Amphibians' response to the lunar synodic cycle-a review of current knowledge, recommendations, and implications for conservation

Behavioral Ecology

Volumn 24, Issue 1, 2013, Pages 53-62

  Grant, Rachel ^a   Halliday, Tim ^a   Chadwick, Elizabeth ^b  

^a ANGLIA RUSKIN UNIVERSITY   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

amphibians; circular statistics; light; lunar cycle; moon phase; predator avoidance; reproductive synchronization

Indexed keywords

AMPHIBIAN; AVOIDANCE REACTION; HOMING BEHAVIOR; LITERATURE REVIEW; LUNAR PHASE; REPRODUCTIVE BEHAVIOR; SIGNALING; SPECIES CONSERVATION; SYNCHRONY; TAXONOMY;

AMPHIBIA; ANIMALIA;

EID: 84871244738     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/ars135     Document Type: Review

References (116)

1. Abrunhosa PA, Wogel H, Pombal JP Jr. 2006. Anuran temporal occupancy in a temporary pond from the Atlantic rain forest south-eastern Brazil. Herp J. 16:115-122.
2. Akre KL, Ryan MJ. 2011. Female túngara frogs elicit more complex mating signals from males. Behav Ecol. 22(4):846-853.
3. Alldredge AL, King JM. 1980. Effects of moonlight on the vertical migration patterns of demersal zooplankton. J Exp Mar Biol Ecol. 44:133-157.
4. Anders TF. 1982. Biological rhythms in development. Psychosom Med. 44(1):61-72.
5. Amézquita, A, Hödl, W. 2004. How, when, and where to perform visual displays: the case of the Amazonian frog, Hyla parviceps. Herpetologica. 60:420-429.
6. Amiet JL. 1974. Voix d'amphibiens camerounais IV-Raninae: genres Ptychadena Hildebrandtia et Dicroglossus. Ann Fac Sci Cameroun. 18:109-128.
7. Backwell PRY, Passmore NI. 1990. Suitable approach perches affect female phonotaxis in an arboreal frog. Herpetologica. 46:11-14.
8. Baker BJ, Richardson JML. 2006. The effect of artificial light on male breeding-season behaviour in green frogs Rana clamitans melanota. Can J Zool. 84(1):1528-1532.
9. Batschelet E. 1981. Circular statistics in biology. London: Academic Press Inc.
10. Baugh AT, Ryan MJ. 2010. Ambient light alters temporal updating behaviour during mate choice in a Neotropical frog. Can J. Zool 88: 448-453.
11. Bell B, Defouw RJ. 1966. Dependence of the lunar modulation of geomagnetic activity on the celestial latitude of the moon. J Geophys Res. 71:951-957.
12. Bouskila A. 1995. Interactions between predation risk and competition: a field study of kangaroo rats and snakes. Ecology. 76:165-178.
13. Brooke PN, Alford RA, Schwartzkopf L. 2000. Environmental and social factors influence chorusing behaviour in a tropical frog: examining various temporal and spatial scales. Behav Ecol Sociobiol. 49:79-87.
14. Brown GP, Shine R. 2002. Influence of weather conditions on activity of tropical snakes. Aust Ecol. 27:596-605.
15. Buchanan BW. 1992. Bimodal nocturnal activity pattern of Hyla squirella. J Herpetol. 26(4):521-522.
16. Buchanan BW. 1998. Low-illumination prey detection by squirrel treefrogs. J Herpetol. 32(2):270-274.
17. Buchanan BW. 2006. Observed and potential effects of arti?cial night lighting on anuran amphibians. In: Rich C, Longcore T, editors. Ecological consequences of arti?cial night lighting. p. 190-220. Washington (DC): Island Press.
18. Byrne PG. 2002. Climatic correlates of breeding simultaneous polyandry and potential for sperm competition in the frog Crinia georgiana. J Herpetol. 36:125-129.
19. Byrne PG, Roberts JD. 2004. Intrasexual selection of group spawning in quacking frogs. Behav Ecol. 15(5):872-882.
20. Campbell SR, Mackessy SP, Clarke JA. 2008. Microhabitat use by brown treesnakes Boiga irregularis: effects of moonlight and prey. J Herpetol. 42(2):246-250.
