Download Light increases the rate of embryonic development

Functional Ecology 2011, 25, 769–776
doi: 10.1111/j.1365-2435.2011.01847.x
Light increases the rate of embryonic development:
implications for latitudinal trends in incubation period
Caren B. Cooper*,1, Margaret A. Voss2, Daniel R. Ardia3, Suzanne H. Austin4 and
W. Douglas Robinson4
1
Cornell Lab of Ornithology, 159 Sapsucker Woods Rd., Cornell University, Ithaca, New York 14850, USA; 2School of
Science, The Pennsylvania State University at Erie, Behrend College, 4205 College Drive, Erie, Pennsylvania 16563,
USA; 3Department of Biology, Franklin and Marshall College, Lancaster, Pennsylvania 17604, USA; and 4Oak Creek
Lab of Biology, Department of Fisheries and Wildlife, 104 Nash Hall, Oregon State University, Corvallis, Oregon 97331,
USA
Summary
1. In wild birds, incubation period shortens and the general pace of life quickens with distance
from the equator. Temperature and various biotic factors, including adult behaviours, cannot
fully account for longer incubation periods of equatorial birds and only explain some of the variation between tropical and temperate life histories. Here we consider the role of differences in
light in driving variation in incubation period. In poultry, incubation periods can be experimentally shortened by exposing eggs to light. The positive influence of light on embryonic growth,
called photoacceleration, can begin within hours after an egg is laid.
2. We artificially incubated house sparrow (Passer domesticus) eggs under photoperiods similar
to those found at temperate (18Light : 6Dark) and tropical (12L : 12D) latitudes. We also measured embryonic metabolic rate during light and dark phases.
3. Eggs of house sparrows collected from the wild developed more rapidly under ‘temperate’
than ‘tropical’ photoperiods and had higher metabolic rates during phases of light exposure than
during phases of darkness. Metabolic rates during light phases were high enough to account for
a 1 day difference in incubation periods between temperate and tropical birds.
4. Based on a synthesis of photoacceleration studies on domesticated galliformes and our experimental results on a wild passerine, we provide the first support for the testable hypothesis that
differences in photoperiod may influence variation in the rate of embryonic development across
latitudes in birds.
Key-words: avian incubation period, embryonic metabolic rate, house sparrow, life-history
evolution, Passer domesticus, photoacceleration, photocycles, photoperiod
Introduction
Organisms exhibit a myriad of behavioural, physiological,
and anatomical adaptations that occur in limited sets of
combinations (i.e. life history strategies). These traits tend
to co-vary and form recurring associations, forming a lifehistory axis characterized as a continuum from a fast to
slow pace of life (Ricklefs & Wikelski 2002). In general,
pace of life increases with latitude. For example, bird species that breed at temperate latitudes typically have higher
metabolic rates (Wiersma et al. 2007), lay more eggs per
nest (Moreau 1944; Lack & Moreau 1965), have shorter
*Correspondence author. E-mail: [email protected]
incubation periods (Ricklefs 1969), and higher nestling
growth rates (Ricklefs 1976) than in closely related tropical
species.
The metabolic pattern of avian development is unique
among vertebrates. Effectively ectotherms early in development, embryos depend on external sources of heat to grow
until development has advanced enough to establish homeothermy, which occurs several days after hatching in altricial
birds. Temperature, atmospheric gases, humidity, and light
influence the rate and quality of embryo growth (Shutze
et al. 1962; Romanoff & Romanoff 1967). Surprisingly,
patterns of female nest attendance, and resulting incubation
temperatures, fail to fully account for latitudinal trends
for incubation periods of birds (Ricklefs 1969; Tieleman,
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770 C. B. Cooper et al.
Williams & Ricklefs 2004; Robinson et al. 2008), particularly when accounting for phylogenetic constraints (Martin
et al. 2007).
