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Home , Bolyeriidae, Candoia, Candoia carinata, Leptotyphlopidae, Tropidophiidae, Tropidophis

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 (: 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 , Vol. 23, No. 4, pp. 450-455, 1989 49-60. Copyright 1989 Society for the Study of Amphibians and INGER,R. F. 1960. A review of the agamid lizards of the PhoxophrysHubrecht. Copeia 1960:221- 225. Physiological Color Change in 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 , 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 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): 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 (), 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 Leptotyphlopsdulcis An adult female (508 mm snout-vent length [SVL]) (), 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 (1 the dorsal ground color was light tan with dark tan species) and (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(; McAlpine, 1983), Tropidophisfeicki to brown with dark brown to black, irregularly-shaped (; 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

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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, 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, . 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 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. 2). When matophore unit is composed of iridophores layered the lights were off, the snakes usually were active and between a xanthophore above and a melanophore in the light phase. When the lights were on, the snakes below. Finger-like projections (processes) of the me- generally were inactive and dark. Complete color lanophore extend up around the iridophores and lie change took between 90 min (dark to light phase) and external to the xanthophore. The actual color change 120 min (light to dark phase) after the lights went off (darkening) occurs when the melanosomes migrate 454 NOTES

TABLE1. Species of snakes showing physiological matophore unit. In the dark phase (Fig. 3A), color change. melanosomes (pigment granules) are concentrated in the melanophore processes which line the base of the 24-hr Distri- Refer- epidermis, and relatively few are seen in the body of cycle Habits' bution2 ence3 the melanophore. In the light phase (Fig. 3B), mela- nosomes concentrated in the of the me- Boidae appear body lanophore and not in the processes. Sections taken Candoia from different portions of each scale were consistent carinata YES T I 1 in these features. color has been recorded in Bolyeriidae Physiological change nine of snakes in four families In Casarea species (Table 1). addition to those it has been ob- dussumieri YES T I 2 published records, served in Boa constrictor(B. Bechtel, pers. comm.; J. Tropidophiidae Murphy, pers. comm.), Candoiabibroni (J. Murphy, pers. Tropidophis comm.), and several species of colubrids (S. Sweet, canus YES T? I 3 pers. comm.). Although it probably will be recorded T. feicki YES A I 3 in additional species, several patterns are now evi- T. greenwayi YES T I 3 dent. In at least seven of those species, color change T. haetianus YES T I 1, 3 followed a 24-hr cycle with the light phase occurring T. melanurus YES T I 1, 3, 4 during the night and associated with activity. In the three species studied in detail (Casareadussumieri, Tro- Viperidae pidophisfeicki, and T. melanurus),snakes were inactive Crotalus and remained in the dark phase for several days prior cerastes ? T M 5 to shedding, and in at least one species (T. melanurus), C. viridis ? T M 5, 6, ,7 color change was associated with feeding. These ob- servations a direct correlation between color T = terrestrial,A = arboreal;data from Lynn and Grant suggest and in Crotalus rest- (1940),Klauber (1956), Pope (1961), Minton and Minton(1973), change activity. However, viridis, Schwartz(1975), McCoy (1980), McAlpine (1983), Rehak (1987), ing snakes lightened rapidly (2-4 min) with increased and personalobservations. temperature or activity, regardless of time of day 2 M = mainland, I = insular. (Sweet, 1985; pers. comm.). 