Abstract
Invasive species cause substantial changes to the biodiversity of freshwater systems. The African Nile tilapia (Oreochromis niloticus) is now widely distributed in tropical freshwaters globally. Despite indications that feral populations can influence native species through competitive effects, direct evidence of competition between Nile tilapia and native species is rare. Moreover, it is not clear if environmental variables such as temperature and oxygen concentration modulate competition. Here, interactions between Nile tilapia and the native Mayan cichlid (Mayaheros urophthalmus) were studied in experimental mesocosms in south-eastern Mexico. We found that Nile tilapia was the more active and aggressive of the two species, and their movement was only weakly influenced by temperature and oxygen concentration. By contrast, movement of the Mayan cichlid was strongly predicted by the movement and aggression of Nile tilapia, and the Mayan cichlid showed a steep decline in behaviours with increased water temperature and reduced oxygen. Our results suggest that broad environmental tolerance of the intrinsically aggressive Nile tilapia provides it with an advantage over native species. Collectively these traits may help to exacerbate its invasive success as those environmental conditions become more commonplace in a changing world.
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Adams, A. J. & R. K. Wolfe, 2007. Occurrence and persistence of non-native Cichlasoma urophthalmus (family Cichlidae) in estuarine habitats of south-west Florida (USA): environmental controls and movement patterns. Marine and Freshwater Research 58: 921–930.
Bates, A. E., C. M. McKelvie, C. J. B. Sorte, S. A. Morley, N. A. R. Jones, J. A. Mondon, T. J. Bird & G. Quinn, 2013. Geographical range, heat tolerance and invasion success in aquatic species. Proceedings of the Royal Society of London B: Biological Sciences 280: 20131958.
Bartoń, K. 2020. MuMIn: Multi-Model Inference. R package version 1.43.17 [available on internet at https://CRAN.R-project.org/package=MuMIn].
Burggren, W. W., J. C. Arriaga-Bernal, P. M. Méndez-Arzate & J. F. Méndez-Sánchez, 2019. Metabolic physiology of the Mayan cichlid fish (Mayaheros uropthalmus): re-examination of classification as an oxyconformer. Comparative Biochemistry and Physiology Part a: Molecular and Integrative Physiology 237: 110538.
Canonico, G. C., A. Arthington, J. K. McCrary & M. L. Thieme, 2005. The effects of introduced tilapias on native biodiversity. Aquatic Conservation: Marine and Freshwater Ecosystems 15: 463–483.
Carmona-Catot, G., K. Magellan & E. García-Berthou, 2013. Temperature-specific competition between invasive mosquitofish and an endangered cyprinodontid fish. PLoS ONE 8: e54734.
Castillo, C., 2019. Intent of increasing tilapia production in Chetumal. Novedades de Quintana Roo [available on internet at https://sipse.com/novedades/pretenden-aumentar-produccion-de-tilapia-342348.html].
Champneys, T., M. J. Genner & C. C. Ioannou, 2021. Invasive Nile tilapia dominates a threatened indigenous tilapia in competition over shelter. Hydrobiologia 848: 3747–3762.
Clark, T. D., E. Sandblom & F. Jutfelt, 2013. Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. Journal of Experimental Biology 216: 2771–2782.
Cuddington, K. & A. Hastings, 2004. Invasive engineers. Ecological Modelling 178: 335–347.
Duenas, M. A., D. J. Hemming, A. Roberts & H. Diaz-Soltero, 2021. The threat of invasive species to IUCN-listed critically endangered species: a systematic review. Global Ecology and Conservation 26: e01476.
Didham, R. K., J. M. Tylianakis, M. A. Hutchison, R. M. Ewers & N. J. Gemmell, 2005. Are invasive species the drivers of ecological change? Trends in Ecology and Evolution 20: 470–474.
Doherty, T. S., A. S. Glen, D. G. Nimmo, E. G. Ritchie & C. R. Dickman, 2016. Invasive predators and global biodiversity loss. Proceedings of the National Academy of Sciences of the USA 113: 11261–11265.
Fick, S. E. & R. J. Hijmans, 2017. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37: 4302–4315.
Ficke, A. D., C. A. Myrick & L. J. Hansen, 2007. Potential impacts of global climate change on freshwater fisheries. Reviews in Fish Biology and Fisheries 17: 581–613.
Fox, J., & S. Weisberg, 2019. An {R} Companion to Applied Regression, 3rd edn. Sage, Thousand Oaks [available on internet at https://socialsciences.mcmaster.ca/jfox/Books/Companion/].
Friard, O. & M. Gamba, 2016. BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods in Ecology and Evolution 7: 1325–1330.
García-Berthou, E., 2007. The characteristics of invasive fishes: what has been learned so far? Journal of Fish Biology 71(Supplement D): 33–55.
