Kelp-forest response to light limitation Matthew Joseph Desmond a thesis submitted for the degree of Doctor of Philosophy at the University of Otago, Dunedin New Zealand. July 2016 i Abstract The loss of canopy-forming macroalgae is one aspect of coastal ecosystem degradation that is being driven by anthropogenic stressors. The drivers of canopy loss are, in many cases, well understood, but the effect of light availability is a factor that has been relatively overlooked given its importance. Light availability controls marine productivity and is a fundamental factor that shapes the structure of kelp-forest communities. When the variability of light availability exceeds natural thresholds as a result of anthropogenic stress, macroalgae struggle to acclimate or adapt and community structure and productivity is altered. Significant modification of the coastal light environment has likely occurred in many of the world’s coastal seas, and further increases in turbidity are predicted as a result of land use intensification, sea level rise and changing climatic conditions. This prediction forms the premise for this body of work. The primary objective was to detail the effect of light availability on the structure and function of kelp-forest communities, and to quantify the physiological processes that underpin this relationship. From this, a better understanding of how kelp-forest communities will respond to future changes in light availability is possible, and more accurate predictions of kelp-forest productivity can be made. Subtidal light availability was significantly less on reefs adjacent to coastlines dominated by urban, agricultural and forestry land use when compared to similar reefs associated with coastlines of native forest. When averaged over a seasonal cycle, light availability at 10 m on the low-light reefs was approximately half that measured on high- light reefs. The kelp-forest communities inhabiting these reefs were also shown to differ significantly. Although similar macroalgal species were shared between regions, community biomass was two to five times greater on high-light reefs. This was primarily due to a greater contribution by large canopy forming macroalgae. Additionally, macroalgae typically had a larger and deeper depth distribution on high-light reefs, in effect, providing more habitat and food to the kelp-forest ecosystem. This resulted in 0.7 – 2.8 times more epifaunal biomass being supported per square metre in high- compared to low-light reefs. Although this difference was largely due to greater habitat availability on high-light reefs, habitat quality was also shown to influence epifaunal biomass. The invasive kelp, Undaria pinnatifida, contributed significantly to community biomass on ii low-light reefs but was shown to support low epifaunal biomass as it offers low refuge value and, being an annual species, is an unstable host. Light limitation and the way that light is delivered to kelp-forest communities was shown to significantly influence the physiological processes of photoacclimation and photosynthesis. A photoacclimation response to light limitation was observed at the individual and kelp-forest community level between the low- and high-light reefs. In both cases greater pigment concentrations and accessory pigment to chlorophyll a ratios were recorded within the low-light setting. The cost of acclimation under low-light conditions helps to explain the disparity in standing biomass between the low- and high-light reefs, as energy, otherwise used for growth, is diverted to synthesise additional photosynthetic pigments. There was also evidence that a number of species on the low-light reef were living at the edge of their photosynthetic ability, and that a further reduction in light would likely result in a loss of those species at deeper depths. The rate that light is delivered to kelp-forest communities was shown to significantly affect macroalgal productivity, and in some cases may be more influential than the total amount of light that they receive. Greater photosynthetic efficiency at lower light intensity was shown to compensate for even large disparities in the total amount of light that dominant kelp-forest species received. This demonstrates that both the limitation of light and variability of its delivery are key determinants of kelp-forest structure and productivity. This thesis provides evidence that is suggestive of a change in kelp-forest communities in southern New Zealand as a result of light limitation. The findings from this study are applicable at a global scale and provide important information that will help improve estimates of kelp-forest productivity and persistence, now, and under future light regimes. iii Acknowledgements The decision to undertake this PhD was one of the best choices I have made. The knowledge that I leave with is far beyond academic, and in many cases totally unrelated to my field of study, in my opinion these were the most important lessons. I owe a great deal of gratitude to my primary supervisor and friend, Chris Hepburn, who has supported me now through two degrees. You were the key factor that encouraged me to take on this challenge and you have provided me with so many fantastic opportunities, both inside and outside of study that I am truly grateful for. The way you value teamwork, relationships and most importantly fun are characteristics that I aspire to as a scientist, thanks! To my secondary supervisor, Will Rayment, your guidance through the final stages of this PhD has been invaluable, as has your friendship and the example you set. To my surrogate supervisor, Dan Pritchard, the time and effort you have dedicated to me, purely because you’re a nice guy, is beyond what I could have expected and I want to acknowledge the role you have played in this PhD, it has been huge! Finally, to Wendy Nelson, I’m extremely grateful for the many hours you spent getting bitten by sandflies and reminding me for the 13th time what seaweed species I was looking at, you are always a pleasure to work with. By far the most enjoyable aspect of this project has been the time spent in the field, and that is due primarily to the people who I have shared it with. To Tiffany Stephens, Peri Subritzky, Rocio Suárez-Jiménez, Emma Kearney, Brenton Twist, Cohen Stewart, Jordan Housiaux, Kyle Swan, Shaun Cunningham, Keiran Pullman, Tom Brough, Derek Richards, Eugene Leahy, Liina Pajusallu, and Maryse Wong-Ah-See, you guys have been amazing to work with and have made this process so easy and enjoyable, cheers dudes! In the same vein I would like to thank all the skippers who I’ve had the pleasure of spending time with, Sean Heseltine, Steve King, Paul Meredith, Bill Dickson, Dave Wilson and Evan Kenton. Although your tendency to talk about the ‘Great White Death’ before each dive was not appreciated, your skills, easy-going attitudes and breadth of knowledge was valued greatly. For the technical expertise of Reuben Pooley, Linda Groenewegen, Bev Dickson and again Dave Wilson, I am very thankful. To Richard Taylor, who provided me with a huge amount of information regarding epifauna both directly and via Rocio, I would like to say thanks. Finally I would like to acknowledge the East Otago Taiāpure iv Committee, and Brendon Flack, who have shown enthusiasm and support for this project, and a number of others that I have been involved in over the past few years. To base my research within a framework where it is applied has added a lot of value and satisfaction for me. My family has given me unwavering support throughout my PhD, and in life in general. You all set an incredible example in unique ways and I attribute a lot of what I have achieved to you guys. Finally, to Rianda, you encouraged me to undertake this PhD and have never stopped since, thanks for being there always, even if it was from the other end of the country, baie dankie! v Table of contents Chapter 1 ............................................................................................................................... 1 1.1 Degradation of global coastal ecosystems .............................................................. 2 1.2 The importance and decline of kelp-forest communities ........................................ 3 1.2.1 What is a kelp-forest community? ................................................................... 3 1.2.2 Kelp-forest community structure in New Zealand .......................................... 4 1.2.3 Ecosystem services provided by kelp-forest communities .............................. 5 1.2.4 The link between kelp-forest communities and upper trophic levels .............. 7 1.2.5 The current state of kelp-forest communities .................................................. 7 1.3 The drivers of kelp-forest loss ................................................................................ 8 1.4 Light in temperate coastal seas ............................................................................. 10 1.4.1 The path of light ............................................................................................ 10 1.4.2 The effect of light limitation .......................................................................... 11 1.4.3 The changing subtidal light environment ...................................................... 12 1.5 Study environment ................................................................................................ 13 1.5.1 Study sites .....................................................................................................