Thermal selection of bullfrog tadpoles (rana catesbeiana) at different stages of development and acclimation tempeatures

Thermal selection of bullfrog tadpoles (rana catesbeiana) at different stages of development and acclimation tempeatures

J Thermal Biology Vol 3, pp 57 to 60 Pergamon Press Lid Printed In Great Britain 0306-4565 78 0,.101-0057 $0200,0 THERMAL SELECTION OF BULLFROG TADP...

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J Thermal Biology Vol 3, pp 57 to 60 Pergamon Press Lid Printed In Great Britain

0306-4565 78 0,.101-0057 $0200,0

THERMAL SELECTION OF BULLFROG TADPOLES (RANA CATESBEIANA) AT DIFFERENT STAGES OF DEVELOPMENT AND ACCLIMATION TEMPERATURES V. H. HUTCHISON AND L. G. HILL Department of Zoology, University of Oklahoma, Norman, Oklahoma 73019, U.S A

(Received 19 July 1977; accepted 6 October 1977)

Abstract--l. Mean preferred temperatures (PT) of bullfrog tadpoles were determined in a laboratory thermal gradient at five stages of development (Gosner stages 25-26, 35-36, 39-40, 41, 43-44) and four acclimation temperatures (AT) (4.4, 15.5, 26 7 and 35°C). 2. Previous thermal history interacts with stage of development in a complex manner, at the earliest stage studied (25-26) high A T resulted in a PT lower than those at an intermediate AT; at stages 43-44 an increased ATresulted in an elevated P T a t all stages; at some combinations of stage and AT the distribution of PT was bimodal; some combinations of early stage and low A T produced strongly truncated distributions of P T a t the cold end of the gradient. 3. The overall mean P T for all groups was 20 66°C and the mode, 20 97°C. The greatest variation among the A T groups was at the highest A T (35°C) and, among the developmental stages, at the most advanced stage (43-44). 4. Previously reported seasonal progressions in the P T of anuran larvae may be due to the stage of development rather than to seasonal progression per se. 5 The plasticity of the P T in response to ATmay be a strategy to circumvent deleterious consequences of rapid thermal change or extremes and aid in maintaining body temperatures as near the bmchemical and physiological optima as environmental conditions allow.

INTRODUCTION TH~ ADVANTAGESassociated with elevated body temperatures in ectothermic vertebrates have been well documented. Within the range of thermal tolerance an increase in temperature usually increases the metabohc rate, improves locomotion and coordination, accelerates feeding, digestion and assimilation and facilitates growth and development. The optimum temperature for these and other functions are often correlated with the preferred temperature (PT) (Hutchison, 1976). We have followed what now appears to be the more common and accepted usage of the term P T for behavioural thermoregulation in laboratory gradients (Lillywhite, 1971; Hutchison & Hill, 1976). Among amphibians, behavioural thermoregulation is often influenced by the acclimation temperature (AT), but not in some species (e.g., Taricha rivularis larvae and adults, Licht & Brown, 1967; plethodontid salamanders, Spotila, 1972; Ascaphus truei tadpoles, DeVlaming & Bury, 1970). Thermal selection has been demonstrated in adult bullfrogs in the field (Lillywhite, 1970), in juveniles in a laboratory gradient and a discrete choice apparatus (Lillywhite, 1971), and in tadpoles in experimental gradients (Lucas & Reynolds, 1967), but no data were available for tadpoles at specific stages of development and after acclimation to controlled temperatures. This study was designed to determine the interactions of P T w i t h different developmental stages and various experimental thermal histories (AT). 57

MATERIALS AND METHODS Tadpoles m different stages of development were collected from ponds in Marshall County, Oklahoma m June and July and were acchmatlzed in aerated aquaria at 4 4, 15.5, 26.7 or 35 + 0.5°C and a photoperiod of LD 16:8 for a minimum of two weeks. The larvae were fed baby food, boiled spinach and commercial catfish food every two days. Tadpoles were staged according to the simplified table of Gosner (1960). Stages 25-26 were first ,,ear larvae Stage 25 is characterized by a spiracle, formation of a pigmentary pattern, independent feeding and complete development of the operculum. Stage 26 is marked by the presence of a hind limb bud with a length less than one-half the diameter and a well-developed oral disc. In stages 35 and 36 (second year of development) the foot is paddleshaped, but with indentations showing the early development of four and five toes on front and hind limbs, respectively. Stage 39 has metatarsal and subarticular tubercles appearing as light spots; in Stage 40 the tubercles are developed and the cloacal tail-piece is still present. Stage 41 is charactermed by the loss of the cloacal tail-piece and the presence of transparent skin over the forelimbs. Stages 43 and 44 have fully differentiated front limbs and fingers, shortened tails and fins and further metamorphosis of the head, partmularly the mouth (Gosner, 1960, Table 3). Tests in the experimental gradient (183 cm long, 15.2 cm diameter) were conducted from mid-June to mid-August during the photophase to lessen the possible mfluence of seasonal (Feder & Pough, 1975; Lucas & Reynolds, 1967) or diel cycles (Clausen, 1973; Spotlla, 1972). The thermal gradient has been fully described and figured by Hill et al. (1975). Water, precooled to the lowest temperature desired, entered the low temperature end of the chamber and drained from the opposite end into the cold-reservoir

