167

Climate Change and the Phenology of Sympatric Birds, Insects,
and Plants in Japan
Shigeto KOIKE1, Go FUJITA2 and Hiroyoshi HIGUCHI2*
1

Hakunan Junior High School
7619 Ibarasone, Niigata-City, Niigata 950-1456, Japan
2
Laboratory of Biodiversity Science, School of Agriculture and Life Sciences,
The University of Tokyo
1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan*Corresponding author

Abstract
We analyzed the relationships between a long-term trend of rising air temperature and the lives ofthree species of creatures: red-cheeked starlings, paleotropical migratory birds that breed in Japan, small
white butterflies and cherry trees (Somei-Yoshino cherry). We studied the egg-laying dates of the starlings in Niigata City located in the central part of Honshu, the largest of the four main islands of Japan.
We obtained the first appearance dates of imagoes of small whites and the blooming dates ofSomei-Yoshino cherry trees in Niigata from the Japan Meteorological Agency. Red-cheeked starlings
had a significant tendency to start their egg-laying earlier each year; over the course of 28 years the laying date became 15.3 days earlier. Their progressively earlier egg-laying dates were significantly correlated with the rise in early spring temperatures in Niigata City, their breeding ground, and with the temperature of Naha City in Okinawa Prefecture, which is a migration stopover area in southern Japan.
Since temperatures of both areas rose significantly during the period, it is likely that the temperature rise
was the cause of the advanced egg-laying dates. The cherries’ blooming date also tended to become earlier year-by-year, showing a strong negative correlation with the temperature of early spring. The first
appearance date of small whites showed no tendency to become earlier year-by-year, but showed a significant negative correlation with the temperature of early spring. We think that the reason for the cherrytrees’ blooming date showing a stronger correlation with the temperature of early spring than the laying
date of the starlings is because, unlike migratory birds, cherry trees grow in the same region for the entire year. Thus they are greatly influenced by the temperature of our investigation area (Niigata City).
Also, unlike small whites whose chrysalises pass the winter close to the surface of the earth covered
with snow, cherry buds are exposed to the air and so might have been more influenced by the long-termwarming trend in early spring air temperatures.
Key words: blooming date, climate change, egg-laying date, first appearance date,
red-cheeked starling, small white, Somei-Yoshino cherry

1. Introduction
The average ground temperature of the earth rose
0.61°C in the 140 years between 1861 and 2000
(IPCC, 2001) and the average temperature of Japanrose 1.0°C in the 100 years of the 20th century (JMA,2002). Changes related to such global warming are
beginning to appear in forests and coral reefs, floral
and faunal distributions, and birds’ migration dates(e.g., Mason, 1995; Hughes, 2000; Masuda, 2003;
Omasa, 2003; Murphy-Klassen et al., 2005). Global
warming may change the life of plants and animals,
and may threaten their existence. It is necessary to
Global Environmental Research
10(2)/2006: 167-174
printed in Japan

examine closely such ecological changes, and to
consider conservation strategies. However, theinfluence of global warming will not be recognizedeasily in the short term, and serious and lengthy
research is necessary.
In Europe and North America, information on
birds’ breeding seasons has been collected for a longtime, and has been analyzed in relation to climatechange. In England, 20 species out of 65 showed
egg-laying dates advancing an average of 9 days in the
25 years between 1971 and 1997 (Crick et al., 1997;
Crick & Sparks, 1999). The egg-laying date of greattits (Parus major) became about 11 days earlier in the©2006 AIRIES168

