Discards regulation vs Mediterranean fisheries sustainability
M. Demestre and F. Maynou (eds)

INTRODUCTIONTop

The impact of the fishing activity on non-target species or bycatch species, together with overexploitation of target species and impacts on habitats, is considered one of the main problems of marine ecosystems (Dulvy et al. 2003Dulvy N.K., Sadovy Y., Reynolds J.D. 2003. Extinction vulnerability in marine populations. Fish Fish. 4: 25-64., Kappel 2005Kappel C.V. 2005. Losing pieces of the puzzle: threats to marine, estuarine, and diadromous species. Front. Ecol. Environ. 3: 275-282., Shester and Micheli 2011Shester G.G., Micheli F. 2011. Conservation challenges for small-scale fisheries: bycatch and habitat impacts of traps and gillnets. Biol. Conserv. 144: 1673-1681.). At a global level, bycatch has been estimated at 27 million t per year (Alverson et al. 1994Alverson D.L., Freeber M.H., Murawski S.A., et al. 1994. A global assessment of fisheries bycatch and discards. FAO Fish. Tech. Pap. 339: 1-233.), but more recently Kelleher (2005)Kelleher K. 2005. Discards in the world’s marine fisheries: an update. FAO Fish. Tech. Pap. 470: 1-134. estimated worldwide discards at an average of 7.3 million t per year. Increasing awareness of the potential impacts of such high levels of unwanted catch on marine ecosystems is becoming an issue of global importance (Stobutzki et al. 2001Stobutzki I., Miller M., Brewer D. 2001. Sustainability of fishery bycatch: a process for assessing highly diverse and numerous bycatch. Environ. Conserv. 28: 167-181., Bellido et al. 2011Bellido J.M., Santos M.B., Pennino M.G., et al. 2011. Fishery discards and bycatch: solutions for an ecosystem approach to fisheries management? Hydrobiologia 670: 317-333.).

Small-scale fisheries have often been described as more selective and more sustainable than industrial fisheries (Chuenpagdee et al. 2006Chuenpagdee R., Liguori L., Palomares M.L.D., et al. 2006. Bottom-up, global estimates of small-scale marine fisheries catches. Fisheries Centre Research Reports, University of British Columbia 14: 1-110., Jacquet and Pauly 2008Jacquet J., Pauly D. 2008. Funding priorities: big barriers to small-scale fisheries. Conserv. Biol. 22: 832-835., Zimmerhackel et al. 2015Zimmerhackel J.S., Schuhbauer A.C., Usseglio P., et al. 2015. Catch, bycatch and discards of the Galapagos Marine Reserve small-scale handline fishery. PeerJ 3: e995.). However, the bycatch level in small-scale fisheries can cause major ecological impacts and, when scaled to per-unit of total catches, be comparable to that in industrial fisheries (Bellido et al. 2011Bellido J.M., Santos M.B., Pennino M.G., et al. 2011. Fishery discards and bycatch: solutions for an ecosystem approach to fisheries management? Hydrobiologia 670: 317-333., Shester and Micheli 2011Shester G.G., Micheli F. 2011. Conservation challenges for small-scale fisheries: bycatch and habitat impacts of traps and gillnets. Biol. Conserv. 144: 1673-1681., Zimmerhackel et al. 2015Zimmerhackel J.S., Schuhbauer A.C., Usseglio P., et al. 2015. Catch, bycatch and discards of the Galapagos Marine Reserve small-scale handline fishery. PeerJ 3: e995.).

In view of these findings, two priority goals emerge: a) to determine and reduce the impact of fishing activity on bycatch species, and b) to find a selective gear that minimizes the capture of non-target species. These goals are of particular importance when the fishing activity is focused on shrimp species, for which the biomass discarded is higher than the marketable biomass (33.0% of all world fishery discards) (Alverson et al. 1994Alverson D.L., Freeber M.H., Murawski S.A., et al. 1994. A global assessment of fisheries bycatch and discards. FAO Fish. Tech. Pap. 339: 1-233., Stobutzki et al. 2001Stobutzki I., Miller M., Brewer D. 2001. Sustainability of fishery bycatch: a process for assessing highly diverse and numerous bycatch. Environ. Conserv. 28: 167-181., Bellido et al. 2011Bellido J.M., Santos M.B., Pennino M.G., et al. 2011. Fishery discards and bycatch: solutions for an ecosystem approach to fisheries management? Hydrobiologia 670: 317-333.), and attaining them will help the search for alternatives to bottom trawling.

Continental shelves are among the richest ecosystems of the sea (e.g. Stobutzki et al. 2001Stobutzki I., Miller M., Brewer D. 2001. Sustainability of fishery bycatch: a process for assessing highly diverse and numerous bycatch. Environ. Conserv. 28: 167-181.), supporting more than 95.0% the world’s fisheries (Pauly and Christensen 1995Pauly D., Christensen V. 1995. Primary production required to sustain global fisheries. Nature 374: 255-257., Pauly 2008Pauly D. 2008. Global fisheries: a brief review. J. Biol. Res. 9: 3-9., Sadovy et al. 2013Sadovy Y., Craig M.T., Bertoncini A.A., et al. 2013. Fishing groupers towards extinction: a global assessment of threats and extinction risks in a billion dollar fishery. Fish Fish. 14: 119-136.), so they are among the marine ecosystems with the clearest signs of overexploitation. Although subjected to a lower fishing intensity, deep ecosystems, including the ones on the slope, are extremely sensitive to fishing activity (Cartes et al. 2007Cartes J.A., Serrano A., Velasco F., et al. 2007. Community structure and dynamics of deep-water decapod assemblages from Le Danois Bank (Cantabrian Sea, NE Atlantic): Influence of environmental variables and food availability. Progr. Oceanog. 75: 797-816., Pajuelo et al. 2010Pajuelo J.G., González J.A., Santana J.I. 2010. Bycatch and incidental catch of the black scabbardfish (Aphanopus spp.) fishery off the Canary Islands. Fish. Res. 106: 448-453., 2016Pajuelo J.G., Seoane J., Biscoito M., et al. 2016. Assemblages of deep-sea fishes on the middle slope off Northwest Africa (26°-33°N, Eastern Atlantic). Deep-Sea Res. I 118: 66-83.), and bycatch has become a major conservation issue (Harrington et al. 2005Harrington J.M., Myers R.A., Rosenberg A.A. 2005. Wasted fishery resources: discarded by-catch in the USA. Fish Fish. 6: 350-361.).

