Acessibilidade / Reportar erro

Analysis of the 90º and 150º angles for increment counting in otoliths of estuarine catfish

Abstract

Fish age can be estimated with the use of age rings in calcified structures, such as otoliths. However, it is important to select an appropriate axis for counting the number of increments and to confirm that the age rings are visible in the otolith and interpreted correctly. In this study, the distance between consecutive age rings in the lapillus otoliths of Cathorops spixii and Genidens genidens catfish from the Cananéia-Iguape Estuarine– Lagoon Complex was measured along otoliths at predetermined 90° and 150° axes. In general, the number of increments observed per otolith ranged from 1 to 14 for both species. The positive linear relationship between the total length of the fish and the radius of the age rings suggests that otolith size is a reliable somatic proxy of C. spixii (=0.872) and G. genidens (=0.896). The axes chosen to measure the distances of each increment were proven accurate, especially the straight axis. Our study indicates that the 90º and 150º angles can be used for increment counting, but caution is required for otoliths with the same growth morphology: potentially confusing increments are more prevalent along the 150º axis, and this may hinder increment analysis of G. genidens and C. spixii. Therefore, the 90º axis provides better visualization of the closest opaque and translucent zones and should be prioritized for increment counting in the C. spixii and G. genidens ariids.

Descriptors:
Cathorops spixii ; Genidens genidens ; Age Rings; Otolith Radius; Biomonitoring

The catfish belonging to the Ariidae family are widely distributed near the coast, in estuaries, inland and marine tropical and temperate waters ( Marceniuk and Menezes, 2007Marceniuk, A. P. & Menezes, N. A. 2007. Systematics of the family Ariidae (Ostariophysi, Siluriformes), with a redefinition of the genera. Zootaxa, 1416(1). DOI: https://doi.org/10.11646/zootaxa.1416.1.1
https://doi.org/10.11646/zootaxa.1416.1....
). Ariids such as Cathorops spixii (Agassiz, 1829) and Genidens genidens (Cuvier, 1829) are distributed throughout the eastern coast of South America, where they are especially abundant in coastal lagoons and estuaries ( Andrade Tubino et al., 2008Andrade Tubino, M. F., Ribeiro, A. L. R. & Vianna, M. 2008. Organização espaço-temporal das ictiocenoses demersais nos ecossistemas estuarinos brasileiros: uma síntese. Oecologia Brasiliensis, 12(4), 640–661.; Schmidt et al., 2008Schmidt, T. C. S., Martins, I. A., Reigada, A. L. D. & Dias, J. F. 2008. Taxocenose de bagres marinhos (Siluriformes, Ariidae) da região estuarina de São Vicente, SP, Brasil. Biota Neotropica, 8(4), 73–81. DOI: https://doi.org/10.1590/s1676-06032008000400006
https://doi.org/10.1590/s1676-0603200800...
; Silva Junior et al., 2013Silva Junior, D. R., Carvalho, D. M. T. & Vianna, M. 2013. The catfish Genidens genidens (Cuvier, 1829) as a potential sentinel species in Brazilian estuarine waters. Journal of Applied Ichthyology, 29(6), 1297–1303. DOI: https://doi.org/10.1111/jai.12280
https://doi.org/10.1111/jai.12280...
). In general, ariids have a benthic feeding habit, thus maintaining an intimate association with the sediment ( Figueiredo and Menezes, 1978Figueiredo, J. L. & Menezes, N. A. 1978. Manual de peixes marinhos do Sudeste do Brasil: Teleostei (1). São Paulo: Museu de Zoologia, Universidade de São Paulo.). Thereby, these species have been considered to be sentinel species, responding to contamination issues in the Brazilian coast, which is under various anthropogenic influences ( Azevedo et al., 2011Azevedo, J. S., Braga, E. S., Favaro, D. T., Perretti, A. R., Rezende, C. E. & Souza, C. M. M. 2011. Total mercury in sediments and in Brazilian Ariidae catfish from two estuaries under different anthropogenic influence. Marine Pollution Bulletin, 62(12), 2724–2731. DOI: https://doi.org/10.1016/j.marpolbul.2011.09.015
https://doi.org/10.1016/j.marpolbul.2011...
, 2013Azevedo, J. S., Braga, E. S., Assis, H. C. S. & Ribeiro, C. A. O. 2013. Biochemical changes in the liver and gill of Cathorops spixii collected seasonally in two Brazilian estuaries under varying influences of anthropogenic activities. Ecotoxicology and Environmental Safety, 96, 220–230. DOI: https://doi.org/10.1016/j.ecoenv. 2013.06.021
https://doi.org/10.1016/j.ecoenv...
), present in environments such as the Santos-São Vicente estuarine system ( Azevedo et al., 2009Azevedo, J. S., Fernandez, W. S., Farias, L. A., Fávaro, D. T. I. & Braga, E. S. 2009. Use of Cathorops spixii as bioindicator of pollution of trace metals in the Santos Bay, Brazil. Ecotoxicology, 18(5), 577–586. DOI: https://doi.org/10.1007/s10646-009-0315-4
https://doi.org/10.1007/s10646-009-0315-...
), one of the most degraded on the southern Brazilian coast, and the Cananéia-Iguape Estuarine Lagoon–Complex - CIELC ( Azevedo et al., 2012Azevedo, J. S., Sarkis, J. E. S., Oliveira, T. A. & Ulrich, J. C. 2012a. Tissue-specific mercury concentrations in two catfish species from the Brazilian coast. Brazilian Journal of Oceanography, 60(2), 209–217. DOI: https://doi.org/10.1590/s1679-87592012000200011
https://doi.org/10.1590/s1679-8759201200...
; Amaral et al., 2021Amaral, T. F., Miyasaki, F. H., Braga, E. S. & Azevedo, J. S. 2021. Temporal and spatial toxicogenetic damage in estuarine catfish Cathorops spixii from a marine protected area with evidence of anthropogenic influences. Science of The Total Environment, 799, 149409. DOI: https://doi.org/10.1016/j.scitotenv.2021.149409
https://doi.org/10.1016/j.scitotenv.2021...
), an aquatic ecosystem subject to minimal anthropogenic influence ( Meniconi, 2012Meniconi, M. F. G. (eds.). 2012. Baía de Guanabara: síntese do conhecimento ambiental. Rio de Janeiro: Petrobras.), but under the influence of human-made materials coming from the Ribeira de Iguape region, located mainly in the northern region of the CIELC ( Schmidt et al., 2008Schmidt, T. C. S., Martins, I. A., Reigada, A. L. D. & Dias, J. F. 2008. Taxocenose de bagres marinhos (Siluriformes, Ariidae) da região estuarina de São Vicente, SP, Brasil. Biota Neotropica, 8(4), 73–81. DOI: https://doi.org/10.1590/s1676-06032008000400006
https://doi.org/10.1590/s1676-0603200800...
; Souza et al., 2012Souza, A. P. R., Braga, E. S. & Bertotti, M. 2012. On site stripping voltammetric determination of Zn(II), Cd(II) and Pb(II) in water samples of the Cananéia-Iguape Estuarine-Lagoon complex in São Paulo state, Brazil. Journal of the Brazilian Chemical Society, 23(7), 1320–1326. DOI: https://doi.org/10.1590/s0103-50532012000700017
https://doi.org/10.1590/s0103-5053201200...
; Mahiques et al., 2013Mahiques, M. M., Figueira, R. C. L., Salaroli, A. B., Alves, D. P. V. & Gonçalves, C. 2013. 150 years of anthropogenic metal input in a Biosphere Reserve: the case study of the Cananéia–Iguape coastal system, Southeastern Brazil. Environmental Earth Sciences, 68(4), 1073–1087. DOI: https://doi.org/10.1007/s12665-012-1809-6
https://doi.org/10.1007/s12665-012-1809-...
; Amaral et al., 2021Amaral, T. F., Miyasaki, F. H., Braga, E. S. & Azevedo, J. S. 2021. Temporal and spatial toxicogenetic damage in estuarine catfish Cathorops spixii from a marine protected area with evidence of anthropogenic influences. Science of The Total Environment, 799, 149409. DOI: https://doi.org/10.1016/j.scitotenv.2021.149409
https://doi.org/10.1016/j.scitotenv.2021...
).

