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www.sciencemag.org SCIENCE VOL 294 26 OCTOBER 2001 793
CREDITS: (TREE) RICHARD KETTLEWELL/ANIMALS ANIMALS EARTH SCENCE;(BUTTERFLY) LAURA SIVELL; PAPILIO/CORBIS
Climate warming (1) is expected to
alter seasonal biological phenomena
such as plant growth and flowering
or animal migration, which depend on ac-
cumulated temperature, that is, the total
heat required for an organism to develop
from one point to another in its life cycle.
These so-called phenological changes are
likely to have a wide range of conse-
quences for ecological processes, agricul-
ture, forestry, human health, and the glob-
al economy. An increasing number of
studies now report changes in plant and
animal cycles from a wide range of re-
gions, from cold and wet to warm and dry
ecosystems. These phenological changes
are sensitive and easily observable indica-
tors of biospheric changes in response to
climate warming.
Phenological changes differ from
species to species (2–12), but some are
substantial (see the figure). In Mediter-
ranean ecosystems, the leaves of most de-
ciduous plant species now unfold on aver-
age 16 days earlier and fall on average 13
days later than they did 50 years ago (7).
In Western Canada, Populus tremuloides
shows a 26-day shift to earlier blooming
over the past century (9). Other shifts are
smaller but go in the same direction. A 6-
day shift to earlier leaf unfolding and a 5-
day delay in autumn leaf coloring over 30
years have been described from Scandi-
navia to Macedonia (4). An earlier onset
of biological spring by about 8 days has
also been reported across Europe for
1969–98 (10, 11) and by about 6 days in
North America for 1959–93 (12). In ma-
rine ecosystems, substantial positive linear
trends in phytoplankton season length and
abundance have been described in areas of
the North Atlantic with warming waters
for 1948–95 (13).
Remote sensing data validate these
ground observations on larger scales. The
Normalized Difference Vegetation Index
(NDVI), which is derived from infrared and
red Earth surface reflectance, scales with
green biomass. NDVI satellite data between
45°N and 70°N for 1982–90 showed an 8-
day shift to an earlier start of the growing
season and a delay of 4 days for the declin-
ing phase (14). New NDVI data suggest
that the growing season has become nearly
18 days longer during the past two decades
in Eurasia and 12 days longer in North
America (15). The data also show a gradual
greening of the northern latitudes above
40°N: Plants have been growing more vig-
orously since 1981, especially in Eurasia.
This lengthening of the plant growing
season is likely to contribute to the global
increase in biospheric activity, which has
been inferred from the
increasing amplitude
of annual oscillations
in the atmospheric CO2between 1960 and
1994 (16). The atmospheric data also sug-
gest an extension of the growing season by
about 7 days in the Northern Hemisphere
between the 1960s and the early 1990s,
mostly after 1980. Accelerated tree growth
across Europe, previously attributed to fer-
tilization by nitrogen compounds and in-
creased CO2(17), may be driven at least
partly by this extended growing season. The
lengthening of the growing season thus
plays a key role in global carbon fixation,
the amount of CO2in the atmosphere, and
related global water and nutrient cycles.
Data on shifts in flowering dates are
abundant and show similar trends. Shifts
to earlier flowering by about 1 week have
been reported in Mediterranean species
for 1952 to 2000 (7), in Hungary for 1851
to 1994 (3), in Wisconsin for 1936–98 (5),
and in Washington, DC, for 1970–99 (6).
These observations agree with model re-
sults, which indicate that the time of maxi-
mum olive pollen concentrations advances
by about 6 days per degree Celsius in the
western Mediterranean (18).
All these plant phenological changes are
highly correlated with temperature changes,
especially in the months before seasonal life
cycle events. Temperature (1) as well as
phenology has changed most noticeably af-
ter the mid-1970s. This correlation does not
necessarily imply a causal connection.
However, available data and current knowl-
edge of plant phenology, including numer-
ous experimental studies (4, 19,20), indi-
cate that the observed changes are mostly
due to the increased temperatures. More-
over, at most sites, the number of freezing
days has decreased sub-
stantially in recent years
(1, 7), decreasing the
probability of frost
damage to young leaves
and flowers (21).
Animal life cycles al-
so depend on climate.
For example, insects are
expected to pass through
their larval stages faster
and become adults earli-
er in response to warm-
ing. Aphid species in the
United Kingdom have
shown a 3- to 6-day ad-
vance in the timing of
different phases in their
life cycle over the past
25 years (22). The date
on which the maximum
numbers of individuals
of the most common
Microlepidoptera in the
Netherlands were count-
ed shifted forward by 12
days on average between 1975 and 1994
(23). Butterflies now appear 11 days earlier
than in 1952 in northeast Spain (7). British
butterflies have not only appeared earlier but
have also shown longer flight periods, that is,
enhanced activity, over the past two decades
(24). In other animal groups, frog calling has
been reported to occur about 10 days earlier
between 1990 and 1999 than between 1900
and 1912 in New York state (25), and bird
species surveyed in the United Kingdom
from 1971 to 1995 showed 9-day shifts to-
ward earlier egg laying (2).
