Abstract
The behavior of sea turtle species can be influenced by the lunar cycle, possibly due to moonlight variability. We analyzed the relationship between nesting behavior and moon phase using nesting hawksbill turtle records for beaches in Northeast Brazil for the 2006–2007 to 2015–2016 seasons. The total number of records was 4807, while the total number with time point registration was 1031. The Eretmochelys imbricata inter-nesting period was approximately half the lunar cycle; we therefore expected nesting phase synchronization with lunar phases within each season. We computed the lunar angle for the hawksbill records, and the Kuiper test for uniformity indicated that the species shows some lunar phase preferences. We observed that oviposition at the first and last quarters of the moon is more frequent than at full moon or new moon phases. We also computed the lunar angle throughout several seasons for remigrant turtles and found an absence of preferential lunar phase across different seasons. This indicates that the hawksbill does not choose a lunar phase previously chosen in other nesting seasons. We analyzed the relationship between the presence of the moon in the sky and nesting turtles, and, in sequence, compared the records of false crawls and nest crawls; no relation was found between these variables.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alligood KT, Sauer TD, Yorke JA, Crawford JD (1997) Chaos: an introduction to dynamical systems. Springer-Verlag, New York
Baldwin WP, Lofton JP (1959) The loggerhead turtles of Cape Romain, South Carolina (abridged and annotated by DK Caldwell). Bull Fla State Mus 4:309–348
Bjorndal KA, Carr A, Meylan AB, Mortimer JA (1985) Reproductive biology of the Hawksbill Eretmochelys imbricata at Tortuguero, Costa Rica, with notes on the ecology of the species in the caribbean. Biol Conserv 34:353–368. https://doi.org/10.1016/0006-3207(85)90040-0
Clayson CA, Weitlich D (2007) Variability of tropical diurnal sea surface temperature. J Clim 20:334–352. https://doi.org/10.1175/JCLI3999.1
Davis GE, Whiting MC (1977) Loggerhead sea turtle nesting in Everglades National Park, Florida, USA. Herpetologica. https://doi.org/10.2307/3891625
Dobbs KA, Miller JD, Limpus CJ, Landry AM Jr (1999) Hawksbill turtle, Eretmochelys imbricata, nesting at Milman Island, northern Great Barrier Reef, Australia. Chelonian Conserv Biol 3:344–361
Dowding CV, Harris S, Poulton S, Baker PJ (2010) Nocturnal ranging behaviour of urban hedgehogs, Erinaceus europaeus, in relation to risk and reward. Anim Behav 80:13–21. https://doi.org/10.1016/j.anbehav.2010.04.007
Ekanayake EL, Ranawana KB, Kapurusinghe T, Premakumara MGC, Saman MM (2002) Impact of lunar cycle on nesting behaviour of marine turtles. Ceylon J Sci (Biol Sci) 30:99–104
Evans JA, Leise TL, Castanon-Cervantes O, Davidson AJ (2011) Intrinsic regulation of spatiotemporal organization within the suprachiasmatic nucleus. PLOS ONE. https://doi.org/10.1371/journal.pone.0015869
Firth BT, Thompson MB, Kennaway DJ, Belan I (1989) Thermal sensitivity of reptilian melatonin rhythms: “cold” tuatara vs. “warm” skink. Am J Physiol 256:R1160–R1163
Girondot M, Fretey J (1996) Leatherback turtles, Dermochelys coriacea, nesting in French Guiana, 1978–1995. Chelonian Conserv Biol 2:204–208
Gomes MGT, Santos MRDD, Henry M (2007) Tartarugas marinhas de ocorrência no Brasil: hábitos e aspectos da biologia da reprodução. Rev Bras Reprod Anim 30:19–27
Haus E, Smolensky MH (1999) Biologic rhythms in the immune system. Chronobiol Int 16:581–622. https://doi.org/10.3109/07420529908998730
Hayes MO (1979) Barrier island morphology as a function of tidal and wave regime. In: Leatherman SP (ed). Academic Press, New York
