Managing sea cucumber fisheries and aquaculture: Studies of social-ecological systems in the Western Indian Ocean

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Managing sea cucumber fisheries and aquaculture

Studies of social-ecological systems in the Western Indian Ocean

Hampus Eriksson

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©Hampus Eriksson, Stockholm 2012 ISBN 978-91-7447-515-9

Printed in Sweden by US-AB, Stockholm 2012

Distributor: Department of Systems Ecology, Stockholm University Cover illustration by Hampus Eriksson

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Till mamma

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Abstract

Collecting sea cucumbers to supply the high value Chinese dried seafood market is a livelihood activity available to many people in the Western Indian Ocean (WIO), making it an important part of local economies. These fisheries are generally not successfully managed and tropical sea cucumber fisheries show continuing signs of decline. This thesis takes a social-ecological systems approach to guide better management of sea cucumber fisheries and aquacul- ture in the WIO. Papers 1 and 2 analyse the fishery situation in Zanzibar and find that in the absence of effective management institutions and income alternatives among fishers, leading to de- pendence, there are unsustainable expanding processes. Paper 3 compares the unmanaged fishery in Zanzibar to the highly con- trolled situation in Mayotte. In Mayotte, a protection effect is evi- dent and the commercial value of stocks is significantly higher than in Zanzibar. The analysis of the situation in Mayotte demonstrates the importance of matching the fishery – management temporal scales through prepared and adaptive management to avoid proc- esses that reinforce unsustainable expansion. Paper 4 analyses sea cucumber community spatial distribution patterns at a coastal sea- scape-scale in Mayotte establishing baseline patterns of habitat utilization and abundance, which can be used as reference in man- agement. Paper 5 reviews the potential for sea cucumber aquacul- ture in the WIO. The review illustrates that this activity, which is currently gaining momentum, does so based on inflated promises and with significant social-ecological risks. Emphasis for improve- ments is, in this thesis, placed on the importance of prepared and adaptive institutions to govern and control expanding processes of the fishery. These institutional features may be achieved by in- creasing the level of knowledge and participation in governance and by integration of sea cucumber resources management into higher-level policy initiatives.

Photo 1 The high value black teat- fish, Holothuria nobilis, on a reef flat in Mayotte.

Photo: Julien Wickel

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List of papers

1. Eriksson H, de la Torre-Castro M, Eklöf J, Jiddawi N (2010) Resource degradation of the sea cucumber fishery in Zanzibar, a need for management reform. Aquatic Living Resources 23: 387-398.

2. Eriksson H, de la Torre-Castro M, Olsson P (2012) Mobility, Expansion and Management of an East African Multi-species Scuba Diving Fishery. PLoS ONE 7(4): e35504.

3. Eriksson H, de la Torre-Castro M, Olsson P. Breaking degra- dation of sea cucumber resources: a social-ecological analysis of Zanzibar and Mayotte Islands in the Western Indian Ocean.

Manuscript

4. Eriksson H, Byrne M, de la Torre-Castro M (2012) Sea cu- cumber (Aspidochirotida) community, distribution and habitat utilization on the reefs of Mayotte, Western Indian Ocean. Marine Ecology Progress Series 452: 159-170.

5. Eriksson H, Robinson G, Slater M, Troell M (2012) Sea cu- cumber aquaculture in the Western Indian Ocean – challenges for sustainable livelihoods and stock improvement. AMBIO 41(2): 109- 121.

Articles are reprinted with the kind permission of the copyright

holders.

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Introduction

Humans’ insatiable desire for seafood

Fisheries resources have been utilized by humans for mil- lennia to satisfy the protein need of a growing and developing soci- ety - exemplifying humanity’s profound dependence on nature (Millennium Ecosystem Assessment (MA) 2005). During the twen- tieth century humans have rapidly transformed the biosphere to suit food and lifestyle needs (Crutzen 2002; Steffen et al. 2007) and marine ecosystems are no exception (Bellwood et al. 2004; Halpern et al. 2008; Scheffer et al. 2001). The craving for seafood by the planet’s growing population has resulted in widespread overfishing with consequent deterioration of marine ecosystems and their resil- ience (Hughes et al. 2005; Jackson et al. 2001). The decline of fish- eries resources has also driven a staggering increase in intensive aquaculture, often operating with environmental negative net ef- fects, to fill the gap from declining catches (Huitric et al. 2002;

Naylor et al. 2000). Aquaculture now provides more than half of all seafood consumed around the world (FAO 2010). Declining fisher- ies, degraded ecosystem resilience and intensive aquaculture is not only worrying for the species that humans exploit (photo 2) – but also for humans themselves, because the degradation is deteriorat- ing the resilience of bundles of ecosystem goods and services that human society depends on (Rockström et al. 2009). Despite the widespread impacts and patterns of decline there are also examples of recoveries, sustainable social-ecological interactions and large- scale governance transformations (Gelcich et al. 2010; Kittinger et al. 2011; Lotze et al. 2011). As human society continues to grow and develop in a rapidly changing world, understanding the trajec- tories to demise or sustainability in these systems is critical to sup- port a future trend of sustainable fisheries and aquaculture.

