respiratory responses to long-term temperature exposure in the box turtle, terrapene ...

7/29/2019 Respiratory Responses to Long-Term Temperature Exposure in the Box Turtle, Terrapene ornata

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J. Comp. Physiol. l3l, 353 359 (1979)

Glass, l4ogens L., James I{. Hicks and }Iarvin L. Riedesel . L975.Respiratory responses to long-term temperature exposure in thebox turtle, Terrapene ornata. J. Cornp. physiol. 111, 353-359.

of Zoophysiology, University of Aarhus. DK-Denmark

Journalof ComParativePhysiology' Bit) by Springer-Verlag 1979

charges on proteins (Reeves, 1972). Thercfore, theoptimum pH of various key enzymes increases withdecrease of body temperature (Hazel et ai., 1978).In fresh-water turtles, Pseudemys sp. and inIguana iguana the change of pH with temperature iscaused by adjustments of the air convention require-ments, i.e. the ratio of ventilation volume, ml BTPSto O, uptake, ml STPD; i"lto. (Jackson, 1971;Kinney et al, 1977 ' Giordano and Jackson, 1913).Alveolar Pqo, is related to the relative alveolar venti-lation (VolVro,) by the equation,

Poro'the ratio i'u1ito.by the equation

(t"l to ) - (iol Vd - R eRT f P,1.o.as V.o.:Rn'Vo. and Vu-to:l^ln these equations Vr:Iotal ventilation volume, Z,: dead space ventil ation, Vo: alveolar ventilation,Rr: the pulmonary gas exchange ratio, R: the gasconstant, and T:the absolute temperature. Increaseof air convection requirements lowers alveolar (andarterial) P.o, which in turn increases plasma pH asshown by the Henderson-Hasselbalch equation:

HCO;pH : pK -1 log:- -^- " (3)1.' L-co.where a:solubility coeflicient for CO, in plasma.The increase ol pH and air convection require-ments with cooling has been described to occur withinhours (Jackson, 1976). However, long-term or sea-sonal effects of temperature on ventilation and airconvection requirements remain unknown. This is thereason for undertaking a study of ventilation. gasexchange, and end-tidal P6,. and P.o. in hibernatingand active box turtles, Teruapene ornata ornota.

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* Department8000 Aarhus C.

Respiratory Responses to Long-Term Temperature Exposurein the Box Turtle, Terrapene ornat&Mogens L. Glass*, James W. Hicks, and Marvin L. RiedeselDepartment ol Biology, University of New Mexico, Albuquerque. New Mexico 87131, USAAccepted March 9, 1979

Summary. ln late February, seven box turtles werecollected with body temperatures between J and9 "C.Ventilation, gas exchange and end-tidal Po. and P6..were recorded at 5, 10, 15 and 25'C, the animalsbeing at each temperature for 2 to 3 weeks. Therewas a pronounced diurnal rhythm of breathing fre-quency at all temperatures. At 5 bC the mean 24-hfrequency was only 3.7 breathsh-1. At 15'C thefrequency was 16 times higher with a l7-fold increaseof ventilation. Oxygen uptake only changed from 3.4lo l2.l ml .kg 1 .h 1. Consequently, the ratio (venti-lation, ml BTPS/Ot uptake, ml STPD) increased from12.5 ar 5 'C to 48 at 15 oC, but decreased lo 24 at25 'C. The decrease of this ratio during cold exposurecontrasts with an increase of the ratio during coolingearlier reported for fresh water turtles, Pseudemys.Cutaneous COt elimination was important at lowtemperature. This caused a decrease of the pulmonarygas exchange ratio so that end-tidal P66, remainedlow at 5'C in spite of an end-tidal Ps, of only 54Torr.

