Thermoregulatory behaviour in the toads Bufo marinus and Bufo cognatus

J therm Bzol Vol 16, No 5, pp 309-312, 1991

0306-4565/91 S3 00 + 0 O0 Copyright © 1991 Pergamon Press pie

Pnnted m Great Bntam All nights reserved

T H E R M O R E G U L A T O R Y BEHAVIOUR IN THE TOADS BUFO M A R I N U S AND BUFO COGNATUS LYNNETrE M SIEVERT* Department of Zoology, Umvers~tyof Oklahoma, Norman, OK 73019, U S A (Recewed 11 October 1990, accepted m rewsed form 5 April 1991)

Abstract--I The temperature preference of Bufo marius m a hnear thermal gradient over a 24 h penod was measured m the spnng using uniform hght (UL) over the length of the gradient and in the spnng and fall usmg a pomt source of hght over the hot end of the gradient only (LH) 2 The temperature preference of Bufo cognatus m a hnear thermal gradient was measured over a 24 h period dunng the fall with the LH regime 3 Light regime and season had no effect on the mean body temperature (Tb) selected over a 24 h period in B marius The pattern of temperature selection over tame was mfluenced by season 4 Temperate B cognatus selected slgmficantlyhigher mean Tbs that the trop,cal B marius and selected significantly higher Tbs dunng late photophase than late scotophase Key Word Index ThermoregulaUon, Bufo, toad

INTRODUCTION

Behaxqoural thermoregulat~on m ectotherms, especially reptiles, has been widely studied (Brattstrom, 1965, 1979, Avery, 1982) Amphlbmns are faced with the same benefits of elevatmg body temperature (Tb) as reptiles. Such benefits mclude increased d~gestwe rate, development, growth and appetite (Brattstrom, 1979; Lillywlnte et a l , 1973, Duellman and Trueb, 1985) Yet, the cost of elevatmg Tb differs between the two groups because amph~b,ans are more prone to dehydration At high Tbs more heat is lost through cutaneous water loss Bufo spmosus lost considerably more mass, presumably due to dehydration, than the hzard Ltolaemus mulnformts dunng baskmg (Pearson and Bradford, 1976) Therefore, only those amphlb i n s with a reliable source of water can allow Tb to rise for any length of time DespRe this problem anurans do bask m the sun, presumably to elevate Tb (Ldlyw~te et a l , 1973, Ldlywhlte, 1975) Amph~bmn thermoregulatory behawour has been observed m the field and in the laboratory (Brattstrom, 1979), but very httle is known concerning pertinent cues for behaviourai thermoregulatlon Some amphibians hvmng m cool, montane habitats behavmurally elevate Tb above ambient (Pearson and Bradford, 1976, Heath, 1975) Some species elevate Tb above normal levels after feeding (Feder, 1982, Ldlywhlte et a l , 1973) Tiger salamanders lower Tb below normal in response to hypoxm (Dupre and Wood, 1988) Necturus maculosus lowers Tb and thermal tolerance when injected with melatomn and chlorpromazme (Erskme and Hutchlson, 1982, Hutchlson, 1981) The purpose of this study was to examme the effects of exogenous cues--hght, t~me of day and *Present address Department of Biology, Maryvdle College, Maryvdle, TN 37801, U S A

season---on temperature selection m Bufo m a r i u s , a resident of lowland tropics where ambient temperatures are fairly stable The effect of time of day on temperature selecUon in B m a r i u s was compared with that of B cognatus a temperate toad which can experience large temperature fluctuations throughout a 24 h period It is hypothesized that B m a r i u s in a hnear thlgmothermal gradient w~th a uniform light source would select warmer Tbs than toads in the gradient with a pomt source of hght over the hot end of the gradient B. m a r i u s occurs m areas where ambient temperatures are stable and therefore should select more constant TbS than temperate B cognatus Because B cognatus lives m an enwronment where it can only be active for a portion of the year it should select higher Tbs than B m a r i u s to increase d~gestlve rate, growth and fat deposition Rana cascadae tadpoles m a montane environment with a short developmental season utilize warm areas of the pond in the early mormng and late afternoon presumably to mcrease growth (Wollmutb et a l , 1987) MATE~LS ANY METHOVS B m a r i u s [213 8 + 47 3 g (mean + SD)] were obtamed from an ammal supply company and B cognatus (47.0 _+ 10 1 g) were collected m the Norman, OK area. Ammals were mamtalned m the laboratory on an LD 12 12 photopenod wRh photophase centred at 12 00 h CST Toads were mamtamed at an air temperature of 25°C, but could elevate their Tbs dunng the photophase by moving under an incandescent light bulb suspended over one end of the cage Toads were fed neonatal mice, crickets or mealworm larvae twice per week Five days prior to the expenmentai period the toads were acchmatized m controlled environmental chambers to a constant 25°C and an LD 12 12

