INTRODUCTIONTop

Bottom trawl fisheries, which are generally multispecies in the Mediterranean Sea, have rather poor selectivity (Özbilgin et al. 2006Özbilgin Y.D., Tosunoğlu Z., Özbilgin H. 2006. By-catch in a 40 mm PE demersal trawl codend. Turk. J. Vet. Anim. Sci. 30: 179-185., Sardà et al. 2006Sardà F., Bahamon N., Molí B., et al. 2006. The use of a square mesh codend and sorting grids to reduce catches of young fish and improve sustainability in a multispecies bottom trawl fishery in the Mediterranean. Sci. Mar. 70: 347-353.). Modifying a fishing gear to reduce the capture of juvenile fish, allowing undersized fish to escape, is one of the main management tools for sustainable fisheries (Suuronen 2005Suuronen P. 2005. Mortality of fish escaping trawl gears. FAO Fish. Tech. Pap. 478: 72 pp., Breen et al. 2007Breen M., Huse I., Ingólfsson O.A., et al. 2007. An assessment of mortality in fish escaping from trawl codends and its use in fisheries management. Quality of Life and Management of Living Resources Q5RS-2002-01603, 300 pp., Sacchi 2008Sacchi J. 2008. The use of trawling nets in the Mediterranean. Problems and selectivity options. Options Mediterranean’s, Series B, No: 62: 87-96.). However, increasing trawl selectivity may only be justified if a significant proportion of the escaping fish survive (Suuronen 2005Suuronen P. 2005. Mortality of fish escaping trawl gears. FAO Fish. Tech. Pap. 478: 72 pp., Gilman et al. 2013Gilman E., Suuronen P., Hall M., et al. 2013. Causes and methods to estimate cryptic sources of fishing mortality. J. Fish. Biol. 83: 766-803.). Escape mortality has been described by ICES (2005)ICES. 2005. Joint report of the Study Group on Unaccounted Fishing Mortality (SGUFM) and the Workshop on Unaccounted Fishing Mortality (WKUFM). ICES CM 2005/B: 08. as “fish that die after actively escaping from a gear prior to the catch being landed by the fishing operation” (Suuronen 2005Suuronen P. 2005. Mortality of fish escaping trawl gears. FAO Fish. Tech. Pap. 478: 72 pp., Broadhurst et al. 2006Broadhurst M.K., Suuronen P., Hulme A. 2006. Estimating collateral mortality from towed fishing gear. Fish Fish. 7: 180-218.). Information on survival rates is available for approximately 40 fish species from many locations during the past half-century: off the coasts of Scotland (Sangster et al. 1996Sangster G.I., Lehmann K., Breen M. 1996. Commercial fishing experiments to assess the survival of haddock and whiting after escape from four sizes of diamond mesh codends. Fish. Res. 25: 323-345., Main and Sangster 1988Main J. Sangster G.I. 1988. A report on an investigation to assess the scale damage and survival of young fish escaping from a demersal trawl. Scottish Fish. Res. Rep. No. 3/88.), Norway (Soldal and Engås 1997Soldal A.V., Engås A. 1997. Survival of young gadoids excluded from a shrimp trawl by a rigid deflecting grid. ICES J. Mar. Sci. 54: 117-124.), the USA (DeAlteris and Reifsteck 1993DeAlteris J.T., Reifsteck D.M. 1993. Escapement and survival of fish from the codend of a demersal trawl. ICES Mar. Sci. Symp. 196: 128-131.) and Australia (Broadhurst et al. 1997Broadhurst M.K., Kennelly S.J., Barker D.T. 1997. Simulated escape of juvenile Sand Whiting (Sillago ciliate, Cuvier) through square-meshes: effects on scale-loss and survival. Fish. Res. 32: 51-60.), and in the Baltic Sea (Suuronen et al. 1996aSuuronen P., Erickson D.L., Orrensalo A. 1996a. Mortality of herring escaping from pelagic trawl codends. Fish. Res. 25: 305-321., bSuuronen P., Lehtonen E., Tschernij V., et al. 1996b. Skin injury and mortality of Baltic cod escaping from two codends equipped with exit windows. Arch. Fish. Mar. Res. 44: 165-178.), and the Barents Sea (Ingólfsson et al. 2007Ingólfsson O.A., Soldal A.V., Huse I., et al. 2007. Escape mortality of cod, saithe, and haddock in a Barents Sea Trawl Fishery. ICES J. Mar. Sci. 64: 1836-1844.).

