Sizing up the role of predators on Mullus barbatus populations in Mediterranean trawl and no-trawl areas
Introduction
Fishing affects the structure and composition of fish populations and assemblages in different ways, leading to drastic changes in their size structure, abundance, composition and diversity (Bianchi et al., 2000; Gristina et al., 2006; McCauley et al., 2015). In intensely fished areas the loss of predatory biomass determine ultimately a reshuffle of trophic cascade processes (Estes et al., 2011; Pauly, 1998; Sala, 2004). In such cases a decline of the average trophic level of the fish community has often been observed, which is sometimes compensated by a biomass increase of the species at the base of the food web (Prugh et al., 2009) with a consequent alteration of the ecosystem functioning and of the integrity of benthic habitats (Bascompte et al., 2005; De Juan et al., 2007; Graham et al., 2017; Guillemot et al., 2014; Stevens et al., 2000; Thrush et al., 2011).
Historical studies have been carried out in different parts of the world that clearly suggest higher abundance and larger size of predators in ancient times (Lotze et al., 2011; McClanahan and Omukoto, 2011; Shaffer et al., 1998). In recent times, the assessment of the effects of marine protected areas (MPAs) provide an idea of the status of predatory fish assemblages before intense human exploitation. In particular, no-take MPAs have proven effective at replenishing fish stocks especially of predator species targeted by fishermen, restoring ecosystems and rebuilding food webs (Claudet et al., 2011; Edgar et al., 2014; Garcia Charton et al., 2000; Lester et al., 2009; Sala and Giakoumi, 2018). While such evidence comes mainly from coastal rocky habitats (Di Franco et al., 2018), data from soft-bottom offshore areas show that also partial protection, namely from industrial fishing may effectively lead to a recovery of fishery resources (Bailey, 1997; Fisher and Frank, 2004; Florin et al., 2013; Jaworski et al., 2006; Murawski et al., 2000).
In areas such as the Mediterranean Sea, where fisheries resources have been exploited for centuries (D’Arienzo and Di Salvia, 2010; Piroddi et al., 2015) it is hard to figure out the trophic relationships and the width and complexity of the trophic web in a pristine ecosystem where top predators must have been larger and more abundant (Jackson et al., 2001; Piroddi et al., 2015; Valdivia et al., 2017). Most Mediterranean MPAs have been established to protect inshore rocky areas and include zones at different degree of protection where the absence or strong reduction of fishing has often led to an increase of mesopredators like serranids, scorpaenids, seabreams and labrids, which are the main targets of artisanal and recreational fishermen (Di Franco et al., 2018, 2016; Sala et al., 2012). The effects of protection in Mediterranean MPAs however cannot be directly extrapolated to the ecosystem at a regional scale due to the small size of their no-take zones (<2 km2 in 60% of MPAs) (Di Franco et al., 2018). Fishery reserves and other spatial management tools created to limit or forbid non-selective fishing activities like trawling occur in larger, soft-bottom offshore areas that host the vast majority of Mediterranean commercial fisheries (Pipitone et al., 2014). To date, few studies have been performed on the ecosystem functioning and trophic structure of such large managed areas.
A case of Mediterranean fishery reserve is provided by two trawl exclusion areas implemented in 1990 off the northern Sicily coast in the Gulf of Castellammare (GCAST) and the Gulf of Patti (GPATT) (Pipitone et al., 2000; Whitmarsh et al., 2003). In GCAST the trawlable resources of the continental shelf, including piscivores like the hake Merluccius merluccius and the black bellied anglerfish Lophius budegassa recovered dramatically after the trawl ban (Badalamenti et al., 2008; Pipitone et al., 2000) and a similar, although less notable biomass increase was observed in GPATT (Potoschi et al., 2006). Despite the increase of teleosts, the elasmobranch assemblage did not seem to recover on the continental shelf of both gulfs (Arena and Bombace, 1970; Badalamenti et al., 2003) although a few species of sharks and rays are occasionally caught by professional fishermen (pers. observ.). Among soft-bottom benthic mesopredators the red mullet Mullus barbatus, an important target of Mediterranean fishing fleets (Tserpes et al., 2002) underwent an impressive biomass increment in GCAST and GPATT since the trawl ban (Pipitone et al., 2000; Potoschi et al., 2006, 1995), becoming one of the most abundant species in the trawlable assemblage (33.7%, 24% and 19.5% of total demersal biomass after 15 years of trawl ban in GCAST in the 10–50 m, 51–100 m and 101–200 m depth ranges respectively) (Badalamenti et al., 2003). The recovery of the red mullet was attributed to a concurrence of management effects and biological traits, namely the effects of reduced fishing mortality on its spawning stock biomass and on its recruitment pattern, an increased abundance of larger and more fecund females and an early age at first maturity (Fiorentino et al., 2008). Moreover in the Gulf of Castellammare, the trophic level of red mullet came out unexpectedly high (about 4.2 for adults with >13.5 cm total length) (Badalamenti et al., 2008) and close to that of top marine predators (Cortes, 1999; Jennings and Van Der Molen, 2015; Stergiou and Karpouzi, 2002), which was explained with an adult diet based on carnivorous polychaetes (Badalamenti et al., 2002).
