Abstract
The aim of this study was to test the hypothesis that a widespread non-native fish species in Brazil displays opportunistic feeding behavior and changes its diet according to environmental conditions. We compared the diet, feeding selectivity, carbon assimilation, trophic niche, and trophic level of Knodus moenkhausii (a small non-native characid fish species of Upper Paraná River) in streams surrounded by natural riparian vegetation (natural cover streams) and in streams impacted by pasture. We analyzed stomach contents and stable isotopes (carbon and nitrogen), simultaneously. Overall, insects were the most common food items (> 65%). In natural cover streams, K. moenkhausii showed higher selectivity among aquatic macroinvertebrates consumed, while in pasture streams, they fed on the most abundant groups. The proportion of feeding groups assimilated by K. moenkhausii and the proportion of primary sources consumed by each feeding group of macroinvertebrates also varied between natural cover and pasture streams, as indicated by stable isotopes. In natural cover streams, fine and coarse particulate organic matter accounted for approximately 80% of K. moenkhausii’s diet, while in pasture streams, algae and periphyton also contributed greatly. As a result, K. moenkhausii occupied a higher trophic level and exhibited a broader niche width in pasture streams. We conclude that K. moenkhausii presents feeding selectivity with capacity to alter the trophic niche depending on environmental conditions. Such opportunism could be one of the reasons underpinning the abundance and wide distribution of this invasive species.
Similar content being viewed by others
References
Alexander ME, Dick JT, Weyl OL, Robinson TB, Richardson DM (2014) Existing and emerging high impact invasive species are characterized by higher functional responses than natives. Biol Lett 10:20130946. https://doi.org/10.1098/rsbl.2013.0946
Barrett SCH (2011) Why reproductive systems matter for the invasion biology of plants. In: Richardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton. Wiley, Oxford, pp 195–210
Barrie A, Prosser SJ (1996) Automated analysis of light-element stable isotopes by isotope ratio mass spectrometry. In: Boutton TW, Yamaski S (eds) Mass spectrometry of soils. Marcel Decker, New York, pp 1–46
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bearhop S, Adams CE, Waldron S (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012
Bellard C, Cassey P, Blackburn TM (2016) Alien species as a driver of recent extinctions. Biol Lett 12:20150623. https://doi.org/10.1098/rsbl.2015.0623
Britton JR, Davies GD, Brazier M, Pinder AC (2007) A case study on the population ecology of a top mouth gudgeon Pseudorasbora parva population in the UK and the implications for native fish communities. Aquat Conserv Mar Freshw Ecosyst 17:749–759
Britton JR, Gozlan RE, Copp GH (2011) Managing non-native fish in the environment. Fish Fish 12:256–274
Buckland A, Baker R, Loneragan N, Sheaves M (2017) Standardising fish stomach content analysis: the importance of prey condition. Fish Res 196:126–140. https://doi.org/10.1016/j.fishres.2017.08.003
Busst GMA, Britton JR (2017) Comparative trophic impacts of two globally invasive cyprinid fishes reveal species-specific invasion consequences for a threatened native fish. Freshw Biol 62:1587–1595. https://doi.org/10.1111/fwb.12970
Carassou L, Whitfield AK, Moyo S, Richoux NB (2017) Dietary tracers and stomach contents reveal pronounced alimentary flexibility in the freshwater mullet (Myxus capensis, Mugilidae) concomitant with ontogenetic shifts in habitat use and seasonal food availability. Hydrobiologia 799:327–348. https://doi.org/10.1007/s10750-017-3230-3
Carvalho DR, Castro DMP, Callisto M, Moreira MZ, Pompeu PS (2015) Isotopic variation in five species of stream fish under the influence of different land uses. J Fish Biol 87:559–578
Casatti L, Ferreira CP, Carvalho FR (2009) Grass-dominated stream sites exhibit low fish species diversity and dominance by guppies: an assessment of two tropical pasture river basins. Hydrobiologia 632:273–283
