Functional Ecology 2010, 24, 112–121
doi: 10.1111/j.1365-2435.2009.01602.x
Mechanism and cost of synchronous hatching
Paul L. Colbert1, Ricky-John Spencer*,2 and Fredric J. Janzen1
1
Department of Ecology, Evolution, and Organismal Biology, Iowa State University, 253 Bessey, Ames, Iowa 50011,
USA; and 2Native and Pest Animal Unit, School of Natural Sciences, College of Health & Science, University of Western
Sydney, Locked Bag 1797, Penrith South DC, New South Wales 1797, Australia
Summary
1. Synchrony in the timing of births is thought to have evolved as a general predator avoidance
strategy. In turtles, synchronous hatching may facilitate group emergence from the nest, which
in turn, may limit predation by diluting an individual’s risk of predation or by simply swamping
predators upon emergence. However, synchronizing hatching should not be easily achieved in
natural nests because of thermal gradients affecting developmental rates.
2. We evaluated pipping synchrony in the painted turtle (Chrysemys picta), where the drive to
hatch synchronously may be reduced, because in many populations, hatching and emergence are
dissociated through hatchlings overwintering within a nest.
3. We also assessed developmental mechanisms through which synchrony occurs and explored
potential trade-offs between pipping synchrony and individual fitness by determining potential
short and long-term neuromuscular developmental costs to hatching prematurely. These data
were also used to develop a theoretical model to determine how differential embryonic maturation rates affect hatching synchrony.
4. Underdeveloped embryos pipped much earlier than expected and at similar times to their
more advanced sibs. In addition, a trade-off between hatching synchronously and neuromuscular development (motility) was evident several days after hatching and up to 9 months later, after
the overwintering period.
5. Synchronous hatching is an ancestral trait in turtles, but its relevance today is not solely for
predator avoidance in all species.
6. Abiotic factors during incubation (e.g. temperature regime and moisture) have long-term
effects on reptiles during ontogeny but it is also clear that incubation behaviour is major factor
for the persistence of these developmental costs.
Key-words: Chrysemys picta, painted turtle, behaviour, early development, long-term developmental costs, trade-off, incubation, synchronous hatching
Introduction
Synchrony in the timing of births has evolved in many species (O’Donoghue & Boutin 1995), but development in
oviparous species is primarily dependent on micro-environmental conditions, essentially making synchrony of hatching between all sibs an apparent improbability. Many
factors promote intra-clutch variation in incubation period,
including differences in egg size, order of ovulation and disparate thermal microenvironments of eggs (Andrews 2004).
Despite these potential sources of developmental asynchrony, synchronous hatching through alteration of incubation period are known in many oviparous taxa, including
invertebrates (Frechette & Coderre 2000), fishes (Bradbury
et al. 2005), amphibians (Sih & Moore 1993; Warkentin
1995, 2000), crocodilians (Ferguson 1985), squamates (Vitt
1991), turtles (Doody et al. 2001; Spencer, Thompson &
Banks 2001) and birds (Lack 1968; Vince 1969; Davies &
Cooke 1983).
Any shortening of the incubation period is likely to incur
some developmental costs; hence it is curious that hatching
synchrony occurs at all. Although organisms that exhibit
plasticity in developmental periods are diverse, the impetus is
often considered the same: predator avoidance. In amphibians, shortened developmental periods and synchronous
hatching occur during predation on egg masses by cat-eyed
snakes (Leptodeira septentrionalis, Warkentin 1995) and
social wasps (Polybia rejecta, Warkentin 2000). In addition,
perceived predation risk to neonates following hatching may
induce some amphibian embryos to prolong development
and hatching (Sih & Moore 1993; but see Anderson & Petran-
*Correspondence author. E-mail: ricky.spencer@uws.edu.au
2009 The Authors. Journal compilation 2009 British Ecological Society
Further dilemmas in reptilian incubation
ka 2003). For most other taxa, group formation as a means of
predator avoidance has been proposed to promote hatching
synchrony (Lack 1968; Clark & Wilson 1981). For chelonians
in particular, synchronous hatching may facilitate group
emergence and mass migration from nests to water (Carr &
Hirth 1961; Spencer, Thompson & Banks 2001), reducing
risks of encountering predators through swamping or the per
capita dilution of predation risk (Arnold & Wassersug 1978;
Dehn 1990). Hence, turtle species that do not emerge until
well after the last neonate in a clutch hatches should not exhibit hatching synchrony if there are associated costs (e.g.
Andrews 2004; Peterson & Kruegl 2005).
Freshwater turtles ovulate clutches of eggs simultaneously,
and embryonic development is arrested within the oviducts at
the gastrula stage until oviposition (Ewert 1985). However,
because eggs are generally deposited in several layers within a
shallow nest, environmental gradients alter developmental
rates (Maloney et al. 1990; Gyuris 1993; Thompson 1997).