Since 1975 shrimp species of the Plesionika genus have been fished with highly selective semi-floating shrimp traps operating between 100 and 500 m depth throughout the Mediterranean Sea (González et al. 1992González J.A., Carrillo J., Santana J.I., et al. 1992. La pesquería de Quisquilla, Plesionika edwardsii (Brandt, 1851), con tren de nasas en el Levante español. Ensayos a pequeña escala en Canarias. Inf. Tec. Sci. Mar. 170: 1-31., García-Rodríguez et al. 2000García-Rodríguez M., Esteban A., Pérez Gil J.L. 2000. Considerations on the biology of Plesionika edwardsii (Brandt, 1851) (Decapoda, Caridea, Pandalidae) from experimental trap catches in the Spanish western Mediterranean Sea. Sci. Mar. 64: 369-379.). Since 1997 (González 1997González J.A. 1997. Transferencia de tecnología a la flota artesanal canaria y desarrollo de nuevas pesquerías de camarones profundos. Instituto Canario de Ciencias Marinas, Gobierno de Canarias. Telde, Las Palmas, 69 pp.), this fishery has expanded to the northeastern Atlantic islands, where a small-scale fishery developed, first in the Canary archipelago (González et al. 2001González J.A., Quiles J.A., Tuset V.M., et al. 2001. Data on the family Pandalidae around the Canary Islands, with first record of Plesionika antigai (Caridea). Hydrobiologia 449: 71-76.) and many years later in Madeira (González et al. 2016González J.A., Pajuelo J.G., Triay-Portella R., et al. 2016. Latitudinal patterns in the life-history traits of three isolated Atlantic populations of the deep-water shrimp Plesionika edwardsii (Decapoda, Pandalidae). Deep-Sea Res. I 117: 28-38.). Only experimental fishing has been conducted around Cape Verde to date. However, the development of these fisheries has not been monitored and information on its impact on target and non-target species (in particular sharks) has not been available.

To bridge this gap, a research programme was developed to evaluate the composition of the catch of the shrimp fishery with semi-floating traps off Madeira, the Canary Islands and Cape Verde. Of particular interest was the bycatch of top predators because of their importance for ecosystem functioning (Pajuelo et al. 2010Pajuelo J.G., González J.A., Santana J.I. 2010. Bycatch and incidental catch of the black scabbardfish (Aphanopus spp.) fishery off the Canary Islands. Fish. Res. 106: 448-453.). In addition, the quantification and diversity of bycatch species is relevant for the current fisheries policy of the European Union, which aims to reduce the catches of some species groups to zero over a short period (Clarke 2009Clarke M.W. 2009. Sharks, skates and rays in the northeast Atlantic: population status, advice and management. J. Appl. Ichthyol. 25: 3-8.). A second objective of this study was to evaluate the behaviour of the fishing system at different levels of ecosystem exploitation.

MATERIALS AND METHODSTop

Sample procedures

Fishing operations (n=90) were done during six research cruises (15 fishing operations each) carried out in the Madeira (n=30), the Canary (n=30) and Cape Verde (n=30) archipelagos, to compare the composition and bycatch of the semi-floating shrimp-trap fishery (SSTF). The research cruises were conducted in the same period of the year (May-July 2017).

Three areas with different levels of fisheries-impacted ecosystems were selected: (1) Cape Verdean waters, a pristine deep ecosystem with little anthropogenic alteration, where no benthic fisheries exist below 100 m; (2) Canary Islands waters, the most fisheries-impacted of the three archipelagos, with full fishing activity from 0 to 1000 m depth and multiple gears such as benthic traps, semi-floating shrimp traps, trammel nets, purse seines, longlines, hand lines and poles; and (3) Madeiran waters, an example of medium fisheries impact.

Fishing operations (n=90) were performed around the islands and not only on a particular side of them. Each fishing operation (n=90) was performed with one ground line (trap-line) with 75 traps equally spaced (25 m) along the length of the fishing rope. Each fishing operation was done at a particular location and a specific depth, with no replicates. Atlantic chub mackerel (Scomber colias) was used as bait in the traps. All fishing operations were conducted over approximately 24 h to include the entire distribution range of species affected by diel migrations. Each fishing operation (30 at each archipelago) was carried out covering a bathymetric range between 175 and 490 m depth, corresponding to the maximum abundance depth for the target species Plesionika edwardsii at the three archipelagos combined (González et al. 2016González J.A., Pajuelo J.G., Triay-Portella R., et al. 2016. Latitudinal patterns in the life-history traits of three isolated Atlantic populations of the deep-water shrimp Plesionika edwardsii (Decapoda, Pandalidae). Deep-Sea Res. I 117: 28-38.). The traps were suspended 2.4 m above the bottom. The semi-floating trap is a cylinder conical trap with a base length of 56 cm and a height of 57 cm, covered with 15×20 mm mesh. Each trap has one truncated cone-shaped opening with a 23 cm outer diameter and 19 cm inner diameter. The specimens caught were identified to species level according to the WoRMS Editorial Board (2018)WoRMS Editorial Board. 2018. World Register of Marine Species. Accessed through: http://www.marinespecies.org at VLIZ on 19/03/2018..

