A Bycatch Assessment of the Gillnet Monkfish Lophius Gastrophysus

Home , Argentine angelshark, Common skate, Lophius, Lophius piscatorius, Merlucciidae, Southern eagle ray

Fisheries Research 72 (2005) 81–95

A bycatch assessment of the gillnet monkﬁsh Lophius gastrophysus ﬁshery off southern Brazil Jose´ Angel Alvarez Perez∗, Roberto Wahrlich

Centro de Ciˆencias Tecnol´ogicas da Terra e do Mar-CTTMar, Universidade do Vale do Itaja´ı-UNIVALI, Cx. Postal 360, Itaja´ı SC CEP 88.302-202, Brazil Received 23 June 2003; received in revised form 7 September 2004; accepted 2 October 2004

Abstract

Bycatch production in the recently developed monkfish (Lophius gastrophysus) fishery off southern Brazil was assessed from 14 observer trips conducted by a chartered gillnet fleet during 2001. Catch composition and discard ratios were estimated in 523 selected sets conducted between latitudes 22◦44S and 34◦21S and longitudes 33◦37W and 52◦23W and between the 132 and 607 m isobaths. The monkfish constituted on average 40.7% of all organisms entangled in each observed set. Among non-targeted species geryonid crabs (mostly the royal crab, Chaceon ramosae) and spider crabs (Majidae) were the main components representing 22.6% and 8.5% of total entangled organisms, respectively. The remaining 23% included mostly teleosts and elasmobranchs, such as beard fish (Polimixia lowei), silver john dory (Zenopsis conchiffer), gulf hake (Urophycis cirrata), argentine hake (Merluccius hubbsi), angel shark (Squatina argentina) and various skates (Rajidae). Geryonid crabs and angel sharks were the most retained and processed bycatch components (88.8, 50.0% of numerical catches, respectively). Discard ratios were higher than 75% in all other species entangled by gillnets, including abundant or valuable species, such as the wreckfish (Polyprion americanus). Catch rates of large-size bycatch components, such as dolphins, birds, sharks, rays and the wreckfish were poorly correlated with fishing effort and seem to have been mostly affected by the overlap between these species concentrations or higher diversity areas and the southernmost monkfish fishing grounds. Geryonid and majid crabs were correlated with monkfish catches and fishing effort, being most frequently caught north of 29◦S. This pattern was related not only to a target/not-target species distribution area overlap, but also to an elevated vulnerability of these crustaceans to gillnet operations. Proposed measures for bycatch reduction in the monkfish fishery in future, include area closures within monkfish southern fishing grounds and effort reduction measures. Whereas the former would minimize mortality on wreckfish, angel shark and also royal crab populations, effort reduction would benefit particularly the royal crab, which constitutes a conflict aspect of deep-water trap and gillnet fishery development off southern Brazil. © 2004 Elsevier B.V. All rights reserved.

Keywords: Southern Brazil; Monkﬁsh; Deep-sea gillnet ﬁshery; Bycatch

∗ Corresponding author. Tel.: +55 47 341 7714; fax: +55 47 341 7715. E-mail address: [email protected] (J.A.A. Perez).

1. Introduction (eastern Canada and Grand Banks) and L. piscatorius and L. budegassa (the NW Iberian Peninsula) (Bruno Deep-water demersal fishing operations off south- et al., 2001; Kulka and Miri, 2001; Pineiro˜ et al., 2001). ◦ ◦ ern Brazil (20 S–34 S) have increased in recent years The new fishing and processing technology motivated as a response to (a) decreasing catch rates of mostly a great interest of the government and the fishing indus- overexploited shelf resources (Valentini et al., 1991; try, since it not only seemed to meet international mar- Haimovici, 1998) and (b) the expansion of interna- ket demands more adequately, but also caught mostly tional markets for traditionally discarded or poorly large and mature fish as compared to traditional trawl- known species. Although gillnet and longline deep- ing practices (Perez et al., 2002, 2003). water operations directed towards rockfish and sharks While the positive aspects of this new fishery were have existed, since mid 1980s (Barcellos et al., 1991; evident, its impact on the deep marine ecosystem, par- Haimovici et al., 1997; Peres and Haimovici, 1998), ticular due to bycatch of other commercial and non- deep-water fisheries development greatly acceler- commercial species, raised concern and required fur- ated after 1999, as a large part of the shrimp and ther investigation to provide ecological support for up- groundfish trawlers expanded their fishing grounds coming management actions. towards outer shelf and slope areas, aiming for During 2001, these operations were observed and re- emerging valuable resources, such as flatfishes (Par- ported in detail providing extensive technological and alichthys spp.), pink cusk-eel (Genipterus brasilien- biological information, which has been the basis for a sis), monkfish (Lophius gastrophysus), skates (fam- complete assessment of the monkfish fishery off south- ily Rajidae), argentinean squid (IIlex argentinus) and ern Brazil (Perez et al., 2002). As part of this monitor- deep-water lobster (Metanephrops rubellus)(Perez ing, the present study aims at producing an analysis on et al.,2001). bycatch of the Brazilian monkfish gillnet fishery as a In addition to this process, the Ministry of Agricul- preliminary assessment of its potential impact on the ture (Brazilian Government) launched in 1998 a deep- Southwest Atlantic deep-water ecosystem. water fishing development policy in an attempt to in- duce the economical exploitation of the outer bounds of Brazilian EEZ. This policy was based on the char- 2. Material and methods tering of foreign vessels by national companies and an intense technological and scientific monitoring of 2.1. Data collection and analysis these deep-water fishing operations. Together, such actions would allow (a) the improvement of the knowl- Monkfish gillnet fishery was conducted off south- edge on potential resources; (b) the evaluation of large- ern Brazil in 2001 by nine authorized vessels originally scale deep-water fishing operations profitability and (c) from Spain. These vessels were 26.7–39.6 m long with the absorption of adequate technologies for deep-water gross tonnage ranging between 72 and 362 t and frozen fishing, handling and processing. Since 2000, chartered stocking capacity ranging between 45 and 110 t. Fish- vessels using pots, bottom longlines, bottom gillnets ing trips included 24–86 sets, each of them consisting and otter trawls started to operate in 200–900 m deep of 60–400 stringed nets, which were kept immersed for areas off southern Brazil being fully monitored by ob- 110.6 h on average (±1.5 S.E.M.). The nets were 50 m servers and a VMS (Vessel Monitoring System) (Perez long and 13.5 meshes high and were anchored to the et al., 2003). sea floor by 60–80 kg weights. Mesh size used by all The monkfish has been one of the main targets iden- vessels was 280 mm (stretched mesh). tified in this fishing expansion process. In 2001, 8830 t Bycatch data were obtained during 14 gillnet fish- were landed, mostly by national trawlers (62%) and ing trips conducted by eight observed vessels between chartered gillneters (36%), the latter introducing in the January and December 2001 (Table 1). These data were area both the monkfish directed bottom gillnet fishing generated as part of a scientific cooperation program method and on board handling and processing prac- established between the Ministry of Agriculture and tices (Perez et al., 2002). This method is conducted in University of “Vale do Itaja´ı” (Santa Catarina State, other fishing areas of the Atlantic for L. americanus Brazil) (Perez et al., 2003). J.A.A. Perez, R. Wahrlich / Fisheries Research 72 (2005) 81–95 83

