Article

Progress in Physical Geography

123
Plant phenology and climate The Author(s) 2015
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change: Progress in methodological DOI: 10.1177/0309133315578940
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approaches and application

Jennifer M. Fitchett
University of the Witwatersrand, South Africa
Stefan W. Grab
University of the Witwatersrand, South Africa
Dave I. Thompson
South African Environmental Observation Network (SAEON), South Africa
University of the Witwatersrand, South Africa

Abstract
Phenology, the timing of annually recurrent reproductive biological events, provides a critical signal of climate
variability and change effects on plants. Considerable work over the past five decades has quantified the
extent to which plant phenophases are responding to local changes in temperature and rainfall. Originally
undertaken through the analysis of ground-based phenological observations, the discipline has more recently
included phenophase indicators from satellite images and digital repeat photography. With research advances
it has become evident that the responses of plant phenology to climate variability and change are both
location- and species-specific. The extent to which plants are affected by changes in temperature and rainfall,
their intrinsic adaptation capacity, will ultimately determine the potential for sustained ecological stability and
food security. We review methodological approaches to plant phenological-climate change over time,
analyse the regions and phenophases for which climate variability demonstrates a clear causal role, and finally
reflect on the applications of phenological climate change investigations in broader biogeographical contexts.

Keywords
Phenology, climate variability, climate change, plant responses, global trends

I Introduction life cycle events (Parmesan and Yohe, 2003;

Primack et al., 2009a; Rosenzweig et al.,
Plants exist in their current locations as a conse-
2008). Such changes are potentially proble-
quence of habitat selection and incremental
matic: economically in terms of agricultural
adaptation to environmental conditions best sui-
ted to their requirements for survival (Hegland
et al., 2009; Walther et al., 2002). However,
Corresponding author:
under rapid climate change, the suitability of
Stefan W. Grab, School of Geography, Archaeology and
these habitats inevitably changes. This mani- Environmental Studies, University of the Witwatersrand,
fests as a local species response, such as a Johannesburg, Private Bag 3, Wits 2050, South Africa.
change in range, abundance or in the timing of Email: stefan.grab@wits.ac.za

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2 Progress in Physical Geography

Figure 1. Global distribution of plant phenology research outputs based on publications.

production and other ecosystem services, and
ecologically through disrupted ecosystem func-
tioning, with the potential for large numbers of
species mismatches and extirpations (Hegland
et al., 2009; Primack et al., 2009a; Visser and
Hollerman, 2001).
Phenology refers to the study of the timing
of recurrent biological events, the causes of
their timing with regard to biotic and abiotic
forces, and the interrelationship among phases
of the same or different species (Badeck
et al., 2004: 295), and includes events such as
leaf unfolding, bud-burst, full bloom, harvest
and leaf fall (Cleland et al., 2012; Van Vliet
et al., 2003). The annual initiation of phenologi-
cal events is driven predominantly by climatic
shifts associated with the change of seasons,
rather than by intrinsic controls (Badeck et al.,
2004). These phenological responses are thus
arguably the most accurate and easily measured
signature of the impacts that changing tempera-
ture and rainfall have on flora (Badeck et al.,
2004; Cleland et al., 2012; Van Vliet et al.,
2003). The magnitude of phenological shifts is
dependent on the rate of climate change in a par-
ticular region and the species response mechan-
isms (Cleland et al., 2012; Zavalloni et al., 2006).
If adaptation to climate change is to succeed, a
comprehensive understanding is required of
the effects that climate change over the past
century has had on as many plant and animal
species, and in as many locations (Figure 1),
for which historical data are available (Led-
neva et al., 2004; Miller-Rushing et al., 2008).
Here we review progress made in various
approaches to the study of phenological

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Fitchett et al.
responses of flora to climate change. We review
current data collection methods: (i) ground-
based historical observations; (ii) satellite
imagery; (iii) digital repeat photography; and
(iv) phenological modelling. Study targets are
then critically compared, including regional
location, plant type and phenological stage.
Thereafter, we detail the species- and
location-specificity of phenological responses
to climate variability and change, and resul-
tant species mismatches within ecosystems.
Finally, we outline current applications of phe-
nological climate change research, specifically
in generating biodiversity indices and climate
models.
II Approaches to obtaining
phenological data
1 Ground-based observations
The predominant approach to phenological data
collection is sourcing historical, ground-based
records of the timing of annually recurrent
events for a particular species and location.
These date back to the Kyoto Cherry Festival
records from 1300 AD and grape harvest
records dating back to 1480, and continue to the
present day through the diaries and log books of
naturalists, and phenology networks and gar-
dens (Ledneva et al., 2004; Meier et al., 2007;
Primack et al., 2009b). Some of the earliest
studies concerned with climate change impacts
on plant phenology investigated the effect of
water stress on tree phenology in Costa Rica
(Reich and Borchert, 1984), and the role of cli-
mate warming on inducing earlier budburst in
the United Kingdom (Cannell and Smith,
1986). The majority of the methods used and
themes raised in these pioneering studies con-
tinue to be incorporated into contemporary phe-
nology research (Schwartz, 2013). The focus
then shifted to analysing longer climate and
phenology records: Sparks and Carey (1995)
determined contemporary climate change sig-
nals from the 200-year Marsham Record; Fitter
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3
et al. (1995) examined the relationship between
first flowering dates and temperature changes in
England (19541989); and Amano et al. (2010)
explored a 250-year record of first flowering
dates of 405 species in the UK.
The volume of research on phenological
responses to climate change increased during
the 1990s (Figure 2), permitting comparisons
between both study sites and subjects. These
comparisons highlighted the extent to which
plant and animal phenological responses to
local climate change are both species- and
location-dependent (Kramer et al., 2000; Men-
zel et al., 2006a). The cogency of these findings
is discussed later, but these comparisons
resulted in a considerable expansion of the
sub-disciplines of biogeography, agrometeorol-
ogy and climate change science, with tangible
value realized in studying as many species in
as many locations as possible (Cleland et al.,
2012; Fitchett et al., 2014a; Rotzer and
Chmielewski, 2001; Schwartz et al., 2006; Van
Vliet et al., 2003). This has most recently been
facilitated through citizen science programmes,
such as Project Budburst, which entails the
compilation of large multivariate datasets and
improves citizen awareness of the value of
phenology records, as well as the establishment
of phenology networks across the United States
and Europe (Mayer, 2010; Polgar and Primack,
2013; Wang et al., 2014).
Shifts in plant phenology over the past half-
century average less than one day per year, so
necessitating consistent daily monitoring of
species to ensure accurate and reliable pheno-
phase dates (Menzel, 2002; Miller-Rushing
et al., 2008). Long and rigorous datasets are thus
required to detect phenological shifts within
natural variability (Menzel, 2002). However,
this temporal resolution is seldom achieved
from farm records or phenological gardens,
where daily observations are not always possi-
ble or guaranteed (Ledneva et al., 2004). In the
case of naturalist diaries and citizen science
programmes, records reflect personal interest
4 Progress in Physical Geography