The species caught were classified as target species (P. edwardsii and other pandalids of the Plesionika and Heterocarpus genera) or bycatch. Bycatch is considered the incidental catch of non-target species (NMFS 2016National Marine Fisheries Service (NMFS). 2016. U.S. National Bycatch Report 1st Edition Update 2. Benaka L.R., Bullock D., Davis J., et al. (eds), National Marine Fisheries Service, U.S. Department of Commerce, 90 pp.) and was further classified into two categories: (1) catch of species or sizes that are discarded because they are not marketable or have no economic value, and (2) catch of regulated species or sizes that are discarded due to regulations (Dunn et al. 2011Dunn D.C., Boustany A.M., Halpin P.N. 2011. Spatio-temporal management of fisheries to reduce by-catch and increase fishing selectivity. Fish Fish. 12: 110-119., Zimmerhackel et al. 2015Zimmerhackel J.S., Schuhbauer A.C., Usseglio P., et al. 2015. Catch, bycatch and discards of the Galapagos Marine Reserve small-scale handline fishery. PeerJ 3: e995., NMFS 2016National Marine Fisheries Service (NMFS). 2016. U.S. National Bycatch Report 1st Edition Update 2. Benaka L.R., Bullock D., Davis J., et al. (eds), National Marine Fisheries Service, U.S. Department of Commerce, 90 pp.).

Data analysis

For each species the abundance in number of individuals and percentage was estimated by areas. For each main group (crustaceans, osteichthyans and chondrichthyans) and for the target/non-target species, the number of species and the abundance were calculated by areas.

A dominance curve, a plot of percentage cumulative abundance by numbers against the species rank, was applied to investigate changes in species dominance in the SSTF by area (Clarke 1990Clarke K.R. 1990. Comparison of dominance curves. J. Exp. Mar. Biol. Ecol. 138: 143-157.).

The analyses focused on the macrofauna caught by the SSTF. For each trap-line, the species composition and abundance (expressed as the number of individuals per trap-line) were recorded. Standardization and logarithmic transformation were applied to data of each trap-line prior to the analysis (Clarke and Warwick 2001Clarke K.R., Warwick R.M. 2001. Change in marine communities: an approach to statistical analysis and interpretation. 2nd Edition. PRIMER-E, Plymouth, 172 pp.), after which a resemblance matrix using the Bray-Curtis similarity index was constructed (Clarke and Warwick 2001Clarke K.R., Warwick R.M. 2001. Change in marine communities: an approach to statistical analysis and interpretation. 2nd Edition. PRIMER-E, Plymouth, 172 pp., Clarke and Gorley 2006Clarke K.R., Gorley R.N. 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, 190 pp.). Of the total trap-lines of the SSTF (n=90), only valid fishing operations (n=87) were used to test differences in species composition and abundance among areas. This was done using a distance-based permutational multivariate analysis of variance, PERMANOVA (Anderson et al. 2008Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, 214 pp.). The factor considered to explain the ordination of the trap-lines of the SSTF was the area (archipelagos). PERMANOVA was performed to test the null hypotheses of no differences among the assemblages of the SSTF among areas. The permutation method used was the unrestricted permutation of raw data with a maximum number of permutations of 9999 due to their good empirical results in the maximum discriminant power (Anderson and Legendre 1999Anderson M.J., Legendre P. 1999. An empirical comparison of permutation methods for tests of partial regression coefficients in a linear model. J. Stat. Comput. Simul. 62: 271-303., Anderson and ter Braak 2003Anderson M.J., ter Braak C.J.F. 2003. Permutation tests for multifactorial analysis of variance. J. Stat. Comput. Simul. 73: 85-113.). For each factor, a pseudo-F test (p-F) and a pairwise test for significant effects were estimated. Statistical analyses were performed using Primer v.6 with PERMANOVA+ software (Clarke and Warwick 1994Clarke K.R., Warwick R.M. 1994. Change in marine communities: an approach to statistical analysis and interpretation. Natural Environmental Research Council, Plymouth Marine Laboratory, Plymouth, 144 pp., Anderson et al. 2008Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, 214 pp.).

The Similarity percentage (SIMPER) analysis procedure was used to identify the species (within and between samples) that contribute the most for a significant intergroup dissimilarity between areas and for a significant intragroup similarity (Clarke and Warwick 1994Clarke K.R., Warwick R.M. 1994. Change in marine communities: an approach to statistical analysis and interpretation. Natural Environmental Research Council, Plymouth Marine Laboratory, Plymouth, 144 pp., 2001Clarke K.R., Warwick R.M. 2001. Change in marine communities: an approach to statistical analysis and interpretation. 2nd Edition. PRIMER-E, Plymouth, 172 pp.). Statistical analyses were also performed with PERMANOVA+ (Clarke and Warwick 1994Clarke K.R., Warwick R.M. 1994. Change in marine communities: an approach to statistical analysis and interpretation. Natural Environmental Research Council, Plymouth Marine Laboratory, Plymouth, 144 pp., Anderson et al. 2008Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, 214 pp.).

Biodiversity was tested among areas. Species diversity of the SSTF was estimated for abundance data with the Shannon-Wiener diversity index (H’) and species richness (S) (Magurran 1988Magurran A.E. 1988. Ecological diversity and its measurement. Princeton University Press, 179 pp.) using the DIVERSE subroutine within the Primer v.6 software. Species diversity of the SSTF was tested for differences among areas by an ANOVA test, considering each trap-line as one observation. This analysis was used to evaluate the null hypothesis of equality in S and H’ for the SSTF among areas with a critical value of F_0.05,2,86=3.15.

Abundance of the most important pandalid species (H. ensifer, P. edwardsii, P. ensis and P. martia), individually and as a whole, and sharks were compared using a catch per unit effort (CPUE) unit estimated as the average number of shrimps per trap at each line (for shrimps), and as the square root of the total count per line (for sharks). Data of abundance were compared by an ANOVA test. This analysis was used to evaluate the null hypothesis of equality in CPUE among areas with a critical value of F_0.05,2,86=3.15.

Statistical significance was set at p<0.05 for all statistical tests performed.

