Erosion of Lizard Diversity by Climate Change and Altered Thermal Niches

Abstract

It is predicted that climate change will cause species extinctions and distributional shifts in coming decades, but data to
validate these predictions are relatively scarce. Here, we compare recent and historical surveys for 48 Mexican lizard species
at 200 sites. Since 1975, 12% of local populations have gone extinct. We verified physiological models of extinction risk
with observed local extinctions and extended projections worldwide. Since 1975, we estimate that 4% of local populations have
gone extinct worldwide, but by 2080 local extinctions are projected to reach 39% worldwide, and species extinctions may reach
20%. Global extinction projections were validated with local extinctions observed from 1975 to 2009 for regional biotas on
four other continents, suggesting that lizards have already crossed a threshold for extinctions caused by climate change.

Full text

DOI: 10.1126/science.1184695
, 894 (2010); 328Science et al.Barry Sinervo,
Altered Thermal Niches
Erosion of Lizard Diversity by Climate Change and
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could occur in C. maculatus through sexual se-
lection on males (18,26–28). If sexual selection is
responsible for the greater strength of the r
ID-BV
coefficients in males, it raises the possibility of
positive feedback, where sexual selection
increases the contribution of deleterious muta-
tions to trait expression, in turn increasing both
good genes benefits from sexual selection and the
benefit of sex itself.
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29. We thank J. Chan for the maintenance of the pedigree
and the collection and management of the data set;
R. Black and F. Gonzalez for statistical advice; B. Booth,
A. Sutton, and S. Jennings for their assistance with the
experiment; and N. Colegrave, W. Hazel, M. Puurtinen,
J. Radwan, M. Ritchie, and L. Simmons for their comments
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Supporting Online Material
www.sciencemag.org/cgi/content/full/328/5980/892/DC1
Materials and Methods
SOM Text
Figs. S1 to S6
Tables S1 to S10
References
5 February 2010; accepted 24 March 2010
10.1126/science.1188013
Erosion of Lizard Diversity by Climate
Change and Altered Thermal Niches
Barry Sinervo,
1,15
*Fausto Méndez-de-la-Cruz,
2
Donald B. Miles,
3,15
Benoit Heulin,
4
Elizabeth Bastiaans,
1
Maricela Villagrán-Santa Cruz,
5
Rafael Lara-Resendiz,
2
Norberto Martínez-Méndez,
2
Martha Lucía Calderón-Espinosa,
6
Rubi Nelsi Meza-Lázaro,
2
Héctor Gadsden,
7
Luciano Javier Avila,
8
Mariana Morando,
8
Ignacio J. De la Riva,
9
Pedro Victoriano Sepulveda,
10
Carlos Frederico Duarte Rocha,
11
Nora Ibargüengoytía,
12
César Aguilar Puntriano,
13
Manuel Massot,
14
Virginie Lepetz,
15
†Tuula A. Oksanen,
16
David G. Chapple,
17
Aaron M. Bauer,
18
William R. Branch,
19
Jean Clobert,
15
Jack W. Sites Jr.
20
It is predicted that climate change will cause species extinctions and distributional shifts in coming
decades, but data to validate these predictions are relatively scarce. Here, we compare recent
and historical surveys for 48 Mexican lizard species at 200 sites. Since 1975, 12% of local
populations have gone extinct. We verified physiological models of extinction risk with observed local
extinctions and extended projections worldwide. Since 1975, we estimate that 4% of local
populations have gone extinct worldwide, but by 2080 local extinctions are projected to reach 39%
worldwide, and species extinctions may reach 20%. Global extinction projections were validated
with local extinctions observed from 1975 to 2009 for regional biotas on four other continents,
suggesting that lizards have already crossed a threshold for extinctions caused by climate change.
Global climate change affects organisms
in all biomes and ecosystems. Two nat-
ural compensatory responses are possi-
ble. Given enough time and dispersal, species
may shift to more favorable thermal environ-
ments, or they may adjust to new environments
by behavioral plasticity, physiological plasticity,
or adaptation. Alternatively, failure to adjust or
adapt culminates in demographic collapse and
extinction. Despite accumulating evidence of
contemporary climate change affecting species
ranges and phenologies (1–3), evidence of ex-
tinctions at either local or global scales is lack-
ing (4–6). Moreover, current forecasting models
(7,8) are not calibrated with actual extinctions,
but are premised on hypothesized effects of
thermal physiology on demography and extinc-
tion. Alternatively, models are based on range
shifts or species-area relations in mobile species
(1), but not extinctions (9). Hence, there is still
much uncertainty regarding the expected mag-
nitude of extinctions resulting from climate
change (10).
