stimuli such as shape, colour, size and brightness (Brannon and Terrace 2000, Davis and Pérusse 1988, Bogale et al. 2011, Dehaene et al. 1998). Animals such as pigeons (Columba livia) appear to be unable to solve the more complex cognitive tasks corvids are capable of (Zorina et al. 1996, Wilson et al. 1985, Wilson and Boakes 1985) but are capable of numerosity (Zorina and Smirnova 1994). Zorina and Smirnova (1994) were able to show that hooded crows and pigeons (Family: Columbidae) both have an understanding of the concepts of greater and lesser, preferring to eat a greater amount of food items when

107 presented with two options of differing quantities. These researchers later varied the ratio of the area covered by the marks to ensure that the subject crows were choosing based on the number of items and not the size of the items (Zorina and Smirnova 1996).

Bogale et al. (2011) trained jungle crows to associate the numerical quantity of ‘5’ with a food reward, and then presented them with five items and a different novel quantity. This was successful when the subjects were presented with five items or less but when offered a larger quantity, they preferred the larger amount. Bogale et al. (2011) also suggested that individual crows may have used different strategies for discrimination suggesting the object- file mechanism used by primates for lower number (Hauser et al. 2000, Kahneman et al. 1992) and the analogue magnitude with larger numbers, a process thought to be used by African grey parrots (Psittacus erithacus) (Al Aïn et al. 2009).

These experiments imply that magnitude influences discrimination ability because as the numerical ratio and quantity increased, accuracy decreased, suggesting that performance of trained subjects was supported by analogue magnitude estimation. According to Irie- Sugimoto et al. (2009), animals’ quantitative abilities, disparity and magnitude effects imply the use of an analogue magnitude model rather than the object-file model. This suggests that Weber’s Law, that states that the discrimination between two quantities becomes easier as their ratio between them increases, applies to the discrimination of number in animals (Emmerton and Renner 2006). Bogale et al. (2011) suggested that jungle crows switch to analogue magnitude when quantities increased, while Al Aïn et al. (2009) found evidence of the use of analogue magnitude in African grey parrots with performance not being affected by number but by ratio. Unlike rhesus monkeys (Macacca mulatta) (Hauser et al. 2000), jungle crows were able to discriminate between 4 and 5.

Learning in Australian birds

Australia is a highly-urbanised country, with approximately 80% of the population living in sprawling suburbia surrounding the major cities (Atkins et al. 2015). This has led to the formation of a uniquely Australian variation of the urban bird assemblage, including a number of endemic species such as the Australian corvids, Cracticids (magpies, butcherbirds and currawongs), honeyeaters and a wide array of parrots (Parsons et al. 2003, Sewell and Catterall 1998, Green et al. 1989), all of which have had to adapt to their new suburban

108 lifestyle, requiring learning to at least some extent (Chace and Walsh 2006). Despite the persisting image of Australia’s fauna being centred around kangaroos, koalas, cassowaries and crocodiles, it is through these suburban birds that the vast majority of Australians interact with the natural world in their everyday lives (Low 2002).

Learning in Australian birds has been tentatively explored to some extent in reports of unusual foraging innovations (Kaplan 2015, Lefebvre et al. 1998). Torresian crows have learned innovative foraging strategies, including flipping over the poisonous cane toad (Bufo marinus) to expose the edible underside (Donato and Potts 2004), feeding on ticks on invasive (Bos javanicus) (Ja 2006) and anecdotes of the birds unzipping children’s school bags in order to access their lunch. In more rural areas, ornithologist Bob Gosford has reported black kites (Milvus migrans) and brown falcons (Falco berigora) picking up smouldering sticks in order to start and spread bushfires, preying on the mammals fleeing the flames (Wilson 2016).

The vast geographical scale of the Australian continent and the relatively limited number of scientists and trained observers has meant that knowledge of learning behaviours among the continent’s native fauna is somewhat more reliant on public anecdotes than in other Western nations. Any empirical investigations into the learning abilities of Australian species would do much to fill a gap in our knowledge. One of the most potentially intelligent Australian bird species which many Australians regularly observed is the Torresian crow, one of the more abundant birds in the suburbs of South-East Queensland (Green et al. 1989, Sewell and Catterall 1998). An investigation into learning and concept formulation in an Australian corvid will add another piece to the puzzle of corvid cognition, and compliment studies of northern hemisphere species.

In this study we investigated both associative learning and rule learning in wild Torresian crows. Could wild Torresian crows, with the environmental complexity they must encounter on a daily basis, learn to associate an arbitrary drawn shape with a food reward and discriminate between this and two other shapes? Whether Torresian crows could learn a ‘greater than’ rule with quantities, associating a larger number of dots with food rewards, was similarly investigated. In doing so, we also assessed how these traits, traditionally tested for in captive animals under controlled conditions, and could be investigated in a wild setting in the complex suburban environment.

109 Methods

Study species

The Corvidae are represented in Australia by five visually-similar species of Corvus, one of which is the Torresian crow, the dominant corvid in the northern half of the continent. Once considered rare and extremely shy in urban areas, they are now one of the most common bird species in the subtropical city of Brisbane (Sinden 2002, Woodall 2004). Medium-sized and all-black, the bird is known mostly for its loud caw, often a source of annoyance for residents who happen to live near a roost (Sinden 2002). The species has developed numerous behavioural changes in its adaptation to urban life in Brisbane, including communal roosting, forming much smaller territories, and dominating commercial areas in search of anthropogenic food (Everding and Jones 2006).

Study sites and apparatus

Five experimental study sites were established within separate Torresian crow territories in suburban Brisbane. These sites were separated by a minimum of 100m, a maximum of 20km and a median of 2km. Two of these sites were located at Griffith University’s Nathan Campus, within a dry sclerophyll forest, while the other three were located in accessible backyards in the surrounding suburbs. Three inverted brown wooden bowls were provided, each with a large, conspicuous shape painted in white on the upward facing base. These shapes were a cross, a triangle and a circle (Fig. 6.1). The bowls were placed 4m apart in a triangular arrangement. Wooden bowls were used to prevent the apparatus from blowing away in strong wind while remaining light enough for crows to easily lift with their bills. Crows were initially familiarised for one to two weeks with the bowls positioned with the edge resting on a small ball of beef mince, visible to the crow but requiring the subjects to interact with the apparatus in order to obtain the food reward. Mince was then placed under the bowl marked with the cross and experimentation did not commence until crows were readily lifting bowls with little to no neophobic behaviours, a training period lasting 2-4 weeks.. The bowl and immediate area was covered by an opaque sheet, and experimenters made explicit actions associated with the apparent placing of mince under all bowls in each trial, ensuring that the crows could not simply view the placing of the meat under the correct bowl, and have any other visual cues to inform their choice of bowl.

110 4m

Figure 6.1 Diagram of shape discrimination experimental apparatus (not to scale)

Consistent with the species’ natural wariness, most would not interact with the apparatus unless the researcher had retreated to a distance of over 20m, or in some cases had left the area entirely. It was therefore impossible to remove the bowls if the crow turned over the incorrect bowl first. In cases where the observer retreated out of sight, the behaviour of the focal animal was recorded with an Acorn Ltl-5210 game camera. Originally, subjects were presented with all three bowls only 50cm apart. However, it was determined that this proximity was insufficient disincentive to them flipping all the bowls without regard for the shape, an action that would result in the same food reward for little additional work. For this reason, the distance between the bowls was increased to 4m, requiring the crows to walk the extra distance if they chose the wrong bowl. This resulted in crows, perched above the study site, making an active choice from above and landing next to their chosen bowl.

111 Shape discrimination

Five territorial pairs of wild Torresian crow were presented with the experiment 20 times each, over a period ranging from 1 to 20 days, depending on the bird’s level of wariness. A trial in which the bird flipped the cross bowl was considered to be a success, whereas flipping any other bowl, resulted in a failure. Flipping was defined as any attempt by the crow to grab the edge of the bowl with its beak, regardless of whether the bowl was actually fully inverted. This meant that any investigation by a crow to determine whether a bowl contained the food reward was counted as the crow choosing that bowl. The total number of successful trials for each site was compared with the theoretical success rate if crows chose randomly (33.33%) with a normal approximation of the binomial.

Numerosity

Subjects that were shown to significantly select the correct shape bowl were subsequently tested in a numerosity experiment. This involved presented the subject bird with the same bowls but this time with a varying number of dots on the inverted base instead of a shape. Four bowls were used in total, with only two being presented during any particular trial. These bowls were marked with 2, 3, 4 and 5 dots, in the arrangement of pits on a die (Fig. 6.2). Initially, mince balls were placed under the larger of the two numbers, but these were later replaced with chicken eggs due to excessive interference by butcherbirds (Cracticus spp). As crows had already been trained to interact with bowls, the training process for the numerosity experiments were much shorter, typically lasting approximately one week.

The four quantities resulted in six combinations of two presentations, which were each offered to a territorial pair five times, giving a total of 30 trials per site. Researchers again retreated to a distance of over 20m or left the area. Again Acorn Ltl-5210 game cameras recorded the interactions in these cases. The trial was considered a success if the crow flipped over the bowl with the larger number of dots, and a failure this did not occur. The total proportion of successes for each site was compared to a random 50% success rate with a normal approximation of the binomial, before Weber’s Law was tested by correlating the ratio between the two numbers presented and the probability of success.

112

4m 4m 4m 4m 4m 4m

Figure 6.2 Each of the 6 possible combinations of quantities that crows were presented with (not to scale)

Data analysis

For the shape discrimination test, rates of success for each site were compared to the success rate that would be achieved by randomly choosing bowls: a 33.33% baseline. To demonstrate that crows were succeeding at a rate significantly higher than random chance, success was compared to this baseline in SAS 9.4 through use of a one-tailed binomial procedure for each site independently. This was repeated for each of the sites in which the numerosity test was conducted with a baseline of 50%, owing to the presence of only two bowls at a time. Finally, to investigate the influcnece of Weber’s Law, where the ratio between quantities correlates with the ability to distinguish them, the data was tested for correlations between the ratio between the two numbers presented (Table 6.1) and the probability of success. This was conducted through use of a logistic regression, also in SAS 9.4.

Table 6.1 Ratios between quantities presented to crows Quantities 2, 3 2, 4 2, 5 3, 4 3, 5 4, 5 presented Ratio 1.5 2 2.5 1.33 1.66 1.25

113 Results

Shape discrimination

A total of 100 trials were conducted within five sedentary crow territories. All crows were territorial breeding adults although at one site two juveniles were also present. Only adult interactions were recorded as juveniles appeared to be more curious of all objects around them than trying to attain a reward.

Three crow pairs significantly preferred the cross to the triangle and circle. Crows at Site A chose the crossed bowl a total of 17 out of 20 trials (Z = 4.9015, p<0.0001), as did the crows at site D (Z = 4.9015, p<0.0001). The crows at Site B were also successful in discriminating between correctly chose in 12 out of 20 trials (Z = 2.9258, p<0.01). Alternatively, crows at the two other sites appeared to choose bowls at random, with Site C choosing correctly 7 of 20 times (Z = 0.1581, p=0.3759) and E being successful in 6 of 20 trials (Z = -0.3162, 0.4372) (Fig. 6.3).

100%

90% * * 80%

70%

60% *

50%

% Success 40%

30%

20%

10%

0% A B C D E Site

Figure 6.3 Success of subject crows in shape discrimination experiment. A, B and D were significantly more successful (*) than random chance (dotted line).

114 Numerosity

Although successful in the shape discrimination task, crows at site D were not able to be tested in numerosity as the site became inaccessible between experimentations. Neither of the crows at Site A (Z=1.4606, p=0.0721) or Site B (Z=1.0954, p=0.1367) significantly preferred the bowl with the larger number of dots. There was also no greater probability of crows choosing the correct bowl with a greater ratio between the number of dots on the two available bowls (χ²=0.684, p=0.7103).

Discussion

In these experiments, wild Torresian crows were shown to be able to successfully learn an arbitrary shape and associate this with a food reward, with relatively little intensive training and an abundance of non-experimental food to distract them from the task. Three of the five crow pairs were successful in the shape discrimination task: two in suburbia and one in a forested university campus. Of the two pairs that were not successful, observations appeared to indicate that environmental distractions were a main reason for their failure to perform the task. Crows at Site C were accompanied by two fledglings who were constantly begging for food, while those at Site E were forced to compete with pied butcherbirds (Cracticus nigrogularis), pied currawongs (Strepera graculina) and an aggressive male Australian brush-turkey (Alectura lathami) to reach the experimental site after baiting, along with the presence of laughing kookaburras (Dacelo novaeguineae) that swooped on any bird that had attained the food offering. It was highly likely that these influences significantly disrupted the crow’s attempts to obtain the food as quickly as possible, minimising opportunities for thought or learning.

