Wild sea cucumber trade in rural Madagascar: Consequences for conservation and human welfare

Overexploitation of fisheries is a challenge to both marine conservation and human welfare. The trade of sea cucumbers is a multi‐billion‐dollar market, spanning over 70 countries. Global concern over unsustainable sea cucumber trade led to the inclusion of three species in CITES Appendix II, two of which are found in Madagascar (Holothuria fuscogilva and Holothuria nobilis). We used 792 structured interviews (2015–2020) to study the intensity of wild sea cucumber collection and exportation in rural northeastern Madagascar, where 30% of all (terrestrial and aquatic) native species are threatened with extinction. Wild sea cucumber collection was common and increased tenfold during the study; one in five coastal households caught and sold wild sea cucumbers. Furthermore, trade relied on threatened species; half of collected sea cucumbers are threatened, including CITES II‐restricted H. nobilis (Endangered) and H. fuscogilva (Vulnerable). While such collection threatens conservation, it improved the welfare of rural collectors. Sea cucumber collectors were significantly wealthier and more food secure than other community members. Given both the high collection of threatened and regulated species and high regional food insecurity (58% of households), the current regulation of threatened species alone is not reducing levels of unsustainable catch.

The Indian Ocean is one of the most biodiverse regions in the world, containing 30% of the world's coral reefs and the world's largest estuaries (Wafar et al., 2011).A lack of regulation in collection has led to the decline of many species across the region (Conand & Muthiga, 2007;Shahabuddin & Yoshimatsu, 2015).Specifically, concern over declines in threatened sea cucumber species led to the inclusion of three native Indian Ocean species within CITES Appendix II in 2019, necessitating national laws to regulate their trade (di Simone et al., 2021;Louw & Bűrgener, 2021).In the western Indian Ocean, sea cucumber fisheries have become common and there is evidence of CITES Appendix II species being overfished, possibly due to poor management and knowledge gaps about species ecology, extraction rates, and economic drivers (Bruckner et al., 2003;Eriksson et al., 2012).
Within the Indian Ocean, Madagascar is one of the largest exporters of sea cucumbers (Conand, 2017;Tridge, 2020).The largest global importers of sea cucumbers from Madagascar are Hong Kong, China, Malaysia, Singapore, and Taiwan (Anderson et al., 2011;Louw & Bűrgener, 2021;Pangestuti & Arifin, 2018).In the last decade, Hong Kong reported a global import value of nearly eight million kilograms of sea cucumbers (Conand, 2017).Madagascar is currently the high-valued exporter of sea cucumbers to Hong Kong, followed by Seychelles and Tanzania (Louw & Bűrgener, 2021).There are at least 122 recorded sea cucumber species in the coastal waters of Madagascar, and at least 30 species are collected (Conand & Muthiga, 2007;Rasolofonirina et al., 2003), two of which are protected through CITES Appendix II restrictions.Furthermore, national laws restrict the collection of sea cucumbers with a body length shorter than 11 cm (typical size at sexual maturity), or the sale of processed sea cucumber (dried) less than 8 cm (Arrêté No. 525 of the 5th of February 1975; Arrêté No. 4796/96 of 16th August 1990).However, these restrictions are rarely enforced, and regulations may not sufficiently protect species that reach sexual maturity before 11 cm, such as H. scabra (Conand & Muthiga, 2007;Yanti et al., 2020).Some of the most sought-after and expensive species are threatened, including H. scabra, H. fuscogilva, and H. nobilis (Conand, 2008).Approximately 1620 tons of sea cucumbers are exported from Madagascar yearly, yet only 12% are produced by aquaculture; thus, 88% of exported products are wild caught (Rasolofonirina et al., 2003;Tridge, 2020).Sellers accumulate wild product from multiple small communities where individuals collect sea cucumbers from waters near where they live.The various collected sea cucumber species are transported to regional centers and then sent to port cities such as Mahajanga, Toamasina (Tamatave), and Antalaha (Sea Rates, 2020).Understanding the motivation and scale of trade in local rural communities is therefore essential to assess and mitigate regional exploitation (Conand & Muthiga, 2007).
Here we examine the scale of wild sea cucumber collection for exportation in rural Madagascar over 6 years (2015)(2016)(2017)(2018)(2019)(2020).Specifically, we examine the scale of collection and how such trade affects sea cucumber conservation and human welfare.This multi-annual assessment of rural sea cucumber extraction is a key step toward developing strategies to address the incentives of resource users and mitigate the negative conservation effects of this marine trade product on vulnerable stakeholders.