Lines of latitude are merely human constructs that describe
a suite of selective pressures actually responsible for latitudinal variation in life-history traits. Many studies focus on
biotic factors as potential drivers of latitudinal patterns, such
as the ultimate and proximate roles of food limitation (Lack
1968), predation on offspring (Skutch 1949, 1985; Martin
et al. 2000), and rates of adult mortality (Karr et al. 1990;
Johnston et al. 1997; Brawn et al. 1999). Incubation period is
a critical variable to consider in life-history studies because
variation in developmental rates has cascading consequences
that influence expression of other traits via carry-over effects
throughout an organism’s entire lifetime (Blount et al. 2006).
Adult attendance and incubation temperature have long been
considered the primary factors affecting latitudinal variation
in incubation period. Yet recent studies have shown conflicting results, which may reflect a diversity of selective pressures
influencing this trait (Ricklefs 1969; Tieleman, Williams &
Ricklefs 2004; Robinson et al. 2008; but see Martin et al.
2007). Research on biotic factors may produce varying results
because the biotic factors may not vary as consistently with
latitude as abiotic factors. The contribution of abiotic factors,
such as those associated with variation in sunlight, is relatively unexplored. To our knowledge, no studies of wild birds
have looked at the role of the abiotic factor sunlight on latitudinal differences in incubation period. We investigated light
because photoperiod is a patently reliable component of the
environment varying predictably with latitude, and it is wellestablished that light increases embryonic development rates
in domesticated species.
HOW LIGHT AFFECTS EMBRYONIC DEVELOPMENT:
INSIGHTS FROM DOMESTICATED SPECIES
In the mid-1960s the poultry industry discovered that light
intensity above a certain threshold accelerated embryonic
development (photoacceleration in sensu Shutze et al. 1962;
Isakson, Huffman & Siegel 1970), prompting experiments to
evaluate possible mechanisms.
There are marked differences between the development
rates of chicken embryos incubated under continuous highintensity light (1100–3000 lx) and those incubated under
continuous darkness. Embryos exposed to light hatched
approximately 1 day earlier than those receiving no, or only
a short pulse of, daily light (Lauber 1975; Ghatpande, Ghatpande & Khan 1995). Photoperiod also affects embryonic
growth and development. Poultry embryos exposed to continuous light produced the shortest incubation periods (Siegel et al. 1969), while those exposed to 12-h light-dark cycles
took 0 to 5 h longer to hatch (Walter & Voitle 1972, 1973;
Rozenboim et al. 2004). The rate and mechanism of photoacceleration varies with stage of embryo development.
Light stimulation produces the fastest rate of embryonic
development during early incubation and a less rapid rate
during the middle of incubation. Light stimulation during
the last week of incubation did not have any apparent effect
on development (for an overview see Siegel et al. 1969). In
experiments comparing 0 and 24-h light treatments, differences in embryonic development can often be detected after
as few as 10 h (Siegel et al. 1969).
The physiological mechanisms by which light stimulates
embryonic growth and development differ prior to and after
formation and maturation of retinal photoreceptors, the
hypothalamic pacemaker and the pineal gland – the primary
components of the avian circadian system (reviewed in Dawson et al. 2001). Light appears to stimulate mitosis in neural
crest mesoderm during the first 2 days of chicken embryo
development, accelerating closure of the neural tube (embryonic d1 or stage 7 of the Hamburger–Hamilton (H–H) classification of avian embryonic development) and subsequent
somite development (Isakson, Huffman & Siegel 1970). This
is consistent with observations that high light intensity
increases embryonic cell proliferation (Ghatpande, Ghatpande & Khan 1995). Recently, Halevy et al. (2006) demonstrated that mesodermal differentiation into myoblast cells
occurred earlier (embryonic d5) in embryos exposed to green
light (560 nm). This process is regulated by a known family
of transcription factors (MyoD) and may be triggered by
photic cues from retinal or pineal photoreceptors acting on
the neuroendocrine system (Halevy et al. 2006). There is also
evidence that when light penetrates to the cellular level, as
would be possible in early stage avian embryos, it can directly
activate cytochromes in the mitochondrial electron transport
chain and stimulate cellular metabolism (Karu 1988). Work
with mammalian cells in the 1980s provided evidence that
