i Habitat creation for animals by teredinid bivalves in Indonesian mangrove ecosystems A thesis submitted in partial fulfilment of the requirements for the award of the degree of Doctor of Philosophy of the University of Portsmouth By Ian Wyndom Hendy Institute of Marine Sciences, School of Biological Sciences University of Portsmouth PO4 9LY October 2012 ii Abstract A better understanding of the fundamental role large woody debris (LWD) plays within mangrove ecosystems may provide further insights into important ecological processes, such as wood degradation and biodiversity maintenance within mangrove forests.Though the volume of fallen wood in mangrove forests can be huge, little is known of the breakdown pathways and biodiversity maintenance of LWD in mangrove ecosystems. The degree of mangrove fauna dependent upon LWD and the need for such substratum in mangrove ecosystems may provide further insights in to the important role of woody biomass in these otherwise globally shrinking habitats due to forest harvesting. The breakdown, recycling and flux of nutrients from LWD within mangrove forests is maintained by biodegrading organisms in areas from terrestrial to marine habitats. The tidal inundation sets limits on the wood degrading communities within the mangrove forests of Sulawesi. This study presents details of the environmental and biological association of biodegrading organisms within the forests in the Wakatobi Marine Park (WMP), Sulawesi. Wood boring animals belonging to the family Teredinidae are the dominant biodegraders of LWD in the mid- to low- intertidal areas of the mangrove forests. Teredinid attack greatly reduces the volume of LWD in the mid- to low intertidal areas of the forests. Within the forests, emersion time was the greatest influence of the distribution of the biodegrading organisms spanning from the supra-tidal down to the low intertidal. The response of Rhizophora stylosa prop-roots to physical damage and the activity of teredinids upon damaged prop-roots were investigated. With severe levels of root damage, the level of teredinid activity increases, resulting in root death and iii detrital input. However, when the roots were exposed to a superficial and moderate level of damage, an over-compensation of tissue re-growth was observed. LWD in the intertidal zone is often tunnelled by teredinids. The tunnels are blind-ending cylinders that taper to a small opening at the wood surface. However, larger openings appear when wood is heavily tunnelled and the surface is broken open. Teredinid death then leaves niches for cryptofauna. The greater the number of teredinid tunnels within LWD, the more diversity was found. Animals of particular interest were the dartfish, Parioglossus interruptus and the intertidal spider, Desis martensi found in the vacant teredinid tunnels. Desid spiders were abundant within the LWD and dartfish collected from within teredinid-attacked LWD were smaller than dartfish populations not within LWD. Desids and dartfish residing within the wood may benefit from the significantly lower temperatures within teredinid-attacked detritus compared to external air temperatures. Desis martensi has a life-history strategy centred on strong parental care, with lots of energy invested in to its young. Vulnerable stages of dartfish exploit the vacant teredinid tunnels. If it were not for the tunnels created by the teredinids the unusual behaviour adopted by dartfish and spiders would not be possible. Thus, many animals in mangrove forests of the WMP rely on LWD as a predation refuge enhanced by the teredinid tunnels within the LWD. A variety of different species were found inside teredinid attacked LWD, and the cryptic behaviour of the fauna ranged from breeding to predator avoidance. These findings indicate that in forests where wood is harvested, reduced availability of LWD will result in reduced biodiversity. iv Acknowledgements First and foremost, I wish express my sincere and total gratitude to Simon Cragg, for seeing something in me which I believed I was not capable of. I thank Simon for his tireless work ethic and professionalism. Thank you for your support, encouragement and guidance. I am very grateful towards Operation Wallacea for providing research funding and providing the resources to make this project possible. I also want to give my sincerest thanks to Amat and Kungdan – my wonderful mangrove posse who worked with me with enthusiasm and passion, in long hard days when in the field. I miss those guys. In addition, I also wish to give an extended very large Ian bear-hug to several Hoga stalwarts – like Simon, you have been a role-model and inspiration to me, Richard Barnes and Chris Todd. To the dynamic and cheerful IMS team – it has been a pleasure to have been