Comp Biochem Phys:ol. 1976. tbl 53A. pp 41 to 44 Per#araon Press Printed m Great Bruam

AESTIVATION AND THERMOREGULATION IN THE TEXAS TORTOISE, GOPHERUS BERLANDIERI

WILLIAM G. VOIGT AND CLIFFORD RAY JOHNSON

Dwlsion of Biological Control, University of Califorma, Berkeley, 1050 San Pablo Avenue, Albany, CA 94706, U.S.A.

(Recewed 13 December 19745

Abstraet--l. Deep body temperatures of three Gopherus herlandwrt were momtored with radio-tele- metry m their natural habitat, m June 1974

2 In contrast to G agass~:n, th,s speoes engages m extenswe pre-emergent basking. It does not emerge untd ~ts body temperatures have reached minimal voluntary hmlts.

3 Actwity was notably curtaded, indicating summer aestwat,on. 4. Aestwating torto,ses maintained lower average body temperatures than actwe indwiduals. 5. Pre-emergent basking allows th,s species to attain full co-ordinat~on of its functions before expos-

mg ,tself. Th~s factor allows it to actwely escape to shelter when &sturbed rather than to depend upon passive resistance

I N T R O D U C T I O N

MACKAY'S original work (1964) with the Galapagos tortoise has generated a large number of studies on thermoregulation in unrestrained reptdes using radio telemtry (McGinms & Brown, 1966; McGmnis, 1967a,b; McGinnis & Dickson, 1967; Stebbins & Bar- wick, 1968; McGinnis & Moore, 1969; Johnson, 1972. 1973; Johnson et al, 1975, in press. Relatively few studies have utilized telemetry m the study of che- lonian thermoregulation, however. McGinms & Voigt (1971) stu&ed thermoregulation m the desert tortoise (Gopherus agassi-n), and Moll & Lagler (1971) studied thermoregulation m the pond turtle. Pseudemys scrtpta.

The Texas tortoise (Gopherus berlandwri) inhabits subtropical habitats in south Texas and northern Mexico, while the desert tortoise, G. agasst-ii, inhabi- tats more xeric environments (Brattstrom, 1961). The purpose of this research was to study the thermoregu- latory behaviour of the Texas tortoise, G. berlandierl, in its natural enwronment, and compare it w~th that of the desert tortoise, G. agassi:ti

MATERIALS AND M E T H O D S

The study was conducted at the Laguna Atascosa Wild- hfe Reserve. Cameron Co, Texas, durmg the month of June 1974. Specifically. tortmses were observed on a small isolated hdl (loma) approximately 300m from the eoast- hne. Honey mesquite (Prosopsts glandulosa), prickly pear (Opunt,a lindhemlerO and other low lymg shrubs covered much of the ground. Sparse grasses occurred on the flats surrounding the loma.

Three adult female Gopherus berlandiert (750-1000g) were force-fed small temperature sensttive transmitters (8 mm dia x 12 mm) (Spencer. 1968) and replaced within 15 mm at their point of capture. W~th a cautious approach. signals could be received with a portable AM radio at a distance of 2 m without any observable disturbance to the ammals. A number was applied to each ammal for individual recogmtion w,th white acryhc paint. A daub of paint was applied to the posterior part of the shell of an

untelemetered control tortoise with a long st~ck to avoid any &sturbance.

Body temperatures were recorded at 30mm intervals and at tmmes of behavioural changes (e.g. emergence, retreat to shade, etc J. Env,ronmental temperatures were recorded at hourly intervals w:th a copper--constantine thermocou- pie probe attached to a Comark electromc thermometer (model 16255. The tip of the thermocouple was affixed to a pole and placed in the micro-environment des,red. Tem- peratures were recorded on shaded and exposed ground surface, and reside and at the entrance of a shallow unoc- cup,ed west-facing burrow. Thermocouples (+ 0.1°C) and transmitters (+ 02°C) were cahbrated against the same standard mercury thermometer

RESULTS

The study period was preceded by a month of drought conditions unusual to the area at that time of year. The sky was usually occluded each morning by a high thin overcast which persisted until noon, followed by partially cloudy skies in the afternoon.

