University of Southampton Faculty of Natural and Environmental Sciences School of Ocean and Earth Sciences The influence of ocean warming on the provision of biogenic habitat by kelp species by Harry Andrew Teagle (BSc Hons, MRes) A thesis submitted in accordance with the requirements of the University of Southampton for the degree of Doctor of Philosophy April 2018 Primary Supervisor: Dr Dan A. Smale (Marine Biological Association of the UK) Secondary Supervisors: Professor Stephen J. Hawkins (Marine Biological Association of the UK, University of Southampton), Dr Pippa Moore (Aberystwyth University) i UNIVERSITY OF SOUTHAMPTON ABSTRACT FACULTY OF NATURAL AND ENVIRONMENTAL SCIENCES Ocean and Earth Sciences Doctor of Philosophy THE INFLUENCE OF OCEAN WARMING ON THE PROVISION OF BIOGENIC HABITAT BY KELP SPECIES by Harry Andrew Teagle Kelp forests represent some of the most productive and diverse habitats on Earth, and play a critical role in structuring nearshore temperate and subpolar environments. They have an important role in nutrient cycling, energy capture and transfer, and offer biogenic coastal defence. Kelps also provide extensive substrata for colonising organisms, ameliorate conditions for understorey assemblages, and generate three-dimensional habitat structure for a vast array of marine plants and animals, including a number of ecologically and commercially important species. This thesis aimed to describe the role of temperature on the functioning of kelp forests as biogenic habitat formers, predominantly via the substitution of cold water kelp species by warm water kelp species, or through the reduction in density of dominant habitat forming kelp due to predicted increases in seawater temperature. The work comprised three main components; (1) a broad scale study into the environmental drivers (including sea water temperature) of variability in holdfast assemblages of the dominant habitat forming kelp in the UK, Laminaria hyperborea, (2) a comparison of the warm water kelp Laminaria ochroleuca and the cold water kelp L. hyperborea as habitat forming species, and further investigation into the impacts of this subtle climate driven substitution of habitat forming kelps, and (3) experimental manipulation of densities of the dominant intertidal kelp in the UK, Laminaria digitata, in order to understand the impacts of climate driven loss of a dominant habitat forming species. L. hyperborea assemblages varied significantly between study regions spanning ~9° of latitude, as well as between and within sites at a local scale. Patterns in mobile and sessile assemblage structure were driven principally by different environmental factors. Overall patterns in the structure of biogenic habitat and assemblage structure did not vary predictably with latitude, indicating that other processes acting across multiple spatial scales are important drivers of assemblage structure. L. ochroleuca hosted impoverished assemblages associated with both holdfasts and stipes, compared with L. hyperborea. Further, climate driven increases in the relative abundance of L. ochroleuca relative to L. hyperborea lead to disruption of an important habitat cascade associated with the stipe of L. hyperborea and epiphytic algae. L. ochroleuca stipes typically lack the dense epiphytic assemblage associated with L. hyperborea, and host depauperate faunal assemblages which may have impacts on higher trophic levels. Experimental reduction in the density of L. digitata led to a dramatic shift in dominance from perennial to annual species, particularly the pseudo-kelp Saccorhiza polyschides on an exposed rocky shore. Impacts on a sheltered shore were subtler, and may have been tempered by the presence of another perennial kelp, Saccharina latissima. Loss of L. digitata led to a reduction in the standing stock of macroalgae after ~2.5 years of manipulation on both shores. These findings have significant implications for the structure and functioning of rocky shores in the future. Overall, anthropogenic climate change is likely to negatively impact the functioning of kelp forests as repositories of biodiversity in the future via the reshuffling of warm- and cold-water kelp species and through an overall loss of algal biomass and associated habitat due to continued increases in seawater temperature in the northeast Atlantic. ii Contents Abstract ii Contents iii Figure List vii Tables List xiv List of Appendices xx Declaration of Authorship xxi Acknowledgements xxiv Chapter 1 – General Introduction 27 1.1. Opening remarks 28 1.2. Role of kelps in ecosystem structure and functioning 28 1.3. Direct provision of biogenic habitat 31 i. Holdfast assemblages 31 ii. Stipe assemblages 39 iii. Blade assemblages 42 iv. Habitat preference of kelp fauna 44 v. The