Specifically, eggs near the top of a nest experience higher temperatures (up to 6 C higher in nests of the Murray River turtle, Emydura macquarii), which results in increased
developmental rates and shortened incubation periods relative to eggs near the bottom of the chamber (Thompson 1988,
1989; Booth & Thompson 1991). Thus hatching synchrony
should not occur within a freshwater turtle nest because incubation times should differ significantly between eggs at the
top and bottom of the nest. However, an Australian freshwater turtle (E. macquarii) hatches synchronously through a
mechanism whereby less developed siblings within a nest simply hatch earlier or increase development rates (independent
of temperature) in response to siblings hatching (Spencer,
Thompson & Banks 2001). This result concurs with the predator avoidance theory because the Australian turtle emerges
from the nest during rain, which may be immediately after
hatching or within 24 h (R.-J. Spencer, unpublished data).
However, if predator avoidance has broadly driven the evolution of synchronous hatching in turtles, then we would not
expect to observe this phenomenon in species that do not
emerge from the nest shortly after hatching because hatching
prematurely is likely to incur both short- and long-term costs
(Bhutta et al. 2002). The acute short- and persistent longterm costs to performance and fitness is not known in any species, but in populations where hatchling turtles remain in the
nest for an extended period after hatching, the connection
between selection for group emergence from the nest to avoid
predation and hatching synchrony should not be linked. To
test this hypothesis, we evaluated pipping synchrony in the
painted turtle (Chrysemys picta; Emydidae), a freshwater species in which many populations of neonates remain in the nest
over winter and emerge the following spring (c. 7 months
after hatching; Gibbons & Nelson 1978; Weisrock & Janzen
1999).
We investigated whether pre-term pipping and subsequent
hatching has potential short- and long-term effects on neuromuscular development. Turtles and precocial birds have similar developmental metabolic profiles during incubation,
whereby the last stages of development are characterized by a
113
reduced rate of oxygen consumption, which is thought to be
associated with maturation of the neuromuscular system
(Vleck, Hoyt & Vleck 1979; Ricklefs & Starck 1998; Peterson
& Kruegl 2005). Hence any shortening of this period may
have deleterious effects on agility and performance.
Materials and methods
STUDY SPECIES AND FIELD SITE
The painted turtle is one of the most common and widespread turtles
in North America. The species ranges from coast to coast in the
northern United States and southern Canada, and is found contiguously from the southern Great Plains to the mid-Atlantic seaboard
and into parts of the South (Ernst, Lovich & Barbour 1994). Chrysemys picta inhabits freshwater environments and deposits c. 6–20 eggs
(c. 10 in our study population; Morjan 2003) in relatively shallow terrestrial nests (c. 9 cm at our study site; Morjan 2003) (Fig. 1). Temperature differentials between the top and bottom of natural nests
may be as much as 8 C in July (F. Janzen, unpublished data), thus
developmental asynchrony in the field is likely the norm.
Eggs were obtained from natural, newly constructed nests
(<1 day old) at the Thomson Causeway, Thomson, Illinois, USA
(4157¢28¢N, 905¢56¢W). From 27 May to 1 June 2004, eggs from 16
nests were collected, labelled according to clutch and egg number
using a blunt pencil (HB), and placed in moist vermiculite for transport to a laboratory at Iowa State University. The majority of hatchlings from this population overwinter within the nest (Filoramo &
Janzen 1999).
INCUBATION METHODS
To evaluate hatching synchrony, we followed protocols similar to
Spencer, Thompson & Banks (2001). Specifically, we induced developmental asynchrony among clutch mates and then reunited eggs at a
common incubation temperature and monitored their hatching times
(Fig. 2). Ninety-six eggs were used in two experimental and two control groups that contained four clutches of six eggs in each. Experimental treatments were designed to determine how synchronous
hatching occurred, whether by less developed eggs hatching early (the
Fig. 1. Hatchling painted turtles (Chrysemys picta) overwintering
within a nest.
2009 The Authors. Journal compilation 2009 British Ecological Society, Functional Ecology, 24, 112–121
114 P. L. Colbert et al.
Fig. 2. General incubation protocol. The three basic steps employed
in this study to evaluate hatching synchrony are outlined above the
schematic. Temperatures used (T1 and T2: 26 or 30 C) depended on
the treatment considered and 11 days indicates the period over which
developmental asynchrony was experimentally established.
26 C. After developmental asynchrony was established, the stimulus
group was reunited (26 C moved: 26M) with their clutch mates held
at 30 C (30 C not moved: 30NM) and incubation continued at
30 C until hatching. The control group was also divided into halfclutches for the first 11 days of incubation, but held at 30 C (30 C
control moved: 30CM; and 30 C control not moved: 30CNM). Control clutches were then reunited and incubation resumed at 30 C
until hatching (Fig. 2). In this case, comparison of the incubation
periods of the more advanced embryos from the experimental treatment to those of the control tested whether more advanced embryos
postponed pipping in the presence of less advanced sibs (30NM vs.
