Renal function and acid–base regulation in two Amazonian erythrinid fishes

14 Pages·2007·1.4 MB·English

Renal function and acid-base regulation in two Amazonian
erythrinid fishes: Hoplias malabaricus, a water breather,
and Hoplerythrinus unitaeniatus, a facultative air breather
JAMESN . CAMERON
University of Texas, Marine Science Laboratory, Port Aransas, TX, U.S.A. 78373
AND
Department ofBiology, McMasrer University, Hamilton, Ont., Canada L8S4Kl
Received February 9, 1977
6 CAMERONJ,. N., and C. M. WOOD. 1978. Renal function and acid-base regulation in two
1 Amazonian erythrinid fishes: Hoplias malabaricus, a water breather, and Hoplerythrinus
10/ unitaeniatus, a facultative air breather. Can. J. Zool. 56: 917-930.
9/ The function of the kidney in ion, water, and acid excretion was investigated in two erythrinid
0
n fishes, the water-breathing Hoplias malabaricus and the facultative air-breathing Hoplerythrinus
o unitaeniatus. Chronic catheterization of the urinary papilla and the dorsal aorta provided infor-
sity pmHat,i oann do cno tnhcee unrtirnaatrioyn psa orfa mNeat+e,r Cs aIn,da mblomoodn aiac,i dti-tbraastaeb lset aatcuisd.i tByy, amndo nliatcotrainteg, ttohtea lt ofltoalw r eonf aulr finluex,
r
ve of water, various ions, and total acid was computed. The kidneys of both species were found
ni capable of acidifying urine, creating gradients of up to 620:l for H+ ion, and contributing
U
substantially to steady-state acid excretion. There was no significant increase in lactate or total
er acid efflux from urine during postoperative (metabolic) acidosis. Respiratory (hypercapnic)
ast acidosis caused a compensatory increase in blood HC0,-, and an increase in branchial Na+
M uptake (presumably by Na-H exchange), but no change in ammonia excretion. There was no
Mc renal response in one Hoplias to hypercapnia, but an increased acid excretion in one Hoplery-
y thrinus. The behavior of the urinary excretion system appears in various respects similar to the
b higher vertebrates. There was no obvious correlation between renal parameters and air breathing
m y. in these two species.
conl
ss.e o CAMERONJ,. N., et C. M. WOOD. 1978. Renal function and acid-base regulation in two
es Amazonian erythrinid fishes: Hoplias malabaricus, a water breather, and Hoplerythrinus
ru
earchpsonal CrOytnhu rnain ietiatdueednsi,i eaH ltueo srpB,l ail aef sad cumu rlatealiatnib vdaear iancisur I sb'e,r xeica rtrehetesipor.in rC adtaienos.n iJ o.an Zqsuo, aodtlei.q I5u'e6ea:, u 9e 1et7 tH- d9oe3ps0l .ae criydthesri cnhuesz u dneiutaxe pnoiaistsuosn as
resper respiration aerienne facultative. Le catheterisme chronique des papilles urinaires et de I'aorte
w.nrcFor dduo rssaanleg .o Ontn p ae rmmeissu dree rIe'eccuoeuillleirm deenst dtoontanle de'su sriunre l,e sc ep aqruaim a eptererms uisr idn'aeivreasle eutr I 'leeq puiHli,b lrees a ccoindcee-bnatrsae-
tions de Na+, de CI- et d'ammoniaque, I'acidite et le lactate titrables, I'ecoulement total d'eau
w
w dans le rein, les concentrations d'ions divers et la cbncentration totale d'acide. Chez les deux
m especes, les reins peuvent acidifier I'urine, creer des wadients allant jusqu'i 620: 1 dans le cas de
o I'ion H+, et favoriser une excretion d'acide relativement stable. L'acidose (metabolique) post-
fr op6ratoire ne cause pas d'augmentation importante de I'excretion du lactate ou de la fraction
d acide totale. L'acidose respiratoire (hypercapnie) entraine une augmentation compensatoire des
e
d ions HC0,- dans le sang et une augmentation de I'absorption du Na+ par les branchies (sans
a
o doute dans des echanges Na-H); I'excretion d'ammoniaque ne subit toutefois pas de change-
nl ments. Un specimen d'Hoplia est reste sans reaction a I'hypercapnie; un specimen d'Hoplery-
w
o thrinus a reagi B I'hypercapnie en excretant plus d'acide. Le systeme excreteur urinaire se
D comporte donc a bien des points de vue, chez ce poisson, comme chez les vertebks superieurs. II
ol. n'y a pas de correlation tres marquee entre les parametres renaux et la respiration aerienne chez
o ces deux especes.
Z
J. [Traduit par le journal]
n.
