INTERNATIONAL JOURNAL OF CLIMATOLOGY
Int. J. Climatol. (2009)
Published online in Wiley InterScience
(www.interscience.wiley.com) DOI: 10.1002/joc.2014
Short Communication
Continental-scale phenology: warming and chilling
Mark D. Schwartz* and Jonathan M. Hanes
Department of Geography, University of Wisconsin-Milwaukee, PO Box 413, Milwaukee, WI 53201, USA
ABSTRACT: With abundant evidence of recent climate warming, most vegetation studies have concentrated on its direct
impacts, such as modifications to seasonal plant and animal life cycle events (phenology). The most common examples are
indications of earlier onset of spring plant growth and delayed onset of autumn senescence. However, less attention has
been paid to the implications of continued warming for plant species’ chilling requirements. Many woody plants that grow
in temperate areas require a certain amount of winter chilling to break dormancy and prepare to respond to springtime
warming. Thus, a comprehensive assessment of plant species’ responses to warming must also include the potential impacts
of insufficient chilling.
When collected at continental scale, plant species phenological data can be used to extract information relating to the
combined impacts of warming and reduced chilling on plant species physiology. In this brief study, we demonstrate that
common lilac first leaf and first bloom phenology (collected from multiple locations in the western United States and
matched with air temperature records) can estimate the species’ chilling requirement (1748 chilling hours, base 7.2 ° C) and
highlight the changing impact of warming on the plant’s phenological response in light of that requirement. Specifically,
when chilling is above the requirement, lilac first leaf/first bloom dates advance at a rate of −5.0/−4.2 days per 100h reduction in chilling accumulation, while when chilling is below the requirement, they advance at a much reduced
rate of −1.6/−2.2 days per 100-h reduction. With continental-scale phenology data being collected by the USA National
Phenology Network (http://www.usanpn.org), these and more complex ecological questions related to warming and chilling
can be addressed for other plant species in future studies. Copyright  2009 Royal Meteorological Society
KEY WORDS
phenology; global warming; lilac; chilling requirement western United States
Received 23 January 2009; Revised 24 July 2009; Accepted 3 August 2009
1.
Introduction
Evidence of recent climate warming, as well as its
impacts on the biosphere are abundant (IPCC, 2007).
Phenology, the study of seasonal plant and animal life
cycles, driven by environmental change ‘. . .is perhaps the
simplest process in which to track changes in the ecology
of species in response to climate change’ (IPCC, 2007).
Numerous phenological studies have identified important
direct effects of warming, such as earlier onset of spring
plant growth and delayed onset of autumn senescence
across temperate mid-latitude climates (Parmesan and
Yohe, 2003; Root et al., 2003; Menzel et al., 2006;
Schwartz et al., 2006). Yet, many woody plant species
growing in these regions also paradoxically require
a certain amount of exposure to cold temperatures
(termed the fall/winter chilling requirement), in order to
properly break their dormancy and be ready to respond to
springtime warming (Sarvas, 1974; Cannell and Smith,
1983; Chuine and Cour, 1999; Baldocchi and Wong,
2008; Luedeling et al., 2009).
* Correspondence to: Mark D. Schwartz, Department of Geography,
University of Wisconsin-Milwaukee, PO Box 413, Milwaukee, WI
53201, USA. E-mail: [email protected]
Copyright  2009 Royal Meteorological Society
Thus, with recent and projected future warming, a
point will eventually be reached (likely different for
every species), where plants in temperate climates will
no longer be able to continue linearly expanding both
ends of their growing season. It is highly likely that
temperate plant species in many regions, especially those
on the warmer (southern) extremes of their range, may
already be inadequately chilled and no longer responding
in the same way to additional spring warming (Zhang
et al., 2007). Therefore, comprehensive assessment of
likely plant species responses (growing season change)
to continued warming in temperate mid-latitude climates
must include the potential impacts of insufficient chilling
(Baldocchi and Wong, 2008; Luedeling et al., 2009).
When necessary chilling is not received, more springtime warming is required to initiate budburst (Murray
et al., 1989). The direct effect of this on a plant species
should be slowing or even a suspension of the rate at
which the onset of the growing season advances towards
earlier dates, with additional climate warming. Perhaps
more importantly, process-based phenology models suggest that lack of chilling also has long-term consequences
for some species viability, through reduced reproductive success (Morin et al., 2007). Lack of chilling may
M. D. SCHWARTZ AND J. M. HANES
also decrease plant productivity, thereby reducing carbon
reserves needed to overcome stress from pests or extreme
weather events. Thus, being able to assess chilling adequacy has important implications for the future ecology
and vulnerability of many temperate plant species.
