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What traits underpin the successful establishment and spread of the invasive water bug Trichocorixa verticalis verticalis?

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Abstract

The introduction of exotic species has a major impact on a wide range of ecosystems, especially in aquatic ecosystems. Trichocorixa v. verticalis (Fieber, 1851), an euryhaline aquatic hemipteran native North America, has occurred as an exotic species in the Iberian Peninsula since at least 1997. In this study, we compared several physiological and biological traits (salinity tolerance of the different developmental stages, thermal tolerance, fecundity, and dispersal ability) in the alien species and three native, syntopic corixidae species (Sigara lateralis, Sigara scripta, and Sigara selecta), to determine which traits may explain its invasion success. Trichocorixa verticalis was the species most resistant to high conductivity at the egg stage, while S. selecta showed the highest halotolerance as adults. The invader had the highest upper thermal limit and a much higher fecundity than Sigara species. Wing morphometry suggested that T. verticalis may be a stronger flier than the native species. Our findings provide an example of how functional and ecological niche interactions among alien and native species can help predict impacts of invasion on aquatic communities.

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References

  • Alonso, A. & J. A. Camargo, 2003. Short-term toxicity of ammonia, nitrite and nitrate to the aquatic snail Potamopyrgus antipodarum (Hidrobiidae, Mollusca). Bulletin of Environmental Contamination and Toxicology 70: 1006–1012.

    Article  PubMed  CAS  Google Scholar 

  • Alonso, A. & J. A. Camargo, 2004. Sub-lethal responses of the aquatic snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca) to unionised ammonia: a tolerant invading species. Fresenius Environmental Bulletin 13: 607–615.

    CAS  Google Scholar 

  • Arribas, P., J. Velasco, P. Abellán, D. Sánchez-Fernández, C. Andújar, P. Calosi, A. Millán, I. Ribera & D. Bilton, 2012. Dispersal ability rather than ecological tolerance drives differences in range size between lentic and lotic water beetles (Coleoptera: Hydrophilidae). Journal of Biogeography 39: 984–994.

    Article  Google Scholar 

  • Aukema, B. & C. Rieger, 1995. Catalogue of the Heteroptera of the Paleartic Region. Enicocephalomorpha, Dipsocoromorpha, Nepomorpha, Gerromorpha and Leptopodomorpha, Vol. 1. Netherlands Entomological Society, Amsterdam.

    Google Scholar 

  • Berwaerts, K., H. Van Dyck & P. Aerts, 2002. Does flight morphology relate to flight performance? An experimental test with the butterfly Pararge aegeria. Functional Ecology 16: 484–491.

    Article  Google Scholar 

  • Blackburn, T. M., P. Pyšek, S. Bacher, J. T. Carlton, R. P. Duncan, V. Jarošík, J. R. U. Wilson & D. M. Richardson, 2011. A proposed unified framework for biological invasions. Trends in Ecology and Evolution 26: 333–339.

    Article  PubMed  Google Scholar 

  • Boda, P. & Z. Csabai, 2009. Seasonal and diel dispersal activity characteristics of Sigara lateralis (Leach, 1817) (Heteroptera: Corixidae) with special emphasis on possible environmental factors and breeding state. Aquatic Insects 31: 301–314.

    Article  Google Scholar 

  • Calosi, P., D. T. Bilton & J. I. Spicer, 2008. Thermal tolerance, acclimatory capacity and vulnerability to global climate change. Biology Letters 4: 99–102.

    Article  PubMed  PubMed Central  Google Scholar 

  • Carbonell, J. A., C. Gutiérrez-Cánovas, D. Bruno, P. Abellán, J. Velasco & A. Millán, 2011. Ecological factors determining the distribution and assemblages of the aquatic hemiptera (Gerromorpha & Nepomorpha) in the Segura river basin (Spain). Limnetica 30: 59–70.

