clarias respiration

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

D A V I D. B E V A NNDD O N A L D. K R A M E R

Department of Biology, McGill Un iversity, 1205 Avenue Docteur Pen jeld , Montre'al, Que ., Canada H3A lB 1

Received July 1 1 , 1986

BE VA N, . J. , and D . L. KR AM ER . 987. 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 innormoxic water without surface access. Buoyancy decreased and water-breathing frequency increased when surface access wasdenied, but growth rate and the frequency of air-breathing attempts did not change. We examined air-breathing and water-breathing 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, and2.0 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 thislevel air breathing continued to increase , but water breathing dropp ed sharply. At higher levels of dissolved oxygen ( 8. 0 and 2. 0mg 02 .L- '), fish in deep water had lower air-breathing and higher water-breathing frequencies than fish in shallow water. V erticaldistance travelled and time spent in air breathing increased with increasing depth and w ith decreasing level of dissolved oxyge n.These results suppo rt the hypotheses that travel is a significan t cost of aerial respiration and that fish respond to increases in thiscost by decreasing their use of atmospheric oxygen when dissolved oxygen concentration permits them to do so.

BEVAN, . J . , et D . L . KRAM ER.987. 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. D es individus (7,6-20 ,9 g) peuvent survivre durantplus de 25 jours dan s de I'eau normoxiqu e, sans accks a la surface. L a flottabilitk des poissons diminue e t la frkquence de leursrespirations dans l'eau augmente a partir du moment oh l'accks a la surface leur est interdit, mais leur taux de croissance et lafrkquence de leurs tentatives de respiration akrien ne ne changent pa s. La frkquence des respirations akriennes et des respirationsaquatiques a kt6 ktudike en eau peu profonde (60 cm) e t en eau profonde (23 5 cm) dans des conditions normoxiques (8,O mg02.L-') et hypoxiques (0 ,3, 0, 7, 1,2 et 2,O mg 02 -L -' )afin de dkterminer de quelle f a ~ o nes changements des coQ ts espiratoiresau cours des dkplacements peuvent affecter chacun des modes de respiration. La frkquence des deux types de respirationaugmente 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.L p',la frkquence des respirations akriennes continue d'aug me nter, mais la frkquence des respirations aquatiques baisse considkrable-ment. Aux concentrations les plus Clevkes (8,O et 2,O mg o2.LP'), es poissons en eau profonde utilisent moins la respirationakrienne et plus la respiration aquatique que les poissons en eau peu profonde. La distance parcourue a la verticale et le tempsconsacrk aux respirations akriennes augmente lorsque la profondeur augmente et lorsque l'oxygkne dissous diminue. Lesrksultats corroborent l'hypothkse selon laquelle la respiration akrienne coQ te cher au cours de dkplacem ents et les poissonspallient a ce coat klevk en utilisant moins l'oxygkne atmosph krique lorsque la concentration d'oxygkne dissous le leur perm et.

[Traduit par la revue]

IntroductionTwo sources of oxygen are potentially available to fishes.

While most use only dissolved oxygen (water breathing oraquatic respiration), others (Lowe -McConn ell 1975) have theability to obtain oxygen from the atm osphere (air breathing oraerial respiration). All air-breathing fishes also use dissolvedoxygen to some extent (bimodal breath ing), but vary consider-ably in the proportional use of each respiratory mode (Johansen1970; Rahn and How ell 197 6; Singh 1976 ). Som e species havereduced gills and, even in normoxic water, must use someatmospheric oxygen to meet their total oxygen demands (obli-gate air breathers). Other bimodal species have a greater w ater-

breathing capacity, and air breathing is not required to meet theirtotal oxygen demand, even under moderately hypoxic condi-tions (facultative air breathers). Physiological studies of short-term changes in respiratory partitioning have revealed two broadclasses of controlling factors: those that iniluence total oxygendemand, e.g., temperature, activity, and ration, and those thatinfluence the efficiency of oxygen uptake, e.g., the partialpressure of dissolved oxygen and carbon dioxide (Johansen1970; Singh 1976; Kram er 1983 ).

