J. therm. Biol. Vol. 7, pp. 23 to 28, I982 0306-4565182,010023-06$03.00/0 Printed in Great Britain. All rights reserved Copyright ¢) 1982 Pergamon Press Ltd

ENVIRONMENTAL VARIABILITY AND THERMAL ACCLIMATION OF METABOLISM IN TROPICAL

ANURANS

MARTIN E. FEDER Department of Anatomy and Committee on Evolutionary Biology, The University of Chicago,

1025 E. 57th Street, Chicago, IL 60637, U.S.A.

(Received 13 May 1981, accepted 16 June 1981)

Ahstraet--l. Capacity for thermal acclimation of oxidative metabolism was examined in five species of tropical anurans. Animals were acclimated at 20 or 30°C, and their routine rates of oxygen consumption determined at 20 and 30°C.

2. Acclimation had little effect on oxygen consumption in four of five species; by contrast, Rana erythraea showed significant inverse acclimation of metabolism and a remarkably high temperature coefficient (Qto) of metabolism.

3. Prolonged acclimation (27 days) did not affect oxygen consumption of Bufo marinus. 4. Of 29 species of amphibians examined to date (7 tropical, 22 temperature zone), all temperate-zone

species show significant acclimation of metabolism, all but one tropical species show no acclimation.

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

THERMAL acclimation is one of several processes by which ectotherms compensate for variation in body temperature. Because thermal acclimation is a re- sponse specifically to variation in temperature, many workers have sought to characterize acclimatory dif- ferences between ectotherms from variable and con- stant thermal environments (reviewed by Feder, 1978). In practice, most studies have compared organisms from the tropics and the temperate zones; the tropics, in general, have less variable thermal regimes at any given elevation than the temperate zones (Janzen, 1967).

Although tropical amphibians typically have higher critical or lethal temperatures than temperate-zone amphibians (Snyder & Weathers, 1975), amphibians from both regions are similar in their ability to undergo acclimation of lethal temperatures (Bratt- strom, 1968, 1970a, b, 1979). Instances of limited accli- matory ability are evident among both the tropical and temperate zone amphibian fauna (Brattstrom, 1968, 1970a). The lack of a correlation between bio- geographic region and acclimatory ability may be due to several factors. Microhabitats exploited by am- phibians, may be equally variable in both the tropics and the temperate zone, or amphibians may thermo- regulate behaviourally and thereby moderate (Bratt- strom, 1979) or accentuate (Lillywhite et al., 1973) their thermal variability. Few long-term records of body temperatures of individual amphibians in the field are available to examine either of these possibili- ties. However, the evident capabilities for behavioural thermoregulation and the paucity of field body-tem- perature records that are at or near lethal tempera- tures suggest that amphibians generally do not experi- ence extreme temperatures (Feder & Pough, 1975). Hence biogeographic differences in acclimatory ability may be more pronounced in "capacity" for maintenance, growth and reproduction within the

zone of tolerance rather than "resistance" acclimation (Feder, 1978).

To evaluate biogeographic differences in acclima- tion of "capacity", a previous study (Feder, 1978) compared thermal acclimation of metabolism in trop- ical and temperate-zone salamanders. Two tropical species showed much more limited abilities to undergo acclimation of resting rates of oxygen con- sumption than two temperate-zone species. The present study extends this comparison by considering thermal acclimation of metabolism in five species of tropical anuran amphibians from the Philippines. Although results are not uniform, tropical anurans also appear to lack acclimatory abilities evident in their temperate-zone counterparts.

M A T E R I A L S A N D M E T H O D S

Collection and maintenance of animals

Specimens of Bufo marinus, Rana cancrivora and Rana erythraea were collected in rice fields at sea level in Duma- guete, Negros Orientale, Philippines. Rana maona were taken along a stream bank at 150 m elevation at Palimpi- nan, Negros Orientale. Ooeidozyoa laevis (Ranidae) were taken in streams flowing into Lake Balinsusaya, Negros Orientale, at 900 m elevation. AIcala (1962) has described these localities.

Animals were taken to the laboratory at sea level and held in tapwater in plastic boxes under a L-D 12:12 photoperiod centered at 1200 local time. Animals were unfed throughout experimentation.

Experiment 1 For each species, animals were sorted into two groups of

similar body-size distributions, and the groups were held at either 20 :l: 0.5°C or 30 + 0.5°C for 7-8 days before experi- mentation. These temperatures are designated acclimation temperatures (AT). Following this period, routine rates of oxygen consumption were measured at both 20 + 0.1°C and 30 + 0.1°C. This temperature is termed the experimen- tal temperature (ET).

