JOURNAL f IF THE EAST AFRICA NATURAL HISTORY ?ilx SOCIETY AND NATIONAL MUSEUM 3rd SEPTEMBER 1982 No. 176 THERMAL ECOLOGY OF CHAMAELEO HOHNELII AND MABUYA VARIA IN THE ABERDARE MOUNTAINS: CONSTRAINTS OF HETEROTHERMY IN AN ALPINE HABITAT J. J. Hebrard Dept, of Zoology, University of Nairobi P.O. Box 30197, Nairobi S.M. Reilly P.O. Box 30261, Nairobi M. Guppy Dept, of Biochemistry, University of Nairobi, P.O. Box 30197, Nairobi THERMAL ECOLOGY OF CHAMAELEO HOHNELII AND MABUYA VARIA IN THE ABERDARE MOUNTAINS: CONSTRAINTS OF HETEROTHERMY IN AN ALPINE HABITAT 3rd SEPTEMBER 1982 No. 176 J. J. Hebrard Dept, of Zoology, University of Nairobi P.O. Box 30197, Nairobi S.M. Reilly P.O. Box 30261, Nairobi M. Guppy Dept, of Biochemistry, University of Nairobi, P.O. Box 30197, Nairobi INTRODUCTION Lizards are termed heterothermic because their body temperatures vary by up to 30° C during a diel cycle, reaching a minimum at night and a maximum during the daylight hours. Body enzymes that must function over a wide range of temperatures are less efficient than those that operate at a set temperature (Low and Somero 1976, Fersht 1977, Holbrook et al. 1975), and most lizards that have been studied are able to maintain their body temperatures within a 3-5° C range when they are fully active during the day. This is accomplished by the animals’ shuttling between sun and shade as ambient temperatures vary (see Cloudsley-Thompson 1971, Heatwole 1970). Reptiles that make no attempt to thermoregulate during the day are apparently exceptional, but this may be because most studies of lizard thermoregulation have been done in desert en- vironments where there is no lack of intense solar radiation. Thermal passivity has been reported in three species of the New World genus Anolis (Fitch 1972, Huey 1974, Hertz 1974); two from lowland tropical forest and one from high elevation cloud forest. In all three cases, the criterion for thermal passivity was high variability in cloacal temperatures, but in only one case were com- parative data used convincingly. Chamaeleo hohnelii Steindachner and Mabuya varia (Peters) are found in the moorlands of the Aberdare range above 3000 m. Skinks of the genus Mabuya are surface-active lizards whose thermoregulatory behaviour generally conforms with that noted in other such lizards (e.g. Withers 1981). Chameleons, as -arboreal forms, may be expected to exhibit different thermal pat- terns from terrestrial forms. In what follows we will examine daily temperature cycles in relation to how each species is thermally adapted to life in their particular microenvironments within the moorlands. STUDY AREA AND METHODS The study was conducted in the course of two visits to the Fishing Camp in Aberdare National Park, from 31 January-2 February and 20-22 February 1981. The camp is situated in ericoid bushland where Cliffortia nitidula and Stoebe kilimanjarica are dominant shrubs. Between stands of shrubs are grassy meadows consisting of dense tussocks of Eleusine jaeger i, Agrostris producta, and Festuca abyssinica. Directly in front of the visitors’ cabins is an area of about 2 ha which is about evenly divided between stands of Cliffortia and grassy patches (Plate 1). Chamaeleo hohnelii were found exclusively in the shrubs while Mabuya varia occurred only in the grass tussocks. Air temperatures during the study period varied over a range of 22.6° C, from a low of -2.10C to a high of 20.5'C, both extremes occurring on 22 February (Fig. 1). Weather patterns were similar on all days of the study, with clear, sunny mornings followed by a build up of cumulus clouds in the afternoon. The only rain was a brief shower on the afternoon of 31 January. Page 2 No. 176 Cloacal temperatures of both species of lizards were taken at intervals throughout the 24 hour cycle with a quick-reading thermometer. Chameleons were easily .located on their sleeping perches within the shrubs, and once located, individuals were followed during their limited ar- boreal movements during the day. Skinks spent the night deep within grass tussocks, and could only be caught during the day when they were active on the surface. To facilitate measurement of nocturnal cloacal temperatures, five skinks were placed in a cardboard box containing an isolated grass tussock. The captive animals appeared to show normal sleeping and rousing behaviour which coincided with the behaviours of free-living skinks. Study area at Fishing Camp in Aberdare N.P. Mabuya varia are found exclusively among the grass tussocks in the foreground, while Chamaeleo hohnelii are confined to the shrubs (Cliffortia nitidula) at the rear. RESULTS Chameleons descended into the interiors of Cliffortia shrubs at night where they slept at a mean height of 2.3 m above the ground. This movement apparently gained them little thermal ad- vantage, though