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Ovarian development of Xiphopenaeus kroyeri (Crustacea: Penaeidae) from Espírito Santo, southeastern Brazil

Desenvolvimento ovariano de Xiphopenaeus kroyeri (Crustacea: Penaeidae) no Espírito Santo, sudeste do Brasil

Abstract

This study aimed to describe and characterize the stages of gonadal development of females of Xiphopenaeus kroyeri caught by artisanal fishers in Espírito Santo state, southeastern region of Brazil. All females (n= 1,831) were subjected to macroscopic and microscopic morphological analysis (n= 333) of the ovaries. From the morphology, coloration and degree of turgidity of the fresh ovary, macroscopic analysis determined five stages of gonadal development. The macroscopic analysis showed difficulties in differentiating the immature and spawning stages due to the similarity between the colors of the ovaries, which confirms the need to perform the macroscopic and histological analysis simultaneously for fisheries management studies. Microscopic observations allowed us to analyze the following six stages of cell development: oogonia, previtellogenic oocytes, primary vitellogenic oocytes, secondary vitellogenic oocytes, mature oocytes and atretic oocytes. From this, five stages of gonadal development were defined, i.e., immature, early development, advanced development, mature and spawned. The presence of peripheral bodies was not observed in this species. These results help to clarify and better understand the reproductive and population aspects of the Atlantic Seabob, which are fundamental for the establishment of management and conservation measures of this resource.

Keywords:
reproduction; gonadal development; maturation stages; histology; germ cells

Resumo

Este estudo teve como objetivo descrever e caracterizar os estágios de desenvolvimento gonadal de fêmeas de Xiphopenaeus kroyeri capturado por pescadores artesanais no Estado do Espírito Santo, região sudeste (Região sudeste = Rio de Janeiro, São Paulo, Minas Gerais e Espírito Santo) do Brasil. Todas as fêmeas (n= 1.831) foram submetidas à análise morfológica macroscópica e microscópica (n= 333) dos ovários. A partir da morfologia, coloração e grau de turgidez do ovário fresco, a análise macroscópica determinou cinco estágios de desenvolvimento gonadal. A análise macroscópica mostrou dificuldades em diferenciar os estágios imaturo e reprodutivo devido à semelhança entre as cores dos ovários, o que confirma a necessidade de realizar a análise macroscópica e histológica simultaneamente para estudos de manejo pesqueiro. As observações microscópicas permitiram analisar os seguintes seis estágios de desenvolvimento celular: oogônias, ovócitos prévitelogênicos, ovócitos em vitelogênese primária, ovócitos em vitelogênese secundária, ovócitos maduros e ovócitos atrésicos. A partir disso, foram definidos cinco estágios de desenvolvimento gonadal, ou seja, imaturo, desenvolvimento inicial, desenvolvimento avançado, maduro e desovado. A presença de corpos periféricos não foi observada nesta espécie. Estes resultados ajudam a esclarecer e compreender melhor os aspetos reprodutivos e populacionais do camarão do Atlântico, que são fundamentais para o estabelecimento de medidas de gestão e conservação deste recurso.

Palavras-chave:
reprodução; desenvolvimento gonadal; estágios de maturação; histologia; células germinativas

1. Introduction

Penaeids shrimp are one of the most commercially captured and valued resources in the world (Pérez-Farfante and Kensley, 1997PÉREZ-FARFANTE, I. and KENSLEY, B., 1997. Penaeoid and segestoid shrimps and prawns of the world: keys and diagnoses for the families and genera. Paris: Éditions du Muséum National d’Histoire Naturalle, 233 p.; FAO, 2022FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS – FAO, 2022. The state of world fisheries and aquaculture 2022: towards blue transformation. Rome: FAO. http://dx.doi.org/10.4060/cc0461en.
http://dx.doi.org/10.4060/cc0461en...
). Fishing for this resource is carried out on a large scale along the Brazilian coast and plays an important social, cultural, and especially economic role in fishing communities (Branco, 2005BRANCO, J.O., 2005. Biologia e pesca do camarão sete-barbas Xiphopenaeus kroyeri (Heller) (Crustacea, Penaeidae), na Armação do Itapocoroy, Penha, Santa Catarina, Brasil. Revista Brasileira de Zoologia, vol. 22, no. 4, pp. 1050-1062. http://dx.doi.org/10.1590/S0101-81752005000400034.
http://dx.doi.org/10.1590/S0101-81752005...
; Knox and Trigueiro, 2015KNOX, W. and TRIGUEIRO, A., 2015. A pesca artesanal no litoral no ES. In: W. KINOX and A. TRIGUEIRO, eds. Saberes, narrativas e conflitos na pesca artesanal. Vitória: EDUFES, pp. 17-49.). According to the Ministry of Fisheries and Aquaculture (MPA), in 2011, 38.7 thousand tonnes (t) of marine shrimp were captured in Brazil. Among the most caught species in fisheries are the Atlantic Seabob Xiphopenaeus kroyeri (Heller, 1862), the pink shrimp (Penaeus spp.) and the white shrimp Penaeus schmitti (Burkenroad, 1936), with the Atlantic Seabob being responsible for 39.8% (15.4 thousand t) of the country’s total marine shrimp production (Brasil, 2012BRASIL. Ministério da Pesca e Aquicultura – MPA, 2012 [viewed 30 May 2022]. Boletim Estatístico da Pesca e Aquicultura 2011 [online]. Available from: https://www.icmbio.gov.br/cepsul/images/stories/biblioteca/download/estatistica/est_2011_bol__bra.pdf
https://www.icmbio.gov.br/cepsul/images/...
).

The X. kroyeri or Atlantic Seabob as popularly known, is distributed in Venezuela, Guyana, Suriname, French Guyana and Brazil (Maranhão, Rio Grande do Norte, Alagoas, Sergipe, Bahia, Espírito Santo, Rio de Janeiro, São Paulo e Santa Catarina states), and in the Eastern Pacific, in Colombia (Carvalho-Batista et al., 2019CARVALHO-BATISTA, A., TEROSSI, M., ZARA, F.J., MANTELATTO, F.L. and COSTA, R.C., 2019. A multigene and morphological analysis expands the diversity of the seabod shrimp Xiphopenaeus Smith, 1869 (Decapoda: Penaeidae), with descriptions of two new species. Scientific Reports, vol. 9, pp. 15281. http://dx.doi.org/10.1038/s41598-019-51484-3. PMid:31653885.
http://dx.doi.org/10.1038/s41598-019-514...
). They inhabit coastal areas and regions with greater depths but are more abundant in shallower depths close to the coast, which have sandy or muddy bottoms (Costa et al., 2003COSTA, R.C., FRANSOZO, A., MELO, G.A.S. and MORAIS, F.A., 2003. Chave ilustrada para identificação dos camarões (Dendrobranchiata) do Litoral norte do Estado de São Paulo, Brasil. Biota Neotropica, vol. 3, no. 1, pp. 1-12. http://dx.doi.org/10.1590/S1676-06032003000100011.
http://dx.doi.org/10.1590/S1676-06032003...
; Costa et al., 2007COSTA, R.C., FRANSOZO, A., FREIRE, F.A. and CASTILHO, A.L., 2007. Abundance and Ecological Distribution of the “Sete-Barbas” Shrimp Xiphopenaeus kroyeri (Heller, 1862) (Decapoda: Penaeoidea) in Three Bays of the Ubatuba Region, Southeastern Brazil. Gulf and Caribbean Research, vol. 19, no. 1, pp. 33-41. http://dx.doi.org/10.18785/gcr.1901.04.
http://dx.doi.org/10.18785/gcr.1901.04...
; Boos et al., 2016BOOS, H., COSTA, R.C., SANTOS, R.A., DIAS NETO, J., RODRIGUES, E.S., RODRIGUES, L.F., D’INCAO, F. and IVO, C.T.C. 2016. Avaliação dos Camarões Peneídeos (Decapoda: Penaeidae). In: M. PINHEIRO and H. BOOS, eds. Livro vermelho dos crustáceos do Brasil: avaliação 2010-2014. Porto Alegre: Sociedade Brasileira de Carcinologia, pp. 300-316.). The life cycle occurs exclusively in the marine environment, and it is common to find juveniles and adults inhabiting the same environment (Branco, 2005BRANCO, J.O., 2005. Biologia e pesca do camarão sete-barbas Xiphopenaeus kroyeri (Heller) (Crustacea, Penaeidae), na Armação do Itapocoroy, Penha, Santa Catarina, Brasil. Revista Brasileira de Zoologia, vol. 22, no. 4, pp. 1050-1062. http://dx.doi.org/10.1590/S0101-81752005000400034.
http://dx.doi.org/10.1590/S0101-81752005...
; Santos and Freitas, 2006SANTOS, M.C.F. and FREITAS, A.E.T.S., 2006. Caracterização Biológica e Pesqueira do Camarão Sete-barbas, Xiphopenaeus kroyeri (Heller, 1862) (Crustacea, Decapoda, Penaeidae), no Pesqueiro Laminha, Área de Proteção Ambiental de Piaçabuçu (Alagoas – Brasil). Boletim Técnico-Científico do CEPENE, vol. 14, no. 1, pp. 71-91.), preferentially inhabiting shallow zones of up to 30 meters (D’Incao, 1999D’INCAO, F., 1999. Subordem Dendrobranchiata (camarões marinhos). In: L. BUCKUP and G. BOND-BUCKUP, eds. Os crustáceos do Rio Grande do Sul. Porto Alegre: Editora da Universidade Federal do Rio Grande do Sul, pp. 275-299.; Costa et al., 2003COSTA, R.C., FRANSOZO, A., MELO, G.A.S. and MORAIS, F.A., 2003. Chave ilustrada para identificação dos camarões (Dendrobranchiata) do Litoral norte do Estado de São Paulo, Brasil. Biota Neotropica, vol. 3, no. 1, pp. 1-12. http://dx.doi.org/10.1590/S1676-06032003000100011.
http://dx.doi.org/10.1590/S1676-06032003...
).

