iii. respiration in fishes everal useful reviews on the respiration of fishes years s . ti f

III. RESPIRATION IN FISHES

BYEDGAR C. BLACK

t of Biology and Botany, University of British Columbia

INTRODUCI'ION

everal useful reviews on the respiration of fishesYears s . ti f .'ed, some as separate reviews or as see ons 0 revIe~s

tive physiology (3, 33, 43, 49, 52, 63), others as dis-(28) or as monographs (60, 61) or as reference texts

res~nt account consists of an attempt to review recentP to the subject matter not covered in the articles by), Krogh (49), and Fry (34). Aspects of respirationin this paper are restricted to external respiration, andmeans of interchange of respiratory gases between the

external environment.lon of fishes has been approached by descriptive ac-mechanisms and quantitative changes; by comparing

with similar ones in other classes of animals; and byrespiratory system to the activity of fish, as well as to

factors, both external and internal (49, 52, 60, 61,such comparisons are made, it is desirable to set out

conditions which govern respiration in fishes and mam-4).

~e of the gill and its projecting filament has beenWith that of the lung of mammals and its recessedLeiner (52), Van Dam (28), and Krogh (49). Krogh

Van Dam's work in demonstrating that the flow of\V~terthrough the gills is opposed to the flow of blood~s, thus making for very efficient extraction of oxygen.ernal respiratory medium. Associated with this an-

8o:ement is the fact that in teleost fishes at least, theof th across. the gill filaments is in one direction, while

of e r~splIatory medium in mammals is tidal in nature.of e;~h:;~e bet,;een the. external respiratory medium

In lIS earned out 111 the same phase (liquid)as th . 'tre d ere are two phases, a gaseous one enteringe OWnto and within the alveolus, opposing a

91

SOME ASPECTS OF THE PHYSIOLOGY OF FITABLE 4 811

RESPIRATION IN FISHES AND MAMMALs

liquid phase (tissue of the alveolus, blood, etc.). Thebetween the blood and the tissues is carried out in the same(liquid for both fishes and mammals).

Physico-chemical conditions governing respiration inmammals are also very different (Table 4). The temperatumin inland fresh waters inhabited by fish is approximately O·and in the sea it is _1.8° to 30°C. In one downwardthrough the thermocline the temperature may drop ~orn8°C. The body temperature of fishes is not greatly difftheir immediate environment. These possible ranges fo~perature of fishes are contrasted with the relativelyfixed body temperature of mammals (37° to 40°). Ch~of the loading and unloading of oxygen to and fromlongwill shift with changes in temperature as was shOWUd'tI'ons.I con 1Barcroft and his associates (12). These specia ratufl'ling oxygen exchange and hemoglobin at .low ~~P;esefirst appreciated in fishes by Krogh and LeItc~ ( hi h mayalso were aware of the variable oxygen levels W ICr e"bathe fish gill, conditions which may range fromh~e~ photstagnant waters to supersaturation in areas of e~gwithillactivity (Table 4). The pressure head of OX

ygd 100 J1IJ1I.

of mammals at sea level ranges between 80 an. h aItittldalthough admittedly mammals living at very hlg

I

p O. of inspiredmedium

p CO. of expiredmedium

O. Diffusion rateO. Capacity of external

mediumDensity of medium

92

ConditionType of respiratory

organCirculationVentilation

Medium of exchange

Body temperature

I"

I:

II

FishGill (Filament)

RESPIRATION IN FISHES 93

1 er loading pressures. The conditions for unloading0':re also different for the two classes, for fishes may:Uboo dioxide vacuum (in sea water as pointed out

• others (29», while for fresh water fish the carbon• nt will usually be a value of less than 1 mm. Hg in~gs. Carbo~ dio~de is e.ver present in the mammalian

pressure is relatively hIgh (39).• canee of the differences in diffusion rate of oxygen

and liquid media to respiration is discussed by Leiner. eoces in oxygen capacity together with the equally

oees in the density of the external respiratory mediaby Leiner (52), Van Dam (28), and Krogh (49).'p of these various factors to the high oxygen utiliza-

'00) rate from the respiratory media is expounded by28).

that a comparison of respiratory mechanisms betweenals is not easily made. Moreover, particular adapta-

. atory mechanisms can be related only to particularenvironment (49). Nevertheless attempts have been

te respiration to environment as well as to activitymany of the papers entitled respiration, a wider use

has been given than employed in this review. In par-consumption, or respiratory metabolism has been

an index of respiration. While no one will deny thatgaseous metabolism are related, and that the latter

e the former, it seems wise to separate the two~~empt ~o study the e~e~ts of either environment or

'phYSIOlogyof respiration. There are further diffi-on ith .stud WI usmg oxygen consumption of fishes as anS:' for at the present time, no paper upon oxygen

leas hes appears to be comparable with any otheron that not all the various conditions now known

t us metaboliSM have been controlled. These con-(22

emg;rature (~O, 79), biological condition (48, 78,

) 'F' ' 71), diurnal variation (80) and previous. mall h' 'hich h y, t e relatmg of respiration to activity is. as a very restricted application for as yet theng the ti 'ac ivity of fishes in absolute terms are

SUbject ofIn a em('rgency respiration (Notatmung) has

recent monograph by Olthof (57).

CounterLiquid flowing in one

directionTissue ( liquid) and

liquidVariable

_2° to 40°C.1-200 mm. Hg

0-10 mm. Hg

Low (liquid)Low

High Low

94 SOME ASPECTS OF THE PHYSIOLOGY OF FISH

ANATOMY OF RESPillATORY SYSTEM

Leiner (52) has rev~ewed ~e literature. on the a~atomy of therespiratory system, and ill addition he has gIven consIderable aution to the accessory organs of respiration. Rora (45) has revie\en.