3(1) this study; (2) McAlpine, 1983;(3) Rehak, 1987; (4) Seven of the species showing physiological color Lando and Williams, 1969; Klauber,1930; Klauber, (5) (6) change are restricted to islands: the (Tro- 1956;and (7) Sweet, 1985. pidophisspp.); Round Island, Indian Ocean (Casarea); and the islands of the southwest Pacific (Candoia). up these melanophore processes and are brought clos- Also, most are relatively small in body size (30-80 cm er to the epidermis while partially blocking the xan- SVL) and terrestrial in habits. Thus physiological col- thophore and iridophores (Bagnara and Hadley, 1973, or change in snakes appears to be associated with figs. 2-23). This can be under hormonal control (An- small, terrestrial, island "boas," and cyclic (24 hr) col- olis) or both hormonal and neural regulation (Cha- or change is known only in those species. However, maeleoand Phrynosoma).Hormonal control of melano- the presence of physiological color change in four some dispersion in dermal melanophores has been diverse snake families suggests that it is a widespread suggested for snakes (Rahn, 1941). phenomenon that will require further documentation In order to determine whether color change in and experimentation before it is completely under- snakes followed the dermal chromatophore unit mod- stood. scales of melanurus.Two el, we sectioned Tropidophis thank Patrick Fairbairn and removed from the dorsolateral of Acknowledgments.-We scales were region Ann Resource Conservation De- 2: one scale the and the Haynes (Natural snake No. during light phase for to collect snakes in other the dark hr After partment) permission Jamaica; during phase (12 later). Minocal and Zustak for field as- the scales were transferred to Stephenson George removal, quickly light- sistance; Herndon for us to make retardant vials 2% Dowling allowing specimen containing glutaralde- observations on the Candoiacarinata; Bernard Bechtel, in 0.1 M cacodylate buffer, pH 7.4, at room tem- hyde Ronald Crombie, James Murphy, and Samuel Sweet Subsequent steps followed standard electron perature. for providing unpublished observations on snake col- and included a postfix with 1% microscopy protocol or change; and William Saidel for assistance with the osmium tetroxide in 0.1 M cacodylate buffer, dehy- Herndon Robert Gat- dration a series of ethanol solutions, histological analysis. Dowling, through graded ten, Richard Samuel Sweet, Richard Thom- and in 812. sections, 0.75 Highton, embedding Epon Multiple as, and Addison offered ultramicro- Wynn helpful suggestions /im thick, were cut on a Reichert Ultracut on the This research was in tome with knives, and on manuscript. part sup- glass placed microscope a National Science Foundation Grant (BSR- slides. The sections were then either viewed ported by directly 83-07115, to Richard and is contribution 48 with contrast or were stained with a Highton), phase optics of the Laboratory for Biological Ultrastructure (Uni- stain and observed with brightfield op- polychrome versity of Maryland). tics on a Zeiss Photomicroscope I. Examination of multiple sections from the two scales LITERATURECITED of Tropidophismelanurus (snake No. 2) revealed dif- ferences in dermal melanophore structure corre- BAGNARA,J. T., AND M. E. HADLEY.1973. Chromato- sponding to predictions based on the dermal chro- phores and color change: the comparative physi- NOTES 455

ology of pigmentation. Prentice-Hall, Inc., Journalof Herpetology,Vol. 23, No. 4, pp. 455-458, 1989 1989 for the Study of and Englewood Cliffs, New Jersey. 202 pp. Copyright Society Amphibians Reptiles BANKS,C. 1981. Notes on seasonal colour change in a western brown snake. Herpetofauna 13:29-30. GEHLBACH,F. R., J. F. WATKINSII, AND H. W. RENO. Should Hindgut Contents Be Included 1968. Blind snake defensive behavior elicited by in Lizard Dietary Compilations? ant attacks. BioScience 18:784-785. THOMAS W. Univer- KLAUBER,L. M. 1930. New and renamed subspecies SCHOENER,Department of Zoology, Davis, 95616, USA. of Crotalusconfluentus Say, with remarks on related sity of California, California species. Trans. San Diego Soc. Nat. Hist. 6:95-144. .1956. Rattlesnakes; their habits, life histo- Several studies of prey consumption in lizards have ries, and influences on mankind. Univ. Calif. Press, used hindgut contents in addition to stomach con- Berkeley. 2 vols., 1476 pp. tents to estimate diet (e.g., Schoener, 1967, 1968; LANDO,R. V., AND E. E. WILLIAMS.1969. Notes on Schoener and Gorman, 1968). This procedure can the herpetology of the U.S. Naval Base at Guan- greatly increase sample size. Additionally, this pro- tanamo Bay, Cuba. Studies Fauna Curacao and Ca- cedure may reduce bias in estimating prey-size dis- ribbean Islands 31:159-201. tributions in the following way. Individual large prey LYNN,W. C., AND C. GRANT. 