Skip to main content
SpringerLink
Log in

Metabolic rate and thermal tolerance in two congeneric Amazon fishes: Paracheirodon axelrodi Schultz, 1956 and Paracheirodon simulans Géry, 1963 (Characidae)

  • ADAPTA
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Temperature is the main factor affecting the distribution of the sympatric Amazon fishes Paracheirodon axelrodi and Paracheirodon simulans. Both species are associated with flooded areas of the Negro river basin; P. axelrodi inhabits waters that do not exceed 30°C, and P. simulans lives at temperatures that can surpass 35°C. The present work aimed to describe the biochemical and physiological adjustments to temperature in those species. We determined the thermal tolerance polygon of species acclimated to four temperatures using critical thermal methodology. We also determined the chronic temperature effects by acclimating the two species at 20, 25, 30, and 35°C and measured the critical oxygen tension (PO2crit) for both species. Additionally, we evaluated the metabolic rate and the enzymes of energy metabolic pathways (CS, MDH, and LDH). Our results showed a larger thermal tolerance polygon, a higher energetic metabolic rate, and higher enzyme levels for P. simulans acclimated to 20 and 35°C compared to P. axelrodi. Paracheirodon simulans also presented a higher hypoxia tolerance, indirectly determined as the PO2cri. Thus, we conclude that the higher metabolic capacity of P. simulans gives this species a better chance to survive at acutely higher temperatures in nature, although it is more vulnerable to chronic exposure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Addo-Bediako, A., S. L. Chown & K. J. Gaston, 2000. Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society of London B 267: 739–745.

    Article  CAS  Google Scholar 

  • Almeida-Val, V. M. F. & P. W. Hochachka, 1995. Air-breathing fishes: metabolic biochemistry of the first diving vertebrates. In Hochachka, P. W. & T. Mommsen (eds.), Biochemistry and Molecular Biology of Fishes. Elsevier Science, Amsterdam: 45–55.

    Google Scholar 

  • Almeida-Val, V. M. F., A. L. Val, W. P. Duncan, F. C. A. Souza, M. N. Paula-Silva & S. Land, 2000. Scaling effects on hypoxia tolerance in the Amazon fish Astronotus ocellatus (Perciformes: Cichlidae): contribution of tissue enzyme levels. Comparative Biochemistry and Physiology, Part B125: 219–226.

    Article  Google Scholar 

  • Anjos, M. B., R. R. De Oliveira & J. Zuanon, 2008. Hypoxic environments as refuge against predatory fish in the Amazonian floodplains. Brazilian. Journal of Biology 68: 45–50.

    CAS  Google Scholar 

  • Anjos, H. D. B., R. M. S. Amorim, J. A. Siqueira & C. R. Anjos, 2009. Exportação de peixes ornamentais do Estado do Amazonas, bacia Amazonica. Brasil. Boletim do Instituto de Pesca 35: 259–274.

    Google Scholar 

  • Anttila, K., R. S. Dhillon, E. G. Boulding, A. P. Farrell, B. D. Glebe, J. A. K. Elliott, W. R. Wolters & P. M. Schulte, 2013. Variation in temperature tolerance among families of Atlantic salmon (Salmo salar) is associated with hypoxia tolerance, ventricle size and myoglobin level. The Journal of Experimental Biology 216: 1183–1190.

    Article  CAS  PubMed  Google Scholar 

  • Axelrod, H. R., W. E. Burgess, N. Pronek & J. G. Walls, 1986. Spawning the neon tetra, Paracheirodon innesi. In Axelrod, H. R, W. E. Burgess, N. Pronek & J. G. Walls, (eds) Dr. Axelrod’s Atlas of Freshwater Aquarium Fishes, 2nd ed. T.F.H. Publications, New York: 194–197.

  • Ballard, F. J. & R. W. Hanson, 1967. Phosphoenolpyruvate carboxykinase and pyruvate carboxylase in developing rat liver. Biochemistry Journal 104: 866–871.

    Article  CAS  Google Scholar 

  • Beitinger, T. L. & W. A. Bennett, 2000. Quantification of the role of acclimation temperature in temperature tolerance of fishes. Environmental Biology of Fishes 58: 277–288.

