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Squids caught by shrimp trawlers off the coast of Sergipe, northeastern Brazil

ABSTRACT

The objective of this study was to identify the squids caught by shrimp trawlers in Sergipe and to describe their populational structure. Four samples were obtained monthly from commercial trawlers based in Pirambu-Sergipe (May/2015-May/2016). Each squid found was separated, identified, weighed individually (wet weight - WW in g) and had its mantle length (ML; cm) and total length (TL, including tentacles; cm) measured. One specimen of Doryteuthis pleii was captured (23.3 cm ML mature male), as well as 152 specimens of Lolliguncula brevis (1.5˗6.7 cm ML). The linear relation between TL and ML of L. brevis was TL=5.1173+2.6190ML (positive allometry) and the power relation between WW and ML was WW=0.1453ML2.5353 (negative allometry). For L. brevis, there were two cohorts in the area during the period analyzed. Studies on the biology of cephalopods are scarce in northeastern Brazil, especially considering that these species are present in the bycatch of shrimp fishing and that the global conservation status of L. brevis is data deficient (DD) according to the International Union for Conservation of Nature (IUCN).

Keywords:
Bycatch; Cephalopoda; Doryteuthis pleii; Lolliguncula brevis

Shrimps are one of the main fishery resources caught in waters off the state of Sergipe and accounted for about 32.3% of the total catch in 2013 (Thomé-Souza et al., 2014Thomé-Souza, M. J. F., Carvalho, B. L. F., Garciov Filho, E. B., Silva, C. O., Deda, M. S., Félix, D. C. F. & Santos, J. C. 2014. Estatística pesqueira da costa do estado de Sergipe e extremo norte da Bahia 2013. São Cristóvão, Editora da UFS .). One of the main problems associated with shrimp trawlers is the impact of repetitive bottom trawling (Meenakumari et al., 2008Meenakumari, B., Bhagirathan, U. & Pravin, P. 2008. Impact of bottom trawling on benthic communities: A review. Fishery Technology, 45(1), 1-22.) and the capture of a high number of juveniles of fish species of commercial interest, but also gastropods, sea stars, crabs, and cephalopods (Alverson et al., 1994Alverson, D. L., Freeberg, M. H., Murawski, S. A. & Pope, J. G. 1994. A global assessment of fisheries bycatch and discards. Rome, FAO Fisheries Technical Paper, No. 339; Keunecke et al., 2007Keunecke, K. A., Vianna, M., Fonseca, D. B. & D’incao, F. 2007. The pink-shrimp trawling bycatch in the northern coast of São Paulo, Brazil, with emphasis on crustaceans. Nauplius, 15, 49-55.; Silva Júnior et al., 2019Silva Júnior, C. A. B., Lira, A. S., Eduardo, L. N., Viana, A. P., Lucena-Frédou, F. & Frédou, T. 2019. Ichthyofauna bycatch of the artisanal fishery of penaeid shrimps in Pernambuco, northeastern Brazil. Boletim do Instituto de Pesca , 45(1), e435. DOI: https://doi.org/10.20950/1678-2305.2019.45.1.435
https://doi.org/10.20950/1678-2305.2019....
).