. f th . b . \leda series of papers on the physiology 0 e au- reathing fihMonopteris favanensis. For a comprehensive treatment of resPirati:~and the physiology of the swimbladder, the works of Rauther (62)and von Ledebur (51) should be consulted. Krogh (49) has dis.cussed adequately the anatomy of fishes in relation to respiratorymechanisms, and has given timely emphasis t? Van Dam's (28)careful work in describing the relation of the circulatory systemofthe gills to the course that respired water takes. (The earlier paperby Woskoboinikoff (88) on circulation of blood through the gillshas not been seen by this reviewer.) The blood of lowest oxygencontent is conducted to the gills as the respired water leaves, andthe oxygenated blood leaves at the point where inspired water(with its higher oxygen tension) enters the gills (28). This prin-~iple of counter circulation obtains for the exchange of metabolitesbetween maternal and foetal circulations in mammals (12),

Bevelander (14) noted in his detailed study of 36 species thatthe respiratory epithelium of the teleosts was of the flat, squam?ustype while in elasmobranchs it was a thicker polyhedral or cubicaltype. Bevelander also reported that mucous cells appear larger andmore numerous on the gill filament proper, and smaller and 1es~numerous in the interlamellar spaces and on the free surfaces 0

the lamellae. By the use of specific stains, Copeland (26) demo;-strated the presence of chloride-secreting cells distinct from t emucous-secreting cells in the respiratory epithelium. , aI

Willem (82, 84, 85, 86) has published a series of anatoml~r_papers on the reduction and modification of the respiratory appatus in certain members of the teleost Plectognaths. 1bt'r

Gray (35, 36) has determined the number of gills, .the nl1:nitsand the length of gill units and the number of resplratoryber of

. . f . fi h s The num .(secondary lamellae) in 8 specIes 0 marme s e . . sand J

respiratory units differs distinctly from species to spec~e '1ys01:lJlf . . tor fi h and relativerelatively great for sur ace active mlgra ory , s

for sluggish bottom fishes. , CO of or:JGudger (38) has called attention to the occunen

breathing valves in 150 species of fish. d SClllatllrtlJ,'f th dctaile nlll (Ba1abai has written a senes 0 papers on c , d fisheS

of the respiratory apparatus in cyclostomes and Jawe

RESPIRATION I FISHES 95

10). Tatarko has describe,d the relationships of the hyoid and. ary bones to the branchiostegal apparatus in the Acipenseridae

1S) and P~lyodontidae (74). ,1~ch of the Russian work in thisd was il1ltiated by Woskobomikoff who wrote on the anatomy

~ the hyoid a~d ?ranchial arches in the lower Gnathostomata inxeJation to respuation (90, 91, 92).

The paper by Pliszka (58) has not been available to the presentreviewer.

MECHANISMS OF BREATHING

an Dam (28) has shown for the rainbow trout, Salmo shasta,t water is expressed over the gills during both the inspiratory

d expiratory phases of the respiratory cycle. During inspirationthe oral cavity is being widened and the opercula are being

ucted, the oral valves are open, the opercular valves are closed,water is drawn along the gills by the widening of the gill

'ties. During expiration when the oral cavity is being decreasedsize, the opercula are abducted, the oral valves are closed, the

ar valves are opened, water is driven along the gills by thease in volume of the oral cavity. "In other words, during in-

tion the gill cavity acts as a suction pump, during expirationmouth cavity acts as a pressure pump; in both cases water is

wn along the gill." (28). The significance of the continuous flowlVater~cross the gill to the counter flow of blood through the gill

ents IS expounded by Van Dam (28). Earlier, Woskoboinikoff~fu?lished a leng~y treatise on the suction pump system and

ation of the suction pump to the pressure pump in a numberteleosts. In 1939 Balabai showed that the alternate suction and

hs pump action is characteristic of the breathing of elasmo-~ s (8~ and sturgeon (9),Iconsl~erable interest are Van Dam's observations on the uni-

fratventIlation and also periodic ventilation in the eel. The

hory pauses may extend to five minutes. The pauses are notW en the a' I' , 'I I'ata nima IS usmg Ul11 atera gIll ventilation. Both the

ry pauses and the unilateral ventilation occur when theIn appears to be in a resting condition (28).

papers a th hani fSij B" n e mec anism 0 movement of gill filaments innt~. 6~~,(l5,16) discuss~s ~e positio~ of the tips of the gilltOuch mg normal r spiration the tips from adjacent gille. 1'h: and thus the respiratory water is forced through the

IS arrangement was deduced by Van Dam (28) from


the high percentage oxygen utilization rates (80%) and obsein living Tinea tinca by Hofdijk-Enklaar (44) and confirme;bdBijtel (15, 16). During the so-called cough reflex the tips of thYfilaments are retracted to permit the sudden flow of water throu hthe gills (15, 16). g

REGULATION OF BREATIllNG AND RESPIR.>\.TORY REFLEXES

. Respiratory centreBabkin and M'Gonigl~ (4) in. their studies ~I~ the respiratory

mechanism in skates, review the literature pertammg to their sub.ject up to .1930. They recount the views of Baglioni (5) whoasserted that the initiation of the respiratory act in fishes is central·of Bethe (13) who contended that the respiratory act is accom~plished through peripheral reflexes; and those of Babak (3) whoassumed an intermediate position by claiming that respiration isactuated primarily by an autonomous centre and modified second-arily through peripheral reflexes. Babkin and M'Gonigle stated thatmuch of the early controversy was due to the variety of speciesstudied, and further, since the place occupied in the evolutionaryscale by elasmobranchs and teleosts is not the same, the respiratorymechanisms may also be different. To these statements should beadded that the variety of mechanisms of respiration in diffe~eDtfishes (5, 49) and even in the same fish (27, 28), and the vane.tyof experimental methods used including the use of anaestheti~which may depress respiration, have not aided physiologists JD

formulating a general scheme of respiration in fishes. . ..Lutz (53) and Babkin and M'Gonigle (4) have funllshed JD

direct evidence that respiration is maintained by an autonorno~centre in certain elasmobranchs. These studies add to the (~.,experimental work of Vulpian (77), Steiner (72) and Hyde f ileJwho demonstrated that in fishes all respiratory movements atials

. d R di I tric potenwhen the medulla was sectioned. ecor mg e ec d"k (1)from the isolated brain stem of goldfish, Adrian and Buyten I}ato!\'observed close correspondence between impulses and resplf 'activity. . us coJll<

More recently Powers and Clark (59) sec~oned ~ar;o medialbinations of the IXth and Xth cranial nerves ImmedIate y f jot'<to the gills in three species of fish (brook trout, Salvelintl~l~e~l,tinalis: rainbow trout Salmo gairdnerii iridens and the.w of tJlB, , d h th . tegn-;Lepomis macrochirus). Their results showe t at e in

RESPIRATIO I FISHES 97

ent pathways from receptors in the gill regions is essential toJIlaintenance of respiratory action. From these results the au-

\bOfS contend that the ~eflex system dominates the control of..,spiration for thes~ s~ecIes.. .