Turkish bottom trawlers in the Aegean Sea (coastal waters of Turkey) typically catch over 50 fish species and are responsible for a considerable amount of by-catch and discards (Özbilgin et al. 2006Özbilgin Y.D., Tosunoğlu Z., Özbilgin H. 2006. By-catch in a 40 mm PE demersal trawl codend. Turk. J. Vet. Anim. Sci. 30: 179-185.). A number of scientific studies have been carried out to improve trawl codend selectivity in the Aegean Sea (Petrakis and Stergiou 1997Petrakis G., Stergiou K.I. 1997. Size selectivity of diamond and square mesh cod- ends for four commercial Mediterranean fish species. ICES J. Mar. Sci. 54: 13-23., Metin et al. 2005Metin C., Özbilgin H., Tosunoğlu Z., et al. 2005. Effect of square mesh escape window on codend selectivity for three fish species in the Aegean Sea. Turk. J. Vet. Anim. Sci. 29: 461-468.). However, few studies have investigated the escape mortality of fish escaping from the trawl codend in the Mediterranean Sea (Metin et al. 2004Metin C., Tokaç A., Ulaş A., et al. 2004. Survival of red mullet (Mullus barbatus L., 1758) after escape from a trawl codend in the Aegean Sea. Fish. Res. 70: 49-53., Düzbastılar et al. 2010aDüzbastılar F.O., Özgül A., Aydın İ., et al. 2010a. A preliminary study on the survival of brown comber, Serranus hepatus (Actinopterygii, Perciformes, Serranidae), escaping from the codend of a bottom trawl. Acta Ichthyol. Piscat. 40: 27-36., bDüzbastılar F.O., Özbilgin H., Aydın C., et al. 2010b. Mortalities of fish escaping from square and diamond mesh codends in the Aegean Sea. Fish. Res. 106: 386-392., cDüzbastılar F.O., Aydın C., Metin G., et al. 2010c. Survival of fish after escape from a 40 mm streched diamond mesh trawl codend in the Aegean Sea. Sci. Mar. 74: 755-761.).

This study reports on escape mortality data obtained in 2011 and 2012 in the summer and winter seasons for red mullet (Mullus barbatus Linnaeus, 1758) escaping from 40-mm square-mesh and 44- and 50-mm diamond-mesh codends mounted in a conventional trawl net off the Turkish coast of the Aegean Sea. The effect of seasonal variation on the codend escapee survival for this species is presented for the first time.

MATERIALS AND METHODSTop

The experiments were conducted in the İzmir Bay, between latitude 38°23′-38°24′N and longitude 26°47′-26°48′E (Fig. 1), at depths ranging from 10 to 30 m. To investigate seasonal effects (winter vs. summer), experimental trials were performed in January and September 2011, and in February and September 2012. Bottom temperature around the cages was recorded by a dive computer (Suunto D6). In total, 48 hauls with 15-min sampling time were conducted (Table 1). The fishing gear was a conventional bottom trawl with 900 meshes around the fishing circle (Düzbastılar et al. 2012Düzbastılar F.O., Lök A., Aydın C., et al. 2012. Investigating the survival of fish escaping from the codends of bottom trawls (in Turkish), TÜBİTAK Project No: 110O335, Final Rep. 174 pp).

Three different codends, all made of the same twisted polyethylene (PE) material (380d/21, 3×7), were tested: 40 mm square-mesh (40S) and 44- and 50-mm diamond-mesh (44D and 50D). The use of a 40-mm square-mesh codend was adopted in September 2008 as an alternative for the 44-mm diamond-mesh codend in Turkish waters of the Mediterranean Sea (Anonymous 2008Anonymous. 2008. The commercial fish catching regulations in seas and inland waters in 2008-2012 fishing period: circular No. 2⁄1 (2008/48) (in Turkish). Republic of Turkey, Minister of Agriculture and Rural Affair, General Directorate of Conservation and Inspection, Ankara.). European Commission Regulation 1967/2006 enforces minimum mesh sizes of 40-mm square mesh or 50-mm diamond mesh for trawl codends in EU Mediterranean waters (EC 2006EC. 2006. Council Regulation (EC 1967/2006) concerning management measures for the sustainable exploitation of fishery resources in the Mediterranean Sea, amending Regulation (EEC) No 2847/93 and repealing Regulation (EC) No 1626/94. Off. J.E.U. 409, 75 pp.).

To determine the mesh sizes, 60 stretched mesh openings (3 lines of 20 consecutive meshes in the towing direction) near the aft part of each codend were measured using a digital calliper with a 39.2266 N (4 kg) weight tied vertically to the stationary jaw. Mean values were 40.28±0.10; 44.04±0.07 and 51.34±0.19 for 40S, 44D and 50D, respectively. In order to fish homogeneously, codends were randomly changed at the end of each haul.

