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Diel variation in the thermal tolerance of Litoria gracilenta (Anura: Hylidae)
Camp. B&hem. Physiol., 1972, Vol. 41A, pp. 727 to 730. PergamonPress. Printed in Great Britain
DIEL VARIATION IN THE THERMAL TOLERANCE OF LITORIA GRACILENTA (ANURA: HYLIDAE) CLIFFORD Department
RAY JOHNSON
of Zoology, The University of New England, Armidale, N.S.W. Australia
2351:
(Received 24 August 1971)
Abstract-l.
Critical thermal maxima (CTM) were determined at various intervals during the die1 cycle for Litoriu grucilentu acclimated at 15 and 25°C in Australia. 2. The CTM fluctuates over a 24-hr period with significant differences occurring among testing periods for both acclimation temperatures. 3. Data are given for other species of Australian anurans and suggest that daily variations in heat resistance may be widespread in anurans. INTRODUCTION
RECENTstudies have demonstrated that thermal tolerance varies within the daily cycle of anurans (Dunlap, 1969; Mahoney & Hutchison, 1969; Johnson, 1971a, b). This paper reports such fluctuations in Litmiu gracihta (formerly Hyla gracilmta; see Tyler, 1971) from subtropical Australia. MATERIALS
AND
METHODS
Specimens of L. grucilentu were collected by hand in early evening during the summer of 1970-71 near Brisbane, southeast Queensland, Australia. The critical thermal maximum (CTM) was determined at various intervals during the die1 cycle. CTM in this paper is the arithmetic mean of the thermal points at which locomotory activity becomes disorganized and the animal loses the ability to escape conditions that will promptly lead to death (Lowe & Vance, 1955). The onset of spasms (OS) (Hutchison et al., 1966) was used to determine the end-point. The effects of photoperiod, acclimation temperature and heating rate on the CTM have been stressed by various workers (Hutchison, 1961; Hutchison & Kosh, 1965; Brattstrom, 1968, 1970). Two groups of frogs were acclimated in total darkness in temperature control rooms (one group at 15°C and the other at 25°C) for 1 week prior to experimentation; the frogs were not fed but had access to water. Subsamples of L. grucilentu were taken at approximately 2-hr intervals throughout a 24-hr period, allowed to thermally equilibrate at room temperature for 1 hr to avoid thermal shock and then placed in a cylindrical glass chamber illuminated by a 250-W i.r. heat lamp (for details of apparatus and methods see Johnson, 1970). The frogs were immersed in water 10 mm deep. Rate of heating was controlled at 1 “C/3 min, the rate at which Hut&&on (1961) found the deep body temperature in salamanders corresponded with the water temperature. When the end-point was reached, cloaca1 temperature was measured with a Schultheis thermometer. Preliminary studies on the CTM of L. grucilentu showed that size and sex did not affect the CTM (Johnson, 1971~). 727
CLIFFORDRAY JOHNSON
728
RESULTS
Daily variation
AND
DISCUSSION
in thermal tolerance
The CTM fluctuates over a compared for each time interval significant differences (P < 0.01) tion temperatures. The pattern
24-hr period (Fig. 1). Acclimation treatments were by a Student’s t-test (Tables 1 and 2). There are in CTM’s among testing periods for both acclimaof change in CTM’s is similar for both acclimation
36
35 I
t 1
I
OIW
I
1
I
I
0300
0500
0700
c900
I
1100
I
1300
I
I500
I
1700
I
I
1900
2100
I 2300
TIME - hr
FIG. 1. Critical thermal maximum as a function of time of day for L. gracihta acclimated at 25°C (upper series) and 15°C (lower series). Curve lines connect means; vertical lines represent ranges with numbers above and below indicating sample size. TABLE ~-MATRIX COMPARING THEMEAN CRITICAL THERMAL L. gYaC&?rraACCLIMATED AT 25°C 0100 0100 0300 0500 0700 0900 1100 1300 1500 1700 1900 2100
0300
MAXIMA
OF SAMPLES OF
0500
0700
0900
1100
1300
1500
1700
1900
2100
2300
-
-
-
+ + + +
+ + + + -
+ + + -
+ + +
+ + + + + + -
+ + + + + -
+ + + + i+ -
A + indicates a significant difference at the 1 per cent confidence level.
