The Impact of Shrimp Trawl Bycatch on Fish Reproduction in Northeastern Brazil

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The impact of shrimp trawl bycatch on fish reproduction in northeastern Brazil

Aline da Costa Bomfim1* Daniel Solon Dias Farias1 Iara Cecília da Costa Morais2 Silmara Rossi3 Simone Almeida Gavilan4 Flávio José de Lima Silva5

1. Biólogo(a) e Doutorando(a) do Programa de Pós-Graduação em Desenvolvimento e Meio Ambiente (Universidade Federal do Rio Grande do Norte, Brasil). 2. Bióloga e Mestra em Ciências Naturais (Universidade Federal do Rio Grande do Norte, Brasil). 3. Bióloga (Pontifícia Universidade Católica de Campinas). Doutora em Ecologia Aplicada (Universidade de São Paulo, Brasil). 4. Bióloga e Doutora em Psicobiologia (Universidade Federal do Rio Grande do Norte, Brasil). 5. Biólogo (Fundação de Ensino Superior de Olinda). Doutor em Psicobiologia (Universidade Federal do Rio Grande do Norte). Professor da Universidade do Estado do Rio Grande do Norte, Brasil. *Autor para correspondência: [email protected]

In the west coast of Rio Grande do Norte many small-scale fisheries targeting mostly shrimp but accidentally catch a large number of

CT fish. Our aim was to evaluate the Ichthyofauna composition and distribution in Potiguar Basin, northeastern Brazil, in order to elucidate the impact of bycatch on fish reproduction. The study area was divided into four stretches (A, B, C and D), and we sampled

TRA 1,426 specimens classified into 10 orders, 23 families and 49 species. We obtained biometric data and gonadal tissue in order to determine the reproductive aspects of the studied fish. Stretch A had the highest values of evenness and dominance; the highest

ABS values of abundance, biomass, richness and diversity were found in stretches B, C and D. Analysis based on faunal similarity revealed three groups: I (found in stretches B and D), II (C), and III (A). In regards to reproductive phase, 76.3% of the specimens were classified as 'immature', 16.7% as 'maturing' and 7% as 'mature'. Through the anatomical and histological analyzes of the gonads and the size of first maturation, we verified that the species Pomadasys corvinaeformes, Menticirrhus littoralis and Larimus breviceps were negatively related to fishing activity; on the other hand, Pellona harroweri was positively related. Our findings indicate that the incidental capture of some non-target species can affects predominantly individuals considered immature, i.e. without reproductive potencial, an indicative of non-sustainable fishing in region.

Keywords: coastal zone; diversity; ichthyofauna; reproductive stages; sexual maturity.

O impacto da pesca acessória do arrasto camaroeiro na reprodução de peixes no nordeste do Brasil

Na costa oeste do Rio Grande do Norte, muitas pescarias de pequena escala têm como alvo principal camarões, mas acidentalmente capturam um grande número de peixes. Nosso objetivo foi avaliar a composição e distribuição da ictiofauna na Bacia Potiguar, Nordeste do Brasil, a fim de elucidar o impacto das capturas acessórias na reprodução dos peixes. A área de estudo foi dividida em quatro trechos (A, B, C e D), e foram amostrados 1.426 espécimes classificados em 10 ordens, 23 famílias e 49 espécies. Obtivemos

RESUMO dados biométricos e tecido gonadal para determinar os aspectos reprodutivos dos peixes estudados. O Trecho A apresentou os maiores valores de equitabilidade e dominância; os maiores valores de abundância, biomassa, riqueza e diversidade foram encontrados nos trechos B, C e D. A análise baseada na similaridade faunística revelou três grupos: I (trechos B e D), II (C) e III (A). Em relação à fase reprodutiva, 76,3% dos espécimes foram classificados como “imaturos”, 16,7% como “em maturação” e 7% como “maduros”. Através das análises anatômicas e histológicas das gônadas e do tamanho da primeira maturação, verificamos que as espécies Pomadasys corvinaeformes, Menticirrhus littoralis e Larimus breviceps foram negativamente relacionadas à atividade pesqueira; Por outro lado, Pellona harroweri estava positivamente relacionada. Nossos achados indicam que a captura incidental de algumas espécies não-alvo pode afetar predominantemente indivíduos considerados imaturos, ou seja, sem potencial reprodutivo, um indicativo de pesca não sustentável na região.

Palavras-chave: diversidade, estágios reprodutivos, ictiofauna, maturidade sexual, zona costeira.

