Opinion TRENDS in Ecology & Evolution Vol.17 No.

10 October 2002 457

Rising atmospheric simplicity a nd rigor ([1], I. Lola dze, PhD thesis,

Arizona Sta te University 2001). A cell conta ins
thousa nds of complex substa nces, but a ll life requires

CO2 and human ~32 different chemica l elements [2]. Life continuously
a ssembles a nd disa ssembles complex substa nces,
but it ca n neither crea te nor decompose chemica l

nutrition: toward elements, a nd it ca nnot convert one element into

a nother. These elementa l la ws a re ra ther
self-evident, but a re frequently overlooked in our

globally imbalanced perception of biologica l dyna mics. Yet the universa lity
a nd certa inty of these la ws, which a re va lid on a ll
orga niza tiona l sca les, from molecules to the

plant stoichiometry? biosphere, provide a unified fra mework tha t helps to

revea l pa tterns hidden on dispa ra te orga niza tiona l
sca les. The stoichiometric a rgument tha t I discuss
here dra ws on multiple sca les, from the structure of
Irakli Loladze ca rbohydra tes to a pla nt cell to a n a gricultura l plot to
globa lly rising [CO 2].

Terrestrial vascular plants obtain their major constituent – carbon (C) – from
atmospheric carbon dioxide (CO2), but draw all other chemical elements largely
from the soil. Concentrations of these elements, however, do not change in
unison w ith steadily increasing concentrations of CO2 [CO2]. Thus, relative to
pre-industrial times, modern plants are experiencing a global elemental
imbalance. Could this imbalance affect the elemental composition of plants,
the most important food source on Earth? Apart from an overall decline in
nitrogen concentration, very little is know n about the effects of high [CO2]
on other chemical elements, such as iron, iodine and zinc, w hich are already
deficient in the diets of the half of human population. Here, I apply stoichiometric
theory to argue that high [CO2], as a rule, should alter the elemental
composition of plants, thus affecting the quality of human nutrition. The first
compilation, to my know ledge, of published data supports the claim and show s
an overall decline of the (essential elements):C ratio. Therefore, high [CO2]
could intensify the already acute problem of micronutrient malnutrition.
Published online: 8 August 2002
The increa sing concentra tion of a tmospheric ca rbon
dioxide CO 2 a nd the qua lity of our nutrition a re two
importa nt problems tha t we a re currently fa cing.
A link between these two problems, however, is not
a ppa rent. Indeed, intensive a nd numerous studies on
the effects of high [CO 2] on pla nts ha ve covered a wide
ra nge of issues, but its effects on pla nt stoichiometry
(i.e. elementa l composition) ha ve received very little
a ttention. Yet, pla nts a re the founda tion of our food
supply. The low concentra tions of severa l essentia l
micronutrients, such a s iron (Fe), iodine (I) a nd
zinc (Zn), in modern crops contribute to the problem of
micronutrient malnutrition (i.e. ‘hidden hunger ’), which
diminishes the hea lth a nd economy of over the ha lf of
the world’s popula tion. Here, by using the theory of
ecological stoichiometry, I can link high [CO2] with plant
stoichiometry and the quality of human nutrition. The
Irakli Loladze
tools of ecological stoichiometry are chemical elements
Dept of Ecology and and their ratios in organisms and the environment.
Evolutionary Biology,
Princeton University,
How can stoichiometry provide insight?
Princeton, NJ 08544, USA.
e-m ail: Ana lysing biologica l dyna mics from a chemica l
iloladze@princeton.edu element perspective ha s a dva nta ges in both its
The need for essential elements and the problem of
micronutrient malnutrition
The huma n body needs a t lea st 24 chemica l elements.
Although some of the elements, such as chromium (Cr),
F e, I, selen iu m (Se), or zin c (Zn ), com pr ise <0.01% of
h u m a n body weigh t , t h eir a bsen ce r en der s ou r life
im possible. Beca u se t h e h u m a n or ga n ism ca n n ot
gen er a t e a n y elem en t t h a t is lost t h r ou gh excr et ion ,
we m u st r eplen ish it fr om ou r food. P la n t s a r e t h e
ba sis of h u m a n n u t r it ion , pr ovidin g a st a gger in g
84% of ca lor ie in t a ke wor ldwide [3]. Alm ost h a lf of
t h is com es fr om t wo st a ple cr ops: r ice a n d wh ea t [3].
