The roles of capelin, climate, harp seals and fisheries in the failure of 2J3KL (northern) cod to recover by c Alejandro D. Buren A thesis submitted to the School of Graduate Studies in partial fulfilment of the requirements for the degree of Doctor of Philosophy Cognitive and Behavioural Ecology Programme Faculty of Science Memorial University of Newfoundland February 2015 St. John's Newfoundland Abstract The Atlantic cod (Gadus morhua) fishery sustained the way of life of Newfound- landers during centuries. Its collapse in the early 1990s represented a socio-economic and cultural crisis. Despite the fishing moratorium imposed in 1992, the northern cod stock (NAFO Divs 2J3KL) is still a shadow of its former self. Several hypotheses have been offered to explain this lack of recovery, many involving ecological interactions between harp seals (Pagophilus groenlandicus) and cod. However, these contentions are based on indirect evidence, while formal assessments are lacking. Availing of long term data series, I addressed the two simplest ways in which harp seals might impede cod's recovery: predation and competition for food resources, particularly for the major forage fish in the system: capelin (Mallotus villosus). I found no supporting evidence for either hypothesis. The biomass dynamics of northern cod during the period 1985-2007 were driven by an interplay between fisheries removals and food (capelin) availability, and potentially affected by water temperature. Harp seal predation was not an important driver of the stock. I provide evidence that a regime shift occurred on the Newfoundland and Labrador Shelf ecosystem during the early 1990s, linking community reorganization to physical perturbations. The capelin stock is regulated by bottom-up processes: ocean climate and the regime shift, acting via food availability. I found also that Atlantic cod did not change its diet following the regime shift. In addition, the diet of Atlantic cod overlapped to a greater extent with the diet of Greenland halibut than with harp seals' diet. These findings consti- ii tute mounting evidence against the consumptive competition hypothesis. The results presented in this thesis are important for the development of ecosystem approaches to fisheries management and raise questions as to the potential impacts of climate change on the structure and productivity of the Newfoundland and Labrador Shelf marine ecosystem. Also, this suggests that reductions in the harp seal population are unlikely to enhance the rebuilding of the northern cod stock; management efforts should be focused on protecting cod itself and the lower trophic levels. iii Acknowledgements I want to thank my co-supervisors Mariano Koen-Alonso and Bill Montevecchi, and committee member Garry Stenson for their guidance and support throughout the duration of my studies at MUN. Pierre Pepin, Fran Mowbray, Brian Nakashima, and Neil Ollerhead were instru- mental in seeing chapter 3 come to completion. I thank George Lilly, John Brattey and Karen Dwyer for sharing their data and comments. I also thank all staff at the Northwest Atlantic Fisheries Centre's Marine Mammal, Groundfish, Pelagics and Ecological Sciences sections who provided support and long term datasets. The Canada-Newfoundland Operational Ocean Forecasting System (C-NOOFS) Team and Andry Ratsimandresy helped with computing. Gary Maillet, Joanne Morgan, Peter Shelton, Hugues Beno^ıt,and Kenneth Drinkwater provided reviews, sugges- tions and/or comments that improved the quality of the chapters presented in this thesis. I would like to thank all members of the Montevecchi Lab ("The Other Guys"), the CABE Programme, and the Marine Mammals Section at DFO for support and encouragement along the way. Funding was provided by the Ecosystem Research Initiative (ERI) of the Depart- ment of Fisheries and Oceans Canada (DFO) for the Newfoundland Region (ERI- NEREUS), and fellowships from Memorial University. Special thanks to Garry Stenson and Jack Lawson for allowing me to complete iv the dissertation while working at the Marine Mammals Section. Most importantly, I would like to thank Sol for her enduring and loving patience and support. This dissertation would not have been possible without her. And to the three brightest lights in my life: Lara, Ana´ıs& Luana. v Contents Abstract ii Acknowledgments iv List of Tables xii List of Figures xiv Chapter 1: Introduction1 1.1 Newfoundland-Labrador Shelf Ecosystem and Species Background.. 3 1.1.1 Capelin .............................. 4 1.1.2 Atlantic cod............................ 5 1.1.3 Harp seal ............................. 6 1.1.4 Major changes to the ecosystem in the early 1990s....... 7 1.2 History of exploitation of marine resources in Newfoundland and Labrador9 1.3 Science in support of Ecosystem Based Fisheries Management in the Northwest Atlantic............................ 