AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS

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1 AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS Aquatic Conserv: Mar. Freshw. Ecosyst. (2013) Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: /aqc.2421 Catastrophic depletion of reef-associated sea cucumbers: resource management/reef resilience issues for an Indonesian marine park and the wider Indo-Pacific DAVID J. W. LANE a,b, * and DANIEL LIMBONG c, a Department of Biology, Universiti Brunei Darussalam, Brunei Darussalam b Honorary Research Fellow, Raffles Museum of Biodiversity Research, Department of Biological Sciences, Faculty of Science, National University of Singapore, Singapore c Faculty of Fisheries and Marine Science, Sam Ratulangi University, Kampus Unsrat, Bahu, Manado 95115, Sulawesi Utara, Indonesia ABSTRACT 1. Commercial species of shallow-water, tropical, aspidochirotid sea cucumbers (bêche-de-mer) in the Indo-West Pacific, many of them, at maturity, large and conspicuous benthic members of coral reef or seagrass/sediment environments, represent a high-value marine resource, traditionally fished for centuries, but which currently are being heavily overfished, largely through a growing demand from mainland China and regional markets in the supply chain. 2. Population losses are exemplified by a study at Bunaken National Marine Park, North Sulawesi, Indonesia, where densities of commercial sea cucumber species are very low following earlier harvesting and where drop-out of species records has occurred over a 17-year study period. 3. Sea cucumber populations have not recovered from overexploitative depredations despite the designation of this area as a National Marine Park in 1991 and the commencement of protection measures. 4. This pattern of overexploitation, replicated across the tropical Indo-Pacific, has detrimental implications for many coastal communities traditionally or currently dependent on this high-value resource. 5. In addition there are potentially serious implications of overharvesting reviewed here for reef ecosystem resilience. Copyright # 2013 John Wiley & Sons, Ltd. Received 29 July 2013; Revised 14 September 2013; Accepted 27 October 2013 KEY WORDS: Aspidochirotida; Bunaken; Echinodermata; Indo-Pacific; overfishing; reef resilience *Correspondence to: D.J.W. Lane, Department of Biology, Universiti Brunei Darussalam, Jalan Tungku Link, BE1410, Brunei Darussalam. david.lane@ubd.edu.bn Present address: Lembaga Penelitian dan Pengabdian Kepada Masyarakat Universitas Kristen Tentena, Jl. Torulemba No. 21, Tentena, Poso 94663, Sulawesi, Indonesia Copyright # 2013 John Wiley & Sons, Ltd.

2 D. J. W. LANE AND D. LIMBONG INTRODUCTION Extraction of living resources from the sea, over periods of decades to centuries, has resulted historically in serial catastrophic population declines, equating to ecological extinctions (Jackson et al., 2001; Pauly and Palomares, 2005) that are perceived to be a leading cause of ecological change and collapse of many coastal ecosystems world-wide (Jackson et al., 2001). This pattern of severe overfishing applies not only to finfish, marine mammals and invertebrate shellfish but to many other invertebrate resources too, including echinoderm species (Micael et al., 2009). Commercial species of aspidichirotid sea cucumbers (Holothuroidea) are a case in point, with serial species overexploitation of this high-value product, known as bêche-de-mer, being a characteristic pattern, particularly throughout much of the tropical Indo-Pacific (Conand, 1998; Uthicke and Benzie, 2000; Uthicke et al., 2004; Conand and Muthiga, 2010; Purcell et al., 2010; Hamilton and Lokani, 2011). The multi-species global fishery for sea cucumbers has expanded rapidly in recent decades (Eriksson et al., 2012b) with the harvest peaking at about metric tonnes (wet weight equivalent) of dried product, valued at about US$ 60 million, in 1995 (Jaquemet and Conand, 1999; Conand, 2001). Sea cucumbers are important to the economies and livelihoods of many coastal communities, particularly in the tropical Indo-Pacific, and are often the most economically important fishery and non-finfish export for many countries (Toral-Granda et al., 2008a). Sea cucumber fishers, estimated to number around 3 million (Purcell et al., 2011), represent almost half of the estimate for reef fishers globally (Teh et al., 2013). Overfishing of sea cucumbers threatens the livelihood opportunities provided by this high-value resource to coastal fishers (FAO, 2013). As with other fishery resources, there is concern that overfished bêche-de-mer stocks are slow to recover in population numbers or that recovery is lacking (Uthicke et al., 2004; Ahmed and Lawrence, 2007; Friedman et al., 2011; Price et al., 2013). Furthermore, sustainable exploitation of sea cucumber stocks is, for many species, hindered by a number of biological and regulatory factors: long life cycle (Uthicke et al., 2010) with, in many species, presumed slow development to maturity; high visibility and accessibility of shallow, sedentary species; low charismatic standing (McClenachen et al., 2012); and lack of any protection by CITES for almost all taxa (Purcell et al., 2010) despite good cases for listing (Bruckner et al., 2003). The recent IUCN listing of seven commercial sea cucumber species as endangered with high risk of extinction (IUCN, 2013) is a welcome development but, in the tropical Indo-Pacific at least, despite moratoria on exports by some countries (Purcell et al., 2010; Friedman et al., 2011), the fishery continues to be generally unregulated or illegally overexploited and is characterized by an accelerating, large-scale ecosystem plunder (Toral-Granda, 2005 Galapagos; Zabludovsky, 2013 Mexico) that is evident for many other marine resources (Berkes et al., 2006). Indonesia has the world s largest fishery for tropical sea cucumber (Tuwo and Conand, 1992; Conand, 2001; Tuwo, 2004; Choo, 2008), yet management of the fishery in the country has been limited or non-existent, species are merged in the trade data (Choo, 2008), and field population data for commercial species are sparse. Fishery data (Tuwo, 2004), although somewhat limited, do show a decline in size and catch per unit effort, indicating that bêche-de-mer species are generally being overexploited in the Archipelago. Hoeksema (2004) and Massin (1999) have noted the near disappearance of commercial species over an approximate 10-year period (mid-1980s to mid-1990s) around reefs of the Spermonde Archipelago, south-west Sulawesi, coincident with the introduction of scuba and hookah diving to the fishery. This pattern of overexploitation and depletion of bêche-de-mer, characteristic throughout the tropical Indo-Pacific (Toral-Granda et al., 2008b; Hamilton and Lokani, 2011), seemed to be evident in north Sulawesi too at the Bunaken National Marine Park (BNMP) and over a similar time period. This perception prompted a review of the first author s detailed echinofaunal data records and photo records, obtained during a series of echinoderm biodiversity scuba surveys at the Bunaken Park over a 17-year period ( ), as well as a series of sea cucumber population density surveys in Initial observations in the early 1990s

3 CATASTROPHIC BÊCHE-DE-MER DEPLETION indicated that while the species richness of sea cucumbers appeared to be high, abundances were not. High-value commercial bêche-de-mer species in particular, all of them within the sediment-feeding order Aspidochirotida, were uncommon or rare (Lane, 1999a), probably representing a legacy of intensive harvesting and overexploitation in earlier decades before establishment of the marine park. Indeed, it has been reported that profits from unrecorded and unregulated sea cucumber harvesting in the area were significant in supporting development of the local diving tourism industry in its early days (L. Herlambang pers. comm.). BACKGROUND AND METHODOLOGY The Bunaken National Marine Park, located at the northern tip of Sulawesi, near the geographic centre of the Coral Triangle (Briggs, 1974; Roberts et al., 2002; Hoeksema, 2007), includes five coral reef-fringed islands, part of the mainland coast of the north-western tip of Sulawesi, near Manado town, and a separate section of coastal reefs at Arakan-Wawontulap, south of Manado Bay (Figure 1). The park covers a marine domain of ha, including some 8010 ha of reef flat, slope and lagoonal habitat, the latter including at least 1300 ha of seagrass beds (Mehta, 1999). The marine park, formally established as Indonesia s first National Marine Park by the Indonesian Ministry of Forestry in October 1991, is currently on the tentative list for World Heritage Site status (UNESCO, 2012). During the park s initial years, management, monitoring and enforcement were under-resourced and there was evidence of continued unsustainable fishing practices, particularly when, during the Asian economic crisis of the late 1990s, cuts in conservation budgets resulted in increased pressures on park resources (Erdmann and Pet, 1999). However, the fall of the Soeharto regime following the Asian economic crisis of the late 1990s led ultimately to greater regional devolution in the Archipelago and, in turn, the development of a multi-stakeholder park management structure (Bunaken National Park Management Advisory Board). This management board has, since March 