Utrecht Studies in Earth Sciences Mededelingen van de Faculteit Geowetenschappen Universiteit Utrecht No. 52 Ecosystem recovery after hypoxia: what can foraminifera indicate? Ecosysteem herstel na zuurstofdeficiëntie: wat kunnen foraminiferen ons vertellen? Margreet Brouwer Utrecht, 2014 Promotores Prof. dr. L.J. Lourens Professor Paleoclimatology at the Department of Earth Sciences at Utrecht University Prof. dr. J.J. Middelburg Professor Geochemistry at the Department of Earth Sciences at Utrecht University Copromotores Dr. M. Wolthers Advanced NERC Research Fellow at the University College London and Associate Researcher at the Department of Earth Sciences at Utrecht University Dr. I.A.P. Duijnstee Adjunct Assistant Professor Integrative Biology at the University of California, Berkeley and Assistant Professor at the Department of Earth Sciences at Utrecht University Members of the dissertation committee Prof. dr. E. Alve University of Oslo, Norway Prof. dr. A.J. Gooday University of Southampton, United Kingdom Prof. dr. J. Bijma Alfred Wegener Institute for Polar and Marine Research, Germany Prof. dr. J.W.F. Reumer Utrecht University, The Netherlands Dr. L.J. de Nooijer Koninklijk Nederlands Instituut voor Onderzoek der Zee, The Netherlands ISBN: 978-90-6266-354-5 ISSN 2211- 4335 Cover graphic: Margreet Brouwer Copyright © 2014 Margreet (G.M.) Brouwer The research presented in this thesis was funded by the Darwin Center for Biogeosciences and the Utrecht University. Niets uit deze uitgave mag worden vermenigvuldigd en/of openbaar gemaakt door middel van druk, fotokopie of op welke andere wijze dan ook zonder voorafgaande schriftelijke toestemming van de uitgevers. All rights reserved. No part of this publication may be reproduced in any form, by print or photo print, microfilm or any other means, without written permission by the publishers. Printed in the Netherlands by CPI – KONINKLIJKE WÖHRMANN, Zutphen Ecosystem recovery after hypoxia: what can foraminifera indicate? Ecosysteem herstel na zuurstofdeficiëntie: wat kunnen foraminiferen ons vertellen? (met een samenvatting in het Nederlands) Proefschrift ter verkrijging van de graad van doctor aan de Universiteit Utrecht op gezag van de rector magnificus, prof.dr. G.J. van der Zwaan, ingevolge het besluit van het college voor promoties in het openbaar te verdedigen op dinsdag 15 april 2014 des ochtends te 10.30 uur door Geertje Marrit Brouwer geboren op 14 augustus 1979 te Franeker Promotoren: Prof. dr. L.J. Lourens Prof. dr. J.J. Middelburg Copromotoren: Dr. M. Wolthers Dr. I.A.P. Duijnstee Contents Chapter 1 General introduction 9 Ecosystem recovery after hypoxia: what can foraminifera indicate? G.M. Brouwer Chapter 2 Recovery potential of benthic foraminiferal communities after 15 re-ventilation of hypoxia-deteriorated habitats: a microcosm experiment G.M. Brouwer, M. Wolthers and I.A.P. Duijnstee Chapter 3 Foraminiferal recolonisation pathways and microhabitat distribution after 35 prolonged hypoxia disturbance G.M. Brouwer, M. Wolthers, V.M. van Onselen and I.A.P. Duijnstee Chapter 4 Differential response of intertidal foraminifera to ecosystem recovery 55 succeeding hypoxia G.M. Brouwer, M. Wolthers, J.H. Hazeleger, F. Rossi, L.J. Lourens, J. J. Middelburg and I.A.P. Duijnstee Chapter 5 Diet shifts and population dynamics of estuarine foraminifera during 73 ecosystem recovery after hypoxia G.M. Brouwer, I.A.P. Duijnstee, J.H. Hazeleger, F. Rossi, L.J. Lourens, J. J. Middelburg and M. Wolthers Chapter 6 Impact of bioirrigation on the vertical distribution of benthic foraminifera 93 from the Swedish Gullmar Fjord G.M. Brouwer, I.A.P. Duijnstee, A.B. Craun and M. Wolthers Chapter 7 Thesis summary & synthesis 117 Ecosystem recovery after hypoxia: what can foraminifera indicate? G.M. Brouwer References 127 Introductie en samenvatting in het Nederlands 137 Ecosysteem herstel na zuurstofdeficiëntie: wat kunnen foraminiferen ons vertellen? G.M. Brouwer Dankwoord 149 Curriculum vitae 151 Contents 7 8 CHAPTER 1 GENERAL INTRODUCTION ECOSYSTEM RECOVERY AFTER HYPOXIA: WHAT CAN FORAMINIFERA INDICATE? G.M. Brouwer 1.1 FORAMINIFERA The unicellular eukaryotic phylum Foraminifera comprises an ecologically and biologically very diverse group of organisms, abundantly present in nearly all marine environments. Most of these extraordinary and beautiful single-celled organisms build a calcareous or agglutinated shell to house the bulk of their cytoplasm. The shell – also called test – of some calcareous species can reach a length of 11 cm or more (Hallock, 1985), while some mud-agglutinating species within the enigmatic group of Xenophyophora even exceed dimensions of 20 cm. Nonetheless, the size of the vast majority of foraminiferal species is less than 1 mm (Loeblich and