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Global Change Stress on Symbiont- Bearing Benthic Foraminifera

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Global Change Stress on Symbiont- Bearing Benthic Foraminifera GLOBAL CHANGE STRESS ON SYMBIONT- BEARING BENTHIC FORAMINIFERA Dissertation zur Erlangung des Doktorgrades in den Naturwissenschaften (Dr. rer. nat.) vorgelegt von Christiane Schmidt Bremen, Januar 2015 GLOBAL CHANGE STRESS ON SYMBIONT- BEARING BENTHIC FORAMINIFERA Dissertation zur Erlangung des Doktorgrades in den Naturwissenschaften (Dr. rer. nat.) im Fachbereich Geowissenschaften der Universität Bremen vorgelegt von Christiane Schmidt Bremen, Januar 2015 1. Gutachter: Professor Dr. Michal Kucera, Mikropaläontologie, Zentrum für Marine Umweltwissenschaften, MARUM, Universität Bremen 2. Gutachter: Professor Dr. Kai Bischof, Marine Botanik, Universität Bremen Datum der Verteidigung: 18. März 2015 1 Contents Zusammenfassung................................................................................................................ 5 Summary............................................................................................................................... 9 1. Introduction ...................................................................................................................11 1.1. The ecology of symbiont-bearing benthic foraminifera............................................11 1.2. The Identity and diversity of symbionts in benthic foraminifera ...............................15 1.3. Bleaching in symbiont-bearing foraminifera............................................................17 1.4. Combined effects of global change ........................................................................20 1.5. Culturing of symbiont-bearing foraminifera .............................................................22 1.6. Aims and interdisciplinary research context............................................................25 1.7. Working hypotheses...............................................................................................26 1.8. Outline of the thesis................................................................................................30 1.9. References.............................................................................................................32 2. Publication I: Combined effects of warming and ocean acidification on coral reef foraminifera Marginopora vertebralis and Heterostegina depressa Coral Reefs ...................43 2.1. Abstract..................................................................................................................45 2.2. Introduction ............................................................................................................45 2.3. Material and Methods.............................................................................................46 2.3.1. Species selection and sample collection.............................................................46 2.3.2. Experimental approach mimicking ‘natural’ conditions ........................................47 2.3.3. Experimental design and carbonate system parameters.....................................47 2.3.4. Survivorship and growth .....................................................................................48 2.3.5. Photobiology, oxygen consumption and chlorophyll a concentration...................48 2.3.6. Experimental light levels .....................................................................................48 2.3.7. Data analysis ......................................................................................................49 2.4. Results...................................................................................................................50 2.5. Discussion..............................................................................................................52 2.5.1. Photosynthesis, respiration, and chlorophyll a content........................................52 2.5.2. Survivorship and growth .....................................................................................53 1 2.5.3. Combined effects of key global change stressors ...............................................55 2.6. References.............................................................................................................56 3. Publication II: Recent invasion of the symbiont-bearing foraminifera Pararotalia into the Eastern Mediterranean facilitated by the ongoing warming trend..........................................59 3.1. Abstract..................................................................................................................61 3.2. Introduction ............................................................................................................62 3.3. Material and Methods.............................................................................................64 3.3.1. Sample collection and maintenance of cultures ..................................................64 3.3.2. Taxonomic identification and habitat...................................................................65 3.3.3. Symbiont culturing and preparation for SEM microscopy ....................................66 3.3.4. PAM Fluorometry................................................................................................67 3.3.5. Reproduction and offspring experiments.............................................................68 3.3.6. Growth measurements........................................................................................69 3.3.7. DNA extraction, amplification, cloning and sequencing.......................................70 3.3.8. Sequence analysis..............................................................................................71 3.3.9. Computation of the habitat model .......................................................................71 3.4. Results and Discussion ..........................................................................................74 3.4.1. The identity of the invasive species and its current distribution ...........................74 3.4.2. Characterization of diatom endosymbionts and their photochemistry..................77 3.4.3. Reproduction, growth and temperature sensitivity of asexual offspring ...............82 3.4.4. Modelling the present and future distribution of the species................................87 3.5. Conclusions............................................................................................................90 3.6. Acknowledgments ..................................................................................................91 3.7. References.............................................................................................................92 3.8. Supporting Information .........................................................................................100 4. Publication III: Extreme heat tolerance of a foraminifera–diatom photo-symbiosis.......109 4.1. Abstract................................................................................................................111 4.2. Introduction ..........................................................................................................112 4.3. Methods ...............................................................................................................114 4.3.1. Sample collection..............................................................................................114 2 4.3.2. Experimental design and sea water parameters ...............................................115 4.3.3. Photochemistry measurements.........................................................................118 4.3.4. Survivorship & Growth measurements..............................................................118 4.3.5. Statistics ...........................................................................................................119 4.4. Results.................................................................................................................119 4.4.1. Seawater data ..................................................................................................121 4.4.2. Symbiont data: Photochemistry ........................................................................121 4.4.3. Holobiont data: Survivorship & Growth .............................................................124 4.5. Discussion............................................................................................................127 4.6. References...........................................................................................................134 4.7. Supporting Information .........................................................................................141 5. Concluding remarks and perspectives............................................................................144 5.1. General discussion and conclusions ........................................................................144 5.2. Implications of the results: the future of symbiont-bearing foraminifera ....................153 5.3. References ..............................................................................................................156 6. Acknowledgements ........................................................................................................161 7. Schriftliche Erklärung......................................................................................................165 3 4 Zusammenfassung Symbionten-tragende benthische Foraminiferen sind wichtige Kalzit Produzenten in den Weltmeeren, welche zu einem Drittel an der Produktion des Karbonat-Sediments der Korallenriffgemeinschaften
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