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phenological networks and flux
monitoring networks for the
purpose of understanding pat-
terns and processes controlling
carbon budgets across a broad
range of scales, explicit activities
to assess the impact of phenol-
ogy on ecosystem carbon bal-
ance are still somewhat lacking
within the carbon cycle commu-
nity. The reasons are clear: long-
term observations, otherwise
called ‘monitoring’ are not popu-
lar with those that sponsor re-
search in this area; three or five
year projects are the norm,
when in practice much longer
records are required to detect
long-term trends and their rela-
tionships to climatic drivers.
There is however, evidence for a
shift in attitudes. Keeling’s meas-
urements of atmospheric CO2
concentrations, that began in
1958, are an outstanding exam-
ple of the value long-term moni-
toring represents in the context
of a changing world (Nisbet,
2007). Moreover, continuous
eddy covariance measurements
of CO2 fluxes began in the early
1990s at a handful of sites. Every
year, more and more sites have
been added to FLUXNET, and
many of these are now providing
useful long term data not only
with regard to spatial patterns of
carbon uptake and release, but
also in relation to the influence
of phenology on carbon seques-
tration.
One example of a synergy be-
tween phenology and flux moni-
toring networks in Europe has
Why observe phenology
within FLUXNET?
Phenology is the study of the
timing of lifecycle events, espe-
cially as influenced by the sea-
sons and by the changes in
weather patterns from year to
year. The oldest phenological
records, observations of cherry
flowering at the Royal Court in
Kyoto date back to 705 AD, and
are still maintained to this day
across Japan where the Japanese
Meteorological Agency use these
data to provide weekly forecast
maps of expected blooming
dates (http://www.jma.go.jp/jma/
en/News/sakura.html). Robert
Marsham, the father of modern
phenological recording, was a
wealthy landowner and amateur
naturalist who recorded
"Indications of spring" in Nor-
folk, England, beginning in 1736.
His family maintained these re-
cords until the 1950s. In the
modern era, phenology has
gained a new impetus, as people
realize that such records, if sus-
tained over many years, can
reveal how plants and animals
respond to climate change.
Moreover, phenological events
such as the spring leaf-out and
the autumn fall exert a strong
control on both spatial and tem-
poral patterns of the carbon
cycle. Phenology also influences
hydrologic processes, as spring
leaf-out is accompanied by a
marked increase in evapotranspi-
ration, and nutrient cycling as
autumn senescence results in a
flush of fresh litter (nutrient)
input to the forest floor.
Phenology is a robust integrator
of the effects of climate change
on natural systems (Schwartz et
al., 2006; IPCC 2007), and it is
recognized that improved moni-
toring of phenology on local-to-
continental scales is needed.
Historically, phenological obser-
vations were a pastime of ama-
teur naturalists (e.g. the Mar-
sham family) and reliable records
were often dependent on the
skills and effort of the observer.
The increased demand for inter-
national co-operation and stan-
dardisation in this area led to the
creation of many large-scale
phenological monitoring net-
works such as the International
Phenology Garden (IPG) pro-
gram (http://www.agrar.hu-
belin.de/struktur/institute/pfb/str
uktur/agrarmet/phaenologie/ipg)
(founded in 1957), the Global
Phenological Monitoring (GPM)
program (http://www.agrar.hu-
belin.de/struktur/institute/pfb/str
uktur/agrarmet/phaenologie/gpm
) (established in 1998) as well as
the recently-established USA-
National Phenology Network
(USA-NPN)
(http://www.usanpn.org) and
associated regional networks
(e.g., http://www.nerpn.org).
