Integrative and Comparative Biology, volume 51, number 1, pp. 100–110
doi:10.1093/icb/icr045
SYMPOSIUM
Hatching Behavior in Turtles
Ricky-John Spencer1,*,† and Fredric J. Janzen‡
*Water and Wildlife Ecology Group (WWE), †Native and Pest Animal Unit (NPAU), School of Natural Sciences,
University of Western Sydney, Penrith South DC, Locked Bag 1797, NSW, 1797, Australia; ‡Department of Ecology,
Evolution, and Organismal Biology, Iowa State University, 253 Bessey, Ames, IA 50011, USA
From the symposium ‘‘Environmentally Cued Hatching across Taxa: Embryos Choose a Birthday’’ presented at the
annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2011, at Salt Lake City, Utah.
E-mail: ricky.spencer@uws.edu.au
Synopsis Incubation temperature plays a prominent role in shaping the phenotypes and fitness of embryos, including
affecting developmental rates. In many taxa, including turtles, eggs are deposited in layers such that thermal gradients
alter developmental rates within a nest. Despite this thermal effect, a nascent body of experimental work on
environmentally cued hatching in turtles has revealed unexpected synchronicity in hatching behavior. This review discusses environmental cues for hatching, physiological mechanisms behind synchronous hatching, proximate and ultimate
causes for this behavior, and future directions for research. Four freshwater turtle species have been investigated experimentally, with hatching in each species elicited by different environmental cues and responding via various physiological
mechanisms. Hatching of groups of eggs in turtles apparently involves some level of embryo–embryo communication and
thus is not a purely passive activity. Although turtles are not icons of complex social behavior, life-history theory predicts
that the group environment of the nest can drive the evolution of environmentally cued hatching.
Introduction
Developing embryos are exposed to numerous environmental factors that elicit a diversity of phenotypic
and fitness effects that are manifested both before
and after birth (e.g., Deeming and Ferguson 1991).
In oviparous species, perhaps the most influential
environmental factor during embryonic development
is temperature. Within the nonlethal range, for example, higher incubation temperatures notably accelerate embryonic development and thereby reduce
time until hatching from eggs (e.g., Andrews 2004).
This timing of birth has enormous implications
for both immediate and future survival. In animals
that produce more than one offspring, assessing environmental cues is important to synchronize birth
with siblings, thus it is not surprising that synchrony
in the timing of births has evolved in many species
(O’Donoghue and Boutin 1995). However, many factors promote intra clutch variation in incubation
period in oviparous species, including differences in
egg size, order of ovulation, and disparate thermal
microenvironments of eggs (Andrews 2004). Despite
these sources of developmental asynchrony, synchronous hatching through alteration of incubation
period occurs in many oviparous taxa, including invertebrates (Frechette and Coderre 2000), fishes
(Bradbury et al. 2005), amphibians (Sih and Moore
1993; Warkentin 1995, 2000), crocodilians (Ferguson
1985), squamates (Vitt 1991), turtles (Doody et al.
2001; Spencer et al. 2001), and birds (Lack 1968;
Vince 1969; Davies and Cooke 1983).
Data from studies of reptiles do not feature prominently in our understanding of environmentally
cued hatching. However, turtles comprise one
group where elements of this concept have been
the subject of experimentation (Doody et al. 2001;
Spencer et al. 2001; Colbert et al. 2010). Turtles ovulate clutches of eggs simultaneously, and embryonic
development is arrested within the oviducts at the
gastrula stage until oviposition (Ewert 1985).
However, as the eggs are generally deposited in several layers within a nest, environmental gradients
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Hatching behavior in turtles
treefrogs, Agalychnis callidryas, hatch early in response to egg-eating snakes and wasps (Warkentin
1995, 2000), as do the frogs Hyla regilla and Rana
cascadae in response to egg-eating leeches (Chivers
et al. 2001). The frog Hyperolius cinnamomeoventris
hatches at a smaller size when exposed to egg-eating
fly larvae (Vonesh 2000). Synchronous or spontaneous hatching is less likely to occur when eggs are
developing at different rates and hatching cues
occur well before the entire clutch has completed
development. In such cases, there are likely consequences for both short- and long-term fitness, which
provide opportunities to test ecological and evolutionary trade-off theories of optimality in the emerging field of embryonic behavior. This review focuses
on the behavior of synchronous hatching in turtles
and incorporates unpublished findings because of the
nascence of this research area. We discuss the environmental cues for hatching, the physiological mechanisms behind synchronous hatching, the proximate
and ultimate causes for this behavior in the context
of optimality theory, and future directions for
research.
