ASSESSMENT AND MONITORING OF THE FISHERY RESOURCES AND THE ECOSYSTEMS IN THE STRAITS OF SICILY

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LIST OF SPECIES

Aristaeomorpha foliacea (Risso, 1827)

  SPECIES DESCRIPTION
  ECOLOGY
    Geographical distribution
    Habitats
    Migrations
  BIOLOGICAL INFORMATION
    Maximum size
    Spawning
    Length at first maturity
    Eggs, larvae and post-larvae
    Recruitment and nursery areas
    Sex ratio
    Length-weight relationships
    Maximum age and natural mortality
    Von Bertalanffy growth function (VBGF)
    Feeding behaviour
    Stock units
  EVALUATION AND EXPLOITATION
    Biomass indices from trawl surveys
    Strength of recruitment
    Stock assessment
    Fisheries
    Fishing zones and seasons
    Yield
    Fishing and discards
    Gears
    Legislation and management


Figure 1. Aristaeomorpha foliacea (from Fischer et al., 1987)

Class:  Malacostraca
Order:  Decapoda
Family:  Aristeidae
English name:  Giant red shrimp
   

SPECIES DESCRIPTION

Aristaeomorpha foliacea (giant red shrimp, Figure 1) was first described in the early nineteenth century by Risso in the Ligurian Sea. Together with Aristeus antennatus (blue and red shrimp) the two red shrimp are the only species of the family Aristeidae found in the Mediterranean. The systematic classification is: phylum Arthropoda, class Malacostraca, subclass Eumalacostraca, superorder Eucarida, order Decapoda, sub-order Dendrobranchiata, superfamily Penaeoidea (Perez Farfante and Kensley, 1997).

A. foliacea is a large-sized decapod crustacean with a scarlet red coloured, firm though flexible and light exoskeleton and black eyes. In mature females the dorsal part of the abdomen is darker due to the black colour of the mature ovaries. The pleon (abdomen) is slightly keeled along the dorsal midlines of the third segment, becoming pronounced on the following three segments and ending in a sharp posterior point (Bianchini, 1999). Other important morphological characteristics are long pleopods, a carapace with antennal, hepatic and branchiostegal spines, very short upper antennal flagella, strong posteromedian spines on the third to sixth abdominal segments, a telson with four small movable lateral spines, an open telicum and secondary sexual dimorphism with regards to body size and the length of the rostrum. Adult females are larger and have a longer rostrum, which extends far beyond the antennal scale. In males the rostrum is short and does not exceed the tip of the antennular peduncle. The rostrum has 6 to 12 upper teeth, including 2 teeth on the carapace (Fischer et al., 1987; Carpenter and Niem, 1998).

ECOLOGY

Geographical distribution – formatting of sections and subsections will be defined at a later stage
The giant red shrimp Aristaeomorpha foliacea has a wide geographic distribution. The species has been reported to occur in the Mediterranean, the Atlantic, the Indian Ocean, the western Pacific (Perez Farfante and Kensley, 1997) and South Africa (Bianchini, 1999). Historically red shrimp were found in the Mesozoic basin of Tethys, which extended from the Indian Ocean to the present day Caribbean Sea, including areas which became the Mediterranean Sea (Cau et al., 2002). In the Mediterranean Sea the distribution of giant red shrimp is patchy in nature, with the highest abundances found in the central-eastern basins (Politou et al., 2004).

In the Central Mediterranean there is a longitudinal segregation between the two species of red shrimp: A. antennatus decreases in abundance from the western to the eastern Mediterranean whilst the opposite is true for A. foliacea (Bianchini and Ragonese, 1994; Cau et al., 2002; D’Onghia et al., 1998; Company et al., 2004; Guillen, 2012). In Tunisian waters the relative abundance of the two species has been reported to be 50% A. foliacea and 50% A. antennatus at La Galite and 80% A. foliacea and 20% A. antennatus on the nearby Sentinelle Bank (Ben Meriem, 1994). In Spanish waters, the Gulf of Lions and the Ligurian Sea A. antennatus outnumbers individuals of A. foliacea (Cau et al., 2002); in the Central Mediterranean, eastern Ionian Sea and waters around Greece A. foliacea is dominant (Politou et al., 2004; Ragonese, 1995; Cau et al., 2002). A number of hypotheses have been proposed to explain this pattern, including differences in hydrological conditions (Ghidalia and Bourgeois, 1961; Orsi and Relini, 1985; Bianchini, 1999; Politou et al., 2004), differences in productivity between the Mediterranean basins (Politou et al., 2004) and different levels of fishing pressure being exerted across the Mediterranean; A. antennatus is more resilient to overfishing than A. foliacea (Matarese et al., 1997; D’Onghia et al., 2003; Politou et al., 2004).

Habitats
A. foliacea is a deep-water benthopelagic shrimp with a reported depth distribution of 120-1300 m, generally on muddy bottoms (Fischer et al., 1987). The species aggregates in submarine trenches and canyons along the continental slope (Ragonese et al., 1997; Bianchini, 1999) and peaks in abundance at 300-800 m depths (Ragonese et al., 1997 and references therein; Politou et al., 2004) (Figures 2-3). In the Sicilian Channel the species has been reported to have a marked preference for habitats between 500-700 m. More specifically, off the coast of Tunisia the depth distribution of A. foliacea increases gradually from the Sisters’ Rock located off Tabarka to the Skerki Channel (Ben Meriem, 1994) and the Pantelleria Channel, where it is only found consistently below 600 m depth (Bianchini, 1999).
Based on the bathymetry of the region, it is likely that giant red shrimp have two main distribution zones, one on the eastern side and one on the western side of the Sicilian Channel. The eastern pocket is in addition separated by the Pantelleria and Malta troughs, and the regional distribution of A. foliacea can, as a result, be divided into 3-4 areas of greater importance. The eastern and western sides of the channel are however connected by a narrow passage deep enough (200-400 m) to allow the migration of individuals (Bianchini, 1999).

