Temporal dynamics of demersal chondrichthyan species in the central western Mediterranean Sea: The case study in Sardinia Island

Fisheries Research 193 (2017) 81–94

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Temporal dynamics of demersal chondrichthyan species in the central western Mediterranean Sea: The case study in Sardinia Island

MARK

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Martina F. Marongiua, , Cristina Porcua, Andrea Bellodia, Rita Cannasa, Alessandro Caua,b, Danila Cuccua, Antonello Mulasa, Maria C. Follesaa a b

Department of Life and Environmental Sciences, University of Cagliari, Via T. Fiorelli 1, 09126 Cagliari, Italy Department of Architecture, Design and Urban Development University of Sassari, Palazzo Pou Salit, Piazza Duomo 6, 07041 Alghero, Italy

A R T I C L E I N F O

A B S T R A C T

Handled by George A. Rose

Occurrence, abundance and size trends of 25 demersal Chondrichthyes (10 Sharks: 3 Carcharhiniformes, 2 Hexanchiformes, 5 Squaliformes; 14 Batoids: 3 Myliobatiformes, 8 Rajiformes, 3 Torpediniformes and 1 Holocephalan: 1 Chimaeriformes) collected from 22 years (1994–2015) of Mediterranean International Trawl Surveys (MEDITS) around Sardinian seas, were given. Data relative to two strata, the continental shelf (10–200 m), the slope (201–800 m), and the overall (10–800 m), were analyzed in order to identify the general species distribution of their habitat preference. From the gathered data it appeared that the shelf was mostly inhabited by batoids while the slope by sharks. Only the small-spotted catshark Scyliorhinus canicula and the thornback skate Raja clavata were equally distributed with high values of occurrence and abundance both in the shelf and in the slope. All the other species showed a preferential distribution only in one stratum (shelf or slope). In general, temporal trends of abundance indexes were stable or increasing in all strata. GAM analysis also confirmed a stable trend. Almost all species displayed stable in size structure analysis, apart from R. brachyura and Dipturus oxyrinchus that showed a statistically increasing trend. Although the investigated chondrichthyan species seemed to display a not alarming status of conservation in Sardinian seas, more investigation should be done to assure a proper management of this threatened resource.

Keywords: Chondrichthyes Temporal trends Trawl surveys central western Mediterranean

1. Introduction The rapid expansion of fisheries and globalized trade are emerging as the principal drivers of coastal and ocean threat (McClenachan et al., 2012). Overfishing and habitat degradation have profoundly altered marine animal populations (Polidoro et al., 2012), especially sharks and rays (Ferretti et al., 2010). Chondrichthyes appear to be particularly vulnerable to overexploitation because of their K-selected life-history strategy (e.g., slow growth, late attainment of sexual maturity, long life spans, low fecundity) (Stevens et al., 2000). Moreover, most of chondrichthyan landings are by-catch from fisheries targeting other species, or are registered in countries without adequate fisheries information-gathering systems with a resulting un-recording of the catches (Stevens et al., 2000). Despite their important role as predators at the top of the food chain in marine ecosystems and the dramatic declines in abundance reported from many parts of the world’s seas (Ward-Paige et al., 2012), data on their stock status remains still poor or non-existent (Polidoro et al., 2008; Worm et al., 2013). Chondrichthyan fisheries have expanded globally in response to the

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Corresponding author. E-mail address: [email protected] (M.F. Marongiu).

http://dx.doi.org/10.1016/j.fishres.2017.04.001 Received 4 August 2016; Received in revised form 28 March 2017; Accepted 4 April 2017 0165-7836/ © 2017 Elsevier B.V. All rights reserved.

growing demand (particularly for valuable parts such as shark fins), expanding the fishing effort to new areas (i.e., open ocean, deep-sea bottom), and involving more technically equipped fishing vessels (Casey and Myers, 1998; Clarke et al., 2007; Polidoro et al., 2008; Worm et al., 2013). These developments, together with the decline in several elasmobranch stocks, have led to a call towards a specific improvement in international actions for the Chondrichthyes management, in order to ensure sustainable fisheries (FAO, 2000; Lucifora et al., 2011; Bradai et al., 2012). The Mediterranean Sea represents a hotspot of marine biodiversity exposed to multiple threats, including fishing pressure, habitat loss and degradation, pollution, eutrophication and, more recently, climate change and invasion by alien species (Coll et al., 2010). More than half of chondrichthyan species assessed by the IUCN in this basin (39 of 73 species) are threatened. 31 are most imperiled: among these species 20 are classified as Critically Endangered and 11 as Endangered. The level of threat may be worse because uncertainty in species status remains moderately high in the Mediterranean Sea; of the 73 assessed species, 13 remain Data Deficient. (Dulvy et al., 2016). At least, half of

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where the number of hauls is proportional to the area of each stratum. The duration of hauls is fixed at 30 min on shallower depths than 200 m and 60 min for deeper sites. All specimens were counted, weighted (grams), and measured as total length (TL, in cm) (MEDITS Handbook, 2016). The total frequency of occurrence (f% = N positive hauls/total hauls *100) and also the Abundance Indexes (Biomass Index BI, kg/km2 and the Density Index DI, N/km2) were calculated for each taxonomic order and by each species considering the continental shelf (10–200 m), the slope (201–800 m), and the overall (10–800 m) depth strata for all the entire examined period. The existence of monothonic temporal trend in abundance was investigated by the Spearman correlation test (Zar, 1999). Due to the taxonomic misclassification issues dealing with the longnose spurdog Squalus blainville, data on frequencies and Abundance Indexes were calculated starting from 2005 when specific morphologic analysis of this species was conducted. Temporal trends of the Abundance Indexes were also tested by means of General Additive Modelling (GAM). The modelling routines were performed with R software, ‘mgcv’ package (Wood, 2000). The aim was to test for significant variations in the relation of the response variable (i.e., density and biomass) with depth (included as a smoother term), over the 22 years of investigation. The swept area was included as offset, a measure of the effort for which we could standardize the recorded indexes of abundance and biomass. Since data exploration revealed outliers in most density and biomass datasets (i.e., N of individuals and total weight per trawl), Log-transformation was performed prior to analysis. Model selection was accomplished using the lowest Akaike Information Criterion (AIC; Akaike, 1974) value and model validation was carried out by visual examination of plots of the normalized residuals versus the fitted values from each of the models. Models were ran for the total abundance and biomass of: i) the entire amount of Chondrichthyes; ii) the two major Chondrichthyes groups (i.e., Batoids and Sharks) and iii) the most abundant species of Sharks and Batoids (G. melastomus, R. clavata, R. miraletus and S. canicula) in Sardinian seas. All metrics were modelled using the Gaussian distribution with an identity link function. According to the MEDITS protocol, the TL has been taken since 1994 only for R. clavata and S. canicula; the other species became targets in the following years (G. melastomus from 1999; the other batoids and sharks starting from 2005). Temporal trends in size were calculated considering the overall depth stratum. Statistical analysis of the temporal size trends were tested with the Spearman test (Zar, 1999). The Kolmogorov-Smirnov (KS) two-sampled test was used to test for significant differences in the size composition of those species that were distributed in both bathymetric strata (shelf and slope).