a part of this institution for a number of years. The enthusiasm, passion and drive of each and every one of you are infectious. In the early years, the support network provided by Maureen and Ray and during the completion of my study Lucy, Graham, Amaia, and Matt has been a constant source of encouragement, thank you. I would also like to give a big thank you to Scott Armbruster, for his expert opinions and rapid feed-back with various drafts of this thesis. My gratitude and appreciation also goes out to David Jones (The Natural History Museum of London) for identification of termites. J. Lawrence for his identification of coleopteran larvae, and G. Jones and L. Ryvarden for their help towards identification of the v basidiomycetes fruiting bodies. A big thank you goes out to Trevor Willis, for his expert advice on using the PRIMER statistical package. Furthermore, I would like to thank my very hard working American colleagues who I have worked with on Hoga Island. Wayne, John and Theresa, each of you have been a pleasure to work with. I have learnt so much with other scientific disciplines – all of which is thanks to you guys. The seemingly hard endless hours you all put in to your lab-work was a lesson in itself. A special mention must go to Peter Chivers – another role model of mine. Although you are gone and missed, you have never been forgotten - your encouragement and belief in me during my A- levels and GCSEs when attending Highbury College was such a boost. Also, very special thanks go out to Tricia Farnham, my A- level biology teacher. Combined with my collaborators and colleagues, to my family and friends – your support and constant belief in me throughout has been amazing and a real source of energy. Clare, thank you for putting up with me over the last year, you have been a ray of sunlight. Mum, Matt thank you both for supporting me all the way. To my boys at the gym, you must be the only bodybuilders who know what teredinid bivalves are! Thank you all, for being so understanding and patient. Grandpa, although you are no longer with us – this PhD is dedicated to you, I miss you… vi List of contents Chapter 1 General introduction 1.1 Overview 1 1.1.1 Indo-Pacific mangrove systems 2 1.1.2 Mangrove biomass and partitioning 6 1.1.3 Detrital input and breakdown pathways 8 1.1.4 Role of fallen mangrove wood 10 1.2 The Teredinidae (Mollusca: Bivalvia) 13 1.3 Study site, the Wakatobi Marine Park 15 1.4 Research aims and objectives 18 Chapter 2 MANGROVE FORESTS OF THE WMP, EAST SULAWESI, INDONESIA 2.1 Introduction 20 2.2 Materials and methods 2.2.1 Belt transects, tree identification, and measurements of emersion time and salinity 22 2.2.2 Mangrove forest descriptions 23 2.2.3 Tree densities and species basal area 29 2.3 Data analysis 31 2.4 Results 32 vii 2.4.1 Mangrove area and botanical distributions 32 2.4.2 Environmental factors 34 2.4.3 Canopy-forming trees and forest characteristics 36 2.4.4 Tree species dominance – basal areas, biomass and tree densities 43 2.4.5 Site similarity and tree species diversity 55 2.5 Discussion 58 Chapter 3 INVESTIGATION OF WOOD BIODEGRADATION IN MANGROVE ECOSYSTEMS 3.1 Introduction 66 3.2 Materials and methods 71 3.2.1 Measurement of wood-loss in panels 71 3.2.2 The measurement and collection of dead wood and arbitrary scale classification and wood-loss from teredinid attack 72 3.2.3 Wood degrading organisms and environmental factors in the Galua and Laulua mangrove forests 75 3.3 Data analysis 76 3.4 Results 77 3.4.1 Wood degradation within the landward, Sombano and seaward, Langira forests 77 3.4.2 Sombano, Langira and Kal 1 panel analysis – wood loss 77 3.4.3 The biodegrading organisms found on LWD 78 3.4.4 The volume of LWD in mangrove forests 87 3.4.5 Wood-degrading organism distribution and environmental variables – emersion, distance from the land and salinity 89 viii 3.4.6 The change between terrestrial and marine wood-degrading organisms 94 3.4.7 Teredinid panel-fragmentation 96 3.5 Discussion 97 Chapter 4 THE EFFECT OF TEREDINID TUNNELLING ON MANGROVE PROP- ROOTS 4.1 Introduction 110 4.2 Materials and methods 115 4.2.1 Root scar experiment 115 4.2.2 Root biscuit analysis 116 4.3 Data analysis 118 4.4 Results 118 4.4.1 Root scar analysis upon live roots 118 4.4.2 Root biscuit analysis 123 4.4.3 Atypical growth of lignified tissues 125 4.5 Discussion 127 Chapter 5 HABITAT CREATION FOR ANIMALS BY TEREDINIDS 5.1 Introduction 132 5.2 Materials and methods 134 ix 5.2.1 Assessing the sediment macro-infauna, root epifauna and LWD cryptic fauna 134 5.2.2 Assessing the effect of teredinid tunnelling on LWD in mangrove forests 135 5.2.3 Recruitment and succession of animals to drilled wooden blocks mimicking teredinid-attacked LWD 136 5.3 Data analysis 137 5.4 Results 138