309

310

LV~t,~TTEM SIEVERT Table I The mean body temperature s e l e c t e d b y t o a d s o v e r a 24 h p e n o d a n d SEM Spnng

Fall

B marmus U L

B cognazus L H

267±073No

277+157Yes

B marmus L H

B marmus L H

24 3 + 0 96 No

24 3 _+0 99

Yes

Yes

r e p r e s e n t s the p r e s e n c e o f Slgmficant ¢hfferences m m e a n l h b o d y t e m p e r a t u r e s s e l e c t e d o v e r the 24 h period

photopenod Toads were fasted dunng acchmatazanon, but were provided a constant source of water One day before the expenment each toad was placed into at thlgraothermal hnear thermal gradient wRh floor temperatures ranging from 10 to 40°C Two hghtmg arrangements were used dunng the experiment For the hght at the hot end treatment (LH) a po|nt-souree of hght, a 60 W broad spectrum |ncandescent hght bulb in a reflector, was suspended over the hot end of the gradient This produced an arrangement where one end of the gradient was hght and warm and the other end was cold and dark For the uniform hght treatment (UL) a broad spectrum fluorescent tube was suspended over the entire length of the gradient Ttus allowed the toad to select for heat levels, but not hght mtensmes A 960 ml water contmner was placed at eRher end of the gradient behind a styrofoam partltmn that prevented the toad access to the container A strip of Handl-gapes (Colgate C o , New York) sewn together to extend the entare length of the gradient sat on the floor of the gradient The ends of the Handi-wlpes were placed in the water containers and acted as wicks wluch kept the floor of the gradient wet The floor of the gradient was made of 0.3 cm thick alununum which was approx 18 x 210 crn The walls [

32

'

i

,

RESULTS

There were no slgmficant differences in the mean Tbs of the B marmus groups. NeRher light treatment nor season influenced means TbS over the 24 h period The spnng UL and LH B marmus groups showed no differences m TbS dunng any hours oftbe expenment (Table 1) The B cognatus had lugher mean TbS (P < 0 01) than the larger B marmus and chose slgmficantly bagher Tbs from 16 00 to 17 00 h CST than from 05 00 to 06 00 h CST The spnng UL group had

i

Bufo marlnus

spring

UL-

32

28

28

26

26

24

24

22

22

20

.

i

.

t

,

i--

'

] 900

'

2 3I 0 0

,

0 3 0I 0

i

.

0 7I0 0

,

18 i

I

1500

~

I

1900

i

i

23100 03'00

,

07'00

.

lIO0

'

q~ O_

32

F

30

30

28

28

26

26

24

24

22

22

20

20

18

t

20

18

© F--

•

30

30

CD

of the gradient were 18 cm lugh and the top of the gradient was covered wRh a thin sheet of acryhc Approx 0,5 h prior to the expenmental period each toad was removed from its thermal gradient and a copper-constantan thermocouple was inserted 1-2 cm into the cloaca The exiting w~re was wrapped m thin-walled polyurethane tubing and was suqgcally stapled to the dorsal surface of the toad Body temperatures were monitored at 10-rmn intervals for 24 h beginning at 12 00 h CST In the spnng (May-June) one group of B m a r m u s was exposed to the UL treatment and a second group was exposed to the LH treatment In the fall (September) one group was exposed to the LH treatment Also, one group of B cognatus was subjected to the LH treatment In all treatment groups the sample raze was 8 An equal number of male and female toads were used and no ammals were used twice A two-way repeated-measures analysis of vanance (ANOVA) was used to compare mean TbS among groups and the pattern of temperature selection over tame (temporal pattern) Tukey's test was used to determine whtch hours of the day toads selected slgmficantly different TbS Means were considered slgmficantly different at P < 0 05

i

i

i

'

i

,

Bufo marmus

i

I

I5OO

i

I

tgoo

i

~'oo

i

i

•

spring

i

03'o0 o4oo

i

LH-.

i

15i00

i

32

i

i

,

i

rio0

i

Bufo rnarmu~

f a l l LH

18

11oo

'

15| O0

'

L 1900

,

2 3i 0 0

.

