Australian Institute of Marine Science, Townsville, Australia
The holothurian fishery has a long tradition in Australia that began with Macassan fishers. The interactions resulting from the sea cucumber fishery provided the first cultural contact between aboriginal and islander communities and non-Australians. The sea cucumber fishery occurred in a typical "boom and bust" fashion, with boom cycles several decades apart. The last of these cycles commenced in the mid 1980s and signs of overfishing are now apparent. The main target species in the fishery on the Great Barrier Reef (GBR) was the black teatfish (Holothuria nobilis). Initiated by a request from the fishing industry and supported by data obtained through studies summarised in this report the fishery for this species was closed in 1998. Surveys on over 60 reefs along the entire reef system (spanning a distance of 2 000 km) conducted in 1998/99 indicated that stocks of this species were generally lower in the southern half of the GBR. It is likely that the lower densities resulted in the concentration of the fishing effort north of Townsville (ca. 12 °S to 19 °S). The existing zoning of the Great Barrier Reef Marine Park allowed a comparison between reefs fished and reefs protected from fishing (Green Reefs or No-Take Zones). This comparison showed that fishing reduced the densities ofH. nobilis on the fished reefs by about 75 %. GIS-based model calculations indicate that an initial ("virgin") biomass of about 5 500 tonnes was reduced by 2 500 to 3 000 tonnes. This figure corresponds well to the total reported catch since the opening of the fishery. These model calculations have three major implications for future management of H. nobilis, and potentially other species, on the GBR and elsewhere. 1) No-Take Zones provide an effective means for stock protection of this species. However, whether the area protected was sufficient as a source of recruits for the whole area is unknown. 2) The agreement between reported catch and total reduction of numbers indicates that recruitment is very low and fishing has simply reduced stocks over more than a decade without appreciable replenishment. Repeated surveys of 23 reefs, one and two years after the closure of the fishery, could not detect any recovery of the stocks, providing further evidence for low levels of recruitment. 3) Annual catches of (on average) less than 5 % of virgin biomass depleted stocks ofH. nobilis. This is in sharp contrast to notions that up to 50 % of virgin stock size might be taken annually. These data suggest an extremely cautious approach should be taken in the management of beche-de-mer fisheries.
Keywords: Resource management, stock size, recruitment, no-take zones, marine protected areas
History of holothurian fishing on the Great Barrier Reef
Holothurian fishing has a long tradition in Australia and provided the first cultural contact of aboriginal and islander communities with non-Australians. These were Macassan fishermen and traders who visited this country centuries before European settlement. Matthew Flinders, one of the early explorers of Australian reported in his "Voyage to Terra Australis":
"The object of their [the Macassans] expedition was a certain marine animal, called trepang. Of this they gave me two specimens; and it proved to be the beche-de-mer, or sea cucumber which we had first seen on the reefs of the East Coast, and had afterwards hauled on shore so plentifully with the seine, especially in Caledon Bay. They get the trepang by diving, in from 6 to 8 fathoms water; and where it is abundant, a man will bring up eight or ten at a time.
This Macassan fishery in the Northern Territories and West Australia was analyzed in detail in a book by MacKnight (1976). The first fishery by Europeans occurred early in the 19th century and was based on the GBR and the Torres Strait, in conjunction with trochus and pear shell exploitation. A first beche-de-mer station was reported in 1804 on Lady Elliott Island, but the operation did not last very long (Sumner, 1981). Further development of the fishery occurred about 40 years later, around 1850, when stations were opened at Green Island (near Cairns), Fitzroy Island and the Frankland Islands (Sumner, 1981). During that period, most fishermen made the long journey from Sydney and played an important role in exploring the tropical east coast of Australia (see reports in Idriess, 1957). The fishery showed the first signs of overfishing in the 1890s (Sumner, 1981). At that time, stocks declined in areas close to the shore and larger boats had to be used to access reefs further off shore.
The author estimated historical catch data for beche-de-mer on the east coast of Australia (Figure 1) with data given in Saville-Kent (1893), Sumner (1981) and Anon (1946). To do this, several assumptions and conversions had to be made (see explanation in figure legend) thus data presented can only be taken as rough estimates. However, it appears that the total volume of previous fisheries was larger than values taken in the current fishery. This may be partly explained by the fact that it is not possible to discern where holothurians were actually fished, because historic data were based on export data from Queensland. These data may therefore include animals fished in the Torres Strait, Coral Sea reefs, Papua New Guinea and the Solomon Islands. This lack of information makes it difficult to put exact figures on boom and bust cycles, but it is clear that the previous cycle ended about the time World War II began, as was also reported by Harriott (1985). It is unclear if this was caused by a single factor such as stock reductions, political or economic reasons, or a combination of factors. The cycles may also be blurred by shifts in species caught, but it appears that most of the catch on the Great Barrier Reef (GBR) at that time was black teatfish (Saville-Kent, 1893), whereas the fishery in the Torres Strait and the Northern Territory was mainly based on sandfish (Holothuria scabra).
