Meliphagidae)

Home , Anthochaera, Banded honeyeater, Bell miner, Black honeyeater, Bridled honeyeater, Brown honeyeater

FORAGING BEHAVIOR, BEHAVIORAL FLEXIBILITY, AND RANGE SIZE OF

AUSTRALIAN HONEYEATERS (MELIPHAGIDAE)

SARAH KATHERINE WAGNER

B.A., Earlham College, 2002

M.A., University of Colorado, 2010

A thesis submitted to the

Faculty of the Graduate School of the

University of Colorado in partial fulfillment

of the requirement for the degree of

Doctor of Philosophy

Department of Ecology and Evolutionary Biology

2015

This thesis entitled:

Foraging behavior, behavioral flexibility, and range size of Australian Honeyeaters

(Meliphagidae)

written by Sarah Katherine Wagner

has been approved for the Department of Ecology and Evolutionary Biology

Alexander Cruz (chair)

Kendi Davies (member)

14 July, 2015

The final copy of this thesis has been examined by the signatories, and we Find that both the content and the form meet acceptable presentation standards Of scholarly work in the above mentioned discipline. iii

Wagner, Sarah Katherine (Ph.D., Department of Ecology and Evolutionary Biology)

Foraging behavior, behavioral flexibility, and range size of Australian Honeyeaters

(Meliphagidae)

Dissertation directed by Professor Alexander Cruz

Anthropogenic disturbance is the leading cause of species extinctions (Vitousek 1997,

Pimm and Raven 2000, Ewers and Didham 2006). Modern ecologists are given the task of determining how to predict and then mitigate species’ response to such disturbances. Species with larger niches, and more behaviorally flexible species, are predicted to better succeed in novel environments in the face of large scale habitat changes (Mayr 1965, Ehlrich 1989, Sol

2002, Shultz 2005). Foraging behavior can be a good descriptor of species’ niches, and the variation in these measures can be used to quantify behavioral flexibility (Sol 2002). My dissertation utilizes the interface between animal behavior data and broad-scale ecological patterns. I collected foraging behavior data (~7,300 independent foraging observations) across 74 of 75 Australian honeyeater (Meliphagidae) species to quantify niche size and position. I used functional dispersion (FDis) to quantify niche size. Related species foraged similarly, and foraging behavior showed significant phylogenetic signal. Generalists utilized a variety of resource acquisition strategies, whereas species with small niches were either highly nectarivorous or insectivorous. In order to determine if foraging niche size can be a predictor of extinction risk, I tested whether niche size was correlated with exposure or sensitivity to climate change. I did not find niche size to be a significant predictor of these risks as assessed by others.

However, synergistic effects between small niche size and anthropogenic disturbance and climate change may put these species at an elevated risk of extinction. I also found a strong iv

positive relationship between species that are highly nectarivorous and species that make attacks to the air for invertebrates. Nectarivorous species supplement their diets with protein, and it appears that these species make costly aerial attacks to acquire protein quickly. Geographic range size was not correlated with foraging niche size, but it was weakly correlated with niche position.

Specifically, species that glean and hang from leaves in forests with high canopies were found to have smaller geographic range sizes. This is likely driven by the fact that such forests occur over a limited area in Australia, and occupy only remnants of their former geographic extent.

ACKNOWLEDGEMENTS

The completion of this dissertation was very much dependent on the support and help from

numerous people. I first want to thank my husband, collaborator and adventure partner, Eliot

Miller for his love, support, patience, and enthusiasm. I also want to thank my parents, Pat and

Lowell Wagner, for encouraging me to be a bird loving conservation scientist even if it meant

spending so many years in school. I am grateful for a shared love of science, natural history and

humor with my siblings and their partners, Becky Wagner and Jed Bopp and Jon Wagner and

Prairie Hale. I am not sure where I would be without the free counseling and editing, and

reminders to keep getting my hands dirty in the garden. I thank my advisor, Alex Cruz for

believing in me, giving me the freedom to study a family of birds all the way in Australia,

sharing his excitement about avian biogeography and conservation and being an incredibly

inspiring educator and mentor. I thank my committee: Sharon Collinge, Kendi Davies, Dan

Doak, and Rob Guralnick for the countless ideas, analyses help, editing suggestions and the

many hours spent brain storming. The Cruz lab family (Marcus Cohen, Clint Francis, Nathan

Kleist, Catherine Ortega, Ty Tuff) have been a comforting examples of how to navigate

academia and lots of fun on whitewater rafting and field work adventures. Kelly Ramirez has been a dear friend since day one of my graduate career at CU and is responsible for many of my more stream-lined and well thought out ideas. I am forever indebted to Bill Buskirk, my

Ornithology professor at Earlham College, who first opened my eyes to the world of birds and thereafter provided multiple opportunities to further pursue my ornithology interests (he also does one stellar American woodcock display impersonation). My Aunt Janet and Uncle Skip bought me my first Ornithology text book and continued to support other Ornithology May terms and excursions, and I am very grateful for that. I taught during every semester that I was a vi

student at CU and I am grateful for the teaching mentorship and guidance from John Basey,

Mike Breed and the wonderful people at the Biological Sciences Initiative at CU. Our work in

Australia would have been impossible without support for Mark Westoby at Macquarie

University and Leo Joseph at the Australian National University. I am also incredibly grateful to

Glen Sanders and Hillary Cherry for being our very comfortable and fun loving Sydney home

base. I thank our new community of friends in Moscow, Idaho where I finished up the last leg of my PhD with the help of: Denim Jochimsen, Rafael Maia, Amy Worthington, Andy Kraemer, and Anahi Espinola.

vii

CONTENTS

CHAPTER

I. INTRODUCTION

Foraging behavior, behavioral flexibility, and range size of Australian honeyeaters

(Meliphagidae)………………………………………….…………………………………1

Summary of chapters two through four………………………………………………...…2

II. A QUANTITATIVE SUMMARY OF THE FORAGING BEHAVIOR OF A

CONTINENTAL RADIATION: AUSTRALIAN

MELIPHAGIDAE…………………………………………………………..…………….4

Abstract………………………………...………………………………………………….4

Introduction…………………………………………………...…………………………...4

Methods……………………………………………...…………………………………...10

Results……………………...…………………………………………………………….15

Discussion…………………………...…………………………………………………...62

III. DOES FORAGING NICHE PREDICT EXTINCTION RISK IN THE AUSTRALIAN

MELIPHAGIDAE?...... 68

Abstract…………………………………………………………………………………..68

Introduction…,,,………………………………………………………………………….68

Methods…………………………………………………………………………………..71

Results……………………………………………………………………………………77

Discussion……………………………………………………………………………...... 82 viii

IV. NICHE SIZE AND THEREFORE BEHAVIORAL FLEXIBILITY ARE ASSOCIATED

WITH LARGE GEOGRAPHIC RANGES……………………………...... 87

Abstract…………………………………………………………………………………..87

Introduction………………………………………………………………………………87

Methods………………………………………………………………………………...... 90

Results……………………………………………………………………………………92

Discussion……………………………………………………………………………...... 99

V. CONCLUSION…………………………………………………………………………104

BIBLIOGRAPHY…………….………………………………………………………………...107

TABLES

2.1 Map of foraging behavior data collection sites……………………………...……………….59

2.2 Bar graph of foraging niche size (FDis) scores per species in order of largest to smallest….64

3.1 Common name, species name, IUCN threat status, IUCN population trends and exposure and sensitivity to climate change……………………………………………………………………..79

3.2 ANOVA results for FDis and sensitivity, exposure and IUCN trend, PC1 with sensitivity, exposure, and IUCN trend, and PC2 with sensitivity, exposure, and IUCN population trend….80

FIGURES

2.1 Hawking (percent of attacks to the air that are not to flowers) and proportion of attacks to flowers (nectarivory) were positively correlated………………………………………………...11

2.2 Bar graph of foraging niche sizes (FDis) scores per species in order of largest to smallest..17

2.3 Plot of foraging niche size (FDis) by species across the phylogeny………………………………………………………………………………………...19

2.4 Plot of nectarivory by species across the phylogeny………………………………………..22

2.5 Plot of proportion of attacks to fruit (frugivory) by species across the phylogeny…………30

2.6 Plot of proportion of attacks to branches by species across the phylogeny…………………36

2.7. Foraging niche size (FDis) and proportion of attacks to flowers (nectarivory) produced a unimodal response which highlights the fact that specialization and small sample size are related ……………………………………………………………………………………………………55

2.8 Hawking (percent of attacks to the air that are not to flowers) and proportion of attacks to flowers (nectarivory) were positively correlated………………………………………………...56

2.9 Meliphagidae phylogeny with position along PC1 mapped in color………………………...58

2.10 Meliphagidae phylogeny with position along PC2 mapped in color……………………….60

3.1 Foraging niche size and IUCN population trend…………………………………………….79

3.2 Niche position on PC2 and IUCN population trends………………………………………...80

4.1 Geographic range sizes per species (occurrence in a 100 x 100 grid cell)…………………..93

4.2 There was a negative relationship between geographic range size and the first principal component………………………..………………………………………………………………95

4.3 Number of vegetation types occupied per species…………………………….……………..98

4.4 As geographic range size increased, so did the number of vegetation types that a species occurred in……………………………………………………………………………………...102 xi

CHAPTER I

INTRODUCTION

FORAGING BEHAVIOR, BEHAVIORAL FLEXIBILITY, AND RANGE SIZE OF AUSTRALIAN HONEYEATERS (MELIPHAGIDAE)

Anthropogenic disturbance is the leading cause of species extinctions (Vitousek 1997,

Pimm and Raven 2000, Ewers and Didham 2006). It is imperative that we find the best ways to predict and then mitigate species’ response to such disturbances. Deciphering which traits and behaviors make species more or less susceptible to future changes could be helpful in predicting their response to future change. Species with larger niches are predicted to better succeed in novel environments in the face of large scale habitat changes (Mayr 1965, Ehrlich 1989, Sol

2002, Shultz et al. 2005). Foraging behavior can be a good descriptor of species’ niches, and the variation in these measures can be used to quantify species’ ability to shift in the face of change

(Sol 2002).

How, where, and under what conditions birds forage can help us to understand more about species’ ecology, how they exploit resources, and how communities are structured

(Thomas et al. 2003, Morrison and Lindell 2010, Maslo et al. 2012). In my dissertation, I used detailed foraging behavior of Meliphagidae to describe the intricacies of their resource use, their foraging behavior, and their vegetation associations across their phylogeny to look at phylogenetic conservatism in foraging traits, relationships with exposure and sensitivity to climate change and to test the niche breadth-range size hypothesis. 2

I collected foraging behavior and ecological data for 74 species of Australian

Meliphagidae (honeyeaters) across much of the continent over 18 months. Australian

Meliphagidae are one of the most abundant passerine groups in both species number and number

of individuals and they are also fairly easy to observe in the field. Their phylogeny is well-

resolved (Joseph et al. 2014) and they are diverse in both behavior and diet. These qualities make

them an ideal family for this study. Because this project involved multiple collaborators for

funding, fieldwork, data entry and analyses, they are written in first-person plural for the purposes of publication and to reflect co-authorship. Species names are written at the first mention (per chapter) and then the common name is used.

SUMMARY OF CHAPTERS I THROUGH IV

Chapter II presents the details of how I quantified foraging behavior into a measurement of foraging behavior niche that is not influenced by sample size. I focused on a number of important axes of resource use and foraging behavior to develop a measurement of foraging niche size per species. I described how components of the foraging niche varied across the phylogeny using functional dispersion (FDis) and multivariate analyses to quantify niche size and position. I was able to show, qualitatively, that most species’ traits were phylogenetically conserved. Because niche size is associated with risk, I wanted to look at which traits were associated with small foraging niches. Small niches belonged to species that were highly nectarivorous or insectivorous and species with large foraging niches usually ate some fruit, insects, lerp, and nectar. This chapter is in prep to be submitted to The AUK.

In Chapter III, I used the fine scale measurement of foraging niche size in conjunction with measurements of exposure and sensitivity to climate change (Franklin and Garnett 2014) to measure extinction risk. I wanted to know if foraging niche size could improve our ability to test 3 for sensitivity. We were not able to show that foraging niche size alone could predict risk, but it was certainly an important component when considering which traits make species more sensitive. It is possible that there could be additive or synergistic effects of having a small foraging niche and being exposed to climate change.

Chapter IV tests a much debated, yet not agreed upon, hypothesis in ecology: the niche breadth-range size hypothesis. This hypothesis has implications for what makes species common in areas and what makes them rare. There are multiple ways to measure niche breadth, but we chose to focus on diet/foraging and habitat breadth (number of vegetation types). Species that include less abundant foraging substrates (tall canopies) are also the species with the smallest niches, which leads me to believe that those things limit range size. Habitat breadth (number of vegetation types occupied) and range size were positively related, but habitat breadth was not related to foraging niche size as one might assume.

Chapter II

A QUANTITATIVE SUMMARY OF THE FORAGING BEHAVIOR OF A CONTINENTAL RADIATION: AUSTRALIAN MELIPHAGIDAE

ABSTRACT

How, where, and under what conditions birds forage can help us to understand more about species’ ecology, how they exploit resources, and how communities are structured

(MacArthur 1972, Pyke 1980, Robinson and Holmes 1982, Shochat 2004), but it also has implications for the role of animal behavior in conservation. Foraging behavior, in particular has proven to be an important component when considering conservation of some species (Thomas et al. 2003, Morrison and Lindell 2010, Maslo et al. 2012). Foraging behavior can be a good descriptor of species’ niches (Elton 1927), and the variation in these measures can be used to quantify behavioral flexibility and response to disturbance (Sol 2002). Here, we use detailed foraging behavior of Meliphagidae to explore the link between animal behavior and conservation. To provide a more direct understanding of patterns in the dataset, we focused on a number of important axes of resource use and foraging behavior to develop a measurement of foraging niche size per species. We look at how components of the foraging niche vary across the phylogeny using: 1) functional dispersion (FDis) and 2) multivariate analyses to quantify niche size and position. Related species foraged similarly, and foraging behavior showed significant phylogenetic signal. Generalists used a variety of resource acquisition strategies, whereas species with small niches were either highly nectarivorous or insectivorous.

INTRODUCTION

We are now well aware that anthropogenic disturbance is one of the greatest threats to biodiversity (Vitousek 1997, Pimm and Raven 2000, Ewers and Didham 2006). Modern ecologists are given the task of determining how to predict and then mitigate species’ response to 5

such disturbances. Australia is experiencing global mass extinction through land use change

(Lovejoy 2005), and there is now an abundance of evidence that many Australian bird species,

including some Meliphagidae, have drastically declined in the face of these modifications in land

use (Garnett et al. 2011, MacNally et al. 2004). Disturbance caused by climate change will create

dramatic shifts on a continent that has already felt the effects of two hundred years’ of habitat

loss and disturbance through forestry, settlement of people, mining, invasive species, and grazing

(Mackey et al. 2008, Elliott et al. 2012).

How, where, and under what conditions birds forage can help us to understand species’

ecology, how species exploit resources, and in turn, how communities are structured (MacArthur

1972, Pyke 1980, Robinson and Holmes 1982, Shochat et al. 2004). These characteristics also have implications for the role of animal behavior in conservation. The connection between conservation and animal behavior has long been established (Geist and Walther 1974, Lima and

Zolner 1996, Sutherland 1998, Harcourt 1999, Stephens and Sutherland 1999, Linklater 2004,

Blumstein and Fernandez-Juricic 2010, Berger-Tal et al. 2011, Candolin and Wong 2012) and has been used effectively as a lens through which to view a variety of research questions

(Slabberkoorn and den Boer-Visser 2006). Foraging behavior, in particular has proven to be an important component when considering conservation of some species because: 1) specialist species tend to be more susceptible to change and 2) increases in foraging effort have fitness costs (Thomas et al. 2003, Morrison and Lindell 2010, Maslo et al. 2012). It can be a good descriptor of species’ niches (Elton 1927), and the variation in these measures can be used to quantify behavioral flexibility and response to disturbance (Sol et al. 2002). Throughout my dissertation research, I used detailed foraging behavior of Australian Honeyeaters

(Meliphagidae) to explore the link between animal behavior and conservation. In this chapter, I 6

describe the methods that I used to generate quantitative foraging data and summarize those data.

I will present general results and family-wide trends, discuss clade-specific patterns, and explain qualitative trends in the data relevant to subsequent chapters.

Species’ niches have been defined in a variety of ways. Grinnell (1917) defined the niche as the current habitat and geographic distribution of a single species. Under this definition, species are limited by both physical and climatic factors, but the definition is habitat-based. Elton

(1927) described niche as the role that a species plays in a community, and its actual distribution

and functional attributes relating to its trophic position. He used the example of white and black

rhinos with mouths adapted for different food items, but with niches that overlap in every other

way. Using paramecium, Gause (1934) explained that competitive exclusion prevents species

from using the same resources. MacArthur (1958) studied the spatial arrangement of warbler

niches in the northeast United States. Hutchinson (1957, 1978) coined the n-dimensional

hypervolume of abiotic conditions, which put biotic and abiotic variables into multivariate space;

coexistence in this framework is made possible by differences in dimensions of the niche. Chase

and Liebold (2003) synthesized the niche concept as a combination of 1) abiotic requirements for

a species birth rate and death rate to be equal and 2) the effects of that species on abiotic

conditions. In this paper, our definition of niche most closely follows that of Elton.

Phylogenetic niche conservatism (PNC) is the tendency of species to maintain their niche

and corresponding traits over time. Depending upon the reason for niche conservatism (e.g.,

canalization and loss of trait variation versus simply stable and similar selection pressures across

a clade), PNC may be relevant to predicting species’ responses to future change and disturbance.

If species show PNC due to an inability to quickly evolve novel phenotypes (in this case,

foraging strategies), then such species may have difficulty adapting to projected climate change 7

scenarios. In this study we are not able to address whether PNC is due to an inability to adapt to

novel climates. Nevertheless, because of its potential relevance to our study question, we

quantify the phylogenetic signal in foraging traits across the Meliphagidae.

Resource partitioning between sympatric species has long been studied in community

ecology (Connell 1983, Diamond 1978, Tillman 1982). After MacArthur’s work on sympatric

Dendroica in the northeast United States (1958), there have been quite a few classic studies on

foraging ecology of closely related co-occurring species from Lack’s work with Parus (1971) to

Grant’s work with Geospiza (1986) to name only a few. Foraging niche patterns between closely related co-occurring species may tell us something about how a shared ancestry not only relates to resource use, but also to competitive interactions (Cavender-Bares et al. 2009). One might hypothesize that closely related species have higher competition for resources than distantly related species (Elton 1946, Williams 1947). Though Mayfield and Levine (2010) would argue that low competitive abilities causes some species to be eliminated, which leads to trait convergence. Traits might be under the same ecological pressure leading to similarities, but competitive interactions might drive species to diverge in their traits (Schluter 2000, Grant and

Grant 2006).

Foraging niche size could have major implications for conservation. A small foraging niche might make species more susceptible to the effects of climate change and disturbance.

Deciphering which foraging traits are associated with small foraging niches can help us to predict response to disturbance. We can assume that species that specialize on a certain food substrate or foraging behavior will have a smaller overall niche than generalist species with larger foraging niches (Pianka 1973). Species with large niches, or behaviorally flexible species, may be able to use different behaviors or food items and therefore decrease their extinction risk 8

in the face of global changes (Mayr 1965, Ehrlich 1989, Sol 2002). Foraging niche size and

geographic range size are often correlated. The combination of a small foraging niche and a

small range size could have synergistic effects in the face of disturbance. Thus, foraging

behavior provides a link between niche, behavioral flexibility and, possibly, species’ responses

to disturbance and susceptibility to extinction (Sol et al. 2002, Harris and Pimm 2008). We predict that highly nectarivorous and insectivorous species will have smaller foraging niches.

Dependence on nectar in Australian Honeyeaters varies (Recher 1971, Ford and Patton

1977, Patton and Ford 1977, Ford et al. 1979), but many species are highly dependent. Nectar sources can be reduced or even depleted in some seasons (Ford et al. 1979) and there are accounts of nectar specialists (including hummingbirds) taking invertebrates on occasion

(especially during the breeding season) (Wagner 1946, Skutch 1972) because nectar contains no amino acids or proteins (Baker and Baker 1973). Recher (1970) noticed that highly nectarivorous species of honeyeaters would occasionally expend large amounts of energy to capture invertebrates. At his field sites near Sydney in patches of Banksia ericifolia, while watching flocks of Honeyeaters forage on abundant nectar, he would occasionally see them make elaborate flights to the air for minute insects. He saw Red Wattlebirds, which are quite large

Honeyeaters, going as far as 30 meters up to catch small insects. He hypothesized that they take these costly journeys to the air for protein, not energy. We predict to see a positive trend between percent nectar in diet and percent of foraging behaviors to the air that are not to flowers.

