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Gut transport characteristics in herbivorous and carnivorous serrasalmid fish from ion-poor Rio Negro water

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Abstract

Three closely related characids, Tambaqui (omnivore), black Piranha (carnivore), and Pacu (herbivore), all Serrasalmidae, inhabit the ion-poor, acidic Rio Negro. We compared O2-consumption and N excretion rates in vivo, and sodium, chloride, glucose, and ammonia transport characteristics of gut sac preparations in vitro. The Pacu had a significantly higher weight-specific oxygen consumption, and a lower N/Q ratio than the omnivorous Tambaqui, and a significantly lower urea-N excretion rate than the carnivorous black Piranha, suggesting N-limitation in the herbivorous Pacu. With a value of 2.62 ± 0.15, gut to fork length ratio in the Pacu was about 2.5 times higher than in the black Piranha, and 2.0 times higher than in the Tambaqui. Anterior intestinal activities of three enzymes involved in N-fixation for amino acid synthesis (glutamate dehydrogenase, glutamate–oxaloacetate transferase, and glutamate–pyruvate transferase) were generally greatest in the carnivore and lowest in the herbivore species. In all three species, sodium, chloride, glucose, and ammonia were taken up at high rates from the intestine, resulting in an isosmotic fluid flux. Comparing the area-specific fluid flux of the anterior, mid, and posterior gut sections, no difference was detected between the three sections of the Pacu, while in the Tambaqui, it was highest in the anterior section, and in the black Piranha highest in the middle section. Overall, the area-specific uptake rates for sodium, chloride, glucose, and ammonia of anterior, mid, and posterior sections were similar in all three species, indicating that there is no difference in the area-specific transport rates associated with trophic position. The net ammonia uptake flux from gut interior was not significantly different from the net ammonia efflux to the serosal fluid, so that the ammonia removed from the intestine by the mucosal epithelium was quantitatively transferred through the tissue to the serosal side in all three species. Thus, metabolic activity of gut tissue did not significantly influence the net ammonia transfer. Due to the much higher gut to fork length ratio, the overall transport capacity of the gut of the herbivorous Pacu by far exceeded the transport capacity of their carnivorous and omnivorous relatives, thus compensating for the lower digestibility and the low Na+, Cl−, and N-content of the plant diet. Accordingly, in order to cope with the more difficult digestible plant material and the very low nitrogen content of plants, herbivorous fish have not evolved more effective area-specific transport capacities, but rather have increased the length of the gut.

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Acknowledgements

Financial supports from INCT ADAPTA–CNPq/FAPEAM, Ciência sem Fronteiras, and NSERC (Canada) are gratefully acknowledged. CMW is supported by the Canada Research Chair Program. ALV and VMFAV are recipients of research fellowships from the Brazilian CNPq. BSR is supported by an NSERC Postdoctoral Fellowship.

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Authors and Affiliations

  1. Institut für Zoologie, Leopold-Franzens-Universität Innsbruck, Technikerstr. 25, 6020, Innsbruck, Austria

    Bernd Pelster

  2. Center for Molecular Biosciences, University Innsbruck, Innsbruck, Austria

    Bernd Pelster

  3. Department of Biology, McMaster University, Hamilton, ON, L8S 4K1, Canada

    Chris M. Wood

  4. Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

    Chris M. Wood

  5. Department of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, A1C 5S7, Canada

    Ben Speers-Roesch & William R. Driedzic

  6. Instituto Nacional de Pesquisas da Amazonia, Manaus, Brazil

    Vera Almeida-Val & Adalberto Val

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  1. Bernd Pelster
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  3. Ben Speers-Roesch
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Correspondence to Bernd Pelster.

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Communicated by G. Heldmaier.

B. Pelster and C. M. Wood contributed equally to this paper.

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360_2014_879_MOESM1_ESM.eps

Fluid transport capacity of the different sections of the gut of a one kg fish within one hour. BP and P, N = 6; T, N = 9. Bars not sharing the same letter are significantly different from each other (p < 0.05). Capital letters denote section differences between species, and lower-case letters denote differences between different sections of one species. Supplementary material 1 (EPS 4847 kb)

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Pelster, B., Wood, C.M., Speers-Roesch, B. et al. Gut transport characteristics in herbivorous and carnivorous serrasalmid fish from ion-poor Rio Negro water. J Comp Physiol B 185, 225–241 (2015). https://doi.org/10.1007/s00360-014-0879-z

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  • DOI: https://doi.org/10.1007/s00360-014-0879-z

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