Migrations
A. foliacea migrates nocturnally into the water column in the Strait of Sicily and as a result fishers using bottom trawl gear prefer to target the species in daylight (Bianchini et al., 1998; Bianchini, 1999). These daily vertical migrations of up to 200-300 m from the bottom (Maurin and Carries, 1968) are related to the feeding behaviour of this species, which feeds both on benthic and pelagic organisms (Rainer, 1992; Pipitone et al., 1994; Bello and Pipitone, 2002). Bianchini et al. (1998) reported a size-dependent difference in the diel behaviour of A. foliacea, with small-sized shrimp seeming to undergo more pronounced migrations into the water column during the night-time.
In addition to such diel migrations, evidence for season movements related to reproductive behaviour has been recorded. An increased abundance of males prior to the spawning season on the upper slope has been attributed to the movement of mature individuals from deep canyons in order to mate (D’Onghia et al., 1998; Belcari et al., 2003). Once spawning has taken place, males are once again displaced to deeper waters (Cau et al., 1987).

BIOLOGICAL DATA

Maximum size
The maximum body length of females according to FAO species identification guides is 225 mm (59 mm carapace length) and that of males 170 mm (45 mm carapace length). Females commonly measure 170-200 mm body length and males 130-140 mm (Fischer et al., 1987; Carpenter and Niem, 1998). For the Strait of Sicily a length range of 16-74 mm and a median carapace length of 36 mm has been reported (Cau et al., 2002; Ragonese et al., 2004).

Spawning
The young of the year recruiting in spring are immature, with only a few individuals reproducing during their first year. Gonadic development begins in winter and individuals become sexually mature in the second summer (Bianchini, 1999; Politou et al., 2004). Once they have reached maturity male giant red shrimp have a protracted reproductive capacity and are ready to mate throughout the year, whilst females mature seasonally (Bianchini, 1999; Perdichizzi et al., 2012). In the Strait of Sicily maturation of female A. foliacea and subsequent spawning occurs from spring until autumn, with a marked maturity peak in summer-autumn (Ragonese et al., 2004).
A. foliacea gather in shoals during the mating and spawning season (Bianchini, 1999), however only very limited information on the location of such spawning areas is available. Ragonese and Bianchini (1995) collected samples over a wide area of the Strait of Sicily and found mature females to be concentrated in the deeper waters between the Malta and Adventure banks and in particular to the west of the Maltese Islands (GSA 15). An analysis of 2003-2007 Maltese MEDITS data confirmed that the highest concentrations both by number and by weight of mature A. foliacea individuals was found to the North of Gozo at a depth of ~400-600 m and to the west of the Maltese Islands at a depth of 600-800 m (Knittweis and Dimech, 2009).

Figure 2. Occurrence of mature Aristaeomorpha foliacea females; light shading indicates the study area and dark shading the presence of ‘ready to spawn’ females (from Ragonese and Bianchini, 1995).

Figure 3. Normalised average density indices of mature giant red shrimp in GSA 15 (Knittweis and Dimech, 2009)

Length at first maturity
Giant red shrimp are dioecious animals and no systematic cases of hermaphroditism have been described. The colour, size and structure of the ovary is used to assess the maturity of female A. foliacea (Levi and Vacchi, 1988), whilst fused petasma, a shortened rostrum, and the presence of emi-spermatophores inside the terminal ampullae are the macroscopic features which distinguish a mature male individual (Bianchini, 1999).
Levi and Vacchi (1988) found the smallest female with ripe ovaries caught in the Strait of Sicily to measure 42 mm length. Bianchini (1999) reported males reaching maturity at 30-33 mm carapace length and undergoing the transition between a long and short rostrum in the 31-32 mm length range; females developed spermatophores in the 30 mm size class and all females larger than 40 mm carapace length had spermatophores. However, although spermatophores are present in all large females, the proportion of mature individuals in a given size class never reaches 100%, even during the reproductive periods (Bianchini, 1999). Ragonese et al. (2004) report a length at 50% maturity of 30-33 mm carapace length for males and of 42 mm for females. The most recent maturity ogive available was estimated by CNR-IAMC based on 2009 data, with a length at 50% maturity for females of 37.17 mm carapace length / a slope g of 0.541 and a length at 50% maturity of 27.41 mm carapace length / a slope g of 0.988 in males (STECF 11-14, 2011).

Eggs, larvae and post-larvae
Penaeoid shrimps do not brood fertilised eggs and instead release them directly into the sea (Bauer, 1991). Information on larval and postlarval stages is scarce and in particular distribution patterns remain almost completely unknown (Cau et al., 2002). It is likely that larvae develop as epipelagic plankton and that hydrological conditions affect recruitment and thus year class strength in giant red shrimp (Bianchini, 1999).
The only description of A. foliacea larval stages is given by Heldt (1955), who was able to identify several morphological characteristics which distinguish A. foliacea larvae from A. antennatus larvae: a projecting anterior part of the carapace and different relative antenna lengths at Protozoea stages II and III; longer uropods at the Protozoea stage III, absence of pterigistomian spines and a longer A2 endopodite compared to the exopodite and a different telson shape at the Mysis stage (Figure 4).

Figure 4. Larval stages of Aristaeomorpha foliacea (from Heldt, 1955)

Recruitment and nursery areas
The recruitment of juvenile A. foliacea in the Central Mediterranean takes place in spring (Ragonese et al., 2004) when individuals have reached a size of 25-31 mm carapace length (Garofalo et al., 2011; Figure 5).
Giant red shrimp recruits have been found dispersed widely at depths of 500-700 m in the Strait of Sicily: based on 1994-2004 south Sicily (Italy, GSA 16) MEDITS and GRUND data Garofalo et al. (2011) carried out a persistence analysis, which found A. foliacea recruits were only spatially structured in five years over the eleven year study period. The two stable nursery areas identified are located in the middle of the Strait and on average supported 30% of the total number of juveniles in the years studied.

