The respiratory behaviour of an air-breathing catfish, Clarias macrocephalus (Clariidae)

DAVID BEVAN DONALD KRAMER J. AND L.

Department of Biology, McGill University, 1205 Avenue Docteur Penjeld, Montre'al, Que., Canada H3A lB1 Received July 1 1 , 1986 BEVAN, J., and D. L. KRAMER. D. 1987. The respiratory behaviour of an air-breathing catfish, Clarias macrocephalus (Clariidae). Can. J. Zool . 65: 348-353. Clarias macrocephalus are continuous, facultative air breathers. Individuals (7.6-20.9 g) survived more than 25 days in normoxic water without surface access. Buoyancy decreased and water-breathing frequency increased when surface access was denied, but growth rate and the frequency of air-breathing attempts did not change. We examined air-breathing and waterbreathing frequency in shallow (60 cm) and deep (235 cm) water under normoxic (8.0 mg O,-L-') and hypoxic (0.3,0.7, 1.2, and 2.0 mg 02.L-') conditions to examine how changes in the travel costs of breathing affected the use of each respiratory mode. Air-breathing and water-breathing frequency increased as dissolved oxygen decreased from 8.0 to 2.0 mg o,-L-'. Below this level air breathing continued to increase, but water breathing dropped sharply. At higher levels of dissolved oxygen (8.0 and 2.0 mg 02.L-'), fish in deep water had lower air-breathing and higher water-breathing frequencies than fish in shallow water. Vertical distance travelled and time spent in air breathing increased with increasing depth and with decreasing level of dissolved oxygen. These results support the hypotheses that travel is a significant cost of aerial respiration and that fish respond to increases in this cost by decreasing their use of atmospheric oxygen when dissolved oxygen concentration permits them to do so. BEVAN, J., et D. L. KRAMER. D. 1987. The respiratory behaviour of an air-breathing catfish, Clarias macrocephalus (Clariidae). Can. J. Zool. 65 : 348-353. Clarias macrocephalus a une respiration akrienne facultative continue. Des individus (7,6-20,9 g) peuvent survivre durant plus de 25 jours dans de I'eau normoxique, sans accks a la surface. La flottabilitk des poissons diminue et la frkquence de leurs respirations dans l'eau augmente a partir du moment oh l'accks a la surface leur est interdit, mais leur taux de croissance et la frkquence de leurs tentatives de respiration akrienne ne changent pas. La frkquence des respirations akriennes et des respirations aquatiques a kt6 ktudike en eau peu profonde (60 cm) et en eau profonde (235 cm) dans des conditions normoxiques (8,O mg 02.L-') et hypoxiques (0,3,0,7, 1,2 et 2,O mg 02-L-')afin de dkterminer de quelle f a ~ o n changements des coQtsrespiratoires les au cours des dkplacements peuvent affecter chacun des modes de respiration. La frkquence des deux types de respiration augmente au cours d'une diminution de l'oxygkne dissous de 8,O a 2,O mg 02.L-'. Aux concentrations infkrieures a 2,O rng.Lp', la frkquence des respirations akriennes continue d'augmenter, mais la frkquence des respirations aquatiques baisse considkrablement. Aux concentrations les plus Clevkes (8,O et 2,O mg o2.LP'), les poissons en eau profonde utilisent moins la respiration akrienne et plus la respiration aquatique que les poissons en eau peu profonde. La distance parcourue a la verticale et le temps consacrk aux respirations akriennes augmente lorsque la profondeur augmente et lorsque l'oxygkne dissous diminue. Les rksultats corroborent l'hypothkse selon laquelle la respiration akrienne coQte cher au cours de dkplacements et les poissons pallient a ce coat klevk en utilisant moins l'oxygkne atmosphkrique lorsque la concentration d'oxygkne dissous le leur permet. [Traduit par la revue]