Recent behavioural studies have suggested that other fac tors,not in themselves directly involved in the physiological aspectsof respiration, may also affect partitioning. One such factor isthe travel cost of air breathin g, w hich results from the add itional

time and energy spent on surfacing activity (Kramer and

McC lure 198 1 Kramer 1983 ). For a bimodal fish, the travel of air breathing can be reduced by an increase in water breing, suggesting that air-breathing frequency should decrewith increased depth, while water-breathing frequency shoincrease (Kramer 1983). Previous studies on the effects of deon air breathing found either increases, decreases, or compchanges which were not clearly attributable to a depth ef(Arunachalam et a1. 1976; Pandian and Vivekanandan 1VivekanandanandPandian1977;Vivekanandan1977a,19

Kramer and McClure 1980; Bevan and Kram er 1986 ). Ov ethese studies suggest that increased depth can reduce the breathing frequency of species with a well-developed wa

breathing capacity, although depth is only one of severalteracting factors. Ho wev er, the effect of depth on w ater breing has not been examined. This is important to determwhether changes in air breathing reflect chang es in the partiting of oxygen uptake.

As part of an ongoing examination of the effect of depththe respiratory behaviour and grow th of air-breathing fishespresent study examines (i) whether juvenile Clarias mrocephalus are facultative air breathers at normoxia and weffect surface access has on their respiratory behaviour growth, and (ii) the effects of dissolved oxygen and depththeir respiratory behaviour and swimm ing activity.

Clarias, a widely distributed genus of African and A

catfish, is characterized by the possession of an accessory



BEVAN AND KRAMER 34 9

on the second and fourth gill arches (Clay 1 977 ).Clarias

is a facultative air breather at normo xia (Jordan 1976)ion betwe en air-breathing frequen-

nd dissolved oxygen (Singh and Hug hes 1971; JordanC .

although both species are comm ercially rearedet al. 1982 ).

Materials and m ethods

Approximately 400 C . macrocephalus fry (4 days post-hatching)obtained from a wild stock originating in Perak, Malaysia ( E.S .P.

Artemianauplii, and later, sinking trout feed (GRT-83G: Martin Feed

s conducted under a photoperiod of 12 h light : 12 h dark0800-200 0 local time) and at 27OC (rang e 26-28°C ). All fish

d in the experiments were randomly drawn from the comm on stock

( 5 0 . 1 m g O ~ - L - ' ) ,with a Yellow Springs

rument model 57 oxygen meter. M eter accuracy was checked w ith

azide modified W inkler method (American P ublic Health Asso cia-

a are mean and standard erro r, unless indicated otherwise.

The survival value of surface access at normoxia was exam ined by

X 34 cm basal area) was divided intohambers (A and B ), with different depths (40 and 33 cm , respec-

2 x 4 6 x 44 cm), with surface access controlled by changing the

r depth. Fiber glass screening (1.7 m m mesh) s eparated chamber A

x 15 cm) were

culation of water (8.1 mg 02 -L -' , 154 Torr, 1 Torr = 133.322 Pa)ami in-I), and subgravel and

Twenty fish (7.6-2 0.9 g, 9.8-14.0 cm total length (TL) ) were

omly selected from a stock of ap proximately 9 0 similar-sized fish,fish were randomly assigned to eac h chamber. Fish were fed

daily at 3% of initial bod y we ight. F or the first 8 day s, fish in both

ishment of a dominance hierarchy. On day 9 , the water level was

sed to 35 cm , denying surface access to fish in chamber B . Th e fish

th was defined as a fish breaking the surface and , on m ost occur-

ed air breath was recorded whe neve r a fish in chambe r B left the

om and made contact with the cover. E xtended sw imming againste cover or repeated con tacts without returning to the bottom were not

imate water-breathing frequency. For each ob servation period the

and their subsequent behaviour was observed . W ilcoxon's signed-

piratory freq uencies and weight gain, respectively (Sokal and Rohlf

ect of depth and dissolved oxygen o n respiratory behaviourIndividual air-breathing and water-breathing frequencies w ere mea-

C . macrocephalus exposed to five levels of dissolved oxygen

and two depths. Tw o independent sets of apparatus were used. Each set

consisted of a main tank ( 30 x 3 0 x 240 cm ), with w ater recirculatedvia a 10-L header tank. D issolved oxygen was adjusted by bubblingnitrogen or air into the header tank. Three cylindrical cages (15 cmdiameter 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 (1 3 .5 x 10 X 7.5 cm), a l lowingdetailed observation of water breathing from behind a blind. A lengthof 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 minimaldisturbance.