Despite the scarcity of more current data, Mishima and Tanji ( 1981Mishima, M. & Tanji, S. 1981. Distribuição geográfica dos bagres marinhos (Osteichthyes, Ariidae) no Complexo Estuarino Lagunar de Cananéia (25 o s 48 o w). Boletim Do Instituto de Pesca, 8, 157–172. ) considered that C. spixii and G. genidens have a complete life cycle in the CIELC (25°00’28.27S/47°56’01.89W). G. genidens are found in greater number in further northern areas of this system, where there are major continental and anthropic influences, mainly by the Ribeira de Iguape fluvial inputs ( Prado et al., 2019Prado, H. M., Schlindwein, M. N., Murrieta, R. S. S., Júnior, D. R. do N., Souza, E. P. de, Cunha-Lignon, M., Mahiques, M. M. de, Giannini, P. C. F. & Contente, R. F. 2019. The Valo Grande Channel in the Cananéia-Iguape Estuary-Lagoon Complex (SP, Brazil): environmental history, ecology, and future perspectives. Ambiente & Sociedade, 22. DOI: https://doi.org/10.1590/1809-4422asoc0182r2vu19l4td
https://doi.org/10.1590/1809-4422asoc018...
), and where salinity ranges from 0 to 16 ( Barcellos et al., 2005Barcellos, R. L., Berbel, G. B. B., Braga, E. S. & Furtado, V. V. 2005. Distribuição e características do fósforo sedimentar no sistema estuarino lagunar de Cananéia-Iguape, estado de São Paulo, Brasil. Geochimica Brasiliensis, 19(1), 22–36.; Pecoraro et al., 2018Pecoraro, G. D., Hortellani, M. A., Hagiwara, Y. S., Braga, E. S., Sarkis, J. E. & Azevedo, J. S. 2018. Bioaccumulation of Total Mercury (THg) in Catfish (Siluriformes, Ariidae) with Different Sexual Maturity from Cananéia-Iguape Estuary, SP, Brazil. Bulletin of Environmental Contamination and Toxicology, 102(2), 175–179. DOI: https://doi.org/10.1007/s00128-018-2485-3
https://doi.org/10.1007/s00128-018-2485-...
; Amaral et al., 2021Amaral, T. F., Miyasaki, F. H., Braga, E. S. & Azevedo, J. S. 2021. Temporal and spatial toxicogenetic damage in estuarine catfish Cathorops spixii from a marine protected area with evidence of anthropogenic influences. Science of The Total Environment, 799, 149409. DOI: https://doi.org/10.1016/j.scitotenv.2021.149409
https://doi.org/10.1016/j.scitotenv.2021...
). Conversely, C. spixii is distributed throughout the estuary, but more abundantly in its southern region ( Mishima and Tanji, 1981Mishima, M. & Tanji, S. 1981. Distribuição geográfica dos bagres marinhos (Osteichthyes, Ariidae) no Complexo Estuarino Lagunar de Cananéia (25 o s 48 o w). Boletim Do Instituto de Pesca, 8, 157–172. ), where marine influxes are more accentuated ( Chiozzini et al., 2010Chiozzini, V. G., Agostinho, K. L., Delfim, R. & Braga, E. 2010. Tide influence on hydrochemical parameters in two coastal regions of São Paulo (Brazil) under different environmental occupations. In: Safety, Health and Environment World Congress (pp. 25–28). São Paulo: Council of Researches in Education and Sciences.; Aguiar et al., 2013Aguiar, V. M. C., Baptista Neto, J. A. & Braga, E. S. 2013. Nutrient dynamics in a pristine subtropical lagoon-estuarine system. London: Lambert Academic Publishing.). The CIELC is part of the Mosaic of Conservation Units of Lagamar (Cananéia-Iguape-Peruibe Environmental Protection Area), which is recognized as the Biosphere Reserve of the Atlantic Forest since 1992 and considered a Natural Heritage of Humanity since 1999 ( UNESCO, 2011UNESCO (United Nations Educational, Scientific and Cultural Organization). 2011. MAB Biosphere Reserves Directory: biosphere reserve information. Accessed: https://whc.unesco.org/en/list/893
https://whc.unesco.org/en/list/893...
). This mosaic was designated as a Ramsar site in 2017, and has been an international priority area for conservation ever since ( RAMSAR, 2017RAMSAR. 2017. Brazil: environmental protection Area of Cananéia-Iguape-Peruíbe. Gland: Ramsar Information Sheet.). Understanding the ecological and biological aspects, such as age and growth, of sentinel ariids, is very important, since these animals’ responses to damages and injuries, used as contamination biomarkers (ei. Micronuclei, enzymatic changes, pathological responses and metal input and biotransformation - Azevedo et al., 2012Azevedo, J. S., Sarkis, J. E. S., Oliveira, T. A. & Ulrich, J. C. 2012a. Tissue-specific mercury concentrations in two catfish species from the Brazilian coast. Brazilian Journal of Oceanography, 60(2), 209–217. DOI: https://doi.org/10.1590/s1679-87592012000200011
https://doi.org/10.1590/s1679-8759201200...
, 2012Azevedo, J. S., Sarkis, J. E. S., Hortellani, M. A. & Ladle, R. J. 2012b. Are Catfish (Ariidae) Effective Bioindicators for Pb, Cd, Hg, Cu and Zn? Water, Air, & Soil Pollution, 223(7), 3911–3922. DOI: https://doi.org/10.1007/s11270-012-1160-2
https://doi.org/10.1007/s11270-012-1160-...
, 2013Azevedo, J. S., Braga, E. S., Assis, H. C. S. & Ribeiro, C. A. O. 2013. Biochemical changes in the liver and gill of Cathorops spixii collected seasonally in two Brazilian estuaries under varying influences of anthropogenic activities. Ecotoxicology and Environmental Safety, 96, 220–230. DOI: https://doi.org/10.1016/j.ecoenv. 2013.06.021
https://doi.org/10.1016/j.ecoenv...
; Amaral et al., 2021Amaral, T. F., Miyasaki, F. H., Braga, E. S. & Azevedo, J. S. 2021. Temporal and spatial toxicogenetic damage in estuarine catfish Cathorops spixii from a marine protected area with evidence of anthropogenic influences. Science of The Total Environment, 799, 149409. DOI: https://doi.org/10.1016/j.scitotenv.2021.149409
https://doi.org/10.1016/j.scitotenv.2021...
), can be altered by factors such as the animals’ age ( van der Oost et al., 2003van der Oost, R., Beyer, J. & Vermeulen, N. P. E. 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology, 13(2), 57–149. DOI: https://doi.org/10.1016/s1382-6689(02)00126-6
https://doi.org/10.1016/s1382-6689(02)00...
). However, there are few studies on these species in this system ( Denadai et al., 2013Denadai, M., Pombo, M., Santos, F. B., Bessa, E., Ferreira, A. & Turra, A. 2013. Population Dynamics and Diet of the Madamango Sea Catfish Cathorops spixii (Agassiz, 1829) (Siluriformes: Ariidae) in a Tropical Bight in Southeastern Brazil. PLoS ONE, 8(11), e81257. DOI: https://doi.org/10.1371/journal.pone.0081257
https://doi.org/10.1371/journal.pone.008...
; Maciel et al., 2007Maciel, T. R., Vaz-dos-Santos, A. M. & Vianna, M. 2018. Can otoliths of Genidens genidens (Cuvier 1829) (Siluriformes: Ariidae) reveal differences in life strategies of males and females? Environmental Biology of Fishes, 101(11), 1589–1598. DOI: https://doi.org/10.1007/s10641-018-0804-5
https://doi.org/10.1007/s10641-018-0804-...
, 2021Maciel, T. R., Vaz-dos-Santos, A. M., Barradas, J. R. D. S. & Vianna, M. 2019. Sexual dimorphism in the catfish Genidens genidens (Siluriformes: Ariidae) based on otolith morphometry and relative growth. Neotropical Ichthyology, 17(1), e180101. DOI: https://doi.org/10.1590/1982-0224-20180101
https://doi.org/10.1590/1982-0224-201801...
). Bioecological data collected in the CIELC, such as increments in ariids’ calcified structures, are important, as they will enrich the biological database for future and integrated analyses in this area, which has been biomonitored using Cathorops spixii as a contaminator bioindicator since 2004 ( Azevedo et al., 2009Azevedo, J. S., Fernandez, W. S., Farias, L. A., Fávaro, D. T. I. & Braga, E. S. 2009. Use of Cathorops spixii as bioindicator of pollution of trace metals in the Santos Bay, Brazil. Ecotoxicology, 18(5), 577–586. DOI: https://doi.org/10.1007/s10646-009-0315-4
https://doi.org/10.1007/s10646-009-0315-...
, 2012Azevedo, J. S., Sarkis, J. E. S., Oliveira, T. A. & Ulrich, J. C. 2012a. Tissue-specific mercury concentrations in two catfish species from the Brazilian coast. Brazilian Journal of Oceanography, 60(2), 209–217. DOI: https://doi.org/10.1590/s1679-87592012000200011
https://doi.org/10.1590/s1679-8759201200...
, 2012Azevedo, J. S., Sarkis, J. E. S., Hortellani, M. A. & Ladle, R. J. 2012b. Are Catfish (Ariidae) Effective Bioindicators for Pb, Cd, Hg, Cu and Zn? Water, Air, & Soil Pollution, 223(7), 3911–3922. DOI: https://doi.org/10.1007/s11270-012-1160-2
https://doi.org/10.1007/s11270-012-1160-...
, 2013Azevedo, J. S., Braga, E. S., Assis, H. C. S. & Ribeiro, C. A. O. 2013. Biochemical changes in the liver and gill of Cathorops spixii collected seasonally in two Brazilian estuaries under varying influences of anthropogenic activities. Ecotoxicology and Environmental Safety, 96, 220–230. DOI: https://doi.org/10.1016/j.ecoenv. 2013.06.021
https://doi.org/10.1016/j.ecoenv...
, 2019Azevedo, J. S., Vaz-dos-Santos, A. M., Perin, S., Braga, E. S. & Rossi-Wongtschowski, C. L. D. B. 2019. Cathorops spixii (Agassiz 1829) at the Cananéia-Iguape Estuarine system. In: Vaz-dos-Santos, André Martins & Rossi-Wongtschowski, Carmen Lúcia Del Bianco (eds.), Growth in fisheriesresources from the Southwestern Atlantic (pp. 68–70). São Paulo: Instituto Oceanográfico.; Pecoraro et al., 2018Pecoraro, G. D., Hortellani, M. A., Hagiwara, Y. S., Braga, E. S., Sarkis, J. E. & Azevedo, J. S. 2018. Bioaccumulation of Total Mercury (THg) in Catfish (Siluriformes, Ariidae) with Different Sexual Maturity from Cananéia-Iguape Estuary, SP, Brazil. Bulletin of Environmental Contamination and Toxicology, 102(2), 175–179. DOI: https://doi.org/10.1007/s00128-018-2485-3
https://doi.org/10.1007/s00128-018-2485-...
; Amaral et al., 2021Amaral, T. F., Miyasaki, F. H., Braga, E. S. & Azevedo, J. S. 2021. Temporal and spatial toxicogenetic damage in estuarine catfish Cathorops spixii from a marine protected area with evidence of anthropogenic influences. Science of The Total Environment, 799, 149409. DOI: https://doi.org/10.1016/j.scitotenv.2021.149409
https://doi.org/10.1016/j.scitotenv.2021...
; Morais and Azevedo, 2021Morais, I. S. & Azevedo, J. S. 2021. The first report of abnormal age rings in otoliths lapillus of ariids catfish. Boletim Do Instituto de Pesca, 47. DOI: https://doi.org/10.20950/1678-2305/bip.2021.47.e615
https://doi.org/10.20950/1678-2305/bip.2...
). This database will be useful to assist decision-makers in the environmental assessment and conservation of local biodiversity ( Amaral and Jablonski, 2005Amaral, A. C. Z. & Jablonski, S. 2005. Conservação da biodiversidade marinha e costeira no Brasil. Megadiversidade, 1(1), 43–51.).