1940. The herpetology may pass through the stomach at a rate less than that of Jamaica. Bull. Inst. Jamaica 1:1-148. of individual small prey, so that at any moment pieces MCALPINE,D. F. 1983. Correlated physiological col- of an individual large prey item are more likely to or change and activity patterns in an Indian Ocean be found in both the stomach and hindgut. Hence, Boa. J. Herpetol. 17:198-210. counting only prey in the stomach may bias the prey- McCo, M. 1980. Reptiles of the . size distribution towards large prey (Schoener, 1967; Wau Ecology Inst. Handbook No. 7, Wau, Papua a bias may exist for the entire tract as well, but it will . 80 pp. be smaller). The procedure of including hindgut con- MINTON,S. A., JR., AND M. R. MINTON. 1973. Giant tents in lizard dietary compilations has been criticized reptiles. Charles Scribner's Sons, New York. 345 by Floyd and Jenssen (1984) as having its own bias, PP. specifically that soft-bodied prey are more likely to MIRTSCHIN,P., ANDR. DAVIS. 1982. Dangerous snakes have disintegrated beyond detection by the time they of Australia. Rigby Publ., Adelaide, Australia. reach the hindgut than are hard-bodied prey. Using MOLL,E. O., K. E. MATTSON,AND E. B. KREHBIEL.1981. their own study of Anolis opalinus (Floyd and Jenssen, Sexual and seasonal dichromatism in the Asian 1983), they argued that this bias has three effects: 1) river turtle Callagur borneoensis.Herpetologica 37: the taxonomic diversity of prey (measured as H = 181-194. -pilog[pi], where pi is the decimal frequency of the PARKER,G. H. 1948. Animal color changes and their ith prey category) is substantially less in the hindgut neurohumours. Cambridge Univ. Press, Cam- than in the stomach; 2) the size diversity of prey is bridge. 377 pp. likewise; and 3) hindgut contents are biased toward POPE,C. H. 1961. The giant snakes. Alfred A. Knopf, smaller prey, because soft-bodied prey tend to be large, New York. 290 pp. not because of the argument given in Schoener (1967). PORTER,K. R. 1972. Herpetology. W. B. Saunders Because the criticisms of Floyd and Jenssen are spe- Co., Philadelphia. 524 pp. cifically directed toward my studies, and because bias- RAHN, J. 1941. The pituitary regulation of melano- es of the order they found for their study are serious, phores in the rattlesnake. Biol. Bull. 80:228-237. I re-analyzed some of my data (whose summary char- REHAK,I. 1987. Color change in the snake Tropidophis acteristics have already been published) to determine feicki (Reptilia: : Tropidophidae). Vestnik the magnitude, if any, of their three effects. Because Ceskoslovenske Spolecnosti Zoolgicke 51:300-303. it is important to have some statistical assessment of SCHWARTZ,A. 1975. Variation in the Antillean boid differences between stomach and hindgut contents, snake Tropidophishaetianus Cope. J. Herpetol. 9: data were analyzed separately for each of a number 303-311. of lizard groups. The largest study meeting this re- SWEET,S. S. 1985. Geographic variation, convergent quirement was for two Grenadan species, Anolis rich- crypsis, and mimicry in gopher snakes (Pituophis ardi and Anolis aeneus (Schoener and Gorman, 1968). melanoleucus) and western rattlesnakes (Crotalus It seemed most appropriate to distinguish here those viridis). J. Herpetol. 19:55-67. lizard groups distinguished in the previous paper VISSER, J. 1966. Colour change in Leptotyphlopsscu- (Schoener and Gorman, 1968), as they were the en- tifrons (Peters) and notes on its defensive behav- tities about which conclusions were drawn. Three iour. Zoologica Africana 2:123-125. groups-adult males, adult females and subadult males WARING,H. 1963. Color change mechanisms of cold- (males spanning roughly the same size as adult fe- blooded vertebrates. Academic Press, New York. males)-were so distinguished for each species. These 266 pp. six groups have large sample sizes, from 287 to 4592 WOOLLEY,P. 1957. Colour change in a chelonian. items each; they have the additional advantage that Nature 179:1255-1256. they span a large range of lizard sizes, larger than the single comparison made by Floyd and Jenssen (which lumped all classes of A. opalinus). In my original prey records, stomach contents were distinguished from hindgut contents, so that the two Accepted: 27 July 1988. can be separated here for an analysis mimicking that