S. KOIKE et al.

27 years between 1971 and 1997 (McCleery & Perrins,
1998). In Germany the egg-laying date of pied
flycatchers (Ficedula hypoleuca) became 4 days
earlier in the 26 years between 1970 and 1995, andtheir clutch size significantly increased (Winkel &Hudde, 1997). In North America, the egg-laying dateof Mexican jays (Aphelocoma ultramarina) became
about 10 days earlier in the 28 years between 1971
and 1998 (Brown et al., 1999), and the egg-laying
date of tree swallows (Tachycineta bicolor) became
about 6 days earlier in the 11 years between 1990 and2000 (Hussell, 2003). In these studies, risingtemperatures were considered to be the cause for theadvanced egg-laying dates.
We have previously pointed out the tendencies forthe first-egg date of red-cheeked starlings (Sturnia
philippensis) to become 2 weeks earlier and for theirclutch size to increase by 1.2 eggs in the 21 years
between 1978 and 1998 in Niigata Prefecture locatedin the central part of Honshu, the largest of the fourmain islands of Japan (Koike & Higuchi, 2002).
Red-cheeked starlings winter in areas of Southeast
Asia such as Borneo, migrating to and breeding inJapan and Sakhalin in summer (Fig. 1; Brazil, 1991;
Koike, 1997; Feare & Craig, 1999; OSJ, 2000). They
migrate over Japan’s southwestern islands between
March and April (Brazil, 1991; MWBA, 2000; Koike& Higuchi, 2002), arriving in Niigata City in early
April. They nest in tree cavities and lay 3-9 eggs.

Because they prefer to use nest boxes, and because
they raise a maximum of only one brood (Koike,1988) their egg-laying dates can be obtained easily
and reliably.
In Japan, information on the first appearance datesof small whites (Pieris rapae) and the blooming datesof Somei-Yoshino cherry trees (Prunus yedoensis) has
been accumulated by the Japan Meteorological
Agency over many years. Small whites, seen easily invarious parts of Japan, pass the winter as chrysalises,
and emerge as imagoes in the early spring. The first
appearance date of this species indicates that achrysalis has emerged for the first time. This species is
not the staple food of red-cheeked starlings, but can beviewed as representative of insects eaten by thestarlings. A Somei-Yoshino cherry tree is a hybrid
between Oshimazakura (Prunis lannesiana) and
Edohigan (Prunis pendula) cherries. Aono (1998) and
Masuda et al. (1999) showed that the blooming dateof Somei-Yoshino cherry trees is becoming earlier invarious parts of Japan. Cherry trees, including theSomei-Yoshino cherry, are among the tree species inthe breeding habitat of red-cheeked starlings. There isbelieved to be a co-relation between the blooming
season and leaf-opening season of these trees and thetime of first appearance of the insects eaten by
red-cheeked starlings.
In this paper, we extend the results of Koike andHiguchi (2002), and clarify the trend of egg laying

Fig. 1 The wintering ground, breeding ground, and spring migration route(arrows) of red-cheeked starlings. Drawn based on Brazil (1991) andFeare & Craig (1999).

Climate Change and the Phenology of Sympatric Birds, Insects, and Plants in Japandates of red-cheeked starlings during the 28 years
until 2005, analyzing its relation to temperatures in thebreeding, stopover and wintering areas. We show how
the change in the egg-laying dates has influenced thebirds’ clutch size and breeding success. Then, weclarify recent changes in the annual first appearance
date of small whites and Somei-Yoshino cherry trees’
blooming date, both of which live and grow in thesame area as the starling, and we search for a relation
with the egg-laying dates of the birds. Such studies
dealing with the phenology of two or more taxonomic
groups in the same area are limited (e.g. Buse et al.,
2002; Sanz et al., 2003; Both & Visser, 2005; Bothet al., 2006).

2. Study Areas and Methods
The breeding ecology of red-cheeked starlings wasstudied in a forest area on the coast of Niigata City
(37°55’N, 139°03’E). This forest area consisted mainly of tree species such as Japanese black pines (Pinus
thunbergii), false acacias (Robinia pseudo-acacia),
Japanese hackberries (Celtis sinensis), and Oshimazakura (Prunus lannesiana). Japanese honeysuckle(Lonicera morrowii) and multiflora rose (Rosamultiflora) dominate the shrub layer.
We conducted our fieldwork between 1978 and2005, excluding between 1980 and 1984, and 1995.
Each year we set 30 to 100 nest boxes on tree trunks
about 2-3 m above ground at intervals of 10-20 m.
Each nest box was 14 cm × 16 cm at the base and30 cm in height, and the diameter of the entrance holewas 4 cm. We used the first egg-laying date of eachpair to set the standard for their breeding season. The
mean of all the breeding pairs’ first egg-laying dates ineach year is indicated as the egg-laying date. In
calculating the mean egg-laying date, we set March 1
as the reference value, “1.” We excluded cases ofre-nesting that occurred after breeding failures. We
also recorded clutch sizes, hatching numbers andfledgling numbers, and calculated the means for eachyear similarly. The breeding success rate wasindicated as number of fledglings / clutch size × 100.
We obtained information on the first appearance
dates of imagoes of small whites, Somei-Yoshinocherry trees’ blooming dates, and temperatures from
CD-ROM data and from the web-site of the Japan
Meteorological Agency (http://www.jma.go.jp/jma/index.html). We also acquired data directly from the
Niigata Local Meteorological Observatory whennecessary. The target period was between 1978 and2005, which is when we studied red-cheeked starlings.
We utilized mean daily temperatures provided by
the Japan Meteorological Agency. We labeled as“early spring temperature” the temperature between
February and April (three months) that were thought
to be related to red-cheeked starlings’ egg-laying,small whites’ appearance and cherry blooming, andwe showed the relation between the target species’169

