Krill in the Arctic and the Atlantic – Climatic Variability and Adaptive Capacity – Dissertation with the Aim of Achieving a Doctoral Degree in Natural Science – Dr. rer. nat. – at the Faculty of Mathematics, Informatics and Natural Sciences Department of Biology of the University of Hamburg submitted by Lara Kim Hünerlage M.Sc. Marine Biology B.Sc. Environmental Science Hamburg 2015 This cumulative dissertation corresponds to the exam copy (submitted November 11th, 2014). The detailed content of the single publications may have changed during the review processes. Please contact the author for citation purposes. Day of oral defence: 20th of February, 2015 The following evaluators recommend the acceptance of the dissertation: 1. Evaluator Prof. Dr. Friedrich Buchholz Institut für Hydrobiologie und Fischereiwissenschaft, Fakultät für Mathematik, Informatik und Naturwissenschaften, Universität Hamburg; Alfred-Wegner-Institut Helmholtz Zentrum für Polar- und Meeresforschung, Funktionelle Ökologie, Bremerhaven 2. Evaluator Prof. Dr. Myron Peck Institut für Hydrobiologie und Fischereiwissenschaft, Fakultät für Mathematik, Informatik und Naturwissenschaften, Universität Hamburg 3. Evaluator Prof. Dr. Ulrich Bathmann Leibniz-Institut für Ostseeforschung Warnemünde; Interdisziplinäre Fakultät für Maritime Systeme, Universität Rostock IN MEMORY OF MY FATHER, GERD HÜNERLAGE DEDICATED TO MY FAMILY PREFACE This cumulative dissertation summarizes the research findings of my PhD project which was conducted from September 2011 to October 2014. Primarily, it was part of the French-German AWIPEV project KOP 124 (RIS ID 3451) but was also supported by the African-German GENUS-I project (BMBF 03F0497F) and benefitted from the French KREVET project (J.Y. Toullec and K. Cascella; Station Biologique de Roscoff). The main focus of the work was to compare the metabolic performance, biochemical composition and adaptive capacity of six krill species, from the Atlantic (the Benguela Current system and the Northern Atlantic) and the Arctic (the high Arctic Kongsfjord), in order to estimate these species’ regional persistence under aspects of climate variability. The thesis includes a general introduction (Chapter 1) and a synoptic discussion (Chapter 7) and is composed of five publications (Chapters 2 – 6) presented as manuscripts as listed below. The general concept of the PhD project was developed by myself with advice from my supervisor Prof. Dr. Friedrich Buchholz. CHAPTER 2 Huenerlage K and Buchholz F Krill of the northern Benguela Current and the Angola-Benguela frontal zone compared: physiological performance and short-term starvation in Euphausia hanseni The study concept was developed by myself and Dr. F. Buchholz. The samples were collected by both authors during a research cruise on-board the German R/V Maria S. Merian in late austral summer 2011. The experiments, analytical work and data evaluation was conducted by me, partly in the frame work of my Master’s thesis. I wrote the manuscript with contributions from Dr. F. Buchholz. The paper was published in the Journal of Plankton Research (2013) 35(2): 337-351. i Preface CHAPTER 3 Huenerlage K, Graeve M, Buchholz C and Buchholz F The other krill: overwintering physiology of adult Thysanoessa inermis (Euphausiacea) from the high Arctic Kongsfjord The scientific concept of the study was developed by myself with advice from Dr. F. Buchholz. T. inermis specimens were sampled by us on-board the Kings Bay AS workboat MS Teisten in summer 2012. I developed the experimental set-up. The experiments were conducted by myself with help from Dr. F. Buchholz. All analyses and data evaluation were performed by me. I wrote the manuscript with contributions from all authors. This paper is in the review process in Aquatic Biology (27.10.2014; manuscript number: AB201408030). CHAPTER 4 Huenerlage K, Graeve M, Buchholz F Lipid composition and trophic relationships of krill species in a high Arctic fjord The concept of this paper was developed by myself and discussed with Dr. M. Graeve. The samples from the Benguela Current system and the Kongsfjord were collected by myself and Dr. F. Buchholz. Krill samples from the Iceland Basin were taken by Dr. F. Buchholz. All analytical analyses and data evaluation were performed by me. The fatty acid and lipid class analyses were advised by Dr. M. Graeve. I wrote the manuscript with scientific contributions of both authors. This paper was published online in Polar Biology S.I. Kongsfjord (30.10.2014; DOI: 10.1007/s00300-014-1607-6). CHAPTER 5 Huenerlage K and Buchholz F Thermal metabolic limits of krill species from the high Arctic Kongsfjord (Spitsbergen) may help explain euphausiid biogeographic variability The scientific concept was developed together with