Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-31T15:29:40.843Z Has data issue: false hasContentIssue false
  • English
  • Français

Inferring ecological connectivity between populations of Opsanus beta (Goode & Bean, 1880) from the southern Gulf of Mexico and the South-western Atlantic coast

Published online by Cambridge University Press:  01 December 2022

Barbara Maichak de Carvalho Open the ORCID record for Barbara Maichak de Carvalho [Opens in a new window] ,
José Antônio Martínez Pérez ,
Alfonso Aguilar-Perera Open the ORCID record for Alfonso Aguilar-Perera [Opens in a new window] ,
Virginia Noh Quiñones ,
Acácio Ribeiro Gomes Tomás ,
Jean Vitule  and
Alejandra Volpedo Open the ORCID record for Alejandra Volpedo [Opens in a new window]
Barbara Maichak de Carvalho*
Affiliation:
Programa de Pós-Graduação em Engenharia Ambiental, Departamento de Engenharia – UFPR, Laboratório de Ecologia e Conservação (LEC), Brazil
José Antônio Martínez Pérez
Affiliation:
Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Laboratorio de Zoología (L 221)
Alfonso Aguilar-Perera
Affiliation:
Departamento de Biología Marina Facultad de Medicina Veterinaria y Zootecnia Universidad Autónoma de Yucatán, México
Virginia Noh Quiñones
Affiliation:
Departamento de Biología Marina Facultad de Medicina Veterinaria y Zootecnia Universidad Autónoma de Yucatán, México
Acácio Ribeiro Gomes Tomás
Affiliation:
Laboratório de Estudos Estuarinos, Centro do Pescado Marinho, Instituto de Pesca, APTA-SAA, Santos, SP, Brazil
Jean Vitule
Affiliation:
Programa de Pós-Graduação em Engenharia Ambiental, Departamento de Engenharia – UFPR, Laboratório de Ecologia e Conservação (LEC), Brazil
Alejandra Volpedo
Affiliation:
CONICET-Universidad de Buenos Aires, Instituto de Investigaciones en Producción Animal (INPA)/Centro de Estudios Transdisciplinarios del Agua (CETA) Facultad de Ciencias Veterinarias Universidad de Buenos Aires, Ciudad Autónoma de Buenos Aires, Buenos Aires, Argentina
*
Author for correspondence: Barbara Maichak de Carvalho, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Otoliths are an excellent tool in studies on ecological connectivity of fish species populations. Opsanus beta is an invasive species introduced on the Brazilian coast, but not native from the Gulf of Mexico. The present study aimed to compare the otolith contours of specimens collected in Mexico (Celestún, CEL) and in two Brazilian estuaries (Santos Bay, STB, and Paranaguá Estuarine Complex, PEC). In the laboratory, 99 otoliths were extracted, photographed and compared using wavelet analysis. The otolith contours varied between sites (39 from CEL, 26 from STB and 34 from PEC). The linear discriminant analysis correctly reclassified 87.9% of otoliths by sites, with the best reclassifications in the CEL (97.36%), followed by PEC (88.23%) and SBT (73.07%). MANOVA showed significant differences in otolith contours between sites (F = 5.37; P < 0.005). The otolith contour from CEL was significantly different from those from the PEC and SBT. However, the otolith contour of the two Brazilian estuaries did not significantly differ among them (MANOVA, P > 0.005). Our results indicate O. beta populations on the Brazilian coast are connected, and probably isolated from the Mexican population.