Figure 5. Density map of Aristaeomorpha foliacea recruits, showing the location of two persistent nurseries (from Garofalo et al., 2011).

Based on an analysis of 2003-2007 MEDITS data collected in GSA 15, two areas with high densities of juvenile giant red shrimp located at a depth of ~600 m have, in addition, been identified (Figure 6). One area is located within the 25 nautical mile Maltese Fisheries Management Zone and the other right on the border of GSA 15 (Knittweis and Dimech, 2009). An updated, joint analysis of GSA 15 and GSA 16 data is needed in order to improve the available knowledge on the location of A. foliacea nursery areas.

Figure 6. Normalised average density indices of immature giant red shrimp in GSA 15 (Knittweis and Dimech, 2009).

Sex ratio
Giant red shrimp sex ratios can vary between areas, seasons and depending on the depth sampled (D’Onghia et al., 1998; Bianchini, 1999; Belcari et al., 2003). For the Mediterranean as a whole, females have been reported to be slightly more abundant than males (Cau et al., 2002; Belcari et al., 2003; Can and Aktas, 2005), although a dominance of males has been reported from Greek waters (Cau et al., 2002; Papaconstantinou and Kapiris, 2003; Politou et al., 2004). 
Based on data from eight seasonal trawl surveys carried out in 1985-1987 a sex ratio of 53% females was reported for giant red shrimp in the Strait of Sicily (Ragonese and Bianchini, 1995). An analysis of GRUND and MEDITS survey data collected in the Central Mediterranean in 1994-2002 revealed a proportion of giant red shrimp females in the whole population of 0.43-0.49 (Ragonese et al., 2004) and a later analysis of 1994-2004 GRUND and MEDITS survey data showed that sex ratios oscillated without any apparent pattern around the expected value of 0.5 during this period (Ragonese et al., 2012). A more recent estimate based on an analysis of Maltese 2009-2011 commercial fisheries monitoring data from GSA 15 gave an average overall catch (including both landings and discards) sex ratio of 0.46 (MRRA, unpublished data).
With regards to sex ratio by size, there is an almost complete separation of sexes for mature individuals, with females being more abundant in the large size classes and males being more abundant in the middle size classes (Bianchini, 1999; Politou et al., 2004; Ragonese et al., 2012; Figure 7).


Figure 7. Aristaeomorpha foliacea sex ratio by size class in the South of Sicily and the Maltese Islands; dotted and solid lines represent MEDITS and GRUND interpolated values respectively (from Ragonese et al., 2012).

Although no relationship between sex ratio and depth has been found for the Strait of Sicily (Bianchini, 1999; Ragonese et al., 2012), it has been hypothesised that males become more abundant with depth and that during the mating season males migrate from the deeper canyons to shallower depths (D’Onghia et al., 1998; Belcari et al., 2003).

Length-weight relationships
The available parameters of allometric length-weight relationships measured in the Central Mediterranean are reported in Table 1.

Table 1. Length-weight parameters of Aristaeomorpha foliacea in the Strait of Sicily (GSA 15 and GSA 16); model: W = a CLb.

Author GSA Period Data Type Sex a b

Ragonese et al., 1997

16 1985-87,1993 Commercial F 0.0013 2.64

Ragonese et al., 2004

16 1994-2002 Survey F 0.00176-0.0021 2.51-2.56

Ragonese et al., 2004

16 1994-2002 Survey M 0.00116-0.00135 2.65-2.56

MRRA, 2009

16 2006-2008 Survey M 0.00153 2.59

MRRA, 2009

16 2006/-2008 Survey F 0.00104 2.68

CNR-IAMC, 2009

16 / / F 0.0016 2.5884

CNR-IAMC, 2009

16 / / M 0.001 2.7456

Gancitano et al., 2009

16 / / F 0.0013 2.636

MRRA, 2012

15 2009-2011 Commercial M 0.00635 2.2129

MRRA, 2012

15 2009-2011 Commercial F 0.00146 2.6065

*In STECF EWG report 11-14 (2011)

Maximum age and natural mortality
Ragonese et al. (1994) used Bhattacharya’s method as implemented in the COMPLEAT ELEFAN package (Gayanilo et al., 1988; 1994), complemented with information on survey season and reproductive patterns to estimate a maximum age of 4 years for female and 5 years for male giant red shrimp.
Cau et al. (2002) calculated growth curves for females based on 1994-1999 MEDITS data using Modal class Progression Analysis (MPA) as implemented in the FAO FiSAT software, and estimated a maximum age of 5 years for individuals from the Strait of Sicily.
Based on age slicing using the LFDA routine with growth parameters estimated by CNR-IAMC (2009), the maximum estimated age in the exploited female A. foliacea standing stock during the period 2006-2009 estimated by STECF 11-14 (2011) was 6 years.
More recently, Ragonese et al. (2012) hypothesized that the longevity parameters for males estimated by classic length frequency distribution analysis may have been underestimated due to reduced growth and an aggregation of older individuals in the larger size classes after the onset of sexual maturity. Based on the Author’s analyses a higher maximum age of 7-10 years for adult male giant red shrimps in the Central Mediterranean was proposed.
Ragonese et al. (1994) analysed a two year time series of A. foliacea length frequency distributions from the Strait of Sicily and estimated an annual instantaneous natural mortality (M) of 0.4 for females. Although the authors stated that values for males are likely to be similar, no estimate was given for males. Other estimates of natural mortality over the species lifespan in the Central Mediterranean are 0.5 for females (Bianchini, 1999), 0.4 for females (Ragonese et al., 2004) and 0.4-0.6 for males (Ragonese et al., 2012). 
Natural mortality rates by age were calculated according to the ProdBiom model developed by Abella et al. (1997) by STECF 11-14 (2011) as reported in Table 2.

