Abstract
Fish communities of tropical lakes are commonly predicted by local environmental variables, including depth, temperature, oxygen concentration, and substrate composition. Increasingly, however, lacustrine fish communities are being impacted by invasive species. In the state of Quintana Roo, on the Caribbean versant of the Yucatan Peninsula in Mexico, inland aquaculture production has resulted in the widespread establishment of African tilapia (Oreochromis sp.). However, there are still limited quantitative data on their abundance relative to indigenous species, or their influence on native fish diversity. Here, we quantified the ichthyofauna of six lakes from this region, alongside physical and chemical environmental variables. Overall, we observed that greater dissolved oxygen concentration and shallower depths were associated with the highest fish biodiversity across lakes. Moreover, spatial comparisons additionally highlighted the importance of substrate heterogeneity and lake area as influential in determining native fish community structure. Notably, in all lakes, tilapia were relatively uncommon, comprising less than 3% of all fish captured, and their presence was not a significant predictor of indigenous fish biodiversity. Based on these results, we suggest that tilapia may have strong limitations on their population size, plausibly due to the presence of predatory native fish species, or scarce suitable ecological resources (food, breeding habitat). Conservation-focussed lake-wide management of native species via protection of core habitat characteristics may be key to promoting environmental resistance against negative effects of tilapia regional expansions.
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All data and analysis codes are available at: https://doi.org/10.5281/zenodo.10845972.
References
Amarasinghe US, Welcomme RL (2002) An analysis of fish species richness in natural lakes. Environ Biol Fish 65:327–339. https://doi.org/10.1023/A:1020558820327
American Society for Testing and Materials (ASTM) (2011) Standard practice for classification of soils for engineering purposes (unified soil classification system). ASTM D2487. West Conshohocken. https://www.astm.org/Standards/D2487.htm
Baltz DM, Moyle PB (1993) Invasion resistance to introduced species by a native assemblage of California stream fishes. Ecol Appl 3:246–255. https://doi.org/10.2307/1941827
Bergerot B, Hugueny B, Belliard J (2013) When local extinction and colonization of river fishes can be predicted by regional occupancy: the role of spatial scales. PLoS One 8(12):e84138. https://doi.org/10.1371/journal.pone.0084138
Bergstrom MA, Mensinger AF (2009) Interspecific resource competition between the invasive round goby and three native species: logperch, slimy sculpin, and spoonhead sculpin. Trans Am Fish Soc 138:1009–1017. https://doi.org/10.1577/T08-095.1
Burleson ML, Wilhelm DR, Smatresk NJ (2001) The influence of fish size on the avoidance of hypoxia and oxygen selection by largemouth bass. J Fish Biol 59:1336–1349. https://doi.org/10.1111/j.1095-8649.2001.tb00196.x
Cornell HV, Harrison SP (2014) What are species pools and when are they important? Ann Rev Ecol Evol Syst 45:45–67. https://doi.org/10.1146/annurev-ecolsys-120213-091759
Crowl TA, Crist TO, Parmenter RR, Belovsky G, Lugo AE (2008) The spread of invasive species and infectious disease as drivers of ecosystem change. Front Ecol Environ 6:238–246. https://doi.org/10.1890/070151
Cvetkovic M, Wei A, Chow-Fraser (2010) Relative importance of macrophyte community versus water quality variables for predicting fish assemblages in coastal wetlands of the Laurentian Great Lakes. J Great Lakes Res 36:64–73. https://doi.org/10.1016/j.jglr.2009.10.003
De Cáceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574. https://doi.org/10.1890/08-1823.1
Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366. https://doi.org/10.1890/0012-9615(1997)067[0345:SAAIST]2.0.CO;2
Esselman PC, Schmitter-Soto JJ, Allan JD (2013) Spatiotemporal dynamics of the spread of African tilapias (Pisces: Oreochromis spp.) into rivers of northeastern Mesoamerica. Biol Invasions 15:1471–1491. https://doi.org/10.1007/s10530-012-0384-9
Fricke R, Eschmeyer WN, Van der Laan R (2024) Eschmeyer’s catalog of fishes: genera, species, references [internet]. San Francisco: California Academy of Science. http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
Froese R, Pauly D (2023) FishBase. World Wide Web electronic publication. www.fishbase.org.