IntroductionIn many ectothermic vertebrates and in some inverte-brates studied, a constant relative alkalinity (i.e.OH /H+ ratio) is maintained when body temperaturechanges (Rahn, 1966; Reeves, 1972; Howell andRahn, 1976). With decrease of body temperature, theplasma pH tends to increase in parallel to pN, thepH of neutral water for which pH:pOH. However,plasma pH is greater than pN, the difference beingspecies dependent. The constant OH /H+ reflects aregulation of the ratio between negative and positive

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Materials and MethodsSeven ornate box turtles (Terrapene o. ornata) were collected inthe fall and hibernated within an outdoor enclosure. In Februarythe turtles were removed from hibernation sites with a body tempei_ature of 7 to 9'C and transferred to an environmental chamberinitially set at 5 "C. Weights ranged from 224 to 390 g (_i:316 g).Experiments were performed in sequence at 5, 10, 15 and 25 "C.The animals were kept at each temperature for 2 to 3 weeks. Theturtles were fasting during all measurements, but were initiallyfed after transfer to 25 'C. Water was available at all times.The experimental setup is shown in Fig. 1. Ventilation wasmonitored by a plethysmographic technique. A closefitting, gas_tight mask was constructed for each turtle. For details see Glassetal. (1978). The mask was skintight except for a funnel_shapedextension surrounding the nares (dead space 0.3 ml). The maskwas lastened and sealed around the turtle's head with cvanoacrvlateand last setting epoxy glue. Leaks uere prevented b! ll,spectingthe seal through the clear mask material. The funnel-shaped exten_sion litted tightly and was glued into a hole in the wall of theplexiglass chamber. The bottom of the chamber was senled withvaseline. As the turtle's body w:rs sealed into the plexiglass chamber,changes in body volume caused by inspiration or expirationresulted in chamber pressure changes which were monitored bya Valydine diflerential pressure transducer (Mp45-1) with a Valy-dine transducer indicator (CDl2), and recorded with an E & MPhysiograph (E & M Instrument Co. Inc., Houston, Texas). Cali_bration olthe system was achieved during breath-holds by injectingor withdrawing known volumes. Leaks in the mask would occasion_ally develop, but were detected as a decrease in the amplitudeol calibration signals.

Catheter tubing placed within the funnel at the nares permittedsampling of end-tidal oxygen and carbon dioxide. A Neubergerpump pulled gases through an 53A oxygen analyzer (Applied E,lec-trochemistry) or a LB-1 COr-analyzer (Beckman Instruments). Atlow flow rates variations in pump activity were reduced by a flowstabilizer vessel (Fig. l). As expired flow rates were low and tidalvolumes small (l 7 ml) several precautions were taken to assurethat end-tidal Pn, and P.o, wcre obtained. The extension ol themask served to funnel the expired gas to avoid contaminationof the sample. Furthermore, sample flow rates werb reduced to

Fig. 1. Schen'ratic drawing of theexperimental setup

40 50ml.min '. The small tidal volune only allowed analysisol one gas at any time (Pn. or- P.,,,). Care was taken to keepdead space at a minimum in the sample inlets of the analyzerpick-up heads. Calibration ol the gas analyzers was perlormedwith dry room air or dry commercial standard calibration gases.Sample flow rates were the same during calibrations and measure-ments. With low flow rates we obtained alveolar plateaus for bothO, and COr. As end-tidal gas pressures and mean zrlveolar partialpressures were very close, values for end-tidal p., and p.u, weretaken to represent alveolar values. Only end-tidal gas pressurescould be recorded at the lower recording speeds which were neces-sary due to low breathing lrequencies at 1ow temperatures. End-tidal P., or P.,,, was continuously recorcled lor 24-h intervals(Coleman Recorder, Hitachi 165). From the recording it was estab-lished that the inspired gas was virtually room air in spite ofa dead space of0.3 ml in the funnel. This was due to the continuouspulling of g:rses from the region of the nares.Total Zo, or Z.u, was obtained by placing the turtles in glassjars sealed with vaseline. A small rubber tube inserted throughthe lid was opened to obtain samples lor gas analysis. Sampleswere taken repeatedly over 2.{-h periods at intervals that resultedin changes of O, or CO, concentrations of approximately l7o.Oxygen upt:rke was calculated as a mean value for a 24-h period.Cutaneous gas exchange was measured by sampling gases fromthe plexiglass chamber. The lace mask assured that expired gasdid not enter the plexiglass chamber. It is also important thatfumes from the glues used for sealing do not interfere with thereadings of gas analyzers. The plexiglass chamber was flushed withroom air 24 h alter gluing and samples were taken 24 h later.As breathing frequency showed a pronounced diurnal rhythm,ventilation was calculated as a mean value lor a 24 h period. Thebreathing frequency was very low and is therefore unconventionallyreported as breaths.h 1. The ventilations reported in the followingare based on inspired volumes. Expired volumes were less dueto cutaneous carbon dioxide elimination. pulmonary gas exchangeratios were calculated lrom the equation (Rahn and Fenn, 1955),Ro:(Pr.o,)(l -Fro,)l(Pro,-PA6, -Pr.6, 4..) 14)where ,4 : alveolar (end-tidal)" 1 : inspired and ,Fr., is the fractionalconcentration of inspired oxygen. Alveolar ventilition was calcu-lated from the equation,