visible light can regulate cellular metabolism by way of
cAMP, subsequently leading to the initiation of DNA synthesis (Karu 1988). Thus, light may influence gene expression
during early development (d1 to d5 in chickens embryos),
thereby accelerating the growth process (Shafey 2004). After
the formation of the pineal gland (H-H stage 17, d3 in chickens), entrainment of the avian embryo to photoperiod is
mediated by production of melatonin (Hill et al. 2004). Light
reduces melatonin production (Akasaka et al. 1995) while
increased melatonin production occurs at night (Dawson &
Van’t Hof 2002). As little as 1 h of light decreases melatonin
production in embryonic chickens (Zeman et al. 1999); and
even very low light intensity (e.g. as low as 0Æ15 lx) can
reduce melatonin production in mammals (Lynch, Deng &
Wurtman 1984). Similarly, low light intensity (10 lx) can
entrain embryonic starlings, Sturnus vulgus (Gwinner, Zeman
& Klaassen 1997). Note that natural light levels in North
American nest boxes often exceed this level during the breeding season (183 ± 196 lx, range 5Æ3–650 lx; M. Voss, unpublished data). Light also influences the activity of clock genes
found in some avian tissues (e.g. multiple regions of the
brain, the ovary; Nakao et al. 2007); however little is known
about the embryonic ontogeny of avian circadian clocks
(Okabayashi et al. 2003). What is known suggests that avian
circadian clocks mature late in the embryonic chicken (d16 in
the suprachiasmatic nucleus; d18 in pineal gland Okabayashi
et al. 2003; d19 retinal photoreceptors Wai et al. 2006), when
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Light and embryo metabolism 771
photoacceleration is no longer significant (Siegel et al. 1969).
Regardless of the mechanism of origin, prenatal entrainment
to photoperiod does not usually persist as chicks tend to reentrain to the ambient photoperiod during the first few days
after hatch in experimentally manipulated studies (Zeman
et al. 1999).
Finally, light exposure can cause changes in embryonic
metabolic rate (Preda et al. 1962). For example, the metabolic
rate of pigeon (Columba livia) embryos is greater in light than
dark (Prinzinger & Hinninger 1992). Heart rate also increases
in in vitro embryo hearts exposed to light (Gimeno, Roberts
& Webb 1967) and in in vivo embryos during daylight hours
(Moriya et al. 1999).
In summary, experimental work in domesticated species
reveals several key conclusions: (i) light accelerates embryonic
development, in part by increasing metabolic activity, (ii) the
extent of photoacceleration is affected by the photoperiod,
and (iii) the rate of photoacceleration varies with the stage of
embryo development, primarily due to differences in the
mechanism by which light affects development. Prior to
pineal gland formation, light affects specific developmental
pathways such as neural crest mitosis. After pineal gland formation, light acts primarily by modifying melatonin synthesis. Taken as a whole, extensive studies in domesticated
species reveal that variation in photoperiod can have critical
and important effects on the rate and route of development of
embryonic birds.
OBJECTIVES
We expect sensitivity to light to be an evolutionarily conserved trait, not one expressed only in domesticated lines of
birds. Indeed, given that selection for increasing developmental speed to maximize production of industrial goods has presumably been quite strong, it is possible that the magnitude of
the response could be greater in wild birds.
We tested for the positive effects of light on house sparrow
(Passer domesticus) development using two experiments: (i)
comparing direct measures of embryonic metabolic rates in
artificial incubators under sequential light and dark phases,
and (ii) comparing total development time of artificially incubated embryos raised under two different photocycles. We
hypothesized that embryo metabolism would be lower during
dark phases and higher during light phases, mimicking circadian rhythms in metabolic rate. We hypothesized that longer
daily exposure to light would result in shorter embryonic
development. We present results from the first photoacceleration experiment conducted on a wild bird species, the house
sparrow. Then we explore the possible implications of photoacceleration on trends in incubation periods (seasonal, latitudinal, between cavity, enclosed- and open-cup nesters) and
variation in egg coloration. We suggest that temperature and
light, received by embryos as a consequence of adult incubation rhythms and the abiotic environment, act as epigenetic
effects (Nichelmann, Hochel & Tzschentke 1999; Nichelmann
2004) that influence the rate of development and imprint a
pace of life on the developing bird.
