Discard analysis and damage assessment in the wedge clam mechanized dredging fisheries of the northern Alboran Sea (W Mediterranean Sea)

Fisheries Research 187 (2017) 58–67

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Discard analysis and damage assessment in the wedge clam mechanized dredging fisheries of the northern Alboran Sea (W Mediterranean Sea) Javier Urra a , Teresa García a,∗ , Helena Gallardo-Roldán b , Estefanía León b , Matías Lozano a , Jorge Baro a , José L. Rueda a a b

Centro Oceanográfico de Málaga, Instituto Espa˜ nol de Oceanografía, Puerto Pesquero s/n, 29640 Fuengirola, Spain Centro Andaluz Superior de Estudios Marinos, Universidad de Cádiz, Polígono Río San Pedro 11510 Puerto Real, Cádiz, Spain

a r t i c l e

i n f o

Article history: Received 5 February 2016 Received in revised form 21 October 2016 Accepted 24 October 2016 Handled by P. He Keywords: Discard Fishing impact Artisanal fisheries Donax trunculus Alboran Sea

a b s t r a c t The composition and structure of discard, as well as the damage caused to target and non-target species, was analyzed in 95 commercial fishing hauls carried out between March 2013 and March 2014 by the mechanized dredging fleet targeting wedge clam (Donax trunculus) in the northern Alboran Sea (southern Spain). A large proportion of the catch (ca. 42% weight) is discarded, mainly wedge clam undersized individuals and non-commercial molluscs, decapods and echinoderms. Total discards within the study period showed a high species richness, with a total of 84 taxa discarded, and biomasses ranging from 337.1 to 8532.5 g haul−1 (1579.9 ± 157.9 g haul−1 , mean ± SE), with maxima in spring. The composition, structure and biomass of discards displayed significant differences among study sites due to differences in the benthic communities of the fishing grounds. Individuals displaying intermediate (intermediate survival chance) and severe (low survival chance) damage in the discard displayed higher values when gravel and bioclastic material was more abundant in the catch. Overall, 15% of the discarded individuals displayed any type of damage, from which 12% were severely damaged, and with Echinoderms displaying the highest mean proportion of damaged individuals (79.5 ± 2.9% of individuals). The target species displayed a high proportion of undamaged individuals to fishing impacts, which may represent an important factor for the maintenance of populations of this commercial species on the fishing grounds. © 2016 Published by Elsevier B.V.

1. Introduction Discards are defined as the portion of the total catch brought on board and then returned to the sea for whatever reason (e.g. unmarketable species, individuals below minimum legal size, etc.) (Kelleher, 2005; Tsagarakis et al., 2013). The incidental capture of non-target species, together with the impact on marine habitats and threatened species, are among the severe ecological effects of commercial fishing, being discard rates highly variable depending on the type of fisheries, and sometimes reaching high values (Kelleher, 2005). An important concern regarding discards relates to the damage caused to individuals during the fishing and the sorting operation on board. This topic is gaining attention worldwide, especially in those fisheries using gears that can cause acute damages on the seafloor components (e.g. trawling fisheries) due to the important implications in terms of conservation, manage-

∗ Corresponding author. E-mail address: [email protected] (T. García). http://dx.doi.org/10.1016/j.fishres.2016.10.018 0165-7836/© 2016 Published by Elsevier B.V.

ment and sustainable use of living resources (Jennings and Kaiser, 1998; Bergmann et al., 2001; Pranovi et al., 2001; Leitão et al., 2009; Lucchetti and Sala, 2012). Artisanal (small scale) fisheries represent one of the main types of fisheries occurring in the Mediterranean Sea, with a high socio-economic importance and a long traditional background (Papaconstantinou and Farrugio, 2000). Nevertheless, mechanized dredges and trawls used in artisanal and trawling fisheries can produce a higher seabed impact than other gears (e.g. trammel nets, gillnets). Trawling fishing gears are designed to catch a complex of target species (e.g. molluscs, flatfishes) generally occurring on the seabed, but they inevitably also catch and damage other organisms that occur in the same fishing grounds, thus even affecting habitat and community structure (Thrush and Dayton, 2002). Despite all this, research has focused mainly on the impact of large scale trawling fisheries usually performed at depths >40 m (e.g. Nephrops and scallop fisheries) on bycatch species (Thrush and Dayton, 2002), and few studies have assessed the impacts of shallow dredging fisheries (e.g. clams fishery) usually carried out at depths <20 m, as it is

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Fig. 1. Map of the study area in the northern Alboran Sea (western Mediterranean Sea), showing the location of the artisanal shellfish hauls analyzed (black circles). Inset: diagram of the fishing technique and detail of the mechanized dredges for capturing wedge clams.

the case of the artisanal fisheries in the southern Iberian Peninsula (Gaspar et al., 2002; Leitão et al., 2009). The wedge clam Donax trunculus Linnaeus, 1758 is one of the most important commercial molluscan species caught by artisanal fisheries in the western Mediterranean Sea and the southern Iberian Peninsula (Gaspar et al., 1999; Tirado et al., 2011). This small bivalve is generally caught in the area with a fishing technique called mechanized dredge, which is currently regulated by different European and Spanish management plans. Nevertheless, there is a lack of scientific information about some aspects of this fishery, which are crucial for a responsible and sustainable management, such as the composition and structure of the catches, the amount and composition of discards, as well as the damage caused to target and non-target species in some Mediterranean coastal areas such as those from the northern Alboran Sea. Because fisheries have a direct impact on the ecosystem (Jennings and Kaiser, 1998; Lucchetti and Sala, 2012), and considering the high bycatch rates of some fisheries (Kelleher, 2005), it is essential to analyze discard composition of fisheries and to assess their impact in order to be able to propose new strategies that could minimize them. In this context, the aims of this study were (1) to study the discard composition of the wedge clam fishery with mechanized dredges carried out in the northern Alboran Sea; (2) to evaluate the impact of this fishery on the benthic-demersal community associated with the fishing grounds; and (3) to analyze the damage caused to bycatch species in relation to different factors linked to this fishery such as the different fishing grounds and seasons. 2. Material & methods 2.1. Study area The study has been conducted in the northern Alboran Sea (W Mediterranean), where mechanized dredges are typically used by

