Deep-water longline fishing has reduced impact on Vulnerable Marine Ecosystems

Christopher K. Pham, Hugo Diogo, Gui Menezes, Filipe Porteiro, Andreia Braga-

Henriques, Frederic Vandeperre, Telmo Morato*

Supplementary information

Figure S1. Spatial distribution of bycatch of epibenthic organisms in deep-sea bottom longline sets estimated from commercial activities and research cruises in the Azores. Bycatch rates were estimated from commercial activities and research cruises as number of organisms 1,000 hooks-1 and were standardized with General Additive Models. Lighter grey area represents water depths in the Exclusive Economic Zone of the Azores exceeding 1,000 m. (a), . (b), Antipatharia. (c) Scleractinia. (d) . (e) Stylasteridae. (f) Porifera.

Maps created using a Geographic Information System (ESRI ARCGIS 10.1).

Figure S2. Proportion of epibenthic organisms with different size-class in the bycatch of deep- sea bottom longline.

Figure S3. The effect of explanatory variables on the bycatch of epibenthic organisms as estimated by a four variable GAM. (a), Vessel number 2 is the research vessel whilst number 1 and 3-6 are commercial vessels). Fishing sets done with the research vessel had higher catch rates compared to the commercial fishing vessels. (b), Site category (seamount or island shelf). There were higher bycatch levels on fishing sets done on seamounts compared to island shelves. (c), Depth showed a nonlinear relationship with the log transformed bycatch of epibenthic organisms. In general, bycatch rates increased between 200 and 450 m depth dropping considerably for fishing sets done at greater depths. (d), Geographic location (latitude and longitude) showed a slight tendency for bycatch levels to increase northwards. (e), Results from the analysis of variance of a four-variable GAM of epibenthic bycatch rates. The y axis in a-c reflects natural log-transformation.

Figure S4. Diagnostic plots of the final GAM model. Left panel: histogram of the raw residuals; centre panel: normal QQ-plot of deviance residuals against theoretical quantiles; right panel: plot of Pearson residuals against fitted values.

Figure S5. Standardised residuals obtained by the final GAM plotted versus their spatial coordinates. Blue circles are negative residuals, and orange circles are positive residuals.

Table S1. Bycatch organisms caught during commercial longline operations and research surveys. Primary bycatch is referred to organisms or organic substrate being hooked by the gear while secondary bycatch organisms are organisms found growing on the primary bycatch. Primary and secondary bycatch were composed of at least 47 and 50 distinct taxa belonging to 4 and 7 different phyla, respectively. In bold are the name of the taxonomic groups used in the text. Primary Secondary Groups / Class Order Taxa bycatch bycatch Phylum N F (%) N F(%) Bryozoa 9 0.8 205 12.6