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M.L. Glass et al.: Respiratory Responses to Temperature in the Box TurtleVA- REV},(RTlPAco),where R:the gas constant equal to 2.785 mlBTPS.Torr."K 1 .ml STPD 1 and I is the absolute temperaturein "K. Dead space was calculated from the equation. tr/r-(.Vt-VoV.Calculation of dead space provided a test that measured totalventilation and calculated alveolar ventilation were in reasonableagreement. As alveolar ventilation was calculated from end-tidalPo, and P6n. (Eq.4 and 5) and oxygen uptake, the comparisonalso provided an additional method of testing measurements ofend-tidal gas pressures.

ResultsThere was a pronounced diurnal rhythm in breathingfrequency. ln extreme cases at 5'C breathing ceasedcompletely during the night (8 t h) whereas thehighest frequency was recorded in the morning. Theturtles had individual characteristics as to patternsof breathing, the typical alternatives being singlebreaths interrupted by regular periods of breath hold-ing or series of breaths separated by longer periodsof apnea. Inspirations without expirations wouldsometimes precede series of breaths. This probablyrelates to shrinkage of the lungs with breath holding(Mithoefer, 1964). The mean 24-h breathing fre-quency was only 3.7 breaths.h 1 at 5 oC, but at 15 'Cthe frequency was 16 times higher whereas tidal vol-umes changed little with temperature (Fig. 2). Ventila-tion, therefore, changed roughly in proportion to thebreathing frequency (Fig. 3). Oxygen uptake at 15 oCwas 3.7 times higher than at 5'C (Fig. 4). Becauseof the larger effect of temperature on ventilation thanoxygen uptake, air convection requirements increasedfrom 12.7 ml BTPSiml STPD at 5 'C to 48 ml BTPS/ml STPD at l5'C (Fig. 5). Oxygen extraction (Eo,)can be estimated from the relationship,Eo.:(RTlP,o)(.Vo,lV,:) (1)where 1:inspired. The low ir,li,o. at 5 oC cor-responds to an oxygen extraction of 0.55, i.e. 55% ofthe inspired oxygen content.Changes of end-tidal P,r, with temperature reflectchanges of oxygen extraction (Fig. 6). At 5 'C meanend-tidal Po, was 55 Torr, but values as low as 15to 20 Torr were recorded. Assuming a pulmonary gas-exchange ratio of 0.75, a mean end-tital Po. of55 Torr corresponds to a mean end-tidal P6e, of60 Torr. Surprisingly, end-tidal P.,r. was only 16 Torr(trig. 6), which was not different from the value at15'C. This was due to extrapulmonary carbon diox-ide elimination which was most important at the lowtemperatures. ln contrast, extrapulmonary oxygen

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5rot52025TEMPERATURE,'CFig. 2. Tidal volume and breathing frequency changes with temper-ature; -t+SE; n:4 al 5 and 25 "C, r-5 at 10 and 15'C

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356

TEMPERATURE, "CFig.4. Changes in oxygen uptake and carbon dioxide eliminationwith temperature; ;+SE; n-4 at 5 and 25 "C, n:5 at 10 and15'C

TEMPERATURE, "CFig. 6, Changes of end-tidal Po, and P..u, with temperature; r * SE ;n:4 at 5 and 25 'C, n:5 at 10 and 15 'C

M.L. Glass et al.: Respiratory Responses to Temperature in the Box Turtle

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Fig. 5. Air convection requirements and oxygen extraction changeswith temperature; x+SE; n:4 at 5 and 25"C, n:5 at l0 andt5'c

