- Email: [email protected]
Fishery strategy affects the loggerhead sea turtle mortality trend due to the longline bycatch
Fisheries Research 212 (2019) 21–28
Contents lists available at ScienceDirect
Fisheries Research journal homepage: www.elsevier.com/locate/fishres
Fishery strategy affects the loggerhead sea turtle mortality trend due to the longline bycatch
T
⁎
José Carlos Báeza,b, , Salvador García-Barcelonac, Juan Antonio Camiñasc, David Macíasc a
Centro Oceanográfico de Canarias, Instituto Español de Oceanografía, Spain Investigador Asociado Facultad de Ciencias, Universidad Autónoma de Chile, Chile c Centro Oceanográfico de Málaga, Instituto Español de Oceanografía, Spain b
A R T I C LE I N FO
A B S T R A C T
Handled by George A. Rose
The western Mediterranean Sea is an important fishing ground for the Spanish surface longline fleet targeting swordfish, bluefin tuna, and albacore. Spanish Mediterranean waters, including contiguous international waters, are important feeding areas for thousands of juvenile and sub-adult loggerhead turtles. Due to the spatial overlap in fishing grounds between different longline métiers and loggerhead distribution, in the early 2000s, an estimated minimum of 60,000 loggerhead sea turtles were caught as bycatch in Mediterranean longline fisheries, including all countries operating in the area. The Spanish surface longline fleet is continually introducing technological and strategic innovations to improve the economic benefits of the fishery. These innovations lead to high variability in fishing gear and operational strategies from year to year. During the study period, there was a change in the specific contribution of each métier to total effort. Thus, since 2000 to the present, the Spanish traditional home-base surface longline targeting swordfish has been gradually modified or in other cases replaced by other métiers, and in most vessels it has been replaced by a new deeper semipelagic longline targeting the same species; which has led to a dramatic decrease in sea turtle mortality. The main result of this study is that loggerhead turtle post-release mortality due to the bycatch by the Spanish surface fleets using different longline métiers has significantly decreased during the last 8 years of the study period. We estimate an average post-release mortality around 1800 loggerheads sea turtles per year. The observed decrease in turtle mortality was an indirect effect of the introduction of changes in technology and fishing strategies in the fleets in the attempt to improve their economic objectives.
Keywords: Longline By-catch Métier Mediterranean Sea
1. Introduction The loggerhead turtle (Caretta caretta) is the most common sea turtle species in the Mediterranean Sea, where it utilizes nesting beaches mainly located in the eastern basin (Margaritoulis et al., 2003; Casale and Margaritoulis, 2010; Casale et al., 2018). Annually, hundreds of juvenile loggerhead turtles, born on the beaches of the North Atlantic Sea (Camiñas and de la Serna, 1995; Encalada et al., 1998; MonzónArgüello et al., 2010; Carreras et al., 2011) and the Mediterranean Sea, are concentrated around the feeding grounds in the Western Mediterranean, mainly in waters around the Balearic Islands (Camiñas and de la Serna, 1995; Carreras et al., 2011; Báez et al., 2014a). It has been suggested that the surface longline fishery is the major source of mortality in the Mediterranean Sea (Camiñas, 2004; Báez et al., 2006; Casale, 2011; Álvarez de Quevedo et al., 2013). The western Mediterranean Sea is an important fishing ground for
⁎
the Spanish surface longline fishery, targeting swordfish, Xiphias gladius, bluefin tuna, Thunnus thynnus, and albacore, T. alalunga (Camiñas et al., 2006; Báez et al., 2007a, 2007b; 2010; García-Barcelona et al., 2010a, 2010b; Báez et al., 2011, 2013). Due to the spatial overlap between longline fishing grounds and loggerhead distribution, in the early 2000s, an estimated minimum of 60,000 loggerhead sea turtles were caught as bycatch in longline fisheries in the entire Mediterranean Sea (Lewison et al., 2004). The Spanish Mediterranean longline fleet targeting swordfish and tuna species in the Mediterranean Sea (Table 1) employs a variety of gear (i.e. métiers), and is characterized by its use of different hook types, type and size of bait, and so on (see Camiñas et al., 2006; Báez et al., 2007a, 2007b; 2010; García-Barcelona et al., 2010a, 2010b; Báez et al., 2011, 2013). The Spanish longline métiers described for the Mediterranean fleet (see Table 1), according to ICCAT (The International Commission for the Conservation of Atlantic Tunas) are as follows: LLALB (longline
Corresponding author at: Centro Oceanográfico de Canarias, Instituto Español de Oceanografía, Spain. E-mail address: [email protected] (J.C. Báez).
https://doi.org/10.1016/j.fishres.2018.11.032 Received 17 May 2018; Received in revised form 19 November 2018; Accepted 20 November 2018 0165-7836/ © 2018 Published by Elsevier B.V.
Fisheries Research 212 (2019) 21–28
J.C. Báez et al.
Table 1 Summary of the métiers observed in the surface longline vessels of the Spanish fleet based in the Western Mediterranean Sea. Metiér
Name
LLALB LLAM LLHB LLJAP LLSP LLPB
Longline Longline Longline Longline Longline Longline
Albacore American Home-Base Japanese Semi-Pelagic Piedra y Bola
LLHB
LLALB
LLJAP
LLAM
LLPB
LLSP
% Coverture
2000 2001 2002 2003 2004 2005 2006 2007* 2008* 2009* 2010 2011* 2012 2013 2014 2015 2016
AV AV AV AV AV AV AV AV AV AV AV AV AV AV AV AV AV
AV NAV NAV NAV AV NAV AV AV AV AV AV AV AV AV AV AV AV
AV AV AV AV AV AV AV AV AV AV AV AV NAV 0 0 NAV AV
0 0 0 0 NAV NAV AV AV AV AV NAV AV AV AV 0 NAV NAV
AV AV AV AV AV NAV AV AV AV AV AV AV AV AV NAV AV AV
0 0 0 0 0 0 0 AV AV AV AV AV AV AV AV AV AV
8.7 4.6 3.9 2.7 4.0 1.3 3.9 3.0 4.0 5.4 5.5 5.7 7.6 9.0 6.4 5.2 5.9
Fishing depth and description
Albacore or little tunny Swordfish Swordfish Bluefin Tuna Swordfish Swordfish
Surface drifting longline Surface drifting longline Surface drifting longline Surface drifting longline Semi-Pelagic drifting longline Bottom longline
longline fishery on loggerhead turtles mortality and, in particular, to determine trends in the bycatch mortality of this species in the Western Mediterranean Sea due to the use of these métiers.
Table 2 Summary available observed data per métier and year. We showed the total percentage of coverture with scientific observers. Key: 0, not applicable; AV, data from scientific observers available; NAV, data from scientific observers non available. Year
Target species
2. Material and methods 2.1. Fisheries and bycatch data In 1997, the Spanish Institute of Oceanography (IEO) implemented an on board observer program in the commercial longline fleet targeting highly migratory species, and a landing monitoring network to obtain direct information and data on effort and catches of target and bycatch species (e.g. retained and discarded species, number of individuals, size, and other biological data) in relation to the different métiers used in the Mediterranean Sea. The information obtained is used to fulfil the requirements of the different Regional Fisheries Management Organizations, such as ICCAT (International Commission for the Conservation of Atlantic Tuna). The present study used data from 2000 to 2016 collected by the observer program mentioned above (for more information on this Spanish observer program, see Camiñas et al., 2006; Báez et al., 2007a,b,c, 2010; García-Barcelona et al., 2010a,b). The observed coverture is variable in function to the economic funds per year and available métiers (Table 3). E-logbook is a mandatory electronic recording and reporting system about fisheries data, which is including in the EU system for fisheries controls (https://ec.europa.eu/fisheries/cfp/control/technologies/ers_ en). It is a system where the skippers keep a record of fishing operations. The coverage in e-logbook is of 100%. Data compiled in e-logbooks was used to estimate the total annual effort of the fleet (expressed as number of hooks). Métiers were assigned to trips using the catch composition recorded in e-logbooks, and information provided by onboard observers, informants from the landing monitoring network, and surveys of fishermen. Thus, we obtained the total effort of the fleet expressed as the number of hooks per métier and year.