58

V H HtTCHISO", A'~D k G Hill_

to be recycled Hot water ~as introduced at a high temperature end and slowly passed through a series of 10. parallel, small tubelets positioned in the lower one-third of the chamber The tubelets, composed of stainless steel one-th,rd of their length and Plexlglas the remaining twothirds, extended the enure length of the chamber and were separated from the area occupied by the animal with a perforated screen As the cold ~ater moved through the chamber, the water temperature was gradually increased by heat exchange with water in the heated tubelets, which moved in the opposite dlrecnon Thermometers were placed every 7 6cm along the tube Valves on cold and heated water inlets allowed maintenance of a stable gradient, and stratification of water within the tube was prevented by a bar ~lth small paddles x~htch was rotated beneath the perforated screen at 100 rpm The gradmnt was uniformly lighted With a uniform temperature (equal to acchmatmn temperature. AT) throughout the chamber, each test ammal was placed m the gradient and left undisturbed for 15 mm The thermal gradient was then formed and the temperature of the water closest to the head of each ammal was recorded from the nearest thermometer at 30s intervals for periods of 30ram The larvae were observed from a distance with the aid of an mchned m,rror Six to nine different tadpoles were used for each test at each acchmatlon temperature, each individual was used only once in the gradient A statistical comparison of the interactions between stage of development and AT~as not possible due to the following conditions: the blmodal distribution of some samples, the unequal numbers of ammals avadable for observat,ons at each stage, the truncation of dlsmbutlons due to the temperature hmlts w~thln the gradient, and the

significant deflation from a normal distribution ol ,,c~cral samples as determined b.~ Kolmogoro~-Sm~rno~ tests for goodness of fit ISlegel, 1956 Sokal & Rohlf, 1969)

RESLLTS Although the larvae moved along the gradient during the observation periods they tended to concentrate thetr acuvlty about d~fferent temperatures, depending upon thmr previous thermal h,story and stage of development (Fig 1, Table 1) If the gradient was modified spatially by the adjustment of flow rates of the entering heated or cooled water, the larvae had a p r o n o u n c e d prochvxty to concentrate actp, W about the PT. an indmatlon that the posmtlon ~ t t h m the gradient was a response to temperature rather than to other stimuli The interactions between developmental stage and A T are clearly evident (Fig 1, Table 1) In stages 25-26 and 35-36 an increase m A T resulted m an increased PT, except at the highest A T o f 3YC where the m o d e was lower. In stages 39-40 and 41 Increased A T r e s u l t e d m an elevated PT, except m stage 41 at 35'~C ,~here a blmodal distribution is evident In stages 43-44 each increase in A T resulted m a marked elevatmn of PT; the highest P T (V = 25 86) found was for the most developed animals (stages 43-44) at the highest A T (3YC) The lm~est P T (.~ = 10.22-C, mode = 50~C) occurred in tadpoles at stages 35-36 and an A T of 4 4 : C where the d]stnbu-

STAGES 35-36

2 5 - 26

l

~'47

39-40

41

43-44

60

4.4"C (40~F)

IO

o

20 15.5"C

(60"F) lO 0 I,z

,5 = 26.?-c (80"F}

z

_o

2O

(95"F)

"F °C

40 ~ 444

~- 10(3 378

LO0 °F

44;

"'378144;

%78[

444

" 37'81

444"

" ~78

"C

Fig. 1 Thermal selection in Rana catesbeiana tadpoles at fi~e different stages of development and four acclimation temperatures, statistics for each comblnatmn are given m Table 1

Thermal selectmn of bullfrog tadpoles

59

Table 1 Thermal selectmn (PT) durmg five &fferent stages of development and at four acchmatlon temperatures in Rana catesbe~ana tadpoles Acchmatlon (°C)

Stage (Gosner, 1960)

Observations (N)

Mean PT +S.E (°C)

Mode PT(°C)

C I.:*

C÷0 6s (~C)

