The effects of biogeochemical stressors on seagrass ecosystems Laura Leone Govers 2014 The effects of biogeochemical stressors on seagrass ecosystems Proefschrift ter verkrijging van de graad van doctor aan de Radboud Universiteit Nijmegen op gezag van de rector magnificus prof. dr. Th.L.M. Engelen, volgens besluit van het college van decanen in het openbaar te verdedigen op vrijdag 12 december 2014 Govers, Laura L. (2014): The effects of biogeochemical stressors on seagrass om 10.30 uur precies ecosystems. PhD thesis, Radboud University Nijmegen, 238p. With summaries in English, Dutch & French. This PhD project was financially supported by Projectbureau Zeeweringen and Rijkswaterstaat Zeeland and part of the project ‘Zeegrasmitigaties Oosterschelde’ door Copyright: Laura Govers 2014. All rights reserved. No part of this publication Laura Leone Govers may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronically, mechanically, photocopying, recording or geboren op 16 september 1985 otherwise, without prior permission in writing from the publisher. te ’s-Hertogenbosch Layout & Design: Lilian Admiraal, [email protected] Photos: Laura Govers Printed by: Ipskamp Drukkers Correspondence: [email protected], lauragovers.com “What we know is a drop, what we do not know is an ocean” Promotor Prof. Dr. Peter M.J. Herman Copromotor Dr. Tjeerd J. Bouma, NIOZ Yerseke Dr. Marieke M. van Katwijk Manuscriptcommissie Prof. dr. Jan G.M. Roelofs Prof. dr. Jack B.M. Middelburg (Universiteit Utrecht) Prof. dr. Marianne Holmer (Syddansk Universitet, Denmark) Isaac Newton Paranimfen Marjolijn Christianen Marloes Hendriks contents contents Contents Chapter 1 Chapter 7 Introduction 8 A three-stage symbiosis forms the foundation of seagrass 102 ecosystems Chapter 2 Chapter 8 Toxic effects of sediment nutrient and organic matter 22 Seagrasses are negatively affected by organic matter 122 loading on Zostera noltii loading and Arenicola marina activity in a laboratory experiment Chapter 3 Rhizome starch as indicator for temperate seagrass winter 38 Chapter 9 survival Experimental evidence linking abiotic stress, mutualism 136 Biogeochemical species interactions breakdown and ecosystem degradation in seagrasses Resilience & Restoration Chapter 4 Feedbacks and local factors affect the disturbance- 54 recovery dynamics of intertidal seagrasses Chapter 10 Synthesis 152 Chapter 5 References 168 Seagrasses as indicators for coastal trace metal pollution: 70 a global meta-analysis serving as a benchmark, and a Summary/Samenvatting/Résumé 204 Pollution Caribbean case study Acknowledgements/Dankwoord 222 Chapter 6 List of Publications 232 Eutrophication threatens Caribbean seagrasses: an 90 Curriculum Vitae 236 example from Curaçao and Bonaire 6 7 Chapter 1 Introduction Chapter Seagrasses are aquatic angiosperms, the only flowering plants that are well 1 adapted to live and reproduce in saline waters. Although they look somewhat similar to terrestrial grasses (Figure 1.1), they are not related to this group of plants, but evolved from freshwater macrophytes about 100 million years ago (den Hartog 1970, Les et al. 1997). The 12 genera of seagrass species belong to four different families: Zosteraceae, Posidoniaceae, Cymodoceae, and Hydrocharitaceae, forming an ecological rather than a taxonomical group (den Hartog and Kuo 2006). Like terrestrial grass species, seagrasses can form extensive meadows in shallow coastal waters all over the world (Green and Short 2003). The depth limit of seagrasses is determined by the water clarity, as they need light for photosynthesis, and the seagrass species Posidonia oceanica can be found up to 50 m depth in the clearest parts of the Mediterranean (Duarte 1991). In contrast, seagrasses in murky waters may grow to very shallow depths Figure 1.1 Impression of the structure of the of only 1 m. Next to subtidal species, tropical seagrass species Cymodocea rotundata. which grow constantly submerged, This plant consists of four clones, which are connected by a horizontal rhizome. Rhizomes there are also seagrasses that occur are used for clonal expansion, but also for the in intertidal areas, where mainly storage of carbohydrate reserves. The roots desiccation stress and hydrodynamics take up nutrients from the sediment and determine their upper depth limits anchor the plants. The shoots consist mainly of photosynthetic tissue, but are also used for the (Leuschner et al. 1998, Bjork et al. uptake of nutrients and carbon from the water 1999). column. Picture © Ruth Berry 9 Introduction Chapter 1 The natural value of seagrass beds is often unknown or unrecognized compared to Wyllie-Echeverria 1996, Burkholder et the attractive and colorful neighboring coral reefs, but the importance of seagrass