they were protected from direct frost. They were observed to supercool when the air temperature dropped below freezing (Figs. 1,2). The skinks burrowed into the cores of grass tussocks where ambient temperatures remained several degrees warmer than outside air tem- perature (Fig. 1). Both animals adopted sleeping postures that reduced their surface area-to- volume ratio, the chameleons with their tails tightly coiled and limbs appressed against the body, and the skinks in a tight coil with the tail wrapped around the body. Though mean body tem- peratures of sleeping chameleons and skinks did not differ significantly in this study (Fig. 3), the latter might gain an advantage in more severe freezes. Moderate supercooling is widespread among cold blooded vertebrates, however, and complete recovery has been reported in reptiles cooled to as low as -8°C (Lowe et al. 1976). AMBIENT TEMPERATURE No. 176 Page 3 25-| AIR r 1 — r 1 — r TIME (EAST) Fig. 1 Air temperatures (solid line) and core temperatures of grass tussocks (dashed line) for the period 20- 22 February 1981. Tussock temperatures are expressed as means (horizontal line) + critical distance (c.d. = s.d J 2/N). SKINK SURFACE ACTIVITY 35n 15- 0- -5 TIME (EAST) Chamaeleo Mabuya Fig. 2. Cloacal temperatures of Chamaeleo hohnelii (solid line) and Mabuya varia (dashed line) over the period 20-22 February 1981. Temperatures are expressed as means (horizontal bar) + critical distance. When critical distances do not overlap, means are significantly different at P .05. Horizontal dashed lines indicate the interval between the first sighting of wild skinks in the mor- ning and the last in the afternoon. 12:00 Page 4 No. 176 o- 5 Fig. 3 Mean cloacaf temperatures (vertical bar) + critical distance (horizontal bar) for sleeping, rousing, and actjve Mabuya varia and Chamaeleo hohnelii. Sample sizes are as follows: Sleeping, Chamaeleo (73). Mabuya (9); First Movement, Chamaeleo (4), Mabuya (5); Active, Chamaeleo (34) Mabuya (20). No. 176 Page 5 Morning arousal in chameleons, as indicated by the first limb movement, occurred at body temperatures not significantly higher than their sleeping temperatures (Fig. 3). Animals were com- pletely immobilized when their body temperatures dropped below freezing, and they appeared dead; some even dropped from their perches. The first sign of life was when the eyes opened and visible breathing began. In some individuals the first movement adjusted the position of the animal on its perch so that one side of the body was perpendicular to the sun’s rays; other in- dividuals made no discernable attempt to bask. In basking animals, the side exposed to the sun was darkened while no colour change occurred on the shaded side. Non-basking individuals began climbing immediately, though very slowly at first. On the morning of 2 February, two animals were each 70 cm above their sleeping perches at 08:50 hrs when the air temperature was 9.3° C, and two others were 1 0 and 1 5 cm above their nocturnal perches. This ascent undoubtedly takes them into more direct sunlight where they quickly reach their active temperature (Figs. 2,3). Because of the lack of a consistent basking period, chameleons were considered active after their first voluntary movement. Thus, body temperatures of active animals were both lower and more variable than those of Mabuya varia. One Chamaeleo hohnelii was observed to capture an insect when its cloacal temperature was only 7°C, suggesting that the tongue muscles are able to func- tion efficiently even when the body musculature is capable of only very slow movement. Even when their body temperatures were at a peak, the chameleons did not move around much, but rather appeared to rely on concealment to ambush prey that approached them. The following arousal sequence for skinks is based on a combination of data from animals kept in a box overnight and from free-living individuals captured when they were active on the surface of the grass tussocks. Skinks within a tussock in early morning exhibited no movements until their cloacal temperatures were above 1 7°C (Fig. 3). Depending on the rate of warming. First movements occurred as early as 07:55 hrs and as late as 09:46 hrs. In each of the five captive animals, the first movements took them from the interior of the grass tussock to a position in full sunlight. In all cases, the first basking site was near the base of the tussock, where the animals were not fully exposed to view. -Initiation of the heating cycle while still under cover has been reported in desert iguanas by McGinnis and Dickson (1967), and is believed to function in shielding the animals from predators before full activity temperature is attained. At a mean cloacal temperature of 26.3° C (s.d. = 0.8), skinks left the grass tussock at a time coinciding with the first