Flood Response and Palaeoecology of the High-Latitude, Terrigenoclastic Influenced Coral Reefs of Hervey Bay, Queensland, Australia

Flood response and palaeoecology of the high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia

Ian Robert Butler

The years 2011 and 2013 were difficult for the corals of Hervey Bay.

A thesis submitted for the degree of Doctor of Philosophy at

The University of Queensland in October 2015

School of Biological Sciences

Abstract

Worldwide, coral reefs are considered to be in a state of decline. While anthropogenic stressors such as land modification, overfishing, coral harvesting, recreational impacts and pollution are known to negatively impact coral reef communities and are of great concern, we have little knowledge of the natural historical range of variability in coral abundance and community structure with which to compare the current state. This is particularly the case for marginal coral reefs, which are not often the subject of research, but can offer unique insights into the natural and anthropogenic stressors of coral reefs.

In order to examine the natural and anthropogenic drivers of the taxonomic composition of marginal coral reefs, we examined both modern and historical coral assemblages from the high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia. To understand the potential impacts of modern terrestrial runoff, a likely driver of historical change on these reefs, photo-transects of modern coral communities before and after repeated flooding from nearby rivers were used to assess the spatial and temporal impacts of these disturbances on: coral abundance; coral community structure, and; flood-resistant trait diversity and composition. Water quality testing was carried out during the repeated flooding of 2013 to improve understanding of flood plume conditions and duration. The historical natural range of variation in coral abundance and community structure was examined through the collection of 17 sediment cores and 120 Uranium- Thorium dated samples, which enabled us to generate a precise chronological history of these coral reefs through the Holocene epoch.

Flooding resulted in significant changes to coral abundance and community structure and this varied along gradients of terrestrial and riverine exposure. Total hard and soft coral abundance decreased by ~40% after flooding in 2011, with a further decrease by ~28% of the remaining coral after flooding in 2013, for a cumulative decrease of ~56%. Salinity, total suspended solids, total nitrogen and total phosphorus at inshore coral reefs were altered for up to six months relative to pre- flooding baselines as a result of flooding in 2013. Submarine groundwater discharge caused substantial reductions in salinity at these reefs for a further four months. Taxonomic composition, as well as some traits, changed significantly as a result of flooding. Although some flood impacts were expected, for example the relative increase in abundance of flood resistant species in the coral community (e.g. Turbinaria), more changes were expected to have occurred in trait composition as a result of the flooding. This indicated the likely importance of other flood associated stressors, for ii

example hyposalinity, to flood related mortality. Spatial variability in the relative abundance of coral functional traits correlated well with both distance from the mainland and distance from rivers, indicating the importance of terrestrial and riverine stressors to reef coral community composition.

Palaeoecological investigations revealed that the coral reefs of Hervey Bay have existed for at least 6500 years. Reef geomorphology varied widely, from solid, vertical relief reefs to simple, non- accreting nearshore coral communities, depending on proximity to the mainland. Historical reef coral diversity was low (13 genera) and coral communities alternated cyclically (~1600 years) between those dominated by Acropora and those dominated by other genera. Modern communities are consistent with this cyclic pattern of change. While the millennial scale periodicity was similar to that of ENSO, it was also similar to the periodicity of Dansgaard-Oeschger, Bond, oceanic tidal and thermohaline cycles. Historical coral abundance and community structure correlated significantly with frequency of ENSO, though the effect on coral community structure varied with distance from mainland. Coral abundance and community structure also correlated with SST, with increased relative abundance of Acropora at higher temperatures, though total coral abundance decreased significantly nearshore with increased SST.

A lack of core material from 1200 - 1969 AD, possibly a hiatus in coral growth, prevented a clear assessment of the impacts of European colonisation and modification of local catchments. However, the contrast between currently low and historical high relative abundance of Acropora and the recent replacement with a novel coral community on Four Mile Reef after colonisation, suggests the possibility of anthropogenic influence.

It is predicted that the oceans will warm substantially in the future and that high-latitude reefs may play a major role as refugia. The coral reefs of Hervey Bay have persisted for 6.5 millennia and were resilient to past changes in climate, rainfall, sea-level and terrestrial runoff. Assuming that there have been no recent anthropogenic changes to the natural stressors of these reefs, there is potential for the reefs of Hervey Bay to act as a high latitude refuge in the future. Land and reef managers should take heed of the importance of terrestrial runoff, ENSO and ocean temperatures and strive to minimise anthropogenic impacts so that the remaining coral reefs will persist for many more millennia. iii

Declaration by author

This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis.

I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my research higher degree candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award.

I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School.

I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis.

Publications during candidature

Butler, I. R., Sommer, B., Zann, M., Zhao, J-x. and Pandolfi, J. M. (2013). "The impacts of flooding on the high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia." Coral Reefs 32(4): 1149-1163.

Butler, I. R., Sommer, B., Zann, M., Zhao, J-x. and Pandolfi, J. M. (2015). "The cumulative impacts of repeated heavy rainfall, flooding and altered water quality on the high-latitude coral reefs of Hervey Bay, Queensland, Australia." Marine Pollution Bulletin (Online) doi:10.1016/j.marpolbul.2015.04.047

Publications included in this thesis

– incorporated as Chapter 2.

Contributor Statement of contribution

Ian R Butler (Candidate) Designed experiments (35%)

Wrote and edited the paper (60%)

Data collection (50%)

Statistical analyses (100%)

Taxonomic identification (100%)

Brigitte Sommer Designed experiments (35%)

Data collection (40%)

Wrote and edited the paper (10%)

Maria Zann Designed experiments (10%)

Data collection (10%)

Wrote and edited the paper (10%)

Jian-xin Zhao Designed experiments (10%)

Wrote and edited the paper (10%)

John M Pandolfi Designed experiments (10%)

Wrote and edited the paper (10%)

– incorporated as Chapter 3.

Contributor Statement of contribution

Ian R Butler (Candidate) Designed experiments (60%)

Wrote and edited the paper (60%)

Data collection (80%)

Statistical analyses (100%)

Taxonomic identification (100%)

Brigitte Sommer Designed experiments (10%)

Data collection (15%)

Wrote and edited the paper (10%)

Maria Zann Designed experiments (10%)

Data collection (5%)

Wrote and edited the paper (10%)

Jian-xin Zhao Designed experiments (10%)

Wrote and edited the paper (10%)

John M Pandolfi Designed experiments (10%)

Wrote and edited the paper (10%)

vii

Contributions by others to the thesis

Brigitte Sommer contributed most of the photos for the baseline year (2010) of flood impacts research and played a major role in the initial design of flood impacts, including methodology for statistics. She assisted with the traits diversity analyses and contributed to the writing and editing of chapters 2, 3 and 4.

Maria Zann contributed photos for the Pt. Vernon East reef location for the baseline year. She also contributed to writing and editing of chapters 2 and 3.

John Pandolfi contributed to the conception, design and funding of the project and interpretation of the data. He also assisted with writing and editing of all chapters.

Jian-xin Zhao contributed to the conception, design and funding of the project and interpretation of the data. He also assisted with writing and editing of all chapters.

Tara Clark assisted with lab work for U-Series analyses and contributed to writing and editing of chapter 5.

Yuexing Feng assisted with all lab work for U-Series analyses.

Mauro Lepore assisted with all of the coring field work and the core processing lab work. He also assisted with the editing for chapters 2 and 5 and interpretation of data for chapter 5.

Statement of parts of the thesis submitted to qualify for the award of another degree

“None”

viii

Acknowledgements

My PhD would not have been possible without the generous help of many people and organisations. It is impossible for me to express my gratitude adequately in this space.

First of all, thank-you to John Pandolfi and Jian-xin Zhao, my supervisors, for all your patience, knowledge and advice. You have made me a much better researcher.

I gratefully acknowledge funding and support from the Australian Postgraduate Research Scholarship, the Australian Research Council Centre of Excellence for Coral Reef Studies and the National Environmental Research Plan (NERP) Tropical ecosystems hub 1.3, Queensland Department of Sports Information Technology, Innovation and the Arts and the Burnett Mary Regional Group. Conference and travel funding was provided by University of Queensland Faculty of Science Postgraduate Travel Awards (2013), the Australian Research Council Centre of Excellence for Coral Reef Studies and the National Environmental Research Plan (NERP) Tropical ecosystems hub 1.3.

I owe many thanks for the generous contribution of logistical support and provision of divers from the friendly, knowledgeable and simply wonderful staff at Queensland Department of National Parks Sport and Racing, Great Sandy Marine Park, Hervey Bay.

This project would have been impossible without generous contributions of time, effort and support from field volunteers for both photographic and coring work: Tyson Martin, Andrew Olds, Ross Smith, Nicole Leonard, Hayden Coburn and Omer Polak.

Many thanks for assistance in the Earth Sciences Radiometric Isotope Lab -Thorium lab from Tara Clark, Ai Nguyen, Yuexing Feng and Wei Zhou. Thanks also to the friendly staff from the Geology Rock lab for assistance with facilities for processing samples.

A big thank-you to Jenn Loder and Jodi Salmond from Reef Check Australia for support through this project. Reef Check is such a great organisation and I hope we continue working together into the future.

Many thanks go to all the members of the Marine Palaeoecology Lab at the University of Queensland for support with presentations and editing of manuscripts. In particular, I would like to

thank K-le Gomez-Cabrera for all the work she has done for me, especially for the extra pain I have caused as a remote student. Special thanks to Alberto Rodriguez-Ramirez for setting me straight on the statistical path. Many thanks to Jez Roff for so many great ideas, bringing reality to my occasional silly ideas and providing me a place to stay in Brisbane. Thanks to Matt Lybolt for initial concepts, coring methodology and planning.

A really big thank-you to Brigitte Sommer. You helped me so much through all aspects of this PhD, not to mention generously providing me with 2010 photographic data.

A big thank-you to Katie Cramer and Dick Norris from the Norris Lab at Scripps Institute, University of California, San Diego for novel ideas, conceptual support and for hosting Mauro and I for the XRF workshop.

I want to thank my thesis milestone readers Steven Salisbury and Kevin Welsh for keeping me on the straight and narrow, reassuring me and sorting out all those other things that could have made my PhD project go off the rails. Thanks for all your ideas Kevin, some of them are not in print…yet!

Mauro Lepore, you are an all-round awesome researcher and friend. You always had time to help me out with any questions, offer suggestions, edit manuscripts, help with field work and lab work, carry out R work, provide a place to stay, etc… I can’t thank you enough!

Thanks to staff at TropWater, James Cook University, in particular Jon Brodie, Michelle Devlin and Eduardo de Silva, for research ideas and support, especially helping out this novice with water quality interpretation!

A big thank you to Juan-Carlos Ortiz and Chris Doropoulos for some excellent statistical advice. Sorry guys if I got the application wrong!

I owe Kirsten Wortel, Amanda Delaforce and Sue Sargent many, many thanks for encouraging me to do this PhD, for providing ideas, local knowledge and assisting with fieldwork.

Thanks to Maria Zann for giving the all-round nudge for this PhD project, the recommendation and all the extra local/state government projects you have included me in. You have been a great mentor to me and you are a vast resource for government issues and local information. x

Thanks to Julian Negri, Bundaberg Aquascuba and Glen Burfit for generously helping me get my dive accreditation updated and renewed!

A very big thank you to my parents,Monique and Douglas Butler. You have provided support and encouragement to me in so many ways for all my life!

Finally, but most importantly, I owe an enormous debt of gratitude to my family – my wife Peta- Jane and my children Bob and Zoe. You have provided me unending patience, support and encouragement through this project. This PhD has taken so much of my time away from you and I will work hard to make sure it was worthwhile.

Keywords

Scleractinian coral, coring, flooding, palaeoecology, submarine groundwater discharge,

U-Series Thorium dating, traits, water quality, hiatus, El Niño Southern Oscillation

Australian and New Zealand Standard Research Classifications (ANZSRC)

ANZSRC code: 060205 Marine Ecology 60%

ANZSRC code: 060206 Palaeoecology 40%

Fields of Research (FoR) Classification

FoR code: 0602 Ecology 100%

xii

Table of Contents

Abstract ...... ii Declaration by author ...... iv Publications during candidature ...... v Publications included in this thesis ...... v Contributions by others to the thesis ...... viii Statement of parts of the thesis submitted to qualify for the award of another degree ...... viii Acknowledgements ...... ix Keywords ...... xii Australian and New Zealand Standard Research Classifications (ANZSRC) ...... xii Fields of Research (FoR) Classification ...... xii Table of Contents ...... xiii List of Figures...... xviii List of Tables ...... xxiii List of Abbreviations ...... xxvi Chapter 1: Introduction ...... 1 Global changes in ecosystems ...... 1 Coral reef crisis ...... 1 Marginal reefs: living on the edge ...... 2 Understanding the past by looking at the present ...... 3 Terrestrial runoff ...... 4 Anthropogenic impacts ...... 6 Hervey Bay and the Mary River ...... 6 Objectives ...... 7 References ...... 9 Figures ...... 15 Chapter 2: The impacts of flooding on the high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia ...... 16 Abstract ...... 17 Introduction ...... 17 Materials and methods ...... 18 The study area ...... 18 Flood plume and ambient water quality data ...... 19 Sampling methods ...... 19 Data analyses ...... 20 Results ...... 21 xiii

Water quality in the flood plume ...... 21 Pre- and post-flood abundance of hard and soft corals ...... 22 Impacts on community structure ...... 23 Discussion ...... 24 Flooding impacts on coral abundance ...... 24 Variability in flood impacts among reefs ...... 26 Changes in community structure ...... 27 Prospects for recovery ...... 28 Implications of flood impacts to Great Sandy Marine Park management ...... 29 Climate change and catchment management ...... 29 Acknowledgments ...... 30 References ...... 30 Chapter 3: The cumulative impacts of repeated heavy rainfall, flooding and altered water quality on the high-latitude coral reefs of Hervey Bay, Queensland, Australia ...... 32 Abstract ...... 33 Introduction ...... 33 Materials and methods ...... 34 The study area ...... 34 Nearshore water quality monitoring ...... 34 Offshore versus nearshore comparison of water quality data ...... 36 Photo-transect methodology for measuring coral abundance ...... 36 Data analyses ...... 37 Results ...... 37 Site variability in water quality ...... 37 Salinity in flood plumes ...... 37 Delayed episode of hyposalinity ...... 37 Turbidity and total suspended solids in the flood plume ...... 37 Total nutrients in the flood plume ...... 37 Nutrients versus TSS and salinity ...... 39 Change in total abundance of hard and soft corals after flooding ...... 39 Discussion ...... 39 Flooding ...... 39 Importance of flood plume pathways and distance from the Mary River on flooding impacts ...... 40 Reduced impacts of subsequent floods ...... 41 Nearshore versus offshore water quality ...... 42 Submarine groundwater discharge ...... 42 Recovery...... 43

xiv

Conclusion ...... 43 Acknowledgements ...... 43 References ...... 43 Chapter 4: Terrestrial runoff, trait filtering and the assembly of resilient coral communities on the high-latitude coral reefs of Hervey Bay, Queensland, Australia ...... 45 Abstract ...... 46 Introduction ...... 47 Materials and methods ...... 49 The study area ...... 49 Sampling methods for measuring taxonomic composition of coral communities ...... 49 Functional traits categories ...... 50 Calculation of functional diversity indices ...... 51 Permutational analyses of variance of the impacts of flooding on coral communities ...... 52 Canonical analyses of the spatial distribution of coral species and traits ...... 53 Predicted outcomes from flooding disturbance ...... 53 Results ...... 54 Impacts on community structure ...... 54 Functional diversity...... 55 Effect of flooding on individual functional traits ...... 55 Spatial distribution of traits relative to distance from mainland and distance from nearest river ...... 55 Discussion ...... 56 Impacts of repeated flooding on Hervey Bay coral communities ...... 56 Changes in the relative composition of coral traits as a result of repeated flooding ...... 57 Spatial distribution of traits ...... 58 Individual trait distributions in Hervey Bay: Resistance to sedimentation ...... 58 Reproduction ...... 59 Larval dispersal and recruitment ...... 60 Transfer of Symbiodinium ...... 61 Conclusion ...... 62 Acknowledgements ...... 62 References ...... 63 Tables ...... 68 Figures ...... 72 Supplementary tables ...... 78 Chapter 5: Historical drivers of spatial and temporal variation in high-latitude coral reef formation and community composition of Hervey Bay, Queensland, Australia ...... 79 Abstract ...... 80

Introduction ...... 81 Materials and methods ...... 83 The study area ...... 83 Modern coral assemblages ...... 84 Coral death assemblages ...... 84 Historical coral assemblages: Reef matrix cores ...... 84 Sediment categories for analyses ...... 85 U-Th dating ...... 85 Accretion ...... 86 ENSO data ...... 86 SST data ...... 87 Data analyses ...... 87 Results ...... 89 Current coral communities ...... 89 Coral composition in death assemblages ...... 90 U-Th dating ...... 90 Core sediments...... 90 Accretion rates ...... 92 El Niño frequency versus sediment types and SST...... 92 Historical community composition through cores ...... 92 Changes in coral abundance with sediment type, accretion rate, ENSO and SST ...... 93 Discussion ...... 95 El Niño Southern Oscillation ...... 95 Climate, temperature and sea-level changes ...... 97 Hiatus in reef growth ...... 99 Refugia potential of Hervey Bay ...... 99 Anthropogenic impacts ...... 100 Conclusion ...... 101 Acknowledgments ...... 102 References ...... 102 Tables ...... 110 Figures ...... 115 Supplementary information ...... 133 Choice of specific coring locations ...... 133 Reef matrix coring methodology ...... 133 Supplementary figures ...... 134 Chapter 6: Concluding remarks...... 135 xvi

El Niño Southern Oscillation, SST and sea-level ...... 136 Anthropogenic effects ...... 137 Refugia in southern Queensland ...... 138 Implications for catchment and marine park management: ...... 138 Future research...... 140 Conclusion ...... 142 References ...... 143

xvii

List of Figures

Chapter 1: Introduction

Fig. 1 Map showing locations of rivers and coral reefs of Hervey Bay, Queensland, Australia ……………………………………………………………………………………15

Chapter 2: The impacts of flooding on the high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia

Fig. 1 Location of Mary River, coral reef study sites and water quality sites near Hervey Bay, Queensland, Australia ………………………………………………………………..19

Fig. 2 Turbidity, salinity, total phosphorus (TP), total nitrogen (TN) and dissolved oxygen

saturation (DOsat) in Great Sandy Strait (site GSS) illustrating passage of the Mary River flood plume from 25 August 2010 to 2 August 2011. a) Mean turbidity and salinity from all depths; b) TN and TP from 0.2 m; c) Dissolved oxygen saturation from all depths ……...21

Fig. 3 Pre- and post-flood abundance of benthos and substrate on Hervey Bay reefs; a) Absolute abundance of benthos and substrate; b) Relative abundance of benthic groups ..22

Fig. 4 Pre- and post-flood absolute abundance of total (hard and soft) live coral on six reefs from Hervey Bay, Queensland, Australia ………………………………………………….23

Fig. 5 Photographs of Turbinaria mesenterina at Pt. Vernon East: a) pre-flood in August 2009 and b) post-flood July 2011 ………………………………………………………….23

Fig. 6 Pre- and post-flood abundance of total (hard and soft) live coral on 6 reefs from Hervey Bay, Queensland, Australia a) relative to distance from the mainland; b) relative to distance from the mouth of the Mary River ………………………………………………..24

Fig. 7 Non-metric multidimensional scaling (NMDS) plot of total (hard and soft) coral community structure on 6 reefs from Hervey Bay, Queensland, Australia pre- and post-flood ………………………………………………………………………………………………26

Fig. 8 Pre- and post-flood relative abundances of coral genera for 6 reefs from Hervey Bay, Queensland, Australia ………………...... 27

Fig. 9 Extent and subsequent contraction of Mary River flood plume during January 2011 flooding of Hervey Bay, Queensland, Australia …………………………………………...28

xviii

Chapter 3: The cumulative impacts of repeated heavy rainfall, flooding and altered water quality on the high-latitude coral reefs of Hervey Bay, Queensland, Australia

Fig. 1 Location of Mary and Burnett rivers, coral reef study sites, nearshore(*) and offshore(**) water quality sites in Hervey Bay, Queensland, Australia. ……………….…35

Fig. 2 Extent of first Mary River flood plume from 26 January to 2 February 2013 in Hervey Bay, Queensland, Australia characterized by remotely sensed colour classification……….36

Fig. 3 Total nitrogen (TN) (a), total phosphorus (TP) (b), salinity (c) and total suspended solids (TSS) (d) measured at nearshore reef water quality sites in Hervey Bay, Queensland, Australia during and after the Mary River floods of 2013………………………………….38

Fig. 4 Rainfall in upper Mary River catchment (Kenilworth) (a), Mary River height (at Miva station) and average salinity at the reef sites (b) in Hervey Bay, Queensland, Australia. …39

Fig. 5 Salinity (a) and turbidity (b) with water depth at the nearshore government water quality site, Urangan Jetty (UJ), Hervey Bay, Queensland, Australia before, during and after the Mary River floods of 2013……………………………………………………………..40

Fig. 6 Total suspended solids (a), total nitrogen (b) and total phosphorus (c) at nearshore reef water quality sites and at the offshore government water quality site in Hervey Bay, Queensland, Australia in comparison with local environmental guidelines (DERM 2010a) ……………………………………………………………………………………….……...40

Fig. 7 Plots of: total nitrogen versus (a) total suspended solids and (b) salinity; total phosphorus versus (c) total suspended solids and (d) salinity, and; (e) total suspended solids versus salinity during the Mary River floods of 2013 in Hervey Bay, Queensland, Australia ………………………………………………………………………………………………41

Fig. 8 Total abundance of hard and soft coral for overall reefs (a) and for each reef (b) in 2010, 2011 and 2013 in Hervey Bay, Queensland, Australia ……………………………..42

Fig. 9 Total abundance of total hard and soft coral on six reefs from Hervey Bay, Queensland, Australia in 2010, 2011 and 2013: (a) relative to distance from mainland; (b) distance from nearest river. ………………………………………………………………...42

Chapter 4: Terrestrial runoff, trait filtering and the assembly of resilient coral communities on the high-latitude coral reefs of Hervey Bay, Queensland, Australia

xix

Fig. 1 Location of Mary River, Burnett River and coral reef study sites in Hervey Bay, Queensland, Australia. All mapped areas are within Great Sandy Marine Park. ………….72

Fig. 2 Non-metric multidimensional scaling (NMDS) plot of total hard and soft coral community structure on the six reefs from Hervey Bay, Queensland, Australia for 2010, 2011 (after single flood) and 2013 (after repeated flooding). ……………………………..73

Fig. 3 Photographs from Hervey Bay, Queensland, Australia; a) Goniopora sp. mortality after flooding; b) Turbinaria spp. thriving; c) Acropora thriving at Big Woody; d) Inshore reefs like Pialba have high sedimentation; e) Favids with large polyps have generally strong sediment removal ability …………………………………………………………………. 74

Fig. 4 Relative abundance of genera of hard and soft corals for the years 2010 and 2013 at the individual six reefs of Hervey Bay, Queensland, Australia (a–f) and for all reefs combined (g). ………………………………………………………………………………75

Fig. 5 Canonical analysis of principal coordinates (CAP) showing (a) hard and soft coral community composition (most common genera) between 2010 and 2013 for coral reefs of Hervey Bay, Queensland, Australia in relation to distance from the mainland and distance from the nearest river. (b) Trait and life-history categories that primarily (Correlation > 0.4) define the communities relative to distance from mainland and distance from nearest river. ………………………………………………………………………………………………76

Fig. 6 Changes in trait categories for a) Depth Range, b) Propagule Development Rate and c) Hard versus Soft corals before (2010) and after repeated flooding (2013) in Hervey Bay, Queensland, Australia …………………………………………………………….………..77

Chapter 5: Historical drivers of spatial and temporal variation in high-latitude coral reef formation and community composition of Hervey Bay, Queensland, Australia.

Fig. 1 Locations of coral reef and coring sites in Hervey Bay, Queensland, Australia…..115

Fig. 2 Locations of cores on: (a) Big Woody Reef , (b) Pialba Reef , (c) Pt. Vernon West Reef and (d) Four Mile Reef in Hervey Bay, Queensland, Australia. ……………………116

Fig. 3 Typical coral assemblages for: (a) Pt. Vernon West Reef, (b) Pialba Reef, (c) Big Woody Reef: thick encrusting Acropora, (d) Big Woody Reef: Goniopora community and (e) Four Mile Reef in Hervey Bay, Queensland, Australia. ………………………………117

Fig. 4 Life assemblages (2011) and death assemblages from (a) Pt. Vernon West Reef, (b) Pialba Reef, (c) Big Woody Reef and (d) Four Mile Reef in Hervey Bay, Queensland, Australia. ……………………………………………………………………………….…118

Fig. 5 Plot of ages of all U-Th aged samples from cores versus paleo water depth from reefs in Hervey Bay, Queensland, Australia. (a) all four reefs, includes accretion trend lines for cores (b) Recent 1000 years for Four Mile Reef samples only. …………………………..119

Fig. 6 Core composition diagrams showing percentage coral (4 mm+), relative abundance of coral genera, sediment facies and locations of U-Series samples and ages for Pt. Vernon West Reef, Hervey Bay, Queensland, Australia. ………………………………………...120

Fig. 7 Core composition diagrams showing percentage coral (4 mm+), relative abundance of coral genera, sediment facies and locations of U-Series samples and ages for Pialba Reef, Hervey Bay, Queensland, Australia. …………………………………………………..…121

Fig. 8 Core composition diagrams showing percentage coral (4 mm+), relative abundance of coral genera, sediment facies and locations of U-Series samples and ages for Big Woody Reef, Hervey Bay, Queensland, Australia. ………………………………………………..122

Fig. 9 Core composition diagrams showing percentage coral (4 mm+), relative abundance of coral genera, sediment facies and locations of U-Series samples and ages for Four Mile Reef, Hervey Bay, Queensland, Australia. ……………………………………………….123

Fig. 10 Frequency of El Niño events with core sediment type from coral reefs from Hervey Bay, Queensland, Australia. ………………………………………………………………124

Fig. 11 Percent total coral (4 mm+) in core subsections relative to sediment type from coral reefs in Hervey Bay, Queensland, Australia. …………………………………………….124

Fig. 12 Regression of percent total coral in core subsections versus frequency of El Niño events for (a) overall reefs and (b) nearshore versus offshore reefs in Hervey Bay, Queensland, Australia. …………………………………………………………………….125

Fig. 13 Regression of percent total coral in core subsections versus frequency of SST at nearshore and offshore reefs of Hervey Bay, Queensland, Australia. ……………………126

Fig. 14 Relative abundance of hard coral genera within sediment types in cores from coral reefs in Hervey Bay, Queensland, Australia. …………………………………………….127

xxi

Fig. 15 Relative abundance of coral genera in cores during fast (>8.4 mm yr-1), medium (0.8 - 8.4 mm yr-1) and slow (<0.8 mm yr-1) accretion periods on coral reefs of Hervey Bay, Queensland, Australia. ……………………………………………………………………127

Fig. 16 Reef coral composition through cores with respect to high, medium and low frequency of El Niño events for (a) nearshore reefs (Pialba and Pt. Vernon West) and (b) offshore reefs (Big Woody and Four Mile) in Hervey Bay, Queensland, Australia. ….…128

Fig. 17 Reef coral composition through cores with respect to high (>29.26 o C), medium (29.00 – 29.26 o C), and low (< 29.00 o C) SST categories for (a) nearshore reefs (Pialba, Pt. Vernon West) and (b) offshore reefs (Big Woody and Four Mile) in Hervey Bay, Queensland, Australia. ………………………………………………………………..…129

Fig. 18 Average relative abundance of coral genera over time for all coral reef cores combined from Hervey Bay, Queensland, Australia with indications of dates for sea level (SL) instability or rise. …………………………………………………………………….130

Fig. 19 Continuous wavelet (Morlet) transform analysis of (a) average percent relative abundance (by century) of Acropora in Hervey Bay, Queensland, Australia (b) frequency of El Niño events per century (Moy et al. 2002). …………………………………………..131

Fig. 20 Autocorrellogram showing the results of autocorrelation analysis of average relative abundance (by century) of Acropora from coral reefs in Hervey Bay, Queensland, Australia. ……………………………………………………………………………………………..132

Supplementary Fig. 1 Plot of all U-Th ages for all samples from cores for the cored coral reefs of Hervey Bay, Queensland, Australia. Accretion trend lines join samples ...... 134

Chapter 6: Concluding remarks

xxii

List of Tables

Chapter 1: Introduction

Chapter 2: The impacts of flooding on the high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia

Table 1 Size, depth range, distance to mainland and distance to mouth of the Mary River of the reef survey sites ……………………………………………………………………...…19

Table 2 Water quality data collected Jan – Feb 2011 from plume water near reef study sites in Hervey Bay, Queensland, Australia ……………………………………………………..20

Table 3 Historical mean (1994 – 2012) total nitrogen (TN), total phosphorus (TP), salinity,

turbidity and dissolved oxygen saturation (DOsat) for Great Sandy Strait (site GSS) and for the Mary River (site MRU), along with Environmental Protection Objectives for that location ……………………………………………………………………………………..22

Table 4 Permutational analysis of variance (PERMANOVA) with distance covariates for changes in absolute cover of total (hard and soft) coral on the reefs of Hervey Bay, Queensland, Australia pre- and post-flood, January 2011 …………………………………23

Table 5 Pre- and post-flood coral community composition (presence/absence) and total species richness on the reef of Hervey Bay, Queensland, Australia ……………………….25

Table 6 SIMPER analysis of pre-flood coral communities on the reefs of Hervey Bay, Queensland, Australia ………………………………………………………………………28

Table 7 Permutational analysis of variance (PERMANOVA) with distance covariates for changes in coral community structure at genus level on the reefs of Hervey Bay, Queensland, Australia pre- and post-flood, January 2011 …………………………………28

Table 8 SIMPER analysis of pre- versus post-flood coral communities on the reefs of Hervey Bay, Queensland, Australia ……………………………………………………..…28

Chapter 3: The cumulative impacts of repeated heavy rainfall, flooding and altered water quality on the high-latitude coral reefs of Hervey Bay, Queensland, Australia

Table 1 Size, depth range, distance to mainland and distance to mouth of the nearest river for the reef survey sites in Hervey Bay, Queensland, Australia ……………………………36

xxiii

Table 2 Comparison of extremes of flood plume water quality parameters and duration below normal (salinity) or above environmental guidelines measured from offshore Great Sandy Straits (WQGSS) location for 2011 and 2013 and the nearshore reefs in 2013 of Hervey Bay, Queensland, Australia ………………………………………………………..39

Table 3 Permutational analysis of variance (PERMANOVA) with distance covariates for changes in absolute cover between 2011 and 2013 for total (hard and soft) coral on the reefs of Hervey Bay, Queensland, Australia ……………………………………………………..42

Table 4 Permutational analysis of variance (PERMANOVA) with distance covariates for changes in absolute cover after repeated flooding (2010 – 2013) for total (hard and soft) coral on the reefs of Hervey Bay, Queensland, Australia ………………………………….43

Chapter 4: Terrestrial runoff, trait filtering and the assembly of resilient coral communities on the high-latitude coral reefs of Hervey Bay, Queensland, Australia

Table 1 List of functional traits and sub-categories for assessing composition of the hard coral communities of Hervey Bay, Queensland, Australia ………………………………...68

Table 2 List of taxa, coral species composition (presence/absence) and total species richness on the reefs of Hervey Bay, Queensland, Australia before recent flooding (2010) and after repeated flooding (2013). ………………………………………………………………..…69

Table 3 Summary results for permutational analysis of variance (PERMANOVA) with distance covariates for changes in taxonomic composition (hard and soft genera) on the reefs of Hervey Bay, Queensland, Australia after single years of flooding (2010 vs. 2011, 2011 vs. 2013) and after repeated years of flooding (2010 vs. 2013). …………………………...70

Table 4 SIMPER analysis of 2010 and 2013 coral communities on the reefs of Hervey Bay, Queensland, Australia. ……………………………………………………………………...70

Table 5 Summary results for permutational analysis of variance (PERMANOVA) with distance covariates for changes in individual functional traits on the reefs of Hervey Bay, Queensland, Australia after single years of flooding (2010 vs. 2011, 2011 vs. 2013) and after repeated years of flooding (2010 vs. 2013). ………………………………………………..71

Supplementary Table 1 Functional traits and life history characterisation for hard coral species of Hervey Bay, Queensland, Australia. ……………………………………………78

xxiv

Chapter 5: Historical drivers of spatial and temporal variation in high-latitude coral reef formation and community composition of Hervey Bay, Queensland, Australia.