In contrast, little evidence of a concept of numerosity was detected in wild Torresian crows. The subject birds were not distracted by outside influences at either site, readily approaching the bowls with little competition from heterospecifics. Even though the tendency of crows at Site A to choose the greater number approached significance, choosing the correct bowl 63% of the time is not indicative of an understanding of the task. Although an Australian magpie did compete with the crows at Site A, which had the potential to rush crows into deciding before thinking the problem through. However, there appeared to be no urgency by the subjects to attain the bait compared to the rest of the

115 trial. To investigate whether a greater sample size or longer training would increase the chances of success, a further 15 trials were conducted on crows at Site B, though no increase in success rate was witnessed.

Torresian crows are capable of learning to associate arbitrary shapes with a food reward and discriminate between this and other shapes. However, in the wild, these processes can be subsumed if haste is required, e.g. intense competition from heterospecifics, in which case crows dismiss their learning and choose randomly until the reward is attained. This suggests that the process of recognition and association takes time to occur, time that is not always available in the highly-competitive urban environment.

Corvids in other countries have been well established as being highly-intelligent and capable of complex problem-solving (Emery 2004, 2006, Clayton and Emery 2005, Seed et al. 2009). Here, we investigated an understudied Australian corvid in the wild using experimentation techniques adapted from those used on captive subjects. Establishing the ability to recognise and discriminate between arbitrary shapes is a significant foundation for studies investigating same-difference and concept formulation in animals. Wild Torresian crows have been shown to be capable of this if they are not hampered by competitors or begging juveniles. This associative learning raises the prospects for further investigations similar to that of Bogale and Sugita (2014) and Smirnova et al. (2000).

This study provides an example of the advantages that can be attained with controlled, laboratory experiments where environmental distractions and access to food can be limited by the researcher. The inability to deny crows a food reward if they chose the incorrect bowl likely impeded learning significantly. Despite this, crows were able to learn to associate a drawn shape with a food reward, and reliably choose that shape over others, with no other cues such as consistent placement or viewing the baiting of bowls.

This study cannot entirely rule out the possibility that smell played a part in the crow’s choice of a bowl, though it appears unlikely for a number of reasons. From observation, Torresian crows appear to be a predominantly visual predator and scavenger, detecting carrion or anthropogenic foods from high perches, only potentially using smell while foraging at close quarters. Additionally, crows did not visit bowls before choosing one to flip. The vast majority of trials involved crows swooping down from high perches either in the

116 middle of the experimental triangle or next to the bowl that they had chosen. Finally, numerous studies of little ravens, a closely related species, noted sight as being the dominant method of hunting (Ekanayake 2015, Ekanayake et al. 2016). It appears unlikely that Torresian crows were utilising any method other than sight to participate in the study.

The methodology used in this study may potentially be of more use if there were a way to deny access to the bait after the bird has made its choice, as was done in previous laboratory studies (e.g., Bogale et al. 2011, Bogale and Sugita 2014). Such a method would likely increase the rate of both learning and data gathering. In addition, this study focussed on territorial adults as it allowed for analyses of birds known to be statistically independent. An investigation using the same methods in less-neophobic juvenile groups, while a statistical challenge, would be of great interest in determining the speed of learning in juvenile crows while also having the potential to study social learning. Such an experiment would likely involve a high degree of trapping and banding, which would greatly increase the difficulty of such as study (see Chapter 4).

117 Responses of wild Torresian crows (Corvus orru) and other corvoids to their own reflection in an urban environment

Abstract

Species that have adapted to live in the suburban environment surrounding the world’s cities tend to have similar traits, both physiological and behavioural. Mirror-image stimulation (MIS) has long been used to ascertain levels of aggression or other behaviours in birds and other species, often in a controlled laboratory setting. In this study the responses of an Australian corvid, the Torresian crow (Corvus orru), and other suburban birds were documented in the city of Brisbane. Torresian crows’ behaviour was significantly affected by the presence of a mirror, and these behaviours were relatively consistent between individuals. Crows also behaved similarly to a number of other suburban birds, including the native Australian magpie (Cracticus tibicen) and pied currawong (Strepera graculina) as well as the invasive common myna (Acridotheres tristis) and spotted dove (Spilopelia chinensis), while the Australian magpie and the spotted dove also reacted similarly. All other studied species reacted in a dissimilar way to each other. Of all species, the grey butcherbird (Cracticus torquatus) interacted most with the mirror non-aggressively, suggesting that this group may be of interest in further investigations of MIS and MSR in Australia.

Introduction

Investigating Mirror-Image Stimulation

Scientific investigations into higher cognition in animals has been conducted in a variety of ways. One such method, the mirror test developed by Gallup (1968), involves placing a mirror in front of an animal and observing the changes in behaviour (Svendsen and Armitage 1973) and is thought to enable the assessment of self-consciousness in animals (Mitchell 1993). While the value of this test has been questioned by some (e.g., Gallup and Povinelli 1993, Mitchell 1993, 1997, De Veer and Van den Bos 1999), the test remains widely used (Bekoff and Sherman 2004) and is useful in producing comparable data between

118 species has enabled researchers to compare the behaviours a variety of species, such as apes, elephants, dolphins and birds (Cohen and Looney 1973, Marino et al. 1994, Walraven et al. 1995, Pepperberg et al. 1995, Prior et al. 2008, Broom et al. 2009, Rajala et al. 2010, Medina et al. 2011).

Studies on mirror self-recognition in birds have included studies of at least fourteen species, none of which have yielded results indicating self-recognition, with the exception of Prior et al.’s (2008) study on the Eurasian magpie (Pica pica) a Corvid. Mirror Image Stimulation (MIS) is often used to assess aggression, as the viewing of their reflection may be treated as a visual confrontation with a conspecific (Svendsen and Armitage 1973, Gallup 1968). Failure to treat the mirror image as their own reflection usually results in the subject displaying aggressive behaviours. While the studies on mirror self-recognition in birds are numerous, they have entirely taken place on captive individuals in an artificial environment. An extension upon these studies would be to conduct similar methods on wild individuals in a complex environment, such as suburbia.

Urbanisation

Urbanisation has had a significant impact on animal diversity and abundance on Australia’s East coast (Parsons et al. 2003). While species are often categorised as either ‘urban avoiders’ that decline with urbanisation and ‘urban exploiters’ that thrive in cities (e.g., Shochat et al. 2006, Kark et al. 2007), many native and non-native species live in the areas of intermediate urbanisation that surround most cities, becoming ‘suburban adapters’ (Kark et al. 2007). In one of the most urbanised countries in the world (Atkins et al. 2015), it is these species with which most Australians interact with in their daily lives (Ryan 2007). Though many such species are invasive generalists such as pigeons and rats (Warne et al. 2010), there is a growing recognition that a considerable number of native species have adapted to become successful in our cities (Jones 2003, Clucas et al. 2015).

Some researchers have suggested there are a number of inherent traits that increase a species’ likelihood to thrive in urban habitats (Bonier et al. 2007b) or adapt to disturbance (Conomy et al. 1998, Evans et al. 2010). Urban communities tend to be dominated by sedentary species territorial species which may force out migratory competitors (Jokimäki and Suhonen 1998, Kark et al. 2007, Lim and Sodhi 2004). The high populations of birds and

119 the diverse habitat in the suburban environment has favoured those species that are highly- territorial. These trends are evident in the Australian city of Brisbane.

Suburban adapters in Brisbane

Brisbane is a subtropical, mostly suburban city with a population of 2.45 million people (ABS 2015). Significant population growth in the early 21st Century has resulted in significant areas of forest cleared for urbanisation (Ryan 2007). Its warm climate and abundance of watered lawns have resulted in both an abundant and diverse avian community, with 50 species living within 15km of the Central Business District (Green et al. 1989, Rollinson et al. 2003, FitzGibbon and Jones 2006, Ryan 2007). Loss of natural habitat due to anthropogenic land use changes have caused significant changes to these bird assemblages, according to historical records (Sewell and Catterall 1998). The city’s urban avifauna remains quite distinct from that of Northern Hemisphere cities, being dominated by parrots, honeyeaters, cracticids and ibises (Ryan 2007, Sewell and Catterall 1998, Green et al. 1989). Of most interest to this study is the Torresian crow, a native Australian corvid.

Torresian crows are a generalist species and are fiercely territorial during adulthood (Rowley 1970, 1973a). The species is most well-known in Brisbane for its tendency to form large urban roosts, and to steal food from local people and businesses in enterprising ways (M. Brown pers. obs.; P. Hemmadi pers. comm.; D. Jones pers. comm). Brisbane also houses a variety of other Corvoids, including the Australian magpie (Cracticus tibicen), grey butcherbird (Cracticus torquatus), pied currawong (Strepera graculina), and magpie-lark ( cyanoleuca). Additionally, several non-corvoid birds were investigated, all of which are commonly found in Brisbane’s environs (Table 7.1).

Table 7.1 Social and territorial aspects of suburban bird species in Brisdbane relevant to this study (Marchant and Higgins 1993, Higgins and Davies 1996, Higgins 1999, Higgins et al. 2006a, b, Sinden 2002, Brown 2011, Blakers et al. 1984) Species Defence of territory Social structure Torresian crow Aggressively defend their territories Live in sedentary pairs as adults, (Corvus orru) from conspecifics. Conflict is usually are social during adolescence vocal and rarely reaches physical and for night roosting. contact.

120 Australian magpie Highly aggressive, physically defend Generally live as breeding pairs (Cracticus tibicen) territory from conspecifics. Will prey on or in family groups, can be found smaller birds. in flocks of 12-20 birds. Grey butcherbird Highly aggressive, physically defend Usually found alone or in pairs. (Cracticus their territory from conspecifics. Will torquatus) prey on smaller birds. Pied currawong Territorial while breeding, defended by Usually found alone or in pairs, (Strepera male. can be found in large flocks in graculina) winter. Magpie-lark Aggressively territorial. Sedentary, usually found in pairs. (Grallina cyanoleuca) Australian brush Male aggressively defends mound. Solitary. turkey (Alectura lathami) Common Myna Family groups defend territory from Usually found in large flocks. (Acridotheres conspecifics and heterospecifics. tristis) Crested pigeon Highly aggressive, will attack and kills Breeds in pairs but often forage (Ocyphaps other birds on sight. in large flocks. lophotes) Spotted dove Non-territorial. Usually found in large flocks. (Spilopelia Rarely found away from humans. chinensis)

Aims

To extend upon previous studies into MIS, a comparative study was conducted on suburban birds in Brisbane to establish fundamental trends of behaviour in response to mirrors. The study aimed to determine the extent to which the presence of mirrors affected Torresian crow behaviour, and whether these behaviours would be self-directed like Prior’s (1997) magpies, or aggressive (as Kusayama et al. (2000) found in jungle crows). Finally, the behaviours of a variety of suburban avian species were compared in the context of their sociality and tendency to defend their territory against conspecifics. Species that actively

121 defend their territories against conspecifics were deemed more likely to respond aggressively towards their reflection.

Methods

Study sites and field work

Mirrors were placed at seven separate sites (A, C, D, E, F, G, H; see Chapter 2) located throughout southern Brisbane with the intent of documenting the behaviours of territorial Torresian crows and other suburban species. Five sites were located at Griffith University’s Nathan Campus situated in the dry eucalypt remnant of Toohey Forest, while the other three were located in accessible yards on private properties in low-density suburbia. Due to inconsistencies in the frequency of crows approaching the mirrors, crows were only recorded adequately at five of these sites.

Two mirror sizes were used in this study, determined by accessibility to the site and the space available. A 21cm x 30cm mirror was used at two sites due to space restrictions, while at all other sites a 30cm x 120cm mirror was used. Mirrors were originally placed to stand independently to allow crows to view the back of the mirror as was implemented by Medina et al. (2011). However, the resulting object created a significant neophobic reaction in crows, making it impossible to obtain any data. This was solved by placing the mirror in a landscape orientation along a vertical wall, fence or log, which greatly reduced the neophobic reaction, though this prevented crows from viewing the back of the mirror in a similar way to Prior et al.’s (2008) experiment.

Mirrors were deployed for one to four months between February 2014 and December 2015, and were baited daily with frozen raw beef mince, hard-boiled chicken eggs and low-quality bird seed. This maximised the time bait would last before spoiling. Behaviour was recorded by Ltl-5210A cameras fastened to a tree or other background object to minimise novelty 3- 4m from the mirror at a 45° angle. Cameras were set to record 30 seconds of footage upon sensing motion.