,/'aFig.7. Changes of pulmonary and total gas exchange ratios withtemperature; -+SE; n:4 at 5 and 25'C, n-5 at 10 and 15'C;Rl"t"':Total Gas Exchange Ratio; Rr:pulmonary Gas ExchangeRatio

aFzL!L!E -to) LIO-O FIFLd colcDcr -l-= EtFo^ot.9gizE.a

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M.L. Glass et al.: Respiratory Responses to Temperature in the Box TurtleTable l Extrapulmonary COr-elimination as a percentage of totalCO2-elimination at various body temperatures, mean t SE

Temperature ("C)15

Cutaneous V.u,(%) 76 (+8.0) 49 (+3.5) 23 (t1.8) 35 (+6.5)

was pronounced at 5 'C (trig. 7) at which temperaturecutaneous CO, elimination was 3/o of the total COtoutput (Table 1). At l5'C, only 1/o of the CO2 elimi-nation occurred through extrapulmonary exchange.The total gas-exchange ratio increased from 0.76 at5'C to 0.91 at l0'C which is similar to effects ofheating in birds and mammals (Chaffee and Roberts,1971). On transition from 10 to 15'C, there was atransient decrease in the total gas-exqhange-ratio' Theratio increased and reached a steady level after aweek. Transfer from 10 to 15 oC caused other tran-sient respiratory responses. Initially, end-tidal Pco.was low, 9 + 3 Torr (t + SD), compared to a meanof 14 Torr two weeks later. The low P.o. was causedby an increase of air convection requirements tovalues ranging from 48 to 124 ml BTPS/ml STPD.After two weeks at 15'C VrlZo, was close to 48 mlBTPS/ml STPD for all the box turtles.Calculated dead space did not change significantlywith temperature. The mean of all calculations isVo:2.04 ml'kg 1 + 0.4 (SE, I/: 18).DiscussionDuring winter, box turtles remain in shallow burrows(20 45 cm deep), where they tolerate body tempera-tures close to the freezing point with 5 oC as a fre-quently recorded temperature. They remain inactiveduring winter and will not emerge in the spring untilthe body temperature is at least 15'C (Legler, 1960).During summer the preferred body temperature ofbox turtles is close to 30 oC, but above 35 'C a varietyof thermoregulatory responses will occur includingexcessive saliva production (Sturbaum and Riedesel,t97 4).The studies on respiration in Pseudemys sp.recorded higher oxygen uptake than for T. ornata(Jackson, 1971; Kinney et al., 1977). Gatlen (19'74)also reported a generally lower standard metabolicrate in T. ornala than in Pseudemys scripta. The effectsof cold exposure on ventilation in Z. ornata deviatemarkedly from the effects of cold on breathing inPseudemys scripta (Jackson, 1971). Whereas meanventilation in P. suipta changed little with tempera-tures ranging from 10 to 35 "C, T. ornata increased

357

ventilation 17-fold when body temperature increasedby only 10'C from 5 to 15'C. Kinney etal. (1971)reported an exponential increase of ventilation withincrease of body temperature in the turtle, Pseudemysfloridana, but ventilation was predicted to increaseby a factor of less lhan 2 with an increase of bodytemperature from 5 to l5 "C.Likewise, the increase of air convection require-ments.with temperatures from 5 to 15 oC contrastswith temperature dependence of this ratio inPseudemys sp. At 10'C the ratio was 76.2mIBTPS/ml STPD in P. suipta (Jackson, 1971) and waspredicted to be 66 ml BTPSiml STPD in P. .floridana,compared to 21.9 ml BTPS/ml STPD in T. ornata.In the Henderson-Hasselbalch equation (Eq 3),the values for pK and ry for a given animal at agiven temperature are constants whereas HCO3 andPs6, c?n be regulated. Changes of end-tidal Pg6. r-sult from alterations of the relative alveolar ventila-tion (Eq. 1). lon exchange in the kidneys or intestinescould regulate the plasma bicarbonate ion concentra-tion, but most evidence favour a constant HCO3-with temperature in reptiles (Howell and Rahn, 1976).Therefore, active pH regulation during temperaturechanges is generally thought to be mediated throughadjustment of the relative alveolar ventilation. Thismodel appears to be valid for fresh water turtles(Pseudemys sp.) exposed to temperatures in the range10 to 35 oC for hours or days, but in the 5 to 15 "Crange Z. ornata air convection requirements increasedwith temperature (Fig. 8). The pronounced decreasesat low temperatures of both breathing frequency andair convection requirements in T. ornata correlatewith seasonal cold exposure and inactivity. A lowair convection requirement during hibernation is anadvantage in terms of energetics because the oxygencost of breathing in percent of total 26, is a constanttimes the VulVo. ratio (Kinney and White, 1977).A low ventilation volume in hibernating box turtleswill also serve to limit respiratory water loss. Theadvantages of saving energy and body water mayconflict with maintenance of a constant OH /H+ asend-tidal P66, wos relatively constant between 5 and15 'C, but measurements of plasma pH are necessaryfor an evaluation of the problem.ln the range of temperatures within which 7. or-nata is active the values for air convection require-ments agree well with previous studies on chelonians(trig. 8). The differences between effects of lowtemperature on respiration of T. ornata andPseudemys seems explainable. Only this study reportson ventilation and Or-uptake of a reptile at low bodytemperature associated with inactivity during the win-ter season. Other studies involved measurements overhours or days. In active P. scripta and inverse rela-