Table 2. Natural mortality at age for Aristaeomorpha foliacea in GSA 15 and 16 as estimated by STECF 11-14 (2011).

Age

0 1 2 3 4 5+

Natural mortality at age

0.62 0.30 0.23 0.19 0.17 0.16

Von Bertalanffy growth function (VBGF)
Von Bertalanffy growth parameters estimated to date for the Strait of Sicily are reported in Table 3 for comparative purposes.

Table 3. Von Bertalanffy growth function estimated for the Strait of Sicily (GSA 15 and 16); L∞, k and t0 refer to the asymptotic carapace length (CL; mm), the curvature coefficient (year-1) and the theoretical age at size 0.

Author Sex L∞ K T0 Remarks

Ragonese et al., 1994

F 65.5 0.67 0.28  

Ragonese et al., 1994

M 41.5 0.96 0.28  

Bianchini, 1999

M 40-41 1.08 /  

Cau et al., 2002

F 65.5 0.67 /  

Bianchini and Ragonese, 2002

F 60-61 0.63-0.66 /  

Ragonese et al., 2004

F 65.8 0.52 -0.23  

AAVV 2008, Red's Project

F 62.24 0.65 0.05  

AAVV 2008, Red's Project

M 40.31 0.79 -0.44  

CNR-IAMC, 2009

F 61.66 0.78 -0.22  

CNR-IAMC, 2009

M 41.95 0.7 -0.18  

SGMED, 02/09/2009

F 68.9 0.61 -0.2  

Ragonese et al., 2012

M 41.9 1.40/0.56 0.2/-0.99 Double phase VBGF: coefficients before / after transitional age

Feeding behaviour
Giant red shrimp are opportunistic carnivores and scavengers (Bianchini, 1999). The first study on the feeding behaviour of A. foliacea found a high diversity in consumed prey types, including pelagic, benthic and benthopelagic organisms in the Ligurian Sea (Brian, 1931). This pattern was later confirmed for the Central Mediterranean: stomach content analysis of giant red shrimp found both strictly benthic and pelagic prey (Bello and Pipitone, 2002). The most widely accepted explanation is that A. foliacea undergoes diel migrations related to its feeding behaviour, feeding on benthic organisms during the day and preying in the water column at night (Bianchini, 1999; Rainer, 1992; Bello and Pipitone, 2002). 
The most important food sources of giant red shrimp in the Strait of Sicily are crustaceans (49%), bony fish (21%), cephalopods (9%), siphonophores (5%), gastropods (5%), bivalves (3%), polychaetes (1%), unidentified prey (7%) and foraminiferans (Bello and Pipitone, 2002). The precise dietary importance of the latter is difficult to estimate because foraminiferans may be unintentionally ingested when feeding on benthic prey (Rainer, 1992; Cartes, 1995). Common benthopelagic decapods ingested by A. foliacea in the Strait of Sicily are Plesionika and Pasiphaea spp., in particular Pasiphaea sivado (Bianchini, 1999). Cephalopods have a higher relative importance in the diet of A. foliacea compared to giant red shrimp from other areas and as a result it is likely that A. foliacea contributes significantly to the mortality of juvenile cephalopods of species such as Heteroteuthis dispar in Central Mediterranean food webs (Bello and Pipitone, 2002).
Diet composition is size related in A. foliacea. Significant differences were found with regards to the number of cephalopods eaten by small compared to large-sized giant red shrimp in the Strait of Sicily, only medium and large shrimp were able to prey on larger cephalopods (Bello and Pipitone, 2002). Bianchini (1999) found that larger individuals consumed more cephalopods, shrimps and siphonophores, while small specimens consumed a larger proportion of benthic mollusks and foraminifera. In the Greek Ionian Sea a similar positive trend of ingesting larger prey with increased size has been observed for female giant red shrimp, whilst immature individuals have a higher occurrence of epibenthic prey in their foreguts (Kapiris, 2012). Large shrimp are likely to be more efficient predators because of their increased swimming ability and larger mandibles.
In addition to the influence of somatic growth on feeding habits, giant red shrimp change their feeding behaviour seasonally. In the Strait of Sicily there are seasonal differences in prey type, with siphonophores of the family Diphyidae consumed mainly in spring and benthic gastropods an important food source in autumn (Bianchini, 1999). In the Greek Ionian Sea giant red shrimp have an increased feeding activity in spring-summer, which is likely related to the increased reproductive activity in this season (Kapris, 2012). In winter A. foliacea has the highest stomach fullness, but the ingested food has a lower quality (Bianchini, 1999; Kapiris, 2012).

Stock units
Despite the commercial importance of A. foliacea, only very little information is available on population structure, larval mixing and migration patterns. Based on the bathymetry of the Strait of Sicily, Bianchini (1999) hypothesized that giant red shrimp in the Strait of Sicily have two main distribution zones, one on the eastern side and one on the western side of the Sicilian Channel, connected with a passage to allow for the movement of individuals. However, Marcias et al. (2010) carried out a study on the genetic connectivity between giant red shrimp populations from Sardinia and the Strait of Sicily and found no significant genetic variability between the populations sampled. The Authors thus concluded that A. foliacea in the western and central Mediterranean forms one large panmictic stock.