Ca Introduction water and ion regulation (Hickman and Trump
Past investigations of the function of the teleost 1969) and nitrogen excretion (Forster and Golds-
kidney have larg- el-y focussed on its function in tein 1969). However the latter role mav be inti-
mately bbund up with another function, namely
'Supported by National Science Foundation grant PCM75-
acid-base regulation, which has not been investi-
23715 to J.N.C., a McMaster Research Boardgrant to C.M.W.,
gated in the teleosts- In higher vertebrates, the
and an NRCC grant in support of the Alpha Helk Amazon
Phase 111 Expedition. kidney is responsible for long-term regulation of
918 CAN. J. ZOOL.
blood pH, for example during chronic hypercapnic Charcoidea, family Elythrinidae), weighing 250-750 g were
acidosis, shorter term adjustments being achieved purchased from fishermen in the neighborhood of Lake
mainly by ventilation and shifts in intracellular and Janauca, about 50 km upstream on the Rio Solimoes from Man-
aus, Brazil. They were held without feeding in running water
extracellular buffer stores (Davenport 1974). In
from the Solim6es at temperatures rangingfrom 28 to 32'C, and
elasmobranchs, the kidney has been shown to con- a mean Na+ concentration of 0.220 rnM.!-l and chloride of
tribute to steady-state acid excretion, but exhibits a 0.135 mM.e-I.
negligible response to acute experimental acidosis
Experimental Procedures
(Cross et al. 1969). So far, all that is known about
Dorsal aortic cannulation was performed as described for
any possible acid-base role of the teleost kidney is trout by Smith and Bell (1964) using urethane or MS222 anes-
that the urine pH tends to be somewhat below that thesia. Cannulae were filled with Cortland saline (Wolf 1963).
of the blood (Hickman and Trump 1969), and de- The urinary papilla was catheterized as described by Wood and
Randall (19736). After surgery, the fish were transferred to
creases further after hypoxic stress (Hunn 1969),
lucite holding chambers supplied with running water and vigor-
but without information on buffering capacity, total
ous aeration. The chambers contained a water volume of
acidity, etc., one cannot assess the contribution of 2500-3000 ml, with a comparable volume of air above the water.
6
1 the urine to acid excretion. The whole unit could be sealed by taping a lid in place.
10/ On the other hand, there is information indicat- Urine was continuously collected in small covered
9/ ing that the gill of teleosts is an important acid-base polyethylene vials over regular intervals (generally Z h). Sam-
0 ples were analyscd For Na- .CI-, and ammonia concentrations.
on regulating organ. In the goldfish, there is a bran- and pH, total volume, I~lctate( in some cases), and total titrat-
y chial exchange of Na+ ions for either NH,+ or H+ able ~rciditv( TA1. In one experiment. recurds of periodic urin-
sit ions, and of C1- ions for either HCO,- or OH- ions, ation werc obtained by leading the outl'low of the urinary cath-
er presumably in the "chloride" cells of the gills eter through a drop counter connected to a strip-chart recorder.
niv (Maetz and Garcia-Romeu 1964; Maetz 1973; De- In fish with patent aortic catheters. small blwd samples werc
U periodically taken for me;lsurernent uibiood pH. total CO:.a nd
r Renzis and Maetz 1973). Similarly, these lacraie cuncentration. Concentmtions of No+. CI -,a nd am-
e
st mechanisms may occur in the trout (Kerstetter et monia in blood were usually measured on larger samples at the
Ma al. 1970; Kerstetter and Kirschner 1972). Further- end of each experiment.
c more, in the grayling, Na+ and C1- uptake vary in a Hypercapnic acidosis was induced by bubbling sealed cham-
M bers with mixtures of 2% or 4% CO, in air, supplied by gas
y manner that would tend to compensate hypercap- mixing pumps (Wosthoff). External pH also changed because of
ss.com be only. rneexicscp raoectniisodeno )st oits o;h yiC.p1ee-. rtcuhapept anrkiaaet,i o(lO eoaHdf -ins ogedx ticour meat niuoepnt t)aa crkicesu em(sH uin+- riltnohe wcisbo elrtrodr.o eeIdadn t miopnnHe feni s tsah,en fwrdrio eittsmho oot aftuh let exuC pruOiesn,rua iarmilyn e vcnraaetltssuh,pe etoshtn eeosr ftes i. m6 t.oe4 - c6ho.y8up restreoc oa0fp. 2cn-hi0aa. 4nw gaeUss
es lation of HC0,- ions in the blood (Cameron 1976).
ru Measurements of gill ammonia fluxes (in fish with urinary
archponal Iatm hmaso nbieae ne xkcnroewtionn f otar kseosm pel aticme et hthroaut gmho stht eo fg tihlles pcaetrhfoertmeresd) obry wsehaollien gb oofdfy t haem cmhaomnibae frlsu wxeitsh ( an ok ncoawthne tveorlsu)m wee oref
w.nrcreseFor pers eraxtStheiernnrc atehl tahmne et hodpeiu pkmoidr tndueenyci tliiynn eftoes lre aiooss nta sen (x Scamhnaiitmnhg ae1l 9we2vi9to)h.l vthees ttwehixmaitstee err.ran Enaanxgl dteep ffrHlonul axlwole wase mwrineme grm otehn eieiana isd nuleecrpvreeeednal sdss evei mnainrtui oaelmfdta c mfnorenooocmnueis an0l tc ytroo.a n tA1ico mten n.tMt hrCea,h taiapnonHdng swoe svri teiehn-r
w onto the land, it might be expected that the corded (6-7) virtually all (199.5%) of the ammonia exists in the
w acid-base regulating ability of the kidney evolved ionized form (NH,+), so loss to the air of the nonionized form
m in concert with other adaptations for terrestrial liv- (NH,) was negligible.