Castro DMP, De Carvalho DR, Pompeu PS, Moreira MZ, Nardoto GB, Callisto M (2016) Land use influences niche size and the assimilation of resources by benthic macroinvertebrates in tropical headwater streams. PLoS ONE 11:e0150527
Castro DMP, Dolédec S, Callisto M (2017) Landscape variables influence taxonomic and trait composition of insect assemblages in neotropical savanna streams. Freshw Biol 62:1472–1486. https://doi.org/10.1111/fwb.12961
CBH Paranaíba: Comitê da bacia hidrográfica do Rio Paranaíba (2012). http://www.paranaiba.cbh.gov.br. Accessed 12 July 2016
Ceneviva-Bastos M, Casatti L (2007) Oportunismo alimentar de Knodus moenkhausii (Teleostei, Characidae): uma espécie abundante em riachos do noroeste do Estado de São Paulo, Brasil. Iheringia Ser Zool 97:7–15
Ceneviva-Bastos M, Casatti L, Rossa-Feres DC (2010) Meso and microhabitat analysis and feeding habits of small nektonic characins (Teleostei: Characiformes) in neotropical streams. Zoologia (Curitiba) 27:191–200
Ceneviva-Bastos M, Taboga SR, Casatti L (2015) Microscopic evidence of the opportunistic reproductive strategy and early sexual maturation of the small-sized characin Knodus moenkhausii (Characidae, Pisces). Anat Histol Embryol 44:72–80. https://doi.org/10.1111/ahe.12112
Chapin FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Diaz S (2000) Consequences of changing biodiversity. Nature 405:234–242
Coppin P, Jonckheere I, Nackaerts K, Muys B, Lambin E (2004) Digital change detection methods in ecosystem monitoring; a review. Remote Sens 25:1565–1596
Cortés E (1997) A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. J Fish Aquat Sci 54:726–738
Costa C, Ide S, Simonka CE (2006) Insetos Imaturos. Metamorfose e identificação. Holos, Editora, Ribeirão Preto
Courtenay WR Jr, Williams JD (1992) Dispersal of exotic species from aquaculture sources, with emphasis on freshwater fishes. In: Rosenfield A, Mann R (eds) Dispersal of living organisms into aquatic ecosystems. Maryland Sea Grant Program, College Park, pp 49–82
Cucherousset J, Bouletreau S, Martino A, Roussel JM, Santoul F (2012) Using stable isotope analyses to determine the ecological effects of non-native fishes. Fish Manag Ecol 19:111–119
Cummins KW, Merritt RW, Andrade PC (2005) The use of invertebrate functional groups to characterize ecosystem attributes in selected streams and rivers in south Brazil. Stud Neotrop Fauna Environ 40:69–89. https://doi.org/10.1080/01650520400025720
Davis MA, Grime JP, Thompson J (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534
De Carvalho DR, Castro D, Callisto M, Moreira M, Pompeu PS (2017) The trophic structure of fish communities from streams in the Brazilian cerrado under different land uses: an approach using stable isotopes. Hydrobiologia 795:199–217. https://doi.org/10.1007/s10750-017-3130-6
Drake JM, Lodge DM (2004) Global hot spots of biological invasions: evaluating options for ballast-water management. Proc R Soc Lond B Biol Sci 271:575–580
Fagundes DC, Leal CG, Carvalho DR, Junqueira NT, Langeani F, Pompeu PS (2015) The stream fish fauna from three regions of the Upper Paraná River basin. Biota Neotrop 15:1–8. https://doi.org/10.1590/1676-06032015018714
FAO - Food and Agriculture Organization of the United Nations (2016) El Estado de los bosques del mundo 2016. Los bosques y la agricultura: desafíos y oportunidades en relación con el uso de la tierra. http://www.fao.org/publications/sofo/2016/es/. Accessed 02 Oct 2017
Funk JL (2008) Differences in plasticity between invasive and native plants from a low resource environment. J Ecol 96:1162–1173. https://doi.org/10.1111/j.1365-2745.2008.01435.x
García L, Cross WF, Pardo I, Richardson JS (2017) Effects of land use intensification on stream basal resources and invertebrate communities. Fresh Sci 36:609–625. https://doi.org/10.1086/693457
Google (2010) Google earth. Google Inc., Mountain View
Graça MAS, Ferreira WR, Firmiano K, França J, Callisto M (2015) Macroinvertebrate identity, not diversity, differed across patches differing in substrate particle size and leaf litter packs in low order, tropical Atlantic forest streams. Limnetica 34:29–40