30CNM).
PERFORMANCE TRIALS
‘catch-up’ hypothesis) or by more developed eggs hatching late (the
‘wait’ hypothesis) (Spencer, Thompson & Banks 2001).
Experimental group 1: ‘catch-up’
The catch-up hypothesis was tested by evenly placing the six eggs of
the clutch (four clutches) into two (three eggs in each) clear plastic
containers (20 cm · 10 cm · 5 cm). To establish developmental
asynchrony, half-clutches (three eggs) were incubated at either 26 or
30 C for 11 days (Spencer, Thompson & Banks 2001). Throughout
incubation, all egg boxes were re-hydrated weekly to maintain a water
potential of )150 kPa in the vermiculite substrate, as well as rotated
clockwise among shelves, and turned 180 within environmental
chambers twice weekly to counteract possible thermal gradients.
After this period, half clutches (three eggs) held at 30 C were
removed from their containers (30 C moved: 30M) and placed next
to their clutch mates held at 26 C (26 C not moved: 26NM).
Incubation was then carried out at 26 C until hatching (Fig. 2). The
control was treated similar to the experimental group, but the halfclutches were held at the same temperature (26 C) for the first
11 days of incubation (26 C control moved: 26CM; and 26 C control not moved: 26CNM).
Essentially, in the ‘catch-up’ experiment, eggs were incubated at
26 C except for a group of ‘stimulus’ eggs that were accelerated by
an initial 11-day period at 30 C. After this period, the stimulus group
was then reunited and incubation resumed at 26 C until hatching.
To determine the incubation period, eggs were visually inspected for
signs of pipping (the initial breaking of the egg shell by the caruncle)
at least three times daily, beginning at day 40 of incubation. Incubation period was measured as the amount of time (days) from initial
egg collection until pipping. Pipping (when the eggshell is first slit) is
better than hatching as an index of the end of the incubation period,
because it shows less variability than hatching (Gutzke et al. 1984;
Les et al. 2007). Moreover, pipping is most relevant in this study
because it is the first observable sign that individuals have actively
begun the hatching process. To test the catch-up hypothesis, we compared incubation periods of less advanced embryos from the experimental treatment to those of the controls. This comparison
demonstrates whether turtles were altering their developmental rate
or pipping prematurely (26NM vs. 26CNM).
Experimental group 2: ‘wait’
A similar methodology was used to evaluate the wait hypothesis,
except that in the ‘wait’ experiment all eggs were incubated at 30 C
except the ‘stimulus’ group that was delayed by an initial period at
Righting trials were performed to assess whether a developmental
cost was associated with the alteration in incubation periods, which
will indicate the mechanism by which synchrony was achieved. Righting ability requires balance and coordination, traits that may be
adversely affected when development time is shortened. In addition,
righting trials are a good indicator due to their possible ecological
importance in turtles; hatchlings that are unable to right themselves
during the terrestrial migration to water may be more susceptible to
avian predation (Burger 1976; Freedberg, Ewert & Nelson 2001; Steyermark & Spotila 2001).
Righting trials were performed on neonates within 12 h of hatching because emergence from the nest of some turtle species occurs
within this period (R.-J. Spencer, unpublished data). Following temperature acclimation at 22 C for 15 min, hatchlings were placed on
their carapace and we recorded the length of time required for an individual to right itself (i.e. flip over). If no movement occurred within
90 s, the trial was terminated and that individual was excluded from
analyses. All individuals that attempted movement within 90 s eventually righted themselves prior to trial termination, thus this time constraint did not excessively influence differential treatment effects.
Neonates were then placed directly on the bottom of large closed plastic cups and overwintered in c. 3 mL of distilled water. Laboratory
incubators were maintained at 5 C (temperature reduced from 22 C
by 3–4 C daily over the first 5 days) until the following spring. Turtles were checked and re-hydrated (with distilled water) every
2 weeks. Environmental temperatures were slowly (over a 3-week period) raised to 18 C at the second week of April 2005 and hatchlings
were maintained at 22 C for 48 h before righting trials were again
performed.
DATA ANALYSES
Three factors could affect hatching times in this experimental design:
initial incubation temperature (26 or 30 C), movement of eggs (i.e.
whether an egg was left in a container or placed into a different container after the first 11 days of incubation) and developmental stage
of neighbouring eggs (i.e. different in developmental stage as in experimental groups or the same developmental stage as in control groups).
A general linear model was used to evaluate the influence of these factors and their interactions on incubation period. Response variables
in each experiment were then analysed using independent t-tests to
determine whether synchrony occurred and by what mechanism
(catching-up or waiting).