Introduction Two sources of oxygen are potentially available to fishes. While most use only dissolved oxygen (water breathing or aquatic respiration), others (Lowe-McConnell 1975) have the ability to obtain oxygen from the atmosphere (air breathing or aerial respiration). All air-breathing fishes also use dissolved oxygen to some extent (bimodal breathing), but vary considerably in the proportional use of each respiratory mode (Johansen 1970; Rahn and Howell 1976; Singh 1976). Some species have reduced gills and, even in normoxic water, must use some atmospheric oxygen to meet their total oxygen demands (obligate air breathers). Other bimodal species have a greater waterbreathing capacity, and air breathing is not required to meet their total oxygen demand, even under moderately hypoxic conditions (facultative air breathers). Physiological studies of shortterm changes in respiratory partitioning have revealed two broad classes of controlling factors: those that iniluence total oxygen demand, e.g., temperature, activity, and ration, and those that influence the efficiency of oxygen uptake, e.g., the partial pressure of dissolved oxygen and carbon dioxide (Johansen 1970; Singh 1976; Kramer 1983). Recent behavioural studies have suggested that other factors, not in themselves directly involved in the physiological aspects of respiration, may also affect partitioning. One such factor is the travel cost of air breathing, which results from the additional time and energy spent on surfacing activity (Kramer and

McClure 1981;Kramer 1983). For a bimodal fish, the travel cost of air breathing can be reduced by an increase in water breathing, suggesting that air-breathing frequency should decrease with increased depth, while water-breathing frequency should increase (Kramer 1983). Previous studies on the effects of depth on air breathing found either increases, decreases, or complex changes which were not clearly attributable to a depth effect (Arunachalam et a1. 1976; Pandian and Vivekanandan 1976; VivekanandanandPandian1977;Vivekanandan1977a,1977b; Kramer and McClure 1980; Bevan and Kramer 1986). Overall, these studies suggest that increased depth can reduce the airbreathing frequency of species with a well-developed waterbreathing capacity, although depth is only one of several interacting factors. However, the effect of depth on water breathing has not been examined. This is important to determine whether changes in air breathing reflect changes in the partitioning of oxygen uptake. As part of an ongoing examination of the effect of depth on the respiratory behaviour and growth of air-breathing fishes, the present study examines (i) whether juvenile Clarias macrocephalus are facultative air breathers at normoxia and what effect surface access has on their respiratory behaviour and growth, and (ii) the effects of dissolved oxygen and depth on their respiratory behaviour and swimming activity. Clarias, a widely distributed genus of African and Asian catfish, is characterized by the possession of an accessory air-

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breathing organ consisting of two pairs of branched dendritic organs on the second and fourth gill arches (Clay 1977). Clarias batrachus is a facultative air breather at normoxia (Jordan 1976) and shows a negative correlation between air-breathing frequency and dissolved oxygen (Singh and Hughes 1971; Jordan 1976). However, there is considerably less known about C . macrocephalus, although both species are commercially reared in Asia (Panayotou et al. 1982).

