"Establishment and persistence of dense stands of the introduced kelp Undaria pinnatifida" by Joseph Peter Valentine BSc(Hons), University of Tasmania Submitted in fulfilment of the requirements for the Degree of Doctor of Philosophy University of Tasmania (April, 2003) II Statement of Originality This thesis contains no material that has been accepted for a degree or diploma by the University or any other institution. To the best of my knowledge and belief, this thesis contains no material previously published or written by another person, except where due acknowledgement is made in the text. Joseph Peter Valentine Statement of Authority of Access This thesis may be made available for loan and limited copying in accordance with the Copyright Act 1968. Joseph Peter Valentine DI Acknowledgements To begin I would like to thank my supervisor, Craig Johnson for his encouragement and support over the duration of the project. Your efforts to secure funds made this work possible and for that I am very grateful. Your help and advice on experimental design and analysis was also appreciated, as was your understanding during some challenging times. An intensive diving project such as this one cannot be completed successfully (and safely) without a reliable diving buddy. This work could not have been conducted without the help of my fellow PhD student and friend Hugh Pederson. Hugh's assistance and advice above and below the water, particularly on all things mechanical was invaluable. I also appreciate Hugh's understanding in accommodating field schedules to meet the needs of both of our projects. It was not all hard work though- a tough day of Undaria surveying around Maria Island was often rounded out by fine cuisine, with 'Peanut butter chicken' a favourite. And Hugh, a Cosmonaut is a Russian Astronaut by definition. Case closed. The Zoology technical staff, in particular Adam Stephens, Simon Talbot and Richard Holmes provided valuable support during the project. I would especially like to thank Richard Holmes for his help with constructing field equipment and repairing gear at short notice (especially that leaky drysuit!). The fieldwork could not be completed without the assistance of numerous volunteers. A big thankyou to Matt Field, Sean Hooper, Dirk Welsford, Jeremy Heath, Scott Ling, Regina Magierowski, Jeff Ross, Piers Dunstan, Susie Forbes, and Phillipe Ziegler. I would particularly like to thank Ed Forbes, Miles Lawler and Liz Pietrokowski for their assistance during numerous field trips. To the members of Craig's lab, thankyou for your advice and friendship over the past 4 1/2 years, it's been a fantastic time. Dr. Ross, your work ethic was an inspiration to me, but I don't want to pump up your tyres too much. Look forward to you returning when you complete your "sentence" on the north island. Piers, you are a strange looking "chap", but your statistical advice was second to none. Regina, thanks for your help and friendship, and for keeping the chocolate shop stocked. Scott, thanks for those epic tales of fishing adventure-from blue water tuna encounters to pan-sized trout escapades. To my family, thankyou for supporting and encouraging me to pursue my dreams, I hope I can repay you someday. Dad, thanks for your guidance and proof-reading prowess. And finally to Jane, thanks for your patience and support over the last few years. I'm really looking forward to spending time with you and "Romy" once this is all over. INT Abstract Despite high rates of occurrence of non-indigenous organisms in the marine environment, few studies have critically examined mechanisms underpinning the invasion process. In this study manipulative experiments and observations of a natural disturbance to native marine algae were used to examine the invasion dynamics of the Asian kelp Undaria pinnatifida on the east coast of Tasmania. Disturbance to reduce cover of the native algal canopy was found to be a critical stage in the establishment of U. pinnatifida, while the presence of a stable canopy of native algae inhibited sporophyte development. In the first season of sporophyte growth following artificial canopy removal, U. pinnatifida recruited at high densities (up to 19 plants m-2) while remaining rare or absent in unmanipulated plots. A similar response was recorded in areas where native macroalgae declined through natural processes. These results suggest that microscopic U. pinnatifida gametophytes or sporophytes presently occur throughout these native algal beds, but do not develop into visible sporophytes while the canopy is intact. The timing of disturbance was also an important factor. U. pinnatifida recruited in higher densities in plots where the native canopy was removed just prior to the sporophyte