21. Church G. 1960a. Annual and lunar periodicity in the sexual cycle of the Javanese toad Bufo melanostictus Schneider. Zoologica. 45:181-188.
22. Church G. 1960b. The effects of seasonal and lunar changes on the breeding pattern of the edible Javanese frog Rana cancrivora. Gravenhorst. Treubia. 25:214-233.
23. Church G. 1961. Seasonal and lunar variation in the numbers of mating toads in Bandung, Java. Herpetologica. 17:122-126.
24. Clarke JA. 1983. Moonlight's influence on predator/prey interactions between short-eared owls (Asio flammeus) and deermice (Peromyscus maniculatus). Behav Ecol Sociobiol. 13(3):205-209.
25. Daly M, Behrends PR, Wilson MI, Jacobs LI. 1992. Behavioural modulation of predation risk: moonlight avoidance and crepuscular compensation in a nocturnal desert rodent Dipodomys merriami. Anim Behav. 44:1-9.
26. da Silva Nunes V. 1988. Vocalizations of treefrogs Smilisca sila in response to bat predation. Herpetologica. 44:8-10.
27. deBruyn MH, Meuwig JJ. 2001. Detecting lunar cycles in marine ecology: periodic regression versus categorical ANOVA. Mar Ecol Prog Ser. 214:307-310.
28. Deeming DC. 2008. Capture of smooth newts Lissotriton vulgaris and great crested newts Triturus cristatus correlates with the lunar cycle. Herpetol J. 18:171-174.
29. De Luna G, Hödl W, A. 2010. Colour, size, and movement: the role of visual stimuli in species recognition by males of the frog Allobates femoralis. Anim. Behav. 79: 739-745.
30. Deutschlander ME, Phillips JB, Borland SC. 1999a. The case for light dependent magnetic orientation in animals. J Exp Biol. 202:891-908.
31. Deutschlander, ME, Borland SC, Phillips JB. 1999b. Extraocular magnetic compass in newts. Nature. 400:324-325.
32. Diego-Rasilla FJ, Phillips JB. 2007. Magnetic compass orientation in larval Iberian freen Frogs, Pelophylax Perezi. Ethology, 113: 474-479.
33. Diego-Rasilla FJ, Luengo RM, Phillips JB. 2005. Magnetic compass mediates nocturnal homing by the alpine newt. Triturus alpestris. Behav. Ecol. Sociobiol. 58, 361-365.
34. Dill LM. 1987. Animal decision making and its ecological consequences: the future of aquatic ecology and behaviour. Can J Zool. 65(4):803-811.
35. Dole JW. 1972. Evidence of celestial orientation in newly-metamorphosed Rana pipiens. Herpetologica. 28:273-276.
36. Donati G, Lunardini A, Kappelar DM, Borgognini Tarli, SM. 2001. Nocturnal activity in the cathemeral red-fronted lemur Eulemur fulvus rufus with observations during a lunar eclipse. Am J Primatol. 53:69-78.
37. Duellman WE. 1967. Courtship isolating mechanisms in Costa Rican hylid frogs. Herpetologica. 23(3):169-183.
38. Ferguson DE. 1960. Observations on movements and behavior of Bufo fowleri in residential areas. Herpetologica. 16(2):112-114.
39. Ferguson DE, Landreth HF. 1966. Celestial orientation of Fowler's toad Bufo fowleri. Behaviour. 26:105-123.
40. Ferguson DE, Landreth HF, Turnipseed MR. 1965. Astronomical orientation of the southern cricket frog, Acris gryllus. Copeia. 1:58-66.
41. Fernandez-Duque E, Di Fiore A, Carrillo-Bilbao G. 2008. Behavior, Ecology, and Demography of Aotus vociferans in Yasuní National Park, Ecuador Int J of Primatol. 29:421-431.
42. Fischer JH, Freake MJ, Borland SC, Phillips JB. 2001. Evidence for the use of magnetic map information by an amphibian. Anim Behav. 62:1-10.
43. Fitzgerald GJ, Bider Jr. 1974. Influence of moon phase and weather factors in locomotory activity in Bufo americanus. Oikos. 25:338-340.
44. Fleischack PC, Small CP. 1978. The vocalizations and breeding behaviour of Kassina senegalensis (Anura, Rhacophoridae) in summer breeding aggregations. Koedoe. 21:91-99.
45. Forester DC, Lykens DV. 1986. Significance of satellite males in a population of spring peepers Hyla crucifer. Copeia. 3:719-724.