The advanced leafing, flowering, fruiting,
and appearance of insects are likely to ad-
vance the availability of food supplies for
SCIENCE’SCOMPASS
PERSPECTIVES
PERSPECTIVES: PHENOLOGY
Responses to a Warming World
Josep Peñuelas and Iolanda Filella
Image not
available for
online use.
Ecological consequences of climate warming on plant and animal
phenology.
The authors are in the Unitat Ecofisiologia CSIC-
CREAF, Center for Ecological Research and Forestry
Applications (CREAF), Edifici C, Universitat Autònoma
de Barcelona, 08193 Bellaterra (Barcelona), Spain. E-
mail: josep.penuelas@uab.es, i.filella@creaf.uab.es
on January 31, 2008 www.sciencemag.orgDownloaded from
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www.sciencemag.org SCIENCE VOL 294 26 OCTOBER 2001 795
birds. However, a later arrival in Europe of
migratory birds wintering south of the Sahel
has been reported (7, 26). For these species,
the decision when to start spring migration
may become maladaptive when the cue for
migration is independent of the environmental
change in the breeding area (7). Climate
change may thus be a serious threat to species
that migrate from tropical wintering grounds
to temperate breeding areas. They may arrive
at an inappropriate time to exploit the habitat
and compete with larger numbers of individu-
als of resident species as more of them sur-
vive the winter. These arguments may partly
explain the decline of these long-distance mi-
gratory species in Western Europe (8), al-
though short-distance migrants may be more
flexible. These findings support previous re-
sults demonstrating that shifts in global cli-
mate patterns can affect migratory birds (27).
These changes in plant phenology and bird
migration show that climate warming may
lead to a decoupling of species interactions,
for example, between plants and their pollina-
tors or between birds and their plant and insect
food supplies (2). Changes not only in mean
temperatures but also in temperature patterns
may affect these interactions even more
strongly because they may alter the synchro-
nization between species (28). An example of
such decoupling was recently reported. The
Great Tit still breeds at the same time, but its
food supply has been advanced because of
earlier plant development in recent years (29).
Different phenological responses (7, 30) may
alter the competitive ability of different species
and thus their ecology and conservation, re-
sulting in unpredictable impacts on communi-
ty structure and ecosystem functioning.
The observed phenological changes
have occurred with a warming only 50% or
less of that expected for the 21st century
(1). Many ecological (carbon sequestration,
nutrient and water cycles, species competi-
tion, pests and diseases, bird migration and
reproduction, and species-species interac-
tions), agricultural (crop suitability, yield
potential, length of growing season, risk of
frost damage, epidemiology of pests and
diseases, timing and amount of pesticide
use, and food quality), and socioeconomic
and sanitary (duration of the pollen season
and distribution and population size of dis-
ease vectors) factors depend strongly on
plant and animal phenology. Phenology is
therefore increasingly relevant in the
framework of global change studies (31).
As in many areas of environmental sci-
ence, the key requirement is long-term data
sets. Today, thousands of people—profes-
sionals and volunteers—record phenologi-
cal changes all over the world, as do inter-
national and national phenological moni-
toring networks such as Global Learning to
Benefit the Environment (GLOBE) or the
European Phenology Network. Together
with remote sensing, atmospheric, and eco-
logical studies, these data will help to answer
the many questions raised by the recently re-
ported climate effects on phenology: What
are the limits of the lengthening of the plant
growth season and the consequent greening
of our planet? Will the (less seasonal) tropical
ecosystems be less affected than boreal, tem-
perate, and Mediterranean ecosystems? How
will different aquatic ecosystems respond?
How will responses to temperature and other
drivers of global change interact to affect
phenology and the distribution of organisms?
How will changes in synchronization be-
tween species affect population dynamics
both in terrestrial and aquatic communities?
Will appropriate phenological cues evolve at
different trophic levels?
References and Notes
1. Intergovernmental Panel on Climate Change,
Climate
Change 2001: The Scientific Basis. Third Assessment
Report of Working Group I,
J. T. Houghton
et al
., Eds.
(Cambridge Univ. Press, Cambridge, 2001).
2. H. Q. Crick, C. Dudley, D. E. Glue, D. L. Thomson,
Na-
ture
388,526 (1997).
3. A.Walkowszky,
Int. J. Biometeorol
.41,155 (1998).
4. A. Menzel, P. Fabian,
Nature
397,659 (1999).
5. N. L. Bradley, A. C. Leopold, J. Ross, W. Huffaker,
Proc.
Natl. Acad. Sci. U.S.A.
96,9701 (1999).
6. M. Abu-Asab
et al.
,
Biodivers. Conserv.
10,597 (2001).
7. J. Peñuelas, I. Filella, P. Comas,
Global Change Biol.
