Aspects of the Biology and Fishery of Lophius Gastrophysus Miranda-Ribeiro, 1915 (Lophiiformes, Lophiidae) in Southeastern Brazil

ICES CM2007/K:19 Theme Session Monkfish across the world: common problems and commons solutions

Aspects of the biology and fishery of Lophius gastrophysus Miranda-Ribeiro, 1915 (Lophiiformes, Lophiidae) in southeastern Brazil

Maria de Fátima Moraes Valentim, Marcelo Vianna and Erica Pellegrini Caramaschi

Universidade Federal do Rio de Janeiro, Instituto de Biologia. Avenida Pau Brasil, 21941- 590, Ilha do Fundão, Rio de Janeiro, Brasil. E-mail: [email protected]

ABSTRACT

Historically, Lophius gastrophysus has been considered a bycatch of the trawler fleet, but it was intensively exploited between 2000 and 2002 because of its high value in the international fish market, resulting in a reduction in the catch during that period. On account of this, a management program for fishery in Brazilian waters was developed to promote sustainable use of such resource. In 2005, measures for commercial exploitation of L. gastrophysus were established through a normative instrument edited by the government. However, the biological basis of this regulatory tool was derived from research on other species of Lophius in the Atlantic Ocean. In order to provide information to guide future changes in legislation and to generate basic biological data on L. gastrophysus ; specimens of this species landed by the trawler fleet of the state of Rio de Janeiro were studied. L. gastrophysus spawning took place primarily between spring and summer. Fishes with size less than the one at the first sexual maturation estimated for females (50 cm) were considered juvenile. The most important category in the diet was fish, which showed the highest IAi. Trawl fishery takes place at a depth of 50 to 130 m, where double-rig nets with a net opening of about 24 m are used. Trips in the sea last about 12 days, making six trawls per day. Data obtained showed that specimens caught by the trawling fleets were mainly of the "small" commercial category, that is, juveniles, which congregate in shallower areas. CPUE values were higher between the end of spring and beginning of summer, coinciding with the reproductive peak of the species. Steps to implement and enforce effective measures, to reduce bycatch of L. gastrophysus by trawler fleet must be taken, to guarantee sustainable fishery for this species in Brazilian waters.

Key-words: Biology, fishery, Lophius gastrophysus , management, southeastern Brazil,

1 INTRODUCTION

The lack of knowledge on the availability of fishing resources on the external continental shelf and slope, associated to the high costs and risks when operating in such areas caused industrial fishery concentration in the internal part of the continental shelf in the southeastern and southern regions of the Brazilian coast up to the end of the 90s, in spite of the serious overfishing tendencies detected in the main demersal resources (e.g. Haimovici, 1998). This fact promoted a new direction in favour of the resources that had not been exploited before, thus focusing on the external continental shelf, as well as in the slope, in the same concentrated way, which potential sustainability is still unknown (Perez et al ., 2001). In 1998, the Agriculture Department, as well as the Cattle Raising and Supply Departments instituted an ocean-fishery program for national companies to be able to acquire foreign vessels through leasing, in an attempt to improve the knowledge of potential fishing resources for a rational occupation of the Brazilian Exclusive Economic Zone (EEZ). This program was implemented in the southern region in 2000, when the leased vessels began to operate at depths of 200 to 900 m using bow nets, gillnets and trawl nets (Perez et al ., 2001). In the subsequent years, besides these vessels acting in the capture of Lophius gastrophysus , the national vessels headed for deeper areas, causing a greater increase in the fishing effort, due to the high commercial value in the international market (Perez et al ., 2001; 2002). In this context, in less than five years L. gastrophysus moved from a subfishing condition to an overfishing threat, as depletion of stocks start to occur , fishing power tends to increase in order to face reduction of captures and to keep the yield. Historically, L. gastrophysus had been registered as a bycatch component of trawler fishery in the southeastern region of the Brazilian coast (Vianna & Almeida 2005). According to the project, Living Resources in the Exclusive Economic Zone (REVIZEE), no potentially important stocks were identified for Brazil. Even the ones considered as promising, as L. gastrophysus , responded to the increase of the fishing effort. To try to avoid a fast depletion of the stock of L. gastrophysus , a fishery management process of the species was implemented. Monitoring of the fishing activity and recommendations of the scientific and government sectors were also carried out. Brazil also agreed to implement the Conduct Code for responsible fishing (FAO, 1995). Management measures were established for commercial exploitation of L. gastrophysus through a government normative instrument (Brazil-MMA, IN - Nº 23, of July 4, 2005), a series of approaches and procedures were also established, such as: vessels nationality (Brazilian); maximum number of vessels