* Indicates the years with scientific observers in all métiers.
albacore), a surface longline targeting albacore and small tuna (depending on the distance to the coast); LLAM (longline American), a surface longline combined with a hydraulically-operated monofilament longline reel targeting swordfish; LLHB (longline home-base), the traditional surface longline targeting swordfish; LLJAP (longline Japanese), a surface longline targeting bluefin tuna; LLPB (longline piedra y bola), a bottom longline targeting swordfish; and LLSP (longline semipelagic), a drifting semipelagic longline targeting Swordfish at depths of 200–700 m or more in the water column. Briefly, the main differences in longline métiers are related to hook type and hook size (although for LLHB, LLAM, LLPB and LLSP is the same hook type and size model), bait type and size, operational depth and the time the hook takes to sink (Table 2). For a detailed review, see García-Barcelona et al., 2010a, 2010b), and Báez et al. (2013). Bycatch rates could be affected by technical differences in fisheries operations and gear configurations (e.g. hook and bait type, and the use or otherwise of lights) and the fishing strategies used (e.g. period of the year, times of hauling and retrieval, distant to the base port, and fishing depths) by Spanish Mediterranean longliners (Camiñas et al., 2006; Báez et al., 2007a, 2007b; Báez et al., 2010). Thus, Báez et al. (2013) estimated that each métier type affected the loggerhead bycatch rate. Thus, métier types should be taken into account when estimating loggerhead bycatch (Báez et al., 2014b). Furthermore, the Spanish surface longline fleet is continually making technological and strategic innovations to improve the economic benefits of the fishery (Báez et al., 2013). The main aim of the present study was to estimate the mortality of loggerhead turtle due to the bycatch by the Spanish longline fleet during the period 2000–2016, while taking into account the historic development and changes of the métiers used during this period. The final goal was to understand the effect of changes in the Spanish
2.2. Statistical analysis In a first step, we estimated the annual average bycatch of loggerhead turtles using two different approaches: 1) by taking into account the average loggerhead bycatch and the average number of hooks for the entire period 2000–2016 per each métier separately; and 2) by estimating the average loggerhead turtle bycatch and the average number of hooks for each year and métier. The annual loggerhead turtle bycatch of a particular year and métier (ALBy), according to the first approach can be expressed as: ALBy = (R/h)*H Where R is the average loggerhead bycatch observed (i.e. average number of turtles caught) for the entire period 2000–2016 per each métier (i); h is the average of hooks observed for the entire period 2000–2016 per each métier (i), and H is the total annual effort of the fleet (expressed as number of hooks). The annual loggerhead turtle bycatch of a particular year and métier (ALBy), according to the second approach can be expressed as: 22
Fisheries Research 212 (2019) 21–28
J.C. Báez et al.
Table 3 Principal characteristics of the métiers observed in the surface longline fleet of the Spanish fleet based in the Western Mediterranean Sea. 1Indicates that they are the same hooks. Gear
LLHB
LLAM
LLSP
LLPB
LLJAP
LLALB
Hooks (N) Hooks form Weights in branchline or mainline Hook size (cm) Depth at sea (m) Baits
1500-4000 J1 No
≈ 1000 J1 Yes
≈ 2500 J1 Yes
600-1000 J1 Yes
250-1100 C No
2000 - 5000 J No
7.5 × 2.5 ≈ 40 - 70 mackerel, small mackerel, chub mackerel, atlantic saury, round sardinella, silver scabardfish or squid
7.5 × 2.5 ≈ 50 - 90 mackerel, chub mackerel, squid, round sardinella or artificial mackerel and squid
7.5 × 2.5 ≈ 200 - 700 mackerel, chub mackerel, squid, round sardinella or plastic mackerel and squid
7.5 × 2.5 ≈ 250 - 350 mackerel, chub mackerel or silver scabardfish
7.5 × 3.0 ≈ 50 - 90 great mackerel, great squid or bogue
4.3 × 1.7 ≈ 20 - 50 sardine and round sardinella
Fig. 1. Distribution of the Spanish longline fishing effort observed over the entire period 2000–2016.
affect its abundance and distribution. For this reason, we decided to also use the second approach. Thus, to fill in years with no data, we extrapolate the mean for years of the immediately anterior and posterior. However, when the gap was very large, a number of years similar to the size of the gap were used. In a second step, we estimated direct mortality and post-release mortality. The direct mortality was estimated from the data provided from the observer program of the IEO. In the periods 1999–2004 (reported in Camiñas et al., 2006) and 2009–2016 the observers recorded, when possible, the situation (alive or dead) of the turtle hooked in the longline. We used the ratio number of dead turtles divided per total number of observed bycatch turtles per métier for both periods together. The observed ratios per métiers are: LLHB = 10/1849, LLAM = 15/370, LLSP = 2/4, LLPB = 0/1, LLJAP = 14/807, LLALB = 16/1027. We used the post-release mortality probability during the 90 days following release (ranged from 0.308 to 0.365) estimated by Álvarez de Quevedo et al. (2013), to estimate mortality per year (TMy) according to the expressions:
ALBy = (Fy/hy)*H Where Fy is the average loggerhead bycatch observed (i.e. average number of turtles caught) for a particular year per each métier (i); h is the average of hooks observed for a particular year per each métier (i), and H is the total annual effort of the fleet (expressed as number of hooks). Subsequently, the estimated total number of turtle bycatch per year (By) is the sum of the estimated bycatch of each métier calculated in these two ways (ALBy): n
By =
∑ ALByi i
Moreover, we calculated the 95% confidence interval (C.I.) from the standard error of the mean observed for each métier and period (i.e. the total or per year) (Sokal and Rohlf, 1995). The first approach has the advantage of eliminating possible bias due to poor coverage in some métiers during some of the study years. However, a drawback of this method is that it assumes a constant abundance of sea turtle in the area. However, in line with Camiñas and de la Serna (1995) and Báez et al. (2014a), there may be annual variations in the total number of loggerhead turtles caught as bycatch due to migration to the study areas and to global climatic conditions that
TMy minimum = 0.308*By ± 95% C.I.; TMy maximum = 0.365* By ± 95% C.I.
23
Fisheries Research 212 (2019) 21–28
J.C. Báez et al.
Fig. 2. Trends in Spanish longline fishing effort per métier over the study period.
year (March, October, and November). During the study period, there was a change in the specific contribution of each métier to total effort (Fig. 2). Thus, from 2000 to 2005, the fishing effort was dominated by LLHB, but since 2005 other métiers have gained ground, such as LLAM. Since 2007, and mainly in the summer months, the métier LLHB has decreased in importance due to the introduction of LLSP. There was also a change in effort of LLALB due to fishing market conditions. We estimated an average of 5317 loggerhead sea turtle bycatch per year (i.e. mean ALBy) based to the approach 1 (maximum mean of 6457 individuals and a minimum mean of 4220 individuals). However, we estimated an average of 5565 loggerhead sea turtle bycatch per year (i.e. mean ALBy) based on approach 2 (i.e. a maximum mean of 8198 individuals and a minimum mean of 3063 individuals). In contrast to the study by Báez et al. (2013), over the entire study period, the main estimated bycatch was by LLHB métiers. We estimated an average of nearly 3000 loggerhead sea turtles per year by the LLHB métier versus 833 loggerhead sea turtles per year by the LLALB over the entire study period. The differences between the two approaches could be due to the standard error and gaps in the annual sampling effort of métiers (Tables 4 and 5). Both approaches showed a significant correlation (r = 0.87, P < 0.001). In a second step, we estimate direct and post-release mortality per year (TMy) according to the expressions explicated above. We observed a low direct mortality for all métiers pooled together per year. Thus according to the approach 1 the mean of the averages of the sea turtles directly dead in the longline was 72 sea turtles, while according to the approach 2 were 82 sea turtles directly dead. We estimate a total mortality average (i.e. direct and post-release mortality) of 1861 loggerhead sea turtle per year based to the approach 1 (maximum mean of 2482 individuals and a minimum mean of 1347 individuals), and average of 1955 loggerhead sea turtle per year based to the approach 2 (maximum mean of 3126 individuals and a minimum mean of 978 individuals). Both approaches showed that there was a significant downward trend (Figs. 3 and 4) in annual turtle mortality, with a significant negative time relation (for the approach 1: R2 = 0.896, P < 0.0001; for the approach 2: R2 = 0.724, P < 0.0001). According to the results from GLMs (Table 6) LLSP is the variable that more reduced the mortality.
Table 4 The global average loggerhead bycatch and mean of the number of hooks for the entire period 2000–2016 per each métier. Métier
N
Turtle mean
Standard error
Hooks mean
LLALB LLHB LLJAP LLSP LLPB LLAM
1236 1803 486 1279 382 121
0.8220 1.3494 1.6564 0.0063 0.0105 0.6860
3.00806 3.99735 4.09012 0.78870 0.12505 2.11750
2746.34 2359.99 1265.23 1988.67 1196.85 1186.24
Key: N, number of sets observed; Turtle mean, mean of the loggerhead sea turtle bycatch observed per set; Standard error, the standard error for the turtle mean; Hooks mean, mean observed hooks per set.
Thereby, we applied a fixed post-release mortality rate. In this case, we assumed that the mortality rate per métier is constant and equal in all métiers. However, this could be only assumed for LLHB, LLAM, LLSP and LLPB, that used the same hook size and type, while LLALB and LLJAP used different hooks. Finally, we summed the direct and postreleased mortality. We use General Linear Models (GLMs) to evaluate the effect of métiers in the sea turtle mortality. For this, we performed GLMs for each dependent variable (approach 1, and approach 2) versus the interaction to the independent variables: LLSP, LLAM, LLHB, LLPB, LLALB, LLJAP, and year. We assessed the parsimony of the GLMs using the Akaike information criterion (AIC) (Akaike, 1973). 3. Results During the study period, the Mediterranean Spanish surface longline fleet decreased from approximately 90 authorized vessels in 2000 to 73 vessels in 2016. The length of the vessels ranged from 12 to 27 m LOA (Overall Length). Until the mid-2000s, the artisanal fleet could also fish for large pelagic fishes, and the number of longliner vessels operating in the area could increase to just over 100. The fishing trips were often of short duration (i.e. 1 day to 8 days, depending on métiers and LOA). Fig. 1 shows the observed effort of the fleet. This fleet fished on a yearround basis, targeting different species until the implementation of temporary closure for swordfish in 2008 (ICCAT Recommendation 0701). Between 2008 and 2016, the fleet stopped fishing for 3 months per 24
25
0 0 71 8 0 4 0 0 0 0 0 0 71
0.6862 0.6862 1.043 0.875 0.6862 0.5 0.6862 0.6862 0.6862 0.6862 0.6862 0.6862 1.043
Turtle mean
2.1182 2.1182 2.637 1.81 2.1182 0.577 2.1182 2.1182 2.1182 2.1182 2.1182 2.1182 2.637
S.E.
