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«Effect of high CO2 and low pH on benthic communities of the deep sea Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften - Dr. rer. ...»

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Effect of high CO2 and low pH on benthic

communities of the deep sea

Dissertation

zur Erlangung des Doktorgrades

der Naturwissenschaften

- Dr. rer. nat. dem Fachbereich 2 Biologie / Chemie

der Universität Bremen

vorgelegt von

Judith Neumann

Bremen, Juni 2012

Die vorliegende Arbeit wurde in der Zeit von Dezember 2008 bis Juni 2012 am MaxPlanck-Institut für Marine Mikrobiologie angefertigt.

1. Gutachter: Prof. Dr. Hans-Otto Pörtner

2. Gutachterin: Prof. Dr. Antje Boetius Tag des Promotionskolloquiums: 16. Juli 2012 Science cannot solve the ultimate mystery of nature. And that is because, in the last analysis, we ourselves are a part of the mystery that we are trying to solve. (Max Planck) Summary The increase of carbon dioxide (CO2) concentration in the atmosphere will intensify climate change although the ocean moderates climate change due to its considerable capacity to store large amounts of CO2. As a consequence the pH in seawater decreases, a process known as ocean acidification. Current state of the art of science and technology proposes mitigation strategies such as Carbon Capture and Storage (CCS) to reduce the amount of CO2 reaching the atmosphere. Storage locations are geological formations of the deep sea, where liquefied CO2 is sequestered. Risks to the environment, caused by CO2 leakage are not satisfactorily studied so far, although commercial projects are already running since 1996.

The deep sea is characterized a stable high pressure, low temperature regime and organisms have adapted to this extreme environment. Changes in environmental conditions as for leakage of CO2 will enhance mortality rates of organisms directly exposed to CO2. This may result in a shift in community structure and potentially the loss of functional groups that maintain ecosystem functioning. In this context, ”natural laboratories”, such as the Yonaguni Knoll IV hydrothermal system located in the Okinawa trough characterized by high CO2 fluxes, are appropriate sites to study responses of the deep-sea benthic community to high CO2 concentrations and thus low pH in situ. In the present study, the influence of these factors on the distribution, abundance and diversity of the deep-sea benthos was investigated, including all size classes of the benthic community from a reference site to low and high CO2 seepage sites.

Specific characteristics of the study site are presented in Chapter I, describing the geochemistry of the sediments and the distribution of microbial processes at the Yonaguni Knoll VI CO2 hydrothermal system. Measured rates of, e.g. sulfate reduction (SR) and anaerobic oxidation of methane (AOM) at the reference in contrast to CO2impacted sites, suggest that microbial communities are adapted to the geothermal and geochemical conditions. These processes were detectable at very low pH and were generally higher at the CO2-impacted vent site compared to the reference. However, microbial processes were limited to the upper 15 cm. This may be due to the high concentrations of dissolved CO2 which is a highly powerful solvent and the proportionally high concentration of carbonic acid (H2CO3) which might be toxic for microbial cells.

In Chapter II responses of the bacterial communities at three distinct sites with varying relative CO2 concentrations were explored. Distribution patterns indicated a shift in community structure from the background to the CO2 -impacted sites with a decrease of some bacterial types and a concurrent increase in particular other types that appear to be able to cope with the low pH. However, the overall abundance of bacteria increased with high CO2/low pH conditions, when these occurred in combination with hydrothermal fluids that may be utilized as an energy source by some bacteria.

Chapter III is concerned with metazoan meiofaunal and macrofaunal abundance, richness, and community distribution patterns in correlation with CO2 gradients. Both size classes showed responses to low pH, that are loss and reduction of some of the taxa groups (e.g. echinoderms and polychaetes) and an increase of others (nematodes). Apparently, the complex interplay of reduced predation and/or competition due to the decrease in macrofaunal echinoderms and polychaetes led to an increase in nematodes (meiofauna) at the intermediate impacted site despite low pH.