Table 1 Summary of the gillnet chartered vessels commercial trips off southern Brazil between January and December 2001, analyzed for bycatch assessment Vessel Period Latitude range Longitude range Depth Conducted tows Immersed Nets Monkﬁsh range (m) (analyzed) (analyzed) catch kg Antoxo 24 Jun–06 Aug −29.139 to −32.256 −47.796 to −50.153 283–574 24 (20) 7719 (1835) 39386 Belen 12 Jul–04 Sep −26.010 to −28.130 −46.010 to −49.500 289–443 49 (22) 15966 (2339) 103223 Eder sands 12 Jun–13 Aug −30.553 to −32.041 −48.440 to −50.038 318–508 50 (36) 16595 (3705) 231500 Juno 12 Jan–02 Mar −23.668 to −26.837 −41.736 to −45.845 300–425 46 (43) 17470 (5060) 123762 19 Jun–17 Jul −30.491 to −31.828 −48.150 to −49.987 338–450 47 (47) 17560 (7420) 125642 19 Sep–10 Nov −28.810 to −33.658 −33.620 to −51.050 244–535 41 (19) 12860 (2469) 28648 Slebech 04 Nov–20 Dec −22.730 to −28.993 −45.779 to −47.832 293–421 41 (39) 14418 (4578) 69386 South coast 24 Feb–30 Apr −23.682 to −24.749 −41.067 to −44.529 252–561 61 (27) 20358 (2689) 60149 18 Oct–17 Dec −23.070 to −23.820 −41.330 to −42.410 132–607 67 (58) 22857 (7410) 100914 Suffolk 04 Feb–06 Apr −24.007 to −25.681 −43.075 to −45.350 222–543 56 (36) 17346 (3487) 131557 chieftain 09 Apr–25 Jun −24.828 to −29.402 −44.573 to −48.201 245–420 47 (27) 18150 (3293) 53130 27 Jun–03 Sep −24.881 to −27.000 −44.661 to −52.383 314–483 61 (54) 23923 (7301) 131296 Titan 17 Jul–24 Sep −28.673 to −34.349 −47.430 to −51.702 243–520 63 (48) 21770 (14490) 95925 l6 Oct–11 Dec −28.830 to −33.940 −47.690 to −51.310 200–485 61 (47) 17750 (14500) 39256 Total 12 Jan–20 Dec −22.730 to −34.349 −33.620 to −52.383 132–607 714 (523) 244739 (80576) 1315674

Observers assessed the catch composition of 80,576 nets immersed during 523 selected fishing sets conducted between latitudes 22◦44S and 34◦21S and longitudes 33◦37W and 52◦23W, and between the 132 and 607 m isobaths (Table 1; Fig. 1). Nearly 40% of all nets immersed during one fishing set, were ran- domly selected for examination. This selection was conducted in intermittent periods during the gear re- trieval procedure. After each set, observers identified and quantified all organisms entangled. In some cases (i.e. invertebrates) specimens were frozen and brought to the laboratory for identification. Photographic and videographic material was also used on land to validate and complete identifications. Monkfish discards due to damage caused by predators and scavengers were also quantified after each tow. Numerical abundance of each entangled species (i) was expressed as the mean number of individuals per 100 nets (Ni). Total numerical catch (C) was further estimated for each ith species as:

Ni Ci = Cmk (1) Nmk Fig. 1. Geographic distribution of fishing sets conducted by the char- where Nmk is the mean number of monkfish caught tered gillnet fleet off southern Brazil from January to December 2001. in 100 nets and Cmk is the total number of monkfish Latitude and longitude are decimal transformed. 84 J.A.A. Perez, R. Wahrlich / Fisheries Research 72 (2005) 81–95 caught by gillnetters in 2001. Cmk was estimated using the total number of monkfish retained by gillnetters in 2001 (Crmk = 775.599) (Perez et al., unpublished data), corrected by the monkfish discard rate as estimated in this study (see results below). The retained catch (Cr) was estimated from each species mean individual processed weight (Wmi) and total processed weight (Wpi): (Wpi/Wmi) Cri = Crmk (2) (Wpmk/Wmmk)

