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Ecological connectivity in East African seascapes

Charlotte Berkström

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©Charlotte Berkström, Stockholm 2012 ISBN 978-91-7447-477-0 Printed in Sweden by US-AB, Stockholm 2012 Distributor: Department of Systems Ecology, Stockholm University Cover photo: Ian Bryceson

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Abstract

Coral reefs, seagrass beds and mangroves constitute a complex mosaic of habitats referred to as the tropical seascape. Great gaps exist in the knowledge of how these systems are interconnected. This thesis sets out to examine ecological connectivity, i.e. the connectedness of ecological processes across multiple scales, in Zanzibar and Mafia Island, Tanzania with focus on functional groups of fish. Paper I examined the current knowledge of interlinkages and their effect on seascape functioning, revealing that there are surprisingly few studies on the influences of cross-habitat interactions and food-web ecology. Furthermore, 50% of all fish species use more than one habitat and 18% of all coral reef fish species use mangrove or seagrass beds as juvenile habitat in Zanzibar. Paper II examined the seascape of Menai Bay, Zanzibar using a landscape ecology approach. The relationship between fish and landscape variables were studied. The amount of seagrass within 750m of a coral reef site was correlated with increased invertebrate feeder/piscivore fish abundance, especially Lethrinidae and Lutjanidae, which are known to perform ontogenetic and feeding migrations. Furthermore, within-patch seagrass cover was correlated with nursery species abundance. Paper III focused on a seagrass-dominated seascape in Chwaka Bay, Unguja Island and showed that small-scale habitat complexity (shoot height and density) as well as large-scale variables such as distance to coral reefs affected the abundance and distribution of a common seagrass parrotfish Leptoscarus vaigiensis. Paper IV studied the connectivity and functional role of two snappers (Lutjanus fulviflamma and L. ehrenbergii) using stable isotopes (δ15N and δ13C) and found that connectivity between habitats was maintained by ontogenetic and foraging migrations by these species. The thesis found that ecological connectivity and multi-habitat usage by fish is a general and important characteristic in the Western Indian Ocean and should be taken into account in conservation and management planning. Furthermore, a landscape ecology approach was found applicable when exploring connectivity within tropical seascapes.

Keywords: fish, functional group, food-web interactions, nursery, coral, seagrass, mangrove, landscape ecology

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Sammanfattning

I många tropiska områden bildar mangrove, sjögräsängar och korallrev en mosaik av habitat, ofta kallat ett tropiskt havslandskap. Vi har ganska goda kunskaper om vart och ett av dessa habitat, men väldigt lite om hur dessa är länkade till varandra och hur havslandskapet fungerar som helhet. Vandrande fiskar utgör en av de viktigaste länkarna i havslandskapet. Tex växer många korallrevsfiskar upp i mangrove eller sjögräsområden och flyttar sedan till korallreven när de blir större. Många korallrevsfiskar simmar även mellan korallrev och sjögräs för att äta och kontrollerar då populationerna av födodjur i sjögräs och bidrar till utbytet av energi och närsalter mellan habitaten. Det flesta studierna har gjorts i Karibien men det saknas till stor del information från andra områden som Afrika och Sydostasien.

Målet med denna avhandling är därför att fylla informationsluckor i förståelsen för hur olika områden är länkade via migrerande fiskar, framförallt i östra Afrika, och vilka funktioner dessa fiskar bidrar med. Avhandligen börjar med en genomgång av litteratur om länkar i det tropiska havslandskapet, med fokus på fiskmigrationer, för att få en akuell bild. Det visade sig att det saknas väldigt mycket information om länkarnas betydelse för havslandskapet som helhet och vad som sker när dessa länkar bryts. Då många fiskar är involverade i födoväven och bidrar med transporter av energi och material kan även länkade områden påverkas om ett intilliggande område förstörs. En sammanställning av information runt Zanzibar visade att hälften av alla korallrevsfiskarter utnyttjar mer än ett habitat och nästan en femtedel utnyttjar mangrove och sjögräs som uppväxtområden. Dessa resultat kullkastar den tidigare uppfattningen att områden i Afrika och Sydostasien är mindre länkade än i Karibien.

Vidare använde jag lanskapsekologiska metoder, utvecklade för terrestra miljöer, i två olika havslandskap (ett sjögräsdominerat och ett korallrevsdominerat) på Zanzibar för att se hur utseendet av havslandskapet påverkade förekomsten av olika viktiga fisksamhällen. Denna metod som tidigare inte använts i marina miljöer visade sig vara en lämplig metod att testa konnektiviet (länkar) i tropiska områden. Slutligen användes stabila isotoper (kol och kväve) som en naturlig ”märkning” för att visa att migrationer mellan mangrove, sjögräs och

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korallrev förekommer hos två fiskarter som liknar varandra till utseendet och ofta simmar tillsammans. Dessutom gjordes maganalyser på dessa fiskar för att förstå vad de äter och på så sätt hur de påverkar födoväven i de olika områdena.

