DOI: 10.1126/science.1187512
, 1164 (2010); 328Science
et al.Stuart H. M. Butchart,
Global Biodiversity: Indicators of Recent Declines
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between ORC binding and nucleosome turnover ,
suggesting that turnover facilitates ORC binding.
In contrast, other chromatin features that would
be exp ected for open or dynamic chromatin, in-
cluding nucleosome density, mononucleosome/
oligonucleosome ratio (a measure of micrococcal
nuclease accessibility), H2Av (an H2A.Z his-
tone variant enriched in active chromatin), and
salt-soluble nucleosomes, show little if any de-
pendence on ORC abundance (Fig. 3, H to P).
Our findings support the hypothesis that repli-
cation origins are determined by chromatin, not
by sequence features (20, 21). The better quan-
titative correspondence of ORC to CATCH-IT
data than to other chromatin measurements implies
that the ORC occupies DNA that is made acces-
sible by nucleosome turnover. In support of this
interpretation, we note that very similar corre-
spondences are seen when CATCH-IT data are
aligned with GAF sites (fig. S9) and that GAF
directs nucleosome turnover in vivo (22, 23).
Our direct strategy for measuring the kinetics
of nucleosome turnover does not rely on trans-
genes or antibodies but rather uses native his-
tones and generic reagents. Thus, CATCH-IT
provides a general tool for studying activities
that influence nucleosome turnover. With use of
CA TCH-IT , we found direct evidence that epige-
ne t i c maintenance involves nucleosome turnover,
a process that erases histone modifications (10).
The fact that EZ is responsible for di- and tri-
methylation of H3K27, but the nucleosomes that
it modifies turn over faster than a cell cycle,
argues against proposals that histone modifica-
tions required for cellular memory themselves
transmit epigenetic information (24). Rather, by
simply increasing or decreasing accessibility of
DNA to sequence-specific binding proteins, regu-
la te d nucleosome turnover may perpetuate active
or silent gene expression states and facilitate ini-
tiation of replication.
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members of our lab for helpful discussions, and the
Hutchinson Center Genomics Shared Resource for
microarray processing. This work was supported by NIH
grant 1R21DA025758 to S.H. and NIH Postdoctoral
Fellowship 1F32GM083449 to R.B.D. All data sets can be
found in GEO: GSE19788.
Supporting Online Material
www.sciencemag.org/cgi/content/full/328/5982/1161/DC1
Materials and Methods
Figs. S1 to S9
Table S1
References
7 January 2010; accepted 1 April 2010
10.1126/science.1186777
Global Biodiversity: Indicators of
Recent Declines
Stuart H. M. Butchart,
1,2
* Matt Walpole,
1
Ben Collen,
3
Arco van Strien,
4
Jörn P. W. Scharlemann,
1
Rosamunde E. A. Almond,
1
Jonathan E. M. Baillie,
3
Bastian Bomhard,
1
Claire Brown,
1
John Bruno,
5
Kent E. Carpenter,
6
Geneviève M. Carr,
7
†
Janice Chanson,
8
Anna M. Chenery,
1
Jorge Csirke,
9
Nick C. Davidson,
10
Frank Dentener,
11
Matt Foster,
12
Alessandro Galli,
13
James N. Galloway,
14
Piero Genovesi,
15
Richard D. Gregory,
16
Marc Hockings,
17
Valerie Kapos,
1,18
Jean-Francois Lamarque,
19
Fiona Leverington,
17
Jonathan Loh,
20
Melodie A. McGeoch,
21
Louise McRae,
3
Anahit Minasyan,
22
Monica Hernández Morcillo,
1
Thomasina E. E. Oldfield,
23
Daniel Pauly,
24
Suhel Quader,
25
Carmen Revenga,
26
John R. Sauer,
27
Benjamin Skolnik,
28
Dian Spear,
29
Damon Stanwell-Smith,
1
Simon N. Stuart,
1,12,30,31
Andy Symes,
2
Megan Tierney,
1
Tristan D. Tyrrell,
1
Jean-Christophe Vié,
32
Reg Watson
24
In 2002, world leaders committed, through the Convention on Biological Diversity, to achieve
a significant reduction in the rate of biodiversity loss by 2010. We compiled 31 indicators to report
on progress toward this target. Most indicators of the state of biodiversity (covering species’
population trends, extinction risk, habitat extent and condition, and community composition)
showed declines, with no significant recent reductions in rate, whereas indicators of pressures
on biodiversity (including resource consumption, invasive alien species, nitrogen pollution,
overexploitation, and climate change impacts) showed increases. Despite some local successes
and increasing responses (including extent and biodiversity coverage of protected areas,
sustainable forest management, policy responses to invasive alien species, and biodiversity-related
aid), the rate of biodiversity loss does not appear to be slowing.