Ground surface temperatures rose steadily after sunrise and reached a peak by 1400 hr CST (Fig. 1). Peak shaded surface temperatures lagged 1 to 2 hr behind exposed surface temperatures. Deep burrow temperatures lagged behind shade temperatures, but increased in the late afternoon, probably due to after- noon insolation on the west facing burrow. After dusk, ground surface temperatures fell slightly below burrow temperatures and equilibrated with shade temperatures (Fig. 1).

Very little activity was observed during the course of the study in all four tortoises. Two animals (tor- toise A and control) moved less than 2 m after their initial marking and release (Fig. 1). Tortoises B and C exhibited limited periods of activity (Figures 2 and 3, 25th June). The deep body temperatures of the first two tortoises showed a gradual increase and decline following environmental temperatures (Fig. l). The more marked fluctuations of tortoises B and C reflect periods of exposure and activity (Figs. 2 and 3). Tor- toise A retreated into the dense shade of a grass

41

42 W.G. VOIGT ̂ NI~ C. R. JOHNSON

O

IN

8 12 16 20 24 4 8 12 16 TIME

Fig. I. Deep body temperature fluctuatmns and actiwty patterns of a telemetered Texas tortoise (A) and actnwty patterns of an untelemetered, control tortoise. Heavy line indicates deep body temperature, stippled area represents the range of environmental temperatures available to the animal, upper limit showing exposed ground surface tern-

• peratures and lower lim]t deep burrow temperature. Dashed line indicates shaded surface temperatures. Bar segments represent: tortoise in dense shade (stippled); in partial shade (horizontal hnes); and in the sun (clear). Saw- tooth segments indicate periods of activity. (June 25 and

26, 1974).

clump after release, and for the following 2 days remained there. Deep body temperatures closely fol- lowed minimal environmental temperatures during the first day, and rose slightly higher foUowmg shaded surface temperatures the second day (Fig. 1). It should be pointed out that environmental temperatures were not taken at the exact same sites occupied by the tortoises. The behaviour of the control tortoise was similar to that of tortoise A (Fig. 1). Its activity con- sisted of moving from one shelter to another (25th June, 0735 b.r) where it remained inactive until 1830 hr (26th June, Fig. 1).

Figure 2 depicts the temperature responses of a more active tortoise (B). On 24th June, this tortoise retreated under a pad of a prostrate Opuntza clump. At 0800 hr, the sun's rays partially struck the tortoise, and it turned so that it was perpendicular to the sun's rays, but was still under cover. It was not until 3 hr later that it finally emerged from shelter (1050 hr) and became active at a temperature of 30.2°C. At 1200 hr (32.5°C) it began to dig a hole with its hind feet; a behaviour described by Auffenberg & Weaver (1969) for a nesting female. At 1215 hr (36-3°C) nesting acti- vity ceased, and the animal retreated to a dense Opun- t/a clump approximately 10m from its previous shelter. Body temperatures dropped rapidly to 34°C following retreat and fell more gradually after that.

50

,0 4°

[30

I I ..... -= ...... ' f

I I I I I I l I I 8 12 16 20 24 4 8 12 16 20

TIME Fig. 2. Deep body temperature fluctuations of an unres-

trained Texas tortoise (13). All symbols as in Fig. 1.

5C

~3o p_.

2O

I I I I I I l I I 8 12 16 20 24 4 8 12 16

TIME

Fig. 3. Deep body temperature fluctuations of an unres- trained Texas tortoise (C). All symbols as in Fig. 1.

