Consequences of Rainforest Fragmentation for FrugivorousVertebrates and Seed Dispersal

Author

Moran, Catherine

Published

2007

Thesis Type

Thesis (PhD Doctorate)

School

Griffith School of Environment

DOI

https://doi.org/10.25904/1912/54

Copyright Statement

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

Downloaded from

http://hdl.handle.net/10072/367385

Griffith Research Online

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Consequences of rainforest fragmentation for frugivorous

vertebrates and seed dispersal

Catherine Moran

B.Sc. (Hons.)

Griffith School of Environment

Faculty of Science, Engineering, Environment and Technology

Griffith University

Submitted in fulfilment of the requirements of the degree of Doctor of Philosophy

June, 2007

i

Abstract

Seed dispersal strongly influences patterns of plant regeneration. Frugivorous

(fruit eating) vertebrates disperse the seeds of between 70% and 90% of rainforest plant

species. Forest fragmentation may affect the abundance and distribution of frugivore

species. Consequently, patterns of seed dispersal and plant regeneration may vary

between extensive forest and fragmented forest landscapes. This thesis assessed

frugivorous vertebrates and seed dispersal in a rainforest landscape in subtropical

Australia. First, this study quantitatively compared the distribution and abundance of

frugivorous bird and bat species between fragmented and extensive rainforest. Second,

the roles of these frugivore species in seed dispersal were evaluated based on their

functional attributes and the plant species that they had been recorded consuming.

Third, secondary consequences of forest fragmentation for seed dispersal were predicted

from these results.

The field components of this study were conducted in the Sunshine Coast region

of southern Queensland. Surveys of frugivorous bird and bat species were undertaken in

a network of 48 study sites distributed throughout a 4 000 km2 area. Sites comprised 16

replicates of each of three site types: extensive forest (> 4 000 ha), rainforest remnants

and patches of secondary regrowth. Extensive forest sites were stratified by altitude

(low (<200 m above sea level (a.s.l.), medium (200-500 m a.s.l.), and high (>500 m

a.s.l.).

Birds were surveyed using 40 minute area searches within a one hectare plot

during the early morning. Each site was surveyed for birds four times: twice during

summer and twice in winter. Forty-two frugivorous bird species were identified during

surveys. Twenty-six of these species occurred frequently enough to quantitatively assess

their abundance pattern in remnant and regrowth sites relative to extensive forest. There

ii

were five species that were recorded in much lower numbers in remnants and/or

regrowth than in extensive forest (‘decreasers’), seven that showed higher abundance in

remnants and/or regrowth than in extensive forest (‘increasers’) and 14 whose

abundance did not vary substantially between the three habitat types (‘tolerant’ species).

The decreasers included four rainforest pigeons (the wompoo, rose-crowned and superb

fruit-doves Ptilinopus magnificus, P. regina and P. superbus and brown cuckoo-dove

Macropygia amboinensis) and the green catbird Ailuroedus crassirostris. There was no

evidence for the complete seasonal movement of frugivorous bird species between high

and low altitudes.

A lack of understanding of the functional roles of frugivorous species has

previously limited our capacity to predict specific consequences for seed dispersal of

frugivore declines. A major dimension of functional variation among frugivore species

is the suite of plant species that they disperse, which depends initially on their patterns

of consumption of plant species. In this thesis, frugivorous bird species that were

expected to have similar patterns of plant species consumption were assembled into

‘functional groups’. These groupings were based on the bird species’ gape width, degree

of frugivory and their methods of seed treatment. For example, it was proposed that

species with wide gapes would be able to consume large fruits, whereas those with

narrow gapes could only consume small fruits. It was also expected that species with

fruit-dominated diets (‘major frugivores’) may consume a different suite of plant

species than species with mixed diets or with diets dominated by non-fruit (‘minor

frugivores’). Species that crushed seeds were expected to disperse few viable seeds.

Analyses showed that decreaser bird species were predominantly from functional

groups that had the potential to disperse large-seeded plant species and may be the main

dispersers of native laurels (Lauraceae). Consequently, it is likely that the dispersal of

these plants may be reduced in fragmented forest.

iii

Relationships between the functional attributes of frugivores and their actual

patterns of plant species consumption were analysed using data on the plant species that

each frugivore species was known to consume. Diet data were collated from 151

published sources as well as field observation and included records for 244 plant

species. Major variation in patterns of plant species consumption corresponded with

variation in frugivore species’ attributes. For example, the average size of fruits

consumed by bird species increased with their gape width, although minor frugivores

tended to consume fruits that were much smaller than their capacity. Statistical

comparisons showed that highly frugivorous bird species consumed the highest number

of plant species from the Lauraceae, whereas bird species with mixed diets consumed

more arillate plant species from the Celastraceae, Sapindaceae, Mimosaceae and

Elaeocarpaceae than other frugivore groups. Bird species from a range of functional

groups consumed figs and small-fruited plants from families such as Euphorbiaceae and

Solanaceae. Minor frugivores and a small number of major and mixed-diet bird species

had species-poor diets that were dominated by these latter plant taxa.

In order to specifically assess the potential consequences of forest

fragmentation for seed dispersal, patterns of plant species consumption were compared

among decreaser, tolerant and increaser frugivore species. In particular, the potential for

tolerant and increaser bird species to substitute for decreasers was evaluated. Analyses

showed that dietary records for 12% of the 220 native plant species represented in the

data set, including several from the Rubiaceae, were restricted to decreaser bird species.

In addition, analyses showed that few non-decreaser species consumed numbers of

native plant species with fruits wider than 10 mm, or from the Lauraceae, Myrtaceae,

Meliaceae, Verbenaceae and Vitaceae that were comparable to decreaser bird species.

Consequently, it is predicted that there is limited potential for functional substitution by

iv

other bird species for decreasers and, therefore, that the dispersal of these plant taxa

may be substantially reduced in fragmented compared with extensive rainforest.

The potential for frugivorous bats to disperse seeds in fragmented forest was

also assessed. Frugivorous bats were surveyed during summer in each of the 48 sites

that had been surveyed for birds. Two observers conducted nocturnal, hour long

searches along a 400-500 m transect. Two flying-fox species (grey-headed flying-fox

Pteropus poliocephalus and black flying-fox P. alecto) and the eastern tube-nosed bat

Nyctimene robinsoni were recorded during surveys. At the time of surveys, Pteropus

spp. were most frequently recorded in regrowth, whereas N. robinsoni was detected

more frequently in extensive forest and remnants than in regrowth. Decreaser bird

species and N. robinsoni are rainforest and fruit specialists whereas tolerant and

increaser bird species and Pteropus spp. have more generalist patterns of habitat and

resource use. N. robinsoni has limited potential to substitute for decreaser bird species

as a seed disperser in fragmented rainforest of the study region, because it is known to

consume only a small number of plant species and because of its rarity in regrowth. In

contrast, Pteropus spp. were widespread in fragmented forest and consumed

approximately one-third of the plant species that were consumed by decreaser bird

species. In fragmented landscapes, Pteropus spp. may potentially substitute for

decreaser bird species as dispersers of large-fruited plant taxa and plants from the

Myrtaceae, although they appear unlikely to disperse seeds >9 mm more than short

distances away from parent plants.

The results of this study show that fragmented remnant and regrowth patches of

rainforest do not adequately conserve the full complement of frugivorous vertebrate

species in the subtropics of eastern Australia. Although the number of frugivore species

that showed sensitivity to rainforest fragmentation was relatively small, this may have

substantial functional consequences. These consequences are likely because decreaser

v

species may be the sole or predominant dispersers of a substantial proportion of native

plant species, which may consequently be susceptible to reduced dispersal away from

parent plants in fragmented forest. Reduced dispersal may have a number of

implications for plant regeneration. First, dispersal to recruitment sites within forest

fragments is likely to be reduced, resulting in lower rates and clumped spatial patterns

of recruitment. Second, dispersal of these species between rainforest fragments may be

lower, leading to low rates of recolonisation following local extinctions. Third, short-

distance dispersal to new habitats may be lower, resulting in low representation of

susceptible plant species in regenerating forest on previously cleared land. Fourth, long

distance dispersal of these plant taxa would be low, which would mean that they may

have a limited capacity to shift their geographical range, for example in response to

changing global climatic conditions.

Further clearing and fragmentation of rainforest would exacerbate the situation

for decreaser frugivore species and may lead to the decline of additional frugivore

species. It is recommended that remaining rainforest be protected from continued

clearing. Restoration of forest areas based on the needs of decreaser frugivore species

may help to re-establish them in fragmented landscapes. These actions could help to

restore the regenerative capacity of many rainforest plant species and hence increase the

long term integrity of fragmented rainforest ecosystems.

vi

Statement of originality

This thesis has not previously been submitted for a degree or diploma in any university.

To the best of my knowledge and belief, the thesis contains no material previously

published or written by another person except where reference is made in the thesis

itself.

…………………………………

C. Moran

Publications arising from this thesis

Slightly modified versions of Chapters Two and Three have previously been

peer reviewed and published as a book chapter and journal article, respectively. I was

responsible for conducting the research reported in those publications. The co-authors

were listed in recognition of their contributions as my academic supervisors. These

publications are listed below:

Chapter Two: Moran C, Catterall CP, Green RJ and Olsen MF (2004) Fates of

feathered frugivores in fragmented forests. pp. 699-712 in Lunney D (Ed.) Conservation

of Australia’s Forest Fauna. Second edition. Royal Zoological Society of NSW,

Mosman.

Chapter Three: Moran C, Catterall CP, Green RJ and Olsen MF (2004) Functional

variation among frugivorous birds: implications for rainforest seed dispersal in a

fragmented subtropical landscape. Oecologia 141, 584-595.

vii

Table of contents

ABSTRACT...............................................................................................................................................I

STATEMENT OF ORIGINALITY ........................................................................................................VI

PUBLICATIONS ARISING FROM THIS THESIS ..............................................................................VI

LIST OF FIGURES ...............................................................................................................................XII

ACKNOWLEDGEMENTS ................................................................................................................. XIII

CHAPTER ONE: EFFECTS OF RAINFOREST FRAGMENTATION ON FRUGIVOROUS

VERTEBRATES AND THE POTENTIAL CONSEQUENCES FOR SEED DISPERSAL AND

PLANT REGENERATION ...................................................................................................................... 1

1.1 RAINFOREST FRAGMENTATION, FOREST FAUNA AND SEED DISPERSAL............................................ 1

1.2 THE FUNCTIONAL ROLE OF FRUGIVORES IN SEED DISPERSAL .......................................................... 2

1.3 THE ROLE OF SEED DISPERSAL IN PLANT REGENERATION................................................................ 8

1.4 CONSEQUENCES OF RAINFOREST CLEARING AND FRAGMENTATION FOR FRUGIVORES .................. 11

1.5 RELATIONSHIPS BETWEEN FRUGIVORE SPECIES’ TRAITS AND THEIR SENSITIVITY TO

RAINFOREST FRAGMENTATION...................................................................................................... 16

1.6 CONSEQUENCES OF CHANGES IN THE COMPOSITION OF FRUGIVORE ASSEMBLAGES FOR SEED

DISPERSAL AND PATTERNS OF PLANT REGENERATION................................................................... 20

1 .7 AIMS AND STRUCTURE OF THIS THESIS......................................................................................... 26

1.8 RAINFOREST FRAGMENTATION, FRUGIVORES AND SEED DISPERSAL IN AUSTRALIA...................... 31

CHAPTER TWO: CHANGES IN THE AVIAN FRUGIVORE ASSEMBLAGE IN

FRAGMENTED RAINFOREST COMPARED WITH EXTENSIVE FOREST IN SUBTROPICAL

AUSTRALIA .......................................................................................................................................... 34

2.1 INTRODUCTION ............................................................................................................................. 34

2.2 METHODS ..................................................................................................................................... 35

2.2.1 Study region.......................................................................................................................... 35

2.2.2 Site network .......................................................................................................................... 37

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2.2.3 Bird surveys .......................................................................................................................... 42

2.2.4 Data treatment...................................................................................................................... 42

2.2.5 Classification of frugivorous birds ....................................................................................... 44

2.3 RESULTS ....................................................................................................................................... 45

2.3.1 Abundance of frugivorous bird species in extensive, remnant and regrowth sites ............... 45

2.3.2 Changes in the frugivorous bird assemblage in fragmented forest ...................................... 51

2.3.3 Seasonal patterns of frugivorous bird abundance ................................................................ 54

2.3.4 Effects of altitude and season on frugivorous bird numbers................................................. 54

2.4 DISCUSSION .................................................................................................................................. 57

2.4.1 Bird species showing a decreaser response to rainforest fragmentation ............................. 57

2.4.2 Bird species showing an increaser response to fragmentation............................................. 60

2.4.3 Frugivore assemblage change in fragmented habitats ......................................................... 61

2.4.4 Seasonal changes in frugivorous bird abundance ................................................................ 62

2.4.5 Frugivorous birds and seed dispersal in remnant and regrowth rainforest:

conservation implications.................................................................................................... 63

CHAPTER THREE: SEED DISPERSAL POTENTIAL OF FRUGIVOROUS BIRD SPECIES IN

RELATION TO THEIR GAPE WIDTH, FRUGIVORY LEVEL AND SEED TREATMENT ............ 67

3.1 INTRODUCTION ............................................................................................................................. 67

3.2 METHODS ..................................................................................................................................... 70

3.2.1 Assessment of the functional attributes of frugivorous bird species: gape width,

frugivory level and seed-crushing behaviour ...................................................................... 70

3.2.2 Data analyses ....................................................................................................................... 72

3.3 RESULTS ....................................................................................................................................... 74

3.3.1 Variation in seed dispersal potential among species within the frugivorous bird

assemblage .......................................................................................................................... 74

3.3.2 Functional group abundance in remnants and regrowth relative to extensive forest........... 78

3.4 DISCUSSION .................................................................................................................................. 81

3.4.1 Characteristics of the frugivorous birds assemblage ........................................................... 81

3.4.2 Functional characteristics of the frugivorous bird assemblage in fragmented

rainforest in subtropical Australia: assessment of potential consequences for seed

dispersal .............................................................................................................................. 81

ix

CHAPTER FOUR: VARIATION IN PATTERNS OF PLANT SPECIES CONSUMPTION BY

FRUGIVOROUS BIRD SPECIES IS RELATED TO GAPE WIDTH, DEGREE OF FRUGIVORY

AND SEED TREATMENT .................................................................................................................... 87

4.1 INTRODUCTION ............................................................................................................................. 87

4.2 METHODS ..................................................................................................................................... 89

4.2.1 Diet composition of the frugivorous bird assemblage .......................................................... 89

4.2.2 Functional attributes of bird species .................................................................................... 91

4.2.3 Data analyses ....................................................................................................................... 92

4.3 RESULTS ....................................................................................................................................... 94

4.3.1 General patterns of plant consumption................................................................................. 94

4.3.2 The effect of gape width and frugivory level on diaspore size selection............................... 97

4.3.3 Plant species richness of the diets of major, mixed and minor frugivores............................ 99

4.3.4 Plant species diet composition in relation to frugivory level, gape width and seed

treatment............................................................................................................................ 100

4.4. DISCUSSION ............................................................................................................................... 109

4.4.1 Overlap and variation among frugivorous bird species in patterns of plant species

consumption....................................................................................................................... 109

4.4.2 Frugivore gape width and patterns of fruit size consumption ............................................ 110

4.4.3 Frugivory level and patterns of plant species consumption................................................ 111

4.4.4 Variation among bird species within a frugivory level....................................................... 113

4.4.5 Gape width and frugivory level as indicators of the functional potential of

frugivorous birds as seed dispersers ................................................................................. 114

CHAPTER FIVE: REDUCED DISPERSAL POTENTIAL OF NATIVE RAINFOREST PLANT

SPECIES IN FRAGMENTED RAINFOREST..................................................................................... 116

5.1 INTRODUCTION ........................................................................................................................... 116

5.2 METHODS ................................................................................................................................... 119

5.2.1 Changes in the frugivorous bird assemblage in fragmented subtropical rainforest........... 119

5.2.2 Fruit consumption database ............................................................................................... 119

5.2.3 Data analyses ..................................................................................................................... 120

5.3 RESULTS ..................................................................................................................................... 121

5.3.1 Diet comparisons between frugivore response groups ....................................................... 121

x

5.3.2 Specific substitution potential between frugivore taxa ....................................................... 128

5.4 DISCUSSION ................................................................................................................................ 137

5.4.1 Reduced dispersal of native rainforest plants as a consequence of rainforest

fragmentation..................................................................................................................... 137

5.4.2 Potential for disperser substitution in fragmented forest ................................................... 139

5.4.3 Implications for conservation of regenerative potential in fragmented rainforest ............. 141

CHAPTER SIX: THE DISTRIBUTION OF FRUGIVOROUS BATS AND THEIR POTENTIAL

TO DISPERSE SEEDS IN FRAGMENTED RAINFOREST. ............................................................. 143

6.1 INTRODUCTION ........................................................................................................................... 143

6.2 METHODS ................................................................................................................................... 146

6.2.1 The study region and site network ...................................................................................... 146

6.2.2 Surveys of frugivorous bat distribution............................................................................... 146

6.2.3 Frugivorous bird data......................................................................................................... 147

6.2.4 Information on the consumption of native plant species by frugivorous bat and bird

species................................................................................................................................ 148

6.2.5 Data handling ..................................................................................................................... 149

6.3 RESULTS ..................................................................................................................................... 150

6.3.1 Distribution and abundance of frugivorous bats ................................................................ 150

6.3.2 Association of bat distribution with environmental attributes............................................ 153

6.3.3 Comparison between frugivorous bat and bird species in their patterns of plant

species consumption .......................................................................................................... 154

6.3.4 Potential for frugivorous bat species to substitute for decreaser bird species as

dispersers in fragmented forest.......................................................................................... 158

6.4 DISCUSSION ................................................................................................................................ 158

6.4.1 The distribution of flying-foxes in fragmented rainforest in the Sunshine Coast................ 158

6.4.2 The distribution of the eastern tube-nosed fruit-bat in fragmented rainforest in the

Sunshine Coast .................................................................................................................. 161

6.4.3 The potential for seed dispersal by frugivorous bats in remnants and regrowth:

comparison with frugivorous birds.................................................................................... 162

CHAPTER 7: GENERAL DISCUSSION: CONSEQUENCES OF FOREST FRAGMENTATION

FOR FRUGIVORES AND IMPLCATIONS FOR SEED DISPERSAL.............................................. 165

xi

7.1 SUMMARY OF THE FINDINGS OF THIS THESIS............................................................................... 165

7.2 THE SENSITIVITY OF FRUGIVOROUS VERTEBRATE SPECIES TO RAINFOREST FRAGMENTATION

IN SUBTROPICAL AUSTRALIA ...................................................................................................... 168

Decreaser species ........................................................................................................................ 168

Tolerant species........................................................................................................................... 171

7.3 CORRELATES OF FRUGIVORE SPECIES’ SENSITIVITY TO RAINFOREST FRAGMENTATION .............. 173

7.4 PATTERNS OF PLANT SPECIES CONSUMPTION ACROSS THE FRUGIVORE ASSEMBLAGE: AN

ALTERNATIVE MODEL ................................................................................................................. 175

7.5 POTENTIAL CONSEQUENCES OF RAINFOREST FRAGMENTATION FOR SEED DISPERSAL AND

PATTERNS OF PLANT REGENERATION .......................................................................................... 179

7.6 CONSERVATION ISSUES............................................................................................................... 185

APPENDIX 1........................................................................................................................................ 187

APPENDIX 2........................................................................................................................................ 193

APPENDIX 3........................................................................................................................................ 198

REFERENCES ………………………………………………………………………………………. 203

xii

List of figures

Figure 1.1 Conceptual representation of patterns of plant species consumption by frugivorous bird species………………………………………………………………………. 7

Figure 1.2 Potential seed dispersal trajectories in fragmented forest landscapes with respect to plant regeneration……………………………………………………………….. 22

Figure 1.3 Conceptual links between the chapters of this thesis…………………………… 30 Figure 2.1 Aerial view of part of the Sunshine Coast study region………………………… 37 Figure 2.2 Map of study region showing site locations……………………………………. 39 Figure 2.3 Examples of the seven patterns of abundance in remnants and regrowth compared

with extensive forest……………………………………………………………. 50 Figure 2.4 Ordination of the 48 study sites based on the abundances of 39 frugivorous bird

species ………………………………………………………………………….. 53 Figure 3.1 Inter-relationships between frugivorous bird attributes ……………………….. 77 Figure 3.2 Ordination of the 48 study sites based on numbers of birds from each functional

group …………………………………………………………………………… 80 Figure 4.1 The average size of diaspores consumed compared with gape width …………. 98 Figure 4.2 The average proportion of diaspores close to the maximum handling capacity

consumed by frugivores………………………………………………………… 99 Figure 4.3 The number of native plant species consumed by each frugivore ……………... 100 Figure 4.4 Overlap in the number of plant species consumed by frugivorous birds in relation to

frugivory level………………………………………………………………….. 101 Figure 4.5 Classification of frugivore species based on Bray-Curtis similarity in patterns of

consumption of native plant species……………………………………………. 106 Figure 4.6 Overlap in the number of plant species consumed by frugivorous birds in relation to

gape width classes………………………………………………………………. 109 Figure 5.1 The proportion of native plant species with large (≥10 mm) diaspores that were

consumed by decreaser, tolerant and increaser frugivore species………………. 125 Figure 5.2 Classification of frugivore species according to presence / absence of native plant

species in the diet……………………………………………………..………… 127 Figure 5.3 The number of native plant species from selected plant families consumed by

decreaser, tolerant and increaser frugivores…………………………………….. 130 Figure 5.4. Overlap in the number of native plant species consumed by frugivore species from

the decreaser, tolerant and increaser response groups…………………………... 132 Figure 6.1. The abundance (mean ± SE) of flying-foxes recorded during a 60 minute search of

extensive, remnant and regrowth forest sites…………………………………… 152 Figure 6.2 The proportion of native plant species with a median diaspore width ≥10 mm that

were known to be consumed by decreaser, tolerant and increaser bird species, and by flying-foxes……………………………………………………………………… 156

Figure 6.3 Classification of frugivore species based on similarity of patterns of consumption of native plant species………………………………………………………………. 157

Figure 7.1 Map of Australia showing the approximate location of other studies in fragmented forest that have included frugivore species…………………………….………… 169

Figure 7.2 A model of variation in patterns of plant species consumption by frugivorous bird species in subtropical Australia………………………………………………….. 176

Figure 7.3 Relationship between bird species’ gape widths and their body mass………….. 179 Figure 7.4 The frugivore species that potentially disperse seeds along different dispersal

trajectories in fragmented forest landscapes ………………………………… 182-3

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Acknowledgements

I thank my principal supervisor, Associate Professor Carla Catterall, for her

contributions to all stages of this project. This thesis and my PhD experience have

greatly benefited from her dedicated attention and brilliant clear thinking. I am also

grateful to my associate supervisors, Drs. Ronda Green and Mike Olsen, for their

important contributions to this project, especially in its formative stages.

I acknowledge the traditional owners of the country in which the field

components of this work were conducted, the Ka’bi or Gubbi Gubbi, Undumbi and

Badtjala people. I am grateful to the people who supported my field work on their land:

Caloundra City Council, Mim Coulstock, David and Bernie Daugaard, John and Joan

Dillon, Wally and Annalies Gogel, Barbara Hansa, Max and Chrissie Hendersen, Ken

and Trish Long, Gillian and Neil MacLeod, Ted McCosker, Maroochy Shire Council,

Noosa Shire Council, John and Valerie Poulson, Arthur and Narelle Powter,

Queensland Environmental Protection Agency, Graham and Annabel Wearne and Greg

and Charmaine Wightman.

I acknowledge and thank the people who have generously contributed data to

this project. John Kanowski conducted bat surveys simultaneously with the author. Carl

Gosper, Damian Hackett and Stephen McKenna provided large amounts of unpublished

data from their work on frugivory and Stephen McKenna contributed information on

fruit attributes from his collection. Lyla, John and Francis Hansen, Val Jones, Valda

McLean and Shirley Rooke voluntarily conducted frugivory observations throughout

the Sunshine Coast.

I am grateful to the people who have facilitated logistical aspects of this project.

Financial support was provided by an Australian Postgraduate Research Award, the

Rainforest Co-operative Research Centre, Griffith University, and the Norman

xiv

Wettenhall Foundation. Dave Curmi assisted with field site set up. Heather Janetski

arranged for access to bird specimens at the Queensland Museum and Chris Stansbury

and John Kanowski helped to measure their gapes. Milton and Merle Rawson provided

generous hospitality during components of my field work. Child care was provided by

Cath Cleary and Bev Moran and especially by Maureen and Peter Kanowski who made

an enormous contribution to the care of Stella while I worked on my thesis.

Helpful advice on various technical aspects of the project was generously

provided by the following people: Nick Clancy, Les Hall, Rachel King, Bill McDonald,

and members of Wildlife Ecology Discussion Group at Griffith University (at various

times including Carla Catterall, Paul Finn, Ronda Green, Peter Grimbacher, Clare

Hourigan, John Kanowski, Stephen McKenna, Aki Nakamura, Wendy Neilan, Scott

Piper, Terry Reis, Billie Roberts and Tang Yong).

During my time at Griffith University, Rachel King, Scott Piper, Naomi Doak

and Sarah Boulter have provided encouragement, empathy, perspective, humour, and

intellectual and musical adventure. These have been so important.

The kindness and encouragement of my friends, parents, siblings, grandparents

and parents- and siblings-in-law has helped keep me going. My family, John, Stella and

Ruby, have been patient, considerate and positive, despite the toll this project has taken

on our time together, among other things. In particular, I thank John for his many

sacrifices and logistical and moral support.

1

Chapter One

Effects of rainforest fragmentation on frugivorous vertebrates and the

potential consequences for seed dispersal and plant regeneration

1.1 Rainforest fragmentation, forest fauna and seed dispersal

Rainforest has been heavily cleared and fragmented worldwide (e.g., Myers,

1984; Turner and Corlett, 1996; Whitmore, 1997). The long-term survival of rainforest

flora and fauna in the wild will therefore depend on their ability to persist in fragmented

rainforest landscapes (Myers, 1984; Laurance, 1991; Daily et al., 2001; Sodhi et al.,

2004).

Rainforest fragmentation has negative consequences for the distribution and

abundance of many forest biota (e.g., Turner, 1996; Laurance and Bierregaard, 1997;

Laurance and Peres, 2006). Because animals play important roles in rainforest

dynamics, changes in the composition of rainforest fauna in fragmented forest

landscapes may have secondary consequences for plant-animal interactions and

ecosystem functions (Burkey, 1993; Didham et al., 1996; Daily et al., 2001; van Bael et

al., 2003; Şekercioğlu et al., 2004; Hooper et al., 2005; Şekercioğlu, 2006). For

example, between 70% and 90% of rainforest plant species are fleshy-fruited (Howe

and Smallwood, 1982; Willson et al., 1989; Butler, 2003). Frugivorous (fruit eating)

fauna are the main dispersers of the seeds of fleshy-fruited plants (van der Pijl, 1982;

Corlett, 1998). Therefore, changes in the frugivore assemblage in rainforest remnants

could alter the dispersal of a large proportion of the rainforest flora in fragmented

landscapes (Corlett, 1998; Silva and Tabarelli, 2000). The extent to which this occurs

2

will depend the level of variation among frugivore species in their function as seed

dispersers.

1.2 The functional role of frugivores in seed dispersal

Seed dispersal is the movement of seed away from a parent plant (Howe and

Smallwood, 1982; Levin et al., 2003). Birds are an abundant and diverse element of the

frugivorous fauna in forests worldwide (e.g., Corlett, 1998). Mammals and to a lesser

extent, reptiles, amphibians, fish and invertebrates may also play a role in seed dispersal

(Corlett, 1998). Frugivorous animal species vary in their functional roles as seed

dispersers as a consequence of several factors. Primary variation among frugivore

species arises from differences in the suite of plant species that they consume and hence

disperse (Crome, 1975; Snow, 1981; Herrera, 1984; Howe, 1986; Innis, 1989; Sun et

al., 1997; Brown and Hopkins, 2002). Variation among frugivore species in the suite of

plant species that they consume is affected by the interaction between the

morphological, physiological and behavioural traits of the frugivore species and the

morphological, chemical and nutritive traits of the fruits of plant species (Gautier-Hion

et al., 1985; Moermond and Denslow, 1985; Corlett, 1996; Kitamura et al., 2002;

Poulsen et al., 2002; Silva et al., 2002).

There is broad variation in patterns of plant consumption among higher

taxonomic groupings of frugivores (van der Pijl, 1982; Gautier-Hion et al., 1985;

Willson et al., 1989; Bollen et al., 2004). For example, because they have teeth, most

mammals can consume large fruits with hard rinds or husks, whereas most birds, whose

beaks limit their capacity to break into or swallow large fruits, cannot (van der Pijl,

1982; Gautier-Hion et al., 1985). This variation in patterns of consumption of plant taxa

has been conceptualised in terms of taxonomic-based ‘dispersal syndromes’, which are

described by suites of fruit characteristics, including size, colour, pulp characteristics

3

and location on a plant, and suites of related frugivore characteristics such as their

perception of fruit colour or odour, digestive physiology and feeding behaviour (van der

Pijl, 1982; Bollen et al., 2004).

However, the broad categories of ‘bird’, ‘bat’ and ‘terrestrial mammal’ dispersal

syndromes obscure the sometimes substantial variation in patterns of plant species

consumption among faunal species within these categories (Willson et al., 1989; Stiles,

1993; Graham et al., 2002; Lord et al., 2002). For example, there is a maximum limit to

the size of fruit that a given frugivore species can handle which results from its body

mass and the size of its oral aperture (Herrera, 1981, 1984; Wheelwright, 1985; Mack,

1993). Consequently, the bird species in an assemblage may vary in substantially in

their capacity to disperse large fruited species because, although they may consume the

fleshy part of fruits piecemeal (Levey, 1987), only frugivore species with wide gapes or

large body mass are able to transport large seeds (Wheelwright, 1985; Silva and

Tabarelli, 2000; Lord et al., 2002).

Beyond the intractable constraint on the maximum size of fruits that a frugivore

species can handle, there is a lack of agreement regarding the factors that are important

in determining major variation in patterns of fruit consumption within frugivore

assemblages (Herrera, 1998, 2002; Levey and Martínez del Rio, 2001). However, the

few studies that have examined interactions among multiple frugivore and plant species

in rainforest (Pratt and Stiles, 1985; Hamann and Curio, 1999; Brown and Hopkins,

2002; Kitamura et al., 2002) have shown that there is additional, unexplained variation

among frugivore species in their patterns of plant consumption beyond that related to

fruit size. For example, Kitamura et al. (2002) considered patterns of consumption of

259 plant species by 25 frugivore species in north eastern Thailand and showed that

certain frugivore species did not consume fruits from certain plant species, despite their

size-related morphological capacity to handle them. Similarly, Pratt and Stiles (1985)

4

found that patterns of consumption of 20 plant species by 35 frugivorous bird species in

Papua New Guinea were related to the interaction between avian taxonomy and fruit

structure in addition to fruit size: capsular fruits were consumed predominantly by birds

of paradise (Paradisideae) whereas drupes and berries were mostly consumed by either

small passerines (which took small fruits) or pigeons and bowerbirds (large fruits).

Several factors other than fruit size potentially influence patterns of plant species

consumption by frugivore species. First, the chemical content of many fruits is

dominated by carbohydrate and water, whereas a small proportion of fruits contain high

levels of lipids or nutrients such as nitrogen (McKey, 1975; Izhaki and Safriel, 1989).

Highly frugivorous species may need to consume the fruits of particular nutrient-rich

plant species in order to obtain a complete diet from fruit (Izhaki and Safriel, 1989;

Bairlein, 1996). Therefore, it is logical to expect that a frugivore species’ level of

nutritional dependence on fruit may influence its patterns of plant species consumption

(Morton, 1973; McKey, 1975; Bairlein, 1996; Bosque and Calchi, 2003). For example,

highly frugivorous species may actively select fruits with high lipid content (McKey,

1975), or fruits with high levels of protein (White, 1993) or other essential minerals and

nutrients (Pulliam, 1975; Schaefer et al., 2003). In contrast, frugivores whose diets

include non-fruit items such as animals or seeds may obtain substantial amounts of

energy, minerals and nutrients from these sources (Izhaki and Safriel, 1989) and hence

be less selective of particular plant species.

A frugivore species’ patterns of plant species consumption may also be strongly

influenced by its digestive physiology. Variation among frugivore species in their

digestive physiology affects their capacity to assimilate certain forms of carbohydrate

(Martínez del Rio et al., 1988; Martínez del Rio and Karasov, 1990) or lipids (Cipollini

and Levey, 1997; Levey and Martínez del Rio, 2001). For example, frugivore species

that are unable to digest sucrose would be expected to consume few of the plant species

5

that produce sucrose-rich fruits (Martínez del Rio and Restrepo, 1993). Furthermore, a

frugivore species’ capacity to cope with secondary compounds is likely to have a strong

influence over the plant species that it consumes (Sun et al., 1997; Izhaki et al., 2002;

Levey and Martínez del Rio, 2001). Because both the occurrence of secondary

compounds in plants and an animal’s capacity to detoxify these compounds (at least in

herbivores) has a strong phylogenetic basis (Bernays and Chapman, 1994),

specialisation by frugivores on particular secondary compounds would be expected to

result in an association between the diets of phylogenetically-related frugivores and

phylogenetically-related plants.

Most discussions of the factors associated with variation in patterns of plant

species consumption by frugivores, other than those associated with fruit size, relate to

three different conceptual models: the lipid-carbohydrate dichotomy (McKey, 1975);

specialisation on core plant taxa (Fleming, 1986); or a null model (Burns, 2006).

The lipid-carbohydrate dichotomy

Several studies in the Neotropics have suggested an association between highly

frugivorous bird species and the consumption of plant species with lipid-rich fruits

(Snow BK, 1962; Snow DW, 1970, 1971; Howe and Primack, 1975; McKey, 1975;

Howe and Estabrook, 1977; Wheelwright, 1983). McKey (1975) proposed a model to

synthesise these findings within a coevolutionary framework, suggesting that a small

number of highly frugivorous species would consume ‘high quality’ fruits that have

lipid-rich pulp, and would preferentially disperse seeds to good germination sites,

whereas the larger group of opportunistic frugivores would consume ‘low quality’,

carbohydrate-rich fruits. The predictions of this model, as they relate to variation among

frugivore species in their patterns of plant consumption, are illustrated in Figure 1.1(a).

6

Empirical tests of the predictions of this model have advanced understanding of

frugivore-plant interactions, although they have shown little support for either a

dichotomous pattern of consumption based on lipid and carbohydrate content (e.g.,

Herrera, 1984; Fuentes, 1994; Corlett, 1996; Sun et al., 1997), or superior dispersal by

highly frugivorous bird species (Wheelwright and Orians, 1982). Although highly

frugivorous bird species may consume large proportions of lipid-rich fruits (Crome,

1975; Herrera, 1984; Stiles, 1993), they may also frequently consume fruits with

relatively low lipid content (Fuentes, 1994; Sun et al., 1997). Furthermore, species that

have mixed diets may also regularly consume lipid-rich fruits (Levey and Karasov,

1989; Howe, 1993; Martinez del Rio and Restrepo, 1993; Fuentes, 1994). It is likely

that patterns of plant species consumption by frugivorous species are influenced by their

need to balance intake of a variety of nutrients and minerals (Pulliam, 1975), or by

chemical compounds (Izhaki et al., 2002), not only by their energetic requirements.

Specialisation on ‘core plant taxa’

Fleming (1986) developed a model of plant consumption for frugivorous

phyllostomid bats, based on data collected in the Neotropics (Barro Colorado Island and

Costa Rica). This model described specialisation by particular bat species on certain

‘core plant taxa’, with the opportunistic addition of other plant species as their fruit

became available (Figure 1.1(b)). The core plant taxa that Fleming identified were

characterised by being available throughout the year; for one set of bat species (in the

Carollia and Sturnira genera) these plant taxa were ‘high quality’ fruits (Piper and

Solanum spp.) that occurred in low densities, while for bat species in the genus

Artibeus, the core taxon comprised high density, ‘low quality’ fruits (Ficus spp.). I am

not aware of any subsequent tests of the generality of this model for frugivorous bats

elsewhere, or for other frugivore taxa.

7

(a)

(b)

(c)

Figure 1.1 Conceptual representations of patterns of plant species consumption by

frugivorous bird species. The outer frames represent available plant species. Arrows

indicate the consumption of plant taxa by frugivores. Three alternative models are

represented: (a) the lipid-carbohydrate dichotomy proposed by McKey (1975) for

Neotropical birds; (b) the ‘core plant taxa’ model proposed by Fleming (1986) for

Neotropical bat genera; and (c) the neutral model proposed by Burns (2006) for

temperate birds.

Carollia, Sturnira

Artibeus

Piper spp. Solanum spp.

Ficus spp.

Remaining fruits

All fruits

All frugivores

Specialist frugivores

Generalist frugivores

Small, sugar rich fruits

Large, lipid-rich fruits

8

Null model of plant consumption

The frugivory literature has been dominated by ‘adaptive’ and ‘coevolutionary’

explanations of patterns of seed consumption and dispersal. Recently, Burns (2006)

proposed a null model in which fruit preferences did not differ among frugivore species,

but rather that frugivores consumed various fruits in proportion to their availability in

the environment. Burns (2006) found some support for this hypothesis amongst a small

number of bird and plant species (six and seven, respectively) in a northern hemisphere

temperate forest. While a null model is valuable for focussing attention on patterns that

can be explained by chance alone, many previous studies have reported strong

deterministic patterns in frugivore feeding behaviour. For example, in a 12-year study

of plant-frugivore interactions in Spanish scrubland, Herrera (1998) showed that plant

species were not consumed in proportion to their availability in the environment. Even

Burns (2006, p.430) concluded that “…deterministic processes are not entirely

unimportant in structuring pair-wise interactions between fruits and frugivores…” in his

study system. The applicability of a neutral hypothesis to patterns of plant consumption

by frugivore species in rainforest ecosystems has not been tested.

1.3 The role of seed dispersal in plant regeneration

Seed dispersal is one of several processes that determine the extent and patterns

of plant regeneration (Wang and Smith, 2002). For example, following dispersal, the

process of plant regeneration may be strongly influenced by seed predation, which in

turn is related to seed predator abundance (Forget, 1993; Wright et al., 2000; Wright

and Duber, 2001; Murray and Garcia, 2002; Babweteera et al., 2007). Nevertheless,

seed dispersal establishes the critical template for plant regeneration (Herrera, 1985;

Nathan and Muller-Landau, 2000; Levin et al., 2003), and makes an important

9

contribution to individual plant reproductive success, plant population dynamics, and

the ability of plant species to colonise new habitats (Howe and Smallwood, 1982).

Individual plant reproductive success

First, seed dispersal may increase the likelihood of successful reproduction by

an individual plant by removing its seeds from the region of highest per capita seed and

seedling mortality (Janzen, 1970; Connell, 1971; Howe and Smallwood, 1982; Harms et

al., 2000). This concept forms the basis of the ‘Janzen-Connell’ hypothesis, which

predicts that seed and/ or seedling mortality should be highest directly beneath parent

plants as a result of density-dependent factors such as sibling competition, and the

activity of fungal pathogens, seed predators and seedling herbivores (Janzen, 1970;

Connell, 1971). However, the benefits of escape (or consequences of not escaping)

depend on how these agents of mortality vary in relation to the position of the parent

tree and to seed and seedling density (Chapman and Chapman, 1995; Levin et al.,

2003). For example, seedlings of certain plant species may suffer very high mortality

beneath parent plants (Howe et al., 1985; Schupp, 1988; Chapman and Chapman, 1995),

whereas those of other plant species may not (Janzen and Martin, 1982; Chapman and

Chapman, 1995; Corlett and Turner, 1997; Baider and Florens, 2006). Nevertheless,

there is increasing evidence that density-dependent mortality is a pervasive factor in

structuring rainforest plant assemblages (Harms et al., 2000; Wright, 2002), and

therefore that localised seed dispersal is an important functional process in rainforest

dynamics (Terborgh et al., 2002).

Seed dispersal may also increase a plant’s reproductive success by delivering

seeds to ‘microsites’ that contain combinations of abiotic conditions (e.g., soil fertility,

moisture, light) and biotic factors (e.g., competitors, predators) that improve

germination, survival and growth (Grubb, 1977; Hubbell, 1979). These may be sites of

10

limited spatial extent that occur in particular topographic positions (e.g., along

watercourses) or that occur stochastically in dynamic forest systems (e.g., light gaps

caused by tree falls) (Schupp, 1993). Hence, the probability of a seed reaching a suitable

microsite and recruiting successfully is likely to increase with the number of seeds

dispersed, and the spatial extent and temporal period of dispersal (Hurtt and Pacala,

1995). In addition, the seeds of many rainforest plant species may persist for only a

short time in the seed bank (Hopkins and Graham, 1984; Alvarez-Bullya and Martínez-

Ramos, 1990). Ongoing dispersal would be required to maintain the chance that seeds

of these plant species were present when a recruitment opportunity arose (Chesson and

Warner, 1981; Muller-Landau et al., 2002).

Plant population dynamics

Seed dispersal affects the demographic characteristics and dynamics of plant

populations. For example, the size and rate of expansion of plant populations are

products of the reproductive success of individual plants, which depends on the

successful dispersal and establishment of propagules (Levin et al., 2003). Furthermore,

seed dispersal to suitable microsites is a critical factor in the recovery of plant

populations following localised extinctions, whether from stochastic environmental and

demographic causes or from human activities (Cochrane et al., 1999).

Patterns of seed dispersal within and among populations may also affect gene

flow and population genetic structure, which in turn may influence the susceptibility of

populations to disturbances (Hamilton, 1999; Jordano and Godoy, 2002).

Colonisation of new habitats

Seed dispersal is fundamental to plant colonisation of new habitats. In

fragmented forest landscapes, seed dispersal strongly influences patterns of plant

11

regeneration on cleared land (McDonnell and Stiles, 1983; Guevara et al., 1986; Silva et

al., 1996; Holl et al., 2000; Zimmerman et al., 2000; Hooper et al., 2004; Laurence,

2004; Franklin and Rey, 2007).

Dispersal over long distances to new habitats determines the biogeographical

distribution of plant species and the potential for species’ range expansions (Ridley,

1930; Levin et al., 2003). Long distance seed dispersal is likely to take on increasing

importance given the changing climatic conditions associated with global warming

(Primack and Miao, 1992; Matlack, 1995; Westoby and Burgman, 2006; Weir and

Corlett, 2007).

1.4 Consequences of rainforest clearing and fragmentation for

frugivores

The composition of frugivore assemblages may change as a consequence of

different species’ responses to forest clearing and fragmentation; throughout the world,

some species have shown sensitivity to forest fragmentation, whereas others are more

tolerant of forest fragmentation (Corlett, 1998; Silva and Tabarelli, 2000). Comparisons

of historical bird species lists with contemporary surveys have revealed that certain

frugivorous species are sensitive to forest fragmentation. For example, Castelletta et al.

(2000) reported that, within 20 years of widespread deforestation in Singapore, four of

the ten frugivorous bird species had become locally extinct. In different regions of the

Colombian Andes, Kattan et al. (1994) documented the local extinction over an 80 year

period of 36% (22 of 61 species) of frugivorous bird species, while Renjifo (1999)

reported that 40% of frugivorous bird species (17 of 42 species) had become extinct

following forest fragmentation. In the Brazilian Atlantic, Ribon et al. (2003) reported

that 10 frugivorous bird species had become extinct and a further 11 were threatened

12

(i.e., approximately 66% of a total of 32 frugivorous bird species) following extensive

forest clearing.

Other than these historical studies, research into the effects of forest

fragmentation on frugivore species has generally involved comparisons of frugivore

assemblages between continuous and fragmented forest, or evaluation of the effects of

fragment size and isolation. I consider these in turn below.

Frugivore assemblage change in forest fragments compared with continuous forest

Two studies have compared frugivore species’ responses to fragmentation using

systematic pre-fragmentation and post-fragmentation surveys. Working in the

experimentally fragmented forests of the Biodynamics of Forest Fragmentation Project

in Brazil (Bierregaard et al., 1992), Bierregaard and Stouffer (1997) compared average

rates of capture of the 12 frugivorous bird species that were most common pre-clearing

with their capture rates 2-3 years after the forest had been fragmented into 1 ha and 10

ha patches. Capture rates of these species declined significantly from 35 individuals/

1000 mist-net hours before clearing to approximately 20 individuals / 1000 net hours.

However, nine additional frugivorous bird species were recorded only after forest

fragmentation. Cosson et al. (1999) compared the abundance of 14 frugivorous bat

species in an area of forest in French Guiana before and after its fragmentation by

flooding of the surrounding landscape to create a dam. Six bat species were not

observed in any forest fragments following flooding, and the average abundance of

seven of the eight remaining frugivorous bat species was lower in fragments (size range

5 - 40 ha) than in the mainland control site (0 – 65% of their abundance in the control

site).

Several studies have compared frugivore assemblages in forest fragments and

continuous forest ‘reference’ sites. In subtropical Australia, Date et al. (1996) surveyed

13

the incidence of nine frugivorous pigeon species in ten rainforest fragments (size range

1 ha to 80 ha) and 15 rainforest sites contiguous with large tracts of forest. Four of the

pigeon species occurred more frequently in continuous than fragmented sites, five

species were recorded in similar frequency between these two site types and one species

was more common in fragments. In Uganda, the average number of frugivore species

(birds and monkeys) in a large tract of forest (8 500 ha in size) was 1.14 times the

number of species in fragments (size range 130 ha – 1 400 ha), although this difference

was not statistically significant (Farwig et al., 2006).

Other workers have compared the number of frugivore species visiting a focal

tree species between continuous forest and rainforest fragments. For example, Graham

et al. (2002) compared frugivorous bird assemblages at Dendropanax arboreus

(Araliaceae) and Bursera simaruba (Burseraceae) between fragments (mean 4.1 ha in

size) and a large forest tract (650 ha) in Mexico. While the average numbers of bird

species, visits to focal trees and fruits consumed were similar for both tree species

between habitats, the species composition of frugivorous birds feeding at D. arboreus

varied between continuous and fragmented forest, largely because two of the bird

species from continuous forest did not visit trees in fragments. In the Atlantic forest of

Brazil, Pizo (1997) reported 35 bird species visiting fruiting Cabralea canjerana

(Meliaceae) trees in an extensive forest tract (49 000 ha) compared with 14 frugivorous

bird species at the same tree species in a 250 ha rainforest remnant. The lower number

of frugivorous bird species in the 250 ha remnant may have been a consequence of its

reduced size and isolation, although the lower sampling effort in the smaller fragment

(45 hours of observation compared with 70 in the large forest tract) may also have

contributed to this result. In Tanzania, five of the ten frugivorous bird species recorded

in fruiting Leptonychia usambarensis (Sterculiaceae) in continuous forest (7 500 ha in

size) were not recorded at trees of this species in three small fragments (2, 13 and 31 ha

14

in size), and mean visitation rates of two additional bird species were at least 75% lower

in fragments than in continuous forest (Cordeiro and Howe, 2003). Although a higher

number of individual trees were observed in continuous forest than in fragments (16

compared with 10) in this study, and this may have contributed to the difference in

species’ totals, it should not have biased the data on average visitation rates per tree

(Cordeiro and Howe, 2003).

In summary, there is some evidence of reduced total frugivore species richness

associated with forest fragmentation (Cordeiro and Howe, 2003; Farwig et al., 2006).

Studies that have evaluated the responses of individual species have reported declined

abundance of one suite of frugivore species, maintained abundance of another group of

species and, in some cases, increased numbers of a further suite of species (Date et al.,

1996; Bierregaard and Stouffer, 1997; Cosson et al., 1999).