Introdução to mitigate the impacts generated by trawling (VAZZOLER, 1996). Coastal areas are exposed to continental and marine processes Studies on the diversity and reproduction of fish species in ecosystems capable of influencing the structural characteristics of ecosystems that with intense human activity, including fishing, are crucial and bring may affect the distribution patterns of fish communities (NERO; knowledgment to improve conservation plans. Thus, our study SEALEY, 2006). The constitution of coastal environments is fundamen- focused on evaluating the composition, distribution and reproductive tal to the biological cycles of several fish species. These environments aspects of the ichthyofauna in the Potiguar Basin, northeastern Brazil, have high concentrations of nutrients and thermohaline gradients that subject to different levels of fishing activity in order to elucidate the provide breeding refuges and support the initial feeding of early-age impact of bycatch on fish reproduction. specimens of a large number of species. These are relevant factors for the conservation of natural resources and biodiversity maintenance Material and Methods (LIVINGSTON, 2002). Many multi-target small-scale fisheries operate in the west coast Study area of Rio Grande do Norte (RN); small boats operate mainly in coastal This research was carried out in the northeastern Brazil, between waters using fishing gear such as gill nets and bottom trawls. The trawl Caiçara do Norte (5°4'1.15"S, 36°4'36.41"W) in Rio Grande do Norte fisheries target fish and shrimp; however, a large number of fish are State (RN) and Icapuı ́ (4°38'48.28"S, 37°32'52.08"W) in Ceará State accidentally captured (BOMFIM, 2014). These fish are often small- (CE), region known as Potiguar Basin; an area of approximately exten- sized juveniles, and therefore, of low economical value (SOUZA; sion of 300 km. CHAVES, 2007), rejected on board or discarded on sandy beaches, Since 2010, the Projeto Cetáceos da Costa Branca - Universidade characterizing bycatch (HELFMAN et al., 2009). High mortality rates of do Estado do Rio Grande do Norte (PCCB-UERN) in Brazil has conduc- juvenile fish may contribute to the decline of recreational and com- ted the Beach Monitoring Program in the Potiguar Basin (Programa de mercial species populations (HELFMAN et al., 2009), leading to a Monitoramento de Praias da Bacia Potiguar – PMP-BP). The PMP-BP is collapse of the current environmental balance and, consequently, part of an environmental constraint compliance enforced by the Bra- generating ecological and economical impacts. zilian Institute of the Environment and Renewable Natural Resources Understanding the reproductive stages of Brazilian fish, including (IBAMA) over oil exploitation operated by PETROBRAS (Petróleo of non-commercial species, as well as the depletion of natural stocks is Brasileiro S.A.) (agreement number 2500.005657510.2). paramount to administer, manage and create conservation measures Due to geomorphological features and enviromental characteris-

Biota Amazônia ISSN 2179-5746 Macapá, v. 9, n. 1, p. 37-42, 2019 Esta obra está licenciada sob uma Licença Disponível em http://periodicos.unifap.br/index.php/biota Creative Commons Attribution 4.0 Internacional Submetido em 18 de Setembro de 2018 / Aceito em 03 de Abril de 2019 tics, the monitoring area was divided into four stretches: (A) stages of gonadal maturation (MADDOCK; BURTON, 1999). Grossos/RN - Icapuı/́ CE, (B) Areia Branca/RN - Porto do Mangue/RN, Formalin-fixed gonadal tissue were routinely processed, sectioned 38 B n T

(C) Guamaré/RN - Macau/RN, and (D) Galinhos/RN - Caiçara do o h at 5 µm, stained with hematoxylin and eosin, and examined under light O r e M t

Norte/RN (Figure 1). i microscopy in order to confirm the sex and stage of gonadal matura- h F m e I M a tion by histological analysis. This procedure was carried out at the p s a , t A c e

Laboratory of Vertebrate Morphophysiology, Morphology Depart- t . r C o n . f e ment, Rio Grande do Norte Federal University (UFRN). B s t r h a a

All procedures for the sample collection were approved by the r l z i . m i Chico Mendes Institute for Biodiversity Conservation (ICMBio) - Minis- l p t

try of the Environment through the Biodiversity Information and r a

Authorization System (SISBIO) number 13694-6, and Authorization w l b

and Information in Biodiversity (ABIO) number 615/2015. y c a t c

Data analysis h o

The abundance in number of individuals and total biomass were n f i analyzed according to the identified taxonomic groups. In addition, we s h r