Age estimation is the basis for calculating growth rate, mortality rate, and productivity ( Campana and Thorrold, 2001Campana, S. E. & Thorrold, S. R. 2001. Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations? Canadian Journal of Fisheries and Aquatic Sciences, 58(1), 30–38. DOI: https://doi.org/10.1139/f00-177
https://doi.org/10.1139/f00-177...
; Mendoza, 2006Mendoza, R. P. R. 2006. Otoliths and Their Applications in Fishery Science. Croatian Journal of Fisheries, 64(3), 89–102.). Fish age can be estimated by counting and interpreting structural patterns that occur in calcified structures such as scales, spines, and otoliths. Otoliths are calcareous structures rich in calcium carbonate (CaCO 3) found in the inner ear (labyrinth) of all teleost fish and responsible for their hearing and balance. These structures grow throughout their lifetimes and act as a permanent life history record. There are three types of otolith structures: sagitta, lapilli, and asteriscus. They differ in their morphology and location in the internal ear of fish ( Popper et al., 2005Popper, A. N., Ramcharitar, J. & Campana, S. E. 2005. Why otoliths? Insights from inner ear physiology and fisheries biology. Marine and Freshwater Research, 56(5), 497–504. DOI: https://doi.org/10.1071/mf04267
https://doi.org/10.1071/mf04267...
).

In fish from the Ostariophysi superorder, such as ariids, the Lapilli otoliths are the most used in age-estimation studies. These structures are larger and more robust than the sagitta otoliths and, therefore, are preferential for growth and age estimation in these taxa ( Assis, 2005Assis, C. A. 2005. The utricular otoliths, lapilli, of teleosts: their morphology and relevance for species identification and systematics studies. Scientia Marina, 69(2), 259–273. DOI: https://doi.org/10.3989/scimar.2005.69n2259
https://doi.org/10.3989/scimar.2005.69n2...
; Santificetur et al., 2017Santificetur, C., Giaretta, M. B., Conversani, V. R. M., Brenha-Nunes, M. R., Siliprandi, C. C. & Rossi-Wongtschowski, C. L. D. B. 2017. Atlas of marine bony fish otoliths of Southeastern-Southern Brazil Part VIII: Siluriformes (Ariidae) and Pleuronectiformes (Achiridae, Paralichthyidae, Cynoglossidae). Brazilian Journal of Oceanography, 65(3), 448–494. DOI: https://doi.org/10.1590/s1679-87592017143106503
https://doi.org/10.1590/s1679-8759201714...
). It has already been observed that, in the lapillus otolith, the narrow opaque zones represent slow growth, while the wide hyaline or translucent zones represent rapid growth. For instance, some researchers have used the lapilli otolith to estimate the age and growth of ariids from different regions, such as Bagre panamensis, from the United States, California ( Maldonado-Coyac et al., 2021Maldonado-Coyac, J. A., Sánchez-Cárdenas, R., Ramírez-Pérez, J. S., Guevara, L. A. S., Valdez-Núñez, K. P., Pérez-Centeno, A. & Maldonado-Amparo, M. D. los A. 2021. Otoliths morphology and age-record in Bagre panamensis (Siluriformes: Ariidae) inhabiting at the southeast of Gulf of California. Latin American Journal of Aquatic Research, 49(3), 404–417. DOI: https://doi.org/10.3856/vol49-issue3-fulltext-2654
https://doi.org/10.3856/vol49-issue3-ful...
), Arius maculatus, from Thailand ( Phaeviset et al., 2021Phaeviset, P., Phomikong, P., Avakul, P., Koolkalaya, S., Kwangkhang, W., Grudpan, C. & Jutagate, T. 2021. Age and growth estimates from three hard parts of the spotted catfish, Arius maculatus (Actinopterygii: Siluriformes: Ariidae), in Songkhla Lake, Thailand’s largest natural lake. Acta Ichthyologica et Piscatoria, 51(4), 371–378. DOI: https://doi.org/10.3897/aiep.51.74082
https://doi.org/10.3897/aiep.51.74082...
), and Plicofollis tenuispinis, Netuma bilineata, Netuma thalassina, and Plicofollis dussumieri, from Kuwaiti waters ( Al-Husaini et al., 2021Al-Husaini, M., Al-Baz, A., Dashti, T., Rajab, S. & Husain, H. 2021. Age, growth, and reproductive parameters of four species of sea catfish (Siluriformes: Ariidae) from Kuwaiti waters. Regional Studies in Marine Science, 46, 101885. DOI: https://doi.org/10.1016/j.rsma.2021.101885
https://doi.org/10.1016/j.rsma.2021.1018...
). In Brazil, some researchers have studied G. genidens and G. barbus ( Reis, 1986Reis, E. G. 1986. Age and growth of the marine catfish, Netuma barba (Siluriformes, Ariidae) in the estuary of the Patos Lagoon (Brazil). Fishery Bulletin, 84(3), 679–686.; Oliveira and Novelli, 2005Oliveira, M. A. & Novelli, R. 2005. Idade e Crescimento do Bagre Genidens Genidens na Barra da Lagoa do Açu, Norte do Estado do Rio de Janeiro. Tropical Oceanography, 33(1), 57–66. DOI: https://doi.org/10.5914/tropocean.v33i1.5070
https://doi.org/10.5914/tropocean.v33i1....
; Gibbs et al., 2013Gibbs, M., Kurth, B. & Bridges, C. 2013. Age and growth of the loricariid catfish Pterygoplichthys disjunctivus in Volusia Blue Spring, Florida. Aquatic Invasions, 8(2), 207–218. DOI: https://doi.org/10.3391/ai.2013.8.2.08
https://doi.org/10.3391/ai.2013.8.2.08...
; Maciel et al., 2007Maciel, T. R., Vaz-dos-Santos, A. M. & Vianna, M. 2018. Can otoliths of Genidens genidens (Cuvier 1829) (Siluriformes: Ariidae) reveal differences in life strategies of males and females? Environmental Biology of Fishes, 101(11), 1589–1598. DOI: https://doi.org/10.1007/s10641-018-0804-5
https://doi.org/10.1007/s10641-018-0804-...
). For the Cathorops spixii species, there is still a scarcity of data on the analysis of the age rings in lapillus otoliths ( Azevedo et al., 2019Azevedo, J. S., Vaz-dos-Santos, A. M., Perin, S., Braga, E. S. & Rossi-Wongtschowski, C. L. D. B. 2019. Cathorops spixii (Agassiz 1829) at the Cananéia-Iguape Estuarine system. In: Vaz-dos-Santos, André Martins & Rossi-Wongtschowski, Carmen Lúcia Del Bianco (eds.), Growth in fisheriesresources from the Southwestern Atlantic (pp. 68–70). São Paulo: Instituto Oceanográfico.).

