You are on page 1of 11

See

discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/8176998

Maternal exposure to first-trimester


sunshine is associated with increased birth
weight in human infants
Article in Developmental Psychobiology December 2004
Impact Factor: 3.31 DOI: 10.1002/dev.20030 Source: PubMed

CITATIONS

READS

31

68

3 authors:
Karen Tustin

Julien Gross

University of Otago

University of Otago

8 PUBLICATIONS 98 CITATIONS

28 PUBLICATIONS 681 CITATIONS

SEE PROFILE

SEE PROFILE

Harlene Hayne
University of Otago
148 PUBLICATIONS 4,439 CITATIONS
SEE PROFILE

All in-text references underlined in blue are linked to publications on ResearchGate,


letting you access and read them immediately.

Available from: Julien Gross


Retrieved on: 01 May 2016

Karen Tustin
Julien Gross
Harlene Hayne
Psychology Department
University of Otago
Dunedin, New Zealand
E-mail: tuska194@student.otago.ac.nz
E-mail: jules@psy.otago.ac.nz
E-mail: hayne@psy.otago.ac.nz

Maternal Exposure to
First-Trimester Sunshine is
Associated with Increased Birth
Weight in Human Infants
ABSTRACT: Two alternative hypotheses have been generated to account for
seasonal variation in the birth weight of human infants born in industrialized
countries. First, it has been hypothesized that low ambient temperature during the
second trimester of gestation decreases birth weight. Second, it has been
hypothesized that exposure to bright sunshine during the first trimester increases
birth weight. We tested these two hypotheses to determine which, if either, accounted
for seasonal variation in birth weight of full-term infants. Birth weight data,
collected over a 5-year period, were analyzed as a function of peak and trough
sunshine and ambient temperature. Although there was no effect of ambient
temperature during any trimester on birth weight, infants whose mothers were
exposed to peak sunshine during their first trimester were born significantly heavier
than infants whose mothers experienced trough levels of sunshine during the same
trimester. Furthermore, infants whose mothers were exposed to trough levels of
sunshine during their second and third trimesters were born significantly heavier
than infants whose mothers were exposed to peak levels of sunshine during the same
trimesters. We hypothesize that high levels of sunshine during early gestation may
increase the level of insulin-like growth factor (IGF)-1, facilitating prenatal growth.
2004 Wiley Periodicals, Inc. Dev Psychobiol 45: 221230, 2004.
Keywords: birth weight; sunshine; ambient temperature; gestation; insulin-like
growth factor; fetal growth

A large number of studies have shown that a persons


season of birth may influence his or her susceptibility to a
wide range of psychological disorders, including schizophrenia (de Messias, Cordeiro, Sampaio, Bartko, &
Kirkpatrick, 2001; Narita et al., 2000; Parker, Mahendran,
Koh, & Machin, 2000; Tatsumi et al., 2002), eating disorders (Eagles, Andrew, Johnston, Easton, & Millar,
2001; van Hanswick de Jonge & Waller, 2002; Watkins,

Received 26 February 2004; Accepted 19 July 2004


Correspondence to: H. Hayne
Contract grant sponsor: University of Otago
Contract grant number: ORG200200520
Published online in Wiley InterScience
(www.interscience.wiley.com). DOI 10.1002/dev.20030
2004 Wiley Periodicals, Inc.

Willoughby, Waller, Serpell, & Lask, 2002), and substance


abuse (Goldberg & Newlin, 2000). In contrast, other studies
have failed to find a relation between season of birth and
mental health outcome (Davies, Ahmad, Chant, Welham,
& McGrath, 2000; Kovalenko et al., 2000; Kunugi,
Nanko, Watanabe, Sekiba, & Kazamatsuri, 1998; Morgan,
Jablensky, & Castle, 2001). Because of the amount of time
that passes between birth and the outcome under study, the
lack of consistency in this area of research is not surprising.
In adult-onset disorders, there is ample opportunity for
other influences, such as experience or upbringing, to mask
or amplify the effects of season of birth, per se. Given this,
there has been renewed interest in examining season-ofbirth effects that might emerge early in life.
At least two studies have shown that the achievement of
major motor milestones during the infancy period varies
as a function of season of birth (Benson, 1993; Hayashi,

222

Tustin, Gross, and Hayne

1990). In both studies, infants born during the colder


months of the year (spring and winter) began to crawl
slightly earlier than those born during the warmer months
(summer and autumn). To explain these results, Benson
(1993) and Hayashi (1992) proposed that heavy clothing
during winter when infants were learning to crawl may
have impeded the movement of infants born during the
summer months. Although this explanation is consistent
with the crawling data, subsequent research by Benson
(1996) showed that infants who are born in spring or
winter not only begin to crawl earlier than those born in
summer or autumn but they also begin to walk earlier. This
finding was obtained despite the fact that these infants are
learning to walk in the colder weather when heavy layers
of restrictive clothing should presumably hinder them.
Given this, the mechanism responsible for the season-ofbirth effect on motor development is not known.
A large body of research also has shown that birth
weight varies as a function of season of birth. In nonindustrialized countries, for example, season-of-birth
effects are typically large, ranging from 30 to 196 g.
Despite the magnitude of this seasonal effect, there is no
consistent relation between birth weight and a particular
season of birth. For instance, in countries with a latitude
between 0 and 10 south, the highest birth weights are
recorded during the dry season and the lowest during
the rainy season (Bantje, 1987; Fallis & Hilditch, 1989;
Greenfield, 1983). At 30 south, the highest birth weights
occur in spring and summer and are the lowest in autumn
and winter (Henneberg & Louw, 1993). In countries from
10 to 25 north, the highest weights occur during winter or
autumn (Adair & Pollitt, 1983; Huizinga & Wijngaard,
1981) whereas in countries between 25 and 30 north, the
highest birth weights are in summer (Hort, 1987; Lakshmi
& Bandyopadhyay, 1987).
Although the relation between birth weight and a
particular season of birth in nonindustrialized countries
appears to be unique to the geographical region, the same
mechanisms can be used to account for all of the findings.
In particular, the nutritional status and energy expenditure
of the mother during pregnancy are the main factors
involved in determining whether an infant will be of a
comparatively high or low weight (Adair & Pollitt, 1983;
Bantje, 1987; Fallis & Hilditch, 1989; Greenfield, 1983;
Henneberg & Louw, 1993; Hort, 1987; Huizinga &
Wijngaard, 1981; Lakshmi & Bandyopadhyay, 1987).
Any given season can bring with it differing agricultural
demands that require heavy labor and result in low food
availability. Low food intake combined with intensive
manual work by an expectant mother results in high
energy expenditure, leaving fewer resources for the developing fetus, thus possibly resulting in a lower birth
weight. Other factors such as the prevalence of disease and
infection that are coincident with certain seasons (e.g.,

