Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-25T07:17:55.621Z Has data issue: false hasContentIssue false
  • English
  • Français

Spatial environmental variability of natural markers and habitat use of Cathorops spixii in a neotropical estuary from otolith chemistry

Published online by Cambridge University Press:  19 August 2020

Barbara Maichak de Carvalho Open the ORCID record for Barbara Maichak de Carvalho [Opens in a new window] ,
Daniel Vicente Pupo ,
Alejandra Vanina Volpedo ,
Jorge Pisonero ,
Ana Méndez  and
Esteban Avigliano Open the ORCID record for Esteban Avigliano [Opens in a new window]
Barbara Maichak de Carvalho
Affiliation:
Programa de Pós-Graduação em Engenharia Ambiental, Departamento de Engenharia - UFPR, Centro Politécnico, CEP 81531-970, Bairro Jardim das Américas, Curitiba, Paraná, Brazil
Daniel Vicente Pupo
Affiliation:
Laboratório de Foraminíferos e Micropaleontologia, Setor de Ciências Biológicas- UFPR, Centro Politécnico, CEP 81531-990, Bairro Jardim das Américas, Curitiba, Paraná, Brazil
Alejandra Vanina Volpedo
Affiliation:
Universidad de Buenos Aires-CONICET. Instituto de Investigaciones en Producción Animal (INPA) / Centro de Estudios Transdisciplinarios del Agua (CETA) Facultad de Ciencias Veterinarias Universidad de Buenos Aires), Av. Chorroarin 280, Buenos Aires, CP1427Argentina
Jorge Pisonero
Affiliation:
Departamento de Física, Facultad de Ciencias, Universidad de Oviedo, Federico García Lorca No 18, Oviedo33007, España
Ana Méndez
Affiliation:
Departamento de Física, Facultad de Ciencias, Universidad de Oviedo, Federico García Lorca No 18, Oviedo33007, España
Esteban Avigliano*
Affiliation:
Universidad de Buenos Aires-CONICET. Instituto de Investigaciones en Producción Animal (INPA) / Centro de Estudios Transdisciplinarios del Agua (CETA) Facultad de Ciencias Veterinarias Universidad de Buenos Aires), Av. Chorroarin 280, Buenos Aires, CP1427Argentina
*
Author for correspondence: Esteban Avigliano, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The goal of this study was to study the distribution of potential habitat markers (Sr/Ca, Ba/Ca, Mn/Ca and Li/Ca) in water from the Paranaguá Estuarine Complex (Brazil) and to study habitat use patterns of Cathorops spixii through ontogeny employing otolith microchemistry. Fish were caught from three sampling sites while water samples were collected at eight stations covering a salinity range from 4.5–33. Elemental concentrations in otolith and water were determined by LA-ICP-MS and ICP-MS, respectively. When the relationship between salinity and elements or ratios in water was studied, significant positive relationships were found for Sr, Li, Ca, Sr/Ca, and negative for Ba, Mn, Ba/Ca and Mn/Ca (P < 0.05). No relationship was observed between water Li/Ca and salinity. A significant positive correlation was found between otolith edge Sr/Ca and salinity (r = 0.63; P < 0.05), positioning this ratio as the best natural tag for reconstructing environmental histories of C. spixii. Change point analysis (CPA) based on otolith Sr/Ca signature through ontogeny revealed potential migrations between environments with different salinity. According to CPA, the number of displacements among different salinities ranged from 3–9 (6.1 ± 1.9), suggesting high plasticity in the migratory patterns. Ba/Ca, Li/Ca and Mn/Ca peaks were observed on the outer margin of the primordium, and could be influenced by physiological, environmental and maternal factors.