Dr. F. Buchholz. The krill samples were collected by us on-board the Kings Bay AS workboat MS Teisten. I performed the experiments, analytical work and data analyses and wrote the manuscript with contributions from Dr. F. Buchholz. This paper was submitted to Marine Ecology Progress Series (29.10.2014 submission number: 17132). ii Preface CHAPTER 6 Huenerlage K, Cascella K, Toullec JY and Buchholz F Towards finding the upper thermal limit of the arcto-boreal krill Thysanoessa inermis: Linking physiology to transcriptomics – first results The scientific concept was developed by all authors. The specimens were sampled by myself and Dr. F. Buchholz in August 2012. I performed the respiration experiments and related data analyses. The heat shock experiments were conducted by Dr. K. Cascella and Dr. J.Y. Toullec. Related data (gene expression of heat shock protein 70) were collected and analysed by Dr. K. Cascella. I wrote the manuscript with contributions from all authors. This paper is in preparation for publication. LARA KIM HÜNERLAGE iii iv TABLE OF CONTENTS Preface i Thesis Summary vii Abbreviations xi 1 General Introduction 1 2 Publication I 15 Huenerlage & Buchholz (2013) Krill of the northern Benguela Current and the Angola-Benguela frontal zone compared: physiological performance and short- term starvation in Euphausia hanseni 3 Publication II 49 Huenerlage et al. (in rev.) The other krill: overwintering physiology of adult Thysanoessa inermis (Euphausiacea) from the high Arctic Kongsfjord 4 Publication III 75 Huenerlage et al. (2014) Lipid composition and trophic relationships of krill species in a high Arctic fjord 5 Publication IV 109 Huenerlage & Buchholz (submitted) Explaining biogeographic distribution: thermal limits of krill species from the high Arctic Kongsfjord (Svalbard) 6 Publication V 133 Huenerlage et al. (in prep.) Towards finding the upper thermal limit of the arcto-boreal krill Thysanoessa inermis: Linking physiology to transcriptomics – first results 7 Synoptic Discussion and Conclusions 149 Acknowledgements 173 Appendix I v vi THESIS SUMMARY Krill are key species in marine food-webs and are distributed in all oceans with 86 species worldwide. They occupy a central role as consumers and as secondary producers forming an important food source for higher trophic levels from fish, squid and sea birds to marine mammals such as seals and whales. A change in regional krill populations would thus have a dramatic impact on the ecosystems of many climate zones. However, scientific knowledge on the ecophysiology of krill is scarce. The state of science is rather patchy (mainly focused on the charismatic Antarctic krill Euphausia superba) and there is no or little data available for an understanding of these key species’ ecology with a view to predict ecosystem changes in the oceans. The present PhD thesis aimed to contribute a broad range of ecophysiological data of abundant and ecologically important krill species from the Atlantic and the Arctic to assess these species’ metabolic performance and elucidate their overall adaptation to their respective environments under the constraints of ecosystem variability. The thesis is composed of five scientific publications (Chapters 2 – 6), which address in detail a) the temperature-induced metabolic performance and starvation capacity of the dominant krill species (Euphausia hanseni) from the highly productive northern Benguela Current system; b) the overwintering physiology, i.e. starvation capacity, of the dominant krill species (Thysanoessa inermis) from the high Arctic Kongsfjord; c) the energetic condition and trophic relationships of five different euphausiid species recently forming the krill community of the high Arctic Kongsfjord (T. inermis, T. raschii, T. longicaudata, Meganyctiphanes norvegica and Nematoscelis megalops) including an extended regional comparison to N. megalops specimens, which were sampled from the north Atlantic (i.e. the Iceland Basin) and the south Atlantic Benguela Current system; d) the temperature- induced metabolic performance of four krill species (T. inermis, T. raschii, M. norvegica and vii Thesis Summary N. megalops) from the high Arctic Kongsfjord and e) the metabolic and transcriptomic response to temperature increase in the dominant krill species (T. inermis) from the high Arctic Kongsfjord. In order to achieve an appropriate approximation of the single species’ physiological condition and adaptive capacity within their respective environments, the particular scientific questions of this thesis were tackled by investigating a variety of key physiological parameters: individual life parameters (stomach fullness, hepatopancreas colour, sex, size and body weight; Publications I – V), species-specific moulting rates