Biodiversity Science ›› 2016, Vol. 24 ›› Issue (9): 1039-1044.doi: 10.17520/biods.2016116

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Effects of substrate color on the body color variation of two agamid lizards, Phrynocephalus versicolor and P. frontalis

Haojie Tong1, Kailong Zhang1, Yuhang Liu1, Lixun Zhang2, Wei Zhao2, Yuanting Jin1, *()   

  1. 1 College of Life Sciences, China Jiliang University, Hangzhou 310018
    2 College of Life Sciences, Lanzhou University, Lanzhou 730000
  • Online:2016-10-09
  • Jin Yuanting E-mail:jinyuanting@126.com

Geographical variation of body color is widely present in reptile populations that survive in different substrate habitats, multiple potential mechanisms can account for this color variation. Phrynocephalus versicolor and P. frontalis, close genetic relatives, constitute a phylogenetic species group together with P. przewalskii. In this study, a fiber spectrophotometer (AvaSpec-2048) was used to record the skin luminous reflectivity of 12 sites across the lizard’s body, and we quantitatively compared the natural color variation of dark P. versicolor and light P. frontalis that lived in “melanistic” and “non-melanistic” habitats, respectively. We aimed to determine whether the color variations of both populations were time reversible, and further discuss potential mechanisms that substrate color may have on color variation of Phrynocephalus lizards. Our results showed that the body color of P. versicolor in “melanistic” habitat was significantly darker than P. frontalis in the “non-melanistic” withered yellow habitat. We also conducted a reciprocal transplantation experiments (i.e. “non-melanistic” withered yellow P. frontalis individuals were transplanted and fed in “melanistic” substrate environment, while “melanistic” P. versicolor individuals were transplanted and fed in withered yellow substrate environment). For “melanistic” P. versicolor, the skin reflectivity of six sites increased significantly after one week, while no significant changes were detected in other sites. For “non-melanistic” P. frontalis, except the skin reflectivity of two sites (left hind limb and top right on the back) significantly changed, compared to corresponding values one week previously, other sites showed no significant changes. Our results suggest that P. versicolor possesses stronger color variation ability than P. frontalis, and the color phenotypes are likely inherited in both species. Short-term changes of substrate color can cause slightly color variations that are difficult to distinguish by naked eyes, suggesting ontogeny related hereditary factors may also play a controlling role.

Key words: melanistic, body color variation, Phrynocephalus, skin reflectivity

Fig. 1

Body color of lizards and the selected sites for color measurement. (A) “Melanistic” P. versicolor were collected from black substrate habitat (above), “non-melanistic” P. frontalis were sampled from withered yellow substrate habitat (below); (B) M1-12 represent twelve color measuring sites for each lizard, including cranial center (M1), top left on the back (M2), top right on the back (M3), left side on the central back (M4), right side on the central back (M5), bottom left on the back (M6), bottom right on the back (M7), left forelimb (M8), right forelimb (M9), left hind limb (M10), right hind limb (M11), and tail root (M12)."

Table 1

Mean values of reflectivity of each site for both “melanistic” P. versicolor and “non-melanistic” P. frontalis"

检测部位
Sites
非黑化草原沙蜥 “Non-melanistic” P. frontalis 黑化变色沙蜥 “Melanistic” P. versicolor
第1天
1st day
第8天
8th day
第9天
9th day
第10天
10th day
第1天
1st day
第8天
8th day
第9天
9th day
第10天
10th day
M1 1.89±0.18 2.10±0.19 2.18±0.22 2.31±0.20 0.27±0.05 0.45±0.08 0.29±0.06 0.38±0.07
M2 2.23±0.18 2.57±0.16 2.87±0.22 2.72±0.20 0.40±0.05 0.75±0.09 0.82±0.09 0.75±0.09
M3 2.52±0.19 3.24±0.23 3.20±0.18 3.12±0.23 0.48±0.05 0.95±0.11 0.83±0.11 0.83±0.11
M4 2.20±0.18 2.42±0.18 2.42±0.24 2.40±0.17 0.29±0.03 0.55±0.06 0.64±0.08 0.60±0.08
M5 2.48±0.16 2.27±0.18 2.25±0.16 2.27±0.15 0.44±0.07 0.72±0.09 0.65±0.07 0.58±0.06
M6 2.37±0.15 2.30±0.15 2.51±0.16 2.96±0.26 0.39±0.05 0.68±0.09 0.73±0.10 0.61±0.08
M7 2.60±0.18 2.37±0.17 2.60±0.19 2.52±0.17 0.41±0.05 0.74±0.13 0.66±0.07 0.66±0.08
M8 2.83±0.37 2.83±0.27 2.81±0.34 1.99±0.17 0.58±0.15 0.53±0.09 0.59±0.18 0.62±0.17
M9 2.83±0.29 2.57±0.33 2.78±0.41 2.61±0.47 0.47±0.16 0.59±0.14 0.54±0.07 0.48±0.07
M10 2.21±0.29 1.67±0.25 0.99±0.13 0.93±0.13 0.18±0.03 0.22±0.06 0.19±0.02 0.21±0.06
M11 2.23±0.26 2.72±0.42 1.87±0.24 1.96±0.27 0.24±0.05 0.28±0.04 0.22±0.03 0.45±0.16
M12 3.82±0.40 3.56±0.38 3.38±0.45 3.09±0.31 0.64±0.11 0.72±0.08 0.96±0.20 1.16±0.25