Current fishery cycle and management
The current cycle for the sea cucumber fishery commenced in the mid 1980s, and signs of overfishing are now apparent. Along the east coast of Australia, there are four different fisheries, managed by different agencies.
The fishery in the Torres Strait is mainly based on sandfish catches on Warrior Reef. This reef is on the border between Papua New Guinea and Australia and was thus also visited by fishermen from Papua New Guinea. This fishery is managed by the Australian Fisheries Management Authority (AFMA), a federal agency, and after only four years of fishing effort, was closed in 1998 due to an extreme stock depletion. These stocks had not recovered when surveyed again in 2000 (Skewes et al., 2000). Likewise, the fishery on black teatfish and surf redfish (Actinopyga mauritiana) in the Torres Strait was closed in 2003 due to over-exploitation.
Another AFMA-managed sea cucumber fishery exists on some offshore reefs in the Coral Sea and allowable catches for this fishery are currently under negotiation. However, logbook surveys (Hunter et al., 2002) indicated that catch rates for high-value species have declined from the year 2000 to 2001.
Some sandfish fisheries exist in the vicinity of Hervey Bay (closed in 2000) and Moreton Bay (an exploratory fishery was opened in 2003) and are managed by the Queensland Fisheries Service (QFS). The same agency also manages the fishery on the GBR, but fishing in the Marine Park also needs to be in accordance with Great Barrier Reef Marine Park regulations. All Australian fisheries for export also need approval from the Department of Environment and Heritage (previously known as Environment Australia).
Figure 1. Historic catch data (in tonnes gutted weight) for holothurians on the Great Barrier Reef and adjacent areas. Early export data were converted from dry-weight (beche-de-mer product) using a conversion factor of 7.6 (combining data for Holothuria nobilis from FAO, 1989; Benzie and Uthicke, 2003). For most years from 1901 to 1940, only the value of the export is reported. These values were converted to weight by assuming an average value of 4.4 Australian Pound per cwt (= 50.8 kg). This figure is the average for the period between 1925 and 1940, derived from Australian export data. Values for the period between 1987 and 2003 are actual catch data obtained from Queensland Fisheries Service (see Fig. 2).
The remainder of this report will focus on the fishery in the Great Barrier Reef Marine Park, where, the main target species was the black teatfish (Holothuria nobilis). Initiated by a request from the fishing industry, and supported by data obtained through studies summarised here, the fishery on this species was closed in 1998. Nearly the entire fishing effort was concentrated north of Townsville (ca. 12°S to 19°S). The main management tool was a Total Allowable Catch (TAC, as gutted weight) of 500 tonnes. This TAC was not species specific, but most of the catch taken was black teatfish. The fishery was also entry-limited, with only about 18 license holders. Catch data provided by QFS (Figure 2), showed that the quota was never achieved, the maximum annual catch of black teatfish was about 360 tonnes.
Since 1994, annual catches declined and also catch rates per unit effort (CPUE) declined distinctly until the fishery for that species was closed (Figure 2). Since the closure of fishing for black teatfish, the fishery concentrated on the white teatfish (H. fuscogilva) and a TAC for this was set at 127 tonnes. This required a change in fishing method to SCUBA or hookah diving because white teatfish are found in deeper waters. In more recent years, fishermen have also collected prickly redfish (Thelenota ananas). The catch for this species increased 10-fold from about 7 tonnes in 1995 to 69 tonnes in 2000. Fishing for lower value species after overfishing of high value species is typical for holothurian fisheries and a clear indicator for over-exploitation. Unfortunately, this also appears to be the trend for the GBR, as fishery data prior to the closure of the black teatfish fishery (1998) contained very little catch of lower value species, whereas combined catches for all medium to low value species (excluding T. ananas) were 51 tonnes in 2001/2002 and 69 tonnes in 2002/2003.
Figure 2. Reported catch ofHolothuria nobilis in the Queensland fishery for the most recent fishing cycle (lefty-axis, bars), and catch per unit effort (right y-axis, line only for the last four years) of the fishery. The asterisk indicates that data from 1998 are only until the time of closure, thus not representing a whole year.
Why is fishery management important?