We examined the impacts of initial incubation temperature, movement of eggs, developmental stage of neighbouring eggs and their
interactions on righting ability of neonates after hatching and in the
2009 The Authors. Journal compilation 2009 British Ecological Society, Functional Ecology, 24, 112–121
Further dilemmas in reptilian incubation
spring, using general linear models. Response variables in the autumn
and spring were also analysed using paired t-tests to determine
whether the method of achieving synchrony was consistent with altering developmental rates (no performance cost predicted) or incubation periods (reduced performance expected). In the spring righting
time analyses, we include data from eight additional clutches to compensate for sample size reductions resulting from post-hatching mortality and non-performing individuals. The additional eight clutches
were half of a replication of the synchrony experiment, the other half
of which was lost due to incubator failure. Although incubation periods and autumn righting times were not recorded for these individuals
from the failed experiment, all 24 clutches were treated in an otherwise identical manner and are therefore included.
In addition to analysing righting times, we also assessed reductions
in neuromuscular function by examining the treatment-specific likelihood of performance using chi-squared tests. A full (i.e. eight parameters) contingency table was used to first determine whether
heterogeneity in the likelihood of performance (righting time) based
on treatment existed, followed by several two-parameter contrasts to
ascertain the developmental mechanism underlying synchronous
hatching. For all evaluations of hatching synchrony and righting ability, the specific contrasts performed are presented alongside their
results. All analyses were performed using JMP 5.1.2 (SAS Institute
2004).
A potential complication in analysis of righting times was sex.
Chrysemys picta exhibits temperature-dependent sex determination in
which males are produced at low temperatures (typically <28Æ5 C)
and females at high temperatures (Ewert & Nelson 1991; Janzen &
Paukstis 1991). Temperatures used in this study would confound
comparisons of righting times with the addition of sex. However,
developmental asynchrony was established before the temperaturesensitive period of sex determination (the middle-third of incubation;
Bull & Vogt 1981; Janzen & Paukstis 1991). Consequently, all hatchlings from the relevant treatment and control comparisons should be
of the same sex. Hence, no between-sex comparisons are made in this
study.
Results
INCUBATION PERIOD AND SURVIVAL
Incubation periods ranged from 48 to 62 days, depending on
treatment (Fig. 3a,b). Treatment-specific incubation periods
followed the expected pattern as eggs held at 30 C for the
entire period pipped first (30CM, 30NM and 30CNM respectively), eggs held at 26 C pipped last (26NM, 26CM and
26CNM respectively), and temperature-switched eggs had
intermediate incubation periods (26M and 30M respectively).
Hatching success of eggs among treatments ranged from
83Æ3% to 100%, and winter survival of neonates from 66Æ7%
to 100%.
HATCHING SYNCHRONY
Initial incubation temperature, treatment group and most
interaction terms had a significant effect on incubation period
(Table 1). However, movement per se of eggs did not impact
incubation period (Table 1). To test for synchrony and its
causes, we compared incubation periods between particular
115
Fig. 3. Mean incubation periods (mean + SE) of eggs from the
experimental treatments: (a) catch-up and (b) wait. In the catch-up
treatment, group abbreviations along the x-axis correspond to: eggs
initially incubated at 30 C and moved to 26 C (30M), eggs initially
incubated at 26 C and not moved (26NM), control eggs initially
incubated at 26 C and moved to 26 C (26CM) and control eggs initially incubated at 26 C and not moved (26CNM). In the wait treatment, group abbreviations along the x-axis correspond to: eggs
initially incubated at 26 C and moved to 30 C (26M), eggs initially
incubated at 30 C and not moved (30NM), control eggs initially
incubated at 30 C and moved to 30 C (30CM), and control eggs initially incubated at 30 C and not moved (30CNM). *Significant difference in incubation times between treatments NS, no significant
differences in incubation times between treatments.
Table 1. Hatching synchrony general linear model results
Source of variation
d.f.
F
P
Treatment (experimental and control)
Movement
Initial temp
Treatment · movement
Treatment · initial temp
Movement · initial temp
Treatment · movement · initial temp
Residual
Total
1
1
1
1
1
1
1
84
91
37Æ7
2Æ1
514
0Æ8
142
34Æ0
63Æ3
<0Æ001
0Æ156
<0Æ001
0Æ380
<0Æ001
<0Æ001
<0Æ001
Bold indicates significance below 0.1.
2009 The Authors. Journal compilation 2009 British Ecological Society, Functional Ecology, 24, 112–121
116 P. L. Colbert et al.
treatment groups. Specifically, we tested the hypotheses that
the mean incubation periods of eggs in the catch-up and
wait #262experimental groups were not significantly different
(Fig. 3a,):
H0 : 30M ¼ 26NM (Fig. 3a)
H0 : 26M ¼ 30NM (Fig. 3b)
Hatching did not occur synchronously in either treatment
(t22 = 12Æ1, P < 0Æ001 and t21 = 2Æ6, P < 0Æ009 respectively); nevertheless, incubation periods of eggs in the catchup treatment support the hypothesis that less developed
embryos in the presence of more developed sibs (stimulus
group), pip earlier than expected (Fig. 3a).