calculated the seasonal distribution of species and their occurrence e p

constancy during the studied year, according to the expression pro- r o d

posed by Dajoz (1978): C= n/N*100 (C= occurrence constancy; n= u c t

number of collections containing the species studied; N= total number i o Figure 1. Location of the studied area, Potiguar Basin, northeastern Brazil. of collections). The rainfall data for the study period was obtained n i from Proclima (Real-Time Climate Monitoring Program for the North- n Sample collection east) (http://www6.cptec.inpe.br/proclima/ accessed 31 Jan 2013). Samples were obtained monthly for 12 months (January - Decem- We analyzed the following community attributes according to the ber 2012) at the time of the drag. Trawl nets varied from 6 to 40 m monitored stretches: abundance in number of specimens, total bio- long X 3 m wide, and were usually made of mono or braided nylon mass, Shannon-Wiener diversity (H') (KREBS, 1989), Pielou's even- (also named “trammel”). Fishermen often use this type of trawl net to capture shrimp during the day, at an average depth of 1.5 m; however, ness (J) (PIELOU, 1989), and Margalef richness (d) (LUDWIG; other animals may also get caught, such as catfish, sauna, anchovy and REYNOLDS, 1988). The Chi-square test was performed to compare the other small fishes. stretches of studied area. In order to analyze faunal similarity among The studied specimens were stored in isothermal bags until arriv- the four areas we performed a cluster analysis using the Jaccard coeffi- ing at the support base, where the fishes were photographed, fixed in cient. 10% formalin, and preserved in 70% alcohol for further anatomical The ratio of captured specimens according to their different repro- identification by experts and according to previous studies (MENEZES; ductive phases (mature, maturing and immature), and the temporal FIGUEIREDO, 2000; SZPILMAN, 2000; JU NIOR et al., 2010;). Biometric distribution of gonadal maturation stages were also analyzed. The data (total length - TL, standard length - SL, total weight - TW, and ANOVA variance was performed in order to evaluate the relationship gonadal weight - GW), sex, and stage of gonadal maturation were between the GSI and the stage of gonadal maturation. The Levene's recorded. test revealed non-homogeneity among the groups, so a Welch F test The stages of gonadal maturation were classified as: immature, followed by the Tukey test was employed. Significance level (alpha) maturing and mature, considering the macro and microstructural was 0.05 for all tests. PAST version 2.14 and Statistica version 9.0 were aspects of the gonads and the mean values of the Gonadosomatic used to process all data. Index (IGS). The gonadosomatic index (GSI) is an indicator of gonadal func- RESULTS tional status represented by the percentage of the gonads in relationship to the body mass (GSI = GW/TW × 100) (WOOTTON et al., 1978). Ichthyofauna composition Maturation of germinative cells occurs simultaneously with the A total of 1,426 individuals classified into 10 orders, 23 families, increase of GW (LE CREN, 1951), therefore, the GSI is a good reference and 49 species of fish were captured (Table 1), with a total biomass of of the reproductive activity of fish, and can be used to determine the 33 kg.

Table 1. Seasonal distribution of the species and their Families, constancies of Occurrence (% C) and abundances in Percentage (PA). Numbers of voucher Family Especie Months %C PA specimens

J F M A M J J A S O N D

Haemulidae Pomadasys corvinaeformis (Steindachner, 1868) UFRN 2440 X X X X X X X X X 81.8 29.66 Sciaenidae Menticirrhus littoralis (Holbrook, 1847) UFRN 2447 X X X X X X X X X 81.8 6.87 Carangidae Selene brownii (Cuvier, 1816) UFRN 2456 X X X X X X X X X 81.8 3.57 Sciaenidae Menticirrhus americanus (Linnaeus, 1758) UFRN 2452 X X X X X X X X X 81.8 1.26 Sciaenidae Larimus breviceps (Cuvier, 1830) UFRN 2469 X X X X X X X X 72.7 9.04 Haemulidae Conodon nobilis (Linnaeus, 1758) UFRN 2451 X X X X X X X X 72.7 6.52 Engraulidae Lycengraulis grossidens (Spix & Agassiz, 1829) UFRN 2435 X X X X X X X X 72.7 3.64 Clupeidae Opisthonema oglinum (Lesueur, 1818) UFRN 2450 X X X X X X X 63.6 9.53 Ariidae Aspistor luniscutis (Valenciennes, 1840) UFRN 2434 X X X X X X X 63.6 3.56 Polynemidae Polydactylus virginicus (Linnaeus, 1758) UFRN 2453 X X X X X X X 63.6 1.96 Ariidae Bagre marinus (Mitchill, 1815) UFRN 2442 X X X X X X 54.5 2.85 Tetraodontidae Sphoeroides testudineus (Linnaeus, 1758) UFRN 2473 X X X X X X 54.5 2.38 Sciaenidae Macrodon ancylodon (Bloch & Schneider, 1801) UFRN 2437 X X X X X X 54.5 1.68 Pristigasteridae Pellona harroweri (Fowler, 1917) UFRN 2439 X X X X X 45.4 4.90 Sciaenidae Stellifer stellifer (Bloch, 1790) UFRN 2474 X X X X X 45.4 1.19 Carangidae Chloroscombrus chrysurus (Linnaeus, 1766) UFRN 2457 X X X X X 45.4 0.49 Paralichthyidae Etropus crossotus (Jordan & Gilbert, 1882) UFRN 2438 X X X X 36.4 0.56 Gerreidae Diapterus rhombeus (Cuvier, 1829) UFRN 2466 X X X X 36.4 0.35 Carangidae Selene vomer (Linnaeus, 1758) UFRN 2463 X X X 27.3 0.91 Ephippidae Chaetodipterus faber (Broussonet, 1782) UFRN 2471 X X X 27.3 0.49 Gerreidae Eucinostomus argenteus (Baird & Girard, 1855) UFRN 2468 X X X 27.3 0.42 Tetraodontidae Lagocephalus laevigatus (Linnaeus, 1766) UFRN 2433 X X X 27.3 0.35 Cont.

