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Morphometric analysis of lapillus otoliths in two estuarine bioindicator catfish (Siluriformes, Ariidae) from a marine protected area in Brazil

Abstract

Some fish species can be used as target species and bioindicators of environmental disturbances. In this context, biological indicators such as the length, weight, and height of lapillus otoliths of the ariid species Cathorops spixii and Genidens genidens were considered bioindicators of contamination of the Cananéia-Iguape estuarinelagoon complex (CIELC) in this study. The CIELC is an estuary with spatial and temporal differences regarding its hydrobiochemical properties and this characteristic has been related to changes in biological predictors such as the otolith morphometrics of estuarine fish. Therefore, this study aimed to verify the responses of otolith dimensions to sexual and temporal changes, throughout the CIELC. In total, 163 wild catfish C. spixii and 55 G. genidens were collected during the winter period of 2009, 2017, and 2018 in the CIELC. In general, the weight and length of lapillus otoliths of C. spixii and G. genidens were good metrics adjusted to fish growth. Females of C. spixii were significantly larger than males and subadults and there were no significant differences regarding the sexual approach of G. genidens. The temporal approach showed significant differences between the years for both catfish. C. spixii sampled in 2009 and 2018 showed greater total length (TL) and total weight (TW) when compared with fish from 2014 and 2017 (p < 0.05). G. genidens collected in 2018 had greater TL and TW than the specimens sampled in the other years (p < 0.05). Otolith dimensions seem to have followed this same pattern, since females of C. spixii had higher values for otolith weight, height, and length than males and subadults (p < 0.05). The data obtained in this study can be a potential tool for application combined with other ecological analyses and conservation studies in the CIELC.

Descriptors:
Cathorops spixii ; Genidens genidens ; Otoliths; Growth; Estuary

INTRODUCTION

Otoliths are structures rich in calcium carbonate (CaCO3) found in the inner ear (labyrinth) of all teleost fish, responsible for hearing and balance (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...
; Quist and Isermann, 2017Quist, M. C. & Isermann, D. A. 2017. Age and Growth of Fishes. Principles and Techniques. Bethesda: American Fisheries Society.). Bony fish have three types of otolith structures, called sagitta, lapilli, and asteriscus, which differ in their morphology and internal location in the ear capsule (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...
). These structures are formed during embryonic development and continue to grow in incremental layers of CaCO3 in an organic matrix (Campana, 1999Campana, S. E. 1999. Chemistry and Composition of Fish Otoliths: Pathways, Mechanisms and Applications. Marine Ecology Progress Series, 188, 263–297.). Since fish body growth and otolith growth are closely linked (Campana, 1999Campana, S. E. 1999. Chemistry and Composition of Fish Otoliths: Pathways, Mechanisms and Applications. Marine Ecology Progress Series, 188, 263–297.), the thickness and increment formation, and consequently the shape of otoliths, reflect periods of environmental and physiological stress, despite the fluctuations in fish growth caused by metabolic deceleration (Morales-Nin, 2000Morales-Nin, B. 2000. Review of growth regulation processes of otolith daily increment formation. Fisheries Research, 46(1), 53-67.). For this reason, as these structures grow, variations in their size and shape can be detected, while maintaining the morphology of the species, since these are species-specific characters (Campana and Casselman, 1993Campana, S. E. & Casselman, J. M. 1993. Stock Discrimination Using Otolith Shape Analysis. Canadian Journal of Fisheries and Aquatic Sciences, 50(5), 1062–1083. DOI: https://doi.org/10.1139/f93-123
https://doi.org/10.1139/f93-123...
).

The analysis of otoliths, based on traditional measurements related to size, length, and width, as well as weight, has been a particularly significant quantitative tool for studies in the identification of fish species and populations, as well as to elucidate how different individual biological processes, such as ontogenetic development and maturity, and geographic factors affect the shape of otoliths during the life cycle of populations (Campana and Casselman, 1993Campana, S. E. & Casselman, J. M. 1993. Stock Discrimination Using Otolith Shape Analysis. Canadian Journal of Fisheries and Aquatic Sciences, 50(5), 1062–1083. DOI: https://doi.org/10.1139/f93-123
https://doi.org/10.1139/f93-123...
; Vaz-dos-Santos, 2015Vaz-dos-Santos, A. M. 2015. Otolitos en estudios de edad y crecimiento en peces. In: Volpedo, A. V. & Vaz-dos-Santos, A. M. (eds.), Métodos de estudios con otolitos: principios y aplicaciones. (pp. 303–332). PIESCE-SPU.). Otolith growth can be used to estimate the size at first maturity. For example, Agostinho (2000Agostinho, C. 2000. Use of otoliths to estimate size at sexual maturity in fish. Brazilian Archives of Biology and Technology, 43(4), 437–440. DOI: https://doi.org/10.1590/s1516-89132000000400014
https://doi.org/10.1590/s1516-8913200000...
) analyzed a method based on the diphasic growth as an alternative method for estimating the size at sexual maturity of females of Plagioscion squamosissimus (Perciformes, Sciaenidae). In this context, Maciel et al. (2019Maciel, 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...
) verified that the Huxley and polyphasic allometric models were adequate in revealing differential growth patterns between males and females of the species G. genidens. Therefore, understanding the processes involved in sexual dimorphism and maturity, the applications of the morphometrics of lapillus otoliths in C. spixii and G. genidens is an interesting and accurate tool, combining allometric models and growth assessments. A more accurate assessment of the size at first maturity between male and female growth may help in stock assessment and fisheries management. Different growth patterns are observed throughout the life cycle of fish, detected using growth rates in length and weight and the biometric relationships between different parts of the body, such as otoliths (Casselman, 1990Casselman, J. 1990. Growth and Relative Size of Calcified Structures of Fish. Transactions of the American Fisheries Society, 119(4), 673–688. DOI: https://doi.org/10.1577/1548-8659
https://doi.org/10.1577/1548-8659...
). Therefore, otolith measurements have been used to detect changes in the growth rate of several fish species (Lombarte and Tuset, 2015Lombarte, A. & Tuset, V. 2015. Morfometría de otolitos. In: Volpedo, A. V. & Vaz-dos-Santos, A. M. (eds.), Métodos de estúdios con otólitos: princípios y aplicaciones. PIESCE-SPU.; Afanasyev et al., 2017Afanasyev, P., Orlov, A. & Rolsky, A. 2017. Otolith Shape Analysis as a Tool for Species Identification and Studying the Population Structure of Different Fish Species. Biology Bulletin, 44(8), 952–959. DOI: https://doi.org/10.1134/s1062359017080027
https://doi.org/10.1134/s106235901708002...
; Taştan and Sönmez, 2021Taştan, Y. & Sönmez, A. Y. 2021. A review on the relationship between the fish length and otolith biometry. Journal of Biometry Studies, 1(1), 26–34. DOI: https://doi.org/10.29329/jofbs.2021.348.06
https://doi.org/10.29329/jofbs.2021.348....
). The development, sex, and sexual maturity of fish, in addition to spatio-temporal variations in environmental conditions, may reflect changes in the shapes and growth of otoliths within the same species in different places and times (Duarte Neto, 2005Duarte Neto, P. José. 2005. Análise multivariada da forma do otólito sagita para discriminação de estoques de dourado, Coryphaena hippurus (Pisces: Coryphaenidae), no Nordeste do Brasil. (mathesis). Universidade Federal Rural de Pernambuco, Recife.).