46. Freake MJ, Phillips JB. 2005. Light-dependent shift in bullfrog tadpole magnetic compass orientation: evidence for a common magnetoreception mechanism in anuran and urodele amphibians. Ethology 111: 241-254.
47. Gliwicz ZM. 1986. A lunar cycle in zooplankton. Ecology. 67(44):883-897.
48. Goldberg CS, Schwalbe CR. 2004. Habitat use and spatial structure of the barking frog. J Herpetol. 38(3): 305-312.
49. Gomez D, Richardson C, Lengagne T, Plenet S, Joly P, Lena J, Théry M. 2009 The role of nocturnal vision in mate choice: females prefer conspicuous males in the European tree frog (Hyla arborea). Proc. R. Soc. B 276 1666: 2351-2358.
50. Gorman RR, Ferguson JH. 1970. Sun-compass orientation in the western toad Bufo boreas. Herpetologica. 26:34-45.
51. Grafe DE. 1997. Costs and benefits of mate choice in the lek-breeding reed frog, Hyperolius marmoratus. Anim Behav. 53(5):1103-1117.
52. Granda JR, Pena RM, Pierce BA. 2008. Effects of disturbance position of observer and moonlight on efficiency of anuran call surveys. Appl Herpetol. 5:253-263.
53. Grant RA, Chadwick EA, Halliday T. 2009. The lunar cycle: a cue for amphibian reproductive phenology? Anim Behav. 78(2):49-357.
54. Hailman JP, Jaeger RG. 1976. A model of phototaxis and its evaluation with anuran amphibians. Behaviour 56 (3-4): 215-248.
55. Halliday TR. 1974. Sexual behaviour of the smooth newt Triturus vulgaris (Urodela: Salamadridae). J Herpetol. 8:277-292.
56. Harvey MB, Pemberton AJ, Smith EN. 2002. New and poorly known parachuting frogs (Rhacophoridae: Rhacophorus) from Sumatra and Java. Herpetol Mon. 16:46-92.
57. Hassinger DD, Anderson JD. 1970. The effect of lunar eclipse on nocturnal stratification of larval Ambystoma opacum. Copeia. 1970:178-179.
58. Hauselberger KF, Alford RA. 2005. Effects of season and weather on calling in the Australian microhylid frogs Austrochaperina robusta and Cophixalus ornatus. Herpetologica. 61(4):349-363.
59. Hettyey A, Herczeg G, Laurila A, Crochet P, Merilä J. 2009. Body temperature, size, nuptial colouration and mating success in male moor frogs Rana arvalis. Amph Rept. 30:37-43.
60. Hiert C, Moura MO. 2010. Abiotic correlates of temporal variation of Hypsiboas leptolineatus (Amphibia: hylidae). Zoologia. 27(5):703-708.
61. Hirschmann W, Hödl W. 2006. Visual signaling in Phrynobatrachus krefftii Boulenger, 1909 (Anura: Ranidae). Herpetologica 62:18-27.
62. Hödl W, Amézquita A. 2001. Visual signaling in anuran amphibians. In: Ryan MJ ed. Anuran Communication. Washington, DC: Smithsonian Institution Press, 121-141.
63. Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin, SL. 2000. Quantitative evidence for global amphibian population declines. Nature. 404:752-755.
64. Hussin AG. 2007. Hypothesis testing of parameters for ordinary linear circular regression. J Appl Sci Res. 3(3):185-188.
65. Inger RF. 1969. Organization of communities of frogs along small rain forest streams in Sarawak. J Anim Ecol. 38:123-148.
66. Ims RA. 1990. The ecology and evolution of reproductive synchrony. Trends Ecol Evol. 5(5):135-140.
67. Iskandar DT. 1998. The amphibians of Java and Bali. Bogor (Indonesia): Research and Development Centre for Biology-LIPI.
68. Jaeger RG, Hailman JP. 1976. Phototaxis in anurans: relation between intensity and spectral preferences. Copeia. 1976(1):92-98.
69. Jaeger RG, Hailman JP. 1981. Activity of neotropical frogs in relation to ambient light. Biotropica. 13(1):59-65.
70. Johnson DH, Batie RD. 2001. Surveys of calling amphibians in North Dakota. Prairie Nat. 33:227-247.
71. Kie JG. 1999. Optimal foraging and risk of predation: effects on behavior and social structure of ungulates. J Mammal. 80(4):1114-1129.
