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Ocean & Coastal Management 92 (2014) 87e94

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Ocean & Coastal Management journal homepage: www.elsevier.com/locate/ocecoaman

Assessment of sea cucumber populations from the Aegean Sea (Turkey): First insights to sustainable management of new fisheries Mercedes González-Wangüemert a, *, Mehmet Aydin b, Chantal Conand c a

Centro de Ciências do Mar (CCMAR), CIMAR e Laboratório Associado, Universidade do Algarve, Gambelas, 8005-139 Faro, Portugal Ordu University, Faculty of Marine Sciences, 52400 Fatsa, Ordu, Turkey c ECOMAR, Université de La Réunion, Saint-Denis de La Réunion, Paris 97715, France b

a r t i c l e i n f o

a b s t r a c t

Article history: Available online

Sea cucumber stocks have been overfished in many countries. As a consequence, several species (Holothuria polii, Holothuria tubulosa and Holothuria mammata) are now caught in Turkish waters without adequate knowledge on their biology and ecology. Here, we address their morphometry, relationships among gutted length and weight, population dynamics, temporal evolution of catches, and we provide the first insights about technical aspects of their fisheries. The largest size classes of H. polii are missing from our sampling collection, possibly due to the heavy fishery pressure on this species. Significant differences in the eviscerated length and weight were found among the Turkish sampled localities for H. polii and H. tubulosa, respectively. These differences could be explained by higher food availability in some areas and/or differential fishery pressure. The size and weight of H. tubulosa specimens were smaller than those registered for the same species in Greek waters, where this species is not fished. All the studied species showed allometric growth. In the last two years, the sea cucumber fishery in Turkey has been increasing rapidly, reaching a total production of ca. 555 000 kg in 2012 (80% H. polii and 20% H. tubulosa plus H. mammata). For a correct management of these species, we recommend: 1) the reestablishment of species-specific closed fishery season according to the specific reproductive cycle; 2) the assessment of the exploited stocks from the Northern Turkish coasts with estimates of recovery time of their populations; 3) the reduction of fishery efforts, mainly on H. polii and H. tubulosa and 4) the establishment of protected areas (where sea cucumber fisheries are forbidden) to conserve healthy populations which will favour the recruitment on nearby areas. Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction Sea cucumbers are key components in marine ecosystems and they represent a significant resource for coastal livelihoods. Ecologically, holothurians are important deposit and filter feeders and have significant roles, recycling nutrients, stimulating microalgae growth, and mixing the upper sediment layers (MacTavish et al., 2012). At least 66 species are fished from more than 40 countries and most of the harvests are processed in loco, and then exported to Asian markets (Purcell, 2010; Purcell et al., 2012a,b). Therefore, from both ecological and socioeconomic perspectives, the long-term sustainability of sea cucumber fisheries is of great importance to coastal communities.

* Corresponding author. Tel.: þ351 289 800 900x7355. E-mail address: [email protected] (M. González-Wangüemert). http://dx.doi.org/10.1016/j.ocecoaman.2014.02.014 0964-5691/Ó 2014 Elsevier Ltd. All rights reserved.

The present status and management of sea cucumber fisheries have been recently reviewed in five large regions of the world (Toral-Granda, 2008; Anderson et al., 2011; Purcell et al., 2012a,b). Tropical fisheries contribute the most to global captures, targeting many species with different ecological and biological traits. These fisheries are often artisanal, typified by fishermen catching sea cucumbers at low tide or free-diving on shallow reefs, and have operated for more than a century, albeit in a boom-and-bust fashion. Sea cucumbers are sometimes consumed locally, whereas most of the captures are boiled, dried and exported (Conand and Byrne, 1993). In contrast, in temperate waters most sea cucumber fisheries have only recently developed, they target single species and are industrialized, using large boats with sophisticated gear to harvest from deep waters. The total volume of the global harvests is difficult to obtain for many reasons, including the lack of speciesspecific declaration (sea cucumber captures are collectively reported and often combined with other marine invertebrates), unclear units chosen for reporting (e.g., dry weight vs. gutted weight),