Figure 2. Increase in the number of publications per method of phenological data collection until 2013.
Publication numbers are based on an exhaustive Google Scholar search with publication period grouping
parameters, and cross-checked against Web of Knowledge and Science Direct.

and often include changing temporal and spa-
tial measurement components, and may conse-
quently have considerable gaps (Ledneva
et al., 2004, Mayer, 2010). Where records are
complete, they are often collected by multiple
observers (cf. Abu-Asab et al., 2001), and so
the consistency between observers, their level
of commitment and associated frequency of
observations, and the yardsticks against which
they determine the various life cycle
events, can lead to considerable data irre-
gularities (Gordo and Sanz, 2005; Sparks
et al., 2000). This highlights a further concern,
that of the definition and delineation of indi-
vidual phenological events. Events such as
flowering, leaf unfolding and colouration rep-
resent significant changes in the appearance of
a plant, yet it is more challenging to determine
the exact timing of the first leaf or flower, or
the precise moment when a tree or orchard
has reached a particular percentage bloom
(Menzel, 2002; Miller-Rushing et al., 2008).
This is important where the transition between
two or more phenophases occurs within a few
days. It is also possible for a single observer
to recognize these events inconsistently
between years, but uniformity in observations
becomes increasingly difficult where multiple
observers are involved (Miller-Rushing et al.,
2008). Emphasis has therefore been placed
on using multiple datasets covering more than
one location, so overcoming much of the sta-
tistical noise arising from observational incon-
sistencies (Sparks et al., 2000).
A crucial part of the analysis of ground-based
phenological and climate data is the assessment
of any errors and limitations associated with the
collection of data. However, long-term pheno-
logical records are too sparse to justify exclud-
ing imperfect records (Ledneva et al., 2004;
Miller-Rushing et al., 2008; Sparks and Carey,
1995). Rather, all available phenological
records should be critically examined and
assessed for their response to climate variability
and change. To facilitate an improved collection
of ground-based phenological data, phenologi-
cal networks are increasingly developing
detailed observation frameworks, which when
used by volunteers, decrease some of the poten-
tial error (Van Vliet et al., 2003).