350

2~-26 35--36 39--40 41 43--44

3264 3305 1575 2025 1480

208 _+013 22.5 _+ 0 11 230 4- 0 16 21.5 -+ 0 17 259_+013

16.7 250 22 2 25.0 306

21.0 15.6 15 7 20 1 115

133--284 162--28 8 16.5--29 3 13 6----284 208--309

26 7

25--26 35--36 3940 41 43--44

3538 1482 2913 1939 2451

25 7 -+ 0 08 206-+017 193 _+ 0 10 216_+013 23.8 _+ 0 14

25 0 175 167 250 278

11 2 175 143 145 164

20 8--30 5 139--273 140---24.6 159--213 17 1--306

155

25--26 35--36 394---40 41 43--44

3016 2665 1561 3831 789

20.9 _+012 207 _+ 0 14 19 8 _+ 0.16 207 +__0 11 21.7 -+ 0 21

195 16.7 16.7 19 5 22 2

176 182 17.2 17 2 15 0

141--27.7 13 7--27 7 13 4---26 3 14 1--27 3 15.8--27 6

44

25--26 35--36 39--40 41 43--44

1904 1767 1706 3144 2869

14.9 -+ 0 12 10.2 -+ 0 15 197 _+ 0 15 18 9 _+ 0.11 20.9 + 0 10

139 50 19.5 19 5 22 2

166 229 17.0 16 7 140

94---20.3 3 8--16 6"{"t 13 3--26 1 12 8--25 0 15 5---264

* Coefticlent of Variation t" Range of Central 68~'o 1"? Calculated value (actual lowest value m gradient 4 4°C) tlon was sharply truncated at the cold end of the gradient (Fig. 1) If all data for each stage are grouped, the grand mean P T for each stage would be: 25-26, 20.57°; 35-36, 18.Y; 39-40, 20.46°; 41, 21.19~; 43-44, 23 07°C. The range of these grand means is 4.57°C. The grand means for each A T with the data grouped for all stages are as follows: 4.4 °, 16.93°; 15.Y, 20.76 °, 22.19°; 35 °, 22 18~C. The range of the latter means was 5.26°C. The overall mean P T for all groups was 20.66°C and the overall mode, 20.97°C. The greatest variation among the different A T groups, as judged by the coefficients of variation (CV) and the ranges of the central 68% (Co 6s), occurred In the animals acclimated to 3YC; among the &fferent developmental stages the greatest variation was in the most advanced tadpoles (stages 43-44) (Table 1). DISCUSSION

The transition from aquatic to aerial breathing in bullfrog tadpoles begins rather abruptly at Stages 41-42 and increases most rapidly through Stages 45--46. The critical phase of respiratory metamorphosis occurs during Stages 42-43 and is completed m about 5 days in animals maintained at 23°C. During this period the larval haemoglobin is replaced by the adult type, DNA synthesis in circulating erythrocytes is accelerated to a peak at Stage 43, blood CO2 tensions increase to a peak at Stage 44, and blood bicarbonate concentration reaches a maximum at Stages 41-42 and remain unchanged into the adult form (Just & Atkmson, 1972; Just et al., 1973). The generally higher P T of tadpoles in Stages 43-44 may be associated with these pronounced metamorphic

TB

32--~

changes. The mode (26--28~C) of the P T of juvenile bullfrogs at an A T o f 25°C (Llllywhlte, 1971) Is similar to that we obtained for Stages 43-44 at an A T of 26.7°C. Lucas & Reynolds (1967) noted a seasonal progression of an increased P T m bullfrog tadpoles tested in a gradient during May-July. Since the stages used are not clear (some were apparently at Stage 30), the increased P T may have resulted from the increased stage of development, rather than from a seasonal progression per se. Our observations mdicate that bullfrog larvae orientate toward a particular temperature, as do juvende bullfrogs (Ldlywhite, 1971), rather than away from a succession of avoided temperatures as reported for some amphibians (Llcht & Brown, 1967). Tadpoles in Stages 25-26 acclimated to the highest ATchose lower PT's than at intermediate AT's. This suggests that the larvae were selecting "optimum" temperatures. A decrease m the P T at an A T above the preferred temperature optimum now appears to be a fairly common response in ectothermic vertebrates, having been reported for fishes (Cheetham et al., 1976), juvenile bullfrogs (Lillywhite, 1971) and lizards CWilhoft & Anderson, 1960; Llcht, 1968; Mueller, 1970); such decreases are likely to enhance survival by lirniling the animals to tolerable temperatures and by optimizing energy utilization. Amphibian embryos normally develop at any temperature within a range of about 15°C, with the upper and lower limits determined genetically. Within the thermal range of survivability the rate of development varies linearly with temperature (Bachman, 1969). Workman & Fisher (1941) found that maximum locomotory activity in Rana pipiens tadpoles occurs at the PT. Species variability of modifications in ther-

