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First published online April 17, 2009
Journal of Experimental Biology 212, 1302-1306 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.027425
Determinants of incubation period: do reptilian embryos hatch after a fixed total number of heart beats?
1 School of Biological Sciences A08, University of Sydney, NSW, 2006
Australia
2 Hangzhou Key Laboratory for Animal Science and Technology, College of
Biological and Environmental Sciences, Hangzhou Normal University, 310036,
Hangzhou, People's Republic of China
* Author for correspondence (e-mail: dwghz{at}126.com)
Accepted 9 February 2009
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: embryonic development, heart rate, metabolic rate, thermal dependence, reptile, thermal time
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). In many
oviparous (egg-laying) organisms, the duration of incubation of the eggs may
be a critical life-history variable. The duration of incubation relative to
the rest of the lifespan can vary even within a single phylogenetic lineage;
for example, some chameleons spend more than 50% of their total lifespan
within the egg (Karsten et al.,
2008) whereas in other lizards, the egg stage comprises <2% of
the maximum lifespan [e.g. Varanus komodoensis
(Cogger and Zweifel, 1992)].
The egg stage differs from later life-history stages in many distinctive
ecological characteristics. Most notably, embryos of most species (except
those with dispersive eggs) are immobile and thus are unable to disperse,
thermoregulate or feed or protect themselves against predators. We might thus
expect strong selection on the duration of the incubation period and on the
timing of hatching (Shine,
1978; Shine and Olsson,
2003).
Despite the strong fitness consequences of intraspecific variation in the
duration of incubation [and thus the timing of hatching, e.g. Amphibolurus
muricatus (Warner and Shine,
2007)], field studies often report extensive environmentally
induced variation in these traits, even within a single population
(Perrins, 1967;
Olsson and Shine, 1997). Some
of this variation is under parental control; for example, many birds delay
brooding the eggs until all have been laid, and the low temperatures of an
unattended nest delay the onset of embryonic development
(Stoleson and Beissinger,
1995). More generally, the thermal regime that an egg experiences
can massively alter its total incubation period, especially in species without
parental control of nest temperatures. For example, eggs of the lizard
Bassiana duperreyi can hatch in 26 days if kept at 30°C but
require more than 60 days if kept at 22°C
(Shine and Harlow, 1996).
What factors determine the relationship between incubation temperatures and
total developmental periods? The simplest explanation is that the
transformation from zygote to hatchling is prolonged by cool conditions
because temperature regulates the rate of chemical activities (including those
contributing to overall metabolic rate and hence rates of embryogenesis).
Although many additional phenomena [e.g. embryonic diapause, precocial
vs altricial hatching (Ar and
Tazawa, 1999; Andrews et al.,
2008)] can also affect the duration of the egg stage, much of the
variation in total incubation periods appears to be driven by variation in
rates of embryogenesis. Consistently, embryos developing at high temperatures
have shorter development times than those kept at low temperatures
(Deeming and Ferguson, 1991;
Hoegh-Guldberg and Pearse,
1995). This phenomenon is so widespread that it has been
formalised by the concept of `thermal time' [the linear relationship between
development rate and temperature (Honek,
1996; Trudgill et al.,
2005)].
The physiological mechanisms that link developmental time to temperature
are probably complex but the cardiovascular system is known to play a critical
role in nutrient and oxygen delivery during embryonic development
(Birchard and Reiber, 1996;
Birchard and Deeming, 2004;
Tazawa, 2005). When embryonic
growth is accelerated by higher temperature, the cardiovascular system must
deliver nutrients at an increased rate to fuel the faster growth. Therefore,
the relationship between temperature and incubation period may be driven by
the thermal dependence of cardiovascular function. In keeping with this idea,
the rate of embryonic heart beat (an indicator of cardiovascular activity) is
positively correlated with developmental rate in birds
(Ar and Tazawa, 1999;
Tazawa, 2005). Within an avian
lineage, the cumulative number of heart beats between oviposition and hatching
is relatively constant, consistent with the general constancy in heart beats
per life span for adult endotherms (Ar and
Tazawa, 1999).