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M. González-Wangüemert et al. / Ocean & Coastal Management 92 (2014) 87e94

Fig. 1. Map showing the sampling localities in Turkish coasts.

import and re-export activities in some countries, and exportation in various forms (e.g., salted, dried or frozen). However, it is has been estimated that the annual total global catch of sea cucumbers in form of live animals is around 100 000 tonnes (Purcell, 2010; Purcell et al., 2012a). Sea cucumber stocks have been overfished in many countries as a result of ever-increasing market demand, uncontrolled exploitation and/or inadequate fisheries management (Conand, 2000, 2004). The life-history traits of holothurians make them especially vulnerable to overfishing due to their low and infrequent recruitment, late age at maturity, high longevity, densitydependent reproductive success and slow growth (Uthicke et al., 2004). Furthermore, most sea cucumber fisheries fall in the class of “S-Fisheries”: small-scale, spatially structured and targeting sedentary stocks (Purcell, 2010). The overfishing of holothurian stocks from the Indo-Pacific has resulted in increased catches of Mediterranean and North-eastern Atlantic species, which were not previously considered economically important (Aydın, 2008; Sicuro and Levine, 2011; GonzálezWangüemert and Borrero-Pérez, 2012; González-Wangüemert et al., 2013a,b). Several of these sea cucumber species, such as H. polii (Delle-Chaije 1823), Holothuria tubulosa (Gmelin 1970) and Holothuria mammata (Grube 1840), inhabit the same area and show similar external morphology. They are thus very difficult to identify and differentiate. In the last few years, some molecular studies have allowed to improve our knowledge on their taxonomy, evolution and population genetics (Borrero-Pérez et al., 2009, 2010, 2011; Vergara-Chen et al., 2010; González-Wangüemert et al., 2011; González-Wangüemert and Borrero-Pérez, 2012). Nevertheless, there are still scarce available information about the life strategies, growth, population dynamics and catch of these species, targeted by new fisheries in the Mediterranean and in the Atlantic (Bulteel

et al., 1992; Coulon and Jangoux, 1993; Simunovic et al., 2000; Despalatovic et al., 2004; Ocaña and Tocino, 2005; GonzálezWangüemert et al., 2013a). Sea cucumber fishery in Turkish waters started in 1996 and focused mainly on H. polii, H. tubulosa and H. mammata, which are being exported to Asian countries as frozen, dried and salted products (Aydın, 2008; Aydın et al., 2011). This fishery is growing and has reached significant annual catches (ca. 77 000 kg; Aydın, 2008). However, to our knowledge, no study about the temporal evolution of these fisheries and their biological features in Turkey or in another Mediterranean places, has been published until now. Therefore, considering this background and the lack of basic information about these species, the main objective of our work is to provide a first insight on the population status of three sea cucumber species (H. polii, H. tubulosa and H. mammata), target by the Aegean fisheries in order to formulate initial recommendations towards sustainable management. Specifically, this study has four aims: 1) to assess the status of these three species analysing the distribution of size classes of their populations from different Turkish areas and their length/weight relationships; 2) to discuss the possible fishery effects on sea cucumbers populations; 3) to describe the temporal evolution of sea cucumber catches in Turkey during the last 10 years; 4) to suggest first recommendations towards sustainable management of the sea cucumber fishery in Turkey. 2. Materials and methods 2.1. Sampling This study was carried out in the Eastern Aegean Sea (39 300 1800 N, 26 290 4800 E; 38 100 1900 N, 26 250 0200 E) during the 2012

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Table 1 Summary of the data used in the lengtheweight relationship. (N: Number of individuals sampled; STD: standard deviation; Min: minimum value; Max: maximum value). N

H. polii H. tubulosa H. mammata

839 754 422

Length (cm)

Weight (g)

