Abstract
The invasion of predators can result in taxonomic, functional and phylogenetic losses in the structure of fish fauna causing ecological damage in the invaded area. We tested the hypothesis that the invasion of the silver croaker (Plagioscion squamosissimus) altered the structure of fish assemblages in a Neotropical reservoir. Using data from long-term fisheries of the Jaguari Reservoir, Brazil, we calculated taxonomic (richness, evenness and beta diversity), functional (richness, evenness and beta diversity) and phylogenetic (richness, dispersion and beta diversity) metrics of diversity of fish assemblages per year and correlated them with the abundance of the invasive fish. We found that the invasion of P. squamosissimus affected all three facets of diversity. Alpha diversity decreased after the invasion, while beta diversity (both taxonomic and functional) and phylogenetic dispersion increased as P. squamosissimus abundance increased. Plagioscion squamosissimus was successful in the invasion process and became the most abundant predator in the reservoir few years after the first record. The generalist reproductive and feeding strategies of this predator, and the distant phylogenetic relationship with the local ichthyofauna may have facilitated its success. As a top predator in the food network, the invader likely interacted with the community mainly through predation and competition, thereby reshaping the fish community structure. We conclude that the P. squamosissimus invasion negatively affected the local biodiversity by detrimental changes to its taxonomic, functional and phylogenetic structure.
Similar content being viewed by others
Change history
20 April 2024
A Correction to this paper has been published: https://doi.org/10.1007/s10530-024-03295-5
References
AGEVAP (2014) UHE Jaguari—Bacia Paraiba do Sul. https://agevap.org.br/
Agostinho AA, Pelicice FM, Petry AC et al (2007) Fish diversity in the upper Paraná River basin: habitats, fisheries, management and conservation. Aquat Ecosyst Health Manag 10:174–186. https://doi.org/10.1080/14634980701341719
Angulo-Valencia MA, Dias RM, Alves DC et al (2022) Patterns of functional diversity of native and non-native fish species in a neotropical floodplain. Freshw Biol 67:1301–1315. https://doi.org/10.1111/fwb.13918
Barros LC, Santos U, Zanuncio JC, Dergam JA (2012) Plagioscion squamosissimus (Sciaenidae) and Parachromis managuensis (Cichlidae): a threat to native fishes of the Doce river in Minas Gerais, Brazil. PLoS ONE 7:e39138. https://doi.org/10.1371/journal.pone.0039138
Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19:134–143. https://doi.org/10.1111/j.1466-8238.2009.00490.x
Baselga A, Orme CDL (2012) betapart: an R package for the study of beta diversity. Methods Ecol Evol 3:808–812. https://doi.org/10.1111/j.2041-210X.2012.00224.x
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw. https://doi.org/10.18637/jss.v067.i01
Baumgartner MT, Baumgartner G, Gomes LC (2017) Spatial and temporal variations in fish assemblage: testing the zonation concept in small reservoirs. Braz J Biol 78:487–500. https://doi.org/10.1590/1519-6984.170424
Baxter CV, Fausch KD, Murakami M, Chapman PL (2004) Fish invasion restructures stream and forest food webs by interrupting reciprocal prey subsidies. Ecology 85:2656–2663. https://doi.org/10.1890/04-138
Bennett JA, Stotz GC, Cahill JF (2014) Patterns of phylogenetic diversity are linked to invasion impacts, not invasion resistance, in a native grassland. J Veg Sci 25:1315–1326. https://doi.org/10.1111/jvs.12199
Bizerril CRSF (1999) A ictiofauna da bacia do Rio Paraíba do Sul. Biodiversidade e padrões biogeográficos. Braz Arch Biol Technol. https://doi.org/10.1590/S1516-89131999000200014
Blackburn TM, Essl F, Evans T et al (2014) A unified classification of alien species based on the magnitude of their environmental impacts. PLoS Biol 12:e1001850. https://doi.org/10.1371/journal.pbio.1001850
Bøhn T, Amundsen P-A, Sparrow A (2008) Competitive exclusion after invasion? Biol Invasions 10:359–368. https://doi.org/10.1007/s10530-007-9135-8
