See-O2 : How Rising CO2 Levels are Affecting Fish Vision

by Karen L. Chisholm, Scripps College [edited by Lars Schmitz as part of BIOL 167 “Sensory Evolution”, an upper division class at the W.M. Keck Science Department. Written for educational purposes only].

Vision is an essential part of many animals’ lives. Smaller animals often rely on vision and fast reaction times to get away from predators and avoid being easy prey. This is true especially in smaller fish, whose lives depend on their ability to quickly recognize a threat and avoid it. Because of the increase in carbon emissions as a product of industrialization, the carbon dioxide (CO2) levels of both air and water are steadily increasing (Figure 1), which has affected fish sensory systems, affecting their abilities to avoid being easy prey.

Figure 1

Figure 1: The estimated increase in CO2 levels in the atmosphere, and the projected impact on the ocean’s pH (McNeil, Matear 2006, Figure 1).

As the ocean takes up CO2, the pH of the water decreases, resulting in a more acidic environment (McNeil, Matear 2006).  And with increased CO2 present, fish are unable to perceive their environment correctly.  In previous studies, fish were exposed to environments with CO2 levels equivalent to the estimated CO2 levels that will be reached in the near future. It has been found that fishes’ olfactory systems and decision making skills have been detrimentally influenced by CO2, which can result in unfavorable behavior in hazardous situations (Munday, et al. 2008). The diminished sensory perception can result in a lack of discrimination in predatory-prey situations (Allan, et al. 2013), with harmful effects on marine life and behavior.

In this blog I want to feature research conducted by Chung, Marshall, Watson, Munday and Nilsson, who investigate how ocean acidification is affecting retinal response time in the visual systems of juvenile, spiny damselfish, Acanthochromis polyacanthus.

Figure 2

Figure 2. The eyesight of this spiny damselfish is negatively impacted by rising CO2 levels. [By Nikita – Flickr: Tropical fish, CC BY 2.0]

It’s been theorized that previously observed changes in the behavior and sensory systems in fish can be linked to CO2 interfering with neurotransmitters. You may wonder, how could CO2 influence neurotransmitters at the retinal level?

Neurons transmit visual signals from the photoreceptors to the optic nerve and by extension, the brain (Figure 3), and many connections in between neurons are made by synapses. To get the signal across synapses, neurotransmitters, or chemical messengers, are critically important. The binding of neurotransmitters on receptors across the synapse leads to the opening of channels on the neuron’s membrane and causes the continued propagation of signals (action potentials) on the neuron across the synapse. So, if the concentration of CO2 in the retina is increased by virtue of diffusion from the ambient environment into the eye, the signal transfer from photoreceptors to the brain may be affected (Figure 3).

Figure 3

Figure 3: This image highlights the interconnected relationship between the eye and the brain via the optic nerve. [By Mads00 (Own work) [CC BY-SA 4.0]

Chung et al. investigated how CO2 levels alter the neurotransmitter, GABA, and its receptors which are located in the eye. GABA is an “inhibitory” neurotransmitter, so when it binds to receptors on a neuron, it actually stops the neuron from firing.  This is counterintuitive because usually neurotransmitters activate neurons, but GABA is used to keep neurons from becoming overstimulated and is useful in controlling activation (this video explains how the neurotransmitter GABA works). The researchers focus on the GABAA receptor because these receptors are present in the eye and would be most likely to be affected by the rising CO2 levels in water (Mora-Ferrer and Neumeyer 2009). In the context of this paper, we are not concerned with how GABA is formed, but rather we are concerned with its function as an “inhibitory” neurotransmitter.

In the experiment, Chung and colleagues investigated the ability of these damselfish to differentiate between flickering light and constant light.  This ability is important because it’s a measure for how well they can resolve super quickly changing scenes, such as rapid movements of predators. When the light flickered, the researchers examined changes in the eye at the retinal level, measuring the eye’s chemical responses by using an electrode placed on the eye.  Eventually, the flickering occurred so fast that the fish was unable to tell whether or not the light was continuous, and thus no chemical response was produced (Figure 4). This was referred to as the fish’s CFF threshold, or “critical flicker fusion threshold” (Chung, et al. 2014).  The threshold differs from fish to fish depending on its circadian rhythm and lighting in its natural environment, but for this experiment Chung et al. focused mainly on the threshold values of the spiny damselfish.

animation

Figure 4. The critical flicker fusion frequency is reached when the light flickers so fast that it appears as a continuous light.

