Thermoregulatory Behavior Is Widespread in the Embryos of Reptiles and Birds

Li, Teng; Zhou, Yongkang; Hu, Rui; Du, Wei‐Guo

doi:10.1086/675065

Cited by 18 publications

(40 citation statements)

References 28 publications

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“…However, C. serpentina eggs experienced thermal gradients approaching this magnitude for only brief periods of the day, with minimal or nonexistent gradients more common. Furthermore, thermal gradients reversed direction every 12 h. Because reptile embryos require multiple days to adjust their position within the egg (Du et al 2011;Li et al 2014), embryos are physically unable to track such diel thermal variation behaviorally.…”

Section: Discussionmentioning

confidence: 99%

“…First, we tested both criteria in the common snapping turtle (Chelydra serpentina), a species that displays thermal taxis in the laboratory by moving toward a moderate heat source (Li et al 2014). Our results suggest that C. serpentina embryos in natural nests do not have the opportunity to behaviorally thermoregulate by moving within the egg.…”

Section: Introductionmentioning

confidence: 96%

“…In contrast, the egg-bound embryos of oviparous species (most reptiles) were long assumed to be at the mercy of the nest environment (e.g., Shine et al 1997;Ackerman and Lott 2004;Refsnider and Janzen 2010). Recent work, however, has demonstrated that the embryos of many amniotes-including species of turtle, crocodile, snake, and bird-adjust their positions within the egg in response to thermal gradients, actively moving toward or away from external heat sources (Du et al 2011;Zhao et al 2013;Li et al 2014). Such observations of embryonic thermal taxis raise the possibility that vertebrate ectotherm embryos behaviorally thermoregulate similar to posthatching individuals (Du et al 2011;Du and Shine 2015).…”

Section: Introductionmentioning

confidence: 99%

“…For example, embryos of the Chinese soft-shell turtle (Pelodiscus sinensis; the only species for which embryo thermal taxis speed has been quantified) require 3 days to substantially alter their position within the egg in response to a thermal gradient (Du et al 2011). All species for which embryonic thermal taxis has been demonstrated appear to require 2-4 days to adjust their position (Zhao et al 2013;Li et al 2014). Given the relatively slow speed of embryonic movement, thermal taxis could allow adaptive thermoregulation only if gradients within nests remain relatively stable over time, changing over the course of days or weeks rather than hours.…”

Section: Introductionmentioning

confidence: 99%

“…Prior studies of embryonic thermal behavior assessed thermal gradients by measuring temperature on the surface of the eggshell (difference between the warm and cool sides of the egg), finding gradients of 17C-27C (Du et al 2011;Zhao et al 2013;Li et al 2014). However, because amniote eggs are fluid-filled structures with active circulatory systems (Thompson and Speake 2004), heat convection and conduction within the egg could largely erase external thermal gradients.…”

Section: Introductionmentioning

confidence: 99%

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Reptile Embryos Lack the Opportunity to Thermoregulate by Moving within the Egg