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5 ro 15 20253035TEMPERATURE,9CFig'8. Air convection requirements reported lor various repllles (Chetonions, Saurians and, OptLidians); rGlass etal., present study;Jackson (1971); 3calculated from Kinney et al. (1917);1wo;d et u,t. 1tolll; sGiordano and Jackson (1973); 6Nielsen iflorl; tB.;;;t(1973); 8calculated from Dmi'el (1472); ',GIass and Johansen (1976)

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tionship between Vrl Vo. and body temperature wasrecorded during transient temperature changes (Jack-son, 1971; Jackson and Kagen, 1976). Respiratoryresponses to low temperature may not be immediateor the applied temperature range may have been in-sufficient to detect a frequency decrease at low tem-perature in P. scripta.Unfortunately, an inconsistent picture emergesfrom studies on air convection requirements versustemperature when non-chelonian reptiles are consid-ered. In the saurians lguana iguana ald Lacerta sp.,air convection requirements increase with cooling, butin Sauromalus this ratio decreases with lower tempera-tures. In varanids the ratio remains constant between25 to 35'C (Fig. 8). In ophidians air convection re-quirements change little with temperatures between20 and 30'C, but tend to decrease at higher tempera-tures (trig. 8). Consistency and better agreement withthe relative alkalinity concept would probably resultfrom experiments including: l) a wide range of tem-perature consistent with the ecology of the reptiles,2) measurements of the time courses of respiratoryand other regulatory responses to temperature, 3)measurements of plasma bicarbonate ion concentra-tions and pH along with air convection requirements.The feeding status of a reptile can influence bothpH (Coulson and Hernandez, 1964) and end-tidalP"o. (Glass et a1., in press). This largely neglectedaspect of reptilian physiology may also aicount forsome inconsistency. Moreover, specialized modes of

life will influence respiratory responses to temperatureand can cause deviations from otherwise commonrules. In the aquatic snake Ac'rochordu,s .jauanicus airconvection requirements were nearly the same at 20and 30 'C (Fig. 8). In this snake ventilation is primar-ily adjusted to meet oxygen demands, as a large frac-tion of the COr-elimination takes place through theskin (Standaert and Johansen, 1974; Glass and Johan-sen, 1976). In the lizard Varanus exanthematicus, arte-rial pH did not change between 25 and 35'C andthe Vnl Vo.-ratio was virtually temperature indepen-dent (Wood et al., l9ll, Fig. 8). Varanid lizards areunusual among reptiles in being " mammal-like " inmany leatures (Bennett, 1973; Millard and Johansen,1974; Wood et al., 1971; Glass et al., in press).The temperature effects on end-tidal P1r, in T.ornota are similar to changes of ventricular Po, inP. scripta (Frankel et al., 1966) although the ventricu-lar P6. values are generally lower. Whereas ventricu-lar P6e, in P. scripta increased with temperaturesfrom 5 to 35'C, the end-tidal P"o, of T. ornata didnot increase until body temperature exceeded 15 oC.Decrease of the pulmonary-gas-exchange ratio (Rs)with low temperature reflects the nature of cutaneousrespiration. As early as 1904 Krogh pointed out thatextrapulmonary gas exchange tends to be constantin spite ol large variations in total gas exchange. Con-sequently, if total exchange decreases, the extrapul-monary exchange will become relatively more impor-tant (Table l). Cutaneous respiration lowers blood