    Article  Google Scholar 

  • Beitinger, T. L., W. A. Bennett & R. W. McCauley, 2000. Temperature tolerance of North American freshwater fishes exposed to dynamic changes in temperature. Environmental Biology of Fishes 58: 237–275.

    Article  Google Scholar 

  • Bennet, W. A. & T. L. Beitinger, 1997. Temperature tolerance of the sheepshead minnow, Cyprinodon variegatus. Copeia 1: 77–87. 

    Article  Google Scholar 

  • Bradford, M. M., 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the protein-dye binding. Analytical Biochemistry 72: 248–254.

    Article  CAS  PubMed  Google Scholar 

  • Burleson, M. L. & P. E. Silva, 2011. Cross tolerance to environmental stressors: effects of hypoxic acclimation on cardiovascular responses of Channel catfish (Ictalurus punctatus) to a thermal challenge. Journal Thermal Biology 36: 250–254.

    Article  Google Scholar 

  • Busch, S., B. M. Johnson & T. Mehner, 2011. Energetic costs and benefits of cyclic habitat switching: a bioenergetics model analysis of diel vertical migration in coregonids. Canadian Journal of Fisheries and Aquatic Sciences 68: 706–717.

    Article  Google Scholar 

  • Calosi, P., D. T. Bilton, J. I. Spicer, S. C. Votie & A. Atfield, 2010. What determines a speciesʼ geographical range? Thermal biology and latitudinal range size relationships in European diving beetles (Coleoptera: Dytiscidae). Journal of Animal Ecology 79: 194–204.

    Article  PubMed  Google Scholar 

  • Clarke, A. & N. M. Johnston, 1999. Scaling of metabolic rate with body mass and temperature in teleost fish. Journal of Animal Ecology 68: 893–905.

    Article  Google Scholar 

  • Compton, T. J., M. J. A. Rijkenberg, J. Drent & T. Piersma, 2007. Thermal tolerance ranges and climate variability: a comparison between bivalves from differing climates. Journal of Experimental Marine Biology and Ecology 352: 200–211.

    Article  Google Scholar 

  • Cortemeglia, C. & T. L. Beitinger, 2005. Temperature tolerances of wildtype and red transgenic zebra danios. Transactions of the American Fisheries Society 134: 1431–1437.

    Article  Google Scholar 

  • Cortemeglia, C. & T. L. Beitinger, 2006. Projected US distributions of transgenic and wildtype zebra danios, Danio rerio, based on temperature tolerance data. Journal of Thermal Biology 31: 422–428.

    Article  Google Scholar 

  • Cristescu, M. E., B. Demiri, I. Altshuler & T. J. Crease, 2014. Gene expression variation in duplicate lactate dehydrogenase genes: do ecological species show distinct responses? Plos One 9: e103964.

    Article  PubMed  PubMed Central  Google Scholar 

  • De Boeck, G., C. M. Wood, F. I. Iftikar, V. Matey, G. R. Scott, K. A. Sloman, M. N. Paula-Silva, V. M. F. Almeida-Val & A. L. Val, 2013. Interactions between hypoxia tolerance and food deprivation in Amazonian oscars, Astronotus ocellatus. Journal of Experimental Biology 216: 4590–4600.

    Article  PubMed  Google Scholar 

  • Driedzic, W. R. & V. M. F. Almeida-Val, 1996. Enzymes of cardiac energy metabolism in Amazonian teleosts and the fresh-water stingray (Potamotrygon hystrix). Journal of Experimental Zoology 274: 327–333.

    Article  CAS  Google Scholar 

  • Eme, J. & W. A. Bennett, 2009. Critical thermal tolerance polygons of tropical marine fishes from Sulawesi, Indonesia. Journal of Thermal Biology 34: 220–225.

    Article  Google Scholar 

  • Gillooly, J. F., E. L. Charnov, G. B. West, V. M. Savage & J. H. Brown, 2001. Effects of size and temperature on developmental time. Nature 417: 70–73.

