Emergence Rhythms of Hatchling Marine Turtles: Is a Time Sense Involved?
Author(s): Michael Salmon and Megan Reising
Source: Chelonian Conservation and Biology, 13(2):282-285.
Published By: Chelonian Research Foundation
DOI: http://dx.doi.org/10.2744/CCB-1121.1
URL: http://www.bioone.org/doi/full/10.2744/CCB-1121.1
Source: Chelonian Conservation and Biology, 13(2):282-285.
Published By: Chelonian Research Foundation
DOI: http://dx.doi.org/10.2744/CCB-1121.1
URL: http://www.bioone.org/doi/full/10.2744/CCB-1121.1
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses.
Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne's Terms of Use, available at www.bioone.org/page/terms_of_use.
Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne's Terms of Use, available at www.bioone.org/page/terms_of_use.
Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
COMMENTARIES AND REVIEWS
Editorial Comment. - This section has been established as a forum for the exchange of ideas, opinions, position statements, policy recommendations, and other reviews regarding turtle-related matters. Commentaries and points of view represent the personal opinions of the authors, and are peer-reviewed only to the extent necessary to help authors avoid clear errors or obvious misrepresentations or to improve the clarity of their submissions, while allowing them the freedom to express opinions or conclusions that may be at significant variance with those of other authorities. We hope that controversial opinions expressed in this section will be counterbalanced by responsible replies from other specialists, and we encourage a productive dialogue in print between the interested parties. The editors reserve the right to reject any submissions that do not meet clear standards of scientific professionalism.
Chelonian Conservation and Biology, 2014. 13(2): 282-285
© 2014 Chelonian Research Foundation
© 2014 Chelonian Research Foundation
Emergence Rhythms of Hatchling Marine Turtles: Is a Time Sense Involved?
MICHAEL SALMON* AND MEGAN REISING
Department of Biological Sciences, Florida Atlantic University,
777 Glades Road, Boca Raton, Florida 3343-0991 USA
[salmon@fau.edu; megan.reising17@gmail.com]
*Corresponding author
777 Glades Road, Boca Raton, Florida 3343-0991 USA
[salmon@fau.edu; megan.reising17@gmail.com]
*Corresponding author
ABSTRACT. - Hatchling marine turtles show a nocturnal rhythm of emergence from the nest. Here, we highlight aspects of the rhythm that are incompletely understood, with special reference to differences in the rhythm's expression among populations as well as its cessation at dawn. We postulate that the rhythm ceases because the hatchlings, as they dig toward the surface, acquire a time sense that suppresses activity if they approach the beach surface too late in the day.
Science is-and how else can I say it? -most fun when it plays with interesting ideas, examines their implications, and recognizes that old information might be explained in surprisingly new ways.
-Stephen Jay Gould
The emergence of hatchlings from the nest is the culmination of a process that begins in loggerhead turtles (Caretta caretts), and presumably other species of marine turtles as well, some 4 d prior to the event (Godfrey and Mrosovsky 1997). It starts when the hatchling breaks through the shell and escapes from the confines of its egg, buried some 40-60 cm below the sand surface.
After this escape, the turtles complete their final stages of preemergence preparation. The turtles gradually unfold from the "curled" position assumed inside the egg to a dorsoventrally flattened posotion that expedites more efficient locomotion. At the same time, the yolk sac is pulled inside the body (Miller et al. 2003). A space is created in the nest by compaction of the eggshells below the mass of hatchlings and by fluid drainage from their eggs. The hatchlings dig upward withing that space,
After this escape, the turtles complete their final stages of preemergence preparation. The turtles gradually unfold from the "curled" position assumed inside the egg to a dorsoventrally flattened posotion that expedites more efficient locomotion. At the same time, the yolk sac is pulled inside the body (Miller et al. 2003). A space is created in the nest by compaction of the eggshells below the mass of hatchlings and by fluid drainage from their eggs. The hatchlings dig upward withing that space,
displacing sand from above them to below. About a day or two before they emerge, the hatchlings can often be found resting at the bottom of an air-filled cavity beneath the surface sand. Just before emergence, the final phase of digging activity by the turtles typically causes the surface sand to sag into the cavity, forming a depression at the surface. The depression collapses when hatchlings finally emerge.