Actinaria Actiniaria 4 0.4 152 9.3

Alcyonacea Cnidaria Anthozoa Alcyonacea Schizophytum echinatum - - 8 0.5 Cnidaria Anthozoa Alcyonacea Sarcodictyon catenatum - - 4 0.2 Cnidaria Anthozoa Alcyonacea Clavularia sp. 1 0.1 7 0.4 Cnidaria Anthozoa Alcyonacea Acanthogorgia armata 26 2.3 10 0.6 Cnidaria Anthozoa Alcyonacea Acanthogorgia hirsuta 29 2.6 - - Cnidaria Anthozoa Alcyonacea Acanthogorgia spp. 2 0.2 - - Cnidaria Anthozoa Alcyonacea Alcyonium rubrum - - 2 0.1 Cnidaria Anthozoa Alcyonacea Alcyonium spp. - - 37 2.3 Cnidaria Anthozoa Alcyonacea Alcyonium bocagei 1 0.1 3 0.2 Cnidaria Anthozoa Alcyonacea Alcyonacea 21 1.9 15 1 Cnidaria Anthozoa Alcyonacea Alcyoniidae 1 0.1 20 1.2 Cnidaria Anthozoa Alcyonacea Anthomastus agaricus 2 0.2 2 0.1 Cnidaria Anthozoa Alcyonacea Bebryce mollis 8 0.7 25 1.5 Cnidaria Anthozoa Alcyonacea Callogorgia verticillata 96 8.5 4 0.2 Cnidaria Anthozoa Alcyonacea Candidella imbricata 8 0.7 6 0.4 Cnidaria Anthozoa Alcyonacea Chrysogorgia agassizii 4 0.4 - - Cnidaria Anthozoa Alcyonacea Chrysogorgia sp. 4 0.4 - - Cnidaria Anthozoa Alcyonacea Corallium johnsoni 3 0.3 - - Cnidaria Anthozoa Alcyonacea Corallium sp. 2 0.2 - - Cnidaria Anthozoa Alcyonacea Dentomuricea aff. meteor 96 8.4 5 0.3 Muriceides Cnidaria Anthozoa Alcyonacea 6 0.5 4 0.2 paucituberculata Paracalyptrophora Cnidaria Anthozoa Alcyonacea 31 2.7 - - josephinae Cnidaria Anthozoa Alcyonacea Paragorgia johnsoni 8 0.8 2 0.2 Cnidaria Anthozoa Alcyonacea Paramuricea sp. 1 0.1 1 0.1 Cnidaria Anthozoa Alcyonacea Placogorgia terceira 3 0.3 4 0.2 Cnidaria Anthozoa Alcyonacea 11 1 3 0.2 Cnidaria Anthozoa Alcyonacea Primnoidae 2 0.2 2 0.2 Cnidaria Anthozoa Alcyonacea Swiftia dubia - - 1 0.1 Thouarella (Euthouarella) Cnidaria Anthozoa Alcyonacea - - 3 0.2 hilgendorfi Cnidaria Anthozoa Alcyonacea Thouarella spp. - - 2 0.1 Cnidaria Anthozoa Alcyonacea Villogorgia bebrycoides 7 0.6 11 0.7 Cnidaria Anthozoa Alcyonacea Viminella flagellum 89 7.8 8 0.5 Primary Secondary Groups / Class Order Taxa bycatch bycatch Phylum N F (%) N F(%) Antipatharia Cnidaria Anthozoa Antipatharia Antipatharia 5 0.5 7 0.5 Cnidaria Anthozoa Antipatharia Elatopathes sp. 1 0.1 - - Cnidaria Anthozoa Antipatharia Leiopathes sp. 32 2.8 1 0.1 Cnidaria Anthozoa Antipatharia Parantipathes sp. 4 0.4 - - Cnidaria Anthozoa Antipatharia Stichopathes gravieri 4 0.4 - - Cnidaria Anthozoa Antipatharia Tanacetipathes sp. 1 0.1 - - Leptothecata Cnidaria Leptothecata Acryptolaria conferta - - 2 0.1 Cnidaria Hydrozoa Leptothecata Acryptolaria crassicaulis - - 1 0.1 Cnidaria Hydrozoa Leptothecata Aglaophenia lophocarpa - - 1 0.1 Cnidaria Hydrozoa Leptothecata Antennella secundaria - - 13 0.8 Cnidaria Hydrozoa Leptothecata Cryptolaria pectinata - - 8 0.5 Cnidaria Hydrozoa Leptothecata Diphasia margareta 11 1.0 3 0.2 Cnidaria Hydrozoa Leptothecata Diphasia sp. 1 0.1 1 0.1 Cnidaria Hydrozoa Leptothecata Filellum serratum - - 3 0.2 Cnidaria Hydrozoa Leptothecata Halecium sp. - - 1 0.1 Cnidaria Hydrozoa Leptothecata Nemertesia antennina - - 2 0.1 Cnidaria Hydrozoa Leptothecata Nemertesia sp. - - 2 0.1 Cnidaria Hydrozoa Leptothecata Lytocarpia myriophyllum 48 4.2 - - Cnidaria Hydrozoa Leptothecata Plumularia sp. 2 0.2 - - Cnidaria Hydrozoa Leptothecata Polyplumaria flabellata 23 2 4 0.2 Cnidaria Hydrozoa Leptothecata gayi - - 3 0.2 Cnidaria Hydrozoa Leptothecata Zygophylax biarmata - - 1 0.1 Cnidaria Hydrozoa Leptothecata Polyplumaria sp. 1 0.1 - - Cnidaria Hydrozoa Unidentified Hydrozoa 74 6.5 409 25.2