Meliphagidae are native to Australia, New Guinea, New Zealand and the Pacific Islands.

In these areas they are one of the most abundant passerine groups in both species and number of individuals (Paton 2000). They are diverse in both behavior and morphology, and they occupy a diversity of habitats (rainforests, eucalypt savannah, riparian sclerophyll forests, mangrove 9

forests, Melaleuca wetlands, etc.), which makes them an ideal family for this study. Many have a

long decurved bill and a prolonged, protrusible and brush-tipped tongue adapted for acquiring

nectar and honeydew, though there is quite a bit of variation in both bill size and shape and

tongue structure, presumably due to the variety of foods taken. It is believed that, as opposed to

other highly nectarivorous species like hummingbirds (Trochilidae), there is only a weak

correlation between bill shape and size and diet (Ford and Patton 1977, Stiles and Stiles1981). A

few ideas have been proposed to explain this lack of correlation between bill size and shape and

diet. Relevant natural history points of interest include that ornithophilous (bird pollinated)

flowers tend to be more abundant and easily accessed in nutrient-poor areas such as Australia (as opposed to South American forests and other habitats), and also that nectarivores are larger in

Australia and supplement their diet with insects (Orians and Milewski 2007). Given that hummingbirds supplement their diet similarly (Wagner 1946, Snow and Snow 1972); this

explanation seems weak at best. While most Honeyeaters take some nectar, some of them eat

predominantly insects or fruit. Some, like the Painted Honeyeater (Grantiella picta), are mistletoe fruit specialists, while others often probe under bark for insects (some species of

Melipthreptus).

Here we present a comprehensive, quantitative dataset summarizing the foraging behavior of a large, diverse, continental radiation of Australian passerines. We describe the patterns in our dataset, including similarities and notable differences between related species, and the foraging characteristics of range-restricted and threatened species. By looking in-depth at

such natural history characteristics as diet, including degree of nectarivory, frugivory and

insectivory, foraging site characteristics (leafiness, height, etc.), propensity to flock, and foraging

maneuver, we will develop a basis for describing foraging niche. Many of the traits show 10

significant phylogenetic conservatism, but there are also some interesting patterns in regards to

co-occurring, closely related species. The level of fine-scale animal behavior data, the

phylogenetic breadth, and the large number of individuals recorded make this a powerful and

flexible dataset that can allow us to look at the relationships between foraging niche size, range

size and sensitivity to disturbance.

METHODS

Design and study area – Over the course of our 18 months in the field, we collected at least 20 independent foraging behavior observations on 74 of 75 species of Australian

Meliphagidae throughout mainland Australia, Kangaroo Island, and Tasmania (Miller and

Wagner 2015). Due to the amount of land covered by this study, study sites ranged widely

(Figure 2.1).

Figure 2.1. Foraging behavior data collection sites where size of the dot is based on sample size (n = 22 – 459).

Foraging Behavior – Over the course of 18 months, we recorded at least 20 independent foraging behavior observations for all 74 species (~7,300 independent foraging observations) according to standardized protocols (Remsen and Robinson 1990), which we modified slightly to fit the study system. Our taxonomy follows that of Joseph et al. 2014. We recorded general site locations using a GPS. Per foraging attack, we recorded details of both the site and maneuver, including foliage density, height of attack, canopy height, distance from the trunk where the attack occurred, food source, and the foraging maneuver. We collected data from sunrise to sunset on all individuals of all Meliphagidae species encountered while walking slowly through 12 the site. In order to prevent observation of the same individuals, we either worked together or communicated with walkie-talkies. If a foraging maneuver was what brought our attention to an individual, we did not collect data on the first maneuver. We did record serial observations for some individuals, but we did not treat them as independent. We weighted these observations by the reciprocal of the number of observations in the series, meaning that a series of observations on the same individual in sum carried the same weight as a single observation from a different individual.

Analyses-Traits- To provide a more direct understanding of patterns in the dataset, we focused on a number of important axes of resource use and ecology. Specifically, we concentrated on traits that represented some of the extreme differences in foraging based on

Remsen and Robinson (1990). We recognized 10 possible foraging substrates: flower, leaf, branch, air, ground, fruit, insect case, web, hanging bark, and woody fruit. Frequently we discuss the proportion of a substrate in a species’ diet. Nectarivory, for example is the proportion of total attacks that were to flowers, and frugivory was the proportion of attacks that were to fruit.

There were seventeen mutually exclusive foraging attack behaviors, which were maneuvers used to acquire food. We discuss percent of the time species used particular maneuvers in the dataset. A few of the more common attack behaviors were: probe, glean, sally- strike and sally hover. Probing is to insert the bill into a substrate (bark, flowers, soil) to acquire food. When an individual gleans, it picks a food item from nearby without using full extension of the legs or neck and is considered to be a very energetically conservative maneuver. To sally is to leave the perch to make an attack and then return to that perch. A sally-strike is to fly out to capture prey without stalling or hovering and a sally-hover is to fly out and hover at a substrate at the end of a sally. While we generally differentiate among different aerial maneuvers, we did 13

sometimes group all such attacks into the category of wing-powered maneuvers. These included

sallies, flush pursues (to remove or flush prey from a perch and then chase it), and flutter chases

(similar to flush purse, but done deliberately vs. on accident). Hang was an important

distinguishing modifier of attack and was a near-perch maneuver that could be further broken

down into direction of the maneuver. When hanging, a bird used its legs and toes to manipulate the body to reach food above, below, or adjacent that would not be accessible from the perch.

Each foraging observation was categorized as coming from a mixed or monotypic species

flock (1), a loose association (0.5), or a single or pair of birds (0). Species’ flockiness scores

were based on the average of these flocking scores. For all traits, rank is ordered from least to

most of the trait in question and is an average, meaning that if three of six species were tied for

most nectarivorous, all three would have a rank of 5. We occasionally provide a range of

numbers within the clade and then provide ± standard deviation (SD) for those numbers.

Four of these traits helped us to understand habitat spatial preferences: horizontal position

(distance from trunk), foliage density, canopy height, and relative height of attack. Horizontal

position is a category (“inner”=1, “middle”=2, “outer”=3, “way outer”=4) describing where the

bird was in the tree, shrub, bare ground (way outer), etc. We used this to see if species preferred a certain area of the vegetation (MacAruthur 1958). Foliage density was a qualitative assessment of how dense the vegetation is. It ranged from “0” to “5”, where “0” = no vegetation within a 1- m imaginary sphere up to “5” = extremely dense, 0-5% of light passes through. The combination of information from both distance from trunk and foliage density has been shown to be informative from a resource-use perspective (Greenburg and Gradwohl 1980, Holmes and

Robinson 1991). Average canopy height and attack height were measured per foraging 14

maneuver. Here we used canopy height and relative attack height, which is the height of the

attack divided by the height of the canopy (with extreme values rounded down to 110%).

After exploring various ways of quantifying foraging niche with species richness and

Shannon diversity measures, we settled upon a metric that is uninfluenced by sample size. We used functional dispersion (FDis, Laliberte and Legendre 2010) to quantify species’ niche volumes. FDis was the weighted mean distance in multidimensional trait space of all foraging observations of a given species from its weighted centroid. As mentioned above, we collected

serial observations, which were weighted. Non-serial single observations had a weight of 1. We

weighted the influence of each observation on FDis by the inverse of the number of observations

in that series. The multidimensional trait space was made with a 10-dimensional non-metric multidimensional scaling ordination (NMDS) based on a Gower distance matrix, with special treatment for ordinal variables (Podani 1999). The Gower distance allowed us to compute the similarity value between individual foraging observations. Thus, all variables can be taken into

account (nominal, ordinal, categorical, and asymmetric binary) and one single distance measure

between each point was derived. A particular distance calculation, e.g. Manhattan for continuous data and Dice’s matching coefficient for categorical data, is used for each variable. These distances between points were used to derive a pairwise distance matrix, which we then used for our ordination. Our choice of 10 dimensions in the NMDS was based on the position of the elbow in a plot showing how stress was reduced with the addition of each additional dimension.

In this paper, we present figures showing the reconstructed evolution of foraging traits

across the Meliphagidae phylogeny (Joseph et al. 2014) and added in 9 species that were not part

of their phylogeny including four Manorina and Melithreptus species (Miller et al. 2013). These figures were made with the contMap function from the R package phytools (Revell 2012). 15

Internal node states are calculated using maximum likelihood, and states along branches were

determined by interpolation according to Felsentein (1985).

In an attempt to boil down the many variables into something more manageable and to

look at trends across the entire family, we used species averages to do a principal components

analysis (PCA). The PCA was done using species averages and includes 15 variables which

describe ecology and foraging behavior. These were centered and scaled. The relationship

between foraging niche size (FDis) and nectarivory was explored using a GLM approach. We

tested for a relationship between hawking (proportion of attacks to the air that are not to flowers)

and nectarivory with both ordinary least squares (OLS) and phylogenetic generalized (confirm

not “general” least squares (PGLS) regressions. We used caper (citation) for the PGLS

regression, allowing it to find the maximum likelihood value for the lambda transformation.

RESULTS

During our 18 months in the field, we recorded at least 20 independent foraging behavior

observations for 74 of the 75 species (~7,300 independent foraging observations) (Miller and

Wagner 2015) (Figure 2.1). Though we spent many field hours searching for the Gray

Honeyeater, we were never able to find any individuals. Independent foraging observations per

species ranged from 22 (for rare or geographically isolated species) to 459 for species that

spanned more of the range that we covered.

1. Green-backed Honeyeater (Glycichaera fallax)

Glycichaera fallax is the only member of a monotypic genus. The species has a limited

range within Australia, and we have a correspondingly limited dataset (n = 20). The species lives

in rainforests, and they foraged in fairly dense vegetation (2.95 ± 0.96 SD), often in the mid to upper canopy with a relative canopy height of 76% (± 0.18 SD) in forests with a mean canopy 16

height of 17.61m ± 2.21SD. They tended to forage in the middle to outer part of branches from

the trunk (2.39 ± 0.50 SD), and had one of the lowest FDis scores (0.21) of any of the study

species (Figure 2.2). They were primarily insectivorous, and stood out as a species that did a lot

of gleaning 86% of the time (ranked 72) and sally-hovering (13%). Most of their attacks were to

leaves (93%). The species was frequently found in mixed species flocks (0.88 ± 0.22 SD). They did a lot of hanging (19%), and focused a considerable proportion of their attacks on dead leaves

(23%). They are known to occasionally take nectar (e.g. Eucalyptus) and fruit, but we did not record these behaviors in our limited observations. 17

0.30

0.25

0.20 Foraging niche size (FDis)

0.15

0.10

0.05

0.00 FuscousHoneyeater BridledHoneyeater Black-chinnedHoneyeater Miner Noisy Tawny-breastedHoneyeater Yellow-tuftedHoneyeater Brown-headedHoneyeater Lewin'sHoneyeater Gray-headedHoneyeater White-napedHoneyeater Macleay'sHoneyeater StripedHoneyeater Yellow-throatedMiner Yellow-tintedHoneyeater Westernwhite-naped Honeyeater KimberleyHoneyeater White-plumedHoneyeater Blue-facedHoneyeater Red-headedHoneyeater RedWattlebird Rufous-throatedHoneyeater CrescentHoneyeater White-gapedHoneyeater White-throatedHoneyeater White-linedHoneyeater EungellaHoneyeater Yellow-plumedHoneyeater MangroveHoneyeater PaintedHoneyeater ScarletHoneyeater Strong-billedHoneyeater Gray-frontedHoneyeater Bar-breastedHoneyeater Rufous-bandedHoneyeater White-earedHoneyeater HelmetedFriarbird Black-headedHoneyeater Tawny-crownedHoneyeater VariedHoneyeater Yellow-facedHoneyeater Yellow-throatedHoneyeater NoisyFriarbird Yellow-spottedHoneyeater White-cheekedHoneyeater YellowHoneyeater CrimsonChat Brown-backedHoneyeater RegentHoneyeater GracefulHonyeater Silver-crownedFriarbird SingingHoneyeater YellowWattlebird LittleWattlebird NewHolland Honeyeater PiedHoneyeater EasternSpinebill Black-earedMiner Purple-gapedHoneyeater YellowChat DuskyHoneyeater LittleFriarbird BrownHoneyeater BlackHoneyeater White-frontedHoneyeater Spiny-cheekedHoneyeater Miner Bell White-frontedChat WesternSpinebill WesternWattlebird Green-backedHoneyeater BandedHoneyeater OrangeChat Gibberbird White-streakedHoneyeater

Figure 2.2. Bar graph of foraging niche sizes (FDis) scores per species in order of largest to smallest. Fuscous Honeyeaters have the largest FDis score (0.34) and White-streaked Honeyeaters have the smallest FDis score (0.14).

2. Tawny-crowned Honeyeater (Phylidonyris melanops now Gliciphila melanops)

The Tawny-crowned Honeyeater is also a member of a monotypic genus. They occur in

the southwest and also in Tasmania. Their FDis score is 0.30 and their FDis rank is 37 (Figure

2.2). They often foraged in short heath (2.56m ± 3.74 SD), 66% (± 0.33 SD) up in the canopy, in

fairly dense vegetation (2.95 ±1.5) and in the outer part of the foliage (2.39 ± 0.86 SD). They

were 46% nectarivorous (Figure 2.3), much of which came from Banksia species. They also

spent a good deal of time on the ground and sallying out from their perches for insects (wing-

powered maneuvers make up 25% of their attacks), and they took no fruit (0%). They ranked low

in their tendency to flock (10). Though the most recent phylogeny does not align this species

with other traditional members of the genus Phylidonyris (pyrrhoptera, nigra, novaehollandiae), it not only resembles them in gross morphology, but foraged in a similar manner (many visits to

Banksia, lots of aerial attacks). They were much less aggressive, found in smaller groups, and

differed in vocalizations from other Phylidonyris species. 19

Green-backed Honeyeater Tawny-crowned Honeyeater Black Honeyeater Dusky Honeyeater Red-headed Honeyeater Scarlet Honeyeater Rufous-banded Honeyeater Rufous-throated Honeyeater Bar-breasted Honeyeater Brown-backed Honeyeater Gibberbird Yellow Chat Crimson Chat Orange Chat White-fronted Chat Banded Honeyeater Brown Honeyeater White-streaked Honeyeater Crescent Honeyeater New Holland Honeyeater White-cheeked Honeyeater Little Friarbird Helmeted Friarbird Noisy Friarbird Silver-crowned Friarbird Macleay's Honeyeater Tawny-breasted Honeyeater Painted Honeyeater Striped Honeyeater Pied Honeyeater Western Spinebill Eastern Spinebill Yellow-throated Honeyeater White-eared Honeyeater Blue-faced Honeyeater Western white-naped Honeyeater White-naped Honeyeater Black-headed Honeyeater White-throated Honeyeater Strong-billed Honeyeater Brown-headed Honeyeater Black-chinned Honeyeater Yellow-spotted Honeyeater Lewin's Honeyeater Graceful Honyeater Kimberley Honeyeater White-lined Honeyeater White-gaped Honeyeater Yellow Honeyeater Yellow-faced Honeyeater White-fronted Honeyeater Purple-gaped Honeyeater Yellow-tufted Honeyeater Bell Miner Black-eared Miner Noisy Miner Yellow-throated Miner Eungella Honeyeater Bridled Honeyeater Spiny-cheeked Honeyeater Little Wattlebird Western Wattlebird Regent Honeyeater Yellow Wattlebird Red Wattlebird Varied Honeyeater Mangrove Honeyeater Singing Honeyeater White-plumed Honeyeater Yellow-plumed Honeyeater Gray-fronted Honeyeater Gray-headed Honeyeater Fuscous Honeyeater Yellow-tinted Honeyeater

0 trait value 0.901

length=8.984

Figure 2.3. Plot of nectarivory by species across the phylogeny. A 0 represents species that take no nectar to species whose diet is composed of 90% nectar.

3. Certhionyx and Myzomela clade: Black Honeyeater (Certhionyx niger), Dusky

Honeyeater (Myzomela obscura), Red-headed Honeyeater (Myzomela erythrocephala) and

Scarlet Honeyeater (Myzomela sanguinolenta)

Members of this clade have long, thin and slightly decurved bills. One might suppose that they focus on tubular flowers, but they tended to take nectar from a diversity of flower types.

This clade is quite nectarivorous. Species ranged from 53% (Scarlet Honeyeater) to 64% nectarivorous (Dusky Honeyeater), which ranked them among other study species from 54

(Scarlet Honeyeater) to 64 (Dusky Honeyeater) (Figure 2.3). We had no records of frugivory in the clade.

Members of the clade tended to forage in relatively open vegetation, ranging from 1.66m

± 1.11 SD to 2.34m ± 1.17 SD for Black Honeyeater and Red-headed Honeyeater, respectively.

Yet they tended to forage in the outer part of trees and shrubs (2.66 ± 0.60 SD - 2.77 ± 0.67 SD), which are otherwise often leafy areas. Thus, they often foraged in the outer canopy on bare and dead branches. They foraged in areas with a variety of canopy heights (4.95m ± 5.08 SD-

19.29m ± 8.77 SD), but they generally foraged in the upper parts of the canopy (66% ± 0.24 SD to 86% ± 0.18 SD). They had high rankings for wing-powered movements, and are ranked from

57-73. One major difference within the clade is the infrequency with which Black Honeyeater used hanging maneuvers (only 3% of the time), but used wing-powered movements 40% of the time (ranked the highest of all Honeyeaters), whereas the others used hanging on average 23% of the time and used wing-powered movements less frequently.

Black Honeyeaters collected many invertebrates in aerial attacks, and often hovered at leaf tips high in the canopy. Eremophila species comprised only half of the species we observed them feeding on, though they are thought to follow flowering events of that genus (Hobbs 1958, 21

Ford 1978). Dusky Honeyeaters were also strongly nectarivorous (rank 64, probe 67% of the time) (Figure 2.3), but they also gleaned 24% of the time. They used fewer aerial attacks, and were less nectarivorous than their bill might suggest (when compared with species like Eastern

Spinebill and Brown Honeyeater). When feeding on nectar, we observed Dusky Honeyeaters on a diverse array of available flowers.

The clade had similar and generally small FDis scores (Figure 2.3); Black and Dusky

Honeyeaters had particularly small niches. They were regularly found in mixed species flocks.

Black Honeyeaters have very little range overlap with the other members of the clade and are found inland. Dusky and Red-headed Honeyeaters are sympatric in large portions of their ranges along northern coastal Australia, but the latter is found primarily in mangroves. Red-headed

Honeyeaters also foraged slightly higher up in available canopy (0.72 % ± 0.25 SD) than Dusky

Honeyeaters (0.66 ± 0.24). Scarlet and Dusky Honeyeaters overlap some in the eastern part of coastal Australia, where Scarlet Honeyeaters foraged quite high in available canopy (0.86% ±

0.18 SD). 22

0.141 trait value 0.345

length=8.984

Figure 2.4 Plot of foraging niche size (FDis) by species across the phylogeny. A score of 0 represents species with smaller foraging niche size and 0.34 represents Honeyeaters with the largest foraging niches.

4. Conopophila clade: Gray Honeyeater (Conopophila whitei), Rufous-banded

Honeyeater (Conopophila albogularis) and Rufous throated Honeyeater (Conopophila rufogularis)

Gray Honeyeater was the only species that we did not get enough observations of to include in our dataset, so we will focus on the other two species in the clade. Rufous-banded and

Rufous-throated Honeyeaters overlap across large parts of their ranges. The Gray Honeyeater shows almost no overlap with either other species; it is also extremely rare throughout its range, and is found in mulga habitat not utilized by either other species. Rufous-banded and Rufous- throated Honeyeaters occupy northern Australia. Their FDis scores were 0.30 and 0.31(Figure

2.2) with a rank for FDis of 41 and 54 for Rufous-banded and Rufous-throated Honeyeaters respectively.