At Site A, the most successful site where crows readily approached the mirror, the mirror was faced towards the wall for a period of two weeks, displaying its non-reflective back. This was intended to act as a control experiment.

122 Behaviour categorisation

Video recordings were selected with videos displaying longer periods of behaviour prioritised over videos where a bird was only visible for a few seconds. A sample of five minutes of footage was randomly selected of each species, with 25min from five sites selected for crows (Sites A, C, D, E, G). Other sites did not produce enough footage of crows for analysis. From a previous categorisation exercise (described in Chapter 4), a large proportion of the video recordings were simply of the bird eating the bait, while aggression towards the mirror was also a common behaviour. Behaviour in this footage sample were then categorised into four states: aggressively interacting with the mirror, non-aggressively interacting with the mirror, foraging, and other behaviours (Table 7.1; Appendix V). The times at which birds were exhibited each of these behavioural states were noted by the scorers. These categories were considered sufficient to give a general overview of the behaviours of all species, as a more detailed coding system was found to produce far too much noise to perceive relevant patterns in the data (Chapter 4). While there were set definitions for each of these states, categorising bird behaviour viewed on a computer screen is at the end of the day a subjective procedure and therefore possibly subject to bias or other factors that may reduce the reliability of the data produced. In other studies (e.g., Prior et al. 2008, Medina et al. 2011) involving such qualitative data, several independent scorers have been used to ensure that the resulting quantitative data is agreeable. In light of this, videos were categorised in this study by seven independent scorers who had no communication with each other while scoring the behaviours. To determine whether the declared behaviours by each of these scorers were accurate, these were tested for agreeability.

Table 7.2 Examples of behavioural states typical of the four categories

Interacting with the mirror Not interacting with the mirror

Aggressive Non-aggressive Foraging Other Aggressive displays Investigating mirror Pecking food Walking Attacks Lightly tapping mirror Swallowing food Taking off Hard pecks Looking behind mirror Searching for food Interacting with other Charges bird Sitting Singing

123

Testing for agreeability

To assess agreeability between scorers, combinations were tested through use of a binary Sorensen’s Index. With seven scorers, 21 binary combinations were each tested individually for each of the 160 videos sampled. Each second of each video was sorted into one of four categories (both scorers agree on behaviour, disagree on behaviour, only one scorer noting bird behaviour, neither scorer noting bird behaviour). The first of these two categories were used to calculate the total Sorensen’s Index for each video. Times for that 30 second video recording that were incorrectly completed by one or both scorers (e.g., no behaviours recorded or two behaviours recorded for the same time periods) were not assessed. After this was completed, each video was associated with a possible 21 Sorensen’s Indices. Those videos for which less than half of these indices were above 0.7 were removed, as were those which had less than 10 indices. These videos were determined to be inconsistently categorised by scorers, requiring removal from the dataset.

Data analysis

After removal of videos which failed to meet the criteria stated above, data for each scorer was summed for each species (or site, for Torresian crows), allowing data to be compared between species. Differences in the relative proportions of mirror- and food-directed behaviours expressed by crows between the mirror treatment and the non-reflective surface at Site A were compared through a χ2 Test of Independence in Microsoft Excel. Differences in the total time spent interacting with the mirror, being aggressive and foraging were all tested. These behavioural states were correlated, as they were measured as a proportion of time in front of the mirror. Any increase in one resulted in a decrease in others. Site A was chosen as it contained the crows that were by far the most ready to approach the mirror, allowing control data to be reliably gathered. Data depicting the time the crows at Site A spent in each behavioural state when the mirror was facing outwards or towards the wall as determined by each scorer was then imported into Primer 6, where it was standardised and transferred into a Bray-Curtis Resemblance Matrix for multivariate analysis. Firstly, the results of the χ2 analysis was checked through use of a Principal Components Analysis of the Resemblance Matrix with 5 Principal Components,

124 supplemented by a dendogram of Bray-Curtis Similarity, to help distinguish trends in the crow behaviour. Each scorer’s data on crows in either the treatment or control state was considered an individual datapoint for the purpose of comparison. Principal Components Analysis were utilised in this scenario in order to more clearly establish the behaviours that were driving the observable trends.

Scorers’ depictions of crow behaviour in front of mirrors across the five sites were then imported separately into Primer, at which point the standardisation and transfer into a resemblance matrix was repeated. The consistency in Torresian crow behaviours across sites was also compared through a Principal Components Analysis supplemented by a dendogram of Bray-Curtis Similarity. Finally, data of crow behaviours at each site, along with data of each of the other species, was imported into Primer as one dataset. This was then treated as the other two datasets before the differences in behaviour between species were assessed with a Multi-Dimensional Scaling (25 permutations) supplemented by a dendogram of Bray- Curtis Similarity, and tested with an Analysis of Similarity (999 permutations). In this analysis, data was divided along species lines. Given the intentions of viewing trends across a large set of data and comparing species statistically, and MDS was deemed the most appropriate method of investigating and establishing trends.

Results

In total, birds were recorded in a total of 2805 videos, and while this is equal to a maximum of 10.5 hours of footage, very few videos had birds present for the entire 30 seconds. Approximately half of these videos involved Torresian crows (Chapter 4). Samples were then retrieved from this dataset and categorised by seven independent scorers before the states noted by scorers were compared. A total of 2536 of 3357 (75.5%) Sorensen’s Indices were above the chosen cut-off point of 0.7, resulting in a total of 44 of 302 (25.4%) videos being removed from the dataset (Appendix VI).

When comparing treatment and control footage of the Torresian crows at Site A scorers agreed unanimously that the presence of a reflective surface significantly affected Torresian crow behaviour (df=3, x2=108.7, p<0.0001). Crows displayed higher levels of aggression and interacted with the mirror more when the reflective surface was faced towards them (Fig. 7.1). These trends were confirmed by a Principal Components Analysis (Fig. 7.2).

125 1000

100

10 Time Time in recording (sec)

1 Interacting with mirror Interacting with mirror Foraging Other aggressively non-aggressively Behavioural state

Non-reflective Reflective

Figure 7.1 Behaviours of Torresian crows at Site A. The existence of a reflective surface results in a significant shift in behaviour.

Figure 7.2 Principal Component Analysis of Torresian crows at Site A shows the existence of a reflective surface affects crow behaviour in a generally agreed-upon way.

126 Between sites, there was widespread agreement between scorers that crows at Sites C and G behaved in a dissimilar way to the other three sites (Fig. 7.3). Crows at site G spent a greater proportion of their time in front of the mirror ignoring both the mirror and the bait, while those at Site C interacted with the mirror in a non-aggressive manner to a much greater extent than the other sites (Fig. 7.3). Other than this, behaviours were relatively similar between sites, with a similarity of over 70% (Fig. 7.3).

150 Site A C Other D 100 E G Similarity 70 50

2 Aggressive C

P

0 Non-Aggressive

Foraging -50

-100 -100 -50 0 50 100 150 200 PC1

Figure 7.3 Principal Components Analysis of Torresian crow behaviours when presented with mirrors. With the exception of two sites, crow responses to the reflective were consistent with a similarity of 70%.

Through the ANOSIM, the behaviour of Torresian crows was found to be dissimilar from that of all species other than its fellow corvoids the Australian magpie (R=-0.079, p=0.73) and pied currawong (R=-0.069, p=0.70), as well as the spotted dove (R=-0.044, p=0.58) and common myna (R=-0.232, p=0.99), while magpies were not found to be significantly dissimilar from the spotted doves (R=0.013, p=0.30). All other pairs of species were found to be significantly dissimilar in their behaviours when presented with a mirror (p<0.05) (Table 7.3, Fig. 7.4). There was high agreeability of behaviours of all species, with the exception of grey butcherbirds, which were far more spread out than other species, with a common

127 theme that they were more likely to interact with the mirror in a non-aggressive way than any other species.

Table 7.3 Comparative table of R-statistics and p-values from ANOSIM test in Primer 6. The analysis found dissimilarity in behaviour was strong between most species. Full ANOSIM table is available in Appendix VII.

SPOTTED CRESTED BRUSH COMMON MAGPIE- PIED GREY AUSTRALIAN DOVE PIGEON TURKEY MYNA LARK CURRAWONG BUTCHERBIRD MAGPIE

TORRESIAN R -0.044 0.979 0.343 -0.232 0.637 -0.069 0.626 -0.079 CROW p 0.579 0.001 0.001 0.99 0.001 0.7 0.001 0.73 AUSTRALIAN R 0.013 1 0.887 0.407 1 0.707 0.914 MAGPIE p 0.307 0.003 0.001 0.005 0.002 0.001 0.001 GREY R 0.832 0.959 0.738 0.877 0.96 0.584 BUTCHERBIRD p 0.001 0.001 0.001 0.002 0.001 0.003 PIED R 0.646 1 0.853 0.342 0.96 CURRAWONG p 0.008 0.002 0.001 0.002 0.001 MAGPIE-LARK R 1 0.911 1 1 p 0.003 0.001 0.002 0.001 COMMON R 0.587 1 1 MYNA p 0.001 0.001 0.002 BRUSH R 0.716 1 TURKEY p 0.001 0.001 CRESTED R 1 PIGEON p 0.002

Figure 7.4 MDS ordination of behaviours of suburban Brisbane birds when presented with mirrors. This 2- dimmensional representation of a multi-dimensional analysis groups classifications of behaviour based on spatially based on their proximity. The representation shows a strong that behaviours of Australian magpies, spotted doves, Torresian crows and pied currawongs are generally more than 70% similar, while behaviour of other species are generally consistent.

128

Discussion

In this study we have been able to produce a highly agreeable dataset of the reactions of the behaviours Brisbane’s suburban bird species display when confronted with their own reflection. These species belong to a wide array of taxa and niches, including columbids, corvids, butcherbirds, turkeys and flycatchers. Of the species studied, all but two were native to the Brisbane region. These native Australian species behaved in a highly variable way to the Mirror Image Stimulation. The two invasive species, the common myna and spotted turtle dove, have a historical relationship with humans in an urban setting, while the native species have formed this relationship far more recently. Meanwhile, several of these species aggressively defend their territories from conspecifics.

The behaviour of wild Torresian crows was significantly affected by the presence of the mirror. Their behaviours towards the mirror were both aggressive and non-aggressive, and included birds looking behind the mirror, manipulating its sides or staring at its own reflection. Behaviours of Torresian crows were generally consistent between sites, with only two of the five sites (Sites C and G) generally lying outside the main group in the multi- dimensional scaling.

Torresian crows reacted to the mirror in a very similar way to the two invasive species in this study, with an analysis of similarity unable to differ between them. The behaviour of Australian magpies, another common urban Australian species, was also similar to spotted turtle-doves. The two columbids, crested pigeons and spotted turtle doves, were at complete opposite ends of the ordination (Fig. 7.4). Spotted turtle doves rarely reacted to the mirror at all, while crested pigeons almost entirely reacted in an aggressive fashion. Meanwhile, grey butcherbirds interacted non-aggressively with the mirror to a much greater extent than any other species studied. Taking this into account, this species may be an excellent candidate for any future investigations in mirror self-recognition into an Australian species.

Adult Torresian crows and Australian magpies are aggressively territorial, with birds swooping and even striking each other is not uncommon (M. Brown pers. obs.). Therefore, the sight of a conspecific that was not the bird’s mate or offspring should have resulted in a

129 conspicuous reaction. Instead, magpies barely reacted at all to the mirror and crows reacted mostly with apparent fear. There are several possible explanations for these observations. One is that the birds did not consider the shape moving in the reflective surface to be a bird. This seems unlikely given the large literature focusing on Mirror-Image Stimulation and Mirror Self-Recognition, as well as the predictably-aggressive reactions of magpie-larks and crested pigeons. It is possible that the birds had had previous experience with vertical reflective surfaces, possibly highly reflective building windows or car mirrors, allowing them to learn that this stimulus is not a threat. Conversely, the crows at Site D and at Site E originally responded to the mirror with fear, suggesting that this stimulus may have been novel. Alternatively, they may have viewed the mirror image as a conspecific but due to the similarity with themselves, may have viewed it as a non-threat. This explanation is unlikely at least for Torresian crows, as the only other adult with which a sedentary adult shares its territory is its mate. Adolescent magpies that may be helpers at the nest are less obvious to humans than juvenile crows in their parents’ territory, but it seems likely that an adult magpie would easily be able to tell the difference between its own young and an adult that is not its mate. Alternatively, it is possible that these birds know what their competitors look like, and only consider them as threats. Quite often territorial Torresian crows will allow other crows to pass over their territories while travelling (M. Brown pers. obs.). Finally, it is possible that these birds understood that the mirror was a reflection of themselves, and therefore did not bother interacting with it for the most part. If this was the case, further experimentation under more controlled conditions would be required in order to assess this, perhaps with a mirror mark test.

