Mediterranean fisheries are characterized by a high rate of unwanted catches and a great number of marine organisms that are discarded at sea (Lleonart 2015, Tsagarakis et al. 2014). One of the fishing methods that produces most discards is otter bottom trawling, which is also one of the least selective fishing gears. The discards include both species with non-commercial value and marketable species that are undersized or of low value. Technical regulations, such as the introduction of the 40-mm square mesh or the 50-mm diamond mesh in the cod-end (EC 1967/2006) can reduce discards to some extent, but cannot solve the impacts of bottom trawling on habitats and benthic communities.

The investigated areas were the Catalan coast, corresponding to FAO division 37.1.1, Geographical Sub-Area 6 (GSA06), and the Ligurian and northern Tyrrhenian seas, corresponding to FAO division 37.1.3, Geographical Sub-Area 9 (GSA09), both comprising chronically exploited fishing grounds. In the last ten years the demersal fisheries carried out mainly by bottom trawl fleets in the two areas accounted for about 40% of the total landings and 70% of the economic value (STECF 2016).

A large fraction of this discarded biomass (30%-50% of the total biomass caught) is composed of species of commercial interest (small-sized or damaged specimens), while the remaining fraction is composed of species with low or no economic value (Machias et al. 2001, Sánchez et al. 2004, 2007). Furthermore, trawl fleets operate in a great variety of soft habitats (e.g. muddy-sand, sandy-muddy, mud, sandy-gravel, sand), so discards are characterized by extremely high species diversity with a high percentage of non-commercial species, some of which are macroinvertebrates (echinoderms, crustaceans, poriferans, ascidians, cnidarians, bryozoans, bivalves and gastropods). In many cases the discarded species belong to sensitive benthic habitats, such as maërl or crinoid beds.

The impact of bottom trawling on benthic habitats and communities and demersal species is little known. The impact depends on the fishing activity (Martín et al. 2014) and can create changes in the ecological functioning of benthic components that have important repercussions on the exploited populations (de Juan et al. 2007, Frid 2011, Hewitt et al. 2008).

The European Marine Strategy Framework Directive (EU 2008/56/E) encourages member states to move towards an ecosystem-based fishery management in order to protect the goods and services that marine ecosystems provide. Therefore, it is important to take into account the link between benthic communities and habitats and fisheries resources, because a great number of ecological interactions may be adversely impacted by fishing. The capture of benthic invertebrates and their discarding at sea will impact benthic habitats to a certain degree, depending on the post-release survival of each species. The survival of habitat-structuring invertebrates, such as crinoids and echinoderms, can help to maintain the good status of the essential fish habitats where the most important commercial resources, such as European hake, red mullet, spiny lobster and cuttlefish, use them as areas of nursery, recruitment or growth (Abella et al. 2008, Colloca et al. 2009).

There is currently very little information on the survival of unwanted and unregulated invertebrates after the stresses of being captured, handled and discarded. The specific biological characteristics make an organism more or less vulnerable to different stressors of the capture method and release process (de Juan and Demestre 2012). Other factors affecting the survival of released animals are related to the handling practices during the sorting and release processes and to the environmental conditions during capture, hauling on board and sorting, such as hypoxia and temperature (Bergmann et al. 2001, Giomi et al. 2008, Tsagarakis et al. 2017).

Some unwanted and unregulated invertebrates such as crinoids and ophiuroids form the basis of essential fish habitats for commercial species such as hake and red mullet. Robust information on discard survival after fishing and release to the seabed can improve the interpretation of the role of unregulated invertebrates on the benthos (Benoît et al. 2012).