Empirical validation of global extinction fore-
casts requires three forms of evidence. First,
actual extinctions should be linked to macro-
climate and validated to biophysical thermal
causes arising from microclimate (11). Second,
the pace of climate change should compromise
thermal adaptation (10), such that evolutionary
rates lag behind global warming owing to con-
straints on thermal physiology (12,13). Third,
extinctions due to climate should be global in
extent.
From 2006 to 2008, we resurveyed 48
Sceloporus lizard species at 200 sites in Mexico
that were first sampled in 1975 to 1995, and 12%
of sites were locally extinct by 2009 (table S1).
Although Sceloporus lizards are heliotherms
that bask and require solar radiation to attain
physiologically active body temperatures (T
b
)
(14,15), activity in hot weather may result in T
b
exceeding CT
max
, the critical thermal maximum,
leading to death. Lizards retreat to cool refuges
rather than risk death by overheating. However,
hours of restriction (h
r
) in thermal refuges limit
foraging, constraining costly metabolic functions
like growth, maintenance, and reproduction, there-
by undermining population growth rates and
raising extinction risk. Lizards could evolve
higher T
b
, but this brings them closer to CT
max
,
which increases risk of overheating. Extinction
risk may increase because of other thermal adap-
tations. For example, viviparity, which is posited
to be a thermal adaptation to cold climates (16),
may elevate extinction risk because high T
b
can compromise embryonic development in
utero (17).
We analyzed rate of change in maximum air
temperature Tmax
˙
at 99 Mexican weather sta-
tions and constructed climate surfaces (tables S2
and S3, 1973 to 2008; fig. S1). Rate of change in
T
max
was greatest for winter-spring (January to
May; fig. S1 and table S3A) and increased faster
in northern and central México and at high ele-
vation, as evidenced by significant coefficients for
fitted climate surfaces. We found a correlation
between rate of change in T
max
during winter-
spring breeding periods and local extinctions of
Sceloporus species (table S3).
Many viviparous species in México are con-
fined to high-elevation “islands,”where climate
change has been most rapid. Logistic regression
and multiple regression with phylogenetic inde-
pendent contrasts (18,19) revealed that extinction
risk was significantly related to low latitudinal
and altitudinal range limits (Fig. 1, A and B),
where thermal physiology and/or ecological
interactions limit species (20,21). Phylogenetic
correlation analysis (18) showed that extinction
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risk of viviparous lizards (18%) was twice that
of oviparous lizards (9%, n=10000 bootstrap
replications P< 0.001). Moreover, multiple re-
gression based on phylogenetic independent
contrasts (PICs; Fig. 1C and table S4) showed that
extinction risk of viviparous taxa was significant-
ly related to low TbðTb,viviparous ¼31:8-CT
0:31 ½SE,Tb,oviparous ¼34:8-CT0:40, t¼
5:92, P<0:0001Þand cool montane habitats
ðTair,viviparous ¼22:4-CT1:79, Tair ,oviparous ¼
28:39-CT1:38, t¼2:89, P<0:006Þ,where
climate has changed most rapidly in México.
To validate patterns of extinction risk and
T
b
, we deployed thermal models (22) that record
operative temperatures (T
e
) at two extinct and
two persistent Yucatán sites of S. serrifer. Hours
of restriction in activity (h
r
) during reproduction
was significantly higher at extinct versus per-
sistent sites (t=9.26,P< 0.0001). By April
2009, h
r
at extinct Yucatán sites had become
so severe that if S. serrifer were still present, it
would have to retreat shortly after emergence
(fig. S4A). Daily T
max
was positively correlated
with h
r
assessed by T
e
(P< 0.001, fig. S4B). The
relation between h
r
as a function of T
max
relative
to S. serrifer’sT
b
[h
r
=6.12+0.74×(T
max
−T
b
),
eq. S2 (23)] is a general formula for predicting
extinctions.
We modeled extinct/persistence status based
on values for h
r
at Sceloporus sites derived from
eq. S2 (23). The Yucatán ground truth for S.
serrifer suggests that extinction occurs when h
r
exceeds 4. We calibrated this value with extinct/
persistent Sceloporus sites. Goodness-of-fit tests
of the model indicate that the best fit for ob-
served and predicted extinctions at Sceloporus
sites is h
r
> 3.85. If a species with a given T
b
at
a given geo-referenced site, subjected to T
max,i
,
experienced h
r
> 3.85 during the 2-month re-
productive period (March to April), we assumed
that it would go extinct by 2009. Association of
predicted and observed extinctions from this
physiological model was significant for ovipa-
rous (c
2
= 49.0, P< 0.001) and viviparous taxa
(c
2
=4.2,P<0.04).