The effect of fragment size on frugivore assemblages

Cordeiro and Howe (2001) conducted transect surveys in five forest patches in

Tanzania that varied in size from 0.5 ha to 3 500 ha. They detected the lowest numbers

of frugivorous bird and primate species in the three smallest fragments (0.5, 9 and 30

ha) but similar species’ numbers between the 521 and 3 500 ha sites. The lower

numbers of species detected in the smaller fragments may have been partly due to the

lower survey effort in these habitats. Şekercioğlu et al. (2002) reported similar numbers

of frugivorous bird species in a large (>200 ha) remnant and in small (approx. 5 ha)

rainforest remnants in Costa Rica. Similarly, in French Guiana, Cosson et al. (1999)

showed that three years after fragmentation, the patterns of reduced abundance of

frugivorous bat species were similar between small (<5 ha) islands and a larger (40 ha)

forest island. Date et al. (1996) reported no association between the abundance of

frugivorous pigeon species and fragment size (with size ranging from 1 to 80 ha), even

15

for species that were less abundant in fragments than continuous forest overall (e.g.,

Ptilinopid fruit-dove species). In Brazil, Bierregaard and Stouffer (1997) reported that

capture rates of only two of the six bird species tested varied between 1 ha and 10 ha

fragments. In both cases, bird species’ abundances were significantly higher in one

hectare than ten hectare fragments. The abundance of other species showed the opposite

pattern, but data were not significant in statistical comparisons.

In summary, most studies have tended to show only a limited effect of fragment

size on the abundance of frugivore species (Cosson et al., 1990; Date et al., 1996;

Şekercioğlu et al., 2002).

The effect of isolation on frugivore assemblages

In Costa Rica, Luck and Daily (2003) reported that the average number of

frugivorous bird species declined from 21.5 at Micona spp. (Melastomaceae) trees that

were located within 2 km of a large rainforest remnant in a low intensity agricultural

matrix, to 14.1 at trees located 5-8 km from forest in areas of high agricultural intensity.

In subtropical Australia, Green (1993) compared visitation by frugivorous bird species

at two species of fig (Ficus platypoda and F. superba), Ehretia acuminata

(Boraginaceae) and Diploglottis australis (Sapindaceae) in more-forested upland areas

and less-forested valleys. This study found that fewer frugivorous bird species visited

the fig trees in the valleys than in the mountain areas, whereas similar numbers of bird

species were recorded at the other two plant species. In Kenya, Eshiamwata et al. (2006)

reported a similar species richness of frugivorous birds at Ficus thonningii located

within 200 m of forest compared with those over 1 km from forest, although the

landscape they worked in may have contained a large amount of forest habitat.

In summary, lower numbers of frugivorous species have been reported visiting

certain fruiting plant species in matrix habitats compared with relatively well-forested

16

areas (Green, 1993; Luck and Daily, 2003), however, there may be variation between

regions or plant species.

1.5 Relationships between frugivore species’ traits and their sensitivity

to rainforest fragmentation

Studies of frugivore species’ responses to forest fragmentation have shown that

certain frugivore species are sensitive to forest fragmentation, whereas other frugivore

species appeared to be relatively tolerant of, or even advantaged by, these changes (see

Section 1.4). Variation among species in their sensitivity to rainforest fragmentation

may be due to differences in behavioural, ecological or demographic attributes (Lovejoy

et al., 1986; Laurance, 1990; Stouffer and Bierregaard, 1995; Turner, 1996; Sieving and

Karr, 1997; Warburton, 1997; Corlett, 1998). Henle et al. (2004) reviewed empirical

and theoretical evidence for the association of different plant and animal species’

attributes with their sensitivity to forest fragmentation. These authors identified certain

aspects of demography (particularly population size and variability), and ecological

traits (patterns of microhabitat and matrix use, rarity and biogeographical distribution)

as being the most consistently related to differing fragmentation responses among

species. Studies of the association between frugivore traits and their responses to forest

fragmentation have focussed mainly on the effects of dispersal ability, degree of

resources specialisation and body size. Among the studies evaluated by Henle et al.

(2004), several factors, including dispersal power, body size, and ecological

specialisation had inconsistent associations with species’ fragmentation sensitivity.

Below, I review the findings of studies relating frugivore species’ attributes to their

fragmentation responses.

17

Ability to disperse through the matrix

A species’ abundance in fragmented forest landscapes depends partly on its

ability to disperse through matrix habitats (Wiens, 1994; Bierregard et al., 1992;

Warburton, 1997; Graham, 2001; Şekercioğlu et al., 2002). This ability would affect a

species’ capacity to recolonise fragments after localised extinctions and to use networks

of patches to satisfy resource requirements.

The natural dispersal ability of volant (flying) taxa is typically greater than that

of terrestrial taxa. However, not all birds (Stouffer and Bierregaard, 1995) or bats

(Cosson et al., 1999) readily disperse through fragmented parts of the landscape. In

practice, a species’ dispersal potential may be limited by resource availability, relative

to cost. For example, Graham (2001) showed that although the keel-billed toucan

Ramphastos sulphuratus did fly among rainforest fragments in Mexico, its movements

were limited to areas of the landscape that contained a minimum threshold amount of

forest and fruit resources. This was interpreted as being a result of this species’ need to

balance the cost of moving a certain distance with the energy gained from available

resources (Graham, 2001).

Dispersal ability may also be related to a species’ scale of movement. For

example, it has been proposed that migratory and nomadic species may have greater

dispersal power than sedentary species and hence have a greater capacity to move

through the modified matrix (reviewed in Henle et al., 2004). However, it has

conversely been reasoned that sedentary species may be more likely to have smaller

area requirements and hence be more capable of persisting in isolated fragments than

species with large area needs (Henle et al., 2004). For example, nomadic frugivore

species may move over large areas to find ripe fruit that is spatially and temporally

patchy (Leighton and Leighton, 1983; Innis, 1989). Forest fragmentation may reduce

18

the capacity of these frugivore species to move among key fruit resources (Karr, 1976;

Leighton and Leighton, 1983; Terborgh, 1986; Wheelwright, 1986; Laurance and

Yensen, 1991). However, different frugivore species’ sensitivity to fragmentation has

not been specifically correlated with variation in their movement patterns.

Degree of specialisation on resources

A species’ ability to traverse the matrix is not only associated with their capacity

or willingness to move, but also with their use of matrix elements, such as isolated trees,

copses of regrowth, windbreaks and agricultural crops (Estrada et al., 1993; Crome et

al., 1994; Graham, 2001). Species with specialised patterns of forest resource use are

arguably less likely to use habitat elements within the cleared matrix, and hence more

likely to be adversely affected by fragmentation, than species with more generalised

habitat requirements (Willis, 1974; Karr, 1976; Leck, 1979; Andrén, 1994; Christiansen

and Pitter, 1994; Turner, 1996; Warburton, 1997; Gascon et al., 1999; Sigel et al.,

2006). For example, in a tropical rainforest landscape in Australia, frugivorous bird

species that were dependent on rainforest were less likely to use matrix resources than

species that used more open forest or a variety of forest types (Crome et al., 1994).

Studies conducted in the Neotropics (Christiansen and Pitter, 1997) and south east Asia

(Castelletta et al., 2000) have shown that frugivorous bird species that specialised on

fruit were disproportionately sensitive to rainforest fragmentation. In contrast, species

with diets that comprised more than one food type tended to be more resilient. In a

study of natural fragments of monsoon rainforest in northern Australia, Price et al.

(1999) found that the use of rainforest patches by specialist frugivorous bird species was

strongly affected by the cumulative amount of rainforest within a landscape, but that

this did not clearly affect bird species that had the ability to switch from fruit to

invertebrates or other dietary items.

19

Body size

Many studies have proposed that large body size may be associated with

frugivore declines in fragmented forest (Kattan et al., 1994; Corlett, 1998, 2002;

Restrepo et al., 1997; Renjifo, 1999; Castelletta et al., 2000; McConkey and Drake,

2002). The distribution of large-bodied species in fragmented forest landscapes may be

restricted as a result of their large area requirements (Leck, 1979; Pimm et al., 1988;

Turner, 1996; Sieving and Karr, 1997; Sodhi et al., 2004). Furthermore, increased

hunting pressure in fragmented forest may disproportionately affect large-bodied

species (Corlett, 2002; Sodhi et al., 2004; Terborgh and Nuñez-Iturri, 2006), especially

large-bodied frugivores (Brash, 1987).

Restrepo et al. (1997) examined changes in the proportional distributions of

body mass of frugivorous bird assemblages along a gradient from forest remnant to

pasture in Colombia. Their results showed that larger-bodied species were consistently

lost from avian frugivore assemblages in more disturbed situations, although small-

bodied species were also lost from assemblages in one of the four landscapes surveyed.

However, Daily and Ehrich (1994) and Luck and Daily (2003) reported greater

persistence of large-bodied than small-bodied avian frugivore species in agricultural

landscapes in Costa Rica. This result was interpreted as a consequence of the superior

position of larger birds in the foraging dominance hierarchy in this region (Daily and

Ehrlich, 1994). Similarly, Cosson et al. (1999) reported a clear positive relationship

between the body size of bat species and their abundance in rainforest fragments in

French Guiana.

20

1.6 Consequences of changes in the composition of frugivore

assemblages for seed dispersal and patterns of plant regeneration

This section develops a framework for the study of the consequences of forest

fragmentation for frugivores, and the secondary consequences for seed dispersal and

plant regeneration. There is variation among frugivore species in the plant species that

they disperse (Section 1.2) and also in their responses to forest fragmentation (Section

1.4). Consequently, it would be expected that forest fragmentation would result in

changes in the dispersal of frugivore-dispersed plant species, and that this in turn would

be likely to affect patterns of plant regeneration (Section 1.3). This logic has been used

to predict changes in seed dispersal and plant regeneration as a consequence of changes

in the abundance of frugivore species in fragmented forest (e.g., Restrepo et al., 1997).

However, because of limited understanding of the specific roles of frugivore species in

seed dispersal, the predicted changes have often been vague. Furthermore, there has

been limited consideration of the potential for different spatial dimensions of seed

dispersal (See Section 1.3) to be differentially affected by changes in the composition of

frugivore assemblages.

Furthermore, for regenerating plants, the different processes of escape from

density dependent mortality, recolonisation of microhabitats and colonisation of new

habitats (described in Section 1.3) occur at different spatial scales. In Figure 1.2 and

Table 1.1, these are described as different seed dispersal trajectories for a given plant or

plant species in fragmented forest landscapes. These seed dispersal trajectories can be

used as a basis for systematically considering potential changes in qualitative aspects of

the dispersal of different plant species that may result from changed composition of

frugivore assemblages in fragmented forest. For example, variation among frugivore

species in their patterns of movement may create different spatial patterns of seed

deposition. First, dispersal along trajectory b (Figure 1.2) would be affected by

21

differences at the scale of patterns of microhabitat use by frugivore species (Reid, 1989;

Schupp, 1993; Wenny and Levey, 1998; Alcántara et al., 2000; Loiselle and Blake,

2002). Second, differences among frugivore species in their patterns of movement

among fragments (e.g., Tewksbury et al., 2002) and into secondary regrowth (e.g., Silva

et al., 1996) would affect dispersal along trajectories c, d and f. Finally, there is also

variation among frugivore species in their propensity to move over large areas across

the landscape (Holbrook et al., 2002; Dennis and Westcott, 2006), and hence to disperse

seeds along trajectory e.

Table 1.1 Description of the potential trajectories of seed dispersal in fragmented forest

landscapes (Figure 1.2) and their relationship to different aspects of the process of

seed dispersal and plant regeneration.

Trajectory Description of seed movement path1 Processes affected a beyond the crown of the parent plant escape from density-dependent mortality b

relatively short distance to regeneration microsites within remnant

recolonisation of microsites

c

moderate distance across non-forest matrix between fragments

recolonisation following local extinction

d

moderate distance into non-forest matrix

colonisation of secondary regeneration

e

long distance across non-forest matrix

biogeographical distribution and range expansion

f

moderate distance from non-forest matrix into remnant

recolonisation of microsites/ colonisation of new habitat (e.g., introduced plant taxa)

g

moderate distance around non-forest matrix

recolonisation of microsites/ colonisation of new habitat

1 relative distances involved in each trajectory refer to different scales of movement; ‘short’ is tens to a hundred metres; ‘moderate’ is hundreds of metres to a kilometre; ‘long’ is in order of kilometres.

22

Figure 1.2 Potential seed dispersal trajectories in fragmented forest landscapes with

respect to plant regeneration. Forest fragments are shown in grey and the surrounding

non-forest matrix is white. A focal plant individual is represented as a diamond. Arrows

show paths of seed movement. Each trajectory is related to different aspects of the

seed dispersal process in fragmented forest landscapes (Table 1.1). Trajectories (a) –

(e) represent potential dispersal trajectories of a focal plant in a forest patch in relation

to the following processes: escape from density-dependent mortality (a); recolonisation

of regeneration microsites within a patch (b); recolonisation following local extinction in

another forest patch (c); colonisation of new habitats in the non-forest matrix (d); and

range expansion via colonisation over long distances (e). Trajectories (f)

(re)colonisation of forest fragment from the non-forest matrix, and (g) (re)colonisation of

new habitats in the non-forest matrix from the non-forest matrix, represent potential

dispersal trajectories of plants in the non-forest matrix that may affect patterns of plant

regeneration in fragments and the non-forest matrix. See Section 1.3 for further

description.

Dispersal failure: potential consequences of the loss of disperser species for plant

regeneration

The loss of all of the dispersers of a given plant species would result in dispersal

failure for the plant species (e.g., Temple, 1977; Silva and Tabarelli, 2000; Terborgh

and Nuñez-Iturri, 2006; Babweteera et al., 2007). Under this scenario, there would be no

a

c

b

d e

g

f

23

dispersal along any of the trajectories shown in Figure 1.2. Dispersal failure, if

combined with recruitment failure beneath parent plants, would eventually lead to a

plant species’ extinction (Temple, 1977; Janzen and Vasquez-Yanez, 1991). However,

since seedlings of many plant species may be able to recruit beneath parent plants

(Section 1.3), dispersal failure may not reduce reproduction to zero. Nevertheless,

dispersal failure is likely to reduce plant reproductive success and lead to population

decline over the longer term (Levin et al., 2003). For example, in Uganda, the tree

Balanites wilsoniana can only be dispersed by African elephants Loxodonta africana

because of the very large size of its fruit (Babweteera et al., 2007). While seedlings of

B. wilsoniana recruited in forest fragments without elephants, the survival of these

undispersed juveniles was substantially lower than that of juveniles that established

away from the parent. Therefore, it would be expected that B. wilsoniana would have

higher reproductive success in the forest where elephants were present (Babweteera et

al., 2007). Other studies have also shown higher germination rates in dispersed than

undispersed seeds (Asquith et al., 1999) and higher growth and survival of juvenile

plants that have germinated beyond the crown of conspecific plants (Hubbell and

Foster, 1990; Bleher and Böhning-Gaese, 2001).

In addition to reducing per capita reproductive success, dispersal failure of a

plant species would eliminate its ability to colonise microsites, either within a fragment

(Orrock et al., 2006; Figure 1.2, trajectory b), or between fragments (Poschlod et al.,

1996; McEuen and Curran, 2004; Figure 1.2, trajectory c). Consequently, the species

would be unable to recolonise following localised extinctions, and its distribution would

become more clumped. The population would consequently be more susceptible to local

extinction if stochastic disturbances affected all individuals in the spatially-constrained

population (Fahrig and Merriam, 1994; Cochrane et al., 1999). Furthermore, plant

species that lacked dispersal would be unable to colonise new habitats, such as

24

regenerating vegetation (Figure 1.2, trajectory d). Finally, the failed dispersal of a plant

species would mean it could not migrate over large distances. This may compromise the

survival of that plant species in the longer term, for example if its existing range became

climatically unsuitable as a result of changed global conditions (Primack and Miao,

1992; Westoby and Burgman, 2006; Weir and Corlett, 2007; Figure 1.2, trajectory e).

Potential consequences of reduced frugivore species richness or abundance for seed

dispersal and plant regeneration

The majority of rainforest plant species are likely to be dispersed by multiple

frugivore species (Wheelwright and Orians, 1982; Moermond and Denslow, 1985;

Bronstein and Hoffman, 1987). Consequently, the loss of all disperser species may be

unlikely for most plant species. In most studies, lower numbers of disperser species

and/or individuals have been reported, rather than the complete absence of dispersers

(e.g., Howe and Cordeiro, 2003; see Section 1.4).

Logically, reduced numbers of frugivore species may be associated with lower

rates of visitation and fruit removal. This has been shown empirically in Tanzania

(Cordeiro and Howe, 2003), Madagascar (Bleher and Böhning-Gaese 2001, 2006) and

Brazil (Pizo, 1997). However, in Costa Rica, Luck and Daily (2003) reported

substantially reduced frugivore species richness, but no change in rates of visitation to

Micona spp. (Melastomaceae). In Kenya, Farwig et al. (2006) reported slightly declined

species richness of frugivores at fruiting Prunus africana (Rosaceae) in forest fragments

compared with a large forest tract, but a concomitant increase in visitation and seed

removal. Therefore, the number of frugivore species visiting a plant may not be directly

related to the rate of dispersal of that plant species. Factors such as changed competitive

interactions (e.g., Willson and Crome, 1989), and density or behavioural compensation

(Loiselle and Blake, 2002) may interact with changes in the composition of the

25

frugivore assemblage to influence seed removal rates in fragmented forest landscapes.

In addition, there is variation among frugivore species in the quantity of seeds that they

disperse (Graham et al., 2002; Cordeiro and Howe, 2003), as well as the temporal

period over which they disperse seeds (Greenberg et al., 1995). Furthermore, there may

be variation among frugivore species in the proportion of seeds that they disperse to

suitable germination microhabitats (e.g, Reid, 1989; Murray et al., 1993; Wenny and

Levey, 1998; Aukema and Martínez del Rio, 2002).

Consequently, the reduced abundance or loss of different frugivore species may

have different impacts on the quantity and quality of seed dispersal. Therefore, the

consequences for seed dispersal may be difficult to predict based on information about

species richness or overall frugivore abundance. However, more detailed consequences

for seed dispersal and plant regeneration of changes in the species composition or

relative abundance of individual frugivore species may be predictable if information

about frugivore species composition is combined with an understanding of functional

variation among species and interpreted in the framework shown in Figure 1.2.

Limited knowledge regarding the disperser assemblage of most plant species

constrains the capacity to predict changes in seed dispersal following changes in the

frugivore assemblage. An exception may be large-fruited plant species; dispersal failure

may be predicted from knowledge of the loss of frugivore species if all of the species

with the morphological capacity to disperse large fruits have gone extinct, because

small frugivores are unable to disperse large fruits (Herrera, 1984; Moermond and

Denslow, 1985; Wheelwright, 1985). Because large frugivores have declined in

fragmented forest in many parts of the world (see Section 1.5), it has been predicted that

dispersal of large-fruited plant species will consequently be reduced or fail (Corlett,

1996, 1998; Corlett and Turner, 1997; Silva and Tabarelli, 2000; McConkey and Drake,

2002; Kitamura et al., 2005). In Uganda, Chapman and Onderdonk (1998) found that

26

the abundance of seedlings, especially of large-seeded plant species, declined in

fragments with reduced abundance of primates, compared with extensive forest.

1 .7 Aims and structure of this thesis

The aim of this thesis is to investigate changes in the frugivorous vertebrate

assemblage as a consequence of rainforest fragmentation in the moist subtropics of

Australia, and to assess the potential for subsequent changes in seed dispersal. This

broad aim is addressed first by investigating the effects of fragmentation on the

frugivore species within a complete regional assemblage, and then by assessing the

potential roles of the different frugivore species in seed dispersal through analyses of

their morphology, behaviour and patterns of consumption of plant species. Finally, this

information is synthesised to predict the consequences of fragmentation for seed

dispersal by frugivores.

In his review of the biological effects of rainforest fragmentation, Turner (1996)

recommended three key research directions to advance ecological understanding of the

consequences of rainforest fragmentation: (1) study in older fragments, (2) the

identification of susceptible groups of taxa, and (3) the assessment of higher order

effects, including seed dispersal. Rainforest landscapes in subtropical Australia present

an opportunity to undertake study of all three research areas. First, forests in this region

have been fragmented for 70-150 years, sufficient time for assemblages to undergo

some degree of ‘relaxation’ (Brooks et al., 1999). Second, for reasons detailed below,

the vertebrate frugivore assemblage in subtropical Australia may be well suited to

identifying variation among species in their responses to fragmentation and functional

roles. Third, this approach may contribute to the development of a predictive

understanding of the secondary consequences of rainforest fragmentation for seed

dispersal.

27

Compared with many other regions of the world, the frugivore assemblage in

Australia is relatively simple (Crome, 1978; Dennis, 1997; Corlett and Primack, 2006).

The dominant frugivores are birds and bats (Green, 1993, 1995). There are no primates

or other non-volant frugivorous mammals as in other regions (e.g., Corlett, 1998).

In addition to its relative simplicity, there is a substantial amount of information

on the consumption of fleshy fruited plants by frugivore species in subtropical Australia

(e.g., Innis, 1989; Green, 1995; Recher et al., 1995; Church, 1997), and dietary

information has been partly compiled for each species in the Handbook of Australian,

New Zealand and Antarctic Birds (HANZAB) series (Marchant & Higgins, 1993;

Higgins & Davies, 1996; Higgins, 1999; Higgins et al., 2001), although it has not been

synthesised across any regional bird assemblage.

Furthermore, there is a sufficient number of species comprising the frugivore

assemblage in subtropical Australia to detect strong patterns of variation among species,

if they exist. Many previous community-wide studies of the of patterns of plant species

consumption by frugivore species have been conducted in ecosystems with few

frugivorous species, such as Mediterranean scrublands (18 bird species; Herrera

(1984)), littoral forest in Madagascar (6 bird species and 7 mammal species; Bollen et

al. (2004)) and temperate rainforest in Canada (6 bird species; Burns (2006)). The small

numbers of frugivore species in these studies may have made it difficult to detect

statistically significant variation among species. Based on the number of frugivorous

bird species recorded at fruiting trees, there are at least 32 frugivorous bird species in

subtropical Australia (Green, 1993).

Specifically, this thesis addresses three sets of questions relating to:

1. the distribution and abundance of frugivorous bird and bat species in

fragmented forest relative to extensive rainforest in a specific study region

(the Sunshine Coast) of subtropical Australia;

28

2. variation among these frugivore species in their seed dispersal potential

(assessed using degree of frugivory, capacity for ingesting large seeds, and

other attributes), and their patterns of consumption of plant species and types

of fruits; and

3. the extent to which the seed dispersal potential of rainforest plant species is

likely to change as a consequence of changes in the frugivorous vertebrate

community in fragmented rainforest.

Figure 1.3 summarises the structure and conceptual links among the subsequent

chapters of this thesis.

In Chapter Two, the specific composition of the frugivorous bird assemblage in

the fragmented subtropical rainforest landscape of the Sunshine Coast, Australia is

identified. This chapter also presents the results of field surveys aimed at assessing

whether the abundance of frugivorous bird species is affected by forest fragmentation,

using replicate sites of extensive, remnant and regrowth rainforest.

In Chapter Three, functional traits of frugivorous bird species that may

influence their role as seed dispersers are assessed for the frugivorous bird assemblage.

Specifically, bird species’ gape width, degree of frugivory and seed treatment are

analysed in relation to their responses to fragmentation. Information about the response

of frugivorous bird species in extensive versus fragmented forest (Chapter Two) is used

to assess the possibility of reduced dispersal potential of rainforest plant species in

fragmented rainforest.

In Chapter Four, data on plant species consumption by frugivorous bird species

are compiled from published literature and field records. Tests of association are

conducted between the frugivore traits that were used in functional analyses conducted

in Chapter Three, and frugivore species’ patterns of plant species consumption.

29

In Chapter Five, patterns of plant species consumption by frugivorous bird

species are assessed using the same data as in Chapter Four in relation to the potential

for reduced dispersal of certain plant species as a result of declined abundance of

particular bird species in fragmented rainforest.

In Chapter Six, the species composition and responses to forest fragmentation

of the frugivorous bat assemblage is identified for the same site network as the bird

assemblage considered in Chapter Two. Information on patterns of plant species

consumption by these bats is used to assess their potential to disperse similar plant

species to frugivorous birds, particularly those bird species that decline in fragmented

forest.

Chapter Seven provides a synthesis of the findings of the previous chapters in

relation to understanding the functional roles of frugivore species in seed dispersal and

predicting consequences of rainforest fragmentation for seed dispersal. This chapter

makes specific predictions regarding seed dispersal and plant regeneration in

fragmented rainforests of the study region and considers the implications for

conservation.

30

C

hap

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in fr

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Ch

apte

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The

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fr

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Sur

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Red

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for

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C

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Fig

ure

1.3

Con

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ual l

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bet

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f th

is t

hesi

s.

31

1.8 Rainforest fragmentation, frugivores and seed dispersal in

Australia

There are three major areas of rainforest along the east coast of Australia. These are the

tropical rainforests of north Queensland (approximately 15ºS - 19ºS), the subtropical

rainforests of southern Queensland and northern New South Wales (26ºS - 30ºS), and

the cooler temperate rainforests of Tasmania (40 - 44ºS) (Webb and Tracey, 1981).

Smaller patches of rainforest (including ‘dry rainforests’) occur across coastal and sub-

coastal areas of northern and eastern Australia (Webb and Tracey, 1981; Bowman,

2000).

Australian rainforests are relicts of ancient rainforests that formerly covered

extensive areas of the continent (Kershaw et al., 1991). Cool and dry climatic conditions

during the late Tertiary, and especially during the Pleistocene, resulted in the retraction

of rainforest to moist and protected refugial areas (Webb and Tracey, 1981; Adam,

1992; Goosem, 2000). During this period, much of the rainforest in Australia was

replaced by open forests, woodland, savanna and grasslands, which were better suited to

the changed climatic conditions and associated increase in fire (Martin, 1990; Kershaw

et al., 1991). There has been some minor re-expansion of rainforest over the last few

thousand years, although the distribution of rainforest remains disjunct, reflecting the

“archipelago of refugia” that were available during former climatic regimes (Webb and

Tracey, 1981: 609). The current distribution of rainforest in Australia is shown in the

National Land and Water Resources Audit (NLWRA) (2001).

Formerly, large tracts of continuous subtropical rainforest (tens of thousands of

hectares) were associated with fertile soil on basalt lava flows on plateaux (e.g., the

Lamington and Maleny plateaux in southern Queensland, and the ‘Big Scrub’ of

northern New South Wales). Rainforest also occurs in areas of less fertile soils. In the

Australian subtropics, rainforests on poor soil are restricted to areas that receive high

32

rainfall, are locally nutrient-enriched and moist (e.g., along watercourses), or are

associated with topographic features that provide protection from fire (e.g., gullies)

(Webb and Tracey, 1981). Patches of subtropical rainforest in these situations are

typically surrounded by more extensive, drier and fire-prone forest types (often

dominated by dry-fruited Eucalyptus and related tree genera).

Large areas of subtropical rainforest have been cleared in Australia (Webb and

Tracey, 1981). Most of the clearing in these rainforest landscapes was for agriculture

and occurred from the mid 1800s (Young and McDonald, 1987; Watson, 1989;

Frawley, 1991; Catterall and Kingston, 1993). The pre-European rainforest cover across

the continent was estimated to have been four million ha; it has been estimated that

approximately three-quarters of this remains (NLWRA, 2001). Subtropical rainforests

have been heavily cleared from basalt plateaux, in the lowlands and along watercourses

(Catterall and Kingston, 1993). For example, less than 1% of the original rainforest

cover remains of the Big Scrub, formerly the most extensive patch of lowland

subtropical rainforest in Australia (Frith, 1952, 1976; Floyd, 1990). Large forest tracts

are now mostly restricted to upland areas (Webb and Tracey, 1981; Catterall and

Kingston, 1993; Date et al., 1996).

Contemporary rainforest landscapes in Australia resemble those in many other

regions of the world in comprising a mosaic of remnant forest patches, grazed land,

agricultural cropland, tree crops, regrowth and suburban development (e.g., Guevara

and Laborde, 1993; Benítez-Malvido and Martínez-Ramos, 2003). An important point

of difference is that there is no shifting agriculture in Australia, whereas this is a feature

of rainforests in some parts of Asia (e.g., Lawrence, 2004) and South America

(Tabarelli and Peres, 2002).

There is a lack of knowledge regarding ecological processes in fragmented

rainforest landscapes in the Australian subtropics, including the dynamics of plant

33

regeneration (Adam, 1992; Green, 1995; Gilmore 1999; Hunter 1999). As a

consequence, the long-term conservation values of the region’s remnant rainforests may

be compromised, for example if regeneration trajectories are truncated by a lack of

dispersal of certain plant taxa. This thesis provides new information relating to these

issues.

34

Chapter Two

Changes in the avian frugivore assemblage in fragmented rainforest

compared with extensive forest in subtropical Australia

2.1 Introduction

Populations of many frugivorous bird species have declined following the

fragmentation of tropical rainforests (Kattan et al. 1994; Date et al., 1996; Bierregaard

and Stouffer, 1997; Pizo, 1997; Corlett, 1998; Renjifo, 1999; Castelletta et al., 2000;

Silva and Tabarelli 2000; Cordeiro and Howe, 2001, 2003; Ribon et al., 2003). It has

been suggested that some frugivorous bird species from subtropical Australia may also

be sensitive to rainforest fragmentation (Frith, 1952; Date et al., 1991; Date et al., 1996;

Price et al., 1999). Furthermore, it has been suggested that certain frugivorous bird

species may migrate seasonally between upland and lowland areas in response to

altitudinal differences in fruit availability (Innis, 1989; Date et al., 1991). Because

rainforests have been heavily cleared in the lowlands of subtropical Australia (Catterall

et al., 1997), seasonal dependence on these areas may limit populations of these

frugivorous bird species (Date et al., 1991). However, species’ responses to forest

fragmentation in subtropical Australia have not been assessed across the avian frugivore

assemblage.

Understanding the use of fragmented forests by birds in the context of extensive

and ongoing rainforest clearing may help develop management strategies appropriate

for avian conservation (Saunders et al., 1991; Sodhi et al., 2004). Furthermore,

frugivores disperse the seeds of a large proportion of rainforest plant species (Willson et

al., 1989; Butler, 2003). Consequently, changed numbers of frugivores in fragmented

rainforest may result in changed patterns of plant regeneration (Janzen and Vasquez-

Yanez, 1991; Harrington et al., 1997; Restrepo et al., 1997; Corlett, 1998; Silva and

35

Tabarelli, 2000). For example, the decline of particular frugivore species in fragmented

landscapes may mean that certain plant species have lower dispersal potential in these

areas. The declined abundance of a suite of frugivorous bird species in small forest

fragments in Tanzania has been associated with reduced seed dispersal, lower levels of

recruitment, and clumped spatial patterns of recruitment of certain plant species

(Cordeiro and Howe, 2001, 2003). In particular, large fruited plant species may be

especially susceptible to reduced dispersal in fragmented landscapes because of the

decline of large bodied frugivores (Corlett, 1996, 1998; Harrington et al., 1997; Silva

and Tabarelli, 2000; Kitamura et al., 2002; McConkey and Drake, 2002; Meehan et al.,

2002).

In this chapter, frugivorous bird species’ abundances are assessed in fragmented

rainforest in a subtropical Australian landscape. Specifically, differences in the

abundance of frugivorous bird species between large tracts of forest, rainforest remnants

and patches of rainforest regrowth are quantified. It is expected that the abundance of

certain species may be lower in remnants and regrowth than in extensive forest, while

that of other species may be higher. The effects of season and altitude on the birds’ use

of rainforest habitats are also assessed. It is anticipated that certain species may occur in

upland areas during summer and lowland areas during winter (Date et al., 1991; Recher

et al. 1995). Potential implications of observed changes in the frugivorous bird

assemblage for the dispersal of large fruited and other rainforest plants in fragmented

landscapes are described.

2.2 Methods

2.2.1 Study region

The study was conducted in a 4 000 km2 subtropical rainforest landscape in the

hinterland of the region known as the Sunshine Coast, approximately 100 km north of

36

the city of Brisbane in Southeast Queensland, Australia (152-154˚ E, 26-27˚ S).

Approximately two-thirds of the pre-European forest cover has been cleared throughout

the region (Catterall et al., 1997), including extensive areas of rainforest (Meier and

Figgis, 1985; Young and McDonald, 1987). Extant forest fragments comprise a mosaic

with cattle grazing land, agricultural cropland, plantation forests and suburban

development (e.g., Figure 2.1).

Rainforest in coastal lowland areas of the study region had been almost totally

cleared by the early 20th century (Frawley, 1991). Except for rainforest patches within

open forests in the Cooloola area in the north, lowland rainforest has been reduced to

scattered, small isolates behind coastal sand dunes or fringing watercourses. Rainforest

in sub-coastal lowlands associated with the Mary River Valley, situated approximately

30 kilometres inland, have also been heavily cleared, mostly for cattle grazing. Much of

the remainder of the study region comprises undulating terrain associated with the

Blackall and Conondale Ranges. A large expanse of continuous rainforest formerly

occurred on the basaltic plateau of the Blackall Range, but this had been extensively

cleared by the early twentieth century, firstly for timber and then for dairy farming

(Young and McDonald, 1987; Watson, 1989; Frawley, 1991), leaving rainforest

remnants in gullies and along steeper slopes (e.g., Figure 2.1). Extensive eucalypt

forest-rainforest mosaics extend from the northern and southern ends of the Blackall

Range and cover large areas of the Conondale Ranges. Unmanaged rainforest regrowth

on previously cleared land makes an increasing contribution to regional forest cover.

Additionally, many small areas have been replanted by private landholders, community

groups and local authorities over the past three decades (Catterall et al., 2004).

37

Figure 2.1 Aerial view of part of the Sunshine Coast study region showing remnant and

regrowth forests interspersed with rural and residential land uses on the south eastern

part of the Blackall Range (Source: Queensland Department of Natural Resources,

1997). Forest cover tends to be associated with undulating terrain or watercourses.

The area seen in this view contains a moderate level of forest cover compared with

other fragmented parts of the landscape.

2.2.2 Site network

Study sites were chosen to represent a range of situations in which rainforest

remains or has re-established in the study region. Sixteen replicate sites within each of

three different states of rainforest landscape context and condition were selected: (i)

rainforest within extensive tracts of forest; (ii) remnant rainforest isolated from

extensive forest by surrounding cleared and modified land; and (iii) regrowth, also

isolated by cleared and modified land (Figure 2.2). Sites were identified using

38

vegetation mapping, aerial photography and on-ground assessment. As far as possible,

replicate sites within each type were distributed throughout the study region. A one-

hectare plot was marked within each of the study sites. The configuration of the plot

was influenced by the shape and landform attributes of each site, but was usually either

200 m x 50 m or 100 m x 100 m.

Extensive forest sites were distributed along eastern slopes of the Conondale

Ranges, on the northern and southern ends of the Blackall Range, and on the Cooloola

sand mass in the north of the study region (Figure 2.2). These sites were located within

forest tracts greater that 4 000 ha in size and comprising at least 20% rainforest. Many

of the extensive forest sites were located in patches of rainforest surrounded by eucalypt

open forest and woodland, together with some large areas of forest timber plantations,

usually the native hoop pine Araucaria cunninghamii. Extensive forest sites that were

located in the smaller rainforest patches (several hectares) contained a more

conspicuous eucalypt element, a lower diversity and abundance of rainforest plant

species and were less structurally complex than sites located among larger rainforest

patches (tens to hundreds of hectares).

The sixteen extensive forest sites were stratified by altitude: five were located in

upland (>500 m a.s.l), six in mid-elevation (200-500 m a.s.l) and the remaining five in

lowland (<200 m a.s.l.) forests (overall range 90-800 m a.s.l., mean 370 m, S.E. 53 m).

Remnants and regrowth were located at mid-elevations and in lowland areas (both

ranging from 20-500 m a.s.l.: remnants, mean 206 m, S.E. 41 m; regrowth, mean 165

m, S.E. 41 m). It was not possible to locate high altitude replicate sites of remnant or

regrowth rainforest.

39

Figure 2.2 Map of study region showing site locations in relation to the coast,

watercourses (dark lines) and major water bodies (speckled areas). Inset: Location of

study region in relation to the Australian continent.

Remnant sites were patches of native vegetation around which all or most of the

original vegetation had been cleared. As far as possible, remnant sites were chosen to

encompass the floristic and structural variation shown in extensive forest sites, so as to

40

concentrate on the influence of landscape situation rather than resource differences.

Eight were remnants of the formerly-extensive rainforest on the basaltic Blackall Range,

seven had a sclerophyll forest component (e.g. trees from Eucalyptus and Lophostemon)

and the remaining site was littoral rainforest. Remnant sites were often situated along

watercourses, in gullies and on slopes that were too steep to be cleared. The interiors of

remnant patches were generally intact, although some had been selectively logged. Sites

were not currently grazed by cattle.

The following fleshy fruited plant taxa were characteristic of extensive and

remnant sites: palms (e.g. Archontophoenix cunninghamiana and Livistona australis),

figs Ficus spp., laurels (especially Cryptocarya spp. and Endiandra spp.),

Elaeocarpaceae (Elaeocarpus and Sloanea spp.), basswoods (especially Polyscias spp.),

Sapotaceae (e.g. Pouteria spp.), Sapindaceae (e.g. Diploglottis australis) and fleshy

fruited Myrtaceae (e.g. Syzygium and Acmena spp.). Fleshy fruited vines, especially the

native grapes (Cissus spp. family Vitaceae), whip vine Flagellaria indica and climbing

pandans Freycinetia spp. (both genera from the Pandanaceae) were common throughout

extensive and isolated remnant sites. Some remnant sites seemed to contain a greater

proportion of pioneer species such as bleeding heart Homalanthus nutans and

macaranga Macaranga tanarius (both Euphorbiaceae), blackwood wattle Acacia

melanoxylon (Mimosaceae) than extensive sites. These and fleshy fruited weeds such as

camphor laurel Cinnamomum camphora (Lauraceae), broad- and small-leaved privet

Ligustrum lucidum and L. sinense (Oleaceae), wild tobacco Solanum mauritianum

(Solanaceae) and lantana Lantana camara (Verbenaceae) were usually found in areas of

ongoing disturbance, such as around walking tracks or near edges, especially in smaller

remnants.

Regrowth sites were located mostly on former cattle pasture that had been

regenerating for at least a decade. The floristic and structural composition of regrowth

41

sites differed from remnant and extensive forest sites. Patches with a developed tree

species layer about 10 to 15 m in height were chosen. Regrowth sites generally

contained a lower abundance and diversity of large-diameter trunks than remnant and

extensive forest sites. Regrowth sites commonly contained the following plant taxa:

sandpaper figs (Ficus coronata and F. fraseri Moraceae), jackwood Cryptocarya

glaucescens, bleeding heart Homalanthus nutans, basswood Polyscias elegans

(Araliaceae), wild quince Guioa semiglauca (Sapindaceae), and piccabeen palms

Archontophoenix cunninghamiana. The suite of introduced woody weeds from the

Lauraceae, Oleaceae, Solanaceae and Verbenaceae that occurred in disturbed areas in

remnants was common in most regrowth sites. Fleshy fruited vines were also common.

There were more patches of rainforest throughout extensive forest mosaics than

in the landscapes surrounding remnant and regrowth sites. Individual remnant and

regrowth sites varied in their isolation from other forest, with some sites located within

relatively well forested (>50% forest cover) areas, many sites in moderately forested

(30-50%) parts of the landscape, and several in areas where over 70% of the forest had

been cleared. Regrowth sites were often situated in more highly cleared parts of the

landscape than remnant sites. Sites of the same type were separated by at least 2 km,

and most were more than 5 km apart. Sites of different types were also usually well

separated, although there were four cases where a remnant and a regrowth site were

closely situated. Most remnant and regrowth sites were between five and 10 km from

extensive forest, although some were located further away. Remnant sites ranged in size

(including interspersed eucalypt forest) from two to 100 ha (approximate mean 46.1 ha,

S.E. 9.4 ha) and regrowth sites were between approximately two and 10 ha in size

(mean 3.4 ha, S.E. 0.5 ha).

42

2.2.3 Bird surveys

The quantitative measure of bird abundance was the number of individuals of

each frugivorous bird species seen or heard during a 40 minute visit to each 1 ha plot.

Bird counts were conducted within four hours of dawn and involved walking throughout

the plot as many times as possible, following up on movements and sounds of falling

fruit. A combination of visual detection and call recognition was used to identify the

bird species. Most of the frugivorous bird species have loud, distinctive calls, making

them equally detectible across site types. Small, canopy-dwelling species (e.g.

mistletoebird) may have been under-recorded if they were not calling. The author

surveyed all sites. Bird surveys were not conducted during strong wind or heavy rain.

Each plot was surveyed in this manner on four separate occasions; twice during

January-March (summer) and twice between July and September (winter) in 2001.

Consecutive surveys at any site were no less than three weeks apart. The total

observation time at each site was 160 minutes; 80 minutes in both summer and winter.

The data on frugivorous bird distribution deriving from these bird surveys was

used in subsequent chapters of this thesis (Chapters Three, Five and Six). The

distribution of frugivorous bats was assessed using the same site network (reported in

Chapter Six).

2.2.4 Data treatment

The number of individuals of each frugivorous bird species was summed across

the two visits made during a season. Data for species that were recorded in less than five

sites in either season were not statistically analysed because their frequency was

considered too low to determine a distribution pattern. A two-way split plot Analysis of

Variance (ANOVA) was used to test whether the abundance of birds that were recorded

in at least five sites during both seasons varied between site types (three levels:

43

extensive, remnant, regrowth) and seasons (two levels: summer, winter). Season was

used as the split, with site nested within site type (site:site type) as the error term when

testing for effect of site type, and site:site type x season as the error term when testing

for the effect of season or the interaction between season and site type. Where a species

was recorded in at least five sites during one season only, a one-way ANOVA was

conducted on the data from only that season to test for an effect of site type on

abundance, and a paired t-test was used to test whether the difference in numbers

between seasons was significant. A species was considered to show a substantial

difference in numbers between summer and winter if the ANOVA result was significant

and the abundance turnover exceeded 50% (after Catterall et al., 1998). The method

used to calculate seasonal turnover:

percent abundance turnover =

Where: max. is number of individuals recorded in the season in which the species was most

common; and

min. is the number in the season in which it was least common.

Where there was a significant effect of site type, Least Significant Difference

(LSD) comparisons were conducted to test for pair-wise differences. ANOVA procedures

and LSD tests were conducted using the SAS statistical package (SAS Institute 1999).

Multidimensional scaling ordination using the semi-strong hybrid technique

(Faith et al., 1987) in WinPATN (Belbin et al., 2003) was used to describe differences

among the 48 sites in terms of patterns of variation in frugivorous bird species

composition. Data for 39 bird species were included in these analyses; three species that

were detected at only one site (rock dove, blue-faced honeyeater and house sparrow)

(max. – min.)

max.

x 100

44

were not included. Principal axis correlations were conducted to determine associations

between the site ordination and the abundance of each bird species; associations found

to be significant (at p<0.05) using a randomisation test (10 000 iterations) were

displayed as species abundance vectors in the ordination space. Analysis of Similarity

(ANOSIM; Clarke and Green, 1988) was used to test for overall and pair-wise

differences (using 10 000 iterations) among the three site types in their frugivorous bird

species composition.

An interaction between site elevation (three levels: high (N=5), mid (N=6) or

low (N=5)) and season (two levels: summer and winter) on selected frugivorous bird

numbers in extensive forest was tested by way of a two-factor ANOVA using the PROC

GLM procedure in SAS (SAS Institute 1999). Analyses were conducted on pooled data

for all frugivorous birds and separately on data for selected species (those nominated as

being altitudinal migrants by Date et al. (1991)).

2.2.5 Classification of frugivorous birds

Literature searches revealed records of many bird species consuming fleshy

fruit. As pointed out by Jones and Crome (1990), almost any rainforest-dwelling

vertebrate will occasionally eat fleshy fruit, although some species do so very rarely.

Reference texts were used to systematically determine which of the bird species

recorded during field surveys were frugivorous. A species was classified as frugivorous

if frugivory was included in its dietary description in Blakers et al. (1984), or if it had

been recorded consuming fruits from more than plant three genera in Barker and

Vestjens (1988, 1989) or in the Handbook of Australian, New Zealand and Antarctic

Birds (HANZAB) series (Marchant and Higgins, 1993; Higgins and Davies, 1996;

Higgins, 1999; Higgins et al., 2001)). Parrots, lorikeets, rosellas, cockatoos (Green,

1993) and some pigeons (Frith, 1982) grind or crush many, if not most of the seeds

45

from the fleshy fruits they consume. Although such birds may have relatively low

potential as seed dispersers (Snow, 1981), they were included in the list of avian

frugivores if they satisfied the previous criteria.

2.3 Results

2.3.1 Abundance of frugivorous bird species in extensive, remnant and regrowth sites

Using the criteria stated in Section 2.2.5, 42 bird species were classified as

frugivores (Table 2.1). In total, 2768 individuals from these species were recorded

during surveys. Other species that were known to eat fruit infrequently were recorded

during surveys but these did not meet the stated criteria and are not considered further in

this study. Of the 42 frugivorous bird species recorded during surveys, 26 were

sufficiently common (present at five or more sites in at least one season) for statistical

analyses (Table 2.1). Twelve of these 26 species showed a statistically significant

(P<0.05) difference in abundance among the three site types in one or both seasons. The

patterns of abundance change between remnant and/or regrowth sites and extensive

forest are indicated in Table 2.2. Eight frugivorous bird species showed a significant

difference between seasons together with greater than 50% seasonal turnover in

abundance. The rose-crowned fruit-dove Ptilinopus regina and scarlet honeyeater

Myzomela sanguinolenta showed a significant interaction between site type and season.

Patterns of statistically significant differences in abundance between site types (Table

2.2, Figure 2.3) grouped readily into three classes:

1. decreasers: species that showed lower numbers outside extensive forest in

remnant and/or regrowth sites;

2. increasers: species that showed higher numbers outside extensive forest in

remnant and/or regrowth sites; and

46

3. tolerant: no significant difference in numbers between remnants, regrowth and

extensive forest.

There were five decreaser species (Tables 2.2, 2.3), three of which were fruit-

doves (Ptilinopus spp.). The fruit-doves generally showed declining abundance from

extensive forest through remnants to regrowth (Tables 2.2, Figure 2.3(i-ii)). The other

two decreasers, the brown cuckoo-dove and green catbird, showed similar abundance in

extensive and remnant forests but were less common in regrowth (Table 2.2, Figure

2.3(iii)). There were seven increaser species (Tables 2.2, 2.3, five of which (rainbow

lorikeet, black-faced cuckoo-shrike, figbird, Torresian crow and silvereye) were

significantly more abundant in regrowth than in either remnant or extensive forest

(Table 2.2, Figure 2.3(v)). The increaser bar-shouldered dove showed similar abundance

between remnant and regrowth sites and was absent from extensive forest (Figure

2.3(iv)), while the Australian magpie was present, but least abundant in extensive forest,

and most abundant in regrowth, with numbers in remnant forest intermediate (Table 2.2,

Figure 2.3(vi)). The remaining 14 species were classified as tolerant (Table 2.3), since

their numbers did not differ significantly among site types (Table 2.2, Figure 2.3(vi)).

47

Table 2.1 Frugivorous bird species recorded in this study. Nomenclature and order

follow Christidis and Boles (1994) († indicates seed grinder (likely to destroy seeds)

and * indicates introduced species). ‘Number of sites’ indicates the number of sites (out

of 48) in which the species was recorded in summer (two surveys), winter (two

surveys) and across all surveys. Analyses (+) shows species that were analysed

statistically.