The main objective of this paper was to estimate survival rates of invertebrates discarded from trawlers working in two northwestern Mediterranean areas, the Catalan coast and the Ligurian and northern Tyrrhenian seas. The study focused on unwanted invertebrates which belong to the unregulated species and are likely to continue to be released after capture. To estimate the vitality rates, a vitality assessment on the captured organisms was carried out under normal fishing activity of the trawl fleets in both selected areas. The approach was developed using a semi-quantitative assessment (SQA) (ICES 2014) according to Benoît et al. (2012). Two different procedures of survival estimation were developed, considering first the survival on the deck of trawlers and second the long-term survival at the laboratory with captive observations. The survival rate of the discarded fraction in the trawl catch can be used to propose management based on better control of discards or spatial restrictions to trawling that may accompany specific management plans based on conserving the functionality and health of benthic ecosystems.

This study was carried out with those individuals that showed signs of vitality when arriving on board, which means they were still alive. In fact, there was a low number of specimens that could be assessed, and this may indicate the severe impact of trawling on the seabed and benthic communities (Kaiser and Spencer 1995, Jennings et al. 2001). The preservation of exploited resources is probably the main goal of fishery management, but the perturbation of chronic fishing activity on fishing grounds has negative ecological effects leading to high levels of mortality (DFO 2006, van Denderen et al. 2013).

Several studies have evidenced an improvement in the health of exploited resources when effort limitation and seasonal or temporal closures of trawl fishing activities are implemented (Demestre et al. 2008, Demestre et al. 2015, Pipitone et al. 2000), but the effects at the level of benthic communities remain less well known. The by-catch of invertebrates in bottom trawling yields a high amount of epifauna or infauna that have important functions for the sea floor ecology. For instance, echinoderms or gastropods are important bioturbators and comprise several feeding guilds, such as deposit or filter feeders, or predators (e.g. Echinus melo, Spatangus purpureus, Echinaster sepositus, Ophiura texturata, Chlamys opercularis, Calliostoma granulatum and Aporrhais serresianus). These organisms play an important role in ecosystem function by maintaining or enhancing secondary marine production. They are very sensitive to disturbance and easily destroyed by fishing impact, and their decrease could have lasting consequences for benthos-pelagic processes (Lohrer et al. 2004, Demestre et al. 2017, de Juan et al. 2011), because the good status of the habitats in which the fisheries resources live depends to a large extent on these organisms.

In order to maintain the good status of the sea bottom, one of the priority actions to be taken is to determine the mortality levels of routinely discarded species. A study carried out near the Catalan coast area related the effects of trawl fishing and feeding of the red mullet Mullus barbatus (Muntadas et al. 2015), showing negative effects due to changes in benthic functional components in the fishing ground. In areas where there was no fishing (fishing closure areas) the macroinfauna which constitutes the food base for M. barbatus was significantly more abundant than in areas disturbed by the trawl. Changes in the habitat structure (homogenization) and functionality of benthic communities caused by fishing can alter the normal supply of food (e.g. polychaetes and crustaceans) for both adult and juvenile red mullet (Fiorentino et al. 2008, Muntadas et al. 2014). Furthermore, as a consequence of the habitat alteration, the characteristics of the seabed that serves as a nursery, spawning or growing habitat could be modified, with possible negative consequences on future recruitment of the species.

The rates of survival shown by invertebrates in both areas investigated in this study showed great variability between VLs of the same species once the individuals had been captured and deposited on the deck of the trawler. Mortality levels also vary from one species to another, depending mainly on the biological and functional traits of each species, such as fragility, emergent or surface position, filter feeding and sedentary motility (Costello et al. 2015, Muntadas et al. 2015). External protection is one of the most relevant traits for increasing survival, as evidenced by the monitoring of VLs on deck to analyse immediate mortality. In both areas the majority of crustaceans remained alive, even reaching percentages of 100%. Invertebrates with regeneration traits such as echinoderms also have a high level of survival.

We went one step further in estimating discarded invertebrate mortality by attempting to identify and separate the injuries of each individual on deck according to its VL. Individuals with VL 1 and 2 at time T0 (time of release on deck) survived on deck until they were released into the sea in a maximum time of 30 min, but those with VL 3 showed low survival on deck. The experiments at the laboratory to analyse survival at 96 h confirmed this behaviour for all analysed species. At the laboratory it was evident that when the survival was not 100% it was because the organism was at VL 3 when released on deck, and in fewer cases at VL 2.