The rise and establishment of sea cucumber fisheries

Collecting and sun-drying sea cucumbers to produce

“bêche-de-mer”, the dried bodywall of the animal, for the Chinese

Photo 2 Clockwise from top left:

Fisherman in the South China Sea, Shark fins for sale in Hong Kong, freshwater crabs tied up alive for sale in Hong Kong, parrotfish spear- fished in Mayotte, shellfish for sale in Hong Kong, woman at fish market in Zanzi- bar. Photos: Ham- pus Eriksson

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dried seafood market started in the productive waters of the Asia Pacific over 300 years ago (MacKnight 1976; Conand 1990). The Chinese upper class society sought this product for its perceived health benefits and exclusive status (Lovatelli et al. 2004). The de- velopment of the trade followed the maritime exploration and ex- pansion at the time with trading agents inhabiting regional trade outposts channelling trade from distant areas to China (Conand 1989). Facilitated by the simple drying procedure required to con- serve the product, and the high commercial value, the trade with sea cucumbers expanded until the early 1900s, when the fishery declined and remained largely inactive during the world wars and Chinas marginalization in global trade (Conand 1989; Uthicke 2004). However, in the early 1960s the sea cucumber trade re- gained some of its importance and with reform of China’s foreign trade policy and integration into the world economy during the 1980s (Li 1997), the market for sea cucumber expanded rapidly into previously unfished regions (Conand 1999; Kinch et al. 2008;

Uthicke 2004).

Today it is estimated that over 3 million people around the world participate in different types of sea cucumber fisheries target- ing more than 60 species on all continents, predominantly to pro- duce bêche-de-mer for the Chinese dried seafood market (Purcell et al. 2011). In the tropics, sea cucumbers are generally sourced from near shore areas using simple collection methods such as gleaning or breath-hold diving, making this resource available to a wide segment of the fishing community. The fishery has historically driven remote village economies (Friedman and Gisawa 2008) and throughout its development it has provided means of income and activity in marginal and poor areas (Toral-Granda et al. 2008), and even helped stimulate societal recovery in disaster zones (Garofe and Tiroba 2007). Sea cucumbers are some of the world’s highest valued marine commodities and in some Pacific islands the export earnings from sea cucumbers have surpassed that of finfish and other marine resources (Purcell et al. 2011), illustrating the high value of the resource and importance to local economies.

Ecologically important but vulnerable to fishing

The sea cucumbers targeted in fisheries belong primarily to the aspidochirotid order (Conand and Byrne 1993), which are im- portant species in tropical ecosystem functioning (Birkeland 1989;

Uthicke 1999, 2000). These organisms have been described as

epibenthic “vacuum cleaners” (Samyn and Tallon 2005) feeding

mainly of detritus and bacteria embedded in the sediment (Bakus

1973; Moriarty 1982; Moriarty et al. 1982) (photo 3). This feeding

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activity indicates their role in nutrient cycling and the trophic flow in the food web as deposit feeding and bioturbating organisms (Crozier 1918; Magnion et al. 2004; Uthicke 1999, 2001). The presence of sea cucumbers has been shown to have a positive effect on growth on seagrass and benthic microalgae, predominantly from the nitrogenous waste from feeding (Uthicke 2001; Uthicke and Klumpp 1998; Wolkenhauer et al. 2010). Sea cucumbers also contribute to the CaCO

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budget on coral reefs through the dissolu- tion of calcareous sediment in the intestine (Schneider et al. 2011), thereby increasing ambient alkalinity and buffering the effects of anticipated ocean acidification in coral reefs. This demonstrates that these organisms influence nutrient dynamics and trophic in- teractions. Such species are critical in the structure and functioning of entire ecosystems (Chapin et al. 1997).

Sea cucumbers are vulnerable to overfishing because of their life-history and reproductive strategy. Many species targeted in the tropical fishery are broadcast spawners that release their gametes into the water column on an infrequent annual basis and processes associated to their recruitment and distribution are com- plex and under-researched (Bell et al. 2008; Conand 1993; Gau- dron et al 2008) (photo 4). This reproductive strategy also brings a vulnerability to reduced fertilization success when there are low densities of breeding adults in the environment, known as the Allee effect (Petersen and Levitan 2001), a poorly understood threshold that can prevent recovery of harvested sea cucumber populations (Friedman et al. 2011; Uthicke et al. 2009).

Photo 3 Pear- sonathuria graeffei with its flower-like tenta- cles feeding off organic material on coral rubble. Photo:

Hampus Eriksson

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Increasing attention to a resource under pressure

Sea cucumbers as fisheries and aquaculture resources have received an increasing research and management attention during the past decade. Much of this work has been driven by interna- tional organisations such as FAO (Lovatelli et al. 2004; Purcell 2010; Toral-Granda et al. 2008). Fisheries and management trends have also been analysed and disseminated through large-scale re- views of fisheries published in peer-review literature (Andersson et al. 2011; Friedman et al. 2011; Purcell et al. 2011). This work has greatly increased the level of understanding on the issue of manag- ing sea cucumber resources. However, despite this positive research trend existing institutions (local and global) have generally failed to prevent destructive fishing processes, which have resulted in a prevalent boom-and-bust fishing pattern (Andersson et al. 2011;

Lovatelli et al. 2004; Toral-Granda et al. 2008). Purcell et al. (2011) found that nearly 75 % of global fisheries are fully exploited, over exploited or depleted. This current global situation has raised con- cerns about extinctions and species are evaluated for red listing by IUCN (Polodoro et al. 2011), and for trade restrictions under the Convention of Trade with Endangered Species (CITES) (Bruckner et al. 2006; Conand 2004). Sea cucumber aquaculture has arisen (figure 1), in this context, as a solution for sustainable management to reduce fishing pressure and replenish stocks (Conand 2008).