Number of sites: Common name Scientific name summer winter all

surveys Analyses

Australian brush-turkey† Alectura lathami 16 14 23 +

rock dove†* Columba livia 0 1 1

white-headed pigeon† C. leucomela 16 13 22 +

brown cuckoo-dove† Macropygia amboinensis 40 37 42 +

emerald dove† Chalcophaps indica 12 8 15 +

bar-shouldered dove† Geopelia humeralis 15 16 23 +

wonga pigeon† Leucoscarcia melanoleuca 3 3 5

wompoo fruit-dove Ptilinopus magnificus 18 20 25 +

superb fruit-dove P. superbus 12 1 13 +

rose-crowned fruit-dove P. regina 36 6 36 +

topknot pigeon Lopholaimus antarcticus 5 1 6 +

galah† Cacatua roseicapilla 2 1 3

sulphur-crested cockatoo† C. galerita 8 14 16 +

rainbow lorikeet† Trichoglossus haematodus 29 22 32 +

scaly-breasted lorikeet† T. chlorolepidotus 4 3 7

Australian king-parrot† Alisterus scapularis 12 18 23 +

crimson rosella † Platycercus elegans 3 1 4

pale-headed rosella† P. adscitus 4 10 14 +

common koel Eudynamys scolopacea 17 0 17 +

channel-billed cuckoo Scythrops novaehollandiae 7 0 7 +

little wattlebird Anthochaera chrysoptera 0 6 6 +

noisy friarbird Philemon corniculatus 0 3 3

blue-faced honeyeater Entomyzon cyanotis 0 1 1

noisy miner Manorina melanocephala 3 1 3

Lewin's honeyeater Meliphaga lewinii 48 48 48 +

scarlet honeyeater Myzomela sanguinolenta 17 26 33 +

black-faced cuckoo-shrike Coracina novaehollandiae 3 10 10 +

barred cuckoo-shrike C. lineata 2 0 2

varied triller Lalage leucomela 2 2 4

olive-backed oriole Oriolus sagittatus 1 1 2

figbird Sphecotheres viridis 31 36 41 +

grey butcherbird Cracticus torquatus 2 2 4

Australian magpie Gymnorhina tibicen 18 20 26 +

pied currawong Strepera graculina 23 35 38 +

paradise riflebird Ptiloris paradiseus 4 3 5

Torresian crow Corvus orru 20 34 35 +

green catbird Ailuroedus crassirostris 32 28 35 +

regent bowerbird Sericulus chrysocephalus 1 4 5

satin bowerbird Ptilonorhynchus violaceus 7 2 7 +

house sparrow†* Passer domesticus 0 1 1

mistletoebird Dicaeum hirundinaceum 3 2 5

silvereye Zosterops lateralis 4 18 20 +

48

Table 2.2 Frugivorous bird species’ abundances in each of the three site types, during

summer and winter. Nomenclature and order follow Christidis and Boles (1994). The

mean abundance of individuals (No. individuals per hectare per hour; summed across

two 40-minute surveys in 1 ha) is shown for all sites (Total), in Extensive forest (Ext, 16

sites), Remnants (Rem, n=16), and Regrowth (Reg, n=16). ANOVA p shows results of

analyses testing for differences in abundance between site types (ST), seasons (S)

and STxS. x indicates season for which effect of site type was not tested (species too

infrequent). Letters next to means show LSD results (means with different letters are

significantly different). Abund. pattern corresponds with Figure 2.2 (i to iii are

“decreasers”, iv to vi “increasers”, and vii “tolerant”).

Mean abundance ANOVA p values

Bird species Season Total Ext Rem Reg ST S ST x S Abund. pattern

Australian brush-turkey s 0.63 0.44 0.82 0.63 0.35 0.17 0.96 vii

w 0.38 0.13 0.56 0.44

white-headed pigeon s 0.63 0.38 0.88 0.63 0.10 0.55 0.11 vii

w 0.77 0.19 0.63 1.50

brown cuckoo-dove s 2.04 2.75a 2.63a 0.75b 0.02 0.20 0.06 iii

w 2.46 2.06 3.63 1.69

emerald dove s 0.42 0.25 0.56 0.44 0.43 0.07 0.89 vii

w 0.23 0.13 0.38 0.19

bar-shouldered dove s 0.52 0.00b 0.88a 0.69a 0.002 0.67 0.29 iv

w 0.46 0.00 0.50 0.88

wompoo fruit-dove s 1.21 2.65a 1.00b 0.00c 0.0002 0.87 0.71 i

w 1.25 2.65 0.82 0.31

superb fruit-dove s 0.29 0.56a 0.25ab 0.06b 0.031 0.00122 ii

w 0.02 0.00 0.06 0.00 x

rose-crowned fruit-dove s 1.88 2.81a 2.00b 0.81c 0.0021 0.0001 0.04 i

w 0.23 0.56 0.13 0.00 0.071

topknot pigeon s 0.44 1.06 0.06 0.19 0.241 0.332 vii

w 0.15 0.00 0.00 0.44 x

sulphur-crested cockatoo s 0.35 0.56 0.31 0.19 0.07 0.54 0.08 vii

w 0.42 0.94 0.13 0.19

rainbow lorikeet s 2.52 1.81b 1.19b 4.56a 0.01 0.08 0.16 v

w 1.73 0.94 1.50 2.75

Australian king-parrot s 0.35 0.38 0.38 0.32 0.31 0.17 0.34 vii

w 0.65 1.06 0.63 0.26

pale-headed rosella s 0.15 0.25 0.19 0.00 x

w 0.69 0.00 0.75 1.31 0.101 0.362 vii

common koel s 0.48 0.38 0.38 0.69 0.401 0.00012 vii

w 0.00 0.00 0.00 0.00 x

channel-billed cuckoo s 0.17 0.06 0.19 0.25 0.461 0.012 vii

w 0.00 0.00 0.00 0.00 x

little wattlebird s 0.00 0.00 0.00 0.00 x

w 0.15 0.00 0.18 0.25 0.211 0.022 vii

Lewin's honeyeater s 4.29 4.13 4.75 4.00 0.46 0.04 0.53 vii

w 3.79 3.88 3.88 3.63

49

scarlet honeyeater s 0.60 1.00 0.56 0.25 0.061 0.12 0.03 vii

w 0.92 0.56 1.13 1.06 0.271

black-faced cuckoo-shrike s 0.08 0.00 0.00 0.25

w 0.60 0.13b 0.06b 1.63a 0.0061 <0.00012 v

figbird s 3.60 1.00b 2.56b 7.25a 0.0006 0.26 0.81 v

w 4.96 1.56 4.94 8.38

Australian magpie s 1.40 0.00c 1.00b 3.19a <0.0001 0.31 0.17 vi

w 1.08 0.13 1.06 2.06

pied currawong s 0.98 0.88 1.06 1.00 0.42 0.0004 0.40 vii

w 2.31 1.88 3.06 2.00

Torresian crow s 1.04 0.25b 0.82b 2.06a 0.0001 0.02 0.81 v

w 1.85 1.19 1.32 3.06

green catbird s 1.58 1.94a 2.44a 0.38b 0.0001 0.55 0.89 iii

w 1.46 1.81 2.19 0.38

satin bowerbird s 0.19 0.13 0.19 0.25 0.751 0.452 vii

w 0.10 0.06 0.00 0.25 x

silvereye s 0.42 0.00 0.00 1.25 x

w 2.59 1.06b 1.69b 5.00a 0.031 0.0022 v 1 p value from single-factor ANOVA testing site type effect within season 2 p value from paired t-test of difference between seasons; all other p values from two-way ANOVA

50

Figure 2.3 Examples of the seven patterns of abundance in remnants and regrowth

compared with extensive forest. Abundance (average of summer and winter data) shows

mean and standard error in Ext = Extensive forest tracts; Rem = Remnant forest; and Reg =

Regrowth patches; Patterns are exemplified using data from selected bird species: i)

wompoo fruit-dove, ii) superb fruit-dove, iii) green catbird, iv) bar-shouldered dove, v)

figbird, vi) Australian magpie, and vii) Lewin’s honeyeater. Means with different letters are

significantly different (P <0.05 in LSD comparisons); see also Tables 2.1 and 2.2.

DECREASERS TOLERANT

Ext Rem Reg Ext Rem Reg

Ext Rem Reg

0

2

4

i) A

bu

nd

ance

0

0.2

0.4

Ab

un

dan

ce

0

1

2

3

iii)

INCREASERS

0

1

iv) A

bu

nd

an

ce

0

4

8

v)

0

2

4

vi)

0

2

4

vii)

a

b

c

b

ab

a ii)

b

a a

a

b

b

a a a

a a

b

a

a a a

a

a

a a a

b

b

b

b

b

b

c

c

ab

b

51

Table 2.3 Frugivorous bird species' responses to rainforest fragmentation, and their

seasonality. Numerals (i-vii) show the pattern of abundance change among the three

site types (see text, Fig. 2.3 and Table 2.2); Season shows the time of greater

abundance if the effect of season was significant and turnover exceeded 50%. †

indicates seed-crusher (likely to destroy seeds).

Species Season i wompoo fruit-dove

rose-crowned fruit-dove summer

ii superb fruit-dove summer

Decreasers

iii brown cuckoo-dove† green catbird

iv bar-shouldered dove† Increasers

v rainbow lorikeet† black-faced cuckoo-shrike figbird Torresian crow silvereye

winter winter

vi Australian magpie

Tolerant

vii Australian brush-turkey† white-headed pigeon† emerald dove† topknot pigeon sulphur-crested cockatoo† Australian king-parrot† pale-headed rosella† common koel channel-billed cuckoo little wattlebird Lewin’s honeyeater scarlet honeyeater pied currawong satin bowerbird

summer summer winter winter

2.3.2 Changes in the frugivorous bird assemblage in fragmented forest

Figure 2.4(i) displays an ordination of the 48 study sites based on the abundance

of frugivorous bird species. The extensive forest sites are grouped towards one extreme

of the ordination space, with regrowth sites at the other and remnant sites intermediate

in terms of bird species composition. The composition of the frugivorous bird

assemblage varied significantly among the three site types (ANOSIM global p<0.001) and

between all site types in separate pair-wise comparisons (ANOSIM p = 0.001 for extensive

versus remnant sites; p<0. 0001 for both other comparisons).

52

Figure 2.4(ii) shows that the bird species associated with the region of the

ordination containing most of the extensive forest sites included the five decreaser

species. In addition, the topknot pigeon and sulphur-crested cockatoo, both of which

showed a decreasing trend (Table 2.2) and the paradise riflebird, which was only

recorded in extensive forest (Table 2.4), were associated with this region of the

ordination. The bird species associated with regrowth sites included the seven increaser

species as well as two non rainforest species (noisy miner and grey butcherbird) and the

pale headed rosella (Figure 2.4(ii)).

53

Figure 2.4 (i) Ordination of the 48 study sites based on the abundances of 39

frugivorous bird species (Stress = 0.28). Extensive forest (filled square), remnants

(open diamond), regrowth (filled triangle). (ii) Abundance vectors for bird species

significantly (p <0.05) associated with the ordination. Fragmentation response patterns

are shown in brackets: Dec decreaser, Tol tolerant, Inc increaser, U untested.

green catbird (Dec)

rose-crowned fruit-dove (Dec)

ii)

grey butcherbird (U)

topknot pigeon (Tol)

sulphur-crested cockatoo (Tol)

wompoo fruit-dove (Dec)

brown cuckoo-dove (Dec)

noisy friarbird (U)

black-faced cuckoo-shrike (Inc) Australian magpie (Inc)

silvereye (Inc)

figbird (Inc)

bar-shouldered dove (inc)

pale-headed rosella (Tol)

noisy miner (U)

Torresian crow (inc) rainbow lorikeet (inc)

paradise riflebird (U)

superb fruit-dove (Dec)

i)

54

2.3.3 Seasonal patterns of frugivorous bird abundance

The common koel and channel-billed cuckoo were absent in winter, yet

relatively common during summer, clearly the result of immigration. The rose-crowned

and superb fruit-doves also showed large and significant summer increases, although

they were present in low numbers during winter months, a pattern that is also consistent

with immigration into the study region. The black-faced cuckoo-shrike, silvereye, little

wattlebird, and pied currawong were recorded in substantially higher numbers during

winter than summer. Numbers of the Lewin’s honeyeater and Torresian crow also

differed between seasons, but their seasonal abundance turnover was less than 50%, and

was probably due to factors such as reproduction or local movements rather than larger-

scale migration. The remaining 18 species showed no significant difference in

abundance between seasons. The decreasing response pattern detected for the rose-

crowned fruit-dove was significant only during summer (Table 2.2). During winter,

numbers of this species were similar across site types, although its abundance was very

low. The significant interaction detected in the ANOVA for the scarlet honeyeater was not

supported by LSD tests, although a tendency towards a decreasing response pattern was

shown in summer, with a trend towards an increasing response pattern in winter (Table

2.2).

2.3.4 Effects of altitude and season on frugivorous bird numbers

The numbers of frugivorous birds (data for all species pooled) and of the

wompoo and rose-crowned fruit-doves, white-headed and topknot pigeons and the

brown cuckoo-dove in extensive forest at different elevations in summer and winter is

shown in Table 2.5. No significant (p<0.05) interactions were detected between the two

factors using ANOVA, indicating that the data on bird abundance patterns were not

strongly influenced by altitudinal movements of rainforest pigeons. Note that the superb

55

fruit-dove was not recorded at any extensive forest sites, and very few other sites, in

winter.

56

Tab

le 2

.5 F

rugi

voro

us b

ird a

bund

ance

pat

tern

in h

igh,

mid

- an

d lo

w e

leva

tion

site

s du

ring

sum

mer

(s)

and

win

ter

(w).

The

mea

n (a

nd s

tand

ard

erro

r)

num

ber

of in

divi

dual

s of

all

frug

ivor

es a

nd s

elec

ted

rain

fore

st p

igeo

ns is

sho

wn

for

each

sea

son

(dat

a fr

om tw

o su

rvey

s su

mm

ed)

in e

ach

elev

atio

n

cate

gory

; AN

OV

A p

sho

ws

resu

lts o

f tw

o-w

ay A

NO

VA

(E

=el

evat

ion,

S=

seas

on a

nd E

xS=

inte

ract

ion)

.

Ele

vatio

n ca

tego

ry (

m a

.s.l.

) A

NO

VA p

B

ird s

peci

es

Sea

s.

>50

0 (n

=5)

20

0-50

0 (n

=6)

<

200

(n=

5)

E

S

ExS

al

l fru

givo

rous

bird

s s

30.2

0 (4

.24)

23

.33

(1.9

2)

20.8

0 (2

.85)

0.

68

0.40

0.

39

w

20

.80

(3.2

0)

21.1

7 (5

.35)

23

.40

(5.8

5)

w

hite

-hea

ded

pige

on

s 0.

00

0.83

(0.

39)

0.

20 (

0.20

) 0.

29

0.39

0.

14

w

0.

40 (

0.41

) 0.

17 (

0.16

) 0.

00

w

ompo

o fr

uit-

dove

s

4.00

(0.

96)

2.00

(0.

57)

2.00

(0.

85)

0.24

0.

98

0.48

w

3.00

(1.

44)

1.67

(0.

74)

3.40

(1.

31)

ro

se-c

row

ned

frui

t-do

ve

s 2.

00 (

0.56

) 3.

50 (

0.75

) 2.

80 (

1.22

) 0.

51

0.00

07

0.35

w

0.40

(0.

25)

0.17

(0.

16)

1.20

(0.

81)

br

own

cuck

oo-d

ove

s 3.

40 (

0.76

) 2.

83 (

0.30

) 2.

00 (

0.64

) 0.

15

0.16

0.

56

w

2.

00 (

0.85

) 2.

67 (

0.33

) 1.

40 (

0.61

)

57

2.4 Discussion

In this study, extensive forest sites were treated as a reference against which to

quantify changes in numbers of frugivorous bird species in remnants and regrowth.

Since remnants and extensive forest sites were similar in fleshy fruited plant species

composition, differences in frugivorous bird numbers between these two site types were

most likely due to differences in site context rather than resource availability within the

site. Differences in frugivorous bird numbers between remnants and extensive forest

may reflect a response to several factors associated with the differing landscape context,

including reduced total area of habitat, edge effects, or greater functional isolation. The

patterns of bird abundance in regrowth sites reflect differences in both the availability of

fleshy fruit resources and the landscape context.

2.4.1 Bird species showing a decreaser response to rainforest fragmentation

A number of studies in different parts of the world have documented bird

declines and local extinctions in fragmented rainforest (e.g., Kattan et al., 1994; Corlett,

1998; Renjifo, 1999; Castelletta et al., 2000; Ribon et al., 2003). Consistent with

descriptions provided by Frith (1952), the wompoo, rose-crowned and superb fruit-

doves were generally less abundant in remnants and regrowth than extensive forest.

Despite being known to fly across cleared land (Frith, 1952; Howe et al., 1981; Date et

al., 1991, 1996; Gosper and Holmes, 2002), fruit-doves used remnant and regrowth

rainforest habitats in the Sunshine Coast much less frequently than extensive forest

areas. The Australian fruit-doves are obligate frugivores and the plants that characterise

their diets are typical of mature rainforest (Crome, 1975, 1990; Innis, 1989).

Consequently, their low numbers in fragmented forest may be due to low availability of

58

the required plant species in remnants and in the local landscapes surrounding remnant

sites.

Although fruit-doves showed overall decreasing abundance in remnants

compared with extensive forest, their abundance in certain individual remnants

resembled that of extensive rainforest sites. These remnant sites, plotted among

extensive forest sites in the ordination space, were mostly located in relatively well

forested parts of the landscape. These remnants may function as part of a network of

patches (Howe et al., 1981; Date et al., 1991, 1996; Price et al., 1999) that, although

discontinuous, are sufficiently close that the energetic costs and perceived predation risk

associated with movement between patches are not too high. In Mexico, Graham (2001)

described a similar situation for the strong-flying keel-billed toucan Ramphastos

sulphuratus, which moved between forest fragments, but only in parts of the landscape

that contained at least a minimum threshold amount of forest and fruit resources.

The brown cuckoo-dove and green catbird showed much lower abundance in

regrowth than in remnants and extensive forest. The brown cuckoo-dove is noted for its

conspicuousness in regrowth vegetation at forest edges and consumes a range of plants

that are common in rainforest regrowth (Frith, 1952; Crome, 1975; Willson and Crome,

1989). However, this species roosts in well-developed forest (Frith, 1982) and may

therefore be limited in its use of isolated regrowth patches, unless these are located

close to mature forest. Furthermore, the brown cuckoo-dove and green catbird are

sedentary or only locally nomadic in subtropical rainforests (Frith, 1982; Blakers et al.,

1984; Innis and McEvoy, 1992; Date et al., 1996). These species may require a larger

area of contiguous vegetation than is provided within or in local landscapes surrounding

most of the regrowth patches surveyed in this study. In general, these areas occur as

narrow strips or small patches with low amounts of surrounding forest cover compared

with many remnant sites. The data presented in this chapter may indicate area-

59

sensitivity of these species at very small patch sizes. Data presented by Howe et al.

(1981) also suggest that brown cuckoo-doves may be unable to persist in very small

remnants; they were ‘common’ in patches of 1 ha to 2.5 ha, but ‘rare’ in those under 1

ha. While both the brown cuckoo-dove and green catbird are highly frugivorous, the

former grinds ingested seeds in a muscular gizzard (Frith, 1982; Dennis and Westcott,

2006) and the later eats flowers, invertebrates, and the eggs and nestlings of other birds

in addition to fruit (Blakers et al., 1984). The consumption of alternative food sources

that are high in protein relative to the pulp of most fruits (Morton, 1973) may mean that

these species are less constrained in their fruit preferences than the fruit-specialists that

rely only on the nutritional quality of fruit pulp (Snow, 1981). They may consequently

be able to satisfy their energetic and nutritional needs in the smaller area of forest

available in remnants than the obligate frugivore species.

Species declines in fragmented habitats may also result from changed biotic

interactions (Terborgh and Winter, 1980; Karr, 1982; Doak et al., 1992). For example,

the aggressive, non-rainforest noisy miner invaded regrowth patches from the

surrounding matrix. This species has been shown to exclude other bird species in open

eucalypt forest (Piper and Catterall, 2003). Rates of nest predation may also increase in

fragmented rainforest (Sieving and Karr, 1997). However, it is not clear whether the

species classified as decreasers in the present work would be disproportionately affected

by these changes.

The differences in bird species’ abundances between habitat types in the present

study were clearly the result of habitat choice by birds within individual species. For

example, four regrowth sites were located adjacent to, or within tens of metres of,

remnant sites (Figure 2.2). However, these remnant and regrowth sites contained

different bird assemblages and were plotted in separate regions of the ordination based

on bird species’ abundance. At one of these site pairs, several bird species were present

60

in the remnant site but never recorded in the regrowth (e.g. the wompoo and rose-

crowned fruit-doves, and green catbird), or were recorded in much lower numbers in the

regrowth than adjacent remnant rainforest (e.g. brown cuckoo-dove). These results

suggest greater habitat preferences of frugivorous birds in subtropical Australia than

shown by Laurance et al. (1996) in their comparison of adjoining extensive and

regrowth rainforest patches in the Atherton Tableland area of North Queensland.

2.4.2 Bird species showing an increaser response to fragmentation

As well as decreasers, the present work detected several species that increased in

abundance in remnant and regrowth rainforest compared with extensive forest.

Consistent with observations made during the 1950s in subtropical rainforest remnants

(Frith, 1952), the seed-crushing bar-shouldered dove was absent from extensive forest

but invaded some rainforest remnant and regrowth patches. This may reflect greater

availability of grasses or other food within and surrounding remnants and regrowth

patches (Frith, 1952).

The black-faced cuckoo-shrike, figbird, rainbow lorikeet, Torresian crow and

silvereye were found in similar abundance in remnants and extensive rainforest but were

most abundant in regrowth. These species commonly use non-rainforest habitats, in

contrast with the rainforest-dependent decreaser species (Blakers et al., 1984; Catterall

et al., 1998). Furthermore, with the exception of the highly frugivorous figbird, these

increaser frugivores regularly eat a variety of other food types (Blakers, et al. 1984). As

suggested for the bar-shouldered dove, high numbers of these species in regrowth may

reflect ready use of the types of resources occurring within and surrounding regrowth

patches. These may include non-fruit food types such as the high nectar availability in

ornamental garden plantings, or resources like fleshy fruited weeds that would boost the

61

availability of food at various times for frugivores that may not be more opportunistic

than fruit-specialists.

Fleshy fruited weeds, in particular camphor laurel, have been identified as

potentially important food sources for the topknot and white-headed pigeons (Frith,

1982; Innis, 1989; Date et al., 1996). It has been suggested that the spread of camphor

laurel has contributed to an increase in numbers of these species throughout certain

Australian subtropical rainforest landscapes following dramatic declines during the

early half of 1900s (Frith, 1952, 1982; Date et al., 1996). Importantly, camphor laurel

bears fruits at a time when the availability of fruiting native rainforest plants is low

(Innis, 1989; Date et al., 1991; Scanlon et al., 2000). Unlike the fruit-doves, neither the

topknot nor white-headed pigeon, both fruit-specialists, showed significantly different

numbers in rainforest remnants or regrowth compared with extensive forests in the

present study, although topknot pigeon numbers showed a decreasing trend.

2.4.3 Frugivore assemblage change in fragmented habitats

The abundance of over half of the bird species (14 of 26) evaluated in the

present work was similar among extensive forest, remnants and regrowth. It has been

proposed that rainforest contraction in regions such as Africa and Australia during the

Pleistocene may have imposed an ‘extinction filter’ on rainforest fauna (Howe et al.,

1981; Balmford, 1996; Corlett and Primack, 2006). As a result, the species that have

persisted may be those that are unspecialised and with the capacity for movement

between disjunct rainforest patches. These attributes may be associated with relatively

high tolerance of anthropogenic forest fragmentation (Howe et al., 1981; Balmford,

1996; Corlett and Primack, 2006).

The changes in the frugivorous bird assemblage in fragmented forest in the study

region resemble those described by a ‘cut-and-paste’ model (Woinarski 1993; Crome et

62

al., 1994). That is, the avian frugivore communities in remnant and regrowth sites

comprised species from diverse habitats, formed by the decline of some species and

concurrent increase of others, in response to changes in habitat quality, area and/ or

landscape forest cover. This model better describes the assemblage changes documented

between extensive, remnant and especially regrowth sites in the present study than those

that emphasise declines (e.g. ‘nested subsets’; Patterson, 1987).

2.4.4 Seasonal changes in frugivorous bird abundance

A greater abundance and diversity of native fleshy fruits are generally available

in subtropical Australian rainforests during summer than winter (Innis, 1989; Church,

1997). During winter, fruit availability seems to be highest in lowland areas (Innis,

1989; Date et al., 1991). The seasonal differences in fruit availability may influence the

abundance of frugivorous birds in rainforest habitats within the study region. Numbers

of the common koel, channel-billed cuckoo, superb and rose-crowned fruit-doves

increased substantially during summer and all are regular summer immigrants to the

study region. The first two species are total migrants (Higgins, 1999). The rose-crowned

fruit-dove is a partial migrant, with some individuals over-wintering in forests within

the study region while the majority of individuals appear to return to tropical forests in

northern Australia or Papua New Guinea (Blakers et al., 1984). The superb fruit-dove is

considered vagrant in subtropical Australia.

Numbers of the little wattlebird, black-faced cuckoo-shrike, pied currawong and

silvereye increased substantially during winter. The higher winter numbers of silvereyes

reflect an influx of individuals of this species from the south to the study region

(Blakers et al., 1984). The silvereye and the black-faced cuckoo-shrike were classed as

increasers in the present study, while the other two winter-abundant species (little

wattlebird and pied currawong) were classified as tolerant. This contrasted with the bird

63

species that were more common in summer than winter in that they were either

decreasers (the fruit-doves) or classed as tolerant (common koel and channel-billed

cuckoo). All four winter-abundant bird species make use of remnant and especially

regrowth rainforests, and their increased winter abundance may indicate a response to

winter fruit availability in regrowth habitat, potentially including the winter-fruiting

weeds. Indeed, silvereyes of a subtropical island population were found to increase

their intake of fruit during winter (Catterall, 1985), and pied currawongs have been

reported to move from eucalypt open forests into rainforest during winter (Lindsey,

1995), concurrent with a dietary shift from insects to fruit (Blakers et al., 1984). There

is some evidence of a winter influx of the little wattlebird into eastern Queensland

(Blakers et al., 1984). This species usually occupies coastal eucalypt forests and

heathlands rather than rainforests (Blakers et al., 1984), but the occurrence of this

species in coastal remnant and regrowth rainforest in the Sunshine Coast, possibly

reflects increased fruit intake during winter.

Date et al. (1991, 1996) suggested that there may be seasonal altitudinal

migration in some species of rainforest pigeon, and proposed the general scenario of

movement into upland forests during summer and lowland forests during winter. The

surveys conducted for the present study may have been too infrequent to detect detailed

seasonal movement patterns, but would have captured substantial turnover between

altitudes. The results do not show a seasonal exchange of frugivorous birds between

extensive forest sites at different elevations.

2.4.5 Frugivorous birds and seed dispersal in remnant and regrowth rainforest:

conservation implications

The wompoo fruit-dove suffered population declines and localised extinctions

from southern parts of its range (the southern limits of subtropical rainforest in

64

Australia) during the early part of the 20th century (Recher et al., 1995) and appeared to

be declining in other parts of subtropical Australia from the late 1920s, following

widespread rainforest clearing and fragmentation. This prompted Frith (1952) to predict

that this species was …”doomed to early extinction” (pp.91-92). Frith (1952) also

forecast ongoing decline in superb fruit-dove populations as a result of rainforest loss

but suggested the nomadic behaviour of rose-crowned fruit-doves would give them

greater resilience to habitat destruction and fragmentation (Frith, 1982). Patterns of

frugivorous bird abundance in Sunshine Coast habitats suggest that neither regrowth nor

remnant rainforest patches provide suitable habitat for significant numbers of these

three fruit-dove species.

Changed dispersal of rainforest plants has been predicted as a consequence of

frugivore declines in fragmented landscapes throughout the world (Howe, 1984; Crome

1990; Janzen and Vasquez-Yanez, 1991; Corlett, 1998; Sodhi et al., 2004; Terborgh and

Nuñez-Iturri, 2006). Silva and Tabarelli (2000) predicted that around 30% of native

plant species could be lost from forest fragments in Brazil, based on an assessment of

the patterns of frugivore decline in that region and the potential for frugivore species to

disperse large seeds and certain plant families. While the present study classified a

group of decreaser frugivore species, it also showed the numerical replacement of these

by a suite of increaser species. Increasers also potentially disperse rainforest seeds, but

it is unclear whether these species may substitute in fragmented forests by dispersing

the same suite of plant species as birds from the decreaser group. In subtropical

Australia, the fruit-doves may swallow and disperse larger fruits and seeds than most

other frugivorous species (Green 1993). If increaser or tolerant species do not disperse

the same large fruited plant species as the decreasers, seedlings of such plants may not

recruit in many rainforest regrowth or remnant patches. Even if non-decreaser

frugivores disperse similar plant species to decreasers, rates of seed dispersal for these

65

plant species will be lower, unless tolerant or increaser frugivores show density

compensation (Renjifo, 1999; Loiselle and Blake, 2002) or increased rates of fruit

consumption. Higher-order interactions involving seed or seedling predators may also

change in fragmented forest landscapes, and may exacerbate or offset the effects of

changed seed dispersal (Harrington et al. 1997; Murray and Garcia, 2002; Wright et al.

2002). Following seed dispersal, factors that influence plant establishment, growth and

survival determine regeneration outcomes (Wang and Smith, 2002).

The seeds of plants dispersed by increaser birds are likely to be moved into and

around fragmented forest landscapes at greater rates than in extensive forest. It has

been suggested that fruits consumed by mixed diet, opportunistic frugivores, such as

characterise the increaser species of the present study, may be mostly sugary, watery

and small seeded (McKey, 1975). Many fleshy fruited weeds fit this description

(Richardson et al., 2000) and their increased dispersal and recruitment in remnants and

regrowth can be expected as a result of the regular use of these habitats by the increaser

bird species. This may lead to positive feedback cycles between the fleshy fruited weeds

and the fragmentation-tolerant opportunistic frugivores in regrowth areas of highly

disturbed rainforest landscapes.

Qualitative aspects of seed dispersal may also change in fragmented forests. For

example, the abundance of two seed-crusher species increased (bar-shouldered dove and

rainbow lorikeet), while only one (the brown cuckoo-dove) decreased in fragmented

forest habitats. This may mean that a greater proportion of the seeds of the plant species

consumed in fragmented forest are destroyed than are dispersed in viable condition,

although neither of the increaser species seem to consume large amounts of fleshy fruit.

Furthermore, the lump-lined stomach of the decliner fruit-doves (Crome, 1975)

potentially influences germination success of seeds. Differences among frugivore

species in their use of particular habitat elements may also change spatial patterns of

66

seed dispersal in fragmented parts of the landscape (Schupp, 1993; Silva et al., 1996;

Alcántara et al., 2000; Jordano and Schupp, 2000; Loiselle and Blake, 2002; Dennis and

Westcott, 2006).

67

Chapter Three

Seed dispersal potential of frugivorous bird species in relation to their

gape width, frugivory level and seed treatment

3.1 Introduction

Fruit-eating birds may disperse the seeds of up to 70% of plant species in

subtropical Australian rainforests (Willson et al., 1989; Green, 1995; Butler, 2003).

There may be variation among bird species in the plant species that they disperse

because of different patterns of plant species consumption (Crome, 1975; Snow, 1981;

Herrera, 1984; Howe, 1986; Innis, 1989; Sun et al., 1997; Brown and Hopkins, 2002).

However, there is little agreement regarding the factors that influence patterns of plant

species consumption by frugivore species (Herrera, 1998, 2002). Consequently, in the

absence of detailed dietary information, which is typically available for only a small

proportion of the species in a frugivore assemblage (e.g., Crome, 1975), there is only a

limited basis for predicting patterns of plant consumption by frugivore species. Major

differences among frugivore species in their patterns of plant species consumption may

be related to certain morphological and behavioural attributes. If so, it may be possible

to use these attributes to describe groups of frugivore species with similar combinations

of attributes (functional groups) that potentially disperse similar plant species to one

another.

The role that a bird species plays in the dispersal of seeds of a particular plant

species depends first on whether it feeds on fruit from that plant species and second on

whether it disperses viable seeds or destroys seeds. Birds may crush and destroy seeds

either in the bill while feeding (parrots: Crome and Shields 1992) or by grinding during

68

digestion (some pigeons and doves: Frith 1982, and megapodes). Seed-crushing birds

would make a small contribution to seed dispersal.

Patterns of plant species consumption reflect variation among frugivorous bird

species in their gape sizes. Gape width imposes an intractable limit on the size of fruits

and/or seeds able to be ingested by a bird species (Herrera, 1981; Moermond and

Denslow, 1985; Wheelwright, 1985). Consequently, bird species with narrow gapes are

physically constrained to swallowing only small fruits, whereas birds with wider gapes

are capable of consuming plant species with larger fruits (Wheelwright, 1985).

The plant species consumed by a bird species may also be influenced by the

extent to which it specialises on fruit rather than other food sources. For example, it was

predicted that birds with fruit-dominated diets would consume fruits with greater

protein and lipid content rather than those with high sugar content (Snow, 1971; Crome,

1975; McKey, 1975; Howe, 1977; Howe and Estabrook, 1977; Stiles, 1993).

Subsequent studies have shown patterns that are inconsistent with this prediction

(Fuentes, 1994; Sun et al., 1997; Witmer and Van Soest, 1998). This may be due to

interspecific variation in factors that influence the net nutritional value of fruit, such as

frugivore digestive adaptations (Martínez del Rio and Restrepo, 1993) and plant

secondary compounds (Cipollini and Levey, 1997). However, it may be reasonable to

expect that highly frugivorous species, and particularly obligate frugivores such as the

Australian fruit-doves (Crome, 1975; Frith 1982; Recher et al., 1995), would need to

consume fruits with certain energetic or nutritional values to satisfy their requirements

(White, 1993; Morton, 1973; Izhaki and Safriel, 1989; Bairlein, 1996). This may

generate variation among frugivore species in the plant species that they consume. For

example, highly frugivorous bird species are associated with the consumption of plants

from the Lauraceae, a family noted for its high lipid content (Snow, 1971, 1981; Crome,

1975; Wheelwright, 1983; Stiles, 1993). Frugivore species that have mixed diets can

69

obtain nutrition from other food sources, most of which are rich in protein and other

nutrients compared with fruit (Morton, 1973; Izhaki and Safriel, 1989). Consequently,

the plant species composition of frugivore diets may vary among frugivore species

depending on their degree of dependence on fruit. Furthermore, the species richness and

volume of fruits consumed by a bird species may be positively related to its degree of

frugivory (Wheelwright et al., 1984), although Pratt and Stiles (1985) proposed that

mixed-diet species were less selective and therefore would consume a wider variety of

plant species.

The identification of groups of functionally distinct frugivore species may make

it possible to forecast consequences of changes in frugivore assemblage composition for

seed dispersal. For example, it has been predicted that declined abundance of certain

frugivorous bird species in fragmented rainforest may result in declining plant

populations in fragmented landscapes (Howe, 1984; Crome 1990; Janzen and Vasquez-

Yanez, 1991; Corlett, 1998; Sodhi et al., 2004; Terborgh and Nuñez-Iturri, 2006). In

particular, it has been proposed that the dispersal of large-seeded plant species will be

limited in fragmented rainforest regions throughout the world (Corlett, 1996, 1998;

Harrington et al,. 1997; Silva and Tabarelli, 2000; Kitamura et al., 2002; McConkey and

Drake, 2002).

Chapter Two described the changes in the frugivorous bird assemblage resulting

from either declined or increased numbers of individual species in fragmented

compared with extensive rainforest in a subtropical region of Australia. The present

chapter asseses the potential functional role of different frugivorous bird species in the

dispersal of seeds from rainforest plants. The approach employed considers variation

among frugivore species in their dietary preferences to be the primary dimension of

functional variation among disperser species.

70

Bird species are categorised into functional groups using information about their

gape width, frugivory level and seed-crushing behaviour. It is proposed that this

approach assembles groups of bird species that potentially disperse a similar suite of

plant species. Data from the field study of bird distribution in the Sunshine Coast region

(Chapter Two) is used to compare between these functional groups in terms of their

numbers in rainforest remnants and regrowth, relative to extensive forest. The extent to

which seed dispersal may vary between forested and fragmented parts of the landscape

as a consequence of functional variation among frugivorous bird species is considered.

3.2 Methods

Chapter Two describes the study region (Section 2.2.1) and site network (2.2.2),

field surveys of bird species abundance (2.2.3), and the classification of the 42

frugivorous bird species (2.2.5). The different abundance patterns that were detected

among frugivorous bird species are detailed in Section 2.3.1 in Chapter Two.

Note that the frugivore attribute data used in this chapter are used in analyses in

Chapter Four.

3.2.1 Assessment of the functional attributes of frugivorous bird species: gape width,

frugivory level and seed-crushing behaviour

Vernier callipers were used to measure (to 0.01 mm) the gape width (width of

the bill at the junction of the upper and lower mandibles) of skin specimens kept in the

Queensland Museum. There may have been some shrinkage of specimens, but this is

should be proportional across species. Measurements were taken from 10 individuals of

each species, except for the Australian king-parrot Alisterus scapulatus for which only

nine specimens were available. Specimens collected from the vicinity of the study area

(i.e. southeast Queensland) were measured where possible. Where there was probably

71

sexual dimorphism in gape width, measurements were taken from five male and five

female specimens. Fruit-doves and the topknot pigeon have a peculiar gape morphology

which enables gape distension (Crome and Shields, 1992). To quantify the extent of this

distension, the closed gape width was measured (as for dried specimens) from two

thawed specimens of the wompoo fruit-dove and one of the rose-crowned fruit-dove

that had been frozen fresh (hence the inter-mandibular flesh was intact) and then

compared with the maximum width of a plasticine ball that could be swallowed by the

specimens. The distension was similar for both species (25%) and this value was used to

augment the average width of measurements taken from skins for the fruit-doves and

topknot pigeon.

Each bird species was allocated to one of three diet groups, reflecting the

relative dominance of fleshy fruit in their diets: major (fruit-dominated diet), mixed

(diet comprising two to several main food types, one of which was fruit), and minor

(diet dominated by foods other than fruit, but occasionally including fruit). These

categories were determined from descriptions in the literature (Blakers et al. (1984) and

the Handbook of Australian, New Zealand and Antarctic Birds (HANZAB) series

(Marchant and Higgins, 1993; Higgins and Davies, 1996; Higgins, 1999, Higgins et al.,

2001)) and in discussion with experts. Dietary descriptions in the literature were usually

qualitative but sufficiently consistent to enable the allocation of species to a relative

level of frugivory.

Bird species that potentially destroy seeds were identified from references in the

literature to the destruction of seeds during feeding, grinding-based digestion, or

detection of crushed seeds in faecal samples (Blakers et al., 1984; Crome and Shields,

1992; and the HANZAB series). Seed-crushing bird species were considered to have

low potential as seed dispersers relative to other frugivorous birds, although some seeds,

particularly if very small or hard, may pass through the bird’s gut intact (Snow, 1981).

72

Bird species for which seed-crushing behaviour was not mentioned were considered to

generally disperse viable seed, although it is recognised that even birds that do not crush

seeds may not always function as effective dispersers, for example if they consume the

flesh of a fruit but not the seed (“fruit-thieving”) (Green, 1993).

3.2.2 Data analyses

To establish whether a bird species’ frugivory level, gape size and seed

treatment were confounded with one another, pair-wise and three-way interactions were

tested using a log linear model in the statistical package SPSS (2001). The factors were

frugivory level (three levels, major (1), mixed (2) and minor (3)), gape width classes

(three levels, small (<10 mm), medium (10 – 15 mm) or large (>15 mm)) and seed

treatment (two levels, seed-disperser and seed-crusher). The data were the number of

bird species (total 42) within each cell of the three-way table of factors.

Each of the 42 bird species recorded during the field study was classed into one

of the following seven functional groups based on combinations of the measured

attributes of seed treatment, gape width and frugivory level. All seed-crushing bird

species were grouped together (as group 8) since the seed dispersal potential of these

birds is likely to be similarly low, irrespective of gape width and frugivory level. Seed-

dispersing birds (species that do not crush seeds) were allocated to the following

groups:

1. large-gaped (>15 mm) with fruit-dominated diet;

2. medium-gaped (10-15 mm) with fruit-dominated diet;

3. large-gaped with mixed diet;

4. medium-gaped with mixed diet;

5. small-gaped (<10 mm) with fruit-dominated diet;

6. small-gaped with mixed diet; and

73

7. fruit a minor dietary component (all gape widths pooled).

The abundance of birds within each functional group was calculated by

summing the data for all species comprising each group, including those species that

were too uncommon for individual analysis (recorded in less than five sites during

summer and winter surveys; Chapter Two, Section 2.3.1). One-way ANOVA, together

with Least Significant Difference (LSD) tests, were conducted using SPSS (2001) to

test for differences in the abundance of each functional group, between extensive,

remnant and regrowth sites.

The eight functional groups described above were further combined to form

three groups that are proposed to differ substantially in their influence on overall seed

dispersal dynamics; functional groups 1- 3 (likely to have high influence), 4 - 6

(medium), and 7 - 8 (low). An association between these three groups and sensitivity to

forest fragmentation, as indicated by decreasing (1), tolerant (2) or increasing (3)

abundance patterns, was tested using Spearman’s rank correlations in SPSS (2001).

Multidimensional scaling ordination using the semi-strong hybrid technique

(Faith et al. 1987) in WinPATN (Belbin et al., 2003) was used to describe differences

among the 48 sites in terms of patterns of variation in functional group composition.

Data for 39 bird species were included in these analyses; three species that were

detected at only one site (rock dove, blue-faced honeyeater and house sparrow) were not

included. Principal axis correlations were conducted to determine associations between

the site ordination and the abundance of each functional group; associations found to be

significant (at p< 0.05) using a randomisation test (MCAO, 10 000 iterations) were

displayed as functional group abundance vectors in the ordination space.

74

3.3 Results

3.3.1 Variation in seed dispersal potential among species within the frugivorous bird

assemblage

The 42 frugivorous bird species that occur in rainforest habitats in the Sunshine

Coast, along with their gape width, frugivory level and seed-crushing behaviour, are

shown in Table 3.1. Just over one-third (15) of these species destroy seeds by crushing

or grinding them. Species’ gape widths ranged from 5.2 mm (scarlet honeyeater) to 32.8

mm (channel-billed cuckoo) (Table 3.1). There were nine species with small (<10 mm)

gapes, 15 with medium (10 – 15 mm) gapes, and 18 with large (>15 mm) gapes. Eleven

bird species had fruit-dominated diets (major frugivores), 15 had mixed diets and 16 had

diets dominated by food types other than fruit (minor frugivores). None of the

interactions between frugivory level, gape width and seed treatment were significant in

the Loglinear model (loglinear model likelihood ratio (L.R.) χ2 = 6.38, p = 0.90 for

three-way interaction; pair-wise chi-squared tests showed no interaction between gape

width and frugivory level (χ2 = 0.38, p = 0.98), frugivory level and seed treatment (χ2 =

0.82, p = 0.66), nor gape width and seed treatment (χ2 = 2.51, p = 0.29) (Figure 3.1).

75

Tab

le 3

.1 C

hara

cter

istic

s an

d re

spon

se p

atte

rn o

f fru

givo

rous

bird

spe

cies

rec

orde

d in

the

field

stu

dy. S

eed

trea

t. in

dica

tes

seed

trea

tmen

t (C

=

crus

her,

D =

dis

pers

er).

The

abu

ndan

ce o

f ind

ivid

uals

rec

orde

d in

1 h

a (a

vera

ged

acro

ss fo

ur s

urve

ys)

is s

how

n fo

r ex

ten

sive

(N

=16

), r

emna

nt

(N=

16)

and

regr

owth

(N

=16

) si

tes.

No.

site

s sh

ows

the

num

ber

of s

ites

(max

imu

m 4

8) a

t whi

ch th

e sp

ecie

s w

as r

ecor

ded

(sum

me

r pl

us w

inte

r

surv

eys)

. R

espo

nse

patte

rn s

how

s th

e ab

unda

nce

patt

ern

in r

elat

ion

to fo

rest

frag

men

tatio

n (b

ased

on

anal

yses

in C

hapt

er T

wo:

D =

dec

reas

er, I

=

incr

ease

r, T

= to

lera

nt, a

nd U

= u

ncer

tain

(i.e

. to

o ra

re fo

r st

atis

tical

ana

lysi

s).

Sci

enti

fic

nam

e 1

Co

mm

on

nam

e 1

See

d

trea

t.

Gap

e w

idth

(m

m) 2

Gap

e cl

ass 3

F

rug

ivo

ry

leve

l 4

Ext

ensi

ve

Rem

nan

t R

egro

wth

N

o.

site

s R

esp

on

se

pat

tern

A

lect

ura

lath

ami

Aus

tral

ian

brus

h-tu

rke

y

C

18.3

(0.

5)

L M

ixed

0.

56

1.38

1.

06

23

T

Col

um

ba li

via

rock

dov

e *

+

C

10.2

(0.

4)

M

Min

or

0.00

0.

00

0.13

1

U

C. l

euco

mel

a w

hite

-hea

ded

pig

eon

C

11

.8 (

0.4)

M

M

ajor

0.

56

1.50

2.

13

22

T

Mac

ropy

gia

am

boi

nens

is

bro

wn

cuck

oo-d

ove

C

10.1

(0.

3)

M

Maj

or

4.81

6.

31

2.44

42

D

C

halc

opha

ps in

dica

em

eral

d do

ve

C

8.

5 (0

.2)

S

Maj

or

0.38

0.

94

0.63

15

T

G

eope

lia h

um

era

lis

bar-

shou

lder

ed d

ove

C

6.

6 (0

.4)

S

Min

or

0.00

1.

38

1.56

23

I

Leuc

osar

cia

mel

ano

leuc

a w

on

ga p

ige

on

C

9.

3 (0

.3)

S

Mix

ed

0.50

0.

06

0.00

5

U

Ptil

inop

us m

ag

nific

us

wo

mp

oo fr

uit-

dov

e

D

19.0

(0.

6)

L M

ajor

5.

25

1.81

0.

31

25

D

P. s

uper

bus

supe

rb fr

uit-

dove

D

12

.6 (

0.3)

M

M

ajor

0.

56

0.31

0.

06

13

D

P. r

egin

a ro

se-c

row

ne

d fr

uit-

dove

D

11

.5 (

0.3)

M

M

ajor

3.

38

2.23

0.

81

36

D

Lop

hola

imus

ant

arct

icus

to

pkno

t pig

eon

D

17

.5 (

0.5)

L

Maj

or

1.06

0.

06

0.63

6

T

Cac

atu

a ro

seic

apill

a ga

lah

C

15

.5 (

0.2)

L

Min

or

0.00

0.

13

0.25

3

U

C. g

aler

ita

sulp

hur-

cres

ted

cock

atoo

C

22

.9 (

0.4)

L

Min

or

1.50

0.

44

0.38

16

T

T

richo

glos

sus

hae

mat

odus

ra

inbo

w lo

rikee

t C

12

.2 (

0.1)

M

M

inor

2.

75

2.69

7.

31

32

I T

. chl

orol

epi

do

tus

scal

y-br

eas

ted

lorik

eet

C

11

.3 (

0.2)

M

M

inor

0.

13

0.69

0.

56

7 U

A

liste

rus

scap

ular

is

Aus

tral

ian

kin

g-p

arro

t C

17

.4 (

0.3)

§

L M

ixed

0.

56

0.26

0.

32

23

T

Pla

tyce

rcus

ele

gans

cr

imso

n ro

sella

C

14

.4 (

0.2)

M

M

ixed

0.

31

0.06

0.

00

4 U

P

. ads

citu

s pa

le-h

ead

ed r

ose

lla

C

12.1

(0.

2)

M

Mix

ed

0.25

0.

94

1.31

14

T

E

udyn

amys

sco

lopa

cea

com

mon

ko

el

D

18.2

(0.

2) §

L

Maj

or

0.38

0.

38

0.69

17

T

S

cyth

rops

nov

aeh

olla

ndi

ae

chan

nel-

bille

d cu

ckoo

D

32

.8 (

0.6)

L

Maj

or

0.06

0.

19

0.25

7

T

Ant

hoch

aera

chr

ysop

tera

lit

tle w

attle

bird

D

9.9

(0.1

) S

M

inor

0.

00

0.19

0.

25

6 T

P

hile

mon

cor

nicu

latu

s no

isy

fria

rbird

D

11

.5 (

0.4)

M

M

inor

0.

06

0.00

0.

44

3 U

E

nto

myz

on

cyan

otis

bl

ue-

face

d ho

ne

yeat

er +

D

13

.1 (

0.4)

M

M

inor

0.

00

0.13

0.