In this article, we reexamine the factors that control the temporal pattern (rhythm) of hatchling emergence. Emergence is primarily a nocturnal activity because high surface sand temperatures during the day inhibit hatchling digging activity (Hendrickson 1958: Bustard 1967; Mrosovsky 1968; Moran et al 1999). Thus if the hatchlings digging toward the surface encounter hot sand, they stop. Those temperatures decline rapidly after sunset, release that inhibition, and trigger emergence activity which at any nesting beach is primarily confined to time periods between dusk and dawn (Fig. 1). However, to fully understand the rhythm, it is essential to know not only how it is triggered but also how it is expressed through the dark period and what mechanisms bring the cycle to an end. There have been many studies dealing with correlations between decreasing temperatures and the initiation of the emergence rhythm. Less understood are the reasons why both populations and species differ in how the rhythm is expressed and what causes emergence activity to end at dawn. Here. we summarize the evidence on those points and present a hypothesis that might explain how the rhythm ends each morning.
Emergence rhythms are usually quantified at the population level by recording how often they occur at half- or full-hour intervals throughout the night (With erington el al. 1990; Gyuris 1993). Counts are usually made for many nests over many evenings. Another way of estimating emergences is to count the number of crawling hatchlings that fall into traps each hour, set between the nest and the ocean. The number of nests from which they came can then be estimated by dividing the counts by the proportion of the clutch that on average exits the nest (Glen et al. 2006). The resulting distribution pattern (Fig. 1) varies from one that can show normality (e.g., loggerheads in Melbourne Beach, Florida, USA) to a pattern that is strongly asymmetrical (hawksbills [Eretmochelys imbricata]) at Antigua, West Indies; green turtles
In this article, we reexamine the factors that control the temporal pattern (rhythm) of hatchling emergence. Emergence is primarily a nocturnal activity because high surface sand temperatures during the day inhibit hatchling digging activity (Hendrickson 1958: Bustard 1967; Mrosovsky 1968; Moran et al 1999). Thus if the hatchlings digging toward the surface encounter hot sand, they stop. Those temperatures decline rapidly after sunset, release that inhibition, and trigger emergence activity which at any nesting beach is primarily confined to time periods between dusk and dawn (Fig. 1). However, to fully understand the rhythm, it is essential to know not only how it is triggered but also how it is expressed through the dark period and what mechanisms bring the cycle to an end. There have been many studies dealing with correlations between decreasing temperatures and the initiation of the emergence rhythm. Less understood are the reasons why both populations and species differ in how the rhythm is expressed and what causes emergence activity to end at dawn. Here. we summarize the evidence on those points and present a hypothesis that might explain how the rhythm ends each morning.
Emergence rhythms are usually quantified at the population level by recording how often they occur at half- or full-hour intervals throughout the night (With erington el al. 1990; Gyuris 1993). Counts are usually made for many nests over many evenings. Another way of estimating emergences is to count the number of crawling hatchlings that fall into traps each hour, set between the nest and the ocean. The number of nests from which they came can then be estimated by dividing the counts by the proportion of the clutch that on average exits the nest (Glen et al. 2006). The resulting distribution pattern (Fig. 1) varies from one that can show normality (e.g., loggerheads in Melbourne Beach, Florida, USA) to a pattern that is strongly asymmetrical (hawksbills [Eretmochelys imbricata]) at Antigua, West Indies; green turtles
Figure 1. Emergence patterns shown by loggerhead (C. caretta), hawksbill (C. mydas) turtle hatchlings at their nesting beaches. n = number of nests sampled, except in e and f, where n = the estimated number of nests based upon hatchlings captured in traps. Locations are (a) loggerheads from North Carolina, USA (modified from Neville et al. 1988); (b) loggerheads from Melbourne Beach, Florida, USA (from Witherington et al. 1990); (c) green turtles from Heron Island, Australia (Gyuris 1993); (d) hawksbills from Antigua, West Indies (Reising 2014); (e-f) green turtles from 2 beaches at Ascension Island (modified from Glen et al. 2006). Note that with one exception, emergences end during 0600 hrs or sooner.
