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

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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).

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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

P crit :

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

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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.

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Correspondence to Tristan. J. McArley.

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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).

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McArley, T.J., Hickey, A.J.R., Wallace, L. et al. Intertidal triplefin fishes have a lower critical oxygen tension (Pcrit), higher maximal aerobic capacity, and higher tissue glycogen stores than their subtidal counterparts. J Comp Physiol B 189, 399–411 (2019). https://doi.org/10.1007/s00360-019-01216-w

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Keywords

  • Hypoxia
  • P crit
  • Intertidal fish
  • Aerobic scope
  • Aerobic metabolism
  • Gills