Factors Influencing Fish Assemblages of Intermittently Closed and Open Lakes and Lagoons (Icolls) of the Central and Near-South Coasts of New South

Factors influencing fish assemblages of Intermittently Closed and Open Lakes and Lagoons (ICOLLs) of the Central and Near-South Coasts of New South

Wales, Australia

Leslie Milton Edwards BSc, MSc

Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy at The University of Newcastle, Australia August 2013

Statement of Originality

The thesis contains no material which has been accepted for the award of any other degree or diploma in any university or other tertiary institution and, to the best of my knowledge and belief, contains no material previously published or written by another person, except where due reference has been made in the text. I give consent to the final version of my thesis being made available worldwide when deposited in the University’s Digital Repository, subject to the provisions of the Copyright Act 1968.

Signed: ……………………………………………………… (Leslie Milton Edwards)

i Acknowledgements

Acknowledgements Firstly to Professor William Gladstone whose supervision and guidance was invaluable over a long, long period of time, especially during those tough and frustrating periods of explaining statistics. However you were always available and provided inspiration during the duration of this epic thesis. To Dr David Powter who provided support, ideas and fun, as well as assistance in the field. To Dr Tom Trnski you gave invaluable advice and direction as well as aid in identification of fishes during the larval fish study.

The work in this thesis was undertaken over a long period of time and involved the assistance of many people both in the field and in the laboratory, without them this project would not have been possible. Field work was a major part of this project and involved many hours spent travelling and sampling in different and sometimes difficult conditions therefore I wish to thank all those people involved. Those who deserve a special mention are Margaret O’Bryan, Dr David Powter, and Glenn Courtney, Steven ‘Scuppers’ Fartek, Hamlet Giragossyan and Jo Walker. Other people who helped out in the field were Norm Boardman, Jill Clancy, Craig Northrop, David McElroy and Tomas Starke-Peterkovic.

A special mention goes to Tom Savage from the Department of Geosciences, University of Sydney for the loan of their boat and other equipment throughout the study and his invaluable knowledge of sediment collection and for help with the preparation and analysis of sediments for trace metal concentrations. To Malcolm Ricketts in the School of Biological Sciences, University of Sydney, for his patient help and assistance in producing graphics and photos for this thesis, along with assistance in the fieldwork and to Dr Liz May and Mark Ahern for their help in proofing the drafts of this thesis.

To David Bishop in the Department of Chemistry, University of Technology, Sydney I am greatly appreciative of his knowledge, assistance and use of their laboratory for the analysis of trace metals in fishes tissues. Also Gemma Armstrong for her assistance in acquiring chemicals and materials for this analysis. To the staff of the Australian Museum who helped in the identification of polychaete fauna (Anna Murray) and larval and juvenile fishes (Dr Tom Trnski and Sally Reader) and Bruce Gill (University of Sydney, Macleay Museum).

Finally, many thanks go to my partner Margaret and daughter Sara, who have always been encouraging and patient as I strive to reach my goals and to Bonnie (Mum), who did not survive to see me reach this milestone: miss you lots.

ii Table of Contents

Table of Contents Statement of Originality ...... i

Acknowledgements ...... ii

Table of contents...... iii

Abstract ...... ix

List of Tables ...... xii

List of Figures ...... xxii

Chapter 1: Introduction ...... 1

1.1 General Introduction ...... 2

1.2 Classification and definitions of estuaries ...... 2

1.2.1 Intermittently Closed and Open Lakes and Lagoons (ICOLLs) ...... 4

1.3 Estuarine fish assemblages ...... 5

1.3.1 Fish assemblages of NSW ICOLLs ...... 6

1.3.2 Recruitment of larval and juvenile fishes into ICOLLs ...... 6

1.4 Ecology of ICOLLs ...... 7

1.4.1 Physical and water chemistry characteristics ...... 7

1.4.2 Habitats within ICOLLs ...... 9

1.5 Feeding ecology of fishes in ICOLLs ...... 10

1.6 Anthropogenic impacts on ICOLLs ...... 11

1.7 Conclusion ...... 13

1.8 Current study ...... 14

1.9 Aims of study...... 14

1.10 Thesis structure ...... 15

Chapter 2: Study area ...... 16

2.1 Study area ...... 17

2.2 Northern Site-Gosford ...... 17

2.2.1 Climate ...... 17

2.2.2 Catchment characteristics ...... 19

2.2.3 Cockrone Lagoon ...... 19

iii Table of Contents

2.2.4 Avoca Lagoon ...... 24

2.2.5 Terrigal Lagoon ...... 28

2.2.6 Wamberal Lagoon ...... 32

2.2.7 Adjacent surf zones ...... 36

2.3 Southern Site–Ulladulla ...... 36

2.3.1 Climate ...... 36

2.3.2 Catchment characteristics ...... 37

2.3.3 Termeil Lake ...... 37

2.3.4 Meroo Lake ...... 38

2.4. Sampling regime ...... 39

Chapter 3: Factors influencing temporal and spatial variations of the invertebrate faunal assemblages of ICOLLs ...... 45

3.1 Introduction ...... 46

3.2 Materials and methods ...... 48

3.2.1 Study area ...... 48

3.2.2 Invertebrate fauna collection and laboratory analysis ...... 48

3.2.3 Environmental variables ...... 49

3.2.4 Data analysis ...... 49

3.3 Results ...... 51

3.3.1 ICOLL openings ...... 51

3.3.2 Invertebrate faunal assemblages of ICOLLs ...... 52

3.3.3 Comparison of invertebrate faunal assemblages between ICOLLs...... 60

3.3.4 Comparison of environmental factors structuring invertebrate faunal assemblages of ICOLLs ...... 64

3.4 Discussion ...... 69

3.4.1 Physical and environmental aspects of ICOLLs ...... 69

3.4.2 Invertebrate faunal assemblages of ICOLLs ...... 70

3.4.3 Spatial and temporal variation of invertebrate faunal assemblages of ICOLLs ...... 71

3.4.4 Influence of environmental variables on invertebrate faunal assemblages ...... 72

3.4.5 Implications of the study ...... 74

iv Table of Contents

3.5 Conclusion ...... 74

Appendices: Invertebrate faunal assemblages and water variables of ICOLLs ...... 76

Chapter 4: Effects of barrier openings on larval and juvenile fish assemblages within ICOLLs and in adjacent surf zones...... 85

4.1 Introduction ...... 86

4.2 Materials and Methods ...... 88

4.2.1 Pilot study ...... 88

4.2.2 Field fish collection and laboratory analyses ...... 90

4.2.3 Life history categories ...... 92

4.2.4 Environmental variables ...... 92

4.2.5 Sampling design and data analysis ...... 93

4.3 Results ...... 94

4.3.1 ICOLL openings and environmental variables of ICOLLs and adjacent surf zones...... 94

4.3.2 Larval and juvenile fishes of ICOLLs...... 97

4.3.3 Temporal variation in assemblages of larval and juvenile fishes of ICOLLs ...... 99

4.3.4 Larval and juvenile fishes of adjacent surf zones ...... 110

4.3.5 Temporal variation in assemblages of larval and juvenile fishes of adjacent surf zones ...... 110

4.3.6 Effects of barrier openings on larval and juvenile fish assemblages ...... 122

4.3.7 Length-frequency distributions of larval and juvenile fishes ...... 123

4.4. Discussion ...... 125

4.4.1 Effects of barrier openings on larval and juvenile fish assemblages of ICOLLs and adjacent surf zones ...... 125

4.4.2 Comparison of larval and juvenile fish assemblages in ICOLLs and adjacent surf zones ...... 128

4.4.3 Implications of this study for ICOLL management ...... 130

4.5 Conclusion ...... 130

Chapter 5: Factors influencing temporal and spatial variations of the fish assemblages of ICOLLs ...... 132

v Table of Contents

5.1 Introduction ...... 133

5.2 Materials and methods ...... 136

5.2.1 Study area ...... 136

5.2.2 Pilot study ...... 141

5.2.3 Sampling design ...... 145

5.2.4 Environmental variables ...... 146

5.2.5 Data analysis ...... 147

5.3 Results ...... 149

5.3.1 ICOLL openings ...... 149

5.3.2 Fish assemblages of ICOLLs ...... 150

5.3.3. Comparison of fish assemblages between ICOLLs ...... 165

5.3.3.1 Multivariate analysis-seine net samples ...... 165

5.3.3.2 Univariate analysis-seine net samples ...... 169

5.3.3.3 Multivariate analysis–multi-panel gill net samples ...... 170

5.3.3.4 Univariate analysis–multi-panel gill net samples ...... 173

5.3.4 Comparison of environmental factors structuring fish assemblages of ICOLLs ...... 175

5.3.4.1 Environmental variables ...... 175

5.3.4.2 Influence of environmental variables on seine net fish assemblages ...... 176

5.3.4.3 Influence of environmental variables on multi-panel gill net fish assemblages ....180

5.4 Discussion ...... 183

5.4.1 Overview of fish assemblages in ICOLLs ...... 183

5.4.2 Diversity of fishes in Central Coast ICOLLs ...... 185

5.4.3 Comparison of fish assemblages in ICOLLs ...... 186

5.4.4 Spatial and temporal variation of fish assemblages of ICOLLs ...... 188

5.4.5 Influence of environmental variables on fish assemblages ...... 189

5.4.6 Implications of this study ...... 190

5.5 Conclusion ...... 191

Appendices: Fish assemblages, water variables and algal mass of ICOLLs ...... 193

Chapter 6: Diets of fishes in ICOLLs and the effects of barrier openings ...... 204

vi Table of Contents

6.1 Introduction ...... 205

6.2 Materials and methods ...... 207

6.2.1 Study area ...... 207

6.2.2 Study species ...... 208

6.2.3 Sample size ...... 209

6.2.4 Examination of gut contents ...... 211

6.2.5 Dietary composition ...... 212

6.2.6 Data analysis ...... 212

6.3 Results ...... 213

6.3.1 Acanthopagrus australis-Cockrone Lagoon ...... 213

6.3.2 Atherinosoma microstoma-Avoca Lagoon ...... 218

6.3.3 Atherinosoma microstoma–Wamberal Lagoon ...... 221

6.3.4 Ambassis jacksoniensis-Terrigal Lagoon ...... 225

6.4 Discussion ...... 228

6.4.1. General overview of diets of fishes in ICOLLs ...... 228

6.4.2 Effects of barrier openings on diets of ICOLL fishes ...... 231

6.5 Conclusions ...... 233

Appendices: Frequency of occurrence (%F) and estimated percentage volumetric contributions (%V) of dietary items of fishes in ICOLLs ...... 234

Chapter 7: Trace metal concentrations in sediments and tissues of Mugil cephalus in ICOLLs: effects of ICOLL condition and barrier openings ...... 239

7.1 Introduction ...... 240

7.2 Materials and methods ...... 242

7.2.1 Study site ...... 242

7.2.2 Study species ...... 244

7.2.3 Sediment collection ...... 244

7.2.4 Environmental variables ...... 244

7.2.5 Sediment processing and analysis ...... 245

7.2.6 Fish tissue collection and trace metal analysis ...... 246

7.2.7 Data analysis ...... 247

vii Table of Contents

7.3 Results ...... 249

7.3.1 Environmental variables ...... 249

7.3.2 Trace metal concentrations in ICOLL sediments ...... 249

7.3.3 Multivariate analysis ...... 253

7.3.4 Length and weight comparisons of Mugil cephalus ...... 254

7.3.5 Metal concentrations in tissues of Mugil cephalus ...... 255

7.3.6 Multivariate analysis ...... 259

7.4 Discussion ...... 266

7.4.1. Environmental variables and sediment characteristics of ICOLLs ...... 266

7.4.2 Sources of trace metals ...... 267

7.4.3 Trace metals in ICOLL sediments ...... 268

7.4.4 Comparison of trace metals in ICOLL sediments ...... 269

7.4.5 Trace metals in liver and gonad tissues of Mugil cephalus ...... 270

7.4.6 Implication and limitations of the study ...... 272

7.5 Conclusion ...... 272

Chapter 8: General discussion and conclusions ...... 274

8.1 General Discussion ...... 275

8.2 Barrier openings ...... 276

8.3 Recruitment of larval and juvenile fishes into ICOLLs ...... 277

8.4 The effects of environmental factors on the invertebrate and fish assemblages of ICOLLs ...... 278

8.4.1 Invertebrate assemblages ...... 278

8.4.2 Fish assemblages...... 278

8.5 Diets of fish in ICOLLs ...... 279

8.6 Trace metals in sediments and fishes in ICOLLs ...... 279

8.7 Implications of this study ...... 280

8.8 Opportunities for Further Research ...... 280

8.9 General conclusions ...... 281

References cited ...... 283

viii Abstract

Abstract Intermittently Closed and Open Lakes and Lagoons (ICOLLs) are coastal waterbodies that have intermittent connection to the ocean due to the formation of a barrier across the entrance. Catchment development is a major cause of pollution and also a justification for artificial barrier openings, which can have an adverse effect on the flora and fauna of ICOLLs. In most cases barrier openings may not have a direct effect on the biota of ICOLLs, but they can affect the factors which may influence invertebrate faunal and fish assemblages. The overall aim of this study was to determine what factors may influence fish assemblages of Central Coast ICOLLs. In order to understand these factors the research looked at the general ecology of Central Coast ICOLLs, including their invertebrate faunal assemblages and environmental parameters that may influence them (Chapter 3). Vegetated habitats within Central Coast ICOLLs include Ruppia sp. and the algae Chara sp. and Entermorpha intestinalis that support an invertebrate fauna dominated by polychaetes, crustaceans and molluscs. No single environmental variable had a major influence in structuring the invertebrate faunal assemblages at all four Central Coast ICOLLs. However, salinity was a major influencing factor at Cockrone, Avoca and Terrigal Lagoons, with percentage sediment composition a major factor at Wamberal Lagoon.

Recruitment processes of larval and juvenile fishes are also presumably influenced by the status of the barrier. Larval and juvenile fishes occurring in Central Coast ICOLLs and their adjacent surf zones were identified to determine if movement of various species occurs once the barrier has been opened (Chapter 4). In this study, larval and juvenile fishes were more abundant in Central Coast ICOLLs but had lower species richness compared to their adjacent surf zones. The dominant larval and juvenile fish species found in ICOLLs included Ambassis jacksoniensis (Terrigal Lagoon), Philypnodon grandiceps (Avoca and Wamberal Lagoons) Atherinosoma microstoma (Wamberal Lagoon) and Acanthopagrus australis (Cockrone Lagoon). Hyperlophus vittatus was the dominant species collected from the adjacent surf zones. In this study there were no significant changes in larval and juvenile fish assemblages in either habitat from before to after barrier openings. Although some marine spawning species such as A. australis were present it could not be determined if these species were recruited from adjacent surf zones or from within these ICOLLs themselves. In most cases, Central Coast ICOLLs are considered to be generally self-recuiting environments, not for all species, but for many of their resident species of fish.

Chapter Five determined the effects environmental parameters have on influencing fish assemblages. Fish assemblages of Central Coast ICOLLs showed low species richness, but high abundances of particular species when sampled using seine nets and multi-panel gillnets.

ix Abstract

Acanthopagrus australis (Cockrone Lagoon), Atherinosoma microstoma (Avoca and Wamberal Lagoons) and Ambassis jacksoniensis (Terrigal Lagoon) were the numerically dominant fish species collected using seine nets. Mugil cephalus was the species which was overall most frequently collected by gill netting. Fish assemblages were shown to be significantly different between Central Coast ICOLLs, and in this case were not directly influenced by barrier openings except at Wamberal Lagoon. However, Terrigal Lagoon, which had more barrier openings over the study period, compared to the other three ICOLLs, did have a higher diversity of fishes, which indicates that frequent barrier openings can influence fish assemblages. The major environmental influence on fish assemblages collected by seine nets at Cockrone and Wamberal Lagoons was salinity, and water temperature at Avoca and Terrigal Lagoons. The major environmental influence on fish assemblages collected by multi-panel gill nets at Cockrone and Avoca Lagoons was salinity, and water temperature at Terrigal Lagoon and >212 µm percentage sediment grain size at Wamberal Lagoon. Also, stochastic factors in the times and durations of barrier openings may play a large part in determining the fish assemblages that may be present at any one time in individual ICOLLs.

High abundances of fish and their isolation from the ocean for long periods can result in competition for limited food resources, along with the effects that barrier openings may have on these resources not being fully understood (Chapter 6). Gut contents for each dominant species examined were similar; however each fish species had a dietary preference for a particular taxonomic group. Amphipods were the main dietary component of Acanthopagrus australis and Atherinosoma microstoma, with zooplankton being the main dietary component of Ambassis jacksoniensis. Barrier openings had a significant effect on the diets of A. australis (in Cockrone Lagoon) and A. microstoma (in Wamberal Lagoon), but not for species examined from Avoca and Terrigal Lagoons.

Trace metal concentrations in sediments of Central Coast and Near-South Coast ICOLLs and gonad and liver tissues of Mugil cephalus were determined (Chapter 7). In the six ICOLLs studied, trace metal concentrations in both sediments and fish tissues were found to be relatively low and below guideline levels. Concentration levels did not differ significantly when compared between near-pristine (Termeil and Meroo Lakes), modified (Avoca and Terrigal Lagoons) and extensively-modified (Cockrone and Wamberal Lagoons) ICOLLs. Trace metal concentrations in sediments were not influenced by barrier openings.

This study has shown that ICOLLs which are located geographically close to each other generally do not have similar environmental characteristics or fish assemblages which can be

x Abstract

attributed to varying levels of development and land use activities within their individual catchments.

xi List of Tables

List of Tables Table 2.1. Physical characteristics of surf zones (after Short 2007) adjacent to ICOLLs used in this study. Aspect is (ESE) east south easterly, and (ENE) east north easterly. Beach types are (RBB) rhythmic bar and beach, (TBR) transverse bar and rip, (LTT) low tide terrace beach. ...36

xii List of Tables

Table 3.3. Presence/absence of invertebrate infauna and epifauna. Collections occurred bimonthly between December 2004 and October 2005. X indicates the species was present at the ICOLL...... 54

Table 3.4. Summary of results of 3-factor PERMANOVA testing for differences in the invertebrate assemblages of ICOLLs...... 60

Table 3.6. Summary of results of univariate PERMANOVA testing for differences among ICOLLs in the mean number of species and mean number of total individuals...... 63

Table 3.7. Results of distance-based multivariate linear model (DISTLM) for environmental variables for Cockrone, Avoca, Terrigal and Wamberal Lagoons that are the BEST predictors of spatial and temporal variation in invertebrate assemblages. The relative importance of each variable in the model linking these variables to assemblage variation (fitted model) and the relative importance of each variable to the total variation in invertebrate assemblages are shown...... 66

Table 3.8. Values of Pearson correlations of selected environmental variables with each of the dbRDA axes for Cockrone, Avoca, Terrigal and Wamberal Lagoons...... 69

Table 4.1. ICOLL and surf zone sampling periods between April 2006 and March 2007. *denotes ICOLLs only sampled due to dangerous surf and adverse weather conditions...... 91

xiii List of Tables

Table 4.4. Summary of one-factor ANOVAs testing for temporal variation in total abundance of larval and juvenile fishes collected from four ICOLLs between April 2006 and March 2007...... 100

Table 4.5. Summary of changes in mean total abundance of larval and juvenile fishes between successive sampling periods in relation to the status of the ICOLL entrance in the interval between sampling periods. Increase and decrease refer, respectively, to significant (p<0.05) increases and decreases in mean abundance...... 101

Table 4.6. Summary of one-factor ANOVAs testing for temporal variation in number of species of larval and juvenile fishes collected from four ICOLLs between April 2006 and March 2007...... 102

Table 4.7. Summary of changes in mean number of species of larval and juvenile fishes between successive sampling periods in relation to the status of the ICOLL entrance in the interval between sampling periods. Increase and decrease refer, respectively, to significant (p<0.05) increases and decreases in mean abundance...... 104

Table 4.8. Summary of one-factor ANOVAs testing for temporal variation in numbers of larvae and juveniles of the dominant species in each ICOLL between April 2006 and March 2007...... 106

Table 4.9. Summary of changes in mean abundance of larvae and juveniles of the dominant species between successive sampling periods in relation to the status of the ICOLL entrance in the interval between sampling periods. Increase and decrease refer, respectively, to significant (p<0.05) increases and decreases in mean abundance...... 106

xiv List of Tables

Table 4.11. Summary of changes in assemblages of larval and juvenile fishes of ICOLLs between successive sampling periods in relation to the status of the ICOLL entrance in the interval between sampling periods. Change refers to a significant (p<0.05) difference in assemblage structure by pairwise ANOSIM test...... 109

Table 4.14. Summary of changes in mean total abundance of larval and juvenile fishes of surf zones between successive sampling periods in relation to the status of the ICOLL barrier at the interval between sampling periods. Increase and decrease refer, respectively, to significant (p<0.05) increases and decreases in mean abundance as detected by SNK tests...... 113

Table 4.16. Summary of changes in the mean number of species of larval and juvenile fishes of surf zones between successive sampling periods in relation to the status of the ICOLL entrance in the interval between sampling periods. Increase and decrease refer, respectively, to significant (p<0.05) increases and decreases in mean abundance as detected by SNK tests. ....116

Table 4.18. Summary of changes in the mean abundance of dominant species of larval and juvenile fishes of surf zones between successive sampling periods in relation to the status of the barrier in the interval between sampling periods. Increase and decrease refer, respectively, to significant (p<0.05) increases and decreases in mean abundance as detected by SNK tests. ....119

xv List of Tables

Table 4.20. Jaccard’s coefficient of similarity for larval and juvenile fish assemblages between ICOLLs and surf zones before and after opening events...... 123

Table 5.1. Fishes collected from Avoca Lagoon during the pilot study using baited traps. (*too damaged to identify)...... 142

Table 5.2. Fishes collected from ICOLLs using seine and multi-panel gill nets during the pilot study. Gill nets were not used in Cockrone Lagoon due to unsuitable weather conditions...... 144

Table 5.5. Presence/absence of fishes collected from ICOLLs between February 2009 and June 2010. Fishes were collected by seine net (s) or gill nets (g) or by both methods (s,g)...... 153

Table 5.6. Summary of 3-factor PERMANOVA testing for differences in the fish assemblages of ICOLLs collected by seine nets. Data was square-root transformed...... 165

xvi List of Tables

Table 5.10. Summary of 3-factor PERMANOVA testing for differences in the fish assemblages of ICOLLs collected by multi-panel gill nets. Data was square-root transformed...... 171

Table 5.14. Values of Pearson correlations of selected environmental variables with each of the dbRDA axes for Cockrone, Avoca, Terrigal and Wamberal Lagoons...... 179

xvii List of Tables

Table 6.1. Summary of results of 1-factor PERMANOVA testing for differences in the gut contents (defined by %V) of Acanthopagrus australis from before to after (i.e. status) barrier openings at Cockrone Lagoon (PERMDISP p=0.013). Data was square-root transformed...... 214

Table 6.4. Summary of results of 1-factor PERMANOVA testing for differences in the mean gut fullness (PERMDISP p=0.40) and mean TL (PERMDISP p=0.0001) of Acanthopagrus australis from before to after the barrier had opened (status) at Cockrone Lagoon. *denotes untransformed, **square-root transformation...... 217

Table 6.5. Summary of results of 1-factor PERMANOVA testing for differences in the gut contents (defined by %V) of Atherinosoma microstoma from before to after (i.e. barrier status) barrier openings at Avoca Lagoon (PERMDISP p=0.91). Data was square-root transformed...... 218

Table 6.6. Summary of results of univariate PERMANOVA testing for differences in the mean numbers of taxonomic units (PERMDISP p=0.02) and the mean number of dietary items (PERMDISP p=0.84) for Atherinosoma microstoma at Avoca Lagoon from before to after the barrier was opened. Data was square-root transformed...... 219

Table 6.7. Summary of results of 1-factor PERMANOVA testing for differences in the mean gut fullness (PERMDISP p=0.28) and mean TL (PERMDISP p=0.003) of Atherinosoma microstoma from before to after the barrier opening (i.e. status) at Avoca Lagoon. *data was untransformed, **data was square-root transfomed...... 220

Table 6.8. Summary of results of 1-way PERMANOVA testing for differences in the %V of gut contents (PERMDISP p=0.25) of Atherinosoma microstoma from before to after barrier openings (i.e. status) at Wamberal Lagoon. Data was square-root transformed...... 222

xviii List of Tables

Table 6.10. Summary of results of univariate PERMANOVA testing for differences in the mean numbers of taxonomic units (PERMDISP p=0.29) and the mean number of dietary items (PERMDISP p=0.09) for Atherinosoma microstoma at Wamberal Lagoon from before to after (i.e. barrier status) barrier opening. Data was untransformed...... 223

Table 6.12. Summary of results of 1-factor PERMANOVA testing for differences in the gut contents (defined by %V) of Ambassis jacksoniensis from open to after (i.e. barrier status) barrier closure at Terrigal Lagoon (PERMDISP p=0.88). Data was square-root transformed...... 226

Table 6.14. Summary of results of unvariate PERMANOVA testing the differences for mean gut fullness (PERMDISP p=0.92) and mean TL (PERMDISP p=0.01) of Ambassis jacksoniensis from open to after (i.e. barrier status) barrier closure at Terrigal Lagoon. *data untransformed, **data square root transfomed...... 228

xix List of Tables

Table 7.4. Pearson’s correlation coefficient (r) and levels of significance (p) for the relationship between trace metal concentrations, Cr, Cu, Fe and Zn, in sediments and the number of barrier openings. As, Cd, Pb and Se were not tested as they were found to be below detectable levels...... 253

Table 7.5. Summary of results of 2-way PERMANOVA testing for differences in the suite of trace metals of sediments resulting from ICOLL status (near-pristine, modified, extensively- modified), and among ICOLLs within each status category...... 254

Table 7.6. Total length (cm) and weight (g) of Mugil cephalus collected from near-pristine (NP) modified (M) and extensively-modified (EM) ICOLLs. n= number of fish collected...... 255

Table 7.7. Summary of results of univariate PERMANOVA testing for differences in the TL (cm) and weight (g) of Mugil cephalus collected from near-pristine, modified and extensively- modified ICOLLs. Univariate dispersions of the TL (PERMDISP p=0.05) and for the weight (PERMDISP p=0.12) were not significantly different...... 255

xx List of Tables

xxi List of Figures

List of Figures Figure 2.1. Study location of ICOLLs at the northern sites (Gosford) and southern sites (Ulladulla)...... 18

Figure 2.2. Aerial view of Cockrone Lagoon (OEH 2011)...... 20

Figure 2.3. Collecting sites (1-9) and sediment types of Cockrone Lagoon, May 2004. Areas not coloured indicate sites where sediment was not collected...... 21

Figure 2.4. Percentage grain size composition of ambient sediment samples collected from nine sites within Cockrone Lagoon in May 2004...... 22

Figure 2.5. Seagrass and algal habitats of Cockrone Lagoon obtained by field measurements during 2004 and derived from aerial photos and West et al. (1985). Fortnightly sampling sites for salinity, turbidity and water temperature and bimonthly invertebrate collection are labelled 1-6 (see Chapter 3). Areas not coloured indicate sites where seagrasses and/or algae were not present or areas that were not assessed...... 23

Figure 2.6. Aerial view of Avoca Lagoon (OEH 2011)...... 24

Figure 2.7. Collecting sites (1-15) and sediment types of Avoca Lagoon, May 2004. Areas not coloured indicate sites where sediment was not collected...... 25

Figure 2.8. Percentage grain size composition of ambient sediment samples collected from fifteen sites within Avoca Lagoon in May 2004...... 26

Figure 2.9. Seagrass and algal habitats of Avoca Lagoon obtained by field measurements during 2004 and derived from aerial photos and West et al. (1985). Fortnightly sampling sites for salinity, turbidity and water temperature and bimonthly invertebrate collection are labelled 1-6 (see Chapter 3). Areas not coloured indicate sites where seagrasses and/or algae were not present or areas that were not assessed...... 27

Figure 2.10. Aerial view of Terrigal Lagoon (OEH 2011)...... 28

Figure 2.11. Collecting sites (1-12) and sediment types of Terrigal Lagoon, May 2004...... 29

xxii List of Figures

Figure 2.12. Percentage grain size composition of ambient sediment samples collected from twelve sites within Terrigal Lagoon in May 2004...... 30

Figure 2.13. Terrigal Lagoon showing positions of fortnightly sampling sites (labelled 1-4) for salinity, turbidity and water temperature and bimonthly invertebrate collection (see Chapter 3). No aquatic vegetation was observed in Terrigal Lagoon...... 31

Figure 2.14. Aerial view of Wamberal Lagoon (OEH 2011)...... 32

Figure 2.15. Collecting sites (1-13) and sediment types of Wamberal Lagoon, May 2004. Areas not coloured indicate sites where sediment was not collected...... 33

Figure 2.16. Percentage grain size composition of ambient sediment samples collected from thirteen sites within Wamberal Lagoon in May 2004...... 34

Figure 2.17. Distribution of seagrass and algae in Wamberal Lagoon obtained by field measurements during 2004 and derived from aerial photos and West et al. (1985). Fortnightly sampling sites for salinity, turbidity and water temperature and bimonthly invertebrate collection are labelled 1-6 (see Chapter 3). Areas not coloured indicate sites where seagrasses and/or algae were not present or areas that were not assessed...... 35

Figure 2.18. Aerial view of Termeil Lake (OEH 2011)...... 38

Figure 2.19. Aerial view of Meroo Lake (OEH 2011)...... 39

Figure 3.1. Comparison of the total number of invertebrates (a) and the total number of invertebrate taxa (b) collected from sites (n) within each ICOLL from December 2004 to October 2005...... 53

Figure 3.2. Temporal and spatial variation of (a) the total number of individual invertebrates and (b) the total number of taxa collected using core samples (sites 1-6) and from Ruppia sp. (site 4R) and algae (sites 4A and 5A) from Cockrone Lagoon. Dotted vertical lines indicate single barrier openings occurred between sampling periods...... 56

xxiii List of Figures

Figure 3.3. Temporal and spatial variation of (a) the total number of invertebrates and (b) the total number of taxa collected using core samples (sites 1-6) and from Ruppia sp. (site 3R) and algae (sites 4A and 5A) from Avoca Lagoon. Dotted vertical lines indicate single barrier openings occurred between sampling periods...... 57

Figure 3.4. Temporal and spatial variation of (a) the total number of individual invertebrates and (b) the total number of taxa collected using core samples (sites 1-4) from Terrigal Lagoon. Solid vertical lines indicate multiple barrier openings occurred between sampling periods...... 58

Figure 3.5. Temporal and spatial variation of (a) the total number of individual invertebrates and (b) the total number of taxa collected using core samples (sites 1-6) and from Ruppia sp. (sites 3R, 4R and 6R) from Wamberal Lagoon. Dotted vertical lines indicate single barrier openings occurred between sampling periods...... 59

Figure 3.6. MDS ordination plots showing the temporal and spatial variability of invertebrate assemblages at sites within each ICOLL. Assemblages are based on the mean abundance of each species in each site at each sampling time. Sampling times are represented by symbols: ▲T1, ▼T2, ■T3, ♦T4, ●T5, +T6. The replicate symbols represent the different sites at each time...... 61

Figure 3.7. Mean number (±se) of species (a) and mean number (±se) of individuals (b) of invertebrate fauna from all ICOLLs. * denotes the ICOLL was significantly different...... 64

Figure 3.8. dbRDA ordination plots showing the structural arrangement of invertebrate assemblages in Cockrone, Avoca, Terrigal and Wamberal Lagoons overlaid with the vectors of the environmental variables that explained significant amounts of variation in the assemblages. Vectors represent the direction and magnitude of the Pearson correlation of each variable with the dbRDA axes. The different symbols represent different sampling times, and the replicate symbols represent the different sites at each time. Sampling times are represented by symbols: ▲T1, ▼T2, ■T3, ♦T4, ●T5, +T6. Sal=salinity, Turb=turbidity, Temp=water temperature, Dist= distance from barrier...... 68

Figure 4.1. Illustration of beach seine net used for sampling larval and juvenile fishes from surf zones and ICOLLs (after Geraghty 2004)...... 89

xxiv List of Figures

Figure 4.2. Pilot study comparison of sampling precision (standard error/mean) for total number of fishes collected using a 20 m and 50 m transect during new and full moon phases in Terrigal Lagoon, for sample sizes of 2 to 6 replicate hauls...... 89

Figure 4.3. Pilot study comparison of sampling precision (standard error/mean) for total number of fishes collected using 30 m transect during new and full moon phases at 3 sites (south, adjacent, north) on Terrigal Beach, for sample sizes of 2 to 6 replicate hauls...... 90

Figure 4.4. Diagrammatic representation of the relative positions of transects used to collect larval and juvenile fishes in surf zones and ICOLLs. ● indicates where environmental variables (salinity and water temperature) were measured...... 91

Figure 4.5. Water surface temperature (°C) sampled at ICOLLs from April 2006 to March 2007. The dotted vertical lines indicate a single barrier opening occurred between sampling periods. The solid vertical lines indicate multiple barrier openings occurred between sampling periods...... 96

Figure 4.6. Water surface temperature (°C) sampled at surf zones from April 2006 to March 2007...... 96

Figure 4.7. Water surface salinity (ppt) sampled at ICOLLs from April 2006 to March 2007. The dotted vertical lines indicate a single barrier opening occurred between sampling periods. The solid vertical lines indicate multiple barrier openings occurred between sampling periods. Salinities were not measured in surf zones...... 97

Figure 4.8. Mean total number (± se) of larval and juvenile fishes collected at ICOLLs from April 2006 to March 2007. Mean values with the same letter are not significantly different. The dotted vertical lines indicate a single barrier opening occurred between sampling periods...... 101

Figure 4.9. Mean number of species (± se) of larval and juvenile fishes collected at ICOLLs from April 2006 to March 2007. Mean values with the same letter are not significantly different. The dotted vertical lines indicate a single barrier opening occurred between sampling periods...... 104

xxv List of Figures

Figure 4.10. Mean abundance (± se) of larvae and juveniles of the dominant species at ICOLLs from April 2006 to March 2007. Mean values with the same letter are not significantly different. The dotted vertical lines indicate a single barrier opening occurred between sampling periods...... 106

Figure 4.11. Dendrograms showing similarity of assemblages of larval and juvenile fishes collected at different sampling times at ICOLLs. Sampling periods occurred bimonthly unless barriers had opened, in which case a sampling period occurred before and after the barrier opening. Sampling periods where no fish were collected were not included in the analysis. ^indicates first sampling period after ICOLLs were opened. The division line is shown at the 50% level...... 108

Figure 4.12. Mean abundance (± se) of larval and juvenile fishes collected at all surf zones from April 2006 to March 2007. Mean values with the same letter are not significantly different. The dotted vertical lines indicate a single barrier opening occurred between sampling periods...... 113

Figure 4.13. Mean number of species (± se) of larval and juvenile fishes collected at all surf zones from April 2006 to March 2007. Mean values with the same letter are not significantly different. The dotted vertical lines indicate a single barrier opening occurred between sampling periods...... 116

Figure 4.14. Mean abundance (± se) of the dominant species of larval and juvenile fishes at all surf zones from April 2006 to March 2007. Mean values with the same letter are not significantly different. The dotted vertical lines indicate a single barrier opening occurred between sampling periods...... 119

Figure 4.15. Dendrogram showing similarity of assemblages of larval and juvenile fishes collected at different sampling times at surf zones. Sampling periods occurred bimonthly unless barriers had opened, in which case a sampling period occurred before and after the barrier opening. Sampling periods where no fish were collected were not included in the analysis. ^indicates first sampling period after barriers were opened. The division line is shown at the 50% level...... 120

Figure 4.16. Length-frequency distributions of the most abundant species collected from each ICOLL before and after opening events. (a) Cockrone Lagoon (no A. australis were collected before the barrier opening ), (b) Avoca Lagoon, (c) Terrigal Lagoon, (d)-(e) Wamberal Lagoon...... 124

xxvi List of Figures

Figure 5.1. Cockrone Lagoon showing subcatchments (C1-C7) and locations of sampling sites (1-5) for bimonthly seine and multi-panel gill netting, and water sampling and algae collection...... 137

Figure 5.2. Avoca Lagoon showing subcatchments (A1-A11) and locations of sampling sites (1-5) for bimonthly seine and multi-panel gill netting, and water sampling and algae collection...... 138

Figure 5.3. Terrigal Lagoon showing subcatchments (T1-T10) and locations of sampling sites (1-4) for bimonthly seine and multi-panel gill netting and water sampling. No algae were present in this lagoon...... 139

Figure 5.4. Wamberal Lagoon showing subcatchments (W1-W10) and locations of sampling sites (1-5) for bimonthly seine and multi-panel gill netting, and water sampling and algae collection...... 140

Figure 5.5. Results of the pilot study comparing three replicate samples of seine and multi-panel gill nets showing (a) total number of fishes collected and (b) the number of species of fishes collected from Cockrone, Avoca, Terrigal and Wamberal lagoons during December 2008. Gill nets were not used in Cockrone Lagoon due to unsuitable weather during sampling...... 145

Figure 5.6. (a) Total abundances of fishes, and (b) the total number of species collected (results from seine and multi-panel gill nets combined) from the four ICOLLs. n=the total number of samples taken over the sampling period...... 152

Figure 5.7. Temporal and spatial variation of fishes collected with seine and multi-panel gill nets for (a) the total number of individuals and (b) the number of species collected bimonthly from Cockrone Lagoon between February 2009 and June 2010. Months and sites with no data indicate no fishes were collected, and the data is the sum of all replicates in each site. The solid vertical line indicates multiple barrier openings that occurred between sampling periods...... 155

Figure 5.8. Length-frequency distribution of Acanthopagrus australis (n=1 491) collected between February 2009 and June 2010 using a seine net in Cockrone Lagoon...... 156

Figure 5.9. Length-frequency distribution of Mugil cephalus (n=136) collected between February 2009 and June 2010 using multi-panel gill nets in Cockrone Lagoon...... 157

xxvii List of Figures

Figure 5.10. Temporal and spatial variation of fishes collected with seine and multi-panel gill nets for (a) the total number of individuals and (b) the number of species collected bimonthly from Avoca Lagoon between February 2009 and June 2010. Months and sites with no data indicate no fishes were collected, and the data is the sum of all replicates in each site. Solid vertical lines indicate multiple barrier openings that occurred between sampling periods...... 158

Figure 5.11. Length-frequency distribution of Atherinosoma microstoma (n=1 702) collected between February 2009 and June 2010 using a seine net in Avoca Lagoon...... 159

Figure 5.12. Length-frequency distributions of Mugil cephalus (n=315) collected between February 2009 and June 2010 using multi-panel gill nets in Avoca Lagoon...... 159

Figure 5.13. Temporal and spatial variation of fishes collected with seine and multi-panel gill nets for (a) total number of individuals and (b) the number of species collected bimonthly from Terrigal Lagoon between February 2009 and June 2010. Solid vertical lines indicate multiple barrier openings occurred between sampling periods...... 160

Figure 5.14. Length-frequency distribution of total lengths of Ambassis jacksoniensis (n=475) collected between February 2009 and June 2010 using a seine net in Terrigal Lagoon...... 161

Figure 5.15. Length-frequency distribution of total length of Myxus elongatus (n=209) collected between February 2009 and June 2010 using multi-panel gill nets in Terrigal Lagoon...... 162

Figure 5.16. Temporal and spatial variation of fishes collected with seine and multi-panel gill nets of (a) the total number of individuals and (b) the number of species collected bimonthly from Wamberal Lagoon between February 2009 and June 2010. The dotted vertical lines indicate a single barrier opening that occurred between sampling periods...... 163

Figure 5.17. Length-frequency distribution of Atherinosoma microstoma (n=5 666) collected between February 2009 and June 2010 using a seine net in Wamberal Lagoon...... 164

Figure 5.18. Length-frequency distribution of Mugil cephalus (n=176) collected between February 2009 and June 2010 using multi-panel gill nets in Wamberal Lagoon...... 164

xxviii List of Figures

Figure 5.19. MDS ordination plots showing temporal and spatial variability in fish assemblages of ICOLLs for species collected by seine net (based on the mean abundance of each species in each site). The different symbols represent different sampling times (T), and the replicate symbols represent the different sites at each time. Sampling times are represented by symbols: ▲T1, ▼T2, ■T3, ♦T4, ●T5, +T6, ΔT7, ΟT8...... 166

Figure 5.20. MDS ordination plots showing temporal and spatial variability in fish assemblages of ICOLLs for species collected by multi-panel gill nets (based on the mean abundance of each species in each site). The different symbols represent different sampling times (T), and the replicate symbols represent the different sites at each time. Sampling times are represented by symbols: ▲T1, ▼T2, ■T3, ♦T4, ●T5, +T6, ΔT7, ΟT8...... 172

Figure 5.21. dbRDA ordination plots showing the spatial and temporal variation of fish assemblages collected using seine nets in Cockrone, Avoca, Terrigal and Wamberal Lagoons overlaid with the vectors of the environmental variables that explained significant amounts of variation in the assemblages. Vectors represent the direction and magnitude of the Pearson correlation of each variable with the dbRDA axes. The different symbols represent different sampling times, and the replicate symbols represent the different sites at each time. Sampling times are represented by: ▲T1, ▼T2, ■T3, ♦T4, ●T5, +T6, ΔT7, ΟT8. Sal= salinity, Temp = water temperature, Dist= distance from barrier, % Bare= % bare substrate and Algae=% cover...... 178

Figure 5.22. dbRDA ordination plots showing the spatial and temporal variation of fish assemblages collected using multi-panel gill nets in Cockrone, Avoca, Terrigal and Wamberal Lagoons overlaid with the vectors of the environmental variables that explained significant amounts of variation in the assemblages. Vectors represent the direction and magnitude of the Pearson correlation of each variable with the dbRDA axes. The different symbols represent different sampling times, and the replicate symbols represent the different sites at each time. Sampling times are represented by: ▲T1, ▼T2, ■T3, ♦T4, ●T5, +T6, ΔT7, ΟT8. Sal=salinity, Temp=water temperature, Dist=distance from barrier, %Bare=bare substrate...... 182

Figure 6.1. Acanthopagrus australis, collected from Cockrone Lagoon (Photo M. Ricketts). .208

Figure 6.2. Atherinosoma microstoma collected from Avoca and Wamberal Lagoons (Photo M. Ricketts)...... 209

Figure 6.3. Ambassis jacksoniensis collected from Terrigal Lagoon (Photo M. Ricketts)...... 209

xxix List of Figures

Figure 6.4. Species accumulation curves showing mean number (for n=9999 permutations) of food species detected with increasing numbers of guts sampled, for Acanthopagrus australis (Cockrone Lagoon), Atherinosoma microstoma (Wamberal Lagoon) and Ambassis jacksoniensis (Terrigal Lagoon)...... 211

Figure 6.5. Estimated percentage volumetric (%V) contribution of different dietary categories associated with the diet of Acanthopagrus australis in relation to the barrier status (before, after openings) at Cockrone Lagoon. *denotes planktonic taxa...... 214

Figure 6.6. MDS ordination plot of the mean percentage volumetric contribution (%V) of the dietary categories for Acanthopagrus australis at sites within Cockrone Lagoon (barrier status: ●=before, ο=after). Each point is based on the mean of 5 guts examined...... 215

Figure 6.7. Mean number (±se) of taxonomic units (a) and mean number (±se) of dietary items (b) of Acanthopagrus australis before and after (i.e. barrier status) barrier openings at Cockrone Lagoon...... 216

Figure 6.8. Mean gut fullness (±s.e.) of Acanthopagrus australis at Cockrone Lagoon before and after the barrier opening...... 217

Figure 6.9. Length-frequency distribution of Acanthopagrus australis used in dietary analysis from Cockrone Lagoon before and after barrier openings...... 217

Figure 6.10. Estimated percentage volumetric (%V) contribution of different dietary categories associated with the diet of Atherinosoma microstoma in relation to the barrier status (before, after openings) at Avoca Lagoon. *denotes planktonic taxa...... 218

Figure 6.11. Mean number (±se) of taxonomic units (a) and mean number (±se) of dietary items (b) of Atherinosoma microstoma from before to after (i.e. barrier status) barrier openings at Avoca Lagoon. * denotes a significant difference...... 219

Figure 6.12. Mean gut fullness (±s.e.) of Atherinosoma microstoma at Avoca Lagoon before and after (i.e. barrier staus) the barrier opening...... 220

Figure 6.13. Length-frequency distribution of Atherinosoma microstoma used in the dietary examination at Avoca Lagoon before and after barrier openings...... 221

xxx List of Figures

Figure 6.14. Estimated percentage volumetric (%V) contribution of different dietary categories associated with the diet of Atherinosoma microstoma in relation to barrier status (before and after barrier opening) at Wamberal Lagoon. *denotes planktonic taxa...... 222

Figure 6.15. MDS ordination plot of the mean percentage volumetric contribution of the dietary categories for Atherinosoma microstoma in relation to the barrier at Wamberal Lagoon (Barrier status: ●=before, ο=after). Each point is based on the mean of 5 guts examined...... 222

Figure 6.16. Mean number (±se) of taxonomic units (a) and the mean number (±se) of dietary items (b) of Atherinosoma microstoma before and after (i.e. barrier status) barrier openings at Wamberal Lagoon...... 224

Figure 6.17. The mean gut fullness (±se) of Atherinosoma microstoma at Wamberal Lagoon before and after the barrier opening...... 225

Figure 6.18. Length-frequency distribution of Atherinosoma microstoma used in dietary examination at Wamberal Lagoon before and after barrier opening...... 225

Figure 6.19. Estimated percentage volumetric (%V) contribution of different dietary categories associated with the diet of Ambassis jacksoniensis in relation to the barrier status (open, after closure) at Terrigal Lagoon. *denotes planktonic taxa...... 226

Figure 6.20. Mean number (±se) of taxonomic units and mean number (±se) of dietary items (b) of Ambassis jacksoniensis open and after (i.e. barrier status) barrier closure at Terrigal Lagoon...... 227

Figure 6.21. Mean gut fullness (±se) of Ambassis jacksoniensis at Terrigal Lagoon open and after the barrier closure...... 228

Figure 6.22. Length-frequency distributions of Ambassis jacksoniensis used in dietary examination at Terrigal Lagoon from open to after barrier closure...... 228

Figure 7.1. Collecting sites for Mugil cephalus, sediment and water samples used in trace metal analysis from near-pristine (Meroo and Termeil Lakes), modified (Avoca and Terrigal Lagoons) and extensively-modified (Cockrone and Wamberal Lagoons) ICOLLs...... 243

xxxi List of Figures

Figure 7.2. Percentage composition of fine sediments (<63 µm) subsampled from sediments collected from each of the 6 ICOLLs. Denotes *near-pristine, **modified and ***extensively- modified ICOLLs...... 250

Figure 7.3. Mean (± s.e.) of trace metal in fine sediments (<63 um). Sample sizes for each ICOLL include; Meroo (n=4), Termeil (n=2), Cockrone (n=2), Avoca (n=2), Terrigal (n=1) and Wamberal (n=1). (a) Al, (b) Ca, (c) Cr, (d) Cu, (e) Fe, (f) Mn, and (g) Zn. Denotes *near- pristine, **modified and ***extensively-modified ICOLLs...... 253

Figure 7.4. MDS ordination plot depicting patterns of similarity in the trace metal content of sediment from 6 ICOLLs. Symbols indicate status of ICOLLs: ▲=Meroo Lake (near-pristine), Δ=Termeil Lake (near-pristine), ■=Avoca Lagoon (modified), □=Terrigal Lagoon (modified) and ●=Wamberal Lagoon (extensively-modified) and ο=Cockrone Lagoon (extensively- modified)...... 254

Figure 7.5. Trace metal levels in liver and gonad tissues of Mugil cephalus. Sample sizes for each ICOLL were: Meroo (n=3), Termeil (n=4), Cockrone (n=10), Avoca (n=10), Terrigal (n=8) and Wamberal (n=6). Levels of trace metals in liver ( ) and gonad ( ) tissues of sea mullet. Mean ± standard error (ug/g wet wt). Wet wt = wet weight. Denotes *near-pristine, **modified and ***extensively-modified ICOLLs...... 259

Figure 7.6. MDS ordination plot depicting patterns of similarity in the trace metal content in gonad tissues of Mugil cephalus from 6 ICOLLs. Symbols indicate status of ICOLLs: ▲= Meroo Lake (near-pristine), Δ=Termeil Lagoon (near-pristine), ■=Avoca Lagoon (modified), □=Terrigal Lagoon (modified) and ●=Wamberal Lagoon (extremely-modified) and ο=Cockrone Lagoon (extensively-modified)...... 261

Figure 7.7. MDS ordination plot depicting patterns of similarity in the trace metal content in liver tissue of Mugil cephalus from 6 ICOLLs. Symbols indicate status of ICOLLs: ▲= Meroo Lake (near-pristine), Δ=Termeil Lagoon (near-pristine), ■=Avoca Lagoon (modified), □=Terrigal Lagoon (modified) and ●=Wamberal Lagoon (extensively-modified) and ο=Cockrone Lagoon (extensively-modified)...... 263

xxxii Chapter 1: Introduction

Chapter 1: Introduction

1 Chapter 1: Introduction

1.1 General Introduction Australia’s coast consists of numerous coastal water bodies such as bays, estuaries, lagoons and tidal rivers that are the result of a dynamic environment of high energy waves and ocean swells, and freshwater input (Allan et al. 1985; Bird 1967). Geologically, the New South Wales (NSW) coastline is relatively young, at around 6 500 years old, and consists of Cainozoic rock deposits and bedrock valleys with narrow discontinuous coastal plains that are the result of constant excavation and infilling of sediments (Roy, 1984; Roy et al., 2001). The coastal valleys retain remnants of sedimentary deposits from the Holocene period, and as a result of flooding, estuaries occupy many of these valleys (Roy 1984; Roy et al. 2001).

Estuaries are an important habitat in fish’s life cycles, as seasonal and migratory fishes use estuaries as pathways to nursery and feeding areas (Kennish 1990) or for shelter and protection (Pollard 1981; Edgar et al. 1999). A large proportion of fish harvested from NSW estuaries are often important commercial and/or recreational species (Pease 1999). However, approximately 45% of NSW estuaries are ‘cut-off’ from the marine environment by a sandy barrier that forms across the entrance (Griffiths and West 1999). These estuaries are referred to as Intermittently Closed and Open Lakes and Lagoons, or ICOLLs (Haines 2006), and the ability of many of these estuarine systems to be important habitats for commercial and recreational species of fishes is uncertain. Species richness in estuaries is affected by environmental conditions and the ability of fishes to recruit successfully into these environments (Kennish 1990); however, the formation of a barrier limits recruitment, thereby restricting species richness (Strydom 2003).

1.2 Classification and definitions of estuaries The major types of estuaries found along the NSW coastline include drowned river valley estuaries, barrier estuaries, and saline coastal lakes and coastal lagoons. The level of barrier development determines estuary evolution (Short 2007), with the amount of infilling determining the maturity of an estuary (Roy 1984).

Early definitions of estuaries were related to the salinity or brackish water content found within water bodies that had connections to the sea (Bell and Edwards 1980; Day 1980). A common definition of an estuary was ‘a semi-enclosed coastal body of water which has free connection with the open sea and within which sea-water is measurably diluted with freshwater from land drainage’ (Pollard 1981). Further examination of this definition showed that it was more correlated to temperate northern hemisphere estuaries and did not take into account that many southern hemisphere estuaries were landlocked for long periods of time (Potter et al. 2010). Extended periods of dry weather and varying rainfall patterns produce sandy barriers across estuary entrances, restricting marine influences for periods of time ranging from hours to years

2 Chapter 1: Introduction

(Pollard 1994a; Potter et al. 2010). The definition of an estuary of Potter et al. (2010) includes features such as intermittent openings, periodic river discharges and the ability of the estuary to become hypersaline, features common to both some Australian and South African estuaries.

Recent definitions of estuaries described by investigators reflected their own perception of the area being studied. For example, researchers use multi-disciplinary approaches that include characterisations of physical, chemical and biological features along with conservation, socio- economic and legal aspects (Elliot and McLusky 2002).

Australian estuaries have been classified according to their condition or ecosystem health. A healthy estuary is generally defined as exhibiting no change in biodiversity over time, over and above the seasonal variations that occur (Turner et al. 2004). The condition of an estuary was originally based on factors related to geology and geomorphology (Roy et al. 2001) or factors related to other structural elements such as habitat integrity, ecological processes and community composition (Heap et al. 2001). Recent evaluations of estuarine health have been reported by Heap et al. (2001), the National Land and Water Resources Audit (NLWRA) (2002), the Healthy Rivers Commission (HRC) (2002) and Roper et al. (2011). However, the ability to evaluate estuarine health was dependant on the data available from state–wide decisions regulated by local councils and environmental agencies.

The criteria used for assessment of the condition of estuaries included the percentage of natural vegetation within the catchment, land use activities, catchment hydrology, tidal regime, disturbances to surrounding floodplains, estuary use, and changes in estuarine ecology (Heap et al. 2001; Turner et al. 2004). The criteria used by the HRC (2002) included the natural sensitivity and current conditions of the water body and its catchment, recognised ecosystem and resource conservation values, and other socio-economic factors. The HRC (2002) criteria relating to management strategies, and ICOLLs were classified as pristine, being in a healthy modified condition and targeted for repair. Although some ICOLL catchments of the current study are highly developed, the criteria considered when assessing the trace metal concentrations in fish tissues and sediments as described in Chapter 7, was derived from the Geosciences Australia database.

Geosciences Australia has produced a national database of Australian estuaries incorporating spatial, geographic, morphological and climatic data for each estuary (Heap et al. 2001; OzCoasts http://www.ozcoasts.gov.au). This database was used to classify the condition of ICOLLs within NSW using the following criteria that included the amount of modification done to an ICOLL to take it away from its pristine state, the factors that initiate this change, decide

3 Chapter 1: Introduction

whether it is susceptible to further change, and key management needs (NLWRA 2002). Using the Ozcoasts database criterion, the ICOLLs of the current study were classified as being near- pristine (Meroo and Termeil Lakes), modified (Avoca and Terrigal Lagoons) and extensively- modified (Cockrone and Wamberal Lagoons).

1.2.1 Intermittently Closed and Open Lakes and Lagoons (ICOLLs) There are approximately between 900-1 000 estuaries recognised throughout Australia (Turner et al. 2004). The NSW coast has 35 estuaries according to Bell and Edwards (1981) and West et al. (1985) upon which 45% of the estuaries are referred to as intermittently closed estuaries, coastal lakes or lagoons (Williams et al. 1998; Griffiths and West 1999). The term ICOLLs has been in use in NSW since 1998 and is gaining national recognition (Haines 2006). Abundant along both the south-western and south-eastern coasts of Australia, ICOLLs include wave- dominated estuaries, coastal lagoons and strandplain–associated coastal creeks (Ryan et al. 2003). Coastal lagoons are also known as closed, blind or inter-barrier estuaries.

This study relates mainly to ICOLLs that have a catchment size of approximately 10 km2 or less. The four main ICOLLs (Cockrone, Avoca, Terrigal and Wamberal Lagoons) are located near coastal settlements that have developed catchments, shallow central basins, ephemeral streams and a sandy barrier across the entrance (Bird 1967; Cheng 1981). ICOLLs of NSW located on the central and south-east coasts are generally located near areas that are highly industrialised and urbanised, support tourism and agricultural activities, and have regulated river flows (Edgar et al. 1999; Webster and Harris 2004). These factors can influence the hydrographic processes of ICOLLs by affecting the barrier status (Pollard 1994a). Hydrographic cycles of ICOLLs in NSW generally follow a similar pattern (Pollard 1994a). The cycle includes high evaporation rates during barrier closure and low rainfall periods. In contrast, water levels can increase from catchment runoff during heavy seasonal rainfall. Water levels reach a point where the barrier may be opened naturally, or in the majority of cases artificially by local councils. A period of tidal exchange with the sea follows, before river discharges and surf conditions result in the deposition of sediments at the entrance, eventually reforming a barrier. The natural cycle was historically dependent on location, rainfall patterns and catchment size. However, due to increased catchment development the natural progression has been disrupted by artificial openings legislated by many local councils to prevent flooding to properties that are adjacent to the ICOLLs (Pollard 1994a).

Barriers of ICOLLs are generally considered to be open if there is a connection between the ICOLLs and the sea, and there is regular movement of water in and out of the estuary. Closed barriers occur when sand forms across the entrance and there is no exchange of water between

4 Chapter 1: Introduction

the two environments. Barriers can remain closed or open for long periods of time, from hours to a few weeks or longer, depending upon the local weather and surf conditions.

1.3 Estuarine fish assemblages Estuarine fish studies in Australia have included permanently open estuaries, large barrier estuaries, coastal riverine systems and ICOLLs. South-western Australian estuaries have been well documented, especially the Lower Swan Estuary (Gaughan et al. 1990), Nornalup and Wilson Inlets (Potter and Hyndes 1994) and others (Humphries et al. 1992; Young et al. 1997; Young and Potter 2002; Hyndes et al. 2003). Studies along the NSW coast have mostly occurred in permanently open estuaries, such as Botany Bay (SPCC 1981; Rotherham and West 2002; York et al. 2006), Port Jackson (Clynick et al. 2008), Port Hacking (Rotherham and West 2002, Mazmunder et al. 2006) and Jervis Bay (Pollard 1973; Ferrell et al. 1993). Riverine studies have included the northern rivers and central coast regions of NSW (Gray et al. 1996; West and King 1996; Gray et al. 1998), with Tasmanian estuaries also being studied (Edgar et al. 1999). The general outcome of these studies was that permanently open estuaries and those with extended connections to the sea have a higher species richness and larger abundance of fishes when compared to ICOLLs.

Spatial and temporal variations of estuarine fishes result from the changing larval and juvenile fish assemblages originating from the continental shelf and variation in the factors that may guide these assemblages to estuaries (Robinson et al. 1983; Trnski 2002). Relevant factors include winds, coastal currents, lunar cycles (Kingsford and Finn 1997; Trnski 2001), tidal cycles and type of habitat (Watt-Pringle and Strydom 2003). Success of estuarine fish recruitment depends upon salinity, turbidity and water temperature (Hannan and Williams 1998; Strydom 2003), and the presence of seagrass meadows, which have high fish species richness and abundances (Bell et al. 1988; Gray et al. 1996; West and King 1996; Rotherham and West 2002). Estuarine fish assemblages of the south-western and south-eastern coastlines show many similarities, with many species common to both regions, including tarwhine (Rhabdosargus sarba), southern bream (Acanthopagrus butcheri), silver biddy (Gerres subfasciatus), sea mullet (Mugil cephalus), and bridled goby (Arenigobius bifrenatus) (Potter and Hyndes 1999).

Many southern hemisphere intermittent estuaries share similar chemical and physical qualities that suggest similarities in their fish assemblages (Pollard 1994a, 1994b). This is the case for many intermittent estuaries located along the Cape Coast of South Africa and in the Indo-Pacific region that show noticeable similarities in their fish faunas with south-western and south-eastern Australian intermittent estuaries (Pollard 1994b; Whitfield 1999). The major difference is that South African intermittent estuaries generally experience seasonal openings of entrances

5 Chapter 1: Introduction

(Cowley and Whitfield 2001), unlike south-eastern Australian intermittent estuaries that have more irregular openings. Fish assemblages have also been documented in similar shallow water habitats in Albania (Peja et al. 1996), Mexico (Warburton 1978; Vega-Cendejas and de Santillana 2004) and Portugal (Gordo and Cabral 2001).

1.3.1 Fish assemblages of NSW ICOLLs Fish assemblages of ICOLLs in NSW have only recently been documented. Early studies provided a snapshot of species found in ICOLLs as sampling was conducted on a short time frame. Studies included the Gosford Lagoons (Weate and Hutchings 1977), Smiths Lake (Robinson et al. 1983) and Dee Why Lagoon (Allan et al. 1985; Potter et al. 1986). However, recent studies have increased the awareness of ICOLLs as functional habitats for many larval, juvenile and adult fishes (Pollard 1994b; Griffiths 1998, 1999; Griffiths and West 1999; Jones and West 2005). Unlike permanently open estuaries, a common aspect of ICOLLS is reduced species richness and high abundances of a resident species (Allan et al. 1985; Young and Potter 2002). Species found to dominate NSW ICOLLS include Ambassis jacksoniensis (Ambassidae), Atherinosoma microstoma (Atherinidae), Philypnodon grandiceps (Eleotridae) and Arenigobius bifrenatus (Gobiidae) (Griffiths 1998, 1999; Jones and West 2005).

1.3.2 Recruitment of larval and juvenile fishes into ICOLLs Larval and juvenile fish recruitment into NSW coastal waters and estuaries is initially aided by currents emanating from the Coral Sea via the East Australian Current (EAC) (Middleton et al. 1997). The EAC flows inshore on the continental shelf until reaching an easterly protrusion of the land where it diverges from the coastline and is responsible for dispersing marine pollution from heavily-populated coastal areas and aids in improving water quality along coastal regions (Middleton et al. 1997; Roy et al. 2001). Different processes of recruitment are required due to the different types of estuaries found along Australia’s coastlines. In order to better understand these processes along with their hydrodynamic and physical characteristics there is a need to review and classify estuary types (Roy et al. 2001; Tagliapietra et al. 2009). This study uses classifications and terms relevant to estuarine systems found along the NSW coastline.

The existence of a barrier means that recruitment of larval and juvenile fishes from adjacent surf zones to ICOLLs is highly irregular (Bell et al. 2001; Griffiths 2001c; Strydom 2003). The possible recruitment linkages between ICOLLs and their adjacent surf zones along the NSW coast have not been well documented. Most recruitment studies in NSW ICOLLs relate to large barrier estuaries (Miskiewicz 1987; Trnski 2001), except for that of Geraghty (2004) who investigated the distribution of larval and juvenile fish assemblages of surf zones in relation to estuary outlets in Jervis Bay on the NSW south-east coast.

6 Chapter 1: Introduction

The importance of surf zones as habitats for larval and juvenile fishes has been recognised in Japan (Senta and Kinoshita 1985; Nanami and Endo 2007; Inui et al. 2010), Mauritius (Sato et al. 2008) and North America (Marrin-Jarrin et al. 2009). Furthermore, South African studies have documented the links between surf zone areas and ICOLLs (Whitfield 1989; Harris and Cyrus 1996; Cowley and Whitfield 2001; Strydom 2003). Many of these studies suggest that larval and juvenile fishes congregate in surf zones adjacent to ICOLL entrances (Cowley and Whitfield 2001; Strydom 2003). Typically, as barriers are generally closed, it has been suggested that fishes need to find alternate habitats in surf zones until these barriers open (Watt- Pringle and Strydom 2003).