Keywords

Ballast waterBatrachoididaebioinvasionestuariesGulf of Mexicoshape
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 102 , Issue 8 , December 2022 , pp. 597 - 603
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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

Abaad, M, Tuset, VM, Montero, D, Lombarte, A, Otero-Ferrer, JL and Haroun, R (2015) Phenotypic plasticity in wild marine fishes associated with fish-cage aquaculture. Hydrobiologia 765, 343–358.CrossRefGoogle Scholar
Almeida-Tubino, MFA, Salgado, FLK, Uehara, W, Utsunomia, R and Araújo, FG (2021) Opsanus beta (Goode & Bean, 1880) (Acanthopterygii: Batrachoididae), a non-indigenous toadfish in Sepetiba Bay, south-eastern Brazil. Journal of the Marine Biological Association of the United Kingdom 101, 1–9.Google Scholar
Blackburn, TM, Bellard, C and Ricciard, A (2019) Alien vs native species as drivers of recent extinctions. Frontiers in Ecology and the Environment 17, 1–5.CrossRefGoogle Scholar
Boltovskoy, D and Correa, N (2015) Ecosystem impacts of the invasive bivalve Limnoperna fortunei (golden mussel) in South America. Hydrobiologia 746, 81–95.CrossRefGoogle Scholar
Caires, RA, Pichler, HA, Spach, HL and Ignácio, JM (2007) Opsanus brasiliensis Rotundo, Spinelli & Zavalla-Camin, 2005 (Teleostei: Batrachoidiformes: Batrachoididae), a junior synonym of Opsanus beta (Goode & Bean, 1880), with notes on its occurrence in the Brazilian coast. Biota Neotropical 7, 1–6.Google Scholar
Capoccioni, F, Costa, C, Aguzzi, J, Menesatti, P, Lombarte, A and Ciccotti, E (2011) Ontogenetic and environmental effects on otolith shape variability in three Mediterranean European eel (Anguilla anguilla, L.) local stocks. Journal of Experimental Marine Biology and Ecology 397, 1–7.CrossRefGoogle Scholar
Carvalho, BM, Ferreira Junior, AL, Fávaro, LF, Artoni, RF and Vitule, JRS (2020) Human facilitated dispersal of the gulf toadfish Opsanus beta (Goode & Bean, 1880) in the Guaratuba Bay, southeastern Brazil. Journal of Fish Biology 97, 1–5.CrossRefGoogle Scholar
Carvalho, BM, Freitas, MO, Lapuch, I, Volpedo, AV and Vitule, JRS (2022) Age, growth, and ontogenetic variation in the sagitta otolith of Opsanus beta (Goode & Bean, 1880), a non-native species in a wetland of international importance. Latin American Journal of Aquatic Research 50, 1–11.CrossRefGoogle Scholar
Castro, MCT, Fileman, TW and Hall-Spencer, JM (2016) Invasive species in the Northeastern and Southwestern Atlantic Ocean: a review. Marine Pollution Bulletin 116, 1–7.Google Scholar
Cerna, F, Saavedra-Nievas, JC, Plaza-Pasten, G, Niklitschek, E and Morales-Nin, B (2019) Ontogenetic and intraspecific variability in otolith shape of anchoveta (Engraulis ringens) used to identify demographic units in the Pacific Southeast off Chile. Marine and Freshwater Research 70, 1794–1804.CrossRefGoogle Scholar
Collette, BB (2002) Batrachoididae. In Carpenter, KE (ed.), The Living Marine Resources of the Western Central Atlantic. v. 2: Bony Fishes Part 1 (Acipenseridae to Grammatidae), vol. 5. Norfolk, Virginia, USA: FAO Species Identification Guide for Fishery Purposes (American Society of Ichthyologists and Herpetologists Special Publication), pp. 1026–1042.Google Scholar
Contente, RF, Brenha-Nunes, MR, Siliprandi, CC, Lamas, RA and Conversani, VRM (2015) Occurrence of the non-indigenous Omobranchus punctatus (Blenniidae) on the São Paulo coast, south-eastern Brazil. Marine Biodiversity Records 8, 1–4.CrossRefGoogle Scholar
Cordeiro, BD, Bertoncini, AA, Abrunhosa, FE, Corona, LS, Araújo, FG and Santos, LN (2020) First report of the aliengulf toadfish Opsanus beta (Goode & Bean, 1880) on the coast of Rio de Janeiro – Brazil. BioInvasions Records 9, 1–8.CrossRefGoogle Scholar
Cutrim, SS, Robles, LT, Galvão, CB and Casaca, AC (2017) Domestic short sea shipping services in Brazil: competition by enhancing logistics integration. International Journal of Shipping and Transport Logistic 9, 280–303.CrossRefGoogle Scholar
Dimitriou, AC, Chartosia, N, Hall-Spencer, JM, Kleitou, P, Jimenez, C, Antoniou, C, Hadjioannou, L, Kletou, D and Sfenthourakis, S (2019) Genetic data suggest multiple introductions of the lionfish (Pterois miles) into the Mediterranean Sea. Diversity 11, 1–12.CrossRefGoogle Scholar