Research vessel, R/V EGESÜF (26.8 m length, ~405 kW engine) was used for trawling. A constant towing duration of 15 min with a mean towing speed of 2.7 knots (as determined from GPS) was applied for all hauls to minimize any potential sampling time effects on mortality (Breen 2004Breen M. 2004. Investigating of the mortality of fish escaping from towed fishing gears- a critical analysis. PhD thesis, Univ. Aberdeen, Scotland, 321 pp.). Commercial tows in the study area typically vary between 1 and 6 hours. The experimental trawl hauls started at depths of approximately 30 m and finished at approximately 10 m, to enable divers to recover the samples at the end of the tow. In the Aegean Sea, commercial trawlers must fish 1.5 miles from the shore, according to the Turkish commercial fishing regulations (Anonymous 2008Anonymous. 2008. The commercial fish catching regulations in seas and inland waters in 2008-2012 fishing period: circular No. 2⁄1 (2008/48) (in Turkish). Republic of Turkey, Minister of Agriculture and Rural Affair, General Directorate of Conservation and Inspection, Ankara.). Thus, trawlers generally work at depths ranging from 50 to 150 m.

The experimental protocol for sampling and monitoring fish after they escape from the codends was similar to that used by Metin et al. (2004)Metin C., Tokaç A., Ulaş A., et al. 2004. Survival of red mullet (Mullus barbatus L., 1758) after escape from a trawl codend in the Aegean Sea. Fish. Res. 70: 49-53. and Düzbastılar et al. (2010aDüzbastılar F.O., Özgül A., Aydın İ., et al. 2010a. A preliminary study on the survival of brown comber, Serranus hepatus (Actinopterygii, Perciformes, Serranidae), escaping from the codend of a bottom trawl. Acta Ichthyol. Piscat. 40: 27-36., bDüzbastılar F.O., Özbilgin H., Aydın C., et al. 2010b. Mortalities of fish escaping from square and diamond mesh codends in the Aegean Sea. Fish. Res. 106: 386-392., c)Düzbastılar F.O., Aydın C., Metin G., et al. 2010c. Survival of fish after escape from a 40 mm streched diamond mesh trawl codend in the Aegean Sea. Sci. Mar. 74: 755-761.. Codend covers were used to collect escapees (Fig. 2). At the end of each haul, the cover was detached from the trawl net. The cover was then moved by divers to an inshore site, where it was anchored to the seabed to form a cage for later monitoring of the fish. During this process, divers moved the cover very slowly to reduce the effect of water flow on fatigued fish in the cage. EGEDERİN (10 m length, 121 kW) was used as a support boat for diving operations. For the control group, fish escaping from an open codend were caught in the same type of codend cover.

The cages for housing the sampled populations (i.e. the anchored covers) had an internal volume of 7.5 m³ and were horizontally stretched out on the seabed using ropes and wooden rods at depths of 3.0 to 8.2 m. They were made of knotless, polyamide (PA) netting (24-mm stretched mesh size) to minimize abrasive injury. The length of the cages after they had been fixed on the seabed was 7.5 m. Their maximum circumference was maintained by two rigid hoops of 1.6 m diameter. The cages were rigged with three 1-m-long horizontal zippers to retrieve any dead fish and to feed the survivors. They were observed by divers three times a day (07:00-08:00; 12:00-13:00 and 16:30-17:30) over a period of 7 days. The behaviour of the captive fish was monitored by divers using underwater camera systems (Sony PC350E, Sea and Sea housing).

During the monitoring period, dead fish were removed and transferred to the laboratory for measuring. Total (TL) and standard lengths (SL) were measured to the nearest mm. If the caudal fin of a fish was injured, SL was transformed to TL. Escape mortality (F_E) was calculated as F_E = n_m/(n_m+n_s), where n_m is the number of dead fish and n_s is the total number of survived fish in a fish cage. At the end of the observation period, the cages were retrieved, survivors were counted and their lengths were measured.

To investigate possible effects of fish condition on escape mortality, Fulton’s condition factor (K) was determined. The factor describes the relationship between total length and weight of an individual fish in terms of

K = W L^–3

where K is the Fulton’s condition factor, W the weight of the fish and L the length (total length, TL) (Ricker 1973Ricker W.E. 1973. Linear regressions in fishery research. J. Fish. Res. Board of Canada 30: 409-434.). The length-weight relationship (LWR) was derived by applying the equation

W = aL^b

where a and b are the coefficients calculated by the least squares method (Sparre 1987Sparre P. 1987. Introduction to tropical fish stock assessment (Part 1. Manual). FAO Fish. Tech. Pap. 101 Suppl. 2: 1-114.). Sex (male and female) was determined by internal examination.