Photo 4 Spawning Stichopus herrmanni at One Tree Reef in Australia. Photo:

Hampus Eriksson

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Sea cucumber fisheries in the Western Indian Ocean

During the past decade a third of global sea cucumber fish- ery volume has come from the WIO (Conand 2008) (photo 5). Sea cucumber fisheries in the region solely supply export markets and do not directly contribute to protein intake among fishers (Conand and Muthiga 2007). To raise the level of knowledge a regional inter-disciplinary marine science for management (MASMA) research project was initiated funded by the Western Indian Ocean Marine Science Association, WIOMSA (Conand et al. 2006; de la Torre-Castro et al. 2007). The regional review of the commercial sea cucumber fishery by Conand and Muthiga (2007) was the first concerted output from this project, illustrating that many countries in the region (e.g. Kenya, Tanzania, Madagascar, and Seychelles) are reporting declining trends and insufficient management. In addition, in the latest global FAO review of the fishery, Conand (2008) lists more countries in the WIO (e.g. Somalia, Comoros, and Mozambique), as well as African countries in the Red Sea (e.g.

Egypt and Eritrea), and other areas in the Indian Ocean (e.g. Sri Lanka, India, and Maldives) where the fishery is showing signs of uncontrolled harvests and depletion. Muthiga et al. (2010) summarize the trends in the WIO: (1) catches have declined by 40 - 80 %, (2) low commercial species abundance, (3) fishers signal declining trends, (4) fishing trips have become longer, and (5) sexually immature individuals and low commercial value species are commonly harvested. Despite the recent focus of research on this resource and fishery, large knowledge gaps remain regarding sea cucumber ecology, social aspects and management in the region. The research presented in this thesis takes this situation as a baseline to extend the MASMA project with in-depth case studies in Zanzibar (Tanzania) and Mayotte (France), as well as a regional review of sea cucumber aquaculture in the WIO.

Figure 1 World aquaculture production of the sea cucumber Aposti- chopus japonicus.

Figure from paper 3 in this thesis.

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Scope of thesis

Problem statement and thesis aim

Sea cucumber fisheries in the WIO are generally not suc- cessfully managed, partially due to a lack of key ecological and socioeconomic information (Conand et al. 2006; de la Torre- Castro et al. 2007). In order to pursue sustainable use of sea cu- cumber resources the management discussion therefore requires a systems perspective on aspects relating to both ecological and social processes surrounding the fishery. The current lack of knowledge relating to these aspects inhibits the development of relevant man- agement institutions. The aim of the thesis is to increase social- ecological knowledge of sea cucumber fisheries and aquaculture to guide better management.

Analytical framework and research objectives

Fisheries management systems in general have been rigid and largely unable to cope with the uncertainty that comes with a limited understanding of ecosystems (Hughes et al. 2005; Kinzig et al. 2003), implicitly treating natural and social systems independ- ently (Folke et al. 2002), often with a simplified view of “fisheries”

(Castilla and Defeo 2005). Integrated in the process of moving away from this discourse has been making the explicit link to the human dimension and how human activities are embedded in the ecosystem (Castilla 1999; Folke et al. 1996; Folke et al. 2002). The linking of social processes to ecosystem management has formed the social-ecological systems approach and facilitated analysis of complex interactions between society and environment (e.g. Berkes et al. 2003; Berkes and Folke 1998). The social-ecological systems framework recognises that ecosystems are complex adaptive sys- tems that influence, and are influenced by, social processes (Levin 1998; Scheffer et al. 2001). This thesis builds on the theoretical foundation that resource users and resources are linked through reciprocal feedbacks. The objectives of the thesis are to:

Photo 5 Fisher- man in Zanzibar preparing sea cucumbers for boiling and drying to produce bêche- de-mer. Photo:

Hampus Eriksson

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1. Identify sea cucumber fisheries patterns and the resource status 2. Analyse existing sea cucumber fisheries management

3. Understand processes that influence the fishery system 4. Reduce knowledge gaps in ecology of target species 5. Analyse sea cucumber aquaculture as an alternative 6. Propose management improvements

Addressing the objectives

This thesis contributes with a novel systems approach to

the utilisation of sea cucumbers through fisheries and aquaculture

in the WIO and analyses the linked social-ecological system. The

fishery in Zanzibar was the initial focal fishery and the research

there strived to understand the patterns of the fishery and analyse

the underlying processes that they result from. This research,

which includes direct in-water visual census of stocks, analysis of

fishery management and patterns in exploitation, is published in

paper 1 and paper 2. The results from the first part of the research

provide a baseline of understanding to formulate a description of

the situation. To move understanding forward on how to improve

the situation, the next part of the research focussed on the island of

Mayotte, as it is one of the few large reef systems in the region pro-

tected from commercial fishing. Mayotte provided an ecological

reference and a governance example where lessons can potentially

be learnt. The third paper presented in this thesis, paper 3, is a

comparative study of the situations in Zanzibar and Mayotte that

investigate the two contrasting fishery contexts for improved sea

cucumber fisheries management. The in-water survey of commer-

cial sea cucumbers in Mayotte, published in paper 4, reveal whole

community distribution patterns and habitat utilisation of commer-

cial sea cucumbers in this protected reef system. In the context of

previous research the final study reviews how sea cucumber aquac-

ulture, which is currently gaining momentum with big expectations

in the region, fits into the context of this fishery. This is presented

in paper 5, which analyses social-ecological problems and potentials

of sea cucumber aquaculture in the WIO.

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Study area and methods

Study area

The research in this thesis is geographically centred in the WIO and data was collected in Zanzibar (Unguja Island) and in Mayotte (figure 2). These two locations provide contrasting sea cucumber fishery situations. Zanzibar is a Tanzanian island that has active and insufficiently managed collection activities for sea cucumbers, while Mayotte is French and experienced a period of fishing from the mid 1990s but the fishery was closed in 2004.

