direct and indirect ecological interactions between aquaculture activities and marine fish ...

405 Pages·2017·22.62 MB·English

DIRECT AND INDIRECT ECOLOGICAL
INTERACTIONS BETWEEN AQUACULTURE
ACTIVITIES AND MARINE FISH COMMUNITIES IN
SCOTLAND

BY
JOLY KARIM GHANAWI

A THESIS SUBMITTED FOR THE DEGREE OF DOCTOR
OF PHILOSOPHY

INSTITUTE OF AQUACULTURE,
UNIVERSITY OF STIRLING, STIRLING, SCOTLAND
MARCH 2018
DECLARATION

This thesis has been composed in its entirety by the candidate. Except where specifically
acknowledged, the work described in this thesis has been conducted independently and
has not been submitted for any other degree.

CANDIDATE NAME: …………………………………………

SIGNATURE: …………………………………………

DATE: …………………………………………

SUPERVISOR NAME: …………………………………………

SIGNATURE: …………………………………………

DATE: …………………………………………
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ACKNOWLEDGMENTS
First and foremost, I want to expresss deep gratitude to my supervisor Dr. Bruce
McAdam. It has been an honor to be your student and given the opportunity to work on
this project. I greatly appreciate all your contributions towards the completion of this
thesis, all the time, all the feedback, ideas and all the funding that was needed for this
PhD project. I am thankful for all your support in mentoring me to become an independent
researcher. I want to also thank my second supervisor Prof. Trevor Telfer for his
contributions, particularly in some aspects of the fieldwork and taxonomic expertise,
throughout this PhD project.
I am very grateful for the funding sources for this PhD scholarship: Marine Alliance
for Science and Technology for Scotland (MASTS) and the University of Stirling. I am
also grateful to MASTS for the additional funding provided for some of the laboratory
work. I would also like to thank the Fisheries Society of the British Isles (FSBI) for the
small grant provided for this PhD project. I would like to thank the Institute of
Aquaculture for providing all the equipment and resources needed to complete this
project.
I would like to thank the Aquaculture Systems Group for all the technical support.
I thank the Nutrition Group for all the technical assistance provided when it was needed.
I thank Mr. James Dick and Dr. Matthew Sprague for all the help with the lipid and fatty
acid analysis. I would like to thank the Breeding and Genetic Improvement Group. I thank
Prof. Herve Migaud and Dr. Eric Leclercq for letting me use the fish farming site and all
the help that was provided during fieldwork.
I am grateful to MASTS for the networking opportunities through which some of
the fish needed for this project were provided; I thank Dr. Clive Fox (The Scottish
Association for Marine Science (SAMS)) and Neil Burns (Marine Scotland). I would like
to thank Kames Fish Farming Ltd. for letting me use their sites and to the staff members
who kindly assisted during some of the fieldwork. I also thank Marine Harvest Scotland
Ltd. for allowing access to their site.
I would like to thank the examining committee, Dr. Pablo Sanchez-Jerez and Dr.
Mike Leaver and the chair of the thesis, Prof. Rachel Norman, for their interest and time
in reviewing the thesis.
All photos in the thesis were taken by Dr. Bruce McAdam, Joly Ghanawi and
Silvère Santos.
I would also like to express my gratitude to Prof. Imad Saoud (American University
of Beirut (AUB)) for his inspirations to become a researcher.
Lastly, I am grateful to my family for all their support and guidance. I thank my
friends for their support and encouragement. And I am grateful to Silvère for all the love,
kindness, support, encouragement, patience and all the laughs. Thank you for your
faithful support throughout this PhD journey and when things got quite difficult.
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Joly Ghanawi