EVALUATION AND EXPLOITATION

Biomass indices from trawl surveys
Fishery independent information regarding the state of the giant red shrimp stock in GSAs 15 and 16 can be derived from the international bottom trawl survey MEDITS, which has been carried out in GSA 16 since 1994 and in GSA 15 since 2002 (Figures 8 and 9). Information presented by STECF 11-14 (2011) shows that patterns recorded in GSA 15 and GSA 16 in 2002- 2010 mirrored one another. The stock declined slightly in 2004-2007, before increasing in 2008 and peaking in 2009. In 2010 the population returned to levels similar to those recorded in 2005-2007. Similar peaks in abundance had previously occurred in 2000 and 2004. The highest number of A. foliacea caught per hour in 1994-2010 was 81.3 individuals in GSA 15 in 2004; the lowest number caught per hour 1994-2010 was 1.79 in GSA 15 in 2009. The lowest biomass of A. foliacea caught per hour in 1994-2010 was 0.36 kg/hour in GSA 16 in 1997; the highest biomass caught per hour 1994-2010 was 1.79 kg/hour in GSA 15 in 2009.

Figure 8. Abundance indices of Aristaeomorpha foliacea for the years 2002-2010 in GSA 15 (left) and 1994-2010 in GSA 16 (right).

 

Figure 9. Biomass indices of Aristaeomorpha foliacea for the years 2002-2010 in GSA 15 (left) and 1994-2010 in GSA 16 (right).

Strength of recruitment
Based on a SURBA analysis (Needle, 2003) of GSA 16 MEDITS survey data for female giant red shrimp, STECF 11-14 (2011) concluded that in 1994-2001 both spawning stock biomass (SSB) and recruitment fluctuated significantly. SSB remained at low but stable levels in 2002-2010 (Figure 10). Recruitment fluctuated at low levels in 2002-2010; a low number of recruits were recorded in 2001, 2006 and 2010. Absolute estimates of female recruitment were in the range of 83 (2008) to 123 million recruits based on an analysis of GSA 15 and GSA 16 commercial data (STECF 11-14, 2011).

Figure 10. Female spawning stock biomass (SSB) in kg/km2 and recruits in n/km2 as a median of SURBA bootstrapped values (from STECF 11-14, 2011).

Stock assessment
The most recent stock assessment available for A. foliacea in the Strait of Sicily was done in 2011 by the STECF 11-14. Only the state of exploitation of the female component of the giant red shrimp stock was assessed. The assessment was presented to the GFCM Sub-Committee for Stock Assessments (SCSA) in 2011 and subsequently endorsed by the GFCM Scientific Advisory Council (SAC) in 2012.
Five complete years of length frequency distributions from Sicilian commercial data (2006-2010) and two years of length frequency distributions sampled onboard Maltese trawlers (2009, 2010) were analysed. The assessment was based on pseudo-cohort assumptions, keeping separate the available years. Cohort (VPA equation) and yield per recruit analysis as implemented in the VIT package (Lleonart and Salat, 1997) were carried out as well as a simulation of the likely variation in yield, biomass and spawning stock biomass per recruit as a function of varying fishing mortality with the Yield package (Branch et al., 2001). A probability estimation of limit and target biological reference points was also carried out using the Yield package. 
Total yields reconstructed by the VIT package for the study period were very close to the actual, observed yields. Other results such as absolute estimates of recruitment, current total mortality rates and fishing mortality rates are listed in Table 4.

Table 4. Overview of main results of VIT analysis based on the female fraction of the Aristaeomorpha foliacea population in the Strait of Sicily.

Year 2006 2007 2008 2009 2010 Median

Total Yield (t)
Estimated SSB (t)
Recruitment (ml)
Mean Z (all ages)
Mean F (all ages)
Mean F (ages 1-4)

1450
1070
98
1.22
0.92
1.14
1574
1370
114
1.00
0.74
1.07
1287
1300
83
0.96
0.7
1.05
1659
1580
118
0.83
0.57
0.81
1684
1260
122
0.99
0.73
1.09
1574
1370
114
0.99
0.73
1.07

The results of estimating spawning stock biomass per recruit (SSB/R) and yield per recruit (Y/R), by varying current fishing mortality (Fc) through a multiplicative factor for 2006- 2010 catches as calculated by the VIT package are reported in Figure 11.


Figure 11. Spawning stock biomass and yield per recruit under varying current fishing mortality (Fc) scenarios for Aristaeomorpha foliacea harvested in the Strait of Sicily according to the VIT package.

The results of the yield per recruit analysis with regards to current levels of fishing mortality (F) as well as target (F0.1) and limit (Fmax) reference points are given in Table 5. The results of estimating spawning stock biomass per recruit (SSB/R) and yield per recruit (Y/R) according to the Yield package are illustrated in Figure 12.

Table 5. Yield (Y), biomass (B), spawning stock biomass (SSB) per recruit (R) varying fishing mortality (F) by a multiplicative factor; Y, B and SSB are given in g per R.

Year Parameter Factor F Y/R B/R SSB

2006

F(0)
F(0.1)
Fmax
Fc
0.00
0.44
0.71
1.00
0.00
0.36
0.81
1.14
0.00
14.41
15.15
14.77
74.97
31.03
22.45
17.36
68.11
24.68
16.35
11.51
2007 F(0)
F(0.1)
Fmax
Fc
0.00
0.38
0.59
1.01
0.00
0.41
0.63
1.07
0.00
13.82
14.50
13.50
107.51
40.97
28.67
17.21
100.68
34.85
22.87
12.01
2008 F(0)
F(0.1)
Fmax
Fc
0.00
0.42
0.70
1.01
0.00
0.44
0.74
1.05
0.00
14.72
15.59
15.17
107.51
44.35
30.50
22.37
100.68
37.98
24.39
16.51
2009 F(0)
F(0.1)
Fmax
Fc
0.00
0.49
0.76
1.01
0.00
0.40
0.61
0.81
0.00
13.30
13.96
13.69
107.51
38.17
25.49
18.84
100.68
32.11
19.75
13.36
2010 F(0)
F(0.1)
Fmax
Fc
0.00
0.39
0.60
1.01
0.00
0.42
0.65
1.09
0.00
13.73
14.36
13.51
107.51
38.06
26.15
15.62
100.68
31.94
20.33
10.31

Figure 12. Median of yield and spawning stock biomass per recruit as well as the corresponding uncertainty limits for Aristaeomorpha foliacea in the Strait of Sicily as estimated by the Yield package.