The red mullet survival data were analysed using generalized linear modelling (GLM) (McCullagh and Nelder 1999McCullagh P., Nelder J. 1999. Generalized Linear Models. Second Edition. Chapman and Hall/CRC, London.), fitted using the binomial error distribution and logit-link function. The significance of several explanatory variables was explored using GLM, including mesh size and shape, season (summer and winter), fish length, and various interactions between them. The 2011 and 2012 data were modelled separately to avoid over-parameterisation. In addition, to address concerns that there may be captive density-dependent mortality, a term for cage stocking density (fish m^–3) was included in the GLM; however, this proved to be not significant for both years (P values for 2011: 0.7727; 2012: 0.1071) and hence it was excluded from the final models. For both models, due to over-dispersion, it was necessary to estimate the dispersion parameter (Φ₂₀₁₁: 1.73; Φ₂₀₁₂: 1.52).

An F test was used to analyse the LWR parameters between fish in codends and covers. The statistical significance of differences between K factors was determined with multi-factor ANOVA (MANOVA). Fitting of the GLM was performed using the R statistical program (R Development Core Team 2007R Development Core Team. 2007. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Version 2.6.1. Vienna, Austria. ), while the SPSS 15.0 statistical program was used for the other statistical analyses.

RESULTSTop

In total, 36661 individuals belonging to 66 species were caught during the experiments. Of these, approximately 80% were teleost. Higher catches were obtained in the summer experiments (Table 2).

2011 experiments: escape mortality

In winter, the mean water temperature at the study site was 13°C. In total, 54 species and 8179 individuals were caught. Of these, 45 species were teleost. With respect to relative numbers of codend escapees sampled in the cages (including open codend cages), red mullet was the most abundant species (2309), followed by annular seabream (1014) (Diplodus annularis, Sparidae), brown comber (823) (Serranus hepatus, Serranidae), solenette (694) (Buglossidium luteum, Soleidae), common pandora (596) (Pagellus erythrinus, Sparidae), scaldfish (572) (Arnoglossus laterna, Bothidae) and blotched picarel (515) (Spicara maena, Centracanthidae).

Escape mortality percentages and size distribution of red mullet in winter are shown in Figures 3 and 4 and Table 3. A total of 2309 red mullet were caught during the experiments, both in codend and cover. Of these, 679 red mullet ranging from 8.5 to 16.5 cm TL were caught in the test cages. A total of 252 individuals ranging from 10.0 to 18.5 cm TL were obtained in open codend cages. Mean mortalities were 31.3%±10.07, 30.3%±30.78 and 37.4%±18.11 for fish escaping from 40-mm square-mesh and 44- and 50-mm diamond-mesh codends, respectively. Mean mortality in open codend cages was 48.3% (±11.09).

In summer, the water temperature around the cages was 25°C. In total, 43 species and 13054 individuals were caught, of which 34 species were teleost. Of these, red mullet (4268) was again the most abundant species, followed by blotched picarel (2295), sardine (1197) (Sardina pilchardus, Clupeidae), red bandfish (891) (Cepola macrophthalma, Cepolidae), brown comber (772), annular seabream (618) and black goby (584) (Gobius niger, Gobiidae). A total of 2618 red mullet ranging from 6.5 to 15.5 cm TL were caught in the test cages, while 873 individuals ranging from 6.5 to 20.0 cm TL were captured in the open codend cages. Mean mortalities were 22.4%±4.75, 33.4%±13.92 and 24.6%±18.67 for red mullet escaping from 40-mm square-mesh and 44- and 50-mm diamond-mesh codends, respectively (Figs 3 and 5, and Table 3). Mean mortality for open codend cages was 39.7%±23.08.

2012 experiments: escape mortality

A total of 4798 individuals and 49 species were caught in 12 experimental hauls in winter; of these, 40 species were teleost. Red mullet (1378) was the most abundant species, followed by common pandora (780), solenette (631) and blotched picarel (590). Mean water temperature was 13°C at the cage site. In the test hauls, 930 red mullets ranging from 7.0 to 16.5 cm TL were caught, while in open codend hauls 134 individuals ranging from 9.0 to 18.0 TL were caught. Figs 4 and 5 and Table 3 show escape mortality percentages and size distribution of red mullet. Mean mortalities were 26.3%±12.67, 46.3%±2.38 and 27.4%±8.37 for red mullet escaping from 40-mm square-mesh and 44- and 50-mm diamond-mesh codends into the codend covers, respectively. Mean mortality for open codend cages was 51.5%±7.24.

A total of 10630 individuals and 54 (40 teleost) species were sampled in September 2012. Red mullet (3170) was the most abundant species, followed by anchovy (1122) (Engraulis encrasicolus, Engraulidae), brown comber (1103), black goby (814), red bandfish (778), blotched picarel (593) and solenette (421). Mean water temperature was 25°C around the cages. A total of 1964 red mullet individuals ranging from 6.0 to 18.5 cm TL were caught by the test codends, while a total of 779 individuals ranging from 6.5 to 19.0 cm TL were caught in open codend hauls. Mean mortalities were 22.2%±8.49, 35.4%±30.67 and 21.3%±3.06 for red mullet escaping from 40-mm square-mesh and 44- and 50-mm diamond-mesh codends, respectively (Figs 4 and 5 and Table 3). Open codend cages had a high mean mortality of 49.1%±16.18.