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Fitchett et al.
2 Satellite remote sensing
With the advent of satellite remote imaging in
the 1970s (Figure 2), and the development of
Advanced Very High Resolution Radiometer
(AVHRR) technology in 1981, an additional
approach towards studying phenological
responses to climate change became available
through measuring leaf reflectance (Stockli and
Vidale, 2004). Satellite data have the advantage
of providing multi-decadal records of plant phe-
nology across larger spatial scales than ground-
based observations, and include observations for
regions where ground-based records are logisti-
cally challenging or impossible (Schwartz,
1999; Stockli and Vidale, 2004). Although prob-
lems in consistency with ground-based observa-
tions exist, phenological research development
increasingly resolves these problems (Shen
et al., 2014). The AVHRR imagery in the near
infrared and red-visible spectra enables the cal-
culation of the Normalized Difference Vegeta-
tion Index (NDVI; Pettorelli et al., 2005;
Schwartz, 1999), which allows for the identifi-
cation of sudden increases and decreases in
regional greenness and which is interpreted
as the beginning and end of the growing season.
It has also effectively been used to determine the
length of the green (vegetative or growing)
season, and the timing of the period of maximum
vegetation in which peak photosynthetic activity
occurs (Pettorelli et al., 2005; Schwartz, 1999).
The global to regional scale of satellite ima-
gery is consistent with many of the associated
climatological drivers, allowing for synoptic-
scale analyses of phenological trends, and spa-
tially relevant studies on the effects that the El
Nino Southern Oscillation (ENSO) and North
Atlantic Oscillation (NAO) have on phenology
(Anser et al., 2000; Broich et al., 2014; Van
Leeuwen et al., 2013; Zhang et al., 2003). This
scale is also more suitable for global climate
models, where species-level information is too
detailed for seamless inclusion (Morisette
et al., 2009). These benefits were first highlighted
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5
in the application of NDVIs for establishing the
productivity of African grasslands, Indian tropi-
cal forests and Chinese agriculture (Dethier,
1974; Justice et al., 1985; Tarpley et al., 1984).
Academic arguments have continued to empha-
size the necessity for phenological studies at
regional to global scales (Figure 1); to improve
the understanding of phenological processes, to
determine the impacts of increasing climate
variability and on-going climate change on phe-
nology, and to improve the integration of pheno-
logical findings into climate and ecological
models (Pettorelli et al., 2005; Schwartz and
Reed, 1999; Stockli and Vidale, 2004).
The physiological and statistical validity of
NDVI-derived green indices remains of con-
cern; whilst positive NDVI values accurately
represent the increase in greening across a
region, it is difficult to identify specific leafing
stages for a particular species, and so NDVI
may represent mean conditions with a variance
that is too large to be of value in identifying
start-points of spring for individual and varied
species (Stockli and Vidale, 2004). Conse-
quently, several studies have compared NDVI-
derived findings with phenology models and/
or available ground-based phenological obser-
vations (Badeck et al., 2004; Chen et al.,
2005; Schwartz and Reed, 1999; Stockli and
Vidale, 2004; White et al., 2009). NDVI results
correlate well with modelled phenological data
for the eastern United States (Schwarz and
Reed, 1999), and satellite observations for Eur-
opean phenology closely agree with the ground-
based observations from the European Phenolo-
gical Network (Stockli and Vidale, 2004).
NDVI measures for the green-up (leaf
unfolding) and brown wave (autumn leaf col-
ouring) most closely correlate with the
ground-level phenological stages of 50% leaf
unfolding and 50% leaf colouration in eastern
China (Chen et al., 2005). Comparisons among
NDVI, phenological model outputs and ground-
based observations have also contributed to an
improved understanding of the regions and
6 Progress in Physical Geography
species for which NDVI indices are most accu-
rate, and for which the most informative data
can be retrieved (Schwartz and Reed, 1999).
The temporal frequency of AVHRR imagery
for specific regions is also of concern (Justice
et al., 1985; Morisette et al., 2009). With a min-
imum imaging frequency of 24 hours, and days
with cloud cover preventing NDVI calculations,
the timing of phenological events has an upper
accuracy limit of approximately one week (Jus-
tice et al., 1985; Morisette et al., 2009; Schwartz
and Reed, 1999). With ground-based observa-
tions revealing global phenological shifts span-
ning fewer than 10 days per decade, such error
margins could greatly over- or under-estimate
these changes (Schwartz and Reed, 1999). Such
concerns have limited the use of TM/ETM
(Thematic Mapper and Enhanced Thematic
Mapper) data from Landsat imagery, which
whilst able to provide improved spatial resolu-
tion that facilitates comparison with ground-
based observations, does not improve the tem-
poral frequency from that of AVHRR (Fischer
et al., 2006; Melaas et al., 2013). The combina-
tion of AVHRR data and Landsat images may
simultaneously be able to address both concerns
(Melaas et al., 2013).
The greatest concern regarding the applica-
tion of satellite imagery in phenology involves
the use of AVHRR, which was not originally
intended for land and specifically vegetation
applications, but rather for monitoring phenom-
ena such as cloud detection and ice breakup
(Latifovic and Pouliot, 2007; Moulin et al.,
1997; Zhang et al., 2003). Since 2000, AVHRR
has increasingly been replaced by higher spatial
resolution MODIS imagery, with the Enhanced
Vegetation Index (EVI) replacing NDVI
(Penuelas et al., 2004; Pettorelli et al., 2005).
This, however, raises the further issue of consis-
tency of data resulting from differing methodol-
ogy. In a study using 10 different methods to
measure phenology from satellite imagery for
a single location, White et al. (2009) reported
differences in results of up to 60 days. Thus,
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whilst improvements in satellite technology
allow for more accurate measures of phenologi-
cal events, they do not support comparison
among studies, regions and time periods due
to differing in the level of accuracy (White
et al., 2009). However, once a more robust
approach to using satellite imagery has been
achieved, it should offer considerable value to
the study of plant phenology, particularly when
used in combination with ground-based obser-
vations and models (Cook et al., 2005; Mori-
sette et al., 2009).
3 Digital Repeat Photography
Digital Repeat Photography (Sonnentag et al.,
2012), also referred to as Near Surface
Remote Sensing (Polgar and Primack, 2011;
Wingate et al., 2008), is the most recent addi-
tion to the suite of methods used in phenolo-
gical data collection (Figure 2), and one that
most successfully addresses the shortfalls of
both ground-based observations and satellite-
derived data. Using regularly captured images
from digital cameras, analysis of oblique views
of vegetation can provide temporal information
concerning the onset and duration of seasons
through their associated phenophases (Sonnen-
tag et al., 2012). The extraction of numeric
Red-Green-Blue (RGB) colour channel bright-
ness information from the digital images facil-
itates phenological analysis for a region of
interest through colour indices such as excess
green, which allow for the timing of canopy
green-up and green-down to be deter-
mined (Richardson et al., 2009; Sonnentag
et al., 2012; Wingate et al., 2008). Through the
inclusion of additional colour indices, addi-
tional phenophases can be determined, such
as the autumn red peak for deciduous forests
(Richardson et al., 2009). The information from
these colour indices best allows for an accurate
determination of the start, end, peak and dura-
tion of the growing season (Richardson et al.,
2009; Wingate et al., 2008).
Fitchett et al.
Digital Repeat Photography has the advan-
tage over remote sensing by retaining species
and location-specificity in observations, whilst
also recording data at a finer and more consis-
tent temporal resolution than ground-based
observations can feasibly achieve (Polgar and
Primack, 2011; Richardson et al., 2009).
Furthermore, it removes the logistical con-
straints of cloud cover for satellite images, and
of consistency, continuity and objectivity in
ground-based observations (Polgar and Pri-
mack, 2011; Sonnentag et al., 2012). Many out-
door webcams already unofficially record
phenological data; these data can be collected
and analysed at minimal cost, even where cam-
eras need to be installed (Richardson et al.,
2007; Wingate et al., 2008). The exact position
of fixed-point cameras is usually known, thus
facilitating both ground-truthing and integration
with data from the nearest weather station
(Sonnentag et al., 2012). Possibly the greatest
advantage over ground-based observations is that
these photographs comprise a permanent record,
which can be re-checked and re-used, thus reduc-
ing single-observer bias (Richardson et al., 2007).
The application of Digital Repeat Photography
to plant phenology has tremendous potential, par-
ticularly when combined with satellite and
ground-based observations (Wingate et al.,
2008). This is currently being facilitated through
the development of websites that digitally quan-
tify colour change in and between images, whilst
enabling comparison with meteorological data
(Bradley et al., 2010a, 2010b). More recent web-
sites facilitate the synthesis of webcam data with
MODIS satellite imagery (Bradley et al., 2010a,
2010b; Klosterman et al., 2014). The develop-
ment of the Phenocam network, operating
together with the United States National Phenol-
ogy Network (USA-NPN), is working to increase
the use of these technologies, and make repeat
photography phenological data available for
North America (Klosterman et al., 2014).
Combining the benefits of satellite imagery
