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Hydrobiologia

, Volume 813, Issue 1, pp 189–198 | Cite as

Native macrophyte leaves influence more specialisation of neotropical shredder chironomids than invasive macrophyte leaves

  • Hugo Henrique Lanzi Saulino
  • Susana Trivinho-Strixino
Primary Research Paper

Abstract

We investigated the composition and specialisation of shredder chironomids in an invasive white ginger lily (Hedychium coronarium) and in native pickerelweed (Pontederia cordata) leaves. We assumed that the difference of the chemical compound in macrophyte leaves would influence the shredder specialisation. A colonisation experiment was performed over 3 years (2013–2015) using 40 bags for each macrophyte species. The main macrophyte leaf chemical compounds (organic matter, nitrogen, phosphorus, cellulose, lignin, soluble polyphenols and soluble carbohydrates) were measured. The herbivore specialisation was estimated using the individual specialisation index (d′) and community specialisation index (H2′). White ginger lily had higher nitrogen and organic matter, resulting in a higher abundance of shredder specimens and lower specialisation than in native leaves. The Polypedilum fallax group, Stenochironomus and Endotribelos calophylli presented high individual specialisation (d′) in pickerelweed leaves, resulting in high community specialisation (H2′). The heterotrophic facilitation hypothesis explained the herbivores thriving in pickerelweed leaves due to their lower nutritional value. The intake-efficiency hypothesis explained the higher consumption of invasive plant tissue by Stenochironomus, due to its mining habit. We found evidence of evolutionary adaptation of freshwater herbivore eating habits.

Keywords

Freshwater herbivory Hedychium coronarium Herbivore adaptations Macroinvertebrates Stenochironomus 

Notes

Acknowledgements

We would like to thank the Brazilian National Council for Technological and Scientific Development (CNPq) for the financial support throughout the research project process 141020/2013. Susana Trivinho-Strixino has a productivity grant awarded by CNPq (Process Number: 306402/2010-6). We would also like to thank Rebecca Clement from Brigham Young University who provided the first English language reviews.

Author contribution

Saulino, HHL and Trivinho-Strixino, S designed the experiments and wrote the manuscript. Saulino, HHL performed the experiments and analysed the dates.