ABSTRACT

Presence of coastal aquaculture activities in marine landscapes is growing.
However, there is insufficient knowledge on the subsequent ecological interactions
between these activities and marine fish communities. The overall aim of this thesis was
to evaluate the direct and indirect ecological effects of aquaculture activities on marine
fish communities in Scotland. A combination of empirical and modelling approaches was
employed to collect evidence of how aquaculture activities affect marine fish
communities at the individual, population and ecosystem levels around coastal sea cages.
The two fish farms evaluated in this research provided the wild fish sampled near
the sea cages with a habitat rich in food resources which is reflected in an overall better
biological condition. Results of the stomach content analysis indicated that mackerel
(Scomber scombrus), whiting (Merlangius merlangus) and saithe (Pollachius virens)
sampled near sea cages consumed wasted feed which was also reflected in their modified
FA profiles. The overall effects of the two fish farms were more pronounced in young
whiting and saithe than in mixed aged mackerel sampled near the sea cages.
The phase space modelling approach indicated that the overall potential for fish
farms to act at the extremes as either population sources (a habitat that is rich in resources
and leads to an overall improved fitness) or ecological traps (a habitat that appears to be
rich in resources but is not and leads to an overall poor fitness) are higher for juvenile
whiting than for mackerel. Based on the empirical evidence and literature the two fish
farms are more likely to be a population source for wild fishes.
Using an ecosystem modelling approach indicated that fish farming impacts the
food web in a sea loch via nutrient loading. Mussel farming relies on the natural food
resources and has the potential to affect the food web in a sea loch via competing with
zooplankton for resources which can affect higher trophic levels. The presence of both
activities can balance the overall impact in a sea loch as compared to the impact induced
if each of these activities were present on their own. Both activities have the potential do
induce direct and indirect effects on the wild fish and the entire sea loch system.
The results of this PhD identified several gaps in data and thus could be used to
improve future sampling designs. It is important to evaluate the cumulative effect of the
presence of aquaculture activities in terms of nutrient loading and physical structure in
the environment. Using a combination of empirical and modelling approaches is
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recommended to gain further insight into the ecological impacts of aquaculture activities
on wild fish communities.
Results of this PhD study could lead to more informed decisions in managing the
coastal aquaculture activities. Establishing coastal fish farms as aquatic sanctuaries can
be of an advantage to increase fish production and conserve species that are endangered
provided that no commercial and recreational fishing is allowed nearby. It would be
useful to have long term monitoring of the fish stocks around the cages and if there is any
production at the regional level. Additionally, information on behaviour, migration
patterns should be collected to understand the impacts of aquaculture activities on fish
stocks. From an aquaculture perspective, ecologically engineered fish farms in addition
to careful site selection in new aquaculture developments may improve nutrient loading
into the ecosystem.
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TABLE OF CONTENTS
LIST OF FIGURES ..................................................................................................... XI
LIST OF TABLES ...................................................................................................... XV
CHAPTER 1 COASTAL AQUACULTURE ACTIVITIES AND MARINE FISH
COMMUNITIES ............................................................................................................ 1
1.1 Introduction ............................................................................................................ 1
1.2 Coastal aquaculture activities and wild fish communities ..................................... 2
1.2.1 Evidence for wild fish attraction to aquaculture structures ........................ 3
1.3 Why are fish attracted to coastal sea cages? .......................................................... 4
1.3.1 Food availability: natural and artificial ...................................................... 4
1.3.2 Other factors attracting fish ......................................................................... 7
1.4 Positive and negative fish farming impacts on wild fish ....................................... 8
1.5 Attraction, ecological trap or production sites? ..................................................... 9
1.6 Marine fish farming and impacts on commercially targeted species ................... 12
1.6.1 Impacts on local commercial and recreational fisheries ........................... 12
1.6.1.1 Effects on flesh quality of wild fish for human consumption ..... 14
1.6.1.2 Chemicals and wild fish ............................................................. 14
1.7 Fish farming industry and wild fish aggregations: benefits and costs ................. 15
1.7.1 Wild fish can mitigate unwanted fish farming effects ................................ 15
1.7.2 Coastal fish farms attract predators .......................................................... 16
1.7.3 Pathogen transmission and wild fish ......................................................... 16
1.8 Capture fisheries and coastal aquaculture in Scotland ......................................... 17
1.8.1 Capture fisheries ........................................................................................ 18
1.8.2 Aquaculture ................................................................................................ 18
1.9 Fish species studied in this thesis ......................................................................... 20
1.10 Objectives and structure of the PhD research .................................................... 23
CHAPTER 2 EMPIRICAL AND MODELLING APPROACHES TO
EVALUATE AQUACULTURE EFFECTS ON WILD FISH POPULATIONS.... 25
2.1 Empirical (fieldwork and laboratory) approaches ................................................ 25
2.1.1 Fieldwork methodologies ........................................................................... 26
2.1.1.1 Overview of ecological experimentation.................................... 26
2.1.2 Use of stomach content analysis ................................................................ 28