and digital repeat photography, unmanned
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7
aerial vehicles (UAVs) as tools for phenological
data collection offer a third means of remote
sensing. These relatively low-cost small aerial
vehicles are controlled remotely, and are able
to carry imaging hardware (Anderson and Gas-
ton, 2013; Berni et al., 2009). Whilst further
developments need to be made to improve
image quality through overcoming environmen-
tal conditions, increasing the flight time, and
facilitating the transport of larger numbers of
sensors, this technology has the potential to
function as another useful source of phenologi-
cal data (Anderson and Gaston, 2013).
4 Phenology models and experiments
Phenology models (Figure 2) are mathemati-
cal approaches that simulate phenological
responses to climate change (Cook et al.,
2005). Their aim is to use commonly available
meteorological variables to project pheno-
phase responses with minimal error margins
(De Melo-Abreu et al., 2004; White et al.,
1997); these are often tested against either
ground-based observations or satellite-derived
data in order to determine their accuracy (De
Melo-Abreu et al., 2004; Zavalloni et al.,
2006). Many models are developed with the
specific aim of projecting future phenophase
shifts for a particular species. These include
projecting the flowering dates of five species
of olives in Cordoba (Spain), based on chilling
and heating requirements (De Melo-Abreu
et al., 2004); and the model PHENOM, devel-
oped using both NDVI data and growing date
summations, as used by Cook et al. (2005) to
predict the future impact of the NAO on
green-up in mixed and boreal forests
across Europe. They also include simulations
developed to understand past phenological
responses to climate variability, as undertaken
for cherries in Michigan (USA) (Zavalloni
et al., 2006).
Mathematical models of plant phenological
events fall into three categories: statistical
8 Progress in Physical Geography
(empirical) models; mechanistic models; and
theoretical models, which are discussed in detail
by Zhao et al. (2013). Statistical models corre-
late the timing of phenophase events and the
concurrent climate conditions. Whilst tradition-
ally assuming linear relationships between these
climate variables and phenophases, more accu-
rate phenological projections are currently
being explored through the use of multiple
regression models and non-linear correlation,
particularly in regions such as alpine environ-
ments where the possibility for phenological
responses, rather than extinction, are already
limited (Iler et al., 2013; Richardson et al.,
2013; Zhao et al., 2013). Mechanistic models
explore the biological processes that statistical
models ignore, in the attempt to replicate the
causeeffect relationships between environ-
mental changes and the onset of phenological
events (Zhao et al., 2013). This approach uses
the behaviour of climate variables, and typically
includes onset models, such as chilling day
models, to determine the termination of dor-
mancy (Richardson et al., 2013; Zhao et al.,
2013). Theoretical models analyse the plants
physiological costbenefit relationships, mod-
elling the influence of climate on, for example,
the carbon balance and hormone intake (Zhao
et al., 2013). All three modelling approaches are
weakened by an incomplete understanding of
the dynamics of climatephenology relation-
ships, particularly under conditions of uncertain
climate change (Richardson et al., 2013; Zhang
et al., 2003).
Phenological models differ from methods of
phenological data collection in that they do not
rely on the availability of phenology and cli-
mate data spanning several decades, except
when testing models. Only an historic or pro-
jected climate record is required to calculate a
likely phenological response, and with a greater
number of weather stations than phenological
records globally, this potentially allows for
more phenological climate change studies.
Although these inferred phenology records
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cannot be used to determine the phenological
response to climate change over time in cases
where they inherently assume these relation-
ships, they can, and do, contribute significantly
to the inclusion of phenology into climate mod-
els and biodiversity indices (Morisette et al.,
2009; Schwartz, 1999). One such phenology
model, constructed using commonly available
meteorological and climate data, was used to
predict the onset of greening for two biomes
in the United States (White et al., 1997). When
the results were compared with satellite data,
mean errors of 7.2 days for deciduous broadleaf
forest and 6.3 days for grasslands were
observed. These errors can obscure the start date
of the season by up to a week, which, given the
current rates of phenophase change averaging
2.3 days per decade (Parmesan and Yohe,
2003), could render such data meaningless.
Furthermore, within the deciduous broadleaf
forest and grassland biomes, species-specific
phenophase shifts would be averaged, conse-
quently accounting for a further generalization
of data shared by models and satellite images,
and which would thus not be accounted for.
However, through providing estimates of phe-
nological shifts for regions where only climate
data are available, these models provide a cru-
cial first step in assessing the broad-based eco-
system response (White et al., 1997).
Mathematical phenology models attempt to
address existing questions concerning climate
change impacts on phenology. The regional
phenology model developed by White et al.
(1997) integrates spring green-up and
autumn brown-up dates with synoptic-level
climate changes. This 20 km  20 km resolution
model has a maximum average error of 1014
days (at 95% confidence), and differentiates
between the driving factors of both phenophases
in deciduous broadleaf woodland and grassland
biomes (White et al., 1997). In an attempt to
interpolate breaks in a three-century dataset for
determining periods of maximum phenological
change, Rutishauser et al. (2007) developed
Fitchett et al.
a substitutable spring phenological value
(Spring Plant) as a weighted average of the
mean flowering dates for apple and cherry, and
the mean budburst for beech in Switzerland.
Such mathematical models are often compared,
so as to determine the most robust model for
a particular plant and region (Crepinsek and
Kajfez-Bogataj, 2006).
Phenological experiments are shorter term
phenological observations made in an environ-
ment in which the environmental factors are
controlled, and range from field experiments
to ones undertaken in highly controlled green-
houses (Kramer et al., 2010; Reyer et al.,
2013; Wolkovich et al., 2012). They are under-
taken to explore the mechanistic plant responses
to specific environmental changes and forcings
(Laube et al., 2014; Morin et al., 2010). Whilst
these experiments can never account for all
environmental variables, their ability to deter-
mine the onset of a climatic change facilitates
a more accurate attribution of a phenophase
response (Dunne et al., 2003; Morin et al.,
2010). Experiments are favoured over ground-
based observations for short-term climatic or
environmental events, which result in dispro-
portionately large phenophase shifts, such as
extreme events (Reyer et al., 2013). Through the
use of experiments, the short-term response to
an extreme event can be distinguished from the
long-term phenological trend (Reyer et al.,
2013). A second application of experiments is
in testing the significance of previously over-
looked environmental drivers, such as humidity,
snow cover and frost (Dunne et al., 2003;
Inouye, 2008; Laube et al., 2014). Through
experimentally controlling for these environ-
mental drivers, their impact on phenophase tim-
ing can conclusively be tested (Laube et al.,
2014; Morin et al., 2010). However, caution is
required, as when comparing observational
records with those from experiments, signifi-
cant differences may be reported and thus
decrease the value of long-term modelling
(Dunne et al., 2003; Wolkovich et al., 2012).
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9
III Selection of target species
and location
1 Spatial dynamics
Phenological responses to climate change are glo-
bal phenomena (Figure 1), yet the extent of these
responses is significantly varied across regions
(Table 1). The poles are warming considerably
faster than the equatorial regions, and changes
in both atmospheric and ocean circulations have
considerably varied impacts on regional climates
and resultant plant responses (Beaubien and Free-
land, 2000; Hye et al., 2007; Walther et al.,
2002). Whilst regional climate variability is in
part responsible for the species- and location-
specific nature of changes in phenological events,
it is important to identify similarities among
regional climate drivers (Parmesan, 2007).
Tropical regions are least suited to phenologi-
cal studies given their weak seasonality and the
predominance of evergreen forests for which sea-
sonal green waves are particularly difficult to
detect (Corlett and Lafrankie, 1998). However,
whilst temperature and incoming solar radiation
are relatively uniform throughout the year, con-
siderable fluctuations in rainfall are common in
the tropics (Chapman et al., 2005; Corlett and
Lafrankie, 1998). Changes in rainfall are respon-
sible for the timing of leaf fall even in evergreen
trees, a physiological response to low rainfall
periods to compensate for water stress, and in the
timing of bud break and anthesis during
periods of higher rainfall in tropical dry forests
(Augspurger, 1981; Reich and Borchert, 1984).
Similarly, significant sub- and supra-annual var-
iations of plant growth and reproduction in asea-
sonal tropical Asian regions have been
established as a consequence of changes in water
availability (Corlett and Lafrankie, 1998). Solar
radiation is most uniform at the tropics, yet
Wright and Van Schaik (1994) argue that the
photoperiod may be significant in tropical plant
phenology, as the extent of cloud cover is varied.
High-latitude and high-altitude regions expe-
rience considerable seasonal fluctuations in
10 Progress in Physical Geography