RESULTSTop

Of the 90 fishing operations carried out around the three archipelagos combined, 29 in Madeira, 28 in Canary Islands and 30 in Cape Verde were considered valid.

A total of 64332 individuals representing 17 crustacean species (63568 individuals, 98.8%) and 28 fish species (764 individuals, 1.2%) were recorded. Only three species of Elasmobranchii (belonging to 3 families and representing <0.1% of the individuals caught), and 23 species of Actinopterygii (16 families, 1.1% in number of individuals) were caught (Table 1). In number of individuals, shrimps of the family Pandalidae (98.7%) dominated the SSTF. By region, the SSTF in Madeira was dominated by pandalid shrimps (99.5%) followed by the fish family Congridae (0.1%). In the Canary Islands, pandalids (99.3%) dominated the catches of the SSTF, followed by the fish family Sparidae (0.2%). In Cape Verde Islands, pandalids represented 96.9% of the catches of the SSTF, followed by the fish family Moridae with 1.9%. In all three regions the dominant species in the catches of the SSTF was the main target species Plesionika edwardsii, which accounted for 96.0% in Cape Verde, 75.8% in Madeira and 59.1% in the Canary Islands. The pandalid target species accounted for more than 96.8% of the total catches.

A total of 18 non-target species were caught in Madeira, 14 in the Canary Islands and 16 in Cape Verde, of which 13, 8 and 11 species, respectively, were always discarded. Bycatch (in numbers) accounted for 0.5% of catches in Madeira, 0.7% in the Canary Islands and 3.1% in Cape Verde. The bycatch can be divided into three types according to the reason for not landing them: regulatory discards, species that are not marketable and individuals that are not marketable due to size. Bycatch due to regulations included only three individuals of Etmopterus pusillus and three of Centroscymnus crepidater in Madeira, three of C. crepidater in the Canary Islands, and 12 of Centrophorus squamosus and six of E. pusillus in Cape Verde. The capture of deep shark protected species was low, accounting for 0.11% of all individuals caught. The most frequently caught non-marketable species were Gadella maraldi, Physiculus dalwigki, Synaphrobranchus affinis and Synaphobranchus kaupii in Madeira; Macroramphosus scolopax, Systellaspis pellucida and S. affinis in the Canary Islands; and Acantholabrus palloni, Lappanella fasciata, Physiculus cyanostrophus and Physiculus caboverdensis in Cape Verde. A total of 5 species in Madeira, 6 in the Canary Islands and 4 in Cape Verde, accounting for 0.2% to 0.8% of total catches, were not landed due to the small size of individuals or low numbers of individuals caught (self-consumption).

The k-dominance curves for species abundance (Fig. 1) showed that the distribution of the number of individuals among species at Cape Verde differed markedly from that at the Canary Islands or at Madeira, which had a smaller number of dominant species. The patterns of the dominance curves of the three areas indicated different patterns of distribution of individuals among species, with the highest number of individuals aggregated in a single species at Madeira.

The results of PERMANOVA analysis (Table 2) in abundance indicated significant differences in the catch assemblage of the SSTF among archipelagos (p<0.001). Pairwise comparisons showed that the trap-lines (assemblages) among archipelagos were significantly different in all cases (Canary Islands-Madeira p<0.0005; Canary Islands-Cape Verde p<0.0001; Madeira-Cape Verde p=0.0001).

The results of the SIMPER analysis of abundance showed that a few species provided the greatest contribution for defining the assemblages of the SSTF in each area, with an average similarity of 55.0 in Madeira, 44.3 in the Canary Islands and 73.8 in Cape Verde (Table 3). Considering the cumulative contribution roughly at 90%, the species that most contributed to intragroup similarity were the three pandalid species Plesionika edwardsii, Plesionika narval and Plesionika williamsi in Madeira; a more diverse set of four species including P. edwardsii, Heterocarpus ensifer, P. narval and Plesionika ensis in the Canary Islands; and the pandalid P. edwardsii and the fish Physiculus cyanostrophus in Cape Verde (Table 2). The target species of the SSTF, P. edwardsii, had a contribution of 80.8% in Cape Verde, 72.2% in Madeira, and 39.2% in the Canary Islands (Table 3).

The comparison among areas, measured as the dissimilarity between each pair of areas, considering the number of species that cumulatively have a contribution of around 90%, is presented in Table 2. The values of dissimilarity ranged from 49.3% (between Cape Verde and Madeira) to 62.8% (between Canary Islands and Cape Verde). Five species, H. ensifer, P. edwardsii, P. ensis, P. narval and P. cyanostrophus, provided the greatest contribution (>76%) to discriminate the SSTF between the Canary Islands and Cape Verde. The pandalid species H. ensifer, P. edwardsii, P. ensis, P. narval and P. williamsi were found to contribute the most to the average dissimilarity between the SSTF of Canary Islands and Madeira. Six species, P. narval, P. cyanostrophus, P. williamsi, P. edwardsii, H. ensifer and Pontinus kuhlii, were found to be the discriminating species most contributing to the dissimilarity of the SSTF between Madeira and Cape Verde (Table 3).

By area, the greatest mean species richness (S) values of the SSTF was found in Cape Verde (S=6.71±1.73 [mean±sd]) and the lowest in the Canary Islands (S=6.26±33.13). The highest diversity values (H’) for the SSTF were also recorded in Cape Verde (H’=1.20±0.36), being lower in Madeira (H’=1.19±0.45) and in the Canary Islands (H’=1.17±0.41). The tests for homogeneity of variances for indexes of species richness (S) and diversity (H’) were not rejected (p=0.124 and p=0.746, respectively). The ANOVA test showed no significant differences either in species richness (p=0.143) or in diversity (H’) (p=0.438).