Keywords

AriidaeBrazilLA-ICP-MSlapilli otolithsmicrochemistrysubtropical environment
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 100 , Issue 5 , August 2020 , pp. 783 - 793
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albuquerque, CQ, Miekeley, N and Muelbert, JH (2010) Whitemouth croaker, Micropogonias furnieri, trapped in a freshwater coastal lagoon: a natural comparison of freshwater and marine influences on otolith chemistry. Neotropical Ichthyology 8, 311–320.CrossRefGoogle Scholar
Albuquerque, CQ, Miekeley, N, Muelbert, JH, Walther, BD and Jaureguizar, AJ (2012) Estuarine dependency in a marine fish evaluated with otolith chemistry. Marine Biology 159, 2229–2239.CrossRefGoogle Scholar
APHA (2017) Standard Methods for the Examination of Water and Wastewater (22nd edn). Washington, DC: American Public Health Association (APHA), the American Water Works Association (AWWA), and the Water Environment Federation (WEF).Google Scholar
Avigliano, E and Volpedo, AV (2013) Use of otolith strontium:calcium ratio as an indicator of seasonal displacements of the silverside (Odontesthes bonariensis) in a freshwater-marine environment. Marine and Freshwater Research 64, 746–751.CrossRefGoogle Scholar
Avigliano, E, Leisen, M, Romero, R, Carvalho, B, Velasco, G, Vianna, M, Barra, F and Volpedo, AV (2017 a) Fluvio-marine travelers from South America: cyclic amphidromy and freshwater residency, typical behaviors in Genidens barbus inferred by otolith chemistry. Fisheries Research 193, 184–194.CrossRefGoogle Scholar
Avigliano, E, Pisonero, J, Dománico, A, Sánchez, S and Volpedo, AV (2017 b) Migration and brackish environment use of Prochilodus lineatus (Characiformes: Prochilodontidae) inferred by Sr:Ca ratio transects of otolith. Neotropical Ichthyology 15, e170055. https://www.scielo.br/pdf/ni/v15n3/1982-0224-ni-15-03-e170055.pdfCrossRefGoogle Scholar
Avigliano, E, Miller, N and Volpedo, AV (2018) Silversides (Odontesthes bonariensis) reside within freshwater and estuarine habitats, not marine environments. Estuarine, Coastal and Shelf Science 205, 123–130.CrossRefGoogle Scholar
Avigliano, E, Carvalho, BM, Miller, N, Gironde, SC, Tombari, A, Limburg, KE and Volpedo, AV (2019) Fin spine chemistry as a non-lethal alternative to otoliths for stock discrimination in an endangered catfish. Marine Ecology Progress Series 614, 147–157.Google Scholar
Azevedo, JS, Fernandez, WS, Farias, LA, Fávaro, DTI and Braga, ES (2009) Use of Cathorops spixii as bioindicator of pollution of trace metals in the Santos Bay, Brazil. Ecotoxicology 18, 577–586.CrossRefGoogle ScholarPubMed
Azevedo, JS, Braga, ES, Silva de Assis, HC and Oliveira Ribeiro, CA (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.CrossRefGoogle ScholarPubMed
Barletta, M, Amaral, CS, Corrêa, MFM, Guebert, F, Dantas, DV, Lorenzi, L and Saint-Paul, U (2008) Factors affecting seasonal variations in demersal fish assemblages at an ecocline in a tropical-subtropical estuary. Journal of Fish Biology 73, 1314–1336.Google Scholar
Barletta, M, Lima, ARA, Costa, MF and Dantas, DV (2017) Estuarine ecoclines and the associated fauna: ecological information as the basis for ecosystem conservation. In Finkl, C and Makowski, C (eds), Coastal Wetlands: Alteration and Remediation, 21st Edn.Cham: Springer, pp. 479–512.CrossRefGoogle Scholar