When barriers are closed for extended periods, recruitment may occur by over-wash events (Cowley and Whitfield 2001; Strydom 2003; Kemp and Froneman 2004). Waves crash over closed barriers during storm events, washing larval and juvenile fishes into the closed ICOLL (Cowley and Whitfield 2001). Therefore, it can be assumed that over-wash events can aid fish recruitment into closed ICOLLs along the NSW coast. Also, if the waves are severe enough they may even cause scouring of the barrier, opening it naturally. However, further investigation of larval and juvenile fish assemblages in NSW surf zones is required, to identify the species found in these habitats and to determine if they utilise ICOLLs when conditions are favourable.

A potential influence on fish communities in NSW ICOLLs is artificial openings implemented by local councils. Artificial openings are used to improve the overall aesthetic and water quality of ICOLLs (Griffiths 1999; Jones and West 2005); however, the effects of artificial openings on the general ecology and fish recruitment is poorly understood, as barriers are usually not specifically opened to coincide with fish recruitment periods (Allan et al. 1985). More studies are needed to fully understand the most appropriate times for artificially opening ICOLLs when recruitment can be optimally maximized.

1.4 Ecology of ICOLLs The interaction of physical, environmental and biological factors influences the composition, abundance and distribution of fishes within ICOLLs (Whitfield 1999; Mariani 2001). The combination of these factors results in fish assemblages having low biological richness but high species abundance (Ward and Ashley 1989; Whitfield 1999).

1.4.1 Physical and water chemistry characteristics Barrier dynamics, water depth and habitat availability along with catchment development influence the spatial variations of fish assemblages within and between ICOLLs (Jones and West 2005). Barriers are formed by wave action and the effects of onshore and longshore sand

7 Chapter 1: Introduction

drift deposited across the entrance (Bird 1967). ICOLLs of NSW generally remain closed for longer periods than they are open (Griffiths 1999). The status of a barrier can influence tides, environmental parameters and recruitment of larval and juvenile fishes, all of which can determine temporal and spatial variations in fish assemblages (Cheng 1981; King and Hodgson 1995; Edgar et al. 1999).

Barrier dynamics play a variable role in the ecology of ICOLLs. Barrier openings influence salinity and turbidity (Pollard 1994a; Schallenberg 2010), along with habitat structure and water quality (Wilson et al. 2002). Barrier openings exert a significant influence on fish abundance in some situations (Vorwerk et al. 2003), but not others (Kok and Whitfield 1986). Gladstone et al. (2006) also found that changes in invertebrate fauna were not influenced by barrier openings.

The major physical factor influencing species richness and abundance of fishes in ICOLLs is salinity (Young et al. 1997; Griffiths 2001a). Salinity of ICOLLs results from the interactions of barrier status, seawater inflow, catchment run-off and evaporation. Small ephemeral streams also help produce hyposaline conditions in ICOLLs during heavy rain events due to increased fresh water inputs. Alternatively, hypersaline conditions can prevail during drier periods when water inputs from these inflowing streams are non-existent. These varying salinity conditions can result in spatial and temporal variations in both fish and invertebrate assemblages (Allan et al. 1985; Dye and Barros 2005a; Griffiths 2001a), as resident fish species are often able to tolerate sudden changes in salinity (Griffiths 2001a). For example, salinity tends to be higher near ICOLL entrances and species richness is generally greater there as marine species generally congregate in these localities (Griffiths 2001a).

Recruitment of many larval and juvenile fish species also occurs when salinity increases near open entrances as marine and transient species are able to enter from adjacent surf zones. Many fishes and invertebrate species rely on seagrass habitats during settlement; however, salinity conditions within and immediately above the seagrass canopy can influence the species richness of organisms utilising these habitats (Hyndes et al. 2003). A study by Lubbers et al. (1990) compared fish species richness of seagrass meadows and bare substrates, both with high salinities, and found species richness was lower in localities of seagrass meadows and bare substrate that had low salinities compared to similar habitats that had high ranges of salinity.

Turbidity of ICOLLs is influenced by barrier status, water depth, and the presence-absence of aquatic vegetation, rainfall, wind, and run-off. High turbidity is the result of increased particulate matter and nutrients within the water column, which may cause reduced visibility, provide protection from predators, increase food resources, and influence habitat preferences

8 Chapter 1: Introduction

(West and King 1996; Whitfield 1999). Water clarity is generally greatly improved during barrier closure but decreases rapidly when barriers are opened. Turbidity also affects vegetative characteristics, as clear water promotes growth of seagrass and algae (Bird 1967).

Due to the shallow nature of ICOLLs, water temperature in them generally mirrors air temperature. Water temperature increases during warmer months and decreases during cooler months, and these changes may be associated with seasonal variations in fish assemblages (Bennett 1989; Pollard 1994a). During warmer seasons food resources tend to increase, which generally correlates to an increase in fish species in ICOLLs (Yanez-Arancibia et al. 1994).

Water depth and surface area of ICOLLs are influenced by barrier status. Extended periods of barrier closure, in conjunction with decreases in salinity, lead to increases in water depth, surface area and algal growth (Bird 1967). Additional habitats are provided by algae, aquatic macrophytes and emergent reeds within flood zones (Becker and Laurenson 2008). Open barriers decrease water depth and surface area, causing habitat destruction, changes in water quality and fish kills (Wilson et al. 2002).

1.4.2 Habitats within ICOLLs The habitats of ICOLLs include open water, shorelines fringed by wetlands, sandy sediments near an intermittent barrier at the entrance, a central muddy basin, seagrasses, and algae (Cheng 1981). Seagrass meadows are well documented as important fish habitats; however, the lack of tidal exchange has resulted in many NSW ICOLLs being dominated by a salt-tolerant species of Ruppia (Pollard 1994a; Roy et al. 2001). Ruppia sp., commonly known as sea tassel, is not a true seagrass but a thread-thin perennial aquatic herb. It is widespread and found in most brackish environments as it is tolerant of a wide range of environmental conditions, including salinity changes and physical disturbances. It has also been shown to support a variety of fish species (Pollard 1994b; Jenkins et al. 1997).

True seagrass species such as Zostera sp. and Halophila sp. may also be present in ICOLLs (Pollard 1994a; Gray et al., 1998) and have been shown to host greater species richness and abundance of fishes compared to assemblages in unvegetated areas (Robinson et al. 1983; Allan et al. 1985; Pollard 1994a; Griffiths 2001c; Jones and West, 2005). In comparison, other studies by Allan et al. (1985) and Gray et al. (1996) have shown that bare substrates near seagrass areas have increased species richness and abundance due to fine substrates. For example, spatial segregation of benthic species such as gobiids is associated with areas having fine substrates, such as muddy basins (Gill and Potter 1993; Cowley and Whitfield 2001). ICOLLs also often

9 Chapter 1: Introduction

have large areas of floating and submerged algae that are potentially ideal habitats for many larval and juvenile fishes, but which have yet to be adequately recognised in the literature.

1.5 Feeding ecology of fishes in ICOLLs The feeding ecology of fishes in permanently open estuaries of NSW (Sanchez-Jerez et al. 2002; Mazumder et al. 2006), Queensland (Morton et al. 1987; Wilson and Sheaves 2001; Hollingsworth and Connolly 2006), Victoria (Crinall and Hindell 2004), Tasmania (Edgar and Shaw 1995) and south-western Western Australia (Prince et al. 1982; Gill and Potter 1993; Humphries and Potter 1993) is well documented. However, there are fewer studies of the feeding ecology of fishes of ICOLLs, with the exception of Western Australia (Sarre et al. 2000; Chuwen et al. 2007), Victoria (Becker and Laurenson 2007) and northern NSW (Hadwen et al. 2007).

Studies by Sarre et al. (2000), Chuwen et al. (2007) and Hadwen et al. (2007) are of particular interest as they compared the diets of species within and between ICOLLs. Sarre et al. (2000) and Chuwen et al. (2007) examined the diet of Acanthopagrus butcheri, an economically important species, within and between three south-western Australian ICOLLs. Hadwen et al. (2007) compared the diets of four economically important species, Acanthopagrus australis, Platycephalus fuscus, Sillago ciliata and Mugil cephalus, within and between two northern NSW ICOLLs. The latter study evaluated two contrasting methods of diet analysis. Firstly, by the common practice of evaluating gut contents for information on recent feeding; and, secondly by, using stable isotope signatures, a relatively new method that can determine food items digested over recent weeks to months. Both methods provided useful information in determining the dietary requirements of fishes in ICOLLs. Sarre et al. (2000) and Chuwen et al. (2007) showed that A. butcheri had marked variations in its diet between ICOLLs; however, this was not able to be confirmed by Hadwen et al. (2007) due to the limited numbers of specimens of this species found in each system. New South Wales ICOLLs are important nursery areas for many important commercial and recreational species (Griffiths 2001a), but dietary studies of these fishes have largely not been assessed in these environments. In order to establish what fish species are common in NSW estuaries, an examination of available food resources and the species that consume them needs to be undertaken as this can be an important resource for the state’s fisheries (Pollard 1994b).

Invertebrates are a major dietary item of fishes in ICOLLs, with the invertebrate fauna generally being dominated by polychaetes, molluscs and crustaceans (Sarre et al. 2000; Becker and Laurenson 2007; Chuwen et al. 2007). Although ICOLLs exhibit low temporal variability in abundances of invertebrate fauna (Weate and Hutchings 1977; Hutchings 1999), they receive

10 Chapter 1: Introduction

large inputs of detritus that many invertebrates utilise for food (Humphries et al. 1992; Whitfield 1999). The spatial distribution of invertebrates in ICOLLs is influenced by primary productivity, temperature, salinity, algal biomass and sediment characteristics (Dye and Barros 2005b; Gladstone et al. 2006). Abundance and species richness of invertebrates are generally lower in the upper reaches of ICOLLs, compared to near their entrances (Dye and Barros 2005b). Habitat disturbances such as barrier openings have no detectable effect on invertebrate assemblages, as most invertebrates are highly mobile and colonisation of disturbed areas is generally rapid (Gladstone et al. 2006).

1.6 Anthropogenic impacts on ICOLLs ICOLLs are naturally stressed ecosystems, with many being used for the disposal of urban and industrial wastes. The effects of pollutants on ICOLL ecology are of great concern as many contaminants are retained within ICOLLs and not flushed out until barriers are opened. A national overview of ICOLLs concluded that the majority were in a healthy modified condition, or slightly better (HRC 2002). Nationally, 974 estuaries have been classified with 50% found to be in a near-pristine condition, 22% largely unmodified, and 17% modified, with 1% extensively modified (Turner et al. 2004). Within NSW one ICOLL, Nadgee Lake, on the far south coast, has been classified as the only ICOLL remaining in a truly pristine condition (HRC 2002). Indicators used to monitor ICOLL health include chlorophyll-a, turbidity, the abundance of macrophytes and the structure of fish assemblages (Roper et al. 2011).

A cocktail of contaminants, including organic pollutants, nutrients, trace metals and sediments enter ICOLLs via stormwater run-off, sewage, or aerial deposition (Zann 2000). In Australian ICOLLs two of these contaminants, trace metals and nutrients, are a major concern to the overall health of ICOLLs. Both contaminants are the result of catchment modifications such as the clearing of natural vegetation for grazing and/or crops and urban and industrial development (Cheng 1981; Roy et al. 2001). The effects of catchment modifications on the species richness and ecology of fish assemblages of ICOLLs are yet to be fully understood. However, management of catchment development and artificial barrier openings are important, as the impact of anthropogenic inputs can be amplified during closure, which can ultimately affect fish health, recruitment and species richness within ICOLLs (Griffiths and West 1999; Islam and Tanaka 2004).

The major concern for ICOLLs is nutrient loading or eutrophication. The effects of eutrophication are widespread and are more immediate and visible compared to trace metal contamination, which is usually gradual and can persist for many years (Davis et al. 2001, Beltrame et al. 2009). Major problems arising from eutrophication include accelerated growth

11 Chapter 1: Introduction

of macroalgae and filamentous algae, which can change water quality characteristics (such as dissolved oxygen levels, water clarity, pH) and destroy seagrasses, all of which can result in changes to species composition of invertebrate and fish faunas (Islam and Tanaka 2004). Extreme cases of eutrophication can result in the death of invertebrates and fishes due to anoxic conditions (Islam and Tanaka 2004).

Trace metals are found naturally in the bedrock of terrestrial and aquatic ecosystems and only become toxic after being released into the environment at concentrations that are above a predetermined threshold (Padmini and Geetha 2007). Many metals, including zinc, copper and selenium, are essential elements needed for growth, development and reproduction in fishes, whereas cadmium and lead are regarded as non-essential elements, having no biological function (Kirby et al. 2001a). Initially, most metal pollutants were considered to be products from industrial waste. Lead and cadmium are products of weed and pest sprays, domestic effluents and petroleum-based wastes (Payne et al. 1997; Edwards et al. 2001). Zinc originates from galvanised iron waste, and copper originates from the brake linings of vehicles (Payne et al. 1997; Davis et al. 2001). These metals are flushed into ICOLLs by stormwater runoff (Davis et al. 2001). Steel works and coal-fired electric power generation stations produce ash contaminated with particulate metals, which can find its way into aquatic systems (Chenhall et al. 2001).

Increased levels of trace metals in ICOLL sediments are generally the result of anthropogenic influences (Payne et al. 1997; Chenhall et al. 2001; Gillis and Birch 2006). However, Jones et al. (2003) found that sediment samples in Burrill Lake, NSW, had increased trace metal concentrations due to the leaching of the natural bedrock formation rather than from anthropogenic influences. Once established in the sediment, trace metals are readily taken up by the flora and fauna and can be retained for long periods (Batley 1987; Kirby et al. 2001a; Brown et al. 2004; Waring et al. 2005; Roach et al. 2008; Birch and Hogg 2011). Also, disturbed sediments due to dredging or reclamation work can release trace metals back into the water column (Batley 1987).

Fishes susceptible to trace metal pollution accumulate these elements within their edible tissues, which is of great concern to human health. The effects on fishes are also of great concern as accumulation of trace metals generally occurs in older fish and the effects, although not immediately obvious, can include cytogenic damage to brain tissue, increased susceptibility to infection, deformities in larvae, and, in severe cases, death (Batley 1987; Kirby et al. 2001a; Brown et al. 2004; Waring et al. 2005; Roach et al. 2008; Birch and Hogg 2011). Trace metal accumulation in fishes is species-dependent and determined by feeding habits (Alquezar et al.

12 Chapter 1: Introduction

2006; Uysal et al. 2008), salinity and water temperature (Yilmaz 2005), and physiological processes (Pourang and Amini 2001; Alquezar et al. 2006; Uysal et al. 2008). Mugil cephalus is a commercially and recreationally fished species that has been studied extensively for metal accumulation in estuarine environments of south-eastern Australia (Kirby et al. 2001a; Roach et al. 2008). Studies by Kirby et al. (2001a) and Roach et al. (2008) were undertaken in Lake Macquarie, a large barrier estuary with industrial areas surrounding the shoreline. Results from both studies showed that this fish’s liver had higher concentrations of metals compared to other tissues analysed, except for the gonads, which had higher levels of zinc.

As with many areas of study regarding ICOLLs, there is limited knowledge about the effects of trace metal concentrations on the general ecology of ICOLLs. Some pristine environments can be found along the NSW coast and comparisons between these environments and urbanised ICOLLs need to be documented to determine background levels of metal contamination.

1.7 Conclusion ICOLLs are an example of the range of estuarine environments occurring in south-eastern Australia. They provide habitats for a diversity of flora and fauna. The invertebrate fauna of ICOLLs is dominated by polychaetes, molluscs and crustaceans, and the fish fauna, although having lower species richness than in other estuarine environments, is distinctive. ICOLLs have also been shown to be important nursery habitats for many species of fishes, with recruitment occurring from adjacent surf zones once the barrier has been opened. ICOLLs also provide aesthetic and recreational opportunities for human activities. Increasing pressure has been placed on the natural integrity of ICOLLs, especially those located in highly-populated areas. Physical, environmental and biological interactions can affect the composition, abundances and distribution of the flora and fauna of ICOLLs. The potential ecological and environmental effects from the increased frequency of barrier openings that is occurring in response to human development of the shorelines and catchments of ICOLLs are also of concern.

Although, many studies have examined the flora and fauna of ICOLLs, there are still many gaps that remain in the overall understanding of the processes that affect the flora and fauna of ICOLLs along the south-eastern coast of NSW. There is a lack of information on the effects of frequent artificial barrier openings, increased catchment development, and the resulting increase of pollutants, on the recruitment of flora and fauna into ICOLLs. Also there are no comparative studies between impacted and pristine ICOLLs, which might explain whether ICOLLs are affected by any of the factors described earlier.

13 Chapter 1: Introduction

1.8 Current study The current study was largely undertaken on the Central Coast of NSW near the city of Gosford, to the north of Sydney, and also on the NSW near south coast near Ulladulla. The study examined the spatial and temporal variations of fish assemblages of four Central Coast ICOLLs (Cockrone, Avoca, Terrigal and Wamberal Lagoons) and the factors that may affect the species richness and abundances of these assemblages. Two near-pristine ICOLLs, Termeil and Meroo Lakes on the near South Coast, were used for comparison in a study of trace metals. The current study is unique in that it compares the effects of barrier openings on the general ecology of ICOLLs, recruitment processes of larval and juvenile fishes, and the spatial and temporal variation of fish assemblages and their dietary preferences; it also compares trace metal concentrations of fishes in near-pristine, modified and extensively-modified ICOLL environments.

1.9 Aims of study The aims of this study were thus: 1. To determine the invertebrate fauna of Central Coast ICOLLs and establish the relative importance of barrier openings and variations in environmental parameters (salinity, turbidity, water temperature) on the spatial and temporal variations in invertebrate assemblages (Chapter 3).

2. To identify the assemblages of larval and juvenile fishes occurring in Central Coast ICOLLs and determine the effects of barrier openings on larval and juvenile fish recruitment by identifying larval and juvenile assemblages in ICOLL entrances and adjacent surf zones and comparing changes in these assemblages before and after a barrier opening (Chapter 4).

3. To identify the fish assemblages of Central Coast ICOLLs and establish the relative importance of barrier openings, variations in environmental parameters (salinity, turbidity, water temperature, and dissolved oxygen), habitat characteristics (algal biomass, sediment composition) and catchment characteristics on the spatial and temporal variations in fish assemblages (Chapter 5).

4. To determine the dietary preferences of the most abundant fish species in each ICOLL, Acanthopagrus australis (Cockrone Lagoon), Atherinosoma microstoma (Avoca and Wamberal Lagoons), Ambassis jacksoniensis (Terrigal Lagoon), and evaluate the effects of barrier openings on variations in the diets of each species (Chapter 6).

14 Chapter 1: Introduction

5. To determine the levels of trace metal concentrations in sediments and tissues of Mugil cephalus by comparing ICOLLs classified as near-pristine (Termeil and Meroo Lakes), modified (Avoca and Terrigal Lagoons) and extensively-modified ICOLLs (Cockrone and Wamberal Lagoons) (Chapter 7).

1.10 Thesis structure Chapter Two is a description of the study area containing the six ICOLLs sampled throughout the study. Chapter Three describes the invertebrate fauna and environmental parameters of the four ICOLLs near Gosford. Invertebrate fauna was sampled bimonthly for 1 yr, with environmental parameters sampled fortnightly for 1 yr.

Chapter Four describes spatial and temporal variations in larval and juvenile fish assemblages near ICOLL entrances and in adjacent surf zone areas south of, immediately adjacent to, and north of ICOLL entrances. Larval and juvenile fish assemblages at each site were compared before and after barrier openings. Sampling by larval beach seine nets occurred bimonthly for 1 yr before and/or after a barrier opening.

Chapter Five compares spatial and temporal variations of fish assemblages in relation to environmental parameters within and between the four Central Coast ICOLLs (Cockrone, Avoca, Terrigal and Wamberal Lagoons). Two methods (seine and multi-panel gill netting) were used to collect fishes. Sampling occurred bimonthly for 16 mo.

Chapter Six describes the dietary preferences of the dominant species of fish by gut contents analysis and determines the changes in diet from before to after barrier openings.

Chapter Seven determines trace metal concentrations in ICOLL sediments and tissues of the sea mullet Mugil cephalus and compares these concentrations between near-pristine (Termeil and Meroo Lakes), modified (Avoca and Terrigal Lagoons) and extensively-modified (Cockrone and Wamberal Lagoons) ICOLLs.

Chapter Eight provides a general discussion of the project highlights, along with the study’s limitations, conclusions, and the opportunities for future research as a result of this study.

15 Chapter 2: Study area

Chapter 2: Study area

16 Chapter 2: Study area

2.1 Study area The present study was carried out in ICOLLs on the coast of New South Wales (NSW) located north and south of Sydney (Figure 2.1). The northern location is situated near Gosford and relates to studies described in Chapters 3-7, while the southern location is situated near Ulladulla and relates only to Chapter 7. Adjacent surf zones were studied for northern ICOLLs only.

2.2 Northern Site-Gosford The northern area is located on the central NSW coast near Gosford, which is approximately 90 km north of Sydney. This region lies in the warm temperate Central Eastern Province (Hawkesbury Shelf Bioregion) that is characterized by high-energy sandy coastlines, barrier sand estuaries with well-developed coastal lakes, rocky headlands, cliffs and long-drowned sandstone river valleys that support 50 estuaries with a total area of 934 km2 (Zann 2000). The Gosford region has numerous coastal waterways and beaches, making the area a popular residential and tourist destination. The majority of the study was undertaken in four ICOLLs that are all located along a 10 km stretch of coastline, within the boundaries of Gosford City Council. These ICOLLs have been classified as group four estuaries (intermittently closed) and saline coastal lagoons (estuary type eight) (Roy et al. 2001). Barriers form across their entrances, and when opened naturally or artificially they flow into adjacent surf zones. The Australian Height Datum (AHD) establishes a berm height and when the water level of the ICOLLs attains this height barriers are artificially opened by Gosford City Council. No powerboat activity is allowed in these ICOLLs.

2.2.1 Climate The general climate of the region is classified as warm temperate (Zann, 2000). Temperature and rainfall readings for the region are recorded at Gosford (Narara Research Station) Automatic Weather Stations (station number 061087). The average annual temperature is 23°C with mean daily maximum temperatures ranging between 17.5°C in July and 27.5°C in January. Mean minimum daily temperatures range between 4.6°C in July and 17.1°C in February. The average annual rainfall is 1306.5 mm, with June being the wettest month and September being the driest month (BoM 2010).

17 Chapter 2: Study area

Figure 2.1. Study location of ICOLLs at the northern sites (Gosford) and southern sites (Ulladulla).

18 Chapter 2: Study area

2.2.2 Catchment characteristics The Gosford district has features characteristic of a drowned coastline formed approximately 6 000 years ago. However, the ICOLLs have a more recent origin featuring rocky headlands joined by sandy beaches with small water bodies separated from surf zones by barriers (Albani and Brown 1976). These ICOLLs have small catchments with varying degrees of development and remnant natural areas. Seawall constructions are prominent around foreshores, especially near bridge structures and where urban dwellings line the foreshores. The general topography of catchments is comprised of low-lying areas around the foreshore which rise steeply to form gullies. Soils are derived from the Narrabeen group that is found on most of the hills and ridges of the area and originates from Triassic sandstone (208-245 million years old). These shallow soils are susceptible to erosion when disturbed and have the potential to produce acid sulphate soils. Outcropping rocks of sandstone and/or siltstone of the Terrigal Formation, with underlying Patonga Claystone, are found only in the Wamberal catchment (Albani and Brown 1976; GCC 1987).

ICOLL sediment and habitat (seagrass, algae) distribution were quantified by transect surveys across each ICOLL and from the published literature (Weate and Hutchings 1977; West et al. 1985). Percentage grain size composition was used to determine coarse sand (≥ 1 mm), medium sand (>0.5 mm), fine sand (>212 µm), and silt/ clay (<212 µm).

2.2.3 Cockrone Lagoon Cockrone Lagoon (33.494°S 151.429°E) is the southernmost ICOLL in the northern study area and is classified as extensively-modified (Heap et al. 2001; OzCoasts 2012). The catchment has an area of 6.7 km2 and water area of 0.32 km2 (Roy et al. 2001). The main tributary, Cockrone Creek, is located on the western side draining 4.2 km2 of the catchment. Several other tributaries including Merchant Creek drain the rest of the catchment (Figure 2.2). Approximately 25% of the catchment is disturbed, due to urban development (9%) and agricultural activities (16%). The remaining catchment area is forest (69%) and water area (6%) (Cardno Lawson Treloar 2010).

19 Chapter 2: Study area

Figure 2.2. Aerial view of Cockrone Lagoon (OEH 2011).

Sediment samples collected from nine sites in Cockrone Lagoon showed that the lagoon bed was mainly fine sand (Figure 2.3), with grain sizes differing between individual sites (Figure 2.4). Fine sand was prominent at all sites, and medium sand also found at all sites. Silt and clay were present at sites 4 to 9, but absent from sites 1 to 3. Coarse sand was greatest at sites 4 to 7. The central basin occupies 0.20 km2 with the algae Chara sp. dominating the aquatic vegetation, along with some patchy areas of Ruppia sp. The backwaters of the lagoon have large meadows of Ruppia sp. with patchy areas located near the entrance. The basin is entirely covered with Chara sp., while floating mats of Enteromorpha intestinalis can be seen drifting on the surface (Figure 2.5).

The fringing vegetation has extensive areas of Phragmites australis near the entrance and scrublands of Baumea juncea, Juncus krausii and Melaleuca ericifolia along with forests of Melaleuca quinquenervia, Melaleuca stypheliodes and Casuarina glauca fringing the majority of the ICOLL. Water depth of Cockrone Lagoon is shallow in the upper reaches (generally <1 m), becoming deeper near the entrances, with depths up to 3 m, and an average depth of 0.6 m (Table 2.2). The berm height for opening the barrier is 2.5 m. The main recreational activities of swimming and fishing occur near the entrance.

20 Chapter 2: Study area

Figure 2.3. Collecting sites (1-9) and sediment types of Cockrone Lagoon, May 2004. Areas not coloured indicate sites where sediment was not collected.

21 Chapter 2: Study area

100

40 % particle composition particle %

0 1 2 3 4 5 6 7 8 9 Site

silt/clay fine sand medium sand coarse sand

Figure 2.4. Percentage grain size composition of ambient sediment samples collected from nine sites within Cockrone Lagoon in May 2004.

22 Chapter 2: Study area

Figure 2.5. Seagrass and algal habitats of Cockrone Lagoon obtained by field measurements during 2004 and derived from aerial photos and West et al. (1985). Fortnightly sampling sites for salinity, turbidity and water temperature and bimonthly invertebrate collection are labelled 1 -6 (see Chapter 3). Areas not coloured indicate sites where seagrasses and/or algae were not present or areas that were not assessed.

23 Chapter 2: Study area

2.2.4 Avoca Lagoon Avoca Lagoon (33.465°S 151.436°E) is an irregularly-shaped ICOLL and is classified as a modified ICOLL (Heap et al. 2001; OzCoasts 2012). Avoca Lagoon has the largest catchment area (10.4 km2) and water area (0.65 km2) of the Central Coast ICOLLs (Roy et al. 2001) and has four arms with the main tributary, Saltwater Creek, draining 6.7 km2 of the catchment (Figure 2.6). Approximately 46% of the catchment is disturbed, due to urban development (25%) and agricultural activities (21%). The remaining catchment area is forest (46%) and water area (8%) (Cardno Lawson Treloar 2010).

Figure 2.6. Aerial view of Avoca Lagoon (OEH 2011).

Sediment samples collected from 15 sites in Avoca Lagoon showed that the lagoon bed was mainly fine sand (Figure 2.7), with grain sizes differing between individual sites (Figure 2.8). Fine sand was prominent at sites 1 and 14. Coarse sand was prominent at sites 2 to 13, with silt and clay also evident at sites 2 to 15, but absent from sites 1 and 14.

The central basin occupies 0.46 km2 with seagrasses covering an area of 0.161 km2. Ruppia sp. is the dominant aquatic vegetation along with small beds of Zostera sp. and floating mats of Enteromorpha intestinalis. Meadows of Ruppia sp. are found throughout the southern, western and northern arms of the ICOLL. Small patches of Zostera sp. are found near the entrance. Shallow water areas had large areas of attached and floating mats of algae (Figure 2.9). Fringing vegetation includes large areas of Phragmites australis and Juncus krausii in the northern arm, along with forests of Melaleuca quinquenervia, and Casuarina glauca found around the northern and western arms of the ICOLL and on the island. Water depth of Avoca Lagoon was greatest in the central basin (4 m), with depths of <1 m in the northern, western and southern arms. The average water depth is 0.4 m (Table 2.2). The berm height for opening the barrier is 2.1 m. The main recreational activities are swimming and fishing along with commercial boat hire near the entrance.

24 Chapter 2: Study area

Figure 2.7. Collecting sites (1-15) and sediment types of Avoca Lagoon, May 2004. Areas not coloured indicate sites where sediment was not collected.

25 Chapter 2: Study area

100

40 % particle composition particle %

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Site

silt/clay fine sand medium sand coarse sand

Figure 2.8. Percentage grain size composition of ambient sediment samples collected from fifteen sites within Avoca Lagoon in May 2004.

26 Chapter 2: Study area

Figure 2.9. Seagrass and algal habitats of Avoca Lagoon obtained by field measurements during 2004 and derived from aerial photos and West et al. (1985). Fortnightly sampling sites for salinity, turbidity and water temperature and bimonthly invertebrate collection are labelled 1 -6 (see Chapter 3). Areas not coloured indicate sites where seagrasses and/or algae were not present or areas that were not assessed.

27 Chapter 2: Study area

2.2.5 Terrigal Lagoon Terrigal Lagoon (33.444°S 151.444°E) is classified as a modified ICOLL (Heap et al. 2001; OzCoasts 2012). It has a catchment area of 8.7 km2 and water area of 0.23 km2 (Roy et al. 2001). The northern tributary is the North Arm Creek draining 4.5 km2 and the West Arm Creek draining 3.7 km2 of the catchment (Figure 2.10). Approximately 80% of the catchment is disturbed, due to urban development (36%) and agricultural activities (44%). The remaining catchment area is forest (16%) and water area (4%) (Cardno Lawson Treloar 2010).

Figure 2.10. Aerial view of Terrigal Lagoon (OEH 2011).

Sediment samples collected from 12 sites in Terrigal Lagoon showed that the lagoon bed was mainly fine sand (Figure 2.11), with grain sizes differing between sites (Figure 2.12). Fine sand was prominent at sites near the entrance (sites 1 to 3) as well as at site 9. Medium sand was prominent at site 8, with the proportion of silt and clay increasing away from the entrance.

The central basin occupies 0.23 km2 and is totally devoid of seagrasses and algae. Previous maps of the ICOLL show areas of Zostera sp. (West et al. 1985), however during the current study only a small poor quality patch (<1 m2) of Zostera sp. was observed in an area previously described as containing Zostera by West et al. (1985). No seagrasses or algae were found during the April 2004 survey. Fringing vegetation mainly occurs around the western arm and consists of Phragmites australis, Juncus krausii and Casuarina glauca. Terrigal Lagoon is the only lagoon to have patchy areas of the mangrove Avicennia marina, mainly located along the western arm foreshore. Most of the foreshore areas have been significantly altered with rock walls. Water depth of Terrigal Lagoon was greatest in the northern arm (up to 4 m), with the western arm’s being <0.5 m. The average water depth is 0.5 m (Table 2.2). The berm height for opening the barrier is 1.2 m. The main recreational activities are swimming and fishing and commercial boat hire near the entrance.

28 Chapter 2: Study area

Figure 2.11. Collecting sites (1-12) and sediment types of Terrigal Lagoon, May 2004.

29 Chapter 2: Study area

100

40 % particle composition particle %

0 1 2 3 4 5 6 7 8 9 10 11 12 Site

silt/clay fine sand medium sand coarse sand

Figure 2.12. Percentage grain size composition of ambient sediment samples collected from twelve sites within Terrigal Lagoon in May 2004.

30 Chapter 2: Study area

31 Chapter 2: Study area

2.2.6 Wamberal Lagoon Wamberal Lagoon (33.430°S 151.449°E) is classified as an extensively-modified ICOLL (Heap et al. 2001; OzCoasts 2012). It has the smallest catchment area of 5.7 km2 and a water area of 0.49 km2 (Roy et al. 2001). The main tributary is Forrester’s Creek draining 2.6 km2 of the northern catchment (Figure 2.14). Approximately 67% of the catchment is disturbed, due to urban development (31%) and agricultural activities (36%). The remaining catchment area is forest (24%) and water area (9%) (Cardno Lawson Treloar 2010).

Figure 2.14. Aerial view of Wamberal Lagoon (OEH 2011).

Sediment samples collected from 13 sites in Wamberal Lagoon showed that the lagoon bed was mainly coarse and fine sand (Figure 2.15). Grain size composition differed between sites (Figure 2.16). Fine sand was prominent at site 1, and coarse sand was prominent at sites 2 to 13. The occurrence of silt and clay increased from sites 4 to 13. Rocky outcrops are also prominent near site 2.

The aquatic vegetation is dominated by patchy areas of Ruppia sp. and small beds of Zostera sp. near the entrance (West et al. 1985; Cheng 1992), along with the algae Chara sp. and floating mats of Enteromorpha intestinalis and Cladophora sp. (Nash 1986; Cheng 1992). Algae were found near the outlet of the creek (Figure 2.17). The central basin occupies 0.41 km2 and there is a total seagrass area of 0.245 km2. Fringing vegetation consists of Phragmites australis, Baumea juncea, Juncus krausii and Melaleuca ericifolia on the northern side with forests of M. ericifolia and M. nodosa found near Forresters Creek. Scrubs of Leptospermum sp. and forests of M. quinquenervia are also found around the foreshores. Water depth of Wamberal Lagoon is greatest near the entrance (up to 3 m), and shallow in the upper reaches (<1 m). The average water depth is 1.7 m (Table 2.2). The berm height for opening the barrier is 2.4 m. The main recreational activities are swimming, fishing and recreational boating near the entrance.

32 Chapter 2: Study area

Figure 2.15. Collecting sites (1-13) and sediment types of Wamberal Lagoon, May 2004. Areas not coloured indicate sites where sediment was not collected.

33 Chapter 2: Study area

100

40 % particle composition particle %

0 1 2 3 4 5 6 7 8 9 10 11 12 13 Site

silt/clay fine sand medium sand coarse sand

Figure 2.16. Percentage grain size composition of ambient sediment samples collected from thirteen sites within Wamberal Lagoon in May 2004.

34 Chapter 2: Study area

35 Chapter 2: Study area

2.2.7 Adjacent surf zones Surf zone sites used in the current study included Copacabana, Avoca, Terrigal and Wamberal Beaches, located adjacent to the four previously-described ICOLLs. The beaches found in this region are representative of beaches found along the NSW coastline, and all exhibit similar physical characteristics (Table 2.1).

Table 2.1. Physical characteristics of surf zones (after Short 2007) adjacent to ICOLLs used in this study. Aspect is (ESE) east south easterly, and (ENE) east north easterly. Beach types are (RBB) rhythmic bar and beach, (TBR) transverse bar and rip, (LTT) low tide terrace beach. Surf zone Aspect Beach length Average wave height Beach type (km) (m) Copacabana Beach ESE 1.1 1.5 RBB Avoca Beach ESE 1.7 1.0-1.5 TBR/RBB Terrigal Beach ENE 0.7 0.5-1.5 TBR/LTT Wamberal Beach ENE 2.1 1.0-1.5 TBR/RBB

2.3 Southern Site–Ulladulla The study area here is located on the near south coast of NSW approximately 15 km south of Ulladulla and approximately 191 km south of Sydney (Figure 2.1). This region is located in the South-Eastern Biotone and Batemans Bay Shelf Bioregion, which is characterized by short sandy or rocky beaches, rocky bays and 44 estuaries with a total area of 181 km2 (Zann 2000). Like Gosford, this region has numerous coastal waterways and beaches making the area a popular residential and tourist destination. Much of the area where the ICOLLs are located has extensive areas of national parks. The study was undertaken in two ICOLLs that are located within 2 km of each other in the Meroo National Park. These ICOLLs were chosen due to their similar characteristics to the ICOLLs studied near Gosford (Table 2.2). Unlike Gosford ICOLLs, barriers at the southern sites mostly open naturally.

2.3.1 Climate The general climate of the region is described as cool temperate (Zann 2000). Temperature and rainfall readings for the region are recorded at Nerriga Composite Research Station Automatic Weather Stations (station number 069049) located at 35.12°S 150.08°E, and an elevation of 630 m. The average annual temperature is 19.1°C with mean daily maximum temperatures ranging between 11.8°C in July and 26.3°C during January. Mean minimum daily temperatures range between 5.4°C in July and 13.8°C in February. The average annual rainfall is 761.3 mm, with March being the wettest month and September being the driest month (BoM 2010).

36 Chapter 2: Study area

Table 2.2. Summary and comparison of ICOLL characteristics based on Roy et al. (2001), BoM (2010) and OEH (2011). IV= intermittently closed estuary; 8 = saline coastal lagoon; Evolution stage: A = youthful, B = intermediate and C = semi-mature, I = intermittent entrance. ICOLL Classification Entrance Catchment Water Water Average condition area (km2) area volume depth (m) (km2) (MI) Wamberal IV/8/B I 5.8 0.5 880.2 1.7 Terrigal IV/8/B I 8.9 0.3 151.2 0.5 Avoca IV/8/A I 10.8 0.7 293.2 0.4 Cockrone IV/8/B I 6.9 0.3 187.4 0.6 Termeil IV/8/C I 14.0 0.6 397.9 0.7 Meroo IV/8/C I 19.3 1.4 1296.8 0.9

2.3.2 Catchment characteristics The ICOLLs were formed during the early Holocene by sea level rises inundating river valleys. Progressive infilling with sediment accompanied by deposition of Quaternary alluvium around the ICOLLs and the formation of coastal barrier dunes, led to the present-day shallow water bodies being typically closed to the ocean (NPWS 2005). Meroo National Park has an area of 36.62 km2 and is located 15 km south of Ulladulla and 30 km north of Batemans Bay. Both Termeil and Meroo Lakes are contained in the southern portion of the national park. The majority of the area is underlain by rocks of the Permian Conjola Formation (conglomerate, sandstone and silty sandstone), with Quaternary sand dunes behind the beaches and alluvium around the lakes (NPWS 2005).

2.3.3 Termeil Lake Termeil Lake (35.46°S 150.39°E) is classified as near-pristine based on the catchment and ICOLL having little or no human impact (Heap et al. 2001; OzCoasts 2012). The catchment has an area of 14 km2 and water area of 0.6 km2. Up to 47% of the catchment surrounding the lake is national park or state forest (Figure 2.18). Approximately 31% of the catchment is disturbed, which includes urban development (1%), and grazing and cleared land (30%). Undisturbed forest areas contribute 65% of the catchment, with other land use activities such as recreational areas contributing 4% of the catchment (Roper et al. 2011). The central basin occupies 0.35 km2. The fringing vegetation includes scrublands of Baumea juncea and Melaleuca ericifolia, along with forests of Casuarina glauca. The lake has been commercially fished with catches including black bream (Acanthopagrus butcheri), yellowfin bream (Acanthopagrus australis), luderick (Girella tricuspidata), sea mullet (Mugil cephalus) and sand whiting (Sillago ciliata). Water depths in Termeil Lake were not measured; however, the average water depth is reported

37 Chapter 2: Study area

as 0.7 m (OEH 2011). Recreational activities include canoeing; jet skiing, power boating, swimming and fishing.

Figure 2.18. Aerial view of Termeil Lake (OEH 2011).

2.3.4 Meroo Lake Meroo Lake (35.48°S 150.39°E) is classified as near-pristine based on the catchment and ICOLL having little or no human impact (Heap et al. 2001; OzCoasts 2012). The catchment has an area of 19.3 km2 and a water area of 1.4 km2. Up to 39% of the catchment surrounding the lake is national park or state forest (Figure 2.19). Approximately 24% of the catchment is disturbed, which includes urban development (2%) and grazing and irrigated land (22%). Undisturbed forest areas contribute 70% of the catchment, with other landuse activities such as recreational areas contributing 6% of the catchment (Roper et al. 2011). The central basin occupies 0.63 km2. The fringing vegetation of the ICOLL has scrublands of Baumea juncea and Melaleuca ericifolia, along with areas of spikerush Eleocharis sp., cumbungi Typha sp. and sawsedge Gahnia sieberiana (Gaia Research 2008). Water depths in Meroo Lake were not measured; however, the average water depth is reported as 0.9 m (OEH 2011). Recreational activities include canoeing; jet skiing, power boating, swimming and fishing.

38 Chapter 2: Study area

Figure 2.19. Aerial view of Meroo Lake (OEH 2011).

2.4. Sampling regime The sampling regime for the collection of invertebrate fauna, larval and juvenile fishes, fish fauna, gut analysis and trace metal concentrations in fish tissue and sediments for this study was conducted between October 2004 and April 2012. Sampling dates, barrier openings, the number of sites sampled and the number of total samples collected for the northern ICOLLs are summarised in Tables 2.3 to Table 2.6. For southern ICOLLs, Meroo Lake was sampled in November 2011 and February 2012 (total number of sites sampled n=4 and the total number of fish samples collected n=3) and Termeil Lake was sampled in March 2012 (total number of sites sampled n=2 and the total number of fish samples collected n=4). No barrier openings have been recorded at both these ICOLLs for a few years.

39 Chapter 2: Study area

Table 2.3. Sampling dates, barrier openings, the number of sites sampled and the total number of samples collected of invertebrate fauna, larval and juvenile fishes (also in adjacent surf zones), fish fauna, gut analysis and trace metal concentrations in fish tissue and sediments at Cockrone Lagoon between October 2004 and April 2012. *denotes no sampling in surf zones due to bad weather conditions. Chapter 3–Invertebrate sampling Sampling dates Barrier opened No. of sites Total no. of samples taken 2004 Dec 4 6 18 Dec 20 2005 Feb 26 6 18 Apr 24 6 18 Jun 19 6 18 Aug 27 6 18 Oct 22 6 18 Chapter 4- Larval and juvenile fishes Sampling dates Barrier opened No. of sites Total no. of samples taken 2006 Apr 19 4 16 Jun 19 4 16 Aug 2 4 16 Sep 7 Sep 19 4 16 Nov 13 4 16 2007 Jan 28 4 16 Mar 12* 1 4 Chapter 5-Fish assemblages Sampling dates Barrier opened No. of sites Total no. of samples taken 2009 Feb 25 5 30 Apr 15 5 30 Jun 15 Jun 23 Jul 27 5 30 Sep 11 5 30 Nov 12 5 30 2010 Jan 20 5 30 Mar 10 5 30 Mar 15 5 30 Jun 15 5 30 Chapter 6-Dietary studies Sampling dates Barrier opened No. of sites Total no. of samples taken 2009 Feb 25 5 120 Apr 15 2 60 Jun 15 Jun 23 Nov 12 5 150 Chapter 7-Trace metal concentrations Sampling dates Barrier opened No. of sites Total no. of samples taken 2012 Feb 16 1 10

40 Chapter 2: Study area

Table 2.4. Sampling dates, barrier openings, the number of sites sampled and the total number of samples collected of invertebrate fauna, larval and juvenile fishes (also in adjacent surf zones), fish fauna, gut analysis and trace metal concentrations in fish tissue and sediments at Avoca Lagoon between October 2004 and April 2012. Chapter 3-Invertebrate sampling Sampling dates Barrier opened No. of sites Total no. of samples taken 2004 Oct 1 Dec 4 6 18 2005 Feb 26 6 18 Apr 24 6 18 Jun 19 6 18 Jul 1 Aug 27 6 18 Oct 10 6 18 Chapter 4-Larval and juvenile fishes Sampling dates Barrier opened No. of sites Total no. of samples taken 2006 Apr 20 4 16 Jun 1 4 16 Jun 6 Jun 15 4 16 Aug 16 4 16 Sep 8 Sep 29 4 16 Nov 27 4 16 2007 Jan 29 4 16 Mar 13 4 16 Chapter 5-Fish assemblages Sampling dates Barrier opened No. of sites Total no. of samples taken 2009 Feb 23 5 30 Apr 9 5 30 May 27 Jun 21 Jul 28 5 30 Sep 3 5 30 Nov 17 5 30 2010 Jan 21 5 30 Mar 2 5 30 Jun 22 5 30 Chapter 6-Dietary studies Sampling dates Barrier opened No. of sites Total no. of samples taken 2009 Apr 9 1 30 May 27 Jun 21 Sep 3 1 30 Nov 17 1 30 Chapter 7-Trace metal concentrations Sampling dates Barrier opened No. of sites Total no. of samples taken 2012 Feb 16 26/1/2012 1 10

41 Chapter 2: Study area

Table 2.5. Sampling dates, barrier openings, the number of sites sampled and the total number of samples collected of invertebrate fauna, larval and juvenile fishes (also in adjacent surf zones), fish fauna, gut analysis and trace metal concentrations in fish tissue and sediments at Terrigal Lagoon between October 2004 and April 2012. Chapter 3-Invertebrate samples Sampling dates Barrier opened No. of sites Total no. of samples taken 2004 Oct 4 Dec 5 4 12 Dec 14 2005 Feb 26 4 12 Mar 24 Apr 20 Apr 24 4 12 May 27 Jun 19 4 12 Jul 7 Aug 27 4 12 Oct 19 Oct 21 Oct 8 4 12 Chapter 4-Larval and juvenile fishes Sampling dates Barrier opened No. of sites Total no. of samples taken 2006 Apr 21 4 16 Jun 4 4 16 Jun 6 Jun 14 4 16 Jun 20 Jul 4 Jul 11 4 16 Jul 20 Aug 3 4 16 Aug 5 Aug 28 Sep 8 Sep 21 4 16 Nov 29 4 16 Dec 21 2007 Jan 13 4 16 Feb 28 Mar 28 4 16 Nov 20 4 24 2010 Jan 18 4 24 Mar 4 4 24 Apr 1 May 25 May 28 Jun 28 4 24

42 Chapter 2: Study area

Table 2.5. continued…. Chapter 5-Fish assemblages Sampling dates Barrier opened No. of sites Total no. of samples taken 2009 Feb 17 Feb 27 4 24 Apr 3 Apr 6 4 24 May 28 Jun 17 Jul 30 4 24 Aug 11 Sep 4 4 24 Oct 26 Nov 20 4 24 2010 Jan 18 4 24 Mar 4 4 24 Apr 1 May 25 May 28 Jun 28 4 24 Chapter 6-Dietary studies Sampling dates Barrier opened No. of sites Total no. of samples taken 2009 Apr 6 2 60 May 28 Jun 17 Aug 11 Nov 20 2 60 Chapter 7-Trace metal concentrations Sampling dates Barrier opened No. of sites Total no. of samples taken 2012 Apr 11 21/2/2012 1 7

43 Chapter 2: Study area

Table 2.6. Sampling dates, barrier openings, the number of sites sampled and the total number of samples collected of invertebrate fauna, larval and juvenile fishes (also in adjacent surf zones), fish fauna, gut analysis and trace metal concentrations in fish tissue and sediments at Wamberal Lagoon between October 2004 and April 2012. *denotes no sampling in adjacent surf zones due to bad weather conditions. Chapter 3-Invertebrate sampling Sampling dates Barrier opened No. of sites Total no. of samples taken 2004 Oct 1 Dec 5 6 18 2005 Feb 26 6 18 Apr 24 6 18 May 18 Jun 19 6 18 Aug 27 6 18 Oct 22 6 18 Chapter 4-Larval and juvenile fishes Sampling dates Barrier opened No. of sites Total no. of samples taken 2006 Apr 23 4 16 Jun 18 4 16 Jun 20 Jun 25 4 16 Aug 18 4 16 Oct 2 4 16 Nov 12 4 16 2007 Jan 12 4 16 Mar 28* 4 4 Chapter 5- Fish assemblages Sampling dates Barrier openings No. of sites Total no. of samples taken 2009 Feb 22 5 18 Apr 14 5 18 Jun 18 Jul 31 5 18 Sep 8 5 18 Nov 19 5 18 2010 Jan 19 5 18 Mar 24 5 18 Jun 22 5 18 Chapter 6-Dietary studies Sampling dates Barrier openings No. of sites Total no. of samples taken 2009 Feb 22 1 30 Apr 14 5 150 Jun 18 Sep 8 1 30 Nov 19 5 150 Chapter 7-Trace metal concentrations Sampling dates Barrier openings No. of sites Total no. of samples taken 2012 Apr 11 21/2/2012 1 6 fish

44 Chapter 3: Factors influencing invertebrate faunal assemblages

Chapter 3: Factors influencing temporal and spatial variations of the invertebrate faunal assemblages of ICOLLs

45 Chapter 3: Factors influencing invertebrate faunal assemblages

3.1 Introduction In New South Wales (NSW) ICOLLs represent 45% of estuarine environments (Griffiths and West 1999), and approximately 72% of these ICOLLs are artificially opened on an irregular basis (Gale et al. 2006). Sandy barriers form across the entrances, and the status of the barrier is dependent upon climatic conditions and catchment development. Natural barrier openings and reformations are the result of a combination of heavy seasonal rainfall, strong wave action and long-shore and/or on-shore sediment deposition (Pollard 1994a). The occurrence of natural barrier openings has in many cases become more infrequent due to local councils implementing artificial openings as a management practice to mitigate flooding of the surrounding urbanised lagoon foreshores (Gale et al. 2006; Gladstone et al. 2006).

The composition and structure of floral and faunal assemblages, and the environmental conditions present in ICOLLs, have generally been associated with the condition of the barrier (Griffiths 2001a; Hirst 2004; Gladstone et al. 2006). ICOLLs that have been isolated for long periods generally have environmental conditions that imitate freshwater or brackish ecosystems (Pollard 1994a). In comparison, ICOLLs that have their barriers opened more regularly due to seasonal or annual rainfall can more resemble marine ecosystems, especially near their entrances (Dye 2006). Regular barrier openings alter and change the overall ecology of ICOLLs, which can have implications for their invertebrate faunas (Schallenberg et al. 2010). Invertebrates are an important food source for higher trophic levels; therefore changes in invertebrate assemblages may be associated with changes in fish assemblages (Hirst 2004; Dye and Barros 2005b).

Estuarine invertebrate taxa including polychaetes, crustaceans and molluscs are typical representatives of ICOLL invertebrate faunas (Weate and Hutchings 1977; Hutchings 1999; Dye and Barros 2005b). However, species richness and abundance can be directly and indirectly influenced by the status of the barrier, with short-term disturbances to invertebrate assemblages occurring during barrier openings (Gladstone et al. 2006). In contrast, long-term isolation from the sea can lead to impoverished invertebrate assemblages (Edgar et al. 1999; Dye, 2006). Also, the types of species found within ICOLLs have been shown to influence the composition of fish assemblages within these environments.

Salinity is a major driving factor in determining the patterns and distribution of most aquatic fauna (Young et al. 1997; Griffiths 2001a). All processes of water exchange in ICOLLs, including barrier openings, freshwater inputs, rainfall and evaporation, dramatically increase or decrease salinity. These changes in salinity can lead to mass mortality of intolerant species, while more resilient species can adapt (Hutchings 1999; Gladstone et al. 2006). Salinity

46 Chapter 3: Factors influencing invertebrate faunal assemblages

gradients are usually associated with tidal exchanges; however, within closed ICOLLs gradients are produced by wind-induced surface currents and the extent and magnitude of freshwater inflow from the catchment (Cheng 1981; King and Hodgson 1995). In areas near the entrances the effect of wind-induced surface currents decreases as depth increases (Gale et al. 2006).

Habitat variability is an important factor determining species richness and abundances of invertebrate fauna (Robinson et al. 1983). Hence, sediment composition and the types of seagrass or algae present can influence the abundance and richness of invertebrate fauna. ICOLLs are generally vegetated with Ruppia sp. along with the submerged alga, Chara sp. and floating mats of Entomorphora intestinalis (Cheng 1981; Pollard 1994a). ICOLLs generally also lack mangrove communities due to limited tidal influences, with shoreline vegetation consisting mainly of macrophtye communities and swamp oak forests (Bird 1967). Partitioning of sediments is a result of the influence of barrier openings and run-off, with deposition of coarse particles occurring near ICOLL entrances and finer particles deposited in the central basin as well as sites further away from the entrances. The species abundances of invertebrate fauna in ICOLLs generally increases with increasing distance from the entrance (Dye and Barros 2005a), while species richness tends to decrease with increasing distance from the entrance (Robinson et al. 1982). Temporal and spatial variations in invertebrate assemblages are also related to seasonal differences in water temperature, contaminants, nutrient loading and sedimentation (Dye and Barros 2005b; Gladstone et al. 2006).

Understanding of the effects of variation in the environmental factors of ICOLLs on invertebrate assemblages has been limited by many studies considering only individual factors such as barrier openings, salinity fluctuations or habitat degradation. Each ICOLL may be unique, therefore this study looked at a combination of environmental factors that may influence invertebrate assemblages and compared these factors between ICOLLs.

To more completely understand the factors influencing invertebrate assemblages of ICOLLs, the aims of the present study were: 1. To describe the spatial and temporal variability of the invertebrate assemblages of ICOLLs. 2. To determine the relative importance of physical, water chemistry and biological factors, and barrier openings, in shaping the observed spatial and temporal variation in invertebrate assemblages of ICOLLs and the consistency of these factors among ICOLLs.

47 Chapter 3: Factors influencing invertebrate faunal assemblages

These aims were addressed by testing the following null hypotheses: 1. There are no differences in spatial and temporal variation in invertebrate assemblages between ICOLLs. 2. The environmental factors structuring variations in invertebrate assemblages do not differ among the four ICOLLs and barrier status is the most important factor.

3.2 Materials and methods

3.2.1 Study area Invertebrate fauna were sampled bimonthly and environmental variables were sampled fortnightly between December 2004 and October 2005 from Cockrone (n=108), Avoca (n=108), Terrigal (n=72) and Wamberal Lagoons (n=108). Detailed habitat descriptions of each ICOLL and the sampling design (the number and frequency of samples) of invertebrate fauna and environmental variables are shown in Chapter 2 (Tables 2.3-2.6).

3.2.2 Invertebrate fauna collection and laboratory analysis Invertebrate fauna were collected randomly within different habitat types from six sites within each ICOLL, except Terrigal Lagoon, where four sites were sampled due to there being fewer habitats (i.e. no seagrass or algae).

Infaunal invertebrates from unvegetated sites were collected within a 1 m2 quadrat, using three replicate poly-vinyl chloride hand-held cores (10 cm diameter), pushed into the sediment to a depth of 20 cm. The collected core sediments were sieved through a 1 mm mesh and the retained contents preserved in 5% formalin until returned to the laboratory. Samples were then washed in water and stored in 70% ethanol until identified.

In vegetated sites, samples of Ruppia sp. and algae were collected to sample epifaunal invertebrates. Algae found in ICOLLs were a mixture of various types, including Chara sp., Entomorphora intestinalis and some blue-green algae, and from this point forward will be collectively referred to as algae. One sample of each vegetation type was collected at each site, in a polyethylene bag (31 x 38 cms), which represented a consistent biomass of approximately 80 g, to which 5% formalin was added. Once returned to the laboratory, the samples were thoroughly washed in tap water several times over a 1 mm sieve to collect any invertebrate fauna, which were then sorted and stored in 70% ethanol until identified.

Invertebrate fauna were sorted and identified to the lowest possible taxon using Williams (1980), Hutchings (1984), Hutchings and Murray (1984), Lamprell and Whitehead (1992), Ponder et al. (2000), Jones and Morgan (2002) and Wilson et al. (2003). In most cases,

48 Chapter 3: Factors influencing invertebrate faunal assemblages

damaged invertebrates could only be classified to family and badly damaged specimens were identified to a higher taxonomic group.

3.2.3 Environmental variables Salinity (ppt), turbidity (ntu) and water temperature (°C) were measured in situ at a depth of 0.5 m using a Yeo-Kal 611 Water Quality Analyser. Variables were recorded fortnightly between December 2004 and October 2005. Artificial barrier openings are generally sanctioned by Gosford City Council (GCC) and their records were examined to determine the dates of openings. In some instances unsanctioned barrier openings have been known to occur, as some members of the public open barriers, by whatever ever means possible, to swim in the outflowing water. Barrier openings are also recorded and posted online by Manly Hydraulic Laboratories (MHL 2004) (http://www.mhl.nsw.gov.au/). Openings documented by MHL were confirmed by visual inspection to determine the validity of these natural and /or illegal openings. The distance of sampling sites from the barrier was measured from topographical maps (LPI 2001). Three replicate sediment samples were collected during May 2004 (see Chapter 2), by a hand held poly-vinyl chloride corer (5 cm diameter) to a depth of 10 cm in shallow waters and by a Petersen Grab (15 cm3) in deeper areas. Sediment samples were dried in an oven at 60°C for four days and then partitioned into individual grain sizes using an Endecotts EFL 2000/2 EC sieve shaker, and then, used as a measure of ‘ambient’ sediment characteristics (Anderson et al. 2004).

3.2.4 Data analysis Non-parametric multivariate analyses were used to determine patterns of spatial and temporal variation in the invertebrate assemblages of ICOLLs and the relationships of this variation to the measured environmental variables and the status of the barrier. Multivariate dispersions in invertebrate fauna were compared using PERMDISP. This program is used to test for homogeneity of dispersions between groups by comparing the average distances from the centroids (Anderson 2004).

Three-way permutational multivariate analysis of variance (PERMANOVA) was used to test the null hypotheses that temporal and spatial variations of invertebrate assemblages do not occur using the following factors: (A) ICOLLs: fixed, four levels; (B) Time: random, six levels; and (C) Site nested in ICOLLs: random, six levels, except for Terrigal Lagoon, which has four levels. Data were fourth-root transformed prior to analysis to reduce the effects of some very abundant, and some rare, taxa (Clarke 1993). Tests were done on the Bray-Curtis dissimilarity resemblance measure permutated 9999 times under the reduced model. Due to large numbers of

49 Chapter 3: Factors influencing invertebrate faunal assemblages

zeros in the data, a dummy value (+1) was added (Clarke and Gorley 2006). Significant effects were further investigated using PERMANOVA pair-wise comparisons.

When a significant difference (p<0.05) was detected between levels of a factor, the Similarity of Percentages (SIMPER) procedure in PRIMER (Clarke 1993) was used to determine the species that caused significant temporal variation in invertebrate assemblages of ICOLLs. Species that contributed up to 90% of the dissimilarity of the significant pair-wise tests were analysed. Species with a percentage dissimilarity >3% and with a dissimilarity/standard deviation (dissimilarity) >1 were regarded as being important contributors to dissimilarity between ICOLLs (Clarke 1993; Terlizzi et al. 2005). Multi-dimensional scaling ordination (MDS) was used to visualise spatial and temporal variations in the structure of invertebrate assemblages.

PERMANOVA was also used to test for differences in the mean numbers of taxa, and the mean total number of individuals, using the same model as the PERMANOVA on assemblages. All tests were based on fourth-root transformations (Clarke 1993) and derived from a Euclidean distance matrix, and significance was determined by n=9999 permutations under a reduced model. Dispersions in the number of taxa and the total number of individuals were compared using PERMDISP. Significant effects were further investigated using PERMANOVA pair-wise comparisons.

To test the null hypothesis that the environmental factors structuring variations in invertebrate assemblages do not differ among the four ICOLLs and that barrier status was the most important factor, environmental variables responsible for spatial variation of invertebrate assemblages were analysed using distance-based linear models (DISTLM). Ten environmental variables were chosen for each ICOLL, incorporating the factors that described their physical, water chemistry and biological environment and barrier status (Table 3.1). Since environmental data were collected at different time periods during the study, the means of each variable were estimated and used in the data analysis. Draftsmen plots of untransformed environmental variables were produced to determine the extent of data skewness and multivariate normality and the need for transformations (Clarke and Ainsworth 1993); however, since no skewness occurred, all environmental data were analysed untransformed. The matrix of pair-wise correlations of environmental variables was examined and for pairs with large correlations (r≥0.95), one of the variables was eliminated from the analysis (Anderson et al. 2008).

The smallest set of environmental variables that together explained a significant amount of variation in the invertebrate assemblages was determined by the BEST procedure in DISTLM, with the Akaike Information Criterion (AIC) used as the selection criterion (Anderson et al.

50 Chapter 3: Factors influencing invertebrate faunal assemblages

2008). The BEST procedure evaluated all possible combinations of environmental variables to identify the combination of variables with the lowest AIC. A distance-based redundancy analysis (dbRDA), based on Pearson linear correlations, was used to visualise the relationship between the selected environmental variables and the invertebrate assemblages. The dbRDA is an ordination technique that overlays vectors for the selected environmental variables on the spatial arrangement of samples, with the length and direction of a vector indicative of the magnitude of the correlation between the variable and depicted sample arrangement. All multivariate and univariate analyses were examined using PRIMER v6 and PERMANOVA+ (PRIMER-E).

Table 3.1. Summary of the 10 environmental variables used in DISTLM analysis. Sediments were grouped according to their grain-sizes, with coarse sand ≥1.0 mm, medium sand >0.5 mm, fine sand >212 µm, coarse silt >63 µm and fine silt/clay <63 µm (Briggs 1977). Variable Units of measure Type Range Salinity ppt Continuous 6.44-36.95 Turbidity ntu Continuous 0-174 Water temperature °C Continuous 12.91-31.89 Barrier status Categorical Open/Closed Distance from barrier m Continuous 120-1500 Sediment –% coarse sand mm Continuous ≥1 Sediment – % medium sand mm Continuous 0.5-1.0 Sediment – % fine sand µm/mm Continuous 212-0.5 Sediment – % coarse silt µm Continuous 63-212 Sediment – % fine silt/clay µm Continuous <63

3.3 Results

3.3.1 ICOLL openings A total of 14 openings occurred across the four ICOLLs. On 10 occasions the ICOLLs were artificially opened by GCC (Table 3.2). Terrigal Lagoon was opened on 11 occasions, and this included 8 openings managed by GCC and 3 illegal openings. Avoca and Wamberal Lagoons were each artificially opened once by GCC (there were no illegal openings) and Cockrone Lagoon was also opened once (confirmed by data from Manly Hydraulic Laboratories).