the batoids (50%, 16 of 32 species) in the Mediterranean Sea faces an elevated risk of extinction, as well as 54% of sharks (22 of 41), whereas the only chimaerid species (Chimaera monstrosa) is considered Least Concern (Dulvy et al., 2016). Italy is characterized by a strong multispecies fishery, which does not allow to correctly define the state of exploitation of single or groups of stocks (Cataudella and Spagnolo, 2011). In addition, strategies based on management plans, according to fishery area and fishing system for cartilaginous fish have not been adopted yet. Although artisanal fisheries are prevalent in Sardinia, large trawlers operating in areas far from the coast, represent a fishing segment relevant in the region (Follesa et al., 2011a,b). Moreover, even if sharks and other chondrichthyans are not targets of Sardinian fisheries, they are often caught as by-catch or they are discarded. Fishery-independent surveys provide valuable measures of relative abundance, rates of population change, sex and size composition for a wide range of species including those not targeted by commercial fishing. As these measures are obtained from scientific sampling or within an experimental design, they are less subject to the unknown and often confounding factors that complicate the interpretation of fishery-dependent indices of stock status. Specifically, scientific trawl surveys have as advantages the design assumptions easier to satisfy a multispecies perspective (Rago, 2005). In this regard, the aim of this work is to assess the status of demersal Chondrichthyes in Sardinian waters, examining temporal changes throughout data obtained from a scientific trawl survey, the Mediterranean International Trawl Survey (MEDITS, Bertrand et al., 2002). This goal will be achieved (i) analyzing time series (1994–2015) trends of abundance (density and biomass) and (ii) assessing the current composition of cartilaginous catches in terms of species and size. 2. Material and methods 2.1. Study area The investigated area (Fig. 1) extends for 23.700 km2 and includes all the seas surrounding the island of Sardinia (central western Mediterranean; Geographical Sub-Area, GSA 11). This region is part of the FAO statistical sub-area 37.1.3 (i.e., Sardinia), which is characterized by 1.846 km of non-homogenous coasts, with different extension, oceanographic, geomorphological and bionomical features (Cau et al., 1994; Addis et al., 1998). From an oceanographical point of view, this area belongs to two different basins: the Algerian-Provençal and the Tyrrhenian ones, which are connected by the Sardinian Channel. For what concerns the bathymorphological features, four main zones can be described: i) the western coast, characterized by a wide extension of the continental shelf; ii) the northern portion of the island, characterized by a moderate extension of the continental shelf and a narrow and steep slope; iii) the eastern coast, characterized by little and steep fishing grounds and iv) the southern coast, characterized by a wide shelf area (Palomba and Ulzega, 1984). The bathymetric division of the GSA 11 bottoms points out that the great part of them (about 67%) are found below a depth of 100 m.

3. Results A total of 25 demersal Chondrichthyes species belonging to 7 orders and 13 families were detected (Table 1). The frequency distributions and abundances of chondrichthyan subdivided per Order were very skewed (Fig. 2), with Carcharhiniformes and Rajiformes dominant. Chimaeriformes, Myliobatiformes, Torpediniformes and Hexanchiformes occurred only sporadically (Fig. 2).

2.2. Surveys and statistical analyses 3.1. Chimaeras Data were collected during the MEDITS scientific bottom trawl survey project (Bertrand et al., 2002) conducted annually in late springearly summer (from May to July) during daylight (between 30 min after sunrise and 30 min before sunset). The examined time series covered 22 years, from 1994 to 2015. A total of 2339 positive hauls (1414 within 200 m, and 925 between 200 and 800 m) were performed according to the MEDITS protocol (MEDITS Handbook, 2016). This survey is carried out according to a stratified random sampling design based on five depth strata: 10–50 m, 51–100 m, 101–200 m, 201–500 m, 501–800 m,

3.1.1. Order Chimaeriformes Sardinian waters host the only species belonging to this order and living in the Mediterranean: C. monstrosa (Table 1). Surveys indicated its exclusive occurrence in the bathyal zone (321–682 m) with low frequencies (f% = 7.28 ± 4.00, mean ± S.D., Table 2) and abundance (DI = 1.74 ± 1.62, BI = 0.12 ± 0.1, mean ± S.D., Table 3) values. Size distribution ranged between 16.6 and 56 cm TL (31.7 ± 10.7 cm TL, mean ± S.D.). The paucity of captures did not 82

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Fig. 1. Map of the study area with indication of the investigated bathymetric strata during the MEDITS project.

significant trends in both Abundance Indexes only in the continental shelf (Table 3). According to the biomass analysis, bigger specimens (30.8 ± 8.3 cm TL, mean ± S.D.) were caught mostly in the shallower stratum rather than the deeper one (23.5 ± 8.3 cm TL, mean ± S.D.) (KS test, P-value < 0.05) (Table 4). A size temporal trend stable overtime was observed (Table 4, Fig. 5). Although the blackmouth catshark G. melastomus presented a wide depth distribution (69–730 m), it clearly preferred deep environments as confirmed by the occurrence analysis (f% = 0.98 ± 1.13 in the shelf, and f% = 77.23 ± 6.27 in the slope, Table 2) and by both Abundance Indexes (Table 3). Mean values of density and biomass indicated a fluctuant pattern with no significant changes throughout the years (Table 3, Fig. 4). Temporal size trend seemed to be decreasing (Table 4; Fig. 5). The last species belonging to this order, M. mustelus was caught only twice in 22 years (at 35 and 227 m). The only measured specimen reached 36.5 cm of TL (Table 4). Due to this extremely low data availability it was not possible to establish its real status in our seas (Table 3).

permit the evaluation of a temporal trend (Table 4).