On-land study

To build understanding on fishery and management pat- terns for papers 1-3 and 5 data was collected using document analy- sis, participant observations and interviews. Documents used for analysis include peer-review literature, public documents and re- ports collected from authorities and agencies in Zanzibar and Mayotte. The interview component included in-depth interviews (Kwale 1998; Denscombe 2004) with resource users and managers.

Semi-structured questionnaires with closed and open-ended ques- tions that allowed for quantitative analysis were also used. The interview component also included focus group interviews, which

Figure 2 A) Map over the study area in the western Indian Ocean, B) map over Zanzibar and, C) map over Mayotte. Dotted lines are areas in the water where sea cucumber stocks were surveyed.

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were interactive and open discussion meetings (Bunce et al. 2008), which supports a more qualitative analysis based on the shared experiences of the participants. Similarly, participant observations were used to build understanding on resource users’ interaction and organisation.

In-water study

The studies in this thesis that contain a stock appraisal component (Papers 1-4) rely on visual census methods for commer- cial sea cucumber stocks (photo 6). Predominantly sea cucumber abundance and habitat data has been collected using the manta tow method as detailed in English et al. (2003). This is an appro- priate method for surveying larger conspicuous immotile resources or features in shallow (<10 m) waters and is commonly employed in commercial sea cucumber appraisals (Uthicke et al. 2004; Pur- cell et al. 2009; Friedman et al. 2011) as it covers large areas and is thereby suitable to locate the often-patchy distributed sea cucum- bers. Manta tow units in this research were 300 x 2 meter as sug- gested by Friedman et al. (2011). Census data was also collected using smaller scale targeted transects covering an area of 40 x 1 m in Paper 1. This method is particularly appropriate to use in benthic areas that are not suitable to survey with manta tows, such as shal- low reef flats or soft benthic lagoon areas, which may be difficult to access due to shallow waters or poor visibility. This method also complements the coarser manta tow as it allows the surveyor to dig and turn over rocks to find cryptic or burying species.

Photo 6 Pearsonathu- ria graeffei that have moved across a transect line during survey in Ilot Mbouzi in Mayotte.

Photo: Julien Wickel

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Synthesis of results | Meeting the objectives

Objective 1. Identify sea cucumber fisheries patterns and the resource status

Around 1000 people were estimated to regularly collect sea cucumbers in Zanzibar (Paper 1). The fishers’ catch consisted of over 90 % low value species, or species that had recently become com- mercialized, indicating how the fishery had progressed from target- ing high value species to those less valuable, a certain sign of over- fishing (Friedman et al. 2011). The fishery in Mayotte operated at a much smaller scale with approximately 100 fishers targeting pre- mium value species (Paper 3). Commercial sea cucumbers were only recorded in less than half of the 600 m

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manta tows in Zanzibar (Paper 1). Notably, out of those sea cucumbers that were observed only 7 % were of medium or high commercial value. This was con- siderably lower than what was recorded in Mayotte where 69 % of sea cucumbers were of medium and high commercial value (Paper 3).

In Mayotte the mean commercial value of the sea cucumbers in each sample station was 65.7 USD, while the corresponding value was 2.2 USD in Zanzibar. In an analysis where commercial value was set as a response variable against a number of habitat variables and the location (Mayotte or Zanzibar) the commercial value was independent of the sampled habitat. Instead, the location was de- terminant, supporting the argument that the protection effect in Mayotte was considerable (Paper 3). The population densities in Zanzibar infer that the self-replenishment of populations there was compromised. A protection effect could be noted in Chumbe Coral Park, but considering the large spatial scale of the fishery and the minute size of the park (300 m x 1100 m), it is unlikely that this area provides demographic connectivity (i.e. Steneck et al. 2009) with adequate supply of recruits to surrounding fishing grounds.

There were many types of resource users employing differ-

ent methods to collect sea cucumbers in Zanzibar. Women and

children collected sea cucumbers in the intertidal zone, while men

ventured further afield using boats and diving to deeper areas by

free-diving or by using scuba equipment (Paper 1,2) (photo 7). The

progression to new technology and high effort methods was em-

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ployed as a response to declining trends in catch. The scuba diving fishers were organised in teams that travelled in a roving manner to fishing grounds around Zanzibar, but also to other costal areas around the region, evading management and control through their mobility (Paper 2). These fishers also targeted other species such as lobster, gastropods and finfish using illegal spearguns, to compen- sate for declining catch value of sea cucumbers. This type of ex- pansion and progression in fishery methods was not noted in Mayotte.

Similar to the historical days of this fishery (Schwertner- Mañes and Ferse 2010), Chinese exporters steered these enterprises and often provided the necessary equipment for the scuba diving fishers. The exporters maintained a trade network where fishers from other parts of the region travelled to Zanzibar to sell their catch, for example from Tanzania where the fishery is illegal. The scuba divers were obliged to continue fishing for the equipment that they rented on credit, consequently losing their independence and trapping them in this dangerous activity. The illustrated fishery situations in Zanzibar and Mayotte have diverse management re- quirements and complement the broad view of a “sea cucumber fishery” used to prescribe management tools. The studies in Zanzi- bar identified how roving dynamics in fisheries, which have been predominantly addressed on a global scale, also take place at a considerably smaller spatial scale. The progression in fishing meth- ods in Zanzibar captures how increasing and expanding processes has been the response to declines in resource abundance and value.

The expansion in Zanzibar was driven by dependence and influ- enced by declining stocks and insufficient management (Paper 1-3).

While reformed local management may suffice for improving the situation of the artisanal segment of the fishery (Paper 1), aspects of greater spatial scales and different actors must be considered for the scuba diving segment (Paper 2).