The fishing of X. kroyeri is carried out either by the artisanal fleet, which acts mainly in the coastal and estuarine environments, or by the industrial fleet, which acts exclusively in oceanic regions (D’Incao et al., 2002D’INCAO, F., VALENTINI, H. and RODRIGUES, L.F., 2002. Avaliação da pesca de camarões nas regiões sudeste e sul do Brasil. Atlântica, vol. 24, no. 2, pp. 103-116.; Boos et al., 2016BOOS, H., COSTA, R.C., SANTOS, R.A., DIAS NETO, J., RODRIGUES, E.S., RODRIGUES, L.F., D’INCAO, F. and IVO, C.T.C. 2016. Avaliação dos Camarões Peneídeos (Decapoda: Penaeidae). In: M. PINHEIRO and H. BOOS, eds. Livro vermelho dos crustáceos do Brasil: avaliação 2010-2014. Porto Alegre: Sociedade Brasileira de Carcinologia, pp. 300-316.). The artisanal fleet involved in this activity is composed basically of wooden vessels, small (6 to 10 meters long) and low power, resulting in short trips (Basilio et al., 2015BASILIO, T.H., SILVA, E.V., FIORESI, D.B., GOMES, M.P. and GARCEZ, D.S., 2015. Sustentabilidade das atividades pesqueiras do município de Piúma, Litoral sul do Espírito Santo, Brasil. Arquivos de Ciências do Mar, vol. 48, no. 1, pp. 69-86.; Musiello-Fernandes et al., 2017MUSIELLO-FERNANDES, J., ZAPPES, C.A. and HOSTIM-SILVA, M., 2017. Small-scale shrimp fisheries on the Brazilian coast: stakeholders perceptions of the closed season and integrated management. Ocean and Coastal Management, vol. 148, no. 1, pp. 89-96. http://dx.doi.org/10.1016/j.ocecoaman.2017.07.018.
http://dx.doi.org/10.1016/j.ocecoaman.20...
). The trawl net is the most used fishing gear in this type of fishing (Hostim-Silva and Soares, 2013HOSTIM-SILVA, M. and SOARES, G.S.S. 2013. Boletim estatístico da pesca do Espírito Santo - ano 2011: programa de estatística pesqueira do Espírito Santo. São Mateus: Universidade Federal do Espírito Santo, 94 p.). Despite the wide use of trawling, this activity causes significant negative impacts on marine ecosystems (Dias-Neto, 2011DIAS-NETO, J., 2011. Proposta de plano nacional de gestão para o uso sustentável de camarões marinhos do Brasil. Brasília: Ibama, 242 p.; Hiddink et al., 2017HIDDINK, J.G., JENNINGS, S., SCIBERRAS, M., SZOSTEK, C.L., HUGHES, K.M., ELLIS, N., RIJNSDORP, A.D., MCCONNAUGHEY, R.A., MAZOR, T., HILBORN, R., COLLIE, J.S., PITCHER, C.R., AMOROSO, R.O., PARMA, A.M., SUURONEN, P., 2017. Global analysis of depletion and recovery of seabed biota after bottom trawling disturbance. Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 31, pp. 8301-8306. http://dx.doi.org/10.1073/pnas.1618858114. PMid:28716926.
http://dx.doi.org/10.1073/pnas.161885811...
), since it is responsible for capturing a high percentage of bycatch, i.e., accompanying fauna (non-target species) and young specimens (Pérez-Roda et al., 2019PÉREZ-RODA, M.A., GILMAN, E., HUNTINGTON, T., KENNELLY, S.J., SUURONEN, P., CHALOUPKA, M. and MEDLEY, P., 2019. A third assessment of global marine fisheries discards. Rome: FAO, 79 p. Fisheries and Aquaculture Technical Paper, no. 633.) that have not reached sexual maturity and/or that have not yet contributed to the maintenance of the species (D’Incao et al., 2002D’INCAO, F., VALENTINI, H. and RODRIGUES, L.F., 2002. Avaliação da pesca de camarões nas regiões sudeste e sul do Brasil. Atlântica, vol. 24, no. 2, pp. 103-116.; Castilho et al., 2015CASTILHO, A.L., BAUER, R.T., FREIRE, F.A.M., FRANSOZO, V., COSTA, R.C., GRABOWSKI, R.C. and FRANSOZO, A., 2015. Lifespan and reproductive dynamics of the commercially important Seabob shimp Xiphopenaeus kroyeri (Penaeoidea): synthesis of a 5-year study. Journal of Crustacean Biology, vol. 35, no. 1, pp. 30-40. http://dx.doi.org/10.1163/1937240X-00002300.
http://dx.doi.org/10.1163/1937240X-00002...
). Studies have indicated a significant reduction in natural stocks over the years due to trawl fishery activities in coastal environments (D’Incao et al., 2002D’INCAO, F., VALENTINI, H. and RODRIGUES, L.F., 2002. Avaliação da pesca de camarões nas regiões sudeste e sul do Brasil. Atlântica, vol. 24, no. 2, pp. 103-116.; Simpson and Watling, 2006SIMPSON, A.W. and WATLING, L., 2006. An investigation of the cumulative impacts of shrimp trawling on mud-bottom fishing grounds in the Gulf of Maine: effects on habitat and macrofaunal community structure. ICES Journal of Marine Science, vol. 63, no. 9, pp. 1616-1630. http://dx.doi.org/10.1016/j.icesjms.2006.07.008.
http://dx.doi.org/10.1016/j.icesjms.2006...
; Pérez-Roda et al., 2019PÉREZ-RODA, M.A., GILMAN, E., HUNTINGTON, T., KENNELLY, S.J., SUURONEN, P., CHALOUPKA, M. and MEDLEY, P., 2019. A third assessment of global marine fisheries discards. Rome: FAO, 79 p. Fisheries and Aquaculture Technical Paper, no. 633.) since this high effort negatively interferes with the recruitment and reproduction of the species (D’Incao et al., 2002D’INCAO, F., VALENTINI, H. and RODRIGUES, L.F., 2002. Avaliação da pesca de camarões nas regiões sudeste e sul do Brasil. Atlântica, vol. 24, no. 2, pp. 103-116.; Boos et al., 2016BOOS, H., COSTA, R.C., SANTOS, R.A., DIAS NETO, J., RODRIGUES, E.S., RODRIGUES, L.F., D’INCAO, F. and IVO, C.T.C. 2016. Avaliação dos Camarões Peneídeos (Decapoda: Penaeidae). In: M. PINHEIRO and H. BOOS, eds. Livro vermelho dos crustáceos do Brasil: avaliação 2010-2014. Porto Alegre: Sociedade Brasileira de Carcinologia, pp. 300-316.).

Understanding of the reproductive aspects of a species is one of the factors that most contributes to good fishery management (Martins et al., 2013MARTINS, A.S., PINHEIRO, H.T. and LEITE-JÚNIOR, N.O., 2013. Biologia Reprodutiva do Camarão Sete-barbas no Litoral Centro Sul e Sul do Espírito Santo, Brasil. Boletim do Instituto de Pesca, vol. 39, no. 3, pp. 205-215. http://dx.doi.org/10.20950/1678-2305.2013v39n3p205.
http://dx.doi.org/10.20950/1678-2305.201...
; Bolognini et al., 2017BOLOGNINI, L., DONATO, F., LUCCHETTI, A., OLIVOTTO, I., TRUZZI, C., RANDAZZO, B., ANTONUCCI, M., ILLUMINATI, S. and GRATI, F., 2017. A multidisciplinary approach to study the reproductive biology of wild prawns. Scientific Reports, vol. 7, no. 1, pp. 16781. http://dx.doi.org/10.1038/s41598-017-16894-1. PMid:29196667.
http://dx.doi.org/10.1038/s41598-017-168...
). In this sense, obtaining information on the reproductive processes of shrimps can help in the development of management policies that minimize the impacts caused by trawling. Among the main studies used is the classification of the stages of gonadal development of the species (Quintero and Gracia, 1998QUINTERO, M.E. and GRACIA, A., 1998. Stages of gonadal development in the spotted pink shrimp Penaeus brasiliensis. Journal of Crustacean Biology, vol. 18, no. 4, pp. 680-685. http://dx.doi.org/10.2307/1549143.
http://dx.doi.org/10.2307/1549143...
; Peixoto et al., 2003PEIXOTO, S., CAVALLI, R.O., D’INCAO, F., MILACH, A.M. and WASIELESKY, W., 2003. Ovarian maturation of wild Farfantepenaeus paulensis in relation to histological and visual changes. Aquaculture Research, vol. 34, no. 1, pp. 1255-1260. http://dx.doi.org/10.1046/j.1365-2109.2003.00933.x.
http://dx.doi.org/10.1046/j.1365-2109.20...
; Simpson and Watling, 2006SIMPSON, A.W. and WATLING, L., 2006. An investigation of the cumulative impacts of shrimp trawling on mud-bottom fishing grounds in the Gulf of Maine: effects on habitat and macrofaunal community structure. ICES Journal of Marine Science, vol. 63, no. 9, pp. 1616-1630. http://dx.doi.org/10.1016/j.icesjms.2006.07.008.
http://dx.doi.org/10.1016/j.icesjms.2006...
; Lopes et al., 2014LOPES, D.F.C., SILVA, E.F., PEIXOTO, S.R.M. and FRÉDOU, F.L., 2014. Population biology of seabob-shrimp Xiphopenaeus kroyeri (Heller, 1862) captured on the south coast of Pernambuco state, Northeastern Brazil. Brazilian Journal of Oceanography, vol. 62, no. 4, pp. 331-340. http://dx.doi.org/10.1590/s1679-87592014079706204.
http://dx.doi.org/10.1590/s1679-87592014...
; Bolognini et al., 2017BOLOGNINI, L., DONATO, F., LUCCHETTI, A., OLIVOTTO, I., TRUZZI, C., RANDAZZO, B., ANTONUCCI, M., ILLUMINATI, S. and GRATI, F., 2017. A multidisciplinary approach to study the reproductive biology of wild prawns. Scientific Reports, vol. 7, no. 1, pp. 16781. http://dx.doi.org/10.1038/s41598-017-16894-1. PMid:29196667.
http://dx.doi.org/10.1038/s41598-017-168...
; Garcia et al., 2021GARCIA, R.C.P., CRAVEIRO, C.F.F., BERNABÉ, C.V., SILVA, M.A., ARIDE, P.H.R., OLIVEIRA, A.T., GONÇALVES, F.R.S.C., SANTANDER-NETO, J., LAVANDER, H.D. and FAGGIO, C., 2021. Gonadal development of females of the white shrimp Penaeus schmitti (Burkenroad, 1936) caught in southeastern Brazil. Journal of Marine Science and Engineering, vol. 9, no. 653, pp. 1-9. http://dx.doi.org/10.3390/jmse9060653.
http://dx.doi.org/10.3390/jmse9060653...
; Craveiro et al., 2022CRAVEIRO, C., SOARES, R., CASTRO-NETO, H., SILVA, E.F., SOARES, A., OLIVEIRA, P.G.V., GONZALEZ, E. and PEIXOTO, S., 2022. Ovarian maturation of Penaeus subtilis (Decapoda: Penaeidae): a new insight to describe oocyte development and somatic structures. Acta Zoologica. In press. http://dx.doi.org/10.1111/azo.12433.
http://dx.doi.org/10.1111/azo.12433...
).

The macroscopic and histological classification of the gonadal development stages is one of the most used methods in the description of the reproductive processes of penaeid shrimps (Quintero and Gracia, 1998QUINTERO, M.E. and GRACIA, A., 1998. Stages of gonadal development in the spotted pink shrimp Penaeus brasiliensis. Journal of Crustacean Biology, vol. 18, no. 4, pp. 680-685. http://dx.doi.org/10.2307/1549143.
http://dx.doi.org/10.2307/1549143...
; Bolognini et al., 2017BOLOGNINI, L., DONATO, F., LUCCHETTI, A., OLIVOTTO, I., TRUZZI, C., RANDAZZO, B., ANTONUCCI, M., ILLUMINATI, S. and GRATI, F., 2017. A multidisciplinary approach to study the reproductive biology of wild prawns. Scientific Reports, vol. 7, no. 1, pp. 16781. http://dx.doi.org/10.1038/s41598-017-16894-1. PMid:29196667.
http://dx.doi.org/10.1038/s41598-017-168...
). The microscopic classification of the ovaries aims to describe the stages of gonadal maturation at the cellular level and is increasingly used to confirm and validate the color scales determined in the macroscopic analysis (Quintero and Gracia, 1998QUINTERO, M.E. and GRACIA, A., 1998. Stages of gonadal development in the spotted pink shrimp Penaeus brasiliensis. Journal of Crustacean Biology, vol. 18, no. 4, pp. 680-685. http://dx.doi.org/10.2307/1549143.
http://dx.doi.org/10.2307/1549143...
; Lopes et al., 2014LOPES, D.F.C., SILVA, E.F., PEIXOTO, S.R.M. and FRÉDOU, F.L., 2014. Population biology of seabob-shrimp Xiphopenaeus kroyeri (Heller, 1862) captured on the south coast of Pernambuco state, Northeastern Brazil. Brazilian Journal of Oceanography, vol. 62, no. 4, pp. 331-340. http://dx.doi.org/10.1590/s1679-87592014079706204.
http://dx.doi.org/10.1590/s1679-87592014...
; Rios et al., 2022RIOS, A.S., SHINOZAKI-MENDES, R.A., SANTANA, J.L. and SOUZA-FILHO, J.F., 2022. Ovarian development of the crab Eriphia gonagra (Fabricius, 1981) (Decapoda: Brachyura: Eriphiidae) in northeastern Brazil. Journal of Crustacean Biology, vol. 42, no. 1, pp. 1-11. http://dx.doi.org/10.1093/jcbiol/ruac040.
http://dx.doi.org/10.1093/jcbiol/ruac040...
). The joint use of these analyzes guarantees a more reliable and complete description of maturation stages than estimates based only on macroscopic observations (Peixoto et al., 2003PEIXOTO, S., CAVALLI, R.O., D’INCAO, F., MILACH, A.M. and WASIELESKY, W., 2003. Ovarian maturation of wild Farfantepenaeus paulensis in relation to histological and visual changes. Aquaculture Research, vol. 34, no. 1, pp. 1255-1260. http://dx.doi.org/10.1046/j.1365-2109.2003.00933.x.
http://dx.doi.org/10.1046/j.1365-2109.20...
). These analyses are considered important tools for the definition of maturational stages, which serve as a basis for population and reproductive parameters and are fundamental for the establishment of management and conservation policies for penaeid shrimps (Peixoto et al., 2003PEIXOTO, S., CAVALLI, R.O., D’INCAO, F., MILACH, A.M. and WASIELESKY, W., 2003. Ovarian maturation of wild Farfantepenaeus paulensis in relation to histological and visual changes. Aquaculture Research, vol. 34, no. 1, pp. 1255-1260. http://dx.doi.org/10.1046/j.1365-2109.2003.00933.x.
http://dx.doi.org/10.1046/j.1365-2109.20...
; Simpson and Watling, 2006SIMPSON, A.W. and WATLING, L., 2006. An investigation of the cumulative impacts of shrimp trawling on mud-bottom fishing grounds in the Gulf of Maine: effects on habitat and macrofaunal community structure. ICES Journal of Marine Science, vol. 63, no. 9, pp. 1616-1630. http://dx.doi.org/10.1016/j.icesjms.2006.07.008.
http://dx.doi.org/10.1016/j.icesjms.2006...
; Garcia et al., 2021GARCIA, R.C.P., CRAVEIRO, C.F.F., BERNABÉ, C.V., SILVA, M.A., ARIDE, P.H.R., OLIVEIRA, A.T., GONÇALVES, F.R.S.C., SANTANDER-NETO, J., LAVANDER, H.D. and FAGGIO, C., 2021. Gonadal development of females of the white shrimp Penaeus schmitti (Burkenroad, 1936) caught in southeastern Brazil. Journal of Marine Science and Engineering, vol. 9, no. 653, pp. 1-9. http://dx.doi.org/10.3390/jmse9060653.
http://dx.doi.org/10.3390/jmse9060653...
).

