Copeia, 1986(1), pp. 65-69

Thermoregulation and Energetics of a Population of Cuban (Cycluranubila) on Isla Magueyes, Puerto Rico

KEITH A. CHRISTIAN, ILEANA E. CLAVIJO, NANCY CORDERO-LOPEZ, EVELYN E. ELIAS-MALDONADO, MIGUEL A. FRANCO, MABEL V. LUGO-RAMIREZ AND MARISOL MARENGO

Cuban iguanas nubila were introduced to Isla Magueyes, Puerto Rico in the mid 1960's and a reproducing population now inhabits the island. Fourteen -days of body temperatures were obtained by radio telemetry from four male iguanas. Time budgets were recorded simultaneously. The iguanas main- tained a relatively constant body temperature (mean = 38.6 C, SD = 1.4) over a long portion of the day (0915-1800). Midday body temperatures were signifi- cantly higher than those of Galapagos land iguanas, pallidus (during hot season) despite similar microclimatic conditions. By combining body tem- peratures with information on the mass and population densities, it was estimated that the energetic expenditure of the population was approximately 4,800 kJ/(ha x d). This very high estimate of energy expenditure results from the combination of large body size and high population density.

RATES of energy utilization by individual cause it allows measurements of body temper- are very low in comparison to atures (Tb's) while the are free to move mammals and birds of equal size (Bennett and about in a relatively normal state during the Dawson, 1976; Bennett and Nagy, 1977). How- monitoring process. This technique has been ever, the population densities of on some used to monitor Tb's of free ranging tortoises tropical islands are extremely high compared and marine iguanas (MacKay, 1964), bearded to mainland populations (Gorman and Har- dragons (Stebbins and Barwick, 1968), desert wood, 1977; Bennett and Gorman, 1979). These monitors (Sokolov et al., 1975) and Galapagos two confounding factors make it difficult to pre- land iguana (Christian et al., 1983, 1985). dict, a priori, the magnitude of the energetic impact of tropical insular lizards. The rate of MATERIALS AND METHODS respiratory metabolism of the lizard community of the island of Bonaire was found to be greater C. nubila (Cuban Iguana) is the largest than that estimated for populations of small of its (male to 468 mm, female 396 mm mammals in temperate areas (Bennett and Gor- snout-vent length) (Schwartz and Carey, 1977). man, 1979) due to the very great density of It is principally found in Cuba, the Isla de la lizards on that island. The data from Bonaire Juventude, on numerous nearby islets and on indicate that, as suggested by Turner et al. the Cayman Islands (Etheridge, 1982). A few (1976), the energetic role of lizards in some specimens of Cuban Iguanas escaped from a zoo natural communities has not been fully appre- in Puerto Rico and a thriving colony has been ciated. Bennett and Gorman (1979) indicated established on Isla Magueyes off the south- the need for comparative studies from addi- western coast of Puerto Rico since the mid tional populations in order to assess the ener- 1960's (Rivero, 1978). Isla Magueyes is 7.2 ha getic role of lizards from tropical islands relative and is the site of the Marine Sciences Depart- to mainland and temperate lizard and small ment of the University of Puerto Rico, Maya- mammal populations. The purpose of this study guez. It is encircled with mangrove, but the was to determine the body temperatures of free interior of the island consists of a dry scrub ranging and to estimate the en- habitat. ergetic expenditure of the population of igua- Body temperatures were measured by telem- nas on Isla Magueyes, Puerto Rico. etry between 14-18 April 1984. The transmit- Radiotelemetry is a particularly valuable ters were calibrated two days before the study technique for studies of thermoregulation be- was initiated and the calibrations were re-

? 1986 by the American Society of Ichthyologists and Herpetologists 66 COPEIA, 1986, NO. 1

for An- - TA in shade/10 cm suggested intraspecific comparisons by --- TA in shade/2m drews and Pough (1985). The input variables --T- Tsoil in shade included temperature, mass and the -=--Tsoil in sun body body 6C maximum mass for the species, which we as- sumed to be The cost of was o 5C 6,000 g. activity assumed to be 5x the resting metabolic rate. ac 4C This value is an estimate derived from Gleeson's F- c- 3C (1979) investigation of the cost of walking in a. two of subcris- : 2C species large iguanas (Conolophus tatus and Amblyrhynchuscristatus). The energetic 1C expenditure for a 24 h period of a given size of