Ha : 26NM<26CNM (Fig. 3a)
Eggs incubated at 26 C with the stimulus group next to
them (26NM) pipped up to 6 days earlier than eggs kept at
26 C with sibs of the same developmental stage next to them
(26CNM; t21 = 6Æ4, P < 0Æ001). In contrast, the wait
hypothesis was not supported. Incubation periods of eggs
held at 30 C with the less advanced stimulus group (30NM)
did not differ from eggs held at 30 C with sibs of the same
developmental stage (30CNM; t22 = 0Æ5, P = 0Æ3), indicating that incubation is not prolonged in the presence of less
developed eggs.
DEVELOPMENTAL COSTS
Initial incubation temperature, treatment group and their
interaction had a significant effect on righting ability of neonates following hatching (Table 2a). However, neither movement of eggs nor any interaction with movement significantly
impacted righting ability (Table 2a). To test the underlying
mechanism of shortening incubation periods, we investigated
whether a developmental cost (i.e. long righting times) was
apparent in groups known (26NM) or thought (26M) to have
pipped early. Specifically, we tested the hypotheses that the
mean righting times of neonates with shortened incubation
periods were not significantly different from their sibs and ⁄ or
corresponding controls (Fig. 4a,b):
H0 : 26NM ¼ 26CNM; 30M (Fig. 4a)
H0 : 26M ¼ 30NM (Fig. 4b)
t-Tests showed that turtles incubated at 26 C with the
advanced stimulus group next to them (26NM) took significantly longer than their more advanced sibs (30M; t21 = 4Æ6,
P < 0Æ001) and controls (26CNM; t20 = 63Æ9, P < 0Æ001)
to right themselves (66Æ69 s vs. 12Æ33 and 15Æ56 sec respectively; Fig. 3a). Similarly, turtles initially incubated at 26 C
and placed next to their stimulus group (26M) took significantly longer than their sibs (30NM) to right themselves (60 s
vs. 11 s; t21 = 3Æ0, P < 0Æ004; Fig. 3b).
Failure to perform during autumn righting trials was noted
solely among early hatching treatments (Table 3), and
resulted in significant heterogeneity in the likelihood of hatch-
Table 2. Righting trial general linear model results: (a) following
hatching and (b) following winter
Source of variation
(a)
Treatment (experimental and control)
Movement
Initial temp
Treatment · movement
Treatment · initial temp
Movement · initial temp
Treatment · movement · initial temp
Residual
Total
(b)
Treatment (experimental and control)
Movement
Initial temp
Treatment · movement
Treatment · initial temp
Movement · initial temp
Treatment · movement · initial temp
Residual
Total
d.f.
F
P
1
1
1
1
1
1
1
80
87
13Æ0
0Æ9
54Æ6
0Æ2
21Æ0
0Æ1
0Æ8
<0Æ001
0Æ340
<0Æ001
0Æ661
<0Æ001
0Æ731
0Æ384
1
1
1
1
1
1
1
76
83
12Æ5
0Æ1
5Æ4
3Æ7
14Æ1
1Æ3
1Æ6
<0Æ001
0Æ72
0Æ022
0Æ058
<0Æ001
0Æ257
0Æ213
Bold indicates significance below 0.1.
lings to perform (v27 = 27Æ9, P < 0Æ001). Neonates that pipped early in the catch-up experiment (26NM) were
significantly less likely to perform than their sibs (30M;
v21 = 5Æ6, P = 0Æ018) and corresponding controls (26CNM;
v21 = 6Æ4, P = 0Æ01; Table 3). Likewise, suspected earlyhatching individuals in the wait treatment (26M) were also
significantly less likely to perform than their sibs (30NM;
v21 = 6Æ8, P = 0Æ009; Table 3).
Following winter, treatment group, initial incubation temperature and their interaction had a significant effect on righting ability of neonates (Table 2b). As in the autumn, egg
movement alone did not significantly impact righting ability.