artisanal fishermen targeting bivalves (e.g. D. trunculus, Chamelea gallina, Callista chione, Acanthocardia tuberculata) that inhabit shallow infralittoral soft bottoms (Fig. 1). The mechanized dredge used to catch wedge clams generally weights approximately 80 kg and consists of a rigid iron frame (ca. 1 m length of the dredge mouth) with iron tines that rake the seabed and a net (17–22 mm mesh size) to hold the catch. The dredge has between 20 and 35 teeth with a length of 10 cm and a diameter of 20 mm as well as a number of iron bars that act as ballast. There are also two metal bars welded to the dredge mouth where the towing cable is attached. The study area comprised fishing grounds around the commercial fishing ports of Fuengirola and Caleta de Vélez because an important artisanal fishing fleet with mechanized dredges occurs on them (34 and 40 commercial vessels respectively), representing the ports with the highest sales for wedge clam along the northern Alboran Sea. The commercial vessels targeting wedge clams have lengths from 7 to 11 m, with engines of 15–80 Hp. During fishing, the stern anchor (locally called “gavilán”) is cast and each vessel typically uses four to five sets of dredges simultaneously, which are hauled at low speed (<10 m min−1 ) by a motorized winch, fishing a mean area of 563 m2 (±10 SE). Each fishing operation (i.e. casting the anchor, hauling dredges, collection of target individuals on board, release of discards) takes about 30 min, and it is repeated making concentric lines around the “gavilán” until a circumference is completed (Fig. 1). 2.2. Sample collection Samples were collected from the catches obtained with three commercial vessels with similar characteristics (Table 1) from March 2013 to March 2014, off Fuengirola and Caleta de Vélez (hereafter Caleta) (Fig. 1). Random samples of a standardized weight of 5 kg were collected from the caught material and handled carefully, in order to avoid additional damage, once the target individuals were collected by fishermen and before the

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Table 1 Vessel and dregde characteristics. Information regarding months, sampling days and number of hauls analyzed are also given. Vessel characteristics

Dredge characteristics

Commercial vessel

Length (m)

Power (HP)

Tonnage (in GT)

Mouth length (cm)

Tooth number

Tooth shape

Tooth length (mm)

Tooth thickness (mm)

Tooth spacing (mm)

Mesh size (mm)

El Lele ˜ Nuevo Hermanos Madueno Nuevo Marielva

10.5 7.7 9

80 15 39

6.3 2.43 2

100 80 110

48 21 32

circular plane plane

100 80 80

9.95 20 19

10 12 19

17.5 22 22

2013→

No. of sampling days No. of hauls analized

2014→

March

April

May

June

July

August

September

October

November

December

January

February

March

2 7

2 6

4 17

1 5

1 5

1 7

2 10

2 10

2 8

1 5

– –

1 5

2 9

non-commercial specimens were discarded at sea. Simulated fishing operations with similar commercial vessels were conducted when temporal closures occur due to reproductive periods of the wedge clams (generally between May and June), or during toxic algal blooms that resulted in high shellfish toxins levels in the wedge clam. A total of 95 hauls corresponding to 21 fishing days of different months (based on fishermen availability) throughout an annual cycle were examined in the present study. Data regarding the fishing operation and the commercial catch (catch was weighed [i.e. total wet weight] using hanging analogue scales) was obtained onboard, and collected 5 kg samples were transported carefully to the laboratory on the same day and stored at −20 ◦ C until further processing in the laboratory. Once defrosted, every specimen from each sample was separated, identified to species level (when possible) and quantified (abundance and biomass [±0.1 g wet weight]). Additionally, data regarding the composition and biomass of inorganic (e.g. bioclasts, pebbles) and plant remains (e.g. seagrass, macroalgae, remains of transported terrestrial plants) were also recorded. Damage caused to individuals of commercial and non-commercial species was assessed using a three level scale depending on the damage degree of the taxa: intact, medium and severe damage following criteria listed in Table 2. Damage of different species was expressed in a standardized form as percentage of individuals (i.e. for each analyzed species) within each damage category (Bergmann et al., 2001; Pranovi et al., 2001; Gaspar et al., 2002). The experimental protocol considered the possibility of autotomy by echinoderms and crustaceans as part of the fishing effects.

Fig. 2. Seasonal variation of the commercial catch (composed mainly of D. trunculus) (white columns), the discarded fraction (black columns) and discarded undersized target individuals of the wedge clam (inset grey columns) in the wedge clam fishery with mechanized dredges of the northern Alboran Sea. Mean + SE. Letters above error bars display the results of post-hoc test; different letters distinguish significantly different means at p < 0.05.

(Analysis of Similarity) was carried out for statistical comparisons of groups of samples according to the different factors considered. The SIMPER procedure was used to identify those species that contributed to the dissimilarity between groups of samples. Univariate statistical analyses were performed using SPSS© statistical software, whereas multivariate analyses were performed using PRIMER© software package.