Photo 7 Women gleaning in the intertidal and scuba diving men returning from fishing trip. The two photos illus- trate two activities with different management requirements.

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Objective 2. Analyse existing sea cucumber fisheries management

The sea cucumber fishery in Zanzibar lacked specific man- agement-plans, but had a size limit of 10 cm across the range of species (Paper 1). Firstly, this illustrated an ecological mismatch in management, as this is smaller than the known sizes of sexual matur- ity for any commercial species (Conand 1993). Secondly, this restric- tion was only known by half of the managers and by two out of 72 fishers that were interviewed. In addition, the fishery was not moni- tored so it was de facto operating without regulation or control. This situation indicated that knowledge about the fishery and resource was lacking, that there were no learning mechanisms in place for adaptive management responses and that cross-level communication flows (fisher to manager) were inadequate. Weaknesses in communi- cation flows undermine adaptive institutions through the absence of feedback from monitoring (Berkes and Folke 1998). This type of limitation exists in Zanzibar because the monitoring agents respon- sible for data-collection are influenced by dilemmas (i.e. kinship, loyalty, poverty and control) in their operation, which interferes with performance of institutions (de la Torre-Castro 2006). In the case of the sea cucumber fishery in Zanzibar, the monitoring agents did not systematically monitor the fishery, which prevented feedback for adaptive management. In addition, the flows of information through social networks between managers and resource users influences institutional dynamics and consequently also conduct (de la Torre- Castro and Lindström 2010). These types of networks of communi- cation can provide avenues for exchange of opinions and knowledge, which has been illustrated as important in positive governance out- comes (Gelchich et al. 2010), and that was also found to be impor- tant for management to transpire in Mayotte (Paper 3).

While the situation in Zanzibar exemplified weak man- agement and a deteriorated fishery, the fishery in Mayotte had followed a different trajectory – one of adaptive management and a persisting high-value resource base (Paper 3). Populations of com- mercial high-value sea cucumber species matched published refer- ence values of “natural” populations (i.e. Kinch et al. 2008), indi- cating that stocks had recovered from previous fishing. Though management in Zanzibar had failed to collect and evaluate infor- mation about the fishery, in Mayotte mechanisms to learn were in place. These mechanisms empowered the people within authorities to vision and to engage learning mechanisms. The authorities em- ployed stock appraisals, benchmarked against other fisheries, and considered the long-term ecological importance of the resource to formulate decision-making material for the management of the fishery.

The lack of knowledge was a critical factor in the studied

system – it was a barrier for informed management decisions and

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gauging effects of the fishery and aquaculture. In fact, the lack of knowledge can be perceived as both a source of erroneous action and as an inhibitor of action. For example, the ecological mismatch in size restriction of the fishery in Zanzibar exemplifies an inaccu- rate decision. At an institutional level, the lack of knowledge about the operation of the fishery in Zanzibar was also a barrier to mak- ing decisions and arranging decision-making at spatial scales rele- vant to the scuba diving fishery. The comparison of the fisheries in Zanzibar and Mayotte demonstrated the effect of matching fishery – management temporal scale with prepared and adaptive institu- tions to “keep up” with the fishery’s development (Paper 3). The importance of timely management was also emphasised in Galapa- gos by Shepperd et al. (2004) because the lack of control led fishers into high dependence on the resource to pay off loans on fishing vessels. This situation led later management interventions to con- flicts – illustrating how it is more difficult to “catch up” as that in- volves breaking processes that are reinforcing the current unsus- tainable situation. In Mayotte this situation was avoided by adap- tive and pro-active intervention. Additionally, there was a govern- ance landscape where visioning and opinions of what ought to be could transpire into management institutions. The comparison of these two contrasting situations illustrates the importance of authorities with capacity to monitor and control fisheries and trade with sea cucumber resources (Purcell et al. 2011).

Objective 3. Understand processes that influence the fishery system

From the research presented in Paper 1-3, a conceptual

model of how the fishery operates – towards sustainability or demise

has been developed (figure 3). This models hinges on the concept of

poverty traps (Jentoft and Midré 2011) and associated social-

ecological traps (Steneck 2009; Cinner 2011), whereby resource

dependence drives higher fishing pressure as a response to declining

resource abundance or catch value. The model also incorporates the

role of management institutions in governing fishers’ conduct. The

unsustainable fishery situation in Zanzibar was reinforced by the

mechanism where expanding fishery processes were developed, in

the context of insufficient management and dependence, in response

to a declining resource base (figure 3A). In contrast, there was adap-

tive management and less dependence in Mayotte, which prevented

expanding and unsustainable reinforcing processes (figure 3B). From

the studies in Zanzibar and Mayotte it appears logical that the large

differences in abundance and coverage of species have different eco-

system effects; however, these potential ecosystem effects have not

yet been quantified. Mechanisms to avoid or break self-reinforcing

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traps involve predominantly the management and social context elements (shaded boxes in figure 3), which influence the conduct of fishers in the model. For example, this may be achieved by increas- ing knowledge about the ecology of the resource and the fishery operation, implementing adaptive management and decreasing de- pendence.

Objective 4. Reduce knowledge gaps in ecology of target species

There is a clear mismatch in the rate of the fishery’s ex- pansion and the rate at which knowledge is gained. Case in point is that species only recently described to science (Actinopyga capillata) (Rowe and Massin 2008) or still without a taxonomic description (Holothuria sp. “pentard”) (Conand 2008) are target species (Paper 1).