The experimental design of this study excluded a number of successful urban bird species, due to the location of the mirrors on the ground and the carnivore-specific bait used. Intelligent parrots such as cockatoos (Kaplan 2015) may have possibly engaged in the experiment if additional mirrors were located on perches and if other foods were used as bait. This, along with the inclusion of nectar-based bait, may have incorporated some of Brisbane’s wide variety of honeyeaters, including the dominant noisy miner, one of the most common birds in Brisbane (Catterall et al. 2010, Ryan 2007). Kaplan (2015) noted that parrots were some of the best candidates for studying interesting behaviours in the Australian avifauna, while Low (2014) singles out Australia’s honeyeaters as a distinguishing

130 taxa of the continent. Including these species in any future investigations would certainly be of interest.

This study has shown that recording MIS in the wild suburban environment is possible. However, the process of recording sufficient footage at several independent locations is particularly resource-intensive. Furthermore, it is impossible to target one particular species and the resulting data must either be broad or noisy. While data between scorers was correlated, the classification of behaviours remained subjective. More defined categories may have produced more empirical results, but also may have simply created so much noise that no obvious patterns could be discerned, as occurred in a preliminary trial of categorisation (See Chapter 4).

Torresian crows’ behaviour is significantly affected by the presence of a reflected surface, with these behaviours being relatively consistent and predictable. Three native corvoids: Torresian crows, Australian magpies and pied currawongs, interact with the mirror in a similar way to the two invasive species studied. Meanwhile, grey butcherbirds reacted in a dissimilar way, interacting with the mirror to a much greater extent than other species in a non-aggressive way. Other species appeared to respond to the mirror in a dissimilar fashion to Torresian crows.

131 Discriminatory string-pulling in wild Torresian crows (Corvus orru) and pied butcherbirds (Cracticus nigrogularis) in a suburban environment

Abstract

Corvids (Family: Corvidae) are a group of considerable interest to students of animal intelligence. One test that has been extremely common in birds has been the string-pulling test, which has been used to investigate both insight and an understanding of causality. These tests have been conducted exclusively in a controlled laboratory environment, and on Holarctic species. In Australia, the Corvidae are represented by just five species of Corvus, although the continent is also home to a wide variety of corvoids, including the extremely common butcherbirds (Cracticus spp). In this study we investigated the ability of wild Torresian crows (Corvus orru) and pied butcherbirds (Cracticus nigrogularis) to discriminate between two parallel horizontal strings in order to receive a food reward. These strings were then crossed, to help determine the processes which birds were using to make their choices. Two of the four crow pairs tested significantly preferred the correct string while parallel, while none were able to succeed in the test when the strings were crossed. Meanwhile, pied butcherbirds succeeded in both the parallel and crossed experiments, suggesting that they could follow the continuity between the string and the food reward while crows did not.

Introduction

String pulling and insight in birds

After many decades of investigations into how non-human animals interact with and perceive their environment (Beck 1980), it is now the opinion of many researchers that a number of large-brained animals are able to confer a causal relationship between two events (Werdenich and Huber 2006). The currently accepted hypothesis, that language accelerates but is not a prerequisite of causal understanding, is contrary to previously accepted concepts in animal learning (Rumbaugh et al. 2000). Causal understanding may be

132 attained through either observation (learned) or insight (spontaneous), and involves establishing cause-effect relationships between two objects or events (Werdenich & Huber 2006). One well-established technique used to investigate spontaneous problem-solving in birds is the string-pulling experiment (e.g., Vince 1958), which relies on the subject’s understanding of the relationship between the pulling of a string in one location and an action in another location (the food moving towards them).

To successfully pass a vertical string-pulling test, subject birds must perfectly repeat a 6- stage process of reaching down, pulling the string and trapping it with their foot at least five times in order to obtain the food (Heinrich 1995b, Heinrich and Bugnyar 2005). While string pulling has been described in more than ten avian species (Vince 1958, Dücker and Rensch 1977, Seibt and Wickler 2006), subsequent studies revealed that the string-pulling abilities in many of these species was only learned when the food was initially placed directly under the perch and lowered over time (i.e., a learned behaviour, not an insightful one) (Heinrich 1995a, Taylor et al. 2010b).

Some corvids (Taylor et al. 2010b, Heinrich 1995a, Heinrich and Bugnyar 2005) and psittacids (Pepperberg 2004, Werdenich and Huber 2006, Schuck-Paim et al. 2009) have been shown to be capable of spontaneously pulling up a food reward attached to a string and hanging from a branch. While other birds have been able to solve the problem, the promptness in which corvids and parrots solving the problem without the need for intermediate, learned steps stands these groups apart from other avifauna in these studies. As such, many authors have proposed success in this experiment as evidence of insight in these species (Taylor et al. 2012b, Heinrich 1995a, 2000, Pepperberg 2004). On the other hand, Taylor et al. (2012b) brought the insight hypothesis into doubt by showing that New Caledonian crows (Corvus moneduloides) – a species celebrated for their remarkable cognitive abilities (Hunt 2000b, Weir et al. 2002, Hunt and Gray 2004, Taylor et al. 2010b, Taylor et al. 2010a, Taylor et al. 2012c, St Clair and Rutz 2013, Jelbert et al. 2014) – failed the vertical string-pulling test when they were not able to view the bait moving up due to their efforts.

Heinrich (1995a) originally investigated string pulling in wild-captured adult common ravens (Corvus corax), which were able to solve the challenge without the need for a learning process, suggesting insight was the most likely explanation. The complexity of the task and

133 the absence of similar circumstances in the wild also ruled out the possibility of chance or genetic programming as possible explanations. This experiment was revisited in 2005 (Heinrich and Bugnyar 2005) with the inclusion of a familiarisation process to reduce the impact of neophobia, and with an additional counter-intuitive test where ravens were required to pull the string down in order for the food to move up. Subjects familiar with the conventional string-pulling task were able to transfer their learned skills to the novel problem while naïve birds failed, leading the researchers to assert that this was evidence for the birds’ understanding of the causal relationship between pulling the string and the reward becoming accessible (Heinrich and Bugnyar 2005). Conversely, Taylor et al. (2010b) suggested that the failure of naïve birds was evidence that ravens were using a perpetual- motor feedback cycle to solve the problem that relied on seeing that their actions were having a desirable impact on the apparatus (i.e., bringing the food closer). This feedback may increase motivation to continue with the task, without which the ravens would simply lose interest or try another method regardless of their insightful abilities (Taylor et al. 2010b). This hypothesis was supported when New Caledonian crows failed to solve the task when their view of the sting was blocked (Taylor et al. 2012b). Heinrich (1995a) also attempted to test wild ravens with the string but the birds did not participate, instead making alarm calls and avoiding the area. Fearfulness, likely caused by neophobia, was suggested as an explanation for this behaviour (Heinrich 1995a).

Discriminatory string pulling

While string-pulling has been instrumental in investigating insight in birds, more recent studies have focussed on string discrimination (Heinrich 2000, Werdenich and Huber 2006, Taylor et al. 2010b, Pfuhl 2012). Providing two choices allows for targeted testing of the cognitive processes behind string-pulling: whether birds are pulling the string as a conscious means to an end (in this case a food reward) and whether birds can visually trace the continuity between the accessible section of string and the food reward in order to predict the effect of pulling the string on the location of the food (Schuck-Paim et al. 2009). Ravens and keas (Nestor notabilis) were able to discriminate between two parallel strings, be they vertical or slanted (Heinrich 2000, Werdenich and Huber 2006, Taylor et al. 2010b). Although, when they were crossed only one raven (Heinrich 2000) and no New Caledonian crows (Taylor et al. 2010b) were able to successfully discriminate between strings, while a

134 majority of tested keas chose the correct string, although this was reduced when the strings were of different colours (Werdenich and Huber 2006).

Taylor et al. (2010b) added a new dimension to the string-pulling experiment by including object discrimination, weight discrimination and string continuity tests with New Caledonian crows. These experiments included slanted and crossed strings to determine whether subjects could comprehend the causal relationship between them pulling the string and the bait approaching them, or whether they were simply pulling the string above the food. While success rates for almost all experiments were high, the low success rates in the crossed-string test and a gradual increase in success over time led Taylor et al. (2010b) to conclude that success was attained via learning, not insight. However, Taylor et al. (2010b) admitted that their small sample sizes (N=4) may have hampered their investigation.

Corvids

Corvids are a group of some 120 species of highly-encephalised (Goodwin 1976) that have become a group of significant interest to students of animal cognition due to their exemplary results in cognitive experiments (Angell and Marzluff 2005, Clayton and Emery 2005). Recent studies in self-recognition (Kusayama et al. 2000, Prior et al. 2008, Medina et al. 2011), tool-use (Montevecchi 1978, Hunt 2000b, a, Caffrey 2000, 2001, Weir et al. 2002, Bluff et al. 2007, Balda 2007, Bird and Emery 2009a, Wimpenny et al. 2009, Mehlhorn et al. 2010), social learning (Templeton et al. 1999b, Holzhaider et al. 2010), cultural evolution (Marzluff and Angell 2005, Marzluff et al. 2010), imagination (Heinrich 1995a, Bird and Emery 2009a), cooperation (Bossema and Benus 1985, Seed et al. 2008) and memory (Kamil and Balda 1990, Balda and Kamil 2002, Clayton et al. 2007, Marzluff et al. 2010) have made the corvids a poster group for avian cognition both in the scientific community and the general public.

While corvids are generally regarded as being well-studied, the vast majority of research is derived from a small number of species, all but one from the Northern Hemisphere (see Chapter 3). While this is the case, there is significant potential for large gaps in our knowledge to persist. Although Australia and the Papuan region are now recognised as the cradle of the passerines and the corvoids (Jønsson et al. 2011, Jønsson et al. 2016, Low 2014, Kaplan 2015), our knowledge of the cognitive abilities of the birds from this region is

135 sparse to non-existent. An investigation into learning and concept formulation in an Australian corvid will add an important piece to the puzzle of corvid cognition. The Corvidae are represented in Australia by five species of Corvus, the Australian raven (C. coronoides), little raven (C. mellori), forest raven (C. tasmanicus), little crow (C. bennetti) and Torresian crow (Corvus orru) (Rowley 1970, Debus 1996, Christidis and Boles 2008).

Study site and species

Brisbane, a sprawling subtropical city on the East coast of Australia, supports a wide variety of bird species, much of it native (Catterall et al. 2010). Of interest to this study are two members of the Superfamily Corvoidea commonly found Brisbane: the Torresian crow and the pied butcherbird (Cracticus nigrogularis). Torresian crows are a medium-sized corvid, distributed throughout the Northern half of the Australian continent (Rowley 1970, 1973d). Once mated, crows become sedentary and territorial, and while they readily share their territories with other corvoids, conspecifics are actively defended against (M. Brown pers. obs.; Rowley 1973a). This is in contrast to the second species studied, pied butcherbirds, which are regularly found in family groups and are known to breed cooperatively (Robinson 1994). Pied butcherbirds are a Cracticid, related to Torresian crows via the Corvoidea. The species is very poorly understood, with the only intensive study being on their cooperative breeding habits (Robinson 1994) and vocalisations (Taylor 2008). Both species are generalist carnivores that are common in open areas (Higgins et al. 2006a) and, while they fill similar niches, will often share habitat without conflict (M. Brown pers. obs.; Brown and Veltman 1987).

Aims

Vertical string pulling requires a series of complex manoeuvres to prevent the meat from falling in between pulls (Taylor et al. 2010b, Taylor et al. 2012b, Werdenich and Huber 2006, Heinrich 1995a). This is not the case in horizontal string pulling, which requires only one strong tug or a gradual pull to access the meat, making horizontal string pulling a much simpler problem to solve and limiting its capacity for testing insight. However, when conducted in the wild, vertical string pulling can hampered by its accessibility to other bird species in the area, potentially leading to the target species being excluded from the area by other, more aggressive, birds (see Chapter 4). Horizontal string pulling, on the other hand,

136 allows for greater exclusion of non-terrestrial foragers such as laughing kookaburras (Dacelo novaeguineae) and noisy miners (Manorina melanocephala).

This study looked to investigate the potential presence of insight in Torresian crows by testing whether they were capable of spontaneously solving a horizontal string-pulling experiment. The ability to solve this problem spontaneously would lend support to the existence of insight in Torresian crows. Torresian crows’ ability to visually recognise the continuity between the string and food, as well as perceive pulling the string as a means to an end, were also tested. Finally, this study sought to investigate the ability to undertake string-pulling experiments in the wild.