Materials and methods
STUDY SPECIES
House sparrows, introduced from Europe to North America in the
1850s, are currently widely distributed across North America. North
American house sparrows lay 1–8 eggs per clutch (mode = 5 eggs),
rear as many as four broods per season, and initiate up to eight
attempts per season (Lowther & Cink 2006). Although only females
develop a brood patch, males assist in incubation. In the wild, the
incubation period ranges from 10 to 14 days, with an average of
11 days from last egg to first hatch (Lowther & Cink 2006). In artificial incubators, Wetherbee & Wetherbee (1961) reported their longest
incubation as 282 h (11Æ75 days).
EMBRYONIC METABOLIC RATE
We collected house sparrow eggs (n = 52 eggs from 13 clutches) from
natural nests found in nest boxes in Erie, PA on the day the 4th egg
was laid. We pre-warmed and calibrated both of our incubators
(36Æ09C ± 2Æ86 SD; still air Hovabator window models) prior to
inserting eggs. Incubators contained an automatic egg turner that
turned eggs 0Æ25 revolutions per hour and with an average relative
humidity of 73Æ3% ± 5Æ3%. Because the egg turner was designed for
larger eggs, we put a square of chemwipe under each egg before positioning it in the automatic turner to prevent them from slipping
through the egg cups. Light within the incubator was limited to the
output from a Zilla mini reptile UVB full spectrum compact fluorescent light (1155Æ09 ± 613Æ52 lx) set to an 18L : 6D photoperiod,
phase-shifted so light phase began at noon (EST). A 20cc syringe fitted with rubber stoppers and tubing was used to make a small respirometer chamber that fit inside the incubator. We pumped room air
through Ascarite filled CO2 scrubbers into ultra-low permeability
Tedlar gas bags in order to standardize ambient CO2 levels. We then
pumped the CO2-free air from the gas bag at 400 mL min)1 through
the respirometer chamber to Quibit gas analyzers (CO2 and O2). We
measured CO2 production for each egg under dark and light conditions within 4 h of each other and paired the observations for individual eggs. Metabolism measurements were made for each egg over
several days of incubation. We weighed and candled eggs daily to
check for adequate development. We excluded from the analysis any
eggs that failed to develop or died early in the incubation period. We
computed metabolic rate in lL CO2 min)1 egg)1 from CO2 measurement adjusted for flow rate.
EMBRYONIC DEVELOPMENT TIME
We gathered house sparrow eggs in Ithaca, NY to simultaneously test
the prediction that 12L : 12D photoperiods would lead to longer incubation periods than eggs incubated under 18L : 6D photoperiods. In
Ithaca, NY, we used a total of four Hovabator still air window incubators, two with egg turners for incubating eggs and two with screens on
the floor for hatching. We refer to the former as egg-rotating incubators and the latter as hatching incubators. The two egg-rotating incubators were kept at 37Æ22C ± 0Æ72 SD with average relative humidity
of 69Æ94% ± 5Æ60 SD and 37Æ23C ± 0Æ49 SD with average relative
humidity of 68Æ53% ± 12Æ65 SD. The two hatching incubators were
kept at slightly lower temperatures and higher relative humidity
(35Æ56C ± 0Æ23 SD with average relative humidity of 84Æ57% ±
2Æ74 SD and 36Æ39C ± 0Æ51 SD with average relative humidity of
81Æ56% ± 7Æ13 SD). Each incubator contained two windows, one of
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772 C. B. Cooper et al.
which we covered with electrical tape and one of which we fitted with a
light fixture containing a full-spectrum florescent light (Zilla mini
reptile UVB full spectrum compact fluorescent). We used electrical
tape to adhere the light to the window and to light-proof the edges.