The gonadal development of the species X. kroyeri was previously described by many authors, for different regions of Brazil (Campos et al., 2009CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12.; Martins et al., 2013MARTINS, A.S., PINHEIRO, H.T. and LEITE-JÚNIOR, N.O., 2013. Biologia Reprodutiva do Camarão Sete-barbas no Litoral Centro Sul e Sul do Espírito Santo, Brasil. Boletim do Instituto de Pesca, vol. 39, no. 3, pp. 205-215. http://dx.doi.org/10.20950/1678-2305.2013v39n3p205.
http://dx.doi.org/10.20950/1678-2305.201...
; Lopes et al., 2017LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951.
http://dx.doi.org/10.1080/07924259.2017....
). Martins et al. (2013)MARTINS, A.S., PINHEIRO, H.T. and LEITE-JÚNIOR, N.O., 2013. Biologia Reprodutiva do Camarão Sete-barbas no Litoral Centro Sul e Sul do Espírito Santo, Brasil. Boletim do Instituto de Pesca, vol. 39, no. 3, pp. 205-215. http://dx.doi.org/10.20950/1678-2305.2013v39n3p205.
http://dx.doi.org/10.20950/1678-2305.201...
used only macroscopic analysis to classify the stages, while Campos et al. (2009)CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12. and Lopes et al. (2017)LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951.
http://dx.doi.org/10.1080/07924259.2017....
used macroscopic and microscopic analyzes together. These studies classified the development of the ovary into four stages of maturation, namely: immature, developing, mature and spawned. However, several authors classified the ovarian development of other penaeid species into five different stages: immature, early maturation, advanced maturation, mature and spawning such as Vogt et al. (1989)VOGT, G., QUINITIO, E.T. and PASCUAL, F.P., 1989. Interaction of the midgut gland and the ovary in vitellogenesis and consequences for the breeding success: a comparison of unablated and ablated spawners of Penaeus monodon. In: DE PAUW, J.N., ACKEFORS, H., WILKINS, N.E. eds. Aquaculture: a biotechnology in progress. Bredene: European Aquaculture Society, pp. 581-592., Castille and Lawrence (1991)CASTILLE, F.L. and LAWRENCE, A.L., 1991. Reproductive studies concerning natural shrimp populations: a description of changes in size and biochemical compositions of the gonads and digestive glands in penaeid shrimps. In: P.F. DE LOACH, W.J. DOUGHERTY and M.A. DAVIDSON, eds. Frontiers of shrimp research. Amsterdam: Elsevier, pp. 17-32., Tan-Fermin (1991)TAN-FERMIN, J.D., 1991. Effects of unilateral eyestalk ablation on ovarian histology and oocyte size frequency of wild and pond-reared Penaeus monodon (Fabricius) broodstock. Aquaculture, vol. 93, no. 1, pp. 77-86. http://dx.doi.org/10.1016/0044-8486(91)90206-M.
http://dx.doi.org/10.1016/0044-8486(91)9...
, Medina et al. (1996)MEDINA, A., VILA, Y., MOURENTE, G.E. and RODRÍGUEZ, A., 1996. A comparative study of the ovarian development in wild and pond-reared shrimp, Penaeus kerathurus (Förskal, 1775). Aquaculture (Amsterdam, Netherlands), vol. 148, no. 1, pp. 63-75. http://dx.doi.org/10.1016/S0044-8486(96)01408-1.
http://dx.doi.org/10.1016/S0044-8486(96)...
; Quintero and Gracia (1998)QUINTERO, M.E. and GRACIA, A., 1998. Stages of gonadal development in the spotted pink shrimp Penaeus brasiliensis. Journal of Crustacean Biology, vol. 18, no. 4, pp. 680-685. http://dx.doi.org/10.2307/1549143.
http://dx.doi.org/10.2307/1549143...
, Palacios et al. (1999)PALACIOS, E., RODRÍGUEZ-JARAMILLO, C. and RACOTTA, I.S., 1999. Comparison of ovary histology between different-sized wild and pond-reared shrimp Litopenaeus vannamei (Penaeus vannamei). Invertebrate Reproduction & Development, vol. 35, no. 3, pp. 251-259. http://dx.doi.org/10.1080/07924259.1999.9652391.
http://dx.doi.org/10.1080/07924259.1999....
, Ayub and Ahmed (2002)AYUB, Z. and AHMED, M.A., 2002. Description of the ovarian development stages of penaeid shrimp from the coast of Pakistan. Aquaculture Research, vol. 33, no. 1, pp. 767-776. http://dx.doi.org/10.1046/j.1365-2109.2002.00715.x.
http://dx.doi.org/10.1046/j.1365-2109.20...
, and recent studies as those by Bolognini et al. (2017)BOLOGNINI, L., DONATO, F., LUCCHETTI, A., OLIVOTTO, I., TRUZZI, C., RANDAZZO, B., ANTONUCCI, M., ILLUMINATI, S. and GRATI, F., 2017. A multidisciplinary approach to study the reproductive biology of wild prawns. Scientific Reports, vol. 7, no. 1, pp. 16781. http://dx.doi.org/10.1038/s41598-017-16894-1. PMid:29196667.
http://dx.doi.org/10.1038/s41598-017-168...
, Craveiro et al. (2019)CRAVEIRO, C., PEIXOTO, S., SILVA, E.F., EDUARDO, L.N., LIRA, A.S., CASTRO-NETO, H., FRÉDOU, F. and SOARES, R., 2019. Reproductive dynamics of the white shrimp Litopenaeus schmitti (Burkenroad 1936) in a beach seine fishery in northeastern Brazil. Invertebrate Reproduction & Development, vol. 63, no. 2, pp. 111-121. http://dx.doi.org/10.1080/07924259.2019.1575923.
http://dx.doi.org/10.1080/07924259.2019....
and Garcia et al. (2021)GARCIA, R.C.P., CRAVEIRO, C.F.F., BERNABÉ, C.V., SILVA, M.A., ARIDE, P.H.R., OLIVEIRA, A.T., GONÇALVES, F.R.S.C., SANTANDER-NETO, J., LAVANDER, H.D. and FAGGIO, C., 2021. Gonadal development of females of the white shrimp Penaeus schmitti (Burkenroad, 1936) caught in southeastern Brazil. Journal of Marine Science and Engineering, vol. 9, no. 653, pp. 1-9. http://dx.doi.org/10.3390/jmse9060653.
http://dx.doi.org/10.3390/jmse9060653...
. This difference is due to the lack of standardization in the maturation classification stages in shrimp, which so far does not have a solid/well-detailed basis to follow, making it difficult to take measures to manage these resources.

In this context, the present study aimed to describe and characterize in detail the stages of ovarian development of the Atlantic Seabob (X. kroyeri) caught in Espírito Santo state, southeastern Brazil, in order to obtain relevant information on the reproductive aspects of the species and contribute to a better management of this resource of great economic importance.

2. Material and Methods

2.1. Study area and sample processing

Shrimps were caught for 12 months (March 2019 to February 2020) by artisanal fishers in the municipalities of Anchieta (20° 48’ 21” S 40° 38’ 44” W), Piúma (20° 50’ 7” S 40° 43’ 42” W) and Itapemirim (21° 0’ 42” S 40° 50’ 2” W), located in the southern region of the state of Espírito Santo, southeastern Brazil (Figure 1).

Figure 1
Geographical location of the study area on the southern coast of the state of Espírito Santo, southeastern region of Brazil.

Sampling was carried out with the authorization of the SISBIO Biodiversity Information and Authorization System No. 67056-1 and 67056-2, based on ICMBio Normative Instruction Nº. 03/2014 (Brasil, 2014BRASIL 2014 [viewed 15 May 2022]. Instrução normativa nº 03, de setembro de 2014 [online]. Diário Oficial da República Federativa do Brasil, Brasilia. Available from: https://www.icmbio.gov.br/flonatapajos/images/stories/INSTRU%C3%87%C3%83O_NORMATIVA_ICMBio_N%C2%BA_3_DE_2014__com_retifica%C3%A7%C3%A3o_do_DOU18062015.pdf
https://www.icmbio.gov.br/flonatapajos/i...
). The specimens were captured by a local motorized vessel 10 meters long, operating with double bottom trawl nets with wooden trawl doors. The net was 12 m long, with a 2.5 m wide mouth, 30 mm meshes (between knots) on the wings and body of the net, and 15 mm (between knots) on the bagger. The trawls were carried out in typical areas of shrimp fisheries, in a range of 4 to 20 meters in depth, lasting 60 minutes each at an approximate speed of 1.5 to 2 knots.

After each trawl, the captured shrimps were separated from the bycatch, then packed in plastic bags and stored in a thermal box with ice. Subsequently, the samples were transported to the laboratory, where individuals were identified as to species according to the Illustrated Key for Dendrobranchiata Shrimp Identification of Costa et al. (2003)COSTA, R.C., FRANSOZO, A., MELO, G.A.S. and MORAIS, F.A., 2003. Chave ilustrada para identificação dos camarões (Dendrobranchiata) do Litoral norte do Estado de São Paulo, Brasil. Biota Neotropica, vol. 3, no. 1, pp. 1-12. http://dx.doi.org/10.1590/S1676-06032003000100011.
http://dx.doi.org/10.1590/S1676-06032003...
, taking into consideration the genetic studies conducted by Carvalho-Batista et al. (2019)CARVALHO-BATISTA, A., TEROSSI, M., ZARA, F.J., MANTELATTO, F.L. and COSTA, R.C., 2019. A multigene and morphological analysis expands the diversity of the seabod shrimp Xiphopenaeus Smith, 1869 (Decapoda: Penaeidae), with descriptions of two new species. Scientific Reports, vol. 9, pp. 15281. http://dx.doi.org/10.1038/s41598-019-51484-3. PMid:31653885.
http://dx.doi.org/10.1038/s41598-019-514...
in the state of Espírito Santo, Brazil. After the identification of the species, they were separated by sex according to their external characters (presence of petasma in males and thelycum in females).

Then, the females were measured for total length (TL: from the tip of the rostrum to the tip of the telson) and the length of the cephalothorax (CL: from the base of the rostrum to the upper margin of the carapace) with analog calipers (0.05 mm).

2.2. Macroscopic and microscopic description of the ovaries

All females were subjected to macroscopic evaluation of the ovaries through morphology (n= 1,831), and the degree of turgidity and coloration of the fresh gonads were compared with a widely available color catalog (Pantone Matching System, Coated Simulation, Pantone, Carlstadt, NJ, USA).

For histological analysis, 333 ovaries were used (approximately 25 females randomly sampled per month), which were dissected, weighed and pre-classified as to their macroscopic maturational stage (adapted from Craveiro et al., 2019CRAVEIRO, C., PEIXOTO, S., SILVA, E.F., EDUARDO, L.N., LIRA, A.S., CASTRO-NETO, H., FRÉDOU, F. and SOARES, R., 2019. Reproductive dynamics of the white shrimp Litopenaeus schmitti (Burkenroad 1936) in a beach seine fishery in northeastern Brazil. Invertebrate Reproduction & Development, vol. 63, no. 2, pp. 111-121. http://dx.doi.org/10.1080/07924259.2019.1575923.
http://dx.doi.org/10.1080/07924259.2019....
; Craveiro et al., 2022CRAVEIRO, C., SOARES, R., CASTRO-NETO, H., SILVA, E.F., SOARES, A., OLIVEIRA, P.G.V., GONZALEZ, E. and PEIXOTO, S., 2022. Ovarian maturation of Penaeus subtilis (Decapoda: Penaeidae): a new insight to describe oocyte development and somatic structures. Acta Zoologica. In press. http://dx.doi.org/10.1111/azo.12433.
http://dx.doi.org/10.1111/azo.12433...
). The samples were fixed in Davidson’s solution for 24 hours, then transferred and stored in 70% ethanol (Bell and Lightner, 1988BELL, T.A. and LIGHTNER, D.V., 1988. A handbook of normal penaeid shrimp histology. Baton Rouge: World Aquaculture Society, 114 p.).

For the microscopic description, fragments of the median portion of each ovary were subjected to dehydration in increasing series of ethanol (70-100%), diaphanized in xylol, impregnated and set in paraffin at 55 °C. After embedding in paraffin, the tissues were sectioned (5 µm) in a rotating microtome and stained using the Haematoxylin(H)/Eosin-phloxine(E-P) method (adapted from Junqueira and Junqueira, 1983JUNQUEIRA, L.C. and JUNQUEIRA, L.M.M.S., 1983. Técnicas básicas de citologia e histologia. São Paulo: Livraria e Editora Santos, 123 p.). All slides were photographed through the optical microscope equipped with a digital camera, using the Leica LAS EZ 3.4 software for the characterization of gonadal development at the cellular level. The photomicrographs of the slides were digitized with Leica software with objectives from 4x to 100x of magnification.