Length-related mortality, and seasonal- and mesh-type effects on mortality

There was a clear length-related mortality in most treatments, with smaller fish having an increased likelihood of dying after escaping (Fig. 5, Tables 4 and 5). The only exception was the 44-mm diamond-mesh treatment in summer 2011, but this had small sample sizes (Fig. 3, Tables 3 and 6).

A seasonal effect on the length-related mortality was observed in both 2011 and 2012, with smaller fish (<13 cm TL) showing lower mortality in summer than in winter (Fig. 5 and Table 6). For larger fish, this seasonal effect seems less apparent. Although the mean size of escaping fish was smaller in summer than in winter (Figs 3 and 4, Table 3), the mean mortality of red mullet was generally higher in each treatment in winter (2011, 33.0%; 2012, 33.3%) than in summer (2011, 26.8%; 2012, 26.3%). Furthermore, the GLM demonstrated a highly significant seasonal effect (p<0.0001), as well as a highly significant interaction between length-related mortality and season (Length:Season p<0.0001) in both years (Tables 4 and 5).

There were also significant differences in mortality according to the different mesh sizes in both years (p<0.0001) (Tables 4 and 5). Generally, the 40-mm square-mesh and 50-mm diamond-mesh codends showed the lowest mortality, irrespective of fish size. The exception to this was observed in winter 2011, when the 44-mm diamond-mesh codend showed the lowest mortality across all length classes. However, we highlight that sample sizes were small for this treatment in that season, so it may not be truly representative. In all size cases, the open codend control treatments showed the highest observed mortality, particularly for the smallest fish.

Cumulative mortality during the monitoring period

Most of the mortality occurred in the first 48 hours of the observation period (Fig. 6). In winter 2011, 45%, 62%, and 48% of the mortality for the 40-mm square-mesh and the 44- and 50-mm diamond-mesh codends, respectively, were observed on the first day. In summer 2011, the mean percentage mortalities were 72%, 87% and 80% for the 40-mm square-mesh and the 44- and 50-mm diamond-mesh codends, respectively, in the first 24 hours. In winter 2012, 62%, 67%, and 53%, and in summer 2012, 80%, 88%, and 85% of mortalities for the 40-mm square-mesh and the 44- and 50-mm diamond-mesh codends, respectively, occurred on the first day.

The relationship between escape mortality and Fulton’s K factor

K factors for dead fish (mean 0.9360) and survivors (mean 0.9569) (K<1) escaping from codends were significantly different from those of the fish retained in the codend (mean 1.0980) (K>1; p<0.01) for all experiments (Table 7). On the other hand, in terms of K factor, there was no significant difference between dead fish and survivors (p>0.01) of the escapees for all the hauls.

In all experiments, the mean weight of dead fish was 24% lower than that of the survivors. Mean weights of retained fish were 54.1% and 43.1% higher than those of the dead fish and survivors, respectively. There were significant differences in the LWR parameters (p<0.001) between the individuals retained in the codend and the escapees in the cover. On the other hand, no significant differences were observed between the LWR parameters of the dead individuals and the survivors in any of the experiments (p>0.01). The exponents (b) of the LWR for dead, surviving and retained fish (means; 3.292, 3.288, and 3.241, respectively) indicated that relative growth of red mullet followed a positive allometry (the change in weight in relation to proportional changes in body size). In winter (2011 and 2012), Fulton’s K factor was significantly different among the dead (0.9266 and 0.8591), surviving (1.0260 and 0.9239) and retained fish (1.1320 and 1.0317) (p<0.001). In summer 2011 and 2012, K factors of dead (0.9508 and 1.0073) and surviving (0.9461 and 0.9317) fish were significantly different from those of the retained fish (1.1368 and 1.0917) (p<0.001).

The relationship between escape mortality and sex

A total of 4930 dead and surviving red mullet were examined to determine sex (Table 8). The mortality of immature fish (mean 67%) was greater than that of mature fish (mean 15% females and 16% males) for all experiments. There was no significant difference (p>0.01) between the escape mortality of females and males; on the other hand, there was a significant difference (p<0.01) between mortality of immature specimens and that of males and females.