I II I I I III... I I I .I I I I was calculated the 2 4 6 8 10 12 14 16 18 20 22 24 iguana by summing energy HOUR OF THE DAY expenditure of each time period using the fol- lowing formula: Expended energy = (resting 1. Meanenvironmental for 15- Fig. temperatures MR) x (time + MR) x (time 18 1984 from Isla Puerto Rico. resting) (resting April Magueyes, in activity) x (5). These calculations were made for three size groups (males, females and juve- checked after the transmitters were recovered. niles). Finally, the energetic expenditure for the Temperature sensitive telemetry transmitters entire population was estimated by summing (Model L, Mini-mitter, Sunriver, Oregon), were the contributions of all individuals. concealed in bananas and fed to four male igua- nas. The iguanas were followed continuously RESULTS throughout the day (0600-1900) and temper- ature measurements were made at intervals of Mean environmental temperatures for the five 15 min. During the night, body temperature days during which telemetry measurements were measurements were made at 2130, 2330 and made are shown in Fig. 1. Air temperature had 0330. Simultaneous measurements of behavior a daily maximum during midday hours (1000- (eating, moving around, chasing other iguanas, 1400) of 30.3 C (SD = 0.22) at 10 cm (lizard etc.) and the duration of behavioral activities height) and of 30.0 C (SD = 0.24) at 2 m. Soil were recorded. Body temperature and duration temperatures in the shade were approximately of activity data were analyzed using one-way 3 C warmer than air during midday and almost analysis of variance (ANOVA) and Tukey's the same as air during the morning. Insolated HSD. soil temperatures were high with a mean max- Air and soil temperatures were taken each imum of 53.8 C (SD = 7.56) at 1400. There was hour during the day and when body tempera- a brief shower at 1300 on one day resulting in tures were measured during the night. Air tem- the drop of mean midday soil temperatures in peratures at 2 m and at 10 cm were measured the sun (Fig. 1). using a Keithley thermocouple thermometer in Fourteen lizard-days of telemetry data were conjunction with 30 gauge chromel-alumel obtained from the iguanas. We divided the day thermocouples with their tips painted white to into four periods based on the pattern of Tb's: reduce errors due to radiation (Christian and (1) rapid warming in the morning (0715-0900); Tracy, 1985a). Soil temperatures in sun and (2) midday (0900-1800); (3) rapid cooling in the shade were measured with a Mikron M80A In- evening (1800-2330); and (4) slow cooling frared thermometer. Sky and wind conditions (2330-0715). Mean Tb's for these periods were were qualitatively described each hour. 33.8, 38.6, 35.7 and 30.5 C, respectively, and Censuses of the iguana population were taken these temperatures were used in the calcula- by a single investigator walking the entire island tions of metabolic expenditure (below). Hourly and counting males, females and juveniles. An means of body temperatures for all four iguanas average of the results of censuses taken on 15 are shown in Fig. 2. During midday, Tb's re- Oct. 1978 and 18 Sept. 1983 was used in the mained around an average value of 38.6 C. calculation of metabolic expenditure of the However, when comparing Tb's among individ- population (below). uals, a one-way ANOVA and a Tukey's HSD The resting metabolic expenditure of the revealed that one individual was significantly iguanas was estimated by using the equations warmer (average Tb = 39.4 C). This was true CHRISTIAN ET AL.-THERMOREGULATION AND ENERGETICS OF IGUANAS 67 whether was defined as 0915-1800 midday 42 = 12.4; P < or as 1200-1600 (Fs,144 0.0001) L) 0 4C (F,6, = 4.5; P = 0.007). The iguanas spent the w in burrows. Air were taken ir 38 night temperatures D 1 in the entrance of the burrows and it was found I I- cr 3E that the were 4-5 C warmer than w iguanas Tb's 0- 2 air throughout the night. w 34 amount of time in The average spent activity 32 a I was not different 0 during midday significantly m among the four iguanas (F,, I = 2.36; P = 0.13). 