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Intertidal triplefin fishes have a lower critical oxygen tension (Pcrit), higher maximal aerobic capacity, and higher tissue glycogen stores than their subtidal counterparts

  • Tristan. J. McArleyEmail author
  • Anthony J. R. Hickey
  • Lisa Wallace
  • Andreas Kunzmann
  • Neill. A. Herbert
Original Paper

Abstract

Decreased oxygen (O2) availability (hypoxia) is common in rock pools and challenges the aerobic metabolism of fishes living in these habitats. In this study, the critical O2 tension (Pcrit), a whole animal measure of the aerobic contribution to hypoxia tolerance, was compared between four New Zealand triplefin fishes including an intertidal specialist (Bellapiscis medius), an occasional intertidal inhabitant (Forsterygion lapillum) and two exclusively subtidal species (F. varium and F. malcolmi). The intertidal species had lower Pcrit values than the subtidal species indicating traits to meet resting O2 demands at lower O2 tensions. While resting O2 demand (standard metabolic rate; SMR) did not show a major difference between species, the intertidal species had higher maximal rates of O2 consumption (\( \dot{M}{\text{O}}_{{2,{ \hbox{max} }}} \)) and higher aerobic metabolic scope (MS). The high O2 extractive capacity of the intertidal species was associated with increased blood O2 carrying capacity (i.e., higher Hb concentration), in addition to higher mass-specific gill surface area and thinner gill secondary lamellae that collectively conveyed a higher capacity for O2 flux across the gills. The specialist intertidal species B. medius also had higher glycogen stores in both white muscle and brain tissues, suggesting a greater potential to generate ATP anaerobically and survive in rock pools with O2 tensions less than Pcrit. Overall, this study shows that the superior Pcrit of intertidal triplefin species is not linked to a minimisation of SMR, but is instead associated with an increased O2 extractive capacity of the cardiorespiratory system (i.e., \( \dot{M}{\text{O}}_{{2,{ \hbox{max} }}} \), MS, Hb and gill O2 flux).

Keywords

Hypoxia Pcrit Intertidal fish Aerobic scope Aerobic metabolism Gills 

Abbreviations

ACD

Above chart datum

ADP

Adenosine diphosphate

ANOVA

Analysis of variance

ANCOVA

Analysis of covariance

ATP

Adenosine triphosphate

CO2

Carbon dioxide

Hb

Haemoglobin

Hct

Haematocrit

\( \dot{M}{\text{O}}_{2} \)

Mass-specific oxygen consumption

\( \dot{M}{\text{O}}_{{2,{ \hbox{max} }}} \)

Maximum aerobic metabolic rate post-exhaustive exercise

MS

Aerobic metabolic scope

O2

Oxygen

Pcrit

Critical oxygen tension

PO2

Oxygen tension

RBC

Red blood cell

SGA

Sectioned gill arch

SL

Gill secondary lamellae

SMR

Standard metabolic rate

WGA

Whole intact gill arch

Notes

Acknowledgements

T.J.M. would like to acknowledge support from the University of Auckland Scholarship Office for doctoral funding. Supplementary funds were also provided by a Marsden Grant awarded to A.J.R.H and N.A.H. (UOA1407: How to avoid brain damage during oxygen deprivation? Intertidal fish provide a unique test model). Technical staff Peter Browne and Errol Murray are acknowledged for their assistance with design and fabricating the respirometry setups and John Atkins is acknowledged for design of the respirometry software. Dr. Nicholas Shears and Dr. Caitlin Blain are thanked for allowing us to use of their oxygen and temperature loggers. We also thank three anonymous reviewers for their effort in providing comments and critiques which were helpful in revising an original version of this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted (University of Auckland AEC approval number 001441).

Data availability

The data generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Marine ScienceUniversity of AucklandLeighNew Zealand
  2. 2.School of Biological SciencesUniversity of AucklandAucklandNew Zealand
  3. 3.Centre for Tropical Marine Research (ZMT)BremenGermany

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