[Chelonia mydas] at Heron Island, Australia). A more typical pattern is skewed toward the early evening but shows less asymmetry (e.g., loggerheads in North Carolina, USA; green turtles at Ascension Island). In all of the asymmetrical distributions, however, more hatchlings emerge from nests during the first half than during the second half of the dark period. Why that should be so is a matter of speculation.
A possible explanation for the skewed pattern has been suggested by Glen, Hays, and coworkers (see citations below). Nests in different locations on the same beach can expose eggs and hatchlings to environments that differ in thermal, moisture, and other conditions. When those conditions are relatively uniform within a nest, the hatchlings develop in synchrony and emerge at the same time. Conversely, when conditions vary within a nest the hatchlings will develop at different rates and emerge over several evening ("multiple emergences"), as several workers have documented (Witheringtopn et al. 1990; Hays et al. 1992; Houghton and Hays 2001; Glen et al. 2005). Similarly, variation in conditions between nests results in hatchlings that dig to the surface at different
A possible explanation for the skewed pattern has been suggested by Glen, Hays, and coworkers (see citations below). Nests in different locations on the same beach can expose eggs and hatchlings to environments that differ in thermal, moisture, and other conditions. When those conditions are relatively uniform within a nest, the hatchlings develop in synchrony and emerge at the same time. Conversely, when conditions vary within a nest the hatchlings will develop at different rates and emerge over several evening ("multiple emergences"), as several workers have documented (Witheringtopn et al. 1990; Hays et al. 1992; Houghton and Hays 2001; Glen et al. 2005). Similarly, variation in conditions between nests results in hatchlings that dig to the surface at different
times of the day and night. Those that reach hot sand during the day will stop, wait, and accumulate throughout the day. It is those nests, containing hatchlings that for hours have been competent to emerge, that are responsible for the surge in emergences that occur earlier in the evening (Glen et al. 2006). Additionally, sand temperatures cool most rapidly during the early evening (Fig. 2). Hatchlings emerge sooner when sands at shallow depths (15 cm) below the surface cool rapidly (Hays et al. 1992). The emergences that occur later in the evening (forming the tail of the asymmetrical distribution) are likely from nests where the hatchlings dug to the surface hours later. When sands were cooling more slowly, if at all (Fig. 2). However, this explanation does not account for why distributions vary in degree of asymmetry or (like those of loggerheads in Florida) show normality.
There still remains the problem of what ends the rhythm in the early morning (Fig. 1). This cessation of emergence activity is unlikely to be caused by a temperature-related inhibition, as emergences stop before solar radiation reheats the surface sand (Fig. 2). Put another way, the emergence rhythm is suppressed twice each day: by hot beach sands (up to 50°C; Witheringtion et al. 1990) during the midday and in the early morning by a factor or factors unknown. It is also unlikely that cycle ends because all of the turtles at that beach, competent to leave their nest, have in fact left. Moran et al. (1999) hypothesize that they have; they suggest that the hatchlings begin their ascent in time to arrive at the beach surface at night. We think this is unlikely for the reasons given above; embryos can develop asynchronously, and so hatchlings probably initiate a dig toward the surface (and arrive near there) at any time of the day or night.
But Moran et al. (1999) may be correct when they imply that hatchlings might have a sense of time. Perhaps the turtles that fail to emerge in the morning are those that sense that they have arrived at the surface too late to emerge and so must dig no farther. Those turtles (at least in Florida) rarely break through the surface sand, and so exposure to light is not a likely cue that stops them. What does? We suggest that they might have a "time sense," perhaps triggered by the rapid decline in sand temperatures following sunset, although any part of a diel cycle of temperature variation could provide a cue and start such temporal "countdown." Those changes would be most apparent to hatchlings that have dug their way to < 20 cm below the beach surface (Fig. 2). The timing mechanism they possess could be analogous to an "hourglass" rhythm (first described by Enright and Hamner 1967) that, once triggered, run its temporal course; it must be triggered again to repeat the cycle and influence the behavior of the hatchlings that dig near to the surface the next morning.