o Measurements of whole animal Na+ flux rates were per-
r ing. We therefore selected for this study two
d f closely related fish, one a strict water breather formed by adding ,,NaCI to the sealed chambers and following
e the decrease in radioactivity and change in total Na+ concentra-
ad (traira, Hoplias malabaricus) and the other a facul- tion at 4-h intervals for 2 h. At the end of the 2-h period, a second
o
nl tative air breather (jej6, Hoplerythrinus uni- aliquot of the isotope was added, 4% CO, was introduced into
w taeniatus), both of which are common in the Ama- the chambers, and after a&-hm ixing period, measurements were
o resumed for a further 2 h. At the end of the experiment, blood
D zon basin. (The jeju breathes air with a modified
ol. swim bladder served by a branch of the coeliac sthaem bplloeos dw. eSrien tcaek tehne f bolro mode asspuerceimfice nrat doifo sapceticvifitiyc rdaiddi onaoctt eivxictyee odf
Zo artery.) Our objectives were to study the steady- 10% of the specific radioactivity of the external medium, influx
J. state acid excretion by the kidney in these two calculations were performed as outlined by Kirschner (1970),
n. species, to assess their capacity to acidify urine, ignoring backflux. External Na+ levels were approximately 0.15
a mM.t-l (representative of the extremely low levels in the
C and to see if there was any response of renal acid
natural environment of these fish) and did not vary greatly over
excretion to acid loading in the blood. the period of the experiments. For the control and the hyper-
capnic period, the four flux measurements were subjected to
regression analysis, and the difference between slopes (rates)
Methods and Materials
for each period compared using analysis of covariance.
All experiments were performed on board the RIV Alpha Measurements of O2 consumption were obtained in non-
Helix during October 1976. Specimens of traira, Hoplias maia- catheterized fish by flow-through respirometry in a blackened
baricus, and jeju, Hoplerythrinus unitaeniarus (both suborder chamber. A thermostatted microelectrode (Radiometer-Copen-
CAMERON AND WOOD
hagen) was used for Po, determinations. In these experiments,
the fish were denied access to the air, so all 0, consumption
occurred from water.
The right set of gill arches from one traira and one jeju of
comparable size were preserved in 2% glutaraldehyde and 3%
formalin in Cortland saline. Branchial dimensions were deter-
mined later by the weighted averages technique of Muir and
Hughes (1969) as modified by Wood (1974).
Analytical Techniques
Sodium concentrations were measured using a flame photo-
meter attachment for a spectrophotometer (Beckman DU-2),
referring samples to a NaCl standard. Chloride analyses were
performed with an amperometric titrator (Buchler-Cotlove). A
micromodification of the method of Solorzano (1969) was used
for the assay of total ammonia concentrations (NH, plus NH,+).
A commercial reagent kit (Sigma 826-UV) was used for lactate
6
1 analyses. Blood and water pHs were measured at the experi-
0/ mental temperature with a microelectrode (Radiometer-Copen-
1
9/ hagen) and a macroelectrode (Fisher), respectively. Total CO,
0 content was determined by the method of Cameron (1971).
n Estimates of Pco, and HC0,- levels in blood were obtained
o
y from pH and total CO, data by use of the Henderson-Hassel-
sit bach equation (Davenport 1974) with appropriate values for
er cuCO, (Severinghaus 1965) and pK' (Albers 1970). A few direct
niv measurements of Pco, in blood, water, and air were made with a FIG.1 . Titration curves for some representative urine sam-
U Severinghaus microelectrode (Radiometer-Copenhagen). Total ples from traira and jeju. Samples were titrated with 0.010 N
r titratable acidity (TA) was measured by titrating a urine sample NaOH back to the blood pH.
e
st back to the blood pH with 0.010 N NaOH, which was standard-
Ma ized with 0.010 N HCI. In some cases where the blood pH was Arterial pHs were unusually high in both species.