00

1 U

M

anor

ina

me

lano

ceph

ala

no

isy

min

er

D

10.2

(0.

3)

M

Min

or

0.00

0.

00

0.38

3

U

Mel

ipha

ga le

win

ii le

win

’s h

one

yeat

er

D

10.5

(0.

2)

M

Mix

ed

8.00

8.

75

7.63

48

T

M

yzo

mel

a sa

ngu

inol

enta

sc

arle

t ho

neye

ater

D

5.2

(0.1

) S

M

inor

1.

56

1.69

1.

25

32

T

Cor

acin

a n

ova

eho

lland

iae

blac

k-fa

ced

cuck

oo-s

hrik

e

D

17.4

(0.

2)

L M

inor

0.

13

0.06

1.

88

10

I C

. lin

eat

a ba

rred

cuc

koo-

shrik

e +

D

13.5

(0.

2)

M

Mix

ed

0.00

0.

00

0.14

2

U

76

Tab

le 3

.1 (

con

t.)

Sci

enti

fic

nam

e 1

Co

mm

on

nam

e 1

See

d

trea

t.

Gap

e w

idth

(c

m) 2

Gap

e cl

ass 3

F

rug

ivo

ry

leve

l 4

Ext

ensi

ve

Rem

nan

t R

egro

wth

N

o.

site

s R

esp

on

se

pat

tern

La

lage

leuc

om

ela

varie

d tr

iller

D

9.1

(0.2

) S

M

ixed

0.

06

0.13

0.

06

4 U

O

riolu

s sa

gitta

tus

oliv

e-ba

cked

ori

ole

D

15

.8 (

0.3)

L

Mix

ed

0.00

0.

00

0.13

2

U

Sph

ecot

here

s vi

ridis

fig

bird

D

17

.8 (

0.3)

L

Maj

or

2.56

7.

50

15.6

3 41

I

Cra

ctic

us to

rqua

tus

gre

y bu

tch

erbi

rd

D

15.3

(0.

2)

L M

inor

0.

00

0.00

0.

38

4 U

G

ymno

rhin

a tib

icen

A

ustr

alia

n m

agpi

e D

18

.5 (

0.2)

L

Min

or

0.13

2.

06

5.25

26

I

Str

eper

a gr

acu

lina

pie

d cu

rra

wo

ng

D

20

.1 (

0.4)

L

Mix

ed

2.75

4.

25

3.00

38

T

P

tilor

is p

arad

iseu

s pa

radi

se r

ifleb

ird

D

16

.7 (

0.3)

§

L M

ixed

0.

50

0.13

0.

00

5 U

C

orvu

s or

ru

Tor

resi

an c

row

D

19

.5 (

0.2)

L

Min

or

1.44

2.

25

5.13

35

I

Ailu

roed

us c

rass

irost

ris

gree

n ca

tbir

d

D

19.5

(0.

2)

L M

ixed

3.

75

4.63

0.

75

35

D

Ser

icul

us c

hrys

ocep

halu

s re

gent

bo

we

rbir

d

D

13.9

(0.

4) §

M

M

ixed

0.

13

0.06

0.

13

5 U

P

tilon

orhy

nchu

s vi

olac

eus

satin

bo

we

rbird

D

18

.5 (

0.2)

§

L M

ixed

0.

19

0.19

0.

50

7 T

P

asse

r do

mes

ticus

ho

use

spar

row

* +

C

8.6

(0.1

) S

M

inor

0.

00

0.00

0.

19

1 U

D

icae

um

hir

undi

nac

eum

m

istle

toe

bird

D

6.9

(0.1

) S

M

ajor

0.

19

0.00

0.

13

5 U

Z

oste

rops

late

ralis

si

lver

eye

D

6.0

(0.2

) S

M

ixed

1.

06

1.69

6.

25

20

I 1 N

omen

cula

ture

and

bir

d sp

ecie

s or

der

afte

r C

hris

tidis

and

Bol

es (

1994

). *

nex

t to

com

mon

nam

e de

note

s in

trod

uced

spe

cies

; + sh

ows

spec

ies

excl

uded

fro

m m

ultiv

aria

te a

naly

ses

(pre

sent

in o

nly

1 si

te)

2 M

ean

(and

sta

ndar

d er

ror)

, N=

10 e

xcep

t Aus

tral

ian

Kin

g P

arro

t (N

=9)

; inc

lude

s ad

just

men

t for

fru

it-do

ves

and

Top

knot

Pig

eon

(see

text

). §

sho

ws

spec

ies

that

may

hav

e se

xual

ly

dim

orph

ic g

ape

wid

ths.

3 S

= S

mal

l (<

10 m

m),

M =

Med

ium

(10

-15

mm

), L

= L

arge

(>

15 m

m).

4 M

ajor

indi

cate

s fr

uit-

dom

inat

ed d

iet,

Mix

ed is

a m

ixed

die

t tha

t inc

lude

s fr

uit,

Min

or in

dica

tes

that

fru

it is

a r

elat

ivel

y m

inor

die

tary

com

pone

nt.

77

.

Figure 3.1 Inter-relationships between frugivorous bird attributes; i) the number of

seed-crushing and seed-dispersing bird species from each frugivory level (major n=11,

mixed-diet n=15, and minor n=12); ii) the number of seed-crushing and seed-dispersing

bird species from each gape width class (small n=6, medium n=15, and large n=17);

and iii) the actual gape width of each bird species in major, mixed-diet and minor

frugivory levels

0

4

8

12

16

Major Mixed Minor

Frugivory level

No

. fru

giv

ore

sp

eci

es Disperser

Crusher

0

4

8

12

16

20

Small Medium Large

Gape width class

No

. fru

giv

ore

sp

eci

es Disperser

Crusher

0

10

20

30

40

Gap

e w

idth

(m

m)

Frugivory

Major Mixed Minor

78

3.3.2 Functional group abundance in remnants and regrowth relative to extensive

forest

The abundance of two functional groups (medium-gaped birds with fruit-

dominated diets and large-gaped birds with mixed diets) showed a decreasing response

to fragmentation and two groups (small-gaped, mixed-diet birds and minor frugivores)

showed an increaser abundance pattern (Table 3.3). The remaining four functional

groups showed a tolerant abundance pattern, although both seed-crushers and the large-

gaped, major frugivore group showed an increasing trend that was not statistically

significant.

Table 3.2 The mean (and S.E.) abundance of frugivorous bird species within each of

the eight functional groups in extensive (n=16), remnant (n=16) and regrowth (n=16)

forest in southeast Queensland.

Functional group 1 Extensive Remnant Regrowth ANOVA p 2 Abund. pattern3

1. Large gape, fruit-dominated diet (5)

9.31 (1.69) 9.94 (1.60) 17.50 (3.84) 0.06 T

2. Medium gape, fruit-dominated diet (2)

3.94 (0.62)a 2.44 (0.35)b 0.88 (0.30)c <0.0001 D

3. Large gape, mixed diet (5) 7.19 (0.88)a 9.19 (1.18)a 4.38 (0.85)b 0.005 D 4. Medium gape, mixed diet (3) 8.13 (0.50) 8.81 (0.63) 7.94 (0.60) 0.54 T 5. Small gape, fruit-dominated diet (1)

0.19 (0.10) 0.00 0.13 (0.09) 0.22 T

6. Small gape, mixed diet (2) 1.13 (0.49)a 1.81 (0.97)a 6.31 (1.70)b 0.005 I 7. Fruit a minor dietary component (all gape width classes) (9)

3.31 (0.67)a 6.38 (1.13)a 14.94 (1.66)b <0.0001 I

8. Seed-crushers (all gape width classes and frugivory levels) (15)

13.19 (1.29) 17.50 (1.76) 18.50 (1.87) 0.07 T

1 The number of species in each group is shown in brackets next to group name. The species comprising

each group are shown in Table 3.2. 2 Results of ANOVA between site types (d.f. = 2, 47). Groups differing significantly in abundance

(p<0.05) are given different letters. 3 The response to fragmentation for each group (D=decreaser, T=tolerant, I=increaser, see Chapter Two

for description of patterns).

There was a positive association between a species’ seed dispersal potential and

its sensitivity to forest fragmentation and disturbance (Spearman’s r = 0.39, p = 0.049).

Bird species making a relatively high potential contribution to seed dispersal tended to

show decreaser or tolerant abundance patterns, while bird species considered to have

79

relatively low dispersal potential mostly had tolerant or increaser abundance patterns

(Table 3.3).

Table 3.3 Relationship between frugivorous bird species’ abundance pattern and their

relative seed dispersal potential. Only bird species that were sufficiently frequent during

field surveys to determine an abundance response pattern (26 out of the 42 species)

are included. ‘ Disp.pot.’ is relative influence over seed dispersal dynamics.

Number of species showing abundance pattern1

Disp. pot. Functional groups2 Decreaser Tolerant Increaser High 1, 2 and 3 4 5 1

Medium 4 and 6 0 1 1

Low 7 and 8 1 8 5 1 see Table 3.1 for species’ abundance pattern data and functional attributes 2 see Table 3.2 for explanation of functional group attributes

Ordination of the study sites based on frugivore abundance at the functional

group level showed extensive forest and regrowth sites tending to cluster at opposite

extremes of the ordination space (Figure 3.2). The three site types differed significantly

in terms of functional group abundance (ANOSIM global p<0.01). Pair-wise tests

showed that regrowth sites differed from both extensive and remnant sites (ANOSIM

p<0.01 for both), but that extensive and remnant sites were not substantially different

(p=0.06). The two functional groups significantly associated with the region of the

ordination containing extensive and some remnant forest sites (Figure 3.2) were those

that that showed decreasing abundance patterns with fragmentation (Table 3.2). The

four groups associated with regrowth sites comprised two ‘increaser’ and two ‘tolerant’

functional groups.

80

Figure 3.2 Ordination of the 48 study sites based on numbers of birds from each

functional group (Stress = 0.22). is extensive forest, is remnants, is regrowth.

The lower panel shows abundance vectors for those functional groups significantly

(p<0.05) associated with the ordination.

Medium-gaped, major frugivores

Minor frugivores

Crushers

Small-gaped, mixed-diet frugivores

Large-gaped, major frugivores

Large-gaped, mixed-diet frugivores

81

3.4 Discussion

3.4.1 Characteristics of the frugivorous birds assemblage

Approximately one-third of the 42 frugivorous bird species recorded in these

surveys crush seeds. This is a similar proportion of the frugivorous bird assemblage as

that recorded in the Neotropics (Terborgh 1986). Seed-crushing species included several

species of parrot, plus certain doves and pigeons, such as the white-headed pigeon and

brown cuckoo-dove. Birds that crush seeds probably contribute relatively little to seed

dispersal, although a small proportion of ingested seeds may remain intact following

passage through the gut of these species (Snow 1981; Corlett, 1998; Dennis and

Westcott, 2006).

Of the 27 seed-dispersing bird species identified, seven species may also

contribute comparatively little to broad patterns of seed dispersal, since fleshy fruits are

only a minor component of their diets. The 20 remaining species do not crush seeds and

have either fruit-dominated or mixed diets in which fruit is a conspicuous component.

These birds would have most influence over seed dispersal dynamics in the study

region, although some species were recorded in low numbers during surveys.

In the frugivore assemblage studied, there was no consistent association between

any of the measured functional attributes. The positive association between gape size

and dietary dominance of fruit that had been reported elsewhere (Fuentes 1994) was not

apparent in this assemblage.

3.4.2 Functional characteristics of the frugivorous bird assemblage in fragmented

rainforest in subtropical Australia: assessment of potential consequences for

seed dispersal

The frugivore attributes of seed crushing behaviour, gape width and frugivory

level were used to describe groups of species that may have similar functional roles in

82

terms of their capacity to disperse the seeds of similar plants, especially plants with

similar-sized diaspores. This dimension of functional variation among frugivore species

is useful in assessing whether changes in the species composition of a frugivore

assemblage may result in the loss of potential dispersal agents for certain plant species

(e.g., Silva and Tabarelli, 2000). In addition to dietary composition, variation among

frugivore species in factors such as their abundance in a habitat, feeding rates, dispersal

distances and patterns of microhabitat use is likely to lead to variation in their role as

seed dispersers (Schupp, 1993; Jordano and Schupp, 2000; Loiselle and Blake, 2002).

The functional groupings were not assembled using specific dietary information,

but the attributes used to form the groups have been linked with dietary composition

(Crome, 1975, 1978; Moermond and Denslow, 1983, 1985; Wheelwright, 1985;

Moermond et al., 1986; Whelan and Willson, 1994). All but one of the groups formed

using these attributes were multispecific, indicating functional overlap and the potential

for substitution among frugivore species (Loiselle and Blake 2002). The only functional

group with a single member (the mistletoebird) was the small-gaped, fruit-dominated

diet group. This species is likely to have a different diet to most other frugivore species

in that it is largely restricted to fruits from mistletoe plants (Loranthaceae). However,

other bird species may also be efficient and effective dispersers of seeds from these

plants (Reid, 1989), and the importance of mistletoe as food for the mistletoebird may

be disproportionate to the importance of the mistletoebird as a disperser of mistletoe, as

has been described for other frugivore-plant interactions (Herrera, 1984; Jordano, 1987;

Silva et al., 2002).

In the context of changes in the frugivore assemblage in fragmented landscapes,

functional overlap may mean that the decline of one frugivore species may be offset by

increased numbers of a functionally similar bird species. Dispersers of large fruited

plants are vulnerable to decline in tropical fragmented landscapes throughout the world

83

(Corlett, 1996, 1998; Harrington et al,. 1997; Silva and Tabarelli, 2000; Kitamura et al.,

2002; McConkey and Drake, 2002). Foraging observations at large-seeded plant species

suggest that this may also be the case in subtropical rainforests of southeast Queensland

(Green, 1993). Approximately 30% of the species comprising the avian frugivore

assemblage of subtropical Australia (14 out of 42 of the species considered in this

study) have wide gapes (>15 mm). Four of these species are minor frugivores and may

make relatively little contribution to the dispersal of these plants. A similar percentage

(24%) of the frugivorous bird species had gapes wider than 15 mm in the Brazilian

Atlantic (Silva and Tabarelli, 2000).

However, the overall abundance of the functional group that may have the

greatest potential to disperse large-seeded plants (large-gaped, major frugivores) did not

decline in fragmented rainforest in the Sunshine Coast, and in fact showed a strong

tendency towards increasing in abundance in regrowth. This increasing tendency was

entirely due to the greatly increased abundance of the figbird in remnant, and

particularly in regrowth, sites, compared with extensive forest. Numbers of other bird

species from this functional group were either low and similar among site types (e.g.

common koel) or much lower in remnants (e.g. wompoo fruit-dove). Although fruit-

doves have been nominated as having the greatest potential among avian frugivores to

disperse large-seeded plants in subtropical Australian rainforests (Frith, 1982; Green,

1995), the present work has shown that figbirds are also morphologically capable of

dispersing large fruits. Consequently, the high abundance of figbirds in remnants and

regrowth habitats of the study region potentially maintains the dispersal of large-seeded

plant species in these parts of the landscape. Furthermore, other bird species with the

potential to disperse large-seeded plants (the topknot pigeon, pied currawong and satin

bowerbird) were also present in these habitats. Hence, in contrast to tropical landscapes

elsewhere, the loss or decline of bird species such as the wompoo fruit-dove from

84

fragmented subtropical Australian rainforest landscapes may not result in reduced

dispersal of large fruited plant species.

However, the functional group approach used here may overstate potential

similarity among frugivore species. For example, although the channel-billed cuckoo

has a large gape and fruit-dominated diet, available information suggests that their diet

may be dominated by figs (Blakers et al., 1984). Consequently, this species may not

contribute to the dispersal of large fruited plants, despite their very large gape. Second,

movement patterns and gut passage rates may mean that certain frugivore species do not

disperse seeds among fragmented habitats (Silva et al., 1996; Alcántara et al., 2000). In

the case of figbirds, radiotracking in northern Australia has shown that birds of this

species regularly fly distances of several kilometres between rainforest patches, and also

visit isolated trees (Price, 1999). Furthermore, aviary tests showed that the gut passage

times of figbirds resembled those of fruit pigeons (Price 1999). Therefore, the role of

figbirds in dispersing seeds within and among remnant and regrowth forests would

probably not be limited by restricted movement patterns nor by very rapid gut passage

times. Third, patterns of plant species consumption are likely to be influenced by a

frugivore species’ digestive adaptations (Levey and Grajal, 1991; Martínez del Rio and

Restrepo, 1993; Cipollini and Levey, 1997) and ability to handle secondary compounds

(Levey and Martínez del Rio, 2001). The relationship between these factors and

frugivory level is not known, although may be likely to be associated with taxonomy.

The two functional groups whose overall abundance decreased in remnants

and/or regrowth were large-gaped birds with mixed diets and medium-gaped birds with

fruit-dominated diets. An overall decrease in the dispersal of plants eaten by birds from

these two groups would be expected to result from declines of these functional groups.

The medium-gaped birds with fruit-dominated diets (superb and rose-crowned fruit-

doves) small fruit-doves may consume a suite of rainforest plants that is distinct from

85

other birds, even the closely-related wompoo fruit-dove. In a detailed dietary study of

these species in north Queensland, the superb and rose-crowned fruit-doves

predominantly consumed species from the family Araliaceae and from the lauraceous

genera Endiandra and Litsea, whereas the wompoo fruit-dove fed more on plants from

the family Elaeocarpaceae and the lauraceous genus Cryptocarya (Crome, 1975). All

three species were associated with extensive forest rather than remnant or regrowth sites

in the present study. It seems likely that the greatly reduced numbers of these birds in

fragmented and disturbed habitats would cause changes in the composition and rate of

seed dispersal in these habitats, even though the figbird replaces them numerically.

Numbers of the small-gaped, mixed diet functional group increased in regrowth

compared with remnant and extensive forest. This group comprised the varied triller and

the silvereye, although the increasing pattern was driven by numbers of the silvereye.

The plant species dispersed by these frugivores would be expected to increase in

fragmented rainforest landscapes of subtropical Australia. Consequently, the

regeneration trajectory of rainforest regrowth in fragmented parts of the landscape may

be strongly influenced by the plant species consumption patterns of these bird species.

If, as may be expected from their small size and mixed diet, these birds consume large

numbers of introduced weed species (Richardson et al., 2000), fragmented rainforest

may be overwhelmed by the input of fleshy-fruited weeds.

There was an overall positive association between a species’ seed dispersal

potential and the extent to which their abundance was negatively impacted in remnants

and regrowth. It was considered that birds with fruit-dominated diets and large or

medium gapes were likely to have a disproportionately high influence over general seed

dispersal patterns. Because these species are nutritionally dependent on fruit, they may

be likely to consistently eat a large volume of fruit and to need to feed on a range of

plant species to cope with the temporal variation in availability of any given species

86

(Leighton and Leighton, 1983). Since having a larger gape gives birds access to a

greater range of available fruits (Wheelwright 1985), it was also expected that large-

gaped birds with mixed diets may have relatively high seed dispersal potential. All

except one of the species (figbird) within these three functional groups showed either a

decreasing or tolerant abundance response to forest fragmentation and disturbance.

Consequently, it is predicted that the overall rate of seed dispersal may be lower, and

that fewer plant taxa plant taxa would be dispersed in remnants and regrowth than in

extensive forest. The plants that are predicted to be most likely to be affected by these

changes are large fruited plants and Lauraceae. Beyond this, predictive power is limited

by a lack of information regarding associations between frugivore traits and patterns of

consumption of plant species.

The approach presented here provides a means of systematically assessing

dispersal potential in relation to frugivore assemblage composition. As this has not

previously been done, specific dietary information is required to assess whether the

functional attributes selected do reflect major variation among frugivorous bird species

in their diet composition.

87

Chapter Four

Variation in patterns of plant species consumption by frugivorous bird

species is related to gape width, degree of frugivory and seed treatment

4.1 Introduction

A primary determinant of functional variation among frugivore species is the

suite of plant species that they consume and disperse (Gautier-Hion et al., 1985; Corlett,

1998; Hamann and Curio, 1999; Kitamura et al., 2002; Poulsen et al., 2002; Silva et al.,

2002). However, information on plant species consumption is extremely time-

consuming to collect and only limited information is available for most of the frugivore

species in an assemblage (Hamann and Curio, 1999; Kitamura et al., 2002; Silva et al.,

2002). In contrast, information regarding the morphology and behaviour of frugivore

species may be more easily gained (e.g, Dunning, 1993). These factors may influence

patterns of plant species consumption by interacting with variation in the traits of plant

species (e.g., fruit size) (van der Pijl, 1982; Gautier-Hion et al., 1985). Potentially,

information about the relevant traits of frugivore species may be used to assess their role

in seed dispersal when detailed dietary information is not available.

Functional classifications of frugivore species, which relate types of frugivores

to the types of plants they consume, are a step in the development of a predictive

understanding of seed dispersal interactions. Most studies of frugivore diets have

documented variation among only a subset of the frugivore or plant species in an

assemblage (e.g, Crome, 1975; Innis, 1989; Sun et al., 1997; Brown and Hopkins, 2002;

Kitamura et al., 2002). Consequently, our understanding of patterns of fruit-frugivore

interactions across frugivore communities is limited (Herrera, 1998, 2001). The

88

traditional approach of comparing among taxonomic groups (e.g., birds and mammals)

has yielded knowledge of broad patterns of dietary variation across a frugivore

community (Van der Pijl, 1982; Gautier-Hion et al., 1985; Bollen et al., 2004).

However, this approach obscures the variation among species within taxonomic groups

(Willson et al., 1989; Stiles, 1993; Graham et al., 2002; Lord et al., 2002). For example,

the gape width of frugivorous bird species imposes an intractable upper threshold on the

size of fruits that they can swallow (Herrera, 1981; Wheelwright, 1985). Consequently,

bird species with wider gapes are capable of consuming plant species with larger fruits

while bird species with narrow gapes are physically constrained to swallowing only

small fruits (Wheelwright, 1985; Silva and Tabarelli, 2000; McConkey and Drake,

2002; Kitamura et al., 2002). In Costa Rica, Wheelwright (1985) showed that the

maximum and mean size of fruits that were consumed by frugivorous bird species were

positively correlated with their gape widths.

Variation in patterns of plant species consumption by different frugivore species

may also be explained by variation in the energetic or chemical content of fruits

(Herrera, 1982, 1987; Stiles, 1993; Jordano, 1995; Cipollini and Levey, 1997).

Frugivore species vary in their capacity to digest plant toxins, lipids and sugars (Izhaki

and Safriel, 1989; Martínez del Rio and Restrepo, 1993; Cipollini and Levey, 1997).

Frugivore species also vary in their degree of nutritional dependence on fruit (Snow,

1971; McKey, 1975). Most frugivorous species eat fruit as part of a varied diet that also

includes other items, such as nectar or invertebrates. The tissues of non-fruit foods,

especially insects, are relatively rich in protein and other nutrients (Morton, 1973;

Herrera, 1987; Izhaki and Safriel, 1989). Frugivore species that only consume fruits, but

crush and digest seeds would obtain nutrition from the seeds as well as the fruit pulp

(Snow, 1981; Innis, 1989; Jones and Crome, 1990). However, fruit is the sole source of

nutrition for a small number of species. It has been proposed that these dietary

89

specialists may be likely to select fruits with relatively high energy and protein content

(Morton, 1973; McKey, 1975; Bairlein, 1996; Bosque and Calchi, 2003). For example,

it has been reported that highly frugivorous bird species prefer to consume lipid-rich

fruits (Snow, 1971; Crome, 1975; McKey, 1975; Howe and Estabrook, 1977; Howe,

1981; Wheelwright, 1983; Stiles, 1993). This may be because lipids provide more

energy than carbohydrates (Johnson et al., 1985; Witmer and Van Soest, 1998), or

because lipids tend to co-occur with high nitrogen levels (Sun et al., 1997).

In Chapter Three, it was proposed that gape width, frugivory level and seed

treatment were important functional attributes of frugivorous bird species because they

are likely to determine variation in the composition of plant species consumed by bird

species. In the present Chapter, actual patterns of plant species consumption by

frugivorous species are examined across the subtropical bird assemblage of eastern

Australia, in relation to the nominated attributes. This is made possible by a relatively

large published record of foraging information for the bird species of this region.

Specifically, tests are conducted for relationships between frugivore species’ gape

width, frugivory level and seed treatment and their patterns of fruit size consumption,

the dietary composition of plant species, and the frequency of specific plant families in

the diet. The results are used to assess whether the selected functional attributes are

useful indicators of differences among frugivorous bird species in their roles as seed

dispersers.

4.2 Methods

4.2.1 Diet composition of the frugivorous bird assemblage

In Chapter Two, 42 frugivorous bird species were identified in subtropical

rainforests of the Sunshine Coast, eastern Australia. Records of the consumption of

native plant species by these birds were obtained from 151 published sources (Appendix

90

1), together with several unpublished data sets (See Acknowledgements). Most records

had been obtained from opportunistic field observation of fruit consumption, although

some were from targeted surveys of particular plant or frugivore species. A small

number of records were obtained from bird gut contents. There was large variation

among bird species in the number of individual frugivory records available (i.e., the

total number of sources that had reported observations of frugivory). These ranged from

2 records for the galah to 228 for the satin bowerbird (including repeat observations of

the consumption of a given plant species by a bird species).

Foraging records included native and exotic species of tree, shrub, vine and herb

(Appendix 2). Because of the large geographic range of many of the bird species from

subtropical Australian rainforests, frugivory records may have been collected from a

region extending from temperate southern Australia (e.g., French, 1990) to tropical

Papua New Guinea (Frith et al., 1976). Records obtained from observation outside the

eastern Australian subtropics were included in analyses only if the plant species also

occurred within this region. The data set included records accumulated during a period

of more than 140 years, with the earliest account published by Gould (1865). For a

given frugivore species, the data potentially included foraging records from multiple

years, seasons and geographic locations. These records were compiled into a binary data

matrix containing the presence or absence of each fleshy-fruited plant species in the diet

of each of the frugivorous bird species.

Records were rejected if it appeared that the bird had not been observed actually

consuming the fruit (e.g., if it was simply observed in the fruiting plant), or if it was

judged from accompanying information that the interaction was an instance of fruit theft

(consumption of the fruit pulp without ingestion of the seed). Diaspore size (see below)

was used to further screen the records for likely cases of fruit theft; if the size of the

fruit greatly exceeded the gape width of the bird species, it was assumed that it would

91

only be capable of consuming part of the fruit and had probably acted as a fruit thief

(Howe and Estabrook, 1977). Cases were excluded if the median diaspore size was

more than twice the gape width of the frugivore species. This approach accounts for

potentially substantial intraspecific variation in diaspore size (Edwards, 2005). Each

record in the screened data set was treated as evidence of the potential for the bird

species to consume and disperse viable seed from the plant species.

For each plant species, diaspore size (the functional dispersal unit) was recorded.

For most plant species, the measurement was the shorter axis (usually diameter) of the

whole fruit. However, seed diameter was used for soft fruits with multiple small seeds

(e.g. many species in the Solanaceae and Moraceae) that can be dispersed as a result of

piecemeal consumption (Corlett, 1998; Kitamura et al., 2002). Similarly, for dehiscent,

arillate fruits such as Alectryon spp. (family Sapindaceae), the diameter of an individual

seed plus the fleshy aril was used. Diaspore size data were collected from published

literature (Williams et al., 1984; Floyd, 1989; Cooper and Cooper, 1994; Hauser and

Blok, 1998; Butler, 2003), supplemented with data from field collections (S. McKenna,

C. Moran) and biological web sites. In most cases, a range of diaspore size values was

reported and the median of these was used in analyses.

Diaspores with a median width greater than 75% of the gape width of a bird

species were considered to be close to the bird species’ morphological handling

capacity. This was used to calculate, for each bird species, the percentage of plant

species consumed that had diaspores close in size to the bird’s handling capacity.

4.2.2 Functional attributes of bird species

Four of the 42 bird species (scarlet honeyeater Myzomela sanguinolenta, house

sparrow Passer domesticus, rock dove Columba livia and Australian magpie

Gymnorhina tibicen) were rarely recorded consuming fruit of native plant species (less

92

than two native plant species recorded) and are therefore not considered further. The

remaining 38 bird species were categorised based on three attributes considered to

influence their patterns of fruit consumption in terms of plant species (see Chapter

Three). Gape width was measured on museum specimens of each bird species and

ranged from 6.0 mm (silvereye Zosterops lateralis) to 32.8 mm (channel-billed cuckoo

Scythrops novaehollandiae). For some analyses these data were used to group bird

species into three gape width categories: small (<10 mm), medium (10 – 15 mm), or

large (>15 mm). Each species’ degree of frugivory was classified into one of three

categories: 11 bird species had a fruit-dominated diet (‘major frugivores’), 15 had a diet

comprising more than one main food type, one of which was fruit (‘mixed-diet

frugivores’) and 12 had a diet dominated by food other than fruit, but which

occasionally included fruit (‘minor frugivores’). The relative level of dependence of

each bird species on fruit was determined primarily from qualitative descriptions in the

literature (Blakers et al., 1984; the Handbook of Australian, New Zealand and Antarctic

Birds (HANZAB) series: Marchant and Higgins, 1993; Higgins and Davies, 1996;

Higgins, 1999; Higgins et al., 2001). Each bird species was also categorised as being

either a seed-disperser or seed-crusher, based on information contained in the HANZAB

series about the destruction of seeds during either feeding (parrots, cockatoos) or

digestion (certain pigeon and dove species, Australian brush turkey). The measurement

and classification of frugivore attributes is explained in more detail in Chapter Three

(Section 3.2.1).

4.2.3 Data analyses

Tests to establish whether a bird species’ frugivory level, gape size and seed

treatment were independent of one another were described in Chapter Three (Section

3.2.2).

93

One-way analyses of covariance (ANCOVA) were used to test the effect of the

independent variable frugivory level (three levels: major (n=10 (the channel-billed

cuckoo was excluded from analyses)), mixed-diet (n=15) and minor (n=12)) on the

following dependent variables: i) the size of diaspores consumed; ii) the percentage of

diaspores consumed that were close to a bird species’ handling capacity (i.e., wider than

75% of its gape width); and iii) the total number of plant species consumed. Species’

gape widths (actual width in mm) were used as the covariate in analyses. Homogeneity

of regression slopes was tested using the interaction between frugivory level and gape

width.

Differences between major and mixed-diet frugivores in the number of species

consumed from plant families with at least three species represented in the data set were

tested using t-tests. A parametric procedure was used for families with >15 plant species

in the data set (three families), while randomisation (1 000 iterations) was used for the

25 plant families with 4 - 15 species represented (using the Pop-tools add-in in MS

Excel (Hood, 2003).

A classification tree for frugivore species, based on their dietary composition,

was generated using the UPGMA algorithm (Manly, 1994) and Bray-Curtis

dissimilarity metric in PRIMER (Clarke and Warwick, 2001). Plant species that had

been recorded in the diet of less than three frugivore species, and frugivores that had

been recorded consuming less than three plant species were excluded from all

multivariate analyses to reduce variation in the data. Multivariate analyses were

subsequently conducted on a data matrix containing information for 35 bird species and

151 plant species. Similarity percentages (SIMPER; Clarke, 1993) analyses were used

to identify the plant species that contributed most to the dissimilarity between these

groups.

94

4.3 Results

Frugivory level, gape width and seed treatment varied independently across the

38 bird species (Chapter Three, Section 3.3.1, Figure 3.1). Therefore, relationships

between each attribute and patterns of plant species consumption were tested

independently.

4.3.1 General patterns of plant consumption

The functional attributes and patterns of native plant species consumption of

frugivorous bird species are shown in Table 4.1. The data set relating bird species to

plant species contained information for 244 native plant species that had been consumed

by at least one of the 38 frugivorous bird species. There was considerable variation

between plant species in the suites of frugivore species that were known to consume

them. An average of 5.2 (S.E. 0.30) frugivorous bird species was recorded consuming

each native plant species (range 1 – 26 bird species).

95

Tab

le 4

.1 T

he f

unct

iona

l att

ribut

es a

nd p

atte

rns

of n

ativ

e pl

ant

spec

ies

cons

umpt

ion

of 3

8 fr

ugiv

orou

s bi

rd s

peci

es in

Aus

tral

ian

subt

ropi

cal

rain

fore

sts.

‘O.’

orde

r, ‘F

.’ fa

mily

. ‘F

rug.

lev.

’ fru

givo

ry le

vel;

‘Gap

e’ g

ape

wid

th; ‘

See

d tr

eat.

’ see

d tr

eatm

ent (

C s

eed-

crus

her,

D s

eed-

disp

erse

r),

‘No.

plan

t sp

p.’ t

he n

umbe

r of

nat

ive

plan

t sp

ecie

s re

cord

ed f

or e

ach

bird

spe

cies

; ‘A

v. d

ias.

siz

e.’ a

vera

ge s

ize

(mm

) of

dia

spor

es c

onsu

med

; ‘D

ias.

siz

e

rang

e’ s

how

s th

e m

inim

um a

nd m

axi

mum

siz

es o

f fru

its c

onsu

med

and

the

num

ber

of p

lant

spe

cies

with

dia

spor

es <

10

mm

and

≥ 1

0 m

m c

onsu

med

;

‘Per

c. ≥

75%

gap

e’ is

the

perc

enta

ge o

f th

e pl

ant

spec

ies

reco

rded

in th

e di

et o

f ea

ch b

ird s

peci

es w

ith d

iasp

ores

wid

er t

han

75%

of t

he

gape

wid

th;

and

‘Per

c. F

icu

s sp

p.’ i

s th

e pe

rcen

tage

of n

ativ

e pl

ant s

peci

es c

onsu

med

tha

t w

ere

from

the

gen

us F

icus

.

Dia

spo

re s

ize

ran

ge

2

Bir

d o

rder

, fam

ily1

Bir

d s

pec

ies1

Co

mm

on

nam

e1 F

rug

. le

v.

Gap

e (m

m)

See

d

trea

t.

No

. p

lan

t sp

p.

Av.

d

ias.

si

ze.

(mm

) m

in

max

N

o.

<10

No

. ≥ 10

Per

c ≥

75%

g

ape

Per

c F

icu

s sp

p.

O.

Gal

lifor

mes

F.M

egap

odi

iae

A

lect

ura

lath

ami

Aus

tral

ian

brus

h tu

rke

y M

ixed

18

.3

C

9 9.

44

1 27

.5

6 3

33

11

O. C

olum

bifo

rmes

F.C

olum

bida

e C

olu

mba

lecu

om

ela

w

hite

-hea

ded

pig

eon

Maj

or

11.8

C

39

9.

29

1 18

.5

19

20

59

8

Mac

ropy

gia

am

boi

nens

is

bro

wn

cuck

oo-d

ove

Maj

or

10.1

C

63

5.

48

1 12

.5

56

7 25

10

Cha

lcop

haps

indi

ca

emer

ald

dove

M

ajor

8

.5

C

9 6.

39

1 14

.5

6 3

44

33

G

eope

lia h

um

era

lis

bar-

shou

lder

ed d

ove

Min

or

6.6

C

3

2.83

1

4.0

3 0

0 33

Leuc

osar

cia

mel

ano

leuc

a w

on

ga p

ige

on

Mix

ed

9.3

C

9

6.65

1

14.0

5

4 44

33

Ptil

inop

s m

agni

ficus

w

om

poo

frui

t-d

ove

Maj

or

19.0

D

81

10

.01

1 27

.5

34

47

15

10

P

. sup

erbu

s su

perb

frui

t-do

ve

Maj

or

12.6

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26

9.

08

1 22

.5

13

13

54

12

P

. reg

ina

rose

-cro

wn

ed

frui

t dov

e M

ajor

11

.5

D

74

8.75

1

22.5

41

33

49

12

Lop

hola

imus

ant

arct

icus

to

pkno

t pig

eon

M

ajor

17

.5

D

73

10.2

5 1

27.5

31

42

23

10

O

. P

sitta

cifo

rmes

F.C

acat

uid

ae

Cac

atu

a ro

seic

apill

a ga

lah

Min

or

15.5

C

2

5.00

1

9.0

2 0

0 50

C

. gal

erita

su

lphu

r-cr

este

d co

ckat

oo

Min

or

22.9

C

11

7.

45

1 27

.5

9 2

9 10

F

.Psi

ttaci

dae

Tric

hogl

ossu

s ha

em

atod

us

rain

bow

lorik

eet

Min

or

12.2

C

12

5.

25

1 14

.0

10

2 17

33

T. c

hlor

ole

pid

otu

s sc

aly-

bre

aste

d lo

rike

et

Min

or

11.3

C

8

4.00

1

7.5

8 0

0 38

Alis

teru

s sc

apul

aris

A

ustr

alia

n ki

ng

par

rot

Mix

ed

17.4

C

59

7.

82

1 20

.0

37

22

8 5

P

laty

cerc

us e

lega

ns

crim

son

rose

lla

Mix

ed

14.4

C

42

7.

20

1 27

.5

31

11

24

10

P

. ads

citu

s pa

le-h

ead

ed r

ose

lla

Mix

ed

12.1

C

5

5.00

2

8.5

5 0

0 0

96

Tab

le 4

.1 (

con

t.)

D

iasp

ore

siz

e ra

ng

e2

Bir

d o

rder

, fam

ily1

Bir

d s

pec

ies1

Co

mm

on

nam

e1 F

rug

. le

v.

Gap

e (m

m)

See

d

trea

t.

No

. p

lan

t sp

p.

Av.

d

ias.

si

ze.

(mm

) m

in

max

N

o.

<10

No

. ≥ 10

Per

c ≥

75%

g

ape

Per

c F

icu

s sp

p.

O. C

ucul

iform

es

F

.Cuc

ulid

ae

Eud

ynam

ys s

colo

pace

a co

mm

on k

oel

M

ajor

18

.2

D

25

7.04

1

20.0

19

6

8 24

Scy

thro

ps n

ovae

hol

lan

dia

e ch

anne

l-bi

lled

cuck

oo

Maj

or

32.8

D

6

2.00

1

7.0

6 0

0 83

O

. P

asse

rifor

mes

F.M

elip

hag

ida

e A

ntho

chae

ra c

hrys

opte

ra

little

wat

tlebi

rd

Min

or

9.9

D

3

3.50

2

6.0

3 0

0 0

P

hile

mon

cor

nicu

latu

s no

isy

fria

rbird

M

inor

11

.5

D

2 7.

25

6 8.

5 2

0 0

0

Ent

om

yzo

n cy

anot

is

blu

e-fa

ced

hon

eye

ater

M

inor

13

.1

D

2 1.

00

1 1.

0 2

0 0

100

M

anor

ina

me

lano

ceph

ala

nois

y m

iner

M

inor

10

.2

D

7 4.

29

1 9.

0 7

0 29

43

Mel

ipha

ga le

win

ii Le

win

’s h

one

yeat

er

Mix

ed

10.5

D

10

6 6.

65

1 20

.0

82

24

32

9

F.C

ampe

pha

gid

ae

Cor

acin

a n

ova

eho

lland

iae

blac

k-fa

ced

cuck

oo-

shrik

e M

inor

17

.4

D

10

3.45

1

8.0

10

0 0

50

C

. lin

eat

a ba

rred

cuc

koo-

shrik

e M

ixed

13

.5

D

10

2.05

1

6.5

10

0 0

70

La

lage

leuc

om

ela

varie

d tr

iller

M

ixed

9

.1

D

10

4.50

1

8.5

10

0 20

30

F

.Art

amid

ae

Cra

ctic

us to

rqua

tus

gre

y bu

tch

erbi

rd

Min

or

15.3

D

3

4.83

4

6.0

3 0

0 0

S

trep

era

grac

ulin

a pi

ed c

urra

wo

ng

Mix

ed

20.1

D

50

8.

20

1 27

.5

32

18

6 20

F

.Par

adis

idae

P

tilor

is p

arad

iseu

s pa

radi

se r

ifleb

ird

Mix

ed

16.7

D

33

6.

57

1 17

.5

26

7 9

12

F.O

riolid

ae

Orio

lus

sagi

ttatu

s ol

ive-

back

ed o

riol

e M

ixed

15

.8

D

30

5.11

1

12.5

26

4

7 20

Sph

ecot

here

s vi

ridis

fig

bird

M

ajor

17

.8

D

74

7.11

1

18.5

52

22

7

14

F.C

orvi

dae

Cor

vus

orru

T

orre

sian

cro

w

Min

or

19.5

D

10

4.

15

1 9.

0 9

1 0

50

F.P

tilon

orh

ynch

idae

A

iluro

edus

cra

ssiro

stris

gr

een

catb

ird

Mix

ed

19.5

D

10

4 9.

08

1 35

.0

60

44

9 9

S

eric

ulus

chr

ysoc

epha

lus

rege

nt b

ow

erb

ird

Mix

ed

13.9

D

10

8 7.

62

1 27

.5

73

35

28

9

Ptil

onor

hync

hus

viol

aceu

s sa

tin b

ow

erb

ird

Mix

ed

18.5

D

10

6 8.

81

1 35

.0

58

48

10

8 F

.Dic

aeid

ae

Dic

aeu

m h

irun

din

aceu

m

mis

tleto

ebi

rd

Maj

or

6.9

D

6

4.33

1.

5 7.

0 6

0 33

0

F.Z

oste

ropi

dae

Z

oste

rops

late

ralis

si

lver

eye

M

ixed

6

.0

D

37

4.45

1

9.0

37

0 59

19

1 T

axon

omy

and

nom

encl

atur

e fo

llow

Chr

isti

dis

and

Bol

es (

1994

).

2 M

edia

n di

aspo

re s

ize

show

n. N

ote

that

ana

lyse

s as

sum

ed in

tra-

spec

ific

var

iati

on in

dia

spor

e si

ze to

a m

axim

um o

f 50

% la

rger

or

smal

ler

than

med

ian

size

.

97

4.3.2 The effect of gape width and frugivory level on diaspore size selection

The channel-billed cuckoo was removed from analyses relating to patterns of

diaspore size consumption, since it showed a strongly different pattern from other major

frugivore species; it predominantly consumed plants with very small diaspores (average

2 mm), despite its very large gape (32.8 mm; Table 4.1). This was a consequence of the

dominance of Ficus spp. in its diet (83%; Table 4.1). ANCOVA showed that the

average size of diaspores consumed varied significantly among the three frugivory

levels. Inspection of the data (Figure 4.1) showed that major and mixed-diet frugivores

consumed larger diaspores than minor frugivores (Figure 4.1; Table 4.2). The average

width (mm) of diaspores that was consumed by a bird species increased with its gape

width (mm) at a ratio of approximately 1:2 (Table 4.2; Figure 4.1). Frugivory level and

gape width together explained 74% of the variation in diaspore size consumption (eta

squared 0.43 and 0.31, respectively).

The consumption of plant species with diaspores that were close to the limit of a

bird species’ handling capacity was also influenced by frugivory level; minor frugivores

consumed a low dietary proportion of plant species with diaspores that were close to the

limit of their handling capacity (Figure 4.2, Table 4.2). The dietary proportion of these

fruits decreased with gape width (Table 4.2, Figure 4.2). Together, these two factors

explained 65% of the variation in consumption of diaspores that were close in size to

bird species’ handling capacity (eta squared 0.39 and 0.26 for frugivory level and gape

width, respectively).

98

Table 4.2 Results of ANCOVA tests for effects of gape width (G.w.) and frugivory level

(F.l.) on i) the average size of diaspores consumed (Dias. size); ii) the dietary

proportion of diaspores that were close to the limit of a bird species’ handling capacity

(Perc. >75% gape); and iii) the number of native plant species consumed (No. plant

spp.). ANCOVA showed homogeneity of regressions for each comparison (no

significant interaction between factors (F.l. x G.w.). β is the slope of the relationship

between gape width and the variable tested. The mean, number of cases, and strength

of regression (r2 ) is shown separately for each frugivory level in Figures 4.2 to 4.4.

Gape width (G.w.) Frugivory level

(F.l.) G.w. x F.l. Factor F p r2 β F p F p i) Dias. size 14.04 0.001 0.50 0.46 12.36 <0.0001 0.57 0.57 ii) Prop. ≥75% gape 1.48 0.002 0.50 -0.42 10.49 <0.0001 2.7 0.08 iii) No. plant spp. 4.36 0.045 0.40 0.28 8.53 0.001 0.83 0.44

Gape width (mm)

302520151050

Ave

rage

dia

spor

e si

ze

12

10

8

6

4

2

0

Minor

Mixed

Major

Figure 4.1 The average size of diaspores consumed compared with gape width for

major (n = 10, av. = 7.77, r2 = 0.36), mixed (n = 15, av. = 6.61, r2 = 0.42) and minor (n =

12, av. = 4.42, r2 = 0.16) frugivores.

99

Gape width (mm)

302520151050

Pro

p. s

peci

es

75%

gap

e w

idth

0.6

0.5

0.4

0.3

0.2

0.1

00.0

Minor

Mixed

Major

Figure 4.2 The average proportion of diaspores close to the maximum handling

capacity (≥ 75% of gape width) consumed by major (n = 10, av. = 0.31, r2 = 0.44),

mixed-diet (n = 15, av. = 0.20, r2 = 0.39) and minor (n = 12, av. = 0.04, r2 = 0.01)

frugivores.

4.3.3 Plant species richness of the diets of major, mixed and minor frugivores

The minimum number of native plant species recorded in the diet of a frugivore

species was two (galah, noisy friarbird and blue-faced honeyeater, all minor frugivores),

compared with a maximum of 128 (the mixed-diet Lewin’s honeyeater) (Table 4.1).

Major and mixed-diet frugivores consumed a higher average number of plant species

than minor frugivores (Table 4.2, Figure 4.3; eta squared 0.34). The relationship

between the number of native plant species consumed by a frugivore and its gape width

(approximately 3:1) was marginally significant (Table 4.2; eta squared 0.12). There was

large variation in the number of native plant species consumed by different major and

mixed-diet frugivore species (Figure 4.3). The frugivore species with low dietary plant

species richness tended to consume plants from a narrow range of plant taxa; for

example, the major frugivore mistletoebird mostly consumed plant species from the

≥

100

Loranthaceae and the mixed-diet barred cuckoo-shrike consumed a high dietary

proportion of Ficus spp. (70%; Table 4.1).

Gape width (mm)

302520151050

No.

nat

ive

plan

t spe

cies

120

100

80

60

40

20

0

Minor

Mixed

Major

Figure 4.3 The number of native plant species consumed by each frugivore in major (n

= 11, av. = 47.00, r2 = 0.35), mixed (n = 15, av. 47.87, r2 = 0.09) and minor (n = 12, av.

= 6.08, r2 = 0.24) frugivory levels.

4.3.4 Plant species diet composition in relation to frugivory level, gape width and seed

treatment

Almost half (104) of the 244 plant species in the data set were recorded in the

diet of both major and mixed-diet frugivores (but were not known to be consumed by

minor frugivores); a further 34 plant species were consumed by at least one frugivore

species from each of the three frugivory levels (Figure 4.4). Minor frugivores consumed

a subset of the plant species consumed by major and mixed-diet frugivores, except for a

single plant species (Melicope vitiflora Rutaceae). There were 32 and 65 plant species

known only from the diets of major or mixed-diet frugivores, respectively (Figure 4.4).

In most cases, these plant species were from families that were also known from the

101

diets of bird species from other frugivory levels, suggesting that these taxa may actually

be consumed by both major and mixed-diet bird species. However, all three of the plant

species in the data set that were from Agavaceae (all from the genus Cordyline) were

only known to be consumed by the mixed-diet regent bowerbird. The four species from

Celastraceae were also only known to be consumed by mixed-diet frugivores.

Figure 4.4 Overlap in the number of plant species consumed by frugivorous birds in

relation to frugivory level (major (n = 11, including channel-billed cuckoo), mixed-diet (n

= 15) and minor (n = 12) frugivores)

Only four plant species, all figs, were consumed by at least half of the 38 bird

species: Ficus macrophylla (consumed by 26 bird species), F. platypoda (25), F.

obliqua (23) and F. fraseri (21). At least two-thirds of the bird species had been

recorded consuming plant species from the families Moraceae, Euphorbiaceae,

Sapindaceae, Myrtaceae and Elaeocarpaceae, although few minor frugivore species

were known to consume these last two families (Table 4.3).

