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Revisiting Amazonian water types: experimental evidence highlights the importance of forest stream hydrochemistry in shaping adaptation in a fish species

  • Gabriel Stefanelli-SilvaEmail author
  • Jansen Zuanon
  • Tiago Pires
Primary Research Paper
  • 73 Downloads

Abstract

Following Alfred Russel Wallace, Amazonian freshwaters are classified into three types: black, white, and clear. Such waters have been demonstrated to affect adaptation and gene flow of the aquatic fauna. However, this classification focuses on large rivers and fails to acknowledge the importance of small forest streams that flow through upland terra firme forests, known as igarapés. Igarapés are surrounded by a distinct floristic composition when compared to the floodplains and contribute with a much greater water load to the Amazon basin than the Amazon River itself. We assessed the importance of blackwater, whitewater, and igarapé water on spawning and habitat choice in Crenuchus spilurus, a small fish composed of distinct genetic lineages that occur in igarapés flowing to blackwater and whitewater systems. Lineages from igarapés connected to the Rio Negro (blackwater) and Amazon River (whitewater) basins have greater spawning success in igarapé water than in the water from their surrounding floodplain. Habitat choice trials showed active selection of igarapé water by both lineages. Our results indicate that the hydrochemical condition of igarapés shapes adaptation in the physiology and behavior of C. spilurus. We suggest expanding upon the current classification to include igarapés as a distinct water type and environment.

Keywords

Igarapé Habitat type Choice experiments Reproductive isolation 

Notes

Acknowledgements

We are grateful to E. Borghezan for his assistance throughout the experiments, P. Friedemann for helping carry over three tons of water, K. Pinto for the Gpick guidance and J. da Silva for manuscript proofing. This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq (Fellowship number 130816/2016-7 to G.S.-S. and productivity Grant 313183/2014-7 to J.Z.) and the Science and Technology Research Partnership for Sustainable Development, SATREPS (Japan Science and Technology Agency/Japan International Cooperation Agency). This is contribution #57 of Projeto Igarapés.

Supplementary material

10750_2018_3860_MOESM1_ESM.docx (261 kb)
Supplementary material 1 (DOCX 260 kb)