51 Chapter 3: Factors influencing invertebrate faunal assemblages

Table 3.2. ICOLL barrier openings between November 2004 and October 2005. *denotes artificial barrier openings undertaken by Gosford City Council. The dates of other openings were obtained from Manly Hydraulic Laboratories (2004) and confirmed by visual inspection. ICOLL Cockrone Avoca Terrigal Wamberal 18/12/04 1/7/05* 14/12/04* 18/5/05* 4/2/05* 24/3/05* 20/4/05* 17/5/05* 25/5/05* 5/6/05 28/6/05* 2/7/05 20/10/05 21/10/05*

3.3.2 Invertebrate faunal assemblages of ICOLLs

3.3.2.1 Overview of invertebrate faunal assemblages A total of 7 363 individual organisms representing 32 identified species (28 families) were collected during the study. Of the vegetated ICOLLs which were sampled at six sites, Avoca Lagoon had the greatest number of invertebrates (n=2 894) whilst the smallest number of invertebrates was collected from Wamberal Lagoon (n=1 635). Wamberal Lagoon had the greatest number of taxa (n=25) whilst the smallest number of taxa from vegetated ICOLLs was collected from Cockrone Lagoon (n=24) (Figure 3.1a). In comparison, Terrigal Lagoon was sampled at four sites only, due to it lacking any aquatic vegetation, and was found to have a total of 500 invertebrates consisting of eight taxa (Figure 3.1b). Eight invertebrate taxa were common to all ICOLLs: oligochaetes; the polychaetes Notomastus estuarius, Australonereis elhersi, Nereis maxillodentata, Simplestia aequisetis, Leitoscoloplos spp. and Scoloplos simplex; the isopod Cymodetta sp. and the bivalve Arthritica helmsi (Table 3.3). Twelve taxa were only collected from one ICOLL: the insects Stenosialis australiensis and Culicini sp. (Cockrone Lagoon); the gastropods Dolabella auricularia, Nassarius jonsii, Onchidella patelloides; nematodes (Avoca Lagoon); a polychaete Marphysa sessilebranchiata; an unidentified spider; an isopod Mesanthura calaena; a decapod crustacean Halicarcinus sp.; and an insect Notostictata solida (Wamberal Lagoon) (Table 3.3).

52 Chapter 3: Factors influencing invertebrate faunal assemblages

3500 (a)

n=6 3000

2500 n=6

2000 n=6

1500 Total no. ofindividuals no. Total 1000 n=4 500

0 Cockrone Avoca Terrigal Wamberal

35 (b)

n=6 30

n=6 25 n=6

15 n=4

Total no. ofno.species Total 10

0 Cockrone Avoca Terrigal Wamberal ICOLL

Figure 3.1. Comparison of the total number of invertebrates (a) and the total number of invertebrate taxa (b) collected from sites (n) within each ICOLL from December 2004 to October 2005.

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Table 3.3. Presence/absence of invertebrate infauna and epifauna. Collections occurred bimonthly between December 2004 and October 2005. X indicates the species was present at the ICOLL. Taxon/Family Species ICOLLS Cockrone Avoca Terrigal Wamberal Hirudinea Glossiphoniidae X X X Oligochaeta X X X X Polychaeta Capitellidae Notomastus estuarius X X X X Eunicidae Marphysa sanguinea X X X Marphysa sessilebranchiata X Nereididae Australonereis elhersi X X X X Nereis maxillodentata X X X X Simplestia aequisetis X X X X Simplestia turveyi X X X Orbiinidae Leitoscoloplos sp. X X X X Scoloplos simplex X X X X Serpulidae X Spionidae Orthoprionospio sp. X X X Chelicerata X Amphipoda Corophiidae Paracorophium sp. X X X Melitidae Melita sp. X X X Paracalliopiidae Paracalliope australis X X X Paracalliope sp. X X X Isopoda Athuridea Mesanthura calaena X Sphaeromatidae Cymodetta sp. X X X X Decapoda Hymenosodiidae Halicarcinus sp. X Insecta Chironomidae Chironomus sp. X X X Corydalidae Stenosialis australiensis X Culicidae Culicini sp. X Protoneuridae Notosticta solida X Pyralidae Nymphula sp. X X Bivalvia Leptonidae Arthritica helmsi X X X X

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Table 3.3 Continued…. Taxon/Family Species ICOLLS Cockrone Avoca Terrigal Wamberal Mytilidae Xenostrobus securis X X Psammobiidae Soletellina alba X X X Trapeziidae Fluviolantus subtortus X X X Gastropoda Amphibolidae Salinator fragilis X X X Aplysiidae Dolabella auricularia X Assimeidae Assiminea siennae X X X Hydrobiidae Tatea rufilabris X X Nassariidae Nassarius jonsii X Onchidiidae Onchidella patelloides X Nematoda X

3.3.2.2 Invertebrate faunal assemblages of Cockrone Lagoon A total of 2 334 individual organisms representing 21 taxa (18 families) were collected from the six sites in Cockrone Lagoon during the study period (Appendix 1a). Polychaetes (representing 49% of the total individuals collected) and bivalve and gastropod molluscs (38%) were the dominant taxa. The dominant polychaete species were Notomastus estuarius (Capitellidae) and Nereis maxillodentata (Nereididae), contributing 11% of the total fauna. The bivalves Arthritica helmsi (Leptonidae) and Fluviolantus subtortus (Trapeziidae) represented 15% and 11%, respectively, of the total abundance of invertebrate taxa. The gastropod Assiminea siennae (Assimeidae) represented 11% of the total fauna. Algal epifauna represented 28% of the total number of individuals. The dominant species, Assiminea sienna, represented 27% and 49% of the total fauna collected from Ruppia sp. and algae respectively.

The total number of invertebrates varied spatially and temporally over the study period (Figure 3.2a). The greatest abundances of invertebrates were attributed to the infauna at site 4 where Ruppia sp. is located. High abundances of epifauna were also collected from Ruppia sp. at site 4R. Overall, abundances decreased after the barrier opening but increased during the colder months of June and August 2005, along with the warmer period of December 2004. The number of taxa was generally similar across the study period at most sites, peaking in October 2005 at site 5 (Figure 3.2b).

55 Chapter 3: Factors influencing invertebrate faunal assemblages

(a) 250

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50 Total no. of individualsof no. Total

0 Dec 04 Feb 05 Apr 05 Jun 05 Aug 05 Oct 05

(b)

2 Total no. of speciesof no. Total

0 Dec 04 Feb 05 Apr 05 Jun 05 Aug 05 Oct 05

Sampling period S1 S2 S3 S4 S4R S4A S5 S5A S6

3.3.2.3 Invertebrate faunal assemblages of Avoca Lagoon A total of 2 894 individuals representing 22 taxa, (20 families) were collected from the six sites in Avoca Lagoon during the study period (Appendix 1b). Bivalve and gastropod molluscs (representing 50% of the total individuals collected) and polychaetes (37%) and crustaceans (11%) were the dominant taxa. The dominant gastropod was Assiminea siennae (Assimeidae) representing 29% of the total fauna. The polychaetes Notomastus estuarius (Capitellidae), Simplestia aequisetis (Nereididae), and the bivalve Arthritica helmsi (Leptonidae) represented 13%, 10% and 11%, respectively, of the total abundance of invertebrate taxa. The amphipods Paracorophium sp. (Corophiidae) and Paracalliope sp. (Paracalliopiidae) represented 5% and 4%, respectively, of the total abundance of invertebrate taxa. Algal epifauna represented 9% and

56 Chapter 3: Factors influencing invertebrate faunal assemblages

32%, respectively of the total number of individuals. The dominant species, A. sienna, represented 39% and 69% of the total fauna collected from Ruppia sp. and algae respectively.

The total number of invertebrates varied spatially and temporally (Figure 3.3a). In general, the abundance of infaunal invertebrates was greater than epifaunal, except at site 5A which had the greatest overall abundance, peaking during October 2005. Seasonal variations occurred as abundances were generally lower between February and April 2005, and increased slightly from June 2005 to October 2005. The number of taxa was generally similar across the study period at most sites and showed only slight temporal variations (Figure 3.3b).

(a) 350

300

250

200

150

100

50 Total no. of individualsof no. Total 0 Dec 04 Feb 05 Apr 05 Jun 05 Aug 05 Oct 05

10 (b)

Total no. of speciesno.of Total 0 Dec 04 Feb 05 Apr 05 Jun 05 Aug 05 Oct 05 Sampling period S1 S2 S3 S3R S4 S4A S5 S5A S6 Figure 3.3. Temporal and spatial variation of (a) the total number of invertebrates and (b) the total number of taxa collected using core samples (sites 1-6) and from Ruppia sp. (site 3R) and algae (sites 4A and 5A) from Avoca Lagoon. Dotted vertical lines indicate single barrier openings occurred between sampling periods.

3.3.2.4 Invertebrate faunal assemblages of Terrigal Lagoon A total of 500 individual organisms representing 8 taxa, (5 families) were collected from the four sites in Terrigal Lagoon during the study period (Appendix 1c). Polychaetes (representing 98% of the total individuals collected) were the dominant taxa. The nereid polychaetes

57 Chapter 3: Factors influencing invertebrate faunal assemblages

Australonereis elhersi and Simplestia aequisetis represented 41% and 31%, respectively, of the total taxa. The orbiinid polychaetes Leitoscolopos sp. and Scoloplos simplex represented 11% and 9%, respectively, of the total fauna. Only infauna were collected from Terrigal Lagoon, with abundances being low at all sites except at site 2, which peaked during June 2005 before decreasing in August and October 2005 (Figure 3.4a). It is difficult to interpret any changes in the total number of individuals because of the sampling regime in relation to the frequency of barrier openings. The peak abundances at site 2 were due to high numbers of Australonereis elhersi, which decreased slightly over the study period, possibly due to seasonal variations. There were only slight spatial and temporal variations in the number of taxa (Figure 3.4b). (a)

200

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50 Total no. of individualsof no. Total 0 Dec 04 Feb 05 Apr 05 Jun 05 Aug 05 Oct 05

(b) 6 5 4 3 2

1 Total no. of speciesof no. Total 0 Dec 04 Feb 05 Apr 05 Jun 05 Aug 05 Oct 05 Sampling period S1 S2 S3 S4 Figure 3.4. Temporal and spatial variation of (a) the total number of individual invertebrates and (b) the total number of taxa collected using core samples (sites 1-4) from Terrigal Lagoon. Solid vertical lines indicate multiple barrier openings occurred between sampling periods.

3.3.2.5 Invertebrate faunal assemblages of Wamberal Lagoon A total of 1 635 individual organisms representing 25 taxa, (23 families) were collected from the six sites in Wamberal Lagoon during the study period (Appendix 1d). Bivalves (representing 42% of the total individuals collected) and polychaetes (26%) and crustaceans (15%) were the dominant taxa. The bivalve Fluviolantus subtortus (Trapeziidae) and the polychaete Simplestia

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aequisetis (Nereididae) represented 36% and 10%, respectively of the total taxa. Epifauna (accounting for 59% of the total fauna) was dominated by the bivalve Fluviolantus subtortus, which represented 30% of the epifauna. Invertebrate abundance varied spatially and temporally (Figure 3.5a). Overall, the greatest abundance of invertebrates was collected as epifauna from Ruppia sp., mainly at sites 3R and 4R. Abundances peaked in December 2004 and April 2005, with a decrease in the total number of individuals after the only barrier opening before the June 2005 sample. The total number of taxa was similar throughout the study period (Figure 3.5b), with numbers generally not affected by the barrier opening. In most cases, the total number of taxa was greatest at site 5, with numbers peaking during February and April 2005.

(a) 200

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50 Total no. of individualsof no. Total 0 Dec 04 Feb 05 Apr 05 Jun 05 Aug 05 Oct 05

(b) 10

Total no. of speciesof no. Total 2

0 Dec 04 Feb 05 Apr 05 Jun 05 Aug 05 Oct 05 Sampling period S1 S2 S3 S3R S4 S4R S5 S6 S6R Figure 3.5. Temporal and spatial variation of (a) the total number of individual invertebrates and (b) the total number of taxa collected using core samples (sites 1-6) and from Ruppia sp. (sites 3R, 4R and 6R) from Wamberal Lagoon. Dotted vertical lines indicate single barrier openings occurred between sampling periods.

59 Chapter 3: Factors influencing invertebrate faunal assemblages

3.3.3 Comparison of invertebrate faunal assemblages between ICOLLs

3.3.3.1 Multivariate analysis Invertebrate assemblages of ICOLLS showed complex patterns of spatial and temporal variation, with significant Time x ICOLL x Site(ICOLL) interactions (Table 3.4). Both interactions were further investigated using pairwise tests in PERMANOVA. The Time x Site(ICOLL) interaction occurred because the patterns of variation among sites at each time differed across the four ICOLLs. Invertebrate assemblages at Cockrone and Avoca Lagoons differed among all sites in each lagoon at all sampling times (i.e. times 1-6). At Wamberal Lagoon invertebrate assemblages differed among sites at sampling times 2, 3 and 5 but not at times 1, 4 and 6. Invertebrate assemblages at Terrigal Lagoon differed among sites at sampling times 2, 4 and 5 but not at times 1, 3 and 6.

The significant Time x ICOLL interaction occurred because invertebrate assemblages at all ICOLLs were different at sampling times 1, 4 and 5, but not at times 2, 3 and 6. At sampling time 6, assemblages differed between Avoca and Wamberal Lagoons and between Wamberal and Terrigal Lagoons. Invertebrate assemblages of all ICOLLs were not significantly different at sampling times 2 and 3.

Table 3.4. Summary of results of 3-factor PERMANOVA testing for differences in the invertebrate assemblages of ICOLLs. Source df MS Pseudo-F p ICOLL 3 15128 1.41 0.04 Time 5 10474 4.45 0.0001 Site (ICOLL) 18 7063 3.00 0.0001 Time x ICOLLs 15 5306 2.25 0.0001 Time x Site (ICOLL) 90 2352 2.62 0.0001 Res 264 897.88

PERMDISP for Time x Site(ICOLL) was significant (F=3.19, df=131, p=0.03) and occurred because sites at only one ICOLL (Cockrone Lagoon) differed in their variability at only one sampling time (sampling time 2). PERMDISP for Time x ICOLL was significant (F=3.63, df=23, p=0.0001) and occurred because the pairwise patterns of differences in variability between ICOLLs were not consistent at each sampling time. Cockrone and Wamberal Lagoons were significantly different at sampling time 5, and Cockrone and Terrigal Lagoons were significantly different at sampling times 5 and 6. Avoca and Wamberal Lagoons were significantly different at sampling time 6, and Avoca and Terrigal Lagoons were significantly different at sampling times 1, 2 and 6. Wamberal and Terrigal Lagoons were significantly

60 Chapter 3: Factors influencing invertebrate faunal assemblages

different at sampling times 2 and 3. There were no significant differences among any ICOLLs at sampling time 4.

The MDS plot illustrates the temporal variability of invertebrate assemblages’ at sites within each ICOLL (Figure 3.6). The stress values of all ICOLLs are high (≥0.19); however, there is not a great deal of pattern shown for each ICOLL.

Cockrone Lagoon Avoca Lagoon 2D Stress: 0.2 2D Stress: 0.24

Terrigal Lagoon Wamberal Lagoon 2D Stress: 0.19 2D Stress: 0.21

SIMPER analysis of the Time x Site ICOLL interaction found differences in invertebrate assemblages among sites for all sampling times (i.e. times 1-6) at Cockrone Lagoon and Avoca Lagoon. Invertebrate assemblages differed among sites for Terrigal Lagoon at sampling times 2, 4 and 5, and for sampling times 2, 3 and 5 at Wamberal Lagoon (Table 3.5).

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Table 3.5. Summary of SIMPER results showing invertebrate species responsible for temporal differences in invertebrate assemblages at each ICOLL. Invertebrate species that contributed up to 90% of the dissimilarity between sampling times are shown. Cockrone Lagoon Time 1 Time 2 Time 3 Time 4 Time 5 Time 6 Arthritica helmsi Orthoprionospio sp. Orthoprionospio sp. Scoloplos simplex Orthoprionospio sp. Leitoscoloplos sp. Fluviolantus subtortus Fluviolantus subtortus Nereis maxillodentata Australonereis Notomastus Melita sp. elhersi estuarius Cymodetta sp. Nereis maxillodentata Arthritica. helmsi Arthritica. helmsi Leitoscoloplos sp. Simplestia aequisetis Chironomus sp. Avoca Lagoon Time 1 Time 2 Time 3 Time 4 Time 5 Time 6 Paracorophium sp. Australonereis elhersi Nereis maxillodentata Simplestia Arthritica. helmsi Arthritica. helmsi aequisetis Assiminea siennae Scoloplos simplex Fluviolantus subtortus Notomastus Notomastus Notomastus estuarius estuarius estuarius Orthoprionospio sp. Notomastus estuarius Scoloplos simplex Nereis maxillodentata Terrigal Lagoon Time 2 Time 4 Time 5 Notomastus estuarius Arthritica helmsi Arthritica helmsi Marphysa sanguinea Simplestia aequisetis Simplestia aequisetis Nereis maxillodentata Scoloplos simplex Scoloplos simplex Oligochate sp. Wamberal Lagoon Time 2 Time 3 Time 5 Mesanthura calaena. Simplestia aequisetis Arthritica helmsi Orthoprionospio sp. Nereis maxillodentata Fluviolantus subtortus Simplestia aequisetis Fluviolantus subtortus Simplestia aequisetis Notomastus estuarius Salinator fragilis Fluviolantus subtortus Oligochaete sp. Melita sp.

SIMPER analysis for differences among ICOLLs found that invertebrate assemblages differed between Cockrone and Wamberal Lagoons and Cockrone and Terrigal Lagoons due to differences in abundances of Orthoprionospio sp. at sampling time 1. Differences among ICOLLs in abundances of Simplestia aequisetis and Notomastus estuarius were responsible for differences in assemblages between Cockrone and Avoca Lagoons at sampling time 4. Differences among ICOLLs in abundances of Arthritica helmsi were responsible for differences in assemblages between Avoca and Wamberal Lagoons at sampling time 6, and differences in S. aequisetis and Leitoscoloplos sp. were responsible for differences in assemblages between

62 Chapter 3: Factors influencing invertebrate faunal assemblages

Wamberal and Terrigal Lagoons at sampling time 6. No differences in assemblages were found between ICOLLs at sampling times 2, 3 and 5.

3.3.3.2 Univariate analysis The mean number of species and the mean total number of individuals were both affected by significant Time x Site(ICOLL) interactions (Table 3.6). Overall, there were no significant differences for the mean number of species between ICOLLs, except for Terrigal Lagoon (Figure 3.7a), which had no vegetated habitats and was only sampled at four sites. However, the significant interaction for mean number of species occurred because differences among sites in each ICOLL were not consistent through time. Sites in Cockrone Lagoon differed significantly at each sampling time. In Avoca Lagoon, the mean number of species differed among sites at sampling times 1, 2, 4 and 5, but not at times 3 and 6. Wamberal Lagoon also showed differences for sampling times 2, 3 and 5 but not at times 1, 4 and 6. In Terrigal Lagoon differences in the mean number of species were found at times 1, 2, 5 and 6, but not at times 3 and 4.

Table 3.6. Summary of results of univariate PERMANOVA testing for differences among ICOLLs in the mean number of species and mean number of total individuals. Number of species Total number of individuals Source df MS Pseudo-F p MS Pseudo-F p ICOLL 3 1.03 0.87 0.56 5.81 1.39 0.20 Time 5 0.90 2.27 0.05 4.71 4.87 0.001 Site (ICOLL) 18 1.19 5.06 0.0002 3.41 3.53 0.0001 Time x ICOLL 15 0.46 1.16 0.32 1.46 1.51 0.12 Time x Site(ICOLL) 90 0.40 1.70 0.001 0.97 2.31 0.0001 Res 264 0.23 0.42

Overall, no significant differences were found for the mean number of individuals between ICOLLs (Figure 3.7b). However, the significant interaction for the total number of individuals occurred because the patterns of differences among sites in each ICOLL differed at each sampling time. Differences among all sites in Cockrone Lagoon were found at sampling times 1-3, 5 and 6, but not at time 4. Differences in the mean number of individuals among sites in Avoca Lagoon were found at all sampling times (i.e. sampling times 1-6). Wamberal Lagoon also showed differences among sites for times 2, 3 and 5 but not at times 1, 4 and 6. In Terrigal Lagoon differences in the mean number of individuals were found at times 2-5, but not at times 1 and 6.

63 Chapter 3: Factors influencing invertebrate faunal assemblages

(a)

5 4.5 4 3.5 3 * 2.5 2 1.5 1

Mean number of speciesMeanofnumber 0.5 0 Cockrone Avoca Terrigal Wamberal

(b)

Mean total no. of individuals ofMeantotalno. 0 Cockrone Avoca Terrigal Wamberal ICOLLs

Figure 3.7. Mean number (±se) of species (a) and mean number (±se) of individuals (b) of invertebrate fauna from all ICOLLs. * denotes the ICOLL was significantly different.

The PERMDISP analysis for Time x Site(ICOLL) was significant (F=6.09, df=131, p=0.0001) for the mean number of species and for the mean total number of individuals (F=3.90, df=131, p=0.0001). Pairwise analysis of dispersion for mean number of species showed that there were no significant differences in variability between sites at all times for Avoca, Wamberal and Terrigal lagoons. In comparison, Cockrone Lagoon had one significant pairwise test at sampling time 2, with times 1 and 3-6 showing no significant differences. The same results were found for the dispersion of the mean number of individuals.

3.3.4 Comparison of environmental factors structuring invertebrate faunal assemblages of ICOLLs

3.3.4.1 Environmental variables Graphical representation for salinity, water temperature and turbidity in each ICOLL are shown at the end of this chapter (Appendix 2a-d). Overall, salinity was similar at each site within each ICOLL, with Cockrone Lagoon recording the highest and lowest salinities of 36.95 and 2.02 ppt respectively. In most cases salinity values increased after barriers had opened, except at Terrigal

64 Chapter 3: Factors influencing invertebrate faunal assemblages

Lagoon, where salinity decreased in some cases after barriers were opened, possibly due to high rainfall and run-off events occurring between sampling periods. In general, turbidity was also similar at each site within each ICOLL, with the highest value at Terrigal Lagoon of 174 ntu and the lowest reading of 0.1 ntu occurring at all ICOLLs. Generally, turbidity did not increase after barrier openings; however spikes occurred in each ICOLL at various times throughout the sampling period. Water temperature in the four ICOLLs was similar and followed seasonal trends that were not influenced by barrier openings. Water temperatures greater than 25°C occurred during the warmer periods of December 2004 to February 2005, with colder water temperatures of below 15°C occurring between June 2005 and August 2005.

3.3.4.2 Influence of environmental variables on invertebrate faunal assemblages Environmental variables were identified using the BEST procedure and AIC selection in DISTLM for all ICOLLs (Table 3.7). Seven variables were identified for Cockrone Lagoon, three variables for Avoca Lagoon, six variables for Terrigal Lagoon and three variables for Wamberal Lagoon. The seven variables selected for Cockrone Lagoon explained 44.75% of the total assemblage variation, with salinity explaining the greatest variation (20.01%), followed by turbidity (11.10%), water temperature (5.78%) and % sediment grain sizes of >212 µm (3.79%), >63 µm (3.05%), <63 µm (0.85%) and distance from the barrier (0.17%). In comparison, the three variables selected for Avoca Lagoon explained 25.32% of the total assemblage variation, with salinity explaining the greatest variation (12.36%), followed by water temperature (7.16%) and distance from the barrier (5.8%). The six variables selected for Terrigal Lagoon explained 67.46% of the total assemblage variation, with salinity explaining the greatest variation (36.71%), followed by turbidity (12.3%), barrier status (9.37%) and % sediment grain size ≥1 mm (6.14%), >0.5 mm (2.57%) and >63 µm (0.37%). The three variables selected for Wamberal Lagoon explained 15.82% of the total assemblage variation, with % sediment grain size >212 µm explaining the greatest variation (8.64%), followed by % sediment grain size <63 µm (5.46%) and turbidity (1.72%).

65 Chapter 3: Factors influencing invertebrate faunal assemblages

Axis Individual Cumulative Individual Cumulative Cockrone Lagoon Salinity 44.71 44.71 20.01 20.01 Turbidity 24.81 69.52 11.10 31.11 Water temperature 12.91 82.43 5.78 36.89 >212 µm % sediment grain size 8.48 90.91 3.79 40.68 >63 µm % sediment grain size 6.82 97.72 3.05 43.73 <63 µm % sediment grain size 1.89 99.62 0.85 44.58 Distance from barrier 0.38 100 0.17 44.75 Avoca Lagoon Salinity 48.79 48.79 12.36 12.36 Water temperature 28.28 77.08 7.16 19.52 Distance from barrier 22.92 100 5.8 25.32 Terrigal Lagoon Salinity 54.42 54.42 36.71 36.71 Turbidity 18.23 72.65 12.3 49.01 Barrier status 13.89 86.54 9.37 58.38 ≥1 mm % sediment grain size 9.11 95.64 6.14 64.53 >0.5 mm % sediment grain size 3.81 99.45 2.57 67.1 >63 µm % sediment grain size 0.55 100 0.37 67.46 Wamberal Lagoon >212 µm % sediment grain size 54.64 54.64 8.64 8.64 <63 µm % sediment grain size 34.50 89.14 5.46 14.10 Turbidity 10.86 100 1.72 15.82

66 Chapter 3: Factors influencing invertebrate faunal assemblages

The influence of each variable on the structuring of invertebrate assemblages for all the ICOLLs was visualised by overlaying vectors in dbRDA (Figure 3.8). Axis 1 of Cockrone Lagoon dbRDA plot explained 44.7% of the fitted variation and 21.1% of the total variation, Axis 2 of the dbRDA plot explained 23.6% of the fitted variation and 11.1% of the total variation. In comparison, Axis 1 of Avoca Lagoon dbRDA plot explained 48.8% of the fitted variation and 12.4% of the total variation, with Axis 2 explaining 28.3% of the fitted variation and 7.2% of the total variation. Terrigal Lagoon axis 1 of the dbRDA plot explained 54.4% of the fitted variation and 36.7% of the total variation with axis 2 explaining 18.2% of the fitted variation and 12.3% of the total variation. Axis 1 of Wamberal Lagoon plot explained 54.6% of the fitted variation and 8.6% of the total variation with axis 2 explaining 34.5% of the fitted variation and 5.5% of the total variation.

Each variable is represented by Pearson correlation of selected environmental variables that are represented on each dbRDA axes (Table 3.8). For Cockrone Lagoon the first dbRDA axis was strongly negatively correlated with distance from barrier (-0.82) and the second axis with temperature (-0.59). The first dbRDA axis of Avoca Lagoon was strongly negatively correlated with temperature (-0.94) and the second axis highly negatively correlated with salinity (-0.89). The first dbRDA axis for Terrigal Lagoon was strongly negatively correlated with % sediment grain size of ≥1 mm (-0.63) and salinity (-0.57) for the second axis. For Wamberal Lagoon the first dbRDA axis was strongly negatively correlated with % sediment grain size >212 µm (-0.90) and the second axis positively correlated with % sediment grain size >63 µm (0.79).

67 Chapter 3: Factors influencing invertebrate faunal assemblages

Cockrone Lagoon Avoca Lagoon )

) 40 40

a t 20 t 20

o Dist

o o

63µm

% Temp

, ,

0 d

d 0

i i

Sal f

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3 Dist

. 4

-20 <63µm 8 -20 2

Temp 2

(

A D

D Sal

b d -40 d -40 -40 -20 0 20 40 60 -40 -20 0 20 40 dbRDA1 (44.7% of fitted, 20% of total variation) dbRDA1 (48.8% of fitted, 12.4% of total variation)

Terrigal Lagoon Wamberal Lagoon )

) 50 30

i r

r 63µm a

a 20

o t

63µm t

f 212µm

o o 10

Closed

, ,

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. Turb 8

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Sal 3

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2 -20

b d -50 d -30 -100 -50 0 50 -40 -30 -20 -10 0 10 20 dbRDA1 (54.4% of fitted, 36.7% of total variation) dbRDA1 (54.6% of fitted, 8.6% of total variation) Figure 3.8. dbRDA ordination plots showing the structural arrangement of invertebrate assemblages in Cockrone, Avoca, Terrigal and Wamberal Lagoons overlaid with the vectors of the environmental variables that explained significant amounts of variation in the assemblages. Vectors represent the direction and magnitude of the Pearson correlation of each variable with the dbRDA axes. The different symbols represent different sampling times, and the replicate symbols represent the different sites at each time. Sampling times are represented by symbols: ▲T1, ▼T2, ■T3, ♦T4, ●T5, +T6. Sal=salinity, Turb=turbidity, Temp=water temperature, Dist= distance from barrier.

68 Chapter 3: Factors influencing invertebrate faunal assemblages

Table 3.8. Values of Pearson correlations of selected environmental variables with each of the dbRDA axes for Cockrone, Avoca, Terrigal and Wamberal Lagoons. Cockrone Lagoon Axes Salinity (ppt) Turbidity (ntu) Water temperature >212 µm >63 µm <63 µm Distance (°C) from barrier (m) dbRDA 1 -0.22 0.05 -0.27 -0.14 0.16 -0.36 -0.84 dbRDA 2 -0.09 -0.13 -0.56 -0.22 0.31 -0.51 0.51 dbRDA 3 -0.65 -0.41 0.47 -0.25 -0.23 -0.24 0.10 dbRDA 4 0.61 -0.57 0.25 -0.40 0.22 -0.06 -0.14 dbRDA 5 -0.06 -0.51 -0.07 0.81 -0.05 -0.25 -0.06 dbRDA 6 -0.03 0.32 0.53 0.22 0.70 -0.26 0.06 dbRDA 7 -0.06 0.35 0.20 -0.02 -0.53 0.65 0.04 Avoca Lagoon Axes Salinity (ppt) Water temperature (°C) Distance from barrier (m) dbRDA 1 -0.30 -0.94 -0.35 dbRDA 2 -0.89 0.209 -0.41 dbRDA 3 -0.72 0.72 0.04 Terrigal Lagoon Axes Salinity (ppt) Turbidity (ntu) Barrier closed Barrier ≥1mm >0.5 >63 µm open mm dbRDA 1 0.25 -0.20 -0.16 0.16 -0.63 -0.47 -0.48 dbRDA 2 -0.57 -0.03 0.24 -0.24 -0.31 -0.51 0.45 dbRDA 3 0.15 -0.54 0.10 -0.10 -0.50 0.55 0.34 dbRDA 4 0.15 -0.40 0.54 -0.54 0.30 -0.14 -0.36 dbRDA 5 -0.22 -0.71 -0.34 0.34 0.40 -0.20 0.07 dbRDA 6 0.72 0.02 0.002 -0.002 0.14 -0.39 0.56 Wamberal Lagoon Axes >212 µm >63 µm Turbidity (ntu) dbRDA 1 -0.90 0.27 -0.35 dbRDA 2 0.42 0.79 -0.45 dbRDA 3 0.16 -0.55 -0.82

3.4 Discussion

3.4.1 Physical and environmental aspects of ICOLLs This study was undertaken to determine the physical and environmental processes of Central Coast ICOLLs of NSW. These processes have the potential to influence fish and invertebrate assemblages found within these ICOLLs. Also, the composition of invertebrate assemblages within ICOLLs can influence fish assemblages as many invertebrates are preferred food items in the diets of many fishes (Platell et al. 2006). This study has shown that the physical and

69 Chapter 3: Factors influencing invertebrate faunal assemblages

environmental aspects of three of the four ICOLLs in the study area were generally similar. All ICOLLs have similar sized catchments, except for Terrigal Lagoon. Cockrone, Avoca and Wamberal Lagoons also have similar barrier opening regimes, seagrass and algal habitats, and in most cases water chemistry. The lack of seagrass and algal habitats in Terrigal Lagoon maybe the result of frequent barrier openings. Generally, marine conditions would promote seagrass growth, however, many barrier openings can expose the bottom sediments for extended periods of time, especially at Terrigal Lagoon (personal observations), thereby restricting any growth of aquatic vegetation.

Water parameters such as salinity are an important factor in causing spatial variations of flora and fauna within ICOLLs (Lill et al. 2012). With an absence of tidal flows and predominance of shallow water, the dispersion of water around the ICOLLs is mainly driven by wind (Cheng 1981; Pollard 1994a). Generally, no salinity gradients existed when barriers were closed as values were relatively similar at each sampling site within the ICOLLs. Variations that did occur in salinity or turbidity were generally associated with heavy periods of rainfall and shallow depths. Salinities at Avoca and Terrigal Lagoons were higher than at Cockrone and Wamberal Lagoons, which was most likely due to the frequent barrier openings at Terrigal Lagoon, along with overtopping events or increased evaporation from shallow areas (Pollard 1994a). Turbidity at Cockrone, Avoca and Wamberal Lagoons was lower compared to Terrigal Lagoon due to a lack of aquatic vegetation that would otherwise stabilise the sediments. Water temperature at all ICOLLs was similar and was not influenced by barrier openings, but generally associated with seasonal changes in air temperature. The hydrological characteristics of ICOLLs in this study show similarities to other shallow ICOLLs along the NSW coast (Pollard 1994a).

3.4.2 Invertebrate faunal assemblages of ICOLLs The total numbers of invertebrate fauna and species richness varied between the ICOLLs; however, ICOLLs that have aquatic vegetation supported greater abundances and species richness. This is a common trait in estuarine environments with seagrasses and algal habitats generally being occupied by a more abundant and richer invertebrate fauna (Robinson et al. 1983; Dye and Barros 2005a, 2005b). Compared to other studies, the numbers of invertebrate taxa found in Central Coast ICOLLs were low, with 21 taxa found at Cockrone Lagoon, 23 taxa collected from Avoca Lagoon, 13 taxa from Terrigal Lagoon and 28 taxa from Wamberal Lagoon. In comparison, Robinson et al. (1983) found 43 taxa, Mikac et al. (2007) found 10 taxa, while Hirst (2004) found 33 taxa, and Edgar et al. (1999) found 120 taxa. Two previous studies on the four Central Coast ICOLLs found differences in some taxa at each of the ICOLLs (Weate and Hutchings 1977; Gladstone et al. 2006). Weate and Hutchings (1977) documented

70 Chapter 3: Factors influencing invertebrate faunal assemblages

similar numbers of taxa with 26 taxa collected from Cockrone Lagoon, 29 taxa at Avoca Lagoon, 24 taxa at Terrigal Lagoon and 23 taxa at Wamberal Lagoon. In comparison, Gladstone et al. (2006) collected a lower number of taxa at these four sites, with a total of 11 taxa. The sampling regime for both previous studies also differed as they did not examine the epifauna of aquatic vegetation, and that of Weate and Hutchings (1977) differed slightly from the current study in that sampling took place at only three sites, near the entrance, in the middle and upper reaches of the ICOLLs, but they were sampled over a similar time frame. In contrast, Gladstone et al. (2006) sampled on three occasions only, once before and twice after barriers were opened, and sampling occurred near the entrances of each ICOLL.

Many similar taxa were recorded from each of these studies, including the polychaetes Australonereis elhersi, Scoloplos sp., Simplestia aequisetis and Leitoscoloplos sp., the bivalves Fluviolantus sp., Xenostrobus securis, and the gastropod Tatea sp., along with the decapod Halicarcinus sp. and the amphipod Paracalliope australis. However, different taxa were collected in the current study that were not found in the two previous studies, such as the polychaetes Notomastus estuarius and Orthoprionspio sp., along with the epifaunal insect Chironomus sp. and the bivalve Arthritica helmsi, both found on vegetation. Generally, invertebrate assemblages from ICOLLs are dominated by crustaceans, polychaetes and molluscs, however these assemblages can change due to environmental conditions and disturbances such as barrier openings (Mikac et al. 2007; Lill et al. 2012), and temporal changes (Weate and Hutchings 1977; Lill et al. 2012).

3.4.3 Spatial and temporal variation of invertebrate faunal assemblages of ICOLLs Complex patterns of spatial and temporal variation occurred in the invertebrate assemblages, and in species richness and total abundance of invertebrates. Small-scale spatial variations of total abundances and species richness of invertebrate fauna within ICOLLs tended to be greater at sites sampled where Ruppia sp. and algae were present. These habitats are known to have higher abundances and species richness as they provide shelter for many fauna (Robinson et al. 1983; Allan et al. 1985). Most of these sites are located in the central basin or further away from entrances which have been shown to contain greater abundances and species richness (Dye and Barros 2005a). Sites within Terrigal Lagoon, which has no vegetation, that were further away from the entrance had greater species richness and greater abundances of invertebrates. These differences were possibly due to changing sediment composition, and the effects of barrier openings at sites closer to entrances (Dye and Barros 2005a; Gladstone et al. 2006; Mikac et al. 2007). Dissimilarities of assemblages within each ICOLL were mainly due to differences in the abundances of nereid and orbiniid polychaetes, Australonereis elhersi and Scoloplos sp., respectively. These species are generally resilient to disturbances and are associated with the

71 Chapter 3: Factors influencing invertebrate faunal assemblages

coarse sediment types found in these areas (Dye and Barros 2005a, 2005b). Further from the entrances, where sediment is generally finer and the organic content is greater, the abundance of capitellid and spionid polychaetes was high (Dye 2006). Spatial variations of epifauna were mainly due to the differences in the abundances of the gastropods Assiminea sienna and Fluviolantus subtortus, although chironomids and crustaceans such as amphipods and isopods also contributed to these variations.

Large-scale spatial variations of invertebrate assemblages between all the ICOLLs were mainly associated with the presence of seagrasses or algae. Dissimilarities of species at Cockrone, Avoca and Wamberal Lagoons are described above; however, richness and abundances in all three were much greater than in Terrigal Lagoon. Gastropods and bivalves were abundant epifauna found on Ruppia sp. and algae within the vegetated ICOLLs, whereas the dominant fauna at Terrigal Lagoon were polychaetes, mainly Australonereis elhersi. This was not unexpected as nereid polychaetes are generally abundant in bare sandy substrates, especially near disturbed sites (Mikac et al. 2007).

Although, habitat and environmental parameters influence the spatial variation in invertebrate assemblages, much of the patchy distribution can be attributed to seasonal or temporal variations (Weate and Hutchings 1977; Lill et al. 2012). Many species were abundant at different times of the year, which is generally associated with increased water temperatures, spawning events, and the life cycles of invertebrates (Hutchings 1999; Aguiaro et al. 2003; Gladstone et al. 2006). However, the bimonthly sampling regime undertaken in this study may not give a true indication of any seasonal differences. Variations found in the invertebrate assemblages of the ICOLLs indicate that the null hypothesis of no differences among ICOLLs in spatial and temporal variation in invertebrate assemblages can be rejected. This is mainly the case for Terrigal Lagoon, which is quite different in a number of respects from the other three ICOLLs.

3.4.4 Influence of environmental variables on invertebrate faunal assemblages The results of the current study show that invertebrate assemblages in the study area were mainly influenced by salinity, turbidity and sediment grain size. All three factors were influential in three different ICOLLs, with water temperature and the distance from the barrier influential at two ICOLLs. Unexpectedly, the barrier status was influential only at Terrigal Lagoon due to the relative frequency of its opening; however, the status of the barrier can indirectly influence invertebrate faunal assemblages by changing the water chemistry, such as salinity and turbidity, within these ICOLLs.

72 Chapter 3: Factors influencing invertebrate faunal assemblages

Salinity was an important factor at Cockrone, Avoca and Terrigal Lagoons. Dramatic changes in salinity can have opposite influences on the composition of invertebrate assemblages. The probable causes of salinity changes between ICOLLs in the current study include, the status of the barrier, overtopping events and the hydrological cycle of ICOLLs, which is the result of changing water levels due to rainfall and run-off, which in turn influences the status of the barrier (Pollard 1994a; Cowley et al. 2001). Elevated salinity levels at Terrigal Lagoon are generally associated with the frequent barrier openings. In contrast, decreased salinity levels at Cockrone Lagoon are associated with long periods of isolation from the sea. Open barriers result in an increase in more marine influenced estuarine species, but when barriers are closed these species tends to decline due to mass mortalities caused by decreasing salinity (Atkinson et al. 1981; Robinson et al. 1983; Hutchings 1999).

Sediment grain size and turbidity were influential factors in determining the structure of infauna at Cockrone, Terrigal and Wamberal Lagoons. Like water parameters, sediment grain sizes generally varied along a gradient, with coarse sand particles found near entrances and finer particles found further away from the entrance. Composition of sediments generally affects turbidity, especially as finer sediments can be resuspended into the water column. Coarse sediment particles are recycled from within Central Coast ICOLLs and adjacent surf zones, while finer material is deposited in the upper reaches from the inputs of creeks and the runoff that enters these ICOLLs around the central basin. Polychaetes such as capitellids and spionids are associated with fine organically-enriched sediments that are found in the central basin and upper reaches, while nereid and orbiinid polychaetes are more abundant near disturbed entrances (Dye and Barros 2005a; Mikac et al. 2007). This was evident in the current study for all ICOLLs, and especially in Terrigal Lagoon, which had no vegetated habitats.

Water temperature and distance from the barrier were also important factors at Avoca and Cockrone Lagoons, and these have also been recognized elsewhere as important variables structuring invertebrate assemblages (Robinson et al. 1983; Dye and Barros 2005a; Gladstone et al. 2006). Many species, including amphipods, are restricted to the entrance areas (Dye 2006); however, the current study found nereid and orbiinid polychaetes dominating sites near the entrances. Abundance and richness of invertebrates generally increases further away from entrances, mainly due to the increase in aquatic vegetation and the sediment type (Dye and Barros 2005a).

The status of the barrier was found to influence invertebrate assemblages only at Terrigal Lagoon, which can be expected due to the numerous openings that occurred throughout the year. However, in some cases it has been shown that barrier openings had little or no effect on

73 Chapter 3: Factors influencing invertebrate faunal assemblages

invertebrate assemblages (Gladstone et al. 2006). Also, changes have been shown to occur due to recruitment from the ocean (Lill et al. 2012). The associated disturbances can cause decreases in species richness and abundance, as well as increased spatial variability (Dye and Barros 2005a; Mikac et al. 2007). Since many invertebrates are highly mobile they are able to rapidly recolonise disturbed areas near ICOLL entrances (Hutchings 1999; Dye and Barros 2005a; Gladstone et al. 2006). Also, due to the constant recycling of sediments after barrier openings, the composition of invertebrate assemblages changes due to mass mortality caused by the smothering action of sediments (Anderson et al. 2004).

Variations found in the invertebrate assemblages of the ICOLLs indicate that the null hypothesis that the environmental factors structuring variations in invertebrate assemblages do not differ among the four ICOLLs and with barrier status being the most important factor, can be rejected.

3.4.5 Implications of the study The invertebrate faunas of ICOLLs have to contend with many environmental changes, including salinity fluctuations, isolation from the sea and habitat degradation. However, they are an important trophic resource for many species of fishes, along with providing essential ecosystem services such as bioturbation of sediments and cycling of nutrients, along with being indicator species for any potential threats (Hirst 2004). Therefore, it is important to understand the factors that influence invertebrate assemblages as these factors are likely to indirectly influence other biota, such as fishes that occur in these ICOLLs, and which utilise invertebrates as food resources (Dye and Barros 2005b). This study has shown that a variety of factors influence invertebrate assemblages, with most being indirectly affected by the status of the barrier. Therefore management strategies increasing artificial openings, or even the lack of openings, may be detrimental to the invertebrate fauna due to changing both water characteristics and habitat destruction. The different invertebrate assemblages occurring within each ICOLL, the different patterns of spatial and temporal variation, and differences among these ICOLLs in the suite of environmental variables responsible for variation in invertebrate assemblages all indicate that each of the Central Coast ICOLLs should be managed independently.

3.5 Conclusion In general, water chemistry characteristics of each ICOLL in this study were shown to be uniform throughout their water area, and variability generally changed after barrier openings, especially for salinity and turbidity. The extensive foreshore development around Terrigal Lagoon resulted in this ICOLL being artificially opened much more frequently than the other ICOLLs. Invertebrate assemblages overall were dominated by crustaceans, polychaetes and

74 Chapter 3: Factors influencing invertebrate faunal assemblages

molluscs, which were more abundant in Cockrone, Avoca and Wamberal Lagoons which have Ruppia sp. and algal habitats. In comparison, Terrigal Lagoon was dominated by polychaetes, probably due to the lack of aquatic vegetation. The type of invertebrate fauna found within each ICOLL may also have consequences on the composition of fish assemblages found in Central Coast ICOLLs, as certain species of fishes target specific invertebrates. Complex patterns of spatial and temporal variation in invertebrate assemblages, species richness, and total abundance were found within and between ICOLLs. No single variable was influential at all ICOLLs; instead, salinity was the main variable influencing the invertebrate fauna, along with turbidity, water temperature and sediment composition. With the exception of Terrigal Lagoon, barrier status was not a major influence on invertebrate assemblages; however, the status of the barrier can indirectly affect other environmental variables such as salinity, turbidity and sediment composition.

75 Chapter 3: Factors influencing invertebrate faunal assemblages

Appendices: Invertebrate faunal assemblages and water variables of ICOLLs

76 Chapter 3: Factors influencing invertebrate faunal assemblages

Appendix 1a. Total abundance of invertebrate infauna collected from Cockrone Lagoon from December 2004 to October 2005 (sites 1-6) and invertebrate epifauna collected from Ruppia sp. (site 4R) and from algae (sites 4A and 5A). Site Taxon/Family Species 1 2 3 4 4 R 4 A 5 5A 6 Total Hirudinea Glossiphoniidae 4 2 6 Oligochaeta 2 1 6 9 Polychaeta Capitellidae Notomastus estuarius 3 7 98 42 113 3 266 Unknown capitellid 3 3 Nereididae Australonereis elhersi 27 30 32 13 102 Nereis maxillodentata 48 91 106 8 8 261 Simplestia aequisetis 43 21 7 43 2 4 9 129 Simplestia turveyi 15 2 7 5 29 Unknown nereid 38 5 43 Orbiinidae Leitoscolopos sp. 13 3 8 20 12 1 57 Scoloplos simplex 13 1 1 15 Spionidae Orthoprionspio sp. 15 28 61 3 93 4 39 243 Amphipoda Corophiidae Paracorophium sp. 1 29 7 34 71 Melitidae Melita sp. 1 5 6 4 6 22 Paracalliopiidae Paracalliope australis 2 7 10 1 20 Paracalliope 5 2 4 11 Isopoda Sphaeromatidae Cymodetta sp. 4 48 52 Insecta Chironomidae Chironomus sp. 4 3 16 6 56 85 Culicidae Culicini sp. 1 1 Pyralidae Nymphula sp. 1 3 4 Bivalva Leptonidae Arthritica helmsi 4 212 85 60 11 15 387 Trapeziidae Fluviolantus subtortus 1 1 78 112 28 14 8 7 249 Gastropoda Amphibolidae Salinator fragilis 1 4 1 6 Assimeidae Assiminea siennae 31 130 4 1 92 258 Hydrobiidae Tatea rufilabris 2 2 Unknown 3 3 Total number of individuals 2334

77 Chapter 3: Factors influencing invertebrate faunal assemblages

Appendix 1b. Total abundance of invertebrate infauna collected from Avoca Lagoon from December 2004 to October 2005 (sites 1-6) and invertebrate epifauna collected from Ruppia sp. (site 3R) and from algae (sites 4A and 5A). Taxon/Family Site Species 1 2 3 3R 4 4A 5 5A 6 Total Hirudinea Glossiphoniidae 17 17 Oligochaeta 1 5 1 7 Polychaeta Capitellidae Notomastus estuarius 4 7 38 13 144 3 10 40 259 Unknown capitellid 1 1 Nereididae Australonereis elhersi 11 18 2 5 26 1 1 1 65 Nereis maxillodentata 14 37 46 41 17 17 1 59 232 Simplestia aequisetis 4 25 62 9 45 13 80 9 23 270 Unknown nereid 1 1 2 Orbiinidae Leitoscoloplos sp. 1 2 2 2 2 2 11 Scoloplos simplex 29 3 3 1 11 47 Spionidae Orthoprionospio sp. 53 21 1 10 5 6 4 3 103 Unknown spionid 8 1 9 Amphipoda Corophiidae Paracorophium sp. 51 15 14 64 14 158 Melitidae Melita sp. 9 2 11 Paracalliopiidae Paracalliope australis 4 5 24 4 1 38 Paracalliope 34 5 17 2 56 1 115 Unknown amphipod 1 1 1 3 Isopoda Sphaeromatidae Cymodetta sp. 1 1 2 Insecta Chironomidae Chironomus sp. 5 8 2 8 9 32 Bivalvia Leptonidae Arthritica helmsi 7 29 1 33 2 116 13 129 330 Mytilidae Xenostrobus securis 2 2 28 1 9 9 48 99 Psammobiidae Soletellina alba 50 1 51 Trapeziidae Fluviolantus subtortus 1 2 5 8 4 12 28 3 63 Gastropoda Amphibolidae Salinator fragilis 12 1 1 23 12 9 60 Aplysiidae Dolabella auricularia 2 2 Assimeidae Assiminea siennae 4 21 113 29 317 33 381 2 900 Nassaridae Nassarius jonsii 1 1 Onchidiidae Onchidella patelloides 2 2 Nematoda 1 1 2 Unknown 1 1 2 Total number of individuals 2894

78 Chapter 3: Factors influencing invertebrate faunal assemblages

Appendix 1c. Total abundance of invertebrate infauna collected from Terrigal Lagoon from December 2004 to October 2005 (sites 1-4). Site Taxon/Family Species 1 2 3 4 Total Bivalva Leptonidae Arthritica helmsi 7 7 Amphipoda Unknown amphipod 2 2 Oligochaeta 3 3 Polychaeta Capitellidae Notomastus estuarius 5 4 9 Unknown capitellid 4 4 Eunicidae Marphysa sanguinea 3 7 10 Nereididae Australonereis elhersi 22 174 7 203 Nereis maxillodentata 1 4 1 6 Simplestia aequisetis 3 81 21 48 153 Unknown nereid 2 2 Orbiinidae Leitoscoloplos sp. 2 10 24 19 55 Scoloplos simplex 17 24 5 46 Total number of individuals 500

79 Chapter 3: Factors influencing invertebrate faunal assemblages

Appendix 1d. Total abundance of invertebrate infauna collected from Wamberal Lagoon from December 2004 to October 2005 (sites 1-6) and invertebrate epifauna collected from Ruppia sp. (sites 3R, 4R and 6R). Taxon/Family Species Site Total 1 2 3 3R 4 4R 5 6 6R Hirudinea Glossiphoniidae 1 3 10 7 1 22 Oligochaeta 2 2 20 12 36 Polychaeta Capitellidae Notomastus estuarius 2 5 17 4 25 6 59 Notomastus sp. 16 16 Unknown capitellid 18 2 20 Eunicidae Marphysa sanguinea 1 1 Nereididae Australonereis elhersi 11 6 11 28 Nereis maxillodentata 6 14 20 Simplestia aequisetis 40 17 52 10 2 35 14 170 Unknown nereid 5 3 8 Orbiinidae Leitoscolopos sp. 2 1 3 Scoloplos simplex 5 5 Unknown orbiinid 1 1 Serpulidae 3 3 Spionidae Orthoprionospio sp. 12 43 8 9 12 11 3 98 Chelicerata 1 1 Amphipoda Corophiidae Paracorophium sp. 17 6 21 1 45 Melitidae Melita sp. 2 2 Paracalliopiidae Paracalliope australis 9 41 3 53 Paracalliope sp. 3 9 32 3 47 Unknown amphipod 2 2 Decapoda Hymenosodiidae Halicarcinus australis 1 1 Isopoda Sphaeromatidae Cymodetta sp. 5 21 9 23 4 2 64 Athuridea Mesanthura calaena 12 2 14 Insecta Chironomidae Chironomus sp. 1 42 16 2 1 4 66 Protoneuridae Notosticta solida 1 1 Pyralidae Nymphula sp. 2 2 Bivalvia Leptonidae Arthritica helmsi 18 19 22 1 1 61 Mytilidae Xenostrobus securis 1 1 1 1 1 30 35 Trapeziidae Fluviolantus subtortus 30 27 14 193 2 303 17 1 587 Gastropoda Amphibolidae Salinator fragilis 1 18 32 3 1 55 Assimeidae Assiminea siennae 1 74 26 101 Hydrobiidae Tatea rufilabris 2 6 7 Unknown gastropod 1 1 Total number of individuals 1635

80 Chapter 3: Factors influencing invertebrate faunal assemblages

Appendix 2a. Spatial and temporal mean (a) salinity (ppt), (b) turbidity (ntu) and (c) water temperature (°C) (sites 1-6) from Cockrone Lagoon between November 2004 and October 2005. The dotted vertical line indicates a single barrier opening that occurred between sampling periods. Symbols denote: (♦) site 1, (■) site 2, (▲) site 3, (□) site 4, (ο) site 5, and (●) site 6. The high turbidity at site 4 (graph b), is possibly due to the effects from run-off and the low water depth at the time of sampling.

(a)

40 35 30 25

20 ppt 15 10 5 0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct 04 04 05 05 05 05 05 05 05 05 05 05

(b)

30 ntu

0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct 04 04 05 05 05 05 05 05 05 05 05 05

(c)

20 C 15

0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct 04 04 05 05 05 05 05 05 05 05 05 05 Sampling period

81 Chapter 3: Factors influencing invertebrate faunal assemblages

Appendix 2b. Spatial and temporal mean (a) salinity (ppt), (b) turbidity (ntu) and (c) water temperature (°C) (sites 1-6) from Avoca Lagoon between November 2004 and October 2005. The dotted vertical line indicates a single barrier opening that occurred between sampling periods. Symbols denote: (♦) site 1, (■) site 2, (▲) site 3, (□) site 4, (ο) site 5, and (●) site 6. The high turbidity at site 6 (graph b), is possibly due to the effects from run-off and the low water depth at the time of sampling.

(a)

40 35 30 25

ppt 20 15 10 5 0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct 04 04 05 05 05 05 05 05 05 05 05 05

(b)

40 ntu 30

0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct 04 04 05 05 05 05 05 05 05 05 05 05 Sampling period

(c)

20 C 15

0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct 04 04 05 05 05 05 05 05 05 05 05 05 Sampling period

82 Chapter 3: Factors influencing invertebrate faunal assemblages

Appendix 2c. Spatial and temporal mean (a) salinity (ppt), (b) turbidity (ntu) and (c) water temperature (°C) (sites 1-4) from Terrigal Lagoon between November 2004 and October 2005. The dotted vertical lines indicate a single barrier opening that occurred between sampling periods. The solid vertical lines indicate multiple barrier openings that occurred between sampling periods. Symbols denote: (♦) site 1, (■) site 2, (▲) site 3, and (□) site 4. The high turbidity at site 1 (graph b), is possibly due to the effects either from stormwater run-off, barrier openings, the lack of seagrass and/or the low water depth and recreational activities at the time of sampling.

(a)

20 ppt 15

0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct 04 04 05 05 05 05 05 05 05 05 05 05

(b)

200 180 160 140 120 100

ntu 80 60 40 20 0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct 04 04 05 05 05 05 05 05 05 05 05 05

(c)

0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct 04 04 05 05 05 05 05 05 05 05 05 05 Sampling period

83 Chapter 3: Factors influencing invertebrate faunal assemblages

Appendix 2d. Spatial and temporal mean (a) salinity (ppt), (b) turbidity (ntu) and (c) water temperature (°C) (sites 1-6) from Wamberal Lagoon between November 2004 and October 2005. The dotted vertical line indicates a single barrier opening that occurred between sampling periods. Symbols denote: (♦) site 1, (ο) site 2, (▲) site 3, (□) site 4, (■) site 5, and (●) site 6. The differences in salinity and turbidity at site 6 (graph a and b), is possibly due to the effects either from freshwater inputs from the creek after a major rainfall event, the lack of seagrass and/or the low water depth along with the effects of strong winds that are evident at this site.

(a)

ppt 15

0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct 04 04 05 05 05 05 05 05 05 05 05 05

(b)

40 35 30 25

ntu 20 15 10 5 0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct 04 04 05 05 05 05 05 05 05 05 05 05

(c)

20 C 15

0 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct 04 04 05 05 05 05 05 05 05 05 05 05 Sampling period

84 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Chapter 4: Effects of barrier openings on larval and juvenile fish assemblages within ICOLLs and in adjacent surf zones.

85 Chapter 4: Effects of barrier openings on larval and juvenile fishes

4.1 Introduction Coastal aquatic habitats are recognised as important nursery areas or temporary habitats for the larval and/or juvenile phases of many species of fish. The highly productive nature of estuaries makes them ideal nursery areas for certain species of fish, including species important for commercial and recreational fisheries (Griffiths 2001a). In comparison, the highly dynamic and complex nature of surf zones make them less suitable as nursery areas due to the lack of structural components important for providing shelter and protection, as does their low primary productivity (Suda et al. 2002; Inoue et al. 2008). Both estuarine and surf zone environments are common along coastlines. However, the biological and environmental interaction between Intermittently Closed and Open Lakes and Lagoons (ICOLLs) and their adjacent surf zones is restricted by barrier formations that isolate these estuaries for extended periods. The dynamics of these barriers can thus strongly influence larval and juvenile fish assemblages that utilise both environments (Griffiths and West 1999; Vorwerk et al. 2003).

ICOLLs comprise 45% of the estuaries of New South Wales (NSW) (Griffiths and West 1999) and generally have similar characteristics, including shallow and deep water, fringing wetlands, sandy sediments near the entrance, and a central muddy basin, along with seagrasses and associated algae (Cheng 1981). ICOLLs are relatively stable and highly-productive environments with small catchments, restricted freshwater inflows and extended barrier closures, and a general lack of large predatory fishes. These factors make ICOLLs potentially suitable as nursery areas for both resident species and marine species recruiting via adjacent surf zones (Griffiths and West 1999; Griffiths 2001a). The widespread occurrence of ICOLLs suggests that they play a role as important fish habitats (Pollard 1994b) influenced by the duration, frequency and timing of barrier openings (Griffiths 1999; Griffiths and West 1999).

In general, ICOLLs are utilised by four broad fish groups: freshwater species, estuarine species, catadromous species and marine species (Whitfield 1989). Species richness of estuaries is dependent on whether fishes use them for nursery areas, migratory pathways, or as a habitat for their entire lifespan (Kennish 1990), and also the type and geographical location of these estuaries. Extended barrier closures result in all ICOLL fauna consisting predominately of small-sized resident fishes (e.g. atherinids, eleotrids and gobiids) that spend their entire lifecycle in ICOLLs, and are able to tolerate the environmental changes that may occur when barriers are opened (Miskiewicz 1987; Griffiths 2001a). Natural or artificial barrier openings encourage the movement of marine–estuary dependant fishes (e.g. sparids, mugilids and silliginids) between the two environments (SPCC 1981; Griffiths 2001a). Marine conditions within ICOLLs resulting from barrier openings, especially near their entrances, support estuarine and marine

86 Chapter 4: Effects of barrier openings on larval and juvenile fishes

fishes (e.g. ambassids and some clupeids) and many marine transients; however, fish densities can decrease when barriers close and salinities begin to decline (Griffiths 2001a).

Recent studies of the fish assemblages of ICOLLs along the south-east coast of Australia have generally been restricted to a few localities and short time frames (Jones and West 2005). In general, there is little information regarding the larval and juvenile fish assemblages of surf zones along the NSW coast (Geraghty 2004) and the effects of ICOLL barrier openings on the assemblages of larval and juvenile fishes of ICOLLs and their adjacent surf zones. Such information is of great importance as many ICOLLs are opened numerous times per year by artificial practices (Gladstone et al. 2006). Also, recruitment processes need to be identified for species that utilise ICOLLs and to recognise if surf zones act as alternate habitats or transition sites for fishes waiting to enter ICOLLs when barriers are opened, and/or whether recruitment can occur via overwash events (Cowley et al. 2001; Strydom 2003; Kemp and Froneman 2004).

Most coastlines have natural or artificial structures that can provide shelter and protection for larval and juvenile fishes; however, surf zones are highly dynamic environments that generally lack any structure. The intermittent nature of barriers make many ICOLLs unavailable to larval and juvenile fishes, therefore alternate habitats need to be found (Lenanton 1984; Strydom 2003; Geraghty 2004). Since many ICOLLs are fronted by sandy beach surf zones the changing dynamics of these areas can form microhabitats (Ayvazian and Hyndes 1995). Temporary shelter and nursery areas are, however, provided by transverse bars, rip current troughs, increased turbidity and turbulence (Watt-Pringle and Strydom 2003; Inoue et al. 2008). Larval and juvenile fishes accumulate in surf zones adjacent to ICOLL entrances (Harris and Cyrus 1996; Clark 1997; Cowley et al. 2001; Strydom 2003), and unlike those of ICOLLs, these surf zone assemblages are generally dominated by a few characteristic species groups (Suda et al. 2002).

Surf zone fish assemblages often consist of large numbers of larval and juvenile individuals of species that dominate these areas as adults (Inui et al. 2010). The seasonal structure of these assemblages is influenced by variations in physical factors such as wave action (Romer 1990; Clark 1997), salinity and turbidity (Strydom 2003; Nanami and Endo 2007; Inui et al. 2010), the timing of spawning (Gibson et al. 1993), recruitment peaks (Mariani 2001), the length of residency (Senta and Kinoshita 1985; Sato et al. 2008), and feeding (Inoue et al. 2008; Marrin- Jarrin et al. 2009).

This study attempts to provide some understanding of the interactions that may occur between ICOLLs and their adjacent surf zones in aiding or impeding the recruitment of larval and 87 Chapter 4: Effects of barrier openings on larval and juvenile fishes

juvenile fishes into these environments. In order to fully understand recruitment processes into ICOLLs, the following questions need to be addressed: 1. Do larval and juvenile fish assemblages of surf zones and ICOLLs differ before and after opening events? 2. Do larval and juvenile fish movements occur between the two environments?

This study tested the following null hypotheses: 1. There is no temporal variation in the assemblages of larval and juvenile fishes of ICOLL and surf zone habitats. 2. There is no spatial variation in the assemblages of larval and juvenile fishes of ICOLL and surf zone habitats. 3. The assemblages of larval and juvenile fishes of ICOLLs and adjacent surf zones do not differ. 4. Opening of ICOLL barriers is not followed by the movement of larval and juvenile surf zone fishes into ICOLLs.