Biota Amazônia ISSN 2179-5746 Table 1. Seasonal distribution of the species and their Families, constancies of Occurrence (% C) and abundances in Percentage (PA). Cont. Numbers of voucher 39 B n Family Especie Months %C PA T o h specimens O r e M t i h F m e

J F M A M J J A S O N D I M a p s a , t A c Cynoglossidae Symphurus plagusia (Bloch & Schneider, 1801) UFRN 2454 X X X 27.3 0.35 e t . r C o n . Ariidae Bagre bagre (Linnaeus, 1766) UFRN 2462 X X 18.2 0.77 f e B s t r h a

Gymnuridae Gymnura micrura (Bloch & Scheneider, 1801) UFRN 2458 X X 18.2 0.56 a r l z i . m i

Paralichthyidae Syacium micrurum (Ranzani, 1842) UFRN 2448 X X 18.2 0.56 l p

Clupeidae Chirocentrodon bleekerianus (Poey, 1867) UFRN 2475 X X 18.2 0.49 t r a

Hemiramphidae Hemiramphus brasiliensis (Linnaeus, 1758) UFRN 2459 X X 18.2 0.42 w l

Triglidae Prionotus punctatus (Bloch, 1793) UFRN 2449 X X 18.2 0.42 b y c

Scomberomorus brasiliensis (Collette, Russo & Zavala- a Scombridae UFRN 2465 X X 18.2 0.42 t

Camin, 1978) c h

Dasyatidae Hypanus guttatus (Bloch & Schneider, 1801) UFRN 2472 X X 18.2 0.28 o n

Narcinidae Narcine sp. UFRN 2461 X 18.2 0.28 f i s Paralichthyidae Syacium papillosum (Linnaeus, 1758) UFRN 2476 X X 18.2 0.21 h r e

Haemulidae Genyatremus luteus (Bloch, 1790) UFRN 2464 X X 18.2 0.14 p r

Carangidae Trachinotus carolinus (Linnaeus, 1766) UFRN 2443 X X 18.2 0.14 o d u

Sparidae Archosargus rhomboidalis (Linnaeus, 1758) UFRN 2477 X X 18.2 0.07 c t i Gerreidae Eucinostomus gula (Quoy & Gaimard, 1824) UFRN 2481 X 9.1 0.91 o n

Haemulidae Haemulon steindachneri (Jordan & Gilbert, 1882) UFRN 2483 X 9.1 0.21 i n Carangidae Trachinotus falcatus (Linnaeus, 1758) UFRN 2478 X 9.1 0.21 Lutjanidae Ocyurus chrysurus (Bloch, 1791) UFRN 2445 X 9.1 0.14 Achiridae Trinectes paulistanus (Miranda Ribeiro, 1915) UFRN 2460 X 9.1 0.14 Gerreidae Eucinostomus melanopterus (Bleeker, 1863) UFRN 2468 X 9.1 0.14 Narcinidae Narcine bancrofti (Grifith & Smith, 1834) UFRN 2436 X 9.1 0.07 Lutjanidae Lutjanus alexandrei (Moura & Lindeman, 2007) UFRN 2441 X 9.1 0.07 Sciaenidae Micropogonias furnieri (Desmarest, 1823) UFRN 2480 X 9.1 0.07 Dasyatidae Hypanus marianae (Gomes, Rosa & Gadig, 2000) UFRN 2484 X 9.1 0.07 Rhinobatidae Pseudobatos percellens (Walbaum, 1792) UFRN 2455 X 9.1 0.07 Carangidae Caranx latus (Agassiz, 1831) UFRN 2482 X 9.1 0.07 Haemulidae Haemulon plumieri (Lacepède, 1801) UFRN 2479 X 9.1 0.07