Catfish species of the Ariidae family occur in freshwater, marine and estuarine systems in tropical and subtropical regions, and are widely distributed along the Brazilian coast (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.; Fischer et al., 2011Fischer, L. G., Pereira, L. E. D. & Vieira, J. P. 2011. Peixes Estuarinos e Costeiros (2nd ed.). Rio Grande: Luciano Gomes Fischer.), and are very important for ecological studies regarding ecophysiological responses in environments with saline and temperature gradients, as found in estuaries. In ariids, lapilli otoliths have been commonly used in growth and population biology studies in general, since they are larger than sagittae and asterisci otoliths (Fuchs and Volpedo, 2009Fuchs, D. V. & Volpedo, A. V. 2009. Morfología de Lapillus de Siluriformes Parano-Platenses. Biología Acuatica, 26, 97–108.; 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...
; 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...
). In this context, some authors have used lapillus otoliths to determine age and growth in populations of ariids that inhabit the Brazilian coast, such as Genidens genidens, Genidens barbus, Netuma barba, and Sciades proops (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....
; 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...
; Freire et al., 2017Freire, K., Oliveira, C. & Rosa, L. 2017. Morphometric analysis of otoliths of juvenile crucifix sea catfish Sciades proops (Valenciennes, 1840). Journal of Applied Ichthyology, 33(3), 485–490. DOI: https://doi.org/10.1111/jai.13321
https://doi.org/10.1111/jai.13321...
; Maciel et al., 2018Maciel, 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-...
, 2019Maciel, 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...
). Some studies on otolith morphometrics in ariids have also been performed to aid in species identification (Chen et al., 2008Chen, H. L., Shen, K. N., Chang, C. W., Iizuka, Y. & Tzeng, W. N. 2008. Effects of water temperature, salinity and feeding regimes on metamorphosis, growth and otolith Sr:Ca ratios of Megalops cyprinoides leptocephali. Aquatic Biology, 3, 41–50. DOI: https://doi.org/10.3354/ab00062
https://doi.org/10.3354/ab00062...
; Vaz-dos-Santos, 2015Vaz-dos-Santos, A. M. 2015. Otolitos en estudios de edad y crecimiento en peces. In: Volpedo, A. V. & Vaz-dos-Santos, A. M. (eds.), Métodos de estudios con otolitos: principios y aplicaciones. (pp. 303–332). PIESCE-SPU.), differentiation of sexual dimorphism (Maciel et al., 2019Maciel, 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...
), and as an indication of habit use and movement between regions of the species by chemical evaluation (i.e., Ca/Sr, Ca/Ba) in lapillus otoliths (Avigliano et al., 2015Avigliano, E., Velasco, G. & Volpedo, A. 2015. Assessing the use of two southwestern Atlantic estuaries by different life cycle stages of the anadromous catfish Genidens barbus (Lacépède, 1803) as revealed by Sr : Ca and Ba : Ca ratios in otoliths. Journal of Applied Ichthyology, 31(4), 740–743. DOI: https://doi.org/10.1111/jai.12766
https://doi.org/10.1111/jai.12766...
, 2020Avigliano, E., Martínez, G., Stoessel, L., Méndez, M., Bordel, N., Pisonero, J. & Volpedo, A. V. 2020. Otoliths as indicators for fish behaviour and procurement strategies of hunter-gatherers in North Patagonia. Heliyon, 6(3), e03438., 2021Avigliano, E., Pisonero, J., Méndez, A., Tombari, A. & Volpedo, A. 2021. Habitat use of the amphidromous catfish Genidens barbus: first insights at its southern distribution limit. New Zealand Journal of Marine and Freshwater Research, 56(2), 284–290. DOI: https://doi.org/10.1080/00288330.2021.1879178
https://doi.org/10.1080/00288330.2021.18...
; Fortunato et al., 2017Fortunato, R. V, D. & Volpedo, A. 2017. Otolith morphometry and microchemistry as habitat markers for juvenile Mugil cephalus Linnaeus 1758 in nursery grounds in the Valencian community Spain. Journal Applied Ichthyology, 33, 163–167. DOI: https://doi.org/10.1111/jai.13291
https://doi.org/10.1111/jai.13291...
; Condini et al., 2019Condini, M. V., Pereyra, P. E. R., Garcia, A. M., Saint’pierre, T. D., Ceni, G., Lugo, R., Fontoura, N. F., Vieira, J. P. & Albuquerque, C. Q. 2019. Use of fresh water by an estuarine-resident marine catfish: evidence from gonadal and otolith chemistry analyses. Journal of the Marine Biological Association of the United Kingdom, 99(7), 1667–1674. DOI: https://doi.org/10.1017/s0025315419000493
https://doi.org/10.1017/s002531541900049...
; Maciel et al., 2020Maciel, T., Avigliano, E., Carvalho, B., Miller, N. & Vianna, M. 2020. Population structure and habitat connectivity of Genidens genidens (Siluriformes) in tropical and subtropical coasts from Southwestern Atlantic. Estuarine, Coastal and Shelf Science, 242, 106839. DOI: https://doi.org/10.1016/j.ecss.2020.106839
https://doi.org/10.1016/j.ecss.2020.1068...
). Finally, lapillus otoliths of C. spixii have been used to compare with those of the species G. genidens (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...
), and these structures have been used in assessments of the somatic growth-otolith growth relationship (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.). However, none of these were focused on sexual approach and maturity.