THERMALTOLERANCE IN LlTORIA
729
GRACILENTA
TABLE 2-MATRIX COMPARING THE MRANCRITICALTHERMALMAXIMAOF SAMPLESOF L. gracihta ACCLIMATED AT 15°C 0100 0100 0300 0500 0700 0900 1100 1300 1500 1700 1900 2100
0300
0500
0700
0900
1100
1300
1500
1700
-
_
+ _ +
+ + -
+ + +
+ + +
+ + + + -
+ + -
1900
+ + + + + + + -
2100
+ +
2300
+ + + + + + + + +
A + indicates a significant difference at the 1 per cent confidence level.
temperatures with more variation occurring in the 15°C group. The results are similar to those reported by Mahoney & Hutchison (1969) for Hyla labialis and Rana pipiens but dissimilar to those of A&s crepitans (Dunlap, 1969), Litoria caerulea and Bufo mar&w (Johnson, 1971a, b). The peak at 2100 hr in L. gracilenta could indicate a shift in the circadian rhythm and a loss of the environmental zeitgeber. Such a peak has been found at 2300-2400 hr in L. caerulea and Bufo marinus. L. caerulea was acclimated under a LD 12 : 12 photoperiod (Johnson, 1971a) while Bufo marks was acclimated in total darkness (Johnson, 1971b). A daily rhythm in heat resistance is evident in L. gracilenta but its significance is unknown. It has been suggested that it might be a by-product of some other underlying physiological rhythm (Dunlap, 1969) or that it might have survival value itself (Dunlap, 1969; Johnson, 1971a, b). Evidence also exists that the CTM’s of Litoria freycinetti, L. glauerti, Cyclorana alboguttatus, Limnodynastes peroni and Taudactylus diurnus are dependent upon the time of day (Johnson, unpublished). T. diurnus as the name implies is a diurnal frog and such an increase in heat resistance during the midday hours may have survival value, although temperatures in the rainforest would seldom reach upper critical limits (Johnson, 1971d). L. glauerti, on the other hand, has been found basking during the day and variation in heat resistance quite possibly has survival value in this case, as also appears to be true for L. caerulea and B. marinus during the breeding season (Johnson, 1971a, b). The above data suggest that daily variation in heat resistance may be widespread in anurans. Acknowledgements--I wish to thank Graham Donnelly for assistance in the field. My wife, Colleen, prepared the figure and also assisted with collection of the material. Space and facilities were provided by the University of Queensland. Dr. Harold F. Heatwole, University of New England, kindly reviewed the manuscript.
730
CLIFFORDRAY JOHNSON REFERENCES
BRATTSTROMB. H. (1968) Thermal acclimation in anuran amphibians as a function of latitude and altitude. Camp. Biochem. Physiol. 24, 93-l 11. BRATTSTROM B. H. (1970) Thermal acclimation in Australian amphibians. Comp. Biochem. Physiol. 35, 69-103. DUNLAP D. G. (1969) Evidence for a daily rhythm of heat resistance in the cricket frog, Acris crepitans. Copeia 1969, 4, 852-854. HUTCHISONV. H. (1961) Critical thermal maxima in salamanders. Physiol. Zoiil. 34, 92125. HUTCH~~ONV. H. & KOSH R. J. (1965) The effect of photoperiod on the critical thermal maxima of painted turtles (Chrysemys picta). Herpetologica 20, 233-238. HUTCHISONV. H., VINEGARA. & KOSH R. J. (1966) Critical thermal maxima in turtles. Herpetologica 22, 3241. JOHNSONC. R. (1970) Observations on body temperatures, critical thermal maxima and tolerance to water loss in the Australian hylid, Hyla caerulea (White). Proc. R. Sot. Qd 82, 47-50. JOHNSONC. R. (1971a) Daily variation in the thermal tolerance of Litoria caeruka (Anura: Hylidae). Camp. Biochem. Physiol. 40, 111 l-l 113. JOHNSONC. R. (197lb) Thermal relations and daily variation in the thermal tolerance in Bufo marinus. J. Herpetology (In press.) JOHNSONC. R. (1971~) Thermal relations in some southern and eastern Australian anurans. Proc. R. Sot. Qd 82, 87-94. JOHNSONC. R. (1971d) Thermal relations and water balance in the day frog, Taudactylus diurnus, from an Australian rainforest. Aust. J. 2001. 19, 35-39. LOWE C. H. & VANCE V. J. (1955) Acclimation of the critical thermal maximum of the reptile, Urosaurus ornatus. Science, N. Y. 122, 73-75. MAHONEYJ. J. & HUTCHISONV. H. (1969) Photoperiod acclimation and 24-hour variations in the critical thermal maxima of a tropical and a temperate frog. Oecologia 2, 143-161. TYLER M. J. (1971) The phylogenetic significance of vocal sac structure in hylid frogs. Univ. Kans. Pubis Mus. nut. Hist. 19, 319-360. Key Word Indejc-Thermal tolerance ; heat resistance ; Australia ; amphibians ; anurans ; Litoria gracilenta; Cyclorana; Limnodynastes; Tauakctylus; Hylidae; Leptodactylidae; temperature; critical thermal maximum; die1 fluctuations.