23

24 MARTIN E. FEDER

o20i oOlO M M A O.I O~ '7

co O0 O0 20 o 30 ° 20 ° 30 u

~ 0.1 0.1 u

- 6 oo oo t~ 20 o 30 o 20 ° 30e

2 0.,~ R. magna

02

Ot ~

oo 20 ° 30 °

Experimental temperature °C

Fig. I. Effect of acclimation temperature (AT) on mass- corrected routine metabolic rates of tropical anuran spe- cies. At each experimental temperature (ET), open bars indicates rates for 20°C AT animals and shaded bars indi- cate rates for 30°C AT animals. Means are plotted :1:95% confidence intervals; n = 6 for each group. Table 1 in-

cludes a statistical analysis of these data.

The rate of oxygen consumption (I;'o2) was measured in constant pressure Seholander respirometers (Scholander, 1950) constructed from glass jars, rubber stoppers and ca- pillary tubing. A plastic bag containing 10% KOH (a COt absorbent) was suspended within each respirometer. Both the experimental chamber and the reference chamber in each respirometer contained small amounts of tapwater. Animals were introduced into respirometers, and respir- ometers were placed in water baths inside temperature chambers regulated at the ET. After 2-3 h for equilibration, respirometers were sealed to begin measurements. Oxygen consumed by animals was replaced with atmospheric air from a syringe. 17o2 was calculated from the amount of air injected, and is reported in ml O2 STPD.hr-1. Precision of measurements was 5-50 #1. Two to five sequential measure- ments of 10-30 min each were averaged for each individual. Sequential measurements of f'o2 undoubtedly produced some decline in oxygen concentration throaghout the measurements. However, no consistent increases or de- creases in 17o~ that might be attributable to hypoxia were evident in later measurements for individual animals. All measurements were made between 1000 and 1.500 local time.

Effects of ET, AT, and body size on I?o~ were analysed with the analysis of covariance procedure in the SPSS MANOVA software package (SPSS, Inc., Chicago, Illinois U.S.A.). Each species was analyzed separately. For each species, Po~ was measured for 24 individuals, i.e. 6 individ- uals for each combination of ET (20 and 30°C) alfd AT (20 and 30°C). Loglo body size and Ioglo I?o~ were used in the analysis of covariance. Significant variation in Ioglo Po~ due to AT alone is designated "thermal acclimation".

To display results in graphical form (e.g. Figs 1-2), values of F'o~ for each animal were transformed through division by M °'s, where M is body size in g and 0.8 is the average of allometric coefficients relating Po~ to M in anurans (Hutchison et al., 1968; Whitford, 1973). These

transformed values are termed "mass-corrected I7o~'. This procedure yields only an approximation of trends in the data for purposes of illustration; all conclusions are based on the analysis of covariance.

For B. marinus, R. cancrivora, and R. erythraea, samples were sufficiently large that individual animals were measured only once. For O. laevis and R. rnagna, animals were held 7-8 days at the alternate AT after the first measurement, and remeasured.

To examine the time of course of thermal acclimation, B. marinus were held at either 20 AT or 30°C AT for up to 29 days, and then their 17o~ was measured according to the above procedure. Analysis of covariance was used to test for significant acclimation.

Experiment 2 Animals were held at 15, 20, 25, 30 or 35 _+ 0.5°C AT,

and their 17o2 determined at ET equal to AT. Measurement procedures were as described above. In some cases, no animals survived the acclimation period at extreme ATs or samples were inadequate for measurements at all tempera- tures.

Temperature coefficients (QLo) were computed according to the formula:

QIo ffi (R,/R1)exp(lO/T, - TI))

where 7"2 and TI are ETs, and R, and RI are mean mass- corrected I?o2 at 7"2 and TI, respectively.

R ESU LTS

In three of five species (R. cancrivora, R. magna and O. laevis), acclimation clearly had no significant effect on log I?o2, and interaction between AT and ET was not significant (Table 1, Fig. 1). By contrast, in R. erythraea AT significantly altered I:'o~. Acclimation to 30°C increased mass-corrected I?o~ by 41% at 30°C ET. Interaction of ET and AT had no significant effect. In B. marinus, the effect of AT alone was not significant (P = 0.143), but A T - E T interaction yielded P -- 0.068. This near-significant interaction makes it

i ~ 0.10[

- - (81 3 0 A T E 0.00" 7 14 21 28 ~ °3°t B ..~_ E T = 3 ° , . , , =o .~oao] "~ 0

"O 0.101 2 0 A T

0.00, 7 14

Days at AT

Fig. 2. Effect of duration of acclimation to the experimen- tal temperature on mass-corrected metabolic rates of Bufo marinus. Vertical line indicates range of values; horizontal line indicates mean; open rectangle indicates mean _+ 95% confidence intervals; n ffi 6 for each group except where noted below figure. For comparison, metabolic rates after acclimation to the alternate temperature are shown to the right of each figure. (a) Experimental temperature ffi 20°C;

(b) Experimental temperature = 30°C.