The primary aim of fishery management is the protection of the respective stock to provide for a continuing and sustainable income for the fishermen. However, in recent years management agencies increasingly take into consideration follow-on effects on other species and on the functioning of the entire ecosystem. This is mainly based on increased understanding of ecosystem functioning and understanding of interactions between trophic groups within these systems. Therefore, the function of holothurians in their ecosystem must also be understood to evaluate indirect impacts of the fishery.
All commercial holothurians are sediment feeders and consume vast amounts of sediments. Massin (1982a) and Birkeland (1988) suggested that the main functions of holothurians on coral reefs are bioturbation of sediments and the recycling of organic matter. Indeed, it has been shown that populations of two species can move the equivalent of the upper 5 mm of sand in their habitat once a year (Uthicke, 1999). This bioturbation is potentially important for the aeration and cleaning of the sediments and may extend the oxidized layer of these.
The main food sources of holothurians are bacteria, microalgae and dead organic matter (Yingst, 1976; Massin, 1982b; Moriarty, 1982). When holothurians are kept in densities above natural levels, they can reduce algal biomass (Moriarty, 1982; Uthicke, 1999). However, when natural densities were used in experiments, it was demonstrated that benthic microalgae on coral reefs have higher production in the presence of these animals (Uthicke and Klumpp, 1997, 1998; Uthicke, 2001b). The microalgae appear to benefit from enhanced nutrient levels resulting from the excretion of holothurians (Uthicke, 2001a). Since the production by microalgae on sands is an important component of the total production on coral reefs, it can be inferred that removal of holothurians can have negative effects on the total production.
Commercial holothurians in other ecosystems, such as H. scabra in seagrass beds, may have other functions such as increasing seagrass production or effecting seagrass densities by their burrowing behavior. To date, most studies have been done with species of low commercial value and further large-scale experiments are required to investigate if these effects are measurable after removal of holothurians through harvesting. However, findings from experimental studies indicate that heavy overfishing, particularly where species with little commercial value are also removed, has impacts on the productivity of the ecosystem.
Large-scale holothurian surveys on the GBR
Surveys on over 60 reefs along the entire (spanning 10 degrees of latitude) Great Barrier Reef (GBR) conducted in 1998/99 indicated that stocks of the black teatfish were generally lower in the southern part of the GBR (Figure 3). The zoning of the Great Barrier Reef Marine Park allowed a comparison between reefs that were fished and reefs protected from fishing (Green Reefs or No-Take Zones). Since the southern sections of the GBR were not fished, there is no difference in densities on open and protected reefs. In the northern two sectors, which represent the main fished area north of Townsville (ca. 12 °S to 19 °S) densities are distinctly higher on reefs which are No-Take Zones (Figure 3). A more detailed analysis showed that densities on each of the protected reefs are higher than on open reefs and this difference is highly significant (Figure 4, updated from Uthicke and Benzie, 2000, two additional reefs added from Uthicke and Byrne, unpublished data). On average, fishing has reduced the densities on the fished reefs by about 75 %, roughly from densities of 21 individuals per hectare down to 5 individuals. It cannot be concluded with certainty that densities found on No-Take reefs are natural densities, still somewhat reduced from previous fishing cycles (see above), or suffer from reduced larval recruitment due to fishing on other reefs.
Figure 3. Average densities of Holothuria nobilis in four sectors (sector 1: northern most sector; Sector 4: southern most), given for Protected Reefs (No-Take Zones) and Fished Reefs (open to fishing) of the Great Barrier Reef. Error bars indicate 1 SE.
Figure 4. Average densities ofHolothuria nobilis on 7 reefs closed to fishing (Protected Reefs = No-Take Zones) and 14 reefs open to fishing (Fished Reefs) in the Central and Northern sectors of the Great Barrier Reef. Error bars indicate 1 SE.
Re-surveys after Fishery closure
Nineteen reefs were re-surveyed in the formerly fished area, one and two years after the closure of the fishery, to determine if stocks recovered in that time. During this period, densities on No-Take reefs remained at a high level, one year (2000) and two years (2001) after the fishery closure (Table 1). No recovery was detected on the reefs previously fished. Densities on these 14 reefs remained on a level substantially below those on the No-Take Zones (Table 1). Although densities on previously fished reefs slightly increased, this increase was not statistically significant (Uthicke et al., in press). The fact that densities do not increase significantly indicates that little recruitment takes place.
Table 1. Individual densities per hectare (standard errors in brackets) ofHolothuria nobilis on the reef flat of five reefs closed to fishing (No-Take Zones) and 14 reefs open to fishing in the fished are of the Great Barrier Reef (North ofTownsville).