Tappan, 1964). Hard-shelled foraminifera commonly secrete calcium carbonate to build a test, while agglutinated species collect foreign particles like clastic sediment grains, sea-urchin spines, or even the shells of other foraminifera to construct their test. During growth, most shell-bearing species add new chambers of increasing size to their test. Small openings – or the group’s namesake: foramina – interconnect these chambers to accommodate for the foraminiferal cytoplasm to use all chambers. The arrangement of chambers – which varies extensively among species – is of great taxonomic importance, since most foraminiferal species are defined based on test morphology. The aperture – the foramen in the youngest chamber – enables a thin threadlike net of cytoplasmic extensions to emerge through the shell. This pseudopodial network of anastomosing so-called reticulopoda is an apomorphic characteristic that all foraminifera share. These dynamic extensions of the cytoplasm can rapidly extend, split, merge and retract in a seemingly orchestrated manner. Foraminifera use their pseudopodia for several purposes, for example to gather or catch food. A diverse array of foraminiferal feeding strategies has been described. Some species graze on algae or bacteria, while others use their pseudopodia to trap detritus (Murray, 2006 – and references therein). Besides carnivorous, parasitic, kleptoplastic and cannibalistic life styles, some species have a symbiotic relation with bacteria or algae incorporated in their cytoplasm. Except for gathering food, benthic foraminifera use their pseudopodia for locomotion. Benthic foraminifera grasp sediment particles with their pseudopodia and drag themselves over and through sediments. By moving, they are not only able to collect food, it also enables them to occupy a favourable niche within the chemically stratified sediment column. Although several species live a planktonic life style in the water column, most foraminifera find their habitat either within, or on top of marine sediments. These benthic species, the subject of this thesis, are distributed along the vertical sediment profile. Among the benthic foraminifera, epifaunal species General introduction Ecosystem recovery after hypoxia: what can foraminifera indicate? 9 live on top, whereas shallow infaunal species occupy the upper part of the sediment (Linke and Lutze, 1993). Deeper-dwelling species, some of which are able to respire with nitrate instead of oxygen (Risgaard-Petersen et al., 2006), occur in high densities below the oxygen-penetration depth. Environmental circumstances determine the taxonomic and spatial structure of the foraminiferal assemblage – the foraminiferal species found in association with one another. Especially the availability of oxygen and food has been considered to shape foraminiferal communities and determine the vertical and geographical distribution of the individual members of the communities (Jorissen et al., 1995; Van der Zwaan et al., 1999). In dynamic ecosystems, for instance in coastal areas, the availability of oxygen and food changes constantly, often on a combination of seasonal, diurnal and semi-diurnal time scales. Each species has its own species-specific preferences and tolerances for environmental parameters such as oxygen concentration, temperature, salinity and food availability. Some foraminiferal species are relatively stress-tolerant, and especially those that have a short life span are able to swiftly respond to environmental perturbations at the population level. Although foraminiferal life cycles are not well studied, among investigated species a high diversity in foraminiferal life span (and generation span, a foraminifers life terminates with reproduction) has been observed (Hallock, 1985). Foraminifera were noticed to postpone reproduction during unfavourable conditions and, if environmental conditions admit, to grow until improved circumstances enable them to reproduce (Hallock, 1985). Several strategies, including changeable numbers of offspring (less offspring increase the size and survival rate of the new individuals) and alternation between asexual and sexual reproduction (with small, but genetically diverse microspheric offspring after sexual reproduction and larger megalospheric offspring after asexual reproduction) may enhance the success of this community in diverse and fluctuating circumstances (Hallock, 1985). The broad diversity of niches suitable for foraminiferal occupation gives rise to a dense presence of living individuals as well as fossil specimens in almost all marine sediments. The fossil record of foraminifera enclosed in marine sediments consists of those species that build a calcareous or agglutinated test. The high fossilisation potential of these