The orders Perciformes (N=27) and Pleuronectiformes (N=5) plumieri (Lacepède, 1801), Haemulon steindachneri (Jordan & Gilbert, represented 65% of the sampled species (Figure 2A), followed by 1882), Bagre bagre (Linnaeus, 1766), Lutjanus alexandrei (Moura & Clupeiformes (N=4), Rajiformes (N=3), Siluriformes (N=3), Tetraodon- Lindeman, 2007), Narcine bancrofti (Griffith & Smith, 1834), Narcine tiformes (N=2), Torpediniformes (N=2), Myliobatiformes (N=1), Scor- sp., Gymnura micrura (Bloch & Scheneider, 1801), and Trinectes paeniformes (N=1) and Beloniformes (N=1). paulistanus (Miranda Ribeiro, 1915); while ten species were captured The families Carangidae, Sciaenidae, Haemulidae, Gerreidae, solely during dry season (August - December): Trachinotus carolinus Ariidae and Paralichthyidae were the most commonly observed; a (Linnaeus, 1766), Eucinostomus melanopterus (Bleeker, 1863), total of 54% of the sampled species (Figure 2B). Eucinostomus gula (Quoy & Gaimard, 1824), Syacium micrurum The analysis of total abundance indicated that 67.6% of the sam- (Ranzani, 1842), Ocyurus chrysurus (Bloch, 1791), Chirocentrodon pled individuals were classified into Order Perciformes, including two bleekerianus (Poey, 1867), Hypanus marianae (Gomes, Rosa & Gadig, of the most abundant species: Larimus breviceps (Cuvier, 1830) and 2000), Pseudobatos percellens (Walbaum, 1792), Archosargus Pomadasys corvinaeformis (Steindachner, 1868). Together, these two rhomboidalis (Linnaeus, 1758), Prionotus punctatus (Bloch, 1793). In species represented 38.9% of all captured specimens (Figure 2C). In regards to species occurrence during rainy and dry season, the most regards to biomass, the order Perciformes was the most prevalent prevalent were, respectively, Opisthonema oglinum (Lesueur, 1818), P. (54.7%) (Figure 2D). corvinaeformis, L. breviceps and Pellona harroweri (Fowler, 1917), and P. corvinaeformis and Lycengraulis grossidens (Spix & Agassiz, 1829) 60 55 14 1212 50 12 (Table 1). 10 40 10 The species occurrence was higher at Mel de Baixo, Porto do 8 8 %

30 % Mangue, Minhoto, and Caiçara do Norte beaches (Figure 3). 6 6 6 4 4 4 4 4 20 4 10 Number of species 10 8 2 2 2 2 2 2 2 2 2 2 2 2 6 6 4 4 2 2 2 2 40 Sampling eﬀort 14 0 0 e e e e e e e e e e e e e e e e e e e e e e s s s s s s s s s e a a

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e e e n e e e e e e e e e e e e e e e e e i r m m m m m m m m m m m m m m m m m m m m r r r r r r r r r r r r r r r r r r r r r a o fo fo fo fo fo fo fo fo o fo fo fo fo fo fo fo fo fo fo fo e i i i ji i i i i if i i i i i ji i i i i i C t t t c t r t t P rc e r a c n n n a r e a c in n n P e up ilu R on e ae lo di b e on up ilu R e d lo ba ae P Cl S od on rp Be pe lio P od Cl S on pe Be lio rp ra ur o or y ra ur or y o et le Sc T M et le T M Sc Stretch A Stretch B Stretch C Stretch D T P Order T P Order Beaches of the Costa Branca RN Figure 2. Animals caught in the Potiguar Basin, northeastern Brazil: (A) proportion of species (%) Figure 3. Distribution of occurrence of ish species in the Potiguar Basin, northeastern Brazil. by taxonomic order; (B) proportion of species (%) by families; (C) numerical abundance, (D) total biomass. Analysis of the community attributes indicated that stretch "A" had The occurrence of the species discarded by shrimp trawling was the lowest values of abundance, biomass, diversity and richness, and distributed as accidental (54%), constant (27%) and accessory (19%), the highest values of evenness and dominance among all four moni- according to Dajoz (1978). Twelve species were captured only during tored area. Stretches "B" and "D" presented the highest abundance, the rainy season (January - July): Caranx latus (Agassiz, 1831), biomass and richness values and "C" presented intermediate values in Trachinotus falcatus (Linnaeus, 1758), Micropogonias furnieri comparison to "B" and "D". Regarding Shannon diversity, the highest (Desmarest, 1823), Genyatremus luteus (Bloch, 1790), Haemulon values were observed for stretches "B" and "C", followed by "D". The

Biota Amazônia ISSN 2179-5746 dominance variable values were higher for "A" and "D" due to the Variations on these values were consistent with the stages of gonadal dominance of species Aspistor luniscutis (Valenciennes, 1840) and P. maturation (Figure 6). 40 B n T o h corvinaeformis, respectively. Variations were more discreet in terms of O x x

6 5 r e A B M t i evenness, with the highest and lowest values for "A" and "D" stretches, h F 5 m