Oocytes were classified according to the histological characteristics described for penaeids (adapted from Craveiro et al., 2019CRAVEIRO, C., PEIXOTO, S., SILVA, E.F., EDUARDO, L.N., LIRA, A.S., CASTRO-NETO, H., FRÉDOU, F. and SOARES, R., 2019. Reproductive dynamics of the white shrimp Litopenaeus schmitti (Burkenroad 1936) in a beach seine fishery in northeastern Brazil. Invertebrate Reproduction & Development, vol. 63, no. 2, pp. 111-121. http://dx.doi.org/10.1080/07924259.2019.1575923.
http://dx.doi.org/10.1080/07924259.2019....
; Craveiro et al., 2022CRAVEIRO, C., SOARES, R., CASTRO-NETO, H., SILVA, E.F., SOARES, A., OLIVEIRA, P.G.V., GONZALEZ, E. and PEIXOTO, S., 2022. Ovarian maturation of Penaeus subtilis (Decapoda: Penaeidae): a new insight to describe oocyte development and somatic structures. Acta Zoologica. In press. http://dx.doi.org/10.1111/azo.12433.
http://dx.doi.org/10.1111/azo.12433...
) and about 100 oocytes (or total number available per category) presenting sectioned nucleus were measured using the Image Tool software version 2.0 for Windows (University of Texas Health Science Center in San Antonio, TX, USA). The mean and standard deviation were obtained for the diameter of the oocytes and were subsequently subjected to analysis of variance (ANOVA) at a 5% confidence interval, considering the necessary assumptions of normality and homoscedasticity, which was followed by the Tukey test (p<0.05) for the separation of means in case of significant differences.

3. Results

Over 12 months, 1,831 females were captured (approximately 153±49 females per month), which varied in total length from 42 to 146 mm (mean: 101.4±19 mm), cephalothorax length from 8 to 35 mm (mean: 21.2±5 mm) and total wet weight ranging from 0.7 to 18.2 g (mean: 6.4±3.3 g).

3.1. Macroscopic description of the ovaries

The ovary of the female of X. kroyeri is a symmetrical organ and presents bilateral symmetry. It has a tubular shape and is fused in the cephalothorax region all the way to the final portion of the abdomen. They have two anterior lobes, seven short lateral lobes and two long posterior lobes, which undergo changes in coloration, consistency, and turgidity as they develop. It has two oviducts located in the dorsal-ventral portion, which connect to the genital pores located at the base of the third pair of pereiopods. From the macroscopic analysis of the ovaries, it was possible to determine five distinct maturational stages for the species X. kroyeri, as described below:

Stage I (immature) – the ovaries are extremely small and thin. They have a smooth, inconsistent surface and translucent coloration (without Pantone code catalog), and they cannot be visualized through the exoskeleton (Figure 2a). The average weight of the ovaries at this stage is 0.01±0.04 g.

Figure 2
Schematic representation of the different stages of ovarian development of the Atlantic Seabob Xiphopenaeus kroyeri (Heller, 1862) caught in southeastern Brazil. Key: (a) Stage I – immature (translucent coloring), (b) Stage II – initial maturation (Pantone code catalog: 375 PC), (c) Stage III – advanced maturation (Pantone code catalog: 377 PC), (d) stage IV – mature (Pantone code catalog: 5753 PC), and (e) Stage V – spawned (Pantone code catalog: 585 PC or translucent coloring).

Stage II (initial maturation) – the ovaries are at the beginning of maturation, with the gonad increasing in size and weight (average weight: 0.28±0.20 g) when compared to Stage I. They have little coloration in the anterior and lateral lobes, and it is possible to visualize them with a light green coloration (Pantone code catalog 375 PC) through the exoskeleton, though only in the cephalothorax region (Figure 2b).

Stage III (advanced maturation) – the ovaries are more developed, larger, and heavier (average weight: 0.34±0.25 g) compared to the previous stage. They have a more pronounced medium green coloration in all lobes (Pantone code catalog 377 PC) and are less evident in the abdominal region (Figure 2c).

Stage IV (mature) – the ovaries are at the maximum level of maturation, and present a rough, consistent surface and more intense dark green coloration (Pantone code catalog 5753 PC) throughout the dorsal cavity (Fig 2d). The average weight of the ovaries at this stage is 0.42±0.27 g.

Stage V (spawned) – the females have already spawned, that is, the mature oocytes have been expelled into the environment. Currently, the ovaries are flabby, with a slightly rough surface and have a very discreet coloration (Pantone code catalog 585 PC) or are translucent (Figure 2e). The average weight of the ovaries at this stage is 0.08±0.07 g.

3.2. Microscopic description of the ovaries

In the microscopic analysis, it was possible to identify six phases of cell development, namely, oogonia (OO), previtellogenic oocytes (PVTG), primary vitellogenic oocytes (VTG1), secondary vitellogenic oocytes (VTG2), mature oocytes (MO) and atretic oocytes (AO). From the macroscopic and histological analysis, it was possible to determine five stages of gonadal development at the cellular level (Figure 3), as described below:

Figure 3
Microphotographs of the stages of ovarian development of the shrimp Xiphopenaeus kroyeri (Heller, 1862) caught off the coast of Espírito Santo, Brazil. (a, b) immature [translucent coloring (Figure 2a)]; (c, d) initial maturation [Pantone code catalog: 375 PC (Figure 2b)]; (e, f) advanced maturation [Pantone code catalog: 377 PC (Figure 2c)]; (g, h) mature [Pantone code catalog: 5753 PC (Figure 2d)]; and (i, j) spawned [Pantone code catalog: 585 PC (Figure 2e)]. (OO) oogonia; (PVTG) previtellogenic oocyte; (VTG1) primary vitellogenic oocyte; (VTG2) secondary vitellogenic oocyte; (OM) mature oocyte; (OA) atretic oocyte; (gw) gonadal wall; (gz) germinative zone; (n) nucleus; (fc) follicular cells. [10x objective (a, c, e, g, i) 40x objective (b, d, f, h, j)].

Stage I (immature) (Figure 33b) – there is a predominance of basophilic cells oogonia (OO) and previtellogenic oocytes (PVTG), i.e., cells evidenced by blue-purple staining (H). OO have a nucleus (n) that is proportionally larger than the cytoplasm, which is a spherical shape and is organized in the germinative zone (gz; Figure 3c), located in the central region of the ovary. The PVTG have an oval shape, cytoplasm that is more developed compared to OO and have nucleoli on the periphery of the nucleus. Follicular cells (fc) are cubic in shape and are dispersed throughout the ovary. The gonadal wall (gw; Figure 3b) is thinner compared to the other stages of gonadal development.

Stage II (initial maturation) (Figure 33d) – there is a dominance of acidophilic cells, which are the primary vitellogenic oocytes (VTG1), i.e., cells evidenced by pink coloring (E-P). In addition, it is possible to visualize the presence of three to six nucleoli that are strongly stained by Haematoxylin, evidencing the basophilic characteristic in the nucleus. The VTG1 has the most developed cytoplasm when compared to the OO and PVTG, this is due to the initial deposit of lipid droplets in the cell cytoplasm. OO and PVTG are also found at this stage, but in smaller quantities. Follicular cells (fc) have a cubic shape and are better organized, forming clusters around VTG1.

Stage III (advanced maturation) (Figure 33f) – there is a predominance of secondary vitellogenic oocytes (VTG2), evidenced by pink staining (E-P) of the cytoplasm and purple staining of the nucleus (H). In addition, it is possible to visualize the presence of acidophilic globules in the periphery of the nucleus and large droplets of yolk along the cytoplasm of the cell, giving it a granular appearance. OO and PVTG are found in smaller amounts. Follicular cells (fc) have a scaly shape and form clusters around VTG2.

Stage IV (mature) (Figure 33h) – there is a predominance of mature oocytes (MO), which have highly acidophilic cytoplasm (E-P) and the basophilic nucleus (H), and are evidenced by the pink and purple coloration, respectively. At this stage, it is possible to observe yolk granules throughout the cell cytoplasm. They present basophilic cells (OO and PVTG) in a lower quantity when compared to stages I, II and III. Follicular cells (fc) form an outer layer of MO.

Stage V (spawned) (Figure 33j) – The OO and PVTG are dominant at this stage, which is evidenced by the blue-purple coloration (Haematoxylin). Oocytes in atresia (AO) have acidophilic nature (Eosin-phloxine) and, due to the rupture of the cell membrane, the shape of this cell is not well defined. This process is the result of resorption of mature oocytes that were not released during spawning or may even be due to environmental stress. Follicular cells (fc) are cubic in shape and are dispersed throughout the ovary. The gonadal wall is thick and has a loose/disorganized appearance (Figure 3i). As the gonads develop and undergo reproductive events, the gonadal wall tends to get thicker and loose, and does not return to its initial state, which is the main characteristic that differentiates the spawned stage from the immature stage.

Germ cells (OO and PVTG) were found in all stages of gonad development and showed greater frequency in the immature and spawned stages. As the gonad develops, the concentration of OO and PVTG decreases, giving way to vitellogenic oocytes (VTG1, VTG2 and MO) (Table 1). As the germ cells develop, the cytoplasm increases in size, with OO having the smallest diameter (5.97±1.88 µm), followed by PVTG (32.82±9.55 µm), VTG1 (95.71±14.94 µm), VTG2 (138.64±16.01 µm) and MO (185.32±22.09 µm) (Table 1).

Table 1
Diameter for each oocyte phase (mean±SD) and cell composition observed at each gonadal maturity stage of Xiphopenaeus kroyeri (Heller, 1862) captured off the coast of Espírito Santo, Brazil.

4. Discussion

Females of penaeid shrimps have different stages of gonadal maturation throughout the reproductive cycle (Dall et al., 1990DALL, W., HILL, B.J., ROTHLISBERG, P.C. and STAPLES, D.J., 1990. The biology of the Penaeidae. In: W. DALL, J. HILL, P. ROTHLISBERG, D.J. SHARPLES and A. SOUTHWARD, eds. Advances in marine biology. Cambridge: Academic Press, pp. 283-314.; Bolognini et al., 2017BOLOGNINI, L., DONATO, F., LUCCHETTI, A., OLIVOTTO, I., TRUZZI, C., RANDAZZO, B., ANTONUCCI, M., ILLUMINATI, S. and GRATI, F., 2017. A multidisciplinary approach to study the reproductive biology of wild prawns. Scientific Reports, vol. 7, no. 1, pp. 16781. http://dx.doi.org/10.1038/s41598-017-16894-1. PMid:29196667.
http://dx.doi.org/10.1038/s41598-017-168...
); however, there is still no standardization of the classification of maturational stages. In the present study, the ovarian development of the species X. kroyeri was classified into five different maturational stages, which have also been described for other shrimp species belonging to the genus Penaeus (Bolognini et al., 2017BOLOGNINI, L., DONATO, F., LUCCHETTI, A., OLIVOTTO, I., TRUZZI, C., RANDAZZO, B., ANTONUCCI, M., ILLUMINATI, S. and GRATI, F., 2017. A multidisciplinary approach to study the reproductive biology of wild prawns. Scientific Reports, vol. 7, no. 1, pp. 16781. http://dx.doi.org/10.1038/s41598-017-16894-1. PMid:29196667.
http://dx.doi.org/10.1038/s41598-017-168...
; Craveiro et al., 2019CRAVEIRO, C., PEIXOTO, S., SILVA, E.F., EDUARDO, L.N., LIRA, A.S., CASTRO-NETO, H., FRÉDOU, F. and SOARES, R., 2019. Reproductive dynamics of the white shrimp Litopenaeus schmitti (Burkenroad 1936) in a beach seine fishery in northeastern Brazil. Invertebrate Reproduction & Development, vol. 63, no. 2, pp. 111-121. http://dx.doi.org/10.1080/07924259.2019.1575923.
http://dx.doi.org/10.1080/07924259.2019....
; Garcia et al., 2021GARCIA, R.C.P., CRAVEIRO, C.F.F., BERNABÉ, C.V., SILVA, M.A., ARIDE, P.H.R., OLIVEIRA, A.T., GONÇALVES, F.R.S.C., SANTANDER-NETO, J., LAVANDER, H.D. and FAGGIO, C., 2021. Gonadal development of females of the white shrimp Penaeus schmitti (Burkenroad, 1936) caught in southeastern Brazil. Journal of Marine Science and Engineering, vol. 9, no. 653, pp. 1-9. http://dx.doi.org/10.3390/jmse9060653.
http://dx.doi.org/10.3390/jmse9060653...
). Notwithstanding, other studies have classified gonad development into only four stages, condensing the early maturation and advanced maturation stages into a single stage, which is named as “in development” (Peixoto et al., 2003PEIXOTO, S., CAVALLI, R.O., D’INCAO, F., MILACH, A.M. and WASIELESKY, W., 2003. Ovarian maturation of wild Farfantepenaeus paulensis in relation to histological and visual changes. Aquaculture Research, vol. 34, no. 1, pp. 1255-1260. http://dx.doi.org/10.1046/j.1365-2109.2003.00933.x.
http://dx.doi.org/10.1046/j.1365-2109.20...
; Campos et al., 2009CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12.; Martins et al., 2013MARTINS, A.S., PINHEIRO, H.T. and LEITE-JÚNIOR, N.O., 2013. Biologia Reprodutiva do Camarão Sete-barbas no Litoral Centro Sul e Sul do Espírito Santo, Brasil. Boletim do Instituto de Pesca, vol. 39, no. 3, pp. 205-215. http://dx.doi.org/10.20950/1678-2305.2013v39n3p205.
http://dx.doi.org/10.20950/1678-2305.201...
; Lopes et al., 2017LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951.
http://dx.doi.org/10.1080/07924259.2017....
). The differentiation in a greater number of stages implies the ability to define maturation with more precision and detail the differences in and phases of cell development, which can assist studies of population and reproductive dynamics (Garcia et al., 2021GARCIA, R.C.P., CRAVEIRO, C.F.F., BERNABÉ, C.V., SILVA, M.A., ARIDE, P.H.R., OLIVEIRA, A.T., GONÇALVES, F.R.S.C., SANTANDER-NETO, J., LAVANDER, H.D. and FAGGIO, C., 2021. Gonadal development of females of the white shrimp Penaeus schmitti (Burkenroad, 1936) caught in southeastern Brazil. Journal of Marine Science and Engineering, vol. 9, no. 653, pp. 1-9. http://dx.doi.org/10.3390/jmse9060653.
http://dx.doi.org/10.3390/jmse9060653...
).