Con cen t r a t ion s of sever a l essen t ia l elem en t s in
m oder n cr ops a r e in su fficien t for opt im a l h u m a n
n u t r it ion , t h u s con t r ibu t in g t o t h e en or m ou s ‘h idden
h u n ger ’pr oblem [4–6]. Ir on deficien cy a ffect s
>3.5 billion people, m ost ly in t h e developin g wor ld,
a n d ‘im pa ir s t h e cogn it ive developm en t of ch ildr en ,
ca u ses pr odu ct ivit y a n d edu ca t ion a l losses, a n d
in cr ea ses m or bidit y a n d m a t er n a l m or t a lit y’[4].
Iodin e deficien cy is a pu blic h ea lt h pr oblem in a t
lea st 130 cou n t r ies, wit h over seven h u n dr ed m illion
people su ffer in g fr om goit r e a n d t en s of m illion s
a fflict ed by br a in da m a ge a n d cr et in ism [4]. Nea r ly
h a lf of t h e wor ld’s popu la t ion is a t r isk of in a dequ a t e
Zn in t a ke [5]. Deficien cies of ot h er essen t ia l
elem en t s a r e a lso widespr ea d, even in in du st r ia l
cou n t r ies, bu t oft en a r e n ot m a n ifest ed in over t
clin ica l syn dr om es.
Global imbalance of essential elements and
plant stoichiometry
H u m a n a ct ivit ies pr ofou n dly a lt er t h e globa l cycles of
sever a l essen t ia l elem en t s [1,7]. Th e pu r su it of
h igh er a gr icu lt u r a l yields, r a t h er t h a n cr op
qu a lit y, fer t ilizes soil dispr opor t ion a t ely wit h N,
ph osph or u s (P ), a n d pot a ssiu m (K). F ossil-fu el
bu r n in g a dds N a n d su lph u r (S) via a t m osph er ic
deposit ion a n d, t oget h er wit h ch a n ges in la n d u se,
in cr ea ses [CO 2 ]. Th u s, h u m a n a ct ivit ies h a ve been
a lt er in g t h e pool of a few essen t ia l elem en t s in sever e

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458 Opinion TRENDS in Ecology & Evolution Vol.17 No.10 October 2002
dispr opor t ion t o ot h er s. Rela t ive t o pr e-in du st r ia l
t im es, we h a ve been r a pidly cr ea t in g a globa l
elem en t a l im ba la n ce. Ca n t h is im ba la n ce, in t u r n ,
a ffect u s by a lt er in g t h e st oich iom et r y of ou r
fu n da m en t a l food sou r ce – pla n t s? To a n swer t h is
question, I concentra te here on the role of rising [CO 2 ]
for t h e followin g t h r ee r ea son s.
F ir st , u n like t h e con t r over sy su r r ou n din g t h e
effect s of [CO 2 ] on clim a t e ch a n ge, t h e in cr ea se
in [CO 2 ] it self is con fir m ed by sever a l in depen den t
sou r ces [8]. Cu r r en t ly, ever y t er r est r ia l pla n t is
exposed t o ~30% h igh er [CO 2 ] r ela t ive t o
pr e-in du st r ia l t im es; du r in g t h is cen t u r y [CO 2 ]
levels cou ld dou ble or t r iple over pr e-in du st r ia l
levels [8]. Th is in cr ea se is in st a n t a n eou s on a
geologica l t im esca le a n d is u n pr eceden t ed in t h e
h ist or y of t h e h u m a n species. Beca u se a m oder n t r ee
m igh t exper ien ce t h e dou blin g of [CO 2 ] over it s
lifet im e, su ch a n in cr ea se is a lso ver y fa st on
evolu t ion a r y a n d even on t ogen et ic t im esca les.