3.2. Sharks 3.2.1. Order Carcharhiniformes This order was represented by two families and three species: the small-spotted catshark S. canicula and the blackmouth catshark G. melastomus, both belonging to the Scyliorhinidae family, and the common smoothhound Mustelus mustelus belonging to the Triakidae family (Table 1). Considering the overall stratum, the small-spotted catshark was the most frequent (f% = 46.16 ± 8.35, mean ± S.D.) and abundant (DI = 350.3 ± 130.4, BI = 26.8 ± 11.7; mean ± S.D.) species caught around Sardinian seas (Tables 2 and 3). It showed a wide depth distribution (28–631 m) appearing, however, more common (Table 2) in the continental shelf (f% = 52.39 ± 8.96, mean ± S.D.) than in the slope (f% = 38.10 ± 9.26, mean ± S.D.). During the examined period, the mean Density Index (with a progressive increase through the years in both macro-strata, Figs. 3 and 4) was higher in the slope than in the shelf. An opposite trend was found for the mean Biomass Indexes (Table 3). The Spearman test highlighted positive statistically

3.2.2. Order Hexanchiformes The sharpnose sevengill Heptranchias perlo and the bluntnose sixgill 83

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Table 1 List of the 25 species inhabiting Sardinian waters and their relative IUCN status in the Mediterranean (Dulvy et al., 2016) and in the world (Abdul Malak et al., 2011). Order

Family

Species

Common name

Mediterranean status

Global status

Carcharhiniformes

Scyliorhinidae

Chimaeriformes Hexanchiformes

Triakidae Chimaeridae Hexanchidae

Myliobatiformes

Dasyatidae

Rajiformes

Myliobatidae Rajidae

Galeus melastomus Rafinesque, 1810 Scyliorhinus canicula (Linnaeus, 1758) Mustelus mustelus (Linnaeus, 1758) Chimaera monstrosa Linnaeus,1758 Heptranchias perlo (Bonnaterre, 1788) Hexanchus griseus (Bonnaterre, 1788) Dasyatis centroura (Mitchill, 1815) Dasyatis pastinaca (Linnaeus, 1758) Myliobatis aquila (Linnaeus, 1758) Dipturus nidarosiensis (Storm, 1881) Dipturus oxyrinchus (Linnaeus, 1758) Leucoraja circularis (Couch, 1838) Raja asterias Delaroche, 1809 Raja brachyura Lafont, 1871 Raja clavata Linnaeus, 1758 Raja miraletus Linnaeus, 1758 Raja polystigma Regan, 1923 Centrophorus granulosus (Bloch e Schneider, 1801) Dalatias licha (Bonnaterre, 1788) Etmopterus spinax (Linnaeus, 1758) Oxynotus centrina (Linnaeus, 1758) Squalus blainville (Risso, 1827) Tetronarce nobiliana Bonaparte, 1835 Torpedo marmorata Risso, 1810 Torpedo torpedo (Linnaeus, 1758)

blackmouth catshark small-spotted catshark common smoothhound rabbitfish sharpnose sevengill bluntnose sixgill shark roughtail stingray common stingray common eagle ray norwegian skate longnosed skate sandy skate starry skate blonde skate thornback skate brown skate speckled skate gulper shark kitefin shark velvet belly angular rough shark longnose spurdog great torpedo ray marbled electric ray common torpedo ray

LC LC VU NT DD LC VU VU VU – NT CR NT NT NT LC LC CR VU LC CR DD LC LC LC

LC LC VU NT NT NT LC DD DD NT NT VU LC NT NT LC NT VU NT LC VU DD DD DD DD

Squaliformes

Torpediniformes

Centrophoridae Dalatidae Etmopteridae Oxynotidae Squalidae Torpedinidae

CR = critically endangered; DD = data deficient; EN = endangered; LC = least concern; NT = near threatened; VU = vulnerable.

for its congeneric, specimens of D. pastinaca were also caught exclusively in the shelf (18–84 m) with a low occurrence (f% = 7.09 ± 4.44, mean ± S.D., Table 2). The year DI plot (Fig. 2) showed signs of increase in the last years confirmed by a significant positive correlation (Spearman test, P-value < 0.05, Table 3). Specimens of D. pastinaca showed a mean TL of 78.3 ± 45.5 with a stable size trend (Table 4). The eagle ray Myliobatis aquila was the only species of the Myliobatidae family sampled in our seas (Table 1). This species, typical of coastal environments (30–49 m), showed scattered catches, as shown in Tables 2 and 3. Given the paucity of data (only 36 specimens in 22 years), it was difficult to infer its densities.

Hexanchus griseus represented the only two species belonging to the Hexanchidae family caught in Sardinan waters. These sharks were sporadically sampled in the slope only (H. griseus three times between 276 and 624 m and H. perlo twice at 273 and 336 m), as indicated by the low values of the occurrence (Table 2) and both Abundance Indexes (Table 3). The only specimens measured for each species reached 80.5 cm and 153 cm of TL for H. perlo and H. griseus, respectively (Table 4). Given the paucity of data collected, it was impossible to give any other information about both species in Sardinian waters. 3.2.3. Order Squaliformes This order was the second most taxonomically heterogeneous in Sardinian waters, having 5 species, belonging to 5 different families (Table 1). The velvet belly Etmopterus spinax and the longnose spurdog Squalus blainville were the most frequent and abundant among this order sharing a wide depth range (130–730 m and 35–678 m, respectively), with a clear preference for the slope (E. spinax f% = 48.91; S. blainville f% = 17.52; Table 2). As representative of the slope, the velvet belly showed an increase of occurrence (Spearman test, Pvalue < 0.05, Table 2) and in abundance (Fig. 4) (Spearman test, Pvalue < 0.05, Table 3). Temporal size trend showed similar mean values during the sampled period (Table 4, Fig. 5). The longnose spurdog data, analyzed from 2005, highlighted increasing mean values of DI with a positive correlation. The largest specimens were caught mostly in the slope (Table 4). The last species, Centrophorus granulosus (353–675 m) and Dalatias licha (534–730 m), were caught exclusively in the bathyal zone (Table 2) with low mean values of DI and BI (Table 3). Finally, Oxynotus centrina (141–539 m) was sampled rarely (Tables 2 and 3), and the scarcity of the collected data made it difficult to make inferences about these species.