60

V H HLTCHISON AND L G HILL

moregulatory beha~ tour V,lth thermal acchmatxon led Llll~wh~te (1971) to conclude that the adaptt',e stgmficance of the plasticity of the P T in response to A T "'remains obscure" We suggest that the adaptive advantages for those species which sho~ a plasttclt? of P T with changes m A T are clear: survival is enhanced by avoidance of lethal temperatures and energetic efficlenc~es are maximized through maintenance of b o d ) temperatures at or near physiological and biochemical optima Such plastlClt) is one of the strategies which ectotherms employ to circumvent the deleterious consequences of rapid changes or thermokmetlc extremes

Acknowledftement--We thank J Plgg for h~s dedicated work and skllful assistance which made this stud? possible

REFERENCES

BACHMAN, K (1976) Temperature adaptations of amphibian embryos Am Nat 103. 115-130 CHEETI-tAM, J L.. GARTEN. C T JR, KINO. C. L. & SMITH, M. H (1976) Temperature tolerance and preference of immature channel catfish {Ictalurus punctatus) Copela 1976(3), 609-612 CLAUSSEN. D L (1973) The thermal relatmns of the tailed frog, Ascaphus truet, and the Pacific treefrog., Hyla regalia Comp Bzochem Phystol 14A, 137-153 DF,VLAMtNG, V k & BURY, R B (1970) Thermal selection in tadpoles of the tailed frog, Ascaphus truer J. Herpetol 4, 179-189. FEDER, M. E & POUGH, F H (1975)Temperature selectmn by the red-backed salamander Plethodon c clnereus (Green)(Caudata Plethodontidae) Comp Blochem. Phys~ol 50A, 91-98 GOSNER, K. L. (19601 A simplified table for staging anuran embryos and larvae with notes on Identification Herpetologwa 16. 183--190 HILL, L. G., SCHNELL. G D & PIGG, J (1975) Thermal acclimation and temperature selectmn in sunfishes (Lepomls, centrarchldae) Southwest Nat 20, 177-184

HbTCHISON, V H (t976) Factors influencing thermal tolerances of individual orgam~ms In Th, rmal txoloq3 II (Edited b y E s c H G W & MCFARLANFR Wt. pp 10-26 U S Energy Research and Development -Xdmmlstratton. National Technical Information Service Springfield. Virginia Ht.TCHISON, V H & HILL, L G (1976~ Thermal selection m the hellbender, Cryptohranchus allegamenszs, and the mudpuppy, Necturus maculosu5 Ht'rpetoloqtca 32, 327-331 JbST, J J & ATKINSON. B 11972) Hemoglobin transmons m the bullfrog Rana catesbelana, during spontaneous and induced metamorphosis J E~p Zool 182. 271--280 LICHT, P & BROWN, A G 11967} Behavioral thermoregulatton and its role m the ecology of the red-belhed newt Tarwha rwularts E~ologv 47. 598 611 LlCHT, P, DAWSO'~, W R SHOEMAKER \ H & NI~,IS, A R (1966) OBSERVATIONSO', THE THtR~I~,L RELATIONS OF WESTERN AUSTRALIAN LIZARDS Copela 1966, 97-110 LILLVWHITE, H B (1970) Behavioral temperature regulation m the bullfrog. Rana catesbelam~ Copela 1970, 158-168 LILLYWHITE, H B (1971) Temperature selectmn by the bullfrog Rana cateshe,ana Comp Btochem Ph3 ~tol 40A, 213-171 LUCAS, E & REYNOLDS, A W (1967) Temperature selection by amphibian larvae Phystol Zool 40, 159-171 MUELLER, C. F (1970) Temperature acchmatlon m two species of Sceloporus Herpetologtca 26. 83-85 SIEGEL, S (1956) Nonparametrtc Stattstws for the Behal Ioral Sc,ences. McGraw-Hill, New York SPOTILA. J R (19721 Role of temperature and v, ater m the ecology of lungless salamanders Ecol ~'~,lono~tr 42, 95-125 WILHOFT, D C & ANDERSON, J D (1960) Effect of acchmatlon on the preferred body temperatures of the lizard, Sceloporus occMentahs Sctence 131, 61(~611 WORKMAN, G. ~ FISHER, K C (1941) Temperature selectton and the effect of temperature on movement m frog tadpoles Am J Phystol 133, 499-500

Key Word Index--Amphibian, behavloural thermoregulatlon, development, frog, preferred temperature, Rana catesbetana, tadpole, temperature acclimation, thermal selecnon