The results of the Wilcoxon test indicated that Haul Time was an important factor for improving organisms’ survival on deck. Injuries increased and VL decreased when invertebrates arrive on deck after long hauls, as was observed in the continental shell hauls, which showed a higher survival of species of crinoids and crustaceans (Table 4 and Figs 3-5). Consequently, failure of individuals to survive for a long time in the laboratory experiment is due to their low VL when they were left on deck. It is therefore important to handle the organisms on deck quickly and safely to increase their survival when they are discarded back into the sea. During fishing operations on deck, it is recommendable to keep the organisms under a wet cover to avoid drying. Another easy method for improving the survival of discards could be a direct operating system such as a duct with water from the deck for throwing animals back into the sea.

It must be taken into account that, in addition to the unhealthy state of the invertebrates who died during the experiment, the mortality may also have been due to the captivity conditions, where no food was available and the environment was only similar to the most appropriate habitat. However, the possibility of discarded invertebrates escaping predators or obtaining food is low because of the injuries they suffer during capture (Ramsay et al. 1996, Bergmann and Moore 2001, IngólfssonIng et al. 2007). Therefore, our experimental results can be assumed as a proxy to the level of survival of discards at sea.

According to the Common Fisheries Policy and the landing obligation to prevent discarding of regulated species (MCRS, Council Reg. EC 1967/2006, Art. 15.4b), a high level of post-capture survival can be adduced by member states to include an exemption from the landing obligation in their discard management plans. Our results for the survival of N. norvegicus can be considered a starting point with information focused on the aim of a possible species exemption but, obviously, more studies based on larger samplings need to be carried out before this exemption can be recommended. Conversely, a second crustacean species regulated by MCRS, Parapenaeus longirostris, showed low survival and would not be a good candidate for exemption.

The species selected for survival estimations were the most representative of different taxonomic levels and were of ecological importance in their habitats. In view of this, the 100% survival of the crinoids A. mediterranea and even L. phalangium, whose increase in post-release mortality started at VL 3, shows that the impact of trawling on crinoid beds may be less serious than assumed until now, as most crinoid individuals would survive the encounter with trawlers and post-catch release. Furthermore, in many cases crinoid beds are essential habitats for nursery and spawning areas of some commercial species (Colloca et al. 2004). The other two echinoderms that were assessed, O. texturata and E. sepositum, gave similar results, both starting mortality at VL 3. Therefore, the results may suggest again an optimistic possibility for maintaining a good environment status and a sustainable structure on the soft-sediment habitats that form the majority of trawl fishing grounds (Piet and Hintzen 2012). However, to maintain this optimistic perspective and a good environment status on the Mediterranean fishing grounds, it is mandatory to contain the current exploitation levels, especially in other types of habitat that may be even more sensitive to trawling than crinoid beds, such as maërl and Isidella (Kamenos et al. 2004, Mastrototaro et al. 2017). To achieve this, fishing activity and fishing effort must be reduced, temporal and spatial closures and even permanent closed areas must be implemented, and the measures regulating the reduction of discards must be implemented (FAO 2011).

The results of the present work offer some new knowledge on the survival of discarded invertebrates that may be useful for improving ecosystem health and productivity. Nevertheless, it should be regarded as a starting point, because mortality after discards at sea depends on many factors, such as susceptibility to predation and lower competitiveness for obtaining food (Bergmann and Moore 2001, Demestre et al. 2000, Kaiser et al. 2006). Knowing levels of survival of discarded invertebrates helps to obtain a more realistic image of the state of the benthic ecosystem, and consequently of the fishing grounds. The sustainability of the exploited populations depends on the conservation of these habitats, because a large part of their life cycle takes place in them.