The ariids G. genidens (Cuvier, 1829) and Cathorops spixii (Agassiz, 1829) are distributed throughout the east coast of South America, from the Guianas to the Rio de la Plata in Argentina, and are one of the most commons ariids on the Brazilian coast (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....
), 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...
). C. spixii has been used to provide response as a bioindicator of contamination in the Brazilian coastal area under different anthropogenic influences (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, Hortellani, M. A. & Ladle, R. J. 2012. Are Catfish (Ariidae) effective bioindicators for Pb, Cd, Hg, Cu and Zn? Water, Air, and Soil Pollution, 223(7), 3911–3922. DOI: https://doi.org/10.1007/s11270-012-1160-2
https://doi.org/10.1007/s11270-012-1160-...
; 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.). In addition, Azevedo et al. (2012Souza Azevedo, J., Souza Sarkis, J. E., Oliveira, T. A. & Ulrich, J. C. 2012. Tissue-specific mercury concentrations in two catfish species from the Brazilian coast. Brazilian Journal of Oceanography. DOI: https://doi.org/10.1590/S1679-87592012000200011
https://doi.org/10.1590/S1679-8759201200...
) suggested that G. genidens has significant potential as a sentinel species for biomonitoring, including the Santos-São Vicente estuarine system, one of the most degraded estuarine systems on the southern Brazilian coast (Meniconi et al., 2012Meniconi, M. F. G., Silva, T. A., Fonseca, O. F., M. L., Lima Sirayama, Lavrado, H. P. & G, F. A. (eds.). 2012. Baía de Guanabara: síntese do conhecimento ambiental. Rio de Janeiro: Petrobras.). On the other hand, the Cananéia-Iguape estuarine-lagoon complex (CIELC) is an aquatic ecosystem subject to minimal anthropogenic influence, where C. spixii and G. genidens have a complete life cycle (Mishima and Tanji, 1981Mishima, M. & Tanji, S. 1981. Distribuição geográfica dos bagres marinhos (Osteichthyes, Ariidae) no Complexo Estuarino Lagunar de Cananéia (25o s 48o w). Boletim Do Instituto de Pesca, 8, 157–172.) with current habitat use partitioning models, as expected in the literature (Yànez-Arancibia and Lara-Dominguez, 1988Yànez-Arancibia, A. & Lara-Dominguez, A. L. 1988. Ecology of three sea catfishes (Ariidae) in a tropical coastal ecosystem - Southern Gulf of Mexico. Marine Ecology Progress Series, 49, 215–230. DOI: https://doi.org/10.3354/meps049215
https://doi.org/10.3354/meps049215...
; 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...
; Torres, 2009).