Methodology

Study sites and species

Wild Torresian crows were tested at six sites throughout southern Brisbane, two of which failed to produce results as crows would not interact with the apparatus. Of the four remaining sites, three (Sites B, C, I) were located in accessible private house yards while one (Site A) was located at Griffith University’s Nathan Campus. Pied butcherbirds interacted with the apparatus at three of these sites.

Experimental procedure

Wild birds were presented with a transparent 50cm x 25cm x 10cm box open on one side, in which two milk bottle caps with string attached were placed. A lid was held in place outside the box along two rails and balanced on a stick, which in turn was attached to the milk bottle caps via a fishing line pulley system (Fig. 8.1). This apparatus was set so that the box would shut once a bird had pulled out one of the two milk bottle caps, preventing it from pulling on both. This ensured that not only would birds be rewarded for pulling the correct string (receiving food), but would be punished for pulling the incorrect string (no food reward).

137

Figure 8.1 Diagram of string discrimination apparatus. Milk bottle caps (MBC) were connected to stick. As string is pulled, stick is moved once MBC exits box, allowing the lid to snap shut. Opening dimensions: 48cm x 9cm.

Wild birds were initially presented with meat in both milk bottle caps placed outside the apparatus as a familiarisation measure. After birds were regularly approaching the apparatus for food with minimal neophobic reactions, the apparatus was set with one cap baited with strings parallel exiting the box. This was continued until either birds were readily pulling the string, at which point the experiment began, or after two weeks had passed. If, after two weeks, the birds were not actively attaining food by pulling string, the birds were deemed unable to spontaneously solve the problem and training was initiated.

Training was conducted with two approaches, one with the caps placed at the back of the box and the correct string connected around another piece of meat outside the box. When the birds pecked at this meat, there was a strong likelihood they would also peck the string, pulling it and moving the cap towards them. This method had limited success. The second approach was to place the caps just inside the box, within reach of birds, and move them backwards on subsequent training trials.

Once crows were readily pulling strings, five training trials were initiated in order for crows to learn which behaviours resulted in food and which did not. After these five trials, pairs of crows were exposed to a minimum of 20 trails where the apparatus was set and the researcher retreated to a distance of no less than 10m, or further if crows would not approach apparatus while the researcher was present. In these cases, crow behaviours were

138 recorded with an Acorn Ltl-5210A motion camera set to record 60 seconds of footage after detecting movement. The milk bottle cap containing the meat was chosen at random before each trial. A crow was deemed to have succeeded in the trial if the first string it pulled was that attached to the meat, while pulling the incorrect string was notes as a failure. A minimum of 20 trials were recorded at each site, first with the strings parallel (Fig. 8.1) and then crossed over so the strings exited the box in-line with the opposite milk bottle lid. The success rates of trials were then compared to a 50% random performance through the use of a one-tailed binomial test in SAS 9.4.

Results

Birds were exposed to the apparatus at six sites. Of these, crows interacted with the apparatus at four sites (A, B, C, I), while pied butcherbirds did so at three (A, D, I). At site I, less than ten trials were successfully completed by either Torresian crows or pied butcherbirds, while pied butcherbirds did not complete sufficient trials at Site A after beginning to interact with apparatus during the crossed experiment. Only the crow at Site C was able to solve the problem spontaneously, with all other crows requiring training. At Site A, a juvenile interacted with the apparatus almost exclusively for a period of three weeks but was expelled from its parents’ territory partway through the crossed string experiment. During this time, adult crows did not approach the apparatus, instead watching their offspring. Only after the juvenile had left did these adults begin interacting with the apparatus. Both the adults and juvenile Torresian crows at Site A performed significantly better than a random choice with parallel strings, while the crows at Sites B and C did not (Table 8.1). Meanwhile, none of the four crows tested performed significantly better than random when the strings were crossed (Table 8.2). Butcherbirds at Site B performed extraordinarily well in both tests, far better than any of the crows studied and at a much higher rate than random (Table 8.1, Table 8.2). Butcherbirds were also able to solve the problem without training, though they may have learned by watching crows solve the problem.

139 Table 8.1 Performance of Torresian crows and pied butcherbirds with parallel strings

SPECIES AGE SITE SUCCESS TRIALS P VALUE SIGNIFICANCE Corvus orru Adult A 14 20 0.0368 * Corvus orru Juvenile A 14 20 0.0368 * Corvus orru Adult B 18 35 0.4329 Corvus orru Adult C 12 26 0.3474 Corvus orru Adult I 2 4 n/a Cracticus Adult B 32 41 0.0002 ** nigrogularis Cracticus Adult I 6 8 n/a nigrogularis

Table 8.2 Performance of Torresian crows and pied butcherbirds with crossed strings

SPECIES AGE SITE SUCCESS TRIALS P VALUE SIGNIFICANCE Corvus orru Adult A 10 20 0.3274 Corvus orru Juvenile A 7 11 0.1829 Corvus orru Adult B 16 27 0.1680 Corvus orru Adult C 12 20 0.1855 Cracticus Adult B 15 20 0.0127 * nigrogularis Cracticus Adult A 3 3 n/a nigrogularis

Crows at Site A appeared to improve their proficiency as the experiment continued, as did the crow at site C after 18 trials, although this was not enough to achieve a result better than random. Crows at Site B chose the correct string at a rate close to that of random chance, while the butcherbird at the same site was exemplary after the first few trials (Fig. 8.2). In the crossed experiment, only the crow at Site C appeared to show any improvement over time, though this improvement appeared to cease once the bird approached a 60% success rate (Fig 8.3).

140

1

0.75

0.5

Cumulative success rate 0.25

0 1 2 3 4 5 6 7 8 9 10111213141516171819202122232425262728293031323334353637383940 Trial

Crow A (adult) Crow A (juvenile) Crow B Crow C Butcherbird B

Figure 8.2 Cumulative success of birds subject to the parallel string test

1

0.75

0.5

Cumulative success rate 0.25

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 Trial

Crow A (adult) Crow A (juvenile) Crow B Crow C Butcherbird B

Figure 8.3 Cumulative success of birds subject to the crossed string experiment

141 Discussion

Corvids (Taylor et al. 2010b, Heinrich 1995a, Heinrich and Bugnyar 2005) and Psittadids (Pepperberg 2004, Werdenich and Huber 2006, Schuck-Paim et al. 2009) have been recorded as solving the vertical string pulling within seconds of being presented with it, without the need for training. This did not occur with the Torresian crows in this study, as all bar one subject required a relatively prolonged period of training before they would regularly pull the string. The only individual crow to spontaneously solve the problem went on to fail both the parallel and crossed string tests.

Torresian crows do appear to be capable of discriminating between parallel strings in order to obtain a food reward, although the performances of subjects in this study were inconsistent. These crows may have visually linked the string with the meat in order to assess their choice, or it may have been determined by the string’s proximity to the meat. However, two of the four crows were unable to reliably distinguish between which string would provide them with a food reward. It is likely that these crows simply observed that pulling a string occasionally resulted in a food reward, and did not attribute any special significance to the string that was attached to the meat. No crow was capable of correctly discriminating between strings when they were crossed. One possible explanation for this result is that crows that passed the parallel experiment were simply pulling the string in line with the meat. This being said, performances in the crossed string experiments were unanimously above 50% (but not significantly so), strongly suggesting that this was not the case. Furthermore, the success rate of crows in the crossed string experiment of 50-75% was very similar to that in New Caledonian crows reported by Taylor et al. (2010b).

Heinrich (1995a) was unable to test common ravens in the wild as they reacted with fear to the apparatus. It is possible that this same neophobia hampered the ability of the birds in this study to properly investigate string-pulling and discrimination. In addition, the success of pied butcherbirds compared to Torresian crows may have also been exaggerated by this fact. Brown and Jones (2016) compared neophobia of Torresian crows with two other Cracticus species, the Australian magpie and grey butcherbird and suggested that neophobia existed to a much lesser extent in these species. It seems quite possible that pied butcherbirds exhibit neophobia to a similarly small degree as these other Cracticids, an idea

142 supported by observations during this study, allowing them to interact with the apparatus in a less cautious manner than Torresian crows. However, after significant familiarisation and training, the Torresian crows in this study were not obviously reacting to the apparatus in a neophobic manner.

In contrast to crows, pied butcherbirds were far more successful in both the parallel and crossed string experiments. It appears likely that pied butcherbirds were able to understand the connectivity between the string and meat. This was especially evident in one trial at site B, where a butcherbird was observed to obviously trace its gaze along the string from the meat to the entrance of the box, before hopping down and pulling the correct string. The habit of butcherbirds to predate on long skinks and (Higgins et al. 2006a) may have predisposed them to understanding this task. Due to the small number of butcherbirds studied, further investigation is required to confirm this phenomenon.

In this study it has been shown that a test of continuity can be accomplished on wild birds in their natural habitat. However, this strategy has several weaknesses including an extensive familiarisation process and an experimental process that required a minimum of one week and in some cases lasted over a month. Furthermore, in some cases when crows failed the experiment, instead of giving up they intentionally dismantled the apparatus in order to access the food by overcoming the closure mechanism. This was particularly evident at site C, the worst-performing crow in the experiment.

It is possible that crows could not adequately view the inside of the box, and instead simply associated pulling one off the strings with a food reward. As these crows were wild, there was nothing preventing them from utilising the abundance of food in their natural habitat, thereby reducing the negative consequences of failing the experiments. Had the researchers been able to deny the crows food outside the experiment, crows may have been far more careful of their choices.

Of most interest in this study is the exemplary and unexpected performance of pied butcherbirds. Any future investigations into continuity should include a more intensive study into this species and possibly into other similar butcherbird species. A replication of Taylor’s (2012b) study of continuity where one string is cut and another is whole would also be interesting

143

Section 3: Conclusions and Reflections

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144 Clever crows; a general discussion

Behavioural capabilities of the Torresian crow compared to conspecifics

The family Corvidae has been intensively studied with respect to animal intelligence and cognition (Angell and Marzluff 2005, Marzluff and Angell 2013, Emery 2004, Clayton and Emery 2005, Emery 2006). A review presented here (Chapter 3) confirmed that research to have been predominantly conducted on relatively few species, generally on animals held in captivity and limited to a small number of research groups. The Corvidae, a group of 120 species, were represented by just over a dozen species in the literature. While this is more extensive than for many other taxa, the fact remains that most studies focused on a relatively small number of species and that large gaps in our knowledge of this group remain. Kaplan (2015) asserts that there is a definite need for further exploratory studies into complex behaviours in the Australian avifauna. The New Caledonian crow, arguably the world’s most intelligent bird, only became well-known when Gavin Hunt (2000b, a) noticed its unusual behaviours while in New Caledonia studying another species (D. Jones per. comm.; Hunt 2013). There is every chance that any of the 100+ barely studied corvid species could display similar behaviours to those recently discovered in the New Caledonian crow. This thesis has attempted to counter these biases in two ways: by investigating the behaviour of an Australian corvid species, and by using wild individuals as subjects.

Torresian crows bear a number of similarities with other corvid species, being highly synanthropic, generalist and are social during adolescence (Rowley 1970, 1973a, b, Rowley et al. 1973, 1973c, Everding 1995, Sinden 2002). Torresian crow populations have also benefited greatly from anthropogenic changes to habitat, which have converted expanses of dry sclerophyll forest into farmland and settlement (Sewell and Catterall 1998, Catterall 2004, Catterall et al. 2010, Sinden 2002, Woodall 2004). This synanthropy is nowhere more obvious than in the city of Brisbane, where a large sea of suburbia is interspersed with small islands of remnant forest. The structure of this habitat, with the typical suburban lot in Brisbane commonly containing one or several large trees and a well-watered lawn, effectively creates continuous edge habitat. Torresian crows in Brisbane have also modified

145 their traditional roosting behaviour to now do so in large numbers (Studer 2010), a behaviour noted to have social learning benefits (Marzluff et al. 1996, Wright et al. 2003). However, these roosts are much smaller than that of urban American crows (Corvus brachyrhynchos), where up to one million crows can reside in a single roost (Gorenzel and Salmon 1992). This behavioural similarity, suggests that Torresian crows are responding to the conditions found in urban environments in a similar manner to conspecifics in other countries. Torresian crows, as well as the other four Australian corvids, have also been documented caching their food, a trait recorded in overseas corvids (e.g., Dally et al. 2006, Bugnyar et al. 2007, Dally et al. 2010, Shaw and Clayton 2013). These observations suggest strongly that these species, though geographically well-separated, are likely to share behavioural characteristics.