Materials and methods

General Approximately 400 C . macrocephalus fry (4 days post-hatching) were obtained from a wild stock originating in Perak, Malaysia (E.S.P. Tan, personal communication). They were initially fed live Artemia salina nauplii, and later, sinking trout feed (GRT-83G: Martin Feed Mills Ltd., Elmira, Ont., Canada). Fish were maintained and all experiments conducted under a photoperiod of 12 h light : 12 h dark (light 0800-2000 local time) and at 27OC (range 26-28C). All fish used in the experiments were randomly drawn from the common stock and were not reused in subsequent experiments. Dissolved oxygen levels were monitored ( 5 0 . 1 mg O ~ - L - ' ) ,with a Yellow Springs Instrument model 57 oxygen meter. Meter accuracy was checked with the azide modified Winkler method (American Public Health Association 1965). Statistical significance was set at the 5% probability level. The data are mean and standard error, unless indicated otherwise. Effect of surface access on survival and respiratory behaviour The survival value of surface access at normoxia was examined by comparing two groups of fish with and without surface access. A Plexiglas experimental tank (79 X 34 cm basal area) was divided into two chambers (A and B), with different depths (40 and 33 cm, respectively). The experimental tank was placed within a larger aquarium (92 x 46 x 44 cm), with surface access controlled by changing the water depth. Fiber glass screening (1.7 mm mesh) separated chamber A from B, and chamber B from the external aquarium. Within each chamber four black plastic tubes (2.5 cm diameter x 15 cm) were provided as shelters, in which fish were usually located. Uniform circulation of water (8.1 mg 02-L-', 154 Torr, 1 Torr = 133.322 Pa) was maintained using a power filter (780 ami in-I), and subgravel and comer filters in the external aquarium. Twenty fish (7.6-20.9 g, 9.8-14.0 cm total length (TL)) were randomly selected from a stock of approximately 90 similar-sized fish, and 10 fish were randomly assigned to each chamber. Fish were fed once daily at 3% of initial body weight. For the first 8 days, fish in both chambers were allowed surface access, permitting acclimation and establishment of a dominance hierarchy. On day 9 , the water level was raised to 35 cm, denying surface access to fish in chamber B. The fish were maintained in the chambers for a further 25 days. Over this period, 20 observations of 30 minutes each were made to determine air-breathing frequency or attempted air-breathing frequency. An air breath was defined as a fish breaking the surface and, on most occurrences, involved the release of bubbles from the opercula. An attempted air breath was recorded whenever a fish in chamber B left the bottom and made contact with the cover. Extended swimming against the cover or repeated contacts without returning to the bottom were not counted as additional attempts. Six observation periods were used to estimate water-breathing frequency. For each observation period the number of opercular beats in 30 s, for five different fish in each chamber, was determined; the mean values were used as group estimates. Surface access was reestablished for fish in group B after 25 days and their subsequent behaviour was observed. Wilcoxon's signedranks test and the Wilcoxon two-sample test were used to compare respiratory frequencies and weight gain, respectively (Sokal and Rohlf 1981). Specific growth rate (SGR) was calculated following Ricker (1979). Effect of depth and dissolved oxygen on respiratory behaviour Individual air-breathing and water-breathing frequencies were measured for C. macrocephalus exposed to five levels of dissolved oxygen

and two depths. Two independent sets of apparatus were used. Each set consisted of a main tank (30 x 30 x 240 cm), with water recirculated via a 10-L header tank. Dissolved oxygen was adjusted by bubbling nitrogen or air into the header tank. Three cylindrical cages (15 cm diameter x 260 cm), constructed of fiber glass screening (1.7-mm mesh) were suspended in each main tank. The bottom of each cage consisted of a transparent plastic box (13.5 x 10 X 7.5 cm), allowing detailed observation of water breathing from behind a blind. A length of black plastic tube (2.5 cm diameter X 8 cm) provided a shelter in which fish were usually located. By slowly raising or lowering the cages the maximum depth of the fish could be altered with minimal disturbance. Twelve fish (9.55-16.63 g, 10.6-13.1 cm TL) were randomly selected from a stock of 100 similar-sized fish. They were acclimated for 1 week in cages similar to the experimental cages, with dissolved oxygen at 2 mg 02.L-' (38 Torr) and a maximum depth of 30 cm. Two trials, each lasting 7 days and using six fish, were performed. For each trial five levels of dissolved oxygen (0.3, 0.7, 1.2, 2.0, and 8.0 mg O~.L-';6, 13, 23, 38, and 152 Torr), and two depths (60 and 235 cm) were tested. The levels of dissolved oxygen were selected after preliminary experiments revealed that respiratory frequencies showed the greatest change below 2 mg O~.L-'. Before each trial, fish were weighed and measured, and then placed into the individual experimental cages (235 cm depth) for a further 2 days acclimation. Fish were fed once daily (1800) at 3% of initial body weight. The sequence of dissolved oxygen levels was randomly selected for each set of apparatus, except that 8.0 mg O~-L-'was always last to allow better control of dissolved oxygen between days. One level of dissolved oxygen and both depth treatments were tested each day. The first depth was tested at 0900, and the second at 1400; the order of depths was determined so that each depth was tested at both times of day for each dissolved oxygen level. For each treatment combination of dissolved oxygen and depth, two 30-min observations of air-breathing and waterbreathing frequencies were made. The average value from the two observations was used in the data analysis. In addition, amplitude of water breathing was ranked from zero to three. Data collection was made using Radio Shack model 100 portable computers as event recorders, accessing the built-in real-time clock. The effects of dissolved oxygen and depth on respiratory frequency were analyzed by Friedman's method for randomized blocks and by Wilcoxon's signedranks test, respectively (Sokal and Rohlf 198 1). Clarias macrocephalus is predominantly benthic and sedentary in habit (unpublished observations). Therefore, the average vertical distance travelled for air breathing was estimated by multiplying the observed air-breathing frequency by twice the treatment depth. In the second trial, observations of the ascent and descent time ( 5 0 . 0 1 s), were made to estimate swimming velocity. The average swimming velocity was used to calculate the time spent on surfacing activity.