The development of management criteria and conservation strategies in aquatic environments to improve or protect ecological properties and functions requires the use of biological indicators, such as fish, and target species to assess habitat quality (Chovanec et al., 2003Chovanec, A., Hofer, R. & Schiemer, F. 2003. Chapter 18: Fish as bioindicators. In: Trace Metals and other Contaminants in the Environment (Vol. 6, pp. 639–676). Elsevier. DOI: https://doi.org/10.1016/s0927-5215(03)80148-0
https://doi.org/10.1016/s0927-5215(03)80...
). Thus, studies with bioindicator species, such as the Ariidae representatives C. spixii and G. genidens (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, Hortellani, M. A. & Ladle, R. J. 2012. Are Catfish (Ariidae) effective bioindicators for Pb, Cd, Hg, Cu and Zn? Water, Air, and Soil Pollution, 223(7), 3911–3922. DOI: https://doi.org/10.1007/s11270-012-1160-2
https://doi.org/10.1007/s11270-012-1160-...
; Maciel et al., 2018Maciel, 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-...
), are very important, since they can be used to improve knowledge about life history, growth, and habitat use (Avigliano et al., 2014Avigliano, E., Martinez, C. & Volpedo, A. 2014. Combined use of otolith microchemistry and morphometry as indicators of the habitat of the silverside (Odontesthes bonariensis) in a freshwater–estuarine environment. Fisheries Research, 149, 55–60. DOI: https://doi.org/10.1016/j.fishres.2013.09.013
https://doi.org/10.1016/j.fishres.2013.0...
), in association with subcellular biochemical, genetic, and histological responses (Chovanec et al., 2003Chovanec, A., Hofer, R. & Schiemer, F. 2003. Chapter 18: Fish as bioindicators. In: Trace Metals and other Contaminants in the Environment (Vol. 6, pp. 639–676). Elsevier. DOI: https://doi.org/10.1016/s0927-5215(03)80148-0
https://doi.org/10.1016/s0927-5215(03)80...
; 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.2013.06...
). Although the CIELC is anthropogenically influenced by continental discharges in the northern area, by the Ribeira de Iguape River inflow via Valo Grande (Mahiques et al., 2009Mahiques, M. M., Burone, L., Figueira, R. C. L., Lavenère, W. A. A. O., Capellari, B., Rogacheski, E. C., Barroso, C. P., Santos, A. L. S., Cordeiro, L. M. & Cussioli, M. C. 2009. Anthropogenic influences in a lagoonal environment: a multiproxy approach at the Valo Grande mouth. Cananéia-Iguape system (SE Brazil). Brazilian Journal of Oceanography, 57(4), 325–337., 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-...
; Cornaggia et al., 2018Cornaggia, F., Jovane, L., Alessandretti, L., Ferreira, P. A. L., Figueira, R. C. L., Rodelli, D., Berbel, G. B. B. & Braga, E. S. 2018. Diversions of the Ribeira River Flow and Their Influence on Sediment Supply in the Cananeia-Iguape Estuarine-Lagoonal System (SE Brazil). Frontiers in Earth Science, 6. DOI: https://doi.org/10.3389/feart.2018.00025
https://doi.org/10.3389/feart.2018.00025...
), this estuarine system still has characteristics of a healthy ecosystem based on its hydrobiogeochemical characteristics (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.; 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...
). Therefore, the use of otolith measurements as a predictor of temporal changes in fish from the CIELC is highly valid. In this context, the present study aimed to analyze whether there were sexual and temporal changes in otolith dimensions within the study period based on the responses of otolith dimensions along the Cananéia-Iguape estuarine-lagoon complex (CIELC).

METHODS

Study area and fish collection

The study area is located on the south coast of São Paulo State (SP), in the Cananéia-Iguape estuarine-lagoon complex (CIELC) (25°00’28.27S/47°56’01.89W). This area is part of the Lagamar Mosaic of Conservation Units (Cananéia-Iguape-Peruíbe Environmental Protection Area), recognized as the Atlantic Forest Biosphere Reserve since 1992, and considered a Natural World Heritage site since 1999 (Côrrea, 1995Côrrea, F. 1995. Caderno no 2: A Reserva da Biosfera da Mata Atlântica Roteiro para o entendimento de seus objetivos e seu Sistema de Gestão. São Paulo: Conselho Nacional da Reserva da Biosfera da Mata Atlântica. Accessed: https://rbma.org.br/n/publicacoes/
https://rbma.org.br/n/publicacoes/...
). Since 2017, it has been an international priority area for conservation, as it was recognized as a Ramsar site (https://rsis.ramsar.org/ris/2310). The northern region of the CIELC is mainly influenced by the Ribeira de Iguape fluvial inputs (Prado et al., 2019Prado, H., Scilndwein, M., Murrieta, R., Junior, D., Souza, E., Cunha-Lignon, M., Mahiques, M., Giannini, P. & Contente, R. 2019. O Canal do Valo Grande no Complexo Estuarino Cananéia-Iguape (SP, Brasil): História Ambiental, Ecologia e Perspectivas Futuras. Ambiente e Sociedade, 22, e01822. DOI: https://doi.org/10.1590/1809-4422asoc0182r2vu19l4td
https://doi.org/10.1590/1809-4422asoc018...
), and where the salinity is lower, ranging from 10 to 30 (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-...
). On the other hand, the southern region is significantly influenced by the ocean and is a region with conserving natural conditions attributed to the major marine influxes (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.). Wetlands considered Ramsar sites are priority regions and very important for achieving sustainable development via local and national actions and international cooperation, for example. Therefore, all abiotic and biological aspects of the CIELC reinforce the importance of obtaining empirical data on the general biology of resident species, such as the ariids C. spixii and G. genidens, to promote their conservation and sustainable use.

Due to the differences between the species regarding habitat use and distribution (Mishima and Tanji, 1981Mishima, M. & Tanji, S. 1981. Distribuição geográfica dos bagres marinhos (Osteichthyes, Ariidae) no Complexo Estuarino Lagunar de Cananéia (25o s 48o w). Boletim Do Instituto de Pesca, 8, 157–172.; Rios, 2001Rios, E. P. 2001. Papel do estuário no ciclo de vida das espécies dominantes da ictiofauna do Complexo Estuarino-Lagunar de Cananéia-Iguape. (phdthesis). Universidade de São Paulo, Instituto Oceanográfico, São Paulo.), C. spixii were collected only in the southern region (site 1) and G. genidens in the northern region (site 2) of the CIELC (SP, Brazil) (Figure 1). The fish were collected in August 2009, 2014, 2017, and 2018, on board the research vessel Albacora of the Oceanographic Institute of the University of São Paulo (USP), using a bottom otter trawl (1.6” mesh wall, 1.2” mesh cod end, and 11 m long), lasting 10 minutes each, trawling at a mean depth of 6 m at 3 mph. The catfish were immediately separated from the other fish, and the species were identified according to 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.) and Marceniuk (2005Marceniuk, A. P. 2005. Chave de identificação das espécies de bagres marinhos (Siluriformes, Ariidae) da costa brasileira. Boletim Do Instituto de Pesca, 31(2), 89–101.), considering the main characteristics of the occipital process of the skull and the dentition. All analyzed and collected C. spixii and G. genidens specimens were authorized by the Chico Mendes Institute for Biodiversity Conservation (ICMBio; SISBIO Processes No. 20398-1; 63087-1) and the recommendations of the Animal Ethics Committee of the Federal University of São Paulo were followed (CEUA-UNIFESP; No. 2597030815; 9841150518). The voucher specimen MZUSP-48529 is deposited in the ichthyological collection of the Museum of Zoology, USP.