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M.L. Glass et al.: Respiratory Responses to Temperature in the Box TurtleP66, and conversely, as stated by Dejours (1915),"the more an animal is a pulmonary breather, thehigher is its blood CO, pressure". Therefore, at lowtemperatures end-tidal Ps6. refiiained low in spiteof a low end-tidal Po,. As total gas exchange increaseswith temperatures from 5 to 15'C, the pulmonary-gas-exchange ratio (Ru) approaches the total-gas-ex-change ratio (R.totor). At 25 'C, the difference betweenthe total and the pulmonary gas exchange ratios isgreater than at 15 oC corresponding to an increaseof the importance of extrapulmonary gas exchange(Table 1). This may correlate with an increase of end-tidal P.o, with increase of temperature from 15 to25 "C as increased blood P.,r, promotes cutaneousCOr-elimination (Crawford and Schultetus, 1910).Cutaneous gas exchange is common in aquatic rep-tiles, but may also occur in terrestrial species (Stan-daert and Johansen, 1914). The values measured at15 and 25 oC for T. ornata are rather high. Experimen-tal error may have given an overestimate of cutaneousCOr-elimination. It is nevertheless certain that cuta-neous COr-elimination is very important in prevent-ing high blood P.,r. in T. ornata at iow temperatures.The respiratory dead space volume (V") of2.04+0.4 ml.kg-t (SE) in T. ornata is lower thanfor Testudo graeca (2.6 ml'kg t), but larger than aVp of 0.6 ml .kg-1 in P. scripta (Crawford et a1.,1976). In Varanus exanthematicus Vj decreased withlow temperature because a decrease of breathing fre-quency increased the time available for intrapulmon-ary diffusion of gases (Wood eI al., 1977). The tem-perature-independent values for Ve rn T. ornata areprobably due to a generally low breathing frequency.Mogens L. Glass was supportcd by a lellowship awarded by ThcUniversity ol Aarhus, Denmark.The authors are indebted to Professors Stephen C. Wood andKjell Johansen for encouragement and support, and to RaymondB. Smith for making the drawing in trig. l.ReferencesBennett, A.F.: Ventilation in two species of lizards during restand activity. Comp. Biochem. Physiol. 46A, 653 671 (\973)Chaffee, R.R.J., Roberts, J.C.: Temperature acclimation in birdsand mammals. Ann. Rev. Physiol. 33, 155 202 (1971)Coulson, R.A., Hernandez, T.: Biochemistry of the Alligator: Astudy of metabolism in slow motion. Baton Rouge: Lor.risiana

State Univ. Press 1955Crar'vford, E.C., Jr., Gatz, R.N., Magnussen, H.. Perry, S.F., Pii-per. J.: Lung volumes, pulmonary blood flow and carbonmonoxide dilfusing capacity of turtles. J. Comp. Physiol. 107,169 178 (1976)Crarvford, E,.C., Jr., Schultetus, R.R.: Cutaneous gas exch:rngein the lizard Saurontalus obesls. Copeia 1910, 179 180 (1970)Dejours, P.: Principles of comparative respiralory physiology. Am-sterdam: North-Holland Publishing Company 1975Dmi'el, R.: E,fflect of activity and temperature on metabolism andwater loss in snakes. Am. .T. Physiol .223,510 516 (1972)Frankel, H.M., Steinberg, G., Gordon, J.: Effects of temperature