2001, obtained revenue from park entrance fees, most of which is directed towards conservation programmes and promotion of sustainable activities within the park (Erdmann et al., 2004). The natural resources of the area and associated tourism support a population of some residents (UNEP, 2005). An aspidochirotid species list for BNMP was compiled initially from echinofaunal checklist records and photorecords of the first author made during 14 scuba survey visits to both northern and southern sectors of the Bunaken Marine National Park, spanning a period of 17 years from June 1993 to March Each visit lasted from 5 to 8 days, with a combined total of 154 scuba dives. Each dive was of 1 h duration and 12 of them were undertaken at night. Records of first and subsequent sightings of sea cucumber taxa were made photographically and/or tallied on a check-list during the dives. Check-list records often consisted of single occurrences during a dive. The general impression was that abundances of many sea cucumber species were low. During a visit in December 2008 (13 dives), quantitative population studies were initiated in the northern sector of the Park. These involved 10m-wide belt transects on reef slope contours based on drift-dives of 1 h duration, and GPS-determined transect lengths ranging from m. An on-line utility ( gps/distance/ ) is available to calculate the linear distances between the GPS coordinates for the start and end points of transects. As sea cucumber encounters were relatively infrequent and underwater visibility was high it was considered to be more effective in terms of efficient use of dive time and areal coverage to set the belt width to 10 m (with few or without replicates) rather than the more usual 2m-wide replicated transects. This protocol, essentially a refinement of that adopted for earlier drift-dive surveys, avoided the problems associated with manta tows (e.g. missed individuals). The area covered and searched during each dive ranged from m 2. During the transect surveys all visible aspidochirotid sea cucumbers, i.e. diurnally active, epibenthic and semi-cryptic individuals within a gauged 10m track width were recorded on a species list, counted, and measured for length. The semi-cryptic forms included individuals either partially hidden in recesses, covered

4 D. J. W. LANE AND D. LIMBONG Figure 1. Map of Bunaken National Marine Park, North Sulawesi, Indonesia. Locations of quantitative transect surveys for aspidochirotid sea cucumbers are indicated by stars. by rock slabs or a layer of debris, or semi-buried in sediment. Belt transect survey coverage included reef slopes at depths of 5 25 m around three of the larger islands in the northern BNMP sector, namely Bunaken, Manado Tua and Mantehage, plus mainland reef slopes within the northern park sector. No attempt was made to quantify sea cucumber records or densities for reef flat species or for nocturnal species observed during night dives, although these records contributed to a species

5 CATASTROPHIC BÊCHE-DE-MER DEPLETION richness assessment. Identifications were based on in situ colour slide or digital photographs, the primary and revisionary taxonomic literature and a recent guide book on commercial sea cucumbers (Purcell et al., 2012). RESULTS Species richness Species records for aspidochirotid sea cucumbers in the BNMP during the series of 14 surveys, from Table 1. Bunaken Marine Park aspidochirotid counts by species for swim-line surveys, The December 2008 column (shaded) represents data acquired using a different protocol (belt-transects). Species value categories derived from Choo, 2008, Conand, 2008, Kinch et al., 2008b, Purcell et al., 2010, NA designates either not applicable for species not known to occur in the fishery, or not available for fished but unrecognized species. Boldened names represent species recently categorized (IUCN, 2013) as Endangered (E) or Vulnerable (V) to extinction

6 D. J. W. LANE AND D. LIMBONG Table 2. Aspidochirotid sea cucumber counts and densities, Bunaken Marine Park belt-transect surveys, December Counts are boldened and densities (numbers per hectare) are in parentheses. HV: high value; MV: medium value; LV: low value; NA: not applicable (species unknown or unrecognized in the fishery) Survey location Bunaken, Fukui S.W. Bunaken, Alung Banua Mantehage N.W. Mantehage S. (Bango pt.) Bunaken N.E. Mantehage E. Mantehage S.E. Manado Tua, N.E. Bunaken, Fukui to Alungabanua Bunaken Fukui Mainland, nr. Tiwoho Mainland, W. of Tiwoho Survey Area ha Market value Taxon HV Holothuria fuscogilva MV Actinopyga palauensis Bohadschia argus LV Bohadschia marmorata Holothuria coluber? Holothuria fuscopunctata Pearsonothuria graeffei 2(4) 1(3.33) 1(2.5) 2(5.26) 7(14) 1(1.61) 2(5) 1(2) 6(7.6) 1(2.63) 3(4.82) 1(2.5) 1(3.33 1(3.33) 2(5) 1(2) 1(1.27) 1(2.63) 1(1.61) 1(2.5) 2(4) 22(35.48) 5(10) 4(10) 2(6.19) 2(2.53) 5(13.16) 3(4.82) 6(15) Thelenota anax 3(6) 1(2.5) 1(3.1) 6(7.6) 3(4.82) 1(2.53) Thelenota rubralineata NA Holothuria edulis (pink) 2(4) 2(4) 1(3.1) 1(1.61)

