Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus

Abstract

We have previously found that the gills of crucian carp Carassius carassius living in normoxic (aerated) water lack protruding lamellae, the primary site of O2 uptake in fish, and that exposing them to hypoxia increases the respiratory surface area of the gills ∼7.5-fold. We here examine whether this morphological change is triggered by temperature. We acclimated crucian carp to 10, 15, 20 and 25°C for 1 month, and investigated gill morphology, oxygen consumption and the critical oxygen concentration at the different temperatures. As expected, oxygen consumption increased with temperature. Also at 25°C an increase in the respiratory surface area, similar to that seen in hypoxia, occurred. This coincided with a reduced critical oxygen concentration. We also found that the rate of this transformation increased with rising temperature. Goldfish Carassius auratus, a close relative to crucian carp, previously kept at 25°C, were exposed to 15°C and 7.5°C. At 7.5°C the respiratory surface area of its gills was reduced by development of an interlamellar cell mass as found in normoxic crucian carp kept at 10-20°C. Thus, both species alter the respiratory surface area in response to temperature. Rather than being a graded change, the results suggest that the alteration of gill morphology is triggered at a given temperature. Oxygen-binding data reveal very high oxygen affinities of crucian carp haemoglobins, particularly at high pH and low temperature, which may be prerequisites for the reduced gill respiratory surface area at low temperatures. As ambient oxygen and temperature can both induce the remodelling of the gills, the response appears primarily to be an adaptation to the oxygen demand of the fish.