Figure 1.
Cananéia-Iguape estuarine-lagoon complex (CIELC), Southeastern Brazil, with sampling sites: 1) South; 2) North.

Laboratory procedure

After collection, the fish were transported to the laboratory of the “Dr. João de Paiva Carvalho” Research Base of the Oceanographic Institute, in Cananéia, using an icebox. Sex identification was performed by identifying the macroscopic, morphological, and color characteristics of the gonads: females – orange gonads, with developing oocytes; males – white-colored tissue in the abdomen. All the fish that did not show a defined gonadal pattern were considered subadults (Gomes et al., 1999Gomes, I. D., Araújo, F. G., Azevedo, M. C. C. & Pessanha, A. L. M. 1999. Biologia reprodutiva dos bagres marinhos Genidens genidens (Valenciennes) e Cathorops spixii (Agassiz) (Siluriformes, Ariidae), na baía de Sepetiba, Rio de Janeiro, Brasil. Revista Brasileira de Zoologia, 16(2), 171-180.; Fávaro et al., 2005Fávaro, L. F., Frehse, F. A., Oliveira, R. N. & Schwarz Júnior, R. 2005. Reprodução do bagre amarelo, Cathorops spixii (Agassiz) (Siluriformes, Ariidae), da Baía de Pinheiros, região estuarina do litoral do Paraná, Brasil. Revista Brasileira de Zoologia, 22(4), 1022–1029. DOI: https://doi.org/10.1590/s0101-81752005000400030
https://doi.org/10.1590/s0101-8175200500...
), who have passed the free embryo stage, which is the juvenile of the free -swimming juvenile (Lima et al., 2012Lima, A. R. A., Barletta, M., Dantas, D. V., Possato, F. E., Ramos, J. A. A. & Costa, M. F. 2012. Early development and allometric shifts during the ontogeny of a marine catfish (Cathorops spixii-Ariidae),. Journal Applied Ichthyology, 28, 217–225.), as they are below length at first maturation, being 9.66-9.80 cm for C. Spixii (Mishima and Tanji, 1983Mishima, M. & Tanji, S. 1983. Maturação e desova dos bagres marinhos (Osteichthyes, Ariidae) no complexo estuarino-lagunar de Cananéia (25oS, 48oW). Boletim Do Instituto de Pesca, 10, 129–141.) and 13 cm for G. Genidens (Araújo et al., 1998Araújo, F. G., Cruz-Filho, A. G., Azevedo, M. C. C. & Santos, A. C. A. 1998. Estrutura da comunidade de peixes demersais da baía de Sepetiba, RJ. Revista Brasileira de Biologia, 58(3), 417-430.). Therefore, we consider subadult fish to be those that most resemble the morphological characteristics of adult fish (Lima et al., 2012Lima, A. R. A., Barletta, M., Dantas, D. V., Possato, F. E., Ramos, J. A. A. & Costa, M. F. 2012. Early development and allometric shifts during the ontogeny of a marine catfish (Cathorops spixii-Ariidae),. Journal Applied Ichthyology, 28, 217–225.), but which are not yet able to reproduce, as they have not yet reached adult size and reproductive maturity. Despite the low number of subadults of C. spixii and females of G. genidens collected, these data were recorded and shown, since there is a paucity of morphometric data on these catfish species concerning their sexual approach in marine protected area such as the CIELC.

The total length (TL; cm) and total weight (TW; g) of C. spixii and G. genidens were obtained, and the catfish were dissected for the removal of the pair of lapilli otoliths from the ear capsule. The lapillus is the most robust pair of otoliths of C. spixii and G. genidens (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...
). Otoliths were extracted using a cross-sectional cut on the inner surface of the fish’s skull to expose the inner ear in which otoliths are inserted (Pisam et al., 1998Pisam, M., Payan, P., Lemoal, C., Edeyer, A., Boeuf, G. & Mayer-Gostan, N. 1998. Ultrastructural study of the saccular epithelium of the inner ear of two teleosts, Oncorhynchus mykiss and Psetta maxima. Cell and Tissue Research, 294, 261–270. DOI: https://doi.org/10.1007/s004410051176
https://doi.org/10.1007/s004410051176...
; 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...
).

Lapilli otoliths were washed in deionized water (≥ 18.2 MΏ cm) obtained from a Milli-Q water purification system (Millipore), dried, and stored in polypropylene microtubes (2 mL). Otoliths were measured for length (OL: the longest horizontal measurement between the posterior and anterior margins of the otolith), height (OH: measured between the dorsal and ventral margins), and weight (OW) (Figure 2). OL and OH were measured using a manual caliper with an accuracy of ± 0.01 mm. OW was obtained using a digital scale with an accuracy of ± 0.001 mg. The left and right otoliths were included in the collection of the Aquatic Toxicology and Fish Ecophysiology Group (AquaTox) in the Federal University of São Paulo (UNIFESP), Diadema, Brazil.