Table 1 List of coral reef study sites in Hervey Bay, Queensland, Australia with descriptions of area, depth, distance from mainland, distance from nearest river (likely to impact), fetch to the southeast and number of cores collected. …………………………..110

Table 2 List of coral samples taken from cores for U- Th dating from four coral reefs of Hervey Bay, Queensland, Australia. ……………………………………………………...110

Table 3 Ages of death assemblages at Pt. Vernon West, Pialba and Big Woody reefs from Hervey Bay, Queensland, Australia. ……………………………………………………..112

Table 4 List of genera present in reef matrix cores of four coral communities of Hervey Bay, Queensland, Australia………………………………………………………………..113

Table 5 Permutational analysis of variance (PERMANOVA) for coral community composition at genus level in core subsections with factors for frequency of El Niño events (high, medium, low) and for distance from mainland (near, far) for the reefs of Hervey Bay, Queensland, Australia. …………………………………………………………………....113

Table 6 Permutational analysis of variance (PERMANOVA) for coral community composition at genus level in core subsections with factors for SST (high, medium, low) and for distance from mainland (near, far) for the reefs of Hervey Bay, Queensland, Australia. ……………………………………………………………………………………………..114

Chapter 6: Concluding remarks

xxv

List of Abbreviations

ANOSIM – Analysis of Similarity

ANZECC – Australia and New Zealand Environment and Conservation Council

CPCe – Coral Point Counts with Excel Extensions

CT – Computed Axial Tomography

DOsat – Dissolved Saturated Oxygen

DSITIA – Department of Science, Information Technology Innovation and the Arts

ENSO – El Niño Southern Oscillation

FDiv – Functional Diversity

FEve – Functional Evenness

GBR – Great Barrier Reef

GSMP – Great Sandy Marine Park

GSS – Great Sandy Strait

HAT – Highest Astronomical Tide

MMR – Mouth of Mary River water quality site

MPD – Mean Pairwise Distance

MRU – Mary River Upstream water quality site

NMDS – Non-Metric Multidimensional Scaling

NOAA – National Oceanic and Atmospheric Administration

NRV – Natural Range of Variability

PERMANOVA – Permutational Analysis of Variance

SES – Standard Effect Size

TN – Total Nitrogen

TP – Total Phosphorus

TSS – Total Suspended Solids

U-Th – U- Series dating, Uranium–Thorium dating

xxvi

Chapter 1 Chapter 1: Introduction

Global changes in ecosystems

Ecological systems are variable over many different temporal scales (Fukami and Wardle 2005). We are currently experiencing loss of biota (McCauley et al. 2015) at rates that some researchers are comparing with events such as the Cretaceous - Paleogene mass extinction (Pimm and Raven 2000; Stork 2010). While anthropogenic changes to the environment and climate are widely implicated for this change, there are also other natural drivers of change such as climate (e.g. El Niño Southern Oscillation (ENSO)), solar cycles / radiative forcing and geological activity (e.g. Volcanism). In addition, the perception of change is clouded by shifting baselines syndrome, whereby what is currently considered natural may actually be a significantly altered state which is not representative of historical natural condition and not an appropriate baseline for measuring change (Pauly 1995). In order to better understand natural variability and change, it is often necessary to examine change over much longer temporal scales than are typically examined in ecology (Fukami and Wardle 2005). One way of identifying the more natural or pristine state of a system is by examining the history of that system and through this we may be able to measure change with respect to the system’s natural historical range of variability (Morgan et al. 1994)

Coral reef crisis

Worldwide, coral reefs appear to be in a state of decline (Pandolfi et al. 2003; Quinn and Kojis 2006; Veron 2008; Aronson 2011; WRI 2011) and it is thought by some that increasing numbers of species of coral are under threat of extinction (Carpenter et al. 2008). Substantial declines in coral cover over recent decades have occurred in the Caribbean (Cramer et al. 2012) and the Pacific (Hughes et al. 2003), including the Great Barrier Reef (GBR) (De’ath et al. 2012), where World Heritage status is now being re-evaluated (Thurlow 2013). Anthropogenic stressors such as overfishing, terrestrial runoff, coral harvesting, recreational impacts and pollution are all implicated in the degradation of coral reef environments (Hughes 2008) and are of increasing concern as climate changes (Hughes et al. 2010). There are many studies documenting short-term declines or impacts on coral reefs (Rogers and Garrison 2001; Jokiel 2006; Adjeroud et al. 2009; Chen et al. 2009; Guillemot et al. 2010; Jones and Berkelmans 2014). However, the magnitude of change from

Chapter 1 an historical perspective is vital to placing these short-term patterns in the context of natural historical variation (Pandolfi et al. 2003; Pandolfi 2011a).

Coral reefs are a model ecosystem for the reconstruction of historical state because of the ability of scleractinian corals and other reef organisms to secrete hard skeletons that build 3-dimensional structures that fossilize. Fossil reef taxa are readily identifiable and measurable and their ages can be determined by a number of high-resolution radiometric methods. Fossil reefs represent an important archive for the understanding of modern reef communities and how they have changed through time (Pandolfi and Greenstein 2007; Montaggioni and Braithwaite 2009). In addition, fossil reefs, through examination of geochemistry, reef development and community change, can act as a proxy for examining palaeoclimate, historical ocean temperatures, salinity, turbidity and pH (Pandolfi 2011b). The extraction of cores from coral reef sediments has proven a useful way of documenting historical changes in coral reefs around the world (Dardeau et al. 2000; Perry et al. 2008; Carilli et al. 2009; Twiggs and Collins 2010; Cramer 2011; Roche et al. 2011; Toth et al. 2012; Roff et al. 2013) where coral growth is optimal.

Marginal reefs: living on the edge

The edge of an organism’s range is a good place to investigate the mechanisms of persistence to less optimal conditions (Parmesan et al. 2005; Kawecki 2008). These edges are locations where even small changes in the environment may result in significant changes to a population, thus potentially providing detailed understanding of drivers of ecological and evolutionary change (Kawecki 2008). Under climate change, geographic range shifts are expected (Poloczanska et al. 2013) and edge populations are known to be important in diversification and speciation (Budd and Pandolfi 2010), enabling adaptation to novel environmental conditions (Sexton et al. 2009; Lynch et al. 2013). Palaeoecological studies along these edges can provide insight into the causes of population turnover or decline (Parmesan et al. 2005).

Scleractinian corals prefer a relatively narrow range of temperature, salinity, nutrient levels, aragonite saturation and light penetration (Kleypas et al. 1999). Outside these optimal conditions, coral reef communities may experience disturbance, physiological distress (e.g. bleaching and disease), reduced calcification and increased mortality (Kleypas et al. 1999). In open ocean coral reefs, these conditions are exceeded occasionally and their communities stressed for a short duration. However, some coral reefs, termed “marginal” (Guinotte et al. 2003), normally exist in 2

Chapter 1 conditions for which some of the parameters are well outside of optimal conditions and, although growth rates and fecundity may be lowered (Harriott and Banks 2002), the coral communities are able to persist in these conditions. These types of habitats offer unique insight into how stressors impact coral reef development and coral community assembly.

Good examples of coral reefs thriving at the edge of their range are the coastal coral reefs found in subtropical eastern Australia. These coral reefs are subject to lower temperatures, relatively low light conditions, and reduced aragonite saturation in comparison with their more tropical counterparts. They also tend to have limited larval transport pathways as a result of limited access to warm water currents (Beger et al. 2014). Under climate change, subtropical reefs are predicted to undergo greater changes than tropical reefs, resulting in increased beta diversity through range shifts, altered dispersal patterns, decreased survivorship and habitat loss (Beger et al. 2014). It is also possible that these marginal areas may become less marginalised through the southward migration of coral species, which has occurred in the past (Greenstein and Pandolfi, 2008) and is currently in progress in Japan (Yamano et al. 2011). Very little research has taken place on higher latitude coral reef areas and, as a consequence, little is understood about their ecology (Beger et al. 2011; Beger et al. 2014). Palaeoecological data from high latitude near-shore reefs are generally lacking, though some work has been carried out in Japan (Hongo and Kayanne 2010) and in Moreton Bay, along the eastern coast of Australia (Lybolt et al. 2011).

Understanding the past by looking at the present

Modern communities are often affected by the same environmental drivers which have shaped historical communities (Rull 2010). Thus, understanding how modern coral reefs change as a result of environmental stressors may provide insight into what has driven change in coral communities through the millennia. Recently, ENSO has been identified as a potential driver for historical variation in coral composition from reefs in Panama (Toth et al. 2012), though the mechanisms are not clearly understood. The responses of coral reefs to current ENSO phases and associated weather events can help to interpret these responses in the past. For the east coast of Queensland, Australia, El Niño phases typically result in low rainfall and drought conditions, while La Niña periods are typified by increased storm activity, including tropical cyclones, high rainfall and flooding. The comparison of modern coral responses to these two phases, particularly with respect to terrestrial runoff, could provide increased understanding of the historical responses. In turn,

Chapter 1 knowledge of how these processes play out over longer time scales will provide insight into the future response of living, sub-tropical reefs to environmental change.

Terrestrial runoff

Increased terrestrial runoff and flooding is one of the major consequences of La Niña associated high rainfall. Terrestrial runoff and flooding, especially in locations in close proximity to fluvial sources (Risk and Edinger 2011), directly affects coral reef environments through hypo-salinity, increased sedimentation and elevated turbidity and nutrients (Fabricius 2005; Risk 2014). The effects of terrestrial runoff on corals can vary dramatically among temporal and spatial scales (Van Woesik et al. 1995; Ayling and Ayling 1998; Fabricius and Wolanski 2000; Fabricius 2005) and little is known about what constitutes lethal exposure, particularly where conditions are already marginal.

Corals are physiologically sensitive to hyposalinity, which affects osmoregulation, and mortality may occur within days of exposure to salinities at or below 30 ppt (Jokiel et al. 1993; Chartrand et al. 2009). During periods of flooding, this sensitivity will also result in reduced capacity for sediment removal (Lirman and Manzello 2009).

Sedimentation may directly affect coral in many ways. A major impact of sedimentation on coral is through the physiological cost of sediment rejection, which can affect growth, calcification and reproduction (ISRS 2004; Fabricius 2005; Perry 2011; Risk and Edinger 2011). Sedimentation may also result in direct polyp tissue damage (Perry 2011), burial or smothering (Sanders and Baron- Szabo 2005; Risk and Edinger 2011) and restrict larval settlement (Risk and Edinger 2011) and survival (Gilmour 1999; Fabricius et al. 2003). Finally, reefs which form in high sediment environments are less likely to vertically accrete carbonate reef only, but instead form layers of sediment with reef matrix interspersed or layered within the sediment (Sanders and Baron-Szabo 2005).

Turbidity results in reduced light penetration through the water column, which may impact a coral reef through physiological stress and starvation due to reduced photosynthetic production of the coral’s zooxanthellae (Philipp and Fabricius 2003; Risk and Edinger 2011). Where turbidity is chronic or long term, the depth range (photic zone) for the corals is reduced (Perry 2011; Risk and

Chapter 1 Edinger 2011) and the reef community may be restricted to certain depths and have lowered biodiversity (Fabricius 2005). Crustose coralline algae may be significantly decreased on turbid reefs relative to non-turbid reefs (Fabricius and De'ath 2001). This reduces the available substrate for coral larvae settlement (Harrington et al. 2004; Nelson 2009) and diminishes the capacity of a reef to form complex three dimensional structures (Sanders and Baron-Szabo 2005; Perry and Smithers 2006), which is important to the diversity found on reefs (Wilson et al. 2007; Walker et al. 2009).

Terrestrial runoff may contain high levels of pollutants such as nitrogen, phosphorus, metal and herbicides (ISRS 2004; Fabricius 2005; Costa et al. 2008; Packett et al. 2009; Brodie et al. 2012a; Brodie et al. 2012b), particularly from urbanised catchments or those highly modified for such land uses as farming and grazing (Packett et al. 2009). Mortality from disease is far more likely if the sediment contains large amounts of nutrients (Fabricius et al. 2003; Risk and Edinger 2011; Pollock et al. 2014). Many agricultural chemicals, industrial chemicals and heavy metals are known to accumulate in and negatively impact coral reef environments (Reichelt-Brushett and Harrison 1999; Cervino et al. 2003; Smith et al. 2003; Jones 2007; Lewis et al. 2009).

Finally, chronic terrestrial runoff can affect coral community structure through diminished growth, calcification and recruitment (Harriott and Banks 2002; Thomson and Frisch 2010), which restrict corals in terms of depth (van Woesik and Done 1997), community complexity (Yamano et al. 2001) and community composition (Dikou and van Woesik 2006; van Woesik 2009; Golbuu et al. 2011). Other organisms, such as macroalgae (Nugues and Roberts 2003) or sponges and ascidians (Costa et al. 2008) may start to competitively dominate a reef community (Fabricius et al. 2005) and then also prevent settlement of coral larvae (Diaz-Pulido et al. 2010). Herbivores, which are important in the control of macroalgae (Hughes et al. 2007; Ledlie et al. 2007; Olds et al. 2011) may also be reduced in reef areas with higher turbidity (Rodriguez 2006). Disturbance, such as that which occurs during significant terrestrial runoff and flooding, can play a major role in the stability of a coral community and the subsequent recovery, or lack thereof, will determine the persistence of the coral community (Karlson 1999; Rachello-Dolmen and Cleary 2007). The warming climate is predicted to increase the frequency of these disturbances (DERM 2009; Dowdy et al. 2015) and for a coral reef to persist, it is necessary that adequate periods of time are available between disturbances for recovery periods which allow for a return of health, enable growth and allow for the recruitment of new corals to the reefs (Karlson 1999; Graham et al. 2011; Johns et al. 2014).

Chapter 1 Anthropogenic impacts

Disturbance to coral reefs occurs naturally as a result of, for example, storms, thermal stress and flooding; however, when these disturbances coincide with or are exacerbated by anthropogenic stressors, such as overfishing or land modifications, then the natural pace of recovery may be significantly altered (McCulloch et al. 2003; IPCC 2007; Hoegh-Guldberg 2011; Pandolfi et al. 2011) and there may be significant alterations to a community. Long-term decline from anthropogenic drivers have been observed from studies of the palaeoecology of reefs from the Caribbean (Cramer et al. 2012), the eastern Pacific (Cortes 1990), and in eastern Australia on the Great Barrier Reef (Roff et al. 2013) and Moreton Bay (Lybolt et al. 2011).

Hervey Bay and the Mary River

The coral reefs of Hervey Bay are located in Great Sandy Marine Park, south of the Great Barrier Reef Marine Park (Lat 25.00o S Long 152.85o E) (Fig. 1). The reefs of Hervey Bay are unique in many ways and their communities may be ecologically linked with both the Great Barrier Reef to the north and higher latitude reefs to the south (DeVantier 2010; Zann 2012) with tropical, subtropical and temperate species present (DeVantier 2010; Zann 2012). Many of the reefs of Hervey Bay are nearshore and although many occur adjacent to the coastline, they differ from fringing reefs in that they do not have a well-developed reef flat. They have been variously described as pre-reefal or incipient (DeVantier 2010; Zann 2012), but also show evidence of complex, three dimensional topography (Zann 2012). These reefs are subject to the lowered temperatures, reduced light and low aragonite of high-latitude waters (Kleypas et al. 1999; Harriott and Banks 2002). They are also subject to the transport of sediment, freshwater, nutrients and pollution from the Mary River (BPA 1989), just south of Hervey Bay as well as the Burnett River at the northern end of Hervey Bay. Both catchments have been extensively modified through land clearance, urbanisation, grazing and farming since colonisation ~1845 AD (Johnson 1996; Van Manen 1999; Campbell and McKenzie 2004; Prange and Duke 2004). Clearance of riparian vegetation from the Mary River catchment is still one of the highest along the Queensland coast (Reefplan 2010). While it is probable that the current coral communities of Hervey Bay have been affected by anthropogenic changes to the catchment, there are currently no estimates of historical natural variation with which to compare modern abundances. This study aims to provide such a dataset.

Chapter 1 Objectives

The aim of this thesis is to use innovative U-Th geochronology and palaeoecology to produce a chronologically precise historical baseline of the coral communities of the high-latitude coral reefs of Hervey Bay and then examine this record for both natural and anthropogenic drivers of change. In order to assist with understanding the historical drivers of community change, I will also examine how modern disturbances, primarily flooding, affect coral abundance and community assembly and then apply this knowledge to the understanding of past communities.

In Chapter 2 (Butler et al. 2013), I examine the impacts of moderate flooding in 2011 on the abundance of hard and soft corals on the coral reefs of Hervey Bay, Queensland, Australia after a decade of severe drought. I also examine the potential relationship between flood mortality and gradients of exposure to terrestrial and riverine stressors.

In Chapter 3 (Butler et al. 2015), I examine water conditions at three nearshore Hervey Bay reefs over the course of repeated flooding events in 2013 to better understand how flooding impacts these high latitude coral reefs. I examine salinity, sediment composition, turbidity and nutrient composition near to and more distant from shore to assess whether this is an important factor for the spatial distribution of mortality. I also assess the impacts of this repeated flooding on absolute abundance of hard and soft corals relative to 2010 and 2011.

In Chapter 4, I examine the coral communities of Hervey Bay over the course of repeated flooding from 2010 to 2013 to determine changes in taxonomic composition, functional trait composition and functional diversity. I also assess the significance of terrestrial and riverine exposure to coral community composition and trait composition.

In Chapter 5, through the use of percussion coring and U-Series (Thorium) dating, I examine the historical range of variation of the coral communities of four Hervey Bay reefs over the Holocene epoch. I generate an historical baseline of coral communities with which to compare the relative impacts of natural environmental stressors with those resulting from European colonisation and modification of adjacent catchments and lands.

Chapter 1 In Chapter 6, I provide concluding remarks on the findings of this thesis. The high-latitude reefs of Hervey Bay have provided substantial and, at times surprising, information about both modern and historical variations in coral abundance. I discuss how this applies to reef, catchment and land management and then suggest directions for future research.

Chapter 1 References

Adjeroud M, Michonneau F, Edmunds PJ, Chancerelle Y, Loma TL, Penin L, Thibaut L, Vidal- Dupiol J, Salvat B, Galzin R (2009) Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a South Central Pacific reef. Coral Reefs 28:775-780 Aronson RB (2011) Intrinsic And Extrinsic Drivers On Coral Reefs. In: Hopley D (ed) Encyclopedia of Modern Coral Reefs. Springer Netherlands, pp610-612 Ayling AM, Ayling AL (1998) The Effect of the Daintree River Flood Plume On Snapper Island Coral Reefs. Great Barrier Reef Marine Park Authority Beger M, Sommer B, Harrison PL, Smith SDA, Pandolfi JM (2014) Conserving potential coral reef refuges at high latitudes. Diversity and Distributions 20:245-257 Beger M, Babcock R, Booth DJ, Bucher D, Condie SA, Creese B, Cvitanovic C, Dalton SJ, Harrison P, Hoey A, Jordan A, Loder J, Malcolm H, Purcell SW, Roelfsma C, Sachs P, Smith SDA, Sommer B, Stuart-Smith R, Thomson D, Wallace CC, Zann M, Pandolfi JM (2011) Research challenges to improve the management and conservation of subtropical reefs to tackle climate change threats. Ecological Management & Restoration 12:e7-e10 BPA (1989) Hervey Bay beaches : a detailed study of coastline behaviour along the mainland beaches of Hervey Bay, South-east Queensland, Australia. Beach Protection Authority, Brisbane 323 Brodie J, Wolanski E, Lewis S, Bainbridge Z (2012a) An assessment of residence times of land- sourced contaminants in the Great Barrier Reef lagoon and the implications for management and reef recovery. Marine Pollution Bulletin 65:267-279 Brodie JE, Kroon FJ, Schaffelke B, Wolanski EC, Lewis SE, Devlin MJ, Bohnet IC, Bainbridge ZT, Waterhouse J, Davis AM (2012b) Terrestrial pollutant runoff to the Great Barrier Reef: An update of issues, priorities and management responses. Marine Pollution Bulletin 65:81- 100 Budd AF, Pandolfi JM (2010) Evolutionary novelty is concentrated at the edge of coral species distributions. Science 328:1558-1561 Butler IR, Sommer B, Zann M, Zhao Jx, Pandolfi JM (2013) The impacts of flooding on the high- latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia. Coral Reefs 32:1149-1163 Butler IR, Sommer B, Zann M, Zhao Jx, Pandolfi J (2015) The cumulative impacts of repeated heavy rainfall, flooding and altered water quality on the high-latitude coral reefs of Hervey Bay, Queensland, Australia. Mar Pollut Bull doi:10.1016/j.marpolbul.2015.04.047 Campbell S, McKenzie LYJ (2004) Flood related loss and recovery of intertidal seagrass meadows in southern Queensland, Australia. Estuarine, Coastal and Shelf Science 60:477-490 Carilli JE, Prouty NG, Hughen KA, Norris RD (2009) Century-scale records of land-based activities recorded in Mesoamerican coral cores. Marine Pollution Bulletin 58:1835-1842 Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, Lydon D, Edgar GJ, Edwards AJ, Fenner D, Guzmán HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Moore JA, Obura DO, Ochavillo D, Polidoro BA, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD, Sanciangco J, Sheppard A, Sheppard C, Smith J, Simon S, Turak E, Veron JEN, Wallace C, Weil E, Wood E (2008) One-Third of Reef-Building Corals Face Elevated Extinction Risk from Climate Change and Local Impacts. Science 321:560-563 Cervino JM, Hayes RL, Honovich M, Goreau TJ, Jones S, Rubec PJ (2003) Changes in zooxanthellae density, morphology, and mitotic index in hermatypic corals and anemones exposed to cyanide. Marine Pollution Bulletin 46:573-586 Chartrand K, Durako M, Blum J (2009) Effect of hyposalinity on the photophysiology of Siderastrea radians. Marine Biology 156:1691-1702

Chapter 1 Chen T, Yu K, Shi Q, Li S, Price G, Wang R, Zhao M, Chen T, Zhao J (2009) Twenty-five years of change in scleractinian coral communities of Daya Bay (northern South China Sea) and its response to the 2008 AD extreme cold climate event. Chinese Science Bulletin 54:2107- 2117 Cortes J (1990) Coral reef decline in Golfo Dulce, Costa Rica, eastern Pacific: Anthropogenic and natural disturbances. Ph.D. Ph.D. thesis, University of Miami, p161-161 p. Costa OS, Nimmo M, Attrill MJ (2008) Coastal nutrification in Brazil: A review of the role of nutrient excess on coral reef demise. Journal of South American Earth Sciences 25:257-270 Cramer KL (2011) Historical change in coral reef communities in Caribbean Panama. Ph.D. Ph.D. thesis, University of California, San Diego, p232 Cramer KL, Jackson JBC, Angioletti CV, Leonard-Pingel J, Guilderson TP (2012) Anthropogenic mortality on coral reefs in Caribbean Panama predates coral disease and bleaching. Ecology Letters 15:561-567 Dardeau M, Aronson RB, Precht WF, Macintyre IG (2000) Use of a hand-operated, open barrel corer to sample uncemented Holocene coral reefs. American Academy of Underwater Sciences De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27–year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences 109:17995-17999 DERM (2009) ClimateQ:toward a greener Queensland Appendix 3: Climate Change Wide Bay Burnett Region. Department of Environment and Resource Management, Brisbane DeVantier L (2010) Reef-building corals of Hervey Bay, South-East Queensland. Baseline Survey Report to the Wildlife Preservation Society of Queensland, Fraser Coast Branch, June 2010. Diaz-Pulido G, Harii S, McCook L, Hoegh-Guldberg O (2010) The impact of benthic algae on the settlement of a reef-building coral. Coral Reefs 29:203-208 Dikou A, van Woesik R (2006) Survival under chronic stress from sediment load: Spatial patterns of hard coral communities in the southern islands of Singapore. Marine Pollution Bulletin 52:1340-1354 Dowdy A, Abbs D, Bhend J, Chiew F, Church J, Ekstrom M, Kirono D, Lenton A, Lucas C, McInnes K, Moise A, Monselesan D, Mpelasoka F, Webb L, Whetton P (2015) East Coast Cluster Report, Climate Change in Australia Projections for Australia's Natural Resource Management Regions. In: Ekstrom M, Whetton P, Gerbing C, Grose M, Webb L, Risbey J (eds). CSIRO, Bureau of Meteorology, Australia Fabricius K, De'ath G (2001) Environmental factors associated with the spatial distribution of crustose coralline algae on the Great Barrier Reef. Coral Reefs 19:303-309 Fabricius K, De'ath G, McCook L, Turak E, Williams DM (2005) Changes in algal, coral and fish assemblages along water quality gradients on the inshore Great Barrier Reef. Marine Pollution Bulletin 51:384-398 Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: Review and synthesis. Marine Pollution Bulletin 50:125-146 Fabricius KE, Wolanski E (2000) Rapid Smothering of Coral Reef Organisms by Muddy Marine Snow. Estuarine, Coastal and Shelf Science 50:115-120 Fabricius KE, Wild C, Wolanski E, Abele D (2003) Effects of transparent exopolymer particles and muddy terrigenous sediments on the survival of hard coral recruits. Estuarine, Coastal and Shelf Science 57:613-621 Fukami T, Wardle DA (2005) Long-term ecological dynamics: reciprocal insights from natural and anthropogenic gradients. Proc Biol Sci 272:2105-2115 Gilmour J (1999) Experimental investigation into the effects of suspended sediment on fertilisation, larval survival and settlement in a scleractinian coral. Marine Biology 135:451-462 Golbuu Y, van Woesik R, Richmond RH, Harrison P, Fabricius KE (2011) River discharge reduces reef coral diversity in Palau. Marine Pollution Bulletin 62:824-831

Chapter 1 Graham N, Nash K, Kool J (2011) Coral reef recovery dynamics in a changing world. Coral Reefs 30:283-294 Greenstein BJ and Pandolfi JM (2008) Escaping the heat: Range shifts of reef coral taxa in coastal Western Australia. Global Change Biology 14(3): 513-528 Guillemot N, Chabanet P, Le Pape O (2010) Cyclone effects on coral reef habitats in New Caledonia (South Pacific). Coral Reefs 29:445-453 Guinotte J, Buddemeier R, Kleypas J (2003) Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22:551-558 Harrington L, Fabricius K, De'ath G, Negri A (2004) Recognition and Selection of Settlement Substrata Determine Post-Settlement Survival in Corals. Ecology 85:3428-3437 Harriott VH, Banks SB (2002) Latitudinal variation in coral communities in eastern Australia: a qualitative biophysical model of factors regulating coral reefs. Coral Reefs 21:83-94 Hoegh-Guldberg O (2011) The Impact of Climate Change on Coral Reef Ecosystems. In: Dubinsky Z, Stambler N (eds) Coral Reefs: An Ecosystem in Transition. Springer Netherlands, pp391- 403 Hongo C, Kayanne H (2010) Relationship between species diversity and reef growth in the Holocene at Ishigaki Island, Pacific Ocean. Sedimentary Geology 223:86-99 Hughes T (2008) Human Impacts on Coral Reefs. In: Hutchings P, Kingsford M, Hoegh-Guldberg O (eds) The Great Barrier Reef: biology, environment and management. CSIRO, Collingwood, Victoria, pp85-94 Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends in Ecology & Evolution 25:633-642 Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase Shifts, Herbivory, and the Resilience of Coral Reefs to Climate Change. Current Biology 17:360-365 Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh- Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929-933 IPCC (2007) Climate Change 2007: Synthesis report. IPCC, Cambridge, UK and New York, USA ISRS (2004) The effects of terrestrial runoff of sediments, nutrients and other pollutants on coral reefs. Briefing Paper 3. International Society for Reef Studies 18 Johns KA, Osborne KO, Logan M (2014) Contrasting rates of coral recovery and reassembly in coral communities on the Great Barrier Reef. Coral Reefs 33:553-563 Johnson DP (1996) State of the Rivers, Mary River and its tributaries: An Ecological and Physical Assessment of the Condition of Streams in the Mary River Catchment State of the Rivers. Department of Natural Resources, Indooroopilly Jokiel PL (2006) Impact of storm waves and storm floods on Hawaiian reefs. Proceedings of the 10th International Coral Reef Symposium 1:390-398 Jokiel PL, Hunter CL, Taguchi S, Watarai L (1993) Ecological impact of a fresh-water “reef kill” in Kaneohe Bay, Oahu, Hawaii. Coral Reefs 12:177-184 Jones AM, Berkelmans R (2014) Flood Impacts in Keppel Bay, Southern Great Barrier Reef in the Aftermath of Cyclonic Rainfall. PLoS ONE 9:e84739 Jones RJ (2007) Chemical contamination of a coral reef by the grounding of a cruise ship in Bermuda. Marine Pollution Bulletin 54:905-911 Karlson RH (1999) Dynamics of coral communities. Kluwer Academic Publishers, London Kawecki TJ (2008) Adaptation to Marginal Habitats. Annual Review of Ecology, Evolution, and Systematics 39:321-342 Kleypas J, Menez A, McManus J (1999) Environmental Limits to Coral Reef Development: Where Do We Draw the Line? American Zoologist 39:146-159 Ledlie M, Graham N, Bythell J, Wilson S, Jennings S, Polunin N, Hardcastle J (2007) Phase shifts and the role of herbivory in the resilience of coral reefs. Coral Reefs 26:641-653 11

Chapter 1 Lewis SE, Brodie JE, Bainbridge ZT, Rohde KW, Davis AM, Masters BL, Maughan M, Devlin MJ, Mueller JF, Schaffelke B (2009) Herbicides: A new threat to the Great Barrier Reef. Environmental Pollution 157:2470-2484 Lirman D, Manzello D (2009) Patterns of resistance and resilience of the stress-tolerant coral Siderastrea radians (Pallas) to sub-optimal salinity and sediment burial. Journal of Experimental Marine Biology and Ecology 369:72-77 Lybolt M, Neil D, Zhao J-x, Feng Y-x, Yu K-F, Pandolfi J (2011) Instability in a marginal coral reef: the shift from natural variability to a human-dominated seascape. Frontiers in Ecology and the Environment 9:154-160 Lynch HJ, Rhainds M, Calabrese JM, Cantrell S, Cosner C, Fagan WF (2013) How climate extremes—not means—define a species' geographic range boundary via a demographic tipping point. Ecological Monographs 84:131-149 McCauley DJ, Pinsky ML, Palumbi SR, Estes JA, Joyce FH, Warner RR (2015) Marine defaunation: Animal loss in the global ocean. Science 347 McCulloch M, Fallon S, Wyndham T, Hendy E, Lough J, Barnes D (2003) Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. Nature 421:727-730 Montaggioni LF, Braithwaite CJR (2009) Chapter One Introduction: Quaternary Reefs in Time and Space. In: Montaggioni LF, Braithwaite CJR (eds) Developments in Marine Geology. Elsevier, pp1-21 Morgan P, Aplet GH, Haufler JB, Humphries HC (1994) Historical Range of Variability. Journal of sustainable forestry 2:87-111 Nelson WA (2009) Calcified macroalgae - critical to coastal ecosystems and vulnerable to change: a review. Marine and Freshwater Research 60:787-801 Nugues MM, Roberts CM (2003) Coral mortality and interaction with algae in relation to sedimentation. Coral Reefs 22:507-516 Olds AD, Connolly RM, Pitt KA, Maxwell PS (2011) Habitat connectivity improves reserve performance. Conservation Letters 5:56-63 Packett R, Dougall C, Rohde K, Noble R (2009) Agricultural lands are hot-spots for annual runoff polluting the southern Great Barrier Reef lagoon. Marine Pollution Bulletin 58:976-986 Pandolfi J, Greenstein B (2007) Chapter 22. Using the past to understand the future: palaeoecology of coral reefs Pandolfi JM (2011a) Historical Ecology of Coral Reefs. In: Hopley D (ed) Encyclopedia of Modern Coral Reefs. Springer Netherlands, pp554-558 Pandolfi JM (2011b) The Paleoecology of Coral Reefs. In: Dubinsky Z, Stambler N (eds) Coral Reefs: An Ecosystem in Transition. Springer Netherlands, pp13-24 Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting Coral Reef Futures Under Global Warming and Ocean Acidification. Science (New York, NY) 333:418-422 Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955-958 Parmesan C, Gaines S, Gonzalez L, Kaufman DM, Kingsolver J, Peterson AT, Sagarin R (2005) Empirical Perspectives on Species Borders: From Traditional Biogeography to Global Change. Oikos 108:58-75 Pauly D (1995) Anecdotes and the shifting baseline syndrome of fisheries. Trends in Ecology & Evolution 10:430 Perry C (2011) Turbid-Zone and Terrigenous Sediment-Influenced Reefs. In: Hopley D (ed) Encyclopedia of Modern Coral Reefs. Springer Netherlands, pp1110-1120 Perry C, Smithers S (2006) Taphonomic signatures of turbid-zone reef development: examples from Paluma Shoals and Lugger Shoal, inshore central Great Barrier Reef, Australia. Palaeography, Paleaeoclimatology, Paleaeocology 242:1-20

Chapter 1 Perry CT, Smithers SG, Palmer SE, Larcombe P, Johnson KG (2008) 1200 year paleoecological record of coral community development from the terrigenous inner shelf of the Great barrier reef. Geology 36:691-694 Philipp E, Fabricius K (2003) Photophysiological stress in scleractinian corals in response to short- term sedimentation. Journal of Experimental Marine Biology and Ecology 287:57-78 Pimm SL, Raven P (2000) Biodiversity: Extinction by numbers. Nature 403:843-845 Pollock FJ, Lamb JB, Field SN, Heron SF, Schaffelke B, Shedrawi G, Bourne DG, Willis BL (2014) Sediment and Turbidity Associated with Offshore Dredging Increase Coral Disease Prevalence on Nearby Reefs. PLoS ONE 9:e102498 Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM, Halpern BS, Holding J, Kappel CV, O/'Connor MI, Pandolfi JM, Parmesan C, Schwing F, Thompson SA, Richardson AJ (2013) Global imprint of climate change on marine life. Nature Clim Change 3:919-925 Prange JA, Duke N (2004) Burnett Mary Regional Assessment: Marine and Estuarine Water Quality and Wetland Habitats of the Burnett Mary Region. Marine Botany Group, Centre for Marine Studies, The University of Queensland, Brisbane Quinn N, Kojis B (2006) Natural Resilience of Coral Reef Ecosystems Coral Reef Restoration Handbook. CRC Press, pp61-75 Rachello-Dolmen PG, Cleary DFR (2007) Relating coral species traits to environmental conditions in the Jakarta Bay/Pulau Seribu reef system, Indonesia. Estuarine, Coastal and Shelf Science 73:816-826 Reefplan (2010) Reef Water Quality Protection Plan - Second Report Card 2010, Burnett Mary Region In: Government A (ed) 2 Reichelt-Brushett AJ, Harrison PL (1999) The Effect of Copper, Zinc and Cadmium on Fertilization Success of Gametes from Scleractinian Reef Corals. Marine Pollution Bulletin 38:182-187 Risk MJ (2014) Assessing the effects of sediments and nutrients on coral reefs. Current Opinion in Environmental Sustainability 7:108-117 Risk MJ, Edinger E (2011) Impacts of Sediment on Coral Reefs. In: Hopley D (ed) Encyclopedia of Modern Coral Reefs. Springer Netherlands, pp575-586 Roche RC, Perry CT, Johnson KG, Sultana K, Smithers SG, Thompson AA (2011) Mid-Holocene coral community data as baselines for understanding contemporary reef ecological states. Palaeogeography, Palaeoclimatology, Palaeoecology 299:159-167 Rodriguez IB (2006) Relationships between reef fish communities, water and habitat quality on coral reefs. 1440655 Ph.D. thesis, University of Puerto Rico, Mayaguez (Puerto Rico), p61 Roff G, Clark T, Reymond-CE, Zhao Jx, Feng Y, McCook L, Done T, Pandolfi J (2013) Palaeoecological evidence of a historical collapse of corals at Pelorus Island, inshore Great Barrier Reef, following European settlement. Proceedings of the Royal Society B 280:20122100 Rogers CS, Garrison VH (2001) Ten years after the crime: Lasting effects of damage from a cruise ship anchor on a coral reef in St. John, U.S. Virgin Islands. Bulletin of Marine Science 69:793-803 Rull V (2010) Ecology and Palaeoecology: Two Approaches, One Objective. The Open Ecology Journal 3:1 - 5 Sanders D, Baron-Szabo RC (2005) Scleractinian assemblages under sediment input: their characteristics and relation to the nutrient input concept. Palaeogeography, Palaeoclimatology, Palaeoecology 216:139-181 Sexton JP, McIntyre PJ, Angert AL, Rice KJ (2009) Evolution and Ecology of Species Range Limits. Annual Review of Ecology, Evolution, and Systematics 40:415-436 Smith LD, Negri AP, Philipp E, Webster NS, Heyward AJ (2003) The effects of antifoulant-paint- contaminated sediments on coral recruits and branchlets. Marine Biology 143:651-657 Stork N (2010) Re-assessing current extinction rates. Biodivers Conserv 19:357-371

Chapter 1 Thomson D, Frisch A (2010) Extraordinarily high coral cover on a nearshore, high-latitude reef in south-west Australia. Coral Reefs 29:923-927 Thurlow R (2013) U.N. Gives Australia Time to Spare Barrier Reef Wall Street Journal (Online), New York, N.Y. Toth LT, Aronson RB, Vollmer SV, Hobbs JW, Urrego DH, Cheng H, Enochs IC, Combosch DJ, van Woesik R, Macintyre IG (2012) ENSO Drove 2500-Year Collapse of Eastern Pacific Coral Reefs. Science 337:81-84 Twiggs EJ, Collins LB (2010) Development and demise of a fringing coral reef during Holocene environmental change, eastern Ningaloo Reef, Western Australia. Marine Geology 275:20- 36 van Manen N (1999) State of the Rivers, Burnett River & Majore Tributaries - an ecological and physical assessment of the conditions of streams in the Burnett, Kolan, Burrum River catchments. The State of Queensland, Dept. Natural Resources & Mines, Brisbane. van Woesik R (2009) Corals' prolonged struggle against unfavorable conditions. Galaxea, Journal of Coral Reef Studies 11:53-58 van Woesik R, Done TJ (1997) Coral communities and reef growth in the southern Great Barrier Reef. Coral Reefs 16:103-115 van Woesik R, De Vantier L, Glazebrook J (1995) Effects of Cyclone 'Joy' on nearshore coral communities of the Great Barrier Reef. Marine Ecology Progress Series 128:261-270 Veron J (2008) A reef in time: the Great Barrier Reef from beginning to end. Belknap Press of Harvard University Press, Cambridge, Massachusetts Walker BK, Jordan LKB, Spieler RE (2009) Relationship of Reef Fish Assemblages and Topographic Complexity on Southeastern Florida Coral Reef Habitats. Journal of Coastal Research:39-48 Wilson SK, Graham NAJ, Polunin NVC (2007) Appraisal of visual assessments of habitat complexity and benthic composition on coral reefs. Marine Biology 151:1069-1076 WRI (2011) Reefs at risk revisited. In: Institute WR (ed). World Resources Institute, Washington DC Yamano H, Hori K, Yamauchi M, Yamagawa O, Ohmura A (2001) Highest-latitude coral reef at Iki Island, Japan. Coral Reefs 20:9-12 Yamano HK, Sugihara K, Nomura K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophysical Research Letters 38(4) Zann M (2012) The Use of Remote Sensing and Field Validation for Mapping Coral Communities of Hervey Bay and the Great Sandy Strait and Implications for Coastal Planning Policy. M Phil. thesis, University of Queensland, St Lucia, p216

Chapter 1 Figures

Fig. 1 Map showing locations of rivers and coral reefs of Hervey Bay, Queensland, Australia.