As demography of high-elevation taxa be-
comes compromised due to climate change, spe-
cies at low elevation that were previously limited
by physiology and competition should expand
into historically cooler habitat that is now warmer
(20,24), perhaps accelerating extinction of high-
elevation forms. For viviparous taxa, six errone-
ously assigned extinct sites involved six of the
eight cases of range expansion by low-elevation
taxa, which all invaded from low to high altitudes
or latitudes (table S1; significant by sign test, P<
0.001). Adding range shifts of competitors as a
factor improved fit significantly between observed
and predicted extinctions (Dlog likelihood = 45.37,
1df,P< 0.0001, logistic regression). Therefore,
competitive exclusion by invading low-elevation
taxa appears to exacerbate climate-change ex-
tinctions of high-elevation taxa.
Lizards cannot evolve rapidly enough to track
current climate change because of constraints
arising from the genetic architecture of thermal
preference (12,13). A phylogenetic correlation
between T
b
and CT
max
constrains adaptation.
PIC regression of CT
max
on T
b
among Phryno-
somatidae suggests that a shift in T
b
by 1°C yields
only a 0.5°C correlated response in CT
max
(table
S5andfig.S7).Thus,CT
max
may not evolve
fast enough to keep up with evolved change in
T
b
. Furthermore, adaptive increase in T
b
due to
climate change is constrained by genetic cor-
relations in which high T
b
necessarily requires
prolonged activity out of retreat sites (25),
further increasing risk of overheating. Genetic
trade-offs with energetically costly traits such as
growth (25) also constrain adaptation.
The evolutionary response (R=h
2
s;sis the
selection differential) necessary to keep pace with
climate change is further constrained by low
heritability for T
b
, which we previously estimated
at h
2
=0.17forSceloporus occidentalis in the
laboratory (25). We used the physiological model
to compute the sustained selection differential at
each site j, such that T
b,j
+D
t
T
b,j
evolves to
match T
max,j
+D
t
T
max,j
, yielding Dh
r,j
=0and
thereby rescuing population j from extinction [D
t
computed over 1975 to 2009 (historical), 2009 to
2050, and 2050 to 2080]. We assumed s
j
=R
j
/h
2
=
D
t
T
b,j
/h
2
, and generation times of 1 year versus
2 years (i.e., lowland versus montane Sceloporus,
table S1). We expressed these critical levels of
adaptive response as surfaces for s
sustained
, the
sustained selection differential (Fig. 2B).
We compared the magnitude of selection al-
lowing a species to adapt to climate change with
maximum rates sustained under artificial or
natural selection (26). Such comparisons are
facilitated by dividing each sustained selection
differential by the standard deviation (s
Tb
=
1.23 for T
b
of Mexican lizards) to obtain i,the
standardized intensity of selection (26). Whereas
i> 0.4 can be sustained in laboratory artificial
selection for nine generations (27), studies in
nature (26) indicate that i> 0.4 computed on
an annual basis are rare (<5%). We also refer-
ence ito other anthropogenic causes of selection.
Overfishing of Atlantic cod yielded i=0.55,
among the highest measured, but this selection
regime caused demographic collapse of the fish-
ery (28). In México, extinct sites sustained sig-
nificantly higher ithan persistent sites ðiextinct ¼
0:34 T0:05 versus ipersistent ¼0:13 T0:02, t¼
4:17, P<0:001Þ. The relation between inten-
sity of selection and demographic collapse is
simple. If sustained for decades, the mortality
fraction necessary for selective shifts to new opti-
ma compromises population growth rate precip-
itating local extinction.
If climate change Tmax
˙
continues unabated in
México, 56% of viviparous sites will be extinct
by 2050 and 66% by 2080 (Fig. 2B). For
oviparous sites, 46% will be extinct by 2050
and 61% by 2080. Based on local extinction of
all populations surveyed for species, we project
58% species extinction of Mexican Sceloporus
by 2080. Species extinction (58% by 2080) mir-
rors local population extinction (61 to 66%) be-
cause high-elevation endemics will go completely
extinct as widespread lowland taxa expand to
high elevations.
