Thin tough skin, slow-growing gills protect larval Antarctic fish

Very thin but hardy, unblemished skin and slow developing gills appear to be keys to survival for newly hatched Antarctic notothenioids, a group of fish whose adults thrive in icy waters because of antifreeze proteins (AFPs) in their blood.

Such adaptations are important, researchers at the University of Illinois at Urbana-Champaign say, because the larval fish of at least two species of notothenioids that inhabit the Ross Sea at McMurdo Sound and Terra Nova Bay surprisingly lack sufficient antifreeze to protect them through their first three months of life.

The unexpected discovery, reported online by the Journal of Experimental Biology ahead of regular publication, counters the assumption that these vital proteins must be present from the time of hatching -- a view held by scientists since fish AFPs were found in the 1960s.

Internal fluids such as blood in many notothenioids are about half as salty as seawater. While seawater reaches its freezing point at -1.91 degrees Celsius, fish fluids will freeze at about -1 degree Celsius. The water where these species dwell rarely rises above the freezing point and is regularly filled with ice crystals.

"The way that we've understood how adult polar fishes survive has been based on their use of these antifreeze proteins to lower the freezing point of their internal fluids," said lead author Paul A. Cziko, a research specialist in the department of animal biology. "We finally got a chance to look at the larval fish, and it seems that they don't always have to have antifreeze proteins to survive."

Cziko, who earned bachelor's degrees in honors biology and biochemistry in 2004 from Illinois, studied in Antarctica as an undergraduate with animal biology professors Chi-Hing (Christina) Cheng and Arthur L. DeVries, who discovered AFPs in notothenioids.

The research team, which also included Clive W. Evans of the University of Auckland in New Zealand, studied three notothenioid species: Gymnodraco acuticeps (naked dragonfish); Pagothenia borchgrevinki (bald notothen); and Pleuragramma antarcticum (Antarctic silverfish). All species develop as eggs for between five and 10 months before hatching in icy waters in the Austral spring. Five years of data, collected from 2000 to 2004, were analyzed.

While each species spawned at different depths, all larvae swam upward into platelet ice, located just below several meters of surface ice, when they hatched, seeking perhaps a safe area to hide from predators, Cziko said.

The average freezing point of the larval fish fluids was about -1.3 degrees Celsius, according to testing with a nanoliter osmometer. Yet the fish hatch into water at almost -2 degrees Celsius. "With all this ice around, there is no way they can prevent freezing," Cheng said. "At -2 degrees Celsius, internal fluids would freeze instantly and the baby fish would die."

"This 0.7 of a degree Celsius is small but very significant," Cziko said. "In adults, we find ice in their bodies but these small crystals don't grow because of antifreeze proteins. Finding that larval fish don't have enough antifreeze really threw off how we understand survival in fish."

While the larvae of one species, the bald notothen, survives using high levels of AFPs like the adults, the researchers were astonished to find that the dragonfish and silverfish hatchlings have too little to allow survival during direct contact with ice. Looking more closely, the researchers discovered that the gills of all three species were undeveloped at hatching, minimizing the risk of ice passing through them to get inside.

The delicately thin skin of the larval fish may offer additional protection, because their skin hasn't yet been exposed to environmental damages, Cheng said. The skin and undeveloped gills, Cziko said, may combine to allow time for antifreeze levels to rise.

The production of AFPs did not show much increase in the larval fish until 84 days after hatching, the researchers found. Adult values weren't reached for 147 days.

"Amazingly," DeVries said, "for about three months the larval fish must rely only on their skin and gills to prevent ice from entering, and to keep them from freezing solid."

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The National Science Foundation supported the research through grants to Cheng and DeVries. Cziko was supported by a grant (Special Undergraduate Research on the Environment) from the U. of I. Environmental Council.

Editor's Note: Paul Cziko, Christina Cheng and Arthur DeVries may be reached at 217-333-4245, or by email, respectively, at pcziko@life.uiuc.edu, c-cheng@uiuc.edu and adevries@uiuc.edu.


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