Both Wmi, and Wpi were informed by the vessel’s fac- tory crew after each set according to the type of organ- Fig. 2. Catch composition, in numbers, of bottom gillnet operations ism (monkfish, other finfish, elasmobranchs and crabs. conducted off southern Brazil during 2001. Table 6). Discards were estimated by subtracting the retained catch (Cr) of each recorded species (i) from its total catch (Ci) and were also expressed as a percentage cetaceans catches were occasionally reported of Ci. (Table 5). Fishing data were pooled in three latitudinal Fourteen taxa composed numerically 96% of gill- strata (North, 21◦S–25◦S; Center, 25◦S–29◦S; South, net catches (Fig. 2). The monkfish, the dominant and 29◦S–34◦S) (Fig. 1). A Principal Component Anal- target species, constituted on average 40.7% of total ysis (PCA) included catch rates of 14 catch compo- catches in numbers. Geryonid crabs (mostly the royal nents (number of individuals per 100 nets) and abiotic crab, Chaceon ramosae) and spider crabs (Majidae) variables: depth (depth), decimal latitude (lat), deci- represented 22.6 and 8.5% of total catch, respectively. mal longitude (long), soaking time (time) and num- The remaining 23% included mostly teleosts, such as ber of immersed nets per fishing set (nets). Selected beard fish (Polymixia lowei), silver John dory (Zenopsis catch components included ten species numerically conchiffer), gulf hake (Urophycis cirrata) and argen- important in the catches and four groups of species tine hake (Merluccius hubbsi)(Fig. 2). (skates, sharks, cetaceans and birds), which were con- Monkfish products made up 88.2% of the gill- sidered critical elements of gillnet bycatch. All vari- net fishery processed catch in weight. The rest of ables were standardized as a proportion of the mean. products processed included principally teleosts, elas- A correlation matrix was calculated for the standard- mobranchs and geryonid crabs (Table 6). Estimated ized variables and new axes (factors, linear combina- monkfish discards reached 6.1% and were due to tions of the original variables) were extracted in the flesh damage caused by scavengers during the im- direction of greatest variance and used to interpret mersion period. Geryonid crabs and angel sharks variables associations in a reduced number of dimen- (Squatina spp.) were the most retained and pro- sions. cessed bycatch components (88.8 and 49.3% of numerical catches, respectively). The yellowtail amberjack (Seriola sp.), although rarely present in the sets, 3. Results also had 67.7% of its numerical catches retained. Discard ratios were higher than 75% in all other 3.1. Catch composition and discards species entangled by gillnets, including abundant or valuable species, such as the wreckfish, the argen- Observed catches of gillnet hauls off southern Brazil tine hake, the gulf hake, the silver John dory, etc. included a total of 101 species (Tables 2, 3, 4 and 5). (Table 6). Beard fish, an abundant teleost, was totally Elasmobranchs, teleosts and crustaceans were discarded. the most diverse groups comprising 78% of Estimated absolute catches in numbers of non-target all identified species. Sea turtles, sea birds and species ranged from 33 to 459,833 in invertebrate J.A.A. Perez, R. Wahrlich / Fisheries Research 72 (2005) 81–95 85

Table 2 Invertebrate components of the deep-water gillnet ﬁshery off southern Brazil Family Species Common name I/N Sp: Monkﬁsh ratio Catch Cnidarians – Antipatharia n.i.a Black coral – – – – Gorgonacea n.i. Aa Gorgonian – – – – Gorgonacea n.i. Ba Gorgonian – – –

Molluscs Volutidae Odontocymbiola simulatrixa –0.033 0.00033 273 Adelomelon riosia –0.155 0.00155 1280 Xenophoridae Xenophora caribaeaa –2.033 0.02035 16809 Octopodidae Eledone massyaea –––– Eledone gauchaa –––– Vosseledone charruaa –0.004 0.00004 33 Ommastrephidae Illex argentinusa Argentine shortﬁn squid 0.048 0.00048 396 Total 2.273 0.02276 18800

Crustaceans Callapidae Acanthocarpus alexandria –0.392 0.00392 3238 Galatheidae Munida spp.a Squat lobster – – – Geryonidae Chaceon ramosaeb Chaceon notialisb Royal crab, red crab 55.606 0.55669 459833 Lithodidae Lithodes cf. turkayia King crab – – – Paralomis cf. longidactylaa King crab – – – Majidae Rochinia crassaa Spider crab 20.935 0.20959 173124 Libidoclaea granariaa –– – Nephropidae Metanephrops rubellusa Deep-sea lobster – – – Nephropsis aculeataa Deep-sea lobster – – – Parthenopidae Parthenope pourtalesiia –––– Polychelidae Polycheles typhlopsa –––– Portunidae Bathvnectes piperitusa –––– Scalpellidae Scalpellidae n.i.a 0.153 0.00153 1264 Cirolanidae Bathvnomus giganteusa, B. miyareia 6.708 0.06716 55475 Total 83.794 0.83890 692942

Echinodernis Cidaridae Cidaroida n.i.a –2.958 0.02961 24458 – Valvatida n.i.a –0.145 0.00145 1198 Total 3.103 25664