2 allowed (nine); fishing method (bottom gillnet); nets maximum limit to be transported by vessels (a thousand nets); gillnet mesh (280 mm between opposite knots); submersion time for nets (no more than 120 hours); minimum depth allowed (250 m); maximum annual limit allowed for capture (1500 tons gutted weight). However, to give support to this normative instruction, biological data from other species of Lophius in the Atlantic Ocean were used, due to the lack of information on L. gastrophysus at that time. Therefore, studies on such species are essential to help future changes in the legislation and to generate information on L. gastrophysus for a better management and sustainable approach on the fishery activity. Therefore, studies to enable an assessment for local population sustainability and to support effective management of fisheries are essential. In order to emphasize reproduction, feeding and fishery aspects, studies on L. gastrophysus , landed by the commercial trawler fleets of the Rio de Janeiro state, are being carried out.

MATERIALS AND METHODS

Reproductive and feeding biology

During April/2004 and March/2006 454 individuals of L. gastrophysus caught by commercial fishing trawlers and landed in the fishing port of Niteroi, in Rio de Janeiro State were acquired. For each individual, the following data were registered: total length (Lt-cm), total weight (Wt-g), liver weight, sex, maturity stage and ovaries weight. The mean size at first sexual maturity (L 50 ) was obtained for females, using King (1995) modified logistic curve. The gonadosomatic and hepatosomatic index (GSI and HSI) were estimated for females. Spawning period was estimated through the temporal frequency analysis of the maturity stages and variation of the GSI and HSI mean values. The frequency of occurrence method (Hyslop, 1980) and weight percentage were applied to characterize the diet. They were combined in the Alimentary index (IAi) proposed by Kawakami and Vazzoler (1980).

Fishery and yield

In order to assess how commercial trawler fleets operate on L. gastrophysus , 47 interviews were carried out with different vessel skippers from March/2004 to February/2006, in the fishing port of Niteroi, in Rio de Janeiro state. An overall count number, of 13.926 of L. gastrophysus individuals, was recorded. Fishes were landed gutted in two commercial categories: small (under 1.0 kg) and large (over 1.0 kg). Size structure analyses of L.

3 gastrophysus were carried out by grouping frequency distribution of individuals in the two commercial categories. The number of size classes was stipulated according to the Sturges formula (k= 1+log 2 n; where k= number of classes, n= number of individuals analyzed). Each class interval was defined according to the Siegel formula (Ci = λ/nc; where ci= classes intervals, nc= number of classes, λ= variation in amplitude of the length. Seasonal abundance was estimated by analysis of the catch per unit effort (CPUE). The records for weight (kg) of the total catch per landing of L. gastrophysus were divided by the number of landings for the two study periods. In order to assess recruitment, the estimated value of L50, obtained for females, was calculated. Such value is considered an estimate of the length at which 50% of the population samples begin their sexual maturity.

RESULTS Reproductive and feeding biology

Size variation in amplitude of the individuals analyzed from 8.9 to 76.0 cm (mean 48.2 ±SD13.2 cm). The mean size at first maturity for females was recorded 50 cm (Figure 1). The period of maximum reproductive activity was registered between August and January, which corresponds to early spring and mid-summer seasons. Unlike the values observed for GSI, lower values of HSI were obtained during this period (Figure 2). Maximum GSI value for females was 12.5%. We identified 40 food items, grouped into four categories: fish, molluscs, crustaceans, and others. Fish was the principal category in the diet (Figure 3), with 25 identified species distributed in 20 families. Among the identified species, flying gurnards Dactylopterus volitans, argentine hake , Merluccius hubbsi and rough scad Trachurus lathami showed the highest IAi rate.