Results Effect of s u ~ a c e access on survival and respiratory behaviour Under normoxic conditions (8.1 mg 0 2 . ~ - ' ) survived all fish the 25-day experiment. Respiratory and growth data are summarized in Table 1. There was no significant difference between the air-breathing frequency of fish with surface access and the attempted air-breathing frequency of fish without surface access (T, = 102.5, P > 0.05, Wilcoxon's signed-ranks test). Waterbreathing frequency was significantly higher for fish without surface access than for fish with access (Ts = 0, P < 0.05, Wilcoxon's signed-ranks test). There was no significant difference in the initial mean weight (Us = 61, P > 0.2, Wilcoxon two-sample test) or final mean weight (Us = 57, P > 0.2) between groups, and the average SGR was 1.25% weightlday for both. After 1-2 days, we noted indications of a lack of buoyancy in the fish without surface access. Normally, C . macrocephalus rest with the anterior region of the body raised off the substrate of an angle of approximately 10". After denial

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TABLE Effect of surface access on survival, specific growth rate, and 1. respiratory behaviour of juvenile C. macrocephalus in the first experiment
Surface access No. of fish Survival rate Initial weight (g) Final weight (g) Specific growth rate (% weightld) Air-breathing frequency (breathsth) Water-breathing frequency (breathstmin) 10 100% 11.66k0.94 (lo)* 17.64k 1.73 (10) 1.25 4.7 1k0.62 (20) 35.0024.82 (6) No surface access 10 100% 12.21k l.lO(10) 18.46k 1.75 (10) 1.25 4.5 1k0.64 (20)t 64.33k4.16 (6)

*Data given as mean 2 SE ( n ) . ?Attempted air breathing; see text for details.

