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Marine Ecology Progress Series 384: 83-96

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Marine Ecology Progress Series 384: 83-96 Vol. 384: 83–96, 2009 MARINE ECOLOGY PROGRESS SERIES Published May 29 doi: 10.3354/meps08024 Mar Ecol Prog Ser OPENPEN ACCESSCCESS How effective are MPAs? Predation control and ‘spill-in effects’ in seagrass–coral reef lagoons under contrasting fishery management Johan S. Eklöf1, 4,*, Sara Fröcklin1, Annika Lindvall1, Nadja Stadlinger1, Alex Kimathi2, Jacqueline N. Uku2, Tim R. McClanahan3 1Department of Systems Ecology, Stockholm University, 106 91 Stockholm, Sweden 2Kenyan Marine and Fisheries Research Institute, PO Box 81651, 080100 Mombasa, Kenya 3Marine Programs, Wildlife Conservation Society, Bronx, New York 10460-1099, USA 4Present address: Department of Marine Benthic Ecology and Evolution, Biological Centre, University of Groningen, Kerklaan 30, PO Box 14, 9750 AA Haren, The Netherlands ABSTRACT: Marine protected areas (MPAs) are heavily promoted as a panacea for marine conserva- tion, but lagging and sometimes idiosyncratic protection effects bring their overall effectiveness into question. In Kenyan lagoons, seagrass overgrazing by the sea urchin Tripneustes gratilla has been linked to removal of predators, but overgrazing has also been observed within well-protected MPAs. In this study we investigated the effectiveness of Kenyan MPAs in facilitating predation control over sea urchins, particularly T. gratilla, in relation to system (seagrass or coral reef), distance to reefs, and seagrass presence. A strong protection effect on urchin densities on reefs and a negative correlation between T. gratilla density and predation pressure (from sea stars, fish and gastropods) in seagrass beds (r2 = 0.345) confirmed the importance of top-down control. Yet there were no clear effects of pro- tection or distance to reefs in seagrass beds, most likely due to (1) low predator densities in the recently established Mombasa MPA; (2) ‘spill-in’ of aggregated T. gratilla into the older Watamu MPA (potentially facilitated by low predation pressure on the large urchins and nutrient enrichment); and (3) a potential buffering effect of seagrass canopies on predation, regardless of distance to reefs. Effects of seagrass presence differed between areas, but indicated that overgrazing in some areas could be self-regulated by inducing higher urchin mortality. As MPA effects appear to be system-, time- and site-specific, managers should also assess other more holistic approaches (e.g. banned fish- ing of urchin predators and reduced nutrient input from land runoff) to protect seagrasses. KEY WORDS: Marine protected areas · Indirect effects · Trophic cascades · Seagrass · Tripneustes gratilla · Thalassodendron ciliatum · Kenya · Shelter Resale or republication not permitted without written consent of the publisher INTRODUCTION agement ‘panacea’ (e.g. Kelleher & Kenchington 1992, Agardy 1994, NRC 2001). MPAs can indeed provide a Coastal fisheries supply a crucial food source for hu- number of benefits, e.g. protection of target stocks (Polu- mans, but have frequently been found to drive depletion nin & Roberts 1993), ‘spill-over’ to adjacent fisheries (Mc- of target and non-target species, weaken trophic cas- Clanahan & Mangi 2000) and strengthening trophic cas- cades, and indirectly cause community shifts associated cades (McClanahan & Shafir 1990, Guidetti & Sala 2007). with reduced ecosystem functioning (Jennings & Kaiser At the same time, however, protection effects can be spa- 1998, Pinnegar et al. 2000, Jackson et al. 2001). Conse- tially idiosyncratic (Guidetti & Sala 2007), show consid- quently, implementation of marine protected areas erable time lags (McClanahan & Graham 2005, Guidetti (MPAs) has become heavily promoted as a global man- & Sala 2007), and when poorly designed and managed *Email: [email protected] © Inter-Research 2009 · www.int-res.com 84 Mar Ecol Prog Ser 384: 83–96, 2009 conflict with local livelihoods (Sale et al. 2005). This strate features that normally buffer cascading effects makes it imperative to investigate in closer detail under (Borer et al. 2005) — e.g. feeding on multiple trophic lev- what circumstances MPAs produce the benefits with els (Heck et al. 2000), and buffering effects of habitat which they are so often associated (e.g. Sale et al. 2005). structural complexity and prey size (Heck & Valentine Seagrasses are rhizomatous marine angiosperms that 1995, Farina et al. 2009) — that can override protection form inter- and sub-tidal beds in coastal areas around the effects (Prado et al. 2008). world (Green & Short 2003). By supplying a range of In East Africa, seagrass beds constitute diverse and ecosystem services to society (e.g. fisheries production productive ecosystems (Ochieng & Erftemeijer 2003) and nutrient filtering), seagrass