    Google Scholar 

  • Carbonell, J. A., S. Guareschi, C. Coccia, D. Sánchez-Fernández, J. Velasco, L. Boyero, A. J. Green & A. Millán, (2012a). Distribución de Trichocorixa verticalis verticalis (Fieber, 1851) (Heteroptera: Corixidae) a nivel mundial y su expansión en la Península Ibérica. (2012) En: GEIB Grupo Especialista en Invasiones Biológicas (ed) EEI 2012 Notas Científicas. 148–152. 4º Congreso Nacional sobre Especies Exóticas Invasoras “EEI 2012”. GEIB, Serie Técnica Nº 5. León: 218 pp.

  • Carbonell, J. A., A. Millán & J. Velasco, 2012b. Concordance between realised and fundamental niches in three Iberian Sigara species (Hemiptera: Corixidae) along a gradient of salinity and anionic composition. Freshwater biology 57: 2580–2590.

    Article  Google Scholar 

  • Castro-Longoria, E., 2003. Egg production and hatching success of four Acartia species under different temperature and salinity regimes. Journal of Crustacean Biology 23: 289–299.

    Article  Google Scholar 

  • Chown, S. L. & W. N. Nicolson, 2004. Insect Physiological Ecology: Mechanisms and Patterns. Oxford University Press, U.K.

    Book  Google Scholar 

  • Chown, S. L. & J. S. Terblanche, 2007. Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology 33: 50–152.

    Article  Google Scholar 

  • Coccia, C., P. Calosi, L. Boyero, A. J. Green & D. T. Bilton, 2013. Does ecophysiology determine invasion success? A comparison between the invasive boatman Trichocorixa verticalis verticalis and the Native Sigara lateralis (Hemiptera, Corixidae) in South-West Spain. PLoS One 8(5): e63105.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Coccia, C., L. Boyero & A. J. Green, 2014. Can differential predation of native and alien corixids explain the success of Trichocorixa verticalis verticalis in the Iberian Peninsula? Hydrobiologia 734: 115–123.

    Article  Google Scholar 

  • Dolédec, S., D. Chessel & C. Gimaret-Carpentier, 2000. Niche separation in community analysis: a new method. Ecology 81: 2914–2927.

    Article  Google Scholar 

  • Dudgeon, D., A. H. Arthington, M. O. Gessner, Z. Kawabata, D. J. Knowler, C. Lévêque, R. J. Naiman, A. H. Prieur-Richard, D. Soto, M. L. J. Stiassny & C. A. Sullivan, 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological reviews of the Cambridge Philosophical Society 81: 163–182.

    Article  PubMed  Google Scholar 

  • Espinar, J. L., R. Díaz-Delgado, M. A. Bravo-Utrera & M. Vilà, 2015. Linking Azolla filiculoides invasion to increased winter temperatures in the Doñana marshland (SW Spain). Aquatic Invasions. doi:10.3391/ai.2015.10.1.02.

    Google Scholar 

  • Figuerola, J., A. J. Green & L. Santamaria, 2003. Passive internal transport of aquatic organisms by waterfowl in Doñana, south–west Spain. Global Ecology and Biogeography 12: 427–436.

    Article  Google Scholar 

  • Gelin, A., A. J. Crivelli, E. Rosecchi & P. Kerambrun, 2001. Can salinity changes affect reproductive success in the brown shrimp Crangon crangon? Journal of Crustacean Biology 21: 905–911.

    Article  Google Scholar 

  • Gérard, C., A. Blanc & K. Costil, 2003. Potamopyrgus antipodarum (Mollusca: Hydrobiidae) in continental aquatic gastropod communities: impact of salinity and trematode parasitism. Hydrobiologia 493: 167–172.

    Article  Google Scholar 

  • Gibb, H., J. Hjalten, J. P. Ball, R. B. Pettersson, J. Landin, O. Alvini & K. Danell, 2006. Wing loading and habitat selection in forest beetles: are red-listed species poorer dispersers or more habitat-specific than common congenerics? Biological Conservation 132: 250–260.