They foraged in fairly dense vegetation, but Rufous-throated foraged in slightly denser vegetation (2.95 ± 1.01SD) than Rufous-banded (2.19 ± 1.23 SD), and in the outer part of the canopy often on the tips of branches. Rufous-throated foraged at a slightly higher relative canopy height (80% ± 0.24 SD) and in taller canopy (8.68m ± 4.77 SD) than Rufous-banded, which had a relative canopy height of 0.68m ± 0.24 SD in an average canopy height of 6.59m ± 3.88 SD.

Rufous-throated was slightly more nectarivorous (39%) than Rufous-banded (35%) and there was very little overlap in flower species utilized. Rufous throated probed 41% of the time and gleaned 38% of the time. Thirty four percent of the time they gleaned leaves and 5% of the time, they went to spider webs. Rufous-banded probe d about the same amount (43%), but they gleaned 47%, which is a bit higher than Rufous throated. Rufous banded gleaned 47% of the time, 40% of the time they went to leaves, and 4% to insect cases. They took very little fruit (1% and 2%) for Rufous-throated and Rufous-banded respectively. The only “fruit” taken was the aril 24

of Acacia holosericea. Rufous-throated used wing-powered movements 21% of the time, but

Rufous-banded used them only 9% of the time. Both species tend to hunt in flocks. We occasionally saw Rufous-breasted hunting low and taking spiders and their prey from webs.

5. Ramsayornis clade: Bar-breasted Honeyeater (Ramsayornis fasciatus) and

Brown-backed Honeyeater (Ramsayornis modestus)

The Ramsayornis clade is sister to the Conopophila clade and foraged similarly. The two

Ramsayornis species overlap only in the far northern part of the Cape York Peninsula. The Bar-

breasted Honeyeater has a large range along the northern coast of Australia. Brown-backed

Honyeaters have a small range within the northern part of Cape York and extending into Papua

New Guinea and adjacent islands. Both species are often associated with Melaleuca-lined

waterways. Brown-backed Honeyeater also occurs in tropical and subtropical mangrove forests.

Both species foraged in fairly dense vegetation 2.21 ± 1.1 SD for Bar-breasted and 2.95 ± 1.10

SD for Brown-backed. They also foraged fairly far from the trunk of the tree (2.70 ± 0.61 SD) for Bar-breasted and 2.55 ± 0.56 SD for Brown-backed. Both foraged about 69% ± 0.23 SD -

70% ± 0.16 SD up in the canopy, but at very different average canopy heights. Bar-breasted

Honeyeaters used an average canopy height of 9.49 m ± 5.7 SD while Brown-backed foraged in higher canopies with an average height of 14.18m ± 7.2 SD. FDis scores were similar for Bar- breasted and Brown-backed respectively (0.29 and 0.30). Like their sister clade, Conopophila, they were very nectarivorous: 52% and 55% respectively.

6. Epthianurinae: Gibberbird (Ashbyia lovensis), Yellow Chat (Epthianura crocea),

Crimson Chat (Epthianura tricolor), Orange Chat (Epthianura aurifrons) and White-fronted

Chat (Epthianura albifrons)

The Gibberbird and chat species are found in the interior and southern Australia, with an outlying population of Yellow Chats on the coast in northern Australia. Gibberbirds are notoriously hard to find and study, and our sample size reflects that (22 independent observations). The foraging niche of this clade was completely unique within the family and largely focused on ground-attacks at insects. FDis scores ranged widely from 0.14 (Gibberbird ranked as the 2nd lowest to 0.29 for Crimson Chat, which is ranked at 29 (Figure 2.2). The

Gibberbird is found in flat pebbled gibber plains in interior Australia where there is little

heterogeneity in habitat, leaving few options for diversity in foraging strategies. They did

employ a few interesting techniques like pecking (1%, ranked as 74) and flaking (0.4%) rocks

aside. From our experience at foraging sites, we think they were taking small ants from the

ground. The Crimson Chat, on the other hand, took a considerable amount of nectar (30% of

attacks), often sally hovered at flowers or leaf tips (8%) and has a correspondingly brushy

tongue. This species also screened (catching insects in sustained, successive aerial attacks) 1% of

the time. We observed Crimson Chats on both Crotalaria cunninghamii and Grevillea

eriostachya. We recorded no other member of this clade taking nectar, and all other chats have

less brushy tongues. We recorded no frugivory for any members of this clade.

Species in this clade move around a lot, and are not always easy to find everywhere that

they occur. They foraged in a variety of vegetation densities with Gibberbird foraging out in the

open (0.57 ± 0.69 SD) to Crimson Chats in slightly more dense vegetation (1.34 ± 1.19). They all

foraged far from the main trunk of plant and were often out in the open. Canopy height ranged 26

from very low for Gibberbirds (0.06m ± 0.08) to nearly a meter for Crimson Chats (0.92m ±

2.15SD). Within these canopy heights they usually foraged at a relative canopy height range of

0.12m ± 0.30 SD to 0.55m ± 0.53 SD for Gibberbirds and Yellow Chats respectively.

They vary dramatically in their tendency to flock from 0.27 ± 0.27 SD (a single or pair of

birds) to 0.93 ± 0.24 (a loose association or flock). We did not see any hanging in this group,

except for Yellow chats, which did 5% of the time. In our small dataset, we witnessed

Gibberbirds using very few wing-powered movements (6%), but the chats ranged from 16-23%.

Lunging is an attack behavior that was more common in Chats than other species. White-fronted

Chats lunged 12% of the time, and Orange Chats lunged 4% of the time. This group stands out as

having the highest proportion of attacks to the ground (ranks 71-74). Yellow Chats are another

species with a limited dataset (n = 22), but we did manage to sample across two subspecies. They

spent less time on the ground than other members of the clade.

7. Banded, Brown, White streaked, Crescent, New Holland, and White-cheeked clade:

Banded Honeyeater, (Certhionyx pectoralis), Brown Honeyeater (Lichmera indistincta), White-

streaked Honeyeater (Trichodere cockerelli), Crescent Honeyeater (Phylidonyris pyrrhoptera),

New Holland Honeyeater (Phylidonyris novaehollandiae) and White-cheeked Honeyeater

(Phylidonyris nigra)

This clade is well represented across much of Australia. The Banded Honeyeater can be

found in the north, and the Brown Honeyeater is widespread throughout Australia. Members of the genus are found on outlying islands, e.g. Papua New Guinea, New Caledonia, and Bali (the only member of the family to cross the Wallace line). Of the approximately 11 species of

Lichmera, only one is found in Australia. White-streaked Honeyeaters have a small range in 27

northern Queensland. Three closely-related species, Crescent, White cheeked and New Holland

Honeyeaters are southern temperate region restricted. All members of the clade were highly

nectarivorous (Figure 2.3). The Phylidonyris species favor Banksia. Most non-nectar attacks

were aerial, and they did very little gleaning. Brown Honeyeaters often foraged low, even when

taller substrates were available, and probed rolled leaves and dead substrates. With the exception

of White-streaked, we have a great deal of data for the Australian members of the clade.

This group was variable in foraging niche size. White-cheeked had the highest FDis score

(0.30) in the clade, and White-streaked had the lowest (0.14), which was the lowest score in our

entire dataset (Figure 2.2). While all species in the clade were highly nectarivorous, there was

some variation. Species that were highly nectarivorous also tended to have low FDis scores. We

observed White-streaked Honeyeaters probing for nectar 90% of the time. Banded Honeyeaters

were highly nectarivorous (76%) (Figure 2.3). We recorded them on 9 flowering plant species.

They tended to go to short-corolla flowers like Eucalyptus (mean flower length = 0.63cm ± 1.09

SD, which ranked them at 17/74). They were also frequently at mistletoe (Amyema). Brown

Honeyeaters were 66% nectarivorous and foraged on 61 different species of flowering plants.

Crescent Honeyeaters are 49% nectarivorous. We observed them taking nectar from 7 species, 2 of which were Banksia species. New Holland Honeyeaters, for which we have a very large data set (n=333), were 60% nectarivorous on 28 different species. White-cheeked Honeyeaters were

58% nectarivorous and foraged on 15 different species. There is no frugivory in this clade.

Banded was previously included in a clade with Certhionyx and Myzomela, (Driskell and

Chrsitidis 2004). Banded has a thinner and more decurved bill than other members of the

Phylidonyris clade. In accordance with this morphological similarity to the previous Certhionyx

members, it was more nectarivorous than most of the other members of the Phylidonyris clade. 28

They all used some form of hanging 15-20% of the time. Most members of the clade used

quite a few wing-powered maneuvers (20-38%), except for White-streaked, which did so only

1% of the time. White-cheeked Honeyeater has the highest sally striking rate (36%) in the

family, and those strikes are always to air. None of them do very much gleaning, and some

members had the lowest gleaning score of the entire family (Banded Honeyeater 3%). They were

similar in their tendency to flock, with the lowest being Banded Honeyeater (0.64) and the

highest being White-cheeked Honeyeater (0.80). As far as their habitat, they tended to forage in

densities of 1.76 ± 1.32 SD to 2.36 ± 1.17 SD, and there was very little variation in their

horizontal distances from the trunk, which was in the outer part of the tree and ranged from 2.64

± 0.65 SD - 2.71 ± 0.56 SD.

8. Friarbird clade: Little Friarbird (Philemon citreogularis), Helmeted Friarbird

(Philemon buceroides), Noisy Friarbird (Philemon corniculatus) and Silver-crowned Friarbird

(Philemon argenticeps)

Members of this clade are found in northern and eastern Australia, Papua New Guinea and adjacent islands. They are large bodied nectarivores and they took some fruit, focused some attention on dead substrates, used sally-pouncing, gleaning (including for lerp), and occasionally took large prey items e.g. Orthoptera, Phasmidae, Mandidae, etc. They were diverse in foraging behaviors and diet.

Foraging niche size varied somewhat within the clade (FDis ranges between 0.27-0.30)

(Figure 2.2) with Little Friarbirds ranked as 14th and Helmeted Friarbirds as 39th. As seen in

other species, high nectarivory scores are often correlated with a smaller foraging niche. Little

Friarbirds were the most nectarivorous of the group (62%) (Figure 2.3) and had the smallest 29

foraging niche. Helmeted Friarbirds were on the other end of the spectrum and were

nectarivorous only 30% of the time, which is still highly nectarivorous for a bird of its size. It is

the largest mainland Honeyeater and the largest Australian Friarbird. Little and Noisy Friarbirds

overlap in their ranges in the eastern part of Australia. We recorded Little Friarbirds on 27

different species, many of which are brush-like in shape e.g. Planchonia, Barringtonia and

Eucaplytus species. Noisy Friarbirds focused 60% of their attacks to flowers and foraged on similar species including Amyema (mistletoe). Thirteen percent of Noisy and Little Friarbird attacks were wing-powered. In the north, Helmeted and Silver-crowned Friarbirds overlap and are more closely related to one another than to the other members of the clade. They were less nectarivorous than the other two members of the clade (30 and 54% respectively), and there was some overlap in plant species that they foraged on. They utilized only about 10% wing-powered maneuvers.

Both Little and Helmeted Friarbirds focused 7% of their attacks on fruit, but Noisy and

Silver-crowned ate less (4 and 2%) (Figure 2.5). They ranged widely in tendency to glean; Little

Friarbird gleaned the least (22%) and Helmeted Friarbirds the most (55%). Helmeted Friarbirds attacked leaves 40% and branches 12% of the time. For Silver-crowned, 32% of attacks were to

leaves and 9% were to branches. For Little and Noisy Friarbirds, only 9 and 10 percent of their

attacks were to air and 5% were to branches. There was some variation in percent of attacks to

leaves, but Helmeted was the highest (40%) and the others ranged from 22-32%. Noisy

Friarbirds screened 1% of the time. 30

0 trait value 0.474

length=8.984

Figure 2.5. Plot of proportion of attacks to fruit (frugivory) by species across the phylogeny. A score of 0 means that we recorded the species taking no fruit and a score of 47 represents 47% of the diet coming from fruit.

Habitat varies across the clade, but most species are found in open forest. Most foraging

attacks occurred in fairly dense areas (2.41 ±1.11 SD - 2.58 ± 1.22 SD) for Silver-crowned and

Helmeted Friarbirds respectively. Helmeted ranked as occupying the densest vegetation of any other species in our dataset, while at the same time remaining the most dominant species in most flocks. All members foraged on middle to outer parts of trees and ranged from 2.50 ± 0.57 SD to

2.63 ± 0.64 SD. Little Friarbirds foraged in average canopy heights of 17.42m ± 7.38 SD, but the other three Friarbirds ranged from 11.23m ± 4.47 SD to 11.80m ± 4.94 SD. Little Friarbirds foraged 73% ± 0.24 SD up in the canopy, Noisy Friarbirds foraged 71% ± 0.27 up in the canopy and Helmeted and Silver-crowned Friarbirds appeared to forage somewhat separately (68% ±

0.30 SD and 74% ±0.22 SD) respectively.

9. Xanthotis clade: Macleay’s Honeyeater (Xanthotis macleayanus) and Tawny-breasted

Honeyeater (Xanthotis flaviventer)

The two members of this clade live in northern Australia and one of them (Tawny- breasted Honeyeater) is also found in Papua New Guinea and adjacent islands. This clade did not have much nectar in their diet, particularly Tawny-breasted. Both species focused largely on dead leaves and other debris caught in vines and on branches. They spent a fair amount of time probing and they foraged at all levels in the forest, but most often in the understory and they were frequently in mixed species flocks. Their ranges do not overlap, but they both can be found in rainforests and mangroves.

Both species had large foraging niches. Macleay’s Honeyeater (n = 58) had an FDis of

0.32, which ranked it as 64th of the dataset and Tawny-breasted (n = 22) had an FDis of 0.33,

ranked at 70th (Figure 2.2). Thirty three percent of Macleay’s attacks were to flowers and Tawny- 32

breasted attacks to flowers were similar (27%) (Figure 2.3). We recorded Macleay’s on six

different species of flowers, three of which were Syzigium species. Tawny-breasted foraged on 2

flowers species: one Syzigium and one Schefflera species. Neither species had any fruit in their

diet. Macleay’s Honeyeater gleaned 32% of the time, and probed 66% of the time. They used wing-powered maneuvers 3% of the time and they used hang maneuvers to attack 31% of the time. Substrates attacked include: 2% hanging bark, 3% insect cases, 47% leaves, 14% branches and 17% of the time, the substrate was dead plant material. Tawny-breasted used gleaning 45% of the time, probing 45% of the time, hanging to attack, 26% of the time, wing-powered maneuvers 7% of the time to various substrates: 4% hanging bark, 58% leaves, 9% to the air, and

32% of the time the substrate was dead plant material.

They varied drastically in their foraging habitat. Macleay’s foraged in leafy vegetation with a density of 2.57 ± 1.38 SD. They foraged near the middle of branches out from the trunk

(2.09 ± 0.60 SD). Tawny-breasted foraged in less dense foliage (1.93 ± 0.97 SD) between the middle and outer part of the tree (2.50 ± 0.73 SD). This clade differed slightly in their tendency to flock. Macleay’s, was somewhat less likely to flock (0.58) than Tawny-breasted (0.77), which we saw in pairs or in mixed species flocks in the rainforest understory. Average canopy height for Macleay’s is 22.30m ± 6.27 SD and they foraged 62% ± 0.28 SD up in the canopy. We saw them making attacks from close to the ground to high up in the canopy. Macleay’s foraged in fairly short canopies (2.56m ± 5.26 SD) and low within them (28% ± 1.93 SD).

10. Painted Honeyeater (Grantiella picta)

The Painted Honeyeater is the only member of a monotypic genus. They occur in the interior southeast part of Australia in open forest, box-ironbark woodland, and in fruiting 33

mistletoe. They had an FDis score of 0.31, ranking them at 46th. They were the most frugivorous

species in our entire data set (47%) (Figure 2.5), and we observed few attacks to flowers (16%)

(Figure 2.3). Both attacks to fruit and attacks to flowers were on one plant species: Amyema quandang, a type of mistletoe. Painted Honeyeaters probed 16% of the time and glean 81% of the time. They used hanging to attack 34% of the time and used wing-powered movements only

2% of the time.

Twenty five percent of their foraging substrates were “intriguing,” ranking them as the species that uses the highest proportion of behaviors categorized as intriguing. Intriguing is a combination of unique substrates like hanging bark, insect cases, woody fruit, and spider webs.

For example, 25% of their attacks are to webs. This species takes many arthropods. We once observed them pull a rolled leaf from a spider web, crack it open, and eat the spider inside.

They foraged in fairly leafy vegetation (2.53 ± 1.73 SD) in the middle to outer part of trees (2.50 ± 0.73 SD). Average canopy height for them was 7.70m ± 2.50 SD and they foraged

75% ± 0.24 SD up in that available canopy. Like closely related species (the Xanthotis clade and the Striped Honeyeater) they were occasionally found in flocks (0.77 ± 0.38 SD).

11. Striped Honeyeater (Plectorhyncha lanceolata)

The Striped Honeyeater is another member of a monotypic clade and is widespread in eastern interior Australia and on the east coast in some places. They can be shy and difficult to observe. There were a few interesting similarities with the closely related Painted Honeyeater,

mainly in their use of intriguing and creative bill maneuvers, but they were less frugivorous than

the Painted Honeyeater. Both species gleaned much more than their relatives. But, Striped

Honeyeaters were also a unique species in their foraging behavior. There was little nectar in their diet, but they did visit some mistletoe. They regularly foraged on woody fruits and insect cases, 34

e.g. Psychidae bags. We observed them using their feet to hold insect cases, pull, pry, probe and

other unique foraging techniques, ranking them just below Painted Honeyeaters for intriguing

substrates attacked. They also used creative bill maneuvers 20% of the time, ranking them at 68.

“Bill creative” is a compilation of attacks that include: pry, peck, pull, hammer, gape, probes not

to flowers, and flake.

Striped Honeyeaters had a large foraging niche (FDis 0.32) (Figure 2.2), which ranks

them as 63. They were similar to Painted Honeyeaters in their low percent of attacks to flowers

(17%) (Figure 2.3). We observed them on five different species of flowers, including two

Eucalyptus species, Amyema, Loranthaceae, and Eremophila longifolia. More of their attacks

(40%) were to leaves. But, unlike Painted Honeyeaters, they are only 7% frugivorous (Figure

2.5) on three species: Geijera parviflora, Monotoca scoparia and Pittosporum undulatum. This species did not use any wing-powered movements. They did hang to attack 44% of the time.

They used pulling 3% of the time, which we only ever also saw in Melithreptus. They were

usually in monotypic flocks (0.70 ± 0.44 SD). They foraged in fairly leafy areas (2.34 ± 1.14 SD)

in the middle to outer part of the tree (2.52 ± 0.57 SD) in average canopy heights of 8.13m ±

3.73 SD.

12. Pied Honeyeater (Certhionyx variegatus)

Another single species in a monotypic genus, the Pied Honeyeater is rare throughout

inland Australia and often found with Black Honeyeaters. Pied Honeyeaters were highly nectarivorous, but they also took a fair amount of fruit according to our data set. Many of our observations came from a large group we found in otherwise undisturbed arid shrub lands feeding on invasive African Boxthorn (Lycium ferocissimum). They have been seen on other 35 occasions eating other fruits. We did not see them on Eremophila as much as the literature would suggest we would.

This species was 39% nectarivorous (Figure 2.3) on four species: Amyema preissi,

Crotalaria cunninghamii, and two species of Eremophila including galeata. We observed 12% of attacks to fruit (Figure 2.5) on Lycium ferocissimum. Pied Honeyeaters gleaned 6% of the time, probed 40% of the time, and we observed no hanging or wing-powered movements.

Substrates foraged on beyond fruit and flowers included branches (14%) (Figure 2.6).

Members of this species foraged in an average foliage density of 2.33 ± 1.14 SDand mostly between the main trunk of the tree and the outer part of the tree (2.66 ± 0.57). Canopy height averaged 3.12m ± 1.64 SD and they foraged 80% ± 0.21 up in that canopy. Pied

Honeyeaters had a strong tendency to flock (0.88 ± 0.24), and we occasionally observed them in mixed species flocks. 36

0 trait value 0.742

length=8.984

Figure 2.6. Plot of proportion of attacks to branches by species across the phylogeny. Species with score of 0 made no attacks to branches and species with a score of 0.74 used attacks to branches 74% of the time.