Cephalopods are not economically exploited in the waters off Sergipe (Thomé-Souza et al., 2014Thomé-Souza, M. J. F., Carvalho, B. L. F., Garciov Filho, E. B., Silva, C. O., Deda, M. S., Félix, D. C. F. & Santos, J. C. 2014. Estatística pesqueira da costa do estado de Sergipe e extremo norte da Bahia 2013. São Cristóvão, Editora da UFS .). However, there are a few localities in northeastern Brazil where cephalopods, especially octopuses, are targeted by commercial fisheries (Haimovici et al., 2014Haimovici, M., Leite, T. S., Marinho, R. A., Batista, B. B., Madrid, R. M., Lins-Oliveira, J. E., Lima, F. D. & Candice, L. 2014. As pescarias de polvos do nordeste do Brasil. In: Haimovici, M., Andriguetto-Filho, J. M. & Sunyé, P. S. (eds.) A pesca marinha e estuarina no Brasil: estudos de caso multidisciplinares. Rio Grande: Editora da FURG.; Lima et al., 2021Lima, F. D., Andrade, L. C. A. & Medeiros, S. L. S. 2021. Cefalópodes No Nordeste Brasileiro. In: Viana, D. L., Lins-Oliveira, J. E., Hazin, F. H. V. & Souza, M. A. C. (eds.) Ciências do Mar: dos oceanos do mundo ao Nordeste do Brasil: Bioecologia, Pesca e Aquicultura. Recife, Via Design Publicações.). In the southeastern and southern regions of Brazil, cephalopods have a considerable fishing production when compared to the northeastern region. Previous efforts, such as the REVIZEE program (Programa de Avaliação do Potencial Sustentável de Recursos Vivos na Zona Econômica Exclusiva do Brasil - Program for the Assessment of the Sustainable Potential of Living Resources in the Brazilian Exclusive Economic Zone), have sought to understand the population dynamics and fishery production of squid species exploited in the region: Doryteuthis pleii (Blainville, 1823) and Doryteuthis sanpaulensis (Brakoniecki, 1984) (Gasalla et al., 2005Gasalla, M. A., Perez, J. A. A., Marques, C. A, Tomás, A. R. G., Aguiar, D. C. & Oliveira, U. C. 2005. Loligo sanpaulensis (Brakoniecki, 1984) . In: Cergole, M. C., Ávila-Da-Silva, A. O. & Rossi-Wongtschowski, C. (eds.) Análise das principais pescarias comerciais do sudeste-sul do Brasil: Dinâmica populacional das espécies em explotação (Série documentos REVIZEE: Score Sul). São Paulo: Instituto Oceanográfico da USP.; Perez et al., 2005Perez, J. A. A., Gasalla, M. A., Aguiar, D. C., Oliveira, U. C., Marques, C. A. & Tomás, A. R. G. 2005. Loligo plei (Blainville, 1823). In: Cergole, M. C., Ávila-Da-Silva, A. O. & Rossi-Wongtschowski, C. (eds.) Análise das principais pescarias comerciais do sudeste-sul do Brasil: Dinâmica populacional das espécies em explotação (Série documentos REVIZEE: Score Sul). São Paulo: Instituto Oceanográfico da USP .).

The occurrence of squids had been already reported in Sergipe by Lima and Couto (2001Lima, G. C. & Couto, E. C. G. 2001. Malacofauna da costa sergipana: classe Polyplacophora Blainwille, 1816; classe Scaphoda Bronn, 1862 e classe Cephalopoda Cuvier, 1798. Revista Nordestina de Biologia, 15(2), 91-98.) and Carneiro and Arguelho (2018Carneiro, M. E. R. & Arguelho, M. L. P. M. 2018. Plataforma continental de Alagoas e Sergipe: geoquímica sedimentar e comunidade bêntica. São Cristóvão, Editora da UFS.), specifically: Lolliguncula brevis (Blainville, 1823), Doryteuthis pleii and Doryteuthis spp. Naef, 1912. Nevertheless, no information other than the occurrence was found. Thus, this study aimed at determining if any other squid species were caught by shrimp trawlers in Sergipe and to describe their population structure.

Four complete samples (target shrimps and bycatch), weighing about six kilograms each, were obtained monthly from four commercial shrimp trawlers based in Pirambu, on the northern coast of Sergipe, northeastern Brazil (11°S; 36°W). The samples were collected from May 2015 to May 2016 and preserved on ice onboard and when landed in the port. No samples were collected during the closed season for the shrimp fishery: from April 1st to May 15th and from December 1st to January 15th (MMA, 2004MMA (Ministério do Meio Ambiente). 2004. Instrução Normativa MMA N. 14, 14 de outubro de 2004. Brasília, DF, Ministério do Meio Ambiente. Available from: Available from: https://www.icmbio.gov.br/cepsul/images/stories/legislacao/Instrucao_normativa/2004/in_mma_14_2004_regulamentapescacamaroesregiao_ne.pdf . Accessed: 1 May 2023.
https://www.icmbio.gov.br/cepsul/images/...
). The samples were then transported to the Laboratório de Ecologia Pesqueira at the Universidade Federal de Sergipe, where they were kept frozen until processing. Each squid found was separated, identified using Jereb and Roper (2010Jereb, P. & Roper, C. F. E. 2010. Cephalopods of the world: An annotated and illustrated catalogue of cephalopod species known to date (vol. 2. Myopsid and Oegopsid Squids). Rome, FAO, Fisheries and Aquaculture Resources Use and Conservation Division.), weighed individually with an electronic scale (wet weight - WW in g; precision: 0.1 g) and had its mantle length (ML; cm) and total length (TL, including tentacles; cm) measured using an ichthyometer (precision: 0.1 cm).