03tO0

,

0 7J0 0

.

I tO0

T~me of Day Ftg I Temperature selection ofB marmus and B cognatus over a 24 h penod m a hnear thermal gradient Each c~rcle~s the mean body temperature of 8 toads over a 1 h interval Verttcal hnes represent I SE above the mean Dark honzontal hnes represent the scotophase

Toad thermoregulataon shghtly (2.4°C) but not sigmficantly ~gher mean TbS than the spnng LH group over the 24 h penod (Table 1, Fig 1) DISCUSSION

Contrary to the author's prediction, B marlnus & d not select significantly higher mean TbS in the UL condllaon than m the LH condmon Although the UL group showed slightly elevated TbS over the 24h penod and very constant Tbs throughout the test period, there was no evidence to support the hypothesis that in B marznus temperature selection was a function of hght posmon The Tbs dunng some portions of photophase were slgmficantly lower than Tbs d u n n g some portions of scotophase for the fall LH control group (Table 1) The spnng LH group showed the same trend of lower photophase Tbs, but the d~fference between day and mght Tbs was not s~gmficantly different This pattern was absent m the UL group which could not select for light intensity Rather than influencing mean Tb, light may play a role m how temperature is selected over time (Fig 1) T~me of day ~s an important factor in temperature selection in reptdes (Smevert and Hutcluson, 1989), but th~s has not been demonstrated in many amphibians N maculosus showed a dlel cycle m temperature selection with the highest preferred Tbs occurnng d u n n g scotophase, the animals' activity period (Hutchison and Spnesterbach, 1986) Rana plplens tadpoles exhibited a bimodal cycle of temperature seleclaon Mean photophase and scotophase Tbs did not differ, but Tb decreased dunng the switch from scotophase to photophase (Casterhn and Reynolds, 1978) In other species of amphlbmns no dlel cycles of temperature seleclaon have been observed (Ldlywh~te, 1971, Woolmuth et a l , 1987, Kluger, 1977) Some species of amphlbmns may display diel cycles of preferred temperature and others may not An alternate posslblhty is that the presence or absence of dlel cycles m temperature seleclaon may be a function of exogenous factors such as light and season This would appear to be the case with B marmus D u n n g the spnng the LH group showed no s~gnlficant difference in temperature seleclaon over time, whereas m the fall the LH group did show sigmficant differences in Tb over lame The mean selected temperature was not influenced by season This is in contrast to tadpoles (R plplens and R catesblena) and mudpupples which showed seasonal shifts in preferred temperature (Lucus and Reynolds, 1967, Hutchlson and Spnesterbach, 1986) In reptiles the highest Tbs are selected dunng activity for both diurnal (Slevert and Hutchlson, 1989) and nocturnal lizards (Slevert and Hutchison, 1988, Bennett and John-Alder, 1986) B marlnus is primarily nocturnal and the highest Tbs in the LH groups were selected at night Peak levels of oxygen consumption also occurred at the onset of scotophase mn B martnus acchmated to the LD 12 12 photoperiod This cycle of oxygen consumplaon was a funclaon of alternating light and dark penods and was absent under LL or DD conditions (Hutchison and Kohl, 1971) B cognatus selected hagher TbS than B martnus, parlacularly d u n n g photophase Unlike B marlnus