quantity of biogenic habitat provided by kelps 45 1.4. Physical and biological regulation of habitat provision 47 i. Physical regulation 47 ii. Biological regulation 49 1.5. Understorey assemblages and wider biodiversity 52 1.6. Ecological goods and services provided by kelp forests 57 1.6. Threats to biogenic habitat provided by kelps 59 1.7. Rational and aims of thesis 62 Chapter 2 - Spatial variability in the diversity and structure of faunal assemblages associated with kelp holdfasts (Laminaria hyperborea) in the northeast Atlantic 65 2.1. Abstract 66 2.2. Introduction 66 2.3. Methods 71 i. Study area 71 ii. Environmental variables 73 iii. Sample collection and processing 74 iv. Statistical analysis 75 2.4. Results 76 iii i. Environmental variables 76 ii. Biogenic habitat structure 77 iii. Overall biodiversity patterns 78 iv. Sessile assemblages 79 v. Mobile assemblages 83 vi. Combined assemblages 86 2.5. Discussion 88 Chapter 3 - Climate-driven substitution of habitat-forming species leads to reduced biodiversity within a temperate marine community 95 3.1. Abstract 96 3.2. Introduction 96 3.3. Methods 100 i. Temporal trends in the relative abundances of kelp HFS 100 ii. Environmental variables 100 iii. Sample collection 100 iv. Sample processing 102 v. Statistical analysis 102 3.4. Results 103 i. Temporal trends in the relative abundances of kelp HFS 103 ii. Biogenic habitat structure 103 iii. Stipe assemblages 104 iv. Holdfast assemblages 108 3.5. Discussion 112 Chapter 4 - Climate-driven range expansion of a foundation species leads to the breakdown of a facilitation cascade and altered community structure 119 4.1. Abstract 120 4.2. Introduction 120 4.3. Methods 125 i. Study area 125 ii. Kelp canopy structure 126 iii. Sample collection and processing 126 iv. Fish stomach contents 127 v. Comparison between pre- and post-climate driven range expansion 127 vi. Statistical analysis 128 iv 4.4. Results 128 i. Habitat structure 128 ii. Assemblage structure 131 iii. Fish stomach contents 133 iv. Comparison between regions, pre- and post-expansion of Laminaria ochroleuca 134 4.5. Discussion 136 i. Consequences of climate-driven shifts for epiphytic assemblages 136 ii. Environment context 138 iii. Trophic consequences 139 iv. Future patterns 140 v. Concluding remarks 140 Chapter 5 - Climate-driven extinction scenario reveals how loss of marine foundation species leads to altered community structure and biomass dynamics on temperate rocky shores 143 5.1. Abstract 144 5.2. Introduction 144 5.3. Methods 149 i. Study sites 149 ii. Experimental reduction and loss of a canopy former at the range edge 150 iii. Data collection 151 iv. Statistical analysis 151 5.4. Results 153 i. Laminaria digitata versus main competitor 153 ii. Multivariate assemblage 156 iii. Destructive sampling 159 1. Canopy forming algae 159 2. Understorey algae 164 3. Total assemblage biomass 165 5.5. Discussion 166 i. Effects of L. digitata manipulation at exposed sites 166 ii. Effects of L. digitata manipulation at sheltered sites 167 v iii. Effects of L. digitata manipulation on understorey algal assemblages 169 iv. Influence of L. digitata manipulation on other Laminaria spp. 169 v. Impacts of L. digitata manipulation on standing stock of macroalgae 170 vi. Conclusions 171 Chapter 6 – General Discussion 173 6.1. Main conclusions 174 6.2. Ecological significance of current findings 175 6.3. Implications for conservation and management 180 6.4. Limitations and future research 186 6.5. Concluding remarks 187 Appendices 189 Appendix 1 190 Appendix 2 191 References 199 vi Figure list Figure 1.1. Approximate global distribution of dominant genera of the Laminariales. Modified and adapted from Steneck et al. (2002) and Steneck and Johnson (2013). 30 Figure 1.2. Schematic depicting the primary biogenic microhabitats (the blade/lamina, stipe and holdfast) provided by kelps, as well as secondary habitat (epiphytes) and the wider substratum modified by kelp canopies. Model kelp species shown are Laminaria hyperborea (left) and Laminaria ochroleuca (right). Interspecific variation in kelp morphology, structure and life history strongly influences habitat provision for the associated community. 31 Figure 1.3. Interspecific variability in the structure of the holdfast habitat provided by kelps. The ‘typical’ laminarian holdfast structure is illustrated by (A) Laminaria ochroleuca (example shown from Plymouth, UK), which is often colonised by a rich and abundant sessile invertebrate assemblage, and (B) Laminaria pallida (South Africa), which provides a highly complex and intricate microhabitat for associated organisms. Other typical laminarian species include (C) Ecklonia radiata (Western Australia), shown here supporting a high coverage of ecologically-important