Thermal acclimation in tropical anurans

Table 1. Effect of acclimation temperature (AT), experimental temperatue (ET) and Iogto body mass on log10 of oxygen consumption (17o2) in tropical anuran species: analysis of covariance*

25

Degrees Species Source of of variation Freedom B. marinus R. raagna R. cancrirora R. erythraea O. laeris

Log10 mass 1 0.835 0.628 0.255 0.022 0.454 41.600 17.254 7.673 1.872 30.187

<0.001 0.001 0.014 0.190 <0.001 ET 1 1.076 0.796 0.494 0.649 0.277

53.568 21.864 14.871 54.034 18.387 <0.001 <0.001 0.001 <0.001 0.001

AT 1 0.048 0.000 0.023 0.061 0.015 2.368 0.000 0.686 5.091 0.970 0.143 1.000 0.420 0.038 0.339

Interaction of 1 0.077 0.001 0.031 0.020 0.002 ET and AT 3.829 0.016 0.942 1.666 0.148

0.068 0.902 0.346 0.215 0.706 Lack of parallelism 3 0.007 0.033 0.010 0.033 0.006

0.365 0.908 0.296 2.784 0.417 0.779 0.459 0.828 0.075 0.743

Within cell error + 16 0.020 0.036 0.033 0.012 0.015 residual . . . . . .

Range of mass (g) 41.7-160.3 11.1-57.3 4.7-36.2 13.1-24.9 3.6--15.0

* In each cell of the table, the upper number is the mean square for the indicated factor, the middle number is F, and the lower number is P of F. Details of the analysis are provided in the text. For each species, n = 24, The table also furnishes the range of body size for each species.

difficult to classify B. marinus as showing either sig- nificant acclimation of 17o2 or not acclimating. More lengthy exposure to 30°C AT (Fig. 2) reduced the dif- ference in 17o2 between 20°C AT and 30°C AT animals (Fig. 2). Therefore, I tentatively classify B. marinus as showing no acclimation of 17o2, but recognize that the alternative classification is also tenable. Obviously further measurements would clarify this situation.

Absence of acclimation, as defined above, may be due either to actual absence of acclimation or to very slow acclimation. To test for slow thermal acclima- tion, B. marinus were held at the AT for up to 29 days (Fig. 2). Length of exposure to the AT had no signifi- cant effect upon log 17o~ either for 20°C AT animals measured at 20°C ET (F3.18 -- 2.339; P -- 0.108), or for 30°C AT B. marinus measured at 30°C ET (Ft.7 = 3.960; P--0.087). At both ETs no ~o: for 20°C AT ever differed significantly from any Vo~ for 30°C AT (P = 0.05).

Table 2 presents the effect of temperature upon I;'o~ in anurans that had been held at the ET 7-8 days prior to measurement. With the exception of those for R. erythraea, Qt0s of 17o~ ranged between 1.12-3.32. For R. erythraea, however, the Q10 of I7o2 between 15-20°C ET was 18.95, and the Qt0 between 20-25°C ET was 4.33. Data for R. cancrivora at 15°C ET are unavailable because all specimens died during the acclimation period.

DISCUSSION

Tropical-temperate d(fferences in capability for accli- mation

These results extend the generality of a conclusion previously based upon measurements of only two spe-

cies of tropical salamanders (Feder, 1978): a positive correlation between environmental thermal variability and capacity for thermal acclimation of 17o2 in am- phibians. Of the five species of tropical anurans exam- ined, three species failed to show significant thermal acclimation of metabolism and a fourth (B. marinus) showed no significant acclimation at 20°C ET, and possibly none at 30°C ET. These data are placed in a larger, comparative context in Table 3, which reviews all studies to date of thermal acclimation of whole organism metabolism in amphibians. These studies account for 22 species of temperate zone amphibians (12 anurans, 10 urodeles); all show significant thermal acclimation of metabolism. Seven species of tropical Amphibia have been examined (2 salamanders, 5 anurans); only one species, R. erythraea, unequivo- cally shows acclimation of 17o Moreover, tropical- . . 2"

temperate differences in ablhty to undergo thermal acclimation of I;'o~ contrast with the pattern for acclima- tion of lethal or critical temperatures, in which trop- ical and temperate zone amphibians show no consist- ent differences (Brattstrom, 1968, 1970a; Feder, 1978).