3C 11 Thus, we used the average of all four iguanas 2E in the calculation of the metabolic expendi- 2 4 6 8 10 12 14 16 18 20 22 24 tures. The average amount of time between HOUROF THE DAY and retreat was morning emergence evening Fig. 2. Mean(+ 1 SD) body temperaturesfor four 678 min. The average total time spent in activ- male Cyclura nubila as a function of time of day for ity per day was 91.6 min. Thus, on the average, 14 lizard-daysof observations. 14% of the daily activity period was spent in movement. veniles. The metabolic expenditure of the pop- There were two assumptions made for the ulation of iguanas on Magueyes is, therefore, calculation of metabolic expenditures. We as- approximately 4,803 kJ/(ha x d). sumed that the amount of time females and ju- veniles spent in activity was equal to that of the DISCUSSION males that we studied. The second assumption was that the Tb's for these three groups were The times of emergence each morning and equal. A comparison of midday Tb's of the adults of retiring to the burrow in the evening, were with the midday Tb's of 30 hatchlings caught regular for each iguana, varying no more than between 27 Aug. and 11 Sept. 1983 (Tb's mea- ? 30 min from the mean time of each individual. sured with thermocouples after capture) re- Regularity in the time of morning emergence vealed no difference between the two groups was also noted in Varanus varius by Stebbins and (Fi,4, = 1.4; P = 0.2). Additionally, we captured Barwick (1968). Immediately after coming out a sample of five females and four additional of the burrows iguanas spent time basking in males and measured their Tb's with thermo- the sun. This accounts for the rapid rise in Tb couples. Neither the females nor the males had during the morning hours illustrated in Fig. 2. mean Tb's that were different from the four The stable Tb observed during the midday was = males that were studied by telemetry (F,,, due to shuttling back and forth between the sun 1.0; P = 0.3 and F,,,5 = 0.97; P = 0.6, respec- and shade, or, in some cases, due to the iguanas tively). There were no differences in mean body lying in partial shade. temperatures between the sexes of Galapagos The difference found in midday Tb among land iguanas (Christian et al., 1985). These re- individuals was also observed in the Galapagos sults suggest that our assumption of similar Tb's land iguana, Conolophuspallidus (Christian et al., for all size groups is not unreasonable and that 1985). The mean midday Tb's for five male Co- the four males selected for the telemetry study nolophus ranged between 36.4 and 37.6 C and were representative males. the means for five females ranged between 35.2 Samples of iguanas were caught and mea- and 37.0 C. The mean midday Tb's for the four sured to obtain an average mass for adult males male Cyclura ranged between 37.9 and 39.4 C. (=4,850 g, N = 7), adult females (=2,850 g, Although these represent statistically signifi- N = 6) and juveniles (=1,500 g, N = 2). Using cant differences among individuals of each of the average masses, the mean Tb's from each these groups of iguanas, the differences are time period and the equations of Andrews and nevertheless small. As was the case with the Ga- Pough (1985) we calculated the daily energetic lapagos iguanas, the difference found among expenditure for an individual male (=245 kJ), individual C. nubila was apparently due to dif- female (=171.5 kJ) and juvenile (=111.6 kJ). ferences in thermoregulatory behavior since all From our censuses, we estimated the population the iguanas were approximately the same size. to consist of 91 males, 66 females and 10 ju- These small inter-individual differences prob- 68 COPEIA, 1986, NO. 1 ably reflect an expected amount of biological temperatures) as follows: Sceloporus occidentalis variability in individual behavior. 