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163

Chapter 2: The impacts of flooding on the high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia

Published in journal Coral Reefs on 20 July 2013

Butler, I. R., B. Sommer, M. Zann, J-x Zhao and J. M. Pandolfi (2013). "The impacts of flooding on the high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia." Coral Reefs 32(4): 1149-1163.

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163

Abstract

Introduction

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163 Materials and methods

The study area

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163 Flood plume and ambient water quality data

Sampling methods

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163 Data analyses

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163 Results

Water quality in the flood plume

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163 Pre- and post-flood abundance of hard and soft corals

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163 Impacts on community structure

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163 Discussion

Flooding impacts on coral abundance

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163 Variability in flood impacts among reefs

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163 Changes in community structure

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163 Prospects for recovery

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163 Implications of flood impacts to Great Sandy Marine Park management

Climate change and catchment management

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163 Acknowledgments

References

Chapter 2: Butler et al. (2013) Coral Reefs 32(4):1149-1163

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047

Chapter 3: The cumulative impacts of repeated heavy rainfall, flooding and altered water quality on the high-latitude coral reefs of Hervey Bay, Queensland, Australia

Published in Marine Pollution Bulletin April 2015

Butler, I.R., B. Sommer, M. Zann, J-x Zhao and J. M. Pandolfi. (2015) The cumulative impacts of repeated heavy rainfall, flooding and altered water quality on the high-latitude coral reefs of Hervey Bay, Queensland, Australia. Mar. Pollut. Bull. http://dx.doi.org/10.1016/j.marpolbul.2015.04.047

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047 Abstract

Introduction

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047

Materials and methods

The study area Nearshore water quality monitoring

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047 Offshore versus nearshore comparison of water quality data Photo-transect methodology for measuring coral abundance

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047 Data analyses Results

Site variability in water quality Salinity in flood plumes Delayed episode of hyposalinity Turbidity and total suspended solids in the flood plume Total nutrients in the flood plume

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047 Nutrients versus TSS and salinity Change in total abundance of hard and soft corals after flooding Discussion

Flooding

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047 Importance of flood plume pathways and distance from the Mary River on flooding impacts

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047 Reduced impacts of subsequent floods

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047 Nearshore versus offshore water quality Submarine groundwater discharge

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047 Recovery Conclusion Acknowledgements

References

Chapter 3: Butler et al. (2015) Marine Pollution Bulletin doi:10.1016/j.marpolbul.2015.04.047

Chapter 4 Chapter 4: Terrestrial runoff, trait filtering and the assembly of resilient coral communities on the high-latitude coral reefs of Hervey Bay, Queensland, Australia

I. R. Butler B. Sommer J.-x. Zhao J. M. Pandolfi

I. R. Butler1 contact email: [email protected]

B. Sommer1

J-x Zhao Radiogenic Isotope Laboratory, School of Earth Sciences, The University of Queensland, Brisbane, Queensland 4072 Australia

J. M. Pandolfi1

1 Australian Research Council Centre of Excellence for Coral Reef Studies and, School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia

Keywords: turbid, flood, functional traits, diversity, sedimentation, reproduction, recruitment

Chapter 4 Abstract

Marine communities around the world are subject to frequent disturbance as a result of increasing anthropogenic modifications to the environment but little is known about the assembly of communities under chronic disturbance. This study examines the impacts of repeated flooding over three years on the taxonomic and functional composition of high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia. In 2011and 2013, after a decade of severe drought, record flooding took place from the highly modified Mary River catchment near Hervey Bay. Although functional diversity indices, species richness/diversity and most functional traits were not significantly altered, there were significant changes in taxonomic composition as a result of the 2011 floods, far greater than the impacts of 2013, despite the greater magnitude of the latter flood. The impacts of these floods produced some expected results, for example the relative increase in abundance in the coral community of species known to be tolerant of hyposalinity and sedimentation (e.g. Turbinaria). Other predicted changes did not eventuate, such as increases in the relative abundance of species with strong sediment removal capabilities or species with large polyps. This indicates the likely importance of other flood associated stressors, for example hyposalinity, to flood related mortality, especially at the reefs near to either mainland or rivers. Overall, though, spatial distribution in the abundance of many of the measured traits in corals in Hervey Bay was not random, but correlated well with both distance from the mainland and distance from rivers, indicating the importance of terrestrial and riverine stressors to reef coral community composition.

Chapter 4 Introduction

Disturbance and stress affect biological communities and habitats worldwide and these have been increasing in recent decades (Parmesan and Yohe 2003; Poloczanska et al. 2013; Steinberg 2012). Understanding the impacts of chronic and acute disturbance and stress on biological communities is critical for minimising anthropogenic disturbances and the resulting adverse changes to these communities. While the usual metrics for community analyses (e.g. taxonomic composition, species richness, relative abundance) can provide a taxonomic viewpoint, communities can be affected in ways that are not evident from a taxonomic perspective (Mouillot et al. 2013). Functional analyses may help discern changes in ecosystems in response to disturbance that are independent of taxonomic structure (McGill et al. 2006; Mouillot et al. 2013), such as: the detection of different kinds of disturbances, which may not otherwise be obvious or are unexpected; the discrimination of different sources of impacts, and; the advanced detection of impacts (Mouillot et al. 2013).

Abiotic stress can lead to environmental filtering, where only species with certain characteristics can establish and persist in chronically stressful or marginal environments (Fischer 1961; Weiher and Keddy 1995; Leibold and McPeek 2006; Cavender-Bares and Reich 2012; Sommer et al. 2014). However, little is known about how acute disturbance events affect biological assemblages that already persist under chronically stressful environmental conditions. Species with different functional characteristics may be unevenly affected by disturbance (Loya et al. 2001; Mouillot et al. 2013). Disturbance shapes community assembly for many ecosystems (Dornelas 2010). Even small differences in an organism’s ability to survive or recover from a disturbance will enhance the proportional presence of that organism in any post-disturbance community and this trait mediated assembly has been shown for organisms subject to wind disturbance (Nagel et al. 2013), logging (Ding et al. 2012), grazing (Pakeman et al. 2011), drought, nutrient enrichment (Arthaud et al. 2012) and low water flow (Walters 2011). Intense or repeated disturbance can cause co-occurring species to become more similar in their functional characteristics (Mouillot et al. 2013; Sommer et al. 2014).

Nowhere are stress and disturbance more chronically prevalent than at the edges of species ranges. Abiotic filtering constrains overall distribution of function observed within assemblages, with the greatest filtering occurring in the least favourable sections of a gradient (Weiher et al. 1998). For instance, the distributions of organisms in more temperate areas are constrained, relative to more tropical areas, as a result of abiotic filtering (Swenson 2012). A good example of organisms at the 47

Chapter 4 edge of their range is sub-tropical corals which are found in the biogeographic transition zones in subtropical eastern Australia. High latitude reefs exist at the edges of their environmental tolerance for temperature, light and aragonite saturation (Kleypas et al. 1999). As a result of limited warm water currents, they also tend to have limited larval transport pathways (Beger et al. 2014) so recruitment and subsequent recovery from disturbance can be very slow. As a result of climate change, subtropical reefs are predicted to undergo greater changes than tropical reefs, resulting in community re-assembly through range shifts, altered dispersal patterns, decreased survivorship and habitat loss (Beger et al. 2014). It is, however, also possible that coral ranges may expand into higher latitudes and become less marginalised (Freeman 2015), as occurred in the Pleistocene from Western Australia (Greenstein and Pandolfi 2008) and more recently in Japan (Yamano et al. 2011), though the latitudinal room for expansion may be limited, for example, by light penetration at higher latitudes (Muir et al. 2015) or as a result of anthropogenic modification (Lybolt et al. 2011).

The coral reefs of Hervey Bay, Queensland, Australia provide an ideal study system to investigate the impacts of repeated acute disturbance events superimposed onto already chronically stressful or marginal conditions, and highlight the effects that acute disturbance events may have on biological communities in environments that are becoming increasingly marginal through climate change. At latitude 25o south, the coral reefs of Hervey Bay are near the southern margin of scleractinian coral reef formation along the eastern Australian coastline (Zann 2012). These reefs are subject to terrestrial runoff and sedimentation from both the nearby mainland and from distant inland areas via the Mary River, which has been highly modified since European colonisation (Johnson 1996; Kroon et al. 2012). Flooding is a common occurrence in the Mary River with “minor” (i.e. height = 5 m at Maryborough, Queensland) or larger floods occurring on average every three to four years, but with occasional decade long gaps between floods (BOM 2014). Flooding can result in multiple stressors, especially on nearshore reefs, including: hypo-salinity, sedimentation, high turbidity and nutrient enrichment (Jokiel et al. 1993; Ayling and Ayling 1998; Wooldridge et al. 2006; Wallace et al. 2009; Devlin et al. 2012; Butler et al. 2013; Jones and Berkelmans 2014; Butler et al. 2015). As a result of this exposure, reef communities of Hervey Bay are composed of a high proportion of coral genera such as Turbinaria, Goniopora and Favia which are relatively tolerant of these stressors (DeVantier 2010; Zann 2012; Butler et al. 2013).

In December 2010 to January 2011, and January to February 2013, after a decade of drought conditions (Gräwe et al. 2010) and 18 years since the last “Major” flood (BOM 2014), the east

Chapter 4 coast of Queensland, Australia experienced intense storms and rainfall which caused severe flooding in the Mary River. Hard and soft coral abundance declined by 40% after the 2011 floods (Butler et al. 2013) and by a total of ~56% after the repeated flooding in 2013 (Butler et al. 2015). Here we assess the impacts of repeated flooding on the coral communities of the high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay. We compare changes in taxonomic composition, functional diversity and trait distribution after individual floods versus those after years of repeated flooding. We also examine changes in taxonomic and functional composition over spatial gradients, including distance from river mouths and distance from the mainland to determine the spatial distribution of environmental filtering in the assembly of the reef coral communities. Finally, we examine life history strategies of the coral species comprising these communities as they relate to flooding, distance from the mainland and distance from the nearest river. Overall, we determine the significance of flooding and terrestrial exposure to the filtering and assembly of coral reef communities of the high latitude coral reefs of Hervey Bay, providing insights into the likely future of these reefs under climate change.

Materials and methods

The study area

Hervey Bay (25.00o S, 152.85o E) is situated at the northern end of the Great Sandy Straits on the southern coast of Queensland, Australia (Fig. 1). Six coral reef sites were examined for this study (Fig. 1): Four Mile Reef, Burkitt’s Reef, Pt. Vernon West, Pt. Vernon East, Pialba and Big Woody. Four Mile Reef occurs at 6-10 m water depth (based on highest astronomical tide (HAT)) and all the other reefs of this study occur in less than 5 m water depth (HAT). All of these reefs are located up to 70 km from either the Burnett or Mary rivers and up to 5 km from the mainland (Fig. 1). All reefs are protected from prevailing oceanic swell by the presence of Fraser Island, although Burkitt’s and 4 Mile reefs are more exposed to wave action due to a longer fetch (70 km) (Fig. 1). Further details of Hervey Bay, the reef sites and the Mary River are described in Butler et al. (2013).

Sampling methods for measuring taxonomic composition of coral communities

We measured total abundance of hard and soft coral using the same photo-transect and software analysis methodologies used in Butler et al. (2013). Each benthic image had 15 points randomly 49

Chapter 4 overlaid and the taxon for each point was identified to estimate percentage benthic cover of hard and soft corals. Hard and soft corals were the dominant taxa in the community and were the only taxa analysed. Due to difficulties with identification to species level on photographs in turbid conditions, Goniopora species were grouped to genus and bushy branching soft corals (e.g. Cladiella, Sinularia) were grouped into Cladiella. The category “Soft Coral” was composed of Xenia and Nephtheid soft corals.

Functional traits categories

To examine the impact of flooding on functional diversity patterns of corals in Hervey Bay, we characterised coral taxa based on functional traits. We were particularly interested in traits which we considered relevant to a coral’s resistance to a flooding event, such as sediment removal, low light tolerance, post-flood recovery and recruitment. Using these criteria, and through extensive search of the literature, we then generated a list of functional traits for Hervey Bay hard coral species (Table 1). The abundance of each trait category was the sum of the abundance (% cover) for all species exhibiting this trait. Soft corals were only compared with hard corals in terms of abundance as there was insufficient functional trait data available. Tolerance to hyposalinity was also of interest, however data were particularly lacking for this stressor for local species. The final list of traits included: colony morphology (Sommer et al. 2014), corallite arrangement (Sommer et al. 2014), corallite size (Veron 2000), reproductive mode (Baird et al. 2009), sex (hermaphroditic/gonochoric) (Baird et al. 2009), propagule development rate (Keith et al. 2013), mode of symbiont transmission across generations (Baird et al. 2009), range of depth (Carpenter et al. 2008) and sediment removal ability (Stafford-Smith and Ormond 1992) (Table 1, Supplementary Table 1). Colony morphology, corallite arrangement, corallite size and sediment removal ability are traits that are relevant to withstanding sediment deposition during and after flooding, as well as subsequent resuspension of sediment. Reproductive mode, sexuality, larval development rate and symbiont transmission are traits relevant to post disturbance recruitment. Range of depth is relevant to flexibility with light variability. All traits were weighted equally in the analyses. Where particular trait data were lacking for a species, data from a similar morphological species from the same genus was used. Where identification was limited to genus, this taxon was removed from analysis if other taxa of the same genus were variable for that particular trait. For example, the taxon Turbinaria sp. was removed from the analyses for spatial differences in colony morphology because Turbinaria has both encrusting and foliose morphologies and these could not be distinguished reliably from photos.

Chapter 4 To evaluate life-history strategies of corals in these marginal reef environments, we classified the coral species recorded in our study as competitive, weedy and stress-tolerant, adapted from a recently proposed coral-life-history framework for scleractinian corals (Darling et al. 2012). In this framework, which is based on a suite of traits, Stress Tolerant species are generally those species that are slow growing, long-lived, and with domed, encrusting to massive morphology. Competitive species are generally those that grow quickly with branching/plate morphology. Weedy species are generally those that are small and brood larvae.

Calculation of functional diversity indices

To characterise patterns in the functional diversity of Hervey Bay coral assemblages and to determine the impacts of multiple flooding events on functional community structure, we calculated three complementary functional diversity indices that characterise different aspects of functional community structure and take the abundances of species into account. These indices were then examined by PERMANOVA as described in the next section.

We calculated functional diversity indices from Gower distances (Gower 1966) of species in functional space, as Gower distance allows the combination of qualitative and quantitative traits. In order to quantify the overall dispersion of functional traits for each local assemblage we calculated the mean pair-wise functional trait distance (MPD) (Webb 2000; Webb et al. 2002; Bello et al. 2013). To test whether local assemblages were more or less functionally diverse than randomly expected, we subsequently compared the observed levels of functional diversity (MPD) to a null model using standardised effect sizes. We calculated standardised effect sizes (SES) using distributions of 1000 random values of mean trait distances between species, obtained by shuffling the species names across all species included in the Gower distance matrix. Positive SES values indicate greater functional distance among species co-occurring in a local assemblage than randomly expected, and negative SES values indicate greater functional similarity of co-occurring species (Webb 2000; Webb et al. 2002; Swenson 2014). We then calculated functional evenness (FEve) and functional divergence (FDiv) to characterise how the niche spaces were filled. FEve quantifies how regularly mean species traits are distributed in the occupied trait space, with high FEve values indicating even distribution. FDiv, a measure of the variance of species traits, quantifies the proportion of total abundance that is comprised by the species with functional traits that differ the most from the local assemblage. High FDiv values indicate that the abundant species possess extreme trait values (Villéger et al. 2008; Mouillot et al. 2013).

Chapter 4

Permutational analyses of variance of the impacts of flooding on coral communities

Multivariate permutational analysis of variance (PERMANOVA) models were created to examine changes in per-transect taxonomic composition (including species richness and Shannon-Weiner diversity), traits composition, traits diversity indices and life history composition of coral communities between 2010 (pre-flood), 2011 (post-flood) and 2013 (after repeated flooding). The models included distance of the reef from the mouth of the closest river and distance from the highest astronomical tide level (from satellite imagery) on the mainland as continuous predictors (covariates), and flood as a categorical fixed factor with two levels (pre- and post-flood). Type I sum of squares were calculated to ensure that any overall effect of time was independent of the effects of the covariates. To determine changes in community structure and traits composition between years, full models with interactions were generated using PERMANOVA on either multivariate Bray-Curtis matrices (taxonomic and traits data) or Euclidean matrices (Functional indices and species richness/diversity), using the mainland and river mouth distances as covariates. Non-significant factors were sequentially removed from the more complicated models to create the simplest model. Because of the multiple hypotheses being tested on these data (26 tests for taxonomic and traits changes), a Bonferroni correction (Dunn 1961) was applied to reduce the probability of making a Type 1 error. A significance level of P ≤ 0.002 was used for removing non- significant factors.

Non-metric multidimensional scaling (NMDS) plots were prepared to visually display the relative similarity of the reefs in terms of coral taxonomic community structure before and after flooding. To simplify the graphical display, relative abundance per transect for each year has been averaged per reef. SIMPER analyses were undertaken to investigate the contribution by particular species to differences found in community structure from 2010 to 2013.

Community analyses of the assemblages before and after the years of flooding were carried out as per previous work (Butler et al. 2013), except that the 2010 versus 2011 analyses were repeated with distance from the river calculated based on distance from the nearest river, as opposed to distance from only the Mary River. Recent information indicates that the most northern of the reef sites, Burkitt’s Reef, may have been more directly impacted by the Burnett River, north of the reef, than by the Mary River to the south (Fig. 1).

Chapter 4 Canonical analyses of the spatial distribution of coral species and traits

Relative abundance of hard and soft coral species and hard coral traits in the community were examined relative to distance from mainland and distance from nearest river in order to assess their contribution to the spatial distribution. To simplify the viewing of this graphical representation, transect data for taxa/traits were averaged per reef per year. Canonical analysis of principle coordinates (CAP) was carried out on the multivariate hard and soft coral abundance data using distance to mainland and distance to nearest river as environmental variables to investigate how coral species abundance varied according to these variables. Pearson correlations were then used to generate vectors representing how these abundances in genera/traits varied with these distance metrics.

We calculated functional trait diversity indices using the packages FD (Laliberte and Legendre 2010) and picante (Kembel et al. 2010) in R (R_Core_Team 2012). Multivariate statistical analyses were conducted using the software PRIMER v6 (Clarke 1993) and the add-on package PERMANOVA (Anderson et al. 2008).

Predicted outcomes from flooding disturbance

Certain outcomes are predicted to occur as a result of the flooding disturbance. Coral community structure is expected to change over the course of flooding, where those species more resistant to flooding will be in higher abundance post-flood compared with others. Turbinaria mesenterina, for example, is considered to be very stress tolerant, being resistant to hyposalinity and sedimentation (hyposalinity (Brown 2012, Faxneld et al. 2010, Sofonia et al. 2008). Those corals classified as Stress Tolerant (Darling et al. 2012), for example Goniopora, are expected to increase in relative abundance post-flood relative to Weedy or Competitive species. Species and trait diversity and richness are also expected to decrease post-flood as a result of high mortality in those species less resistant to flooding. Certain traits are expected to prevail over the course of flooding. Corals with large polyps and others considered to have strong sediment removal capabilities (Stafford-Smith 1992) are expected to increase in relative abundance post-flood. Corals with dome shaped morphology are generally associated with stressful conditions (Darling et al. 2012) in comparison with branching forms (Jackson and Hughes 1985) and these are expected to increase post-flood. Given the high turbidity that was experienced in the flooding (Butler et al. 2015), corals which

Chapter 4 tolerate wide depth ranges and wide ranges of light conditions are also expected to increase in relative abundance post-flood.

Results

Impacts on community structure

A total of 42 hard and soft coral taxa (genus or species level) were recorded during the overall 2010 – 2013 study period (Table 2) out of the known 101 taxa that have been previously recorded for the Burnett-Mary region (Coppo et al. 2014). The most common genera/taxa encountered in this study were Cladiella, Goniopora, Turbinaria, Pocillopora, Acropora and Montipora. The coral communities among the years at each reef were similar but, with the exception of Pialba and Pt. Vernon Reefs which are quite similar, each of the reef’s communities is distinct from the others (Fig. 2). The distances between 2010, 2011 and 2013 on the plot suggest no obvious differences in the magnitude of the impacts on community structure between the 2011 and 2013 floods, but rather a gradual alteration. Burkitt’s Reef shows the greatest directional change (Fig. 2).

Total hard and soft coral community structure was altered as a result of repeated flooding, but the primary impacts occurred as a result of the first flood in 2011 (Table 3). Distance from either mainland (Yr X D_Mn) or river (Yr X D_Rv) did not contribute significantly to the flooding impacts, though they played a major role in the underlying spatial distribution of traits. Genus level data were used for the multivariate PERMANOVA model since it yielded the same simplified model as the species level data (Table 3). All of the models for taxonomic composition showed significant underlying differences in community structure between reefs as a result of distance gradients and this is shown by the significant factors for distance from mainland, distance from river and their interaction term (D_Rv x D_Mn). There were also significant differences as a result of flooding (Yr factor), but only for the test for the initial flood (2010 vs. 2011) and repeated flooding (2010 vs. 2013) (Table 3). There were no significant differences in community structure from 2011 to 2013 as a result of repeated flooding and the factor “Yr” was removed from that model (Table 3). There were no significant differences in species richness or diversity attributable to flooding and neither species richness nor diversity varied with distance from mainland or river.

There was a disproportionate decrease in the overall relative abundances of Cladiella and Goniopora from 2010 to 2013, which accounted for ~53% of the change in hard and soft coral 54

Chapter 4 community (Table 4)(Fig. 3a). Though changes in the relative abundance of this genus varied from reef to reef (Figs. 4a-f), decreases in relative abundance of Cladiella were particularly evident overall (Fig. 4g). While absolute abundance of Turbinaria decreased overall (Table 4), relative abundance increased after the 2011 flooding (Figs. 3b, 4g). Distance from either mainland and river played a major role in the underlying spatial distribution of genera. Cladiella, Goniopora and Turbinaria increase in abundance at reefs closer to the mainland and closer to rivers while Acropora, Pocillopora and Montipora are more abundant on the reefs more distant from the mainland and from the rivers (Figs. 3c, d, 5a).

Functional diversity

Functional Divergence (FDiv), Functional Evenness (FEve), Mean Pairwise Distance (MPD) and MPD (null) indices were not significantly altered as a result of flooding impacts. They also did not vary according to distance from mainland or river.

Effect of flooding on individual functional traits

The community composition of traits for depth range, hard/soft categories and propagule development rates varied significantly as a result of flooding, but the impacts did not vary according to distance from mainland (Yr X D_Mn) or river (Yr X D-Rv), so these interactions were removed. Corals with propagule development rate 3 increased after flooding, while development rate 4 decreased. Corals with a 20 m depth range increased post flood, while the corals with a 30 m range decreased. Hard corals increased in abundance relative to soft corals post flood (Fig. 6a, b, c).

Relative abundance of life history categories in the coral communities did not change significantly as a result of flooding. The underlying spatial factors, distance from mainland (D_Mn) and distance from nearest river (D_Rv) were significant to most traits and life history categories (Table 5).

Spatial distribution of traits relative to distance from mainland and distance from nearest river

Many of the traits found in Hervey Bay were correlated with distance from mainland and distance from nearest river (Fig. 5b). To simplify the figures, only vectors for the most common genera and those traits with a Pearson correlation of 0.4 or greater were plotted (Fig. 5a, b). Increased abundance of species with poor (5) or passive sediment removal only (6) were correlated with reefs 55

Chapter 4 further from the mainland and further from rivers, as were; branching and encrusting-massive morphologies; brooders; plocoid and cerioid corallites; hermaphroditism; depth ranges 10 m, 20 m and 40 m; very small polyps; vertical symbiont transmission, and; propagule development rates 1(brooders), 3 and 5. Soft corals, gonochorism, and sediment clearance group 2 were more correlated with those inshore reefs, closer to the mainland and generally closer to rivers (Fig. 3e).

All three life history categories (as per Darling et al. 2012) were included on the graph (Fig. 5b). Increased abundance of species categorised as having a stress tolerant life history was found to occur nearer the mainland and nearer to rivers, while competitive and weedy life histories were correlated with increasing distance from the mainland and increasing distance from rivers (Fig. 5b).

Discussion

Disturbance often plays a central role in the ecology of communities (Steinberg-CR 2012) from high mountains (Milbau et al. 2013) to the deep sea (Radziejewska 2002). It can result in the disruption of community succession, recovery and competition and, if chronic, can exert selective pressure on community composition (Karlson 1999; Ding et al. 2012; Tanentzap et al. 2013). Taxonomic and functional analyses of communities can provide complimentary methods of examining the impacts of disturbance on community structure. Taxonomic analyses provide measures of change in biodiversity, while functional analyses enable a directed understanding of the capabilities of community members to persist through disturbance. In this study, the combination of the two provides insights into the recent changes in taxonomic composition and relative abundance of individual functional traits as a result of flooding, but also highlights the spatial distribution of traits relative to the mainland and to rivers.

Impacts of repeated flooding on Hervey Bay coral communities

There are numerous studies worldwide showing how repeated disturbance on coral communities can result in changes in coral communities (Harii et al. 2014; Pratchett et al. 2011; Thompson et al. 2014). Like these other studies, significant changes took place in the coral communities of Hervey Bay over the course of repeated flooding from 2010 to 2013, both as a result of the high mortality in 2011 and the short recovery period between the 2011 and 2013 floods. The floods of 2011 and 2013 exceeded by several weeks (Butler et al. 2015) the tolerances of many corals to hypo-salinity (Berkelmans et al. 2012, Jones and Berkelmans, 2014), including those nearshore reef corals 56

Chapter 4 regularly exposed to hyposalinity, which might be expected to show adaptation and reduced mortality (True and Piromvaragorn, 2012). Exposure to the combination of sedimentation and high nutrient levels was also of much longer duration than is needed to induce bacterially mediated mortality, which can occur in a matter of days (Fabricius et al. 2003). Overall there was a ~56% decrease in absolute abundance of coral (Butler et al. 2015). Coral community composition also changed as a result of the repeated flooding. Decreases in abundance were most evident for the hard coral Goniopora and the branching soft corals (esp. Cladiella), while the coral Turbinaria, which is known for tolerance to sedimentation and hyposalinity (Brown 2012, Faxneld et al. 2010, Sofonia et al. 2008), showed relatively reduced mortality. Despite the combination of a severe storm, multiple floods and higher flood levels in 2013, the greater part of the overall impacts to the coral communities of Hervey Bay had already occurred in the relatively smaller magnitude, but longer duration flood of 2011 (Butler et al. 2013), which occurred after the decade long Millennium Drought (Cai et al. 2014). Increases in terrestrial runoff after an extended period of reduced rainfall are known to temporarily result in increased mortality of corals as a result of disease (Thompson et al. 2014) and this would have likely contributed further to the mortality seen in 2011. Also, disturbance free periods are vital to reefs for recruitment and these recovery periods must be of sufficient duration to allow substantial recovery, otherwise the ability of the community to thrive is compromised (Johns et al. 2014). The 1.5 year gap between floods, from mid-2011 until early 2013, was too short for any recruitment or growth to result in significant recovery. Should future disturbance occur with similar frequency, then coral community structure on Hervey Bay reefs could be further altered, potentially with coral abundance diminishing over time.

Changes in the relative composition of coral traits as a result of repeated flooding

There were far fewer flooding impacts on traits and life history categories than was expected, given the significant changes that were seen in species composition. No significant changes were detected over the course of repeated flooding in functional divergence, functional evenness or functional diversity indices, indicating the relative overall spread of functional traits through the community remained unchanged as a result of flooding. Most of the traits did not vary either, which was surprising in particular for traits such as strong sediment clearance ability, large polyp size or the stress tolerant life history which were expected to confer improved resistance through flooding. The difference in hard/soft trait categories supports the changes seen the coral communities where Cladiella, the most dominant of soft corals, showed high mortality and the greatest contribution to the changes seen in the coral communities from 2010 to 2013. The conferred flood resistance of mid-range depth range or propagule development rates are not clear. 57

Chapter 4

It appears that the impacts of flooding affected the corals in ways which surpassed the resistance or in ways different from the benefits conferred by the traits. Although localised impacts were not targeted for this research, patchy mortality of up to 100% was observed at various reefs around Hervey Bay after the 2011 floods and within a week of the onset of 2013 floods, indicating that water conditions were highly lethal in some places, most likely due to the combination of hyposalinity and elevated nutrients. Resistance to hyposalinity and elevated nutrients would likely improve the chances of persistence through these floods, but were not assessed due to a lack of information in the literature about these traits for the species found in Hervey Bay.

Spatial distribution of traits

Overall, there was a clear spatial distribution of traits and life histories according to proximity to the mainland and to rivers. In the marine environment, proximity to land and proximity to rivers and the resulting exposure to terrestrial runoff and flooding can be a major influence on community composition. Along the Great Barrier Reef, coral communities vary over large scales from mainland to offshore reefs as a result of terrestrial exposure and water quality (Done 1982; De'ath and Fabricius 2010). Likewise, the presence of large volumes of freshwater is detrimental to coral reefs and where there are locations of large fluvial output, there are fewer coral reefs (Furnas 2003; Hopley et al. 2007). The general trend for communities and traits on Hervey Bay coral reefs to vary with distance from shore and river is indicative of the importance of terrigenous and riverine stressors to the assembly of these communities. Water quality in the near shore waters has been shown to be highly modified by terrestrial runoff and/or flooding relative to the more offshore waters (Butler et al. 2015) so coral species which persist in these nearshore environments need to be less sensitive to hyposalinity, higher turbidity and high nutrient levels than those occupying offshore habitats. The high relative abundance of coral species showing a stress tolerant life history on reefs closer to the mainland, relative to those weedy and competitive life histories further from the mainland and rivers, further supports this.

