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University of Groningen Multi-trophic interactions within the seagrass beds of Banc d'Arguin, Mauritania van der Geest, Matthijs IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Early version, also known as pre-print Publication date: 2013 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): van der Geest, M. (2013). Multi-trophic interactions within the seagrass beds of Banc d'Arguin, Mauritania: A chemosynthesis-based intertidal ecosystem. s.n. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 25-09-2021 Multi-trophic interactions within the seagrass beds of Banc d'Arguin, Mauritania A chemosynthesis-based intertidal ecosystem Matthijs van der Geest Multi-trophic interactions within the seagrass beds of Banc d’Arguin, Mauritania A chemosynthesis-based intertidal ecosystem The work presented in this thesis was conducted at the Department of Marine Ecology (MEE), Royal Netherlands Institute for Sea Research (NIOZ) according to the requirements of the Graduate School of Science (Faculty of Mathematics and Natural Sciencees, University of Groningen). The research was funded by a grant from the Netherlands Organisation for Scientific Research (NWO-WOTRO Integrated Programme, W.01.65.221.00) awarded to T. Piersma. The printing of this thesis was funded by the Royal Netherlands Institute for Sea Research (NIOZ) and the Faculty of Mathematics and Natural Sciences of the University of Groningen. This thesis should be cited as: van der Geest, M. (2013) Multi-trophic interactions within the seagrass beds of Banc d’Arguin, Mauritania: a chemosynthesis-based intertidal ecosystem. PhD Thesis, University of Groningen, Groningen, The Netherlands Cover design: Marije van Overmeeren Lay-out & figures: Dick Visser Photographs: Jimmy de Fouw (cover Chapter 2, 3), Han Olff (cover Chapter 4), Jan van Gils (cover Chapter 5, 6), Jan van de Kam (cover Chapter 7, 8 (top photo)), Jeroen Onrust (cover Chapter 8, right bottom photo), Piet van den Hout (cover Chapter 9, left page), Joop van Eerbeek (cover Chapter 9, right page), Brecht de Meulenaer (cover ‘References’), Theunis Piersma (cover ‘Acknowledgements’), and Matthijs van der Geest (other). Printed by: Ipskamp Drukkers, Enschede ISBN: 978-90-367-6571-8 ISBN: 978-90-367-6570-1 (electronic version) RIJKSUNIVERSITEIT GRONINGEN Multi-trophic interactions within the seagrass beds of Banc d’Arguin, Mauritania A chemosynthesis-based intertidal ecosystem Proefschrift ter verkrijging van het doctoraat in de Wiskunde en Natuurwetenschappen aan de Rijksuniversiteit Groningen op gezag van de Rector Magnificus, dr. E. Sterken, in het openbaar te verdedigen op vrijdag 15 november 2013 om 12.45 uur door Matthijs van der Geest geboren op 7 april 1978 te Leiderdorp Promotores: Prof. dr. T. Piersma Prof. dr. J. van der Meer Prof. dr. H. Olff Copromotor: Dr. J. A. van Gils Beoordelingscommissie: Prof. dr. L. Chauvaud Prof. dr. C. M. Duarte Prof. dr. P. M. J. Herman Voor Sem “In the long history of humankind (and animal kind, too) those who learned to collaborate and improvise most effectively have prevailed.” Charles Darwin (1809-1882) Contents Chapter 1 General introduction 9 Box A Molecular evidence for sulphide-oxidizing endosymbiosis in Loripes lucinalis 18 Chapter 2 Nutritional and reproductive strategies in a chemosymbiotic bivalve living in a 23 tropical intertidal seagrass bed Chapter 3 A three-stage symbiosis forms the foundation of seagrass ecosystems 47 Chapter 4 Suitability of calcein as an in situ growth marker in burrowing bivalves 69 Chapter 5 Trophic cascade induced by molluscivore predator alters pore-water biogeochemistry 85 via competitive release of prey Chapter 6 Seasonal changes in mollusc abundance in a tropical intertidal ecosystem, 103 Banc d’Arguin (Mauritania): testing the ‘shorebird depletion’ hypothesis Chapter 7 Size- and season-specific predation moulds timing of reproduction in a tropical 121 marine bivalve Chapter 8 Toxin constraint explains diet choice, survival and population dynamics in a 139 molluscivore shorebird Chapter 9 Density-dependent growth in three tropical intertidal bivalves: importance of 163 feeding style, habitat and season Chapter 10 General discussion: the functioning of the Banc d’Arguin ecosystem revisited 183 References 199 Summary 222 Samenvatting 227 Résumé 232 Dankwoord / Acknowledgements / Remerciement 239 Names and addresses of authors 250 List of publications 252 Chapter1 General introduction Matthijs van der Geest CHAPTER 1 The distribution and abundance of organisms in space and time, and the interactions within and between species (e.g., predation, competition, mutualism), and between species and their physical and chemical environment, are