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Mosquito larvae consumption in turbid waters: the role of the type of turbidity and the larval stage in native and invasive fish

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Abstract

Agricultural runoff and biological invasions alter native species interactions with implications for the management of pests. Here, we used live larvae of common house mosquito Culex pipiens to test the efficiencies of the invasive fish Gambusia holbrooki and the IUCN endangered fish Aphanius iberus to manage mosquitoes at three ecologically relevant concentrations of algae and clay. Both species reduced mosquito abundance in aquaria and outdoor mesocosms though A. iberus reduced it at a slower pace. However, G. holbrooki preferentially captured larger larvae at all fish sizes, whereas smaller individuals of A. iberus captured higher number of smaller larvae. Algal turbidity, but not clay, reduced the efficiency of both species, probably because of an adaptation to inorganic turbidity. Fish efficiency was not reduced in mesocosms where fish captured mosquito larvae interacting with natural invertebrate assemblages. Managers should maintain algal turbidity at < 10 FTU based on the visual detection threshold for both species. Our study shows that algal turbidity threatens the potential of waterbodies to naturally control mosquitoes and discusses why the faster foraging rates of alien species such as G. holbrooki should not be used to justify more introductions.

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References

  • Alcaraz, C. & E. García-Berthou, 2007. Food of an endangered cyprinodont (Aphanius iberus): ontogenetic diet shift and prey electivity. Environmental Biology of Fishes 78: 193–207.

    Google Scholar 

  • Alcaraz, C., A. Bisazza & E. García-Berthou, 2007. Salinity mediates the competitive interactions between invasive mosquitofish and an endangered fish. Oecologia 155: 205–213.

    PubMed  Google Scholar 

  • Asimeng, E. J. & M. J. Mutinga, 1992. Field evaluation of Tilapia zilli (Gervais) as a biological control agent for mosquito control. Biological Control 2: 317–320.

    Google Scholar 

  • Bates, D., M. Maechler, B. Bolker & S. Walker, 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.

    Google Scholar 

  • Becker, N., D. Petrić, C. Boase, J. Lane, M. Zgomba, C. Dahl & A. Kaiser, 2010. Mosquitoes and Their Control, 2nd ed. Springer, Heidelberg.

    Google Scholar 

  • Billman, E. J., E. J. Wagner & R. E. Arndt, 2007. A comparison of mosquito consumption and prey selection between least chub (Iotichthys phlegethontis) and western mosquitofish (Gambusia affinis). Western North American Naturalist 67: 71–79.

    Google Scholar 

  • Bin Omar, A. & M. Bin MatJafri, 2009. Turbidimeter design and analysis: a review on optical fiber sensors for the measurement of water turbidity. Sensors 9: 8311–8335.

    CAS  Google Scholar 

  • Blanco, S., S. Romo & M. J. Villena, 2004. Experimental study on the diet of mosquitofish (Gambusia holbrooki) under different ecological conditions in a shallow lake. International Review of Hydrobiology 89: 250–262.

    Google Scholar 

  • Caiola, N. & A. de Sostoa, 2005. Possible reasons for the decline of two native toothcarps in the Iberian Peninsula: evidence of competition with the introduced Eastern mosquitofish. Journal of Applied Ichthyology 21: 358–363.

    Google Scholar 

  • Cano-Rocabayera, O., A. de Sostoa, L. Coll & A. Maceda-Veiga, 2019. Managing small, highly prolific invasive aquatic species: exploring an ecosystem approach for the eastern mosquitofish (Gambusia holbrooki). Science of the Total Environment 673: 594–604.

    CAS  PubMed  Google Scholar 

  • Cardona, L., 2006. Trophic cascades uncoupled in a coastal marsh ecosystem. Biological Invasions 8: 835–842.

    Google Scholar 

  • Carpenter, S. R., 2005. Eutrophication of aquatic ecosystems: bistability and soil phosphorus. Proceedings of the National Academy of Sciences of USA 102: 10002–10005.

    CAS  Google Scholar 

  • Clements, A. N., 1992. The biology of mosquitoes. In Development, Nutrition and Reproduction, Volume 1. Chapman and Hall, London.

  • Cronin, T. W., S. Johnsen, N. J. Marshall & E. J. Warrant, 2014. Visual Ecology. Princeton University Press, Princeton.

    Google Scholar 

  • De Buen, F., 1929. La invasión de nuestras aguas dulces por las Gambusias (Gambusia holbrooki Grd.). Revista de Biología forestal y Limnología 1: 49–53.

    Google Scholar 

  • de-Bashan, L. E., Y. Bashan, M. Moreno, V. K. Lebsky & J. J. Bustillos, 2002. Increased pigment and lipid content, lipid variety, and cell and population size of the microalgae Chlorella spp. when co-immobilized in alginate beads with the microalgae-growth-promoting bacterium Azospirillum brasilense. Canadian Journal of Microbiology 48: 514–521.