Scleractinia Cnidaria Anthozoa Scleractinia Scleractinia 4 0.4 27 1.7 Cnidaria Anthozoa Scleractinia Caryophyllia cyathus 3 0.3 25 1.5 Cnidaria Anthozoa Scleractinia Caryophyllia alberti - - 3 0.2 Cnidaria Anthozoa Scleractinia Caryophyllia spp. 1 0.1 20 1.2 Cnidaria Anthozoa Scleractinia Caryophylliidae 1 0.1 3 0.2 Cnidaria Anthozoa Scleractinia Dendrophyllia cornigera 3 0.3 - - Cnidaria Anthozoa Scleractinia Dendrophyllia ramea 2 0.2 - - Cnidaria Anthozoa Scleractinia Dendrophyllia sp. 24 2.1 2 0.1 Cnidaria Anthozoa Scleractinia Desmophyllum dianthus 5 0.4 10 0.6 Cnidaria Anthozoa Scleractinia Enallopsammia rostrata 5 0.4 - - Cnidaria Anthozoa Scleractinia Enallopsammia sp. 1 0.1 - - Cnidaria Anthozoa Scleractinia Flabellum sp. 1 0.1 - - Cnidaria Anthozoa Scleractinia Lophelia pertusa 3 0.3 - - Cnidaria Anthozoa Scleractinia Madrepora oculata 17 1.5 5 0.3 Cnidaria Anthozoa Scleractinia Solenosmilia variabilis 19 1.7 1 0.1 Cnidaria Anthozoa Scleractinia Stenocyathus vermiformis - - 15 0.9 Stylasteridae Cnidaria Hydrozoa Anthoathecata Stylasteridae 4 0.4 - - Cnidaria Hydrozoa Anthoathecata Crypthelia sp. 1 0.1 - - Primary Secondary Groups / Class Order Taxa bycatch bycatch Phylum N F (%) N F(%) Cnidaria Hydrozoa Anthoathecata Errina atlantica 7 0.6 2 0.1 Cnidaria Hydrozoa Anthoathecata Errina dabneyi 43 3.8 8 0.5 Cnidaria Hydrozoa Anthoathecata Errina sp. 2 0.2 2 0.1 Cnidaria Hydrozoa Anthoathecata Pliobothrus symmetricus 2 0.2 2 0.1 Zoantharia Cnidaria Anthozoa Zoanthidea Zoanthidea 2 0.2 38 2.3 Cirripedia Crustacea Maxillopoda - - 21 1.3

Crinoidea - - 5 0.3

Foraminifera Polythalamea Rotaliida Miniacina miniacea - - 6 0.4 Bivalvia - - 19 1.2 Porifera 213 18.8 381 23.4

Inorganic 74 6.5 3 0.2 subtrate Non-id 15 1.8 14 0.9

Table S2. Results from the backward GAM model selection summarized in terms of AIC, residual deviance and Pseudo coefficient of determination (Pseudo-R2). The model selection followed 7 distinct backward steps based on the AIC values and significance of covariates. Total fish catch per fishing set (Chi-square; p=0.57) and type of longline gear (Chi-square; p=0.31) were dropped from the full model for decreasing the AIC value and not being significant covariates. Although cumulative fishing effort showed an effect in the model fit as evaluated by the AIC, it was not a significant covariate (Chi-square; p=0.06). The remaining covariates were kept in the model (Chi-square; p<0.05). The final model included 2 categorical variables (vessel name and site category) with hooks as an offset, and smooth function of depth and geographic location (latitude and longitude).

Step Model AIC Residual deviance d.f. Pseudo-R2

Full model* 1689.880 275.872 19.263 37.7

1 - fish catch 1687.906 275.880 18.281 37.7

2 - fishing gear 1686.795 300.262 17.193 37.5

3 - fishing effort 1723.474 290.602 18.404 38.5

4 - vessel 1766.818 211.208 18.487 31.6

5 - depth 1752.746 245.088 19.456 34.3

6 - site category 1727.080 290.380 20.097 38.5

7 - lat, long 1739.874 229.372 9.498 33.1

Footnote: * Full model: bycatch~vessel + site category + s(depth) + s(long, lat) + fish catch + fishing effort + fishing gear + offset (hooks) Table S3. Occurrence and morphological classification of the various epibenthic groups in the bycatch of deep-sea bottom longline. Longline sets done by commercial fishing operations and research surveys in the Azores between 2007 and 2011. Primary bycatch is referred to organisms or organic substrate being hooked by the gear while secondary bycatch organisms were found growing on the primary bycatch. The morphological classification of the epibenthic organisms was adapted from previous assessment1.