13 1.4 Cod-seals conflict............................. 17 vi 1.4.1 The conflict in Atlantic Canada................. 19 1.5 Thesis Objectives and Chapter Outlines ................ 21 1.6 Co-authorship Statement ........................ 24 1.7 References................................. 26 1.8 Figures................................... 43 Chapter 2: Is competition with harp seals and Greenland halibut a parsimonious hypothesis for the non-recovery of north- ern cod? Diet overlap and changes following the stock collapse 45 2.1 Abstract.................................. 45 2.2 Introduction................................ 46 2.3 Materials & Methods .......................... 49 2.3.1 Study Area ............................ 49 2.3.2 Data collection .......................... 50 2.3.3 Stomach content analysis..................... 51 2.3.4 Spatio-temporal distribution of predators............ 51 2.3.5 Factors affecting diet composition................ 52 2.3.6 Diet description.......................... 54 2.3.7 Comparison of predators' diets.................. 56 2.4 Results................................... 57 2.5 Discussion................................. 62 vii 2.6 References................................. 68 2.7 Tables................................... 78 2.8 Figures................................... 83 Chapter 3: Bottom-up regulation of capelin, a keystone forage species 93 3.1 Abstract ................................. 93 3.2 Introduction................................ 94 3.3 Materials and Methods.......................... 98 3.3.1 Data series ............................ 98 3.3.1.1 Climate......................... 98 3.3.1.2 Sea ice.......................... 99 3.3.1.3 Capelin ......................... 99 3.3.1.4 Prey of Capelin ....................101 3.3.2 Analyses .............................102 3.3.2.1 Capelin biomass ....................102 3.3.2.2 Capelin spawning....................104 3.3.2.3 Prey availability ....................104 3.4 Results...................................105 3.4.1 Climate ..............................105 3.4.2 Sea ice...............................106 3.4.3 Capelin biomass..........................106 3.4.4 Capelin spawning ........................107 viii 3.4.5 Prey availability..........................108 3.5 Discussion ................................108 3.5.1 The regime shift .........................111 3.5.2 The capelin regulating mechanism . 113 3.6 Concluding remarks ...........................118 3.7 References.................................120 3.8 Figures...................................135 Chapter 4: The role of harp seals, fisheries and food availability in driving the dynamics of northern cod 143 4.1 Abstract .................................143 4.2 Introduction ...............................144 4.3 Materials and methods .........................148 4.3.1 The Data .............................148 4.3.2 The model ............................151 4.3.3 Model implementation ......................154 4.3.4 Model comparison and selection . 155 4.3.5 Somatic condition ........................156 4.4 Results...................................158 4.4.1 Model Selection .........................158 4.4.2 Model Fits ............................160 4.4.3 Model Projections and hindcast . 161 ix 4.4.4 Balancing the effects of fisheries removals and capelin avail- ability on cod dynamics .....................162 4.4.5 Mortality .............................163 4.4.6 Somatic condition ........................164 4.5 Discussion ................................165 4.5.1 Main drivers of northern cod dynamics . 166 4.5.1.1 Fisheries removals as a driver . 167 4.5.1.2 Capelin availability as a driver . 167 4.5.1.3 Harp seal consumption as a driver . 171 4.6 Concluding remarks ...........................176 4.7 References.................................177 4.8 Tables ...................................192 4.9 Figures...................................202 Chapter 5: Summary and Synthesis: Interactions between Harp Seals and Northern Cod 218 5.1 Summary and synthesis of research Chapters . 219 5.1.1 Summary .............................219 5.1.2 Synthesis .............................224 5.2 Cod-seals in Atlantic Canada ......................226 5.3 Implications for management and conservation . 228 5.4 Future Directions.............................230 x 5.5 Conclusion.................................235 5.6 References.................................237 5.7 Figures...................................245 xi List of Tables Table 2.1 Annual sample sizes of Atlantic cod, Greenland halibut and harp seals stomachs, discriminated by ontogenic state and NAFO Divisions. 79 Table 2.2 Description