2-2.5 x (Bennett and Nagy, 1977); Callisaurus The mean Tb's ofC. nubila (38.5 C) at midday draconoides1.5 x; Cnemidophorustigris 3.3 x (An- (assumed to be 1200-1600 for this comparison) derson and Karasov, 1981); Sceloporusgraciosus were significantly greater (F1,.6 = 44.1; P < 2.4x (Congdon and Tinkle, 1982); Sceloporus 0.0001) than midday Tb's of male Conolophus virgatus 2.1-4.6x (Merker and Nagy, 1984); pallidus during the hot season (36.6 C). Even Eremiaslugubris 3.1 x; E. lineoocellata2.2 x (Nagy the individual Cyclura nubila with the lowest et al., 1984); and Amblyrhynchuscristatus 1.7 x mean midday Tb (37.9 C) was significantly (Nagy and Shoemaker, 1984). These results warmer than male Galapagos iguanas (F,,29 = suggest that either our estimates of activity en- 6.95; P = 0.01). The air temperature on Ma- ergy metabolism are conservative, or that Cy- gueyes during this study (Fig. 1) was very similar clura nubila are less active than most of the liz- to the air temperature on Santa Fe, Galapagos ards cited above. Nagy (1982) derived an during the hot season (anuary-May) and the empirical equation to predict the field meta- substrate temperatures on Magueyes were a few bolic rate of iguanids based on the results of degrees less than on Santa Fe (Fig. 1 in Christian studies using doubly labeled water. Using this et al., 1983). This suggests that the difference empirical equation, the estimate for the ener- is due to a difference in preferred Tb rather getic expenditure of the iguanas on Magueyes than differences between the thermal environ- is 3,799 kJ/(ha x d). This result suggests that ments, although the absorbtivity of solar radia- our estimate may be too high. However, the tion may be greater in the darker C. nubila. empirical equation is based on iguanids with C. nubila body temperatures reached a min- masses of < 1,500 g, so it may not be valid to imum at 0700 (mean = 30.4 C). At this time extrapolate to a lizard as large as C. nubila. Also, the average air temperature was 26.4 C. The while the equation is based on species that gen- fact that the iguanas remained 4-5 C warmer erally have daytime Tb's similar to C. nubila (that than air temperature at night illustrates the ef- is, 35-38 C; Nagy, 1982), many of the temper- fect of sleeping in the burrow, which is the ate species probably had nighttime Tb's lower warmest microhabitat available (Christian et al., than C. nubila (mean minimum = 30.4 C). In 1984). any event, the estimate of energetic expendi- The estimated energetic expenditure of the ture by either method for the population of iguana population on Magueyes is greater than iguanas on Magueyes is higher than any of the that estimated for Conolophus pallidus on Isla other lizards or mammals mentioned above. Santa Fe, Galapagos (432-616 kJ/[ha x d]) The population of iguanas on Magueyes was (Christian and Tracy, 1985b), for Conolophus introduced and we know nothing of the popu- subcristatus on Plaza Sur, Galapagos (Snell and lation densities of the iguanas on Cuba. Visitors Christian, in press), for extremely dense pop- to Magueyes occassionally feed the individuals ulations of small lizards on Bonaire (3,580 kJ/ close to the dock, so the population may be [ha x d]) (Bennett and Gorman, 1979) and much artificially dense. However, these results show greater than the estimates for small mammals that a combination of large size in a lizard and (2,050 kJ/[ha x d]) listed in Table 6 of Bennett high population density can result in a very large and Gorman (1979). energetic expenditure by a population of rep- Our observation that an average of 14% of tiles. the activity period was spent in movement is intermediate between the sit and wait predator Callisaurus draconoides (2%) and the active for- ACKNOWLEDGMENTS agers Cnemidophorustigris (91%) (Anderson and Karasov, 1981) and C. hyperythrus (56-78%) We wish to thank Manuel Hernandez Avila, (Karasov and Anderson, 1984). Our estimates Director of the Department of Marine Sciences, of energetic expenditure are 1.3 x the estimate University of Puerto Rico, Mayaguez, for his obtained (calculated from the equations of An- permission to do this study on Magueyes. drews and Pough, 1975) for iguanas assumed Assistance in the field was contributed by Pe- to remain at rest with the same Tb's. Studies ter E. Maldonado and Jose Baez. Lucy Diaz Mi- using doubly labeled water have found meta- randa helped with the calibration of the trans- bolic expenditures of lizards active in the field mitters. The Biology Department of the to be greater than resting levels (at field active Univeristy of Puerto Rico, Rio Piedras and Of- CHRISTIAN ET AL.