malaria or gastrointestinal illnesses) also may play a role


in determining final birth weight in these nonindustrialized countries (Adair & Pollitt, 1983; Bantje, 1987; Fallis
& Hilditch, 1989).
In industrialized countries, on the other hand, heavy
labor and seasonal food shortages have largely been
eliminated with the introduction of the supermarket.
Although the quantity and quality of food continues to
vary as a function of socioeconomic status, seasonal
variation has been largely eliminated. Despite this, seasonal effects in birth weight continue to occur. Although
the magnitude of the difference is smaller (e.g., <30 g) in
industrialized relative to nonindustrialized countries, the
fact that a difference occurs at all suggests that mechanisms other than maternal energy intake and expenditure
play a role in seasonal variation in infant birth weight.
As with nonindustrialized countries, there is no
consistent pattern between the exact season of birth and
birth weight in industrialized countries. For example, in
some countries, such as New Zealand (40 south), Austria
(47 north), and Denmark (56 north), the highest birth
weights occur in spring (Bodnarchuk & Eaton, 2002;
Waldie, Poulton, Kirk, & Silva, 2000; Weber, Prossinger,
& Seidler, 1998; Wohlfahrt, Melbye, Christens, Andersen,
& Hjalgrim, 1998). In contrast, in countries such as
Ireland (55 north), the highest birth weights occur in
winter (Murray et al., 2000).
In general, there are two competing hypotheses that
have been offered to explain seasonal variations in the
birth weight of infants born in industrialized countries.
First, temperature may play a crucial role in determining
seasonal variation in birth weight. Murray et al. (2000)
argued that colder temperatures during the second
trimester of gestation result in lower birth weights by
reducing uteroplacental blood flow, which restricts fetal
growth. In support of this hypothesis, Murray et al. found
that seasonal effects on birth weight disappeared in their
sample after statistical adjustment for ambient temperature during the second trimester of gestation.
Second, maternal exposure to bright sunshine also may
play a crucial role in determining seasonal variation in
birth weight (Bodnarchuk & Eaton, 2002; Waldie et al.,
2000; Weber et al., 1998). For example, Waldie et al.
(2000) found that maternal exposure to increased
sunshine during the first trimester of gestation was coincident with increased weight (and length) at birth as well as
increased height at age 18 years. These authors argued that
maternal exposure to comparatively large amounts of
sunshine during early pregnancy increases birth weight,
possibly by altering prenatal growth hormone production.
Thus, infants whose mothers are exposed to many hours
of bright sunshine during the first trimester of gestation
may be heavier at birth than those whose mothers are not
exposed.

Season of Birth

In the present study, we pitted these two hypotheses


against each other in an attempt to determine which hypothesis best explains seasonal variation in birth weight.
Our first step was to clarify the definition of season. In
prior studies, researchers have defined seasons in an
inconsistent fashion. In some studies, terms such as rainy
season or dry season have been used to describe the
climate in a specific region. In other studies, more traditional terms such as spring, summer, autumn, and winter
have been used to describe a particular season; the
calendar months that make up a particular season often
vary across studies and may or may not reflect actual
meteorological changes. In the present study, season was
defined according to hours of bright sunshine and mean
ambient temperature.
We examined the effects of maternal exposure to bright
sunshine and ambient temperature during gestation on the
birth weight of infants born in Dunedin, New Zealand
(latitude 46 south). There are at least two factors that
make Dunedin an ideal location to study seasonal variation in birth weight. First, New Zealand experiences a high
percentage of bright sunshine during daylight hours
(Gentilli, 1971), and there is extreme seasonal variation
in the amount of daylight between summer and winter. At
latitudes around 40 south (where New Zealand lies), the
peak day length in summer (December, 15.02 hr) is
approximately 5.68 hr longer than the peak day length in
winter (June) (Gentilli, 1971). At lesser latitudes, such as
10 south (e.g., where Peru and Brazil lie), this difference
in day length is only 1.15 hr. Second, although the
average ambient temperature during winter is not cold by
some standards, houses in New Zealand are among the
most poorly heated in industrialized countries (personal
communication, B. Lloyd, Energy Management Group,
Department of Physics, University of Otago, February 2,
2004). The World Health Organization recommends a
minimum indoor temperature of 16 C, but the average
winter indoor temperature in Dunedin is 12 to 14 C; when
it is cold outside, it is cold inside. The large seasonal
variation in mortality in Dunedin provides further evidence for the combined impact of cold weather and poor
heating. These conditions make Dunedin an ideal place to
study seasonal effects of temperature on birth weight.

