Response of spiny damselfish to elevated levels of carbon dioxide. Fish (N=20) were offered either control water or water containing a chemical alarm cue in the choice chamber. *Denotes statistical significance from respective control value at P < 0.05. Graphic: Heuer, et al., 2016 / Scientific Reports

MIAMI, 12 September 2016 (University of Miami) – In a first-of-its-kind study, researchers from the University of Miami (UM) Rosenstiel School of Marine and Atmospheric Science and the ARC Centre of Excellence for Coral Reef Studies at James Cook University showed that increased carbon dioxide concentrations alters brain chemistry that may lead to neurological impairment in some fish. Understanding the impacts of increased carbon dioxide levels in the ocean, which causes the ocean to become more acidic, allows scientists to better predict how fish will be impacted by future ocean acidification conditions. “Coral reef fish, which play a vital role in coral reef ecosystems, are already under threat from multiple human and natural stressors,” said lead author of the study Rachael Heuer, a UM Rosenstiel School alumna which conducted the study as part of her Ph.D. work. “By specifically understanding how brain and blood chemistry are linked to behavioral disruptions during CO2 exposure, we can better understand not only ‘what’ may happen during future ocean acidification scenarios, but ‘why’ it happens.” In this study, the researchers designed and conducted a novel experiment to directly measure behavioral impairment and brain chemistry of the Spiny damselfish, (Acanthochromis polyacanthus) a fish commonly found on coral reefs in the western Pacific Ocean. During a three-week period, the scientists collected spiny damselfish from reefs off Lizard Island located on Australia’s Great Barrier Reef. The fish were separated into two groups—those exposed to ordinary CO2 “control” conditions and those exposed to elevated CO2 levels that are predicted to occur in the near future, but have already been observed in many coastal and upwelling areas throughout the world. Following the exposure, the fish were subjected to a behavioral test, and brain and blood chemistry were measured. The unique behavioral test, employed a two-choice flume system, where fish were given the choice between control seawater or water containing a chemical alarm cue, which they typically avoid since it represents the smell associated with an injured fish of its own species. The researchers found that the damselfish exposed to elevated carbon dioxide levels were spending significantly more time near the chemical alarm cue than the control fish, a behavior that would be considered abnormal. The measurements of brain and blood chemistry provided further evidence that elevated CO2 caused the altered behavior of the fish. “For the first time, physiological measurements showing altered chemistry in brain and blood have been directly linked to altered behavior in a coral reef fish,” said UM Rosenstiel School Maytag Professor of Ichthyology and lead of the RECOVER Project Martin Grosell, the senior author of the study. “Our findings support the idea that fish effectively prevent acidification of internal body fluids and tissues, but that these adjustments lead to downstream effects including impairment of neurological function.” “If coral reef fish do not acclimate or adapt as oceans continue to acidify, many will likely experience impaired behavior that could ultimately lead to increased predation risk and to negative impacts on population structure and ecosystem function,” said Heuer, currently a postdoctoral researcher at the University of North Texas. “This research supports the growing number of studies indicating that carbon dioxide can drastically alter fish behavior, with the added benefit of providing accurate measurements to support existing hypotheses on why these impairments are occurring.” The study, titled “Altered brain ion gradients following compensation for elevated CO2 are linked to behavioural alternations in a coral reef fish,” was published in the 13 September 2016 online issue of the journal Scientific Reports. The study’s co-authors include: Rachael Heuer; Martin Grosell; Megan J. Welch and Jodie L. Rummer and Philip L. Munday from the ARC Centre of Excellence for Coral Reef Studies at James Cook University. The National Science Foundation, a University of Miami Koczy Fellowship, and the ARC Centre of Excellence provided funding support for the study. Heuer was also funded by an NSF Graduate Research Fellowship to conduct the research.

Study Links Altered Brain Chemistry, Behavioral Impairments in Fish Exposed to Elevated CO2

ABSTRACT: Neurosensory and behavioural disruptions are some of the most consistently reported responses upon exposure to ocean acidification-relevant CO2 levels, especially in coral reef fishes. The underlying cause of these disruptions is thought to be altered current across the GABAA receptor in neuronal cells due to changes in ion gradients (HCO3− and/or Cl−) that occur in the body following compensation for elevated ambient CO2. Despite these widely-documented behavioural disruptions, the present study is the first to pair a behavioural assay with measurements of relevant intracellular and extracellular acid-base parameters in a coral reef fish exposed to elevated CO2. Spiny damselfish (Acanthochromis polyacanthus) exposed to 1900 μatm CO2 for 4 days exhibited significantly increased intracellular and extracellular HCO3− concentrations and elevated brain pHi compared to control fish, providing evidence of CO2 compensation. As expected, high CO2 exposed damselfish spent significantly more time in a chemical alarm cue (CAC) than control fish, supporting a potential link between behavioural disruption and CO2 compensation. Using HCO3− measurements from the damselfish, the reversal potential for GABAA (EGABA) was calculated, illustrating that biophysical properties of the brain during CO2 compensation could change GABAA receptor function and account for the behavioural disturbances noted during exposure to elevated CO2.

Altered brain ion gradients following compensation for elevated CO2 are linked to behavioural alterations in a coral reef fish