2.1.2.1 Occurrence of waste feed in wild fish ........................................ 29
2.1.3 Biological condition ................................................................................... 29
2.1.4 Lipids and fatty acids in wild fish .............................................................. 31
2.1.3.1 Overview of fatty acids in fish .................................................... 31
2.1.3.2 Use of fatty acid as biomarkers ................................................. 35
2.1.3.3 Use of fatty acids biomarkers and wild fish aggregations ......... 35
2.2 Modelling approaches .......................................................................................... 37
2.2.1 Role of modelling ....................................................................................... 38
2.2.1.1 Statistical modelling ................................................................... 38
2.2.1.2 Single species population models .............................................. 41
2.2.1.3 Ecosystem based models ............................................................ 42
2.3 Conclusions .......................................................................................................... 43
CHAPTER 3 FIELD AND LABORATORY STUDY METHODS ......................... 44
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3.1 Overview .............................................................................................................. 44
3.2 Farm sites and farm characteristics ...................................................................... 45
3.2.1 Loch Melfort ............................................................................................... 45
3.2.2 Loch Leven ................................................................................................. 48
3.2.3 Comparison of selected lochs and farms ................................................... 50
3.3 Underwater video recordings ............................................................................... 53
3.4 Macrobenthic sampling ........................................................................................ 55
3.4.1 Macrobenthic sampling.............................................................................. 55
3.5 Environmental data collection.............................................................................. 58
3.6 Fish sampling and processing .............................................................................. 58
3.6.1 Fish sampling ............................................................................................. 58
3.6.2 Sampling design ......................................................................................... 60
3.6.3 Fish processing .......................................................................................... 62
3.6.3.1 Stomach content analysis ........................................................... 62
3.6.3.2 Condition indices ....................................................................... 62
3.6.3.3 Lipid extraction and fatty acid methyl esters (FAMEs) ............. 63
3.6.3.4 Total lipid extraction .................................................................. 63
3.6.3.5 Fatty acid methyl esters (FAME) preparation ........................... 64
PART I: EMPIRICAL STUDIES ............................................................................... 66
CHAPTER 4 FATTY ACID BIOMARKERS INDICATE EFFECTS OF A
HALIBUT FARM IN MACKEREL AND SAITHE ................................................. 67
4.1 Introduction .......................................................................................................... 67
4.2 Methods ................................................................................................................ 68
4.2.1 Statistical analysis...................................................................................... 70
4.2.1.1 Stomach content description ...................................................... 70
4.2.1.2 Testing for differences in condition, lipids and total fatty acids
between sites 70
4.2.1.3 Multivariate analysis of FAs ...................................................... 71
4.3 Results .................................................................................................................. 72
4.3.1 Observations (anecdotal accounts) ............................................................ 72
4.3.2 Scatter plots................................................................................................ 74
4.3.2.1 Mackerel .................................................................................... 74
4.3.2.2 Saithe .......................................................................................... 74
4.3.3 Stomach contents........................................................................................ 80
4.3.3.1 Mackerel .................................................................................... 80
4.3.3.2 Saithe .......................................................................................... 80
4.3.4 Testing for differences in length, mass and condition ............................... 82
4.3.4.1 Mackerel .................................................................................... 82
4.3.4.2 Saithe .......................................................................................... 83
4.3.5 Total lipids and fatty acid profiles ............................................................. 86
4.3.5.1 Commercial diet composition .................................................... 86
4.3.5.2 Mackerel .................................................................................... 86
4.3.5.3 Saithe .......................................................................................... 88
4.4 Discussion .......................................................................................................... 104
4.4.1 Impacts of the halibut farm on mackerel ................................................. 104
4.4.2 Impacts of the halibut farm on saithe....................................................... 108
4.4.3 Comparison between mackerel and saithe ............................................... 110
4.4.4 Using fatty acids as biomarkers ............................................................... 111
4.4.5 Limitations of the study ............................................................................ 112
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4.5 Conclusions ........................................................................................................ 114
CHAPTER 5 USING FATTY ACID BIOMARKERS TO CONTRAST AND
DISTINGUISH PHYSIOLOGICAL EFFECTS ON MACKEREL AND