4.2 Materials and Methods

4.2.1 Pilot study A larval beach seine (Figure 4.1) was used to collect sub-adult fishes from ICOLLs (near the entrance barrier) and from the adjacent surf zones. A pilot study was undertaken to select the optimal sampling strategy by assessing four factors as sources of variation in the mean numbers of species and total numbers of fishes captured: number of replicates (n=2 to n=6), transect length (20, 30 and 50 m), lunar cycles (new and full moon) and time of day (day, night). Day and night samplings were compared on full moons and new moons during January and February 2006 at Terrigal Lagoon and surf zone areas of Terrigal Beach. Six transects of 20 m and 50 m were seined longitudinally in the lagoon entrance. Due to safety concerns, especially at night, only 30 m transects were sampled in the surf zone at low tide. Alternative sampling strategies were compared using sampling precision (standard error (SE)/ mean) (Andrew and Mapstone 1987). Specimens were collected with permission from the University of Newcastle’s Animal Care and Ethics Committee (ACEC Permit number 9711006) and the NSW Department of Primary Industries (Fisheries Permit number P05/0092).

Results for Terrigal Lagoon show that sampling precision for total number of fishes was similar for 20 m and 50 m hauls during both full and new moon phases and that sample sizes of n=4 to n=6 replicate hauls provided mean values with an acceptable precision (Figure 4.2). Terrigal Beach results also show some similarities of sampling precision for total number of fishes

88 Chapter 4: Effects of barrier openings on larval and juvenile fishes

between new and full moon phases and at each site. The analysis of sampling precision suggested n=4 replicates provided means with an acceptable precision (Figure 4.3).

Figure 4.1. Illustration of beach seine net used for sampling larval and juvenile fishes from surf zones and ICOLLs (after Geraghty 2004).

Terrigal Lagoon New and Full Moon

0.9

0.8

0.7

0.6 50m full moon 50m new moon 0.5 20m full moon 20m new moon 0.4

0.3 se/meannumber of individuals 0.2

0.1

0 2 3 4 5 6 Number of replicates

89 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Terrigal Beach New and Full Moon

1.2

0.8 south full moon adjacent full moon north full moon 0.6 south new moon adjacent new moon north new moon

0.4 se/meannumber of individuals

0.2

0 2 3 4 5 6 Number of replicates

4.2.2 Field fish collection and laboratory analyses ICOLLs and surf zones were sampled bimonthly and after a barrier opening, during the low tide period between April 2006 and March 2007 (Table 4.1). Variations in lunar phases were not considered due to the small variations in abundances of larval and juvenile fishes collected between the new and full moons during the pilot study. The order in which ICOLLs and surf zones were sampled was randomized. No sampling was conducted in surf zones during March 2007 at Copacabana and Wamberal Beaches due to dangerous seas and adverse weather conditions. Sampling occurred immediately after barriers had closed, with barriers taking 1-7 d to close. Four parallel 30 m transects were hauled by hand approximately 10 m from the shore or up to a maximum depth of 1.5 m. To maintain independence of replicates, tows were performed 10 m apart. To account for possible small-scale spatial variation in the abundances of fishes (Gray et al. 2009), sampling in surf zones occurred at three sites that were located approximately 100 m south, 100 m north and adjacent to ICOLL entrances (Figure 4.4). The sampling design (the number of samples and the timing of sampling) are described in Chapter Two (Tables 2.3-2.6).

90 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Table 4.1. ICOLL and surf zone sampling periods between April 2006 and March 2007. *denotes ICOLLs only sampled due to dangerous surf and adverse weather conditions. ICOLL Cockrone Avoca Terrigal Wamberal Lagoon/Copacabana Beach Lagoon/Avoca Lagoon/Terrigal Beach Lagoon/Wamberal Beach Beach 19/4/06 20/4/06 21/4/06 23/4/06 19/6/06 1/6/06 4/6/06 18/6/06 15/6/06 14/6/06 25/6/06 11/7/06 2/8/06 16/8/06 3/8/06 18/8/06 19/9/06 29/9/06 21/9/06 2/10/06 13/11/06 27/11/06 29/11/06 12/11/06 28/1/07 29/1/07 13/1/07 12/1/07 12/3/07* 13/3/07 28/3/07 28/3/07*

91 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Collected fish were euthanased in an ice slurry and fixed in 70% ethanol in the field. Samples were returned to the lab where fishes were identified, counted, and measured to the nearest 1 mm (total length). Fishes were identified to the lowest possible taxon using Collette (1974), Neira et al. (1998) and Leis and Carson-Ewart (2000). Large numbers of adult fishes were collected from both environments; however, only specimens defined as sub-adult fishes, which are generally considered to comprise the size class between juveniles and mature adults, were considered for data analysis. Terminologies used to describe sub-adult fishes follow Neira et al. (1998). A larva is the developmental stage between hatching and the attainment of full external meristic characteristics (fins and scales) and includes yolk-sac, preflexion and flexion stages as well as transitional and transformation stages of some demersal and benthic fishes. Juvenile fishes are defined as having lost all larval characteristics (Neira et al. 1998) and were sub- adults.

4.2.3 Life history categories Collected species were categorised into one of the following life history categories based on information in SPCC (1981), Griffiths (2001a) and Geraghty (2004): Freshwater (F): are species that are usually confined to freshwater or brackish environments. Resident (R): are species that spend their entire life cycle in estuarine systems. Marine-estuary dependant (MED): are species that use estuaries as juvenile nursery areas. Estuarine and Marine (EM): include species for which all life-cycle stages have been observed in both estuarine and marine waters. Transient (T): include marine species that occasionally enter estuaries and are usually found in low numbers where salinities are relatively high. Marine (M): are marine species that spend their entire life in marine waters.

4.2.4 Environmental variables Salinity and water temperature were recorded in situ, as these are important factors linked to the recruitment of larval and juvenile fishes into ICOLLs (Strydom 2003). Each variable was measured at a depth of 0.5 m at each site (Figure 4.4) using an YSI 30 water quality probe meter. Where salinity values were not measured in situ due to probe malfunction, water samples were collected and frozen in the laboratory until measured in parts per thousand (ppt) using a WTW LF 330 conductivity meter. Salinities were not measured in surf zones, as they were considered to be near the standard sea values of ~35 ppt. Artificial barrier openings are managed by Gosford City Council (GCC) and data on the dates of openings was provided by GCC. There is, however, also the possibility of illegal openings by residents and natural openings and these were also determined with water level data from the Manly Hydraulic Laboratories website (http://mhl.nsw.gov.au). When the data indicated this type of opening had occurred it was confirmed by visual inspection. 92 Chapter 4: Effects of barrier openings on larval and juvenile fishes

4.2.5 Sampling design and data analysis It was not possible to use a before-after-control-impact (BACI) design to test if barrier openings affected larval and juvenile fishes of ICOLLs and surf zones for the following reasons: (i) ICOLLs differed in their frequency, timing and duration of openings, (ii) the unpredictable nature of ICOLL openings meant that it was not possible to assign, a priori, a particular set of ICOLLs as unopened controls and (iii) the frequency of ICOLL openings meant there was insufficient time to develop a baseline of natural temporal variation before an opening occurred. Therefore an alternative approach was used to assess the likelihood of an effect of ICOLL openings on fish assemblages.

One-factor analyses of variance (ANOVA) were used to test whether there were significant differences in the numbers of species, total fish abundance, and total abundances of individual species among sampling periods, in both ICOLLs and surf zones. A large number of samples from surf zones caught no fishes, therefore data from north, adjacent and southern sites at each beach were combined and analysed as a single sample with 12 replicates. Time was analysed as a fixed factor. For all ANOVAs, homogeneity of variance was tested with Cochran’s test, and when necessary data sets were transformed prior to ANOVA. When transformation did not eliminate heterogeneous variance the raw data were analysed at an adjusted significance level of p=0.01 (Underwood 1997). Significant effects were further investigated post-hoc using Student- Newman-Keuls (SNK) tests (Underwood 1997). ANOVA analyses were performed using GMAV5 software (Centre for Research on Ecological Impacts of Coastal Cities, University of Sydney). The number of occasions in which a significant SNK test of successive sample periods coincided with an ICOLL opening between these periods was compared with the number of occasions when a significant SNK test did not coincide with an ICOLL opening. A chi-square test was used to test the hypotheses that changes in fish abundance, the number of species and the abundances of each of the dominant species, over a sampling period (i.e. increase, decrease, no change) were independent of the status of the ICOLL entrance (i.e. open, closed).

Multivariate analysis was used to test the null hypothesis that assemblages of larval and juvenile fishes of ICOLLs and adjacent surf zones did not differ through time. Sampling periods when no larval and juvenile fishes were collected were not included in the analysis. Data were square- root transformed and the Bray-Curtis resemblance measure was used. Temporal variations in assemblages were visualised by hierarchical agglomerative clustering. A one-factor Analysis of Similarities (ANOSIM) was used to test the null hypotheses of no temporal variation in assemblages of larval and juvenile fishes of each ICOLL and of each surf zone. Multivariate analyses were done with PRIMER v6 (Plymouth Routines in Multivariate Ecological Research).

93 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Using the same approach as previously described, a decision about an effect of ICOLL openings was based on an examination of the magnitude and significance of pair-wise R-values between successive bi-monthly samples with and without an ICOLL opening. A chi-square test was used to test the hypothesis that changes in fish assemblages over the sampling period (i.e. change, no change) were independent of the status of the ICOLL entrance (i.e. open, closed). The Similarity of Percentages (SIMPER) procedure in PRIMER (Clarke 1993) was used to determine the species that caused significant temporal variation in assemblages of larval and juvenile fishes of ICOLLs and surf zones. Species that contributed up to 90% of the dissimilarity of the significant ANOSIM pair-wise tests were analysed. Large values (i.e. >1) of the ratio of dissimilarity/standard deviation(dissimilarity) for a species (where dissimilarity is the average contribution of the ith species to the overall dissimilarity between 2 groups of standard deviation) indicated that it was consistently important to dissimilarity in all pairwise comparisons of samples in 2 groups (Clarke 1993). Species with a percentage dissimilarity >3% and with a dissimilarity/standard deviation (dissimilarity) >1 were regarded as being important contributors to dissimilarity between the barrier status (Terlizzi et al. 2005).

Jaccard’s similarity coefficient was used to test the null hypothesis that ICOLL openings were followed by the movement of larval and juvenile surf zone fishes into the adjacent ICOLL or vice-versa. Records of species presence from two sampling periods before and two sampling periods after an opening event were used to test this hypothesis. Jaccard’s coefficient represents similarities in species between two sites using the formula [a/ (a+b+c)], where a=number of species present at both sites, b=number of species present only at site 1 (i.e. ICOLLs) and c=number of species present only at site 2 (i.e. surf zones). The resulting values vary between 0 (no species in common) to 1 (identical species composition) (Gibson et al. 1993; Harrison and Whitfield 1995). A t-test was used to test whether there was a significant difference in the mean Jaccard’s coefficient from before to after ICOLL openings. A significant increase would suggest indirectly that species were leaving ICOLLs and gathering in the adjacent surf zone, or alternatively that species were entering ICOLLs from the surf zone. In order to determine if larval and juvenile fishes had moved between the two environments a Kolmogorov-Smirnov (K-S) test was used to determine length frequency differences before and after barrier openings.

4.3 Results

4.3.1 ICOLL openings and environmental variables of ICOLLs and adjacent surf zones Over the course of the larval and juvenile fish study, between them the four ICOLLs opened 14 times. Terrigal Lagoon opened on nine occasions, Avoca and Wamberal Lagoons opened twice, and Cockrone Lagoon opened once (Table 4.2). 94 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Table 4.2. ICOLL barrier openings between April 2006 and February 2007. *denotes Gosford City Council sanctioned artificial barrier opening. Other barrier opening data, whether an illegal artificial opening or #natural opening, were obtained from Manly Hydraulic Laboratories and confirmed by visual inspection. ICOLL Cockrone Avoca Terrigal Wamberal 7/9/06* 6/6/06* 5/6/06* 20/6/06* 20/6/06* 4/7/06* 19/7/06* 25/7/06* 5/8/06* 25/8/06* 8/9/06* 8/9/06* 9/9/06# 21/12/06* 27/2/07*

Water temperature of ICOLLs varied from 11.8°C (Terrigal in July 2006) to 27°C (Avoca in January 2007) (Figure 4.5). Water temperatures of the surf zones varied from 15°C (Terrigal Beach in July 2006) to 22.6°C (Avoca Beach in March 2007) (Figure 4.6). Salinity varied between ICOLLs with Cockrone Lagoon ranging between 4.7 and 27.4 ppt, Avoca Lagoon ranging between 8 and 26.9 ppt, Terrigal Lagoon ranging between 11.6 and 31.4 ppt, and Wamberal Lagoon ranging between 4.6 and 23.7 ppt (Figure 4.7). In the majority of cases salinity increased in ICOLLs after barrier openings. Salinities were not measured in surf zones, as they were considered to be near the standard sea values of ~35 ppt.

95 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Cockrone Lagoon Avoca Lagoon

30 30

25 25

20 20

C) °

15 15

10 10 Water temperature ( temperature Water

5 5

0 0 Apr-06 May-06 Jun-06 Jul-06 Aug-06 Sep-06 Oct-06 Nov-06 Dec-06 Jan-07 Feb-07 Mar-07 Apr-06 May-06 Jun-06 Jul-06 Aug-06 Sep-06 Oct-06 Nov-06 Dec-06 Jan-07 Feb-07 Mar-07

Terrigal Lagoon Wamberal Lagoon

30 30

25 25

C) °

20 20

15 15 Water temperature ( temperature Water

10 10

5 5

0 0 Apr-06 May-06 Jun-06 Jul-06 Aug-06 Sep-06 Oct-06 Nov-06 Dec-06 Jan-07 Feb-07 Mar-07 Apr-06 May-06 Jun-06 Jul-06 Aug-06 Sep-06 Oct-06 Nov-06 Dec-06 Jan-07 Feb-07 Mar-07 Month Month Figure 4.5. Water surface temperature (°C) sampled at ICOLLs from April 2006 to March 2007. The dotted vertical lines indicate a single barrier opening occurred between sampling periods. The solid vertical lines indicate multiple barrier openings occurred between sampling periods.

Copacabana Beach Avoca Beach

22 25 21 20

C) °

19 15

18 10

17 Water temperature temperature ( Water 5 16

15 0 Apr 06 Jun 06 Aug 06 Sept 06 Nov 06 Jan 07 Mar 07 Apr 06 Jun 06 Aug 06 Sept 06 Nov 06 Jan 07 Mar 07 Terrigal Beach Wamberal Beach

25 25

20 20

C) ° 15 15

10 10 Water temperature temperature ( Water 5 5

0 0 Apr 06 Jun 06 Jul 06 Aug 06 Sep 06 Nov 06 Jan 07 Mar 07 Apr 06 Jun 06 Aug 06 Oct 06 Nov 06 Jan 07 Mar 07 Month Month Figure 4.6. Water surface temperature (°C) sampled at surf zones from April 2006 to March 2007.

96 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Cockrone Lagoon Avoca Lagoon

30 30

25 25

20 20 ppt

15 15

10 10

5 5

0 0 Apr 06 Jun 06 Aug 06 Sept 06 Nov 06 Jan 07 Mar 07 Apr 06 Jun 06 Aug 06 Sept 06 Nov 06 Jan 07 Mar 07

Terrigal Lagoon Wamberal Lagoon 35 25

30 20 25 15

20 ppt 15 10 10 5 5

0 0 Apr 06 Jun 06 Jul 06 Aug 06 Sept 06 Nov 06 Jan 07 Mar 07 Apr 06 Jun 06 Aug 06 Oct 06 Nov 06 Jan 07 Mar 07 Month Month Figure 4.7. Water surface salinity (ppt) sampled at ICOLLs from April 2006 to March 2007. The dotted vertical lines indicate a single barrier opening occurred between sampling periods. The solid vertical lines indicate multiple barrier openings occurred between sampling periods. Salinities were not measured in surf zones.

4.3.2 Larval and juvenile fishes of ICOLLs A total of 3 308 larval and juvenile fishes representing 12 species (9 families) were collected from the four ICOLLs between April 2006 and March 2007. Eleotridae (n=1844), Sparidae (n=623), Atherinidae (n=564) and Gobiidae (n=171) were the numerically-abundant families collected (Table 4.3). The greatest total number of fishes was recorded from Wamberal Lagoon (n=1 842) and the smallest total number was recorded from Terrigal Lagoon (n=89). Cockrone Lagoon (5 families, 5 species) was dominated by a marine-estuary dependant (MED) species the yellowfin bream, Acanthopagrus australis (Sparidae) (n=623). Avoca Lagoon (5 families, 6 species) was dominated by an R species, the flathead gudgeon, Philypnodon grandiceps (Eleotridae) (n=513). Terrigal Lagoon (5 families, 5 species) was dominated by an estuarine and marine (EM species), the Port Jackson perchlet, Ambassis jacksoniensis (Ambassidae) (n=60). Wamberal Lagoon (4 families, 4 species) was dominated by two resident (R) species, the flathead gudgeon, P. grandiceps (n=1 319), and the small-mouthed hardyhead, Atherinosoma microstoma (Atherinidae) (n=409).

Table 4.3. Total numbers of larval and juvenile fishes collected in ICOLLs from April 2006 to March 2007, showing life history categories (F=Freshwater, R=Resident, MED=Marine–estuary dependant, EM=Estuarine and marine, T=Transient and M=Marine species), and range in total length (TL). ICOLLs Family Species Life history Cockrone Avoca Terrigal Wamberal TL (mm) Total number Ambassidae Ambassis jacksoniensis EM 0 0 60 0 13-21 60 Ambassis marianus EM 0 0 0 16 6-11 16 Atherinidae Atherinosoma microstoma R 64 91 0 409 8-23 564 Eleotridae Philypnodon grandiceps R 5 513 7 1319 7-23 1844 Gobiidae Gobiopterus semivestitus R 0 0 2 0 16-18 2 Pseudogobius olorum R 10 61 0 98 6-22 169 Hemiramphidae Hyporhamphus regularis EM 0 0 1 0 23 1 Mugilidae Mugil cephalus MED 5 3 0 0 20-24 8 Myxus elongatus MED 0 1 0 0 10 1 Poeciliidae Gambusia holbrooki F 0 1 0 0 15 1 Sillaginidae Sillago ciliata M 0 0 19 0 13-29 19 Sparidae Acanthopagrus australis MED 623 0 0 0 9-18 623 Total number 707 670 89 1842 3308

Chapter 4: Effects of barrier openings on larval and juvenile fishes

4.3.3 Temporal variation in assemblages of larval and juvenile fishes of ICOLLs The mean number of larval and juvenile fishes collected per haul across all sampling periods for each ICOLL varied, Cockrone Lagoon ( =25.2±11.4, n=28), Avoca Lagoon ( =21.5±6.1, n=33), Terrigal Lagoon ( =2.5±0.9, n=36) and Wamberal Lagoon ( =57.6±16.8, n=32). Significant temporal variations in total abundance of larval and juvenile fishes occurred in all ICOLLs (Table 4.4). Mean abundance of larval and juvenile fishes was greatest during November 2006 for Cockrone and Wamberal Lagoons and November 2006 and January 2007 for Avoca Lagoon. At Terrigal Lagoon, mean abundances were greater during April 2006 and March 2007, with low numbers of fish sampled in between these sampling periods (Figure 4.8). Post-hoc SNK comparisons of successive samples across all ICOLLs showed openings were not followed by either a significant increase or decrease in the mean total abundance of larval and juvenile fishes (Table 4.5). The magnitude of change in the mean total abundance was independent of the status of the lagoon entrance during the sampling period did not show any significant patterns (Pearson’s Chi-square=0.230, df=2, p=0.89).

The mean numbers of species of larval and juvenile fishes collected per haul across all sampling periods for each ICOLL were similar. Means were determined by the hauls that caught fishes, Cockrone Lagoon ( =1.2±0.1, n=16) with 11 hauls where no fishes were caught, Avoca Lagoon ( =1.6±0.2, n=19) with 13 hauls where no fishes were caught, Terrigal Lagoon ( =1.7±0.2, n=12) with 21 hauls where no fishes were caught and Wamberal Lagoon ( =1.2±0.2, n=21) with 10 hauls where no fishes were caught. Significant temporal variation in the number of species collected occurred only at Terrigal and Wamberal lagoons (Table 4.6). Mean numbers of species were greatest during April 2006, January and March 2007 for Terrigal Lagoon and November 2006 for Wamberal Lagoon, although significant differences in the number of species between November 2006 and January and March 2007 could maybe attributed to chance (Figure 4.9). Post-hoc SNK comparisons of successive samples across all ICOLLs show openings were followed by either a significant increase or decrease in the mean number of species of larval and juvenile fishes (Table 4.7). The magnitude of change in the mean number of species was dependent on the status of the ICOLL entrance during the sampling period (Pearson’s Chi-square=7.27, df=2, p=0.03).

Table 4.4. Summary of one-factor ANOVAs testing for temporal variation in total abundance of larval and juvenile fishes collected from four ICOLLs between April 2006 and March 2007. Cockrone Lagoon Avoca Lagoon Terrigal Lagoon Wamberal Lagoon ln(x+1) transformed ln(x+1) transformed untransformed ln(x+1) transformed Cochrans C=0.42, p<0.05 Cochrans C=0.40, p<0.05 Cochrans C=0.85, p<0.01 Cochrans C=0.25, p<0.05 Source of variation df MS F p df MS F p df MS F p df MS F p Time 6 11.51 14.15 <0.01 7 8.26 4.82 <0.01 8 159.99 3.47 <0.01 7 13.22 4.39 <0.01 Residual 21 0.81 24 1.71 27 46.11 24 3.01

Chapter 4: Effects of barrier openings on larval and juvenile fishes

Cockrone Lagoon Avoca Lagoon

6 5 B 5 B 4 B

4 3 3 A 2 2

Mean number number Mean of fish A 1 A A A 1 A A A 0 A 20/4/06 1/6/06 15/6/06 16/8/06 29/9/06 27/11/06 29/1/07 13/3/07 0 19/4/06 19/6/06 2/8/06 19/9/06 13/11/06 28/1/07 12/3/07 Wamberal Lagoon

Terrigal Lagoon 7 B 25 B 6

20 B 5

4 15 A 3 A A A 10

Mean number number Mean of fish 2 A 5 1 A A A A A A A A 0 0 21/4/06 4/6/06 14/6/06 11/7/06 3/8/06 21/9/06 29/11/06 13/1/07 28/3/07 23/4/06 18/6/06 25/6/06 18/8/06 2/10/06 12/11/06 12/1/07 28/3/07 Sampling period Sampling dates Figure 4.8. Mean total number (± se) of larval and juvenile fishes collected at ICOLLs from April 2006 to March 2007. Mean values with the same letter are not significantly different. The dotted vertical lines indicate a single barrier opening occurred between sampling periods.

101

Table 4.6. Summary of one-factor ANOVAs testing for temporal variation in number of species of larval and juvenile fishes collected from four ICOLLs between April 2006 and March 2007. Cockrone Lagoon Avoca Lagoon Terrigal Lagoon Wamberal Lagoon ln(x+1) transformed untransformed untransformed untransformed Cochrans C=0.45, p<0.05 Cochrans C=0.30, p<0.01 Cochrans C=0.68, p<0.01 Cochrans C=0.38, p<0.01 Source of variation df MS F p df MS F p df MS F p df MS F p Time 6 0.33 2.41 0.06 7 1.24 1.34 0.27 8 2.49 9.59 <0.01 7 6.14 20.32 <0.01 Residual 21 0.14 24 0.93 27 0.26 24 0.30

Chapter 4: Effects of barrier openings on larval and juvenile fishes

Cockrone Lagoon Avoca Lagoon

1 3

0.5

1 Mean number of species of number Mean

0 0 19/4/06 19/6/06 2/8/06 19/9/06 13/11/06 28/1/07 12/3/07 20/4/06 1/6/06 15/6/06 16/8/06 29/9/06 27/11/06 29/1/07 13/3/07

Terrigal Lagoon Wamberal Lagoon 3 5

B C 4 B 2

B 3

2 B

1 Mean number number Mean of species A 1 A

A A A A A A 0 0 23/4/06 18/6/06 25/6/06 18/8/06 2/10/06 12/11/06 12/1/07 28/3/07 21/4/06 4/6/06 14/6/06 11/7/06 3/8/06 21/9/0629/11/0613/1/07 28/3/07 Sampling period Sampling dates Figure 4.9. Mean number of species (± se) of larval and juvenile fishes collected at ICOLLs from April 2006 to March 2007. Mean values with the same letter are not significantly different. The dotted vertical lines indicate a single barrier opening occurred between sampling periods.

The dominant species collected at each ICOLL differed, except for Avoca and Wamberal Lagoons, which were both dominated by Philypnodon grandiceps, with Acanthopagrus australis dominant at Cockrone Lagoon and Ambassis jacksoniensis dominant at Terrigal Lagoon. Atherinosoma microstoma was also collected in high numbers from Wamberal Lagoon. Significant temporal variation in the total number of dominant species occurred at Cockrone and Terrigal Lagoons, but not at Avoca or Wamberal lagoons (Table 4.8). Mean abundances of the dominant species of A. australis were greatest in November 2006 at Cockrone Lagoon which could be the result of a recruitment pulse occurring after the only barrier opening. For P. grandiceps mean abundances at Wamberal Lagoon also peaked during November 2006, with A. jacksoniensis mean abundances greatest during April 2006 at Terrigal Lagoon, after which

103 Chapter 4: Effects of barrier openings on larval and juvenile fishes

abundances were extremely low, which is possibly due to this species departing the ICOLL after the first barrier opening (Figure 4.10). Post-hoc SNK comparisons of successive samples across all ICOLLs show openings were not followed by either a significant increase or decrease in the mean total abundance of larval and juvenile fishes (Table 4.9). The magnitude of change in the mean abundance of dominant species was independent of the status of the ICOLL entrance during the sampling period (Pearson’s Chi-square=5.20, df=2, p=0.07).

104

Table 4.8. Summary of one-factor ANOVAs testing for temporal variation in numbers of larvae and juveniles of the dominant species in each ICOLL between April 2006 and March 2007. Cockrone Lagoon Avoca Lagoon Terrigal Lagoon Wamberal Lagoon Wamberal Lagoon Acanthopagrus australis Philypnodon grandiceps Ambassis jacksoniensis Atherinosoma microstoma Philypnodon grandiceps untransformed untransformed untransformed untransformed ln(x+1) transformed Cochrans C=1.0, p<0.01 Cochrans C=0.30, p<0.01 Cochrans C=0.68, p<0.01 Cochrans C=0.38, p<0.01 Cochrans C=0.41,p<0.05 Source of variation df MS F p df MS F p df MS F p df MS F p df MS F p Time 6 13706.75 16.63 <0.01 7 1348.49 2.04 0.09 8 86.00 10.75 <0.01 7 1672.60 2.14 0.08 7 9.15 2.78 0.03 Residual 21 824.23 24 661.47 27 8.00 24 780.97 24 3.30

Chapter 4: Effects of barrier openings on larval and juvenile fishes

Cockrone Lagoon Avoca Lagoon Acanthopagrus australis Philypnodon grandiceps 70 250 60 B 200 50

150 40

30 100 20

Mean abundance of fish of abundance Mean 50 10

A A A A A A 0 0 20/4/06 1/6/06 15/6/06 16/8/06 29/9/06 27/11/06 29/1/07 13/3/07 19/4/06 19/6/06 2/8/06 19/9/06 13/11/06 28/1/07 12/3/07

Terrigal Lagoon Wamberal Lagoon Ambassis jacksoniensis Atherinosoma microstoma 20 90 B 18 80 16 70 14 60 12 50 10 40 8

Mean number of fish of number Mean 30 6 4 20

2 A 10 A A A A 0 A A A 0 21/4/06 4/6/06 14/6/06 11/7/06 3/8/06 21/9/0629/11/0613/1/07 28/3/07 23/4/06 18/6/06 25/6/06 18/8/06 2/10/06 12/11/06 12/1/07 28/3/07

Wamberal Lagoon Philypnodon grandiceps 6

B 5

A Mean abundance of fish of abundance Mean 1 A 0 23/4/06 18/6/06 25/6/06 18/8/06 2/10/06 12/11/06 12/1/07 28/3/07 Sampling dates

106 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Temporal variations in assemblages of larval and juvenile fishes in ICOLLs were compared using cluster analysis (Figure 4.11). In most cases, two distinct groups occurred below the 50% level, with no distinct differences in assemblages of larval and juvenile fishes occurring from before to after barrier openings. Higher groupings above the 50% level generally coincided with peak abundances of the dominant species found within each ICOLL, except for Cockrone Lagoon which in most cases had low abundances, except during November 2006. In Avoca Lagoon, the similarity in assemblages in November 2006 and January 2007 coincided with the increase in abundances of the dominant species, Philypnodon grandiceps. In Terrigal Lagoon, the similarity in assemblages in April 2006 coincided with the increase in abundances of the dominant species, Ambassis jacksoniensis and in March 2007, which resulted from an increase in abundances of other species. In Wamberal Lagoon, the similarity in assemblages in April 2006 coincided with the increase in abundances of P. grandiceps and in November 2006, coincided with peak abundances of Atherinosoma microstoma (Figure 4.10).

Similarities (ANOSIM) tests were used to compare the larval and juvenile fish assemblages of ICOLLs between successive sampling periods and before and after barrier openings (Table 4.10). Global R-statistic values for assemblages were similar for Cockrone and Avoca Lagoons, while Wamberal Lagoon had the smallest Global R, and Terrigal Lagoon had the greatest Global R. Differences in Global R values indicate distinct differences in assemblages between ICOLLs (Table 4.10).

In general, pair-wise ANOSIM comparisons showed that no significant changes in assemblages of larval and juvenile fishes of ICOLLs occurred from before to after barriers were opened. However, sampling periods 1 and 2 (April and June 2006) at Cockrone Lagoon showed significant variations as did sampling periods 4 and 5 (August and September 2006) at Avoca Lagoon, which occurred during a barrier opening (Table 4.10). Table 4.11 shows the variations in larval and juvenile fish assemblages between the closed and open barrier phases; however, variations in assemblages were not influenced by barrier openings as there was no significant difference in assemblages (Pearson’s Chi-square=0.09, df=1, p=0.76). However, there is a suggestion of temporal patterns in larval and juvenile fish assemblages in ICOLLs (Table 4.10).

107 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Cockrone Lagoon 2 Aug-06 19 Jun-06 28 Jan-07 19 Apr-06 13 Nov-06 19 Sep-06^ 0 20 40 60 80 100 % Similarity

Avoca Lagoon 29 Jan-07 27 Nov-06 1 Jun-06 20 Apr-06 15 Jun-06^ 29 Sep-06^ 16 Aug-06 0 20 40 60 80 100 % Similarity Terrigal Lagoon 28 Mar-07^

21 Apr-06

13 Jan-07^

29 Nov-06

0 20 40 60 80 100 % Similarity

Wamberal Lagoon 12 Nov-06 23 Apr-06 18 Aug-06 25 Jun-06^ 12 Jan-07 18 Jun-06 28 Mar-07 0 20 40 60 80 100 % Similarity Figure 4.11. Dendrograms showing similarity of assemblages of larval and juvenile fishes collected at different sampling times at ICOLLs. Sampling periods occurred bimonthly unless barriers had opened, in which case a sampling period occurred before and after the barrier opening. Sampling periods where no fish were collected were not included in the analysis. ^indicates first sampling period after ICOLLs were opened. The division line is shown at the 50% level.

108 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Table 4.10. Summary of pair-wise ANOSIM tests comparing larval and juvenile fish assemblages of ICOLLs between successive sampling periods from April 2006 to March 2007 (→ denotes period during which ICOLL was opened). Monthly samples where no fish were collected are not included in the analysis. The values shown are pairwise R-values and their significance levels. Significant values are in italics. Sample Cockrone Sample Avoca Sample Terrigal Sample Wamberal 1-2 0.01 1-2 0.18 1-7→ 0.67 1-2 -0.06 (p>0.05) (p>0.05) (p=0.03) (p>0.05) 2-3 -0.14 2-3→ -0.17 7-8 0.67 2-3→ -0.14 (p>0.05) (p>0.05) (p=0.03) (p>0.05) 3-4→ 0.27 3-4 -0.05 8-9→ 0.73 3-4 -0.08 (p>0.05) (p>0.05) (p=0.03) (p>0.05) 4-5 0.64 4-5→ 0.04 4-6→ 0.54 (p=0.03) (p>0.05) (p=0.03) 5-6 0.50 5-6 0.57 6-7 0.98 (p=0.03) (p=0.03) (p=0.03) 6-7 0.33 6-7 0.19 7-8 0.5 (p>0.05) (p>0.05) (p=0.03) Global R 0.30 0.30 0.63 0.19 p 0.001 0.003 0.001 0.01

Species that contributed up to 90% of the dissimilarity of the significant ANOSIM pair-wise tests were analysed using SIMPER. At Cockrone Lagoon dissimilarity of larval and juvenile fish assemblages were found between sampling periods 1 and 2 (Table 4.10). The most frequent causes of assemblage dissimilarity between the two times were differences in the abundance of Atherinosoma microstoma. At Avoca Lagoon, differences in abundances of Mugil cephalus and A. microstoma were the most frequent causes of assemblage dissimilarity between sampling times 4 and 5.

109 Chapter 4: Effects of barrier openings on larval and juvenile fishes

4.3.4 Larval and juvenile fishes of adjacent surf zones A total of 598 fishes belonging to 16 species (14 families) were collected from surf zones between April 2006 and March 2007 (Table 4.12). Clupeidae was the most abundant family collected from surf zones (n=514). The greatest total number of fishes was recorded from Terrigal Beach (n=388) and the smallest number of fishes was recorded from Copacabana Beach (n=19). The most abundant species collected from surf zones was Hyperlophus vittatus (n=492). Copacabana Beach (7 families, 7 species) was characterised by an M species the surfsardine Iso rhothophilus (Isonidae) (n=10). Avoca Beach (11 families, 13 species) was characterised by an EM species the sandy sprat H. vittatus (Clupeidae) (n=129). Terrigal Beach (8 families, 10 species) was also characterised by H. vittatus (n=345), as was Wamberal Beach (5 families, 5 species) (n=17) (Table 4.12). Six families (Ambassidae, Atherinidae, Eleotridae, Gobiidae, Mugilidae and Sparidae) were collected from both ICOLLs and surf zone sites, however the number of fishes in each sample collected from the surf zones for each family was considerably less than collected from ICOLLs.

4.3.5 Temporal variation in assemblages of larval and juvenile fishes of adjacent surf zones Average total abundances of larval and juvenile fishes in surf zones were generally low, with patchy distribution amongst all sites. The mean number of larval and juvenile fishes collected per haul across all sampling periods for each surf zone varied, Copacabana Beach ( =0.3±0.1, n=72), Avoca Beach ( =1.7±1.0, n=96), Terrigal Beach ( =3.4±0.8, n=118) and Wamberal Lagoon ( =0.3±0.1, n=28). Significant temporal variations in total abundances of larval and juvenile fishes were found only at Terrigal Beach (Table 4.13). Mean abundances at Terrigal Beach were greatest during early June and July 2006 and March 2007 (Figure 4.12). Post-hoc SNK comparisons of successive samples across all surf zones showed ICOLL barrier openings were not followed by either a significant increase or decrease in the mean total abundance of larval and juvenile fishes (Table 4.14). The magnitude of change in the mean total abundance was independent of the status of the barrier during the sampling period (Pearson’s Chi- square=0.87, df=2, p=0.64).

110

Table 4.12. Total number of larval and juvenile fishes collected in adjacent surf zones from April 2006 to March 2007. Surf zone sampled ~100 m south of ICOLL entrance, adjacent to ICOLL entrance and ~100 m north of ICOLL entrance. Also shown are the life history categories (F=Freshwater, R=Resident, MED=Marine–estuary dependant, EM=Estuarine and marine, T=Transient and M=Marine species), and range in total length (TL). Family Species Life Surf zone TL Total history (mm) number Copacabana Avoca Terrigal Wamberal North Adjacent South North Adjacent South North Adjacent South North Adjacent South Ambassidae Ambassis jacksoniensis EM 0 0 0 0 0 0 6 0 0 0 0 0 15-19 6 Ambassis marianus EM 0 0 0 0 0 0 0 0 1 0 0 0 12 1 Atherinidae Atherinosoma microstoma R 0 0 0 0 0 2 0 0 0 0 0 0 14-15 2 Clupeidae Hyperlophus vittatus EM 1 0 0 8 10 111 86 147 112 0 1 16 12-40 492 Sardinops sagax M 0 0 0 1 0 1 2 10 8 0 0 0 23-35 22 Congridae Unidentified species M 1 0 0 0 0 0 0 0 0 0 0 0 96 1 Eleotridae Philypnodon grandiceps R 0 0 0 0 0 3 0 0 0 0 0 7 11-23 10 Unidentified species R 0 0 2 0 0 0 0 0 0 0 0 0 10-12 2 Gerreidae Gerres subfasciatus EM 0 0 0 3 2 0 0 0 1 0 1 0 7-18 7 Girellidae Girella tricuspidata T 0 0 0 2 0 3 0 0 2 0 0 0 10-12 7 Gobiidae Gobiopterus semivestitus R 0 0 0 0 0 0 0 0 1 0 0 0 9 1 Pseudogobus olorum R 0 0 0 0 0 2 0 0 0 0 0 0 12-14 2 Isonidae Iso rhothophilus M 4 3 3 0 0 0 0 0 0 0 0 0 19-27 10 Leptoscopidae Lesueurina platycephala M 0 0 0 0 0 1 1 3 6 0 0 1 16-21 12 Lutjanidae Unidentified species M 0 0 0 1 1 0 0 0 0 0 0 0 8 2 Mugilidae Mugil cephalus MED 0 0 0 0 1 0 1 0 0 0 0 0 22-23 2 Myxus elongatus MED 0 0 1 4 1 4 0 0 0 0 1 1 11-14 12 Paralichthyidae Pseudorhombus sp. EM 1 0 0 1 0 0 0 0 0 0 0 0 6-11 2 Sparidae Acanthopagrus australis MED 0 0 3 1 0 0 0 1 0 0 0 0 10-14 5 Total number 7 3 9 21 15 127 96 161 131 0 3 25 598

Table 4.13. Summary of results of one-factor ANOVA testing for temporal variation in total abundance of larval and juvenile fishes collected from four surf zones between April 2006 and March 2007. Copacabana Beach Avoca Beach Terrigal Beach Wamberal Beach untransformed untransformed ln(x+1) transformed untransformed Cochrans C=0.63, p<0.01 Cochrans C=0.98, p<0.01 Cochrans C=0.23, p<0.05 Cochrans C=0.40, p<0.01 Source of variation df MS F p df MS F p df MS F p df MS F p Time 5 1.05 1.70 0.15 7 99.92 1.02 0.43 8 9.05 18.01 <0.01 6 1.86 1.29 0.27 Residual 66 0.62 88 98.42 99 0.50 77 1.45

Chapter 4: Effects of barrier openings on larval and juvenile fishes

Copacabana Beach Avoca Beach 2 18 16 14 12 10 1 8

6 Mean number of fish of number Mean 4 2 0 0 20/4/06 1/6/06 15/6/06 18/6/06 29/9/06 27/11/06 29/1/07 13/3/07 19/4/06 19/6/06 2/8/06 19/9/06 13/11/06 28/1/07

Terrigal Beach Wamberal Beach 3 C 2

B 2

1 A 1 Mean number number Mean of fish A A A A A A 0 0 21/4/06 4/6/06 14/6/06 11/7/06 3/8/06 21/9/06 29/11/06 13/1/07 28/3/07 23/4/06 18/6/06 25/6/06 18/8/06 2/10/06 12/11/06 12/1/07 Sampling dates Sampling dates Figure 4.12. Mean abundance (± se) of larval and juvenile fishes collected at all surf zones from April 2006 to March 2007. Mean values with the same letter are not significantly different. The dotted vertical lines indicate a single barrier opening occurred between sampling periods.

The mean numbers of species of larval and juvenile fishes collected per haul across all sampling periods for each surf zone were similar. Means were determined by the hauls that caught fishes, Copacabana Beach ( =1.1±0.1, n=10) with 62 hauls where no fishes were caught, Avoca Lagoon ( =1.2±0.1, n=33) with 62 hauls where no fishes were caught, Terrigal Lagoon ( =1.3±0.1, n=42) with 65 hauls where no fishes were caught and Wamberal Lagoon ( =1.0±0.0, n=10) with 74 hauls where no fishes were caught. Significant temporal variations were found for the number of species at Avoca, Terrigal and Wamberal Beaches (Table 4.15). Mean numbers of species were greatest during June 2006 at Avoca Beach, June and July 2006 and March 2007 at Terrigal Beach and, November 2006 at Wamberal Beach (Figure 4.13). Post-hoc SNK comparisons of successive samples across all surf zones showed openings were

113 Chapter 4: Effects of barrier openings on larval and juvenile fishes

not followed by either a significant increase or decrease in the mean number of species of larval and juvenile fishes (Table 4.16). The magnitude of change in the mean number of species was independent of the status of the barrier during the sampling period (Pearson’s Chi-square=1.11, df=2, p=0.57).

114

Table 4.15. Summary of results of one-factor ANOVA testing for temporal variation in number of species of larval and juvenile fishes collected from four surf zones between April 2006 and March 2007. Copacabana Beach Avoca Beach Terrigal Beach Wamberal Beach untransformed ln(x+1) transformed untransformed untransformed Cochrans C=0.49, p<0.01 Cochrans C=0.22, p<0.05 Cochrans C=0.41, p<0.01 Cochrans C=0.41, p<0.01 Source of variation df MS F p df MS F p df MS F p df MS F p Time 5 0.25 1.62 0.17 7 0.32 2.40 0.03 8 2.77 6.43 <0.01 6 0.27 2.94 0.01 Residual 66 0.15 88 0.13 99 0.43 77 0.09

Chapter 4: Effects of barrier openings on larval and juvenile fishes

Copacabana Beach Avoca Beach 1 1

0.5 0.5 Mean number of species of number Mean

0 A 0 19/4/06 19/6/06 2/8/06 19/9/06 13/11/06 28/1/07 20/4/06 1/6/06 15/6/06 16/8/06 29/9/06 27/11/06 29/1/07 13/3/07

Terrigal Beach Wamberal Beach 1 2

B B B 0.5 1

A A A Mean number of species of number Mean A A A A A 0 0 23/4/06 18/6/06 25/6/06 18/8/06 2/10/06 12/11/06 12/1/07 21/4/06 4/6/06 14/6/06 11/7/06 3/8/06 21/9/0629/11/0613/1/07 28/3/07 Sampling dates Sampling dates Figure 4.13. Mean number of species (± se) of larval and juvenile fishes collected at all surf zones from April 2006 to March 2007. Mean values with the same letter are not significantly different. The dotted vertical lines indicate a single barrier opening occurred between sampling periods.

Significant variations through time were tested for the dominant species collected at each surf zone; Iso rhothophilus (Copacabana Beach) and Hyperlophus vittatus (Avoca, Terrigal and Wamberal Beaches). Terrigal Beach was the only surf zone to show significant temporal variation in the abundance of a single species, H. vittatus (Table 4.17), which was most abundant during early June 2006 (Figure 4.14). Post-hoc SNK comparisons of successive samples across all surf zones showed openings were not followed by either a significant increase or decrease in the mean abundance of the dominant species (Table 4.18). The

116 Chapter 4: Effects of barrier openings on larval and juvenile fishes

magnitude of change in the mean abundance of dominant species was independent of the status of the barrier during the sampling period (Pearson’s Chi-square=3.56, df=2, p=0.17).

117

Table 4.17. Summary of results of one-factor ANOVA testing for temporal variation in dominant species of larval and juvenile fishes collected from four surf zones between April 2006 and March 2007. Copacabana Beach Avoca Beach Terrigal Beach Wamberal Beach Iso rhothophilus Hyperlophus vittatus Hyperlophus vittatus Hyperlophus vittatus untransformed untransformed untransformed untransformed Cochrans C=0.67, p<0.01 Cochrans C=0.99, p<0.01 Cochrans C=0.84, p<0.01 Cochrans C=0.50, p<0.01 Source of variation df MS F p df MS F p df MS F p df MS F p Time 5 0.69 1.81 0.12 7 94.44 0.96 0.47 8 466.27 9.78 <0.01 6 1.25 1.41 0.22 Residual 66 0.38 88 98.76 99 47.68 77 0.88

Chapter 4: Effects of barrier openings on larval and juvenile fishes

Copacabana Beach Avoca Beach Iso rhothophilus Hyperlophus vittatus 1 14

8 0.5 6

Mean number of fish of number Mean 4

0 0 19/4/06 19/6/06 2/8/06 19/9/06 13/11/06 28/1/07 20/4/06 1/6/06 15/6/06 18/6/06 29/9/06 27/11/06 29/1/07 13/3/07

Terrigal Beach Wamberal Beach Hyperlophus vittatus Hyperlophus vittatus 30 2

25 B

15 1

10 fish of number Mean Mean abundance abundance fish of Mean

A A A A A A A 0 0 21/4/06 4/6/06 14/6/06 11/7/06 3/8/06 21/9/06 29/11/06 13/1/07 28/3/07 23/4/06 18/6/06 25/6/06 18/8/06 2/10/06 12/11/06 12/1/07 Sampling dates Sampling dates Figure 4.14. Mean abundance (± se) of the dominant species of larval and juvenile fishes at all surf zones from April 2006 to March 2007. Mean values with the same letter are not significantly different. The dotted vertical lines indicate a single barrier opening occurred between sampling periods.

Temporal variations in assemblages of larval and juvenile fishes in surf zones were visualized using cluster analysis (Figure 4.15). In most cases, two distinct groups of assemblages occurred below the 50% level in surf zones, with no apparent change in assemblage structure occurring from before to after barrier openings. Unlike ICOLL abundances, higher groupings above the 50% level did not coincide with peak abundances of the dominant species; instead they represent the patchy distribution of larval and juvenile fishes occurring in these surf zones.

119 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Copacabana Beach 2 Aug-06

19 Jun-06

28 Jan-07

13 Nov-06

19 Sep-06^

0 20 40 60 80 100 Avoca Beach 29 Jan-07 27 Nov-06 19 Sep-06^ 20 Apr-06 15 Jun-06^ 13 Mar-07 16 Aug-06 0 20 40 60 80 100 Terrigal Beach 28 Mar-07^ 13 Jan-07^ 3 Aug-06^ 14 Jun-06^ 11 Jul-06^ 4 Jun-06 21 Sep-06^ 21 Apr-06 0 20 40 60 80 100 Wamberal Beach 12 Jan-07

18 Aug-06

12 Nov-06

25 Jun-06^

0 20 40 60 80 100 % Similarity Figure 4.15. Dendrogram showing similarity of assemblages of larval and juvenile fishes collected at different sampling times at surf zones. Sampling periods occurred bimonthly unless barriers had opened, in which case a sampling period occurred before and after the barrier opening. Sampling periods where no fish were collected were not included in the analysis. ^indicates first sampling period after barriers were opened. The division line is shown at the 50% level.

ANOSIM tests were used to test for differences in the larval and juvenile fish assemblages of surf zones between successive sampling periods and before and after barrier openings (Table 4.19). Global R-statistic values for assemblages differed significantly between surf zones

120 Chapter 4: Effects of barrier openings on larval and juvenile fishes

indicating distinct differences in assemblages, especially at Terrigal Beach. Pair-wise ANOSIM comparisons showed significant variations in assemblages occurred from before to after barriers were opened, and also occurred between sampling periods when there were no openings. Significant variations occurred for most sampling periods in all surf zones regardless of whether barriers had been opened or not. Terrigal Beach was the exception as only two periods showed any significant differences (Table 4.19).

Species that contributed up to 90% of the dissimilarity of the significant ANOSIM pair-wise tests were analysed using SIMPER. At Copacabana Beach dissimilarity of larval and juvenile fish assemblages was found between sampling periods 2-3, 3-4, 4-5 and 5-6. The most frequent causes of assemblage dissimilarity between times 2-3 and 3-4 was differences in the abundance of Iso rthothophilus, with differences in abundance of Acanthopagrus australis the cause of changes at times 4-5 and 5-6. The most frequent cause of assemblage dissimilarity between sampling periods 1-3 and 5-6 at Avoca Beach was differences in the abundance of Hyperlophus vittatus. Although significant pair wise tests were evident for times 6-7 and 7-8 at Avoca Beach, no species fitted the criteria described above for the SIMPER analysis. At Terrigal Beach dissimilarity of larval and juvenile fish assemblages was found for sampling periods 8-9, and was caused by changes in abundance of H. vittatus. Philypnodon grandiceps was the most frequent cause of assemblage dissimilarity between sampling periods 3-4 at Wamberal beach, however, no species fitted the criteria described above for the SIMPER analysis at sampling times 4-6 and 6-7 at Wamberal Beach.

121 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Table 4.19. Summary of pair-wise ANOSIM tests comparing larval and juvenile fish assemblages of surf zones between successive sampling periods from April 2006 to March 2007 (→ denotes period during which ICOLL was opened). Absence of a test value for some surf zones for some sampling period occurs because sampling did not occur due to poor weather or no fish were collected. The values shown are pairwise R-values and their significance levels. Significant values are in italics. Sample Copacabana Sample Avoca Sample Terrigal Sample Wamberal 2-3 0.01 1-3→ 0.04 1-2 0.86 3-4 -0.03 (p>0.05) (p>0.05) (p=0.001) (p>0.05) 3-4→ <0.001 3-4 0.14 2-3→ 0.54 4-6→ 0.004 (p>0.05) (p=0.01) (p=0.001) (p>0.05) 4-5 0.03 4-5→ 0.05 3-4→ 0.31 6-7 0.04 (p>0.05) (p>0.05) (p=0.001) (p>0.05) 5-6 0.02 5-6 -0.03 4-5→ 0.46 (p>0.05) (p>0.05) (p=0.001) 6-7 -0.01 5-6→ 0.05 (p>0.05) (p>0.05) 7-8 0.01 6-8 0.07 (p>0.05) (p>0.05) 8-9→ 0.01 (p>0.05) Global R 0.03 0.02 0.28 0.01 p 0.02 0.09 0.001 0.21

4.3.6 Effects of barrier openings on larval and juvenile fish assemblages Jaccard’s coefficient values range from 0 to 1, where a 0 value indicates no species in common between the two sites while a value of 1 indicates the same species occurred at both sites (Gibson et al. 1993; Harrison and Whitfield 1995). There was little/no variation in the Jaccard’s coefficient from before to after openings for Cockrone Lagoon/Copacabana Beach and Wamberal Lagoon/Wamberal Beach (Table 4.20). Fish assemblages were less similar after the lagoon opening at Avoca and more similar at Terrigal. Across all lagoons, there was no significant change in average Jaccard’s coefficient from before ( =0.42±0.15) to after ( =0.52±0.02) lagoon openings (t=-0.66, p=0.56).

122 Chapter 4: Effects of barrier openings on larval and juvenile fishes

Table 4.20. Jaccard’s coefficient of similarity for larval and juvenile fish assemblages between ICOLLs and surf zones before and after opening events. Jaccard’s coefficient Habitats compared Before After Cockrone Lagoon/Copacabana Beach 0.5 0.6 Avoca Lagoon/Avoca Beach 0.7 0.5 Terrigal Lagoon/ Terrigal Beach 0 0.5 Wamberal Lagoon/ Wamberal Beach 0.5 0.5

4.3.7 Length-frequency distributions of larval and juvenile fishes Kolmogorov-Smirnov (K-S) tests were not performed on larval and juvenile fishes collected in Cockrone and Terrigal Lagoons. Comparisons could not be made due to the possible recruitment of Acanthopagrus australis occurring in Cockrone Lagoon after the only barrier opening (Figure 4.16a), whereas, low numbers of Ambassis jacksoniensis were collected after the barrier opening at Terrigal Lagoon (Figure 4.16c). Kolmogorov-Smirnov (K-S) tests were performed for Philypnodon grandiceps collected at Avoca and Wamberal Lagoons and for Atherinosoma microstoma in Wamberal Lagoon as these species were caught in greater numbers before and after openings. The length-frequency distribution of P. grandiceps did not differ significantly from before to after Avoca Lagoon was opened (KS=0.11, p=0.11), which appears to be due to similar percentage range of fishes in most of the length classes (Figure 4.16b). The mean total length did not change from before ( =18.07±0.19, n=149) to after ( =17.83±0.15, n=359) when Avoca Lagoon was opened (t=1.02, p=0.31).

The length-frequency distribution of Philypnodon grandiceps differed significantly from before to after Wamberal Lagoon was opened (KS=0.69, p=<0.001), which appeared to be due to a reduced percentage of fishes in the 16 and 18 mm length classes, and an increased percentage of fishes in the 20 and 22 mm length classes (Figure 4.16d). The mean total length did change from before ( =16.65±0.06, n=624) to after ( =19.68±0.11, n=236) Wamberal Lagoon was opened (t=24.2, p=<0.01). These changes are possibly due to growth of P. grandiceps found in this ICOLL before the barrier was opened. The length-frequency distribution of Atherinosoma microstoma differed significantly from before to after Wamberal Lagoon was opened (KS=0.14, p=0.04), which appeared to be due to a reduced percentage of fishes in the 16 and 18 mm length classes, and an increased percentage of fishes in the 12, 14, 20 and 22 mm length classes (Figure 4.16e). The mean total length did not change from before ( =16.19±0.17, n=134) to after ( =15.89±0.17, n=265) Wamberal Lagoon was opened (t=1.29, p=0.20). K-S tests were not performed on species collected in surf zones as these species were not found in ICOLLs,

123 Chapter 4: Effects of barrier openings on larval and juvenile fishes

therefore it was determined that openings may not effect these species (Figure 4.17). However, the majority of Iso rhothophilus collected from Copacabana Beach had a total length of 25 mm, with the total length of Hyperlophus vittatus varying between 20-25 mm at Avoca Beach, 20-30 mm at Terrigal Beach and 15-25 mm at Wamberal Beach (Figure 4.17).

(a) Acanthopagrus australis (b) Philypnodon grandiceps after n=623 before n=149 after n=359 35 60 30 50 25 40 20 30

15 % frequency % 20 10

10 5

0 0 8 10 12 14 16 18 20 12 14 16 18 20 22 24

100 50 90 45 80 40 70 35 60 30 50 25

% frequency % 40 20 30 15 20 10 10 5 0 0 12 14 16 18 20 22 24 12 14 16 18 20 22 24 26 28

(e) Atherinosoma microstoma before n=134 after n=265

50 45 40 35 30 25 20

% frequency % 15 10 5 0 10 12 14 16 18 20 22 24 Total length (mm)

124 Chapter 4: Effects of barrier openings on larval and juvenile fishes

(a) Iso rhothophilus (b) Hyperlophus vittatus n=10 n=129 70 60

60 50 50 40 40 30 30

% Frequency % 20 20

10 10

0 0 5 10 15 20 25 30 35 5 10 15 20 25 30 35

(c) Hyperlophus vittatus (d) Hyperlophus vittatus n=345 n=17 40 40 35 35 30 30 25 25 20 20 15 15 % Frequency % 10 10 5 5 0 5 10 15 20 25 30 35 40 0 5 10 15 20 25 30 35 Total length (mm) Total length (mm)

Figure 4.17. Length-frequency distributions of the most abundant species collected from surf zones near each ICOLL. (a) Copacabana Beach, (b) Avoca Beach, (c) Terrigal Beach, (d) Wamberal Beach.

4.4. Discussion

4.4.1 Effects of barrier openings on larval and juvenile fish assemblages of ICOLLs and adjacent surf zones Surf zones and ICOLLs in the Central Coast region have vastly different abundances and species richness of larval and juvenile fishes. Total abundances were generally greater in ICOLLs during the summer months and greater in surf zones during the winter months. However, in both environments the total abundances of larval and juvenile fishes were dominated by only a few species. The dominant species at Cockrone and Terrigal Lagoons differed from those at Avoca and Wamberal Lagoons. Acanthopagrus australis and Ambassis jacksoniensis were the dominant species in Cockrone and Terrigal Lagoons, respectively. Philypnodon grandiceps and Atherinosoma microstoma were the dominant species in both Avoca and Wamberal Lagoons. The dominant species within these ICOLLs, as in most other temperate ICOLLs, were shown to have their highest abundances once during the year. Such

125 Chapter 4: Effects of barrier openings on larval and juvenile fishes

abundances are known to coincide with spawning activities and/or increasing water temperatures (Roper 1986; Neira and Potter 1994).

Similarly, larval and juvenile fishes in adjacent surf zones were dominated by a single species, typically Hyperlophus vittatus. Generally the abundance of H. vittatus peaked during the summer months (Strydom 2003), with a second peak occurring during the winter months (Senta and Kinoshita 1985; Harris and Cyrus 1996). Overall, fish abundances in the surf zone sites in the current study were generally low, with the exception of Terrigal Beach. These low patchy abundances can be due to factors associated with surf zone characteristics such as wind, coastal currents, lunar cycles (Kingsford and Finn 1997; Trnski 2001), tidal cycles, and type of habitat (Watt-Pringle and Strydom 2003). Low numbers can also be attributed to the sampling regime, as bimonthly sampling does not take into account those species of larval and juvenile fishes that may occur between sampling periods. Therefore, it does not give a true indication of any seasonal variations that may occur.

In most cases, barriers were closed, with the exception of the barrier at Terrigal Lagoon which was opened much more frequently than in the other ICOLLs. However, when barriers are closed it has been suggested by Cowley et al. (2001) and Strydom (2003) that larval and juvenile fishes can still react to chemical cues from water seepage through the barrier. Hence many fishes aggregate near the entrances of ICOLLs waiting to enter once the barrier has been breached. This was in contrast to what was found in the current study, as abundances of larval and juvenile fishes tended to be greater at the southern ends of the adjacent surf zones, away from the lagoon entrances. These differences can possibly be related to the factors described earlier by Kingsford and Finn (1997), Trnski (2001) and Watt-Pringle and Strydom (2003). However another factor not investigated is the effect that ambient shore lights may have on larval and juvenile fishes in surf zones. Hernandez and Shaw (2003) suggested that the ambient lights from an offshore petroleum platform were a factor in attracting larval and juvenile fishes to the platforms. A similar phenomenon may have occurred in the current study, especially at Terrigal and Avoca Beaches, where the southern beach areas are brightly illuminated by urban development’s located close to the beach, which might have had some influence on the increased larval and juvenile fish abundances at these southern sites. Sites at Copacabana and Wamberal Beaches are generally less illuminated, with lower abundances compared to the other two southern surf zones, hence increased abundances at these particular southern sites could be influenced by the factors described earlier.

In general, Central Coast ICOLLs and their adjacent surf zone habitats were found to have low species richness. ICOLLs in most cases have a more stable environment due to the prolonged

126 Chapter 4: Effects of barrier openings on larval and juvenile fishes

closure of their barriers. Most studies of fish assemblages in ICOLLs have found a relatively low species richness (Allan et al. 1985; Young and Potter 2002). The low species richness found in these surf zones, however, is generally uncommon, though species richness can be influenced by spatial and temporal factors similar to those described earlier (Harris and Cyrus 1996).With the exception of Terrigal Lagoon, opening events at the other three ICOLLs generally occurred at similar times throughout the study, and there were no significant differences in Jaccards co-efficient between the two environments, indicating that there was no movement of species between the two habitats. However, the collection of some marine spawning species of larval and juvenile fishes during this study (Table 4.3), indicates that these species may have entered into Central Coast ICOLLs at some stage, possibly at times between the current bimonthly sampling periods. High species richness of larval and juvenile fishes has been documented near the entrances of ICOLLS when barriers have been opened, due to changes in hydrological characteristics causing temporary marine conditions (Griffiths 2001a). Although the barriers of these ICOLLs in the current study had opened when larval and juvenile fish abundances in surf zones tended to be at their peak, there was no evidence to suggest that barrier openings had any effect on these abundances in the surf zones.

Fishes that utilise ICOLLs as nursery areas generally tend to enter at a settlement stage in their life history (Hannan and Williams 1998). Comparison of the total length of larval and juvenile fishes before and after barrier openings can determine if species have moved between the two habitats. Acanthopagrus australis was collected at Cockrone Lagoon after the only barrier opening, with most of these fishes having a total length of 12-14 mm, indicating that individuals of this species were past their normal settlement stage of 8-11 mm TL (Trnski 2002). Generally, sparids have a demersal life style at lengths of 14-15 mm TL (Senta and Kinoshita 1985), which is similar to the size range found in the present study. In comparison, Ambassis jacksoniensis were collected in low numbers from Terrigal Lagoon, with the majority having total lengths of 18-20 mm before barrier openings. In general, total lengths of larval and juvenile fishes in ICOLLs did not change significantly from before to after barrier openings, indicating that they probably remained within these ICOLLs, and that populations of these species were not supplemented with smaller individuals that may have migrated into these ICOLLs from their adjacent surf zones. Surf zone species were predominately postflexion to transformation larvae (Neira et al. 1998), indicating that Hyperlophus vittatus collected may use surf zones as nursery areas (Ayvazian and Hyndes 1995), which is reinforced by the lack of this species being collected from ICOLLs. The other dominant surf zone species, Iso rhothophilus, is generally not known to frequent estuarine environments (Kuiter 2000).

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Sampling regimes and methods also influence detected patterns in spatial variations. The current study was undertaken at night during low tide using a larval beach seine. High abundances generally tend to occur at night (Ruple 1984; Harris and Cyrus 1996) and at low tide (Whitfield 1989; Cowley et al. 2001; Strydom 2003; Geraghty 2004). However, Senta and Kinoshita (1985) found contrasting evidence of increased abundances during the day, with no relationship to tidal phases. Net avoidance by many species was unlikely to occur due to the shallow sampling depths encountered (Roper 1986). Sampling efficiency can be compromised when using such fine mesh nets as they tend to scoop up sediments and vegetation, increasing drag resistance and decreasing the capture of benthic and mobile species (Senta and Kinoshita 1985). The collection of sediments while seining was a common problem encountered during this study, along with wave exposure, which can also increase drag (Romer 1990; Clark 1997).