3. Results 2.3. Data analysis 3.1. Catch description The composition of the discarded catch was analyzed for estimating the abundance, weight, dominance index values (percentage of individuals/biomass of a species from the total catch), and frequency index values (percentage of samples in which a species is present) of every discarded species. Catch abundance and biomass were standardized to 15 min haulings (average hauling duration; n = 95), and log (x + 1) transformed when expressed as a percentage. Comparison between catch fractions and damage sustained by discards was performed with a two-factor ANOVA, in order to test the statistical differences regarding sites (i.e. fishing grounds) and seasons, and post hoc tests were used for a posteriori multiple comparisons. A Spearman rank correlation was run to test the relationship between the amounts of hard inert material (e.g. gravels, hard shells) collected and the damage sustained by discard. Multivariate methods using the Bray-Curtis similarity index were carried out for contrasting discard samples of different sites. A fourth root transformation pretreatment was applied on the quantitative data in order to minimize the contribution of the most abundant species to the analysis. The ANOSIM procedure

Each haul was mainly composed of shell remains and gravel, representing up to 60% of the total weight, followed by the commercial catch (23%) and the discarded fraction (17%). The mean total catch (commercial fraction + discards) was 3722.5 ± 191.6 g haul−1 (mean ± SE), and ca. 57.6% belonged to the target species. The discards ratio (discards/total catch by weight) is highly variable depending on the haul, ranging between 0.94 (large discarded fraction) and 0.06 (very low discarded fraction), whereas the overall discard ratio (␴ discards/␴ total catch) for the fishery was 0.82. The commercial catch was composed mainly of the wedge clam, and it displayed slightly but significant higher values in Caleta than in Fuengirola with the maximum biomasses observed in summer (3445.1 ± 334.9 g haul−1 ) (Two-factor ANOVA; Factor site: F = 7.5, p < 0.05; Factor season: F = 18.5, p < 0.005; Interaction: F = 4.1, p < 0.05) (Fig. 2; Table 3). Other commercial species were captured but always in low numbers, such as the bivalves Chamelea gallina, Acanthocardia tuberculata and Callista chione, and the flatfish Pegusa lascaris.

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Table 2 Criteria used for damage assessment of different benthic groups in discards from the mechanized dredge fishery targeting Donax trunculus in the northern Alboran Sea. Taxon

Intermediate damage

Mollusca

Damaged apex (gastropods) or cracked beak/hinge Slightly cracked around the aperture (gastropods) or at the outer lip (bivalves) (bivalves), or high level of fragmentation in shells At least two undamaged arms and disc displaying no No arms and/or crushed disc damage Weak damage in the exoesqueleton or loss of some spines Crushed or pinched exoesqueleton or loss of most spines Body weakly scratched/damaged Fragmented body or highly crushed Presence of at least two pereopods at both sides and one Less than two pereopods per side and/or no chelas, or with chela injured carapace Nearly all individuals are considered severely damaged since it was difficult to distinguish intermediate-severe damage due to different degree of body fragmentation All individuals are considered severely damaged due to their physiological injures caused by air exposure and their low probability of survival

Asteroidea/Ophiuroidea Echinoidea Holoturoidea/Nemertea/Sipunculida Decapoda Annelida Fishes

Severe damage

Table 3 Mean commercial catch and discard abundance and biomass (±SE) regarding main faunistic groups and weight of inert material collected in the wedge clam fishery with mechanized dredges of Fuengirola and Caleta de Vélez (northern Alboran Sea). Site

Fuengirola

Fraction

Abundance (ind. haul−1 )

Biomass (g haul−1 )

Abundance (ind. haul−1 )

Biomass (g haul−1 )

Commercial catch

502.7 (±52.5)

2123.8 (±224.1)

512.1 (±49.5)

2163.4 (±209.1)

454.1 (±50.8)

212.2 (±34.0)

296.9 (±74.2) 3 (±0.4) 118.8 (±39.2) 538.7 (±51.6) 19.8 (±4.1) 1.8 (±0.1) 2.3 (±0.2)

710.5 (±80.1) 5.5 (±1.3) 386.9 (±87.2) 29.4 (±3.4) 594.6 (±179.2) 978.4 (±98.3) 18.3 (±3.8) 16.6 (±2.0) 53.9 (±8.9)

122.3 (±16.6)

347.4 (±54.4) 30.3 (±21.9) 161.8 (±25.2)

19.8 (±6.3) 336.8 (±40.1) 8.5 (±1.8)

35.6 (±13.4) 942.7 (±174.4) 29.3 (±18.6)

1454.1 (±103.2)

4030.1 (±279.7)

2.1 (±0.2) 2.1 (±0.1) 999.5 (±64.4)

65.8 (±13.6) 0.8 (±0.1) 3380.8 (±256.3)

Discarded Fraction: Donax trunculus (target species) Annelids Arthropods Decapods Cnidarians Echinoderms Molluscs Bivalves Molluscs Gastropods Molluscs Cephalopods Fishes Sipunculids Total catch

Caleta de Vélez

Inert material: Gravel Biogenic (shells)

3790.4 (±1830.1) 1322.4 (±229.7)

3868.5 (±567.3) 1814.4 (±331.5)

Table 4 Top-20 dominant and frequent discarded species in the wedge clam fishery with mechanized dredges of Fuengirola and Caleta de Vélez (northern Alboran Sea).%B proportion of the total discarded biomass; %N proportion of the total discarded abundance; %F frequency of occurrence in discards. Species belong to the following taxonomic groups: 1 Class Bivalvia (Mollusca); 2 Order Decapoda (Crustacea); 3 Class Echinoidea (Echinodermata); 4 Class Ophiuroidea (Echinodermata); 5 Class Gastropoda (Mollusca). Site