EXPERIMENT 1
In Experiment 1, we determined whether ambient temperature during the second trimester of gestation (temperature hypothesis) or sunshine during the first trimester
(sunshine hypothesis) provided the best explanation for
seasonal variation in birth weight. First, the birth weights
of infants whose second trimester of gestation corresponded to the peak or trough in annual ambient tem-

223

perature were compared (temperature hypothesis).


Second, the birth weights of infants whose first trimester
corresponded to the peak or trough in ambient sunshine
also were compared (sunshine hypothesis).

Method
Information regarding 8,516 infants born between
January 1999 and December 2003 at the Queen Mary
Maternity Unit at Dunedin Public Hospital or at home in
Dunedin, New Zealand was obtained via public birth
records. The information included date of birth, sex, birth
weight (g), and gestational age (weeks). Overall, 1,477
births (17.34%) were premature, and 4,468 infants
(52.47%) were male. Information for infants who had
died since the time of birth also was included.
The analyses reported here were restricted to full-term
infants (gestation  38 weeks). The original dataset included 7,039 infants who were born full-term. The
average length of gestation for these infants was 39.65
(.013) weeks, and the average birth weight was 3,542.97
(5.719) g across all 5 years of birth weight data. For each
infant, the primary variables of interest were birth weight
and gestational age.
Mean daily readings for temperature ( C) and bright
sunshine (hours) between 1999 and 2002 were obtained
from the National Institute of Water and Atmospheric
Research (NIWA). These data were averaged to obtain a
mean value for each month of the 4 years of interest
(19992002) (see Figure 1). For each of the 4 years of
meteorological data, mean daily values for the sunshine
and the temperature data were averaged over each possible combination of 3 consecutive months. In this way, we
were able to identify peak and trough sunshine and
temperature periods for each year.
Each peak and trough in sunshine corresponded to the
first trimester for infants born 40 weeks later; each peak
and trough in temperature corresponded to the second
trimester of infants born 28 weeks later. Specifically, the
first month for each peak and trough was used as the
starting point from which to calculate the month of birth of
infants whose first or second trimester of gestation corresponded to the peak or trough in sunshine and temperature,
respectively. Therefore, only data from infants whose first
(n 903) or second trimester (n 955) corresponded to
the peaks and troughs in bright sunshine and temperature
were used in subsequent analyses.

Results and Discussion


The two dependent measures (gestational age and birth
weight) were averaged across infants to obtain a mean
value as a function of peaks and troughs in sunshine or
ambient temperature. These data are presented in Figure 2.

224

Tustin, Gross, and Hayne

FIGURE 1

Mean daily temperatures ( C) and hours of bright sunshine between 1999 and 2002.

The data were subjected to separate one-way analyses of


variance (ANOVAs). As shown in Figure 2a, average
gestational age did not differ as a function of sunshine,
F(1, 901) .03, p > .05, or as a function of ambient
temperature, F(1, 953) .18, p > .05. Thus, any subsequent differences are not due to seasonal variation in
gestational age.
Average birth weight was significantly higher when
mothers were exposed to peak, as opposed to trough,
periods of sunshine during their first trimester of gestation, F(1, 901) 4.61, p < .05. In contrast, average birth
weight did not differ as a function of ambient temperature,
F(1, 953) .31, p > .05 (see Figure 2b).
Recall that two competing hypotheses have been
offered to explain seasonal variation in birth weight of
infants born in industrialized countries. On one hand, it

has been hypothesized that maternal exposure to periods


of low ambient temperature during the second trimester of
gestation may reduce birth weight. On the other hand, it
has been hypothesized that maternal exposure to periods
of high ambient sunshine during the first trimester of
gestation may increase birth weight.
The results of Experiment 1 provide no support for the
temperature hypothesis. The birth weight of infants whose
mothers experienced periods of low ambient temperature
during their second trimester of gestation did not differ
from that of infants whose mothers experienced periods of
high ambient temperature during their second trimester. In
contrast, the results of Experiment 1 provide substantial
support for the sunshine hypothesis. Infants whose
mothers experienced high levels of sunshine during their
first trimester of gestation were born significantly heavier

FIGURE 2 Gestational age and birth weight as a function of peak and trough sunshine exposure
during the first trimester of gestation and peak and trough temperature periods during the second
trimester of gestation: (a) average gestational age (weeks) (1 SE) and (b) average birth weight (g)
(1 SE).