3.3.2. Order Rajiformes This order presented 8 species belonging to the Rajidae family (Table 1). Among all these species, R. clavata was well represented in both strata (28–625 m) with quite similar frequencies (Table 2) and abundance values (Table 3). A slight preference was detected for the shelf, where its density and biomass were higher than in the slope (Table 3). The years DI plots showed a not statistically significant values increase in the overall and in the shelf strata (Spearman test, Pvalue > 0.05) (Fig. 3, Table 3) and an opposite trend in the slope (Table 3, Fig. 4). Bigger individuals (46.3 ± 13.8 cm TL, mean ± S.D.) were mainly caught in the upper stratum rather than in the deepest one (39.7 ± 14.9 cm TL, mean ± S.D.) as revealed by the KS test (P-value < 0.05, Table 4). An increasing size temporal trend, not statistically significant, was found (Fig. 5). Another Rajidae showing a wide distribution was R. polystigma (32–551 m). The analysis of the occurrence (Table 2) and the Abundance Indexes (Table 3) highlighted that biggest specimens (32.8 ± 9.0 cm TL, mean ± S.D., Table 4) preferred to inhabit the shelf. The temporal DI plot (Fig. 3) seemed to be slightly decreasing with no statistically significant differences (Table 3). However, size temporal trend was stable (Fig. 5). R. miraletus, as the other species mentioned above, showed a wide depth distribution (28–416 m), with a clear preference for the shelf (Tabb. 2, 3) where it displayed a temporal increasing density statistically significant (Spearman test, P-value < 0.05; Fig. 3, Table 3). The few individuals caught in the slope showed bigger sizes

3.3. Batoids 3.3.1. Order Myliobatiformes Within this order, the Dasiatidae family was represented by two species: Dasyatis centroura and D. pastinaca (Table 1). Only two adult specimens of D. centroura were sampled in 2013 in shallow waters (40 m), showing a TL of 247 cm and 243 cm respectively (Table 4). As 84

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Fig. 2. Frequency of occurrence (A), Density Index (B) and Biomass Index (C) of Chondrichthyes orders caught in Sardinian waters. Bars represent standard deviation.

increase from 2005 to 2015, (Spearman test, P-value < 0.05; Table 4, Fig. 5). The congeneric D. nidarosiensis, instead, was rarely caught during the entire sample period (only twice in 22 years) as displayed in Tables 2 and 3, preferring deeper waters (145–719 m). At last, survey data indicated as Leucoraja circularis presented an exclusively bathyal distribution (225–583 m) (Table 2). The year DI and BI analysis showed a slow positive trend in the last surveys (Spearman test, P-value < 0.05, Table 3).

(36.3 ± 7.3 cm TL, Table 4) than those observed in the shelf (29.5 ± 7.5 cm TL, KS test, P-value < 0.05). The general size temporal trend was stable (Fig. 5). Differently from the other congenerous, R. asterias (26–88 m) and R. brachyura (28–195 m) were exclusively sampled in the first 200 m of the water column. In particular, the blonde skate showed statistically increasing trends both in density (Fig. 3) and in size (Fig. 5) (Spearman test, P-value < 0.05). The DI and BI analysis of R. asterias showed a fluctuant pattern with higher values from 2005. Despite the wide distribution (76–671 m), Dipturus oxyrinchus was observed mostly in the bathyal zone (f% = 42.22; Table 2) (Table 3). As shown by the years DI plot, a constant trend was present in the slope (Fig. 4). In the first 200 m, specimens showed a mean TL higher than the slope (Table 4) (KS test, P-value < 0.05; Table 4). The blox plot of TL per years (Fig. 5) displayed a statistically significant

3.3.3. Order Torpediniformes The Torpedinidae family was represented by 3 species: the great torpedo ray Tetronarce nobiliana, the marbled electric ray Torpedo marmorata, and the common torpedo ray T. torpedo (Table 1). These species were not so commonly caught in Sardinian waters, as showed in 85

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Table 2 Percentage of occurrence (f%, mean ± S.D.) by depth stratum (10–800 m, overall; 10–200 m, shelf; 201–800 m, slope) investigated, for all species, in the MEDITS trawl surveys around Sardinian waters from 1994 to 2015, except for S. blainville (from 2005 to 2015). Order

Species

Depth Range (m)

f% overall

f% shelf

f% slope

Carcharhiniformes

G. melastomus M. mustelus S. canicula C. monstrosa H. griseus H. perlo D. centroura D. pastinaca M. aquila D. nidarosiensis D. oxyrinchus L. circularis R. asterias R. brachyura R. clavata R. miraletus R. polystigma C. granulosus D. licha E. spinax O. centrina S. blainville T. marmorata T. nobiliana T. torpedo

69–730 35–227 28–631 321–682 276–624 273–336 40 18–84 30–49 145–719 76–671 225–583 26–88 28–195 28–625 28–416 32–551 353–675 534–730 130–730 141–539 35–678 28–450 21–651 21–162