We used the model to derive global extinc-
tion projections (Fig. 3) for 34 lizard families
(Table 1) with 1216 geo-referenced T
b
records
(table S6). Our data include heliotherms that
bask and thermoconformers that do not bask,
but track ambient air and surface temperature.
T
max
was obtained from the WorldClim database
(29)at10–arc min resolution (1975, 2020, 2050,
and 2080). We used distributional limits of he-
liothermic lizards of the world in 1975 to cal-
ibrate h
r
by family, which if exceeded at a given
site would precipitate extinction. The extinction
model is easily adapted to thermoconformers that
maintain T
b
close to T
air
or retreat when T
air
>
T
preferred
.AssumingasinewaveforT
air
between
T
min
and T
max
(24-hour period), if the cumulative
hours that T
air
>T
b
for a thermoconformer at a
given geo-referenced site (table S6) exceeded
the h
r
of a given lizard family, we assumed it
would go extinct. Given T
max
−T
b
at each geo-
referenced site, we computed the h
r
each species
sustained in 1975, and for each family we used
1
Department of Ecology and Evolutionary Biology, University of
California, Santa Cruz, CA, 95064, USA.
2
Laboratorio de
Herpetología, Instituto de Biología, Universidad Nacional
Autónoma de México, D.F., 04510, México.
3
Department of
Biology, Ohio University, 131 Life Sciences Building, Athens,
OH 45701, USA.
4
CNRS UMR 6553, Station Biologique,
35380 Paimpont, France.
5
Laboratorio de Biología de la
Reproducción Animal, Departamento de Biología Comparada,
Facultad de Ciencias, Universidad Nacional Autónoma de
México, D.F., 04510, México.
6
Instituto de Ciencias Naturales,
Universidad Nacional de Colombia, Sede Bogotá, Colombia.
7
Instituto de Ecología, A.C., Miguel de Cervantes No. 120
(Cubículo 30C), Complejo Industrial, C.P. 31109, Chihuahua,
México.
8
Centro Nacional Patagónico, Consejo Nacional de
Investigaciones Científicas y Técnicas, Blvd. Brown 2915,
U9120ACD, Puerto Madryn, Chubut, Argentina.
9
Museo
Nacional de Ciencias Naturales, CSIC, C/ José Gutiérrez, Abascal
2, 28006 Madrid, Spain.
10
Universidad de Concepción, Dpto.
Zoología, Casilla 160-C, Concepción, Chile.
11
Department of
Ecology, Institute of Biology, Universidade do Estado do Rio de
Janeiro, Rua São Francisco Xavier 524, Maracanã 20550-019,
Rio de Janeiro, Brazil.
12
Instituto de Investigación en Biodiversi-
dad y Medio Ambiente (INIBIOMA), Consejo Nacional de
Investigaciones Científicas y Técnicas, Centro Regional Uni-
versitario Bariloche, Universidad Nacional del Comahue,
Quintral 1250, San Carlos de Bariloche, Río Negro 8400,
Argentina.
13
Departamento de Herpetología, Museo de
Historia Natural, Universidad Nacional Mayor de San Marcos,
Av. Arenales 1256, Jesús María Apdo 14-0434, Lima 14, Perú.
14
Laboratoire Ecologie-Evolution, Université UPMC, CNRS UMR
7625, 7 quai Saint Bernard, 75005 Paris, France.
15
Station
d'Ecologie Expérimentale du CNRS a Moulis USR 2936, Moulis,
09200 Saint-Girons France.
16
Centre of Excellence in Evolu-
tionary Research, Department of Biological and Environmental
Science, Post Office Box 35, FI-40014, University of Jyväskylä,
Finland.
17
School of Biological Sciences, Monash University,
Victoria 3800, Australia.
18
Department of Biology, Villanova
University, 800 Lancaster Avenue, Villanova, PA 19085, USA.
19
Bayworld, Post Office Box i13147, Humewood 6013, South
Africa.
20
Department of Biology and Bean Life Science Museum,
Brigham Young University, Provo, UT 84602, USA.