7 CATASTROPHIC BÊCHE-DE-MER DEPLETION other high-value species, recorded in previous BNMP surveys, were not seen. Low frequency of encounters is apparent in the high-value species records for surveys before 2008 (Table 1) and drop-out of certain taxa is apparent. For example, one of the highest value species, Holothuria whitmaei, has not been seen since March 2000 and the medium-value Actinopyga echinites and Stichopus herrmanni, both considered vulnerable to extinction (IUCN, 2013), have not been seen since singleton records in 1994 (Table 1). Figure 2. Size frequency plot for the five most abundant species in the December 2008 belt- transect surveys at Bunaken National Marine Park to 2010, are given in Table 1. The fauna list (28 species) includes several records of rare or recently described Indo-Pacific species, e.g. Actinopyga caerulea (Samyn et al., 2006), Stichopus ocellatus (Massin et al., 2002) and Thelenota rubralineata (Massin and Lane, 1991). The inventory also includes two rarely encountered species, Holothuria whitmaei and Thelenota ananas (Table 1), categorized recently as endangered by the International Union for the Conservation of Nature (IUCN, 2013). Abundances and population densities Records for high-value aspidochirotids during the 17-year series of swim-line surveys often consisted of low numbers or singletons (Table 1). Higher counts in June 2009 are attributed to an observer effect, there being two observer divers at that time compared with a single observer on other swim-line surveys. Belt-transect surveys in December 2008 (Table 1 highlighted column) resulted in low encounter rates for high-value species and low densities for most species (Table 2). In these quantitative surveys the most abundant sea cucumber, Pearsonothuria graeffei, a low-value species with a thin body wall, had a peak density of 35 ind. ha -1. In contrast, except for the medium-value species Bohadschia argus at one site, the densities for medium- and high-value species were less than 10 ind. ha -1 (Table 2). In fact during the belt transect surveys only one high-value species, Holothuria fuscogilva, was found (Table 2) and Size composition of populations Size frequency plots (Figure 2), derived from the December 2008 transect survey data, are meaningful only for those species that were sufficiently abundant (barely in some cases). The most abundant species, Pearsonothuria graeffei and Bohadschia argus show a normal distribution, peaking in abundance in the cm size class. It should be noted, however, that the reliability of length data for P. graeffei is influenced by the fact that undisturbed individuals are frequently found in varied states of contraction or extension. Thelenota anax was generally found as large to very large individuals and no individuals under 30 cm in length were seen. Size frequency plots are given for two other commercial species, Holothuria fuscogilva and Holothuria fuscopunctata (Figure 2); the data are too few to show patterns of population size structure clearly, but again small individuals are very few or absent. DISCUSSION The series of visits to BNMP revealed a high aspidochirotid species richness (28), consistent with the location at the geographic centre of the zone of maximum marine biodiversity, but abundances were low an observation which stimulated the quantitative aspects of this study. In contrast, observations for nocturnally active species indicated much higher numbers and densities. Night surveys were not quantitative because of logistic difficulties but large nocturnal species, notably Stichopus noctivagus and

8 D. J. W. LANE AND D. LIMBONG Holothuria turriscelsa, were commonly seen (> 10 individuals per dive) on the reef slopes and walls during night dives at Bunaken Island. These two nocturnally emergent species are not currently on the list of commercially targeted species but many other burrowing forms are (Kinch et al., 2008a). Cryptic behaviour in nocturnal species hiding within the reef matrix or sediment by day and emerging only after sunset may afford them some protection from harvesting (but see comments below). Bêche-de-mer population densities measured during the series of surveys in December 2008 are very low, except for the thin-walled, low-value Pearsonothuria graeffei at some sites (Table 2). All other species, including high- and medium-value