Studies on these species ecology are consequently also missing and so formulating management that is ecologically relevant is very difficult, and so is gauging the impact of their removal. In this con- text, paper 4 was one of the first whole community studies in a pro-

Figure 3 A) Fishery situation in Zanzibar, driven by high dependence and lack of alternatives, where increasing fishing pressure was used as a response to declining catch value in the context of weak management. B) Fishery situation in Mayotte where adaptive management intervened prior to resource value declines thereby pre- venting increasing expanding responses and high dependence.

The two situations have different, but so far not quantified, effects on ecosystems.

Figure from paper 3.

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tected reef system and contributed with patterns of spatial distribu- tion and habitat utilization. The sea cucumber community in Mayotte was largely similar between five surveyed areas and three habitats. While this similarity was driven by species that were ubiquitous throughout the coastal seascape other species were unique to areas or habitats. These rare species are evidently prone to over-exploitation and should be exempt from harvesting, not only to preserve diversity, but also due to the difficulty in monitor- ing them. The distribution of species was associated to the presence of a number of habitat variables (e.g. substrate type and abiotic variables such as depth). Consequently, the spatial distribution patterns can likely be attributed to the heterogeneous mosaic of habitats encountered within the coastal seascape.

Although sea cucumber communities were largely similar

between areas and habitats, differences in number of species were

noted (Paper 4). For example, in the outside barrier reef area 8 spe-

cies were recorded, compared to 12 in the inside barrier reef and

11 in fringing reefs. Similar patterns were also evident between the

surveyed areas, where one area was less diverse (6 species) than

others (7-10 species). The diversity of species was not correlated to

habitat complexity. Instead complexity as a habitat variable only

partially explained the distribution of two species, Thelenota ananas

and Holothuria fuscopunctata, but for most species other habitat vari-

ables were important drivers of distribution. Importantly, the asso-

ciation to habitat variables provides baseline information that al-

lows for predictions about what can be expected from certain habi-

tats in terms of presence of species and their abundance. For ex-

ample, appraisals can lean onto expected abundances of a species

when sampled within a habitat. This type of information can con-

tribute to spatial planning in ecosystem-based management, de-

signing surveys and improve the scope to further study ecological

processes that determine these patterns. Importantly, this study

exemplifies that ecological patterns relevant to the fishery can be

established through relatively rapid appraisal methods suitable for

management teams with limited resources, which can feed into

learning-mechanisms in management, as outlined in the fishery

model (figure 3). However, the processes that determine the pat-

terns are under-researched and the lack of understanding on life-

history and habitat utilization across stages of life-history greatly

limits the ability to implement ecosystem based management, as

prescribed by Purcell (2010), and to gauge the ability of species to

cope with fishing.

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Objective 5. Analyse sea cucumber aquaculture as an alternative

Sea cucumber aquaculture proposals appeal to political agendas of economic growth and employment, and to NGOs am- bitions of supporting village economies through the creation of an alternative livelihood (Robinson and Pascal 2012), but they fail to acknowledge or address the knowledge gaps associated with pro- posed farming systems. For example, the review in this thesis (Paper 5) identified that there is no research gauging the impact sea cu- cumber farms will have on resident benthic communities through competition for space and resources or how this will affect the flow of ecosystem goods and services from habitats where farming oc- curs. Similarly, there is a paucity of information relating to genetic integrity of wild populations, or the likelihood of disease outbreaks among densely farmed sandfish, which is of particular concern when grow out takes place in the natural environment. Impor- tantly, there has also been a lack of systems analysis on how farms will be integrated into coastal communities and how they should be governed.

The intuitive assumption that new and diverse economic

activities will alleviate pressure on fishing resources and deliver

alternative sources of income may, contrary to the objective, in-

crease pressure on fishing resources. This has been demonstrated

in seaweed farming in Asia Pacific where profits on occasions have

been used to re-invest in fisheries (Sievanen et al. 2005). That ac-

tivities are often perceived as complements, not replacements, illus-

trates the commonly employed strategy of diversification in fishing

communities to multiply income options in periods of uncertainty

(Allison and Ellis 2001; Andersson and Ngazi 1998). It can there-

fore not be taken for granted that sea cucumber aquaculture will

decrease dependence and influence the conduct of fishers in the

manner required to break reinforcing processes in the fishery

model (figure 3). Nevertheless, farming has the potential to provide

an added source of social resilience as an alternative economic

activity (Allison and Ellis 2001). Unfortunately the discussion has

been one-sided focussing on improving the technical aspects of

farming (e.g. Agudo 2006; Battaglene et al. 2002) and with less

emphasis on the social-ecological context (Paper 5). Taking on a

social-ecological systems approach, and placing farming in the

context of the operating fishery, balances the discussion and pro-

vides reference for decision-making in regard to farming enter-

prises. Until critical evaluation of existing farming enterprises has

been conducted a precautionary approach to sea cucumber aquac-

ulture in the WIO is recommended.

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Objective 6. Propose management improvements

1. Prepared and adaptive institutions – “keep up or catch up”.

Management systems, or management reforms, have to suit indi- vidual contexts taking into account resource users, mode of opera- tion (methods), target species, and target habitats. Recent prag- matic output has provided vital directions to assess and manage sea cucumber fisheries (Friedman et al. 2008; Purcell 2010). These toolbox-style references are helpful for guiding appraisals and de- velopment of appropriate tools in management. Management that does not keep up with the development of the fishery runs the risk of loosing control and attempting to govern much more complex and reinforcing processes to catch up. Keeping up with fishery activities requires adaptive management systems that can influence fishing activities through timely and appropriate action upon feed- back. Management plans should therefore strive to enhance adap- tive decision-making through governance systems building on so- cial networks and vertical (fisher – manager) reciprocal information flows, as this improves knowledge and builds social capital. These aspects can perhaps be positively influenced through co- management schemes or fishery cooperatives that increase equity and incentives in the resource management and decision-making.