Avhandligens fyra studier har ökat vår förståelse för hur mangrove, sjögräsängar och korallrev är länkade via fiskmigrationer, framförallt i östra Afrika där man tidigare inte trodde detta var särskilt betydelsefullt. Den har även bidragit med information som kan användas inom förvaltning av fisk i dessa områden.

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List of papers

This thesis is based on the following papers, referred to by roman numerals:

I. Exploring 'knowns' and 'unknowns' in tropical seascape connectivity: a review with insights from East African coral reefs. Berkström C, Gullström M, Lindborg R, Kautsky N, Mwandya AW, Yahya SAS and Nyström M. (In press, Estuarine, Coastal and Shelf Science).

II. Seascape configuration influences connectivity of reef fish

assemblages. Berkström C, Lindborg R, Thyresson M, Gullström M. (Submitted to Landscape Ecology).

III. Scale-dependent patterns of variability of a grazing parrotfish

(Leptoscarus vaigiensis) in a tropical seagrass-dominated seascape. Gullström M, Berkström C, Öhman MC, Bodin M, Dahlberg M. Marine Biology 158 (7): 1483-1495.

IV. Interlinkages and trophic relationships within a tropical

seascape in East Africa. Berkström C, Lund Jörgensen T, Hellström M. (In Review, Marine Ecology Progress Series).

My contribution: Planning and designing the study (Paper I, II and IV), collecting the data (Paper I, II and IV), constructing the fish database (Paper I), analysing the data (Paper I, II, III and IV) and writing the paper (Paper I, II, III and IV). The published papers are reprinted with kind permission from the publishers.

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Contents

Abstract ................................................................................................................................ 3

Sammanfattning................................................................................................................ 5

List of papers ...................................................................................................................... 7

Introduction .................................................................................................................... 11

Theoretical framework ............................................................................................... 13 Connectivity in the tropical seascape .............................................................. 13 Fish migrations ......................................................................................................... 13 Ecological connectivity and seascape functioning ..................................... 15 Incorporating landscape ecology – a new approach ................................. 16

Study region .................................................................................................................... 18

Methods ............................................................................................................................. 21

General findings ............................................................................................................. 23 Paper I .......................................................................................................................... 23 Paper II ......................................................................................................................... 24 Paper III ....................................................................................................................... 24 Paper IV ....................................................................................................................... 25

General discussion ........................................................................................................ 27

Concluding remarks ..................................................................................................... 31

Acknowledgements ...................................................................................................... 32

References ........................................................................................................................ 33

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Introduction

The tropical seascape is comprised of a complex mosaic of mangroves, seagrass beds and coral reefs influenced by terrestrial as well as open ocean activities (Ogden 1988). The seascape provides ecosystem services that are fundamental for economical and societal development (Moberg & Folke 1999) where one of the most important and recognized ecosystem services provided is the supply of catch from fisheries (Jiddawi & Öhman 2002). These life-supporting systems are subjected to a number of stressors including climate change, eutrophication, land-based pollution and over-harvesting. Furthermore, there is a remarkable increase in the demand of marine resources from local and international markets around the world. In the light of this, there is a need to depart from current management philosophy and recognize that the cost of overexploitation extends beyond the immediate impacts of depletion of targeted stocks (Hughes et al. 2005; Berkes et al. 2006). A fundamental steppingstone in this process is to recognize the functional aspects of species and their interactions in the seascape across habitat boundaries. We need to treat shallow-water ecosystems as inter-linked support areas that underpin ecosystem services across scales. Little attention has been given to manage ecosystem functions provided by different sets of species (i.e. functional groups) (Steneck 2001; Nyström 2006). However, species that maintain critical ecosystem functions operate at multiple scales (Peterson et al. 1998). Consequently, if management is to succeed, the understanding of cross-scale interactions is imperative for understanding the system as a whole. Connectivity is in this sense a key issue.

Bellwood et al. (2004) highlighted the importance to scale up management and governance systems to secure the future of diverse functional groups and their roles in supporting the functioning of shallow-water habitats. A number of coral reefs around the world have undergone phase-shifts, where healthy reefs previously dominated by live coral cover have changed to degraded habitats covered in large fleshy algae, losing many of the ecosystem services previously provided. To avoid such phase-shifts, we need to increase the understanding of underlying processes governing the state of the habitat and their connectivity in the system as a whole. To date, the majority of studies

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have been conducted at relatively small spatial scales and in single habitats, limiting our ability to identify the potentially important interactions operating at a variety of scales including mobile links in a landscape context (Grober-Dunsmore et al. 2007). A number of organisms are known to move within the seascape, often crossing boundaries of habitat contributing to the energy-flux within the seascape system (Sheaves 2009). Fish form the greatest mobile link within the seascape and will be the focal organism investigated in this thesis.

