Can the introduction of non-native fish induce variation in life-history traits of a native species in a neotropical lake?
Thaís Paula de Araújo A B , Ludmila Silva Brighenti A , Bárbara Martins Dolabela C , Sérvio Pontes Ribeiro C , Hélio Batista dos Santos B and Ralph Gruppi Thomé B *A Universidade do Estado de Minas Gerais, Unidade Divinópolis, Avenida Paraná, no. 3001, Jardim Belvedere, CEP: 35501170, Divinópolis, MG, Brazil.
B Laboratório de Processamento de Tecidos (LAPROTEC), Universidade Federal de São João Del-Rei, Campus Centro-Oeste, Rua Sebastião Gonçalves Coelho, no. 400, Chanadour, CEP: 35501296, Divinópolis, MG, Brazil.
C Laboratório de Ecohealth, Insetos de Dossel e Sucessão Natural, NUPEB – Universidade Federal de Ouro Preto, Campus Morro do Cruzeiro, CEP: 35400000 Ouro Preto, MG, Brazil.
Marine and Freshwater Research 73(5) 651-661 https://doi.org/10.1071/MF21138
Submitted: 13 May 2021 Accepted: 21 November 2021 Published: 18 February 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Abstract
Top predator fish, such as peacock bass (Cichla kelberi) and red-bellied piranha (Pygocentrus nattereri), were introduced in the lacustrine system of the Rio Doce basin and these introductions are associated with loss of aquatic biodiversity. The present work aims to investigate the life-history traits of a native species, thraira (Hoplias malabaricus), in the context of the pressures caused by the introduction of top predator fishes. Two lakes were selected in a conservation unit Doce River State Park (PERD), namely, Lake Carioca, where P. nattereri and C. kelberi were introduced, and Lake Gambazinho, where H. malabaricus occurs in the absence of introduced fish. In total, 146 specimens of H. malabaricus were caught, including 95 in Lake Gambazinho and 51 in Lake Carioca. Significant differences were found in the length–weight relationship (LWR) in the diet, the reproductive period, the vitellogenic follicle size, and the gonadosomatic index (GSI). In the lake with introduced species, thrairas showed allometric growth, a less diversified diet, longer duration of the reproductive period, and high GSI values compared with the control lake. The results indicated that the life-history traits of thrairas can be influenced by the environmental modification caused by the introduction of non-native peacock bass and red-bellied piranha.
Keywords: Biological invasions, conservation units, diet, gonadosomatic index, Hoplias, length–weight relationship, predation, reproduction.
References
Alix, M, Kjesbu, OS, and Anderson, KC (2021). From gametogenesis to spawning: how climate-driven warming affects teleost reproductive biology. Journal of Fish Biology 97, 607–632.| From gametogenesis to spawning: how climate-driven warming affects teleost reproductive biology.Crossref | GoogleScholarGoogle Scholar |
Anson, JR, Dickman, CR, Boonstra, R, and Jessop, TS (2013). Stress triangle: do introduced predators exert indirect costs on native predators and prey? PLoS One 8, e60916.
| Stress triangle: do introduced predators exert indirect costs on native predators and prey?Crossref | GoogleScholarGoogle Scholar | 23585861PubMed |
Barros, NHC, Lima, LTB, Araújo, AS, Gurgel, LL, Chellappa, NT, and Chellappa, S (2016). Estudos sobre as táticas e as estratégias reprodutivas de sete espécies de peixes de água doce do Rio Grande de Norte, Brasil. Holos 3, 84–103.
| Estudos sobre as táticas e as estratégias reprodutivas de sete espécies de peixes de água doce do Rio Grande de Norte, Brasil.Crossref | GoogleScholarGoogle Scholar |
Bellard, C, Cassey, P, and Blackburn, TM (2016). Alien species as a driver of recent extinctions. Biology Letters 12, 20150623.
| Alien species as a driver of recent extinctions.Crossref | GoogleScholarGoogle Scholar | 26888913PubMed |
Bezerra-Neto, JF, Briguenti, LS, and Pinto-Coelho, RM (2010). A new morphometric study of Carioca Lake, Parque Estadual do Rio Doce (PERD), Minas Gerais State, Brazil. Acta Scientiarum. Biological Sciences 32, 49–54.
| A new morphometric study of Carioca Lake, Parque Estadual do Rio Doce (PERD), Minas Gerais State, Brazil.Crossref | GoogleScholarGoogle Scholar |
Bizzott, PM, and Godinho, HP (2007). Morphometric evaluation of the spermatogenesis in trahira Hoplias malabaricus (Bloch) (Characiformes, Erythrinidae). Revista Brasileira de Zoologia 24, 541–544.