Such activities are underway in Vanuatu, where community pro- grammes that supports incentives and stewardship to rebuild stocks of commercial sea cucumbers have been initiated (Pakoa 2011).

This can provide valuable reference for similar efforts elsewhere and shows that it is important to look outside the region to learn at large spatial scales.

2. Increase knowledge and awareness to support cooperative govern- ance. A critical element to improving the preparedness and adapt- ability of management institutions is raising the level of knowledge and awareness of all stakeholders. This will require an increased level of participation in the governance of the fishery, at multiple levels, to increase vertical flows of information and social networks to facilitate collective learning and decision-making at appropriate scales. Pragmatic developments should focus on regional dialog and support network because while there may be limited informa- tion available in countries, information can be gleaned and utilized through sharing of experiences and information. This can allow individuals that have the ability to influence management institu- tions to learn from mistakes or successes in other fisheries. In No- vember 2012, a sea cucumber fishery’s manager’s workshop will be held in Zanzibar. This workshop follows a template from a work- shop held in Fiji 2011 (Purcell and Lovatelli 2012) and aims to provide an arena for exchange of experiences to analyse govern- ance systems and raising the level of knowledge among managers.

Photo 8 Beche-de- mer that have been smoked over mangrove wood in Zan- zibar are taken out for final sun drying to produce export- ready product.

Photo: Hampus Eriksson

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3. Integration of fishery management into larger scale or higher-level management initiatives. Sea cucumber resources have the potential to strongly influence coastal economies in the WIO; therefore their management should be better integrated into other development and conservation policies (e.g. climate change adaptation, poverty alleviation). Increased attention at an interdisciplinary policy level might increase the ability to mobilize resources needed, through greater access to agendas on international arenas, to strengthen the capacity of organizations and to support appraisals and adaptive reforms in management. It may also allow for new angles on re- search and pragmatic activities to support reforms so that profits to a higher extent are captured at a fisher-level, thereby contributing to peoples’ economies to its full potential (photo 8, 9). Economic alternatives aimed towards shifting effort away from the fishery, such as sea cucumber aquaculture, should be integrated in reforms rather than an isolated an activity.

Photo 9 Two middlemen in Mazizni holding up today’s best catch, the high value Holothuria lessoni Photo:

Hampus Eriksson

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Future research direction

A major research challenge for the future is to extend the systems perspective to focus on global governance by including international trade networks and the recipient market in Asia.

There is surprisingly little research in peer review literature regard- ing the institutions that govern the import trade of dried seafood to Hong Kong. Similarly, very little work (if any) has been done focus- ing on the consumers and their attitudes or perceptions. The lack of access to information is a significant barrier towards understand- ing the role that recipient markets and consumers play in the gov- ernance of global fisheries systems in general. Future research should also focus on how sea cucumber resources can better profit the fishing communities. Such research should take gender aspects into account, as research in this thesis has indicated that there are major discrepancies in commercial value when men or women trade with sea cucumbers.

The lack of biological and taxonomic data not only limits fisheries management but also efforts to control trade at multiple scales including limitations to the Convention of International Trade of Endangered Species (CITES) protection of appropriate species. Therefore, resources to obtain taxonomic stability are ur- gently required, as is research on how global governance tools such as CITES can impact the trade in a positive way considering the limited governance capacity of many harvesting nations. Finally, better understanding the ecological effect of fishing is required to estimate the ecological contribution to overall social-ecological resilience. Integrated in this research agenda should be the im- proved understanding of life-history of organisms to gauge their ability to cope with fishing – and recover from overfishing.

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Sammanfattning på svenska

Sjögurkor utgör en viktig inkomstkälla för många kustnära samhällen i tropikerna. Dessa djur kokas och torkas för export till den kinesiska marknaden som en av de högst värderade fiskeripro- dukterna i världen. Det höga värdet, att de är lätta att samla, och den relativt enkla förädlings- och konserveringsmetoden gör den till en unik resurs som är viktig för lokala ekonomier i områden där tillgång på andra inkomstalternativ är begränsade. Tyvärr tillåter inte sjögurkornas biologi ett högt fisketryck och bestånden av sjö- gurkor är idag mycket dåliga i de länder där fiske förekommer.

Avhandlingen har en systemekologisk vinkling och innehåller fem studier av sociala och ekologiska mönster och processer i resursut- nyttjandet. Forskningen syftar till att bättre förstå och kunna styra förvaltningen av fiske och vattenbruk av sjögurkor i västra Indiska Oceanen.

Studie 1 och 2 analyserar fisket i Zanzibar, Tanzania. Stu- dierna visar att bestånden av sjögurkor är kraftigt överfiskade. Ut- vecklingen har gått från utfiskning av de grunt förekommande ar- terna till en ökad fiskeansträngning med båt och dykning för att exploatera arter som förekommer längre bort och på större djup.