Table 2

Paired t test analyses on reflectivity for each site in lizards before and after transplantation"

检测部位Sites 非黑化的草原沙蜥 “Non-melanistic” P. frontalis 黑化的变色沙蜥 “Melanistic” P. versicolor
第1天vs.第8天
1st day vs. 8th day
第1天vs.第9天
1st day vs. 9th day
第1天vs.第10天
1st day vs. 10th day
第1天vs.第8天
1st day vs. 8th day
第1天vs.第9天
1st day vs. 9th day
第1天vs.第10天
1st day vs. 10th day
M1 t28 = 1.085, P = 0.287 t27 = 1.346, P = 0.189 t27 = 1.742, P = 0.093 t28 = 1.660, P = 0.108 t28 = 1.659, P = 0.109 t27 = 1.646, P = 0.112
M2 t28 = 1.382, P = 0.178 t27 = 1.724, P = 0.096 t27 = 1.990, P = 0.057 t28 = 3.598, P = 0.001* t27 = 4.297, P < 0.001* t27 = 3.099, P = 0.005*
M3 t28 = 2.376, P = 0.025* t27 = 3.773, P = 0.001* t27 = 1.828, P = 0.079 t27 = 4.385, P < 0.001* t27 = 3.051, P = 0.005* t27 = 2.995, P = 0.006*
M4 t28 = 0.741, P = 0.465 t27 = 0.530, P = 0.600 t27 = 0.515, P = 0.611 t28 = 3.669, P = 0.001* t27 = 3.749, P = 0.001* t27 = 3.438, P = 0.002*
M5 t28 = -0.644, P = 0.525 t28 = -0.909, P = 0.372 t27 = -1.476, P = 0.152 t28 = 2.473, P = 0.020* t28 = 2.205, P = 0.036* t27 = 1.611, P = 0.119
M6 t27 = -0.348, P = 0.731 t26 = 0.467, P = 0.644 t23 = 1.593, P = 0.126 t27 = -2.686, P = 0.012* t26 = -3.366, P = 0.002* t23 = 2.248, P = 0.035*
M7 t28 = -1.010, P = 0.321 t28 = -0.383, P = 0.705 t27 = -0.759, P = 0.455 t28 = -2.472, P = 0.020* t28 = -2.891, P = 0.007* t27 = 2.686, P = 0.012*
M8 t16 = -0.068, P = 0.947 t16 = -0.111, P = 0.913 t16 = -1.789, P = 0.095 t16 = -0.527, P = 0.606 t16 = -0.396, P = 0.698 t16 = -0.100, P = 0.922
M9 t17 = 0.059, P = 0.954 t17 = 0.552, P = 0.589 t17 = 0.126, P = 0.902 t17 = -0.208, P = 0.838 t17 = 0.005, P = 0.996 t17 = -0.229, P = 0.822
M10 t16 = -1.477, P = 0.162 t16 = -4.168, P = 0.001* t16 = -4.049, P = 0.001* t16 = 0.639, P = 0.533 t16 = 0.046, P = 0.663 t16 = 0.564, P = 0.582
M11 t16 = 1.092, P = 0.293 t16 = -0.899, P = 0.384 t16 = -0.259, P = 0.799 t16 = 0.349, P = 0.733 t16 = -0.405, P = 0.691 t16 = -1.018, P = 0.372
M12 t16 = -0.261, P = 0.798 t16 = -0.605, P = 0.555 t16 = -1.630, P = 0.125 t16 = 1.428, P = 0.175 t16 = -1.847, P = 0.086 t16 = 2.235, P = 0.051
[24] Rosenblum EB, Hoekstra HE, Nachman MW (2004) Adaptive reptile color variation and the evolution of the Mc1r gene. Evolution, 58, 1794-1808.
[25] Rosenblum EB, Römpler H, Schöneberg T, Hoekstrac HE (2010) Molecular and functional basis of phenotypic convergence in white lizards at white sands. Proceedings of the National Academy of Sciences, USA, 107, 2113-2117.
[26] Schlichting CD, Pigliucci M (1999) Phenotypic evolution: a reaction norm perspective. American Journal of Physical Anthropology, 109, 144-146.
[27] Stegen JC, Gienger CM, Sun LX (2004) The control of color change in the Pacific tree frog, Hyla regilla. Canadian Journal of Zoology, 82, 889-896.
[28] Stuart-Fox DM, Moussalli A, Marshall NJ, Owens IPF (2003) Conspicuous males suffer higher predation risk: visual modelling and experimental evidence from lizards. Animal Behaviour, 66, 541-550.
[29] Stuart-Fox D, Moussalli A, Whiting MJ (2008) Predator- specific camouflage in chameleons. Biology Letters, 4, 326-329.