The number of individuals caught in 100 nets (I/N) was estimated in a total of 80,576 nets sampled during 14 fishing trips of chartered vessels conducted between January and December 2001. Sp: monkfish, numeric ratio between number of bycatch species and number of monkfish caught in 100 nets; catch, number of individuals caught by the gillnet fishery off southern Brazil estimated from a total of 826,013 monkfish caught in 2001 and the Sp: Monkfish ratio. a Discarded species. n.i., non-identified. b Non-target retained species. species, 41 to 23,954 in elasmobranches, 41 to 119,665 on average, being quantitatively less important in in teleosts and 8 to 711 in turtle, cetacean and bird very large or very small species (Fig. 3). In addi- species (Tables 2–5). Indirect mortality impacts tended tion, the elevated fishing impact on geryonid crab was to be higher in organisms between 200 and 1000 g noteworthy. 86 J.A.A. Perez, R. Wahrlich / Fisheries Research 72 (2005) 81–95

Table 3 Agnathan and cartilaginous fish components of the deep-water gillnet fishery off southern Brazil Family Species Common name I/N Sp: Monkfish ratio Catch Agnats Myxinidae Mixinidae n.i.a Hagfish 0.005 0.00005 41 Total 0.005 0.00005 41

Elasmobranchs Callorhynchidae Callorhynchus callorhynchusa Elephant fish – – – Chimaeridae Hydrolagus sp.a Chimera 0.005 0.00005 41 Alopiidae Alopias sp.b Thintail thersher 0.012 0.00012 99 Carchariidae Carcharias taurusb Sand tiger shark 0.006 0.00006 50 Carcharhinidae Carcharhinus falciformisb Silky shark 0.236 0.00236 1949 Carcharhinus sjgnatusb Night shark 0.105 0.00105 867 Prionace gjaucab Blue shark 0.019 0.00019 157 Galeocerdo cuvierib Tiger shark 0.086 0.00086 710 Sphyrna lewinib Scalloped hammerhead 0.418 0.00418 3453 Echinorhinidae Echinorhinus brucusa Bramble shark 0.552 0.00553 4378 Hexanchidae Hexanchus griseusa, Bluntnose sixgill shark, 0.267 0.00267 2205 Heptranchias perloa sharpnose sevengill shark Lamnidae Isurus oxyrinchusb Shortfin make – – – Lamna nasusb Porbeagle – – – Scyliorhinidae Schroederichthyes Catshark 0.004 0.00004 33 saurisgualusa Scyliorhinus haeckellia, S. Freckled catshark, 0.554 0.00555 4584 besnardia polkadot catshark Squalidae Squalus megalopsa Shortnose spurdog 1.476 0.01478 12208 S. asper Roughskin spurdog Etmopterus sp.a Lanternshark – – – Scymnodon obscurusa Smallmouth velvet –– – dogfish Squatinidae Squatina argentinac Argentine angelshark 1.052 0.01053 8698 Triakidae Galeorhinus galeusb Tope shark 0.004 0.00004 33 Dasyatidae Pteroplatytrigon violaceaa Pelagic stingray – – – Mobulidae Mobula sp.a Devil ray 0.098 0.00098 809 Myliobatidae Myliobatis goodeib Southern eagle ray 0.015 0.00015 124 Dasyatis sp.b Stingray – – – Rajidae Atlantoraja cyclophorab Eyespot skate 0.458 0.00458 3783 Atlantoraia casteunauib Spotback skate 0.108 0.00108 892 Dipturus menniib, D. Longnosed skate 2.897 0.02900 23954 trachydermab Torpedinidae Torpedo puelchaa Argentine torpedo 1.275 0.01258 10391 Total 9.652 79710

Table 4 Bony fish components of the deep-water gillnet fishery off southern Brazil Family Species Common name I/N Sp: Monkfish ratio Catch Carangidae Decapterus sp.a Scad 0.132 0.00132 1090 Seriola sp.b Yellowtail amberjack 0.170 0.00170 1404 Centriscidae Notopogon fernandezianusa Orange bellowfish 0.005 0.00005 41 Gempylidae Ruvettus pretiosusa Oilfish 0.066 0.00061 504 Lophiidae Lophius gastrophvsusc Monkfish 99.886 1.00000 826013 Macrouridae Malacocephalus occidentalisc Western softhead granadier 0.012 0.00012 99 Malacanthidae Lopholatilus villariib Tilefish 1.811 0.01813 14976 Caulolatilus chrysopsb Atlantic goldeye tilefish 0.010 0.00010 83 Merlucciidae Merluccius hubbsib Argentine hake 7.622 0.07631 63033 Ogcocephalidae Ogcocephalus notatusa Batfish 0.01 I 0.00011 91 Ophidiidae Genypterus brasiliensisb Pink cusk-eel 0.146 0.00146 1206 Peristidiidae Peristedion sp.a Armoured searobin 0.128 0.00128 1057 Phycidae Urophycis cirratab Gulf hake 9.176 0.09186 75878 Pinguipedidae Pseudopercis numidab Namorado sandperch 0.373 0.00373 3081 Polymixiidae Polymixia loweya Beardfish 14.470 0.14487 119665 Serranidae Polyprion americanusa, Wreckfish, snowy grouper 1.240 0.01241 10251 Epinephelus niveatusb Scombridae Katsuwonus pelamisa, Auxis Skipjack tuna, frigate tuna 0.057 0.00057 471 thazard thazarda Thunnus sp.b Yellowfin tuna 0.022 0.00022 182 Scorpaenidae Helicolenus dactylopterus Blackbelly rosefish 0.128 0.00128 1057 dactylopterusa Sparidae Pagrus pagrusa Common seabream 0.006 0.00006 50 Trachichthyidae Gephyroberyx darwinib Darwin’s slimehead 0.384 0.00384 3172 Trichiuridae Evoxymetopon taeniatusa Channel scabbardfish 0.083 0.0083 1 6864 Triglidae Prionotus punctatusa Bluewing searobin 0.006 0.00006 50 Xiphiidae Xiphias gladiusb Swordfish 0.496 0.00497 4105 Zeidae Zenopsis conchifferb Silver John dory 10.146 0.10158 83906 Total 146.586 302048