The present study has also found a number of additional traits in which Torresian crows are similar to their overseas cousins. The high levels of neophobia commonly attributed to the family has been confirmed in this species (Chapter 5), in contrast with other corvoids predominant in Australia. Torresian crows performed at a similar level to New Caledonian crows when participating in the crossed string discrimination experiment (Taylor et al. 2010b), while some crows were successful in distinguishing between two parallel strings (Chapter 8). Like jungle crows and hooded crows, Torresian crows were able to associate a shape with a food reward and distinguish between this and other shapes. The crows in this study also showed some promise with quantity discrimination, though this was not at a significant level (Chapter 6). It is possible that the distractions of the wild setting may have hampered these results, and conducting further experiments in captivity may be more telling. The subjects also reacted to their own reflection in a non-aggressive way, a surprising finding for the highly-territorial breeding pairs studied (Chapter 7). This indicates that crows may not see their mirror reflection as a conspecific, and while these results do not offer solid evidence for Mirror Self-Recognition, it raises questions for further study. Based on the evidence complied in this thesis, Torresian crows do appear to extend this similarity in behaviour to more complex learning behaviours.

146 Surprising results: the behaviours of non-corvid native urban birds in Brisbane

While the results from the target species were certainly indicative of a similarity between Torresian crows and certain Northern Hemisphere corvids, perhaps more surprising and interesting results came from the additional species studied (Chapter 8). The five species of butcherbirds (Genus: Cracticus) are commonly found in urban areas throughout Australia, including the well-studied Australian magpie (e.g., Pellis 1981b, Brown and Veltman 1987, Jones and Thomas 1999, O'Leary and Jones 2002, Jones 2002, O'Leary 2002, Rollinson 2002, Warne and Jones 2003, Jones and Nealson 2003, Kaplan 2004, 2008, Warne et al. 2010). Despite the familiarity and abundance of these species, most remain poorly-studied. While studies have been conducted into their comparative breeding behaviours (Robinson 1994, Kaplan 2004) and song (Kaplan 2004, Johnson 2003, Taylor 2008), there have been no investigations of learning or problem solving in these species. Taking into account the evidence provided in this thesis, the neglect of behavioural studies of the cracticids needs to be reconsidered. Pied butcherbirds were found to be particularly adept at problem-solving in their readiness to participate and success in solving the parallel and crossed string discrimination experiments (Chapter 8). Additionally, grey butcherbirds interacted far more frequently with their reflection in a non-aggressive way than any of the other species investigated (Chapter 7). Kaplan (2004, 2015) has also noted that Australian magpies, another butcherbird species, have commonly shown behaviours considered indicative of higher intelligence, in particular that of play. There are also several anecdotal reports of Australian magpies interacting with humans in complex ways (Kaplan 2004), furthering the prospect of this group being a source of future interest.

Conducting learning experiments in the wild

The literature on corvid cognition is heavily biased towards studies of captive animals, with approximately 85% of studies in the field conducted in the laboratory (Chapter 3). These studies individually have been influential in improving our understanding of animal minds (Emery 2004, Emery and Clayton 2004, Emery 2006, Angell and Marzluff 2005, Marzluff and Angell 2013). The bias towards captive studies, however, means that this approach could be missing contextual significance, potentially leading to incomplete or incorrect data or the

147 misinterpretation of the behaviours observed. Studies of animals in the wild have shown to potentially produce inconsistent or even contradictory results to studies of the same species in the lab (Calisi and Bentley 2009), and are therefore important in tying the literature to the real world of these species.

Sample sizes reported in the literature are typically quite small, with four individuals being the most common sample size and most studies sampled taking place on less than ten individuals, with subjects usually tested a number of times individually (Chapter 3; e.g., Medina et al. 2011, Bogale et al. 2011, Taylor et al. 2012b, Bogale and Sugita 2014). In the present studies, a small number of individual adult breeding pairs were captured and banded to allow for individual identification. This allowed researchers to distinguish between the two mates and enable differences between the two to be investigated, as well as exposing both to experimental apparatus.

Methods usually used to catch pest crows, which usually formed large flocks, proved to be inadequate at catching mated territorial pairs (Chapter 4). Based on Heinrich’s (1995b) results, which showed that juvenile crows were far more neophillic than adults, and the observation that most flocks of Torresian crows tend to consist of juveniles and non- breeding adults (M. Brown pers. obs.), it is possible that a heightened sense of neophobia in adult pairs hampered the ability to catch crows in large traps.

Crows were eventually caught and banded through use of a camouflaged noose carpet trap, with a total of five birds being banded. However, these birds, with the exception of one, subsequently avoided researchers and experimental apparatus for months after banding. This avoidance behaviour made it impossible to conduct any kind of investigation on these birds, and experiments were therefore conducted in different territories on unbanded birds. As these individuals could not be distinguished, sites were considered as independent statistical units. After continued observation of banded and unbanded birds around Griffith University’s Nathan Campus, crows were deemed to consistently inhabit and defend patches of land, allowing researchers to be certain they were testing the same pair of birds throughout experimentation. This was consistent with Rowley’s (1973a) account of rural Torresian crow territories.

148 The experimental apparatus was not always effective in eliciting participation from crows. Neophobia and wariness of anthropogenic objects required apparatus to be either camouflaged or redesigned to be less conspicuous. This process took months of time as apparatus was deployed, assessed, redesigned, reconstructed and redeployed, sometimes several times. Occasionally, crow interaction with the apparatus was not consistent between sites, so assessment of apparatus interaction at one site was not always indicative of the overall suitability of the apparatus.

Conducting experiments in the field also meant that apparatus was accessible to many other species of bird that inhabit Brisbane, many of which were attracted to the bait provided for crows. While the interventions of these birds in the experiments on crows provided an opportunity for comparison with other species, many of these interactions meant that crows were frequently excluded from study sites by more aggressive birds and bait was often consumed before crows could approach the apparatus. This lengthened the data collection period considerably, and reduced the opportunity to include larger samples. Several sites that were initially trialled ended up being abandoned due to either heterospecifics completely excluding crows or crows simply not interacting with apparatus readily enough to facilitate the collection of data.

Weaknesses in methodology

Due to the reluctance of banded crows to interact with any apparatus that was subsequently deployed, experiments were conducted on unbanded birds. The study utilised the highly territorial nature of breeding crows to ensure that independent samples could be taken. However, this did result in the combining of data from both breeding adults in a pair as one sample. While this was not ideal, it is an indication of the difficulties of conducting experiments on wild birds. Additionally, the difficulty in accumulating data resulted in rather small samples sizes. While the number of individuals was similar to the majority of studies in the literature (Chapter 3), many of these studies had a large number of replicates per individual. This present study typically conducted 20-30 replicates per individual pair which, while still valuable, is considerably less that the number of replicates reported for many laboratory studies (e.g., Bogale et al. 2011, Bogale and Sugita 2014) though similar to some studies on wild-caught individuals (e.g., Taylor et al. 2010b, Taylor et al. 2012b). Such large

149 sample sizes were simply infeasible in the wild where it is impossible to coerce subjects into interacting with the apparatus. Furthermore, it is common practice in captive studies that subject birds are starved for a period before experimentation, ensuring that they will readily interact with the apparatus. This was a condition not available when studying wild birds.

Additionally, the wild environment meant that intensive training was not possible, requiring any familiarisation or training needed to be conducted over a much longer period of time. During this time birds were under no requirement to interact with the apparatus as they had access to many other sources of food. The main driver of training was the quality of bait provided, as crows preferred a large piece of beef mince to invertebrates that they may find while foraging. The tendency of caught birds to avoid apparatus also meant that the intention of conducting a mirror-mark test on wild birds was impractical. This resulted in the study reducing in scope into a far more generalistic observational study of mirror image stimulation (Chapter 7).

In conclusion, the act of undertaking this study involving wild animals ensured that the subjects were representative of the animals’ natural state. However, this decision reduced the ability to accumulate a large sample size by increasing the effort and time required for familiarisation, training and experimentation. Additionally, the scope of studies was significantly reduced by these issues, and some planned experiments were not able to be attempted.

Propositions for future research

Of most surprise was the readiness and capability of pied butcherbirds to participate in interactive experiments, especially that of string-pulling. The cognitive abilities of this species is completely unknown. The low level of apparent neophobia among any of the butcherbirds, their abundance in urban areas, along with the promising results shown in Chapter 7 and Chapter 8, make them a prime candidate for further investigation into cognition in an Australian bird. Their relative independence from the Corvidae is also of relevance to the study of avian cognition in general, as it would create a third group in which higher cognition could be documented and studied. Finally, comparative studies with other species of butcherbird such as the grey butcherbird and Australian magpie could easily be accomplished if they were the focus of a single project. Three of the five species of

150 Cracticids are common in the urban environment, suggesting ready availability for further study.

Torresian crows’ capacity to learn, remember and discriminate between arbitrarily drawn shapes also raises the exciting possibility of investigating the ability of this species to learn rules and concepts such as same-difference, analogical thinking and to replicate Bogale’s (2014) study into how much one can alter a shape before a crow stops recognising it as that particular shape. These experiments have been entirely conducted on captive animals and it is questionable whether they are representative of the wild behaviour of these birds. Such experiments could lead to a greater understanding of these cognitive processes in both crows and in general.

151

Section 4: References and Appendices

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152 References

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167 Appendices

Appendix I: EQ ratio of native study species

The Encephalisation Quotient (EQ) compares the log mass of an animal’s brain with the log of its body mass. It is hypothesised to provide a rough estimate of the animal’s intelligence relative to other species (Emery 2006). Information of body and brain mass has been extracted from Kaplan’s (2015) review of cognition in native Australian birds.

168 Appendix II: Studies reviewed in Chapter 3 analysis

Author Title

Hunter III and Object-discrimination learning set and hypothesis behaviour in the northern Kamil (1971) bluejay (Cynaocitta cristata) Kamil et al. (1973) Learning-set behaviour in the learning-set experienced blue jay (Cynaocitta cristata) (Hunter III and Marginal learning-set formation by the crow (Corvus brachyrhynchos) Kamil 1975) (Kamil and Intraproblem retention during learning-set acquisition in bluejays Mauldin 1975) (Cynaocitta cristata) (Kamil et al. 1977) Positive transfer from successive reversal training to learning set in blue jays (Cynaocitta cristata) Katzir (1982) Relationships between social structure and response to novelty in captive jackdaws Corvus monedula L., I. Response to novel space Heinrich (1988b) Winter foraging at carcasses by three sympatric corvids, with emphasis on recruitment by the raven, Corvus corax Balda and Kamil The spatial memory of Clark's nutcrackers (Nucifraga columbiana) in an (1988) anologue of the radial arm maze Bennett (1993) Spatial memory in a food storing corvid (Kamil et al. 1994) Performance of four seed-caching corvid species in the radial-arm maze analog Heinrich (1995a) An experimental investigation of insight in common ravens (Corvus corax) Heinrich (1995b) Neophilia and exploration in juvenile common ravens, Corvus corax Heinrich et al. Fear and food recognition in common ravens (1995) Olson et al. (1995) Performance of four seed-caching corvid species in operant tests of nonspatial and spatial memory Marzluff et al. Raven roosts are mobile information centres (1996) Bednekoff and Social caching and observational spatial memory in pinyon jays Balda (1996b) Bednekoff and Observational spatial memory in Clark's nutcrackers and Mexican jays Balda (1996a)

169 Kamil and Jones The seed-storing corvid Clark's nutcracker learns geometric relationships (1997) among landmarks Clayton and Episodic-like memory during cache recovery by scrub jays Dickinson (1998) Heinrich and Influence of competitors on caching behaviour in the common raven, Corvus Pepper (1998) corax Clayton and Scrub jays (Aphelocoma coerulescens) remember the relative time of Dickinson (1999b) caching as well as the location and content of their caches Clayton and Memory for the content of caches by scrub jays (Aphelocoma coerulescens Dickinson (1999a) Fritz and Kotrschal Social learning in common ravens, Corvus corax (1999) Kamil et al. (1999) Patterns of movement and orientation during caching and recovery by Clark's nutcrackers, Nucifraga columbiana Kusayama et al. Responses to mirror-image stimulation in jungle crows (Corvus (2000) macrorhynchos) Dukas and Kamil The cost of limited attention in blue jays (2000) Kamil and Jones Geometric rule learning by Clark's nutcrackers, Nucifraga columbiana (2000) Pollok et al. (2000) Development of object permanence in food-storing magpies (Pica pia) Clayton et al. Scrub jays (Aphelocoma coerulescens) form integrated memories of the (2001) multiple features of caching episodes Emery and Clayton Effects of experience and social context on prospective caching strategies by (2001) scrub jays Bugnyar et al. Food calling in ravens: are yells referential signals? (2001) Gibson and Kamil Tests for cognitive mapping in Clark's nutcrackers (Nucifraga columbiana) (2001b) Gibson and Kamil Search for a hidden goal by Clark's nutcrackers (Nucifraga columbiana) is (2001a) more accurate inside than outside a landmark array Bugnyar and Scrounging tactics in free-ranging ravens, Corvus corax Kotrschal (2002b)