phenology and early spring temperature. We also
investigated the annual temperature change based on
the mean temperatures of the above three months. In
examining the correlations and tendencies, the year
1978 was set as 0 for analysis. For red-cheeked
starlings, we investigated the relation of the egglaying date with the temperature of Niigata City, Kota
Kinabalu City (5°93’N, 116°04’E) in Borneo (thewintering ground) and Naha City (26°12’N, 127°41’E,
the resting area for the starlings) on Okinawa, one of
the southwestern islands of Japan.
To show changes in annual egg-laying dates andclutch sizes, we conducted a one-way ANOVA as well
as a Pearson’s product-moment correlation analysis.
In investigating the correlation of temperature withchanges in red-cheeked starlings’ annual egg-laying
dates and clutch sizes, small whites’ first appearance
dates and cherry trees’ blooming dates, we conducteda Pearson’s product-moment correlation analysis. We
implemented a Bonferroni correction for the significance level when examining the comparison of two or
more relations using the same material. In investigating year-by-year changes in red-cheeked starlings’
clutch size, we paid attention to the relationship ofclutch size to egg-laying date. We predicted that clutch
size would have increased because the egg-laying date
had advanced. In order to test this prediction, we
divided the first egg dates into ten-day intervals andnoted whether there was year-by-year change in clutch
size in the same period.
For statistical analysis we used STATISTICA(ver.5.5) and JMP (ver.6).

3. Results
3.1 Changes in red-cheeked starlings’ annual
egg-laying date
The egg-laying date of red-cheeked starlings
became earlier year-by-year (Fig. 2; F = 48.12, df =21,836, P <0.0001; one-way ANOVA). The latest date
was day 86.4 (25.4 May) in 1978 and the earliest date
was day 64.5 (3.5 May) in 2002. There is a significant
negative relation (r = − 0.876, P < 0.0001, N = 22) of
y = 83.94 − 0.57x（1978 = 0）between yearly egglaying date (y) and year (x), indicating that the egglaying date advanced 0.57 days per year, and 15.3
days in 28 years. Also, a significant decreasing
tendency was observed in the standard deviation foreach year’s egg-laying date (r = − 0.616, P < 0.0005,
N = 22), indicating that the breeding period became
shorter each year.
3.2 Red-cheeked starlings’ egg-laying date andearly spring temperature
A significant negative correlation was observed
between red-cheeked starlings’ egg-laying dates andearly spring temperatures of Niigata City (Fig. 3(a);r = − 0.617, P < 0.01, with Bonferroni correction,
N = 22). There was also a significant negative correla-

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S. KOIKE et al.

y = 83.94 − 0.57x, r = − 0.876, P < 0.0001, N = 22.