4 e I M a respectively (Figure 4). 4 p s a ,

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0,8 0,5 Stages of gonadal maturation Stages of gonadal maturation o 0,4 d 0,6 Figure 6. Gonadosomatic index (GSI) of stages of gonadal maturation: (A) Pellona harroweri; (B) u E D 0,3 0,4 c 0,2 Larimus breviceps; (C) Menticirrhus littoralis, (D) Pomadasys corvinaeformis. t i 0,2 0,1 o 0 0 n i Stretch A Stretch B Stretch C Stretch D Stretch A Stretch B Stretch C Stretch D Analysis of the sampled species and the period in which the study n Monitoring stretches Monitoring stretches was conducted demonstrated that P. harroweri had the highest relative Figure 4. Total values (rainy and dry) of abundance, biomass, Shannon diversity, richness, evenness, frequency of "mature" individuals (60%) in January. After this period, and dominance in diﬀerent stretches of monitoring in the Potiguar Basin, northeastern Brazil. the occurrence of mature individuals decreased, and there was a Faunal similarity along the monitored area could be divided into simultaneous increase in the proportion of "maturing" and "imma- three groups: (I) found in stretches "B" and "D" and characterized by ture" individuals, reaching 100% of "immature" individuals in Septem- the presence of a greater number of species and abundance ber and October. Specimens identified as L. breviceps and M. littoralis uniformity; (II) found in stretch "C", with an intermediate pattern were classified predominantly as "maturing" and "immature", and the between groups I and III, and greater similarity to group I; (III) found highest relative frequency of "maturing" individuals was observed in in stretch "A" and represented by two species (A. luniscutis and the rainy season. For P. corvinaeformis, the relative frequency of "im- Hemiramphus brasiliensis Linnaeus, 1758); the former being the mature" individuals remained high throughout the studied period most abundant (Figure 5). (Figure 7). A B D C Mature Maturation Immature Mature Maturation Immature 0,96 100 100 90 90 0,84 80 80 70 70 60 60 0,72 equency (%) equency (%) 50 50 r r 40 40 e F e F 30 30 v 0,60 v 20 20 10 10 elati Group I elati R 0,48 R 0 A 0 B J F M A M J J A S O N D J F M A M J J A S O N D Similarity 0,36 Months Months Mature Maturation Immature Mature Maturation Immature 0,24 Group II 100 100 90 90 80 80 0,12 70 70 60 60 equency (%) 50 equency (%) 50 r 0 r Group III 40 40 e F 30 e F 30 v Figure 5. Dendogram of faunal similarity among four stretches of monitored area with presence 20 v 20 and absence of species using the Jaccard coeficient. 10 10 elati elati R 0 C R 0 D Reproductive phase J F M A M J J A S O N D J F M A M J J A S O N D The classification of sexual maturity was based on the macro and Months Months Figure 7. Temporal variation in the stages of gonadal maturation, from January to December microstructural aspects of the gonads. We observed that 76.3% of the 2012: (A) Pellona harroweri; (B) Larimus breviceps; (C) Menticirrhus littoralis, (D) Pomadasys sampled specimens were classified as "immature". On the other hand, corvinaeformis. "maturing" and “mature” stages represented 16.7% and 7%, respectively. Species Pellona harroweri, Larimus breviceps, Menticirrhus The average size at first maturity for each studied species was littoralis (Holbrook, 1847) and Pomadasys corvinaeformis were the based on literature data (Table 2). most captured. Considering these four species, we also observed a Table 2. Average size of irst maturation for Pellona harroweri, Larimus breviceps, Menticirrhus higher percentage of "immature" individuals (76.3%), followed by littoralis and Pomadasys corvinaeformis captured as bycatch at Potiguar Basin beaches, northeastern, "maturing" and "mature" (18.9% and 4.8%, respectively). These Brazil. results indicate that trawling captures predominantly "immature" Species L (50) (cm) according with references individuals. Pellona harroweri 7 (SILVA-JU NIOR et al., 2013) We observed an increase in the GSI values from "immature" to "mature" stage, and a significant difference between "mature" stage Larimus breviceps 14 (SILVA-JU NIOR et al., 2013) and "maturing" and "immature" stages. Levene's test indicated non- Menticirrhus littoralis 23 (BRAUN; FONTOURA, 2004) homogeneity among the groups (P. harroweri, p = 0.002391; L. Pomadasys corvinaeformis 15,8 (SILVA-JU NIOR et al., 2013) breviceps, p = 0.719; M. littoralis, p = 1.029 × 10-5; and P. corvinaeformis, p = 1.782 × 10-6); however, the Welch F test demonstrated differences In the discharges analyzed in this study, a higher proportion of M. for P. harroweri (p = 0.02019), L. breviceps (p = 0.002744), and P. littoralis, P. corvinaeformis and L. breviceps specimens, were captured corvinaeformis (p = 0.0191). The Tukey test detected differences before reach the average size and gonadal stage associated to the first between immature and mature stages for P. harroweri: (p = 0.003922), maturity, presenting negative relation with fishing activity. On the L. breviceps (p = 0.007636), and P. corvinaeformis (p = 2.175 × 10-5). other hand, the evaluation of size and gonadal tissue revealed that the These same species also presented differences between maturing and most specimens of Pellona harroweri had already spawned at least mature stages (p = 0.0186, p = 0.01, and p = 2.175 × 10-5, respectively). once, and were positively related with fishing activity (Figure 8).

Biota Amazônia ISSN 2179-5746 30 200 sented higher levels of species occurrence, which indicates major 27 180 inputs of fish in coastal areas. During the rainy season, nutrient con- 24 160 41 B n centrations increase and there is a reduction of salinity, favoring pri- T o h 21 140 O r e M

mary productivity and higher trophic levels (THURMAN; TRUJILLO, t i 18 120 h F m e I M a 15 100 2008; FREDOU et al., 2009). p s a , equency equency t A c r r 12 80 Fish assemblage differed among monitoring stretches (A, B, C, and e t . F F r C o 9 60 n .