Van Dam (28) m his observations on the respiration of the eel~uilla vulgaris in a resting condition found that there wereresPiratory pauses up to five minutes' duration; at other times theeel ventilated on one .side orli~, althou~h no respiratory pausestptervened when the animal ventilated unilaterally. These peculiari-

in the respiration of the eel suggest a stronger dependence ofrespiratory centre upon metabolism than appears in other fishes.

'ratory reflexes1. Mechanical. Baglioni (5) described changes in respiratory

ythm for teleosts and elasmobranchs when air was introducedto the respiratory passages. Lutz (53) studied the effect of sud-

y starting and stopping the respiratory flow of water conductedthe spiracles of the dogfish, Scyllium canicula, and found thatlbition of respiration occurred, followed by reflex ejection ofer from the mouth and gills. When the respiratory flow was

sed gradually, respiratory movements increased; on graduallycing the flow, the rate of respiratory movement decreased tostarting level. Ogden (56) observed in the dogfish, Mustelusomicus, a simple quantitative relationship between the respira-water pumped over the gills and the hydrostatic pressure be-

.the mouth and the gill slits from -7 to 3 cm. water, yet thething frequency remained constant.

2. Chemical. The response of some fishes to changes in theen ~d also the carbon dioxide content of the inspiratory waterown m Table 5. Where possible, cases have been listed where

bauthors included a simultaneous accounting of the frequencyreathing d th . f . .an e quantity 0 water moved durmg each resprra-cycle. Observations by Baglioni (5) and Westerlund (81)made on frequency only.

~e response in the dogfish, Mustelus californicus, to lowered: and also to increased carbon dioxide is one of struggling

11emg to Ogden (56). No change was noted in either breathingnc~ or quantity of water shifted. Clear indication of a similart.m elasmobranchs is to be found in the earlier studies of

S ~~~and Willem (69) for the ray, Torpedo ocellata, and dog-cy tum. canicula, and by Bethe (13) for the dog£shes, Scyl-


TABLE 5

EFFECTS OF DECREASED OXYGEN .AND INCREASED CARBON DIOXIDE:Uro RESPIRATION IN FISHES

Increased rateand activity


Increased rateNone on volumeIncreased rateNone on volume

one on rateIncreased

volumeIncreased rateIncreased

volume; orapnea

. 'mentallium canicula, and S. catulus. In all these studies the e~per~ be-animal was held in a fixed position. Baglioni (5) studwd e diJll

11 d to S''''haviour of the dogfish, Scyllium caiulus, when a owe . uteSfreely in oxygen-free sea water. He found that within three ~In tor'!the fish became restless, swam aimlessly and that the resplf;'eri_

. D' g the ex]-frequency increased from 54 to 66 per minute. urm eOC\'th . t ry frequ 'mental period of 1hour and 56 minutes, e respira 0 ueocY

. h tivity d the freqrose at one point to 90 per minute; t e ac VI an

ELASMOBRA CHS

Torpedo ocellata

Scyllium canicula

Scyllium catulus

Scyllium caniculaScyllium catulusMustelus 'californicus

TELEOSTS

"Karausch"Carassius vulgaris?Serranus scriba

Scorpaena ustulata

Spheroides maculatus Hall ( 40 )

Baglioni (5)

Schoenlein andWillem (69)

Schoenlein andWillem (69)

Baglioni (5)

Bethe (13)Bethe (13)Ogden (56)

Westerlund(81)

Baglioni (5)

Uranoscopus scaber Meyer (55)

Salmo shasta Van Dam (28)

Anguilla vulgaris Van Dam (28)

lone on rate

None on rate

Increased rateand swimming

None on rateNone on rateNone on rateNone on volumeStruggling

response

Increased rate



Increased rateone on volume

None on rateIncreased

volumeIncreased rateIncreased

volume

..............

None on rateNone on rateNone on rateNone on volumeStruggling

response

Increased rate


breathing seemed to correspond. The control animal remainedthe same position throughout the experiment, and except for one

obServationof an increased rate to 60 respirations per minute, theremained at 54 per minute.

••terrom studies made on teleosts (Table 5) it appears that adecrease in oxygen tension or an increase in carbon dioxide in

ter flowing over the gills brings about changes in respiration.;e response is not always the same in detail. In Uranoscopus,cober, Meyer (55) found that the frequency alone changes; in therainbowtrout, Salmo shasta, Van Dam (28) found that both factorschanged.Struggling, dyspnea and apnea also occurred in the eel inresponseto carbon dioxide depending on the concentration used(28). Woskoboinikoff and Balabai (94) showed that the carprespondedto oxygen lack by an increase in breathing activity.

Ogden (56) states that the response in the dogfish to increasedearbon dioxide or decreased oxygen in respired water is one ofswimming.Tracy (75) found that carbon dioxide initiated the"'random"body movements in the larval form of the teleost toadfish,Opsanus tau. However the earlier work of BagHoni (5) for the dog-

Scyllium catulus, still must be recognized; in this study the~sh responded to oxygen-free sea water by swimming and by

increase in respiratory frequency. In Ogden's (56) experiments,fish was held in a fixed position, and the response was one ofggling only. It is possible to argue that in the natural environ-t the increase in frequency of respiration in the dogfish, Mus-californicus, may be due to the increased metabolism which

~wed the swimming movements caused by the unfavourable.anment. It is possible too that the mechanism in the species

died by Baglioni is different from that in the species studied byden. The response to changes in respiratory gases in elasmo-

ehs should be tested further. As far as the teleosts are con-ed the respiratory response is positive, though variable.