Fuengirola

Species Donax trunculus Linnaeus, 17581 Paguroidea2 Echinocardium cf. mediterraneum (Forbes, 1844)3 Chamelea gallina (Linnaeus, 1758)1 Portumnus latipes (Pennant, 1777)2 Liocarcinus vernalis (Risso, 1816)2 Tellina tenuis da Costa, 17781 Mactra stultorum (Linnaeus, 1758)1 Ophiura ophiura (Linnaeus, 1758)4 Nassarius reticulatus (Linnaeus, 1758)5 Ensis minor (Chenu, 1843)1 Donax vittatus (da Costa, 1778)1 Mactra glauca Born, 17781 Donax semistriatus Poli, 17951 Acanthocardia tuberculata (Linnaeus, 1758)1 Acrocnida brachiata (Montagu, 1804)4 Donax intermedia1 Spisula subtruncata (da Costa, 1778)1 Dosinia lupinus (Linnaeus, 1758)1 Nassarius granum (Lamarck, 1822)5

%N 47.8 25.5 9.3 1.9 1.9 3.5 2.4 0.6 0.8 1.1 0.8 0.8 0.6 0.3 0.1 0.3 0.2 0.1 0.2 0.2

3.2. Discarded fraction The discarded fraction was composed by 84 taxa, however the number of species should even be even higher because Paguroidea (Crustacea) and Annelida could not be identified to species level. Discards were dominated by molluscs (62% of total biomass and

Caleta de Vélez %B 37.3 13.5 25.7 2.9 0.9 4.1 0.7 1.8 0.2 0.5 1.6 0.7 2.7 0.2 2.2 0.1 0.2 0.1 0.3 0.03

%F 100 96 58 78 96 92 68 54 44 66 52 28 6 30 26 32 24 22 26 30

%N 44.5 15.0 1.7 15.3 6.8 3.2 1.2 4.4 1.9 1.1 1.0 0.4 0.04 0.3 0.6 0.1 0.2 0.5 0.2 0.1

%B 29.5 6.7 2.2 24.9 2.5 3.5 0.3 11.9 0.3 0.5 1.0 0.3 0.3 0.2 8.9 0.01 0.2 0.3 0.2 0.02

%F 100 100 58 93 98 98 47 89 64 58 71 40 9 40 36 18 22 44 22 24

individuals respectively), decapods (17.7% and 29.3%) and echinoderms (17.6% and 8.4%). Other taxa displayed lower dominances (<3% of the biomass and individuals) such as fishes, annelids (polychaetes) and sipunculids. Each haul displayed a mean of 14 ± 1 species (spp.) haul−1 and 731 ± 60 individuals (ind.) haul−1 that weighed 1579.9 ± 157.9 g haul−1 . Bivalvia displayed the highest

29.4 (±6.8) 185.1 (±30.6) 1.8 (±0.2) 59.6 (±7.1) 31.7 (±7.5) 24.4 (±3.8) 1204.2 (±274.2) 1421.8 (±175.0) 823.2 (±93.1)

25.2 (±6.2)

54.9 (±14.7)

16.6 (±1.9) 38.7 (±6.9) 550.7 (±212.1) 1.8 (±0.1) 2.5 (±0.2) 105.2 (±30.9)

455.4 (±52.6)

34.3 (±8.3) 31.6 (±8.4) 26.8 (±12.5) 97.8 (±16.3) 23.6 (±7.4) 6.2 (±1.6) 0.7 (±0.4) 12.9 (±2.3) 10.2 (±3.4) 2.1 (±1.7) 36.8 (±11.1) 13.5 (±5.2) 3.1 (±1.8) 0.4 (±0.3) 15.1 (±2.1) 10.3 (±5.6) 1.1 (±0.6) 0.4 (±0.3)

Biomass Abundance Biomass Abundance

13.6 (±3.1) 19.8 (±3.1) 9.3 (±5.3) 29.8 (±4.3) 325.8 (±52.5) 110.8 (±18.6) 4.1 (±1.3) 1082.3 (±274.1) 9.2 (±2.1)

Biomass Abundance

208.4 (±33.7) 92.6 (±16.7) 0.9 (±0.2) 355.1 (±52.8) 8.6 (±1.8) 18.9 (±4.6) 34.8 (±9.5) 539.1 (±217.0) 48.1 (±9.1)

Biomass Abundance Biomass

705.5 (±81.5) 338.0 (±87.1) 154.1 (±58.6) 940.9 (±96.5) 18.1 (±3.7)

Donax trunculus Arthropoda Decapods Echinoderms Mollusca Bivalves Mollusca Gastropods Mollusca Cephalopods Fishes Total

Biomass Abundance

457.8 (±52.7) 264.2 (±74.1) 29.0 (±11.1) 520.3 (±52.4) 19.4 (±4.1)

Discarded Fraction

Abundance

6.9 (±1.6) 18.2 (±2.2) 79.5 (±33.6) 18.9 (±3.9)