Group Primary bycatch Secondary bycatch

N of Percent N of Percent

genera occurrence* Size Complexity genera occurrence* Size Complexity

Porifera n.a. 18.8 M H n.a. 23.5 S H

Actiniaria n.a. 0.4 M H n.a. 9.4 S L

Alcyonacea 18 40.7 L H 18 11.7 S L

Antipatharia 5 4.1 L H 1 0.5 M H

Scleractinia 8 7.8 M H 6 6.8 S H

Zoantharia ? 0.2 S L n.a. 2.3 S n.a.

Leptothecata 4 14.1 M H 10 28.0 S L

Stylasteridae 3 5.2 M H 2 0.9 M H

Bryozoa n.a. 0.8 n.a. n.a. n.a. 12.6 S L

Bivalvia n.a. 1.2 S L

Cirripedia n.a. 1.3 S L

Crinoidea n.a. 0.3 n.a. n.a.

Foraminifera 1 0.4 S n.a.

Footnote: n.a., information not available; S, small; M, medium; L, large; H, high; L, low * Bycatch items not in the table included organisms not identified (1.3% and 1.1% of the total for primary and secondary bycatch, respectively) and inorganic substrate (6.5% of the primary bycatch).

Table S4. Physical condition of two of cold-water corals with distinct morphological characteristics in the vicinity of lost fishing gear on a case study location.

Physical Survival V. D. aff. Description Total condition potential flagellum meteor Intact No evidence of physical damage Full 72% 51% 63% Individual not dislocated but not in Bent High 24% 0% 12% normal vertical stance Few broken/missing branches (< 50% Minor damage High 0% 6% 3% of the colony damaged) Major Large portion of the organism structural missing/broken (>50% of the colony Mid 3% 38% 20% damage damaged) Individuals completely displaced but Displaced Null 0% 1% 1% still alive as revealed by coloration No remaining color pigment, or Dead Null 1% 3% 2% totally covered by epibionts

Table S5. Removal rates of different groups of benthic organisms per bottom trawl reported in the literature.

Target Trawl Removal Depth Organism Area Ref. Species type rate (%) (m) † 2

Shrimp OT ¶ 4 Algae Australia 20-35 ‡ BT 3 Fish 31 Annelid worms North Sea 45

* 2

Shrimp OT 11 Ascidians Australia 20-35 2

Shrimp OT 10 Asteroids Australia 20-35 3

Fish BT 68 Bivalves North Sea 45 2

Shrimp OT 9 Bivalves Australia 20-35 * 2

Shrimp OT 9 Bryozoans Australia 20-35 * 2

Shrimp OT 8 Crinoids Australia 20-35 3

Fish BT 49 Crustaceans North Sea 45 2

Shrimp OT 13 Crustaceans Australia 20-35 2

Shrimp OT 14 Echinoids Australia 20-35 2

Shrimp OT 20 Gastropods Australia 20-35 2

Shrimp OT 11 Holothurians Australia 20-35 * 2

Shrimp OT 8 Hydrozoans Australia 20-35 Fish OT 15.5 Macrobenthos (>20cm) Australia 50 4 Shrimp OT 13* Octocorals Australia 20-50 5 Fish OT 4* Octocorals Australia 78 6 * 2

Shrimp OT 9 Octocorals (Nephtheid) Australia 20-35 * 2

Shrimp OT 15 Octocorals (Octocorals) Australia 20-35 Shrimp OT 10* Octocorals (sea fans) Australia 20-50 7 * 7

Shrimp OT 5 Octocorals (sea whips) Australia 20-50 2

Shrimp OT 9 Ophiuroids Australia 20-35 3

Fish BT 40 Sea urchins North Sea 45 * 5

Shrimp OT 6 Sponges Australia 20-50 * 2

Shrimp OT 12 Sponges Australia 20-35 * 7

Shrimp OT 20 Sponges (large) Australia 20-50 Shrimp OT 90* Sponges (large) Australia 20-50 8 * 6