13. Spinebill clade: Western Spinebill (Acanthorhynchus superciliosus) and Eastern

Spinebill (Acanthorhynchus tenuirostris)

These two species have no overlap in their ranges and occur in eastern and southern

Australia. They were very nectarivorous and appeared to visit tubular flowers more than other

Australian Honeyeaters. When not taking nectar, they tended to chase insects in presumably energetically costly aerial pursuits. Perhaps to counter this, when making aerial pursuits, they often caught large invertebrates e.g. Tabanidae. Their foraging niches were quite small compared to other members of the family: 0.25 for Eastern Spinebill and 0.23 for Western Spinebill (Figure

2.2).

Western Spinebills attacked flowers 67% of the time on six different species and 64% of the time for Eastern Spinebill (Figure 2.3) on 31 totally different species. Western spinebill foraged on long and tubular flowers (2.58cm ± 0.91SD) ranked as 68th for mean flower length

and Eastern on flowers of 1.35cm ± 1.19 SD) ranked only at 51. For example, we observed

Western Spinebill foraging on solitary Adenanthos flowers below New Holland Honeyeaters

foraging on flowering Banksia. Neither species had any fruit in their diet. Both gleaned from

leaves about 8% of the time. Western Spinebill would hang to attack 9% of the time and Eastern

Spinebill did so 13% of the time.

When not feeding on flowers, they were generally catching insects in aerial pursuits.

Combined wing-powered movements comprised 21% of attacks done by Western Spinebill and

30% for Eastern. Both Spinebills used flush pursue 4% of the time, a maneuver used only by

these two species. Other species would jump into foliage and then chase things that flew out, but we’ve classified these observations as flutter-chases. In Eastern spinebill, individuals, especially

females, would fly low through shrubs, landing on the bare middle branches, flaring their tails 38

and pursuing insects that they flushed, both within the shrubs and just outside the foliage.

Western Spinebills used hanging to attack 9% of the time, but Eastern Spinebills used it 13% of

the time.

They foraged in vegetation that ranges from 2.11 ± 1.19 SD to 2.24 ± 0.99 SD in density

and in the middle part of the vegetation 2.40 ± 0.71SD to 2.63 ± 0.63SD for Eastern and Western

Spinebills, respectively. Western foraged in lower vegetation (3.50m ± 3.49 SD) than Eastern

Spinebills (9.45m ± 6.25 SD) and both were found in loose associations or flocks.

14. Nesoptilotis clade: Yellow-throated Honeyeater (Nesoptilotis flavicollis), White-eared

Honeyeater (Nesoptilotis leucotis)

Members of this clade have no overlap in their geographic range. The White-eared

Honeyeater occurs in eastern and southern Australia, including Kangaroo Island, while the

Yellow-throated Honeyeater is a Tasmanian endemic. They did not frequently visit flowers, but

instead focused most of their attacks to branches (Figure 2.6), presumably probing for honeydew.

Both species would hang up frequently, including on the trunk itself. Both have a foraging niche

size of 0.30.

Nectarivory ranged from 21% for White-eared, which fed on 10 different species to 44%

for Yellow-throated Honeyeaters, which only went to Banksia marginata during our data

collection (Figure 2.3). Though it does exist outside of Tasmania, we have no accounts of White-

eared going to B. marginata. Neither species has any fruit in their diet. Yellow-throated gleaned

47% of the time and White-eared only 27% of the time. Yellow-throated probed 37% of the time

(often under bark) and White-eared 61% of the time. It is likely that most of the time when they are probing under bark, they are taking honeydew or manna. Thirty-one percent of Yellow- 39

throated attacks were to branches and 9% were to the air. White-eared focused 13% of attacks to air and 6% to branches (Figure 2.6). Wing-powered movements made up 16% of Yellow- throated attacks and 12% of White-eared attacks. Some of those wing-powered maneuvers were flutter-chases, which Yellow-throated used 5% of the time and White-eared Honeyeater only 1% of the time. Yellow-throated used hanging to attack more often (35% of the time) than White- eared (18% of the time) does. Of those hanging maneuvers, most were hang-ups: Yellow- throated would hang up 35% of the time and White-eared 34%, which are some of the highest percentages in the dataset.

Yellow-throated is very widely distributed throughout Tasmania, yet, they almost always occurred as individuals or pairs. We never saw them in monotypic flocks, but they were occasionally in loose associations and flocks (0.68). White-eared Honyeaters were widely distributed across continental Australia, yet like its sister species, they were less likely to flock

(0.40) and generally found alone, in pairs, or occasionally in loose associations. On only one occasion did we ever witness a flock of White-eared Honeyeaters. Both birds occurred in open leafy vegetation (1.19 ± 1.19 SD for Yellow-throated and 1.60 ± 1.25 SD for White-eared).

Yellow-throated foraged closer to the main trunk of the tree (1.94 ± 0.80 SD) and White-eared foraged further out (2.25 ± 0.34 SD), in canopies that were 8.54m ± 5.87 SD and 17.19m ± 11.32

SD, respectively.

15. Entomyzon and Melithreptus clade: Blue-faced Honeyeater (Entomyzon cyanotis),

Western White-naped Honeyeater, (Melithreptus chloropsis), White-naped Honeyeater

(Melithreptus lunatus), Black-headed Honeyeater (Melithreptus affinis), White-throated

Honeyeater (Melithreptus albogularis), Strong-billed Honeyeater (Melithreptus validirostris), 40

Brown-headed Honeyeater (Melithreptus brevirostris) and Black-chinned Honeyeater

(Melithreptus gularis)

This 8-member clade occurs throughout continental Australia, including two endemic

species in Tasmania. Blue-faced Honeyeater, the largest member of this clade, is also found in

parts of adjacent Papua New Guinea, as is the White-throated Honeyeater. The clade was

generally not highly nectarivorous, though Blue-faced visited more flowers than the rest of the

clade. Members of this clade would often hang while foraging and did a lot of leaf gleaning.

They have a unique jaw morphology that translates into unique foraging techniques. Specifically,

they employ a foraging technique known as gaping, where the bill is inserted into a substrate,

e.g. a rolled leaf, and then used to lever open and gain access to food within that substrate. This

unique ability is likely related to their ectethmoid-mandibular articulation (Bock & Morioka

1971). Gaping is used by several groups including European starlings (Sturnus vulgaris),

Brown-headed Cowbirds (Molothrus ater) and New World Blackbirds (Bernhardt et al. 1987).

This clade was fairly similar in their foraging niche size with a range of 0.31-0.33 (Figure

2.2). Species in this clade usually occurred in flocks with other Melithreptus. There was some variability in their tendency to go to flowers, from as low as 1% for White-naped Honeyeaters to

as high as 46% for Blue-faced Honeyeaters (Figure 2.3). Blue-faced is large compared to many

other nectarivores. The only member of the clade that we saw going to fruit was Blue-faced

Honeyeater, when we observed it feeding on Mangifera indica (mango) (Figure 2.5). The clade was variable in their tendency to hang. Blue-faced used hang maneuvers least frequently (32% of the time) and Black-chinned used hanging the most (72%). Most used few wing-powered maneuvers (1-8%) except for Western-white cheeked (22%) and White-throated Honeyeater

(27%). Three species in the clade gaped: Blue-faced (3%), White-gaped (5%), and Strong-billed 41

(8%). All members of the clade did some probing, but Blue-faced stood out as doing more than other members (62%) and Black-headed stood out as doing very little (20%). Like, the Manorina

clade, they focused on attacks to branches (Figure 2.6) with a range from 6% for White-throated

Honeyeaters to 74% for Strong-billed Honeyeaters. Strong-billed attacked hanging bark 16% of

the time and Black-headed 4% of the time. Attacks to leaves ranged between 42-54% for most

species, except for Strong-billed, which was only 3%, and Blue-faced, which was only 31%.

Strong-billed and Black-headed Honeyeaters are Tasmanian endemics. While Strong-

billed is generally in forests, and can be found across most of Tasmania, Black-headed

Honeyeaters are mostly in mature dense vegetation on the eastern part of the island. Both species

did a fair amount of hanging, but Strong-billed did much more probing and had a higher

tendency to attack branches. Black-headed did more gleaning (usually to leaves or branches)

than any other member of the clade. Like White-naped, we have observed them lapping up

pooled nectar at the base of Banksia inflorescences. Strong-billed are almost always with

monotypic flocks, but occasionally those groups were mixed in with mixed species flocks. They

foraged from ground level to high up in the canopy and they had the highest percentage of

creative bill techniques in the entire dataset (65%) including pulling (3%). They foraged closer to

the trunk of the tree than any other species in the data set (1.89 ± 0.64 SD), in vegetation that is

not very dense (1.06 ± 1.07 SD), in the second tallest vegetation in the dataset with an average

canopy height of 21.7m ± 13.06 SD. We often watched them high up in Eucalyptus regnans

forests, though we occasionally found them foraging on or near the ground. Most of their attacks

were 88% ± 0.15 SD up in the canopy. These species are almost always in flocks, both mixed

species and monotypic.

16. Meliphaga clade: Yellow-spotted Honeyeater (Meliphaga notata), Lewin’s

Honeyeater (Meliphaga lewinii), Graceful Honeyeater (Meliphaga gracilis), Meliphaga fordiana

(Kimberley Honeyeater) and White-lined Honeyeater (Meliphaga albilineata)

This clade has five species in Australia, but there are six more in Papua New Guinea,

Indonesia and East Timor. They are a monophyletic lineage with cryptic diversity (Norman et al.

2007). They are generally wet forest birds, but two species live in sandstone gorges of northern

Australia and are divergent from other members of the genus (Miller and Wagner 2014, Miller and Wagner 2015). They were the most frugivorous Honeyeater clade in Australia (Figure 2.5).

Most of the species in this clade also take some nectar and seem to have a predilection for blue- colored fruits, e.g. Elaecarpus (Figure 2.5). They focus some attention on dead substrates, including probing into dead wood.

Their foraging niche size varies, but Graceful Honeyeater has the smallest (0.29) and

Lewin’s has the largest (0.33), ranking it as having the 7th largest foraging niche in the data set

(Figure 2.2). Nectarivory varies across the clade from 19% for Lewin’s to 49% for Kimberley

Honeyeaters, but all members of Meliphaga took some nectar (Figure 2.3). We did not record

White-lined consuming fruit, but others have observed it (White 1917, Deignan 1964, Storr

1977). Other members took between 8% and 25% fruit for Graceful and Lewin’s Honeyeaters, respectively. Every species except White-lined was within the top seven most frugivorous

Honeyeater species in Australia.

Most Meliphaga used complex, creative bill maneuvers (White-lined 15%, Lewin’s 14%,

Graceful and Yellow-spotted 6%, and Kimberley 3%). White-lined Honeyeaters probed more frequently than other Meliphaga (53%), and thirty percent of their attacks were directed at branches (Figure 2.6), which is also the highest in the clade. Yellow-spotted probed the least 43

frequently. 58% of the time they gleaned, which is much higher than other members of the clade.

All members of the clade occasionally made attacks to leaves, but Graceful did so most often

(39%). Wing-powered movements were used most often by Lewin’s (27%). We witnessed hovering in all members, but particularly in Graceful (11%) and Lewin’s (9%). Graceful almost never used hang maneuvers to attack, but the others did so occasionally; Kimberley Honeyeater did so 30% of the time.

They had a tendency to be alone, in pairs, or in loose associations. We found White-lined

to forage in pairs or small groups in the early morning and then to disperse by the afternoon.

Graceful foraged in the densest vegetation (2.99 ± 1.00 SD), and White-lined in the least dense

(1.95 ± 1.27SD). Canopy height ranged from 5.54m ± 3.74 for Kimberley Honeyeater to 19.00m

± 8.10 SD for Graceful Honeyeater, which foraged in wet forest in northern Queensland. There was some variation in relative attack height, Yellow-spotted foraged only 53% ± 0.31 SD up in

the canopy and White-lined foraged 72% ± 0.29 SD up in fairly short canopy.

17. Stomiopera clade: 17a. Stomiopera unicolor – White-gaped Honeyeater, 17b.

Stomiopera flavus – Yellow Honeyeater

White-gaped and Yellow Honeyeater occur in northern Australia and they are a unique

clade in terms of foraging. They visited many flowers, but also took some fruit and employed the

gape behavior. Yellow and White-gaped Honeyeaters probed branches, and White-gaped also spent a great deal of time searching dead substrates. White-gaped had a notable penchant for

Planchonia flowers.

They had foraging niche sizes of 0.30 for Yellow Honeyeater and 0.31 for White-gaped

Honeyeater (Figure 2.2). White-gaped went to flowers 35% of the time on 17 different species 44

including 2 Planchonia species. Yellow Honeyeater went to flowers 30% of the time on 7

species with overlap in only a couple of them (Figure 2.3). They had a small amount of fruit in

their diet: 3% for White-gaped and 5% for Yellow Honeyeaters (Figure 2.5). White-gaped used

hang to attack 22% of the time, and Yellow Honeyeater did so 14% of the time. Yellow

Honeyeater used many more (27%) wing-powered movements than White-gaped Honeyeater

(5%). Both species did a fair amount of gaping: White-gaped 5% and Yellow 2%. We observed

Yellow Honyeaters lever bark up, presumably to acquire honeydew. They foraged in different parts of the tree; White-gaped tended to be closer to the trunk than Yellow. Average canopy height was 11. 62m ± 4.77 SD and 77% up ± 0.19 SD for Yellow Honeyeater, and 9.33m ± 4.94

SD and 63% ± 0.24 SD up for White-gaped Honeyeater. Both of these species duet, which is unique in the family. Both species did join mixed species flocks and are also occasionally found in small groups away from other species.

18. Yellow-faced Honeyeater (Calligavis chrysops)

This is the sole Australian member of this clade. The other two species are found in

Papua New Guinea. The Yellow-faced Honeyeater is found in eastern Australia. They used hanging frequently (15%), often downwards (40% of hangs were in this direction), to glean from leaves. They seemed to favor Eucalyptus foliage, even where those species occurred infrequently. They readily took nectar (47%) of Eucalyptus and other species (Figure 2.3). In many ways this species is similar to clade 20 in that they would hang down frequently and gleaned often from leaves, but they were much less aggressive than that clade. They also seemed to frequently seek out Eucalyptus. Even in rainforest habitats of north Queensland, we saw them foraging in solitary Eucalyptus flowers. They use aerial and wing powered attacks frequently 45

(24%). We did not observe them eating fruit. Average canopy height was 14.63m ± 7.45SD and

they foraged 71% ± 0.27 SD up in the canopy.

19. White-fronted Honeyeater (Phylidonyris albifrons)

The White-fronted Honeyeater occurs in the southern and western interior of Australia.

Morphologically and foraging-wise, this species looks a lot like Phylidonyris, but sits by itself

phylogenetically. They are “nomadic” and difficult to find reliably. They had a relatively small

foraging niche (0.25) (Figure 2.2) and they were largely nectarivorous (65%) (Figure 2.3) on 13

different flower species, meaning that they also probed frequently (67%). They used hang

maneuvers 8% of the time and also used many wing-powered attacks (22%), 17% of those were

sally striking. Average canopy height where they foraged was fairly short (5.01m ± 3.29), and

they forage about 65% ± 0.32 up in the canopy. They had a high flocking score (0.88).

20. Purple-gaped and Yellow-tufted Honeyeater clade: Purple-gaped Honeyeater

(Lichenostomus cratitius) and Yellow-tufted Honeyeater (Lichenostomus melanops)

Both species occur in southern Australia and are largely allopatric. They were quite

nectarivorous (33% for Purple-gaped and 34% for Yellow-tufted) (Figure 2.3), including many

visits to Eucalyptus, Myrtaceae, and Banksia species. Purple gaped probed 38%, gleaned 49%,

used wing-powered maneuvers 12% of the time, and used hang 8% of the time. As far as

substrates attacked, 48% of maneuvers were to leaves, 11% were to branches, and 33% were to

flowers. Yellow-tufted gleaned 32%, probed 51%, used wing-powered maneuvers 17% and used

hang 28%. They attacked leaves and branches 24%, flowers 34%, and air 15%. Foliage density was variable in this clade. Purple-gaped foraged in dense vegetation (2.37 ± 1.26 SD), whereas 46

Yellow-tufted foraged in more open vegetation (1.90 ± 1.33 SD). They were also very aggressive and often occurred in colonies. They were difficult to find and seem habitat-specific—Purple-

gaped was almost always found in mallee. Average canopy height for Purple-gaped was 5.90 m

± 3.30 SD, 83% ± 0.16 SD up. Yellow-tufted foraged in much higher canopy (12.39m ± 6.15

SD), 66% ± 0.28 up in the canopy. Yellow-tufted had a higher tendency to flock (0.82) than

Purple-gaped Honeyeaters (0.68). Neither species had any fruit in their diet.

21. Manorina clade: Bell Miner (Manorina melanophrys), Black-eared Miner (Manorina melanotis), Noisy Miner (Manorina melanocephala) and Yellow-throated Miner (Manorina flavigula)

Manorina are distributed throughout Australia. The Black-eared Miner is restricted to mature mallee in southern Australia and is considered endangered (IUCN) due to genetic swamping from the Yellow-throated Miner and from habitat destruction (Baker-Gabb 2007). The clade varied in the amount of gleaning that they did. Both Bell and Black-eared Miners did much more gleaning than the other two members of the clade. Bell Miners gleaned from leaves, taking lerp (dome-like coverings of certain psyllid bugs) leaving psyllids (resulting in dieback) (Stone

1996). They did a lot of hanging, and all species in the clade were very aggressive and found in monotypic flocks with a complex breeding system. They also were somewhat nectarivorous and sometimes used gaping.

This clade varied drastically in foraging niche size (0.25 for Bell Miner and 0.33 for

Noisy Miner) (Figure 2.2). Bell and Black-eared Miners gleaned more than any other Australian

Meliphagidae (92%). Noisy Miners gleaned only 62% of the time and Yellow-throated gleaned even less at 35%. Bell Miners went to leaves 79% of the time. Forty-eight percent of their attacks 47

were made while hanging, which places it in the top 7 hanging species in our dataset. Bell

Miners took no fruit or nectar and we observed them sally-pouncing 3% of the time. Noisy

Miners went to flowers 13% of the time, Yellow-throated 35% and Black-eared Miners only 4%

(Figure 2.3). Black-eared Miners are the only species in the clade that had fruit in their diet (4%) for one plant species: Cassytha. They also frequently attacked leaves (60%). Bell Miners did no probing but other members ranged from 6% (Black-eared Miners) to 43% (Yellow-throated

Miners), which makes sense given their percentage of attacks to flowers. Black-eared Miners gaped 2%. Wing-powered maneuvers varied greatly throughout the clade, and ranged from 1%

(Black-eared Miner) to 21% (Yellow-throated Miner).

One unique behavior used by Yellow-throated Miners is a sally-stall, which they do 6% of the time. They are in the top 3 species who use this maneuver most. They also use creative bill maneuvers 8% of the time. Noisy Miners flutter-chased 51%. Attacks to branches (Figure 2.6) ranged from 12% (Yellow-throated Miner) to 24% (Noisy Miner). Black-eared and Noisy

Miners occasionally went to the ground (8% and 5% respectively).

Foliage density varied from 1.94 ± 1.36 SD to 2.42 ± 1.37 SD, and they generally foraged in the middle to outer parts of trees. Canopy height ranged from 7.8m ± 3.45 SD for Black-eared

Miners to 15.54m ± 2.94 SD for Bell Miners. Most attacks occurred from 60% ± 0.23 SD up in the canopy or higher.

22. Bolemoreus clade: Eungella Honeyeater (Bolemoreus hindwoodi) and Bridled

Honeyeater (Bolemoreus fernatas)

These species are range-restricted montane rainforest species in northeastern Australia.

Eungella was not found until the 1970’s and then was described later (Longmore and Boles

1983). They gleaned leaves frequently, and Bridled would hang to do so. Bridled would cling to 48

trunks (hang up) to probe at moss and bark. Both species would flutter-chase after insects.

Bridled, in particular, seemed to visit a wide breadth of flowers, including many small, white

flowers that characterize Gondwanan rainforests. We often saw Eungella Honeyeater on

Freycinetia flowers. Both species were frequently found in monotypic groups.

Their foraging niches were quite different. Eungella had an FDis of 0.31 and Bridled’s was 0.34, which is the second largest niche in the data set. These two species were similar in their percent nectarivory (29% for Eungella and 35% for Bridled Honeyeaters) (Figure 2.3).