3.2. Spatial patterns birds and cetaceans were mostly entangled in hauls conducted in the southern stratum. Catches in numbers per net decreased towards The association among samples was analyzed from southern grounds due to a reduction in crustacean, the scores produced by the first three calculated PCA teleost and, less importantly, equinoderms (Fig. 4). This factors that explained together 65.1% of the total vari- pattern was clearly exhibited by geryonid crab catches, ance (Factor I, 34.3%; Factor II, 16.7%: Factor III, whereas majid crabs and the abundant beard fish and 13.9%) (Table 7). The bi-dimensional representation of the silver John dory were mostly caught in the north- the first two factors, which explained 51% of the total ern stratum decreasing sharply southwards (Fig. 4). The variance, depicted two main groups of bycatch compo- wreck fish and other large organisms, such as sharks, nents whose presence in the gill net sets were highly 88 J.A.A. Perez, R. Wahrlich / Fisheries Research 72 (2005) 81–95

Table 5 Chelonids, birds and cetaceans components of the deep-water gillnet ﬁshery off southern Brazil Family Species Common name I/N Sp: Monkﬁsh ratio Catch Chelonids Cheloniidae Eretmochelys imbricataa Hawksbill turtle – – – Dermocheliidae Dermochelys coriaceaa Leatherback turtle 0.001 0.00001 8 Total 0.001 0.00001 8

Birds Procellaridae Procellaria aequinoctialisa White-chinned petrel 0.005 0.00005 41 Diomedea spp. Albatross – – – Daption capensisa Cape petrel 0.001 0.00001 8 Pufﬁnus gravisa Greather shearwater 0.005 0.00005 41 Procellaridae n.i. 0.086 0.00086 711 Total 0.097 0.00097 802

Cetaceans Delphinidae Stenella coeruleoalbaa Stripped dolphin Stenella sp.a 0.002 0.00002 16 Delphinus sp.a 0.009 0.00009 70 Delphinidae n.i. 0.019 0.00019 157 Total 0.030 0.00030 248

correlated. Large organisms, such as the cetaceans, wreckfish, skates, angel shark and other sharks composed the first group, which presented high negative weight in the first rotated component (Table 7, Fig. 5). This group was represented in the left end of the first component greatly opposing the high positive weight of both latitude and longitude (both negative values) and secondarily depth, suggesting that their occurrence was predominant in southern upper slope fishing grounds. The second group was defined by the correlation between monkfish, royal crab, spider crab and silver John dory whose loadings were determined by their high scores in both factors (Fig. 5). This spatial representation suggests that the occurrence of such organisms tended to be related to deep central and northern fish- Fig. 3. Size variation of bycatch components of the monkfish gillnet fishery off southern Brazil. Mk, monkfish; Tf, tilefish; Wf, wreckfish; ing grounds as well as effort variables, in particular, im- Hk, argentine hake; Be, beardfish; Sd, silver John dory; Sk, various mersion time and number of nets (Table 7). An opposed skates; An, angel shark; Sh. various sharks; Ch, royal crab; Sc, spider pattern was shown by the argentine hake, scored in the crab; Bt, Bathynomus; Bd, seabirds; Ct, cetaceans. Sp: monkfish, fourth quadrant, and less conspicuously by seabirds. numeric ratio between number of bycatch species and number of Also isolated from bycatch associations, the abundant monkfish caught in 100 nets. Number of individuals caught by the gillnet fishery off southern Brazil, estimated from a total of 826,013 isopod Bathynomus was slightly correlated with im- monkfish caught in 2001 and the Sp: Monkfish ratio. mersion time. J.A.A. Perez, R. Wahrlich / Fisheries Research 72 (2005) 81–95 89

Table 6 Composition of processed catch landed by chartered gillnet vessels off southern Brazil between January and December 2001 and estimates of number of individuals retained, individuals discarded and numeric discard ratio Species Processed % Wm (kg) Sp: Monkfish ratio Total number Total number Discard weight (kg) (processed catch) retained discarded ratio (%) Bony fishes Monkfish 1121840 88.16 4.2 1.00000 775599 50414 6.1 Tylefish 7670 0.60 7.0 0.00411 3168 11790 78.7 Gulf hake 6347 0.50 1.0 0.02380 18456 57422 75.7 Swordfish 5636 0.44 30.0 0.00070 546 3559 86.7 Wreckfish 3311 0.26 9.0 0.00138 1070 9181 89.6 Argentine hake 2689 0.21 1.0 0.01008 7819 55214 87.6 Yellowtail amberjack 1307 0.10 4.0 0.00123 950 454 32.3 Silver John dory 872 0.07 0.8 0.00409 3170 80736 96.2 Slimehead 518 0.04 3.0 0.00065 502 2670 84.2 Yellowfin tuna 121 0.01 9.0 0.00005 39 143 78.5 Brazilian sandperch 95 0.01 7.0 0.00005 39 3042 98.7 Pink cusk-eel 40 0.00 5.0 0.00003 23 1183 98.1 Various teleosts 180 0.01 Total 1150626 90.40

Cartilaginous ﬁshes Various sharks 20080 1.58 12.0 0.00627 4866 25901 84.2 Various skates 21122 1.66 5.0 0.01584 12284 27669 69.3 Angel shark 11810 0.93 8.0 0.00553 4293 4405 50.7 Total 49784 4.17

Crustaceans Royal crab 68858 5.41 0.56 0.46100 357554 102279 22.2 Total 68858 5.41