c not measured at the time of urine collection, the urine samples This phenomenon was especially pronounced in
M were titrated to the average pH determined from earlier mea- jeju, where the value was significantly greater than
y surements on the same fish, or from measurements on other fish
m by. ocfo nthcee nsatrmatei osnp ewciaess uthnedne rc sailmcuillaarte cdo nadsi tTioAn sp.l Tush et ototatal la rmenmalo Hni+a itne mtrpaeirraa taunrde i(nR aohthne arn Adm Gaazroeny f1is9h7 3a)t. aS cinocmep tahrea pblHe
ss.coe onlcceonntcreantitorant iios nc o(nDsaivdeenrepdo retf f1e9c7ti4v)e.l yT oetqaul aul rtion aNryH ,a+m imono ncioan ccoenn-- oraf tinoe ufotrra tlriatyir a(p iNs )5 3a:t 1 3, 0a°nCd ifso r6 j.e9j1u6 58,9 t:h 1e, cOomHp--aHre+d
archpreonal ustatrimtartmaitoiononn,i afco uerxr aviste tstsh wae sep rNeH Hs ol,+ifg htahtnleyd u strihignemere o(fio~dr,7e a .sc4 as)rhar,oit e wlse naa s ipnt r9Fo9it%go.n o.1 f;U mtroiotnaselt w19it7h0 )2, 4a:n 1d f o3r2 t:h 1 ef otur rgtlrea,y 4li0n:g 1 faonrd thtreo ufrto g(C (aHmoewreolnl
resepersthiaodn aonf inthfleeicr tibounf fpeor incta apta acibtoyu (ts ploHp 6e).8, ato b 7u.0ff. eAr si nadne axp p(BroIx)i mwaa-s e1n97c6e; bReatwndeaelnl jaenjud Canadm terraoinra 1a9p7p3e).a rTsh teo pbHe dduifefe tro-
nrcor calculated as TA divided by the difference between blood and the higher HCO, concentrations in the former, for
w.Furine pH. calculated arterial Pco, values were virtually iden-
ww Results tical in the two species (=5 torr, 1 torr = 133.322
m Blood Composition Pa). Plasma ammonia levels were also higher in
o Concentrations of various ions and pH of the both species than in other teleosts (cf. Payan and
r
f
d blood of resting fish are given in Table 1 for 15 traira Matty 1975). Blood lactate concentrations were
e
d and 17 jeju; these values exhibit some marked dif- low in all fully recovered fish.
a
o ferences from normal teleost patterns. Naf and C1-
nl
w levels were unusually low in both species (cf. Renal Function in Resting Fish
Do Holmes and Donaldson 1969) and there appeared to Recovery from surgery was rapid in these
ol. be a rather large anion deficit. This deficit was species, with urine flow rates stabilizing in a few
o particularly large in traira, where both C1- and hours, and blood pH reaching stable values in 2 to
Z
J. HCO,- values were significantly below the jeju 6 h. Table 2 contains a summary of urine charac-
n. values. Though no analyses were performed, the teristics and urinary effluxes for eight traira and six
Ca blood seemed to have a high protein content, and jeju after at least a 6 hr ecovery following surgical
the volume of TCA (tricarboxylic acid) precipitate implantation of aortic and urinary catheters. There
was large. Anionic proteins could account for the was considerable variability in the concentrations
anion deficit if they were highly acidic and thereby of all measured parameters both within individual
help reduce the ion pumping requirements in the fish and among different fish of the same species.
dilute waters inhabited by these fish. We have no The urinary effluxes were somewhat less variable,
definitive explanation of the anion deficit. since there was a tendency for flows and concentra-
CAN. J. ZOOL. VOL. 56, 1978
TABL1E. Mean blood values (k SE) for traira and jejli after at least
6 h recovery from surgery
Traira Jeju P*
Na 110.4+4.1 (11) 120.4k7.6 (5) NS t
C1- + 72.8k4.9 (11) 87.0k2.9 (8) <0.05
HCO, - 8.73k0.35 (3) 11.97+1.02 (6) <0.05
NH4 0.85k0.17 (12) 0.86+0.09 (10) NS
+
Lactate 0.59k0.40 (3) 1.00 (1) NS
pH 7.78+0.03 (10) 7.87+0.02 (11) <0.02
-0.04 -0.02
NOTE:A ll concentrations in milliequivalents per litre; numbers of animals in
parentheses.
'Student's two-tailed f-test.
?Not significant.
6
1 tions to be inversely related. Urine pH ranged as drawn during the period or urine collection. The
0/
1 low as 4.99 in one 2-h collection from traira, and as consequent reduction of urine volume is shown in
09/ low as 6.40 from one jeju during the resting, re- Fig. 2.