Fishery and yield Variation in amplitude of L. gastrophysus measured in the fishing port was from 15.6 to 83.0 cm (mean 40.6 ±SD 11.0 cm). Overall sampling measurement presented 5.911 (42.4%) for small and 8.015 (57.6%) for large commercial categories (Figure 4), where only 20.6% of the individuals presented a higher mean size at first sexual maturity estimated for females (L 50 =50.0 cm), that is, they were adults (Figure 1) . Seasonality and percentage frequency of occurrence of juveniles and adults is shown in Figure 5. A slight increase on adults landing was observed in spring and summer months on the two-year study.

4 Interviews carried out next to skippers of the boats showed that all the trawlers that landed fish at the sampling location, as well as for L. gastrophysus were outfitted with double-rig trawl nets, having a mean total length of 20.4± S.D. 2.4 m, engines of 296.2±42.5 HP, a crew of 5.9±0.6, a net opening of about 23.0±2.2 m with 159 kg ±24.0 kg otter boards, and an average work of 12.0±2.3 days at sea, with 5.9±0.3 hour hauls, making four hauls per fishing day, operating in depths from 50 to 130 m. Samplings carried out for two consecutive years showed that capture of individuals for the large commercial category increased during the mid summer months (November- December), decreasing on the subsequent term. This result was not evident for the landed individuals, which belonged to the small category, except for Nov-Dec in 2005, when a high fluctuation was registered (Figure 6). The production landed was an estimate of the 160 landings and the CPUE average value was of 618.5 ± S.D. 474.6 kg for small and 3.224.06 ±1.626.6 kg for large categories.

DISCUSSION

Individuals analyzed for the reproductive biology studies, as well as for the feeding studies showed to be larger than the ones analyzed by Soares et al . (1993), which were caught in the internal continental shelf, but similar to the ones recorded by Muto et al . (2005) that examined samples collected in the external continental shelf and slope area. The same area used by the commercial trawler fleet, where the material for the present study was obtained. Size determination at first sexual maturity is important information when stocks that are being exploited have to be assessed, as they provide adequate information to establish capture and consequent minimum nets mesh size (Branco et al ., 2002). In the present study, the estimated value for females showed to be lower than the one registered for congeneric species (Azevedo, 1996; Duarte et al ., 2001; Landa et al ., 2001). Several studies have demonstrated a long spawning period for the species of the genus Lophius (e.g. Armstrong et al ., 1996). For L. piscatorius and L. budegassa , Quincoces et al . (1998ab) observed reproductive periods from May to August and from April to July, respectively, that is, between spring and summer. For L. gastrophysus spawning took place primarily from August to January, which corresponds to spring and summer months. In L. gastrophysus an inverse relationship between GHI and HSI was recorded, suggesting that weight loss during maturation was probably caused by the gonad development process. Liver alterations during this period have been associated more to the vitellinic precursor supply than to energetic mobilization reserves. The