1186.242 1186.242 1195.73 870 1186.242 1100 1186.242 1186.242 1186.242 1186.242 1186.242 1186.242 1196
Hooks
N 93 34 29 46 40 56 20 56 20 7 74 3 0 0 0 26 8
Turtle mean 3.699 8.35 1.1034 1.457 0.825 0.125 0.15 0.3036 0.55 0 0.0946 0 0.163 0.163 0.163 0.16 0
LLJAP S.E. 5.307 9.085 1.74 1.39 1.5 0.384 0.366 0.537 0.759 0 0.0946 0 0.213 0.213 0.213 0.21 0
Hooks 1584 1738 2066 1697 1376 959.5 910 998 1222 959 629 167 7443 7443 7443 744 0
N 337 220 119 122 213 41 66 85 116 95 99 12 122 53 47 14 42
LLHB Turtle mean 3.45 1.577 0.689 2.48 2.038 0.927 0.61 0.3411 0.18 0.421 0.303 0 0.0082 0.0566 0 0 0
S.E. 6.3014 3.3061 1.582 6.95 3.9774 2.75 0.298 0.795 1.169 0.41 0.224 0 0.091 0.305 0 0 0
Hooks 3069 2963 3567 2188 1327 1438 2066 2597 2044 2474 2536 2000 1539 1919 1608 1986 1097
N 13 1 19 8 15 36 21 84 43 50 45 11 18 44 0 10 0
LLPB Turtle mean 0 0 0 0 0 0.0833 0.1429 0 0 0 0 0 0 0.0227 0.0114 0 05
S.E. 0 0 0 0 0 0.368 0.478 0 0 0 0 0 0 0.151 0.0764 0 05
Hooks 1477 2000 2098 1704 1957 1721 1553 939 796 1100 1234 1739 958 1065 10124 1373 13735
LLSP
5 119 178 90 215 125 225 125 62 135
N
Key: N, number of sets observed; Turtle mean, average loggerhead sea turtle bycatch observed; S.E., the standard error for the turtle mean; Hooks mean, mean observed hooks per set. 1 Estimated figures using data from 2000, 2004, 2006, and 2007. 2 Estimated figures using data from 2006, 2007, 2009, and 2016. 3 Estimated figures using data from 2008, 2009, 2010, and 2011. 4 Estimated figures using data from 2012 and 2013. 5 Estimated figures using data from 2015.
Hooks 2664 28831 28831 28831 2175 28831 3558 2422 2600 3022 3010 2732 2571 2935 2834 2721 2466
N
S.E. 4.43 4.561 4.561 4.561 4.56 4.561 5.65 2.95 0 2.73 8.16 0.59 1.86 1.54 0.175 0.148 0.306
N 7 0 0 0 40 0 69 36 26 49 73 124 206 170 159 179 98
2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016
Turtle mean 7.7143 2.2431 2.2431 2.2431 0 2.2431 3.49 1.278 0 1.327 4.534 0.12 0.888 0.4059 0.0314 0.0223 0.306
LLAM
LLALB
Year
Table 5 Estimations of average loggerhead turtle bycatch and average number of hooks per year and métier.
0 0.0336 0 0 0.0047 0 0.0133 0 0 0
Turtle mean
0 0.18 0 0 0.07 0 0.12 0 0 0
S.E.
2020 1323 1706 2003 2214 1902 1820 2142 2542 2542
Hooks
J.C. Báez et al.
Fisheries Research 212 (2019) 21–28
Fisheries Research 212 (2019) 21–28
J.C. Báez et al.
Fig. 3. Annual loggerhead sea turtle mortality per year (all métiers pooled together) based on the global average loggerhead bycatch for the entire period 2000–2016 per métier.
Fig. 4. Annual loggerhead sea turtle mortality per year (all métiers pooled together) based on the average loggerhead bycatch per métier and year. Table 6 Results from the General Linear Models for the mortality of sea turtle, according to the approaches 1(annual loggerhead sea turtle mortality per year -all métiers pooled together- based on the average loggerhead bycatch per métier) and 2 (annual loggerhead sea turtle mortality per year -all métiers pooled together- based on the average loggerhead bycatch per métier and year). Approach
Interaction
AIC
Omnibus test signification
Approach 1
LLJAP*LLALB*LLPB*LLHB LLJAP*LLALB*LLPB*LLHB*LLAM LLJAP*LLALB*LLPB*LLHB*LLAM*LLSP LLJAP*LLALB*LLPB*LLHB*LLAM*LLSP*year LLJAP*LLALB*LLPB*LLHB LLJAP*LLALB*LLPB*LLHB*LLAM LLJAP*LLALB*LLPB*LLHB*LLAM*LLSP LLJAP*LLALB*LLPB*LLHB*LLAM*LLSP*year
141.826 142.046 151.946 103.812 159.34 159.494 165.810 126.317
< 0.0001 < 0.0001 0.096 < 0.0001 0.009 0.009 0.502 < 0.0001
Approach 2
26
Fisheries Research 212 (2019) 21–28
J.C. Báez et al.
4. Discussion
A comparable situation appeared in Italy, when the surface longline fleets also changed the métiers targeting swordfish. In 2010, the traditional surface longline was substituted by a new mesopelagic longline in the southern Italy swordfish fishery (i.e. in the Ligurian Sea and Ionian Calabria). The impact of this new gear on protected or endangered species, such as sea turtles, was absolutely negligible (Cambiè et al., 2013; Garibaldi, 2015). In addition, the size of the turtles caught varies according to the métier used. According to Báez et al. (2013), turtles caught on longline gear targeting albacore and small tunas are smaller than turtles caught using longline gear targeting bluefin tuna and swordfish. Several studies have analysed best practices to reduce loggerhead bycatch from longline fisheries (Gilman et al., 2006; Báez et al., 2007b). However, as shown by results from the western and central Mediterranean Sea (i.e. near Spain and Italy), by only modifying the depth of fishing (i.e. leaving the longline at a depth inaccessible to sea turtles), the bycatch of loggerhead turtles can be reduced by up to 99.5% compared to the percentages caught on other métiers such as LLHB. The introduction in Spanish and Italian surface longline vessels of new gear and fishing strategies targeting swordfish has decreased both captures and the fishing mortality of loggerhead turtles and other species. However, these new métiers could target large individual swordfish, which could have negative consequences for Mediterranean swordfish stocks if there is a reduction in the number of reproductive individuals such that the stocks cannot be sustained (for example, Cambiè et al., 2013; Garibaldi, 2015). Moreover, the new métiers could bycatch other species with slow growth and retarded maturity, such as Zu cristatus (García-Barcelona et al., 2016). This aspect could be the topic of further research.
Surface longline fishing involves the use of a suite of gear targeting different species. The efficiency of the gear varies according to the target species. However, bycatch rates also vary depending on a range of technological and strategic approaches. Changes in the métiers are driven by established Spanish and EU management measures and the economic revenues of the fleets. During the study period, the traditional home-base surface longline targeting swordfish métier (LLHB) used by the Spanish Mediterranean fleet was partially replaced, initially by the American longline (LLAM), and subsequently by the semipelagic longline métier (LLSP) targeting the same species. Thus, the incorporation of the LLAM could explain the upward trend between 2003 and 2005, whereas the incorporation of the LLSP in 2007 could explain the downward trend observed since this year. This last trend was increased by the fact that the LLSP replace the LLHB mainly in summer season, when the impact of LLHB on sea turtles is higher in the area (Báez et al., 2007a, 2007b). The mean of the averages the loggerhead sea turtles bycatches in the period 2000–2003 was estimated to be about 8800 (according to the approach 1), and 11,800 (according to the approach 2). These estimations are similar to the reported by Álvarez de Quevedo et al., (2013) but discussed by Báez et al., (2014a, 2014b). The scientific observer program it's very expensive, it is no possible to on-boarding the scientific observers in all métiers every year. Thus, the years with real data for all métiers are only 4 (Table 3). For this reason, we have filled the gaps with no data. We considered that this could be a weakness of the analysis. Moreover, both approaches showed a high oscillation in their estimations, which were highest to end of the time series, thus in the period 2015-2016. According to the approach 1, the mortality rate was estimated to be, on average, 1000 loggerhead sea turtles but, according the approach 2, it was, on average, 50 in the same period. Consequently, these estimations should be used with caution. However, despite the differences of the two approaches, they show an important decreasing in the mortality trend due to longline bycatch. Thus, the veterinarians from the marine recovery centers observed a decrease in the causes of strandings loggerhead death due to the longline fisheries (Jiménez et al., 2017), confirming our results. This study presents an updated estimation of loggerhead sea turtle mortality due to the bycatch by métier in the Spanish Mediterranean longline fleet. Each bycatch event is customarily considered as affecting a different individual; even when there is evidence of released turtles being caught again on other nearby longlines (e.g. see Tomas et al., 2001). For this reason, the bycatch and mortality estimates presented in this study represent hypothetical maximum values. There are different direct mortality rate in function to métier type. Thus, we observed that direct mortality in LLSP is about 50%, while LLPB, LLHB and LLAM showed the percentage lowest. Nevertheless, the direct mortality per year is very low. During the last 8 years, there has been a significant decrease in the bycatch of loggerhead turtles by the Spanish surface fleets using different métiers. There is a strong correlation between the use of the new métiers and the decreasing numbers of loggerhead sea turtle as bycatch, with the potential positive effect of increasing the number of loggerheads of reproductive age in the Mediterranean and Atlantic populations present in the Spanish fishing grounds. However, the decrease in bycatch is not due to the implementation of new management actions to reduce the bycatch of sea turtles or other protected species; rather, it is due to the collateral effect of the introduction of technical changes in fishing gear and to changes in fishing strategies based on the economic objectives of each fleet. If the reduction in turtle bycatch is due to changes in the main gear used and the related fishing strategy (mainly due to deeper sets, and a significant reduction in the time the hook takes to sink), then forthcoming technological changes or the implementation of other fishing strategies by the fleet could reverse the current situation.