However, the interaction between movement and treatment
was marginally significant in the spring (Table 2b). To evaluate whether developmental costs associated with shortened
incubation periods were persistent, we made the same treatment-specific comparisons as in the autumn (Fig. 4c,d):
H0 : 26NM ¼ 26CNM; 30M (Fig. 4c)
H0 : 26M ¼ 30NM (Fig. 4d)
Developmental costs were still apparent following overwintering, albeit somewhat reduced; early hatching treatments
shortened righting times by c. 20 s in both cases. Yet, in the
catch-up treatment, individuals known to have pipped prematurely (26NM) still took significantly longer than their sibs
(30M; t26 = 4Æ76, P < 0Æ001) and controls (26CNM;
t22 = 4Æ2, P < 0Æ001) to right themselves (47 s vs. 10 and 9 s
respectively; Fig. 4c). In the wait treatment, individuals
thought to have pipped prematurely (26M) also took longer
than their sibs (30NM) to right themselves (40 s vs. 18 s),
although this difference was but marginally nonsignificant
(t13 = 1Æ67, P = 0Æ06; Fig. 4d). Retrospective power analysis of the t-test comparison estimated power at 0Æ38, indicat-
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Further dilemmas in reptilian incubation
117
Fig. 4. Mean righting times (mean + SE) of
hatchlings prior to (autumn) and following
(spring) overwintering: (a), (c) catch-up and
(b), (d) wait. In the catch-up treatment, group
abbreviations correspond to: hatchlings initially incubated at 30 C and moved to 26 C
(30M), hatchlings initially incubated at 26 C
and not moved (26NM), control hatchlings
initially incubated at 26 C and moved to
26 C (26CM), and control hatchlings initially incubated at 26 C and not moved
(26CNM). In the wait treatment, group
abbreviations correspond to: hatchlings initially incubated at 26 C and moved to 30 C
(26M), hatchlings initially incubated at 30 C
and not moved (30NM), control hatchlings
initially incubated at 30 C and moved to
30 C (30CM), and control hatchlings initially incubated at 30 C and not moved
(30CNM).
ing that the sample size for this contrast (n = 15; Table 3)
was insufficient given our observed effect size (d = 11Æ02).
Significant heterogeneity existed among treatments in the
likelihood of hatchlings to perform during spring righting trials (v27 = 27Æ88, P < 0Æ001). Five of eight treatments exhibited higher proportions of non-performers than expected
(higher than 30%), including both early hatching experimental treatments (26NM and 26M) and all warm incubation
treatments (30NM, 30CNM and 30CM; Table 3). Treatment-specific contrasts provided additional support for the
view that altering incubation periods elicited chronic reductions in neuromuscular function. Neonates that pipped early
in the catch-up experiment (26NM) were significantly less
likely to perform than their sibs (30M; v21 = 13Æ41,
P < 0Æ001) and corresponding controls (26CNM;
v21 = 7Æ58, P = 0Æ007; Table 3). In the wait treatment, sus-
Table 3. Proportion of non-performers during autumn and spring
righting trials. Values are reported as the number of non-performing
individuals per the total number of hatchlings evaluated. Treatment
abbreviations are as described in the Methods
Autumn
non-performers
Spring non-performers
(n non-performers (n non-performers ⁄
Experiment Treatment ⁄ n total)
n total)
Catch-up
Wait
30M
26NM
26CM
26CNM
26M
30NM
30CM
30CNM
0⁄9
4 ⁄ 11
0 ⁄ 10
0 ⁄ 11
4 ⁄ 11
0 ⁄ 12
0 ⁄ 12
0 ⁄ 12
1 ⁄ 21
11 ⁄ 19
3 ⁄ 20
3 ⁄ 19
5 ⁄ 11
2 ⁄ 11
4⁄9
7 ⁄ 10
pected early-hatching individuals (26M) were substantially
less likely to perform than their sibs (30NM; Table 3),
yet this difference was not statistically significant
(v21 = 1Æ89, P = 0Æ17).
Discussion
HATCHING SYNCHRONY
Contrary to expectations based on current adaptive theory,
we detected a similar catch-up mechanism in our population
of C. picta to freshwater turtles that emerge from the nest
shortly after hatching (Spencer, Thompson & Banks 2001).
Failure of less advanced embryos to fully catch-up to their
sibs in this study is probably due to the length of time over
which developmental asynchrony was established. Spencer,
Thompson & Banks (2001) established developmental asynchrony over a 7-day period; however, we allowed 11 days
before reuniting clutch mates. The resulting difference in
developmental stage between more and less advanced
C. picta embryos appears to have been beyond a critical point
where synchronous hatching can still occur. Developmental
rate is highly dependent on incubation temperature in general
(Deeming & Ferguson 1991; Thompson 1997), but the
strength of the temperature effect on developmental rate may
be dependent on developmental stage (Birchard & Reiber
1995; Birchard 2000; Shine & Elphick 2001; Andrews 2004).
Development time necessary for neurulation, organogenesis
and early growth decreases with increasing temperature,
while the length of the late growth interval is independent of
temperature (Andrews 2004). In the context of our study, this
pattern means that less advanced embryos from the catch-up
(26NM) and wait (26M) treatments were even farther behind
in development, and had even less chance to catch-up, than
2009 The Authors. Journal compilation 2009 British Ecological Society, Functional Ecology, 24, 112–121
118 P. L. Colbert et al.
predicted if temperature and developmental rate varied
linearly.