Eungella foraged on two species during our data collection: Freycinetia excelsa and a

Loranthaceae species. Bridled Honeyeaters foraged on 7 flower species, including three

Syzigium species. Neither took any fruit. They differed markedly in propensity to hang. Eungella used hang only 1% of the time while Bridled did so 28% of the time. Of those hanging maneuvers, they would hang sideways most frequently (35%). They often did this on trunks of trees to explore areas between the trunk and the vines that grow along them. They were similar in their use of wing-powered maneuvers—23% and 24% of the time for Bridled and Eungella, respectively. Eungella gleaned 44% of the time and Bridled 40%. Eungella probed 32% and

Bridled 38%. For Eungella, if attacks were not to flowers, they were to branches 17% of the time, air 10%, or leaves 43%. For Bridled, attacks that are not to flowers include: branches 16%, air 14%, and leaves 33%. They flutter-chased 5% of the time and Bridled do 4%.

They were quite different in their tendency to flock. Eungella were often seen as individuals or pairs and only occasionally in small groups (0.30), while Bridled were frequently in flocks (0.63). They were somewhat similar in the density of vegetation that they were found in (2.04 ± 1.20 SD for Eungella and 2.34 ± 1.41 SD for Bridled), but they differed on where in the canopy they tended to forage. Bridled foraged closer to the trunk of the tree (2.35 ± 0.77 SD) 49 and Eungella was further out (2.50 ± 0.63SD). Eungella foraged in very tall subtropical rainforest canopy (28.88 m ± 5.18 SD) and forage 56% ± 5.18 SD up in the canopy. That was the highest canopy habitat that any Australian Honeyeater used. Bridled also foraged in high subtropical rainforest (21.13 m ± 6.56 SD) and within that canopy, attacks occurred, on average

66% ± SD 0.26 up in the canopy.

23. Anthochaera, Acanthagenys, and Xanthomyza clade includes: Spiny-cheeked

Honeyeater (Acanthagenys rufogularis), Little Wattlebird (Anthochaera chrysoptera), Western

Wattlebird (Anthochaera lunulata), Regent Honeyeater (Xanthomyza Phrygia), Yellow

Wattlebird (Anthochaera paradoxa), Red Wattlebird (Anthochaera carunculata)

Little and Red Wattlebirds are found across southern Australia, Western Wattlebird is in the southwest corner of Australia, Spiny-cheeked Honeyeater is found throughout inland

Australia, Yellow Wattlebirds are Tasmanian endemics, and Regent Honeyeaters are in the southeast of Australia and are endangered (IUCN) with an estimated breeding population of

1,500 individuals (Liu et al. 2014). The foraging niche of this clade was incredibly variable.

They were all similar in propensity to visit flowers. Regent Honeyeaters and Red Wattlebirds seemed to prefer Eucalyptus flowers, while Little and Western Wattlebird preferred Banksia.

Yellow Wattlebird is the largest Meliphagidae in the world. We had few observations for Yellow

Wattlebirds on flowers, but they are known to take nectar regularly. There was only a very small amount of frugivory in the clade. They took many insects from the air, but employed a few otherwise rarely seen maneuvers: sally-pounce, sally-glide and sally-stall and they also visited sap flows. 50

Foraging niche size varied from Western Wattlebird (0.21), which was quite low to Red

Wattlebird (0.31), dramatically higher (Figure 2.2). This was one of the most nectarivorous clades, the other being the Myzomela/Certhionyx clade (Figure 2.3). Yellow Wattlebird stood out

as having much lower nectarivory scores than the others (6%). Western Wattlebird was the most

nectarivorous species (79%), and fed on 4 species, including 2 Banksia species, Adenanthos, and

a Eucalyptus. Other members took at least 45% nectar. Yellow Wattlebirds gleaned frequently

(72%), which ranks them in the top three species for gleaning. Other members of the clade

gleaned occasionally (4%-20%). Fifty-seven percent of Yellow Wattlebird attacks were to

branches and 33% were to leaves. Those numbers are much lower for the other more

nectarivorous members of the clade. The most nectarivorous member (Western Wattlebird) was

also the member that had the highest rate of probing and the 2nd highest in the family within

Australia. Frugivory was low (Figure 2.5). Little and Western Wattlebirds and Regent

Honeyeaters took no fruit, Yellow and Red Wattlebirds took 1%, and Spiny-cheeked

Honeyeaters took 11% (for 7 different species). We only saw Red Wattlebirds take fruit on one

occasion, and that was the Kangaroo Island subspecies.

Hanging was used most frequently by Regent Honeyeaters (59%), which was high

in the dataset. Others used some hanging. Wing-powered movements were used variably: 9% for

Yellow Wattlebird up to 25% for Little Wattlebird. Red and Yellow Wattlebirds used sally-glide

maneuvers 3% and 1% of the time, respectively. These behaviors were much less common in

other species. Little Wattlebird sally-stalled above the canopy 5% of the time. Spiny-cheeked

Honyeaters sally-hovered 1% of the time, which is impressive for a bird of that size. Red

Wattlebirds sally pounced to trunks 3% of the time. Yellow Wattlebirds also used reaching 9%

of the time (more than any other species in the data set). 51

Tendency to flock was variable and ranged from 0.45 for Western Wattlebirds, which tended to forage alone or in pairs, to 0.81 for Spiny-checked, which were more frequently in flocks. Foliage density varies from 2.06 ± 1.46 SD (Red Wattlebird) to 2.59 ± 1.24 SD (Spiny- cheeked Honeyeater) and distance from the trunk varied from 2.38 ± 0.77 SD (Yellow

Wattlebird) to 2.95 ± 0.49 SD (Western Wattlebird). Canopy height varied between 5.94 m ±

3.60 SD for Western Wattlebird to as high as 21.39m ± 4.56 SD for Regent Honeyeater. Western

Wattlebirds occur in coastal woodlands, heaths, and gardens. Regent Honeyeaters are found in tall box-ironbark forests and spend most of their time high up in the canopy (81% up ± 0.16 SD).

24. Gavicalis clade: Varied Honeyeater (Glavicalis versicolor), Mangrove Honeyeater

(Gavicalis fasciogularis) and Singing Honeyeater (Gavicalis virescens)

Within this clade, there are two mangrove-restricted species that are found along the northeast coast and into Papua New Guinea. According to the most recent phylogeny, these species do not appear to be sister to each other. Members of the clade were largely nectarivorous, but they also took some fruit, gleaned, and made aerial attacks. The mangrove species were similar to Singing Honeyeaters, but also gleaned from branches and stilt roots and even probed for invertebrates in tidal mud.

Foraging niches varied for this group from 0.28 for Singing, to 0.31 for Mangrove

Honeyeater (Figure 2.2). Nectarivory was highest in Singing Honeyeaters (56%), and we saw them on 33 different species of plants. Varied Honeyeater was 32% nectarivorous on three species and Mangrove Honeyeater was the lowest, with 23% of attacks to flowers on two different species (Figure 2.3). Frugivory was variable. Mangrove Honeyeaters took no fruit,

Singing took 5%, and Varied took 6% (Figure 2.5). 52

Mangrove Honeyeaters used hang down maneuvers to attack more frequently than the

others (23%), which only did so 14% and 15%. They all had probe rates that were higher than

their nectarivory rates, because so many of their attacks were probes to branches and the ground.

All members gleaned some, but the Mangrove Honeyeater gleaned the most at 56% and probed

30%. Mangrove Honeyeaters attacked branches 31% of the time and leaves 35% of the time.

Varied Honeyeaters, when not foraging on fruit, attacked branches 7% (Figure 2.6) of the time,

the ground 6% of the time, and leaves 35% of the time. Singing were similar to Varied in attacks

to air (8%), branches (6%), ground 3%, and leaves 22%. Varied used fewer wing-powered

maneuvers than the others (8%).

Varied Honeyeaters are often found in flocks (0.44) and did not seem to often associate

with other species, which is also true for Mangrove (0.83) and Singing Honeyeaters (0.69).

Singing seemed to be less often associated with mixed species flocks than many other species in

the arid interior. Foliage density in foraging areas varied from 2.20 ± 0.66 SD for Mangrove

Honeyeaters to 2.47 ± 0.61 SD for Singing Honeyeaters. Canopy height was quite low for

Singing Honeyeaters (4.23m ± 2.88 SD), which foraged low in shrub lands, woodlands, and in

suburban gardens. Canopy was higher for Varied Honeyeaters (9.12m ± 3.11SD), which foraged

in mangroves. Mangrove Honeyeaters had a much shorter average canopy height (6.5m ± 2.32).

All three members of the clade foraged at about 60% up in their relative canopies.

25. Ptilotula clade: White-plumed Honeyeater (Ptilotula penicillatus), Yellow-plumed

Honeyeater (Ptilotula s ornatus) Gray-fronted Honeyeater (Ptilotula plumulus), Gray-headed

Honeyeater (Ptilotula keartlandi), Fuscous Honeyeater (Ptilotula s fuscus) and Yellow-tinted

Honeyeater (Ptilotula flavescens) 53

This clade occurs widely throughout most of Australia, but is absent from the northernmost part of the continent. They would often hang down to glean from leaves, but also visited flowers, particularly Eucalyptus flowers. White-plumed and Yellow-plumed performed aerial displays and were often found in aggressive monotypic flocks. Most species used wing- powered maneuvers.

Foraging niche for this clade appeared to be conserved and is quite high. The lowest FDis score was the Gray-fronted Honeyeater (0.30) and the highest FDis score belonged to the

Fuscous Honeyeater (0.34), which was the largest foraging niche of all species sampled (Figure

2.2). This clade frequently gleaned. Yellow-tinted gleaned 53% of the time and the lowest percentage of gleaning was from Yellow-plumed (34%). They also did a fair amount of probing, which Yellow-plumed did the most of (46%) and White-plumed, the least (26%). Fuscous and

Yellow-tinted used hang 37% of the time. Fuscous Honyeaters used wing-powered maneuvers

31% of the time and Yellow-tinted used them only 15% of the time. Fuscous Honyeaters used sally-strikes 6% of the time, and that ranked them in the top 3 sally-striking Honeyeaters. White- plumed gaped 5%.

Substrates attacked varied between members of the clade, but Yellow-plumed was the most nectarivorous (45%) on 7 different species and Gray-fronted was the least (18%) on 5 species (Figure 2.3). Yellow-plumed was the only member to take any fruit (Enchylaena tomentosa) (Figure 2.5). Gray-fronted attacked leaves 58% of the time and Yellow-plumed only

25%. Gray-headed went to branches 14% and Yellow-plumed only 8% (Figure 2.6).

Propensity to flock ranged from 0.62 in Gray-fronted to 0.94 ± 0.28 SD in Fuscous

Honeyeaters. Fuscous foraged in really open vegetation (1.80 ± 1.30 SD) and Yellow-plumed foraged in the densest (2.37 ±1.31SD). They all foraged between the middle and outer parts of 54

the canopy. Fuscous Honeyeater foraged in the highest canopy (14.17 m ±7.74 SD) while the shortest canopy foraged in was Gray-fronted (3.71m ± 1.83 SD). Fuscous also foraged at the highest relative height at 75% ± 0.29 SD up in the canopy and White-plumed and Yellow-tinted foraged 66% up ± 0.31 SD and ± 0.23 SD up in the canopy.

Trends across the family

There were some interesting patterns that emerged across the entire family, including a unimodal response between foraging niche size and percent nectarivory (R2 = 0.66, p = < 2.2e-

16) (Figure 2.7). Both species that took little to no nectar (e.g. Gibberbirds and Chats) and species that were highly nectarivorous had small niches. The largest niches belonged to species that took some nectar. We also found a strong positive relationship between species that frequently hawked (use aerial maneuvers that are not to flowers) and species that were highly nectarivorous (R2 = 0.43, p <0.001) (Figure 2.8). After controlling for phylogeny, the

relationship is still significant, but the pattern is slightly less strong (R2 = 0.32, p <0.001)

0.35 0.30 0.25 Foraging niche size 0.20 0.15

0.0 0.2 0.4 0.6 0.8

Nectarivory

Figure 2.7 Foraging niche size (FDis) and proportion of attacks to flowers (nectarivory) produced a unimodal response which highlights the fact that specialization and small sample size are related. Highly insectivorous and nectarivorous species generally have smaller niches and generalists have larger niches (R2 = 0.66, p = 2.2e-16).

0.8 0.6 Hawking 0.4 0.2 0.0

0.0 0.2 0.4 0.6 0.8

Nectarivory

Figure 2.8 Hawking (percent of attacks to the air that are not to flowers) and proportion of attacks to flowers (nectarivory) were positively correlated (R2 = 0.43, p= 1.466e-10).

PC1 explained 30% of the variation in the dataset (Figure 2.9). The first axis was driven

by nectarivory, attacks to the air, and wing powered maneuvers on one end of the spectrum and

on the other end was hanging, gleaning and high canopies (Table 2.1). A clade that loaded

heavily on the hanging, gleaning, and high canopy end is the Melithreptus clade, which foraged on bark, on trunks of trees and occurred in areas with high canopies. And a clade that loaded heavily on the nectarivory, attacks to the air, and wing-powered maneuvers is the clade with

Banded, Brown, White-streaked, Crescent, New Holland, and White-cheeked clade (clade 7).

Green-backed Honeyeater Tawny-crowned Honeyeater Black Honeyeater Dusky Honeyeater Red-headed Honeyeater Scarlet Honeyeater Rufous-banded Honeyeater Rufous-throated Honeyeater Bar-breasted Honeyeater Brown-backed Honeyeater Gibberbird Yellow Chat Crimson Chat Orange Chat White-fronted Chat Banded Honeyeater Brown Honeyeater White-streaked Honeyeater Crescent Honeyeater New Holland Honeyeater White-cheeked Honeyeater Little Friarbird Helmeted Friarbird Noisy Friarbird Silver-crowned Friarbird Macleay's Honeyeater Tawny-breasted Honeyeater Painted Honeyeater Striped Honeyeater Pied Honeyeater Western Spinebill Eastern Spinebill Yellow-throated Honeyeater White-eared Honeyeater Blue-faced Honeyeater Western white-naped Honeyeater White-naped Honeyeater Black-headed Honeyeater White-throated Honeyeater Strong-billed Honeyeater Brown-headed Honeyeater Black-chinned Honeyeater Yellow-spotted Honeyeater Lewin's Honeyeater Graceful Honyeater Kimberley Honeyeater White-lined Honeyeater White-gaped Honeyeater Yellow Honeyeater Yellow-faced Honeyeater White-fronted Honeyeater Purple-gaped Honeyeater Yellow-turfted Honeyeater Bell Miner Black-eared Miner Noisy Miner Yellow-throated Miner Eungella Honeyeater Bridled Honeyeater Spiny-cheeked Honeyeater Little Wattlebird Western Wattlebird Regent Honeyeater Yellow Wattlebird Red Wattlebird Varied Honeyeater Mangrove Honeyeater Singing Honeyeater White-plumed Honeyeater Yellow-plumed Honeyeater Gray-fronted Honeyeater Gray-headed Honeyeater Fuscous Honeyeater Yellow-tinted Honeyeater

-4.412 trait value 4.411

length=8.984

Figure 2.9 Meliphagidae phylogeny with position along PC1 mapped in color. See table 2.1 for exact loadings. Qualitatively, this axis is driven by a gradient from nectarivorous, aerial species (in red) to gleaning, hanging species that often forage in high canopies (in blue).

PC1 PC2 mean.canopy.height 0.212 -0.232 mean.percent.canopy 0.006 -0.386 mean.FD 0.117 -0.326 mean.third -0.207 0.345 hanging 0.293 -0.176 gleaning 0.325 0.305 probing -0.217 -0.378 bill.creative 0.278 -0.079 wing.powered -0.346 0.003 air -0.369 0.017 branches 0.273 -0.069 nectarivory -0.335 -0.295 frugivory 0.057 0.019 ground -0.06 0.451 leaves 0.325 0.0420 dead 0.168 -0.032

Table 2.1. PC1 and PC2 loadings for species summaries.

PC2, the second principal component, explained another 25% of the variation (Figure

2.10). It was driven by negative numbers for mean percent canopy, foliage density (FD) and probing (in red) to large positive numbers for ground maneuvers, distance from the trunk of the tree and gleaning (in blue) (Table 2.1). Species with large negative values along this axis included Banded, White-streaked, Macleay’s, and Regent Honeyeaters and those with large positive loadings along the axis were the Gibberbird and Chats clade. 60

Green-backed Honeyeater Tawny-crowned Honeyeater Black Honeyeater Dusky Honeyeater Red-headed Honeyeater Scarlet Honeyeater Rufous-banded Honeyeater Rufous-throated Honeyeater Bar-breasted Honeyeater Brown-backed Honeyeater Gibberbird Yellow Chat Crimson Chat Orange Chat White-fronted Chat Banded Honeyeater Brown Honeyeater White-streaked Honeyeater Crescent Honeyeater New Holland Honeyeater White-cheeked Honeyeater Little Friarbird Helmeted Friarbird Noisy Friarbird Silver-crowned Friarbird Macleay's Honeyeater Tawny-breasted Honeyeater Painted Honeyeater Striped Honeyeater Pied Honeyeater Western Spinebill Eastern Spinebill Yellow-throated Honeyeater White-eared Honeyeater Blue-faced Honeyeater Western white-naped Honeyeater White-naped Honeyeater Black-headed Honeyeater White-throated Honeyeater Strong-billed Honeyeater Brown-headed Honeyeater Black-chinned Honeyeater Yellow-spotted Honeyeater Lewin's Honeyeater Graceful Honyeater Kimberley Honeyeater White-lined Honeyeater White-gaped Honeyeater Yellow Honeyeater Yellow-faced Honeyeater White-fronted Honeyeater Purple-gaped Honeyeater Yellow-turfted Honeyeater Bell Miner Black-eared Miner Noisy Miner Yellow-throated Miner Eungella Honeyeater Bridled Honeyeater Spiny-cheeked Honeyeater Little Wattlebird Western Wattlebird Regent Honeyeater Yellow Wattlebird Red Wattlebird Varied Honeyeater Mangrove Honeyeater Singing Honeyeater White-plumed Honeyeater Yellow-plumed Honeyeater Gray-fronted Honeyeater Gray-headed Honeyeater Fuscous Honeyeater Yellow-tinted Honeyeater

-2.596 trait value 8.664

length=8.984

Figure 2.10 Meliphagidae phylogeny with position along PC2 mapped in color. See table 2.1 for exact loadings. Qualitatively, this axis is driven by a gradient from relative foraging height, and probing (red) and ground maneuvers, distance from the trunk of the tree, gleaning (blue).

Another interesting finding was with the trait of attacks to branches (Figure 2.6). In

Tasmania, there are eleven species of Honeyeaters, four of which are endemic to Tasmania.

Three of those species had higher proportions of attacks to branches than any other member of

the family, and the fourth is not far off.

There were some interesting patterns with closely related co-occurring species (Table

2.2). The two sympatric, Tasmanian-endemic Melithreptus species were frequently found in large flocks together. Both are forest and woodland inhabitants. They seemed to overlap on

Tasmania more than their mainland counterparts. Strong-billed foraged at a lower canopy

(13.56m ± 8.10 SD) than Black headed (27.71m ± 13.33 SD). Strong-billed also foraged in lower

relative canopy (63% ± 0.27 SD) than Black-headed (88% ± 0.24 SD). Black-headed gleaned

(77%) from leaves (50%) predominantly, but Strong-billed foraged by probing (56%) branches

(74%). They also had some morphological differences. Black-headed have much smaller bill that

is more aligned with foliage gleaning and Strong-billed have a deeper and much longer bill for

probing bark. This is a possible example of character displacement between sympatric species,

and future work should look into possible continental examples of this.

Species Canopy relative canopy gleaning probing leaves branches height height

Strong-billed 13.56m ± 63% ± 0.27 SD 30% 56% 3% 74% honeyeater 8.10 SD

Black- 21.71m ± 88% ± 0.24 SD 77% 20% 50% 41% headed 13.33 SD honeyeater

Table 2.2. Closely related and co-occurring Tasmanian endemics show some character displacement in their foraging niche.

DISCUSSION

This robust foraging behavior dataset has allowed us to describe the patterns (including

similarities and notable differences between related species) of a large and diverse group of

Australian passerines. Many of the traits show qualitative phylogenetic conservatism, but there

were also some interesting relationships with co-occurring, closely related species. The fine- scale animal behavior data, the phylogenetic breadth, and the large number of individuals recorded make this a flexible and robust dataset that can allow us to look at the relationships between foraging niche size, range size and sensitivity to disturbance.