Table 1. Summary of publications addressing the effect of climate change on phenology.

Year Phenological
Author published Time period Location Taxona responseb
Cannell and 1986 19211950 England Apple 79 d/ C
Smith
Fitter et al. 1995 19541989 Central England 267 species 46 d/ C
Sparks and 1995 17361925 England Multi-species 4 d/ C
Carey
Kramer 1996 Europe Fagus sylvatica 3.6 d/ C
Walkovszky 1998 18511930; Hungary Locust Tree 510 d/ C
19521981;
19831994
Bradley et al. 1999 19631947; Wisconsin, USA Multiple species 2.7 d/ C
19761998
Sparks et al. 2000 18751947 British Isles 11 plant species 210 d/ C
Chmielewski 2001 19691998 Europe White Birch, Sweet 5 d/ C
and Rotzer Cherry, Mountain
Ash, Alpine Currant
Chmielewski 2002 19612000 Europe Multi-species 6.7 d/ C
Germany Apple and Cherry 5 d/ C
Chmielewski 2002 19691998 Europe Multi-species 8 d/0.8 C
and Rotzer
Keatley et al. 2002 19401962 Australia Eucalyptus sp. 41.4 d/ C increase
5% ppt
decrease
Wielgolaski 2003 19951997 Norway Multi-species 46 d/ C
Chmielewski 2004 19612000 Germany Apple 4.6 d/ C
et al. Cherry 4.7 d/ C
De Melo-Abreu 2004 Modelled Portugal Olives 5.27.4 d/ C
et al.
Ledneva at al. 2004 19702002 Southern Goldthread 3 d/ C
Massachusetts, Spice Bush 0.45 d/ C
USA Wood Anemone 1.13 d/ C
Sparks et al. 2005 19802000 England Agricultural plants 412 d/ C
Crepinsek and 2006 19552000 Slovenia Hazel 8 d/ C
Kajfez-Bogataj Apple and Plum 46 d/ C
Lu et al. 2006 19502004 Beijing, China Peach 2.88 d/ C
Almond 2.19 d/ C
Lilac 2.43 d/ C
Acacia sp. 2.89 d/ C
Menzel et al. 2006c 19712000 Europe 542 plants 2.5 d/ C
Tao et al. 2006 19812000 China Wheat 2.98 d/ C
Estrella et al. 2007 19512004 Germany 20 agricultural plants 4.31 d/ C
Miller-Rushing 2007 19812005 Japan Cherry 29 d/ C
et al.
Miller-Rushing 2008 18521858; Massachusetts, 43 species 3.4 d/ C
and Primack 18781902; USA
19631993;
20032006
(continued)

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Fitchett et al. 11

Table 1. (continued)
Year Phenological
Author published Time period Location Taxona responseb
Wang et al. 2008 19832004 Northern China Wheat 3.4 d/ C
Cotton 0.66 d/ C
Gordo and Sanz 2009 19432003 Spain 21 species 8.21 d/ C
Beech 7.62 d/ C
Kalbarczyk 2009 19662004 Poland Granny Smith Apple 2.4 d/ C
Ground Cucumber 3.68 d/ C
Miller-Rushing 2009 19732006 Colorado, USA Delphinium sp. 6.17.1 d/ C
and Inouye
Primack et al. 2009a 8002007 Japan Cherry 35 d/ C
Primack et al. 2009b 19532005 Japan and Korea Prunus, Taraxacum, 4 d/ C
Camellia sp.
Amano et al. 2010 18911947 Central England 405 plant species 5 d/ C
(17532010
modelled)
Lambert et al. 2010 19752008 Colorado, USA Glacier Lilly 0.5d/day change
snowmelt;
1.2d/cm
precipitation
Beaubien 2011 19362006 Alberta, Canada 7 plant species 1.55.3 d/ C
Grab and 2011 19732009 South Africa Golden Delicious 4.2 d/ C
Craparo Apple 2.4 d/ C
Granny Smith Apple
Chen and Xu 2012 19862005 China Siberian Elm 2.8 d/ C
Darbyshire et al. 2012 19632009 Australia Apple and Pear 2.87.5 d/ C
Liu and Hu 2012 20002009 Tibetan Plateau Meadow species 8.17 d/ C
Steppe species 5.69 d/ C
Panchen et al. 2012 18402010 Greater 28 Piedmont species 2.7 d/ C
Philadelphia,
USA
Grewling et al. 2014 19962011 Poznan, Poland Oak 1.9 d/ C
Guo et al. 2013 19632008 Beijing, China Chestnut 2.4 d/ C
Bock et al. 2014 19852011 Guernsey 232 plant species 1.7 d/ C
Ellwood et al. 2014 19812011 Massachusetts, Cranberry 22.7 d/ C
USA
Fitchett et al. 2014b 19602010 Kerman & Citrus 0.16.5 d/ C
Shiraz, Iran
Park and 2014 19512009 Southeast USA >1700 species 3.4 d/ C
Schwartz
Polgar et al. 2014 18521860; Massachusetts, 43 woody plant 5 d/ C
20092013 USA species
Wang et al. 2014 19512000 30 European 50 species 3.8 d/ C
counties
a
Individual genera or species, up to a maximum of five, are listed where known.
b
All shifts are towards earlier dates.
Studies that do not present shifts in phenology resultant from changes in climate variables are excluded; only phenological
shifts of spring events (leaf unfolding, budburst or flowering) are reported.