Twelve fish (9.55-16.63 g, 10.6-13.1 cm TL) were randomlyselected from a stock of 100 similar-sized fish. Th ey were acclim ated

for 1 week in cages similar to the experimental ca ges, with dissolved

oxygen at 2 mg 02.L - ' (38 Torr) and a maximum depth of 30 cm. Tw o

trials, each lasting 7 days and using six fish, were performed. For eachtrial five levels of dissolved oxygen (0.3, 0.7 , 1.2, 2.0 , and 8 .0 mg

O~ .L - ' ; , 13, 23, 38, and 152 Torr) , and two depths (60 and 235 cm)were tested. The levels of dissolved oxygen were selected after pre-

liminary experiments revealed that respiratory frequen cies showed thegreatest change below 2 mg O ~ .L -' . Before each trial, fish were

weighed and measured, and then placed into the individual ex-perimental cages (23 5 cm depth) for a further 2 day s acclimation. Fishwere fed once daily (1800) at 3% of initial body weight. Th e sequence

of dissolved oxygen levels was randomly selected for each set ofapparatus, 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 eac h day . The first depthwas tested at 0900, and the secon d at 1 400; the order of depths wasdetermined s o that each depth was tested at both times of day for eachdissolved oxygen level. For each treatment combination of dissolvedoxygen and depth, tw o 30-min observations of air-breathing and water-

breathing frequencies were made. The average value from the twoobservations was used in the data analysis. In addition, amplitude of

water breathing was ranked from zero to three. Data collection wasmade using Rad io Shack model 100 portable computers as event

recorders, accessing the built-in real-time clock. The effects of dis-

solved oxygen and depth on respiratory frequency were analyzed by

Friedman's method for randomized blocks and by Wilcoxon's signed-ranks test, respectively (Sokal and Rohlf 198 1).

Clarias macrocephalus is predominantly benthic and sedentary in

habit (unpublished observations). Therefo re, the averag e vertical dis-tance travelled for air breathing was estimated by multiplying the

observed air-breathing freq uency by tw ice the treatment depth. In thesecond trial , observations of the ascent and descent t ime ( 5 0. 0 1 s),were made to estimate swimming velocity. The average swimming

velocity was used to calculate the time sp ent on surfacing activity.

Results

Effect of su ~ a c e ccess on survival and respiratory behaviour

Under normoxic conditions (8.1 mg 0 2 . ~ - ' )ll fish survivedthe 25-day experiment. R espiratory and growth data are summ a-

rized in Table 1. There was no significant difference between theair-breathing frequency of fish with surface access and theattempted air-breathing frequency of fish without surface access(T , = 102.5,P > 0.05 , Wilcoxon's signed-ranks test). Water-breathing frequency was significantly higher for fish withoutsurface access than for fish with access (Ts = 0 , P < 0 .05 ,Wilcoxon's signed-ranks test). There w as no significant differ-ence in the initial mean w eight (Us = 61, P > 0.2 , W ilcoxontwo-sample test) or final mean weight (Us = 5 7 , P > 0.2)between groups, and the average SGR was 1.25% weightldayfor both. After 1-2 days, we noted indications of a lack ofbuoyancy 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



350 CAN. J . ZOOL. VOL. 65, 1987

TABLE. Effect of surface access on survival, specific growth rate, andrespiratory behavio ur of juvenile C. macrocephalus in the first experi-

ment

Surface No surfaceaccess access

No. of fish 10 10Survival rate 100% 100%Initial weight (g) 11 .66 k0 .94 (lo )* 12.21k l . lO(10)Final weight (g) 17 .64 k 1.73 (10) 18. 46k 1.75 (10)Specific growth rate

(% weightld) 1.25 1.25Air-breathing frequency

(breathsth) 4.7 1k0 . 62 (20) 4 .5 1k 0 .6 4 ( 2 0 ) tWater-breathing frequency

(breathstmin) 35.00 24.82 (6) 64.3 3k4.1 6 (6)

*Data given as mean 2 SE ( n ) .

?Attempted air breathing; see text for details.

of surface access, the a nterior region remained on the substratewhen the fish were at rest, and swimm ing appeared laboured andawkw ard. Immediately after the reestablishment of surface ac-

cess, individuals made vigorous attempts to obtain air. Sur-facing frequency was high (16.8 breathslh), and strong swim-ming actions often raised the entire head out of the water as largeamounts of air were released from the opercula and mouth.Normal buoyancy was regained several hours later.