Gamboa-Pérez HC, Schmitter-Soto JJ (1999) Distribution of cichlid fishes in the littoral of Lake Bacalar, Yucatan Peninsula. Environ Biol Fish 54:35–43. https://doi.org/10.1023/A:1007443408776
Gido KB, Whitney JE, Perkin JS, Turner TF (2016) Fragmentation, connectivity and fish species persistence in freshwater ecosystems. In: GP Closs, M Krkosek, and JD Olden (eds). Conservation of Freshwater Fishes. Cambridge, UK: Cambridge University Press
Gracida-Juárez CA (2020) Competitive behaviour, impact and success of invasive tilapia (Oreochromis spp.) in Quintana Roo, Mexico. [PhD Thesis]. University of Bristol. https://research-information.bris.ac.uk/en/studentTheses/competitive- behaviour-impact-and-success-of-invasive-tilapia-oreo
Griffiths D (1997) Local and regional species richness in North American lacustrine fish. J Anim Ecol 66:49–56. https://doi.org/10.2307/5963
Harrison E, Lorenz JJ, Trexler JC (2013) Per capita effects of non-native Mayan cichlids (Cichlasoma urophthalmus; Gunther) on native fish in the estuarine southern Everglades. Copeia 2013:80–96. https://doi.org/10.1643/CE-11-182
Hinojosa-Garro D, Arceo-Gómez J, Zambrano L, Escalera-Vázquez LH (2013) Fish diet composition in permanent and semi-permanent pools in tropical wetlands of the Yucatan Peninsula. Neotrop Ichthyol 11:881–890. https://doi.org/10.1590/S1679-62252013000400016
Hodell DA, Brenner M, Curtis JH (2005) Terminal classic drought in the northern Maya lowlands inferred from multiple sediment cores in Lake Chichancanab (Mexico). Quat Sci Rev 24:1413–1427. https://doi.org/10.1016/j.quascirev.2004.10.013
Jeppesen E, Meerhoff M, Holmgren K, González-Bergonzoni I, Teixeira-de Mello F, Declerck SA, De Meester L, Søndergaard M, Lauridsen TL, Bjerring R, Conde-Porcuna JM (2010) Impacts of climate warming on lake fish community structure and potential effects on ecosystem function. Hydrobiologia 646:73–90. https://doi.org/10.1007/s10750-010-0171-5
Jeschke JM, Genovesi P (2011) Do biodiversity and human impact influence the introduction or establishment of alien mammals? Oikos 120:57–64. https://doi.org/10.1111/j.1600-0706.2010.18621.x
Jonsson B, Jonsson N, Hindar K, Northcote TG, Engen S (2008) Asymmetric competition drives lake use of coexisting salmonids. Oecologia 157:553–560. https://doi.org/10.1007/s00442-008-1103-1
Latini AO, Petrere M Jr (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
Marsh PC, Douglas ME (1997) Predation by introduced fishes on endangered humpback chub and other native species in the Little Colorado River, Arizona. T Am Fish Soc 126:343–346. https://doi.org/10.1577/1548-8659(1997)126%3c0343:PBIFOE%3e2.3.CO;2
Martinez Arbizu P (2017) pairwiseAdonis: pairwise multilevel comparison using adonis. R package version 0.4.1. https://github.com/pmartinezarbizu/pairwiseAdonis
Neves LM, Teixeira TP, Franco TP, Pereira H, Araújo FG (2013) Fish composition and assemblage structure in the estuarine mixing zone of a tropical estuary: comparisons between the main channel and an adjacent lagoon. Mar Biol Res 9:661–675. https://doi.org/10.1080/17451000.2013.765575
Oberdorff T, Hugueny B, Compin A, Belkessam D (1998) Non-interactive fish communities in the coastal streams of north-western France. J Anim Ecol 67:472–478. https://doi.org/10.1046/j.1365-2656.1998.00211.x
Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O'Hara R, Solymos P, Stevens M, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Evangelista H, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill M, Lahti L, McGlinn D, Ouellette M, Ribeiro Cunha E, Smith T, Stier A, Ter Braak C, Weedon J (2022) vegan: community ecology package. R package version 2.6–4. https://CRAN.R-project.org/package=vegan
Paradis E, Schliep K (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528. https://doi.org/10.1093/bioinformatics/bty633
Peterson AT (2003) Predicting the geography of species’ invasions via ecological niche modeling. Q Rev Biol 78:419–433. https://doi.org/10.1086/378926
Poole JR, Bajer PG (2019) A small native predator reduces reproductive success of a large invasive fish as revealed by whole-lake experiments. PLoS One 14:e0214009. https://doi.org/10.1371/journal.pone.0214009
Priede IG, Solbé JDL, Nott JE, O’Grady KT, Cragg-Hine D (1988) Behaviour of adult Atlantic salmon, Salmo salar L., in the estuary of the River Ribble in relation to variations in dissolved oxygen and tidal flow. J Fish Biol 33:133–139. https://doi.org/10.1111/j.1095-8649.1988.tb05567.x
R Core Team (2023) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Ruiz-Campos G, Camarena-Rosales F, Contreras-Balderas S, Reyes-Valdez CA, De La Cruz-Agüero J, Torres-Balcazar E (2006) Distribution and abundance of the endangered killifish Fundulus lima, and its interaction with exotic fishes in oases of central Baja California, Mexico. Southwest Nat 51:502–509