| Morphometric evaluation of the spermatogenesis in trahira Hoplias malabaricus (Bloch) (Characiformes, Erythrinidae).Crossref | GoogleScholarGoogle Scholar |
Brown-Peterson, NJ, Wyanski, DM, Saborido-Rey, F, Macewicz, BJ, and Lowerre-Barbieri, SK (2011). A standardized terminology for describing reproductive development in fishes. Marine and Coastal Fisheries 3, 52–70.
| A standardized terminology for describing reproductive development in fishes.Crossref | GoogleScholarGoogle Scholar |
Caramaschi, EP, Godinho, HM, and Foresti, F (1982). Reprodução de Hoplias malabaricus (Bloch, 1794) (Teleostei, Erythrinidae) na represa do Rio Pardo (Botucatu, SP). I Histologia e escala de maturação do ovário. Revista Brasileira de Biologia 42, 635–640.
Carvalho, LN, Fernandes, CHV, and Moreira, VSS (2002). Alimentação de Hoplias malabaricus (Bloch, 1794) (Osteichthyes, Erythrinidae) no rio Vermelho, Pantanal Sul Mato-Grossense. Revista Brasileira de Zoociências 4, 227–236.
Chellappa, S, Bueno, RM, Chellappa, T, Chellappa, NT, and Val, VMFA (2009). Reproductive seasonality of the fish fauna and limnoecology of semi-arid Brazilian reservoirs. Limnologica 39, 325–329.
| Reproductive seasonality of the fish fauna and limnoecology of semi-arid Brazilian reservoirs.Crossref | GoogleScholarGoogle Scholar |
Coleman, RM, and Galvani, AP (1998). Egg size determines offspring size in neotropical cichlid fishes (Teleostei: Cichlidae). Copeia 1998, 209–213.
| Egg size determines offspring size in neotropical cichlid fishes (Teleostei: Cichlidae).Crossref | GoogleScholarGoogle Scholar |
Costa Lima, MC, de Lira, RD, Barros, NHC, Nascimento, WS, and Chellappa, S (2017). Biologia reprodutiva do peixe traíra, Hoplias malabaricus (Bloch, 1794) (Characiformes: Erythrinidae) no açude Marechal Dutra, Rio Grande do Norte, Brasil. Biota Amazônia 7, 21–25.
| Biologia reprodutiva do peixe traíra, Hoplias malabaricus (Bloch, 1794) (Characiformes: Erythrinidae) no açude Marechal Dutra, Rio Grande do Norte, Brasil.Crossref | GoogleScholarGoogle Scholar |
Dergam, JA, Paiva, SR, Schaeffer, CE, Godinho, AL, and Vieira, F (2002). Phylogeography and RAPD-PCR variation in Hoplias malabaricus (Bloch, 1794) (Pisces, Teleostei) in southeastern Brazil. Genetics and Molecular Biology 25, 379–387.
de Winter, JC (2013). Using the Student’s t-test with extremely small sample sizes. Practical Assessment, Research, and Evaluation 18, 1–12.
| Using the Student’s t-test with extremely small sample sizes.Crossref | GoogleScholarGoogle Scholar |
Fonseca-Silva, FM, Carvalho, MA, and Ribeiro, SP (2015). Caracterização da matéria orgânica particulada dos últimos 10 mil anos a partir de um testemunho do Parque Estadual do Rio Doce, MG, Brasil: implicações paleoambientais. Revista Brasileira de Paleontologia 18, 161–170.
| Caracterização da matéria orgânica particulada dos últimos 10 mil anos a partir de um testemunho do Parque Estadual do Rio Doce, MG, Brasil: implicações paleoambientais.Crossref | GoogleScholarGoogle Scholar |
Fontoura, NF, Ceni, G, Braun, A, and Marques, CDS (2018). Defining the reproductive period of freshwater fish species using the Gonadosomatic Index: a proposed protocol applied to ten species of the Patos Lagoon basin. Neotropical Ichthyology 16, e170006.
| Defining the reproductive period of freshwater fish species using the Gonadosomatic Index: a proposed protocol applied to ten species of the Patos Lagoon basin.Crossref | GoogleScholarGoogle Scholar |
Fragoso-Moura, EN, Oporto, LT, Maia-Barbosa, PM, and Barbosa, FAR (2016). Loss of biodiversity in a conservation unit of the Brazilian Atlantic Forest: the effect of introducing non-native fish species. Brazilian Journal of Biology 76, 18–27.