Bittar, VT, Castello, BFL and Di Beneditto, APM (2008) Hábito alimentar do peixe-espada adulto, Trichiurus lepturus, na costa norte do Rio de Janeiro, sudeste do Brasil. Biotemas 21, 83–90.CrossRefGoogle Scholar
Bouchard, C, Thorrold, SR and Fortier, L (2015) Spatial segregation, dispersion and migration in early stages of polar cod Boreogadus saida revealed by otolith chemistry. Marine Biology 162, 855–868.CrossRefGoogle Scholar
Bradbury, IR, Campana, SE and Bentzen, P (2008) Otolith elemental composition and adult tagging reveal spawning site fidelity and estuarine dependency in rainbow smelt. Marine Ecology Progress Series 368, 255–268.CrossRefGoogle Scholar
Brown, RJ and Severin, KP (2009) Otolith chemistry analyses indicate that water Sr:Ca is the primary factor influencing otolith Sr:Ca for freshwater and diadromous fish but not for marine fish. Canadian Journal of Fisheries and Aquatic Sciences 66, 1790–1808.CrossRefGoogle Scholar
Burton, KW and Vigier, N (2011) Handbook of environmental isotope geochemistry. Handbook of Environmental Isotope Geochemistry 1–2, 1–951.Google Scholar
Campana, SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Marine Ecology Progress Series 188, 263–297.Google Scholar
Campana, SE (2014). Otolith elemental as a natural marker of fish stocks. In Cadrin, SX, Kerr, LA and Mariani, S (eds), Stock Identification Methods: Applications in Fishery Science, 2nd Edn. San Diego, CA: Academic Press, pp. 227–245.Google Scholar
Campana, SE, Chouinard, GA, Hanson, JM, Fréchet, A and Brattey, J (2000) Otolith elemental fingerprints as biological tracers of fish stocks. Fisheries Research 46, 343–357.Google Scholar
Catalán, IA, Alós, J, Díaz-Gil, C, Pérez-Mayol, S, Basterretxea, G, Morales-Nin, B and Palmer, M (2018) Potential fishing-related effects on fish life history revealed by otolith microchemistry. Fisheries Research 199, 186–195.CrossRefGoogle Scholar
Cattani, AP, Santos, LO, Spach, HL, Budel, BR and Gondim Guanais, JHD (2011) Avaliação da ictiofauna da fauna acompanhante da pesca do camarão sete-barbas do município de Pontal do Paraná, litoral do Paraná, Brasil. Boletim do Instituto de Pesca 37, 247–260.Google Scholar
Coffey, M, Dehairs, F, Collette, O, Luther, G, Church, T and Jickells, T (1997) The behaviour of dissolved barium in estuaries. Estuarine, Coastal and Shelf Science 45, 113–121.CrossRefGoogle Scholar
Dantas, DV, Barletta, M, Lima, ARA, de Assis Almeida Ramos, J, da Costa, MF and Saint-Paul, U (2012) Nursery habitat shifts in an estuarine ecosystem: patterns of use by sympatric catfish species. Estuaries and Coasts 35, 587–602.CrossRefGoogle Scholar
Dantas, DV, Barletta, M, de Assis Almeida Ramos, J, Lima, ARA and da Costa, MF (2013) Seasonal diet shifts and overlap between two sympatric catfishes in an estuarine nursery. Estuaries and Coasts 36, 237–256.CrossRefGoogle Scholar
Daros, FA, Spach, HL and Correia, AT (2016) Habitat residency and movement patterns of Centropomus parallelus juveniles in a subtropical estuarine complex. Journal of Fish Biology 88, 1796–1810.CrossRefGoogle Scholar
Denadai, M, Pombo, M, Santos, FB, Bessa, E, Ferreira, A and 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, 1–8.Google Scholar
Di Rienzo, JA, Casanoves, F, Balzarini, MG, Gonzalez, L, Tablada, M and Robledo, YCW (2011) InfoStat versión 2011. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. Available at http://www.Infostat.com.ar.Google Scholar