Total 1272496 100.00

When variables were plotted according to the scores tal catch composition was considered, it could be esti- determined by Factors I and III (which together rep- mated that for every monkfish landed 1.02 non-targeted resented 48.2% of the total variance), the association organisms were discarded in 2001. This value, while between bycatch components was sustained except for much lower than the ratios normally produced by trawl- the displacement of the royal crab to the third quadrant, ing practices worldwide, would still place this fishery separated from monkfish, spider crabs and the silver among the ones with elevated discard ratios by number John dory (Fig. 5). This new representation likely re- (ratios ranging from 12.3 to 0.39), according to Natural flects the higher negative weighting exhibited by fish- Resources Consultants, NRC world bycatch database ing depth in factor III (Table 7), suggesting that the (Alverson et al., 1994). presence of royal crab is associated to deeper grounds. Abundant catches of monkfish, crabs, angel sharks and skates indicated that gillnet catch efficiency seemed to be principally related to highly mobile bot- 4. Discussion tom dwellers. Pelagic and demersal finfish, elasmobranchs and benthic invertebrates, although also vul- The deep-water gillnet fishery developed off south- nerable, were less frequently entangled in the immersed ern Brazil was efficient in selecting its primary target, nets. Cetaceans, turtles and birds were rare, and proba- the monkfish L. gastrophvsus. Nevertheless, when to- bly, caught in surface waters during net deployment as 90 J.A.A. Perez, R. Wahrlich / Fisheries Research 72 (2005) 81–95

Fig. 4. Catch rate (individuals, per 100 nets) latitudinal variation of monkfish and bycatch components of the deep-water gillnet fishery off southern Brazil between January and December 2001. (A) All major groups of organisms; (B) teleosts; (C) elasmobranchs; (D) crustaceans; (E) other invertebrates; (F) large vertebrates. North (19◦S–25◦S), Center (25◦S–29◦S), South (29◦S–34◦S). reported by observers. Because this procedure is con- This hypothesis was further supported by fact that en- ducted with the vessel moving at five to six knots, the tangled birds and dolphins were often highly damaged nets tend to remain stretched as they sink. Birds and dol- by scavengers and in some cases only carcasses were phins, normally seen in the vicinity of the vessel during found. such operation, may become vulnerable to sinking nets, Regardless of catch rate variation of non-target particularly considering that these are not completely species, the elevated fishing effort as generated by ap- cleaned after a fishing set and often maintain attractive proximately 180,000 h of immersion of over 611,000 residues from the previous catch (Cox et al., 2004). nets, may have induced a significant unintended mor- J.A.A. Perez, R. Wahrlich / Fisheries Research 72 (2005) 81–95 91

Fig. 5. Spatial representation of correlations between bycatch components and geographic and effort variables scored by the first three factors obtained from the Principal Component Analysis. (A) Factor I against Factor II; (B) Factor I against Factor III. Tf, tilefish; Wf, wreckfish; Hk, argentine hake; Be, beardfish; Sd, silver John dory; Sk, various skates; An, angel shark; Sh, various sharks; Ch, royal crab; Sc, spider crab; Bt, Bathynomus; Bd, seabirds; Ct, cetaceans. tality on such species which were poorly retained or sible impact scenarios at the population level should completely discarded. Particularly relevant, were dis- be made taking into account generally known life his- cards of species already exploited and even targeted tories, demographic and fishery patterns of the main by deep-water trawling, longlining and trapping off discarded species. In this sense, species targeted by southern Brazil, such as the silver John dory, the ar- other commercial fisheries (that already support di- gentine hake, the wreckfish the tilefish, skates, sharks rected fishing mortality) and long-lived species hav- and the royal crab (Haimovici et al., 1997; Peres and ing low reproductive and natural mortality rates (re- Haimovici, 1998; Avila-da-Silva´ et al., 2001; Perez et ferred to as k-strategists) would be particularly sus- al., 2003). Consequences of such losses on popula- ceptible to incidental mortality as induced by bot- tions or ecosystems are uncertain at the moment, since tom gillnet fishing (Alverson et al., 1994; Jeenings et they may not be a direct function of numbers of dis- al.,1998; Hall, 1999; Cook, 2001; Stobutzki et al., 2001, cards (Cook, 2001). However, inferences of some pos- 2002). 92 J.A.A. Perez, R. Wahrlich / Fisheries Research 72 (2005) 81–95