The light produced 1203Æ59 ± 974Æ36 lx at egg height. Since we left
small holes open for air circulation, we surrounded each incubator
with black-out curtains to prevent ambient light from reaching the
eggs. Thus, eggs experienced light only from the light fixtures attached
to the windows. Desired humidity levels were reached by maintaining
a specific surface area of water in each incubator. For first broods, one
set of egg-rotation and hatching incubators were set at 12L : 12D, the
equatorial photoperiod, and one set of egg-rotation and hatching
incubators were set at 18L : 6D, a photoperiod common to temperate
latitudes during the breeding season. The temperature, humidity, and
air flow levels in incubators are difficult to control precisely. For this
reason, other studies (e.g. Lauber 1975) kept control and illuminated
eggs in the same incubators and applied light exposure via optical
fibres placed into a small hole in the eggshell. Instead, we repeated the
experiment with second broods after switching which incubators were
assigned as 18L : 6D and 12L : 12D treatments. Both treatments
began the light phase at 6:00 EST.
We monitored house sparrows nests in boxes several times a week
from late April through June 2009. We collected eggs between 9:00
and 11:00. We numbered each egg with a permanent marker, weighed
it to the nearest 0Æ01 g on portable electronic balance, and alternated
the assignment to 18L : 6D and 12L : 12D treatments for each egg
collected from different nests. We transported eggs between the field
and incubators in a compartmentalized sewing box filled with bird
seed, with each egg’s air sac facing up (Kuehler et al. 1993). We
weighed and candled eggs daily during incubation. Eggs were typically transferred to hatching incubators on day 9 when candling indicated normal growth and several days of consistent embryo
movement. After transfer to hatching incubators, eggs were rotated
and checked for signs of pipping twice daily. Seven of the 88 eggs
cracked during handling and were excluded from the experiment.
Fig. 1. Embryonic metabolic rate measured on 52 eggs collected from
nests of wild House Sparrows. (a) Least square mean estimate of
embryonic metabolic rate (lL CO2 min)1 egg)1) was higher during
light phases than dark phases (bars with 95% confidence intervals)
from measurements across embryo development. (b) The average difference in embryonic metabolic rate between light and dark phases
was always greater than zero.
Results
EMBRYONIC METABOLIC RATE
The variance around each treatment mean was approximately
equal and the distributions were normal. The mean metabolic
rate was 1Æ30 ± 0Æ57 lL CO2 min)1 egg)1 (mean ± 95%
C.I.) for the dark treatment and 1Æ92 ± 0Æ73 lL CO2 min)1
egg)1 for the light treatment. We used a general linear mixed
model with egg ID as a random effect to estimate the difference in light and dark phase metabolic rates (SAS version 9.1,
SAS 2002). The positive least square mean estimates of the
difference in light-to-dark phase metabolic rate indicated that
light phase metabolic rate was greater than dark phase metabolic rate throughout egg development (Fig. 1).
EXTRAPOLATING ADDITIVE EFFECTS
We used the average light and dark metabolic rates to estimate the difference in incubation period for 18L : 6D and
12L : 12D photoperiods. These photoperiods represent
approximate temperate and tropical daylengths, respectively.
With the temperate house sparrow incubation period of
11 days as a point of reference, we assumed that a typical
temperate day during the incubation period had 1080 light
minutes and 360 dark minutes. If total daily CO2 production
consists of 1080 min of light · 1Æ92 lL CO2 min)1 egg)1 and
360 min of dark · 1Æ30 CO2 lL)1 min)1 egg)1 then the metabolic rate to support daily development would be 2548 lL
CO2 day)1 egg)1; total metabolism for 11 days of development would produce 28024 lL CO2 egg)1. We also calculated the daily CO2 production under a tropical photoperiod
(720 min light · 1Æ92 lL CO2 min)1 egg)1 and 720 mins dark · 1Æ30 lL CO2 min)1 egg)1 = 2324 lL CO2 day)1 egg)1).
