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Fooling Nemo


Ocean acidification results in behaviour that decreases the odds of survival for reef fish

By Kate Osborne

Clownfish use their sense of smell to warn them of the presence of predators, but the pH conditions expected as a result of climate change fool them into swimming towards impending danger.

Have you ever had the feeling that something is wrong? “The hair on my neck prickled” and “I smelt a rat” are two examples of expressions to describe that feeling. What we perceive as intuition is our sensory system sending messages to our brain.

For the orange clownfish (Amphiprion percula), “I smell danger” is literally true. Larval fish have an innate ability to avoid seawater that has come from a predator tank. However, scientists have found that when the pH of the water is lowered to conditions that are expected as a result of climate change, the clownfish were attracted to the water where the predators were living.

Clownfish spend most of their life within a few metres of their host anemone. However, like many reef fish, the earliest life stage as larval fishes is spent away from the reef surface, living and feeding in the water column.

Initial research on the clownfish olfactory system, or sense of smell, sought to discover how the larval fish were able to locate an anemone amongst the myriad of life on the reef. Scientists found that the larval fish were able to smell chemicals released by the anemone and were attracted towards them.

Now there is a growing body of research suggesting that clownfish can detect a surprising variety of scents. They can, for example, smell traces of leaf litter from rainforest plants that indicate they are swimming near the fringing reef of an island – their preferred habitat. They can also tell the difference between a predator and other fishes just from the scent in the water.

The olfactory world of the clownfish was revealed by putting the fish into an aquarium called a flume chamber that is set up like a two-bedroom apartment. Seawater flows from two sources and is directed into one “room” or the other of the aquarium. The rooms are separated by a partition, and fish can choose where they spend their time.

Orange clownfish showed an astonishing ability to discriminate and choose between rooms based on the olfactory cues in the water. When one room had a predator scent and the other was just seawater, they chose seawater 100% of time. But when the scent of non-predator fish was in one tank and seawater in the other they showed no preference between rooms, suggesting that not only could they detect the scent of another fish but could discriminate if that fish was a potential threat.

The experimental set-up allows scientists to change not only the scents in the water but the chemical composition of the seawater itself.

Approximately 25% of greenhouse gases produced by human activities are absorbed by the ocean. Atmospheric carbon dioxide (CO2) at the ocean surface reacts with seawater, producing carbonic acid and releasing hydrogen ions that make the water more acidic. Ocean acidification is measured by pH, with lower values of pH being more acidic. Over the past 400,000 years the pH of seawater has fluctuated by ± 0.1, and is currently at its lowest point within this range.

Dr Danielle Dixson of James Cook University designed experiments to test how clownfish would respond to changes in seawater chemistry. When she lowered the pH to mimic ocean conditions expected to occur by the end of the century, the results were surprising. “The behaviour of the fish completely changed,” she said. “They were no longer able to distinguish between the smell of a predator and a non-predator, and became strongly attracted to the seawater that had come from the predator tank.”

In another reef fish species, Pomacentrus chrysurus, experiments have already shown that behavioural changes caused by acidified water led to lower survival in the ocean. When P. chrysurus was raised in low pH water and then relocated back to the reef, mortality due to predation in the first few hours increased dramatically.

The next step is to understand how ocean acidification can lead to behavioural change. One possibility is that the physical structure of the organs that enable smell is damaged by exposure to the low pH water or that some other abnormality occurs during the early stages of growth. For the clownfish this seems unlikely. Prof Phillip Munday, who researches the effects of climate change on fishes at James Cook University, examined the nasal cavity of fish exposed to low pH with an electron microscope. He found the sensory lining seemed normal and there was a dense covering of cilia and numerous receptor neurons within the nasal cavity.

The answer appears to lie in changes occurring in the brain. Dixson’s and Munday’s experiments are among a number of studies that suggest that acidification is causing cognitive failure through disruption of the chemical gradients within the fish’s sensory system. “It’s not just their olfactory system that’s affected,” Dixson said. “We know that their hearing is affected, and we’ve shown that their ability to learn is affected. The fish are bolder when they have been treated with CO2. They venture farther away from the habitat and they swim around more. It’s multiple levels of systems that are not obviously connected, so we’re really thinking it’s a cognitive issue.”

As Dixson’s experimental fish were tested in conditions that are still far removed from the current ocean environment, a pertinent question to ask is: how much is too much? Dixson explained that tolerance to acidity varies, even between closely related fish species. She expects some fish species will be able to adapt but the prognosis for the clownfish is not good.

“Clownfish can live for over 20 years,” she said. “The longer the generation time, the less likely it is that the species will be able to adapt in an evolutionary sense to relatively rapid changes in seawater chemistry.”

While genetic change will be slow, fish may be able to acclimatise to changes in ocean chemistry. Acclimatisation refers to change that occurs within the lifetime of an individual. As yet, there is no evidence to suggest that reef fish can acclimatise to gradual ocean acidification. In one experiment where reef fish were exposed to higher temperatures, physiological acclimatisation came at a cost of smaller size and poorer condition.

The discovery that ocean acidification results in behaviour that decreases the odds of survival for reef fish has potentially dire implications for all ocean-dwelling creatures. Ultimately behaviour in all animals is regulated by chemical gradients that are sensitive to very small changes. Changes in ocean chemistry are occurring at an unprecedented rate, and the ability of ecosystems such as coral reefs to adapt or acclimatise is unknown.

Ocean acidification is just one of many challenges that coral reef ecosystems face as a result of global climate change. Munday said that it seems in terms of their life history traits and their physical traits that reef fish may be quite resilient to ocean acidification expected to occur as a result of climate change. “Their behaviour is remarkably sensitive,” he said. “It may be the indirect effects of CO2 on ocean pH, moderated through behaviour, that may be most important.”

Kate Osborne is an ecologist and science writer.