Table 7 essentially increase by 50% the proposed sustainable Principal Component Analysis employed to evaluate the associations effort levels. Royal crab bycatch has been, therefore, an between catch components (individuals, per 100 nets) of the deep- important element concerning the development of both water gillnet fishery off southern Brazil and variables related to effort and fishing areas deep-water gillnet and trap fisheries in Brazil (Perez et al., 2002). Variables Factors Regarded as fully exploited and highly susceptible I II III to overfishing, the wreckfish has been the main target Imersion time, time (h) −0.229 0.699 0.196 of a longline fleet established off southern Brazil since Decimal latitude, lat 0.968 −0.053 −0.207 the 1980s (Peres and Haimovici, 1998; Haimovici et . . − . Decimal longitude, long 0 849 0 045 0 420 al., 1997). Despite the elevated fishing effort exerted Fishing depth, depth (m) 0.413 0.015 −0.535 Number of nets, nets 0.120 0.857 −0.020 by this fleet, chartered longline vessels were autho- Monkfish, Mk 0.297 0.579 0.293 rized to operate during 2000 in areas already occupied Tylefish, Tf 0.326 0.060 0.765 by national vessels, introducing a substantial additional Wreckfish, Wf −0.969 0.158 0.029 effort (Peres and Haimovici, 1998; Perez et al., 2003). . − . . Argentine hake, Hk 0 195 0 603 0 160 Although these operations were unauthorized shortly Beardfish, Be 0.100 −0.203 0.062 Silver John dory, Sd 0.394 0.673 0.170 after, through fishing depth limitations, it seems that Various skates, Sk −0.792 0.039 −0.108 the impact on the wreckfish stock persisted off southern Angel shark, An −0.916 0.167 0.056 Brazil through gillnet incidental catches. In this area, Various sharks, Sh −0.915 0.195 −0.153 an estimate of 10,200 individuals or over 90 t (consid- . . − . Royal crab, Ch 0 317 0 459 0 769 ering that entangled wreckfish weighted around 9 kg) Spider crab, Sc 0.408 0.593 0.470 Bathynomus,Bt −0.277 0.315 −0.714 may have been caught in 2001, 96% of which were Seabirds, Bd 0.211 −0.021 0.002 discarded at sea characterizing an extreme scenario of Cetaceans, Ct −0.772 0.047 −0.118 high grading (sensu Alverson et al., 1994). According Eigenvalue 6.519 3.181 2.648 to the official landing statistics, this discarded biomass Variance explained (%) 34.311 16.742 13.938 in 2001 may have reached nearly 15% of all wreckfish landed in Brazil (MMA, 2003). Considering that Values shown for all variables are standardized. The linear coeffi- cients of the variables in the first three factors rotated by the PCA are the stock has been declining since 1998, the impact of indicated. The eigenvalues and the variance explained by each factor gillnet incidental catch in 2001 may have been even are indicated in the last two rows. more significant suggesting that such fishing interac- tion should be one of the critical elements considered The royal crab was the most abundant bycatch in in the establishment of monkfish fishery management the monkfish gillnet fishery and has recently moti- measures in Brazil. vated a valuable chartered trap fishery off southern Longnosed skates (Diptururs spp.) were the elas- Brazil (Perez et al., 2003). Although its biology is still mobranchs most abundantly caught by monkfish gill- poorly understood, like all other studied geryonids, the nets off southern Brazil. Catches of spurdogs (Squalus species is probably long lived, grows slowly and ma- sp.), argentine torpedo (Torpedo puelcha), angel sharks tures after 5–15 years (Hastie, 1995). In 2001, a total (Squatina argentina), bramble sharks (Echinorhinus of 1770 t were caught off southern Brazil; 9.16% of the spp.), catsharks (Scyliorhinus spp.) and other species 11,636.4 t virgin biomass estimated for the entire fish- were also significant. Although most of these species ing area (Pezzuto et al., umpublished data). According have just recently been commercially exploited by to these authors, the nine gillnet vessels in operation in multispecific deep-water trawling (Mazzoleni and 2001 were able to catch together around 30 t in 1 month, Schwingel, 1999; Perez et al., 2001, 2003), the un- which was roughly the monthly production of one trap intended mortality exerted by monkfish gillnets may vessel. Considering that only two chartered trap ves- produce a significant impact on their sustainability be- sels would suffice to catch the estimated 593.5 t MSY cause they (a) tend to be highly susceptible to capture (Maximum Sustainable Yield) in a 12-month fishery by such fishing gear and (b) exhibit a limited ability for the species (Pezzuto et al., unpublished data), inci- to recover depletion (Stobutzki et al., 2002). Benthic dental mortality, as induced by such gillnet fleet, would longnosed skates, for example, have been regarded as J.A.A. Perez, R. Wahrlich / Fisheries Research 72 (2005) 81–95 93 particularly sensitive to fishing mortality as they gen- 8 turtles and 802 birds were estimated to be entan- erally attain large sizes, mature late and lay a limited gled by deep-water gillnets; the latter, including mostly amount of eggs cases on the seabed (Brander, 1981; the oceanic petrels Procellaria aequinoctialis, Daption Jeenings et al., 1998; Dulvy et al., 2000). capensis and Puffinus gravis. The former species also S. argentina has been commonly found year round composes the bycatch produced by the pelagic tuna off Rio Grande do Sul State (30◦S–34◦S) and is the longline fishery conducted at the south Atlantic sub- less abundant of the three angel shark species cap- tropical convergence which annually can catch 2650 tured by the fishing practices conducted in the region birds (Vaske, 1991). Since the 1970s, Puffinus gravis (Haimovici et al., 1997; Mazzoleni and Schwingel, has been subjected to a significant incidental mortal- 1999). The numerous incidental catch produced ity induced by gillnetting for halibut and flounder in by monkfish gillnetting in 2001 (8698 individu- Monterrey Bay (Hall, 1999). Annual bird catches esti- als) suggests that the development of this fishery mated for this fishery reached roughly 20,000 individu- off southern Brazil may not only generate a sub- als between 1979 and 1987. Whereas the figures above stantial increase in population mortality, but also suggest that the impact of the developing monkfish introduce adverse effects in the recruitment pro- fishery off southern Brazil on these non-commercial cess, considering that the species reproductive cy- k-strategists is relevant and requires continuous moni- cle may exceed one year (Cousseau and Perrota, toring, its magnitude may not represent a major source 1998). In fact, in the other angel shark species