Zusammenfassung Der stetige Anstieg der Kohlendioxid-Konzentration (CO2) in der Atmoshpäre wird fortlaufend den Klimawandel verstärken, obwohl der Ozean einen bedeutenden Teil der CO2-Konzentration aufnimmt. Diese Funktion als CO2-Senke führt zu einer Verringerung des pH-Wertes, bekannt als Ozeanversauerung. Der aktuelle wissenschaftliche und technische Stand ermöglicht es, bereits große Mengen von CO2 in sogenannten Carbon Capture and Storage (CCS) Projekten abzuspeichern und damit die Menge an CO2 zu verringern, die in die Atmosphäre gelangt. CO2-Speicherstätten hierfür sind geologische Formationen in der Tiefsee, in denen das verflüssigte CO2 sequestriert wird. Obwohl es seit 1996 kommerziell durchgeführte CCS Projekte gibt, sind mögliche Risiken durch das Austreten des gespeicherten Kohlendioxids bisher nur ansatzweise untersucht worden. Die Tiefsee ist charakterisiert durch extremen Druck und niedrige Temperatur. Aufgrund dieses hohen Anpassungsgrades von Tiefseeorganismen an ihr Habitat könnten bei CO2-Leckagen erhöhte Mortalitätsraten auftreten. Dies hätte Veränderungen innerhalb der Gesellschaftstruktur zur Folge und würde einen Verlust von funktionellen Gruppen bedeuten, welche essentiell für die Funktionsfähigkeit des Ökosystems sind. „Natürliche Laboratorien“ wie z.B. das Yonaguni Knoll IV, ein hydrothermales CO2-Emissionsgebiet im Okinawa Graben, stellen dabei geeignete Gebiete dar, um den Einfluss erhöhter Kohlendioxid-Konzentrationen und einen geringen pH-Wert auf benthische Tiefseegemeinschaften in situ zu untersuchen. In der vorliegenden Arbeit wurde der Einfluss dieser Faktoren im Hinblick auf Verteilungsmuster, Abundanzen und Diversität aller Größenklassen der benthischen Tiefseegemeinschaft an drei unterschiedlichen Gebieten untersucht: eine Referenzstation, eine Station mit einer mittleren und eine Station mit einer hohen CO2-Konzentration.





Die Biogeochemie des Studiengebietes wird in Kapitel I beschrieben. Hierbei wurden die Geochemie des Sediments und die Verteilung der mikrobiellen Prozesse innerhalb des CO2-hydrothermalen-Systems Yonaguni Knoll IV untersucht. Anhand der untersuchten Prozesse von beispielsweise Sulfatreduktion (SR) und anaerober Methanoxidation (AOM) an der Referenz sowie den vergleichenden CO2-beeinflussten Gebieten wird vermutet, dass sich die mikrobiellen Gemeinschaften an die geothermalen und geochemischen Umweltparameter angepasst haben. Die mikrobiellen Prozesse waren, trotz des sehr niedrigen pH-Wertes, an den CO2-beinflussten Gebieten zu messen. Allerdings waren diese auf die ersten 15 cm des Sediments beschränkt. Mögliche Gründe hierfür wären die hohe Konzentration an gelöstem CO2, welches als starkes Lösungsmittel wirkt, als auch die im Verhältnis sehr hohe Konzentration an Kohlensäure (H2CO3), die eine toxische Wirkung auf die Mikroorganismen haben könnte.

In Kapitel II werden die Ergebnisse der Untersuchung der bakteriellen Gemeinschaft an den drei unterschiedlichen Gebieten dargestellt. Die bakteriellen Verteilungsmuster weisen auf eine Veränderung innerhalb der Gemeinschaftszusammensetzung des Referenzgebietes, im Vergleich zu den zwei stark CO2-beeinflussten Gebieten hin. Dies wird deutlich durch den Verlust einiger CO2sensitiven Bakterientypen, bei gleichzeitiger Zunahme acidotoleranter Bakterien.

Interessanterweise hatte der saure pH-Wert keinen Einfluss auf die Bakterienabundanz.

Anscheinend liefern die hydrothermalen Fluide Energie, die manche Bakterien für sich nutzen können.

Kapitel III befasst sich vergleichend mit Verteilungsmustern, Abundanzen und der Vielfalt der vielzelligen Meiofauna- und Makrofauna-Gemeinschaft entlang eines CO2-Gradienten. Diese Untersuchungen ergaben, dass die Meiofaunagesellschaft weniger beeinflusst wurde als die Makrofaunagesellschaft. Dennoch wurden beide Gemeinschaften durch die hohe Konzentration an CO2 und dem daraus resultierenden sauren pH-Wert beeinträchtigt. Möglicherweise führten geringerer Fraßdruck und/oder Konkurrenz im gemäßigt CO2-beeinflussten Gebiet zu einer erhöhten Anzahl der Meiofauna, insbesondere der Nematoden.