Season of Birth

than infants whose mothers experienced low levels of


sunshine during their first trimester.
Although seasonal differences in birth weight in
industrialized countries tend to be small, the magnitude
of the difference in birth weight in the present experiment
is akin to that found in nonindustrialized countries (i.e.,
67.9 g). There are two possible explanations for the size of
the effect that we observed. First, unlike prior research of
this kind, our definition of season was based on actual
meteorological measures (i.e., hours of bright sunshine
and temperature) rather than on calendar months.
Although calendar months and meteorological data may
be correlated, the correlation is not perfect. For example,
in the present experiment, the trough in sunshine level for
each year consistently occurred from May to July (late
autumn to winter), but the peaks varied from year to year,
occurring from January to March (midsummer to early
autumn) or from October to December (midspring to early
summer). Annual peaks and troughs in temperature were
more consistent across years, yet they still did not occur
during one season alone. In fact, when we reanalyzed the
present data across all 7,039 full-term infants according to
the traditional seasonssummer (DecemberFebruary),
autumn (MarchMay), winter (JuneAugust), and spring
(SeptemberNovember)there were no seasonal
differences in birth weight at all, F(3, 7035) 2.0,
p > .05. Thus, the large difference in birth weight that
we observed is almost certainly a product of the specificity
of the measures that were employed to define season.
Second, it also is possible that the magnitude of the
effect that we observed was due to the large seasonal
difference in sunshine level in this part of the world.
Dunedin, New Zealand, is relatively far from the equator
(46 south), and seasonal differences in sunshine here are
substantial. Given this, mothers of infants whose first
trimester corresponded to a peak period of sunshine were
exposed to, on average, 2.7 more hr of bright sunshine
each day than were mothers of infants whose first
trimester corresponded to a trough period of sunshine.
By comparison, mothers of infants gestated at the equator
would experience virtually no seasonal variability in
sunshine, and mothers of infants gestated in the middle of
the United States (e.g., Denver, CO, 39 north) would
experience a 17-min difference between peak and trough
sunshine (Bryson & Hare, 1974). On the basis of the
present findings, we suggest that maternal exposure to
large amounts of bright sunshine during the first trimester
of gestation is associated with heavier birth weight.

EXPERIMENT 2
The design of Experiment 1 was based on two competing
hypotheses regarding the effects of ambient temperature

225

and sunshine on infant birth weight. The specific trimesters that were included in the analyses were selected
on the basis of those hypotheses. But what about the effect
of temperature and sunshine during other trimesters of
gestation? We addressed this question in Experiment 2. To
do this, we investigated the effect of maternal exposure to
sunshine and temperature during the trimesters that were
not included in Experiment 1.

Method
Information regarding the same 7,039 full-term infants
from Experiment 1 was reanalyzed in Experiment 2. As in
Experiment 1, the first month for each peak and trough
was used as the starting point from which to calculate the
month of birth of infants whose first, second, or third
trimester of gestation corresponded to the peak or trough
in sunshine and temperature. Infants whose first trimester
corresponded to a peak or a trough in climate data were
born 40 weeks later, infants whose second trimester
corresponded to a peak or a trough were born 28 weeks
later, and infants whose third trimester corresponded to a
peak or a trough were born 16 weeks later. Average values
of peaks and troughs in temperature and sunshine for each
year are presented in Table 1, along with the month of birth
for infants born during each trimester and the number of
infants born during each month.

Results and Discussion


Temperature. In Experiment 1, we examined the effect of
peak and trough temperature during Trimester 2 on
gestational age and birth weight. The mean values for
gestational age and birth weight as a function of peaks and
troughs in ambient temperature for the remaining trimesters (1 and 3) are shown in Table 2. These data were
subjected to a two-way ANOVA. As shown in Table 2,
there was no main effect of trimester, no main effect of
temperature (peak vs. trough), and no interaction for
either gestational age or birth weight, largest F 1.20,
p > .05. That is, birth weight did not differ as a function of
maternal exposure to peak or trough temperatures during
Trimester 1, 2 (Experiment 1), or 3. As such, variation in
ambient temperature can be ruled out as a mechanism to
account for seasonal differences in birth weight, at least in
New Zealand.
Sunshine. In Experiment 1, we examined the effect of
peak and trough sunshine during Trimester 1 on gestational age and birth weight. The mean values for
gestational age and birth weight as a function of peaks
and troughs in sunshine for the remaining trimesters (2
and 3) are shown in Table 3. These data were subjected to a
two-way ANOVA. For gestational age, there was no main

226
Table 1.

Tustin, Gross, and Hayne


The Peak and Trough Periods of Sunshine and Ambient Temperature and the Corresponding Distribution of Births
Sunshine
Month of Birth for Each Trimester

Year

Peak/Trough

Period

Daily Sun (hr)

Trimester 1

Trimester 2

Trimester 3

1999

Peak
Trough
Peak
Trough
Peak
Trough
Peak
Trough

JanMar
MayJul
OctDec
MayJul
JanMar
MayJul
OctDec
MayJul

6.69
3.53
6.56
3.24
5.89
3.72
5.67
3.5

Oct-99
Feb-00
Jul-01
Feb-01
Oct-01
Feb-02
Jul-03
Feb-03

129
114
97
111
117
91
140
104

Jul-99
Nov-99
Apr-01
Nov-00
Jul-01
Nov-01
Apr-03
Nov-02

114
120
105
115
97
137
113
118

Apr-99
Aug-99
Jan-01
Aug-00
Apr-01
Aug-01
Jan-03
Aug-02

111
148
107
156
105
123
97
109

2000
2001
2002

Temperature
Month of Birth for Each Trimester


Year

Peak/Trough

Period

Daily Temp ( C)

Trimester 1

Trimester 2

Trimester 3

1999

Peak
Trough
Peak
Trough
Peak
Trough
Peak
Trough

JanMar
JunAug
JanMar
JunAug
JanMar
MayJul
JanMar
JunAug

15.92
7.88
14.01
7.47
13.47
7.54
13.99
7.87

Oct-99
Mar-00
Oct-00
Mar-01
Oct-01
Feb-02
Oct-02
Mar-03

129
130
118
126
117
91
129
131

Jul-99
Dec-99
Jul-00
Dec-00
Jul-01
Nov-01
Jul-02
Dec-02

114
122
138
138
97
137
115
94

Apr-99
Sep-99
Apr-00
Sep-00
Apr-01
Aug-01
Apr-02
Sep-02

111
112
121
133
105
123
100
129

2000
2001
2002

effect of trimester, no main effect of sunshine (peak vs.


trough), and no interaction, largest F 1.53, p > .05. For
birth weight, on the other hand, there was a main effect of
sunshine (peak vs. trough), F(1, 1871) 7.89, p < .01.
Infants whose mothers were exposed to trough periods of
sunshine during their second and third trimesters were
heavier than infants whose mothers who were exposed to
peak periods of sunshine during the same trimesters.
There was no main effect of trimester and no interaction,
largest F .12, p > .05.