ones, occurred at densities of less than 10 ind. ha -1 (except for the medium-value Bohadschia argus at one transect site). Low densities and drop-out of species records for these large, conspicuous invertebrates at BNMP is indicative of overexploitative extraction of this resource. Similar low densities have been recorded for heavily fished localities in the western central Pacific (Kinch et al., 2008a). The most striking finding of the recent (December 2008) quantitative survey is the absence from the transect census of several high-value species previously recorded in BNMP, notably Holothuria whitmaei, Holothuria scabra, Stichopus herrmanni and Thelenota ananas (Table 2). Thelenota ananas (the prickly redfish), formerly one of the more abundant and widely distributed large stichopodid sea cucumbers in the tropical west Pacific (personal observation of first author), is now considered endangered with extinction (IUCN, 2013). At Bunaken, and many other locations, it is now rarely sighted, unlike its lower value congeners T. anax (Tables 1, 2) and, in some locations, T. rubralineata (Lane, 1999b, 2008). The only high-value species recorded in the BNMP transect surveys, Holothuria fuscogilva, occurred at low population densities of ind. ha -1. Low count rates or total absence (combined survey area of 5.6 ha) indicate that stocks of many high-value species are indeed very low on reefs within the marine park. Density values for large-bodied, commercially targeted sea cucumbers are typically much higher on protected or underexploited reefs in the tropical Indo-Pacific. For example, Holothuria whitmaei (the black teatfish), Holothuria fuscogilva (the white teatfish) and Holothuria scabra (the sand fish) were reported to occur at peak densities of 30, 50 and 500 ind. ha -1, respectively, on the unfished reefs of Eastern Torres Strait (Long and Skewes, 1997). For H. whitmaei, one of the most valuable species in the west Pacific, densities at protected sites on the Great Barrier Reef (about 20 ind. ha -1 ) were about four times the values for fished reefs (Uthicke and Benzie, 2000 as H. nobilis). Population densities of H. whitmaei above 12.5 ind. ha -1 are characteristic of protected or unfished reefs and are considered by Kinch et al. (2008a) as representing natural densities. However, perception is susceptible to the phenomenon of creeping normalcy (Diamond, 2005) and it is quite possible, or even likely, that much higher climax densities on unexploited reef sediments prevailed in the past. Epibenthic tropical sea cucumbers, as adults, have few predators (Preston, 1993) thus, on undisturbed reef-associated habitats, population densities can build up either due to successive recruitment of sexually derived juveniles or, for several species in the tropics, by natural, transverse asexual fission (Emson and Wilkie, 1980), or a combination of both. However, there is some evidence that, for Holothuria atra and Stichopus chloronotus at least, population densities remain relatively stable following periods of intense asexual reproduction (Uthicke, 2001c). Densities below threshold levels envisaged by Kinch et al. (2008a), or comparable values for other bêche de mer species, result in increased average inter-individual distances that, for non-aggregating, broadcast-spawning species, may impair fertilization success, thus ultimately reducing or delaying recruitment to the adult populations. This interpretation, in essence operation of the Allee effect (Stephens et al., 1999), is supported by evidence that cessation of fishery pressure on depleted sea cucumber stocks does not result in a rapid or marked recovery of stocks (Uthicke et al., 2004; Ahmed and Lawrence, 2007; Kinch et al., 2008a; Price et al., 2013). Large-bodied bêche-de-mer species may be particularly vulnerable in this regard as their biomass per hectare corresponds to lower population densities (and thus increased average

9 CATASTROPHIC BÊCHE-DE-MER DEPLETION inter-individual distances) than for a similar biomass of small-bodied species (Lawrence, 1980). Because fertilization success is density dependent it is likely that, at very low densities and without an external source of larval/juvenile recruits, economic pressure on the resource can continue beyond the tipping point where relaxation of remnant populations and local ecological extinction would occur. Fishery statistics for sea cucumbers are, unfortunately, lacking for the Bunaken area and for North Sulawesi generally but verbal reports (cited in Lane, 1999b) indicate that intensive harvesting, before establishment of the BNMP in 1991, probably brought stock densities on reef slopes to their present low levels. Size frequency data for remnant