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.

Interspecific Differences in Hypoxia-Induced Gill Remodeling in Carp

“…However, upon exposure to hypoxia or conditions that increase metabolic demands, a low gill surface area may impede O 2 uptake, and both crucian carp and goldfish respond by reducing the size of the ILCM, exposing the lamellae and increasing the functional surface area of the gill. In general, this response requires days to complete at low temperatures, because it involves increasing the rate of apoptosis and decreasing the rate of mitosis in the ILCM, although faster responses have been noted at higher temperatures or during sustained exercise (Sollid et al 2005a;Brauner et al 2011;Tzaneva et al 2011a;Perry et al 2012). The list of species that possess an ILCM and subsequently undergo gill remodeling in response to changes in O 2 requirements has increased, and beyond crucian carp and goldfish, hypoxia-induced gill remodeling has also been shown to occur in the scaleless carp (Gymnocypris przewalskii; Matey et al 2008) and the mangrove killifish (Kryptolebias marmoratus; Ong et al 2007), both hypoxia-tolerant species, albeit not to the same extent as crucian carp and goldfish.…”

“…Since the first description of hypoxia-induced gill remodeling in crucian carp (Sollid et al 2003), similar temperature-and exercise-dependent responses in crucian carp and/or goldfish have been described (Sollid et al 2005b;Sollid and Nilsson 2006;Fu et al 2011;Brauner et al 2011;Nilsson et al 2012;Perry et al 2012). In all these studies, it is clearly shown that crucian carp and goldfish under resting, normoxic conditions Table 1: List of groups, mean weight, and GenBank accession numbers…”

Implications for Osmorespiratory Compromise by Anatomical Remodeling in the Gills of Arapaima gigas

“…Conversely, the gills of sluggish or benthic fishes have low numbers of lamellae per millimeter of filament length and thus display a small respiratory surface area (Gray, 1954;Hughes, 1984). Recently, the plasticity of the gill dimensions and the reversible remodeling of gill morphology have been studied in fish exposed to pollutants and transferred to clean water (Cerqueira and Fernandes, 2002;Fernandes and Mazon, 2003;Nilsson et al, in press), in response to hypoxia and temperature (Sollid et al, 2003;Sollid and Nilsson, 2006;Perry et al, 2012) and during defense against parasite infections (Nilsson et al, 2012).…”

Gill paracellular permeability and the osmorespiratory compromise during exercise in the hypoxia-tolerant Amazonian oscar (Astronotus ocellatus)

“…Previously, the ILCM has also been found in a variety of cyprinids (e.g. Sollid et al 2003Sollid et al , 2005Matey et al 2008;Perry et al 2010Perry et al , 2012Smith et al 2012;Dhillon et al 2013) and cyprinodonts (e.g. Ong et al 2007; Barnes et al 2014).…”

“…The function of the ILCM is generally thought to be minimization of unfavorable ionic and osmotic fluxes under conditions where some restriction of respiratory gas exchange is tolerable (Sollid and Nilsson 2006;Nilsson 2007). For example, in crucian carp and goldfish, it is present at close to 100 % coverage in resting fish at cold temperatures, but is reduced or eliminated when the fish are exercised or acclimated to high temperatures (Sollid et al 2003(Sollid et al , 2005Sollid and Nilsson 2006;Nilsson 2007;Perry et al 2010Perry et al , 2012Brauner et al 2011;Smith et al 2012). Its presence in the oscar at about 30 % lamellar height, even at relatively high temperature (28 °C), and after 4 h of exercise (Table 2; Fig.…”