In relation to the macroscopic ovarian coloration pattern found in this study, the initial maturation stage was characterized by light green coloration that intensified as the gonads developed until they reached the mature stage, which is characterized by a more intense dark green coloration. The same pattern was found for the same species in other regions of Brazil, such as in the south (Campos et al., 2009CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12.), southeast (Martins et al., 2013MARTINS, A.S., PINHEIRO, H.T. and LEITE-JÚNIOR, N.O., 2013. Biologia Reprodutiva do Camarão Sete-barbas no Litoral Centro Sul e Sul do Espírito Santo, Brasil. Boletim do Instituto de Pesca, vol. 39, no. 3, pp. 205-215. http://dx.doi.org/10.20950/1678-2305.2013v39n3p205.
http://dx.doi.org/10.20950/1678-2305.201...
) and northeast (Lopes et al., 2017LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951.
http://dx.doi.org/10.1080/07924259.2017....
). The coloring of the ovary may be due to the type of carotenoid pigment assimilated by the body during feeding (Liñán-Cabello et al., 2002LIÑÁN-CABELLO, M.A., PANIAGUA-MICHEL, J. and HOPKINS, P.M., 2002. Bioactive roles of carotenoids and retinoids in crustaceans. Aquaculture Nutrition, vol. 8, no. 4, pp. 299-309. http://dx.doi.org/10.1046/j.1365-2095.2002.00221.x.
http://dx.doi.org/10.1046/j.1365-2095.20...
). In these organisms, the intensification of the green color occurs due to the constant accumulation of carotenoid pigments during the vitellogenic phase (Liñán-Cabello et al., 2002LIÑÁN-CABELLO, M.A., PANIAGUA-MICHEL, J. and HOPKINS, P.M., 2002. Bioactive roles of carotenoids and retinoids in crustaceans. Aquaculture Nutrition, vol. 8, no. 4, pp. 299-309. http://dx.doi.org/10.1046/j.1365-2095.2002.00221.x.
http://dx.doi.org/10.1046/j.1365-2095.20...
), which are important components for the embryonic development and reproductive success of these species (Bolognini et al., 2017BOLOGNINI, L., DONATO, F., LUCCHETTI, A., OLIVOTTO, I., TRUZZI, C., RANDAZZO, B., ANTONUCCI, M., ILLUMINATI, S. and GRATI, F., 2017. A multidisciplinary approach to study the reproductive biology of wild prawns. Scientific Reports, vol. 7, no. 1, pp. 16781. http://dx.doi.org/10.1038/s41598-017-16894-1. PMid:29196667.
http://dx.doi.org/10.1038/s41598-017-168...
; Souza et al., 2017SOUZA, T.L., BRAGA, A.A., LÓPEZ-GRECO, L. and NUNES, E.T., 2017. Dynamic of oogenesis in ghost shrimp Callichirus major (Crustacea: Axiidea): a morphofunctional and histochemical study. Acta Histochemica, vol. 119, no. 8, pp. 769-777. http://dx.doi.org/10.1016/j.acthis.2017.09.001. PMid:28988659.
http://dx.doi.org/10.1016/j.acthis.2017....
).

The stages of gonadal development in penaeid shrimps are basically determined by the presence of basophilic, vitellogenic and/or atretic oocytes (Quintero and Gracia, 1998QUINTERO, M.E. and GRACIA, A., 1998. Stages of gonadal development in the spotted pink shrimp Penaeus brasiliensis. Journal of Crustacean Biology, vol. 18, no. 4, pp. 680-685. http://dx.doi.org/10.2307/1549143.
http://dx.doi.org/10.2307/1549143...
; Peixoto et al., 2003PEIXOTO, S., CAVALLI, R.O., D’INCAO, F., MILACH, A.M. and WASIELESKY, W., 2003. Ovarian maturation of wild Farfantepenaeus paulensis in relation to histological and visual changes. Aquaculture Research, vol. 34, no. 1, pp. 1255-1260. http://dx.doi.org/10.1046/j.1365-2109.2003.00933.x.
http://dx.doi.org/10.1046/j.1365-2109.20...
). Previtellogenic oogonia and oocytes develop from the proliferation zone (germinative zone) and, as they mature, they give rise to vitellogenic oocytes (Peixoto et al., 2003PEIXOTO, S., CAVALLI, R.O., D’INCAO, F., MILACH, A.M. and WASIELESKY, W., 2003. Ovarian maturation of wild Farfantepenaeus paulensis in relation to histological and visual changes. Aquaculture Research, vol. 34, no. 1, pp. 1255-1260. http://dx.doi.org/10.1046/j.1365-2109.2003.00933.x.
http://dx.doi.org/10.1046/j.1365-2109.20...
; Abraham and Manisseri, 2012ABRAHAM, J. and MANISSERI, M.K., 2012. Histological and morphological changes associated with ovarian development of speckled shrimp Matapenaeus monoceros (Fabricius, 1798). Indian Journal of Fisheries, vol. 59, no. 1, pp. 119-124.). In the present study, basophilic oocytes (OO and PVTG) were found in all stages of development; however, in stages I and V they were more frequent. In addition, it was also possible to visualize the increase in the diameter of oocytes throughout the maturation process (Table 1), which occurs due to the constant accumulation of yolk granules (reserve substances) deposited in the cell cytoplasm. The frequency and increase in the size of X. kroyeri oocytes showed similarity to results found in studies with the same species (Lopes et al., 2017LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951.
http://dx.doi.org/10.1080/07924259.2017....
), as well as other species of penaeids (Quintero and Gracia, 1998QUINTERO, M.E. and GRACIA, A., 1998. Stages of gonadal development in the spotted pink shrimp Penaeus brasiliensis. Journal of Crustacean Biology, vol. 18, no. 4, pp. 680-685. http://dx.doi.org/10.2307/1549143.
http://dx.doi.org/10.2307/1549143...
; Bolognini et al., 2017BOLOGNINI, L., DONATO, F., LUCCHETTI, A., OLIVOTTO, I., TRUZZI, C., RANDAZZO, B., ANTONUCCI, M., ILLUMINATI, S. and GRATI, F., 2017. A multidisciplinary approach to study the reproductive biology of wild prawns. Scientific Reports, vol. 7, no. 1, pp. 16781. http://dx.doi.org/10.1038/s41598-017-16894-1. PMid:29196667.
http://dx.doi.org/10.1038/s41598-017-168...
; Peixoto et al., 2018PEIXOTO, S., CALAZANS, N., SILVA, E.F., NOLÉ, L., SOARES, R. and FRÉDOU, F.L., 2018. Reproduction cycle and size at first sexual maturity of the white shrimp Penaeus schmitti (Burkenroad, 1936) in northeastern Brazil. Latin American Journal of Aquatic Research, vol. 46, no. 1, pp. 1-9. http://dx.doi.org/10.3856/vol46-issue1-fulltext-1.
http://dx.doi.org/10.3856/vol46-issue1-f...
; Craveiro et al., 2019CRAVEIRO, C., PEIXOTO, S., SILVA, E.F., EDUARDO, L.N., LIRA, A.S., CASTRO-NETO, H., FRÉDOU, F. and SOARES, R., 2019. Reproductive dynamics of the white shrimp Litopenaeus schmitti (Burkenroad 1936) in a beach seine fishery in northeastern Brazil. Invertebrate Reproduction & Development, vol. 63, no. 2, pp. 111-121. http://dx.doi.org/10.1080/07924259.2019.1575923.
http://dx.doi.org/10.1080/07924259.2019....
).

In addition to germ cells, other components were also considered essential in stage differentiation, such as gonadal wall thickness and follicular cells (Craveiro et al., 2022CRAVEIRO, C., SOARES, R., CASTRO-NETO, H., SILVA, E.F., SOARES, A., OLIVEIRA, P.G.V., GONZALEZ, E. and PEIXOTO, S., 2022. Ovarian maturation of Penaeus subtilis (Decapoda: Penaeidae): a new insight to describe oocyte development and somatic structures. Acta Zoologica. In press. http://dx.doi.org/10.1111/azo.12433.
http://dx.doi.org/10.1111/azo.12433...
). The thickness of the gonadal wall changes in size and arrangement as females undergo reproductive events (Craveiro et al. 2022CRAVEIRO, C., SOARES, R., CASTRO-NETO, H., SILVA, E.F., SOARES, A., OLIVEIRA, P.G.V., GONZALEZ, E. and PEIXOTO, S., 2022. Ovarian maturation of Penaeus subtilis (Decapoda: Penaeidae): a new insight to describe oocyte development and somatic structures. Acta Zoologica. In press. http://dx.doi.org/10.1111/azo.12433.
http://dx.doi.org/10.1111/azo.12433...
). As a result, the ovary wall tends to become thicker and looser, unlike immature ovaries which have a thin, consistent wall. Therefore, these characteristics have become fundamental in identifying immature females from females that have already spawned at least once. Follicular cells were also considered key components in differentiating the stages of maturation, because their shape and arrangement changed as the oocytes increased in size (Worsmann et al., 1976WORSMANN, T.U., BARCELOS, S.R. and FERRI, A.C., 1976. Étude histologique de l’ovaire de Penaeus paulensis Pérez-Farfante, 1967. Boletim do Instituto Oceanográfico, vol. 25, no. 1, pp. 43-54. http://dx.doi.org/10.1590/S0373-55241976000100003.
http://dx.doi.org/10.1590/S0373-55241976...
; Chang and Shih, 1995; Craveiro et al., 2022CRAVEIRO, C., SOARES, R., CASTRO-NETO, H., SILVA, E.F., SOARES, A., OLIVEIRA, P.G.V., GONZALEZ, E. and PEIXOTO, S., 2022. Ovarian maturation of Penaeus subtilis (Decapoda: Penaeidae): a new insight to describe oocyte development and somatic structures. Acta Zoologica. In press. http://dx.doi.org/10.1111/azo.12433.
http://dx.doi.org/10.1111/azo.12433...
). Contributing to the differentiation of stages into early, advanced and mature maturation, confirmed from the significant difference in the diameter of the oocyte in these different stages. Studies such as Campos et al. (2009)CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12. and Lopes et al. (2017)LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951.
http://dx.doi.org/10.1080/07924259.2017....
, probably did not consider the behavior of follicular cells in their descriptions, which ended up grouping the early and advanced maturation stages into a single stage, the developmental stage.