Acknowledgements This article is offered In Memoriam of the recently deceased Dr. Giulia Cambié, an Italian colleague who studied the Mediterranean fisheries and marine turtle bycatch. For some time she worked in Spain and in collaboration with our team. The onboard observer program in commercial longline vessels was supported by different projects from the IEO based in Malaga, GPM-4 programs (IEO). This project has been co-funded by the EU through the European Maritime and Fisheries Fund (EMFF) within the National Program of collection, management and use of data in the fisheries sector and support for scientific advice regarding the Common Fisheries Policy. We thank the IEO scientists and the captains and crews of the different research and leisure vessels who were involved in the onboard observation program of the IEO. We are grateful to three anonymous reviewers, for insightful comments that improved the manuscript. References Akaike, H., 1973. Information theory and an extension of the maximum likelihood principle. Petrov, B.N., Csaki, F. (Eds.), Proceedings of the Second International Symposium on Information Theory 267–281. Álvarez de Quevedo, I., San Félix, M., Cardona, L., 2013. Mortality rates in bycaught loggerhead turtle Caretta caretta in the Mediterranean Sea and implications for the Atlantic populations. Mar. Ecol. Prog. Ser. 489, 225–234. Báez, J.C., Camiñas, J.A., Rueda, L., 2006. Accidental fishing capture of marine turtles in South Spain. Mar. Turtle Newsl. 111, 11–12. Báez, J.C., Real, R., Camiñas, J.A., 2007a. Differential distribution within longline transects of loggerhead and swordfish captured by the Spanish Mediterranean surface longline fishery. J. Mar. Biol. Assoc. U.K. 87, 801–803. Báez, J.C., Real, R., García Soto, C., de la Serna, J.M., Macías, D., Camiñas, J.A., 2007b. Loggerhead turtle bycatch depends on distance to the coast, independent of fishing effort: implications for conservations and fisheries management. Mar. Ecol. Prog. Ser. 338, 249–256. Báez, J.C., Real, R., Macías, D., de la Serna, J.M., Bellido, J.J., Camiñas, J.A., 2010. Swordfish Xiphias gladius Linnaeus1758 and loggerhead Caretta caretta (Linnaeus 1758) captures associated with different combinations of bait in the Western Mediterranean surface longline fishery. J. Appl. Ichthyol. 26, 126–127. Báez, J.C., Real, R., Bellido, J.J., Macias, D., de la Serna, J.M., Camiñas, J.A., 2011. Validating an ecological model with fisheries management applications: the relationship between loggerhead bycatch and distance to the coast. J. Mar. Biol. Assoc.
27
Fisheries Research 212 (2019) 21–28
J.C. Báez et al.
Encalada, S.E., Bjorndal, K.A., Bolten, A.B., Zurita, J.C., Schroeder, B., Possardt, E., Sears, C.J., Bowen, B.W., 1998. Population structure of loggerhead turtle (Caretta caretta) nesting colonies in the Atlantic and Mediterranean as inferred from mitochondrial DNA control region sequences. Mar. Biol. 130, 567–575. García-Barcelona, S., Ortiz de Urbina, J.M., de la Serna, J.M., Alot, E., Macías, D., 2010a. Seabird by-catch in Spanish Mediterranean large pelagic logline fisheries, 1998–2008. Aquat. Living Resour. 23, 363–371. García-Barcelona, S., Macías, D., Ortiz de Urbina, J.M., Alba, E., Real, R., Báez, J.C., 2010b. Modelling abundance and distribution of seabird by-catch in the Spanish Mediterranean longline fishery. Ardeola 57, 65–78. García–Barcelona, S., García–Cancela, R., Cayuela Fernández–Peralta, L., de Carlos, M.J., Bañón, R., Macías, D., Báez, J.C., 2016. Descripciín de dos ejemplares de Zu cristatus (Bonelli, 1820) capturados accidentalmente con un palangre semipelágico en el Mediterráneo occidental. Arx. Misc. Zool. 14, 91–98. Garibaldi, F., 2015. By-catch in the mesopelagic swordfish longline fishery in the Ligurian Sea (Western Mediterranean). Collect. Vol. Sci. Pap. ICCAT 71 (3), 1495–1498. Gilman, E., Zollet, E., Beverly, S., Nakano, H., Davis, K., Shiode, D., Dalzell, P., Kinan, I., 2006. Reducing sea turtle bycatch in pelagic longline fisheries. Fish Fish. 7, 2–23. Jiménez, J., Gómez, J.A., Eymar, J., Gago, C., 2017. Cambios en las causas de mortalidad de las tortugas marinas. Quercus 381, 28–35. Lewison, R.L., Freeman, S.A., Crowder, L.B., 2004. Quantifying the effects of fisheries on threatened species: the impact of pelagic longlines on loggerhead and leatherback sea turtles. Ecol. Lett. 7, 221–231. Margaritoulis, D., Argano, R., Baran, I., Bentivegna, F., Bradai, M.N., Camiñas, J.A., Casale, P., De Metrio, G., Demetropoulos, A., Gerosa, G., Godley, B.J., Haddoud, D.A., Houghton, J., Laurent, L., Bojan, L., 2003. Loggerhead turtles in the Mediterranean: present knowledge and conservation perspectives. In: Bolten, A.B., Witherington, B.E. (Eds.), Loggerhead Sea Turtles. Smithsonian Institution Press, Washington, DC, USA, pp. 175–198. Monzón-Argüello, C., Rico, C., Naro-Maciel, E., Varo-Cruz, P., López, A.M., López-Jurado, L.F., 2010. Population structure and conservation implications for the loggerhead sea turtle of the Cape Verde Islands. Conserv. Genet. 11 (5), 1871–1884. Sokal, R.R., Rohlf, F.J., 1995. Biometry, 3rd edition. W.H. Freeman and Co, New York. Tomas, J., Dominici, A., Nannarelli, S., Forni, L., Badillo, F.J., Raga, J.A., 2001. From hook to hook: the odyssey of a loggerhead sea turtle in the Mediterranean. Mar. Turtle Newsl. 92, 13–14.
U.K. 91, 1381–1383. Báez, J.C., Macías, D., Camiñas, J.A., Ortiz De Urbina, J.M., García-Barcelona, S., Bellido, J.J., Real, R., 2013. Bycatch frequency and size differentiation in loggerhead turtles as a function of surface longline gear type in the western Mediterranean Sea. J. Mar. Biol. Assoc. U.K. 93, 1423–1427. Báez, J.C., Macías, D., García-Barcelona, S., Real, R., 2014a. Interannual differences for sea turtles by-catch in Spanish longliners from Western Mediterranean Sea. Sci. World J. https://doi.org/10.1155/2014/861396. Báez, J.C., García-Barcelona, S., Real, R., Macías, D., 2014b. Estimating by-catch of loggerhead turtles in the Mediterranean: Comment on Álvarez de Quevedo et al. Mar. Ecol. Prog. Ser. 504, 301–302. Cambiè, G., Muiño, R., Mingozzid, T., Freire, J., 2013. From surface to mid-water: is the swordfish longline fishery “hitting rock bottom”? A case study in southern Italy. Fish. Res. 140, 114–122. Camiñas, J.A., 2004. Sea turtles of the Mediterranean Sea: Population Dynamics, Sources of Mortality and Relative Importance of Fisheries Impacts. FAO Fisheries Report 738. pp. 27–84. Camiñas, J.A., de la Serna, J.M., 1995. The loggerhead distribution in the western Mediterranean Sea as deduced from captures by the Spanish longline fishery. In: Llorente, G.A., Montori, A., Santos, X., Carretero, M.A. (Eds.), Scientia Herpetologica. Asociación Herpetológica Española, Barcelona, pp. 316–323. Camiñas, J.A., Báez, J.C., Valeiras, X., Real, R., 2006. Differential loggerhead bycatch and direct mortality in surface longline according to boat strata and gear type. Sci. Mar. 70, 661–665. Carreras, C., Pascual, M., Cardona, L., Marco, A., Bellido, J.J., Castillo, J.J., Tomás, J., Raga, J.A., Sanfélix, M., Fernández, G., Aguilar, A., 2011. Living together but remaining apart: Atlantic and Mediterranean loggerhead sea turtles (Caretta caretta) in shared feeding grounds. J. Hered. 102, 666–677. Casale, P., 2011. Sea turtle bycatch in the Mediterranean. Fish Fish. 12 (3), 299–316. Casale, P., Margaritoulis, D., 2010. Sea Turtles in the Mediterranean: Distribution, Threats and Conservation Priorities. Gland, Switzerland IUCN 294 pp. Casale, P., Broderick, A.C., Camiñas, J.A., Cardona, L., Carreras, C., Demetropoulos, A., Fuller, W.J., Godley, B.J., Hochscheid, S., Kaska, Y., Lazar, B., Margaritoulis, D., Panagopoulou, A., Rees, A.F., Tomás, J., Türkozan, O., 2018. Mediterranean sea turtles: current knowledge and priorities for conservation and research. Endanger. Species Res. 36, 229–267.