BNMP populations of the five most abundant species (Figure 2) show very low numbers or absence of small size classes, notably for the low-value species, Thelenota anax, perhaps suggesting a failure of recruitment. However, juveniles of tropical, reef-associated sea cucumbers are infrequently observed in the wild and recruitment ecology is generally poorly understood for these invertebrates (Mercier et al., 1999; Shiell, 2004; Trentin, 2011). Reduction of stocks for non-aggregating, broadcast-spawning sea cucumbers to below threshold densities may result in drastically reduced sexual reproductive success and consequent failure of natural recruitment and population recovery, even within a protected marine park. Furthermore, it should also be noted that the BNMP management plan of the late 1990s (Mehta, 1999) and subsequent zoning revisions (Erdmann and Merrill, 2004) make no mention of sea cucumber resources or their protection. Thus it is possible that continued low-level exploitation is occurring. The BNMP area has developed a high international profile in terms of diving and ecotourism, an industry which has a self-interest in the preservation of marine resources (particularly photogenic species) and which, through the collection of park entrance fees, funds marine policing and conservation measures. What is needed in addition, with regard to sea cucumber management, are more extensive surveys repeated at intervals to monitor population recoveries, if any, accompanied by the inclusion in the park management plan of core zones and no-take areas for commercial species. Artificial aggregation of pre-spawning adults in protected areas, to overcome potentially severe sperm limitation effects (Levitan and Petersen, 1995; Yund, 2000), could be undertaken as a low-cost research/ management initiative that offers the prospect of recovery of populations (Bell et al., 2008) and might lead eventually to a sustainable bêche-de-mer fishery within the park. Overfishing and stock depletion of bêche-de-mer at BNMP exemplifies what has been happening in recent decades to this high-value resource on a wider scale globally in the tropical Indo-Pacific (Conand and Byrne, 1993; Anderson et al., 2011; Purcell et al., 2011). Serial population and fishery collapse throughout the tropical Indo-Pacific, brought about by the overexploitative practices of bêche-de-mer traders and entrepreneurs have, following the boom times, incurred consequential losses in sustainable revenue for small Indo-Pacific island nations and their coastal communities - to the point where a link between overexploitation and low Human Development Indices has been demonstrated (Purcell et al., 2011). In addition, there may be significant, but as yet under-researched, effects on reef ecosystem productivity, functioning, and resilience resulting from the wholesale removal of these macrodetritivorous, seabed sediment processors (Wolkenhauer et al., 2010; Anderson et al., 2011; Friedman et al., 2011). Echinoderms, particularly aspidochirotid sea cucumbers, are a prominent if not dominant component of the benthic marine fauna, in both the tropics and at high latitudes, and they play a key role in structuring many marine ecosystems (Uthicke et al., 2009). Aspidochirotids are in effect earthworms of the sea; their important contribution to sediment turnover (Coulon and Jangoux, 1993; Uthicke, 1999) and carbon cycling (Moriarty et al., 1985) is well known, yet knowledge of the ecological impact of wholesale removal through overharvesting of these large invertebrates is poor (Eriksson et al., 2012a). Recent studies indicate that the sediment-feeding/organic-recycling activities of dense populations are important for microalgal (Uthicke, 2001b) and seagrass bed (Wolkenhauer et al., 2010) productivity, nutrient cycling (Uthicke, 2001a), and potentially in the CaCO 3 balance on

10 D. J. W. LANE AND D. LIMBONG reefs (Schneider et al., 2011). Sand flats and slopes account for large areas in and around many coral reefs (Moriarty et al., 1985) and at unexploited, high densities, populations of aspidochirote sea cucumbers, feeding on carbonate sediments, are calculated to be a greater contributor to night-time dissolution of calcium carbonate and alkalinity than endolithic carbonate bioeroders (Schneider et al., 2011) thus potentially countering the effects of ocean acidification on reefs, at least locally. Dense sea cucumber populations may promote reef health and resilience in another way. Sheltered reef-associated sediment fields with low sea cucumber abundances in the west Pacific are often noted to be characterized by undisturbed microalgal mats (observations of the first author). Further investigation