D), with the highest value of abundance, biomass and indexes of rich- f e B s

6 40 t r h

ness and diversity in stretches "B", "C", and "D". Stretch "A" showed a a r l z 3 20 i . m higher values for dominance and evenness. The most abundant spe- i 0 0 l cies for stretches "B", "C", and "D" were L. breviceps, P. harroweri, O. p 0 3 6 9 12 15 18 21 24 27 30 0 2 4 6 8 10 12 14 16 18 20 t Length (cm) Length (cm) r oglinum, P. corvinaeformis, M. littoralis, and C. nobilis. According to a 40 30 w Bomfim (2014), the analysis of gut content demonstrated that all these l 36 b y

32 25 species are carnivorous, and feed especially on shrimp; except the last c a t

28 one, which presented a fish preference. These results indicate an c

20 h

24 abundance of such food items in the monitored stretches. o 20 15 n Unequal access to resources, such as food or space, or different f i s equency equency r

16 r levels of predation may lead to differences in fish species composition h F F 10 12 r (HYNDES et al., 2003). Therefore, food availability promotes the distri- e 8 p 5 r bution of the observed species in the three stretches (B, C, and D), o

4 d

which comprise a region where trawling is more common, and the u

0 0 c t

0 2 4 6 8 10 12 14 16 18 20 0 2 4 6 8 10 12 14 16 18 20 geographical areas have the highest percentages of shrimp production i o

Length (cm) n Length (cm) by trawl nets. Total production accounts for 36.8%, 30.8%, and 28.8% Figure 8. Proportion of specimens per class of total length (cm): (A) Menticirrhus littoralis; (B) i n Pomadasys corvinaeformis; (C) Larimus brevicps; (D) Pellona harroweri. respectively, according to the Operating Unit of Exploration and Pro- duction of Rio Grande do Norte and Ceará - UO-RNCE (2012). Discussion In stretch "A", trawl net shrimp fishing is not as frequent as in other Ichthyofauna composition segments, and represented only 3.5% of shrimp production according The diversity of fish species bycaught in the Potiguar Basin was to the Operating Unit of Exploration and Production of Rio Grande do higher than that found by Silva e Fonteles-Filho (2009) (18 species) for Norte and Ceará - UO - RNCE (2012). Lobster and shellfish fishing is the same fishing category and region. Our data indicated that the sam- predominant in this monitored stretch. ple size was adequate to represent the species occurring in the discard- The fishing panorama of stretch "A" seems to indicate a lower ing of fish from trawl nets on the northwest coast of RN. Ninety-six availability of shrimp in the region, leading to lower fish diversity, species of fish were reported in this region (GARCIA, 2006). The num- richness, abundance, and biomass. Thus, the fishing panorama could ber of species described in this study differed from an ichthyofaunistic be an indicator of the availability of the main food source of fish acci- survey conducted by Garcia (2006), possibly because various means of dentally caught by nets, which is reflects on community attributes and, fishing devices (gill nets, seines, handlines, dip nets, cast nets, and consequently, in the distribution of fish species in the Potiguar Basin. trammel) and different sampled environments (estuaries and sandy beaches) were analyzed. Reproductive phase In regards to species composition, order Peciformes was the most The factors that define the exploitation of a species relate directly commonly observed. Such finding may be due to the fact that this order to abundance and catchability, but also to life cycle characteristics. represents half of the demersal teleostei occurring in Brazil, that along Researchers still question whether it is more harmful removing young with Pleuronectiformes, Anguilliformes and Tetraodontiformes repre- specimens or adults in reproductive age from a population (SOUZA; sent over 70% of the brazilian species (HAIMOVICI; KLIPPEL, 1999). CHAVES, 2007; DANTAS et al., 2012; FORREST et al., 2013). Regardless The most abundant families in terms of number of individuals of the analyzed period and season, shrimp trawling will always affect were Haemulidae, Scianidae, Clupeidae and Ariidae. On the other some percentage of the reproductive individuals of a fish population. hand, the most abundant families in number of species were Studies that analyzed the accompanying ichthyofauna of shrimp Carangidae, Scianidae, Haemulidae, and Gerreidae. fishing in the north coast of Santa Catarina state indicated that both Studies of the bio-ecological analysis of fish production in the situations occur with the same intensity (SOUZA; CHAVES, 2007). Our northern coast of RN, recorded the families Haemulidae, Carangidae, results showed that, throughout the study period, shrimping drag Lutjanidae, Scianidae, Scombridae and Serranidae as the most abun- focused predominantly on immature individuals. dant in number of species (31), of which 18 were considered dis- Species with late-maturation are highly vulnerable to extinction carded fish (bycatch) (SILVA; FONTELES-FILHO, 2009). Families (JENNINGS et al., 2001; HUTCHINGS; REYNOLDS, 2004). Many speci- registered in our study are in accordance with other studies carried mens of Menticirrhus littoralis, Pomadasys corvinaeformes and Larimus out in different subtropical and tropical regions. Dantas et al., (2012) breviceps were still juveniles when captured, before reaching the also found a similar pattern of composition and structure of demersal appropriate size and gonadal development associated with reproduc- fish at the São Cristóvão Beach, Areia Branca, RN: families Scianidae, tive maturity, thus these species may possibly be considered negatively Ariidae, Carangidae, Engraulidae, Haemulidae and Pristigasteridae related with fishing activity. According to Silva-Junior et al., (2013), were the most representative in number of species and individuals. captured individuals that spawned at least once may be positively It is difficult to compare species diversity and relative abundance correlated with fishing activity, which was also observed in our results in different areas due to habitat heterogeneity, changes in environmen- (e.g. Pellona harroweri), since a great proportion of the captured indi- tal variables, and fishing effort; however, it is evident that this coastal viduals were larger than they would be at first maturity. Studies at the area is important in these species' life cycle. On the other hand, Guedes São Cristóvão Beach, Areia Branca, RN reported similar results for P. et al., (2005) reported a uniform ichthyofauna along the Brazilian coast harroweri and P. corvinaeformis (SILVA-JUNIOR et al., 2013). in regards of families. Our results demonstrated that the number of Overfishing is defined by a greater number of captured organisms species per family differed among previous studies due to variations in comparison to the number of produced organisms (CORDUE, among different samples and years. However, the most common 2012). It is difficult fishery to reach equilibrium when the fishing effort families are often the same, especially in regards of family Scianidae. is reduced during a short period after overexploitation (KING, 2007). A The vast majority of species captured in this study presented low population may decline if the natural mortality rate, combined with constancy, which has been observed in previous studies in the the mortality caused by fishing, reduces inventory levels. This phe- Potiguar Basin, as well as in other regions with similar characteristics. nomenon could continue even after cessation of fishing (WOOTTON, On the other hand, we verified a high constancy of occurrence and 1989). abundance for Larimus breviceps, Pomadasys corvinaeformis, Commercial drag is typically performed in deep waters and far- Opisthonema oglinum, Pellona harroweri, Conodon nobilis, Menticirrhus ther offshore. However, in the Potiguar Basin, drag is performed in littoralis, Menticirrhus americanus, Lycengraulis grossidens and Selene shallow waters and very close to the coast. Furthermore, the incidental brownii, suggesting that their life cycles are connected to sandy beach capture of non-target species in this are in not sustainable because ecosystems. The same pattern was previously described for P. many organisms are caught before reaching their first maturity size. corvinaeformis, Cathorops spixii, Stellifer rastrifer, P. harroweri, Stellifer Among the species that had their reproductive stage studied, P. stellifer, Chirocentrodon bleekerianus, L. breviceps, M. americanus and C. corvinaeformes, M. littoralis and L. breviceps were found to be nega- nobilis at the São Cristóvão Beach, Areia Branca, RN (DANTAS et al., tively related to fishing activity, being therefore, even more vulnerable 2012). In regards to seasonality, the rainy season (January-July) pre- to shrimping trawl nets.