Objectives and structure of thesis This thesis aims to increase the understanding of using a holistic view on the tropical seascape by acknowledging the importance of multiple scales, connectivity and the functional roles of species for seascape functioning. The thesis starts with a theoretical framework, introducing the topic and forming the basis for research questions. The results of the four papers are summarised and findings are then synthesised and generally discussed.

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Theoretical framework

Connectivity in the tropical seascape Connectivity in the tropical seascape can generally be divided into physico-chemical and biological interactions (Kathiresan & Alikunhi 2011). Examples of physico-chemical interactions are coral reefs protecting seagrass beds from wave action, creating a protective environment for seagrasses to thrive, and mangrove outwelling fuelling adjacent food webs through nutrient dispersal (Harborne et al. 2006). Biological interactions, on the other hand, are those of organisms moving and interacting between systems. Nowadays, the term ecological connectivity is common in the literature and encompasses both physico-chemical and biological interactions and particularly refers to the connectedness of ecological processes at multiple scales (Fischer & Lindenmayer 2007; Nagelkerken 2009). The majority of studies, which include all major habitats within the tropical seascape, have focused on adult and juvenile fish- and crustacean migrations operating at different temporal and spatial scales. Most studies, however, have only documented movements per se and not recognised the importance of movement for exchange of energy and matter, food-web ecology or ecosystem processes that are operating at the seascape level. Viewing connectivity in this context as connectedness of ecological processes (ecological connectivity) at multiple scales will be the type of connectivity addressed in this thesis.

Fish migrations Within the tropical seascape different types of fish migrations occur, including tidal, foraging, ontogenetic and spawning migrations, operating at different temporal and spatial scales. These migrations have consequences for the exchange of energy and food-web interactions across boundaries (Valentine et al. 2008). In many tropical regions shallow areas within the seascape are subjected to tides, excluding many marine organisms (particularly fishes) from mangrove

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and seagrass areas. Organisms are therefore forced to use alternative adjacent habitats during extended periods of time, resulting in tidal migrations (Sheaves 2005). Seagrass beds and mangroves are often used as foraging grounds by coral reef fish, transferring energy and nutrients from one habitat to another (Meyer et al. 1983, Fig. 1). Diurnally active herbivores forage in seagrass beds during daytime hours and migrate to the shelter of coral reefs at night (Tribble 1981; Maciá & Robinson 2005). Conversely, nocturnally active zoo-benthivores move from daytime resting areas on coral reefs or within mangroves to feed in seagrass beds and sand flats at night (Helfman et al. 1982; Verweij et al. 2006b). Some studies have compared day and night-time abundances (Rooker & Dennis 1991; Nagelkerken et al. 2000; Unsworth et al. 2007) while others have followed tagged individuals during foraging migrations (Meyer et al. 2000; Beets et al. 2003; Verweij & Nagelkerken 2007). Recent studies have examined stable isotopes in fish tissue to prove foraging between habitats (Nagelkerken & van der Velde 2004; Nagelkerken et al. 2008).

Seagrass beds and mangroves are suggested to function as nurseries for juvenile coral reef fish before undertaking ontogenetic migrations to coral reef habitats (Nagelkerken et al. 2001; Mumby et al. 2004, Fig. 1). Most young coral reef fish spend their first few weeks in the pelagic zone, settling when a suitable habitat is encountered (Sale 2004). Predation is believed to be particularly intense on coral reefs, especially on juvenile fishes. Furthermore, space and food are in limited supply on coral reefs, and hence nearby habitats such as mangroves and seagrass beds may provide recruiting juveniles with adequate food and shelter before they migrate to the coral reef (Parrish 1989). The majority of studies are descriptive, showing high densities of young reef fish in mangroves and seagrass beds, and generally lower total density of adult fish in the same habitats (e.g. Gillanders 1997; Nagelkerken & van der Velde 2001; Appeldoorn et al. 2003; Nakamura & Sano 2004; Dorenbosch et al. 2006). Others have found low densities or absence of adults of so-called nursery species on coral reefs where nursery habitats are very scarce or not present (e.g. Nagelkerken et al. 2002; Mumby et al. 2004; Dorenbosch et al. 2007). Experimental studies have shown that habitat complexity and/or food availability in mangroves and seagrass beds attract juvenile fishes (Cocheret de la Morinière et al. 2004; Verweij et al. 2006a).

Many species of fish conduct spawning migrations to areas that transport their pelagic eggs and larvae away from extensive predation (Claydon 2004). The favoured locations are often close to outer reef crests and slopes or channels leading through the reef (Johannes 1978). Most studies have focused on movement within the same focal habitat (most commonly coral reefs), ignoring movement between other

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habitats like seagrass/algal beds and mangroves, and only few studies have examined spawning migrations across the whole seascape including other habitats adjacent to coral reefs (Johannes 1978; Chaves & Bouchereau 2000).