al. 2007). These high nutrient levels ecosystems is comparable to that of coral reefs, mangroves and salt marshes in lead to increased turbidity and lower terms of ecosystem services and ecological richness. More importantly, these light-availability for seagrasses, as coastal ecosystems are often interconnected by means of migrating animals, these favor fast growing plankton and nutrient fluxes, and organic carbon (Nagelkerken 2000, Cowen et al. 2006, Gillis macroalgae species at the expense of et al. 2014). Seagrass ecosystems rank among the most productive and most seagrasses (Figure 1.2) (Hauxwell et al. valuable ecosystems on earth, in terms of value ($) per hectare (Costanza et al. 2003, Kemp et al. 2005). Additionally, 1997). This value can be attributed to the many ecosystem services that seagrass eutrophication may also directly affect beds can provide: high rates of production and nutrient cycling (Duarte and seagrasses by promoting ammonium Chiscano 1999), carbon sequestration (Fourqurean et al. 2012), coastal protection and sulfide toxicity (van Katwijk et al. Figure 1.2 Seagrasses (Syringodium filiforme) by attenuation of waves and currents and by stabilizing the sediment (Christianen 1997, Koch and Erskine 2001, Van der and (Thalassia testudinum) growing in a turbid, et al. 2013), nursery habitat for commercial fish species (Nagelkerken 2000), Heide et al. 2008). eutrophic bay on Curaçao, Netherlands Antilles. and habitat and food for many endangered species (Valentine and Heck 1999, Christianen et al. 2012). Disappearance of seagrass beds also implies the loss of important ecosystem services that seagrasses provide, such as coastal protection (Christianen et Seagrass beds under threat al. 2013), fisheries (Gillanders 2006), and carbon sequestration (Fourqurean Regrettably, seagrass beds have been declining rapidly over the past decades: et al. 2012). Moreover, seagrass beds are strongly connected to other coastal with about 7% per year since 1990 – a rate of decline comparable to that of coral ecosystems so degradation or disappearance of seagrasses may also affect reefs and tropical rainforests (Orth et al. 2006, Waycott et al. 2009). The main ecosystem functioning and ecosystem services (e.g. fisheries) of nearby coral reason for this decline is the increase of human activities in coastal areas (Short reefs, mangroves, and salt marshes. Therefore, stressors threatening seagrass and Wyllie-Echeverria 1996). Nowadays, billions of people live in coastal areas all beds and thus other coastal ecosystems should be recognized and halted to over the world (Cohen et al. 1997, Small and Nicholls 2003), and in a few decades, prevent further loss of coastal key-ecosystems and related ecosystem services. probably 50% of the entire human population will be living within 150 km from Fortunately, there is an increasing number of marine protected areas (MPAs) the shore (Cohen 2003). This development has lead to a steep increase of human that include seagrass beds (Orth et al. 2006), and there have been worldwide activities in coastal areas such as dredging, aquaculture, sewage discharge, initiatives on the restoration of seagrass meadows (Van Katwijk et al. submitted). industrial activities, and deforestation (Cohen 2003, Mora 2008), which severely threaten coastal ecosystems, including seagrass beds. Seagrass dynamics and restoration Seagrass beds form naturally dynamic landscapes which are maintained through These activities have resulted in eutrophication, high trace metal levels, habitat asexual clonal expansion, sexual recruitment and the turnover of shoots (Duarte et degradation, and increased water column sediment loads, which negatively al. 2006). These processes act over various spatial and time scales and unbalances affect seagrass ecosystems. In addition, also climate change may put pressure in in these dynamic processes may result in changes on a meadow scale, such as on global seagrass ecosystem functioning (Orth et al. 2006, Waycott et al. 2009). patchy and heterogeneous landscapes, which may be more vulnerable to stressors In theory, climate change may lead to circumstances favorable to seagrasses, as than healthy seagrass beds (Chapter 2). Unbalanced seagrass dynamics may even they evolved about 100 million years ago in times of higher CO2 concentrations, result in catastrophic declines, due to altered disturbance-recovery dynamics temperatures and sea levels. However, current global change is much more rapid (Chapter 4), which we discussed above (1.1) (Duarte et al. 2006). As seagrass beds than ancient change rates and it may thus be hard for seagrasses to adapt to have been disappearing on a global scale, many attempts have been made to present changing environmental