No afternoon emergence occurred. Late afternoon fluctuations in deep body temperatures reflect partial exposure of the tortoise due to changes in the sun's azimuth (Fig. 2). On the morning of 26th June, the rays of the sun struck tortoise B and it moved deeper into its shelter (24.5°C) before any appreciable changes in body temperature. Body temperatures closely followed shaded surface temperatures for the remainder of the day. At 1720 hr tortoise B emerged (32.8°C) and again engaged in nesting behaviour, but stopped and retreated to a nearby shelter at 1850 hr (33.2°C, Fig. 2).

Tortoise C (Fig. 3) continuously used the same retreat deep under a large Opuntia clump. Inside the clump, was a pallet used for evening retreat. At 0715 hr (25th June, Fig. 3) it became active but did not emerge. It shuttled about in the sun/shade mosaic under the Opuntia clump and stayed in the sun. It did not emerge until body temperatures exceeded 28°C (l135hr). After moving through some dense brush, it basked in the sun from 1200 to 1215hr (29.0°C-32.0°C) and by 1300hr had retreated to a partially shaded Opuntia clump (34'5°C). Body tem- peratures continued to rise, probably due to the sparse cover provided, and at 1330 hr (36.3°C) tortoise C retreated to its original shelter. Body temperature dropped back to 32"5°C by 1500 hr (Fig. 3). The rise in body temperatures in the late afternoon resulted from the selection of sunny spots inside tortoise C's shelter. It assumed a posture characteristic of basking Gopherus aoassiziz (McGinnis & Voigt, 1971); the body was perpendicular to the sun's rays with the limbs and neck outstreached. Final retreat of tortoise C to its pallet within the Opuntia dump occurred at 1740 hr (36.0°C, Fig. 3).

Activity the following morning was restricted to shuttling under the Opunt~a clump. Howe~;er, due to a heavier overcast, the tortoise did not receive as much sun. Body temperatures followed shade temper- atures for the rest of the day, and a sharp rise in body temperature followed afternoon emergence (1700hr, Fig. 3; 34.0°C). Retreat occurred at 1730hr (35.5°C).

Table 1 summarises the daily mean body tempera- tures of the inactive tortoise from 0800 to 2000 hr, and of active tortoises from emergence through even- ing, retreat. The temperatures for each type of activity pattern are similar. Mean body temperatures of inac- tive tortoises were consistently lower than tempera- tures of active individuals (Table 1).

Aestivation and thermoregulation in the Texas tortoise 43

T a b l e ~t. Mean body t e m p e r a t u r e s o f t h r e e Gophox~t8 berlltn(~Liori,dt~Lu K

aemt~vat ion (N£) and a o t t ~ l W ( £ ) . Ina©tXye n o a n e r o o o r d e d

f r ~ 0800 to 2000 h r s . A o t i w s moene r ~ o o r d e d f r ~ 8 ~ t e r

mornlnK quaorgenoo ~o emorsenoo t o owsn lnK r o t r o a t .

- ~ a S . D . X • 3 . D .

£ 29.7 + 2.5 28 N£ 29.0 + 4.0 21 NA

B 32,2 +- 2.2 23 £ 29.0 +- 3.0 ~ 22 IU.

0 33.3. 4- 1.6 21 £ 29.3 *-- 3.0 23. lq£

D I S C U S S I O N A N D C O N C L U S I O N S

The thermal ecology of the desert tortoise (Gopherus agassizii) has been studied extensively (Voigt, 1972), and several areas of contrast and com- parison with G. berlan&eri can be made.