The simulation of biological reference points (BRP) with 2000 repeats gave the Fmax and F0.1 probability distributions shown in Figure 13; the median value of F0.1 was 0.4 and the median value of Fmax was 0.75. The F0.1 estimate is thus the same as that estimated by VIT, whilst the Fmax estimate is slightly higher.

Figure 13. Probability distribution of Fmax and F0.1 according to the Yield package.

Based on this information STECF 11-14 (2011) and GFCM SAC (2012) proposed FMSY=0.4 (F0.1 basis) as management reference point of the female part of the A. foliacea stock, and concluded that the stock in the Strait of Sicily is considered to be subject to overfishing since the current fishing mortality (Fc=1 in 2010) exceeds this reference point. Indeed, the median current F in 2006-2010 was 0.73, and thus higher than both Fmax (median in 2006-2010 = 0.73) and F0.1 (median in 2006-2010 = 0.41) during the study period.
GFCM SAC recommended a reduction in fishing mortality. STECF similarly advised to continuously reduce current fishing mortality through consistent effort reductions and an improvement in current exploitation patterns. STECF further advised the relevant fisheries’ effort to be reduced until fishing mortality is below or at the proposed reference level, in order to avoid future loss in stock productivity and landings, and suggested this should be achieved by means of a multi-annual management plan taking into account mixed-fisheries effects (STECF 12-19, 2012).

Fisheries
A. foliacea is an important target species for bottom otter trawlers operating on the continental slope in the Strait of Sicily. Although no specific information on Italian vessels targeting red shrimp fisheries is available, the number of trawlers larger than 24 m LOA can be considered as an overestimated proxy of vessel that potentially can catch red shrimps. In 2011, 140 Italian trawlers measuring over 24m in length carrying out longer fishing trips (up to 4 weeks) were active in both the Italian and the international waters of the Central and Eastern Mediterranean. The Tunisian fleet was composed of 75 trawlers measuring over 24 m, which targeted deep water crustaceans primarily in Northern Tunisia. The great majority of Tunisian catches are landed in the towns Bizerte and Kelibia. In the Maltese Islands 14 trawlers measuring 12-24 m and 8 measuring over 24 m in length were active in 2011, 11 of which had a license to operate within the 25 nm Maltese Fisheries Management Zone (Ben Meriem et al., 2012a; 2012b). The contribute of Libyan trawlers to red shrimp catches can be considered negligible.
With regards to fishing effort, data submitted by Italy and Malta in response to the annual EU fisheries Data Collection Framework (DCF) data-call in 2012 revealed a 32% decrease in fishing effort for Italian bottom otter trawl vessels larger than 24 m in the period 2004-2011 (Figure 14). Maltese vessels were only responsible for 1.6% of total trawling effort in GSAs 15 and 16 in 2006-2011, however the total nominal effort of Maltese trawlers increased by 67% in 2006-2011 (STECF 12-19, 2012).

Figure 14. Nominal effort (kW*days at sea) trends for trawlers (OTB) by Italian (left y-axis) and Maltese (right y-axis) fleet segments (from STECF 12-19, 2012).

Although the deep water bottom otter trawling in the Mediterranean is a multispecies fishery, red shrimps represent the most abundant and highest value fraction of catches. Based on 102 daylight hauls Bianchini (1999) found the mean catch by weight of the A. foliacea fishery to be composed of: 49% giant red shrimp, 1% blue and red shrimp, 26% bony fish, 16% cartilaginous fish, 7% other crustaceans. Other commercial species frequently caught together with giant red shrimp are the deep water rose shrimp (Parapenaeus longirostris), Norway lobster (Nephrops norvegicus), blue and red shrimp (Aristeus antennatus), greater forkbeard (Phycis blennoides), hake (Merluccius merluccius), rockfish (Helicolenus dactylopterus), black-bellied anglerfish (Lophius budegassa), four spotted megrim (Lepidorhombus boscii), blue whiting (Micromesistius poutassou) and several species of squid (Illex spp., Todarodes sagittatus, Todaropsis eblanae). In terms of the absolute number of marketable individuals caught, deep water rose shrimp and Norway lobster, together with giant red shrimp, make up the bulk of catches (Bianchini, 1999; Knittweis, pers. observation).

Fishing zones and seasons
In order to estimate variations in crustacean catch compositions in the Strait of Sicily Vitale et al. (2006) divided the Central Mediterranean into seven sub-areas based on the morphology of the single areas, hydrological features as well as feedback from fishers with regards to target areas for different species (Figure 15). In spring 2001 estimates of catches (i.e. landings and discards) were made for P. longirostris, N. norvegicus and A. foliacea in each sub-area. Based on three day and three night hauls, made by the employed commercial crews at random locations in each area, the Authors recorded the following total catch for giant red shrimp in decreasing order of importance: area 7 = 50 t, area 4 = 33 t, area 3 = 18 t, areas 1 and 4 = 8 t, areas 6 and 2 = 1 t, area 5 = no catches.

Figure 15. Areas surveyed by Vitale et al. (2006) to estimate catch composition of decapod crustaceans from trawl fishery catches in the Central Mediterranean.