Fig. 2 Changes in the annual first egg-laying date in red- cheeked starlings (1 March =day 1). The value for each year is the mean ± s.e. The numbers across the topof the figure indicate sample sizes (One-way ANOVA: F = 48.12, df = 21,836,
P < 0.0001).

tion of egg-laying dates with early spring temperaturesof Naha City, Okinawa (Fig. 3(b); r = − 0.651,
P < 0.005, with Bonferroni correction, N = 22). No
significant correlation was observed between egglaying dates and temperatures between February and
April of Kota Kinabalu in Borneo, the wintering
ground (r = − 0.114, P > 0.05, with Bonferroni
correction, N = 20, 1982-2005).
Early spring temperatures of Niigata City (Fig. 4(a);r = 0.464, P < 0.05, N = 28) and of Naha City (Fig.
4(b); r = 0.495, P < 0.01, N = 28) have risen
significantly in recent years. Niigata City’s early
spring temperature (y) is indicated in relation to year(x) by y = 5.90 + 0.06x (1978 = 0), and is rising by anaverage of 0.06°C per year for a total of 1.5°C in 28
years. Naha City’s early spring temperature (y) is
indicated in relation to year (x) by y = 18.48 + 0.04x(1978 = 0), and is rising by an average of 0.04°C peryear for a total of 1.1°C in 28 years. The mean annual
temperatures of Niigata City [r = 0.537, P < 0.01,
y = 13.22 + 0.04x (1978 = 0), N = 28] and Naha City[r = 0.722, P < 0.0001, y = 22.32 + 0.04x (1978 = 0),
N = 28] are also rising significantly. However, thetemperature of Kota Kinabalu between February and
April and the mean annual temperature there haveshown no significant rise (r = − 0.032, P > 0.05,
N = 24 for between February and April; r = 0.187,
P > 0.05, N = 24, for the annual temperature;
1982-2005). Thus, the advancement of the redcheeked starlings’ egg-laying date is related to temperature rises at both their breeding grounds and at astop-over site during spring migration.

3.3 Year-by-year changes in red-cheeked starlings’
clutch size and breeding success
The clutch size tended to increase significantly
each year (Fig. 5; F = 4.52, df = 21,782, P < 0.0001;
one-way ANOVA). Based on the regression formulaof y = 5.03 + 0.04x (1978 = 0), which can be obtained
from the mean clutch size (y) of each year and year (x),it increased by 0.04 eggs a year for a total of 1.03 eggs
in 28 years (r = 0.781, P < 0.0001). The clutch size
tends to vary with the time of year, such that the earlier the first egg-laying date is, the larger the clutch is.
For example, in 1991, as indicated by the regression
formula of y = 13.46 − 0.17x, (y: clutch size, x: firstegg laying date, r = − 0.621, P < 0.001, N = 39), there
was a decrease of 0.17 eggs per day in that season. A
significant negative relation was also observed
between the egg-laying date (x) and mean clutch size(y) (Fig. 6; y = 10.05 − 0.06x, r = − 0.782, P < 0.0001,
N = 22). When the results were divided into late April(r = − 0.419, P > 0.05, N = 15), early May (r =− 0.018, P > 0.05, N = 292), mid May (r = − 0.091,
P > 0.05, N = 409) and late May (r = − 0.008, P > 0.05,
N = 80), no significant annual increase or decrease
occurred in the relation between egg-laying date andclutch size. While a significant decreasing trend wasobserved in early June (r = − 0.794, P < 0.05, N = 8),
no significant difference was observed by a one-way
ANOVA across all periods (F = 3.25, df = 3,8,
P > 0.05).
No significant annual change was observed inbreeding success (r = 0.338, P > 0.05, N = 14).
However, as described by the quadratic curve, y =0.6513 + 0.0146x − 0.0004x², (r² = 0.300, P > 0.05,
1978 = 0), it appears that breeding success rose until
the first half of the 1990s and then descended slightly
afterwards.

Climate Change and the Phenology of Sympatric Birds, Insects, and Plants in Japan

171

Fig. 3 Relation between the mean temperature of early spring (February-April) and red-cheeked starlings’ egg-laying datein Niigata City (a), central Japan, and in Naha City (b), southern Japan.

Fig. 4 Mean temperature in early spring (February-April) in Niigata City (a), and in Naha City (b) from 1978 to 2005.

Fig. 5 Clutch size in red-cheeked starlings from 1978 to
2005. The value for each year is the mean ± s.e.
The numbers across the top of the figure indicate
sample sizes. (One-way ANOVA: F = 4.52, df =21,782, P < 0.0001)

Fig. 6 Relation of egg-laying date (1 March = day 1) andclutch size in red-cheeked starlings.

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S. KOIKE et al.