Compliance with ethical standards

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Association of Official Agricultural Chemists, 1995. Official Methods of Analysis of the AOAC. AOAC International, Arlington: 1–30.Google Scholar
  2. Bakker, E. S., K. A. Wood, J. F. Pagès, G. C. Veen, M. J. Christianen, L. Santamaría, B. A. Nolet & S. Hilt, 2016. Herbivory on freshwater and marine macrophytes: A review and perspective. Aquatic Botany 135: 18–36.CrossRefGoogle Scholar
  3. Biasi, C., A. M. Tonin, R. M. Restello & L. U. Hepp, 2013. The colonisation of leaf litter by Chironomidae (Diptera): the influence of chemical quality and exposure duration in a subtropical stream. Limnologica-Ecology and Management of Inland Waters 43: 427–433.CrossRefGoogle Scholar
  4. Borkent, A., 1984. The systematics and phylogeny of the Stenochironomus complex (Xestochironomus, Harrisius, and Stenochironomus) (Diptera: Chironomidae). Memoirs of the Entomological Society of Canada 116: 5–270.CrossRefGoogle Scholar
  5. Boyero, L., L. A. Barmuta, L. Ratnarajah, K. Schmidt & R. G. Pearson, 2012. Effects of exotic riparian vegetation on leaf breakdown by shredders: a tropical–temperate comparison. Freshwater Science 31: 296–303.CrossRefGoogle Scholar
  6. Blüthgen, N., F. Menzel & N. Blüthgen, 2006. Measuring specialization in species interaction networks. BMC Ecology 6: 1–12.CrossRefGoogle Scholar
  7. Carlsson, N. O. & J. O. Lacoursiere, 2005. Herbivory on aquatic vascular plants by the introduced golden apple snail (Pomacea canaliculata) in Lao PDR. Biological Invasions 7: 233–241.CrossRefGoogle Scholar
  8. Carreira, B. M., M. P. Dias & R. Rebelo, 2014. How consumption and fragmentation of macrophytes by the invasive crayfish Procambarus clarkii shape the macrophyte communities of temporary ponds. Hydrobiologia 721: 89–98.CrossRefGoogle Scholar
  9. Choi, C., C. Bareiss, O. Walenciak & E. M. Gross, 2002. Impact of polyphenols on growth of the aquatic herbivore Acentria ephemerella. Journal of Chemical Ecology 28: 2245–2256.CrossRefPubMedGoogle Scholar
  10. Chung, N. & K. Suberkropp, 2009. Contribution of fungal biomass to the growth of the shredder Pycnopsyche gentilis(Trichoptera: Limnephilidae). Freshwater Biology 54: 2212–2224.CrossRefGoogle Scholar
  11. Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in community structure. Austral Journal of Ecology 18: 117–143.CrossRefGoogle Scholar
  12. Coelho-Silva, J. F., 1967. Noções Sobre Análise de Alimentos. Imprensa Universitária da Universidade Rural do Estado de Minas Gerais, Viçosa.Google Scholar
  13. Corbi, J. J. & S. Trivinho-Strixino, 2017. Chironomid species are sensitive to sugarcane cultivation. Hydrobiologia 785: 91–99.CrossRefGoogle Scholar
  14. Cornut, J., V. Ferreira, A. L. Gonçalves, E. Chauvet & C. Canhoto, 2015. Fungal alteration of the elemental composition of leaf litter affects shredder feeding activity. Freshwater Biology 60: 1755–1771.CrossRefGoogle Scholar
  15. de Castro, W. A. C., R. V. Almeida, M. B. Leite, R. H. Marrs & D. M. S. Matos, 2016. Invasion strategies of white ginger lily (Hedychium coronarium) J. König (Zingiberacea) under different competitive and environmental conditions. Environment and Experimental Botany 127: 55–62.CrossRefGoogle Scholar
  16. Dormann, C. F., J. Fruend, B. Gruber, M. C. F. Dormann & T. R. U. E. LazyData, 2016. Package ‘bipartite’.Google Scholar
  17. Dubois, M., K. A. Gilles, J. K. Hamilton, P. A. Rebers & F. Smith, 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28: 350–356.CrossRefGoogle Scholar
  18. Friedlin, B. & J. L. Gastwirth, 2000. Should the median test be retired from general use? The American Statistician 54: 161–164.Google Scholar
  19. Gonçalves Jr., J. F., R. S. Rezende, J. França & M. Callisto, 2012. Invertebrate colonization during leaf processing of native, exotic and artificial detritus in a tropical stream. Marine and Freshwater Research 65: 428–439.CrossRefGoogle Scholar
  20. Hammer, Ø., D. A. T Harper & P. D. Ryan, 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1): 9 pp.Google Scholar
  21. König, R., L. U. Hepp & S. Santos, 2014. Colonisation of low-and high-quality detritus by benthic macroinvertebrates during leaf breakdown in a subtropical stream. Limnologica-Ecology and Management of Inland Waters 45: 61–68.CrossRefGoogle Scholar
  22. Koroiva, R., C. W. O. Souza, D. Toyama, F. Henrique-Silva & A. A. Fonseca-Gessner, 2013. Lignocellulolytic enzymes and bacteria associated with the digestive tracts of Stenochironomus (Diptera: Chironomidae) larvae. Genetics and Molecular Research 12: 3421–3434.CrossRefPubMedGoogle Scholar
  23. Kozovtis, A. R., M. M. C. Bustamente, C. R. Garofalo, S. Bucci, A. C. Franco, G. Goldstein & F. C. Meinzer, 2007. Nutrient reabsorption and patterns of litter production and decomposition in a Neotropical Savanna. Functional Ecology 21: 1034–1043.CrossRefGoogle Scholar
  24. Kubanek, J., M. E. Hay, P. J. Brown, N. Lindquist & W. Fenical, 2001. Lignoid chemical defenses in the freshwater macrophyte Saururus cernuus. Chemoecology 11: 1–8.CrossRefGoogle Scholar
  25. Kuehne, L. M., J. D. Olden & E. S. Rubenson, 2016. Multi-trophic impacts of an invasive aquatic plant. Freshwater Biology 61: 1846–1861.CrossRefGoogle Scholar
  26. Leite-Rossi, L. A. & S. Trivinho-Strixino, 2012. Are sugarcane leaf-detritus well colonized by aquatic macroinvertebrates? Acta Limnologica Brasiliensia 24: 303–313.CrossRefGoogle Scholar