These networks have focused on
developing standardized proto-
cols for phenological observa-
tions, and ensuring overlap be-
tween plant species found across
locations. Although there are
obvious advantages in creating
explicit linkages between these
Page 14
Keeping an eye on the carbon balance: linking canopy
development and net ecosystem exchange using a webcam
Lisa Wingate, Andrew D. Richardson, Jake F. Weltzin, Kenlo N. Nasahara and John Grace
occurred between the Tharandt
International Phenological Gar-
den (also one of the 24 GPM
gardens) and the nearby Car-
boeurope-IP site Anchor Station
Tharandt over the past 12 years
(Niemand et al., 2005; Grünwald
& Bernhofer, 2007). Using the
standard observations from both
networks it was demonstrated
that the appearance of the Mait-
rieb (May shoot) for Norway
spruce is correlated with annual
estimates of ecosystem gross
primary productivity (GPP) and
net ecosystem productivity
(NEP) (with the exception of the
extreme drought event of 2003
in Europe). This indicates that
the earlier appearance of shoots
potentially increases the length
of the growing season, leading to
a greater annual carbon seques-
tration. Mean March-April tem-
peratures were correlated with
the data of May shoot, indicating
a potential scalar for GPP and
NEP when coupled to longer
time-series from such IPG re-
cords. Similarly, an analysis cou-
pling budburst observations and
CO2 flux measurements at the
Howland (since 1996) and Har-
vard (since 1992) AmeriFlux
sites indicated that earlier bud-
burst resulted in greater spring-
time GPP (5 g C m-2 per 1 day
advancement of budburst date),
but these increases in carbon
uptake were offset by increases
in springtime ecosystem respira-
tion (RE), resulting in an uncer-
tain effect (not significantly dif-
ferent from zero) on springtime
cont. on page 15
resources (that are typically
scarce) and, as a consequence,
these observations are not pur-
sued at the majority of flux sites.
Several of the phenology net-
works include a substantial vol-
unteer or “citizen science” com-
ponent, wherein trained observ-
ers track the response of plants
using standardized protocols, on-
line data entry forms and visuali-
zations designed and streamlined
for the more casual observer
(e.g., UK Nature Watch, US
Project BudBurst and USA-NPN,
and the GLOBE project (Gazal et
al., in press). These networks of
observers represent a potential
bridge between phenological and
flux observations, in that data
collected by such “citizen scien-
tists” can be used to (a) increase
the density of observation sites
and species, (b) collect informa-
tion on presence/absence of
NEP (Richardson et al., in prepa-
ration).
Phenological Activities
within FLUXNET
At FLUXNET sites around the
world that overlook forests,
pastures, and wetlands, we have
the opportunity of establishing
precision measurements of
phenological events by simply
mounting networked digital
cameras (‘webcams’) and re-
cording daily (or even hourly)
images of the vegetation canopy,
as recommended by Baldocchi et
al. (2005). A recent FLUXNET
survey
(http://www.geos.ed.ac.uk/homes
/lwingate/webcam.html) has
uncovered at least 26 such web-
cams already ‘keeping an eye’ on
canopy development (Figure 1).
Although this network is in its
infancy, it appears to be growing
steadily, and already represents
some 58 site-years of combined
flux and webcam data. A large
number of these sites are in Asia
where the Phenological Eyes
Network was set-up in 2003 to
create a much needed validation
platform for remote sensing
products such as NDVI
(http://www.asiaflux.net/newslett
er/no21_2007.pdf). It is also
promising to learn that this num-
ber should continue to grow
with the addition of sites in the
US National Ecological Observa-
tory Network
(www.neoninc.org). However,
just as phenological gardens
must commit to observations in
excess of ten year periods it is
also necessary for this webcam
activity to maintain a long-term
perspective, especially when it
comes to unravelling the rela-
tionships between forest carbon
balance and phenology.
The opportunity presented to us
is clear: webcam measurements
at FLUXNET sites will reveal the
link between phenology and
carbon uptake; they will also
provide much-needed ground
verification of phenology prod-
ucts derived from satellite re-
mote sensing (e.g., MODIS).
The role of the phenology
network and citizen scien-
tists
Within FLUXNET a protocol for
phenological observations was
also created to harmonise
phenological observations across
flux sites
(http://www.fluxdata.org/DataInf
o/Dataset%20Doc%20Lib/FLUX
NET_phenophase_protocol.pdf).
However, initiation of such long
term monitoring requires a sus-
tained commitment of human
Page 15
Keeping an eye on the carbon balance cont. from page 14
Figure 1 Global distribution of flux sites with webcams (Agarwal et al., 2008)
cont. on page 16
webcam network presents a way
to directly link on-the-ground
observer records to remotely-
sensed data, and moreover to
link these to ecosystem physiol-
ogy measured with flux towers.