*To whom correspondence should be addressed. E-mail:
lizardrps@gmail.com
†Present address: Laboratoire d'Etude Environnementales des
Systèmes Anthropisés (LEESA), UFR Sciences, 2 Bd Lavoisier,
49045 Angers cedex 01, France.
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the upper 95% confidence level of h
r
(Table 1)
as the extinction threshold (iteratively estimated,
given global climate surfaces). Calibration with
these 1975 distributional limits for Sceloporus
yields h
r
= 3.9, which was cross-validated by
h
r
= 3.85 computed from observed extinctions
in México (1975 to 2009), and h
r
= 4, which
was estimated directly from T
e
at persistent
S. serrifer sites on the verge of extinction.
Fig. 1. (A) Logistic regression of
extinction probability (0 = extant,
1 = extinct) of Sceloporus lizards
and reproductive mode: c
2
= 7.41,
P=0.025,Delevation (c
2
=8.53,
P=0.014),Dlatitude (c
2
=7.14,P=
0.004), and Dlongitude (not signif-
icant), where Drefers to deviations
from species range midpoints. (B)
Phylogenetic independent contrasts
(PICs) of lineage survival (survival
probability of local populations)
and Delevation (t= 2.15, P=0.03),
Dlatitude (t=3.94,P= 0.0001),
and Dlongitude (t = 2.66, P=
0.009). (C) PICs of lineage surviv-
al, T
b
(t= 2.32, P= 0.02), T
air
(t=
2.31, P= 0.02), and reproductive
mode (t=−2.92, P= 0.005).
∆ Latitude ∆ Longitude
∆ Elevation
PIC ∆ Latitude PIC ∆ LongitudePIC ∆ Elevation
-1
0
1
-2000 -1000 0
-1
0
1
-
6 -4 -2 0 2 4 6 8
-1
0
1
0 2 4 6-8 -6 -4 -21000
PIC Lineage Survival
PIC Lineage Survival
PIC Lineage Survival
Extinct
Extant
Extinct
Extant
Extinct
Extant
-8 -6 -4 -2 0 2 4 6 8
-1000 0 1000 -6 -4 -2 0 2 4 6
A
B
C
-0.25
-0.20
-0.15
-0.10
-0.05
0.00
0.05
0.10
0.15
-
4 -3 -2 -1 0 1 2 3
-0.25
-0.20
-0.15
-0.10
-0.05
0.00
0.05
0.10
0.15
-10 -5 0 5 10
-0.25
-0.20
-0.15
-0.10
-0.05
0.00
0.05
0.10
0.15
-0.60 -0.30 0.00 0.30 0.60
PIC Air Temperature (° C)PIC Body Temperature (° C)
PIC Lineage Survival
PIC Lineage Survival
PIC Lineage Survival
PIC Oviparity-Viviparity
viviparous
oviparous
Fig. 2. (A) Sustained selection differentials per year required for T
b
to keep pace with global warming. (B) Extinctions of Mexican Sceloporus lizards
(1975 to 2009, 2009 to 2050, 2050 to 2080).
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As in the validation of Mexican Sceloporus
extinction, we computed h
r
for temperate lizards
over 2 critical reproductive months, but were
conservative in modeling critical months re-
quired for h
r
to be exceeded in the equatorial
zone (T12° latitude) where lizards potentially
breed year-round (h
r
exceeded over 12 months),
and in the wet-dry tropical zone (T12° to 24°
latitude: h
r
exceeded for 5 to 6 months).
Geo-referenced T
b
samples indicate that current
(2009) local extinctions average 4% worldwide
(Table 1). Global averages will increase fourfold
to 16% by 2050 and nearly eightfold to 30% by
2080, while equatorial extinctions will reach 23%
by 2050 and 40% by 2080. Assuming reproduc-
tion shifts 1 month earlier in temperate zones [h
2
=
1.0 lay date (30)] and proportionately less to the
trade zones (i.e., no shift), 2080 global extinctions
jump to 38% because spring seasons are warm-
ing faster across the globe. Our model is robust
to plasticity in T
b
(table S7) and initial assump-
Fig. 3. Contour plots of global levels of local extinction for heliothermic lizards (1975 to 2009, 1975 to 2050, 1975 to 2080), assuming hr= 4.55
(23) and various T
b
values.
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tions made for reproductive periods in the tropics.
If h
r
for equatorial taxa is computed over the 9
hottest months of reproduction, rather than the
conservative assumption of 12 months, global
extinctions increase to 39% by 2080.
The global generality of our model is verified
by concordant distributions of current observed
and predicted local extinctions of lizard biotas
from four other continents (table S7). Our model
pinpoints exact locations of two Liolaemid species
going extinct in South America (Liolaemus lutzae,
Phymaturus tenebrosus:c
2
=32.1,P< 0.0001).