    CAS  PubMed  Google Scholar 

  • Doadrio, I., 2002. Atlas y libro de los peces continentales de España, 2nd ed. Museo Nacional de Ciencias Naturales, Dirección General de Conservación de la Naturaleza, Madrid.

    Google Scholar 

  • Eritja, R., J. R. B. Palmer, D. Roiz, I. Sanpera-Calbet & F. Bartumeus, 2017. Direct evidence of adult Aedes albopictus dispersal by car. Scientific Reports 7: 14399.

    PubMed  PubMed Central  Google Scholar 

  • Ford, M., 2016. Project Fartet, Barcelona (2007–2013): A Case of Conflicting Interests. Saving Freshwater Fishes and Habitats. Newsletter of the IUCN SSC/WI Freshwater Fish Specialist Group. Issue 11, May 2016.

  • Fox, J. & S. Weisberg, 2011. An R Companion to Applied Regression, 2nd edition. Sage, Thousand Oaks [available on internet at http://socserv.socsci.mcmaster.ca/jfox/Books/Companion]. Accessed May 2019.

  • Fryxell, D. C., H. A. Arnett, T. M. Apgar, M. T. Kinnison & E. P. Palkovacs, 2015. Sex ratio variation shapes the ecological effects of a globally introduced freshwater fish. Proceedings of the Royal Society B: Biological Sciences 282: 20151970.

    PubMed  Google Scholar 

  • Garchitorena, A., S. H. Sokolow, B. Roche, C. N. Ngonghala, M. Jocque, A. Lund, M. Barry, E. A. Mordecai, G. C. Daily, J. H. Jones, J. R. Andrews, E. Bendavid, S. P. Luby, A. D. LaBeaud, K. Seetah, J. F. Guégan, M. H. Bonds & G. A. De Leo, 2017. Disease ecology, health and the environment: a framework to account for ecological and socio-economic drivers in the control of neglected tropical diseases. Philosophical Transactions of the Royal Society B: Biological Sciences 372: 20160128.

    Google Scholar 

  • Haas, R., 1982. Notes on the ecology of Aphanius dispar (Pisces, Cyprinodontidae) in the Sultanate of Oman. Freshwater Biology 12: 89–95.

    Google Scholar 

  • Hartman, E. J. & M. V. Abrahams, 2000. Sensory compensation and the detection of predators: the interaction between chemical and visual information. Proceedings of the Royal Society of London: Series B: Biological Sciences 267: 571–575.

    CAS  Google Scholar 

  • Homski, D., M. Goren & A. Gasith, 1994. Comparative evaluation of the larvivorous fish Gambusia affinis and Aphanius dispar as mosquito control agents. Hydrobiologia 284: 137–146.

    Google Scholar 

  • Horppila, J., A. Liljendahl-Nurminen & T. Malinen, 2004. Effects of clay turbidity and light on the predator–prey interaction between smelts and chaoborids. Canadian Journal of Fisheries and Aquatic Sciences 61: 1862–1870.

    Google Scholar 

  • Hotez, P. J., 2016. Neglected tropical diseases in the Anthropocene: the cases of Zika, Ebola, and other infections. PLoS Neglected Tropical Diseases 10: e0004648.

    PubMed  PubMed Central  Google Scholar 

  • Jaeger, B., 2017. R2glmm: Computes R Squared for Mixed (Multilevel) Models, R package version 0.1.2 [available on internet at https://CRAN.R-project.org/package=r2glmm]. Accessed May 2019.

  • Kadlec, R. H., 2009. Wetlands for contaminant and wastewater treatment. In Maltby, E. & T. Barker (eds), The Wetlands Handbook. Wiley-Blackwell, Hoboken: 440–463.

    Google Scholar 

  • Lacey, L. A., 2007. Bacillus thuringiensis serovariety israelensis and Bacillus sphaericus for mosquito control. Journal of the American Mosquito Control Association 23: 133–164.

    CAS  PubMed  Google Scholar 

  • Lardeux, F. J. R., 1992. Biological control of Culicidae with the copepod Mesocyclops aspericornis and larvivorous fish (Poeciliidae) in a village of French Polynesia. Medical and Veterinary Entomology 6: 9–15.

    CAS  PubMed  Google Scholar 

  • Leisnham, P. T., D. P. Slaney, P. J. Lester & P. Weinstein, 2005. Increased larval mosquito densities from modified landuses in the Kapiti Region, New Zealand: vegetation, water quality, and predators as associated environmental factors. EcoHealth 2: 313–322.

    Google Scholar 

  • Lemasson, J., 1937. L’utilisation de “Gambusia affinis” et “Girardinus guppyi” pour la lutte antimalarienne. Bulletin économique de l’Indo-Chine 40: 328–330.

    Google Scholar 

  • Levine, J. S. & E. F. MacNichol Jr., 1982. Color vision in fishes. Scientific American 246: 140–149.

