Respiration

Physiology

VENTILATION,

(1976) 21, 369-377; North-Holland

GAS EXCHANGE AND METABOLIC OF A SEA TURTLE’

HENRY D. PRANGE Physiology

Section,

Indiana Universtiy

of Biomedical

Publishing Company,

and DONALD

School of Medicine,

Sciences, Brown University,

Amsterdam

SCALING

C. JACKSON

Bloomington,

Providence,

Ind. 47401, and Division

of

R. I. 02912, U.S.A.

Abstract. Ventilation of green turtles (Chelonia my&s) was affected by the position in which the animal was placed: supine animals breathed slowly (0.07 breaths/min) and deeply (8.0 L/breath); prone animals breathed more rapidly (0.43 breaths/min) and more shallowly (3.5 L/breath). From the respiratory exchange ratio and other indicators it appears that green turtles hyperventilate during exercise and hypoventilate during recovery. 0, consumption of the resting sea turtle (0.024 L. kg- ’ h- ‘) is similar to that of other large turtles. Maximal 0, consumption (0.25 L. kg- 1 h- ‘) is greater than that of other large turtles. Minimal 0, consumption scaled in proportion to the - 0.17 power of the body mass of green turtles over the range of 0.030 to 141.5 kg. The maximal 0, consumption scaled in proportion to the - 0.06 power of body mass for the same range of body masses. Oxygen consumption Ventilatory requirement

Allometric relations Breathing pattern Muscular exercise

The green turtle engages in sustained activity in the water and on land. Its periodic migrations from feeding grounds to breeding beach may involve an open water journey of as much as 2400 km each way (Carr and Goodman, 1970). At the breeding beach a female must crawl laboriously across the sand to excavate its nest and lay eggs. This process is repeated several times during the breeding season. In the environments in which they are active, opportunities for aerial gas exchange are either constantly available (on land), periodically available (while swimming) or not available at all (while diving). Green turtles have been shown to be capable of continuous aerobic activity while swimming (Prange, 1976) and to be tolerant of anoxia while diving (Berkson, 1966). This variety of modes of activity and of environments suggests that the gas exchange capabilities of the green turtle are highly adaptable and worthy of investigation. Furthermore, previous investigators (Hutton et al., 1960; Hughes et al., 1971) have suggested that the metabolism of turtles may not follow the scaling relationship to body mass commonly found in other vertebrate groups. Since data on the oxygen Accepted for publication

8 May 1976.

1 This study was supported in part by NSF grants GA-36638 to A. Carr and GB-42578 to D. C. Jackson. 369

370

H. D. PRANCE AND D. C. JACKSON

consumption at rest and during activity were already available for smaller green turtles (Prange and Ackerman, 1974; Prange, 1976), similar data from adults of the species which could be obtained from this study would allow a further evaluation of the generality of this seemingly anomalous scaling of metabolism among chelonians.

Materials and methods Adult, female green turtles (Chelonia mydas) were studied during August, 1975 at Tortuguero, Costa Rica, a major site for green turtle breeding and nesting in the western Caribbean. Two animals, with body masses of 127 and 142 kg were captured on separate nights, in each case after nesting had been completed. Ventilation and respiratory gas exchange were measured on each animal by analysis of the volume and composition of expired air. A funnel-shaped mask, constructed from a 2000 ml plastic flask from which the bottom had been removed, was placed over the turtle’s head. A plastic bag, taped to the large end of the flask and to the turtle’s neck, provided an airtight seal. A Douglas valve (Collins, P-3 1l), connected to the opening at the small end of the flask, served to separate inspiratory and expiratory flow. The inspiratory side of the valve was open to the air while the expiratory side was connected, via large bore tubing, to a 6-L spirometer (Collins, P-802) for measurement of tidal volumes. For tidal volumes which were regularly larger than 6-L the tubing was connected to a Douglas bag which was subsequently emptied into the spirometer in increments for measurement. The spirometer volume after each breath and the time when the breath occurred were recorded. The spirometer was then emptied into a 30-L Douglas bag and prepared for the next breath. The usual breathing pattern of the resting green turtle, which consists of single breaths at well-spaced intervals, allowed reliable sampling with this technique. From these measurements the mean tidal volume, expired respiratory minute volume and respiratory frequency were calculated. After a series of breaths had been collected in the Douglas bag, the tilled bag was replaced. The gas in the tilled bag was analyzed for oxygen and carbon dioxide with a Scholander 0.5 cc respiratory gas analyzer. Ambient air was also analyzed to determine inspired air composition. Respiratory CO, production was computed from the product of expired volume and the difference between the fractional concentrations of CO, in the inspired and expired air. The computation of oxygen consumption was corrected for the calculated difference between the inspired and expired volumes, based on the change in the fractional concentration of nitrogen. Ventilation and gas exchange were measured on turtle A (127 kg) while it rested in both the supine and prone positions. The same measurements were made on turtle B (142 kg) while it rested in the prone position and while it crawled on a flat, grassy area for about 45 minutes.