We used pipping instead of actual hatchling emergence
from the egg to test for synchronous hatching in C. picta.
Although pipping coincides with various physiological
changes to prepare the neonate for life outside the egg, the
time interval between pipping and hatching is subject to variability both among and within clutches. So pipping may actually signify a willingness for an individual to hatch; in reality,
turtles that pipped prematurely may take significantly longer
to emerge from the egg than their more advanced sibs.
Means of communication of developmental stage
between embryos could not be discerned in this study, and
is poorly known for turtles. Avian and crocodilian embryos
may communicate developmental stage by means of audible
clicks (Driver 1965; Wolf, Bixby & Capranica 1976;
Ferguson 1985; Nicolai, Sedinger & Wege 2004). 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 turtles, and there was no contact between eggs during
incubation in our experiment. Spencer, Thompson & Banks
(2001) note that the auditory sounds produced in pipping
could be a potential cue, as well as the changes in oxygen
consumption, carbon dioxide production and heart rate
that are characteristic of the overall decrease in metabolic
rate before hatching (Birchard & Reiber 1995; Birchard
2000; Peterson & Kruegl 2005).
COSTS OF ALTERING INCUBATION PERIODS
The autumn righting trials (after hatching) clearly show that
hatching early comes at an immediate developmental cost to
coordination and movement, which is consistent with the
hypothesis that shortened incubation periods were achieved
by hatching prematurely rather than accelerating developmental rates. This undermines current theory for a single,
predator avoidance-driven origin for synchronous hatching
in turtles. In addition, the long righting times of less advanced
sibs in the wait treatment is evidence that these individuals
also pipped prematurely in the presence of more advanced
sibs (Fig. 4b). This finding is consistent with late-developmental patterns of precocial birds: which shorten developmental times (Cannon, Carpenter & Ackerman 1986) and
subsequently have reduced motor skills (Vince & Chinn
1971).
Incubation temperature can have profound long-term
effects on vital life history parameters of reptiles. Lower incubation temperatures reduced hatchling performance in two
other emydid turtles (Freedberg, Ewert & Nelson (2001), and
Spencer, Janzen & Thompson (2006) demonstrated the effect
of incubation temperature on growth of wild Australian turtles until the ages of 4–5. However, incubation temperature
alone could not account for the variation (early hatching = slower righting times) observed in righting ability. The
long-term effect observed in this study suggests that some
deeper physiological or neurological adjustment has
occurred. The lack of statistically significant differences in
both spring righting times and performance probabilities
between early-hatching turtles and their sibs from the wait
treatment (26M vs. 30NM) is probably due to a combination
of reduced sample size and temperature effects. Turtles from
warm incubation treatments exhibited high incidence of nonperformers, thus making distinctions between groups less
apparent than in catch-up comparisons. Such temperature
effects become more clear when comparing the frequency
of non-performers among control treatments only; hatchlings that experienced warm incubation conditions were
significantly less likely to perform than those produced
from low temperatures (57Æ9% vs. 15Æ4% non-performers;
v21=11Æ14, P<0Æ001). As such, we believe that in both cases,
persistent performance reductions were significantly linked to
the alteration in incubation periods, a result that does not
support the theory that synchronous hatching is a general
response to predation in turtles (Spencer, Thompson & Banks
2001).
POSSIBLE SIGNIFICANCE OF HATCHING SYNCHRONY
IN C. PICTA
It is not understood why synchronous hatching occurs in our
population of C. picta, but we do know that it can have significant long-term effects on performance and co-ordination.
Group formation theory for the evolution of hatching synchrony is not applicable when hatching and emergence are
substantially decoupled because formation of groups is intrinsic. Instead, in species like C. picta, and other species that can
also overwinter in the nest, hatching early may be adaptive
prior to emergence from the nests. Position within the nest
has profound implications for winter survival, 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 (Lindeman 1991; Packard et al. 1997; Packard & Packard 2004). 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.
Costanzo et al. (1995) reported that minimum temperatures
experienced at depths of 5 cm vs. 10 cm (the typical range for
C. picta nest chambers) were as much as 2 C lower during
two winters in Garden County, Nebraska, USA. Furthermore, the cumulative amount of time of potential freezing
events experienced at 5 cm was from 98 to 504 h longer than
at 10 cm. In addition, hatchlings on the periphery of the nest
may be at greater risk of freeze mortality as they are more
likely to come in contact with soil, ice and ice nucleating
agents (Hotaling, Wilhoft & McDowell 1985; Costanzo et al.
2000). Hence, synchronously hatching may be a response to
compete for overwintering positions, but whether hatchlings
actually ‘jockey’ for position within the nest remains a question for future investigation.