The standardized CPUEs, estimated as the average number of shrimps per trap in each trap-line (for shrimps) and as the square root of the total count per line (for sharks), showed that all pandalid species (H. ensifer, P. edwardsii, P. ensis and P. martia) individually had significant differences in CPUE level among areas (ANOVA Brown-Forsythe, p<0.033). However, when all species were analysed together, no significant differences in CPUE level among areas were found (ANOVA, Brown-Forsythe, p=0.055). Shark CPUE values were also significantly different among areas (ANOVA Brown-Forsythe, p=0.031).

DISCUSSIONTop

Fishing produces ecological impacts on the biological community structure by exploiting non-target, high-trophic-level species that are important in the structure of the ecosystems, such as sharks (Myers et al. 2007Myers R.A., Baum J.K., Shepherd T.D., et al. 2007. Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315: 1846-1850., Shester and Micheli 2011Shester G.G., Micheli F. 2011. Conservation challenges for small-scale fisheries: bycatch and habitat impacts of traps and gillnets. Biol. Conserv. 144: 1673-1681., Zimmerhackel et al. 2015Zimmerhackel J.S., Schuhbauer A.C., Usseglio P., et al. 2015. Catch, bycatch and discards of the Galapagos Marine Reserve small-scale handline fishery. PeerJ 3: e995.). The ratio of deep sharks increases with depth (Clarke et al. 2015Clarke J., Milligan R.J., Bailey D.M., et al. 2015. A scientific basis for regulating deep-sea fishing by depth. Current Biol. 25: 2425-2429.), and their exploitation causes changes in the community via trophic cascades (Pauly et al. 1998Pauly D., Christensen V., Dalsgaard J., et al. 1998. Fishing down marine food webs. Science 279: 860-863., Lewison et al. 2004Lewison R.L., Crowder L.B., Read A.J., et al. 2004. Understanding impacts of fisheries bycatch on marine megafauna. Trends Ecol. Evol. 19: 598-604., Zimmerhackel et al. 2015Zimmerhackel J.S., Schuhbauer A.C., Usseglio P., et al. 2015. Catch, bycatch and discards of the Galapagos Marine Reserve small-scale handline fishery. PeerJ 3: e995.). In the fishing system analysed herein, the bycatch volume varied from 0.5% to 3.2% in numbers. These values are in accordance with those of Kelleher (2005)Kelleher K. 2005. Discards in the world’s marine fisheries: an update. FAO Fish. Tech. Pap. 470: 1-134., who indicated that small-scale fisheries have a low or negligible discard rate (3.7% of total catches). The bycatch of the SFTF was diverse but showed a low number of individuals per species. Individuals of bycatch composition are mainly discarded because they are not marketable, but a low percentage are discarded because of regulatory restrictions. In addition, a very low proportion are discarded because they are undersized commercial species, but their bycatch makes an almost negligible contribution to the stock mortality.

The low number of individuals of non-target species caught confirmed the high selectivity of this fishing gear for a low number of target species of pandalid shrimps. Also, the overall bycatch of protected species such as sharks recorded in the present study was very low in comparison with that recorded in other small-scale activities in the area, such as the Aphanopus fishery, in which the ratio in number of individuals is one deep shark per target individual of black scabbardfish (Pajuelo et al. 2010Pajuelo J.G., González J.A., Santana J.I. 2010. Bycatch and incidental catch of the black scabbardfish (Aphanopus spp.) fishery off the Canary Islands. Fish. Res. 106: 448-453.). Cape Verde was the only area in which a single species, the morid P. cyanostrophus, was associated with the bycatch in the assemblage of the SSTF. Differences in the bycatch among areas can be best explained by a combination of local oceanographic factors and biogeographical patterns of the region considered. According to Spalding et al. (2007)Spalding M.D., Fox H.E., Allen G.R., et al. 2007. Marine ecoregions of the world: A bioregionalization of coastal and shelf areas. BioScience 57: 573-583., Madeira and the Canary Islands belong to the Macaronesian ecoregion within the Lusitanian biogeographic province of the Temperate Northern Atlantic realm, whereas Cape Verde belongs to its own ecoregion within the West African transition province of the Tropical Atlantic realm.

Estimated bycatch ratios of between 0.5% and 3.2% in numbers were significantly much lower than the current global fisheries bycatch estimates of 40.4% (Davies et al. 2009Davies R.W.D., Cripps S.J., Nickson A., et al. 2009. Defining and estimating global marine fisheries bycatch. Mar. Policy 33: 661-672.), and lower than those recorded in many small-scale fisheries such as lobster traps (15.1%), drifting gillnets (18.5%), fixed gillnets (34.4%) or bottom longlines (42.0%-50.0%) (Pajuelo et al. 2011Pajuelo J.G., García S., Lorenzo J.M., et al. 2011. Population biology of the shark Squalus megalops harvested in the central-east Atlantic Ocean. Fish. Res. 108: 31-41., Shester and Micheli 2011Shester G.G., Micheli F. 2011. Conservation challenges for small-scale fisheries: bycatch and habitat impacts of traps and gillnets. Biol. Conserv. 144: 1673-1681., Zimmerhackel et al. 2015Zimmerhackel J.S., Schuhbauer A.C., Usseglio P., et al. 2015. Catch, bycatch and discards of the Galapagos Marine Reserve small-scale handline fishery. PeerJ 3: e995.). The level of bycatch recorded is in agreement with that reported by Shester and Micheli (2011), who pointed out that bycatch and habitat impacts of traps are non-significant. This low level of bycatch in a fishery is extremely positive, because a high level of bycatch has important ecological consequences at the species, population/stock (Hall et al. 2000Hall M.A., Alverson D.L., Metuzals K.I. 2000. Bycatch: Problems and solutions. Mar. Poll. Bull. 41: 204-219., Lewison et al. 2004Lewison R.L., Crowder L.B., Read A.J., et al. 2004. Understanding impacts of fisheries bycatch on marine megafauna. Trends Ecol. Evol. 19: 598-604.) and ecosystem levels (Dulvy et al. 2003Dulvy N.K., Sadovy Y., Reynolds J.D. 2003. Extinction Kappel C.V. 2005. Losing pieces of the puzzle: threats to marine, estuarine, and diadromous Read A.J., Drinker P., Northridge S. 2006. Bycatch of marine mammals in U.S. and global fisheries. Conserv. Biol. 20: 163-169.), particularly for shark species due to their life strategies (Hall et al. 2000Hall M.A., Alverson D.L., Metuzals K.I. 2000. Bycatch: Problems and solutions. Mar. Poll. Bull. 41: 204-219., Stevens et al. 2000Stevens J., Bonfil R., Dulvy N., et al. 2000. The effects of fishing on sharks, rays and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J. Mar. Sci. 57: 476-494., Figueiredo et al. 2008Figueiredo I., Moura T., Neves A., et al. 2008. Reproductive strategy of leafscale gulper shark Centrophorus squamosus and the Portuguese dogfish Centroscymnus coelolepis on the Portuguese continental slope. J. Fish Biol. 73: 206-225.). These impacts include reduction of the reproductive rates, reduction of population biomass, and less resilient marine ecosystems (Zimmerhackel et al. 2015Zimmerhackel J.S., Schuhbauer A.C., Usseglio P., et al. 2015. Catch, bycatch and discards of the Galapagos Marine Reserve small-scale handline fishery. PeerJ 3: e995.).