In addition, the model predicts recent (2009)
extinctions among 24 resurveyed populations of
L. lutzae (c
2
=8.8,P= 0.003). In Europe, our
Table 1. Sample size, T
b
range, TbTSE,Tmax ,h
r
,andn
species
for 34 lizard
families. Local extinction rates are based on geo-referenced T
b
data and a
physiological model of extinction. We also validated model predictions of local
extinction risk in 2080 for six families: 57% (T3, n= 200) for Mexican
Phrynosomatidae, 13% (T2, n= 3155) for South American Liolaemidae, 56%
(T5, n= 117) for European Lacertidae (L. vivipara), 13% (T2, n= 1438) for
African Cordylidae + Gerrhosauridae, 57% (T4, n= 125) on Madagascar, and
10% (T1, n= 2841) for Australian Egernia Group lizards species. Estimates of
species extinctions in each family are derived from the relationships for
extinction of all local populations for these six families (table S8).
Family nT
b
range Tb±SE Tmax h
r
Mode of
thermoregulation
Local extinction levels Species extinction
n
spp
2009 2050 2080 2050 2080
Agamidae 74 19.0–43.8 35.6T0.34 29.8 7.0 Heliothermic 381 0.000 0.169 0.292 0.059 0.266
Amphisbaenidae 2 21.1–21.2 21.2T0.05 28.8 16.2 Fossorial
thermoconformer
160 0.000 0.000 0.250 0.000 0.228
Anguidae 10 21.4–32.3 26.7T0.94 20.9 5.6 Heliothermic, a few
fossorial
112 0.111 0.111 0.111 0.039 0.101
Annielliidae 2 21.0–23.6 22.3T2.09 20.5 11.5 Fossorial
thermoconformer
2 0.000 0.000 0.000 0.000 0.000
Chamaeleonidae 18 22.2–33.5 30.0T0.70 26.8 12.0 Forest
thermoconformer
161 0.063 0.063 0.063 0.022 0.057
Cordylidae 11 27.8–33.8 31.5T0.82 23.6 6.8 Heliothermic 54 0.000 0.000 0.200 0.000 0.182
Corytophanidae 4 26.0–35.0 31.9T1.48 29.4 13.4 Forest
thermoconformer
9 0.250 0.250 0.250 0.088 0.228
Crotaphytidae 23 35.5–38.9 37.3T0.62 23.3 1.2 Heliothermic 12 0.111 0.167 0.222 0.059 0.202
Carphodactylidae 11 15.1–35.5 24.5T1.59 34.7 10.9 Thermoconformer 30 0.350 0.820 0.820 0.289 0.748
Diplodactylidae 42 16.9–35.9 27.3T0.59 31.2 10.9 Thermoconformer 141 0.070 0.190 0.190 0.067 0.173
Eublepharidae 18 26.6–33.0 28.5T0.44 32.9 10.9 Thermoconformer 28 0.060 0.240 0.240 0.084 0.219
Gekkonidae 40 26.0–35.3 30.1T0.58 32.6 10.9 Thermoconformer 700 0.000 0.000 0.000 0.000 0.000
Phyllodactylidae 13 16.6–38.9 30.6T1.42 30.4 10.9 Thermoconformer 100 0.000 0.000 0.000 0.000 0.000
Pygopodidae 21 24.9–35.1 25.4T0.46 17.9 11.5 Fossorial
thermoconformer
38 0.000 0.000 0.000 0.000 0.000
Sphaerodactylidae 19 25.3–38.6 30.2T0.75 33.0 10.9 Thermoconformer 200 0.000 0.000 0.000 0.000 0.000
Gerrhosauridae 4 31.8–33.3 32.6T2.09 28.3 6.8 Heliothermic 16 0.333 0.333 0.333 0.117 0.304
Gymnophthalmidae 20 21.5–29.9 26.4T0.66 30.3 13.8 Leaf litter
thermoconformer
193 0.095 0.333 0.667 0.117 0.608
Helodermatidae 2 29.4–30.2 29.8T2.09 24.8 2.7 Heliothermic/thermal
inertia
2 0.000 0.000 1.000 0.000 0.912
Iguanidae 20 32.9–42.1 37.3T0.79 28.1 3.7 Heliothermic 36 0.143 0.143 0.286 0.050 0.261
Lacertidae 89 26.7–40.2 35.4T0.31 25.6 3.1 Heliothermic 279 0.034 0.241 0.460 0.085 0.420
Lanthanotidae 1 –28.0 30.5 9.4 Forest
thermoconformer
1 1.000 1.000 1.000 0.352 0.912
