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The life cycle of the alien boatman Trichocorixa verticalis (Hemiptera, Corixidae) in saline and hypersaline wetlands of south-west Spain

  • Vanessa Céspedes
  • Cristina Coccia
  • José Antonio Carbonell
  • Marta I. Sánchez
  • Andy J. Green
Primary Research Paper

Abstract

Trichocorixa verticalis (Corixidae) is native to North America but is well established as an alien in the Western Mediterranean region, where it is invasive in permanent coastal wetlands with high salinities. We investigated the annual cycle and generation time of T. verticalis in the introduced range in south-west Spain, through a combination of field surveys and laboratory experiments. Field surveys were conducted on a monthly basis over 1 year in three saline fish ponds in Doñana and four hypersaline salt ponds in the Odiel marshes. Adults were present all year round, whereas nymphs were only absent in August, when temperatures and salinities were high. Adult sex ratios were idiosyncratic and often male or female biased for a given location and month. Adults were smaller during summer months. Laboratory experiments revealed an oviposition rate of 11.5 eggs per day and a generation time of about 54 days from egg to adult, suggesting T. verticalis may complete around six generations per year in permanent wetlands. A combination of a high oviposition rate and continuous reproduction throughout the year gives T. verticalis an advantage over native corixid competitors (Sigara spp), and appears to explain the success of this alien aquatic insect.

Keywords

Trichocorixa verticalis Fecundity Fish ponds Generation time Invasive species Salt ponds Life cycle 

Notes

Acknowledgements

E. Martinez (Director of Marismas del Odiel Natural Park) and Doñana Natural Space provided permission for fieldwork. J. Miguel Medialdea and Pesquerías Isla Mayor, S.A. provided facilities in VLP. Miguel Lozano Terol, Raquel López Luque, Natalia Ospina-Alvarez, and Simona Kacmarcikova helped with laboratory and fieldwork. Andres Millán and Josefa Velasco provided helpful advice. Ruben Izquierdo and the “MiBuho” company provided the graphic design for Fig. 7. The staff of the Aquatic Ecology (LEA-EBD) and GIS and Remote Sensing (LAST-EBD) laboratories of EBD-CSIC provided essential support. This research was funded by the Consejería de Innovación, Ciencia y Empresa, Junta de Andalucía project (P10-RNM-6262) to AJG, a Severo Ochoa predoctoral contract (SVP-2013-067595) from the Spanish Ministry of Science and Innovation (MICINN) to VC, a JAE predoctoral grant from CSIC and a post doc project 3160330 financed by FONDECYT to CC, a predoctoral FPU grant to JAC and a Ramón y Cajal postdoctoral contract from MICINN to MIS. Two anonymous referees greatly improved an earlier version of the manuscript.

Supplementary material

10750_2018_3782_MOESM1_ESM.docx (34 kb)
Supplementary material 1 (DOCX 34 kb)