growth season (winter), compared to plots where the canopy was removed six months earlier during the period of spore release (spring). In the second year following canopy removal, U. pinnatifida abundance declined significantly, associated with a substantial recovery of native canopy-forming species. This supports the hypothesis that continued disturbance or stress to reduce cover of native algae is required for persistence of dense stands of U. pinnatifida. Recovery of native algae after infestation by U. pinnatifida was investigated in greater detail in a large manipulative experiment conducted on a sea urchin 'barren' (Heliocidaris erythrogramma) seasonally dominated by dense cover of U. pinnatifida. This habitat was chosen as a model system to investigate persistence of U. pinnatifida for two reasons. Firstly, U. pinnatifida occurs most abundantly in Tasmanian waters on these urchin barrens and secondly, the level of disturbance could be easily manipulated in this system by controlling sea urchin density. The experiment examined the response of U. pinnatifida and native macroalgae to treatments comprising all combinations of presence and absence of sea urchins, presence and absence of U. pinnatifida sporophytes, and presence and absence of fertile native macroalgae. U. pinnatifida not only persisted in the absence of sea urchin grazing, but was significantly more abundant compared to areas where urchin densities remained un-manipulated. Recovery of native canopy-forming species was minimal, even in treatments from which sea urchins and U. pinnatifida were removed, and an enhanced supply of native algal spores provided. Thus, factors other than urchin grazing were limiting development of native algae, consequently there was no evidence of inhibition of U. pinnatifida by native canopy species. Recovery of native canopy-forming species was also examined in a transplant experiment. Settlement pavers colonised by high densities of native canopy-forming species were transplanted from an algal bed to sea urchin removal areas on an adjacent urchin barren. Following transplantation a marked reduction in cover of V canopy-forming algal recruits occurred in the absence of high densities of sea urchins, while cover was not affected on handling controls (pavers treated similarly but re- deployed into the algal bed). These results suggest that U. pinnatifida may persist in the absence of disturbance in some circumstances, because other factors are limiting the recovery of native algae on the urchin barren. Canopy removal led to accumulation of a sediment matrix on the substratum, which is likely to influence settlement and development of early developmental stages of native algae. A consistent cover of sediment was observed on a large scale on the urchin barren, and rapidly developed on pavers transplanted to the urchin barren. Accumulation of sediment on the natural substratum, beneath dense algal cover was minimal by comparison. It appears that sediment accumulation plays a major role in inhibiting recruitment of native canopy-forming species. The results of this work provide management options for control of U. pinnatifida. Where disturbance is linked to anthropogenic activity, managing the disturbance is likely to prove a more practical and cost-effective method of controlling invasion of U. pinnatifida at high densities than targeting the plant directly. On the east coast of Tasmania, preventing formation of H. erythrogramma barrens is of fundamental importance in this context. VI Table of Contents TITLE PAGE DECLARATIONS II ACKNOWLEDGEMENTS III ABSTRACT IV TABLE OF CONTENTS VI CHAPTER 1 1 General Introduction 1 CHAPTER 2 9 "Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages" 9 2.1 Abstract 9 2.2 Introduction 10 2.3 Materials and methods 13 2.3.1 Study site 13 2.3.2 Experimental manipulations 15 2.3.3 Assessment of algal abundance 16 2.3.4 Analysis 17 2.4 Results 20 2.4.1 The effect of canopy removal on density of Undaria pinnatifida and native canopy-forming algae 20 2.4.2 Native canopy-forming algae: Species composition 23 2.4.3 Recovery of native canopy algae: Percentage cover 23 2.4.4 Response of understorey algae to canopy disturbance 26 2.4.5 Effect of canopy removal on sediment cover 29 2.4.6 Community level effects 34 2.5 Discussion 37 2.5.1 Undaria pinnatifida: opportunist or super competitor? 37 2.5.2 Maintenance of Undaria pinnatifida stands post-establishment 41 2.5.3 Recovery of native canopy-forming species following disturbance 42 2.5.4 Canopy removal and the sediment matrix 44 2.5.5 Destructive sea urchin grazing: an important source of disturbance? 46 2.5.6 Conclusions 47 CHAPTER 3 48 "Establishment of the introduced kelp Undaria pinnatifida following dieback