The growing webcam network
now represents a novel opportu-
nity to implement both regional
and global monitoring of phenol-
ogy at flux sites. Thus efforts to
extend the spatial coverage of
phenological observations at flux
sites through the simple addition
of cameras on towers are now
required within FLUXNET. In
time this network will not only
establish an archive of images
documenting seasonal and inter-
annual changes in forest phenol-
ogy, but also capture associated
snow, flowers or foliage unde-
tectable to remote sensing plat-
forms, and (c) ground-truth
observations from ‘near’ (e.g.,
camera, or eddy correlation) or
‘far’ remote sensing platforms
(e.g., AVHRR, MODIS). Devel-
opment of a volunteer program
for FLUXNET sites would
greatly strengthen tools available
for the interpretation of eddy
flux data.
Towards an international
canopy phenology camera
network
In situ phenological observations,
gas exchange and radiometric
signals at the same flux sites are
currently required for compari-
son with remotely sensed prod-
ucts. This is especially the case if
we are to understand the appar-
ent contradiction in findings
between the CO2, phenology
and remote sensing communities
with respect to the timing of
canopy green up and senescence
and how this relates directly to
changes in the atmospheric CO2
record, especially during spring
and autumn in the northern
hemisphere (e.g., Piao et al.,
2008). This webcam network
could soon be in a position to
test whether the start, maximum
and end of the growing season
derived from satellite NDVI data
really correspond to the actual
start, maximum and end of the
growth period of plants as ob-
served in flux sites. Thus the
Page 16
variability in forest function and
its potential impact on ecosys-
tem carbon balance in response
to long-term changes in climate.
This multi-scale monitoring of
phenology and net ecosystem
exchange of CO2 will enrich our
understanding and efforts at
modelling not only the impacts
of climate on phenology but also
the impact of phenology on
climate through feedbacks on
the carbon and energy cycle of
the planet. Moreover, it has the
potential to link the CO2 flux
community to the thousands of
amateur observers, many of
them school-children who will
become the next generation of
scientists.
As we have illustrated above,
webcams are an important way
of tracking canopy phenology.
The digital images when col-
lected at such regular intervals
can be easily assembled into
time-lapse movies such as those
in Box 1, providing an important
product for raising public aware-
ness on phenological and carbon
cycle research. The color infor-
mation of these very same im-
ages can also be analyzed to
retrieve information on canopy
development in both deciduous
and evergreen forests as de-
scribed in Box 1 and 2. If you
plan to mount a camera at your
flux site in the near future and
have any queries for the net-
work please do not hesitate to
contact us and we will do our
best to help get you started.
Acknowledgements
Many thanks to all those that
took the time to respond to the
recent survey on the phenology
Keeping an eye on the carbon balance cont. from page 15
BOX 1— Time-lapse animations of canopy development and net ecosystem exchange can illus-
trate the degree of coupling between the two signals and the additional influence of understorey
and snow cover on flux measurements. A number of such animations can be observed below and
at the following website (http://www.geos.ed.ac.uk/homes/lwingate/webcam.html). These observa-
tions were taken at flux sites within the Carboeurope-IP, Ameriflux and Asiaflux networks.
Figure 2 : Time-lapse movie links for the Howland Ameriflux site (http://www.forest.sr.unh.edu/richardson/Howland2007b.avi),
a Betula ermanii Cham. at the Takayama Asiaflux site (http://pen.agbi.tsukuba.ac.jp/~TKY/summary/dc/dc_2007_digest_TKY__y18bb/)
and the Hainich Carboeurope-IP site (http://xweb.geos.ed.ac.uk/~lwingate/Hainich_forest_Flux_phenology.avi)
cont. on page 17
activities within FLUXNET. We
also thank Technical Computing
Microsoft (www.microsoft.com/
science).
Literature
Agarwal, D., Humphrey, M., van Ingen,
C., Beekwilder, N., Goode, M., Jack-
son, K., Rodriguez, M. and Weber, R.
"The Fluxdata Data and Collaboration
Server (http://www.fluxdata.org),"
Berkeley Laboratory Technical Report,
May, 2008. Available at http://
bwc.berkeley.edu/.