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12
temperature, solar radiation and precipitation,
and the additional climatic drivers of snow
cover and snowmelt dates (Inouye and Wielgo-
laski, 2013; Kudo, 1991; Walker et al., 1995;
Wielgolaski and Inouye, 2013). Snowmelt con-
trols spring soil temperature and moisture, and
also has a direct effect on both leafing and flow-
ering phenology, and thus arguably has the
greatest impact in cold environments (Inouye
and Wielgolaski, 2013; Walker et al., 1995).
Shorter snow-free periods reduce flowering and
seeding, and encourage the production of vege-
tative rather than reproductive shoots (Kudo,
1991; Inouye and Wielgolaski, 2013; Oberbauer
et al., 2013). Recent studies on recorded snow-
melt dates report that these significantly influ-
ence phenology (Inouye et al., 2002; Saavedra
et al., 2003). These include an 11-day advance
in flowering dates following a two-week earlier
snowmelt date in Colorado (Dunne et al., 2003).
Similarly, a very strong correlation between
snowmelt and first flowering dates is found for
Colorado, where snowmelt dates accounted for
73.4% of phenophase shifts (Inouye, 2008).
The timing of snowmelt is dependent on tem-
perature and the volume of winter snow, and thus
responds more strongly to local temperatures,
driven by the amount of shade and wind to which
the snow is exposed (Inouye, 2008; Inouye and
Wielgolaski, 2013; Oberbauer et al., 2013).
Furthermore, in the Arctic, where snow cover
persists throughout the year, temperature has a
primary influence, whilst in sub-Arctic regions
with seasonal snow cover, rainfall is of greater
importance to the timing of phenological events
(Wielgolaski and Inouye, 2013; Wookey et al.,
1993). Despite the complexity of these drivers,
under extreme polar climate warming recorded
in recent decades, advances in spring onset in
high latitudes are already occurring at a more
rapid pace, and at lower heat sums, than phenolo-
gical shifts at lower latitudes (Hye et al., 2007;
Oberbauer et al., 2013).
Mid-latitude regions, with highly seasonal,
temperate conditions, enable the most accurate
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Progress in Physical Geography
attribution of climate variability to long-term
shifts in phenology (Chmielewski et al., 2004;
Cook et al., 2012; Schwartz and Reiter, 2000).
Whilst annual temperature, photoperiod and
precipitation are all important in controlling
plant phenology, the sub-annual periods during
which these factors are most significant, are not
necessarily uniform. Moreover, data for these
variables are generally easily available and
hence phenological response can, for the most
part, be accounted for (Badeck et al., 2004; Pol-
gar and Primack, 2013). The most difficult fac-
tor to account for when studying phenological
changes in the mid-latitudes is the risk of frost
damage, particularly where warmer spring tem-
peratures induce considerably earlier flowering
(Cannell and Smith, 1986; Fitchett et al., 2014b;
Inouye, 2008; Polgar and Primack, 2013; Wang
et al., 2014). Closely associated with daily min-
imum temperature, the effect of frost can more
easily be attributed to changes in phenological
events and yields than snowmelt dates, which
would need to be recorded separately (Rigby
and Porporato, 2008).
Further factors need to be considered at more
local scales; the first is the distance from major
water bodies, particularly if the coastline is in
close proximity to a major current of the thermo-
haline circulation (Beaubien and Freeland, 2000).
Whilst proximity to large water bodies has a mod-
erating effect on climate, changes in sea or inland
water temperatures, together with shifts in the
thermohaline circulation, strongly influence
regional climate variability/change and associ-
ated phenological responses (Beaubien and Free-
land, 2000). Secondly, the position of the study
region in relation to urban areas is critical given
the potential urban heat island effect and anthro-
pogenically controlled temperature, photoperiod
and water availability (Lu et al., 2006).
2 Phenological stage or event
Very few datasets span more than one phenolo-
gical event (Amano et al., 2010; CaraDonna
Fitchett et al.
et al., 2014; Gordo and Sanz, 2005). Conse-
quently, when obtaining a dataset for analysis
of phenological responses to climate change, a
site with data for a phenological stage that is
strongly climate-controlled is preferable (Beau-
bien and Freeland, 2000; Schwartz, 1999). Pre-
ference has been to study the initiation of spring
phenophases such as leaf unfolding, bud burst
and flowering, rather than autumn phenophases
such as fruit fall, leaf colouring and leaf fall
(Chmielewski and Rotzer, 2002; Cook et al.,
2012; Schwartz and Reiter, 2000; Wang et al.,
2014). Spring events often have a double tem-
perature control through chilling requirements
for the breaking of dormancy and a subsequent
warming requirement to induce a shift to the next
ontogenetic stage (Wang et al., 2014). Whilst this
requires more intricate analysis to distinguish the
two drivers, it is preferable to a combination of
intrinsic and extrinsic factors. Further, because
these events signal the end of the dormancy
period, they do not suffer from cumulative effects
of climate warming across the growing season
(Beaubien and Freeland, 2000; Chmielewski and
Rotzer, 2002; Nordli et al., 2008).
Leaf unfolding is a relatively easily distin-
guishable event and thus has considerable poten-
tial for use in both ground-based and satellite
observations. However, leafing is induced by
both intrinsic factors and external climate con-
trols (Pettorelli et al., 2005; Polgar and Primack,
2013; Schwartz et al., 2006). For evergreen trees
and deciduous trees with multiple leaf flushes
annually, the leaf unfolding date is triggered to
a greater extent by internal controls, such as car-
bohydrate deficits and water availability, only
indirectly associated with rainfall (Arora and
Boer, 2005; Stockli and Vidale, 2004; Zhang
et al., 2003). The timing of flowering is more
tightly controlled by climate, with a reliance on
winter temperatures for the fulfilment of chilling
requirements and spring warming to induce bud-
burst (Nordli et al., 2008; Sparks et al., 2000). Not
only are these climatic controls more robust, but
intrinsic controls have a lesser effect on
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13
flowering, with any deficits accommodated
through changes in leaf, shoot and root growth
(Arora and Boer, 2005; McCormack et al., 2014).
Given flowering as the preferable event for
studying phenological responses to climate
changes, it becomes necessary to assess the rela-
tive suitability of measured bloom stages (first
flowering, 50%, 75% or peak bloom). First
flowering dates, which capture the timing of the
first visible open flower, are often easiest to
record as they do not rely on human subjectivity
to establish when 50% or the majority of flowers
are open (Amano et al., 2010; Fitter et al., 1995).
However, errors arise during data collection if
first flowering occurs on a day or at a location