n covered period. Urinary total CO, concentrations
o Partitioning of Acid and Ammonia Excretion
y were always below the sensitivity of the analytical
sit method (i.e. <1 mM-rl), as were urinary urea In addition to the higher urinary excretions of
ver concentrations (<0.5 mM. t-I). NH4+, TA, and ZH+ in traira, there was also a
ni Virtually every parameter was significantly dif- significant difference in the proportion of ZH+
U excretion occurring as N&+ (Table 3; the anomal-
r ferent between the two species (Table 2) except the
e ous data from J10 have been omitted). TA was
st mean flow of urine. Effluxes of NH4+a nd ZH+ (TA
a + relatively more important in traira, though it com-
M NH4+) were significantly different for the two
Mc species if data from J10 were eliminated. This fish prised less than 30% of the ZH+ efflux in either
species. Absolute TA excretion was over five times
y had atypically high rates of TA and NH4+ excre-
b higher in traira than in jeju. Gill ammonia effluxes
m y. tion, which were not seen for any other jeju. The were extremely variable both within individual fish
conl role of the kidney in acid excretion was obviously and among different fish of the same species, but
ss.e o greater in traira, and this difference was reflected in the mean values were comparable in traira and jeju
es all associated parameters: i.e. lower urine pH,
archpronal u hTAig h, Ner& u+ri,n ea nBd IZ, Hhi+g,h aenrd u hriingahreyr nceotn ecfeflnutxraetsi oonf sT Ao f, a(Tbsaoblluet e3 )N. HHo4w+ eexvcerre, tliaorng einly t hbee cuaruinsee , otfh eth fer alcotwioenr
es of total ammonia excretion by the gill was sig-
w.nrcresFor per tNhHaUn4r i+tnr,aaa irnryda l ,Zo tsHhsoe+us.g ohf Nthae+ daantda Cw1-e rwe eerxe threigmheelry i nv jaerjiu- fnwoiafris cb aloentshtsl y st phheaicgnih ee1sr0. %in joefj uth. eT thoeta ml aemanm roenniaal eexxccrreettiioonn
w able (Table 2). Comparisons of the whole animal
Changes in water pH were monitored during the
w Na+ efflux rates in Table 5 with the renal effluxes in
m Table 2 reveal that urinary Naf losses were only ammonia flux experiments. Values fluctuated con-
o siderably from time to time, but the long-term trend
fr about 4% of the total for traira, on the average, and
ed about 10% forjeju. was consistently upward (seven of eight jeju, seven
d of eight traira) at a mean rate of 0.06 pH units per
a Casual observation suggested that the flow of
o hour in both species.
nl urine was intermittent. The hen omen on was di-
w
o rectly observed in traira T12 khich voided urine in
ol. D ffrooumr ' b3u3r stots ' 1d3u8 rsin ign ad 4u-hr aptieornio, da.n Tdh per boudrusctesd r an2g.0e2d, 5 4.l hJ4 4- -J- -4- -
o
Z 0.38, 2.24, and 0.31 ml at intervals of almost exactly
J. 1 h. The catheter in this fish was insertedless than 1 :::: :::: !:: :::: :I:::
an. cm beyond the opening of the urinary papilla. No ~;-r;tjr~r~;:t;;;~:::i~j~jii;~~ij::ji~;~i~;:i: ~~~.~~~~~ii~ii~ii~ii~ij.j~ij~~~i
C comparable observations were made on jeju, but it ::::::::::::I::.:......................................................... .I..:..:..:..:.::..:..:' .:.::..:.:.. :.....................................................:....:.....:. ..: ..:.. .
is our impression that urination is periodic in this ,.., ....................
species also. 2400 .-
An demonstration of the 71 l.M. t
FIG.1. Influence of serial withdrawal ofO.4-ml blood samples
regulating function of the was provided
(indicated by arrows) on the urine flow of jejli 54 (324 g), The
JeJu 54. This fish had Patent aortic and urinary broken line represents mean urine flow for all jejli corrected to
catheters, and a series of 0.4-ml blood samples was that weight (cf. data in Table 2).
n
mea C1-
h
wit h-'
he table, . v/100 g Na +
d in t pequi
use es, H+
a sets Efflux Z
at +
e d H,
6 et N
1 pl
0/ m
1 o
09/ of c
y on mber C1-
www.nrcresearchpress.com by McMaster UniversitFor personal use only. x jejCi after at least h recovery from surgery. Nis the nu6 each fish values shown for Concentrations, pequiv/ml BZ. TA v/ml. NH4 Na pH-' + +
m si ui
fro and peq
d a
de air
wnloa eight tr
Do or
Can. J. Zool. TABLE Mean urinary parameters f2. Flow . Fish N m1/100 h-I g Traira TI1 3 T12 7 T8 5 4 T9 T7 5 4 T13 T15 2 4 T6 a+ SE Jej ti J3 2 5 54 J8 1 6 J9 2 J10 4 Jll Z+SE 'Student's two-tailed t-test. of P tOmitting data J10, < 0.05.
CAN. J. ZOOL. VOL. 56, 1978
TABLE3 . Partitioning of total acid excretion in urine between TA and NH4+, and par-
titioning of NH4+e xcretion between the gill and the kidney. All NH4+ and ZH+ flux data
are expressed as microequivalents per 100 g per hour. TA can be obtained by subtracting
urinary NH4+ from ZH+. Significance assessed using unpaired t-test
% total
Urinarv efflux acid Gill efflux % total
excretion of NH~";e xcretion
NH4 ZH as NH4+ ammonia by kidney
+ +
Traira
TI1 1.74 2.85 61% - -
T12 3.38 4.45 76 61.4 5.2%
T8 3.63 4.95 73 37.3 8.9
T9 5.89 7.27 81 43.8 11.9
T7 2.45 3.49 70 27.4 8.2
6 T13 6.60 8.37 79 63.8 9.4
1
0/ TI 5 1.15 1.95 59 28.8 3.8
1 T6 3.48 5.32 65 25.1 12.2
9/
n 0 x- 3.54 4.83 71 41.1 8.5
rsity o Jej53u 43 11..1921 21..0376 9822 2-3.1 -7.7
e
v 58 1.91 2.08 92 100.6 1.9
ni J9 1.42 1.63 87 49.1 2.8
U
r Jl l 1.59 1.94 82 48.6 3.2
e
st X 1.59 1.82 87 55.4 3.9
Ma P* <0.05 <0.02 <0.01 NS <0.05
c
M *Two-tailed Student's t-test.