Figure 2.
Schematic drawing of the left lapillus otolith of C. spixii with identification of measurements and morphological structures. Otolith length (OL) and otolith height (OH). Position relative to the fish: D: Dorsal; P: Posterior; A: Anterior; and V: Ventral.

Data analysis

Non-linear (exponential) regressions were used to determine the relationships between otolith variables (length, height, and weight) and fish weight and length (Y = a × Xb), where a is the intercept of the regression curves and b is the slope of the regression (Harvey et al., 2000Harvey, J. T., Oughlin, T. R., Perez, M. A. & Oxman, D. S. 2000. Relationship between fish size and otolith length for 63 species of fishes from the eastern North Pacific Ocean. NOAA Technical Report, 150, 1–36.; Zar, 2009Zar, J. H. 2009. Biostatistical analysis (4th ed.). New Jersey: Prentice Hall.).

Differences between otolith measurements regarding the sexual and temporal approach of both species were tested using nonparametric analysis of variance (ANOVA) with post-hoc test (Kruskal-Wallis test with Dunn’s multiple comparisons). The significance level considered was p < 0.05. The dispersion of the data between the response variable and the exploratory variable was verified by R-squared (R2). Since there was no difference in the measurements of the left and right otoliths (length, weight, and height) (rs = 0.95), in this study, only the left otoliths were processed for morphometric analysis.

The accuracy of the measurements was determined by calculating the mean percentage error. The mean percentage prediction error was calculated as average of the percentage prediction error (%PE) values for all specimens, in accordance with Smith (1980), following the formula:

\begin{gathered} \%PE= \chi_{Predicted}-\chi_{Observed}1 \times 100\\\chi_{Observed} \end{gathered}

RESULTS

In total, 163 wild catfish C. spixii and 55 G. genidens were collected during the winter period (August) of 2009 (C. spixii: n = 17), 2014 (C. spixii: n = 27; G. genidens: n = 21), 2017 (C. spixii: n = 35; G. genidens: n = 7), and 2018 (C. spixii: n = 33; G. genidens: n = 25). Otolith measurements were self-consistent, with %PE ranging from 0.80 (TL x OW) to 20.90 (TW x OL) for G. genidens and from 3.35 (TL x OW) to 20.68 (TW x OH) for C. spixii (tbl. 1). tbl. 2 shows the measurements of the catfish species and the biometric data of lapillus otoliths. In general, females of C. spixii were significantly larger than males and subadults (TLfemales = 29 ± 86 cm; TLmales = 20 ± 60 cm; TLsubadults = 15 ± 8 cm; p < 0.05). On the other hand, no significant differences were observed regarding the sexual approach (females and males) of G. genidens (TLfemales = 23 ± 28 cm; TLmales = 21 ± 48 cm; p > 0.05). With respect to the temporal approach, C. spixii sampled in 2009 and 2018 showed greater total length (TL) and total weight (TW) when compared with fish from 2014 and 2017 (p < 0.05). G. genidens collected in 2018 had greater TL and TW than specimens sampled in the other years (p < 0.05). The same pattern was observed for otolith measurements (tbl. 2), since females of C. spixii had higher values for otolith weight, height, and length than males and subadults (p < 0.05); and no statistically significant differences were observed regarding these measurements between males and females of G. genidens (p > 0.05). In the temporal context, otoliths of C. spixii from 2009 and 2018 had greater OW, OH, and OL, while in G. genidens, higher values were observed only in otoliths of fish from 2018 (tbl. 2).

Table 1.
Percentage prediction error (%PE) regarding fish size and weight (TL: Total length) and otolith measurements (OW: Otolith weight; OH: Otolith height; OL: Otolith length) for males, females, and subadults and the temporal approach of Cathorops spixii and Genidens genidens from the CIELC, SP, Brazil.

Table 2.
Mean and standard deviation of otolith length (OL), weight (OW), and height (OH) —total length (TL) and total weight (TW)— of adults (males and females) and subadults of catfish species.

The relationships between fish and otolith measurements are shown in Figures 3 (fish length and otolith length, height, and weight) and 4 (fish weight and otolith length, height, and weight) for both the sexual and temporal approaches of C. spixii specimens. Regarding G. genidens, the same relationships are expressed in Figures 5 (fish length and otolith length, height, and weight) and 6 (fish weight and otolith length, height, and weight). Regression analysis shows significant differences (p < 0.05) between catfish size and weight (C. spixii and G. genidens) and otolith measurements (length, height, and weight) (Figures 3, 4, 5, and 6).

Figure 3.
Relationship between fish size (TL: Total length) and otolith measurements (OW: Otolith weight; OH: Otolith height; OL: Otolith length) of males, females, and subadults of Cathorops spixii from the CIELC, SP, Brazil.

Figure 4.
Relationship between fish weight (TW: Total weight) and otolith measurements (OW: Otolith weight; OH: Otolith height; OL: Otolith length) of males, females, and subadults of Cathorops spixii from the CIELC, SP, Brazil.

Figure 5.
Relationship between fish size (TL: Total length) and otolith measurements (OW: Otolith weight; OH: Otolith height; OL: Otolith length) of males, females, and subadults of Genidens genidens from the CIELC, SP, Brazil.

Figure 6.
Relationship between fish weight (TW: Total weight) and otolith measurements (OW: Otolith weight; OH: Otolith height; OL: Otolith length) of males, females, and subadults of Genidens genidens from the CIELC, SP, Brazil.