References

  1. Aiken, R. B. & N. Malatestinic, 1995. Life history, gonad state, and changes in functional sex ratio in the salt-marsh waterboatman, Trichocorixa verticalis (Fieber) (Heteroptera: Corixidae). Canadian Journal of Zoology 73: 552–556.CrossRefGoogle Scholar
  2. Apha, A., 1995. WPCF, standard methods for the examination of water and wastewater. American Public Health Association, Washington, DC.Google Scholar
  3. Barahona, J., A. Millan & J. Velasco, 2005. Population dynamics, growth and production of Sigara selecta (Fieber, 1848) (Hemiptera, Corixidae) in a Mediterranean hypersaline stream. Freshwater Biology 50: 2101–2113.CrossRefGoogle Scholar
  4. Bij de Vaate, A., K. Jazdzewski, H. A. Ketelaars, S. Gollasch & G. Van der Velde, 2002. Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Canadian Journal of Fisheries and Aquatic Sciences 59(7): 1159–1174.CrossRefGoogle Scholar
  5. 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(4): 301–314.CrossRefGoogle Scholar
  6. Boros, E., S. Andrikovics, B. Kiss & L. Forro, 2006. Feeding ecology of migrating waders (Charadrii) at sodic-alkaline pans in the Carpathian Basin. Bird Study 53: 86–91.CrossRefGoogle Scholar
  7. Carbonell, J. A., A. Millán, A. J. Green, V. Céspedes, C. Coccia & J. Velasco, 2016. What traits underpin the successful establishment and spread of the invasive water bug Trichocorixa verticalis verticalis? Hydrobiologia 768: 273–286.CrossRefGoogle Scholar
  8. Carbonell, J. A., J. Velasco, A. Millán, A. J. Green, C. Coccia, S. Guareschi & C. Gutiérrez-Cánovas, 2017. Biological invasion modifies the co-occurrence patterns of insects along a stress gradient. Functional Ecology 31: 1957–1968.CrossRefGoogle Scholar
  9. Céspedes, V., M. I. Sánchez & A. J. Green, 2017. Predator-prey interactions between native brine shrimp Artemia parthenogenetica and the alien boatman Trichocorixa verticalis: influence of salinity, predator sex, and size, abundance and parasitic status of prey. PeerJ 5: e3554.CrossRefGoogle Scholar
  10. Céspedes, V., Valdecasas, A.G., Green, A.J. & Sánchez, M.I. submitted. Effects of water mite parasites and salinity stress on aquatic insects.Google Scholar
  11. 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.CrossRefGoogle Scholar
  12. Coccia, C., L. Boyero & A. J. Green, 2014. Can differential predation of native and alien corixids explain the success of Trichocorixa verticalis verticalis (Hemiptera, Corixidae) in the Iberian Peninsula? Hydrobiologia 734(1): 115–123.CrossRefGoogle Scholar
  13. Coccia, C., B. Fry, F. Ramírez, L. Boyero, S. E. Bunn, C. Diz-Salgado, M. Walton, L. Le Vay & A. J. Green, 2016a. Niche partitioning between invasive and native corixids (Hemiptera, Corixidae) in south-west Spain. Aquatic Sciences 78: 779–791.CrossRefGoogle Scholar
  14. Coccia, C., B. Vanschoenwinkel, L. Brendonck, L. Boyero & A. J. Green, 2016b. Newly created ponds complement natural waterbodies for restoration of macroinvertebrate assemblages. Freshwater Biology 61: 1640–1654.CrossRefGoogle Scholar
  15. Drake, J. A., H. A. Mooney, F. di Castri, R. H. Groves, F. J. Kruger, M. Rejmánek & M. Williamson (eds), 1989. Biological invasions: a global perspective. Wiley, Chichester.Google Scholar
  16. Espinar, J. L., R. Diaz-Delgado, et al., 2015. Linking Azolla filiculoides invasion to increased winter temperatures in the Donana marshland (SW Spain). Aquatic Invasions 10(1): 17–24.CrossRefGoogle Scholar
  17. Euliss, N. H. & R. L. Jarvis, 1991. Feeding ecology of waterfowl wintering on evaporation ponds in California. Condor 93: 582–590.CrossRefGoogle Scholar
  18. Fernando, C. H., 1959. The colonization of small freshwater habitats by aquatic insects, 2. Hemiptera (The water bugs). Ceylon Journal of Science 2: 5–32.Google Scholar
  19. Fuentes, C., M. I. Sanchez, N. Selva & A. J. Green, 2004. The diet of the Marbled Teal Marmaronetta angustirostris in southern Alicante, eastern Spain. Revue D’ Ecologie-La Terre Et La Vie 59: 475–490.Google Scholar
  20. Giles, N., M. Street & R. M. Wright, 1990. Diet composition and prey preference of tench, Tinca tinca (L.), common bream, Abramis brama (L.), perch, Perca fluviatilis L. and roach, Rutilus rutilus (L.), in two contrasting gravel pit lakes: potential trophic overlap with wildfowl. Journal of Fish Biology 37(6): 945–957.CrossRefGoogle Scholar