28
Contents lists available at ScienceDirect
Fisheries Research journal homepage: www.elsevier.com/locate/fishres
Fishery strategy affects the loggerhead sea turtle mortality trend due to the longline bycatch
T
⁎
José Carlos Báeza,b, , Salvador García-Barcelonac, Juan Antonio Camiñasc, David Macíasc a
Centro Oceanográfico de Canarias, Instituto Español de Oceanografía, Spain Investigador Asociado Facultad de Ciencias, Universidad Autónoma de Chile, Chile c Centro Oceanográfico de Málaga, Instituto Español de Oceanografía, Spain b
A R T I C LE I N FO
A B S T R A C T
Handled by George A. Rose
The western Mediterranean Sea is an important fishing ground for the Spanish surface longline fleet targeting swordfish, bluefin tuna, and albacore. Spanish Mediterranean waters, including contiguous international waters, are important feeding areas for thousands of juvenile and sub-adult loggerhead turtles. Due to the spatial overlap in fishing grounds between different longline métiers and loggerhead distribution, in the early 2000s, an estimated minimum of 60,000 loggerhead sea turtles were caught as bycatch in Mediterranean longline fisheries, including all countries operating in the area. The Spanish surface longline fleet is continually introducing technological and strategic innovations to improve the economic benefits of the fishery. These innovations lead to high variability in fishing gear and operational strategies from year to year. During the study period, there was a change in the specific contribution of each métier to total effort. Thus, since 2000 to the present, the Spanish traditional home-base surface longline targeting swordfish has been gradually modified or in other cases replaced by other métiers, and in most vessels it has been replaced by a new deeper semipelagic longline targeting the same species; which has led to a dramatic decrease in sea turtle mortality. The main result of this study is that loggerhead turtle post-release mortality due to the bycatch by the Spanish surface fleets using different longline métiers has significantly decreased during the last 8 years of the study period. We estimate an average post-release mortality around 1800 loggerheads sea turtles per year. The observed decrease in turtle mortality was an indirect effect of the introduction of changes in technology and fishing strategies in the fleets in the attempt to improve their economic objectives.
Keywords: Longline By-catch Métier Mediterranean Sea
1. Introduction The loggerhead turtle (Caretta caretta) is the most common sea turtle species in the Mediterranean Sea, where it utilizes nesting beaches mainly located in the eastern basin (Margaritoulis et al., 2003; Casale and Margaritoulis, 2010; Casale et al., 2018). Annually, hundreds of juvenile loggerhead turtles, born on the beaches of the North Atlantic Sea (Camiñas and de la Serna, 1995; Encalada et al., 1998; MonzónArgüello et al., 2010; Carreras et al., 2011) and the Mediterranean Sea, are concentrated around the feeding grounds in the Western Mediterranean, mainly in waters around the Balearic Islands (Camiñas and de la Serna, 1995; Carreras et al., 2011; Báez et al., 2014a). It has been suggested that the surface longline fishery is the major source of mortality in the Mediterranean Sea (Camiñas, 2004; Báez et al., 2006; Casale, 2011; Álvarez de Quevedo et al., 2013). The western Mediterranean Sea is an important fishing ground for
⁎
the Spanish surface longline fishery, targeting swordfish, Xiphias gladius, bluefin tuna, Thunnus thynnus, and albacore, T. alalunga (Camiñas et al., 2006; Báez et al., 2007a, 2007b; 2010; García-Barcelona et al., 2010a, 2010b; Báez et al., 2011, 2013). Due to the spatial overlap between longline fishing grounds and loggerhead distribution, in the early 2000s, an estimated minimum of 60,000 loggerhead sea turtles were caught as bycatch in longline fisheries in the entire Mediterranean Sea (Lewison et al., 2004). The Spanish Mediterranean longline fleet targeting swordfish and tuna species in the Mediterranean Sea (Table 1) employs a variety of gear (i.e. métiers), and is characterized by its use of different hook types, type and size of bait, and so on (see Camiñas et al., 2006; Báez et al., 2007a, 2007b; 2010; García-Barcelona et al., 2010a, 2010b; Báez et al., 2011, 2013). The Spanish longline métiers described for the Mediterranean fleet (see Table 1), according to ICCAT (The International Commission for the Conservation of Atlantic Tunas) are as follows: LLALB (longline
Corresponding author at: Centro Oceanográfico de Canarias, Instituto Español de Oceanografía, Spain. E-mail address: [email protected] (J.C. Báez).
https://doi.org/10.1016/j.fishres.2018.11.032 Received 17 May 2018; Received in revised form 19 November 2018; Accepted 20 November 2018 0165-7836/ © 2018 Published by Elsevier B.V.
Fisheries Research 212 (2019) 21–28
J.C. Báez et al.
Table 1 Summary of the métiers observed in the surface longline vessels of the Spanish fleet based in the Western Mediterranean Sea. Metiér
Name
LLALB LLAM LLHB LLJAP LLSP LLPB
Longline Longline Longline Longline Longline Longline
Albacore American Home-Base Japanese Semi-Pelagic Piedra y Bola
LLHB
LLALB
LLJAP
LLAM
LLPB
LLSP
% Coverture
2000 2001 2002 2003 2004 2005 2006 2007* 2008* 2009* 2010 2011* 2012 2013 2014 2015 2016
AV AV AV AV AV AV AV AV AV AV AV AV AV AV AV AV AV
AV NAV NAV NAV AV NAV AV AV AV AV AV AV AV AV AV AV AV
AV AV AV AV AV AV AV AV AV AV AV AV NAV 0 0 NAV AV
0 0 0 0 NAV NAV AV AV AV AV NAV AV AV AV 0 NAV NAV
AV AV AV AV AV NAV AV AV AV AV AV AV AV AV NAV AV AV
0 0 0 0 0 0 0 AV AV AV AV AV AV AV AV AV AV
8.7 4.6 3.9 2.7 4.0 1.3 3.9 3.0 4.0 5.4 5.5 5.7 7.6 9.0 6.4 5.2 5.9
Fishing depth and description
Albacore or little tunny Swordfish Swordfish Bluefin Tuna Swordfish Swordfish
Surface drifting longline Surface drifting longline Surface drifting longline Surface drifting longline Semi-Pelagic drifting longline Bottom longline
longline fishery on loggerhead turtles mortality and, in particular, to determine trends in the bycatch mortality of this species in the Western Mediterranean Sea due to the use of these métiers.
Table 2 Summary available observed data per métier and year. We showed the total percentage of coverture with scientific observers. Key: 0, not applicable; AV, data from scientific observers available; NAV, data from scientific observers non available. Year
Target species
2. Material and methods 2.1. Fisheries and bycatch data In 1997, the Spanish Institute of Oceanography (IEO) implemented an on board observer program in the commercial longline fleet targeting highly migratory species, and a landing monitoring network to obtain direct information and data on effort and catches of target and bycatch species (e.g. retained and discarded species, number of individuals, size, and other biological data) in relation to the different métiers used in the Mediterranean Sea. The information obtained is used to fulfil the requirements of the different Regional Fisheries Management Organizations, such as ICCAT (International Commission for the Conservation of Atlantic Tuna). The present study used data from 2000 to 2016 collected by the observer program mentioned above (for more information on this Spanish observer program, see Camiñas et al., 2006; Báez et al., 2007a,b,c, 2010; García-Barcelona et al., 2010a,b). The observed coverture is variable in function to the economic funds per year and available métiers (Table 3). E-logbook is a mandatory electronic recording and reporting system about fisheries data, which is including in the EU system for fisheries controls (https://ec.europa.eu/fisheries/cfp/control/technologies/ers_ en). It is a system where the skippers keep a record of fishing operations. The coverage in e-logbook is of 100%. Data compiled in e-logbooks was used to estimate the total annual effort of the fleet (expressed as number of hooks). Métiers were assigned to trips using the catch composition recorded in e-logbooks, and information provided by onboard observers, informants from the landing monitoring network, and surveys of fishermen. Thus, we obtained the total effort of the fleet expressed as the number of hooks per métier and year.
* Indicates the years with scientific observers in all métiers.
albacore), a surface longline targeting albacore and small tuna (depending on the distance to the coast); LLAM (longline American), a surface longline combined with a hydraulically-operated monofilament longline reel targeting swordfish; LLHB (longline home-base), the traditional surface longline targeting swordfish; LLJAP (longline Japanese), a surface longline targeting bluefin tuna; LLPB (longline piedra y bola), a bottom longline targeting swordfish; and LLSP (longline semipelagic), a drifting semipelagic longline targeting Swordfish at depths of 200–700 m or more in the water column. Briefly, the main differences in longline métiers are related to hook type and hook size (although for LLHB, LLAM, LLPB and LLSP is the same hook type and size model), bait type and size, operational depth and the time the hook takes to sink (Table 2). For a detailed review, see García-Barcelona et al., 2010a, 2010b), and Báez et al. (2013). Bycatch rates could be affected by technical differences in fisheries operations and gear configurations (e.g. hook and bait type, and the use or otherwise of lights) and the fishing strategies used (e.g. period of the year, times of hauling and retrieval, distant to the base port, and fishing depths) by Spanish Mediterranean longliners (Camiñas et al., 2006; Báez et al., 2007a, 2007b; Báez et al., 2010). Thus, Báez et al. (2013) estimated that each métier type affected the loggerhead bycatch rate. Thus, métier types should be taken into account when estimating loggerhead bycatch (Báez et al., 2014b). Furthermore, the Spanish surface longline fleet is continually making technological and strategic innovations to improve the economic benefits of the fishery (Báez et al., 2013). The main aim of the present study was to estimate the mortality of loggerhead turtle due to the bycatch by the Spanish longline fleet during the period 2000–2016, while taking into account the historic development and changes of the métiers used during this period. The final goal was to understand the effect of changes in the Spanish
2.2. Statistical analysis In a first step, we estimated the annual average bycatch of loggerhead turtles using two different approaches: 1) by taking into account the average loggerhead bycatch and the average number of hooks for the entire period 2000–2016 per each métier separately; and 2) by estimating the average loggerhead turtle bycatch and the average number of hooks for each year and métier. The annual loggerhead turtle bycatch of a particular year and métier (ALBy), according to the first approach can be expressed as: ALBy = (R/h)*H Where R is the average loggerhead bycatch observed (i.e. average number of turtles caught) for the entire period 2000–2016 per each métier (i); h is the average of hooks observed for the entire period 2000–2016 per each métier (i), and H is the total annual effort of the fleet (expressed as number of hooks). The annual loggerhead turtle bycatch of a particular year and métier (ALBy), according to the second approach can be expressed as: 22
Fisheries Research 212 (2019) 21–28
J.C. Báez et al.