72. Kühn ER, Gevaerts H, Jacobs G, Vandorpe G. 1987. Reproductive cycle thyroxine and corticosterone in females of the giant swamp frog Dicroglossus occipitalis at the equator. Gen Comp Endocrinol. 66:137-144.
73. Lang AB, Kalko EKV, Romer H, Bockholdt C, Dechmann DKN. 2006. Activity levels of bats and katydids in relation to the lunar cycle. Oecologia. 146:659-666.
74. Llusia D, Márquez R, Beltrán JF. 2010. Non-selective and time-dependent behavioural responses of common toads Bufo bufo to predator acoustic cues. Ethology. 116:1146-1154.
75. Longcore T, Rich C. 2004. Ecological light pollution. Front Ecol Environ. 2:191-198.
76. Loredo I, VanVuren D, Morrison, ML. 1996. Habitat use and migration behavior of the California tiger salamander. J Herpetol. 30(2):282-285.
77. Magnusson WE, Pimental LA, Hero JM, Carmozina de Araújo M. 1999. The rise and fall of a population of Hyla boans: reproduction in a neotropical gladiator frog. J Herpetol. 33:647-656.
78. Neumann D. 1981. Tidal and lunar rhythms. In: J Aschoff, editor. Handbook of behavioral neurobiology. Biological rhythms. Vol. 4. New York: Plenum Press.
79. Newman DG. 1990. Activity dispersion and population densities of Hamilton's frog Leiopelma hamiltoni on Maud and Stephens Islands, New Zealand. Herpetologica. 46:319-330.
80. Nowinszky L. 2004. Nocturnal illumination and night flying insects. Appl Ecol Environ Res. 2(1):17-52.
81. Omori K. 1995. The adaptive significance of a lunar or semi-lunar reproductive cycle in marine animals. Ecol Model. 82:41-49.
82. Orrock J, Danielson B, Brinkerhoff R. 2004. Rodent foraging is affected by indirect but not by direct cues of predation risk. Behav Ecol. 15:433-437.
83. Phillips JB. 1986a. Two magnetoreception pathways in a migratory salamander. Science. 233(4765):765-767.
84. Phillips JB. 1986b. Magnetic compass orientation in the eastern red-spotted newt Notophthalmus viridescens. J Comp Physiol A. 158(1):103-109.
85. Phillips JB, Adler K, Borland SC. 1995. True navigation by an amphibian. Anim Behav. 50:855-858.
86. Phillips JB, Borland SC. 1992. Wavelength-specific effects of light on magnetic compass orientation of the eastern red-spotted newt Notophthalmus viridescens. Ethology Ecology & Evolution 4(1):33-42.
87. Phillips JB, Borland SC, Freake MJ, Brassart J, Kirschvink JL. 2002. "Fixed-axis" magnetic orientation by an amphibian: non-shoreward-directed compass orientation misdirected homing or positioning a magnetite-based map detector in a consistent alignment relative to the magnetic field? J Exp Biol. 205:3903-3914.
88. Rahman MS, Takemura A, Takano K. 2000. Correlation between plasma steroid hormones and vitellogenin profiles and lunar periodicity in the female golden rabbitfish Siganus guttatus Bloch. Comp Biochem Physiol. B. 127:113-122.
89. Rand AS, Bridarolli ME, Dries L, Ryan MJ. 1997. Light levels influence female choice in túngara frogs: predation risk assessment? Copeia. 1997:447-450.
90. Rosenthal GG, Rand AS, Ryan MJ. 2004. The vocal sac as a visual cue in anuran communication: an experimental analysis using video playback. Anim Behav. 68:55-58.
91. Ryan MJ. 1985. The Túngara frog. Chicago (IL): University of Chicago Press.
92. Seligmann H, Anderson SC, Autumn K, Bouskilad A, Safa R, Tuniyeve BS, Wernera YL. 2007. Analysis of the locomotor activity of a nocturnal desert lizard (Reptilia: Gekkonidae: Teratoscincus scincus) under varying moonlight. Zoology. 110:104-117.
93. Shapiro DY, Sadovy Y, McGehee MA. 1993. Size composition and spatial structure of the annual spawning aggregation of the red hind Epinephelus guttatus Pisces: Serranidae. Copeia. 1993(2):399-406.