Intermediate damage No damage

Caleta de Vélez

Severe damage No damage

Intermediate damage Fuengirola

Overall, 84.9% of the discarded individuals were undamaged, 3.4% displayed intermediate damage and 11.6% displayed severe damage including fishes and cephalopods (100% ind.) and bivalves with fragile shells such as razor clams (ca. 80%). Discard displayed an overall higher damage level in Caleta than in Fuengirola for both the intermediate damage (6.2% vs. 3.3%) and the severe damage (14.2% vs. 11.5%), with the highest proportion of intermediate damage observed in spring (7.2%) (Two-factor ANOVA; Factor site: F = 14.9, p < 0.005; Factor season: F = 4.4, p < 0.05; Interaction: F = 4.5, p < 0.05), and of severe damage in autumn (17.4%) (Twofactor ANOVA; Factor site: F = 2.2, p > 0.05; Factor season: F = 5.3, p < 0.005; Interaction: F = 4.5, p < 0.05). In general, a slight but significant increase of the proportion of damaged individuals was observed in those hauls with a higher content of gravel and hard shells (rs = 0.4, p < 0.005). Considering the proportion of damaged individuals within each category and site, the highest differences were observed for severe damage, with echinoderms dominating at Fuengirola (>70% of total abundance and biomass) and molluscs at Caleta (>45%) (Fig. 3; Table 5). Regarding faunistic groups, echinoderms displayed the highest mean proportion of damaged individuals (79.5%), with an average of more than 40% showing severe damage in both sites and displaying significant maxima in autumn (65.1% ind.) (Two-factor ANOVA; Factor site: F = 1.2, p > 0.05; Factor season: F = 5.7, p < 0.005; Interaction: F = 3.6, p < 0.05). The most severely damaged echinoderms were E. cf. mediterraneum (76% ind. presenting crushed exoskeletons), and the brittle stars O. ophiura and A. brachiata (nearly 80% ind. with intermediate damage for each species; ca. 5% and 7% ind. with severe damage respectively) (Fig. 4). The proportion of damaged individuals of these species was high throughout the year, with maxima in different seasons and in some cases displaying significant spatio-seasonal differences (Fig. 5A–C; Table 6). Decapods displayed similar values of damaged individuals in both sites (Table 5), with the highest level of severe damage in winter (27.9% ind.) (Two-factor ANOVA; Factor site: F = 0.7, p > 0.05; Factor season: F = 4.1, p < 0.05; Interaction: F = 0.7, p > 0.05). Overall, this group showed the highest level of intermediate damage in both sites (Fig. 3), with L. vernalis and P. latipes displaying the highest proportion of damaged individuals (41.1% and 34.7% ind. with severe damage respectively) (Figs. 4, 5D–E), being this proportion significantly higher in Caleta for L. vernalis (Table 6).

Type of damage

3.3. Damage to discarded species

Site

number of species (29 spp.) (Table 4), and undersized target individuals of the wedge clam represented the highest discarded biomass (34.4%) and abundance (46.7%). Discard displayed significant differences in the faunistic composition and structure among sites (abundance: RANOSIM = 0.16, p < 0.001; biomass: RANOSIM = 0.12, p < 0.001) and among seasons (abundance: RANOSIM = 0.14, p < 0.001; biomass: RANOSIM = 0.12, p < 0.001). Regarding biomass, discard displayed significant spatial and temporal differences (Two-factor ANOVA; Factor site: F = 5.7, p < 0.05; Factor season: F = 4.2, p < 0.05; Interaction: F = 0.9, p > 0.05), with maximum values in Fuengirola (Table 3) and in spring (2209.4 ± 381.9 g haul−1 ). These spatial differences (SIMPER: average dissimilarity = 48.9%) were mainly related to the higher discarded biomass of the bivalves C. gallina and Mactra stultorum and the ophiuroid Ophiura ophiura in Caleta, and of E. cf. mediterraneum, Paguroidea and L. vernalis in Fuengirola. Results were very similar when considering abundance data (SIMPER: average dissimilarity = 47.1%). The discarded fraction belonging to the target species was significantly higher in Fuengirola than in Caleta in relation to the abundance (Two-factor ANOVA; Factor site: F = 5.5, p<0.05; Factor season: F = 2.6, p > 0.05; Interaction: F = 0.9, p > 0.05), and mean values were slightly higher in summer (Fig. 2; Table 3).

Severe damage

J. Urra et al. / Fisheries Research 187 (2017) 58–67 Table 5 Mean abundance (ind haul−1 ) and biomass (g haul−1 ) (±SE) of the undamaged and damaged discarded fractions of dominant fauna in the wedge clam fishery with mechanized dredges of Fuengirola and Caleta de Vélez (northern Alboran Sea).

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Fig. 3. Composition of discarded catch of wedge clam fisheries with mechanized dredges in relation to site and damage category. Percentages calculated as number or weight of individuals from each group from the total belonging to each damage category.

Fig. 4. Proportion of individuals displaying no damage (white columns) as well as intermediate (grey columns) and severe damage (black columns) for the most abundant discarded species in Fuengirola (A) and Caleta de Vélez (B) (northern Alboran Sea).

Only 9.3% of the molluscs displayed any type of damage, being mostly bivalves with severe damage (Fig. 3). The proportion of severely damaged individuals was significantly higher in Caleta

(12.4% vs. 4.9%) (Two-factor ANOVA; Factor site: F = 6.9, p < 0.05; Factor season: F = 2.1, p > 0.05; Interaction: F = 5.8, p < 0.005). The highest mean proportion of severely damaged individuals was

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Fig. 5. Seasonal variation of abundance (N: solid bars) and proportion of damaged individuals (intermediate and severe) (%N: empty bars) for the most abundant discarded species. Mean + standard error. Letters above error bars display the results of post-hoc test; different letters distinguish significantly different means at p < 0.05.