If we assume that 28024 lL CO2 egg)1 over 11 days is the
baseline metabolic rate required to produce a normal embryo
under the temperate photoperiod, then 12Æ10 days would be
necessary under the tropical photoperiod to reach the same
point. The difference in daylight hours should result in tropical incubation periods only 1Æ10 days longer, about 10%,
than those under temperate photoperiods.
EMBRYONIC DEVELOPMENT TIME
We considered alpha £0Æ05 to be statistically significant. We
included eggs for which the laydate accuracy was high, i.e. the
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Light and embryo metabolism 773
difference between the estimated minimum and maximum
laydate was zero (n = 23) or 1 (n = 13) or 2 (n = 11). Of
these 47 eggs, 24 were in the 18L : 6D treatment (n = 14 in
incubator 1, n = 10 in incubator 2) and 23 were in the
12L : 12D treatment (n = 10 in incubator 1, n = 13 in incubator 2). Thirteen eggs, distributed approximately equal
across treatments, failed to pip or hatch. Including all 47 eggs
in a general linear mixed (GLM; Proc Mixed in SAS) model of
treatment with nest origin as a random effect, indicated no
difference in the initial mass of eggs entering each treatment
(GLM, d.f. = 39, P = 0Æ67). Including the 34 eggs that survived to pip in a mixed model of treatment, incubator, and
their interaction, with nest origin as a random effect, eggs in
18L : 6D treatment had significantly (GLM, d.f. = 23,
P = 0Æ007) shorter incubation periods (12Æ7 days ±
0Æ26 SD) than eggs in the 12L : 12D treatment (13Æ7 days ±
0Æ26 SD; Fig. 2). Incubation periods also differed between
incubators, but the interaction between incubators and treatment was not significant (GLM, d.f. = 23, P = 0Æ73).
Results were similar after removing the potential outlier
(GLM, d.f. = 22, P = 0Æ03 with shorter incubation periods
(12Æ7 days ± 0Æ21) in 18L : 6D than in the 12L : 12D treatments (13Æ4 days ± 0Æ22), P = 0Æ04 for incubator effect, and
P = 0Æ8 for the treatment-incubator interaction). The results
confirm our prediction regarding photoacceleration: eggs
incubated under the longer photoperiod hatched about 1 day
earlier than eggs incubated under the shorter photoperiod.
Discussion and synthesis
The combined body of evidence, from research on precocial
domesticated birds and our experimental evidence on an altricial wild bird species, suggests that light can accelerate embryonic development within a species. Embryos raised in
Fig. 2. Incubation period (number of day from laydate to pipping)
measured on 34 eggs collected from nests of wild House Sparrows
(open circles) in two incubators under two photoperiod treatments,
with the least square mean estimates from a mixed model (black circles). The incubation period for eggs incubated under temperate
(18L : 6D) photoperiod was shorter than for eggs incubated under
tropical (12L : 12D) photoperiod, even with outlier (inc 1, tropical)
removed.
common garden conditions showed differences in metabolic
activity and development period based purely on differences
in light. The differences we report in incubation period in
house sparrows under 12L : 12D (tropical) vs. 18L : 6D
(temperate) photoperiods are consistent with the hypothesis
that photoacceleration may be an underlying mechanism contributing to latitudinal gradients in incubation periods. The
effective biological relevance of sunlight on embryonic development in the wild may depend on (i) the relative importance
of circadian rhythms compared to additive effects, (ii) interactions with other influential features of the embryonic environment, such as temperature, habitat, and parental behaviour
that influences how photoperiod translates into the amount
and quality of light received by embryos, and (iii) the importance of phylogenetic constraints and local adaptations. Temperature, in particular, likely plays an important role in
driving incubation period, as experimental work has revealed
the direct effect of temperature on development periods
(Martin et al. 2007; Ardia et al. 2009; Ardia, Perez & Clotfelter 2010), but differences in incubation periods are not
explained only by temperature (Robinson et al. 2008).