| METHODS
We used extensive structured interviews of 792 households, and 1750 individuals aged 2 weeks to 91 years old, in eight coastal communities over 6 years (2015-2020) on Madagascar's largest coastal peninsula, the Masoala (Figure 1).BJR, Dr, and CB are fluent or native speakers of the local dialect of Betsimisaraka Malagasy.To determine the extent of wild sea cucumber collection we asked household members the number of each sea cucumber species they collected during the prior year.To examine the incentives for, and effects of, collection on human welfare we also asked participants about their household demographics, wealth, and food security.Interviews lasted 1-2 h.We surveyed all households in communities with 50 households or less.In communities with more than 50 households, we randomly selected study households by using a grid system in each village, assigning a number to each household in each grid, and selecting a subset of households in all quadrants using a random number array.To control the change in household numbers during the study, we repeated surveys of all households within our long-term study sites and controlled for study size changes within our analysis.That said, because households moved from and into the communities throughout the study, and because a subset of households was surveyed in large communities, caution should be used when interpreting results as the individuals surveyed may vary from year to year.Individuals provided information about prices in Malagasy Ariary (MGA), and we converted estimates of cash income to United States Dollar (USD) at the conversion rate at the time of data collection (mean US$ 1.00 = 3212.02MGA).

| Scale of sea cucumber trade and its potential effects on conservation
We asked households about the quantity and method of capture of 24 different species that include 14 locally recognized vernacular groups of collected sea cucumbers bought and sold during the prior year (Table 1).Local vernacular names are based on similar external phenotypes across multiple species (Data S1).For example, the local name traiktaira includes four scientific species within two genera, grouped due to similar external coloration and skin type.Participants recalled the number of catches from each vernacular group during the prior year.Of the 24 species collected, eight are threatened with extinction, including H. scabra, H. lessoni, H. nobilis, H. fuscogilva, and A. miliaris (Table 1).To examine the scale of the collection, we calculated both the total and mean (± standard deviation) number of whole individual sea cucumbers collected per household per year.We used linear regression analysis to test whether collection rates significantly increased or decreased over time.
To determine the conservation status of each local vernacular name, we identified each scientifically named species under the International Union for Conservation of Nature (IUCN) Red list.We took the Red list status of each scientific species within that local vernacular group   and converted that status to a 4-point numeric scale (where 4 is Critically Endangered, and 1 is Least Concern).Data-deficient species were excluded from these calculations, likely underestimating total risk.We used the mean and standard deviation of the threatened status of all scientific species to indicate the potential threatened status of local vernacular groups.We then calculated means and standard deviations of weights (dried product), as well as average numbers of whole individuals collected over the years (2015-2020).To understand the potential effects on conservation, we used a two-way T-test to determine if the increase (2015-2020) in the collection of threatened and CITES Appendix II protected species was significantly different from unregulated and least concern species.

| Effects on human welfare
To determine if sea cucumber collection improves human livelihoods, we measured two indicators of human welfare: wealth and food security.To quantify wealth, we asked individuals about how much they earned during the prior year from cash-generation activities (i.e.sales, land ownership, and trade).To quantify food security, we used a weighted Coping Strategies Index (CSI) (CARE, 2008) to measure changes in feelings, perceptions, and behaviors during the prior week in response to insufficient access to food (coping strategies).CSI weights were determined based on the qualitative perception of the severity of each coping strategy in each community (categorically ranked on a scale of 1-4).A CSI score of 0 reflects a household that perceives itself as food secure and higher CSI scores reflect greater perceived food insecurity.We defined a food insecure household as any household that could not access adequate food to feed their family for one or more days during the prior week.

| Scale of sea cucumber trade and its potential effects on conservation
Fishers sold 7187 kg of dry weight (9374 kg fresh weight) of sea cucumbers during the six-year study, and the collection of both overall and individual species increased (Table 2; Figure 1).From 2015 to 2020, fishers caught a total of 31,873 sea cucumbers, including 57.14% (8 of the 14) of local vernacular groups (Table 1; Data S1).Both the number and proportion of households that collected sea cucumbers increased throughout the study (R 2 = .08,χ 2 = 62.76, p < .0001).Continuously studied sites having nearly 10 times the number of collectors in 2020 as 2015, and the percentage of households engaged in the trade increasing from 6.9% to 50.0%.Despite this increase, each collector was also able to intensify their pressure, catching significantly more sea cucumbers over time (R 2 (141), F = 7.52, p = .0071).In fact, over a third (38.0%) of catch occurred during the final year of the study alone (Table 2).Fishers who went out to collect sea cucumbers snorkeled a mean 8.50 ± 5.84 (range: 0-60) times per month (at night), traveling 29.76 ± 20.59 (0.15-1200) minutes offshore to collect sea cucumbers at a depth of 6.72 ± 3.32 (0-30) meters.Most sea cucumber collectors were adult (91.78%) men (100%).Across all years, each household collected a mean of 48.59 ± 47.58 (range: 0-1400) sea cucumbers (Table 2).Local vernacular groups with a greater mean threatened score, tend to contain individuals that are sold at higher market prices, increasing their value on both economic and conservation scales (Table 1).