Table 6 Two-factor ANOVA analyses for testing differences in the proportion of damaged individuals in relation to seasons (summer, autumn, winter, spring) and sites (Fuengirola, Caleta de Vélez). Source of variation

n

Echinocardium cf. mediterraneum Seasons Sites Seasons*Sites Error

95

Ophiura ophiura Seasons Sites Seasons*Sites Error

95

Liocarcinus vernalis Seasons Sites Seasons*Sites Error

95

Donax trunculus Seasons Sites Seasons*Sites Error

95

Ensis minor Seasons Sites Seasons*Sites Error

95

Mactra stultorum Seasons Sites Seasons*Sites Error

95

df

SS

MS

F

p

3 1 3 87

6.80 0.33 7.90 66.77

2.27 0.33 2.63 0.77

2.96 0.43 3.43

<0.05 >0.05 <0.05

3 1 3 87

9.53 9.62 0.57 75.76

3.18 9.62 0.19 0.87

3.65 11.04 0.22

<0.05 <0.005 >0.05

3 1 3 87

0.98 0.96 3.52 25.44

0.33 0.96 1.17 0.29

1.12 3.29 4.01

>0.05 >0.05 <0.05

3 1 3 87

2.29 4.34 3.58 14.27

0.76 4.34 1.19 0.16

4.66 26.46 7.28

<0.05 <0.005 <0.005

3 1 3 87

6.79 4.29 6.77 70.33

2.26 4.29 2.26 0.81

2.80 5.30 2.79

<0.05 <0.05 <0.05

3 1 3 87

1.87 14.98 1.35 41.90

0.62 14.98 0.45 0.48

1.29 31.11 0.93

>0.05 <0.005 >0.05

J. Urra et al. / Fisheries Research 187 (2017) 58–67

observed for E. minor (79.2%), M. stultorum (33.9%) and Tellina tenuis (15.6%), with maxima in spring and winter (Fig. 5G–I; Tables 4 and 6), whereas only 6.4% of the discarded wedge clam was damaged, mainly in Caleta and especially in spring (Fig. 5F; Tables 5 and 6). Regarding less dominant taxa, nearly all annelids were fragmented or highly crushed, and several fishes had a large amount of scales missing and sometimes severe wounds (fragmented body) (e.g. Ophidion rochei, Trachinus draco). Nevertheless most fishes remained on the deck for at least 20 min and they were dead when released to the sea.

4. Discussion The discards generated by wedge clam fisheries in the northern Alboran Sea showed a high biodiversity (84 spp., of which 5 are of commercial interest), with the dominant species corresponding to components of the “Sables Fins Bien Calibrés” biocoenosis (well-sorted fine sands) defined for the Mediterranean Sea by Pérès and Picard (1964). Although comparisons are not easy since the available information is very limited, the dominant species in the northern Alboran Sea are similar to those observed in the eastern Adriatic Sea (Vaccarella et al., 1998). Nevertheless, the higher species richness values documented here (84 spp. vs. 12 spp) reflects the high biodiversity of the faunistic communities associated with shallow sedimentary habitats of the northern Alboran Sea, partly due to the confluence of fauna from different biogeographical regions (García Raso et al., 2010; Gallardo-Roldán et al., 2015). The commercial catch and the structure of discards are probably related to different habitat characteristics. The studied soft bottoms are composed mainly by fine sands in Fuengirola, and by fine and medium sands in Caleta de Vélez, with different mud and organic matter contents (Sanz et al., 2007; Urra et al., 2011), resulting in different facies of the well sorted fine sand community. Spatial differences in discard composition were also reported by Pranovi et al. (2001) when analyzing discards of the Rapido trawl fishery from the northwestern Adriatic Sea, and they were always related to differences of the benthic communities due to different environmental settings. Furthermore, the artisanal fleet operates in Fuengirola at a mean depth of ca. 2.9 m and in Caleta de Vélez at ca. 3.3 m. Despite this small difference, the wedge clam has been reported to display a depth segregation phenomenon with larger individuals situated at greater depths down to their bathymetric limit (4–5 m) (Gaspar et al., 1999; Manca Zeichen et al., 2002), and this could promote the higher commercial catches observed in Caleta. The overall discard ratio of the analyzed wedge clam fishery was close to one, reflecting the high proportion of discard generated by this fishery, which represented the 42.4% of the total catch (i.e. commercial catch + discard), approximately 34% of which was composed of small individuals of the target species and the rest corresponded to non-commercial species, which were released to the sea. These values are comparable to those reported by Morello et al. (2005) for the hydraulic dredging fleet targeting C. gallina (3–12 m depth) in the western Adriatic Sea (Italy), where it was emphasized the occurrence of high proportions of discards (ca. 50%). A similar pattern was found by Hauton et al. (2003) who reported average commercial landings of <30% of total catch from hydraulic dredging fisheries targeting Ensis spp. in the Clyde Sea (Scotland). On the other hand, Pranovi et al. (2001) reported very different discard/commercial ratios as well as contrasting selectivity values for Rapido trawl fisheries in the northern Adriatic Sea (Italy), being of 87% when targeting Aequipecten opercularis and of 10% for Pecten jacobeus. This high variability was attributed to differences in the habitat and the associated community, the spatial