This report is, therefore, fundamental: it provides descriptions of increments or age rings present in the lapillus otoliths of the Cathorops spixii species, which helps to estimate the age of these animals. For age validation, the first essential step is the selection of an appropriate counting path or axis to assess the number of increments, which is an important component of any age and growth study, and to confirm that the age rings are visible and being interpreted correctly ( Campana and Thorrold, 2001Campana, S. E. & Thorrold, S. R. 2001. Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations? Canadian Journal of Fisheries and Aquatic Sciences, 58(1), 30–38. DOI: https://doi.org/10.1139/f00-177
https://doi.org/10.1139/f00-177...
).

In total, 100 wild C. spixii catfish and 33 G. genidens were collected during the winter periods (August) of 2017 ( C. spixii – n=41; G. genidens – n=07) and 2018 ( C. spixii – n=59; G. genidens – n=26). C. spixii (TL: 13.5-41.6 cm) and G. genidens (TL: 11.1-30.6 cm) were dissected to allow the removal of the lapilli otolith pair from the auditory capsule. The Lapillus is the most robust otolith pair of C. spixii and G. genidens ( Santificetur et al., 2017Santificetur, C., Giaretta, M. B., Conversani, V. R. M., Brenha-Nunes, M. R., Siliprandi, C. C. & Rossi-Wongtschowski, C. L. D. B. 2017. Atlas of marine bony fish otoliths of Southeastern-Southern Brazil Part VIII: Siluriformes (Ariidae) and Pleuronectiformes (Achiridae, Paralichthyidae, Cynoglossidae). Brazilian Journal of Oceanography, 65(3), 448–494. DOI: https://doi.org/10.1590/s1679-87592017143106503
https://doi.org/10.1590/s1679-8759201714...
). Only the left otoliths were processed for rings analysis (observation of opaque and translucent increments) and sectioned transversally, to a cross-section thickness of approximately 3 mm, using a low-speed metallographic saw (Buehler Isomet) ( Morais and Azevedo, 2017Morais, I. S. & Azevedo, J. S. 2017. O uso da microanálise em otólitos de bagres bioindicadores em estudos de biomonitoramentoambiental. Biota Amazônia, 7(2), 65–77., 2021Morais, I. S. & Azevedo, J. S. 2021. The first report of abnormal age rings in otoliths lapillus of ariids catfish. Boletim Do Instituto de Pesca, 47. DOI: https://doi.org/10.20950/1678-2305/bip.2021.47.e615
https://doi.org/10.20950/1678-2305/bip.2...
). The left otoliths were deposited in the collection of the Group of Aquatic Toxicology and Fish Ecophysiology (AquaTox), in the Universidade Federal de São Paulo (UNIFESP), Diadema, Brazil. The sections were then embedded in water and observed under transmitted light using a Zeiss Discovery V20 stereo microscope under 40X magnification and photographed using the AxioVision 4.8 program. There were no significant differences between the otolith measurements of male and female C. spixii from the two regions (northern and southern) of the CIELC (t-test, p>0.05). For this reason, otolith measurements of both sexes were pooled. The distance (mm) between consecutive rings was measured along the otolith at pre-determined 90° and 150° axes ( Figure 1), in order to be compared with the literature ( Cheraghi et al., 2015Cheraghi, S. M., Valinassab, T., Hafezieh, M. & Taghavi. 2015. Morphological characteristics of lapillus and aging of Plicofollis dussumieri (Ruppell, 1837) from Oman Sea. Iranian Journal of Fisheries Sciences, 14(2), 494–502.; Hauser et al., 2018; Maciel et al., 2018; Flinn et al., 2019Flinn, S., Midway, S. & Ostrowski, A. 2019. Age and Growth of Hardhead Catfish and Gafftopsail Catfish in Coastal Louisiana, USA. Marine and Coastal Fisheries, 11(5), 362–371. DOI: https://doi.org/10.1002/mcf2.10089
https://doi.org/10.1002/mcf2.10089...
; Maldonado-Coyac et al., 2021Maldonado-Coyac, J. A., Sánchez-Cárdenas, R., Ramírez-Pérez, J. S., Guevara, L. A. S., Valdez-Núñez, K. P., Pérez-Centeno, A. & Maldonado-Amparo, M. D. los A. 2021. Otoliths morphology and age-record in Bagre panamensis (Siluriformes: Ariidae) inhabiting at the southeast of Gulf of California. Latin American Journal of Aquatic Research, 49(3), 404–417. DOI: https://doi.org/10.3856/vol49-issue3-fulltext-2654
https://doi.org/10.3856/vol49-issue3-ful...
). The validation of the periodicity of formation of the age rings has not been conducted for these catfish species from the CIELC. Therefore, the ring groups were only treated as CaCO 3 increments.

Figure 1.
Cross-section of the left lapillus of Cathorops spixii and Genidens genidens under reflected light. Structures: nucleus (N), translucent zone (H), opaque zone (O), dorsal (D), ventral (V), posterior (P), anterior (A), internal lateral face (Li), and external lateral face (Le) (positions relative to the fish). The dashed line indicates the orientation of the otolith section. The red dots indicate the growth rings and the measured axis.