5 same result was observed for a congeneric species of L. litulon (Yoneda et al ., 2001). According to the authors, in teleost and in other vertebrates, yolk precursor protein, called vitellogenin (vitellogenesis) is synthesized in the liver. In this study, diet composition of L. gastrophysus showed that this species is essentially piscivorous, with fish predominance in the stomach contents. Previous studies have highlighted the importance of fish in the L. gastrophysus diet (Soares et al ., 1983; Muto et al ., 2005). Tendency for a greater consumption of fish was also observed by different authors for congeneric species (e.g. Crozier, 1985; Armstrong et al ., 1996). In the present study, the feeding spectrum of L. gastrophysus showed a wide variety of preys, such as the ones observed by Crozier (1985) and Laurenson & Priede (2005) for L. piscatorius , which were called opportunistic feeders. In the present study, the size of L. gastrophysus specimens measured in the landings was similar to the one registered by Lopes (2005) when analyzing L. gastrophysus specimens coming from leased foreign vessels that acted basically in the southern region. However, their samples indicated a marked predominance of adult individuals, leading the author to suggest that the capture of larger fishes would be associated to gillnet selectivity. In the same way, Bruno et al . (2001) analyzing L. piscatorius in Spain noted that practically all specimens captured by gillnet were adults, whereas specimens captured by trawl were juveniles. The predominance of juveniles in our analysis suggests that the commercial trawler fleet that lands individuals in the fishing port of Niteroi, seems to be acting with higher intensity on the L. gastrophysus juveniles. Such situation can be related to the low selectivity level of trawler catch used by these vessels, or even a reflex of the operation carried out by these vessels in low-depth areas, with a dominance of small fishes. Caddy (1993) reported that this was a general rule for demersal species exploited with small trawl mesh. Perez et al. (2002), when analyzing L. gastrophysus landing in the southern region, stated that smaller and immature individuals were found in low-depth areas, while the larger ones, as well as adults were in the deeper areas. Perez et al . (2005) demonstrated that among the analyzed fishing modalities, the double-rig is one of the mostly used methods with greater impact. In this context, these results require special consideration as data obtained in the present study were obtained from trawl landing and according to the government normative instrument as the capture of this species is limited to gillnet. The catch per unit effort (CPUE) for individual biomass or number is an important abundance index in the assessment and management studies of fishing stocks, specially when surveys are not available. The highest catches per unit effort can be related to different

6 factors. For Lophius , one of the reasons cited is the spawning aggregation (e.g., Bruno et al ., 2001). Vianna et al . (2005), when analyzing the Brazilian Institute for the Environment and Renewable Natural Resources (IBAMA) official landing data observed that the highest captures of L. gastrophysus occurred in spring. In the present study, the highest CPUEs were recorded in late spring and early summer, coinciding with the spawning season observed for this species in this work. The largest catches were also observed by Vianna & Almeida (2005) in this period, associating peak catch rates to the incursion of the South Atlantic Central Water (SACW), as they reported that L. gastrophysus showed a restricted distribution related to this cold water mass. Probably, the largest catches of L. gastrophysus by the trawler fleet in Southeastern Brazil are related to the greater availability of resources in shallower waters which follow the SACW, providing a more feasible catch of species to the less-specialized fleet. All these factors require special consideration regarding this kind of fishery sustainability, not only because of the L. gastrophysus catch as a target species, but also because of the bycatch. We urgently recommend that effective measures be implemented and enforced, to reduce the bycatch of L. gastrophysus by commercial trawler fleet, in order to guarantee sustainable fishery for this species in Brazilian waters.

ACKNOWLEDGMENTS

This research was financially supported by UFRJ-UNIVALI agreement (Contract UNIVALI- SEAP/PR/001/2003). We are grateful to CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for Maria de Fátima M. Valentim’s doctoral scholarship. We thank Manuela Azevedo for suggestions on the manuscript, skippers Sebastião da Silva for obtaining the samples analyzed in this study, and other fishermen in the fishing port of Niteroi for making available the individuals measured during this study.

REFERENCES

Armstrong, M.P.; Musick, J.A & Colvocoresses, J.A. 1996. Food and ontogenetic shifts in feeding of the goosefish , Lophius americanus. Journal of Northwest Atlantic Fishery Science , 18: 99-103 . Azevedo, M. 1996. Contribution to the study of the biology of black monkfish, Lophius budegassa, spinola (ICES Division VIIIc and IXa). Boletim Instituto Portugues Investigacao Maritima , IPIMAR-Lisboa, 2:5-13 Branco, J.O.; Lunardon-Branco, M.J. & Souto, F.X. 2002. Estrutura Populacional de Portunus spinimanus Latreille (Crustacea, Portunidae) na Armação do Itapocoroy i, Penha, Santa Catarina, Brasil. Revista Brasileira de Zoologia . 19(3): 731-738 Brasil, Ministério do Meio Ambiente, Secretaria Especial de Aqüicultura e Pesca da Presidência da República. Instrução Normativa, Nº 23, de 4 de Julho de 2005. Dispões sobre critérios e procedimentos para o ordenamento da pesca do peixe-sapo ( Lophius gastrophysus) nas águas jurisdicionais brasileiras das regiões Sudeste-Sul, entre o paralelo