WHITING CAUGHT NEAR TWO FISH FARMS ................................................ 115
5.1 Introduction ........................................................................................................ 115
5.2 Methods .............................................................................................................. 115
5.2.1 Statistical analysis.................................................................................... 118
5.3 Results ................................................................................................................ 119
5.3.1 Observations (anecdotal accounts) .......................................................... 119
5.3.2 Data patterns............................................................................................ 120
5.3.2.1 Mackerel .................................................................................. 120
5.3.2.2 Whiting ..................................................................................... 120
5.3.3 Stomach contents...................................................................................... 126
5.3.3.1 Mackerel .................................................................................. 126
5.3.3.2 Whiting ..................................................................................... 126
5.3.4 Length, mass and condition ..................................................................... 128
5.3.4.1 Mackerel .................................................................................. 128
5.3.4.2 Whiting ..................................................................................... 128
5.3.5 Total lipids and fatty acid composition .................................................... 133
5.3.5.1 Commercial diets ..................................................................... 133
5.3.5.2 Mackerel .................................................................................. 133
5.3.5.3 Whiting ..................................................................................... 134
5.3.6 Linear discriminant analysis .................................................................... 143
5.3.6.1 Mackerel .................................................................................. 143
5.3.6.2 Whiting ..................................................................................... 143
5.4 Discussion .......................................................................................................... 147
5.4.1 Impacts of two fish farms (halibut and salmon) on mackerel .................. 147
5.4.2 Impacts of two fish farms (halibut and salmon) on whiting ..................... 150
5.4.3 Comparison between the halibut and salmon farm ................................. 154
5.4.4 Study limitations ....................................................................................... 156
5.5 Conclusions ........................................................................................................ 158
CHAPTER 6 EVALUATING THE POTENTIAL OF TWO COASTAL FISH
FARMS TO ACT AS ECOLOGICAL TRAPS OR PRODUCTIVITY SITES.... 159
6.1 Introduction ........................................................................................................ 159
6.2 Methods .............................................................................................................. 160
6.2.1 Data analysis............................................................................................ 160
6.3 Results ................................................................................................................ 162
6.3.1 Sizes and condition of fish near and away from cages ............................ 162
6.3.2 Length and mass relationships ................................................................. 173
6.3.3 Diets of fish near and away from cages ................................................... 179
6.4 Discussion .......................................................................................................... 181
6.5 Conclusions ........................................................................................................ 184
PART II: MODELLING STUDIES .......................................................................... 185
CHAPTER 7 A PHASE SPACE MODEL FOR EVALUATING THE POSITIVE
AND NEGATIVE EFFECTS OF FISH FARMING ON WILD FISH .................. 186
7.1 Introduction ........................................................................................................ 186
7.2 Methods .............................................................................................................. 187
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7.2.1 Basic phase space model .......................................................................... 187
7.2.2 Leslie population models ......................................................................... 190
7.2.2.1 Population growth rates and stable age structure ................... 191
7.2.3 Parameterization of basic matrices ......................................................... 192
7.2.3.1 Mackerel .................................................................................. 192
7.2.3.2 Whiting ..................................................................................... 194
7.2.4 Scenarios for both mackerel and whiting found near sea cages .............. 195
7.2.4.1 Mackerel .................................................................................. 195
7.2.4.2 Whiting ..................................................................................... 196
7.2.5 Matrix elasticities ..................................................................................... 197
7.2.6 Model implementation.............................................................................. 198
7.3 Results ................................................................................................................ 198
7.3.1 Population growth rate for mackerel and whiting under current state
model ................................................................................................................. 198
7.3.2 Phase space models for mackerel and whiting ........................................ 199
7.3.3 Elasticity Analysis .................................................................................... 201
7.3.3.1 Mackerel .................................................................................. 201
7.3.3.2 Whiting ..................................................................................... 201
7.4 Discussion .......................................................................................................... 202
7.4.1 Mackerel................................................................................................... 202