94. Smith MJ, Withers PC, Roberts JD. 2003. Reproductive energetics and behavior of an Australian myobatrachid Frog Crinia georgiana. Copeia. 2:248-254.
95. Sih A. 1994. Predation risk and the evolutionary ecology of reproductive behaviour. J Fish Biol. 45:111-130.
96. Sinsch U. 1988. Seasonal changes in the migratory behaviour of the toad Bufo bufo: direction and magnitude of movements. Oecologia. 76:390-398.
97. Stolov HL. 1965. Further investigations of a variation of geomagnetic activity with lunar phase. J Geophys Res. 70:4921-4926.
98. Summers K, Symula R, Clough M, Cronin T. 1999. Visual mate choice in poison frogs. Proc Biol Sci. 266(1434):2141-2145.
99. Surlykke A, Kalko EKV. 2008. Echolocating bats cry out loud to detect their prey. PLoS ONE. 3(4):e2036.
100. Swannack TM, 2007. Modeling aspects of the ecological and evolutionary dynamics of the endangered Houston toad [PhD Dissertation]. College Station (TX): Texas A&M University.
101. Swannack TM, Granta WE, Forstnerb, MRJ. 2009. Projecting population trends of endangered amphibian species in the face of uncertainty: a pattern-oriented approach. Ecol Model. 220(2):148-159.
102. Takemura A, Rahman S, Nakamura S, Park YJ, Takano K. 2004. Lunar cycles and reproductive activity in reef fishes with particular attention to rabbitfishes. Fish Fish. 5:317-328.
103. Takemura A, Ueda S, Hiyakawa N, Nikaido Y. 2006. A direct influence of moonlight intensity on changes in melatonin production by cultured pineal glands of the golden rabbitfish Siganus guttatus. J Pineal Res. 40:236-241.
104. Taylor RC, Buchanan BW, Doherty JL. 2007. Sexual selection in the squirrel treefrog Hyla squirella: the role of multimodal cue assessment in female choice. Anim Behav. 74:1753-1763.
105. Taylor RC, Klein BA, Stein J, Ryan, MJ. 2008. Faux frogs: multimodal signaling and the value of robotics in animal behavior. Anim Behav. 76:1089-1097.
106. Taylor RC, Klein BA, Stein J, Ryan MJ. 2011. Multimodal signal variation in space and time: how important is matching a signal with its signaller? J Exp Biol. 214:815-820.
107. Tracy TR, Dole JW. 1969. Orientation of displaced California toads Bufo boreas to their breeding sites. Copeia. 1969(4):693-700.
108. Tsukamoto K, Otake T, Mochioka N, Lee TW, Fricke H, Inagaki T, Aoyama J, Ishikawa S, Kimura S, Miller MJ. 2003. Seamounts, new moon and eel spawning: the search for the spawning site of the Japanese eel. Environ Biol Fish. 66:3.
109. Tuttle MD, Taft, LK, Ryan MJ. 1982. Evasive behaviour of a frog in response to bat predation. Anim Behav 30(2):393-397.
110. Tuttle MD, Ryan MJ. 1982. The role of synchronized calling ambient light and ambient noise in anti-bat-predator behaviour of a treefrog. Behav Ecol Sociobiol. 11:125-131.
111. Vasquez, T, Pfennig, K. 2007. Looking on the bright side: females prefer coloration indicative of male size and condition in the sexually dichromatic spadefoot toad, Scaphiopus couchii. Behav Ecol Sociobiol. 62:127-135.
112. Vincent SE, Shine R, Brown GP. 2005. Does foraging mode influence sensory modalities for prey detection in male and female filesnakes, Acrochordus arafurae? Anim Behav. 70(3):715-721.
113. Watanuki Y. 1986. Moonlight avoidance behavior in Leach's stormpetrels as a defense against slaty-backed gulls. Auk. 103(1):14-22.
114. Wells KD. 2007. The ecology and behavior of amphibians. Chicago (IL): University of Chicago Press.
115. Wikelski M, Hau M. 1995. Is there an endogenous tidal foraging rhythm in marine iguanas? J Biol Rhythms. 10:335-350.
116. Yetman CA, Willem J, Ferguson H. 2011. Spawning and non-breeding activity of adult giant bullfrogs Pyxicephalus adspersus. Afr J Herpetol. 60(1):13-29.