on blood gases, lactate and pyruvatescripta elegan,s, in vivo. Comp. Biochem

359

in turtles, Pseudemys. Physiol. 19,219 283( l e66)Gatten, R.E.: Effects of temperature and activity on aerobic andanaerobic metabolism and heart rate in the twlles Psettdemysscripta and Terrapene ornuto. Comp. Biochem. Physiol. 48A,619 648 (1974)Giordano, R.V., Jackson, D.C.: The eflect of temperature on \enti-lation in the green iguana. Comp. Biochem. Physiol. 45,235 238 (1973)Glass, M.L., Johansen, K.: Control of breathing in Acrochordusjaranicus, and aquatic snake. Physiol. Zool. 49,328 340 (1976)Glass, M.L., Wood, S.C., Johansen, K.: The application of pneu-motachography on small unrestrained animals. Comp. Bio-chem. Physiol. 594,425'427 (1918)Glass, M.L., Wood, S.C., Hoyt, R.W., Johansen, K.: Chemicalcontrol of breathing in the lizard, Varanus ex(mthemati(:us.Comp. Biochem. Physiol. (in press) (1979)Hazel, J.R., Garlick, W.S., Scllner, P.A.: The ellects of :rssaytemperature upon the pH optima of enzymes from poikilo-therms: A test of the imidazole alphastat hypothesis. .T Con]p.Physiol. 123,9t 104 (1918)Howell, B.J., Rahn, H.: Regulation of acid-base balance in reptiles.In: Biology of the Reptilia, Vol. 5, Physiology A. Gans, e ,Dawson, W.R. (eds.), pp. 335 365. London: Academic Pressr91 6Jackson. D.C.: The effect of temperature on ventilation in theInrrle, Pseudeml,-s scripta elegun,s. Resp. Physiol. 12, 131 140(le7l)Jackson, D.C.. Kagen, R.D.: Elfects of tempcrature transientson gas exchange and acid-base status of turtles. Am. J. Physiol.230. 1389 1393 (1976)Kinney,.l.S., White, F.N.: Oxidative cost olventil:rtion in a trLrtle,PseLrdemys.floridana. Resp. Physiol. 31,327 332 (1977)Kenney, .T.S., Matsuura, D.T., White, F.: Cardiorespiratory effectsof temperature in the turtle. Pseudem,vs florirlana. Resp. Physiol3r, 309 32s (1977)Krogh, A.: On the cutaneous and pulmonary respiration ol thefrog. Scand. Arch. Physiol. 15, 328-419 (1904)Legler, J.M.: Natural history ol the ornate box turtle, Terrapeneornctta ornata. Agassiz. Univ. Kan. Publ. Mus. Nat. Hist. ll,527 669 (\960Millard, R.W., Johansen, K.: Ventricular outflow dynamics inthe lizard Varanu.s nilolictts: Responses to hypoxia. hypercarbiaand diving. J. Exp. Biol. 60, 871 880 (1974)Mithocfcr, J.C.: Breath holding. In: Handbook of physiology.Sect. 3, Vo1. Il, Respiration. Fenn, W.O., Rahn, H. (eds.), pp.l0ll 1025. Washington, D.C.: Am. Physiol. Soc. 19621Nielsen, B.: The regulation of the respiration in leptiles. I. Theeffect of temperature and CO2 on the respiration of lizards(Lacerta). J. Exp. Biol. 38, 301 314 (1961)Rahn, H.: Gas transport from the external environment to thecell. In: Ciba Foundatior.r Symposium on the Developmentof the Lung. deRench, A.V.S.. Porter, R. (eds.), pp. 3 23. Lon-don: J.A. Churchill Ltd. 1966Rahn. H., Fenn, W.O.: A graphical analysis ol the respiratorygas exchange. Washington, D.C.: Am. Physiol. Soc. 1955

Reeves, R.B.: An imidazol alphastat hypothesis for vertebrate acid-base regulation; tissue carbon dioxide content and body temper-ature in bnllfrogs. Resp. Physiol. 14,219 236 (1972)Standaert, T., Johansen, K.: Cutancous gas exchange in sntrkes.J. Comp. Physiol.89,313 320 (1974)Sturbaum. B.A., Riedesel, M.L.: Temperature regulation responscsol ornate box turtles, Terrapene ornato, Io heat. Comp. Bio-chem. Physiol. 48A,521 538 (1974)Wood, S.C., Glass, M.L., Johansen, K.: Elfucts of temperatureon respiration and acid-base balance in a monitor lizard. J.Comp. Physiol. 116,287 296 (1971)

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