Dias, TH, Oliveira, J, Sanders, CJ, Carvalho, F, Sanders, LM, Machado, EC and Sá, F (2016) Radium isotope (223Ra, 224Ra, 226Ra and 228Ra) distribution near Brazil's largest port, Paranaguá Bay, Brazil. Marine Pollution Bulletin 111, 443–448.CrossRefGoogle Scholar
Dorval, E and Jones, CM (2005) Chemistry of surface waters: distinguishing fine-scale differences in sea grass habitats of Chesapeake Bay. Limnology Oceanography 50, 1073–1083.CrossRefGoogle Scholar
Dos Anjos, VE, da Machado, EC and Grassi, MT (2012) Biogeochemical behavior of arsenic species at Paranaguá Estuarine Complex, Southern Brazil. Aquatic Geochemistry 18, 407–420.CrossRefGoogle Scholar
dos Passos, AC, Contente, RF, Abbatepaulo, FV, Spach, HL, Vilar, CC, Joyeux, JC, Cartagena, BFC and Fávaro, LF (2013) Analysis of fish assemblages in sectors along a salinity gradient based on species, families and functional groups. Brazilian Journal of Oceanography 61, 251–264.CrossRefGoogle Scholar
Du Laing, G, Rinklebe, J, Vandecasteele, B, Meers, E and Tack, FMG (2009) Trace metal behaviour in estuarine and riverine floodplain soils and sediments: a review. Science of the Total Environment 407, 3972–3985.CrossRefGoogle ScholarPubMed
Duponchelle, F, Pouilly, M, Pécheyran, C, Hauser, M, Renno, JF, Panfili, J, Darnaude, AM, García-Vasquez, A, Carvajal-Vallejos, F, García-Dávila, C, Doria, C, Bérail, S, Donard, A, Sondag, F, Santos, RV, Nuñez, J, Point, D, Labonne, M and Baras, E (2016) Trans-Amazonian natal homing in giant catfish. Journal of Applied Ecology 53, 1511–1520.Google Scholar
Elsdon, TS and Gillanders, BM (2003) Relationship between water and otolith elemental concentrations in juvenile black bream Acanthopagrus butcheri. Marine Ecology Progress Series 260, 263–272.CrossRefGoogle Scholar
Elsdon, TS and Gillanders, BM (2005) Alternative life-history patterns of estuarine fish: barium in otoliths elucidates freshwater residency. Canadian Journal of Fisheries and Aquatic Sciences 62, 1143–1152.CrossRefGoogle Scholar
Elsdon, TS, Wells, BK, Campana, SE, Gillanders, BM, Jones, CM, Limburg, KE, Secor, DH, Thorrold, SR and Walther, BD (2008) Otolith chemistry to describe movements and life-history parameters of fishes: hypotheses, assumptions, limitations and inferences. Oceanography and Marine Biology: An Annual Review 46, 297–330.CrossRefGoogle Scholar
Freire, KMF and Pauly, D (2005) Richness of common names of Brazilian marine fishes and its effect on catch statistics. Journal of Ethnobiology 25, 279–296.CrossRefGoogle Scholar
Gauldie, RW, Thacker, CE, West, IF and Wang, L (1998) Movement of water in fish otoliths. Comparative Biochemistry and Physiology 120, 551–556.Google Scholar
Gillanders, B, Clarke, LM, Thorrold, SR and Conover, DO (2011) Population differences in otolith chemistry have a genetic basis in Menidia menidia. Canadian Journal of Fisheries and Aquatic Sciences 68, 105–114.Google Scholar
Graça Lopes, R, Tomás, ARG, Tutui, SLS, Severino Rodrigues, E and Puzzi, A (2002) Fauna acompanhante da pesca camaroeira no litoral do estado de São Paulo, Brasil. Boletim Do Instituto de Pesca 28, 173–188.Google Scholar
Jochum, KP, Weis, U, Stoll, B, Kuzmin, D, Yang, Q, Raczek, I, Jacob, DE, Stracke, A, Birbaum, K, Frick, DA, Günther, D and Enzweiler, J (2011) Determination of reference values for NIST SRM 610-617 glasses following ISO guidelines. Geostandards and Geoanalytical Research 35, 397–429.CrossRefGoogle Scholar