4.4.2 Comparison of larval and juvenile fish assemblages in ICOLLs and adjacent surf zones The larval and juvenile fishes of the four ICOLLs were generally dominated by different species with differing life histories. Cockrone Lagoon was dominated by a marine-estuarine dependent (MED) species Acanthopagrus australis that spawns between late autumn and winter (Griffiths 2001b; Trnski 2001; Geraghty 2004). Generally, larval and juvenile A. australis recruit into ICOLLs during spring or summer when barriers are more likely to be opened; however, these fishes are unable to enter ICOLLs if their barriers remain closed (Griffiths 1999, 2001b). This was shown at Cockrone Lagoon, with abundances of A. australis increasing after the only barrier opening that occurred, during September 2006. The majority of these fishes were collected in the one sampling period and had a total length range between 9-18 mm, which indicates that they were most probably new recruits to the ICOLL (see Griffiths 2001b). Low numbers (n=3) of A. australis were collected during the following two sampling periods, indicating that these newly recruited fishes had either dispersed throughout the ICOLL, or had suffered mortality. Acanthopagrus australis was not collected in the surf zones during the sampling periods prior to this barrier opening; however, the lack of numbers found in the surf zone could also indicate that this species had moved from surf zones into the ICOLL between sampling periods. Studies by Trnski (2001) have shown that A. australis congregates in estuarine plume fronts, exhibiting entrainment into channels of large barrier estuaries following suitable tidal flow from surf zones. They have also been found to enter ICOLLs during barrier closure via overwash events (Cowley et al. 2001).

Avoca and Wamberal Lagoons had similar dominant fish assemblages but different abundances of each species. Both ICOLLs were dominated by the resident (R) species Phyilypnodon

128 Chapter 4: Effects of barrier openings on larval and juvenile fishes

grandiceps and Atherinosoma microstoma that are characteristic of other NSW ICOLLs (Pollard 1994b; Griffiths 1999; Jones and West 2005). Atherinosoma microstoma is an R species capable of inhabiting waters of high salinity (Molsher et al. 1994). Abundances of both these species peaked during spring to summer months, and this coincides with their spawning periods (Potter et al. 1986; McDowall 1996; Allen et al. 2003). Similar trends were seen in the current study, as abundances of A. microstoma peaked during November, after which abundances decreased dramatically, a similar pattern of A. microstoma studied at Dee Why Lagoon by Potter et al. (1986). Terrigal Lagoon was dominated by an estuarine marine (EM) species, Ambassis jacksoniensis, which peaked in abundance during autumn (March and April) corresponding to peak abundances found by Miskiewicz (1987) at Lake Macquarie, NSW.

In comparison, surf zone larval and juvenile fish assemblages were dominated by an estuarine marine (EM) species Hyperlophus vittatus, which may spawn many times during the year (Blaxter and Hunter 1982; Rogers and Ward 2007). This species was dominant at both Avoca and Terrigal Beaches, which could indicate that these areas provide alternate habitats for this species until ICOLL barriers are opened (Ayvazian and Hyndes 1995). The fact that only one species dominated the surf zones in great abundances indicates the depauperate nature of these particular surf zones compared to other surf zone studies. However, the bimonthly sampling regime must be taken into account, as stated earlier, this does not give a true indication of any seasonal variations in larval and juvenile fish assemblages.

Comparing the study of larval and juvenile fishes with the study of adult fish assemblages in Chapter 5 shows that although sampling times between the two studies differed by approximately two years, and sampling methods and sites also differed, the dominant species of each ICOLL were the same. Similar but larger sized fishes were targeted in the Chapter 5 study, where Acanthopagrus australis was dominant at Cockrone Lagoon, Atherinosoma microstoma was dominant at both Avoca and Wamberal Lagoons, and Ambassis jacksoniensis at Terrigal Lagoon. This suggests that that the fish assemblages of these ICOLLs do not show any significant longer term temporal changes despite the changing environmental conditions they experience, and that the larval and juvenile fish species collected during this study remain within ICOLLs.

Comparisons of larval and juvenile fish assemblages between the present study and previous studies is difficult, apart from that of Geraghty (2004), as most did not determine if recruitment into ICOLLs occurred from the adjacent surf zones though ultimately they must! Geographic differences in abundances and species collected from ICOLLs could reflect unique or similar environmental variables, barrier dynamics, sampling regimes and gear type. Ideally, a more

129 Chapter 4: Effects of barrier openings on larval and juvenile fishes

intensive sampling regime would encompass all factors in order to obtain the best possible representation of larval and juvenile fishes that may recruit into ICOLLs from adjacent surf zones. For example, monthly sampling of each habitat would show any seasonal variations that may occur, as many larval and juvenile species of fish may be more abundant between bimonthly sampling periods. Also, sampling in the entrance channel would give a more direct measure of the recruitment of larval and juvenile fishes into ICOLLs. However, due to difficulties in undertaking regular monthly samples, and the irregular opening times of barriers, a more intensive sampling regime was impossible. The results from the present study are similar to results from other NSW ICOLLs in collecting greater numbers of juvenile fishes (Griffiths 1999), which indicates that Central Coast ICOLLs are also important nursery areas for certain species of fishes.

4.4.3 Implications of this study for ICOLL management The main implication in managing ICOLLs for local councils is in relationship the effects of the artificial opening of barriers, and in particular the timing of these openings. Most artificial openings are related to the impact of high water levels on the surrounding foreshores. Local councils rely on artificial openings to alleviate flooding and help to improve the aesthetic integrity of the area. Although the practice of managed artificial openings is of concern, the current study has shown that barrier openings did not influence the recruitment of larval and juvenile fishes between either of the two main habitats studied, or the assemblages of larval and juvenile fishes within each habitat. ICOLLs were dominated mainly by resident species before and after barrier openings, with surf zones being dominated by species that are common to this habitat type. Therefore, with the exception of A. australis into Cockrone Lagoon, this suggests that barrier openings do not affect the recruitment to and the composition of fish assemblages found in most Central Coast ICOLLs. However, many physical and environmental factors can influence the recruitment of larval and juvenile fishes into ICOLLs, and the depauperate nature of the adjacent surf zone habitats may have resulted in no recruitment between the two habitats occurring during this study. However, further long-term studies are required to determine any definite temporal or spatial patterns that may occur in the fish assemblages of these ICOLLs.

4.5 Conclusion This study showed that ICOLLs have higher abundances and lower species richness of larval and juvenile fishes than their adjacent surf zones. Resident species were dominant in the ICOLLs, with EM species dominating the adjacent surf zones. Results also suggest that assemblages of larval and juvenile fishes vary temporally and spatially in ICOLLs. Small scale spatial variations occurred between sites (north, immediately adjacent to and south of the

130 Chapter 4: Effects of barrier openings on larval and juvenile fishes

ICOLL entrances) in the adjacent surf zones, with greater variations being found south of the ICOLL entrances. The patchy distribution of surf zone larval and juvenile fishes and differences in the assemblages between the two environments before and after barrier openings indicates that much of the recruitment into Central Coast ICOLLs generally does not occur from their adjacent surf zones, with the exception of Cockrone Lagoon, as numerous juvenile Acanthopagrus australis were collected after the only barrier opening there. Although, the life history of this A. australis and other MED and EM species collected in this study, suggests recruitment from adjacent surf zones does occur at some stage. However, during this study period, it could not be determined if larval and juvenile fishes were recruited from the adjacent surf zone or from within these ICOLLs themselves. Therefore, in most cases, from the evidence of this study, Central Coast ICOLLs are considered to be generally self-recruiting environments, not for all species, but for many of their resident species of fish.

131 Chapter 5: Factors influencing fish assemblages

Chapter 5: Factors influencing temporal and spatial variations of the fish assemblages of ICOLLs

132 Chapter 5: Factors influencing fish assemblages

5.1 Introduction The coastline of Australia has many shallow coastal waterbodies that provide a refuge for various species of fishes. Shallow water estuaries have become an important focal point for fish studies due to their connectivity between terrestrial, freshwater and marine environments and in the case of many ICOLLs, their relative isolation from marine influences due to the formation of barriers across their entrances. Most shallow water estuaries are concentrated along the south- eastern (Griffiths 2001a; Jones and West 2005) and south-western (Young and Potter 2002; Hyndes et al. 2003) coasts of Australia. Along the New South Wales (NSW) coast, many ICOLLs have catchments and foreshores that are highly developed and which consequently require the regular artificial opening of their barriers to the sea.

Barriers of ICOLLs are generally considered to be open if there is a connection between the ICOLLs and the sea, with regular movement of water in and out of the estuary. Closed barriers occur when sand forms across the entrance and there is no exchange of water between the two environments. The degree to which a barrier remains open or closed is dependent on the geographic location of the ICOLL, with many barriers remaining open from hours to a few weeks or even longer.

Fish species that utilise these environments have to contend with sudden changes in environmental conditions associated in some cases with frequent barrier openings. For instance, ICOLLs where barriers remain closed for long periods of time can come to resemble freshwater environments, but if barriers are opened more frequently environments resemble brackish to estuarine ecosystems (Jones and West 2005). Also, during the open phase, ICOLLs can resemble more marine environments, allowing recruitment processes to take place (Bennett 1989; Vorwerk et al. 2003). Therefore, it is generally considered that the timing, frequency and duration of barrier openings have a major influence on structuring fish assemblages in ICOLLs (Allan et al. 1985; Vorwerk et al. 2003; Jones and West 2005).

The effects that environmental variations may have on fish assemblages are of economic importance as ICOLLs have been regarded as important nursery habitats for many commercial and recreational fish species (Pollard 1994b; Griffiths 1999, 2001b). Previous studies have determined that the fish assemblages of ICOLLs are influenced by physical factors such as catchment size and habitat type (Allan et al. 1985; Griffiths and West 1999), water chemistry (Kennish 1990; Gordo and Cabral 2001; Jones and West 2005) or biotic factors (Kennish 1990; Vega-Cenejas and de Santillana 2004). Each factor can directly or indirectly influence one or more of the other factors, with the status of the barrier usually exerting an overriding influence (Griffiths 1999).

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Shallow water fish assemblages of ICOLLs have been well documented in NSW (Allan et al. 1985; Pollard 1994b; Griffiths and West 1999; Jones and West 2005), Western Australia (Potter and Hyndes 1999), and Victoria (Becker and Laurenson 2008). International studies have been focussed along the Cape Coast of South Africa (Harrison and Whitfield 1995; Cowley and Whitfield 2001), Albania (Peja et al. 1996), Portugal (Gordo and Cabral 2001) and Mexico (Vega-Cendjes and de Santillana 2004).

Most studies on spatial and temporal variations of fish assemblages isolate the effects of one or more particular environmental parameters on the structure of these assemblages. Salinity influences the movement of species and community structure (Young et al. 1997; Griffiths 2001a; Walsh et al. 2013). Variation in turbidity is also influential, especially for larval and juvenile fishes, as it provides protection from predators and is associated with increased nutrient levels that produce abundant food resources (West and King 1996; Whitfield 1999). Other factors known to influence assemblages include: the presence and extent of seagrass and other aquatic vegetation (Robinson et al. 1983; Allan et al. 1985; Pollard 1994a; Griffiths 2001c; Jones and West 2005), substrate composition (with many benthic species being associated with finer substrates compared to coarse substrates) (Gill and Potter 1993; Cowley and Whitfield 2001); and water temperature (Bennett 1989; Pollard 1994a). Spatial studies have been carried out which have determined the fish assemblages of several ICOLLs, Smiths Lake (Robinson et al. 1983), Dee Why Lagoon (Allan et al. 1985), Shellharbour Lagoon (Griffiths 1998, 2001a) and the Surrey Estuary (Becker and Laurenson 2008). In comparison, the current study compares four ICOLLs located along a 10 km stretch of coastline on the NSW Central Coast

One factor not generally considered is how land use within catchments influences temporal and spatial variations of ICOLL fish assemblages. The coastal locations of ICOLLs, especially those located near major cities, make for ideal settlement and recreational areas. Most catchments have varying degrees of urban and agricultural uses, along with remnant areas of natural vegetation. Urban development within catchments is of great interest as it is generally considered to exert a major influence on the environmental health of the ICOLLs (Davies et al. 2010). The amount of impervious material such as pavements, roads and buildings associated with developed catchments increases the amount of stormwater runoff that eventually changes the hydrology of ICOLLs (Beavan et al. 2001; Paul and Meyer 2001; Davies et al. 2010). Stormwater runoff contains high levels of sediments, nutrients and pollutants that can change water and sediment physicochemical qualities (Mikac et al. 2007; Waugh et al. 2007). The major consequences of this for ICOLLs are changes in salinity, turbidity and pH, and an increased risk of eutrophication (Pollard 1994a; Waugh et al. 2007; Davies et al. 2010).

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However, many of these effects occur intermittently as they are generally associated with heavy rainfall patterns (Waugh et al. 2007).

Few studies have compared the invertebrate faunas of natural and urbanised ICOLLs, with the exception of Mikac et al (2007) and Edgar and Barrett (2000). Mikac et al. (2007) found no significant differences between natural and modified water and sediment physicochemical qualities or invertebrate fauna in south-eastern NSW ICOLLs. The authors attributed these results to the modified catchments being less populated and industrialised compared to other urbanised catchments (Mikac et al. 2007). Edgar and Barrett (2000) compared a large number of Tasmanian estuaries, finding estuarine species to be resilient to urban development, but found that invertebrate assemblages differed between estuaries with different levels of human population density.

There is even less direct evidence of urban impacts on estuarine fish assemblages, especially in Australia. A review by Paul and Meyer (2001) showed that the degree of urban development within United States catchments resulted in fish diversity being lower in urban streams than natural streams; however, the processes causing these changes were not investigated. It is this lack of understanding that has resulted in this study being undertaken to provide some understanding of the physical and environmental factors that interact between ICOLLs and their catchments and how they affect their fish assemblages. In order to more fully understand the fish assemblages of ICOLLs and the influence of environmental variation on these assemblages, the following questions need to be addressed: 1. What species of fishes are found within ICOLLs and how abundant are these species? 2. How spatially and temporally variable are the fish assemblages of ICOLLs? 3. What is the relative importance of physical and biological factors, and barrier openings, in shaping the observed spatial and temporal variations in fish assemblages of ICOLLs, and are these factors consistent among ICOLLs?

This study thus investigated the following null hypotheses: 1. There are no differences in spatial and temporal variation in fishes assemblages between ICOLLs. 2. The environmental factors structuring variations in fish assemblages do not differ among the four ICOLLs, and barrier status is the most important factor.

135 Chapter 5: Factors influencing fish assemblages

5.2 Materials and methods

5.2.1 Study area The study area included Cockrone, Avoca and Wamberal Lagoons, in which all of the main habitat types found in ICOLLs, such as bare substrates, seagrass and algal meadows, and shallow and deep water, were sampled. Habitats of each ICOLL are described in Chapter 2. Terrigal Lagoon was also included in the study, however this ICOLL lacks any vegetated habitats. Catchments of each ICOLL have different land use characteristics (see Chapter 2). Subcatchment boundaries within each ICOLL catchment were defined and their land use characteristics determined for the purposes of this study (after Cardno Lawson Treloar 2010). The water area of each ICOLL is included as a subcatchment area. Cockrone Lagoon has 7 subcatchments (Figure 5.1) and at the time of the study 27% of the total catchment area comprised urban development. Urban refers to the dwellings and industrial structures and their associated infrastructure found within the catchment. Avoca Lagoon has 11 sub-catchments (Figure 5.2) and 35% of the total catchment area comprised urban development. Terrigal Lagoon has 10 subcatchments (Figure 5.3) and 79% of the total catchment area comprised urban development. Wamberal Lagoon has 10 sub-catchments (Figure 5.4) and 73% of the total catchment area comprised urban development.

Habitats common to all ICOLLs included a bare sandy area near the entrance, a central muddy basin, and shorelines fringed with macrophytes. However, one major difference distinguished Terrigal Lagoon from the other ICOLLs, in that it lacked aquatic vegetation. Ruppia sp., and algae (mainly floating mats of Enteromorpha intestinalis and the substrate attached Chara sp.) occurred in Cockrone, Avoca and Wamberal Lagoons. Water depth varied throughout the ICOLLs from less than 1 m in the backwaters and up to 4 m near the entrances.

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Figure 5.1. Cockrone Lagoon showing subcatchments (C1-C7) and locations of sampling sites (1-5) for bimonthly seine and multi-panel gill netting, and water sampling and algae collection.

137 Chapter 5: Factors influencing fish assemblages

Figure 5.2. Avoca Lagoon showing subcatchments (A1-A11) and locations of sampling sites (1-5) for bimonthly seine and multi-panel gill netting, and water sampling and algae collection.

138 Chapter 5: Factors influencing fish assemblages

139 Chapter 5: Factors influencing fish assemblages

Figure 5.4. Wamberal Lagoon showing subcatchments (W1-W10) and locations of sampling sites (1-5) for bimonthly seine and multi-panel gill netting, and water sampling and algae collection.

140 Chapter 5: Factors influencing fish assemblages

5.2.2 Pilot study A pilot study was undertaken in all ICOLLs. Bait traps, seine nets and multi-panel gill nets were trialled to determine their effectiveness for sampling fishes in different habitats of ICOLLs. Other studies have found these methods to be appropriate in the determination of ICOLL fish assemblages (Pollard 1994b; Griffiths 1998; Griffiths and West 1999; Gray et al. 2005; Rotherham et al. 2006).

Due to the logistics of setting traps and seine and multi-panel gill nets together, the bait traps were trialled separately from the seine and multi-panel gill nets. Bait traps were used in Avoca and Terrigal Lagoons only as these ICOLLs are between them representative of the range of ICOLLs to be sampled. The bait traps used were collapsible and made of green nylon mesh with approximate dimensions of 50 cm x 23 cm x 20 cm. Sites where bait traps were set covered the range of depths and habitats found within each ICOLL, including bare substrate, seagrass, and algae. Traps were baited with either frozen pilchards or tinned cat food containing seafood. The pilchards were thawed and cut into pieces. Three traps were set approximately 10 m apart at each site before sunset and left overnight before being retrieved just after dawn the next morning. Captured fish were collected and traps were reset and left all day before being re- collected just before sunset. Many traps set in Terrigal Lagoon were destroyed in the early stages of the pilot study, possibly by larger fish such as, long-finned eels Anguilla reinhardtii, known to frequent this ICOLL (personnel observation). All traps were thereafter reinforced with aluminium wire to prevent further damage and reset at the same sites. Specimens were collected with permission from the University of Newcastle’s Animal Care and Ethics Committee (ACEC Permit number 9711008) and the NSW Department of Primary Industries (Fisheries Permit number P05/0092). No fish were collected in traps from Terrigal Lagoon, and 16 fishes representing 3 species (3 families) were collected from Avoca Lagoon (Table 5.1). Most fish captured were Philypnodon grandiceps (Eleotridae). All fishes were only collected during the day using three bait traps per site.

Three seine hauls and three multi-panel gill nets were trialled in all ICOLLs and targeted different sizes and species of fishes (Gonzales et al. 2009). These two methods have been used effectively in previous studies of the fish assemblages of estuaries in southeast Australia and have shown to cause minimal environmental impact across a range of habitats (Gray et al. 2005). The short soak time of gill nets was deemed optimal for NSW estuaries and likely to reduce fish mortality (Rotherham et al. 2006). Gill nets were not used in Cockrone Lagoon as weather conditions deteriorated before the nets could be deployed.

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Table 5.1. Fishes collected from Avoca Lagoon during the pilot study using baited traps. (*too damaged to identify). Site Habitat type Water depth (m) Bait Species Sample period Size range Total Day Night (mm) Northern arm Bare mud <1 Pilchard Philypnodon grandiceps 2 0 31-37 2

Cat food Philypnodon grandiceps 5 0 29-51 5 Central basin Bare mud 4 Pilchard 0 0 0 Cat food Philypnodon grandiceps 2 0 30-53 2 Western arm Algae 1.5 Pilchard Philypnodon grandiceps 1 0 27 1 Cat food Philypnodon grandiceps 1 0 42 1 Unknown fish* 1 0 - 1 Gambusia holbrooki 2 0 29-30 2 Southern arm Ruppia 1.5 Pilchard Philypnodon grandiceps 1 0 32 1 Cat food Philypnodon grandiceps 1 0 48 1 Total 16

Chapter 5: Factors influencing fish assemblages

Multi-panel gill nets were 25 m total length with a drop of 2 m. The length of each panel was 5 m with mesh sizes of each panel being 25 x 19 mm; 30 x 50 mm; 25 x 80mm; 40 x 65mm; and 25 x 36 mm. Gill nets generally target larger mobile fishes and are suitable for use in both shallow and deep water areas within vegetated and unvegetated habitats (Rozas and Minello 1997). Fish become wedged, gilled or entangled in the nets. While gill nets were deployed the seine netting took place. The seine net was 20 m long x 1.5 m deep with a 12 mm mesh. Seine nets are generally more effective in shallow unvegetated and unobstructed areas (Rozas and Minello 1997), and were used to sample smaller species of fishes that frequented shoreline areas.

A total of 678 fishes representing 19 species (14 families) were collected using both seine and multi-panel gill nets (Table 5.2). Seine netting represented 88% of the total catch while gill netting represented 12% of the total catch. The greatest abundance of fishes was collected using seine nets from Wamberal Lagoon (n=265 fishes), these catches predominately consisting of Atherinosoma microstoma (Atherinidae). Terrigal Lagoon had the greatest number of fishes collected by gill netting (n=70 fishes), dominated by Liza argenta (Mugilidae) (Figure 5.5a). Terrigal Lagoon also had the highest species richness between all ICOLLs using seine nets (n=10) and gill nets (n=7) (Figure 5.5b). The only species common to all ICOLLs was Philypnodon grandiceps (Eleotridae). The results indicate that the use of three seine hauls and three multi-panel gill nets to be a better choice for determining fish assemblages in ICOLLs compared to three bait traps due to the number and diversity of fishes collected.

A pilot study usually determines the number of replicate samples chosen and statistical analysis confirms the number required. However, other considerations were taken into account such as the type of gear used in sampling. In this study three replicates samples were chosen to give a representative sample of fishes in ICOLLs. Firstly, this number of replicates has been deemed to be an effective number for use in estuarine studies (Gray et al. 2005; Rotherham et al., 2006). Secondly, the size of the ICOLLs dictated the number of replicates at a particular site that can be effective (Vorwerk et al. 2003). For example, some sites were small enough for 1-3 replicate gill and seine nets to cover almost the entire site, therefore in order to standardise the sampling regime it was decided that three replicate samples were sufficient. Thirdly, ICOLLs generally have low species richness with a greater abundance of a particular species, hence a greater number of replicate samples would not give a greater richness of species (Allan et al. 1985; Young and Potter 2002).

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Table 5.2. Fishes collected from ICOLLs using seine and multi-panel gill nets during the pilot study. Gill nets were not used in Cockrone Lagoon due to unsuitable weather conditions. ICOLLs Family/Species Cockrone Avoca Terrigal Wamberal Total seine gill seine gill seine gill seine gill Ambassidae Ambassis jacksoniensis 1 105 106 Atherinidae Atherinosoma microstoma 9 49 245 303 Callionymidae Repomucenus calcaratus 1 1 Clupeidae Herklotsichthys castelnaui 2 1 1 4 Eleotridae Philypnodon grandiceps 13 1 9 6 29 Gerreidae Gerres subfasciatus 1 1 Gobiidae Arenigobius bifrenatus 4 4 Pseudogobius species no.9 3 3 Mugilidae Liza argenta 12 34 2 48 Mugil cephalus 2 33 2 4 6 2 3 52 Myxus elongatus 1 10 25 7 43 Percichthyidae Macquaria colonorum 1 1 Platycephalidae Platycephalus fuscus 2 2 4 Platycephalus longispinis 3 3 Pseudomugilidae Pseudomugil signifer 1 1 Sillangidae Sillago ciliata 1 2 1 4 Sparidae Acanthopagrus australis 62 5 1 68 Rhabdosargus sarba 2 2 Tetraodontidae Tetractenos hamiltoni 1 1 Total 99 - 84 5 146 70 265 9 678

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(a)

300 250 200 150

100 Total no. of individualsno.of Total 50 0 Cockrone Avoca Terrigal Wamberal

(b) 12 10 8 6 4

Total no. of speciesno.of Total 2 0 Cockrone Avoca Terrigal Wamberal ICOLLs seine gill Figure 5.5. Results of the pilot study comparing three replicate samples of seine and multi -panel gill nets showing (a) total number of fishes collected and (b) the number of species of fishes collected from Cockrone, Avoca, Terrigal and Wamberal lagoons during December 2008. Gill nets were not used in Cockrone Lagoon due to unsuitable weather during sampling.

5.2.3 Sampling design The sampling design of the current study was undertaken with the bimonthly collection of fishes, when possible, as sampling could not be undertaken after barriers were opened due to extremely low water levels and in some cases the complete exposure of bottom sediments. Although, the barrier at Terrigal Lagoon was opened more frequently, this ICOLL took less time to increase water levels due to marine influxes, rainfall and stormwater run-off. Therefore, sampling took place after barrier closure and when water levels had increased. All sampling took place during daylight hours of between 07.30 and 15.00 hr from February 2009 to June 2010. Three replicate multi-panel gill nets were deployed approximately 30 m apart by boat and left to soak for 1–1.5 hr, while three replicate seine net hauls were performed by hand from the shoreline. Replicate seine net hauls were approximately 10 m apart to maintain independence

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between replicate hauls. Fishes collected from seine nets were euthanased in ice slurry and then fixed in 10% formalin in the field. In some cases, high numbers of a particular species were collected, therefore fishes collected with a TL between the range of the smallest and largest fishes of that species collected were counted only and returned at the point of capture. In the laboratory a subsample of the dominant species of fishes collected from each ICOLL by seine nets were used for the dietary studies and processed as described in Chapter 6. All other fishes collected by seine nets were put through a change of 10% formalin for 1 wk and then after 1 wk specimens were thoroughly rinsed with tap water and stored in 70% ethanol until they were processed. All fishes were counted and measured to the nearest 1 mm TL and identified to the lowest possible taxon using Collette (1974), McDowall (1996), Hutchins and Swainston (1999) and Kuiter (2000).

Fishes collected from multi-panel gill nets were removed from the nets, identified and measured to the nearest 1 mm TL. Live fishes were released at the point of capture. From the outset of the study one sample of each species was collected from gill nets to confirm identification and was kept as a voucher specimen. These fishes were also euthanased by ice slurry in the field and kept on ice until returned to the laboratory where they were transferred to 70% ethanol. Dead fishes collected from the nets were kept on ice until returned to the laboratory where the carcasses were disposed of as biological waste according to animal ethics requirements.

Large numbers of juvenile sparids were collected from both Cockrone and Avoca Lagoons, however, in some cases identification of sparids found in ICOLLs to species-level can be difficult due to hybridisation (Roberts et al. 2009). The majority of species collected were Acanthopagrus australis determined from their fin meristics and characteristic yellow fins (Kuiter 2000). However, there were occasions when some juvenile fishes did not have yellow fins indicating they maybe Acanthopagrus butcheri or a hybrid between the two species. Since it is difficult to distinguish morphologically between these hybrids and A. butcheri (Roberts et al. 2009), all juvenile sparids in the present study were classed as A. australis.

5.2.4 Environmental variables Salinity (ppt), turbidity (ntu), temperature (°C) and dissolved oxygen (mg/L) were recorded in situ at a depth of 0.5 m at each location (see Figures 5.1-5.4) using a Yeo-Kal 611 Water Quality Analyser. Percentage cover of algae, Ruppia sp., bare and rocky substrates was estimated visually by scanning the area where multi-panel gill nets were deployed and where seine nets were hauled at each sampling site. The biomass of algae (Enteromorphora intestinalis and Chara sp.) occurring in each sampling site was quantified using five replicate 0.5 m2 quadrats haphazardly placed throughout each site. Within each quadrat only algae deemed to be

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‘living’ was collected and placed into dark polyethylene bags for transportation to the laboratory. Terrigal Lagoon does not have any seagrass or algal habitats. In the laboratory, algal samples were thoroughly rinsed with tap water and all extraneous material including, sediment, seagrass and fauna were removed and the dry weight determined by oven drying at 60°C for 48 hr (da Cunha and Wasserman 2003). The distance of sampling sites from the barrier was measured (to the nearest 10 m) using topographical maps (LPI 2001). The percentage of land- use within each sub-catchment was determined from Cardno Lawson Treloar (2010). Ambient sediment grain size composition of each site was determined from samples collected during May 2004 (see Chapter Two).

Artificial barriers openings are generally undertaken by Gosford City Council, and the dates of openings were obtained from the Council. ICOLLs may also open naturally or are sometimes opened illegally. Therefore to supplement the data from Gosford City Council, the Manly Hydraulic Laboratories website (http://mhl.nsw.gov.au) was also checked. Real time data on ICOLL water levels were recorded by a pressure-sensing automatic water level device that stored data for up to 6 mo. Once data was accessed from the website, barrier openings were also confirmed by visual inspection to ensure accuracy of the data downloaded on the website.

5.2.5 Data analysis Non-parametric multivariate analyses were used to determine patterns of spatial and temporal variation in the fish assemblages of ICOLLs and the relationships of this variation to the measured environmental variables and the status of the barrier. Data for seine and gill nets were analysed separately due to their different selectivity for species and fish sizes (Gonzales et al. 2009). Three-way permutational multivariate analysis of variance (PERMANOVA) was used to test the null hypotheses that there are no differences in spatial and temporal variation in fish assemblages among ICOLLs using the following factors: (A) ICOLLs: fixed, four levels; (B) Time: random, eight levels and (C) Site nested in ICOLLs: random, five levels, except for Terrigal Lagoon which has four levels. Data were square-root transformed and all tests were derived from the Bray-Curtis dissimilarity resemblance measure permutated 9999 times under the reduced model to determine significance. Due to large numbers of zeros in the data a dummy value (+1) was added (Clarke and Gorley 2006). Significant effects were further investigated using PERMANOVA pair-wise comparisons. PERMANOVA is sensitive to multivariate dispersion, therefore significant results were investigated with the PERMDISP routine. This program is used to test for homogeneity of dispersions between groups by comparing the average of distances from the centroids (Anderson 2004).

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For significant factors, the Similarity of Percentages (SIMPER) procedure in PRIMER was used to determine the fish species responsible for these differences (Clarke 1993). Species that contributed up to 90% of the dissimilarity of the significant pair-wise tests were analysed. Large values (i.e. >1) of the ratio of dissimilarity/standard deviation(dissimilarity) (where dissimilarity is the average contribution of the ith species to the overall dissimilarity between 2 groups of standard deviation) for a species indicated the species was consistently important to dissimilarity in all pair-wise comparisons of samples in 2 groups (Clarke 1993). Species with a percentage dissimilarity >3% and with a dissimilarity/standard deviation (dissimilarity) >1 were regarded as being important contributors to dissimilarity (Terlizzi et al. 2005). Multi- dimensional scaling ordination (MDS) was used to visualise spatial and temporal differences in fish assemblages.

PERMANOVA was also used to test for differences in mean numbers of species and the mean total number of individuals. All tests were based on square-root transformations (Clarke 1993) and derived from a Euclidean distance matrix permutated 9999 times under a reduced model to test for significance. Dispersions in the mean number of species and the mean total number of individuals were compared using PERMDISP. Significant effects were further investigated using PERMANOVA pair-wise comparisons.

Distance-based linear models (DISTLM) analysis was used to test the hypothesis that the environmental factors structuring variations in fish assemblages do not differ among the four ICOLLs and that barrier status is the most important factor. Data on 17 environmental variables were used for each ICOLL, incorporating the factors that described the physical and biological environment, barrier status, and characteristics of the sub-catchment (Table 5.3). Draftsmen plots of untransformed environmental variables were produced to determine the extent of data skewness and multivariate normality and the need for transformations (Clarke and Ainsworth 1993), however since no skewness occurred, all data were analysed untransformed. The matrix of pair-wise correlations of environmental variables was examined for large pair-wise correlations (r≥0.95) for each ICOLL, with one of the variables being eliminated from the analysis (Anderson et al. 2008).

The smallest set of environmental variables that together explained a significant amount of variation in fish assemblages was determined by the BEST procedure in DISTLM, with the Akaike Information Criterion (AIC) used as the selection criterion (Anderson et al. 2008). The BEST procedure evaluated all possible combinations of environmental variables to identify the combination of variables with the lowest AIC. A distance-based redundancy analysis (dbRDA), based on Pearson’s linear correlations, was used to visualise the relationship between the

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selected environmental variables and the fish assemblages. The dbRDA is an ordination technique that overlays vectors for the selected environmental variables on the spatial arrangement of samples, with the length and direction of a vector indicative of the magnitude of the correlation between the variable and depicted sample arrangement. All multivariate and univariate analyses were examined using PRIMER v6 and PERMANOVA+ (PRIMER-E).

Table 5.3. Summary of the 17 environmental variables used in DISTLM analysis. Sediments were separated into different grain-sizes; coarse sand ≥1mm, medium sand >0.5 mm, fine sand >212 µm, coarse silt >63 µm and fine silt/clay <63 µm (Briggs 1977). Variable Units of measure Type Range Salinity ppt Continuous 6.44-36.95 Temperature °C Continuous 12.91-31.89 Barrier status - Categorical Open/Closed Algal cover % Continuous 0-100 Ruppia cover % Continuous 0-100 Bare substrate cover % Continuous 0-100 Rock cover % Continuous 0-100 Algal mass g Continuous 0-314 Distance from barrier m Continuous 90-1500 Urban development % Continuous 0-100 Agricultural land-use % Continuous 0-100 Forest land-use % Continuous 0-100 Sediment - % coarse sand mm Continuous ≥1.0 Sediment – % medium sand mm Continuous 0.5-1.0 Sediment – % fine sand µm Continuous 212-0.5 Sediment – % coarse silt µm Continuous 63-212 Sediment – % fine silt/clay µm Continuous <63

5.3 Results

5.3.1 ICOLL openings Over the course of this study the four ICOLLs were opened a total of 34 occasions, including 29 artificial openings managed by Gosford City Council and two openings that were deemed to be natural openings (based on data from MHL). The Council also documented three illegal openings. Terrigal Lagoon was opened on 24 occasions, Avoca on five, Cockrone three times and Wamberal Lagoon twice (Table 5.4).

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5.3.2 Fish assemblages of ICOLLs

5.3.2.1 Overview of fish assemblages A total of 14 765 fishes representing 35 species (25 families) were collected using both seine and multi-panel gill nets from all ICOLLs between February 2009 and June 2010. The greatest abundance of fishes was collected from Wamberal Lagoon (n=6 298) and the smallest number was collected from Terrigal Lagoon (n=2 105) (Figure 5.6a). The total numbers of seine and multi-panel gill nets deployed in Wamberal and Terrigal Lagoons were 240 and 192 samples respectively. The greatest number of species was found at Terrigal Lagoon (n=29) and the smallest number at Wamberal Lagoon (n=13) (Figure 5.6b). Nine species were common to all ICOLLs: Atherinosoma microstoma, Philypnodon grandiceps, Arenigobius bifrenatus, Pseudogobius species no. 9, Hyporhamphus regularis, Mugil cephalus, Myxus elongatus, Platycephalus fuscus and Acanthopagrus australis (Table 5.5). Fourteen species were only collected from one ICOLL: Repomucenus calcaratus (Cockrone Lagoon); Arripis trutta, Pseudocarnx georgiannus, Hyperlophus vittatus (Avoca Lagoon); Ambassis jacksoniensis, Trachinotus sp., Gerres subfasciatus, Heterodontus portusjacksoni, Monodactylus argenteus, Pseudorhombus arsius, Macquaria colonorum, Pomatomus saltatrix and Centropogon australis (Terrigal Lagoon); and Anguilla reinhardtii (Wamberal Lagoon).

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Table 5.4. ICOLL barrier openings between February 2009 and June 2010. *denotes artificial barrier opening by Gosford City Council. #denotes illegal barrier opening confirmed by Gosford City Council. Other barrier opening data, natural or artificial, were obtained from MHL and confirmed by visual inspection. n= the number of barrier openings. ICOLLs Cockrone Avoca Terrigal Wamberal (n=3) (n=5) (n=24) (n=2) 3/6/09* 22/5/09* 13/2/09* 18/6/09* 15/6/09 27/5/09* 16/2/09* 4/6/10* 23/6/09 12/6/09# 9/3/09* 13/6/09# 2/4/09* 27/6/09# 27/4/09* 1/5/09* 21/5/09* 24/5/09* 26/5/09* 30/5/09* 16/6/09* 22/6/09* 17/7/09* 22/7/09* 5/8/09* 11/8/09* 25/10/09* 6/2/10* 31/3/10* 1/5/10* 21/5/10* 25/5/10* 28/5/10* 10/6/10*

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(a)

7000 n=240 6000

5000 n=240 4000

3000 Total no. of fishof no. Total n=240 n=192 2000

1000

0 Cockrone Avoca Terrigal Wamberal

(b)

35 30 n=192 25 n=240 20 n=240 15 n=240 10

Total no. of speciesof no. Total 5 0 Cockrone Avoca Terrigal Wamberal

ICOLLs Figure 5.6. (a) Total abundances of fishes, and (b) the total number of species collected (results from seine and multi-panel gill nets combined) from the four ICOLLs. n=the total number of samples taken over the sampling period.

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Table 5.5. Presence/absence of fishes collected from ICOLLs between February 2009 and June 2010. Fishes were collected by seine net (s) or gill nets (g) or by both methods (s,g). ICOLL Family/Species Common name Cockrone Avoca Terrigal Wamberal Ambassidae Ambassis jacksoniensis Port Jackson perchlet s s Ambassis marianus Ramsay’s glassfish s Anguillidae Anguilla reinhardtii Marbled eel s Arripididae Arripis trutta Eastern Australian salmon g Atherinidae Atherinosoma microstoma Small-mouthed hardyhead s s s s Callionymidae Repomucenus calcaratus Spotted sand-dragonet s Carangidae Pseudocaranx georgiannus White trevally g Trachinotus sp. s Clupeidae Herklotsichthys castelnaui Southern herring g s,g g Hyperlophus vittatus Sandy sprat s Eleotridae Philypnodon grandiceps Flathead gudgeon s s s s Gerreidae Gerres subfasciatus Common silver belly s,g Girellidae Girella tricuspidata Luderick g g Gobiidae Arenigobius bifrenatus Bridled goby s s s s Favonigobius tamarensis Tamar River goby s s s Gobiopterus semivestitus Glass goby s Pseudogobius species no.9 Blue-spot goby s s s s Hemiramphidae Hyporhamphus regularis River garfish s s,g s s Heterodontidae Heterodontus portusjacksoni Port Jackson shark g

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Table 5.5 continued... ICOLL Family/Species Common name Cockrone Avoca Terrigal Wamberal Monodactylidae Monodactylus argenteus Silver batfish g Mugilidae Liza argenta Flat-tail mullet s s g Mugil cephalus Sea mullet s,g s,g s,g s,g Myxus elongatus Sand mullet s,g s,g s,g s,g Paralichthyidae Pseudorhombus arsius Large-tooth flounder s Percichthyidae Macquaria colonorum Estuary perch g Platycephalidae Platycephalus fuscus Dusky flathead g g s,g g Platycephalus longispinis Long-spined flathead s Poeciliidae Gambusia holbrooki Mosquito fish s s s Pomatomidae Pomatomus saltatrix Tailor g Pseudomugilidae Pseudomugil signifer Pacific Blue-eye s s Scorpaenidae Centropogon australis Fortescue s Sillangidae Sillago ciliata Sand whiting s,g g s,g Sparidae Acanthopagrus australis Yellow-finned bream s,g s,g s,g g Rhabdosargus sarba Tarwhine g g g Tetraodontidae Tetractenos hamiltoni Common toadfish s s s,g

5.3.2.2 Fish assemblages of Cockrone Lagoon A total of 2 235 fishes representing 18 species (12 families) were collected using seine and multi-gill nets from Cockrone Lagoon between February 2009 and June 2010 (Appendix 1a). The numerically dominant species collected was the yellowfin bream, Acanthopagrus australis (Sparidae) (n=1 532) representing 68% of the total number of fishes collected. Graphical representation of temporal and spatial patterns of fish abundances collected by seine and multi- panel gill nets combined varied at each site throughout the study (Figure 5.7a). Overall, the greatest abundance of fishes collected was from site 1 near the entrance with abundances peaking during November 2009 before decreasing over the next three sampling periods. Fish

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abundances were consistent before the barrier opening, but decreased dramatically in the next two sampling periods after the barrier was opened, indicating that fishes have departed from the ICOLL during the barrier opening. The large temporal and spatial variation tended to coincide with the high densities of A. australis. The total number of species showed similar trends to total abundances (Figure 5.7b). In most cases, the total number of species was greatest at site 1, with numbers peaking during April and November 2009. Species numbers also decreased in the two sampling periods after the barrier had opened.

(a)

400 350 300 250 200 150

Total no. of individualsof no. Total 100 50 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10

(b) 9 8 7 6 5 4 3

2 Total no. of speciesof no. Total 1 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Sampling period Site 1 Site 2 Site 3 Site 4 Site 5

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5.3.2.2.1 Seine net sample A total of 1 989 fishes representing 16 species (12 families) were collected by seine nets. The dominant species was Acanthopagrus australis (n=1 491) representing 75% of the total catch. The TL of A. australis ranged between 23-142 mm with approximately 70% of the species ranging between 40-59 mm (Figure 5.8). The length-frequency distribution indicates that all of the fishes captured were juveniles to sub-adults (Hannan and Williams 1998).

5.3.2.2.2 Multi-panel gill net sample A total of 246 fishes representing 6 species (5 families) were collected by the multi-panel gill nets. The dominant species was Mugil cephalus (n=136), representing 55% of the total catch. Size ranged between 160-437 mm TL, dividing into two distinct cohorts, with approximately 26% being 200-219 mm TL and 24% being 180-199 mm TL (Figure 5.9). The length-frequency distribution indicates that the majority of fishes captured were sub-adults (Rowling et al. 2010).

Acanthopagrus australis (n=1 491) 80 70 60 50

40 % frequency % 30 20 10 0 20-39 40-59 60-79 80-99 100-119 120-139 >140 Size (mm) Figure 5.8. Length-frequency distribution of Acanthopagrus australis (n=1 491) collected between February 2009 and June 2010 using a seine net in Cockrone Lagoon.

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Mugil cephalus (n=136) 30

% frequency % 10

0 160- 180- 200- 220- 240- 260- 280- 300- 320- 340- >360 179 199 219 239 259 279 299 319 339 359 Size (mm) Figure 5.9. Length-frequency distribution of Mugil cephalus (n=136) collected between February 2009 and June 2010 using multi-panel gill nets in Cockrone Lagoon.

5.3.2.3 Fish assemblages of Avoca Lagoon A total of 4 127 fishes representing 19 species (14 families) were collected using seine and gill nets from Avoca Lagoon between February 2009 and June 2010 (Appendix 1b). The numerically dominant species collected were the small-mouthed hardyhead Atherinosoma microstoma (Atherinidae) (n=1 702) and the yellowfin bream, Acanthopagrus australis (Sparidae) (n=1 571) representing 41% and 38% respectively of the total number of fishes collected. Graphical representation of total number of fishes collected by seine and multi-panel gill nets combined revealed considerable spatial and temporal variation (Figure 5.10a). In most cases the greatest numbers of fishes collected were from site 1 near the entrance, with abundances peaking during April 2009 before decreasing over the sampling period after the barrier had opened, indicating that fishes have departed from the ICOLL during the barrier opening. Fish abundances gradually increased between September 2009 and January 2010 before beginning to decline towards the end of the study period. The large temporal and spatial variation in total abundance mostly reflected temporal and spatial variation in numbers of A. microstoma. The total number of species collected was generally consistent across sampling periods, except that it decreased slightly in the sampling period after the barrier had opened. Overall, site 1 near the entrance had the greatest number of species.

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(a)

800 700 600 500 400 300

Total no. of individualsno.of Total 200 100 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10

(b) 9 8 7 6 5 4 3

2 Total no. of speciesof no. Total 1 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Sampling period Site 1 Site 2 Site 3 Site 4 Site 5 Figure 5.10. Temporal and spatial variation of fishes collected with seine and multi-panel gill nets for (a) the total number of individuals and (b) the number of species collected bimonthly from Avoca Lagoon between February 2009 and June 2010. Months and sites with no data indicate no fishes were collected, and the data is the sum of all replicates in each site. Solid vertical lines indicate multiple barrier openings that occurred between sampling periods.

5.3.2.3.1 Seine net sample A total of 3 674 fishes representing 12 species (8 families) were collected by seine nets. The dominant species were Atherinosoma microstoma (n=1 702) and Acanthopagrus australis (n=1 492) representing 46% and 41% respectively of the total catch. The TL of A. microstoma ranged between 18 mm and 94 mm with approximately 30% of the fishes being between 30 mm and 39 mm and 28% between 40 mm and 49 mm (Figure 5.11). The length-frequency distribution indicates that the majority of fishes captured were juveniles to sub-adults (Hannan and Williams 1998).

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Atherinosoma microstoma (n=1 702) 35

% frequency % 10

0 10-19 20-29 30-39 40-49 50-59 60-69 70-79 80-89 >90 Size (mm) Figure 5.11. Length-frequency distribution of Atherinosoma microstoma (n=1 702) collected between February 2009 and June 2010 using a seine net in Avoca Lagoon.

5.3.2.3.2 Multi-panel gill net sample A total of 453 fishes representing 11 species (10 families) were collected by multi-panel gill nets. The dominant species was Mugil cephalus (n=315), representing 76% of the total species. Total length ranged between 173 and 545 mm, with approximately 40% of M. cephalus being between 400 and 449 mm (Figure 5.12). The length-frequency distribution indicates that the majority of fishes captured were adults (Rowling et al. 2010). Mugil cephalus (n=315) 45 40 35 30 25 20 % frequency % 15 10 5 0 150-199 200-249 250-299 300-349 350-399 400-449 450-499 >500 Size (mm) Figure 5.12. Length-frequency distributions of Mugil cephalus (n=315) collected between February 2009 and June 2010 using multi-panel gill nets in Avoca Lagoon.

5.3.2.4 Fish assemblages of Terrigal Lagoon A total of 2 105 fishes representing 29 species (22 families) were collected using seine and gill nets from Terrigal Lagoon between February 2009 and June 2010 (Appendix 1c). The

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numerically dominant species collected were the sand mullet Myxus elongatus (Mugilidae) (n=479) and the Port Jackson Perchlet, Ambassis jacksoniensis (Ambassidae) (n=475) representing 23% and 22% respectively of the total fishes collected. Graphical representation of total number of fishes collected by seine and multi-panel gill nets combined revealed considerable spatial and temporal variation (Figure 5.13a). In most cases the greatest number of fishes was collected from site 2 with abundances peaking during April and November 2009. The numerous barrier openings did not appear to affect fish abundances throughout the study period, except in June 2010, indicating that fishes have departed from the ICOLL during the barrier opening. The total numbers of species collected was generally consistent at sites 1, 2 and 4, with smaller number of species at site 3. The number of species did not appear to be influenced by barrier openings (Figure 5.13b).

(a)

250

200

150

100 Total no. of individualsno. of Total 50

0 Feb-09 Apr-09 Jul-09 Sep-09 Nov-09 Jan-10 Mar-10 Jun-10 (b) 14

4 Total no. of speciesno.of Total 2

0 Feb-09 Apr-09 Jul-09 Sep-09 Nov-09 Jan-10 Mar-10 Jun-10 Sampling period Site 1 Site 2 Site 3 Site 4 Figure 5.13. Temporal and spatial variation of fishes collected with seine and multi-panel gill nets for (a) total number of individuals and (b) the number of species collected bimonthly from Terrigal Lagoon between February 2009 and June 2010. Solid vertical lines indicate multiple barrier openings occurred between sampling periods.

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5.3.2.4.1 Seine net sample A total of 1 678 fishes representing 25 species (15 families) were collected by seine netting, with the numerically dominant species being Ambassis jacksoniensis (n=475), representing 28% of the total catch. Total lengths of A. jacksoniensis ranged from 37 to 67 mm, with approximately 56% these fishes being between 50 and 59 mm (Figure 5.14). The length- frequency distribution indicates that the majority of fishes captured were adults (Mazumder et al. 2006).

Ambassis jacksoniensis (n=475) 60

30 % frequency % 20

0 30-39 40-49 50-59 60-69 Size (mm) Figure 5.14. Length-frequency distribution of total lengths of Ambassis jacksoniensis (n=475) collected between February 2009 and June 2010 using a seine net in Terrigal Lagoon.

5.3.2.4.2 Multi-panel gill net sample A total of 425 fishes representing 14 species (11 families) was collected by multi-panel gill nets, with Myxus elongatus (n=209) being the numerically dominant species, representing 49% of the total catch. Total lengths of M. elongatus ranged from 185 to 330 mm, with approximately 50% being between 220-239 mm (Figure 5.15). The length-frequency distribution indicates that the majority of fishes captured were adults (Rowling et al. 2010).

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Myxus elongatus (n=209) 60

30 % frequency % 20

0 180-199 200-219 220-239 240-259 260-279 280-299 >300 Size (mm) Figure 5.15. Length-frequency distribution of total length of Myxus elongatus (n=209) collected between February 2009 and June 2010 using multi-panel gill nets in Terrigal Lagoon.

5.3.2.5 Fish assemblages of Wamberal Lagoon A total of 6 298 fishes representing 13 species (10 families) were collected using seine and gill nets from Wamberal Lagoon (Appendix 1d). The numerically dominant species collected was the small-mouthed hardyhead, Atherinosoma microstoma (Atherinidae) (n=5 666), representing 90% of the total catch. Graphical representation of the total number of fishes collected by seine and multi-panel gill nets combined revealed considerable spatial and temporal variation (Figure 5.16a). The greatest number of fishes was collected from site 1 near the entrance, with abundances peaking during April 2009 and January and March 2010, before decreasing in the sampling period after the barrier had opened, indicating that fishes have departed from the ICOLL during the barrier opening. The large temporal and spatial variation in total fish abundance mostly reflected temporal and spatial variation in numbers of A. microstoma. In contrast, the total numbers of species were generally consistent across the sampling period, except that it decreased slightly in the sampling period after the barrier had opened (5.16b).

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(a)

1600 1400 1200 1000 800 600

400 Total no. of individualsno.of Total 200 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10

(b) 8 7 6 5 4 3 2

Total no. of speciesno.of Total 1 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Sampling period Site 1 Site 2 Site 3 Site 4 Site 5

Figure 5.16. Temporal and spatial variation of fishes collected with seine and multi -panel gill nets of (a) the total number of individuals and (b) the number of species collected bimonthly from Wamberal Lagoon between February 2009 and June 2010. The dotted vertical lines indicate a single barrier opening that occurred between sampling periods.

5.3.2.5.1 Seine net sample A total of 5 995 fishes representing 10 species (7 families) were collected by seine nets. The dominant species was Atherinosoma microstoma (n=5 666), contributing to 94% of the total catch. Total lengths ranged between 16 and 82 mm, with the majority of fishes being between 30 and 59 mm (Figure 5.17). The length-frequency distribution indicates that the majority of fishes captured were sub-adults and adults (Molsher et al. 1994).

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Atherinosoma microstoma (n=5 666) 30

15 % frequency % 10

0 10-19 20-29 30-39 40-49 50-59 60-69 70-79 >80 Size (mm) Figure 5.17. Length-frequency distribution of Atherinosoma microstoma (n=5 666) collected between February 2009 and June 2010 using a seine net in Wamberal Lagoon.

5.3.2.5.2 Multi-panel gill net sample A total of 303 fishes representing 5 species (4 families) were collected by gill netting, with the sea mullet Mugil cephalus (n=176) representing 58% of the total catch. Total lengths ranged between 159-528 mm, with the majority of fishes being between 300-499 mm (Figure 5.18). The length-frequency distribution indicates that the majority of fishes captured were adults (Rowling et al. 2010).

Mugil cephalus (n=176) 30

15 % frequency % 10

0 150-199 200-249 250-299 300-349 350-399 400-449 450-499 >500 Size (mm) Figure 5.18. Length-frequency distribution of Mugil cephalus (n=176) collected between February 2009 and June 2010 using multi-panel gill nets in Wamberal Lagoon.

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5.3.3. Comparison of fish assemblages between ICOLLs

5.3.3.1 Multivariate analysis-seine net samples Spatial and temporal variability of fish assemblages were significant for the factors Time x Site (ICOLL) and Time x ICOLL (Table 5.6), therefore both significant variations were further investigated using pairwise tests in PERMANOVA. The significant Time x Site(ICOLL) interaction occurred because patterns of variation among sites in fish assemblages changed through time in different ways in the four ICOLLs. Fish assemblages in Cockrone Lagoon varied significantly among all sites at sampling times 2, 7 and 8; at Avoca Lagoon at sampling times 1, 2 and 5-7; at Wamberal Lagoon at times 2, 6 and 7; and at Terrigal Lagoon at sampling times 2-7. The significant Time x ICOLL interaction occurred because fish assemblages of Cockrone and Avoca Lagoons, and of Wamberal and Terrigal Lagoons, were significantly different at sampling times 3 and 5-8, and assemblages of Avoca and Terrigal Lagoons, and Wamberal and Terrigal Lagoons, differed at sampling times 1 and 4.

Table 5.6. Summary of 3-factor PERMANOVA testing for differences in the fish assemblages of ICOLLs collected by seine nets. Data was square-root transformed. Source df MS Pseudo-f p Time 7 24898 12.26 0.0001 ICOLL 3 43453 3.10 0.0001 Site (ICOLL) 15 6016 2.96 0.0001 Time x ICOLL 21 8657 4.26 0.0001 Time x Site(ICOLL) 105 2030 2.70 0.0001 Res 304 752.64

PERMDISP for Time x Site(ICOLL) was significant (F=9.60, df=151, p=0.0001) and occurred because sites at each ICOLL differed in their variability at different sampling times. Cockrone Lagoon differed in variability at five sampling times (sampling time 3-7); Avoca Lagoon differed in variability at two sampling times (sampling time 3 and 4); Terrigal and Wamberal Lagoons differed in variability at one sampling time (sampling time 8).

PERMDISP for Time x ICOLL was significant (F=7.36, df=31, p=0.0001) and occurred because the pairwise patterns of differences in variability between ICOLLs were not consistent at each sampling time. Cockrone and Avoca Lagoons were significantly different at sampling times 3 and 6-8, and Cockrone and Wamberal Lagoons were significantly different at sampling times 3, 4 and 8, and Cockrone and Terrigal Lagoons were significantly different at all sampling times (1-8). Avoca and Wamberal Lagoons were significantly different at sampling times 3 and

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6-8, and Avoca and Terrigal Lagoons were significantly different at sampling times 1, 3 and 5. Wamberal and Terrigal Lagoons were significantly different at all sampling times (1-8).

The MDS plots illustrate the variability of fish assemblages where the distances between points indicate dissimilarity (Figure 5.19). Cockrone Lagoon shows that replicate sites at different times have distinct groups at sampling times 1, 2 5 and 8, compared to Avoca, Wamberal and Terrigal Lagoons where there was no clustering shown.

Cockrone Lagoon Avoca Lagoon 2D Stress: 0.07 2D Stress: 0.11

Terrigal Lagoon Wamberal Lagoon 2D Stress: 0.2 2D Stress: 0.06

SIMPER analysis of the Time x Site ICOLL interaction found differences in fish assemblages among sites at sampling times 2, 7 and 8 at Cockrone Lagoon, and sampling times 1, 2 and 5-7 at Avoca Lagoon, and sampling times 2, 3 and 5-7 at Terrigal Lagoon, and at sampling times 2 and 6 at Wamberal Lagoon (Table 5.7).

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Table 5.7. Summary of SIMPER results showing fish species collected by seine net responsible for temporal differences among sites in fish assemblages of each ICOLL. Species that contributed up to 90% of the dissimilarity between sampling times are shown. Cockrone Lagoon Time 2 Time 7 Time 8 Atherinosoma microstoma Acanthopagrus australis Pseudogobius no. 9 Acanthopagrus australis Sillago ciliata Myxus elongatus Hyporhamphus regularis Philypnodon grandiceps Avoca Lagoon Time 1 Time 2 Time 5 Time 6 Time 7 Acanthopagrus australis Atherinosoma microstoma Acanthopagrus Atherinosoma Atherinosoma australis microstoma microstoma Atherinosoma microstoma Favonigobius tamarensis Philypnodon Acanthopagrus Philypnodon grandiceps australis grandiceps Philypnodon grandiceps Philypnodon grandiceps Philypnodon Hyporhamphus grandiceps regularis Hyporhamphus Tetractenos regularis hamiltoni Terrigal Lagoon Time 2 Time 3 Time 5 Time 6 Time 7 Philypnodon grandiceps Myxus elongatus Philypnodon grandiceps Pseudomugil Philypnodon signifer grandiceps Myxus elongatus Mugil cephalus Sillago ciliata Philypnodon Arenigobius grandiceps bifrenatus Ambassis jacksoniensis Sillago ciliata Myxus elongatus Myxus Ambassis elongatus jacksoniensis Philypnodon grandiceps Arenigobius bifrenatus Mugil cephalus Gobioterus semivestitus Pseudogobius no. 9 Atherinosoma Liza argenta microstoma Gerres Gerres subfasciatus subfasciatus Gambusia holbrooki Wamberal Lagoon Time 2 Time 6 Atherinosoma microstoma Atherinosoma microstoma Hyporhamphus regularis Philypnodon grandiceps Favonigobius tamarensis Hyporhamphus regularis Gambusia holbrooki Pseudogobius no. 9

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SIMPER analysis of the Time x ICOLL interaction found differences in fish assemblages between Cockrone and Avoca Lagoons at sampling times 1, 2 and 6, between Cockrone and Terrigal Lagoons at sampling times 1, 2 and 5, between Cockrone and Wamberal Lagoons at sampling times 1, 2, 4 and 5-8. Differences in fish assemblages occurred between Avoca and Terrigal Lagoons at sampling times 5 and 6, and between Avoca and Wamberal Lagoons at sampling times 2, 5-7. Differences in fish assemblages were found between Terrigal and Wamberal Lagoons at sampling times 1, 2 and 5-7 (Table 5.8).

Table 5.8. Summary of SIMPER results showing fish species collected by seine net responsible for temporal differences among fish assemblages between ICOLLs. (Species that contributed up to 90% of the dissimilarity between sampling times are shown). Time 1 ICOLLs Cockrone Terrigal Avoca Acanthopagrus australis Philypnodon grandiceps Atherinosoma microstoma Terrigal Acanthopagrus australis Philypnodon grandiceps Wamberal Acanthopagrus australis Atherinosoma microstoma Philypnodon grandiceps Atherinosoma microstoma Time 2 Cockrone Avoca Terrigal Avoca Acanthopagrus australis Philypnodon grandiceps Atherinosoma microstoma Terrigal Acanthopagrus australis Philypnodon grandiceps Wamberal Acanthopagrus australis Atherinosoma microstoma Atherinosoma microstoma Philypnodon grandiceps Hyporhamphus regularis Atherinosoma microstoma Time 4 Cockrone Wamberal Acanthopagrus australis Philypnodon grandiceps

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Table 5.8. continued… Time 5 Cockrone Avoca Terrigal Terrigal Acanthopagrus australis Acanthopagrus australis Wamberal Acanthopagrus australis Atherinosoma microstoma Atherinosoma microstoma Atherinosoma microstoma Acanthopagrus australis Time 6 Cockrone Avoca Terrigal Avoca Acanthopagrus australis Terrigal Acanthopagrus australis Wamberal Philypnodon grandiceps Atherinosoma microstoma Atherinosoma microstoma Atherinosoma microstoma Philypnodon grandiceps Hyporhamphus regularis Hyporhamphus regularis Time 7 Cockrone Avoca Terrigal Wamberal Atherinosoma microstoma Atherinosoma microstoma Atherinosoma microstoma Philypnodon grandiceps Time 8 Cockrone Wamberal Philypnodon grandiceps

5.3.3.2 Univariate analysis-seine net samples The mean number of species and the mean total number of individuals showed significant Time x Site(ICOLL) and Time x ICOLL interactions (Table 5.9). Mean number of species varied significantly among sites in Cockrone Lagoon at sampling times 1, 2, 4, 7 and 8, in Avoca Lagoon at sampling times 1, 2 and 4, in Terrigal Lagoon at sampling times 2, 3, 5 and 7, and in Wamberal Lagoon only at sampling time 7. Mean number of individuals varied significantly among in Cockrone Lagoon at sampling times 1, 2, 4, 7 and 8, in Avoca Lagoon at sampling times 1, 2, 5 and 6, in Terrigal Lagoon at sampling times 1-7, and in Wamberal Lagoon at sampling times 1, 2, 6 and 7.

Mean number of species varied significantly among ICOLLs between Cockrone and Avoca Lagoons and between Wamberal and Terrigal Lagoons sampling times 2-4 and 6-8. At sampling times 2-4 assemblages differed between Avoca and Terrigal Lagoons, and between Wamberal and Terrigal Lagoons. Mean number of individuals varied significantly among ICOLLs between Cockrone and Avoca Lagoons and between Wamberal and Terrigal Lagoons at sampling times 1, 3, 4, 6 and 7. At sampling time 3 assemblages differed between Avoca and Terrigal Lagoons and between Wamberal and Terrigal Lagoons.

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Table 5.9. Summary of results of 3-factor univariate PERMANOVA testing for differences in the mean number of species and mean total number of individuals collected by seine nets. Data was square-root transformed. Mean number of species Mean number of individuals Source df MS Pseudo-f p MS Pseudo-f p ICOLLs 3 9.97 2.65 0.02 84.85 0.77 0.67 Time 7 16.04 40.69 0.0001 280.14 15.13 0.0001 Site(ICOLL) 15 0.99 2.51 0.003 77.47 4.18 0.0001 Time x ICOLL 21 2.91 7.39 0.0001 57.26 3.09 0.0001 Time x Site(ICOLL) 105 0.39 2.50 0.0001 18.52 2.98 0.0001 Res 304 0.16 6.21

PERMDISP for Time x Site(ICOLL) was significant (F=5.21, df=151, p=0.0001) for the mean number of species and for the mean total number of individuals (F=5.12, df=151, p=0.0005). Pairwise analysis of dispersion for mean number of species showed significant differences for Cockrone Lagoon at sampling times 3, 4 and 6-8, in Avoca Lagoon at sampling times 1-5 and 7 and 8. At sampling times 1, 3, 4 and 8 mean number of species showed significant differences at Terrigal Lagoon, and in Wamberal Lagoon at sampling times 1-3, and 6-8.

PERMDISP for Time x ICOLL was significant (F=6.63, df=31, p=0.0001) for the mean number of species and the mean total number of individuals (F=7.36, df=31, p=0.0001). Pairwise analysis of dispersion for the mean number of species showed that there were significant differences in variability of ICOLLs at different times. Cockrone and Avoca Lagoons were significantly different at sampling times 1-3 and 8, and between Cockrone and Wamberal lagoons at sampling times 3, 4 and 8, and between Cockrone and Terrigal Lagoons at sampling times 2, 3, 5, 6 and 8. At sampling times 1-3 and 8 the mean number of species differed between Avoca and Wamberal Lagoons, and between Avoca and Terrigal Lagoons at sampling times 1, 3, 5 and 8, and between Wamberal and Terrigal Lagoons at sampling times 1-3, 5, 6 and 8.