I
n 2002 , world leaders committed, through the
Convention on Biological Diversity (CBD),
“to achieve by 2010 a significant reduction of
the current rate of biodiversity loss” (1), and this
“2010 target” has been incorporated into the
United Nations Millennium Development Goals
in recognition of the impact of biodiversity loss
on human well-being (2). The CBD created a
framework of indicators to measure biodiversity
loss at the level of genes, populations, species,
and ecosystems (3, 4). Although a minority have
been published individually (5), hitherto they have
not been synthesized to provide an integrated
outcome. Despite suggestions that the target is
unlikelytobe(6–8), or has not been (4, 9, 10),
met, we test this empirically using a broad suite of
biodiversity indicators.
To evaluate achievement of the 2010 tar get,
we (i) determined the trend, and timing and direction
of significant inflections in trend for individual
indicators (11) and (ii) calculated aggregated in-
dices relating to the state of biodiversity, pres-
sures upon it, policy and management responses,
and the state of benefits (ecosystem services) that
people derive from biodiversity, using the best
available sources. T o calculate aggregate indices,
we first scaled each of 24 indicators (out of 31)
with availabl e trend information to a value of 1 in
the first year with data from 1970 onward (only
eight indicators had earlier trends) and calculated
annual proportional change from this first year.
Then we used a generalized additive modeling
framework (5, 12, 13) and determined significant
inflections (12). Although absolute values are
difficult to interpret because they aggregate dif-
ferent elements of biodiversity, this approach
permits a synthetic interpretation of rate changes
across the elements measured: For example, the
aggregated state index should show positive
inflections if biodiversity loss has been signifi-
cantly reduced.
28 MAY 2010 VOL 328 SCIENCE www.sciencemag.org
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Our analyses suggest that biodiversity has
continued to decline over the past four decades,
with most (8 out of 10) state indicators showing
negative trends (Fig. 1 and Table 1). There have
been declines in population trends of (i) ver-
tebrates (13) and (ii) habitat specialist birds; (iii)
shorebird populations worldwide; extent of (iv)
forest (14, 15); (v) mangroves; (vi) seagrass beds;
and (vii) the condition of coral reefs. None show
significant recent reductions in the rate of decline
(Table 1), which is either fluctuating (i), stable (ii),
based on too few data to test significance (iii to vi),
or stable after a deceleration two decades ago (vii).
Two indicators, freshwater quality and trophic in-
tegrity in the marine ecosystem, show stable and
marginally improving trends, respectively, which
are likely explained by geographic biases in data
availability for the former and spatial expansion
of fisheries for the latter (5). Aggregated trends
across state indicators have declined, with no sig-
nificant recent reduction in rate: The most recent
inflection in the index (in 1972) was negative (Fig.
2). Because there were fewer indicators with trend
data in the 1970s, we recalculated the index from
1980, which also showed accelerating biodiversity
loss: The most recent inflection (2004) was neg-
ative. Finally, aggregated species’ extinction risk
(i.e., biodiversity loss at the species level) has ac-
celerated: The International Union for Conservation
of Nature ( IUCN) Red List Index (RLI), measuring
rate of change (16, 17), shows negative trends.