170 Bugnyar and Observational learning and the raiding of food caches in ravens, Corvus Kotrschal (2002a) corax: is it 'tactical deception? Chappell and Tool selectivity in a non-primate, the New Caledonian crow (Corvus Kacelnik (2002) moneduloides) Jones et al. (2002) A comparative study of geometric rule learning by nutcrakcers (Nicifraga columbiana), pigeons (Columba livia) and jackdaws (Corvus monedula) Emery et al. (2003) Western scrub-jays use cognitive strategies to protect their caches from thieving conspecifics Wright et al. Communal roosts as structured information centres in the raven, Corvus (2003) corax Bond et al. (2003) Social complexity and transitive inference in corvids Bugnyar et al. Ravens, Corvus corax follow gaze direction of humans around obstacles (2004) Bugnyar and Leading a conspecific away from food in ravens (Corvus corax)? Kotrschal (2004) Chappell and Selection of tool diameter by New Caledonian crows Corvus mondeduloides Kacelnik (2004) Weir et al. (2004) Lateralisation of tool use in New Caledonian crows (Corus moneduloides) Bond et al. (2004) Pinyon jays use transitive inference to predict social dominance Dally et al. (2005) Cache protection strategies by western scrub-jays, Aphelocoma californica: implications for social cognition Dally et al. (2004) Cache protection strategies by western scrub-jays (Aphelocoma californica): hiding food in the shade Bugnyar and Ravens, Corvus corax, differentiate between knowledgeable and ignorant Heinrich (2005) competitors Kenward et al. Behavioural ecology: Tool manufacture by naïve juvenile crows (2005) Kenward et al. Development of tool use in New Caledonian crows: inherited action patterns (2006) and social influences Gibson and Kamil The fine-grained spatial abilities of three seed-caching corvids (2005) Dally et al. (2006) Food-caching Western Scrub-Jays keep track of who was watching when Stahler et al. Common ravens preferentially associate with grey wolves as a foraging (2001) strategy in Winter

171 Stöwe et al. Novel object exploration in ravens (Corvus corax): effects of social (2006b) relationships Stöwe et al. Effects of group size on approach to novel objects in ravens (Corvus corax) (2006a) Bugnyar and Pilfering ravens, Corvus corax, adjust their behaviour to social context and Heinrich (2006) identity of competitors Seed et al. (2006) Investigating physical cognition in rooks, Corvus frugilegus Weir and Kacelnik A New Caledonian crow creatively re-designs tools by bending or unbending (2006) alumninum strips Kenward et al. Development of tool use in New Caledonian crows: inherited action patterns (2006) and social influences Stafford et al. Does seed-caching experience affect spatial memory by Pinyon Jays? (2006) Lewis and Kamil Interference effects in the memory for serially presented locations in Clark's (2006) Nutcrackers, Nucifraga columbiana Raby et al. (2007) Planning for the future by western scrub-jays Bugnyar et al. The ontogeny of caching in ravens, Corvus corax (2007) Schloegl et al. Gaze following in common ravens, Corvus corax: ontogeny and habituation (2007) Tebbich et al. Non-tool-using rooks, Corvus frugilegus solve the trap tube problem (2007) Taylor et al. (2007) Spontaneous metaool use by New Caledonian crows Scheid et al. (2007) When, what and whom to watch? Quantifying attention in ravens (Corvus corax) and jackdaws (Corvus monedula) von Bayern et al. The role of food- and object-sharing in the development of social bonds in (2007) juveile jackdaws (Corvus monedula) Bond et al. (2007) Serial reversal learning and the evolution of behavioral flexibility in three species of North American corvids (Gymnorhinus cyanocephalus, Nucifraga columbiana, Aphelocoma californica) Scheid and Sort-term observational spatial memory in jackdaws (Corvus monedula) and Bugnyar (2008) ravens (Corvus corax) Schloegl et al. Do common ravens (Corvus corax) rely on human or conspecific gaze cues to (2008) detect hidden food?

172 Seed et al. (2008) Cooperative problem solving in rooks Holzhaider et al. Do wild New Caledonian crows (Corvus moneduloides) attend to the (2008) functional properties of their tools? Prior et al. (2008) Mirror-induced behaviour in the magpie: evidence of self-recognition Stulp et al. (2009) Western scrub-jays conceal auditory information when competitors can hear but cannot see Bird and Emery Insightful problem solving and creative tool modification by captive nontool- (2009a) using rooks Bird and Emery Rooks use stones to raise the water level to reach a floating worm (2009b) Bird and Emery Rooks perceive support relations similar to six-month-old babies (2010) Goto and Visual working memory of jungle crows (Corvus macrohynchos) in operant Watanabe (2009) delayed matching-to-sample Taylor et al. (2009) Do New Caledonian crows solve physical problems through causal reasoning? von Bayern et al. The Role of experience in problem solving and innovative tool use in crows (2009) Wimpenny et al. Cognitive processes associated with sequential tool use in New Caledonian (2009) crows Marzluff et al. Lasting recognition of threatening people by wild American crows (2010) Taylor et al. Complex cognition and behavioural innovation in New Caledonian crows (2010a) Taylor et al. An investigation into the cognition behind spontaneous string pulling in New (2010b) Caledonian crows Bond et al. (2010) Cognitive representation in Transitive interference: a comparison of four corvid species Bugnyar (2010) Knower-guesser differentiation in ravens: others' viewpoints matter Pika and Bugnyar The use of referential gestures in ravens (Corvus corax) in the wild (2011) Schmidt et al. Gaze direction - A cue for hidden food in rooks (Corvus frugilegus)? (2011)

173 Medina et al. New Caledonian crows' responses to mirrors (2011) Holzhaider et al. The social structure of New Caledonian crows (2011) Taylor et al. (2011) New Caledonian crows learn the functional properties of novel tool types von Bayern et al. Can jackdaws (Corvus monedula) select individuals based on their ability to (2011) help? Cheke and Clayton Eurasian jays (Garrulus glandarius) overcome their current desires to (2011) anticipate two distinct future needs and plan for them appropriately Clary and Kelly Cache protection strategies of a non-social food-caching corvid, Clark's (2011) nutcracker (Nucifraga columbiana) Cornell et al. Social learning spreads knowledge about dangerous humans among (2012) American crows Taylor et al. An end to insight? New Caledonian crows can spontaneously solve problems (2012b) without planning their actions Pizzey and Knight New Caledonian crows reason about hidden causal agents (2012) Taylor et al. Context-dependent tool use in New Caledonain crows (2012a) Hunt et al. (2012) Prolonged parental feeding in tool-using New Caledonian crows Shaw and Clayton Careful cachers and prying pilferers: Eurasian jays (Garrulus glandarius) limit (2013) auditory information available to competitors Shaw and Clayton Eurasian jays, Garrulus glandarius, flexibly switch caching and pilfering tactics (2012) in response to social context Ostojić et al. Evidence suggesting that desire-state attribution may govern food sharing in (2013) Eurasian jays Clucas et al. (2013) Do American crows pay attention to human gaze and facial expressions? Seed et al. (2007) Postconflict third-party affiliation in rooks, Corvus frugilegus St Clair and Rutz New Caledonian crows attend to multiple functional properties of complex (2013) tools Cibulski et al. Familiarity with the experimenter influenced the performance of Common (2014) ravens (Corvus corax) and Carrion crows (Corvus corone corone) in cognitive tasks

174 Miller et al. (2014) Tolerance and Social Facilitation in the foraging behaviour of free-ranging crows (Corvus corone corone; C. c. cornix) Taylor et al. (2014) Of babies and birds: complex tool behaviours are not sufficient for the evolution of the ability to create a novel causal intervention Logan et al. (2014) Modifications to the Aesop's Fable paradigm change New Caledonian crow performances Jelbert et al. (2014) Using Aesop's fable paradigm to investigate causal understanding of water displacement by New Caledonian crows Soler et al. (2014) Mirror-mark tests performed on jackdaws reveal potential methodological problems with the use of stickers in avian mark-test studies Shaw and Clayton Pilfering Eurasian jays use visual and acoustic information to locate caches (2014)

175 Appendix III: Detailed description of study species Corvoids Australian magpie (Cracticus tibicen) The Australian magpie (hereafter, the magpie) is a medium-sized black and white bird, usually weighing approximately 200-350g (Higgins et al. 2006a), that is common throughout most of the mainland continent. Magpies are perhaps Australia’s most well-studied bird and, excepting perhaps the laughing kookaburra (Dacelo novaeguineae), the most well- known Australian bird (O'Leary 2002, Kaplan 2004). A part of this popularity may be due to their virtual ubiquity in Australia and their common contact with humans in urban areas, though their song is undoubtedly a large contributor (Kaplan 2004, Higgins et al. 2006a, O'Leary 2002). Magpie song is often described as beautiful, contrasting with the harsh calls of Australian crows (Kaplan 2004, Higgins et al. 2006a, O'Leary 2002). Although it holds the name magpie, it is no more closely related to the Eurasian magpie (Pica pica), a true Corvid, than it is to the crows.

Magpies are found in a wide variety of habitats, including dry open forests, grasslands, residential areas, shrublands and occasionally in wet closed forests (Higgins et al. 2006a). Populations in rural areas have increased markedly as native vegetation has been replaced with open farmland, and are now extraordinarily common in suburban areas, particularly those with open grassy areas (Higgins et al. 2006a).

Magpies may be found in flocks of 12-20 birds and even up to 100 in rural areas, though are usually only seen in pairs or singly (Higgins et al. 2006a). Territories may be defended by a breeding pair or territorial groups, although birds on Eastern Australia predominantly live in pairs (Higgins et al. 2006a).

Australian magpies are generalists, both in a suburban (O'Leary and Jones 2002, Jones 2002) and natural and rural habitats (Vestjens and Carrick 1974). Unlike butcherbirds and currawongs, which gather food from various forest levels, magpies forage exclusively on the ground. They are also the most commonly fed birds in Brisbane (Rollinson et al. 2003). Magpies, currawongs and butcherbirds will often forage in the same area peacefully, though a hierarchical order will form with magpies at the top and the other birds avoiding conflict with them (Kaplan 2004). While Torresian crows may also participate in this heterospecific

176 foraging, adult magpies will attack them if present (M. Brown pers. obs.). Magpies feed on a wide range of foods, from seeds to invertebrates, reptiles and even small mammals and birds (Kaplan 2004). Unlike other species in their niche, magpies occasionally forage by using exclusively auditory cues, listening for the sound of scarab larvae below the ground (Floyd and Woodland 1981).

Pied butcherbird (Cracticus nigrogularis) Pied butcherbirds are a small-medium sized bird, usually about 30cm long and weighting approximately 120g (Higgins et al. 2006a). They are larger than the less-common grey butcherbirds and while determining between the sexes can be difficult, juveniles have a distinct grey plumage that contrasts with the black and white of adults (Higgins et al. 2006a). Pied butcherbirds are common throughout Australia, predominantly in open forests and in modified environments with plentiful trees. Butcherbirds typically feed on insects and occasionally carrion and bird hatchlings. Unlike Torresian crows, they are considered “friends of the farmer” for their tendency to eat pests (Higgins et al. 2006a). Besides Robinson’s (1994) thesis on cooperative breeding, there is little known about the social behaviour of pied butcherbirds. Of most interest, pied butcherbirds parents do not seem to evict their young from their territories; therefore it is most common to find territorial groups of both adult and juvenile pied butcherbirds, being territorially sedentary throughout the year (Robinson 1994, Higgins et al 2006).

Undoubtedly the most well-known aspect of the species is its voice, which, like Australian magpies and unlike Torresian crows, is appealing to the human ear (Higgins et al. 2006a). The song has been described as “one of the finest in the world” (Higgins et al. 2006a, p522) and like “a person with a good flute playing it well” (Hartshorne 1953, p118). Many Australians are familiar with the song of the pied butcherbird, without knowing the bird that is uttering it (pers. com. with Brisbane residents).