Defining synchronous hatching
Synchronous emergence of neonatal turtles from the
nest is well documented (De Pari 1996; Tucker 1997,
1999; Nagle et al. 2004), although it is not ubiquitous (e.g., Kolbe and Janzen 2002), with many
marine turtles hatching throughout the day but delaying emergence until dusk or night (Bustard 1967;
Mrosovsky 1968, 1980). Indeed, social facilitation behavior of hatchling green turtles (Chelonia mydas)
occurs during emergence from the nest (Carr and
Hirth 1961). But such emergence behavior should
not be confused with synchronous hatching, which
refers to coordinated departure from eggs of fully
formed embryos (i.e., hatchlings). Experimental evidence of environmentally cued hatching in turtles
has focused on three freshwater species, where thermal variability in the shallow nests is well established
(Thompson 1988). Pig-nose turtles (Carettochelys
insculpta) can hatch spontaneously, embodying the
traditional view of synchronous hatching as described above for various anurans. Two other species
of freshwater turtle have displayed some capabilities to hatch synchronously by responding to developmental and hatching cues of clutch mates:
E. macquarii can hatch synchronously under
warmer incubation temperature regimes (Spencer
et al. 2001), and the painted turtle, Chrysemys
picta, was unable to hatch synchronously in experimental protocols, despite clearly adjusting hatching
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alter developmental rates among clutchmates
(Maloney et al. 1990; Gyuris 1993; Thompson
1997). In particular, eggs near the top of a nest
experience higher temperatures (up to 68C higher
in nests of the Murray River turtle, Emydura
macquarii), which increases developmental rates
and shortens incubation relative to eggs near the
bottom of the chamber (Thompson 1988, 1989;
Booth and Thompson 1991). Thus, hatching synchrony presumably should not occur within a
turtle nest because incubation times should differ
between eggs at the top and bottom of the nest.
Arguably,
the
best-known
example
of
environmentally cued hatching is the image of hatchling sea turtles emerging from the nest en masse.
However, this scenario confounds hatching from
eggs with emergence from the nest and does not
clarify mechanism in either case. For example, embryos might hatch synchronously because temperatures are relatively similar between the top and
bottom of the nest (Fig. 1) or because they are responding to other cues. Similarly, hatchlings dig upwards from the nest chamber (Bustard 1967), but if
they approach the surface during daylight, hatchlings
will wait until dusk to emerge from the nest (Bustard
1967; Mrosovsky 1968, 1980). Mass emergence from
the nest by sea turtles thus may result from delayed
emergence rather than environmentally cued synchronous hatching. Hence, freshwater turtles have
been used as nascent models to experimentally
assess hatching behavior because variability of temperatures within their nests (Fig. 1) conveniently disconnects temperature, embryonic development, and
the timing of hatching.
Incubation temperature is the primary determinant of incubation times in reptiles (Dmi’el 1967;
Sexton and Marion 1974; Mrosovsky and Yntema
1980; Miller 1985; Gutzke and Packard 1987;
Packard et al. 1987), but its influence on hatching
from eggs per se is not known. The timing of hatching may be phenotypically plastic within certain
boundaries set by incubation temperature, but the
actual cues for hatching derive from a range of
biotic and abiotic factors. Factors such as predation,
hypoxia, dehydration, and flooding occur commonly
in a range of ectothermic vertebrates (fish: Martin
and Swiderski 2001; Speer-Blank and Martin 2004;
amphibians: Warkentin 1995, 2000; reptiles: Doody
et al. 2001; Spencer et al. 2001). With many of these
taxa, hatching is spontaneous because embryonic development throughout a clutch is complete and the
species can enter embryonic aestivation until conditions for hatching are optimal (Georges et al. 2008).