,in press.
8. C. Both, M. E. Visser,
Nature
411,296 (2001).
9. E. G. Beaubien, H. J. Freeland,
Int. J. Biometeorol
.44,
53 (2000).
10. F. M. Chmielewsky, T. Roetzer,
Agric. Forest Meteorol
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108,101 (2001).
11. R.Ahas,
Int. J. Biometeorol
.42,119 (1999).
12. M. D. Schwartz, B. E. Reiter,
Int. J. Climatol.
20,929
(2000).
13. P. C. Reid, M. Edwards, H. G. Hunt, A. J.Warner,
Nature
391,546 (1998).
14. R. B.Myneni
et al
.,
Nature
386,698 (1997).
15. L. Zhou
et al
.,
J. Geophys. Res.
106,20069 (2001).
16. C. D. Keeling, J. F. S. Chin,T. P. Whorf,
Nature
382,146
(1996).
17. H. Spiecker
et al
., Eds.,
Growth Trends in European
Forests: Studies from 12 Countries
(Springer, Berlin,
1996).
18. C. P. Osborne
et al
.,
Plant Cell Environ.
23,701
(2000).
19. W. Larch er,
Physiological Plant Ecology
(Springer,
Berlin, 1995).
20. M.V. Price, N. M. Waser,
Ecology
79,1261 (1998).
21. Note, however, that species requiring a certain num-
ber of frost days for budbursting (
19
) may suffer an
impact not linearly correlated with temperature.
22. R. A. Fleming, G. M. Tatchell, in
Insects in a Changing
Environment
,R.Harrington, N. Stork, Eds. (Academic
Press, London, 1995), pp. 505–508.
23. W. N. Ellis, J. H. Donner, J. H. Kuchlein,
Entomol. Ber.
Amsterdam
57,66 (1997).
24. D. B. Roy, T. H. Sparks,
Global Change Biol.
6,407
(2000).
25. J. P. Gibbs, A. R. Breisch,
Conserv. Biol.
15,1175
(2001).
26. C . F. Mason,
Bird Study
42,182 (1995).
27. T. S. Sillet, R. T. Holmes, T. W. Sherry,
Science
288,
2040 (2000).
28. R. Harrington, I. Woidwod,T. Sparks,
Trends Ecol. Evol
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14,146 (1999).
29. M. E. Visser
et. al
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30. A. H. Fitter
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Funct. Ecol.
9,55 (1995).
31. A conference, “The times they are a changing. Climate
change, phenological responses and their conse-
quences for biodiversity, agriculture, forestry and hu-
man health,” will be held in Amsterdam in December
2001; see www.dow.wau.nl/msa/epn/conference.
SCIENCE’SCOMPASS
The walls of higher plants contain small
amounts of a mysterious polysaccha-
ride known as rhamnogalacturonan II
(RGII). RGII is thought to be the most com-
plex polysaccharide on Earth, and its pres-
ence and strong conservation in all higher
plants suggest that it is important for the
structure or growth of plant cell walls. The
study by O’Neill et al. (1) on page 846 of
this issue convincingly shows, 23 years after
its discovery (2), that RGII is essential for
plant growth and that minor changes in its
structure cause growth defects.
More than 300 years ago, Robert Hooke
pointed his primitive microscope at a slice
of cork and discovered the cellular basis of
organisms. Sadly, since then, plant cell
walls, which formed the compartments he
actually observed, have never been consid-
ered particularly entertaining structures. In-
deed, the word wall itself evokes something
dull and rigid, built only to enclose, sup-
port, divide, and protect. However, a closer
look reveals just how erroneous this view
is. Walls of growing plant cells are extreme-
ly sophisticated composite materials made
of dynamic networks of polysaccharides,
protein, and phenolic compounds. Cellu-
lose microfibrils with a tensile strength
comparable to that of steel provide the plant
with a load-bearing framework. These mi-
crofibrils are rigid wires made of crys-
talline arrays of β-1,4-linked chains of glu-
cose residues, which are extruded from lit-
tle hexameric spinnerets in the plant cell
plasma membrane and surround the grow-
ing cell like the hoops around a barrel. Be-
cause cellulose microfibrils constrain tur-
gor-driven cell expansion in one preferen-
tial direction, they control the shape of
plant cells and ultimately that of the plants
themselves. Hemicelluloses, such as xy-
loglucans, are tethered by hydrogen bonds
to cellulose and form cross-links that may
control the separation of the cellulose mi-
crofibril hoops. The cellulose-hemicellu-
lose network is embedded in a matrix of
complex galacturonic acid–rich pectic
PERSPECTIVES: PLANT BIOLOGY
A Baroque Residue in Red Wine
Herman Höfte
The author is in the Laboratoire de Biologie Cellu-
laire, INRA, 78210 Versailles Cedex, France. E-mail:
hofte@versailles.inra.fr
on January 31, 2008 www.sciencemag.orgDownloaded from