The majority of indicators of pressures on
biodiversity show increasing trends over recent
decades (Fig. 1 and Table 1), with increases in (i)
aggregate human consumption of the planet’s
ecological assets, (ii) deposition of reactive nitro-
gen, (iii) number of alien species in Europe, (iv)
proportion of fish stocks overharvested, and (v)
impact of climate change on European bird pop-
ulation trends (18). In no case was there a signif-
icant reduction in the rate of increase (Table 1),
which was stable (i, iii, and v), fluctuating (iv), or
based on too few data to test significance (ii),
although g rowth in global nitrogen deposition may
have slowed, and this may explain why the most
recent inflection in aggregated trends (in 2006)
was negative (Fig. 2) (5). Global trends for
habitat fragmentation are unavailable, but it is
probably increasing; for example, 80% of remain-
ing Atlantic Forest fragments are <0.5 km
2
in
size (19), and 59% of larg e river systems are
moderately or strongly fragmented by dams and
reservoirs (20).
1
United Nations Environment Programme W orld Conservation
Monitoring Centre, 219 Huntingdon Road, Cambridge CB3
0DL, UK.
2
BirdLife International, Wellbrook Court, Cambridge
CB3 0NA, UK.
3
Institute of Zoology, Zoological Society of
London, Regent’sPark,LondonNW14RY,UK.
4
Statistics
Netherlands, Post Office Box 24500, The Hague, 2490 HA,
Netherlands.
5
Department of Marine Sciences, University of
North Carolina at Chapel Hill, 340 Chapman Hall, CB 3300,
Chapel Hill, NC 27599, USA.
6
International Union for
Conservation of Nature (IUCN) and Conservation International
Global Marine Species Assessment, Biological Sciences, Old
DominionUniversity,Norfolk,VA23529,USA.
7
United
Nations Environment Programme, Global Environment Mon-
itoring System —Water, c/o National Water Research Institute,
867 Lakeshore Road, Burlington, Ontario L7R 4A6, Canada.
8
IUCN Species Survival Commission, Conservation Interna-
tional, Biodiversity Assessment Unit, c/o Center for Applied
Biodiversity Science, Conservation International, 2011 Crystal
Drive, Suite 500, Arlington, VA 22202, USA.
9
Fisheries and
Aquaculture Management Division, Food and Agriculture
Organization of the United Nations, Viale delle Terme di
Caracalla 00153, Rome, Italy.
10
SecretariatoftheRamsar
Convention on Wetlands, Rue Mauverney 28, 1196 Gland,
Switzerland.
11
European Commission Joint Research Centre,
Institute for Environment and Sustainability, TP290, Via
Enrico Fermi 2749, 21027 Ispra (VA), Italy.
12
Center for
Applied Biodiversity Science, Conservation International,
2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA.
13
Global Footprint Network, 312 Clay Street, Suite 300,
Oakland, CA 94607–3510, USA.
14
Environmental Sciences
Department, University of Virginia, Ch arlot tesv ille, VA
22903, U SA.
15
Istituto Superiore per la Protezione e la
Ricerca Ambientale, Via Curtatone 3, I-00185 Rome, Italy.
16
Royal Society for the Protection of Birds, The Lodge, Sandy
SG19 2DL, UK, and European Bird Census Council.
17
School of I ntegrative Systems, University of Queensland,
St. Lucia, Brisbane, Qld 4067, Australia.
18
Department of
Zoology, University of Cambridge, Downing Street, Cam-
bridge CB2 3EJ, UK.
19
National Center for Atmospheric
Research, 3450 Mitchell Lane, Boulder, CO 80301, USA.
20
World Wildlife Fund (WWF) Internat ional, 1196 Gland,
Switzerland.
21
South African National Parks, Centre for
Invasion Biology and Global Invasive Species Programme,
Post Office Box 216, Steenberg 7947, South Africa.
22
United
Nations Educational, Scientific, and Cultural Organization,
7 place de Fontenoy, 75352 Paris, France.
23
TRAFFIC
International, 219 Huntingdon Road, Cambridge CB3 0DL,
UK.