H. D. PRANCE

Ambient air temperatures 27 “C.

371

AND D. C. JACKSON

during-the

measurement

periods ranged from 23 to

Results and discussion VENTILATION

I.

Supine vs prone

There was a marked difference in the breathing pattern of turtle A according to its position. When supine, tidal volumes were large (range for five consecutive breaths : 6.4 to 10.3 L) and respiratory frequency was low (mean value: 0.07 breaths/min). In their study of the respiratory mechanics of a supine adult green turtle, Tenney et al. (1974) recorded tidal volumes of a similar magnitude and suggested that the largest measured represented the total lung volume of the animal. “E

I

4r



33 E $2 m ?I -Ib 0

Fig. 1. Respiration after during

transport which

0

-_

of green turtles.

Below, a plot of the breathing

to the field laboratory. mean

This figure illustrates

respiratory

Above,

ventilation

the regularity

Minutes of turtle B in the prone position,

the test period

(9~)

and oxygen

of the turtle’s and oxygen

breathing

has been subdivided consumption

(v,,)

and the close matching

shortly

into four intervals

have been calculated. between

ventilation

consumption.

When we placed turtle A in a prone position, however, its breathing pattern was quite different. Tidal volumes were smaller (mean volume of 31 breaths: 4.1 L) and respiratory frequency was higher (0.43 breaths/min for the same series of breaths).

372

SEA TURTLE RESPIRATION

Nearly identical results were obtained from turtle B over a 2i hour period (mean tidal volume: 3.5 L; frequency: 0.40 breaths/min). The consistancy of tidal volume and respiratory frequency can be seen from fig. 1 which shows the first 1: hours of the measurements on turtle B. Thus, placement of a green turtle in a supine position, while convenient for the experimenter, may alter the normal respiration of the animal. Tenney et al. (1974) noted, as did we, that the initial expiration phase of the respiratory cycle was, in either position, explosive and produced a sound much like the forced expiration of a human. These authors, in fact, reported that the peak expiratory flow velocities in their turtles were similar in magnitude to those occurring in man during maximal exertion. The sound of this expiration is such that on dark nights on the nesting beach a female turtle can, at times, be detected first from the sound of her ‘heavy breathing’. 2. Rest t‘s exercise Crawling on the land, which is clearly heavy exercise for a large green turtle, produced a pronounced increase in respiratory activity. The increase we observed was primarily in the frequency of breathing rather than in the depth of each breath. Over the course of a 45-minute ‘walk’ which was terminated by the turtle’s return to the sea, respiratory frequency averaged 4.0 breaths/min while a selection of 20 breaths measured in the period averaged 4.2 L in volume. The respiratory minute volume during exercise was thus about 15-16 L/min compared with resting values from the same animal which ranged from 0.74- 1.80 L/min. Most of the increased ventilation in the active turtle was due to the approximately ten-fold increase in respiratory frequency. Significantly, even during heavy exercise, the tidal volume did not approach the large values we observed on the supine, resting turtles. We made several counts of the respiratory frequency of turtles on the beach while they deposited eggs and covered their nests. These rates were 3-4 breaths/min, similar to that we observed from turtle B during her walk. Assuming the tidal volumes of the nesting turtles (which we were not able to measure) are also similar, we can infer that these animals sustain a high rate of ventilation and metabolism during their stay on the beach which can last several hours. Similarly, a tethered turtle, swimming in the surf parallel to the beach, was observed in two periods of 18 and 21 minutes to breathe about three times per minute.

