Acute temperature effects on metabolic rate, ventilation, diffusive water exchange, osmoregulation, and acid–base status in the Pacific hagfish (Eptatretus stoutii)

Abstract

The Pacific hagfish (Eptatretus stoutii) is a representative of the most basal extant craniates, and is a marine osmoconformer with an extremely low metabolic rate (MO2 = 475 µmol O2/kg/h at 12 °C). We investigated potential physiological trade-offs associated with compensatory changes in gill ventilation and perfusion when 12 °C-acclimated hagfish were acutely exposed to 7 °C or 17 °C, as reflected in diffusive unidirectional water flux (\({J_{{{\text{H}}_2}{\text{O}}}}\), measured with tritiated water: 3H2O), net ammonia flux (Jamm), and plasma ion and acid–base status. \({J_{{{\text{H}}_2}{\text{O}}}}\) was high (~ 1.4 L/kg/h at 12 °C) in comparison to marine teleosts and elasmobranchs. MO2 increased linearly with temperature (R2 = 0.991), and was more sensitive (Q10 = 3.22) in the 12–7 °C range than either Jamm (1.86) or \({J_{{{\text{H}}_2}{\text{O}}}}\) (1.35), but the pattern reversed from 12 to 17 °C (Q10s: MO2 = 2.77, Jamm = 2.88, \({J_{{{\text{H}}_2}{\text{O}}}}\) = 4.01). Heart rate, ventilatory index (a proxy for total ventilation), and coughing frequency also increased but with different patterns. At 17 °C, plasma [Ca2+] and [Mg2+] decreased, although osmolality increased, associated with elevations in plasma [Na+] and [Cl]. Blood pH and PCO2 were unaffected by acute temperature changes while [HCO3] increased. Hyperoxia (PO2 > 300 Torr) attenuated the increase in \({J_{{{\text{H}}_2}{\text{O}}}}\) at 17 °C, did not affect Jamm, and had diverse effects on plasma ion and acid–base status. Our results suggest a clear osmorespiratory compromise occurring for the diffusive water fluxes as a result of acute temperature changes in this osmoconformer.

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Acknowledgements

This study was supported by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants to CMW and PMS. MG is supported by a 4-year graduate fellowship from the University of British Columbia. We would like to thank Dr. Eric Clelland (Bamfield Marine Sciences Centre research coordinator) for excellent logistic support, Dr. Alex Clifford for providing helpful advice with calculations, and three anonymous reviewers whose comments and suggestions have greatly improved the manuscript.

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Correspondence to Marina Giacomin.

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Communicated by G. Heldmaier.

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Giacomin, M., Eom, J., Schulte, P.M. et al. Acute temperature effects on metabolic rate, ventilation, diffusive water exchange, osmoregulation, and acid–base status in the Pacific hagfish (Eptatretus stoutii). J Comp Physiol B 189, 17–35 (2019). https://doi.org/10.1007/s00360-018-1191-0

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Keywords

  • Temperature
  • Gill permeability
  • Hagfish
  • Metabolic rate
  • Osmoconformer
  • Tritiated water
  • pH regulation