24
Sea Around Us Project, Fisheries Centre, University of
British Columbia, 2202 Main Mall, Vancouver, BC V6T1Z4,
Canada.
25
National Centre for Biological Sciences, Tata
Institute of Fundamental Research, GKVK Campus, Bellary
Road, Bangalore 560 065, India.
26
The Nature Conservancy,
4245 North Fairfax Drive, Arlington, VA 22203, USA.
27
U.S.
Geological Survey, Patuxent Wildlife Research Center, 12100
Beech Forest Road, Laurel, MD 20708–4039, USA.
28
Amer-
ican Bird Conservancy, 1731 Connecticut Avenue, N.W., 3rd
Floor, Washington, DC 20009, USA.
29
Centre for Invasion
Biology, Stellenbosch University, Private Bag X1, Matieland
7602, South Africa.
30
IUCN Species Survival Commission,
Department of Biology and Biochemistry, University of Bath,
Bath BA2 7AY, UK.
31
Al Ain Wildlife Park and Resort, Post
Office Box 45553, Abu Dhabi, United Arab Emirates.
32
IUCN,
Rue Mauverney 28, 1196 Gland, Switzerland.
*To whom correspondence should be addressed. E-mail:
stuart.butchart@birdlife.org
†Present address: Indian and Northern Affairs Canada, 15
Eddy, Gatineau QC K1A 0H4, Canada.
Fig. 1. Indicator trends for (A)thestateofbiodiversity,(B) pressures upon it, (C) responses to address its
loss, and (D) the benefits humans derive from it. Data scaled to 1 in 1970 (or for first year of data if
>1970), modeled (if >13 data points; see Table 1), and plotted on a logarithmic ordinate axis. Shading
shows 95% confidence intervals except where unavailable (i.e., mangrove, seagrass, and forest extent,
nitrogen deposition, and biodiversi tyaid).WBI,WildBirdIndex;WPSI,Waterbird Population Status Index;
LPI, Living Planet Index; RLI, Red List Index; IBA, Important Bird Area; AZE, Alliance for Zero Extinction
site; IAS, invasive alien species.
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Table 1. Summary of global biodiversity indicator trends.
Indicator
Data
availability
(years)†
% Change since
1970‡
Mean annual % change§
Trends in
rate of change║
1970s 1980s 1990s 2000s Since 1970
State
Living Planet Index (LPI)
(mean population trends of vertebrates)
1970–2006 –31* –0.2 –1.4 –1.4 –0.9 –1.0 F
Wild Bird Index [mean population trends
of habitat specialists in Europe and North
America, disaggregated for terrestrial (t)
and wetland (w) species]
1980–2007 –2.6*
–16*(t)
+40*(w)
–0.6
–1.3
+1.1
–0.2
–0.7
+1.3
+0.6
+0.3
+1.1
–0.1
–0.7
+1.2
S
D 1982–2007
S
Waterbird Population Status Index
(% shorebird populations increasing,
stable, or decreasing)
1985–2005†–33 –1.4 –2.0 –2.4 –2.0 A?
Red List Index (RLI) (extinction risk of
mammals, birds, amphibians, and corals)
1986–2008 –6.1* –0.1 –0.2 –0.5 –0.3 A
Marine Trophic Index
(shift in fishing catch from top
predators to lower trophic levels)
1950–2006 +3.0* +0.1 –0.1 +0.1 +0.1 +0.1 S
Forest extent 1990–2005†–3.1 –0.2 –0.2 –0.2 S?
Mangrove extent 1980–2005†–19 –1.0 –0.7 –0.7 –0.8 S?
Seagrass extent 1930–2003†–20 –0.4 –0.5 –0.5 –2.4 –0.7 A?