A frequency distribution for the mantle length and the wet weight was calculated for the main species caught. Additionally, the relation between total and mantle length was estimated using a linear model (TL = a + bML) (Zar, 2010Zar, J. H. 2010. Biostatistical analysis (5th ed.). New Jersey, Pearson Prentice Hall.). A logarithmic form of the power model (WW = aMLb) was fitted to the relation between wet weight and mantle length. Confidence intervals were estimated for both parameters in both models and the isometry was tested (b = 1 for the length-length relation and b = 3 for the weight-length relation) using confidence intervals (Zar, 2010Zar, J. H. 2010. Biostatistical analysis (5th ed.). New Jersey, Pearson Prentice Hall.). The significance of each parameter was tested using a significance level of 5%. All analyses were performed in R software version 4.2.1 (R Core Team, 2023R Core Team. 2023. R: A language and environment for statistical computing. Vienna - Austria, R Foundation for Statistical Computing. Available from: Available from: https://www.r-project.org/ Accessed: December 2023.
https://www.r-project.org/...
).

Two squid species were found in the bycatch of shrimp trawlers off Sergipe in 2015-2016: Doryteuthis pleii and Lolliguncula brevis. Only one specimen of D. pleii was captured: a male with 23.3 cm ML (137.7 g WW), caught in November 2015. Its size corresponded to 67% of the maximum size registered for this species (Vaske Júnior and Costa, 2011Vaske Júnior, T. & Costa, F. A. P. 2011. Lulas e polvos da costa brasileira (Coleção Habitat 5). Fortaleza, UFC/LABOMAR/NAVE.) and was larger than the size at first maturity (Lm) for males, which corresponds to 8.7 cm ML in southeastern-southern Brazil (Martins and Juanicó, 2018Martins, R. S. & Juanicó, M. 2018. Biology, distribution and geographic variation of loliginid squids (Mollusca: Cephalopoda) off southwestern Atlantic. Zoologia, 35, e23176. DOI: https://doi.org/10.3897/zoologia.35.e23176
https://doi.org/10.3897/zoologia.35.e231...
) and to 14.7 cm ML in southern Brazil (Martins and Perez, 2007Martins, R. S. & Perez, J. A. A. 2007. The ecology of loliginid squid in shallow waters around Santa Catarina Island, southern Brazil. Bulletin of Marine Science, 80(1), 125-145.).

Conversely, 152 specimens of Lolliguncula brevis were caught during the same period, with 1.5-6.7 cm ML (3.65 ± 1.12 cm; mean ± standard deviation) and 0.2-18.8 g WW (4.88 ± 4.28 g). Most specimens were smaller than the Lm of 5 cm ML for females and males, as estimated for São Paulo (southeastern Brazil, Vaske-Júnior et al., 2014Vaske Júnior, T., Knoeller, J. M. S. & Viliod, M. C. L. 2014. Ocorrência e aspectos da biologia da lula Atlântica Lolliguncula brevis no estuário de São Vicente-SP, Sudeste do Brasil. Unisanta BioScience, 3(2), 66-77.) (Figure 1A). This species is not commercially exploited in Sergipe due to its small size. The distribution of WW was asymmetrical, with 63.2% of the specimens falling into the first two classes (< 4 g) (Figure 1B). This species reproduces at approximately the same size, regardless of where it occurs. Thus, its reproduction is more related to size than age. The difference among areas is related to the rate at which individuals reach this specific size, which is faster in warmer waters (Jackson et al., 1997Jackson, G. D., Forsythe, J. W., Hixon, R. F. & Hanlon, R. T. 1997. Age, growth, and maturation of Lolliguncula brevis (Cephalopoda: Loliginidae) in the northwestern Gulf of Mexico with a comparison of length-frequency versus statolith age analysis. Canadian Journal of Fisheries and Aquatic Sciences, 54, 2907-2919. DOI: https://doi.org/10.1139/f97-192
https://doi.org/10.1139/f97-192...
).