Guo Z, Sheath D, Amat-Trigo F, Britton JR (2017) Comparative functional responses of native and high impacting invasive fishes: impact predictions for native prey populations. Ecol Freshw Fish 26:533–540. https://doi.org/10.1111/eff.12297
Hamada N, Nessimian JL, Querino RB (2014) Insetos aquáticos na Amazônia brasileira: taxonomia, biologia e ecologia. Editora do INPA, Manaus
Herborg LM, Jerde CL, Lodge DM, Ruiz GM, MacIsaac HJ (2007) Predicting invasion risk using measures of introduction effort and environmental niche models. Ecol Appl 17:663–674
Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6:324–337
Hutchinson GE (1957) The multivariate niche. Cold Spring Harb Symp Quant Biol 22:415–421
Hyslop EJ (1980) Stomach contents analysis—a review of methods and their application. J Fish Biol 17:411–429. https://doi.org/10.1111/j.1095-8649.1980.tb02775.x
Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—stable isotope Bayesian ellipses in R. J Anim Ecol 80:595–602
Johnson PT, Olden JD, Vander Zanden MJ (2008) Dam invaders: impoundments facilitate biological invasions in freshwaters. Front Ecol Environ 6:357–363
Kaufmann PR, Levine P, Robison EG, Seeliger C, Peck DV (1999) Quantifying physical habitat in wadeable streams. U.S. Environmental Protection Agency EPA/620/R-99/003. USEPA, Washington, DC
Kawakami E, Vazzoler G (1980) Método gráfico e estimativa de Índice Alimentar aplicado no estudo de alimentação de peixes. Bolm Inst Oceanogr 29:205–207
Keough JR, Hagley CA, Ruzycki E, Sierszen M (1998) 13C composition of primary producers and role of detritus in a freshwater coastal ecosystem. Limnol Oceanogr 43:734–740
Kilroy C, Snelder TH, Floerl O, Vieglais CC, Dey KL (2008) A rapid technique for assessing the suitability of areas for invasive species applied to New Zealand’s rivers. Divers Distrib 14:262–272
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204
Kulhanek SA, Brian L, Ricciardi A (2011) Using ecological niche models to predict the abundance and impact of invasive species: application to the common carp. Ecol Appl 21:203–213
Langeani F, Castro RMC, Oyakawa OT, Shibatta OA, Pavanelli CS, Casatti L (2007) Ichthyofauna diversity of the upper rio Paraná: present composition and future perspectives. Biota Neotrop 7:181–197. https://doi.org/10.1590/S1676-06032007000300020
Lazorchak JM, Klemm DJ, Peck DV (1998) Environmental monitoring and assessment program-surface waters: field operations and methods for measuring the ecological condition of wadeable streams. U.S. Environmental Protection Agency EPA 620/R-94/004F. Cincinnati, OH, USEPA
Lever C (1998) Introduced fishes: an overview. In: Cowx IG (ed) Stocking and Introduction of Fish. Fishing News Books, Oxford, pp 143–152
Levins R (1968) Evolution in changing environments, some theoretical explorations. Monographs in population biology. Princeton University Press, Princeton
Lima LPZ, Pompeu PS, Suzuki FM, Carvalho LMT (2010) Dinâmica espacial de lagoas marginais presentes no rio Aiuruoca, MG, em períodos de cheia e seca. Rev Bras Biocienc 8:253–256
Lima-Junior SE, Goitein RA (2001) A new method for the analysis of fish stomach contents. Acta Sci Biol Sci 23:421–424
Linares MS, Callisto M, Marques JC (2017) Compliance of secondary production and eco-exergy as indicators of benthic macroinvertebrates assemblages’ response to canopy cover conditions in Neotropical headwater streams. Sci Total Environ 613–614:1543–1550. https://doi.org/10.1016/j.scitotenv.2017.08.282
Manetta GI, Benedito-Cecílio E (2003) Aplicação da técnica de isótopos estáveis na estimativa da taxa de turnover em estudos ecológicos: uma síntese. Acta Sci Biol Sci 25:121–129
Marchetti MP, Light T, Moyle PB, Viers J (2004a) Fish invasions in California watersheds: testing hypotheses using landscape patterns. Ecol Appl 14:1507–1525
Marchetti MP, Moyle PB, Levine R (2004b) Invasive species profiling? Exploring the characteristics of non-native fishes across invasion stages in California. Freshw Biol 49:646–661
McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390. https://doi.org/10.1034/j.1600-0706.2003.12098.x
McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–453
Merritt RW, Cummins K, Berg M (2008) An introduction to the aquatic insects of North America. Kendall/Hunt Publishing, Dubuque
Minchinton TE (2002) Disturbance by wrack facilitates spread of Phragmites australis in a coastal marsh. J Exp Mar Biol Ecol 281:89–107
Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11:470–480. https://doi.org/10.1111/j.1461-0248.2008.01163.xPMID:18294213
Mugnai R, Nessimian JL, Baptista DF (2010) Manual de Identificação de Macroinvertebrados Aquáticos do Estado do Rio de Janeiro. Technical Books, Rio de Janeiro
Neres-Lima V, Brito EF, Krsulović FA, Detweiler AM, Hershey AE, Moulton TP (2016) High importance of autochthonous basal food source for the food web of a Brazilian tropical stream regardless of shading. Int Rev Hydrobiol 101:132–142. https://doi.org/10.1002/iroh.201601851
Neres-Lima V, Machado-Silva F, Baptista DF, Oliveira RBS, Andrade PM, Oliveira AF, Sasada-Sato CY, Silva-Junior EF, Feijó-Lima R, Angelini R, Camargo PB, Moulton TP (2017) Allochthonous and autochthonous carbon flows in food webs of tropical forest streams. Freshw Biol 62:1012–1023. https://doi.org/10.1111/fwb.12921
Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e09672. https://doi.org/10.1371/journal.pone.0009672
Peck DV, Herlihy AT, Hill BH, Hughes RM, Kaufmann PR, Klemm DJ, Lazorchak JM, Mccormick FH, Peterson SA, Ringold PL, Magee T, Cappaert MR (2006) Environmental monitoring and assessment program: surface waters western pilot study—field operations manual for wadeable streams. EPA 620/R-06/003. US Environmental Protection Agency, Washington, DC
Peterson AT, Vieglais DA (2001) Predicting species invasions using ecological niche modeling: new approaches from bioinformatics attack a pressing problem. Bioscience 51:363–371
Pettitt-Wade H, Wellband KW, Heath DD, Fisk AT (2015) Niche plasticity in invasive fishes in the Great Lakes. Biol Invasions 17:2565. https://doi.org/10.1007/s10530-015-0894-3
Polito MJ, Trivelpiece WZ, Karnovsky NJ, Ng E, Patterson WP, Emslie SD (2011) Integrating stomach content and stable isotope analyses to quantify the diets of pygoscelid penguins. PLoS ONE 6:e26642. https://doi.org/10.1371/journal.pone.0026642
R Core Team (2017) A language and environment for statistical computing. 55:275–286. http://www.r-project.org. Accessed 28 Sept 2017
Rahel FJ (2002) Homogenization of freshwater faunas. Ann Rev Ecol Syst 33:291–315
Ramírez A, Gutiérrez-Fonseca PE (2014) Functional feeding groups of aquatic insect families in Latin America: a critical analysis and review of existing literature. Rev Biol Trop 62:155–167
Ricciardi A, MacIsaac HJ (2011) Impacts of biological invasions on freshwater ecosystems. In: Richardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton. Wiley, Oxford, pp 211–224
Richardson DM (2011) Fifty years of invasion ecology: the legacy of Charles Elton. Wiley, Oxford
Richardson JS, Zhang Y, Marczak LB (2010) Resource subsidies across the land–freshwater interface and responses in recipient communities. River Res Appl 26:55–66
Scott MC (2006) Winners and losers among stream fishes in relation to land use legacies and urban development in the southeastern US. Biol Conserv 127:301–309
Scott MC, Helfman GS (2001) Native invasions, homogenization, and the mismeasure of integrity of fish assemblages. Fisheries 26:6–15
Shanmugam P, Ahn Y, Sanjeevi SA (2006) A comparison of the classification of wetland characteristics by linear spectral mixture modelling and traditional hard classifiers on multispectral remotely sensed imagery in southern India. Ecol Model 194:379–394
Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176
Simberloff D, Martin J, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P, Sousa R, Tabacchi E, Vila M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66
Stock BC, Semmens BX (2016a) MixSIAR GUI user manual (version 3.1). https://github.com/brianstock/MixSIAR/. Accessed 19 Feb 2018