y
b Postoperative Acidosis
m y. A brief, but often severe acidosis followed the
conl anaesthesia and surgery necessary to implant
ss.e o catheters in both species. Blood samples taken
es
archpronal u ibmutm peHdi arteetluyr naeftde rt os unrogremrya lh bayd a6 hpH. I no f F7ig.2. t3oa 7t.h6e,
es time course of pH correction is illustrated for sev-
resper eral fish in which the acidosis was particularly pro-
nrcor nounced. The pH depressions were associated
w.F with depressions of blood total CO, content, which
w
w returned to normal over a similar period (Fig. 36).
m The latter indicates an acidosis of largely metabolic
o origin (i.e. displacement of HCO,- by fixed
r
f
d metabolic acid), and this was confirmed by mea-
e
d sured blood l actate levels of 9 to 14 m'M.t?-l im- 0
a
o mediately postoperatively, in contrast with resting 0 4 8 12
wnl levels of < 1 mM . t?-' (Table 1). A slight respiratory Hours After Surgery
Do acidosis (i.e. elevated Pco,) may also have occurred FIG.3 . Time course of arterial blood pH (pHa) and total CO,
ol. in some individuals, but there were no consistent Tco6n, tseonlitd f oclilrocwleins g= a nTalOes;t hoepseina tarniadn sgulergs e=ry j.e Ojlip 5e7n, c siorclilde str =ia tnrgaliersa
o variations in calculated arterial PCO(,P aco,) values.
Z = J5.
J. Data from urinary collections made during this
n. period of metabolic acidosis (i.e. the 6 h following Lactate dynamics during recovery are illustrated
Ca surgery) are summarized in Table 4. There was no by the data of traira T6 in Fig. 4. Note that although
elevation of urinary H+ excretion, and in fact none blood lactate was still considerably elevated at 3 h,
of the means were significantly different from the the urine lactate had returned to nearly control
resting data in Table 2. Lowest urine pH values levels. The blood lactate level at the first sample
during this period were 5.18 in traira and 5.69 in period for T6 was 13.9 mM-e-l, and the control
jeju. In many of the individual fish, there occurred a value was 0.22 mM .[-I. Assuming a blood volume
slight postoperative diuresis, but the variance in of 4% of body weight, and an equivalent lactate
lumped data obscured the trend. space, this 426-g fish would have had a total lactate
0 > > z 8 0 0
d 8 1 6 7 6 9 3 8 2 6 9 9 0
ata an C1- 2.50.60.12.40.00.2 1.00.4f -0.10.46.8 2.42.2f
d
e
s
ween the xes Na + 5.01 0.97 5.35 4.65 0.39 1.06 2.91 f0.95 - 0.30 3.67 11.16 5.04 k3.21
6 of the differences bet Efflu H+ NH,+ 1.27 2.14 1.43 1.86 7.01 4.30 7.89 4.60 3.72 4.77 3.64 2.30 2.94 4.55 k0.60 k1.02 2.45 2.94 1.47 1.37 8.48 10.70 3.03 2.82 3.78 4.54 k1.60 f2.09
0/1 ne
1 o
9/ N
researchpress.com by McMaster University on 0personal use only. ng the first 6 h following surgery. Units as in Table 2. ata in Table 2 are statistically significant (r-test) Concentrations TA NH, Na C1- + + 0.90 1.43 4.70 2.83 0.95 3.40 2.17 1.50 6.30 9.99 12.44 0.38 5.00 7.13 6.95 3.70 4.82 16.03 3.81 0.26 9.34 16.67 7.70 2.14 4.55 9.11 6.30 1.80 1.32 f2.59 f1.48 k0.56 f 1.36 6.87 - - 0.23 2.88 0.04 0.63 4.48 15.93 5.87 0.85 0.21 3.05 13.76 9.10 1.57 7.18 6.75 3.33 1.01 f3.08 k3.81 k2.89 f
m www.nrcFor our jeju durithe resting d BI 0.83 0.46 2.41 2.86 2.31 4.91 2.30 + 0.65 0.65 0.74 3.39 0.44 1.31 f0.70
ro d f
d f an
de ra
Downloa or six trai PH 6.79 5.96 5.18 5.98 5.95 5.74 5.70 +0.29 -0.17 5.80 7.38 6.63 7.17 6.32 +0.63 -0.25
Zool. eters f
Can. J. ry param Flow 0.84 0.42 0.43 0.67 0.23 0.58 0.53 k0.09 0.36 0.47 0.61 0.87 0.58 +0.11 -
a
n
ri
u
n
a
e
TABLE 4. M N Fish Traira TI1 5 TI2 3 T9 1 T7 2 TI3 4 T6 2 R*SE Jeju J4 1 J9 2 J10 4 Jll 3 RkSE
924 CAN. J. ZOOL. VOL. 56, 1978
6
1
0/
1
9/
0
n
o
y
sit
r
e
v
ni
U
r
e
st
a
M
c
M Hours After Surgery
ss.com by e only. ta(honepdFse IinuaG r aai.n nn4add.r yCsf uihllrlaagecndetg racyeties.r ceilnfef slbu, lxor eoisndp etarcantidirv aeu lTryi6n),e (u 4lr2ai6nc tega )tf elfo owcllo,o nwZcHienn+gt raeanftfialouensxs-, artFerIiGal. 5P. cToim, e( ccaolcu0url saet eodf) TafrIot4Mell roEiwa,l i nhpg H o8(np sHeta ),o ft o1te2axl pCerOim,, enantadl
archpreonal us te8hx.3ec 3ee spxsMc oe fsw s2e.3 rI4en peaxm csoreelc.to eIndnd it nht rteah iferi arus,r ti Tn81e h3, ,op lroa osctntoalypte e3 re.a6xt%icor oenf-, hsoylpide rcciarcplneisa .= O jepjeun 5 c6ir, calneds o=p jeejnu tJri4a,n sgolleisd =tri jaenjug lJe5s .= traira T10,
es maximum values of'P~ow, ould all have coincided.