  21. Grabowski, M., K. Bacela & A. Konopacka, 2007. How to be an invasive gammarid (Amphipoda: Gammaroidea)–comparison of life history traits. Hydrobiologia 590(1): 75–84.CrossRefGoogle Scholar
  22. Green, A. J., J. Bustamante, G. F. E. Janss, R. Fernández-Zamudio & C. Díaz-Paniagua, 2018. Doñana Wetlands (Spain). In Finlayson, C. M., G. R. Milton, R. C. Prentice & N. C. Davidson (eds), The Wetland Book: II: Distribution, Description and Conservation. Springer, New York.  https://doi.org/10.1007/978-94-007-4001-3_139.CrossRefGoogle Scholar
  23. Griffith, M. E., 1945. The environment, life history and structure of the water boatmen Ramphocorixa acuminata (Uhler) (Hemiptera Corixidae). The University of Kansas Science Bulletin 30: 241–365.Google Scholar
  24. 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: e59757.CrossRefGoogle Scholar
  25. Henrikson, L. & H. G. Oscarson, 1978. Fish predation limiting abundance and distribution of Glaenocorisa p. propinqua. Oikos 31(1): 102–105.CrossRefGoogle Scholar
  26. Henrikson, L. & H. G. Oscarson, 1981. Corixids (Hemiptera—Heteroptera), the new top predators in acidified lakes: with 2 tables in the text. Internationale Vereinigung für theoretische und angewandte Limnologie: Verhandlungen 21(3): 1616–1620.Google Scholar
  27. Horváth, Z., C. Lejeusne, F. Amat, J. Sanchez-Matamoros, C. F. Vad & A. J. Green, 2018. Eastern spread of the invasive Artemia franciscana in the Mediterranean Basin, with the first record from the Balkan Peninsula. Hydrobiologia.  https://doi.org/10.1007/s10750-018-3683-z.CrossRefGoogle Scholar
  28. Hutchinson, G. E., 1959. Homage to Santa Rosalia or Why are there so many kinds of animals? The American Naturalist 93: 145–149.CrossRefGoogle Scholar
  29. 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
  30. Jeschke, J. M., Gómez Aparicio, L., Haider, S., Heger, T., Lortie, C. J., Pyšek, P., & Strayer, D. L. 2012. Support for major hypotheses in invasion biology is uneven and declining.Google Scholar
  31. Kelts, L. J., 1979. Ecology of a tidal marsh corixid, Trichocorixa verticalis (Insecta, Hemiptera). Hydrobiologia 64: 37–57.CrossRefGoogle Scholar
  32. Kloskowski, J., A. J. Green, M. Polak, J. Bustamante & J. Krogulec, 2009. Complementary use of natural and artificial wetlands by waterbirds wintering in Doñana, south-west Spain. Aquatic Conservation: Marine and Freshwater Ecosystems 19: 815–826.CrossRefGoogle Scholar
  33. Kumari, P. & A. Kumer, 2003. Biodiversity of aquatic insects of Jharkhand state with reference to their ecological niche. Environment, pollution and management. APH Publishing Corporation, Delhi: 453–460.Google Scholar
  34. Melo, M. C. & E. E. Scheibler, 2011. Description of the immature instars of Sigara (Tropocorixa) jensenhaarupi (Hemiptera: Heteroptera: Corixidae: Corixini), with ecological notes. Revista Mexicana de Biodiversidad 82(1): 117–130.Google Scholar
  35. Munoz-Fuentes, V., A. J. Green, & J. J. Negro, 2013. Genetic studies facilitated management decisions on the invasion of the ruddy duck in Europe. Biological Invasions 15(4): 723–728.CrossRefGoogle Scholar
  36. Perán, A., 1997. Ciclos de vida y producción secundaria en un río de características semiáridas (Río Chícamo, SE de la Península Ibérica): El caso de Caenis luctuosa y Sigara scripta.M.S. dissertation, Universidad de Murcia, Murcia.Google Scholar
  37. Rajagopal, S., G. Van der Velde, B. G. P. Paffen, F. W. B. Van den Brink & A. Bij de Vaate, 1999. Life history and reproductive biology of the invasive amphipod Corophium curvispinum (Crustacea: Amphipoda) in the Lower Rhine. Archiv fur Hydrobiologie 144(4): 305–326.CrossRefGoogle Scholar
  38. Redon, S., F. Amat, M. I. Sanchez & A. J. Green, 2015. Comparing cestode infections and their consequences for host fitness in two sexual branchiopods: alien Artemia franciscana and native A. salina from syntopic-populations. Peerj 3: e1073.CrossRefGoogle Scholar
  39. Richardson, D. M. & P. Pyšek, 2006. Plant invasions: merging the concepts of species invasiveness and community invasibility. Progress in Physical Geography 30(3): 409–431.CrossRefGoogle Scholar