In total, 100 C. spixii otoliths were analyzed, of which 20 (20%) were discarded because they could not be interpreted. For the same reason, 6 (20%) G. genidens otoliths were discarded, while 27 were analyzed. The maximum number of increments observed per otolith ranged from 1 to 13 (0.17–4.4 mm from the core) for C. spixii and from 1 to 14 (0.30–3.31 mm from the core) for G. genidens ( Table 1). The positive linear relationship between the total length of the fish and the radius of the age rings ( Figure 2) suggests that otolith size is a reliable somatic proxy of C . spixii (R 2=0.872) and G. genidens (R 2=0.896). These results confirm that growth rings are visible in the lapilli otolith of C. spixii and G. genidens from the CIELC, which makes it possible to determine this species’ ages, a fact corroborated by Carvalho et al. ( 2014Carvalho, B. M., Corrêa, M. F. M. & Volpedo, A. 2014. Otólito lapillus de Cathorops spixii (Spix & Agassiz, 1829) e Genidens genidens (Cuvier, 1829) (Actinopterygii - Ariidae). Acta Scientiarum. Biological Sciences, 36(3), 343–347. DOI: https://doi.org/10.4025/actascibiolsci.v36i3.21117
https://doi.org/10.4025/actascibiolsci.v...
), Santificetur et al. ( 2017Santificetur, C., Giaretta, M. B., Conversani, V. R. M., Brenha-Nunes, M. R., Siliprandi, C. C. & Rossi-Wongtschowski, C. L. D. B. 2017. Atlas of marine bony fish otoliths of Southeastern-Southern Brazil Part VIII: Siluriformes (Ariidae) and Pleuronectiformes (Achiridae, Paralichthyidae, Cynoglossidae). Brazilian Journal of Oceanography, 65(3), 448–494. DOI: https://doi.org/10.1590/s1679-87592017143106503
https://doi.org/10.1590/s1679-8759201714...
), Azevedo et al. ( 2019Azevedo, J. S., Vaz-dos-Santos, A. M., Perin, S., Braga, E. S. & Rossi-Wongtschowski, C. L. D. B. 2019. Cathorops spixii (Agassiz 1829) at the Cananéia-Iguape Estuarine system. In: Vaz-dos-Santos, André Martins & Rossi-Wongtschowski, Carmen Lúcia Del Bianco (eds.), Growth in fisheriesresources from the Southwestern Atlantic (pp. 68–70). São Paulo: Instituto Oceanográfico.), Morais and Azevedo ( 2021Morais, I. S. & Azevedo, J. S. 2021. The first report of abnormal age rings in otoliths lapillus of ariids catfish. Boletim Do Instituto de Pesca, 47. DOI: https://doi.org/10.20950/1678-2305/bip.2021.47.e615
https://doi.org/10.20950/1678-2305/bip.2...
). The use of lapilli otoliths for age estimation in other sea catfish species has also been made by Reis ( 1986Reis, E. G. 1986. Age and growth of the marine catfish, Netuma barba (Siluriformes, Ariidae) in the estuary of the Patos Lagoon (Brazil). Fishery Bulletin, 84(3), 679–686.), Cheraghi-Shevi et al. ( 2015Cheraghi, S. M., Valinassab, T., Hafezieh, M. & Taghavi. 2015. Morphological characteristics of lapillus and aging of Plicofollis dussumieri (Ruppell, 1837) from Oman Sea. Iranian Journal of Fisheries Sciences, 14(2), 494–502.), Al-Husaini et al. ( 2021Al-Husaini, M., Al-Baz, A., Dashti, T., Rajab, S. & Husain, H. 2021. Age, growth, and reproductive parameters of four species of sea catfish (Siluriformes: Ariidae) from Kuwaiti waters. Regional Studies in Marine Science, 46, 101885. DOI: https://doi.org/10.1016/j.rsma.2021.101885
https://doi.org/10.1016/j.rsma.2021.1018...
) and Phaeviset et al. ( 2021Phaeviset, P., Phomikong, P., Avakul, P., Koolkalaya, S., Kwangkhang, W., Grudpan, C. & Jutagate, T. 2021. Age and growth estimates from three hard parts of the spotted catfish, Arius maculatus (Actinopterygii: Siluriformes: Ariidae), in Songkhla Lake, Thailand’s largest natural lake. Acta Ichthyologica et Piscatoria, 51(4), 371–378. DOI: https://doi.org/10.3897/aiep.51.74082
https://doi.org/10.3897/aiep.51.74082...
), and Hauser et al. ( 2013Hauser, M., Doria, C. R. C., Melo, L. R. C., Santos, A. R., Ayala, D. M., Nogueira, L. D., Amadio, S., Fabré, N., Torrente-Vilara, G., García-Vásquez, Á., Renno, J.-F., Carvajal-Vallejos, F. M., Alonso, J. C., Nuñez, J. & Duponchelle, F. 2018. Age and growth of the Amazonian migratory catfish Brachyplatystoma rousseauxii in the Madeira River basin before the construction of dams. Neotropical Ichthyology, 16(1). DOI: https://doi.org/10.1590/1982-0224-20170130
https://doi.org/10.1590/1982-0224-201701...
) applied this method to freshwater catfishes.

Table 1.
Summary of descriptive statistics of the average radius (mm) of otolith increments in Cathorops spixii and Genidens genidens from the CIELC, Brazil. Rn: number of rings (Mean ± SD, standard deviation) of otolith increments for 90º and 150º axes.

As observed in other studies, the axes chosen to carry out the measurements of the distances between increments proved to be accurate (especially the straight axis) ( Cheraghi et al., 2015Cheraghi, S. M., Valinassab, T., Hafezieh, M. & Taghavi. 2015. Morphological characteristics of lapillus and aging of Plicofollis dussumieri (Ruppell, 1837) from Oman Sea. Iranian Journal of Fisheries Sciences, 14(2), 494–502.; Hauser et al., 2013Hauser, M., Doria, C. R. C., Melo, L. R. C., Santos, A. R., Ayala, D. M., Nogueira, L. D., Amadio, S., Fabré, N., Torrente-Vilara, G., García-Vásquez, Á., Renno, J.-F., Carvajal-Vallejos, F. M., Alonso, J. C., Nuñez, J. & Duponchelle, F. 2018. Age and growth of the Amazonian migratory catfish Brachyplatystoma rousseauxii in the Madeira River basin before the construction of dams. Neotropical Ichthyology, 16(1). DOI: https://doi.org/10.1590/1982-0224-20170130
https://doi.org/10.1590/1982-0224-201701...
; Maldonado-Coyac et al., 2021Maldonado-Coyac, J. A., Sánchez-Cárdenas, R., Ramírez-Pérez, J. S., Guevara, L. A. S., Valdez-Núñez, K. P., Pérez-Centeno, A. & Maldonado-Amparo, M. D. los A. 2021. Otoliths morphology and age-record in Bagre panamensis (Siluriformes: Ariidae) inhabiting at the southeast of Gulf of California. Latin American Journal of Aquatic Research, 49(3), 404–417. DOI: https://doi.org/10.3856/vol49-issue3-fulltext-2654
https://doi.org/10.3856/vol49-issue3-ful...
) and were, therefore, used in this study. Hauser et al. ( 2013Hauser, M., Doria, C. R. C., Melo, L. R. C., Santos, A. R., Ayala, D. M., Nogueira, L. D., Amadio, S., Fabré, N., Torrente-Vilara, G., García-Vásquez, Á., Renno, J.-F., Carvajal-Vallejos, F. M., Alonso, J. C., Nuñez, J. & Duponchelle, F. 2018. Age and growth of the Amazonian migratory catfish Brachyplatystoma rousseauxii in the Madeira River basin before the construction of dams. Neotropical Ichthyology, 16(1). DOI: https://doi.org/10.1590/1982-0224-20170130
https://doi.org/10.1590/1982-0224-201701...
) and Maldonado-Coyac et al. ( 2021Maldonado-Coyac, J. A., Sánchez-Cárdenas, R., Ramírez-Pérez, J. S., Guevara, L. A. S., Valdez-Núñez, K. P., Pérez-Centeno, A. & Maldonado-Amparo, M. D. los A. 2021. Otoliths morphology and age-record in Bagre panamensis (Siluriformes: Ariidae) inhabiting at the southeast of Gulf of California. Latin American Journal of Aquatic Research, 49(3), 404–417. DOI: https://doi.org/10.3856/vol49-issue3-fulltext-2654
https://doi.org/10.3856/vol49-issue3-ful...
) reported similar types of rings in lapillus otoliths of the Brachplatystoma rousseuxii, a freshwater catfish from the Orinoco River, and the Bagre panamensis, a freshwater catfish from the southeast of the Gulf of California. Hauser et al. ( 2013Hauser, M., Doria, C. R. C., Melo, L. R. C., Santos, A. R., Ayala, D. M., Nogueira, L. D., Amadio, S., Fabré, N., Torrente-Vilara, G., García-Vásquez, Á., Renno, J.-F., Carvajal-Vallejos, F. M., Alonso, J. C., Nuñez, J. & Duponchelle, F. 2018. Age and growth of the Amazonian migratory catfish Brachyplatystoma rousseauxii in the Madeira River basin before the construction of dams. Neotropical Ichthyology, 16(1). DOI: https://doi.org/10.1590/1982-0224-20170130
https://doi.org/10.1590/1982-0224-201701...
) reported that the stress caused by the increased salinity in the Orinoco River during August and September, competition for food and long periods of starvation were critical factors in the formation of ring anomalies. Regarding C. spixii collected in the same area of our study (the CIELC), Morais and Azevedo ( 2021Morais, I. S. & Azevedo, J. S. 2021. The first report of abnormal age rings in otoliths lapillus of ariids catfish. Boletim Do Instituto de Pesca, 47. DOI: https://doi.org/10.20950/1678-2305/bip.2021.47.e615
https://doi.org/10.20950/1678-2305/bip.2...
) have reported anomalies in the age rings of lapillus otoliths of C. spixii, indicating a possible relationship between these anomalies and environmental stressors, such as increased salinity, in the Cananéia-Iguape estuarine region. Although this has not been tested on the ariids from the CIELC, previous evidence does link salinity stress to anomalies on age rings ( Hauser et al., 2013Hauser, M., Doria, C. R. C., Melo, L. R. C., Santos, A. R., Ayala, D. M., Nogueira, L. D., Amadio, S., Fabré, N., Torrente-Vilara, G., García-Vásquez, Á., Renno, J.-F., Carvajal-Vallejos, F. M., Alonso, J. C., Nuñez, J. & Duponchelle, F. 2018. Age and growth of the Amazonian migratory catfish Brachyplatystoma rousseauxii in the Madeira River basin before the construction of dams. Neotropical Ichthyology, 16(1). DOI: https://doi.org/10.1590/1982-0224-20170130
https://doi.org/10.1590/1982-0224-201701...
). Given the particular results of our study and its notable differences from previous studies, it is important to recommend cross-sectioning for age estimation, which helps reduce errors, since our study and its methods are more suitable for age estimation in C. spixii. Maciel et al. ( 2007Maciel, T. R., Vaz-dos-Santos, A. M. & Vianna, M. 2018. Can otoliths of Genidens genidens (Cuvier 1829) (Siluriformes: Ariidae) reveal differences in life strategies of males and females? Environmental Biology of Fishes, 101(11), 1589–1598. DOI: https://doi.org/10.1007/s10641-018-0804-5
https://doi.org/10.1007/s10641-018-0804-...
) suggest the same for the G. genidens species.