RESPIRATION AND CIRCULATION

~~~oenleinand Willem (69) long ago reported for the dogfish,m canicula, and the ray, Torpedo ocellata, that the heart

th:e!exly in~~ite~ w~en the spiracles closed, the sensory limb'0 ~flexongmatmg in the pharyngeal cavity. Bethe (13) and

ni (5) stated that cardiac and respiratory inhibition occurreder' 1chez . In e asmobranchs. Lyon (54) reported for the shark,nas, that the cardiac rate was intimately related to the


respiratory rate, and that there were indications that the hnormally takes its rate from respiration. Nevertheless the myo :a~nature of the heart-beat is shown by the fact that the heart g l1icb I af usuaUeat~ ong ter res~iration has ceased (54). Lutz (53) studi Yrespiratory and cardiac r~Hexes in the do~fish, S~yllium canicuedan~ reported that electrical and mechamcal stimuli applied ~,vanous parts of the body and certain viscera caused reflex inhib' . 0

f b th . ti d di .. S· Iliono 0 respIra IOn an car lac activity. toppmg or starlin thHow of respiratory water over the gills caused respiratory inhifili eand someti:nes. c~r~~ac inhibition~ stimula.tion of the ventri~:ca~sed cardiac inhibition and sometimes respiratory inhibition (53).Willem (83) has recounted the published work on synchronism frespiratory movements and heart-beats in fish. 0

Hart (42) investigated the stroke volume of the heart in fourspecies of freshwater fish and noted that the values correlated~nvers~ly with the Bohr effect of the bloods of the same speciesinvestigated by Black (17) as discussed below. Hart suggested thatthe differences in circulation may compensate for differences inoxygen transport imposed by the differences in the bloods for trans-porting oxygen.

RESPIRATORY BLOOD-GASES AND TISSUE TENSIONS

MethodsSince th~ comprehensive review by Redfield (49) appeared on

the respiratory functions of blood, more evidence has been obtainedon the fragility of fish blood. Black and Irving (21) reported thathemolysis abolished the Bohr effect for the bloods of at least twOteleosts, and that hemolysis of the blood of the carp, Gypriniscarpio, may be brought about by the use of the anticoagulantpotassium oxalate. Hamdi and Ferguson (41) found that fluorid~Sused to prevent glycolysis of mammalian blood, caused hernolYs~of ~sh bl~od. Krogh and Leitch (50) used leech head extractad.their studies of fish blood; they also used defibrinated fish blo dIrving, Black and Safford (47) and Black and Black (20) faunthat blood which had been drawn from fish for longer than 12 torea-18 hours could not be used for blood-gas studies, although no rJl-

sons were presented for the anomalous changes in both CO~ COtedbining power and oxygen capacity. Ferguson and Black (31) n~TltlS

that the CO2 combining power in bloods from the carp, Gypr thecarpio, and rainbow trout, Salmo gairdnerii, increased when


was stored fully oxygenated, and decreased when stored ingen. The importance of lactic acid in altering the properties

fish blood has been emphasized by Von Buddenbrock (24),t (64), Redfield (63), Black and Irving (21), Secondat and

(70) and Auvergnat and Secondat (2).

fttJ1ISPortof carbon dioxideRedfield (63) has reviewed the literature relating to the equi-. of carbon dioxide with the blood of fishes. In a number ofps of animals which carry hemoglobin as the respiratory pig-t the form of the curve is much the same, although the quantity

bicarbonate increases as the hemoglobin content increases. Thisborne out by the work of Root (64) on marine fishes.The effect of hemolysis of fish blood in reducing the content of2 is very great as shown by Black and Irving (21) for certain

water fishes and by Root, Irving and Black (67) for certain. e fishes. The integrity of the red cell is of importance to the

ort of CO2

as well as for oxygen transport (11). Ferguson,ath and Pappenheimer (32) and Ferguson and Black (31)

:vedemonstrated that chloride and bicarbonate ions interchange. g oxygenation and de-oxygenation of whole blood of fishes,ich brings this aspect of the transport of CO2 carriage in har-y with that of mammalian blood as demonstrated by Vane (76). Ferguson, Horvath and Pappenheimer (32) have also. hed evidence that the transport of CO2 in the carbamino

is possibly absent in the blood of the dogfish, Mustelis canis,may be present in the bloods of the carp, Cyprinus carpio, andbow trout, Salmo gairdnerii (31).The buffer power of fish blood is not so great as that of humanb between the partial pressures of 10 to 60 mm. Hg (63), yet

. uffer power of fish blood over what is probably the physio-(4).range for fishes (0-15 mm. Hg) is considerable (20, 31,

'Ze.Haldane effect (25) or the effect of oxygenation on CO2

t l~ng power is present in the bloods of certain teleosts accord-~l oot (64), Ferguson and Black (31), Black (17) and Black

aack (20). Dill, Edwards and Florkin (29) found that a

ne efle t .O II

c IS present over the physiological range for the skate,ce ata hilald ,w e Ferguson, Horvath and Pappenheimer found

ana effect in the dogfish, Mustelus canis (32).


Transport of oxygenKrogh and Leitch (50) described the properties of fish bl