central to ecology (Begon, Townshend & Harper 2006). Understanding which interactions drive life histories, population dynamics, and com- munity functioning and their response to environmental change is critical for management and preservation of natural communities and ecosystems in a rapidly changing world (Lubchenco et al. 1991). This thesis is about the distribution and abundance of organisms living in a tropical seagrass-covered intertidal mudflat, and the physical, chemical, but espe- cially biological features and interactions that determine these distributions and abundances. The tidal flat ecosystem A tidal flat can be defined as an area of sea floor that is submerged at high tide and exposed during low tide. Tidal flat occur along tidal channels in bays and lagoons, in estuaries, and along coastal seas and inlets and connect the terrestrial and the marine environments. They range from bare flats to sediments covered with seagrasses or mangroves and can be found in all climate zones, from the Arctic Circle up to the Equator (Eisma 1998). Intertidal flat systems are known for their high primary productivity, and great abun- dance of benthic invertebrates (e.g., mollusks, polychaetes, crustaceans) and secondary con- sumers (e.g. shrimps, crabs, fish, shorebirds) living from this production (Swennen 1976; Pihl & Rosenberg 1982; Jensen & Jensen 1985; Zwarts & Blomert 1992; van der Veer et al. 1998; van de Kam et al. 2004). Extensive tidal flat systems are quite rare and are usually found at the outflows of major rivers. Indeed, only about two handfuls of coastal intertidal flat systems worldwide support the great majority of northern shorebird migrants, who con- gregate at such sites during the nonbreeding seasons in large numbers, arriving there from the vast expanses of boreal to high Arctic taiga and tundra (van de Kam et al. 2004). In addition, tidal flat systems fulfil great ecological roles as nursery areas for the juvenile stages of offshore fishes and shrimp (Zijlstra 1972; van der Veer, Dapper & Witte 2001), as a habitat for sedentary fishes, their predators and other marine biota and by dissipating wave energy, thus reducing coastal erosion. They are also of great economic value, since many of the organisms that depend on these coastal systems (e.g., lugworms, shellfish, shrimp, fish) are commercially exploited (Beukema 1995; Dijkema 1997; Piersma et al. 2001; Lotze 2007). Many studies have focused on the functioning of intertidal food webs at temperate lati- tudes, but many fewer ecological studies have been carried out in tropical intertidal ecosys- tems (Alongi 1990). This lack of knowledge includes the Banc d’Arguin ecosystem off the coast of Mauritania, which has received ecological scrutiny in the 1980s (reviewed by Wolff et al. 1993b), but not much since, even though many of the basic questions remained un- answered. This is surprising, since a good understanding of the functioning of this pristine coastal ecosystem, which became a National Park in 1976 and a UNESCO World Heritage Site in 1989, is critical for optimal management and conservation of its natural resources. 10 GENERAL INTRODUCTION The riddle of the Banc d’Arguin The Banc d’Arguin, Mauritania, northwest Africa, is an area of over 10,000 km2 of inter- tidal flats and shallow inshore waters bordering the Sahara desert (Fig. 1.1). With over two million wintering shorebirds, this intertidal system is the most important coastal wintering site along the East Atlantic coast (Trotignon et al. 1980; Altenburg et al. 1982; Engelmoer et al. 1984; Smit & Piersma 1989; Zwarts et al. 1990; Zwarts et al. 1998). These large num- bers of shorebirds are distributed over ca. 500 km2 of tidal flats only (Wolff & Smit 1990). Not surprisingly, average feeding densities of wintering waders in the intertidal zone of Banc d’Arguin are extremely high when compared to other coastal wintering sites along the East Atlantic coast (Zwarts 1988; Zwarts et al. 1990; van Gils et al. 2009). In the past decades some research was carried out to make a beginning of an explana- tion for the very high densities of wintering shorebirds at Banc d’Arguin. In several studies data was collected on biomass of benthic macrofauna on the intertidal flats, the food of the large majority of these wintering shorebirds (see review in Table 1.1). These studies established that, contrary to initial expectation, food resources potentially available to shorebirds were relatively low, 7.6–28.6 g ash-free dry mass (AFDM) per m2, compared to other tidal flat areas in the world where biomass values of 100 g AFDM per m2 are no exception (Heip 1995; Michaelis & Wolff 2001; Purwoko & Wolff 2008).

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