nrcresor per NtioMn .b y the kidney in the first 6.5 h totalled only 3.2 amUmnoidniirae cwtieornea l mfleuaxseusr eodf Ndau+ri nagn da n emt oerfef lusxeevse oref
w.F Hypercapnic Acidosis hypercapnic acidosis (4% CO,, 30 torr) in five traira
w
The response of blood pH, total CO, and PWO, and four jeju (Table 5). The fish were not
w
m (calculated) to 2% CO, (15 tom) is shown in Fig. 5 catheterized, so the figures in Table 5 represent
o for three jeju and one traira. Arterial pH dropped whole animal flux rates. There was a significant
r
d f rapidly, reaching a minimum by about 2 h, and increase in Na+ influx in the jeju, but no other
de stayed constant or increased slightly over the ensu- significant change. This increase in Na+ influx
a
o ing 10 h. Total CO, (largely plasma HC0,-), on the roughly corresponded to the net increase in am-
wnl other hand, gradually increased throughout the ex- monia efflux seen for the jeju, but the latter was not
Do perimental period. PWO,f ollowed a similar trend, statistically significant.
ol. and in three of the fish did not surpass 15 torr until Urinary CH+ efflux was measured during ex-
o 11 h. This was due to the slow time course of Pco, tended hypercapnia (4% CO,) in one jeju and one
Z
J. increase in the chambers after the introduction of traira (Fig. 6). There was a slight drop in ZH+
n. 2% CO,, a fact confirmed by direct measurements excretion in the traira, but a large increase in the
Ca of Pco2i n blood, water, and air. Nevertheless, the jeju, manifested in both TA and NH,+ effluxes. The
experiment did illustrate an active compensation of jeju also had atypically high urinary Na+ and C1-
the respiratory acidosis by HCO, accumulation in losses.
the blood, for pH remained stable or increased
slightly in the face of increasing Pwo,. If compen- Urinary Relationships
sation had not occurred, the minimum values of Complete data sets for both species (all post-
pH, the maximum values of total CO,, and the operative and resting state data except that taken
CAMERON AND WOOD
TABLE5. Whole animal Nat and ammonia fluxes (a* SE) for five traira and four jeju during
control and hypercapnic (4% COz) periods. All fluxes in microequivalents per 100 g per hour
-
Sodium
Ammonia
Influx Efflux Net flux net flux
Traira
Control 27.85k6.15 33.00k3.31 -5.15k4.13 -43.6k5.9
Hypercapnic 32.04k7.79 39.91k7.06 -7.87k3.10 -43.8k5.1
P* NS NS NS NS
Jeju
Control 44.56k0.44 42.69k 1.94 1.87k2.34 -65.4k10.4
Hypercapnic 49.85k1.56 48.2823.04 1.57k3.73 -73.0k10.3
P* <0.02 NS NS NS
6
1 *Covariance analysis for Na+ fluxes; paired Student's t-test for ammonia fluxes.