2009 The Authors. Journal compilation 2009 British Ecological Society, Functional Ecology, 24, 112–121
Further dilemmas in reptilian incubation
Although shortening the developmental period had significant long-term negative effects on coordination and movement of neonatal painted turtles, whether these behavioural
differences are selected against in nature is unknown. Synchronous hatching may represent a primitive trait in this species retained through phylogenetic inertia. In some
populations, the majority of C. picta hatchlings emerge from
the nest prior to winter, indicating that autumn nest emergence is possibly an ancestral trait (Costanzo, Lee & Ultsch
2008). The potential ubiquity of synchronous hatching within
Testudines is supported by the presence of this phenomenon
in two species as distantly related as C. picta (megaorder
Cryptodira, hidden-necked turtles) and E. macquarii (megaorder Pleurodira, side-necked turtles; Ernst & Barbour 1989).
Such a scenario does not rule out a single, group formationdriven origin of synchronous hatching in turtles. However,
group emergence of neonates, even in classic sea turtle examples, may not be as prevalent as commonly perceived (Houghton & Hays 2001).
THEORETICAL CONSIDERATION OF SYNCHRONOUS
HATCHING IN TURTLES
We developed a general model to describe a possible mechanism behind synchronous hatching and provide a theoretical
framework of interspecific and intraspecific comparisons.
The constant-temperatures synchrony (CTS) model (Fig. 5)
makes four primary assumptions. First, physical developmental rates differ significantly between the top and bottom
eggs in a nest, only up to a period of late growth, at which
point they do not differ. Second, plasticity in hatching time
must also occur whereby a minimum embryonic stage exists
at which stage, hatching can also occur. Similarly, a maximum embryonic stage exists at which hatching must occur,
and these stages are independent of temperature. Third, the
minimum and maximum hatching stages correspond to minimum (early-hatching) and maximum (full-term) incubation
periods, respectively, the lengths of which are dependent on
temperature. Temperature-dependent incubation periods
result in the potential for hatching asynchrony. Finally, a
characteristic synchrony potential exists in the form of a right
triangle, the area of which is determined by the lengths of the
intervals between the minimum and maximum developmental
stages for hatching and the resultant minimum and maximum
incubation periods.
The CTS model demonstrates clearly that hatching synchrony occurs when synchrony potentials overlap, a situation
that would arise when temperature differentials within a nest
are small, or when synchrony potentials are large. In addition,
synchrony potentials could be used to derive incubation plasticity indices for any given species under standard conditions,
and thus a means for comparisons. Although fluctuating nest
temperatures can be converted to constant temperature
equivalents (CTEs; Georges 1989), differences in egg size,
composition and metabolic rate may affect the CTS model.
However, the CTS model is useful for visualizing the tradeoff between the advantages of hatching synchronously and
119
Fig. 5. Constant-temperatures synchrony model. On the y-axis is
developmental stage, the x-axis is time and the solid lines correspond
to the developmental rate of eggs near the top (rate 1) and bottom
(rate 2) of the nest. The model assumes that a minimum embryonic
stage exists at which point hatching may occur, and a maximum
embryonic stage exists at which point hatching must occur, and these
stages are independent of temperature. The minimum and maximum
embryonic stages for hatching correspond to early (E1 and E2) and
full-term (T1 and T2) hatching times respectively. The inflection point
of the ‘rate 1’ line indicates the onset of late development, when developmental rate is no longer influenced by temperature. The model
assumes that a characteristic ‘synchrony potential’ exists, the area of
which corresponds to a species’ incubation plasticity and therefore
the likelihood of hatching synchrony. As no evidence has been found
for waiting to occur, this potential is absent. Hatching synchrony
occurs in areas of overlap between synchrony potentials.
the costs of altering incubation periods, and leads to several
predictions regarding patterns in synchrony potential.
In conclusion, synchronous hatching in turtles comes at a
developmental cost, but whether these laboratory tests translate into reduced fitness in the field is unknown. It is likely that
synchronous hatching is an ancestral trait in turtles, but its
relevance today is not solely for predator avoidance in all
species.
Acknowledgements
We thank R. Paitz and N. Fry for assistance in nest location and egg collection, Y. Ortiz and K. Birk for their help in setting up and maintaining experimental treatments, K. Bowen and S. Titterington for their aid in
measurements of hatchling morphology and performance, and the rest of the
Janzen Lab and Turtle Camp crews for their support. As always, we are
indebted to the U.S. Army Corps of Engineers and the U.S. Fish and Wildlife
Service for permitting us access to lands under their purview. K. Bowen, J.
Costanzo, multiple anonymous reviewers and numerous Janzen Lab members
offered constructive comments on early drafts of this manuscript. Eggs were
collected under Illinois DNR permit NH04.0073 and experiments were performed in accordance with COAC protocol 6-04-5684-DJ from Iowa State
University. This research was supported by a National Science Foundation
grant DEB-0089680 awarded to F.J.J.
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Received 6 August 2008; accepted 22 May 2009
Handling Editor: Raoul van Damme
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