Table 3 Principal characteristics of the métiers observed in the surface longline fleet of the Spanish fleet based in the Western Mediterranean Sea. 1Indicates that they are the same hooks. Gear
LLHB
LLAM
LLSP
LLPB
LLJAP
LLALB
Hooks (N) Hooks form Weights in branchline or mainline Hook size (cm) Depth at sea (m) Baits
1500-4000 J1 No
≈ 1000 J1 Yes
≈ 2500 J1 Yes
600-1000 J1 Yes
250-1100 C No
2000 - 5000 J No
7.5 × 2.5 ≈ 40 - 70 mackerel, small mackerel, chub mackerel, atlantic saury, round sardinella, silver scabardfish or squid
7.5 × 2.5 ≈ 50 - 90 mackerel, chub mackerel, squid, round sardinella or artificial mackerel and squid
7.5 × 2.5 ≈ 200 - 700 mackerel, chub mackerel, squid, round sardinella or plastic mackerel and squid
7.5 × 2.5 ≈ 250 - 350 mackerel, chub mackerel or silver scabardfish
7.5 × 3.0 ≈ 50 - 90 great mackerel, great squid or bogue
4.3 × 1.7 ≈ 20 - 50 sardine and round sardinella
Fig. 1. Distribution of the Spanish longline fishing effort observed over the entire period 2000–2016.
affect its abundance and distribution. For this reason, we decided to also use the second approach. Thus, to fill in years with no data, we extrapolate the mean for years of the immediately anterior and posterior. However, when the gap was very large, a number of years similar to the size of the gap were used. In a second step, we estimated direct mortality and post-release mortality. The direct mortality was estimated from the data provided from the observer program of the IEO. In the periods 1999–2004 (reported in Camiñas et al., 2006) and 2009–2016 the observers recorded, when possible, the situation (alive or dead) of the turtle hooked in the longline. We used the ratio number of dead turtles divided per total number of observed bycatch turtles per métier for both periods together. The observed ratios per métiers are: LLHB = 10/1849, LLAM = 15/370, LLSP = 2/4, LLPB = 0/1, LLJAP = 14/807, LLALB = 16/1027. We used the post-release mortality probability during the 90 days following release (ranged from 0.308 to 0.365) estimated by Álvarez de Quevedo et al. (2013), to estimate mortality per year (TMy) according to the expressions:
ALBy = (Fy/hy)*H Where Fy is the average loggerhead bycatch observed (i.e. average number of turtles caught) for a particular year per each métier (i); h is the average of hooks observed for a particular year per each métier (i), and H is the total annual effort of the fleet (expressed as number of hooks). Subsequently, the estimated total number of turtle bycatch per year (By) is the sum of the estimated bycatch of each métier calculated in these two ways (ALBy): n
By =
∑ ALByi i
Moreover, we calculated the 95% confidence interval (C.I.) from the standard error of the mean observed for each métier and period (i.e. the total or per year) (Sokal and Rohlf, 1995). The first approach has the advantage of eliminating possible bias due to poor coverage in some métiers during some of the study years. However, a drawback of this method is that it assumes a constant abundance of sea turtle in the area. However, in line with Camiñas and de la Serna (1995) and Báez et al. (2014a), there may be annual variations in the total number of loggerhead turtles caught as bycatch due to migration to the study areas and to global climatic conditions that
TMy minimum = 0.308*By ± 95% C.I.; TMy maximum = 0.365* By ± 95% C.I.
23
Fisheries Research 212 (2019) 21–28
J.C. Báez et al.
Fig. 2. Trends in Spanish longline fishing effort per métier over the study period.
year (March, October, and November). During the study period, there was a change in the specific contribution of each métier to total effort (Fig. 2). Thus, from 2000 to 2005, the fishing effort was dominated by LLHB, but since 2005 other métiers have gained ground, such as LLAM. Since 2007, and mainly in the summer months, the métier LLHB has decreased in importance due to the introduction of LLSP. There was also a change in effort of LLALB due to fishing market conditions. We estimated an average of 5317 loggerhead sea turtle bycatch per year (i.e. mean ALBy) based to the approach 1 (maximum mean of 6457 individuals and a minimum mean of 4220 individuals). However, we estimated an average of 5565 loggerhead sea turtle bycatch per year (i.e. mean ALBy) based on approach 2 (i.e. a maximum mean of 8198 individuals and a minimum mean of 3063 individuals). In contrast to the study by Báez et al. (2013), over the entire study period, the main estimated bycatch was by LLHB métiers. We estimated an average of nearly 3000 loggerhead sea turtles per year by the LLHB métier versus 833 loggerhead sea turtles per year by the LLALB over the entire study period. The differences between the two approaches could be due to the standard error and gaps in the annual sampling effort of métiers (Tables 4 and 5). Both approaches showed a significant correlation (r = 0.87, P < 0.001). In a second step, we estimate direct and post-release mortality per year (TMy) according to the expressions explicated above. We observed a low direct mortality for all métiers pooled together per year. Thus according to the approach 1 the mean of the averages of the sea turtles directly dead in the longline was 72 sea turtles, while according to the approach 2 were 82 sea turtles directly dead. We estimate a total mortality average (i.e. direct and post-release mortality) of 1861 loggerhead sea turtle per year based to the approach 1 (maximum mean of 2482 individuals and a minimum mean of 1347 individuals), and average of 1955 loggerhead sea turtle per year based to the approach 2 (maximum mean of 3126 individuals and a minimum mean of 978 individuals). Both approaches showed that there was a significant downward trend (Figs. 3 and 4) in annual turtle mortality, with a significant negative time relation (for the approach 1: R2 = 0.896, P < 0.0001; for the approach 2: R2 = 0.724, P < 0.0001). According to the results from GLMs (Table 6) LLSP is the variable that more reduced the mortality.
Table 4 The global average loggerhead bycatch and mean of the number of hooks for the entire period 2000–2016 per each métier. Métier
N
Turtle mean
Standard error
Hooks mean
LLALB LLHB LLJAP LLSP LLPB LLAM
1236 1803 486 1279 382 121
0.8220 1.3494 1.6564 0.0063 0.0105 0.6860
3.00806 3.99735 4.09012 0.78870 0.12505 2.11750
2746.34 2359.99 1265.23 1988.67 1196.85 1186.24
Key: N, number of sets observed; Turtle mean, mean of the loggerhead sea turtle bycatch observed per set; Standard error, the standard error for the turtle mean; Hooks mean, mean observed hooks per set.
Thereby, we applied a fixed post-release mortality rate. In this case, we assumed that the mortality rate per métier is constant and equal in all métiers. However, this could be only assumed for LLHB, LLAM, LLSP and LLPB, that used the same hook size and type, while LLALB and LLJAP used different hooks. Finally, we summed the direct and postreleased mortality. We use General Linear Models (GLMs) to evaluate the effect of métiers in the sea turtle mortality. For this, we performed GLMs for each dependent variable (approach 1, and approach 2) versus the interaction to the independent variables: LLSP, LLAM, LLHB, LLPB, LLALB, LLJAP, and year. We assessed the parsimony of the GLMs using the Akaike information criterion (AIC) (Akaike, 1973). 3. Results During the study period, the Mediterranean Spanish surface longline fleet decreased from approximately 90 authorized vessels in 2000 to 73 vessels in 2016. The length of the vessels ranged from 12 to 27 m LOA (Overall Length). Until the mid-2000s, the artisanal fleet could also fish for large pelagic fishes, and the number of longliner vessels operating in the area could increase to just over 100. The fishing trips were often of short duration (i.e. 1 day to 8 days, depending on métiers and LOA). Fig. 1 shows the observed effort of the fleet. This fleet fished on a yearround basis, targeting different species until the implementation of temporary closure for swordfish in 2008 (ICCAT Recommendation 0701). Between 2008 and 2016, the fleet stopped fishing for 3 months per 24
25
0 0 71 8 0 4 0 0 0 0 0 0 71
0.6862 0.6862 1.043 0.875 0.6862 0.5 0.6862 0.6862 0.6862 0.6862 0.6862 0.6862 1.043
Turtle mean
2.1182 2.1182 2.637 1.81 2.1182 0.577 2.1182 2.1182 2.1182 2.1182 2.1182 2.1182 2.637
S.E.