for transporting oxygen and observed a degree of difference in~~dability of bloods of different species to combine with oxygen. Th ealso noted a sensitivity of the union of blood with oxygen to ~ypresence of low tensions of carbon dioxide. They contended th ethe sensitivity of fish blood to carbon dioxide was an adaptatio~tfor these authors appreciated the work that Barcroft and his col:laborators (11) had published to the effect that a decrease in tem_perature increased the affinity of hemoglobin for oxygen, and thatthis effect was countered by the Bohr effect (23), namely thatcarbon dioxide reduces the affinity of hemoglobin for oxygen, andhence physiological conditions would operate to augment thetension at which oxygen would be unloaded to the tissues at lowtemperatures. Krogh and Leitch also appreciated the significanceof the Bohr effect on the loading tension of oxygen in bloods offishes in poor oxygen supply. These various relationships are clearlyset out by Krogh (49) and Leiner (28). These reviewers list thefishes showing a very large Bohr effect as first observed by Root(64) in certain marine fishes. Green and Root (37) postulated thatthe marked reduction of oxygen combining power by carbon dioxidemight be due to the inactivation of one or more prosthetic groupsof the hemoglobin molecule. At the suggestion of Dr. D. B. Dill,Black and Irving (21) hemolyzed bloods of two freshwater fishesand found that the sensitivity to carbon dioxide was obliterated.These studies were extended by Root, Irving and Black (67), Rootand Irving (66) and Black (17), who found that in some instancesthe Bohr effect was not abolished totally by hemolysis. These Snddings and later data obtained by Irving, Black and Safford (47) anhBlack (18, 19) substantiated the early view proposed by Kra?and Leitch (50) that the specificity of fish blood as regards affil~~for oxygen must rest partly on the hemoglobin and partly on hespecial chemical milieu maintained by the intact membrane of terythrocyte. Black

In a limited series of four species of freshwater fishes, d for(17) found specific differences in the affinity of £sh bloo £ishoxygen and also in the Bohr effect. The indications are that har-blood with a low Bohr effect and a high affinity for oxygen k ill

acterize fish which inhabit warmer waters of a temperate la Bgellsummer; and that a large Bohr effect and a low affinity for o~o\V-characterize fish which inhabit the colder waters in summer.


r as Krogh (49) warned, it is possible to find an ecologicalptation between the physiological machinery and limited en-

~nrnents, but usually the relationship does not hold for larger~ternatic groups and wider environmental lattices.S'j Black (18), and Black and Black (20) investigated the bloodf the Atlantic salmon, Salmo 'salar salar, and Black (19) the brook

:.out, Salvelinus fontinalis, acclimated to summer and winter con-ditions, but found no difference in the Bohr effect for the twoseasons.

Oxygen capacity of the blood of fishes is variable both withinthe species and from species to species (63). In some instances theoxygen capacity is so low that at low temperatures a significantmeasure of the transport of oxygen must be attributed to the oxygenphysically dissolved (29, 32, 64).

Tissue tensionsConditions for discharging and loading carbon dioxide and

oxygen to and from the blood must be known if the transportcapacity of the blood for the respiratory gases is to be rationalized.ignificant among the conditions are the temperature and the

physiological tensions of oxygen and carbon dioxide at the twophases of respiratory cycle, namely, the tissues and the gills. Accord-ing to the work of Von Buddenbrock (24) on fish and of Scho-lander (68) on diving mammals, the level of lactic acid in theplasma must also be considered.

The determination of tissue tensions in fishes is difficult indeedas . ,.IS recounted by Root (64). Dill, Edwards and Florkin (29)

~ated the tension of carbon dioxide in "arterialized" blood takenl.~m the efferent side of the gills of the skate, Raia ocellata, to be0( ;m. Hg. Root (64) estimated the tension of carbon dioxidefin e blood taken from the gills of the sea robin, Prionotus caro-0( ~' to be 2 mm. Hg, and the "venous" blood taken from the heart(Sl)e toa~fish, Opsanus tau, to be 10 mm. Hg. Ferguson and Blacktaken obtamed values of 5 to 10 mm. Hg carbon dioxide for blood<;arp /;r0rrr. the heart of the rainbow trout, Salmo gairdnerii, the(I8), a~~nnus carpio, and the bullhead, Ameiurus nebulosus. Blackcarbo di ~Iack and Black (20) noted that the venous tension of

su. n 10Xldefor the Atlantic salmon, Salmo salar salar acclimatedIllIller w 6 8 '·ons. as to mm. Hg and 3 to 6 mm. Hg for winter con-

tactic id Iaci evels have been recorded for fish by Van Budden-


brock (24), Secondat and Diaz (70), and Auvergnat and Second(2). These works indicate that lactic acid accumulates in ~tplasma during activity. Von Buddenbrock (24) discusses the inl~portance of lactic acid to the carriage of oxygen, particularly fofish blood sensitive to CO2• r

Root (64) estimated the venous tensions of oxygen in a seriof four marine teleosts ranged from 0 to 20 mm. Hg, in three fres~~water teleosts Ferguson and Black ( 31) estimated the venoUstensions of oxygen to range from 3 to 10 mm. Hg.

SUMMARY

Recent papers on respiration in fishes were reviewed. By respira_tion is meant the exchange of oxygen and carbon dioxide betweenthe external environment and the gills. Papers on the respiratoryfunction of the blood were included, but the literature on oxygenconsumption in fishes was excluded.