GENERAL DISCUSSION
In summary, birth weight did not differ as a function of
ambient temperature during any trimester of gestation.

Conversely, birth weight did differ as a function of ambient


sunshine during all three trimesters of gestation. Infants
whose mothers were exposed to peak sunshine periods
during the first trimester of gestation were heavier at birth
than infants whose mothers experienced trough sunshine
periods during the same trimester (Experiment 1), and
increased birth weight was associated with maternal
exposure to trough sunshine periods during the second
and third trimesters of gestation (Experiment 2).
In addition to genetics, at least two other factors
contribute to individual differences in birth weight: Duration
of gestation and fetal growth (Smith et al., 2002). The present
experiment was based on all infants who were born in
Dunedin during a 5-year period. Thus, we can assume that
genetic differences in birth weight were randomly distributed throughout the year. In addition, gestational age did not

Table 2. Average Birth Weight (g) and Gestational Age (Weeks) for Peak
and Trough Temperature Exposure during the First and Third Trimesters of Gestation
Trimester
Trimester 1
Trimester 3

Peak/Trough

Gestational Age (Weeks)

Birth Weight (g)

Peak
Trough
Peak
Trough

39.69 (.048)a
39.61 (.047)a
39.59 (.051)a
39.70 (.049)a

3,553.68 (23.13)a
3,565.59 (21.65)a
3,518.53 (23.14)a
3,552.20 (20.73)a

Note. Data for the second trimester are shown in Figure 2.


a
There was no effect of trimester or temperature (peak/trough) on either gestational age or birth weight.

Season of Birth

227

Table 3. Average Birth Weight (g) and Gestational Age (Weeks) for Peak and Trough Sunshine
Exposure during the Second and Third Trimesters of Gestation
Trimester
Trimester 2
Trimester 3

Peak/Trough

Gestational Age (Weeks)

Peak
Trough
Peak
Trough

39.59 (.050)
39.63 (.047)a
39.64 (.051)a
39.70 (.046)a

Birth Weight (g)


3496.01 (21.27)b
3561.49 (21.39)c
3508.03 (22.16)b
3564.33 (21.22)c

Note. Data for the first trimester are shown in Figure 2.


a
There was no effect of trimester or sunshine (peak/trough) on gestational age.
b,c
There was a main effect of sunshine (peak/trough) on birth weight, but no effect of trimester.

differ as a function of sunshine level during any trimester.


Therefore, the differences in birth weight reported here must
be due to factors that influence growth, per se.
What biological mechanism could explain the effect of
sunshine level on prenatal growth? Sunshine level had a
different effect on birth weight depending upon the
trimester of gestation. First, we will consider the effect of
peak sunshine during the first trimester.
How might exposure to bright sunshine during the first
trimester of gestation influence fetal growth? Waldie et al.
(2000) hypothesized that high levels of sunshine during
early gestation might increase birth weight by altering
hormone levels that are involved in growth. It has been
argued, for example, that increased exposure to sunshine
during the first trimester of gestation may inhibit maternal
melatonin production and stimulate the release of growth
hormone (GH). Although high levels of melatonin are
typically associated with high levels of GH (Laartz,
Losee-Olson, Ge, & Turek, 1994; Zeman, Buyse,
Lamosova, Herichova, & Decuypere, 1999), there is
some evidence in both deer (Webster, Corson, Littlejohn,
Stuart, & Suttie, 1998) and humans (Bellastella et al.,
1994) for an inverse relation between melatonin and GH
production. From this perspective, greater exposure to
light during the first trimester of gestation may increase
GH levels by inhibiting melatonin production.
Although an explanation based on melatonin and GH is
consistent with prior studies of postnatal growth, it may be
insufficient to explain the effect of bright sunshine on
prenatal growth reported here. For example, GH receptors
are structurally and functionally immature prior to
approximately 36 weeks of gestation; even after this point,
GH has only a limited influence on fetal growth (Gluckman
& Pinal, 2003). Experimental removal of the pituitary gland
which synthesizes GH, for example, has no effect on
prenatal growth (Baker, Liu, Robertson, & Efstratiadis,
1993). This finding provides further support for the
conclusion that GH may play little or no role in our effect.
If melatonin and GH are not responsible for the relation
between first trimester sunshine and prenatal growth, what
other hormones might play a role? At least three lines of
research have shown that insulin-like growth factor (IGF)-

1 is involved in fetal growth (Gluckman & Pinal, 2003).