| Loss of biodiversity in a conservation unit of the Brazilian Atlantic Forest: the effect of introducing non-native fish species.Crossref | GoogleScholarGoogle Scholar |
Glantz AS (2014) ‘Princípios de bioestatística,’ 7th edn. (AMGH: Porto Alegre, Brazil)
Gomes, BVC, Scarpelli, RS, Arantes, FP, Sato, Y, Bazzoli, N, and Rizzo, E (2007). Comparative oocyte morphology and early development in three species of trahiras from the São Francisco River basin, Brazil. Journal of Fish Biology 70, 1412–1429.
| Comparative oocyte morphology and early development in three species of trahiras from the São Francisco River basin, Brazil.Crossref | GoogleScholarGoogle Scholar |
Gomes, ADO, Tolussi, CES, Ribeiro, C, Honji, RM, and Moreira, RG (2015). The role of ovarian steroids in reproductive plasticity in Hoplias malabaricus (Teleostei: Characiformes: Erythrinidae) in tropical reservoirs with different degrees of pollution. General and Comparative Endocrinology 222, 1–10.
| The role of ovarian steroids in reproductive plasticity in Hoplias malabaricus (Teleostei: Characiformes: Erythrinidae) in tropical reservoirs with different degrees of pollution.Crossref | GoogleScholarGoogle Scholar |
Gozlan, RE, Britton, JR, Cowx, I, and Copp, GH (2010). Current knowledge on non‐native freshwater fish introductions. Journal of Fish Biology 76, 751–786.
| Current knowledge on non‐native freshwater fish introductions.Crossref | GoogleScholarGoogle Scholar |
Latini, AO, and Petrere, M (2004). Reduction of a native fish fauna by alien species: an example from Brazilian freshwater tropical lakes. Fisheries Management and Ecology 11, 71–79.
| Reduction of a native fish fauna by alien species: an example from Brazilian freshwater tropical lakes.Crossref | GoogleScholarGoogle Scholar |
Lubzens, E, Young, G, Bobe, J, and Cerdà, J (2010). Oogenesis in teleosts: how fish eggs are formed. General and Comparative Endocrinology 165, 367–389.
| Oogenesis in teleosts: how fish eggs are formed.Crossref | GoogleScholarGoogle Scholar | 19505465PubMed |
Magalhães, AL, Daga, VS, Bezerra, LA, Vitule, JR, Jacobi, CM, and Silva, LG (2020). All the colors of the world: biotic homogenization−differentiation dynamics of freshwater fish communities on demand of the Brazilian aquarium trade. Hydrobiologia 847, 3897–3915.
| All the colors of the world: biotic homogenization−differentiation dynamics of freshwater fish communities on demand of the Brazilian aquarium trade.Crossref | GoogleScholarGoogle Scholar |
Marques, DKS, Gurgel, HDCB, and de Lucena, I (2001). Época de reprodução de Hoplias malabaricus Bloch, 1794 (Osteichthyes, Erythrinidae) da barragem do rio Gramame, Alhandra, Paraíba, Brasil. Revista Brasileira de Zoociências 3, 61–67.
McBride, RS, Somarakis, S, Fitzhugh, GR, Albert, A, Yaragina, NA, Wuenschel, MJ, Alonso-Fernandez, A, and Basilone, G (2015). Energy acquisition and allocation to egg production in relation to fish reproductive strategies. Fish and Fisheries 16, 23–57.
| Energy acquisition and allocation to egg production in relation to fish reproductive strategies.Crossref | GoogleScholarGoogle Scholar |
Montenegro, AKA, Vieira, ACB, Cardoso, MML, Souza, JERTD, and Crispim, MC (2013). Piscivory by Hoplias aff. malabaricus (Bloch, 1794): a question of prey availability? Acta Limnologica Brasiliensia 25, 68–78.
| Piscivory by Hoplias aff. malabaricus (Bloch, 1794): a question of prey availability?Crossref | GoogleScholarGoogle Scholar |
Murua, H, Kraus, G, Saborido-Rey, F, Witthames, PRPR, Thorsen, A, and Junquera, S (2003). Procedures to estimate fecundity of marine fish species from field samples in relation to reproductive strategy. Journal of Northwest Atlantic Fishery Science 33, 33–54.