Increment counting in otoliths does not have to be performed along a straight line —it can be useful to change the count axis ( Campana and Thorrold, 2001Campana, S. E. & Thorrold, S. R. 2001. Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations? Canadian Journal of Fisheries and Aquatic Sciences, 58(1), 30–38. DOI: https://doi.org/10.1139/f00-177
https://doi.org/10.1139/f00-177...
). Our study suggests that the 90º and 150º angles can be used for increment counting, but caution is necessary for otoliths with the same growth morphology, since potentially confusing increments are more prevalent along the 150º axis, which may hinder increment analysis in G. genidens and C. spixii. Moreover, the same pattern of distance between otoliths in C. spixii and G. genidens that contain more than eight increments or age rings increases the difficulty in visualizing them, due to the approximation of the opaque and translucent zones. This can lead to underestimation in the age ring count. Therefore, we suggest using the 90-degree axis when evaluating these ariid species.

Figure 2.
Scatterplots correlating otolith variables. A - B: correlation between the total length of the fish and the radius of the rings. C – F: correlation between ring radius (mean with SD) of lapillus of Cathorops spixii (yellow color) and Genidens genidens (blue color) from the Cananéia-Iguape Estuarine-Lagoon Complex.

Despite not being validated in this study, the periodicity of age ring formation in C. spixii and G. genidens from the CIELC, along with previous studies on age and growth in ariid catfish, indicate that one age ring is formed per year following the reproductive cycle ( Mishima and Tanji, 1981Mishima, M. & Tanji, S. 1981. Distribuição geográfica dos bagres marinhos (Osteichthyes, Ariidae) no Complexo Estuarino Lagunar de Cananéia (25 o s 48 o w). Boletim Do Instituto de Pesca, 8, 157–172. ; Gomes and Araújo, 2004Gomes, I. D. & Araújo, F. G. 2004. Reproductive biology of two marine catfishes (Siluriformes, Ariidae) in the Sepetiba Bay. Revista de Biologia Tropical, 52(1), 143–156.; Oliveira and Novelli, 2005Oliveira, M. A. & Novelli, R. 2005. Idade e Crescimento do Bagre Genidens Genidens na Barra da Lagoa do Açu, Norte do Estado do Rio de Janeiro. Tropical Oceanography, 33(1), 57–66. DOI: https://doi.org/10.5914/tropocean.v33i1.5070
https://doi.org/10.5914/tropocean.v33i1....
). Conversely, Maciel et al. ( 2007Maciel, T. R., Vaz-dos-Santos, A. M. & Vianna, M. 2018. Can otoliths of Genidens genidens (Cuvier 1829) (Siluriformes: Ariidae) reveal differences in life strategies of males and females? Environmental Biology of Fishes, 101(11), 1589–1598. DOI: https://doi.org/10.1007/s10641-018-0804-5
https://doi.org/10.1007/s10641-018-0804-...
) reported the formation of two rings per year in the lapillus otoliths of G. genidens from the Guanabara Bay (Rio de Janeiro, Brazil), which is related to the species’ reproductive cycle and period of lower metabolism due to cooler water temperatures. This reinforces the importance of carrying an analysis of the periodicity of the rings in the two species from the CIELC, since this area has fluctuating environmental conditions due to continental input in the northern portion and marine flow in the southern portion ( Chiozzini et al., 2010Chiozzini, V. G., Agostinho, K. L., Delfim, R. & Braga, E. 2010. Tide influence on hydrochemical parameters in two coastal regions of São Paulo (Brazil) under different environmental occupations. In: Safety, Health and Environment World Congress (pp. 25–28). São Paulo: Council of Researches in Education and Sciences.; Azevedo and Braga, 2011Azevedo, J. S. & Braga, E. S. 2011. Caracterização hidroquímica para qualificação ambiental dos estuários de Santos-São Vicente e Cananéia. Arquivos de Ciências Do Mar, 44(2), 52–61.; Azevedo et al., 2013Azevedo, J. S., Braga, E. S., Assis, H. C. S. & Ribeiro, C. A. O. 2013. Biochemical changes in the liver and gill of Cathorops spixii collected seasonally in two Brazilian estuaries under varying influences of anthropogenic activities. Ecotoxicology and Environmental Safety, 96, 220–230. DOI: https://doi.org/10.1016/j.ecoenv. 2013.06.021
https://doi.org/10.1016/j.ecoenv...
; Amaral et al., 2021Amaral, T. F., Miyasaki, F. H., Braga, E. S. & Azevedo, J. S. 2021. Temporal and spatial toxicogenetic damage in estuarine catfish Cathorops spixii from a marine protected area with evidence of anthropogenic influences. Science of The Total Environment, 799, 149409. DOI: https://doi.org/10.1016/j.scitotenv.2021.149409
https://doi.org/10.1016/j.scitotenv.2021...
), which can lead to the formation of abnormal age rings.

During the interpretation of the otolith increments in C. spixii and G. genidens, some difficulties were encountered: 1- the lesser thickness of the increments in the 7-8 ring made measurements difficult and even impossible in some otoliths, which may increase the variance of measurements in these rings; 2- the reading of the first ring was particularly difficult due to the opacity in the initial phase of otolith growth (Maciel et al. ( 2007Maciel, T. R., Vaz-dos-Santos, A. M. & Vianna, M. 2018. Can otoliths of Genidens genidens (Cuvier 1829) (Siluriformes: Ariidae) reveal differences in life strategies of males and females? Environmental Biology of Fishes, 101(11), 1589–1598. DOI: https://doi.org/10.1007/s10641-018-0804-5
https://doi.org/10.1007/s10641-018-0804-...
) also state that accurately verifying the approximation of the rings may be difficult in otoliths with more than 10 increments); 3- a 90º angle is better for visualization and counting in species such as G. genidens, due to the lower variation and opacity of their increments.

ACKNOWLEDGMENT

The authors would like to thank the reviewers for their comments and suggestions that were useful to improve this study.