  27. Leite-Rossi, L. A., V. S. Saito, M. B. Cunha-Santino & S. Trivinho-Strixino, 2016. How does leaf litter chemistry influence its decomposition and colonization by shredder Chironomidae (Diptera) larvae in a tropical stream? Hydrobiologia 77: 119–130.CrossRefGoogle Scholar
  28. Lodge, D. M., 1991. Herbivory on freshwater macrophytes. Aquatic Botany 41: 195–224.CrossRefGoogle Scholar
  29. Lorenzi, H., 1991. Plantas daninhas do Brasil: terrestres, aquáticas, parasitas, tóxicas e medicinais. Instituto Plantarum, Nova Odessa.Google Scholar
  30. Lorenzi, H. & H. Souza, 2001. Plantas ornamentais. Plantarum, São Paulo.Google Scholar
  31. Makkar, H. P., M. Blümmel, N. K. Borowy & K. Becker, 1993. Gravimetric determination of tannins and their correlations with chemical and protein precipitation methods. Journal of the Science of Food and Agriculture 61: 161–165.CrossRefGoogle Scholar
  32. Martin-Creuzburg, D., B. Beck & H. M. Freese, 2011. Food quality of heterotrophic bacteria for Daphnia magna: evidence for a limitation by sterols. FEMS Microbiology Ecology 76: 592–601.CrossRefPubMedGoogle Scholar
  33. Matsuda, J. T., F. A. Lansac-Tôha, K. Martens, L. F. M. Velho, R. P. Mormul & J. Higuti, 2015. Association of body size and behavior of freshwater ostracods (Crustacea, Ostracoda) with aquatic macrophytes. Aquatic Ecology 49: 321–331.CrossRefGoogle Scholar
  34. Mertens, D. R., 2002. Gravimetric determination of amylase treated neutral detergent fiber in feeds with refluxing in beaker or crucibles: collaborative study. Journal of AOAC International 85: 1217–1240.PubMedGoogle Scholar
  35. Morrison, W. E. & M. E. Hay, 2011a. Induced chemical defenses in a freshwater macrophyte suppress herbivore fitness and the growth of associated microbes. Oecologia 165: 427–436.CrossRefPubMedGoogle Scholar
  36. Morrison, W. E. & M. E. Hay, 2011b. Herbivore preference for native vs. exotic plants: generalist herbivores from multiple continents prefer exotic plants that are evolutionarily naïve. PLoS One 6: e17227.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Morrison, W. E. & M. E. Hay, 2012. Are lower-latitude plants better defended? Palatability of freshwater macrophytes. Ecology 93: 65–74.CrossRefPubMedGoogle Scholar
  38. Provenza, F. D., J. J. Villalba, L. E. Dziba, S. B. Atwood & R. E. Banner, 2003. Linking herbivore experience, varied diets, and plant biochemical diversity. Small Ruminant Research 49: 257–274.CrossRefGoogle Scholar
  39. R Development Core Team, 2014. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria [available on internet at http://www.R-project.org] (accessed 26.10.16).
  40. Robertson, J. B. & P. J. Van Soest, 1981. The detergent system of analysis and its application to human foods. In James, W. P. T. & O. Theander (eds), The Analysis of Dietary Fiber in Food. Marcel Deller, New York: 123–158.Google Scholar
  41. Sanchez, J. L. & J. C. Trexler, 2016. The adaptive evolution of herbivory in freshwater systems. Ecosphere.  https://doi.org/10.1002/ecs2.1414.Google Scholar
  42. Sarruge, J. R. & H. P. Haag, 1974. Análises Químicas em Plantas, Escola Superior de Agricultura Luiz de Queiroz. Universidade de São Paulo, Piracicaba.Google Scholar
  43. Saulino, H. H. L., J. J. Corbi & S. Trivinho-Strixino, 2014. Aquatic insect community structure under the influence of small dams in a stream of the Mogi-Guaçu river basin, state of São Paulo. Brazilian Journal of Biology 74: 79–88.CrossRefGoogle Scholar
  44. Theel, H. J., E. D. Dibble & J. D. Madsen, 2008. Differential influence of a monotypic and diverse native aquatic plant bed on a macroinvertebrate assemblage: an experimental implication of exotic plant induced habitat. Hydrobiologia 600: 77–87.CrossRefGoogle Scholar
  45. Tiner, R. W., 1991. The concept of a hydrophyte for wetland identification. Bioscience 41: 236–247.CrossRefGoogle Scholar
  46. Trivinho-Strixino, S., 2014. Ordem Diptera. Família Chironomidae. Guia de identificação de larvas. In Hamada, N., J. L. Nessimian, & R. B. Querino (eds), Insetos Aquáticos na Amazônia brasileira: taxonomia, biologia e ecologia. Editora do INPA, Manaus: 457–660Google Scholar
  47. Zenni, R. D. & S. R. Ziller, 2011. An overview of invasive plants in Brazil. Brazilian Journal of Botany 34: 431–446.CrossRefGoogle Scholar
  48. Wetzel, R. G., 1983. Limnology, 2nd ed. W. B. Saunders, Philadelphia.Google Scholar
  49. Wong, P. K., Y. A. N. Liang, N. Y. Liu & J. W. Qiu, 2010. Palatability of macrophytes to the invasive freshwater snail Pomacea canaliculata: differential effects of multiple plant traits. Freshwater Biology 55: 2023–2031.CrossRefGoogle Scholar
  50. Wood, K. A., M. T. O’Hare, C. McDonald, K. R. Searle, F. Daunt & R. A. Stillman, 2016. Herbivore regulation of plant abundance in aquatic ecosystems. Biological Reviews.  https://doi.org/10.1111/brv.12272.PubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Hugo Henrique Lanzi Saulino
    • 1
  • Susana Trivinho-Strixino
    • 2
  1. 1.Programa de Pós-Graduação em Ecologia e Recursos NaturaisUniversidade Federal de São CarlosSão CarlosBrazil
  2. 2.Laboratório de Ecologia de Insetos aquáticos, Departamento de HidrobiologiaUniversidade Federal de São CarlosSão CarlosBrazil

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