0/
1
9/
0 both animals, but despite this relationship, urine
n .
o pH still dropped with increasing TA Two relation-
rsity tsrhaiiprsa odfa ptaar:t itchuel nare gimatpivoer tcaonrcree lwateiroen s beeentw oenelyn iunr itnhee
e
v N&+ concentration and pH, and the positive cor-
ni
U relation between urine CI- concentration and pH.
er (Similar interactions for NH4+ and C1- with other
ast parameters of urine acidity are also apparent from
M
Table 6.)
c
M
y
b Respiratory Parameters
m y. Total secondary lamellar surface area was over
conl twice as large in the strict water breather, traira, as
ss.e o in the facultative airbreather, jeju (Table 7). These
es
earchprsonal ujejuF I(uGp6.p .e Rr pesapnoenl,s JeI o If, u 3r1i0n agr)Ty aI anMcdEi da, etrhxa cirreat (iolonw toer h, yTp6e,r4c2a6p ngi)a. in a tasrproeeuactsi e (aTsr eaob hfl iegs h7im )r.ei Sllaaurtci vhpe rh etidogah tt hosaurtyr of afh caaenb a iartcset,ai vst,he e etve emranpi nienbr otahwtee
resperduring hypercapnia) were subjected to correlation air breather, may be adaptations to the frequently
nrcor analysis to test for relationships between variables. hypoxic environment of these erythrinids. The dif-
w.FThe results for several urinary parameters plus ference between traira and jeju was expressed in a
w
w blood pH are shown in Table 6. In jeju, there was a greater total number of gill filaments, a greater
m strong positive correlation between Na+ and CI- weighted mean filament length, and a greater
o concentrations in the urine, but essentially no such weighted mean lamellar spacing in the former;
r
f
d relationship in traira (the weak positive correlation however, weighted mean surface areas of an indi-
e
d here is in fact due to 3 anomalous data pairs out of vidual lamella were virtually identical. Despite this
a
o 49). In neither species were the concentrations of difference in respiratory surface area, routine 0,
nl
w these ions related to flow. consumption (entirely from water) was comparable
Do In traira, parameters of urine acidity (i.e. NH4+, in the two species: jeju, 59.1 & 5.6 (4) ml
ol. TA, ZH+, BI, and pH) tended to decrease as urine O,-kg-l.h-l; and traira, 49.7 + 3.3 (4) (X 2
o flow increased, so that ZHf efflux was independent SE (N)).
Z
J. of flow. However, in jeju, the flow-concentration The observed frequency of air breathing in jej6
n. relationships were less well defined, so CH+ efflux was variable: some animals did not breathe air at
Ca was positively correlated with flow. In neither all, others at intervals as short as a minute. Accord-
species was there a relationship between blood pH ing to Stevens and Holeton (personal communica-
and any parameter of urine acidity. In both species, tion), this variability is reflected in 0, consumption
the two components of urine acidity, NH,+ and TA , data when access to air is provided, resting animals
were strongly correlated with each other (and of taking anywhere from 0 to 50% of their 0, from the
course with 2Hf), indicating that these vary in air. During experimental hypercapnia, the fre-
concert. TA and BZ were also strongly correlated in quency of air breathing noticeably increased,
926 CAN. J. ZOOL. VOL. 56. 1978
TABLE6 . Correlation analysis for urinary flow (m1/100 g . h-I), urine pH,, concentrations (NH4+, Na+, C1-, TA, Hf,
(~.lequiv/ml)),b uffer index (BI, (pequiv/ml . pH-')), ZH+ efflux (pequiv/100 g * h-I), and blood pH (pHb) for traira (14-52
data sets from nine fish) and jeju (14-35 data sets from nine fish)
Flow P H ~ P H ~ NH4+ TA ZH+ BI Na C1-
+
Traira
6
1
0/
1
9/
0
n
y o * * ** * * * * * *
sit ZH+ efflux - -0.36 - +0.42 +0.32 +0.40 +0.32 - -0.36
r
ve Jeju
ni Flow pH,, P H ~ NH4+ TA ZH BI Na C1-
U pH. - + +
er pHb - -
st
a
M
c
M
y
b
m y.
conl
ss.e o
es
ru
archponal * *** *** *** ***
es
resper XH+ efflux +0.35 - - +0.60 +0.73 +0.65 +0.74 - -
nrcor NOTE:O nly significant correlations given; r significant at the 5% level (*), IS, level (**I, or 0.1:Z (***I.
w.F
w TABLE7. Branchial dimensions of a traira, a jejd, and a rainbow trout of
w comparable size
m
o
fr Traira Jejii Rainbow trout?
d
de Weight, g 374 395 340
oa Total number of filaments 3162 201 8 1672
nl Filament length, mm* 5.69 4.53 7.56
w
Lamellar spacing, no./mm* 58.66 50.09 39.03
o
D Total no. of lamellae 1 055 098.0 457 906.0 493 509.0
ol. Lamellar surface area, mm2* 0.2094 0.2163 0.1764
o Total lamellar surface area,
Z mm2/g body weight 591 25 1 256
J.
an. *tWWoeiogdh t1ed9 7a4v.e rages.
C
though it remained variable, and was not precisely large extent, this variability may reflect differences
recorded. in the condition of experimental animals. While an
effort was made to select fish in good condition, all
Discussion
the animals used had suffered some degree of abra-
Branchial and Urinary Fluxes sion or scale loss during capture and handling. As
Urine flows and Naf and Cl- loss rates were urine flows in fresh water reflect total body per-
variable in both traira and jeju (Tables 2, 4). To a meability (Hickman 1965), somewhat lower urine