Leiocephalidae 1 –36.3 31.7 2.8 Heliothermic 29 0.000 1.000 1.000 0.352 0.912
Liolaemidae 125 24.4–40.8 33.7T0.27 17.8 1.4 Heliothermic 219 0.027 0.071 0.107 0.025 0.098
Opluridae 3 36.2–39.8 37.7T1.71 31.8 4.0 Heliothermic 7 0.333 0.667 0.667 0.235 0.608
Phrynosomatidae 215 26.8–41.5 35.2T0.20 24.9 3.9 Heliothermic 125 0.037 0.087 0.149 0.031 0.136
Polychrotidae 121 19.6–35.0 29.6T0.27 29.6 14.4 Forest
thermoconformer
393 0.018 0.043 0.068 0.015 0.062
Scincidae 210 20.3–38.0 32.9T0.20 26.5 6.2 Heliothermic, a few
fossorial
1305 0.015 0.092 0.308 0.032 0.281
Sphenodontidae 1 14.5–21.0 14.5T2.09 18.0 10.7 Nocturnal
thermoconformer
1 0.000 0.000 0.000 0.000 0.000
Teiidae 91 26.8–41.3 37.9T0.31 29.0 4.2 Heliothermic 121 0.012 0.136 0.210 0.048 0.192
Trogonophidae 2 22.0–22.5 22.3T0.25 28.8 16.2 Fossorial
thermoconformer
8 0.000 0.000 0.000 0.000 0.000
Tropiduridae 72 26.2–38.0 33.7T0.35 28.3 7.7 Heliothermic 111 0.043 0.058 0.087 0.020 0.079
Varanidae 46 28.8–38.9 35.8T0.44 29.7 4.6 Heliothermic/thermal
inertia
68 0.001 0.023 0.178 0.008 0.162
Xantusidae 8 18.7–33.0 25.4T1.32 20.7 0.0 Thigmothermic
thermoconformer
29 0.000 0.000 0.000 0.000 0.000
Xenosauridae 5 20.3–25.6 23.2T1.48 26.4 11.4 Thigmothermic
thermoconformer
6 0.200 0.200 0.600 0.070 0.547
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resurvey of Lacerta vivipara revealed 14 extinct
sites out of 46 (30%), which are predicted quite
precisely by the model (c
2
=24.4,P< 0.001). In
Australia, the model pinpoints 2009 extinctions
of Liopholis slateri (c
2
= 17.8, P< 0.00001) and
2009 extinctions of Liopholis kintorei (c
2
= 3.93,
P= 0.047). In Africa, analysis of Gerrhosauridae
and Cordylidae at 165 sites predicts <1% extinc-
tions, and yet the model pinpoints the single ex-
tinction reported by 2009 (exact P-value = 0.006).
We temper this value with extinction projections
of 23% for 2009 at Malagasy Gerrhosauridae sites,
which is validated by the observed 21% levels
of local extinction across several lizard families
in Madagascar nature reserves (23).
Thermoconforming lizards have been posited
(31) to be more vulnerable to climate change
relative to heliotherms. Even though Tbof ther-
moconformers (27.5°C T1.8°) is significantly
less than Tbof heliotherms (33.5ºC T1.3, t=
2.66, P< 0.02, n= 34 families; Table 1), PICs
show that extinction risk was unrelated to ther-
moregulatory mode (fig. S8), but was signifi-
cantly increased by low Tb,lowh
r
, and high
Tmax. The similar level of local extinctions in
2009 for Malagasy thermoconformers (21%, n=
63) and heliotherms [21%, n= 34; (23)] supports
this view. Evolved changes in thermoregulatory
mode, T
b
,h
r
, lay date, and habitat preference set
risk as T
max
rises, but owing to trade-offs, T
b
and
h
r
cannot be simultaneously maximized, hence
extinction risk is independent of mode (fig. S8).
Moreover, extinction risk is not higher for con-
formers because heliotherms inhabit equatorial
regions (i.e., sub-Saharan Africa) that are un-
available to thermoconformers [a factor not con-
sideredby(31)orothermodels(10)], and these
areas are warming rapidly (Fig. 3).
