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First published online September 9, 2003
Inside JEB |
REMARKABLE REMODELLING GILLS
kathryn{at}biologists.com
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Despite their exotic name, crucian carp aren't the most charismatic creatures. Although the drab fish are unexceptional on the surface, they are amazingly hypoxia tolerant when their lakes freeze over. In fact, the fish can survive complete anoxia for several months. Intrigued by the carp's remarkable tolerance of oxygen deprivation, Göran Nilsson looked at the dowdy fish's gills to see how they had adapted to life in a frozen lake. But surprisingly, the carp's gills were almost featureless. They seemed to lack the lamellae that are crucial for fish's respiration.
So why were the fish's gills so smooth? Nilsson suspected that it could have something to do with energy conservation throughout the year. Freshwater fish are constantly battling against their element, continually absorbing water by osmosis; some species absorb as much as 80% of their body weight every hour! So they constantly excrete the excess water, but they also lose crucial metabolic ions that they replenish with an elaborate suite of pumps and ion channels; but at a high metabolic cost. Nilsson reasoned that if the fish could cut down on their flooding problem, they'd retain their osmotic balance and save energy in the long run. Could the carp have done away with their gill's lamellae to reduce the water influx and save energy? Working with Jørund Sollid, Nilsson decided to scrutinise the gills under more realistic conditions (p. 3667).
First, they needed some crucian carp. Sollid remembers that the fish were extremely cooperative and easy to catch in traps. Returning with the fish to the lab, Sollid began slowly dropping the oxygen level in the carp's aquarium, collecting samples of the fish's gills as the water became progressively more hypoxic and looking at the tissue with electron microscopy.
But what he saw was completely unexpected. Sure enough the gills were smooth and featureless when the oxygen levels were high, but as the levels dropped, tiny lamellae began appearing, and within one week, the adult fish's gills were transformed to look like any other water-breathing fish! Nilsson and Sollid were astonished. No one had ever seen an adult vertebrate change its respiratory surface area. The team suspect that the carp increased their gill area as the oxygen levels dwindled to improve their oxygen uptake, despite the cost.
But how were the carp doing it? Were the lamellae growing or had that they been buried in packing tissue that had vanished? With the help of Paula de Angelis and Kristian Gundersen, Sollid began looking for evidence of cell growth if the lamellae grew, or apoptosis if packing tissue around the lamellae was shrinking back. After several months of tricky immunohistology Sollid realised that instead of growing lamellae, the cells in the gills had stopped dividing and began receding by apoptosis, revealing that the gill's lamellae were already there but obscured by the packing tissue.
Sollid is keen to investigate the gill's physiology and begin dissecting the complex cellular controls that regulate the gill's remarkable remodelling. The only thing that's holding Sollid back is that he can't do everything all at once, `but it's still very exciting' he adds.
References
Sollid, J., de Angelis, P., Gundersen, K. and Nilsson, G. E.
(2003). Hypoxia induces adaptive and reversible gross
morphological changes in crucian carp gills. J. Exp.
Biol. 206,3667
-3673.
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