Figure 1. Schematic illustration showing a) dial foraging migration between coral reef and seagrass habitats, and b) ontogenetic migration of juvenile coral reef fish between mangrove/seagrass and coral reef habitats. Image symbol courtesy of the Integration and Application Network, University of Maryland.

Ecological connectivity and seascape functioning Ecologists are nowadays aware that ecosystem dynamics are rarely confined within a focal area and that factors outside a system may substantially affect (and even dominate) local patterns and dynamics (Polis et al. 1997). Local populations are often linked closely with other populations, and the movement of nutrients and organisms (consumers and their prey) among habitats is often a central feature of population, consumer-resource, food-web and community dynamics (Polis et al. 1997; Forbes & Chase 2002). Despite this knowledge, very few studies have assessed connectivity of functional groups between shallow-water systems and their influence on community ecology. As connectivity between systems can be represented by mobile links (e.g. different groups of fish), and in turn represent trophic levels within a food chain,

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it is important to look at all trophic levels and estimate energy flow not based on one species or one group only. Each trophic level or functional group may provide or support several essential functions within and between areas. For example, parrotfish have an important role on coral reefs, feeding on competing algae, and in this way maintaining high coral cover and diversity (Bellwood et al. 2004). They also feed on seagrass leaves adjacent to coral reefs, altering and often stimulating seagrass communities (Eklöf et al. 2008); hence performing more than one function by foraging in two habitats. Furthermore, when moving from one habitat to another, energy is exchanged through excreta (Meyer & Schultz 1985), and yet another function is performed. The resilience of one habitat may therefore extend into, or be dependent of other habitats in its close proximity through the connectivity of functional groups (Nyström & Folke 2001).

Incorporating landscape ecology – a new approach A rapidly emerging field that holds great promise in ecological studies focusing on coastal seascapes is the application of landscape ecology to marine and coastal systems (Hinchey et al. 2008). Landscape ecology deals with mosaics of different habitats and how the composition and arrangement of these habitats affect species distribution and abundance in time and space (Turner 1989). It also deals with the effect of large-scale spatial patterns of habitats on ecological processes including competition, predation and the flow of energy (Turner 1989). The seascape is comprised of a mosaic of habitat patches (e.g. patches of mangrove, seagrass and coral reef habitat) and includes a variety of highly mobile species, making the application of landscape ecology ideal when studying movement of fish. As the arrangement of habitat patches within the seascape affects the direction of movement for a number of organisms and hence habitat connectivity, landscape parameters such as patch size, shape and context cannot be ignored.

The seascape can be viewed in a hierarchical landscape fashion (Pittman et al. 2004) by dividing the substratum structure into three levels/scales: (i) landscape mosaic structure, (ii) structure of individual habitat types, and (iii) within-patch structural variables (see Fig. 2). It is well-known that small-scale parameters like percent coral cover and seagrass structural complexity (within-patch parameters) can influence species abundance, distribution and diversity of many fish species. What is less known, however, is the influence of landscape parameters like habitat configuration, patch shape, patch size and edge-effect within level (i) and level (ii). Landscape parameters seem to be of great

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influence particularly in studies including migrating species and species with large home ranges.

Figure 2. Illustration of a hierarchical landscape approach showing habitat metrics at 3 levels (scales): (i) landscape mosaic scale, (ii) individual habitat scale, and (iii) within-patch scale. Modified from Pittman (2001) and Pittman et al. (2004).

The earliest application of landscape ecology in the marine environment was in the study of seagrass systems in the late 1960s and early 1970s. Scientists began to discuss seagrass patch arrangement as an attribute of the ecosystem and considered its role in seagrass functions and processes (Fonseca et al. 2006). However, it was not until the mid-1990s that Robbins and Bell (1994) directly addressed the application of using a landscape ecology approach when studying seagrass dynamics. In the late 1990s landscape ecology was applied to coral reef systems (Lindeman et al. 1998) and in early 2000, Nagelkerken et al. (2001) applied landscape ecology theory to reef fish connectivity when comparing fish fauna between bays with and without seagrass and mangrove habitat. Most studies have been conducted in the Caribbean and there is a great paucity of studies combing landscape ecology and fish connectivity in other parts of the world.

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Study region

The studies in this thesis were conducted between 2004 and 2010 around Unguja, the main island of the Zanzibar Archipelago, and Mafia Island, both situated in the Indian Ocean approximately 40 and 20 km from the Tanzanian mainland, respectively (Fig. 3). The marine environment of Unguja and Mafia Island is characterised by a mosaic of mangroves, seagrass beds, coral reefs, sandy beaches and muddy tidal flats, making it ideal for the studies in this thesis.