where observations were not made, or if that
flower is located above eye level (Miller-
Rushing et al., 2008). These first flowers are
less likely to be noticed than a later flower in
a more visible position. Intrinsic errors also
result from recording this single event rather
than a percentage floral extent: a single event
reduces the sample number, and consequently
could occur much earlier or later inter-
annually, during a period in which peak bloom
may remain relatively constant (Amano et al.,
2010; Fitter et al., 1995; Miller-Rushing et al.,
2008). First flowering could also be triggered
during brief favourable conditions sufficient
to cause a few buds to open, but be followed
by a cold period preventing peak bloom (Fitter
et al., 1995; Miller-Rushing et al., 2008). Thus,
for a more statistically accurate phenophase
date, with less likelihood of error or bias, esti-
mates of peak or 5075% bloom dates are pre-
ferred (Miller-Rushing et al., 2008).
IV Species and location-specificity
The magnitude of the phenological response to
climate change is dependent on the species;
whether warming, chilling, or both, are required
to induce a phenological event; the time period
during which climate is most influential; and
threshold temperatures for that species (Cleland
14
et al., 2012; Lambert et al., 2010; Parmesan,
2007; Visser and Holleman, 2001). For
instance, Chinese cotton flowering dates have
advanced by only 0.66 days/ C in Beijing,
whilst wheat grown in the same area has experi-
enced flowering advances of as much as 3.4
days/ C (Wang et al., 2008). Location-specific
phenophase shifts among trees of the same spe-
cies are also apparent, such as the earlier flower-
ing dates for granny smith apples (4.2 days/ C)
in South Africa (Grab and Craparo, 2011) than
in Poland (2.4 days/ C; Kalbarczyk, 2009). A
summary of species and location-specificity of
spring phenological responses to climate
change is presented in Table 1.
1 Species mismatches
Species- and location-specificity of phenologi-
cal responses to climate change affects individ-
ual plant species and regional ecosystems
(Stenseth and Mysterud, 2002). Overlaps in
time and space between predators and prey,
plants and pollinators, and species varieties for
cross-pollination, have evolved over long time
periods (CaraDonna et al., 2014; Durant et al.,
2007; Hegland et al., 2009; McKinney et al.,
2012; Stenseth and Mysterud, 2002). With vari-
able responses to climate change, between spe-
cies and locations, many of these overlaps
and species interactions are likely to weaken
(Durant et al., 2007; Lambert et al., 2010; Mem-
mot et al., 2007; Polgar and Primack, 2013).
Predator-prey and plant-herbivore mis-
matches have been observed in terrestrial envir-
onments, such as the winter moth currently
hatching up to three weeks earlier than the
unfolding of oak leaves, which are their primary
food source (Visser and Holleman, 2001). This
is owing to the winter moth taking its hatching
cue from warming temperatures, whilst the oak
tree has a chilling requirement for leafing
(Durant et al., 2007; Polgar and Primack,
2013; Visser and Holleman, 2001). Similarly,
with progressive advances in peak and first
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Progress in Physical Geography
flowering dates of nectar-providing plants, the
overlap between the appearance of broad-
tailed hummingbirds and their food is decreas-
ing, particularly at high latitudes (McKinney
et al., 2012). Even where both species take their
phenological cues from warming temperatures,
mismatches arise where the time period and
duration for which temperatures are important
differ (Lambert et al., 2010).
Mismatches also have an effect on pollina-
tion. Variable timing in the flowering of plants
and the availability of pollinators potentially
changing for both partners can considerably
decrease the likelihood of pollination and, con-
sequently, the quality and size of seed and fruit
yields (Hegland et al., 2009; Memmott et al.,
2007; Park and Schwartz, 2014; Thomson,
2010). This can be driven by changes in the tim-
ing and duration of flowering, and the quantity
of flowers produced alone, but is enhanced for
plants pollinated by insects rather than wind,
due to differences in the phenophases of these
insects (Hegland et al., 2009; Memmott et al.,
2007; Thomson, 2010). For plants pollinated
by insects, such mismatches would also result
in food supply, and the eventual extinction of
the pollinator (Kaiser-Bunbury et al., 2010;
Memmott et al., 2007; Park and Schwartz,
2014).
For cross-pollination of self-incompatible
species, an overlap in flowering time of dif-
ferent individuals is required to maintain both
yields and fundamental genetic diversity
(CaraDonna et al., 2014; Moghadam et al.,
2009). This becomes particularly problematic
in species such as cherries, where the flowering
duration is less than a week (Moghadam et al.,
2009). Mismatches in phenophases are of con-
siderable concern for species survival and for
that of their ecosystems (CaraDonna et al.,
2014; Memmott et al., 2007). However, Visser
and Both (2005) argue that these mismatches
may provide a necessary yardstick against
which to measure the magnitude of climate
change effects on plant survival. In addition,
Fitchett et al.
there may be a considerable under-reporting of
cases where mismatches are not found, given
that the species studied are responding in paral-
lel to climatic changes (Visser and Both, 2005;
Parmesan, 2007).
V Applications of plant phenology
research
Phenology has considerable potential to con-
tribute towards improving the academic disci-
plines that develop biodiversity indices and
climate models (Morisette et al., 2009). The dis-
cipline has also been used as a proxy for climate
change where phenological records extend back
further than climate records (Chuine et al.,
2004; Souriau and Yiou, 2012); in agricultural
management (Crepinsek and Kajfez-Bogataj,
2006; Menzel, 2002; Van Vliet et al., 2003); and
even in healthcare, addressing the influences of
phenological shifts on allergy-causing pollens
and disease-carrying insects (Luvall et al.,
2012).
1 Biodiversity indices
The development of biodiversity indices, which
allow for the health of ecosystems to be moni-
tored and managed, is critically important given
the risks of climate change to species extinction
(Dawson et al., 2011; Spano et al., 1999; Visser
and Both, 2005). Phenological observations
provide indicators of the extent to which plants
and animals are being affected by, and respond-
ing to, climate variability and change, and
increasingly form fundamental components of
broader ecosystem assessments (Crepinsek and
Kajfez-Bogataj, 2006; Dawson et al., 2011;
Kramer et al., 2000). Meta-analyses of the exist-
ing phenology literature aim to uncover glob-
ally coherent fingerprints (Parmesan and
Yohe, 2003: 37) of climate change impacts on
the phenology, location and distribution range
of plant and animal species, facilitating the
broad-based inclusion of phenology in
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15
biodiversity indices (Dawson et al., 2011).
However, even single-species studies are of