Major frugivores consumed higher numbers of native plant species from the

Lauraceae than mixed-diet species (Table 4.4). Mixed-diet frugivores consumed a

higher number of native plant species from the families Celastraceae, Mimosaceae,

Sapindaceae, Smilacaceae and Urticaceae.

Major

Mixed

Minor

32

65104

34

11

7

102

Table 4.3 The proportion of frugivorous bird species in each frugivory level that had

been recorded consuming native plant species from 40 of the plant families

represented in the data set1. Plant families that were consumed by at least half of the

bird species in a frugivory level are shown in bold. The total number of bird species that

was known to consume plant species from each family is also shown.

Proportion of frugivore species

Plant family No. plant spp.

Major (n=11)

Mixed-diet (n=15)

Minor (n=12)

Total no. frug.spp.

Agavaceae 3 0.00 0.13 0.00 2 Philesiaceae 2 0.00 0.20 0.00 3 Thymelaecae 2 0.09 0.20 0.00 4 Apocynaceae 2 0.00 0.27 0.11 5 Araceae 2 0.18 0.20 0.00 5 Celastraceae 4 0.00 0.33 0.00 5 Cucurbitaceae 3 0.18 0.20 0.00 5 Epacridaceae 3 0.09 0.20 0.11 5 Eupomatiaceae 2 0.18 0.20 0.00 5 Smilacaceae 3 0.09 0.27 0.00 5 Sterculiaceae 2 0.00 0.33 0.00 5 Menispermaceae 4 0.27 0.20 0.00 6 Myrsinaceae 3 0.18 0.27 0.00 6 Santalaceae 2 0.00 0.27 0.22 6 Sapotaceae 4 0.27 0.20 0.00 6 Icacinaceae 2 0.45 0.13 0.00 7 Symplocaceae 2 0.36 0.20 0.00 7 Rosaceae 4 0.27 0.33 0.00 8 Mimosaceae 3 0.09 0.53 0.11 10 Solanaceae 3 0.27 0.40 0.11 10 Pittosporaceae 4 0.36 0.47 0.00 11 Verbenaceae 5 0.36 0.40 0.00 11 Ebenaceae 4 0.64 0.33 0.00 12 Oleaceae 6 0.64 0.33 0.11 13 Rubiaceae 10 0.45 0.53 0.00 13 Urticaceae 3 0.18 0.53 0.22 13 Anacardiaceae 2 0.45 0.60 0.00 14 Vitaceae 6 0.64 0.47 0.00 14 Lauraceae 21 0.73 0.53 0.00 16 Ulmaceae 2 0.18 0.60 0.56 16 Rutaceae 11 0.64 0.60 0.11 17 Arecaceae 5 0.64 0.60 0.11 18 Araliaceae 4 0.73 0.67 0.11 19 Meliaceae 7 0.64 0.67 0.22 19 Rhamnaceaae 4 0.45 0.80 0.22 19 Elaeocarpaceae 6 0.73 0.73 0.11 20 Myrtaceae 20 0.91 0.53 0.22 21 Sapindaceae 17 0.64 0.80 0.67 26 Euphorbiaceae 11 0.82 0.80 0.67 28 Moraceae 13 0.91 0.87 0.78 31 1 The remaining 28 plant families represented in the data set had only been recorded in the diet of one frugivorous bird species

103

Table 4.4 The average number of native plant species from selected plant families that

were consumed by major and mixed-diet frugivores. Plant families with three or more

plant species in the data set were included. ‘No spp.’ shows the number of native plant

species from each family represented in the data set. ‘p’ shows the results of t-tests

comparing the number of plant species between major and mixed-diet frugivores;

significant (p<0.05) results are shown in bold. Statistical significance was determined

from randomisation for all plant families except Lauraceae, Myrtaceae and

Sapindaceae (see text).

Average no. plant spp. Plant family No.

spp. Major1 n = 8

Mixed1 n = 10

p

Araliaceae 4 1.63 1.60 0.38 Arecaceae 5 1.88 1.60 0.25 Celastraceae 4 0.00 0.60 0.005 Curcurbitaceae 3 0.25 0.40 0.58 Ebenaceae 4 1.25 1.20 0.85 Elaeocarpaceae 6 2.75 3.20 0.40 Epacridaceae 3 0.25 0.30 0.94 Euphorbiaceae 11 2.38 3.20 0.81 Lauraceae 21 9.88 4.80 0.04 Meliaceae 7 1.88 3.20 0.16 Menispermaceae 4 0.38 0.40 0.66 Mimosaceae 3 0.25 1.40 0.03 Moraceae 13 7.13 7.40 0.49 Myrsinaceae 3 0.38 0.40 0.58 Myrtaceae 20 4.13 5.50 0.26 Oleaceae 6 1.75 1.20 0.24 Pittosporaceae 4 0.50 0.80 0.17 Rhamnaceae 4 0.88 1.70 0.08 Rosaceae 4 0.63 0.90 0.57 Rubiaceae 10 1.13 1.70 0.45 Rutaceae 11 2.13 2.10 0.90 Sapindaceae 17 2.13 5.00 0.003 Sapotaceae 4 0.38 0.30 0.65 Smilacaceae 3 0.13 0.40 0.01 Solanaceae 3 0.63 0.70 0.93 Urticaceae 3 0.13 1.10 <0.001 Verbenaceae 5 0.63 0.90 0.47 Vitaceae 6 2.63 2.50 0.83 1 Three major frugivore species (emerald dove, channel-billed cuckoo and mistletoebird) and five mixed-diet frugivore species (Australian brush turkey, wonga pigeon, pale-headed rosella, barred cuckoo-shrike and varied triller) were not included in these analyses because of the low plant species richness of their diets (Table 4.1, Figure 4.4). Minor frugivores were not included in analyses because of the low number of plant species that they consumed from most families.

The UPGMA classification assembled frugivore species into four groups that

broadly corresponded with frugivory level (Figure 4.5). Most major frugivores were

classified together in Group 1, most mixed-diet frugivores were in Group 2 and most

104

minor frugivores were in Group 3 (Figure 4.5). Group 4 comprised species from all

three frugivory levels; the two major frugivore species in Group 4 were small gaped,

and the three mixed-diet species were either small gaped or seed crushers.

Table 4.5 shows the percentage dissimilarity between the different groupings of

bird species in the classification and the plant species that contributed most to these

differences. There was a high level of dissimilarity among all groups: the two groups of

bird species that had the least dissimilar patterns of plant species consumption were

Groups 1 and 2 (Table 4.5). The plant species listed for each set of pair-wise

comparisons were consumed by many of the bird species in one of the groups and

relatively few of the bird species in the other group. In many cases, the same plant

species may have contributed to differences among more than two groups. For example,

Guioa semiglauca (Sapindaceae) was more common in the diets of bird species in

Group 4 than 3 but more common among Group 2 birds than those in Group 4. Bird

species in Groups 3 and 4 generally consumed low numbers of plant species.

Consequently, the plant species that contributed most to the dissimilarity between the

groups were all more frequent in the diets of species in Groups 1 and 2 than 3 or 4

(Table 4.5). In terms of differences in diet composition, bird species in Groups 3 and 4

consumed few of the species consumed by Groups 1 and 2. In contrast, bird species in

Groups 1 and 2 consumed most of the plant species consumed by the other birds.

The plant taxa that distinguished the bird species in Group 1 from Groups 2, 3

and 4 consistently included several from the Lauraceae (Table 4.5). This was consistent

with the results of univariate comparisons of major and mixed-diet bird species (Table

4.4). In addition, consumption of the large fruited Eleaocarpus grandis (22.5 mm

median diameter) and individual species from Burseraceae, Ebenaceae and Vitaceae

distinguished this group of bird species from all other groups (Table 4.5). The bird

species in Group 2 were distinguished from birds in Groups 1, 3 and 4 by their

105

consumption of arillate species from the Elaeocarpaceae, Mimosaceae and Sapindaceae

(Table 4.5); five of the six plant species that distinguished between Groups 2 and 1, and

which were more abundant in the diets of species in Group 2, were arillate species.

Shared consumption of species from Araliaceae and Arecaceae distinguished birds in

Group 1 and 2 from those in Groups 3 and 4. Bird species in Group 3 were

distinguished from Group 4 by their consumption of Ficus spp. Bird species in Group 4

were distinguished by Euphorbiaceae, Solanaceae and certain species in Sapindaceae

and Rhamnaceae.

10

6

Fig

ure

4.5

Cla

ssifi

catio

n of

frug

ivor

e sp

ecie

s ba

sed

on B

ray-

Cur

tis s

imila

rity

in p

atte

rns

of c

onsu

mpt

ion

of n

ativ

e pl

ant s

peci

es. ‘

ST

.’ is

see

d

trea

tmen

t (D

see

d-di

sper

ser,

C s

eed-

crus

her)

; ‘G

’ is

gape

wid

th c

lass

( S

sm

all (

< 1

0 m

m),

M m

ediu

m (

10 -

15

mm

) , L

larg

e (>

15

mm

)); a

nd ‘F

L’ is

frug

ivor

y le

vel (

■ M

ajor

, ◊

Mix

ed, ▲

Min

or).

4 3 2 1

S

L S

S

S

L S

S

M

L

L

L M

L S

M

M

L M

L

L M

M

S

L M

L

L

L

L M

L

L M

MGF

L

ST

D

C

C

C

D

D

C

D D

D

D

D

D

D

C

C

C

C

C

C

D D C

D

D

D

D

D

D

D

D

D

D

D

C

■ ◊

▲ ■

◊

▲

◊

▲

◊

▲

■

■

▲

▲ ◊

▲ ▲

▲

◊

◊

◊

◊ ■ ◊

◊

◊

◊

◊ ■

■

■

◊ ■

■ ■

107

Table 4.5 The ten plant species that contributed most to the dissimilarity between each pair of

groups formed in the classification. ‘Pair-wise comparison’ shows the two groups being compared,

‘Average dissimilarity’is the percentage dissimilarity between the two groups based on their

patterns of plant species consumption (100 is total dissimilarity). The numbers in columns show the

group in which the corresponding plant species was consumed by the higher number of bird

species. Note that in comparisons of Groups 1 (n=10) and 2 (n=7) with Groups 3 (n=10) and 4

(n=8), distinguishing plant species were always consumed by the highest number of bird species

from Groups 1 and 2.

Pair-wise comparison Average dissimilarity

1 v 2 63.58

1 v 3 83.65

1 v 4 92.40

2 v 3 79.55

2 v 4 88.52

3 v 4 90.25

Plant species family Euroschinus falcata Anacardiaceae 2 2 Polyscias elegans Araliaceae 1 1 2 2 P. murrayi Araliaceae 1 1 2 2 Archontophoenix cunninghamiana

Arecaceae 1 1 2 2

Canarium australasicum Burseraceae 1 1 1 Diospyros pentamera Ebenaceae 1 1 1 Elaeocarpus grandis Elaeocarpaceae 1 1 1 E. kirtonii Elaeocarpaceae 1 1 E. obovatus Elaeocarpaceae 2 2 Sloanea australis Elaeocarpaceae 2 2 2 Glochidion ferdinandi Euphorbiaceae 2 4 Macaranga tanarius Euphorbiaceae 3 Omalanthus nutans Euphorbiaceae 1 4 Beilschmedia obtusifolia Lauraceae 1 B. elliptica Lauraceae 1 1 1 Cinnamomum oliveri Lauraceae 1 1 1 Cryptocarya glaucescens

Lauraceae 1

C. obovata Lauraceae 1 1 1 C. triplinervis Lauraceae 1 1 Litsea australis Lauraceae 1 1 1 L.reticulata Lauraceae 1 1 1 Neolitsea dealbata Lauraceae 1 1 1 Melia azedarach Meliaceae 1 3 Acacia maidenii Mimosaceae 2 2 2 A. melanoxylon Mimosaceae 2 2 2 Ficus coronata Moraceae 2 2 F. fraseri Moraceae 3 F.macrophylla. Moraceae 2 3 F. obliqua Moraceae 1 2 3 F. platypoda Moraceae 2 3 F. rubiginosa Moraceae 1 3 F. superba Moraceae 3 F. virens Moraceae 3 F. watkinsiana Moraceae 1 4 Streblus brunonianus Moraceae 2 2 Acmena smithii Myrtaceae 1 1 3 Olea.paniculata Oleaceae 1 Piper novae-hollandiae Piperaceae 1 1 Alphitonia excelsa Rhamnaceae 2 2 4

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Table 4.5 (cont.) Pair-wise comparison Average dissimilarity

1 v 2 63.58

1 v 3 83.65

1 v 4 92.40

2 v 3 79.55

2 v 4 88.52

3 v 4 90.25

Plant species family A. petreii Rhamnaceae 2 2 Coprosma quadrifida Rubiaceae 2 Acronychia oblongifolia Rutaceae 2 1 1 Melicope micrococca Rutaceae 2 2 2 Exocarpus cupressifolius

Santalaceae 3

Diploglottis australis Sapindaceae 2 2 3 Elattostachys xylocarpa Sapindaceae 2 2 2 Guioa semiglauca Sapindaceae 2 2 4 Jagera pseudorhus Sapindaceae 4 Sarcopteryx stipitata Sapindaceae 2 Solanum aviculare Solanaceae . 4 Aphananthe philipensis Ulmaceae 2 3 Dendrocnide excelsa Urticaceae 2 Cissus sterculifolia Vitaceae 1 1 1

Large- and medium-gaped bird species are interspersed in the classification (Figure 4.5).

Frugivores with small (<10 mm) gapes mostly consumed a subset of the plant species that were

consumed by frugivores with medium or large gapes (Figure 4.6). There was considerable overlap

in the plant species consumed by birds from all gape widths. Of the 48 plant species only consumed

by large-gaped frugivores, a large number (27; 56%) had large (≥10 mm) diaspores, compared with

seven (23%) of the 30 species for medium-gaped birds and one (14%) of the seven plant species

only consumed by small-gaped birds (Chi square 3x2 contingency table comparing the number of

plant species with diaspores ≥10 mm and <10 mm among the three gape width classes, χ2 = 11.05, p

= 0.004).

109

Figure 4.6 Overlap in the number of plant species consumed by frugivorous birds in relation to

gape width classes (small (< 10 mm, n = 6), medium (10 – 15 mm, n = 15) and large (> 15 mm, n =

17) gape widths).

4.4. Discussion

4.4.1 Overlap and variation among frugivorous bird species in patterns of plant species

consumption

This study shows that many of the rainforest plant species in subtropical Australia are

consumed by multiple frugivorous bird species. Frequently, the bird species that consume fruits

from a given plant species may vary in their degree of frugivory, gape size and seed treatment. As

in other regions, figs are consumed by most frugivore species, irrespective of their degree of

frugivory, gape size or other attributes (Ridley, 1930; Janzen, 1979; Snow, 1981; Wheelwright et

al., 1984; Shanahan et al., 2001). Many of the plant species in the Euphorbiaceae and Sapindaceae

are also consumed by many frugivorous bird species in the present study, as in other regions (Snow,

1981; Wheelwright et al., 1984; Silva et al., 2002). However, the present work also shows that there

is substantial variation among sets of frugivore species in their consumption of certain plant species.

This variation is related to bird species’ gape width, degree of frugivory and seed treatment. For

example, species in the Araliaceae and Arecaceae were recorded in the diets of a large number of

major and mixed-diet bird species, particularly seed dispersing species with gapes > 10 mm, but

were consumed by few minor frugivores.

7 3

246

108

48

30

Large

Medium

Small

110

The present study documents less overlap among frugivorous bird species in their patterns of

plant species consumption than has previously been implied in functional classifications that have

grouped most bird species together as a functional unit (e.g., van der Pijl, 1982; Gautier-Hion et al.,

1985; Bollen et al., 2004). It is possible that increased data on fruit-frugivore interactions in the

study region would show greater overlap among bird species in their patterns of consumption of

plant species. For example, interactions involving rarer plant and/or bird taxa are likely to be under-

recorded in field observations of frugivory (Silva et al., 2002). However, the data used in the

present work were collected over large geographical and temporal scales. This suggests that the

major differences among frugivore species in their pattern of plant species consumption may be

consistent over space and time.

4.4.2 Frugivore gape width and patterns of fruit size consumption

There was a positive association between a bird species’ gape width and the average size of

fruits that it consumed. The average size of fruits consumed by minor frugivore species was

substantially smaller than their handling capacity. This contrasted with major and mixed-diet

frugivores that consumed relatively high proportions of fruits that were close to their maximum

handling capacity. The patterns of plant consumption shown by most major and mixed-diet

frugivorous bird species are consistent with the gape-limited patterns of fruit size consumption

reported by Wheelwright (1985) for frugivorous birds in Costa Rica. It has been proposed that net

energy yield would be higher for fruits that are close to a species’ fruit size handling capacity

because there may be additional searching and handling costs associated with consuming small

fruits (Martin, 1985; Herrera, 1987; Sallabanks and Courtney, 1993). Furthermore, because larger

seeds may be regurgitated more readily than smaller seeds, and hence eliminated more rapidly than

small seeds can be defecated, net rates of pulp intake may be higher when consuming larger fruits

(Murray et al., 1993).

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However, larger-gaped birds also consumed small fruits, as has been documented in Costa

Rica (Wheelwright, 1985) and Thailand (Kitamura et al., 2002). Even the exclusively frugivorous

bird species with larger gapes (the Ptilinopus fruit doves and topknot pigeon) consumed some small

fruits (Table 4.1). Consequently, rather than consuming a distinctly different set of plant species,

small-gaped frugivore species consumed the small-fruited subset of the plant species that were

collectively consumed by larger-gaped bird species. With the exception of the largest fruits, which

were only consumed by some of the bird species with gapes wider than 15 mm, there was also

considerable overlap in patterns of plant species consumption between birds with medium and large

gapes. Although there may be energetic or nutritional advantages to consuming larger fruits,

patterns of fruit size consumption may be complicated by variation among plant species in factors

such as their fruit pulp to seed ratios (Howe and van der Kerckhove, 1980; Herrera, 1987) and pulp

chemistry (Martínez del Rio and Restrepo, 1993; Cipollini and Levey, 1997).

4.4.3 Frugivory level and patterns of plant species consumption

McKey (1975) proposed that patterns of plant consumption would vary between highly

frugivorous species and those with mixed diets. Specifically, it was reasoned that highly

frugivorous species would specialise on lipid-rich fruits, while mixed-diet frugivores would

consume fruits from carbohydrate-rich plant species (McKey, 1975; Howe and Estabrook, 1977;

Snow, 1981). In subtropical Australia, there is substantial overlap among major and mixed-diet

frugivores in their patterns of plant species consumption, contrary to the predicted dichotomy.

Major frugivores did consume the highest number of plant species from the family Lauraceae, a

family known for the high lipid content of fruit pulp (Snow, 1971, 1981; Crome, 1975; Stiles 1993).

However, as in other regions (e.g., Howe, 1981; Herrera, 1984; Fuentes, 1994; Sun et al., 1997),

major frugivores were not the only consumers of plant species that may contain high lipid content.

There is little information regarding nutrient, mineral or chemical content of Australian fruits.

However, the plant taxa that characterised the diets of mixed-diet frugivores included families that

112

bear fruits with lipid-rich pulp in other regions, including Celastraceae (Corlett, 1996) and

Sapindaceae (Snow, 1981). These data suggest that lipids may be energetically important for both

major and mixed-diet frugivores in subtropical Australia.

However, neither major nor mixed-diet species specialised on lipid-rich fruits, and both

groups consumed many plant taxa that are associated with high carbohydrate content in other

regions (e.g., Moraceae). This may reflect the need to consume a variety of nutrients and minerals

(Pulliam, 1975; Schaefer et al., 2003), or to avoid consuming toxic amounts of fats (Bairlein, 1998)

or secondary chemicals that may be associated with particular plant taxa (Bairlein, 1996; Cipollini

and Levey, 1997). In addition, lipid-specialisation may not be possible because plants that bear

lipid-rich fruits may not always be fruiting (Leighton and Leighton, 1983; Wheelwright, 1986;

Innis, 1989).

There was a consistent difference between major and mixed-diet frugivores in their

consumption of plant species with arillate fruits. It is difficult to provide a mechanistic explanation

for the disproportionate consumption of arillate species by mixed-diet frugivores. It was reported

that birds of paradise (family Paradisidae) were the sole consumers of certain arillate fruits in Papua

New Guinea, interpreted to be a function of their relatively long and narrow bills (Pratt and Stiles,

1985). However, a more recent study showed that other frugivore groups, including fruit pigeons,

also consumed arillate fruits in Papua New Guinea (Brown and Hopkins, 2002).

In the present study, a set of bird species that were classified as mixed-diet frugivores

showed patterns of plant species consumption that closely resembled several major frugivores

(Group 1 in the classification). The major frugivore bird species in this group included the

Ptilinopus fruit-doves and topknot pigeon, which are among the most highly frugivorous bird

species in the world (Crome, 1975). These species shared a substantial proportion of plant species

with the mixed-diet green catbird, satin and regent bowerbirds (all in the family Ptilonorhynchidae)

and pied currawong. Similar patterns of plant species consumption were shown for fruit-dove and

bowerbird species from these same genera in Papua New Guinea (Pratt and Stiles, 1985; Brown and

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Hopkins, 2002). Similarity in patterns of plant species consumption between these bird species may

be related to a substantial increase in the degree of frugivory of the bowerbirds, catbird and pied

currawong during the non-breeding season (Blakers et al. 1984; Innis and McEvoy, 1992; Frith et

al., 2004). This seasonal switch to a fruit-dominated diet may necessitate the consumption of plant

taxa with particular nutritional attributes (Bairlein, 1996). Hence, frugivore species that have fruit-

dominated diets during part of the year may show overall patterns of plant consumption similar to

species that have fruit-dominated diets throughout the year.

4.4.4 Variation among bird species within a frugivory level

Although the structure of fruit-frugivore interactions in the assemblage studied is related to

degree of frugivory, there is also substantial variation in patterns of plant consumption within the

major and mixed-diet frugivore groups. Minor frugivore species were similar to one another; they

consumed a low number of native plant species, predominantly Ficus spp., and were mostly

classified together in Group 3. However, there were several major and mixed-diet frugivore species

(in Groups 3 and 4 in the classification) that consumed only a subset of the plant species consumed

by other major and mixed-diet frugivores. Based on data collected in Papua New Guinea, Brown

and Hopkins (2002) suggested that some relatively frugivorous species, including the barred

cuckoo-shrike (“yellow-eyed cuckoo-shrike” in their study), may specialise on figs. It appears that

this is the case for this and certain other major and mixed-diet species that had high dietary

proportions of figs (e.g., in the present study, channel-billed cuckoo, common koel, wonga pigeon).

Overall, seed-crushing species were not distinguished from seed-dispersing species based on

dietary composition, although there were insufficient data to test for an effect of seed treatment

within frugivory levels. For example, it may be reasonable to expect that seed-crushing major

frugivore species show patterns of plant species consumption similar to mixed-diet frugivores, since

they derive nutrition from seed as well as fruit pulp (Snow, 1981; Innis, 1989; Jones and Crome,

1990). In this study, two of the three seed-crushing species that were classed as major frugivores

114

(emerald dove and brown cuckoo-dove) had diets that resembled mixed-diet species more than

major frugivores. The diet of the seed-crushing white-headed pigeon was relatively similar to the

other major frugivore species.

Classification based on functional attributes may overestimate the functional similarity

between certain species at finer scales. For example, in the present study, both the figbird and

wompoo fruit-dove have large gapes and fruit-dominated diets and have relatively similar dietary

composition in the context of the entire avian frugivore assemblage. However, in a pair-wise

comparison of plant species dietary composition, the figbird was only known to consume 44% of

the plant species consumed by the wompoo fruit-dove (see Chapter Five). Consideration of

taxonomic relatedness among species may help elucidate some of the additional variation within the

groups formed using functional attributes. In the present study, close taxonomic relatives with

similar functional traits tended to have the most similar diets (e.g., the wompoo and rose-crowned

fruit-doves and topknot pigeon; bowerbirds and catbird). However, some sets of close relatives with

different functional traits also had similar diets (e.g., black-faced and barred cuckoo-shrike),

whereas others did not (e.g., figbird and olive-backed oriole). Secondary chemical compounds may

generate similar patterns of plant species consumption by taxonomic relatives.

4.4.5 Gape width and frugivory level as indicators of the functional potential of frugivorous birds

as seed dispersers

There is a worldwide concern that large fruited plant species may not be dispersed in

disturbed rainforest (Corlett, 1996, 1998; Corlett and Turner, 1997; Harrington et al,. 1997; Silva

and Tabarelli, 2000; McConkey and Drake, 2002). Studies investigating the potential for a

frugivorous bird species to disperse large-fruited plants have often considered its gape width as an

indication of its functional capacity (e.g., Silva and Tabarelli, 2000; McConkey and Drake, 2002). It

has recently been argued that gape size is an unreliable measure of fruit size handling capacity

(Dennis and Westcott, 2006). However, with the notable exception of the channel-billed cuckoo, the

115

present study has shown a strong association between gape width and patterns of fruit size

consumption among the avian frugivore assemblage of subtropical Australia, provided that gape

distensibility and frugivory level are accounted for. For example, the consumption of large fruits by

Ptilinopus fruit-doves could not be predicted on the basis of hard-tissue bill dimensions (Dennis and

Westcott, 2006). However, their capacity to handle larger fruits is evident if their gape distensibility

is incorporated into the measurement of gape width (as described in Chapter Three, Section 3.2.1).

The present work has also shown the importance of incorporating a measure of frugivory level into

analyses of seed dispersal potential to avoid over-estimating the ability of minor frugivore species

to disperse large seeds. For example, based on the results presented here, it would be predicted that,

despite its wide gape, the black-faced cuckoo-shrike would only consume small fruits because of its

low degree of frugivory. In most studies relating patterns of fruit size selection to frugivore

attributes (e.g., Silva and Tabarelli, 2000), frugivory level has not been explicitly considered.

In Chapter Three, it was proposed that classification of frugivorous bird species based on

their gape width, frugivory level and seed crushing behaviour should yield functionally similar

groups of species. The results of the present chapter show that groups formed using these frugivore

attributes are associated with major differences in dietary composition among bird species in

subtropical Australia. The classification of frugivorous species using readily available functional

attributes provides a framework for predicting substantial differences among frugivore species in

their roles as seed dispersers. In application to conservation, this approach could be used to forecast

and manage the consequences of frugivore declines in fragmented forests for seed dispersal (Silva

and Tabarelli, 2000; Kitamura et al., 2002). Ideally, classification based on the chosen attributes

would not entirely substitute for detailed, species-specific dietary information. However, the

collection of such information is extremely time-consuming. Furthermore, scientists are required to

inform management decisions in the absence of this information. The approach demonstrated here

provides a systematic means of identifying the plant and frugivore species that may be a priority for

conservation and for research into patterns of plant-frugivore interactions.

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Chapter Five

Reduced dispersal potential of native rainforest plant species in fragmented

rainforest

5.1 Introduction

Seed dispersal enhances the reproductive success of plants by removing seeds from

competition, predation and other causes of seed and seedling mortality that are most intense directly

beneath the parent (Janzen, 1970; Connell, 1971; Harms et al., 2000). Seed dispersal is also the

agent of plant mobility, enabling colonisation of suitable germination microsites that become

available following local disturbances within forest (Grubb, 1977; Hubbell, 1979). Frugivorous

vertebrates disperse the seeds of most rainforest plants (Howe and Smallwood, 1982: Willson et al.,

1989). Therefore, declines in the abundance of frugivores following rainforest clearing and

fragmentation may alter the rates or patterns of seed dispersal and plant regeneration (Corlett, 1998,

2002; Bleher and Böhning-Gaese, 2001, 2006; Cordeiro and Howe, 2001, 2003). For example, the

complete absence of dispersers for a particular plant species would mean that recruitment could

only occur beneath the crown of the parent plant, and may result in reduced recruitment (Bleher and

Böhning-Gaese, 2001; Cordeiro and Howe, 2003; Babweteera et al., 2007). Dispersal failure in

fragmented forests would prevent the plant species from recolonising forest remnants from which it

had gone extinct, and would mean it was unable to colonise cleared land during secondary

succession (Poschlod et al., 1996; Duncan and Chapman, 2002). Consequently, plant species that

experience dispersal failure would have low recruitment rates and restricted spatial distribution and

be vulnerable to stochastic extinction (Fahrig and Merriam, 1994; Cochrane et al., 1999).

In the situation where dispersers are present but their abundance is greatly reduced, dispersal

may not fail but would potentially be reduced. The consequences of substantially reduced dispersal

117

of a plant species for plant regeneration may resemble those described for dispersal failure,

although the extent to which recruitment would be spatially and quantitatively limited would

depend on the feeding rates and patterns of intra- and inter-habitat movements by remaining

dispersers (Loiselle and Blake, 2002; Schupp et al., 2002; Dennis and Westcott, 2006).

The decline of certain frugivore species in fragmented landscapes may result in dispersal

failure or reduction for plant species, but this depends on the dietary composition of other frugivore

species in the regional frugivore assemblage. For example, it has been predicted that large-seeded

plant species are unlikely to be dispersed in fragmented tropical rainforest regions worldwide as a

result of the decline of the entire suite of frugivore species that are capable of dispersing large seeds

(Chapman and Chapman, 1995; Corlett, 1998, 2002; Silva and Tabarelli, 2000; Kitamura et al.,

2002; McConkey and Drake, 2002). On the other hand, most fleshy-fruited plant species are eaten

and dispersed by multiple frugivore species (Howe, 1977; Howe and Smallwood, 1982;

Wheelwright and Orians, 1982; Brown and Hopkins, 2002), and many frugivore species do occur in

fragmented landscapes (Estrada et al., 1993; Corlett, 1998; Renjifo, 1999; Chapters Two and Six of

this thesis). Therefore, the consequences of the decline of one frugivore species for plant dispersal

may be offset by increases in the density or consumption rates of other, functionally similar

frugivore species (Corlett, 1998; Renjifo, 1999; Nathan and Muller-Landau, 2000; Loiselle and

Blake, 2002).

The potential for functional substitution among frugivore species can be examined by

identifying the attributes of frugivores that reflect their role as seed dispersers (Silva and Tabarelli,

2000; Dennis and Westcott, 2006). For example, in Chapter Three, I showed that, while the bird

species that declined in fragmented parts of subtropical Australia had large gapes and fruit-

dominated diets, these attributes were shared by some of the frugivorous bird species that persisted

or increased in abundance in fragmented parts of the landscape. I proposed that the plant species

dispersed by decreaser species may not necessarily experience dispersal failure, although dispersal

may be reduced, depending on whether the abundance and behaviour of substitute disperser species

118

fully compensated for the declines. The use of functional attributes of frugivores may be a useful

means of identifying broad sets of plant taxa that they consume (Chapter Four), and hence the

plants that may be vulnerable to frugivore declines (e.g., Silva and Tabarelli, 2000; Kitamura et al.,

2002; Chapter Three of this thesis). However, it may be necessary to compare actual dietary

composition across the frugivore assemblage to determine the specific plant taxa that would be

affected by changes in the abundance of individual frugivore species (Galetti, 2001). Among the

studies that have considered the specific plant species consumed by individual frugivore species,

most attention has been paid to large frugivore species and large-fruited plant species (e.g.,

Kitamura et al., 2002; McConkey and Drake, 2002; Babweteera et al., 2007).

The present study considers patterns of plant species consumption across an entire regional

avian frugivore assemblage to assess the likelihood that the effects of fragmentation-related

decreases in some bird species could be offset by the presence of other frugivore species with

similar dietary composition. This study does not explicitly evaluate the potential for the changed

abundance of certain frugivore species to result in other changes to seed dispersal, such as the

dispersal of fewer seeds, or seed input to fewer or different microsites (Schupp, 1993; Jordano and

Schupp, 2000; Loiselle and Blake, 2002). Frugivore species were previously identified as showing

decreased, increased or similar abundance in fragmented compared with intact forest in a rainforest

landscape of subtropical Australia (Chapter Two). Here, records of the consumption of plant species

by frugivore species are used to assess dietary similarity among frugivore species and among the

groups of species that showed different abundance responses to fragmentation. Diet composition is

assessed in terms of plant species, genus, family, and fruit size. This approach identifies plant taxa

that are vulnerable to reduced dispersal, for example because they are known only from the diets of

frugivores with decreased abundance in fragmented landscapes. This chapter will also examine

potential changes in the dispersal of introduced plant species. The potential implications for the

maintenance of plant regenerative potential in fragmented rainforest are considered.

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5.2 Methods

5.2.1 Changes in the frugivorous bird assemblage in fragmented subtropical rainforest

The distribution and clearing history of subtropical rainforest in Australia were described in

Chapter One (Section 1.4.1). Chapter Two described the study region and site network used in the

present work (Section 2.2.1), and field and analytical methods (Section 2.2.2).

The responses of avian frugivores to rainforest fragmentation in a region of subtropical

Australia were assessed in Chapter Two (Section 2.3.1). Three response patterns were identified

among 26 frugivorous bird species by comparing species’ abundances between rainforest remnants

and areas of regrowth relative to extensive forest. These three patterns were “decreaser” species

(n=5), which had lower abundance in remnants and / or regrowth than in extensive forest;

“increaser” species (n=7), which had higher abundance in remnants and / or regrowth than

extensive forest; and “tolerant” species (n=14), which showed no clear difference in abundance in

either remnant or regrowth habitats, compared with extensive forest. Other frugivorous bird species

(n=16) in the region were too uncommon for statistical analyses, and may therefore be likely to

make a relatively small contribution to seed dispersal because of their low abundance. Nine of the

26 bird species grind or crush seeds (Chapter Three, Section 3.2.1) and are not considered further in

the present chapter as they probably contribute relatively little to the dispersal of viable seed. The

non-seed-crushing scarlet honeyeater Myzomela sanguinolenta was also excluded, due to the low

number of observations of fruit consumption recorded to the level of plant species. Therefore, 16

frugivorous bird species (four decreaser, five increaser, and seven tolerant species) are considered

here.

5.2.2 Fruit consumption database

Data on the consumption of plant species by the 16 frugivore species were derived from 100

published sources (Appendix 1), together with several unpublished data sets. The data used in the

present study of 16 bird species in relation to their fragmentation-related abundance responses

120

comprised a subset of the database described in Chapter Four (Section 4.2.1); this chapter deals

with 16 of the 38 frugivorous bird species that were considered in Chapter Four. The plant species

included in analyses are listed in Appendix 2.

5.2.3 Data analyses

Spearman rank correlations were used to test for an association between the frugivore

species’ sensitivity to fragmentation (scored as increaser (low sensitivity) = 1, tolerant = 2,

decreaser (high sensitivity) = 3) and the total number of native plant species, genera and families

that they consumed. Spearman rank correlation was also used to test the association between

sensitivity to fragmentation and the number of native plant species consumed from the plant

families with at least five species in the data set. The dietary proportions of exotic plant species and

of native plant species with large (≥10 mm diameter) diaspores were compared among decreaser,

tolerant and increaser frugivores, using Spearman’s rank correlations and with analysis of variance

(ANOVA), using frugivore species as replicates within each fragmentation response group. Pair-

wise differences were tested using least significant difference (LSD) comparisons.

To examine similarities among the 16 frugivore species in their dietary composition, a

classification tree was generated using the UPGMA algorithm (Manly, 1994) in PRIMER (5.2.9)

(Clarke and Warwick, 2001), with the Bray-Curtis dissimilarity metric. The statistical significance

of overall dietary differences between frugivore response groups was tested using analysis of

similarity, with 9 999 iterations (ANOSIM; Clarke and Green, 1988), also in PRIMER. Plant

species with less than three consumer species, and frugivore species that consumed less than three

native plant species were excluded. For analyses based on patterns of consumption of plant species,

the Bray-Curtis dissimilarity was based on the presence of native plant species in the diet of

frugivore species. For analyses at higher taxonomic levels, counts of the number of native species

consumed from each plant genus or family were used. Genera or families with only one plant

species in the data set were excluded.

121

Potential redundancy between pairs of frugivore species was quantified as the percentage of

plant species in the diet of each decreaser frugivore that was also consumed by the other frugivore

species. The redundancy between individual decreaser species and particular combinations of other

species was also similarly quantified. The magnitude of potential dispersal reduction that would

result from the absence of each individual frugivore species was assessed by calculating the number

of plant species recorded solely in the diet of each frugivore species, as well as the number of plant

species known only from the collective diet of groups of certain frugivore species (for example, all

decreaser frugivores). The attributes of the plant species that were recorded only in the diet of

decreaser frugivores were identified (higher taxonomic association, growth form and diaspore size)

and compared with those of the remaining plant species in the data set. This comparison was made

using chi-squared tests on cross-tabulations of species’ frequencies within attribute classes in SPSS

(2001).

5.3 Results

The data matrix comprised information for 254 plant species from 164 genera and 67

families, including 31 plant species introduced to subtropical eastern Australia from other

continents, and three introduced from tropical Australia (collectively referred to as “exotic species”)

(Appendix 2). The data on plant species' presence in the diet of the 16 frugivore species yielded

records of 912 different combinations of plant and frugivore species. Most of the 220 native plants

(70%) were recorded in the diet of more than one frugivore species.

5.3.1 Diet comparisons between frugivore response groups

There was considerable variation among frugivore species in the numbers of plant taxa they

consumed, with numbers of native plant species ranging from one to 106 (Table 5.1). All decreaser

frugivores, together with several tolerant or increaser species, consumed relatively high numbers of

plant species, genera and families (Table 5.1). There was no statistically significant correlation

122

between sensitivity to fragmentation and the number of native plant species (Rs = 0.45, p = 0.08, n

= 16), genera (Rs = 0.36, p = 0.17) or families (Rs = 0.37, p = 0.16) consumed, although all

associations were positive. Exotic plants comprised a larger average percentage of the diet of

increasers (41%) than of tolerant (25%) or decreaser (9%) frugivores (Table 5.1) (Rs = 0.70, p =

0.002; ANOVA F = 4.24, p = 0.04).

12

3

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ed b

y ea

ch f

rugi

vore

spe

cies

. Bir

d sp

ecie

s w

ith

gape

s <

10 m

m a

re a

ster

iske

d. ‘

Gen

.’ a

nd

‘Fam

.’ a

re g

ener

a an

d fa

mil

ies,

res

pect

ivel

y.

N

um

ber

s o

f p

lan

t ta

xa

Res

po

nse

p

atte

rn1

Co

mm

on

nam

e2 C

od

e G

enu

s an

d s

pec

ies

Fam

ily

Sp

ecie

s G

en.

Fam

. S

pec

ies

<10

mm

S

pec

ies

≥1

0 m

m

N

E

N

E

N

E

D

ecre

aser

wom

poo

frui

t-do

ve

supe

rb fr

uit-

dove

ro

se-c

row

ned

frui

t-do

ve

gree

n ca

tbird

wom

p sf

d rc

fd

gcat

Ptil

inop

us m

agni

ficus

P

. sup

erbu

s P

. reg

ina

Ailu

rioe

dus

cras

siro

stris

Col

umbi

dae

Col

umbi

dae

Col

umbi

dae

Ptil

onor

hync

hida

e

81

25

74

104

4 4 7 7

56

31

54

77

37

22

32

40

34

11

41

60

4 3 6 7

47

14

33

44

0 1 1 0 T

oler

ant

topk

not p

igeo

n co

mm

on k

oel

chan

nel-b

illed

cuc

koo

little

wat

tlebi

rd *

Le

win

’s h

oney

eate

r pi

ed c

urra

won

g sa

tin b

ower

bird

topk

ko

el

chan

lw

at

Lew

he

pcur

r sa

tbb

Loph

olai

mus

ant

arct

icus

E

udyn

amys

sco

lopa

cea

Scy

thro

ps n

ovae

holla

ndia

e A

ntho

chae

ra c

hrys

opte

ra

Mel

ipha

ga le

win

ii S

trep

era

grac

ulin

a P

tilon

orhy

nchu

s vi

olac

eus

Col

umbi

dae

Cuc

ulid

ae

Cuc

ulid

ae

Mel

ipha

gida

e M

elip

hagi

dae

Art

amid

ae

Ptil

onor

hync

hida

e

73

25

6 3 104

50

106

4 8 0 3 21

10

12

46

26

2 7 89

39

89

28

19

3 7 47

25

52

30

19

6 3 77

32

55

3 4 0 3 17

7 9

43

7 0 0 27

18

51

1 4 0 0 4 3 3 In

crea

ser

blac

k-fa

ced

cuck

oo-s

hrik

e fig

bird

T

orre

sian

cro

w

silv

erey

e *

Aus

tral

ian

mag

pie

blfc

s fig

b T

crow

se

ye

Am

ag

Cor

acin

a no

vaeh

olla

ndia

e S

phec

othe

res

virid

is

Cor

vus

orru

Z

oste

rops

late

ralis

G

ymno

rhin

a tib

icen

Cam

peph

agid

ae

Orio

lidae

C

orvi

dae

Zos

tero

pida

e A

rtam

idae

10

74

10

36

1

5 17

6 17

5

12

60

16

39

6

11

33

15

30

6

10

49

9 35

1

5 13

5 15

3

0 25

1 1 0

0 4 1 2 2

M

ean

SE

48

.9

9.7

8.1

1.5

40.6

7.

2 25

.4

3.7

29.5

5.

7 6.

5 1.

2 19

.4

4.8

1.6

0.4

Tot

al

220

34

164

67

130

22

90

12

1 Fro

m C

hapt

er T

wo

(Sec

tion

2.3.

1); c

ompa

riso

ns o

f ab

unda

nce

in e

xten

sive

for

est (

E),

rem

nant

s (M

) an

d re

grow

th (

G);

Dec

reas

ers'

abu

ndan

ce p

atte

rn is

E>

M>

G e

xcep

t for

gre

en

catb

ird

(E=

M>

G);

Tol

eran

t pat

tern

is E

=M

=G

; Inc

reas

ers'

patt

ern

is E

=M

<G

exc

ept f

or A

ustr

alia

n m

agpi

e (E

<M

<G

).

2 Nom

encl

atur

e fo

llow

s C

hris

tidis

and

Bol

es (

1994

).

3 D

iasp

ore

size

s <

10 m

m a

nd ≥

10 m

m d

iam

eter

are

bas

ed o

n m

edia

ns o

f pu

blis

hed

dim

ensi

ons

for

each

spe

cies

(se

e C

hapt

er F

our,

Sec

tion

4.2

.1).

124

The average dietary proportion of native plant species with large diaspores (≥10 mm

diameter) was significantly greater for decreasers (0.49) and tolerant frugivores (0.31) than

increasers (0.09), (Rs = 0.72, p =0.004; ANOVA F = 6.09, p = 0.02, Figure 5.1). There was

substantial variation among individual species within the tolerant response group; only two species

(topknot pigeon and satin bowerbird) consumed dietary proportions of native plants with large

diaspores within the range shown by decreaser frugivores (Figure 5.1).

ANOSIM showed that the overall native plant species composition of the diets of decreaser

frugivores was not significantly different from that of either tolerant or increaser frugivores (global

R = 0.137, p = 0.12). This was consistent both at the level of plant genus (R = 0.115, p = 0.15) and

family (R = 0.093, p = 0.18). Most decreaser frugivore species consumed a broadly similar suite of

plant species to one another (Figure 5.2), and were also similar to two tolerant frugivores: topknot

pigeon (which resembled wompoo and rose-crowned fruit-doves), and satin bowerbird (similar to

green catbird). The increaser figbird, tolerant Lewin’s honeyeater and tolerant pied currawong had

the next most similar dietary composition to the group containing most of the decreaser species

(Figure 5.2). These patterns were similar when classification was conducted on both plant genus

and family data. The superb fruit-dove’s diet did not closely resemble that of the other decreaser

species, probably due to the low abundance of this mostly tropical bird species in subtropical

Australia (Innis, 1989; Date et al., 1996; Gosper and Holmes, 2002), and consequently the low

number of subtropical plant species known in its diet (Table 5.1).

125

. 7 0

. 6 0

. 5 0

. 4 0

. 3 0

. 2 0

. 1 0

0 . 0 0

Figure 5.1 The proportion of native plant species with large (≥10 mm) diaspores that were

consumed by decreaser (Dec), tolerant (Tol) and increaser (Inc) frugivore species. Only species

with gape widths >10 mm are included. The horizontal lines show the mean values. Letters above

the scatter plot for each group indicate results of LSD comparisons; groups with different letters

had significantly different means (p<0.05).

Spearman rank correlation showed that there was a positive association between increasing

sensitivity to fragmentation and the number of plant species consumed from six of the 13 plant

families that had more than five plant species represented in the data set (Table 5.2). The decreaser

wompoo and rose-crowned fruit doves and green catbird generally consumed high numbers of

native plant species from Lauraceae, Meliaceae, Myrtaceae, Rubiaceae, Verbenaceae and Vitaceae

(Figure 5.3). Two tolerant species, satin bowerbird and Lewin’s honeyeater, consumed numbers of

plant species from the Meliaceae, Myrtaceae, Rubiaceae, Verbenaceae and Vitaceae, within the

range shown by decreaser frugivore species (Figure 5.3). The tolerant topknot pigeon consumed a

high number of native plant species from the Lauraceae and Vitaceae, similar to decreaser species.

The only increaser frugivore known to consume comparable numbers of native plant species from

Dec Tol

topknot pigeon satin bowerbird

Lewin’s honeyeater

Inc

Response group

Pro

po

rtio

n n

ativ

e sp

ecie

s ≥

10m

m

a ab

b

126

these families was the figbird, which consumed relatively high numbers of species from Lauraceae

and Meliaceae (Figure 5.3).

12

7

silv

ere

ye

ch

an

ne

l-b

ille

d c

uck

oo

bla

ck-f

ace

d c

uck

oo

-sh

rike

To

rre

sia

n c

row

com

mo

n k

oe

l

su

pe

rb f

ruit-

do

ve

gre

en

ca

tbir

d

sa

tin b

ow

erb

ird

ro

se-c

row

ne

d f

ruit-

do

ve

to

pk

no

t p

ige

on

wo

mp

oo

fru

it-d

ove

pie

d c

urr

aw

on

g

fig

bir

d

Le

win

's h

on

eye

ate

r

10

08

06

04

02

00

De

cre

ase

r

To

lera

nt

Incr

ea

ser

Fig

ure

5.2

Cla

ssifi

catio

n of

frug

ivor

e sp

ecie

s (b

ased

on

Bra

y-C

urtis

dis

sim

ilarit

y m

atrix

and

UP

GM

A s

ortin

g) a

ccor

ding

to

pres

ence

/ a

bsen

ce o

f

nativ

e pl

ant s

peci

es in

the

diet

. Sym

bol

s ne

xt to

nam

es s

how

the

resp

onse

gro

up fo

r ea

ch fr

ugiv

ore

spec

ies

(see

text

). T

he li

ttle

wat

tlebi

rd a

nd

Aus

tral

ian

mag

pie

wer

e no

t in

clud

ed b

ecau

se t

hey

cons

umed

onl

y th

ree

and

one

nativ

e sp

ecie

s, r

espe

ctiv

ely.

Dis

sim

ilarit

y

128

Table 5.2 The average number of native plant species from specified families consumed by

decreaser (Dec n = 4), tolerant (Tol n = 7) and increaser (Inc n = 5) frugivores. The total number of

native plant species from these families that are represented in the data set is shown. Significant (p

<0.05) results are shown in bold.

Number of plant species No. in

data set Mean no. consumed Spearman rank

correlation Plant family Dec Tol Inc Rs p Arecaceae 5 1.8 1.1 0.6 0.38 0.08 Elaeocarpaceae 6 3.3 2.6 1.4 0.32 0.11 Euphorbiaceae 8 0.8 2.0 1.8 -0.23 0.20 Lauraceae 21 12.8 5.4 2.0 0.63 0.004 Meliaceae 7 2.8 2.1 0.6 0.44 0.04 Moraceae 13 8.0 7.4 5.8 0.21 0.21 Myrtaceae 19 6.5 4.4 1.0 0.59 0.008 Oleaceae 5 1.5 0.9 0.4 0.39 0.07 Rubiaceae 10 3.0 0.6 0.2 0.64 0.004 Rutaceae 10 2.8 1.7 0.8 0.41 0.06 Sapindaceae 15 2.5 3.1 2.8 0.11 0.68 Verbenaceae 5 1.3 0.7 0.0 0.58 0.01 Vitaceae 6 4.3 2.3 0.2 0.71 0.001

5.3.2 Specific substitution potential between frugivore taxa

Among tolerant and increaser frugivores, two tolerant species, topknot pigeon and satin

bowerbird, consumed the greatest percentage of plant species that were consumed by individual

decreaser species (Table 5.3; 56-73% and 52-66% respectively). A moderate percentage of the plant

species recorded in the diets of individual decreaser frugivore species was consumed by the tolerant

Lewin’s honeyeater (38-49%), tolerant pied currawong (35-48%) and increaser figbird (40-53%),

while other individual frugivore species consumed only a small percentage of the plant species

recorded in the diets of decreasers (Table 5.3). In combination, the topknot pigeon and satin

bowerbird consumed 72-81% of the plants recorded in the diets of individual decreaser frugivore

species. The cumulative effect of remaining tolerant frugivores increased the percentage of shared

plant species to 80-86%, while the addition of increaser species did not increase this further (80-

88%) (Table 5.3).