First, in many species (including humans), birth weight
and placental weight are positively correlated with fetal
IGF-1 levels in umbilical cord blood (Gluckman, 1995;
Gluckman, Morel, Ambler, Breier, & McCutcheon, 1992;
Gluckman & Pinal, 2002; Han & Carter, 2001). There also
is greater risk of low birth weight if placental IGF-1 levels
are very low during early pregnancy (Smith et al., 2002).
Second, growth deficiency occurs in fetal mice with a
mutation in the gene that codes for IGF-1 and its receptors
(Baker et al., 1993; Liu, Baker, Perkins, Robertson, &
Efstratiadis, 1993). Third, both endogenous and exogenous IGF-1 has been shown to abolish or reduce the effect
of maternal uterine restrictions (e.g., space, nutrient
availability) on fetal growth (Gluckman et al., 1992;
Gluckman & Pinal, 2002; Kennaway et al., 2001).
In addition, IGF-1 also may mediate nutritional
influences on fetal growth. The supply of nutrients available to the fetus following conception shapes placental
and embryonic development, and it has recently been
suggested that IGF-1 regulates the development of the
placenta by controlling how nutrients are distributed
between the fetus and the placenta (Gluckman, 1995;
Gluckman & Pinal, 2002). Greater levels of IGF-1 are
thought to partition nutrients in favor of the fetus
(Gluckman, 1995; Gluckman & Pinal, 2002). For example, infusions of IGF-1 to normal fetal lambs increase
amino acid uptake by the fetus (Gluckman et al., 1992).
Moreover, IGF-1 increases mRNAs for the GLUT1
(maternalplacental glucose transport) and GLUT3
(fetalplacental glucose transport) glucose transporters.
Therefore, increased levels of IGF-1 may mediate glucose
(nutrient) exchange in favor of the fetus (Gluckman &
Pinal, 2002).
Taken together, the data described earlier provide
substantial evidence for the role of IGF-1 in prenatal
growth. Relevant to the present study, there also is
evidence that IGF-1 levels vary with exposure to light. For
example, Webster et al. (1998) showed that male red deer
exposed to a simulated short-day cycle exhibited an earlier
cessation of growth that was accompanied by a decrease in
both IGF-1 and GH levels relative to animals that were

228

Tustin, Gross, and Hayne

exposed to a long-day period. That is, animals exposed to


more light had greater levels of IGF-1 and GH, and were
heavier than animals exposed to less light. Similarly,
reindeer calves maintained on a long-day cycle exhibited
higher IGF-1 levels and greater weight gain relative to
those maintained on a short-day cycle (Suttie, White,
Breier, & Gluckman, 1991). Thus, exposure to a greater
amount of light during the first trimester may increase the
level of IGF-1 which, in turn, may increase growth.
Thus far, we have focused our discussion on the potential influence on prenatal growth of maternal exposure to
peak sunshine during the first trimester of gestation. In
Experiment 2, however, decreased maternal exposure to
sunshine during the second and third trimesters also was
associated with increased fetal growth. Although it is
possible that a lack of light during the second and third
trimesters is causally related to birth weight, this explanation seems unlikely. At present, there is no literature
linking exposure to darker conditions with growth or
growth-promoting hormones in mammals. A relation
between dark conditions and growth has been reported,
but only for nonmammalian species (Laartz et al., 1994;
Zeman et al., 1999). All available data point to greater
exposure to light as being involved in fetal growth. It is
apparent from the sunshine data in Figure 1 that a peak in
first-trimester sunshine is followed by a trough in secondor third-trimester sunshine and vice versa. Given that all of
the available data point to greater exposure to light as
influencing prenatal growth, it is most likely that maternal
exposure to high levels of sunshine during early gestation
is the driving force behind the effect documented here.
From a practical perspective, what are the implications
of the present findings for infant health and development?
It has been well documented that higher birth weight is
associated with better outcome. Higher birth weight
decreases the risk of perinatal morbidity and mortality
(Han & Carter, 2001; Smith et al., 2002) as well as the
risk of several adult-onset diseases including hypertension, ischemic heart disease, non-insulin-dependent
diabetes mellitus, and metabolic cardiovascular disease
(Gluckman & Pinal, 2002; Han & Carter, 2001). Low birth
weight also may impair neuroendocrine regulation (Han
& Carter, 2001) and, specifically, melatonin secretion
(Kennaway et al., 2001). The consequences of low
melatonin secretion are not well understood, but low
secretion of the hormone has been linked to a higher
incidence of depression, cardiovascular disease, stroke,
and delayed psychomotor development (Kennaway et al.,
2001; Tauman, Zisapel, Laudon, Nehama, & Sivan,
2002). It may be no coincidence that the incidence of
many of these disorders also varies according to season of
birth (Joiner, Pfaff, Acres, & Johnson, 2002; Poe, 2000).
Understanding the relation between light and growth
throughout the fetal period has important implications for

lighting regimes in neonatal intensive-care nurseries.


Traditionally, neonatal nurseries were brightly lit throughout the day and night using artificial light (Glotzbach,
Rowlett, Edgar, Moffat, & Ariagno, 1993; Kennaway,
Goble, & Stamp, 1996). More recently, the trend has been
to decrease the overall level of ambient lighting and to
vary the light according to some fixed day:night cycle
(Glotzbach et al., 1993; Mirmiran & Ariagno, 2000). On
the basis of the present findings, we hypothesize that
higher levels of natural light might optimize growth,
particularly under conditions in which additional calorie
loading is not possible. Further research is required to
determine the precise role that exposure to sunshine plays
in growth throughout the neonatal period.
On one hand, the major strength of the present study
was the use of a definition of season that was based on
atmospheric conditions (i.e., ambient temperature, hours
of bright sunshine) rather than on calendar months. On the
other hand, one potential weakness was the use of
traditional trimesters to divide human pregnancy into
thirds. We acknowledge that from a biological perspective, the use of trimesters is somewhat arbitrary. Further
research is required to determine the precise stage(s) of
prenatal development during which maternal exposure to
sunshine influences growth. The present study provides a
basis from which to further examine these effects.
In summary, we hypothesize that exposure to a greater
amount of bright sunshine increases the level of IGF-1,
which in turn increases growth, most probably by altering
placental metabolism during early pregnancy when placental growth is most rapid (Han & Carter, 2001). This
hypothesis remains to be tested.

