Bottom trawl fisheries, which are generally multispecies in the Mediterranean Sea, have rather poor selectivity (Özbilgin et al. 2006, Sardà et al. 2006). 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 2005, Breen et al. 2007, Sacchi 2008). However, increasing trawl selectivity may only be justified if a significant proportion of the escaping fish survive (Suuronen 2005, Gilman et al. 2013). Escape mortality has been described by ICES (2005) as “fish that die after actively escaping from a gear prior to the catch being landed by the fishing operation” (Suuronen 2005, Broadhurst et al. 2006). 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. 1996, Main and Sangster 1988), Norway (Soldal and Engås 1997), the USA (DeAlteris and Reifsteck 1993) and Australia (Broadhurst et al. 1997), and in the Baltic Sea (Suuronen et al. 1996a, b), and the Barents Sea (Ingólfsson et al. 2007).

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. 2006). A number of scientific studies have been carried out to improve trawl codend selectivity in the Aegean Sea (Petrakis and Stergiou 1997, Metin et al. 2005). However, few studies have investigated the escape mortality of fish escaping from the trawl codend in the Mediterranean Sea (Metin et al. 2004, Düzbastılar et al. 2010a, b, c).

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.

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. 2012).

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 2008). 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 2006).

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 2004). 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 2008). 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) and Düzbastılar et al. (2010a, b, c). 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 1973). 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 1987). Sex (male and female) was determined by internal examination.

The red mullet survival data were analysed using generalized linear modelling (GLM) (McCullagh and Nelder 1999), 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 2007), while the SPSS 15.0 statistical program was used for the other statistical analyses.

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).

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), 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), 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) 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. 1996b, Breen 2004). 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. 2007).

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. 1998 and Breen et al. 2007). 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 2014). 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 2005).

A size-related mortality has previously been described for red mullet (Lök et al. 2002), as well as for other species (Sangster et al. 1996, Wileman et al. 1999, Breen 2004). Likewise, many studies have shown an inverse relationship between physical injury and fish length (Suuronen et al. 1996a). 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 1995, Breen 2004).

Fulton’s K factor (Ricker 1973) 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 1987, Carscadden and Frank 2002). This study demonstrated that K values in September were generally higher than those in winter for all the specimens. Özbilgin et al. (2011) 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 1988, Özbilgin and Wardle 2002). There is some controversy about this aspect: Düzbastılar et al. (2010a) 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) 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. 2013). The species shows a discrete recruitment concentrated in late summer; Kınacıgil et al. (2001) 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. 1996, Suuronen 2005). 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. 1996, Suuronen et al. 1996a, Wileman et al. 1999).

The mesh shape also appears to play a role in reducing escape mortality (Main and Sangster 1990, Suuronen 2005), because round fish may escape more easily through square-mesh than through diamond-mesh codends (Suuronen 2005). Moreover, Düzbastılar et al. (2010b) 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. 2010b). 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) 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.