30.65 ± 2.23 0.09 ± 0.82 46.16 ± 8.35* – – – –

0.98 ± 1.13 0.7 ± 0.31 52.39 ± 8.96* – – – 0.25 ± 0.22 7.09 ± 4.44* 1.12 ± 1.33 0.08 ± 0.36 7.49 ± 2.71 – 10.75 ± 5.38* 12.73 ± 8.42* 29.25 ± 5.68 36.93 ± 9.26* 39.86 ± 9.11* – – 0.16 ± 0.7 0.23 ± 0.56 2.66 ± 1.38 2.52 ± 3.20* 2.78 ± 3.08 2.53 ± 2.91

77.23 ± 6.27 0.14 ± 0.62 38.10 ± 9.26 7.28 ± 4.00 0.37 ± 0.92 0.28 ± 0.71 –

Chimaeriformes Hexanchiformes Myliobatiformes

Rajiformes

Squaliformes

Torpediniformes

– 0.10 ± 0.31 21.18 ± 2.39 – – – 29.92 ± 3.84 23.16 ± 5.80* 29.86 ± 6.46* – – 18.96 ± 3.07 0.64 ± 0.73 8.16 ± 3.35 2.22 ± 2.28* 2.06 ± 1.96 –

– 0.13 ± 0.58 42.22 ± 5.11 2.14 ± 3.08* – – 32.59 ± 7.22 1.63 ± 1.81 14.57 ± 5.78 1.78 ± 2.68 2.19 ± 3.07 48.91 ± 7.22* 1.26 ± 1.36 17.52 ± 8.64 0.83 ± 1.4 2.06 ± 1.96 –

* Statistical significant differences: Spearman test, P < 0.05.

4. Discussion

Tables 2 and 3. The common torpedo ray was the only one sampled only in the shelf (21–162 m). The marbled electric ray, distributed between 28 and 450 m with a clear preference for the shelf (f% = 2.52), was the only species that showed positive trends through all the entire survey period, both in frequencies of captures (Table 2) that in abundance (Table 3). And finally, the great torpedo ray, differently from the other members of the family, reached deeper bathymetries (21–651 m), but seemed to choose the shelf as a preferential habitat (Table 3). Specimens caught in slope (45.4 ± 17.5 cm TL) were bigger than those from shelf (25.2 ± 13.3 cm TL) (Table 4).

Understanding the population dynamics of Chondrichthyes requires several factors to be considered that can often act synergically, such as exploitation, changes in ecological interactions (e.g., predation and competition), different exposure to fishing (e.g., catchability, availability, commercial value, breeding clusters) and susceptibility to other stressors such as habitat degradation and pollution (Ferretti et al., 2013). All these aspects can alter the species-specific response to exploitation, generating complex community changes over time and space (Ferretti et al., 2010). Among the above mentioned factors, there has been an increasing international concern about changes in the abundance and diversity of chondrichthyan species principally due to the emerging evidence of their inability to sustain high levels of fishing pressure like the majority of teleost species (Stevens et al., 2000). This becomes even more alarming if we consider that many species, particularly those living on the continental slope, are poorly known both in terms of taxonomy and population status (i.e., often Data Deficient; Norse et al., 2012). Focusing on fishing exposure, this study reports data from a 22 yeartrawl survey describing temporal changes of Chondrichthyes in Sardinian waters. Regarding the available scientific literature in the Mediterranean, long time series of catches (i.e., > 50 years) highlighted decreasing trends in several areas: Gulf of Lion (Aldebert, 1997), Ligurian seas (Ligas et al., 2013) and Adriatic (Jukic-Peladic et al., 2001; Ferretti et al., 2013; Barausse et al., 2014; Fortibuoni et al., 2016). However, considering a shorter time series (i.e., ∼20 years), in Tuscan waters stocks are thought to be under rebuilding according to an increase in catches (Ligas et al., 2013). In contrast with features described worldwide, including the Mediterranean (Graham et al., 2001), our results showed a stable pattern or even increasing trend of Chondrichthyes abundance in the seas around Sardinia. This result is confirmed by the GAM routine conducted both for the density/depth and biomass/depth relation across years (Fig. 6). The factors mainly contributing to the observed

3.4. GAM model analysis The GAM performed to test variations in the density/depth and biomass/depth relation for Chondrichthyes over the 22 years of investigation, although significant, showed very low percentages of explained deviance (i.e., < 10% for both response variables), emphasizing stability across years for the investigated parameters (Table 5, Fig. 6). When the model was performed for the major sub-categories (i.e., Batoids and Sharks), the percentage of explained deviance, which remained significant for both categories, increased to 24.7% for Batoids and 13% for Sharks. Also when the analysis was focused on the most abundant species of Batoids and Sharks, annual variations appeared to be significant but without any specific trend. This is the case of S. canicula and G. melastomus, which showed values of explained deviance of 17% and 18.8% for abundance and 15.4% and 12.9% for biomass, respectively. A similar trend was found also in R. miraletus, showing 18.7% and 13.6% of explained deviance for the density/depth and biomass/depth relation across years. The highest explained deviance was observed for R. clavata, which showed 32.5% for abundance and 25.7% for biomass, emphasizing a less stable trend compared to other species during the 22 years of investigation. For all models, no residual pattern was observed.

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Table 3 Mean Density Index N/km2 (DI ± S.D.) and mean Biomass Index kg/km2 (BI ± S.D.) by depth stratum for all chondrichthyan species sampled in Sardinian waters between 1994 and 2015 (MEDITS), except for S. blainville (from 2005 to 2015). Temporal trends are given. Order

Species

Overall 10–800 m

Trend

Shelf 10–200 m

Trend

Slope 201–800 m

Trend

Carcharhiniformes

G. melastomus

S I NE NE I I –

DI = 1.04 ± 2.5 BI = 0.2 ± 0.5 DI = 0.02 ± 0.08 BI = 0.01 ± 0.02 DI = 293.9 ± 119.4* BI = 32.1 ± 18.0* – – – – – – DI = 0.04 ± 0.2 BI = 1.64 ± 7.7 DI = 49.1 ± 37.3* BI = 29.9 ± 19.9 DI = 0.88 ± 1.81 BI = 0.80 ± 1.51 DI = 0.01 ± 0.07 BI = 0.001 ± 0.004 DI = 7.0 ± 7.3 BI = 9.6 ± 10.0 – – DI = 15.9 ± 13.4 BI = 11.7 ± 7.7* DI = 38.2 ± 44.9* BI = 17.2 ± 20.9* DI = 51.7 ± 18.6 BI = 40.1 ± 16.1 DI = 48.8 ± 30.0* BI = 7.4 ± 4.0* DI = 53.2 ± 25.5 BI = 15.5 ± 9.2 – – – – DI = 0.24 ± 1.12 BI = 0.04 ± 0.2 DI = 0.03 ± 0.09 BI = 0.01 ± 0.3 DI = 1.56 ± 0.9* BI = 0.7 ± 0.5* DI = 1.12 ± 1.60* BI = 0.55 ± 0.87* DI = 0.70 ± 0.82 BI = 0.32 ± 0.51* DI = 1.02 ± 1.97 BI = 0.50 ± 1.19