5.3.3.3 Multivariate analysis–multi-panel gill net samples Spatial and temporal variability of fish assemblages were significant for the factors Time x Site (ICOLL) and Time x ICOLL (Table 5.10), therefore both significant variations were further investigated using pairwise tests in PERMANOVA. The significant Time x Site(ICOLL) interaction occurred because patterns of variation among sites in fish assemblages changed through time in different ways in the four ICOLLs. Fish assemblages in Cockrone Lagoon varied significantly among all sites at sampling times 1 and 2; at Avoca Lagoon at sampling times 1, 2, 5, 7 and 8; at Terrigal Lagoon at sampling times 1, 2 and 5-7 and at Wamberal Lagoon at sampling times 1 and 4-8. The significant Time x ICOLL interaction occurred

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because fish assemblages of Cockrone and Avoca Lagoons, and of Wamberal and Terrigal Lagoons significantly differed at sampling times 4-6 and 8, and assemblages of Avoca and Wamberal Lagoons significantly differed at sampling time 6, and assemblages of Avoca and Terrigal Lagoons and Wamberal and Terrigal Lagoons, differed at sampling times 1 and 4. No significant differences in assemblages were found between ICOLLs at sampling times 2 and 7.

Table 5.10. Summary of 3-factor PERMANOVA testing for differences in the fish assemblages of ICOLLs collected by multi-panel gill nets. Data was square-root transformed. Source df MS Pseudo-f p Time 7 7308 6.58 0.0001 ICOLL 3 14776 2.71 0.0005 Site (ICOLL) 15 3901 3.51 0.0001 Time x ICOLL 21 1967 1.77 0.001 Time x Site (ICOLL) 105 1110 1.89 0.0001 Res 304 586.84

PERMDISP for Time x Site(ICOLL) was significant (F=7.85, df=151, p=0.0001) and occurred because sites at each ICOLL differed in their variability at different sampling times. Cockrone Lagoon differed in variability at three sampling times (sampling times 1-3); Avoca Lagoon differed in variability at one sampling time (sampling time 2); Terrigal Lagoon differed in variability at two sampling times (sampling time 2 and 4); and Wamberal Lagoons differed in variability at four sampling times (sampling time 1, 2, 4, and 5).

PERMDISP for Time x ICOLL was significant (F=8.84, df=31, p=0.0001) was significant and occurred because the pairwise patterns of differences in variability between ICOLLs were not consistent at each sampling time. Cockrone and Wamberal Lagoons and Cockrone and Terrigal Lagoons were significantly different at sampling times 3-6, and between Avoca and Wamberal Lagoons at sampling times 1, 3 and 5, and between Avoca and Terrigal Lagoons at sampling times 1, 2 and 6, and between Wamberal and Terrigal Lagoons at sampling times 2 and 3.

The MDS plots illustrate the variability of fish assemblages where the distances between points indicate dissimilarity (Figure 5.20). Cockrone Lagoon showed some groupings of sites within the sampling period, especially at sampling times 1 and 2. In comparison Avoca, Terrigal and Wamberal Lagoons showed no discernible patterns.

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Cockrone Lagoon Avoca Lagoon 2D Stress: 0.06 2D Stress: 0.13

Terrigal Lagoon Wamberal Lagoon 2D Stress: 0.15 2D Stress: 0.07

SIMPER analysis of the Time x Site (ICOLL) interaction found differences in fish assemblages among sites at sampling times 1 and 2 at Cockrone Lagoon, and sampling times 1, 2, 5 and 8 at Avoca Lagoon, and sampling times 1, 2, and 5-7 at Terrigal Lagoon, and at sampling times 1 and 4-8 at Wamberal Lagoon (Table 5.11).

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Table 5.11. Summary of SIMPER results showing fish species responsible for temporal differences among sites in fish assemblages at each ICOLL. Species that contributed up to 90% of the dissimilarity between sampling times are shown. Cockrone Lagoon Time 1 Time 2 Acanthopagrus australis Myxus elongatus Myxus elongatus Mugil cephalus Avoca Lagoon Time 1 Time 2 Time 5 Time 8 Mugil cephalus Mugil cephalus Mugil cephalus Mugil cephalus H. castelnaui Myxus elongatus Terrigal Lagoon Time 1 Time 2 Time 5 Time 6 Time 7 Myxus elongatus Myxus elongatus Mugil cephalus Myxus elongatus Mugil cephalus Mugil cephalus Mugil cephalus Mugil cephalus Gerres subfasciatus Gerres subfasciatus Gerres subfasciatus Gerres subfasciatus Sillago ciliata Platycephalus fuscus Wamberal Lagoon Time 1 Time 4 Time 5 Time 6 Time 7 Time 8 Mugil cephalus Mugil cephalus Mugil cephalus Mugil cephalus Mugil cephalus Mugil cephalus Myxus elongatus Myxus elongatus Myxus elongatus

SIMPER analysis for differences among ICOLLs found that fish assemblages differed between Terrigal and Avoca Lagoons due to differences in abundances of Myxus elongatus and Sillago ciliata, and between Terrigal and Wamberal Lagoons due to differences in S. ciliata at sampling time 1. Differences among ICOLLs in abundances of Mugil cephalus were responsible for differences in assemblages between Cockrone and Avoca Lagoons and between Terrigal and Wamberal Lagoons at sampling time 3. Differences among ICOLLs in abundances of M. cephalus were responsible for differences in assemblages between Cockrone and Terrigal Lagoons, between Cockrone and Wamberal Lagoons and between Terrigal and Wamberal Lagoons at sampling time 4. Differences among ICOLLs in abundances of M. cephalus were responsible for differences in assemblages between Cockrone and Avoca Lagoons, between Avoca and Wamberal Lagoons and between Terrigal and Wamberal Lagoons at sampling time 6. Differences among ICOLLs in abundances of M. cephalus were responsible for differences in assemblages between Cockrone and Avoca Lagoons at sampling times 7 and 8.

5.3.3.4 Univariate analysis–multi-panel gill net samples Mean number of species and the mean total number of individuals showed significant Time x Site(ICOLL) interactions, however only the mean number of species showed significant Time x ICOLL interactions (Table 5.12). Mean number of species varied significantly among sites in

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Cockrone Lagoon at sampling times 1, 2 and 7, in Avoca Lagoon at sampling times 1, 2 and 6- 8, in Terrigal Lagoon at sampling times 2 and 5, and in Wamberal Lagoon at sampling times 2-6 and 8. Mean number of individuals varied significantly in Cockrone Lagoon at sampling times 1 and 2, in Avoca Lagoon at sampling times 1, 2 and 5-8, in Terrigal Lagoon at sampling times 2, 5 and 6, and in Wamberal Lagoon at sampling times 1, 4, 5, 7-8.

Mean number of species varied significantly between ICOLLs of Cockrone and Avoca Lagoons at sampling times 5-8, and between Cockrone and Wamberal Lagoons at sampling times 6 and 7, and between Cockrone and Terrigal Lagoons at sampling times 4-7. At sampling time 4, the mean number of species varied significantly between Avoca and Terrigal Lagoons at sampling time 4, and between Wamberal and Terrigal Lagoons at sampling times 1, 4 and 6.

Table 5.12. Summary of 3-factor univariate PERMANOVA testing for differences in the mean number of species and mean total number of individuals collected by multi-panel gill nets. Data was square-root transformed. Mean number of species Mean total number of individuals Source df MS Pseudo-f p MS Pseudo-f p Time 7 4.48 13.82 0.0001 17.31 9.35 0.0001 ICOLL 3 8.31 4.51 0.001 18.53 2.08 0.05 Site(ICOLL) 15 1.14 3.52 0.0002 6.89 3.72 0.0001 Time x ICOLL 21 0.77 2.39 0.002 2.90 1.57 0.07 Time x Site(ICOLL) 105 0.32 1.59 0.001 1.85 2.52 0.0001 Res 304 0.20 0.73

PERMDISP for Time x Site(ICOLL) was significant (F=6.33, df=151, p=0.0001) for the mean number of species and for the mean total number of individuals (F=4.09, df=151, p=0.0001) and occurred because sites at each ICOLL differed in their variability at different sampling times. Cockrone Lagoon differed in variability at five sampling times (sampling times 3-5, 6 and 8); Avoca Lagoon differed in variability at five sampling times (sampling times 1-4 and 6); Terrigal Lagoon differed in variability at three sampling times (sampling time 2, 6 and 7); and Wamberal Lagoons differed in variability at five sampling times (sampling time 1, 4, 5, 7 and 8). Mean total number of individuals varied significantly in Cockrone Lagoon at sampling times 1-8, in Avoca Lagoon at sampling times 3 and 4, in Wamberal Lagoon at sampling times 4, 5 and 8. No significant differences in the mean total number of individuals were found at Terrigal Lagoon at any sampling time.

PERMDISP for Time x ICOLL was significant (F=4.11, df=31, p=0.0001) for the mean number of species. Pairwise analysis of dispersion for the mean number of species showed that there

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were significant differences in variability ICOLLs at different times. Cockrone and Avoca Lagoons and between Cockrone and Wamberal Lagoons were significantly different at sampling times 4 and 5, and between Cockrone and Terrigal Lagoons at sampling times 3, 4 and 7. At sampling time 6 the mean number of species differed between Avoca and Wamberal Lagoons, and between Avoca and Terrigal Lagoons at sampling time 8, and between Wamberal and Terrigal Lagoons at sampling times 3.

5.3.4 Comparison of environmental factors structuring fish assemblages of ICOLLs

5.3.4.1 Environmental variables Graphical representations of salinity, water temperature, turbidity, dissolved oxygen and algal biomass in each ICOLL are shown at the end of this chapter (Appendix 2a-d). Salinity was generally higher at Terrigal, Avoca and Cockrone Lagoons (generally higher than 15 ppt) compared with Wamberal Lagoon (mostly lower than 15 ppt). Salinity was similar at each site within each ICOLL, and in most cases increased at each site after barriers was opened. Water temperatures in the four ICOLLs were generally similar to each other and followed seasonal trends that were not influenced by barrier openings. Temperatures greater than 25°C occurred during November 2009 and January and March 2010. Water temperatures below 15°C occurred in July 2009 and June 2010.

Turbidity was greater in Terrigal Lagoon compared to the other ICOLLs, with values generally greater than 10 ntu. The other three ICOLLs had turbidity’s that were lower than 10 ntu, except for some spiking that occurred in Avoca Lagoon. Variation in turbidity among sites within ICOLLs was generally related to differences in the presence of aquatic vegetation, and in some cases turbidity increased after barriers were opened. Dissolved oxygen for each ICOLL was generally lower during the warmer months (from November 2009 to March 2010), being less than 5 mg/L. During April to July 2009, dissolved oxygen increased to greater than 10 mg/L. In some cases dissolved oxygen increased or decreased after barrier openings, and readings were similar for most sites within each ICOLL.

Algal biomass was greater in Cockrone Lagoon than in Avoca and Wamberal Lagoons, and in Terrigal Lagoon, in which no algae was collected throughout the study. In all cases no algae was collected during the sampling period after the barrier had opened (July 2009). Also, no algae was collected from site 1 near the entrance mainly due to its sandy substrate; however sites further away from the entrance generally had a higher algal biomass.

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5.3.4.2 Influence of environmental variables on seine net fish assemblages Environmental variables structuring seine net fish assemblages were identified using the BEST procedure and AIC selection in DISTLM (Table 5.13). Five variables were identified for Cockrone Lagoon, two variables for Avoca Lagoon, four variables for Terrigal Lagoon, and five variables for Wamberal Lagoon. The five variables selected for Cockrone Lagoon explained 62.49% of the total assemblage variation, with salinity explaining the greatest variation (31.74%), followed by water temperature (17.06%), percentage algal cover (7.7%) and algal mass (4.61%) and ≥1 mm percentage sediment grain size (1.38%). In comparison, the two variables selected for Avoca Lagoon explained 35.69% of the total assemblage variation, with water temperature explaining the greatest variation (23.91%), followed by percentage forest catchment cover (11.78%). The four variables selected for Terrigal Lagoon explained 50.87% of the total assemblage variation, with temperature explaining the greatest variation (22.03%), followed by percentage bare substrate (13.62%), distance from the barrier (10.49%) and >0.5 mm percentage sediment grain size (4.73%). The five variables selected for Wamberal Lagoon explained 64.97% of the total assemblage variation, with salinity explaining the greatest variation (27.25%), followed by the barrier status (23.20%), algal mass (8.98%) and percentage sediment grain sizes >0.5 mm (5.38%) and >63 µm (0.16%).

The influence of each variable on the structuring of fish assemblages was visualised by overlaying vectors in dbRDA (Figure 5.21). Axis 1 of Cockrone Lagoon dbRDA plot explained 51.8% of the fitted variation and 31.7% of the total variation. Axis 2 of the dbRDA plot explained 27.3% of the fitted variation and 17.1% of the total variation. In comparison, Axis 1 of Avoca Lagoon dbRDA plot explained 67% of the fitted variation and 23.9% of the total variation. Axis 2 of the dbRDA plot explained 33% of the fitted variation and 11.8% of the total variation. Terrigal Lagoon axis 1 of the dbRDA plot explained 43.3% of the fitted variation and 22% of the total variation. Axis 2 of the dbRDA plot explained 26.8% of the fitted variation and 13.6% of the total variation. Axis 1 of Wamberal Lagoon plot explained 41.9% of the fitted variation and 27.3% of the total variation. Axis 2 of the dbRDA plot explained 35.7% of the fitted variation and 23.2% of the total variation.

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Table 5.13. Results of distance-based multivariate linear model (DISTLM) for environmental variables for Cockrone, Avoca, Terrigal and Wamberal Lagoons that is the BEST predictor of temporal and spatial variation in seine net fish assemblages. The relative importance of each variable in the model linking these three variables to assemblage variation (fitted model) and the relative importance of each variable to the total variation in fish assemblages are shown. % Explained variation % Explained variation (fitted model) (total variation) Individual Cumulative Individual Cumulative Axis Cockrone Lagoon Salinity 50.8 50.8 31.74 31.74 Water temperature 27.3 78.1 17.06 48.81 % Algae cover 12.32 90.42 7.7 56.51 Algal mass 7.37 97.79 4.61 61.11 ≥1mm % sediment grain size 2.21 100 1.38 62.49 Avoca Lagoon Water temperature 67 67 23.91 23.91 % Forest 33 100 11.78 35.69 Terrigal Lagoon Temperature 43.31 43.31 22.03 22.03 % Bare substrate 26.76 70.07 13.62 35.65 Distance from barrier 20.63 90.7 10.49 46.14 >0.5mm % sediment grain size 9.3 100 4.73 50.87 Wamberal Lagoon Salinity 41.95 41.95 27.25 27.25 Barrier 35.71 77.66 23.2 50.45 Algal mass 13.82 91.48 8.98 59.43 >0.5mm % sediment grain size 8.28 99.76 5.38 64.81 >63 µm % sediment grain size 0.24 100 0.16 64.97

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Cockrone Lagoon Avoca Lagoon

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b d d -40 -50 -40 -20 0 20 40 -50 0 50 100 dbRDA1 (43.3% of fitted, 22% of total variation) dbRDA1 (41.9% of fitted, 27.3% of total variation) Figure 5.21. dbRDA ordination plots showing the spatial and temporal variation of fish assemblages collected using seine nets in Cockrone, Avoca, Terrigal and Wamberal Lagoons overlaid with the vectors of the environmental variables that explained significant amounts of variation in the assemblages. Vectors represent the direction and magnitude of the Pearson correlation of each variable with the dbRDA axes. The different symbols represent different sampling times, and the replicate symbols represent the different sites at each time. Sampling times are represented by: ▲T1, ▼T2, ■T3, ♦T4, ●T5, +T6, ΔT7, ΟT8. Sal= salinity, Temp = water temperature, Dist= distance from barrier, % Bare= % bare substrate and Algae=% cover.

Each variable is represented by Pearson correlation of selected environmental variables that are represented on each dbRDA axis (Table 5.14). For Cockrone Lagoon the first dbRDA axis was highly positively correlated with water temperature (0.78) and the second axis was highly negatively correlated with salinity (-0.81). The first dbRDA axis of Avoca Lagoon was highly positively correlated with water temperature (0.92) and the second was highly negatively correlated with percentage forest catchment cover (-0.92). The first dbRDA axis for Terrigal Lagoon was highly positively correlated with distance from the barrier (0.72) and the second axis was positively correlated with percentage sediment grain size >0.5 mm (0.68). For Wamberal Lagoon the first dbRDA axis was negatively correlated with the barrier status

178 Chapter 5: Factors influencing fish assemblages

(closed -0.62) and (open 0.62) and the second axis was highly negatively correlated with salinity (-0.83).

Table 5.14. Values of Pearson correlations of selected environmental variables with each of the dbRDA axes for Cockrone, Avoca, Terrigal and Wamberal Lagoons. Cockrone Lagoon Axes Salinity (ppt) Water % Algae Algal mass ≥ 1mm % sediment temperature (g) grain size (°C) dbRDA 1 0.46 0.78 0.25 -0.15 0.31 dbRDA 2 -0.81 0.39 0.41 0.004 -0.12 dbRDA 3 -0.10 -0.41 0.38 -0.51 0.65 dbRDA 4 -0.32 0.20 -0.65 0.22 0.62 dbRDA 5 0.11 -0.17 0.45 0.82 0.29 Avoca Lagoon Axes Temperature % Forest (°C) cover dbRDA 1 0.92 -0.40 dbRDA 2 -0.40 -0.92 Terrigal Lagoon Axes Temperature % Bare Distance from >0.5 mm % sediment grain size (°C) substrate barrier dbRDA 1 0.31 0.62 0.72 -0.03 dbRDA 2 0.50 0.31 -0.44 0.68 dbRDA 3 0.80 -0.50 0.06 -0.32 dbRDA 4 -0.10 -0.53 0.53 0.66 Wamberal Lagoon Axes Salinity (ppt) Barrier Barrier open Algal mass >0.5 mm >63 µm % closed (g) % sediment sediment grain size grain size dbRDA 1 0.28 -0.62 0.62 -0.32 -0.18 0.12 dbRDA 2 -0.83 -0.14 0.14 0.002 -0.47 -0.21 dbRDA 3 -0.47 -0.15 0.15 -0.08 0.71 0.47 dbRDA 4 -0.06 0.15 -0.15 -0.88 0.17 -0.37 dbRDA 5 0.01 -0.22 0.22 0.33 0.46 -0.76

179 Chapter 5: Factors influencing fish assemblages

5.3.4.3 Influence of environmental variables on multi-panel gill net fish assemblages Environmental variables were identified using the BEST procedure and AIC selection in DISTLM for all ICOLLs (Table 5.15). Three variables were identified for Cockrone Lagoon, four variables for Avoca Lagoon, three variables for Terrigal Lagoon and four variables for Wamberal Lagoon. The three variables selected for Cockrone Lagoon explained 51.9% of the total assemblage variation, with salinity explaining the greatest variation (41.99%), followed by temperature (6.22%) and <63 µm percentage sediment grain size (3.69%). In comparison, the four variables selected for Avoca Lagoon explained 24.57% of the total assemblage variation, with salinity explaining the greatest variation (16.06%), followed by percentage forest catchment cover (5.07%) and percentage sediment grain size (>63 and >0.5 mm) explaining a total of 3.44%. The three variables selected for Terrigal Lagoon explained 41.93% of the total assemblage variation, with temperature explaining the greatest variation (32.82%), followed by percentage sediment grain size of >63 µm (6.65%) and sediment grain size of <63 µm (2.47%). The four variables selected for Wamberal Lagoon explained 43.47% of the total assemblage variation, with percentage sediment grain size of >212 µm explaining the greatest variation (37.06%), followed by the barrier status (4.59%), percentage forest cover (1.86%) and percentage bare substrate (-0.04%).

The influence of each variable on the structuring of assemblages for all the ICOLLs was visualised by overlaying vectors in dbRDA (Figure 5.22). Axis 1 of Cockrone Lagoon dbRDA plot explained 80.9% of the fitted variation and 42% of the total variation. Axis 2 of the dbRDA plot explained 12% of the fitted variation and 6.2% of the total variation. In comparison, Axis 1 of Avoca Lagoon dbRDA plot explained 65.4% of the fitted variation and 16.1% of the total variation. Axis 2 of the dbRDA plot explained 20.6% of the fitted variation and 5.1% of the total variation. Terrigal Lagoon axis 1 of the dbRDA plot explained 78.3% of the fitted variation and 32.8% of the total variation with axis 2 of the dbRDA plot explaining 15.8% of the fitted variation and 6.6% of the total variation. Axis 1 of Wamberal Lagoon dbRDA plot explained 85.3% of the fitted variation and 37.1% of the total variation with axis 2 of the dbRDA plot explaining 10.5% of the fitted variation and 4.6% of the total variation.

180 Chapter 5: Factors influencing fish assemblages

Table 5.15. Results of distance-based multivariate linear model (DISTLM) for environmental variables for Cockrone, Avoca, Terrigal and Wamberal Lagoons that are the BEST predictors of temporal and spatial variation in multi-panel gill net fish assemblages. The relative importance of each variable in the model linking these three variables to assemblage variation (fitted model) and the relative importance of each variable to the total variation in fish assemblages are shown. % Explained variation % Explained variation (fitted model) (total variation) Individual Cumulative Individual Cumulative Axis Cockrone Lagoon Salinity 80.9 80.9 41.99 41.99 Water temperature 11.99 92.89 6.22 48.21 <63 µm % sediment grain size 7.11 100 3.69 51.9 Avoca Lagoon Salinity 65.35 65.35 16.06 16.06 % Forest cover 20.62 85.97 5.07 21.12 >63 µm % sediment grain size 8.43 94.4 2.07 23.20 >0.5 mm % sediment grain size 5.60 100 1.37 24.57 Terrigal Lagoon Water temperature 78.27 78.27 32.82 32.82 >63 µm % sediment grain size 15.85 94.12 6.65 39.47 <63 µm % sediment grain size 5.88 100 2.47 41.93 Wamberal Lagoon >212 µm % sediment grain size 85.27 85.27 37.06 37.06 Barrier status 10.55 95.82 4.59 41.65 % Forest cover 4.27 100.09 1.86 43.5 % Bare substrate -0.09 100 -0.04 43.47

181 Chapter 5: Factors influencing fish assemblages

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b b d d -40 -20 -40 -20 0 20 40 -20 0 20 40 dbRDA1 (78.3% of fitted, 32.8% of total variation) dbRDA1 (85.3% of fitted, 37.1% of total variation) Figure 5.22. dbRDA ordination plots showing the spatial and temporal variation of fish assemblages collected using multi-panel gill nets in Cockrone, Avoca, Terrigal and Wamberal Lagoons overlaid with the vectors of the environmental variables that explained significant amo unts of variation in the assemblages. Vectors represent the direction and magnitude of the Pearson correlation of each variable with the dbRDA axes. The different symbols represent different sampling times, and the replicate symbols represent the different sites at each time. Sampling times are represented by: ▲T1, ▼T2, ■T3, ♦T4, ●T5, +T6, ΔT7, ΟT8. Sal=salinity, Temp=water temperature, Dist=distance from barrier, %Bare=bare substrate.

Each variable is represented by Pearson correlation of selected environmental variables that are represented on each dbRDA axes (Table 5.16). For Cockrone Lagoon the first dbRDA axes was highly positively correlated with water temperature (0.89) and the second axis was highly negatively correlated with salinity (-0.91). The first dbRDA axis of Avoca Lagoon was highly negatively correlated with percentage forest cover (-0.92) and the second axis was highly positively correlated with salinity (0.82). For Terrigal Lagoon the first dbRDA axis was highly positively correlated with percentage sediment grain size of >63 µm (0.92) and the second axis were highly positively correlated with water temperature (0.80). The first dbRDA axis of Wamberal Lagoon was highly positively correlated with percentage sediment grain size of >212

182 Chapter 5: Factors influencing fish assemblages

µm (0.89) and the second axis were positively and negatively correlated with the barrier status (closed 0.51) and open (-051).

Table 5.16. Values of Pearson correlations of selected environmental variables with each of the dbRDA axes for Cockrone, Avoca, Terrigal and Wamberal Lagoons. Cockrone Lagoon Axes Salinity (ppt) Water temperature <63 µm sediment grain size (°C) dbRDA 1 0.23 0.89 0.39 dbRDA 2 -0.91 0.34 -0.22 dbRDA 3 0.33 0.31 -0.89 Avoca Lagoon Axes Salinity (ppt) % Forest cover >63 µm % >0.5 mm % sediment grain size sediment grain size dbRDA 1 -0.11 -0.92 -0.28 0.23 dbRDA 2 0.82 -0.04 -0.47 -0.30 dbRDA 3 -0.49 -0.04 -0.34 -0.80 dbRDA 4 0.25 -0.38 0.76 -0.46 Terrigal Lagoon Axes Water >63 µm % sediment < 63 µm % sediment grain size temperature (°C) grain size dbRDA 1 -0.16 0.92 -0.35 dbRDA 2 0.80 0.33 0.51 dbRDA 3 0.58 -0.20 -0.79 Wamberal Lagoon Axes >212 µm % Barrier closed Barrier open % Forest % Bare substrate sediment grain cover size dbRDA 1 0.89 0.21 -0.21 -0.17 0.30 dbRDA 2 -0.44 0.51 -0.51 -0.37 0.37 dbRDA 3 -0.05 0.12 -0.12 0.87 0.46 dbRDA 4 0.11 0.42 -0.42 0.29 -0.75

5.4 Discussion

5.4.1 Overview of fish assemblages in Central Coast ICOLLs This study has shown that fish assemblages varied among the four Central Coast ICOLLs and among sites within each ICOLL, and it also showed similarities in assemblages to other south- eastern Australian ICOLLs located along the NSW coastline (Pollard 1994b; Griffiths 2001; Jones and West 2005). Many ICOLLs are often subjected to the effects associated with artificial barrier openings, however, variations of fish assemblages within the current study were not

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directly influenced by barrier openings, but more with the indirect effects such as changing environmental factors along with the sampling methods and the bimonthly sampling design. A total of 14 764 fishes representing 35 species from 25 families were collected during the study. Seine and multi-panel gill nets were used to target different sizes and species of fishes (Gonzales et al. 2009). These methods are effective when sampling shallow water habitats (Gray et al. 2005; Rotherham et al. 2006). Although the numbers of species caught were generally low, seine netting sampled more species and more fishes than the multi-panel gill nets.

At Avoca and Wamberal Lagoons, Atherinosoma microstoma was the numerically most abundant species (1 702 and 5 666 individuals respectively). The life history of A. microstoma suggests that it is a resident R (resident) species which is also commonly found in high abundances at other ICOLLs (Molsher et al. 1994). Atherinids are generally highly abundant in ICOLLs, with new recruits hatching 5-7 days after eggs are laid, generally from September to October, with abundances thus peaking around November. Atherinids are generally annual species which die shortly after breeding, and therefore adult numbers can decrease dramatically in ICOLLs (Potter et. al. 1986). The success of atherinids is attributed to their ability to tolerate environmental variations, especially changes in salinity (Molsher et al. 1994). Ambassis jacksoniensis is somewhat similar to the atherinids in being a small fish that was present in high numbers at Terrigal Lagoon (n=475 individuals). This species can also complete its entire lifecycle within ICOLLs. Generally, ambassids spawn during autumn and tolerate a wide range of salinities (Miskiewicz 1987). ICOLLs are also nursery areas for many species of fishes including the mugilid Myxus elongatus, which was also found in high numbers at Terrigal Lagoon at various stages throughout the study. Another species present mainly as juveniles, the sparid Acanthopagrus australis, was numerically dominant at Cockrone Lagoon (n=1 532 individuals). Sparids generally enter ICOLLs after barrier openings to utilise these environments as nursery areas (Griffiths 1999, 2001b). High abundances of A. australis were also collected at Avoca Lagoon, which suggests that both of these ICOLLs may be important nursery areas for this species.

The majority of fishes collected using multi-panel gill nets were mugilids, mainly Mugil cephalus and Myxus elongatus. At Cockrone, Avoca and Wamberal Lagoons, Mugil cephalus was the numerically dominant species (n=136, 315 and 176 individuals, respectively), and Myxus elongatus was the dominant species (n=209 individuals) at Terrigal Lagoon. Sea mullet generally leave ICOLLs to spawn in the open ocean (Waltham et al. 2013). In most cases ICOLLs have limited connection to the sea, restricting this movement; however, many ICOLLs have suitable habitats and resources able to sustain sea mullet, and along with their ability to adapt to changing salinities, these mullets are able to remain in ICOLLs for very long periods

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(Griffiths 1998). In the current study sea mullet were generally collected in the shallow upper reaches and observed in creeks where substrates have high organic content and generally lack aquatic vegetation, especially when water depth was extremely low due to barrier openings (personal observation). Myxus elongatus is similar to other mullets in that they are associated with bare substrates, hence the high abundances collected in Terrigal Lagoon, with increased abundances being associated with barrier openings (Griffiths 1998).

5.4.2 Diversity of fishes in Central Coast ICOLLs The species richness of fishes among ICOLLs of the Central Coast differed and in most cases was low. Terrigal Lagoon had the most diverse assemblage, with 29 species, while Wamberal Lagoon had the lowest number, with 13 species. Both Cockrone and Avoca lagoons had similar numbers of species, with 18 and 19 species being collected, respectively. The high species diversity associated with Terrigal Lagoon may be due to the high frequency of barrier openings. A relatively small number of species present is generally associated with ICOLLs that have similar catchment areas to this study, along with the frequency of barrier openings (Griffiths and West 1999; Becker and Laurenson 2008). In the current study, small fishes <100 mm TL, including ambassids, atherinids, eleotrids and gobiids, along with juvenile mugilids and sparids, dominated seine net hauls in these ICOLLs. Seine net hauls were also dominated by hemiramphids at various stages of the study. In most cases these ICOLLs were generally dominated by one species, except for gobiids and juvenile mugilids, which were more diverse (Table 5.5).

In comparison, species richness of larger mobile fishes (>100 mm) collected by multi-panel gill nets was generally low, with the majority of fishes collected being Mugil cephalus and Myxus elongatus. However, Acanthopagrus australis and Rhabdosargus sarba (Sparidae), Sillago ciliata (Sillangidae), Gerres subfasciatus (Gerreidae) and Platycephalus fuscus (Platycephalidae) were also collected periodically throughout the study (Table 5.5). One unusual species collected in this study, which has not been documented before in ICOLLs of a similar size, was the Port Jackson shark (Heterodontus portusjacksoni). The Port Jackson shark was caught in Terrigal Lagoon after the barrier had been opened, and after measuring the TL of the shark it was released, but was not recaptured in any subsequent sampling periods, even though the barrier had closed. The Port Jackson shark is not known to be a normal resident in ICOLLs (Kuiter 2000). The diversity of species described above can be associated with barrier openings as many of these species enter and exit ICOLLs when barriers are open.

Species richness has also been previously associated with various factors such as salinity (Young et al. 1997; Griffiths 2001a), size of the estuary (Griffiths and West 1999; Becker and

185 Chapter 5: Factors influencing fish assemblages

Laurenson 2008), presence of seagrasses (Robinson et al. 1983; Allan et al. 1985; Pollard 1994a; Griffiths 2001c; Jones and West 2005) and the status of the barrier (Vorwerk et al. 2003).

The collection methods used in this study are effective in providing a sufficiently representative sample of fishes in these environments; however, sampling failures can occur that can influence species richness. Common such failings might include net avoidance when turbidity is low, small fishes passing through the mesh, fish escaping by jumping out of the net, along with fishes being missed when sorting through thick algae and weed collected by the net (Rozas and Minello 1997, Gonzales et al. 2009). Also, the sampling design can influence the abundance and number of species collected. For example, as discussed in Chapter 4, bimonthly sampling does not account for any seasonal variations that may occur.

All of the dominant species collected by either method are common to many NSW ICOLLs (Griffiths 1998, 1999; Jones and West 2005); however, most of the species found within Central Coast ICOLLs were either juveniles, such as Acanthopagrus australis, or species that can spend their entire lifecycle in ICOLLs, including Atherinosma microstoma and Ambassis jacksoniensis. This suggests that Central Coast ICOLLs are not only important nursery areas, but for some species they may also be self-recruiting. Comparisons of the species collected throughout this study to the study of the larval and juvenile fish assemblages within the ICOLLs (Chapter 4) show that the dominant species in both studies were similar, and since no change in assemblages occurred over time, this may indicate that these ICOLLs are suitable habitats for a variety of life history stages of A. australis, A. microstoma and A. jacksoniensis.

5.4.3 Comparison of fish assemblages in ICOLLs Many of the published studies compare the fish assemblages of intermittently opening to permanently open estuaries (Pollard 1994b; Griffiths 1999; Jones and West 2005), however comparative studies on similar sized ICOLLs are generally limited. A previous study of Gosford Lagoons by Weate and Hutchings (1977) documented 7 species from Cockrone Lagoon, 6 species from Avoca Lagoon, 1 species from Terrigal Lagoon and 2 species from Wamberal Lagoon. The number of species collected was much lower compared with the current study; however, abundances were high, with similar species being collected, including Atherinosoma microstoma, Mugil cephalus and Acanthopagrus australis. It is difficult to make comparisons with the previous study as it is not understood how and if the fishes documented there were sampled by the authors.

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Fish assemblages of the same Central Coast ICOLLs were previously studied during 1986-1988 (Pollard, unpublished data NSW Fisheries Research Institute), which found somewhat different results compared to the current study. Pollard found that Terrigal Lagoon had a greater number of species (n=27) and abundance (n=4 206) compared to the other three ICOLLs. The current study also found that Terrigal Lagoon had the greatest number of species (n=29), but Wamberal Lagoon had the greater abundances (6 298). Overall, the species found in Pollard’s study were basically similar to those found in the current study, with the exception of a few species including Achoerodus viridis (eastern blue groper), and Chelidonichthys kumu (red gunard). It appears that this previous study may have targeted larger species, as no small fish such as atherinids, gobiids, and ambassids were collected compared to the current study, in which these fishes were numerically dominant. Pollard’s methods also varied in using seine and multi-panel gill nets, but also beam trawls and rotenone poisoning, all of which are designed to collect a variety of species.

Other NSW ICOLLs also demonstrated similar fish faunas to the current study, with additional species there including Australian salmon (Arripididae), trevally (Carangidae), luderick (Girellidae), batfish (Monodactylidae), estuary perch (Percichthyidae) and tailor (Pomatomidae), all of which have been documented by Pollard (1994b), Griffiths (1999) and Jones and West (2005). Griffiths (1999, 2001b) studied south-eastern NSW ICOLLs at Werri and Shellharbour Lagoons, and found 18 and 26 fish species, respectively. Another study in the same general location undertaken by Griffiths and West (1999) found 7 species at Bellambi Lagoon, 21 species at Werri Lagoon and 20 species at Fairy Creek. In contrast, other studies have found a higher number of species, such as 41 species from Dee Why Lagoon (Allan et al. 1985), 39 species from Swan Lake, and 41 species from Lake Wollumboola (Pollard 1994b), both of which are much larger sized lagoons compared to those of the current study. Also, Jones and West (2005) sampled seagrass meadows in NSW south coast ICOLLs and found higher richness at Lake Conjola (57 species), Burril Lake (53 species), Coilia Lake (41 species) and Wallaga Lake (52 species) all of which are also much larger lagoons compared to those of the current study.

Many of the studies described make use of the two common sampling methods, seine and multi- panel gill nets, except for the study by Pollard (1994b) which used a variety of additional methods described earlier. Other studies compare assemblages between day and night sampling, and in some cases species richness was greater at night, which was attributed to more fishes being more active (e.g. foraging for food) (Griffiths 2001c). Griffiths and West (1999) and Becker and Laurenson (2008) reported that the number of species was correlated with the size of the ICOLL. Comparing ICOLLs from all studies with water areas of less than 5 km2, most

187 Chapter 5: Factors influencing fish assemblages

were found to have a lower species richness (<30 species), with the exception of Dee Why Lagoon. Therefore, it can be concluded that small sized ICOLLs tend to be characterised by low species richness.

5.4.4 Spatial and temporal variation of fish assemblages of ICOLLs Significantly different spatial and temporal variations of fish assemblages sampled by seine and multi-panel gill nets were evident. Multivariate analysis suggests that these variations occur within sites, as well as, between each of the Central Coast ICOLLs, but at different times. These variations occurred at different sampling times due to a number of factors such as possible seasonal variations and changes in environmental factors (i.e. salinity, percentage sediment composition, water temperature, status of barrier). Therefore, the mean number of species was significantly different between sampling times and sites within ICOLLs and between sampling times and ICOLLs, however the mean numbers of individuals were only significantly different between sampling times and sites within ICOLLs.

Spatial variations within and between Central Coast ICOLLs were generally related to the increased abundances of the dominant fish species in each ICOLL, which were generally greater near lagoon entrances, except at Terrigal Lagoon. Studies by Griffith and West (1999) and Jones and West (2005) found higher salinity, especially when barriers had been opened, which contributed to an increase in fish abundance and species richness near entrances. Allan et al. (1985) suggested that increases in abundances and species richness may also be attributed to water depth which is generally greater at entrances compared to sites further upstream. Also, when barriers have been opened, water depth and area decreases along with habitat availability causing differences in abundances and species richness due to movement of species into creeks upstream or out to sea, and also the possibility of fish kills (Wilson et al. 2002).

In the current study, Atherinosoma microstoma was generally found at sites near the entrances of Avoca and Wamberal Lagoons. This was also the case for Acanthopagrus australis in Cockrone and Avoca Lagoons. Many estuarine and marine fish species prefer water conditions near the entrances as salinity is generally higher there, however, A. microstoma is tolerant of a wide range of salinities (Molsher et al. 1994). Atherinosoma microstoma was also found in high abundances throughout Wamberal Lagoon, which could be attributed to the shallow depths and higher water temperatures, as well as potential foraging areas. At Terrigal Lagoon, species richness and abundances were similar throughout the ICOLL, possibly due to the high number of barrier openings resulting in relatively similar conditions occurring throughout the study. Therefore the null hypothesis that there are no differences in spatial and temporal variation in fish assemblages between ICOLLs can be rejected.

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5.4.5 Influence of environmental variables on fish assemblages The environmental factors influencing the spatial and temporal variations in fish assemblages differed in each ICOLL, with no one factor being significant in all ICOLLs. Salinity and water temperature were the most influential factors affecting changes in fish assemblages for both sampling methods, along with sediment grain size. Although, barrier openings have been shown to influence fish assemblages in ICOLLs, openings were not shown to directly influence fish assemblages in Central Coast ICOLLs, however, they can indirectly influence fish assemblages by changing environmental factors such as salinity and turbidity.

The main factor influencing seine net fish assemblages at Cockrone and Wamberal lagoons was salinity, with water temperature being the most important factor at Avoca and Terrigal Lagoons. In comparison, at Cockrone and Avoca Lagoons salinity was the main influencing factor on multi-panel gill net samples, with water temperature and percentage sediment grain size (>212 µm) being most influential at Terrigal and Wamberal Lagoons, respectively. When studying estuarine fish assemblages’, salinity is the most common variable that has been shown to determine the spatial variability and composition of fish assemblages, especially in permanently open estuaries (Pollard 1994b; Jones and West 2005). In ICOLLs, salinity gradients generally occur due to wind currents, and similar species being found throughout each ICOLL may indicate that there were no salinity gradients occurring. However, many resident species of fish can tolerate changing environmental conditions (Pombo et al. 2005). Throughout this study salinity was similar at most sites within each ICOLL; however, it was not the major factor influencing fish assemblages at Terrigal Lagoon, since the high number of barrier openings in this case resulted in salinities remaining relatively high. In contrast, the barrier was opened, fewer times at Cockrone, Avoca and Wamberal Lagoons, and thus when their barriers are opened salinity would increase dramatically from values more typical of a brackish environment to values resembling a marine environment (Walsh et al. 2013). Other studies in NSW (Griffiths 1999; Jones and West 2005) and internationally (Gordo and Cabral 2001; Vega-Cendejas and de Santillana 2004) have found that salinity was the major factor in influencing fishes assemblages in these small shallow environments.

Water temperatures varied in response to seasonal variations in air temperatures. Other studies have found that as water temperatures increase, so does fish species richness and abundance (Bennett 1989; Pollard 1994a; Pombo et al. 2005, Walsh et al. 2013). The changes in fish assemblages when sampling in warmer months are mainly due to an increase in larval and juvenile fishes as spawning activities of most fishes occurs during warmer periods, as do the physiological processes such as swimming speed, allowing larval and juvenile fishes to move into and around ICOLLs (Trnski 2002; Specziar et al. 2013). Water temperature was influential

189 Chapter 5: Factors influencing fish assemblages

at Terrigal Lagoon on the catches for both sampling methods, which could be attributed to two factors. Firstly, the catchment surrounding Terrigal Lagoon is highly developed, with surfaces that retain heat, so waters may be heated up as run-off from these surfaces enters into the ICOLL (Paul and Meyer 2001). Secondly, the shallow nature of Terrigal Lagoon and the other three ICOLLs, generally have large areas that are <1 m in depth, which may cause their waters to be heated naturally.

Sediment composition has been shown to influence estuarine fish assemblages (Allan et al. 1985; Bergman et al. 2001; Pombo et al. 2005), with many benthic species such as gobiids being spatially segregated according to the type of sediment present (Gill and Potter 1993; Cowley and Whitfield 2001). Larger mobile species such as sea mullet are especially influenced by sediment composition as they feed on the organic matter associated with the finer particles of sediments (Waltham et al. 2013). Barrier status was only shown to be influential at Wamberal Lagoon, which is surprising since the barrier there was only opened 1-2 times per year compared to more than 10 times at Terrigal Lagoon. However, when the barrier opens at Wamberal Lagoon, the water area and depth decrease greatly, with most of the ICOLL floor becoming exposed, apart from small puddles and shallow channels. Therefore the areas that fishes can utilise are limited and in some cases fish kills have been observed (Wilson et al. 2002). The current study also found that percentage forest cover in one of the subcatchments in Avoca and Wamberal Lagoons catchment area influenced fish assemblages. The direct influence of forested catchments on fish assemblages is unknown; however a study by Mikac et al. (2007) found no physiochemical differences between sediments and macrofauna sampled from forested and urbanised catchments.

Both seine and multi-panel gill netting used to assess fish assemblages in ICOLLs showed that some common environmental factors influenced these assemblages, however the suite of environmental factors differed for each ICOLL. Therefore, the null hypothesis that environmental factors structuring fish assemblages do not differ among the four ICOLLs should be rejected.

5.4.6 Implications of this study This study has provided information on the fish assemblages found in the ICOLLs of the Central Coast of NSW and the factors influencing these assemblages. The influence of barrier openings on ICOLL fish assemblages could not be fully evaluated, as no comparisons could be made between a control site (i.e. any ICOLL whose barrier was not opened). However, in this study, statistical analysis showed that Wamberal Lagoon fish assemblages were shown to be influenced by barrier openings. In contrast, the frequency of artificial opening regimes in

190 Chapter 5: Factors influencing fish assemblages

Terrigal Lagoon has been increased due to flood mitigation practices, and as a result this ICOLL has a greater number of fish species with a lower abundance of fishes compared to Cockrone, Avoca and Wamberal Lagoons (Figure 5.6). This study has shown that no one factor has any influence on the structure of fish assemblages in all of these ICOLLs, however, the main factor influencing fish assemblages in Cockrone and Wamberal Lagoons was salinity, compared to water temperature in Avoca and Terrigal Lagoons, when sampling with seine nets. Fish assemblages in Cockrone and Avoca Lagoons differed due to salinity and water temperature, and to sediment grain size at Terrigal and Wamberal Lagoons, respectively, when using multi- panel gill nets. These differences in environmental factors affecting the assemblages in the different ICOLLs indicate the possible need for differing management practices. The continuing assessment of fish assemblages in ICOLLs is also recommended due to increasing catchment development and the possible effects associated with climate change.

5.5 Conclusion Fish assemblages of ICOLLs in the current study were found to have relatively low species richness, but high abundances of a particular species. Greater abundances and species richness were found in samples collected by seine nets compared to multi-panel gill nets. Terrigal Lagoon had the highest species richness, while Wamberal Lagoon had the highest fish abundance. The relatively high abundances of fishes observed in these lagoons are attributed to one dominant species within each ICOLL, which included atherinids, ambassids, mugilids and sparids in the various ICOLLs studied. The high numbers of juvenile sparids collected at Cockrone and Avoca Lagoons suggests that these ICOLLs may be important nursery areas for this species. Significant differences were evident in spatial and temporal variations within and between ICOLLs. Therefore the null hypothesis that there are no differences in spatial and temporal variation in fish assemblages between these ICOLLs was rejected. The numbers of species found in the ICOLLs of the current study area was much lower than the numbers of species found at other south-eastern NSW ICOLLs; however, this can be attributed to the relatively small sizes of the ICOLLs studied here. Although this question was not examined here, studies of other NSW ICOLLs have shown higher species richness in larger sized ICOLLs.

Seine and multi-panel gill net fish assemblages were influenced by different specific environmental factors such as salinity, water temperature and percentage sediment composition. However, the most important environmental factors structuring variations in fish assemblages differed among the four ICOLLs, with the status of the barrier generally not an important factor in directly changing fish assemblages. However, certain species of fish collected and the changing environmental factors found within Central Coast ICOLLs suggests otherwise. Therefore, the null hypothesis that environmental factors structuring fish assemblages do not

191 Chapter 5: Factors influencing fish assemblages

differ among the four ICOLLs studied, and that barrier status in this instance was the most important factor, can be rejected.

Also, it is possible that stochastic factors in the times and durations of barrier openings probably play a large part in determining the fish assemblages that may be present at any one time in individual ICOLLs, even those that maybe close nearby to each other, as in the case here.

192 Chapter 5: Factors influencing fish assemblages

Appendices: Fish assemblages, water variables and algal mass of ICOLLs

193 Chapter 5: Factors influencing fish assemblages

Appendix 1a. Fishes collected bimonthly by seine and multi-panel gill nets at Cockrone Lagoon between February 2009 and June 2010. The numbers of each species are the sum of the numbers collected across all replicate samples in all sampling periods. Site Family/Species Common name 1 2 3 4 5 Total seine gill seine gill seine gill seine gill seine gill Ambassidae Ambassis jacksoniensis Port Jackson perchlet 2 2 Atherinidae Atherinosoma microstoma Small-mouthed hardyhead 74 3 3 3 2 85 Callionymidae Repomucenus calcaratus Spotted sand-dragonet 1 1 Eleotridae Philypnodon grandiceps Flathead gudgeon 49 62 23 78 73 285 Gobiidae Arenigobius bifrenatus Bridled goby 1 1 Favonigobius tamarensis Tamar River goby 1 1 2 Pseudogobius species no.9 3 3 3 9 Hemiramphidae Hyporhamphus regularis River garfish 5 9 7 7 28 Mugilidae Liza argenta Flat-tail mullet 2 2 Mugil cephalus Sea mullet 76 42 8 17 1 18 17 179 Myxus elongatus Sand mullet 20 29 5 4 8 1 4 1 16 88 Platycephalidae Platycephalus fuscus Dusky flathead 1 1 Platycephalus longispinis Long-spined flathead 2? 2 Poeciliidae Gambusia holbrooki Mosquito fish 5 5 Sillangidae Sillago ciliata Sand whiting 5 4 9 Sparidae Acanthopagrus australis Yellow-finned bream 602 13 243 2 81 5 267 2 298 19 1532 Rhabdosargus sarba Tarwhine 3 3 Tetraodontidae Tetractenos hamiltoni Common toadfish 1 1 Total number of individuals 2235

194 Chapter 5: Factors influencing fish assemblages

Appendix 1b. Fishes collected bimonthly by seine and gill nets at Avoca Lagoon between February 2009 and June 2010. The numbers of each species are the sum of the numbers collected across all replicate samples in all sampling periods. Site Family/Species Common name 1 2 3 4 5 seine gill seine gill seine gill seine gill seine gill Total Arripididae Arripis trutta Eastern Australian salmon 1 4 5 Atherinidae Atherinosoma microstoma Small-mouthed hardyhead 1510 114 18 12 48 1702 Carangidae Pseudocaranx georgianus White trevally 1 1 Clupeidae Herklotsichthys castelnaui Southern herring 15 6 1 4 26 Hyperlophus vittatus Sandy sprat 3 3 Eleotridae Philypnodon grandiceps Flathead gudgeon 32 5 17 59 22 135 Girellidae Girella tricuspidata Luderick 1 1 Gobiidae Arenigobius bifrenatus Bridled goby 3 1 1 5 Favonigobius tamarensis Tamar River goby 24 3 2 29 Pseudogobius species no.9 1 1 Hemiramphidae Hyporhamphus regularis River garfish 8 1 15 5 10 39 Mugilidae Mugil cephalus Sea mullet 217 10 42 2 122 58 83 534 Myxus elongatus Sand mullet 1 2 23 2 28 Platycephalidae Platycephalus fuscus Dusky flathead 4 2 1 2 9 Poeciliidae Gambusia holbrooki Mosquito fish 3 3 Sillangidae Sillago ciliata Sand whiting 6 1 7 Sparidae Acanthopagrus australis Yellow-finned bream 175 7 722 50 398 17 46 3 151 2 1571 Rhabdosargus sarba Tarwhine 3 2 5 Tetraodontidae Tetractenos hamiltoni Common toadfish 15 8 23 Total number of individuals 4127

195 Chapter 5: Factors influencing fish assemblages

Appendix 1c. Fishes collected bimonthly by seine and gill nets form Terrigal Lagoon between February 2009 and June 2010. The numbers of each species are the sum of the numbers collected across all replicate samples in all sampling periods. Site Family/Species Common name 1 2 3 4 Total Seine gill seine gill seine gill seine gill Ambassidae Ambassis jacksoniensis Port Jackson perchlet 353 21 101 475 Ambassis marianus Ramsay’s glassfish 3 1 4 Atherinidae Atherinosoma microstoma Small-mouthed hardyhead 2 1 3 Carangidae Trachinotus sp. 1 1 Clupeidae Herklotsichthys castelnaui Southern herring 7 1 9 2 19 Eleotridae Philypnodon grandiceps Flathead gudgeon 22 6 20 259 307 Gerreidae Gerres subfasciatus Common silver belly 7 12 38 2 9 3 15 2 88 Girellidae Girella tricuspidata Luderick 3 3 Gobiidae Arenigobius bifrenatus Bridled goby 4 73 77 Favonigobius tamarensis Tamar River goby 2 2 Gobiopterus semivestitus Glass goby 1 24 25 Pseudogobius species no.9 Blue spot goby 5 5 1 52 63 Hemiramphidae Hyporhamphus regularis River garfish 2 17 1 8 28 Heterodontidae Heterodontus portusjacksoni Port Jackson shark 1 1 Monodactylidae Monodactylus argenteus Silver batfish 1 1 Mugilidae Liza argenta Flat-tail mullet 12 9 20 41 Mugil cephalus Sea mullet 33 28 7 48 17 19 5 39 196 Myxus elongatus Sand mullet 211 113 103 94 27 2 32 582 Paralichthyidae Pseudorhombus arsius Large-tooth flounder 1 1 Percichthyidae Macquaria colonorum Estuary perch 6 6

196 Chapter 5: Factors influencing fish assemblages

Appendix 1c. Continued……

Site 1 2 3 4 Family/Species Common name Seine Gill Seine Gill Seine Gill Seine Gill Total Platycephalidae Platycephalus fuscus Dusky flathead 2 2 3 1 8 Poeciliidae Gambusia holbrooki Mosquito fish 3 4 7 Pomatomidae Pomatomus saltatrix Tailor 1 1 Pseudomugilidae Pseudomugil signifer Pacific Blue-eye 30 1 2 33 Scorpaenidae Centropogon australis Fortesque 1 2 3 Sillangidae Sillago ciliata Sand whiting 4 17 61 5 5 6 98 Sparidae Acanthopagrus australis Yellow-finned bream 4 5 3 1 2 1 7 2 25 Rhabdosargus sarba Tarwhine 3 1 4 Tetraodontidae Tetractenos hamiltoni Common toadfish 2 1 3 Total number of individuals 2105

197 Chapter 5: Factors influencing fish assemblages

Appendix 1d. Fishes collected bimonthly by seine and gill nets at Wamberal Lagoon between February 2009 and June 2010. The numbers of each species are the sum of the numbers collected across all replicate samples in all sampling periods. Site Family/Species Common name 1 2 3 4 5 Seine gill seine gill seine gill seine gill seine gill Total Anguillidae Anguilla reinhardtii Marbled eel 1 1 Atherinidae Atherinosoma microstoma Small-mouthed hardyhead 3744 419 597 344 562 5666 Clupeidae Herklotsichthys castelnaui Southern herring 5 5 Eleotridae Philypnodon grandiceps Flathead gudgeon 2 66 49 29 8 154 Gobiidae Arenigobius bifrenatus Bridled goby 1 1 Pseudogobius species no.9 Blue-spot goby 4 5 3 1 13 Hemiramphidae Hyporhamphus regularis River garfish 23 18 37 28 106 Mugilidae Liza argenta Flat-tail mullet 4 4 Mugil cephalus Sea mullet 1 12 23 36 33 5 24 71 205 Myxus elongatus Sand mullet 8 98 11 6 2 2 3 130 Platycephalidae Platycephalus fuscus Dusky flathead 1 1 Pseudomugilidae Pseudomugil signifer Pacific Blue-eye 7 7 Sparidae Acanthopagrus australis Yellow-finned bream 1 1 3 5 Total number of individuals 6298

198 Chapter 5: Factors influencing fish assemblages

Appendix 2a. Salinity (ppt) sampled at each site in all ICOLLs between February 2009 and June 2010. The solid vertical line indicates multiple barrier openings that occurred between sampling periods, with dotted lines showing a single barrier opening that occurred between sampling periods. Months with no data indicates readings were unable to be recorded due to malfunctioning water meter. Symbols denote: (♦) site 1, (ο) site 2, (▲) site 3, (□) site 4, (■) site 5. Only four sites were sampled at Terrigal Lagoon. High salinity at site 1 Cockrone Lagoon can be related overwash events, whereas low salinity at sites 4 Avoca Lagoon and after openings at Terrigal Lagoon can be related to the effects of high rainfall events resulting in increased stormwater run-off occurring between sampling times.

Cockrone Lagoon Avoca Lagoon

35 30

30 25 25 20 20

15 ppt ppt 15 10 10

5 5

0 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10

Terrigal Lagoon Wamberal Lagoon

35 20 18 30 16 25 14 12 20

ppt ppt 15 8 10 6 4 5 2 0 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Sampling period Sampling period

199 Chapter 5: Factors influencing fish assemblages

Appendix 2b. Water temperature (°C) sampled at each site in all ICOLLs between February 2009 and June 2010. The solid vertical line indicates multiple barrier openings that occurred between sampling periods, with dotted lines showing a single barrier opening that occurred between sampling periods. Months with no data indicates readings were unable to be recorded due to malfunctioning water meter. Symbols denote: (♦) site 1, (ο) site 2, (▲) site 3, (□) site 4, (■) site 5. Only four sites were sampled at Terrigal Lagoon.

Cockrone Lagoon Avoca Lagoon

30 35

25 30 25 20

20 C

C 15 ° ° 15 10 10

5 5

0 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10

Terrigal Lagoon Wamberal Lagoon 35 30

30 25

25 20

20 C

° 15 C ° 15 10 10

5 5

0 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Sampling period Sampling period

200 Chapter 5: Factors influencing fish assemblages

Appendix 2c. Turbidity (ntu) sampled at each site in all ICOLLs between February 2009 and June 2010. The solid vertical line indicates multiple barrier openings that occurred between sampling periods, with dotted lines showing a single barrier opening that occurred between sampling periods. Months with no data indicates readings were unable to be recorded due to malfunctioning water meter. Symbols denote: (♦) site 1, (ο) site 2, (▲) site 3, (□) site 4, (■) site 5. Only four sites were sampled at Terrigal Lagoon. The high turbidity at individual sites within each ICOLL can be related to the effects of the following; high rainfall, increased stormwater run-off, barrier openings, the lack of seagrass and/or the low water depth and recreational activities occurring at the time of sampling.

Cockrone Lagoon Avoca Lagoon

40 8 35 7 30 6 25 5 20

4 ntu ntu 15 3 10 2

1 5

0 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10

Terrigal Lagoon Wamberal Lagoon

8 90 80 7 70 6

60 5 50

4 ntu ntu 40 3 30 2 20 10 1 0 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Sampling period Sampling period

201 Chapter 5: Factors influencing fish assemblages

Appendix 2d. Dissolved oxygen (mg/L) sampled at each site in all ICOLLs between February 2009 and June 2010. The solid vertical line indicates multiple barrier openings that occurred between sampling periods, with dotted lines showing a single barrier opening that occurred between sampling periods. Months with no data indicates readings were unable to be recorded due to malfunctioning water meter. Symbols denote: (♦) site 1, (ο) site 2, (▲) site 3, (□) site 4, (■) site 5. Only four sites were sampled at Terrigal Lagoon. In most cases dissolved oxygen was within acceptable limits, with anoxia only occurring once in Cockrone and Avoca Lagoons

Cockrone Lagoon Avoca Lagoon 16 14

14 12 12 10 10 8

8 mg/L

mg/L 6 6 4 4

2 2

0 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10

Terrigal Lagoon Wamberal Lagoon

12 16 14 10 12 8 10

6 8

mg/L mg/L 6 4 4 2 2

0 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Sampling period Sampling period

202 Chapter 5: Factors influencing fish assemblages

Appendix 3. The combined total algal mass of 5 replicate samples collected at each site in Cockrone, Avoca and Wamberal lagoons between February 2009 and June 2010. Months and sites with no data indicate no algae were collected, and the data is the sum of all replicates in each site. The solid vertical line indicates multiple barrier openings that occurred between sampling periods, with dotted lines showing a single barrier opening that occurred between sampling periods. No alga was collected from Terrigal Lagoon. In most cases, total algal mass decreased after barrier openings in these ICOLLs.

Cockrone Lagoon

900 800 700 600 S1 500 S2 400 S3 grams S4 300 S5 200 100 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10

Avoca Lagoon 500 450 400 S1 350 S2 S3 300 S4 250 S5 grams 200 150 100 50 0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10

Wamberal Lagoon 300

250 S1 S2 200 S3 S4 S5

150 grams 100

0 Feb 09 Apr 09 Jul 09 Sep 09 Nov 09 Jan 10 Mar 10 Jun 10 Sampling period

203 Chapter 6: Diets of fishes in ICOLLs

Chapter 6: Diets of fishes in ICOLLs and the effects of barrier openings

204 Chapter 6: Diets of fishes in ICOLLs

6.1 Introduction Intermittently Closed and Open Lakes and Lagoons (ICOLLs) are highly-productive ecosystems and the formation of barriers across their entrances prevents the movement of fishes into and out of these lagoon environments. Many ICOLLs can be isolated for long periods of time and their fish faunas must thus be able to contend with both changing environmental conditions and isolation from marine influences (Griffiths 1999, 2001a). The fish assemblages of ICOLLs generally have relatively low species diversity and are dominated numerically by only a few species (Allan et al. 1985; Young and Potter 2002).

ICOLLs generally have high abundances of fish and long periods of isolation from the sea, which may indicate that many ICOLL fishes have to contend with limited food and shelter resources. Limiting factors of these food and shelter resources in ICOLLs include barrier status, changing environmental conditions, loss of vegetated habitats, varying sediment characteristics, and changes in water area. Overall, the status of the barrier is generally regarded as the main influencing factor in ICOLLs changing environmental conditions such as fluctuations in salinity, reducing aquatic vegetation, modifying sediment characteristics, and changing water area, all of which can affect both possible food resources and shelter (Robinson et al. 1983; Dye and Barros 2005b; Gladstone et al. 2006). Water area is an important component, especially in small ICOLLs, as the area of possible fish habitats and areas for fish dispersion diminish when barriers are opened. In contrast when barriers are closed the water area increases and flood zones offer alternative habitats and additional food resources (Becker and Laurenson 2007). Fish are highly mobile and can reduce competition by dispersing throughout the ICOLL; however, the ability of fishes to disperse is restricted by the size of the estuary and the status of the barrier (Becker and Laurenson 2007). Other factors have been shown to reduce feeding competition, such as variations in mouth morphology and feeding behaviour (Gill and Potter 1993), ontogenetic changes in diet (Kennish 1990; Gill and Potter 1993), timing of feeding, seasonal changes in diet, fish size (Sanchez-Jerez et al. 2002), and differences in habitat preferences (Becker and Laurenson 2007).

Invertebrate fauna are preferred food items of many fishes, however, the diets of different species vary with habitat (Platell et al. 2006). Common habitats found in most ICOLLs include shallow and deep waters, fringing wetlands, sandy sediments near the entrance, a central muddy basin, seagrasses, and algae (Cheng 1981). Seagrasses and other submerged macrophyes are of particular importance in trophic studies as they provide high abundances and richness of invertebrates (Humphries and Potter 1993; Edgar and Shaw 1995) and also microhabitats for small fishes. They also provide epifauna and associated infauna (Humphries and Potter 1993; Sanchez-Jerez et al. 2002). A common submerged aquatic macrophyte found in ICOLLs,

205 Chapter 6: Diets of fishes in ICOLLs

Ruppia sp. or sea tassel, is also tolerant of a wide range of environmental conditions, including salinity and physical disturbances (Sainty and Jacobs 1981). Similar to other submerged macrophytes, Ruppia sp. supports high densities of fishes, but is limited in the number and types of invertebrates it can support (Humphries and Potter 1993). Algae also provide alternate habitats and food sources. The products of increased nutrients, algae, are now common throughout most ICOLLs and are utilised as shelter by many species of fishes (Prince et al. 1982).

Bare sedimentary substrates are common throughout ICOLLs and support a variety of infauna that is a potential food resource see Chapter 3 (Humphries and Potter 1993). Bare areas of substrate are generally found near the entrance and parts of the central basin that are devoid of aquatic vegetation. Substrates also accumulate detritus, which is a known food source of many invertebrates, which in turn provide a food source for fishes (Humphries and Potter 1993).