Of particular note are the taxonomic affÉnities of the species listed in Table 4. Ranid frogs are prepon- derant among both the tropical and temperate zone species. The representation of ranids in both zoogeo- graphic categories and the diverse systematic status of the other species examined suggest that the observed pattern is indeed correlated with differences between the tropics and the temperate zone, rather than with the genera, families, or orders of the species studied to date.

A recent study of larvae of the frog Limnodynastes peroni (Leptodactylidae) (Marshall & Grigg, 1980) found no acclimation of metabolism in this species.

26 MARTIN E. FEDER

Table 2. Effect of temperature on routine rates of oxygen consumption in five species of tropical anurans

Experimental temperature CC) 15 20 25 3O 35

B. marinus 57_+4 65_+5 79_+ 13 144+_29 206_+5 4 6 6 6 3

- - 1.30 1.48 3.32 2.05 70___ 10 88 + 12 149___28 158 + 15 181 + 2 3

3 6 4 6 2 - - 1.58 2.87 1.12 1.31

Died 93 + 18 141 + 3 2 2 0 2 + 2 5 3 6 7 + 4 3 6 6 6 3 - - 2.30 2.05 2.05

1 7 + 7 7 4 _ 11 154_+26 202 + 13 367 + 4 5 3 6 6 6 4

- - 18.95 4.33 1.72 3.30 83 + 19 169 + 15

6 6 - - 2.04

O. laeris

R. cancricora

R. erythraea

R. magna

Tabled values are mean 17o2 (in #1 O2 .g - °8 .h - t ) __ SE, sample size, and Qto of oxygen consumption between indicated temperature and the next lowest temperatures for that species. All animals were acclimated to the experimental temperature for 7-8 days before measurement.

Table 3. Acclimation of routine oxygen consumption in amphibians as related to order and zoogeographic status

AMPHIBIANS SHOWING SIGNIFICANT ACCLIMATION OF METABOLISM

Reference Anura

Acris crepitans Bufo boreas Bufo woodhousei Hyla regilla Pseudaeris triseriata Rana catesbeiana Rana esculenta Rana pipiens Rana ridibunda Rana temporaria Rana virgatipes Rana erythraea*

Caudata Batrachoseps attenuatus Desmognathus fuscus Desmognathus ochrophaeus

Eurycea multiplicata Notophthalmus viridescens Plethodon dorsalis Salamandra atra Taricha torosa Triturus alpestris Triturus valgaris

Dunlap (1969, 1971, 1980) Bishop & Gordon (1967): Carey (1979a) Fitzpatrick & Atebara (1974) Jameson et al. (1970) Packard (1972); Dunlap (1980) Weathers (1976) Stangenberg (1955); Locker & Weish (1966) Rieck et al. (1960); Parker (1967); Jones (1972) Rozhaga, cited in Altman & Dittmer (1966) Grainger (1960); Jankowsky (1960): Harri (1973) Holzman & McManus (1973) Present study

Feder (1978) Fitzpatrick et al. (1972) Fitzpatrick et al. (1971): Fitzpatrick & Brown (1975) Brown & Fitzpatrick (1981a) Rieck et al. (1960); Pitkin (1977) Brown & Fitzpatrick (1981b) Knapp (1974) Feder (1978) Pocrnj'ic (1965); Knapp (1974) Pocrnjic (1965)

AMPHIBIANS SHOWING NO ACCLIMATION OF METABOLISM Anura

Bufo marinus* Limnodynastes peroni Rana cancrivora* Rana magna* Ooeidozyga laevis*

Caudata Bolitoglossa occidentalis* Pseudoeurycea smithi*

Present study Marshall & Grigg (1980) Present study Present study Present study

Feder (1978) Feder (1978)

Asterisks indicate tropical species; temperate zone species are unmarked.

Thermal acclimation in tropical anurans 27

The bearing of this finding on the present study is uncertain, partly because the range of this species in- cludes both the tropics and the temperate zone. Mar- shall and Grigg attribute lack of acclimation in Lim- nodynastes larvae to reduced thermal variability in exclusively aquatic habitats. If this explanation is suf- ficient, then aquatic amphibians in general should lack capacity for thermal acclimation of metabolism. However, four species of aquatic amphibians from the temperate zone, including larvae of R. pipiens, do undergo acclimation of I7o2 (Pocrnjic, 1965; Parker, 1967; Pitkin, 1977).