appearance of free-living skinks on the surface. Temperatures of active skinks during the warm part of the day averaged just over 28° C, significantly higher than those of chameleons (Fig. 3). In addition, the variation about the mean was significantly smaller than that for active chameleons (F = 3.74, P < .01), suggesting more efficient thermoregulation. The interiors of grass tussocks, which may have provided thermal refuges for skinks at night, became thermal traps during the day, as their temperatures never reached the levels required for full skink activity (Fig. 1). DISCUSSION Because of the lack of clearly defined basking, the greater variability in body temperatures of active animals, and the lower maximum body temperatures, Chamaeleo hohnelii can be said to be thermally passive relative to Mabuya varia on the moorlands of the Aberdares. Their respective microhabitats offer different thermal environments which are exploited by the two species in ac- cordance with their behavioural and physiological limitations. The open grassland inhabited by the skinks receives maximum solar radiation, allowing the animals to rapidly attain a high, and, more importantly, a relatively constant body temperature. Skinks of the genus Mabuya pursue prey actively, and are capable of very rapid movement over short distances. Thus, it is to their ad- vantage to maintain their body temperatures within a narrow range to maximize biochemical ef- ficiency. The dense, shady shrubs inhabited by C. hohnelii afford fewer suitable basking perches (see Huey 1974), with the result that body temperatures of active animals fluctuate over a wide range. According to our initial hypothesis, this should result in lowered biochemical efficiency, and this is borne out by the animals' lethargic behaviour and their ambush method of prey cap- ture. The chameleon’s tongue-shooting ability at 7°C (see Results) may seem contrary to ex- pectation, but the muscular involvement in this mechanism is akin to a slow pumping up, and does not necessitate a high rate of metabolism (Bellairs 1969) Page 6 No. 176 The retreat of skinks to the interiors of grass tussocks and of chameleons into the interiors of shrubs may serve the dual function of protecting the animals from formation of frost on the body surface, and protection from predators while they are immobilized by low body temperatures. Unfortunately, no long term records of temperature are kept above inhabited levels on the Aber- dares, so we cannot discuss extreme minimum temperatures experienced by the lizards. The study was conducted during the southern hemisphere summer, thus it is unlikely that the low tem- peratures recorded were annual minima. Depending on the extremes in the area, the chameleons might have to seek greater protection during colder periods or perhaps suffer local extinction. ACKNOWLEDGEMENTS This study was supported by a grant from the National Geographic Society (U.S.). A number of people helped with the work as follows: Sarah Guppy, Thomas Madsen, and Monika Osterkamp provided expert assistance in the field, Alex Duff-Mackay and Gary Ferguson criticised the manuscript, and George Kinoti gave advice and encouragement. REFERENCES Bellairs. A. 1969. The life of reptiles. Vol. 1. Weidenfeld and Nicholson. London. CloudSley-Thompson. J. L. 1971. The temperature and water relations of reptiles. Merrow. Watford Herts. Fersht. A. 1977. Enzyme structure and function. W. H. Freeman. San Francisco. Fitch. H. S. 1972. Ecology of Anolis tropidolepis in Costa Rican cloud forest. Herpetologica 28:10-21. Heatwole. H. 1970. Thermal ecology of the desert dragon Amphibolurus inermis. Ecological Monographs 40:425-457. Hertz. P. E. 1974. Thermal passivity of a tropical forest lizard, Anolis polylepis. Journal of Herpetology 8:323-327. Holbrook. J., Liuas. A., Steindel. S., and Rossman. M. 1975. Lactate, dehydrogenase. In The enzymes, (ed. P. D. Boyer). Huey. R. B. 1974. Behavioral thermoregulation in lizards: importance of associated costs. Science 184:1001- 1003. Low. P. S. & Somero. G. N. 1976. Adaptations of muscle pyruvate kinase to environmental temperatures and pressures. Journal of Experimental Zoology 198:1-11. Lowe. C. H., Lardner. P. J., & Halpern. E. A. 1971. Supercooling in reptiles and other vertebrates. Com- parative Biochemistry and Physiology 3 9 A : 125-135. McGinnis. S. M. & Dickson. L. L. 1967. Thermoregulation in the desert iguana Dipsosaurus dorsalis. Science 156:1757-1759. Withers. P. C. 1981. Physiological correlates of limblessness and fossoriality in Scincid lizards. Copeia 1981:197-204. Revision received 25 November 1981 Joint Editors M.E.J. Gore Shereen Karmali No. 176 Page 7 NOTICE TO CONTRIBUTORS Papers on natural history subjects will be considered on the understanding that these are being offered exclusively to the Society and