Individual trait distributions in Hervey Bay: Resistance to sedimentation

Sedimentation can adversely impact corals in a number of ways: from direct smothering/burial and abrasion or indirectly through increased turbidity and associated reduction in light penetration and photosynthetic yield (Fabricius 2005; Erftemeijer et al. 2012). Combined with nutrients,

Chapter 4 sedimentation can cause rapid mortality (Fabricius et al. 2003; Pollock et al. 2014). The effort to remove sediment places large energetic demands on corals, competing with other energetic demands, such as reproduction (Philipp and Fabricius 2003) and immune response (Sheridan et al. 2014). The ability to persist through periods of high sedimentation would be essential for corals living in Hervey Bay. Accordingly, the relative abundance of many traits, such as, sediment clearance ability, polyp size, colony morphology and depth range, varies with distance from the mainland and rivers. Close proximity to either precludes the presence of weak (e.g. Group 5) or passive (Group 6) sediment clearance ability, as occurs in species with a branching morphology (Stafford-Smith and Ormond 1992; Stafford-Smith 1993) or those intolerant of stress (Fellegara 2008). In contrast, strong sediment clearance ability (e.g. Group 2) was strongly correlated with those reefs nearer to the rivers and the mainland. Species with very small polyps are also missing from these reefs near to the rivers and mainland and this may be a result of both poor sediment removal ability (Stafford-Smith and Ormond 1992; Stafford-Smith 1993) and poor disease resistance (Díaz and Madin 2011) relative to those with larger polyps. Finally, relatively narrow depth ranges (10 – 20 m) are also correlated with reefs more distant from mainland/rivers, which may indicate the benefits of wide light and temperature tolerances in the variable inshore waters.

Reproduction

Reproductive strategies and subsequent recruitment can play a major role in the persistence of communities of organisms (Pianka 1970; Fogarty et al. 1992; Bonser and Ladd 2011). In communities where sexual gametes and/or offspring are released for dispersion and settlement, timing of reproduction may be paramount to the success of recruitment. There is strong evidence for the benefits of hermaphroditism to reproductive success in communities of sessile organisms, where direct contact between conspecifics is limited (Eppley and Jesson 2008; Preece and Mao 2009). However, while worldwide over 70% of scleractinian corals are hermaphrodites, and dominate the assemblages of most tropical reefs (Harrison 2011), hermaphroditic corals are relatively uncommon on the near-mainland reefs of Hervey Bay. Around 90% of the corals, by relative abundance, in the four reefs nearest the shore are gonochoric and it is only on the reefs more distant from the mainland where hermaphroditic corals become common, making up 100% on the most offshore reef, Four Mile Reef. There is much speculation as to the reasons behind the proportions of gonochorism versus hermaphroditism in communities (Meagher 2007; Eppley and Jesson 2008). While the use of separate sexes as a part of sexual reproduction has been historically considered a strategy for promoting outbreeding, this gender specialization is more recently thought of as a way of enhancing reproductive success of the individual sexes (Meagher 2007). There is evidence that 59

Chapter 4 for plants in drought conditions, separate sexes are beneficial for persisting through stressful conditions (Case and Barrett 2004). The high mortality in recent flooding highlights that conditions can be very stressful in Hervey Bay, particularly in the nearshore reefs (Butler et al. 2013; 2015), so gonochorism may confer some unknown benefits to coral flood resistance. It is also possible that because the communities of Hervey Bay are isolated from other coral reef areas in Queensland that outbreeding from gonochorism promotes genetic traits that enable persistence. Further support for the prevalence of gonochorism is shown through the dominance of gonochoristic soft corals on many reefs of the region (Coppo et al. 2014).

Larval dispersal and recruitment

High latitude reefs are considered to have low recruitment (Hughes et al. 2002; Nozawa et al. 2006) and the apparent shift towards increasing levels of brooding as a mechanism of larval development (Harriott and Banks 2002) indicate that the most common, tropical method of reproduction (hermaphroditic broadcast spawning) is perhaps not the optimal method in more marginal areas. In the Caribbean, where major disturbances have occurred over the centuries, brooding is now the dominant form of larval dispersal on many reefs (Baird et al. 2009). While the exact spawning time is not known for Hervey Bay, it is likely that spawning takes place between November and January, much like those in the more southern Moreton Bay (Fellegara et al. 2013). Brooding would be expected to be common in Hervey Bay, both as a result of its location at higher latitude and because of this time of year of spawning, when heavy rainfall and flooding are common (BOM 2014) and larval transport and settlement are likely to be difficult. Brooding allows for extended release of offspring, enabling a wider window of release, which increases the likelihood of successful settlement. Brooding, however, is not commonplace throughout Hervey Bay, although it is prevalent at Four Mile Reef, the reef in this study most distant from the mainland and from rivers and presumed to have optimal conditions. This suggests the potential relative importance of broadcast spawning where there are significant terrestrial or riverine stressors, despite the perceived benefits of brooding on high-latitude reefs along the east coast of Australia (Harriott and Banks 2002). It is possible, for example, that species which broadcast spawn represent an important source of recruits after high mortality events such as flooding.

Like brooding, the trait for use of large eggs (Propagule development rate 5), which are associated with slower larval development and long distance transport (Keith et al. 2013), was found to be more abundant on reefs distant from the mainland and rivers. Long distance transport of larvae from

Chapter 4 the GBR may be very limited given that the East Australian Current, the primary means of larval transport southward from the GBR, has limited connection to Hervey Bay (Gräwe et al. 2010). A local source from within Hervey Bay or from inshore reefs to the north may be an important source for recruits. Long distance transport of larvae may be important in other ways to these offshore reefs or perhaps co-occur with other traits. Slower development rates were limited to Acropora, which are generally considered sensitive to hyposalinity and sedimentation, and so this association with offshore reefs may be for reasons not related to larvae but to those other traits. Further research is required to understand this association.

Transfer of Symbiodinium

The benefits conferred to coral species that demonstrate horizontal (symbiont not transferred to offspring) versus vertical (symbiont provided to offspring) transmission of Symbiodinium are still a matter of debate (Stambler 2011; Fabina et al. 2012; Byler et al. 2013). It is widely accepted that vertical transmission enables the continuity of a successful symbiont-host relationship, while horizontal transmission avoids the cost of transmission and allows for flexibility by offspring in adopting novel symbionts, perhaps those better adapted to the local environment (Stambler 2011). The diversity of Symbiodinium is not known in Hervey Bay, but if they are of low diversity like Moreton Bay (Fellegara 2008), just south of Hervey Bay, it would be expected that method of symbiont transfer may make little difference as the available genetic source of symbionts may only be small. Horizontal transmission is the most common form of symbiont transmission in Scleractinian corals (Stambler 2011) and species which show this trait are relatively abundant on Hervey Bay near-mainland reefs in comparison with the abundance of vertical transmission. The ability, for example, to adopt Symbiodinium better suited to changing light conditions could be advantageous in the variably clear to turbid waters of Hervey Bay, particularly during times of flooding, when turbidity may be raised for several months and then immediately afterwards when silt is continually being resuspended (Butler et al. 2015). Moreover, there is a strong positive correlation of vertical transmission with increased distance from mainland and river to the point where the trait for vertical transmission is shown by nearly 100% of the coral occurrences at Four Mile Reef, the most distant from either mainland or river. The relative increase in comparison with horizontal transmission could be explained by the lack of terrigenous or riverine effect; however, Four Mile reef is located at a greater depth (10 m) than most coral reefs known in Hervey Bay and light availability may be an additional factor governing transmission mode of Symbiodinium. Some corals show substantial variability in symbiont composition over short periods of time within the

Chapter 4 same colony (Neal 2013), so it is possible that mode of transmission has no selective importance and its occurrence is coincident with other traits.

Conclusion

The coral reefs of Hervey Bay are commonly subject to flooding. We have shown that this flooding caused altered relative abundances in coral communities for taxonomic composition, but the impacts were not so evident via changes in trait composition in the communities. The impacts of these floods produced some expected results, for example the increase in relative abundance of species in the coral community resistant to hyposalinity and sedimentation (e.g. Turbinaria). The general lack of impact of flooding on the composition of many other traits (e.g. sediment removal ability or polyp size) was not expected. This indicates the likely importance of other flood associated stressors, for example hyposalinity, to flood related mortality, especially at those reefs nearer the mainland or rivers. Overall though, spatial distribution in the abundance of many of the measured traits in Hervey Bay correlated well with both distance from the mainland and distance from rivers, indicating the importance of terrestrial and riverine stressors to reef coral community composition. The frequency of severe storms and flooding are predicted to increase under climate change and these changes, and the resulting reduced periods of recovery, may further alter the composition of the coral communities of Hervey Bay such that only the corals most resistant to terrestrial and riverine stressors will persist.

Acknowledgements

We acknowledge support and funding from the Australian Research Council Centre of Excellence for Coral Reef Studies, The University of Queensland and the National Environmental Research Program Tropical Ecosystems Hub Project 1.3., the Burnett Mary Regional Group, Reef Check Australia and the Queensland Government Department of Science, Information Technology, Innovation and the Arts, Brisbane. We gratefully acknowledge generous field support from the staff of the Queensland Parks and Wildlife, Great Sandy Region, Hervey Bay, Queensland, as well as Ross Smith, Tyson Martin and Andrew Olds. Thanks to Maria Zann for provision of photo transect data for Pt. Vernon East for 2010. Sincere thanks to the many fellow researchers of the Marine Palaeoecology Lab, the Spatial Ecology Lab, and Earth Sciences at The University of Queensland for advice, assistance with statistical analyses and manuscript preparation.

Chapter 4

References

Anderson M, Gorley R, Clarke KR (2008) PERMANOVA+ for Primer: Guide to Software and Statistical Methods. Primer-E, Plymouth, UK Arthaud F, Vallod D, Robin J, Bornette G (2012) Eutrophication and drought disturbance shape functional diversity and life-history traits of aquatic plants in shallow lakes. Aquat Sci 74:471-481 Ayling AM, Ayling AL (1998) The Effect of the Daintree River Flood Plume On Snapper Island Coral Reefs. Great Barrier Reef Marine Park Authority Baird AH, Guest JR, Willis BL (2009) Systematic and Biogeographical Patterns in the Reproductive Biology of Scleractinian Corals. Annual Review of Ecology, Evolution, and Systematics 40:551-571 Beger M, Sommer B, Harrison PL, Smith SDA, Pandolfi JM (2014) Conserving potential coral reef refuges at high latitudes. Diversity and Distributions 20:245-257 Berkelmans R., Jones AM, Schaffelke B (2012). Salinity thresholds of Acropora spp. on the Great Barrier Reef. Coral Reefs 31(4): 1103-1110. Bello F, Carmona CP, Mason NWH, Sebastia MT, Leps J (2013) Which dissimilarity for functional diversity: trait means or trait overlap? Journal of Vegetation Science 24(5):807-819 BOM (2014) Flood warning system for the Mary River. Australian Government Bureau of Meteorology Bonser S, Ladd B (2011) The evolution of competitive strategies in annual plants. Plant Ecol 212:1441-1449 Browne, N. K. (2012) Spatial and temporal variations in coral growth on an inshore turbid reef subjected to multiple disturbances. Marine Environmental Research 77(0): 71-83 Butler IR, Sommer B, Zann M, Zhao Jx, Pandolfi JM (2013) The impacts of flooding on the high- latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia. Coral Reefs 32:1149-1163 Butler IR, Sommer B, Zann M, Zhao Jx, Pandolfi J (2015) The cumulative impacts of repeated heavy rainfall, flooding and altered water quality on the high-latitude coral reefs of Hervey Bay, Queensland, Australia. Mar Pollut Bull doi:10.1016/j.marpolbul.2015.04.047 Byler KA, Carmi-Veal M, Fine M, Goulet TL (2013) Multiple Symbiont Acquisition Strategies as an Adaptive Mechanism in the Coral Stylophora pistillata. PLoS ONE 8:e59596 Cai W, Purich A, Cowan T, van Rensch P, Weller E (2014) Did Climate Change–Induced Rainfall Trends Contribute to the Australian Millennium Drought? Journal of Climate 27:3145-3168 Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, Lydon D, Edgar GJ, Edwards AJ, Fenner D, Guzmán HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Moore JA, Obura DO, Ochavillo D, Polidoro BA, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD, Sanciangco J, Sheppard A, Sheppard C, Smith J, Simon S, Turak E, Veron JEN, Wallace C, Weil E, Wood E (2008) One-Third of Reef-Building Corals Face Elevated Extinction Risk from Climate Change and Local Impacts. Science 321:560-563 Case A, Barrett SH (2004) Environmental stress and the evolution of dioecy: Wurmbea dioica (Colchicaceae) in Western Australia. Evolutionary Ecology 18:145-164 Cavender-Bares J, Reich PB (2012) Shocks to the system: community assembly of the oak savanna in a 40-year fire frequency experiment. Ecology 93:S52-S69 Clarke, K. R. (1993). Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18(1): 117-143

Chapter 4 Coppo C, Brodie J, Butler IR, Mellors J, Sobtzick S (2014) Status of the Coastal and Marine Assets in the Burnett Mary Region. Centre for Tropical Water and Aquatic Ecosystem Research (TropWATER), James Cook University 81 Darling ES, Alvarez-Filip L, Oliver TA, McClanahan TR, Côté IM (2012) Evaluating life-history strategies of reef corals from species traits. Ecology Letters 15:1378-1386 De'ath G, Fabricius K (2010) Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl 20:840-850 DeVantier L (2010) Reef-building corals of Hervey Bay, South-East Queensland. Baseline Survey Report to the Wildlife Preservation Society of Queensland, Fraser Coast Branch, June 2010. Devlin MJ, McKinna LW, Álvarez-Romero JG, Petus C, Abott B, Harkness P, Brodie J (2012) Mapping the pollutants in surface riverine flood plume waters in the Great Barrier Reef, Australia. Marine Pollution Bulletin 65:224-235 Díaz M, Madin J (2011) Macroecological relationships between coral species’ traits and disease potential. Coral Reefs 30:73-84 Ding Y, Zang R, Letcher SG, Liu S, He F (2012) Disturbance regime changes the trait distribution, phylogenetic structure and community assembly of tropical rain forests. Oikos 121:1263- 1270 Done TJ (1982) Patterns in the distribution of coral communities across the central Great Barrier Reef. Coral Reefs 1:95-107 Dornelas M (2010) Disturbance and change in biodiversity. Philos Trans R Soc Lond B Biol Sci 365:3719-3727 Dunn, OJ (1961). Multiple Comparisons Among Means. Journal of the American Statistical Association 56(293): 52-64 Eppley SM, Jesson LK (2008) Moving to mate: the evolution of separate and combined sexes in multicellular organisms. Journal of Evolutionary Biology 21:727-736 Erftemeijer PLA, Riegl B, Hoeksema BW, Todd PA (2012) Environmental impacts of dredging and other sediment disturbances on corals: A review. Marine Pollution Bulletin 64:1737-1765 Fabina NS, Putnam HM, Franklin EC, Stat M, Gates RD (2012) Transmission Mode Predicts Specificity and Interaction Patterns in Coral-Symbiodinium Networks. PLoS ONE 7:e44970 Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: Review and synthesis. Marine Pollution Bulletin 50:125-146 Fabricius KE, Wild C, Wolanski E, Abele D (2003) Effects of transparent exopolymer particles and muddy terrigenous sediments on the survival of hard coral recruits. Estuarine, Coastal and Shelf Science 57:613-621 Faxneld S, Jörgensen TL, Tedengren M (2010) Effects of elevated water temperature, reduced salinity and nutrient enrichment on the metabolism of the coral Turbinaria mesenterina. Estuarine, Coastal and Shelf Science 88:482-487 Fellegara I (2008) Ecophysiology of the marginal, high-latitude corals (Coelenterata: Scleractinia) of Moreton Bay, QLD. The University of Queensland, p151 Fellegara I, Baird AH, Ward S (2013) Coral reproduction in a high-latitude, marginal reef environment (Moreton Bay, south-east Queensland, Australia). Invertebrate Reproduction & Development 57:219-223 Fischer AG (1961) LATITUDINAL VARIATIONS IN ORGANIC DIVERSITY. American Scientist 49:50-74 Fogarty MJ, P SM, Cohen EB (1992) Recruitment variability and the dynamics of exploited marine populations. Trends in Ecology & Evolution 6:241 - 245 Freeman, L. A. (2015). Robust Performance of Marginal Pacific Coral Reef Habitats in Future Climate Scenarios. PLoS ONE 10(6): e0128875 Furnas MJ (2003) Catchments and corals:Terrestrial runoff to the Great Barrier Reef. Australian Institute of Marine Science, Townsville

Chapter 4 Gower JC (1966) Some Distance Properties of Latent Root and Vector Methods Used in Multivariate Analysis. Biometrika 53:325-338 Gräwe U, Wolff JO, Ribbe J (2010) Impact of climate variability on an east Australian bay. Estuarine, Coastal and Shelf Science 86:247-257 Greenstein BJ and Pandolfi JM (2008) Escaping the heat: Range shifts of reef coral taxa in coastal Western Australia. Global Change Biology 14(3): 513-528 Harii S, Hongo C, Ishihara M, Ide Y, Kayanne H (2014) Impacts of multiple disturbances on coral communities at Ishigaki Island, Okinawa, Japan, during a 15 year survey. Marine Ecology Progress Series 509: 171-180. Harriott VH, Banks SB (2002) Latitudinal variation in coral communities in eastern Australia: a qualitative biophysical model of factors regulating coral reefs. Coral Reefs 21:83-94 Harrison P (2011) Sexual Reproduction of Scleractinian Corals. In: Dubinsky Z, Stambler N (eds) Coral Reefs: An Ecosystem in Transition. Springer Netherlands, pp59-85 Hopley D, Smithers SG, Parnell KE (2007) The Geomorphology of the Great Barrier Reef. Cambridge University Press, Cambridge Hughes TP, Baird AH, Dinsdale EA, Harriott VJ, Moltschaniwskyj NA, Pratchett MS, Tanner JE, Willis BL (2002) Detecting Regional Variation Using Meta-Analysis and Large-Scale Sampling: Latitudinal Patterns in Recruitment. Ecology 83:436-451 Jackson JBC and Hughes TP (1985) Adaptive Strategies of Coral-Reef Invertebrates: Coral-reef environments that are regularly disturbed by storms and by predation often favor the very organisms most susceptible to damage by these processes. American Scientist 73(3): 265- 274 Johns KA, Osborne KO, Logan M (2014) Contrasting rates of coral recovery and reassembly in coral communities on the Great Barrier Reef. Coral Reefs 33:553-563 Johnson DP (1996) State of the Rivers, Mary River and its tributaries: An Ecological and Physical Assessment of the Condition of Streams in the Mary River Catchment State of the Rivers. Department of Natural Resources, Indooroopilly Jokiel PL, Hunter CL, Taguchi S, Watarai L (1993) Ecological impact of a fresh-water “reef kill” in Kaneohe Bay, Oahu, Hawaii. Coral Reefs 12:177-184 Jones AM, Berkelmans R (2014) Flood Impacts in Keppel Bay, Southern Great Barrier Reef in the Aftermath of Cyclonic Rainfall. PLoS ONE 9:e84739 Karlson RH (1999) Dynamics of coral communities. Kluwer Academic Publishers, London Keith SA, Baird AH, Hughes TP, Madin JS, Connolly SR (2013) Faunal breaks and species composition of Indo-Pacific corals: the role of plate tectonics, environment and habitat distribution. Proceedings of the Royal Society B: Biological Sciences 280 Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463-1464 Kleypas J, Menez A, McManus J (1999) Environmental Limits to Coral Reef Development: Where Do We Draw the Line? American Zoologist 39:146-159 Kroon FJ, Kuhnert PM, Henderson BL, Wilkinson SN, Kinsey-Henderson A, Abbott B, Brodie JE, Turner RDR (2012) River loads of suspended solids, nitrogen, phosphorus and herbicides delivered to the Great Barrier Reef lagoon. Marine Pollution Bulletin 65(4-9): 167-181. Laliberte E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299-305 Leibold MA, McPeek MA (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87:1399-1410 Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecology Letters 4:122-131 McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends in Ecology & Evolution 21:178-185

Chapter 4 Meagher TR (2007) Linking the Evolution of Gender Variation to Floral Development. Annals of Botany 100:165-176 Milbau A, Shevtsova A, Osler N, Mooshammer M, Graae BJ (2013) Plant community type and small-scale disturbances, but not altitude, influence the invasibility in subarctic ecosystems. New Phytologist 197:1002-1011 Mora C, Frazier AG, Longman RJ, Dacks RS, Walton MM, Tong EJ, Sanchez JJ, Kaiser LR, Stender YO, Anderson JM, Ambrosino CM, Fernandez-Silva I, Giuseffi LM, Giambelluca TW (2013) The projected timing of climate departure from recent variability. Nature 502:183-187 Mouillot D, Graham NAJ, Villéger S, Mason NWH, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends in Ecology & Evolution 28:167-177 Muir, P. R. et al. (2015). Limited scope for latitudinal extension of reef corals. Science 348(6239): 1135-1138

Nagel TA, Svoboda M, Kobal M (2013) Disturbance, life history traits, and dynamics in an old- growth forest landscape of southeastern Europe. Ecol Appl 24:663-679 Neal, B. P. (2013) Growth and recovery of three Caribbean scleractinian coral species following the severe thermally-mediated bleaching event of 2005. Biological Sciences, University of California, San Diego. PhD: 175. Nozawa Y, Tokeshi M, Nojima S (2006) Reproduction and recruitment of scleractinian corals in a high-latitude coral community, Amakusa, southwestern Japan. Marine Biology 149:1047- 1058 Pakeman R, Lennon J, Brooker R (2011) Trait assembly in plant assemblages and its modulation by productivity and disturbance. Oecologia 167:209-218 Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37-42 Philipp E, Fabricius K (2003) Photophysiological stress in scleractinian corals in response to short- term sedimentation. Journal of Experimental Marine Biology and Ecology 287:57-78 Pianka ER (1970) On r- and K-Selection. The American Naturalist 104:592-597 Pollock FJ, Lamb JB, Field SN, Heron SF, Schaffelke B, Shedrawi G, Bourne DG, Willis BL (2014) Sediment and Turbidity Associated with Offshore Dredging Increase Coral Disease Prevalence on Nearby Reefs. PLoS ONE 9:e102498 Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM, Halpern BS, Holding J, Kappel CV, O/'Connor MI, Pandolfi JM, Parmesan C, Schwing F, Thompson SA, Richardson AJ (2013) Global imprint of climate change on marine life. Nature Clim Change 3:919-925 Pratchett MS, Trapon M, Berumen ML, Chong-Seng K (2011) Recent disturbances augment community shifts in coral assemblages in Moorea, French Polynesia. Coral Reefs 30(1): 183-193. Preece T, Mao Y (2009) Sustainability of dioecious and hermaphrodite populations on a lattice. Journal of Theoretical Biology 261:336-340 R_Core_Team (2012) R: A language and environment for statistical computing. R Core Team. R Foundation for Statistical Computing. Vienna, Austria. Radziejewska T (2002) Responses of Deep-Sea Meiobenthic Communities to Sediment Disturbance Simulating Effects of Polymetallic Nodule Mining. International Review of Hydrobiology 87:457-477 Sheridan C, Grosjean P, Leblud J, Palmer CV, Kushmaro A, Eeckhaut I (2014) Sedimentation rapidly induces an immune response and depletes energy stores in a hard coral. Coral Reefs 33:1067-1076 Sofonia JJ, Anthony KRN (2008) High-sediment tolerance in the reef coral Turbinaria mesenterina from the inner Great Barrier Reef lagoon (Australia). Estuarine, Coastal and Shelf Science 78:748-752 66

Chapter 4 Sommer B, Harrison PL, Beger M, Pandolfi JM (2014) Trait-mediated environmental filtering drives assembly at biogeographic transition zones. Ecology 95:1000-1009 Stafford-Smith M, Ormond R (1992) Sediment-rejection mechanisms of 42 species of Australian scleractinian corals. Marine and Freshwater Research 43:683-705 Stafford-Smith MG (1993) Sediment-rejection efficiency of 22 species of Australian scleractinian corals. Marine Biology 115:229-243 Stambler N (2011) Zooxanthellae: The Yellow Symbionts Inside Animals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer Netherlands, pp87-106 Steinberg CR (2012) Stress Ecology: Environmental Stress as Ecological Driving Force and Key Player in Evolution. Springer Netherlands Swenson (2012) Phylogenetic and functional alpha and beta diveristy in temperate and tropical tree communities Swenson (2014) Functional & Phylogenetic Ecology in R Tanentzap AJ, Lee WG, Schulz KAC (2013) Niches drive peaked and positive relationships between diversity and disturbance in natural ecosystems. Ecosphere 4:art133 Thompson A, Schroeder T, Brando V, Schaffelke B (2014) Coral community responses to declining water quality Whitsundays. Coral Reefs 33: 923–938. True, J. D. and Piromvaragorn S (2012). Salinity as a structuring force for the near shore coral communities. 12th International Coral Reef Symposium, Cairns, Australia. Veron J (2000) Corals of the World. Australian Institute of Marine Science, Townsville Villéger S, Mason NWH, Mouillot D (2008) New Multidimensional Functional Diversity Indices for a Multifaceted Framework in Functional Ecology. Ecology 89:2290-2301 Wallace J, Stewart L, Hawdon A, Keen R, Karim F, Kemei J (2009) Flood water quality and marine sediment and nutrient loads from the Tully and Murray catchments in north Queensland, Australia. Marine and Freshwater Research 60:1123-1131 Walters AW (2011) Resistance of aquatic insects to a low-flow disturbance: exploring a trait-based approach. Journal of the North American Benthological Society 30:346-356 Webb CO (2000). Exploring the Phylogenetic Structure of Ecological Communities: An Example for Rain Forest Trees. The American Naturalist 156(2): 145-155. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and Community Ecology. Annual Review of Ecology and Systematics 33:475-505 Weiher E, Keddy PA (1995) Assembly Rules, Null Models, and Trait Dispersion: New Questions from Old Patterns. Oikos 74:159-164 Weiher E, Clarke GDP, Keddy PA (1998) Community Assembly Rules, Morphological Dispersion, and the Coexistence of Plant Species. Oikos 81:309-322 Wooldridge S, Brodie J, Furnas M (2006) Exposure of inner-shelf reefs to nutrient enriched runoff entering the Great Barrier Reef Lagoon: Post-European changes and the design of water quality targets. Marine Pollution Bulletin 52:1467-1479 Yamano HK, Sugihara K, Nomura K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophysical Research Letters 38(4) Zann M (2012) The Use of Remote Sensing and Field Validation for Mapping Coral Communities of Hervey Bay and the Great Sandy Strait and Implications for Coastal Planning Policy. M Phil thesis, University of Queensland, St Lucia, p216

Chapter 4 Tables

Table 1 List of functional traits and sub-categories for assessing composition of the hard coral communities of Hervey Bay, Queensland, Australia.

Trait Trait Category Description Source Sediment Group 1 Easily and rapidly manipulates all Stafford-Smith and Ormond clearance ability sediment sizes 1992 Group 2 Easily but slowly manipulates silt, fine and coarse sand Group 3 Easily and rapidly manipulates silt to fine sand, while larger material is much slower Group 4 Slow manipulation of silt to fine sand, larger material very slowly Group 5 Slow, delayed manipulation of silt and sand, little rejection of larger material Group 6 Virtually no active rejection mechanism, passive Colony Branching Sommer et al. 2014 morphology Plate Massive encrusting Foliose Sex Hermaphroditic Both sexes in colony Baird et al. 2009 Gonochoric Single sex only Propagule Larval group 1 Brooding Keith et al. 2013 development Larval groups 2 - 6 From small to large egg size = from fast to slow larval development Corallite Plocoid Corallites with own walls Sommer et al. 2014 arrangement Cerioid Corallites with shared walls Meandroid Elongate meandering corallites Polyp size Very small < 2 mm Veron 2000 Small 2 – 5 mm Medium 6 – 8 mm Large 8+ mm Symbiont Horizontal Not transferred to offspring Baird et al. 2009 transmission Vertical Transferred to offspring Depth range (m) 10, 20, 30, 40, 50 Typical range of depth Carpenter et al.2008 Reproductive Broadcast spawning Release of gametes Baird et al. 2009 mode Brooding

Chapter 4 Table 2 List of taxa, coral species composition (presence/absence) and total species richness on the reefs of Hervey Bay, Queensland, Australia before recent flooding (2010) and after repeated flooding (2013).

Four Mile Burkitt's Big Woody Pialba Pt. Vernon Pt. Vernon Reef Reef Reef East West Taxa 2010 2013 2010 2013 2010 2013 2010 2013 2010 2013 2010 2013 Acanthastrea lordhowensis ------+ - Acropora bushyensis + - - - - - + - - - - - Acropora digitifera - - - - + + ------Acropora glauca + + + ------Acropora spp. + - + ------Cyphastrea seraila - + ------+ - - Favia danae ------+ Favia favus* ------Favia maritima - - - - + + - - + + + + Favia spp. ------+ Favia veroni* ------Favites chinensis - - - - + ------Favites flexuosa ------+ - Favites pentagona - - - - - + + - - - - - Favites spp. ------Goniastrea aspera - - - - - + - - - - - + Goniastrea australensis ------+ - Goniastrea favulus ------+ Goniopora spp. - - + + + + + + + + + + Montastrea curta ------+ + - Montipora mollis - + - - + ------Montipora spongodes + + ------Montipora spp. - + ------Montipora turtlensis - + ------Plesiastrea versipora - - - - - + - - + - - - Pocillopora damicornis + + + - + + - - + - + + Psammocora superficialis ------+ + - - Psammocora spp. ------+ - - - - - Turbinaria bifrons ------+ - - - - - Turbinaria frondens - - - + - - - + + - - - Turbinaria mesenterina ------+ + + + - - Turbinaria patula - - - - - + - - - - + - Turbinaria peltata - - - - + + + + + + + + Turbinaria radicalis - - + + - + - + + - + + Turbinaria reniformis ------+ - - - + - Turbinaria spp. - - - - - + + - - - + - Turbinaria stellulata - - + - - + - + + - + + Cladiella group + + + + + + + + + + + + Gorgonian - - + + ------Lobophytum spp. + - + + + + + + + - + + 69

Chapter 4

Sarcophyton spp. - - + + + - + - + + + + Soft coral (Mostly Xenia spp.) - + + + - - + - - - + + Total Species 7 9 11 8 10 14 13 8 13 9 17 14 * Present in 2011 survey only

F (pseudo) value for factor D_Rv x Yr x Yr x Metric Period D_Rv D_Mn D_Mn Yr D_Rv D_Mn Taxonomic composition 2010 - 2011 30.975** 11.841** 10.099** 6.2928** ns ns (Hard and soft) 2011 - 2013 23.933** 9.4527** 14.793** ns ns ns 2010 - 2013 33.004** 12.507** 12.007** 11.011** ns ns ns=not significant (P>0.002) **P≤0.002 (Bonferroni correction) D_Rv = Distance from river; D_Mn = Distance from mainland; Yr = between years (flood effect)

Table 4 SIMPER analysis of 2010 and 2013 coral communities on the reefs of Hervey Bay, Queensland, Australia. Percent contribution based on Bray-Curtis dissimilarity of abundance of genera (cut off set to minimum 5% contribution).

Genus Mean Abundance Mean Abundance Contribution to Cumulative 2010 (% Cover) 2013 (% Cover) Dissimilarity (%) (%)

Cladiella 22.21 5.55 37.12 37.12 Goniopora 7.96 3.35 16.01 53.13 Turbinaria 5.32 4.47 13.86 66.99 Pocillopora 4.24 1.68 10.33 77.31 Montipora 2.1 2.25 7.79 85.1 Acropora 3.57 2.6 7.68 92.78

Chapter 4 Table 5 Summary results for permutational analysis of variance (PERMANOVA) with distance covariates for changes in individual functional traits on the reefs of Hervey Bay, Queensland, Australia after single years of flooding (2010 vs. 2011, 2011 vs. 2013) and after repeated years of flooding (2010 vs. 2013). Significance of PERMANOVA model factors based on P value with Bonferroni correction to P ≤ 0.002.

F (pseudo) value for factor D_Rv x Yr x Yr x Metric Period D_Rv D_Mn D_Mn Yr D_Rv D_Mn Sediment clearance 2010 - 2011 28.599** 20.733** 8.4261** ns ns ns 2011 - 2013 22.420** 19.584** 14.257** ns ns ns 2010 - 2013 26.602** 24.114** 7.973** ns ns ns Colony morphology 2010 - 2011 9.5773** 10.310** ns ns ns ns 2011 - 2013 12.63** 7.1358** 7.3067** ns ns ns 2010 - 2013 8.7305** 10.053** ns ns ns ns Sex 2010 - 2011 43.29** 20.193** 10.142** ns ns ns 2011 - 2013 36.754** 13.032** 22.728** ns ns ns 2010 - 2013 46.387** 21.501** 13.157** ns ns ns Reproductive mode 2010 - 2011 21.559** 6.487** 11.761** ns ns ns 2011 - 2013 21.655** 5.0571 25.013** ns ns ns 2010 - 2013 16.897** 3.7497 12.362** ns ns ns Propagule development 2010 - 2011 15.815** 7.6732** 4.4796** ns ns ns rate 2011 - 2013 12.408** 6.3467** 11.717** ns ns ns 2010 - 2013 17.844** 8.2562** 4.7154** 4.7794** ns ns Corallite arrangement 2010 - 2011 5.6681** ns ns ns ns ns 2011 - 2013 9.2852** 2.4429 9.3456** ns ns ns 2010 - 2013 5.8439** 0.68256 5.9447** ns ns ns Polyp size (Category) 2010 - 2011 16.973** 0.753 5.4798** ns ns ns 2011 - 2013 12.749** 2.6846 11.690** ns ns ns 2010 - 2013 15.444** 0.5986 5.7125** ns ns ns Symbiont transmission 2010 - 2011 55.127** 11.202** 21.3** ns ns ns 2011 - 2013 52.891** 8.7345** 40.784** ns ns ns 2010 - 2013 55.401** 8.7874** 23.335** ns ns ns Depth range 2010 - 2011 16.942** 1.2148 4.9721** ns ns ns 2011 - 2013 12.341** 1.8135 10.546** ns ns ns 2010 - 2013 16.420** 2.465* 4.8873** 3.850** ns ns Hard v Soft 2010 - 2011 17.827** ns ns 5.9579** ns ns 2011 - 2013 15.849** 4.4049 14.479** ns ns ns 2010 - 2013 23.347** 0.657 8.5834** 16.11** ns ns Life History 2010 - 2011 43.298** 20.733** 13.85** ns ns ns 2011 - 2013 38.019** 15.166** 26.938** ns ns ns 2010 - 2013 44.681** 23.388** 14.891** ns ns ns ns=not significant (P>0.002) **P≤0.002 (Bonferroni Correction) D_Rv = Distance from river; D_Mn = Distance from mainland; Yr = between years (flood effect)

Chapter 4 Figures

Fig. 1 Location of Mary River, Burnett River and coral reef study sites in Hervey Bay, Queensland, Australia. All mapped areas are within Great Sandy Marine Park.