Gozlan, R. E., S. St-Hilaire, S. W. Feist, P. Martin & M. L. Kent, 2005. Disease threat to European fish. Nature 435: 1046.
Gurevitch, J. & D. K. Padilla, 2004. Are invasive species a major cause of extinctions? Trends in Ecology and Evolution 19: 470–474.
Hernández, M., E. Gasca-Leyva & A. Milstein, 2014. Polyculture of mixed-sex and male populations of Nile tilapia (Oreochromis niloticus) with the Mayan cichlid (Cichlasoma urophthalmus). Aquaculture 418: 26–31.
Hess, S., S. Fischer & B. Taborsky, 2016. Territorial aggression reduces vigilance but increases aggression towards predators in a cooperatively breeding fish. Behaviour 113: 229–235.
Hui, W., Z. Xiaowen, W. Haizhen, Q. Jun, X. Pao & L. Ruiwei, 2014. Joint effect of temperature, salinity and pH on the percentage fertilization and hatching of Nile tilapia (Oreochromis niloticus). Aquaculture Research 45: 259–269.
Jenny, J. P., P. Francus, A. Normandeau, F. Lapointe, M. E. Perga, A. Ojala, A. Schimmelmann & B. Zolitschka, 2016. Global spread of hypoxia in freshwater ecosystems during the last three centuries is caused by rising local human pressure. Global Change Biology 22: 1481–1489.
Kiesecker, J. M., A. R. Blaustein & C. L. Miller, 2001. Potential mechanisms underlying the displacement of native red-legged frogs by introduced bullfrogs. Ecology 82: 1964–1970.
Kolding, J., L. Haug & S. Stefansson, 2008. Effect of ambient oxygen on growth and reproduction in Nile tilapia (Oreochromis niloticus). Canadian Journal of Fisheries and Aquatic Sciences 65: 1413–1424.
Kuznetsova, A., P. B. Brockhoff & R. H. B. Christensen, 2017. lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82: 1–26.
LaManna, J. & P. Eason, 2007. Effects of predator presence on territorial establishment. Behaviour 144: 985–1001.
Lovell, S. J., S. F. Stone & L. Fernandez, 2006. The economic impacts of aquatic invasive species: a review of the literature. Agricultural and Resource Economics Review 35: 195–208.
Martin, C. W., M. M. Valentine & J. F. Valentine, 2010. Competitive interactions between invasive Nile tilapia and native fish: the potential for altered trophic exchange and modification of food webs. PLoS ONE 5: e14395.
Martinez-Palacios, C. A., C. Chavez-Sanchez, & M. A. Olvera-Novoa, 1993. The potential for culture of the American Cichlidae with emphasis on Cichlasoma urophthalmus. In Muir, J. F & R. J. Roberts (eds), Recent Advances in Aquaculture IV. Blackwell, Oxford: 193–232.
Mazerolle, M. J. 2020. AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.3-1 [available on internet at https://cran.r-project.org/package=AICcmodavg].
McBryan, T. L., T. M. Healy, K. L. Haakons & P. M. Schulte, 2016. Warm acclimation improves hypoxia tolerance in Fundulus heteroclitus. Journal of Experimental Biology 219: 474–484.
Mexico Government, 2012. Acuerdo mediante el cual se aprueba la carta nacional acuicola. Diario Oficial de la Federacion, Mexico [available on internet at http://dof.gob.mx/nota_detalle.php?codigo=5313326&fecha=09/09/2013].
Njiru, M., J. B. Okeyo-Owuor, M. Muchiri & I. G. Cowx, 2004. Shifts in the food of Nile tilapia, Oreochromis niloticus (L.) in Lake Victoria, Kenya. African Journal of Ecology 42: 163–170.
Orr, J. A., R. D. Vinebrooke, M. C. Jackson, K. J. Kroeker, R. L. Kordas, C. Mantyka-Pringle, P. J. Van den Brink, F. De Laender, R. Stoks, M. Holmstrup, C. D. Matthaei, W. A. Monk, M. R. Penk, S. Leuzinger, R. B. Schäfer & J. J. Piggott, 2020. Towards a unified study of multiple stressors: divisions and common goals across research disciplines. Proceedings of the Royal Society b: Biological Sciences 287: 20200421.
Oyugi, D. O., J. Cucherousset & J. R. Britton, 2012. Temperature-dependent feeding interactions between two invasive fishes competing through interference and exploitation. Reviews in Fish Biology and Fisheries 22: 499–508.
Payne, N. L., J. A. Smith, D. E. van der Meulen, M. D. Taylor, Y. Y. Watanabe, A. Takahashi, T. A. Marzullo, C. A. Gray, G. Cadiou & I. M. Suthers, 2016. Temperature dependence of fish performance in the wild: links with species biogeography and physiological thermal tolerance. Functional Ecology 30: 903–912.
