Thermal acclimation of tropical coral reef fishes to global heat waves

  1. Jacob L Johansen  Is a corresponding author
  2. Lauren E Nadler  Is a corresponding author
  3. Adam Habary
  4. Alyssa J Bowden
  5. Jodie Rummer
  1. Hawaii Institute of Marine Biology, University of Hawaii, United States
  2. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Australia
  3. Halmos College of Arts and Sciences, Nova Southeastern University, United States
  4. College of Science and Engineering, James Cook University, Australia
  5. CSIRO, Australia
  6. Institute of Marine and Antarctic Studies, University of Tasmania, Australia
11 figures, 2 tables and 3 additional files

Figures

Effect of 5 weeks’ exposure to elevated temperatures (+3.0°C) on whole blood.

(A) Lactate and (B) glucose concentrations in Caesio cuning. The first blue column in each figure illustrates the control (29.0°C). Letters above columns indicate significant differences between treatment groups, determined through multiple comparisons post-hoc testing (based on linear mixed-effects model analysis). ‘NS’ denotes that the model did not indicate any significant effects of temperature. Error bars are s.e.m., and numbers in parentheses below each category on the x-axis denote sample sizes for each group.

Effect of 5 weeks’ exposure to elevated temperature (+3.0°C) on citrate synthase (CS) and lactate dehydrogenase (LDH) enzyme activity in the pectoral muscle of Caesio cuning (A and B) and Cheilopterus quinquelineatus (C and D).

The first blue column in each figure illustrates the control (29.0°C). Letters above columns indicate significant differences between treatment groups, determined through multiple comparisons post-hoc testing (based on linear mixed-effects model analysis). Error bars are s.e.m., and numbers in parentheses below each category on the x-axis denote sample size.

Gill parameters examined throughout the five weeks’ exposure to elevated temperature (+3.0 ̊C).

(A) Illustration of gill parameters examined. The response of lamellar perimeter to elevated changed through time (in mm) in Caesio cunning (B) and Cheilopterus quinquelineatus (C). The first blue column in each figure illustrates the control (29.0 ̊C). Letters above columns indicate significant differences between treatment groups, determined through multiple comparisons post-hoc testing (based on linear mixed-effects model analysis). The white bar denotes data excluded from analyses due to low n, but shown for clarity. Error bars are s.e.m., and numbers in parentheses below each category on the x-axis denote sample size.

Effect of 5 weeks’ exposure to elevated temperatures (+3.0°C) on epithelial thickness and lamellar width (both in μm) in the gills of Caesio cuning (A and B) and Cheilopterus quinquelineatus (C and D).

The first blue column in each figure illustrates the control (29.0°C). Letters above columns indicate significant differences between treatment groups, determined through multiple comparisons post-hoc testing (based on linear mixed-effects model analysis). The white bar denotes data excluded from analyses due to low n, but shown for clarity. ‘NS’ denotes that the model did not indicate any significant effects of temperature. Error bars are s.e.m., and numbers in parentheses below each category on the x-axis denote sample size.

Effect of 5 weeks’ exposure to elevated temperatures (+3.0°C) on metabolic performance of Caesio cuning (A and B) and Cheilopterus quinquelineatus (C and D).

Estimates of standard (white circles) and maximum (black circles) metabolic rates (A and C) and aerobic scope (ASc = triangles, B and D) are illustrated. The first blue data point in panels B and D represent the control (29.0°C). Letters above data points indicate significant differences between treatment groups, determined through multiple comparisons post-hoc testing (based on linear mixed-effects model analysis). Error bars are s.e.m., and numbers in parentheses below each category on the x-axis denote sample size.

Effect of 5 weeks’ exposure to elevated temperatures (+3.0°C) on spleen somatic index and spleen hemoglobin concentration of Caesio cuning (A and B) and Cheilopterus quinquelineatus (C and D).

The first blue column in each figure illustrates the control (29.0°C). Letters above columns indicate significant differences between treatment groups, determined through multiple comparisons post-hoc testing (based on linear mixed-effects model analysis). ‘NS’ denotes that the model did not indicate any significant effects of temperature. Error bars are s.e.m., and numbers in parentheses below each category on the x-axis denote sample size.

Summary of the timing and duration of the physiological responses of two stenothermal fishes (Caesio cuning, top, and Cheilodipterus quinquelineatus, bottom) to a five-week acute heating event.

Summary of the timing and duration of the physiological responses of two stenothermal fishes (Caesio cuning, top, and Cheilodipterus quinquelineatus, bottom) to a 5-week acute heating event, including responses in mortality, whole organism demand (standard metabolic rate, SMR), whole organism supply (maximum metabolic rate, MMR, and aerobic scope, ASc), tissue demand (citrate synthase, CS, and lactate dehydrogenase, LDH, enzyme activity in the gill and muscle tissue), and tissue supply (lamellar width and perimeter, blood glucose, spleen [Hb], and spleen somatic index, SSI).

Appendix 1—figure 1
Effect of exhaustive exercise on the mortality (%) of Cheilopterus quinquelineatus.