Less common in nature is early hatching. Red-eyed
102
R.-J. Spencer and F. J. Janzen
times (Colbert et al. 2010). Spontaneous or synchronous hatching in species that hatch early or accelerate development (as opposed to delaying hatching) is
difficult to achieve, thus for the remainder of this
review the term ‘‘synchronous hatching’’ should be
understood to include any response of an embryo to
the developmental stage or hatching behavior of
clutch mates, which may not necessarily result
in spontaneous hatching, but does result in the adjustment of incubation times. Such synchronous
hatching occurs in precocial birds (Vince and
Chinn 1971) and turtles (Spencer et al. 2001,
Colbert et al. 2010).
Synchronous hatching and turtles
There has long been suspicion that hatching in sea
turtles is somewhat coordinated, similar to their
emergence from the nest. However, given that these
large animals construct deep nests where both the
thermal gradient and variance between the top and
bottom of the nest is low (Packard and Packard
1988), there is no conclusive evidence that embryos
respond to anything other than temperature. Much
research into sea turtle biology has focused on cues
for emergence (Bustard 1967; Mrosovsky 1968, 1980;
Gyuris 1993) and hatchling orientation postnest
emergence (Mrosovsky 1978; Salmon and Lohmann
1989; Lohmann 1991), thus, these turtles now need
experimental study of hatching synchrony.
As mentioned earlier, three freshwater turtle species have a demonstrated capacity to hatch synchronously in the broad sense of the term (Spencer et al.
2001; Georges et al. 2008; Colbert et al. 2010). One
other species (Chelodina longicollis) has conclusively
demonstrated that it does not have the capacity to
either delay or speed up hatching to ensure synchrony (R.-J. Spencer, unpublished data). Pig-nose
turtle nesting and embryonic developmental behavior
is primarily geared to predictable weather patterns
of northern Australia (Georges et al. 2008). The
response of C. insculpta embryos to rising water
levels promotes synchronous hatching, but there is
some evidence that biotic factors like vibration (see
below) are also cues for hatching (Georges et al.
2008). Full-developed offspring only hatch from
eggs when a nest is inundated with river water.
There is also no evidence that pig-nose turtles
hatch in a premature developmental state. On the
other hand, the Australian turtle E. macquarii
(Spencer et al. 2001) and the North American
turtle C. picta (Colbert et al. 2010) adjust incubation
period in response to some unknown factor(s)
related to developmental stage of sibling embryos
to ensure that hatching of eggs within a clutch
occurs over a short time period. In contrast, the
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Fig. 1 Temperature at various depths in freshwater turtle nesting areas at Albury, Australia. Data loggers (IBUTTONTM) were placed at
5 depths (5–60 cm), and the hole was refilled with the original sand (predominantly river sand) with little or no vegetation. Ten plots
were randomly located throughout the nesting beach (see Spencer 2002; Spencer et al. 2006) for 7 days (January 2–9, 2000). Average
(SD) temperatures are shown at each depth recorded. Small–medium-sized freshwater turtles construct nests 5–20 cm deep (light
gray region), and sea turtles construct nests 440 cm deep (dark gray region).
Hatching behavior in turtles
Australian turtle (C. longicollis) does not hatch synchronously or adjust incubation times independent
of temperature (R.-J. Spencer, unpublished data).
Mechanisms and cues of synchronous
hatching in turtles
species and nests are usually constructed close to
water (Bowen et al. 2005). Clutch sizes vary depending on female size and location, but both species
construct nests that are about 5–15 cm deep
(Jackson et al. 2004). Incubation lasts 72–80 days
in C. picta nests (Zweifel 1989) and 66–85 days in
E. macquarii nests (Cann 1998). The major difference
between the natural history of nests of C. picta and
E. macquarii is that painted turtle hatchlings in the
northern part of their range typically arrange themselves symmetrically in the nest and overwinter to
emerge the following spring (Costanzo et al. 2008),
whereas no delayed emergence occurs in E. macquarii
(Cann 1998).