[30] Thurman CL (1988) Rhythmic physiological color change in crustacea: a review. Comparative Biochemistry & Phy- siology Part C. Comparative Pharmacology, 91, 171-185.
[31] Vignieri SN, Larson JG, Hoekstra HE (2010) The selective advantage of crypsis in mice. Evolution, 64, 2153-2158.
[32] Vroonen J, Vervust B, Fulgione D, Maselli V, Damme RV (2012) Physiological colour change in the Moorish gecko, Tarentola mauritanica (Squamata: Gekkonidae): effects of background, light, and temperature. Biological Journal of the Linnean Society, 107, 182-191.
[33] Wang YZ, Fu JZ (2004) Cladogenesis and vicariance patterns in the toad-headed lizard Phrynocephalus versicolor species complex. Copeia, 2004, 199-206.
[34] Woolley P (1957) Colour change in a chelonian. Nature, 179, 1255-1256.
[35] Yang CC, Cai Y, Liang W (2011) Analysis of the correlation between plumage color and male quality in yellow- throated buntings. Sichuan Journal of Zoology, 30(1), 1-5. (in Chinese with English abstract)
[杨灿朝, 蔡燕, 梁伟 (2011) 黄喉鹀的羽色与雄鸟质量相关性分析. 四川动物, 30(1), 1-5.]
[36] Yang CC, Liang W (2013) Using spectra and visual modeling to study animal coloration. Zoological Research, 34, 564-573. (in Chinese with English abstract)
[杨灿朝, 梁伟 (2013) 通过光谱与视觉模型研究动物体色. 动物学研究, 34, 564-573.]
[37] Zhao EM, Jiang YM, Huang QY, Hu SQ, Fei L, Ye CY (1998) Latin-Chinese-English Names of Amphibians and Reptiles. Science Press, Beijing. (in Chinese)
[赵尔宓, 江跃明, 黄庆云, 胡淑琴, 费梁, 叶昌媛 (1998) 拉汉英两栖爬行动物名称. 科学出版社, 北京.]
[38] Zhao EM, Zhao KT, Zhou KY (1999) Fauna Sinica, Reptilia Vol. 2, Squamata, Lacertilia. Science Press, Beijing. (in Chinese)
[赵尔宓, 赵肯堂, 周开亚 (1999) 中国动物志, 爬行纲第二卷, 有鳞目, 蜥蜴亚目. 科学出版社, 北京.]
[39] Zhao X, Bi JH, Liu R, He ZC, Chen SY (2013) The feeding habits of toad-headed lizard (Phrynocephalus frontalis) in autumn. Chinese Journal of Zoology, 48, 321-330. (in Chinese with English abstract)
[赵雪, 毕俊怀, 刘睿, 何志超, 陈绍勇 (2013) 草原沙蜥秋季食性分析. 动物学杂志, 48, 321-330.]
[1] Alibardi L (2013) Observations on the ultrastructure and distribution of chromatophores in the skin of chelonians. Acta Zoologica, 94, 222-232.
[2] Barlett PN, Gates DM (1966) The energy budget of a lizard on a tree trunk. Ecology, 48, 315-322.
[3] Bennett ATD, Cuthill IC (1994) Ultraviolet vision in birds: what is its function? Vision Research, 34, 1471-1478.
[4] Boback SM, Siefferman LM (2010) Variation in color and color change in island and mainland boas (Boa constrictor). Journal of Herpetology, 44, 506-515.
[5] Cai B (2014) Rapid color variation in reptile animals. Bull- etin of Biology, 49(12), 4-6. (in Chinese)
[蔡波 (2014) 爬行动物体色的快速变化. 生物学通报, 49(12), 4-6.]
[6] Chen Q, Han ZX, Song ZM (1993) A study on the reproduction of lizard Phrynocephalus versicolor. Journal of Lanzhou University, 29, 199-203. (in Chinese with English abstract)
[陈强, 韩昭雪, 宋志明 (1993) 变色沙蜥繁殖的研究. 兰州大学学报, 29, 199-203.]
[7] Choi N, Jang Y (2014) Background matching by means of dorsal color change in treefrog populations (Hyla japonica). Journal of Experimental Zoology Part A Ecological Genetics & Physiology, 321, 108-118.
