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University of Southampton Research Repository Eprints Soton University of Southampton Research Repository ePrints Soton Copyright © and Moral Rights for this thesis are retained by the author and/or other copyright owners. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder/s. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holders. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given e.g. AUTHOR (year of submission) "Full thesis title", University of Southampton, name of the University School or Department, PhD Thesis, pagination http://eprints.soton.ac.uk UNIVERSITY OF SOUTHAMPTON FACULTY OF ENGINEERING, SCIENCE AND MATHEMATICS National Oceanography Centre School of Ocean and Earth Science Community and trophic responses of benthic Foraminifera to oxygen gradients and organic enrichment by Kate E. Larkin Thesis for the degree of Doctor of Philosophy July 2006 Graduate School of the National Oceanography Centre This PhD dissertation by Kate E. Larkin has been produced under the supervision of the following persons: Supervisors: Prof. Andrew J. Gooday Dr. Brian J. Bett Chair of Advisory Panel: Prof. Paul A. Tyler ‘As objects of beauty they (Foraminifera) arrest the attention of even the casual observer by the delicacy of their structure as well as the symmetry and variety of their forms’ (JM Flint 1899). UNIVERSITY OF SOUTHAMPTON ABSTRACT FACULTY OF ENGINEERING, SCIENCE & MATHEMATICS SCHOOL OF OCEAN & EARTH SCIENCES Doctor of Philosophy COMMUNITY AND TROPHIC RESPONSES OF BENTHIC FORAMINIFERA TO OXYGEN CONCENTRATION AND ORGANIC ENRICHMENT by Kate E. Larkin Global warming and eutrophication are driving an expansion of hypoxia in the World Ocean. This will favour organisms, such as Foraminifera (testate protists), that tolerate low-oxygen conditions and may lead to an overall decline in marine biodiversity. With this in mind, community and trophic responses of benthic Foraminifera were investigated at two contrasting sites in the upper boundary (140 m water depth; bottom-water oxygen concentrations = 2.05 mll-1 during the spring intermonsoon and 0.11 mll-1 during the SW monsoon) and the core (300 m water depth; bottom-water oxygen concentration consistently ~ 0.11 mll-1) of an intense, natural, mid-water oxygen minimum zone (OMZ) on the Pakistan Margin, NE Arabian Sea. Live macrofaunal (>300 µm fraction) Foraminifera (including soft- walled species) and metazoans were examined at each site during the 2003 spring intermonsoon (April) and SW monsoon (October) seasons (4 replicate multicores/site/season, 25.5cm2 surface area, 0-5 cm depth). Wet-sorting revealed a low diversity assemblage dominated (> 60 %) by calcareous Foraminifera at both sites. A total of 36 species was recognised and diversity was not greatly affected by water depth or season. At both sites, >86 % of Foraminifera were restricted to the upper 0-1 cm layer of sediment and the Average Living Depth (ALD) decreased from the spring intermonsoon to the SW monsoon (140 m, ALD5 = 0.41 to 0.33; 300 m, ALD5 = 0.65 to 0.44). Foraminifera increased in mean abundance from 124 to 153 individuals per 10 cm2 from the spring intermonsoon to the SW monsoon at 140 m and from 86 to 122 individuals per 10 cm2 at 300 m. The calcareous species Uvigerina ex. gr. semiornata dominated communities and increased in mean abundance from 54 to 118 individuals (140 m) and from 41 to 69 individuals (300 m) per 10 cm2 following the SW monsoon. At 140 m, Foraminifera were 3.6 times more abundant than metazoans during the spring intermonsoon, rising to 13.9 times during the SW monsoon. The corresponding proportions at 300 m, where metazoans were rare, were 12.4 and 14.5. Fatty acid biomarkers suggest that foraminiferal diets vary between species. The calcareous species U. ex. gr. semiornata, Bolivina aff. dilatata and Globobulimina cf. G. pyrula selectively ingested phytodetrital material, whereas the agglutinated species, Ammodiscus aff. cretaceus, Bathysiphon sp. nov. 1, and Reophax dentaliniformis favoured bacteria. Moreover, U. ex. gr. semiornata, rapidly ingested (within two days) 13C-labelled diatoms in shipboard laboratory and in situ pulse-chase experiments at the 140-m site following the SW monsoon. This enabled the uptake and processing of organic matter (OM) to be tracked in the foraminiferal cell into individual fatty acids, using Gas Chromatography - Mass Spectrometry (selective ion scan). These results suggest that calcareous Foraminifera, in particular U. ex. gr. semiornata, play a central role in OM cycling on the sea-floor in the upper part of the Pakistan margin OMZ. Declaration of Authorship I, Kate Elisabeth