130

Fig

ure

5.3

The

num

ber

of n

ativ

e pl

ant s

peci

es c

onsu

med

by

decr

ease

r (D

ec),

tole

rant

(T

ol)

and

incr

ease

r (I

nc)

frug

ivor

es,

for

plan

t fa

mili

es w

here

ther

e w

as a

sig

nific

ant (

p <

0.0

5) a

ssoc

iatio

n be

twee

n se

nsiti

vity

to fr

agm

enta

tion

and

the

num

ber

of p

lant

spe

cies

con

sum

ed b

y di

ffer

ent r

espo

nse

grou

ps.

top

knot

pig

eon,

satin

bow

erbi

rd,

Lew

in’s

hon

eyea

ter.

Mos

t inc

reas

er s

peci

es w

ere

not k

now

n to

con

sum

e an

y pl

ant s

peci

es

from

thes

e fa

mili

es.

L

au

rac

ea

e

0

5

10

15

20

M

eli

ac

ea

e

0246

M

yrta

ce

ae

0510

15

R

ub

iac

ea

e

0

2

4

6

8

V

erb

en

ac

ea

e

01234

V

ita

ce

ae

0 2 4 6 8

No. of native species

Res

pons

e gr

oup

Dec

T

ol

Inc

Dec

T

ol

Inc

Dec

T

ol

Inc

131

Table 5.3 The percentages of native plant species that were recorded in the diets of

each decreaser frugivore species (column head) and also consumed by each other

frugivore (bird) species (row head)1, and by particular groups of species (‘Bird groups’).

The number of native plant species consumed by each bird species is shown in Table

5.1.

Decreaser bird species womp sfd rcfd gcat Decreaser birds

wompoo fruit-dove (womp) 80 70 55 superb fruit-dove (sfd) 25 23 15 rose-crowned fruit-dove (rcfd) 64 68 51 green catbird (gcat) 70 64 72

Tolerant birds topknot pigeon (topk) 73 68 68 56 common koel 19 16 22 16 chanel-billed cuckoo 7 8 7 5 little wattlebird 0 0 0 1 Lewin’s honeyeater 38 40 49 46 pied currawong 41 48 42 35 satin bowerbird (satbb) 58 52 61 66

Increaser birds black-faced cuckoo-shrike 6 8 7 8 figbird 44 52 53 40 Torresian crow 9 8 9 9 silvereye 12 24 18 18 Australian magpie 1 0 1 1

Bird groups topk & satbb 80 72 78 81 tolerant spp. (excl. topk & satbb) 59 64 66 58 tolerant & increaser spp. (excl. topk & satbb) 64 68 70 63 all tolerant spp. 86 80 86 86 all increaser spp. 46 56 55 48 all tolerant & increaser spp. 86 80 86 88

e.g., the cells in the top left of the table show that the wompoo fruit-dove is known to eat 80% of the plants recorded as eaten by the superb fruit-dove, but that the superb fruit-dove has only been recorded eating 25% of the plants eaten by the wompoo fruit-dove.

Twenty-seven native plant species were recorded only in the diet of decreaser

frugivores (Figure 5.4, Table 5.4). These varied widely in their taxonomy, growth form

and diaspore size, although plant species from the Rubiaceae comprised a much greater

percentage of the 27 species (26%), than they did in the remainder of the data set (2%)

(χ2 = 27.1, p<0.0001). Tree species comprised a smaller proportion of plants consumed

only by decreaser frugivores (29%), compared with the proportion of trees among the

remaining species in the data set (52%) (χ2 = 4.02, p = 0.045). There was a trend for

132

vines to be more common among the plant species only known from the diets of

decreasers than among remaining species (29%, 15%, χ2 = 2.93, p = 0.086). Among the

plant species that were only known to be consumed by decreasers, there was no

significant difference in the number of species that were shrubs (41%, 33%, χ2 = 0.32, p

= 0.57), had large (≥10 mm) diaspores (48%, 40%; χ2 = 0.37, p = 0.54), or were from

the Rutaceae, Lauraceae or Myrtaceae (11%, 7%, 11%, compared with 4%, 10%, 8%; p

= 0.21, 0.96, 0.90). Eight of the 27 plant species that were only known to be consumed

by decreaser frugivores belong to genera that were known to be consumed by tolerant or

increaser frugivores, and all but one of the plant species were from families that were

known to be consumed by non-decreaser bird species (Group 1, Table 5.5).

Figure 5.4 Overlap in the number of native plant species consumed by frugivore

species from the decreaser, tolerant and increaser response groups.

The satin bowerbird and topknot pigeon consumed a relatively high number of

native plant species that were otherwise only consumed by decreaser frugivores (11 and

9, respectively; Table 5.4). The magnitude of dispersal reduction in fragmented parts of

the landscape would be substantially higher if, in addition to decreasers, either the satin

bowerbird or topknot pigeon were absent from these areas (23% and 17%, respectively;

Decreaser

Increaser

Tolerant

27

13

44

3

54

1861

133

Table 5.4). Apart from these two tolerant species and decreaser species, there are no

known additional dispersers among the species analysed here for 32% of native plant

species. Species with diaspores ≥10 mm diameter were much more common among the

plant species that were only consumed by the bird species group comprising the topknot

pigeon, satin bowerbird and decreasers, than in the remainder of the data set (60%

compared with 32%; χ2 =14.34, p = 0.0002). In addition, species from the Rubiaceae

(11%, 1%; χ2 = 9.00, p = 0.003) were more frequent among the plant species that were

only consumed by members of this group. There was no significant difference in the

number of species from the Lauraceae (13% , 8%; χ2 = 0.80, p = 0.37), Myrtaceae (both

9%; χ2 = 0.05, p = 0.81), or Rutaceae (7%, 3%; χ2 0.84, p = 0.36), or in the number of

species that were trees (44%, 52%; χ2 = 0.85, p = 0.36), shrubs (33%, 35%; χ2 = 0.01, p

= 0.91) or vines (23%, 13%; χ2 = 2.51, p = 0.11). Plant species that were only consumed

by members of this group included both of the species from the Icacinaceae, three of the

four native Verbenaceae and two of the three native Sapotaceae that were represented in

the data set.

The Lewin’s honeyeater, satin bowerbird and figbird were the unique consumers

of a relatively high number of native plant species (20, 12 and 8, respectively, Table

5.4). Therefore, the loss of any of these species may also result in substantially reduced

dispersal of a noteworthy percentage of native rainforest plant species. In particular, the

declined abundance of the Lewin’s honeyeater may cause a substantial reduction in the

dispersal of 23% of the native plant species in the data set. Most other non-decreaser

frugivore species had few native plant species for which they were the only recorded

consumer (Table 5.4).

134

Table 5.4 For each frugivore (frug.), the number of native plant species that it

consumed that were not consumed by another frugivore species (sp.), or were only

also consumed by a decreaser (Dec.) frugivore(s) is shown. The magnitude of potential

dispersal failure that would result from the absence of each individual frugivore species

together with decreaser frugivores, if there were no gaps in the data set, is also shown.

Bird codes are explained in Table 5.1.

No native plant species consumed:

Dispersal failure in absence of decreasers plus each other species1:

not by other frug.

Only by subject sp. plus any Dec

no. of plant species

% of plant species (n=220)

Decreaser species womp 6 5 sfd 1 4 rcfd 5 5 gcat 8 4 All decreaser 27 27 27 12 Tolerant species topk 1 9 37 17 koel 0 0 27 12 chan 0 0 27 12 lwat 0 0 27 12 Lewhe 20 4 51 23 pcurr 1 0 28 13 satbb 12 11 50 23 Increaser species bfcs 1 1 29 13 figb 8 0 35 16 Tcrow 0 2 29 13 seye 3 0 30 13 Amag 0 0 27 12 Species groups topk and satbb 13 30 70 32 all tolerant 44 54 125 57 all tolerant and inc 75 118 220 100

1 calculated by adding the 27 plant species recorded only in the diet of decreasers, the number of plant species recorded only in the diet of the subject non-decreaser, and those plant species only recorded in their diet plus that of decreasers.

13

5

Tab

le 5

.5 P

lant

spe

cies

that

wer

e on

ly r

ecor

ded

in th

e di

et o

f dec

reas

er fr

ugiv

ores

, and

tole

rant

or

incr

ease

r sp

ecie

s th

at m

ay s

ubst

itute

for

them

. Bird

spe

cies

cod

es a

re e

xpla

ined

in T

able

5.1

. Med

. di

as.

size

= m

edia

n di

aspo

re s

ize

(for

exp

lana

tion

see

Sec

tion

4.2.

1).

Gro

up

P

lan

t sp

ecie

s F

amily

M

ed.

dia

s.

size

(m

m)

Gro

wth

fo

rm3

Dec

reas

er

fru

giv

ore

sp

ecie

s

To

lera

nt

and

incr

ease

r sp

p.

kno

wn

to

co

nsu

me

con

gen

eric

(o

r co

n-f

amili

al)

pla

nts

4

R

ubus

moo

rei

Ros

acea

e 1.

0 V

w

omp

Lew

he,

sat

bb, f

igb,

Tcr

ow

, se

ye

(pcu

rr,

Am

ag)

Acr

onyc

hia

wilc

oxia

na

Rut

acea

e 14

.0

S

wom

p to

pk, k

oel,

Lew

he, p

curr

, sat

bb,

figb

(s

eye)

Ja

smin

ium

did

yum

O

leac

eae

6.0

V

wom

p, r

cfd

satb

b (t

opk,

ko

el, L

ew

he,

pcu

rr, b

fcs,

fig

b, s

eye

) S

yzyg

ium

fran

cisi

i M

yrta

ceae

15

.0

T

wom

p to

pk, k

oel,

Lew

he, s

atbb

, fig

b (p

curr

) S

yzyg

ium

john

soni

i M

yrta

ceae

12

.5

T

sfd

topk

, koe

l, Le

whe

, sat

bb, f

igb

(pcu

rr)

Cry

ptoc

arya

rig

ida

Laur

acea

e 13

.0

T

rcfd

to

pk, L

ew

he,

pcu

rr, s

atbb

, fig

b (k

oel,

bfcs

, Tcr

ow,

seye

) E

ndia

ndra

mue

lleri

Laur

acea

e 14

.0

T

wom

p, r

cfd,

sfd

to

pk, k

oel (

Lew

he, p

curr

, sat

bb,

figb

, bf

cs, T

crow

, se

ye)

Gro

up 1

1

Sym

ploc

os s

taw

ellii

S

ympl

ocac

eae

3.0

T

wom

p, r

cfd,

sfd

to

pk, s

atbb

S

mila

x au

stra

lis

Sm

ilaca

ceae

7.

5 V

w

omp

(sat

bb)

Sm

ilax

glyc

iphy

lla

Sm

ilaca

ceae

10

.0

V

gcat

(s

atbb

) C

alam

us m

uelle

ri A

reca

ceae

10

.5

V

wom

p (t

opk,

koe

l, Le

wh

e, p

curr

, sat

bb, f

igb,

T

cro

w)

Ela

eagn

us tr

iflor

a E

laea

gnac

eae

12.0

V

w

omp

- Le

gnep

hora

moo

rei

Men

ispe

rmac

eae

13.0

V

rc

fd, g

cat

(Le

whe

) O

wen

ia c

epio

dora

M

elia

ceae

17

.5

T

rcfd

(t

opk,

koe

l, Le

wh

e, p

curr

, sat

bb, f

igb)

E

mbe

lia a

ustr

alia

na

Myr

sina

ceae

6.

5 V

sf

d, g

cat

(koe

l, Le

wh

e, s

atbb

, se

ye)

Mic

rom

elum

min

utum

R

utac

eae

6.0

S

rcfd

(t

opk,

koe

l, Le

wh

e, p

curr

, sat

bb, f

igb,

se

ye)

Sar

com

elic

ope

sim

plic

ifolia

R

utac

eae

12.5

T

gc

at

(top

k, k

oel,

Lew

he,

pcu

rr, s

atbb

, fig

b,

seye

)

Arc

hirh

odom

yrtu

s beck

leri

Myr

tace

ae

8.5

S

gcat

(t

opk,

koe

l, Le

wh

e, p

curr

, sat

bb, f

igb)

Gro

up 2

2

Pha

leria

che

rmsi

dean

a T

hym

elac

eae

9.0

S

gcat

(L

ew

he,

seye

)

136

Tab

le 5

.5 (

cont

.)

Pla

nt

spec

ies

Fam

ily

Med

ian

d

iasp

or

e si

ze

(mm

)

Gro

wth

fo

rm3

Dec

reas

er

fru

giv

ore

sp

ecie

s

To

lera

nt

and

incr

ease

r sp

p.

kno

wn

to

co

nsu

me

con

gen

eric

(o

r co

nfa

mili

al o

nly

) p

lan

ts4

Rho

dosp

haer

a rh

odan

them

a A

naca

rdia

ceae

9.

5 T

gc

at

(top

k, k

oel,

Lew

he,

sat

bb, f

igb,

se

ye)

Hod

gkin

soni

a ov

atifl

ora

Rub

iace

ae

4.0

S

gcat

(L

ew

he,

satb

b, b

fcs,

Tcr

ow,

seye

) P

sych

otria

loni

cero

ides

R

ubia

ceae

5.

5 S

gc

at

(Le

whe

, sa

tbb,

bfc

s, T

crow

, se

ye)

Aid

ia r

acem

osa

Rub

iace

ae

7.5

S

rcfd

(L

ew

he,

satb

b, b

fcs,

Tcr

ow,

seye

) Ix

ora

beck

leri

Rub

iace

ae

8.0

S

wom

p, r

cfd,

gca

t (L

ew

he,

satb

b, b

fcs,

Tcr

ow,

seye

) C

anth

ium

cop

rosm

oide

s R

ubia

ceae

11

.0

S

wom

p, s

fd, g

cat

(Le

whe

, sa

tbb,

bfc

s, T

crow

, se

ye)

Can

thiu

m o

dora

tum

R

ubia

ceae

6.

5 S

rc

fd

(Le

whe

, sa

tbb,

bfc

s, T

crow

, se

ye)

Gro

up 2

(c

ont.)

Ran

dia

bent

ham

iana

R

ubia

ceae

17

.5

S

gcat

(L

ew

he,

satb

b, b

fcs,

Tcr

ow,

seye

) 1 p

lant

spe

cies

that

are

in g

ener

a co

nsum

ed b

y to

lera

nt o

r in

crea

ser

spec

ies.

2 pl

ant s

peci

es th

at a

re in

gen

era

not c

onsu

med

by

tole

rant

or

incr

ease

r sp

ecie

s.

3 S

ourc

e: B

utle

r, 2

003;

S =

shr

ubs

and

smal

l tre

es, T

= tr

ees,

C =

tall

clim

bers

and

und

erst

orey

clim

bers

(co

mbi

ned

in a

naly

ses)

. 4 in

clud

ing

reco

rds

of c

onsu

mpt

ion

of p

lant

gen

us o

nly

(i.e

. uni

dent

ifie

d sp

ecie

s) a

nd f

rom

exo

tic p

lant

spe

cies

.

137

5.4 Discussion

5.4.1 Reduced dispersal of native rainforest plants as a consequence of rainforest

fragmentation

Based on patterns of consumption of plant species by frugivorous bird species,

substantially reduced dispersal is likely for 27 native rainforest plant species in the

absence of four frugivorous bird species from fragmented rainforest. The analyses

underpinning this result are based on data for approximately half of the fleshy-fruited

plant species that were recorded in subtropical Australian rainforest in a comprehensive

inventory by Butler (2003). If these data reflect patterns among the general fleshy-

fruited flora of the region, 12% of native rainforest plant species may have severely

reduced regenerative potential in fragmented forest because of the absence of known

disperser species. If these plant species are unable to germinate under parent plants, for

example due to high levels of fungal attack or seed predation, these species will fail to

regenerate and may become extinct in rainforest fragments. Similar predictions have

been made elsewhere where numbers of disperser species have declined dramatically

(Janzen and Vasquez-Yanez, 1991; Chapman and Chapman, 1995; Terborgh and

Nuñez-Iturri, 2006).

However, many plant species do regenerate in the absence of dispersers (Janzen

and Martin, 1982; Chapman and Chapman, 1995; Corlett and Turner, 1997), although

their recruits may be less abundant and more spatially aggregated than in forest with an

intact disperser assemblage (Hubbell and Foster, 1990; Bleher and Böhning-Gaese,

2001; Schupp et al., 2002; Cordeiro and Howe, 2003). Plant species without dispersers

would also be unable to colonise rainforest fragments following local extinction

(McEuan and Curran, 2004) or secondary regrowth on cleared land (Duncan and

Chapman, 2002; Ingle, 2003). The low regenerative potential of plant species may result

138

in high vulnerability to extinction in fragmented rainforest (Poschlod et al., 1996;

Cochrane et al., 1999).

The plant family Rubiaceae is well represented among the species that were

identified as being vulnerable to substantially reduced dispersal in the fragmented

rainforest landscapes of subtropical Australia. Substantially reduced dispersal in forest

fragments may result in reduced numbers and a clumped spatial distribution of recruits

(e.g., Cordeiro and Howe, 2003; Babweteera et al., 2006). Recruitment of plants in the

Rubiaceae has been shown to be relatively low in isolated forest patches in both Brazil

(Tabarelli et al., 1999) and Singapore (Turner et al., 1996). This has been attributed to

unsuitable germination conditions in fragments (Turner et al., 1996; Tabarelli et al.,

1999). If the patterns detected in the present study reflect the situation in other regions,

low recruitment of plants from the Rubiaceae may be a consequence of frugivore

declines, and subsequently reduced dispersal in fragmented forest.

However, it is also possible that plant species from the Rubiaceae are consumed

by additional frugivore species in subtropical Australia than available data show. It is

thought that many frugivore species disperse Rubiaceae in tropical regions (Snow,

1981; Silva et al., 2002), although patterns of consumption of this family are not well

understood (Wheelwright et al., 1984). As in other regions (e.g., Corlett, 1996), plant

species within the Rubiaceae in subtropical Australia are typically shrubs or small trees

that bear medium-sized (average diameter 8.04 mm, n = 22) drupes or berries that are

mostly black or orange in colour (Butler, 2003). These fruit characteristics are typically

associated with consumption by many bird species (Gautier-Hion et al., 1985;

Wheelwright, 1985; Brown and Hopkins, 2002; Bollen et al., 2004). On the other hand,

factors such as secondary metabolites that require specific digestive adaptation may

limit the suite of frugivores that consume a plant taxon (Martínez del Rio and Restrepo,

1993; Izhaki et al., 2002). It is possible that chemistry is a factor limiting the

139

consumption of Rubiaceae by many bird species, since Izhaki et al. (2002) have shown

that anthraquinones, a particular class of secondary compound, were especially common

in the species of Rubiaceae that they studied, and that these deterred consumption by

some bird species.

5.4.2 Potential for disperser substitution in fragmented forest

In general, increaser species in subtropical Australia have low potential to

substitute for decreaser species as seed dispersers, since they consume a low number of

native plant taxa, a high dietary proportion of exotic plants and a low dietary proportion

of plant species with large fruits. In contrast, the overall diet consumption patterns of

tolerant frugivores resembled those of the decreaser species, suggesting considerable

potential for disperser substitution by tolerant frugivores in fragmented rainforest.

Hence, many native rainforest plants should retain some potential for dispersal within

and between remnants and into regrowth, although this would depend on whether

increaser species such as the figbird, and tolerant frugivores, particularly the topknot

pigeon, satin bowerbird and Lewin’s honeyeater actually moved and transported seeds

across habitat boundaries. However, this assessment of bird species’ potential to

substitute for one another as seed dispersers is based on the presence or absence of plant

species in their diets and does not account for variation in other factors that may

influence plant regeneration outcomes, including the numbers of fruits consumed, or

the microsites to which seeds are dispersed (Schupp, 1993).

Where the movement of frugivore species in fragmented forest has been studied

in other parts of the world, few frugivore species have moved between forest fragments

or into cleared areas (Duncan and Chapman, 2002; Silva et al., 1996; McEuen and

Curran, 2004). Patterns of native plant recruitment in weed-dominated regrowth in

subtropical eastern Australia indicate that frugivorous birds do disperse seeds from a

140

variety of native plant species across cleared land (Neilan et al., 2006). In particular

figbirds and large flocks of topknot pigeons regularly travel many kilometres over

cleared land (Frith, 1957; Price 1999) and consequently may disperse seeds among

fragmented rainforest patches.

However, most individual tolerant species consumed a relatively low percentage

of the plant species that were consumed by decreaser frugivores. Consequently, the

continued dispersal in remnant and regrowth patches of 30 of the plant species dispersed

by decreasers (an additional 14% of plant species in the data set) may depend on only

two tolerant frugivore species; the topknot pigeon and satin bowerbird. The reduced

number of disperser species for these plant species, combined with a relatively low

abundance of both topknot pigeon and satin bowerbird during site-based surveys in

remnants and regrowth (Chapter Two, Table 2.2), suggests that dispersal of seeds of

these plant species would be reduced in fragmented rainforest.

In addition to the Rubiaceae, this study identifies the plant families Lauraceae,

Meliaceae, Myrtaceae, Verbenaceae and Vitaceae, as well as those species with

diaspores ≥ 10 mm wide, as being susceptible to reduced dispersal in fragmented forest

in subtropical Australia. As with Rubiaceae, restricted recruitment of plants from the

families Lauraceae, Myrtaceae and Meliaceae in forest fragments in other regions has

been attributed to germination limitation (Turner et al., 1996; Tabarelli et al., 1999). As

suggested by the results of the present study for subtropical Australia, reduced dispersal

may also be important in these regions, especially since many plant species from these

families are consumed by only a subset of the frugivore assemblage (Snow, 1981;

Wheelwright et al., 1984; Silva and Tabarelli, 2000).

In subtropical Australia, the Lewin’s honeyeater is known to consume several

plant species from the families identified as being susceptible to reduced dispersal in

fragmented forest. Populations of these bird species appear to be stable (Blakers et al.,

141

1984; Higgins et al., 2001), and numbers of this species were consistently high in the

surveys conducted for this study (Chapter Two, Table 2.2). Therefore, in addition to the

topknot pigeon and satin bowerbird, the Lewin’s honeyeater may help maintain the

regenerative potential of some plant families in fragmented forest, although it may

contribute little to the dispersal of large-seeded plant species from any family. In the

study region, frugivorous Pteropid bats also use remnants and regrowth (Chapter Six).

These bats consume a range of plant species from the Myrtaceae (Eby, 1995; Chapter

Six of this thesis) and can transport large fruits in their teeth or claws (Ratcliffe, 1932).

However the seeds that they move beyond about 100-200 m from source trees are likely

to be those that they swallow or carry in cheek pouches; smaller than 9 mm diameter

(Eby, 1995; McConkey and Drake, 2002; Meehan et al., 2005). Therefore, frugivorous

bats may play an important role in dispersing seeds of these plants within remnants and

possibly into adjacent cleared areas (Galindo-González and Sosa, 2003), but may

contribute little to their dispersal among more widely separated fragments.

5.4.3 Implications for conservation of regenerative potential in fragmented rainforest

Data presented here and in Chapter Four suggest that most native Australian

rainforest plant species are probably dispersed by multiple frugivore species. However,

it is predicted that fragmentation-related changes in the frugivore assemblage of

subtropical rainforests may result in substantially reduced dispersal of a suite of plant

species. The size of this suite of plants is strongly dependent on the responses of two

“tolerant” frugivore species. Additional understanding of the factors affecting the

abundance of both the topknot pigeon and satin bowerbird in response to landscape

change is required because of the disproportionate effect that losing these species would

have over seed dispersal. The topknot pigeon is widespread in certain fragmented

rainforest landscapes of subtropical Australia (Date et al., 1996; Gosper and Holmes,

142

2002; Neilan et al., 2006). However, the distribution of the topknot pigeon was shown

to be restricted in small fragments compared with extensive forest in another area of

subtropical Australia (Howe et al., 1981). While the abundance pattern of topknot

pigeons suggested fragmentation tolerance, there was a trend toward a decreaser

abundance pattern, and numbers of this species were relatively low and highly variable

in the region of the present study (Chapter Two). This species has previously undergone

dramatic population declines following rapid rainforest clearing by European settlers in

the late nineteenth century (Frith, 1952, 1957; Date et al., 1996). Similarly, the

assessment of fragmentation tolerance of the satin bowerbird was based on relatively

low occurrence during the surveys conducted for the present study, although this species

was reported by Howe et al. (1981) to be relatively common in fragmented subtropical

rainforest. If, in addition to identified decreaser species, the satin bowerbird and topknot

pigeon declined in fragmented parts of the landscape, the present analyses suggest that

the dispersal of one-third of native rainforest plant species may be substantially reduced

in these areas. A comparable magnitude of dispersal reduction has been predicted from

Brazil (Silva and Tabarelli, 2000) and Thailand (Kitamura et al., 2002), regions in

which a large proportion of rainforest has also been cleared.

143

Chapter Six

The distribution of frugivorous bats and their potential to disperse

seeds in fragmented rainforest.

6.1 Introduction

Seed dispersal by frugivorous fauna plays several important roles in the

maintenance of biodiversity in fragmented landscapes. The dispersal of seeds within and

between large forest tracts, remnant forest patches and other habitats helps maintain

species and genetic diversity, initiates recolonisation after local extinction, and is crucial

for natural regeneration of rainforest on cleared land (Howe and Smallwood, 1982;

Guevara et al., 1986; Young et al., 1996; Galindo-González et al., 2000; Wright, 2002).

Frugivore species differ in their capacity to disperse plant species in fragmented

parts of the landscape, depending first on whether they use fragmented habitats, second,

on the suite of plant species they consume and third on their patterns of movement

within and between different habitat types. Hence, the species composition of the

frugivore assemblage in remnant and regrowth forest will influence patterns of seed

dispersal and forest regeneration. Dispersal of certain plant species may be reduced in

these areas if they are not dispersed by the frugivore species that occur in fragmented

parts of the landscape (Hamann and Curio, 1999; Silva and Tabarelli, 2000; Corlett,

1998, 2002; Cordeiro and Howe, 2001, 2003). For example, relatively few frugivores

have the capacity to disperse fruits with large seeds and those that do are often

vulnerable to the effects of fragmentation (Wheelwright, 1985; Chapman and Chapman,

1995; Corlett, 1998, 2002; Silva and Tabarelli, 2000; Kitamura et al., 2002; McConkey

and Drake, 2002; Walker, 2006).

144

Frugivorous birds and bats are the main seed dispersers in Australian subtropical

rainforests (Green, 1995), where approximately 70% of plant species are fleshy-fruited

(Willson et al., 1989; Butler 2003). Surveys in remnants and regrowth patches in a

fragmented subtropical rainforest landscape in Australia have found that frugivorous

bird species showed one of three patterns of abundance relative to extensive forest: (i)

lower numbers in remnant and/or regrowth rainforest patches compared with extensive

forest (‘decreaser’ pattern); (ii) higher numbers in remnant and/or regrowth rainforest

patches compared with extensive forest (‘increaser’ pattern); or (iii), no substantial

difference in numbers between the three site types (‘tolerant’ pattern: Chapter Two).

The impact of the decreased abundance of certain bird species on seed dispersal in

remnant and regrowth rainforest patches depends on whether remaining frugivore

species perform similar seed dispersal roles in these habitats.

In Australia, three species of frugivorous bat species occur regularly in

subtropical rainforests: the grey-headed and black flying-foxes (Pteropus poliocephalus

and P. alecto) and eastern tube-nosed fruit-bat (Nyctimene robinsoni). Two additional

species, the little red flying-fox (P. scapulatus) and Queensland blossom bat

(Syconycteris australis), occasionally feed on fruit but are not common in rainforest

(Ratcliffe, 1932; Law and Spencer, 1995). The consequences of the extensive loss and

fragmentation of subtropical Australian rainforest for the distribution of frugivorous

bats are not well understood. It is widely held that populations of P. poliocephalus have

suffered dramatic declines since European settlement (Eby et al., 1999; Eby and

Lunney, 2002; Dickman and Fleming, 2002). Elsewhere throughout the Old World

tropics, pteropid populations have undergone large declines (Cox et al., 1991; Corlett,

1998; McConkey and Drake, 2002), in some cases associated with restricted distribution

in fragmented habitats (Mildenstein et al., 2005). In Australia, both P. poliocephalus

(Eby 1991a, 1998; McDonald-Madden et al., 2005) and P. alecto (Markus and Hall,

145

2004) are known to use forest resources in fragmented parts of the landscape, but their

distribution has not been systematically compared between fragmented and intact forest.

The distribution and habits of N. robinsoni are poorly known, especially in the southern

parts of its range.

Chapter Five assessed the potential for tolerant and increaser bird species to

substitute for decreaser bird species as seed dispersers, based on a comparison of their

patterns of plant species consumption. The results of analyses showed that certain plant

taxa may be solely or predominantly dispersed by decreaser bird species, and therefore

may be susceptible to substantially reduced dispersal in fragmented rainforest.

However, Chapter Five also showed that a large proportion of the plant species

dispersed by decreaser bird species are potentially dispersed by certain tolerant bird

species in fragmented forest. The ability of frugivorous bats to substitute for decreaser

bird species as seed dispersers in fragmented forest landscapes of subtropical Australia

has not been evaluated. If frugivorous bats do not consume a similar suite of plant

species to decreaser frugivores, or if their distribution is restricted to extensive forest,

they would have low potential to substitute for decreaser bird species as seed dispersers.

Studies conducted in north Queensland, the Philippines, Madagascar and Peru have

reported little overlap between the diets of frugivorous bird and bat species (Gorchov et

al., 1995; Hamann and Curio, 1999; Bollen et al., 2004; Richards, 1990). In contrast,

Eby (1998) found that the plant species consumed by P. poliocephalus in subtropical

Australian rainforests comprised a subset of those that were collectively consumed by

the sympatric assemblage of frugivorous birds. However, more detailed dietary

comparisons between individual species are needed to show whether frugivorous bats

have the potential to substitute as seed dispersers for the frugivorous bird species that

decline in fragmented subtropical rainforest landscapes.

146

This chapter tests the overall hypothesis that the distribution of frugivorous bats

is restricted in a fragmented rainforest landscape of subtropical Australia. The presence

and abundance of foraging flying-foxes and N. robinsoni are compared between

extensive forest, and patches of remnant and regrowth patches that have been isolated

by clearing (16 sites of each type). The effect of site altitude and presence of a

watercourse are also evaluated. Information about the native plant species known to be

consumed by frugivorous bats is compiled and used, in conjunction with information

about their use of remnant and regrowth habitats, to assess their potential to disperse

seeds in fragmented parts of the study region. In particular, the potential for frugivorous

bat species to substitute for decreaser bird species as seed dispersers in fragmented

habitats is assessed, especially in relation to the dispersal of plant species with large

seeds and other plant taxa that have been identified as vulnerable to reduced dispersal in

fragmented forest (Chapter Five).

6.2 Methods

6.2.1 The study region and site network

Bat surveys were conducted in the same network of 48 sites as the bird surveys.

A description of the site network and study region is provided in Chapter Two (Section

2.2.1). The distribution and clearing history of subtropical rainforest in Australia were

described in Chapter One (Section 1.4.1).

6.2.2 Surveys of frugivorous bat distribution

The occurrence of frugivorous bats was assessed using a single, hour-long

nocturnal search at each site during summer (January-February) 2003. Surveys were

timed to occur during the period of maximum fruit abundance in rainforest in

subtropical Australia (Innis, 1989; Church, 1997). Searches were conducted between

147

one hour after sunset (usually around 8 pm) and 2 am. Two observers searched for bats

(the author and J. Kanowski), each using a spotlight (30 W) and walking slowly for

approximately 400-500 m, usually along a watercourse or path. Bats were located

through movement, calls and foraging sounds, using binoculars for identification when

necessary. Most flying-fox records involved sighting of individuals, although records

were occasionally made from calls. Abundance estimates may consequently have been

biased towards remnant and especially regrowth sites where visibility was greater.

However, presence-absence information would be a reliable measure of site use, since

flying-foxes were usually heard when they alighted in vegetation or when they dropped

or dislodged fruit. Where possible, flying-foxes were identified to species; otherwise the

record was made as ‘Pteropus sp.’ Only large flying-foxes were involved in the

instances of undetermined species, so it was assumed that these were either P.

poliocephalus or P. alecto, since P. scapulatus are noticeably smaller (Hall and

Richards, 2000; personal observation). Some N. robinsoni individuals were both seen

and heard but this species was usually detected by the distinctive, squeaky call which it

emits while flying. Except in the unlikely circumstance that this species has different

calling behaviour between habitat types, presence-absence information for this species

would not be biased toward any particular habitat type.

6.2.3 Frugivorous bird data

The patterns of abundance of frugivorous birds in the same site network were

determined from 40 minute searches of a 1 ha plot at each site, conducted twice in

summer and twice in winter, 2001 by the author (described in Section 2.2.3). Of the 26

bird species that had been recorded frequently enough to assign a fragmentation

response pattern, 14 are known to either destroy seeds (i.e., ‘seed crushers’; e.g., white-

headed pigeon Columba leucomela, Australian king-parrot Alisterus scapulatus) or to

148

consume fleshy fruits only infrequently (e.g., black-faced cuckoo-shrike Coracina

novaehollandiae, Torresian crow Corvus orru (i.e., ‘minor frugivores’)) (Chapter

Three). These species potentially make relatively little contribution to seed dispersal,

either because they do not disperse viable seed or because they consume a small number

of plant taxa (Chapter Four). Therefore, only the remaining 12 bird species that usually

disperse intact seeds and have fruit-dominated or mixed diets are considered in the

present chapter.

6.2.4 Information on the consumption of native plant species by frugivorous bat and

bird species

Information about the fleshy-fruited plant species consumed by the 12

frugivorous bird species, P. poliocephalus, P. alecto and N. robinsoni were obtained

from 130 published sources (Appendix 1) and several unpublished data sets. The data

set containing records of plant species consumption by frugivorous bird species was

described in Chapter Four (Section 4.2.1). The majority of the foraging records for

flying-foxes came from data published by Eby (1995, 1998). Most of the published

foraging records for both birds and bats were obtained from direct field observation

although a relatively small proportion of records were obtained from gut contents, scats,

or regurgitated seeds. There was large variation among frugivore species in the amount

of foraging information available. Except in the case of targeted surveys of particular

frugivore or plant species, records were typically accompanied by minimal information

about the observed interaction, such as details of fruit handling. Records were rejected if

it appeared that the frugivore had not been observed actually consuming the fruit (i.e., it

was only observed in the fruiting plant), or if it was judged from accompanying

information that the interaction was likely to be an instance of fruit theft (consumption

of the flesh without ingesting the seed). Diaspore size (the average width of the

149

functional dispersal unit; see Section 4.2.1) was used to evaluate the likelihood that

flying-foxes would transport the seed away from source plants. Although the size of

fruits that flying-foxes are able to consume is not constrained by their gape width

(Ratcliffe, 1932), their ability to transport seeds is size-limited, since only small seeds

can pass through their gut (c.a. 4 mm for P. poliocephalus (Eby, 1991b)), or be carried

in cheek pouches (c.a. 9 mm (Eby, 1995)). Flying-foxes may also carry larger fruits in

their jaws, but are only likely to transport these over short distances (in the order of

metres) (Ratcliffe, 1932). For the purpose of this work, it was considered that flying-

foxes were potentially able to carry in their cheek pouches diaspores with a maximum

median width of 18 mm, based on the possibility of large intraspecific variation in fruit

size (Edwards, 2005).

Because of the wide geographical range of many of the frugivore species that

occur in subtropical Australia, frugivory records may have been collected from an area

extending from temperate southern Australia to tropical Papua New Guinea, but the

analyses presented here only considered records of the consumption of plant species that

were native to the study region (based on published accounts of plant distribution and

expert advice). Plant taxa included in analyses are listed in Appendix 2. For a given

frugivore species, the data potentially included foraging records from multiple years,

seasons and geographic locations. The data were compiled into a binary matrix showing

whether or not each fleshy-fruited plant species had been recorded in the diet of each of

the frugivore species.

6.2.5 Data handling

Bat distribution in extensive, remnant and regrowth sites

The presence of frugivorous bats (and the abundance of flying-foxes) was (i)

compared across habitat types; and (ii) analysed in relation to environmental attributes

150

of sites (altitude and the presence of a watercourse), which may be related to the

foraging distribution of frugivorous bats Australia (Palmer and Woinarski 1999; Palmer

et al. 2000). I did not attempt to quantify abundance of N. robinsoni as most records

were from calls. For flying-foxes, the abundance measure was the number of individuals

recorded during the hour survey. Log-transformation normalised abundance data for ‘all

flying-foxes’ (i.e., positively identified P. poliocephalus and P. alecto plus unidentified

large flying-foxes), but not for P. poliocephalus alone. Non-parametric statistical tests

were used on raw abundance data for P. poliocephalus.

Patterns of plant species consumption

The number of native plant species, genera and families, the proportion of plant

species with a median diaspore size ≥10 mm, and the average diaspore size of plant

species consumed were calculated for each frugivore species under consideration in the

present work. A dendrogram showing multivariate similarities among the diets of

frugivores (flying-foxes and the 12 frugivorous bird species) was generated using the

UPGMA algorithm and Bray-Curtis similarity metric (Manly 1994) in the statistical

program PRIMER, based on the presence or absence of native plant species in the

frugivores’ diets. Plant species known to be eaten by less than three frugivores were

excluded from this analysis.

6.3 Results

6.3.1 Distribution and abundance of frugivorous bats

Frugivorous bats were recorded in most of the sites surveyed (Table 6.1). P.

scapulatus and S. australis were recorded only once each (both in the same coastal

remnant site); data for these two species are not considered further. While it was often

not possible to distinguish between P. poliocephalus and P. alecto during surveys, many

151

more individuals of P. poliocephalus were positively identified than P. alecto. During

the survey period, P. poliocephalus was recorded in significantly more sites in remnant

and regrowth forest than extensive forest (Table 6.1). The abundance of P.

poliocephalus also varied significantly between site types (Kruskal-Wallis H = 11.17,

d.f .= 2, P = 0.004), being higher in regrowth and remnants than extensive forest (Figure

6.1). The occurrence of ‘all flying-foxes’ (P. poliocephalus, P. alecto and unidentified

large flying-foxes) was not statistically different between site types, although there was

a similar trend to that shown when data for definitely identified P. poliocephalus was

analysed separately (Table 6.1). The abundance of ‘all flying-foxes’ was higher in both

remnant and regrowth forest than in extensive forest (ANOVA F2, 47 =8.99, P=0.001)

(Figure 6.1). N. robinsoni was detected in more extensive forest and remnant sites than

in regrowth (Table 6.1).

Table 6.1 Distribution of frugivorous bats in surveys of extensive, remnant and

regrowth rainforest in the Sunshine Coast, Queensland, Australia. The table shows the

number of sites in which each species was recorded.

Species Total Extensive Remnant Regrowth p (n = 48) (n = 16) (n = 16) (n = 16) P. poliocephalus 25 4 9 12 0.044 P. alecto 3 1 1 1 - Unidentified large flying-foxes 19 7 8 4 - All large flying-foxes1 39 10 15 14 0.064 N. robinsoni2 13 6 6 1 0.025 Any fruit-eating bat3 41 12 15 14 0.314 1 includes unidentified individuals considered to be P. poliocephalus or P. alecto. 2 extensive and remnant sites pooled for statistical test. 3 includes all flying-foxes and N. robinsoni. 4 χ2 test of independence for distribution in different forest types, d.f.=2 5 Fisher’s exact test, regrowth versus extensive and remnant sites

152

Figure 6.1 The abundance (mean ± SE) of flying-foxes recorded during a 60 minute

search of extensive, remnant and regrowth forest sites within the Sunshine Coast,

Queensland, Australia. i) P. poliocephalus; ii) all flying-foxes (grey-headed, black and

unidentified large flying-foxes). Ext = extensive forest, Rem = remnant forest and Reg =

regrowth (n = 16 for each site type). Means with different letters were significantly

different (P<0.05) using: i) Fisher’s exact tests for P. poliocephalus data, and ii) LSD

comparisons for all flying-foxes.

i) P. poliocephalus

0

2

4

6

8A

bun

da

nce

a

b

b

ii) all flying-foxes

0

2

4

6

8

10

Site type

Abun

danc

e

a

b

b

Ext Rem Reg

153

6.3.2 Association of bat distribution with environmental attributes

N. robinsoni was recorded at nine of the 34 sites that contained a watercourse

and four of the 14 sites without, showing no clear association with watercourses (χ2 =

0.02). In contrast, the presence of flying-foxes was strongly associated with

watercourses; P. poliocephalus was present at 24 of the 34 sites with watercourses and

at only one of the 14 sites without (Fisher’s exact test, p<0.001), while ‘all large flying-

foxes’ (P. poliocephalus, P. alecto and unidentified large flying-foxes) were present in

32 of the sites with watercourses and in seven of the sites without (Fisher’s exact test, p

= 0.001). The mean abundance of P. poliocephalus was also higher in sites with a

watercourse (average of 4.1 bats per survey) than in sites without (0.1 bats per survey;

Wilcoxon rank test z = -3.83, p = 0.0001). There was a similar result for ‘all large

flying-foxes’ (5.3 bats per survey in sites with watercourse, 1.5 bats per survey in sites

without; t-test = 3.38, p = 0.001, d.f. = 46).

For N. robinsoni, there was no clear association between altitude and occurrence

within extensive and remnant forest (logistic regression R = -0.13, N = 32, p = 0.09).

This species was recorded at 7 of 13 sites below 200 m, 5 of 13 sites located between

200 and 500 m, and none of six sites above 500 m a.s.l. Similarly, no altitudinal trend

was detected in the distribution of flying foxes within the habitats in which they were

most abundant (remnant and regrowth sites), either in terms of abundance (Pearson’s

correlation coefficient R = -0.15, N = 32, p = 0.21), or presence/ absence (logistic

regression R<0.0001, N = 32, p = 0.28). Flying-foxes were recorded at 16 of the 17

remnant and regrowth sites below 200 m and 13 of 15 sites above 200 m.

154

6.3.3 Comparison between frugivorous bat and bird species in their patterns of plant

species consumption

There were a total of 811 foraging records for birds and bats, from 221 native

species of trees, shrubs, vines and herbs. N. robinsoni had only been positively recorded

feeding on the fruits of four native plant species in subtropical Australia (Table 6.2),

Elaeocarpus grandis (Elaeocarpaceae), Ficus watkinsiana (Moraceae), Endiandra

discolor (Lauraceae) and Melodorum leichardtii (Annonaceae). Several additional plant

species, especially figs, are likely to be consumed by this bat, but as observations had

been recorded only to genus level (e.g., ‘Ficus sp.’), these were not quantifiable in the

present data set. Flying-foxes were known to consume 48 species, 31 genera and 29

families of native plants; values which are moderate in comparison with the ranges

shown by bird species (6 – 106 species, 2 – 89 genera, 3 – 52 families) (Table 6.2).

Flying-foxes were known to consume ten of the 20 plant species in the dataset from the

Myrtaceae, and ten of the 13 species from the Moraceae. For the remaining 27 plant

families known to be consumed by flying-foxes, only one or two plant species had been

recorded.

15

5

Tab

le 6

.2 P

atte

rns

of n

ativ

e pl

ant c

onsu

mpt

ion

for

frug

ivor

ous

bats

and

the

mos

t im

port

ant

frug

ivor

ous

bird

spe

cies

in t

he s

tudy

reg

ion

(see

Sec

tion

6.2.

3). ‘

Av.

dia

s. s

ize’

is th

e av

erag

e si

ze (

mm

) of

dia

spor

es c

onsu

med

. ‘P

rop

cons

f-fo

x’ is

the

prop

ortio

n of

the

plan

ts s

peci

es c

onsu

med

by

each

bird

spe

cies

that

wer

e al

so k

now

n to

be

cons

umed

by

flyin

g-fo

xes.

Fru

giv

ore

sp

ecie

s A

bu

nd

. p

atte

rn1

Nu

mb

er o

f p

lan

t ta

xa

Av.

d

ias.

si

ze2

Pro

p

con

s f-

fox

Sp

ecie

s G

ener

a F

amili

es

≥10

mm

4

Bat

s

Nyc

timen

e ro

bins

oni

4

4 4

3 12

.1

fl

ying

-fox

es P

tero

pus

spp.

48

(44)

31

(3

0)

29

(28)

22

(1

8)

9.5

(7

.8)

B

irds1

w

ompo

o fr

uit-

dove

Ptil

inop

us m

agni

ficus

D

ec

81

56

37

47

10

.1

0.36

s

uper

b fr

uit-

dove

P. s

uper

bus

Dec

26

31

22

13

9.

1 0.

27

ros

e-cr

owne

d fr

uit-

dove

P. r

egin

a D

ec

74

54

32

33

8.8

0.31

g

reen

cat

bird

Ailu

roed

us c

rass

irost

ris

Dec

10

4 77

40

44

9.

1 0.

34

topk

not p

igeo

n Lo

phol

aim

us a

ntar

ctic

us

Tol

73

46

28

42

10

.3

0.36

c

omm

on k

oel E

udyn

amys

sco

lopa

cea

T

ol

25

26

19

6 7.

0 0.

52

cha

nnel

-bill

ed c

ucko

o S

cyth

rops

nov

aeho

lland

iae

T

ol

6 2

3 0

2.0

0.83

L

ewin

’s h

oney

eate

r M

elip

haga

lew

inii

Tol

10

6 89

47

24

6.

7 0.

26

pie

d cu

rraw

ong

Str

eper

a gr

acul

ina

T

ol

50

39

25

18

8.2

0.50

s

atin

bow

erbi

rd P

tilon

orhy

nchu

s vi

olac

eus

Tol

10

6 89

52

48

8.

8 0.

31

figb

ird S

phec

othe

res

virid

is

Inc

74

60

33

22

7.1

0.32

s

ilver

eye

Zos

tero

ps la

tera

lis

Inc

37

39

30

0 4.

5 0.

35

1 Abu

nd. p

atte

rn is

the

abun

danc

e pa

ttern

det

ecte

d fo

r ea

ch b

ird

spec

ies;

Dec

dec

reas

er, T

ol to

lera

nt, I

nc in

crea

ser

(Cha

pter

Tw

o).

2 T

he n

umbe

r of

nat

ive

plan

t spe

cies

that

had

dia

spor

es w

ith a

med

ian

size

of ≥1

0 m

m th

at w

ere

know

n to

be

cons

umed

by

each

fru

givo

re s

peci

es. F

or f

lyin

g-fo

xes,

the

seco

nd

num

ber

(in

brac

kets

) sh

ows

resu

lts

whe

n fr

uits

that

are

too

larg

e to

be

tran

spor

ted

inte

rnal

ly a

re e

xclu

ded.

It w

as c

onsi

dere

d th

at p

lant

spe

cies

wit

h a

med

ian

dias

pore

siz

e up

to 1

8 m

m m

ay b

e tr

ansp

orte

d in

tern

ally

due

to in

tras

peci

fic

vari

atio

n in

fru

it di

men

sion

.