1186.242 1186.242 1195.73 870 1186.242 1100 1186.242 1186.242 1186.242 1186.242 1186.242 1186.242 1196
Hooks
N 93 34 29 46 40 56 20 56 20 7 74 3 0 0 0 26 8
Turtle mean 3.699 8.35 1.1034 1.457 0.825 0.125 0.15 0.3036 0.55 0 0.0946 0 0.163 0.163 0.163 0.16 0
LLJAP S.E. 5.307 9.085 1.74 1.39 1.5 0.384 0.366 0.537 0.759 0 0.0946 0 0.213 0.213 0.213 0.21 0
Hooks 1584 1738 2066 1697 1376 959.5 910 998 1222 959 629 167 7443 7443 7443 744 0
N 337 220 119 122 213 41 66 85 116 95 99 12 122 53 47 14 42
LLHB Turtle mean 3.45 1.577 0.689 2.48 2.038 0.927 0.61 0.3411 0.18 0.421 0.303 0 0.0082 0.0566 0 0 0
S.E. 6.3014 3.3061 1.582 6.95 3.9774 2.75 0.298 0.795 1.169 0.41 0.224 0 0.091 0.305 0 0 0
Hooks 3069 2963 3567 2188 1327 1438 2066 2597 2044 2474 2536 2000 1539 1919 1608 1986 1097
N 13 1 19 8 15 36 21 84 43 50 45 11 18 44 0 10 0
LLPB Turtle mean 0 0 0 0 0 0.0833 0.1429 0 0 0 0 0 0 0.0227 0.0114 0 05
S.E. 0 0 0 0 0 0.368 0.478 0 0 0 0 0 0 0.151 0.0764 0 05
Hooks 1477 2000 2098 1704 1957 1721 1553 939 796 1100 1234 1739 958 1065 10124 1373 13735
LLSP
5 119 178 90 215 125 225 125 62 135
N
Key: N, number of sets observed; Turtle mean, average loggerhead sea turtle bycatch observed; S.E., the standard error for the turtle mean; Hooks mean, mean observed hooks per set. 1 Estimated figures using data from 2000, 2004, 2006, and 2007. 2 Estimated figures using data from 2006, 2007, 2009, and 2016. 3 Estimated figures using data from 2008, 2009, 2010, and 2011. 4 Estimated figures using data from 2012 and 2013. 5 Estimated figures using data from 2015.
Hooks 2664 28831 28831 28831 2175 28831 3558 2422 2600 3022 3010 2732 2571 2935 2834 2721 2466
N
S.E. 4.43 4.561 4.561 4.561 4.56 4.561 5.65 2.95 0 2.73 8.16 0.59 1.86 1.54 0.175 0.148 0.306
N 7 0 0 0 40 0 69 36 26 49 73 124 206 170 159 179 98
2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016
Turtle mean 7.7143 2.2431 2.2431 2.2431 0 2.2431 3.49 1.278 0 1.327 4.534 0.12 0.888 0.4059 0.0314 0.0223 0.306
LLAM
LLALB
Year
Table 5 Estimations of average loggerhead turtle bycatch and average number of hooks per year and métier.
0 0.0336 0 0 0.0047 0 0.0133 0 0 0
Turtle mean
0 0.18 0 0 0.07 0 0.12 0 0 0
S.E.
2020 1323 1706 2003 2214 1902 1820 2142 2542 2542
Hooks
J.C. Báez et al.
Fisheries Research 212 (2019) 21–28
Fisheries Research 212 (2019) 21–28
J.C. Báez et al.
Fig. 3. Annual loggerhead sea turtle mortality per year (all métiers pooled together) based on the global average loggerhead bycatch for the entire period 2000–2016 per métier.
Fig. 4. Annual loggerhead sea turtle mortality per year (all métiers pooled together) based on the average loggerhead bycatch per métier and year. Table 6 Results from the General Linear Models for the mortality of sea turtle, according to the approaches 1(annual loggerhead sea turtle mortality per year -all métiers pooled together- based on the average loggerhead bycatch per métier) and 2 (annual loggerhead sea turtle mortality per year -all métiers pooled together- based on the average loggerhead bycatch per métier and year). Approach
Interaction
AIC
Omnibus test signification
Approach 1
LLJAP*LLALB*LLPB*LLHB LLJAP*LLALB*LLPB*LLHB*LLAM LLJAP*LLALB*LLPB*LLHB*LLAM*LLSP LLJAP*LLALB*LLPB*LLHB*LLAM*LLSP*year LLJAP*LLALB*LLPB*LLHB LLJAP*LLALB*LLPB*LLHB*LLAM LLJAP*LLALB*LLPB*LLHB*LLAM*LLSP LLJAP*LLALB*LLPB*LLHB*LLAM*LLSP*year
141.826 142.046 151.946 103.812 159.34 159.494 165.810 126.317
< 0.0001 < 0.0001 0.096 < 0.0001 0.009 0.009 0.502 < 0.0001
Approach 2
26
Fisheries Research 212 (2019) 21–28
J.C. Báez et al.
4. Discussion
A comparable situation appeared in Italy, when the surface longline fleets also changed the métiers targeting swordfish. In 2010, the traditional surface longline was substituted by a new mesopelagic longline in the southern Italy swordfish fishery (i.e. in the Ligurian Sea and Ionian Calabria). The impact of this new gear on protected or endangered species, such as sea turtles, was absolutely negligible (Cambiè et al., 2013; Garibaldi, 2015). In addition, the size of the turtles caught varies according to the métier used. According to Báez et al. (2013), turtles caught on longline gear targeting albacore and small tunas are smaller than turtles caught using longline gear targeting bluefin tuna and swordfish. Several studies have analysed best practices to reduce loggerhead bycatch from longline fisheries (Gilman et al., 2006; Báez et al., 2007b). However, as shown by results from the western and central Mediterranean Sea (i.e. near Spain and Italy), by only modifying the depth of fishing (i.e. leaving the longline at a depth inaccessible to sea turtles), the bycatch of loggerhead turtles can be reduced by up to 99.5% compared to the percentages caught on other métiers such as LLHB. The introduction in Spanish and Italian surface longline vessels of new gear and fishing strategies targeting swordfish has decreased both captures and the fishing mortality of loggerhead turtles and other species. However, these new métiers could target large individual swordfish, which could have negative consequences for Mediterranean swordfish stocks if there is a reduction in the number of reproductive individuals such that the stocks cannot be sustained (for example, Cambiè et al., 2013; Garibaldi, 2015). Moreover, the new métiers could bycatch other species with slow growth and retarded maturity, such as Zu cristatus (García-Barcelona et al., 2016). This aspect could be the topic of further research.
Surface longline fishing involves the use of a suite of gear targeting different species. The efficiency of the gear varies according to the target species. However, bycatch rates also vary depending on a range of technological and strategic approaches. Changes in the métiers are driven by established Spanish and EU management measures and the economic revenues of the fleets. During the study period, the traditional home-base surface longline targeting swordfish métier (LLHB) used by the Spanish Mediterranean fleet was partially replaced, initially by the American longline (LLAM), and subsequently by the semipelagic longline métier (LLSP) targeting the same species. Thus, the incorporation of the LLAM could explain the upward trend between 2003 and 2005, whereas the incorporation of the LLSP in 2007 could explain the downward trend observed since this year. This last trend was increased by the fact that the LLSP replace the LLHB mainly in summer season, when the impact of LLHB on sea turtles is higher in the area (Báez et al., 2007a, 2007b). The mean of the averages the loggerhead sea turtles bycatches in the period 2000–2003 was estimated to be about 8800 (according to the approach 1), and 11,800 (according to the approach 2). These estimations are similar to the reported by Álvarez de Quevedo et al., (2013) but discussed by Báez et al., (2014a, 2014b). The scientific observer program it's very expensive, it is no possible to on-boarding the scientific observers in all métiers every year. Thus, the years with real data for all métiers are only 4 (Table 3). For this reason, we have filled the gaps with no data. We considered that this could be a weakness of the analysis. Moreover, both approaches showed a high oscillation in their estimations, which were highest to end of the time series, thus in the period 2015-2016. According to the approach 1, the mortality rate was estimated to be, on average, 1000 loggerhead sea turtles but, according the approach 2, it was, on average, 50 in the same period. Consequently, these estimations should be used with caution. However, despite the differences of the two approaches, they show an important decreasing in the mortality trend due to longline bycatch. Thus, the veterinarians from the marine recovery centers observed a decrease in the causes of strandings loggerhead death due to the longline fisheries (Jiménez et al., 2017), confirming our results. This study presents an updated estimation of loggerhead sea turtle mortality due to the bycatch by métier in the Spanish Mediterranean longline fleet. Each bycatch event is customarily considered as affecting a different individual; even when there is evidence of released turtles being caught again on other nearby longlines (e.g. see Tomas et al., 2001). For this reason, the bycatch and mortality estimates presented in this study represent hypothetical maximum values. There are different direct mortality rate in function to métier type. Thus, we observed that direct mortality in LLSP is about 50%, while LLPB, LLHB and LLAM showed the percentage lowest. Nevertheless, the direct mortality per year is very low. During the last 8 years, there has been a significant decrease in the bycatch of loggerhead turtles by the Spanish surface fleets using different métiers. There is a strong correlation between the use of the new métiers and the decreasing numbers of loggerhead sea turtle as bycatch, with the potential positive effect of increasing the number of loggerheads of reproductive age in the Mediterranean and Atlantic populations present in the Spanish fishing grounds. However, the decrease in bycatch is not due to the implementation of new management actions to reduce the bycatch of sea turtles or other protected species; rather, it is due to the collateral effect of the introduction of technical changes in fishing gear and to changes in fishing strategies based on the economic objectives of each fleet. If the reduction in turtle bycatch is due to changes in the main gear used and the related fishing strategy (mainly due to deeper sets, and a significant reduction in the time the hook takes to sink), then forthcoming technological changes or the implementation of other fishing strategies by the fleet could reverse the current situation.