When studying the feeding habitats of fishes, the most common method used is to examine their gut contents (Hyslop 1980). However, examining the gut contents of a particular species of fish does not always give an accurate account of its actual eating habits (Windell and Bowen 1978). Many species of small fishes, such as atherinids, lack a discrete stomach and therefore they are able to digest food items rapidly, making the gut contents difficult to identify (Prince et al. 1982). Traumatic sampling techniques such as chemical treatments, electrofishing and extended gill-netting, can also cause regurgitation, resulting in high numbers of empty stomachs (Windell and Bowen 1978). Passive sampling techniques, such as seine netting or short-term gillnetting, are less traumatic. Stable isotope analysis provides information on dietary items consumed over recent weeks or months, compared to gut analysis which provides information on contents consumed within hours (Hadwen et al. 2007).

Many studies of the diets of fishes in ICOLLs have shown that opportunistic feeders are best suited to these environments (Becker and Laureson 2007; Chuwen et al. 2007; Hadwen et al. 2007), along with species that utilise food resources found within the substrate and throughout the entire water column (Prince et al. 1982). However, some species tend to be restricted to a select number of dietary items, with other species having a preference for specific food items (Chuwen et al. 2007; Hadwen et al. 2007).

Sandy barriers are formed by wave action and the effects of both onshore and longshore drifting of sand being deposited across the entrance, and these barriers generally can remain closed for longer periods than they are open (Bird 1967; Pollard 1994a; Griffiths 1999). The timing, frequency and duration of barrier openings are dependent upon climatic conditions and the

206 Chapter 6: Diets of fishes in ICOLLs

amount of development within the catchment. The occurrence of natural barrier openings has become more infrequent due to local councils implementing artificial openings as a management practice to mitigate flooding of the surrounding urbanised lagoon foreshores (Gale et al., 2006, Gladstone et al., 2006). The literature reviewed does not give an indication of the effects of barrier openings on the feeding ecology of fishes within ICOLLs. Instead, information can be interpreted from the effects that such barrier openings have on their potential food sources such as invertebrate fauna. The lack of understanding of the effects of barrier openings on the feeding ecology and diets of fishes in ICOLLs thus needs to be directly explored. Therefore this study was undertaken with the following aims: 1. To determine the diets of the dominant species of fishes within Central Coast ICOLLs. 2. To determine the effects, if any, of barrier openings on the diets of dominant fish species within Central Coast ICOLLs. This study thus tested the following null hypotheses: 1. There are no differences between the diets of fishes in Central Coast and other ICOLLs. 2. The changing barrier status of ICOLLs has no effect on the diets of their fishes.

6.2 Materials and methods

6.2.1 Study area The fish species used for gut analysis were collected bimonthly from the four Central Coast ICOLLs (Cockrone, Avoca, Terrigal and Wamberal Lagoons) between February and November 2009. Detailed habitat descriptions of each ICOLL are provided in Chapter 2. Sites where fishes were collected are shown in Chapter 5 (Figures 5.1-5.4). Over the course of the study period there were; 3 barrier openings at Cockrone Lagoon, 5 openings at Avoca Lagoon, 17 at Terrigal Lagoon, and 1 at Wamberal Lagoon. Gut contents were examined before a barrier opening and after the barrier had re-formed, except at Terrigal Lagoon, where gut contents were examined while the barrier was open and after the barrier had re-formed. At Cockrone Lagoon gut contents of Acanthopagrus australis were combined and analysed for two sampling times before the barrier had opened and one sampling time after the barrier had re-formed, at Avoca Lagoon gut contents of Atherinosoma microstoma were analysed for one sampling time before the barrier had opened and for two sampling times combined after the barrier had re-formed. At Wamberal Lagoon gut contents of Atherinosoma microstoma were combined and analysed for two sampling times before the barrier had opened and combined for two sampling times after the barrier had re-formed, and at Terrigal Lagoon gut contents of Ambassis jacksoniensis were analysed at one sampling time while the barrier was open and at one sampling time after the barrier had re-formed. Specimens were collected with the permission from the University of

207 Chapter 6: Diets of fishes in ICOLLs

Newcastle’s Animal Care and Ethics Committee (ACEC Permit number 9711008) and the NSW Department of Primary Industries (Fisheries Permit number P05/0092).

6.2.2 Study species The species selected for this study were determined by their abundances in the samples of fish collected by seine nets (Chapter 5).

Cockrone Lagoon - Acanthopagrus australis (Sparidae) (Figure 6.1), the yellow-fin bream, is endemic to estuaries, coastal rivers, lakes and bays along the eastern coast of Australia (Allen et al. 2003). Regarded as a recreationally and commercially important species, A. australis is an opportunistic feeder on a diverse range of invertebrates, including polychaetes and amphipods, as well as plant material and other teleosts (Chuwen et al. 2007). The size range of A. australis examined in this study was 38-82 mm TL (Chapter 5).

Figure 6.1. Acanthopagrus australis, collected from Cockrone Lagoon (Photo M. Ricketts).

Avoca Lagoon and Wamberal Lagoon - Atherinosoma microstoma (Atherinidae) (Figure 6.2), the small-mouthed hardyhead, is an annual pelagic fishes common in NSW, Victorian and Tasmanian lakes and lagoons. This species is resilient to extreme changes in salinities (Molsher et al. 1994), prefers calm and shallow waters, and schools in large numbers (Prince et al. 1982). The diet of A. microstoma generally includes small crustaceans and insects (McDowall 1996). The size range of A. microstoma from Avoca Lagoon was 27-67 mm TL, and from Wamberal Lagoon 45-80 mm TL (Chapter 5).

208 Chapter 6: Diets of fishes in ICOLLs

Figure 6.2. Atherinosoma microstoma collected from Avoca and Wamberal Lagoons (Photo M. Ricketts).

Terrigal Lagoon - Ambassis jacksoniensis (Ambassidae) (Figure 6.3), commonly known as glassfish, is a small schooling species endemic to eastern Australian estuaries, lakes and marine waters (Kuiter 2000). It feeds on zooplankton (mainly shore crab larvae) and insects (Kuiter 2000, Hollingsworth and Connolly 2006). The size range of A. jacksoniensis in this study was 45-70 mm TL (Chapter 5).

Figure 6.3. Ambassis jacksoniensis collected from Terrigal Lagoon (Photo M. Ricketts).

6.2.3 Sample size In order to obtain a representative sample of the diet of each species, a species accumulation curve was produced to ensure adequate numbers of fish guts had been examined to accurately describe the diet (Cortes 1997). Dietary items were identified to the lowest possible taxon and in most cases were identified by morphological features that remained after digestion. Gastropods and bivalves were identified by their shell topography and markings, while soft-bodied polychaetes were identified by their chaetae and/or mouthparts. Crustaceans and terrestrial insects were identified by their hard limbs, carapaces and wings, while chironomid larvae were recognizable by their chitinous heads (Hyslop 1980). However, most digested zooplankton was difficult to identify to individual species, therefore they were classified as unidentifiable

209 Chapter 6: Diets of fishes in ICOLLs

zooplankton (Hollingsworth and Connolly 2006). During the present study, some gut contents could not be identified due to extensive maceration and/or rapid digestion, which made it difficult to confirm identification to species (Windell and Bowen 1978, Prince et al. 1982). Also, in most cases molluscs could only be identified to two major grouping: gastropods or bivalves, due to lack of any distinguishing features or markings. The number of taxonomic units described throughout this study refers to the number of invertebrate fauna consumed, and the number of dietary items refers to the abundance of invertebrate fauna consumed related to the estimated percentage volume (%V) contributed by each invertebrate fauna type.

The species accumulation curves were produced using PRIMER-6 with 9999 permutations, with mean number of species plotted against the number of guts examined (Figure 6.4). When the curve reaches a stable asymptote the number of guts analysed is considered sufficient for describing the diet. Using this criterion, for Acanthopagrus australis, the number of species appeared to reach a stable asymptote at n=12; however, further guts were examined to obtain a greater sample size for statistical analysis, hence the number of guts examined was determined at n=30. Although a stable asymptote was not achieved for Atherinosoma microstoma and Ambassis jacksoniensis, the number of guts examined (n=30) showed that this was almost achieved, therefore the same number of guts were used for both of these species in the current study (Figure 6.4).

210 Chapter 6: Diets of fishes in ICOLLs

Acanthopagrus australis 15

t 10

e p

S 5

0 0 5 10 15 20 25 30 35 Atherinosoma microstoma 12

t 8

s 6

e p

S 4

0 0 5 10 15 20 25 30 35 Ambassis jacksoniensis 15

t 10

e p

S 5

0 5 10 15 20 25 30 35 No. of guts examined Figure 6.4. Species accumulation curves showing mean number (for n=9999 permutations) of food species detected with increasing numbers of guts sampled, for Acanthopagrus australis (Cockrone Lagoon), Atherinosoma microstoma (Wamberal Lagoon) and Ambassis jacksoniensis (Terrigal Lagoon).

6.2.4 Examination of gut contents The size of each of the species used for gut content analysis was less than 100 mm TL. This small fish size is more effective in fixation of the whole fish and gut contents when stored in 10% formalin for 1 mo (Mazumder et al. 2006). Specimens were then thoroughly rinsed with tap water and stored in 70% ethanol until gut contents were examined. Atherinids do not possess a stomach and have short intestines (Prince et al. 1982); therefore the entire intestinal tract (called the ‘gut’) was in this case examined. In order to standardise the methods of dietary analysis, both stomachs and guts were examined for Acanthopagrus australis and Ambassis jacksoniensis.

211 Chapter 6: Diets of fishes in ICOLLs

Each individual fish was measured to the nearest 1 mm TL and then the entire gut removed. The gut fullness was visually estimated on a scale from 1 (10% full) to 5 (100% full), with empty guts given a zero rating (Chuwen et al. 2007). The contents were then spread in a Petri dish and examined under a dissecting microscope using reflected light. Dietary items were identified using the same procedure described for the pilot study.

6.2.5 Dietary composition The points estimated volumetric method was used to describe the dietary composition for each species (Hyslop 1980). This method was deemed suitable due to the small size of the fishes (making other methods such as weighing consumed items difficult), along with the rapid digestion and volume of macerated materials found in many of the gut contents (Prince et al. 1982). In addition to gut fullness, the frequency of occurrence (%F) of each dietary item in the guts of each species and the percentage volumetric contribution (%V) of each dietary item to the total amount of gut contents of each fish were estimated (Hyslop 1980).

6.2.6 Data analysis Data analysis was restricted to single species within single ICOLLs, and focused on tests of the effects of barrier openings on gut contents. Fish were collected from different sites and times within each ICOLL; however, due to small sample sizes (i.e. fishes were not collected at all times in all sites), these factors were excluded from the data analysis. Fishes from each ICOLL were randomly pooled into six groups of five fishes and the means of gut contents calculated for each group (Sarre et al. 2000). Permutational multivariate analysis of variance (PERMANOVA) (Anderson 2001; McArdle and Anderson 2001) was used to test the null hypothesis that the changing barrier status of ICOLLs had no effect on the diet, which was based on the %V data, of the target species using the following factor: Status: fixed, two levels (before and after barrier opening). All data were square-root transformed prior to analysis (Schafer et al. 2002) and all tests were based on the Bray-Curtis dissimilarity resemblance measure, with the significance determined from 9999 permutations under a reduced model. PERMANOVA is sensitive to differences in the variability of data, therefore significant results were further investigated for multivariate dispersions using PERMDISP. This program was used to test for homogeneity of dispersions between groups by distance from centroids and comparing the average distances (Anderson 2004).

Where significant differences were detected from before and after openings, the prey categories responsible for dissimilarity in the diets were determined using the Similarity of Percentages (SIMPER) procedure in PRIMER (Clarke 1993). Large values (i.e. >1) of the ratio of dissimilarity/standard deviation(dissimilarity) for a dietary item (where dissimilarity is the

212 Chapter 6: Diets of fishes in ICOLLs

average contribution of the ith dietary item to the overall dissimilarity between 2 groups of standard deviation) indicated that the item was consistently important to dissimilarity in all pairwise comparisons of samples in 2 groups (Clarke 1993). Dietary items with a percentage dissimilarity >3% and with a dissimilarity/standard deviation(dissimilarity) greater than one were regarded as being important contributors to dissimilarity between the barrier status (Terlizzi et al. 2005). Multi-dimensional scaling ordination (MDS) plots were used to visualise differences in the dietary composition of each species.

Univariate PERMANOVA was used to test the null hypothesis for single variables, including the number of taxonomic units in the diet, the number of total dietary items in each gut, the gut fullness and the mean length of species before and after barriers had opened. Euclidean distance was used as the measure of resemblance, and analyses were done with 9999 permutations on unrestricted permutation of raw data. Prior to testing the effects of barrier openings on the number of taxonomic units in the diet, the number of dietary items in each gut, the gut fullness, and the mean length of each species, the homogeneity of variances was tested using the PERMDISP routine (Anderson 2004). Raw data were square-root transformed to eliminate heterogeneity of variances, and when this transformation was unsuccessful the analyses were done with raw data and an adjusted significance level of p=0.01. All multivariate and univariate analyses were examined using PRIMER v6 and PERMANOVA+ (PRIMER-E).

6.3 Results

6.3.1 Acanthopagrus australis-Cockrone Lagoon A total of 330 guts (180 before barrier opening, 150 after barrier opening) of Acanthopagrus australis were examined. Gut contents contained nine broad dietary categories that included bivalves, crustaceans, dipterans, gastropods, nematodes, plant material, polychaetes, terrestrial insects and zooplankton (Appendix 1a). The total number of taxonomic units (before barrier opening n=12, after barrier opening n==10) and the total dietary items (82% before barrier opening, 57% after barrier opening) differed for guts examined before and after barrier opening. The number of empty guts represented 8.3% (n=15) and 4.7% (n=7) of the guts examined before and after barrier opening respectively.

The dietary categories found within the guts examined were mostly similar but the relative amounts differed, especially for amphipods (Figure 6.5). The gut contents of Acanthopagrus australis at Cockrone Lagoon changed significantly from before to after barrier opening (Table 6.1). The MDS ordination plot of the gut contents defined by %V shows a fairly good separation of gut contents between the fish collected before the barrier was opened and fish collected after

213 Chapter 6: Diets of fishes in ICOLLs

the opening, with almost all fish collected before the opening located to the left of the ordination plot (Figure 6.6). The multivariate dispersion (F=7.45, df1, p=0.013) of %V gut contents for Acanthopagrus australis was heterogeneous for the barrier status (p<0.05), with the gut contents of fish collected after the barrier was opened being more variable, as shown also by the greater spread of points on the MDS ordination for before. Therefore, the significant difference in gut contents occurred because of a difference in the composition of the contents (as indicated by the difference in location of guts on the MDS ordination) and a difference in the variability of the contents (with the contents after the opening being more variable).

100 Unknown eggs* Copepods* 80 Unidentifiable material Sediments Polychaetes 60 Plant material Nematodes 40 % volume % Isopods Ephemeropterans 20 Chironomids Terrestrial insects Gastropods 0 Before After Decapods Barrier status Bivalve Amphipoda Figure 6.5. Estimated percentage volumetric (%V) contribution of different dietary categories associated with the diet of Acanthopagrus australis in relation to the barrier status (before, after openings) at Cockrone Lagoon. *denotes planktonic taxa.

214 Chapter 6: Diets of fishes in ICOLLs

2D Stress: 0.21

SIMPER analysis shows that the dietary categories responsible for dissimilarities in the gut contents were amphipods, gastropods, polychaetes, chironomid larvae and plant material (Table 6.2). Amphipods were found in the gut contents in greater quantities after the barrier had opened, as were chironomid larvae and plant material, compared to gastropods that were found in the gut contents in greater quantities before the barrier had opened. Polychaetes did not change despite the status of the barrier.

Table 6.2. Summary of SIMPER results showing taxonomic units responsible for differences in the gut contents of Acanthopagrus australis in Cockrone Lagoon from before to after a barrier opening. (Taxonomic units that contributed up to 90% of the dissimilarity of the before and after samples are shown). Average dissimilarity=61.15 Before After Taxon Av.Abund Av.Abund Av.Diss Diss/SD Contrib% Cum.% Amphipod 1.26 5.99 15.01 1.83 24.55 24.55 Gastropod 4.27 0.85 11.49 1.64 18.78 43.33 Polychaete 3.54 3.36 9.01 1.27 14.74 58.08 Chironomid larvae 1.88 2.73 7.90 1.21 12.92 71.00 Plant material 2.44 3.35 7.85 1.29 12.85 83.84

The mean numbers of taxonomic units in gut contents (%V) did not differ in guts collected before and after barrier openings (Table 6.3 and Figure 6.7a); however, slight significant differences were found for the mean number of dietary items (Table 6.3 and Figure 6.7b).

215 Chapter 6: Diets of fishes in ICOLLs

Table 6.3. Summary of results of 1-factor PERMANOVA testing for differences in the number of taxonomic units (PERMDISP p=0.80) and the number of dietary items (PERMDISP p=0.003) of Acanthopagrus australis from before to after barrier openings (status) at Cockrone Lagoon. Data was square-root transformed. No. of taxonomic units No. of dietary items Source df MS Pseudo-F p MS Pseudo-F p Status 1 0.002 0.02 0.88 20.03 19.14 0.0002 Residual 64 0.007 1.05

(a) 5

1 Mean no.Mean of taxonomic units 0 Before After Barrier status

(b)

100

20 Mean no.Mean of dietary items 0 Before After Barrier status

The mean gut fullness did not change from before to after the barrier opening; however, the mean TL of the fish (before barrier opening =59.0±0.6 mm, after barrier opening =53.0±0.3 mm) was significantly different (Table 6.4 and Figure 6.8). The range in total fish length measured before the barrier opening was 38-82 mm TL, compared to 46-63 mm TL after the barrier had opened (Appendix 1a). The highest percentage of total length frequency of fish

216 Chapter 6: Diets of fishes in ICOLLs

sampled before the barrier had opened ranged in size between 45-74 mm TL compared to 45-64 mm TL after the barrier had opened (Figure 6.9).

1 Mean gut fullnessgut Mean

0 Before After Barrier status

Figure 6.8. Mean gut fullness (±s.e.) of Acanthopagrus australis at Cockrone Lagoon before and after the barrier opening.

80 70 60 50 40 30

20 % frequency% 10 0 35-44 45-54 55-64 65-74 75-84 TL (mm) before (n=180) after (n=150) Figure 6.9. Length-frequency distribution of Acanthopagrus australis used in dietary analysis from Cockrone Lagoon before and after barrier openings.

217 Chapter 6: Diets of fishes in ICOLLs

6.3.2 Atherinosoma microstoma-Avoca Lagoon A total of 90 guts (30 before barrier opening, 60 after barrier opening) of Atherinosoma microstoma were examined. Gut contents contained six broad dietary categories that included bivalves, crustaceans, dipterans, polychaetes, terrestrial insects and zooplankton (Appendix 1b). The total number of taxonomic units (before barrier opening n=3, after barrier opening n=8) and the total dietary items (51% before barrier opening, 77% after barrier opening) differed for guts examined before and after barrier opening. The number of empty guts represented 43.3% (n=13) and 60% (n=36) of the guts examined before and after barrier opening respectively.

The dietary categories found within the guts examined differed between before and after the barrier opened, and the relative amounts also differed (Figure 6.10). The gut contents (%V) of Atherinosoma microstoma at Avoca Lagoon did not change significantly from before to after barrier opening (Table 6.5).

100 Copepoda* Bivalve* 80 Unknown material

60 Sediment Polychaete

40 Plant material % volume % Isopoda 20 Terrestrial insect Chironomidae 0 Before After Bivalve Barrier status Amphipod

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The mean number of taxonomic units and the mean number of dietary items in gut contents did not differ in guts collected before and after barrier openings (Table 6.6, Figure 6.11a), although there is a significant difference shown in the mean number of dietary items in Figure 6.11b.

(a)

Mean no. of taxonomicno.unitsof Mean 0 Before After Barrier status

(b)

20 *

Mean no. of dietaryno.itemsof Mean 0 Before After Barrier status

219 Chapter 6: Diets of fishes in ICOLLs

The mean gut fullness and the mean fish TL (before barrier opening =54.6±0.6 mm, after barrier opening =48.2±1.8 mm) did not change from before to after the barrier opening (Table 6.7 and Figure 6.12). The range in fish lengths differed from 50-63 mm TL (before) and 27-67 mm TL (after) the barrier had opened (Appendix 1b). The highest percentage frequency of fish sampled before the barrier had opened ranged in size from 45-64 mm TL compared to 55-64 and 25-34 mm TL after the barrier had opened (Figure 6.13).

1.5

0.5 Mean gut fullnessgutMean

0 Before After

Barrier status Figure 6.12. Mean gut fullness (±s.e.) of Atherinosoma microstoma at Avoca Lagoon before and after (i.e. barrier staus) the barrier opening.

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% frequency% 20

0 25-34 35-44 45-54 55-64 65-74 TL (mm)

before (n=30) after (n=60) Figure 6.13. Length-frequency distribution of Atherinosoma microstoma used in the dietary examination at Avoca Lagoon before and after barrier openings.

6.3.3 Atherinosoma microstoma–Wamberal Lagoon A total of 360 guts (180 before barrier opening, 180 after barrier opening) of Atherinosoma microstoma were examined. Gut contents contained eight broad dietary categories: bivalves, crustaceans, dipterans, gastropods, nematodes, polychaetes, terrestrial insects and zooplankton (Appendix 1c). The total number of taxonomic units (before barrier opening n=9, after barrier opening n=10) and the total dietary items (91% before barrier opening, 88% after barrier opening) differed for guts examined before and after barrier opening. The number of empty guts represented 26.1% (n=47) and 13.3% (n=36) of the guts examined before and after barrier opening respectively.

The dietary categories found within the guts examined were mostly similar but the relative amounts differed, especially for amphipods and gastropods (Figure 6.14). The gut contents of Atherinosoma microstoma at Wamberal Lagoon changed significantly from before to after barrier opening (Table 6.2). The MDS ordination plot of the gut contents defined by %V shows some separation of gut contents between fish collected before the barrier was opened and fish collected after the opening, although there is some overlapping. Fishes collected after the barrier had opened are mainly located to the left of the MDS ordination plot (Figure 6.15). The multivariate dispersion (F=1.46, df1, p=0.25) of %V gut contents for A. microstoma were homogeneous for the barrier status (p>0.05), with the gut contents of fish collected after the barrier was opened being more variable as shown also by the greater spread of points on the MDS ordination for before. Therefore, the significant difference in gut contents occurred because of a difference in the composition of the contents (as indicated by the difference in location of guts on the MDS ordination) and a difference in the variability of the contents (with the contents after the opening being more variable).

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100 Copepods*

Unidentifiable material

80 Ephemeropterans

Sediments

Polychaetes 60 Plant material

Nematodes % volume % 40 Isopods

Chironomids

20 Terrestrial insects

Gastropods

0 Bivalves Before After Amphipods Barrier status

2D Stress: 0.23

222 Chapter 6: Diets of fishes in ICOLLs

SIMPER analysis shows that the dietary categories responsible for dissimilarities in the gut contents were amphipods, polychaetes and gastropods (Table 6.9). Gastropods and polychaetes were found in the gut contents in greater quantities after the barrier had opened, compared to amphipods that were found in gut contents in greater quantities before the barrier had opened.

The mean numbers of taxonomic units in gut contents did not differ in guts collected before and after barrier openings (Table 6.10 and Figures 6.16a), however significant differences were found for the mean number of dietary items (Table 6.10 and Figures 6.16b).

Table 6.9. Summary of SIMPER showing taxonomic units responsible for differences in the gut contents of Atherinosoma microstoma in Wamberal Lagoon from before to after a barrier opening. Taxonomic units that contributed up to 90% of the dissimilarity of the before and after samples are shown. Average dissimilarity=68.04 Before After Taxon Av.Abund Av.Abund Av.Diss Diss/SD Contrib% Cum.% Amphipod 3.85 2.01 12.73 1.37 18.71 18.71 Polychaete 2.88 3.19 10.45 1.23 15.36 34.07 Gastropod 1.57 3.13 10.23 1.16 15.04 49.10 Chironomid larvae 1.22 2.15 8.52 0.96 12.53 61.63 Terrestrial insect 1.36 1.62 7.07 0.99 10.39 72.02 Bivalve 1.72 0.47 5.95 0.87 8.75 80.77 Nematode 1.24 0.14 4.53 0.65 6.65 87.42 Isopod 0.00 1.18 4.06 0.57 5.97 93.39

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(a)

0 Mean no. of taxonomicno.of units Mean Before After Barrier status

(b)

20 Mean no. of dietaryitemsof no. Mean 0 Before After Barrier status

The mean gut fullness and the mean fish TL (before barrier opening =58.3±0.4 mm, after barrier opening =65.1±.3 mm) were significantly different from before to after barrier opening (Table 6.11 and Figure 6.17). The range in fish lengths differed from 45-74 mm TL (before) and 52-80 mm TL (after) the barrier had opened (Appendix 1c). The highest percentage frequency of fish sampled before the barrier had opened ranged from 45-64 mm TL compared to 55-74 mm TL after the barrier had opened (Figure 6.18).

Table 6.11. Summary of results of 1-way PERMANOVA testing for differences in the mean gut fullness (PERMDISP p=0.002) and mean TL (PERMDISP p=0.46) of Atherinosoma microstoma from before to after barrier openings (i.e. status) at Wamberal Lagoon. Data was square-root transformed. Mean gut fullness Mean TL Source df MS Pseudo-F p df MS Pseudo-F p Status 1 0.26 4.58 0.03 1 3.41 88.6 0.0001 Residual 70 0.05 70 0.04

224 Chapter 6: Diets of fishes in ICOLLs

1 Mean gut fullnessgut Mean

0 Before After Barrier status

Figure 6.17. The mean gut fullness (±se) of Atherinosoma microstoma at Wamberal Lagoon before and after the barrier opening.

20 % frequency% 10

0 45-54 55-64 65-74 75-84 TL (mm) before (n=180) after (n=180) Figure 6.18. Length-frequency distribution of Atherinosoma microstoma used in dietary examination at Wamberal Lagoon before and after barrier opening.

6.3.4 Ambassis jacksoniensis-Terrigal Lagoon Terrigal Lagoon was unique during this study, as the ICOLL was sampled while the barrier was opened (barrier status=open) and after the barrier had closed (barrier status=after). A total of 120 guts (60 before barrier opening, 60 after barrier closure) of Ambassis jacksoniensis were examined. Gut contents contained six broad dietary categories that included crustaceans, insects, bivalves, nematodes, polychaetes and zooplankton (Appendix 1d). The number of empty guts represented 23.3% (n=14) and 31.7% (n=19) of the guts examined before and after barrier closure respectively. The dietary categories and the relative amounts differed within the guts examined, especially for planktonic copepods and unidentified zooplankton (Figure 6.19). The

225 Chapter 6: Diets of fishes in ICOLLs

gut contents of Ambassis jacksoniensis at Terrigal Lagoon did not change significantly from when the barrier was open to after barrier closure (Table 6.12).

100 Unidentifiable zooplankton* Decapods*

80 Copepods*

Bivalves*

Amphipods* 60 Unidenifiable material

Sediment % volume % 40 Polychaetes

Plant material

Nematodes 20 Terrestrial insect

Bivalves

0 Copepods Before After Barrier status Amphipods

The mean number of taxonomic units and the mean number of dietary items in gut contents differed significantly in guts collected when the barrier was open and after barrier closure (Table 6.13 and Figures 6.20 a,b).

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Table 6.13. Summary of results of univariate PERMANOVA testing for differences in mean numbers of taxonomic units (PERMDISP p=0.19) and the mean number of dietary items (PERMDISP p=0.28) for Ambassis jacksoniensis from open to after (i.e. barrier status) barrier closure at Terrigal Lagoon. Data was untransformed. Mean no. of taxonomic units Mean no. of dietary items Source df MS Pseudo-F p MS Pseudo-F p Status 1 21.10 9.87 0.004 5362 9.70 0.005 Residual 20 2.14 552.87

(a)

Mean no. of taxonomicunitsof no. Mean 0 Open After Barrier status

(b)

Mean no. of dietaryitemsof no. Mean 0 Open After Barrier status

Figure 6.20. Mean number (±se) of taxonomic units and mean number (±se) of dietary items (b) of Ambassis jacksoniensis open and after (i.e. barrier status) barrier closure at Terrigal Lagoon.

The mean gut fullness and the mean TL did not change from open to after the barrier opening (Table 6.14 and Figure 6.21). The range in fish length differed from 45-74 mm TL (open) and 52-80 mm TL (after) the barrier closure (Appendix 1d). The highest percentage frequency of fish sampled while the barrier was open ranged in size from 55-69 mm TL compared to 60-69 mm TL after the barrier closure (Figure 6.22).

227 Chapter 6: Diets of fishes in ICOLLs

1 Mean gut fullnessgutMean

0 Open After Barrier status

Figure 6.21. Mean gut fullness (±se) of Ambassis jacksoniensis at Terrigal Lagoon open and after the barrier closure.

50 45 40 35 30 25 20 15 % frequency% 10 5 0 45-49 50-54 55-59 60-64 65-69 70-74 TL (mm) open (n=60) after (n=60) Figure 6.22. Length-frequency distributions of Ambassis jacksoniensis used in dietary examination at Terrigal Lagoon from open to after barrier closure.

6.4 Discussion

6.4.1. General overview of diets of fishes in ICOLLs A variety of food items were consumed by fishes in Central Coast ICOLLs. Food items such as amphipods, bivalves, polychaetes, terrestrial insects and zooplankton were common dietary

228 Chapter 6: Diets of fishes in ICOLLs

items of all three species. Plant material and sediment were also common items found in the guts of all species although they were not considered to be food items in this study.

Acanthopagrus australis is a commercial species that utilises ICOLLs as nursery areas, and the diet of this species changes with increasing age and length (Chuwen et al. 2007). In this study, the lengths of the fishes sampled (range=38-82 mm TL) suggested that they were juveniles, and less than 2 years old (Rowling et al. 2010). Yellow-fin bream primarily consumed epifauna, including amphipods, gastropods and chironomid larvae, along with infaunal polychaetes. Plant material was also a major component of the gut with a 26% estimated volumetric contribution. In most cases, the consumption of plant material could be considered incidental, since plants may be ingested along with the accompanying epifauna when foraging. However, many sparids have been known to intentionally consume plant material as they possess the appropriate enzymes required for digesting and utilising it (Chuwen et al. 2007). The majority of guts analysed showed that yellow-fin bream rarely had empty guts, with gut fullness generally high, and, along with the variety of taxa consumed, these data show that A. australis is an opportunistic feeder. Sparids, including A. australis, were found to be opportunistic feeders in other ICOLLs (Chuwen et al. 2007; Hadwen et al. 2007), and also in permanently open estuaries (Morton et al 1987), or both types of estuaries (Sarre et al 2000).

Results of this study indicate that Acanthopagrus australis is an opportunistic omnivore that feeds throughout the entire water column, and that they rarely had empty guts, which is comparable to studies by Morton et al. (1987) and Hadwen et al. (2007). The major dietary items retrieved from gut analysis were crustaceans, polychaetes, plant material and bivalves. Chuwen et al. (2007) found another sparid, Acanthopagrus butcheri, from Western Australian ICOLLs, to have similar dietary characteristics to A. australis in the current study.

In comparison, Atherinosoma microstoma is a small fish (maximum size sampled 82 mm TL) which has no commercial importance, but is sometimes used by recreational fisherman as bait and as a food resource by predatory fishes and birds (Prince et al. 1982). Small-mouthed hardyheads occurred in high abundances in both Avoca and Wamberal Lagoons. This species occurred throughout Wamberal Lagoon but was only found near the entrance within Avoca Lagoon. Avoca Lagoon hardyheads consumed a variety of epifauna, including amphipods, bivalves, isopods, chironomid larvae and infaunal polychaetes. Terrestrial insects, zooplankton, plant material and sediment were also consumed. The taxa consumed by small-mouthed hardyheads at Wamberal Lagoon were similar to the taxa consumed by hardyheads at Avoca Lagoon, except that mayfly nymphs and nematodes were found in the gut contents of these fishes at Wamberal Lagoon. Gut fullness and the number of empty guts differed between fishes

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from the latter two ICOLLs, with hardyheads from Avoca Lagoon having a higher number of empty guts and lower gut fullness compared to hardyheads from Wamberal Lagoon.

Differences in gut fullness and the number of empty guts between hardyheads in the two ICOLLs can be related to a number of factors. Firstly, atherinids lack a true stomach and digestion tends to be rapid, hence the high incidence of empty guts and low gut fullness (Prince et al. 1982). Secondly, hardyheads at Wamberal Lagoon, were more widely distributed throughout the ICOLL, so a wider range of food items was likely to be available to this species (Becker and Laurenson, 2008).

Similarly, diets of Atherinosoma microstoma have been studied extensively in Western Australia (Prince et al. 1982; Humphries and Potter 1993) and Victoria (Crinall and Hindell 2004; Becker and Laurenson 2007). These studies found dietary preferences similar to those reported here, with the main dietary items including polychaetes, crustaceans, zooplankton and molluscs. Diets were also found to frequently contain sediment and plant material; however, this could be the result of incidental ingestion when foraging, especially in seagrass habitats (Humphries and Potter 1993). High volumetric contributions of macerated material were also common in A. microstoma, which is probably due to the rapid digestion of foods associated with the lack of a discreet stomach in atherinids (Prince et al. 1982; Crinall and Hindell 2004).

Ambassis jacksoniensis is also a small fish species (maximum size sampled 70 mm TL) that has no recreational or economic significance, but is also a common and abundant species found in most ICOLLs (Griffiths 1998). Glassfish consumed a variety of food items, but predominately consumed microcrustacean zooplankton. Terrestrial insects, polychaetes, plant material and sediment were also consumed. Most fishes collected spanned the mid-size range of the species (i.e. 55-69 mm TL), indicating that the diversity of food items consumed here was unlikely to reflect ontogenetic changes in diets (Mazumder et al. 2006). The majority of guts analysed showed that glassfishes had a high number of empty guts, yet the gut fullness was generally high.

Studies on the diets of Ambassis jacksoniensis show similar trends to the current study, with this species feeding on a variety of prey items, but preferring zooplankton, mainly crustaceans (Hollingsworth and Connolly 2006; Mazumder et al. 2006; McPhee 2009). These latter studies found that A. jacksoniensis had a preference for crab larvae; however, the current study found that planktonic calanoid copepods were preferred. It is difficult to compare dietary preferences here, as zooplankton were also not sampled and adult crabs and copepods were not present amongst the invertebrate fauna sampled within Terrigal Lagoon and (see Chapter 3). However,

230 Chapter 6: Diets of fishes in ICOLLs

the sampling methods used in the invertebrate survey did not target these individuals. Also, adult copepods were present in the gut contents of A. jacksoniensis and it could be possible for planktonic copepods to enter the ICOLL during the many barrier openings (Aguiaro et al. 2003).

Dietary studies of fishes in ICOLLs have been recently documented for sparids from NSW (Hadwen et al. 2007) and Western Australia (Chuwen et al. 2007; Sarre et al. 2000). Atherinid’s gut contents have been studied in ICOLLs from Western Australia (Humphries and Potter 1993) and Victoria (Becker and Laurenson 2007). Gut analyses of sparids have also been documented in permanently open estuaries from Queensland (Morton et al. 1987), and for atherinids from estuaries in NSW (Mazumder et al. 2006) and Victoria (Crinall and Hindell 2004) estuaries, and for glassfish from NSW estuaries (Hollingsworth and Connolly 2006; Mazumder et al. 2006; McPhee 2009). Most studies identified the food items using the common points method described by Hyslop (1980); however, more recent studies have used stable isotope analysis (Hadwen et al. 2007; Pasquaud et al. 2010). Most of these studies reported similar dietary items to those found in the guts of those species investigated in the current study.

However, many dietary studies of fishes examine the gut contents without determining whether the fish species eats because the food is readily available, or whether they have a liking for a particular food item due to both its availability and its nutritional value. Many species in open estuaries have the advantage that preferred prey items can move with the tidal flow; however, fishes in ICOLLs do not have this benefit and must feed on whatever food items are available, hence many species in these habitats are opportunistic feeders (Becker and Laurenson 2007; Chuwen et al. 2007; Hadwen et al. 2007).

6.4.2 Effects of barrier openings on diets of ICOLL fishes The results suggested that barrier openings had an effect on the composition of the gut contents of Acanthopagrus australis at Cockrone Lagoon and of Atherinosoma microstoma at Wamberal Lagoon, but not for A. microstoma at Avoca Lagoon or Ambassis jacksoniensis at Terrigal Lagoon. The gut fullness for each species did not differ significantly, although A. australis was the only species in which the TL changed significantly from before to after the barrier opening, with the mean length and size range of the yellow-fin bream being greater before barriers had opened. This is possibly due to larger specimens leaving the ICOLLs during barrier openings. The change in gut contents of A. australis from before to after the barrier opening is thus possibly confounded by this change in fish length, as shown by the significant difference in the TL of these fishes before and after barrier openings (Table 6.4). Although the change in TL

231 Chapter 6: Diets of fishes in ICOLLs

from before to after the ICOLL opening was not great (~10 mm), differences in the length of yellow-fin bream can account for differences in dietary items present (Chuwen et al. 2007).

No significant differences were found for the number of taxa in the diet of Ambassis jacksoniensis, or for the number of dietary items examined from Atherinosoma microstoma (Avoca Lagoon). Differences in the numbers of taxa and the numbers of dietary items were probably due to the lower numbers of each species collected from Terrigal and Avoca Lagoons, along with the high number of empty guts there. In most cases, zooplankton abundance and biomass in the diets were generally greater after the barrier was opened, which is in contrast to the findings of Lill et al. (2012), who found abundance and biomass of zooplankton in the diet to be greater before the barrier was opened. Another possibility could be due to the limited number of sites from which each species was collected within each ICOLL. Both species were collected from only two sites within their respective ICOLLs, compared to Acanthopagrus australis and Atherinosoma microstoma that were collected at all sites within their respective ICOLLs.

Generally, shifts in diets of fishes are the result of changing prey items attributed to barrier openings or seasonal variations (Aguiaro et al. 2003). Once a barrier has been opened, ICOLL water levels decrease dramatically, exposing sediments and aquatic vegetation that can alter invertebrate assemblages (Robinson et al. 1983; Dye and Barros 2005b; Gladstone et al. 2006). This can also been seen in the current study (refer to Chapter 3). The effects of barrier openings on the diets of fishes in ICOLLs are not well documented, except for Aguiaro et al (2003), who found that barrier openings in Brazilian coastal lagoons tended to supplement the diet of the clupeid Platanichthys platana (the River Plate sprat), as invertebrate marine species entering during opening events added to the number of taxa available for consumption. However, dietary studies were not compared with a control site, i.e. ICOLLs where the barrier remained closed. The Central Coast ICOLLs have small catchments that are highly developed and are generally artificially opened more than two times per year. Since there are limited studies regarding barrier effects, these results must be regarded as only possible effects in the present case.

The null hypothesis that the changing barrier status of ICOLLs had no effect on the diet of fishes can thus be rejected for Acanthopagrus australis (Cockrone Lagoon) and Atherinosoma microstoma (Wamberal Lagoon), in this case. In contrast, the null hypothesis can here be accepted for Atherinosoma microstoma (Avoca Lagoon) and Ambassis jacksoniensis (Terrigal Lagoon).

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6.5 Conclusions The dietary items consumed by fishes in ICOLLs in the current study were similar, with most species feeding in a range of habitats within each ICOLL. The high mean gut fullness and low number of empty guts of Acanthopagrus australis and Atherinosoma microstoma (Wamberal Lagoon) indicate that these species are generally opportunistic feeders there. This is in contrast to these fishes collected from Avoca and Terrigal Lagoons, which had relatively high numbers of empty guts and low gut fullness. Significant differences were found in the volumetric contribution of gut contents before to after barrier openings in fishes collected from Cockrone and Wamberal Lagoons; however, there were no such significant differences for fishes from Avoca and Terrigal Lagoons, though the latter lagoon was sampled under different opening- closing conditions. The null hypothesis that the changing barrier status of ICOLLs had no effect on the diet of fishes can generally be rejected. Comparisons have shown that fishes in these ICOLLs feed on the resources available within these Central Coast ICOLLs, generally consuming similar dietary items to fishes in other NSW ICOLLs, and therefore the null hypothesis that there is no significant difference between the diets of fishes in Central Coast and other ICOLLs can be accepted.

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Appendices: Frequency of occurrence (%F) and estimated percentage volumetric contributions (%V) of dietary items of fishes in ICOLLs

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Appendix 1a. Frequency of occurrence (%F) and estimated percentage volumetric contribution (%V) of each dietary item and major dietary group (in bold), percentage gut fullness and fish size range (TL) of Acanthopagrus australis sampled from Cockrone Lagoon, before and after barrier opening/closures. Fish samples were collected between February 2009 and June 2010. *denotes data not used in the dietary analysis. # denotes planktonic dietary items. Dietary categories Before After % F % V % F % V Bivalvia 7.2 2.6 2 0.1 Crustacea 13.8 6.2 62 4.4 Amphipoda 12.2 5.5 60.7 4.3 Decapoda 1.1 0.6 0 0 Isopoda 0.5 0.1 1.3 0.1 Diptera 18.9 13.3 26.7 14.1 Chironomid larvae 13.9 9.1 26.7 14.1 Ephemeroptera 5 4.2 0 0 (pre-adult stage) Gastropoda 23.3 20 15.3 2.1 Nematoda 1.1 0.05 0 0 Polychaeta 25 16.3 29.3 18 Terrestrial insects 20 13.2 4 1.7 Zooplankton 1.7 1.2 1.3 0.1 Copepoda (calanoid)# 1.7 1.2 0 0 Unknown eggs# 0 0 1.3 0.1 Plant material 13.9 9 32 17 Sediment* 16.7 4.5 4 0.5 Macerated material* 17.8 13.7 3.3 3 Number of guts examined 180 150 Number of empty guts 15 7 % Mean gut fullness (± se) 2.11±0.10 2.30±0.11 Fish length range (TL mm) 38-82 46-63

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Appendix 1b. Frequency of occurrence (%F) and estimated percentage volumetric contribution (%V) of each dietary item and major dietary group (in bold), percentage gut fullness and fish size range (TL mm) of Atherinosoma microstoma sampled from Avoca Lagoon, before and after barrier opening/closures. Fish samples were collected between February 2009 and June 2010. *denotes data not used in the dietary analysis. # denotes planktonic dietary items. Dietary categories Before After % F % V % F % V Bivalvia 3.3 16.8 1.7 0.7 Crustacea 0 0 8.3 13.3 Amphipoda 0 0 5 7.5 Isopoda 0 0 3.3 5.8 Diptera 3.3 0.3 0 0 Chironomid larvae 3.3 0.3 0 0 Polychaetes 0 0 6.7 13.1 Terrestrial insects 0 0 6.7 11.4 Zooplankton 0 0 10 24.2 Bivalve# 0 0 5 9.9 Copepods (calanoid)# 0 0 5 14.3 Plant material 3.3 33.6 1.7 14.5 Sediment* 50 25 8.3 8.3 Macerated material* 20 24.3 10 14.5 Number of guts examined 30 60 Number of empty guts 13 36 % Mean gut fullness (± se) 0.97 ± 0.19 0.72 ± 0.16 Fish length range (TL mm) 50-63 27-67

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Appendix 1c. Frequency of occurrence (%F) and estimated percentage volumetric contribution (%V) of each dietary item and major dietary group (in bold), percentage gut fullness and fish size range (TL) of Atherinosoma microstoma sampled from Wamberal Lagoon, before and after barrier closures. Fish samples were collected between February 2009 and June 2010. *denotes data not used in the dietary analysis. # denotes planktonic dietary items.

Dietary categories Before After % F % V % F % V Bivalvia 7.8 8.6 2.8 1.7 Crustacea 30.1 22.1 Amphipoda 30.5 30 17.2 16 Isopoda 0.5 0.1 8.9 6.1 Diptera 7.8 13.7 Chironomid larvae 6.7 7.8 16.7 11.9 Ephemeroptera 0 0 2.2 1.8 (pre-adult stage) Gastropoda 9.4 9 25 19 Nematoda 5 5.9 0 0 Polychaeta 21.1 21.5 25.5 20.7 Terrestrial insects 7.2 7.1 11.1 7.3 Zooplankton 0 0.1 Copepoda (calanoid)# 0 0 1.1 0.1 Plant material 1.1 0.9 6.1 3 Sediment* 11.1 5.8 7.2 1.8 Macerated material* 3.3 3.3 9.4 10.6 Number of guts examined 180 180 Number of empty guts 47 24 % Mean gut fullness (± se) 1.53±0.10 1.79±0.09 Fish length range (TL mm) 45-74 52-80

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Appendix 1d. Frequency of occurrence (%F) and estimated percentage volumetric contribution (%V) of each dietary item and major dietary group (in bold), % gut fullness and fish size range (TL) of Ambassis jacksoniensis sampled from Terrigal Lagoon, while the barrier was open and then after barrier closure. Fish samples were collected between February 2009 and June 2010. *denotes data not used in the dietary analysis. # denotes planktonic dietary items. Open After Dietary categories % F %V % F %V Bivalvia 8.3 2.5 1.7 1 Crustacea 26.6 22.2 1.7 3.5 Amphipoda 8.3 6.2 1.7 3.5 Copepoda (calanoid) 18.3 16 0 0 Nematoda 1.7 1.1 0 0 Polychaeta 10 5.8 1.7 2.4 Terrestrial insects 6.7 3.5 8.3 8.6 Zooplankton 56.7 52.2 40.1 49 Amphipoda# 6.7 3.4 0 0 Bivalvia# 11.7 7.4 1.7 0.02 Copepoda (calanoid)# 30 33.4 16.7 23 Decapoda# 5 4.1 0 0 Unidentifiable zooplankton# 3.3 3.9 21.7 26 Plant material 1.7 1.7 3.3 3.6 Sediment* 36.7 9.3 38.3 23.5 Macerated material* 3.3 1.7 10 8.4 Number of guts examined 60 60 Number of empty guts 14 19 Mean gut fullness (± se) 1.50±0.16 1.25±0.15 Fish range (TL mm) 50-68 45-70

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Chapter 7: Trace metal concentrations in sediments and tissues of Mugil cephalus in ICOLLs: effects of ICOLL condition and barrier openings

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7.1 Introduction In many cases, ICOLLs are associated with urban settlements resulting in modified catchments that have historically been used as sinks for pollutants. Many pollutants can be of great concern to both aquatic fauna and flora and humans, as they can change the ecological integrity of ICOLLs as described earlier in Chapter 1. Trace metals are found naturally in the environment, with their background concentrations being influenced by the geology of the area (Jones et al. 2003; Acevedo-Figueroa et al. 2006). Background concentrations of naturally occurring trace metals become elevated when these elements are processed by humans and their waste products re-enter the environment. This is of particular concern as many trace metals can persist in the environment for decades (Davis et al. 2001; Beltrame et al. 2009).

Trace metals in estuaries can be produced from many sources, including lead and cadmium waste from weed and pest sprays, domestic effluents, petroleum-based products, and zinc from galvanised iron waste and copper from brake linings (Payne et al. 1997; Edwards et al. 2001; Davis et al. 2001). Urban dwellings and automobiles are also primary sources of trace metals (Davis et al. 2001). Many elements such as zinc, copper and selenium are essential for human and fish development. In contrast, cadmium and lead are non-essential elements that have no biological function (Kirby et al. 2001a; Duruibe et al. 2007). It is when levels of elements greatly increase that they can potentially result in adverse human and animal health effects (Acevedo-Figueroa et al. 2006; Uysal et al. 2008).

Approximately 90% of the trace metal load that enters ICOLLs bonds to the finer fractions of particulate matter and surface sediments (Forstner and Salomons 1980; Acevedo-Figueroa et al. 2006; Gillis and Birch 2006; Birch and Hogg 2011). Over time pollutants can also become entrapped in the deep sediment layers by further sedimentation (Jones et al. 2003; Hollins et al. 2011), and, disturbing these sediments by dredging, bioturbation and wind-generated currents resuspends the fine sediments within the water column where they can be redistributed or removed from ICOLLs during barrier openings (Acevedo-Figueroa et al. 2006). Once bound to sediments, trace metals can be assimilated by the flora (Batley 1987), invertebrate fauna (Brown et al. 2004; Waring et al. 2005; Fabris et al. 2006), and fish fauna (Campbell 1994; Edwards et al. 2001; Kirby et al. 2001a; Roach et al. 2008).

Fish are generally highly mobile species and can move from one area to another if conditions are not acceptable, therefore they may become exposed to different concentrations of trace metals. However, metals that are bound to fine sediments resuspended into the water column can also be redistributed around ICOLLs by wind induced currents. Sediments that are flushed out of ICOLLs during barrier openings may change the sediment geochemistry thereby possibly

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altering the concentrations of trace metals found within ICOLLs. This has implications for species such as Mugil cephalus that feed on fine organic particulate matter, as their tissues can vary in trace metal concentrations. Also, open barriers increase the salinity within ICOLLs. This is important as salinity reduces the uptake and accumulation of metals by fish, as the rate of their accumulation is inversely proportional to the salinity (Somero et al. 1977; Jezierska and Witeska 2006).

Many ICOLLs have been used for commercial and recreational fishing (Pease 1999), therefore the bioaccumulation of trace metals by fish in ICOLLs is of concern, particularly with respect to species regularly harvested for human consumption. Eating contaminated fish can cause various biochemical disorders in humans (Duruibe et al. 2007). Fishes that forage on the surface layer of sediments, such as mullets, have the potential to accumulate higher levels of trace metals (Eustace 1974; Sultana and Rao 1998; Kirby et al. 2001a; Padmini and Geetha 2007). Mugil cephalus was chosen for the current study as this species is generally robust and abundant in NSW estuaries (Rowling et al. 2010) and is generally tolerant of polluted waterways, although it can be susceptible to high concentrations of trace metals (de Souza and Naqvi 1979). Mugil cephalus has been studied extensively and has been shown to be a good indicator of trace metals in the surrounding environment.

Trace metal levels were shown to vary in different tissues of M. cephalus from different contaminated environments in NSW (Kirby et al. 2001a), Western Australia (Plaskett and Potter 1979) and Tasmania (Eustace 1974), and internationally from India (de Souza and Nagvi 1979; Sultana and Rao 1998; Padmini and Geetha 2007) and Turkey (Yilmaz 2005; Uysal et al. 2008). Pollutants generally accumulate in the liver and gonads (Rashed 2001; Kirby et al. 2001a; Alquezar et al. 2006; Roach et al. 2008). However, these organs are generally not consumed by humans, but other tissues such as the flesh or skin may still contain high levels. In contrast, the effects of increased trace metal concentrations on fishes can be acute and/or chronic (Roach et al. 2008) and include behavioural and metabolic changes, inhibition of spawning, abnormalities in juvenile fishes, and increased mortality (Kirby et al. 2001a; Roach et al. 2008; McKinley et al. 2011).

Although, trace metal concentrations have been documented in sediments and fishes from some NSW ICOLLs (Roy and Crawford 1984; Kirby et al. 2001b; Brown et al. 2004; Gillis and Birch 2006), there is limited information on the influence that catchment development and barrier openings may have on the trace metal content of sediments and fish in ICOLLs. Information about trace metals in the environment and biota of ICOLLs is important and necessary because of increasing development within their catchments and human intervention affecting the natural

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dynamics of ICOLLs (e.g. artificial openings). Therefore, the main aim of this study was to understand the effects of catchment development and barrier openings on the occurrences of trace metals in ICOLLs. This study tested the following null hypotheses: 1. There are no differences in the trace metal levels of sediments between pristine and impacted ICOLLs. 2. The frequency of barrier openings has no influence on trace metal levels in sediments of ICOLLs. 3. There are no differences in trace metal levels for gonad and liver tissues of Mugil cephalus between pristine and impacted ICOLLs.

7.2 Materials and methods

7.2.1 Study site This study was conducted at 6 ICOLLs on the NSW coast located to the north and south of Sydney (Figure 7.1). Each ICOLL was identified by using a number of criteria such as catchment land cover, land-use, catchment hydrology, estuary use and ecology as determined by the National Land and Water Resources Audit (NLWRA 2002). The criteria used were changes in urban land use, the effects of increased sedimentation and nutrients and the frequency of artificial barrier openings (Heap et al. 2001, OzCoasts 2010). ICOLLs to the north of Sydney that were studied included ICOLLs classified as extensively-modified (Cockrone Lagoon 33.494°S 151.429°E and Wamberal Lagoon 33.430°S 151.449°E), modified (Avoca Lagoon 33.465°S 151.436°E and Terrigal Lagoon 33.444°S 151.444°E); and near-pristine ICOLLs located to the south of Sydney that were studied included Termeil Lake (35.46°S 150.39°E) and Meroo Lake (35.48°S 150.39°E). All of these ICOLLs are described in detail in Chapter 2 and their condition classification is described by the Geosciences Australia website (Ozcoasts http://www.ozcoasts.gov.au).

Surface sediment collection sites occurred where gill nets were deployed, and only where the target species, Mugil cephalus, was caught (Figure 7.1). In some cases, multiple sites in each of these ICOLL were sampled to obtain the required numbers of M. cephalus (n=10) for trace metal analysis. Meroo Lake was sampled in November 2011 and February 2012 (n=4 sites) and Termeil Lake was sampled in March 2012 (n=2 sites). Cockrone (n=1 site) and Avoca (n=2 sites) Lagoons were sampled during October 2011 and February 2012 respectively. Terrigal Lagoon (n=1 site) was sampled during October 2011 and April 2012 and Wamberal Lagoon (n=1 site) was sampled during November 2011 and April 2012 (Figure 7.1).

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7.2.2 Study species Trace metals were examined in the liver and gonads of the sea mullet, Mugil cephalus (Mugilidae). Mugil cephalus can grow to 50 cm and up to 10 yr old (Rowling et al. 2010). This species is a benthic feeder that forages on sediment surface layers, plant surfaces and submerged rocks (Eustace 1974), feeding on the micro-algae (benthic and epiphytic), plant detritus and inorganic particles of sediments (Thomson 1954). Mugil cephalus were collected in each ICOLL using three replicate multi-panel gill nets deployed at a selected site, approximately 30 m apart for 3 hr, or until 10 individuals were captured. Unfortunately, in most cases 10 individuals of M. cephalus could not be collected in the allocated sampling time, therefore sample sizes were small. To avoid contamination in the field, care was taken not to allow fishes to come into contact with the aluminium boat. Retrieved fishes were handled using rubber gloves and sealed into individual polyethylene bags and euthanased in an ice slurry. The ice slurry was changed regularly to avoid any contamination. The mullet were then stored on ice in a cooler until being returned to the laboratory. Once in the laboratory the fishes were stored at - 20°C until they were processed. Other species caught in the gill nets were removed from the nets, identified and measured to the nearest 1 mm TL and released at the point of capture. Specimens were collected with permission from the University of Newcastle’s Animal Care and Ethics Committee (ACEC Permit number A-2011-126) and the NSW Department of Primary Industries (Fisheries Permit number P05/0092).

7.2.3 Sediment collection Four replicate samples of sediment were collected within an area of 1 m2 at each site by a Petersen Grab (15 cm3). Grab sampling is the preferred method for collecting surface sediments as it can collect a range of sediments, minimises washout of fine grain sediments and protects the sample from being disturbed after collection (Simpson et al. 2005). To avoid contamination from the grab, a subsample of approximately 250 g was collected from the middle of each grab sample using a polyethylene bag (Forstner and Salomons 1980). The four subsamples were combined to make one sample from each site and placed into a fresh polyethylene bag and sealed airtight. The sample was placed on ice in a dark container until it was returned to the laboratory and stored at -20°C until processed.

7.2.4 Environmental variables Environmental variables recorded at the time of sampling included salinity (ppt), turbidity (ntu), temperature (°C), dissolved oxygen (mg/L) and pH. They were recorded in situ at a depth of 0.5 m using a Yeo-Kal 611 Water Quality Analyser. Some measurements were not recorded due to probe malfunction. In this case water samples were collected, placed on ice and frozen in the

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laboratory until measured. Environmental variables were measured only where gill nets were deployed and where the target species were caught.

7.2.5 Sediment processing and analysis Sediment samples were processed and analysed according to the US EPA method 200.8 (1994) in the sediment laboratory of the University of Sydney. Metals analysed included: aluminium (Al), arsenic (As), cadmium (Cd), calcium (Ca), chromium (Cr), cobalt (Co), copper (Cu), iron (Fe), manganese (Mn), nickel (Ni), lead (Pb), selenium (Se) and zinc (Zn). A subsample of each sample (5g) was placed in a beaker with distilled water filled to 100 mL to allow any salts to be dissolved from the sediment. Samples were soaked in this way for 24 hr, after which the water was decanted off, and the sediment placed in an oven to dry for 24 hr at 60°C. Once dried, samples were prepared for digestion. Muddy samples were crushed using a mortar and pestle. Approximately, 0.5 g of sediment was placed into a test tube to which 10 mL of ultra-high purity water was added, along with 2 mL of nitric acid and 2 mL of hydrochloric acid. The mixture was then heated in a water bath for 2 hr at 120°C. After 2 hr, the sample was removed and allowed to cool at room temperature, then made up to 30 mL with ultra-high purity water. Samples were mixed and allowed to settle for 48 hr, when approximately 10 mL of solution was poured off into sample tubes for analyses of trace metal concentrations. The instrument used to analysis sediment samples at the University of Sydney was a Varian 720-ES Optical Emission Spectrometer which utilise Inductively Coupled Plasma Atomic Emission Spectrocopy (ICP-AES).

Samples of sediments that had high contents of sand or mud were replicated to ensure reproducibility of results (Beltrame et al. 2009). A blank and reference material AGAL-10 river sediment (Australian Government Laboratories Reference Material-Hawkesbury River Sediment) were included in the digestion and analysis (Table 7.1) (Birch and Hogg 2011).

Trace metals are found in fine sediments of coastal waterbodies (Gillis and Birch 2006), therefore, a subsample of sediment was wet sieved through a 63 µm sieve to determine the percentage of sediment sample in this size fraction. Both the fine material (<63 µm) and sand component (>63 µm) were allowed to settle for 24 hr before the water was extracted off and the sediment was placed in an oven at 60 °C for 48 hr. Samples were then weighed to calculate the fraction of fine material (<63 µm). Once calculated the data were used to normalise the trace metal results to account for differences in the amounts of fine sediment among samples and ICOLLs (Gillis and Birch 2006).

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Table 7.1. Mean trace metal concentrations (±s.e.) and detection limits for sediment reference material (AGAL-10 river sediment) and the lowest level established by ANZECC and ARMCANZ (2000) and Interim Sediments Quality Guidelines (ISQG- in mg/kg). (-) no guidelines available. Metals Reference values Reference detection limits ISQG-low (mg/L) (mg/L) (mg/kg) Aluminium 8950±1400 0.01 - Arsenic 17.2±3 0.05 20 Calcium 2060±140 0.001 - Cadmium 9.33±0.64 0.1 1.5 Cobalt 9.16±1.11 0.05 - Chromium 82±11 0.01 80 Copper 23.2±1.9 0.01 65 Iron 20000±1170 0.01 - Manganese 241±10.5 0.005 - Nickel 17.8±2.7 0.05 - Lead 40.4±2.7 0.1 50 Selenium 11±1.4 0.1 - Zinc 57±4.2 0.005 200

7.2.6 Fish tissue collection and trace metal analysis Individual sea mullet were measured to the nearest mm TL and weighed to the nearest g. Fishes were then dissected to remove liver and gonad tissues. These organs were chosen for analysis as the liver is a site for the storage, detoxification and elimination of metals in fishes and the gonads are also known as storage sites of metals (Kirby et al. 2001a; Alquezar et al. 2006; Roach 2008). Only liver samples were collected from sea mullet at Cockrone Lagoon as gonads were not fully developed in these fishes due to their small size (<220 mm TL). Each fish was dissected on a plastic sheet with the instruments and dissection area cleaned between dissections with 70% ethanol (v/v) (Kirby et al. 2001a). Liver and gonad samples were collected from the middle portion of the organ, and weighed in a sterile vial to obtain approximately 100 mg of tissue. All gonad samples were taken from the left gonad in order to standardise the analysis. Once measured, samples were frozen at -20°C until they could be digested and analysed.

Trace metal concentrations were determined at the University of Technology, Sydney. Metals analysed included: Al, As, boron (B), Ca, Cd, Cr, Cu, Pb, Mn, molybdenum (Mo), Se, silver (Ag), strontium (Sr) and Zn. Tissue samples were added to teflon jars along with 1 mL of nitric acid and 1 mL of hydrogen peroxide. The mixture was then heated on a hot plate for 1.5-2 hr at 80°C. Each sample was then poured into a clean tube that had been rinsed twice with ultra-pure water to remove any residual liquid. The liquid transferred was weighed and stored in a

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refrigerator at 4°C until analysed using Inductively Coupled Plasma Mass Spectrometry (ICP- MS). Each liver and gonad sample was replicated in order to ensure reproducibility of results. A blank and reference material DOLT-4 dogfish liver (National Research Council Canada) was included in the digestion and analysis (Table 7.2).

Table 7.2. Mean trace metal concentrations (±s.e.) for tissue reference material (DOLT-4 dogfish liver) and guidelines from ANZFA (1999). *indicates the level was below detectable limits or (-) no guidelines available. Metals Reference values (µg/g) ANZFA limits (mg/kg) Aluminium 133.97±79.94 - Arsenic 26.30±15.56 2.0 Boron 0.55±0.29 - Calcium 179.32±101.40 - Cadmium 63108±39259 2.0 Chromium 1.06±0.72 - Copper 79.17±47.41 10.0 Manganese 28.25±16.72 - Lead * 0.5 Molybdenum 0.86±0.57 - Selenium 28.97±16.14 - Silver 0.82±0.55 - Strontium 26.57±12.27 - Zinc 283.02±178.78 200

7.2.7 Data analysis A Pearson’s (r) correlation was used to test the relationship between the percentage of fine sediments (<63 µm) from each ICOLL and the relationship between the concentration of individual trace metals (Cr, Cu, Fe, Zn) and the frequency of barrier openings that occurred at each ICOLL between February 2009 and April 2012. Barriers at Meroo and Termeil Lakes were not opened during this study period, while Cockrone and Wamberal Lagoons had opened 4 times, Avoca Lagoon 7 times, and Terrigal Lagoon 24 times. Pearson’s correlation was used to test the null hypotheses that the frequency of barrier openings has no influence on trace metal levels in sediments of ICOLLs. Pearson’s correlation was also used to test the relationship between concentrations of individual metals in the liver and gonads of Mugil cephalus, and their TL (cm) and mass (g), and also to determine if there was any correlation between the levels of trace metals in ICOLL sediments and the their levels in the liver and gonad tissues of the sea mullet. The statistical package used for Pearson’s correlation was SPSS v20.