3.4 First appearance date of small whites
The average first appearance date of small whites
during the 28 year period in Niigata City was day 38.5
(7.5 April ). The latest first appearance was day 52 (23April ) in 1984 , and the earliest, day 13 (13 March )in 2002 . The first appearance date of small whites in
Niigata in 1978 and after did not significantly advanceeach year with a linear regression (r = − 0.151 P >0.05, N = 28) or two-dimensional regression (Fig. 7;
r² ＝ 0.048, P > 0.05, N = 28). However, remarkably
early first appearance dates become noticeable in thelatest years. There was also a significant correlation
between the early spring temperatures of Niigata Cityand the first appearance date. Thus, it is estimated thatthe insects emerged earlier in the year when thetemperature was higher (Fig. 8; r = − 0.554, P < 0.005,
N = 28).

day 57 (28 April) in 1984, and the earliest, day 30 (30March) in 2002. The blooming date advanced byabout 8.46 days in 28 years, or 0.31 days per year
(Fig. 9; blooming date y; year x; y = 45.05 − 0.31x,
r = − 0.437, P < 0.05, N = 28). The blooming date wassignificantly negatively correlated with early spring
temperatures (Fig. 10; r = − 0.952 , P < 0.0001,
N = 28). The degree of the correlation of early spring
temperatures with the cherry blooming date wasgreater than that with either the red-cheeked starlings’
egg-laying date or first appearance date of small
whites.

4. Discussion

3.5 Cherry blooming date
The average blooming date of Somei-Yoshinocherry trees during the 28 year period in Niigata City
was day 40.8 (9.8 April). The latest blooming date was

Detailed data on egg-laying dates can be obtainedusing nest boxes. Based on various studies using nest
boxes, comparison of egg-laying date advancement
per year according to regions and species has yielded
the following results. In England, egg laying of greattits advanced 0.44 days/year (McCleery & Perrins,
1998); in Germany, that of great tits advanced 0.26

Fig. 7 First appearance date (1 March = day 1) of small
whites in Niigata City from 1978 to 2005.

Fig. 9 Cherry blooming date (1 March = day 1) in Niigata
City from 1978 to 2005.

Fig. 8 Relation between the mean temperature of early spring(February-April) and small whites’ first appearance
date in Niigata City.

Fig. 10 Relation between the mean temperature of early spring(February-April) and cherry blooming date in Niigata
City.

Climate Change and the Phenology of Sympatric Birds, Insects, and Plants in Japan

days/year; blue tits, 0.26 days/year; and pied flycatchers, 0.17 days/year (Winkel & Hudde, 1997). In
Canada, that of tree swallows advanced 0.55 days/year(Hussell, 2003). Both et al. (2004) examined the
egg-laying date advancement of pied flycatchers in
25 places in Europe, and found that the region where
the change was the greatest was Lingen, Germany(52°27’N, 07°15’E), which showed an advancement of
0.49 days/ year. In Niigata City (37°55’N, 139°03’E),
red-cheeked starlings advanced 0.57 days/year, which
is a greater change than in the other areas mentioned
above.
The difference in the temperature change in eachregion might influence the degree of change in
egg-laying dates. According to Both et al. (2004), in
Lingen, Germany, where the advancement of pied
flycatchers’ egg-laying date was the most marked, thetemperature rise was also marked, rising 0.12°C/ year.
However, in Niigata City where the temperature rose
only 0.06°C a year, the advancement of red-cheeked
starlings’ egg-laying date was even more marked thanthat of pied flycatchers in Lingen.
The causes of the red-cheeked starlings’ marked
advancement in egg-laying date may go beyond thetemperature of the breeding ground to include theinfluence of rising temperatures at migratory stopover sites in spring. As noted earlier, the early spring
temperature of Naha City, Okinawa, rose 1.1°C in the
28 years between 1978 and 2005, or 0.04°C/year.
When compared with the temperature change ofLingen, the rate of the rise of Okinawa and Niigata issmall, but it is more remarkable when compared withthe world’s annual mean temperature rise over thesame period, 0.01°C/year (r = 0.764, P < 0.0001). If
the temperature increase of two or more regions such
as Okinawa and Niigata is multiplicative, the effect on
the egg-laying date might accelerate. At the moment,
it is not possible to compare the annual increases intemperature that birds in all parts of the world havebeen and are experiencing. For migratory birds like
red-cheeked starlings though, we think it is necessary
to consider the advancement of their first breedingdate to be related to the temperatures of both theirbreeding grounds and their resting grounds during
migration.
Regarding analytical methods, in this paper wehave shown a simple Pearson’s correlation between
red-cheeked starlings’ egg-laying date and the early
spring temperature of each of the three areas of
Niigata, Naha and Kota Kinabalu. In another analysis(Koike et al., in preparation), we tried a model
selection procedure (Burnham & Anderson, 2002) ofgeneralized linear models (GLMs) based on Akaike’s
Information Criterion (AIC). The results obtained aresimilar to those shown in this paper. That is, threeplausible models (i.e., ∆AIC < 4) included the early
spring temperature of Niigata and/or Naha, and bothvariables showed negative effects on the starlings’
egg-laying date. Details will be described elsewhere.