Grey butcherbird (Cracticus torquatus) Slightly smaller than the pied butcherbird, the grey butcherbird is common in suburban Brisbane where eucalyptus and other Myrtaceae are present (Sewell and Catterall 1998, Johnson 2003, Higgins et al. 2006a). Brisbane’s patchwork of disturbed native vegetation, which predominantly follows gullies, steep slopes and the tops of high hills, is thought to

177 assist in the species’ persistence in the urban habitat (Johnson 2003), though they are also found in non-native flora, being one of the few native Australian birds found in exotic pine plantations (Johnson 2003). Grey butcherbirds are also one of the most commonly-fed species by bird feeders in Brisbane (Rollinson et al. 2003). The species is small-medium sized, ranging from 24-30cm (Pizzey and Knight 2012) with black, white and grey plumage (Pizzey and Knight 2012, Higgins et al. 2006a) and can be found throughout much of Southern and Eastern Australia. Juveniles and immatures are discernible from the presence of brown plumage (Higgins et al. 2006a).

Unlike the pied butcherbird, where cooperative breeding is common (Robinson 1994), grey butcherbirds are usually found alone or in pairs (Blakers et al. 1984). Grey butcherbirds prey on animals such as invertebrates, small lizards and mammals (Johnson 2003, Higgins et al. 2006a) and small birds and nestlings, even chasing down birds in the air (Johnson 2003). Like the pied butcherbird, the predominant literature on the grey butcherbird regards its vocalisations (Johnson 2003).

Pied currawong (Strepera graculina) Originally thought to be a member of the Genus Corvus (White 1790), the pied currawong is a predominantly black bird with small white patches on its wings and long tail (Higgins et al. 2006a). The species is more slender than the Torresian crow and larger than a magpie, being 48cm in length and weighing 280-320g (Higgins et al. 2006a). Currawongs are usually seen singly or in pairs, but can be found in flocks that can become quite large in winter. They are much tamer in urban areas but are far less likely to interact with humans than either butcherbirds or magpies (M. Brown pers. obs.; Higgins et al. 2006a). Common in eucalypt forests and rainforests, currawongs feed on a variety of food, from fruits and seeds to invertebrates and occasionally vertebrates (Higgins et al. 2006a). Currawongs, like the previously-mentioned species, are common in modified areas, though only inhabit these areas seasonally (Higgins et al. 2006a), being far more common in Brisbane during the winter months (D. Jones pers. comm.; M. Brown pers. obs.). Higgins et al. (2006a) state that the seasonality of currawong populations in urban areas is decreasing, with the birds becoming more permanent residents in these areas. Although the birds have many positive impacts, including eating invasive moths and phasmids, currawongs have been considered a

178 pest for eating fruits and corn and are often shot (Higgins et al. 2006a). The species can be found throughout much of the Australian East.

Other species

During the experimentation process of Chapter 7, several non-corvoid species that also inhabit the suburbs of Brisbane were included. The Encephalisation Quotients for all native study species have been provided in Appendix I.

Magpie-lark (Grallina cyanoleuca) Magpie-larks are a large (50cm, 85g) flycatcher of the family Dicruidae covered in black and white plumage (Higgins et al. 2006a). Magpie-larks are members of the Corvoidea superfamily, though they are not closely related to magpies or butcherbirds. Most common in open grasslands and eucalypt forests, usually near water, and in built-up areas, magpie- larks are sedentary in much of northern Australia (Higgins et al. 2006a). The birds are primarily insectivorous and terrestrial foragers, rarely preying on food in canopies or in the air.

Australian brush-turkey (Alectura lathami) The Australian brush-turkey is a large ground-dwelling bird, usually 60-70cm and approximately 2.3kg, that is common along the Eastern coast of Queensland to as far South as (Marchant and Higgins 1993). The species lives in forested areas and can be found in both rainforests and dry sclerophyll forests (Marchant and Higgins 1993) and has also become common in suburbs adjacent to these areas (Jones and Everding 1991). Adults are sedentary and promiscuous, incubating their eggs in mounds of dirt and debris defended by the males (Marchant and Higgins 1993). Marchant and Higgins (1993) note that almost all knowledge of the species is based on work by Jones (1990a, 1990b, 1991).

Crested pigeon (Ocyphaps lophotes) Crested pigeons are an endemic, medium-sized pigeon that is found throughout the Australian continent. Named after a crest on the top of their head, they are relatively poorly studied regarding their social organisation and behaviour (Higgins and Davies 1996). Higgins and Davies (1996) note that the species is unusually aggressive and will attack and even kill other birds on sight, particularly other bronze-winged pigeons.

179 Spotted dove (Spilopelia chinensis) The spotted dove is an invasive dove native to South and South-East Asia that has become common in urban and suburban areas throughout Australia and New Zealand (Higgins and Davies 1996). The species is rarely found in native Australian bushland or away from developed landscapes. Behaviours of the species are poorly-known in Australia, despite its abundance (Higgins and Davies 1996). Feeding mainly on seeds and waste food, spotted turtle doves are found in suburban areas year-round.

Common myna (Acridotheres tristis) Common mynas are an invasive urban species in Australia, being native to the Indian Subcontinent (Higgins et al. 2006a). A small- to medium-sized species, it is considered a pest in agricultural areas, with several eradication programs established around Australia. Common mynas are sedentary, often living in flocks and competing with the native noisy miner for territory. Of most interest in common mynas are their problem solving abilities (Sol et al. 2011) and complex song (Higgins et al. 2006a).

180 Appendix IV: Scorer sheet used in trial categorisation

Video Time Behaviour Responding Social, self- Any comments? to mirror? directed or other?

181 Appendix V: Scorer sheets used in final mirror classification

Video Interacting with Mirror Not interacting with mirror Comments Aggressive Other Eating Other

182 Appendix VI: Correlations between scorers

After sample videos were identified, bird behaviours were categorised by seven independent scorers. For methodology, see Chapter 7.

Scorers:

Ma Matthew Brown C Chetan Hemmadi V Vikasini Hemmadi L Lyndall Brown Mi Michelle Brown S Scott Brown P Priyanka Hemmadi

Common myna

C V L Mi S P

Ma 0.79 0.92 1.00 0.99 0.95 0.93

C 0.79 0.85 0.88 0.88 0.81

V 0.92 0.93 0.84 0.84

L 0.97 0.98 0.87

Mi 0.96 0.94

S 0.86

Crested pigeon

C V L Mi S P

Ma 0.84 0.76 0.97 1.00 1.00 0.99

C 0.83 0.88 0.90 0.88 0.89

V 0.76 0.76 0.76 0.80

L 0.97 0.97 0.97

Mi 1.00 0.98

S 0.99

Torresian crow (Site A)

183

C V L Mi S P

Ma 0.45 0.77 0.78 0.80 0.80 0.81

C 0.84 0.86 0.91 0.87 0.84

V 0.95 0.97 0.97 0.92

L 0.99 0.99 0.92

Mi 1.00 0.94

S 0.92

Torresian crow (Site C)

CM C V L Mi S P

Ma 0.54 0.89 0.87 0.91 0.87 0.90

C 0.69 0.86 0.68 0.56 0.67

V 0.91 0.97 0.86 0.87

L 0.97 1.00 0.93

Mi 0.93 0.95

S 0.86

Torresian crow (Site D)

C V L Mi S P

Ma 0.90 0.98 0.90 0.93 0.96 0.97

C 0.91 0.83 0.90 0.86 0.88

V 0.95 0.95 0.94 0.98

L 0.87 0.96 0.91

Mi 0.88 0.95

S 0.92

Torresian crow (Site E)

184

C V L Mi S P

Ma 0.89 0.90 0.88 0.91 0.83 0.96

C 0.92 0.85 0.93 0.94 0.84

V 0.91 0.96 0.94 0.88

L 0.98 0.91 0.89

Mi 0.97 0.91

S 0.86

Torresian crow (Site A) (Control)

\ C V L Mi S P

Ma 0.99 0.97 0.98 0.98 0.96 0.97

C 0.95 0.98 0.97 0.96 0.98

V 0.98 0.99 0.95 0.97

L 1.00 0.97 1.00

Mi 1.00 1.00

S 0.96

Torresian crow (Site G)

C V L Mi S P

Ma 0.92 0.85 0.94 0.89 0.82 1.00

C 0.88 0.88 0.82 0.68 0.92

V 0.95 0.89 0.74 0.90

L 0.92 1.00 0.94

Mi 1.00 0.90

S 0.85

185 Australian brush turkey

C V L Mi S P

Ma 0.92 0.91 0.94 0.98 1.00 0.93

C 1.00 0.86 0.99 1.00 0.96

V 0.90 1.00 1.00 0.98

L 0.98 0.98 0.93

Mi 1.00 1.00

S 1.00

Australian magpie

C V L Mi S P

Ma 0.83 0.89 0.93 0.96 0.96 0.91

C 0.89 0.88 0.95 0.95 0.81

V 0.93 0.97 0.95 0.88

L 0.97 0.97 0.96

Mi 1.00 1.00

S 0.98

Pied currawong

C V L Mi S P

Ma 0.73 0.89 0.95 0.98 0.98 0.90

C 0.85 0.74 0.72 0.70 0.65

V 0.93 0.94 0.98 0.93

L 1.00 1.00 0.88

Mi 1.00 0.91

S 0.85

186

Grey butcherbird

C V L Mi S P

Ma 0.66 0.88 0.75 0.80 0.82 0.64

C 0.71 0.50 0.71 0.75 0.85

V 0.85 0.90 0.88 0.63

L 0.94 0.94 0.62

Mi 1.00 0.79

S 0.84

Magpie-lark

C V L Mi S P

Ma 0.91 0.92 0.88 0.94 0.93 0.92

C 0.95 0.88 0.96 0.95 0.97

V 0.92 0.96 0.97 0.97

L 0.98 0.97 0.95

Mi 1.00 0.99

S 0.98

Spotted dove

V L Mi S P

C 0.89 0.87 0.99 0.99 0.89

V 0.92 0.89 0.92 0.80

L 0.89 0.89 0.82

Mi 1.00 0.97

S 0.97

187 Appendix VII: Results of ANOSIM

Groups R Statistic Significance Possible Actual Number Level % Permutations Permutations >=Observed

Common myna, Crested 1 0.1 1716 999 0 pigeon Common myna, -0.232 99.9 26978328 999 998 Torresian crow Common myna, Brush 1 0.2 1716 999 1 turkey Common myna, 0.407 0.5 1716 999 4 Australian magpie Common myna, Pied 0.342 0.2 1716 999 1 currawong Common myna, Grey 0.877 0.2 1716 999 1 butcherbird Common myna, Magpie- 1 0.1 1716 999 0 lark Common myna, Spotted 0.587 0.1 1716 999 0 dove Crested pigeon, Torresian 0.979 0.1 26978328 999 0 crow Crested pigeon, Brush 1 0.1 1716 999 0 turkey Crested pigeon, 1 0.3 1716 999 2 Australian magpie Crested pigeon, Pied 1 0.2 1716 999 1 currawong Crested pigeon, Grey 0.959 0.1 1716 999 0 butcherbird Crested pigeon, Magpie- 0.911 0.1 1716 999 0 lark

188 Crested pigeon, Spotted 1 0.2 1716 999 1 dove Torresian crow, Brush 0.343 0.1 26978328 999 0 turkey Torresian crow, -0.079 73 26978328 999 729 Australian magpie Torresian crow, Pied -0.069 70 26978328 999 699 currawong Torresian crow, Grey 0.626 0.1 26978328 999 0 butcherbird Torresian crow, Magpie- 0.637 0.1 26978328 999 0 lark Torresian crow, Spotted -0.044 57.9 4496388 999 578 dove Brush turkey, Australian 0.887 0.1 1716 999 0 magpie Brush turkey, Pied 0.853 0.1 1716 999 0 currawong Brush turkey, Grey 0.738 0.1 1716 999 0 butcherbird Brush turkey, Magpie- 1 0.2 1716 999 1 lark Brush turkey, Spotted 0.716 0.1 1716 999 0 dove Australian magpie, Pied 0.707 0.2 1716 999 1 currawong Australian magpie, Grey 0.914 0.1 1716 999 0 butcherbird Australian magpie, 1 0.2 1716 999 1 Magpie-lark Australian magpie, 0.013 30.7 1716 999 306 Spotted dove Pied currawong, Grey 0.584 0.3 1716 999 2 butcherbird

189 Pied currawong, Magpie- 0.96 0.1 1716 999 0 lark Pied currawong, Spotted 0.646 0.8 1716 999 7 dove Grey butcherbird, 0.864 0.1 1716 999 0 Magpie-lark Grey butcherbird, 0.832 0.1 1716 999 0 Spotted dove Magpie-lark, Spotted 1 0.3 1716 999 2 dove

190

191