Queen Mary University of London The indirect impacts of ecosystem engineering by invasive crayfish Guillermo Eduardo Willis-Jones Tambo Submitted in partial fulfillment of the requirements of the Degree of Doctor of Philosophy 1 I, Guillermo Eduardo Willis-Jones Tambo, confirm that the research included within this thesis is my own work or that where it has been carried out in collaboration with, or supported by others, that this is duly acknowledged below and my contribution indicated. Previously published material is also acknowledged below. I attest that I have exercised reasonable care to ensure that the work is original, and does not to the best of my knowledge break any UK law, infringe any third party’s copyright or other Intellectual Property Right, or contain any confidential material. I accept that the College has the right to use plagiarism detection software to check the electronic version of the thesis. I confirm that this thesis has not been previously submitted for the award of a degree by this or any other university. The copyright of this thesis rests with the author and no quotation from it or information derived from it may be published without the prior written consent of the author. Signature: Date: Details of collaboration and publications: I have co authored a book chapter on crayfish ecology: Willis-Jones E., Jackson M.C. & Grey J. (2016) Environmental Drivers for Population Success: Population Biology, Population and Community Dynamics. In: Biology and Ecology of Crayfish. (Eds M. Longshaw & P. Stebbing), pp. 251–286. CRC Press. 2 Abstract Bioturbation by invasive crayfish can significantly alter sediment properties and its transport in invaded water bodies; however, the indirect impacts of this on ecosystem functioning are poorly understood. In this thesis I present data from mesocosm and field manipulation experiments used to assess the effect of bioturbation by three widely distributed invasive crayfish species (Procambarus clarkii, Pacifastacus leniusculus and Astacus leptodactylus) on a variety of ecosystem properties across seasons. In the mesocosm experiments, P. clarkii caused significantly more bioturbation than the other species, although increased bioturbation by all species in the spring and/or summer was associated with: reduced dissolved oxygen concentrations in near-surface water, indicating a large increase in oxygen demand by the water column; increased methane oxidation potential within the water (MOPwat), indicating the re- suspension of methane oxidising bacteria (MOB) along with the sediment; and a shift in zooplankton community structure towards dominance by large cladoceran species. Stable 13 isotope analysis of the zooplankton showed a strong relationship between δ C and MOPwat, suggesting that bioturbation increases MOB consumption. Given the importance of zooplankton as a trophic link to the higher food web, crayfish bioturbation may increase the importance of methane derived (chemosynthetic) carbon in invaded ecosystems. Temperature was identified as the key driver of seasonal variations in crayfish bioturbation intensity through laboratory mesocosm experiments, enabling estimation of the full annual pattern of bioturbation intensity for each species. The optimal temperature for P. clarkii was much higher than for the other species meaning that its bioturbation impacts exhibited large seasonal fluctuations whilst P. leniusculus and A. leptodactylus maintained a lower but more consistent level. Field manipulation experiments of enclosed sections of Chalgrove Brook, Oxfordshire, found significant bioturbation activity by P. leniusculus in early autumn; however, the increase in turbidity was too small to detect other effects observed in the mesocosm experiments. 3 Acknowledgements Firstly I would like to thank my supervisors Professors Jon Grey and Mark Trimmer for all their help and support over the course of my PhD. Their advice and enthusiasm have been indispensible. I also wish to thank the other members of the Grey and Trimmer labs for their advice and help. Particular thanks go to Felicity Shelley and Paul Fletcher for their invaluable practical and technical support. I am also extremely grateful to my friends and family outside of QMUL; particularly my parents and sister who have always been ready with interest, support and encouragement. Importantly, I must thank Clare, your support and patience has been invaluable; I could not have done it without you! I would like to thank Bob Campbell for giving me access to his property and allowing me to conduct experiments on his section of the Chalgrove Brook. In addition, I would like to thank Adrian Brooker at the City of London Corporation for giving me access to the Hampstead heath ponds to catch red swamp and Turkish crayfish and Jamie Godson of Lee Valley Park Authority for providing me with virile crayfish. This work was supported by a Natural Environment Research Council CASE studentship with the Environment Agency. 4 Contents List of Figures ............................................................................................................. 8 List of Tables .............................................................................................................. 9 Chapter 1: Introduction ......................................................................................... 10 1.1 Ecosystem Engineering and Bioturbation ......................................................................... 10 1.2 Crayfish as ecosystem engineers ...................................................................................... 12 1.3 Potential ramifications of crayfish bioturbation ............................................................... 13 1.4 Differences in bioturbation activity between crayfish species ......................................... 18 1.5 Experimental approach ..................................................................................................... 19 1.6 Mesocosms as the study system ...................................................................................... 19 1.7 Structural outline of the thesis ......................................................................................... 21 Chapter 2: Indirect impacts of Procambarus clarkii bioturbation on ecosystem processes: a seasonal mesocosm study ..................................................................... 22 2.1 Introduction ...................................................................................................................... 22 2.2 Methods ............................................................................................................................ 24 2.2.1 Experimental setup ................................................................................................ 24 2.2.2 Turbidity ................................................................................................................. 25 2.2.3 Dissolved Oxygen ................................................................................................... 25 2.2.4 Dissolved Methane ................................................................................................ 26 2.2.5 Methanogenic & Methane Oxidation Potentials ................................................... 26 2.2.6 Chlorophyll a .......................................................................................................... 27 2.2.7 Nutrients ................................................................................................................ 27 2.2.8 Conductivity ........................................................................................................... 27 2.2.9 Zooplankton ........................................................................................................... 28 2.2.10 Data Analysis .......................................................................................................... 28 2.3 Results ............................................................................................................................... 29 2.3.1 Turbidity ................................................................................................................. 29 5 2.3.2 Dissolved Oxygen ................................................................................................... 30 2.3.3 Chlorophyll a .......................................................................................................... 33 2.3.4 Nutrients and conductivity .................................................................................... 33 2.3.5 Methanogenesis, dissolved methane, and methane oxidation ............................. 33 2.3.6 Zooplankton δ13C ................................................................................................... 35 2.3.7 Zooplankton community structure ........................................................................ 39 2.4 Discussion ......................................................................................................................... 39 Chapter 3: Comparison of bioturbation impacts with other crayfish species .......... 46 3.1 Introduction ...................................................................................................................... 46 3.2 Methods ............................................................................................................................ 48 3.2.1 Experimental design ..............................................................................................