ADDITIVE OR CIRCADIAN
Light could have an additive effect, with more total light
resulting in incrementally more rapid development. This
effect would produce a latitudinal gradient in incubation periods where tropical species have incubation periods 1–2 days
longer, on average, than eggs exposed to long photoperiods
of temperate latitudes. Our results reveal an approximate
10% difference in incubation period produced from a 6-h
daily difference in light exposure to embryos of one species in
an experimental environment. Phylogenetically controlled
comparisons of incubation periods between temperate and
tropical species exhibiting approximately 2-h day)1 differences in daylength show greater differences in incubation period, ranging from 30% to 50% (Martin et al. 2007; Martin &
Schwabl 2008). The 10% difference we measured indicates
that light, via photoacceleration, could explain a portion of
the variation in incubation period across latitudes. Our values
are more comparable to seasonal declines in incubation period, reported to be about 1 day between spring and summer
for Eastern Bluebirds (Cooper et al. 2005). Additional studies
that combine measurements of incubation period across latitudes with experimental manipulation of light exposure to
eggs collected across latitudes will be needed to assess the relative contribution of photoacceleration compared with other
contributing factors.
Although our results only permit us to infer summative
effects of light, the potential importance of the circadian
aspects of photocycles is also ecologically relevant because
physiological processes can be influenced by pulses of light.
After development of the pineal gland, pulses of light during
adult recesses may register as complete photoperiods to
embryos. It is widely established that brief periods of light to
signal the beginning of the day and another to signal the
end of the day, called skeleton photoperiods or intermittent
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774 C. B. Cooper et al.
lighting, can be interpreted by birds as a ‘subjective day’
(Bacon 1984; Rowland 1985) and entrain physiological processes (Slaugh et al. 1988). It is conceivable that the incubation patterns of birds could create a skeleton photoperiod by
exposing eggs to brief pulses of light, essentially defining a
subjective day. These could then entrain metabolic cycles that
are higher during the ‘light’ phase than the ‘dark’ phase. Most
evidence suggests that activity periods of wild birds are tightly
linked to the local photoperiod (Daan & Aschoff 1975).
Therefore, dawn and dusk pulses of light during adult
recesses may be enough to synchronize embryonic biological
rhythms to the local photoperiod. In adults, experimental
exposure to skeleton photoperiods can entrain daily rhythms
in metabolism (Wikelski et al. 2008) and while to the best of
our knowledge this has not been directly tested in embryos,
light pulses during daylight hours may be sufficient to entrain
metabolic rhythms (Styrsky, Berthold & Robinson 2004).
INTERACTIONS WITH OTHER FEATURES
Under natural incubation conditions, eggs are contact-incubated by adults and therefore experience conditions greatly
different from conditions in experimental incubators. Specifically, in the wild, eggs are unlikely to receive heat generated
by contact incubation at the same time as receiving light,
though there may be situations where ambient conditions
provide equivalent heat or in which light reaches eggs through
the sides of nests while an adult is incubating. Most eggs experience their longest exposures to sunlight during the laying
period (females typically lay one egg per day), when eggs
receive little parental attendance. Presumably, light cannot
enhance development outside the embryonic thermoneutral
zone, although we are not aware of studies that examine this
possibility. A possible scenario may be that light stimulates
protein production (Shafey 2004; Halevy et al. 2006), and
when heat resumes more proteins are then available as molecular switches to turn on metabolic pathways. Furthermore,
some species may initiate incubation before all eggs in a clutch
are laid when adults sleep on nests at night (Rompré & Robinson 2008). This transfer of heat at night, while leaving eggs
mostly unattended during the day, may launch developmental processes in the embryo and also allow embryos to entrain
to photoperiod during the first days prior to full onset of diurnal incubation.
Inferring the ecological significance of lab-based photoacceleration is complicated by many other factors. Many eggs
are in nests located in areas of low light intensities, such as
forests or in cavities. In full sunlight, light intensity is over
10 000 lx, cloudy days about 1000 lx, nest boxes can range
from 5 to over 500 lx, and natural cavities may receive even
less light. Interestingly, cavity nesting species have longer
incubation periods than open nesting species (Martin 1995).