I I NE NE I I –

DI = 786.1 ± 267.4 BI = 48.9 ± 15.4 DI = 0.12 ± 0.56 BI = 0.03 ± 0.13 DI = 402.4 ± 161.01 BI = 17.6 ± 6.3 DI = 1.74 ± 1.62 BI = 0.12 ± 0.1 DI = 0.04 ± 0.1 BI = 0.72 ± 2.27 DI = 0.02 ± 0.08 BI = 0.03 ± 0.09 – – – – – – DI = 0.01 ± 0.06 BI = 0.002 ± 0.008 DI = 19.7 ± 17.1 BI = 14.8 ± 7.2 DI = 0.6 ± 0.9* BI = 0.4 ± 0.6* – – – – DI = 37.1 ± 17.0 BI = 17.9 ± 6.0 DI = 1.4 ± 3.9 BI = 0.2 ± 0.7 DI = 10.1 ± 6.2 BI = 1.5 ± 1.6* DI = 0.3 ± 0.6 BI = 1.1 ± 2.2 DI = 0.25 ± 0.34 BI = 0.6 ± 1.4 DI = 87.5 ± 39.2* BI = 4.9 ± 2.2* DI = 0.12 ± 0.14 BI = 0.3 ± 0.4 DI = 6.6 ± 3.4* BI = 5.5 ± 2.9* DI = 0.07 ± 0.15 BI = 0.02 ± 0.05 DI = 0.13 ± 0.23 BI = 0.11 ± 0.55* – –

S I NE NE I D I S NE NE NE NE – – – – – – NE NE S I I I – – – – D D D D D D NE NE NE NE I I NE NE I D S D D D – –

Chimaeriformes

C. monstrosa

DI = 285.9 ± 98.6 BI = 17.8 ± 5.3 DI = 0.05 ± 0.2 BI = 0.01 ± 0.05 DI = 350.3 ± 130.4 BI = 26.8 ± 11.7 –

Hexanchiformes

H. griseus

–

–

H. perlo

–

–

D. centroura

–

–

D. pastinaca

–

–

M. aquila

–

–

D. nidarosiensis

L. circularis

DI = 0.01 ± 0.05 BI = 0.001 ± 0.004 DI = 11.6 ± 6.4 BI = 11.5 ± 6.6 –

NE NE D D –

R. asterias

–

–

R. brachyura

–

–

R. clavata

C. granulosus

DI = 46.3 ± 14.2 BI = 32.0 ± 11.3 DI = 31.4 ± 18.8* BI = 4.8 ± 2.5* DI = 38.7 ± 13.0 BI = 11.6 ± 7.0 –

I I I I D D –

D. licha

–

–

M. mustelus S. canicula

Myliobatiformes

Rajiformes

D. oxyrinchus

R. miraletus R. polystigma Squaliformes

E. spinax O. centrina S. blainville Torpediniformes

T. marmorata T. nobiliana T. torpedo

*

DI = 35.1 ± 19.9 BI = 2.21 ± 1.98* DI = 0.07 ± 0.1 BI = 0.2 ± 0.25 DI = 3.16 ± 1.4* BI = 2.3 ± 1.21* DI = 0.74 ± 1.05* BI = 0.35 ± 0.55* DI = 0.49 ± 0.54* BI = 0.24 ± 0.18* –

I I NE NE I D I I D D –

– – – – NE NE I I I I NE NE D D – – I I I I I I I I D D – – – – NE NE NE NE I I I I D D S S

D = decreasing trend; I = increasing trend; NE = not evaluable trend; S = stable trend. * Statistical significant differences: Spearman test, P < 0.05.

that the trawling fleet operating in Sardinia comprises 137 boats over an area of 23.700 km2 with a production amounted to slightly over 3.000 t (Follesa et al., 2011b). Considering the same year, if we compare Sardinian fleet with, for example, the north Adriatic one (1271 trawl boats over an area of 92.660 km2 with a production of 32.698 t estimated in 2009; Manfredi and Piccinetti, 2011), the difference in fishing effort should immediately come to light. In addition, the average activity for trawling boats in Sardinian seas was 147 days per boat, compared to a national figure of 159 days (Follesa et al., 2011b). In this work, the analysis conducted on the two bathymetric strata (shelf, 10–200 m; slope 200–800 m) highlighted a similar distribution pattern common to other Mediterranean areas (e.g. Bertrand et al., 2000; Massutì and Moranta, 2003), but with different abundance patterns. In the shelf, S. canicula was the most abundant species as

pattern are not easy to discern; however, the application of fishing bans, the absence or limitation of long lines fishery (which often includes Chondrichthyes catches; Cataudella et al., 2011), and the dominance of artisanal fishery targeting other species such as the spiny lobsters Palinurus elephas (Follesa et al., 2011a), partially explain the absence of alarming signals of Chondrichthyans depletion. In addition, the policy of fleet modernization adopted by the Regional Government of Sardinia since the late 1980s has aimed to build large trawlers able to fish off shore, moving the trawling pressure towards deeper areas, with a consequent improvement of the status of shelf fishery resources (Cau, 2008). Given this displacement fishing pressure increase, Chondrichthyes inhabiting deep waters should be more affected than those inhabiting the shallow. However our data highlighted a good condition in both strata that could be due to low numbers of trawlers of Sardinian fleet when compared to other areas. Data reported in 2009 highlighted 87