[8] Cooper WE, Greenberg N (1992) Reptilian coloration and behavior. In: Biology of the Reptilia, Vol. 18. Physiology E: Hormones, Brain and Behavior (eds Gans C, Crews D), pp. 298-422. University of Chicago Press, Chicago.
[9] Cott HB (1940) Adaptive Coloration in Animals. Methuen and Co. Ltd., London.
[10] Devi SF, Adnan M (2009) Camouflage, communication and thermoregulation: lessons from colour changing org- anisms. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 463-470.
[11] Geen MRS, Johnston GR (2014) Coloration affects heating and cooling in three color morphs of the Australian bluetongue lizard, Tiliqua scincoides. Journal of Thermal Biology, 43, 54-60.
[12] Guo L, Zhao CG (2001) Study on the reproductive strategy of lizard Phrynocephalus frontalis. Acta Scientiarum Naturalium Universitatis Neimongol (Natural Science Edition), 32, 214-275. (in Chinese with English abstract)
[郭砺, 赵辰光 (2001) 草原沙蜥(Phrynocephalus frontalis)生殖策略的研究. 内蒙古大学学报(自然科学版), 32, 214-275.]
[13] Hanlon R (2007) Cephalopod dynamic camouflage. Current Biology, 17, 400-404.
[14] Hemmi JM, Marshall J, Pix W, Vorobyev M, Zeil J (2006) The variable colours of the fiddler crab Uca vomeris and their relation to background and predation. Journal of Experimental Biology, 209, 4140-4153.
[15] Jin YT, Liao PH (2015) An elevational trend of body size variation in a cold-climate agamid lizard, Phrynocephalus theobaldi. Current Zoology, 61, 444-453.
[16] Mäthger LM, Land MF, Siebeck UE, Marshall NJ (2003) Rapid colour changes in multilayer reflecting stripes in the paradise whiptail, Pentapodus paradiseus. Journal of Experimental Biology, 206, 3607-3613.
[17] Merilaita S, Lyytinen A, Mappes J (2001) Selection for cryptic coloration in a visually heterogeneous habitat. Proceedings of the Royal Society of London B: Biological Sciences, 268, 1925-1929.
[18] Moretz JA, Morris MR (2003) Evolutionarily labile responses to a signal of aggressive intent. Proceedings of the Royal Society B: Biological Sciences, 270, 2271-2277.
[19] Nery LEM, Castrucci AMDL (1997) Pigment cell signalling for physiological color change. Comparative Biochemistry & Physiology Part A Physiology, 118, 1135-1144.
[20] Norris KS (1965) Color adaptation in desert reptiles and its thermal relationships. In: Lizard Ecology: A Symposium (ed. Milstead WW), pp. 162-226. University of Missouri Press, Columbia, Missouri.
[21] Porter WP, Gates DM (1969) Thermodynamic equilibria of animals with environment. Ecological Monographs, 39, 227-244.
[22] Qu YF, Gao JF, Mao LX, Ji X (2011) Sexual dimorphism and female reproduction in two sympatric toad-headed lizards, Phrynocephalus frontalis and P. versicolor (Agamidae). Animal Biology, 61, 139-151.
[23] Quan RZ, Chen DF, Zhang JF (2006) Studies on the hunger-resistance and the feeding habit of Phrynocephalus versicolor. Journal of Shihezi University (Natural Science), 24, 436-438. (in Chinese with English abstract)
[全仁哲, 陈道富, 张继锋 (2006) 变色沙蜥(Phryno- cephalus versicolor)的耐饥能力与食性研究. 石河子大学学报(自然科学版), 24, 436-438.]
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