Yet, in some ways, extrapolating photacceleration results
from domesticated to wild birds is highly conservative
because eggshell density, which is much lower in wild birds,
plays a role in the amount of light that reaches the blastodisc
(Shafey 2004). There is some evidence that passerine eggs
could be affected by even lower light intensities than reported
for domesticated birds (Rahn & Paganelie 1989). The condition of reduced eggshell density allowing increasing light to
penetrate shells and the potential for increased sensitivity to
light may allow (or have been selected to) link the physiological mechanisms underlying photoacceleration with pulsed
and reduced light cues. Furthermore, egg colour could influence the extent to which photoacceleration is important in
natural settings. The thickness of eggshell and degree of pigmentation may preferentially filter some wavelengths of light
(Romanoff & Romanoff 1949), reducing the efficiency of the
photoacceleration mechanism. A recent poultry study (Shafey et al. 2004) showed that eggshells are particularly efficient
at blocking UV wavelengths, and that the brown eggs of one
breed are more effective than the white eggs of another breed
in blocking light transmittance across the spectrum. The eggs
used in our experiment varied in colour from white to blue to
grey, but we did not quantify the degree of pigmentation or
opacity of each egg. Future research is needed to examine the
role of photoacceleration in explaining the longer incubation
periods of cavity nesting birds relative to open nesting birds,
and the potential to account for variation in egg pigmentation.
PHYLOGENETIC CONSTRAINTS AND LOCAL
ADAPTATIONS
Some species may show no differences in incubation period
across a broad geographic range, suggesting a lack of
response to light and other environmental features. For
example, the incubation period of white-crowned sparrow
subspecies (Zonotrichia sp.) appears phylogenetically constrained as it does not vary among subspecies, with altitude,
nor with latitude (Morton 1976; King & Hubbard 1981; Carey et al. 1982). Nevertheless, the incubation period of whitecrowned sparrows does decrease between spring and summer
(Mead & Morton 1985). Because photoacceleration is a proximate mechanism contributing to the rate of development,
selection pressures may result in adaptations that enhance or
diminish photoacceleration. For example, the degree of eggshell pigmentation has been shown to mediate the amount of
light reaching the blastodisc during early avian development
(Shafey et al. 2004). Ghatpande, Ghatpande & Khan (1995)
demonstrated that the amount of light reaching the embryo
determines the extent to which photoacceleration enhances
development. Species with heavily pigmented eggshells, such
as the white-crowned sparrow, may therefore not experience
photoacceleration to the extent of other species.
Pigmented eggshells represent one example of adaptations
that may augment photoacceleration. A variety of adaptations, such as reduced shell pigmentation, increasingly
exposed nesting sites, or possibly variation in key isozymes
responsible for energy metabolism, may play a role in the
greater differences in natural incubation period between temperate and tropical species, even when differences in photoperiod length are shorter than those in our experiment. For
example, Schaefer et al. (2004) measured 35–40% longer
2011 The Authors. Functional Ecology 2011 British Ecological Society, Functional Ecology, 25, 769–776
Light and embryo metabolism 775
incubation periods in Sylvia species in tropical Africa (14Æ5–
15 days) compared with many temperate-zone Sylvia species
in Europe (10–12 days, averaging around 11 days). Since our
study only included house sparrows living in temperate
regions (presumably with many local adaptations to temperate conditions), we cannot make greater inferences about
how the embryonic development of house sparrows residing
in the tropics may or may not respond to light.
Although we provide experimental evidence for photoaccelerated development in a Passerine species, the broader
influence of light exposure on avian development and metabolism still requires additional investigation. Our synthetic
review, coupled with limited experimental evidence from a
wild species, suggest some major latitudinal differences in lifehistory traits could be explained, in part, by variation in basic
environmental features such as latitudinal differences in
quantity and quality of light.
Acknowledgements
We received support from the U. S. National Science Foundation IRCEB
(grant 0212587 to WDR).
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Received 13 July 2010; accepted 7 February 2011
Handling Editor: Alistair Dawson
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