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Table 4 In this table the minimum and maximum sizes and the mean ± standard deviation of the total length of all the 25 chondrichthyan species were displayed. Kolmogorov-Smirnov (KS) test was used to detect statistical significant differences of those species that inhabit both macro-strata (shelf and slope). Size temporal trends were showed. Order

Species

N

Range TL (cm) Mean ± S.D. Shelf (10–200 m)

Range TL (cm) Mean ± S.D. Slope (201–800 m)

KS P-value

Overall size trend

Carcharhiniformes

G. melastomus

17,900

D

1

–

NE

S. canicula

26,769

< 0.05

S

Chimaeriformes

C. monstrosa

37

–

NE

Hexanchiformes

H. griseus

1

–

–

NE

H. perlo

1

–

–

NE

D. centroura

2

–

NE

D. pastinaca

683

–

–

S

M. aquila

29

–

–

NE

D. nidarosiensis

3

243–247 245 ± 2.83 27–151.4 78.3 ± 45.5 47–67.9 60.8 ± 9.7 24.7

5.5–63 28.5 ± 10.3 – – 6.1–53.5 23.5 ± 8.3 16.6–56 31.7 ± 10.7 153 – 80.5 – –

< 0.05

M. mustelus

13.3–48.1 29.1 ± 11.7 36.5 – 8.3–58.7 30.8 ± 8.3 –

–

NE

D. oxyrinchus

729

< 0.05

I*

L. circularis

35

–

NE

R. asterias

589

–

I

R. brachyura

1813

–

–

I*

R. clavata

6128

I

1696

< 0.05

S

R. polystigma

1513

< 0.05

S

C. granulosus

15

–

NE

D. licha

11

–

–

NE

E. spinax

1906

> 0.05

S

O. centrina

4

–

NE

S. blainville

208

> 0.05

S

T. marmorata

48

> 0.05

NE

T. nobiliana

9

> 0.05

NE

T. torpedo

13

22.5–31 27.4 ± 3.6 63.3–65.5 64.4 ± 2.5 28–74 44.5 ± 12.7 11.7–53 22.9 ± 10.5 13–44 25.2 ± 13.3 13.6–47.5 27.5 ± 13.1

10.5–106 39.7 ± 14.9 26–45.4 36.3 ± 7.3 13.2–41.1 25.3 ± 4.5 44.1–103 77.5 ± 23.8 32.2–99 47.8 ± 21.6 9.5–43 21.3 ± 7.0 40.1–60.9 50.5 ± 14.7 21.2–89 52.2 ± 15.7 12.8–42.2 18.8 ± 11.6 32.1–70 45.4 ± 17.5 –

< 0.05

R. miraletus

19.1–91.9 47.5 ± 11.3 12–106 34.7 ± 13.9 6.8–96 46.3 ± 13.8 13.5–46.5 29.5 ± 7.5 10.3–59.5 32.8 ± 9.0 –

26.9–129.7 78.3 ± 72.7 10.6–111.5 47.9 ± 23.9 16.6–73.4 44.9 ± 13.9 –

–

NE

Myliobatiformes

Rajiformes

Squaliformes

Torpediniformes

23–115.3 69.2 ± 19.1 –

D = decreasing trend; I = increasing trend; NE = not evaluable trend; S = stable trend. * Statistical significant differences: Spearman test, P < 0.05.

abundant. The variables involved in the Chondrichthyes resilience seem to be related to several factors like particular phases of the life history such as reproduction and feeding (e.g. Saïdi et al., 2008; Barría et al., 2015; Finotto et al., 2015) and also to specific surviving capability after discarding, especially in the shallows, during the short climb (JukicPeladic et al., 2001; Ragonese et al., 2013). Our results emphasized two different patterns for the investigated strata. In the shelf, increasing trends were observed in those species (e.g., S. canicula, R. brachyura, R. clavata, R. miraletus) that, although have a low commercial value (only big individuals landed), are in large extent discarded. Among the species principally inhabiting deep environments and

reported in other Mediterranean seas (e.g. France, Spain, Greece) (Bertrand et al., 2000) but differently from south Tyrrhenian, Western Adriatic and Ionian Sea (Bertrand et al., 2000) where it was less abundant. Also batoid species, belonging principally to the Rajiformes (except for genus Dipturus and Leucoraja), were consistent at these depths. The paucity and the solitary habits of torpedos (Bertrand et al., 2000) and the ability to avoid the trawl action due to semi-pelagic habits of eagle rays (Holtzhausen et al., 2009) could be a possible explanation to their very low frequency in bottom trawls. On the contrary, sharks (e.g. G. melastomus, S. canicula, E. spinax and S. blainville) were more frequently caught on the slope, while batoids (e.g. R. clavata and D. oxyrinchus, the most representative) were less 88

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Fig. 3. Density Indexes of the six most abundant species found in the continental shelf (10–200 m) (S. canicula, R. clavata, R. polystigma, R. miraletus, D. pastinaca and R. brachyura) during the MEDITS surveys (1994–2015).

It is known that fish overexploitation could lead to densitydependent changes in certain life-history characteristics (Fahy, 1989) that in some elasmobranch populations could be reflected on a decrease in population size (Sosebee, 2005; Paesch and Oddone, 2008). In Sardinian seas the majority of the analyzed stocks showed stable size temporal trends and, furthermore, two batoids, R. brachyura and D. oxyrinchus, even displayed a positive correlation, giving another encouraging signal of the good status of cartilaginous fish in Sardinian waters for the most abundant species. Differences in size distribution found between strata could reflect interspecific and intraspecific competition as reported by many authors (e.g., Gouraguine et al., 2011; Valls et al., 2011; Mulas et al., 2015). Bathymetric segregation may be a useful tool to minimize competition for food resources and to prevent the predation particularly in these environments, which become more oligotrophic with depth, as stated by Valls et al. (2011). Similarly to what was found in the western Mediterranean (Gouraguine et al., 2011), it seemed that Sardinian adults (higher values of mean total length and biomass) of ubiquitous species as S. canicula and R. clavata were mainly distributed in the shallows, and

