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Difference in the Hypoxia Tolerance of the Round Crucian Carp and Largemouth Bass: Implications for Physiological Refugia in the Macrophyte Zone

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Difference in the Hypoxia Tolerance of the Round Crucian Carp and Largemouth Bass: Implications for Physiological Refugia in the Macrophyte Zone Short Report Difference in the hypoxia tolerance of the round crucian carp and largemouth bass: implications for physiological refugia in the macrophyte zone Hiroki Yamanaka1**, Yukihiro Kohmatsu2, and Masahide Yuma3 1 Center for Ecological Research, Kyoto University, 2-509-3 Hirano, Otsu, Shiga 520-2113, Japan 2 Research Institute for Humanity and Nature, 457-4 Motoyama, Kamigamo, Kita-ku, Kyoto 603-8047, Japan 3 Department of Environmental Solution Technology, Faculty of Science & Technology, Ryukoku University, 1-5 Seta-Oe, Otsu, Shiga 520-2194, Japan * Present address: Research Institute for Humanity and Nature (RIHN), 457-4 Motoyama, Kamigamo, Kita-ku, Kyoto 603-8047, Japan (e-mail: [email protected]) Received: August 28, 2006 / Revised: November 28, 2006 / Accepted: December 1, 2006 Abstract The hypoxia tolerance of larval and juvenile round crucian carp, Carassius auratus gran- Ichthyological doculis, and largemouth bass, Micropterus salmoides, was determined using respirometry to examine the potential of hypoxic areas in the macrophyte zone as physiological refugia for round crucian carp. Research The tolerance, which was measured as the critical oxygen concentration (Pc), was 1.32 mg O /l in the ©The Ichthyological Society of Japan 2007 2 round crucian carp and 1.93 mg O2/l in the largemouth bass. As the round crucian carp tolerated Ichthyol Res (2007) 54: 308–312 hypoxia better than the largemouth bass, hypoxic areas in the macrophyte zone might function as physiological refugia for round crucian carp. DOI 10.1007/s10228-006-0400-0 Key words Hypoxia tolerance · Critical oxygen concentration (Pc) · Physiological refugia · Carassius auratus grandoculis · Micropterus salmoides or many larval and juvenile fi shes, the macrophyte early life history (Miura, 1966; Yuma et al., 1998). This Fzone is essential. It harbors large numbers of food observation suggests that cyprinid fi shes dwelling in the organisms (Petr, 2000; Grenouillet et al., 2002) and func- macrophyte zone have the physiological potential to endure tions as physical refugia in which the structural complexity hypoxic conditions. For example, Fujiwara et al. (1995) of macrophyte stands serves as a barrier to predators reported that the larvae of the round crucian carp Carassius (Savino and Stein, 1982; Werner and Hall, 1988; Warfe and auratus grandoculis use the innermost part (nearest to Barmuta, 2004). However, as the predator population shore) of the macrophyte zone, where hypoxia is severe. naturally contains individuals of various sizes, not all are Despite this ecological information, no physiological study excluded by macrophyte stands, and prey species in the has compared the hypoxia tolerance of cyprinid fi shes macrophyte zone are always exposed to the threat of small and their predators, including introduced largemouth bass, predators. Micropterus salmoides. The macrophyte zone tends to be hypoxic because of the In this study, the hypoxia tolerance of round crucian carp decomposition of macrophytes and oxygen consumption by and largemouth bass was measured experimentally using bacteria (Petr, 2000). Because dissolved oxygen (DO) is one respirometry and compared to examine the potential of the of the most important environmental factors affecting fi sh macrophyte zone as physiological refugia for indigenous habitat utilization, a difference may exist in the species or cyprinid fi sh. The largemouth bass was selected as a poten- size composition of fi sh between the inside and outside of tial predator of cyprinids. It has depleted the indigenous fi sh the macrophyte zone. Chapman et al. (1996) compared the community in many bodies of water in Japan (Maezono and fi sh community in the hypoxic macrophyte zone and a well- Miyashita, 2003; Yonekura et al., 2004), and thus it has been oxygenated open area in Lake Nabugabo, Uganda, and recognized as a serious problem. The round crucian carp found that the hypoxic conditions in the macrophyte zone was used to represent the potential prey of the largemouth might protect endemic species from the introduced Nile bass, as it spends much time in the macrophyte zone during perch, Lates niloticus. As hypoxia tolerance differs among its larval and juvenile stages, from early spring to late fi sh species (Davis, 1975), it is quite possible that the mac- summer (Miura, 1966). Because largemouth bass also rophyte zone provides physiological refugia for hypoxia- inhabit the shallow littoral zone (including the macrophyte tolerant prey. zone), these two species must be associated in a predator– Many fi shes in Lake Biwa, Japan, inhabit the macrophyte prey relationship, making them suitable for a pilot study zone (Miura, 1966), and most