Figure 3. Map of study areas in East Africa, a) Mafia Island and b) Unguja Island (Zanzibar), Tanzania

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The seascapes are highly productive and provide important biological and economical resources for local communities (Francis et al. 2002), the most important resources being the catch from local fisheries (Jiddawi & Öhman 2002). More than 500 species are utilized for food, where most of the fish catch is used for subsistence purposes. A small fraction is exported overseas (Jiddawi & Öhman 2002). The shallow-water habitats of Unguja and Mafia Island are, however, increasingly subjected to a wide range of natural and anthropogenic disturbances, exacerbated by rapidly increasing populations and poverty (Francis et al. 2002). Management efforts have been initiated and a number of marine reserves and conservation areas were established during the 1990s including Menai Bay Conservation Area and Mafia Island Marine Park (MIMP) which are part of the study area in paper II and paper IV, respectively (Wood 2007). The whole of Unguja Island is represented in paper I while paper II focuses on Menai Bay, in the southwest part of Unguja and paper III focuses on a seagrass-dominated seascape in Chwaka Bay, east Unguja. Paper IV is conducted in Mafia Island, South of the Zanzibar Archipelago (Fig. 3).

Catching juvenile snappers in Mafia Island, Tanzania. Photo: Ian Bryceson

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Methods

In paper I, peer-reviewed literature was surveyed to provide an overview of the current knowledge of interlinkages and their effect on seascape functioning. Scientific data bases were searched using a combination of keywords. A study based on compiled data from Unguja Island (Zanzibar) was also conducted to fill some of the knowledge gaps identified in the literature survey. Peer-reviewed published and unpublished data from within the area and detailed data on juvenile abundance in mangrove and seagrass habitats obtained by contacting the authors of Gullström et al. (2008) and Mwandya et al. (2010) were examined. In these studies, juvenile fish in mangrove and seagrass areas were caught using a seine net (mangrove) with a mesh size of 1.9 cm and a beam trawl (seagrass) with an upstretched mesh size of 6 mm and a cod end of 1 mm. All coral reef fish surveys (published and unpublished data) were conducted between 2004 and 2009 on fringing coral reefs at 3 - 14m depth using 2 x 30m and 5 x 50m belt transects or by using a point census technique where all fish were recorded within a 5m radius during a 10 min period.

The point census technique was also used in paper II to estimate fish abundance and diversity in Menai Bay, Zanzibar in 2009. This paper examines the relationship between fish abundance/species richness and habitat variables such as distance to mangrove, connectivity and % coverage of seagrass and coral. Habitat data at different scales was obtained by estimating depth and percent seagrass cover within a 5m buffer zone of each fish point census and using aerial photographs to map habitat boundaries. Habitats were visited in the field for validation and mangrove areas were identified through aerial photographs and literature (Ngoile & Shunula 1992; Mease 2009; Saunders et al. 2010). A thematic habitat map was created in ArcGIS 10.0. and habitat classifications were created following that by Kendall et al. (2001). Seascape variables including distance and habitat cover (expressed as habitat connectivity) of major habitat types within different radii (250m, 500m, 750m, 1000m, 1500m and 2000m) around each sampled site were calculated using spatial analyst and geoprocessing tools in ArcGIS 10.0. Fishing activity was estimated by conducting semi-structured interviews with local fishers. Fishing

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activity was used in the analysis as the whole area is fished, supplying the local people with their main protein.

Paper III examines the spatial patterns of an important function (herbivory) within a seagrass-dominated seascape incorporating habitat variables from different scales. Fish data (abundance and biomass of the herbivore Leptoscarus vaigiensis) was collected November 2002 to January 2003 using the same beam trawl as in paper I. Seagrass structural complexity in terms of shoot density, shoot (above-ground) biomass and canopy height were estimated and used as predictor variables in regression analyses as well as describing study sites. Seagrass leaves were collected in order to measure the amount of epiphytes and physical environmental conditions such as water temperature, salinity and depth were recorded near the top of the seagrass canopy at the start and end positions of each fish sampling haul performed. Gut content analysis was carried out for 15 specimens of L. vaigiensis and in situ bite rates by L. vaigiensis on seagrass leaves were recorded during daytime hours using SCUBA.

Paper IV examines the connectivity between mangroves, seagrass beds and coral reefs by studying ontogenetic and diurnal feeing migrations in two species of fish, Lutjanus fulviflamma and Lutjanus ehrenbergii. Stable isotopes (δ15N and δ13C) in fish tissue, potential food items and primary producers from the different areas were examined. DNA analyses were also performed to assure correct species identification among the two very similar looking fish species. Juvenile fish samples of L. fulviflamma and L. ehrenbergii were collected during February/March 2010 and 2011, at low tide in mangrove and seagrass habitats using a modified mosquito net or small-scale fishing net. All adults and most subadults were purchased from local fishers. These were mainly caught in seagrass and coral reef habitats using traditional fishing methods, such as hook and line, small nets and intertidal fence nets. Fin clips from every caught specimen were stored in 95% alcohol for DNA analysis. A piece of flesh from the dorsal area (close to the tail) was removed from each individual fish for stable isotope analysis, placed in a vial and frozen. Samples were later dried in an oven at 60-70oC for 48-72h. The digestive tract including stomach and intestines was removed and placed in 95% alcohol. Potential food items (shrimps, crabs, and small fish) as well as other specimens (mangrove leaves, seagrass leaves, and algae) used as reference specimens for the isotope study, were collected in mangrove creeks, seagrass beds, and coral reefs. These were frozen and later dried in an oven at 60-70oC for 48-72h.