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distribution of the target species and the result of over-exploitation (Pranovi et al., 2001). In the case presented here, the target species exhibited a large-scale of patchiness, reflected by the highly variable discard/total catch ratios per haul. This type of fishery can have a potential high impact on benthic fauna and habitats, as fishermen are forced to repeat the fishing operation as many times as needed to get an economically profitable amount of the target species, which is of importance considering the bathymetricalnarrow coastal area where the wedge clam inhabits (Gaspar et al., 2002; Gofas et al., 2011). The higher catches and discards of the wedge clam were observed in spring and summer months, coinciding with the highest fishing activity due to the touristic demand in those months and of higher reproductive activity (with high juvenile density) that takes place along the northwestern Alboran coasts between April and September (Tirado and Salas, 1998). The present study redisplays the importance of this period of the year for the reproductive processes (close season in fishing grounds of the northern Alboran Sea are established in May-June) of the wedge clam in this area of southern Europe. In relation to the significant seasonal differences observed in the structure of discard, some of the species analyzed showed a marked seasonality that could be related to their biology and ecology (e.g. reproductive or feeding strategies). In this line, food availability can influence a higher collection of the species during specific seasons, as could be the case of the deposit feeders O. ophiura and T. tenuis and the carnivorous L. vernalis in Caleta. The former two species reached high discarded abundances in autumn, which could be linked to a higher amount of organic particles coming from close rivers during the rainy season (September-February), as previously observed for other bivalve species (Urra et al., 2013). On the other hand, the benthic community structure in areas with a long fishing history is usually dominated by small opportunistic predators/scavengers (Tillin et al., 2006), and this could be the case for some highly abundant detritivore echinoderms such as E. cf. mediterraneum and O. ophiura, and for scavengers such as Paguridae decapods and Nassaridae gastropods. In the case of the dominant species P. latipes, the higher abundances were observed in winter in Caleta, which coincide with a period of high feeding activity and the spawning season (Chartosia et al., 2010). This could be related to a migration to shallow areas for feeding or spawning, benefiting from the recruitments occurred during the summer season for a large number of species, including the wedge clam. The analyzed fishing fleet have showed to cause a direct impact to nearly 15% of the collected individuals, with 12% of them displaying severe damage. Gaspar et al. (2002) reported a very low mean percentage of both damaged and dead individuals of the overall catch from some Portuguese shallow clam dredge fisheries, such as those targeting Spisula solida (8–10 m depth). Molluscs, specially gastropods, and hermit crabs were the most resistant taxa to the effects of mechanized dredges due to the efficient and strong protection provided by shells, as observed previously in different fisheries (Hall-Spencer et al., 1999; Bergmann et al., 2001; Pranovi et al., 2001; Gaspar et al., 2002). The target species showed a low proportion of damaged individuals, similar to other commercial (e.g. C. gallina, C. chione) and non-commercial molluscs (e.g. Spisula subtruncata). The resistance of molluscs to fishing gears and handling of the bycatch on board varies depending on the shell morphometrics (round vs. long forms, size) and strength of each species (Kaiser and Spencer, 1995; Bergmann et al., 2001; Pranovi et al., 2001; Vasconcelos et al., 2011), enabling the survival of molluscs for several hours or even days (Vasconcelos et al., 2011). A high resistance of the target species, both the adults and undersized individuals, to the fishing gears used for their collection is essential for maintaining populations of these commercial species in the fishing grounds where artisanal fleets operate, as it is the case observed here. In the case of hermit crabs, their resistance

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to fisheries could promote a high dominance in these bottoms, where they can find an additional food source from discarded damaged and dead organisms (Ramsay et al., 1997). The absence of any damage in exoskeletons and vital systems of discarded species promotes their survival once they are returned to the sea (Kaiser and Spencer, 1995), being higher if they are released in a short time and on similar original habitats, as occur in the wedge clam fishery of the northern Alborán Sea. Nevertheless, some authors have reported that there is a potential for high levels of mortality in discarded individuals at every level of damage, even when they are undamaged (Bergmann and Moore, 2001a,b). Therefore caution must be taken when evaluations and conclusions are made for apparently low-damaging fisheries, as post-trawling mortality of discarded individuals has usually been underestimated in the past. The amount of gravel and hard shells collected together with the catch determine partly the impact and damage on both the target species and discard. In this line, an overall higher degree of damage was observed in those sites with a higher component of gravel and hard shells, with significant spatial differences in the proportion of intermediate and severely damaged individuals. Pranovi et al. (2001) reported that an important factor to consider is the catch volume, including inert material as hard shells, as these components macerate the catch during hauling and can damage many species with soft bodies or vulnerable shells or exoskeletons. The higher sediment movement caused by stronger currents and storms in autumn and winter could explain the significant higher damage level observed in this time of the year. Nevertheless, temporal differences in the proportion of damaged individuals could be also related to the biology of species (e.g. molt in decapods, lack of biomineralization during certain periods), their behavior (e.g. bathymetric migrations linked to reproductive strategies) or to the fishing operation (e.g. higher probability of recapturing damaged individuals, long periods of aerial exposure on deck) (Kaiser, 1996; Bergmann et al., 2001). Echinoderms (mainly ophiuroids and asteroids) and decapods showed the highest proportions of damage (broken arms and damaged disc in echinoderms, loss of chelas and/or pereiopods and crushed carapace in decapods), because of their fragile morphology with arms and appendages that are easy to lose (Kaiser, 1996; Bergmann and Moore, 2001a,b; Pranovi et al., 2001), and their autotomize capacity (i.e. self-amputate) when subjected to stress (McVean, 1982; Wilkie, 2001). Despite their regenerative capacity, which could potentially support their recuperation to the impact of mechanized dredges, post-fishing survival is affected by a high range of factors (e.g. hypoxia due to long after-catch sorting times, temperature and irradiance changes, physical damage due to handling). Moreover, discarded injured individuals may be more susceptible to predation and infection and are likely to be less competitive in resource acquisition, which would involve a low in situ survival (Bergmann and Moore, 2001a,b and references therein). The species that usually presented this type of damage are somewhat similar to those reported for different trawling and dredging fisheries (Kaiser and Spencer, 1995; Bergmann et al., 2001; Pranovi et al., 2001; Gaspar et al., 2002), and included mobile species (e.g. Astropecten spp., O. ophiura, Portumnus spp.) that sometimes are widely distributed and not restricted to a certain type of sediment, which promote similarities between study areas. The resistance of the target species to mechanized dredges promotes the maintenance of their populations in the fishing grounds of the northern Alboran Sea.