173

Red-cheeked starlings, small whites, and SomeiYoshino cherry trees that live and grow in the same
area responded differently to the same climate change.
Red-cheeked starlings’ egg-laying dates and SomeiYoshino cherry trees’ blooming dates tended toadvance each year, but the small whites’ first appearance dates did not show a similar significant tendency.
However, in the last decade there have been someyears when small whites’ first appearances wereremarkably early, so we should look out for continued
advancement in the future.
Red-cheeked starlings’ egg-laying dates and cherry
tree blooming dates are not necessarily changing at
the same pace. However, there was a tendency for thedifference in the dates of the two to become less eachyear (y = 40.86 − 0.35x, r = − 0.571, P < 0.01, N = 22).
This means that the acceleration of red-cheeked starlings’ egg-laying dates is greater than the accelerationof cherry trees’ blooming dates. According to theabove-mentioned regression formula, the difference ofthe two was 40.9 days in 1978, but only 31.5 days in
2005, a reduction of 9.3 days.
The parents of red-cheeked starlings feed theirnestlings not only insects, but also fruits of cherrytrees and Japanese honeysuckles (Koike, 1988). With
the change in blooming, the fruiting season is alsochanging. If the difference between the red-cheeked
starlings’ breeding season and the plants’ blooming
season becomes smaller in the future, red-cheeked
starlings may finish raising their nestlings in the nest
before cherry trees and Japanese honeysuckles bear
fruit. In fact, in the 1970s, many seeds from Japanesehoneysuckles and cherries regurgitated by nestlings
were found in red-cheeked starlings’ nests. After 2000
though, cherry seeds were still found but Japanesehoneysuckle seeds were rarely seen.
Because the clutch size is increasing and because
the gap between the egg-laying date and the phenology of insects and plants during breeding is narrowing,
one might predict a change in the red-cheeked starling’s breeding success. At present, there is no indication of such a change. However, if the temperature
keeps rising in the future, the gap in the floral andfaunal phenologies will become narrower, and it ispossible that the red-cheeked starlings’ breeding success will decrease, as shown by Both et al. (2006) for
pied flycatchers.
The correlation between Somei-Yoshino cherrytrees’ blooming dates and early spring temperatures
was stronger than that of red-cheeked starlings’ egglaying dates and early spring temperatures. It isthought that this is because the cherry tree is a plantand cannot move, resulting in its being directly
influenced by the temperature of Niigata City where it
grows. As the red-cheeked starling, a paleotropicalmigratory bird, is influenced by temperatures at its
stop-over sites on the spring migration route, it ispossible that the correlation of their breeding season
and temperatures in Niigata is weaker. Individual

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small whites live in the same area throughout the year.
Although their time of first appearance was significantly correlated with early spring temperature, thecorrelation was smaller compared than that of SomeiYoshino cherry trees. The wintering site of small
whites’ chrysalises is the vicinity of the earth’s surface,which is often covered by snow until March. It is
likely that this snow cover has reduced the effect of
the long-term increase in air temperature on thisbutterfly.

Acknowledgment
We thank Tom Grubb, Jr., for reviewing a draft ofthis paper. The project was supported in part by The
University of Tokyo’s 21st Century COE program,“Biological Diversity and Ecosystem Restoration.”
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(Received 6 September 2006, Accepted 26 September 2006)