Although a number of studies have investigated the trophodynamics of the red mullet including feeding habits (Caragitsou and Tsimenidis, 1982; Lipari et al., 1998; Vassilopoulou and Papaconstantinou, 1993), interspecific trophic interactions (Badalamenti et al., 1993), resource partitioning with other species (Bautista-Vega et al., 2008; Golani, 1994; Labropoulou and Papadopoulou-Smith, 1999) and trophic level (Badalamenti et al., 2008, 2002), the relationships with its predators remain poorly investigated. It is especially interesting to investigate such relationships in an ecosystem that is recovering from intense trawling, where theoretically it could be assumed that non-selective piscivores have a diet composed of more than 20% (i.e., mean biomass of all strata) of red mullet. Dell et al. (2015) have shown that longer and more complex food webs have developed in a tropical no-take MPA with changes in the diet of a mid-level consumer such as grouper, possibly as a consequence of increased prey availability. A similar situation could have developed in the two untrawled Sicilian gulfs, where the increased red mullet biomass represents a huge food resource to its potential predators. A few ecological questions arise: have predators increased as a consequence of protection? Have they benefited from an increased potential prey in the untrawled gulfs? Does the red mullet have the same importance as a prey in the different gulfs? In order to answer the above questions, we contrasted two untrawled and two trawled areas, to assess (i) what are the main predators of the red mullet, and (ii) if their biomass is higher in the untrawled areas.
Section snippets
Study area
The study area comprised four localities off the northern Sicily coast (Fig. 1): the Gulfs of Castellammare (GCAST, 38°03′N 12°54′E), Termini Imerese (GTERM, 38°00′N 13°44′E), Sant’Agata (GSANT, 38°03′N 14°23′E) and Patti (GPATT, 38°10′N 15°06′E). GCAST and GPATT are no-trawl areas subject to a year-round ban on commercial trawling since 1990 (Regional Act no. 25/1990), while artisanal and recreational fishing are permitted (Pipitone et al., 2000; Potoschi et al., 1995). GTERM and GSANT host
Identification of predators
The initial list of potential red mullet predators responding to basic ecological criteria, included ten elasmobranchs and nine teleosts (Table 1).
The red mullet exhibited the highest mean δ15N values in the two untrawled gulfs (GCAST: 10.62 ± 0.81‰, GPATT: 9.61 ± 0.62‰), while δ13C values were similar among all gulfs. The ellipse overlap analysis (Fig. 2, Table 3) suggests that, among the nineteen species initially identified, the following four species can be considered predators of the red
Discussion
Our study suggests that E. aeneus and L. budegassa are the main potential predators of the red mullet in the study area. Curiously, the feeding habits of these two fish genera are poorly studied overall, and this is particularly so for our two species. However, along the Ivorian coast (western Africa) E. aeneus is known to feed primarily on fish and secondarily on crustaceans (Kouassi et al., 2010) while in the Cyclades Islands (eastern Mediterranean) its main preys are fish followed by
Acknowledgements
Many thanks to Mr Giuseppe Di Stefano and Mrs Marilena Coppola for the precious help provided during field sampling and laboratory analysis. This work has been realized with the contribution of the Italian Ministry of Politiche Agricole Alimentari e Forestali, project n. 6A84.
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