Chapter 4 Fig. 2 Non-metric multidimensional scaling (NMDS) plot of total hard and soft coral community structure on the six reefs from Hervey Bay, Queensland, Australia for 2010, 2011 (after single flood) and 2013 (after repeated flooding).

Chapter 4 Fig. 3 Photographs from Hervey Bay, Queensland, Australia; a) Goniopora sp. mortality after flooding; b) Turbinaria spp. thriving; c) Acropora thriving at Big Woody; d) Inshore reefs like Pialba have high sedimentation; e) Favids with large polyps have generally strong sediment removal ability. a b

d e

Chapter 4 Fig. 4 Relative abundance of genera of hard and soft corals between 2010 and 2013 for the individual six reefs of Hervey Bay, Queensland, Australia (a–f) and for all reefs combined (g).

Chapter 4 Fig. 5 Canonical analysis of principal coordinates (CAP) showing (a) hard and soft coral community composition (most common genera)(Red Vectors) between 2010 and 2013 for coral reefs of Hervey Bay, Queensland, Australia in relation to distance from the mainland and distance from the nearest river (Black vectors). (b) Trait categories (Red vectors) and life-history categories (Black vectors) that primarily define the communities relative to distance from mainland and distance from nearest river. Vectors for trait categories are only those with correlation > 0.4. All vectors for life history classification were included.

Chapter 4 Fig. 6 Changes in trait categories for a) Depth Range, b) Propagule Development Rate and c) Hard versus Soft corals before (2010) and after repeated flooding (2013) in Hervey Bay, Queensland, Australia. a

Chapter 4

Supplementary tables

Supplementary Table 1 Functional traits and life history characterisation for hard coral species of

Hervey Bay, Queensland, Australia.

Corallite Corallite

Formation

Horizontal

Vertical

Horizontal

Vertical

Horizontal

Vertical

Horizontal

Symbiont Symbiont

Transmission

Size

Small

Large

Medium

Verysmall

Corallite Corallite

rate

Propagule Propagule

development development

of of

depth

Range

Active Active

Sediment Sediment

clearance

Brooding

Broadcast

Dispersal Dispersal

Sex

Gonochoric

Hermaphroditic

2.5

3.5

2.5

Size Size

(mm)

Polyp Polyp

Plate

Local Local

Shape

Foliose

Colony Colony

Enc-mass

Branching

Enc-mass

Branching

Enc-mass

Life Life

History History

spp. spp.

Species

spp.

spp. spp.

spp.

Enc-mass = Encrusting-Massive Enc-mass

Life History: W = weedy, C = competitive, S = stress tolerant Sstress = C competitive, = weedy, = W History: Life

Turbinaria stellulata Turbinaria

Turbinaria Turbinaria

Turbinaria reniformis reniformis Turbinaria

Turbinaria radicalis Turbinaria

Turbinaria peltata Turbinaria

Turbinaria patula patula Turbinaria

Turbinaria mesenterina mesenterina Turbinaria

Turbinaria frondens Turbinaria

Turbinaria bifrons bifrons Turbinaria

Psammocora

Psammocora superficialis Psammocora superficialis

Pocillopora damicornis Pocillopora

Plesiastrea versipora Plesiastrea

Montipora turtlensis turtlensis Montipora

Montipora Montipora

Montipora spongodes spongodes Montipora

Montipora mollis mollis Montipora

Montastrea curta

Goniopora Goniopora

Goniastrea favulusGoniastrea

Goniastrea australensis australensis Goniastrea

Goniastrea aspera Goniastrea

Favites

Favites pentagona

Favites flexuosa

Favites chinensis Favites chinensis

Favia veroni

Favia

Favia maritima

Favia favus

Favia danae

Cyphastrea seraila

Acropora Acropora

Acropora glauca Acropora

Acropora digitifera Acropora Acropora bushyensis Acropora Acanthastrea lordhowensis

Chapter 5 Chapter 5: Historical drivers of spatial and temporal variation in high-latitude coral reef formation and community composition of Hervey Bay, Queensland, Australia

I. R. Butler M. Lepore T.R. Clark J.-x. Zhao J. M. Pandolfi

I. R. Butler1 contact email: [email protected]

M. Lepore1

T. Clark2

J-x Zhao2

J. M. Pandolfi1

1Australian Research Council Centre of Excellence for Coral Reef Studies and, School of Biological Sciences, The University of Queensland, Brisbane, Australia

2Radiogenic Isotope Laboratory, School of Earth Sciences, The University of Queensland, Brisbane, Queensland 4072 Australia

Keywords: palaeoecology, high-latitude, Australia, coral, historical, coring, accretion, communities, U-Series Thorium dating, cyclicity

Chapter 5 Abstract

In Queensland, Australia, colonisation and land clearance in the1850’s and associated increased terrestrial runoff are considered to have had a detrimental effect on marine communities, including coral reefs, however, we cannot be sure of the change without adequate knowledge of historical range of variation. Here we examine the palaeoecological history of four coral reefs in Hervey Bay, Queensland, Australia. Through the collection of percussion cores and death assemblages and the use of Uranium-Thorium dating, we generate a precise chronological history of these coral reefs through the Holocene epoch to assess temporal changes in coral communities and reef development. Despite high-latitude and close proximity to the frequently flooding Mary River, coral reef communities have thrived here for ~6500 years. Reef coral diversity is low (13 genera) and communities have alternated between Acropora dominated assemblages and assemblages dominated by stress tolerant genera, such as Goniopora and Turbinaria, suggesting that conditions are temporally variable in terms of optimal conditions for particular communities, resulting in multiple stable states. While the taxonomic composition of some communities (e.g. Goniopora / Turbinaria) has coincided with periods of sea level instability, the relative abundance of Acropora versus other genera varies regularly with a cyclicity of ~1600 years, a similar periodicity to some published lunar, solar and thermohaline cycles, as well as a possible millennial scale ENSO cycle. The current high relative abundance of stress tolerant genera is consistent with the periodicity for these genera. There is a positive correlation of total coral abundance and high frequency of El Niño events. ENSO also affects the composition of coral communities, but this differs depending on distance from the mainland. Away from the mainland, dry El Niño conditions result in generally higher abundance of coral and generally higher abundance of the rapid growing, but stress sensitive Acropora, while low frequency of El Niño events (La Niña periods) resulted in reduced total coral and increased relative abundance of the more stress tolerant corals such as Goniopora and Turbinaria. In contrast, nearer the mainland, El Niño conditions result in increased abundance of stress tolerant coral (e.g. Goniopora, Turbinaria), perhaps as a result of increased bleaching, while La Niña conditions unexpectedly results in higher abundance of Acropora. Coral community structure is also correlated with SST, with increased relative abundance of Acropora at higher temperatures, though total coral abundance decreased significantly nearshore with increased SST. Although there was a lack of core material from 1200 - 1969 AD, most likely the result of a hiatus in coral growth, which prevents a clear assessment of the impacts of European colonisation and catchment modification, the contrast between currently low and historical high relative abundance of Acropora and the replacement with a novel coral community on Four Mile Reef after

Chapter 5 colonisation, suggests the possibility of anthropogenic influence. Although proximity to the Mary River and terrestrial runoff may restrict diversity of future coral community assemblages, the long history of relatively uninterrupted coral presence and reef growth indicates the potential for Hervey Bay to act as a high latitude refugia under climate change.

Introduction

Ecological systems vary in composition and structure over many different spatial and temporal scales (Fukami and Wardle 2005). However, it is becoming increasingly clear that we are experiencing global defaunation (McCauley et al. 2015) at a rate that some authors are comparing with the mass extinctions of the Cretaceous – Paleogene boundary 66 million years ago (Pimm and Raven 2000; Schulte et al. 2010; Stork 2010). While humans are widely implicated for the recent changes, natural variability makes it difficult to discern the causes of change and, in some cases, to detect its presence. Our ability to detect ecological change is often clouded by shifting baselines syndrome, whereby what is being considered as natural now may already be a significantly altered state and not representative of historical natural conditions (Pauly 1995). In order to understand the magnitude of ecological degradation, it is necessary to quantify both environmental drivers and the corresponding response in community structure and function over periods of time that typically exceed conventional experimentation and observation (Fukami and Wardle 2005). One way of evaluating the natural or pristine state of a system is by documenting ecological and environmental data from the past, gaining an understanding of the natural historical range of variability (Morgan et al. 1994; Pitcher 2001; Hessburg and Povak 2015).

Worldwide there is strong evidence that coral reefs are in a state of degradation (Pandolfi et al. 2003; Quinn and Kojis 2006; Veron 2008; WRI 2011). Significant declines in coral cover over recent decades have occurred in the Caribbean (Cramer et al. 2012; Jackson et al. 2014) and the Pacific (Hughes et al. 2003), including the GBR (De’ath et al. 2012). There are also increasing numbers of coral species considered by some to be under threat of extinction (Carpenter et al. 2008). While there are a number of potential natural and geological drivers for this change, such as orbital forcing (Miall 2010), ENSO (Toth et al. 2012), volcanoes (Pandolfi et al. 2006) and earthquakes (Aronson et al. 2011), where coral reef communities may naturally shift from one stable state to another, there is increasing concern about the effects of anthropogenic stressors such as overfishing, terrestrial runoff, coral harvesting, recreational impacts, pollution (Hughes 2008; Hughes et al. 2010) and climate change (Pandolfi et al. 2011). Coral reef communities are variable 81

Chapter 5 in their ability to return to their former state after disturbance (Holling 1973). While some reef communities have been known to persist with relatively uninterrupted community composition over millennia (DiMichele et al. 2004; Pandolfi and Jackson 2006), species composition can also vary frequently and over much shorter time scales (Karlson 1999). There are many studies documenting declines or impacts on living coral reefs; however, they are generally limited to a short time frame, so it remains uncertain the magnitude of change from communities that existed prior to human interaction. As a result, these studies are not able to determine whether substantial degradation is new or if the change is within the natural range of variability (NRV). These historical perspectives are vital to the correct differentiation of what was natural in the sea versus what is the result of anthropogenic impacts (Pandolfi et al. 2003; Pandolfi 2011a, b) .

Coral reefs are an excellent habitat for reconstructing historical state as a result of scleractinian corals’ ability to accrete living reef structures that then fossilize. Fossil coral reefs represent an important historical database for understanding modern reef communities and how they have changed over time (Pandolfi and Greenstein 2007; Montaggioni and Braithwaite 2009). Individual species or groups preserved in the fossil record are readily identifiable and precise ages can be determined by a number of high-resolution radiometric methods (Montaggioni and Braithwaite 2009). Fossil reefs, through examination of geochemistry, reef development and community change, can also act as a proxy for examining palaeoclimate, including historical temperatures, salinity, turbidity and pH (Grottoli and Eakin 2007; Pandolfi 2011b).

High-latitude coral reefs have historically been considered inferior versions of tropical reefs, growing in marginal conditions with low productivity, reduced accretion and comprised of depauperate communities (Kleypas et al. 1999). Despite the less optimal conditions of lower temperatures, light availability and aragonite saturation state, corals have shown remarkable adaptability and these reef communities are being recognized as unique, highly productive and diverse (Lybolt et al. 2011; Zann 2012; Dalton and Roff 2013; Denis et al. 2013; Sommer et al. 2014). With the exception of Moreton Bay Queensland (Lybolt et al. 2011), very little is known regarding the historical ecology of high latitude, terrigenoclastic influenced reefs. Previous coring work has been carried out in the central Great Barrier Reef region and, with a few exceptions (Roche et al. 2011; Roff et al. 2013) this work has primarily focussed on geomorphic development rather than coral communities (Hopley et al. 2007).

Chapter 5 Increased terrestrial runoff as a result of coastal and catchment modification is considered one of the major threats to coral reefs, especially for more marginal, nearshore reefs (Brodie et al. 2012; Kroon et al. 2014). In Queensland, Australia, colonisation and land clearance in the1850’s (Matthews 1995; Brown 2012) and the resulting increased terrestrial runoff (Kroon et al. 2012) likely had a major influence on marine communities, especially those near the coastline (Wooldridge et al. 2006; Brodie et al. 2012; Waterhouse et al. 2012; Bartley et al. 2014). The potential impacts of high sedimentation and turbidity on coral reefs are well known (Fabricius 2005; Erftemeijer et al. 2012; Pollock et al. 2014) and, while there is some evidence that this has occurred historically as a result of colonisation and the associated catchment land changes (Lybolt et al. 2011; Roff et al. 2013), the degree to which anthropogenic changes are impacting reefs is still contested (Szmant 2002; Perry et al. 2008). In some places, reefs survive well under what would otherwise be considered unsuitable, highly turbid conditions (Perry et al. 2008; Browne et al. 2012) and the reef has kept pace with (or promoted) rapidly accumulating fine sediment (Perry et al. 2012; Perry et al. 2013).

Here we examine the palaeoecological history of the coral reefs of Hervey Bay, Queensland, Australia. Hervey Bay reefs are near the southern margin for fringing coral reef formation along the east coast of Australia. Along the mainland south of Hervey Bay, corals tend to form communities on non-coralline hard substrate (Harriott and Banks 2002). Hervey Bay coral reefs are also subject to terrestrial runoff and flooding from the highly modified Mary River catchment (Butler et al. 2013). Through the collection of reef matrix cores and the use of U-Th dating, we generate a precise chronological history of four coral reefs through the Holocene epoch to assess temporal changes in coral communities and their relation to reef sediments and accretion rates. With this historical baseline, we then assess the likely impacts on coral reefs since European colonisation and the associated modification of adjacent catchments and lands.

Materials and methods

The study area

Hervey Bay (25.00o S, 152.85o E) is situated at the northern end of the Great Sandy Straits on the southern coast of Queensland, Australia (Fig. 1). Four coral reef sites were examined for this study including two reefs near the mainland, Pt. Vernon West and Pialba, and two reefs more distant from

Chapter 5 the mainland, Four Mile and Big Woody (Fig. 1). Three of the four reefs are fringing reefs that occur in less than 5 m water depth HAT(Highest Astronomical Tide) and are exposed at the lowest tides of the year. Four Mile Reef is a near-shore detached reef that is found at ~10 m water depth HAT and is not exposed at low tide (Table 1). The reefs are located from 0.4 to 5 km from the mainland and 18 to 70 km from the Mary River. As a result, they are variably exposed to terrestrial runoff (Table 1) (Butler et al. 2013). All reefs are protected from prevailing oceanic swell and the fetch from the dominant south-east trade winds is reduced by either Fraser Island or the mainland (Fig. 1, Table 1)

Modern coral assemblages

Data for the relative abundance of modern assemblages of hard coral for Hervey Bay for 2011 were obtained from photo-transects carried out by Butler et al. (2013).

Coral death assemblages

Dead coral rubble was haphazardly collected at three locations at each core site – immediately adjacent to the core and five meters away in opposing directions. From each location, these death assemblages were scooped into one 10 litre cloth bag. The sizes of the coral pieces were limited by the circumference of the opening of the bag (maximum size approx. 15 x 15 cm). The death assemblages from each bag were sorted by genus and genera weighed to determine relative abundance. These relative abundances were then compared to those measured in modern assemblages using Analysis of Similarity (ANOSIM) (Clarke and Gorley 2006).

Historical coral assemblages: Reef matrix cores

To investigate the historical ecology of these reefs, a total of seventeen reef matrix cores were taken from between 5 and 10 metres water depth (HAT) at various locations on the four reefs (Figs. 2a-d) using percussion coring techniques based on that of Dardeau (2000) (Detailed coring methodology: Supplementary Information).

Chapter 5 Prior to sectioning the cores, their internal contents were scanned with computed axial tomography (CT). Cores were then cut lengthwise in half with a table saw and one core half was archived at 4o C at The University of Queensland Quaternary Core Facility and the other half designated for sub- sectioning and analysis. The core material in the non-archived half was divided into 5 cm subsections and the total material in each sub-section was wet weighed. All objects greater than ~4 mm were manually removed from each sub-section and placed in a 4 mm sieve, where all material < 4 mm was rinsed and retained for future use. All of the 4 mm+ coral from each subsection was identified to genus and weighed and this category called “Total Coral”. The pieces of coral material that could not be identified were placed into an “unknown coral” category which was incorporated into the Total Coral category but excluded from analyses of coral relative abundance among communities.

Sediment categories for analyses

Through visual examination of CT scans and core sediments, core facies were identified and described according to a combination of the Wentworth scale and the textural nature of the sediments (Mount 1985). Because the facies descriptions were in part based on the position and amount of coral, where sediment type was a factor in the statistical analyses of coral abundance, only the non-coral portion of the sediment description was used to categorise sediment types. For example, a core subsection described as being “floatstone and bafflestone in medium to coarse sand” was placed into the category “medium to coarse sand”.

U-Th dating

In order to generate a chronology for each of the cores, samples of coral were selected for U-Th dating from subsections at: the tops of the cores; the lowest layers in the cores which contained coral pieces; locations with obvious transitions (e.g. layers of particularly low or high abundance of coral material), and; where changes between sediment facies were obvious. The ages of individual subsections between these dated subsections were calculated by interpolation. Corals from death assemblages were also selected for U-Th dating to determine the recent composition of certain genera. For Big Woody Reef, where Acropora is common, it was assumed that death assemblages would have a high composition of recent Acropora, so non-Acropora samples were chosen from these assemblages for dating to estimate the more recent appearance of these genera. For Pialba

Chapter 5 and Pt. Vernon West reefs, where Acropora is no longer present, Acropora specimens were selected from death assemblages to determine the timing of the disappearance of Acropora from these reefs. As a result of the already large number of samples dated from the near-surface facies in the cores from Four Mile Reef, no death assemblages were U-Th dated. A total of 93 samples from core subsections and 27 samples from death assemblages were taken for U-Th dating at the Radiogenic Isotope Facility at The University of Queensland, following rigorous cleaning, separation of uranium and thorium and measurements by Nu Plasma Inductively Coupled Plasma Mass Spectrometer (MC-ICP-MS) (as per Clark et al.(2014)).

Accretion

For the purposes of this study, reef accretion is defined as the accumulation of autogenic carbonate materials - including sediment, hard shelled biota and coral skeletons - into a three dimensional structure, which may or may not be cemented together through the presence of coralline algae. Accretion rates were calculated between subsections which contained U-Th dated samples using the following equation:

(Depth (mm) Sample 2 – Depth (mm) Sample 1) ⁄ ( Date Sample 2 – Date Sample 1)

Each subsection within this interval was considered as having this accretion rate. For multivariate analyses of coral abundance, it was necessary to create slow, medium and fast accretion rate categories. The slow, medium and fast accretion rate categories were determined by calculating the 1st and 3rd quartiles from all the accretion intervals for all cores. To maintain context with accretion rates for other inshore reef areas of Queensland, we also calculated the slow, medium and fast rates in the same way from published coring data for the inner shelf reefs of the east coast of Queensland, Australia (Perry and Smithers 2011). Negative accretion rates were assigned where age reversals indicated a temporal mixing of sedimentary layers, and these were excluded from the calculations of accretion rate categories and also analyses. The presence of an unusual deposition event was defined by the presence of a facies which clearly differed from adjacent facies, where the measured U-Th dates at the top and bottom of the interval were the same. Through the course of investigations, only one such deposition event was found and this layer was excluded from analyses to prevent disproportionate influence of this event on results.

ENSO data

Chapter 5

The relationships between ENSO cycles and both coral reef development and reef coral community composition were assessed by using historical ENSO data from Lake Palcacocha, Ecuador (Moy et al. 2002). These data consist of frequency of El Niño events per 100 year intervals through 12,000 years of the Holocene. These data were used as is for comparisons with total coral. For multivariate analyses, the ENSO data were converted to low (0 - 2 events), medium (3 - 8 events) and high (9+ events) categories based on the 1st and 3rd quartiles of the data. These calculations only include data for the time period for which it is known that coral were living in Hervey Bay.

SST data

The relationships between SST and coral abundance and coral community composition were assessed by using average SST proxy data from stable oxygen isotopes from foraminifera in the tropical western Pacific (Stott et al. 2004). These data consist of estimates of average SST (o C) in 250 year bins. These data were used as is for comparisons with total coral. For multivariate analyses, the SST data were converted to low (<29.00 o C), medium (29.00 – 29.26 o C) and high (> 29.26 o C) categories based on the 1st and 3rd quartiles of the SST bins. These calculations only include data for the time period for which it is known that coral were living in Hervey Bay.

Data analyses

Changes in total coral were compared with accretion rate, sediment type, ENSO frequency and temperature. All core subsections were used where marine sediments were apparent and contained other marine organisms, such as mollusks. To assess changes in total coral with respect to accretion rate, ENSO frequency and SST, linear (or non-linear depending on fit) models were generated for square-root of total coral versus untransformed accretion rate, SST and ENSO frequency. The significance of the regression was tested by Pearson correlation. For SST and ENSO, separate linear models were also generated for nearshore and offshore data. We used ANOSIM to assess if total coral varied with sediment composition. Subsections composed of rudstone were excluded from analyses of total coral abundance because they are high in coral by definition and would skew the results in favour of significance.

Chapter 5 Coral community composition in the cores was compared with accretion rate categories, sediment type, distances from mainland, ENSO categories and SST categories. For analyses of coral community composition, the only subsections included in the analyses were those in which identifiable coral was present. For multivariate changes in coral communities, the square root of absolute abundance of coral genera from each core sub-section was compared with every other core sub-section using the Bray-Curtis similarity index. Relative changes in abundance through subsections corresponding to accretion rate groups and sediment types were analysed with ANOSIM. To examine changes of coral community structure with ENSO and SST, additional factors were included in the analyses to distinguish the possible effects of proximity to mainland. Data from reefs near to the mainland (Factor = Near) (Pialba and Pt. Vernon West reefs) were compared with those more distant from the mainland (Factor = Far) (Big Woody and Four Mile reefs). These were then analysed against ENSO or SST categories with a two fixed factor Permutational Analysis of Variance (PERMANOVA) (Anderson et al. 2008).

To examine temporal variation in coral community structure, all of the cores with recognisable genera were combined by averaging absolute abundances from all core subsections dated to a particular century, then converting to relative abundance for that century. Dates for centuries were used as interpolated between the dated samples and there was no attempt to account for hiatuses in the calculation of the relative abundances. To investigate cyclicity in Acropora abundance, the relative abundance data for Acropora were then analysed by wavelet analysis using a Morlet transformation (Torrence and Compo 1998) with a 0 lag time and 95% confidence limits (in comparison with white noise). The cone of influence was also calculated, which highlights the ends of the dataset where edge effects may alter the results. For comparison with the Acropora data, the same wavelet analysis was carried out on a subset (i.e. same time period) of the data for frequency of El Niño events per century (Moy et al. 2002). In order to present an alternate method of assessing cyclicity, autocorrelation was also carried out on these data sets to measure peaks in correlation of time lags, where 95% confidence limits are based on comparison with white noise (Davis 1986; Hammer and Harper 2006).

Other analyses were carried out to examine relationships between physical and climate factors. Frequency of El Niño events was compared with the sediment type through ANOSIM. SST and frequency of El Niño events were compared via linear regression.

Chapter 5 All univariate statistics were carried out with Graphpad Prism 6 software. Multivariate statistics were carried out with Primer v6 software (Clarke 1993; Clarke and Gorley 2006). Wavelet and autocorrelation analyses were carried out using the software package PAST (Hammer et al. 2001).

Results

Current coral communities

The study site at Pt. Vernon West Reef supports a coral community with little in the way of three dimensional reef structure (Fig. 3a). It is the nearest of the cored reefs to the mainland and is frequently turbid (Butler et al. 2015). Despite the turbidity, it is equal highest in species richness of the study reefs (DeVantier 2010; Butler et al. 2013) and supports very large coral colonies. Seventy- five percent of the coral community is Goniopora, ~20% Turbinaria and the balance made up of a diverse range of “Other”, mostly favid, coral genera (Fig. 4a).

Pialba Reef is a fringing reef composed of primarily large Turbinaria colonies surrounded by fine sediment, though these large colonies appear to be currently coalescing horizontally into increasingly large reef structures (Fig. 3b). Species richness is second lowest of the study reefs (Butler et al. 2013) and the reef community is dominated by Turbinaria (95%), the balance almost all Goniopora (Fig.4b).

Big Woody Reef shows some vertical structure reminiscent of reef structures on the Great Barrier Reef (Fig. 3d), particularly in places where there has been a rapid growth of Acropora branches combined with the thick, encrusting morphology (Fig. 3c). Big Woody reef is substantial, rising ~5 m as a mound from the sea floor. This reef is found near the northern entrance to Great Sandy Strait and is subject to the impacts of terrestrial runoff, especially flooding from the Mary River 18 km away (Butler et al. 2013). Big Woody Reef is the second most distant reef from the mainland (4 km) and the coral community is dominated by Goniopora (~50%), Acropora (~20%) and Turbinaria (~20%) (Fig. 4c).

Four Mile Reef shows substantial structural relief, with vertical, high-density coral rising up to 1 m above the surrounding seascape (Fig. 3e), but with little evidence of the cementation that occurs in more tropical areas through the consolidation of coral rubble with coralline algae. The coral 89

Chapter 5 communities on Four Mile Reef contain the lowest number of taxa of all the reefs and are currently dominated by Pocillopora (~65%) and Montipora (~30%) (Fig. 4d) (Butler et al. 2013).

Coral composition in death assemblages

The relative abundance of coral genera in the death assemblages was significantly different (ANOSIM, P<0.05) to the modern life assemblages at all reefs (Fig. 4a-d). This was particularly the case at Pialba and Big Woody reefs, where Acropora was dominant in the death assemblages but was replaced by Turbinaria and Goniopora, respectively, as the dominant hard coral in the modern communities (Fig. 4b).

U-Th dating

The distribution of the U-Th dates from the coral samples, including death assemblages, indicates that corals were present in Hervey Bay for at least the past ~6500 years (Table 2, 3, Fig. 5a)(See also Supplementary Fig. 1 for age vs depth in core). Only one hiatus in coral presence is evident from the data and this was most apparent at Four Mile Reef, where samples from adjacent core subsections indicate a gap from ~1218 – 1969 (Fig. 5b) (with the exception of a narrow window of coral presence ~1835 to 1863 AD). While there is a general lack of samples dated from this time period, indicating that this hiatus may have occurred at all reefs, coral samples from nearby shore deposits have been dated to this hiatus period (Butler, unpublished data) and this casts some doubt as to whether this is a region-wide occurrence.

Core sediments

The cores collected varied in length from 0.5 to 4.7 m (uncompacted) for all reefs (Figs. 6 - 9). In thirteen of the seventeen cores, the base of the core includes Pleistocene clay or rock, therefore cores covered the full Holocene history of the reefs. Sediment composition was variable between and within cores from fine silt to coarse sand, pebbles and cobble (Figs. 6 - 9).

Pt. Vernon West Reef cores were composed of shallow reef sediments (0.10 to 0.7 m.) on top of either rock or Pleistocene clay (Fig. 6). U-Series dating suggests coral has been present since at

Chapter 5 least ~745 BC (Fig. 6, PC09). The combination of shallow core depths combined with wide ranging Th dates indicates that Pt. Vernon West has historically been more of a coral community than an accreting reef, though some areas (e.g. Core PC09, Fig. 6) do show accretion. For all analyses of historical communities and accretion in core material, where reefs were examined individually or combined, only core PC09 from Pt. Vernon West was used.

Pialba Reef cores are generally short, with a maximum length of 1.2 m, uncompacted, with reef material on top of Pleistocene clay (Fig. 7). Reef inception dates to at least 2887 BC (Fig. 7, PC08). Core material was largely composed of mixed floatstone and bafflestone in silt to coarse sand (Fig. 7).

Big Woody cores, at up to 4.7 m uncompacted length (e.g. Fig. 8, PC01), are some of the longest collected from Hervey Bay. Big Woody cores generally show well developed reef sediment facies with variable quantities of silt to coarse sand mixed with coral bafflestone and floatstone (Fig. 8). Most cores show a large (0.5 – 2.5 m), well-defined facies of coral floatstone and bafflestone in silt to medium sand. One core (Fig. 8, PC04) shows evidence of a substantial depositional event (~0.50 m silt) which took place ~1067 BC. Big Woody Reef has a long history with coral dating back to at least ~4531 BC (Fig. 8, core PCT2). Inception of coral reef formation was on Pleistocene clay (e.g. Fig. 8, cores PC02, PC04), rock (e.g. Fig. 8, core PCT2) or silt / wood (e.g. Fig. 8, core PC01).

Four Mile Reef cores are up to 4.5 m in length, uncompacted (Fig. 9). As a result of the difficulties inserting cores into the dense, living portions of Four Mile Reef, we obtained only one core (Fig. 9, PC05) from this part of the reef. Three others we obtained from the rubble immediately adjacent to the reef structure. Two of the Four Mile Reef cores have Pleistocene clay (Fig. 9, PC03, PC04) at the base and U-Th dating indicates reef inception ~875 AD (Fig. 9, PC03). Four Mile Reef cores are composed of variable quantities of silt to coarse sand mixed with coral bafflestone and floatstone (Fig. 9). Most cores have a large (0.5 – 3.0 m), well-defined facies of coral floatstone and bafflestone in silt to medium sand. Where the cores were taken from the rubble zone, immediately adjacent to the reef (PC02, PC03, PC04), each of the cores has a distinct, well-mixed, facies of floatstone in medium coarse sand in the top 0.5 m – 0.6 m of the cores. The core subsections from the bottom of these rubble facies were dated from ~1000 to 1200 AD. Reversals near the surface in PC02 and PC03, show mixing of coral rubble from 1835 to 2010 AD. With the exception of a small window from 1835 to 1863 AD, U-Th dated samples indicate a likely 700+ year hiatus in the presence of coral from 1218 to 1969 AD (Fig. 9). A well-defined hiatus in coral growth is most

Chapter 5 evident in core PC05, the one core that went straight through the more solid, higher relief portions of the reef where coral is currently alive.

Accretion rates

Accretion rates for intervals within the Hervey Bay cores varied from 0.1 mm yr-1 (Fig. 7, PC09) to 24.0 mm yr-1 (Fig. 8, PC02). Accretion rate groups were calculated to be Slow (< 0.8 mm yr-1), Medium (0.9 – 8.4 mm yr-1) and Fast (>8.4 mm y-1). These groups are similar to those calculated for the east coast of Queensland: Slow (<1.4 mm yr-1), Medium (1.4 – 5.4 mm yr-1) and Fast (>5.4 mm y-1) (Data from (Perry and Smithers 2011)).

El Niño frequency versus sediment types and SST

Sediment type was found to vary significantly with frequency of El Niño (Global R = 0.089, P = 0.01), but the very low Global R value indicates small differences in El Niño frequency between the sediment groups. Coarse sand and pebble and silt were associated with high frequency of El Niño events (~16 per 100 years) while coarse sand was associated with low frequency El Niño periods (Fig. 10). SST did not vary significantly with frequency of El Niño events (F = 0.307, p > 0.05).

Historical community composition through cores

A total of 13 genera were found across all the cores (Table 4). Typically, only one or two coral genera were found in any single sub-section of a core. The composition of the coral communities was variable spatially and temporally. Historical coral diversity was low on Pt. Vernon West Reef, with only four genera (Table 4), though this was based on the short lengths of core material and death assemblages. Goniopora dominated this coral community, although Acropora and Turbinaria were also present (Fig. 6). Goniopora death assemblages at Pt. Vernon West reef were all recent (Table 3). Historical diversity on Pialba Reef was second highest with eight genera (Table 4). Acropora was dominant from 2887 BC until 1527 AD (Fig. 7, PC09) and Turbinaria was also present throughout this interval (Fig. 7, PC09). Pialba Reef death assemblages corroborate the timing of Acropora disappearance, with the most recent Acropora dated to 1519 AD (Table 3). Big Woody Reef had the greatest past diversity of the studied reefs with 12 genera (Table 4). The coral communities of Big Woody Reef alternated in dominance between Acropora and other genera, 92

Chapter 5 mostly Goniopora, Turbinaria, and various favids (Fig. 8). Evidence from three cores (Fig. 8, PC01, PC04, and PCT2) indicates that coral assemblages prior to 1000 BC consist of mixed genera, but with a high proportion of Acropora. After what appears to be a major depositional event (~0.40 m silt layer) at ~1067 BC (Fig. 8, PC04), coral assemblages were generally dominated by Acropora until near present times. The exception to this was from ~500 AD until 1000 AD when a relatively high proportion of genera such as Goniopora, Turbinaria and favids occurred (Fig. 8, PC01, PC02, PC03, PC06, PCT1). Goniopora and Turbinaria on Big Woody Reef were virtually all recent, with the exception of one sample which was aged at 530 AD (Table 3). Acropora was the overwhelmingly dominant coral genus through all Four Mile Reef cores from reef inception, though this changed in the top ~0.6 m of each of the cores (Fig. 9). Acropora was absent from 1218 to 1835 AD, then re-appeared until 1863 AD and disappeared again after that (Fig. 9). There was a rapid transition to Pocillopora dominance in the top 0.50 – 0.60 m of all cores and this was most evident in PC05 which went through the consolidated reef (Fig. 9). U-Th dates indicated that Pocillopora became the dominant component of the coral community around 1969AD, 105 years after the Acropora all but disappeared from that reef (Fig 9).