Non-avian reptiles present an additional complication in this respect
because embryonic development occurs over a much wider range of temperatures
than in birds (Deeming and Ferguson,
1991). So, does the cumulative number of heart beats predict
incubation duration in lizards and turtles (as it does in birds) despite the
enormous variation in incubation periods generated by fluctuations in nest
temperatures? Although previous attempts to monitor heart rates in reptile
embryos have had to overcome major technical obstacles
(Birchard and Deeming, 2004),
recent methodological advances facilitate non-invasive monitoring
(Radder and Shine, 2006;
Du and Shine, 2008) and thus
provide an opportunity to clarify the issues raised above. In the present
study, we measured the thermal dependence of embryonic heart beat rates in
three species of non-avian reptiles. With data on the duration of incubation
at each of these temperatures, we could then calculate the total number of
heart beats of embryos during incubation. The results of these calculations
allowed us to assess whether (as in birds) we can predict the duration of
reptilian incubation from the cumulative total number of heart beats since
oviposition.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Shine et al.,
1997) for details of study area and species biology]. In May 2008,
we collected 14 T. septentrionalis eggs laid in captivity by females
recently field-collected in Zhejiang, eastern China, and obtained 35 P.
sinensis eggs from a private turtle farm, also in Zhejiang. The mean
developmental stages of embryos at oviposition [based on the classification
schemes of Hubert and Tokita and Kuratani
(Hubert, 1985;
Tokita and Kuratani, 2001)]
were stage 31, 26 and 5 for B. duperreyi, T. septentrionalis and
P. sinensis, respectively. All eggs were weighed (±0.001 g)
and individually incubated in 64 ml glass jars filled with moist vermiculite
(–200 kPa). The jars were then incubated at 25°C (for B.
duperreyi eggs) or 28°C (for T. septentrionalis and P.
sinensis eggs), close to the mean temperature of natural nests in each
species (Shine et al., 1997;
Du, 2003;
Du and Feng, 2008).
Heart rate detection
We measured heart rates of embryos approximately 25% through the total
incubation period in all species. Previous studies on one of our study species
(Radder and Shine, 2006) and
our unpublished data on both of the other taxa (W.-G.D. and R.S., unpublished
data), reveal no significant ontogenetic shift in mean heart rates from
<25% to >90% of incubation (at any given temperature); thus, the exact
timing of our heart rate measurements relative to embryogenesis should have
little impact on the rate estimates. Heart rates [beats per minute (beats
min–1)] were measured using an infrared heart rate monitor
(Buddy system; Avian Biotech;
http://www.avianbiotech.com/buddy.htm)
on day 10 in B. duperreyi, day 7 in T. septentrionalis and
day 15 in P. sinensis, respectively. All eggs were placed in
incubators set at 20°, 25°, 30°, 33° or 35°C for a two
hour acclimation period prior to measurement and were then placed individually
on the monitor to record heart rate. The Buddy system works by shining an
infrared beam onto the surface of the egg, detecting minute distortions caused
by embryonic heart beats; recording heart rates generally takes less than a
minute and does not affect the egg or embryo. As our measure of mean heart
beat rate, we used the mean rate in the first 30 s after the monitor first
gave a reliable, consistent reading (which typically occurred a few seconds
after the machine was switched on but occasionally took 10 or 15 s to
stabilise). The order of exposure of each egg to test temperatures was
random.
Calculations of total heart beats and total effective heart beats
We used the heart rate data to develop quadratic equations that describe
the relationship between test temperature and heart beat rates of individual
embryos. These equations were then used to predict the heart beat rate of
embryos at each incubation temperature. Data on the total duration of
embryogenesis (=incubation period, from oviposition to hatching) of these
species at different incubation temperatures were obtained from previous
studies [B. duperreyi (Shine and
Harlow, 1996); T. septentrionalis
(Du, 2003); P.
sinensis (Du and Ji,
2003; Ji et al.,
2003)]. We calculated relative developmental rate for a given
temperature by dividing the reported incubation duration at that temperature
by the shortest incubation duration recorded for that species in the
laboratory (25 days at 30°C for B. duperreyi, 23.5 days at
33°C for T. septentrionalis and 40 days at 33°C for P.
sinensis) and taking the inverse of this value
(Shine and Harlow, 1996). The
`developmental zero' of each species (the critical minimum temperature at
which the rate of embryogenesis fell to zero) was then calculated from the
linear relationship between developmental rate and incubation temperature
(Shine and Harlow, 1996).