Both these freshwater turtle species do not delay
hatching, unlike C. insculpta, and they can hatch
prematurely (Colbert et al. 2010) or compensate by
increasing developmental rates (J. McGlashan et al.,
submitted for publication) to synchronize hatching.
Respiration rates in reptiles and precocial birds generally drop by up to 25% before hatching occurs
(Birchard and Reiber 1995; Birchard 2000; Peterson
and Kruegl 2005), but hatching can occur at any
time after peak metabolism. The fall in metabolism
prior to hatching is present in some species as resting, or the secondary developmental stage, which is
variable in length (Fig. 2). If turtles like C. picta do
not adjust their developmental rate, they may significantly shorten the secondary development stage
(Fig. 2), which could reduce post-hatching fitness
(Colbert et al. 2010).
Premature hatching in C. picta was inferred from
behavioral and morphological assessments of neonates (Colbert et al. 2010). That is, turtles that were
known or suspected to have hatched prematurely exhibited reduced ability to turn themselves when
overturned in performance trials and typically had
substantial residual yolk extruding from the abdominal cavity. In contrast, a recent study monitored
embryonic rates of development in E. macquarii
throughout the entire incubation period and found
that these turtles do not hatch in a premature developmental state because less developed embryos responded to the presence of more advanced eggs
within a clutch by increasing metabolic and heart
rates. The assumption is that turtles have limited
capacity to regulate metabolic processes independent
of temperature, because they are ectothermic and
thermoconformers. Hence, increases in metabolic
rates and embryonic development above temperature
regimes are improbable and early, or synchronous
hatching, should be achieved through incomplete de_ 2 and
velopment (Colbert et al. 2010). Both VCO
heart rate of E. macquarii increased in response to
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Pig-nose turtles nest late in the dry season from
mid-July to early November in northern Australia
(Georges and Kennett 1988, Doody et al. 2003).
The incubation and hatching biology of C. insculpta
is different in comparison to most turtles. Eggs require 64–74 days at 308C to develop to a point where
hatching is possible (i.e., until yolk internalization)
after which they enter embryonic aestivation (Webb
et al. 1986). At the onset of aestivation, metabolic
rate decreases, embryonic growth ceases, and yolk is
used during diapause at a rate that yields an extra 59
days until yolk is exhausted (at 28–308C; Webb et al.
1986). The proximal cue for hatching is anoxia,
which can be caused by immersing eggs in water
or in a nitrogen-only atmosphere (Webb et al.
1986). In the field, torrential rain or flooding stimulates hatching (Georges 1992), an adaptation that
synchronizes hatching with the onset of the wet
season. Although a mature hatchling can remain in
the egg for 59 days to yolk exhaustion, the anoxia
stimulus to hatch in the field normally occurs within
20 days (Doody et al. 2001) after the eggs are developmentally mature (Georges et al. 2004, 2005, 2008).
Hatching of C. insculpta is typically ‘‘explosive’’
(Webb et al. 1986; Doody et al. 2001): On immersion of eggs, the turtles hatch within minutes.
Behavior of hatching clutch mates may also be important. In laboratory experiments, groups of eggs
hatched faster than single eggs treated in the same
way, indicating a function of sibling vibrations
(Georges et al. 2008).
The ability of C. insculpta to hatch early prior to
the aestivation period is limited. Nest mortality due
to flooding was 20% when turtles nested late after a
below average wet season (Doody et al. 2004). Most
nests destroyed by floods were constructed at low
elevations and had not completed development by
the time flooding began (Doody et al. 2004). In contrast, C. picta and E. macquarii do not display developmental aestivation during incubation and have the
capability of shortening the incubation period to
hatch synchronously or early (Spencer et al. 2001;
Colbert et al. 2010). Although the nesting cues may
differ slightly between the species, the timing of nesting and incubation period is similar between C. picta
and E. macquarii (Bowen et al. 2005). Nesting generally occurs in late spring-early summer in both
103
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R.-J. Spencer and F. J. Janzen
Secondary
Development
1.2
1
Vo2(ml.h-1)
0.8
0.6
Group
Incubation
Begins
0.4
0.2
0
0
10
20
30
40
50
60
70
80
Fig. 2 Metabolic profile of turtle embryos (eggs) throughout the incubation period. Solid black line represents the stimulus eggs that
have been incubated separately at warmer temperatures for the first week of development. The gray line represents eggs that are not
stimulated to increase their developmental rates throughout incubation, but reduce their secondary developmental stage to hatch
synchronously with the stimulus eggs. The dashed line represents eggs that are stimulated to increase their developmental rates and
hatch at a similar developmental stage as the stimulus eggs. The gray regions represent the secondary developmental stage. The
secondary developmental stage of eggs that simply hatch early is approximately half (dark gray region) of that of the other eggs (light
gray þ dark gray regions). Based on the metabolic profile of E. macquarii (Thompson 1989). From J. McGlashan et al. (unpublished data).