Biota Amazônia ISSN 2179-5746 The removal of species from an ecosystem may lead to diversity loss and local extinction. According to Silva-Junior et al., (2013), non- 42 B n T o

target species that are accidentally caught during fishing can be classi- h O r e M t i

fied as vulnerable. Therefore, shrimp fishing in the studied area threat- h F m e I M a ens the ichthyofauna, especially estuarine species from families p s a , t A c Carangidae and Scianidae. e t . r C o n . Finally, the exploitation of this target resource (shrimp) has f e B s t r h a caused environmental and economical impact in the northwest coast a r l z i . m i of Rio Grande do Norte. l p t r a

Conclusion w l

Our results indicate that the incidental capture of some non-target b y c

species can affects predominantly individuals considered immature, a t c

i.e. without reproductive potencial, an indicative of non-sustainable h o

fishing in region. So, we highlight the need for collective efforts, includ- n f ing co-management among government, production sector and i s h

research institutes to find ways to solve this problem. r e p r o

Acknowledgments d u

We would like to thank the Petrobras; staff of the Programa de c t i o

Monitoramento de Praias da Bacia Potiguar (PMP-BP); Projeto Cetáce- n i os da Costa Branca, Universidade do Estado do Rio Grande do Norte n (UERN); Programa de Pós-Graduação em Ciências Biológicas, Univer- sidade Federal do Rio Grande do Norte (UFRN); Professor PhD Sergio Maia Queiroz Lima from Departamento de Botânica, Ecologia e Zoolo- gia , Universidade Federal do Rio Grande do Norte for species identification; Professor PhD José Henrique Hildebrand Grisi-Filho from Laboratório de Epidemiologia e Estatıś tica (LEB), Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medici- na Veterinária e Zootecnia, Universidade de São Paulo for the assistan- ce with statistical analyses; and Coordenação de Aperfeiçoamento de Pessoal de Nıv́ el Superior (CAPES) (grant number, 1107351) by support.

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