Average  STD

Min

Max

Average  STD

Min

Max

10.51  1.61 16.40  2.96 17.01  3.37

6.50 8.00 10.00

18.20 26.00 28.00

37.59  9.10 88.78  30.93 109.08  28.2

17.00 30.00 30.00

84.00 211.00 210.00

fishing season (Fig. 1). The sea cucumber sampling was done using the facilities offered by hookah diving vessels which are commercially operating in different Turkish localities (Ayvalik, Aliaga, Çesme, Foça, Izmir and Sakran). Live samples were transferred to the laboratory in sea water and under aeration conditions. We registered the total eviscerated length (EL) and gutted weight (EW) of each individual with an accuracy 0.01 cm and 0.01 g, respectively. To improve the accuracy of the measures, specimens were measured and weighted after death, once they were eviscerated and completely cleaned. We analysed 2015 individuals (839 H. polii; 754 H. tubulosa; and 422 H. mammata). Sea cucumber captures were authorized by the General Directorate of Fisheries and Aquaculture (GDAR) and by the Ministry of Food, Agriculture and Livestock (MoFAL) (http://www.tarim.gov.tr/ ). MoFAL is the public institute managing the sea cucumber fisheries in Turkey. In 2002, MoFAL established a closed fishery season for sea cucumber during the summer (1st August e 15th September) in the Northern Turkish coasts. This closed fishery season was maintained until 2007, when MoFAL published a new regulation allowing hand catch of sea cucumbers (using diving equipment) from the 15th of September to the 15th of July in the Northern Aegean Sea (Turkey). The Southern coast was closed to this fishery. Finally, in September 2012, MoFAL restricted the sea cucumber fishery in the Northern Aegean Sea and opened to this activity the Southern region, establishing a closed fishery season from June to October. During the samplings, MoFAL carried out interviews to fishermen about economical, social and technical aspects of this activity. Fishermen from fifty commercial sea cucumber fishing vessels working on the Aegean Sea coast from Turkey were interviewed face-to-face using the official questionnaire from GDAR.

Participants were informed of the study aims and that their answers would remain anonymous. Those participants giving consent were interviewed. In this study, we are using only the information concerning the technical characteristics of fishery vessels, duration/ depth of dives to catch sea cucumbers and number of employees per vessel. This information was verified in situ by one of the authors, Dr. Aydin who participated to the sampling and interviews. Economic and social data from these interviews were not used, because more accurate and complete information is necessary for a correct economic assessment of this activity in Turkey. Production data from the processing companies of sea cucumbers, which export nearly 90% of total product based on the GDAR records, were included as estimations of the sea cucumber catches in Turkish waters to assess their temporal evolution. 2.2. Statistical analysis The size classes (EL) for each species were represented using bar graphics. The relationship among gutted weight and length was established using the linear regression analysis EW ¼ a þ b (EL), where a is the intercept of the regression line (coefficient related to body form) and b the regression coefficient (exponent indicating isometric growth when equal to 3). The significance of the regression was assessed by F-statistic, and the b-value for each species was tested by the t-test to check if it was significantly different from the isometric growth (b ¼ 3) (Sokal and Rohlf, 1981). Also, we resorted to the linear models among two parameters (gutted length and weight) for each species. Differences in the length and weight parameters among localities for each species were tested by ANOVA considering “locality” as factor. Two-way ANOVA tests considering “locality” and “species” as factors, were

Fig. 2. Lengthefrequency distribution of our target species (Holothuria polii, H. tubulosa and H. mammata) along Turkish coast.

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M. González-Wangüemert et al. / Ocean & Coastal Management 92 (2014) 87e94 Table 2 Coefficients of the linear models (EW vs. EL) for each one of the three sea cucumber species. Significance of p codes: 0 ‘***’ 0.001 ‘**’ 0.01 ‘*’ 0.05 ‘ ’. Coefficients H. polii Intercept EL H. tubulosa Intercept EL H. mammata Intercept EL

Estimate

Std. error

t value

Pr(>jtj)

2.225 3.791

1.510 0.142

1.474 26.686

0.141