Regarding C. spixii, there were no significant differences in weight and height between males and females of C. spixii, except that otolith length of females was greater than that of males and subadults (OLfemales = 0.94 ± 0.26; OLmales = 0.82 ± 0.20; OLsubadults = 0.61 ± 0.17). Subadults were lighter than males and females (OWmales = 0.24 ± 0.17; OWfemales = 0.36 ± 0.29; OWsubadults = 0.09 ± 0.03). It was possible to observe that otolith length and weight of females of C. spixii were greater compared with males (Figures 3 and 4). Regarding G. genidens, the same pattern was observed, with no significant sex differences in otolith weight, length, and height between males and females (Figures 5 and 6). In fact, the number of females was very low, and this aspect may have influenced these results. Subadults of G. genidens had a lower weight than adults (OWmales = 0.24 ± 0.17; OWfemales = 0.36 ± 0.29; OWsubadults = 0.09 ± 0.03). The temporal approach showed significant differences within the study period for both catfish species C. spixii (Figures 3 and 4) and G. genidens (Figures 5 and 6).

DISCUSSION

In this study, we could verify the potential of applying regression analysis for testing morphometric relationships between the total length and lapillus otolith dimensions of adults and subadults of Genidens genidens. In general, otolith weight, length, and height were good metrics adjusted to fish growth, as has also been reported in other studies with the same species. Although using adjusted linear regression analysis, 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...
) also found high correlation coefficient values between otolith height, weight, and length versus fish biometrics when analyzing the same species studied from another location. Otolith length of the catfish C. spixii and G. genidens proved to have a stronger relationship with fish length than otolith weight (Figures 3 and 5). This relationship has been previously demonstrated in the literature (Avigliano and Volpedo, 2016Avigliano, E. & Volpedo, A. 2016. A Review of the Application of Otolith Microchemistry Toward the Study of Latin American Fishes. Reviews in Fisheries Science & Aquaculture, 24(4), 369–384. DOI: https://doi.org/10.1080/23308249.2016.1202189
https://doi.org/10.1080/23308249.2016.12...
; Winkler et al., 2019Winkler, A. C., Duncan, M. I., Farthing, M. W. & Potts, W. M. 2019. Sectioned or whole otoliths? A global review of hard structure preparation techniques used in ageing sparid fishes. Reviews in Fish Biology and Fisheries, 29(3), 605–611. DOI: https://doi.org/10.1007/s11160-019-09571-1
https://doi.org/10.1007/s11160-019-09571...
; Ozpicak et al., 2021Ozpicak, M., Saygin, S., Yilmaz, S. & Polat, N. 2021. Otolith phenotypic analysis for the endemic Anatolian fish species, Caucasian bleak Alburnus escherichii Steindachner, 1897 (Teleostei, Leuciscidae), from Selevir Reservoir, Akarçay Basin, Turkey. Oceanological and Hydrobiological Studies, 50(4), 430–440. DOI: https://doi.org/10.2478/oandhs-2021-0037
https://doi.org/10.2478/oandhs-2021-0037...
).

In this study, we intended to analyze whether there are sexual and temporal changes in otolith dimensions of the two ariid species C. spixii and G. genidens. Some studies have shown that, although G. genidens does not present evident sexual dimorphism demonstrated by body morphometrics, significant differences are observed, mainly in head and mouth measurements, related to the oropharyngeal incubation of offspring performed by males (Paiva et al., 2015Paiva, L., Prestrelo, L., Sant’anna, K. & Vianna, M. 2015. Biometric sexual and ontogenetic dimorphism on the marine catfish Genidens genidens (Siluriformes, Ariidae) in a tropical estuary. Latin American Journal of Aquatic Research, 43(5), 895–903. DOI: https://doi.org/10.3856/vol43-issue5-fulltext-9
https://doi.org/10.3856/vol43-issue5-ful...
). In addition, studies using otolith measurements of G. genidens found differences between the sexes with respect to growth parameters such as length and age rings (Maciel et al., 2018Maciel, 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-...
).

An important highlight of this study is the lack of significant differences regarding otolith height in adults (males and females) and subadults of catfish species (Figure 3, 4, 5, and 6). In fact, in some cases, it is possible that otolith weight fits better to fish length and height, since otoliths stop growing in size when the fish reaches its maximum length. Therefore, once the fish reaches its asymptotic length, the otolith mainly increases in weight. Thus, otolith height does not grow proportionally to fish growth and these results also may suggest that, in the case of these catfish species, the variable is not reliable for growth studies.

As dispersion can indicate the degree of variation in otolith biometric data, the dispersion found in the morphometric relationship of C. spixii and G. genidens may indicate the effect of temporal variability. In this sense, it is possible that there is more than one cohort collected with a difference in otolith growth rate, since the specimens collected in 2009, 2014, 2017, and 2018 were exposed to different environmental conditions (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...
). Some studies have reported the environmental effect on otolith growth (Lombarte and Lleonart, 1993aLombarte, A. & Lleonart, J. 1993a. Otolith size changes related with body growth, habitat depth and temperature. Environmental Biology of Fishes, 37(3), 297–306. DOI: https://doi.org/10.1007/BF00004637
https://doi.org/10.1007/BF00004637...
; Sadovy and Severin, 1994Sadovy, Y. & Severin, K. P. 1994. Elemental patterns in red hind (Epinephelus guttatus) otoliths from Bermuda and Puerto Rico reflect growth rate, not temperature. Canadian Journal of Fisheries and Aquatic Sciences, 51(1), 133–141. DOI: https://doi.org/10.1139/f94-015
https://doi.org/10.1139/f94-015...
; Chen et al., 2008Chen, H. L., Shen, K. N., Chang, C. W., Iizuka, Y. & Tzeng, W. N. 2008. Effects of water temperature, salinity and feeding regimes on metamorphosis, growth and otolith Sr:Ca ratios of Megalops cyprinoides leptocephali. Aquatic Biology, 3, 41–50. DOI: https://doi.org/10.3354/ab00062
https://doi.org/10.3354/ab00062...
). 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...
) reported the existence of abnormal age rings in lapillus otoliths of C. spixii from the same sampling site of this study, the region of greatest marine influx in the CIELC, indicating the potential effect of environmental conditions of this coastal region on age ring formation.

