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Physiological Color Change in Snakes Physiological Color Change in Snakes 450 NOTES FIG. 3. Dorsal views of heads of Japalura chapaensis (holotype; A), and J. swinhonis (KUZ R2933; B). The scale indicates 10 mm. by a Grant-in-Aid from the Japan Ministry of Edu- 1989b. Re-evaluation of the status of Japalura cation, Science and Culture, No. A-6379027. mitsukurii Stejneger 1898 (Agamidae: Reptilia). Amphibia-Reptilia. In press. H. 1967. Liste der rezenten LITERATURECITED WERMUT, Amphibien und Reptilien. In R. Mertens, W. Hennig, and H. Wermuth (eds.), Das Tierreich, Vol. 86. Walter de BOURRET,R. 1937a. Notes Herpetologiques sur l'In- Gruyter & Co., Berlin. dochine Francaise. XII. Bull. Gen. Instr. Publ. 1937: 3-22. Accepted: 13 July 1988. 1937b. Notes Herpetologiques sur l'Indo- chine Francaise. XV. Bull. Gen. Instr. Publ. 1937: 57-82. 1939. Notes Herpetologiques sur l'Indo- chine Francaise. XX. Bull. Gen. Instr. Publ. 1939: Journal of Herpetology, Vol. 23, No. 4, pp. 450-455, 1989 49-60. Copyright 1989 Society for the Study of Amphibians and Reptiles INGER,R. F. 1960. A review of the agamid lizards of the genus PhoxophrysHubrecht. Copeia 1960:221- 225. Physiological Color Change in Snakes LEVITON,A. E., R. H. GIBBS,JR., E. HEAL,AND C. E. S. BLAIR CARLA ANN AND TIMOTHY DAWSON. 1985. Standards in herpetology and HEDGES,' HASS,', K. MAUGEL, ichthyology: Part I. Standard symbolic codes for Department of Zoology, University of Mary- institutional resource collections in land, College Park, Maryland 20742, USA. '(Present Ad- herpetology dress: 208 Mueller The and ichthyology. Copeia 1985(3):802-832. Departmentof Biology, Laboratory, LIANG,Y.-S., AND C.-S. WANG. 1976. Review of the Pennsylvania State University, University Park, Pennsyl- vania genus Japalura(Lacertilia: Agamidae) found from 16802, USA.) Taiwan. Q. J. Taiwan Mus. 29:153-189. Lou, S.-K., ANDJ.-Y. LIN. 1983. Biochemical system- Among reptiles, physiological color change is well atics of the genus Japalura(Sauria: Agamidae) in known in lizards (Parker, 1948; Porter, 1972; Bagnara Taiwan. Bull. Inst. Zool., Academia Sinica 22:91- and Hadley, 1973), and has been reported in turtles 104. (Woolley, 1957) and snakes. It usually involves the OTA, H. 1988. Karyotypic differentiation in an aga- rapid (minutes to hours) movement of melanosomes mid lizard, Japaluraswinhonis swinhonis. Experientia into (darkening) or out of (lightening) dermal me- 44:66-68. lanophore processes. Morphological color change is 1989a. Japalurabrevipes Gressitt (Agamidae: a longer process (days to weeks) and involves an ab- Reptilia), a valid species from a high altitude area solute increase in melanosomes and melanophores of Taiwan. Herpetologica. In press. (Bagnara and Hadley, 1973; Moll et al., 1981). NOTES 451 A B C E F FIG. 1. Three individual snakes photographed in light phase (A, C, E) and dark phase (B, D, F): Candoia carinata (A, B), Tropidophishaetianus (C, D), and T. melanurus (E, F). Color change in snakes appears to be very uncom- describe the phenomenon in three additional species: mon. Seasonal change has been observed in three Candoia carinata (Boidae), Tropidophishaetianus, and T. Australian elapids (Banks, 1981; Mirtschin and Davis, melanurus. Common aspects of these six species, and 1982) and in the viperid Vipera berus (Rehak, 1987), three other species for which physiological color and apparently involves morphological color change change has been mentioned, are reviewed. (Waring, 1963). In the thread snake Leptotyphlopsdulcis An adult female (508 mm snout-vent length [SVL]) (Leptotyphlopidae), rapid color change is a defensive Candoia carinata (locality unknown) was obtained in behavior achieved by elevating the scales (Gehlbach April 1986. After color change was noted, the snake et al., 1968). A similar type of color change in L. scu- was maintained under fluorescent light for approxi- tifrons (Visser, 1966) probably involves the same mately 11-13 hr per day and spot checks for coloration mechanism. were made at about 1-hr intervals over a one week Rahn (1941) was able to induce physiological color period (1-8 May 1986). In the light phase (Fig. 1A), change in snakes from the families Viperidae (1 the dorsal ground color was light tan with dark tan species) and Colubridae (4 species). However, natu- to grayish-brown middorsal blotches. Dorsolateral rally-occurring physiological color change has been blotches or mottling were barely evident. In the dark described in only three species of snakes: Casareadus- phase (Fig. 1B), the dorsal ground color was dark tan sumieri(Bolyeriidae; McAlpine, 1983), Tropidophisfeicki to brown with dark brown to black, irregularly-shaped (Tropidophiidae; Rehak, 1987), and Crotalusviridis (Vi- blotches forming a relatively continuous middorsal peridae; Klauber, 1930, 1956; Sweet, 1985). Here, we band. A majority of observations (13/17) made during 452 NOTES Off On Off Light - 100- Snake 1 0 '-''~~ 100 1111ll1 11II a)0 a 50- 0 o c 0 o I I II I I I 1I i I 2I I I 12 18 24 . - 0 100 50ix - -Snake 2 0 50 - I~~~~~~- as n 50 0 0 C. I I i I l I I 12 18 24 Time FIG.2. Color change and activity patterns in two Tropidophismelanurus under a controlled light cycle (13L: 11D). Bar at top indicates light cycle. Values are averages of observations (N = 330, total) during 5 wk experiment. For color phase: white = light phase; black = dark phase; and vertical lines = transitional. lighted hours revealed the snake in its dark phase, the snake was again examined and found to be almost whereas a majority of the observations (5/7) made completely black. After return to the laboratory, it during dark hours revealed the snake in its light phase. was maintained alive for 19 days during which only The shortest period recorded for a complete transition occasional observations were made. In the light phase from one phase to the other (in this case, dark to light) (Fig. 1C), the dorsal ground color was yellow and was 140 min. heavily patterned with dark green, reddish-brown, We obtained an adult female (486 mm SVL) Tropi- brown, and black markings. In the dark phase (Fig. dophis haetianus from a resident of Quick Step, Tre- 1D), the dorsal surface was entirely black with vir- lawny Parish, Jamaica on 9 October 1984. The snake tually no trace of a pattern. was collected during the day and the collector be- Two adult Tropidophismelanurus (snake 1 = 395 mm lieved it to be a young black snake (Alsophis ater). SVL; snake 2 = 420 mm SVL) were collected in March However, when we arrived at 2130 hr (after dark) and 1987 on Guantanamo Bay Naval Station, Cuba. Color examined the snake, it had a yellow ground color change was noticed soon after capture. In the light with two rows of dark dorsal markings and we were phase (Fig. 1E), the dorsal ground color was a grayish suprised that it had been confused with Alsophis, a pink, and the dorsal markings were a greenish brown. much darker snake. The following morning, the rea- The dorsal pattern was composed of a series of blotch- son for the apparent confusion became obvious when es along a middorsal stripe. In the dark phase (Fig. NOTES 453 A _,,---~~~~~~-- I ! aI1e~ I I IM" l 11..11A,!t!!l ",No - -.- -- ""--w0lL ?- rC' :~; J~(~~ ;,.r -. - ,.. .? . I ' .l FIG.3. Cross sections of two scales (removed 12 hr apart) from the dorsolateral region of a living Tropidophis melanurus (dark bars = 10 ,m). A) Dark phase: melanosomes fill the melanophore processes (arrowheads) just below the epidermis, leaving fewer in the melanophore body (m). B) Light phase: melanosomes are concen- trated in the melanophore body, with relatively few in the processes. Portions of other melanophores also are visible in both sections. 1F), the pattern was barely discernible as the ground (or on). The level of activity changed much more color darkened to a light brown. quickly, often within minutes after a change in the A light cycle experiment was performed with the lights. The only times that the snakes were observed two specimens of Tropidophismelanurus. They were moving were during the first three hours in darkness. placed on a 13L:11D light cycle within a week after They usually rested during the dark hours with their capture, and housed in wide-mouth gallon jars with head held up at an angle, probably typical of "sit- paper toweling. Observations (N = 330) on coloration and-wait" predators. When the lights went on, the and activity were made as often as possible during snakes would respond relatively quickly, withdraw- the course of the study (10 April-16 May 1987) and ing their heads into the paper toweling within a few were taken on the hr (+10 min). A flashlight was minutes. The strongest evidence that color change used for observations made during the dark hours. was directly correlated with activity was obtained Snake color was assigned to one of three categories: when the snakes were fed, or prior to shedding. Ac- light, transition, and dark. Snakes were considered tivity usually ceased after feeding and the snakes "active" when prowling, or (more commonly) resting would remain dark and inactive for 24-48 hr. Color with the head oriented above the body (ca. 45? angle) change data obtained after feeding and before shed- and protruding from the paper toweling. Snakes were ding were not included in Fig. 2. scored as "inactive" if they were completely con- The primary mechanism for rapid color change in cealed in the paper toweling, or if exposed, they were lizards involves the movement of melanosomes (pig- motionless and their head was flat on the substrate. ment-containing organelles) within dermal melano- Color change in Tropidophismelanurus closely fol- phores (Bagnara and Hadley, 1973). A dermal chro- lowed a 24-hr light and activity cycle (Fig.
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