Bonnet (1980) carried out a survey of demersal fishery resources along the Tunisian coast, and found A. foliacea to be dominant in hauls at depths of ~500 m taken off the coast of Tabarka, in the north of Tunisia. More recently, Missaoui (2004) list giant red shrimp as one of about twenty commercial crustacean target species caught in Tunisian fisheries, stating that A. foliacea is concentrated on the northern side of Tunisia.
In Maltese waters, trawlers target giant red shrimp within the 25 nm trawl fisheries management zone to the north-west of the Island of Gozo and south-west of Malta, at depths of 600-700 m (Dimech et al., 2012)(Figure 16).

Figure 16. Trawl lanes within the Maltese 25 nautical mile Fisheries Management Zone (after Dimech et al., 2012).

Information on the location of fishing zones targeted by the Sicilian trawl fleets is available from Ragonese (1995) as well as Bianchini et al. (2003), who give an outline of the most important A. foliacea target areas in the Strait of Sicily (Figure 17).
Due to a reduction in catch rates since 2004, some distant trawlers based in Mazara del Vallo, which is the main fleet in the area, moved to the eastern Mediterranean (Aegean and Levant Sea) to fish red shrimps (Garofalo et al., 2007).
Italian and Maltese trawlers catch A. foliacea on the continental slope of the Strait of Sicily throughout the year; a slight decrease in total landings during the first quarter of the calendar year (January-April) is generally followed by a peak in landings in the second quarter (May-August) (STECF 11-14, 2011).

Figure 17. Main fishing grounds of Aristaeomorpha foliacea targeted by Sicilian fishers; (A) after Ragonese (1995), (B) after Bianchini et al. (2003).

Yield
No information is available on total yield of A. foliacea from Tunisian trawlers. As Missaoui (2004) pointed out, sampling is difficult for several crustacean species in Tunisia, including A. foliacea. Part of the reason for this is that giant red shrimp are generally landed frozen since the species is primarily destined for export markets (Mosbah et al., 2012; Ben Meriem, pers. communication). Yield of both the Italian and Maltese trawlers reached the highest values of the period 2004-2009 in 2009, with 1620 t and 42 t respectively (Figure 18).
The most abundant size classes in 2006-2009 catches by Sicilian trawlers were 42-50 mm carapace length (Figure 19). Giant red shrimp caught by Maltese trawlers in 2009 and 2010 were generally smaller, with the most abundant size classes measuring 32-34 mm carapace length (STECF 11-14, 2011) (Figure 20).

Figure 18. Bottom otter trawl fleet landings (t) by year in 2004-2009 as reported through the EU fisheries Data Collection Regulation (based on STECF data 11-14, 2011).

Figure 19. Annual length structure of giant red shrimp landed (absolute numbers) by Sicilian trawlers fishing in the Strait of Sicily (from STECF 11-14, 2011)

Figure 20. Annual length structure of giant red shrimp landed (absolute numbers) by Maltese trawlers fishing in the Strait of Sicily (from STECF 11-14, 2011).

Fishing and discards
Mediterranean bottom otter trawling is a multi-species fishery which discards both undersized commercial species and unwanted species with no commercial value. It has been estimated that over 560 000 t of unwanted species are discarded in the Mediterranean every year, although the composition of discards varies depending on seasons, depth, gear characteristics, haul duration and the location of the fishing ground (Alverson et al., 1994). More recently a lower estimate of discards produced by fisheries in the Mediterranean, was given by Tsagarakis et al. (2103). Discard is around 230 000 t, corresponding to 18.6% (13.3–26.8%) of the catch.
Altough Castriota et al. (2001) reported a mean discard rate in shrimp fisheries of 49% of catch in the Strait of Sicily, the overall amount of discards generated by red shrimp fisheries is generally low (Ragonese et al., 2001; STECF 11-14, 2011) as a significant fraction of the by-catch is made up of economically important species (Bianchini, 1999). However long-haul fishing vessels aiming to maximize profits have been reported to discard practically all non-crustacean catches (Bianchini, 1999; Castriota et al., 2001).
Discarding of undersized juvenile commercial species is also an important concern (Vitale et al., 2006) (Figure 21). An analysis of discards data collected onboard Maltese trawlers in 2009 and 2010 revealed that the Maltese fleet discarded an estimated 1.3 t of A. foliacea in 2009 and 0.2 t in 2010 (STECF 11-14, 2011). On average the ratio of discards to landings for Maltese trawlers in 2009 and 2010 was 2%; the majority of discarded individuals were too small to be of commercial value, whilst some larger specimens were crushed during fishing and too damaged to be sold. The decrease in discards in 2010 is likely to be due to the general drop in giant red shrimp landings in 2010 as well as the introduction of larger mesh sizes on Maltese trawlers in line with the Mediterranean Regulation (EC 1967/2006) (STECF 11-14, 2011).


Figure 21. Annual length structure of Aristaeomorpha foliacea discards in absolute numbers by Maltese trawlers fishing in the Strait of Sicily.

A number of discarded species with no commercial value are caught as by-catch in the giant red shrimp fishery. They include several species of grenadier (Hymenocephalus italicus, Nezumia sclerorhynchus, Coelorhynchus coelorhynchus), argentines (Argentina sphyraena, Glossanodon leioglossus), shortnose greeneye (Chlorophthalmus agassizi) and several species of cartilaginous fish: blackmouth catshark (Galeus melastomus), small-spotted catshark (Scyliorhinus canicula), velvet belly lanternshark (Etmopterus spinax), thornback ray (Raja clavata), longnosed skate (Dipturus oxyrinchus) and rabbit fish (Chimaera monstrosa) (L. Knittweis, pers. observation).
Regarding invertebrates and overall benthic communities, the gorgonian Isidella elongata is generally caught by trawlers targeting red shrimps. In the Mediterranean Isidella elongata characterises bathyal compact mud biocenoses between 500 and 1200 m depth (Peres, 1967), providing a habitat for a multitude of fish and invertebrates. I. elongata is removed during bottom trawling activities and, as a result, is becoming increasingly rare. Destroying coral communities is likely to have a long term negative impact on the bottom otter trawling industry by reducing species richness, abundance and biomass of commercial species (Maynou and Cartes, 2011).