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General findings

Paper I Paper I sets the frame of this PhD by reviewing available information on seascape connectivity with an emphasis on mobile links of fish in the tropical seascape. Critical science gaps were identified and an in-depth literature survey was conducted to fill some of the gaps. The review showed that the majority of previous studies are from the Caribbean describing movements of single fish species. Few studies have quantified movement patterns or acknowledged them as important links of energy-exchange between systems. Even less has been done on the importance of mobile linkages for individual habitat functioning and on potential consequences of disrupted connectivity. Our in-depth study was conducted in the Western Indian Ocean and the results suggest that seascape habitats of this region may be equally connected as those in the Caribbean. Half of all fish species found within the Zanzibar seascape use more than one habitat. Furthermore, a large number of coral reef fish species (18%) were found in mangroves and seagrass beds as juveniles, suggesting that these habitats act as nursery areas for coral reef fishes. We incorporated the functional aspects of these species in terms of trophic level and discussed the implications of disrupted ontogenetic linkages and replenishment for coral reef functioning. We show that all functional groups of fish on coral reefs but two are represented among these species. Overall, half of all piscivores and about one third of fish/invertebrate feeders found on Zanzibar coral reefs use an alternative habitat as juveniles. Fifteen to 20 percent of invertebrate feeders, omnivores and herbivores also use mangrove and seagrass beds as juvenile habitat. Breakage of these ontogenetic pathways could have profound effects on trophic organisation, potentially cascading throughout the coral reef system.

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Paper II Paper II continues to take a holistic view of the seascape and examines connectivity of important fish functional groups within the Menai Bay seascape. It focuses on coral reefs and their connectivity with seagrass beds and mangroves. This paper uses a landscape ecology approach, trying to capture the important scales at which connectivity operates. As predicted, there was a positive relationship between seagrass connectivity (distance and area) and invertebrate feeder/piscivore abundance at the scale of 750m. When looking closer, the relationship was especially apparent for adults from the family Lutjanidae (snappers), known to perform feeding migrations from coral reefs to seagrass beds in the Caribbean. Contrary to predictions, however, there was a positive relationship between distance from mangrove and total fish species richness. Sites further away from mangrove areas had higher species richness. As predicted, the abundance of species known to use mangrove or seagrass beds as nursery habitat (identified in paper I) were higher in sites with large amounts (% cover) of seagrass within the fish point census (meter scale). Fishing activity was found to differ in Menai Bay, but landscape and within-patch variables were more important in influencing fish communities in this study. However, a positive relationship between fishing activity and parrotfish (Scaridae) abundance was found. Juvenile parrotfish had higher abundances in sites where fishing activity was high.

Paper III In contrast to Paper II, where the primary focus was on coral reefs and connectivity with other habitats (seagrass beds and mangroves), Paper III focuses on seagrass systems. This paper examines the spatial patterns of an important function (herbivory) within a seagrass-dominated seascape incorporating habitat variables from two hierarchical scales mentioned in the introduction; (i) the landscape mosaic scale and (iii) the within-patch scale (Fig. 2). Although the focus is on one habitat (seagrass beds), the influence of the proximity of other habitats (mangroves and coral reefs) and their associated predators are incorporated and discussed. We found that the parrotfish Leptoscarus vaigiensis was by far the most abundant herbivorous fish within our study sites. Almost 100 percent of its gut content consisted of seagrass and feeding observations revealed that individuals of L. vaigiensis fed at a constant rate of 7 bites per minute during each feeding spout. The abundance and biomass of L. vaigiensis differed between seagrass beds of different structural complexity and was greater in seagrass beds

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dominated by long-leaved Enhalus acoroides than those dominated by short-leaved Thalassia hemprichii. Multiple regression analysis revealed that seagrass shoot density explained 60-85 percent of the variability in juvenile and sub-adult density and that distance to coral reefs explained 87 percent of the variability in sub-adult biomass. Potential predators of L. vaigiensis were mainly reef-associated and followed a similar pattern to L. vaigiensis, being more common in seagrass beds dominated by E. acoroides compared to Thalassia-dominated beds. Canopy height explained 79-85 percent of the variability in predator density and biomass.