of surface access, the anterior region remained on the substrate when the fish were at rest, and swimming appeared laboured and awkward. Immediately after the reestablishment of surface access, individuals made vigorous attempts to obtain air. Surfacing frequency was high (16.8 breathslh), and strong swimming actions often raised the entire head out of the water as large amounts of air were released from the opercula and mouth. Normal buoyancy was regained several hours later.
Effect of depth and dissolved oxygen on respiratory behaviour Increased depth resulted in significantly lower frequencies of air breathing and higher frequencies of water breathing at 8.0 and 2.0 mg 02.L-' (Fig. 1). At lower levels of dissolved oxygen the effect of depth was more complex. At 0.7 and 1.2 mg 02-L-' both air-breathing and water-breathing frequencies tended to be lower in deeper water, although the effect was statistically significant only for air breathing at 0.7 mg 02.Lp1.At 0.3 mg O2.L-', air-breathing frequency was higher and water-breathing frequency was lower in deeper water, but here the trend was significant only for water breathing. The effect of dissolved oxygen on air-breathing frequency was significant at both depths (60 cm, X2 = 25.1, P < 0.0001; 235 cm, X2 = 42.1, P < 0.0001, Friedman's method for randomized blocks). At 60 cm, air-breathing frequency averaged 3.6 breathslh at normoxia and increased to a maximum of 11.8 breathslh at 0.7 mg o,.L-'. At 235 cm, the frequency increased from 1.2 breathslh- at normoxia to a maximum of 9.5 breathslh at 0.3 mg O,-L-' (Fig. 1A). Water-breathing frequency increased with a reduction in dissolved oxygen, reaching a maximum at 2.0 mg 02.L-' at both depths. A further reduction in dissolved oxygen resulted in a rapid decline in waterbreathing frequency (Fig. 1B) . The amplitude and frequency of opercular movements were positively correlated (Kendall correlation coefficient r = 0.78, P = 0.0001). Furthermore, both tended to increase as an air breath became more imminent, especially below 1.2 mg 0,-L-'. The vertical distance travelled for air breathing was negatively correlated with dissolved oxygen level (Kendall correlation coefficient r = - 0.39, P < 0.0001) and positively correlated with depth ( r = 0.48, P = 0.0001), and ranged from 4.36 to 44.65 m-h-' (Table 2). The descent velocity (3.7 TLIs) was significantly greater than ascent (2.0 TLIs, P < 0.04, sign test).

DISSOLVED

OXYGEN

(mg O,/L)

FIG. 1. The effect of dissolved oxygen and water depth on (A) air-breathing frequency and (B) water-breathing frequency of juvenile C. macrocephalus. The data are mean k SE. Significant differences in respiratory frequencies between depths are shown as *, P < 0.05; **, P < 0.01 (Wilcoxon's signed-ranks test).

Using the average swimming velocity of 2.9 TLIs, the temporal cost of this surfacing activity ranged from 0.2 1 min-h-' (0.35% of total time), to 2.22 min-h-' (3.7%, Table 2).

'

Discussion Respiratory mode of Clarias macrocephalus Clarias macrocephalus possesses accessory respiratory structures similar to those described for Clarias batrachus (Munshi 1961). That these are actually used for air breathing is indicated by the frequent surfacing accompanied by the release of bubbles from the opercula and by the inverse relationship between opercular and surfacing frequencies. Kulakkattolickal (1986) has shown that this species can survive in hypoxic water only when permitted to surface. Since C . macrocephalus surface in normoxic water, even though they can survive without surfacing, the species can be classified as a continuous, facultative air breather (Gee 1980; Kramer 1983). Similar conclusions have been drawn for C . batrachus (Jordan 1976) and Clarias lazera (Abdel-Magid 1971; Abdel-Magid and Babiker 1975). Other studies of Clarias spp. report them to be obligate air breathers at normoxia (Moussa 1957; Singh and Hughes 1971; Johnston et al. 1983). These differences may be due to variation

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TABLE Estimate of the average vertical distance travelled and surfacing time of C. 2. macrocephalus, as a result of air breathing, in the second experiment
60 cm depth Dissolved oxygen (mg o~.L-') Distance travelled (mwh-I) Surfacing time (min. h-' ) 235 cm depth Distance travelled (me h-') Surfacing time (min.h-')

NOTE: Estimates are based on air-breathing frequencies of individual fish and an average swimming speed of 2.9 TL/s. Data are presented as mean + SE; n = 12, unless indicated otherwise. *n = 11; one fish omitted because of exceptionally high surfacing frequency in both sessions (182 and 1 10 surfacings/h); many of these surfacings were not air breaths and were from less than the maximum depth.