Gears
Up to recent years Italian and Maltese trawlers targeting giant red shrimp in the Strait of Sicily used a type of bottom otter trawl net known as a ‘fondale’ net. In shallower waters a different net referred to as a ‘banco’ net is used. Banco nets have a shorter extension piece, larger cod end mesh sizes and smaller extension piece mesh sizes compared to fondale nets. Both nets were characterized by a low vertical opening of only up to 1.5 m, although dimensions change with the engine power of individual vessels (Fiorentino et al., 2003) (Table 6).
A detailed study of the functions between otter door spread, horizontal and vertical net opening as well as warp length on fishing vessels with differing engine strengths the performance of demersal fishing gears used in Italy was carried out by Fiorentini et al. (1994). In the last years some changes in the structure of the mazarese net were introduced. They were aimed at reducing the weight and increase the vertical opening during trawling.

Table 6. Main characteristics of traditional Sicilian trawl nets based on a study carried out using a reference trawler of 375-450 kW engine (Fiorentino et al., 2003 in MedSudMed, 2008).

Net Characteristics

Banco net

Fondale net

Length of codend
Length of extension piece
Lastridge rope
Circumference of codend
Circumference of extension piece

5 - 6 m
20 - 21 m
Absent
400-500 mesh * 40-36 mm
900-1000 mesh * 44-40 mm

5 - 6 m
23 - 25 m
Absent
600-600 mesh * 28-26 mm
400 mesh * 50-52 mm

Legislation and management
At present there are no formal management objectives for giant red shrimp fisheries in the Strait of Sicily. As in other areas of the Mediterranean, the stock management in Tunisia, Italy and Malta is based on control of fishing capacity (licenses), fishing effort (fishing activity), technical measures (mesh size and area/season closures) (Jarboui, 2009; STECF 12-19, 2012).
In Tunisia law 94-13, issued on the 31st January 1994 as well as an order of the Ministry of Agriculture issued on the 28th September 1995 regulate marine fishing activities (Jarboui, 2009). In Malta and Italy both national legislation and EU legislation apply; key pieces of EU legislation are the recently reformed Common Fisheries Policy (EC 1380/2013), the Fisheries Data Collection Framework (DCF) (EC 199/2008, EC 665/2008, EC 93/2010), the Mediterranean Regulation (EC 1967/2006) and the Control Regulation (EC 1224/2009, EC 404/2011).
In order to limit the over-capacity of the fishing fleet, no new fishing licenses have been assigned in Italy since 1989 and a progressive reduction of the trawl fleet capacity is currently underway. Maltese fishing capacity licenses had been fixed at a total of 16 trawlers since 2000, but eight new licenses were issued in 2008 and one in 2011, a move made possible by capacity reductions in other segments of the Maltese fishing fleet (STECF 12-19, 2012). In order to control fishing effort, Tunisia also restricts the number of fishing licenses (Jarboui, 2009); the number of Tunisian trawlers has increased from 70 in 2009 (GFCM SCSA, 2010) to 75 in 2011 (GFCM SCSA, 2012).
A compulsory 30-day fishing ban in August-September was recently adopted by Sicilian Government (STECF 12-19, 2012). In Tunisia closed seasons were established for the first time in 2009 for the Gulf of Gabès (south Tunisia, GSA 14). The ‘biological rest period’ (Repos Biologique) is in July, August and September each year. Although A. foliacea does not benefit directly from this measure since it is not fished in the Gulf of Gabes, this new regulation may in future be extended to other areas if stocks are found to be overexploited and in need of protection (Jarboui, 2009).
There is no closed season in place in Malta, but the Maltese Islands are surrounded by a 25 nautical mile fisheries management zone, in which fishing effort and capacity are being managed by limiting vessel sizes, as well as total vessel engine powers (EC 813/04; EC 1967/06). Trawling is allowed within this designated conservation area, however only by vessels not exceeding an overall length of 24 m and only within designated areas. Vessels fishing in the management zone hold a special fishing permit in accordance with Regulation EC 1627/94. Moreover, the overall capacity of the trawlers allowed to fish in the 25nm zone can not exceed 4 800 kW, and the total fishing effort of all vessels is not allowed to exceed an overall engine power and tonnage of 83 000 kW and 4 035 GT respectively. The fishing capacity of any single vessel with a license to operate at less than 200m depth cannot exceed 185 kW.
In order to protect coastal habitats, the use of towed gears is prohibited within 3 nm of the coast or within the 50 m isobath if the latter is closer to the coast (EC 1967/2006; Res. GFCM 36/2012/3). In order to protect deep water habitats, trawling at depths beyond 1000 m is also prohibited at EU and GFCM level (EC 1967/2006; Rec. GFCM 2005/1).
In terms of technical measures, EC 1967/2006 fixed a minimum mesh size of 40 mm (opening) for bottom trawling by EU fishing vessels. In July 2008 the mesh size had to be modified to square 40 mm mesh or, if duly justified by the vessel owner, a 50 mm diamond mesh; derogations were only possible up to 2010. Moreover, diamond mesh panels can only be used if it is demonstrated that size selectivity is equivalent to or higher than using 40 mm square mesh panels (EC 1343/2011). In Tunisia benthic trawlers targeting demersal species have a minimum diamond mesh size of 20 mm side, corresponding to 40 mm opening (Jarboui, 2009). There is at present no minimum landings size for A. foliacea in European or Tunisian legislation.

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