311

which selected their coolest TbS d u n n g rmdphotophase, B cognatus chose their coolest TbS d u n n g late scotophase The difference in mean Tb was not due to s~ze alone T h e B cognatus spent more lame m the hotter parts of the gradient and both species could readily elevate their TbS to over 30°C In summary, the mean selected TbS In B marmus over a 24 h period were not influenced by season or hght regime. In contrast, the pattern of temperature seleclaon over a 24 h penod was altered by season in the LH groups The temperate B cognatus selected significantly higher mean TbS over a 24 h period than the tropical B marmus in the fall The pattern of temperature seleclaon over time was different between the two specaes T h e B cognatus selected their lowest TbS dunng late scotophase and the B marmus selected their lowest Tbs d u n n g rmdphotophase Acknowledgements--Specaal thanks 8o to D Mullens for

assistance w~th ammal care and experimentation and to V H Hutcluson for advace, use of eqmpment and critical revaew of the manuscript I thank G Slevert for catclung the B cognatus, W. Porter for construclang the equipment and the Department of Zoology at the Umverslty of Oklahoma for partial funding of this project REFERENCES

Avery R A (1982) Field studies of body temperatures and thermoregulataon In Bwlogy of the Reptdla, Vol 12 (Edited by Gans C ), pp 93-165 Acadermc Press, New York Bennett A F and John-Alder H 0986) Thermal relations of some Austrahan skmks (Sauna Scmcldae) Copeta 1986, 57--48 Brattstrom B H (1965) Body temperature of reptdes Am Midl Nat 73, 376-422 Brattstrom B H (1979) Amphibian temperature regulation studies in the field and laboratory Am Zool 19, 345-356 Casterlln M E and Reynolds W W (1978) Behavloural thermoregulatton in Rana p~pwns tadpoles J therm Bwl 3, 143-145 Duellman W E and Trueb L (1985) Biology of Arnphlblans McGraw-Hill, New York Dupre R K and Wood S C (1988) Behavioral temperature regulation by aquatic ectotherms dunng hypoxta Can J Zool 66, 2649-2652 Erskme D J and Hutchlson V H (1982) Reduced thermal tolerance in an amphibian treated with melatonm J therm Bwl 7, 121-123 Feder M E (1982)Thermal ecology of neotropical lungless salamanders (Amptubia Plethodontidae) environmental temperatures and behavmral responses Ecology 63, 1665-1674 Heath A G (1975) Behavioral thermoregulatlon m high altitude tiger salamanders, Ambystoma ttgrmura HerpetoIoglca 31, 84-93 Hutchlson V H and Kohl M A (1971) The effect of photopenod on dally rhythms of oxygen consumption tn the tropical toad, Bufo marmus Z vergl Phystol 75, 367-382 Hutchison V H and Kohl M A (1981) Pharmacological studies on the behavioral thermoregulation m the salamander, Necturus maculosus J Iherm Bwl 6, 331-339 Hutcluson V H and Spnestersbach K K (1986) Did and seasonal cycles of acuvlty and behavioral thermoregulatton in the salamander Necturus maculosus Copeia 1986, 612-618 Kluger M J (1977) Fever m the frog Hyla cmerea J therm BIol 2, 79-81

312

LVNm~MSIEv~RT

Lfllywhlte H B (1971) Temperature selecUon by the bullfrog, Rana catesbetana Comp B:ochem Physwl 4OA, 213-227 Llllywl"ate H B (1975) Physiological correlates of basing m amplublans Comp Bwchem Physwl 52A, 323-330 Lfllywhlte H B, L~cht P and Chelgren P (1973) The role of behavioral thermoregulaUon m the growth energetlcs of the toad, Bufo boreas Ecology 54, 375-383 Lucas E A and Reynolds W A (1967) Temperature selection by amphthsan larvae Phystol Zool 40, 159-171 Pearson O P and Bradford D F (1976) Thermoregulatlon

of hzards and toads at high alutudes m Peru Copeta 1976, 155-170 Slevert L M and Hutchlson V H (1988) Light versus heat thermoregulatory behavior m a nocturnal hzard (Gekko gecko) Herpetologlca 44, 266-273 Slevert L M and Hutchlson V H (1989) Influence of season, Ume ofday, hght and sex on the thermoregulatory behavlour of Crotaphytus collarts J therm Bwl 14, 159-165 Woolmuth L. P , Crawshaw L I , Forbes R B and Grahn D A (1987) Temperature selecuon dunng development in a montane anuran spe~es, Rana cascadae Physwl Zool 60, 472--480