REFERENCES

  • Aguiar, V. M. C., Baptista Neto, J. A. & Braga, E. S. 2013. Nutrient dynamics in a pristine subtropical lagoon-estuarine system. London: Lambert Academic Publishing.
  • Al-Husaini, M., Al-Baz, A., Dashti, T., Rajab, S. & Husain, H. 2021. Age, growth, and reproductive parameters of four species of sea catfish (Siluriformes: Ariidae) from Kuwaiti waters. Regional Studies in Marine Science, 46, 101885. DOI: https://doi.org/10.1016/j.rsma.2021.101885
    » https://doi.org/10.1016/j.rsma.2021.101885
  • Amaral, A. C. Z. & Jablonski, S. 2005. Conservação da biodiversidade marinha e costeira no Brasil. Megadiversidade, 1(1), 43–51.
  • Amaral, T. F., Miyasaki, F. H., Braga, E. S. & Azevedo, J. S. 2021. Temporal and spatial toxicogenetic damage in estuarine catfish Cathorops spixii from a marine protected area with evidence of anthropogenic influences. Science of The Total Environment, 799, 149409. DOI: https://doi.org/10.1016/j.scitotenv.2021.149409
    » https://doi.org/10.1016/j.scitotenv.2021.149409
  • Andrade Tubino, M. F., Ribeiro, A. L. R. & Vianna, M. 2008. Organização espaço-temporal das ictiocenoses demersais nos ecossistemas estuarinos brasileiros: uma síntese. Oecologia Brasiliensis, 12(4), 640–661.
  • Assis, C. A. 2005. The utricular otoliths, lapilli, of teleosts: their morphology and relevance for species identification and systematics studies. Scientia Marina, 69(2), 259–273. DOI: https://doi.org/10.3989/scimar.2005.69n2259
    » https://doi.org/10.3989/scimar.2005.69n2259
  • Azevedo, J. S. & Braga, E. S. 2011. Caracterização hidroquímica para qualificação ambiental dos estuários de Santos-São Vicente e Cananéia. Arquivos de Ciências Do Mar, 44(2), 52–61.
  • Azevedo, J. S., Sarkis, J. E. S., Oliveira, T. A. & Ulrich, J. C. 2012a. Tissue-specific mercury concentrations in two catfish species from the Brazilian coast. Brazilian Journal of Oceanography, 60(2), 209–217. DOI: https://doi.org/10.1590/s1679-87592012000200011
    » https://doi.org/10.1590/s1679-87592012000200011
  • Azevedo, J. S., Sarkis, J. E. S., Hortellani, M. A. & Ladle, R. J. 2012b. Are Catfish (Ariidae) Effective Bioindicators for Pb, Cd, Hg, Cu and Zn? Water, Air, & Soil Pollution, 223(7), 3911–3922. DOI: https://doi.org/10.1007/s11270-012-1160-2
    » https://doi.org/10.1007/s11270-012-1160-2
  • Azevedo, J. S., Braga, E. S., Assis, H. C. S. & Ribeiro, C. A. O. 2013. Biochemical changes in the liver and gill of Cathorops spixii collected seasonally in two Brazilian estuaries under varying influences of anthropogenic activities. Ecotoxicology and Environmental Safety, 96, 220–230. DOI: https://doi.org/10.1016/j.ecoenv 2013.06.021
    » https://doi.org/10.1016/j.ecoenv.2013.06.021
  • Azevedo, J. S., Braga, E. S., Favaro, D. T., Perretti, A. R., Rezende, C. E. & Souza, C. M. M. 2011. Total mercury in sediments and in Brazilian Ariidae catfish from two estuaries under different anthropogenic influence. Marine Pollution Bulletin, 62(12), 2724–2731. DOI: https://doi.org/10.1016/j.marpolbul.2011.09.015
    » https://doi.org/10.1016/j.marpolbul.2011.09.015
  • Azevedo, J. S., Fernandez, W. S., Farias, L. A., Fávaro, D. T. I. & Braga, E. S. 2009. Use of Cathorops spixii as bioindicator of pollution of trace metals in the Santos Bay, Brazil. Ecotoxicology, 18(5), 577–586. DOI: https://doi.org/10.1007/s10646-009-0315-4
    » https://doi.org/10.1007/s10646-009-0315-4
  • Azevedo, J. S., Vaz-dos-Santos, A. M., Perin, S., Braga, E. S. & Rossi-Wongtschowski, C. L. D. B. 2019. Cathorops spixii (Agassiz 1829) at the Cananéia-Iguape Estuarine system. In: Vaz-dos-Santos, André Martins & Rossi-Wongtschowski, Carmen Lúcia Del Bianco (eds.), Growth in fisheriesresources from the Southwestern Atlantic (pp. 68–70). São Paulo: Instituto Oceanográfico.
  • Barcellos, R. L., Berbel, G. B. B., Braga, E. S. & Furtado, V. V. 2005. Distribuição e características do fósforo sedimentar no sistema estuarino lagunar de Cananéia-Iguape, estado de São Paulo, Brasil. Geochimica Brasiliensis, 19(1), 22–36.
  • Campana, S. E. & Thorrold, S. R. 2001. Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations? Canadian Journal of Fisheries and Aquatic Sciences, 58(1), 30–38. DOI: https://doi.org/10.1139/f00-177
    » https://doi.org/10.1139/f00-177
  • Carvalho, B. M., Corrêa, M. F. M. & Volpedo, A. 2014. Otólito lapillus de Cathorops spixii (Spix & Agassiz, 1829) e Genidens genidens (Cuvier, 1829) (Actinopterygii - Ariidae). Acta Scientiarum. Biological Sciences, 36(3), 343–347. DOI: https://doi.org/10.4025/actascibiolsci.v36i3.21117
    » https://doi.org/10.4025/actascibiolsci.v36i3.21117
  • Cheraghi, S. M., Valinassab, T., Hafezieh, M. & Taghavi. 2015. Morphological characteristics of lapillus and aging of Plicofollis dussumieri (Ruppell, 1837) from Oman Sea. Iranian Journal of Fisheries Sciences, 14(2), 494–502.
  • Chiozzini, V. G., Agostinho, K. L., Delfim, R. & Braga, E. 2010. Tide influence on hydrochemical parameters in two coastal regions of São Paulo (Brazil) under different environmental occupations. In: Safety, Health and Environment World Congress (pp. 25–28). São Paulo: Council of Researches in Education and Sciences.
  • Denadai, M., Pombo, M., Santos, F. B., Bessa, E., Ferreira, A. & Turra, A. 2013. Population Dynamics and Diet of the Madamango Sea Catfish Cathorops spixii (Agassiz, 1829) (Siluriformes: Ariidae) in a Tropical Bight in Southeastern Brazil. PLoS ONE, 8(11), e81257. DOI: https://doi.org/10.1371/journal.pone.0081257
    » https://doi.org/10.1371/journal.pone.0081257
  • Figueiredo, J. L. & Menezes, N. A. 1978. Manual de peixes marinhos do Sudeste do Brasil: Teleostei (1). São Paulo: Museu de Zoologia, Universidade de São Paulo.
  • Flinn, S., Midway, S. & Ostrowski, A. 2019. Age and Growth of Hardhead Catfish and Gafftopsail Catfish in Coastal Louisiana, USA. Marine and Coastal Fisheries, 11(5), 362–371. DOI: https://doi.org/10.1002/mcf2.10089
    » https://doi.org/10.1002/mcf2.10089
  • Gibbs, M., Kurth, B. & Bridges, C. 2013. Age and growth of the loricariid catfish Pterygoplichthys disjunctivus in Volusia Blue Spring, Florida. Aquatic Invasions, 8(2), 207–218. DOI: https://doi.org/10.3391/ai.2013.8.2.08
    » https://doi.org/10.3391/ai.2013.8.2.08
  • Gomes, I. D. & Araújo, F. G. 2004. Reproductive biology of two marine catfishes (Siluriformes, Ariidae) in the Sepetiba Bay. Revista de Biologia Tropical, 52(1), 143–156.
  • Hauser, M., Doria, C. R. C., Melo, L. R. C., Santos, A. R., Ayala, D. M., Nogueira, L. D., Amadio, S., Fabré, N., Torrente-Vilara, G., García-Vásquez, Á., Renno, J.-F., Carvajal-Vallejos, F. M., Alonso, J. C., Nuñez, J. & Duponchelle, F. 2018. Age and growth of the Amazonian migratory catfish Brachyplatystoma rousseauxii in the Madeira River basin before the construction of dams. Neotropical Ichthyology, 16(1). DOI: https://doi.org/10.1590/1982-0224-20170130
    » https://doi.org/10.1590/1982-0224-20170130