    Article  Google Scholar 

  • Guareschi, S., C. Coccia, D. Sánchez-Fernández, J. A. Carbonell, J. Velasco, L. Boyero, A. J. Green & A. Millán, 2013. How far could the alien boatman Trichocorixa verticalis verticalis spread? Worldwide estimation of its current and future potential distribution. PLoS One 8(3): e59757. doi:10.1371/journal.pone.0059757.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Guareschi, S., P. Abellán, A. Laini, A. J. Green, J. A. Sánchez-Zapata, J. Velasco & A. Millán, 2015. Cross-taxon congruence in wetlands: assessing the value of waterbirds as surrogates of macroinvertebrate biodiversity in Mediterranean Ramsar sites. Ecological Indicators 49: 204–215.

    Article  Google Scholar 

  • Günther, H., 2004. Trichocorixa verticalis verticalis (Fieber), eine nearktische Ruderwanze in Europa (Heteroptera: Corixidae). Mitteilungen des Internationalen Entomologischen Verereins 29: 45–49.

    Google Scholar 

  • Havel, J. E. & J. B. Shurin, 2004. Mechanisms, effects, and scales of dispersal in freshwater zooplankton. Limnology and Oceanography 49: 1229–1238.

    Article  Google Scholar 

  • Havel, J. E., K. E. Kovalenko, S. M. Thomaz, S. Amalfitano & L. B. Kats, 2015. Aquatic invasive species: challenges for the future. Hydrobiologia 750: 147–170.

    Article  Google Scholar 

  • Hoffsten, P., 2004. Site-occcupancy in relation to flight-morphology in caddisflies. Freshwater Biology 49: 810–817.

    Article  Google Scholar 

  • Hutchinson, G. E., 1931. On the occurrence of Trichocorixa kirkaldy (Corixidae, Hemiptera-Heteroptera) in salt water and its zoo-geo-graphical significance. American Naturalist 65: 573–5749.

    Article  Google Scholar 

  • Jansson, A., 2002. New records of Corixidae (Heteroptera) from northeastern USA and eastern Canada, with one new synonymy. Entomologica Fennica 13: 85–88.

    Google Scholar 

  • Kelts, L. J., 1979. Ecology of a tidal marsh corixid, Trichocorixa verticalis (Insecta, Hemiptera). Hydrobiologia 64: 37–57.

    Article  Google Scholar 

  • L’Mohdi, O., N. Bennas, O. Himmi, K. Hajji, M. El Haissoufi, C. Hernando, J. A. Carbonell & A. Millán, 2010. Trichocorixa verticalis verticalis (Fieber 1851) (Hemiptera, Corixidae): une nouvelle especie exotique au Maroc. Boletín de la Sociedad Entomológica Aragonesa 46: 395–400.

    Google Scholar 

  • Macan, T. T., 1976. A Revised Key to the British Water Bugs (Hemiptera-Heteroptera) with Notes on their Ecology, Vol. 16. Freshwater Biological Association Scientific Publication, Ambleside.

    Google Scholar 

  • Martínez, I., 2002. Técnicas básicas de anatomía microscópica y de morfometría para estudiar los insectos. Boletín de la Sociedad Entomológica Aragonesa 30: 187–195.

    Google Scholar 

  • Millán, A., J. Velasco, N. Nieser & C. Montes, 1988. Heterópteros acuáticos (Gerromorpha & Nepomorpha) de la Cuenca del Río Segura. S.E. de la Península Ibérica. Anales de Biología 11: 71–80.

    Google Scholar 

  • Millán, A., C. Hernándo, P. Aguilera, A. Castro & I. Ribera, 2005. Los coleópteros acuáticos y semiacuáticos de Doñana: reconocimiento de su biodiversidad y prioridades de conservación. Boletín de la Sociedad Entomológica Aragonesa 36: 157–164.

    Google Scholar 

  • Moreno, J. L., A. Millán, M. L. Suarez, R. Vidal-Abarca & J. Velasco, 1997. Aquatic Coleoptera and Heteroptera assemblages in waterbodies from ephemeral coastal streams (“ramblas”) of south-eastern Spain. Archiv für Hydrobiologie 141: 93–107.