Encarnação, J, Teodósio, MA and Morais, P (2021) Citizen science and biological invasions: a review. Frontiers in Environmental Science 8, 1–14.CrossRefGoogle Scholar
Franco-López, J, González, AGS, Arenas, LGA, Sánchez, CB, Escorcia, HB, Pérez, JAM, Rodríguez, EP and Legorreta, JLV (2017) Ecología y reproducción de Opsanus beta (Actinopterygii: Batrachoididae) en la Laguna de Alvarado, Veracruz, México. Revista de Biologia Tropical 65, 1381–1396.CrossRefGoogle Scholar
Gallardo-Torres, A, Martinez-Perez, JA and Lezina, BJ (2004) Reproductive structures and early life history of the gulf toadfish, Opsanus beta, in the Tecolutla estuary, Veracruz, Mexico. Gulf and Caribbean Research 16, 109–113.CrossRefGoogle Scholar
Gauldie, RW and Crampton, JS (2002) An eco-morphological explanation of individual variability in the shape of the fish otolith: comparison of the otolith of Hoplostethus atlanticus with other species by depth. Journal of Fish Biology 60, 1204–1221.CrossRefGoogle Scholar
Greenfield, DW, Winterbottom, R and Collette, BB (2008) Review of the toadfish genera (Teleostei: Batrachoididae). Proceedings of the California Academy of Sciences 59, 665–710.Google Scholar
Gutiérrez-Mendieta, FJ and Lanza Espino, GL (2019) Physicochemical characterization of Mexican coastal lagoons, current status, and future environmental scenarios. In Mexican Aquatic Environments, pp. 77–91. https://doi.org/10.1007/978-3-030-11126-7_3CrossRefGoogle Scholar
Hoff, NT, Dias, JF, Zani-Teixeira, ML and Correia, AT (2020) Spatio-temporal evaluation of the population structure of the bigtooth corvina Isopisthus parvipinnis from Southwest Atlantic Ocean using otolith shape signatures. Journal of Applied Ichthyology 36, 1–12.CrossRefGoogle Scholar
Ibañez, AL, Hernández-Fraga, K and Alvarez-Hernández, S (2017) Discrimination analysis of phenotypic stocks comparing fish otolith and scale shapes. Fisheries Research 185, 6–13.CrossRefGoogle Scholar
Kikuchi, E, Cardoso, LG, Canel, D, Timi, JT and Haimovici, M (2021) Using growth rates and otolith shape to identify the population structure of Umbrina canosai (Sciaenidae) from the Southwestern Atlantic. Marine Biology Research 17, 272–285.CrossRefGoogle Scholar
Lana, PC, Marone, E, Lopes, RM and Machado, EC (2001) The subtropical estuarine complex of Paranaguá Bay, Brazil. In Seeliger, U and Kjerfve, B (eds), Coastal Marine Ecosystems of Latin America, Ecological Studies, vol. 144. Berlin: Springer-Verlag, pp. 131–145.CrossRefGoogle Scholar
Lasso-Alcalá, O, Nunes, JLS, Lasso, C, Posada, J, Robertson, R, Piorski, NM, Tassell, JV, Giarrizzo, T and Gondolo, G (2011) Invasion of the Indo-Pacific blenny Omobranchus punctatus (Perciformes: Blenniidae) on the Atlantic Coast of Central and South America. Neotropical Ichthyology 9, 571–578.CrossRefGoogle Scholar
Lessa, GC, Santos, FM, Filho, PWS and Corrêa-Gomes, LC (2018) Brazilian estuaries: a geomorphologic and oceanographic perspective. In Lana, PC and Bernardino, AF (eds), Brazilian Estuaries: A Benthic Perspective. Berlin: Springer, pp. 1–38.Google Scholar
Lombarte, A and Tuset, VM (2015) Morfometria de otólitos. In Volpedo, A and Vaz-dos-Santos, AM (eds), Métodos de Estudos com Otólitos: Princípios e Aplicações. Buenos Aires: CAFP-BA-PIESCI, pp. 1–12.Google Scholar
Maciel, TR, Vianna, M, Carvalho, BM, Miller, N and Avigliano, E (2021) Integrated use of otolith shape and microchemistry to assess Genidens barbus fish stock structure. Estuarine, Coastal and Shelf Science 261, 1–9.Google Scholar
Malca, E, Barimo, JF, Serafy, JE and Walsh, PJ (2009) Age and growth of the gulf toadfish Opsanus beta based on otolith increment analysis. Journal of Fish Biology 75, 1750–1761.CrossRefGoogle ScholarPubMed
Mallat, S (1991) Zero crossings of a wavelet transform. IEEE Transactions on Information Theory 37, 1019–1033.CrossRefGoogle 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
Morissette, O and Whitledge, GW (2022) Listening with the invasive fish ear: applications and innovations of otolith chemistry analysis in invasive fish biology. Environmental Biology of Fishes 105, 1–17.CrossRefGoogle Scholar