OXYGEN CONSUMPTION AND THE SCALING OF METABOLISM

The minimum oxygen consumption of the adult, female green turtle was 0.024 L. kg- 1 . h- ‘. This value was measured from turtle B after one day in the prone position. Minimum values for this animal measured during the first day were from 2 to 3 times greater. Similar or even longer periods of time have been reported to be required for the establishment of true minimal or ‘basal’ conditions in other reptiles (Huggins et al., 1969; Irvine and Prange, 1976). The existing literature on

SEA TURTLE RESPIRATION

373

the metabolic rate of the adult green turtle is scant. Mrosovsky and Pritchard (1971) have estimated a greater oxygen consumption (0.069 L. kg- ’ . h- ‘); their value was derived from calculations of heat production which were, in turn, based on measurements of the core and surface temperatures and an assumed value for conductance. Minimum oxygen consumptions for large turtles of other species are 0.031 to 0.049 L. kg- 1 . h- ’ for the Aldabra giant tortoise (Geochelone (Test&o) gigantea) with body masses of 28.40 to 35.45 kg (Hughes et al., 1971) and 0.012 to 0.024 L.kgg’.h-’ for G a 1apagos tortoises (Geochefone (Test&) uicina or nigrita) with body masses of 69.4 to 149.7 kg (Benedict, 1932). The measurements on the tortoises were made at temperatures between 21 and 26 “C. The maximum oxygen consumption was measured from turtle B while it crawled on a level grassy surface. From 7 to 9 minutes after the crawling began the oxygen consumption was 0.162 L. kg- ’ . h- ‘. After 21 minutes of activity the oxygen consumption had increased to 0.25! L. kg- ’ . h- ‘. The mean of these values is 0.206 L. kg- ’ . h- ‘. Hughes et al. (1971) report that the oxygen consumption of their large tortoises rose to 0.119 to 0.147 L. kg- ’ . h- ’ when the animals were active while confined in their respirometer. Thus, although the minimal values of 0, consumption in the tortoises were similar to those of the green turtle, the maximum rates were rather different in these genera of large chelonians. The green turtle increased its 0, consumption during its walk some 7 to 10 times over resting levels while the tortoises’ consumption increased by only 3 to 5 times during activity. This disparity could be due to differences in phylogeny or in size (the green turtles were about 4 times greater in mass) or to the difference in the way the measurement of activity was made in the two studies. The effects of body size on oxygen consumption can be compared for the giant tortoise and the green turtle. Hughes et al. (1971) studied animals with a 300-fold range in body mass (0.118 to 35.45 kg). Data on the maximum and minimum oxygen consumption of the green turtle are available for hatchlings with a body mass of 0.030 kg (Prange and Ackerman, 1974), for immature animals with a body mass of 0.735 kg (Prange, 1976) and for adult animals of 127 and 141.5 kg body mass in this study. The range of body masses for the green turtle is more than three orders of magnitude. In addition, there are the data of Hutton et al. (1960) on freshwater turtles over the range of 0.2 to 1.8 kg. Because the range of body masses is so much smaller in that study we will confine our discussion of the effects of body size to the giant tortoise and the green turtle. In both of these species the minimal mass specific oxygen consumption decreases nearly identically as body mass increases (fig. 2). The least squares power regression lines for these data have slopes which indicate that the minimal consumption is proportional to the - 0.17 to - 0.18 power of body mass. In contrast, the maximal oxygen consumption remains very nearly directly proportional to body mass in both species; for both the exponent by which it scales to body mass is between -0.03 and -0.06.