Botelho M, Gomiero LM, Braga FMS (2007) Feeding of Oligosarcus hepsetus (Cuvier, 1829) (Characiformes) in the Serra do Mar State Park—Santa Virgínia Unit, São Paulo, Brazil. Braz J Biol 67:741–748. https://doi.org/10.1590/S1519-69842007000400022
Brito MFG, Daga VS, Vitule JRS (2020) Fisheries and biotic homogenization of freshwater fish in the Brazilian semiarid region. Hydrobiologia 847:3877–3895. https://doi.org/10.1007/s10750-020-04236-8
Britton JR (2022) Contemporary perspectives on the ecological impacts of invasive freshwater fishes. J Fish Biol. https://doi.org/10.1111/jfb.15240
Cavender-Bares J, Hozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715. https://doi.org/10.1111/j.1461-0248.2009.01314.x
CESP (2000) Programa de manejo pesqueiro: plano de trabalho 2000–2001. CESP, São Paulo, p 74
Clavero M, Hermoso V, Aparicio E, Godinho FN (2013) Biodiversity in heavily modified waterbodies: native and introduced fish in Iberian reservoirs. Freshw Biol 58:1190–1201. https://doi.org/10.1111/fwb.12120
Colautti RI, Richardson DM (2009) Subjectivity and flexibility in invasion terminology: Too much of a good thing? Biol Invasions 11:1225–1229. https://doi.org/10.1007/s10530-008-9333-z
Costa ID, Angelini R (2020) Gut content analysis confirms the feeding plasticity of a generalist fish species in a tropical river. Acta Limnol Bras. https://doi.org/10.1590/s2179-975x7819
Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion1. Écoscience 12:316–329. https://doi.org/10.2980/i1195-6860-12-3-316.1
Cucherousset J, Olden JD (2011) Ecological impacts of non-native freshwater fishes. Fisheries 36:215–230. https://doi.org/10.1080/03632415.2011.574578
Daga VS, Skóra F, Padial AA et al (2015) Homogenization dynamics of the fish assemblages in neotropical reservoirs: comparing the roles of introduced species and their vectors. Hydrobiologia 746:327–347. https://doi.org/10.1007/s10750-014-2032-0
Daga VS, Olden JD, Gubiani ÉA et al (2020) Scale-dependent patterns of fish faunal homogenization in neotropical reservoirs. Hydrobiologia 847:3759–3772. https://doi.org/10.1007/s10750-019-04145-5
de Moraes MB, Polaz CNM, Caramaschi EP, Santos Júnior SS, Souza G, Carvalho FL (2017) Espécies exóticas e alóctones da bacia do rio Paraíba do Sul: implicações para a conservação. Biodiv Bras 7(1):34–54. https://doi.org/10.37002/biobrasil.v%25vi%25i.563
de Souza CP, Rodrigues-Filho CAS, Barbosa FAR, Leitão RP (2021) Drastic reduction of the functional diversity of native ichthyofauna in a Neotropical lake following invasion by piscivorous fishes. Neotrop Ichthyol 19:03. https://doi.org/10.1590/1982-0224-2021-0033
Dutra MCF, Pereyra PER, Hallwass G, Poesch M, Silvano RAM (2023) Fishers’ knowledge on abundance and trophic interactions of the freshwater fish Plagioscion squamosissimus (Perciformes: Sciaenidae) in two Amazonian rivers. Neotrop Ichthyol 21:e220041. https://doi.org/10.1590/1982-0224-2022-0041
Fragoso-Moura EN, Oporto LT, Maia-Barbosa PM, Barbosa FAR (2016) Loss of biodiversity in a conservation unit of the Brazilian Atlantic Forest: the effect of introducing non-native fish species. Braz J Biol 76:18–27. https://doi.org/10.1590/1519-6984.07914
Franco ACS, García-Berthou E, Santos LN (2021) Ecological impacts of an invasive top predator fish across South America. Sci Total Environ 761:143296. https://doi.org/10.1016/j.scitotenv.2020.143296
Franco ACS, Petry AC, García-Berthou E, dos Santos LN (2022) Invasive peacock basses (Cichla spp.) and decreased abundance of small native fish in Brazilian reservoirs. Aquat Conserv 32:1852–1866. https://doi.org/10.1002/aqc.3874
Gubiani ÉA, Ruaro R, Ribeiro VR et al (2018) Non-native fish species in Neotropical freshwaters: How did they arrive, and where did they come from? Hydrobiologia 817:57–69. https://doi.org/10.1007/s10750-018-3617-9
Hixon MA, Jones GP (2005) Competition, predation, and density-dependent mortality in demersal marine fishes. Ecology 86:2847–2859. https://doi.org/10.1890/04-1455
Kembel SW, Ackerly DD, Blomberg SP, Cornwell WK, Cowan PD, Helmus MR (2020) picante: integrating phylogenies and ecology. Version 1(8):2
Kirk MA, Maitland BM, Rahel FJ (2020) Spatial scale, reservoirs and nonnative species influence the homogenization and differentiation of Great Plains—Rocky Mountain fish faunas. Hydrobiologia 847:3743–3757. https://doi.org/10.1007/s10750-019-04129-5