7 21º00’ S e limite Sul da Zona Econômica Exclusiva brasileira (ZEE) e dá outras providências. Diário Oficial da República Federativa do Brasil, Brasília, 128, Seção 1, Quarta-feira, 6 de Julho de 2005. Bruno, L.; Faria, A.C.; Landa, J. & Morlan, R. 2001. The gillnet fishery for anglerfish (Lophius piscatorius ) in deep water in the Northwest of Iberian Peninsula. Scientific Council Meeting . NAFO.SCR.01/99. Crozier, W.W. 1985. Observations on the food and feeding of the angler-fish Lophius piscatorius L., in the northern Irish Sea. Journal Fish Biology , 27: 655-665. Duarte, R.; Azevedo, M.; Landa, J. & Pereda, P. 2001. Reproduction of anglerfish ( Lophius budegassa Spinola and Lophius piscatorius Linnaeus) from the Atlantic Iberian coast. Fish. Res. 51:349-361. Food and Agriculture Organization of the United Nations (FAO).1995. Code of conduct for responsible fisheries: background, purpose, content and role www.fao.org/docrep . (11.01.2006) Haimovici, M. 1998. Present state and perspectives for the southern Brazil shelf demersal fisheries. Fisheries Management and Ecology. 5:277-289. Hyslop, E.J. 1980. Stomach content analysis a review of methods and their application. Journal Fish Biology , 17, 411-429. Kawakami, E. & Vazzoler, G., 1980. Método gráfico de índice alimentar aplicado no estudo de alimentação de peixes. Boletim do Instituto Oceanográfico , 29(2), 205-207. King, M. 1995. Fisheries biology assessment and management . Fishing New Books. Osney Mead, Oxford, England. Landa, J.; Pereda, P.; Duarte, R. & Azevedo, M. 2001. Growth of anglerfish (Lophius piscatorius and L. bu degassa) in Atlantic Iberian waters. Fisheries Research, 51: 361- 376. Laurenson, C.H. & Priede, I.G. 2005. The diet and trophic ecology of anglerfish Lophius piscatorius at the Shetland Islands, UK. Journal of the Marine Biological Association of the United Kingdom, 85: 419-424 Lopes, F.R.A. 2005. Reprodução, idade de crescimento do peixe-sapo ( Lophius gastrophysus ) (Ribeiro, 1915) na região sudeste e sul do Brasil. Dissertação de Mestrado. Universidade do Vale do Itajaí – UNIVALI. 66p. Muto, E.Y. & Silva, M.H.C., Vera, G.R., Leite, S.S.M., Navarro, D.G. & Rossi- Wongtschowski, C.L.D.B., 2005. Alimentação e relações tróficas de peixes demersais da plataforma externa e talude superior da região sudeste-sul do Brasil. Série Documentos REVIZEE-Score Sul . pp. 64. Perez, J. A. A.; Pezzuto, P. R.; Vale, W. G.; Ribas, T. M. & Soares, G. S. 2001. Padrões espaciais e temporais de pesca da frota camaroneira industrial de Santa Catarina: implicações na explotação da fauna acompanhante e no ordenamento . Notas Técnicas FACIMAR , 5: 35-58 Perez, J.A.A.; Pezzuto, P.R. & Andrade, H.A. 2005. Biomass assessment of the monkfish Lophius gastrophysus stock exploited by a new deep-water fishery in southern Brazil. Fisheries Research , 72:149-162. Perez, J.A.A.; Wahrlich, R.; Pezzuto, P.R.; Schwingel, P.R.; Lopes, F.R.A. & Rodrigues- Ribeiro, M. 2002. Deep-sea fishery off southern Brazil: recent trends of the Brazilian fishing industry. J. Northw. Atl. Fish. Sci . 31:1-18. Quincoces, I.; Lucio, P. & Santurtún, M. 1998b. Biology of black anglerfish (Lophius budegassa) in the Bay of Biscay waters, during 1996-1997. ICES Council Meeting papers , CM/O:47