Schmitter-Soto JJ, Caro CI (1997) Distribution of tilapia, Oreochromis mossambicus (Perciformes: Cichlidae), and water body characteristics in Quintana Roo, Mexico. Rev Biol Trop 45:1257–1261
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
Shechonge A, Ngatunga BP, Bradbeer SJ, Day JJ, Freer JJ, Ford AG, Kihedu J, Richmond T, Mzighani S, Smith AM, Sweke EA, Tamatamah R, Tyers AM, Turner GF, Genner MJ (2019) Widespread colonisation of Tanzanian catchments by introduced Oreochromis tilapia fishes: the legacy from decades of deliberate introduction. Hydrobiologia 832:235–253. https://doi.org/10.1007/s10750-018-3597-9
Sitoki L, Gichuki J, Ezekiel C, Wanda F, Mkumbo OC, Marshall BE (2010) The environment of Lake Victoria (East Africa): current status and historical changes. Int Rev Hydrobiol 95:209–223. https://doi.org/10.1002/iroh.201011226
Soares MGM, Menezes NA, Junk WJ (2006) Adaptations of fish species to oxygen depletion in a central Amazonian floodplain lake. Hydrobiologia 568:353–367. https://doi.org/10.1007/s10750-006-0207-z
Strecker U (2006) The impact of invasive fish on an endemic Cyprinodon species flock (Teleostei) from Laguna Chichancanab, Yucatan, Mexico. Ecol Freshw Fish 15:408–418. https://doi.org/10.1111/j.1600-0633.2006.00159.x
Tejerina-Garro FL, Fortin R, Rodríguez MA (1998) Fish community structure in relation to environmental variation in floodplain lakes of the Araguaia River, Amazon Basin. Env Biol FIshes 51:399–410. https://doi.org/10.1023/A:1007401714671
Trejo-Torres JC, Durán R, Olmsted I (1993) Manglares de la Península de Yucatán. In: Salazar-Vallejo SI, González NE, eds. Biodiversidad Marina y Costera de México. Mexico City: CONABIO & CIQRO 420–443. http://bibliotecasibe.ecosur.mx/sibe/book/000018359
Turner JS, Snelson FF (1984) Population structure, reproduction and laboratory behavior of the introduced Belonesox belizanus (Poeciliidae) in Florida. Environ Biol Fishes 10:89–100. https://doi.org/10.1007/BF00001665
Vidotto-Magnoni AP, Carvalho ED (2009) Aquatic insects as the main food resource of fish the community in a Neotropical reservoir. Neotrop Ichthyol 7:701–708. https://doi.org/10.1590/S1679-62252009000400020
Vörösmarty CJ, McIntyre PB, Gessner MO, Dudgeon D, Prusevich A, Green P, Glidden S, Bunn SE, Sullivan CA, Reidy Liermann C, Davies PM (2010) Global threats to human water security and river biodiversity. Nature 467:555–561. https://doi.org/10.1038/nature09440
Wannamaker CM, Rice JA (2000) Effects of hypoxia on movements and behavior of selected estuarine organisms from the southeastern United States. J Exp Mar Biol Ecol 249:145–163. https://doi.org/10.1016/S0022-0981(00)00160-X
Werner EE, Hall DJ, Laughlin DR, Wagner DJ, Wilsmann LA, Funk FC (1977) Habitat partitioning in a freshwater fish community. J Fish Res Board Can 34:360–370. https://doi.org/10.1139/f77-058
Weyl OLF (2008) Rapid invasion of a subtropical lake fishery in central Mozambique by Nile tilapia, Oreochromis niloticus (Pisces: Cichlidae). Aquat Conserv 18:839–851. https://doi.org/10.1002/aqc.897
Acknowledgements
We thank S. Mariani and M. Yallop for useful comments.
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The work was funded by a CONACYT (Consejo Nacional de Ciencia y Tecnología) studentship to CAGJ.
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Carlos Gracida: conceptualization, methodology, formal analysis, investigation, data curation, writing—original draft, writing—review and editing, visualisation, and funding acquisition. Juan Schmitter-Soto: validation and writing—review and editing. Martin Genner: conceptualization, methodology, investigation, formal analysis, writing—review and editing, visualisation, supervision, and funding acquisition.
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Fieldwork was conducted under permit PPF/DGOPA-053/15 of Conapesca (National Fishing Council, Mexico), authorised by its scientific and ethical committee. Specimens collected have been deposited in the Ichthyological Collection ECO-CH-P, at El Colegio de la Frontera Sur, Unidad Chetumal, Mexico.
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Gracida-Juárez, C.A., Schmitter-Soto, J.J. & Genner, M.J. Community structure of indigenous fishes relative to habitat variation and invasive tilapia in lakes of Quintana Roo, Mexico. Environ Biol Fish 107, 401–414 (2024). https://doi.org/10.1007/s10641-024-01537-y
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DOI: https://doi.org/10.1007/s10641-024-01537-y