Paper IV In paper IV we focus on two important commercial fish species (L. fulviflamma and L. ehrenbergii) in East Africa and their connectivity and functional role in the tropical seascape. We examined stable isotopes (δ15N and δ13C) in fish tissue, potential prey items (crabs, shrimp, small fish) and primary producers within the different habitats (mangroves, seagrass beds, and coral reefs) in order to identify ontogenetic and feeding migrations in L. fulviflamma and L. ehrenbergii. Fish of all life stages were found to feed on crabs, small fish, and shrimps. However, the ratio of fish as feed increased with size and life stage in L. fulviflamma. L. fulviflamma and L. ehrenbergii overlapped in habitat use but differed slightly in feeding patterns indicating resource partitioning between the two species. The δ13C values of juvenile L. fulviflamma from mangrove creeks closely matched values of food items originating from corresponding habitats and differed from signatures in adult specimens from seagrass beds and/or coral reefs, indicating ontogenetic separation of habitat in this species. Adult L. fulviflamma from coral reefs displayed δ13C values closer to food items collected in seagrass beds indicating that feeding migrations from coral reefs to seagrass beds take place.

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General discussion

It is clear that information on ecological connectivity within the seascape is generally lacking (paper I), particularly information on trophic interactions across boundaries and their implication for seascape functioning. There is a great paucity of information on seascape connectivity in the Indo-Pacific, which led to the belief that fish migration between habitats is not of importance in this region (Quinn & Kojis 1985; Parrish 1989; Laroche et al. 1997). However, paper I and paper IV as well as other recent studies in the Indo-Pacific region (e.g. Dorenbosch et al. 2005; Lugendo et al. 2007; Gullström et al. 2008; Unsworth et al. 2008) have found that a large amount of coral reef fish species use mangroves and seagrass beds as juvenile habitat connecting shallow-water habitats within the tropical seascape through ontogenetic movement. In Zanzibar 18% of coral reef fish species use mangroves and seagrass beds as juvenile habitat (paper I) and disrupting connectivity between coral reefs and these habitats may therefore have implications for coral reef fish replenishment and ultimately fisheries production. Studies in the Caribbean have compared fish abundances in coral reef areas with and without mangroves (Mumby et al. 2004) and seagrass beds (Grober-Dunsmore et al. 2007) giving an indication of what might happen to fish communities if areas of mangrove and/or seagrass are lost. Both studies found that the abundance and biomass of coral reef fishes was lower in areas were mangrove and seagrass beds were absent. Breakage of ontogenetic linkages, due to habitat loss or fragmentation, could also have profound impacts on important processes on coral reefs, such as algal grazing and top-down control of prey species. Between 17-59% percent of invertebrate feeder/piscivore abundance on Zanzibar coral reefs use mangrove and/or seagrass as juvenile habitat (paper I). Breaking the ontogenetic pathway of these species could potentially lead to predator release of prey species (e.g. sea urchins, starfish and gastropods) that are destructive for coral reefs if found in high numbers (Carreiro-Silva & McClanahan 2001; Herrera-Escalante et al. 2005; Burkepile & Hay 2007; Pratchett et al. 2009). Seagrass beds and mangroves are also used as foraging grounds by many coral reef fish (paper I & paper IV, Maciá & Robinson 2005; Verweij et al. 2006b). Mangrove- and coral reef-associated invertebrate

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feeders/piscivores have been found in seagrass beds in close proximity to these habitats (paper II, paper III & paper IV, Gullström et al. 2008). In paper II we found higher abundances of invertebrate feeders/piscivores in areas with high seagrass connectivity within 750m, especially of adult snappers (Lutjanidae). This family has earlier been shown to perform both ontogenetic migrations and daily feeding migrations from coral reefs to seagrass beds in other parts of the world (Nakamura et al. 2008; Luo et al. 2009), which thus also seems to be the case in the Western Indian Ocean (paper I, paper II & paper IV). The consequences of these migrations are not well understood, but it seems that the presence of such migrating fish may have a strong influence on the distribution and abundance of prey species living in adjacent seagrass beds. Small fish were found in the guts of L. fulviflamma and L. ehrenbergii (paper IV), and fish as feed was increasing with size and life stage in L. fulviflamma. Predation by L. fulviflamma, L. ehrenbergii, and other piscivores could hence affect the distribution and abundance of their prey species. In a seagrass-dominated seascape in Chwaka Bay, Zanzibar, the abundance and distribution of the common herbivorous parrotfish Leptoscarus vaigiensis was found to differ between seagrass beds located at different distances from mangrove and coral reefs and in seagrass beds of different structural complexity (paper III). Shoot density (small scale) and distance to coral reef (large scale) were two factors found to explain the variability in density and biomass of juvenile and sub-adult L. vaigiensis (paper III). Potential predators of L. vaigiensis found in seagrass beds were mainly coral-reef associated and followed similar distribution patterns to L. vaigiensis. These results suggest that the potential predators may influence the abundance and distribution of L. vaigiensis. When comparing different seagrass beds, Leptoscarus vaigiensis seemed to prefer feeding on the short-leaved T. hemprichii plants (Gullström et al., unpublished data) while they were found in highest densities in beds composed of long-leaved E. acoroides (paper III). This indicates that L. vaigiensis may limit its distribution to E. acoroides beds due to predator avoidance by hiding in the taller seagrass canopy. This is supported by Heck & Orth (2005), who suggested that the height of the seagrass leaves and the degree to which they overlap can have an impact on the ability of down-looking predators to detect prey. Furthermore, Bartholomew et al. (2000) reasoned that spaces between seagrass shoots can impede predator movement if too narrow and hence provide protection in predator-prey encounters. A recent approach to the study of fish-habitat interactions at various scales is the application of landscape ecology. This approach was applied in paper II and paper III where connectivity and interactions at various scales were studied. The results show that a