DIEL VARIATION IN THE THERMAL TOLERANCE OF LITORIA GRACILENTA (ANURA: HYLIDAE) CLIFFORD Department
RAY JOHNSON
of Zoology, The University of New England, Armidale, N.S.W. Australia
2351:
(Received 24 August 1971)
Abstract-l.
Critical thermal maxima (CTM) were determined at various intervals during the die1 cycle for Litoriu grucilentu acclimated at 15 and 25°C in Australia. 2. The CTM fluctuates over a 24-hr period with significant differences occurring among testing periods for both acclimation temperatures. 3. Data are given for other species of Australian anurans and suggest that daily variations in heat resistance may be widespread in anurans. INTRODUCTION
RECENTstudies have demonstrated that thermal tolerance varies within the daily cycle of anurans (Dunlap, 1969; Mahoney & Hutchison, 1969; Johnson, 1971a, b). This paper reports such fluctuations in Litmiu gracihta (formerly Hyla gracilmta; see Tyler, 1971) from subtropical Australia. MATERIALS
AND
METHODS
Specimens of L. grucilentu were collected by hand in early evening during the summer of 1970-71 near Brisbane, southeast Queensland, Australia. The critical thermal maximum (CTM) was determined at various intervals during the die1 cycle. CTM in this paper is the arithmetic mean of the thermal points at which locomotory activity becomes disorganized and the animal loses the ability to escape conditions that will promptly lead to death (Lowe & Vance, 1955). The onset of spasms (OS) (Hutchison et al., 1966) was used to determine the end-point. The effects of photoperiod, acclimation temperature and heating rate on the CTM have been stressed by various workers (Hutchison, 1961; Hutchison & Kosh, 1965; Brattstrom, 1968, 1970). Two groups of frogs were acclimated in total darkness in temperature control rooms (one group at 15°C and the other at 25°C) for 1 week prior to experimentation; the frogs were not fed but had access to water. Subsamples of L. grucilentu were taken at approximately 2-hr intervals throughout a 24-hr period, allowed to thermally equilibrate at room temperature for 1 hr to avoid thermal shock and then placed in a cylindrical glass chamber illuminated by a 250-W i.r. heat lamp (for details of apparatus and methods see Johnson, 1970). The frogs were immersed in water 10 mm deep. Rate of heating was controlled at 1 “C/3 min, the rate at which Hut&&on (1961) found the deep body temperature in salamanders corresponded with the water temperature. When the end-point was reached, cloaca1 temperature was measured with a Schultheis thermometer. Preliminary studies on the CTM of L. grucilentu showed that size and sex did not affect the CTM (Johnson, 1971~). 727
CLIFFORDRAY JOHNSON
728
RESULTS
Daily variation
AND
DISCUSSION
in thermal tolerance
The CTM fluctuates over a compared for each time interval significant differences (P < 0.01) tion temperatures. The pattern
24-hr period (Fig. 1). Acclimation treatments were by a Student’s t-test (Tables 1 and 2). There are in CTM’s among testing periods for both acclimaof change in CTM’s is similar for both acclimation
36
35 I
t 1
I
OIW
I
1
I
I
0300
0500
0700
c900
I
1100
I
1300
I
I500
I
1700
I
I
1900
2100
I 2300
TIME - hr
FIG. 1. Critical thermal maximum as a function of time of day for L. gracihta acclimated at 25°C (upper series) and 15°C (lower series). Curve lines connect means; vertical lines represent ranges with numbers above and below indicating sample size. TABLE ~-MATRIX COMPARING THEMEAN CRITICAL THERMAL L. gYaC&?rraACCLIMATED AT 25°C 0100 0100 0300 0500 0700 0900 1100 1300 1500 1700 1900 2100
0300
MAXIMA
OF SAMPLES OF
0500
0700
0900
1100
1300
1500
1700
1900
2100
2300
-
-
-
+ + + +
+ + + + -
+ + + -
+ + +
+ + + + + + -
+ + + + + -
+ + + + i+ -
A + indicates a significant difference at the 1 per cent confidence level.