Secon d, pla n t s bu ild t h e bu lk of t h eir dr y weigh t by
fixin g C fr om CO 2 . Th ir d, beca u se of t h e ga seou s
pr oper t ies of CO 2 a n d h igh m ixin g r a t es in t h e
a t m osph er e, n o ot h er h u m a n im pa ct com pa r es t o
r isin g [CO 2 ] in it s u n ifor m it y. P la n t s wor ldwide,
bot h a gr icu lt u r a l a n d wild, a r e exposed t o ver y
sim ila r [CO 2 ] con cen t r a t ion s. F or t h ese r ea son s,
globa l pa t t er n s in t h e ch a n ges of pla n t
st oich iom et r y ca n pr eva il in spit e of loca l
en vir on m en t a l h et er ogen eit y (t em per a t u r e,
h u m idit y, fer t ilizer s, et c.).
Plants in enriched CO2 atmospheres
Th e effect s of h igh [CO 2 ] on pla n t st oich iom et r y h a ve
r eceived lit t le a t t en t ion , bu t it s effect s on ot h er pla n t
ch a r a ct er ist ics h a ve been t h or ou gh ly st u died.
F r ee-Air CO 2 E n r ich m en t (FACE ) exper im en t s
h a ve been r u n n in g a t 32 loca t ion s wor ldwide a n d
>2700 st u dies h a ve been pu blish ed in t h e pa st deca de
a lon e [9]. Dou blin g a m bien t [CO 2 ] gen er a lly
st im u la t es ph ot osyn t h esis, en h a n ces pla n t gr owt h
a n d in cr ea ses a gr icu lt u r a l yields, on a ver a ge,
by 41% [10–13]. Th ese ben efit s, h owever, becom e
qu est ion a ble if en r ich ed [CO 2 ] a lt er s cr op
st oich iom et r y. Th a t ch em ica l com posit ion of pla n t s
ca n ch a n ge u n der in cr ea sed [CO 2 ] h a s been
su ggest ed [e.g. 1,7,10], bu t m u ch of t h e exper im en t a l
wor k h a s ign or ed ch em ica l elem en t s a n d h a s
in st ea d focu sed on com plex com pou n ds, m a n y of
wh ich sh ow lit t le con sist en cy in t h eir r espon se t o
h igh [CO 2 ] [14,15]. A clea r pa t t er n , h owever, exist s
for N, t h e on ly elem en t wh ose con cen t r a t ion s in
pla n t s u n der con dit ion s of h igh [CO 2 ] h a ve been
st u died ext en sively. Th e m et a -a n a lysis of t h e
con cen t r a t ion s of N in a bovegr ou n d pla n t t issu es
r evea led, on a ver a ge, a 14% declin e in it s
con cen t r a t ion s u n der h igh [CO 2 ] levels [16].
Micr oelem en t s, su ch a s F e, I, a n d Zn , in pla n t s a r e
vit a l for h u m a n h ea lt h , bu t lit t le is kn own a bou t
t h eir r espon se t o h igh [CO 2 ]. Not a sin gle st u dy,
http://tree.trends.com
t o m y kn owledge, a n a lyses t h e effect s of h igh [CO 2 ]
on t h e con cen t r a t ion s of Se, wh ich is a n im por t a n t
a n t ioxida n t , or Cr, wh ich is ext r em ely im por t a n t in
t h e r egu la t ion of blood-su ga r levels a n d wh ich is
pr oba bly deficien t in h u m a n n u t r it ion [17].
Th e obscu r it y of da t a m igh t expla in wh y n o
com pr eh en sive r eview exist s a bou t t h e effect s of
h igh [CO 2 ] on pla n t st oich iom et r y a n d wh y it s r ole in
m icr on u t r ien t m a ln u t r it ion h a s n ot been a ddr essed.
As St er n er a n d E lser [1] poin t ou t ‘t h e lim it ed a n d
diffu se da t a on elem en t a l com posit ion …r esu lt in
lit t le a wa r en ess a n d lit t le a bilit y t o per ceive pa t t er n s
of in t er est ’, wh ich in t u r n ‘r esu lt in lit t le n ew da t a
bein g gen er a t ed a n d lit t le effor t a t com pilin g t h ose
a lr ea dy a va ila ble’. In lieu of r ea l exper im en t s on
pla n t st oich iom et r y u n der in cr ea sed [CO 2 ],
I h a ve r u n a ‘t h ou gh t exper im en t ’(see below).