8 Quincoces, I.; Santurtún, M. & Lucio, P. 1998a. Biological aspects of white anglerfish (Lophius piscatorius) in the Bay of Biscay (ICES Divison VIIIa, b, d) in 1996-1997. ICES Council Meeting papers , CM/O:48. Soares, L.S.H., Gasalla, M.A., Rios, M.A.T., Arrasa, M.V. & Rossi-Wongtschowski, C.L.D.B. 1993. Grupos tróficos de onze espécies dominantes de peixes demersais da plataforma continental interna de Ubatuba, Brasil. Publção. Esp. Inst. Oceanogr. São Paulo . 10:189-198 Vianna, M. & Almeida, T. 2005. Bony fish bycatch in the southern Brazil pink shrimp (Farfantepenaeus brasiliensis and F. paulensis ) fishery. Braz. Arch. Biol. Technol . 48(4):611-623. Vianna, M.; Valentim, M.F.M. & Filho, A.L.E.S. 2005. Análise do desembarque da frota de arrasto industrial no Rio de Janeiro, com estudo de caso do peixe-sapo ( Lophius gastrophysus ). Relatório Técnico Cientifico do Comitê Consultivo Permanente de Gestão dos Recursos Demersais de Profundidade (CPG/Demersais)/SEAP/PR, DOC 14 SCC CPG 03 2005 Yoneda, M.; Tokimura, M.; Fujita, H.; Takeshita, N.; Takeshita, K.; Matsuyama, M. & Matsuura, S. 2001. Reproductive cycle, fecundity, and seasonal distribution of the anglerfish Lophius litulon in the East China and Yellow seas. Fishery Bulletin , 99: 356- 370.

9 100

25 Proportion adults females adults Proportion

4 2 0 4 2 6 4 8 6 -3 4 -4 -5 -6 -7 <20 8 0 8 0 2 20-2 24-28 2 32-36 36- 4 44-48 4 52-5 56-60 6 64-6 68-72 7 Length (cm)

Figure 1– Proportion (%) of adults females of L. gastrophysus , per size classes. Arrow indicates mean size at first sexual maturity.

14 N=15 12 N=15

10 N=18 8

N=27 N=21 6 N=7 N=12 Average values Average 4 N=37 N=13 N=15 2 N=8 N=22

0 AprMay4 JunJul4 AugSep4 OctNov4 DecJan5 FebMar5 AprMay5 JunJul5 AugSep5 OctNov5 DecJan6 FebMar6

GSI HSI

Figure 2– Mean values of the gonadosomatic (GSI) and hepatosomatic (HSI) index of adults females of L. gastrophysus (N= number individual examined).

7.7%

91.5% 0.5% 0.3%

Fish Molluscs Crustaceans Others Figure 3 – Alimentary index (IAi%) of the items consumed by Lophius gastrophysus

10 100

50 Proportion

0 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61 63 65 67 69 71 73 75 77 79 81 Length (cm) Small Large

Figure 4- Proportion (%) of Lophius gastrophysus landed in the small and large categories, per size classes from March 2004 to February 2006. Arrow indicates mean size at first sexual maturity for females.

100

50 Proportion Proportion

5 5 04 05 05 05 06 r/0 / eb/ n/0 ec b/ rAp yJu D nFe ulAug/ a a ulAug/ a MarApr/04 MayJun/04 J SepOct/04 NovDec/04 JanF M M J SepOct/05 Nov J Juveniles Adults Figure 5– Proportion (%) of Lophius gastrophysus landed in the fishing port from March 2004 to February 2006.

2100 N=11 1800

1500 N=9 1200 N=12 N=11 900 N=12 N=20 N=8 N=15 N=22 N=13 N=18 N=9

CPUE(Kg/landing) 600

300

4 4 4 4 4 5 5 5 5 5 5 6 0 0 0 0 0 0 0 0 0 0 0 0 / / / / / / / / / / / / r t c r t c n g c b n g c b p u u e e p u u e e J J A A O D F A A O D F r y l p v n r y l p v n a a u e o a a a u e o a J S J J S J M M N M M N Large Small Mixed Total Figure 6– Values of CPUE (kg/n olanding) of Lophius gastrophysus landed at the fishing port of Niteroi, Rio de Janeiro state, from March 2004 to February 2006. (N= number of landing)