Perkins, D. M., G. Yvon-Durocher, B. O. Demars, J. Reiss, D. E. Pichler, N. Friberg, M. Trimmer & G. Woodward, 2012. Consistent temperature dependence of respiration across ecosystems contrasting in thermal history. Global Change Biology 18: 1300–1311.
Pörtner, H. O. & R. Knust, 2007. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315: 95–97.
R Core Team, 2019. R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna:
Rana, K. J., 1990. Influence of incubation temperature on Oreochromis niloticus (L.) eggs and fry. I. Gross embryology, temperature tolerance and rates of embryonic development. Aquaculture 87: 165–181.
Sanches, F. H. C., C. A. Miyai, T. M. Costa, R. A. Christofoletti, G. L. Volpato & R. E. Barreto, 2012. Aggressiveness overcomes body-size effects in fights staged between invasive and native fish species with overlapping niches. PLoS ONE 7: e29746.
Schmitter-Soto, J. J. & C. I. Caro, 1997. Distribution of tilapia, Oreochromis mossambicus (Perciformes: Cichlidae), and water body characteristics in Quintana Roo, Mexico. Revista De Biología Tropical 45: 1257–1261.
Schofield, P. J., W. F. Loftus, R. M. Kobza, M. I. Cook & D. H. Slone, 2010. Tolerance of nonindigenous cichlid fishes (Cichlasoma urophthalmus, Hemichromis letourneuxi) to low temperature: laboratory and field experiments in south Florida. Biological Invasions 12: 2441–2457.
Schofield, P. J., W. F. Loftus & J. A. Fontaine, 2009. Salinity effects on behavioural response to hypoxia in the non-native Mayan cichlid Cichlasoma urophthalmus from Florida Everglades wetlands. Journal of Fish Biology 74: 1245–1258.
Smith, J. E., N. N. Price, C. E. Nelson & A. F. Haas, 2013. Coupled changes in oxygen concentration and pH caused by metabolism of benthic coral reef organisms. Marine Biology 160: 2437–2447.
Stauffer, J. R. & S. E. Boltz, 1994. Effect of salinity on the temperature preference and tolerance of age-0 Mayan Cichlids. Transactions of the American Fisheries Society 123: 101–107.
Vitousek, P. M., C. M. D’antonio, L. L. Loope, M. Rejmanek & R. Westbrooks, 1997. Introduced species: a significant component of human-caused global change. New Zealand Journal of Ecology 21: 1–16.
Webster, M. M., A. J. W. Ward & P. J. B. Hart, 2009. Individual boldness affects interspecific interactions in sticklebacks. Behavioral Ecology and Sociobiology 63: 511–520.
Wing, J. D. B., T. S. Champneys & C. C. Ioannou, 2021. The impact of turbidity on foraging and risk taking in the invasive Nile tilapia (Oreochromis niloticus) and a threatened native cichlid (Oreochromis amphimelas). Behavioral Ecology and Sociobiology 75: 49.
Whitney, K. D. & C. A. Gabler, 2008. Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Diversity and Distributions 14: 569–580.
Worthington, E. B. & R. Lowe-McConnell, 1994. African lakes reviewed: creation and destruction of biodiversity. Environmental Conservation 21: 199–213.
Xie, S., K. Zheng, J. Chen, Z. Zhang, X. Zhu & Y. Yang, 2011. Effect of water temperature on energy budget of Nile tilapia, Oreochromis niloticus. Aquaculture Nutrition 17: 683–690.
Zambrano, L., E. Martínez-Meyer, N. Menezes & A. T. Peterson, 2006. Invasive potential of common carp (Cyprinus carpio) and Nile tilapia (Oreochromis niloticus) in American freshwater systems. Canadian Journal of Fisheries and Aquatic Sciences 63: 1903–1910.
Zamora, J. 2018. Quintana Roo, the main producer of Tilapia in Mexico. Novedades de Quintana Roo [available on internet at https://sipse.com/novedades/produccion-tilapia-quintana-roo-calidad-superior-conapesca-mexico-pesca-exportacion-312516.html].
Acknowledgements
We thank Karlos Velazques for his support during the experimental trials. We are grateful to S. Mariani, M. Yallop, anonymous reviewers and the editors for useful comments.
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CAGJ, CCI and MJG designed the experiment, CAGJ conducted the experiment and collected the data, CAGJ and MJG analysed the data, CAGJ and MJG wrote the first draft paper, CAGJ, CCI and MJG worked on subsequent drafts.
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The experimental work was approved by the Animal Welfare and Ethics Review Board of the University of Bristol (UIN Code UB/17/055).
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Gracida-Juárez, C.A., Ioannou, C.C. & Genner, M.J. Competitive dominance and broad environmental tolerance favour invasive success of Nile tilapia. Hydrobiologia 849, 1161–1176 (2022). https://doi.org/10.1007/s10750-021-04778-5
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DOI: https://doi.org/10.1007/s10750-021-04778-5