    Google Scholar 

  • Nieman, C. L., A. L. Oppliger, C. C. McElwain & S. M. Gray, 2018. Visual detection thresholds in two trophically distinct fishes are compromised in algal compared to sedimentary turbidity. Conservation Physiology 6: coy044.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oksanen, J., F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, E. Szoecs & H. Wagner, 2019. Community Ecology package, R package version 2.5-4 [available on internet at https://CRAN.R-project.org/package=vegan]. Accessed May 2019.

  • Paaijmans, K. P., S. Blanford, A. S. Bell, J. I. Blanford, A. F. Read & M. B. Thomas, 2010. Influence of climate on malaria transmission depends on daily temperature variation. Proceedings of the National Academy of Sciences of USA 107: 15135–15139.

    CAS  Google Scholar 

  • Pyke, G. H., 2008. Plague Minnow or mosquito fish? A review of the biology and impacts of introduced Gambusia species. Annual Review of Ecology, Evolution, and Systematics 39: 171–191.

    Google Scholar 

  • R Core Team, 2018. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna [available on internet at http://www.R-project.org/]. Accessed May 2019.

  • Reynolds, J. D., T. J. Webb & L. A. Hawkins, 2005. Life history and ecological correlates of extinction risk in European freshwater fishes. Canadian Journal of Fisheries and Aquatic Sciences 62: 854–862.

    Google Scholar 

  • Ruiz-Navarro, A., M. Torralva & F. Oliva-Paterna, 2013. Trophic overlap between cohabiting populations of invasive mosquitofish and an endangered toothcarp at changing salinity conditions. Aquatic Biology 19: 1–11.

    Google Scholar 

  • Shelton, J. M., M. S. Bird, M. J. Samways & J. A. Day, 2016. Non-native rainbow trout (Oncorhynchus mykiss) occupy a different trophic niche to native Breede River redfin (Pseudobarbus burchelli) which they replace in South African headwater streams. Ecology of Freshwater Fish 26: 484–496.

    Google Scholar 

  • Shoup, D. E. & D. H. Wahl, 2009. The effects of turbidity on prey selection by piscivorous largemouth bass. Transactions of the American Fisheries Society 138: 1018–1027.

    Google Scholar 

  • Strauss, R. E., 1979. Reliability estimates for Ivlev’s electivity index, the forage ratio, and a proposed linear index of food selection. Transactions of the American Fisheries Society 108: 344–352.

    Google Scholar 

  • Turner, A. M. & J. C. Trexler, 1997. Sampling aquatic invertebrates from marshes: evaluating the options. Journal of the North American Benthological Society 16: 694–709.

    Google Scholar 

  • Utne-Palm, A. C., 2002. Visual feeding of fish in a turbid environment: physical and behavioural aspects. Marine and Freshwater Behaviour and Physiology 35: 111–128.

    Google Scholar 

  • Verhoeven, J., B. Arheimer, C. Yin & M. Hefting, 2006. Regional and global concerns over wetlands and water quality. Trends in Ecology and Evolution 21: 96–103.

    PubMed  Google Scholar 

  • Walton, W. E., J. A. Henke & A. M. Why, 2012. Gambusia affinis (Baird & Girard) and Gambusia holbrooki Girard (mosquitofish). In Francis, R. A. (ed.), A Handbook of Global Freshwater Invasive Species. Easthscan, Washington, DC: 261–273.

    Google Scholar 

  • WHO, 2018. World Malaria Report 2018. World Health Organization, Geneva.

    Google Scholar 

  • WWF, 2018. In Grooten, M. & R. E. A. Almond (eds), Living Planet Report – 2018: Aiming Higher. WWF, Gland.

    Google Scholar 

  • Zuur, A. F., E. N. Ieno, N. Walker, A. A. Saveliev & G. M. Smith, 2009. Mixed Effects Models and Extensions in Ecology with R. Springer, New York.

    Google Scholar 

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Acknowledgements

We are grateful to F. X. Santaeufemia for providing Aphanius iberus from the Espais Naturals del Delta del Llobregat conservation programme. We also thank all the staff from the aquatic animal facilities at UB: Faculty of Biology. English was reviewed by Laura Massana. This study was funded by the Fundació Barcelona Zoo - Ajuntament de Barcelona. SVA was financed by a Fundació Bosch i Gimpera grant and OCR by an APIF Grant from the University of Barcelona.

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Correspondence to Oriol Cano-Rocabayera.

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The experimental procedure was authorized by the Natural Environment and Biodiversity Division at the Catalan Department of Agriculture and Fisheries (Num. DAAM 8289). Fish capture and maintenance were approved by the Committee for an Ethical Use of Experimental Animals at the University of Barcelona (Num. 193/15). Lab experimentation with endangered Aphanius iberus stocks for ex situ conservation purposes was compensated by returning the experimental individuals and the newborn hatchlings born in the lab to wildlife.

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Cano-Rocabayera, O., Vargas-Amengual, S., Aranda, C. et al. Mosquito larvae consumption in turbid waters: the role of the type of turbidity and the larval stage in native and invasive fish. Hydrobiologia 847, 1371–1381 (2020). https://doi.org/10.1007/s10750-020-04195-0

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