Rate of thermal acclimation is an additional vari- able that may affect interpretation of tropical-temper- ate zone differences in acclimatory capacity. Dunlap (1969) reported that thermal acclimation of metab- olism is complete within 4 days in the temperate zone anuran Acris crepitans. By this standard, 7-8 days exposure to the AT in the present study should be adequate to induce acclimation if it occurs, and accli- mation did occur within this time in R. erythraea. The data, however, do not exclude the possibility that ex- tremely slow acclimation of metabolism occurs in tropical amphibians. Yet, no acclimation of metab- olism with a time course greater than 7 days has been reported for any amphibian. In B. marinus, 29 days of exposure to an AT were insufficient to induce thermal acclimation of metabolism, and up to 75 days were insufficient in larvae of Linmodynastes peroni (Mar- shall & Grigg~ 1980).

The frog R. erythraea is exceptional in being the only tropical species to show thermal acclimation of metabolism and in having the highest Qto of I7o~ in the present study. The ecological significance of these features is enigmatic, as R. erythraea is microsympa- tric with B. marinus and R. cancrivora at the collection site.

The ability to undergo acclimation of I7o2 does not appear to result in major changes in the Qt0 of I7o~ for amphibians. With the exception of the Qlo for R. erythraea, Qtos of acclimated Vo, for tropical anurans in this study (Table 3) do not differ markedly from Qtos previously reported for temperate zone anurans {Hutchison et al., 1968). Tashian & Ray (1957), Hut- chison et al. (1968) and Weathers & Snyder (1977) reached the same conclusion previously.

Consequences of tropical-temperate zone differences

The ecological consequences, if any, of a limited ability to undergo acclimation are unclear at this time and require further analysis. A first step would be to gather detailed temperature records for individual amphibians in the field to document actual differences in thermal variability. Few such records exist (reviewed by Carey, 1978); the only available study of body temperature in a free-ranging tropical amphib- ian (Pearson & Bradford, 1976) reports diel variation of 20°C for a montane toad. This record may not be typical of tropical amphibians, but is certainly at vfiri- ance with the notion of reduced thermal variability in the tropics.

Despite the paucity of reliable field data, some workers have analyzed geographic and altitudinal range size to discern possible correlates of acclimatory ability. Species with limited acclimatory ability might be able to live and reproduce in only a narrow clima-

tic range (Janzen, 1967; Feder, 1978; Huey, 1978). Hence a consequence of limited ability to undergo thermal acclimation of I?o~ may be a limited geo- graphic range. Indeed, Huey (1978) inferred from measurements of faunal overlap that tropical amphib- ians (shown to have limited acclimatory ability in the present study) and reptiles have more narrow alti- tudinal ranges than their temperate zone counter- parts. Similarly, Brattstrom (1968, 1970a) reported that amphibian species with limited geographic ranges showed lesser abilities to undergo acclimation of the critical thermal maximum than species with large ranges.

A problem with unambiguously assigning ecologi- cal consequences to a given pattern of thermal accli- mation is that variation in body temperatures and lack of thermal homeostasis is apparently important to many amphibian species. Some forms rely on vari- ation in body temperature to minimize energy re- quirements at low temperatures and maximize 17o2 at high temperatures (Lillywhite et al., 1973; Brattstrom, 1979; Carey, 1979b). To this end, patterns of acclima- tion that increase the Qlo of I>o, may be beneficial to some amphibians, and acclimation resulting in ther- mal homeostasis may sometimes be counterproduc- tive. For example, lack of acclimation or inverse accli- mation may enable salamanders to overwi:ater with- out starving. If salamanders were to compensate for cool winter temperatures by increasing I:'o~, their caloric reserves would be insufficient to sustain them during the inactive season (Fitzpatrick, 1973a, b; Fitz- patrick & Brown, 1975). Hence, it seems illogical to assert that all tropical amphibians are unable to exploit wide ranges because they lack the ability to undergo acclimation of Vow.

Acknowledoements--I thank R. Huey, M. LaBarbera, H. Pough, A. de Ricql6s, T. Taigen, J. Teeri and B. Brattstrom for their helpful comments on the manuscript; George, Amy, Ari Gorman, J. Feder, C. Lumhod and B. Gargar for aid in collection of experimental animals; anc~ A. C. Alcala for hospitality and use of his laboratory facilities. Research was supported by NSF Grant DEB 78-23896 to the author, The Andrew Mellon Foundation, The Louis Block Fund of The University of Chicago, and a National Geographic Society Grant to George Gorman.

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Key Word Index--Acclimation: amphibian: Anura; environmental variability; metabolism; temperature; ther- mal acclimation: tropical.