Interspecific Differences in Hypoxia-Induced Gill Remodeling in Carp

Abstract

The gills of many fish, but in particular those of crucian carp (Carassius carassius) and goldfish (Carassius auratus), are capable of extensive remodeling in response to changes in oxygen (O2), temperature, and exercise. In this study, we investigated the interspecific variation in hypoxia-induced gill modeling and hypoxia tolerance in 10 closely related groups of cyprinids (nine species, with two strains of Cyprinus carpio). There was significant variation in hypoxia tolerance, measured as the O2 tension (P(O2)) at which fish lost equilibrium (LOEcrit), among the 10 groups of carp. In normoxia, there was a significant, phylogenetically independent relationship between mass-specific gill surface area and LOEcrit, with the more hypoxia-tolerant carp having smaller gills than their less hypoxia-tolerant relatives. All groups of carp, except the Chinese bream (Megalobrama pellegrini), increased mass-specific gill surface area in response to 48 h of exposure to hypoxia (0.7 kPa) through reductions in the interlamellar cell mass (ILCM) volume. The magnitude of the hypoxia-induced reduction in the ILCM was negatively correlated with LOEcrit (and thus positively correlated with hypoxia tolerance), independent of phylogeny. The hypoxia-induced changes in gill morphology resulted in reduced variation in mass-specific gill surface area among species and eliminated the relationship between LOEcrit and mass-specific gill surface area. While behavioral responses to hypoxia differed among the carp groups, there were no significant relationships between hypoxia tolerance and the Po2 at which aquatic surface respiration (ASR) was initiated or the total number of ASR events observed during progressive hypoxia. Our results are the first to show that the extent of gill remodeling in cyprinids is associated with hypoxia tolerance in a phylogenetically independent fashion.

Warm acclimation improves hypoxia tolerance in Fundulus heteroclitus

“…Remodelling of gill morphology has primarily been investigated in the context of acclimation to hypoxia (e.g. Crispo and Chapman, 2010), and this has been shown to occur via changes in the ILCM in a variety of fish species (Sollid et al, 2003(Sollid et al, , 2005aNilsson, 2007;Ong et al, 2007;Matey et al, 2008;Turko et al, 2012;Dhillon et al, 2013;Johannsson et al, 2014;Anttila et al, 2015) including killifish (Borowiec et al, 2015). Less is known about the effects of thermal acclimation on gill morphology, but decreases in the ILCM at warmer temperatures have been observed in crucian carp, goldfish (Sollid et al, 2005b;Mitrovic and Perry, 2009) and killifish (Barnes et al, 2014).…”

“…It is unclear whether the ability to remodel the ILCM is broadly distributed across fish taxa, or whether it represents a specialization of fishes occupying habitats that undergo periodic hypoxia (Nilsson, 2007;Dhillon et al, 2013). Thermal acclimation does not improve hypoxia tolerance in two species of coral reef fishes (Nilsson et al, 2010), which suggests that either these species lack the capacity to modify the ILCM or the ILCM is fully regressed at all of the relatively high temperatures tested in these tropical fishes.…”

Ecological Influences and Morphological Correlates of Resting and Maximal Metabolic Rates across Teleost Fish Species

“…When faced with hypoxic and hypercapnic conditions, several fish species increase oxygen extraction and transport efficiency by modulating gill surface area, oxygen affinity of haemoglobin and muscle mitochondrial density (Dhillon et al 2013;Fu et al 2014;Nilsson and Renshaw 2004). Additionally, at least three cyprinid species (Carassius carassius, C.…”

“…In our dataset, species belonging to the genera Carassius, Rhodeus, Cyprinus, Hypophthalmichthys and Aristichthys, which are known to tolerate very high levels of hypoxia (Dhillon et al 2013;Fu et al 2014), exhibit very low levels of adjusted RMR (range:…”

The hypoxia signaling pathway and hypoxic adaptation in fishes

“…Second, they alter the shape and structure of the gill to enhance oxygen exchange [41][42][43][44][45][46]. Some fishes alter the cardiac K(ATP) channel, metabolic rate, and increase the number of red blood cells [47,48].…”