Interspecific differences in hypoxia-induced gill remodeling in carp.
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.
Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia V6T 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, Queen's University, 116 Barrie Street, Kingston, Ontario K7L 3N6, Canada.
Rashpal S
RS
Dhillon
Lili
L
Yao
Victoria
V
Matey
Bo-Jian
BJ
Chen
An-Jie
AJ
Zhang
Zhen-Dong
ZD
Cao
Shi-Jian
SJ
Fu
Colin J
CJ
Brauner
Yuxiang S
YS
Wang
Jeffrey G
JG
Richards
D000818:Animals; D002347:Carps / Q000235:genetics / Q000378:metabolism*; D045303:Cytochromes b / Q000737:chemistry / Q000235:genetics; D004247:DNA / Q000737:chemistry / Q000235:genetics; D005880:Gills / Q000378:metabolism* / Q000648:ultrastructure; D000860:Hypoxia / Q000378:metabolism*; D008855:Microscopy, Electron, Scanning / Q000662:veterinary; D010100:Oxygen / Q000378:metabolism*; D010802:Phylogeny; D016133:Polymerase Chain Reaction / Q000662:veterinary
D004247:DNA; D045303:Cytochromes b; D010100:Oxygen