    Google Scholar 

  • Nieser, N., M. Baena, J. Martínez-Avilés & A. Millán, 1994. Claves para la identificación de los heterópteros acuáticos (nepomorpha & gerromorpha) de la Península Ibérica–Con notas sobre las especies de las Islas Azores, Baleares, Canarias y Madeira. Asociación Española de Limnología, Madrid.

    Google Scholar 

  • Pajunen, V. I. & A. Jansson, 1969. Dispersal of the rock pool corixids Arctocorixa carinata (Sahlb.) and Callicorixa producta (Reut.) (Heteroptera, Corixidae). Annales Zoologici Fennici 6: 391–427.

    Google Scholar 

  • Parker, I. M., D. Simberloff, W. M. Lonsdale, K. Goodell, M. Wonham, P. M. Kareiva, M. H. Williamson, B. Von Holle, P. B. Moyle, J. E. Byers & L. Goldwasser, 1999. Impact: toward a framework for understanding the ecological effects of invaders. Biological Invasions 1: 3–9.

    Article  Google Scholar 

  • Popham, E. J., 1964. The migration of aquatic bugs with special reference to the Corixidae (Hemiptera Heteroptera). Archiv für Hydrobiologie 60: 450–496.

    Google Scholar 

  • Rabitsch, W., 2008. Alien true bugs of Europe (Insecta: Hemiptera: Heteroptera). Zootaxa 1827: 1–44.

    Google Scholar 

  • Quinn, G. & M. J. Keough, 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge. 537 pp.

    Book  Google Scholar 

  • R Core Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org.

  • Ricciardi, A., 2006. Are modern biological invasions an unprecendent form of global change? Conservation Biology 21: 329–336.

    Article  Google Scholar 

  • Richards, D. C., 2002. The New Zealand mudsnail invades the Western United States. Aquatic Nuisance Species 4: 42–44.

    Google Scholar 

  • Rodríguez-Pérez, H. & A. J. Green, 2012. Strong seasonal effects of waterbirds on benthic communities in shallow lakes. Freshwater Science 31: 1273–1288.

    Article  Google Scholar 

  • Rodríguez-Pérez, H., M. Florencio, C. Gómez-Rodríguez, A. J. Green, C. Día-Paniagua & L. Serrano, 2009. Monitoring the invasion of the aquatic bug Trichocorixa verticalis verticalis (Hemiptera: Corixidae) in the wetlands of Doñana National Park (SW Spain). Hydrobiologia 634: 209–217.

    Article  Google Scholar 

  • Sakai, A. K., F. W. Allendorf, J. S. Holt, D. M. Lodge, J. Molofsky, K. A. With, S. Baughman, R. J. Cabin, J. E. Cohen, N. C. Ellstrand, D. E. McCauley, P. O’Neil, I. M. Parker, J. N. Thompson & S. G. Weller, 2001. The population biology of invasive species. Annual Review of Ecology and Systematics 32: 305–332.

    Article  Google Scholar 

  • Sala, J. & D. Boix, 2005. Presence of the nearctic water boatman Trichocorixa verticalis verticalis (Fieber, 1951) (Heteroptera, Corixidae) in the Algarve region (S Portugal). Graellsia 61: 31–36.

    Article  Google Scholar 

  • Sánchez-Fernández, D., P. Calosi, A. Atfield, P. Arribas, J. Velasco, J. I. Spicer, A. Millán & D. T. Bilton, 2010. Reduced salinities compromise the thermal tolerance of hypersaline specialist diving beetles. Physiological Entomology 35: 265–273.

    Article  Google Scholar 

  • Sánchez, M., C. Coccia, A. G. Valdecasas, L. Boyero & A. J. Green, 2015. Parasitism by water mites in native and exotic Corixidae: are mites limiting the invasion of the water boatman Trichocorixa verticalis (Fieber, 1851)? Journal of Insect Conservation. doi:10.1007/s10841-015-9764-7.