Denna utveckling har kunnat ske p g a bristande förvaltning och

avsaknad av inkomstalternativ bland fiskare. Eftersom dessa pro-

cesser är självförstärkande (ökande fisketryck leder till sämre fångs-

ter som i sin tur leder till ökande fisketryck) hamnar vi i en negativ

spiral som är svår att bryta och förvalta. Studie 3 jämför det oregle-

rade fisket i Zanzibar med den betydligt mer kontrollerade situa-

tionen runt den franska ön Mayotte. Jämförelsen visar att bestån-

den i Mayotte har ett nästan 30 gånger högre kommersiellt värde

än bestånden i Zanzibar. Analysen av situationen i Mayotte visar

på vikten av att matcha tidsskalan för fiskeutveckling och förvalt-

ning genom att fatta adaptiva beslut grundade på kunskap. Denna

kunskap uppnås lämpligen genom systematisk övervakning av fisket

från myndigheters sida och genom direkt informationsutbyte mel-

lan fiskare och förvaltare. Förberedda och adaptiva förvaltningsin-

stitutioner kan förhindra uppkomsten av expansiva och destruktiva

processer som fångar fisket i den negativa spiral som fisket i Zanzi-

bar befinner sig i. Studie 4 kartlägger utbredningen av kommersiella

arter av sjögurkor i de skyddade bestånden i Mayotte. Studien visar

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på komplexa ekologiska mönster. På en stor skala (mellan korallrev) så är bestånden relativt lika. På en mindre skala (inom korallrev) så finns det stora skillnader i mångfald och täthet, vilka styrs av miljö- faktorer. Studien ger viktiga referenser för hur skyddade bestånd ser ut och bidrar med information till en ekosystem-baserad för- valtning. Studie 5 analyserar odling som ett alternativ till fisket efter sjögurkor. Analysen visar tydligt på bristen av kunskap vad det gäller effekter på samhällen och ekosystem av odlingar. Dessutom förekommer ofta uppblåsta löften som inte kan hållas – vilket leder till att nationer och samhällen tar onödiga risker vilket i sin tur försvårar en hållbar förvaltning av fisket och kustzonsmiljön. Slut- satsen är att effekten av existerande odlingar måste utvärderas och att riktlinjer bör utformas för att den globala expansionen av vat- tenbruk ska kunna ske på ett hållbart sätt.

Avhandlingen betonar vikten av adaptiv förvaltning för att

kunna styra fiskets och vattenbrukets utveckling. Detta kan åstad-

kommas genom ökad kunskap och deltagande i styrning och för-

valtning, samt genom att inkludera sjögurkor i policy- och förvalt-

ningsstrategier på en högre nivå. Väl förvaltade resurser av sjögur-

ka har potential att spela en stor roll i fattigdomsbekämpning i

västra Indiska Oceanen.

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Reflections and acknowledgements

The pursuit of research is very much a personal endeavour driven by curiosity and a “need to know”. It certainly requires commit- ment and loyalty to the task. In everyday life that means smudging the border between the personal and the professional. A majority of the content here has been created on weekends, during after- hours, or under a mosquito net in assertive heat – all under a great deal of self inflicted stress. It’s particularly during these periods that having supervisors to guide you is invaluable. My supervisors, Maricela de la Torre-Castro, Nils Kautsky and Per Olsson have been invaluable in that role to push me when I’m holding back and to hold me back when I rush too far afield. Their guidance and support has made my research and my personal ambitions possible.

I am forever thankful for that.

Monumental for my career in a chronological order have also been

James Scandol that housed me through my projects at NSW Fish-

eries in Sydney, followed by Kim Friedman at SPC in Nouméa

that first linked me on to work with sea cucumber fisheries in the

South Pacific (which we later published in the journal Fish and

Fisheries). From there I went on to meet Maria Byrne and Chantal

Conand in Sydney 2006 and 2007, both Maria and Chantal have

been a constant source of support ever since. This is also when I

first made contact with Maricela and the embryo of what came to

be the research for my PhD was conceived. When I took up my

PhD at the Department of Systems Ecology in February 2009 I

had no idea of the collaborations and friendships that I would

come across. The support by Narriman Jiddawi, Leonard Duras-

nel, Benjamin Esperance and Patrick Frouin has been both

monumental and encouraging. In the field I have had the invalu-

able assistance of friends like Muumin Hamad and Said Shabaan

in Zanzibar, and Alban Jamon, Didier Frey, Julien Wickel and

Karani Saindou in Mayotte. I have also had the help of Caroline

Raymond, Malin Dahlgren and Maria Eggertsen, and a lot of fun

with my newfound friends and co-authors Georgina Robinson,

Matthew Slater and Max Troell. I am particularly grateful for the

time given by all the fishers and fishery participants in the studies

in this thesis. In addition, I would like to thank Jim Prescott, Kalo

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Pakoa, Nyawira Muthiga. Steve Purcell and Sven Uthicke, which have all contributed to thoughts, ideas and motivation. Thanks also to my family and friends for support and encouragement during these past years, there have been both happy days and sad ones.

Here it is appropriate to highlight all my great colleagues at the Department of Systems Ecology and in particular the straight faces kept by Sara Fröcklin and Nadja Stadlinger that I share an office with – it must have been a nightmare for you. The layout of this thesis was inspired by the well-crafted thesis of Jerker Lokrantz.

Redmond O’Hanlon in his fictional travel book Congo Journey ob- serves that the genuine scientists “have that slight absence, the manner of men with real interests outside themselves, an inner distance from the concerns of family, the earning of money”, essen- tially glorifying the socially inept and sometimes introvert appear- ance that comes with the job. I’m very lucky to have found some- one that can look past all my imperfections and embrace the bore in me. Thanks Leah, I am in awe of your patience.

Support for this research was provided by the Institute of Marine

Science (IMS) in Zanzibar, La Direction de l’agriculture et de la

Forêt (DAF), and Conseil General in Mayotte, the Swedish Inter-

national Development Cooperation Agency (Sida), the Western

Indian Ocean Marine Science Association (WIOMSA), the School

of Biological Sciences of Sydney University, Université de la Réun-

ion, Rhodins Memorial Foundation, and the International Foun-

dation for Science (IFS).

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