The immature and spawned stages are similar in relation to their (transparent) coloring, which makes it difficult to observe the gonads through the exoskeleton during the macroscopic classification of the ovaries (Dumont and D’Incao, 2004DUMONT, L.F.C. and D’INCAO, F., 2004. Estágios de desenvolvimento de fêmeas do camarão-barba-ruça (Artemesia longinaris – Decapoda: penaeidae). Iheringia. Série Zoologia, vol. 94, no. 4, pp. 389-393. http://dx.doi.org/10.1590/S0073-47212004000400006.
http://dx.doi.org/10.1590/S0073-47212004...
; Campos et al., 2009CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12.; Lopes et al., 2017LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951.
http://dx.doi.org/10.1080/07924259.2017....
). However, histological analysis helps to differentiate these stages with greater precision due to the visualization being at the cellular level, thus allowing us to observe characteristics such as the presence of atretic oocytes, which is considered one of the main characteristics used to differentiate the immature gonads from the spawned stage (Quintero and Gracia, 1998QUINTERO, M.E. and GRACIA, A., 1998. Stages of gonadal development in the spotted pink shrimp Penaeus brasiliensis. Journal of Crustacean Biology, vol. 18, no. 4, pp. 680-685. http://dx.doi.org/10.2307/1549143.
http://dx.doi.org/10.2307/1549143...
; Peixoto et al., 2003PEIXOTO, S., CAVALLI, R.O., D’INCAO, F., MILACH, A.M. and WASIELESKY, W., 2003. Ovarian maturation of wild Farfantepenaeus paulensis in relation to histological and visual changes. Aquaculture Research, vol. 34, no. 1, pp. 1255-1260. http://dx.doi.org/10.1046/j.1365-2109.2003.00933.x.
http://dx.doi.org/10.1046/j.1365-2109.20...
; Lopes et al., 2017LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951.
http://dx.doi.org/10.1080/07924259.2017....
). Oocytes in atresia are the result of resorption of mature oocytes that were not released during spawning (Peixoto et al., 2005PEIXOTO, S., CAVALLI, R.O. and WASIELESKY, W., 2005. Recent developments on broodstock maturation and reproduction of Farfantepenaeus paulensis. Brazilian Archives of Biology and Technology, vol. 48, no. 6, pp. 997-1006. http://dx.doi.org/10.1590/S1516-89132005000800016.
http://dx.doi.org/10.1590/S1516-89132005...
). Although atretic oocytes were only observed at the spawning stage in the present study, oocyte resorption can also be triggered by environmental impacts, such as pesticide contamination, for example (Rodríguez et al., 2021RODRÍGUEZ, E.M., MEDESANI, D.A., CANOSA, I.S. and AVIGLIANO, L., 2021. The effect of glyphosate on the reproduction of estuarine crabs: Neohelice granulata as a study model. Frontiers in Endocrinology, vol. 12, pp. 643168. http://dx.doi.org/10.3389/fendo.2021.643168. PMid:33841335.
http://dx.doi.org/10.3389/fendo.2021.643...
); and they should only be used as the main classification characteristic when one has full knowledge of the local environmental parameters. In this case, we also used the differentiation of the stages according to the thickness of the gonadal wall, which tends to become thicker, and looser as new reproductive events occur.

Macroscopic analysis is widely used to classify ovarian development in shrimp due to the practicality of differentiating the stages from the color pattern of the gonads (Bolognini et al., 2017BOLOGNINI, L., DONATO, F., LUCCHETTI, A., OLIVOTTO, I., TRUZZI, C., RANDAZZO, B., ANTONUCCI, M., ILLUMINATI, S. and GRATI, F., 2017. A multidisciplinary approach to study the reproductive biology of wild prawns. Scientific Reports, vol. 7, no. 1, pp. 16781. http://dx.doi.org/10.1038/s41598-017-16894-1. PMid:29196667.
http://dx.doi.org/10.1038/s41598-017-168...
; Garcia et al., 2021GARCIA, R.C.P., CRAVEIRO, C.F.F., BERNABÉ, C.V., SILVA, M.A., ARIDE, P.H.R., OLIVEIRA, A.T., GONÇALVES, F.R.S.C., SANTANDER-NETO, J., LAVANDER, H.D. and FAGGIO, C., 2021. Gonadal development of females of the white shrimp Penaeus schmitti (Burkenroad, 1936) caught in southeastern Brazil. Journal of Marine Science and Engineering, vol. 9, no. 653, pp. 1-9. http://dx.doi.org/10.3390/jmse9060653.
http://dx.doi.org/10.3390/jmse9060653...
). However, we found it difficult to differentiate the immature and spawned stages due to the similarity between the colors of the ovaries (translucent) visualized through the exoskeleton. This same difficulty was reported by Campos et al. (2009)CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12. and Lopes et al. (2017)LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951.
http://dx.doi.org/10.1080/07924259.2017....
for X. kroyeri, and also for other penaeid species, such as Artemesia longinaris (Spence Bate, 1888) (Dumont and D'Incao, 2004DUMONT, L.F.C. and D’INCAO, F., 2004. Estágios de desenvolvimento de fêmeas do camarão-barba-ruça (Artemesia longinaris – Decapoda: penaeidae). Iheringia. Série Zoologia, vol. 94, no. 4, pp. 389-393. http://dx.doi.org/10.1590/S0073-47212004000400006.
http://dx.doi.org/10.1590/S0073-47212004...
), Penaeus brasiliensis (Latreille, 1817) (Quintero and Gracia, 1998QUINTERO, M.E. and GRACIA, A., 1998. Stages of gonadal development in the spotted pink shrimp Penaeus brasiliensis. Journal of Crustacean Biology, vol. 18, no. 4, pp. 680-685. http://dx.doi.org/10.2307/1549143.
http://dx.doi.org/10.2307/1549143...
), Penaeus paulensis (Pérez Fartante, 1967) (Peixoto et al., 2003PEIXOTO, S., CAVALLI, R.O., D’INCAO, F., MILACH, A.M. and WASIELESKY, W., 2003. Ovarian maturation of wild Farfantepenaeus paulensis in relation to histological and visual changes. Aquaculture Research, vol. 34, no. 1, pp. 1255-1260. http://dx.doi.org/10.1046/j.1365-2109.2003.00933.x.
http://dx.doi.org/10.1046/j.1365-2109.20...
; 2018PEIXOTO, S., CALAZANS, N., SILVA, E.F., NOLÉ, L., SOARES, R. and FRÉDOU, F.L., 2018. Reproduction cycle and size at first sexual maturity of the white shrimp Penaeus schmitti (Burkenroad, 1936) in northeastern Brazil. Latin American Journal of Aquatic Research, vol. 46, no. 1, pp. 1-9. http://dx.doi.org/10.3856/vol46-issue1-fulltext-1.
http://dx.doi.org/10.3856/vol46-issue1-f...
), Penaeus kerathurus (Forskal, 1775) (Bolognini et al., 2017BOLOGNINI, L., DONATO, F., LUCCHETTI, A., OLIVOTTO, I., TRUZZI, C., RANDAZZO, B., ANTONUCCI, M., ILLUMINATI, S. and GRATI, F., 2017. A multidisciplinary approach to study the reproductive biology of wild prawns. Scientific Reports, vol. 7, no. 1, pp. 16781. http://dx.doi.org/10.1038/s41598-017-16894-1. PMid:29196667.
http://dx.doi.org/10.1038/s41598-017-168...
) and Penaeus schmitti (Craveiro et al., 2019CRAVEIRO, C., PEIXOTO, S., SILVA, E.F., EDUARDO, L.N., LIRA, A.S., CASTRO-NETO, H., FRÉDOU, F. and SOARES, R., 2019. Reproductive dynamics of the white shrimp Litopenaeus schmitti (Burkenroad 1936) in a beach seine fishery in northeastern Brazil. Invertebrate Reproduction & Development, vol. 63, no. 2, pp. 111-121. http://dx.doi.org/10.1080/07924259.2019.1575923.
http://dx.doi.org/10.1080/07924259.2019....
; Garcia et al., 2021GARCIA, R.C.P., CRAVEIRO, C.F.F., BERNABÉ, C.V., SILVA, M.A., ARIDE, P.H.R., OLIVEIRA, A.T., GONÇALVES, F.R.S.C., SANTANDER-NETO, J., LAVANDER, H.D. and FAGGIO, C., 2021. Gonadal development of females of the white shrimp Penaeus schmitti (Burkenroad, 1936) caught in southeastern Brazil. Journal of Marine Science and Engineering, vol. 9, no. 653, pp. 1-9. http://dx.doi.org/10.3390/jmse9060653.
http://dx.doi.org/10.3390/jmse9060653...
).

In this study, the macroscopic analysis proved to be inefficient in differentiating these stages, and with the aim of reducing classification errors, we decided to intensify our histological sampling. Histology was therefore used to confirm or correct the macroscopic pre-classification, resulting in a more detailed and accurate description of the ovarian development stages of the species under study. Therefore, in view of the subjectivity and doubts generated by the macroscopic analysis, we emphasize the need to carry out the macroscopic and microscopic analysis simultaneously, mainly for studies with the purpose of conservation and fisheries management, which need accurate information and that demonstrate the real situation that the stock meets.

Regarding the maturation of oocytes, it was possible to observe a difference in the final stage of development of germinative cells of the species under study. The presence of peripheral bodies (cortical rods) is a very common feature during the final stage of oocyte maturation for different species of penaeids, e.g., P. brasiliensis (Quintero and Gracia, 1998QUINTERO, M.E. and GRACIA, A., 1998. Stages of gonadal development in the spotted pink shrimp Penaeus brasiliensis. Journal of Crustacean Biology, vol. 18, no. 4, pp. 680-685. http://dx.doi.org/10.2307/1549143.
http://dx.doi.org/10.2307/1549143...
), P. paulensis (Peixoto et al., 2003PEIXOTO, S., CAVALLI, R.O., D’INCAO, F., MILACH, A.M. and WASIELESKY, W., 2003. Ovarian maturation of wild Farfantepenaeus paulensis in relation to histological and visual changes. Aquaculture Research, vol. 34, no. 1, pp. 1255-1260. http://dx.doi.org/10.1046/j.1365-2109.2003.00933.x.
http://dx.doi.org/10.1046/j.1365-2109.20...
), P. kerathurus (Bolognini et al., 2017BOLOGNINI, L., DONATO, F., LUCCHETTI, A., OLIVOTTO, I., TRUZZI, C., RANDAZZO, B., ANTONUCCI, M., ILLUMINATI, S. and GRATI, F., 2017. A multidisciplinary approach to study the reproductive biology of wild prawns. Scientific Reports, vol. 7, no. 1, pp. 16781. http://dx.doi.org/10.1038/s41598-017-16894-1. PMid:29196667.
http://dx.doi.org/10.1038/s41598-017-168...
), P. schmitti (Craveiro et al., 2019CRAVEIRO, C., PEIXOTO, S., SILVA, E.F., EDUARDO, L.N., LIRA, A.S., CASTRO-NETO, H., FRÉDOU, F. and SOARES, R., 2019. Reproductive dynamics of the white shrimp Litopenaeus schmitti (Burkenroad 1936) in a beach seine fishery in northeastern Brazil. Invertebrate Reproduction & Development, vol. 63, no. 2, pp. 111-121. http://dx.doi.org/10.1080/07924259.2019.1575923.
http://dx.doi.org/10.1080/07924259.2019....
; Garcia et al., 2021GARCIA, R.C.P., CRAVEIRO, C.F.F., BERNABÉ, C.V., SILVA, M.A., ARIDE, P.H.R., OLIVEIRA, A.T., GONÇALVES, F.R.S.C., SANTANDER-NETO, J., LAVANDER, H.D. and FAGGIO, C., 2021. Gonadal development of females of the white shrimp Penaeus schmitti (Burkenroad, 1936) caught in southeastern Brazil. Journal of Marine Science and Engineering, vol. 9, no. 653, pp. 1-9. http://dx.doi.org/10.3390/jmse9060653.
http://dx.doi.org/10.3390/jmse9060653...
) and X. kroyeri (Campos et al., 2009CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12.; Lopes et al., 2017LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951.
http://dx.doi.org/10.1080/07924259.2017....
). The peripheral bodies are formed after the complete accumulation of vitellogenin in the cell cytoplasm, which indicates the final phase of oocyte maturation; however, in the present study, this characteristic was not found in any of the individuals analyzed, thus diverging from the result found by the authors cited above.

The study by Campos et al. (2009)CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12. mention that previous investigations on ovarian maturation did not report the presence of peripheral bodies in X. kroyeri, and that according to Clark Junior et al. (1980)CLARK JUNIOR, W.H., LYNN, J.W., YUDIN, A.I. and PERSYN, H.O., 1980. Morphology of the cortical reaction in the eggs of Penaeus aztecus. The Biological Bulletin, vol. 158, no. 2, pp. 175-186. http://dx.doi.org/10.2307/1540929.
http://dx.doi.org/10.2307/1540929...
, the absence of this structure may be related to the water temperature. Campos et al. (2009)CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12. and Lopes et al. (2017)LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951.
http://dx.doi.org/10.1080/07924259.2017....
developed their studies in the South and Northeast of Brazil, respectively, regions with different environmental conditions in the Southeast region studied. Santa Catarina is the limit coastal zone for the occurrence of the species X. kroyeri in the south of the country, which is a region characterized by its low temperature waters (Campos et al., 2009CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12.). Low temperatures can slow down gonadal development (Campos et al., 2009CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12.), while higher temperatures can accelerate this process and trigger the spawning of marine invertebrates (Bauer, 1992BAUER, R.T., 1992. Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. Invertebrate Reproduction & Development, vol. 22, no. 1, pp. 193-202. http://dx.doi.org/10.1080/07924259.1992.9672272.
http://dx.doi.org/10.1080/07924259.1992....
).

In Northeastern Brazil, the annual temperature variation is very small, Lopes et al. (2017)LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951.
http://dx.doi.org/10.1080/07924259.2017....
found a variation of only 2 °C between the maximum (28 °C) and minimum values (~26.5 °C) during the period from August 2011 to July 2012, showing that in this region the waters remain warm throughout the year. Different from what was found by Heckler et al. (2013)HECKLER, G.S., SIMÕES, S.M., LOPES, M., ZARA, F.J. and COSTA, R.C., 2013. Biologia populacional e reprodutiva do camarão sete-barbas na Baía de Santos, São Paulo. Boletim do Instituto de Pesca, vol. 39, no. 3, pp. 283-297. http://dx.doi.org/10.20950/1678-2305.2013v39n3p283.
http://dx.doi.org/10.20950/1678-2305.201...
in the Southeast region of the country, where the temperature range was much higher throughout the year (~10 °C between the maximum and minimum values), with a water temperature of approximately 18.5 °C in the spring to a maximum temperature of 28.0 °C in the summer. These same authors reported a significant and positive relationship between water temperature and the abundance of mature females of X. kroyeri. The climatic conditions along the Brazilian coast and the results found in the literature mentioned above indicate that ovarian development may have different characteristics between regions, even when dealing with the same species.