Baldocchi, D.D., et al., 2005. Predicting
the onset of net carbon uptake by
deciduous forests with soil temperature
and climate data: a synthesis of FLUX-
NET data. International Journal of
Biometeorology 49: 377-387.
Gazal, R. et al., 2008. GLOBE students,
BOX 2— Coupling webcam technology with flux observations can help us understand sea-
sonal changes in forest physiology. Recent advances in camera technology and the interpreta-
tion of digital imagery now allow the quantification of plant canopy development at flux sites auto-
matically and without the inherent subjectivity of observer-based systems (Richardson et al., 2007).
Besides the obvious information on snow or foliage presence at our flux sites we can also perform
image analysis on the red, green and blue (RGB) colour channel brightness to obtain the informa-
tion about the timing and rate of canopy green-up and senescence. Richardson et al. (2007) evalu-
ated relationships between indices derived from RGB colour information and radiometric measure-
ments of the fraction of incident photosynthetically active radiation absorbed by the canopy (fAPAR)
and NDVI, as well as the canopy-level photosynthetic capacity (Amax) derived from eddy covariance
measurements at a deciduous forest (Figure 3). This study showed that webcams, although they
are not calibrated radiometric instruments, could provide valuable insights into canopy development
and function. A more recent analysis (Fig. 3b) has shown that a “green excess” index (2 x G% - R%
- B%; Richardson et al. 2007) tracks the seasonal variation in tower-based estimates of GPP at an
evergreen conifer forest, offering the possibility that “near” remote sensing can provide additional
insights into canopy-scale physiological activity.
teachers, and scientists demonstrate
variable differences between urban and
rural leaf phenology. Global Change
Biology, doi:10.1111/j.1365-
2486.2008.01602.x.
Grunwald, T. and Bernhofer, C., 2007.
A decade of carbon, water and energy
flux measurements of an old spruce
forest at the Anchor Station Tharandt.
Tellus, 59B: 387-396.
IPCC. Climate Change 2007: The Physi-
cal Sciences Basis: Contribution of
Working Group I to the Fourth Assess-
ment Report of the Intergovernmental
Panel on Climate Change. (Cambridge
University Press, Cambridge, 2007).
Niemand, C., Kostner, B., Prasse, H.,
Grunwald, T. and Bernhofer, C., 2005.
Relating tree phenology with annual
carbon fluxes at Tharandt forest. Mete-
orologische Zeitschrift, 14(2): 197-202.
Nisbet, E., 2007. Earth monitoring:
Cinderella science. Nature 450: 789-
790.
Piao, S. et al., 2008. Net carbon dioxide
losses of northern ecosystems in re-
sponse to autumn warming. Nature,
451(7174): 49-52.
Richardson, A.D. et al., 2007. Use of
digital webcam images to track spring
green-up in a deciduous broadleaf
forest. Oecologia, 152: 323-334.
Schwartz, M.D., Ahas, R. and Aasa, A.
2006. Onset of spring starting earlier
across the Northern Hemisphere.
Global Change Biology, 12: 343-351.
contact: L. Wingate
lwingate@ed.ac.uk
Page 17
Keeping an eye on the carbon balance
FluxLetter
The Newsletter of
FLUXNET
Vol.1 No.2 May, 2008
FluxLetter is produced
quarterly at the FLUXNET
Office with support from the
National Science Foundation.
This issue of FluxLetter was
edited, designed and produced by:
Dennis Baldocchi
Rodrigo Vargas
FLUXNET Office, 137 Mulford
Hall, University of California,
Berkeley, CA 94720
ph: 1-(510)-642-2421
Fax: 1-(510)-643-5098
We plan to make the FLUXNET
newsletter a powerful information,
networking, and communication
resource for the community. If you
want to contribute to any section or
propose a new one please contact the
FLUXNET Office. THANKS!!
Figure 3a: Red, green and blue image analysis of canopy development.
Figure 3b: Measured ‘green excess index’ from image analysis of webcam images of an evergreen conifer canopy alongside daily
GPP estimates derived from eddy flux measurements. Data are from the Howland AmeriFlux site in Maine, USA; a movie of the camera
images is available online (http://www.forest.sr.unh.edu/richardson/Howland2007b.avi). Also indicated are observed average budburst
cont. from page 16
(a)
(b)