In summary, an additional element (a time sense) is required to account for how emergence rhythms are controlled from start to finish each day. Emergence
There still remains the problem of what ends the rhythm in the early morning (Fig. 1). This cessation of emergence activity is unlikely to be caused by a temperature-related inhibition, as emergences stop before solar radiation reheats the surface sand (Fig. 2). Put another way, the emergence rhythm is suppressed twice each day: by hot beach sands (up to 50°C; Witheringtion et al. 1990) during the midday and in the early morning by a factor or factors unknown. It is also unlikely that cycle ends because all of the turtles at that beach, competent to leave their nest, have in fact left. Moran et al. (1999) hypothesize that they have; they suggest that the hatchlings begin their ascent in time to arrive at the beach surface at night. We think this is unlikely for the reasons given above; embryos can develop asynchronously, and so hatchlings probably initiate a dig toward the surface (and arrive near there) at any time of the day or night.
But Moran et al. (1999) may be correct when they imply that hatchlings might have a sense of time. Perhaps the turtles that fail to emerge in the morning are those that sense that they have arrived at the surface too late to emerge and so must dig no farther. Those turtles (at least in Florida) rarely break through the surface sand, and so exposure to light is not a likely cue that stops them. What does? We suggest that they might have a "time sense," perhaps triggered by the rapid decline in sand temperatures following sunset, although any part of a diel cycle of temperature variation could provide a cue and start such temporal "countdown." Those changes would be most apparent to hatchlings that have dug their way to < 20 cm below the beach surface (Fig. 2). The timing mechanism they possess could be analogous to an "hourglass" rhythm (first described by Enright and Hamner 1967) that, once triggered, run its temporal course; it must be triggered again to repeat the cycle and influence the behavior of the hatchlings that dig near to the surface the next morning.
In summary, an additional element (a time sense) is required to account for how emergence rhythms are controlled from start to finish each day. Emergence
Figure 2. Average temperatures at the beach surface and below plotted against time of day at different nesting beaches. Upper left, Heron Island, Australia (modified from Gyuris 1993); lower left, at a leatherback (D. coriacea), olive ridley (L. olivacea), and green turtle (C. mydas) nesting beach in Costa Rica (modified from Drake and Spotila 2002); right, at depths of 10 cm (upper graph) and 20 cm (lower graph) from the darker sands of the warmer North East Bay and the lighter sands of the cooler Long Beach green turtle nesting sites at Ascension Island (from Glen et al. 2006). When these studies were done, the light cycle at all locations varied between 12 and 13 hrs in duration. As temperature measurements are made closer to the beach surface, daily fluctuations in those temperatures become more apparent. Note that at all sites sand temperatures rise in the morning about an hour or two after emergence activity ceases.
rhythms (as documented by others) are 1) suppressed by hot sand temperatures during the day, 2) initiated by the temperature decline after sunset, 3) persist throughout the night while sand temperatures remain low, and (as we propose here) 4) are stopped in the morning by some type of time sense. How long that effect lasts remains to be determined; perhaps it ends once beach temperatures start to rapidly rise once again (Fig. 2).
Field observations consistent with this hypothesis were made some years ago by Gyuris (1993) at Heron Island. During several days of overcast and rain, she reported that "... hatchling emergence was greatly reduced for the first day or so ... then returned to normal numbers although these were spread throughout the 24 hours of the day ..." (italics ours). Thus, hatchlings that reached the surface when sands were cool and which should have emerged at any time-if only sand temperature inhibited their activity-failed to do so for about 24 hrs. Apparently, the turtles waited in the nest only so long before emerging arhythmically (during the day and at night) probably because, in the absence of a signal to emerge, they must eventually do so to begin an offshore migration. Waiting indefinitely sacrifices energy
Field observations consistent with this hypothesis were made some years ago by Gyuris (1993) at Heron Island. During several days of overcast and rain, she reported that "... hatchling emergence was greatly reduced for the first day or so ... then returned to normal numbers although these were spread throughout the 24 hours of the day ..." (italics ours). Thus, hatchlings that reached the surface when sands were cool and which should have emerged at any time-if only sand temperature inhibited their activity-failed to do so for about 24 hrs. Apparently, the turtles waited in the nest only so long before emerging arhythmically (during the day and at night) probably because, in the absence of a signal to emerge, they must eventually do so to begin an offshore migration. Waiting indefinitely sacrifices energy
reserves needed to power that migration (Hays et al. 1992).