Acknowledgements This article is offered In Memoriam of the recently deceased Dr. Giulia Cambié, an Italian colleague who studied the Mediterranean fisheries and marine turtle bycatch. For some time she worked in Spain and in collaboration with our team. The onboard observer program in commercial longline vessels was supported by different projects from the IEO based in Malaga, GPM-4 programs (IEO). This project has been co-funded by the EU through the European Maritime and Fisheries Fund (EMFF) within the National Program of collection, management and use of data in the fisheries sector and support for scientific advice regarding the Common Fisheries Policy. We thank the IEO scientists and the captains and crews of the different research and leisure vessels who were involved in the onboard observation program of the IEO. We are grateful to three anonymous reviewers, for insightful comments that improved the manuscript. References Akaike, H., 1973. Information theory and an extension of the maximum likelihood principle. Petrov, B.N., Csaki, F. (Eds.), Proceedings of the Second International Symposium on Information Theory 267–281. Álvarez de Quevedo, I., San Félix, M., Cardona, L., 2013. Mortality rates in bycaught loggerhead turtle Caretta caretta in the Mediterranean Sea and implications for the Atlantic populations. Mar. Ecol. Prog. Ser. 489, 225–234. Báez, J.C., Camiñas, J.A., Rueda, L., 2006. Accidental fishing capture of marine turtles in South Spain. Mar. Turtle Newsl. 111, 11–12. Báez, J.C., Real, R., Camiñas, J.A., 2007a. Differential distribution within longline transects of loggerhead and swordfish captured by the Spanish Mediterranean surface longline fishery. J. Mar. Biol. Assoc. U.K. 87, 801–803. Báez, J.C., Real, R., García Soto, C., de la Serna, J.M., Macías, D., Camiñas, J.A., 2007b. Loggerhead turtle bycatch depends on distance to the coast, independent of fishing effort: implications for conservations and fisheries management. Mar. Ecol. Prog. Ser. 338, 249–256. Báez, J.C., Real, R., Macías, D., de la Serna, J.M., Bellido, J.J., Camiñas, J.A., 2010. Swordfish Xiphias gladius Linnaeus1758 and loggerhead Caretta caretta (Linnaeus 1758) captures associated with different combinations of bait in the Western Mediterranean surface longline fishery. J. Appl. Ichthyol. 26, 126–127. Báez, J.C., Real, R., Bellido, J.J., Macias, D., de la Serna, J.M., Camiñas, J.A., 2011. Validating an ecological model with fisheries management applications: the relationship between loggerhead bycatch and distance to the coast. J. Mar. Biol. Assoc.
27
Fisheries Research 212 (2019) 21–28
J.C. Báez et al.
Encalada, S.E., Bjorndal, K.A., Bolten, A.B., Zurita, J.C., Schroeder, B., Possardt, E., Sears, C.J., Bowen, B.W., 1998. Population structure of loggerhead turtle (Caretta caretta) nesting colonies in the Atlantic and Mediterranean as inferred from mitochondrial DNA control region sequences. Mar. Biol. 130, 567–575. García-Barcelona, S., Ortiz de Urbina, J.M., de la Serna, J.M., Alot, E., Macías, D., 2010a. Seabird by-catch in Spanish Mediterranean large pelagic logline fisheries, 1998–2008. Aquat. Living Resour. 23, 363–371. García-Barcelona, S., Macías, D., Ortiz de Urbina, J.M., Alba, E., Real, R., Báez, J.C., 2010b. Modelling abundance and distribution of seabird by-catch in the Spanish Mediterranean longline fishery. Ardeola 57, 65–78. García–Barcelona, S., García–Cancela, R., Cayuela Fernández–Peralta, L., de Carlos, M.J., Bañón, R., Macías, D., Báez, J.C., 2016. Descripciín de dos ejemplares de Zu cristatus (Bonelli, 1820) capturados accidentalmente con un palangre semipelágico en el Mediterráneo occidental. Arx. Misc. Zool. 14, 91–98. Garibaldi, F., 2015. By-catch in the mesopelagic swordfish longline fishery in the Ligurian Sea (Western Mediterranean). Collect. Vol. Sci. Pap. ICCAT 71 (3), 1495–1498. Gilman, E., Zollet, E., Beverly, S., Nakano, H., Davis, K., Shiode, D., Dalzell, P., Kinan, I., 2006. Reducing sea turtle bycatch in pelagic longline fisheries. Fish Fish. 7, 2–23. Jiménez, J., Gómez, J.A., Eymar, J., Gago, C., 2017. Cambios en las causas de mortalidad de las tortugas marinas. Quercus 381, 28–35. Lewison, R.L., Freeman, S.A., Crowder, L.B., 2004. Quantifying the effects of fisheries on threatened species: the impact of pelagic longlines on loggerhead and leatherback sea turtles. Ecol. Lett. 7, 221–231. Margaritoulis, D., Argano, R., Baran, I., Bentivegna, F., Bradai, M.N., Camiñas, J.A., Casale, P., De Metrio, G., Demetropoulos, A., Gerosa, G., Godley, B.J., Haddoud, D.A., Houghton, J., Laurent, L., Bojan, L., 2003. Loggerhead turtles in the Mediterranean: present knowledge and conservation perspectives. In: Bolten, A.B., Witherington, B.E. (Eds.), Loggerhead Sea Turtles. Smithsonian Institution Press, Washington, DC, USA, pp. 175–198. Monzón-Argüello, C., Rico, C., Naro-Maciel, E., Varo-Cruz, P., López, A.M., López-Jurado, L.F., 2010. Population structure and conservation implications for the loggerhead sea turtle of the Cape Verde Islands. Conserv. Genet. 11 (5), 1871–1884. Sokal, R.R., Rohlf, F.J., 1995. Biometry, 3rd edition. W.H. Freeman and Co, New York. Tomas, J., Dominici, A., Nannarelli, S., Forni, L., Badillo, F.J., Raga, J.A., 2001. From hook to hook: the odyssey of a loggerhead sea turtle in the Mediterranean. Mar. Turtle Newsl. 92, 13–14.
U.K. 91, 1381–1383. Báez, J.C., Macías, D., Camiñas, J.A., Ortiz De Urbina, J.M., García-Barcelona, S., Bellido, J.J., Real, R., 2013. Bycatch frequency and size differentiation in loggerhead turtles as a function of surface longline gear type in the western Mediterranean Sea. J. Mar. Biol. Assoc. U.K. 93, 1423–1427. Báez, J.C., Macías, D., García-Barcelona, S., Real, R., 2014a. Interannual differences for sea turtles by-catch in Spanish longliners from Western Mediterranean Sea. Sci. World J. https://doi.org/10.1155/2014/861396. Báez, J.C., García-Barcelona, S., Real, R., Macías, D., 2014b. Estimating by-catch of loggerhead turtles in the Mediterranean: Comment on Álvarez de Quevedo et al. Mar. Ecol. Prog. Ser. 504, 301–302. Cambiè, G., Muiño, R., Mingozzid, T., Freire, J., 2013. From surface to mid-water: is the swordfish longline fishery “hitting rock bottom”? A case study in southern Italy. Fish. Res. 140, 114–122. Camiñas, J.A., 2004. Sea turtles of the Mediterranean Sea: Population Dynamics, Sources of Mortality and Relative Importance of Fisheries Impacts. FAO Fisheries Report 738. pp. 27–84. Camiñas, J.A., de la Serna, J.M., 1995. The loggerhead distribution in the western Mediterranean Sea as deduced from captures by the Spanish longline fishery. In: Llorente, G.A., Montori, A., Santos, X., Carretero, M.A. (Eds.), Scientia Herpetologica. Asociación Herpetológica Española, Barcelona, pp. 316–323. Camiñas, J.A., Báez, J.C., Valeiras, X., Real, R., 2006. Differential loggerhead bycatch and direct mortality in surface longline according to boat strata and gear type. Sci. Mar. 70, 661–665. Carreras, C., Pascual, M., Cardona, L., Marco, A., Bellido, J.J., Castillo, J.J., Tomás, J., Raga, J.A., Sanfélix, M., Fernández, G., Aguilar, A., 2011. Living together but remaining apart: Atlantic and Mediterranean loggerhead sea turtles (Caretta caretta) in shared feeding grounds. J. Hered. 102, 666–677. Casale, P., 2011. Sea turtle bycatch in the Mediterranean. Fish Fish. 12 (3), 299–316. Casale, P., Margaritoulis, D., 2010. Sea Turtles in the Mediterranean: Distribution, Threats and Conservation Priorities. Gland, Switzerland IUCN 294 pp. Casale, P., Broderick, A.C., Camiñas, J.A., Cardona, L., Carreras, C., Demetropoulos, A., Fuller, W.J., Godley, B.J., Hochscheid, S., Kaska, Y., Lazar, B., Margaritoulis, D., Panagopoulou, A., Rees, A.F., Tomás, J., Türkozan, O., 2018. Mediterranean sea turtles: current knowledge and priorities for conservation and research. Endanger. Species Res. 36, 229–267.
28