Eggs of many reptile species can tolerate temperatures well below the
developmental zero [indeed, some can withstand temperatures close to freezing
(Packard and Packard, 1988)].
Although embryonic growth ceases at such temperatures
(Georges et al., 2005), the
cardiovascular system of the animals continues to function [e.g. we have
detected a heart beat of B. duperreyi embryos at 11°C (W.-G.D.
and R.S., unpublished data)] and presumably this continued metabolic effort
plays an important role in maintaining embryo viability. Accordingly, we
defined two `cumulative heart beat' parameters, based on either including or
excluding heart beats occurring at temperatures below the developmental zero.
The first parameter was the total number of heart beats (THB) of an embryo
throughout its embryonic development, calculated at any given incubation
temperature using the formula: THB = temperature-specific heart rate x
total minutes of developmental time (= from oviposition to hatching) of eggs
incubated at that temperature. Secondly, the total number of effective heart
beats (TEHB) was calculated by subtracting heart rate at developmental zero
from the formula, i.e. TEHB = (heart rate at that temperature–heart rate
at the developmental zero) x total minutes of developmental time. The
heart rate at developmental zero was estimated from the equation describing
the relationship between heart rate and temperature within each species. This
second parameter thus focuses only on heart beats likely to contribute to
embryogenesis, i.e. those above the basal heart beat rate at which embryos
survive but do not develop.
Statistical analysis
We used the software package of STATISTICS 6.0 to analyse data. Normality
of distributions and homogeneity of variances were tested using the
Kolmogorov–Smirnov test and Bartlett's test, respectively. One-way
analysis of variances (ANOVAs) were conducted to test for the influence of
incubation temperature on the total number of heart beats and the total number
of effective heart beats, and Tukey's post-hoc multiple comparisons
were used to distinguish among mean values of heart beats at each incubation
temperature.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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)
(W.-G.D. and R.S., unpublished data). Our measurements of heart beat rates in
lizard and turtle embryos reveal a broad similarity to the results of previous
studies on birds in terms of the absolute number of heart beats required to
complete embryogenesis [5 to 6x106 in the two lizard species,
8x106 in the turtle species
(Fig. 2) and approximately 6 to
13x106 in birds (Ar and
Tazawa, 1999)]. The total number of heart beats may, however, span
a wider range in some other vertebrate lineages, such as mammals [e.g. human
embryos take more than 6x107 heart beats to complete
embryogenesis whereas mouse embryos take about 5x106 heart
beats: calculated from data in Meier et al.
(Meier et al., 1983)]. Lizards
and turtles also resemble other taxa in showing a broad constancy of total
heart beat numbers within embryos of a single species
(Fig. 2). That relative
constancy applies despite a twofold variation in total incubation duration in
the non-avian reptiles we studied, a variation driven by incubation
temperature (Fig. 1B).
The numbers quoted above actually underestimate the degree of similarity
between birds, turtles and lizards in total number of heart beats during
incubation. Both turtles and birds lay eggs with relatively undeveloped
embryos, so that the period from oviposition to hatching encompasses all of
embryogenesis (Booth and Thompson,
1991; Andrews,
2004). By contrast, most squamates (including the two lizard
species that we studied) delay oviposition until the embryo is partway
(typically around 25%) through the total period of embryonic development
(Shine, 1983;
Andrews, 2004); and, thus, the
number of heart beats estimated for lizards over the period from oviposition
to hatching is substantially less than the total number over the entire course
of embryogenesis. It would be of great interest to study lizards that lay
their eggs at much earlier stages of embryonic development, as in some
chameleons (Andrews et al.,
2008) and to determine whether the inclusion of this `missing'
fraction (pre-laying) brings the sum heart beat count for lizards up to the
same level as in birds and turtles.
Despite these similarities, the total number of heart beats for embryonic
development clearly is not a fixed number and is affected both by
developmental factors (such as the degree of offspring development at laying
and at hatching) and by ecological factors (such as nest temperature). For
example, the offspring of altricial birds hatch after fewer heart beats than
do the offspring of precocial species (Ar
and Tazawa, 1999; Tazawa et
al., 2001). Similarly, egg size strongly affects heart beat rates
in birds (Ar and Tazawa, 1999)
and developmental time in many organisms
(Gillooly et al., 2002). In
non-avian reptiles, thermal conditions in the nest will probably be the most
important proximate factor affecting both heart rates and the duration of
incubation. Laboratory experiments generally have reported little to no effect
of hydric conditions on incubation duration (e.g.