Estuarine ecosystems are highly dynamic environments, subject to changes in the water regarding salinity, pH, dissolved oxygen levels, and temperature. These abiotic changes promote environmental modifications in the habitat that are reflected in fish growth (Bøeuf and Payan, 2001Bøeuf, G. & Payan, P. 2001. How should salinity influence fish growth? Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 130(4), 411–423. DOI: https://doi.org/10.1016/s1532-0456(01)00268-x
https://doi.org/10.1016/s1532-0456(01)00...
). Some authors have reported changes in the growth of otoliths of other species collected in different coastal regions (Buttler et al., 1996; Dehghani et al. 2016Dehghani, S., M., Kamrani, E., Salarpouri, A. &. Sharifian. 2016. Otolith dimensions (length, width), otolith weight and fish length of Sardinella sindensis (Day,1878), as index for environmental studies, Persian Gulf, Iran. Marine Biodiversity Records, 9, 44.). These variations in otolith growth could be due to differences in habitat, food availability, and physiochemical factors of the environment waters (Aydin et al., 2004Aydin, R., Calta, M., Sen, D. & Coban, M. Z. 2004. Relationships between fish lengths and otolith length in the population of Chondrostoma regium (Heckel, 1843) Inhabiting Keban Dam Lake. Pakistan Journal of Biological Science, 7, 1550–1553.; Javor et al., 2011Javor, B., Lo, N. & Vetter, R. 2011. Otolith morphometrics and population structure of Pacific sardine (Sardinops sagax) along the west coast of North America. Fishery Bulletin, 109, 402–415.). Furthermore, the difference in otolith growth may be related to the changes in life history between juveniles, subadults, and adults.

The majority of subadults of C. spixii were collected in the northern region of the CIELC. These specimens had a total length above first maturity (10.6 to 16.1 cm) compared with those reported by Mishima and Tanji (1983Mishima, M. & Tanji, S. 1983. Maturação e desova dos bagres marinhos (Osteichthyes, Ariidae) no complexo estuarino-lagunar de Cananéia (25oS, 48oW). Boletim Do Instituto de Pesca, 10, 129–141.) of 9.6 and 9.8 cm. Therefore, this result is interesting to be assessed regarding the presence of subadults in both regions of the CIELC (north and south), as well as the variation in length at first maturity in this species over the years, since it can respond to environmental variables (Lombarte and Lleonart, 1993bLombarte, A. & Lleonart, J. 1993b. Otolith size changes related with body growth, habitat depth and temperature. Environmental Biology of Fishes, 37(3), 297–306. DOI: https://doi.org/10.1007/bf00004637
https://doi.org/10.1007/bf00004637...
; Ozpicak et al., 2021Ozpicak, M., Saygin, S., Yilmaz, S. & Polat, N. 2021. Otolith phenotypic analysis for the endemic Anatolian fish species, Caucasian bleak Alburnus escherichii Steindachner, 1897 (Teleostei, Leuciscidae), from Selevir Reservoir, Akarçay Basin, Turkey. Oceanological and Hydrobiological Studies, 50(4), 430–440. DOI: https://doi.org/10.2478/oandhs-2021-0037
https://doi.org/10.2478/oandhs-2021-0037...
). Moreover, the variation in length at first maturity may be related to the difficulty in separating subadults from those starting a new reproductive cycle. Especially when the assessment of length at first maturity is based on analyses of gonadal maturity, as in the present study and the study by Mishima and Tanji (1983Mishima, M. & Tanji, S. 1983. Maturação e desova dos bagres marinhos (Osteichthyes, Ariidae) no complexo estuarino-lagunar de Cananéia (25oS, 48oW). Boletim Do Instituto de Pesca, 10, 129–141.).

Finally, the results presented here are fundamental for the advancement of age and growth studies in catfish such as C. spixii and G. genidens, since the proportionality between fish and otolith weight and length was verified. Although otolith length of C. spixii and G. genidens had a strong relationship with fish length, for this information to be effectively used, especially with regard to fishery stock assessments, the relationship has to be linked to fish age. To achieve this, further studies would be needed to assess how otolith growth relates to fish growth. Important perspectives that can be explored by this study refer to the combined use of otolith morphometrics with other analyses, such as otolith microchemistry, to investigate the life history and habitat use of these bioindicator catfish species.

CONCLUSION

The morphometric data of lapillus otoliths of these catfish species, regarding the temporal approach, evidenced the potential of these metrics to predict temporal variations in aquatic ecosystems with differential hydrobiogeochemical characteristics such as those observed in the CIELC.

ACKNOWLEDGMENTS

The authors would like to thank the Oceanographic Institute of the University of São Paulo (IOUSP), Brazil, and the team of the IOUSP research vessel Albacora for their support in fish sampling. This study was funded in part by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) – Brazil – Finance Code 001 (Morais, I.S.).

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Edited by

Associate Editor:

Carmen G. Castro

Publication Dates

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

History

  • Received
    18 Mar 2022
  • Accepted
    29 Sept 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