References

  1. Barlow, J., T. Gardner, I. Araujo, T. Ávila-Pires, A. Bonaldo, J. Costa, M. Esposito, L. Ferreira, J. Hawes, M. Hernandez, M. Hoogmoed, R. Leite, N. Lo-Man-Hung, J. Malcolm, M. Martins, L. Mestre, R. Miranda-Santos, A. Nunes-Gutjahr, W. Overal, L. Parry, S. Peters, M. Ribeiro-Junior, M. da Silva, C. Motta & C. Peres, 2007. Quantifying the biodiversity value of tropical primary, secondary, and plantation forests. Science 104: 18555–18560.Google Scholar
  2. Beheregaray, L., G. Cooke, N. Chao & E. Landguth, 2015. Ecological speciation in the tropics: insights from comparative genetic studies in Amazonia. Frontiers in Genetics 5: 1–19.CrossRefGoogle Scholar
  3. Biggs, J., S. von Fumetti & M. Kelly-Quinn, 2017. The importance of small waterbodies for biodiversity and ecosystem services: implications for policy makers. Hydrobiologia 793: 3–39.CrossRefGoogle Scholar
  4. Bührnheim, C. & C. Fernandes, 2003. Structure of fish assemblages in Amazonian rain-forest streams: effects of habitats and locality. Copeia 2003: 255–262.CrossRefGoogle Scholar
  5. Campbell, D., D. Daly, G. Prance, G. David & N. York, 1986. Quantitative ecological inventory of terra firme and várzea tropical forest on the Rio Xingu, Brazilian Amazon. Brittonia 38: 369–393.CrossRefGoogle Scholar
  6. Chapman, F., D. Colle, R. Rottmann & J. Shireman, 1998. Controlled spawning of the neon tetra. The Progressive Fish-Culturist 60: 32–37.CrossRefGoogle Scholar
  7. Cooke, G., N. Chao & L. Beheregaray, 2012a. Divergent natural selection with gene flow along major environmental gradients in Amazonia: insights from genome scans, population genetics and phylogeography of the characin fish Triportheus albus. Molecular Ecology 21: 2410–2427.CrossRefGoogle Scholar
  8. Cooke, G., N. Chao & L. Beheregaray, 2012b. Natural selection in the water: freshwater invasion and adaptation by water colour in the Amazonian pufferfish. Journal of Evolutionary Biology 25: 1305–1320.CrossRefGoogle Scholar
  9. Cooke, G., N. Chao & L. Beheregaray, 2012c. Marine incursions, cryptic species and ecological diversification in Amazonia: the biogeographic history of the croaker genus Plagioscion (Scienidae). Journal of Biogeography 39: 724–1738.CrossRefGoogle Scholar
  10. de Paula, J., F. Luizão & M. Piedade, 2016. The size distribution of organic carbon in headwater streams in the Amazon basin. Environmental Science Research 23: 11461–11470.Google Scholar
  11. Duarte, R., D. Smith, A. Val & C. Wood, 2016. Dissolved organic carbon from the upper Rio Negro protects zebrafish (Danio rerio) against ionoregulatory disturbances caused by low pH exposure. Scientific Reports 6: 1–10.CrossRefGoogle Scholar
  12. Engström-Öst, J. & U. Candolin, 2006. Human-induced water turbidity alters selection on sexual displays in sticklebacks. Behavioral Ecology 18: 393–398.CrossRefGoogle Scholar
  13. Fink, W. & S. Fink, 1979. Central Amazonia and its fishes. Comparative Biochemistry and Physiology 62A: 13–29.CrossRefGoogle Scholar
  14. Fisher, H., B. Wong & G. Rosenthal, 2006. Alteration of the chemical environment disrupts communication in a freshwater fish. Proceedings of the Royal Society of London B 273: 1187–1193.CrossRefGoogle Scholar
  15. Fittkau, E., 1967. On the ecology of Amazonian rain-forest streams. Atas do Simpósio sobre a Biota Amazônica 3: 97–108.Google Scholar
  16. Furch, K., 1984. Water chemistry of the Amazon basin: the distribution of chemical elements among freshwaters. In Sioli, H. (ed.), The Amazon. Monographiae Biologicae, Vol. 56. Springer, Dordrecht: 215–244.Google Scholar
  17. Gentry, A., 1988. Tree species richness of upper Amazonian forests. Proceedings of the National Academy of Sciences of the United States of America 85: 156–159.CrossRefGoogle Scholar