the developmental stage of neighboring eggs. This
outcome supports the dashed-line scenario illustrated
in the graphical model of the ‘‘catchup’’ hypothesis
for synchronous hatching (Fig. 2). However, differ_ 2 and heart rate in stimulated E. macences in VCO
quarii embryos do not manifest until the last
one-third of incubation, rather than throughout the
incubation period as illustrated in Fig. 2.
How development is accelerated is unknown.
Turtle embryonic development requires a fixed
number of heart beats (Du et al. 2009); thus, faster
heart rates induced by warmer temperatures should
result in shorter incubation times. But heart rate is
not fixed even at constant temperatures, hence incubation temperature may determine the upper and
lower ranges, rather than a specific heart rate, for
an individual. Heart rate in E. macquarii can vary
by up to 15% around the average rate throughout
a day, with diurnal peaks and troughs throughout
the entire incubation period (F. K. Loudon et al.,
unpublished data) (Fig. 3). It may be possible for
embryonic turtles in the presence of more advanced
eggs to maintain increased heart rates and thus develop faster than normal rates. However, diurnal patterns of heart rate have not been compared between
more- and less-developed embryos within a clutch.
At a metabolic level, maturation of cardiovascular
control mechanisms in late-term embryos may also
be important. Slight physiological increases in
metabolic (and thus, developmental) rate could provide a means to accelerate embryonic development
and growth, given the inability of an embryo to thermoregulate behaviorally. However, mechanisms responsible for ontogenetic shifts in heart rates and
metabolism are unknown, but may relate to maturation of both hormonal and nervous regulatory
systems (Crossley et al. 2003). One possible factor
is thyroid hormone, which is crucial in growth,
development, and function of most vertebrate tissues, such as brain, bone, fat, and muscle (Brent
2000). Thyroid hormone affects embryonic tissue accretion and differentiation through both metabolic
and nonmetabolic mechanisms (Fowden 1995).
Critically, thyroid hormone affects various metabolic
pathways, especially energy metabolism and also
plays a role in mammalian and reptilian metabolic
responses to temperature acclimation (HimmsHagen 1983; Stamper et al. 1990; O’Steen and
Janzen 1999; Du et al. 2010). Although thyroid hormone is a key regulator of postnatal growth and the
complex processes of transition from allantoic to
pulmonary respiration (Decuypere et al. 1991;
Dewil et al. 1996; Cassar-Malek et al. 2007), the thyroid is also one of the earliest endocrine organs to
differentiate and (Lynn 1960) thus the metabolic adjustment of turtle embryos in these experiments
could lie with changes in thyroid hormones.
Indeed, thyroid hormone plays a role in length of
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Incubation time (days)
Hatching behavior in turtles
105
the incubation process of chickens and hypoxic conditions induce its production in embryos (Decuypere
et al. 1991; Dewil et al. 1996; Buys et al. 1998; De
Smit et al. 2006).