of the indigenous cyprinid of physiological refugia in the macrophyte zone in Lake fi shes have a profound association with this zone in their Biwa. Implications for physiological refugia 309 Materials and Methods for round crucian carp and 2–7 days for largemouth bass. There is little information on the details of acclimation time Fish metabolism was measured as the routine metabolic for the larvae and juveniles of the two species with large rate (RMR; Fry, 1971), which is the mean rate for fi sh swim- variety of body size as used in the present study; thus, the ming voluntarily, i.e., normal activity, so it refl ects the acclimation time was decided by referring to Oikawa et al. oxygen consumption of fi sh under natural conditions (Fry, (1991), which set the period depending on the size of each 1971; Saint-Paul, 1984). Under normoxic conditions, fi sh individual of the sea bream Pagrus major for measuring consume oxygen at a constant rate (the RMR level in this oxygen consumption. All the fi sh were used for the experi- case), independent of the ambient DO. As the ambient DO ment in the fasting state, with an empty gut. Measurements starts to decrease, fi sh can maintain a constant level to some were made using a semiclosed respirometry system similar extent. However, below a specifi c DO level, oxygen con- to that described by Oikawa et al. (1991). Respiration sumption starts to decrease and becomes oxygen dependent chambers ranging in size from 30 to 4650 ml were prepared with further decrements in the DO (Fry, 1971). The thresh- for fi sh of different sizes. The system can operate four res- old DO level is called the critical oxygen concentration (Pc; piration chambers simultaneously. Each chamber was Ultsch et al., 1978; Saint-Paul, 1984). The Pc can be inter- equipped with an oxygen electrode (BRM-5; Iijima Elec- preted as the threshold level in the ambient DO below tronics, Gamagori, Japan). To avoid stimulating the fi sh, a which fi sh cannot maintain their normal activity. Pc and DO blind was placed around the respirometry system. are both expressed in mg O2/l, so Pc can be applied to fi eld After temperature acclimation, fi sh were carefully trans- DO distribution data directly to quantify the macrophyte ferred into each chamber. The number of fi sh placed in a zone as physiological refugia. Round crucian carp probably single chamber was determined so as to result in a constant −1 −1 survives under more severe hypoxic conditions, less than oxygen depletion speed of 1 mg O2 l h across the experi- the Pc, by adopting anaerobic metabolism, as does the ments. To facilitate acclimation to the chamber, the fi sh European crucian carp Carassius auratus (see Nilsson and were left in the chamber overnight. During this period, Renshaw, 2004), which is a related species. However, the chamber was supplied with oxygen-equilibrated water. anaerobic metabolism is an emergent way to withstand Then, the water supply was stopped and the DO in the anoxia, and metabolic condition will be depressed consider- chambers was measured at 5-min intervals. Three of the ably (Smith et al., 1996). Pc, used in the present study, is an four chambers were used to measure fi sh oxygen consump- indicator of hypoxia tolerance within the aerobic metabolism tion and the last one was kept as a control to measure the and a threshold DO level above which the normal background oxygen consumption by bacteria in the water. metabolism can be maintained. Therefore, the Pc can be a The result for the empty chamber was used to calibrate the suitable indicator to judge the specifi c DO condition as to fi sh oxygen consumption. The DO in the chambers decreased whether it is physiologically preferable and is comparable with fi sh respiration, and the difference between the initial among aquatic animals regardless of whether the animal and fi nal DO values for each measurement was noted as can employ anaerobic metabolism. the mass-specifi c oxygen consumption (mg O2/g-ww/h). The Round crucian carp were obtained from a fi sh farm in mean of the decrease in DO during an interval was consid- Takashima, Shiga Prefecture, Japan. They were the fi rst ered to approximate the DO at which oxygen consumption fi lial generation of wild round crucian carp from Lake Biwa. occurred. During the experiment, fi sh condition was moni- Largemouth bass were caught from a reservoir in Otsu, tored through a slit in the blind, and the experiment was Shiga Prefecture, Japan, by angling and cast netting. The continued until either the fi sh lost its equilibrium or no body weight (BW) range of the round crucian carp used was more DO decrease was detected during a measurement 0.025–5.115 g wet weight (ww) and the range of standard interval. With the experimental system used in the present length (SL) was 9.75–51.42 mm; included were postlarval to study, the each chamber was closed during the measurement young-of-the-year juvenile fi sh found in the macrophyte of oxygen consumption; therefore, the partial pressure of zone (ca. 50 mm; Miura, 1966).
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