Coral reef condition
(live hard coral cover)
1980–2004 –38* –3.9 –0.3 +0.2 –1.8 D 1985–1988
Water Quality Index
(physical/chemical quality of freshwater)
1980–2005 0 +0.1 +0.0 –0.2 +0 S
Number of state indicators declining 2/3 8/9 8/10 7/10 8/10
Pressures
Ecological footprint
(humanity’s aggregate resource-consumption)
1961–2006 +78* +2.0 +1.3 +1.3 +2.1 +1.6 S
Nitrogen deposition rate
(annual reactive N deposited)
1850–2005† +35 +2.0 +1.3 –0.3 +0.2 +0.9 D?
No. alien species in Europe
(Mediterranean marine, mammal, and freshwater)
1970–2007 +76* +2.0 +1.4 +1.6 +1.1 +1.5 S
Exploitation of fish stocks
(% overexploited, fully exploited, or depleted)
1974–2006 +31* +0.6 +0.6 +1.1 +1.2 +0.9 F
Climatic Impact Indicator
(degree to which European bird population trends
have responded in the direction
expected from climate change)
1980–2005 +23* –0.8 +3.2 +1.2 +1.2 S
Number of pressure indicators increasing 4/4 4/5 4/5 5/5 5/5
Responses
Extent of Protected Areas (PAs) 1888–2006 +400* +7.6 +4.5 +3.4 +2.4 +4.7 S
Coverage by PAs of Important
Bird Areas and Alliance for Zero Extinction sites
1888–2009 +360* +5.6 +4.6 +2.6 +0.8 +3.4 D 1999–2008
Area of forest under sustainable
management (FSC certified)
1995–2008 +12,000* +100 +20 +46 D 2006
International IAS policy adoption
(no. signatories to conventions
with provision for tackling IAS)
1952–2008 +2700* +10 +6.9 +14 +5.1 +9.1 S
National IAS policy adoption
(% countries with relevant legislation)
1964–2009 +10,000* +30 +8.7 +12 +4.1 +13 D 2004–2009
Official development assistance
(US
$
per year provided in support of CBD)
2005–2007† +17 +8.4 +8.3 D?
Number of response indicators increasing 4/4 4/4 5/5 6/6 6/6
Benefits
LPI for utilized vertebrate populations 1970–2006 –15* +1.0 –0.3 –1.3 –1.7 –0.4 A 1972–2006
RLI for species used for food and medicine 1986–2008 –3.5* –0.2 –0.2 –0.2 –0.2 A
RLI for bird species in international trade 1988–2008 –0.5* –0.01 –0.03 –0.02 –0.03 A
Number of benefits indicators declining 0/1 3/3 3/3 3/3 3/3
*Significant trends (P < 0.05). †Identifies indicators with insufficient data to test significance of post-1970 trends, usually because annual estimates are unavailable. ‡Since earliest
date with data if this is post-1970. §Because the indicators measure different parameters, some comparisons of mean annual % change between indicators are less meaningful than
comparisons between decades for the same indicator. ║Rate of change decelerating (D), accelerating (A), stable (S, i.e., no years with significant changes), fluctuating (F, i.e., a sequence of
significant positive and negative changes), or with too few data points to test significance (?); years indicate periods in which second derivatives differed significantly from zero (P < 0.05).
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All indicators of policy and management
responses show increasing trends (Fig. 1 and
Table 1), with increases in (i) extent of protected
areas (PAs) (Table 2); (ii) coverage by PAs of two
subsets of Key Biodiversity Areas (21) [39% of
the area of 10,993 Important Bird Areas and 42%
of the area of 561 Alliance for Zero Extinction
sites (22) by 2009]; (iii) area of sustainably
managed forests [1.6 million km
2
under Forest
Stewardship Council (FSC) certification by 2007];
(iv) proportion of eligible countries signing inter-
national agreements relevant to tackling invasive
alien species (IAS) [reaching 82% by 2008 (23)];
(v) proportion of countries with national legisla-
tion to control and/or limit the spread and impact
of IAS [reaching 55% by 2009 (23)]; and (vi)
biodiversity-related aid (reaching US$3.13 billion
in 2007). The rate of increase was stable (i and iv),
slowing (ii, iii, and v), or based on too few data to
test significance (vi) (T able 1). The last three in-
flections in aggregated trends (2002, 2004, and
2008) were all negative (Fig. 2), indicating that
the rate of improvement has slowed. T w o other
indicators have only baseline estimates: Manage-
ment effectiveness was “sound” for 22% of PAs
(“basic” for 65% and “clearly inadequate” for
13%), and the proportion of genetic diversity for
200 to 300 important crop species conserved ex
situ in gene banks was estimated to be 70% (24).