The absence of peripheral bodies in this study hindered the differentiation of the advanced maturation stages and mature stages since this characteristic facilitates the classification of these stages. However, this differentiation was characterized by an increase in the size of yolk granules and their displacement to the cell end, and these characteristics were also observed for the species A. longinaris (Dumont and D’Incao, 2004DUMONT, L.F.C. and D’INCAO, F., 2004. Estágios de desenvolvimento de fêmeas do camarão-barba-ruça (Artemesia longinaris – Decapoda: penaeidae). Iheringia. Série Zoologia, vol. 94, no. 4, pp. 389-393. http://dx.doi.org/10.1590/S0073-47212004000400006.
http://dx.doi.org/10.1590/S0073-47212004...
) due to the absence of cortical rods. Other studies of penaeid shrimps also did not observe the presence of this structure, such as Metapenaeopsis dalei (Rathbun, 1902) (Sakaji et al., 2000SAKAJI, H., TSUCHIYA, K. and SEGAWA, S., 2000. Oocyte development of Metapenaeopsis dalei (Penaeidae, Decapoda, Crustacea). Invertebrate Reproduction & Development, vol. 38, no. 1, pp. 7-12. http://dx.doi.org/10.1080/07924259.2000.9652431.
http://dx.doi.org/10.1080/07924259.2000....
) and Metapenaeus monoceros (Fabricius, 1798) (Abraham and Manisseri, 2012ABRAHAM, J. and MANISSERI, M.K., 2012. Histological and morphological changes associated with ovarian development of speckled shrimp Matapenaeus monoceros (Fabricius, 1798). Indian Journal of Fisheries, vol. 59, no. 1, pp. 119-124.). The absence of peripheral bodies in the present study and in the other studies cited above, allows us to state that this type of structure is not mandatory in the final phase of maturation of penaeid shrimps.

The results presented in this study contribute to a greater understanding of the reproductive aspects of the species X. kroyeri. The detailed classification of the stages of gonadal development was fundamental in order to provide relevant information, which in the future will assist in studies on the population and reproductive dynamics of the species. These studies are considered essential for the development of adequate guidelines for the sustainable management of fishing activity. We suggest that further analyzes be carried out to better investigate the absence of peripheral bodies in the final stage of maturation of X. kroyeri, since this structure seems to be predominant in the species of penaeids captured in Brazil.

5. Conclusion

Five stages of ovarian development were identified for females of the Atlantic Seabob (X. kroyeri) found in southeastern Brazil, which is important since the stages of early and advanced maturation had not been previously described for this species. In addition, no peripheral bodies were found at the final stage of oocyte maturation, which differs from the results found in the literature for the same species in other regions of the country. These results can help us to better understand the reproductive characteristics of the species X. kroyeri and generate important information that serves as a basis for the development of conservation and management measures that ensure the sustainable use of this resource.

Acknowledgements

This study was funded by the Espírito Santo Research and Innovation Foundation and the Espírito Santo State Secretariat for Agriculture, Supply, Aquaculture and Fisheries. Authorization for scientific activity: Ministry of the Environment-MMA, Chico Mendes Institute of Biodiversity Conservation-ICMBio, Authorization and Information System in Biodiversity-SISBIO number: 67056-1 and 67056-2.