WERE TRAITS PHYLOGENETICALLY CONSERVED? - Many foraging behavior traits were phylogenetically conserved with only a few exceptions. Nectarivory is a trait that appears to be phylogenetically conserved across Australian Meliphagidae (Figure 2.3). Pyke (1980) and

Keast (1976) found that species within the same genus tended to be similar with respect to the amount of nectar and insects in their diets. In Pyke’s (1980) synthesis of foraging behavior, he

and Keast (1976) found Acanthorhynchus, Anthochaera, Acanthagenys, Myzomela, Certhionyx,

Phylidonyris and Lichmera to include the most nectar in their diets and for the species they were

able to include, the results align with our data. They found Meliphaga, Xanthotis,

Lichenostomus, Melithreptus and Manorina to take very little nectar, which is consistent with

our general findings across the entire continent. Blue-faced Honeyeaters stand out in our dataset

as taking more nectar than other Melithreptus members. Pyke (1980) lists Blue-faced Honeyeater

as a species that takes some nectar, some fruit, and some insects. This is also consistent with

what we found. In our dataset, they were the only member of the clade to go to fruit.

Those early studies were before Epthianurinae (the clade to which Gibberbirds and Chats

belong) were included with the Honyeaters. Generally, we observed very few attacks to flowers 63

in this group. They spent most of their time gleaning insects from the ground, except for the

Crimson Chat, which had some nectar in their diet and a much more brush-tipped tongue than other members of the clade (Parker 1973). A highly nectarivorous clade was number 7 (Banded,

Brown, White streaked, Crescent, New Holland, and White-cheeked clade). In Darwin, Franklin

(1997) found Dusky Honeyeaters to be the most flower-dependent Honeyeater in the area.

Similarly, it was ranked at 64th in our entire dataset on a diverse group of 21 plant species including only one Eucalyptus species. Black Honeyeaters are thought to be totally dependent on

Emu bush (Eremophila) (Hobbs 1958, Gannon 1962, Pyke 1980) and adversely affected by the removal this species from grazing and weed control. We saw them on four flower species, two of which were species of Eremophila, which highlights the importance of also attempting to protect those additional species.

Frugivory was a rare trait within the family, but lit up in a few distinct areas (Figure 2.6).

Painted Honeyeaters were the most frugivorous in the family and are known to specialize on mistletoe fruit (Amyema) (Eddy 1966, Chisholm 1944). We recorded them only on Amyema quandang. Pied Honeyeaters were thought to specialize on nectar from Eremophila and to follow those blooming events (Ford et al. 1979, Schodde 1982), but we never found them at Eremophila patches. When we did find the species, they were feeding on African boxthorn fruit (a highly invasive species). They were previously lumped with a totally nectarivorous group, but the recent phylogeny has them down here among other species that take fruit.

ATTACKS TO BRANCHES IN TASMANIA - There were some interesting patterns with respect to attacks to branches in Tasmanian species (Figure 2.6). Eleven Honeyeater species occur on Tasmania, four of which are endemic. Three of those endemics had the highest percentage of attacks to branches. Yellow Wattlebirds, for instance, stood out dramatically in 64

their clade with their propensity to forage on branches. All Melithreptus attacked branches to some extent, but Strong-billed Honeyeaters, one of two endemic Melithreptus in Tasmania, made attacks to branches more frequently than any other species in our study. Keast (1970) also found a much higher percentage of attacks to branches for Strong-billed compared to its close mainland relative, the Black-chinned Honeyeater. Similarly, the Tasmanian endemic Yellow-throated

Honeyeater had the 2nd highest percentage of attacks to branches. Its mainland sister species, the

White-eared Honeyeater, also did a fair amount of gleaning to branches, though less so than the

Yellow-throated Honeyeater. Keast (1970) noticed a similar pattern with a shift toward attacks to

branches and trunks of trees in Tasmania. He hypothesized that Strong-billed vary so much from

their mainland counterparts because they are filling an adaptive zone left empty by the absence

of Australian tree-creepers (Climacteridae) and sittellas (Neosittidae). With our dataset, one would quickly notice that those species in Tasmania with a propensity for branch attacks come from lineages that were predisposed to foraging on branches and it could be that that trait allowed them to be successful there. That predilection toward branch attacks may have given these species an advantage on adapting to Tasmania.

CLOSELY RELATED CO-OCCURRING SPECIES - Overall, closely related species had similar foraging niche sizes (Figure 2.4), but there was some variation in closely related sympatric species like Strong-billed and Black-headed Honeyeaters in Tasmania (Table 2.2).

Slater (1994) first described such a separation between Black-headed and Strong-billed

Honeyeaters in foraging site, foraging method and social structure. He also explained that the shorter-billed Melithreptus, Black-headed Honeyeater, is better adapted for foliage gleaning

(Keast 1970) and in fact has the highest gleaning score for the clade in our dataset. Strong-billed 65

foraged at a lower relative canopy height than Black-headed. Black-headed gleaned from leaves

predominantly and Strong-billed mostly probed branches.

TRAITS ASSOCIATED WITH SMALL FORAGING NICHES - There were several traits

that were associated with a small foraging niche: nectarivory, insectivory, and ground foraging

(Figure 2.9). Species that used a variety of foraging attack behaviors for a variety of food

substrates in a variety of habitats had the largest niches. We found that generally, species that

specialized on one food substrate had small niches. Highly nectarivorous and insectivorous

species tended to have small foraging niches. While there is not a tight co-evolutionary

relationship between flower species and their Honeyeater pollinators (Ford et al. 1979), there

was a strong tendency for nectar specialists to also have small foraging niches. Some species,

like the Western Wattlebird, which was ranked as 73 most nectarivorous, foraged on only 4

flower species during our observations. Some Honeyeater species were dependent on very few

plant species. Ground foraging insectivores like members of the Epthianurinae clade also had

very small niches. Species with large niches tended to take a variety of resources and obtain those resources with a variety of maneuvers.

ASSOCIATED TRAITS - Using species summaries, we plotted species’ positions along the PC axes onto the phylogeny (Figures 2.7 & 2.8). The first principal component (PC1) was

driven by negative numbers for nectarivory, attacks to air and wing-powered maneuvers to

positive numbers for hanging and gleaning species that often forage in high canopies (Figure

2.7). Species with large negative values along this axis included Tawny-crowned, Black,

Banded, and White-fronted Honeyeaters and Red and Yellow Wattlebirds (species taking nectar from the tops or outer parts of trees or making attacks to the air). Species with large positive values along this axis included Green-backed Honeyeater, Western White-naped, and many of 66 the other Melithreptus species (species gleaning from leaves and bark). The second principal component (PC2) is driven by negative numbers for mean percent canopy, foliage density (FD) and probing (in red) to large positive numbers for ground maneuvers, distance from the trunk of the tree, gleaning (in blue) (Figure 2.10). Species with large negative values along this axis included Banded, White-streaked, Macleay’s, and Regent Honeyeaters (species that were highly nectarivorous) and those with large positive values along the axis were members of the

Epthianurinae subfamily. Members of this clade stood out from other Honeyeaters due to their propensity to forage in open areas. Gibberbirds are also one of two species in the dataset that forages in the least dense vegetation.

HAWKING AND NECTARIVORY - The fact that PC1 was driven by nectarivory, attacks to air, and wing powered movements on one end of the spectrum, and then hanging, gleaning, and high canopies on the other end was at first surprising. Many of the most nectarivorous species were also the species that used the highest proportions of wing-powered movements and attacks to the air (Black Honeyeater, New Holland and White-cheeked). The relationship between frequent attacks to the air and percent nectarivory has not gone unnoticed in the world of Australian ornithology. Recher (1970) published the first account of high nectarivory and costly flights to the air for insects. Our dataset allowed us to test his hypothesis and 45 years later

Recher’s casual observation was borne out continent wide across the entire family. Hawking was positively correlated with percent of nectar in the diet.

With this continent wide study of Australian Meliphagidae, we have been able to document important natural history data across large geographic ranges and seasons. The fine scale at which foraging niche was measured has proven to be an important tool in looking at how traits are arranged across a phylogeny, which traits are associated, and which traits are aligned 67 with small foraging niches. Foraging niche size may prove to be an important tool for conservation.

CHAPTER III

DOES FORAGING NICHE PREDICT EXTINCTION RISK IN THE AUSTRALIAN MELIPHAGIDAE?

ABSTRACT

Recent work on foraging behavior has explored the relationship between small niche sizes and vulnerability to changes in the environment (Purvis 2000, Hodgson et al. 2006,

Sokolov 2012, Clavel 2010). Generally, we can say that specialist species have smaller foraging niches than generalist species due to the lack of variety in what they eat and the mechanisms necessary to acquire those resources (Ford 1990, Beissinger 1994). In avian biology, diet traits are often better predictors of sensitivity than other life history traits (reviewed Gray et al. 2007).

Some have suggested that there is a relationship between niche size and sensitivity (Brown,

1995, Thuiller 2005). We predicted that species with large foraging niches would be most likely to also be categorized outside of the “least concern” category (IUCN) and considered “low” on

Garnett and Franklin’s (2014) sensitivity and exposure to climate change categories. We found that while foraging niche size and position are likely good additions to assessment of risk from

anthropogenic disturbance, they alone cannot be proxies because of dynamic and uneven

pressure from shifts in land use, fragmentation, drought, competition with other native species.

INTRODUCTION

Long ago MacArthur and Pianka (1966) recognized that an animal’s foraging behavior

could be used as a tool for predicting multiple ecological phenomena. One of those tools may be

predicting response to anthropogenic disturbance (Brown, 1995, Thuiller et al. 2005). There is

reason to think that species may be threatened by having a limited range of resources that they

exploit (Hockey and Curtis 2009). Within species, increased disturbance in the form of 69

urbanization has been shown to lead to higher stress levels (Schoech et al. 2004), shifts in

singing behavior in relation to noise pollution (Slabbekoorn and Peet 2003, Francis et al. 2011)

and changes in migratory patterns in some bird species (Walther et al. 2002), which all

presumably result in decreased fitness. Extinction risk is generally higher in species that are

geographically isolated, locally rare and therefor have small niches (McKinney 1997, Brändle et

al. 2003). Small niche size has been shown to be a good predictor of extinction risk due to a

limited repertoire of behaviors and resources utilized (Walker and Preston 2006, Lee and Jetz

2010). In this chapter, I will use foraging niche size of Australian Meliphagidae (honeyeaters)

and current assessments of threat and populations trends to see if small foraging niches are good

predictors of risk and decline.

Foraging behavior is one means of describing species’ niches (MacArthur 1972). Because of this, foraging behavior may also be a good descriptor of species’ behavioral flexibility (Sol et al. 2002). Behavioral flexibility is an adaptive response to changes in the environment.

Generally, species with larger niches, and more behaviorally flexible species, are predicted to better succeed in novel environments (Mayr 1965, Ehrlich 1989, Sol 2002). Innovations in foraging behavior and an innate repertoire of feeding mechanisms can allow species to adjust to

changes in the environment and persist in novel conditions. Such flexibility may help organisms

tolerate anthropogenic disturbance. Foraging behavior flexibility in response to changes in

climate and resources has been explored with a variety of taxa and scenarios. Dill (1983) noted

flexibility in foraging behavior in salmon in response to spatial and temporal shifts in resources.

Memmott and others (2007) found a reduction of diet breadth in pollinator species in simulated

future phenology shifts. Wilson et al. (2008) saw that in coral reef fish, diet specialists would be hindered in the face of climate change. Innovations in foraging behavior correlates positively 70 with successful invasion in novel environments (Sol 2002, reviewed in Wright et al. 2010). To successfully invade a new environment, species often need to shift their niche to include new foraging substrates, habitats, and shelters (Duncan et al. 2003, Martin and Fitzgerald 2005). In birds, there has been quite a bit of work with brain size and innovation (Sol et al. 2005), which has implications for climate change and future disturbance scenarios.

Climate change is one form of disturbance that is already affecting some bird species in

Australia and will likely cause more changes in the future (Hughes 2003, Williams et al. 2003).

Accompanying the unknown shifts in temperature and precipitation may be synergistic or additive relationships with other stressors that could lead to extinction. Şekercioğlu et al. (2012) estimated that by the year 2100, we will have lost 10% of bird species worldwide due to climate change. Though there have been fewer studies on the effects of climate change on migration and phenological mismatch in Australia than in North America and Europe, there have recently been a few. Smith and Smith (2012) studied arrival and departure dates for 16 bird species in New

South Wales. They found evidence of earlier arrival dates of spring migrants with increased temperature. Beaumont et al. (2006) found similar shifts in first arrival date and last departure date as have been found in North American studies. Related to these shifts, Gardner (2009) reported a decrease in body size for at least four species of Australian birds. Some seabirds have declined because they have shifted their range in response to changes in climate and ocean dynamics, which has decreased breeding success (Chambers 2011).

Niche position along various climatic and habitat axes has been useful to determine potential sensitivities to climate change in fish, bumblebees, ticks and birds (Broennimann et al.

1996, Williams et al. 2007, Buisson 2008, Tingley et al. 2009). Niche position or resource/habitat availability can help us to see if species that have low or high habitat availability 71 have increased exposure or sensitivity. It could allow us to see if certain traits or suites of traits predispose species to risk.

Australian bird species have experienced declines as a result of anthropogenic land use shifts (Garnett et al. 2011, MacNally et al. 2004). Many of Australia’s honeyeaters are listed by the International Union for Conservation of Nature (IUCN version 3.1, 2001) as having populations that are in decline. It is possible that current conservation efforts do not have tools that are powerful or precise enough to appropriately assess species’ vulnerability and susceptibility to extinction risk. We predicted that species with large foraging niches will be most likely to also be categorized outside of the “least concern” category (IUCN) and categorized as “low” in Garnett and Franklin’s (2014) analysis of risk and exposure to climate change. We also predicted that species’ with declining populations will have smaller foraging niches than those that are stable.

Using a measure of foraging niche size for 37 honeyeater species in Australia, climate change risk assessment by Garnett and Franklin (2014), and IUCN threat status, we explored the potential for foraging niche size to predict threat. Garnett and Franklin (2014) assessed both exposure to climate change (sea level rise, shifts in climate) and sensitivity, which may make species more susceptible to that climate change on a categorical scale from “low” to “very high.”

We expected that the broader a species’ niche, the more likely that species is to persist somewhere in a climate-changed world. Therefore, as foraging niche size increased, we would see an increase in exposure to climate change. We also predicted that species that are “very sensitive” to climate change would have smaller foraging niches than species that have “low” sensitivity to climate change.

METHODS 72

SENSITIVITY TO DISTURBANCE AND CLIMATE CHANGE – The IUCN places almost

all Australian Honeyeaters in the least concern (LC) category with three exceptions: the Painted

Honeyeater (Grantiella picta) is considered vulnerable; the Regent Honeyeater (Anthochaera

Phrygia) is considered critically endangered; and the Black-eared Miner (Manorina melanotis) is considered endangered (Table 3.1). Threat status is based on extinction risk of a species under current conditions. Three species afford little statistical power to assess how niche size relates to extinction risk. As an alternative approach, we used the recent assessments of Garnett and

Franklin (2014). These authors categorized about half of the honeyeaters according to their sensitivity and exposure to climate change. While this report does not address threat status or extinction risk outside of threat from climate change, it is helpful, in many ways in answering some of our questions. Australian bird species may potentially be exposed to increased temperature (McKechnie and Wolf 2009), change in rainfall, and in turn, fire frequency and sea level rise (Hughs 2003).

Table 3.1 Common name, species name, IUCN threat status, IUCN population trends and exposure and sensitivity to climate change. IUCN status is LC = least concern, CE = critically endangered, V = vulnerable, and E = endangered IUCN IUCN population Common Name Species Name status trend Exposure Sensitivity Red Wattlebird Anthochaera carunculata LC Decreasing very high low Yellow Wattlebird Anthochaera paradoxa LC Decreasing high low Western Wattlebird Anthochaera lunulata LC Increasing NA NA Little Wattlebird Anthochaera chrysoptera LC NA very high low Spiny-cheeked Honeyeater Acanthagenys rufogularis LC Decreasing NA NA Striped Honeyeater Plectorhyncha lanceolata LC Stable NA NA Helmeted Friarbird Philemon buceroides LC Stable very high low Silver-crowned Philemon argenticeps LC Stable very high low 73

Friarbird Noisy Friarbird Philemon corniculatus LC Stable high low Little Friarbird Philemon citreogularis LC Stable NA NA Regent Honeyeater Xanthomyza phrygia CE Decreasing low high Blue-faced Honeyeater Entomyzon cyanotis LC Stable high low Macleay's Honeyeater Xanthotis macleayanus LC Stable NA NA Tawny-breasted Honeyeater Xanthotis flaviventer LC Stable low high Bell Miner Manorina melanophrys LC Stable NA NA Noisy Miner Manorina melanocephala LC Decreasing high low Yellow-throated Miner Manorina flavigula LC Stable very high medium Black-eared Miner Manorina melanotis E Decreasing very high very high Lewin's Honeyeater Meliphaga lewinii LC Stable very high high Yellow-spotted Honeyeater Meliphaga notata LC Stable high low Graceful Honeyeater Meliphaga gracilis LC Stable very high low White-lined Honeyeater Meliphaga albilineata LC Stable very high low Kimberley Honeyeater Meliphaga fordiana NA NA NA NA Bridled Honeyeater Lichenostomus frenatus LC stable high low Eungella Honeyeater Lichenostomus hindwoodi LC Stable high medium Yellow-faced Honeyeater Lichenostomus chrysops LC Decreasing high low Singing Honeyeater Lichenostomus virescens LC Increasing very high low Varied Honeyeater Lichenostomus versicolor LC Stable high low Mangrove Lichenostomus Honeyeater fasciogularis LC Decreasing NA NA White-gaped Honeyeater Lichenostomus unicolor LC Stable NA NA Yellow Honeyeater Lichenostomus flavus LC Decreasing NA NA White-eared Honeyeater Lichenostomus leucotis LC Decreasing very high low Yellow-throated Lichenostomus flavicollis LC Stable NA NA 74

Honeyeater Purple-gaped Honeyeater Lichenostomus cratitius LC Decreasing very high low Gray-headed Honeyeater Lichenostomus keartlandi LC Stable very high low Yellow-tinted Honeyeater Lichenostomus flavescens LC Stable low high Yellow-tufted Lichenostomus melanops LC Decreasing NA NA Fuscous Honeyeater Lichenostomus fuscus LC Stable NA NA Gray-fronted Honeyeater Lichenostomus plumulus LC Unknown high low Yellow-plumed Honeyeater Lichenostomus ornatus LC Decreasing NA NA White-plumed Lichenostomus Honeyeater penicillatus LC Decreasing very high low Black-chinned Honeyeater Melithreptus gularis LC Stable NA NA Strong-billed Honeyeater Melithreptus validirostris LC Stable NA NA Brown-headed Honeyeater Melithreptus brevirostris LC Stable high low White-throated Honeyeater Melithreptus albogularis LC Decreasing NA NA White-naped Honeyeater Melithreptus lunatus LC Stable NA NA Western white- naped Honeyeater Melithreptus chloropsis NA NA low high Black-headed Honeyeater Melithreptus affinis LC decreasing high low Green-backed Honeyeater Glycichaera fallax LC Decreasing NA NA White-streaked Honeyeater Trichodere cockerelli LC Stable very high medium Crescent Honeyeater Phylidonyris pyrrhoptera LC Stable NA NA White-fronted Honeyeater Phylidonyris albifrons LC Stable NA NA White-cheeked Honeyeater Phylidonyris nigra LC Stable NA NA New Holland Phylidonyris Honeyeater novaehollandiae LC Stable low low Tawny-crowned Honeyeater Phylidonyris melanops LC Decreasing high high Brown Lichmera indistincta LC Decreasing very high low 75

Honeyeater Painted Honeyeater Grantiella picta V Decreasing NA NA Bar-breasted Honeyeater Ramsayornis fasciatus LC Stable NA NA Brown-backed Honeyeater Ramsayornis modestus LC Stable NA NA Gray Honeyeater Conopophila whitei LC Decreasing very high high Rufous-throated Honeyeater Conopophila rufogularis LC stable NA NA Rufous-banded Honeyeater Conopophila albogularis LC Stable NA NA Acanthorhynchus Eastern Spinebill tenuirostris LC Decreasing NA NA Western Acanthorhynchus Spinebill superciliosus LC Decreasing NA NA Dusky Honeyeater Myzomela obscura LC Stable NA NA Red-headed Honeyeater Myzomela erythrocephala LC Stable NA NA Scarlet Honeyeater Myzomela sanguinolenta LC Stable NA NA Banded Honeyeater Certhionyx pectoralis LC Stable NA NA Pied Honeyeater Certhionyx variegatus LC Stable NA NA Black Honeyeater Certhionyx niger LC Decreasing NA NA Crimson Chat Epthianura tricolor LC Stable NA NA Orange Chat Epthianura aurifrons LC Stable NA NA Yellow chat Epthianura crocea LC NA high medium White-fronted Chat Epthianura albifrons LC Increasing NA NA Gibberbird Ashbyia lovensis LC Increasing very high low

According to the Franklin and Garnett (2014) study, a species must be both exposed to change caused by climate shifts and sensitive to that exposure to be considered vulnerable

(Foden et al. 2008, Dawson et al. 2011). Exposure was the extent of climate change likely to be experienced by a species (Dawson et al. 2011) and this was scored from low to very high. 76

Sensitivity was based on species-specific properties that modified the potential impact experienced from exposure and was also ranked from low to very high. Exposure data were collected from BirdLife Australia, part of the Atlas of Living Australia and consolidated into unique points at a grid size of 2 km x 2km. For terrestrial species, they built climate space models based on presence-only species distribution models, which provides the environmental limits of species. Sea-level rise was rated qualitatively. Fire sensitivity was based on literature.