The first blue column illustrates control mortality (29.0°C), while red columns illustrate elevated temperature effects (+3.0°C). No mortality was seen in Caesio cuning during the experimental period (not depicted). Numbers in parentheses below each category on the x-axis denote sample sizes for each group.

Appendix 1—figure 2
Effect of 5 weeks’ exposure to elevated temperatures (+3.0°C) on citrate synthase (CS) and lactate dehydrogenase (LDH) activity in the gills of Caesio cuning (A and B) and Cheilopterus quinquelineatus (C and D).

The first blue column in each figure illustrates the control (29.0°C). Letters above columns indicate significant differences between treatment groups, determined through multiple comparisons post-hoc testing (based on linear mixed-effects model analysis). ‘NS’ denotes that the model did not indicate any significant effects of temperature. Error bars are s.e.m., and numbers in parentheses below each category on the x-axis denote sample sizes for each group.

Appendix 1—figure 3
Effect of 5 weeks’ exposure to elevated temperatures (+3.0°C) on Fulton’s K condition factor in Caesio cuning (A) and Cheilopterus quinquelineatus (B).

The first blue column in each figure illustrates the control (29.0°C). ‘NS’ denotes that the linear mixed-effects model analysis did not indicate any significant effects of temperature. Error bars are s.e.m., and numbers in parentheses below each category on the x-axis denote sample sizes for each group.

Appendix 1—figure 4
Effect of 5 weeks’ exposure to elevated temperatures (+3.0°C) on (A) hemoglobin concentration, (B) hematocrit, and (C) mean corpuscular haemoglobin content (MCHC) in Caesio cuning.

The first blue column in each figure illustrates the control (29.0°C). ‘NS’ denotes that the linear mixed-effects model analysis did not indicate any significant effects of temperature. Error bars are s.e.m., and numbers in parentheses below each category on the x-axis denote sample sizes for each group.

Tables

Table 1
Acclimation responses of 18 hematological and cardiorespiratory parameters.
TypeParameterDefinition
Muscle + GillCitrate synthase activity (CS)An exclusive marker of the mitochondrial matrix and a marker of mitochondrial density in tissues
Lactate dehydrogenase (LDH)An enzyme involved in anaerobic energy production
SpleenSpleen somatic index (SSI)The relative spleen to body mass, used to assess release of red blood cell stores into the blood stream
Spleen [Hb]An indicator of red blood cell production within the spleen
BloodMean corpuscular hemoglobin content (MCHC)Hemoglobin concentration in red blood cells, indicative of blood oxygen carrying capacity
Hematocrit (Hct)The ratio of red blood cells to the total volume of blood
Hemoglobin (Hb)The protein responsible for transporting oxygen in the blood
Whole blood lactateLactic acid appears in the blood as a result of anaerobic metabolism
Whole blood glucoseUsed to support the metabolic pathways in the mitochondria and cytoplasm
GillLamellar perimeterThe perimeter of a cross-section of the lamellae measured histologically as a proxy for total diffusible surface area for O2 transport over the lamellae.
Lamellar widthThe histological total diameter of the lamellae epithelium and capillary. Lamellar width is here used to indicate the epithelial thickness of the lamellae (i.e. diffusion distance for O2).
Epithelial thicknessA measure of the diameter of the epithelia on the lamellae
Whole body metabolismStandard metabolic rate (SMR)Baseline oxygen consumption required to maintain bodily functions.
Maximum metabolic rate (MMR)Maximal oxygen consumption
Aerobic scope (ASc)The difference between MMR and SMR, indicating the maximal O2 available for activity.
Whole body conditionFulton’s K condition factorLength-mass relationship used to estimate health of an individual
Table 2
Sample size of each parameter across species and exposure week.

For histological samples, each Individual was used for both tissue and gill analyses. For respirometry (due to ethical requirements to minimize sample numbers), we used a mixed-staggered repeated measures design in which each individual was tested twice where possible, but with a 3-week separation between each trial (i.e. Week 0 and Week 3, Week 1 and Week 4, and Week 2 and Week 5).

SpeciesParameterCtrl Week 0Crtl Week 5Week 0Week 1Week 2Week 3Week 4Week 5
C. quinquelineatusTissue88788886
C. quinquelineatusGill (thickness, perimeter, width)5, 4, 46, 3, 35, 5, 55, 6, 67, 6, 62, 2, 27, 4, 46, 5, 5
C. quinquelineatusRespirometry / mortality881410913130
C. cuningTissue / blood88888888
C. cuningGill (thickness, perimeter, width)7, 6, 65, 4, 48, 8, 87, 5, 55, 5, 58, 5, 57, 5, 76, 6, 6
C. cuningRespirometry / mortality88878878

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  1. Jacob L Johansen
  2. Lauren E Nadler
  3. Adam Habary
  4. Alyssa J Bowden
  5. Jodie Rummer
(2021)
Thermal acclimation of tropical coral reef fishes to global heat waves
eLife 10:e59162.
https://doi.org/10.7554/eLife.59162