Figure 1
Histogram for the mantle length (A) and wet weight (B) of Lolliguncula brevis caught by shrimp trawlers along the coast of Sergipe in northeastern Brazil (2015-2016). The red line corresponds to the length at first maturity for females and males for the state of São Paulo (Vaske Júnior et al., 2014Vaske Júnior, T., Knoeller, J. M. S. & Viliod, M. C. L. 2014. Ocorrência e aspectos da biologia da lula Atlântica Lolliguncula brevis no estuário de São Vicente-SP, Sudeste do Brasil. Unisanta BioScience, 3(2), 66-77.). (C) Boxplot indicating median, 1st and 3rd quartiles of the mantle length per month for L. brevis caught by shrimp trawlers along the coast of Sergipe (2015-2016). Black circles indicate outliers.

The linear relation fitted between the total length (including tentacles) and mantle length of L. brevis was statistically significant and indicated a positive allometry (slope >1; Table 1). The relation between the wet weight and mantle length indicated a negative allometry of the growth in weight (b < 3; Table 1), as was also found in São Paulo (southeastern Brazil, Vaske Júnior et al., 2014Vaske Júnior, T., Knoeller, J. M. S. & Viliod, M. C. L. 2014. Ocorrência e aspectos da biologia da lula Atlântica Lolliguncula brevis no estuário de São Vicente-SP, Sudeste do Brasil. Unisanta BioScience, 3(2), 66-77.) and Santa Catarina (southern Brazil, Martins and Perez, 2007Martins, R. S. & Perez, J. A. A. 2007. The ecology of loliginid squid in shallow waters around Santa Catarina Island, southern Brazil. Bulletin of Marine Science, 80(1), 125-145.).

Table 1
Parameters estimated for the linear relation between the total length (cm) and mantle length (cm), and between the wet weight (g) and mantle length (cm) for Lolliguncula brevis caught by shrimp trawlers along the coast of Sergipe (2015-2016). TL = total length (including tentacles; cm); ML = mantle length (cm); WW = wet weight (g); SE = standard error; r2 = coefficient of determination; n = sample size (which differs between relations, as total length could not be measured in all specimens); Lower and Upper represent the limits of the confidence interval for each parameter.