Flatt et al., 2001;
Ji and Du, 2001;
Booth, 2002) or heart rates
(Du and Shine, 2008) whereas
temperature strongly affects both of these variables
(Birchard and Deeming, 2004;
Radder and Shine, 2006) (see
Fig. 1A and
Fig. 1B). The thermal
dependencies of embryogenesis and of heart rates effectively cancel each other
out over a range of warm conditions, i.e. development accelerates with
temperature as the same rate as heart beat, thus maintaining an approximate
constancy in total heart beats prior to hatching
(Fig. 2). That equivalence
disappears at lower temperatures, however, such that cool-incubated embryos
complete more heart beats prior to hatching than do their warm-incubated
siblings (Fig. 2). Although
thermal acclimation might affect the rate of embryonic heart beats [as found
in the snapping turtle, Chelydra serpentina
(Birchard and Reiber, 1996)],
most studies on this topic have concluded that the growth efficiencies and
energetics of reptilian embryos show little evidence of thermal acclimation
(Whitehead et al., 1992;
Angilletta et al., 2006).
We attribute the increase in cumulative number of heart beats at lower
temperatures to a thermally-driven shift in the magnitude of maintenance costs
relative to the cardiovascular effort devoted to `productive' embryogenesis.
At the developmental zero temperature, heart beat rates decline but do not
cease. Under these conditions, all of the embryo's metabolic work is directed
to maintenance. Below the developmental zero temperature, the embryo continues
to respire (and thus its heart continues to beat, albeit slowly) but it does
not grow or differentiate. Thus, for example, an embryo exposed to a
fluctuating thermal regime that rises above developmental zero for only a few
hours per day will necessarily accumulate a large number of `maintenance'
heart beats that achieve little or nothing towards furthering its ontogenetic
development. By the end of incubation, such an embryo will thus have completed
many more heart beats, in absolute terms, than a warm-incubated sibling. This
interpretation is supported by the constancy of `cumulative number of
effective heart beats' across a wide range of incubation conditions, in
contrast to the thermal dependence of total number of heart beats
(Fig. 2). These results support
and extend ideas regarding a constancy in the number of degree-days needed to
complete the developmental process
(Trudgill et al., 2005). The
concept of the total effective heart beat provides a functional explanation
for the relationship between incubation temperature and developmental
time.
Why don't bird eggs show similar thermal dependence in total numbers of
heart beats? They may well do so but any thermal effect is masked by the fact
that: (1) maternal brooding reduces the variance in thermal regimes during
incubation, both among eggs within a clutch and among clutches; and (2)
temperature may have little effect on heart beat rate within the bird's
thermoneutral zone (Ar and Tazawa,
1999; Tazawa,
2005). Non-avian reptiles experience different conditions. Many
embryos of oviparous reptiles develop in shallow nests that display wide
thermal fluctuations on a diel and/or seasonal cycle
(Shine et al., 1997;
Ackerman and Lott, 2004;
Shine, 2004;
Du and Feng, 2008).
Accordingly, embryos often experience temperatures below the developmental
zero for considerable periods of time. For example, developmental zero is
14.2°C in T. septentrionalis and B. duperreyi but
temperatures in natural nests have been recorded to fall to 11.6°C for
T. septentrionalis (Du and Ji,
2006) and 9°C for B. duperreyi
(Shine and Harlow, 1996).
Because they experience a more variable and less predictable thermal
environment (unlike maternally-brooded bird eggs), squamate eggs thus must be
able to adjust their total cardiovascular effort flexibly to conditions in the
nest.
|
Footnotes |
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Deceased 
We thank Melanie Elphick and Rory Telemeco for collecting B. duperreyi eggs from the field, and Hua Ye for assistance in the laboratory. Keith Simpson of Avian Biotech helped us to refine the use of the infrared monitoring system. Ethics approval was given by the University of Sydney Animal Ethics Committee. This work was supported by grants from the Natural Science Foundation of China (30770274) and the University of Sydney to W.-G.D., and by the Australian Research Council to R.S.
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