The interactive effects of exercise and gill remodeling in goldfish (Carassius auratus)

Abstract

Gill remodeling in goldfish (Carassius auratus) is accomplished by the appearance or retraction of a mass of cells (termed the interlamellar cell mass or ILCM) between adjacent lamellae. Given the presumed effects of gill remodeling on diffusing capacity, the goals of the current study were (1) to determine the consequences of increased aerobic O(2) demand (swimming) on gill remodelling and (2) to assess the consequences of the presence or absence of the ILCM on aerobic swimming capacity. Fish acclimated to 7 °C exhibited a marked increase in the ILCM which occupied, on average, 70.0 ± 4.1% of the total interlamellar channel area in comparison to an average ILCM area of only 28.3 ± 0.9% in fish acclimated to 25 °C. Incrementally increasing swimming velocity in fish at 7 °C to achieve a maximum aerobic swimming speed (U (CRIT)) within approximately 3 h resulted in a marked loss of the ILCM area to 44.8 ± 3.5%. Fish acclimated to 7 °C were subjected to 35 min swimming trials at 30, 60 or 80% U (CRIT) revealing that significant loss of the ILCM occurred at swimming speeds exceeding 60% U (CRIT). Prior exposure of cold water-acclimated fish to hypoxia to induce shedding of the ILCM did not affect swimming performance when assessed under normoxic conditions (control fish U (CRIT) = 2.34 ± 0.30 body lengths s(-1); previously hypoxic fish U (CRIT) = 2.99 ± 0.14 body lengths s(-1)) or the capacity to raise rates of O(2) consumption with increasing swimming speeds. Because shedding of ILCM during U (CRIT) trials complicated the interpretation of experiments designed to evaluate the impact of the ILCM on swimming performance, additional experiments using a more rapid 'ramp' protocol were performed to generate swimming scores. Neither prior hypoxia exposure nor a previous swim to U (CRIT) (both protocols are known to cause loss of the ILCM) affected swimming scores (the total distance swum during ramp U (CRIT) trials). However, partitioning all data based on the extent of ILCM coverage upon cessation of the swimming trial revealed that fish with less than 40% ILCM coverage exhibited a significantly greater swimming score (539 ± 86 m) than fish with greater than 50% ILCM coverage (285 ± 70 m). Thus, while loss of the ILCM at swimming speeds exceeding 60% U (CRIT) confounds the interpretation of experiments designed to assess the impact of the ILCM on swimming performance, we suggest that the shedding of the ILCM, in itself, coupled with improved swimming scores in fish exhibiting low ILCM coverage (<40%), provide evidence that the ILCM in goldfish acclimated to cold water (7 °C) is indeed an impediment to aerobic swimming capacity.