Clearly, some interesting experiments remain to be done!
Acknowledgments. - We thank D. Addision, R. Forward, K.J Lohmann, J. Wyneken, and two anonymous refrees for comments that improved the manuscript. M. Reising's study at Antigua was supported by the National Save-the-Sea-Turtle Foundation of Fort Lauderdale, Florida, and permitted by Antigua Fisheries. We thank the staff of the Jumby Bay Hawksbill Project for their hospitality.
BUSTARD, H.R. 1967. Mechanisms of nocturnal emergence from the nest in green turtle hatchlings. Nature 214:317.
DRAKE, D.L. AND SPOTILA< J.R 2002. Thermal tolerances and the timing of sea turtle hatchling emergence. Journal of Thermal Biology 27:71-81.
ENRIGHT, J.T AND HAMNER, W.M 1967. Vertical diurnal migration and endogenous rhythmicity. Science 157:937-941.
GLEN, F., BRODERICK, A.C GODLEY, B.J., AND HYS, G.C. 2005.
patterns in the emergence of green (Chelonia mydas) and
Clearly, some interesting experiments remain to be done!
Acknowledgments. - We thank D. Addision, R. Forward, K.J Lohmann, J. Wyneken, and two anonymous refrees for comments that improved the manuscript. M. Reising's study at Antigua was supported by the National Save-the-Sea-Turtle Foundation of Fort Lauderdale, Florida, and permitted by Antigua Fisheries. We thank the staff of the Jumby Bay Hawksbill Project for their hospitality.
LITERATURE CITED
DRAKE, D.L. AND SPOTILA< J.R 2002. Thermal tolerances and the timing of sea turtle hatchling emergence. Journal of Thermal Biology 27:71-81.
ENRIGHT, J.T AND HAMNER, W.M 1967. Vertical diurnal migration and endogenous rhythmicity. Science 157:937-941.
GLEN, F., BRODERICK, A.C GODLEY, B.J., AND HYS, G.C. 2005.
patterns in the emergence of green (Chelonia mydas) and
loggerhead (Caretta caretta) turtle hatchlings from their nests. Marine Biology 146: 1039-1049.
GLEN, F, BRODERICK, A.C., GODLEY, B.J., AND HAYS, G.C. 2006.
Thermal control of hatchling emergence patterns in marine turtles. Journal of Experimental Marine Biology and Ecology 334:31-42.
GODFREY, M.H. AND MROSOVSKY, N 1997. Estimating the time between hatching of sea turtles and their emergence from the nest. Chelonian Conservation and Biology 2:581-584.
GYURIS, E. 1993. Factors that control the emergence of green turtle hatchlings from the nest. Wildlife Research 20:345-353.
HAYS, G.C., SPEAKMAN, J.R., AND HAYS, J.P 1992. The pattern of emergence by loggerhead turtle (Caretta caretta) hatchlings on Cephalonia, Greece. Herpetology 48:396-401.
HENDRICKSON, J.R. 1958. The green turtle. Chelonia mydas (L.) in Malaya and Sarwak. Proceedings of the Zoological Society of London 130: 455-535.
HOUGHTON, J.D.R. AND HAYS, G.C. 2001. Asynchronous emergence by loggerhead turtle (Caretta caretta) hatchlings. Naturwissenschaften 88:133-136.
MILLER, J.D., LIMPUS, C.J., AND GODFREY, M.H. 2003. Nest site selection, oviposition, eggs, development, hatching, and emergence of loggerhead turtles. In: Bolten, A.B. and witherington, B.E. (Eds.). Loggerhead Sea Turtles. Smithsonian Books, pp. 125-143.
GLEN, F, BRODERICK, A.C., GODLEY, B.J., AND HAYS, G.C. 2006.