They found each damselfish’s threshold by immobilizing the fish on a plastic board and covering one of its eyes. They placed an electrode on the uncovered eye (which was exposed to air) and flashed a light at the fish.  From the signals measured, the researchers found that when the fish were kept in water with CO2 levels equal to levels that the ocean is estimated to reach by the year 2100, their CFF threshold values significantly decreased.  This means their ability to see worsened substantially.  This could affect the survivability of a fish, impairing its ability to quickly recognize harmful situations and avoid capture by predators.

For the second part of the experiment, the researchers sought to examine whether or not it was truly GABAA receptors being influenced by the increasing acidification of the environment. They treated the fish with GABA antagonists and ran the same trials to test their thresholds. An antagonist is a chemical that binds to neurotransmitter receptors to prevent neurotransmitters from binding to these receptors. Antagonists share highly similar molecular structures to the neurotransmitter that the receptor normally binds with, and is therefore able to bind to these receptors in order to reduce the effects of a neurotransmitter by blocking the receptors. In this case, a GABA antagonist would reverse the effects of GABA and in turn cause more neural stimulation because it stops GABA’s ability to reduce a neuron’s ability to send signals.

In addition to the reversal effects of the GABA antagonist, researchers also found that the length of exposure to the GABA antagonist was correlated to the extent of the reversal (Figure 4). When introduced to the GABA antagonist for 20 minutes, the CFF threshold of the fish in elevated CO2 water increased significantly and became closer to normal.  These findings are in conjunction with knowing that when GABA binds to its receptors, it stops neurons from firing, so with lower levels of GABA binding, the neurons in the eye will activate more. This GABA decrease would allow the fish to react to stimuli more quickly and be able to identify more changes in their environment. Although the thresholds for the fish in normal water also increased slightly when GABA antagonists were added, this change was not statistically significant.

Figure 5

Figure 5. Using GABA antagonists, the thresholds of fish exposed to high levels of CO2 can increase.  This graph shows the thresholds of fish in normal water (triangles) and fish in water with high CO2 levels (squares).  The fish were introduced to GABA antagonists at time zero. (Chung, et al. 2014, Figure 1)

Chung and colleagues convincingly demonstrate how ocean acidification decreases the ability of fish to resolve sudden visual changes. What they don’t discuss yet is how we could go about counteracting the effects of ocean acidification, should it reach the predicted levels in Figure 1, but it’s a distressing possibility that is recognized as a very big issue and is being researched.  Further research should also investigate how GABAA receptors are actually changed by ocean acidification or how the brain itself may be affected, as the authors mention.  Another important topic to look into is how high CO2 levels affect GABAA receptors in all fish, not just this specific species of damselfish.

To conclude, the above example delves into a real-world consequence of global warming.  By showing that damselfish were not able to react to stimuli as well or quickly when exposed to acidified water, this research is further evidence that unless we cut down on carbon and fossil fuel emissions and slow the acidification of the ocean, it’s likely that the sensory systems and behavior of fish will begin to endure harmful effects.  This sensory deprivation could likely result in a decrease of the fitness of affected species and even extinction, reversing millions of years of evolution and mutations because of their inability to react in dangerous environments.  Larger devastation up and down the food chain may occur, unless species have sufficient time to adapt to the impending threats. These adaptations could take hundreds of years to occur and it’s unknown if the damselfish would survive long enough.

 

References

Allan BJM, Domenici P, McCormick MI, Watson S-A, Munday PL. 2013 Elevated CO2 affects predator-prey interactions through altered performance. PLoS ONE 8, e58520. (doi:10.1371/journal.pone.0058520).

Chung, W.-S, Marshall, N.J., Watson, S.-A., Munday, P.L., Nilsson, G.E. 2014. Ocean acidification slows retinal function in a damselfish through interference with GABAA receptors. Journal of Experimental Biology 217: 323-326. (doi: 10.1242/jeb.092478)

McNeil, B. I., and R. J. Matear. 2006. Projected climate change impact on oceanic acidification. Carbon Bal. Manag. 1:1–6. (doi: 10.1002/ece3.756).

Mora-Ferrer, C and Neumeyer, C. 2009. Neuropharmacology of vision in goldfish: a review. Vision Res. 49, 960-969.

Munday P, Dixson D, Donelson J, Jones G, Pratchett M, Devitsina G, Døving K. 2009. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc Natl Acad Sci 106:1848–1852. (doi:10.1073/pnas.0809996106).

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