Table of Contents

1. Introduction

1.1 Climate Change and Ocean Acidification

1.1.1 Effects of Ocean Acidification on marine ecosystem

1.1.2 Carbon Capture and Storage (CCS)

1.2 Life at the extremes

1.2.1 Organisms in acidic environments

1.2.2 Adaptation strategies to acidic environments

1.2.3 Previous acidification experiments and mesocosm studies

1.3 Natural laboratories to study the risk of CCS and consequences of ocean acidification........ 30 1.3.1 Ecosystem responses and community ecology

1.3.2 Resistance, resilience or death - responses to acidification and synergistic effects

1.4 Objectives

1.5 Material and Methods

1.5.1 The setting of the investigated “natural laboratory” – Yonaguni Knoll IV hydrothermal vent system

1.5.2 Methods and tools used for the identification of faunal and bacterial diversity...... 41 1.5.2.1 Automated Ribosomal Intergenic Spacer Analysis (ARISA)

1.5.2.2 454 Massively Parallel Tag Sequencing

1.5.2.3 Extraction and identification of benthic meiofauna and macrofauna........... 44 1.5.2.4 Procedure for permanent nematode slides

1.6 Publication outline

2. Thesis chapters

Chapter I Life in extreme environments: Biogeochemical processes in CO2 vented deep-sea sediments

Chapter II Effects of subsurface CO2 leakage on deep-sea bacterial communities of the Yonaguni Knoll IV hydrothermal sediments (Okinawa Trough, 1350 m)................ 80 Chapter III Impact of high CO2 leakage on macrobenthic and meiobenthic community structure of the Yonaguni Knoll IV hydrothermal system (Okinawa Trough, 1350 m)

3. Discussion & Perspectives

3.1 Naturally CO2-influenced sediments may provide information on the impact of CCS leakage on benthic communities

3.2 Bacterial communities influenced by high CO2 and low pH

3.3 Impact of high CO2 and low pH on the benthic faunal assemblage

3.4 Responses on ecosystem level

3.5 Perspectives for monitoring

Bibliography

Acknowledgements

Posters and Oral Presentations

Cruise Participation

1.

Introduction

1.1 Climate Change and Ocean Acidification The climate system is a complex, interactive system comprising the atmosphere, hydrosphere, geosphere, and biosphere (Treut et al. 2007). Modification of the composition of atmospheric gases through e.g. the increase of carbon dioxide (CO2) emissions led to alterations and thus to climate change (Fig. 1). In recent years, climate change has been synonymously used to describe the latter factor – human-induced changes on the level of global warming - and has become a term describing postindustrial warming of the Earth’s atmosphere and oceans due to the anthropogenic production and release of greenhouse gases to the atmosphere, such as carbon dioxide (CO2) (c.f. United Nations Framework Convention on Climate Change, UNFCC).

Figure 1 Schematic overview of the components of the climate system and its dynamic processes and interactions (adapted from IPCC 2007).

Carbon dioxide is, besides water vapor, methane, and nitrous oxide, a so called greenhouse gas that absorbs and emits solar radiation within the thermal infrared range, causing an elevation of the average surface temperature and thus climate change. Since the beginning of high-accuracy measurements of atmospheric CO2 concentrations in 1958 by Charles David Keeling on Mauna Loa in Hawaii, time series of the composition of the atmosphere have been documented and, hence, constituted modern research on climate change (Treut et al. 2007). In order to evaluate atmospheric gas composition of the past and to make predictions for the future, enclosed air bubbles of ice cores dating back 10,000 years before present, which had been retrieved from Greenland and Antarctica, were analyzed. Studies on these ice cores revealed that CO2 concentrations had been stable within a range of 280 ± 20 ppm (parts per million) up to the year 1750 (Indermühle et al. 1999). During industrialization, concentrations of the greenhouse gas rose roughly exponentially to 367 ppm in 1999 (Neftel et al. 1985; Etheridge et al. 1996;

IPCC 2001) and to 397 ppm in the year 2005 (Treut et al. 2007). Other major greenhouse gases such as methane (CH4) and nitrous oxide (N2O) increased to a minor extent (1% and 0.25% yr-1, respectively) (Graedel and McRae 1980; Fraser et al. 1981; Weiss 1981;

Blake et al. 1982; Khalil and Rasmussen 1988).

While the incoming sunlight and outgoing infrared radiation determine the global climate, the increasing concentration of CO2 as the most influencing greenhouse gas traps the incoming radiation, thereby heating up the Earth’s surface (Fig. 2). An additional effect of rising concentrations of CO2 in the atmosphere is the acidification of ocean waters, with yet largely unknown effects on marine ecosystems. Both, climate change (i.e. global warming) and ocean acidification are phenomena that have their origin in increasing concentrations of greenhouse gases, especially rising CO2 levels.

Figure 2 “Keeling Curve” showing the history of atmospheric CO2 concentrations measured at Mauna Loa, Hawaii. The annual fluctuation of CO2 is caused by a seasonal variation, indicating atmospheric signal of a sink, which is the massive uptake by terrestrial and oceanic plants during summer in the northern hemisphere (inset figure). Atmospheric CO2 concentrations have reached more than 380 ppmv (parts per million per volume) in the year 2010 (www.wikipedia.org). Recently, values of 397 ppmv have been recorded.



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