  18. Gibson, L., T. Lee, L. Koh, B. Brook, T. Gardner, J. Barlow, C. Peres, C. Bradshaw, W. Laurance, T. Lovejoy & N. Sodhi, 2011. Primary forest are irreplaceable for sustaining tropical biodiversity. Nature 478: 378–381.CrossRefGoogle Scholar
  19. Guevara-Fiore, P., A. Skinner & P. Watt, 2009. Do male guppies distinguish virgin females from recently mated ones? Animal Behaviour 77: 425–431.CrossRefGoogle Scholar
  20. Gottsberger, G., 1978. Seed dispersal by fish in the inundated regions of Humaitá, Amazonia. Biotropica 10: 170–183.CrossRefGoogle Scholar
  21. Hankison, S. & M. Morris, 2003. Avoiding a compromise between sexual selection and species recognition: female swordtail fish assess multiple species-specific cues. Behavioral Ecology 14: 282–287.CrossRefGoogle Scholar
  22. Henderson, P., 1990. Fish of the Amazonian igapó: stability and conservation in a high diversity-low biomass system. Journal of Fish Biology 37: 61–66.CrossRefGoogle Scholar
  23. Ikeda, T. & S. Kohshima, 2009. Why is the neon tetra so bright? Coloration for mirror-image projection to confuse predators? “Mirror-image decoy” hypothesis. Environmental Biology of Fishes 86: 427–441.CrossRefGoogle Scholar
  24. Junk, W., 1970. Investigations on the ecology and production-biology of the ‘floating meadows’ (Paspalo-Echinochloetum) on the middle Amazon. I: the floating vegetation and its ecology. Amazoniana 2: 449–495.Google Scholar
  25. Junk, W., 1983. Ecology of swamps on the middle Amazon. In Gore, A. (ed.), Mires: Swamp, Bog, Fen and Moor. Ecosystems of the World - Regional Studies. Elsevier, Amsterdam: 269–294.Google Scholar
  26. Junk, W., 1984. Ecology of the várzea, floodplain of Amazonian whitewater rivers. In Sioli, H. (ed.), The Amazon. Monographiae Biologicae, Vol. 56. Springer, Dordrecht: 215–244.Google Scholar
  27. Junk, W. & K. Furch, 1980. Química da água e macrófitas aquáticas de rios e igarapés na Bacia Amazônica e nas áreas adjacentes. Parte I: Trecho Cuiabá - Porto Velho - Manaus. Acta Amazonica 10: 611–633.CrossRefGoogle Scholar
  28. Junk, W., F. Wittmann, J. Schöngart & M. Piedade, 2015. A classification of the major habitats of Amazonian black-water river floodplains and a comparison with their white-water counterparts. Wetlands Ecology and Management 23: 677–693.CrossRefGoogle Scholar
  29. Klinge, H., 1967. Podzol soils: a source of blackwater rivers in Amazonia. Atas do Simpósio sobre a Biota Amazônica 3: 117–125.Google Scholar
  30. Küchler, I., N. Miekeley & B. Forsberg, 1994. Molecular mass distributions of dissolved organic carbon and associated metals in waters from Rio Negro and Rio Solimões. Science of the Total Environment 156: 207–216.CrossRefGoogle Scholar
  31. Küchler, I., N. Miekeley & B. Forsberg, 2000. A contribution to the chemical characterization of rivers in the Rio Negro Basin, Brazil. Journal of the Brazilian Chemical Society 11: 286–292.CrossRefGoogle Scholar
  32. Lindström, J., 1999. Early development and fitness in birds and mammals. Trends in Ecology and Evolution 14: 343–348.CrossRefGoogle Scholar
  33. Markewitz, D., E. Davidson, R. Figueiredo, R. Victoria & A. Krusche, 2001. Control of cation concentrations in stream waters by surface soil processes in an Amazonian watershed. Nature 410: 802–805.CrossRefGoogle Scholar
  34. Mayr, E., 1963. Animal Species and Evolution. Harvard University Press, Cambridge.CrossRefGoogle Scholar
  35. McLennan, D. & M. Ryan, 1997. Responses to conspecific and heterospecific olfactory cues in the swordtail Xiphophorus cortezi. Animal Behaviour 54: 1077–1088.CrossRefGoogle Scholar