Su ch ‘exper im en t s’a r e con ven t ion a lly r eser ved for
in h er en t ly sim pler ph ysica l r a t h er t h a n biologica l
syst em s, bu t t h e r elia n ce on st oich iom et r y sim plifies
t h e biology a n d pr ovides su fficien t r igor t o ga in
a n in sigh t in t o t h e effect of in cr ea sed [CO 2 ] on
pla n t st oich iom et r y.
A FACE ‘thought experiment’
Two underpinnings of ecologica l stoichiometry a re
useful when running a FACE ‘experiment’:
(1) a self-evident but importa nt fa ct tha t orga nisms
ca nnot crea te or convert elements; a nd (2) the
proportions of elements in a pla nt cell ca n va ry
widely, la rgely beca use of the presence of a la rge
centra l va cuole, which is unique to pla nt cells [1];
for exa mple, Fe or Zn content ca n va ry tenfold or more
in gra ss fora ge [18].
Suppose tha t a terrestria l va scula r pla nt, for
exa mple whea t, ha s been grown on two plots, A a nd B,
in identica l conditions, except tha t [CO2] is a mbient
in A but is doubled in B. If the dry weight of the
sta nding stock in B is δ % higher tha n in A, a re the
stoichiometries of A pla nts a nd B pla nts different?
Even though the a mounts of ea ch individua l element
in the soil were the sa me in the two plots, the higher
bioma ss in plot B is the result of stimula ted
photosynthesis tha t increa sed ca rbohydra te
production. If the increa se in ca rbohydra tes, the
chief constituent of plants, had been the only difference
between the two plots, then the C, oxygen (O)
a nd hydrogen (H) content in B pla nts would differ
very little from tha t in A pla nts (Box 1, Eqn II). But
δ
every other element would ha ve decrea sed by %
1+ δ
(Box 1, Eqn III), which provides a ba seline
estima te of the potentia l shift in the pla nt
stoichiometry. This underlines the dichotomy
between C, O, H (which constitute >90% of the dry
weight of pla nts) a nd other elements. Hence, pa tterns
in the cha nges of pla nt chemica l composition should
be more evident on the chemica l sca le of elements
ra ther tha n on the coa rser sca les of complex
compounds, ma ny of which conta in C, O, H a nd other
elements simulta neously.
 Opinion TRENDS in Ecology & Evolution Vol.17 No.10 October 2002
Box 1. Elemental vectors: the shift in the stoichiometry of B plants
because of carbohydrate dilution
In ecological stoichiom etry, elem ental vectors are very useful because they
provide a sim ple m eans w ith w hich to apply the pow er of m ass balance law s to
every elem ent.
Let (a1,a2,…,an ),(b 1,b 2,…b n ) and (c1,c2,c3,0…,0) denote elem ental vectors
for dry A plants, dry B plants and carbohydrates respectively, w here the first
three term s represents carbon (C), oxygen (O) and hydrogen (H) concentrations
and other term s represent concentrations of every other elem ent. Then
n n n
∑ ai = ∑ bi = ∑ ci =1
.
1 1 1
Let M denote the total dry w eight of A plants. If the δ% increase in biom ass of
B plants is solely because of the increase in carbohydrates, then m ass balance
yields (Eqn I):
M ·(a1,a2,…,an ) + δ·M ·(c1,c2,c3,0…,0) = (1 + δ)·M ·(b 1,b 2,…,b n ) [Eqn I]
ai + δci aj
Thus, b i = , i = 1,2,3 and b j = , j = 4,..., n .. The percentage change in
1+ δ 1+ δ
bi δ c i −a i
concentrations of C, O and H is −1= , i = 1,2,3 but because*
ai 1 + δ ai
the content of these three elem ents in plants and carbohydrates is sim ilar,
(i.e. ai ≈ ci ), it follow s that (Eqn II)
ai ≈ b i , i = 1,2,3 [Eqn II]
For the rest of the elem ents, the percentage change equals to (Eqn III)
bj δ ca n a ga in sh ow t h a t pla n t st oich iom et r y ch a n ges.)