DISCUSSIONTop

The main aim of this study was to compare the survival of escapees of red mullet from square- and diamond-mesh codends of otter bottom trawl. We used hauls with open codends in an attempt to have methodological controls for the experiment, according to ICES (2014)ICES. 2014. Report of the Workshop on Methods for Estimating Discard Survival (WKMEDS), 17-21 February 2014, ICES HQ, Copenhagen, Denmark. ICES CM 2014/ACOM: 51. 114 pp., as this was the only method available to catch red mullet as control fish in a size range comparable to the test subjects. Specimens caught with this method showed a significantly higher mortality than the treatments. Similarly, Metin et al. (2004)Metin C., Tokaç A., Ulaş A., et al. 2004. Survival of red mullet (Mullus barbatus L., 1758) after escape from a trawl codend in the Aegean Sea. Fish. Res. 70: 49-53., who also collected control fish using an open codend, reported a significantly higher mortality of red mullet in the control than in the tested codend cages. In the same area, the Aegean Sea, similar controls were abandoned by Düzbastılar et al. (2010b)Düzbastılar F.O., Özbilgin H., Aydın C., et al. 2010b. Mortalities of fish escaping from square and diamond mesh codends in the Aegean Sea. Fish. Res. 106: 386-392. due to a higher density of fish and the presence of predators in the control cage. This approach only controls for escape through the codend meshes, while the fish are subjected to other stresses (e.g. exhaustion, physical contact with the net and catch), so it should not be considered as a valid methodological control. The higher mortality in the open codend may have been induced by the forced swimming and the injuries, through skin abrasion, in the codend cover, as a result of the excessive water flow (Suuronen et al. 1996bSuuronen P., Lehtonen E., Tschernij V., et al. 1996b. Skin injury and mortality of Baltic cod escaping from two codends equipped with exit windows. Arch. Fish. Mar. Res. 44: 165-178., Breen 2004Breen M. 2004. Investigating of the mortality of fish escaping from towed fishing gears- a critical analysis. PhD thesis, Univ. Aberdeen, Scotland, 321 pp.). Future studies should aim to develop methods for the collection of more valid methodological controls. However, where this is unavoidable, the use of a lined codend and/or codend cover may reduce exhaustion and the risk of physical injuries (Breen et al. 2007Breen M., Huse I., Ingólfsson O.A., et al. 2007. An assessment of mortality in fish escaping from trawl codends and its use in fisheries management. Quality of Life and Management of Living Resources Q5RS-2002-01603, 300 pp.).

The experimental hauls used in this study have different characteristics from those of the commercial fishing hauls, as they were shallower (10-30 m, compared with 50-150 m) and shorter (15 min, compared with 1-6 hours) than commercial trawl hauls. The shallow depth was chosen to enable the divers to operate at safe depths. The short hauling time was necessary to avoid over-filling the sampling cages with fish. Moreover, the limited resources available for this project did not allow the use of more technologically advanced sampling techniques, which would allow short sampling times following long fishing tows (e.g. Lehtonen et al. 1998Lehtonen E., Tschernij V., Suuronen P. 1998. An improved method for studying survival of fish that escape trawl-codend meshes. Fish. Res. 38: 303-306. and Breen et al. 2007Breen M., Huse I., Ingólfsson O.A., et al. 2007. An assessment of mortality in fish escaping from trawl codends and its use in fisheries management. Quality of Life and Management of Living Resources Q5RS-2002-01603, 300 pp.). Finally, extending the towing duration to 3 to 6 hours in this experiment would have meant that fish were collected over a much wider depth range, and would have exposed them to higher decompression stress.

The lack of valid methodological controls and the deviance from standard commercial fishing practices may undermine our confidence in the absolute estimates of the magnitude of the escape mortality, as the methodology may have induced some of the observed mortality in the treatment cages (ICES 2014ICES. 2014. Report of the Workshop on Methods for Estimating Discard Survival (WKMEDS), 17-21 February 2014, ICES HQ, Copenhagen, Denmark. ICES CM 2014/ACOM: 51. 114 pp.). However, the consistent and highly significant effects observed between treatments (i.e. season, as well as mesh size and shape) may provide strong evidence that these effects influence the survival of red mullet escaping from trawl codends, although the magnitude of these effects remains uncertain. Furthermore, this experiment observed a length-related mortality, which is consistent with other escape mortality studies (Suuronen 2005Suuronen P. 2005. Mortality of fish escaping trawl gears. FAO Fish. Tech. Pap. 478: 72 pp.).