Changes in coral abundance with sediment type, accretion rate, ENSO and SST

Total coral varied significantly with sediment type (Global R = 0.246, P = 0.01). Aside from Rudstone, which was inherently high in coral, total coral abundance was highest in coarse sand facies, followed by silt to medium sand facies and lowest total abundance was found in silt facies and coarse sand rock facies (Fig. 11). Total coral did not vary significantly with accretion rate (F = 2.792, p > 0.05). Total coral increased with increased frequency of El Niño events (F = 9.352, p = 0.002), though there was a low goodness of fit of the linear model (R2 = 0.014) (Fig. 12a). When treated separately, total coral on reefs near the mainland (Pialba, Pt. Vernon West) did not vary significantly with frequency of El Niño events (F = 0.135, p >0.05) (Fig. 12b) while total coral on the far reefs (Big Woody and Four Mile) significantly increased with frequency of El Niño events (F = 17.25, p < 0.0001), though the goodness of fit of the model was low (R2 = 0.031) (Fig. 12b). Total coral overall did not vary significantly with SST (F = 0.015, p > 0.05). Total coral at offshore reefs did not vary significantly with SST (F = 0.460, p > 0.05) (Fig. 13), while total coral on nearshore reefs decreased significantly with increased SST (F = 7.874, p = 0.007), though goodness of fit was low (R2 = 0.1080) (Fig. 13).

Chapter 5 Coral community composition varied significantly with the different sediment types (Global R = 0.283, P = 0.01). Rudstone facies were largely composed of Acropora and Pocillopora. Coarse sand facies were composed almost entirely of Acropora, while the silt, coarse sand and pebble and silt to medium sand facies contained increased relative abundance of Turbinaria and Goniopora (Fig. 14). Historical coral community composition varied significantly between accretion rate categories from Hervey Bay (Global R = 0.081, P = 0.01), as well as those from all of Queensland (Global R = 0.047, P = 0.01), but the very low Global R values indicate small differences in coral community composition between the accretion rate groups. Relative abundances of coral genera among accretion groups were similar for both Hervey Bay and Queensland. There was increased relative abundance of Acropora (~80%) during periods of fast accretion compared with periods of slow accretion (~58%) (Fig. 15).

Historical coral community structure varied significantly between nearshore and offshore reefs and this varied with ENSO. Nearshore and offshore reef communities differed significantly (factor = Distance Mainland, Table 5), but there was a strong interaction with El Niño group (factor = Distance Mainland X El Niño Frequency, Table 5). On reefs near the mainland (Pialba, Pt. Vernon West), relative abundance of Acropora varied from ~25% during high frequency El Niño to ~85% during low frequency El Niño (Fig. 16a). Increased El Niño frequency resulted in greater relative abundance of species such as Goniopora and Turbinaria (Fig. 16a). On the far reefs (Big Woody, Four Mile), relative abundance of Acropora varied from 40% during low frequency El Niño events to 75% during high and moderate frequency El Niño events (Fig. 16b). Decreased El Niño frequency resulted in increasing relative abundance of species such as Goniopora and Turbinaria (Fig. 16b).

Historical community structure varied significantly with SST. Communities differed between nearshore and offshore reefs (factor = Distance Mainland, Table 6) and among SST categories (factor = SST, Table 6). There was also an interaction between these factors (factor = Distance Mainland X SST, Table 6). On nearshore reefs, relative abundance of Acropora was lowest in the low temperature group (18%) and increased to 100% in the high temperature group (Fig. 17a). Goniopora increased with lower SST. On offshore reefs, relative abundance of Acropora was lowest in the low temperature group (55%) and increased to 90% in the high temperature group (Fig. 17b). Pocillopora was the most abundant genus at the lowest temperatures offshore.

Chapter 5 Overall, when all cores are combined by century (Fig. 18), reef coral community assemblages regularly alternate between those dominated by Acropora and those dominated by other species, notably Goniopora and Turbinaria. Current assemblages (Year 2011) are consistent with this pattern of change (Fig. 18). Wavelet analysis of relative abundance of Acropora by century indicates a significant (95% confidence) band of cyclicity at the ~1600 year scale (Fig. 19a), though this band changes at ~3000 BC near the edge of the data (i.e. outside the cone of influence). This 1600 year cyclicity is corroborated by the significant (95% confidence limit) peak in time lag at ~1600 -1700 years found through autocorrelation (Fig. 20). An additional autocorrelation peak occurs at a lag time of 100-200 years, indicating the similarity in Acropora abundance between adjacent centuries. Wavelet analysis of El Niño frequency data (Fig. 19b) also show a significant band of cyclicity at ~1600 years, though the significance of this drops around 3000 BC outside the cone of influence. The El Niño data showed no significant peaks in lag time through autocorrelation.

Discussion

All organisms on Earth are affected by cycles of change on many temporal and spatial scales. Short term cyclic changes, such as daily changes in tides (Bos and Gumanao 2012; Bijoux et al. 2013), or circadian exposure to sunlight and water temperature (Paranjpe and Sharma 2005), can be part of yet larger temporal cycles (e.g. seasonal changes) which affect the dynamics and scale of these shorter term cycles (Longhurst 1995; Raimondo 2012). In a similar fashion, changes to habitats can be driven by forces on a local scale (e.g. storms), which may also be in-turn driven by larger forces at a global scale (e.g. sea surface temperatures) (Yeh et al. 2010; Cai et al. 2011). Coral reefs are no different from any other habitat on Earth. Global drivers such as climate change, sea surface temperature, sea level change and El Niño Southern Oscillation (ENSO) have the potential to influence reef communities and reef formation.

Despite its high-latitude location adjacent to a major river, Hervey Bay has a 6500 year history of coral reefs. This study has shown that these reefs change through different temporal scales – from decadal changes in abundance as a result of ENSO driven flood mortality (Butler et al. 2013; Butler et al. 2015), to longer term changes in ENSO and SST, to cyclic changes in abundance at a millennial scale.

El Niño Southern Oscillation 95

Chapter 5

Of the different possible drivers of change, the potentially large temporal scale influence of ENSO on coral reefs is becoming increasingly apparent (Gischler et al. 2009; Lybolt et al. 2011; Toth et al. 2012). In the Hervey Bay region, El Niño results in increased frequency of hot, dry periods with little rainfall (BOM 2012) and therefore reduced potential for terrestrial runoff. In contrast, La Niña periods have much higher rainfall which results in increased terrestrial runoff and flooding. The negative lethal and sub-lethal effects of terrestrial runoff and high turbidity on coral physiology and recruitment are numerous and potentially long lasting (Fabricius 2005; Erftemeijer et al. 2012; Flores et al. 2012; Pollock et al. 2014). The effect of La Niña on coral reefs is exemplified by the flooding associated with the late 2010 to early 2013 La Niña period which resulted in a cumulative loss of ~56% of coral and significant changes in coral community composition on the coral reefs of Hervey Bay (Butler et al. 2015).

This study reveals contrasting responses of communities to prevailing ENSO conditions depending on proximity to the mainland. Proximity to mainland has been shown to be a significant factor in constructing communities in Hervey Bay (Chapter 4), where flooding causes elevated near-shore turbidity, total suspended solids, nutrients and hyposalinity (including that from prolonged submarine groundwater discharge) relative to more offshore areas (Butler et al. 2015). The present study shows that this is also reflected in historical reef development. In Hervey Bay, where stress from terrestrial runoff and flooding is common (Preen et al. 1995; Gräwe et al. 2010; Butler et al. 2013), reef structure can be highly variable over kilometres. At the more offshore reefs like Big Woody and especially Four Mile, where water quality issues appear reduced, reef development is three dimensional, reminiscent of the high vertical relief reef structures found further north in the Great Barrier Reef. Those reefs nearer the shore such as Pialba and in particular Pt. Vernon West, which are subject to terrestrial runoff and water quality issues, have relatively reduced reef development with shallow reefal sediments on Pleistocene clay or rock.

Modern coral communities also vary with proximity to mainland, with relatively high abundance of stress tolerant corals nearer the mainland and a high abundance of the more stress intolerant species more distant from the mainland (Chapter 4). In terms of historical communities, the responses of those more distant from the mainland to prevailing ENSO conditions match expectations. El Niño, dry conditions result in increased total coral, with communities dominated by rapid growing, stress- intolerant Acropora. In contrast, La Niña wet conditions result in reduced total coral and communities with increased stress tolerant species such as Goniopora and Turbinaria. Our data,

Chapter 5 however, indicate the opposite pattern to be occurring at reefs nearer the mainland. El Niño results in greater abundance of stress tolerant genera, such as Goniopora and Turbinaria, while increased abundance of Acropora is more associated with La Niña periods. Although the results are counterintuitive given recent experience with La Niña conditions including the flooding impacts and the loss of nearshore Acropora during these floods (Chapter 4), this pattern may be explained by the prevalence of, for example, heat or light induced bleaching, which is generally associated with El Niño periods (Berkelmans et al. 2004; Oliver et al. 2009), and which could play a major role in these near-mainland, historically shallow water communities. It is also possible that although La Niña causes high mortality, there are short recovery periods which can be taken advantage of by the rapidly growing Acropora corals. Alternatively, as occurred in 2011 after an El Niño drought period, high mortality and stress may result from post drought transport of relatively high levels of sediment and nutrients, far in excess of what might be transported during regular rainfall periods, when sediment and nutrients are evenly transported and distributed over time. This is supported by the presence of silt, which would be expected from terrestrial runoff, in facies associated with medium to high El Niño frequency rather than low El Niño frequency. Historical SST may also play a role here, for example through warmer temperatures during winter, when water is clearest in Hervey Bay.

Climate, temperature and sea-level changes

While the significant ~1600 year cyclicity in the relative abundance of Acropora and other species and the corresponding ~1600 year cyclicity in El Niño indicates the likely connection of coral abundance with ENSO or a linked process. This periodicity, however, is also similar to other reported cyclicity, such as the Dansgaard-Oeschger (1470-1600 years) (Pisias et al. 2010; Petersen et al. 2013) or Bond cycles (Bond et al. 1997), lunar influenced oceanic tidal variation (~1800 years) (Keeling and Whorf 2000) and oceanic thermohaline circulation (~1500 - 1600 years) (Debret et al. 2007; Debret et al. 2009). In each case, sea surface temperatures (Loehle and Singer 2010) and associated climate (e.g. ENSO) vary as a result of altered circulation patterns. Temperature itself affects many aspects of coral biology and these impacts have been well documented for Acropora with regard to disease resistance (Muller and van Woesik 2014), genetic makeup (Ogawa et al. 2013), Symbiodinium uptake (Cooper et al. 2011), growth (Crabbe 2007), reproduction, larval development and settlement (Randall and Szmant 2009; Winkler et al. 2015). Temperature is of primary importance to the distribution of corals, for example, through latitudinal distribution with changing sea temperatures (Greenstein and Pandolfi 2008; Yamano et al. 2011).

Chapter 5 Along the coast of eastern Australia, temperature plays a major role in the distribution of Acropora through not only average temperatures (Harriott and Banks 2002), but also through the extremes of temperature (Sommer et al. 2014). Assuming the proxy SST used for analyses in this study (i.e. Stott et al. 2004) indicate comparable changes in Hervey Bay SST, then substantial changes in relative abundance of Acropora and other species in Hervey Bay have occurred over only a 0.7 o C change in SST. Climate change predictions are for increased global SST of 1 – 3 o C by 2100 AD (Collins et al. 2013) which exceeds any SSTs experienced by coral reefs of Hervey Bay over the last 6500 years. It is probable, however, that this SST proxy is not directly comparable. Increases in SST in subtropical/temperate waters of Australia are predicted to be 3-4 times that of tropical areas (Lough 2008).

Ocean temperatures and climate (e.g. ENSO oscillations) are inextricably linked, and through the thermal expansion of the ocean and the melting of glaciers and ice caps (Cazenave and Llovel 2010), both are also linked to sea-level change (Han and Huang 2009; Cazenave et al. 2012). The indigenous Butchulla people of the Hervey Bay region have a story passed through many generations about a giant cyclone which generated large waves and removed large portions of northern K’gari (Fraser Island), killing many people (Miller 1993). While it is certainly possible that such a storm occurred and resulted in the major deposition event found at Big Woody Reef, it is also possible that this event was at least in part a result of a sea-level oscillation, which has been identified for that approximate time period (~1500 BC) (Baker and Haworth 2000; Lewis et al. 2013; Leonard et al. In review). Other major changes in environmental conditions occurred ~1500 BC, including changes in forest composition on nearby Fraser Island (Donders et al. 2006) indicating that this may have been a time of significant local climate change. Sea level changes are often a direct result of change in climate (Meier et al. 2007; Camoin and Webster 2015) and such changes they can affect coral communities through the intertwined effects of ocean temperature and changes in water depth. Changes in water depth can impact coral reefs in many ways, for example through increased or decreased growth space in the water column (Perry and Smithers 2011), through sea-level direction of change which can affect the relative abundances of coral colony morphologies (Hongo and Kayanne 2011), and through effects on hydrology and shoreline erosion (Theuerkauf et al. 2014) and resulting changes in, for example, turbidity (Storlazzi et al. 2011). It is likely that such changes in sea level would result in significant changes to the environment of shallow water, sediment-filled embayment like Hervey Bay. Increases in relative abundance of species such as Goniopora, Turbinaria in Hervey Bay coincide with centennial scale sea level instability centred at ~3500 (Lewis et al. 2013; Leonard et al. In review), ~1500 BC (Baker and

Chapter 5 Haworth 2000), ~400AD (Lewis et al. 2013; Leonard et al. In review) and then recently (Gehrels and Woodworth 2013).

Hiatus in reef growth

Coral communities and reef development are variable over time (Karlson 1999; Hopley et al. 2007) and episodic growth and hiatuses have been reported for Holocene coral communities such as Panama (Toth et al. 2012), along the Great Barrier Reef (Perry and Smithers 2011) and in Moreton Bay in south-east Queensland (Lybolt et al. 2011). Coral has been present in Hervey Bay throughout the most recent 6500 years of the Holocene and reef growth has occurred throughout the vast majority of this time. Four Mile Reef shows strong evidence of a hiatus from ~1200 – 1835 AD. This hiatus corresponds with the epoch of prominent La Niña activity in southeast Queensland from 1260 to 1860 (Vance et al. 2013; Vance et al. 2015). Palaeoclimate research has shown that the Intertropical Convergence Zone had migrated southward at this time (Sachs et al. 2009), and this may have resulted in increased rainfall in southern parts of Australia relative to northern areas (Vance et al. 2013), and therefore greater exposure of southern reefs to terrestrial runoff. It is possible that additional hiatuses and/or rapid coral growth periods occur in the coral record and are part of the regular changes seen in coral communities, but were simply not identified as a result of inadequate numbers of dated samples.

Refugia potential of Hervey Bay

With the warming climate, high-latitude reefs will increase in importance as potential refugia for coral (Beger et al. 2014; Freeman 2015; Makino et al. 2014). The southern GBR has been identified as an area with perhaps the greatest potential as a long term refugia for coral under future climate change (van Hooidonk et al. 2013) and Hervey Bay is just south of the park boundary. A number of criteria, using both current (Jones and Berkelmans 2010) and historical (Lybolt et al. 2011) measures, have been proposed for the assessment of coral reefs as potential refugia under climate change. These include light extinction, average daily temperature, coral cover, macro-algal cover, species richness, presence of thermally tolerant symbionts, diverse depths, historical persistence of reef building corals, habitat building capacity and historical ecological stability. Hervey Bay reefs meet many of these criteria. For example, although species diversity is lower at this high-latitude location than more northern parts of the Queensland coast such as the GBR (Veron 2008), it still

Chapter 5 contains at least 101 hard and soft coral species among structurally diverse reefs and at varying depths (Coppo et al. 2014). Recent flood disturbances have highlighted the potential for rapid changes in coral cover and water quality (Butler et al. 2015), as well as the effects of terrestrial and riverine exposure to community composition (Chapter 4), yet these coral communities show 6500 years of near-continuous coral presence indicating resilience to these conditions. In addition, many of the coral communities in Hervey Bay contain large, thriving colonies of massive, foliose and branching corals. This indicates the possibility that recent conditions, perhaps through favourable SST or ENSO conditions, supports strong coral growth in this high-latitude region, despite the effects of occasional flooding. Although there are many uncertainties as to how global warming will affect terrestrial runoff, which is an important factor for community structure, Hervey Bay shows potential as a refugia as the oceans warm.

Anthropogenic impacts

The Mary River is an example of a river catchment highly modified by European colonisation, with only 1% in a natural condition and erosion is considered a major problem (Johnson 1996; Mackenzie and Duke 2011). Since colonisation, the Mary River has filled with sediment and is no longer navigable by large, deep drafted ships (Titmarsh 2007), indicating major changes to the catchment which are likely to impact downstream areas. There are some indications of potential anthropogenic impacts to the coral reefs. For example, Acropora was the dominant genus on Four Mile Reef until ~1863 AD and was replaced by Pocillopora as the dominant genus in assemblage after coral reappeared on Four Mile Reef ~1969. The timing of the disappearance around 1845 to 1863 coincides with the colonisation of the Mary River catchment and the timing of the commencement of land clearance for sheep grazing, timber industry and gold mining ~1840 to 1860 (Matthews 1995; Brown 2012). This time period also marks the end of the La Niña epoch (Vance et al. 2013; Vance et al. 2015), which should have resulted in the subsequent flourishing of coral in Hervey Bay, however, corals have been absent for >100 years until recent decades.

The lack of coral samples that were U-Th dated in Hervey Bay from ~1200 AD until recent decades reduces the ability to detect any anthropogenic driven changes in coral reef attributable to European colonisation. While the historical data indicate a high abundance of Acropora at all of the cored reefs, most reefs are currently dominated by the more stress tolerant corals such as Turbinaria and Goniopora (Butler et al. 2013; Butler et al. 2015). The degree to which this change can be attributed to colonisation along the Queensland coast is not clear since such stress tolerant 100

Chapter 5 assemblages previously occurred naturally in Hervey Bay and appear to be part of a cyclicity of coral communities over the millennia. Current assemblages are consistent with this pattern.

Conclusion

The high-latitude coral reefs of Hervey Bay, Queensland, Australia are near the southern limits for coral reef growth along the east coast of Australia. Despite the colder temperatures, lower light levels, reduced aragonite saturation state and close proximity to the frequently flooding Mary River, coral reefs and communities thrived here for ~6500 years, though there has been substantial spatial and temporal variation in the species composition of the reef communities and overall reef development. Hervey Bay reef geomorphology varies considerably from solid, vertical structures found well offshore from terrigenous influence, such as Four Mile Reef, to simpler non-structural nearshore coral communities at Pt. Vernon West Reef, which are subject to frequent sedimentation (and resuspension) and hypo-salinity from flooding. Historically, reef coral diversity is low with only 13 genera found through all cores. Communities have varied temporally on a ~1600 year cycle, alternating between dominating Acropora assemblages and assemblages dominated by other genera (e.g. Goniopora, Turbinaria), suggesting that optimal conditions for particular communities are cyclic. While this cyclicity matches the periodicity of a number of cycles, for example lunar and solar cycles, Hervey Bay data correlate well with millennial scale ENSO cycles. ENSO affects the composition of coral communities, but this differs depending on distance from the mainland. Away from the mainland, dry El Niño conditions resulted in higher abundance of coral and especially the rapid growing, but stress sensitive Acropora, while low frequency of El Niño events resulted in reduced total coral and increased relative abundance of the more stress tolerant corals such as Goniopora and Turbinaria. In contrast, near the mainland, El Niño conditions resulted in increased abundance of stress tolerant coral (e.g. Goniopora, Turbinaria), while La Niña conditions unexpectedly resulted in higher abundance of Acropora. Some historical changes in the coral communities of Hervey Bay coincided with times of sea level change. Coral communities in Hervey Bay also correlated with SST, with increased relative abundance of Acropora with higher temperatures and increased abundance of other species, notably Goniopora and Turbinaria at lower temperatures. While the lack of coral samples dated from ~1200 AD until the mid 1900’s prevents a clear assessment of the impacts of European colonisation, major changes have taken place in the local Mary River catchment resulting in siltation of river channels and elevated levels of sediment, nutrients and hyposaline waters transported to Hervey Bay, especially during recent La Niña episodes. The abrupt cessation of coral growth on Four Mile Reef coinciding with colonisation of

101

Chapter 5 the Mary River catchment and the subsequent replacement of historically dominant Acropora assemblage by a novel assemblage of Pocillopora support the possibility of anthropogenic driven change. Although proximity to the Mary River and terrestrial runoff may limit the diversity of coral assemblages, the long history of relatively uninterrupted coral presence and resilience to disturbances indicates the potential for Hervey Bay to act as high latitude refugia under climate change.

Acknowledgments

We acknowledge support and funding from the Australian Research Council Centre of Excellence for Coral Reef Studies, The University of Queensland and the National Environmental Research Program Tropical Ecosystems Hub Project 1.3. We gratefully acknowledge generous field support from the staff of the Queensland Parks and Wildlife, Great Sandy Region, Hervey Bay, Queensland and field assistance by Hayden Coburn, Omer Polak and especially Nicole Leonard, who provided valuable insight into historical sea levels. We also gratefully acknowledge the assistance of staff from the Radiogenic Isotope Facility for assistance with U-Series Thorium dating. Sincere thanks to fellow researchers of the Marine Palaeoecology Lab and the Spatial Ecology Lab, in particular George Roff, who was always good for a reality check.

References

Anderson M, Gorley R, Clarke KR (2008) PERMANOVA+ for Primer: Guide to Software and Statistical Methods. Primer-E, Plymouth, UK Aronson RB, Precht WF, Macintyre IG, Toth LT (2011) Catastrophe and the life span of coral reefs. Ecology 93:303-313 Baker RGV, Haworth RJ (2000) Smooth or oscillating late Holocene sea-level curve? Evidence from the palaeo-zoology of fixed biological indicators in east Australia and beyond. Marine Geology 163:367-386 Bartley R, Bainbridge ZT, Lewis SE, Kroon FJ, Wilkinson SN, Brodie JE, Silburn DM (2014) Relating sediment impacts on coral reefs to watershed sources, processes and management: A review. Science of The Total Environment 468–469:1138-1153 Beger M, Sommer B, Harrison PL, Smith SDA, Pandolfi JM (2014) Conserving potential coral reef refuges at high latitudes. Diversity and Distributions 20:245-257 Berkelmans R, De’ath G, Kininmonth S, Skirving W (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral Reefs 23:74-83 Bijoux JP, Dagorn L, Gaertner JC, Cowley PD, Robinson J (2013) The influence of natural cycles on coral reef fish movement: implications for underwater visual census (UVC) surveys. Coral Reefs 32:1135-1140

102

Chapter 5 BOM (2012) Record breaking La Nina events: An analysis of the La Nina life cycle and the impacts and significance of the 2010-2011 and 2011-2012 La Nina events in Australia. Australian Bureau of Meteorology, Melbourne 28 Bond G, Showers W, Cheseby M, Lotti R, Almasi P, deMenocal P, Priore P, Cullen H, Hajdas I, Bonani G (1997) A Pervasive Millennial-Scale Cycle in North Atlantic Holocene and Glacial Climates. Science 278:1257-1266 Bos AR, Gumanao GS (2012) The lunar cycle determines availability of coral-reef fishes at fish markets. Journal of Fish Biology 81:2074-2079 Brodie JE, Kroon FJ, Schaffelke B, Wolanski EC, Lewis SE, Devlin MJ, Bohnet IC, Bainbridge ZT, Waterhouse J, Davis AM (2012) Terrestrial pollutant runoff to the Great Barrier Reef: An update of issues, priorities and management responses. Marine Pollution Bulletin 65:81- 100 Brown E (2012) Maryborough and Its History: Placing the Maryborough Environment in Historical Context. Queensland Review 19:6-14 Browne NK, Smithers SG, Perry CT (2012) Coral reefs of the turbid inner-shelf of the Great Barrier Reef, Australia: An environmental and geomorphic perspective on their occurrence, composition and growth. Earth-Science Reviews 115:1-20 Butler IR, Sommer B, Zann M, Zhao Jx, Pandolfi JM (2013) The impacts of flooding on the high- latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia. Coral Reefs 32:1149-1163 Butler IR, Sommer B, Zann M, Zhao Jx, Pandolfi J (2015) The cumulative impacts of repeated heavy rainfall, flooding and altered water quality on the high-latitude coral reefs of Hervey Bay, Queensland, Australia. Mar Pollut Bull doi:10.1016/j.marpolbul.2015.04.047 Cai W, van Rensch P, Cowan T, Hendon HH (2011) Teleconnection Pathways of ENSO and the IOD and the Mechanisms for Impacts on Australian Rainfall. Journal of Climate 24:3910- 3923 Camoin GF, Webster JM (2015) Coral reef response to Quaternary sea-level and environmental changes: State of the science. Sedimentology 62:401-428 Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, Lydon D, Edgar GJ, Edwards AJ, Fenner D, Guzmán HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Moore JA, Obura DO, Ochavillo D, Polidoro BA, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD, Sanciangco J, Sheppard A, Sheppard C, Smith J, Simon S, Turak E, Veron JEN, Wallace C, Weil E, Wood E (2008) One-Third of Reef-Building Corals Face Elevated Extinction Risk from Climate Change and Local Impacts. Science 321:560-563 Cazenave A, Llovel W (2010) Contemporary Sea Level Rise. Annual Review of Marine Science 2:145-173 Cazenave A, Henry O, Munier S, Delcroix T, Gordon AL, Meyssignac B, Llovel W, Palanisamy H, Becker M (2012) Estimating ENSO Influence on the Global Mean Sea Level, 1993–2010. Marine Geodesy 35:82-97 Clark TR, Roff G, Zhao J-x, Feng Y-x, Done TJ, Pandolfi JM (2014) Testing the precision and accuracy of the U–Th chronometer for dating coral mortality events in the last 100 years. Quaternary Geochronology 23:35-45 Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18:117-143 Clarke KR, Gorley R (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth Collins M, Knutti R, Arblaster J, Dufresne J-L, Fichefet T, Friedlingstein P, Gao X, Gutowski WJ, Johns T, Krinner G, Shongwe M, Tebaldi C, Weaver AJ, Wehner M (2013) Long-term Climate Change: Projections, Commitments and Irreversibility. In: Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change Cambridge University Press, . In:

103

Chapter 5 Stocker TF, D. Qin, G.-K. Plattner, M. Tignor, S.K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex and P.M. Midgley (eds.), Cambridge, United Kingdom and New York, NY, USA. Cooper TF, Berkelmans R, Ulstrup KE, Weeks S, Radford B, Jones AM, Doyle J, Canto M, O'Leary RA, van Oppen MJH (2011) Environmental Factors Controlling the Distribution of Symbiodinium Harboured by the Coral Acropora millepora on the Great Barrier Reef. PLoS ONE 6:e25536 Coppo C, Brodie J, Butler IR, Mellors J, Sobtzick S (2014) Status of the Coastal and Marine Assets in the Burnett Mary Region. Centre for Tropical Water and Aquatic Ecosystem Research (TropWATER), James Cook University 81 Crabbe MJC (2007) Global warming and coral reefs: Modelling the effect of temperature on Acropora palmata colony growth. Computational Biology and Chemistry 31:294-297 Cramer KL, Jackson JBC, Angioletti CV, Leonard-Pingel J, Guilderson TP (2012) Anthropogenic mortality on coral reefs in Caribbean Panama predates coral disease and bleaching. Ecology Letters 15:561-567 Dalton SJ, Roff G (2013) Spatial and Temporal Patterns of Eastern Australia Subtropical Coral Communities. PLoS ONE 8:e75873 Dardeau M, Aronson RB, Precht WF, Macintyre IG (2000) Use of a hand-operated, open barrel corer to sample uncemented Holocene coral reefs. American Academy of Underwater Sciences Davis JC (1986) Statistics and data analysis in geology. Wiley, New York De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27–year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences 109:17995-17999 Debret M, Sebag D, Crosta X, Massei N, Petit JR, Chapron E, Bout-Roumazeilles V (2009) Evidence from wavelet analysis for a mid-Holocene transition in global climate forcing. Quaternary Science Reviews 28:2675-2688 Debret M, Bout-Roumazeilles V, Grousset F, Desmet M, McManus JF, Massei N, Sebag D, Petit JR, Copard Y, Trentesaux A (2007) The origin of the 1500-year climate cycles in Holocene North-Atlantic records. Clim Past 3:569-575 Denis V, Mezaki T, Tanaka K, Kuo C-Y, De Palmas S, Keshavmurthy S, Chen CA (2013) Coverage, Diversity, and Functionality of a High-Latitude Coral Community (Tatsukushi, Shikoku Island, Japan). PLoS ONE 8:e54330 DeVantier L (2010) Reef-building corals of Hervey Bay, South-East Queensland. Baseline Survey Report to the Wildlife Preservation Society of Queensland, Fraser Coast Branch, June 2010. DiMichele WA, Behrensmeyer AK, Olszewski TD, Labandeira CC, Pandolfi JM, Wing SL, Bobe R (2004) Long-term stasis in ecological assemblages: Evidence from the fossil record Annual Review of Ecology, Evolution, and Systematics 285-322 Donders TH, Wagner F, Visscher H (2006) Late Pleistocene and Holocene subtropical vegetation dynamics recorded in perched lake deposits on Fraser Island, Queensland, Australia. Palaeogeography, Palaeoclimatology, Palaeoecology 241:417-439 Erftemeijer PLA, Riegl B, Hoeksema BW, Todd PA (2012) Environmental impacts of dredging and other sediment disturbances on corals: A review. Marine Pollution Bulletin 64:1737-1765 Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: Review and synthesis. Marine Pollution Bulletin 50:125-146 Figueira, W. F. and D. J. Booth (2010) Increasing ocean temperatures allow tropical fishes to survive overwinter in temperate waters. Global Change Biology 16(2): 506-516. Flores F, Hoogenboom MO, Smith LD, Cooper TF, Abrego D, Negri AP (2012) Chronic Exposure of Corals to Fine Sediments: Lethal and Sub-Lethal Impacts. PLoS ONE 7:e37795 Freeman, L. A. (2015). Robust Performance of Marginal Pacific Coral Reef Habitats in Future Climate Scenarios. PLoS ONE 10(6): e0128875. Fukami T, Wardle DA (2005) Long-term ecological dynamics: reciprocal insights from natural and anthropogenic gradients. Proc Biol Sci 272:2105-2115 104

Chapter 5 Gehrels WR, Woodworth PL (2013) When did modern rates of sea-level rise start? Global and Planetary Change 100:263-277 Gischler E, Hudson JH, Storz D (2009) Growth of Pleistocene massive corals in south Florida: low skeletal extension-rates and possible ENSO, decadal, and multi-decadal cyclicities. Coral Reefs 28:823-830 Gräwe U, Wolff JO, Ribbe J (2010) Impact of climate variability on an east Australian bay. Estuarine, Coastal and Shelf Science 86:247-257 Greenstein BJ, Pandolfi JM (2008) Escaping the heat: Range shifts of reef coral taxa in coastal Western Australia. Global Change Biology 14:513-528 Grottoli AG, Eakin CM (2007) A review of modern coral δ18O and Δ14C proxy records. Earth- Science Reviews 81:67-91 Hammer O, Harper DAT (2006) Paleontological Data Analysis. Blackwell Hammer O, Harper DAT, Ryan PD (2001) PAST:Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4:9 Han G, Huang W (2009) Low-frequency sea-level variability in the South China Sea and its relationship to ENSO. Theor Appl Climatol 97:41-52 Harriott VH, Banks SB (2002) Latitudinal variation in coral communities in eastern Australia: a qualitative biophysical model of factors regulating coral reefs. Coral Reefs 21:83-94 Hessburg P, Povak N (2015) Applying historical range of variability concepts. Landscape Ecol 30:753-755 Holling CS (1973) Resilience and Stability of Ecological Systems. Annual Review of Ecology and Systematics 4:1-23 Hongo C, Kayanne H (2011) Key species of hermatypic coral for reef formation in the northwest Pacific during Holocene sea-level change. Marine Geology 279:162-177 Hopley D, Smithers SG, Parnell KE (2007) The Geomorphology of the Great Barrier Reef. Cambridge University Press, Cambridge Hughes T (2008) Human Impacts on Coral Reefs. In: Hutchings P, Kingsford M, Hoegh-Guldberg O (eds) The Great Barrier Reef: biology, environment and management. CSIRO, Collingwood, Victoria, pp85-94 Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends in Ecology & Evolution 25:633-642 Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh- Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929-933 Jackson JBC, K. DM, Cramer KL, Lam V (2014) Status and Trends of Caribbean Coral Reefs: 1970-2012. Global Coral Reef Monitoring Network, IUCN, Gland, Switzerland Johnson DP (1996) State of the Rivers, Mary River and its tributaries: An Ecological and Physical Assessment of the Condition of Streams in the Mary River Catchment State of the Rivers. Department of Natural Resources, Indooroopilly Jones, A. M. and R. Berkelmans (2010). Marine refugia in the Keppel region of the Great Barrier Reef. Headmark(136): 19-27. Karlson RH (1999) Dynamics of coral communities. Kluwer Academic Publishers, London Keeling CD, Whorf TP (2000) The 1,800-year oceanic tidal cycle: a possible cause of rapid climate change. Proceedings of the National Academy of Sciences of the United States of America 97:3814-3819 Kleypas J, Menez A, McManus J (1999) Environmental Limits to Coral Reef Development: Where Do We Draw the Line? American Zoologist 39:146-159 Kroon FJ, Kuhnert PM, Henderson BL, Wilkinson SN, Kinsey-Henderson A, Abbott B, Brodie JE, Turner RDR (2012) River loads of suspended solids, nitrogen, phosphorus and herbicides delivered to the Great Barrier Reef lagoon. Marine Pollution Bulletin 65(4-9): 167-181.