Effect of depth and dissolv ed oxygen on respiratory behaviourIncreased depth resulted in significantly lower frequencies of

air breathing and higher frequencies of water breathing at 8.0and 2.0 mg 02 .L- ' (Fig. 1) . At lower levels of dissolved oxygenthe effect of depth was more complex. At 0.7 and 1.2 mg 02 -L -'both air-breathing and water-breathing frequencies tended to belower in deeper water, although the effect was statistically

significant only for air breathing at 0.7 mg 02.Lp1.At 0.3 mgO2.L-', air-breathing frequency wa s higher and water-breathingfrequency was lower in deeper water, but here the trend wassignificant only for water breathing.

The effect of dissolved oxygen on air-breathing frequencywas significant at both depths (6 0 cm , X2 = 25.1, P < 0.0001;235 cm, X2 = 42.1, P < 0.0001, Friedman's method forrandomized blocks). At 60 cm, air-breathing frequency aver-aged 3.6 breathslh at normoxia and increased to a max imum of11.8 breathslh at 0. 7 mg o,.L-'. At 235 cm , the frequencyincreased from 1 2 breathslh- ' at normoxia to a maximum of 9. 5breathslh at 0. 3 mg O,-L-' (Fig. 1A). W ater-breathing frequen-cy increased with a reduction in dissolved oxygen, reaching amaximum at 2.0 mg 02 .L -' at both depths. A further reductionin dissolved oxygen resulted in a rapid decline in water-breathing frequency (Fig. 1B) .

The amplitude and frequency of opercular movements werepositively correlated (Ken dall correlation coefficient r = 0.78,P = 0.0001). Furthermore, both tended to increase as an airbreath became m ore im mine nt, especially below 1 2 mg0,-L- ' .

The vertical distance travelled for air breathing was nega tive-ly correlated with dissolved oxygen level (Kenda ll correlationcoefficient r = - .39, P < 0.0001) and positively correlatedwith depth ( r = 0.48, P = 0.0001), and ranged from 4.36 to44.65 m-h-' (Table 2). The descent velocity (3.7 TLIs) wassignificantly greater than ascent ( 2. 0 TLIs, P < 0.04 , sign test).

D I S S O L V E D O X Y G E N (mg O , / L )

FIG . 1. The effect of dissolved oxygen and water depth on

air-breathing frequency and (B ) water-breathing frequency of juve

C.macrocephalus. The data are mean k SE . Significant differencerespiratory frequencies between dep ths are shown as *, P < 0.05; **< 0.01 (Wilcoxon's signed-ranks test).

Using the average swimming ve locity of 2. 9 TLIs, the tempocost of this surfacing activity ranged from 0 .2 1 min-h -' (0.3of total time), to 2.22 m in-h-' (3. 7% , Table 2).

Discussion

Respiratory mode of Clarias macrocephalusClarias macrocephalus possesses accessory respirat

structures similar to those described for Clarias batrach(Munshi 19 61). That these are actually used for air breathing

indicated by the frequent surfacing accompanied by the releof bubbles from the opercula and by the inverse relationsbetween opercular and surfacing freq uenc ies. Kulakkattolic(1986) has shown that this species can survive in hypo xic waonly when permitted to surface. Since C . macrocephalus sface in normoxic water, even though they can survive withsurfacing, the species can be c lassified as a con tinuous, facutive air breather (Gee 1980; Kramer 1983 ). Similar conclusihave been drawn for C . batrachus (Jordan 1976) and Clarlazera (Abdel-Magid 197 1 Abdel-Magid and Babiker 1 97Other studies of Clarias spp. report them to be obligatebreathers at normoxia (Moussa 1957; Singh and Hughe s 19Johnston et al. 1983 ). These differences m ay be due to variat



BEVAN AND KRAMER

TABLE. Estimate of the average vertical distance travelled and surfacing time of C.macrocephalus, as a result of air breathing , in the second experiment

60 cm depth 235 cm depth

Dissolved Distance Surfacing Distance Surfacingoxygen travelled time travelled time

(m g o ~ . L - ' ) (mwh-I) (m in. h-' ) (me h-') (min.h-')

NOT E: stimates are based on air-breathing frequencies of individual fish and an average swimmin g speed

of 2 .9 TL /s. Data are presented as mean + SE ; n = 12, unless indicated otherwise.