Auffenberg & Weaver (1969, Table 7) observed a bimodal activity period for G. berlandieri during mid- June. More active tortoises were encountered during the morning and late afternoon hours than at midday. Also, fewer total active tortoises were encountered during mid-June than in the spring or fall months (Auffenberg & Weaver, 1969; Table 7). McGirmis & Votgt (1971) also noted less activity in the desert tor- toise (G. agassizii) during summer and attributed th~s reduction to a partial aestivation. Figure 4 depicts the thermal behaviour of an aestivating and an active G. agassizii in the western Mojave Desert, Californm (data from McGmnis & Vo]gt, 1971, and unpublished data for the same animals) Tortoise A spent a greater part of its time deep in its burrow, while tortoise B spent most of its time above ground. A much higher mean body temperature can be observed in tortoise B, and its body temperature fluctuated more than that of the sequestered animal (Fig. 4). Sequestered G. ber- landzeri also averaged lower, more stable tempera- tures than active ones (Table 1).

Auffenberg & Weaver (1969) noted that G. berlan- dzeri will feed on Opuntia pads and fruits m the sum- mer. During the 2"5 days of observation, none of the

8 12 16 2 24 4 8 12 16 2 TIME

Fig 4. Deep body temperature fluctuations of an aestivat- mg (A) and an active (B) desert tortoise measured by radio- telemetry on the Mojave Desert. Heavy lines denote deep body temperatures. Stippled areas represent range of ambient temperatures available, limited by the exposed surface temperature above and deep burrow temperature below. Dashed line represents shaded surface temperatures. Horizontal bar segments represent: m the burrow (stip- pled); in the shade (horizontal lines); in the sun (clear); and under a bush at mght (vertical lines). Sawtooth seg- ments indicate periods of acUvity. Data partially from

McGmnis & Voigt (1971).

four G. berlandieri were observed to eat. This is in contrast to G. agassizii which continues to feed on dried grasses throughout the summer (Woodbury & Hardy, 1948; McGinnis & Voigt, 1971).

The burrows of desert tortoises are generally longer than those used by the Texas tortoise, therefore pro- riding a much more stable environment within (Fig. 1 burrow temp vs Fig. 4 burrow temp). Vegetation is sparse and scattered on the Mojave Desert, and provides only minimal shelter from high midday tem- peratures. G. berlandieri inhabitats areas of more dense vegetation (Auffenberg & Weaver, 1969) which would provide greater protection against temperature extremes. Burrows, if used at all, are usually barely large enough to cover its occupant (Auffenberg & Weaver, 1969).

In this study, G. berlandierz emerged after a pro- longed "warm-up" period inside the shelter. Emer- gence did not occur until body temperatures exceeded 28°C, and only minimal basking occurred after emer- gence. Emergence in G. cu3assizii is independent of body temperature, occurring at temperatures of 16- 30.I°C, and followed by a basking period. Basking invariably ceased at 28-29°C. Ambient epigean tem- peratures at morning emergence were always higher than body temperatures. Emergence at this time favors heat gain from the environment (Voigt, 1972).

The emergence behaviour of G. berlandieri is sinfi- lar to that of the lizard, Dipsosaurus dorsalis (McGinnis & Dickson, 1967). This lizard retreats to rodent burrows at night and prior to emergence, basks at the shallow warmer sections of the burrow until it attains minimal voluntary temperatures at which time it emerges. This allows the lizard to be fully co-ordinated, without the necessity of a vulner- able basking period.

An obvious behavioural difference between Texas and desert tortoises is in their reactions to distur- bances. G. agassizii will usually "freeze" when it detects movements, and withdraw into the shell if approached closely. After 10-15 min, normal activities are resumed. However, the three telemetered G. ber- landieri each retreated to the nearest cover after being fed a transmitter. Another tortoise, encountered later in the study, also fled to cover. Such shyness may be adaptive in the smaller species (G. berlandieri) in areas offering suitable shelter. The larger size attained by G. agassizzi renders it safer from predation. Also, the relative scarcity of cover may reduce the effective- ness of active withdrawal. The emergence behaviour of each species can be correlated with their defensive reactions, in that active escape requires higher body temperatures and greater co-ordination than required for passive withdrawal into their shell.