Myers, N, Mittermeier, RA, Mittermeier, CG, Da Fonseca, GA, and Kent, J (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
| Biodiversity hotspots for conservation priorities.Crossref | GoogleScholarGoogle Scholar | 10706275PubMed |
Nakazawa, T, Ishida, N, Kato, M, and Yamamura, N (2007). Larger body size with higher predation rate. Ecology of Freshwater Fish 16, 362–372.
| Larger body size with higher predation rate.Crossref | GoogleScholarGoogle Scholar |
Paugy, D (2002). Reproductive strategies of fishes in a tropical temporary stream of the Upper Senegal basin: Baoulé River in Mali. Aquatic Living Resources 15, 25–35.
| Reproductive strategies of fishes in a tropical temporary stream of the Upper Senegal basin: Baoulé River in Mali.Crossref | GoogleScholarGoogle Scholar |
Pelicice, FM, and Agostinho, AA (2009). Fish fauna destruction after the introduction of a non-native predator (Cichla kelberi) in a Neotropical reservoir. Biological Invasions 11, 1789–1801.
| Fish fauna destruction after the introduction of a non-native predator (Cichla kelberi) in a Neotropical reservoir.Crossref | GoogleScholarGoogle Scholar |
Pelicice, FM, Latini, JD, and Agostinho, AA (2015). Fish fauna disassembly after the introduction of a voracious predator: main drivers and the role of the invader’s demography. Hydrobiologia 746, 271–283.
| Fish fauna disassembly after the introduction of a voracious predator: main drivers and the role of the invader’s demography.Crossref | GoogleScholarGoogle Scholar |
Pompeu, PDS, and Godinho, AL (2001). Mudança na dieta da traíra Hoplias malabaricus (Bloch) (Erythrinidae, Characiformes) em lagoas da bacia do rio Doce devido à introdução de peixes piscívoros. Revista Brasileira de Zoologia 18, 1219–1225.
| Mudança na dieta da traíra Hoplias malabaricus (Bloch) (Erythrinidae, Characiformes) em lagoas da bacia do rio Doce devido à introdução de peixes piscívoros.Crossref | GoogleScholarGoogle Scholar |
Pinto-Coelho, RM, Bezerra-Neto, JF, Miranda, F, Mota, TG, Resck, R, Santos, AM, Maia-Barbosa, PM, Mello, NAST, Marques, MM, Campos, MO, and Barbosa, FAR (2008). The inverted trophic cascade in tropical plankton communities: impacts of exotic fish in the Middle Rio Doce lake district, Minas Gerais, Brazil. Brazilian Journal of Biology 68, 1025–1037.
| The inverted trophic cascade in tropical plankton communities: impacts of exotic fish in the Middle Rio Doce lake district, Minas Gerais, Brazil.Crossref | GoogleScholarGoogle Scholar |
Poot-López, GR, Arce-Ibarra, AM, Elías-Gutiérrez, M, and Cervantes‐Martínez, A (2009). Differences in reproductive seasonality of the Central American cichlid Cichlasoma urophthalmus from three ‘cenotes’ (sinkholes). Journal of Applied Ichthyology 25, 85–90.
| Differences in reproductive seasonality of the Central American cichlid Cichlasoma urophthalmus from three ‘cenotes’ (sinkholes).Crossref | GoogleScholarGoogle Scholar |
Prado, CPA, Gomiero, LM, and Froehlich, O (2006). Spawning and parental care in Hoplias malabaricus (Teleostei, Characiformes, Erythrinidae) in the southern Pantanal, Brazil. Brazilian Journal of Biology 66, 697–702.
| Spawning and parental care in Hoplias malabaricus (Teleostei, Characiformes, Erythrinidae) in the southern Pantanal, Brazil.Crossref | GoogleScholarGoogle Scholar |
Rickter, WE (1973). Linear regressions in fisheries research. Journal of Fisheries Board of Canada 30, 409–434.
| Linear regressions in fisheries research.Crossref | GoogleScholarGoogle Scholar |
Rizzo E, Bazzoli N (2020) Reproduction and embryogenesis. In ‘Biology and physiology of freshwater neotropical fish’. (Eds B Baldisserotto, EC Urbinati, J Cyrino) pp. 287–313. (Academic Press: London, UK)
Royce WF (1972) ‘Introduction to the fishery science’, (Academic Press: New York, NY, USA)
Santos, HB, Thomé, RG, Arantes, FP, Sato, Y, Bazzoli, N, and Rizzo, E (2008). Ovarian follicular atresia is mediated by heterophagy, autophagy, and apoptosis in Prochilodus argenteus and Leporinus taeniatus (Teleostei: Characiformes). Theriogenology 70, 1449–1460.