Fish OT 27 Sponges (large) Australia 78 * 6

Fish OT 11 Sponges (medium) Australia 78 * 6

Fish OT 15 Sponges (small) Australia 78 * 2

Shrimp OT 11 Zoantharians Australia 20-35 * values of direct comparison with the impact of longlining; † is Beam trawl, ‡ is Otter trawl Table S6. Bycatch rates of deep-sea sharks (% of total catch) reported for different longline and trawl fisheries around the world. Bycatch Location Gear Target species Depth (m) Source data Ref. rate * 9

Azores LL Blackspot seabream 300-750 2.6% Obs, commercial fishing † 9

Azores HL Blackspot seabream 100-500 0.0% Obs, commercial fishing 10

South Portugal LL European hake 200-550 37.2% Survey 11

Rockall Trough LL not known 600-1400 58.8% Survey || 12

Hatton Bank LL DW fish & sharks 750-1500 80.4% Survey 13

Bay of Biscay LL DW fish & sharks not known 43.2% Commercial fishing 14

Faeroe LL deep water sharks 750-1480 82.5% Survey 14

Reykjanes Ridge LL deep water fish 600-960 56.3% Survey 15

Reykjanes Ridge LL not known 500-2000 10.1% Survey 15

Reykjanes Ridge LL not known 500-1700 37.2% Survey 15

Hecate Seamount LL not known 500-1800 22.2% Survey 15

North Azores LL not known 500-1300 63.2% Survey ‡ 16 Azores DLL Black sccabardfish 650-1500 14.6% Obs, commercial fishing 17

Canary Islands DLL Black sccabardfish 200-3000 35.1% Survey 18

Continental Portugal DLL Black sccabardfish 800-1450 8.2% Commercial fishing § 19 Azores T Orange roughy 850-1300 2.9% Obs, commercial fishing 11

Rockall Trough T not known 600-1400 22.4% Survey 13

Hatton Bank T not known not known 21.1% Commercial fishing 15

Faraday Seamounts T not known 500-1200 6.9% Survey 20

Icelandic waters T not known 800-1200 23.0% Survey 21

ICES Sub-areas V-VII T DW fish & sharks not known 9.0% Commercial fishing * Longline, † Handline, ‡ drifting longline, § bottom trawl; || DW is deep-water

Table S7. The categories of cumulative fishing effort along with the number of corresponding 10 x 10 km cells and the number of fishing sets done per category to investigate the effect of fishing effort on the bycatch rate of epibenthic organisms.

Effort category (total nº of longlines Nº of different Nº of fishing sets for bycatch 100km-2 between 1998-2012) cells quantification 0-1000 31 121 1001-2000 20 47 2001-3000 17 95 3001-4000 6 56 >4000 18 156