occurring of concern at the moment. off southern Brazil (S. guggenhein and S. oculta)a3- The impact of gillnet operations on the ecosystem year reproductive cycle has been estimated and recruit- off southern Brazil exhibited latitudinal as well as ef- ment overfishing has been diagnosed for all of them fort components. Firstly, bycatch abundance decreased (Vooren, 1997; Perez et al., 2001). Restricted latitudi- and changed its basic composition southwards as small nal and depth ranges may also affect the elasmobranchs teleosts, crustaceans and other invertebrates tended to susceptibility to capture by the monkfish gillnet fishery be replaced by large teleosts, elasmobranchs, cetaceans (Stobutzki et al., 2002). In that sense, it can be general- and birds. Furthermore, catch rates of large compo- ized that, as the monkfish, the species above are bathy- nents, such as dolphins, birds, sharks, rays and the metrically limited to the outer shelf and slope grounds wreckfish were poorly correlated with fishing effort and of the southwest Atlantic. Unlike the target species, seem to have been mostly affected by the overlap be- however, they tend to concentrate south of 29◦S, being tween these species concentration or higher diversity captured off southern Brazil at the northern boundary areas and the southernmost monkfish fishing grounds. of their latitudinal distribution range. Efforts to ensure Conversely, geryonid and majid crabs were correlated their sustainability as bycatch species of a developing with monkfish catches and fishing effort being most monkfish fishery, therefore, may consider the limita- frequently caught north of 29◦S; a pattern that sug- tion of fishing effort at the southernmost slope grounds gests not only a target/not-target species distribution of Brazilian EEZ. area overlap, but also an elevated vulnerability of such Non-commercial k-strategists impacted by deep- crustaceans to bottom gillnet operations. water gillnet fishing operations conducted off southern Alverson et al. (1994) observed that discards in Brazil, included dolphins, birds and turtles. One dol- tropical regions were mostly dominated by small- phin was killed for every 12.8 t of landed monkfish, an bodied animals, whereas temperate and sub-polar fish- impact that approximates the one exerted by a similar eries discarded mainly commercially important larger- bottom gillnet fisheries conducted in the Gulf of Maine, bodied species. In the north Atlantic, such a trend where one dolphin is killed for every 10 t of landed seems to be consistent with patterns exhibited by groundfish (Alverson et al., 1994). Whereas such mor- deep-water fish fauna which tend to be less diverse tality is highly concentrated in one local stock in the and dominated by larger species towards higher lati- latter fishery, off southern Brazil, however, the fishing tudes (Merret and Haedrich, 1997). In general, monk- impact seems to occur in a large geographical area and fish gillnet catch composition seems to reflect the to be spread over several species included in the gen- same pattern considering that the coast off southern era Delphinus and Stenella. In addition, approximately Brazil (19◦S–34◦S) is influenced by the seasonal in- 94 J.A.A. Perez, R. Wahrlich / Fisheries Research 72 (2005) 81–95 teraction between tropical and subtropical regimes of contribute to minimize mortality of highly vulnerable the South Atlantic ocean and has been regarded as crustaceans, particularly the royal crab, which consti- a transitional zoogeographical zone (Palacio,´ 1982). tutes a conflict aspect of deep-water trap and gillnet Whereas such trend has been often confirmed by the fishery development off southern Brazil (Perez et al., latitudinal distribution patterns of different zoological 2002). groups on the continental shelf and upper slope regions (Figueiredo, 1981; Haimovici and Perez, 1991), in deeper areas, where hydrographic variation is less Acknowledgements pronounced, diversity changes have been more subtle ´ (Haimovici et al., 1994; Avila-da-Silva, 2002). The authors are indebted to all members of the Char- In any case, the latitudinal distribution of the monk- tered Fleet Observers Program for their hard work fish gillnet fisheries bycatch off southern Brazil seems and the quality of collected data. We also thank ves- to be consistent with distribution patterns defined either sel owners, captains and crew members of all mon- by deep-water fishing activities or scientific surveys. itored vessels for their support and good will dur- In particular, primary concentration areas of wreckfish ing the long fishing trips. Mauricio Hostim Silva, and royal crab have been defined by commercial fleets ◦ ◦ ◦ ◦ Paulo Ricardo Schwingel. Andre Barreto, Paulo Ri- between 28 S and 30 S and 27 S and 30 S, respec- cardo Pezzuto, Joaquim Olinto Branco (UNIVALI) tively (Peres and Haimovici, 1998; Perez et al., 2003). and Gustavo Augusto Schmidt de Mello (Zoology Longline experimental fishing conducted on the up- Museum, University of Sao˜ Paulo) provided identi- per slope off southern Brazil confirmed the (a) pre- fications of several taxa essential for this work. The dominance of the wreckfish and argentine-hake at the Ministry of Agriculture (Brazilian Government) pro- southern and northern extremes of the study area, re- ◦ ◦ vided funds for this study through a scientific co- spectively (22 S–28 S), as well as (b) the relatively ho- operation program with “Universidade do Vale do mogeneous latitudinal distribution of the gulf hake and Itaja´ı” (MA/SARC/03-2000; MAPA/SARC/DPA/03- ´ tilefish (Avila-da-Silva, 2002). A southward increase 2001; MAPA/SARC/DENACOOP/126-2002). of cetacean diversity has been partially supported by a biogeographical analysis of species occurrences off Brazilian coast (Siciliano and Oliveira, 2002). The bycatch produced by the monkfish fishery de- References veloped off southern Brazil in 2001, was dominated Alverson, D.L., Freeberg, M.G., Murawsky, S.A., Pope, J.G., 1994. by organisms that were also important in the bycatch A global assessment of fisheries bycatch and discards. FAO Fish- of other monkfish fisheries in the Atlantic (Marteens, eries Technical Paper 330. 2000; Bruno et al., 2001). In some of them, bycatch Avila-da-Silva,´ A.O., 2002. A evoluçao˜ da pesca de linha-de-fundo production has been one major concern of fishery man- e a dinamicaˆ de populaçao˜ do peixe-batata, Lopholatilus vil- agement plans which tended to include actions, such as larii (Teleostei: Malacanthidae) na margem continental da costa brasileira entre os paraleios 22◦ e28◦S. 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