Thermal control of hatchling emergence patterns in marine turtles. Journal of Experimental Marine Biology and Ecology 334:31-42.
GODFREY, M.H. AND MROSOVSKY, N 1997. Estimating the time between hatching of sea turtles and their emergence from the nest. Chelonian Conservation and Biology 2:581-584.
GYURIS, E. 1993. Factors that control the emergence of green turtle hatchlings from the nest. Wildlife Research 20:345-353.
HAYS, G.C., SPEAKMAN, J.R., AND HAYS, J.P 1992. The pattern of emergence by loggerhead turtle (Caretta caretta) hatchlings on Cephalonia, Greece. Herpetology 48:396-401.
HENDRICKSON, J.R. 1958. The green turtle. Chelonia mydas (L.) in Malaya and Sarwak. Proceedings of the Zoological Society of London 130: 455-535.
HOUGHTON, J.D.R. AND HAYS, G.C. 2001. Asynchronous emergence by loggerhead turtle (Caretta caretta) hatchlings. Naturwissenschaften 88:133-136.
MILLER, J.D., LIMPUS, C.J., AND GODFREY, M.H. 2003. Nest site selection, oviposition, eggs, development, hatching, and emergence of loggerhead turtles. In: Bolten, A.B. and witherington, B.E. (Eds.). Loggerhead Sea Turtles. Smithsonian Books, pp. 125-143.
MORAN, K.L., BJORNDAL, K.A., AND BOLTEN, A.B. 1999. Effects of the thermal environment on the temporal pattern of emergence of hatchling loggerhead turtles (Caretta caretta).
Marine Ecology Progress Series 189:251-261.
MROSOVSKY, N. 1968. Nocturnal emergence of hatchling sea turtles: control by thermal inhibition of activity. Nature 220: 1338-1339.
NEVILLE, A., WEBSTER, W.D., GOUVENIA, J.F., HENDRICKS, E.L., HENDRICKS, I., MARVING, G., AND MARVIN, W.H. 1988. The effect of nest temperature on hatchling emergence in the loggerhead sea turtle (Caretta caretta). In: Schroeder, B.A. (Comp.). Proceedings of the Eighth Annual Conference on Sea Turtle Biology and Conservation. NOAA Tech. Memor.
NMFS-A0SEFC-214, pp. 71-73.
REISING, M. 2014. The hawksbill rookery at Antigua, W.I.: nest success, hatchling behavior, and hatchling survival during offshore migration. MS Thesis, Florida Atlantic University, Boca Raton.
WITHERINGTION, B.E., BJORNDAL., K.A., AND McCABE, C.M. 1990.
Temporal patterm of nocturnal emergence of loggerhead turtle hatchlings from natural nests. Copeia 1990(4):1165-1168.
Recived: 28 May 2014
Revised and Accepted: 21 August 2014
Handling Editor: Jeffrey A. Seminoff
Marine Ecology Progress Series 189:251-261.
MROSOVSKY, N. 1968. Nocturnal emergence of hatchling sea turtles: control by thermal inhibition of activity. Nature 220: 1338-1339.
NEVILLE, A., WEBSTER, W.D., GOUVENIA, J.F., HENDRICKS, E.L., HENDRICKS, I., MARVING, G., AND MARVIN, W.H. 1988. The effect of nest temperature on hatchling emergence in the loggerhead sea turtle (Caretta caretta). In: Schroeder, B.A. (Comp.). Proceedings of the Eighth Annual Conference on Sea Turtle Biology and Conservation. NOAA Tech. Memor.
NMFS-A0SEFC-214, pp. 71-73.
REISING, M. 2014. The hawksbill rookery at Antigua, W.I.: nest success, hatchling behavior, and hatchling survival during offshore migration. MS Thesis, Florida Atlantic University, Boca Raton.
WITHERINGTION, B.E., BJORNDAL., K.A., AND McCABE, C.M. 1990.
Temporal patterm of nocturnal emergence of loggerhead turtle hatchlings from natural nests. Copeia 1990(4):1165-1168.
Recived: 28 May 2014
Revised and Accepted: 21 August 2014
Handling Editor: Jeffrey A. Seminoff