105

Chapter 5 Kroon, FJ, Schaffelke B, Bartley R (2014). Informing policy to protect coastal coral reefs: Insight from a global review of reducing agricultural pollution to coastal ecosystems. Marine Pollution Bulletin 85(1): 33-41. Leonard ND, Zhao Jx, Welsh KJ, Feng Y, Smithers S, Pandolfi J, Clark TR (In review) Holocene sea level instability in the southern Great Barrier Reef, Australia: high precision U-Th dating of fossil microatolls. Geochimica et Cosmochimica Acta Lewis SE, Sloss CR, Murray-Wallace CV, Woodroffe CD, Smithers SG (2013) Post-glacial sea- level changes around the Australian margin: a review. Quaternary Science Reviews 74:115- 138 Loehle C, Singer SF (2010) Holocene temperature records show millennial-scale periodicity. Canadian Journal of Earth Sciences 47:1327-1336 Longhurst A (1995) Seasonal cycles of pelagic production and consumption. Progress in Oceanography 36:77-167 Lough JM (2008) Shifting climate zones for Australia's tropical marine ecosystems. Geophysical Research Letters 35(14) Lybolt M, Neil D, Zhao J-x, Feng Y-x, Yu K-F, Pandolfi J (2011) Instability in a marginal coral reef: the shift from natural variability to a human-dominated seascape. Frontiers in Ecology and the Environment 9:154-160 Mackenzie J, Duke N (2011) State of the Mangroves 2008: Condition assessment of the tidal wetlands of the Burnett Mary region. School of Biological Sciences, University of Queensland, Brisbane 430 Makino A, Yamano H, Beger M, Klein CJ, Yara Y, Possingham HP (2014) Spatio-temporal marine conservation planning to support high-latitude coral range expansion under climate change. Diversity and Distributions 20:859-871 Matthews T (1995) River of dreams: a history of Maryborough and district. Maryborough City Council, Maryborough McCauley DJ, Pinsky ML, Palumbi SR, Estes JA, Joyce FH, Warner RR (2015) Marine defaunation: Animal loss in the global ocean. Science 347 Meier MF, Dyurgerov MB, Rick UK, O'Neel S, Pfeffer WT, Anderson RS, Anderson SP, Glazovsky AF (2007) Glaciers Dominate Eustatic Sea-Level Rise in the 21st Century. Science 317:1064-1067 Miall A (2010) Orbital Forcing The Geology of Stratigraphic Sequences. Springer Berlin Heidelberg, pp327-353 Miller O (1993) Careen - The Dead Land Fraser Island Legends. Jacaranda, Brisbane, pp43 - 45 Montaggioni LF, Braithwaite CJR (2009) Chapter One Introduction: Quaternary Reefs in Time and Space. In: Montaggioni LF, Braithwaite CJR (eds) Developments in Marine Geology. Elsevier, pp1-21 Morgan P, Aplet GH, Haufler JB, Humphries HC (1994) Historical Range of Variability. Journal of sustainable forestry 2:87-111 Mount J (1985) Mixed siliciclastic and carbonate sediments: a proposed first-order textural and compositional classification. Sedimentology 32:435-442 Moy CM, Seltzer GO, Rodbell DT, Anderson DM (2002) Variability of El Nino/Southern Oscillation activity at millennial timescales during the Holocene epoch. Nature 420:162-165 Muller EM, van Woesik R (2014) Genetic Susceptibility, Colony Size, and Water Temperature Drive White-Pox Disease on the Coral Acropora palmata PLoS ONE 9:e110759 Narayan YR, Lybolt M, Zhao J-x, Feng Y, Pandolfi JM (2015) Holocene benthic foraminiferal assemblages indicate long-term marginality of reef habitats from Moreton Bay, Australia. Palaeogeography, Palaeoclimatology, Palaeoecology 420:49-64 Ogawa D, Bobeszko T, Ainsworth T, Leggat W (2013) The combined effects of temperature and CO2 lead to altered gene expression in Acropora aspera. Coral Reefs 32:895-907 Oliver JK, Berkelmans R, Eakin CM (2009) Coral Bleaching in Space and Time. In: van Oppen MH, Lough J (eds) Coral Bleaching. Springer Berlin Heidelberg, pp21-39 106

Chapter 5 Pandolfi J, Greenstein B (2007) Chapter 22. Using the past to understand the future: palaeoecology of coral reefs Pandolfi JM (2011a) Historical Ecology of Coral Reefs. In: Hopley D (ed) Encyclopedia of Modern Coral Reefs. Springer Netherlands, pp554-558 Pandolfi JM (2011b) The Paleoecology of Coral Reefs. In: Dubinsky Z, Stambler N (eds) Coral Reefs: An Ecosystem in Transition. Springer Netherlands, pp13-24 Pandolfi JM, Jackson JBC (2006) Ecological persistence interrupted in Caribbean coral reefs. Ecology Letters 9:818-826 Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting Coral Reef Futures Under Global Warming and Ocean Acidification. Science (New York, NY) 333:418-422 Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955-958 Pandolfi JM, Tudhope AW, Burr G, Chappell J, Edinger E, Frey M, Steneck R, Sharma C, Yeates A, Jennions M, Lescinsky H, Newton A (2006) Mass mortality following disturbance in Holocene coral reefs from Papua New Guinea. Geology 34:949-952 Paranjpe DA, Sharma VK (2005) Evolution of temporal order in living organisms. Journal of Circadian Rhythms 3:7-7 Pauly D (1995) Anecdotes and the shifting baseline syndrome of fisheries. Trends in Ecology & Evolution 10:430 Perry CT, Smithers SG (2011) Cycles of coral reef ‘turn-on’, rapid growth and ‘turn-off’ over the past 8500 years: a context for understanding modern ecological states and trajectories. Global Change Biology 17:76-86 Perry CT, Smithers SG, Gulliver P (2013) Rapid vertical accretion on a ‘young’ shore-detached turbid zone reef: Offshore Paluma Shoals, central Great Barrier Reef, Australia. Coral Reefs 32:1143-1148 Perry CT, Smithers SG, Gulliver P, Browne NK (2012) Evidence of very rapid reef accretion and reef growth under high turbidity and terrigenous sedimentation. Geology 40:719-722 Perry CT, Smithers SG, Palmer SE, Larcombe P, Johnson KG (2008) 1200 year paleoecological record of coral community development from the terrigenous inner shelf of the Great barrier reef. Geology 36:691-694 Petersen SV, Schrag DP, Clark PU (2013) A new mechanism for Dansgaard-Oeschger cycles. Paleoceanography 28:24-30 Pimm SL, Raven P (2000) Biodiversity: Extinction by numbers. Nature 403:843-845 Pisias NG, Clark PU, Brook EJ (2010) Modes of Global Climate Variability during Marine Isotope Stage 3 (60–26 ka). Journal of Climate 23:1581-1588 Pitcher TJ (2001) Fisheries Managed to Rebuild Ecosystems? Reconstructing the Past to Salvage the Future. Ecol Appl 11:601-617 Pollock FJ, Lamb JB, Field SN, Heron SF, Schaffelke B, Shedrawi G, Bourne DG, Willis BL (2014) Sediment and Turbidity Associated with Offshore Dredging Increase Coral Disease Prevalence on Nearby Reefs. PLoS ONE 9:e102498 Preen A, Lee Long WJ, Coles RY (1995) Flood and cyclone related loss, and partial recovery, of more than 1000 km2 of seagrass in Hervey Bay, Queensland, Australia. Aquatic Botany 52:3-17 Quinn N, Kojis B (2006) Natural Resilience of Coral Reef Ecosystems Coral Reef Restoration Handbook. CRC Press, pp61-75 Raimondo S (2012) Incorporating temperature-driven seasonal variation in survival, growth, and reproduction into population models for small fish. Marine Ecology Progress Series 469:101-112 Randall CJ, Szmant AM (2009) Elevated Temperature Affects Development, Survivorship, and Settlement of the Elkhorn Coral, Acropora palmata (Lamarck 1816). Biological Bulletin 217:269-282 107

Chapter 5 Roche RC, Perry CT, Johnson KG, Sultana K, Smithers SG, Thompson AA (2011) Mid-Holocene coral community data as baselines for understanding contemporary reef ecological states. Palaeogeography, Palaeoclimatology, Palaeoecology 299:159-167 Roff G, Clark T, Reymond-CE, Zhao Jx, Feng Y, McCook L, Done T, Pandolfi J (2013) Palaeoecological evidence of a historical collapse of corals at Pelorus Island, inshore Great Barrier Reef, following European settlement. Proceedings of the Royal Society B 280:20122100 Sachs JP, Sachse D, Smittenberg RH, Zhang Z, Battisti DS, Golubic S (2009) Southward movement of the Pacific intertropical convergence zone AD[thinsp]1400-1850. Nature Geosci 2:519- 525 Schulte P, Alegret L, Arenillas I, Arz JA, Barton PJ, Bown PR, Bralower TJ, Christeson GL, Claeys P, Cockell CS, Collins GS, Deutsch A, Goldin TJ, Goto K, Grajales-Nishimura JM, Grieve RAF, Gulick SPS, Johnson KR, Kiessling W, Koeberl C, Kring DA, MacLeod KG, Matsui T, Melosh J, Montanari A, Morgan JV, Neal CR, Nichols DJ, Norris RD, Pierazzo E, Ravizza G, Rebolledo-Vieyra M, Reimold WU, Robin E, Salge T, Speijer RP, Sweet AR, Urrutia-Fucugauchi J, Vajda V, Whalen MT, Willumsen PS (2010) The Chicxulub Asteroid Impact and Mass Extinction at the Cretaceous-Paleogene Boundary. Science 327:1214-1218 Sommer B, Harrison PL, Beger M, Pandolfi JM (2014) Trait-mediated environmental filtering drives assembly at biogeographic transition zones. Ecology 95:1000-1009 Stork N (2010) Re-assessing current extinction rates. Biodivers Conserv 19:357-371 Storlazzi CD, Elias E, Field ME, Presto MK (2011) Numerical modeling of the impact of sea-level rise on fringing coral reef hydrodynamics and sediment transport. Coral Reefs 30:83-96 Stott L, Cannariato K, Thunell R, Haug GH, et al. (2004) Decline of surface temperature and salinity in the western tropical Pacific Ocean in Holocene epoch. Nature 431:56-59 Szmant AM (2002) Nutrient Enrichment on Coral Reefs: Is It a Major Cause of Coral Reef Decline? Estuaries 25:743-766 Theuerkauf EJ, Rodriguez AB, Fegley SR, Luettich RA (2014) Sea level anomalies exacerbate beach erosion. Geophysical Research Letters 41:5139-5147 Titmarsh L (2007) Tandora: A Pioneer's Dream. Jinglestix, Toowoomba Torrence C, Compo GP (1998) A practical guide to wavelet analysis. Bulletin of the American Meteorological Society 79:61-78 Toth LT, Aronson RB, Vollmer SV, Hobbs JW, Urrego DH, Cheng H, Enochs IC, Combosch DJ, van Woesik R, Macintyre IG (2012) ENSO Drove 2500-Year Collapse of Eastern Pacific Coral Reefs. Science 337:81-84 van Hooidonk R, Maynard JA, Planes S (2013) Temporary refugia for coral reefs in a warming world. Nature Clim Change 3:508-511 Vance TR, van Ommen TD, Curran MAJ, Plummer CT, Moy AD (2013) A Millennial Proxy Record of ENSO and Eastern Australian Rainfall from the Law Dome Ice Core, East Antarctica. Journal of Climate 26:710-725 Vance TR, Roberts JL, Plummer CT, Kiem AS, van Ommen TD (2015) Interdecadal Pacific variability and eastern Australian megadroughts over the last millennium. Geophysical Research Letters 42:129-137 Veron J (2008) A reef in time: the Great Barrier Reef from beginning to end. Belknap Press of Harvard University Press, Cambridge, Massachusetts Waterhouse J, Brodie J, Lewis S, Mitchell A (2012) Quantifying the sources of pollutants in the Great Barrier Reef catchments and the relative risk to reef ecosystems. Marine Pollution Bulletin 65:394-406 Winkler NS, Pandolfi JM, Sampayo EM (2015) Symbiodinium identity alters the temperature- dependent settlement behaviour of Acropora millepora coral larvae before the onset of symbiosis

108

Chapter 5 Wooldridge S, Brodie J, Furnas M (2006) Exposure of inner-shelf reefs to nutrient enriched runoff entering the Great Barrier Reef Lagoon: Post-European changes and the design of water quality targets. Marine Pollution Bulletin 52:1467-1479 WRI (2011) Reefs at risk revisited. In: Institute WR (ed). World Resources Institute, Washington DC Yamano H, Sugihara K, Nomura K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophysical Research Letters 38 Yeh S-W, Kang S-K, Kirtman B, Kim J-H, Kwon M-H, Kim C-H (2010) Decadal change in relationship between western North Pacific tropical cyclone frequency and the tropical Pacific SST. Meteorol Atmos Phys 106:179-189 Zann M (2012) The Use of Remote Sensing and Field Validation for Mapping Coral Communities of Hervey Bay and the Great Sandy Strait and Implications for Coastal Planning Policy. M Phil thesis, University of Queensland, St Lucia, p216

109

Chapter 5 Tables

Distance Distance from from nearest Depth m mainland river Fetch to Number Reef Area (ha) (HAT) (km) (km) SE (km) cores Big Woody Fringing 5 4 18 13 8 Pialba Fringing 5 0.7 24 1 3 Pt. Vernon West Fringing 5 0.4 30 0.3 3 Four Mile 2 10 5 70 50 4

Table 2 List of coral samples taken from cores for U-Series (Th) dating from four coral reefs of Hervey Bay, Queensland, Australia.

Core Year Error Sample Name Depth Location (AD) +/- Species HB_BW_12_PC01_0-9 0 Big Woody Reef 1606 5 Acropora HB_BW_12_PC01_30-34 30 Big Woody Reef 899 5 Turb HB_BW_12_PC01_60-64 60 Big Woody Reef 493 6 Platygyra HB_BW_12_PC01_90-94 90 Big Woody Reef 467 8 Acropora HB_BW_12_PC01_175-179 175 Big Woody Reef -679 13 Alveopora HB_BW_12_PC01_290-294 290 Big Woody Reef -3458 31 Unknown HB_BW_12_PC02_0-4 0 Big Woody Reef 2010 2 Acropora HB_BW_12_PC02_50-54 50 Big Woody Reef 1177 4 Acropora HB_BW_12_PC02_100-104 100 Big Woody Reef 1109 5 Acropora HB_BW_12_PC02_200-204 200 Big Woody Reef 1061 7 Acropora HB_BW_12_PC02_250-254 250 Big Woody Reef 847 5 Acropora HB_BW_12_PC02_290-294 290 Big Woody Reef -125 8 Acropora HB_BW_12_PC03_0-4 0 Big Woody Reef 1081 7 Acropora HB_BW_12_PC03_55-59 55 Big Woody Reef 1049 7 Acropora HB_BW_12_PC03_70-74 70 Big Woody Reef 1034 5 Acropora HB_BW_12_PC03_125-129 125 Big Woody Reef 828 8 Acropora HB_BW_12_PC03_160-164 160 Big Woody Reef 536 6 Turbinaria HB_BW_12_PC03_185-189 185 Big Woody Reef 449 8 Acropora HB_BW_12_PC03_290-294 290 Big Woody Reef 13 8 Acropora HB_BW_12_PC03_340-344 340 Big Woody Reef -335 14 Acropora HB_BW_12_PC04_0-4 0 Big Woody Reef -652 12 Acropora HB_BW_12_PC04_50-54 50 Big Woody Reef -1067 11 Acropora HB_BW_12_PC04_90-94 90 Big Woody Reef -1094 11 Acropora HB_BW_12_PC04_95-99 95 Big Woody Reef -1066 16 Acropora HB_BW_12_PC04_140-144 140 Big Woody Reef -1714 16 Goniopora HB_BW_12_PC04_160-164 160 Big Woody Reef -1740 12 Goniopora HB_BW_12_PC04_185-189 185 Big Woody Reef -2442 15 Acropora HB_BW_12_PC04_225-229 225 Big Woody Reef -3093 11 Turbinaria HB_BW_12_PC04_250-254 250 Big Woody Reef -4323 24 Goniopora 110

Chapter 5

HB_BW_12_PC06_0-4 0 Big Woody Reef 1788 4 Acropora HB_BW_12_PC06_120-124 120 Big Woody Reef 1090 10 Acropora HB_BW_12_PC06_140-44 140 Big Woody Reef 1008 5 Cyphastrea HB_BW_12_PC06_180-184 180 Big Woody Reef 1026 5 Cyphastrea HB_BW_12_PC06_220-224 220 Big Woody Reef 494 7 Acropora HB_BW_12_PC06_245-249 245 Big Woody Reef 41 7 Pocillopora HB_BW_12_PC06_350-354 350 Big Woody Reef -1078 11 Acropora HB_BW_11_PCT1_10-15 10 Big Woody Reef 824 9 Acropora HB_BW_11_PCT1_75-80 75 Big Woody Reef 447 12 Goniopora HB_BW_11_PCT1_120-125 120 Big Woody Reef 444 10 Goniopora HB_BW_11_PCT1_135_139_rpt 135 Big Woody Reef 260 9 Goniopora HB_BW_11_PCT1_140_145 140 Big Woody Reef 207 14 Goniopora HB_BW_11_PCT2_0-5 0 Big Woody Reef 333 35 Acropora HB_BW_11_PCT2_50-55 50 Big Woody Reef -3938 20 Acropora HB_BW_11_PCT2_60-64 60 Big Woody Reef -4110 23 Acropora HB_BW_11_PCT2_110-115 110 Big Woody Reef -4412 17 Acropora HB_BW_11_PCT2_115-119 115 Big Woody Reef -4531 33 Unrecognizable

HB_P_12_PC01_0 -9 0 Pialba Reef 1992 3 Goniopora HB_P_12_PC01_25-29 25 Pialba Reef 857 6 Acropora HB_P_12_PC01_35-39 35 Pialba Reef 864 7 Acropora HB_P_12_PC01_60-64 60 Pialba Reef 203 8 Acropora HB_P_12_PC08_0-4 0 Pialba Reef -1193 16 Acropora HB_P_12_PC08_35-39 35 Pialba Reef -1108 16 Acropora HB_P_12_PC08_95-99 95 Pialba Reef -2362 19 Acropora HB_P_12_PC08_110-114 110 Pialba Reef -2886 21 Acropora HB_P_12_PC09_0-4 0 Pialba Reef 1527 5 Acropora HB_P_12_PC09_45-49 45 Pialba Reef -2091 14 Acropora HB_P_12_PC09_65-69 65 Pialba Reef -2319 18 Acropora HB_P_12_PC09_95-99 95 Pialba Reef -2325 15 Acropora

HB_4M_13_PC02_0 -9 0 Four Mile Reef 2010 2 Pocillopora HB_4M_13_PC02_0-9_rpt 0 Four Mile Reef 1856 5 Acropora HB_4M_13_PC02_20-24 20 Four Mile Reef 1863 5 Acropora HB_4M_13_PC02_55-59 55 Four Mile Reef 1835 2 Acropora HB_4M_12_PC02_85-89 85 Four Mile Reef 1068 4 Acropora HB_4M_13_PC02_110-114 110 Four Mile Reef 1030 6 Acropora HB_4M_13_PC03_0-4 0 Four Mile Reef 2002 2 Pocillopora HB_4M_13_PC03_0-4_rpt 0 Four Mile Reef 1845 2 Acropora HB_4M_13_PC03_25-29 25 Four Mile Reef 1997 2 Pocillopora HB_4M_13_PC03_35-39 35 Four Mile Reef 1841 2 Acropora HB_4M_13_PC03_65-69 65 Four Mile Reef 1997 3 Pocillopora HB_4M_13_PC03_80-84 80 Four Mile Reef 1042 6 Acropora HB_4M_13_PC03_100-104 100 Four Mile Reef 1026 5 Acropora HB_4M_12_PC03_165-169 165 Four Mile Reef 996 6 Acropora HB_4M_13_PC03_200-204 200 Four Mile Reef 939 6 Acropora HB_4M_13_PC03_215-219 215 Four Mile Reef 942 8 Acropora HB_4M_13_PC03_300-304 300 Four Mile Reef 911 5 Acropora HB_4M_13_PC03_350-354 350 Four Mile Reef 876 21 Acropora HB_4M_13_PC05_0-4 0 Four Mile Reef 2008 2 Pocillopora HB_4M_13_PC05_45-49 45 Four Mile Reef 1969 3 Pocillopora HB_4M_13_PC05_50-54 50 Four Mile Reef 1218 9 Acropora HB_4M_13_PC05_100-104 100 Four Mile Reef 1172 9 Acropora HB_4M_12_PC05_150-154 150 Four Mile Reef 1077 5 Acropora HB_4M_13_PC05_200-204 200 Four Mile Reef 988 33 Acropora

111

Chapter 5

HB_4M_13_PC04_0-4 0 Four Mile Reef 2001 9 Pocillopora HB_4M_13_PC04_30-34 30 Four Mile Reef 1996 4 Pocillopora HB_4M_13_PC04_55-59 55 Four Mile Reef 1214 21 Acropora HB_4M_13_PC04_80-84 80 Four Mile Reef 1082 4 Acropora HB_4M_13_PC04_105-109 105 Four Mile Reef 1038 22 Acropora HB_4M_13_PC04_200-204 200 Four Mile Reef 1021 29 Acropora HB_4M_13_PC04_285-289 285 Four Mile Reef 947 6 Acropora HB_4M_13_PC04_305-309 305 Four Mile Reef 930 5 Acropora HB_4M_13_PC04_395-399 395 Four Mile Reef 893 5 Acropora

HB_PV_12_PC04_0 -4 0 Pt. Vernon Reef 1954 16 Goniopora HB_PV_12_PC04_10-14 10 Pt. Vernon Reef 1968 13 Goniopora HB_PV_12_PC09_0-9 0 Pt. Vernon Reef 1994 5 Goniopora HB_PV_12_PC09_20-24 20 Pt. Vernon Reef 1567 4 Acropora HB_PV_12_PC09_50-54 50 Pt. Vernon Reef -744 14 Turbinaria

Table 3 Ages of death assemblages at Pt. Vernon West, Pialba and Big Woody reefs from Hervey Bay, Queensland, Australia.

Reef Genus U-Th (AD) error Point Vernon West Goniopora 1989.2 6.7 Goniopora 1988.5 6.5 Goniopora 2000.7 4.3 Goniopora 1978.5 8.8 Goniopora 2003.7 2.2 Goniopora 1938.6 12.3 Goniopora 1991.5 5.2 Goniopora 1993.8 3.7 Goniopora 1994.2 4.5

Pialba Acropora 1519.0 4.5 Acropora 1517.5 3.6 Acropora -1173.8 8.8 Acropora -1163.1 9.9 Acropora -995.1 8.9 Acropora 852.7 6.6 Acropora -2147.9 15.4 Acropora -2061.3 10.2 Acropora -1992.2 9.9

Big Woody Goniopora 1924.0 13.1 Goniopora 1978.5 6.8 Goniopora 530.7 9.7 Goniopora 1979.1 6.0 Turbinaria 1980.8 3.6 Goniopora 1990.2 4.3 Turbinaria 2002.7 2.0 Goniopora 1994.8 2.9 Goniopora 1990.8 4.5 112

Chapter 5

Table 4 List of genera present in reef matrix cores of four coral communities of Hervey Bay, Queensland, Australia.

Pt. Big Four Vernon Genus Woody Pialba Mile West Acropora + + + + Culicia + + + + Goniopora + + + Turbinaria + + + Pocillopora + + + Montipora + + + Cyphastrea + + Psammocora + + Tubastrea + + Euphyllia + Playtgyra + Goniastrea + Alveopora +

Source of Variation df MS Pseudo-F P El Niño Frequency (High, Med, Low) 2 1894 1.2744 ns Distance Mainland (Near, Far) 1 3595.5 2.4192 0.05 Distance Mainland X El Niño Frequency 2 13665 9.1945 0.001 Error 620 1486.2 - - ns=not significant (P>0.05)

113

Chapter 5 Table 6 Permutational analysis of variance (PERMANOVA) for coral community composition at genus level in core subsections with factors for SST (high, medium, low) and for distance from mainland (near, far) for the reefs of Hervey Bay, Queensland, Australia.

Source of Variation df MS Pseudo-F P SST (High, Med, Low) 2 13146 8.9973 0.001 Distance Mainland (Near, Far) 1 11075 7.5797 0.001 Distance Mainland X SST 2 8410.4 5.756 0.001 Error 620 1461.1 - - ns=not significant (P>0.05)

114

Chapter 5 Figures

Fig. 1 Locations of coral reef and coring sites in Hervey Bay, Queensland, Australia.

115

Chapter 5 Fig. 2 Locations of cores on: (a) Big Woody Reef , (b) Pialba Reef , (c) Pt. Vernon West Reef and (d) Four Mile Reef from Hervey Bay, Queensland, Australia. a ` b

c d

116

Chapter 5 Fig. 3 Typical coral assemblages for: (a) Pt. Vernon West Reef, (b) Pialba Reef, (c) Big Woody Reef: thick encrusting Acropora, (d) Big Woody Reef: Goniopora community and (e) Four Mile Reef in Hervey Bay, Queensland, Australia. (Photo c courtesy of Brigitte Sommer) a b

c d

117

Chapter 5 Fig. 4 Life assemblages (2011) and death assemblages from (a) Pt. Vernon West Reef , (b) Pialba Reef, (c) Big Woody Reef and (d) Four Mile Reef in Hervey Bay, Queensland, Australia.

118

Chapter 5 Fig. 5 Plot of ages of all U-Th aged samples from cores versus paleo water depth from reefs in Hervey Bay, Queensland, Australia. (a) all four reefs, includes accretion trend lines for cores (b) Recent 1000 years for Four Mile Reef samples only. Shows El Niño (in brown) and La Niña (in blue) epochs (Vance et al. 2015).

119

Chapter 5 Fig. 6 Core composition diagrams showing percentage coral (4 mm+), relative abundance of coral genera, sediment facies and locations of U-Series samples and ages for Pt. Vernon West Reef, Hervey Bay, Queensland, Australia. Core depth is uncompressed.

120

Chapter 5 Fig. 7 Core composition diagrams showing percentage coral (4 mm+), relative abundance of coral genera, sediment facies and locations of U-Series samples and ages for Pialba Reef, Hervey Bay, Queensland, Australia. Core depth is uncompressed.

121

Chapter 5 Fig. 8 Core composition diagrams showing percentage coral (4 mm+), relative abundance of coral genera, sediment facies and locations of U-Series samples and ages for Big Woody Reef, Hervey Bay, Queensland, Australia. Core depth is uncompressed.

122

Chapter 5 Fig. 9 Core composition diagrams showing percentage coral (4 mm+), relative abundance of coral genera, sediment facies and locations of U-Series samples and ages for Four Mile Reef, Hervey Bay, Queensland, Australia. Core depth is uncompressed.

123

Chapter 5 Fig. 10 Frequency of El Niño events with core sediment type from coral reefs from Hervey Bay, Queensland, Australia.

Fig. 11 Percent total coral (4 mm+) in core subsections relative to sediment type from coral reefs in Hervey Bay, Queensland, Australia.

124

Chapter 5 Fig. 12 Regression of percent total coral in core subsections versus frequency of El Niño events for (a) overall reefs and (b) nearshore versus offshore reefs of Hervey Bay, Queensland, Australia. El Niño frequency data from Moy et al. (2002).

125

Chapter 5 Fig. 13 Regression of percent total coral in core subsections versus frequency of SST at nearshore and offshore reefs of Hervey Bay, Queensland, Australia. SST data from Stott et al.(2004).

126

Chapter 5 Fig. 14 Relative abundance of hard coral genera within sediment types in cores from coral reefs in Hervey Bay, Queensland, Australia.

127

Chapter 5 Fig. 16 Reef coral composition through cores with respect to high, medium and low frequency of El Niño events for (a) nearshore reefs (Pialba and Pt. Vernon West) and (b) offshore reefs (Big Woody and Four Mile) in Hervey Bay, Queensland, Australia. El Niño frequency categories derived from data from Moy et al. (2002).

128

Chapter 5 Fig. 17 Reef coral composition through cores with respect to high (>29.26 o C), medium (29.00 – 29.26 o C), and low (< 29.00 o C) SST categories for (a) nearshore reefs (Pialba, Pt. and Vernon West) and (b) offshore reefs (Big Woody and Four Mile) in Hervey Bay, Queensland, Australia. SST categories derived from data from Stott et al. (2004).

129

Chapter 5 Fig. 18 Average relative abundance of coral genera over time for all coral reef cores combined from Hervey Bay, Queensland, Australia with indications of dates for sea level (SL) instability or rise. Coloured lines to the right represent cores for which the relative abundance was calculated for a given century: Big Woody Reef (BWPC), Four Mile Reef (4MPC), Pialba Reef (PPC), Pt. Vernon West Reef (PVPC). Year 2011 AD represents the modern overall relative abundance of hard coral genera at the cored reefs measured in that year and not averaged into a century.

130

Chapter 5 Fig. 19 Continuous wavelet (Morlet) transform analysis of (a) average percent relative abundance (by century) of Acropora in Hervey Bay, Queensland, Australia (b) frequency of El Niño events per century (Moy et al. 2002). Cone of influence shows area where edge effects may alter the strength of the correlation. a

131

Chapter 5 Fig. 20 Autocorrellogram showing the results of autocorrelation analysis of average relative abundance (by century) of Acropora from coral reefs in Hervey Bay, Queensland, Australia.

132

Chapter 5 Supplementary information

Choice of specific coring locations

In the case of Pt. Vernon West, Pialba and Big Woody reefs, individual coring locations were chosen from satellite images to ensure wide spatial coverage of the reefs. The locations of the Four Mile Reef cores were chosen by first mapping the dimensions of the reef using the depth sounder of the research vessel. Four coring locations were chosen so that they were well distributed over the full extents of the shallowest portions of the reef (~10 m HAT). All coring took place in the immediate vicinity of extensive living coral. Prior to coring, the research vessel was anchored so that the stern of the vessel was directly above the desired GPS coordinate. The core was transported to, or lowered at, that location and the exact coring location chosen based on best estimate of the centre of the stern of the boat above. In some cases, the location was altered by up to several metres to: ensure diver safety; because it was too difficult to insert a core; or, to prevent extensive damage to large foliose corals, in which case the cores were inserted immediately adjacent to the colony.

Reef matrix coring methodology

Coring was carried out through the insertion of a 6.5 m length, 100 mm diameter aluminium pipe with the use of a collar and slide hammer. The pipe was hammered in as far as possible, either encountering an impenetrable layer or else the pipe was entirely inserted. As a result of the difficulty in obtaining cores through the thick portion of Four Mile Reef, which was very consolidated and prevented insertion, only one core was obtained from it. Three cores were obtained from the softer rubble zone immediately adjacent to the thick portions of the reef. A tape measure was used to measure the depth of the sediment surface within the pipe and outside of the pipe relative to the top of the pipe in order to determine compression that resulted from the insertion of the pipe. The top of the pipe was then sealed so that the core material would not slide out during removal of the pipe, which, in most cases, required the aid of a high-lift jack. Once the pipe was removed completely, a cap was placed over the bottom end of the pipe to retain the core material. Once removed from the water, the cores were cut into <1.8 m lengths for easy transport to the Marine Palaeoecology Lab located at The University of Queensland, Brisbane.

133

Chapter 5

Supplementary figures

Supplementary Fig. 1 Plot of all U-Th ages for all samples from cores for the cored coral reefs of Hervey Bay, Queensland, Australia. Accretion trend lines join samples.

134

Chapter 6 Chapter 6: Concluding remarks

Cyclic environmental change affects all organisms, from daily variations in solar, lunar and tidally influenced activity (Bos and Gumanao 2012; Bijoux et al. 2013) and circadian rhythms (Paranjpe and Sharma 2005) to seasonal and annual cycles (Longhurst 1995; Naylor 2010). Longer chronological cycles, such as the El Niño Southern Oscillation (ENSO) (Wooster 1959) and Pacific Decadal Oscillation (MacDonald and Case 2005), can vary at decadal scales (Sun and Yu 2009) or longer (Vance et al. 2013), and affect organisms ranging from mollusks (Carstensen et al. 2010) to mammals (Dunham et al. 2011). There is also increasing physical evidence for longer term millennial scale climate cycles, such as Bond cycles (Bond et al. 1997), and oceanic tidal (Keeling and Whorf 2000) and thermohaline cycles (Debret et al. 2007), though there has been little evidence until now of their ecosystem impacts. Finally, there are multi-millennial scale cycles, with cosmic connections (Öpik 1965), such as glacial cycles (Forbes 1931; Crowley et al. 2015) and Milankovitch cycles (Kerr 1987) for which there is fossil evidence of ecological impact, including extinctions (Bennett 1990; Haynes 2013).

Like all organisms, scleractinian corals are also subject to these cycles. There are many examples where corals are subject to short-term cycles such as daily activity (Sebens and DeRiemer 1977) or lunar and annual reproductive and spawning cycles (Babcock et al. 1986; Baird et al. 2009). There are also indications that corals may be subject to longer term cycles, such as the decadal changes in sea temperatures and rainfall associated with ENSO (Gischler et al. 2009). While episodic growth of corals has been previously proposed as occurring at the millennial scale (Smithers et al. 2006; Lybolt et al. 2011), prior to this study, there has been little or no evidence for scleractinian corals being subject to long term regular cycles at a centennial or millennial scale.

The purpose of this thesis was to examine natural range of variability of high latitude coral communities at different spatial and temporal scales and then assess the likely natural or anthropogenic drivers of this variability. The importance of terrestrial runoff and its relationship with climatic factors such as ENSO became apparent with the significant impacts of flooding on coral communities through changes in total abundance, community structure and changes in relative abundance of traits. Through the innovative use of a combination of cutting edge, high-precision U- Th geochronology and palaeoecology, I found centennial scale correlations of coral community structure with SST and ENSO, as well as millennial scale cyclic changes which may be related to even longer term ENSO linked epochs. 135

Chapter 6

El Niño Southern Oscillation, SST and sea-level

At decadal scales, ENSO can play a major role in the distribution and abundance of corals. In Queensland, for example, periods of La Niña typically result in increased storm activity and rain, with associated increases in the frequency of floods (BOM 2012). This, in turn, results in increased terrestrial runoff and increased submarine groundwater discharge, which exposes corals to prolonged episodes of hyposalinity, elevated sedimentation, increased resuspension, elevated turbidity and elevated nutrient levels, as has been shown in this study (Butler et al. 2015). These stressors have wide ranging negative impacts on coral reefs, including direct mortality (Jokiel et al. 1993; Ayling and Ayling 1998; Butler et al. 2013; Jones and Berkelmans 2014), increased morbidity (Erftemeijer et al. 2012; Pollock et al. 2014; Sheridan et al. 2014), and reduced reproduction, larval success and recruitment (Harrington et al. 2004; Fabricius 2005; Risk and Edinger 2011; Risk 2014). As shown in this thesis, mortality of coral can be very high during La Niña periods (Butler et al. 2013; Butler et al. 2015), resulting in changes to both species and trait composition in coral communities (Chapter 4). While we found that hyposalinity was likely a major driver of mortality, especially through flooding (Butler et al. 2015), there were other factors, such as sedimentation and turbidity, which drove coral community assembly, and this was shown through changes in species and traits relative to terrestrial and riverine exposure (Chapter 4).