There is discussion among scientists about differences between the populations of L. brevis inhabiting the northernmost areas of its distribution (e.g., the population in the Caribbean and the USA) and the southernmost areas (e.g., the population in Brazil) (Simone, 1997Simone, L. R. L. 1997. Redescription of Lolliguncula brevis (Blainville) (Myopsida, Loliginidae) from southeastern Brazil. Iheringia, 82, 141-150.; Vaske Júnior et al., 2014Vaske Júnior, T., Knoeller, J. M. S. & Viliod, M. C. L. 2014. Ocorrência e aspectos da biologia da lula Atlântica Lolliguncula brevis no estuário de São Vicente-SP, Sudeste do Brasil. Unisanta BioScience, 3(2), 66-77.). In fact, the northernmost specimens reach larger sizes (maximum of 8.3 to 12.0 cm ML, Haefner-Júnior, 1964Haefner-Júnior, P. A. 1964. Morphometry of the common Atlantic squid, Loligo pealei, and the brief squid, Lolliguncula brevis in Delaware Bay. Chesapeake Science, 5(3), 138-144.; Jackson et al., 1997Jackson, G. D., Forsythe, J. W., Hixon, R. F. & Hanlon, R. T. 1997. Age, growth, and maturation of Lolliguncula brevis (Cephalopoda: Loliginidae) in the northwestern Gulf of Mexico with a comparison of length-frequency versus statolith age analysis. Canadian Journal of Fisheries and Aquatic Sciences, 54, 2907-2919. DOI: https://doi.org/10.1139/f97-192
https://doi.org/10.1139/f97-192...
; Bartol et al., 2002Bartol, I. K., Mann, R. & Vecchione, M. 2002. Distribution of the euryhaline squid Lolliguncula brevis in Chesapeake Bay: effects of selected abiotic factors. Marine Ecology Progress Series, 226, 235-247. DOI: https://doi.org/10.3354/meps226235
https://doi.org/10.3354/meps226235...
) when compared to the specimens in Brazil (maximum of 5.0 to 7.6 cm ML, Berry, 1911Berry, S. S. 1911. A note on the genus Lolliguncula. Proceedings of the Academy of Natural Sciences of Philadelphia, 63(1), 100-105.; Simone, 1997Simone, L. R. L. 1997. Redescription of Lolliguncula brevis (Blainville) (Myopsida, Loliginidae) from southeastern Brazil. Iheringia, 82, 141-150.; Martins and Perez, 2007Martins, R. S. & Perez, J. A. A. 2007. The ecology of loliginid squid in shallow waters around Santa Catarina Island, southern Brazil. Bulletin of Marine Science, 80(1), 125-145.; Coelho et al., 2010Coelho, L. I., Muto, E. Y., Marian, J. E. A. R. & Soares, L. S. H. 2010. Contribuição ao conhecimento da dieta, atividade alimentar e reprodução de Lolliguncula brevis (Blainville, 1823) na região costeira de Santos (estado de São Paulo). Boletim do Instituto de Pesca, 36, 225-236.; Zaleski et al., 2012Zaleski, T., Perez, J. A. A., Gandara-Martins, A. L. 2012. Morphological and morphometric variability of the squid Lolliguncula brevis (Mollusca: Cephalopoda) in Brazilian waters: evidence for two species in the Western Atlantic? Anais da Academia Brasileira de Ciências, 84(4), 1015-1028.; Vaske Júnior et al., 2014Vaske Júnior, T., Knoeller, J. M. S. & Viliod, M. C. L. 2014. Ocorrência e aspectos da biologia da lula Atlântica Lolliguncula brevis no estuário de São Vicente-SP, Sudeste do Brasil. Unisanta BioScience, 3(2), 66-77.). Other morphological characteristics also strengthen this hypothesis, such as the shape of the mantle and fins, and a few modified suckers, suggesting that these two populations could actually be two species (Simone, 1997Simone, L. R. L. 1997. Redescription of Lolliguncula brevis (Blainville) (Myopsida, Loliginidae) from southeastern Brazil. Iheringia, 82, 141-150.; Zaleski et al., 2012Zaleski, T., Perez, J. A. A., Gandara-Martins, A. L. 2012. Morphological and morphometric variability of the squid Lolliguncula brevis (Mollusca: Cephalopoda) in Brazilian waters: evidence for two species in the Western Atlantic? Anais da Academia Brasileira de Ciências, 84(4), 1015-1028.).

The ML of L. brevis off Sergipe remained approximately stable from January to May and increased from September to November (Figure 1C). Both periods correspond to the dry season in Sergipe (Carneiro and Arguelho, 2018Carneiro, M. E. R. & Arguelho, M. L. P. M. 2018. Plataforma continental de Alagoas e Sergipe: geoquímica sedimentar e comunidade bêntica. São Cristóvão, Editora da UFS.). According to Jackson et al. (1997Jackson, G. D., Forsythe, J. W., Hixon, R. F. & Hanlon, R. T. 1997. Age, growth, and maturation of Lolliguncula brevis (Cephalopoda: Loliginidae) in the northwestern Gulf of Mexico with a comparison of length-frequency versus statolith age analysis. Canadian Journal of Fisheries and Aquatic Sciences, 54, 2907-2919. DOI: https://doi.org/10.1139/f97-192
https://doi.org/10.1139/f97-192...
), the life span of L. brevis is less than 200 days, which corresponds to approximately six months. Thus, Figure 1C may be showing the presence of two different cohorts in the waters of Sergipe, as also observed in Chesapeake Bay (USA) (Bartol et al., 2002Bartol, I. K., Mann, R. & Vecchione, M. 2002. Distribution of the euryhaline squid Lolliguncula brevis in Chesapeake Bay: effects of selected abiotic factors. Marine Ecology Progress Series, 226, 235-247. DOI: https://doi.org/10.3354/meps226235
https://doi.org/10.3354/meps226235...
). The highest number of L. brevis specimens was found in August 2015 (38 specimens), at the end of the rainy season, and in January 2016 (37 specimens), during the dry season in Sergipe. In all other months, the number was lower than 50% of that observed in January and August. Here again, there is an indication of the presence of two squid cohorts in the area.