H. D. PRANCE AND D. C. JACKSON

374 1.0

I

c

I

-----____

I

I

-----___

;:-:::::-:-::-----_

-.

I 0.1

0.01 0.01

-.

I 100

1 10

I 1

-\

Body Mass (kg) Fig. 2. Scaling are derived

of minimal

(1974) and Prange regression

and maximal

from mean data (+) (1976). Dashed

equations

for the Aldabra

oxygen

tortoise:

minimal,

consumption

from

lines arc from Hughes

are, for the green turtle:

giant

consumption

on the green turtle minimal,

and from Prange

et al. (1971) for the Aldabra

y = 0.058(~)-“.“~;

y = 0.045(.~)-~.~‘~;

in L. kg-’

to body mass of large turtles. this study

maximal,

maximal,

Solid lines

and Ackerman

giant tortoise. .r = 0.260(x))’

.V -0.141(.~)-“~~”

The 056;

; y is oxygen

hh ’ and x is body mass in kg.

A consequence of the divergence of the scaling of resting and active metabolism is that the larger animals are capable of much greater relative increases in activity than are the smaller animals. This trend is more pronounced in the green turtles because their maximal oxygen consumption is higher at any given body mass than that of the giant tortoise while the minimum values are nearly the same. A second consequence of the relatively higher metabolic rate of the green turtle during activity is that the internal body temperature of this animal may rise well above ambient temperature if the activity is sustained. We found that the cloaca1 temperature of turtle A at rest was 29 “C when the air temperature was 26 “C. No temperature measurements were taken from turtle B during activity but the duration of the activity was so short that, even if all the heat produced were stored, the body temperature woulch have risen only about 1 “C. This level of activity would have had to be sustained for several hours to achieve a large temperature difference. In this regard, Frair et al. (1972) reported a deep body temperature (in the region of the heart) of 25.5 “C in a 417 kg leatherback turtle, Dermochelys coriacea, only 60 minutes after its removal from a tank of 7.5 “C water in which it had been quite active. Cloaca1 temperatures, measured from the same animal, were 4-5 “C lower than deep body temperatures, which could mean that our measurement of the green. turtle’s temperature was an underestimate.

SEA TURTLE RESPIRATION

375

RESPIRATORY GAS EXCHANGE

The relationship between CO, loss and 0, uptake or respiratory exchange ratio (R), varied considerably in the study depending on the condition of the animal. Values obtained soon after moving the animal to the experimental site were low, ranging from 0.42 to 0.45 for turtle A and 0.38 to 0.41 for turtle B. In both cases the process of moving the turtle involved considerable activity on their part as well as ours, so that these measurements presumably depict the recovery from an exercise stress situation; these values of R are indicative of CO, retention. The pattern of breathing in the two animals was quite different since turtle A was supine and turtle B was prone during the measurements. It appears, therefore, that the low R value was due to the preceding activity in each case rather than to the position of the animal. R values were higher on the following day and in both animals approached 0.7. In turtle A the value was 0.65 and in turtle B values of 0.56 and 0.68 were recorded. Since the turtles reach the nesting area at Tortuguero after a long migration during which they do not feed (Carr and Goodman, 1970) an R value of 0.7 would be expected for an animal in steady-state gas exchange which was presumably deriving its energy from metabolism of stored lipids. We suggest, therefore, that when these data were obtained the turtles were in a condition approximating steady-state gas exchange. When turtle B exercised its respiratory exchange ratio increased to measured values of 0.95 and 1.06. This increase in R could be due either to a shift to carbohydrate metabolism (unlikely in an animal during a prolonged fast) or to hyperventilation and CO, unloading. We favor the latter interpretation, particularly in view of the post-exercise gas exchange we observed. We suggest that, during exercise, the turtle hyperventilates and loses CO, in excess of metabolic production while, during the recovery from exercise, the animal replenishes its CO, store. This description of the ventilatory state of the turtle is further borne out by the value of the ventilatory ratio, %‘E/V~, . This ratio remains quite constant for an animal under normal steady-state conditions. An increase generally denotes hyperventilation; a decrease denotes hypoventilation. The values obtained from animals during what we considered their resting steady-state condition ranged from 14.8 to 18.8 ml(nTPS)/ml(srPD). These values are similar to unpublished data we obtained earlier on yearling green turtles at 30 “C in which irE/7iT,, averaged 20.7 for 3 animals. Similar values have also been measured for the frewshwater turtle, Pseudemys scripta elegans (Jackson, 1971). Significant departures from the normal values for 7i’~/%‘~, were observed only during exercise when the ratio was high (hyperventilation) and the ‘post-stress’ condition of the green turtle when the ratio was low (hypoventilation). This analysis of the ventilatory state is based on the relationship between %‘E and metabolic rate, which is estimated most reliably by the Vo2. If Vco2 is employed instead, then the ‘post-stress’ ventilation cannot be regarded as hypo-