− 1= − , j = 4,..., n . [Eqn III].
aj 1+ δ
The dilution by ca rbohydra tes, however,
is unlikely to be the only difference between A a nd
B pla nts. B pla nts might a da pt to doubled [CO 2]
by cha nging their tra nspira tion, root:shoot ra tio,
root morphology, root a ctivity or symbiotic
association with mycorrhizae. Could these adaptations
equa lize the stoichiometries of A a nd B pla nts by
increa sing the net upta ke of every element by the
sa me percenta ge a s the net increa se in C? I argue
here tha t these a da pta tions could a lter the δ %
decline ca used by ca rbohydra te dilution, 1 + δ
but will not neutra lize it.
Th e plot s A a n d B a r e m on ocu lt u r es, a s a r e m ost
st a ple cr op fields; t h u s, by em ployin g a n y of t h e
a da pt a t ion s list ed a bove, a n in dividu a l B pla n t is
u n likely t o ga in a n y a dva n t a ge r ela t ive t o it s
a lm ost iden t ica l n eigh bou r s. Mor eover, n on e of t h e
a da pt a t ion s per se ca n ch a n ge t h e t ot a l m a ss of
a n y elem en t in t h e plot (except C, O a n d H ),
bu t t h ey do a lt er con dit ion s in t h e soil, in clu din g t h e
st oich iom et r y of soil n ea r r oot s a n d soil m oist u r e.
Beca u se elem en t s differ in t h eir diffu sion r a t es a n d
u pt a ke kin et ics, t h e n et u pt a ke of ea ch elem en t
ca n n ot in cr ea se by t h e sa m e per cen t a ge. F or
exa m ple, a t h igh er con cen t r a t ion s, [CO 2 ] diffu ses
in t o lea ves m or e ea sily, t h u s en a blin g pla n t s t o
n a r r ow st om a t a l a per t u r es a n d con sequ en t ly t o lose
less wa t er, t h a t is t o decr ea ses t r a n spir a t ion . Th is
effect h a s been well docu m en t ed in exper im en t s
wit h dou bled [CO 2 ] on bot h C3 (e.g. r ice a n d wh ea t )
a n d C4 (e.g. m a ize a n d su ga r ca n e) pla n t s wit h a n
a ver a ge 23% r edu ct ion of t r a n spir a t ion [11–13].
http://tree.trends.com
*atypo in Box 1 corrected, I.L.
459
Redu ced t r a n spir a t ion lea ds t o r edu ced m a ss flow in
t h e soil a n d it ca n a lso in cr ea se soil m oist u r e [19].
Th u s, t h e t wo pr im a r y m ech a n ism s t h a t t r a n spor t
elem en t s t o t h e vicin it y of r oot s, m a ss flow a n d
diffu sion , a r e a lt er ed in plot B. Ma ss flow is gen er a lly
m or e im por t a n t for m obile elem en t s, su ch a s N,
a n d diffu sion is m or e im por t a n t for im m obile
elem en t s, su ch a s P. H en ce, t h e ch a n ge in u pt a ke
r a t es sh ou ld be differ en t a m on g elem en t s in plot B.
F u r t h er m or e, in cr ea sed ph ot osyn t h esis pu t s
differ en t ia l in t er n a l dem a n ds on elem en t s. F or
exa m ple, u n der h igh [CO 2 ], pla n t dem a n d ca n
in cr ea se for P bu t decr ea se for N [20,21]. To
su m m a r ize, B pla n t s h a ve h igh er C fixa t ion r a t es,
a lt er ed in t er n a l elem en t a l dem a n ds a n d ch a n ged
a va ila bilit y of elem en t s n ea r r oot s. Th er efor e, A a n d
B pla n t s sh ou ld differ n ot on ly in C:(ot h er elem en t s)
r a t ios bu t a lso in t h e r a t ios a m on g ot h er elem en t s
(e.g. C:N, N:P a n d P :Zn sh ou ld a lso be differ en t ).
In ot h er wor ds, t h e ch a n ge in t h e st oich iom et r y of
B pla n t s sh ou ld be n on u n ifor m a cr oss elem en t s.
H en ce, A pla n t s h a vin g t h e sa m e st oich iom et r y a s
B pla n t s sh ou ld be a n except ion . (If pla n t biom a ss
decr ea ses in h igh [CO 2 ], t h en a sim ila r a r gu m en t
Th er efor e, t h e con clu sion is t h a t h igh [CO 2 ],
a s a r u le, a lt er s pla n t st oich iom et r y.