Hays GC, Broderick AC, Glen F et al (2002) Water temperature and internesting intervals for loggerhead (Caretta caretta) and green (Chelonia mydas) sea turtles. J Therm Biol 27:429–432. https://doi.org/10.1016/S0306-4565(02)00012-8
Hirth HF (1980) Some aspects of the nesting behavior and reproductive biology of sea turtles. Am Zool 523:507–523. https://doi.org/10.1017/CBO9781107415324.004
Horning M, Trillmich F (1999) Lunar cycles in diel prey migrations exert a stronger effect on the diving of juveniles than adult Galápagos fur seals. Proc Biol Sci 266:1127–1132. https://doi.org/10.1098/rspb.1999.0753
Hughes DA, Richard JD (1974) The nesting of the Pacific Ridley turtle Lepidochelys olivacea on Playa Nancite, Costa Rica. Mar Biol 24:97–107. https://doi.org/10.1007/BF00389343
Jacobs GH, Deegan JF, Crognale MA, Fenwick JA (1993) Photopigments of dogs and foxes and their implications for canid vision. Vis Neurosci. https://doi.org/10.1017/s0952523800003291
Kamel SJ, Mrosovsky N (2005) Repeatability of nesting preferences in the hawksbill sea turtle, Eretmochelys imbricata, and their fitness consequences. Anim Behav 70:819–828. https://doi.org/10.1016/j.anbehav.2005.01.006
Law A, Clovis T, Lalsingh GR, Downie JR (2010) The influence of lunar, tidal and nocturnal phases on the nesting activity of leatherbacks (Dermochelys coriacea) in Tobago, West Indies. Mar Turt Newsl 127:12–17
López JC, Vargas JP, Gómez Y, Salas C (2003) Spatial and non-spatial learning in turtles: the role of medial cortex. Behav Brain Res 143:109–120. https://doi.org/10.1016/S0166-4328(03)00030-5
Marcovaldi MÂ, Dei Marcovaldi GG (1999) Marine turtles of Brazil: the history and structure of Projeto TAMAR-IBAMA. Biol Conserv 91:35–41. https://doi.org/10.1016/S0006-3207(99)00043-9
Marcovaldi MÂ, Lopez GG, Soares L, Belini C, dos Santos AS, Lopez M (2011) Avaliação do estado de conservação da tartaruga marinha Eretmochelys imbricata (Linnaeus, 1766) no Brasil. Biodiversidade Brasileira (1)
Meylan AB, Donnelly M (1999) Status justification for listing the hawksbill turtle (Eretmochelys imbricata) as critically endangered on the 1996 IUCN red list of threatened animals. Chelonian Conserv Biol 3:200–224
Mikulecky M, Bounias M (1997) Worker honeybee hemolymph lipid composition and synodic lunar cycle periodicities. Braz J Med Biol Res 30:275–279. https://doi.org/10.1590/S0100-879X1997000200018
Minutini L, Innocenti A, Bertolucci C, Foà A (1995) Circadian organization in the ruin lizard Podarcis sicula: the role of the suprachiasmatic nuclei of the hypothalamus. J Comp Physiol A 176:281–288. https://doi.org/10.1007/BF00239930
Miranda-Anaya M, Bartell PA, Yamazaki S, Menaker M (2000) Circadian rhythm of ERG in Iguana iguana: role of the pineal. J Biol Rhythms 15:163–171. https://doi.org/10.1177/074873040001500210
Moncada FG, Nodarse G, Medina Y, Escobar E (2010) Twelve years of monitoring hawksbill turtle (Eretmochelys imbricata) nesting at Doce Leguas Keys and Labyrinth, Jardines de la Reina Archipelago. Marine Turtle Newsletter 127(6)
Nelson RJ, Demas GE (1996) Seasonal changes in immune function. Q Rev Biol 71:511–548. https://doi.org/10.1086/419555
Österholm H (1964) The significance of distance receptors in the feeding behaviour of the fox, Vulpes vulpes L. Acta Zoologica Fenica 106
Pendoley KL, Schofield G, Whittock PA et al (2014) Protected species use of a coastal marine migratory corridor connecting marine protected areas. Mar Biol 161:1455–1466. https://doi.org/10.1007/s00227-014-2433-7
Pike DA (2008) Environmental correlates of nesting in loggerhead turtles, Caretta caretta. Anim Behav 76:603–610. https://doi.org/10.1016/j.anbehav.2008.04.010
Plytycz B, Seljelid R (1997) Rhythms of immunity. Arch Immunol Ther Exp (Warsz) 45:157–162