376

H. D. PRANCE

AND D. C. JACKSON

ventilation since VE/TiTco2at this stage was the same as during the pre-dive period. Another way to express this result is by analysis of the oxygen extraction coeflicient (E), the fraction of the inspired 0, which is utilized. The values of E for the green turtle ranged from 0.11 during exercise to 0.51 during the recovery phase. These data on gas exchange and ventilation are summarized in tables 1 and 2. TABLE Gas exchange Gas exchange

1

values obtained

ratio (R)

on turtle

B

‘?~/\jo* (LBTPS/LSTPD)

Extraction

Rest (‘post exercise’)

0.39 (4)

9.1 (4)

0.47 (4)

Rest (‘steady

0.62 (2)

15.3 (2)

0.32 (2)

I .oo(2)

44.2 (2)

0.12 (2)

state’)

Exercise Number

of observation

periods

in parentheses. TABLE

Mean respiratory

2

values obtained f (mini

Rest (‘post exercise’)

VT (L) 3.5

0.4

Rest (‘steady

4.1

9.2

4.2

4.0

state’)

Exercise

coefficient(E)

on turtle B ‘)

\jE (Ljmin)

-16

\‘o, (Ljmin)

I .29

0.140

0.82

0.054 0.34

From our observations we are not able to explain the cause of the apparent hyperventilation that accompanied activity in the green turtle. A possible basis is that the turtle became acidotic due to anaerobic metabolism and that the acidosis stimulated breathing. In many reptiles intense activity is powered acutely by anaerobic metabolism and lactic acid accumulates in the body fluids (Bennett and Licht, 1972; Moberly, 1968). In freshwater turtles, blood lactate increases dramatically during apneic diving and the resultant acidosis is presumably one of the factors contributing to the high rates of ventilation observed during the recovery from such dives (Jackson and Silverblatt, 1974). In contrast, Berkson (1966) observed only a slight increase in blood lactate, following similar dives, in green turtles. The green turtle is an active reptile with a high aerobic capacity (Prange, 1976) and may, like certain varanid lizards (Bennett, 1972; 1973) sustain these high levels of metabolic activity with little reliance on non-aerobic metabolic pathways. Direct measurements of blood acid-base status in exercising green turtles are needed to verify the occurrence of lactic acidosis.

Acknowledgements

We would like to thank the staff of the Green Turtle Station at Tortuguero, Costa Rica and the Caribbean Conservation Corporation for their assistance. Particular

SEA TURTLE

377

RESPIRATION

thanks go to Perran Ross for contributing study.

both his ideas and muscle-power to the

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Respiration Physiology VENTILATION, (1976) 21, 369-377; North-Holland GAS EXCHANGE AND METABOLIC OF A SEA TURTLE’ HENRY D. PRANGE Physiology Sec...
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