Jochum, KP, Scholz, D, Stoll, B, Weis, U, Wilson, SA, Yang, Q, Schwalb, A, Börner, N, Jacob, DE and Andreae, MO (2012) Accurate trace element analysis of speleothems and biogenic calcium carbonates by LA-ICP-MS. Chemical Geology 318–319, 31–44.Google Scholar
Kalish, J (1990) Use of otolith microchemistry to distinguish the progeny of sympatric anadromous and non-anadromous salmonids. Fishery Bulletin 88, 657–666.Google Scholar
Lana, PC, Marone, E, Lopes, RM and Machado, EC (2001) The subtropical estuarine complex of Paranaguá Bay, Brazil. Ecological Studies 144, 131–145.CrossRefGoogle Scholar
Li, YH and Chan, LH (1979) Desorption of Ba and 226Ra from river-borne sediments in the Hudson estuary. Earth and Planetary Science Letters 43, 343–350.CrossRefGoogle Scholar
Liberoff, AL, Miller, JA, Riva-Rossi, CM, Hidalgo, FJ, Fogel, ML, Pascual, MA and Tierney, K (2014) Transgenerational effects of anadromy on juvenile growth traits in an introduced population of rainbow trout (Oncorhynchus mykiss). Canadian Journal of Fisheries and Aquatic Sciences 71, 398–407.CrossRefGoogle Scholar
Lima, ARA, Barletta, M, Dantas, DV, Possatto, FE, Ramos, JAA and Costa, MF (2012) Early development and allometric shifts during the ontogeny of a marine catfish (Cathorops spixii – Ariidae). Journal of Applied Ichthyology 28, 217–225.CrossRefGoogle Scholar
Limburg, KE, Olson, C, Walther, Y, Dale, D, Slomp, CP and Hoie, H (2011) Tracking Baltic hypoxia and cod migration over millennia with natural tags. Proceedings of the National Academy of Sciences USA 108, 177–182.Google ScholarPubMed
Limburg, KE, Walther, BD, Lu, Z, Jackman, G, Mohan, J, Walther, Y, Nissling, A, Weber, PK and Schmitt, AK (2015) In search of the dead zone: use of otoliths for tracking fish exposure to hypoxia. Journal of Marine Systems 141, 167–178.CrossRefGoogle Scholar
Maciel, TR, Avigliano, E, Maichak de Carvalhoc, B, Miller, N and Viannaa, 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. https://doi.org/10.1016/j.ecss.2020.106839CrossRefGoogle Scholar
Marone, E, Machado, EC, Lopes, RM and and Silva, ET (2005) Land-ocean fluxes in the Paranaguá Bay Estuarine System, Southern Brazil. Brazilian Journal of Oceanography 53, 169–181.Google Scholar
Martin, P, Allen, JT, Cooper, MJ, Johns, DG, Lampitt, RS, Sanders, R and Teagle, DAH (2016) Sedimentation of acantharian cysts in the Iceland Basin: strontium as a ballast for deep ocean particle flux, and implications for acantharian reproductive strategies. Limnology and Oceanography 55, 604–614.CrossRefGoogle Scholar
Melo, SC and Teixeira, RL (1992) Distribuição, reprodução e alimentação de Cathorops spixii e Arius Rugispinis (Pisces: Ariidae) do Complexo Mundaú/Manguaba. Revista Brasileira de Biologia 52, 169–180.Google Scholar
Miotto, ML, De Carvalho, BM, Spach, HL and Barbieri, E (2017) Ictiofauna demersal na alimentação do gaivotão (Larus dominicanus) em um ambiente subtropical. Ornitologia Neotropical 28, 27–36.Google Scholar
Mizerkowski, BD, Hesse, K, Ladwig, N, Machado, EC, Rosa, R, Araújo, T and Koch, D (2012) Sources, loads and dispersion of dissolved inorganic nutrients in Paranaguá Bay. Ocean Dynamics 62, 1409–1424.CrossRefGoogle Scholar
Mohan, JA and Walther, BD (2015) Spatiotemporal variation of trace elements and stable isotopes in subtropical estuaries: II. Regional, local, and seasonal salinity-element relationships. Estuaries and Coasts 38, 769–781.CrossRefGoogle Scholar