Only three indicators address trends in the
benefits humans derive from biodiversity (Fig.
1 and Table 1): (i) population trends of utilized
vertebrates have declined by 15% since 1970, a nd
aggregate species’ extinction risk has increased
Fig. 2. Aggregated indices of (A)thestateofbio-
diversity based on nine indicators of species’ population
trends, habitat extent and condition, and community
composition; (B) pressures on biodiversity based on five
indicators of ecological footprint, nitrogen deposition,
numbers of alien species, overexploitation, and climatic
impacts; and (C) responses for biodiversity based on six
indicators of protected area extent and biodiversity cov-
erage, policy responses to invasive alien species, sustain-
able forest management, and biodiversity- related aid.
Values in 1970 set to 1. Shading shows 95% confidence
intervals derived from 1000 bootstraps. Significant
positive/upward (open circles) and negati ve/downward
(filled circles) inflections are indicated.
A
B
C
Table 2. Examples of successes and positive trends relevant to the 2010 target (5).
Indicator Successes and positive trends
State
Living Planet Index of Palearctic
vertebrate populations
Increased by 43% since 1970 (e.g., Eurasian beaver and common buzzard)
Waterbird populations in
North America and Europe
Increased by 44% since 1980 owing to wetland protection and sustainable management
(but populations remain below historic levels).
Species downlisted on the
IUCN Red List
Species qualifying for downlisting to lower categories of extinction risk owing to successful
conservation action include 33 birds since 1988 (e.g., Lear’s macaw), 25 mammals since
1996 (e.g., European bison), and 5 amphibians since 1980 (e.g., Mallorcan midwife toad).
Wild Bird Index and Red List
Index for species listed on the
European Union Birds Directive
Annex 1–listed species’ population trends have improved in EU countries (27) and
extinction risk reduced (RLI increased 0.46% during 1994–2004) owing to designation of
Special Protected Areas and implementation of Species Action Plans under the directive
(e.g., white-tailed eagle).
Extinctions prevented At least 16 bird species extinctions were prevented by conservation actions during 1994–2004,
e.g., black stilt (28).
Water Quality Index in Asia Improved by 7.4% since 1970.
Pressures
Deforestation in
Amazonian Brazil
Slowed from 2.8 million ha in 2003–2004 to 1.3 million ha in 2007–2008, but it is uncertain
to what extent this was driven by improved enforcement of legislation versus reduced
demand owing to economic slowdown.
Responses
National biodiversity strategies
and action plans (NBSAPs)
87% of countries have now developed NBSAPs and therefore have outlined coherent plans
for tackling biodiversity loss at the national scale.
Protected areas (PAs) Nearly 133,000 PAs designated, now covering 25.8 million km
2
: 12% of the terrestrial
surface (but only 0.5% of oceans and 5.9% of territorial seas), e.g., Juruena National Park,
Brazil, designated in 2006, covering 19,700 km
2
of Amazon/cerrado habitat.
Invasive alien species (IAS)
policy, eradication, and control
82% of eligible countries have signed international agreements relevant to preventing the
spread and promoting the control/eradication of IAS. Successful eradications/control of IAS
include pigs on Clipperton Atoll, France (benefiting seabirds and land crabs), cats, goats and
sheep on Natividad, Mexico (benefiting black-vented shearwater), and red fox in southwest
Australia (benefiting western brush wallaby).
Official development
assistance for biodiversity
Increased to at least US$3.13 billion in 2007.
www.sciencemag.org SCIENCE VOL 328 28 MAY 2010 1167
REPORTS
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