A series of cloacal temperatures taken with quick- recording thermometers is fraught with considerable uncertainty introduced by the observer and his tech- nique, especially in a species so prone to disturbance as Gopherus berlandieri. The ease and duration of dis- turbance to normal behavlour in G. berlandieri emphasize the usefulness of telemetry for the monitor- ing of body temperatures in this species.

Acknowledgements---The Rob and Bessie Welder Wildlife Foundation provided housing during periods away from the field. The work was partially funded by a grant from

44 W.G. VOIGT AND C. R. JOHNSON

the National Geographic Society (to C. R. Johnson). Thanks are due Christine M. Merritt for her valuable sug- gestions and criticisms of the manuscript.

REFERENCES

AUFFEIqBERG W. & WEAVER W. G. JR. (1969) Gopherus ber- landieri in southern Texas. Bull. Fla. State Mus. Biol. Sei. 13, 1-203.

BRAt Jsn~OM B. H. (1961) Some new fossil tortoises from North America with remarks on zoogeography and paleoecology of tortoises, d. Paleont. 35, 543-560.

JOHNSON C. R. (1972) Thermoregulation in pythons----I. Effect of shelter, substrate type and posture on body temperature of the Australian carpet python, Morelia spilotes oariegata. Camp. Biochem. Physiol. 43A, 271-278.

Jom~SOlq C. R. (1973) Thermoregulation in pythons---II. Head-body temperature differences and thermal prefer- enda in Australian pythons Camp. Biochem. Physiol. 45A, 1065-1087.

JOHNSON C. R., WEBa G. J. W. & JOI-nqsoN C. (1975) Ther- moregulation in pythons--111. Thermal ecology and be- havior of the black-headed rock python, Aspidites raelanocephalus. Herpetologica 31, (In press).

MAcr~¥ R. S. (1964) Galapagos tortoise and marine iguana deep body temperatures measured by radio tele- metry. Nature, N.Y. 204, 355-358.

McGI~IS S. M. (1967a) Telemetry applied to studies of thermoregulation in reptiles. Proc. hath. Tele. Conf. 1967, 252-254.

McGtNNIs S. M. (1967b) The adaptation of biotelemetry techniques to small reptiles. Copem 1967, 474-475.

MCGINNIS S. M. & BROWN C. W. (1966) Thermal behavior of the green iguana, Iguana iguana. Herpetologwa 22, 189-199.

MCGINNIS S. M. & DICKSON L. L. (1967) Thermoregula- tion in the desert iguana, Dipsosaurus dorsalis. Science, N.Z 156, 1757-1759.

McGINIms S. M. & MOORE R. G. (1969) Thermoregulation in the boa constrictor, Boa constrictor. Herpetologica 25, 38-45.

MCGINNIS S, M. & VOIOT W. G (1971) Thermoregulation in the desert tortoise, Gopherus agasslzil. Camp, Bioehem Physiol. 40A, 119-126.

MOLL E. O & LEGLER J. M. (1971) The life history of the slider turtle, Pseudemys scripta (Schoep0 in Panama. Bull. Los Angeles Mils. Nat. Hist. Sci. No. I I.

SPENCER H. (1968) Thermally stable telemeter for thermoreg- ulation studies. Science, N.Y. 161, 574-575

STEBBINS R. C. & BARWlCK R. E. (1968) Radiotelemetric study of thermoregulatlon in a lace monitor. Copeia 1968, 541-547.

VOlGT W. G (1972) Thermal ecology of the desert tortoise, Gopherus agassizii in the Mojave Desert, Kern County, California. M.A. Thesis, California State Umvermty, Hayward.

VOIOT W. G. (1975) Heating and cooling rates and their effects upon heart rates and subcutaneous temperatures in the desert tortoise, Gopherus agassizii Camp Biochem. Physiol. 52A, 527-531.

WOODaURV A. M. & HARDY R. (1948) Studies of the desert tortoise, Gopherus agasstzii. Ecol. Monogr. 18, 145-200.