In contrast, El Niño years in Queensland generally result in reduced rainfall and increased drought conditions. As a result, transport of freshwater, sediment and nutrients to marine waters is reduced, resulting in generally clear waters, with greater light penetration. Though El Niño periods may increase the likelihood of bleaching on high-latitude reefs, they may also play an important role in post-disturbance recovery, as shown by historical post-disturbance recovery in Hervey Bay (Butler et al. 2013) and in the Keppel Islands (Jones and Berkelmans 2014) over the course of the largely ENSO driven Millennium Drought (Cai et al. 2014).

This study has also found that ENSO plays a significant role in the distribution and abundance of coral reefs over much longer temporal scales. Impacts of ENSO at these scales have only recently been detected for coral reefs (Lybolt et al. 2011; Toth et al. 2012). Here, we find that not only did coral abundances vary with El Niño frequency, but that changes in relative abundance were cyclic at a millennial scale (Chapter 5). During low-rainfall, high-frequency El Niño periods, coral abundance increased, as did relative abundance of Acropora at offshore areas. During the high- 136

Chapter 6 rainfall, low-frequency El Niño periods (i.e. La Niña periods), coral abundance was lower and offshore coral communities were dominated by species (generally stress tolerant) other than Acropora. While we found the ~1600 year periodicity of changes in relative abundance of coral consistent with a cyclic periodicity in ENSO frequency (Chapter 5), there are other cycles related to earth’s rotation and lunar and solar activity which also have a similar periodicity and may also play a global role through changes in sea temperatures, climate and sea-level, including: Dansgaard- Oeschger (Pisias et al. 2010; Petersen et al. 2013) and Bond cycles (~1470-1600 years) (Bond et al. 1997), thermohaline circulation cycles (~1500 – 1600 years) (Debret et al. 2007) and oceanic tidal cycles (~1800 years) (Keeling and Whorf 2000). Sea level change, ocean temperature and climate are enmeshed (Meier et al. 2007; Camoin and Webster 2015) and collectively, they can affect morphology (Hongo and Kayanne 2011) and distribution of coral species (Veron 2000; Yamano et al. 2011) and this has been apparent along the east coast of Australia (Harriott and Banks 2002; Sommer et al. 2014). This study reveals that small changes in either sea-level (< 0.5 m) or temperature (< 0.07o C) are associated with substantial changes in coral reef community structure (Chapter 5). In the future, changes in ocean temperatures and sea level are predicted to be substantial (Collins et al. 2013) and, as a result, coral communities are likely to change dramatically.

Anthropogenic effects

Anthropogenic driven stressors such as terrestrial runoff (Williams et al. 2003; Jupiter et al. 2008; Brodie et al. 2012), overfishing (Knowlton and Jackson 2008; Valdivia-Acosta 2014) and direct physical damage (Hannak et al. 2011; Sarmento et al. 2011) are considered to have a major impact on coral reefs and are of increasing concern with climate change (Hughes et al. 2003; Hughes 2008; Hoegh-Guldberg 2011; Pandolfi et al. 2011). One of the major stressors to inshore reefs worldwide is terrestrial runoff, and this is exemplified by the Mary River which empties into Hervey Bay. Like many of the rivers along the east coast of Queensland (Kroon et al. 2012), the Mary River, is a highly modified river (Johnson 1996) which transports highly elevated levels of sediments and nutrients into Hervey Bay (Kroon et al. 2012; Butler et al. 2015). Riparian vegetation is still cleared from this catchment at rates that exceed other catchments in Queensland (Reefplan 2010) and the river has in the last century become very restricted to ships as a result of siltation (Matthews 1995; Titmarsh 2007). The historical (Preen 1996; FRC 2007) and recent (Butler et al. 2013; Butler et al. 2015) effects of flooding on Hervey Bay marine habitats indicate the potential for this river, like many other rivers worldwide, to significantly and adversely affect downstream marine

137

Chapter 6 environments. Worldwide, modifications to catchments have resulted in substantial changes to freshwater, sediment and nutrient run-off, for example in Florida (Hudson et al. 1994), Hawaii (Prouty et al. 2010), Indonesia (Marion et al. 2005) as well as Australia (Lewis et al. 2007; McCulloch et al. 2003). While anthropogenic driven changes to the Mary River catchment could not be directly implicated in changes to Hervey Bay reefs by these studies, palaeoecological research elsewhere in Queensland has found that changes to other catchments such as the Burdekin River (Roff et al. 2013) and the Brisbane River (Lybolt et al. 2011) have resulted in significant changes to coral communities. Catchment and land managers both in Queensland and worldwide should take heed of the growing body of evidence for the need to improve the quality of catchments to minimise degradation to downstream habitats.

Refugia in southern Queensland

The importance of high-latitude refugia to organisms such as corals will increase as the climate changes, the oceans warm and their distribution ranges change (Beger et al. 2011; Freeman 2015; Makino et al. 2014). A number of criteria have been proposed for assessing the potential of coral reefs as refugia based on modern state (e.g. species richness, coral abundance and average daily temperature (Jones and Berkelmans 2010)) and based on historical state (e.g. persistence of coral and ecological stability (Lybolt et al. 2011)). Research by ourselves (Chapter 5) and others in southern Queensland (Jones and Berkelmans 2010), indicates that this region may offer suitable refuge for corals in a warming climate. The importance of the southern GBR and those reefs further south as a potential for long term refuge under climate change has been highlighted frequently (Lybolt et al. 2011; van Hooidonk et al. 2013; Beger et al. 2014) and reefs such as those in the Keppel Islands and those of Hervey Bay should be added to the list of likely candidates for enhanced protection into the future.

Implications for catchment and marine park management:

In order to effectively manage marine protected areas, managers need up to date information about the condition of their managed areas and the potential stressors. This thesis reveals some important information for managers of catchments and marine protected areas, particularly those in the Hervey Bay region.

138

Chapter 6 Our data indicate the importance of ENSO cycles and terrestrial runoff to the temporal and spatial abundance of corals in Hervey Bay. Coral communities have varied substantially over the millennia, sensitive to changes in natural environmental conditions. In order to persist, coral communities must have been resilient to these environmental changes, which would have included acute disturbance events resulting in high mortality. Flooding from the coastal rivers is a common occurrence in Hervey Bay and reefs can suffer high mortality as a result of these floods (Butler et al. 2013; Butler et al. 2015). The Mary and Burnett rivers are a major source of freshwater, sediment and nutrients to Hervey Bay (BPA 1989; Kroon et al. 2012). Increasing effort should be made to minimise the transport of these by improving gully and bank stability and increasing, rather than decreasing, riparian vegetation. Worldwide, such efforts to mitigate terrestrial impacts are showing real potential for improvements to coastal marine environments (Kroon et al. 2014). The maintenance of more natural conditions of erosion and sediment and nutrient transport will allow the continuation of the natural cycles of change. This will have downstream benefits through reduced transport of floodwaters, sediments and nutrients to not only the coral reefs, but to other downstream habitats, such as the internationally significant RAMSAR wetlands in Great Sandy Strait and the large expanse of seagrasses in Hervey Bay which collectively make up the diverse ecosystem of Hervey Bay. As a way of monitoring the changes in the catchment, water quality testing of Hervey Bay waters should take place on a regular basis, ideally automated, and at a much more frequent interval than the monthly testing taking place now (Butler et al. 2013, 2015)

Best practice for marine protected areas often includes the desirability for representative areas to be included at high levels of protection (Fernandes et al. 2005). Post-disturbance, these areas act as a source of recruits for recovery to adjacent areas. The potentially high impacts of flooding and flooding frequency have ramifications for choosing locations for marine protected areas in order to maintain the quality of the marine communities to maximise benefits to those areas adjacent to them. As a result of repeated flooding in 2013, there was extensive (~99%) coral mortality on reefs located in Marine National Park, the no-take areas of Hervey Bay/Great Sandy Marine Park (Butler unpublished), while other reefs nearby (with reduced zonal protection) still had substantial living coral cover (e.g. Big Woody Reef outside green zone (Butler et al. 2013; Butler et al. 2015)). Protection of lower risk communities, assuming they have adequate diversity and abundance, could assist with better overall recovery outcomes (Game et al. 2008). Marine protected area zoning in Great Sandy Marine Park should be improved so that more protection is afforded to reefs which are able to maintain populations of coral, despite disturbance, so that post-disturbance communities have the best opportunity for recovery and persistence. Local research has shown that protected areas harbour greater abundances and size of herbivorous fish (Martin et al. 2015) which graze on 139

Chapter 6 algae, thereby promoting recruitment and survival of corals (Adam et al. 2011). Big Woody Reef stands out as one reef that requires protection for the full reef area. It has a long uninterrupted history (~6500 years) of coral presence and is located in such a way as to be able to provide larvae southward, to reefs in Great Sand Strait, westward to reefs along the Hervey Bay (city) foreshore and northward to reefs along the Woongarra coastline. Also, given the high rates of flood mortality (Butler et al. 2015) and in order to maintain international best practices (Fernandes et al. 2005), increased percentages of Hervey Bay coral reefs should be afforded further protection so that it is in-line with, for example, the GBR at ~33% no-take zones.

Future research

This study suggests some pathways for future research in Hervey Bay and other high latitude reefs. With the predicted impacts that will inevitably arise from climate change, it is more relevant than ever to further research on coral reefs in higher latitude areas such as Hervey Bay, especially where there is potential for refugia.

Recruitment is a basic requirement for recovery after disturbance (Pratchett et al. 2011) and this recruitment is dependent on a reliable source of recruits, whether sexually or asexually derived. There are large gaps in our basic knowledge of reproduction and recruitment in Hervey Bay coral communities. Recruitment in these turbid waters is a mystery – we do not know when spawning takes place, when recruitment takes place or where larvae come from. The impacts of terrestrial run-off and flooding on reproduction and recruitment are unknown for this area, especially with regard to the effects of sedimentation and the availability of suitable places for settlement. Also, there are clear spatial differences in the distribution of recruitment/reproductive traits, such as hermaphrodites versus gonochores or species which have horizontal versus vertical transfer of Symbiodinium, which are not yet understood. This area would benefit from a detailed examination of genetic composition of not only coral species, to understand the connectivity among reefs, but of Symbiodinium to understand their diversity at these higher latitudes.

While some correlations have been made between coral communities and ENSO/SST at the decadal scale (Nakamura et al. 2011), few studies establish long term correlations between coral communities and ENSO (e.g. Toth et al. 2012) or SST, and not with any cyclicity. Further work should be pursued to elucidate the mechanisms of the ~1600 year regular periodicity of coral communities. It would be beneficial to obtain historical proxy data for ENSO and SST much closer 140

Chapter 6 to Hervey Bay as the behaviour of ENSO and SST vary considerably with latitude and longitude. The ENSO and SST data used for most of this study were collected from more tropical areas in Ecuador (Moy et al. 2002) and Indonesia (Stott et al. 2004) and this could be quite different from that of higher latitudes. Although local ENSO data (Pacific Decadal Oscillation data) (Vance et al. 2013; Vance et al. 2015) were examined with regard to coral presence (Chapter 5), the 1000 year time frame of these data, much of which was taken up by the recent hiatus in coral presence, was insufficient for detailed analyses. It will be appropriate to use more local data as this data set is expanded to include earlier periods of the Holocene (Vance pers. com.). More U-Th dating could be carried out to generate a more detailed chronologically correct dataset. Both the hiatus from 1200 – 1835, and the rapid accretion at ~1000AD probably also occurs in other cores and these will become more evident through more detailed examination. Other rapid accretion periods and hiatuses may also become apparent, which will allow for a better understanding of their latitudinal variability. Finally, the increase in U-Th dates will enable a more constrained chronology for attributing anthropogenic drivers to ecological responses in Hervey Bay coral reefs.

Other data from the cores are available for follow-up work, including historical ecology or taxonomy of molluscs. For example, it was noted that bivalves from the family Spondylidae were very common through the cores, attached to coral pieces consistently throughout the ~6500 year history of Hervey Bay. Core sediments were not analysed for detailed grain size or for mineral or chemical composition, all of which could provide additional information about sedimentary and environmental conditions through time. X-ray Fluorescence (XRF) analyses could also assist with sedimentary analyses, especially through ENSO periods. Analyses could also be carried out on coral pieces, particularly of massive type corals like Goniopora which, through isotopic analyses, may provide a proxy for environmental conditions over large portions of the 6500 year history.

The coring methodology should be applied to additional reefs from this latitude, particularly those likely to have a long history – such as around Lady Musgrave and Lady Elliott islands, as well as those reefs south of the GBR and at the northern end of Fraser Island. These reefs have developed well offshore with substantial reef structure and the historical dataset from these potentially long, detailed cores may provide a clearer understanding of climate and latitudinal changes less exposed to the influences of terrestrial exposure.

Information about submarine groundwater discharge for this region has only ever been anecdotal, with occasional remarks about the presence of scattered submerged freshwater outlets known as

141

Chapter 6 “Wonky Holes” (Nowak 2002). This groundwater clearly affects nearshore waters post-flood, but the volume of the discharge and the likely areas affected are unknown, though there are indications that such groundwater discharge has increased recently relative to the mid Holocene and that it may affect coral reefs (Gagan et al. 2002). The source of this groundwater discharge is also unknown and should be investigated to ensure that the quality of the groundwater is maintained at levels suitable to avoid negative impacts to downstream habitats.

Conclusion

The coral reefs of Hervey Bay are a great example of a marine habitat under modern duress, but which have shown unusual persistence through time in comparison with other inshore coral reefs. Through 6.5 millennia, these reefs have persisted through changes in climate, sea-level and temperature, and have done so subject to environmental changes which favour the presence of particular traits that lead to multiple recurring stable communities over millennial scales. Hervey Bay reef communities are currently largely composed of stress tolerant genera and these communities are consistent with the natural range of variability shown in the past. Our research also indicates that SST and ENSO may play a major role in community structure and that exposure to terrestrial runoff may be an important driver of change. Catchments along the east coast of Australia have been highly modified and rates of terrestrial runoff, including sediments, nutrients and pollutants are many times higher than prior to European colonisation of the Queensland coast of Australia. Given the apparent worldwide decline in coral reefs, it is imperative that coral reefs which retain high coral abundances, such as those of Hervey Bay, do not reach a tipping point into an alternate, stable, yet degraded state. Not only do high-latitude coral reefs, especially those on the edge of coral ranges like Hervey Bay, have great potential to inform us about the drivers of coral reef formation and coral communities, they have the potential to be important refuges for coral reefs as ocean temperatures increase and coral reefs migrate to higher latitudes.

142

Chapter 6 References

Adam TC, Schmitt RJ, Holbrook SJ, Brooks AJ, Edmunds PJ, Carpenter RC, Bernardi G (2011) Herbivory, Connectivity, and Ecosystem Resilience: Response of a Coral Reef to a Large- Scale Perturbation." PLoS ONE 6(8): e23717. Ayling AM, Ayling AL (1998) The Effect of the Daintree River Flood Plume On Snapper Island Coral Reefs. Great Barrier Reef Marine Park Authority Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Marine Biology 90:379-394 Baird AH, Guest JR, Willis BL (2009) Systematic and Biogeographical Patterns in the Reproductive Biology of Scleractinian Corals. Annual Review of Ecology, Evolution, and Systematics 40:551-571 Beger M, Sommer B, Harrison PL, Smith SDA, Pandolfi JM (2014) Conserving potential coral reef refuges at high latitudes. Diversity and Distributions 20:245-257 Beger M, Babcock R, Booth DJ, Bucher D, Condie SA, Creese B, Cvitanovic C, Dalton SJ, Harrison P, Hoey A, Jordan A, Loder J, Malcolm H, Purcell SW, Roelfsma C, Sachs P, Smith SDA, Sommer B, Stuart-Smith R, Thomson D, Wallace CC, Zann M, Pandolfi JM (2011) Research challenges to improve the management and conservation of subtropical reefs to tackle climate change threats. Ecological Management & Restoration 12:e7-e10 Bennett KD (1990) Milankovitch Cycles and Their Effects on Species in Ecological and Evolutionary Time. Paleobiology 16:11-21 Bijoux JP, Dagorn L, Gaertner JC, Cowley PD, Robinson J (2013) The influence of natural cycles on coral reef fish movement: implications for underwater visual census (UVC) surveys. Coral Reefs 32:1135-1140 BOM (2012) Record breaking La Nina events: An analysis of the La Nina life cycle and the impacts and significance of the 2010-2011 and 2011-2012 La Nina events in Australia. Australian Bureau of Meteorology, Melbourne 28 Bond G, Showers W, Cheseby M, Lotti R, Almasi P, deMenocal P, Priore P, Cullen H, Hajdas I, Bonani G (1997) A Pervasive Millennial-Scale Cycle in North Atlantic Holocene and Glacial Climates. Science 278:1257-1266 Bos AR, Gumanao GS (2012) The lunar cycle determines availability of coral-reef fishes at fish markets. Journal of Fish Biology 81:2074-2079 BPA (1989) Hervey Bay beaches : a detailed study of coastline behaviour along the mainland beaches of Hervey Bay, South-east Queensland, Australia. Beach Protection Authority, Brisbane 323 Brodie JE, Kroon FJ, Schaffelke B, Wolanski EC, Lewis SE, Devlin MJ, Bohnet IC, Bainbridge ZT, Waterhouse J, Davis AM (2012) Terrestrial pollutant runoff to the Great Barrier Reef: An update of issues, priorities and management responses. Marine Pollution Bulletin 65:81- 100 Butler IR, Sommer B, Zann M, Zhao Jx, Pandolfi JM (2013) The impacts of flooding on the high- latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia. Coral Reefs 32:1149-1163 Butler IR, Sommer B, Zann M, Zhao Jx, Pandolfi J (2015) The cumulative impacts of repeated heavy rainfall, flooding and altered water quality on the high-latitude coral reefs of Hervey Bay, Queensland, Australia. Mar Pollut Bull doi:10.1016/j.marpolbul.2015.04.047 Cai W, Purich A, Cowan T, van Rensch P, Weller E (2014) Did Climate Change–Induced Rainfall Trends Contribute to the Australian Millennium Drought? Journal of Climate 27:3145-3168 Camoin GF, Webster JM (2015) Coral reef response to Quaternary sea-level and environmental changes: State of the science. Sedimentology 62:401-428

143

Chapter 6 Carstensen D, Riascos JM, Heilmayer O, Arntz WE, Laudien J (2010) Recurrent, thermally-induced shifts in species distribution range in the Humboldt current upwelling system. Marine Environmental Research 70:293-299 Collins M, Knutti R, Arblaster J, Dufresne J-L, Fichefet T, Friedlingstein P, Gao X, Gutowski WJ, Johns T, Krinner G, Shongwe M, Tebaldi C, Weaver AJ, Wehner M (2013) Long-term Climate Change: Projections, Commitments and Irreversibility. In: Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change Cambridge University Press, . In: Stocker TF, D. Qin, G.-K. Plattner, M. Tignor, S.K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex and P.M. Midgley (eds.) (ed), Cambridge, United Kingdom and New York, NY, USA. Crowley JW, Katz RF, Huybers P, Langmuir CH, Park S-H (2015) Glacial cycles drive variations in the production of oceanic crust. Science 347:1237-1240 Debret M, Bout-Roumazeilles V, Grousset F, Desmet M, McManus JF, Massei N, Sebag D, Petit JR, Copard Y, Trentesaux A (2007) The origin of the 1500-year climate cycles in Holocene North-Atlantic records. Clim Past 3:569-575 Dunham AE, Erhart EM, Wright PC (2011) Global climate cycles and cyclones: consequences for rainfall patterns and lemur reproduction in southeastern Madagascar. Global Change Biology 17:219-227 Erftemeijer PLA, Riegl B, Hoeksema BW, Todd PA (2012) Environmental impacts of dredging and other sediment disturbances on corals: A review. Marine Pollution Bulletin 64:1737-1765 Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: Review and synthesis. Marine Pollution Bulletin 50:125-146 Fernandes L, Day JON, Lewis A, Slegers S, Kerrigan B, Breen DAN, Cameron D, Jago B, Hall J, Lowe D, Innes J, Tanzer J, Chadwick V, Thompson L, Gorman K, Simmons M, Barnett B, Sampson K, De'Ath G, Mapstone B, Marsh H, Possingham H, Ball IAN, Ward T, Dobbs K, Aumend J, Slater DEB, Stapleton K (2005) Establishing Representative No-Take Areas in the Great Barrier Reef: Large-Scale Implementation of Theory on Marine Protected AreasEstablecimiento de Áreas sin Captura Representativas en la Gran Barrera Arrecifal: Implementación a Gran Escala de la Teoría sobre Áreas Marinas Protegidas. Conservation Biology 19:1733-1744 Freeman, L. A. (2015). Robust Performance of Marginal Pacific Coral Reef Habitats in Future Climate Scenarios. PLoS ONE 10(6): e0128875. Forbes WTM (1931) The Great Glacial Cycle. Science 74:294-295 FRC (2007) Beach Nourishment at Hervey Bay, Assessment and Monitoring of Environmental Impacts (Coral and Seagrass); Report to Hervey Bay City Council. In: Thorogood J, Conacher C, Moore B, Olds A, Thorogood J (eds). FRC Environmental Gagan MK, Ayliffe LK, Opdyke BN, Hopley D, Scott-Gagan H, Cowley J (2002) Coral oxygen isotope evidence for recent groundwater fluxes to the Australian Great Barrier Reef. Geophysical Research Letters 29:43-41-43-44 Game ET, McDonald-Madden EVE, Puotinen ML, Possingham HP (2008) Should We Protect the Strong or the Weak? Risk, Resilience, and the Selection of Marine Protected Areas Debemos Proteger al Fuerte o al Débil? Riesgo, Resiliencia y la Selección de Áreas Marinas Protegidas. Conservation Biology 22:1619-1629 Gischler E, Hudson JH, Storz D (2009) Growth of Pleistocene massive corals in south Florida: low skeletal extension-rates and possible ENSO, decadal, and multi-decadal cyclicities. Coral Reefs 28:823-830 Hannak JS, Kompatscher S, Stachowitsch M, Herler J (2011) Snorkelling and trampling in shallow- water fringing reefs: Risk assessment and proposed management strategy. Journal of Environmental Management 92:2723-2733

144

Chapter 6 Harrington L, Fabricius K, De'ath G, Negri A (2004) Recognition and Selection of Settlement Substrata Determine Post-Settlement Survival in Corals. Ecology 85:3428-3437 Harriott VH, Banks SB (2002) Latitudinal variation in coral communities in eastern Australia: a qualitative biophysical model of factors regulating coral reefs. Coral Reefs 21:83-94 Haynes G (2013) Extinctions in North America’s Late Glacial landscapes. Quaternary International 285:89-98 Hoegh-Guldberg O (2011) The Impact of Climate Change on Coral Reef Ecosystems. In: Dubinsky Z, Stambler N (eds) Coral Reefs: An Ecosystem in Transition. Springer Netherlands, pp391- 403 Hongo C, Kayanne H (2011) Key species of hermatypic coral for reef formation in the northwest Pacific during Holocene sea-level change. Marine Geology 279:162-177 Hudson, JH, Hanson KJ, Halley RB, Kindinger JL (1994) Environmental Implications of Growth Rate Changes in Montastrea Annularis: Biscayne National Park, Florida. Bulletin of Marine Science 54(3): 647-669 Hughes T (2008) Human Impacts on Coral Reefs. In: Hutchings P, Kingsford M, Hoegh-Guldberg O (eds) The Great Barrier Reef: biology, environment and management. CSIRO, Collingwood, Victoria, pp85-94 Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh- Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929-933 Johnson DP (1996) State of the Rivers, Mary River and its tributaries: An Ecological and Physical Assessment of the Condition of Streams in the Mary River Catchment State of the Rivers. Department of Natural Resources, Indooroopilly Jokiel PL, Hunter CL, Taguchi S, Watarai L (1993) Ecological impact of a fresh-water “reef kill” in Kaneohe Bay, Oahu, Hawaii. Coral Reefs 12:177-184 Jones AM, Berkelmans R (2010) Marine refugia in the Keppel region of the Great Barrier Reef. Headmark:19-27 Jones AM, Berkelmans R (2014) Flood Impacts in Keppel Bay, Southern Great Barrier Reef in the Aftermath of Cyclonic Rainfall. PLoS ONE 9:e84739 Jupiter S, Roff G, Marion G, Henderson M, Schrameyer V, McCulloch M, Hoegh-Guldberg O (2008) Linkages between coral assemblages and coral proxies of terrestrial exposure along a cross-shelf gradient on the southern Great Barrier Reef. Coral Reefs 27:887-903 Keeling CD, Whorf TP (2000) The 1,800-year oceanic tidal cycle: a possible cause of rapid climate change. Proceedings of the National Academy of Sciences of the United States of America 97:3814-3819 Kerr RA (1987) Milankovitch Climate Cycles through the Ages. Science 235:973-974 Knowlton N, Jackson JBC (2008) Shifting Baselines, Local Impacts, and Global Change on Coral Reefs. PLoS Biology 6:e54 Kroon FJ, Kuhnert PM, Henderson BL, Wilkinson SN, Kinsey-Henderson A, Abbott B, Brodie JE, Turner RDR (2012) River loads of suspended solids, nitrogen, phosphorus and herbicides delivered to the Great Barrier Reef lagoon. Marine Pollution Bulletin 65(4-9): 167-181. Kroon, FJ, Schaffelke B, Bartley R (2014) Informing policy to protect coastal coral reefs: Insight from a global review of reducing agricultural pollution to coastal ecosystems. Marine Pollution Bulletin 85(1): 33-41. Lewis S E, Shields GA, Kamber BS, Lough JM (2007) A multi-trace element coral record of land- use changes in the Burdekin River catchment, NE Australia. Palaeogeography, Palaeoclimatology, Palaeoecology 246(2-4): 471-487 Longhurst A (1995) Seasonal cycles of pelagic production and consumption. Progress in Oceanography 36:77-167

145

Chapter 6 Lybolt M, Neil D, Zhao J-x, Feng Y-x, Yu K-F, Pandolfi J (2011) Instability in a marginal coral reef: the shift from natural variability to a human-dominated seascape. Frontiers in Ecology and the Environment 9:154-160 McCulloch M, Fallon S, Wyndham T, Hendy E, Lough J, Barnes D (2003) Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. Nature 421(6924): 727-730 MacDonald GM, Case RA (2005) Variations in the Pacific Decadal Oscillation over the past millennium. Geophysical Research Letters 32:n/a-n/a Makino A, Yamano H, Beger M, Klein CJ, Yara Y, Possingham HP (2014) Spatio-temporal marine conservation planning to support high-latitude coral range expansion under climate change. Diversity and Distributions 20:859-871 Marion GS, Dunbar RB, Mucciarone DA, Kremer JN, Lansing JS, Arthawiguna A (2005) Coral skeletal δ15N reveals isotopic traces of an agricultural revolution. Marine Pollution Bulletin 50(9): 931-944 Martin, TSH, Olds AD, Pitt KA, Johnston AB, Butler IR, Maxwell PS, Connolly RM (2015). Effective protection of fish on inshore coral reefs depends on the scale of mangrove-reef connectivity. Marine Ecology Progress Series 527: 157-165 Matthews T (1995) River of dreams: a history of Maryborough and district. Maryborough City Council, Maryborough Meier MF, Dyurgerov MB, Rick UK, O'Neel S, Pfeffer WT, Anderson RS, Anderson SP, Glazovsky AF (2007) Glaciers Dominate Eustatic Sea-Level Rise in the 21st Century. Science 317:1064-1067 Moy CM, Seltzer GO, Rodbell DT, Anderson DM (2002) Variability of El Nino/Southern Oscillation activity at millennial timescales during the Holocene epoch. Nature 420:162-165 Nakamura N, Kayanne H, Iijima H, McClanahan TR, Behera SK, Yamagata T (2011). Footprints of IOD and ENSO in the Kenyan coral record. Geophysical Research Letters 38(24) Naylor E (2010) Chronobiology of Marine Organisms. Cambridge University Press, Cambridge, GBR Nowak R (2002) 'Wonky holes' blamed for coral death New Scientist. Reed Business Information UK, London 5 Öpik EJ (1965) Climatic change in cosmic perspective. Icarus 4:289-307 Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting Coral Reef Futures Under Global Warming and Ocean Acidification. Science (New York, NY) 333:418-422 Paranjpe DA, Sharma VK (2005) Evolution of temporal order in living organisms. Journal of Circadian Rhythms 3:7-7 Petersen SV, Schrag DP, Clark PU (2013) A new mechanism for Dansgaard-Oeschger cycles. Paleoceanography 28:24-30 Pisias NG, Clark PU, Brook EJ (2010) Modes of Global Climate Variability during Marine Isotope Stage 3 (60–26 ka). Journal of Climate 23:1581-1588 Pollock FJ, Lamb JB, Field SN, Heron SF, Schaffelke B, Shedrawi G, Bourne DG, Willis BL (2014) Sediment and Turbidity Associated with Offshore Dredging Increase Coral Disease Prevalence on Nearby Reefs. PLoS ONE 9:e102498 Pratchett MS, Trapon M, Berumen ML, Chong-Seng K (2011) Recent disturbances augment community shifts in coral assemblages in Moorea, French Polynesia. Coral Reefs 30(1): 183-193. Prouty NG, Field ME, Stock JD, Jupiter SD, McCulloch M (2010) Coral Ba/Ca records of sediment input to the fringing reef of the southshore of Moloka’i, Hawai’i over the last several decades. Marine Pollution Bulletin 60(10): 1822-1835 Preen A (1996) Abstract: Unprecedented die-off of seagrass and dugongs in Hervey Bay resulted from Mary River floods and associated cyclone. In: Hunter H, Eyles A, Rayment G (eds) Downstream Effects of Land Use. Department of Natural Resources, Queensland, Brisbane, pp119 146

Chapter 6 Reefplan (2010) Reef Water Quality Protection Plan - Second Report Card 2010, Burnett Mary Region In: Government A (ed) 2 Risk MJ (2014) Assessing the effects of sediments and nutrients on coral reefs. Current Opinion in Environmental Sustainability 7:108-117 Risk MJ, Edinger E (2011) Impacts of Sediment on Coral Reefs. In: Hopley D (ed) Encyclopedia of Modern Coral Reefs. Springer Netherlands, pp575-586 Roff G, Clark T, Reymond-CE, Zhao Jx, Feng Y, McCook L, Done T, Pandolfi J (2013) Palaeoecological evidence of a historical collapse of corals at Pelorus Island, inshore Great Barrier Reef, following European settlement. Proceedings of the Royal Society B 280:20122100 Sarmento VC, Barreto AFS, Santos PJP (2011) The response of meiofauna to human trampling on coral reefs. Sci Mar 75:559-570 Sebens KP, DeRiemer K (1977) Diel cycles of expansion and contraction in coral reef anthozoans. Marine Biology 43:247-256 Sheridan C, Grosjean P, Leblud J, Palmer CV, Kushmaro A, Eeckhaut I (2014) Sedimentation rapidly induces an immune response and depletes energy stores in a hard coral. Coral Reefs 33:1067-1076 Smithers SG, Hopley D, Parnell KE (2006) Fringing and Nearshore Coral Reefs of the Great Barrier Reef: Episodic Holocene Development and Future Prospects. Journal of Coastal Research 22:175-187 Sommer B, Harrison PL, Beger M, Pandolfi JM (2014) Trait-mediated environmental filtering drives assembly at biogeographic transition zones. Ecology 95:1000-1009 Stott L, Cannariato K, Thunell R, Haug GH, et al. (2004) Decline of surface temperature and salinity in the western tropical Pacific Ocean in Holocene epoch. Nature 431:56-59 Sun F, Yu J-Y (2009) A 10–15-Yr Modulation Cycle of ENSO Intensity. Journal of Climate 22:1718-1735 Titmarsh L (2007) Tandora: A Pioneer's Dream. Jinglestix, Toowoomba Toth LT, Aronson RB, Vollmer SV, Hobbs JW, Urrego DH, Cheng H, Enochs IC, Combosch DJ, van Woesik R, Macintyre IG (2012) ENSO Drove 2500-Year Collapse of Eastern Pacific Coral Reefs. Science 337:81-84 Valdivia-Acosta A (2014) Fish assemblages of caribbean coral reefs: Effects of overfishing on coral communities under climate change. Ph.D. Ph.D. thesis, The University of North Carolina at Chapel Hill, p213 van Hooidonk R, Maynard JA, Planes S (2013) Temporary refugia for coral reefs in a warming world. Nature Clim Change 3:508-511 Vance TR, van Ommen TD, Curran MAJ, Plummer CT, Moy AD (2013) A Millennial Proxy Record of ENSO and Eastern Australian Rainfall from the Law Dome Ice Core, East Antarctica. Journal of Climate 26:710-725 Vance TR, Roberts JL, Plummer CT, Kiem AS, van Ommen TD (2015) Interdecadal Pacific variability and eastern Australian megadroughts over the last millennium. Geophysical Research Letters 42:129-137 Veron J (2000) Corals of the World. Australian Institute of Marine Science, Townsville Williams D, Roth C, Reichelt R, Ridd P, Raymet G, Larcombe P, Brodie J, Pearson R, Wilkinson C, Talbot F, Furnas M, Fabricius K, McCook L, Hughes T, Hough Gulberg O, Done T (2003) The current level of scientific understanding on impacts of terrestrial run-off on the Great Barrier Reef World Heritage Area Wooster WS (1959) Oceanographic observations in the Panama Bight, "Askoy" Expedition, 1941. Bulletin of the American Museum of Natural History 118:117 Yamano H, Sugihara K, Nomura K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophysical Research Letters 38

147