| Effects on human welfare
Collecting sea cucumbers improved both the food security and economic welfare of the households.While over half (58%) of coastal households were food insecure, those who collected sea cucumbers during the prior year were significantly more food secure than those who did not (T[257.16]= À3.18,p = .0017;4.83 ± 9.57 versus 7.88 ± 13.04 weighted CSI score, respectively; Data S2).
Sea cucumber collectors became wealthier than the general population for the first time in 2020, earning twice as much as those that did not (T[45.19]= 1.90, p = .03;$1341.68 ± 1995.14 USD vs. $693.29 ± 854.66 USD).A quarter of all income earned in 2020 (23.11 ± 33.89%) came from the sale of marine products (Data S3; Figure 2), and a fifth of this marine-based income (20.60 ± 31.61%) came from the sale of sea cucumbers (Data S4).While overall household income did not significantly increase during our study (R 2 (280) < .01,F = 2.48, p = .12),the proportion of income from fishing increased (R 2 (280) = .06,F = 17.33, p < .0001)as did the proportion of fishing income that came from sea cucumbers (R 2 (280) = .02,F = 7.02, p = .009).Salaried employment was insufficient and did not significantly reduce the likelihood that someone would collect sea cucumbers; in fact, households who collected sea cucumbers contained significantly more predictably salaried household members than those who did not (T[191.5]= 3.59, p = .0004;1.01 ± 0.99 vs. 0.68 ± 0.93 predictably salaried household members).Most (71.23%) fishers snorkeled to earn sufficient cash income; only 20.60% snorkeled with the primary intention to feed their household.Yet, people who collected sea cucumbers made most of their money from selling other ocean products with sea cucumbers comprised a third (35.36%) of all ocean-based income.
Over half (54.4%) of sea cucumber income came from threatened species (H.nobilis, H. fuscogilva, H. scabra, H. lessoni, A. echinites, A. miliaris, A. mauritiana, and Thelenota ananas), and of that, one-fifth from CITES Appendix II restricted species (H.nobilis and H. fuscogilva).Furthermore, the catch of Endangered species such as H. scabra, H. nobilis, and H. fuscogilva is increasing.CITES-restricted species have a disproportionate effect on benthic marine ecology (Bruckner et al., 2003).Sea cucumbers play crucial roles in their marine habitats as bioturbators and symbionts (Purcell et al., 2016;Zamora et al., 2018).Without them, bacterial build-up in sediments would have the potential to reduce water quality in already fragile ecosystems (Lee et al., 2017;Purcell et al., 2016;Zamora et al., 2018).Bioturbating species collected in northeastern Madagascar include the threatened H. lessoni and H. scabra, others such as H. fuscogilva and H. nobilis form crucial symbiotic relationships with crustaceans and annelids (Bruckner et al., 2003;Purcell et al., 2016).Thus, the reliance on these species will have ecosystem-wide consequences that affect fishers beyond sea cucumber collection.This pattern of overexploitation of the most threatened and key sea cucumbers within an ecosystem is not exclusive to northeastern Madagascar; such species are overexploited elsewhere, from southern Madagascar (McVean et al., 2005;Rasolofonirina et al., 2003) to the Great Barrier Reef (Wolfe & Byrne, 2022).Increased national regulation of sea cucumber collection on protected species will benefit marine regions both within and outside the Masoala Peninsula, yet alone it is unlikely to affect the incentives of collectors.
In a region characterized by high poverty and low food security, sea cucumber collection leads to increased wealth and food security.Those who collected sea cucumbers during the prior year became significantly wealthier and more food secure than those who did not.This is consistent with findings in the southwest of Madagascar and globally, where households depend on collecting sea cucumbers as part of their income by farming them in shallow waters (Al-Rashdi & Claereboudt, 2010;Purcell et al., 2018;Rasolofonirina et al., 2003;Zulfaqar et al., 2016).Yet, farming is not a viable option for collectors in many regions due to the lack of shallow waters they require.This leads to an increase in the collection of wild species, and yet we fail to see subsequent regulations that ensure sustainable catch.Such regulations, however, may reduce catch while increasing both food insecurity and poverty, as those who rely on sea cucumbers appear to have an increased reliance on cash income (as opposed to subsistence production).This may explain why households with salaried and employed members were more likely to collect sea cucumbers.As such, conservation initiatives that aim to reduce the reliance on land clearing for subsistence production may benefit from first increasing sustainable sources of cash-based income, lest they unintentionally increase the market sales of ocean resources to meet insufficient incomes.
Increasingly, coastal Malagasy collects wild sea cucumbers for a cash-based income in a growing and demanding global market.Because trade depends on threatened species, without intervention a crash in both the stocks of these species and the wealth and food security of their collectors is likely.Legislative tools that regulate the exportation of threatened sea cucumber species (e.g., CITES) are not, currently, affecting trade.Thus, additional economic tools at the national and local level may be needed to fully address incentives.If such actions ensure the long-term financial and food security of rural households, they may benefit collectors and marine ecosystems alike.However, these actions will only work if they truly reduce the collection of wild sea cucumbers in the face of an expanding and tempting economic market.
People may simply continue to collect sea cucumbers in addition to new economic opportunities if these opportunities are insufficient.Therefore, research that quantitatively tests the relative effects of various economic activities on sea cucumber collection is urgently needed.
T A B L E 1 The local and scientific names of collected sea cucumbers and their conservation status, mean threatened status, dried weight per kg, and price in local communities (2020) on the Masoala Peninsula in Madagascar.

F
I G U R E 2 Mean annual income (USD) by source and year in coastal northeastern Madagascar (2015-2020; 792 households).