Kitchell JF, Schindler DE, Ogutu-Ohwayo R, Reinthal PN (1997) The Nile perch in Lake Victoria: interactions between predation and fisheries. Ecol Appl 7(2):653–664. https://doi.org/10.1890/1051-0761(1997)007[0653:TNPILV]2.0.CO;2
Kuczynski L, Legendre P, Grenouillet G (2018) Concomitant impacts of climate change fragmentation and non-native species have led to reorganization of fish communities since the 1980s. Global Ecol Biogeogr 27:213–222. https://doi.org/10.1111/geb.12690
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305. https://doi.org/10.1890/08-2244.1
Latini AO, Petrere M (2004) Reduction of a native fish fauna by alien species: an example from Brazilian freshwater tropical lakes. Fish Manag Ecol 11:71–79. https://doi.org/10.1046/j.1365-2400.2003.00372.x
Leibold MA, Economo EP, Peres-Neto P (2010) Metacommunity phylogenetics: separating the roles of environmental filters and historical biogeography. Ecol Lett 13:1290–1299. https://doi.org/10.1111/j.1461-0248.2010.01523.x
Leitão RP, Zuanon J, Villéger S et al (2016) Rare species contribute disproportionately to the functional structure of species assemblages. Proc R Soc B Biol Sci 283:20160084. https://doi.org/10.1098/rspb.2016.0084
Li D, Olden JD, Lockwood JL et al (2020) Changes in taxonomic and phylogenetic diversity in the Anthropocene. Proc R Soc B Biol Sci 287:20200777. https://doi.org/10.1098/rspb.2020.0777
Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology. Wiley, Hoboken
Loiola PP, de Bello F, Chytrý M, Götzenberger L, Carmona CP, Pyšek P, Lososová Z (2018) Invaders among locals: Alien species decrease phylogenetic and functional diversity while increasing dissimilarity among native community members. J Ecol 106:2230–2241. https://doi.org/10.1111/1365-2745.12986
MacDougall AS, Gilbert B, Levine JM (2009) Plant invasions and the niche. J Ecol 97:609–615. https://doi.org/10.1111/j.1365-2745.2009.01514.x
Magurran AE (2003) Measuring biological diversity. Wiley, Hoboken
Magurran AE, Dornelas M, Moyes F, Henderson PA (2019) Temporal β diversity—a macroecological perspective. Glob Ecol Biogeogr 28:1949–1960. https://doi.org/10.1111/geb.13026
Mason NWH, Mouillot D, Lee WG, Wilson JB (2005) Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111:112–118. https://doi.org/10.1111/j.0030-1299.2005.13886.x
Matsuzaki SS, Sasaki T, Akasaka M (2016) Invasion of exotic piscivores causes losses of functional diversity and functionally unique species in Japanese lakes. Freshw Biol 61:1128–1142. https://doi.org/10.1111/fwb.12774
McKinney ML (2004) Do exotics homogenize or differentiate communities? Roles of sampling and exotic species richness. Biol Invasions 6:495–504. https://doi.org/10.1023/B:BINV.0000041562.31023.42
Milardi M, Gavioli A, Soininen J, Castaldelli G (2019) Exotic species invasions undermine regional functional diversity of freshwater fish. Sci Rep 9:17921. https://doi.org/10.1038/s41598-019-54210-1
Milardi M, Gavioli A, Soana E et al (2020) The role of species introduction in modifying the functional diversity of native communities. Sci Total Environ 699:134364. https://doi.org/10.1016/j.scitotenv.2019.134364
Moyle PB, Light T (1996) Biological invasions of fresh water: empirical rules and assembly theory. Biol Conserv 78:149–161. https://doi.org/10.1016/0006-3207(96)00024-9
Nakamura G, Vicentin W, Súarez YR, Duarte L (2020) A multifaceted approach to analyzing taxonomic, functional, and phylogenetic β diversity. Ecology. https://doi.org/10.1002/ecy.3122
Neves MP, Delariva RL, Guimarães ATB, Sanches PV (2015) Carnivory during ontogeny of the Plagioscion squamosissimus: a successful non-native fish in a lentic environment of the upper Paraná river basin. PLoS ONE 10:e0141651. https://doi.org/10.1371/journal.pone.0141651
Nobile AB, Cunico AM, Vitule JRS et al (2020) Status and recommendations for sustainable freshwater aquaculture in Brazil. Rev Aquac. https://doi.org/10.1111/raq.12393
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, Mcglinn D, Minchin PR, O’hara RB, Simpson GL, Solymos P (2019). Vegan: community ecology package; R Package Version 2.5–2