A size-related mortality has previously been described for red mullet (Lök et al. 2002Lök A., Metin C., Özbilgin H., et al. 2002. Survival ratios of red mullet (Mullus barbatus) and annular sea bream (Diplodus annularis) after escaping from trawl codend in the Eastern Aegean Sea. ICES CM 2002/V:08.), as well as for other species (Sangster et al. 1996Sangster G.I., Lehmann K., Breen M. 1996. Commercial fishing experiments to assess the survival of haddock and whiting after escape from four sizes of diamond mesh codends. Fish. Res. 25: 323-345., Wileman et al. 1999Wileman D.A., Sangster G.I., Breen M., et al. 1999. Roundfish and nephrops survival after escape from commercial fishing gear. Final Report, EC Contract FAIR-CT95-0753, Brussels., Breen 2004Breen M. 2004. Investigating of the mortality of fish escaping from towed fishing gears- a critical analysis. PhD thesis, Univ. Aberdeen, Scotland, 321 pp.). Likewise, many studies have shown an inverse relationship between physical injury and fish length (Suuronen et al. 1996aSuuronen P., Erickson D.L., Orrensalo A. 1996a. Mortality of herring escaping from pelagic trawl codends. Fish. Res. 25: 305-321.). This study has shown that length-related mortality was significantly more pronounced in winter, particularly for the smallest specimens. This finding suggests that the observed mortality may be related to the physical condition of the fish: the fish less nourished during winter months may be physically less able to avoid and/or recover from exhaustion and physical injuries during the catching process (Chopin and Arimoto 1995Chopin F., Arimoto T. 1995. The condition of fish escaping from fishing gears - a review. Fish. Res. 21: 315-327., Breen 2004Breen M. 2004. Investigating of the mortality of fish escaping from towed fishing gears- a critical analysis. PhD thesis, Univ. Aberdeen, Scotland, 321 pp.).

Fulton’s K factor (Ricker 1973Ricker W.E. 1973. Linear regressions in fishery research. J. Fish. Res. Board of Canada 30: 409-434.) can give an indication of the condition of fish. It varies with, and is strongly affected by, age, sex, environment, water temperature, feeding pattern and stress factors (Barton and Schreck 1987Barton B.A., Schreck C.B. 1987. Metabolic cost of acute physical stress in juvenile steelhead. Trans. Am. Fish. Soc. 116: 257-263., Carscadden and Frank 2002Carscadden J.E., Frank K.T. 2002. Temporal variability in the condition factors of Newfoundland capelin (Mallotus villosus) during the past two decades. ICES J. Mar. Sci. 59: 950-958.). This study demonstrated that K values in September were generally higher than those in winter for all the specimens. Özbilgin et al. (2011)Özbilgin H., Tosunoğlu Z., Tokaç A., et al. 2011. Seasonal variation in the trawl codend selectivity of red mullet (Mullus barbatus). Turkish J. Fish. Aquat. Sci. 11: 191-198. reported that the condition factors at minimum landing size of red mullet were 1.0187 (January), 1.0555 (April), 1.0710 (July) and 1.0765 (September).

Water temperatures in İzmir Bay were substantially lower in winter (13°C) than in summer (25°C). Thus, an alternative explanation of the lower survival rates in winter months, particularly among smaller fish, is the lower swimming ability due to lower water temperatures (He and Wardle 1988He P., Wardle C.S. 1988. Endurance at intermediate swimming speeds of Atlantic mackerel, Scomber scombrus L., herring, Clupea harengus L., and saithe, Pollachius virens L. J. Fish. Biol. 33: 348-360., Özbilgin and Wardle 2002Özbilgin H., Wardle C.S. 2002. Effect of seasonal temperature changes on the escape behaviour of haddock, Melanogrammus aeglefinus, from the codend. Fish. Res. 58: 323-331.). There is some controversy about this aspect: Düzbastılar et al. (2010a)Düzbastılar F.O., Özgül A., Aydın İ., et al. 2010a. A preliminary study on the survival of brown comber, Serranus hepatus (Actinopterygii, Perciformes, Serranidae), escaping from the codend of a bottom trawl. Acta Ichthyol. Piscat. 40: 27-36. found that the mortality of brown comber escaping from diamond-mesh codends was not affected by water temperature (13°C and 25°C); conversely, Suuronen et al. (2005)Suuronen P., Lehtonen E., Jounela P. 2005. Escape mortality of trawl-caught Baltic cod (Gadus morhua) - the effect of water temperature, fish size and codend catch. Fish. Res. 71: 151-163. observed lower mortality of cod at lower water temperatures (<10°C compared with >15°C).

The seasonal differences in abundance and size distribution of red mullet agree with the characteristics of the ecology of the species. Red mullet is a warm-water fish (18°C) that is homogenously distributed around the Mediterranean Sea (Cheung et al. 2013Cheung W.W.L., Watson R., Pauly D. 2013. Signature of ocean warming in global fisheries catch. Nature 497: 365-369.). The species shows a discrete recruitment concentrated in late summer; Kınacıgil et al. (2001)Kınacigil H.T., İlkyaz A.T., Akyol O., et al. 2001. Growth parameters of Red Mullet (Mullus barbatus L.,1758) and seasonal cod-end selectivity of traditional bottom trawl nets in Izmir Bay (Aegean Sea). Acta Adriatica 42: 113-123. reported the first recruitment of red mullet in August in İzmir Bay, which explains the small mean size of the specimens caught in this study in September. In winter, the species moves to deeper waters to avoid lower temperatures.