Sensitivity was based on three things: specialization, low genetic diversity, and age at reproductively capable. Species with delayed reproduction are able to allocate more energy to future reproduction and could wait for optimal environmental conditions before breeding, leading to more favorable population status in the long term. To determine specialization, they considered: number of habitats, number of food types, number of foraging strategies, ecological niche factor analysis (ENFA), relative brain size (which they inferred from body size), and maximum number of young that can be raised in on year (Garnett and Franklin 2014).

ANALYSES

Foraging niche size and position – In order to use all of our variables, foraging niche size was calculated using functional dispersion (FDis) of foraging behavior metrics in multivariate space (Laliberte and Legendre 2010) (Chapter 1). Foraging niche size was developed from ordinating 17 mutually exclusive foraging attack behaviors, a measure of propensity to flock, position in the vegetation, distance from the ground, canopy height where foraging behavior took place, and food substrate. We used a 10-dimensional non-metric multidimensional scaling ordination (NMDS) based on a Gower distance matrix to compute the similarity value between individual foraging observations. FDis is the weighted mean distance in multidimensional trait space of all foraging observations of a given species from its centroid. Species were ranked and 77

ordered from least to most of the trait in question and is an average, meaning that if three of six

species were tied for most nectarivorous, all three would have a rank of 5. Occasionally, we

provided a species rank after their range size. Niche position was developed by using species

averages in a principal components analysis (PCA). We chose 15 foraging and ecology variables

to ordinate in the PCA. We looked at the relationship between foraging niche size and position to

sensitivity and exposure with a one way analysis of variance (ANOVA). We evaluated significant

differences with a posthoc Tukey’s Honest Significance test (HSD).

RESULTS

None of the three species listed outside of IUCN’s threat status of least concern (LC) had especially small foraging niches (FDis), though both Black-eared Miner (0.27) (18) and Regent

Honeyeater (0.29) (27) were on the lower end of the spectrum. Painted Honeyeater, listed as vulnerable (V) had an average niche size (0.31) (46). There were no significant patterns between

FDis and sensitivity or exposure. There was a non-significant trend between FDis and exposure to climate change. Species with higher levels of exposure also had smaller niches (Table 3.2)

Table 3.2 ANOVA results for FDis and sensitivity, exposure and IUCN trend, PC1 with sensitivity, exposure, and IUCN trend, and PC2 with sensitivity, exposure, and IUCN population trend.

sensitivity exposure IUCN trend Fstatistic pvalue Fstatistic pvalue Fstatistic pvalue FDis 1.493 0.235 1.919 0.163 7.480 0.001* PC1 1.364 0.271 1.282 0.291 1.224 0.301 PC2 0.553 0.650 0.525 0.596 7.167 0.001*

IUCN population trends were loosely associated with niche size and position. Foraging

niche size and IUCN population trend inversely related, opposite to our predictions (Figure 3.1).

Stable populations had the largest niches and increasing populations had the smallest niches,

though only three species are in that category (F (2, 65) = 7. 48, p = 0.001). The posthoc Tukey’s

test showed that there is a significant difference between increasing and decreasing (p = 0.003)

and increasing and stable (p < 0.00) populations. There was no trend between PC1 and niche

size, position, or population trend. PC2 was significantly related to IUCN population trend

(Figure 3.2). Large values of PC2 are associated with ground maneuvers, distance from trunk and

gleaning and small values were associated with mean percent canopy, foliage density, and

probing (F (2, 65) = 7.167, p value = 0.002). The Tukey’s posthoc test showed a significant difference between increasing and decreasing (p = 0.002) and increasing and stable (p = 0.001).

The species’ whose populations are decreasing or stable are those that forage in places with

dense canopy vegetation. Species with increasing populations are those that spanned the axis.

That pattern was largely driven by White-fronted Chats and Gibberbirds (which gleaned from the

ground out in the open) to Singing Honeyeaters (Lichenostomus virescens) (which ate variety of

things in a variety of ways across a large part of the continent). 79

0.35 0.30 0.25 foraging niche sizeforaging 0.20 0.15

decreasing stable increasing IUCN population trend

Figure 3.1 Foraging niche size and IUCN population trend. Stable populations had the largest niches and increasing populations had the smallest niches, though only three species are in that category (F (2, 65) = 7. 48, p = 0.001). Tukey’s posthoc test confirms that there is a significant difference between decreasing and increasing (p = 0.003) and stable and increasing (p > 0.00). 80

Ground maneuvers

Distance from trunk of tree8 Gleaning

PC2

-2 Mean percent canopy Foliage density Probing decreasing stable increasing IUCN population trend

Figure 3.2 Niche position on PC2 and IUCN population trends. The second principal component (PC2) was loaded positively for ground maneuvers, distance from trunk and gleaning and negatively for mean percent canopy, foliage density, and probing (F (2, 65) = 7.167, p value = 0.002). The species’ whose populations were decreasing or stable were groups that foraged in places with dense canopy vegetation and increasing population numbers came from species that made attacks to the ground, foraged far from the trunk of the tree, and gleaned frequently (this pattern is largely driven by White-fronted Chats and Gibberbirds, which were two out of three species in this category). Tukey’s posthoc test confirmed that there was a significant difference between decreasing and increasing (p = 0.002) and stable and increasing (p = 0.001).

Franklin and Garnett (2014) also included other risk factors associated with climate change. Honeyeaters most exposed to either a loss of climate space or a reduction in climate suitability are Gray-headed Honeyeater (Lichenostomus keartlandi), Black-eared Miner, Gray 81

Honeyeater (Conopophila whitei) and Tawny-breasted Honeyeater (Xanthotis flaviventer). Gray- headed and Tawny-breasted Honeyeaters have quite large niches, Black-eared Miners have smaller niches, and we have no data on Gray Honeyeaters. For species (like Black-eared Miners) which could experience a loss of climate space or reduction in climate suitability combined with a small foraging niche size, the effects could act additively or synergistically. In their projections of fire risk, the only honeyeater that was directly affected was the Helmeted Friarbird subspecies

(Philemon buceroides ammitophila). This subspecies occurs in the far north of the Northern

Territory and we observed them at Kakadu National Park. The Helmeted Friarbird species had a medium foraging niche size (0.30) (39). A Yellow-tufted subspecies (Lichenostomus melanops cassidix) has a very small population outside of Melbourne in Victoria and are listed as high exposure and sensitivity. There are only two species of Australian Honyeaters that are both highly sensitive and highly exposed to climate change. The Yellow-tinted Honeyeater

(Lichenostomus flavescens) subspecies (melvillensis) lives on the Tiwi Islands off the coast of northern Australia. This species occupies a series of small islands that are projected to have a total loss of climate space. They are highly sensitive because they have a small climatic space and are also said to be highly specialized in their foraging substrate and maneuvers (Higgens et al. 2001).

There were a few species that may experience the synergistic effects of a small niche and high exposure and sensitivity to that exposure. White-streaked Honeyeater (Trichodere cockerelli) (FDis = 0.14), for example, is ranked as having very high exposure and medium sensitivity to that exposure. They also have the smallest foraging niche size of any other species in our dataset. White-streaked Honyeaters probed for nectar 90% of the time during our observations on three different species of flowers. Tawny-crowned Honeyeaters are listed as 82 high for both exposure and sensitivity, and they have a medium foraging niche (0.30) (37). They are highly nectarivorous across their range. They use wing-powered maneuvers; forage on the ground, in coastal heath and even occur in the sand plains of the interior.

DISCUSSION

Because of their broad-scale focus, lists from organizations like the IUCN, Birdlife

Australia, and Australian Government Department of the Environment may not be the best measurement of threat for our purposes. Our dataset may lend itself better to a non-categorical approach which may be more helpful for predicting response. Small foraging niches were not related to a species’ threat status, but may relate to the availability of the food source.

The three Australian honeyeater species that IUCN has listed with a status other than least concern do not have overly small foraging niches as we expected. Regent Honeyeaters, listed as critically endangered, have a typical niche size compared to other Australian honeyeaters. This species once migrated north/south following flowering events (Ley 1996). The cause of decline in this species is difficult to identify because of the multitude of factors involved including drought. That stress has been compounded by habitat loss due to clearing for agriculture, and competition with other native bird species (Ford et al. 2001). Garnett and

Franklin (2014) list this species as having a high sensitivity to climate change, but a low exposure to it. Exposure does not take into account the potential effects of continued drought.

Regent Honeyeater’s box-ironbark habitat has been under extreme drought for the last 13 years which has caused a collapse of the local avifauna (Nally and Bennett 2009). During our foraging observations from two different times of year, we saw Regent Honeyeaters foraging on only two plant species: Mahogany and Red Ironbarks (Eucalyptus robusta and sideroxylon). While 83

foraging niche size as quantified with FDis does not adequately predict threat, the details of their

limited diet are highlighted in this study. They used a variety of foraging maneuvers, which gave

them a larger foraging niche, but their diet is limited and that puts them at great risk.

Black-eared Miners, listed as endangered, have a smaller foraging niche than average and

are limited to semi-arid mallee habitat seldom taller than 10 m and unburned for at least 45 years

(Clarke 2011). Woinarski (1999) explained that they forage on decorticating bark (bark ribbons)

that would not be available right after a burn. We observed them foraging on hanging bark only

4% of the time. They rank 54th for attacks to hanging bark, which means that 24 other species of

honeyeater foraged on hanging bark more frequently than them. They are also cooperative

breeders and need large tracts of land (Clarke 2011). Their current range is much smaller than

their historic range as a result of clearing and manipulating (draining) land for human settlement, fire, and fragmentation (Clarke 2005). Franklin and Garnett (2014) list them as highly vulnerable to climate change because modeled climate space will be gone by 2085. Their foraging niche

was restricted to mostly gleaning (92%) branches (21%) and leaves (60%) and some probing to

just one species of flower: Grevillea huegelii, though we suspect they visit more species.

Attacks to leaves were generally to lerp, which is consistent with the literature, but we recorded

fewer attacks to invertebrates than the literature alluded to (McLaughlin 1990). While their diet

is specific to a certain forest type under specific post-fire conditions, their cooperative breeding

status and dependence on large tracts of land are much more powerful indicators.

Painted Honeyeaters, listed as vulnerable, had an average to high FDIS score, but are

considered to be “the most specialized” for their dependence on two different species of

mistletoe fruit (Keast 1968, Barea and Watson 2007). They have been shown to breed in

response to Grey mistletoe (Amyema quandong) fruiting events as well as food supplementation 84

experiments (Barea and Watson 2007). They nest preferentially in Amyema (mistletoes) in

Acacia (Barea 2008). The patterns in their large foraging niche are driven by their consumption of fruit. All species in our dataset that have some fruit in their diet also have larger niches. Their dependence on dry acacia woodlands for specific species of fruit is the major driver of their

threat. Acacia woodlands are threatened by habitat loss and fragmentation (Oliver 2003). This is

another example of foraging niche size being driven by maneuvers, but diet is specialized.

Using Franklin and Garnett’s 2014 assessment of climate change risk, we compared

foraging niche size of the 37 Meliphagidae with exposure and sensitivity. We found no pattern

with foraging niche size and their categories of exposure and sensitivity. There was only one

species (Black-eared Miner) in the “very high” sensitivity category. Qualitatively, species with increasing niche sizes had increased sensitivity scores, which was the counter to what we expected.

The niche position (PC2) and IUCN population trend highlighted the fact that the species’ whose populations are decreasing or stable are groups that foraged in places with dense

canopy vegetation (Figure 3.2). Locations with dense canopies have decreased in since human

settlement in Australia. Increasing population numbers came from species that spanned the PC2

axis. This pattern was largely driven by White-fronted Chats and Gibberbirds, which were two

out of three species in this category, the other being Singing Honeyeater.

Niche position and population trend were significantly related (Figure 3.2). Stable

populations had the largest niches and increasing populations had the smallest niches, which is

counter to what would be expected. Scale may be an important factor when considering which

birds are “increasing.” In Birds Australia’s monitoring program, Singing Honeyeaters had no 85

change between the first Atlas of Australian Birds and the 2nd (Barrett 2003). White-fronted

Chat, however declined significantly between the first and 2nd atlas (Barrett 2003). Reasoning for

a listed population increase for Gibberbirds was not clear, though some authors suggest that

increased grazing and clearing of vegetation has allowed for increases for both Gibberbirds and

White-fronted Chats (Reid and Flemming 1992). Our personal experience would lead us to

believe otherwise, and regardless, their total population remains very small. In New South

Wales, Jenner et al. (2011) suggested that White-fronted Chats were in rapid decline and they

were listed as vulnerable under the New South Wales Threatened Species Conservation Act

1995. They are also listed as threatened in the Adelaide-Mount Lofty region of South Australia

(Turner 2001). Species that may appear to be increasing continent-wide often have more

complex regional stories.

Foraging niche size does not appear to be a helpful tool for predicting extinction risk

among Australian honeyeaters. Specialization in diet and habitat breadth certainly make species

more sensitive to disturbance, but the story is often more complex. While the natural history

information from our study can only help to be able to better predict sensitivity to change, there

was no relationship between Franklin and Garnett’s categories of exposure and sensitivity to our

measurement of foraging niche size. It is possible that a categorical approach is not best for

deciphering threat. A linear approach would allow us to look for thresholds in different variables

to look at sensitivity to future change (Travis 2003). Our information on diet could certainly be a

nice addition to how IUCN lists species that are threatened, but with only 3 species to look at in

terms of foraging size there was little pattern. It would be irrational to make conservation

decisions on lists from places like the IUCN alone or over large sweeping scales (Possingham et 86 al. 2002, Farrier and Mooney 2007). Hopefully our fine scale behavior measurements can be used to add to assessment of species threat and behavioral flexibility.

CHAPTER IV

NICHE SIZE AND THEREFORE BEHAVIORAL FLEXIBILITY ARE ASSOCIATED WITH LARGE GEOGRAPHIC RANGES

ABSTRACT

The niche breadth-range size hypothesis assumes that species that use a wide range of resources should be able to occupy larger geographic areas due to the diversity of microhabitats occupied, variety of foods eaten and range of physiological conditions tolerated; accordingly, we should expect to see a positive relationship between niche breadth and range size (Brown 1984,

Gaston 1994, Boulangeat et al. 2012). The support for this hypothesis is mixed across different axes of niche measurements and across different scales. We used the foraging behavior niche size (FDis) and foraging niche position with our measurement of range size to test the hypothesis on a continent and family wide scale. Geographic range was defined as species’ occurrence in

100 x 100 km grid cells using a spatially and taxonomically cleaned data base with specimen and sight records from GBIF, eBIRD, and Atlas of Living Australia with a total of more than 2 million unique data points (Miller 2013). We predicted that a relationship would exist between niche size, behavioral flexibility, and range size, whereby behaviorally flexible species would occupy larger ranges. We found mixed support for the niche breadth-range size hypothesis. The strongest relationships were between range size and niche position and range size and habitat breadth. Species that forage in forests with tall canopies had smaller geographic ranges than species that forage on more widespread habitat types. We also found that species with larger range sizes occur in areas with more vegetation types.

INTRODUCTION

One of the best predictors of extinction for terrestrial species is range size (Harris and

Pimm 2008, Purvis 2000, IUCN 2001, Gaston 2009). The niche breadth-range size hypothesis 88

assumes that species that use a wide range of resources should be able to occupy larger

geographic areas due to the diversity of microhabitats occupied, variety of foods eaten and range

of physiological conditions tolerated. Accordingly, we should expect to see a positive

relationship between niche size and range size. The niche breadth-range size hypothesis has been discussed and debated in the literature (Brown 1984, Gaston 1994, Boulangeat et al. 2012), but there is currently no consensus on the topic. A better understanding of the relationship between niche size and range size could be helpful as a possible explanation for rarity and commonness

(Kunin and Gaston 2013, Rabinowitz 1981) and as a tool for predicting extinction risk. Gaston and Blackburn (2000) concluded that there was generally little support for the hypothesis, but a recent meta-analysis by Slatyer et al. (2013) on multiple taxonomic groups found that environmental tolerance, habitat and, to a lesser degree, diet breadth were associated with range size. Niche breadth can be broken down in a variety of ways. In this chapter, we address the niche breadth-range size hypothesis using a comprehensive dataset of species occurrences, habitat breadth and diet breadth. We will address the following question: 1) Are species with small niches at greater risk of extinction? We predict that: 1) The broader a species’ niche, the more likely that niche is to persist somewhere in a climate-changed world. 2) Species that are

“very sensitive” to climate change have smaller foraging niches than species that have “low” sensitivity to climate change. 3) Species whose populations are “decreasing” will have smaller foraging niches than species that have “increasing” populations.

Diet niche and geographic range size have had mixed support depending on the species, scale, and data collection. Some have described a negative relationship because species with large local niches will have smaller regional niches. Jahner et al. (2011) found that butterfly species with a generalist diet are more likely to forage on novel (non-native) vegetation. They explain that a large range size exposes individuals to a multitude of plant species and thereby increases their foraging niche size. Frequently, species that are diet generalists are habitat specialist and vice versa (Cody 1974). In a study of microhylid frogs in tropical Australia,

Williams et al. (2006) found a negative relationship between range size and niche breadth, concluding that geographically rare species are more likely to persist if they are diet generalists, which they call extinction filtering.

Niche position is a species’ location in multivariate foraging space. Using British breeding bird data, Gregory and Gaston (2000) found niche position to be correlated with geographic range size, but found no relationship between diet and range size. In their review on the topic, Gaston and Blackburn (2008) proposed that niche position was more important than niche size. Widespread species are those that use widespread and common resources (Hanski

1993).

Habitat breadth is a measurement of the number of vegetation types that a species occupies. Range restricted species likely have a smaller range of environmental tolerance and vegetation types that they interact with (Brown 1995). Species with larger habitat breadths that interact with multiple vegetation types will then have the ability to fare better in the face of human altered environments. A large proportion of the current literature on this topic comes from forest fragmentation studies (Henle et al. 2004). There are examples with gecko habitat generalists faring better than gecko habitat specialists (Sarre et al. 1995). The same has been 90

found in beetles in the Wog Wog fragmentation plots of Australia (Davies et al. 2004). Gascon et

al. (1999) found that habitat breadth predicted Amazonian animals’ response to the matrix post

fragmentation. Bentley (2000) and others found that habitat specialization in mammals in vine

forests in Queensland did not allow species to persist after habitat fragmentation and loss.

Using our dataset of foraging behavior of Australian Meliphagidae (honeyeaters), we

have developed a measure of foraging niche size and position per species (Miller and Wagner

2015, chapter 1). Our definition of foraging niche most closely resembled Elton’s definition

(Elton 1946) and includes food type, attack maneuver, location in space where the attack

occurred and species of plant where foraging maneuver took place. We combined this robust and

fine scale measurement with geographic range size to test the niche breadth-range size hypothesis. Habitat breadth was a measurement of honeyeater occurrence points with vegetation type at those occurrence points which gave us a species average of vegetation types that they overlapped with. We predicted that a relationship would exist between foraging niche size and range size, whereby species with large foraging niches occupied larger geographic ranges. In testing the relationship between niche position and range size, we predicted that species whose foraging behavior is dependent on less abundant habitat types would have smaller niches than species whose foraging maneuvers were dependent on more widespread habitats. In testing habitat breadth and foraging niche, we predicted that species that have a large foraging niche will occupy a larger habitat breadth than species with small foraging niches. Because the likelihood of acquired vegetation types with increased range size was likely, we predicted to see a positive relationship between habitat breadth (number of vegetation types a species occurs in) and geographic range size.