Important in the advance of knowledge of respiratory mechan-isms has been the description of the principle of counter circulationbetween the respiratory flow of water and blood through the gills,and the efficient extraction of oxygen from teleost gills made pos-sible by the continuous circulation of respired water in onedirection, and by the position of the tips of adjacent gill filaments,which are so held that during normal respiration water is forcedthrough the lamellae. During "coughing" the filament tips separatereflexly. .

The importance of the respiratory centre of the medulla to theautonomous activity of respiration has been established by e~~experiments on sectioning, and by action potential studies whi.show a correspondence between impulses arising from the bra:and respiratory frequency. However, the centre seems todominated by reflexes in certain teleosts. . tirDuIi

Respiration may be modified by a variety of physI?al :tirDuIithrough reflex. patterns. The respiratory response to chemical sioll

db di 'de tensuch as lowered oxygen tension or increase car on ~ox~ lasJ1lO"'is definite although variable in teleosts but uncertam III e

branchs. f 11o\\'s •Transport of carbon dioxide by the blood of teleosts . 0 bloael

somewhat conventional pattern established for mammaha~raJlcIJSwith unexplained peculiarities, while the blood of elas~O is cO'"shows little or no Haldane effect. The buffering capaCity


ble over the physiological range of carbon dioxide tension fOT

blood of teleosts varies in oxygen capacity, in the affinityblood for oxygen, and in the Bohr effect. In some instancesgen affinity and Bohr effect constitute an adaptation to a

ed environment.e physiological tensions of carbon dioxide are very muchtha~ those found ~ mamma~s. The tensions of oxygen at

g III fishes are vanable. The Importance of lactic acid levelsplasma to the unloading and loading of both gases is

erable.

ACKNOWLEDGMENTS

generous and invaluable assistance given by the Referenceent of the Library, The University of British Columbia is

ly .acknowledged. Without the literature provided througherlibrary Loan Service, this review could not have been

LITERATURECITED

('" original paper not consulted)

N, E. D. and BUYTENDIJK,F. J. J. Potential changes inthe isolated brain stem of the goldfish. J. Physiol., 71:121-135, 1931.

DVER~NAT,.R. et SECONDAT,M. Retentissement plasmatiquede I exercise musculaire chez la carpe (Cyprinus carpio L.)Compt. Rend. des Seances de l'Academie des Sciences 215:92-94, 1942. '

~, E. Die Mechanik und Innervation der Atmung.~~~~erstein's Handbuch verg!. Physiol., 1:597-706, 1912-

ION, B. P. and M'GONIGLE, R. H. Studies on the respiratory

3111echanismin skates. Contr. Can. BioI and Fish N S 6·17-339, 1931. " .. , .LION! S D At h .Ph .,. er mungsmec amsmus der Fische. Z. allg.

YSIOl.,7:177-282, 1907.des i ~P. Der Atmungsapparat bei Cyclostomata. Academiede clen~es de. la It S S d'Ukraine. Travaux de l'Institut

Zoologre et Biologie. Vol. III: 11-105. 1935.


7. --- Zur Frage iiber die Homologie der visceralen Bogen dCyclostomen und Gnathstomen. Academie des Sciences ~tla R S S d'Ukraine. Travaux de l'Institut de Zoologie eBiologie. Vol. XVI:27-45. 1937. et

8. --- A study of the work of the respiratory apparatus .Selachians. Academy of Science of the Ukraine S S R Ins~tute of Zoology, Papers on Iorphology. 73-110. 1939. -

9. --- A study of the work of the respiratory apparatus inAcipenseridae. Academy of Science of the Ukraine S S R.Institute of Zoology, Papers on Morphology. 111-145. 1939.

10. --- Metamorphosis of the visceral apparatus of the lamprey.C.R. Acad. Sci. Moscow. N.S. 53:765-768, 1946.

11. BARCROFT,J. The respiratory function of the blood. Cam_bridge, 1914. . .

12. --- Features in the architecture of physiological function.Cambridge, 1938.

13. BETHE, A. Atmung; Allgemeines and Vergleichendes. Hand-buch norm. path. Physiol., 2: 1-36, 1925.

14. BEVELANDER,G. A comparative study of the branchial epi-thelium of fishes; with special reference to the extrarenalexcretion. J. Morph., 57:335-352, 1935.

15. BIJTEL, J. H. The mechanism of movement of the gill.£lamentsin Teleostei. Experientia, 3: 158-165, 1947.

16. --- The structure and the mechanism of movement o~ ~~gill-filaments in Teleostei. Arch. Neerland. de Zool., 8.2288, 1949. fr sir

17. BLACK,E. C. The transport of oxygen by the blood of ewater fish. BioI. Bull., 79:215-229, 1940. tl tic

18. Respiratory characteristics of the blood of the A ~:IJI'salmon Salmo salar salar L., acclimated to sumrne~ V.

, S C SectiOnperatures in fresh-water. Proc. Roy. oc. an.,(Abstract). 50. 1947. h broO~

19. --- Respiratory characteristics of the blood of t d wintertrout Salvelinus fontinalis acclimated to summer antemperatures. Unpublished data, 1947. . ciaUoJl

V Sad co dlsso _11Ii20. BLACK, E. C. and BLACK, . . xygen an 2 salaf slY

curves of the blood of the Atlantic salmon Salma Arner. 5oC-L. acclimated to winter temperatures. Fed. Proc.Exp, BioI. (Abstract) 5: 8, 1946. . poo tIJ'

21. BLACK,E. C. and IRVING,L. The effect of hem~yslps t~hysioJ..affinity of fish blood for oxygen. J. Cell. and ornv-12:255-262, 1938.

RESPIRATIO IN FISHES 107