THERMALTOLERANCE IN LlTORIA
729
GRACILENTA
TABLE 2-MATRIX COMPARING THE MRANCRITICALTHERMALMAXIMAOF SAMPLESOF L. gracihta ACCLIMATED AT 15°C 0100 0100 0300 0500 0700 0900 1100 1300 1500 1700 1900 2100
0300
0500
0700
0900
1100
1300
1500
1700
-
_
+ _ +
+ + -
+ + +
+ + +
+ + + + -
+ + -
1900
+ + + + + + + -
2100
+ +
2300
+ + + + + + + + +
A + indicates a significant difference at the 1 per cent confidence level.
temperatures with more variation occurring in the 15°C group. The results are similar to those reported by Mahoney & Hutchison (1969) for Hyla labialis and Rana pipiens but dissimilar to those of A&s crepitans (Dunlap, 1969), Litoria caerulea and Bufo mar&w (Johnson, 1971a, b). The peak at 2100 hr in L. gracilenta could indicate a shift in the circadian rhythm and a loss of the environmental zeitgeber. Such a peak has been found at 2300-2400 hr in L. caerulea and Bufo marinus. L. caerulea was acclimated under a LD 12 : 12 photoperiod (Johnson, 1971a) while Bufo marks was acclimated in total darkness (Johnson, 1971b). A daily rhythm in heat resistance is evident in L. gracilenta but its significance is unknown. It has been suggested that it might be a by-product of some other underlying physiological rhythm (Dunlap, 1969) or that it might have survival value itself (Dunlap, 1969; Johnson, 1971a, b). Evidence also exists that the CTM’s of Litoria freycinetti, L. glauerti, Cyclorana alboguttatus, Limnodynastes peroni and Taudactylus diurnus are dependent upon the time of day (Johnson, unpublished). T. diurnus as the name implies is a diurnal frog and such an increase in heat resistance during the midday hours may have survival value, although temperatures in the rainforest would seldom reach upper critical limits (Johnson, 1971d). L. glauerti, on the other hand, has been found basking during the day and variation in heat resistance quite possibly has survival value in this case, as also appears to be true for L. caerulea and B. marinus during the breeding season (Johnson, 1971a, b). The above data suggest that daily variation in heat resistance may be widespread in anurans. Acknowledgements--I wish to thank Graham Donnelly for assistance in the field. My wife, Colleen, prepared the figure and also assisted with collection of the material. Space and facilities were provided by the University of Queensland. Dr. Harold F. Heatwole, University of New England, kindly reviewed the manuscript.
730
CLIFFORDRAY JOHNSON REFERENCES
BRATTSTROMB. H. (1968) Thermal acclimation in anuran amphibians as a function of latitude and altitude. Camp. Biochem. Physiol. 24, 93-l 11. BRATTSTROM B. H. (1970) Thermal acclimation in Australian amphibians. Comp. Biochem. Physiol. 35, 69-103. DUNLAP D. G. (1969) Evidence for a daily rhythm of heat resistance in the cricket frog, Acris crepitans. Copeia 1969, 4, 852-854. HUTCHISONV. H. (1961) Critical thermal maxima in salamanders. Physiol. Zoiil. 34, 92125. HUTCH~~ONV. H. & KOSH R. J. (1965) The effect of photoperiod on the critical thermal maxima of painted turtles (Chrysemys picta). Herpetologica 20, 233-238. HUTCHISONV. H., VINEGARA. & KOSH R. J. (1966) Critical thermal maxima in turtles. Herpetologica 22, 3241. JOHNSONC. R. (1970) Observations on body temperatures, critical thermal maxima and tolerance to water loss in the Australian hylid, Hyla caerulea (White). Proc. R. Sot. Qd 82, 47-50. JOHNSONC. R. (1971a) Daily variation in the thermal tolerance of Litoria caeruka (Anura: Hylidae). Camp. Biochem. Physiol. 40, 111 l-l 113. JOHNSONC. R. (197lb) Thermal relations and daily variation in the thermal tolerance in Bufo marinus. J. Herpetology (In press.) JOHNSONC. R. (1971~) Thermal relations in some southern and eastern Australian anurans. Proc. R. Sot. Qd 82, 87-94. JOHNSONC. R. (1971d) Thermal relations and water balance in the day frog, Taudactylus diurnus, from an Australian rainforest. Aust. J. 2001. 19, 35-39. LOWE C. H. & VANCE V. J. (1955) Acclimation of the critical thermal maximum of the reptile, Urosaurus ornatus. Science, N. Y. 122, 73-75. MAHONEYJ. J. & HUTCHISONV. H. (1969) Photoperiod acclimation and 24-hour variations in the critical thermal maxima of a tropical and a temperate frog. Oecologia 2, 143-161. TYLER M. J. (1971) The phylogenetic significance of vocal sac structure in hylid frogs. Univ. Kans. Pubis Mus. nut. Hist. 19, 319-360. Key Word Indejc-Thermal tolerance ; heat resistance ; Australia ; amphibians ; anurans ; Litoria gracilenta; Cyclorana; Limnodynastes; Tauakctylus; Hylidae; Leptodactylidae; temperature; critical thermal maximum; die1 fluctuations.