Mohan, JA, Halden, NM and Rulifson, RA (2015) Habitat use of juvenile striped bass Morone saxatilis (Actinopterygii: Moronidae) in rivers spanning a salinity gradient across a shallow wind-driven estuary. Environmental Biology of Fishes 98, 1105–1116.Google Scholar
Morales-Nin, B (2000) Review of the growth regulation processes of otolith daily increment formation. Fisheries Research 46, 53–67.CrossRefGoogle Scholar
Panfili, J, Darnaude, AM, Lin, YJ, Chevalley, M, Iizuka, Y, Tzeng, WN and Crivelli, AJ (2012) Habitat residence during continental life of the European eel Anguilla anguilla investigated using linear discriminant analysis applied to otolith Sr:Ca ratios. Aquatic Biology 15, 175–185.CrossRefGoogle Scholar
Pearce, NJG, Perkins, WT, Westgate, JA, Gorton, MP, Jackson, SE, Neal, CR and Chenery, SP (1997) A compilation of new and published major and trace element data for NIST SRM 610 and NIST SRM 612 glass reference materials. Geostandards Newsletter 21, 115–144.CrossRefGoogle Scholar
Reis, EG (1986) Reproduction and feeding habits of the marine catfish, Netuma barba (Siluriformes, Ariidae), in the estuary of the Patos Lagoon (Brazil). Atlantica 8, 35–55.Google Scholar
Rocha, ML, Sá, F, Campos, MS, Grassi, MT, Combi, T and Machado, EC (2017) Metals impact into the Paranaguá Estuarine Complex (Brazil) during the exceptional flood of 2011. Brazilian Journal of Oceanography 65, 54–68.CrossRefGoogle Scholar
Rogers, TA, Fowler, AJ, Steer, MA and Gillanders, BM (2019) Discriminating natal source populations of a temperate marine fish using larval otolith chemistry. Frontiers in Marine Science 6, 1–17. https://doi.org/10.3389/fmars.2019.00711.CrossRefGoogle Scholar
Santos, LO, Cattani, AP and Spach, HL (2016) Ictiofauna acompanhante da pesca de arrasto para embarcações acima de 45 HP no litoral do Paraná, Brasil. Boletim Do Instituto de Pesca 42, 819–834.CrossRefGoogle Scholar
Shrimpton, JM, Warren, KD, Todd, NL, McRae, CJ, Glova, GJ, Telmer, KH and Clarke, AD (2014) Freshwater movement patterns by juvenile Pacific salmon Oncorhynchus spp. before they migrate to the ocean: Oh the places you'll go! Journal of Fish Biology 85, 987–1004.CrossRefGoogle ScholarPubMed
Tabouret, H, Bareille, G, Claverie, F, Pécheyran, C, Prouzet, P and Donard, OFX (2010) Simultaneous use of strontium:calcium and barium:calcium ratios in otoliths as markers of habitat: application to the European eel (Anguilla anguilla) in the Adour basin, South West France. Marine Environmental Research 70, 35–45.CrossRefGoogle ScholarPubMed
Tabouret, H, Lord, C, Bareille, G, Pécheyran, C, Monti, D and Keith, P (2011) Otolith microchemistry in Sicydium punctatum: indices of environmental condition changes after recruitment. Aquatic Living Resources 24, 369–378.CrossRefGoogle Scholar
UNESCO (1999). WHC Nomination Documentation. United Nations Educational, Scientific and Cultural Organization. Available at https://whc.unesco.org/uploads/nominations/893rev.pdf.Google Scholar
Walther, BD and Nims, MK (2015) Spatiotemporal variation of trace elements and stable isotopes in subtropical estuaries: I. Freshwater endmembers and mixing curves. Estuaries and Coasts 38, 754–768.CrossRefGoogle Scholar
Yoshinaga, J, Nakama, A, Morita, M and Edmonds, JS (2000) Fish otolith reference material for quality assurance of chemical analyses. Marine Chemistry 69, 91–97.CrossRefGoogle Scholar