  • Maciel, T. R., Vaz-dos-Santos, A. M., Barradas, J. R. D. S. & Vianna, M. 2019. Sexual dimorphism in the catfish Genidens genidens (Siluriformes: Ariidae) based on otolith morphometry and relative growth. Neotropical Ichthyology, 17(1), e180101. DOI: https://doi.org/10.1590/1982-0224-20180101
    » https://doi.org/10.1590/1982-0224-20180101
  • Maciel, T. R., Vaz-dos-Santos, A. M. & Vianna, M. 2018. Can otoliths of Genidens genidens (Cuvier 1829) (Siluriformes: Ariidae) reveal differences in life strategies of males and females? Environmental Biology of Fishes, 101(11), 1589–1598. DOI: https://doi.org/10.1007/s10641-018-0804-5
    » https://doi.org/10.1007/s10641-018-0804-5
  • Mahiques, M. M., Figueira, R. C. L., Salaroli, A. B., Alves, D. P. V. & Gonçalves, C. 2013. 150 years of anthropogenic metal input in a Biosphere Reserve: the case study of the Cananéia–Iguape coastal system, Southeastern Brazil. Environmental Earth Sciences, 68(4), 1073–1087. DOI: https://doi.org/10.1007/s12665-012-1809-6
    » https://doi.org/10.1007/s12665-012-1809-6
  • Maldonado-Coyac, J. A., Sánchez-Cárdenas, R., Ramírez-Pérez, J. S., Guevara, L. A. S., Valdez-Núñez, K. P., Pérez-Centeno, A. & Maldonado-Amparo, M. D. los A. 2021. Otoliths morphology and age-record in Bagre panamensis (Siluriformes: Ariidae) inhabiting at the southeast of Gulf of California. Latin American Journal of Aquatic Research, 49(3), 404–417. DOI: https://doi.org/10.3856/vol49-issue3-fulltext-2654
    » https://doi.org/10.3856/vol49-issue3-fulltext-2654
  • Marceniuk, A. P. & Menezes, N. A. 2007. Systematics of the family Ariidae (Ostariophysi, Siluriformes), with a redefinition of the genera. Zootaxa, 1416(1). DOI: https://doi.org/10.11646/zootaxa.1416.1.1
    » https://doi.org/10.11646/zootaxa.1416.1.1
  • Mendoza, R. P. R. 2006. Otoliths and Their Applications in Fishery Science. Croatian Journal of Fisheries, 64(3), 89–102.
  • Meniconi, M. F. G. (eds.). 2012. Baía de Guanabara: síntese do conhecimento ambiental. Rio de Janeiro: Petrobras.
  • Mishima, M. & Tanji, S. 1981. Distribuição geográfica dos bagres marinhos (Osteichthyes, Ariidae) no Complexo Estuarino Lagunar de Cananéia (25 o s 48 o w). Boletim Do Instituto de Pesca, 8, 157–172.
  • Morais, I. S. & Azevedo, J. S. 2017. O uso da microanálise em otólitos de bagres bioindicadores em estudos de biomonitoramentoambiental. Biota Amazônia, 7(2), 65–77.
  • Morais, I. S. & Azevedo, J. S. 2021. The first report of abnormal age rings in otoliths lapillus of ariids catfish. Boletim Do Instituto de Pesca, 47. DOI: https://doi.org/10.20950/1678-2305/bip.2021.47.e615
    » https://doi.org/10.20950/1678-2305/bip.2021.47.e615
  • Oliveira, M. A. & Novelli, R. 2005. Idade e Crescimento do Bagre Genidens Genidens na Barra da Lagoa do Açu, Norte do Estado do Rio de Janeiro. Tropical Oceanography, 33(1), 57–66. DOI: https://doi.org/10.5914/tropocean.v33i1.5070
    » https://doi.org/10.5914/tropocean.v33i1.5070
  • van der Oost, R., Beyer, J. & Vermeulen, N. P. E. 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology, 13(2), 57–149. DOI: https://doi.org/10.1016/s1382-6689(02)00126-6
    » https://doi.org/10.1016/s1382-6689(02)00126-6
  • Pecoraro, G. D., Hortellani, M. A., Hagiwara, Y. S., Braga, E. S., Sarkis, J. E. & Azevedo, J. S. 2018. Bioaccumulation of Total Mercury (THg) in Catfish (Siluriformes, Ariidae) with Different Sexual Maturity from Cananéia-Iguape Estuary, SP, Brazil. Bulletin of Environmental Contamination and Toxicology, 102(2), 175–179. DOI: https://doi.org/10.1007/s00128-018-2485-3
    » https://doi.org/10.1007/s00128-018-2485-3
  • Phaeviset, P., Phomikong, P., Avakul, P., Koolkalaya, S., Kwangkhang, W., Grudpan, C. & Jutagate, T. 2021. Age and growth estimates from three hard parts of the spotted catfish, Arius maculatus (Actinopterygii: Siluriformes: Ariidae), in Songkhla Lake, Thailand’s largest natural lake. Acta Ichthyologica et Piscatoria, 51(4), 371–378. DOI: https://doi.org/10.3897/aiep.51.74082
    » https://doi.org/10.3897/aiep.51.74082
  • Popper, A. N., Ramcharitar, J. & Campana, S. E. 2005. Why otoliths? Insights from inner ear physiology and fisheries biology. Marine and Freshwater Research, 56(5), 497–504. DOI: https://doi.org/10.1071/mf04267
    » https://doi.org/10.1071/mf04267
  • Prado, H. M., Schlindwein, M. N., Murrieta, R. S. S., Júnior, D. R. do N., Souza, E. P. de, Cunha-Lignon, M., Mahiques, M. M. de, Giannini, P. C. F. & Contente, R. F. 2019. The Valo Grande Channel in the Cananéia-Iguape Estuary-Lagoon Complex (SP, Brazil): environmental history, ecology, and future perspectives. Ambiente & Sociedade, 22. DOI: https://doi.org/10.1590/1809-4422asoc0182r2vu19l4td
    » https://doi.org/10.1590/1809-4422asoc0182r2vu19l4td
  • RAMSAR. 2017. Brazil: environmental protection Area of Cananéia-Iguape-Peruíbe. Gland: Ramsar Information Sheet.
  • Reis, E. G. 1986. Age and growth of the marine catfish, Netuma barba (Siluriformes, Ariidae) in the estuary of the Patos Lagoon (Brazil). Fishery Bulletin, 84(3), 679–686.
  • Santificetur, C., Giaretta, M. B., Conversani, V. R. M., Brenha-Nunes, M. R., Siliprandi, C. C. & Rossi-Wongtschowski, C. L. D. B. 2017. Atlas of marine bony fish otoliths of Southeastern-Southern Brazil Part VIII: Siluriformes (Ariidae) and Pleuronectiformes (Achiridae, Paralichthyidae, Cynoglossidae). Brazilian Journal of Oceanography, 65(3), 448–494. DOI: https://doi.org/10.1590/s1679-87592017143106503
    » https://doi.org/10.1590/s1679-87592017143106503
  • Schmidt, T. C. S., Martins, I. A., Reigada, A. L. D. & Dias, J. F. 2008. Taxocenose de bagres marinhos (Siluriformes, Ariidae) da região estuarina de São Vicente, SP, Brasil. Biota Neotropica, 8(4), 73–81. DOI: https://doi.org/10.1590/s1676-06032008000400006
    » https://doi.org/10.1590/s1676-06032008000400006
  • Silva Junior, D. R., Carvalho, D. M. T. & Vianna, M. 2013. The catfish Genidens genidens (Cuvier, 1829) as a potential sentinel species in Brazilian estuarine waters. Journal of Applied Ichthyology, 29(6), 1297–1303. DOI: https://doi.org/10.1111/jai.12280
    » https://doi.org/10.1111/jai.12280
  • Souza, A. P. R., Braga, E. S. & Bertotti, M. 2012. On site stripping voltammetric determination of Zn(II), Cd(II) and Pb(II) in water samples of the Cananéia-Iguape Estuarine-Lagoon complex in São Paulo state, Brazil. Journal of the Brazilian Chemical Society, 23(7), 1320–1326. DOI: https://doi.org/10.1590/s0103-50532012000700017
    » https://doi.org/10.1590/s0103-50532012000700017
  • UNESCO (United Nations Educational, Scientific and Cultural Organization). 2011. MAB Biosphere Reserves Directory: biosphere reserve information. Accessed: https://whc.unesco.org/en/list/893

Edited by

Associate Editor:

Carmen G. Castro

Publication Dates

  • Publication in this collection
    08 Dec 2023
  • Date of issue
    2023

History

  • Received
    28 Sept 2022
  • Accepted
    16 Aug 2023
Instituto Oceanográfico da Universidade de São Paulo Praça do Oceanográfico 191, CEP: 05508-120, São Paulo, SP - Brasil, Tel.: (11) 3091-6501 - São Paulo - SP - Brazil
E-mail: diretoria.io@usp.br