commonly caught as by-catch in the red shrimp fisheries, only two species displayed increasing trend: the longnosed spurdog S. blainville (having a low commercial value) and E. spinax (entirely discarded). Two other species totally discarded as G. melastomus and D. oxyrinchus, exhibited a quite stable condition. The high resilience displayed by these epi-bathyal elasmobranchs could be explained, another time, by the high level of survival due to a minimum barotrauma suffered as a consequence to the lack of swimming bladder (Davis, 2002; Revil et al., 2005). A further reason of survival of deep species could be explained by the fact that these species, mainly scavenger or generalist feeders, took advantage, in terms of energy, from the trawl activity finding discarded dead bony fish and invertebrates at the sea bottom (Olaso et al., 1998). In addition, species as the velvet belly and the blackmouth catshark, living beyond the usual commercial trawl limits, could find a refuge in the deepest waters escaping from the gear action (Dimech et al., 2012). In fact, as reported by Follesa et al. (2011c), these sharks (especially G. melastomus) are well represented in deep Sardinian waters with high biomass values found at depths of 720–1099 m, denoting the presence of large specimens in the bathyal zone. 89

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Fig. 4. Density Indexes of the six most abundant species found in the slope (200–800 m). G. melastomus, S. canicula, E. spinax, R. clavata, D. oxyrinchus from 1994 to 2015 and S. blainville from 2005 to 2015, during the MEDITS surveys.

received very little scientific attention in the past. In this regard, our study provided important data on their size distributions about species as C. monstrosa, D. nidarosiensis (recently discovered by Cannas et al. in 2010 in Sardinian seas) and D. licha. Additionally, useful information about other species belonging to the Centrophoridae (C. granulosus), Oxynotidae (O. centrina) and Triakidae (M. mustelus) family, all listed as vulnerable (VU) and even critically endangered (CR) by the IUCN (Dulvy et al., 2016) have been acquired. Even if in Sardinian waters the general status of demersal Chondrichthyes does not show alarming signals of depletion, the implementation of an effective conservation and fishery management plans would be desirable. Technical measures directed to by-catch species and adopted according to the Ecosystem Approach to Fisheries Management (EAFM, Garcia et al., 2003) within management plans targeted to main fisheries, could be more effective to mitigate fishery impacts on Chondrichthyes. For example, improvement of trawl design, as well as the identification and protection of those Essential Fishing

juveniles (lower values of mean total length and biomass) preferred to stay below 200 m. It is possible an interspecific bathymetric overlap between juveniles and adults of these species with a probable competition for space and trophic resources. This pattern was found also for R. polystigma. Sardinian specimens appeared generally bigger in size than those living the eastern parts of the basin as for S. canicula (Moutopoulos et al., 2013; Finotto et al., 2015), R. clavata (Demirhan and Can, 2007; Başusta et al., 2012) and D. oxyrinchus (Yigin and Ismen, 2010) and in general smaller or similar to those caught in the Balearic islands (western Mediterranean) by Gouraguine et al. (2011) and Barria et al. (2015). These differences could be related to different environmental and biological factors, fisheries impacts, and also to the sampling itself (Froese, 2006). In the Mediterranean, some Chondrichthyes are generally defined as non-common or rare due to many reasons (e.g., solitary behaviors, sampling type, habitat degradation) and, for this reason, they have

90

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Fig. 5. Size temporal trend analysis of S. canicula, G. melastomus, R. clavata, R. polystigma, R. miraletus, R. brachyura, D. oxyrinchus and E. spinax through the years.

no unique bycatch reduction solution can adequately improve selectivity of all species (Petrakis and Stergiou, 1997; Sala et al., 2008). Analysis like the average body size should be extended over time because of its significant role as sensitive indicator of chondrichthyan stock status with respect to catch rates, when a sufficient long time series data is available (Megalofonou, 2005). Future perspectives should define sound conservation measures incorporating minimum

Habitats (EFH) that act as nursery and spawning grounds represent a fundamental tool for future implementations of conservation measures (Walker, 2005; Etnoyer and Warrenchuk, 2007; Heupel et al., 2007; Cau et al., 2016). Furthermore, improvements of selective fishing techniques to avoid and reduce unwanted catches as shark-excluding grid devices (Brčić et al., 2015) are highly encouraged. Due to the multispecies character of Mediterranean trawl catches, it is clear that

91

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Fig. 6. Box-plots representing the temporal trends of Abundance Indexes (DI and BI) for the entire Chondrichthyes population, and Batoids and Sharks separately.

Acknowledgments

size thresholds, which are based on the studies focused on life-history traits. This could be a promising solution given the high survival rates of discarded elasmobranchs documented for several species (Revill et al., 2005; Mandelman and Farrington, 2007; Enever et al., 2009). At least, given the seasonal differences in the Chondrichthyes distribution seen in the Strait of Sicily (Ragonese et al., 2013), studies on temporal pattern covering other seasons of the year are necessary to support conservation plans in this area.

This study was financed by Autonomous Region of Sardinia within the frame of the research project ‘Approccio multidisciplinare per la conservazione e gestione della selacofauna del Mediterraneo' (LR7 CRP25321) and carried out within the Data Collection Regulation and Framework − module trawl surveys MEDITS (Mediterranean International Trawl Survey). We also wish to thank the editor and the two anonymous referees 92

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Table 5 Results of Generalized Additive Model (GAM) performed for the entire Chondrichthyes population, Batoids, Sharks, and for the most abundant species. Density, N/Km2

Chondrichthyes Batoids Sharks G. melastomus R. clavata R. miraletus S. canicula

Biomass, kg/km2

P-value

DE%

P-value

DE%

< 2e-16*** < 2e-16*** < 2e-16*** < 2e-16*** < 2e-16*** < 2e-16*** < 2e-16***

1.87 24.7 7.69 18.8 32.5 18.7 17

< 2e-16*** < 2e-16*** < 2e-16*** < 2e-16*** < 2e-16*** < 2e-16*** < 2e-16***

7.65 13 8.07 12.9 25.7 13.6 15.4

DE = deviance explained; *P-value = 0.

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