Interspecific Differences in Hypoxia-Induced Gill Remodeling in Carp Author(s): Rashpal S. Dhillon, Lili Yao, Victoria Matey, Bo-Jian Chen, An-Jie Zhang, Zhen- Dong Cao, Shi-Jian Fu, Colin J. Brauner, Yuxiang S. Wang, and Jeffrey G. Richards Source: Physiological and Biochemical Zoology, Vol. 86, No. 6 (November/December 2013), pp. 727-739 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/10.1086/673180 . Accessed: 18/11/2013 16:25 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to Physiological and Biochemical Zoology. http://www.jstor.org This content downloaded from 137.82.81.121 on Mon, 18 Nov 2013 16:25:38 PM All use subject to JSTOR Terms and Conditions 727 Interspecific Differences in Hypoxia-Induced Gill Remodeling in Carp Rashpal S. Dhillon1,* (and thus positively correlated with hypoxia tolerance), inde- Lili Yao1 pendent of phylogeny. The hypoxia-induced changes in gill mor- Victoria Matey2 phology resulted in reduced variation in mass-specific gill surface Bo-Jian Chen3 area among species and eliminated the relationship between 3 An-Jie Zhang LOEcrit and mass-specific gill surface area. While behavioral re- Zhen-Dong Cao3 sponses to hypoxia differed among the carp groups, there were Shi-Jian Fu3 no significant relationships between hypoxia tolerance and the 1 Colin J. Brauner Po2 at which aquatic surface respiration (ASR) was initiated or Yuxiang S. Wang4 the total number of ASR events observed during progressive Jeffrey G. Richards1 hypoxia. Our results are the first to show that the extent of gill 1Department of Zoology, University of British Columbia, remodeling in cyprinids is associated with hypoxia tolerance in 6270 University Boulevard, Vancouver, British Columbia V6T a phylogenetically independent fashion. 1Z4, Canada; 2Department of Biology, San Diego State University, San Diego, California; 3Laboratory of Evolutionary Physiology and Behavior, Chongqing Key Laboratory of Animal Biology, Chongqing Normal University, Chongqing, China; 4Department of Biology, Introduction Queen’s University, 116 Barrie Street, Kingston, Ontario K7L 3N6, Canada Environmental hypoxia can be common in many aquatic habitats (Val et al. 2006; Diaz and Breitburg 2009), and the fish that Accepted 7/14/2013; Electronically Published 9/23/2013 inhabit these waters have evolved a suite of strategies to enhance hypoxic survival. These strategies serve to either enhance oxygen (O2) uptake from the O2-depleted water or prolong survival when environmental O tensions (Po ) are below levels where routine ABSTRACT 2 2 metabolic rate can be maintained. Crucian carp (Carassius car- The gills of many fish, but in particular those of crucian carp assius) and goldfish (Carassius auratus), both members of the (Carassius carassius) and goldfish (Carassius auratus), are capable family Cyprinidae, are considered the champions of hypoxia (and of extensive remodeling in response to changes in oxygen (O2), even anoxia) tolerance, surviving months of severe hypoxia at temperature, and exercise. In this study, we investigated the in- cool temperatures (Van den Thillart et al. 1976; Walker and terspecific variation in hypoxia-induced gill modeling and hyp- Johansen 1977). This impressive hypoxia tolerance is associated oxia tolerance in 10 closely related groups of cyprinids (nine with their high hemoglobin-O2 binding affinity (Weber and Lyk- species, with two strains of Cyprinus carpio). There was significant keboe 1978; Lomholt and Johansen 1979; Sollid et al. 2005b), variation in hypoxia tolerance, measured as the O2 tension (Po2) large hepatic glycogen stores, alternative anaerobic pathways (in- at which fish lost equilibrium (LOEcrit), among the 10 groups of cluding ethanol production (Shoubridge and Hochachka 1980; carp. In normoxia, there was a significant, phylogenetically in- Johnston and Bernard 1983), and an ability to undergo reversible dependent relationship between mass-specific gill surface area depression of metabolic rate (Van Waversveld et al. 1989; Muusze and LOEcrit, with the more hypoxia-tolerant carp having smaller et al. 1998; Nilsson and Ostlund-Nilsson 2008). More recently, gills than their less hypoxia-tolerant relatives. All groups of carp, Sollid et al. (2003) also showed that crucian carp and goldfish except the Chinese bream (Megalobrama pellegrini), increased are capable of a dramatic remodeling of their gill morphology mass-specific gill surface area in response to 48 h of exposure to in response to hypoxia, greatly increasing gill surface area and hypoxia (0.7 kPa) through reductions in the interlamellar cell O2 diffusing capacity (Nilsson et al. 2012; Sollid et al. 2003; mass (ILCM) volume. The magnitude of the hypoxia-induced Tzaneva et al. 2011a, 2011b). reduction in the ILCM was negatively correlated with LOEcrit 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 * Corresponding author; e-mail: [email protected]. have been described (Sollid et al. 2005b; Sollid and Nilsson Physiological and Biochemical Zoology 86(6):727–739. 