References 1 Sampaio, I. et al. Cold-water corals landed by bottom longline fisheries in the Azores (north-eastern Atlantic). J. Mar. Biol. Assoc. U. K. 92, 1547-1555, doi:10.1017/s0025315412000045 (2012). 2 Burridge, C. Y., Pitcher, C. R., Wassenberg, T. J., Poiner, I. R. & Hill, B. Measurement of the rate of depletion of benthic fauna by prawn (shrimp) otter trawls: an experiment in the Great Barrier Reef, Australia. Fish Res. 60, 237-253, doi:10.1016/s0165- 7836(02)00179-0 (2003). 3 Bergman, M. J. N. & van Santbrink, J. W. Mortality in megafaunal benthic populations caused by trawl fisheries on the Dutch continental shelf in the North Sea in 1994. ICES J. Mar. Sci. 57, 1321-1331, doi:10.1006/jmsc.2000.0917 (2000). 4 Moran, M. J. & Stephenson, P. C. Effects of otter trawling on macrobenthos and management of demersal scalefish fisheries on the continental shelf of north-western Australia. ICES J. Mar. Sci. 57, 510-516, doi:10.1006/jmsc.2000.0718 (2000). 5 Pitcher, C. R., Burridge, C. Y., Wassenberg, T. J., Hill, B. J. & Poiner, I. R. A large scale BACI experiment to test the effects of prawn trawling on seabed biota in a closed area of the Great Barrier Reef Marine Park, Australia. Fish Res. 99, 168-183, doi:10.1016/j.fishres.2009.05.017 (2009). 6 Wassenberg, T. J., Dews, G. & Cook, S. D. The impact of fish trawls on megabenthos (sponges) on the north-west shelf of Australia. Fish Res. 58, 141-151, doi:10.1016/s0165-7836(01)00382-4 (2002). 7 Poiner, I. et al. Final Report on Effects of Trawling in the Far Northern Section of the Great Barrier Reef: 1991–1996. Vols. 1 and 2. CSIRO Division of Marine Research, Cleveland, Qld. (1998). 8 Sainsbury, K. J., Campbell, R. A. & Whitelaw, W. Effects of trawling on the marine habitat on the north west shelf of Australia and implications for sustainable fisheries management. Paper presented at Sustainable Fisheries Through Sustaining Fish Habitat, Aust. Fish Biol. Soc. Workshop, Canberra. Australian Government Publishing Service. (1992). 9 Pham, C. K. et al. Total marine fishery catch for the Azores (1950-2010). ICES J. Mar. Sci. 70, 564-577, doi:10.1093/icesjms/fst024 (2013). 10 Coelho, R. et al. Reduction of elasmobranch by-catch in the hake semipelagic near- bottom longline fishery in the Algarve (Southern Portugal). Fish. Sci. 69, 293-299, doi:10.1046/j.1444-2906.2003.00620.x (2003). 11 Clarke, M., Borges, L. & Officer, R. Comparisons of trawl and longline catches of deepwater elasmobranchs west and north of Ireland. J. Northwest Atl. Fish. Soc. 35, 429-442, doi:10.2960/J.v35.m516 (2005). 12 Muñoz, P. D. et al. Effects of deep-sea bottom longlining on the Hatton Bank fish communities and benthic ecosystem, north-east Atlantic. J. Mar. Biol. Assoc. U. K. 91, 939-952, doi:10.1017/s0025315410001773 (2011). 13 Piñeiro, C. G., Casas, M. & Bañón, R. The deep-water fisheries exploited by Spanish fleets in the Northeast Atlantic: a review of the current status. Fish Res. 51, 311-320, doi:10.1016/s0165-7836(01)00254-5 (2001). 14 Vinnichenko, V. I. Russian deep-sea investigations and fisheries In the northeast Atlantic in 2007. ICES Working Group on the Biology and Assessment of Deep-Sea Fisheries Resources. (2008). 15 Hareide, N.-R. & Garnes, G. The distribution and catch rates of deep water fish along the Mid-Atlantic Ridge from 43 to 61°N. Fish Res. 51, 297-310, doi:http://dx.doi.org/10.1016/S0165-7836(01)00253-3 (2001). 16 Machete, M., Morato, T. & Menezes, G. Experimental fisheries for black scabbardfish (Aphanopus carbo) in the Azores, Northeast Atlantic. ICES J. Mar. Sci. 68, 302-308, doi:10.1093/icesjms/fsq087 (2011). 17 Pajuelo, J. G., Gonzalez, J. A. & Santana, J. I. Bycatch and incidental catch of the black scabbardfish (Aphanopus spp) fishery off the Canary Islands. Fish Res. 106, 448-453, doi:10.1016/j.fishres.2010.09.019 (2010). 18 Bordalo-Machado, P. et al. The black scabbardfish (Aphanopus carbo Lowe, 1839) fisheries from the Portuguese mainland and Madeira Island. Sci. Mar. 73, 63-76, doi:10.3989/scimar.2009.73s2063 (2009). 19 Melo, O. & Menezes, G. M. Projecto de acompanhamento de experiencia de pesca dirigida ao peixe-relógio (Hoplostethus atlanticus)-FISHOR. Arquivos do DOP, Série Estudos. 4: 2002 (In Portuguese) (2002). 20 Jakobsdóttir, K. B. Biological aspects of two deep-water squalid sharks: Cetnroscyllium fabricii (Reinhardt, 1825) and Etmopterus princeps (Collett, 1904) in Icelandic waters. Fish Res. 51, 247-265, doi:10.1016/s0165-7836(01)00250-8 (2001). 21 Lorance, P. & Dupouy, H. CPUE abundance indices of the main target species of the French deep-water fishery in ICES Sub-areas V-VII. Fish Res. 51, 137-149, doi:10.1016/s0165-7836(01)00241-7 (2001).