  40. Rodríguez-Pérez, H. & A. J. Green, 2012. Strong seasonal effects of waterbirds on benthic communities in shallow lakes. Freshwater Science 31: 1273–1288.CrossRefGoogle Scholar
  41. Rodríguez-Pérez, H., M. Florencio, C. Gómez-Rodríguez, A. J. Green, C. Díaz-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.CrossRefGoogle Scholar
  42. Sailer, R. I., 1948. The genus Trichocorixa (Corixidae, Hemiptera). The University of Kansas Science Bulletin 32: 289–407.Google Scholar
  43. Sánchez, M. I., A. J. Green & E. M. Castellanos, 2006a. Temporal and spatial variation of an aquatic invertebrate community subjected to avian predation at the Odiel salt pans (SW Spain). Archive für Hydrobiologie 166: 199–223.CrossRefGoogle Scholar
  44. Sanchez, M. I., A. J. Green & E. M. Castellanos, 2006b. Spatial and temporal fluctuations in presence and use of chironomid prey by shorebirds in the Odiel saltpans, south-west Spain. Hydrobiologia 567: 329–340.CrossRefGoogle Scholar
  45. Sánchez, M. I., 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 19(3): 433–447.CrossRefGoogle Scholar
  46. Simberloff, D., & B. Von Holle, 1999. Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions 1(1): 21–32.CrossRefGoogle Scholar
  47. Simonis, J. L., 2013. Predator ontogeny determines trophic cascade strength in freshwater rock pools. Ecosphere 4: 1–25.CrossRefGoogle Scholar
  48. Sims, G. K., T. R. Ellsworth, & R. L. Mulvaney, 1995. Microscale determination of inorganic nitrogen in water and soil extracts. Communications in Soil Science and Plant Analysis 26(1–2): 303–316.CrossRefGoogle Scholar
  49. Sweeney, B. W., & J. A. Schnack, 1977. Egg development, growth, and metabolism of Sigara Alternata (Say) (Hemiptera: Corixidae) in fluctuating thermal environments. Ecology 58: 265–277.CrossRefGoogle Scholar
  50. Talling, J. F., & D. Driver, 1963. Some problems in the estimation of chlorophyll a in phytoplankton. In Doty, M., (ed), Proceedings of the Conference on Primary Productivity Measurement, Marine and Freshwater, pp. 142–146. US Atomic Energy Engineering Commission, Honolulu, Hi.Google Scholar
  51. Tones, P. I., 1977. The life cycle of Trichocorixa verticalis interiores Sailer (Hemiptera, Corixidae) with special reference to diapause. Freshwater Biology 7: 31–36.CrossRefGoogle Scholar
  52. Van de Meutter, F., H. Trekels, A. Green & R. Stoks, 2010. Is salinity tolerance the key to success for the invasive water bug Trichocorixa verticalis? Hydrobiologia 649: 231–238.CrossRefGoogle Scholar
  53. Walton, M. E. M., C. Vilas, C. Coccia, A. J. Green, J. P. Cañavate, A. Prieto, S. A. van Bergeijk, J. M. Medialdea, H. Kennedy, J. King & L. Le Vay, 2015. The effect of water management on extensive aquaculture food webs in the reconstructed wetlands of the Doñana Natural Park, Southern Spain. Aquaculture 448: 451–463.CrossRefGoogle Scholar
  54. Ward, J. V. & J. A. Stanford, 1982. Thermal responses in the evolutionary ecology of aquatic insects. Annual Review Entomological 27: 97–117.CrossRefGoogle Scholar
  55. Williamson, M. H. & A. Fitter, 1996. The characters of successful invaders. Biological Conservation 78(1–2): 163–170.CrossRefGoogle Scholar
  56. Wurtsbaugh, W., 1992. Food-web modification by an invertebrate predator in the Great Salt Lake (USA). Oecologia 89: 168–175.CrossRefGoogle Scholar

Dataset

  1. Life cycle of T. verticalis; indoor-outdoor microcosms. http://digital.csic.es/handle/10261/162936
  2. Life cycle of T. verticalis; field-data approximation. http://digital.csic.es/handle/10261/162934
  3. Life cycle of T. verticalis; physico- chemical data. http://hdl.handle.net/10261/168612

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Wetland Ecology DepartmentEstación Biológica de Doñana, CSICSevilleSpain
  2. 2.Center of Applied Ecology and Sustainability (CAPES-UC)Pontificia Universidad Católica de ChileSantiagoChile
  3. 3.Laboratory of Evolutionary Stress Ecology and EcotoxicologyUniversity of LeuvenLeuvenBelgium
  4. 4.Department of Biology, Faculty of Marine and Environmental SciencesUniversity of CádizCádizSpain

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