Stock BC, Semmens BX (2016b) Unifying error structures in commonly used biotracer mixing models. Ecology 97:2562–2569. https://doi.org/10.1002/ecy.1517
Strahler AN (1957) Quantitative analysis of watershed geomorphology. Trans Am Geophys Union 38:913–920. https://doi.org/10.1029/tr038i006p00913
Strassburg BBN, Brooks T, Feltran-Barbieri R, Iribarrem A, Crouzeilles R, Loyola R, Latawiec AE, Oliveira Filho FJB, de Mattos Scaramuzza CA, Scarano FR, Soares-Filho B, Balmford A (2017) Moment of truth for the Cerrado hotspot. Nat Ecol Evol 99:1–3. https://doi.org/10.1038/s41559-017-0099
Tabarelli M, Peres CA, Melo FPL (2012) The ‘few winners and many losers’ paradigm revisited: emerging prospects for tropical forest biodiversity. Biol Conserv 155:136–140. https://doi.org/10.1016/j.biocon.2012.06.020
Teresa FB, Casatti L (2013) Development of habitat suitability criteria for neotropical stream fishes and an assessment of their transferability to streams with different conservation status. Neotrop Ichthyol 11:395–402
Tomanova S, Goitia E, Helešic J (2006) Trophic levels and functional feeding groups of macroinvertebrates in neotropical streams. Hydrobiologia 556:251–264. https://doi.org/10.1007/s10750-005-1255-5
Tran TNQ, Jackson MC, Sheath D, Verreycken H, Britton JR (2015) Patterns of trophic niche divergence between invasive and native fishes in wild communities are predictable from mesocosm studies. J Anim Ecol 84:1071–1080
Tricarico E, Junqueira AOR, Dudgeon D (2016) Alien species in aquatic environments: a selective comparison of coastal and inland waters in tropical and temperate latitudes. Aquat Conserv 26:872–891
Van Valen L (1965) Morphological variation and width of ecological niche. Am Nat 99:377
Vander Zanden MJ, Cabana G, Rasmussen JB (1997) Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (15 N) and literature dietary data. Can J Fish Aquat Sci 54:1142–1158
Welcomme RL (1988) International introductions of inland aquatic species. FAO fisheries technical paper 294
Winkelmann C, Schneider J, Mewes D, Schmidt SI, Worischka S, Hellmann C, Benndorf J (2014) Top-down and bottom-up control of periphyton by benthivorous fish and light supply in two streams. Freshw Biol 59:803–818. https://doi.org/10.1111/fwb.12305
Acknowledgements
We thank the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq), the Coordination for the Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, CAPES), Minas Gerais Energy Company (Companhia Energética de Minas Gerais, CEMIG) and P&D ANEEL/CEMIG GT-487 for the financial support for the project and for the Master’s and Doctoral scholarships granted. Thanks to Ludmilla Portela Zambaldi Lima (Federal University of Lavras/UFLA) and Diego Rodrigues Macedo (Federal University of Minas Gerais/UFMG) for analyses of land use and to UFLA and the Ministry of Environment (MMA) to grant the RapidEye images. Thanks to Amelia K. Weiss (Cornell University) for the English revision. Thanks also to the Benthos Ecology Laboratory (UFMG) and the Laboratory of Fish Ecology (UFLA) who assisted in the collection and processing of samples, to the Centre for Nuclear Energy in Agriculture (CENA) for their support and partnership in the isotopic analysis. DRC was partialy funded by CAPES – Finance Code 001. DMPC received a PDJ scholarship (150307/2018-7) from CNPq. MC was awarded a research productivity CNPq (303380/2015-2, 446155/2014-4) and from the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG No. PPM 00104-18). PSP received a research fellowship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq No. 306325/2011-0) and from the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG No. PPM-00237/13).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Télesphore Sime-Ngando.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
de Carvalho, D.R., de Castro, D.M.P., Callisto, M. et al. Stable isotopes and stomach content analyses indicate omnivorous habits and opportunistic feeding behavior of an invasive fish. Aquat Ecol 53, 365–381 (2019). https://doi.org/10.1007/s10452-019-09695-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-019-09695-3