Funding This study was developed under the collaboration agreement ˜ de between the Junta de Andalucía (Spain) and Instituto Espanol

Oceanografía (IEO) (Contract 126/2012-SEN), within the framework of the research project entitled “Estudio integral en zonas de protección pesquera y marisquera y otras áreas marinas protegidas del litoral andaluz: Estudio previo para la protección, ordenación y determinación de reservas marisqueras en el litoral mediterráneo de Andalucía” (REMAN-REMARAN). This project was funded by the European Fisheries Fund. Acknowledgements We really thank the captains and crew of the commercial vesno and El Lele, who sels Nuevo Marielva, Nuevo Hermanos Madue˜ have collaborated with the REMARAN team; to Ana Garrido, Ale˜ Yuste and Alejando Terrón Sigler (AGAPA-Junta de jandro J. Ibanez Andalucía) for the collection of faunistic samples and continuous interest; to Alba Rojas García, Blanca Orúe Montaner and Marina ˜ Gallardo Núnez for their help in processing the samples; to José Miguel Serna (Centro Oceanográfico de Málaga) for his help with the GIS facilities and other members of the research team for their collaboration. References Bergmann, M., Moore, P.G., 2001a. Mortality of Asterias rubens y Ophiura Ophiura discarded in the Nephrops fishery of the Clyde Sea area, Scotland. ICES J. Mar. Sci. 58, 531–542. Bergmann, M., Moore, P.G., 2001b. Survival of decapods crustaceans discarded in the Nephrops fishery of the Clyde Sea area, Scotland. ICES J. Mar. Sci. 58, 163–171. Bergmann, M., Beare, D.J., Moore, P.G., 2001. Damage sustained by epibenthic invertebrates discarded in the Nephrops fishery of the Clyde Sea area, Scotland. J. Sea Res. 45, 105–118. Chartosia, N., Kitsos, M.S., Koukouras, A., 2010. Seasonal diet of Portumnus latipes (Pennant, 1777) (Decapoda, portunidae). Crustaceana 83 (9), 1101–1113. Gallardo-Roldán, H., Urra, J., García, T., Lozano, T., Antit, M., Baro, J., Rueda, J.L., 2015. First record of the starfish Luidia atlantidea Madsen, 1950 in the Mediterranean Sea, with evidence of persistent populations. Cah. Biol. Mar. 56, 263–270. ˜ García Raso, J.E., Gofas, S., Salas, C., Manjón-Cabeza, M.E., Urra, J., García Munoz, J.E., 2010. El mar más rico de Europa: Biodiversidad del litoral occidental de Málaga entre Calaburras y Calahonda. Consejería de Medio Ambiente, Junta de Andalucía. Sevilla. Gaspar, M.B., Ferreira, R., Monteiro, C.C., 1999. Growth and reproductive cycle of Donax trunculus L., (Mollusca Bivalvia) off Faro, southern Portugal. Fish. Res. 41, 309–316. Gaspar, M.B., Leitão, F., Santos, M.N., Sobral, M., Chícharo, L., Chícharo, A., Monteiro, C.C., 2002. Influence of mesh size and tooth spacing on the proportion of damaged organisms in the catches of the Portuguese clam dredge fishery. ICES J. Mar. Sci. 59, 1228–1236. Gofas, S., Moreno, D., Salas, C., 2011. Moluscos marinos de Andalucía. Servicio de Publicaciones e Intercambio Científico. Universidad de Málaga, Málaga. Hall-Spencer, J.M., Froglia, C., Atkinson, R.J.A., Moore, P.J., 1999. The impact of Rapido trawling for scallops, Pecten jacobaeus (L), on the benthos of the Gulf of Venice. ICES J. Mar. Sci. 56, 111–124. Hauton, C., Atkinson, R.J.A., Moore, P.G., 2003. The impact of hydraulic blade dredging on a benthic megafaunal community in the Clyde Sea area, Scotland. J. Sea Res. 50, 45–56. Jennings, S., Kaiser, M.J., 1998. The effects of fishing on marine ecosystems. Adv. Mar. Biol. 34, 201–352. Kaiser, M.J., Spencer, B.E., 1995. Survival of bycatch from a beam trawl. Mar. Ecol. Prog. Ser. 126, 31–38. Kaiser, M.J., 1996. Starfish damage as an indicator of trawling intensity. Mar. Ecol. Prog. Ser. 134, 303–307. Kelleher, K., 2005. Discards in the world’s marine fisheries. An update. FAO Fisheries Technical Paper No. 470. Leitão, F., Gaspar, M.B., Santos, M.N., Monteiro, C.C., 2009. A comparison of bycatch and discard mortality in three types of dredge used in the Portuguese Spisula solida (solid surf clam) fishery. Aquat. Living Resour. 22, 1–10. Lucchetti, A., Sala, A., 2012. Impact and performance of Mediterranean fishing gear by side-scan sonar technology. Can. J. Fish. Aquat. Sci. 69, 1806–1816. Manca Zeichen, M., Agnesi, S., Mariani, A., Maccaroni, A., Ardizzone, G.D., 2002. Biology and population dynamics of Donax trunculus L. (Bivalvia: Donacidae) in the South Adriatic Coast (Italy). Estuar. Coast. Shelf Sci. 54, 971–982. McVean, A., 1982. Autotomy. In: Bliss, D.E. (Ed.), In The Biology of Crustacea, vol. 4. Academic Press, New York, pp. 107–132. Morello, E.B., Froglia, C., Atkinson, R.J.A., Moore, P.G., 2005. Hydraulic dredge discards of the clam (Chamelea gallina) fishery in the western Adriatic Sea, Italy. Fish. Res. 76, 430–444. Pérès, J.M., Picard, J., 1964. Nouveau manuel de bionomie benthique de la Mer Mediterranée. Recl. Trav. Sta. Mar. d’Endoume 31, 5–137.

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