Ojaveer, H, Galil, BS, Carlton, JT, Alleway, H, Goulletquer, P, Lehtiniemi, M and Zaiko, A (2018) Historical baselines in marine bioinvasions: implications for policy and management. PLoS ONE 13, 1–49.CrossRefGoogle ScholarPubMed
Olenin, S, Gollasch, S, Lehtiniemi, M, Sapota, M and Zaiko, A (2017) Biological invasions. In Snoeijs-Leijonmalm, P (ed.), Biological Oceanography of the Baltic Sea. Dordrech: Springer Science Business Media, pp. 1–40.Google Scholar
Parisi-Baradad, V, Manjabacas, A, Lombarte, A, Olivella, R, Chic, Ò, Piera, J and García-Ladona, E (2010) Automatic taxon identification of teleost fishes in an otolith online database. Fisheries Research 105, 13–20.CrossRefGoogle Scholar
Popper, AN and Fay, RR (2011) Rethinking sound detection by fishes. Hearing Research 273, 25–36.CrossRefGoogle ScholarPubMed
Porcaro, RR, Zani-Teixeira, ML, Katsuragawa, M, Namiki, C, Ohkawara, MH and Favero, JM (2014) Spatial and temporal distribution patterns of larval sciaenids in the estuarine system and adjacent continental shelf off Santos, Southeastern Brazil. Brazilian Journal of Oceanography 62, 149–164.CrossRefGoogle Scholar
Richardson, DM, Pysek, P, Rejmánek, M, Barbour, MG, Panetta, FD and West, CJ (2000) Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 6, 93–107.CrossRefGoogle Scholar
Sadighzadeh, Z, Valinassa, T, Vosugi, G, Motallebi, AA, Fatemi, MR, Lombarte, A and Tuset, VM (2014) Use of otolith shape for stock identification of John's 74 snapper, Lutjanus johnii (Pisces: Lutjanidae), from the Persian Gulf and the Oman Sea. Fisheries Research 155, 59–63.CrossRefGoogle Scholar
Schulz-Mirbach, T, Ladich, F, Plath, M and Heb, M (2019) Enigmatic ear stones: what we know about the functional role and evolution of fish otoliths. Biological Reviews 94, 457–482.CrossRefGoogle ScholarPubMed
Soeth, M, Spach, HL, Daros, FA, Adelir-Alves, J, Almeida, ACO and Correia, AT (2019) Stock structure of Atlantic spadefish Chaetodipterus faber from Southwest Atlantic Ocean inferred from otolith elemental and shape signatures. Fisheries Research 211, 81–90.CrossRefGoogle Scholar
Spalding, MD, Fox, HE, Allen, GR, Davidson, N, Ferdaña, ZA, Finlayson, M, Halpern, BS, Jorge, MA, Lombana, A, Lourie, SA, Martin, KD, Mcmanus, E, Molnar, J, Recchia, CA and Robertson, J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57, 573–584.CrossRefGoogle Scholar
Stransky, C and Maclellan, SE (2005) Species separation and zoogeography of redfish and rockfish (genus Sebastes) by otolith shape analysis. Canadian Journal of Fisheries and Aquatic Sciences 62, 2265–2276.CrossRefGoogle Scholar
Tempesti, J, Mangano, MC, Langeneck, JL, Lardicci, C, Maltagliati, F and Castelli, A (2020) Non-indigenous species in Mediterranean ports: a knowledge baseline. Marine Environmental Research 161, 1–12.CrossRefGoogle Scholar
Tomás, ARG, Tutui, SLS, Fagundes, L and Souza, MR (2012) Opsanus beta: an invasive fish species in the Santos estuary, Brazil. Boletim do Instituto de Pesca 38, 349–355.Google Scholar
Tuset, VM, Imondi, R, Aguado, G, Otero-Ferrer, JL, Santschi, L, Lombarte, A and Love, M (2015) Otolith Patterns of Rockfishes from the Northeastern Pacific. Journal of Morphology 276, 458–469.CrossRefGoogle ScholarPubMed
Tuset, VM, Otero-Ferrer, JL, Omez-Zurita, JG, Venerus, LA, Stransky, C, Imondi, R, Orlov, AM, Ye, Z, Santschi, L, Afanasie, PK, Zhuang, L, Farré, M, Love, MS and Lombarte, A (2016) Otolith shape lends support to the sensory drive hypothesis in rockfishes. Journal of Evolutionary Biology 29, 2083–2097.CrossRefGoogle Scholar
Vignon, M and Morat, F (2010) Environmental and genetic determinant of otolith shape revealed by a non-indigenous tropical fish. Marine Ecolology Progress Series 411, 231–241.CrossRefGoogle Scholar
Vitule, JRS, Occhi, TVT, Kang, B, Matsuzaki, SI, Bezerra, LA, Daga, VS and Padial, AA (2019) Intra-country introductions unraveling global hotspots of alien fish species. Biodiversity and Conservation 28, 3037–3043.CrossRefGoogle Scholar
Watkins, HV, Yan, HF, Dunic, JC and Côté, IM (2021) Research biases create overrepresented “poster children” of marine invasion ecology. Conservation Letters 14, 13.CrossRefGoogle Scholar
Wonham, MJ, Carlton, JT, Smith, DJ and College, W (2000) Fish and ships: relating dispersal frequency to success in biological invasions. Marine Biology 136, 1111–1121.CrossRefGoogle Scholar