Telemeco

Gangloff

Cordero

et al. 2016

The American Naturalist

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Historically, egg-bound reptile embryos were thought to passively thermoconform to the nest environment. However, recent observations of thermal taxis by embryos of multiple reptile species have led to the widely discussed hypothesis that embryos behaviorally thermoregulate. Because temperature affects development, such thermoregulation could allow embryos to control their fate far more than historically assumed. We assessed the opportunity for embryos to behaviorally thermoregulate in nature by examining thermal gradients within natural nests and eggs of the common snapping turtle (Chelydra serpentina; which displays embryonic thermal taxis) and by simulating thermal gradients within nests across a range of nest depths, egg sizes, and soil types. We observed little spatial thermal variation within nests, and thermal gradients were poorly transferred to eggs. Furthermore, thermal gradients sufficiently large and constant for behavioral thermoregulation were not predicted to occur in our simulations. Gradients of biologically relevant magnitude have limited global occurrence and reverse direction twice daily when they do exist, which is substantially faster than embryos can shift position within the egg. Our results imply that reptile embryos will rarely, if ever, have the opportunity to behaviorally thermoregulate by moving within the egg. We suggest that embryonic thermal taxis instead represents a play behavior, which may be adaptive or selectively neutral, and results from the mechanisms for behavioral thermoregulation in free-living stages coming online prior to hatching. KeywordsChelydra serpentina, microclim, nest, play, soil, snapping turtle, temperature Disciplines Ecology and Evolutionary Biology | Evolution | Population Biology CommentsThis article is from The American Naturalist 188 (2016) abstract: Historically, egg-bound reptile embryos were thought to passively thermoconform to the nest environment. However, recent observations of thermal taxis by embryos of multiple reptile species have led to the widely discussed hypothesis that embryos behaviorally thermoregulate. Because temperature affects development, such thermoregulation could allow embryos to control their fate far more than historically assumed. We assessed the opportunity for embryos to behaviorally thermoregulate in nature by examining thermal gradients within natural nests and eggs of the common snapping turtle (Chelydra serpentina; which displays embryonic thermal taxis) and by simulating thermal gradients within nests across a range of nest depths, egg sizes, and soil types. We observed little spatial thermal variation within nests, and thermal gradients were poorly transferred to eggs. Furthermore, thermal gradients sufficiently large and constant for behavioral thermoregulation were not predicted to occur in our simulations. Gradients of biologically relevant magnitude have limited global occurrence and reverse direction twice daily when they do exist, which is substantially faster than embryos can shift position within the...

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Reptile Embryos Lack the Opportunity to Thermoregulate by Moving within the Egg

Telemeco

Gangloff

Cordero

et al. 2016

The American Naturalist

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How frequent and important is behavioral thermoregulation by embryonic reptiles?

Shine

2018

J Exp Zool Pt A

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The debate about behavioral thermoregulation inside reptile eggs centers on the frequency (and hence, biological significance) of the phenomenon, not about its validity. Both sides of the debate agree that large eggs in shallow nests laid in sun-exposed soil will experience clines in mean temperature and (especially) diel thermal variance; that embryos in the middle phase of development have the ability to reposition themselves, and room to do so; and that small changes in developmental temperatures can influence offspring fitness. Equally, all protagonists agree that thermal clines will be too low in some other kinds of nests, and that embryonic repositioning is impossible very early and very late in development. Based on an array of other fitness-enhancing behaviors exhibited by tetrapod embryos, and general principles for recognizing adaptation, we conclude that behavioral thermoregulation inside the egg likely is adaptive in some but not all reptile species. We identify productive directions for empirical research to resolve points of contention.

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Heat tolerance of reptile embryos: Current knowledge, methodological considerations, and future directions

Hall

Sun

2020

J Exp Zool Pt A

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Aspects of global change result in warming temperatures that threaten biodiversity across the planet. Eggs of non‐avian, oviparous reptiles (henceforth “reptiles”) are particularly vulnerable to warming due to a lack of parental care during incubation and limited ability to behaviorally thermoregulate. Because warming temperatures will cause increases in both mean and variance of nest temperatures, it is crucial to consider embryo responses to both chronic and acute heat stress. Although many studies have considered embryo survival across constant incubation temperatures (i.e., chronic stress) and in response to brief exposure to extreme temperatures (i.e., acute stress), there are no standard metrics or terminology for determining heat stress of embryos. This impedes comparisons across studies and species and hinders our ability to predict how species will respond to global change. In this review, we compare various methods that have been used to assess embryonic heat tolerance in reptiles and provide new terminology and metrics for quantifying embryo responses to both chronic and acute heat stress. We apply these recommendations to data from the literature to assess chronic heat tolerance in 16 squamates, 16 turtles, five crocodilians, and the tuatara and acute heat tolerance for nine squamates and one turtle. Our results indicate that there is relatively large variation in chronic and acute heat tolerance across species, and we outline directions for future research, calling for more studies that assess embryo responses to acute thermal stress, integrate embryo responses to chronic and acute temperatures in predictive models, and identify mechanisms that determine heat tolerance.

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Thermoregulatory Behavior Is Widespread in the Embryos of Reptiles and Birds

Cited by 18 publications

References 28 publications

Reptile Embryos Lack the Opportunity to Thermoregulate by Moving within the Egg

Reptile Embryos Lack the Opportunity to Thermoregulate by Moving within the Egg

How frequent and important is behavioral thermoregulation by embryonic reptiles?

Heat tolerance of reptile embryos: Current knowledge, methodological considerations, and future directions

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