  36. Mendonça, F., W. Magnusson & J. Zuanon, 2005. Relationships between habitat characteristics and fish assemblages in small streams of Central Amazonia. Copeia 4: 751–764.CrossRefGoogle Scholar
  37. Moreira, C. & F. Lima, 2017. Two new Hyphessobrycon (Characiformes: Characidae) species from Central Amazon basin, Brazil. Zootaxa 4318: 123–134.CrossRefGoogle Scholar
  38. Olsson, M., 1993. Male preference for large females and assortative mating for body size in the sand lizard (Lacerta agilis). Behavioral Ecology and Sociobiology 32: 337–341.CrossRefGoogle Scholar
  39. Petry, P., P. Bayley & D. Markle, 2003. Relationships between fish assemblages, macrophytes and environmental gradients in the Amazon River floodplain. Journal of Fish Biology 63: 547–579.CrossRefGoogle Scholar
  40. Pires, T., E. Borghezan, V. Machado, D. Powell, C. Röpke, C. Oliveira, J. Zuanon & I. Farias, 2018. Testing Wallace’s intuition: water type, reproductive isolation and divergence in an Amazonian fish. Journal of Evolutionary Biology 31: 882–892.CrossRefGoogle Scholar
  41. Pires, T., T. Farago, D. Campos, G. Cardoso & J. Zuanon, 2016. Traits of a lineage with extraordinary geographical range: ecology, behavior and life-history of the sailfin tetra Crenuchus spilurus. Environmental Biology of Fishes 99: 925–937.CrossRefGoogle Scholar
  42. Pitman, N., J. Terborgh, M. Silman, P. Núñez, D. Neill, C. Cerón, W. Palacios & M. Aulestia, 2001. Dominance and distribution of tree species in upper Amazonian terra firme forests. Ecology 82: 2101–2117.CrossRefGoogle Scholar
  43. Planquette, P., P. Keith & P.-Y. Le Bail, 1996. Atlas des poissons d’eau douce de Guyane. IEGB-MNHN/INRA/CSP/Min. Env, Paris.Google Scholar
  44. R Development Core Team, 2018. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.Google Scholar
  45. Ramírez, F., T. Davenport & J. Mojica, 2015. Dietary–morphological relationships of nineteen fish species from an Amazonian terra firme blackwater stream in Colombia. Limnologica: Ecology and Management of Inland Waters  52: 89–102.CrossRefGoogle Scholar
  46. Ríos-Villamizar, E., M. Piedade, J. Da Costa, J. Adeney & W. Junk, 2013. Chemistry of different Amazonian water types for river classification: a preliminary review. In Brebbia, C. (ed.), Water and Society II. WIT Press, Southampton: 19–28.Google Scholar
  47. Roque, F., D. Lima, T. Siqueira, L. Vieira, M. Stefanes & S. Trivinho-Strixino, 2012. Concordance between macroinvertebrate communities and the typological classification of white and clear-water streams in Western Brazilian Amazonia. Biota Neotropica 12: 83–92.CrossRefGoogle Scholar
  48. Rosenthal, G., W. Wagner Jr. & M. Ryan, 2002. Secondary reduction of preference for the sword ornament in the pygmy swordtail Xiphophorus nigrensis (Pisces: Poeciliidae). Animal Behaviour 6: 37–45.CrossRefGoogle Scholar
  49. Saint-Paul, U., J. Zuanon, M. Correa, M. García, N. Fabré, U. Berger & W. Junk, 2000. Fish communities in central Amazonian white- and blackwater floodplains. Environmental Biology of Fishes 57: 235–250.CrossRefGoogle Scholar
  50. Sioli, H., 1984. The Amazon and its main affluents: hydrography, morphology of the river courses, and river types. In Sioli, H. (ed.), The Amazon. Monographiae Biologicae, Vol. 56. Springer, Dordrecht: 126–166.Google Scholar
  51. Stearns, S., 1989. Trade-offs in life-history evolution. Functional Ecology 3: 259–268.CrossRefGoogle Scholar
  52. Steinberg, C., S. Kamara, V. Prokhotskaya, L. Manusadžianas, T. Karasyova, M. Timofeyev, Z. Jie, A. Paul, T. Meinelt, V. Farjalla, A. Matsuo, B. Burnison & R. Menzel, 2006. Dissolved humic substances: ecological driving forces from the individual to the ecosystem level? Freshwater Biology 51: 1189–1210.CrossRefGoogle Scholar