Differences found in the catch assemblage of the SSTF among archipelagos indicate that the relative composition among species in the catches is different, and that the fishing system affects them in a different way.

These differences seem to be associated with the degree of human fishing exploitation of each area due to this fishing gear and particularly to other fishing systems used in the area, such as bottom traps, lines and longlines (Pajuelo and Lorenzo 1995Pajuelo J.G., Lorenzo J.M. 1995. Análisis y predicción de la pesquería demersal de las Islas Canarias mediante un modelo ARIMA. Sci. Mar. 59: 155-164., Pajuelo et al. 2011Pajuelo J.G., García S., Lorenzo J.M., et al. 2011. Population biology of the shark Squalus megalops harvested in the central-east Atlantic Ocean. Fish. Res. 108: 31-41., Biscoito et al. 2015Biscoito M., Freitas M., Pajuelo J.G., et al. 2015. Sex-structure, depth distribution, intermoult period and reproductive pattern of the deep sea red crab Chaceon affinis (Brachyura, Geryonidae) in two populations in the north-eastern Atlantic. Deep-Sea Res. I 95: 99-114.). In the area where there is no fishing exploitation, the main target species represented 96.8% of the catches but, when the exploitation increases in each area, there is a relative increase of the other pandalid target species that occupy the niche left by the species directly or indirectly affected by the fishing exploitation.

The archipelagos that showed the greatests differences were the Canary Islands and the Cape Verde, i.e. the most exploited and the unexploited marine areas, respectively, while Madeira was in an intermediate position in accordance with its moderate degree of exploitation. As the degree of exploitation changes from one area to another and as the communities are altered or degraded (Pajuelo et al. 2010Pajuelo J.G., González J.A., Santana J.I. 2010. Bycatch and incidental catch of the black scabbardfish (Aphanopus spp.) fishery off the Canary Islands. Fish. Res. 106: 448-453., 2011Pajuelo J.G., García S., Lorenzo J.M., et al. 2011. Population biology of the shark Squalus megalops harvested in the central-east Atlantic Ocean. Fish. Res. 108: 31-41., Shester and Micheli 2011Shester G.G., Micheli F. 2011. Conservation challenges for small-scale fisheries: bycatch and habitat impacts of traps and gillnets. Biol. Conserv. 144: 1673-1681., Zimmerhackel et al. 2015Zimmerhackel J.S., Schuhbauer A.C., Usseglio P., et al. 2015. Catch, bycatch and discards of the Galapagos Marine Reserve small-scale handline fishery. PeerJ 3: e995.), the present results suggest that the structure of catches and their relative proportions change, and therefore the assemblages obtained with SSTF will change. These changes are supported by historical data. In the Canary Islands, the first fishing surveys with semi-floating shrimp traps in 1997 yielded 90.1% of P. edwardsii in the catches, with only 8.8% of other pandalids, mainly P. narval and H. ensifer (González 1997González J.A. 1997. Transferencia de tecnología a la flota artesanal canaria y desarrollo de nuevas pesquerías de camarones profundos. Instituto Canario de Ciencias Marinas, Gobierno de Canarias. Telde, Las Palmas, 69 pp.). In Cape Verde, the first fishing surveys with this selective fishing system in 2010 yielded 93.4% (Santiago island) and 96.9% (Boa Vista island) of P. edwardsii (unpublished data).

However, it is important to point out that these changes do not generate an increase in the species exploited, or a reduction in the standard mean abundance for each SSTF between areas, given that no changes are found in diversity, so there are only changes in the species dominance in the assemblage. CPUE data confirm these results, showing that values for each individual species differed among areas. However, pandalids as a whole showed no differences in CPUE values among areas.

The present results suggest that semi-floating shrimp traps do not change their selectivity for the main target species, P. edwardsii, because of a change in selective capacity or losses of selective capacity in an exploited marine ecosystem versus a pristine area such as Cape Verde, but because of changes in the community. Changes in the community produce changes in the species dominance, probably associated with the degree of human exploitation in the marine ecosystems, which is the case of the overexploited Canary Islands waters. In Madeiran waters, the situation seems to be intermediate. Despite these changes in relative abundance between the main target species and other target species, the bycatch rate is always very low regardless of the marine ecosystem conditions.

Taking into account that 22 million fishers work globally in small-scale fisheries and that these fisheries provide over 50% of the world’s catches (Berkes et al. 2001Berkes F., Mahon R., McConney P., et al. 2001. Managing small-scale fisheries: alternative directions and methods. IDRC, Ottawa, 320 pp., Chuenpagdee et al. 2006Chuenpagdee R., Liguori L., Palomares M.L.D., et al. 2006. Bottom-up, global estimates of small-scale marine fisheries catches. Fisheries Centre Research Reports, University of British Columbia 14: 1-110., Teh and Sumaila 2013Teh L.C.L., Sumaila U.R. 2013. Contribution of marine fisheries to worldwide employment. Fish Fish. 14: 77-88.), the use and development of this kind of selective fishing system makes an important contribution to reducing bycatch and conserving the community and habitat, especially in deep-sea marine ecosystems.