METHODS 91

We collected foraging behavior for 74 Australian Honeyeaters over the course of

eighteen months across Australia following Remsen and Robinson’s (1990) standardized

protocols (Miller and Wagner 2015, explained in depth in Chapter 1). We visited 267 locations

over the course of 18 months. The taxonomy follows Joseph and others (2014). Missing species

were added into the phylogeny according to Miller et al. (2013). Included in this behavior dataset

is: site where behavior took place, foraging attack, attack height, foraging substrate, plant species

of substrate (where relevant), canopy height, foliage density, location in canopy, and propensity

to flock. On the occasions where we recorded serial observations for an individual, subsequent

maneuvers were weighted by the reciprocal of the number of observations in the series.

Therefore a series for an individual will carry the same weight as one independent foraging

observation.

Geographic range for Australian Meliphagidae was defined as species’ occurrence in 100

x 100 km grid cells. Miller et al. (2013) used a spatially and taxonomically cleaned database with

specimen and sight records from the Global Biodiversity Information Facility (GBIF), eBIRD

(Sullivan et al. 2009), and Atlas of Living Australia with a total of more than 2 million unique

data points. We used functional dispersion (FDis, Laliberte and Legendre 2010) to quantify

foraging niche size per species. FDis is the weighted mean distance in multidimensional trait space of all foraging observations of a given species from its weighted centroid (Chapter 1). To look at niche position in multivariate space, we used species averages from 15 foraging traits to do a principal components analysis (PCA), with the variables scaled and centered. The first axis explained 30% of the variation and two axes explained 55% of the variation.

We combined the raw occurrence file of species’ latitude and longitude with the current present major vegetation subgroups vegetation layer (Albers 100m analysis product 92

State/Territory data custodians and Department of Environment, Water, Population and

Communities (DSEWPaC), Australian Government). This is in a 100 x 100 m (1 ha) cell size

using an Albers equal area projection with 85 subgroups. We then used the number of vegetation

categories that intersect with each species’ occurrences to derive a measure of habitat breadth.

We used a linear model to look at the relationship between number of vegetation types with both

foraging niche size and geographic range size.

RESULTS

Geographic range size (Figure 4.1) varied from 1 – 611 (sum of occurrences for 100 x

100 km grid cells) for the 75 species. The top three species with the largest geographic range

were the Singing Honeyeater (Lichenostomus virescens) (611) followed by Yellow-throated

Miner (Manorina flavigula) (595) and then Spiny-cheeked Honeyeater (Acanthagenys rufogularis) (530). All three occur across a large proportion of Australia and are sedentary and common over the majority of their ranges. On the low end of the geographic range size list were

Eungella Honeyeater (Lichenostomus hindwoodi) (1), Green-backed Honeyeater (Glycichaera fallax) (4) and Macleay’s Honeyeater (Xanthotis macleayanus) (8). Eungella Honeyeaters occur in a small area of plateau rainforest in the Clark Range of Queensland. Green-backed

Honeyeaters occur in lowland tropical forests of Queensland and they also occur in New Guinea.

Macleay’s Honeyeater spans a broader range north to south in Queensland than Green-backed

Honeyeaters, and they are also found in dry tropical forest. Our prediction that we would see a positive relationship between geographic range size and foraging niche size was not supported

(R<0.00, p = 0.94). When these axes are broken down into single traits and regressed against geographic range size, there are no significant patterns either. 93

600

500

400

Geographic range size range Geographic 300

200

100

0 SingingHoneyeater Yellow-throatedMiner Spiny-cheekedHoneyeater BrownHoneyeater CrimsonChat White-plumedHoneyeater BlackHoneyeater White-frontedHoneyeater PiedHoneyeater Gray-frontedHoneyeater OrangeChat Black-chinnedHoneyeater LittleFriarbird Blue-facedHoneyeater White-frontedChat Brown-headedHoneyeater RedWattlebird White-earedHoneyeater Gray-headedHoneyeater Miner Noisy NoisyFriarbird White-throatedHoneyeater StripedHoneyeater Yellow-plumedHoneyeater Rufous-throatedHoneyeater Yellow-facedHoneyeater NewHolland Honeyeater PaintedHoneyeater EasternSpinebill White-gapedHoneyeater Tawny-crownedHoneyeater BandedHoneyeater White-napedHoneyeater Silver-crownedFriarbird FuscousHoneyeater Yellow-tintedHoneyeater Bar-breastedHoneyeater LittleWattlebird ScarletHoneyeater White-cheekedHoneyeater Yellow-tuftedHoneyeater DuskyHoneyeater Lewin'sHoneyeater RegentHoneyeater Purple-gapedHoneyeater GrayHoneyeater Gibberbird CrescentHoneyeater Red-headedHoneyeater HelmetedFriarbird YellowChat Rufous-bandedHoneyeater YellowHoneyeater Miner Bell WesternWattlebird WesternSpinebill Westernwhite-naped Honeyeater Brown-backedHoneyeater Yellow-spottedHoneyeater GracefulHonyeater MangroveHoneyeater Yellow-throatedHoneyeater Black-headedHoneyeater Strong-billedHoneyeater White-streakedHoneyeater YellowWattlebird VariedHoneyeater Black-earedMiner Tawny-breastedHoneyeater BridledHoneyeater KimberleyHoneyeater White-linedHoneyeater Macleay'sHoneyeater Green-backedHoneyeater EungellaHoneyeater

Figure 4.1 Geographic range sizes per species (occurrence in a 100 x 100 grid cell).

Niche position was derived from a principal components analysis. The first principal

component (PC1) was weakly negatively correlated with geographic range size (R2 = 0.10, p =

0.005) (Figure 4.2). Species that gleaned (0.32) and used hanging manuevers to attack (0.29), used creative bill manuevers (0.28), and attacked substrates like leaves (0.32) and branches

(0.27) were found to have smaller geographic range sizes than species that were highly nectarivorous (-0.34) and took a large proportion of aerial attacks (-0.37).

6 5 4 (log)Geographic range size range (log)Geographic 3 2 1 0

-4 -2 0 2 4

PC1

Figure 4.2 There was a negative relationship between geographic range size and the first principal component (R2 = 0.10, p = 0.005). The PC1 axis was driven by a gradient from nectarivorous, aerial species (negative numbers) to gleaning, hanging species that often foraged in high canopies (positive numbers). Species that gleaned and hung from leaves and branches in tall canopies were found to have smaller geographic range sizes than species that were highly nectarivorous and aerial.

On the low geographic range size and positive loadings end of the spectrum was the entire Melithreptus clade. This group foraged on bark, on trucks of trees, and were often found in tall canopies. A species with a small geographic range on the positive end of the axis was

Macleay’s Honeyeater. They have a geograhic range size of 8 (tied at 3.5 smallest geographic range). Macleay’s frequently gleaned (33%), probed 66%, but used wing-powered manuevers very infrequently (3%). Forty seven percent of their attacks were to leaves. Another example at this end is Black-eared Miners. They had a range size of 11 (8). They, along with the Bell

Miners, gleaned more than any other Australian Honeyeater (92%). Generally, they were gleaning leaves (60%) and branches (21%). They took very few wing-powered manuevers (1%) and were only 4% nectarivorous.

On the other end were species with large ranges that tend to have a fair amount of nectar in their diets, and frequently used wing powered manuevers to make attacks to the air. Black

Honeyeaters occurred across a large geographic range (378) and are ranked as having the 69th largest niche. Black Honeyeaters are highly nectarivorous (69%) and used more attacks to air than any other honeyeater in Australia (28%). White-fronted Honeyeaters (Purnella albifrons) were 60% nectarivorous (ranked 60th) . They also used many wing-powered manuevers (22%).

They are considered to be nomadic. Banded Honeyeaters (Certhionyx pectoralis) were 76% nectarivorous (ranked 72nd). Banded Honeyeaters had the lowest gleaning scores in the family

(3%).

The number of habitat types each species occurred in ranged from as low as 7 to has high as 78 out of the 85 types possible (Figure 4.3). The fewest vegetation types were for Eungella and Kimberley Honeyeaters (Meliphaga fordiana), which both occurred in 7 types. Eungella

Honeyeaters are limited to a small area of plateau rainforest in Queensland and Kimberley 97

Honeyeaters occupy a small area of sandstone and adjacent rainforest in the Kimberley region of

Western Australia. The other species that occupied only a few vegetation types was Green- backed Honeyeater. In the moist lowland forest where they occur, there are 8 vegetation types represented. Singing Honeyeaters occurred in 78 different habitat types and they are widely distributed across Australia. Singing Honeyeaters had the largest geographic range in the dataset.

Just behind them was the Spiny-cheeked Honeyeater with 77 habitat types. They had the 3rd largest geographic range size. Yellow-throated Miners were found in 76 habitat types including mallee, gardens, and woodlands. We predicted that the number of habitat types and foraging niche size would be positively correlated, but there was no significant pattern (R2 = 0.02, p =

0.27). 98

Habitat breadth (number of vegetatio of (number breadth Habitat 40

0 White-plumedHoneyeater SingingHoneyeater Spiny-cheekedHoneyeater Yellow-throatedMiner Miner Noisy RedWattlebird BrownHoneyeater LittleFriarbird Brown-headedHoneyeater NoisyFriarbird Blue-facedHoneyeater CrimsonChat White-earedHoneyeater StripedHoneyeater White-frontedChat Black-chinnedHoneyeater Yellow-facedHoneyeater Gray-frontedHoneyeater NewHolland Honeyeater White-frontedHoneyeater BlackHoneyeater Yellow-plumedHoneyeater EasternSpinebill OrangeChat White-napedHoneyeater Tawny-crownedHoneyeater PiedHoneyeater FuscousHoneyeater White-throatedHoneyeater PaintedHoneyeater LittleWattlebird Rufous-throatedHoneyeater Yellow-tuftedHoneyeater ScarletHoneyeater White-cheekedHoneyeater CrescentHoneyeater Purple-gapedHoneyeater Gray-headedHoneyeater White-gapedHoneyeater Lewin'sHoneyeater BandedHoneyeater Yellow-tintedHoneyeater Silver-crownedFriarbird DuskyHoneyeater HelmetedFriarbird Bar-breastedHoneyeater YellowHoneyeater Miner Bell RegentHoneyeater YellowChat GracefulHonyeater Yellow-spottedHoneyeater Gibberbird Red-headedHoneyeater Brown-backedHoneyeater Rufous-bandedHoneyeater Yellow-throatedHoneyeater YellowWattlebird WesternSpinebill WesternWattlebird MangroveHoneyeater Black-headedHoneyeater Strong-billedHoneyeater Macleay'sHoneyeater GrayHoneyeater VariedHoneyeater Westernwhite-naped Honeyeater BridledHoneyeater Tawny-breastedHoneyeater White-streakedHoneyeater Black-earedMiner White-linedHoneyeater Green-backedHoneyeater EungellaHoneyeater KimberleyHoneyeater

Figure 4.3 Number of vegetation types occupied per species.

As predicted, the number of vegetation types and geographic range size were positively

related (R2 = 0.74, p <0.001) (Figure 4.4). There was an interesting non-linearity in the

relationship, where species that occurred in the most habitat types occurred over a proportionally

larger range size than species that occurred in fewer habitat types. Species with small geographic

range size (occurrence in <50 grid cells) that also occurred in only a few habitat types (< 10)

were species such as the Green-backed and Eungella Honeyeaters. Then, there were species like

Gibberbird (Ashbyia lovensis), Yellow chats (Epthianura crocea), Red-headed Honeyeaters

(Myzomela erythrocephala) and Black-eared Miners that had low to intermediate range sizes and vegetation types that they occurred in. From 50-60 vegetation types, range size ranges from 100 -

200 grid cells. After 60 vegetation types, there was a drastic increase in the geographic range size. Species that occurred in over 60 vegetation types included: Orange Chats (Epthianura aurifrons), Pied (Certhionyx variegatus), Black, White-fronted, Crimson (Epthianura tricolor),

Brown (Lichmera indistincta) and Spiny-cheeked Honeyeaters (Acanthagenys rufogularis), and

Yellow-throated Miners (Manorina flavigula).

DISCUSSION The mixed support for a geographic range size and foraging niche size was surprising given the support in the literature, but there are several potential explanations. It could simply be that the relationship is much more complex than a simple regression can pick up. Range size is likely driven by things other than foraging niche. Dispersal ability (Beck and Kitching 2007,

Lester and Ruttenburg 2007, Arribas 2011), evolutionary history (Webb and Gaston 2000,

Swaegers et al. 2014), body size and other physiological correlates (Gaston and Blackburn 1996,

Wollenberg 2011), and species density and abundance (Purvis 2000, Gaston et al. 1997, Johnson

1998) are just a few of the current explanations for differences in range size. In Slatyer’s 2013 100 meta-analysis of the niche breadth – range size hypothesis, he found good support of habitat breadth and range size and also between environmental tolerance and range size, but the relationship was less strong and only marginally significant for diet. He suggested that it is potentially an issue of scale. It is possible that local specialists may be regional generalists. Our foraging behavior measurements were taken on a very fine scale, whereas geographic range size is a species’ occurrence in a 100 x 100 km grid cell, which might have only one vegetation layer or many. Species can likely access multiple food types per vegetation type. While our measurement of geographic range size is more precise than other types of range maps (like extent of occurrence - EOO), our measurement might not be as precise as using species distribution maps, (Austin 1990, Guisan and Thullier 2005). EOO maps have been criticized for overestimating a species’ range (Jetz et al. 2007 and 2008) especially for rare species.

We did not see a significant relationship between foraging niche size and habitat breadth.

One might assume that if there is more potential foraging space and diversity in vegetation type, species might be more diverse in their foraging behavior, but we did not find that. A more telling assessment might include pulling vegetation layers from specific points (latitude and longitude) where a foraging behavior occurred. In this paper we are not breaking species down to subspecies, but that might be a taxonomic scale at which we would see a trend. It is possible that a continent-wide approach is not the best fit because specialization or generalization of diet could be scale dependent (Hughes 2000).

There was a weak, but significant negative relationship between foraging niche position and geographic range size. Foraging niche position was derived from a principal components analysis. The first principal component (PC1) was significantly related to geographic range size.

On one extreme of that axis were some distinct foraging techniques: hang to attack, glean and 101 creative bill maneuvers. Foraging substrates included leaves and branches and they tended to be species that forage in high canopies. The species at that extreme also had smaller geographic ranges like the Melithreptus clade, Macleay’s Honeyeater, Mangrove Honeyeater (Lichenostomus fasciogularis), and Eungella Honeyeater. The other end of the axis was species that were highly nectarivorous and species that frequently made attacks to the air for insects. Some species on that end were Black Honeyeaters, White-fronted Honeyeaters, Eastern Spinebills (Acanthorhynchus tenuirostris), and Tawny-crowned Honeyeaters. These highly nectarivorous species are often nomadic or short-distance migrants that follow blooming events and therefore are dependent on a larger geographic range size than species with less ephemeral diets. There is also the possibility that this trend was somewhat driven by forests with tall canopies occurring in only a small proportion of Australia. Species dependent on these forest types likely occupy only remnants of their former extent due to conversion of land for agriculture and development, grazing, and fire.

The number of vegetation types a species occurred in (habitat breadth) was positively associated with geographic range size, which makes intuitive sense. A linear response between geographic range size and habitat breadth is to be expected, but the trend is actually quadratic

(Figure 4.4). After around 50 vegetation types accumulated, there was much more variation in range size. This may be because such habitat generalist species can occur nearly everywhere in

Australia. Habitat specialists usually occupy smaller geographic areas and generalists are more widespread (Brown 1984, Pyron 1999, Slatyer 2013). 102

600 500 400 Geographic range size (sum of occupied occu of size (sum range Geographic 300 200 100 0

10 20 30 40 50 60 70 80

Habitat breadth (number of occupied vegetatio

Figure 4.4 As geographic range size increased, so did the number of vegetation types that a species occurred in (R2 =0.74, p <0.001). The unimodal response highlights increased variance after a species occurs in 50 vegetation types.

These results combine a large data set of fine scale foraging behavior measurements with coarse-scale landscape measurements to test assumptions of niche size and range size. To better predict response to future change, one might include measurements of dispersal power or ability, 103

and take a closer look at evolutionary history. Ability to disperse or an innate migratory behavior

could give species the ability to change locations in times of drought, fire, or habitat

modification (Lester et al. 2007, Thomas et al. 2004). If range size is strictly determined by the

age of a species, we would expect that there would be a positive relationship between a species’

age and a species’ range size (Gaston 1998, Hodge and Bellwood 2015). In this paper we are not

addressing the evolutionary processes driving patterns of range size. The combined effects of being a specialist and also having a small range size make many of these species much more susceptible to disturbance from land use change than even previously anticipated (Purvis 2000,

Davies et al. 2004).

104

CHAPTER V

CONCLUSION

We now have clear and dramatic evidence of anthropogenic disturbance and our ability to predict how ecosystems may respond to future shifts has never been more important. Using an entire family of birds across the continent of Australia, I was able to quantify the foraging niche per species. That foraging niche description contains pertinent information for the future of many of Australia’s honeyeaters. In this dissertation, I have developed a method for measuring foraging niche, found evidence for the tight link between behavior and conservation, described foraging niche traits across a phylogeny, applied that foraging niche to measures of sensitivity and exposure to climate change and tested a much argued and often supported hypothesis where niche breadth and geographic range size are positively correlated. While foraging behavior studies are not novel to ornithology, incorporating the many variable types into one measurement of niche, to my knowledge, is.

Foraging behavior is a good measurement of which species specialize either on a certain behavior or food item, or habitat type. That specialization is something that makes species more susceptible to disturbance. It is clear that most foraging niche traits are phylogenetically conserved (Chapter II). Closely related species forage in similar ways, except in some cases where they co-occur. There was strong evidence for insectivores and nectarivores having the smallest niches. I was also able to test the hypothesis that as nectar increases in a species’ diet, so do attacks to the air for insects (protein sources). 105

While foraging niche size was not directly related to sensitivity and exposure as

categorized by Franklin and Garnett (2014), and there were too few IUCN categories outside of

least concern to do an analysis, qualitatively we can say that species at high risk often have diet

specializations. They also often have a plethora of threats including drought, habitat

modification, fire, and genetic swamping. These stresses can have additive or synergistic effects

on species that also have fewer ways that they acquire food and fewer food items. There was a

trend in the opposite direction than I had anticipated with IUCN’s categories of population trend

when compared to both the 2nd axis of the principal components analysis and foraging niche size.

Decreasing populations belonged to species with larger niche sizes than species whose populations were increasing, though there were only 3 species in that category. Species whose populations were decreasing also were affiliated with dense vegetation with closed canopies and increasing populations spanned the axis.

In Chapter IV, I was able to test the niche breadth-range size hypothesis and found no

support for geographic range size and foraging niche size, but we did find a significant positive

trend between habitat breadth (number of vegetation types a species occurs in) and geographic

range size (species occurrence in a 100 x 100km grid cells). That result in conjunction with a

lack of a relationship between number of vegetation types and foraging niche size highlights the

importance of the behavior and attack maneuvers used by different species. It is not just a more

structurally heterogeneous habitat that drives a larger niche size. I also found good evidence of a

relationship between geographic range size and the first principal component (PC1). Species

with small ranges were associated with hanging, gleaning, and high canopies.

I will continue to work with this dataset to look at how the addition of my foraging niche

size metric (FDis) to Garnett and Franklin’s (2012) sensitivity to climate change category 106 changes the outcome. I assume that their assessment could be strengthened by the fine scale detail in my foraging dataset. I predict that sensitivity will increase for many species. In addition to the analyses of niche breadth-range size, I want to add species’ abundance and range size

(Purvis 2000, Gaston et al. 1997, Johnson 1998). I expect that this relationship is dependent on the vegetation structure of occupied cells and that closely related species will show similar patterns. Following Brown’s (1984) thinking, species that occupy wider diet and habitat niches will have higher local abundances and be more geographically widespread and specialized species will show the opposite trend. This component would be nice addition to chapter IV.

107

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