Phenological studies have provided primary evidence
of the direct impacts of climate warming on the temperate biosphere. Now, we contend that, when recorded
at a continental-scale, plant species’ phenological data
can also be used to extract information relating to the
large-scale impacts of warming (and reduced chilling) on
plant species’ physiology. A recent study supports this
contention, and asserts that some southern parts of the
United States are already experiencing the impacts of
the chilling inadequacy described above (Zhang et al.,
2007). However, these and similar studies that rely on
remotely sensed information cannot explore this issue as
thoroughly as surface species-based phenological observations (Schwartz, 1998). In this study, we demonstrate
how first leaf and first bloom phenology from multiple
locations across the western United States (when matched
with temperature records) can estimate a plant species’
chilling requirement and evaluate the changing impact of
warming on the plant’s phenological response in light of
that requirement.
2.
Figure 1. Western United States study area and station distribution
(black dots are locations with both first leaf and first bloom lilac data;
grey dots are locations with first bloom lilac data only).
Data and methods
We obtained common lilac (Syringa vulgaris) first leaf
(660 cases/84 stations) and first bloom dates (1428
cases/111 stations) recorded over the 1967–2003 and
1956–2003 periods respectively at National Weather
Service Cooperative (COOP) stations distributed across
the western United States (from 32.10 to 48.78 ° N,
99.73 to 121.17 ° W, and elevations of 119 to 2404 m;
Figure 1), and combined these with co-located daily maximum–minimum air temperature records (Cayan et al.,
2001; Schwartz and Caprio, 2003; NCDC, 2005). The
first leaf event is defined as occurring when the widest
part of the newly emerging leaf has grown beyond
the ends of its opening winter bud scales (inset within
Figure 2). The first bloom event is defined as occurring
when at least 50% of the flower clusters (a grouping of
many small individual flowers) have at least one open
flower (inset within Figure 3).
We evaluated the impact of chilling levels on first leaf
and first bloom dates by first calculating accumulated
chilling hours (below a 7.2 ° C base temperature, commonly used for horticultural trees and shrubs; Linvill,
1990; Schwartz, 1997) and chill units received between
1 October and 1 February each year from the air temperature records. The chill unit method assigns variable
weights (determined by a sinusoidal curve) to chilling
hours associated with different temperature levels, such
that temperatures of 0 ° C or less are set to zero, temperatures above 0 ° C increase in value to a maximum of
+1 at 7 ° C, then begin decreasing, reaching zero again
and becoming negative after 14 ° C, eventually reaching
Copyright  2009 Royal Meteorological Society
Figure 2. Change in common lilac first leaf date by chilling accumulation level (red crosses are 1748 chilling hours and below, blue dots
are above 1748 chilling hours).
a minimum of −1 at temperatures higher than 25 ° C
(Richardson et al., 1974; Linvill, 1990; Table I). We then
matched these chill hour and chill unit values with the
corresponding phenology data at the same locations. For
all of the resulting phenology/chilling data sets (first leaf
and first bloom), we next applied K-means clustering
(two-cluster solution) to determine the best breakpoint in
the relationship between phenological date and chilling
accumulation. Lastly, linear regression equations were
calculated (and residuals assessed) for both resulting clusters (in all data sets) in order to quantify the differing
Int. J. Climatol. (2009)
DOI: 10.1002/joc
CONTINENTAL-SCALE PHENOLOGY: WARMING AND CHILLING
Figure 3. Change in common lilac first bloom date by chilling
accumulation level (red crosses are below 1748 chilling hours, blue
dots are 1748 chilling hours and above).
Table I. Chill unit calculation for each hour spent at a specific
temperature (constant = π × 2/28, Sine is computed in radians;
Linvill, 1990).
Temperature range
0 ° C or less
Greater than 0 ° C, up to 25 ° C
Greater than 25 ° C
Calculation method
Chill unit = 0
Chill unit = Sin
(constant × temperature)
Chill unit = −1
relationships between chilling accumulation and phenological data. We used scatter plots to graphically display
the overall relationships.