The results of this study demonstrate that escape mortality is also affected by mesh size, with increasing mesh size from 44 mm to 50 mm generally reducing escape mortality. It has been hypothesized that increasing codend mesh size may reduce mortality, because larger meshes reduce the risk of abrasive injury when escaping fish pass through them (Lowry et al. 1996Lowry N., Sangster G.I., Breen M. 1996. Codend selectivity and fish mortality. European Commission Study Contract No. 1994/005, Brussels, EC, Final Report., Suuronen 2005Suuronen P. 2005. Mortality of fish escaping trawl gears. FAO Fish. Tech. Pap. 478: 72 pp.). Other studies have reported that codend mesh size is not related to fish mortality and has only small effects on the survival of escaping fish (Sangster et al. 1996Sangster G.I., Lehmann K., Breen M. 1996. Commercial fishing experiments to assess the survival of haddock and whiting after escape from four sizes of diamond mesh codends. Fish. Res. 25: 323-345., Suuronen et al. 1996aSuuronen P., Erickson D.L., Orrensalo A. 1996a. Mortality of herring escaping from pelagic trawl codends. Fish. Res. 25: 305-321., Wileman et al. 1999Wileman D.A., Sangster G.I., Breen M., et al. 1999. Roundfish and nephrops survival after escape from commercial fishing gear. Final Report, EC Contract FAIR-CT95-0753, Brussels.).

The mesh shape also appears to play a role in reducing escape mortality (Main and Sangster 1990Main J., Sangster G.I. 1990. An assessment of the scale damage to and survival rates of young fish escaping from the codend of a demersal trawl. Scottish Fish. Res. Rep. Report 46: 90., Suuronen 2005Suuronen P. 2005. Mortality of fish escaping trawl gears. FAO Fish. Tech. Pap. 478: 72 pp.), because round fish may escape more easily through square-mesh than through diamond-mesh codends (Suuronen 2005Suuronen P. 2005. Mortality of fish escaping trawl gears. FAO Fish. Tech. Pap. 478: 72 pp.). Moreover, Düzbastılar et al. (2010b)Düzbastılar F.O., Özbilgin H., Aydın C., et al. 2010b. Mortalities of fish escaping from square and diamond mesh codends in the Aegean Sea. Fish. Res. 106: 386-392. found that the 40-mm square-mesh codend produced a higher mean survival rate for red mullet than the 44-mm diamond-mesh codend. In the present study, though the mesh size of the square-mesh codend was smaller than that of the other test codends, it showed lower mortality than the 44-mm diamond-mesh codend and comparable mortality to the 50-mm diamond-mesh codend.

The overall mortality of red mullet escaping from codends (21.3-35.4%) was greater than those reported in previous experiments performed at the same site in summer (<7%, Metin et al. 2004; 5-9%, Düzbastılar et al. 2010bDüzbastılar F.O., Özbilgin H., Aydın C., et al. 2010b. Mortalities of fish escaping from square and diamond mesh codends in the Aegean Sea. Fish. Res. 106: 386-392.). This difference may be due to a larger number of replicates (48 hauls), the trawl net characteristics (mesh size and number of meshes), the presence of predators (e.g. rays) in the cages and the trawling conditions (e.g. weather).

To date, few studies have been done to quantify the effect of sex and sexual maturity on the mortality of escaping fish. Wileman et al. (1999)Wileman D.A., Sangster G.I., Breen M., et al. 1999. Roundfish and nephrops survival after escape from commercial fishing gear. Final Report, EC Contract FAIR-CT95-0753, Brussels. reported no effects of sex on the escape mortality of sexually immature haddock and whiting. In the present study, we determined that there was no significant difference in escape mortality due to sex. The significantly higher escape mortality found in immature fish corresponds to the inverse length-related mortality.

In conclusion, this study has demonstrated that codend escapee mortality for red mullet is higher, particularly for the smallest fish, in winter months, which coincide with low water temperature and poorer physical condition. Codend mesh size and shape and fish condition and size (fish length) are also factors significantly affecting escape mortality. However, due to a lack of valid methodological controls, there is some uncertainty about the absolute magnitude of the mortality estimates. For fishery management purposes, escape mortality investigations should be carried out together with selectivity studies to consider the likely factors affecting mortality.

ACKNOWLEDGEMENTSTop

This study was part of the project 110O335 funded by the TÜBİTAK (Scientific and Technological Research Council of Turkey). We would like to thank Drs İlker Aydın and Cengiz Metin from the Fisheries Faculty, Ege University, and MSc and PhD students of the Fisheries Faculty, Ege University, for their assistance during the experiments and analyses, as well as the crew and skippers of the dive boats EGE DERİN and the R/V EGESÜF.

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