Environmental Change Impacts on Marine Calcifiers: Spatial and Temporal Biomineralisation Patterns in Mytilid Bivalves Luca Telesca Gonville and Caius College University of Cambridge This dissertation in submitted for the degree of Doctor of Philosophy Department of Earth Sciences & British Antarctic Survey September 2018 Environmental Change Impacts on Marine Calcifiers: Spatial and Temporal Biomineralisation Patterns in Mytilid Bivalves Luca Telesca Abstract Environmental change is a major threat to marine ecosystems worldwide. Understanding the key biological processes and environmental factors mediating spatial and temporal species’ responses to habitat alterations underpins our ability to forecast impacts on marine ecosystems under any range of scenarios. This is especially important for calcifying species, many of which have both a high climate sensitivity and disproportionately strong ecological impacts in shaping marine communities. Although geographic patterns of calcifiers’ sensitivity to environmental changes are defined by interacting multiple abiotic and biotic stressors, local adaptation, and acclimation, knowledge on species’ responses to disturbance is derived largely from short- and medium-term laboratory and field experiments. Therefore, little is known about the biological mechanisms and key drivers in natural environments that shape regional differences and long-term variations in species vulnerability to global changes. In this thesis, I examined natural variations in shell characteristics, both morphology and biomineralisation, under heterogeneous environmental conditions i) across large geographical scales, spanning a 30° latitudinal range (3,334 km), and ii) over historical times, using museum collections (archival specimens from 1904 to 2016 at a single location), in mussels of the genus Mytilus. The aim was to observe whether plasticity in calcareous shell morphology, production, and composition mediates spatial and temporal patterns of resistance to climate change in these critical foundation species. For the morphological analyses, the combined use of new statistical methods and multiple study systems at various geographical scales allowed the uncoupling of the contribution of development, genetic status, and environmental factors to shell morphology. I found salinity had the strongest effect on the latitudinal patterns of Mytilus shape. Temperature and food supply, however, were the main predictor of mussel shape heterogeneity. My results suggest the potential of shell shape plasticity in Mytilus as a powerful indicator of rapid environmental changes. I found decreasing shell calcification towards high latitudes. Salinity was the best predictor of regional differences in shell deposition, and its mineral and organic composition. In polar, low-salinity environments, the production of calcite and organic shell layers was increased, while aragonite deposition was enhanced under temperate, higher-salinity regimes. Interacting strong effects of decreasing salinity and increasing food availability on compositional shell plasticity predict the deposition of a thicker external organic layer (periostracum) at high latitudes under forecasted future i conditions. This response potential of Mytilus shell suggests an enhanced protection of temperate mussels from predators and a strong capacity for increased resistance of polar and subpolar individuals to dissolving water conditions. Analyses of museum specimens indicated increasing shell calcification during the last century. Deposition of individual shell layers was more closely related to temporal changes in the variability of key environmental drivers than to alterations of mean habitat conditions. Calcitic layer and periostracum showed marked responses to alterations of biotic conditions, suggesting the potential of mussels to trade-off between the deposition of calcareous and organic layers as a compensatory response to strategy-specific predation pressure. These changes in biomineralisation indicated a marked resistance to environmental change over the last century in a species predicted to be vulnerable, and how locally heterogeneous environments and predation levels can have a stronger effect on Mytilus responses than global environmental trends. My work illustrates that biological mechanisms and local conditions, driving plastic responses to the spatial and temporal structure of multiple abiotic and biotic stressors, can define geographic and temporal patterns of unforeseen species resistance to global environmental change. ii A Vito e Carlo My mama always said “Life was like a box of chocolates. You never know what you're going to get.” Forrest Gump (1994) Acknowledgment I would like to give a big thank you to my supervisors, Dr Elizabeth Harper and Prof. Lloyd Peck, for their kind availability and continual support throughout my PhD, and for being inspiring scientists of great integrity. Without their guidance and advice, this PhD would have been harder and less feasible. I would like to thank the members and staff of the Department of Earth Sciences and the British Antarctic Survey for the friendly and collaborative environment. A special thanks to Emma, Javier, Emily, and Ben at the Dept. of Earth Sciences and to the friends at the British Antarctic Survey Teja, Leyre, and Vicky for their advices during different stages of my research. I would also like to thank Dr Trystan Sanders, Dr Kati Michalek, Dr Jakob Thyrring, and Dr Mikael K Sejr for useful and thorough discussions, and for help with obtaining materials for this study. I am also grateful to Guy Hillyard, Dr Iris Buisman, and Dr Giulio Lampronti for their technical assistance. Thanks also to my academic friends Prof. Simon Conway Morris and Dr Alistair Crame for their guidance and monitoring of my research progresses. I am grateful to Dr Thierry Backeljau at the Royal Belgian Institute of Natural Sciences for his help and for making available invaluable archival collections for this PhD. Special thanks also to the curator Yves Samyn, and to James and Yan. My greatest gratitude goes to Mamma, Papà, nonno Carlo, nonna Augusta, and the rest of my family for everything they do for me and for always supporting my dreams. I am also very thankful to my lifetime friends back home and here in the U.K., particularly Marco & Paolo, Lorenzo, Mayo, Alfio, Basco, Sibbo, and Michele for their encouragement and for being always available. A sweet special thanks to Roberta for her patience and being there every day. I would like to thank you also all the nice people I have met from the College for always feel me welcome and included. Special thanks also to Prof. Marco Oliverio and Dr Alessandro Criscoli at the University of Rome “La Sapienza” who encouraged me into this academic journey abroad. Finally, I would like to thank the Marie Curie CACHE International Training Network of the European Union Seventh Framework Programme for the generous funding for this PhD under the grant agreement n° 605051. A special thanks to the CACHE fellows, Kati, Trystan, Teja, Kirti, David, Michele, Alex, Nadege, Carlos, and Phoebe, and to the administrators, particularly Dr Melody Clark and Rita Pereira for their commitment and help. iii Declaration This dissertation is the result of my own work and includes nothing which is the outcome of work done in collaboration except where specifically indicated in the text. It is not substantially the same as any that I have submitted, or is being concurrently submitted, for a degree or other qualification at the University of Cambridge or any other. I further state that no substantial part of my dissertation has already been submitted, or is being concurrently submitted, for any such degree or other qualification at the University of Cambridge or any other University or similar institution. It does not exceed the prescribed page limit specified by the Earth Sciences and Geography Degree Committee. Luca Telesca September 2018 iv Table of Contents Abstract ...................................................................................................................................... i Acknowledgment .................................................................................................................... iii Declaration............................................................................................................................... iv Table of Contents ..................................................................................................................... v List of Figures .......................................................................................................................... ix List of Tables ........................................................................................................................... xi 1 Introduction ...................................................................................................................... 1 1.1 Environmental change............................................................................................................. 1 1.1.1 Physical and chemical changes ................................................................................... 2 1.1.2 Biological and ecosystem effects of environmental change ....................................... 5 1.1.3 Multiple drivers .......................................................................................................... 5 1.1.4 Environmental change study approaches ...................................................................