Are overall patterns possible?
Th e a bove a r gu m en t su ggest s t h a t t h e ch a n ge in t h e
con cen t r a t ion of elem en t s (except C, O a n d H ) m oves
in a n opposit e dir ect ion t o t h e ch a n ge in biom a ss,
bu t it does n ot exclu de t h e possibilit y t h a t levels of
som e elem en t s ca n in cr ea se or r em a in u n ch a n ged
wit h a n in cr ea se in biom a ss u n der h igh [CO 2 ]. F or
h u m a n n u t r it ion , h owever, it is im por t a n t t o kn ow
wh et h er over a ll pa t t er n s wou ld exist in h igh [CO 2 ]
wor ld. Ter r est r ia l va scu la r pla n t s wor ldwide sh a r e
wh a t is fu n da m en t a lly t h e sa m e ph ysiology a n d a r e
exposed t o essen t ia lly t h e sa m e [CO 2 ], su ggest in g
t h a t over a ll pa t t er n s in t h e ch a n ges of pla n t
st oich iom et r y a r e possible. A pa r t icu la r ly dist u r bin g,
bu t pla u sible pa t t er n is on e in wh ich t h e
con cen t r a t ion s of essen t ia l elem en t s, in clu din g
t h ose t h a t a r e a lr ea dy deficien t in t h e diet s of t h e
h a lf of t h e wor ld’s popu la t ion , decr ea se in pla n t s.
As su ggest ed a bove, bot h in cr ea sed ca r boh ydr a t e
a ccu m u la t ion a n d r edu ced m a ss flow ca n lea d t o t h is
pa t t er n . All else bein g equ a l, t h is pa t t er n wou ld
m ea n lower (n u t r it ion a l va lu e):(ca lor ic va lu e) of
cr ops a n d t h e a ggr a va t ion of t h e m icr on u t r ien t
m a ln u t r it ion pr oblem . It wou ld a lso in cr ea se t h e
im per a t ive t o br eed r ice, wh ea t a n d ot h er st a ple
cr ops wit h su per ior a bilit y t o con cen t r a t e essen t ia l
elem en t s su ch a s F e, Zn , I a n d Se [6].
What do the scant published data reveal?
Motiva ted by the conclusion of the ‘thought
experiment’, I sea rched extensively for published
da ta on the effects of high [CO 2] on the elementa l
460 Opinion TRENDS in Ecology & Evolution Vol.17 No.10 October 2002
Element
Change in mean concentration (%)
N P K Ca S Mg Fe Zn Mn Cu
5.0
–5.0
–15.0
–25.0
TRENDS in Ecology & Evolution
Fig. 1. Changes (%) in the m ean concentration of essential elem ents in plants grow n in tw ice-am bient
atm ospheric [CO2] relative to those grow n at am bient levels [all plants (foliar), green; w heat (grains),
yellow ]. The figure is based on 25 studies covering 19 herbaceous and 11 w oody plant species,
and five w heat cultivars [21,24–47], in w hich m ultiple elem ents w ere m easured under increased
concentrations of atm ospheric carbon dioxide [CO2]. If several [CO2] levels w ere reported, the data for
the levels closest to the am bient and tw ice-am bient w ere used. The studies w ith superenriched or
naturally high [CO2] w ere excluded. M ultiple data for a single species or a cultivar w ere averaged
before calculating m eans. Error bars indicate the standard error of the m ean; for foliar data, n = 30 for
nitrogen (N), phosphorous (P), and potassium (K), 29 for calcium (Ca), 26 for m agnesium (M g),
14 for iron (Fe) and m anganese (M n), 12 for zinc (Zn), 9 for sulphur (S) and copper (Cu); for w heat
grains, n = 5 for N, P, K, Ca, M g, Fe and Zn, and 3 for S and M n. Upon request, I w ill gladly provide a
detailed table w ith all the data on w hich this figure is based.