beds are one of the most that are highly important fishing grounds (de la Torre- valuable coastal ecosystems (Costanza et al. 1997). The Castro & Rönnbäck 2004). Grazing by parrotfish and ‘bottom-up’ paradigm (i.e. that resources limit produc- sea urchins is a common natural disturbance in most tion) has dominated seagrass ecology and management, areas (Alcoverro & Mariani 2004), known to enhance but is currently questioned by accumulating evidence of seagrass production (Eklöf et al. 2008). Over the last the importance of ‘top-down’ (consumer) control over decades, however, highly dense aggregations of the seagrasses and associated macroalgae (see Valentine & urchin Tripneustes gratilla has overgrazed entire beds Duffy 2006 for review). As many seagrass communities of the dominating seagrass Thalassodendron ciliatum display features that generally promote cascading ef- (Fig. 1a) in a number of areas along the Kenyan coast fects of top predators, e.g. strong interactions between (Eklöf et al. 2008). On adjacent coral reefs, protection few keystone species or functional groups at each of sea urchin predators (primarily the triggerfish Bal- trophic level (Valentine & Duffy 2006, Moksnes et al. istapus undulatus and the wrasse Cheilinus undulatus) 2008), it has been suggested that overharvest of top indirectly reduces densities of sea urchins (McClana- predators could be a major driver behind seagrass loss han & Muthiga 1989, McClanahan & Shafir 1990). It (Heck & Valentine 2007, Moksnes et al. 2008). At the has therefore been suggested that coral reef fisheries same time, however, many seagrass systems demon- could contribute to high densities of urchins in sea- Fig. 1. (a) Thalassodendron ciliatum seagrass beds. Left panel: healthy bed with low urchin density. Right panel: overgrazed bed in Watamu Marine Park with aggregation of the herbivorous sea urchin Tripneustes gratilla. Photos: Maria Asplund and Annika Lindvall. (b) Hypothesized effects of protection on predation on urchins, urchin densities, and urchin grazing on seagrasses. (c) Hypothesized effects of distance to coral reefs on predation rates on urchins (solid lines: protected areas; dashed lines: fished areas). (d) Hypothesized self-regulated sea urchin overgrazing in protected but not in fished areas Eklöf et al.: Cascading effects in MPAs? 85 grass beds as well (Alcoverro & Mariani 2004). At the 1.5 to 4 m, and surface water temperature ranges from same time, several of the overgrazing events have 25 to 31°C (Obura 2001). Seagrass beds are a dominat- occurred within old and well-protected MPAs (Alcov- ing feature of the lagoons, with 12 species encountered erro & Mariani 2002, Zanre & Kithi 2004). Conse- in mixed and monospecific beds (Ochieng & Erftemei- quently, there is an obvious need to investigate to what jer 2003). The dominant seagrass is Thalassodendron extent these MPAs actually facilitate predation on sea- ciliatum L., found subtidally from the shore to the reef grass-residing sea urchins and thereby control their flats (Obura 2001) in densities of ~700 shoots m–2 and grazing pressure on seagrasses (Fig. 1b). with leaf biomass of ~150 g DW m–2 (Uku & Bjork 2005). In many tropical areas seagrass beds subsidize adja- Survey 1. Survey design: Effects of protection and cent coral reef food webs, as many reef-associated pre- area on sea urchins on coral reefs were estimated dur- dators (often large finfish) feed on seagrass-associated ing low water spring tides in Feb to March 2006 by grazers and other primary consumers (Heck et al. 2008). sampling in 4 fished and 4 protected coral reef areas In East Africa, such feeding migrations seem to be re- along a 200 km stretch of the southern Kenyan coast stricted to seagrass areas closest to reefs (Dorenbosch et (Fig. 2). The 4 MPAs (from north to south) were Ma- al. 2005). Consequently, if reef-associated predators con- lindi, Watamu, Mombasa and Kisite Marine National trol sea urchins close to reefs, urchin densities should Parks, gazetted in 1968, 1971, 1991 (fully protected in increase with increasing distance from reefs, at least in 1995) and 1978, respectively (Obura 2001). In these areas where reef predators are abundant (Fig. 1c). parks fishing and extraction of other natural resources Structural habitat complexity can mediate predator– (e.g. invertebrate collection) is banned, resulting in prey interactions, e.g. between predatory fish and sea higher diversity, density and biomass of predatory fish urchins (Hereu et al. 2005), and even override protec- inside than outside parks (e.g. Obura 2001, McClana- tion effects (Guidetti & Sala 2007). As seagrass leaves han & Graham 2005). The 4 fished areas were (from form dense canopies that can shelter invertebrates north to south) Vipingo, Kanamai, Ras Iwatine and (e.g. Heck et al. 2003) and seagrass protection
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