in species, size, and experimental stress. There is evidence for size dependence in the requirement for surface access in C . lazera (Abdel-Magid 197 1; Abdel-Magid and Bibiker 1975), although this was not found in C . batrachus (Jordan 1976). Experimental stress elevates oxygen consumption (Wedemeyer 1976; Schreck 198 1; Pickering et al. 1982), and may be a factor in studies reporting Clarias to be an obligate air breather. The present study endeavoured to reduce such stress and clearly showed that juvenile C . macrocephalus can obtain sufficient oxygen by aquatic respiration to meet their metabolic demands. The identical SGR of fish with or without surface access suggests that the difference in energetic cost between aquatic and bimodal respiration is small at normoxia. This may explain the large coefficient of variation for air-breathing frequency at normoxia in the second experiment (1 10% and 161% at 60 and 235 cm, respectively, as compared with a range of 19-47% under hypoxic conditions). Gee and Graham (1978) suggested that air breathing by callichthyid catfishes at normoxia may function to maintain buoyancy, and our observations indicate a similar role in Clarias. Fish prevented from surfacing showed a dramatic loss of buoyancy. Some of this loss probably occurred because oxygen absorbed from the air-breathing organ was not replaced by carbon dioxide, which is excreted primarily via the gills in bimodal fish (Johansen 1970). However, the fish may have also lost buoyancy from the release of bubbles during initial attempts to breathe air after removal of surface access. The loss of gas may have caused the air-breathing organs to become flooded, necessitating vigorous and repeated surfacing to clear them when surface access was reestablished.
Effect of dissolved oxygen on respiratory behaviour Clarias macrocephalus responds to changes in dissolved oxygen by altering the ventilatory frequency of both gills and air-breathingorgans. Similar increases in air-breathing frequency and initial increases in water-breathing frequency and amplitude followed by decreases with declining dissolved oxygen were found in other Clarias spp. (Singh and Hughes 1971; Abdel-Magid and Babiker 1975; Bronchart-Lannoye and Thines 1975; Jordan 1976; Johnston et al. 1983), as well as in other air-breathing fishes (reviews by Johansen 1970 and Singh 1976). Studies that have quantified the changes of respiratory partitioning of Clarias in relation to changes in dissolved ox-

ygen (Singh and Hughes 197 1; Jordan 1976; Johnston et al. 1983) indicate that the ability to regulate oxygen uptake breaks down at about 2 mg O2.L-' (38 Ton), and total oxygen consumption decreases. In our study, the changes in air-breathing frequency under extreme hypoxia (Fig. 1A) and the decline in water-breathing frequency below 2 mg O2.L-' (Fig. 1B) probably reflect a similar reduction in the total oxygen consumption.
Effect of water depth on respiratory behaviour Our study shows that water depth has important effects on the respiratory behaviour of C . macrocephalus. At 8.0 and 2.0 mg O2-L-l the fish responded to increased depth by reducing their air-breathing frequency. Similar responses are known for other species of fish and tadpoles (Arunachalam et al. 1976; Feder and Moran 1985; Bevan and Kramer 1986). However, ours is the first demonstration that water-breathing frequency increases with depth. When taken together with the positive correlation between water-breathing frequency and amplitude, this provides strong, indirect evidence for a depth-induced increase in the proportional uptake of dissolved oxygen. However, the magnitude of the change in respiratory partitioning is unknown because oxygen uptake is not a simple, linear function of ventilation frequency and amplitude. At lower levels of dissolved oxygen, the fish did not exhibit a simple, inverse relationship between water-breathing and air-breathing frequencies, probably because they responded to the increased cost of breathing by reducing their total oxygen demand. The travel cost of air breathing For a benthic and normally sedentary fish such as Clarias, surfacing represents a large proportion of total activity. The time and energy devoted to surfacing depend primarily upon water depth, air-breathing frequency, and swimming velocity. For C . macrocephalus at 0.3 mg 02.L-', the temporal cost of this surfacing activity increased by nearly 350% as depth increased from 60 to 235 cm, while at normoxia this increase was less than 40% because of the reduction in air-breathing frequency. The fish never spent more than 4% of their total time budget on breathing during our study. These estimates, however, are minimal values since Clarias generally increase their activity at night (personal observations; Jordan 1976). Nevertheless C . macrocephalus appears to spend less time breathing than other species do, for example Channa striatus at 40 cm (22%: Viveka-