and quantification is needed but it is quite possible that feeding and bioturbation by sea cucumbers may be important in controlling the build-up of potentially harmful microorganisms and cyanobacterial mats (Bruckner et al., 2003). In essence, these non-charismatic animals, the literature of which is often relegated to obscurity, may hold one of the keys to the ecological integrity of reefal habitats. Management of tropical sea cucumber fisheries has, historically, either been non-existent or inefficient (Choo, 2008; Toral-Granda et al., 2008a) yet even while the bêche-de-mer resource has experienced intense fishing pressure and become heavily overexploited, the market demand for this high-value product continues, to the ultimate detriment of coastal community livelihoods and, potentially, reef resilience. A recent development and concern is that as the bêche-de-mer resource has become depleted, buyers and harvesters have begun to target not only lower value species (Kerr, 2013) and small-sized individuals (Kinch et al., 2008a, b), but in several Indo-Pacific areas are now shifting their extractive efforts to nocturnal species, particularly infaunal ones that emerge at night (Kinch et al., 2008b; Dissanayake et al., 2010; Choo, 2012; Suharsono pers. comm. Indonesia). This trend, if permitted or tolerated on a broad geographic scale, might result in further adverse ecological consequences for reef- or sea grass-associated benthic ecosystems, and their sustainable exploitation. ACKNOWLEDGEMENTS The authors express their thanks to the diving section of Cha Cha Nature Resort on Bunaken Island for their logistical support during the more recent visits and surveys, and in particular to Soleman Laikun for assistance during the sea cucumber transect surveys. Thanks are also due to Gustav Paulay and Alexander Kerr for assistance with identification of some problematic species. Partial funding for the field work was provided initially from an EEC/National University of Singapore grant (CL1-CT ), then subsequently from a Universiti Brunei Darussalam Research Grant (UBD/PNC2/2/RG/1(20)). REFERENCES Ahmed MI, Lawrence AJ The status of commercial sea cucumbers from Egypt s northern Red Sea Coast. SPC Beche-de-mer Information Bulletin 26: Anderson SC, Mills Flemming J, Watson R, Lotze HK Serial exploitation of global sea cucumber fisheries. Fish and Fisheries 12: Bell JD, Purcell SW, Nash WJ Restoring small-scale fisheries for tropical sea cucumbers. Ocean and Coastal Management 51: Berkes F, Hughes TP, Steneck RS, Wilson JA, Bellwood DR, Crona B, Folke C, Gunderson LH, Leslie HM, Norberg J, et al Globalization, roving bandits, and marine resources. Science 311: Briggs JC Marine Zoogeography. McGraw-Hill: New York. Bruckner AW, Johnson KA, Field JD Conservation strategies for sea cucumbers: can a CITES Appendix II listing promote sustainable international trade? SPC Beche-de-mer Information Bulletin 18: Choo PS Population status, fisheries and trade of sea cucumbers in Asia. In Sea cucumbers. A Global Review of Fisheries and Trade, Toral-Granda V, Lovatelli A, Vasconcellos M (eds). FAO Fisheries and Aquaculture Technical Paper, No. 516: Rome; Choo PS The sea cucumber fishery in Semporna, Sabah, Malaysia. SPC Beche-de-mer Information Bulletin 32: Conand C Overexploitation in the present world sea cucumber fisheries and perspectives in mariculture. In Echinoderms San Francisco. Proceedings of the Ninth International Echinoderm Conference, San Francisco, California, USA, 5 9 August 1996, Mooi R and Telford M (eds). AA Balkema: Rotterdam/Brookfield; Conand C Overview of sea cucumbers fisheries over the last decade what possibilities for durable management? In Echinoderms Proceedings of the 10th International Conference, Dunedin, 31 January 4 February 2000, Barker M (ed.). Swets and Zeitlinger; Conand C Population status, fisheries and trade of sea cucumbers in Africa and the Indian Ocean. In Sea Cucumbers.

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13 CATASTROPHIC BÊCHE-DE-MER DEPLETION Uthicke S, Welch D, Benzie JAH Slow growth and lack of recovery in overfished holothurians on the Great Barrier Reef: evidence from DNA fingerprints and repeated large scale surveys. Conservation Biology 18: Wolkenhauer SM, Uthicke S, Burridge C, Skewes T, Pitcher R The ecological role of Holothuria scabra (Echinodermata: Holothuroidea) within subtropical seagrass beds. Journal of the Marine Biological Association UK 90: Yund PO How severe is sperm limitation in natural populations of marine free-spawners? Trends in Ecology and Evolution 15: Zabludovsky K Quest for illegal gain at the sea bottom divides fishing communities. New York Times, 19 March 2013 ( html )