The cues for hatching in C. picta and E. macquarii
are unknown and may differ between the species, as
do the mechanisms for synchronous hatching. With
C. picta hatching at a developmentally premature
stage, the cues for hatching are likely to be localized
toward the end of incubation when more advanced
embryos begin to hatch. Avian and crocodilian embryos may communicate developmental stage by
means of audible clicks (Driver 1965; Ferguson
1985). Additional cues might come from vibrations
of eggs in close contact at hatching or other means
of physical disturbance, such as a predator opening a
nest or disturbing a clutch (Vitt 1991; Warkentin
1995, 2000). However, vocalization is not known in
embryonic or hatchling turtles, and there is no contact between eggs during incubation in these synchrony experiments (Spencer et al. 2001; Colbert
et al. 2010; J. McGlashan et al., unpublished data;
R.-J. Spencer, unpublished data). Spencer et al.
(2001) note that sounds produced by pipping eggs
could be a potential cue, as well as the changes in
oxygen consumption, CO2 production, and heart
rate that are characteristic of the overall decrease in
metabolic rate before hatching (Birchard and Reiber
1995; Birchard 2000; Peterson and Kruegl 2005).
As described above, E. macquarii embryos are
stimulated to increase developmental rates well
before hatching. The increase in metabolic rates
during the last third of development in E. macquarii,
indicates that both elevated CO2 levels and heart
rates are plausible explanations for a potential hatching cue (Spencer et al. 2001). With eggs not incubated in contact with each other, differences in heart
rate may only be detected during the last phase of
incubation when the heartbeat strengthens. Similarly,
CO2 levels in a nest may only reach high concentrations during the last phases of incubation when embryonic development and metabolism accelerate.
High CO2 levels within a nest may indicate imminent hatching and may cue the production of thyroid hormone, as in chickens (Decuypere et al.
1991), and increased development of less advanced
embryos. Audible cues from pipping eggs and gas
exchange within a nest thus may be responsible for
synchronous or early hatching in E. macquarii and
other species. The close proximity of eggs and likely
higher CO2 concentrations in nests relative to the lab
experiment accentuate the ecological probability of
this scenario.
Proximate and ultimate significance of
synchronous hatching in turtles
Life-history theory predicts that the timing of transitions between different life stages should vary with
the costs and benefits accruing in current and succeeding stages (Werner and Gilliam 1984). Adaptive
responses of posthatching animals to predators are
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Fig. 3 Diurnal shifts from mean heart rate of eggs incubated at 268C and 308C at various stages before and after peak heart rates.
Data for up to a month before hatching were pooled, and the x axis represents hours away from the peak heart rate (from F. K.
Loudon et al., unpublished data).
106
found no support for the predator-swamping hypothesis. Instead, neonates emerging from nests,
and particularly those emerging early, had the highest survivorship. Prey that are first to perform a particular behavior may have better chances for survival
due to the lag time before predators switch to new
prey (Ims 1990; Testa 2002). The prey-switching hypothesis also supports selection for the ‘‘catchup’’
mechanisms of synchronous hatching in C. picta,
E. macquarii, and, possibly, C. insculpta. This developmental pattern makes sense if selection favors early
synchronous emergence from nests (in accordance
with prey switching) rather than delayed synchronous emergence (in accordance with predator
swamping) (Tucker et al. 2008).
Substantial costs are associated with the ‘‘catchup’’
or early-hatching mechanisms for synchronous
hatching. Increases in metabolic rate by E. macquarii
translate directly into increases in rate of embryonic
development and utilization of yolk reserves, which
are vital for the initial few weeks of neonatal development and survival (J. McGlashan et al., unpublished data). However, the costs of hatching
prematurely are likely to be more immediate. The
trade-off between the benefits of premature hatching
and the costs are primarily embedded in the secondary development period of incubation (Fig. 2).
Varying the length of this stage may have both
short- and long-term costs because secondary development is associated with the maturation of the neuromuscular system, whereas primary development
(up to the peak metabolic rate) is associated with
organ and tissue development. Examples of such
costs are reflected by Japanese quail chicks
(Coturnix coturnix japonica) with accelerated development, which take 1–2 h later to stand than normal
chicks (Vince and Chinn 1971), and by
early-hatching C. picta, whose neuromuscular function is reduced for at least 9 months after hatching
(Colbert et al. 2010). However, a subsequent release
experiment involving these C. picta neonates found
that these performance disadvantages did not appear
to translate into reduced survival early in life (P. L.