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landscape ecology approach is applicable when studying ecological connectivity of fish. Especially since the seascape is comprised of a mosaic of habitat patches (e.g. patches of mangrove, seagrass and coral reef habitat) and includes a variety of highly mobile species. We did, however, find that the type of seascape and home range of study organism need to be acknowledged a priori designing the study to properly capture seascape effects on different fish species. Seascapes can be rather different in their composition of mangrove, seagrass and coral and the appropriate scale to use seems to be species- and life-stage specific (paper II, Grober-Dunsmore et al. 2007). Furthermore, the quality of the matrix (surrounding area between focal habitat patches) may have a large impact on the mobility of species and hence overall connectivity in the study area (paper II). Recent terrestrial studies have found that high quality matrix positively influences dispersal of insects between habitat fragments, and hence the functional connectivity of the landscape (Rundlöf et al. 2008; Öckinger et al. 2011). In paper II, scattered coral rock and sparse seagrass between sites seemed to function as high quality matrix compared to sand, which is usually experienced by fishes as a hostile environment due to lack of hiding places and hence increased predation. Finally, a third dimension (depth), departing from the two dimensional approach in terrestrial studies, needs to be considered in seascape ecology. Depth was found to have a strong influence on fish assemblages in paper II.

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31

Concluding remarks

The four studies conducted in this thesis confirm that ecological connectivity plays an important role within the tropical seascape and that connectivity by migrating fishes is a common feature in East African seascapes. It shows that factors affecting the abundance and distribution of species operate at multiple scales, and that trophic interactions occur across boundaries. Both small scale variables (habitat cover and structural complexity within habitats) and large scale (landscape) variables are of importance when studying the abundance and distribution of fish communities. Results also indicate that a landscape ecology approach is applicable and very useful when studying ecological connectivity and seascape dynamics. The functional roles of species involved in ecological connectivity have previously been ignored. This thesis, however, has made a first attempt to acknowledge the connectivity of functions and its consequences. An important next step is to identify thresholds at which ecological connectivity is reduced or completely broken. No such thresholds have been reported, although it has been suggested that species richness of coral reef fish may show considerable declines when surrounding seagrass coverage drops below 30%. This thesis did not find such a threshold; however, 750 m seems to be the scale at which seagrass connectivity is important in Menai Bay, Zanzibar.

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Acknowledgements

Firstly I would like to thank my supervisors Nils Kautsky, Martin Gullström, and Magnus Nyström for their guidance and support. A special thanks to my co-authors, Regina Lindborg and Micaela Hellström for all their great input. Thanks to my roommates throughout the years, Johan Näslund, Gustaf Lilliesköld Sjöö, Göran Samuelsson and Lena Konovalenko for keeping the spirit up with coffee, chocolate and the occasional beer. Big hugs to the rest of my colleagues and friends at the department, especially Matilda, Sara, and Siggi with whom I have had a great time during Zanzibar field trips and international conferences. Thank you, Ian Bryceson and Narriman Jiddawi for guidance in the field and big thanks to the rest of the staff at the Institute of Marine Sciences (IMS), Zanzibar and Mafia Island Marine Park (MIMP). Thank you Yussuf, Nahoda, Tove, and all my Master students (Esmeray, Sanja, Aurora, Linda, Maria and Sara) for all your help and good times in the field. Finally, big hugs and thanks to my family and loved ones. Daniel thanks for all your wonderful support! Funding from the Swedish International Development Cooperation Agency (Sida), Stockholm University Centre for Marine Research (SMF) and Wallenbergs Stiftelse has made this thesis possible.

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AbstractSammanfattningList of papersIntroductionTheoretical frameworkConnectivity in the tropical seascapeFish migrationsEcological connectivity and seascape functioningIncorporating landscape ecology – a new approach

Study regionMethodsGeneral findingsPaper IPaper IIPaper IIIPaper IV

General discussionConcluding remarksAcknowledgementsReferences