    Google Scholar 

  • Scudder, G. G. E., 1983. A review of factors governing the distribution of two closely related corixids in the saline lakes of British Columbia. Hydrobiologia 105: 143–154.

    Article  Google Scholar 

  • Simonis, J. L., 2013. Predator ontogeny determines trophic cascade strength in freshwater rock pools. Ecosphere 4: 1–25.

    Article  Google Scholar 

  • Thioulouse, J., D. Chessel, S. Dolédec & J. M. Olivier, 1997. ADE-4: a multivariate analysis and graphical display software. Statistics and Computing 7: 75–83.

    Article  Google Scholar 

  • Tones, P. I., 1977. Life-cycle of Trichocorixa verticalis interiores Sailer (Hemiptera: Corixidae) with special reference to diapause. Freshwater Biology 7: 31–36.

    Article  Google Scholar 

  • Van de Meutter, F., H. Trekels & A. Green, 2010a. The impact of the North American waterbug Trichocorixa verticalis (Fieber) on aquatic macroinvertebrate communities in southern Europe. Fundamental and Applied Limnology 177: 283–292.

    Article  Google Scholar 

  • Van de Meutter, F., H. Trekels, A. Green & R. Stoks, 2010b. Is salinity tolerance the key to success for the invasive water bug Trichocorixa verticalis? Hydrobiologia 649: 231–238.

    Article  Google Scholar 

  • Velasco, J., A. Millán & N. Nieser, 1990. Observaciones sobre la colonización y el ciclo de vida de Heliocorisa vermiculata (puton, 1874) (Heteroptera, Corixidae) en pequeños estanques del se español. Limnetica 6: 101–108.

    Google Scholar 

  • Weigelhofer, G., W. Weissmair & J. Waringer, 1992. Night migration activity and the influence of meteorological parameters on light-trapping for aquatic Heteroptera. Zoologischer Anzeiger 229: 209–218.

    Google Scholar 

  • Williams, D. D., 2006. The Biology of Temporary Waters. Biology, Oxford.

    Google Scholar 

  • Wilson, P. W., A. F. Heneghan & A. D. J. Haymet, 2003. Ice nucleation in nature: supercooling point (SCP) measurements and the role of heterogeneous nucleation. Cryobiology 46: 88–98.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Raquel López, Susana Pallarés, Simone Guareschi, Cayetano Gutiérrez-Cánovas and Félix Picazo for field and laboratory assistance; Paula Arribas, David Sánchez-Fernández, Pedro Abellán and David Bilton for their help and suggestions; José Galián for technical support and the members of the Aquatic Ecology research group (Universidad de Murcia, Spain) and the Wetlands Ecology department (EBD—CSIC, Seville, Spain) for their help at various stages of this project. This work was partially supported by funding from a predoctoral FPU grant to J.A. Carbonell, a JAE predoctoral grant to C. Coccia, an 11º Arquímedes young investigators award to V. Céspedes and projects P10-RNM-6262 (Consejería de Innovación, Ciencia y empresa, Junta de Andalucía), “Atlas de los coleópteros acuáticos de España peninsular” (A.M.) (Ministerio de Agricultura, Alimentación y Medio Ambiente) and CGL2010-15378 (J.V.) cofinanced by FEDER funds.

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Authors and Affiliations

  1. Department of Ecology and Hydrology, University of Murcia, Murcia, Spain

    J. A. Carbonell, A. Millán & J. Velasco

  2. Department of Wetland Ecology, Doñana Biological Station (EBD-CSIC), Seville, Spain

    A. J. Green, V. Céspedes & C. Coccia

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  1. J. A. Carbonell
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  2. A. Millán
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  3. A. J. Green
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  4. V. Céspedes
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  5. C. Coccia
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  6. J. Velasco
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Correspondence to J. A. Carbonell.

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Carbonell, J.A., Millán, A., Green, A.J. et al. What traits underpin the successful establishment and spread of the invasive water bug Trichocorixa verticalis verticalis?. Hydrobiologia 768, 273–286 (2016). https://doi.org/10.1007/s10750-015-2556-y

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