The distribution of loliginid paralarvae was assessed at latitudes 22°-25°S in the Western Atlantic, where upwelling events and oceanographic conditions linked to water temperature and salinity control the distribution and abundance of squid species over time (Araujo and Gasalla, 2018). According to these authors, L. brevis paralarvae were more abundant in shallow, coastal and low salinity waters close to estuaries. This information may partly explain the large quantity of this species in bycatch samples in Sergipe, as shrimp trawling is concentrated on the muddy bottom, in 10-30 m deep waters (Pennino et al., 2016Pennino, M. G., Thomé-Souza, M. J. F., Carvalho, A. R., Fontes, L. C. S., Parente, C. & Lopes, P. F. M. 2016. A spatial multivariate approach to understand what controls species catch composition in small-scale fisheries. Fisheries Research, 175, 132-141. DOI: http://dx.doi.org/10.1016/j.fishres.2015.11.028
http://dx.doi.org/10.1016/j.fishres.2015...
).

Cephalopods are known for their physiological limitations preventing them from occupying shallow, highly variable, and euryhaline habitats. However, L. brevis is one exception, inhabiting areas with salinity ranging from 17.9 to 35.0 (Bartol et al., 2002Bartol, I. K., Mann, R. & Vecchione, M. 2002. Distribution of the euryhaline squid Lolliguncula brevis in Chesapeake Bay: effects of selected abiotic factors. Marine Ecology Progress Series, 226, 235-247. DOI: https://doi.org/10.3354/meps226235
https://doi.org/10.3354/meps226235...
), but also being able to live in waters with salinity down to 8 (Vaske Júnior and Costa, 2011Vaske Júnior, T. & Costa, F. A. P. 2011. Lulas e polvos da costa brasileira (Coleção Habitat 5). Fortaleza, UFC/LABOMAR/NAVE.). According to Coelho et al. (2010Coelho, L. I., Muto, E. Y., Marian, J. E. A. R. & Soares, L. S. H. 2010. Contribuição ao conhecimento da dieta, atividade alimentar e reprodução de Lolliguncula brevis (Blainville, 1823) na região costeira de Santos (estado de São Paulo). Boletim do Instituto de Pesca, 36, 225-236.), this species prefers to use the inner shelf and feed on crustaceans. However, the samples collected in Sergipe could not be georeferenced, sex was not identified, and their gut content was not analyzed, three issues that should be addressed in future studies with L. brevis, which are still scarce in northeastern Brazil. Finally, it would be important to assess the role of L. brevis in the region using ecosystem models. According to the International Union for Conservation of Nature (IUCN), the global status of this species is data deficient - DD (Allcock and Taite, 2019Allcock, A. L. & Taite, M. 2019. Lolliguncula brevis. The IUCN Red List of Threatened Species 2019: e.T163081A970763. DOI: https://doi.org/10.2305/IUCN.UK.2019-2.RLTS.T163081A970763.en
https://doi.org/10.2305/IUCN.UK.2019-2.R...
), which demonstrates the importance of making more data available on this species in different regions.

ACKNOWLEDGMENTS

We would like to thank Thaiza Barreto, Aline Dias, Ana Cláudia Gaspar, and Sandra Lima for helping with the sample processing; and Mrs. Maria Moraes for organizing the sample collection with the fishers and for receiving and storing all samples until they were taken to the Laboratório de Ecologia Pesqueira at the Universidade Federal de Sergipe. This study was supported by the Projeto de Monitoramento Participativo do Desembarque Pesqueiro (PMPDP) and the Fundação de Apoio à Pesquisa e Extensão de Sergipe (FAPESE) (grant numbers 2600.0094374.14.4 and 2600.0099827.15.4). We are grateful to the two reviewers who contributed to the revised version of this paper.

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Edited by

Editor:

Rubens Lopes

Publication Dates

  • Publication in this collection
    17 May 2024
  • Date of issue
    2024

History

  • Received
    28 June 2023
  • Accepted
    10 Jan 2024
Instituto Oceanográfico da Universidade de São Paulo Praça do Oceanográfico 191, CEP: 05508-120, São Paulo, SP - Brasil, Tel.: (11) 3091-6501 - São Paulo - SP - Brazil
E-mail: diretoria.io@usp.br