*n = 11; one fish omitted because of excep tionally high surfacing frequency in both sessions (1 82 and 1 10

surfacings/h); many of these surfacings were not air breaths and were from less than the maximum depth.

perimental stress. There is evidence forC .

(Abdel-Magid 197 1 Abdel-Magid and Bibiker 1975 ),

C . batrachus (Jordan 1976).stress elevates oxygen con sumption (W edeme yer

Schreck 198 1 Pickering et al. 19 82 ), and may be a factories reporting Clarias to be an obligate air breather. The

C . macrocephalus can obtain sufficientby aquatic respiration to meet their me tabolic demand s.

The identical SGR of fish with or without surface access

d bimodal respiration is small at normo xia. T his may exp lainof v ariation for air-breathing frequen cy at

n the secon d experiment (1 10% and 161% at 60 and5 cm, respectively, as compa red with a range of 19-47%

er hypoxic condition s).Gee and Graham (197 8) suggested that air breathing by cal-

, and our observations indicate a sim ilar role in Clar-Fish prevented from surfacing showed a dramatic loss of

e of this loss probably o ccurred because oxy gen

l fish (Johansen 197 0). Ho we ver, the fish may have alsost buoyancy from the release of b ubbles du ring initial attempts

en surface access w as reestablished.

ct of dissolved oxygen on respira tory behaviourClarias macrocephalus responds to changes in d issolved ox-

organ s. Similar increases in air-breathing frequen-ncreases in w ater-breathing frequency and am pli-

Clarias spp. (Singh and Hughes 1971;

es 19 75; Jordan 1976; Johnston et al. 19 83 ), as well as inr air-breathing fishes (reviews by Joh ansen 1970 and Singh

Studies that have quantified the chang es of respiratoryClarias in relation to changes in dissolved ox-

ygen (Singh and H ughes 197 1; Jordan 1976; Johnston et al.1983) indicate that the ability to regulate oxygen uptake breaksdown at about 2 mg O2.L-' (38 To n ), and total oxygen con-

sumption decreases. In our study, the changes in air-breathingfrequency under extreme hypoxia (Fig. 1A) and the decline inwater-breathing frequency below 2 mg O2.L-' (Fig. 1B) prob-ably reflect a similar reduction in the total oxyg en con sumption.

Effect of water depth o n respirator y behaviourOur study shows that water depth has im portant effects on the

respiratory behaviour of C . macrocephalus. At 8.0 and 2.0 mgO2 -L-l the fish responded to increased d epth by reduc ing theirair-breathing frequency. Similar responses are know n for otherspecies of fish and tadpoles (Arunach alam e t al. 1976; Feder andMoran 1985; Bevan and Kramer 1986). However, ours is thefirst demonstration that water-breathing frequency increases

with depth. When taken together with the positive correlationbetween water-breathing frequency and amplitude, this pro-vides strong, indirect evidence for a depth-induced increase inthe proportional uptake of dissolved oxygen. However, themagn itude of the change in respiratory partitioning is unknow nbecause oxygen uptake is not a simple, linear function of ven-tilation frequency and amplitude. At lower levels of dissolvedoxygen, the fish did not exhibit a simple, inverse relationshipbetween water-breathing and air-breathing frequencies, prob-ably because they responded to the increased cost of breathingby reducing their total oxygen d em and .

The travel cos t of air brea thingFor a benthic and normally sedentary fish such as Clarias,

surfacing represents a large proportion of total activity. T he timeand energy devoted to surfacing depend primarily upon waterdepth, air-breathing frequency, and swimming velocity. For C .macrocephalus at 0 .3 mg 0 2. L- ', the temporal cost of thissurfacing activity increased by nearly 350% as depth increasedfrom 60 to 235 cm , while at normox ia this increase was less than40% because of the reduction in air-breathing frequency. Thefish never spent more than 4% of their total time budget onbreathing during our study. These estimates, however, areminimal values since Clarias generally increase their activity atnight (personal observations; Jordan 1976). Nevertheless C .macrocephalus appears to spend less time breathing than otherspecies do, for example Channa striatus at 40 cm (22%: Viveka-



BEVAN AND KRAMER 353

Edited by G . M . Hughes.

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clarias respiration

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