Estimating virgin biomass
GIS-based calculations indicate that about 25 % of the total available habitat area of H. nobilis was protected on No-Take Zones (Figure 5). Using area estimates and assuming "natural" densities as currently found on the No-Take zones, the initial ("virgin") biomass for the total area was estimated to be about 5 500 tonnes (Uthicke et al., in press). During fishing since the mid 1980s this biomass was reduced by 2 500 tonnes to 3 000 tonnes. More than half of the remaining H. nobilis biomass is now located on the No-Take reefs. The total reduction in stock size estimated from these calculations corresponds well to the reported catch of 2 000-2 500 tonnes during the fishing period (catch data from QFS; see Figure 2, Uthicke et al., in press).
Figure 5. Maps indicating the total habitat area ofHolothuria nobilis in the fished area of the Great Barrier Reef and the area protected from fishing ("No-Take zones"). About 25 % of the area is protected from fishing.
The results from the studies discussed here have three major implications for future management ofH. nobilis, and potentially other species, on the GBR and elsewhere.
(1) No-Take zones can provide an effective tool for stock protection of these species. However, whether the area protected on reefs mentioned above (ca. 25 %) was sufficient as a source of recruits for the whole area is currently unknown. In broadcast spawning invertebrates, the number of juveniles produced declines disproportionally when densities are reduced. This phenomenon is called the "Allee Effect" due to proximity of mates, and involves the problem of sperm dilution, the declining probability of sperm encountering eggs when animals are further apart (Levitan and Petersen, 1995). For example, a fourfold decline in densities as was seen in the fishery on the GBR, results in the doubling of the average distance between individuals of H. nobilis. Assuming animals are randomly dispersed, this means that average distances between animals increase from about 22 to 44 m. Applying a model developed for scallop populations, Claereboudt (1999) found that fishing scallops to 50 % of their original density reduced larval output of the population to 10 % of the initial value. Although not enough information on fertilization kinetics is known forH. nobilis, it may be assumed that populations fished to 25 % will have very limited larval output. These calculations suggest protecting sufficient spawners in No-Take zones may be a more efficient management tool than controlling Total Allowable Catch rates. However, if this were done it would still be necessary to investigate how many holothurians could be removed from fished areas without impacting on the ecological functioning of these areas.
(2) The agreement between reported catch and total reduction of numbers indicates that recruitment is very low and fishing has simply reduced stocks over more than a decade without appreciable replenishment. These data are corroborated by the fact that no recovery was discovered two years after the fishery closure and the fact that very few recruits or juveniles (animals < 500 g) where ever found during the course of these studies. It is uncertain if the small number of recruits is already a result of reduced larval output due to reduced adult density (see above), or a general feature ofH. nobilis populations of the GBR. Very few other studies on the recovery and recruitment in holothurian populations exist. One study in the Solomon Islands (Lincoln-Smith et al., 2000) detected very little or no recovery for several holothurian species after the declaration of a Marine Park. Similarly, sandfish stocks on the Warrior Reef complex had not recovered even four years after the fishery closure (Skewes et al., 2000). Further anecdotal evidence suggests that reefs are often not fished for several decades after the "boom" of a fishery, a situation that may arise from slow recovery of the stock.
(3) Annual catches of (on average) less than 5 % of virgin biomass distinctly reduced stocks ofH. nobilis on the GBR. This is in sharp contrast to notions that 50 % of virgin stock size might be taken annually (Long et al., 1996). This was based on the assumption of a natural mortality rate of 1 (equivalent to 37 % survival annually). Data collated here suggest that mortality rates are likely to be much smaller than that. These data, in conjunction with indications for very low growth rates of this species (Uthicke and Benzie, 2002; Uthicke et al., in press) and little recruitment as discussed above, suggest an extremely cautious approach should be taken in the management of this species, and potentially holothurian fisheries in general.
Recommendations and research needs
Unless indications for higher recruitment are shown, the TAC for H. nobilis should be below 5 % of virgin biomass.
To ensure sufficient production of juveniles, large areas should be set aside as No-Take zones.
Further research on the following topics is urgently required:
effects of density reduction on larval production in holothurians;
natural recruitment rates and recovery of populations after fishing;
growth, mortality and longevity of holothurians;
the effects of holothurian removal on ecosystem functioning in coral reefs and seagrass beds.
Until further data are available, fisheries should only continue with strict adherence to the precautionary principle. This may require a large percentage of the total habitat protected in No-Take zones and calculations of catch rates based on worst case scenarios.
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