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Non-parametric multivariate analysis was used to test for differences in the trace metal content of sediments and tissues of Mugil cephalus from the different ICOLLs. Of all the elements tested, only trace metals considered as being the result of catchment modifications (As, Cd, Cr, Cu, Fe, Pb and Zn) (Davis et al. 2001; Waugh et al. 2007) were used in the multivariate analyses. Some elements were not analysed as they were below detectable levels in either or both sediments (As, Cd, Pb and Se) and fish organs (Cd and Pb). Data were square-root transformed prior to analysis (Clarke 1993). A two-way permutational multivariate analysis of variance (PERMANOVA) was used to test the null hypothesis that there are no differences in the trace metal contents of sediments between near-pristine and impacted ICOLLs using the following factors: Status (fixed, 3 levels, near-pristine, modified and extensively-modified) and ICOLLs (random, 6 levels) nested in status.

One-way PERMANOVA was used to test for significant differences in mean length and weight of Mugil cephalus amongst ICOLLs. Where significant differences were found, length and weight of M. cephalus were added to the two-factor PERMANOVA as co-variates. A two factor PERMANOVA was used to test the null hypothesis that there was no variation in the trace metal content of liver and gonad tissue of M. cephalus among ICOLLs using the following factors: Status (fixed, 3 levels, near-pristine, modified and extensively-modified), ICOLLs (random, 6 levels) nested in status. One-way PERMANOVA analyses were based on a Euclidean distance similarity matrix, with other analyses based on the Bray-Curtis similarity matrix. Significance of the F-values was determined by 9999 permutations under a reduced model. Monte Carlo p-values were used when the maximum possible number of permutations was less than 30 (McKinley et al. 2011). Multi-dimensional scaling ordination (MDS) plots were used to visualise spatial differences in trace metals.

Significant effects in a PERMANOVA analysis can be caused by differences in the location (in multivariate space) and/or variability of the levels of the significant factor (Anderson et al. 2008). When a significant result was found the PERMDISP routine was used to test for homogeneity of variability between groups by comparing the average of distances of samples from their group centroids (Anderson 2004).

A two-way PERMANOVA was also used to test any variations in individual trace metal content (As, Cr, Cu, Se, Zn) in liver and gonad tissue for Mugil cephalus among ICOLLs using the following factors: Status (fixed, 2 levels, gonad tissue, and liver tissue), ICOLLs (random, 6 levels) nested in status. All multivariate and univariate analyses were done using PRIMER v6 and PERMANOVA+ (PRIMER-E).

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7.3 Results

7.3.1 Environmental variables During the actual sampling period for heavy metal analysis, the barriers at Avoca, Terrigal and Wamberal Lagoons were opened once (Table 7.3). The mean salinity of the two near-pristine ICOLLs, Meroo and Termeil, were 1.76 and 6.59 ppt respectively, compared to the modified ICOLLs Avoca and Terrigal, which had mean salinities of 25.59 and 21.80 ppt respectively. Cockrone Lagoon had a mean salinity of 7.73 ppt, while Wamberal Lagoon had a mean salinity of 31.92 ppt. Differences in salinities were due to Avoca, Terrigal and Wamberal Lagoon barriers being artificially opened before the sampling period. In most cases, water temperature, dissolved oxygen (DO), pH and water depth were relatively similar across all ICOLLs (Table 7.3).

7.3.2 Trace metal concentrations in ICOLL sediments In the majority of cases sediment samples were collected from one site only and at one sampling time for some ICOLLs during this study, therefore, each sample was pooled together for that particular site and time. Also, since most ICOLLs did not have barrier openings during this sampling period, the number of barrier openings described in Chapter 5 was also included in the analysis. Terrigal Lagoon had the greatest percentage of fine sediments (i.e. <63 µm, 34.67%) and Cockrone Lagoon had the lowest percentage (0.65%) (Figure 7.2). There was no correlation (r=0.255, n=15, p=0.63) between the percentage of fine sediments (n=the number of pooled sediment samples) and the number of barrier openings. Trace metal levels for sediments varied across ICOLLs, with Cockrone Lagoon having the highest content of trace metals (Figure 7.3). Amounts of As, Cd, Co, Ni, Pb and Se were all found to be below detectable limits in all of the ICOLLs.

7.3.2.1 Aluminium Al was detected in all ICOLLs with the greatest concentration of 89 022 mg/L being found at Cockrone Lagoon, which classed as an extensively-modified ICOLL. Mean Al concentrations from the near-pristine ICOLLs of Meroo and Termeil Lakes were also higher, 59 977 and 49 932 mg/L respectively, than from the other three remaining ICOLLs. The lowest concentration of 34 355 mg/L was found at Terrigal Lagoon, a modified ICOLL (Figure 7.3a).

7.3.2.2 Calcium Mean Ca concentrations were very low across all ICOLLs with the exception of Cockrone Lagoon, which had a value of 368 346 mg/L. Concentrations of less than 50 000 mg/L were found at Avoca Lagoon and Meroo and Termeil Lakes (Figure 7.3b).

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40 35 30 25 20 15 10 5

0 % fine sediment (<63µm) sedimentfine%

ICOLLs

Figure 7.2. Percentage composition of fine sediments (<63 µm) subsampled from sediments collected from each of the 6 ICOLLs. Denotes *near-pristine, **modified and ***extensively- modified ICOLLs.

7.3.2.3 Chromium Mean Cr concentrations were found to be similar to those of Al. Cr was recorded in all ICOLLs, and the highest concentration of 242.15 mg/L occurred at Cockrone Lagoon. Concentrations of chromium from the near-pristine ICOLLs of Meroo and Termeil Lakes were also higher, 67.67 and 81.61 mg/L respectively, than from the other three remaining ICOLLs. The lowest concentration of 38.44 mg/L was found at Wamberal Lagoon, an extensively-modified ICOLL (Figure 7.3c).

7.3.2.4 Copper Cockrone Lagoon had the highest mean Cu levels of 134.6 mg/L, with Wamberal Lagoon having the lowest levels at 15.55 mg/L. The levels at the near-pristine ICOLLs of Meroo and Termeil Lakes were lower, 23.12 and 28.08 mg/L respectively, than from the modified ICOLLs of Avoca and Terrigal Lagoons (37.48 and 30.38 mg/L respectively) (Figure 7.3d).

7.3.2.5 Iron Mean Fe concentrations were highest at Cockrone Lagoon (742 384 mg/L), with the lowest at Wamberal Lagoon (43 794 mg/L). Avoca Lagoon and Meroo Lake had similar values of 102 096 and 81 473 mg/L respectively (Figure 7.3e).

250

Table 7.3. Environmental variable ranges and means ± s.e. for surface waters and average depth for all ICOLLs at sites where the target species was collected. # derived from (OEH, 2011). *indicates ICOLL had opened once during this sampling period. Environmental variable ranges (means± s.e.) and average depth # Salinity (ppt) Temperature Turbidity DO pH Depth ICOLL Condition (°C) (ntu) (mg/L) (m) Meroo Near-Pristine 1.0–2.0 21.54–25.30 0.76–1.69 3.70–5.30 5.72-8.32 0.9 (1.76±0.05) (23.06±0.40) (1.27±0.27) (4.4±0.1) (6.96±0.23) Termeil Near-Pristine 2.9–8.4 22.52–25.64 1.29-3.19 3.80–5.60 7.53–8.38 0.7 (6.59±0.59) (24.49±0.48) (2.19±0.41) (5.0±0.3) (7.94±0.10) *Avoca Modified 18.53-33.50 23.46–26.10 0.13–0.25 3.90–6.90 7.20–8.23 0.4 (25.95±3.27) (24.80±0.54) (0.19±0.03) (5.4±0.6) (7.71±0.22) *Terrigal Modified 16.51–25.70 17.60–20.03 2.55–3.94 4.70–6.60 7.60-7.68 0.5 (21.18±2.03) (18.57±0.45) (3.15±0.41) (5.7±0.3) (7.65±0.01) Cockrone Extensively- 5.75–9.70 20.37–26.10 0.17–0.40 7.30–8.20 7.58–8.96 0.6 Modified (7.73±0.88) (23.55±1.17) (0.28±0.07) (7.8±0.1) (8.29±0.29) *Wamberal Extensively- 29.79–34.10 15.70–23.98 5.78–8.83 5.20–7.20 7.75–7.84 1.7 Modified (31.92±0.95) (19.85±1.84) (6.98±0.94) (6.2±0.4) (7.79±0.02)

Chapter 7: Trace metals in ICOLLs

7.3.2.6 Manganese Cockrone Lagoon had the highest mean Mn concentration level of 4 042 mg/L with Terrigal Lagoon having the lowest level at 96.83 mg/L. The levels at the near-pristine ICOLLs of Meroo and Termeil Lakes were lower, 199.48 and 269.33 mg/L respectively, than the modified ICOLL of Avoca Lagoon 355.69 mg/L, but higher than the extensively-modified ICOLL of Wamberal Lagoon (107.09 mg/L) (Figure 7.3f).

7.3.2.7 Zinc Mean concentrations of Zn were highest at Cockrone Lagoon (851.35 mg/L) and lowest at Wamberal Lagoon (44.85 mg/L). Concentrations of Zn from the near-pristine ICOLLs of Meroo and Termeil lakes were lower, 153.7 and 177.35 mg/L respectively, than from the modified ICOLLs of Avoca and Terrigal Lagoons (182.81 and 211.86 mg/L respectively) (Figure 7.3g).

(a) Aluminium (b) Calcium

140000 800000 700000 120000 600000 100000 500000 80000 mg/L 400000 60000 300000 40000 200000 20000 100000 0 0

350 200 300 180 160 250 140 200 120 100 mg/L 150 80 100 60 50 40 20 0 0

(e) Iron (f) Manganese

1000000 6000 900000 5000 800000 700000 4000 600000 mg/L 500000 3000 400000 2000 300000 200000 1000 100000 0 0

252 Chapter 7: Trace metals in ICOLLs

(g) Zinc

1200 1000 800

mg/L 600 400 200 0

ICOLLs Figure 7.3. Mean (± s.e.) of trace metal in fine sediments (<63 um). Sample sizes for each ICOLL include; Meroo (n=4), Termeil (n=2), Cockrone (n=2), Avoca (n=2), Terrigal (n=1) and Wamberal (n=1). (a) Al, (b) Ca, (c) Cr, (d) Cu, (e) Fe, (f) Mn, and (g) Zn. Denotes *near-pristine, **modified and ***extensively-modified ICOLLs.

There was no correlation between the concentrations of individual metals (Cr, Cu, Fe, and Zn) and the number of barrier openings (Table 7.4).

7.3.3 Multivariate analysis The suite of trace metals in sediments was not affected by the modification status of ICOLLs (Table 7.5), and there was only a marginally non-significant difference among the ICOLLs within each status category (Table 7.5). The MDS plot illustrates differences, and overlap, in the suite of trace metals in the sediment from the ICOLLs. The value of stress for the MDS was strong (0.01), with patterns of trace metals between ICOLLs evident. Replicates from Cockrone Lagoon (extensively-modified) are located to the left of the ordination plot, only replicates from Meroo Lake (near-pristine) are located to the right of the ordination plot, and there is broad overlap of samples from all other ICOLLs Figure 7.4).

253 Chapter 7: Trace metals in ICOLLs

Table 7.5. Summary of results of 2-way PERMANOVA testing for differences in the suite of trace metals of sediments resulting from ICOLL status (near-pristine, modified, extensively-modified), and among ICOLLs within each status category. Source df MS Pseudo-F p Status 2 831.07 0.97 0.63 ICOLL(Status) 3 1096 2.8 0.05 Res 14 392.94

2D Stress: 0.01

7.3.4 Length and weight comparisons of Mugil cephalus The mean TL (cm) and mean weight (g) of Mugil cephalus were greatest from the near-pristine ICOLLs Termeil (43.12 ±4.2 TL cm) and Meroo (895.85±260 g) Lakes respectively (Table 7.6). Cockrone Lagoon had the smallest mean TL and weight of M. cephalus at 20.8±0.2 cm and 103.25±4.6 g respectively.

254 Chapter 7: Trace metals in ICOLLs

Table 7.6. Total length (cm) and weight (g) of Mugil cephalus collected from near-pristine (NP) modified (M) and extensively-modified (EM) ICOLLs. n= number of fish collected. Total length (cm) Weight (g) ICOLLs Status n range mean ± s.e. range mean ± s.e. Meroo NP 3 33.6 – 46.2 41.9 ± 4.2 380.08– 1215.92 895.85 ± 260 Termeil NP 4 41.5 – 45.8 43.12 ± 0.94 833.89 - 1125.02 960.0 ± 64 Avoca M 10 25.4 – 48.3 40.4 ± 2.2 525.33 – 1524.22 841.98 ± 144 Terrigal M 8 33.9 - 45 39.5 ± 1.3 383.92 – 1110.41 695.96 ± 81.4 Cockrone EM 10 19.8 – 21.8 20.8 ± 0.2 87.94 – 132.06 103.25 ± 4.6 Wamberal EM 6 37.6 – 48.1 42.0 ± 1.4 613.41 – 1246.39 833.95 ± 90

Mean TL and mean mass of sea mullet differed significantly among ICOLLs (Table 7.7). Significant differences were further investigated post-hoc by pairwise comparisons. All TL and weight pairwise comparisons between ICOLLs were significant for Cockrone Lagoon and each of the other five ICOLLs, as was the pairwise comparison for the mass of M. cephalus for Termeil Lake and Terrigal Lagoon.

Table 7.7. Summary of results of univariate PERMANOVA testing for differences in the TL (cm) and weight (g) of Mugil cephalus collected from near-pristine, modified and extensively-modified ICOLLs. Univariate dispersions of the TL (PERMDISP p=0.05) and for the weight (PERMDISP p=0.12) were not significantly different. TL (cm) Weight (g) Source df MS Pseudo-F p MS Pseudo-F p ICOLLs 5 664.48 33.55 0.0001 6.37 37.62 0.0001 Res 38 19.81 0.17

7.3.5 Metal concentrations in tissues of Mugil cephalus Concentrations of Cd, Pb and Ag were below detectable limits in both gonad and liver tissues from sea mullet at all ICOLLs.

7.3.5.1 Aluminium The greatest mean concentrations of Al were found in liver tissue compared to gonad tissue, with the exception of fishes collected from Cockrone Lagoon. The greatest levels of Al in liver tissue were from the near-pristine ICOLL Meroo Lake (49.9 µg/g) and the lowest level (0.83 µg/g) was recorded from the extensively-modified ICOLL Cockrone Lagoon. The highest levels in gonad tissue were also from Meroo Lake (14.9 µg/g) and the lowest at the modified ICOLL Terrigal Lagoon (1.21 µg/g) (Figure 7.5a).

255 Chapter 7: Trace metals in ICOLLs

7.3.5.2 Arsenic Mean concentrations of As were found in liver tissue compared to gonad tissue. The greatest levels of As in liver tissues were found at the modified ICOLL Avoca Lagoon (4.67 µg/g) and the near-pristine ICOLL Termeil Lake (4.07 µg/g), and the lowest level (1.52 µg/g) were recorded from the near-pristine ICOLL Meroo Lake. The highest levels in gonad tissue were recorded from the near-pristine ICOLL Termeil Lake (2.02 µg/g), and the lowest at the extensively- modified ICOLL Wamberal Lagoon (0.25 µg/g) (Figure 7.5b).

7.3.5.3 Boron Liver tissue had a higher mean concentration of B compared to gonad tissue, except at Cockrone Lagoon. The greatest levels of B in liver tissues were found at Avoca Lagoon (0.64 µg/g) and the lowest level was recorded from Cockrone Lagoon (0.11 µg/g) Undetectable levels of boron were found at Meroo Lake. The highest levels in gonad tissue were recorded at Cockrone Lagoon (0.55 µg/g) and the lowest level recorded at both Termeil Lake and Terrigal Lagoon (0.09 µg/g) (Figure 7.5c).

7.3.5.4 Calcium Mean concentrations of Ca were generally greater in gonad tissue. The greatest concentrations of Ca were recorded in gonad tissues at Cockrone Lagoon (69.9 µg/g) and the lowest levels found at Terrigal Lagoon (2.61 µg/g). The greatest levels of Ca in liver tissues were found at Meroo Lake (29.3 µg/g) with the lowest levels recorded at Wamberal Lagoon (3.38 µg/g) (Figure 7.5d).

7.3.5.5 Chromium Gonad tissues had the highest levels of Cr compared to liver tissues. The greatest level of Cr in gonad tissues was found at Wamberal Lagoon (0.66 µg/g) and the lowest levels recorded in both Termeil Lake and Terrigal Lagoon (0.07 µg/g). The greatest levels of Cr in liver tissues were recorded at Avoca Lagoon (0.25 µg/g) and Wamberal Lagoon (0.24 µg/g) and the lowest levels found at Cockrone Lagoon (0.04 µg/g) and Termeil Lake (0.05 µg/g) (Figure 7.5e).

7.3.5.6 Copper Liver tissue had the highest levels of Cu across all ICOLLs. The greatest level of Cu in liver tissue was found at Wamberal Lagoon (49.9 µg/g) and the lowest recorded at Meroo Lake (8.02 µg/g). The highest levels in gonad tissue were also found at Wamberal Lagoon (7.47 µg/g) and the lowest levels found at Cockrone Lagoon (0.47µg/g) (Figure 7.5f).

7.3.5.7 Manganese Mean concentration of Mn varied across all ICOLLs, and was undetectable in gonad tissue at Meroo Lake and Terrigal and Wamberal Lagoons. The highest level of Mn in liver tissue was

256 Chapter 7: Trace metals in ICOLLs

recorded at Avoca Lagoon (2.26µg/g) and the lowest level found at Wamberal Lagoon (0.19 µg/g). The highest levels in gonad tissue were recorded at Termeil Lake (1.98 µg/g) and the lowest level found at Avoca Lagoon (1.32 µg/g) (Figure 7.5g).

7.3.5.8 Molybdenum Detectable levels of Mo were found only in liver tissue, with the highest level being recorded at Meroo Lake (1.56 µg/g) and the lowest level recorded at Wamberal Lagoon (0.33 µg/g) (Figure 7.5h).

7.3.5.9 Selenium The highest levels of Se were found in liver tissues compared to gonad tissue. The highest levels of Se in liver tissue were found at Terrigal Lagoon (3.68 µg/g) and the lowest levels recorded at Termeil Lake (1.57 µg/g). The highest levels in gonad tissue were recorded at Wamberal Lagoon (1.12 µg/g) and the lowest levels were found at Termeil Lake (0.28 µg/g) (Figure 7.5i).

7.3.5.10 Strontium Mean concentrations of Sr were higher in gonad tissues, except at Meroo Lake and Terrigal and Wamberal Lagoons, where it was below detectable levels in both liver and gonad tissues. The greatest levels of Sr in gonad tissue were found at Cockrone Lagoon (6.87 µg/g) and the lowest levels were recorded at Termeil Lake (0.83 µg/g). The highest levels in liver tissue were recorded at Meroo Lake (2.47 µg/g) and the lowest levels were found at Termeil Lake (0.52 µg/g) (Figure 7.5j).

7.3.5.11 Zinc Mean concentrations of Zn were higher in gonad tissue compared to liver tissue, except at Cockrone Lagoon. The highest levels of Zn in gonad tissue were found at Wamberal Lagoon (239.9 µg/g) and the lowest levels recorded at Cockrone Lagoon (19.7 µg/g). The highest levels in liver tissue were found at Wamberal Lagoon (91.9 µg/g) and the lowest levels were recorded at Meroo Lake (34.2 µg/g) (Figure 7.5k).

257 Chapter 7: Trace metals in ICOLLs

(a) Aluminium (b) Arsenic 60 6 50 5 40 4 30 3

20 2 ug/g (wet wt) (wet ug/g 10 1 0 0

(e) Chromium (f) Copper 1.2 70 1 60 0.8 50 40 0.6 30 0.4

20 ug/g (wet wt) (wet ug/g 0.2 10 0 0

(g) Manganese (h) Molybdenum 3 3

2 2

1 1 ug/g (wet wt) (wetug/g

0 0

(i) Selenium (j) Strontium 12 5 10 4 8 3 6

2 4 ug/g (wet wt) (wet ug/g 1 2 0 0

258 Chapter 7: Trace metals in ICOLLs

(k) Zinc 300 250 200 150

100 ug/g (wet wt) (wet ug/g 50 0

ICOLLs Figure 7.5. Trace metal levels in liver and gonad tissues of Mugil cephalus. Sample sizes for each ICOLL were: Meroo (n=3), Termeil (n=4), Cockrone (n=10), Avoca (n=10), Terrigal (n=8) and Wamberal (n=6). Levels of trace metals in liver ( ) and gonad ( ) tissues of sea mullet. Mean ± standard error (ug/g wet wt). Wet wt = wet weight. Denotes *near-pristine, **modified and ***extensively-modified ICOLLs.

7.3.6 Multivariate analysis There was no effect of ICOLL modification status on the trace metal content of gonad tissues, with total length and weight of Mugil cephalus included as covariates (Table 7.8). This result is reflected in the MDS ordination plot (Figure 7.6). For example, the samples collected from Meroo and Termeil Lakes (both near-pristine) are located close to the samples for Avoca and Terrigal Lagoons (both modified ICOLLs). The trace metal content of gonads also did not vary among ICOLLs within each status category. This result is also evident in the MDS ordination plot, with samples from Meroo and Termeil Lakes located close to one another on the plot and samples from Avoca and Terrigal Lagoons also located close to one another.

259

Table 7.8. Summary of results of 2-factor PERMANOVA, with total length and weight as co-variates testing for differences in trace metal concentrations in gonad tissues of Mugil cephalus from near-pristine, modified and extensively-modified ICOLLs. Source df MS Pseudo-F p Source df MS Pseudo-F p Length 1 26246 17.26 0.001 Weight 1 23658 16.20 0.002 Status 2 1804 1.57 0.35 Status 2 1124 0.74 0.65 ICOLLs(Status) 3 1033 1.25 0.29 ICOLLs (Status) 3 1489 1.58 0.17 Length x Status 2 1143 1.38 0.24 Weight x Status 2 852.39 0.90 0.44 Length x ICOLLs(Status) 3 1206 1.46 0.20 Mass x ICOLLs (Status) 3 1066 1.13 0.36 Res 23 825.28 Res 23 940.86

Chapter 7: Trace metals in ICOLLs

2D Stress: 0.01

There was no effect of ICOLL status on the trace metal content of liver tissue with total length and weight of Mugil cephalus included as covariates; however, there was a significant effect between ICOLL and modification status (Table 7.9). Post-hoc pairwise tests were used to further investigate the significant differences. Differences in pairwise tests found the interaction occurred between Meroo and Termeil Lakes (both near-pristine) and Avoca and Terrigal Lagoons (both modified). The result is reflected in the MDS ordination plot (Figure 7.7). For example, the samples collected from Meroo and Termeil Lakes (both near-pristine) are separated from each other. This is similar for samples collected from Avoca and Terrigal Lagoons (both modified), however, samples collected from Cockrone and Wamberal Lagoons (both extensively-modified) are located closer together compared to the other ICOLLs. PERMDISP analysis showed this was not caused by significant differences in the variability of trace metal content for the analyses with TL (F=1.48, df=5, p=0.33) and weight (F=1.48, df=5, p=0.34) as covariates.

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Table 7.9. Summary of results of 2-factor PERMANOVA, with length and weight as co-variates testing for differences in trace metal concentrations in liver tissues of Mugil cephalus from near-pristine, modified, and extensively-modified ICOLLs. Source df MS Pseudo-F p Source df MS Pseudo-F p Length 1 1156 2.66 0.11 Mass 1 914.71 2.17 0.18 Status 2 988.15 3.01 0.07 Status 2 867.15 1.98 0.10 ICOLLs (Status) 3 295.86 3.58 0.003 ICOLLs (Status) 3 437.74 5.07 0.0001 Length x Status 2 93.03 1.12 0.34 Mass x Status 2 73.98 0.86 0.50 Length x ICOLLs (Status) 3 39.92 0.48 0.84 Mass x ICOLLs (Status) 3 33.38 0.39 0.90 Res 32 82.63 Res 32 86.24

Chapter 7: Trace metals in ICOLLs

2D Stress: 0.08

Pearson’s correlation (r) was computed to assess the relationship between the concentrations of individual trace metals (As, Cr, Cu, Se, and Zn) in gonad and liver tissues and the TL and mass of sea mullet (Table 7.10) and between trace metals found in ICOLL sediments and those found in both the liver and gonad tissues (Al, Ca, Cr, Cu, Mn and Zn). Copper was highly positively correlated with TL for gonad tissue, and Zn was moderately positively correlated with both TL and mass for gonad tissue. Chromium was the only metal to be moderately positively correlated with the liver for TL (Table 7.10). All other metals were not significantly correlated for TL and weight for liver tissue. No correlations were found between the concentrations of trace metals in ICOLL sediments and liver and gonad tissues of Mugil cephalus.

Table 7.10. Pearson’s correlation coefficients (r) and levels of significance (p) for the relationship between concentrations of individual metals in the liver and gonads of Mugil cephalus, and their TL and mass. * p<0.05 **p<0.001. TL (cm) Mass (g) Trace metal Gonad Liver Gonad Liver Arsenic -0.046 0.214 0.089 0.279 Chromium 0.033 0.349* 0.219 0.389 Copper 0.601** 0.239 0.524 0.160 Selenium 0.103 0.341 0.281 0.262 Zinc 0.399** 0.411 0.448* 0.391

263 Chapter 7: Trace metals in ICOLLs

Univariate analyses of individual trace metal concentrations (Table 7.11) found significant Tissue x ICOLL(Status) interactions for As and Zn. Post-hoc pairwise tests found the interaction occurred because concentrations of As varied between Cockrone and Wamberal Lagoons (extensively-modified) for gonad tissue, and concentrations varied in liver tissue varied significantly between Termeil and Meroo Lakes (near-pristine). Post-hoc pairwise tests found the interaction occurred because concentrations of Zn varied between Cockrone and Wamberal Lagoons (extensively-modified) for gonad tissue, and concentrations varied in liver tissue varied significantly between Avoca and Terrigal Lagoons (modified) and Cockrone and Wamberal Lagoons (extensively-modified).

Trace metal concentrations for Tissue x Status interactions were significant for Cr, and post-hoc pairwise tests found the interaction occurred because concentrations of Cr varied between gonad and liver tissue for Avoca and Terrigal Lagoons (modified). Trace metal concentrations were significantly different for ICOLL(Status) for Cu, and post-hoc pairwise tests found the interaction varied between gonad and liver tissue for Avoca and Terrigal Lagoons (modified). Concentrations of Cu and Se varied significantly between liver and gonad tissues.

264

Table 7.11. Summary of p-value results for 3-factor PERMANOVA testing for differences in trace metal concentrations in liver and gonad tissues of Mugil cephalus from near-pristine, modified, extensively-modified ICOLLs. Data transformed using log(x+1)* and square root** to obtain a PERMDISP that is not significant. *** indicates PERMDISP significant using any data transformation. Trace metals Source As** Cr*** Zn*** Cu* Se*** df MS Pseudo p MS Pseudo- p MS Pseudo- p df MS Pseudo-F p df MS Pseudo-F p -F F F Tissue 1 14263 23.67 0.01 188.09 0.88 0.43 2021 2.32 0.19 1 33.50 135.37 0.00 1 14930 71.21 0.004 1 Status 2 210.93 0.11 0.82 516.23 0.43 0.78 265.41 0.08 1.0 2 2.33 0.57 0.56 2 1342 2.85 0.13 ICOLL (Status) 3 1939 10.14 0.001 1232 2.34 0.06 3550 11.34 0.001 3 4.44 12.34 0.00 3 486 2.37 0.05 2 Tissue x Status 2 433.17 0.68 0.62 1296 6.75 0.04 404.32 0.44 0.76 2 0.26 1.15 0.43 2 656.96 3.13 0.13 Tissue x ICOLL(Status) 3 659.87 3.45 0.004 170.35 0.32 0.87 949.86 3.03 0.01 3 0.21 0.59 0.62 3 210 1.03 0.39 Res 61 191.17 525.41 313.02 52 0.36 60 204.56

Chapter 7: Trace metals in ICOLLs

7.4 Discussion

7.4.1. Environmental variables and sediment characteristics of ICOLLs The environmental features of ICOLLs in the current study were generally similar, with most ICOLLs having a mean water depth of <2 m, which is typical of these shallow water environments. pH levels were 6-8 and turbidity and dissolved oxygen in each ICOLL were generally low. Mean water temperature was characteristic of seasonal temperatures. These environmental features were similar when compared to other ICOLLs from NSW including Smiths Lake (Robinson et al. 1983), Dee Why Lagoon (Allan et al. 1985), Swan and Wollumboola Lakes (Pollard 1994a) and ICOLLs in New Zealand (Schallenberg et al. 2010). The main differences in the environmental features were in mean salinity as Meroo and Termeil Lakes and Cockrone Lagoon had not been opened during the sampling period for this study and therefore mean salinities were low, at <8 ppt. In comparison, Avoca, Terrigal and Wamberal Lagoons had opened before sampling, hence mean salinities were high, at 16-30 ppt. Water variables are often important factors as variations in pH, salinity and water temperature can influence the remobilisation, bioavailability and uptake of trace metals by the biota (Batley 1987; Alquezar et al. 2006; Gillis and Birch 2006). Also, increased turbidity can transport trace metals attached to particulate matter around ICOLLs (Birch and Hogg 2011).

Trace metals are generally associated with the finer organic particles (i.e. <63 µm) of sediments (Roy and Crawford 1984). The results have shown that Terrigal Lagoon had the highest content of fine particles, which is unexpected as it had no aquatic vegetation and frequent barrier openings that can flush out the finer particles from the lagoon sediments. Also, there was no correlation between the amount of fine sediment and the number of barrier openings for the any of the other ICOLLs. Aquatic vegetation can trap and stabilise sediment particles, however finer particles are easily resuspended into the water column and can be moved around ICOLLs by wind currents or flushed out when the barrier has opened. Also, there is little change in sediment composition over a single year, with deposition generally being patchy and associated with heavy rainfall (Anderson et al. 2004). Given these factors, it is possible to suggest that no correlation between fine sediments and barrier openings would be expected.

A summary of the results of the current study show that trace metals in ICOLL sediments varied and were generally low, with As, Cd, Co, Ni, Pb and Se all being below detectable levels. The definition of a healthy estuary states that there is no change in biodiversity over time and over and above the natural variations that occur; the health of the Central Coast ICOLLs may thus be regarded as healthy, in relation to trace metal pollution. This is in contrast to many estuarine

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Chapter 7: Trace metals in ICOLLs

environments that are regarded as polluted environments due to high industrial activity and increased development within their catchments. Trace metal levels in sediments were all found to be higher in Cockrone Lagoon, which may be attributed to sediment samples having been collected near a stormwater outlet (Gillis and Birch 2006; McKinley et al. 2011). There were no significant differences in the trace metal content of sediments among the different status categories of ICOLLs or among ICOLLs within each condition status category. Also, there was no correlation between these elements and the frequency of barrier openings. The trace metal concentrations in liver and gonad tissues of Mugil cephalus were also generally low, with Cd, Pb and Ag below detectable levels. In most cases there were significant interactions between trace metal levels in liver and gonad tissues; however, Se was the only trace metal to show a significant difference in concentration between these tissues. In a few cases trace metal concentrations were positively correlated with the total length and mass of the sea mullet. Also, there were no significant differences in trace metal levels between ICOLLs and condition status for gonad tissue, but there were significant differences for liver tissues.

7.4.2 Sources of trace metals The two major sources of trace metals are the natural environment and anthropogenic activities. Background levels of metals from the environment can be high, e.g. Al is one of the most common and abundant elements found in the natural geology of NSW coastlines (Jones et al. 2003). However, the catchments of ICOLLs in the study area have different levels of land use activities, which provide the main source of contaminants. Transport of trace metals into near- pristine ICOLLs occurs via the natural landscape, with some run-off occurring from surrounding roads and recreational activities. In more highly developed catchments contaminants generally enter ICOLLs via stormwater run-off (Zann 2000). Anthropogenic sources of the elements As, Cd, Cr, Cu, Pb, Se and Zn are described as they are the metals of interest and they are the main constituents derived from developed catchments surrounding ICOLLs.

Within the catchments of these ICOLLs in the study area, the major source of trace metals would be from urban dwellings and some minor industrial estates (see Chapter Two), along with associated infrastructure such as transportation, and impervious structures such as roads and pavements (Cardno Lawson Treloar 2010). Sources of Cd, Cu, Pb and Zn include building walls and automobile tyre emissions (Davis et al. 2001). Zinc is produced from galvanised iron waste and Cu is derived from brake linings (Payne et al. 1997; Davis et al. 2001). Lead and Cd are derived from waste from weed and pest sprays, domestic effluents and petroleum-based products (Payne et al. 1997; Edwards et al. 2001). Arsenic has a variety of sources including lumber and cement manufacturing, and also livestock and agricultural activities. Chromium is

267 Chapter 7: Trace metals in ICOLLs

also derived from wood treatment plants, paint pigments and waste effluents, with selenium being a product of fungicides and insecticides. Although not present in the vicinity of the Central Coast ICOLLs, steel works and coal-fired electric power generation stations produce particulate matter (ash) that can find its way into aquatic systems (Chenhall et al. 2001).

Since many ICOLLs support many commercial and recreational fishes, the input of trace metals is of concern as the feeding habits of species such as Mugil cephalus can increase the uptake and accumulation of trace metals to the various organs of the fish.

7.4.3 Trace metals in ICOLL sediments The sediments of ICOLLs in the study area had a variety of trace metals in them, with Al found to have the greatest levels in all of the studied ICOLLs. This would not be unexpected as aluminium is the third most common element on the planet and is found in high abundance in the NSW coastal geology (Jones et al. 2003). Most of the other elements had low levels, with the highest levels of all metals being found in Cockrone Lagoon, an extensively-modified ICOLL which also had the lowest amount of fine sediments. A study by Cheng (1992) measured the trace metal concentration in sediments of the Central Coast ICOLLs and found that Cockrone Lagoon had the highest concentrations of trace metals in its sediments compared to the other three ICOLLs. However, no reasons were given for these elevated levels. Possible reasons for the high levels of trace metals in Cockrone Lagoon during the current study could be related to the sampling site selection, which was located near the entrance, an area that generally has a greater sand content. However, fine particulate matter carrying trace metals could have been deposited at this site by wind currents, airborne deposition or stormwater outlets. Also the barrier is opened infrequently and the water depth is >2 m near the entrance, hence there would likely be limited movement of sediments via wind induced currents or by other means. Trace metals have an affinity for fine sediments and particulate matter (Roy and Crawford 1984), along with areas that have high organic content, such as sites with seagrass meadows (Batley 1987). In ICOLLs, organic rich fine sediments are generally located in the central basin or in the upper reaches where detritus is deposited from riverine inputs (Whitfield et al. 2012).

In the current study, sample sites were chosen based on the possible availability of sea mullet, which in most cases were collected from one site as determined from the intensive sampling for fishes described in Chapter 5. Hence, sediment samples may not have been sampled at ideally randomised locations or at sites that have fine sediments and high organic contents where trace metals tend to accumulate. The sampling site for Cockrone Lagoon was located at the entrance of the ICOLL near a stormwater outlet, and these outlets are known to be a major source of pollutant inputs (Gillis and Birch 2006; McKinley et al. 2011). Sample sites for the other

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ICOLLs were generally devoid of seagrasses, as sea mullet generally prefer shallow, muddy bare substrates (Whitfield et al. 2012).

The results suggest that the modified condition of the Central Coast ICOLLs did not influence the concentration of trace metals in their sediments, as the multivariate analyses showed no significant effect of ICOLL status on trace metal content of sediments. Therefore, the null hypothesis that there are no differences in trace metal content of sediments from these near- pristine and human impacted ICOLLs is accepted. The spatial variability of metals in ICOLLs is related to their metal speciation, which determines their behaviour and toxicity (Roy and Crawford 1984). The potential of trace metals to become remobilised can influence their individual mobility (Batley 1987) and their impact on their bioavailability to the biota (Gillis and Birch 2006). The geochemical aspects of sediments were not tested in the current study, however, the study by Roy and Crawford (1984) found that Zn levels tended to increase with a decrease in Pb, and that Zn was also more mobile than Pb, Cu and Cd. This could not be established here as Pb levels in the current study were below detectable levels, possibly due to its reduction as a major fuel additive for automobiles (Paul and Meyer 2001).

Trace metal concentrations were not influenced by the frequency of barrier openings, possibly due to the increases in salinity and the redistribution or flushing of sediments out of the ICOLLs. Trace metal concentration varies depending on the status of the barrier. For example, when barriers are closed for long period’s salinity lowers and the uptake and accumulation of metals by fish is greater compared to when barriers have opened and salinities are higher. Therefore, due to the low sample size of sediments collected during this study, not enough data was gathered to determine any spatial variation or geochemical effects on trace metals within these ICOLLs, therefore, further research needs to be undertaken in order to determine the true effects of barrier openings on trace metals in sediments.

7.4.4 Comparison of trace metals in ICOLL sediments There are few studies on trace metals in ICOLL sediments, except for those of Albani and Brown (1976) and Mikac et al. (2007). Albani and Brown (1976) examined concentrations of As, Cu, Pb and Ni in these same Gosford Lagoons. Their results were similar to those of the current study in that levels were fairly low, although the current study found that As, Pb and Ni were below detection levels. This suggests that concentrations have not increased over time, even though urban development has increased within these catchments. However, the results may not change if the sources of trace metals within the catchment are being suitably managed. The low levels of trace metals in sediments found by both Albani and Brown (1976) and in the current study may also be due to sedimentation rates that changed over time or to the possible

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effects of bioturbation (Roy and Crawford 1984). The study by Mikac et al. (2007) investigated the effects of natural forested and urban catchments on the invertebrate fauna in ICOLLs along the NSW coast south. The authors found no significant effect of catchment type on invertebrate structure, which they attributed to the developed catchments being less densely populated and industrialised. Similarly, the current study found no consistent effects of ICOLL status on trace metals.

In general, smaller sized ICOLLs have been neglected in relation to the possible effects of trace metals, with the majority of studies occurring in large lakes, such as Lake Illawarra (Payne et al. 1997; Gillis and Birch 2006) and Lake Macquarie, which have heavily industrialised and urbanised catchments (Roy and Crawford 1984; Batley 1987). Due to increased catchment development smaller ICOLLs need to be further investigated and comparisons also need to be made between impacted and natural ICOLLs.

7.4.5 Trace metals in liver and gonad tissues of Mugil cephalus In most cases the mean levels of trace metals in liver and gonads of sea mullet showed great variations and were generally lower than the Australian and New Zealand Food Authority Standards (ANZFA 1999). Levels of Cd, Pb and Ag were found to be below detectable levels. Aluminium, Ca, Cr, Cu, Mn and Zn were found in both sediments and fish tissues. The results show that there were some significant interactions of trace metal concentration between liver and gonad tissue; however, Se was the only metal that showed a significant difference without any significant interactions for trace metal concentrations between liver and gonad tissue. This is a common trend of studies that examined both liver and gonads in sea mullet (Sultana and Rao 1998; Kirby et al. 2001a; Yilmaz 2005). Also, there was no correlation found between the trace metal concentration in these ICOLL sediments and the liver and gonad tissues of Mugil cephalus.

Generally, the size (length and mass) of fish has been shown to influence concentrations of trace metals in tissues (Canali and Atili 2003; Damodharan and Reddy 2013). Univariate analyses showed that there were significant differences in the TL and mass of sea mullet among some ICOLLs, which was mainly due to the small sizes of Mugil cephalus collected from Cockrone Lagoon. The mean TL of sea mullet from Cockrone Lagoon was approximately half the TL of other ICOLLs, with their mean mass also much lower (Table 7.6). However, there were no significant differences in metal concentrations of As, Cr, Cu, Se and Zn in gonad and liver tissues between any of the ICOLLs and their condition status, with length and mass as covariates. Waltham et al. (2013) also found no significant relationships between trace metals and the length and mass of sea mullet when reviewing other coastal biomonitoring studies. In

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comparison, other studies have found that increasing size of fish resulted in a lowering in metal accumulation (Canli and Atli 2003; Damodharan and Reddy 2013).

In the current study, concentrations of Cu and Zn in sea mullet gonads were positively correlated with fish TL, and the concentration of Cr in the liver was also positively correlated with fish TL. Only Zn concentrations in sea mullet gonads were positively correlated with fish mass. The increase in concentration of Cu and Zn along with an increase in size of fishes could be due to these elements being essential for growth and development (Uysal et al. 2008). In the current study the size of fish collected was generally greater than 300 mm, which can affect metal accumulation, as younger individuals accumulate metals at a higher rate than older fishes due to their higher metabolic rate (Canli and Atli 2003; Damodharan and Reddy 2013). Individual metals were significantly different for As in gonad tissues between Cockrone and Wamberal Lagoons (extensively-modified) and for liver tissue between Termeil and Meroo Lakes (near-pristine). Pairwise tests were significant for Zn with gonad tissues between Cockrone and Wamberal Lagoons and for liver tissues between Avoca and Terrigal Lagoons and Cockrone and Wamberal Lagoons. The differences in metal concentrations between liver and gonad tissue can be related to the amounts of metallothioneins, metal binding proteins found in the liver (Canli and Atli 2003; Alquezar et al. 2006). The liver has also been shown to eliminate metals (Alquezar et al. 2006; Roach et al. 2008). Statistical analysis showed that there were many significant interactions in trace metal contents of fish tissues from near-pristine and impacted ICOLLs, therefore it is difficult to generalise about the outcomes of these interactions.

A comparison of the results in this study for trace metal levels in liver and gonad tissues of sea mullet with other studies shows that metal concentrations were much lower in the Central Coast and near-South Coast ICOLLs compared with values reported from studies of other sea mullet from ICOLLs found along the coast of south-eastern NSW (Kirby et al. 2001a, 2001b) and in Turkey (Yilmaz 2005). Although not studied in the present study, the sex and age of fish can result in greater accumulation of certain metals (Edwards et al. 2001; Kirby et al. 2001a; Fabris et al. 2006). Environmental factors also have an effect on the uptake and bioavailability of metals in fishes (Alquezar et al. 2006; Padmini and Geetha 2007). The ICOLLs studied had similar environmental factors, including pH and temperature, however, salinity varied between them mainly due to barrier openings. Salinity reduces the uptake and accumulation of metals by fish, as the rate of accumulation is inversely proportional to the salinity (Somero et al. 1977; Jezierska and Witeska 2006). For example, when barriers are closed for long periods, salinity lowers and the uptake and accumulation of metals by fish is greater, compared to when barriers have opened and salinities are higher.

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7.4.6 Implication and limitations of the study Although the results indicate that there were no significant differences in trace metal concentrations of sediments and fish tissues from between near-pristine and impacted ICOLLs of the near-South Coast and Central Coast, it does show the need for comparative studies between the two different environments. Due to increased desires for human development in coastal areas, there is a strong need for catchment managers and scientists to further explore pristine areas in order to have a full understanding of their environmental processes and potential future threats to them, especially from pollutants. Pristine ICOLLs can provide information on the natural physical, environmental and biological processes, which can then be compared to more impacted sites. Pollutants, and especially trace metals, are of particular concern as they can alter biological communities, and since many ICOLLs are not flushed for extremely long periods of time, trace metals can persist in these environments for decades (Davis et al. 2001; Beltrame et al. 2009). Further studies need to be undertaken to understand the temporal and spatial variations of trace metals not only in pristine environments but within impacted sites.

This study attempted to examine spatial variations of trace metals in ICOLLs; however, the results may only be relevant to these Central and near-South Coast ICOLLs, though these results can be used as guidelines for further studies in other similar sized NSW ICOLLs. Mugil cephalus is a common species in NSW ICOLLs, therefore trace metal levels in sediments and fish tissue can be readily compared. ICOLLs have varying degrees of catchment development, and with low numbers of pristine ICOLLs remaining it would be appropriate for further research to be undertaken to ascertain if the results from these Central Coast ICOLLs would be similar to the other numerous ICOLLs located along the NSW coast.

7.5 Conclusion The current study showed that concentrations of trace metals varied in sediments but were not significantly affected by the condition status of the study ICOLLs. Therefore, the null hypothesis that there are no significant differences in trace metal contents of sediments between these near-pristine and impacted ICOLLs must be accepted. Also, trace metals were not influenced by barrier openings, so the null hypothesis that the frequency of barrier openings has no influence on trace metal levels in sediments of these ICOLLs can be accepted. Metal concentrations also varied between liver and gonad tissues of Mugil cephalus, but levels were generally greater in the liver, with the exception of zinc and strontium, which were greater in the gonad tissues. Copper and Zn were positively correlated for gonad tissue and fish TL, with Zn also being correlated with gonad tissue and fish mass. Chromium was correlated with the TL of the fishes in their livers. Trace metal levels were significantly different for As and Zn between

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near-pristine and impacted ICOLLs, however a number of significant interactions occurred and therefore it is difficult to generalise about these results.

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Chapter 8: General discussion and conclusions

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Chapter 8: General discussion and conclusions

8.1 General Discussion Intermittently Closed and Open Lakes and Lagoons (ICOLLs) is an acronym used to describe intermittently closed estuaries, coastal lakes or lagoons. Approximately 135 estuarine water bodies have been identified along the NSW coast of which 45% are classified as ICOLLs (Williams et al. 1998; Griffiths and West 1999). In most cases these ICOLLs have relatively small catchments with water areas of generally <10 km2; however, they are known to be functional habitats which are important for many larval, juvenile and adult fishes (Pollard 1994b; Griffiths 1998, 1999; Griffiths and West 1999; Jones and West 2005). The generally small size of ICOLLs and their locations have placed much stress on these environments. Many ICOLLs in NSW are located near areas which have highly modified catchments due to industrialised and urban development, and also tourism and agricultural activities. The formation of a barrier across the entrances of ICOLLs increases the pressures placed on these environments from human activities, and these barriers are often artificially opened to prevent flooding of surrounding developed foreshores. Also, many contaminants washed into the waterways from run-off and stormwater outlets are retained in these water bodies. Therefore, in order to implement appropriate management practices, ecological processes such as barrier openings, flora and fauna assemblages and contaminants of NSW ICOLLs need to be investigated.

The main aim of this study was therefore to understand the factors that influence the fish assemblages of the ICOLLs of the Central Coast, NSW, Australia. In order to understand these factors, both environmental and physical aspects of each ICOLL were studied. Environmental parameters, habitat variability, food resources, recruitment processes and trace metal concentrations were examined. In other previous studies, generally one or two important factors influencing fish assemblages have been determined, such as salinity (Young et al. 1997; Griffiths 2001a), habitat variability (Gill and Potter 1993; Cowley and Whitfield 2001; Griffiths 2001c; Jones and West 2005), barrier openings, and recruitment processes (Bell et al. 2001; Griffiths 2001c; Strydom 2003).

The current study is unique in that combinations of factors were assessed for their relative contribution to spatial and temporal variations of fish assemblages. This study is also unique in that the four main ICOLLs investigated are located geographically close to each other, along a 10 km stretch of coastline. Their similarities in physical characteristics, catchment size and water area and the close proximity of these ICOLLs to each other would suggest that they might have similar environmental characteristics, and that these characteristics may be a driving force in influencing their fish assemblages. However, due to varying levels of land use activities, ecological variations can arise. To further investigate the impacts that catchments may have on

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fish assemblages, the effects of trace metals in near-pristine ICOLLs were compared to those in the modified ICOLLs.

In order to determine what factors influence fish assemblages, aspects of the ecology of each ICOLL needed to be investigated by examining the spatial and temporal variability of invertebrate assemblages and what environmental factors may influence their variability (Chapter 3). And also, by examining what fishes utilise these ICOLLs by studying the movement of larval and juvenile fishes between ICOLLs and their adjacent surf zones (Chapter 4). The main part of the study was to identify the fishes present in Central Coast ICOLLs and to establish what environmental factors, if any, are responsible for any changes in adult fish assemblages (Chapter 5). Dietary preferences are an important aspect of fish ecology, and food resources can be limited depending on the status of the barrier. Therefore the gut contents of Central Coast ICOLL fishes were examined to establish their diets and to determine if barrier openings have any effect on their food resources (Chapter 6). Trace metal concentrations found in the biota and sediments of ICOLLs is generally associated with catchment development and can influence fish assemblages. Samples of Central Coast and near South Coast ICOLL sediments along with liver and gonad tissue samples from sea mullet were examined to determine concentrations within each sample and to see if barrier openings affected levels of trace metals in samples taken from near-pristine, modified and extensively-modified ICOLLs (Chapter 7).

8.2 Barrier openings Approximately 45% of NSW estuaries have an intermittent barrier across their entrance that can isolate them from the sea for short periods of a few days to longer periods of months to years. It is generally considered that the status of the barrier (closed/open) is a driving force influencing the overall ecology of ICOLLs (Vorwerk et al. 2003). Barrier dynamics are usually influenced by climatic and oceanic conditions, however due to catchments being highly developed; barriers are now artificially opened at a frequency determined by the water level or berm height. However, the decline of natural openings and an increase in artificial barrier openings has effects on the ecology of ICOLLs. The effects of barrier openings are immediately noticeable, with water levels decreasing dramatically, exposing large areas of substrate and aquatic vegetation, and resulting in poor aesthetic values and in some cases fish kills (Wilson et al. 2002). Fish kills can also occur in closed ICOLLs, as the water can become stagnant due to low dissolved oxygen levels. In the current study, Terrigal Lagoon was opened approximately 10 times more often than Cockrone, Avoca and Wamberal lagoons. Other studies have shown that barrier openings influence salinity and turbidity (Pollard 1994a; Schallenberg 2010), and habitat structure and water quality (Wilson et al. 2002). Dye and Barros (2005a) and Mikac et al.

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(2007) have suggested that the disturbance from barrier openings can decrease species richness and abundance of invertebrate faunal assemblages as well as increasing their spatial variability. Possible recruitment linkages for larval and juvenile fishes between ICOLLs and their adjacent surf zones have been found to be highly irregular and generally occur when barriers are opened or by overwash events when barriers are closed (Bell et al. 2001; Griffiths 2001c; Strydom 2003). Although the timing of barrier openings can influence the recruitment of larval and juvenile fishes (Griffiths and West 1999; Vorwerk et al. 2003), fish assemblages can also change when barrier openings occur due to marine species entering ICOLLs (Bennet 1989; Vorwerk et al. 2003; Jones and West 2005) and fishes leaving them. In the current study, there was no consistent evidence for any significant effects of barrier openings on the invertebrate faunal assemblages, recruitment of larval and juvenile fishes, ICOLL fish assemblages, feeding preferences of ICOLL fishes, or trace metal concentrations. However, barrier openings did alter environmental parameters such as salinity, turbidity and habitat structure, which can inadvertly effect invertebrate and fish assemblages.

8.3 Recruitment of larval and juvenile fishes into ICOLLs Recruitment of larval and juvenile fishes into estuarine environments after coastal spawning is facilitated by nearshore currents, tidal influences, and the species’ swimming abilities. However, this process is disrupted in the case of ICOLLs by the formation of an intermittent barrier. The timing and frequency of artificial openings can impact on recruitment, as these openings may not occur at peak spawning periods. Also, differences in larval and juvenile fish assemblages between ICOLLs and adjacent surf zones relate to the availability of species that move between the two environments. Surf zone fishes have to contend with different environmental factors compared to fishes in ICOLLs. For example, wave energy gradients in surf zones associated with each ICOLL can result in patchy distribution of larval and juvenile fishes (Romer 1990; Clark 1997). Although, this study shows no evidence to suggest that larval and juvenile species enter ICOLLs from adjacent surf zones into Central Coast ICOLLs, many marine-spawning species were collected throughout the study, such as Mugil cephalus, suggesting recruitment from the adjacent surf zones is a high possibility. However, the small numbers and diversity of marine spawning species collected during this study could be related to the barrier dynamics of each individual ICOLL. Cockrone Lagoon was the only ICOLL to show a distinct change in larval and juvenile fish assemblages as a result of recruitment from adjacent surf zones, with numerous juvenile Acanthopagrus australis being collected after the only barrier opening. However, it could not be determined if this species is well established within this ICOLL or as a marine spawner was recruited from the adjacent surf zones. Therefore in most cases, Central Coast ICOLLs are self-recruiting environments for some resident species of fishes which are not influenced by barrier openings.

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8.4 The effects of environmental factors on the invertebrate and fish assemblages of ICOLLs

8.4.1 Invertebrate assemblages Central Coast ICOLLs with seagrasses and algal habitats possessed a similar invertebrate fauna (Robinson et al. 1982; Hutchings 1999). This invertebrate fauna consisted predominantly of polychaetes, crustaceans, gastropods and bivalves. In contrast, the invertebrate fauna of Terrigal Lagoon was mainly comprised of nereid polychaetes, which is attributed to the lack of vegetation there.

Although the Central Coast ICOLLs studied are in close proximity to each other, the factors influencing their invertebrate assemblages differed slightly between these ICOLLs. Salinity was a major factor in all ICOLLs except at Wamberal Lagoon. This is not unusual as many other studies have shown that salinity is a major factor determining the composition of the invertebrate fauna (Atkinson et al. 1981; Robinson et al. 1983; Hutchings 1999; Hyndes et al. 2003). Other factors included distance from the barrier, turbidity, and particular sediment grain sizes, especially at Wamberal Lagoon. Barrier status was a factor only at Terrigal Lagoon, which could indirectly influence salinity due to the greater number of openings there. The effect that barrier openings may have on invertebrate assemblages varies with Lill et al. (2012) suggesting that many invertebrate species are recruited from the ocean during such barrier openings, and Dye and Barros (2005a) and Mikac et al. (2007) found that spatial variability of invertebrate fauna was greater during openings. In contrast, Gladstone et al. (2006) found barrier openings had no effect on invertebrate assemblages.

8.4.2 Fish assemblages Seine and multi-panel gill nets were used to sample fish assemblages of ICOLLs, with the fish assemblages detected being similar to those found in other studies in that they have large abundances of particular species but relatively low species richness. This has been attributed to the small size of the study ICOLLs. The numerically abundant species were generally smaller- bodied fish (<100 mm TL), including Atherinosoma microstoma (Avoca and Wamberal lagoons) and Ambassis jacksoniensis (Terrigal Lagoon). In contrast, Cockrone Lagoon was dominated by juvenile Acanthopagrus australis, a recreationally and commercially important fish species that was also found in high abundances at Avoca Lagoon. This suggests that these ICOLLs can be important nursery areas for this species. Larger sized fishes were dominated by mugilids, mainly Mugil cephalus.

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Comparable to factors influencing the invertebrate fauna, the environmental factors influencing fish assemblages of ICOLLs also differed in their effects. Salinity and water temperature were the main factors influencing fish assemblages. Previous studies have found these factors to be important in spatial and temporal variations in fish assemblages (Bennett 1989; Pollard 1994a; Young et al. 1997; Griffiths 2001a). Wamberal Lagoon was the only site where the status of the barrier showed some effect. Percentage area of bare substrate was important at Terrigal Lagoon, which is understandable as there are no seagrasses or algae present there, compared to Cockrone and Wamberal Lagoons where the percentage algal cover and algal mass were also influential factors. These habitats have been shown to provide suitable nursery habitats and food resources for larval and juvenile fishes (Gill and Potter 1993; Cowley and Whitfield 2001). Also, the effect various land use activities have on fish assemblages of ICOLLs has not been previously documented in the literature.

8.5 Diets of fish in ICOLLs ICOLLs are highly productive ecosystems providing nutrients and food resources for both invertebrates and fishes. This is significant as invertebrates are an important food source for many species of fishes. Polychaetes, crustaceans and molluscs are typical of fish food resources found in ICOLLs (Hutchings 1999), and the availability of these resources can depend upon the environmental conditions in these ICOLLs. Also, since ICOLLs can be isolated from the sea for long periods of time and have relatively high abundances of similar fish species, it is expected that competition for food would be intense. The diets of each species examined included similar invertebrate taxa; however, the amount of different food types consumed differed between species and was influenced by the range of habitats present in the ICOLL. The gut contents of the most numerically abundant fish species were therefore examined. The more abundant fishes from Cockrone and Wamberal Lagoons, Acanthopagrus australis and Atherinosoma microstoma, respectively, had different diets before and after the lagoon barriers had opened. In contrast, the diets of A. microstoma and Ambassis jacksoniensis (the most abundant species in Avoca and Terrigal Lagoons, respectively), did not change with changes in the barrier status. In the current study it was shown that different factors influence invertebrate assemblages of Central Coast ICOLLs, and the composition of invertebrate food items showed considerable temporal and spatial variations. Most species of fishes in ICOLLs are predominately opportunistic feeders due to the limited range of resources present and competition for these resources.

8.6 Trace metals in sediments and fishes in ICOLLs The geology of a region influences the background levels of trace metals present; however, these metals can become toxic when they have been extracted and processed in industrial

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centres for various uses, and the waste products are returned to the environment. ICOLLs can receive the full impact of trace metals associated with urbanisation, stormwater inputs and atmospheric deposition, where they settle initially in the basin. Here they are distributed throughout the water body via wind, water movements and organisms that live and feed on and in the substrate. In this study, the near-pristine near-south coast ICOLLs were distinguished by their surrounding catchments being dominated by national parks that have limited human activities, compared to the modified and extensively-modified ICOLLs of the Central Coast. Also, barrier openings of these near-pristine ICOLLs were generally infrequent, with the barrier not being breached for many years. Trace metal levels in sediments and in the tissues of Mugil cephalus from all of these ICOLLs were generally low, with some metals below detectable levels. There were no significant differences found in the levels of trace metals in Mugil cephalus tissues and sediments from near-pristine or modified and extensively-modified ICOLLs.

8.7 Implications of this study This study was undertaken in order to better understand these small coastal lagoon ecological systems that are threatened by human influences. These influences can directly or indirectly affect the ecology of ICOLLs. Increased artificial barrier openings by local councils may appear to be beneficial to these small systems, however they could inadvertently be aiding in the degradation of the overall richness of the system. Barrier openings have resulted in fish kills and habitat destruction which can impact on the flora and fauna within these ICOLLs. Despite this, there was no consistent evidence for a significant effect of barrier openings on the invertebrate assemblages, fish assemblages, feeding preferences of fishes and trace metal concentrations in fishes. Also, the fish assemblages were influenced by different environmental factors, making each ICOLL unique and possibly requiring different management practices. Many ICOLLs have different factors influencing their ecology, therefore it is not easy to relate the outcomes for one ICOLL to another (Turner et al. 2004). Fish assemblages in this study were directly influenced by environmental factors such as salinity, water temperature and sediment composition, all of which can be influenced by the status of the barrier. In most cases barrier status can be managed, however management of the effects of development can prove to be complex and costly. An ideal start to appropriate management would be to continue with ongoing monitoring programs to assess any strategies that need to be put into place.

8.8 Opportunities for Further Research This study has shown that the ecological factors that influence the ecology of Central Coast ICOLLs vary and may change over time. Taking this into consideration there is an opportunity for further research to be undertaken not only on Central Coast ICOLLs, but other ICOLLs that

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are scattered along the NSW coastline. For example, the current study has shown that fish assemblages of the Central Coast ICOLLs consist mainly of resident species that spend their whole lifecycle within these ICOLLs. However, little information is known about their reproductive biology or the genetic variation that may occur between species within and between Central Coast ICOLLs. Also, it is not known what happens to fishes when barriers are opened. It is assumed that many species exit the ICOLLs to the ocean, or they may remain in the ICOLL and its ephemeral streams, or die. Monitoring fish movements in and out of ICOLLs by electronic tagging would be beneficial, especially for economic and recreationally important species that are known to utilise ICOLLs as nursery areas. Information can be collected on whether some of these species utilise the same ICOLLs annually or whether they move along the coastline to different ICOLLs. Movement of smaller species between the sea and the ICOLLs can be determined by sampling in the entrance channel once barriers have been opened. Extreme water exchange occurs when barriers are opened and therefore many larval and juvenile fishes may be washed out with the outflow. Overwash events are another possible way for larval and juvenile fishes to enter ICOLLs, however this was not investigated.

One factor not considered during this study, but which may have an impact on these ICOLLs in the near future, is climate change. Predicted effects include a rise in both water temperatures and sea levels, changes in seagrass communities, increased catchment run-off, and changing barrier dynamics. All of these factors have the potential to affect the invertebrate and fish faunas of these shallow water environments, however this study has provided a background to the influences that may affect the biota, and this may aid in the future management of ICOLLs. However, continued studies are required to monitor the impacts of not only climate change but further catchment development in relation to NSW ICOLLs.

8.9 General conclusions The main conclusions from this study were;  Barrier openings did not have a direct influence on invertebrate faunal and fish assemblages of Central Coast ICOLLs, however, marine spawning species such as Acanthopagrus australis and Mugil cephalus were found throughout this study suggesting that this may not be the case.  Invertebrate assemblages reflect the habitat types found within each ICOLL, with aquatic vegetation providing a greater species richness and abundance than bare substrates.  Salinity along with percentage sediment grain size were the main variables affecting invertebrate assemblages.

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 Abundances of larval and juvenile fishes of these ICOLLs were greater than their adjacent surf zones, with these ICOLLs dominated by small species of fishes, Atherinosoma microstoma, Ambassis jacksoniensis and Philypnodon grandiceps. Hyperlophus vittatus was the dominated species found in the adjacent surf zones.  These ICOLLs are considered to be generally self-recruiting habitats, not for all fish species, but for many of their resident species of fish.  Fish assemblages were characterized by high abundances of particular species of fishes, with small fishes (<100 mm TL) being numerically most abundant, including Atherinosoma microstoma (Avoca and Wamberal Lagoons) and Ambassis jacksoniensis (Terrigal Lagoon). Mugilids, Mugil cephalus and Myxus elongatus, were the numerically abundant larger fishes found at ICOLLs.  Central Coast ICOLLs are also important nursery areas as shown by the large abundances of juvenile Acanthopagrus australis collected throughout the study.  Salinity and water temperature were the main factors influencing fish assemblages in these ICOLLs.  Trace metals in sediments were relatively low, with ICOLLs showing no indication of being significantly polluted by trace metals, and many metals below detectable levels. There were no significant differences in trace metal levels in near-pristine and impacted ICOLLs, and barrier openings did not affect the concentrations of metals in these ICOLLS.  Trace metal concentrations in liver and gonad tissues of Mugil cephalus differed for some metals, but they were only present in relatively low concentrations, with many metals being below detectable levels. There were no differences in trace metal levels of tissues in fish from near-pristine and impacted ICOLLs.

282 References cited

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