    Article  Google Scholar 

  • Gillooly, J. F., J. H. Brown, G. B. West, V. M. Savage & E. L. Charnov, 2002. Effects of size and temperature on metabolic rate. Science 293: 2248–2251.

    Article  Google Scholar 

  • Harris, P. & P. Petry, 2001. Preliminary report on the genetic population structure and phylogeography of cardinal tetra (Paracheirodon axelrodi) in Rio Negro basin. In Chao, L. N., P. Petry, G. Prang, L. Sonneschein & M. Tlusty (eds.), Conservation and Management of Ornamental Fish Resources of the Rio Negro Basin, Amazonia, Brazil- Project Piaba, 1st ed. Editora da Universidade Federal do Amazonas-EDUA, Manaus: 205–225.

    Google Scholar 

  • Hochachka, P. W., 1996. Oxygen sensing and metabolic regulation: short, intermediate, and long term roles. In Val, A. L., V. M. F. Almeida-Val & D. J. Randall (eds.), Physiology and Biochemistry of the Fishes of the Amazon. INPA, Manaus: 233–256.

    Google Scholar 

  • Hochachka, P. W. & G. N. Somero, 2002. Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford University Press, New York.

    Google Scholar 

  • Intergovernmental Panel on Climate Change (IPCC), 2014.Climate Change, 2014: Mitigation of Climate Change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.Cambridge University Press, Cambridge.

  • López-Olmeda, J. F. & F. J. Sánchez-Vázquez, 2011. Thermal biology of zebrafish (Danio rerio). Journal of Thermal Biology 36: 91–104.

    Article  Google Scholar 

  • Lutterschmidt, W. I. & V. H. Hutchison, 1997. The critical thermal maximum: history and critique. Canadian Journal of Zoology 75: 1561–1574.

    Article  Google Scholar 

  • Magozzi, S. & P. Calosi, 2014. Integrating metabolic performance, thermal tolerance, and plasticity enables for more accurate predictions on species vulnerability to acute and chronic effects of global warming. Global Change Biology 21: 181–194.

    Article  PubMed  Google Scholar 

  • Marshall, B. G., B. R. Forsberg, L. L. Hess & C. E. C. Freitas, 2011. Water temperature differences in interfluvial palm swamp habitats of Paracheirodon axelrodi and P. simulans (Osteichthyes: Characidae) in the middle Rio Negro, Brazil. Ichthyological Exploration of Freshwaters 22: 377–383.

    Google Scholar 

  • Mora, C. & M. F. Moya, 2006. Effect of the rate of temperature increase of the dynamic method on the heat tolerance of fishes. Journal of Thermal Biology 31: 337–341.

    Article  Google Scholar 

  • Oliveira, S. R., R. T. Y. B. Souza, É. S. S. Nunes, C. S. M. Carvalho, G. C. Menezes, J. L. Marcon, R. Roubach, E. A. Ono & E. G. Affonso, 2008. Tolerance to temperature, pH, ammonia and nitrite in cardinal tetra, Paracheirodon axelrodi, an Amazonian ornamental fish. Acta Amazonica 38: 773–779.

    Article  Google Scholar 

  • Peck, L. S., K. E. Webb & D. M. Bailey, 2004. Extreme sensitivity of biological function to temperature in Antarctic marine species. Functional Ecology 18: 625–630.

    Article  Google Scholar 

  • Pörtner, H. O., 2001. Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88: 137–146.

    Article  PubMed  Google Scholar 

  • Pörtner, H. O. & A. P. Farrell, 2008. Physiology and climate change. Science 322: 690–692.

    Article  PubMed  Google Scholar 

  • Pörtner, H. O. & R. Knust, 2007. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315: 95–97.

    Article  Google Scholar 

  • Pörtner, H. O., P. M. Schulte, C. M. Wood & F. Schiemer, 2010. Niche dimensions and limits in fishes: an integrative view. Illustrating the role of physiology in understanding ecological realities. Physiological and Biochemical Zoology 83: 808–826.

    Article  Google Scholar 

  • Rees, B. B., F. A. Sudradjat & J. W. Love, 2001. Acclimation to hypoxia increases survival time of zebrafish, Daniorerio, during lethal hypoxia. Journal of Experimental Zoology 289: 266–272.