156

The proportion of native plant species with a median diaspore size ≥10 mm that

was consumed by flying-foxes was similar to that consumed by decreaser bird species

(Figure 6.2), although many of these diaspores could only be transported externally by

flying-foxes. The only other non-decreaser frugivore taxa that were known to consume

a similar proportion of plant species with diaspores ≥10 mm were two tolerant bird

species, topknot pigeon L. antarcticus and the satin bowerbird Ptilonorhynchus

violaceus (Table 6.2). Similar patterns were evident when the data were analysed in

terms of: (i) the average size of diaspores consumed by flying-foxes, relative to birds,

and (ii) the number of diaspores with a median width ≥10 mm consumed by flying-

foxes, relative to birds (Table 6.2).

Figure 6.2 The proportion of native plant species with a median diaspore width ≥ 10

mm that were known to be consumed by decreaser (Dec, n=4), tolerant (Tol, n=6) and

increaser (Inc, n=2) bird species, and by flying-foxes (F-foxes). The open circle shows

the proportion of plant species with a median diaspore ≥10 mm that could be

transported internally by flying-foxes, allowing for up to 50% intraspecific variation in

diaspore width.

0

0.2

0.4

0.6

Frugivore group

Pro

p. d

iasp

ores

10

mm

Dec Tol Inc F-foxes

≥

157

Figure 6.3 Classification of frugivore species based on Bray-Curtis dissimilarity metric

using patterns of consumption of native plant species.

Frugivorous bats did not consume a different set of plant species to frugivorous

birds overall; for all of the native plant species known to be consumed by either flying-

foxes or N. robinsoni, at least one of the 12 bird species considered here was also

known to be a consumer. In the multivariate analysis, flying-foxes were not strongly

separated from frugivorous birds based on dietary composition (Figure 6.3). The plant

species that comprised flying-fox diets represented around one-third of the plant species

consumed by most of the frugivorous bird species considered here, including decreaser

bird species (Table 6.3).

silver eye

common koel

channel-billed cukoo

pied currawong

Pteropus

figbird

Lewin's honeyeater

green catbird

satin bowerbird

rose-crowned fruit-dove

wompoo fruit-dove

topknot pigeon

superb fruit-dove

100 80 60 40 20 0

Dissimilarity

silvereyecommon koelchannel-billed cuckoo

pied currawongflying-foxes

figbirdLewin's honeyeatergreen catbirdsatin bowerbirdrose-crowned fruit-dovewompoo fruit-dovetopknot pigeonsuperb fruit-dove

100 80 60 40 20 0

Dissimilarity

158

6.3.4 Potential for frugivorous bat species to substitute for decreaser bird species as

dispersers in fragmented forest

The eastern tube-nosed fruit-bat consumed a very low percentage of the plant

species that were consumed by decreaser bird species. The percentage of plant species

consumed by each decreaser bird species that was known to be consumed by flying-

foxes is shown in Table 6.2; flying-foxes consumed around one-third of the plant

species known from the diets of each decreaser bird species. Neither flying-foxes nor

the eastern tube-nosed bat were known to consume any of the plant species that were

only known from the diets of decreaser species among frugivorous birds (Chapter Five,

Table 5.5). In relation to the plant families that were most frequent in the diets of

decreaser species (and hence predicted to be vulnerable to reduced dispersal in

fragmented rainforest), flying-foxes consumed half of the plant species from Myrtaceae

(10 out of 20). The average number of species from the Myrtaceae consumed by

decreaser bird species was 6.5 (Table 5.2). There were no records of flying-foxes

consuming plants from the Verbenaceae, and they were only known to consume one

species from each Meliaceae (Melia azedarach; out of a total of seven species) and

Lauraceae (Cryptocarya obovata; out of 21 species). Flying-foxes had been recorded

consuming one-third (two out of six) of the plant species from the Vitaceae in the data

set.

6.4 Discussion

6.4.1 The distribution of flying-foxes in fragmented rainforest in the Sunshine Coast

Pteropus poliocephalus and P. alecto are similar in many respects, including

size and reproductive characteristics, communal roosting behaviour (Ratcliffe 1932;

Hall and Richards 2000) and the consumption of both fruit and nectar (Richards and

159

Hall 1998). Because it was not always possible to identify these flying-foxes to species

during surveys for the present work, the two species are henceforth considered

collectively, although it is acknowledged that all comments may not apply equally to

both species. P. scapulatus is not included in subsequent uses of the term ‘flying-foxes’

in the context of the present work.

During surveys for this work, flying-foxes were recorded foraging in most of the

48 sites across all three habitat types. They were not restricted to extensive forest, and

used remnants and regrowth, despite their relatively small size and isolation and any

floristic and structural differences between the site types. The ability of flying-foxes to

use fragmented habitats may be due, in part, to their mobility over large geographic

areas. P. poliocephalus has been recorded travelling tens of kilometres from daytime

roosts to forage in multiple feeding areas (Eby, 1991b; Spencer et al,. 1991). This is in

contrast to the Philippines were large flying-foxes have been reported to have

comparatively restricted foraging ranges (0.4 to 12 km) and apparently avoid disturbed

habitats in agricultural areas (Mildenstein et al., 2005). The capacity of Australian

flying-foxes to routinely traverse large distances would readily enable movement

between most forest patches in the Sunshine Coast, including those that have been

isolated by clearing. Australian flying-foxes also forage in a range of forest types,

including rainforest, eucalypt forests, paperbark and mangrove forests (Ratcliffe, 1932;

Eby, 1995). Their diets are fairly broad and comprise nectar, pollen and fruit from a

range of flowering and fruiting plant species, genera and families (Parry-Jones and

Augee, 1991; Eby, 1998; Southerton et al., 2004). Similarly, generalist patterns of forest

and food resource use by Neotropical phyllostomid bats in Brazil are associated with

higher abundance in fragmented and modified habitats, compared with specialist bat

taxa (Marinho-Filho and Sazima, 1998).

160

During the period of the surveys conducted for the present study, flying-foxes

were recorded in higher frequency and abundance in remnant and especially regrowth

rainforest sites compared with extensively forested areas. Since the distribution of

flying-foxes is known to correspond with localised food availability (Eby, 1991a; Parry-

Jones and Augee, 1992; Palmer et al., 2000), the relatively high numbers observed in

remnants and regrowth probably reflected fruit availability in these sites at this time.

During surveys, most observations of foraging flying-foxes in all three site types were at

native sandpaper figs, especially Ficus coronata. These figs appeared to be especially

common in regrowth sites, and are associated with early stages of rainforest regrowth in

subtropical Australia (Kooyman, 1996).

The capacity to infer general patterns of flying-fox distribution from the survey

conducted for this work is limited. This is due to the combination of a temporally

restricted survey effort, and the potential for the geographic distribution of nomadic

flying-foxes in eastern Australia to vary considerably with the availability of ephemeral

food resources (Nelson, 1965; Parry-Jones and Augee, 1992; Eby, 1995). Many daytime

roost sites are located in small remnants and regrowth vegetation in extensively-cleared

parts of the region (Roberts, 2005) and flying-foxes forage and roost in vegetation in

urban landscapes elsewhere in Australia (Parry-Jones and Augee, 1991; Markus, 2004;

McDonald-Madden et al., 2005)

However, while flying-foxes may make use of fragmented and disturbed

rainforest habitats in the Sunshine Coast, they apparently have not benefited at a

population level from such changes to the landscape. As is the case for Pteropid

populations throughout the Old World tropics (Fujita and Tuttle, 1991), flying-fox

numbers are declining in subtropical Australia (Lunney and Moon, 1997; Eby et al.,

1999; Eby and Lunney, 2002; Dickman and Fleming, 2002). Declines were reported by

the early part of the 20th century as a result of habitat loss and persecution (Ratcliffe,

161

1932). Although they use rainforest, including disturbed habitats, flying-foxes

(particularly P. poliocephalus) appear to depend on nectar resources for at least part of

the year (Ratcliffe, 1932; Eby et al., 1999; Southerton et al., 2004). Hence, clearing of

large tracts of nectar-producing open forests in south-east Queensland (Catterall et al.,

1997) would have removed resources that may be critical for maintaining flying-fox

populations (Eby et al., 1999). Consequently, even a scenario of increased extent of

rainforest regrowth would be unlikely to compensate for the loss of seasonally-

important nectar resources in terms of maintaining flying-fox populations.

Flying-foxes were more abundant in sites associated with a watercourse than in

‘dry’ sites. This may reflect their use of Ficus coronata as a major food resource at the

time of surveys, since these plants tend to occur most abundantly close to water (Floyd,

1989). However, watercourses are also strongly associated with the location of flying-

fox colonial day roosts (‘camps’) in south-east Queensland (Roberts, 2005), and may be

used by flying-foxes to navigate through the landscape (Palmer and Woinarski, 1999).

Hence, flying-fox foraging activity in the Australian subtropics may generally be

concentrated in vegetation along drainage lines, as has been described for P. alecto in

the monsoonal forests of northern Australia (Palmer et al., 2000), for Pteropus spp. in

the Philippines (Mildenstein et al., 2005) and for frugivorous bats in Mexico (Galindo-

González and Sosa, 2003). Although flying-fox camps in south-east Queensland are

mostly restricted to low altitudes (below 120 m a.s.l., Roberts, 2005), foraging is not

confined to lowland rainforest in the Sunshine Coast.

6.4.2 The distribution of the eastern tube-nosed fruit-bat in fragmented rainforest in

the Sunshine Coast

Nyctimene robinsoni was recorded in 13 of the 48 subtropical rainforest sites in

the study region. Previous reports have suggested that the geographical range of N.

162

robinsoni in Australia is mostly tropical, based on infrequent records of this species

from subtropical rainforests (Hall and Richards, 1979; Milledge, 1987; Hall et al.,

1995). However, the surveys conducted for the present study indicate that it may be

more common in subtropical rainforest than previously thought, at least in the study

region.

N. robinsoni was recorded more frequently in extensive and remnant rainforest

than in regrowth sites. In contrast with flying-foxes and the frugivorous bird species that

showed tolerant or increaser abundance patterns (Chapter Two), N. robinsoni depends

on rainforest, mostly consumes fruit, and makes only limited foraging movements

(Spencer and Fleming, 1989; Hall and Richards, 2000). These attributes were also

typical of the frugivorous bird species that were less common in remnants and regrowth

than in extensive forest in the study region. These characteristics were also associated

with the bat species that had restricted distribution in fragmented forests in the neo-

tropics (Cosson et al., 1999). The physical separation of remnants did not prevent their

use by N. robinsoni. The low frequency of this species in regrowth patches may have

been a result of insufficient availability of food plants and the small size of these sites

(see Chapter Two, Section 2.2.2 for description of characteristic floristics of regrowth in

relation to remnants and extensive forest). Given the habitat specialisation of N.

robinsoni, coupled with its apparent preference for mature rainforest rather than

regrowth, rainforest clearing must have substantially reduced the extent of suitable

habitat and is likely to have led to reduced populations of this species.

6.4.3 The potential for seed dispersal by frugivorous bats in remnants and regrowth:

comparison with frugivorous birds

Both N. robinsoni and flying-foxes potentially disperse seeds in fragmented

subtropical rainforest. N. robinsoni probably only disperses a small number of plant

163

species, and may disperse few seeds into or within patches of regrowth. In contrast,

flying-foxes are known to consume at least one-third of the native plant species

consumed by decreaser bird species. Since opportunistic observation of the foraging

patterns of night-feeding flying-foxes would be lower than for diurnal birds, the actual

proportion may be higher than reported here. Hence, flying-foxes have the potential to

at least partially compensate for decreaser bird species with respect to the dispersal of

rainforest plant species. For example, only a few frugivorous bird species,

predominantly decreasers, consume high numbers of native plant species from the

Myrtaceae in subtropical Australia (Chapter Five). However, flying-foxes are also

known to consume many plant species from the Myrtaceae (Eby, 1995; this study) and

may help maintain dispersal of these plants in fragmented parts of the landscape.

In addition to consuming the fruits of a particular plant, the potential of a

frugivore to disperse seeds between fragmented habitats is influenced by its foraging

and ranging behaviour, combined with its gut passage rate (Schupp, 1993; Wenny and

Levey, 1998; Loiselle and Blake, 2002). Flying-foxes may consume fruits within the

source plant and drop the seeds beneath the crown of the parent. Alternatively, flying-

foxes may transport seeds relatively short distances away from parent plants by flying to

a nearby tree to consume harvested fruits, behaviour which may be particularly common

when other foraging flying-foxes are present (Richards, 1990). In addition, P.

poliocephalus may move continually between successive feeding trees, sometimes over

several kilometres, including across cleared land (Eby, 1991b). Hence, flying-foxes

potentially disperse seeds both within and between extensive forest, remnant and

regrowth patches. Many frugivorous bird species also routinely travel across cleared

land between forest areas in subtropical Australia, and may play a similar role in seed

dispersal in fragmented parts of the landscape. However, birds tend to eliminate seeds

while perched (McDonell and Stiles, 1983). In contrast, frugivorous bats may also

164

defecate in flight (Charles-Dominique, 1986), and hence potentially disperse seeds to

cleared areas as well as areas with standing vegetation. Work in West Africa (Thomas,

1982) and Mexico (Medellín and Gaona, 1999; Galindo-González and Sosa, 2003) has

shown that frugivorous bats are responsible for the majority of seed input to cleared

land, while birds make little contribution to seed input in these areas, although the

reverse has been found in the Philippines (Ingle, 2003).

The frugivorous bird species that decline in remnants and regrowth in the

Sunshine Coast consume many large-fruited plant species. Nevertheless, flying-foxes,

along with two tolerant bird species topknot and satin bowerbird, may disperse large-

seeded plant species in fragmented parts of subtropical Australia. However, while

flying-foxes can carry fruits as large as mangoes in their jaws or claws (Ratcliffe, 1932),

they spit out or drop most large seeds close to the parent tree (van der Pijl, 1982; Eby,

1995; McConkey and Drake, 2002; Meehan et al., 2005). Longer distance dispersal may

be restricted to small seeds that can be transported internally in the gut, or possibly

cheek pouches. Indeed, Pteropid fruit bats may potentially disperse some very small

seeds over hundreds of kilometres (Shilton et al., 1999). Hence, although flying-foxes

potentially disperse large seeds a short distance away from the source tree, they may

contribute relatively little to the dispersal of large seeds between distant forest patches

or regenerating areas.

Although flying-foxes do not consume different plant species to frugivorous

birds in subtropical Australia (c.f., Fleming et al., 1987; Richards, 1990; Gorchov et al.,

1995; Hamann and Curio, 1999; Bollen et al., 2004), they potentially have a distinctive

role as dispersers of rainforest plants in deforested parts of the landscape. This is

because of their use of fragmented rainforest, mobility over long distances, ability to

defecate seeds in treeless areas, and consumption of a large number of plant species

from the Myrtaceae.

165

Chapter 7

General discussion: Consequences of forest fragmentation for

frugivores and implcations for seed dispersal

7.1 Summary of the findings of this thesis

This thesis has evaluated consequences of forest fragmentation for fauna and the

potential for impacts on higher order interactions. Specifically, this work has assessed

changes in the abundance and distribution of frugivorous vertebrate species in a

fragmented rainforest landscape and evaluated the functional roles of frugivore species

to make predictions regarding potential changes in the process of seed dispersal in

fragmented rainforest.

The salient findings of each chapter of this thesis are summarised in Table 7.1.

Frugivorous bird and bat species showed varied responses to rainforest fragmentation

(Chapters 2 and 6). The abundance of a subset of frugivorous species was lower in

fragmented compared with extensive rainforest. Frugivorous bird species that declined

in fragmented rainforest habitats shared similar functional traits (Chapter 3). There was

a strong association between functional attributes of frugivores and their actual patterns

of plant species consumption (Chapter 4). A substantial proportion of native rainforest

plant species may be dispersed solely or predominantly by the frugivore species that

declined in fragmented forest landscapes (Chapters 5 and 6). It was predicted that

dispersal of these plant species in fragmented habitats would depend on only a small

subset of frugivore species, and consequently that regeneration of these plants would be

reduced in fragmented forest.

166

Tab

le 7

.1 S

umm

ary

of th

e sc

ope

and

maj

or f

indi

ngs

of th

e co

mpo

nent

stu

dies

rep

orte

d in

the

chap

ters

of

this

thes

is.

Fo

cus

Ke

y fi

nd

ing

s C

hap

ter

2 A

sses

smen

t of

the

abun

danc

e of

frug

ivor

ous

bird

spe

cies

in fr

agm

ente

d an

d ex

tens

ive

fore

st.

For

ty-t

wo

subt

ropi

cal A

ustr

alia

n bi

rd s

peci

es a

re a

t lea

st p

artly

frug

ivor

ous.

Fie

ld s

urve

ys d

ocum

ente

d th

ree

gene

ral

abun

danc

e pa

ttern

s am

ong

the

26 m

ost c

omm

on fr

ugiv

orou

s bi

rd s

peci

es: d

ecre

aser

(ab

unda

nce

low

er in

rem

nant

an

d/or

reg

row

th th

an in

ext

ensi

ve fo

rest

(fiv

e sp

ecie

s), i

ncre

aser

(ab

unda

nce

high

er in

rem

nant

and

/or

regr

owth

than

ex

tens

ive

fore

st (

seve

n sp

p.),

and

tole

rant

(ab

unda

nce

sim

ilar

acro

ss s

ite ty

pes

(14

spp.

)). R

espo

nse

patte

rns

wer

e ge

nera

lly c

onsi

sten

t bet

wee

n se

ason

s. F

urth

erm

ore,

the

abun

danc

e o

f fru

givo

rous

bird

spe

cies

in e

xten

sive

fore

st a

t di

ffere

nt a

ltitu

des

(low

(<

200

m a

.s.l.

), m

ediu

m (

200-

500

m a

.s.l.

) an

d hi

gh (

>50

0 m

a.s

.l.))

did

not

var

y be

twee

n se

ason

s.

C

hap

ter

3 A

sses

smen

t of

the

func

tiona

l rol

es o

f bird

sp

ecie

s an

d po

tent

ial

chan

ges

in s

eed

disp

ersa

l in

frag

men

ted

fore

st.

The

bird

trai

ts p

ropo

sed

to s

tron

gly

influ

ence

a s

peci

es’ s

eed

disp

ersa

l pot

entia

l wer

e ga

pe w

idth

(sm

all,

med

ium

, la

rge)

, fru

givo

ry le

vel (

maj

or, m

ixed

-die

t and

min

or fr

ugiv

ores

) an

d se

ed tr

eatm

ent (

seed

-dis

pers

ers

and

seed

-cr

ushe

rs).

Tes

ts s

how

ed th

at d

ecre

aser

bird

spe

cies

tend

ed to

be

seed

-dis

pers

ing

maj

or fr

ugiv

ores

with

larg

e or

m

ediu

m g

apes

. It w

as p

redi

cted

that

this

wou

ld r

esul

t in

redu

ced

disp

ersa

l of

plan

t spe

cies

with

larg

e fr

uits

and

from

La

urac

eae.

Ch

apte

r 4

Tes

t of t

he

asso

ciat

ion

betw

een

patte

rns

of p

lant

spe

cies

con

sum

ptio

n an

d th

e tr

aits

iden

tifie

d in

C

hapt

er 3

.

The

ave

rage

siz

e of

frui

ts c

onsu

med

by

a bi

rd s

peci

es in

crea

sed

with

gap

e w

idth

, exc

ept f

or m

inor

frug

ivor

es. M

inor

fr

ugiv

ores

con

sum

ed s

mal

l fru

its, i

rres

pect

ive

of th

eir

gape

wid

th. M

ajor

and

mix

ed-d

iet f

rugi

vore

s co

nsum

ed a

hig

her

num

ber

of p

lant

spe

cies

than

min

or fr

ugiv

ores

. The

die

ts o

f min

or fr

ugiv

ores

and

bird

spe

cies

with

sm

all g

apes

mos

tly

com

pris

ed p

lant

spe

cies

from

the

Mor

acea

e an

d E

upho

rbia

ceae

. Am

ong

the

spec

ies

with

gap

es w

ider

than

10

mm

, m

ajor

frug

ivor

es c

onsu

med

the

high

est n

umbe

r of

nat

ive

plan

t spe

cies

from

the

fam

ily L

aura

ceae

, whe

reas

mix

ed-

diet

frug

ivor

es c

onsu

med

the

high

est n

umbe

r of

spe

cies

from

the

Cel

astr

acea

e, M

imos

acea

e, S

apin

dace

ae a

nd

Sm

ilaca

ceae

.

Ch

apte

r 5

Eva

luat

ion

of th

e po

tent

ial f

or c

hang

ed s

eed

disp

ersa

l in

frag

men

ted

rain

fore

st la

ndsc

apes

, usi

ng

info

rmat

ion

on p

atte

rns

of

plan

t spe

cies

con

sum

ptio

n by

frug

ivor

e sp

ecie

s,

toge

ther

with

dat

a on

thei

r re

spon

se to

frag

men

tatio

n (C

hapt

er 2

)

The

re w

as c

onsi

dera

ble

over

lap

in th

e di

et o

f fru

givo

re s

peci

es th

at s

how

ed d

iffer

ent r

espo

nses

to fr

agm

enta

tion.

H

owev

er, t

here

wer

e no

kno

wn

tole

rant

or

incr

ease

r di

sper

sers

for

12%

of t

he n

ativ

e pl

ant s

peci

es in

the

data

set

. T

his

incl

uded

sev

eral

spe

cies

from

the

Rub

iace

ae. I

t was

pre

dict

ed th

at d

ispe

rsal

of t

hese

pla

nt s

peci

es w

ould

be

seve

rely

red

uced

in fr

agm

ente

d ra

info

rest

. In

addi

tion,

dec

reas

ers

cons

umed

the

high

est n

umbe

r of

pla

nt s

peci

es

with

frui

ts ≥

10 m

m in

dia

met

er, a

nd o

f pla

nt s

peci

es fr

om th

e La

urac

eae,

Mel

iace

ae, M

yrta

ceae

, Ver

bena

ceae

and

V

itace

ae. O

nly

a sm

all n

umbe

r of

oth

er b

ird s

peci

es c

onsu

med

sim

ilar

num

bers

of t

hese

pla

nt ta

xa. I

t was

pre

dict

ed

that

dis

pers

al o

f the

se p

lant

s w

ould

be

subs

tant

ially

red

uced

in fr

agm

ente

d ra

info

rest

. Inc

reas

er fr

ugiv

ores

had

lim

ited

pote

ntia

l to

subs

titut

e fo

r de

crea

sers

as

seed

dis

pers

ers

in fr

agm

ente

d fo

rest

.

16

7

Fo

cus

Ke

y fi

nd

ing

s C

hap

ter

6 A

sses

smen

t of

the

dist

ribut

ion

of fr

ugiv

orou

s ba

t spe

cies

in fr

agm

ente

d an

d ex

tens

ive

fore

st.

Eva

luat

ion

of th

eir

pote

ntia

l to

dis

pers

e th

e pl

ant

spec

ies

cons

umed

by

‘dec

reas

er’ b

ird

spec

ies.

Thr

ee fr

ugiv

orou

s ba

t spe

cies

occ

ur in

rai

nfor

ests

of s

ubtr

opic

al A

ustr

alia

. Fly

ing-

foxe

s us

ed a

ll th

ree

habi

tats

stu

died

(in

tact

, rem

nant

and

reg

row

th r

ainf

ores

t), w

here

as th

e ea

ster

n tu

be-n

osed

bat

was

larg

ely

rest

ricte

d to

ext

ensi

ve a

nd

rem

nant

fore

st. T

he d

istr

ibut

ion

of fl

ying

-fox

es, b

ut n

ot th

e ea

ster

n tu

be-n

osed

bat

, was

pos

itive

ly a

ssoc

iate

d w

ith

wat

erco

urse

s. F

rugi

voro

us b

ats

used

rai

nfor

est a

t all

altit

udes

. The

pla

nt s

peci

es c

onsu

med

by

frug

ivor

ous

bats

wer

e al

so c

onsu

med

by

frug

ivor

ous

bird

spe

cies

. Fly

ing-

foxe

s po

tent

ially

sub

stitu

te fo

r de

crea

sers

as

disp

erse

rs o

f pla

nt

spec

ies

with

larg

e fr

uits

and

from

the

Myr

tace

ae in

frag

men

ted

part

s of

the

land

scap

e, a

lthou

gh th

ey m

ay n

ot

disp

erse

frui

ts >

9 m

m v

ery

far

from

par

ent t

rees

.

168

7.2 The sensitivity of frugivorous vertebrate species to rainforest

fragmentation in subtropical Australia

There have been no previous assessments of effects of forest fragmentation

across a regional frugivore assemblage in Australia. However, some of the frugivore

species that were evaluated in the present work had been included in other studies of

faunal change in fragmented landscapes. These studies provide an opportunity to asses

whether the species’ response patterns detected in the present study may be consistent

among regions or at different times. The locations of the studies that have been

conducted in Australia are shown in Figure 7.1.

Decreaser species

In the present study, the abundance of five bird species, and the occurrence of

the eastern tube-nosed bat, was lower in fragmented than in extensive rainforest. Three

bird species, all seed-dispersing Columbidae from the genus Ptilinopus (wompoo,

superb and rose-crowned fruit-doves), showed a clear reduction in abundance in

rainforest fragments compared with extensive forest. They were also absent from most

of the isolated regrowth patches surveyed for this study. Similarly, Howe et al. (1981)

only once recorded the wompoo fruit-dove during surveys of small rainforest remnants

in the Dorrigo region, while Warburton (1997) reported that both the wompoo and

superb fruit-doves were relatively uncommon in small remnants in the Wet Tropics. In

contrast, it has been reported that Ptilinopus species are widespread in fragmented

rainforest landscapes in the Big Scrub region (Gosper and Holmes, 2002). It has been

postulated that extensive patches of advanced regrowth dominated by the fleshy-fruited,

introduced species camphor laurel Cinnamomum camphora may facilitate the use of

fragmented rainforest landscapes in the Big Scrub region by these species (Date et al.,

1996; Gosper and Holmes, 2002; Neilan et al., 2006). The present work showed that, in

169

the Sunshine Coast region, Ptilinopus species made limited use of regrowth, including

patches dominated by C. camphora. However, patches of C. camphora are far more

extensive in the Big Scrub region than in other parts of Australia (Scanlon et al., 2000)

and provide a high degree of forest cover in a formerly highly cleared landscape.

Figure 7.1 Map of Australia showing the approximate location of other studies in

fragmented forest that have included frugivore species. Rainforest is shown in red.

(Source of base map: National Land and Water Resources Audit, 2001). The star

shows the location of the present study.

Outside Australia, Ptilinopus species have been reported to be sensitive to forest

clearing on Pacific Islands (Steadman and Freifeld, 1998; McConkey and Drake, 2002)

and in parts of south-east Asia (Hamann and Curio, 1999; Kitamura et al., 2002),

although hunting has also been implicated in these declines. Species in the Columbidae

were detected in relatively low numbers in rainforest fragments during surveys in

Tanzania (genus Columba; Cordeiro and Howe, 2001), but at least some Columbid

species persist in fragmented rainforest landscapes in the Indo-Malaysian region

(Corlett, 1998).

Crome et al., (1994) Warburton (1997)

McDonald-Madden et al. (2005)

Eby, 1991a Date et al. (1996) Gosper and Holmes (2002) Neilan et al. 2006)

Howe et al. (1981)

Wet Tropics

Sunshine Coast

Big Scrub Dorrigo

170

In the present study, three frugivore species, the brown cuckoo-dove

(Columbidae), green catbird (Ptilonorhynchidae) and eastern tube-nosed bat

(Pteropidae) had similar numbers in extensive forest and remnants, but much lower

abundance or frequency of occurrence in regrowth. To my knowledge, there have been

no other studies of the eastern tube-nosed fruit-bat in fragmented landscapes. Consistent

with the results of the present study, the frequency of the brown-cuckoo-dove was

similar between remnants and extensive forest in studies in the Big Scrub (Date et al.,

1996) and Wet Tropics (Warburton, 1997). Neilan et al. (2006) reported that the brown

cuckoo-dove was common in regrowth patches adjacent to extensive forest in the Big

Scrub region, but that this species was uncommon in regrowth sites distanced from

extensive forest.

The two other studies of the distribution of the endemic green catbird in

fragmented forest landscapes have reported divergent patterns from those documented

in the present study. The first (Howe et al., 1981) reported very low abundance in

remnants in the Dorrigo region (i.e., greater sensitivity to fragmentation than reported

here), while the second (Neilan et al., 2006) reported high abundance in regrowth

patches in the Big Scrub region (i.e., greater tolerance of fragmentation than detected in

the present study). In the case of the remnants studied by Howe et al. (1981), many sites

may have been too small (0.1-2.5 ha) for this species to maintain a territory (average 2.1

ha; Innis and McEvoy, 1992). The greater resilience of the green catbird in the Big

Scrub region mirrors the trend already described for other decreaser bird species, and

may at least partly be attributed to the more extensive occurrence of advanced regrowth

in that region.

171

Tolerant species

Fifteen vertebrate frugivore taxa (14 bird species and Pteropid flying foxes)

showed similar abundances across extensive, remnant and regrowth in the study region.

Among these tolerant species was the topknot pigeon, the only seed-dispersing

Columbid species that did not decrease in fragmented rainforest in the study region. The

topknot pigeon is also widespread in fragmented landscapes in the Big Scrub region

(Date et al., 1996; Neilan et al., 2006), but its numbers were much lower in small

remnants than in nearby extensive forest in the Dorrigo area (Howe et al., 1981). In the

Wet Tropics, this species occurred only infrequently in remnants smaller than 30 ha

(Warburton, 1997).

In agreement with the classification of the satin bowerbird as tolerant in the

present study, this species occurred in most of the small remnants surveyed in the

Dorrigo region by Howe et al. (1981). However, in the Wet Tropics, Warburton (1997)

reported strongly decreased abundance of the satin bowerbird in remnants smaller than

around 660 ha. However, this species occupies highland rainforest in north Queensland

(Nix and Switzer 1991), and its low incidence in the remnants surveyed by Warburton

may have been the result of the lower altitude of smaller remnants, rather than their

decreased size. The satin bowerbird was uncommon in the regrowth sites surveyed in

the Big Scrub region by Neilan et al. (2006), whereas it may have been expected to be

more widespread if it were tolerant of fragmentation.

Consistent with the present study, the Lewin’s honeyeater and pied currawong

were recorded in all (or almost all) of the remnant and regrowth sites surveyed

respectively by Warburton (1997) and Neilan et al. (2006). The white-headed pigeon,

emerald dove and Australian king-parrot occurred in most of the rainforest remnants

surveyed in the Big Scrub by Date et al. (1996) and/ or in the Wet Tropics by

Warburton (1997). These species, as well as the Australian brush turkey were also

172

frequently recorded in regrowth patches in the Big Scrub region by Neilan et al. (1996).

There have been no other studies of the fragmentation sensitivity of the common koel,

but a congeneric species, Eudynamys cyanocephala, also uses fragmented forest

landscapes in south east Asia (Corlett and Ko, 1995).

Australian flying-foxes are known to range widely in fragmented forest

landscapes (Eby, 1991a; McDonald-Madden et al., 2005). Outside Australia, the

distribution of flying-foxes appears to be limited in fragmented forest landscapes

(Mildenstein et al., 2005), although increased hunting and persecution of flying-foxes

have typically accompanied forest loss and fragmentation in these areas (Cox et al.,

1991; Corlett, 1998; McConkey and Drake, 2002). Use of modified parts of the

Sunshine Coast landscape by flying-foxes may reflect reduced levels of persecution

since 1995 (Eby and Lunney, 2002).

Increaser species

In the present study, the bar-shouldered dove only occurred in remnants and

regrowth sites. Similarly, Date et al. (1996) detected this species in remnants but not in

extensive forest in the Big Scrub. While the figbird was moderately common in the

extensive and remnant forests surveyed for the present study, it was very abundant in

the regrowth sites surveyed. Similarly, this species was common in regrowth in the Big

Scrub region (Neilan et al., 2006), and occurred in the fragments and planted

windbreaks assessed in the Wet Tropics by Crome et al. (1994). In contrast, the

incidence of the figbird was relatively low in the smallest fragments surveyed by

Warburton (1997) in the Wet Tropics. As in the present study, the Torresian crow and

silvereye were common in regrowth in the Big Scrub (Neilan et al., 2006), and the

silvereye was present in rainforest fragments in the Wet Tropics (Crome et al., 1994).

173

White-eyes (Zosteropidae) also appear to be tolerant of forest fragmentation in Asia

(Corlett, 1998).

In summary, frugivore species that were classified as increasers in the present

study have generally also been reported to be widespread in fragmented rainforest

landscapes in other parts of Australia. However, for decreasers and certain tolerant

species, there was considerable variation among studies in the reported consequences of

forest fragmentation. In particular, decreaser species may be more widespread in the Big

Scrub region than in the Sunshine Coast, possibly due to the extent of advanced

regrowth in the former. Although classified as tolerant species in the present study, the

topknot pigeon, satin bowerbird and flying-foxes showed sensitivity to forest

fragmentation in certain studies in other regions.

7.3 Correlates of frugivore species’ sensitivity to rainforest

fragmentation

This thesis has shown large interspecific variation in sensitivity to forest

fragmentation within the broadly defined frugivore guild in subtropical Australia. There

is also variation among frugivore species in their responses to forest fragmentation in

other regions (e.g., Restrepo et al., 1997; Corlett, 1998; Luck and Daily, 2003).

Understanding species’ characteristics associated with different responses to

fragmentation may improve our predictive capacity in relation to the biological

consequences of forest clearing and fragmentation (Henle et al., 2004). Because most

studies of the consequences of forest fragmentation for frugivores have not evaluated

species-specific responses, there is limited understanding of the general profile of a

fragmentation-sensitive frugivore species. Although the present study was not explicitly

deigned to test correlates of susceptibility to fragmentation, the community-wide data

174

set provides an opportunity to assess whether certain factors were clearly correlated

with variation in species’ responses to forest fragmentation.

As proposed by Henle et al. (2004) and reviewed in Chapter One of this thesis

(Section 1.5), a species’ sensitivity to forest fragmentation is likely to be influenced by

combinations of demographic traits (particularly population size and variability,

dispersal power and generation time), and ecological traits (specialised patterns of

microhabitat and matrix use and biogeographical distribution). Specific demographic

data were unavailable for most of the species in the present study, but information on

their ecological traits was generally accessible. Thus, information on body size,

biogeographical position, rarity and patterns of resource use of frugivore species (see

Appendix 3) were evaluated with respect to their sensitivity to rainforest fragmentation

in subtropical Australia.

In summary, of the factors examined, specialised patterns of resource use were

most closely associated with sensitivity to fragmentation (see analyses in Appendix 3).

Specifically, frugivorous bird and bat species that were sensitive to forest fragmentation

were rainforest-dependent fruit-specialists. In contrast, species that used open eucalypt

forest or a variety of forest types, or that consumed fruit as well as other food types

were more likely to be tolerant or to show increased abundance in fragmented

rainforest. This is consistent with results from other regions (Kattan et al., 1994;

Castelletta et al., 2000). For example, bird species that consumed one type of food went

extinct more rapidly in Singapore than species that consumed multiple food types (e.g.,

Castelletta et al., 2000). Rainforest-dependent bird species were also more sensitive to

rainforest fragmentation than species that used a variety of forest types in the Australian

Wet Tropics (Crome et al., 1994; Warburton, 1997). Contrary to findings in other

regions (e.g., Restrepo et al., 1997; Renjifo, 1999), large body size was not associated

with sensitivity to forest fragmentation.

175

An exception to the general profile of fragmentation-sensitive species presented

above may be the topknot pigeon. The topknot pigeon is a rainforest and fruit-specialist

that was classified as tolerant in the present study, although this species has shown

fragmentation sensitivity in some other regions (Howe et al., 1981; Warburton, 1997).

The topknot pigeon differs from the rainforest- and fruit-specialist decreaser species in

its frequent aggregation into large flocks (50 to hundreds of individuals), whereas the

decreaser pigeon species mostly forage alone or in pairs (Frith, 1982; Westcott and

Dennis, 2006). Gregarious foraging behaviour may reduce risk of predation (Pulliam,

1973; Howe, 1979; Watson et al., 2007), and hence increase a species’ willingness to

traverse the non-forest matrix. Thus, the profile of a fragmentation-sensitive frugivore

species may include non-gregarious foraging behaviour, at least in subtropical

Australia.

7.4 Patterns of plant species consumption across the frugivore

assemblage: an alternative model

Frugivory level, gape width and seed treatment were associated with variation

among frugivorous bird species in their patterns of plant species consumption (Chapter

4). In Figure 7.2, I propose a model of the relationships between bird attributes and

major dimensions of dietary variation in subtropical Australian rainforest. To my

knowledge, this has been the first assessment of patterns of plant species consumption

based on information for individual frugivore species across an entire assemblage of

frugivorous rainforest birds. This is also the first community-wide evaluation of

associations among frugivore species’ attributes and their patterns of consumption of a

large number of plant species.

176

Figure 7.2 A model of variation in patterns of plant species consumption by frugivorous

bird species in subtropical Australia. The outer frame represents all available plant

species and the inner frames represent the division of these plant resources by

frugivore species. Arrows show the groups of plant taxa consumed by each frugivore

group. The vertical arrow shows that an increasing number of frugivore species

consumes plant taxa in lower sections of the frame. *The major frugivore classification

may include species that are seasonally highly frugivorous but have mixed diets during

other times of the year.

The conceptual model presented in Figure 7.2 synthesises the variation among

frugivore species that has been shown in the present study (see especially Tables 4.3,

4.4 and 4.5 and Figure 4.5). Plant taxa that contributed to the distinctions between bird

groups classified in Chapter Four (Figure 4.5, Table 4.5) have been used to illustrate the

structure of frugivore-plant interactions in subtropical Australia. For example, Group A

comprises the Lauraceae, Burseraceae, Ebenaceae and Vitaceae, which were mostly

consumed by highly frugivorous bird species with gapes wider than 10 mm. Group B

includes plant taxa that distinguished mixed-diet frugivores (gapes >10 mm) from other

Mixed-diet frugivores (>10 mm gapes)

Major frugivores* (>10 mm gapes)

GROUP C Larger fruits (>10 mm), Araliaceae, Arecaceae

GROUP A Lauraceae, Burseraceae, Ebenaceae, Vitaceae

GROUP B Mostly arillate fruits from Sapindaceae, Celastraceae Mimosaceae, Elaeocarpaceae

Small-gaped and/or seed-crushing major and mixed-diet frugivores

Most minor frugivores, a small number of major and mixed-diet frugivores

GROUP E Moraceae

GROUP D Small fruits (<10 mm) e.g., Euphorbiaceae, Solanaceae, certain Sapindaceae

Incr

easi

ng n

umbe

r of

frug

ivor

e sp

ecie

s

177

bird species; these are mostly arillate fruited species from Sapindaceae, Mimosaceae

and Celastraceae. Plant taxa represented as Group C (Araliaceae, Arecaceae) in Figure

7.2 were consumed by both of these groups of bird species, but generally not by minor

frugivores, bird species with small gapes or by seed-crushing species. Although most

frugivorous bird species consumed Moraceae (Chapter Four, Table 4.3), bird species in

Group D may also consume small-fruited pioneer taxa (e.g., Euphorbiaceae), whereas

the minor and other frugivore species in Group E may have had fig-dominated diets

(Figure 7.2).

Although patterns of plant species consumption across this frugivore community

did not conform neatly to any of the existing models of plant species consumption

(Section 1.2, Figure 1.2), elements of all of these models may describe components of

the model presented in Figure 7.2. For example, certain small fruited plant species

(Group D) and figs (Group E) were consumed by most frugivorous birds, despite

variation among species in their gape width, frugivory level or seed treatment (Figure

7.2). A neutral model of plant-frugivore interactions, as proposed by Burns (2006), may

describe patterns of consumption of these plant species. However, the dichotomous

consumption of plants in Groups A and B by major and mixed-diet frugivores

respectively may more closely resemble the pattern proposed by McKey (1975).

Contrary to initial predictions (McKey, 1975), the differences are not based on strict

lipid or carbohydrate preferences. Furthermore, this dietary distinction was only evident

in a portion of the diets of major and mixed-diet frugivores; species from both groups

consumed several other plant taxa (e.g., Group C in Figure 7.2), despite their different

degrees of frugivory.

It is possible that, for major and mixed-diet frugivores (with gapes wider than 10

mm), plant species in Groups D and E resemble ‘core plant taxa’, while those in Groups

A, B and C are added as they become available, in the manner proposed in the ‘core

178

plant taxa’ model by Fleming (1986). A major characteristic of the ‘core plant taxa’ that

distinguished between groups of Neotropical bat genera was their extended fruit

availability (Fleming, 1986). An analysis of fruiting phenology in subtropical Australian

rainforest showed that several plant in Groups D and E (e.g., Moraceae, Solanaceae and

Euphorbiaceae) fruit over extended periods (Innis, 1989). However, in contrast to

Fleming’s model, major and mixed-diet frugivore species in the present study were

distinguished by their consumption of intermittently-available species (i.e., Groups A

and B), rather than by their consumption of plant species that had longer periods of

availability.

The extent to which the model presented in Figure 7.2 may be consistent in other

regions is not known, although it is based on a much larger amount of data than existing

models of frugivore-plant interactions. However, a functional attribute approach, such

as that used in Chapter Three, could be used to assess potential functional similarity and

variation among frugivore species in many situations where diet information is lacking.

Data on bird species’ body mass may be more accessible than gape width measurements

for species in other regions (e.g., Dunning, 1993). For the bird species included in the

present study, gape width is strongly positively associated with body mass (Figure 7.3).

The gape width of seven bird species was smaller than expected from their body size;

six of these species (encircled) were the seed-crushing Columbidae in the assemblage

(feral pigeon, emerald dove, bar-shouldered dove, brown cuckoo-dove, wonga pigeon

and white-headed pigeon). The seventh species was the Australian brush-turkey, also a

seed-crusher. Seed-crushers may therefore have a larger ratio of body mass to gape

width. The capacity of a bird species to fly with seeds is limited by its body size (Mack,

1993) and non-crushing species may therefore rapidly regurgitate or defecate

indigestible seed ballast (Murray et al., 1993). In contrast, seed-crushing species may

retain seeds for a relatively long time in order to digest them. Therefore, seed-crushers,

179

especially those species that have a diet dominated by the seeds of fleshy-fruited plants

(e.g., brown cuckoo-dove, white-headed pigeon), may require a large body mass. The

channel-billed-cuckoo had a much larger gape than expected from its body size (Figure

7.3). In general, body mass may be useful as a surrogate measure of relative seed size

handling capacity for most bird species, but would over estimate this capacity for seed

crushers. This would not affect predictions if seed crushers were classified in a separate

functional group with limited potential to disperse viable seed, as they were in the

present study.

Log body mass (g)

8765432

Gap

e w

idth

(m

m)

40

30

20

10

0

Figure 7.3 Relationship between bird species’ gape widths and their (ln+1) body mass

(R2 = 0.48, p <0.00001, d.f. = 40; with outliers removed, R2 = 0.83, p <0.00001, d.f. =

32).

7.5 Potential consequences of rainforest fragmentation for seed

dispersal and patterns of plant regeneration

Chapter One introduced the concept of seed dispersal trajectories to highlight the

consequences of the multiple spatial dimensions of seed dispersal for plant regeneration

outcomes (Section 1.6, Figure 1.2, Table 1.1). Incorporating the knowledge developed

in this thesis regarding frugivore species’ responses to forest fragmentation and

channel-billed cuckoo

Australian brush-turkey seed-crushing

Columbidae

180

information regarding their patterns of movement in the landscape, may be used to

asses: (1) the potential for variation among frugivore species in their contribution to the

movement of seeds along certain trajectories; and therefore, (2) whether particular

aspects of plant regeneration may be disproportionately affected by changes in the

frugivore assemblage in fragmented forest.

Dennis and Westcott (2006) developed a classification of frugivorous vertebrate

species in tropical Australia based partly on differences in their spatial scale and rate of

movements and gut passage rates. Table 7.1 combines information from the present

study with that presented by Dennis and Westcott (2006) to examine consequences of

forest fragmentation for seed dispersal in the study region. For example, species that

range widely across the landscape, travel fast and have a slow gut passage rate and use

remnant and regrowth habitats (e.g., topknot pigeon, channel-billed cuckoo, barred

cuckoo-shrike; Table 7.1), may disperse seeds along all trajectories, except over short

distances to microsites within a forest fragment (trajectory b). In contrast, the black-

faced cuckoo-shrike, which predominantly uses regrowth rainforest (Chapter Two),

would be expected to disperse relatively few seeds from or into remnants (trajectories c,

d, e and f). Because decreaser fruit-doves were in very low numbers in fragmented

forest (Chapter Two), they may not disperse seeds along any of the dispersal trajectories

in fragmented forest (Table 7.1). The decreaser green catbird and eastern tube-nosed bat

were considered to have the potential to disperse seeds only along trajectory b (Table

7.1) because, although these species occurred in fragments during the present work

(Chapters Two and Six), the eastern tube-nosed bat makes limited foraging movements

(Spencer and Fleming 1989) and the green catbird is territorial (Innis and McEvoy,

1992). The satin bowerbird potentially disperses seeds along trajectories c, d, f and g if

the distances are short.

181

Table 7.1 Characteristics of frugivore species that may influence their role in dispersing

seed along different dispersal trajectories in fragmented rainforest in subtropical

Australia. ‘Move. scale’ is scale of movement, ‘Move rate’ is rate of movement, and

‘Gut pass.’ is gut passage rate. ‘Frag. resp.’ shows species’ fragmentation responses.

This information was combined to asses the potential for each species to contribute to

dispersal along individual trajectories (Refer to Figure 7.4 and Section 1.6). Note that,

although it was included in the original (Figure 1.2), dispersal away from the crown of

the parent plant (trajectory a) is not shown as it is implied by the movement of seed

along any of the other trajectories.

Bird species1 Characteristics2 Frag. resp.3

Potential dispersal trajectories

Move. scale Move.rate

Gut pass.

b c d e f g

wompoo fruit-dove short slow long Dec

superb fruit-dove short slow long Dec

rose-crowned fruit-dove short slow long Dec

topknot pigeon wide-very wide fast long Tol x x x x x

common koel moderate-wide fast long Tol x x x x x

channel-billed cuckoo wide-very wide fast long Tol x x x x x

Lewin's honeyeater short slow long Tol x x x x x

black-faced cuckoo-shrike wide-very wide fast long Inc x x

barred cuckoo-shrike wide-very wide fast long Undet x x x x x

varied triller short slow short Undet x

olive-backed oriole short slow long Undet x x x x x

figbird wide-very wide fast short Inc x x x x x

pied currawong moderate-wide fast long Tol x x x x x

green catbird - - - Dec x

satin bowerbird short slow short Tol x

mistletoebird short slow long Undet x x x x x

silvereye short slow long Inc x x x x x

eastern tube-nosed bat wide-very wide fast long Dec x

flying foxes wide-very wide fast long Tol x xS xS xS xS xS

1 Frugivore species shown were those considered in both the Wet Tropics study of Dennis and Westcott (2006) and the present study, except the green catbird which is endemic to subtropical Australia but for which sufficient information was available to characterise its potential to contribute to dispersal along different trajectories. Where species’ fragmentation responses in the study region had not been determined (e.g., barred cuckoo-shrike, varied triller, olive-backed oriole and mistletoebird), potential dispersal trajectories shown may be affected by unmeasured differences in their patterns of use of remnants and regrowth. Details for seed crushing bird species and minor frugivores were not provided by Dennis and Westcott (2006). 2 Information on species’ characteristics after Dennis and Westcott (2006). Movement scale during the average gut passage time of a seed (short <100 m, moderate = 100-200 m, wide = 200-800 m, very wide >800 m). Movement rate was determined by the slope of the relationship between distance moved and time, measured using radio-tracked individuals; slow <2, fast >2. Gut passage was short (<30 min.), long (>30 min). 3 Fragmentation response is the response pattern detected in the present work (Chapters Two and Six) ; Dec is Decreaser, Tol is Tolerant, Inc is Increaser and Undet is Undetermined. S only small (ca. < 9mm) seeds would be likely to be moved along these trajectories by flying-foxes.