-THERMOREGULATION AND ENERGETICS OF IGUANAS 69 icina de Coordinacion de Estudios e Investiga- KARASOV,W. H., AND R. A. ANDERSON.1984. In- ciones provided funds for telemetry equipment. terhabitat differences in energy acquisition and ex- penditure in a lizard. Ecology 65:235-247. MACKAY,R. S. 1964. Galapagos tortoise and marine LITERATURE CITED iguana deep body temperatures measured by radio telemetry. Nature 204:355-358. ANDERSON,R. A., ANDW. H. KARASOV.1981. Con- MERKER, G. P., AND K. A. NAGY 1984. uti- trasts in intake and in sit-and- Energy energy expenditure lization by free-ranging Sceloporus virgatus lizards. wait and widely foraging lizards.Oecologia 49:67- 65:575-581. 72. Ecology NAGY,K. A. 1982. of free-liv- R. AND F. H. POUGH. 1985. Metabo- Energy requirements ANDREWS, M., lizards. 49-59. In: of the lism of allometricand ing iguanid p. Iguanas squamatereptiles: ecological world: their and conservation. Zool. 58:214-231. behavior, ecology, relationships.Physiol G. M. and A. S. Rand Pub- A. AND W. R. DAWSON. 1976. Metab- Burghardt (eds.). Noyes BENNETT, F., Park New 127-223. In: of the vol. lications, Ridge, Jersey. olism, p. Biology reptilia, R. B. HUEYAND A. F. BENNETT.1984. Field 5. C. Gansand W. R. Dawson Academic , (eds.). Press, and mode of Kalahari lacertid New New York. energetics foraging York, lizards. 65:588-596. ANDG. C. GORMAN.1979. Ecology , Population density ANDV. H. SHOEMAKER.1984. Field and of lizardson a island. Oeco- , energet- energetics tropical ics and food of the marine 42:339-358. consumption Galapagos logia cristatus. Zool. 57:281- , ANDK. A. NAGY. 1977. iguana, Amblyrhynchus Physiol Energy expenditure 290. in lizards. 58:697-700. free-ranging Ecology RIVERO, A. 1978. Los anfibios de Puerto K. AND C. R. TRACY. 1985a. Mea- J. y reptiles CHRISTIAN, A., Rico. Editorial Universidad de Puer- air in field studies. Thermal Universitaria, suring temperature J. to Rio Puerto Rico. Biol. 10:55-56. Rico, Piedras, SCHWARTZ,A., ANDM. CAREY.1977. and AND . 1985b. The and biotic Systematics , physical evolution in the West Indian determinantsof utilization the iguanid genus Cyclura. space by Galapagos Stud. Fauna Curacao Other Carib. Is. 173:23-30. land iguana(Conolophus pallidus). Oecologia 66:132- H. AND K. A. CHRISTIAN.In En- 140. SNELL, L., press. of land A AND W. P. PORTER. 1983. Seasonal ergetics Galapagos iguanas: comparison of two island shifts in and use of microhabitats populations. Herpetologica. body temperature V. V. P. SUKHOVAND Y. M. CHERNY- land SOKOLOV, E., by Galapagos iguanas (Conolophuspallidus). SHOV. 1975. A radio telemetric of diurnal 64:463-468. study Ecology fluctuations of in the desert mon- , AND . 1984. The body temperature physiological itor Zhurnal. 54:1347- and of site selec- (Varanus grieseus). Zoolog. ecological consequences sleeping 1356. tion the Land by Galpagos Iguana Conolophuspal- R. ANDR. E. BARWICK.1968. Radiote- lidus.Ibid. 65:752-758. STEBBINS, C., lemetric of in a lace mon- AND . 1985. Inter- and intra- study thermoregulation itor. 1968:541-547. individual variation in of the Copeia body temperatures F. P. A. AND Land TURNER, B., MEDICA B. W. KOWALEWSKY. Galapagos Iguana (Conolophuspallidus). J. 1976. utilization a desert lizard Thermal Biol. 10:47-50. Energy by (Uta stansburiana).US/IBP Desert Biom. Monogr. 1. CONGDON, J. D., AND D. W. TINKLE. 1982. Energy in lizards expenditure free-ranging sagebrush (Sce- DEPARTMENT OF UNIVERSITY OF loporusgraciosus). Can. J. Zool. 60:1412-1416. BIOLOGY, PUERTO RIO PUERTO RICO ETHERIDGE,R. E. 1982. Checklist of the iguanine RICO, PIEDRAS, and malagasyiguanid lizards. p. 7-37. In: Iguanas 00931 (KAC, NC-L, EE-M, MAF, ML-R, of the world: their behavior, ecology and conser- MM); DEPARTMENTOF MARINE SCIENCES, vation.G. M. Burghardtand A. S. Rand(eds.). Noyes UNIVERSITY OF PUERTO RICO, MAYAGUEZ, Publications,Park Ridge, New Jersey. PUERTORICO 00708 (IEC); PRESENTADDRESS T. T. GLEESON, 1979. Foraging and transport costs (KAC) SCHOOLOF BIOLOGICALSCIENCES, THE in the Galapagosmarine iguana,Amblyrhynchus cris- FLINDERSUNIVERSITY OF SOUTHAUSTRALIA, tatus. Zool. 52:549-557. Physiol. BEDFORDPARK, SOUTH AUSTRALIA5042, GORMAN,G. C., AND R. HARWOOD.1977. Notes on AUSTRALIA;PRESENT ADDRESS (IEC) DIVI- populationdensity, vagilityand activitypatterns of SION OF FISH AND WILDLIFE,101 ESTATE the Puerto Ricangrass lizard, Anolis pulchellus (Rep- ST. US VIRGIN tilia, Lacertiliaand ).J. Herpetol. 1:363- NAZERETH, THOMAS, ISLANDS 368. 00802. Accepted 3 May 1985.