Larkin, declare that the thesis entitled Community and trophic responses of benthic Foraminifera to oxygen gradients and organic enrichment and the work presented in it are my own. I confirm that: • This work was done wholly or mainly while in candidature for a research degree at this University; • Where any part of this thesis has previously been submitted for a degree or any other qualification at this University or any other institution, this has been clearly stated; • Where I have consulted the published work of others, this is always clearly attributed; • Where I have quoted from the work of others, the source is always given. With the exception of such quotations, this thesis is entirely my own work; • I have acknowledged all main sources of help; • Where the thesis is based on work done by myself jointly with others, I have made clear exactly what was done by others and what I have contributed myself; • None of this work has been published before submission. Signed: Kate E Larkin Date: 30/7/2006 Acknowledgments Firstly I would like to thank the NERC for providing the funding to support my research (NER/A/S/2000/01280). My sincere thanks go to my supervisor Prof. Andrew Gooday for his contagious enthusiasm for Foraminifera, his enlightening discussions, and his unrelenting support. I would also like to thank Dr. David Pond at the British Antarctic Survey for welcoming me into the laboratories at BAS and for helpful advice concerning the lipid analysis and Dr. Brian Bett for his inspiring leadership at sea and for helpful advice with statistics. I would like to acknowledge Dr. Mike Bell and James Dick at Stirling University for their help and expertise with the GC-MS and Prof. Lisa Levin at SCRIPPS, USA, for welcoming me into her lab and home and for her vision, drive and strong American coffee at sea! Many thanks also to Prof. Hiroshi Kitazato, Dr. Hidetaka Nomaki and Dr. Toyofuku for their collaboration and hospitality during my stay at JAMSTEC, Japan, and for useful discussions on Foraminifera. Thanks to all the scientists, crew and officers involved in all of the cruises on RRS Charles Darwin in 2003 to the Pakistan margin and especially to Xana, Rachel and Christine for making my time at sea very enjoyable and an amazing experience that I will never forget. I would also like to thank my friends and colleagues at the National Oceanography Centre, including Prof. Paul Tyler who first welcomed me into the world of oceanography, and to the George Deacon Department and the DEEPSEAS team. Thanks to Ross for musical jamming sessions keeping me sane and to Jacqui, Steph and Chris for two fun years as the ‘Cromwell girls’. Thanks to Haris, Thanos, Yiannis, Irene and my ‘big sister’ Aggie for their friendship. Steph, Sally and Vanessa – thank you for keeping me smiling with innocent outsider views of deep-sea research like ‘Wow! Four months in the Arabian Sea – what a holiday! How big was the swimming pool on board?!’ My deepest thanks go to my family, Mum, Dad, James and Sally, for believing in me no matter what and for R&R when I needed it most. I am also indebted to Uncle John and Linda for hosting me so wholeheartedly during my many trips to BAS. And lastly, but by no means least, my warmest thanks go to Corrado, who has totally supported me throughout. His energy and optimism have kept me sane and smiling despite the many obstacles I have encountered, especially near the end of this journey. List of Contents 1 Introduction 1 1.1 Global oceanic regime shifts: a cause for concern 1 1.2 Marine benthic hypoxia: a growing phenomenon 2 1.3 Benthic Foraminifera 3 1.4 Aims and hypotheses of this study 4 2 Environmental influences on deep-sea Foraminifera 5 2.1 Deep-sea organisms and environmental gradients 5 2.2 Low Oxygen Environments 6 2.2.1 Terminology 6 2.2.2 Oxygen Minimum Zones (OMZs) 6 2.2.3 Benthic faunas in oxygen-deficient environments 9 2.2.4 Benthic Foraminifera in oxygen-deficient environments 11 2.2.4.1 Regional patterns 11 2.2.4.2 Controls within the sediment profile 14 2.3 Organic matter availability in the deep sea 16 2.3.1 Benthic-pelagic coupling 16 2.3.2 The response of benthic Foraminifera to organic matter 17 flux 2.4 Nutrition of benthic Foraminifera 19 2.4.1 Food sources and feeding preferences 19 2.4.2 Foraminiferal feeding mechanisms 22 2.4.3 The use of fatty acids as biomarkers 24 3 The study area in the Arabian Sea 29 3.1 The Arabian Sea OMZ 29 3.1.1 Monsoonal Winds and primary productivity 29 3.1.2 Development of the OMZ 31 3.2 The Pakistan Margin OMZ during 2003 33 3.2.1 General trends 36 3.2.1.1 The pelagic environment 36 3.2.1.2 Evidence
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