7.4.1.1 Mackerel population dynamics ................................................ 202
7.4.1.2 Interpretation of impacts on mackerel ..................................... 203
7.4.2 Whiting ..................................................................................................... 204
7.4.2.1 Whiting population dynamics................................................... 204
7.4.2.2 Interpretation of impacts on whiting ........................................ 204
7.4.3 Species contrast........................................................................................ 205
7.4.4 Limitation of the modelling approach ...................................................... 206
7.5 Conclusions ........................................................................................................ 207
CHAPTER 8 USING AN ECOSYSTEM-BASED APPROACH TO DETECT
AQUACULTURE EFFECTS ON THE FOOD WEB IN A SEA LOCH .............. 209
8.1 Introduction ........................................................................................................ 209
8.2 Methods .............................................................................................................. 210
8.2.1 Study site .................................................................................................. 210
8.2.2 Ecopath production and consumption ..................................................... 211
8.2.3 Loch Melfort models construction ........................................................... 212
8.2.3.1 Loch Melfort functional groups ............................................... 212
8.2.3.2 Model inputs ............................................................................. 213
8.2.4 Model analysis ......................................................................................... 214
8.3 Results ................................................................................................................ 215
8.3.1 Trophic structure and flow ....................................................................... 215
8.3.1.1 Loch Melfort with fish and mussel farming (scenario 1) ......... 215
8.3.1.2 Loch Melfort with fish farming activity (scenario 2) ............... 216
8.3.1.3 Loch Melfort with mussel farming activity (scenario 3) .......... 216
8.3.1.4 Loch Melfort with no aquaculture activities (scenario 4)........ 216
8.3.2 Summary statistics and network flow indices .......................................... 226
8.3.2.1 Loch Melfort with fish and mussel farming (scenario 1) ......... 226
8.3.2.2 Loch Melfort with fish farming (scenario 2) ............................ 227
8.3.2.3 Loch Melfort with mussel farming (scenario 3) ....................... 227
8.3.2.4 Loch Melfort no aquaculture activities (scenario 4) ............... 227
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8.3.3 Mixed trophic impact analysis ................................................................. 229
8.4 Discussion .......................................................................................................... 235
8.4.1 The food web in Loch Melfort .................................................................. 235
8.4.2 Effects of aquaculture activities on the ecosystem ................................... 239
8.4.2.1 Effects of mussel farming ......................................................... 239
8.4.2.2 Effects of fish farming .............................................................. 240
8.4.2.3 Effects of both activities ........................................................... 241
8.4.3 Model assumptions and limitations.......................................................... 242
8.5 Conclusions ........................................................................................................ 244
PART III: GENERAL DISCUSSION AND CONCLUSIONS .............................. 245
CHAPTER 9 COMBINING EMPIRICAL AND MODELLING STUDIES
REVEALS A MORE HOLISTIC VIEW OF AQUACULTURE EFFECTS ....... 246
9.1 Introduction ........................................................................................................ 246
9.2 Fish farms attract fish and lead to direct individual level impacts ..................... 246
9.2.1 Coastal sea cages provide enhanced feeding (natural and artificial food)
grounds for fish ................................................................................................. 247
9.2.2 More food: better condition ..................................................................... 250
9.3 Fish farms: population sources, ecological traps or none? ................................ 251
9.4 Direct and indirect aquaculture effects on the ecosystem .................................. 252
9.5 Potential implications for fisheries, conservation and environment .................. 253
9.5.1 Potential benefits of fish farming to fisheries and conservation .............. 254
9.5.2 Implications for the environment ............................................................. 255
9.5.2.1 Environmental regulation of fish farming in Scotland ............ 255
9.5.2.2 Potential management solutions .............................................. 256
9.6 The use of pluralistic approach .......................................................................... 256
9.6.1 Empirical methodologies ......................................................................... 257
9.6.2 Modelling approaches .............................................................................. 258
9.6.3 The use of pluralistic approach ............................................................... 259
9.7 Conclusions ........................................................................................................ 260
REFERENCES ............................................................................................................ 263
APPENDIX A MARINE ORGANISMS CAUGHT NEAR TWO FISH FARMS:
CHAPTER 3 ................................................................................................................ 290
APPENDIX B ADDITIONAL INFORMATION FOR CHAPTER 4 ................... 313
APPENDIX C ADDITIONAL INFORMATION FOR CHAPTER 5 ................... 335
APPENDIX D ADDITIONAL INFORMATION FOR CHAPTER 6 ................... 358
APPENDIX E MODEL IMPLEMENTATION: CHAPTER 7 .............................. 364
APPENDIX F PARAMETRISATION OF FUNCTIONAL GROUPS IN
ECOPATH MODELS: CHAPTER 8 ....................................................................... 368
APPENDIX G ADDITIONAL INFORMATION FOR ECOPATH MODEL
SCENARIOS: CHAPTER 8. ..................................................................................... 382

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