182

i) Plant taxa consumed by most frugivore species

ii) Plant taxa consumed predominantly by decreaser frugivore species

topknot pigeon channel-billed cuckoo barred cuckoo-shrike flying-foxesS

topknot pigeon common koel channel-billed cuckoo Lewin’s honeyeater barred cuckoo-shrike olive-backed oriole figbird pied currawong mistletoebird silvereye flying-foxesS

common koel Lewin’s honeyeater varied triller olive-backed oriole figbird pied currawong green catbird satin bowerbird mistletoebird silvereye eastern tube-nosed bat flying-foxes

topknot pigeon common koel channel-billed cuckoo Lewin’s honeyeater barred cuckoo-shrike olive-backed oriole

c

b

d e

g

f

figbird pied currawong mistletoebird silvereye flying-foxesS

topknot pigeon common koel channel-billed cuckoo Lewin’s honeyeater black-faced cuckoo-shrike barred cuckoo-shrike olive-backed oriole figbird pied currawong mistletoebird silvereye flying-foxesS

topknot pigeon Lewin’s honeyeater flying-foxesS

c

b

d e

g

f

Lewin’s honeyeater green catbird satin bowerbird eastern tube-nosed bat flying-foxes

topknot pigeon Lewin’s honeyeater flying-foxesS

topknot pigeon Lewin’s honeyeater flying-foxesS

topknot pigeon flying-foxesS

ii) Plant taxa consumed only by decreaser frugivore species

c

b

de

g

f

green catbird eastern tube-nosed bat

183

Figure 7.4 (on previous page)The frugivore species that potentially disperse seeds

along different dispersal trajectories in fragmented forest landscapes for plant taxa that

are i) consumed by most frugivore species; ii) predominantly consumed by decreaser

species; and iii) only consumed by decreaser species. The grey patches in this figure

represent forest fragments and the white area represents the cleared or modified

matrix. ‘Decreaser’ frugivore species that occurred in low frequency in rainforest

remnants in this study (all fruit-doves; Chapter 2), are not shown in this figure because

they are likely to disperse few seeds in fragmented forest. Seed-crushing frugivore

species are not shown in this figure because they are likely to disperse few viable

seeds. The white diamond represents an individual plant. Arrows show the trajectories

of seed movement. Table 7.1 shows the characteristics associated with bird species’

potential to disperse seeds along different trajectories. S flying-foxes are likely to

disperse only small seeds (<9 mm) along trajectories involving movement beyond tens

of metres.

Many plant species, including Moraceae, and Euphorbiaceae, are consumed by

most frugivore species (Chapters 4 and 5). Consequently, seeds of these plant taxa are

potentially dispersed by multiple frugivore species along most dispersal trajectories

(Figure 7.4i). However, a relatively small number of frugivore species had the potential

to disperse plant taxa over long distances to new habitats (trajectory e). With the

exception of the topknot pigeon and flying-foxes, these frugivore species had fig-

dominated diets (Chapter Four). Flying-foxes may only disperse small-seeded plant

species along this trajectory (Eby, 1991b, 1995; Shilton et al., 1999). Consequently, the

topknot pigeon may be the main agent of colonisation of new habitats for most plant

taxa. Plant taxa that are not dispersed to new habitats may have a limited ability to cope

with climate change (Primack and Miao, 1992; Matlack, 1995; Westoby and Burgman,

2006; Weir and Corlett, 2007).

There was a suite of plant taxa, including Lauraceae, Myrtaceae, Meliaceae,

Verbenaceae and Vitaceae and plant species with large fruits (>10 mm), that were

predominantly consumed by decreaser frugivores. Analyses of the potential of tolerant

and increaser species to disperse these plants have shown that only a small subset of

184

frugivore species (topknot pigeon, satin bowerbird, Lewin’s honeyeater or flying-foxes)

may be likely to substitute for decreaser frugivore species as dispersers of these plant

taxa in fragmented rainforest (Chapters Five and Six). The decreaser green catbird and

eastern tube-nosed bat potentially disperse seeds within fragments, although the eastern

tube-nosed bat may only consume a small number of these plant species (Chapter Six).

Figure 7.4 (ii) shows that a small number of frugivore species potentially disperse these

plant taxa along each trajectory. Unless these frugivore species increase their feeding

rates on these plant taxa concurrent with the decline of decreaser species (i.e.,

‘behavioural compensation’ (Loiselle and Blake, (2002)), dispersal rates of these plants

would be likely to be reduced in fragmented forest.

In the case of plant taxa that were only known to be consumed by decreaser

frugivore species, which is likely to include several species from the Rubiaceae

(Chapter Five), dispersal along any of the trajectories shown would be severely limited

in fragmented rainforest (Figure 7.4 (iii)). Consequently, regeneration of these plant

taxa would be likely to be substantially reduced in fragmented forest landscapes.

The predicted reductions in dispersal of certain plant taxa may be tested by

comparing observations of fruit removal between fragmented and extensive forest

landscapes. Predictions relating to the consequences of frugivore declines for seed

dispersal along certain trajectories in fragmented rainforest, for example, reductions in

dispersal to recruitment microsites, may be assessed using seed trapping (e.g., Harvey,

2000), or seed tracking techniques (e.g., Levey and Sargent, 2000; Tewksbury et al.,

2002). Dispersal over long distances to new habitats (Figure 7.4, trajectory e) may be

infrequent for most plant species (Nathan and Muller-Landau, 2000), but may be

severely limited in fragmented landscapes for certain plant taxa (e.g., those not

consumed by the topknot pigeon). Differences among plant species in their potential for

185

dispersal over long distances may be inferred by analysing changes in species’

distributions, for example in response to global climatic changes.

Many frugivore species may contribute to the dispersal of seeds from the non-

forest matrix into fragments and within the non-forest matrix (trajectories f and g,

Figure 1.6; Table 7.1). Consequently, high rates of fruit removal from plants in the non-

forest matrix, and seed input from these plants into fragments and secondary regrowth

are expected. Introduced plant species are ubiquitous in most fragmented landscapes

(Buckley et al., 2006) and, depending on the patterns of consumption of plant species by

frugivore species, may be among the plant species with high dispersal rates in

fragmented forest landscapes. Based on their consumption of a relatively high dietary

proportion of introduced plant taxa (Chapter Five, Table 5.1), it is predicted that

increaser bird species would disperse the seeds of introduced plant species. Studies of

fruit removal and seed input (e.g., Guevara and Laborde, 1993; Medellín and Gaona,

1999), and of plant recruitment within fragments (e.g., Janzen, 1983) or in regrowth

(e.g., Neilan et al., 2006) may asses these predictions.

7.6 Conservation issues

This thesis has shown that existing fragmented rainforest in the study region is

likely to have lost a component of the vertebrate frugivorous fauna and, as a

consequence, that the regenerative potential of a substantial proportion of native plant

species may be reduced. Continued clearing and fragmentation of rainforest would be

likely to exacerbate this situation by further disadvantaging decreaser species, and

potentially leading to the decline of additional frugivore species.

All of the decreaser frugivore species identified in this work used at least a

subset of the rainforest remnants surveyed. The specific patterns of use of fragmented

rainforest habitats by these frugivore species may be related to the size and

186

configuration of fragments (Doak et al., 1992; Andrén, 1994; Wiens, 1994; With et al.,

1997; Price et al., 1999; Graham, 2001; Graham and Blake, 2001; Develey and

Metzger, 2006). Identification of factors that influence the distribution of decreaser

frugivore species in fragmented parts of the landscape, such as a threshold fragment size

or degree of connectivity, would highlight the areas of highest conservation value for

these susceptible vertebrate taxa. This understanding could also inform rainforest

restoration actions in terms of the landscape attributes that are necessary to reinstate

populations of decreaser frugivore species in fragmented landscapes. Information

provided in this thesis may be used to identify specific plant resources that would be

useful for decreaser frugivore species. For example, Lauraceae may be important for

fruit-pigeons (Crome, 1975; Innis, 1989; Recher et al., 1995), while strangling figs (e.g.,

Ficus watkinsiana, F. macrophylla) and Elaeocarpus grandis may be important for the

eastern tube-nosed bat.

Based on the secondary consequences of frugivore declines that have been

predicted in this thesis, rainforest restoration would also be necessary to return the

regenerative capacity of several plant taxa in fragmented parts of the landscape. In the

short-term, replanting or direct-seeding of the plant taxa that are vulnerable to reduced

dispersal in fragmented forest could be incorporated into ecological management and

restoration works. In the longer term, ecological restoration that enables the movement

of frugivore species across modified parts of the landscape may facilitate seed dispersal

by frugivores in these habitats (Tucker and Murphy, 1997; Tewksbury et al., 2002;

Martínez-Garza and Howe, 2003; Jansen, 2005).

187

Appendix 1

Original published sources of records of plant species consumption by frugivore

species. The thesis chapters in which data from each source was included are shown

following each reference.

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Barker, R.D., Vestjens, W.J.M., 1990. The food of Australian birds: Passerines. C.S.I.R.O., Melbourne. 4, 5, 6

Bedggood, G.W., 1970. Bird notes from East Gippsland. Australian Bird Watcher 3, 252-265. 4, 5, 6

Béland, P., 1977. Mimicry in Orioles of south-eastern Queensland. Emu 77, 215-218. 4, 5, 6

Binns, G. 1954. The camp out at Lake Barrine, Atherton Tableland, North Queensland. Emu 54, 29-46. 4

Bourke, P.A., 1949. The breeding population of a thirty-five acre ‘Timber Paddock’. Emu 49, 73-83. 4, 5, 6

Bravery, J.A., 1970. The birds of Atherton Shire, Queensland. Emu 66, 267-271.4, 5, 6 Brookes, G.B. 1919. Report on investigation in regard to the spread of prickly-pear by

the Scrub Turkey. Q. Ag. J. 11, new series, 26-28. 4 Burton, A.C.G., Morris A.K., 1993. New South Wales Bird Report. Aust. Birds 26, 89-

133. 4, 5, 6 Campbell, A.J., Barnard, H.G., 1917. Birds of the Rockingham Bay district, North

Queensland. Emu 17, 1-12. 4, 5, 6 Carter, T., 1924. Birds of the Broome Hill district. Part III. Emu 23, 306-318. 4, 5, 6 Chisholm, A.H., 1938. The birds of Barellan, N.S.W. with botanical and other notes.

Emu 37, 301-313. 4 Chisholm, A.H., 1944. An interesting old notebook. Emu 43, 281-288. 4, 5, 6 Church R., 1997. Avian frugivory in a subtropical rainforest: Eleven years of

observations in Lamington National Park. The Sunbird 27, 85-97. 4, 5, 6 Cleland, J.B., 1911. Examination of contents of stomachs and crops of Australian birds.

Emu 11, 79-95. 4 Cleland, J.B. Cited in Higgins, P.J. (Ed.), 1999. Handbook of Australian, New Zealand

and Antarctic Birds: V4 Parrots to Dollarbirds. Oxford University Press, Melbourne. 4, 5, 6

Cleland, J.B., Maiden, J.H., Froggatt, W.W., Ferguson, E.W., Musson, C.T., 1918. The food of Australian birds. N.S.W. Department of Agricultural Science Bulletin No. 15. 4, 5, 6

Cooper, R.P., 1962. A revision of the distribution of the Brown Pigeon. Emu 61, 266-269. 4

Cooper, R.M., Knight, B., 1989. New South Wales Bird Report for 1985 Aust. Birds 22, 1-45.

Cooper W., Cooper, W.T., 1994. Fruits of the rain forest: A guide to fruits in Australian tropical rain forests. Geo Production, Chatswood. 4, 5, 6

Crome, F.H.J., 1975a. The ecology of fruit pigeons in tropical northern Queensland. Aust. Wildl. Res. 2, 155-185. 4, 5, 6

188

Crome, F.H.J., 1975b. Breeding, feeding and status of the Torres Strait Pigeon at Low Isles, north Queensland. Emu 75,189-98. 4, 5, 6

Crome, F.H.J., 1978. Foraging ecology of an assemblage of birds in lowland rainforest in northern Queensland. Aust. J. Ecol. 3, 195-212. 4, 5, 6

Crome F.H.J., Shields J., 1992. Parrots and Pigeons of Australia. Angus & Robertson, Pymble. 4, 5, 6

Crouther, M.M., 1985. Some breeding records of the common koel Eudynamis scolopacea. Australian Bird Watcher 11, 49-56. 4, 5, 6

Date, E.M, Recher, H.F., 1990. Ecology and Management of Rainforest Pigeons in NSW – An interim report. NSW NPWS, Sydney. 4, 5, 6

Denny, T., Dudman, D., 1979. Koel behaviour. Sunbird 10,78.4, 5, 6 De Warren, J.J., 1928. The avifauna of the upper reaches of the Macleay River, NSW.

Emu 28,11-120. 4, 5, 6 Drew, R.A.I., 1987. Reduction in fruit fly (Tephritidae: Dacinae) populations in their

endemic rainforest habitat by frugivorous vertebrates. Aust. J. Zool. 35, 283-8. 4, 5, 6

Eby, P. ,1991 “Finger-winged night workers”: managing forests to conserve the role of Grey-headed Flying Foxes as pollinators and seed dispersers. pp. 91-100 in (D. Lunney (ed.)) Conservation of Australia’s Forest Fauna. Royal Zoological Society of NSW, Mosman. 6

Eby, P., 1995. The biology and management of flying foxes in New South Wales. Species Management Report No. 18. New South Wales National Parks and Wildlife Service, Hurstville. 6

Eby, P. 1998. An analysis of diet specialisation in frugivorous Pteropus poliocephalus (Megachiroptera) in Australian subtropical rainforest. Aust. J. Ecol. 23, 443-456. 6

Firth, D.J., 1979. Ecology of Cinnamomum camphora (l.) Nees and Eberm (camphor laurel) in the Richmond-Tweed region of north-eastern New South Wales. Unpublished thesis, Department of Botany, University of New England, Armidale. 4, 5

Floyd, A.G., 1989. Rainforest trees of mainland south-eastern Australia. Forestry Commission of New South Wales, Sydney. 4, 5, 6

Floyd, A.G., 1990. Australian Rainforests in New South Wales. Volume 1. Surrey Beatty & Sons, Chipping Norton. 4, 5, 6

Forde, N., 1986. Relationships between birds and fruits in temperate Australia. in Ford, H.A., Paton, D.C. (Eds.), The dynamic partnership: Birds and plants in southern Australia. D.J. Woolman, Government Printers, Adelaide, pp. 42-58. 4, 5, 6

Forshaw, J.M., 1969. Australian Parrots. Landsdowne Press, Melbourne. 4 Forshaw, J.M., Muller, K.A., 1978. Annotated list of birds observed at Iron Range,

Cape York Peninsula, Queensland, during October 1974. Aust. Bird Watcher 7, 171-194. 4, 5, 6

Forshaw, J.M., Cooper, W.T. (1981) Australian Parrots. Second edition. Landsdowne Editions, Melbourne. 4

French, K., 1990. Evidence for frugivory by birds in montane and lowland forests in South-east Australia. Emu 90,185-189. 4, 5, 6

Frith, H.J., 1952. Notes on the pigeons of the Richmond River. Emu 52,89-99. 4, 5, 6 Frith H.J., 1957. Food habits of the Topknot Pigeon. Emu 57, 341-345. 4, 5, 6 Frith H.J., 1982. Pigeons and doves of Australia. Rigby Publishers, Adelaide. 4, 5, 6 Frith, H.J., Crome, F.H.J., Wolfe, T.O., 1976. Food of fruit-pigeons in New Guinea.

Emu 76, 49-58. 4, 5, 6 Frith, C.B., Frith, D.W., 2004. Bird Families of the World: The Bowerbirds

Ptilonorhynchidae. Oxford University Press: Oxford. 4, 5, 6

189

Gannon, G.R., 1936. Plants spread by the Silvereye. Emu 35, 314-316. 4, 5, 6 Gibson, J.D., 1977. The birds of the County of Camden (including the Illawarra

district). Aust. Birds 11, 41-80. 4, 5, 6 Gilbert, P.A., 1936. The Topknot Pigeon. Emu 35, 301-312. 4, 5, 6 Gosper, C.R., 1994. Comparison of the avifauna of rainforest remnants with regrowth

dominated by the exotic tree camphor laurel Cinnamomum camphora. Unpublished thesis, University of New England, Armidale. 4, 5, 6

Gosper, C.R., 1999. Plant food resources of birds in coastal dune communities in New South Wales. Corella 2, 53-62. 4, 5, 6

Gosper, D.G., cited in Higgins, P.J. (Ed.), 1999. Handbook of Australian, New Zealand and Antarctic Birds: V4 Parrots to Dollarbirds. Oxford University Press, Melbourne. 4, 5, 6

Gosper, D.G., 1962. Breeding records of the koel. Aust. Bird Watcher 1, 226-228. 4, 5, 6

Gould, J., 1865. Handbook to the Birds of Australia. 2 volumes. J. Gould, London. 4, 5, 6

Green R.J., 1993. Avian seed dispersal in and near subtropical rainforests. Wildl. Res. 20, 535-557. 4, 5, 6

Hackett, D., 1996. Frugivory and Ligustrum lucidum in north-eastern NSW: Implications for seed dispersal and avifauna conservation. Integrated project, Southern Cross University, Lismore. 4, 5, 6

Hall, L.S., Richards, G. 2000. Flying foxes: Fruit and blossom bats of Australia. UNSW Press: Sydney. 6

Halse, S.A., 1978. Feeding habits of six species of honeyeaters in south-western Australia. Emu 78, 145-148. 4, 5, 6

Hindwood, K.A., 1959. The Purple-crowned Pigeon in southeastern Australia. Emu 59, 219-20. 4, 5, 6

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Holland, L., 1964. Pigeons of the Woolgoolga District, N.S.W. Aust. Bird Watcher 2, 61-69. 4, 5, 6

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eastern Queensland. Aust. Wildl. Res. 16, 365-94. 4, 5, 6 Innis, G.J., McEvoy, J., 1992. Feeding ecology of green catbirds (Ailuroedus

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190

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191

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Shanks, D.. 1949. Observations from the Upper King River district, Victoria. Emu 49, 132-141. 4 Smith, L., 1984. Garden plants attractive to birds. Aust. Birds 18, 17-32. 4, 5, 6 Spencer, H.J., Fleming, T.H. 1989. Roosting and Foraging Behaviour of the Queensland

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192

Storr, G.M., 1953. Birds of the Cooktown and Laura districts, north Queensland. Emu 53, 225-248. 4, 5, 6

Vestjens, W.J.M., Carrick, R., 1974. Food of the Black-backed Magpie, Gymnorhina tibicen, at Canberra. Aust. Wildl. Res. 1, 71-83. 4, 5

Waterhouse cited in Higgins, P.J., Davies, S.J.J.F., (Eds.), 1996. Handbook of Australian, New Zealand and Antarctic Birds: V3 Snipe to Pigeons. Oxford University Press, Melbourne. 4, 5, 6

Waterhouse, R.D., 1995. Observations on the diet of the Lewin's Honeyeater Meliphaga lewinii in the Illawarra Rainforest, New South Wales. Corella 19, 102-105. 4, 5, 6

Wheeler, W.R., 1967. The birds of Cairns, Cooktown and the Atherton Tablelands. Aust. Bird Watcher 3, 55-76. 4, 5, 6

Wheeler, W.R., 1972. Bird notes 1970-71. Bird Obs. 484, 4-8. 4, 5, 6

193

Appendix 2

List of plant species used in the data sets analysed in Chapters Four, Five and

Six and the total number of frugivorous bird and bat species (data for Pteropus alecto

and P. poliocephalus combined) known to consume each plant species.

Thesis Chapter Family Genus Species 4 5 6 Total number

frugivore species

Agavaceae Cordyline petiolaris 4 5 6 2 Agavaceae Cordyline rubra 5 6 1 Agavaceae Cordyline stricta 5 6 1 Akaniaceae Akania bidwillii 4 5 6 4 Alangiaceae Alangium villosum 4 5 6 5 Anacardiaceae Euroschinus falcata 4 5 6 14 Anacardiaceae Rhodosphaera rhodanthema 4 5 6 1 Annonaceae Melodorum leichhardtii 4 5 6 2 Annonaceae Polyalthia nitidissima 4 5 6 1 Apocynaceae Carissa ovata 4 5 6 2 Apocynaceae Melodinus australis 4 5 6 4 Araceae Alocasia brisbanensis 4 5 6 1 Araceae Pothos longipes 4 5 6 5 Araliaceae Cephalaralia cephalobotrys 5 6 1 Araliaceae Polyscias elegans 4 5 6 18 Araliaceae Polyscias murrayi 4 5 6 15 Araliaceae Polyscias sambucifolia 4 5 6 1 Arecaceae Archontophoenix cunninghamia 4 5 6 18 Arecaceae Calamus muelleri 4 5 6 3 Arecaceae Linospadix monostachya 4 5 6 3 Arecaceae Livistonia australis 5 6 7 Arecaceae Ptychosperma elegans 4 5 6 1 Boraginaceae Ehretia acuminata 4 5 6 15 Burseraceae Canarium australasicum 4 5 6 9 Caprifoliaceae Sambucus australasica 4 5 6 2 Celastraceae Celastrus subspicata 4 5 6 4 Celastraceae Maytenus bilocularis 4 5 6 1 Celastraceae Maytenus cunninghamii 4 5 6 1 Celastraceae Siphonodon australis 5 6 2 Chenopodiaceae Enchylaena tomentosa 4 5 6 1 Cucurbitaceae Diplocyclos palmatus 5 6 4 Cucurbitaceae Sicyos australis 5 6 1 Cucurbitaceae Zehneria cunninghamii 4 5 6 2 Cunoniaceae Schizomeria ovata 4 5 6 7 Dilleniaceae Hibbertia scandens 4 5 6 6 Ebenaceae Diospyros australis 4 5 6 3 Ebenaceae Diospyros fasciculosa 4 5 6 3 Ebenaceae Diospyros geminata 4 5 6 6 Ebenaceae Diospyros pentamera 4 5 6 12 Elaeagnaceae Elaeagnus triflora 4 5 6 1 Elaeocarpaceae Elaeocarpus grandis 4 5 6 8 Elaeocarpaceae Elaeocarpus kirtonii 4 5 6 9 Elaeocarpaceae Elaeocarpus obovatus 4 5 6 15 Elaeocarpaceae Elaeocarpus reticulatus 4 5 6 11 Elaeocarpaceae Sloanea australis 4 5 6 8 Elaeocarpaceae Sloanea woollsii 4 5 6 11 Epacridaceae Leucopogon parviflorus 4 5 6 1 Epacridaceae Monotoca elliptica 4 5 6 2 Epacridaceae Trochocarpa laurina 4 5 6 3 Euphorbiaceae Actephila lindleyi 5 6 1 Euphorbiaceae Breynia oblongifolia 4 5 6 4 Euphorbiaceae Claoxylon australe 4 5 6 3 Euphorbiaceae Cleistanthus cunninghamii 5 6 3 Euphorbiaceae Drypetes deplanchei 4 5 6 7

194

Thesis Chapter Family Genus Species 4 5 6 Total number

frugivore species

Euphorbiaceae Flueggea leucopyrus 5 6 1 Euphorbiaceae Glochidion ferdinandi 4 5 6 12 Euphorbiaceae Glochidion sumatranum 4 5 6 4 Euphorbiaceae Macaranga tanarius 4 5 6 7 Euphorbiaceae Mallotus discolor 4 5 6 7 Euphorbiaceae Omalanthus nutans 4 5 6 15 Eupomatiaceae Eupomatia laurina 4 5 6 1 Eupomatiaceae Galbulimima belgraveana 4 5 6 4 Flacourtiaceae Caesaria multinervosa 4 5 6 2 Flacourtiaceae Scolopia braunii 4 5 6 6 Flacourticaeae Berberidopsis beckleri 5 6 1 Flagellariaceae Flagellaria indica 4 5 6 6 Grossulariaceae Polyosma cunninghamii 4 5 6 4 Icacinaceae Citronella moorei 4 5 6 4 Icacinaceae Pennantia cunninghamii 4 5 6 7 Lauraceae Beilschmedia elliptica 4 5 6 7 Lauraceae Beilschmedia obtusifolia 4 5 6 8 Lauraceae Cinnamomum oliveri 4 5 6 10 Lauraceae Cinnamomum virens 4 5 6 6 Lauraceae Cryptocarya bidwillii 4 5 6 6 Lauraceae Cryptocarya erythroxylon 4 5 6 4 Lauraceae Cryptocarya foetida 4 5 6 1 Lauraceae Cryptocarya glaucescens 4 5 6 6 Lauraceae Cryptocarya hypospodia 4 5 6 3 Lauraceae Cryptocarya macdonaldii 4 5 6 4 Lauraceae Cryptocarya microneura 4 5 6 4 Lauraceae Cryptocarya obovata 4 5 6 9 Lauraceae Cryptocarya rigida 4 5 6 1 Lauraceae Cryptocarya triplinervis 4 5 6 11 Lauraceae Endiandra discolor 4 5 6 5 Lauraceae Endiandra muelleri 4 5 6 4 Lauraceae Endiandra sieberi 4 5 6 2 Lauraceae Litsea australis 4 5 6 9 Lauraceae Litsea reticulata 4 5 6 11 Lauraceae Neolitsea australiensis 4 5 6 7 Lauraceae Neolitsea dealbata 4 5 6 10 Liliaceae Dianella caerulea 4 5 6 5 Loganiaceae Strychnos psilosperma 4 5 6 4 Meliaceae Anthocarapa nitidula 4 5 6 7 Meliaceae Dysoxylum fraserianum 4 5 6 7 Meliaceae Dysoxylum mollissimum 4 5 6 8 Meliaceae Dysoxylum rufum 4 5 6 3 Meliaceae Melia azedarach 4 5 6 18 Meliaceae Owenia cepiodora 4 5 6 2 Meliaceae Synoum glandulosum 4 5 6 5 Menispermaceae Hypserpa laurina 5 6 1 Menispermaceae Legnephora moorei 4 5 6 2 Menispermaceae Stephania japonica 4 5 6 2 Menispermaceae Tinospora smilacina 5 6 1 Mimosaceae Acacia aulacocarpa 5 6 2 Mimosaceae Acacia maidenii 4 5 6 7 Mimosaceae Acacia melanoxylon 4 5 6 8 Monimaceae Palmeria scandens 4 5 6 2 Monimiaceae Hedycarya angustifolia 4 5 6 4 Moraceae Ficus coronata 4 5 6 13 Moraceae Ficus fraseri 4 5 6 22 Moraceae Ficus macrophylla 4 5 6 27 Moraceae Ficus microcarpa 4 5 6 6 Moraceae Ficus obliqua 4 5 6 24 Moraceae Ficus platypoda 4 5 6 25 Moraceae Ficus rubiginosa 4 5 6 15 Moraceae Ficus superba 4 5 6 17 Moraceae Ficus virens 4 5 6 12 Moraceae Ficus watkinsiana 4 5 6 17 Moraceae Maclura cochinchinensis 4 5 6 7 Moraceae Streblus brunonianus 4 5 6 10 Moraceae Trophis scandens 4 5 6 3 Myoporaceae Myoporum insulare 4 5 6 2 Myrsinaceae Embelia australiana 4 5 6 2

195

Thesis Chapter Family Genus Species 4 5 6 Total number

frugivore species

Myrsinaceae Rapanea howittiana 4 5 6 4 Myrsinaceae Rapanea variabilis 4 5 6 2 Myrtaceae Acmena hemilampra 4 5 6 6 Myrtaceae Acmena ingens 4 5 6 10 Myrtaceae Acmena smithii 4 5 6 15 Myrtaceae Archirhodomyrtus beckleri 4 5 6 2 Myrtaceae Austromyrtus bidwillii 4 5 6 3 Myrtaceae Austromyrtus dulcis 5 6 1 Myrtaceae Austromyrtus hillii 4 5 6 2 Myrtaceae Decaspermum humile 4 5 6 7 Myrtaceae Pilidiostigma rhytispermum 4 5 6 1 Myrtaceae Rhodamnia argentea 4 5 6 8 Myrtaceae Rhodamnia rubescens 4 5 6 7 Myrtaceae Rhodomyrtus psidioides 4 5 6 6 Myrtaceae Syzgium luehmannii 4 5 6 2 Myrtaceae Syzygium australe 4 5 6 8 Myrtaceae Syzygium corynanthum 4 5 6 8 Myrtaceae Syzygium crebrinerve 4 5 6 6 Myrtaceae Syzygium francisii 4 5 6 1 Myrtaceae Syzygium johnsonii 4 5 6 1 Myrtaceae Syzygium oleosum 4 5 6 2 Myrtaceae Syzygium paniculatum 4 5 6 7 Oleaceae Chionanthus ramiflora 4 5 6 4 Oleaceae Jasminum dallachii 5 6 2 Oleaceae Jasminum didymum 4 5 6 4 Oleaceae Jasminum simplicifolium 4 5 6 1 Oleaceae Notelaea longifolia 4 5 6 4 Oleaceae Olea paniculata 4 5 6 11 Pandanaceae Freycinetia excelsa 5 6 1 Pandanaceae Freycinetia scandens 5 6 1 Philesiaceae Eustrephus latifolius 4 5 6 2 Philesiaceae Geitonoplesium cymosum 4 5 6 2 Piperaceae Piper novae-hollandiae 4 5 6 12 Pittosporaceae Citriobatus pauciflorus 4 5 6 1 Pittosporaceae Pittosporum rhombifolium 4 5 6 2 Pittosporaceae Pittosporum undulatum 4 5 6 10 Pittosporaceae Pittosporum venulosum 4 5 6 1 Podocarpaceae Podocarpus elatus 4 5 6 5 Polygonaceae Muehlenbeckia gracillima 4 5 6 1 Rhamnaceaae Alphitonia excelsa 4 5 6 18 Rhamnaceaae Alphitonia petriei 4 5 6 10 Rhamnaceae Emmenosperma alphitonioides 4 5 6 4 Rhamnanceae Rhamnella vitiensis 5 6 1 Rosaceae Rubus moluccanus 4 5 6 4 Rosaceae Rubus moorei 4 5 6 3 Rosaceae Rubus parvifolius 4 5 6 1 Rosaceae Rubus rosifolius 4 5 6 6 Rubiaceae Aidia racemosa 4 5 6 1 Rubiaceae Canthium coprosmoides 4 5 6 4 Rubiaceae Canthium odoratum 4 5 6 1 Rubiaceae Coprosma quadrifida 4 5 6 4 Rubiaceae Hodgkinsonia ovatiflora 4 5 6 4 Rubiaceae Ixora beckleri 4 5 6 3 Rubiaceae Morinda jasminoides 4 5 6 7 Rubiaceae Morinda umbellata 4 5 6 1 Rubiaceae Psychotria loniceroides 4 5 6 1 Rubiaceae Randia benthamianus 4 5 6 1 Rutaceae Acronychia laevis 4 5 6 5 Rutaceae Acronychia oblongifolia 4 5 6 11 Rutaceae Acronychia suberosa 4 5 6 2 Rutaceae Acronychia wilcoxiana 4 5 6 1 Rutaceae Halfordia kendack 4 5 6 5 Rutaceae Melicope elleryana 4 5 6 5 Rutaceae Melicope micrococca 4 5 6 6 Rutaceae Melicope vitiflora 5 6 1 Rutaceae Micromelum minutum 4 5 6 1 Rutaceae Sarcomelicope simplicifolia 4 5 6 2 Rutaceae Zanthoxylum brachyacanthum 4 5 6 1 Santalaceae Exocarpos cupressiformis 4 5 6 7

196

Thesis Chapter Family Genus Species 4 5 6 Total number

frugivore species

Santalaceae Santalum lanceolatum 5 6 1 Sapindaceae Alectryon coriaceus 4 5 6 2 Sapindaceae Alectryon subcinereus 4 5 6 2 Sapindaceae Alectryon tomentosus 4 5 6 2 Sapindaceae Arytera distylis 4 5 6 4 Sapindaceae Cupaniopsis anacardioides 4 5 6 5 Sapindaceae Cupaniopsis baileyana 5 6 1 Sapindaceae Cupaniopsis flagelliformus 5 6 1 Sapindaceae Cupaniopsis parvifolia 4 5 6 1 Sapindaceae Diploglottis australis 4 5 6 19 Sapindaceae Elattostachys xylocarpa 4 5 6 7 Sapindaceae Guioa acutifolia 4 5 6 1 Sapindaceae Guioa semiglauca 4 5 6 15 Sapindaceae Jagera pseudorhus 4 5 6 11 Sapindaceae Mischarytera lautereriana 4 5 6 4 Sapindaceae Mischocarpus anodontus 4 5 6 3 Sapindaceae Mischocarpus pyriformis 4 5 6 2 Sapindaceae Sarcopteryx stipata 4 5 6 7 Sapotaceae Planchonella queenslandica 4 5 6 2 Sapotaceae Pouteria australis 4 5 6 3 Sapotaceae Pouteria chartacea 4 5 6 1 Sapotaceae Pouteria myrsinoides 5 6 1 Smilacaceae Ripogonum album 4 5 6 2 Smilacaceae Smilax australis 4 5 6 2 Smilacaceae Smilax glycophylla 4 5 6 1 Solanaceae Duboisia myoporoides 4 5 6 5 Solanaceae Solanum aviculare 4 5 6 8 Solanaceae Solanum stelligerum 5 6 1 Sterculiaceae Brachychiton acerifolius 4 5 6 4 Sterculiaceae Brachychiton discolor 4 5 6 3 Surianaceae Guilfoylia monostylis 4 5 6 2 Symplocaceae Symplocos stawellii 4 5 6 3 Symplocaceae Symplocos thwaitesii 4 5 6 6 Thymelaecae Wikstroemia indica 4 5 6 4 Thymelaeceae Phaleria chermsideana 4 5 6 2 Ulmaceae Aphananthe philippinensis 4 5 6 15 Ulmaceae Trema tomentosa 4 5 6 7 Urticaceae Dendrocnide excelsa 4 5 6 10 Urticaceae Dendrocnide photinophylla 4 5 6 3 Urticaceae Pipturus argenteus 4 5 6 9 Verbenaceae Callicarpa pedunculata 4 5 6 3 Verbenaceae Clerodendrum floribundum 4 5 6 2 Verbenaceae Clerodendrum tomentosum 4 5 6 1 Verbenaceae Gmelina leichhardtii 4 5 6 2 Verbenaceae Vitex lignum-vitae 4 5 6 7 Vitaceae Cayratia clematidea 4 5 6 3 Vitaceae Cayratia eurynema 4 5 6 8 Vitaceae Cissus antarctica 4 5 6 11 Vitaceae Cissus hypoglauca 4 5 6 8 Vitaceae Cissus sterculiifolia 4 5 6 10 Vitaceae Tetrastigma nitens 4 5 6 8 Zingiberaceae Alpinia caerulea 4 5 6 4 Introduced from outside Australian subtropics

Araliaceae Schefflera actinophylla 4 5 6 11 Arecaceae Archontophoenix alexandrae 4 5 6 5 Boraginaceae Cordia dichotoma 4 5 6 1 Introduced from outside Australia

Anacardiaceae Schinus terebinthifolia 4 5 6 7 Arecaceae Syagrus romanzoffianum 5 6 1 Caesalpiniaceae Tamarindus indica 4 5 6 3 Lauraceae Cinnamomum camphora 4 5 6 26 Liliaceae Asparagus africanus 4 5 6 2 Liliaceae Asparagus densiflorus 5 6 2

197

Thesis Chapter Family Genus Species 4 5 6 Total number

frugivore species

Liliaceae Asparagus plumosus 4 5 6 2 Moraceae Ficus benjamima 4 5 6 11 Myrsinaceae Ardissia crenata 4 5 6 1 Myrtaceae Eugenia uniflora 4 5 6 2 Myrtaceae Psidium guajava 5 6 6 Ochnaceae Ochna serrulata 4 5 6 11 Oleaceae Ligustrum lucidum 4 5 6 15 Oleaceae Ligustrum sinense 4 5 6 13 Oleaceae Olea europea 4 5 6 3 Passifloraceae Passiflora suberosa 4 5 6 4 Phytolaccaceae Phytolacca americana 4 5 6 2 Phytolaccaceae Phytolacca octandra 4 5 6 18 Phytolaccaceae Rivina humilis 4 5 6 2 Rosaceae Duchesnea indica 4 5 6 4 Rosaceae Rosa rubiginosa 4 5 6 2 Rosaceae Rubus fructosus 4 5 6 8 Rubiaceae Coffea aribica 4 5 6 1 Rutaceae Murraya paniculata 4 5 6 2 Solanaceae Lycium ferocissimum 4 5 6 9 Solanaceae Physalis peruviana 4 5 6 5 Solanaceae Solanum americanum 4 5 6 9 Solanaceae Solanum capsicoides 5 6 1 Solanaceae Solanum erianthum 5 6 2 Solanaceae Solanum hispidum 4 5 6 2 Solanaceae Solanum mauritianum 4 5 6 21 Solanaceae Solanum nigrum 4 5 6 5 Solanaceae Solanum pseudocapsicum 5 6 1 Solanaceae Solanum seaforthianum 4 5 6 6 Ulmaceae Celtis sinensis 4 5 6 10 Verbenaceae Lantana camara 4 5 6 21 Vitaceae Vitis vinifera 4 5 6 11

198

Appendix 3

Associations between frugivore species’ responses to forest fragmentation as

detected in this thesis and their ecological attributes are assessed (Table A3.1). This

topic was introduced in Section 1.4.2 and the results are discussed in Section 7.1.2 in

the main body of this thesis.

Body mass

Body mass among frugivorous species in subtropical Australia ranges from 9 g

(mistletoebird) to 2 300 g (Australian brush turkey) (average 263 g S.E. 59 g). There is

no association between body size and fragmentation sensitivity (sensitivity scored as

Increaser = 1, Tolerant = 2, Decreaser = 3; Spearman’s Rank correlation coefficient =

0.01, p = 0.96). The body mass of the species that were sensitive to forest

fragmentation ranged from 48 g to 485 g (average 199 g). Of the nine large-bodied

species (> 400 g), seven were tolerant of fragmentation, one was a decreaser and one

was an increaser (Table A3.1).

Biogeographical distribution

There is no clear association between species that are endemic to Australia and

sensitivity to forest fragmentation. Only six of the frugivore species that were common

enough in survey data to analyse for response to fragmentation are endemic to

Australia; one was a decreaser, one an increaser and four were tolerant (Table A3.1). Of

the six frugivore species that were decreasers, only one (the green catbird) is endemic to

Australia; the remaining decreaser species had large geographical distributions.

199

Rarity

In the present study, a species’ relative abundance (or rarity) was indicated by its

average abundance in extensive forest sites during surveys (Table A3.1). There is an

association between a species’ abundance and its sensitivity to fragmentation

(sensitivity scored as Increaser = 1, Tolerant = 2, Decreaser = 3; Spearman’s Rank

correlation coefficient = 0.37, p = 0.05). However, contrary to the expectation that less

common species may be more susceptible to fragmentation (Henle et al., 2004), this

analysis shows that decreaser species were typically common in extensive forest.

Patterns of resource specialisation

A frugivore species’ degree of habitat and dietary specialisation was determined

from information on their degree of dependence on rainforest and fruit, respectively.

Consistent with the expectation that resource specialists are more fragmentation

sensitive (see Section 1.4.2.2), decreaser species tended to be both rainforest and fruit

specialists. Five out of six (83%) decreaser frugivore species were rainforest specialists,

compared with (4 of 14) 29% of tolerant frugivore species and none of the five increaser

species were rainforest specialists (Fisher’s exact test (decreaser versus tolerant and

increaser species) χ2 = 8.68, p =0.008; Table 7.2). Similarly, 83% of decreaser frugivore

species were fruit specialists, compared with 36% of tolerant frugivores and 14% of

increasers (Fisher’s exact test (decreaser versus tolerant and increaser species) χ2 = 5.80,

p =0.03; Table 7.2)

200

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e ch

arac

teris

tic h

abita

t of

eac

h sp

ecie

s. D

iet

show

s th

e m

ain

food

item

s. N

o. g

ener

a is

the

num

ber

of p

lant

gen

era

(incl

udin

g in

trod

uced

taxa

) kn

own

to b

e co

nsum

ed b

y ea

ch

spec

ies.

Fra

g. R

esp

.1 C

om

mo

n n

ame

Bo

dy

mas

s (g

)2

Dis

trib

uti

on

ou

tsid

e A

ust

ralia

3 A

v.

abu

nd

. F

ore

st

typ

e5 D

iet6

Dec

reas

er

east

ern

tube

-nos

ed fr

uit-

bat

48

PN

G

0.38

R

F

F

br

own

cuck

oo-d

ove†

24

0 P

hil.,

Bor

n., S

uma.

, Mol

uc.,

Sul

aw.,

PN

G

4.80

M

F

F, S

wom

poo

frui

t-do

ve

465

PN

G

5.25

R

F

F

su

perb

frui

t-do

ve

110

Indo

., S

ulaw

., M

oluc

., P

NG

0.

56

RF

F

rose

-cro

wne

d fr

uit-

dove

12

5 In

do.

3.38

R

F

F

gr

een

catb

ird

207

End

emic

(su

btro

p)

3.75

R

F

F, I

, V

Tol

eran

t gr

ey-h

eade

d fly

ing-

fox

700

End

emic

M

F

N, F

blac

k fly

ing-

fox

674

End

emic

0.

50M

F

F, N

Aus

tral

ian

brus

h-tu

rkey

† 23

00

End

emic

0.

56

MF

S

, F, I

, V

w

hite

-hea

ded

pige

on†

420

End

emic

0.

56

RF

F

, S

em

eral

d do

ve†

135

Indi

a, C

hina

, Ind

o-M

alay

a, P

hil.

PN

G

0.38

M

F

S, F

, I

to

pkno

t pig

eon

475

End

emic

1.

06

RF

F

sulp

hur-

cres

ted

cock

atoo

† 86

0 P

NG

1.

5 M

F

S, F

, i

sc

aly-

brea

sted

lorik

eet†

75

E

ndem

ic

0.13

M

F

N, F

, S, I

Aus

tral

ian

king

-par

rot†

24

3 E

ndem

ic

1.44

R

F

S, F

, N

pa

le-h

eade

d ro

sella

† 11

0 E

ndem

ic

0.25

O

F

S, F

, N, I

com

mon

koe

l 24

5 Ir

an, P

akis

tan,

Indi

a, C

hina

, Phi

l., In

do.

0.38

M

F

F

ch

anne

l-bill

ed c

ucko

o

748

Indo

., P

NG

0.

06

MF

F

, I, V

little

wat

tlebi

rd

65

End

emic

0.

00

OF

N

, F, I

Lew

in's

hon

eyea

ter

34

End

emic

8.

00

RF

F

, N, I

pied

cur

raw

ong

398

End

emic

2.

75

MF

F

, I, V

satin

bow

erbi

rd

201

End

emic

0.

19

MF

F

, I, P

20

1

Fra

g. R

esp

.1 C

om

mo

n n

ame

Bo

dy

mas

s (g

)2

Dis

trib

uti

on

ou

tsid

e A

ust

ralia

3 A

v.

abu

nd

. F

ore

st

typ

e5 D

iet6

Incr

ease

r ro

ck d

ove†

* 30

8 al

l con

tinen

ts e

xcep

t Ant

arct

ic

0.00

M

OD

S

, I

ba

r-sh

ould

ered

dov

e†

130

PN

G

0.00

M

F

S

ra

inbo

w lo

rikee

t†

125

Indo

., P

NG

2.

75

MF

N

, S, F

, I

bl

ack-

face

d cu

ckoo

-shr

ike

134

Sou

th-e

ast A

sia,

PN

G, I

ndia

0.

13

MF

I,

S, F

figbi

rd

128

End

emic

2.

56

Mf,

Mod

F

Aus

tral

ian

mag

pie

299

PN

G (

Intr

od in

NZ

) 0.

13

OF

, Mod

. I,

S

T

orre

sian

cro

w

499

PN

G

1.44

O

F, M

od

V, I

, P, F

silv

erey

e 11

P

acifi

c Is

land

s, N

Z

1.06

M

F

N, I

, F

Und

eter

min

ed

won

ga p

igeo

n†

415

End

emic

0.

50

MF

S

, F, I

para

dise

rifl

ebird

10

4*

End

emic

(su

btro

p.)

0.50

R

F

F, I

rege

nt b

ower

bird

10

2 E

ndem

ic (

subt

rop.

) 0.

13

RF

F

, I

cr

imso

n ro

sella

†

135

End

emic

0.

31

MF

S

, F, N

, I

no

isy

fria

rbird

11

0 P

NG

0.

06

OF

N

, F, I

, V

bl

ue-f

aced

hon

eyea

ter

105

PN

G

0.00

O

F

I, N

, F

ba

rred

cuc

koo-

shrik

e 70

P

NG

0.

00

MF

F

, I

va

ried

trill

er

34

PN

G

0.06

R

F

I, F

, S

ol

ive-

back

ed o

riole

96

P

NG

0.

00

MF

I,

F

gr

ey b

utch

erbi

rd

91

End

emic

0.

00

OF

, Mod

I,

V, P

, S, F

mis

tleto

ebird

9

Pac

ific

Isla

nds

0.19

M

F

F, I

gala

h†

330

End

emic

0.

00

OF

S

, F, I

nois

y m

iner

75

E

ndem

ic

0.00

O

F

I, N

, F, V

1 F

ragm

enta

tion

resp

onse

is th

e re

spon

se p

atte

rn (

Dec

reas

er, T

oler

ant o

r In

crea

ser)

sho

wn

in th

is s

tudy

(C

hapt

er T

wo)

. Und

eter

min

ed is

spe

cies

that

wer

e de

tect

ed to

o in

freq

uent

ly

duri

ng s

urve

ys to

ass

ign

a fr

agm

enta

tion

res

pons

e. B

at r

espo

nses

wer

e de

term

ined

fro

m a

sin

gle

sum

mer

sur

vey.

2 M

ass

data

was

obt

aine

d fr

om (

Chu

rchi

ll, 1

998)

for

bat

s an

d B

aker

et a

l. (1

997)

for

bir

ds, e

xcep

t the

bar

red

cuck

oo-s

hrik

e (D

unni

ng, 1

993)

. * d

ata

for

the

para

dise

rif

lebi

rd f

rom

on

e in

divi

dual

. and

bat

s.

3 D

istr

ibut

ion

info

rmat

ion

was

fro

m th

e H

AN

ZA

B s

erie

s fo

r bi

rds

and

(Chu

rchi

ll, 1

998)

for

bat

s ; ‘

subt

rop.

’ sh

own

in b

rack

ets

afte

r E

ndem

ic s

peci

es in

dica

tes

that

the

spec

ies

is

ende

mic

to s

ubtr

opic

al A

ustr

alia

; rem

aini

ng e

ndem

ic s

peci

es a

re e

ndem

ic to

the

Aus

tral

ian

cont

inen

t. B

orn.

is B

orne

o, I

ndo.

is I

ndon

esia

, Mol

uc. i

s M

oluc

cas,

PN

G is

Pap

ua N

ew

Gui

nea,

Phi

l. is

Phi

lipp

ines

, Sum

a. is

Sum

atra

, Sul

aw. i

s S

ulaw

esi.

4 Bir

d sp

ecie

s’ a

vera

ge a

bund

ance

was

det

erm

ined

fro

m f

our

surv

eys

in e

ach

of th

e 16

site

s. B

at a

bund

ance

was

sur

veye

d on

ce in

eac

h si

te.

202

5 For

est t

ype(

s): R

F is

rai

nfor

est,

MF

is r

ainf

ores

t as

wel

l as

open

for

est a

nd/o

r w

oodl

and,

OF

is o

pen

fore

st, G

is g

rass

land

, MO

D is

mod

ifie

d.

6 Foo

d is

: F (

frui

t) S

(se

ed)

I (i

nver

tebr

ates

) N

(ne

ctar

) P

(no

n-fr

uit/

seed

pla

nt m

ater

ial)

V (

vert

ebra

tes)

. Lis

ted

in a

ppro

xim

ate

orde

r of

rel

ativ

e di

etar

y pr

opor

tion.

Foo

d an

d fo

rest

ty

pe in

form

atio

n fr

om B

lake

rs e

t al (

1984

), H

AN

ZA

B s

erie

s or

Cat

tera

ll et

al.

(200

4) f

or b

irds

and

fro

m E

by (

1995

), R

icha

rds

and

Hal

l (19

98),

Hal

l and

Ric

hard

s (2

000)

for

bat

s.

203

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