ACKNOWLEDGEMENTSTop

The authors are grateful to one anonymous reviewer and to Dr. Margarida Castro (University of Algarve) for their comments, which greatly improved our manuscript. The European Regional Development Fund, in the framework of the ‘Programa de Cooperación Transnacional MAC (Madeira-Azores-Canarias)’ projects MACAROFOOD (MAC/2.3d/015) and MARISCOMAC (MAC/2.3d/097), gave logistic and financial support.

REFERENCESTop

Alverson D.L., Freeber M.H., Murawski S.A., et al. 1994. A global assessment of fisheries bycatch and discards. FAO Fish. Tech. Pap. 339: 1-233.

Anderson M.J., Legendre P. 1999. An empirical comparison of permutation methods for tests of partial regression coefficients in a linear model. J. Stat. Comput. Simul. 62: 271-303.
https://doi.org/10.1080/00949659908811936

Anderson M.J., ter Braak C.J.F. 2003. Permutation tests for multifactorial analysis of variance. J. Stat. Comput. Simul. 73: 85-113.
https://doi.org/10.1080/00949650215733

Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, 214 pp.

Bellido J.M., Santos M.B., Pennino M.G., et al. 2011. Fishery discards and bycatch: solutions for an ecosystem approach to fisheries management? Hydrobiologia 670: 317-333.
https://doi.org/10.1007/s10750-011-0721-5

Berkes F., Mahon R., McConney P., et al. 2001. Managing small-scale fisheries: alternative directions and methods. IDRC, Ottawa, 320 pp.

Biscoito M., Freitas M., Pajuelo J.G., et al. 2015. Sex-structure, depth distribution, intermoult period and reproductive pattern of the deep sea red crab Chaceon affinis (Brachyura, Geryonidae) in two populations in the north-eastern Atlantic. Deep-Sea Res. I 95: 99-114.
https://doi.org/10.1016/j.dsr.2014.10.010

Cartes J.A., Serrano A., Velasco F., et al. 2007. Community structure and dynamics of deep-water decapod assemblages from Le Danois Bank (Cantabrian Sea, NE Atlantic): Influence of environmental variables and food availability. Progr. Oceanog. 75: 797-816.
https://doi.org/10.1016/j.pocean.2007.09.003

Chuenpagdee R., Liguori L., Palomares M.L.D., et al. 2006. Bottom-up, global estimates of small-scale marine fisheries catches. Fisheries Centre Research Reports, University of British Columbia 14: 1-110.

Clarke K.R. 1990. Comparison of dominance curves. J. Exp. Mar. Biol. Ecol. 138: 143-157.
https://doi.org/10.1016/0022-0981(90)90181-B

Clarke K.R., Gorley R.N. 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, 190 pp.

Clarke K.R., Warwick R.M. 1994. Change in marine communities: an approach to statistical analysis and interpretation. Natural Environmental Research Council, Plymouth Marine Laboratory, Plymouth, 144 pp.

Clarke K.R., Warwick R.M. 2001. Change in marine communities: an approach to statistical analysis and interpretation. 2nd Edition. PRIMER-E, Plymouth, 172 pp.

Clarke J., Milligan R.J., Bailey D.M., et al. 2015. A scientific basis for regulating deep-sea fishing by depth. Current Biol. 25: 2425-2429.
https://doi.org/10.1016/j.cub.2015.09.035

Clarke M.W. 2009. Sharks, skates and rays in the northeast Atlantic: population status, advice and management. J. Appl. Ichthyol. 25: 3-8.
https://doi.org/10.1111/j.1439-0426.2008.01069.x

Davies R.W.D., Cripps S.J., Nickson A., et al. 2009. Defining and estimating global marine fisheries bycatch. Mar. Policy 33: 661-672.
https://doi.org/10.1016/j.marpol.2009.01.003

Dulvy N.K., Sadovy Y., Reynolds J.D. 2003. Extinction vulnerability in marine populations. Fish Fish. 4: 25-64.
https://doi.org/10.1046/j.1467-2979.2003.00105.x

Dunn D.C., Boustany A.M., Halpin P.N. 2011. Spatio-temporal management of fisheries to reduce by-catch and increase fishing selectivity. Fish Fish. 12: 110-119.
https://doi.org/10.1111/j.1467-2979.2010.00388.x

Figueiredo I., Moura T., Neves A., et al. 2008. Reproductive strategy of leafscale gulper shark Centrophorus squamosus and the Portuguese dogfish Centroscymnus coelolepis on the Portuguese continental slope. J. Fish Biol. 73: 206-225.
https://doi.org/10.1111/j.1095-8649.2008.01927.x

García-Rodríguez M., Esteban A., Pérez Gil J.L. 2000. Considerations on the biology of Plesionika edwardsii (Brandt, 1851) (Decapoda, Caridea, Pandalidae) from experimental trap catches in the Spanish western Mediterranean Sea. Sci. Mar. 64: 369-379.
https://doi.org/10.3989/scimar.2000.64n4369

González J.A. 1997. Transferencia de tecnología a la flota artesanal canaria y desarrollo de nuevas pesquerías de camarones profundos. Instituto Canario de Ciencias Marinas, Gobierno de Canarias. Telde, Las Palmas, 69 pp.

González J.A., Carrillo J., Santana J.I., et al. 1992. La pesquería de Quisquilla, Plesionika edwardsii (Brandt, 1851), con tren de nasas en el Levante español. Ensayos a pequeña escala en Canarias. Inf. Tec. Sci. Mar. 170: 1-31.