References

  • ABRAHAM, J. and MANISSERI, M.K., 2012. Histological and morphological changes associated with ovarian development of speckled shrimp Matapenaeus monoceros (Fabricius, 1798). Indian Journal of Fisheries, vol. 59, no. 1, pp. 119-124.
  • AYUB, Z. and AHMED, M.A., 2002. Description of the ovarian development stages of penaeid shrimp from the coast of Pakistan. Aquaculture Research, vol. 33, no. 1, pp. 767-776. http://dx.doi.org/10.1046/j.1365-2109.2002.00715.x
    » http://dx.doi.org/10.1046/j.1365-2109.2002.00715.x
  • BASILIO, T.H., SILVA, E.V., FIORESI, D.B., GOMES, M.P. and GARCEZ, D.S., 2015. Sustentabilidade das atividades pesqueiras do município de Piúma, Litoral sul do Espírito Santo, Brasil. Arquivos de Ciências do Mar, vol. 48, no. 1, pp. 69-86.
  • BAUER, R.T., 1992. Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. Invertebrate Reproduction & Development, vol. 22, no. 1, pp. 193-202. http://dx.doi.org/10.1080/07924259.1992.9672272
    » http://dx.doi.org/10.1080/07924259.1992.9672272
  • BELL, T.A. and LIGHTNER, D.V., 1988. A handbook of normal penaeid shrimp histology Baton Rouge: World Aquaculture Society, 114 p.
  • BOLOGNINI, L., DONATO, F., LUCCHETTI, A., OLIVOTTO, I., TRUZZI, C., RANDAZZO, B., ANTONUCCI, M., ILLUMINATI, S. and GRATI, F., 2017. A multidisciplinary approach to study the reproductive biology of wild prawns. Scientific Reports, vol. 7, no. 1, pp. 16781. http://dx.doi.org/10.1038/s41598-017-16894-1 PMid:29196667.
    » http://dx.doi.org/10.1038/s41598-017-16894-1
  • BOOS, H., COSTA, R.C., SANTOS, R.A., DIAS NETO, J., RODRIGUES, E.S., RODRIGUES, L.F., D’INCAO, F. and IVO, C.T.C. 2016. Avaliação dos Camarões Peneídeos (Decapoda: Penaeidae). In: M. PINHEIRO and H. BOOS, eds. Livro vermelho dos crustáceos do Brasil: avaliação 2010-2014 Porto Alegre: Sociedade Brasileira de Carcinologia, pp. 300-316.
  • BRANCO, J.O., 2005. Biologia e pesca do camarão sete-barbas Xiphopenaeus kroyeri (Heller) (Crustacea, Penaeidae), na Armação do Itapocoroy, Penha, Santa Catarina, Brasil. Revista Brasileira de Zoologia, vol. 22, no. 4, pp. 1050-1062. http://dx.doi.org/10.1590/S0101-81752005000400034
    » http://dx.doi.org/10.1590/S0101-81752005000400034
  • BRASIL. Ministério da Pesca e Aquicultura – MPA, 2012 [viewed 30 May 2022]. Boletim Estatístico da Pesca e Aquicultura 2011 [online]. Available from: https://www.icmbio.gov.br/cepsul/images/stories/biblioteca/download/estatistica/est_2011_bol__bra.pdf
    » https://www.icmbio.gov.br/cepsul/images/stories/biblioteca/download/estatistica/est_2011_bol__bra.pdf
  • BRASIL 2014 [viewed 15 May 2022]. Instrução normativa nº 03, de setembro de 2014 [online]. Diário Oficial da República Federativa do Brasil, Brasilia. Available from: https://www.icmbio.gov.br/flonatapajos/images/stories/INSTRU%C3%87%C3%83O_NORMATIVA_ICMBio_N%C2%BA_3_DE_2014__com_retifica%C3%A7%C3%A3o_do_DOU18062015.pdf
    » https://www.icmbio.gov.br/flonatapajos/images/stories/INSTRU%C3%87%C3%83O_NORMATIVA_ICMBio_N%C2%BA_3_DE_2014__com_retifica%C3%A7%C3%A3o_do_DOU18062015.pdf
  • CAMPOS, B.R., DUMONT, L.F.C., D’INCAO, F. and BRANCO, J.O., 2009. Ovarian development and length at first maturity of the sea-bob-shrimp Xiphopenaeus kroyeri (Heller) based on histological analysis. Nauplius, vol. 17, no. 1, pp. 9-12.
  • CARVALHO-BATISTA, A., TEROSSI, M., ZARA, F.J., MANTELATTO, F.L. and COSTA, R.C., 2019. A multigene and morphological analysis expands the diversity of the seabod shrimp Xiphopenaeus Smith, 1869 (Decapoda: Penaeidae), with descriptions of two new species. Scientific Reports, vol. 9, pp. 15281. http://dx.doi.org/10.1038/s41598-019-51484-3 PMid:31653885.
    » http://dx.doi.org/10.1038/s41598-019-51484-3
  • CASTILHO, A.L., BAUER, R.T., FREIRE, F.A.M., FRANSOZO, V., COSTA, R.C., GRABOWSKI, R.C. and FRANSOZO, A., 2015. Lifespan and reproductive dynamics of the commercially important Seabob shimp Xiphopenaeus kroyeri (Penaeoidea): synthesis of a 5-year study. Journal of Crustacean Biology, vol. 35, no. 1, pp. 30-40. http://dx.doi.org/10.1163/1937240X-00002300
    » http://dx.doi.org/10.1163/1937240X-00002300
  • CASTILLE, F.L. and LAWRENCE, A.L., 1991. Reproductive studies concerning natural shrimp populations: a description of changes in size and biochemical compositions of the gonads and digestive glands in penaeid shrimps. In: P.F. DE LOACH, W.J. DOUGHERTY and M.A. DAVIDSON, eds. Frontiers of shrimp research Amsterdam: Elsevier, pp. 17-32.
  • CHANG, C.F. and SHIH, T.W., 1995. Productive cycle of ovarian development and vitellogenin profiles in the freshwater prawns, Macrobrachium rosenbergii. Invertebrate Reproduction & Development, vol. 27, no. 1, pp. 11-20. http://dx.doi.org/10.1080/07924259.1995.9672429
    » http://dx.doi.org/10.1080/07924259.1995.9672429
  • CLARK JUNIOR, W.H., LYNN, J.W., YUDIN, A.I. and PERSYN, H.O., 1980. Morphology of the cortical reaction in the eggs of Penaeus aztecus. The Biological Bulletin, vol. 158, no. 2, pp. 175-186. http://dx.doi.org/10.2307/1540929
    » http://dx.doi.org/10.2307/1540929
  • COSTA, R.C., FRANSOZO, A., FREIRE, F.A. and CASTILHO, A.L., 2007. Abundance and Ecological Distribution of the “Sete-Barbas” Shrimp Xiphopenaeus kroyeri (Heller, 1862) (Decapoda: Penaeoidea) in Three Bays of the Ubatuba Region, Southeastern Brazil. Gulf and Caribbean Research, vol. 19, no. 1, pp. 33-41. http://dx.doi.org/10.18785/gcr.1901.04
    » http://dx.doi.org/10.18785/gcr.1901.04
  • COSTA, R.C., FRANSOZO, A., MELO, G.A.S. and MORAIS, F.A., 2003. Chave ilustrada para identificação dos camarões (Dendrobranchiata) do Litoral norte do Estado de São Paulo, Brasil. Biota Neotropica, vol. 3, no. 1, pp. 1-12. http://dx.doi.org/10.1590/S1676-06032003000100011
    » http://dx.doi.org/10.1590/S1676-06032003000100011
  • CRAVEIRO, C., PEIXOTO, S., SILVA, E.F., EDUARDO, L.N., LIRA, A.S., CASTRO-NETO, H., FRÉDOU, F. and SOARES, R., 2019. Reproductive dynamics of the white shrimp Litopenaeus schmitti (Burkenroad 1936) in a beach seine fishery in northeastern Brazil. Invertebrate Reproduction & Development, vol. 63, no. 2, pp. 111-121. http://dx.doi.org/10.1080/07924259.2019.1575923
    » http://dx.doi.org/10.1080/07924259.2019.1575923
  • CRAVEIRO, C., SOARES, R., CASTRO-NETO, H., SILVA, E.F., SOARES, A., OLIVEIRA, P.G.V., GONZALEZ, E. and PEIXOTO, S., 2022. Ovarian maturation of Penaeus subtilis (Decapoda: Penaeidae): a new insight to describe oocyte development and somatic structures. Acta Zoologica In press. http://dx.doi.org/10.1111/azo.12433
    » http://dx.doi.org/10.1111/azo.12433
  • D’INCAO, F., VALENTINI, H. and RODRIGUES, L.F., 2002. Avaliação da pesca de camarões nas regiões sudeste e sul do Brasil. Atlântica, vol. 24, no. 2, pp. 103-116.
  • D’INCAO, F., 1999. Subordem Dendrobranchiata (camarões marinhos). In: L. BUCKUP and G. BOND-BUCKUP, eds. Os crustáceos do Rio Grande do Sul. Porto Alegre: Editora da Universidade Federal do Rio Grande do Sul, pp. 275-299.
  • DALL, W., HILL, B.J., ROTHLISBERG, P.C. and STAPLES, D.J., 1990. The biology of the Penaeidae. In: W. DALL, J. HILL, P. ROTHLISBERG, D.J. SHARPLES and A. SOUTHWARD, eds. Advances in marine biology Cambridge: Academic Press, pp. 283-314.
  • DIAS-NETO, J., 2011. Proposta de plano nacional de gestão para o uso sustentável de camarões marinhos do Brasil Brasília: Ibama, 242 p.
  • DUMONT, L.F.C. and D’INCAO, F., 2004. Estágios de desenvolvimento de fêmeas do camarão-barba-ruça (Artemesia longinaris – Decapoda: penaeidae). Iheringia. Série Zoologia, vol. 94, no. 4, pp. 389-393. http://dx.doi.org/10.1590/S0073-47212004000400006
    » http://dx.doi.org/10.1590/S0073-47212004000400006
  • FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS – FAO, 2022. The state of world fisheries and aquaculture 2022: towards blue transformation. Rome: FAO. http://dx.doi.org/10.4060/cc0461en
    » http://dx.doi.org/10.4060/cc0461en
  • GARCIA, R.C.P., CRAVEIRO, C.F.F., BERNABÉ, C.V., SILVA, M.A., ARIDE, P.H.R., OLIVEIRA, A.T., GONÇALVES, F.R.S.C., SANTANDER-NETO, J., LAVANDER, H.D. and FAGGIO, C., 2021. Gonadal development of females of the white shrimp Penaeus schmitti (Burkenroad, 1936) caught in southeastern Brazil. Journal of Marine Science and Engineering, vol. 9, no. 653, pp. 1-9. http://dx.doi.org/10.3390/jmse9060653
    » http://dx.doi.org/10.3390/jmse9060653
  • HECKLER, G.S., SIMÕES, S.M., LOPES, M., ZARA, F.J. and COSTA, R.C., 2013. Biologia populacional e reprodutiva do camarão sete-barbas na Baía de Santos, São Paulo. Boletim do Instituto de Pesca, vol. 39, no. 3, pp. 283-297. http://dx.doi.org/10.20950/1678-2305.2013v39n3p283
    » http://dx.doi.org/10.20950/1678-2305.2013v39n3p283
  • HIDDINK, J.G., JENNINGS, S., SCIBERRAS, M., SZOSTEK, C.L., HUGHES, K.M., ELLIS, N., RIJNSDORP, A.D., MCCONNAUGHEY, R.A., MAZOR, T., HILBORN, R., COLLIE, J.S., PITCHER, C.R., AMOROSO, R.O., PARMA, A.M., SUURONEN, P., 2017. Global analysis of depletion and recovery of seabed biota after bottom trawling disturbance. Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 31, pp. 8301-8306. http://dx.doi.org/10.1073/pnas.1618858114 PMid:28716926.
    » http://dx.doi.org/10.1073/pnas.1618858114
  • HOSTIM-SILVA, M. and SOARES, G.S.S. 2013. Boletim estatístico da pesca do Espírito Santo - ano 2011: programa de estatística pesqueira do Espírito Santo. São Mateus: Universidade Federal do Espírito Santo, 94 p.
  • JUNQUEIRA, L.C. and JUNQUEIRA, L.M.M.S., 1983. Técnicas básicas de citologia e histologia São Paulo: Livraria e Editora Santos, 123 p.
  • KNOX, W. and TRIGUEIRO, A., 2015. A pesca artesanal no litoral no ES. In: W. KINOX and A. TRIGUEIRO, eds. Saberes, narrativas e conflitos na pesca artesanal Vitória: EDUFES, pp. 17-49.
  • LIÑÁN-CABELLO, M.A., PANIAGUA-MICHEL, J. and HOPKINS, P.M., 2002. Bioactive roles of carotenoids and retinoids in crustaceans. Aquaculture Nutrition, vol. 8, no. 4, pp. 299-309. http://dx.doi.org/10.1046/j.1365-2095.2002.00221.x
    » http://dx.doi.org/10.1046/j.1365-2095.2002.00221.x
  • LOPES, D.F., FRÉDOU, F.L., SILVA, E., CALAZANS, N. and PEIXOTO, S., 2017. Reproductive cycle of seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeidea) from the northeast coast of Brazil. Invertebrate Reproduction & Development, vol. 61, no. 3, pp. 137-141. http://dx.doi.org/10.1080/07924259.2017.1311951
    » http://dx.doi.org/10.1080/07924259.2017.1311951
  • LOPES, D.F.C., SILVA, E.F., PEIXOTO, S.R.M. and FRÉDOU, F.L., 2014. Population biology of seabob-shrimp Xiphopenaeus kroyeri (Heller, 1862) captured on the south coast of Pernambuco state, Northeastern Brazil. Brazilian Journal of Oceanography, vol. 62, no. 4, pp. 331-340. http://dx.doi.org/10.1590/s1679-87592014079706204
    » http://dx.doi.org/10.1590/s1679-87592014079706204
  • MARTINS, A.S., PINHEIRO, H.T. and LEITE-JÚNIOR, N.O., 2013. Biologia Reprodutiva do Camarão Sete-barbas no Litoral Centro Sul e Sul do Espírito Santo, Brasil. Boletim do Instituto de Pesca, vol. 39, no. 3, pp. 205-215. http://dx.doi.org/10.20950/1678-2305.2013v39n3p205
    » http://dx.doi.org/10.20950/1678-2305.2013v39n3p205
  • MEDINA, A., VILA, Y., MOURENTE, G.E. and RODRÍGUEZ, A., 1996. A comparative study of the ovarian development in wild and pond-reared shrimp, Penaeus kerathurus (Förskal, 1775). Aquaculture (Amsterdam, Netherlands), vol. 148, no. 1, pp. 63-75. http://dx.doi.org/10.1016/S0044-8486(96)01408-1
    » http://dx.doi.org/10.1016/S0044-8486(96)01408-1
  • MUSIELLO-FERNANDES, J., ZAPPES, C.A. and HOSTIM-SILVA, M., 2017. Small-scale shrimp fisheries on the Brazilian coast: stakeholders perceptions of the closed season and integrated management. Ocean and Coastal Management, vol. 148, no. 1, pp. 89-96. http://dx.doi.org/10.1016/j.ocecoaman.2017.07.018
    » http://dx.doi.org/10.1016/j.ocecoaman.2017.07.018
  • PALACIOS, E., RODRÍGUEZ-JARAMILLO, C. and RACOTTA, I.S., 1999. Comparison of ovary histology between different-sized wild and pond-reared shrimp Litopenaeus vannamei (Penaeus vannamei). Invertebrate Reproduction & Development, vol. 35, no. 3, pp. 251-259. http://dx.doi.org/10.1080/07924259.1999.9652391
    » http://dx.doi.org/10.1080/07924259.1999.9652391
  • PEIXOTO, S., CALAZANS, N., SILVA, E.F., NOLÉ, L., SOARES, R. and FRÉDOU, F.L., 2018. Reproduction cycle and size at first sexual maturity of the white shrimp Penaeus schmitti (Burkenroad, 1936) in northeastern Brazil. Latin American Journal of Aquatic Research, vol. 46, no. 1, pp. 1-9. http://dx.doi.org/10.3856/vol46-issue1-fulltext-1
    » http://dx.doi.org/10.3856/vol46-issue1-fulltext-1
  • PEIXOTO, S., CAVALLI, R.O. and WASIELESKY, W., 2005. Recent developments on broodstock maturation and reproduction of Farfantepenaeus paulensis. Brazilian Archives of Biology and Technology, vol. 48, no. 6, pp. 997-1006. http://dx.doi.org/10.1590/S1516-89132005000800016
    » http://dx.doi.org/10.1590/S1516-89132005000800016
  • PEIXOTO, S., CAVALLI, R.O., D’INCAO, F., MILACH, A.M. and WASIELESKY, W., 2003. Ovarian maturation of wild Farfantepenaeus paulensis in relation to histological and visual changes. Aquaculture Research, vol. 34, no. 1, pp. 1255-1260. http://dx.doi.org/10.1046/j.1365-2109.2003.00933.x
    » http://dx.doi.org/10.1046/j.1365-2109.2003.00933.x
  • PÉREZ-FARFANTE, I. and KENSLEY, B., 1997. Penaeoid and segestoid shrimps and prawns of the world: keys and diagnoses for the families and genera Paris: Éditions du Muséum National d’Histoire Naturalle, 233 p.
  • PÉREZ-RODA, M.A., GILMAN, E., HUNTINGTON, T., KENNELLY, S.J., SUURONEN, P., CHALOUPKA, M. and MEDLEY, P., 2019. A third assessment of global marine fisheries discards Rome: FAO, 79 p. Fisheries and Aquaculture Technical Paper, no. 633.
  • QUINTERO, M.E. and GRACIA, A., 1998. Stages of gonadal development in the spotted pink shrimp Penaeus brasiliensis. Journal of Crustacean Biology, vol. 18, no. 4, pp. 680-685. http://dx.doi.org/10.2307/1549143
    » http://dx.doi.org/10.2307/1549143
  • RIOS, A.S., SHINOZAKI-MENDES, R.A., SANTANA, J.L. and SOUZA-FILHO, J.F., 2022. Ovarian development of the crab Eriphia gonagra (Fabricius, 1981) (Decapoda: Brachyura: Eriphiidae) in northeastern Brazil. Journal of Crustacean Biology, vol. 42, no. 1, pp. 1-11. http://dx.doi.org/10.1093/jcbiol/ruac040
    » http://dx.doi.org/10.1093/jcbiol/ruac040
  • RODRÍGUEZ, E.M., MEDESANI, D.A., CANOSA, I.S. and AVIGLIANO, L., 2021. The effect of glyphosate on the reproduction of estuarine crabs: Neohelice granulata as a study model. Frontiers in Endocrinology, vol. 12, pp. 643168. http://dx.doi.org/10.3389/fendo.2021.643168 PMid:33841335.
    » http://dx.doi.org/10.3389/fendo.2021.643168
  • SAKAJI, H., TSUCHIYA, K. and SEGAWA, S., 2000. Oocyte development of Metapenaeopsis dalei (Penaeidae, Decapoda, Crustacea). Invertebrate Reproduction & Development, vol. 38, no. 1, pp. 7-12. http://dx.doi.org/10.1080/07924259.2000.9652431
    » http://dx.doi.org/10.1080/07924259.2000.9652431
  • SANTOS, M.C.F. and FREITAS, A.E.T.S., 2006. Caracterização Biológica e Pesqueira do Camarão Sete-barbas, Xiphopenaeus kroyeri (Heller, 1862) (Crustacea, Decapoda, Penaeidae), no Pesqueiro Laminha, Área de Proteção Ambiental de Piaçabuçu (Alagoas – Brasil). Boletim Técnico-Científico do CEPENE, vol. 14, no. 1, pp. 71-91.
  • SIMPSON, A.W. and WATLING, L., 2006. An investigation of the cumulative impacts of shrimp trawling on mud-bottom fishing grounds in the Gulf of Maine: effects on habitat and macrofaunal community structure. ICES Journal of Marine Science, vol. 63, no. 9, pp. 1616-1630. http://dx.doi.org/10.1016/j.icesjms.2006.07.008
    » http://dx.doi.org/10.1016/j.icesjms.2006.07.008
  • SOUZA, T.L., BRAGA, A.A., LÓPEZ-GRECO, L. and NUNES, E.T., 2017. Dynamic of oogenesis in ghost shrimp Callichirus major (Crustacea: Axiidea): a morphofunctional and histochemical study. Acta Histochemica, vol. 119, no. 8, pp. 769-777. http://dx.doi.org/10.1016/j.acthis.2017.09.001 PMid:28988659.
    » http://dx.doi.org/10.1016/j.acthis.2017.09.001
  • TAN-FERMIN, J.D., 1991. Effects of unilateral eyestalk ablation on ovarian histology and oocyte size frequency of wild and pond-reared Penaeus monodon (Fabricius) broodstock. Aquaculture, vol. 93, no. 1, pp. 77-86. http://dx.doi.org/10.1016/0044-8486(91)90206-M
    » http://dx.doi.org/10.1016/0044-8486(91)90206-M
  • VOGT, G., QUINITIO, E.T. and PASCUAL, F.P., 1989. Interaction of the midgut gland and the ovary in vitellogenesis and consequences for the breeding success: a comparison of unablated and ablated spawners of Penaeus monodon In: DE PAUW, J.N., ACKEFORS, H., WILKINS, N.E. eds. Aquaculture: a biotechnology in progress Bredene: European Aquaculture Society, pp. 581-592.
  • WORSMANN, T.U., BARCELOS, S.R. and FERRI, A.C., 1976. Étude histologique de l’ovaire de Penaeus paulensis Pérez-Farfante, 1967. Boletim do Instituto Oceanográfico, vol. 25, no. 1, pp. 43-54. http://dx.doi.org/10.1590/S0373-55241976000100003
    » http://dx.doi.org/10.1590/S0373-55241976000100003

Publication Dates

  • Publication in this collection
    06 Jan 2023
  • Date of issue
    2022

History

  • Received
    15 July 2022
  • Accepted
    07 Dec 2022
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