value, particularly if those species are highly
sensitive to climate change, and if the study
aims to contribute to the development of such
indices (Dawson et al., 2011; Spano et al.,
1999). Recent research suggests that invasive
species may be particularly tolerant to climate
change and climate impacts on their phenologi-
cal cycle, prompting further species-specific
studies for inclusion in biodiversity and ecosys-
tem adaptation assessments (Polgar et al.,
2014).
2 Climate models
Phenological shifts are driven predominantly by
climate variability and change, yet these shifts
will also have an impact on future climate
change through feedbacks to the atmospheric
system (Hogg et al., 2000; Penuelas et al.,
2009; Richardson et al., 2013). The timing of
leaf phenology (both leaf flush and senescence)
significantly alters the surface albedo, water
balance, carbon intake and canopy surface
roughness (Arora and Boer, 2005; Penuelas
et al., 2009; Richardson et al., 2013). The chal-
lenge lies in modelling leaf phenology to allow
future phenological changes to be included in
climate projection models (Arora and Boer,
2005; Hogg et al., 2000; Richardson et al.,
2013). Difficulty exists because the shifts in
plant phenology are driven, to a large extent,
by the same climate change that these models
attempt to project (Arora and Boer, 2005; Zhao
et al., 2013). This can be compensated for
through modelling leaf phenology based on the
plants carbon budget, rather than air tempera-
ture, thus preventing double counting. However,
considerably more information is required
across far greater spatial scales than is presently
available (Arora and Boer, 2005; Penuelas et al.,
2009; Richardson et al., 2012). Furthermore,
phenological records spanning multiple centu-
ries are increasingly used for reconstructing past
16
climates, which enables more accurate climate
modelling (Chuine et al., 2004; Meier et al.,
2007; Souriau and Yiou, 2012).
A challenge to modelling phenological
events and using them for climate projection
purposes is the influence of extreme climate
events, which are projected to increase in mag-
nitude and frequency (Jentsch et al., 2007;
Reyer et al., 2013). Both plant and animal phe-
nophases have been affected disproportionately
by the duration of extreme weather events such
as flooding, droughts, heatwaves and cyclones
(Jentsch and Beierkuhnlein, 2008; Jentsch
et al., 2007; Parmesan et al., 2000). These phe-
nological responses to extreme events often
obscure the long-term response to mean cli-
mate, and have the potential to influence subse-
quent phenological patterns over longer periods
(Jentsch and Beierkuhnlein, 2008; Rich et al.,
2008). Furthermore, the phenophase responses
to extreme events appear to be more compli-
cated than those of long-term mean climate
changes, with far greater significance of the tim-
ing and duration of temporal forcing (Friedl
et al., 2014), and a possible two-phase ecosys-
tem response following such events with the
dieback of larger vegetation but regrowth of
small shrubs (Rich et al., 2008). To enable
higher resolution climate modelling, these
extreme events need to be better modelled, the
responses of phenophases to these events better
understood, and the long-term interactions
between these responses and resultant micro-
climates explored (Reyer et al., 2013).
VI Looking ahead
Considerable work has been undertaken over the
past few decades to understand the location- and
species-specific phenological responses of plants
to climate variability and change. The most nota-
ble research gaps are spatial, including Africa,
South America and the Middle to Near East (Fig-
ure 1). The limited phenological research in these
regions is detrimental to the discipline as a whole,
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Progress in Physical Geography
as it restricts inter-regional or global-scale
comparisons. Furthermore, floral species ende-
mic to such understudied regions have yet to be
assessed for their climate change-related phe-
nological responses. Many of these areas
include less economically developed countries,
which are likely to be more adversely affected
by climate change due to their lower societal
adaptive capacity, and which additionally may
be very reliant on agriculture (Blanc, 2012;
Hegland et al., 2009).
Investigations of phenological responses to
climate change have expanded rapidly since the
first studies in the 1960s, most notably to
include advancing technologies such as satellite
and webcam imagery, and derived indices for
analysis (Schwartz, 1999; Sparks et al., 2005).
The application of NDVI and EVI from satellite
imagery allow for phenological analysis in
regions for which no ground-based phenologi-
cal data exist, thus enabling the aforementioned
research gaps to be addressed. Many of these
regions maintain web cameras, which would
likely have unintentionally captured images of
value to phenology studies. With relatively low
costs to initiate and maintain, webcams and
webcam networks provide possibly the best
method for future phenological data capturing,
as they facilitate a high temporal resolution,
broad spatial scale of inclusion and the possibil-
ity for both ground-truthing and digital compar-
ison with satellite imagery. The promotion of
citizen science also provides opportunities for
the continued expansion of ground-level obser-
vations to enhance existing records.
In addition to continued efforts to address
regional omissions, it is critical that high-
resolution temporal and spatial investigations
into climate influences on plant phenology be
prioritized. The majority of phenology studies
analyse the impacts of monthly to annual climate.
It is likely that the absolute dates of phenophase
shifts for a particular year are rather driven by cli-
mate deviations on a maximum scale of days.
Where phenological investigations currently
Fitchett et al.
work with daily minimum and maximum tem-
perature, plant thresholds are more likely deter-
mined by the most frequently occurring high or
low temperature in a period of days than a daily
peak reading that may have occurred for a period
of a few seconds to many hours. We propose that
future phenological investigations take greater
cognizance of meteorological conditions at the
same locality where plant phenology is measured,
and also consider a focus on plants grown at the
boundaries of their natural habitat (e.g. upper
limit of alpine plants), or in artificial environ-
ments such as cities. It is anticipated that as the
global climate continues to warm and experi-
ences greater temperature and precipitation
extremes, so our understanding of associated
plant phenophase responses will become increas-
ingly important in the context of future agricul-
tural planning and species conservation.
Acknowledgements
The authors wish to acknowledge the insightful com-
ments of the three reviewers, which assisted in
improving this manuscript.
Funding
This research received no specific grant from any
funding agency in the public, commercial or not-
for-profit sectors.
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