Colbert et al., unpublished data). Selection for early
hatching without reduced capabilities may be far
stronger in E. macquarii compared with C. picta
because the Australian turtle emerges from the nest
much sooner than the North American turtle.
Indeed, hatchlings in some populations of C. picta
can spend more than 9 months overwintering within
a nest (Costanzo et al. 2008) and selection may favor
individuals that minimize the mobilization of yolk
reserves during incubation because they are required
to survive overwintering. Position within the nest
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common and include morphological changes,
life-history shifts, and behavioral responses (Lima
and Dill 1989; Harvell 1990). With such a diverse
range of mechanisms underpinning synchronous
hatching in turtles, the ecological, physiological,
and evolutionary causes are also likely to be diverse.
Collectively, embryonic aestivation, explosive hatching, and sibling communication in Carettochelys are
unique adaptations for matching timing of hatching
with the onset of the wet season, especially important, given the high annual variation in timing of
nesting (Doody et al. 2001, 2004). The proximal
cue for hatching is anoxia and, as water levels increase, clarity of the aquatic environment declines
and predation risk of hatchlings may further decrease. Timing emergence from the nest with the
onset of the wet season may also maximize
food availability for hatchlings (Webb et al. 1986;
Doody et al. 2001). In Papua New Guinea, though,
hatchlings may have to contend with osmoregulatory
challenges because many nests are constructed on
coastal beaches where salinity of the surrounding
water can approach ocean water levels (Georges
et al. 2008). Irrespective of any synchronized hatching, hatchling C. insculpta emerge from the nest as
nest temperatures are decreasing, at night (Doody
et al. 2001).
The timing of hatching, the transition from egg to
larval and juvenile stages, varies with risk of mortality to both embryos and hatchlings (Sih and Moore
1993, Warkentin 1995, 2000). The link between synchronous hatching and group emergence has been
tied closely to the concept of predator swamping.
Predator swamping is typically invoked, even if
only implicitly, as an explanation for temporal and
spatial synchrony in behavior among individuals in a
population (Tucker et al. 2008). Among these instances where per capita predation is presumably diluted by synchrony are included the iconic arribada
nesting of sea turtles (Pritchard 1969) and behavioral
synchrony of hatchling turtles in nests (Tucker et al.
2008). In the olive ridley sea turtle (Lepidochelys
olivacea), first-night predation was higher for solitary
nests compared with arribada nests (Eckrich and
Owens 1995). Tucker (1997) suggested that synchronous nesting in the red-eared slider turtle (Trachemys
scripta elegans) was a predator-swamping tactic
(Tucker 1997; Tucker et al. 2008).
Most predators on hatchling turtles are generalists
(e.g., Janzen et al. 2000), so the factors responsible
for synchronization of hatching or emergence may
involve prey switching rather than predator swamping (Ims 1990). Indeed, Tucker et al. (2008) released
T. s. elegans neonates in different-sized groups and
R.-J. Spencer and F. J. Janzen
107
Hatching behavior in turtles
Conclusions and future research
This review highlights that hatching behavior in turtles is poorly understood. However, although temperature is the major factor controlling embryonic
development in ectotherms, its effects on hatching
times may be less substantial. The plasticity of hatching times in turtles may have upper and lower
boundaries roughly set by developmental stage,
within which specific biotic and abiotic factors
serve as key cues for actual hatching. These cues,
particularly in turtles that are hatching early, are
poorly known and require further in-depth experimentation. For example, communication between
siblings within nests is not a new phenomenon
(e.g., chicks [Driver 1965] and crocodiles [Ferguson
1985]). However, less obvious cues drive synchronous hatching in some species, so much so that
they induce accelerated developmental rates at certain stages of the incubation period (J. McGlashan
et al., submitted for publication). The physiological
mechanisms behind this plasticity of developmental
rate are not known but could even have implications
for understanding the evolution of endothermy in
vertebrates.