In order to provide additional information to put the
results in context, we also calculated 1961–1990 average annual accumulated chilling hours (received between
1 October and 1 February) for COOP stations in the study
area (with at least 25 years of data available over this
30-year period), and examined individual stations for any
trends in chilling hour accumulation over the 1956–2003
period. Further, we calculated the average timing (calendar date) of the relationship breakpoint between phenological date and chilling hour accumulation, as well as
its variation by year and location, over the 1956–2003
period.
3.
Results
Scatter plots, K-means clustering, and regression analyses
did not indicate any strong or significantly changing
relationships among chill unit accumulation and first
leaf/first bloom date; therefore, no further analyses were
conducted with chill units. The K-means clustering
analyses did indicate a break in the relationship between
chilling hour accumulation and phenological date at
Copyright  2009 Royal Meteorological Society
1748 chilling hours for both the first leaf and first
bloom phenology/chilling data sets (Figures 2 and 3).
For station/years that reached this chilling accumulation
level, the 1956–2003 study area-wide average date that it
was achieved was 13 January, with averages at specific
locations varying from 21 December to 20 April, and
the overall study area yearly averages ranging from 28
December to 14 February.
The regression equations showed changes for both
events in the relationship between accumulated chilling
hours and phenology (dates get earlier as chilling gets
less) for the clusters containing chilling accumulations
above the 1748 threshold level (slopes from linear
regression equation of −5.0 days/−100 chilling hours
for first leaf and −4.2 days/−100 chilling hours for first
bloom). For the clusters of both events with chilling
accumulations below that level, the rate at which the
phenology advances is greatly reduced (slopes from linear
regression of −1.6 days/−100 chilling hours for first leaf
and −2.2 days/−100 chilling hours for first bloom), as
suggested by the chilling theory (previously discussed).
All regression slope values were significant as per the ttest at α = .0005. Residual distributions for all regression
equations were not significantly different from normal,
with α values >.10 as per the K–S test with Lilliefors
significance correction. None of the residuals showed
any coherent spatial patterns; however, all four sets
were correlated with their corresponding phenological
dates.
The average study area-wide chilling accumulation
over the 1956–2003 period was 2235 h, with overall
yearly averages varying from 2082 to 2415 h. Chilling
accumulation varied much more rapidly in the southern portions of the study region (Figure 4). A small
number of locations (28) showed significant changes
in chilling accumulation over the 1956–2003 period,
with some indication of regional trends toward less
chilling in Washington State, California, and Arizona,
and more chilling in interior portions of the study
area.
4.
Discussion
The residual correlations suggest that follow-up work
should consider non-linear options for describing the relationship between chilling accumulation and first leaf/first
bloom date. Our results agree with much more extensive studies that show on-going reductions in chilling
accumulations (projected to continue throughout this century) within the fruit growing regions of California (Baldocchi and Wong, 2008; Luedeling et al., 2009). Yet,
possible chilling accumulation trends in other regions
may also be worth examining in detail, along with
an assessment of the impact of topography on this
variable.
Overall, the encouraging results for common lilac
suggest that similar continental-scale phenological measurements could facilitate a better understanding of
Int. J. Climatol. (2009)
DOI: 10.1002/joc
M. D. SCHWARTZ AND J. M. HANES
References
Figure 4. Average 1961–1990 chilling hour accumulation (base 7.2 ° C,
received between 1 October and 1 February) for stations in the Western
United States study area with at least 25 years of temperature data over
the averaging period.
relationships among chilling requirements, phenological response, and springtime warming for other species.
Further, such data, because they would provide plants
species’ responses across large portions of species geographic ranges, will facilitate deeper understanding of the
full range of plant–environment responses and consequently foster the development of more robust phenological models.
As we have shown how important chilling considerations are for evaluating the impacts of likely future
warming on plant species, several important follow-up
plant ecology questions should also be addressed in future
studies using the same general methodology: (1) Are the
chilling requirements for a species the same across its
entire range? (2) Do species adapt to warming conditions by changing their chilling requirements? (3) How
much variation is there among species chilling requirements within the same community? Such investigations,
as facilitated by continental-scale phenological data sets
being developed by the USA National Phenology Network (http://www.usanpn.org), will be essential for the
understanding of (and eventually consideration of possible adaptations to) the coming impacts of climate warming on temperate plant communities.
Acknowledgements
We are grateful for advice and comments from I. Chuine
and J. R. Strickler.
Copyright  2009 Royal Meteorological Society
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