González J.A., Quiles J.A., Tuset V.M., et al. 2001. Data on the family Pandalidae around the Canary Islands, with first record of Plesionika antigai (Caridea). Hydrobiologia 449: 71-76.
https://doi.org/10.1023/A:1017532801641

González J.A., Pajuelo J.G., Triay-Portella R., et al. 2016. Latitudinal patterns in the life-history traits of three isolated Atlantic populations of the deep-water shrimp Plesionika edwardsii (Decapoda, Pandalidae). Deep-Sea Res. I 117: 28-38.
https://doi.org/10.1016/j.dsr.2016.09.004

Hall M.A., Alverson D.L., Metuzals K.I. 2000. Bycatch: Problems and solutions. Mar. Poll. Bull. 41: 204-219.
https://doi.org/10.1016/S0025-326X(00)00111-9

Harrington J.M., Myers R.A., Rosenberg A.A. 2005. Wasted fishery resources: discarded by-catch in the USA. Fish Fish. 6: 350-361.
https://doi.org/10.1111/j.1467-2979.2005.00201.x

Jacquet J., Pauly D. 2008. Funding priorities: big barriers to small-scale fisheries. Conserv. Biol. 22: 832-835.
https://doi.org/10.1111/j.1523-1739.2008.00978.x

Kappel C.V. 2005. Losing pieces of the puzzle: threats to marine, estuarine, and diadromous species. Front. Ecol. Environ. 3: 275-282.
https://doi.org/10.1890/1540-9295(2005)003[0275:LPOTPT]2.0.CO;2

Kelleher K. 2005. Discards in the world’s marine fisheries: an update. FAO Fish. Tech. Pap. 470: 1-134.

Lewison R.L., Crowder L.B., Read A.J., et al. 2004. Understanding impacts of fisheries bycatch on marine megafauna. Trends Ecol. Evol. 19: 598-604.
https://doi.org/10.1016/j.tree.2004.09.004

Magurran A.E. 1988. Ecological diversity and its measurement. Princeton University Press, 179 pp.
https://doi.org/10.1007/978-94-015-7358-0

Myers R.A., Baum J.K., Shepherd T.D., et al. 2007. Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315: 1846-1850.
https://doi.org/10.1126/science.1138657

National Marine Fisheries Service (NMFS). 2016. U.S. National Bycatch Report 1st Edition Update 2. Benaka L.R., Bullock D., Davis J., et al. (eds), National Marine Fisheries Service, U.S. Department of Commerce, 90 pp.

Pajuelo J.G., Lorenzo J.M. 1995. Análisis y predicción de la pesquería demersal de las Islas Canarias mediante un modelo ARIMA. Sci. Mar. 59: 155-164.

Pajuelo J.G., González J.A., Santana J.I. 2010. Bycatch and incidental catch of the black scabbardfish (Aphanopus spp.) fishery off the Canary Islands. Fish. Res. 106: 448-453.
https://doi.org/10.1016/j.fishres.2010.09.019

Pajuelo J.G., García S., Lorenzo J.M., et al. 2011. Population biology of the shark Squalus megalops harvested in the central-east Atlantic Ocean. Fish. Res. 108: 31-41.
https://doi.org/10.1016/j.fishres.2010.11.018

Pajuelo J.G., Seoane J., Biscoito M., et al. 2016. Assemblages of deep-sea fishes on the middle slope off Northwest Africa (26°-33°N, Eastern Atlantic). Deep-Sea Res. I 118: 66-83.
https://doi.org/10.1016/j.dsr.2016.10.011

Pauly D. 2008. Global fisheries: a brief review. J. Biol. Res. 9: 3-9.

Pauly D., Christensen V. 1995. Primary production required to sustain global fisheries. Nature 374: 255-257.
https://doi.org/10.1038/374255a0

Pauly D., Christensen V., Dalsgaard J., et al. 1998. Fishing down marine food webs. Science 279: 860-863.
https://doi.org/10.1126/science.279.5352.860

Read A.J., Drinker P., Northridge S. 2006. Bycatch of marine mammals in U.S. and global fisheries. Conserv. Biol. 20: 163-169.
https://doi.org/10.1111/j.1523-1739.2006.00338.x

Sadovy Y., Craig M.T., Bertoncini A.A., et al. 2013. Fishing groupers towards extinction: a global assessment of threats and extinction risks in a billion dollar fishery. Fish Fish. 14: 119-136.
https://doi.org/10.1111/j.1467-2979.2011.00455.x

Shester G.G., Micheli F. 2011. Conservation challenges for small-scale fisheries: bycatch and habitat impacts of traps and gillnets. Biol. Conserv. 144: 1673-1681.
https://doi.org/10.1016/j.biocon.2011.02.023

Spalding M.D., Fox H.E., Allen G.R., et al. 2007. Marine ecoregions of the world: A bioregionalization of coastal and shelf areas. BioScience 57: 573-583.
https://doi.org/10.1641/B570707

Stevens J., Bonfil R., Dulvy N., et al. 2000. The effects of fishing on sharks, rays and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J. Mar. Sci. 57: 476-494.
https://doi.org/10.1006/jmsc.2000.0724

Stobutzki I., Miller M., Brewer D. 2001. Sustainability of fishery bycatch: a process for assessing highly diverse and numerous bycatch. Environ. Conserv. 28: 167-181.
https://doi.org/10.1017/S0376892901000170

Teh L.C.L., Sumaila U.R. 2013. Contribution of marine fisheries to worldwide employment. Fish Fish. 14: 77-88.
https://doi.org/10.1111/j.1467-2979.2011.00450.x

WoRMS Editorial Board. 2018. World Register of Marine Species. Accessed through: http://www.marinespecies.org at VLIZ on 19/03/2018.

Zimmerhackel J.S., Schuhbauer A.C., Usseglio P., et al. 2015. Catch, bycatch and discards of the Galapagos Marine Reserve small-scale handline fishery. PeerJ 3: e995.
https://doi.org/10.7717/peerj.995