Olden JD, Poff NL (2004) Ecological processes driving biotic homogenization: testing a mechanistic model using fish faunas. Ecology 85:1867–1875. https://doi.org/10.1890/03-3131
Olden JD, LeRoy PN, Douglas MR et al (2004) Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19:18–24. https://doi.org/10.1016/j.tree.2003.09.010
Olden JD, Poff NL, Bestgen KR (2006) Life-history strategies predict fish invasions and extirpations in the Colorado river basin. Ecol Monogr 76:25–40. https://doi.org/10.1890/05-0330
Olden JD, Kennard MJ, Pusey BJ (2008) Species invasions and the changing biogeography of Australian freshwater fishes. Glob Ecol Biogeogr 17:25–37. https://doi.org/10.1111/j.1466-8238.2007.00340.x
ONS. Operador Nacional de Sistema Elétrico. Histórico da Operação. http://ons.org.br/paginas/resultados-da-operacao/historico-da-operacao, Accessed 01 March 2022
Pelicice FM, Agostinho AA (2009) Fish fauna destruction after the introduction of a non-native predator (Cichla kelberi) in a Neotropical reservoir. Biol Invasions 11:1789–1801. https://doi.org/10.1007/s10530-008-9358-3
Pelicice FM, Latini JD, 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. https://doi.org/10.1007/s10750-014-1911-8
Pereira FW, Vitule JRS (2019) The largemouth bass Micropterus salmoides (Lacepède, 1802): impacts of a powerful freshwater fish predator outside of its native range. Rev Fish Biol Fish 29:639–652. https://doi.org/10.1007/s11160-019-09570-2
Pérez-Toledo GR, Villalobos F, Silva RR et al (2022) Alpha and beta phylogenetic diversities jointly reveal ant community assembly mechanisms along a tropical elevational gradient. Sci Rep 12:7728. https://doi.org/10.1038/s41598-022-11739-y
Pla L, Casanoves F, Di Rienzo J (2012) Functional diversity indices, pp 27–51
Qian H, Chu C, Li D et al (2023) Effects of non-native species on phylogenetic dispersion of freshwater fish communities in North America. Divers Distrib 29:143–156. https://doi.org/10.1111/ddi.13647
Queiroz-Sousa J, Brambilla EM, Garcia-Ayala JR et al (2018) Biology, ecology and biogeography of the South American silver croaker, an important Neotropical fish species in South America. Rev Fish Biol Fish 28:693–714. https://doi.org/10.1007/s11160-018-9526-1
R Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rahel FJ (2002) Homogenization of freshwater faunas. Annu Rev Ecol Syst 33:291–315. https://doi.org/10.1146/annurev.ecolsys.33.010802.150429
Renault D, Hess MCM, Braschi J et al (2022) Advancing biological invasion hypothesis testing using functional diversity indices. Sci Total Environ 834:155102. https://doi.org/10.1016/j.scitotenv.2022.155102
Ricciardi A, Mottiar M (2006) Does Darwin’s naturalization hypothesis explain fish invasions? Biol Invasions 8:1403–1407. https://doi.org/10.1007/s10530-006-0005-6
Rojas P, Castro SA, Vila I, Jaksic FM (2021) Exotic species elicit decoupled responses in functional diversity components of freshwater fish assemblages in Chile. Ecol Indic 133:108364. https://doi.org/10.1016/j.ecolind.2021.108364
Rolls RJ, Deane DC, Johnson SE, Heino J, Anderson MJ, Ellingsen KE (2023) Biotic homogenisation and differentiation as directional change in beta diversity: synthesising driver–response relationships to develop conceptual models across ecosystems. Biol Rev 98(4):1388–1423. https://doi.org/10.1111/brv.12958
Ruesink JL (2005) Global analysis of factors affecting the outcome of freshwater fish introductions. Conserv Biol 19:1883–1893. https://doi.org/10.1111/j.1523-1739.2005.00267.x-i1
Sharpe DMT, De León LF, González R, Torchin ME (2017) Tropical fish community does not recover 45 years after predator introduction. Ecology 98:412–424. https://doi.org/10.1002/ecy.1648
Shuai F, Lek S, Li X, Zhao T (2018) Biological invasions undermine the functional diversity of fish community in a large subtropical river. Biol Invasions 20:2981–2996. https://doi.org/10.1007/s10530-018-1751-y
Sobral FL, Lees AC, Cianciaruso MV (2016) Introductions do not compensate for functional and phylogenetic losses following extinctions in insular bird assemblages. Ecol Lett 19:1091–1100. https://doi.org/10.1111/ele.12646