| Ovarian follicular atresia is mediated by heterophagy, autophagy, and apoptosis in Prochilodus argenteus and Leporinus taeniatus (Teleostei: Characiformes).Crossref | GoogleScholarGoogle Scholar | 18701155PubMed |
Schreck, CB, Contreras-Sanchez, W, and Fitzpatrick, MS (2001). Effects of stress on fish reproduction, gamete quality, and progeny. Reproductive Biotechnology in Finfish Aquaculture 197, 3–24.
| Effects of stress on fish reproduction, gamete quality, and progeny.Crossref | GoogleScholarGoogle Scholar |
Sharpe, DMT, De León, LF, González, R, and Torchin, ME (2017). Tropical fish community does not recover 45 years after predator introduction. Ecology 98, 412–424.
| Tropical fish community does not recover 45 years after predator introduction.Crossref | GoogleScholarGoogle Scholar |
Spurgeon, JJ, Paukert, CP, Healy, BD, Kelley, CA, and Whiting, DP (2015). Can translocated native fishes retain their trophic niche when confronted with a resident invasive? Ecology of Freshwater Fish 24, 456–466.
| Can translocated native fishes retain their trophic niche when confronted with a resident invasive?Crossref | GoogleScholarGoogle Scholar |
Strecker, U (2006). The impact of invasive fish on an endemic Cyprinodon species flock (Teleostei) from Laguna Chichancanab, Yucatan, Mexico. Ecology of Freshwater Fish 15, 408–418.
| The impact of invasive fish on an endemic Cyprinodon species flock (Teleostei) from Laguna Chichancanab, Yucatan, Mexico.Crossref | GoogleScholarGoogle Scholar |
Sunaga, T, and Verani, JR (1991). The fish communities of the lakes in Rio Doce Valley, Northeast Brazil. SIL Proceedings, 1922-2010 24, 2563–2566.
| The fish communities of the lakes in Rio Doce Valley, Northeast Brazil.Crossref | GoogleScholarGoogle Scholar |
Tarkan, AS, Gaygusuz, Ö, Gürsoy Gaygusuz, Ç, Saç, G, and Copp, GH (2012). Circumstantial evidence of gibel carp, Carassius gibelio, reproductive competition exerted on native fish species in a mesotrophic reservoir. Fisheries Management and Ecology 19, 167–177.
| Circumstantial evidence of gibel carp, Carassius gibelio, reproductive competition exerted on native fish species in a mesotrophic reservoir.Crossref | GoogleScholarGoogle Scholar |
Teixeira de Mello, F, Iglesias, C, Borthagaray, AI, Mazzeo, N, Vilches, J, Larrea, D, and Ballabio, R (2006). Ontogenetic allometric coefficient changes: implications of diet shift and morphometric traits in Hoplias malabaricus (Bloch) (Characiforme, Erythrinidae). Journal of Fish Biology 69, 1770–1778.
| Ontogenetic allometric coefficient changes: implications of diet shift and morphometric traits in Hoplias malabaricus (Bloch) (Characiforme, Erythrinidae).Crossref | GoogleScholarGoogle Scholar |
Valverde, MP, Sharpe, DM, Torchin, ME, Buck, DG, and Chapman, LJ (2020). Trophic shifts in a native predator following the introduction of a top predator in a tropical lake. Biological Invasions 22, 643–661.
| Trophic shifts in a native predator following the introduction of a top predator in a tropical lake.Crossref | GoogleScholarGoogle Scholar |
Vazzoler AEAM (1996) ‘Biologia da reprodução de peixes teleósteos: teoria e prática’, (Eduem: Maringá, Brazil)
Vitousek, PM, Mooney, HA, Lubchenco, J, and Melillo, JM (1997). Human domination of Earth’s ecosystems. Science 277, 494–499.
| Human domination of Earth’s ecosystems.Crossref | GoogleScholarGoogle Scholar |
Winemiller, KO (1989). Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan ilanos. Environmental Biology of Fishes 26, 177–199.
| Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan ilanos.Crossref | GoogleScholarGoogle Scholar |
Winemiller, KO (2005). Life history strategies, population regulation, and implications for fisheries management. Canadian Journal of Fisheries Aquatic Sciences 62, 872–885.
| Life history strategies, population regulation, and implications for fisheries management.Crossref | GoogleScholarGoogle Scholar |