NOTES
This research was supported by a Division of Sciences Grant
from the University of Otago to Harlene Hayne. Experiment 1
was based on Karen Tustins Year-3 (Junior) undergraduate
honors thesis, which was conducted under the direction of
Harlene Hayne and Julien Gross. Karen Tustin was supported by
a Neural System Structure and Function Theme Summer
Bursary during the preparation of the article. We thank Amy
Smyth for help with data collection and the National Institute of
Water and Atmospheric Research (NIWA) for the provision of
temperature and sunshine data. We also thank three anonymous
reviewers for their insightful comments and recommendations
on an earlier draft of this article.

REFERENCES
Adair, L., & Pollitt, E. (1983). Seasonal variation in pre- and
postpartum maternal body measurements and infant birth
weights. American Journal of Physical Anthropology, 62,
325331.

Season of Birth
Baker, J., Liu, J., Robertson, E., & Efstratiadis, A. (1993). Role
of insulin-like growth factors in embryonic and postnatal
growth. Cell, 75, 7382.
Bantje, H. (1987). Seasonality of births and birth weights in
Tanzania. Social Science and Medicine, 24, 733739.
Bellastella, A., Criscuolo, T., Iorio, S., Parlato, F., Sinisi, A. A.,
Sinisi, A. M., Pasquali, D., & Pisano, G. (1994). Normal
plasma insulin-like growth factor 1 levels and impaired final
stature in adult blind subjects. Journal of Endocrinological
Investigation, 17, 3740.
Benson, J. (1993). Season of birth and onset of locomotion:
Theoretical and methodological implications. Infant Behavior and Development, 16, 6981.
Benson, J. (1996). Replication study: Seasonality and locomotor onset. Infant Behavior and Development, 19, 329.
Bodnarchuk, J., & Eaton, W. (2002, April). Seasonal factors
and birth weight: New evidence from the southern hemisphere. Poster presented at the International Conference on
Infant Studies, Toronto.
Bryson, R., & Hare, F. (Eds.). ( 1974). World survey of climatology: Vol. 11. Climates of North America. Amsterdam:
Elsevier.
Davies, G., Ahmad, F., Chant, D., Welham, J., & McGrath, J.
(2000). Seasonality of first admissions for schizophrenia
in the Southern Hemisphere. Schizophrenia Research, 41,
457462.
de Messias, E., Cordeiro, N., Sampaio, J., Bartko, J., &
Kirkpatrick, B. (2001). Schizophrenia and season of birth in a
tropical region: Relationship to rainfall. Schizophrenia
Research, 48, 227234.
Eagles, J., Andrew, J., Johnston, M., Easton, E., & Millar, H.
(2001). Season of birth in females with anorexia nervosa in
northeast Scotland. International Journal of Eating Disorders,
30, 167175.
Fallis, G., & Hilditch, J. (1989). A comparison of seasonal
variation in birth weights between rural Zaire and Ontario.
Canadian Journal of Public Health, 80, 205208.
Gentilli, J. (Ed.). ( 1971). World survey of climatology: Vol. 13.
Climates of Australia and New Zealand. Amsterdam: Elsevier.
Glotzbach, S., Rowlett, E., Edgar, D., Moffat, R., &
Ariagno, R. (1993). Light variability in the modern neonatal
nursery: Chronobiologic issues. Medical Hypotheses, 41,
217224.
Gluckman, P. (1995). The endocrine regulation of fetal growth
in late gestation: The role of insulin-like growth factors.
Journal of Clinical Endocrinology and Metabolism, 80,
10471050.
Gluckman, P., Morel, P., Ambler, G., Breier, H., &
McCutcheon, S. (1992). Elevating maternal insulin-like
growth factor-1 in mice and rats alters the pattern of fetal
growth by removing maternal constraint. Journal of Endocrinology, 134, R1R3.
Gluckman, P., & Pinal, C. (2002). Maternalplacentalfetal
interactions in the endocrine regulation of fetal growth.
Endocrine, 19, 8189.
Gluckman, P., & Pinal, C. (2003). Regulation of fetal growth
by the somatotrophic axis. Journal of Nutrition, 133, 1741S
1746S.