Socolar JB, Gilroy JJ, Kunin WE, Edwards DP (2016) How should beta-diversity inform biodiversity conservation? Trends Ecol Evol 31:67–80. https://doi.org/10.1016/j.tree.2015.11.005
Srivastava DS, Cadotte MW, MacDonald AAM et al (2012) Phylogenetic diversity and the functioning of ecosystems. Ecol Lett 15:637–648. https://doi.org/10.1111/j.1461-0248.2012.01795.x
Strauss SY, Webb CO, Salamin N (2006) Exotic taxa less related to native species are more invasive. Proc Natl Acad Sci 103:5841–5845. https://doi.org/10.1073/pnas.0508073103
Strayer DL (2012) Eight questions about invasions and ecosystem functioning. Ecol Lett 15:1199–1210. https://doi.org/10.1111/j.1461-0248.2012.01817.x
Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651. https://doi.org/10.1016/j.tree.2006.07.007
Teixeira TP, Pinto BCT, Terra BF et al (2005) Diversidade das assembléias de peixes nas quatro unidades geográficas do rio Paraíba do Sul. Iheringia Ser Zool 95:347–357. https://doi.org/10.1590/S0073-47212005000400002
Teixeira DF, Neto FRA, Gomes LC et al (2020) Invasion dynamics of the white piranha (Serrasalmus brandtii) in a Neotropical river basin. Biol Invasions 22:983–995. https://doi.org/10.1007/s10530-019-02138-y
Toussaint A, Beauchard O, Oberdorff T et al (2014) Historical assemblage distinctiveness and the introduction of widespread non-native species explain worldwide changes in freshwater fish taxonomic dissimilarity. Glob Ecol Biogeogr 23:574–584. https://doi.org/10.1111/geb.12141
Toussaint A, Charpin N, Beauchard O et al (2018) Non-native species led to marked shifts in functional diversity of the world freshwater fish faunas. Ecol Lett 21:1649–1659. https://doi.org/10.1111/ele.13141
Tucker CM, Cadotte MW (2013) Unifying measures of biodiversity: understanding when richness and phylogenetic diversity should be congruent. Divers Distrib 19:845–854. https://doi.org/10.1111/ddi.12087
Tucker CM, Cadotte MW, Carvalho SB et al (2017) A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biol Rev 92:698–715. https://doi.org/10.1111/brv.12252
Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301. https://doi.org/10.1890/07-1206.1
Villéger S, Miranda JR, Hernández DF, Mouillot D (2010) Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation. Ecol Appl 20:1512–1522. https://doi.org/10.1890/09-1310.1
Villéger S, Grenouillet G, Brosse S (2013) Decomposing functional β-diversity reveals that low functional β-diversity is driven by low functional turnover in European fish assemblages. Glob Ecol Biogeogr 22:671–681. https://doi.org/10.1111/geb.12021
Wang J, Chen L, Tang W et al (2021) Effects of dam construction and fish invasion on the species, functional and phylogenetic diversity of fish assemblages in the Yellow River Basin. J Environ Manag 293:112863. https://doi.org/10.1016/j.jenvman.2021.112863
Webb CO, Ackerly DD, Mcpeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448
Welcomme RL (1988) International introductions of inland aquatic species. FAO Fish Tech Pap 294:1–318
Winemiller KO, Fitzgerald DB, Bower LM, Pianka ER (2015) Functional traits, convergent evolution, and periodic tables of niches. Ecol Lett 18:737–751. https://doi.org/10.1111/ele.12462
Wood SN (2017) Generalized additive models. Chapman and Hall/CRC, Boca Raton
Zaret TM, Paine RT (1973) Species introduction in a tropical lake. Science (1979) 182:449–455. https://doi.org/10.1126/science.182.4111.449
Zuur AF, Ieno EN (2016) Beginner’s guide to zero-inflated models with R. Highland Statistics Limited, Newburgh
Zuur AF, Ieno EN, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Funding
This work was financed by the São Paulo Research Foundation (FAPESP) [Grant Numbers 2020/00590-6 and 2022/08244-5].
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. The data preparation and curation, and analysis were performed by AON. The first draft of the manuscript was written by AON and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Orlandi Neto, A., Caneppele, D., Marques, H. et al. Long-term impact of an invasive predator on the diversity of fish assemblages in a neotropical reservoir. Biol Invasions 26, 1255–1267 (2024). https://doi.org/10.1007/s10530-023-03243-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-023-03243-9