  53. ter Steege, H., N. Pitman, D. Sabatier, C. Baraloto, R. Salomão, J. Guevara, O. Phillips, C. Castilho, W. Magnusson, J.-F. Molino, A. Monteagudo, P. Vargas, J. Montero, T. Feldpausch, E. Coronado, T. Killeen, B. Mostacedo, R. Vasquez, R. Assis, J. Terborgh, F. Wittmann, A. Andrade, W. Laurance, S. Laurance, B. Marimon, B.-H. Marimon, I. Vieira, I. Amaral, R. Brienen, H. Castellanos, D. López, J. Duivenvoorden, H. Mogollón, F. Matos, N. Dávila, R. García-Villacorta, P. Diaz, F. Costa, T. Emilio, C. Levis, J. Schietti, P. Souza, A. Alonso, F. Dallmeier, A. Montoya, M. Piedade, A. Araujo-Murakami, L. Arroyo, R. Gribel, P. Fine, C. Peres, M. Toledo, G. Aymard, T. Baker, C. Cerón, J. Engel, T. Henkel, P. Maas, P. Petronelli, J. Stropp, C. Zartman, D. Daly, D. Neill, M. Silveira, M. Paredes, J. Chave, D. Lima Filho, P. Jørgensen, A. Fuentes, J. Schöngart, F. Valverde, A. Di Fiore, E. Jimenez, M. Mora, J. Phillips, G. Rivas, T. van Andel, P. von Hildebrand, B. Hoffman, E. Zent, Y. Malhi, A. Prieto, A. Rudas, A. Ruschell, N. Silva, V. Vos, S. Zent, A. Oliveira, A. Schutz, T. Gonzales, M. Nascimento, H. Ramirez-Angulo, R. Sierra, M. Tirado, M. Medina, G. van der Heijden, C. Vela, E. Torre, C. Vriesendorp, O. Wang, K. Young, C. Baider, H. Balslev, C. Ferreira, I. Mesones, A. Torres-Lezama, L. Giraldo, R. Zagt, M. Alexiades, L. Hernandez, I. Huamantupa-Chuquimaco, W. Milliken, W. Cuenca, D. Pauletto, E. Sandoval, L. Gamarra, K. Dexter, K. Feeley, G. Lopez-Gonzalez & M. Silman, 2013. Hyperdominance in the Amazonian tree flora. Science 342: 1243092.CrossRefGoogle Scholar
  54. Val, A. & G. De Boeck, 2017. Preface: ADAPTA-adaptations of the aquatic biota of the Amazon. Hydrobiologia 789: 1–5.CrossRefGoogle Scholar
  55. Venticinque, E., B. Forsberg, R. Barthem, P. Petry, L. Hess, A. Mercado, C. Cañas, M. Montoya, C. Durigan & M. Goulding, 2016. An explicit GIS-based river basin framework for aquatic ecosystem conservation in the Amazon. Earth System Science Data 8: 651–661.CrossRefGoogle Scholar
  56. Wada, S., Y. Arashiro, F. Takeshita & Y. Shibata, 2011. Male mate choice in hermit crabs: prudence by inferior males and simple preference by superior males. Behavioral Ecology 22: 114–119.CrossRefGoogle Scholar
  57. Walker, I., 1987. The biology of streams as part of Amazonian forest ecology. Experientia 43: 279–287.CrossRefGoogle Scholar
  58. Wallace, A., 1889. Travels on the Amazon and Rio Negro: with an account of the native tribes, and observations on the climate, geology, and natural history of the Amazon valley. Ward, Lock & Company Limited, London.CrossRefGoogle Scholar
  59. Werner, N. & A. Lotem, 2003. Choosy males in a haplochromine cichlid: first experimental evidence for male mate choice in a lekking species. Animal Behaviour 66: 293–298.CrossRefGoogle Scholar
  60. Wong, B. & G. Rosenthal, 2006. Female disdain for swords in a swordtail fish. The American Naturalist 167: 136–140.CrossRefGoogle Scholar
  61. Wood, C., A. Matsuo, R. Wilson, R. Gonzalez, M. Patrick, R. Playle & A. Val, 2002. Protection by natural blackwater against disturbances in ion fluxes caused by low pH exposure in freshwater stingrays endemic to the Rio Negro. Physiological and Biochemical Zoology - Ecological and Evolutionary Approaches 76: 12–27.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Programa de Pós-Graduação em EcologiaInstituto Nacional de Pesquisas da AmazôniaManausBrazil
  2. 2.Coordenação de Biodiversidade, Laboratório de Ecologia Comportamental e EvolutivaInstituto Nacional de Pesquisas da AmazôniaManausBrazil

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