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nandan and Pandian 1977) and Corydoras aeneus at 120 c m (1 1%: Kramer and McClure 1981). In terms of distance travelled, the cost of breathing for Clarias in our experiment varied from less than 5 m-h-' to nearly 45 m-h-'. This converts to a range of about 900-9000 TL/d. Although significant, the energy cost of this travel does not produce a strong growth reduction at greater depths (Bevan 1986). In conclusion, there is now sufficient evidence from studies of ventilation frequencies to warrant more detailed physiological investigations of the effect of water depth on respiratory partitioning. The present study, by showing how depth and dissolved oxygen interact in the control of ventilation patterns, suggests an explanation for the variation among previous studies of airbreathing frequency and water depth. Species with a welldeveloped capacity for dissolved oxygen uptake can respond to increased depth by substituting dissolved for atmospheric oxygen, provided that the partial pressure of dissolved oxygen is adequate. When the capacity for dissolved oxygen uptake is limited, either by its availability in the environment or the organism's capacity to extract it, fish may respond to increased depth by either increasing air-breathing frequency to meet the increased cost of surfacing, or by reducing total oxygen demand. The importance of water depth for fish ecology (Power 1984, 1986) and the socioeconomic significance of airbreathing fish in Africa and Asia suggest that further examination of these patterns would be worthwhile.

Acknowledgements
This study was carried out by D.J.B. in partial fulfillment of the requirements for an M .Sc . degree at McGill University. We thank E.S.P. Tan, Universiti Sains Malaysia, for the Clarias fry, G . Gagnon for technical assistance, and W . C . Leggett for laboratory space. J. Gee, W. C. Leggett, and D. Roff provided useful comments on earlier versions of the manuscript. The study was supported by an operating grant to D.L.K. from the Natural Sciences and Engineering Research Council of Canada. Computer time was provided by the McGill University Computing Centre. ABDEL-MAGID, M. 1971. The ability of Clarias lazera (Pisces) to A. survive without air breathing. J. Zool. 163: 63-72. ABDEL-MAGID,M., and M. M. BAB~KER. Oxygen consumpA. 1975. tion and respiratory behaviour of three Nile fishes. Hydrobiologia, 46: 359-367. AMERICAN PUBLIC HEALTH ASSOCIATION. Standard methods for 1965. the examination of water and wastewater. American Public Health Association, New York. ARUNACHALAM, VIVEKANANDAN, J. PANDIAN. S., E. and T. 1976. Food intake, conversion and swimming activity in the air-breathing catfish Heteropneustes fossilis. Hydrobiologia, 51: 2 13-2 17. BEVAN, J. 1986. The effect of dissolved oxygen and water depth on D. the respiratory behaviour and growth of Clarias macrocephalus (Pisces, Clariidae). M.Sc. thesis, McGill University, MontrCal, Que. BEVAN, J . ,and D. L. KRAMER. D. 1986. The effect of swimming depth on respiratory behaviour of the honey gourami, Colisa chuna (Pisces, Belontiidae). Can. J. Zool. 64: 1893- 1896. S. BRONCHART-LANNOYE, G. T H I N ~ 1975. Influence de quelM., and ques facteurs physiques sur le comportement des poissons a double systkme de respiration. Bull. C1. Sci. Acad. R. Belg. 5" Ser. 61: 525-542. CLAY, 1977. Biology of the tropical catfish (family: Clariidae) with D. special emphasis on its suitability for culture (including a bibliogra-

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