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Ecophysiology of Habitat-Forming Seaweeds in a Changing Environment

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Ecophysiology of Habitat-Forming Seaweeds in a Changing Environment Ecophysiology of habitat-forming seaweeds in a changing environment Emma Flukes BMarSci (Hons) A thesis submitted in fulfilment of the requirements for the Degree of Doctor of Philosophy in Marine Science Institute for Marine and Antarctic Studies (IMAS) University of Tasmania July 2015 This page intentionally left blank Declarations Statement of originality This thesis contains no material which has been accepted for a degree or diploma by the University or any other institution, except by way of background information and duly acknowledged in the thesis, and to the best of my knowledge and belief no material is previously published or written by another person except where due acknowledgement is made in the text of the thesis, nor does the thesis contain any material that infringes copyright. Signed: (Emma Flukes) Date: 3rd July 2015 Statement of authority of access This thesis may be available for loans and limited copying and communication in accordance with the Copyright Act 1968. Signed: (Emma Flukes) Date: 3rd July 2015 i Abstract ‘Ecosystem engineering’ species play a disproportionately important role in ecological systems by modifying (creating or destroying) habitat for other species. Understanding the impact of climate change is particularly critical for habitat-forming ecosystem engineers, as these species are generally facilitative and form the basis of hierarchically organised communities. In temperate marine environments, seaweed beds provide the fundamental structure of most shallow rocky reef communities. The coastline of southeastern Australia is warming at nearly four times the global average rate, with temperature increases occurring simultaneously with reduced nutrient availability due to strengthening seasonal incursions of warm, oligotrophic East Australian Current water. Climate change-driven range contractions in this area have already been documented for the canopy-forming Ecklonia radiata and Phyllospora comosa, while the areal coverage of Macrocystis pyrifera forests in Tasmania has declined by ~95% over the last 3-4 decades. Continued climatic change in this region is likely to impact on the physiological performance, reproductive capacity, survival, and ultimately the distribution of important habitat-forming seaweeds. Predicting the future impacts of climate change on species distributions has largely focused around the use of bioclimate envelope models (BEMs), which relate field observations of a species’ geographic distribution with environmental predictor variables to forecast its future distribution. This generalised modelling approach relies on the assumption that the physiological performance of a species under a given set of environmental conditions will be consistent across its range. However, Elser’s Growth Rate Hypothesis (GRH) predicts that the performance of photosynthetic organisms will vary with latitude due to increased selective pressure for rapid growth at high latitudes resulting from a growth season that is shortened by low light availability. Determining whether the GRH is applicable to habitat- forming seaweeds is a critical step to evaluating the efficacy of BEMs in predicting the future impacts of climate change on seaweed distributions. This thesis assesses the likely impacts of climate change on the physiology of the key biogenic habitat-forming seaweeds E. radiata, P. comosa and M. pyrifera in southeastern Australia. It employs a unique multivariate approach by assessing a complex suite of ii performance and ecophysiological characteristics including photophysiological indicators (photosynthetic characteristics via PAM fluorometry and concentration of photosynthetic pigments), nutrient uptake dynamics (% C, % N and C:N ratios), C metabolism (stable C isotope δ13C), and RNA:DNA ratios (as a proxy for growth rate). These physiological performance indicators are assessed within the conceptual framework of the GRH, and ultimately enable evaluation of the suitability of bioclimate envelope models for predicting the future performance and distribution of seaweeds under projected climate change scenarios. The thesis also investigates the likely impacts of climate change-driven loss of seaweed canopy on associated understory communities, which is critical in evaluating the use of BEMs as the effects of biotic (competitive) interactions among species are normally assumed to be unimportant. Chapter 2 investigates the influence of temperature and nitrate – two key environmental factors predicted to vary with future climate change – on the growth and ecophysiology of P. comosa from the northern and southern parts of its range. The physiological performance of this species was strongly temperature-dependent, but the deleterious effects of high temperatures on photosystem functionality were particularly pronounced in thalli originating from higher latitude. In contrast, nitrate availability played only a minor role in regulating seaweed physiology, suggesting that P. comosa at high latitudes may be less susceptible to nutrient stress than predicted by the GRH, but that the species will respond to predicted levels of warming with a loss of photosystem functionality unless rapid adaptation is possible. Chapter 3 explores the extent to which E. radiata and P. comosa may acclimatise to environmental change through phenotypic plasticity, and how this plasticity may vary across their latitudinal distributions. Thalli were transplanted from low to high latitudes (with appropriate controls) and their physiological performance monitored over four months. Trait expression was found to be largely under environmental control despite considerable ecophysiological differences between in situ populations from sites at high and low latitudes, demonstrating the considerable capacity of these species to acclimatise to a wide range of environmental conditions. Chapter 4 examines longer-term patterns in the seasonal in situ physiology of E. radiata, P. comosa and M. pyrifera in relation to environmental characteristics, and how this varies across their latitudinal and depth distributions. Temperature and irradiance were determined iii to be important regulators of seaweed physiology, but as with controlled laboratory experiments, nitrate availability was less important (except for M. pyrifera, which has very limited internal nitrogen storage capacity). Seaweeds at high latitudes were more adversely affected by high temperature and low nutrients during summer than their lower latitude counterparts (particularly in shallower water) seemingly due to the synergistic interaction of climatic stressors with high irradiance. Thus, while predicted climate-driven changes may impact similarly on seaweeds across their latitudinal distributions, high latitude populations are likely to experience increasingly stressful summers and may retreat to deeper waters and/or become more sparse and patchy. Chapter 5 assesses the impacts of potential climate change-driven thinning of seaweed canopy on the structure of associated understory community assemblages. Canopy thinning of E. radiata (as opposed to total canopy removal) affected a shift towards a foliose algal- dominated understory, with an associated loss of sponges, bryozoans and encrusting algae. While the structure of kelp-associated understory assemblages in southeastern Tasmania appears relatively stable, even partial loss of kelp canopy cover under future climate change scenarios will likely shift these communities towards a foliose algal-dominated state, which has important biodiversity implications. This thesis demonstrates the considerable capacity of seaweeds to respond to environmental change through phenotypic plasticity. While no evidence was found to support the GRH, multivariate ecophysiological measurements revealed subtle latitudinal variation in seaweed physiology in situ; indicating that a broad-scale climate envelope approach will not adequately predict the future performance and distribution of seaweeds under predicted climate change. The key findings of this thesis are: (1) a multivariate approach is required to describe and interpret seaweed physiology, particularly when attempting to detect organismal-scale changes that may ultimately impact on the performance and local survival of a species; (2) the GRH does not apply to E. radiata and P. comosa, but seaweeds at higher latitudes are more susceptible to increasing water temperature than is often assumed due to the synergistic interaction between high temperature and high irradiance over summer; and (3) bioclimate envelope models are unlikely to be a useful tool for predicting the performance and distribution of seaweeds under future climate change scenarios. iv Contents Declarations i Abstract ii Contents v List of Tables x List of Figures xi Acknowledgements xiv Statement of co-author contributions xvi 1 Introduction 1 2 Phenotypic plasticity and biogeographic variation in physiology of a habitat- forming seaweed: response to temperature and nitrate 10 2.1 Abstract ..................................................................................... 10 2.2 Introduction ................................................................................. 11 2.3 Materials and Methods .................................................................... 14 2.3.1 Study species, seaweed collection, and in situ sampling .............................14 2.3.2 Experimental design and culture conditions ...........................................15 2.3.3 Ecophysiological measurements .........................................................17
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