Brain cooling marginally increases maximum thermal tolerance in Atlantic cod

Background

• The critical thermal maximum (CT_MAX) is the temperature where fish exhibit loss of equilibrium (LOE) because of a temperature-induced collapse of vital physiological functions. CT_MAX defines the upper limit of a species’ fundamental thermal niche and has been applied widely in studies on the responses of fishes to ocean warming (Sunday et al., 2012). Identifying the physiological functions underlying the LOE at CT_MAX is therefore highly relevant for understanding how anthropogenic climate change will affect aquatic ecosystems.
• The oxygen-limitation hypothesis, described in the concept of oxygen- and capacity-limited thermal tolerance (reviewed in Pörtner, 2010), posits a temperature-induced collapse of the cardiovascular system and insufficient tissue oxygen supply for vital physiological functions as the central mechanism underlying the LOE in fishes at CT_MAX. However, recent studies find several fish species maintain cardiovascular performance at thermal extremes (reviewed in Jutfelt et al., 2018), indicating that the thermal tolerance of other vital functions must be responsible for their LOE at CT_MAX.
• Early literature suggests that compromised brain nerve function at thermal extremes is the mechanism underlying the LOE in fishes at CT_MAX (Friedlander et al., 1976). To test this hypothesis, Jutfelt et al. mounted cooling plates on the head of Atlantic cod (Gadus morhua) and assessed if localised cooling of the brain increased the CT_MAX of this species.

Methods

• Custom-built aluminium brain coolers (Fig. 1A) were attached to the top of the head of the cod using cyanoacrylate glue and silk sutures (Fig. 1B) and connected to a thin flexible silicone tubing that allowed water to be flushed through the coolers to control their temperature (Fig. 1C).
• Tests on terminally anesthetised fish with thermocouples in the brain showed the cooling capacity of the brain coolers on brain tissue in different brain regions was 2–6°C.
• CT_MAX was assessed in three groups of fish: 1) a control group without brain-coolers, 2) a group with brain-coolers supplied with ambient ramping-temperature water, and 3) a group with brain-coolers supplied with ice-cold water.
• The CT_MAX trials were performed in aquaria with fully aerated water using a temperature ramping rate of 10°C h⁻¹. Fish were deemed to have reached their CT_MAX at the temperature where they exhibited LOE and were unable to right themselves within three seconds.

Figure 1. Design and attachment method of the brain coolers on Atlantic cod.

Results

• The authors made the following CT_MAX measurements (Fig. 2):
• Control fish without brain-coolers: 25.82 ± 0.58°C
• Ambient fish with brain-coolers with ambient ramping-temperature water: 25.96 ± 0.36°C
• Cooled fish with brain-coolers with ice-cold water: 26.33 ± 0.49°C

Figure 2. Critical thermal maximum measured as loss of equilibrium temperature in the three groups of Atlantic cod.

Discussion and Conclusion

• The small difference in CT_MAX between control fish and ambient fish indicates that the brain-coolers had a minimal effect on CT_MAX.
• The small increase in CT_MAX of brain cooled fish (0.5–0.7°C), relative to the large cooling effect of the brain coolers (2–6°C depending on the brain region), indicates that compromised brain nerve function is not the sole mechanism underlying LOE at CT_MAX. The authors suggest that peripheral neurons and muscles could potentially have very similar thermal limits as the brain and therefore also be involved in setting the CT_MAX. The authors also note that insufficient tissue oxygen supply is likely not the principal mechanism underlying the LOE of cod at CT_MAX as brain cooling would not have protected against cardiac collapse.
• The authors conclude that the marginally increased CT_MAX in cooled fish supports the hypothesis that LOE at thermal extremes is linked to compromised brain nerve function.

Interest

• Compromised nerve function in fishes at thermal extremes was first proposed almost 50 years ago (e.g., Friedlander et al., 1976), but the findings have been largely forgotten because of the dominating role of the oxygen-limitation hypothesis in the field of fish ecophysiology. The study by Jutfelt et al. nicely bridges these early studies with the recent studies showing that fishes maintain tissue oxygen supply at thermal extremes.

Future directions

• Using externally mounted coolers (as in this study) or internally implanted thermodes, future studies aimed at identifying organs linked to the LOE in fishes at CT_MAX could test if CT_MAX is affected by localised cooling (or heating) of other organs and tissues, such as the heart.
• Future studies could also test if brain-cooling increases the CT_MAX of crustaceans, as species from this group have also been shown to maintain tissue oxygen supply at thermal extremes.
• Finally, a 10°C h^-1 ramping rate is high both from an environmental perspective and relative to other CT_MAX studies on fishes. Future studies could test how reducing the temperature ramping rate affect the magnitude of brain-cooling on CT_MAX.

References

• Friedlander MJ, Kotchabhakdi N, Prosser CL. 1976. Effects of cold and heat on behavior and cerebellar function in Goldfish. Comp. Physiol. 112, 19–45.
• Jutfelt F et al. 2018. Oxygen- and capacity-limited thermal tolerance: blurring ecology and physiology. Exp. Biol. 221, jeb169615. (doi: 10.1242/jeb. 169615)
• Pörtner HO. 2010. Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. Exp. Biol. 213, 881–893. (doi: 10.1242/jeb.037523)
• Sunday JM, Bates AE, Dulvy NK. 2012. Thermal tolerance and the global redistribution of animals. Clim. Change 2, 686-690 (doi: 10.1038/nclimate1539)

 

doi: https://doi.org/10.1242/prelights.11453

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