have not been submitted, at the same time, to any other journal. They should be addressed to the Editors, Journal of the East Africa Natural History Society and National Museum, P.O. Box 44486, Nairobi, and be accompanied by a covering letter from the author responsible for correspondence and decisions regarding the typescript. Two copies of the contribution should be forwarded to the Society; a further copy should be kept by the author for reference. The typescript should be on A4 size paper. Use one side only, double-spaced with margins of at least 5 cm at the top and left-hand side of the pages to allow for editorial instruction to printers. The pages must be numbered and all measurements are to be in metric units. The title page should contain the title of the article followed by the name of the author(s) and institution(s) where the research was carried out. A present address, if applicable, should be included as a footnote. Abstract to be on the second page and contain not more than 150 words. State the purpose of the study, procedures, main findings and conclusions. This should be intelligible in itself without reference to the paper. Nomenclature In cases where there are well known and accepted English names, e.g. for birds and larger mammals, these should be used throughout the text, accompanied by the scientific name on first mention. Authorities should be given beside the generic and specific names, when quoted for the first time, forall groups, with the exception of ornithological papers not dealing with taxonomic discussion. Text This is usually, but not necessarily, divided into parts with the headings Introduction, Methods, Results and Discussion, these being broken up with sub-headings where necessary. Main heads should be centred on the page and typed in capital letters. Subheads should be ranged to the left margin and typed in capitals. Any further headings should start with a capital letter followed by small letters on the left margin. No headings should be underlined. Underlining is an instruction to the printer to use italic type and should be reserved for all generic and species names, foreign words not adopted into English and for descriptions of bird or animal vocalisation. Acknowledgements As acknowledgements may imply endorsement of the data and conclusions contained in the authors work, it is advisable to obtain permission before quoting persons who have made contributions to the study. References Care should be taken to see that all references quoted in the text are given in full, in this section. To avoid confusion, references to books and periodicals should not be abbreviated and neither should they be underlined. For example: (in text) Cave & Macdonald (1955) or (Cave & Macdonald 1955) (in reference list) CAVE, F.O. & MACDONALD, J.D. 1955. Birds of the Sudan, Oliver & Boyd, London. Tables Each table must be typed, double-spaced on a separate sheet and numbered. Leave good spaces between columns and omit internal vertical and horizontal rules. Cite tables in the text in consecutive order. Illustrations Submit two sets of figures which should be well drawn on bristol board or heavy tracing paper with a photographed or xeroxed copy. Lettering must be of first quality (e.g. lettraset) and consideration must be given to size when reduced. Typewritten or freehand lettering will not be accepted unless put onto an overlay which can be followed by the printers for typesetting. Each figure should have a label pasted on its back giving the number of the figure, caption details and accreditation. Cite each figure in the text in consecutive order. A separate caption sheet should be added to the typescript. Photographs are acceptable if they have good definition and contrast and should be produced on glossy paper. Proofs The author will be sent one set of galley proofs for correction of typographical errors. Authors may be charged for any changes from the original typescript made by him at this stage, and which result in additional printing expense. Plates or page proofs will not be sent. Published material The author is entitled to 25 copies free of charge. Further copies can be supplied at cost price, provided the order is placed when the typescript is submitted. If there is more than one author, 30 copies will be sent to the corresponding author for distribution. The society is supported entirely by membership subscriptions and may not, for financial reasons, be able to accept all submissions of value. Wherever possible an author should seek a grant, from his institution or other source, to help with costs of publication. Page 8 No. 176 Published by The East African Natural History Society, Box 44486, Nairobi, Kenya. Phototypesetting by Kul Graphics Ltd., P.O. Box 18095 and printed by Manhattan Displays, P.O. Box 30434, Nairobi. 3 9088 01313 7468