2013. ᭧ 2013 by The 2006; Fu et al. 2011; Brauner et al. 2011; Nilsson et al. 2012; University of Chicago. All rights reserved. 1522-2152/2013/8606-3039$15.00. Perry et al. 2012). In all these studies, it is clearly shown that DOI: 10.1086/673180 crucian carp and goldfish under resting, normoxic conditions This content downloaded from 137.82.81.121 on Mon, 18 Nov 2013 16:25:38 PM All use subject to JSTOR Terms and Conditions 728 Dhillon, Yao, Matey, Chen, Zhang, Cao, Fu, Brauner, Wang, and Richards Table 1: List of groups, mean weight, and GenBank accession numbers SEM (g) GenBank accession number ע Species Common name Mean weight KC808485 37. ע Spinibarbus sinensis Qingbo 2.35 KC808480 1.46 ע Cyprinus carpio Common carp 17.48 KC808479 1.63 ע C. carpio Koi 21.88 KC808478 19. ע Carassius auratus Goldfish 4.26 KC808477 70. ע Carassius carassius Crucian carp 10.80 KC808486 29. ע Megalobrama pellegrini Chinese bream 8.80 KC808484 79. ע Hypophthalmichthys molitrix Silver carp 14.71 KC808481 1.36 ע Aristichthys nobilis Bighead carp 7.46 KC808482 1.44 ע Ctenopharyngodon idellus Grass carp 10.90 KC808483 64. ע Mylopharyngodon piceus Black carp 6.57 at low temperature possess a large interlamellar cell mass tive traits involved in hypoxia tolerance (Mandic et al. 2009a, (ILCM; Sollid et al. 2003, 2005b), which substantially reduces 2009b, 2013), but to date, no phylogenetically corrected com- total gill surface area. When O2 is plentiful or metabolic de- parative analysis has been performed on cyprinids, and the re- mands are low, the smaller gill surface area is thought to min- lationship between the capacity and extent of gill remodeling and imize ionoregulatory challenges (Sollid et al. 2003; Nilsson et hypoxia tolerance is largely unknown. al. 2012) or provide a barrier to toxic substances or pathogens In this study, we used a phylogenetically corrected comparative that target the gill (Nilsson et al. 2012). However, upon ex- approach to determine whether hypoxia-induced gill remodeling posure to hypoxia or conditions that increase metabolic de- is a general feature of cyprinids or related to their ability to survive mands, a low gill surface area may impede O2 uptake, and both hypoxia. To accomplish this goal, we selected 10 groups from crucian carp and goldfish respond by reducing the size of the the family Cyprinidae (including two strains of the common ILCM, exposing the lamellae and increasing the functional sur- carp Cyprinus carpio) from central China that are found in en- face area of the gill. In general, this response requires days to vironments ranging from stagnant ponds that can be prone to complete at low temperatures, because it involves increasing eutrophication and winter ice cover (in the case of crucian carp, the rate of apoptosis and decreasing the rate of mitosis in the goldfish, and common carp) to faster-moving rivers (e.g., qingbo ILCM, although faster responses have been noted at higher Spinibarbus sinensis, silver carp Hypophthalmichthys molitrix, temperatures or during sustained exercise (Sollid et al. 2005a; black carp Mylopharyngodon piceus, and Chinese bream Mega- Brauner et al. 2011; Tzaneva et al. 2011a; Perry et al. 2012). lobrama pellegrini; Kong et al. 2007; Yi et al. 2010; Lou 1990). The list of species that possess an ILCM and subsequently Other species (e.g., black carp and grass carp Ctenopharyngodon undergo gill remodeling in response to changes in O2 require- idellus) are known to occupy the full spectrum of freshwater ments has increased, and beyond crucian carp and goldfish, hyp- habitats. We propose a hypothesis for the phylogenetic relation- oxia-induced gill remodeling has also been shown to occur in ship among the study groups based on the cytochrome b se- the scaleless carp (Gymnocypris przewalskii; Matey et al. 2008) quence, and we use the phylogenetic information in our com- and the mangrove killifish (Kryptolebias marmoratus; Ong et al. parative analysis of hypoxia tolerance, assessed as the Po2 at which 2007), both hypoxia-tolerant species, albeit not to the same extent individuals showed a loss of equilibrium, and our measures of as crucian carp and goldfish. Although it is tempting to assign the extent of gill remodeling observed during a 48-h exposure Њ adaptive value to hypoxia-induced gill remodeling as a response to a Po2 of 0.7 kPa at 12 C.