Our model, based on T
b
,h
r
in activity during
reproduction, and timing of breeding, assesses
salient adaptations that affect thermal extinc-
tions. Concordant verification of 2009 levels of
local lizard extinction in North and South Amer-
ica, Europe, Africa, and Australia confirm that
extinctions span tropical, temperate, rainforest,
and desert habitats. Estimates of evolutionary
rates required to keep pace with global change
indicate that sustained and intense selection
compromises population growth rates, precip-
itating extinctions. Probability of local extinction
is projected to result in species extinction prob-
abilities of 6% by 2050 and 20% by 2080 (table
S8). Range shifts only trivially offset losses, be-
cause widespread species with high T
b
shift to
ranges of endemics, thereby accelerating their
demise. Although global efforts to reduce CO
2
may avert 2080 scenarios, 2050 projections are
unlikely to be avoided; deceleration in Tmax
˙
lags
atmospheric CO
2
storage by decades (4). There-
fore, our findings indicate that lizards have al-
ready crossed a threshold for extinctions.
References and Notes
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Society, UC Mexus, UCSC Committee-On-Research, NSF
awards (DEB 0108577, IBN 0213179, LTREB DEB
051597), CNRS fellowships, and visiting professorships
(Museum Nationale d’Histoire Naturelle, Université Paris
6, Université Paul Sabatier Toulouse III), PAPIIT-UNAM
IN213405 and 224208 to F.M.-C., a Université Paul
Sabatier Toulouse III Visiting Professorship to D.B.M.,
CONACYT grants (4171N and 52852Q) to M.V.-S.C.,
grant CONACYT-SEP (43142-Q) to H.G., a CONACYT
fellowship to R.N.M.-L., CNRS funding to B.H., and M.M.,
Biodivera: Tenlamas and from ANR Blanche: DIAME
to J.C., CONICET grants to L.J.A. and M.M., FONDYCET
1090664 grants to P.V.S., CGL2005-03156 and
CLG2008-04164 grant from SMSI to I.J.R., APCT-
PICT1086 grant to N.I., scholarships and grants from
Universidad Nacional Autónoma de México and American
Museum of Natural History to M.V.-S.C., Academy of
Finland grant (108955) to T.A.O., Australian Research
Council grants to D.G.C., NSF awards DEB 0515909
and 0844523 to A.M.B., NSF award OISE 0530267,
PIRE-Patagonia grant to J.W.S., L.J.A., M.M., and P.V.S.
and Brigham Young University funding (Biology
Department, Kennedy Center for International Studies,
Bean Life Science Museum) to J.W.S.
Supporting Online Material
www.sciencemag.org/cgi/content/full/328/5980/894/DC1
Materials and Methods
Figs. S1 to S9
Tables S1 to S8
References
16 November 2009; accepted 7 April 2010
10.1126/science.1184695
Carbon Dioxide Enrichment Inhibits
Nitrate Assimilation in Wheat
and Arabidopsis
Arnold J. Bloom,*Martin Burger,†Jose Salvador Rubio Asensio, Asaph B. Cousins‡
The concentration of carbon dioxide in Earth’s atmosphere may double by the end of the
21st century. The response of higher plants to a carbon dioxide doubling often includes a decline
in their nitrogen status, but the reasons for this decline have been uncertain. We used five
independent methods with wheat and Arabidopsis to show that atmospheric carbon dioxide
enrichment inhibited the assimilation of nitrate into organic nitrogen compounds. This inhibition
may be largely responsible for carbon dioxide acclimation, the decrease in photosynthesis and
growth of plants conducting C
3
carbon fixation after long exposures (days to years) to carbon
dioxide enrichment. These results suggest that the relative availability of soil ammonium and
nitrate to most plants will become increasingly important in determining their productivity
as well as their quality as food.
The concentration of CO
2
in Earth’satmo-
sphere has increased from about 280 to 390
mmol CO
2
per mol of atmosphere (mmol
mol
–1
) since 1800, and predictions are that it will
reach between 530 and 970 mmol mol
–1
by the end
of the 21st century (1). Plants could mitigate these
changes through photosynthetic conversion of
atmospheric CO
2
into carbohydrates and other
organic compounds, yet the potential for this miti-
gation remains uncertain. Photorespiration is the
biochemical pathway in which the chloroplast
enzyme Rubisco catalyzes the oxidation of the
high-energy substrate RuBP rather than cata-
lyzes the carboxylation of RuBP through the C
3
carbon-fixation pathway (2). Elevated CO
2
(or
Department of Plant Sciences, University of California at Davis,
Davis, CA 95616, USA.
*To whom correspondence should be addressed. E-mail:
ajbloom@ucdavis.edu
†Present address: Department of Land, Air and Water Resources,
University of California at Davis, Davis, CA 95616, USA.
‡Present address: School of Biological Sciences, Post Office
Box 646340, Washington State University, Pullman, WA
99164–6340, USA.
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