BLACK,E. C., FRY, F. E. J. and SCOTT, W. J. Maximum ratesof oxygen transport for certain freshwater fish (abstract).Anat. Rec., 75: ( Supplement) 80, 1939.

BOlIR, C., HASSELBALCH,U. KROGH, A. Ueber einen in biolo-gischer Beziehung wichtigen Einfluss, den die Kohlen-saurespannung des Elutes auf dessen Sauerstoffbindung iibt.Skand. Arch. Physiol., 16:402-412, 1904.

BUDDENBROCK,W. vo . What physiological problems are ofinterest to the marine biologist in his studies of the mostimportant species of fish? Rapports et proces-verbaux desreunions du Conseil permanent international pour I'explora-tion de la mer. 101, pt. 1:3-14, 1936.

. CHRISTIANSEN,J., DOUGLAS, C. G. and HALDANE, J. S. Theabsorption and dissociation of carbon dioxide by humanblood. J. Physiol., 48:244-271,1914.

COPELAND,D. E. The cytological basis of chloride transfer inthe gills of Fundulus heteroclitus. J. Morph., 82:201-228,1948.

CROZIER,W. J. and STIER, T. B. Critical increment for oper-cular breathing rhythm of the goldfish. J. Gen. Physiol., 57:699-704, 1925.

A DAM, L. On the utilization of oxygen and regulation ofbreathing in some aquatic animals. Groningen, 1938.

DIu, D. B., EDWARDS,H. T. and FLORKIN, M. Properties ofthe blood of the skate (Raia ocellata). Biol. Bull. 62:23-361932. ' ,

EcE, R. and KROGH, A. On the relationship between the tem-perature and the respiratory exchange in fishes. Intern.

~evue f. Hydrobiol. u. Hydrogr., 7:48, 1915-1916.GUSON,J. K. W. and BLACK,E. C. The transport of CO2 in

~~ blood of certain freshwater fishes. BioI. Bull., 80: 139-F'b ,1941.

;so ,J. K. W., HORVATH,S. M. and PAPPENHEIMER,J. R.. e transport of carbon dioxide by erythrocytes and plasma

1I'to~~gfish blood: Bio~. Bull., 75:381-388, 1938.E '. M. La biologie des hematinoproteides oxygen ables.'t "~enentia, 4:176-191, 1948.t1ni~E. J. Effects of the environment on animal activity.55'1' Toronto Stud. Biol. 68, Pub. ant. Fish. Res. Lab.

. -62, 1947't IE'~ . The relation between gill surface and activity in

e fishes. Anat. Rec. (Abstract) 96:518, 1946.

108 SOME ASPECTS OF THE PHYSIOLOGY OF FISH .

36. --- Respiratory area of the toadfish. Anat. Rec. (Abstract).105:49, 1949.

37. GREEN,A. A. and ROOT, R. W. The equilib~ium betweellhemoglobin and oxygen in the blood of certain fishes. BiolBull., 64:383-404, 1933.

38. GUDGER,E. W. Oral breathing valves in fishes. J. Morph., 79.263-285, 1946. .

39. HALDANE,J. S. and PRIESTLEY,J. G. Respiration. Oxford, 193540. HALL, F. G. The respiration of puffer fish. BioI. Bull., 61:457:

467, 1931.41. HAMDI,T. M. and FERGUSON,J. K. W. Hemolytic action of

fluorides on certain nucleated erythrocytes. Proc. Soc. Exp.Biol. and Med., 44:427-428, 1940.

42. HART,J. S. The cardiac output of four freshwater fish. Can.J.Research, 21:77-84, 1943.

43. HENSCHEL,J. Der Atmungsmechanismus der Teleosteer. J.Conseil Copenhague, 14:249-260, 1939.

44. HOFDI}K-ENKLAAR,M. A. Work cited by Bijtel, J. H.45. HORA,S. L. Physiology of respiration of the air-breathing fish

Monopterus javanensis Lacepede: A review. Current Sci.Bangalore, 10:379-380, 1941.

46. HYDE,I. H. Localization of the respiratory centre in the skate.Amer. J. Physiol., 10:236-258, 1904.

47. IRVING,L., BLACK,E. C. and SAFFORD,V. The inHu~nce;temperature upon the combination of oxygen WIthblood of trout. Biol. Bull., 80:1-17, 1941. alin-

48. KEyS,A. B. A study ~f ~e selective ac~on o~ ~ecreasedn~uJuIity and of asphyxiation on the Pacific killifish, Fu .411-parvipinnis. Bull. Scripps. Inst. of Ocean. Tech. Ser., 2.490, 1931. . rnecb-

49. KROGH,A. The comparative physiology of respIratoryanisms. Philadelphia, 1941. . of tbI

50. KROGH,A. and LEITCH,I. The respiratory functionblood in fishes. J. PhysioI., 52:288-300, 1919. tioo ~

51. YON LEDEBUR,J. Ueber die Sekretion und Resorp 211-~Gasen in der Fischschwimmblase. Biol. Rev., 12:1937. 'g l~

52. LEINER,M. Die Physiologic der Fischatmung. LeipZ~;y~53. LUTZ,B. R. Respiratory rhythm in the Elasmobranch,

canicula. BioI. Bull., 59: 179-186, 1930. ute54. LYON,S. P. A study of the circula~on, blood p~es;926.

respiration of sharks. J. Gen. PhySIOl., 8:279-29 ,


MEYER,H. Die Atmung von Uranoscopus scaber in ihrerAbhangigkeit vom Sauerstoffdruck, vorn Ph and von derTemperatur im Aussenmedium. Z. vergl. Physiol., 22:435-449, 1935.

()<;DE" E. Respiratory How in Mustelus. Amer. J. Ph . I145:134-139, 1945. ySIO.,

OLTHOF,H. J. Die verglei:hende Physiologie der otatmungund verwandter Erschemungen. Groningen, 1941.

~ZKA, F. Obs;rwacje nad oddychanicm ryb. Les Observa-tions sur des echanges respiratoires des poissons. C.R. Soc.Sci, Lett. Varsovie IV. 31:115-135.

POWERS,EDWIN B., and CLARKJR., ROBERTT. Control ofnormal breathing in fishes by receptors located in the regionof the gills and innervated by the IXth and Xth cranialnerves. Amer. J. Physiol., 138: 104-107, 1942.

POWERS,E. B. et al. The relation of respiration of fishes toenvironment. EcoI. Monographs, 2:385-473, 1932.

~, .A. Recherches sur Ie Metabolisme respiratoire desPoikilothermes aquatiques. Ann. de L'Inst. Ocean. deMonaco. N.S. 13:262-393, 1933.UTHER,M. Zur vergleichende Anatomie der Schwirnmblaseder Fische. Ergeb. undo Fort. Zool., 5:1-66, 1922.

FIELD, A. C. The evolution of the respiratory function ofthe blood. Quart. Rev. Biol., 8:31-57, 1933.