229

Goldberg, A., & Newlin, D. (2000). Season of birth and


substance abuse: Findings from a large national sample.
Alcoholism: Clinical and Experimental Research, 24, 774
780.
Greenfield, H. (1983). Birth weights in Goroka and Kainantu
hospitals. Papua New Guinea Medical Journal, 26, 9398.
Han, V., & Carter, A. (2001). Control of growth and
development of the feto-placental unit. Current Opinion in
Pharmacology, 1, 632640.
Hayashi, K. (1990). Correlation between temperature and
infants gross motor development. Developmental Medicine
and Child Neurology, 32, 833834.
Hayashi, K. (1992). The influence of clothes and bedclothes on
infants gross motor development. Developmental Medicine
and Child Neurology, 34, 557558.
Henneberg, M., & Louw, G. (1993). Further studies on the
month-of-birth effect on body size: Rural schoolchildren and
an animal model. American Journal of Physical Anthropology, 91, 235244.
Hort, K. (1987). Seasonal variation of birth weight in
Bangladesh. Annals of Tropical Paediatrics, 7, 6671.
Huizinga, J., & Wijngaard, E. (1981). Birth weights in Sapone,
a village near Ouagadougou (Upper-Volta). Collegium
Antropologicum, 5, 179189.
Joiner, T., Pfaff, J., Acres, J., & Johnson, F. (2002). Birth month
and suicidal and depressive symptoms in Australians born in
the Southern vs. the Northern hemisphere. Psychiatry Research, 112, 8992.
Kennaway, D., Flanagan, D., Moore, V., Cockington, R.,
Robinson, J., & Phillips, D. (2001). The impact of fetal size
and length of gestation on 6-sulphatoxymelatonin excretion
in adult life. Journal of Pineal Research, 30, 188192.
Kennaway, D., Goble, F., & Stamp, G. (1996). Factors
influencing the development of melatonin rhythmicity in
humans. Journal of Clinical Endocrinology and Metabolism,
81, 15251532.
Kovalenko, P., Hoven, C., Wicks, J., Moore, R., Mandell, D., &
Liu, H. (2000). Seasonal variations in internalizing, externalizing, and substance use disorders in youth. Psychiatry
Research, 94, 103119.
Kunugi, H., Nanko, S., Watanabe, H., Sekiba, K., &
Kazamatsuri, H. (1998). Season of birth of chronic alcoholics. Journal of Psychiatric Research, 32, 321323.
Laartz, B., Losee-Olson, S., Ge, Y., & Turek, F. (1994). Diurnal,
photoperiodic, and age-related changes in plasma growth
hormone levels in the golden hamster. Journal of Biological
Rhythms, 9, 111123.
Lakshmi, G., & Bandyopadhyay, S. (1987). Birth weight in a
hospital sample from Dehra Dun City with special reference
to seasonal variation. Journal of the Indian Medical Association, 83, 332335.
Liu, J., Baker, J., Perkins, A., Robertson, E., & Efstratiadis, A.
(1993). Mice carrying null mutations of the genes encoding
insulin-like growth factor 1 (Igf-1) and type 1 IGF receptor
(Igf1r). Cell, 75, 5972.
Mirmiran, M., & Ariagno, R. (2000). Influence of light in the
NICU on the development of circadian rhythms in preterm
infants. Seminars in Perinatology, 24, 247257.

230

Tustin, Gross, and Hayne

Morgan, V., Jablensky, A., & Castle, D. (2001). Season of birth


in schizophrenia and affective psychoses in Western
Australia 191661. Acta Psychiatrica Scandinavica, 104,
138147.
Murray, L., OReilly, D., Betts, N., Patterson, C., Davey Smith,
G., & Evans, A. (2000). Season and outdoor ambient temperature: Effects on birth weight. Obstetrics and Gynecology,
96, 689695.
Narita, K., Sasaki, T., Akaho, R., Okazaki, Y., Kusumi, I., Kato,
T., Hashimoto, O., Fukuda, R., Koyama, T., Matsuo, K.,
Okabe, Y., Nanko, S., Hohjoh, H., & Tokunaga, K. (2000).
Human leukocyte antigen and season of birth in Japanese
patients with schizophrenia. American Journal of Psychiatry,
157, 11731175.
Parker, G., Mahendran, R., Koh, E., & Machin, D. (2000).
Season of birth in schizophrenia: No latitude at the equator.
British Journal of Psychiatry, 176, 6871.
Poe, M. (2000). Associations between risk of disease and birth
season using Medicare hospital claims data. Dissertation
Abstracts International, 62, 792B. UMI number 3003367.
Smith, G., Stenhouse, E., Crossley, J., Aitken, D., Cameron, A.,
& Connor, J. (2002, June 27). Early pregnancy origins of low
birth weight. Nature, 417, 916.
Suttie, J., White, R., Breier, B., & Gluckman, P. (1991).
Photoperiod associated changes in insulin-like growth factor1 in reindeer. Endocrinology, 129, 679682.
Tatsumi, M., Sasaki, T., Iwanami, A., Kosuga, A., Tanabe, Y.,
& Kamijima, K. (2002). Season of birth in Japanese
patients with schizophrenia. Schizophrenia Research, 54,
213218.

Tauman, R., Zisapel, N., Laudon, M., Nehama, H., & Sivan, Y.
(2002). Melatonin production in infants: Association with
perinatal factors and development. Pediatric Neurology, 26,
379382.
van Hanswick de Jonge, L., & Waller, G. (2002). Influence of
environmental temperatures during gestation and at birth on
eating characteristics in adolescence: A replication and
extension study. Appetite, 38, 181187.
Waldie, K., Poulton, R., Kirk, I., & Silva, P. (2000). The effects
of pre- and post-natal sunlight exposure on human growth:
Evidence from the Southern Hemisphere. Early Human
Development, 60, 3542.
Watkins, B., Willoughby, K., Waller, G., Serpell, L., & Lask, B.
(2002). Pattern of birth in anorexia nervosa I: Early-onset
cases in the United Kingdom. International Journal of Eating
Disorders, 32, 1117.
Weber, G., Prossinger, H., & Seidler, H. (1998). Height depends
on month of birth. Nature, 391, 754755.
Webster, J., Corson, I., Littlejohn, R., Stuart, S., & Suttie, J.
(1998). Effects of photoperiod on the cessation of growth
during autumn in male red deer and growth hormone and
insulin-like growth factor-1 secretion. General and Comparative Endocrinology, 113, 464477.
Wohlfahrt, J., Melbye, M., Christens, P., Andersen, A., &
Hjalgrim, H. (1998). Secular and seasonal variation of length
and weight at birth. Lancet, 352, 1990.
Zeman, M., Buyse, J., Lamosova, D., Herichova, I., &
Decuypere, E. (1999). Role of melatonin in the control of
growth and growth hormone secretion in poultry. Domestic
Animal Endocrinology, 17, 199207.