    Article  CAS  PubMed  Google Scholar 

  • Smale, M. A. & C. F. Rabeni, 1995. Hypoxia and hyperthermia tolerances of headwater stream fishes. Transactions of the American Fisheries Society 124: 698–710.

    Article  Google Scholar 

  • Soares, M. G. M. & W. J. Junk, 2000. Commercial fishery and fish culture of the state of Amazonas: status and perspectives. In Junk, W. J., J. J. Ohly, M. T. F. Piedade & M. G. M. Soares (eds), The Central Amazon Floodplain: Actual Use and Options for a Sustainable Management. Backhuys Publishers, Leiden: 433–461.

    Google Scholar 

  • Somero, G. N., 2010. The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine “winners” and “losers”. Journal of Experimental Biology 213: 912–920.

    Article  CAS  PubMed  Google Scholar 

  • Steffensen, J., 1989. Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiology and Biochemistry 6: 49–59.

    Article  CAS  PubMed  Google Scholar 

  • Stillman, J. H., 2002. Causes and consequences of thermal tolerance limits in rocky intertidal porcelain crabs, genus Petrolisthes. Integrative and Comparative Biology 42: 790–796.

    Article  PubMed  Google Scholar 

  • Stillman, J. H., 2003. Acclimation capacity underlies susceptibility to climate change. Science 301: 65.

    Article  CAS  PubMed  Google Scholar 

  • Suarez, R. K. & T. P. Mommsen, 1987. Gluconeogenesis in teleost fish. Canadian Journal of Zoology 65: 1869–1882.

    Article  CAS  Google Scholar 

  • Tewksbury, J. J., R. B. Huey & C. A. Deutsch, 2008. Putting the heat on tropical animals. Science 320: 1296–1297.

    Article  CAS  PubMed  Google Scholar 

  • Val, A. L. & V. M. F. Almeida-Val, 1995. Fishes of the Amazon and Their Environments: Physiological and Biochemical Features. Springer, Heidelberg.

    Book  Google Scholar 

  • Verberk, W. C., U. Sommer, R. L. Davidson & M. R. Viant, 2013. Anaerobic metabolism at thermal extremes: a metabolomic test of the oxygen limitation hypothesis in an aquatic insect. Integrative and Comparative Biology 53: 609–619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was funded by the Brazilian National Research Council (CNPq, N° 573976/2008-2) and Amazonas State Research Foundation (FAPEAM, N° 3159/08) that supported INCT/ADAPTA, and International Cooperation Brazil—Portugal (Capes-FCT 320/2011). VMFAV is the recipient of a Research Fellowship from CNPq. DC was the recipient of MSc. Fellowship from CNPq. We would like to thank Dr. Adalberto Luis Val and anonymous referees for their valuable contribution with suggestions and discussions to this work.

Author information

Authors and Affiliations

  1. LEEM - Laboratório de Ecofisiologia e Evolução Molecular, Instituto Nacional de Pesquisas da Amazônia, Manaus, AM, Brazil

    D. F. Campos, T. F. Jesus, D. Kochhann, W. Heinrichs-Caldas & V. M. F. Almeida-Val

  2. cE3c - Center for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal

    T. F. Jesus & M. M. Coelho

Authors
  1. D. F. Campos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. F. Jesus
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Kochhann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. W. Heinrichs-Caldas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. M. Coelho
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. M. F. Almeida-Val
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. F. Campos.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Guest editors: Adalberto L. Val, Gudrun De Boeck & Sidinei M. Thomaz / Adaptation of Aquatic Biota of the Amazon

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Campos, D.F., Jesus, T.F., Kochhann, D. et al. Metabolic rate and thermal tolerance in two congeneric Amazon fishes: Paracheirodon axelrodi Schultz, 1956 and Paracheirodon simulans Géry, 1963 (Characidae). Hydrobiologia 789, 133–142 (2017). https://doi.org/10.1007/s10750-016-2649-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-2649-2

Keywords

Search

Navigation