, R. W. The respiratory function of marine fishes. Biol.Bull., 61:427-456, 1931.

OOT, ~. W. and IRVING,L. The equilibrium between hemo-globm and oxygen in whole and hemolyzed blood of thetautog, with a theory of the Haldane effect. Biol. Bull. 3:307-323, 1941. '

, R. W. and IRVING,L., with the assistance of SAFFORDVand B· ' .ROWN,H. The influence of oxygenation upon the~ansport of CO2 by the blood of marine fish. J. Cell. and

omp. PhysioI., 17:85-96, 1940.

1 '. R. W., IRVING,L. and BLACK,E. C. The effect of hemo-ySlS upon the combination of oxygen with the blood ofSOme' fish '313, l:~~ne lIS es. J. Cell. and Compo PhysioI., 13:303-

tOLANDER,~. F. Experimental investigations on the respira-c;:; functIon in diving mammals and birds. Hvalraadets. r. 22, orske Vid. Akad., 1-131, 1940.

RESPLRATIO IN FISHES 111110 SOME ASPECTS OF THE PHYSIOLOGY OF FISH

69. SCHONLEIN, K. and WILLEM, V. Beobachtungen liber Blkreislauf und Respiration bei einigen Fischen, Z. BioI., ~:510-547, 1895. .

70. SECONDATM. et DIAz, D. Recherches sur la lactacidemie roh, ~~Ie Poisson d' eau douce. Compt. Rend. des Seances deL'Academie des Sciences, 215:71-73, 1942.

71. SPOOR,W. A. A quantitative study of the relationship betweenthe activity and oxygen consumption of the .goldfish, andits application to the measurement of respiratory meta.bolism in fishes. BioI. Bull., 91:312-325, 1946.

072. STEINER, J. Die Functionen des Centralnervensystems uudihre Phylogenes. 2 Abt., die Fische. Braunschweig, 1888.

73. TATARKO,K. Der Kiemendeckelapparat und seine Verbinduugmit dem Hyoid- und Kieferbogen bei den Acipenseriden.Academie des Sciences de la R S S d'Ukraine. Travaux del'Institut de Zoologie et Biologie. Vol. X:5-65. 1936.

74. --- Der Kiefer- und Hyoidbogen und der Kiemendeckel.apparat bei den Polyodontiden. Academie des Sciences dela R S S d'Ukraine. Travaux de l'Institut de Zoologie et Bi-ologie. Vol. XVI:47-76. 1937.

75. TRACY, H. C. The relation of CO2 to spontaneous movementsin the larvae of Opsanus tau. Biol. Bull., 48:408-431, 1925.

76. VAN SLYKE, D. D. The carbon dioxide carriers of the blood.Physiol. Rev., 1: 141-176, 1921.

077. VULPIAN, A. Physiologie generale et comparee du systeme

nerveux. Paris, 1886.78. W ASHBUR,R. Metabolic rates of trout fry from swift and

slow-running waters. J. Exp. Biol., 13:145-147, 1936. .th Plfa-

79 WELLS . A. The influence of temperature upon e res .. , arCI-tory metabolism of the Pacific killifish, Fundulus Ppinnis. Physiol. Zool., 8:196-227, 1935. iDe

80. Variations in the respiratory metabolism of the ~acowkillifish Fundulus parvipinnis due to size, season, an 1~s5.tinued constant temperature. Physiol. Zool., 8:318-336, de!

81. WESTERLUND, A. Studien iiber di~ Athembewegun~~enenKarausche mit besonderer Rucksicht auf den versc . 1 18:Gasgehalt des Athemwassers. Skand. Arch. Physlo.,263-280, 1906. aciot'-

82. WILLEM, V. Le mode respiratoire de Balistes et ostrBull. Mus. roy. Hist. nat. Belg., 27 :288-294, 1941.

__ - Le synchronisme des mouvements respiratoires et despulsations cardiaques chez les poissons. Bull. Mus. roy. Hist.nat. Belg., 27:49-64, 1941.

__ - Contributions ~ l'etude des organes respiratoires chezles Teh~osteens Plectognathes. Ire Partie: Les Balistedes.Bull. Mus. Hist. nat. Belg., 18:1-24, 1942.

85 --- Contributions a l'etude des organes respiratoires chez· les Teleosteens Plectognathes. 2e Partie: les Chaetodonti-

formes. Bull. Mus. roy. Hist. nat. Belg., 20: 1-21, 1944.__ - Contributions a l'etude des organes respiratoires chez

les Teleosteens Plectognathes. 3e partie: Les Ostracionides;4e partie: Le role de l'interoperculaire dans la manoeuvrerespiratoire chez les Teleosteens. Bull. Mus. Hist. nat. Belg.,21:1-16, 1945.

· WINTERSTEIN, H. Beitrage zur Kenntnis der Fischatmung.Pflugers Arch. f.d. ges. Physiol., 125:73-98, 1908.

· WOSKOBOINKOFF,M. Ueber den Mechanismus der Blutzirkula-tion in den Kiemenblattchen del' Teleostei. Proc. I. Congr.Zool. Anat. and. Hist. Leningrad, 1923.

· --- Der Apparat der Kiemenatmung bei den Fischen. EinVersuch der Synthese in der Morphologie. Zool. Jahrb. Abt.Anat. u. Ontog. Tiere, 55:315-488, 1932.

• ---. Der Kiemenatmenapparat bei Dipnoi. Academie desSCIences de la R S S d'Ukraine. Travaux de l'Institut deZoologie et Biologie. Vol. X. 67-77. 1936.

-- Del' Kiemenbogen del' Gnathostomata. Academie desSciences de la R S S d'Ukraine. Travaux de l'Institut deZoologie et Biologie. Vol. XVI. 3-26. 1937.

--- The hyoid arch and branchial arches in lower Gnathos-t~mata. Academy of Science of the Ukraine S S R Institute

W 0 Zoology, Papers on Morphology. 3-16, 1939.OSKOBOINIKOF M d BF, . an ALABAI,P. Vergleichende experi-;entelle Untersuchung des Atmungsapparates bei Knochen-Tschen. Academie des Sciences de la R S S d'Ukraine.

ravaux de l'I tit d Z 1 -145 ns I ut e ooogie et Biologic. Vol. X.-155. 1936.

--- Yer I . h dap g eic en -experimentelle Untersuchung des Atmungs-parates bei K h fi 1 I B b •.vo noc en sc aen. . eo achtungsergebnisse

Dkm .Jahre 1935. Academie des Sciences de la R S S d'yrIal7ne.Travaux de l'Institut de Zoologie et Biologic. Vol.

. 7-127. 1937.S~ER, W. Physiologie del' Susswasserfische Mitteleuropas.

. ttgart, 1936.

iii. respiration in fishes everal useful reviews on the respiration of fishes years s . ti f

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