This review identifies four different mechanisms of
hatching behavior in turtles from the only four species that have been assessed experimentally (Spencer
et al. 2001; Georges et al. 2008; Colbert et al. 2010;
R.-J. Spencer, unpublished data). The breadth of
behaviors involved in development and hatching of
embryonic turtles is only just being revealed, and
clearly more experimentation is required in species
that have shown some propensity to exhibit environmentally cued hatching. Similarly, the proximate
and ultimate causes for these behaviors are not
known and require both physiological experimentation on embryonic development and hatchling release experiments to assess longer-term implications
for fitness. Hatching in turtles is not a passive activity and there is clear, but currently limited, evidence
for embryo–embryo communication in turtles.
Reptiles are not icons of complex social behavior,
but in the group environment of the nest, optimality
or trade-off theory predicts that behavior, such as
environmentally cued hatching, can evolve.
Acknowledgments
We are particularly grateful to K. Martin,
K. Warkentin, and R. Strauthman for the invitation
to present a manuscript to ICB and for organizing
the symposium ‘‘Environmentally Cued Hatching
across Taxa: Embryos Choose A Birthday’’ at the
SICB 2011 annual conference. We also thank the
Downloaded from http://icb.oxfordjournals.org/ at Iowa State University on April 12, 2012
also has profound implications for winter survival in
C. picta (Costanzo et al. 2008), thus, individuals
hatching first may have a distinct advantage in securing optimal overwintering sites within the nest
(i.e., surrounded by clutch mates near the bottom
of the nest). Winter conditions within nest chambers
can present a serious challenge to survival, even for a
cold-adapted species such as the painted turtle
(Costanzo et al. 2008). Nest thermal gradients that
differentially affect developmental rates of clutch
mates in the summer may also have differential effects on freezing mortality in the winter (Weisrock
and Janzen 1999). Hence, despite both species hatching earlier than expected, the ultimate and proximate
(i.e., increased developmental rates vs. premature
hatching) mechanisms for synchronous hatching
in C. picta may be very different from those in
E. macquarii. In contrast to C. picta, growth and
performance of accelerated E. macquarii is not significantly different from normally incubated embryos, at hatching and even several months after
hatching (J. McGlashan et al., unpublished data).
Even in species where synchronous or early hatching occurs, disparate proximate mechanisms probably underlie superficially similar phenotypic traits
(Colbert et al. 2010; J. McGlashan et al., unpublished
data). Colbert et al. (2010) suggested that phylogenetic inertia may be responsible for its presence in
modern day turtles, but for a trait to remain
common in many species, it must, at a minimum,
offer no selective disadvantage to individuals displaying it. Clearly, less-developed embryos in C. picta are
potentially disadvantaged, in terms of neuromuscular
capabilities, by hatching early. Also in species that
synchronize nesting and nest in high densities, the
dilution or predator swamping effect in reducing the
individual risk of predation may be a strong positive
selective force, but with solitary nesters, the disadvantage of synchronous hatching (reduced coordination and resources) may far exceed any advantages of
group emergence from a nest. Moreover, the trait
must be conserved across taxa. In three species of
freshwater turtles where hatching has been experimentally determined to be synchronous (or partially
synchronous), the mechanisms by which it occurs
are very different. A fourth species, C. longicollis,
does not hatch synchronously or even show signs
of developmental adjustment in response to moreor less-advanced siblings within a clutch (R.-J.
Spencer, submitted for publication). Thus, the
behavior of hatching in turtles in response to environmental cues currently has enigmatic evolutionary
implications.
108
R.-J. Spencer and F. J. Janzen
in amphibians: egg predation induces hatching. Oikos
92:135–42.
Colbert PL, Spencer R-J, Janzen FJ. 2010. Mechanism and
cost of synchronous hatching. Funct Ecol 24:112–21.
Funding
Costanzo JP, Lee RE Jr, Ultsch GR. 2008. Physiological ecology of overwintering in hatchling turtles. J Exp Zool Part A
309:297–37.
A research grant from the School of Natural Sciences
at the University of Western Sydney supported travel
to the symposium.
Crossley DA, Bagatto BR, Dzialowski EM, Burggren WW.
2003. Maturation of cardiovascular control mechanisms in
the embryonic emu (Dromiceius novaehollandiae). J Exp
Biol 206:2703–10.
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