R Development Core Team R (2011) R: a language and environment for statistical computing. R Found Stat Comput 1:409
Rahman MS, Morita M, Takemura A, Takano K (2003) Hormonal changes in relation to lunar periodicity in the testis of the forktail rabbitfish, Siganus argenteus. Gen Comp Endocrinol 131:302–309. https://doi.org/10.1016/S0016-6480(03)00025-X
Rahman MS, Kim BH, Takemura A et al (2004) Effects of moonlight exposure on plasma melatonin rhythms in the seagrass rabbitfish, Siganus canaliculatus. J Biol Rhythms 19:325–334. https://doi.org/10.1177/0748730404266712
Santos A, Bellini C, Vieira D et al (2013) Northeast Brazil shows highest hawksbill turtle nesting density in the South Atlantic. Endanger Species Res 21:25–32. https://doi.org/10.3354/esr00505
Santos AJB, Neto JXL, Vieira DHG et al (2016) Individual nest site selection in hawksbill turtles within and between nesting seasons. Chelonian Conserv Biol 15:109–114. https://doi.org/10.2744/CCB-1136.1
Sato K, Matsuzawa Y, Tanaka H et al (1998) Internesting intervals for loggerhead turtles, Caretta caretta, and green turtles, Chelonia mydas, are affected by temperature. Can J Zool 76:1651–1662. https://doi.org/10.1139/cjz-76-9-1651
Takemura A, Susilo ES, Rahman MDS, Morita M (2004) Perception and possible utilization of moonlight intensity for reproductive activities in a lunar-synchronized spawner, the golden rabbitfish. J Exp Zool Part A Comp Exp Biol 301:844–851. https://doi.org/10.1002/jez.a.105
Talbert OR Jr, Stancyk SE, Dean JM, Will JM (1980) Nesting activity of the loggerhead turtle (Caretta caretta) in South Carolina. I. A rookery in transition. Copeia 1980:709–719
Tilden AR, Hutchison VH (1993) Influence of photoperiod and temperature on serum melatonin in the diamondback water snake, Nerodia rhombifera. Gen Comp Endocrinol 92:347–354. https://doi.org/10.1006/gcen.1993.1172
Tosini G, Bertolucci C, Foà A (2001) The circadian system of reptiles: a multioscillatory and multiphotoreceptive system. Physiol Behav 72:461–471. https://doi.org/10.1016/S0031-9384(00)00423-6
Underwood H (1985) Pineal melatonin rhythms in the lizard Anolis carolinensis: effects of light and temperature cycles. J Comp Physiol A 157:57–65
Vivien-Roels B, Arendt J, Bradtke J (1979) Circadian and circannual fluctuations of pineal indoleamines (serotonin and melatonin) in Testudo hermanni gmelin (reptilia, chelonia). I. Under natural conditions of photoperiod and temperature. Gen Comp Endocrinol 37:197–210
Walcott J, Eckert S, Horrocks JA (2012) Tracking hawksbill sea turtles (Eretmochelys imbricata) during inter-nesting intervals around Barbados. Mar Biol 159:927–938. https://doi.org/10.1007/s00227-011-1870-9
Wells MC, Lehner PN (1978) The relative importance of the distance senses in coyote predatory behaviour. Anim Behav. https://doi.org/10.1016/0003-3472(78)90025-8
Acknowledgments
This study was conducted with support provided by Pro-TAMAR Foundation, which is among the institutions responsible for implementing conservation actions under the National Action Plan For The Conservation Of Sea Turtles - NAP ICMBio/MMA. Projeto TAMAR is officially sponsored by Petrobras. Biodiversity authorization and information system (SISBio) issued data collection license 42760. We would also like to thank the Pipa Ecological Sanctuary and all the field volunteers for their help. The authors also gratefully acknowledge the financial support of the Conselho Nacional de Desenvolvimento Científico e Tecnologico, Brazil.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Nakamura, M.F., Santos, A.J.B., Lobão-Soares, B. et al. Lunar phases and hawksbill sea turtle nesting. J Ethol 37, 307–316 (2019). https://doi.org/10.1007/s10164-019-00604-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10164-019-00604-7