composition of pla nts. The da ta a re surprisingly
sca nt. I hope tha t the sca rcity a nd importa nce of the
da ta will encoura ge the genera tion of new da ta on the
cha nges in pla nt stoichiometry ca used by a globa lly
a ltered environment. It is sta rtling tha t, a mong
thousa nds of publica tions on doubled [CO 2], only one
investiga ted its effects on the gra in stoichiometry of
rice, the world’s most importa nt crop [22]. This study
found decrea sed concentra tions of four out of five
mea sured elements in brown rice gra ins (N, on
a vera ge, dropped by 14%, P by 5%, Fe by 17%, Zn by
28%, but ca lcium (Ca ) increa sed by 32%). One ca n
only hope tha t subsequent studies will not show such
a disturbing drop in the levels of Fe a nd Zn. If high
[CO 2] does decrea se Fe or Zn content in va rious rice
cultiva rs, even by a few percent, the consequences for
the economy a nd hea lth of regions with strong dieta ry
dependence on rice, such a s southea st Asia , could be
dra stic. For exa mple, rice provides 76% of a ll ca lorie
inta kes for Ba ngla desh [3], the world’s eighth most
populous country, where micronutrient deficiency
a lrea dy lowers by 5% its gross domestic product [23].
F or t h e wor ld’s secon d m ost im por t a n t cr op,
wh ea t , da t a a r e a lso ver y lim it ed, bu t exist for a t
lea st five cu lt iva r s. All t h r ee st u dies sh ow
st a t ist ica lly sign ifica n t ch a n ges in gr a in
Acknow ledgements st oich iom et r y [24–26] (F ig. 1). On a ver a ge, t h e
I thank M . Iarova for help con cen t r a t ion of ever y m ea su r ed elem en t except
in the data com pilation K declin ed. No sim ila r da t a , t o m y kn owledge,
and discussions. I am also
grateful to S. Levin,
h a s been pu blish ed on ot h er im por t a n t cr ops su ch a s
E. Palson, N. Yarova, m a ize or r ye. Ir on ica lly, r ela t ively m or e da t a exist on
E. Zea, and three n on st a ple cr ops [27–35] a n d ot h er t er r est r ia l
anonym ous review ers for
va scu la r pla n t s [21,36–47], pa r t icu la r ly on t h eir
helpful com m ents. This
w ork was supported by folia r con t en t . All st u dies fou n d st a t ist ica lly
NSF grant DEB-0083566. sign ifica n t ch a n ges in t h e st oich iom et r y of pla n t
http://tree.trends.com
t issu es. Alt h ou gh t h e levels of a few elem en t s
in cr ea sed in som e st u dies, t h e con cen t r a t ion of ever y
elem en t , on a ver a ge, decr ea sed (F ig. 1). (Not e t h a t
t h e decr ea se in folia r N is close t o t h e 14% decr ea se
seen for N in a bovegr ou n d pa r t s, a s r epor t ed in a
m et a -a n a lysis by Cot r u fo et al. [16].) I will n ot
con t em pla t e h er e on t h e con sequ en ces of t h ese
ch a n ges t o h u m a n n u t r it ion a n d h ea lt h , bu t I h ope
t h a t it is clea r t h a t fu r t h er r esea r ch on t h e effect s of
h igh [CO 2 ] on pla n t st oich iom et r y is vit a l.
Further questions
Are there positive a spects of high [CO 2] for huma n
nutrition, other tha n the expected increa ses in
a gricultura l yields? Some vita mins, such a s A or C,
a re ba sed entirely on the elements C, O a nd H; hence,
a n increa se in the levels of those vita mins is not
constra ined stoichiometrica lly. For exa mple,
vita min C increa sed by 5% in ora nge juice ha rvested
from optima lly fertilized trees grown under
twice-a mbient [CO 2] [15]. If the overa ll content of
elements (except C, O a nd H) decrea ses, then it is
possible tha t levels of ha rmful hea vy meta ls, such a s
lea d (Pb) or mercury (Hg), would follow the sa me
trend. If high [CO 2], however, a ggra va tes the dieta ry
deficiency of essentia l elements then none of the
a bove mentioned or a ny other benefits could induce
huma n bodies to ma ke up the deficit.
Do cha nges in pla nt stoichiometry themselves
persist over yea rs? Beca use sta ple crops ha ve a life
span of only a few months, this question is more suited
for perennia ls. In lea ves of ora nge trees, declines
in the concentra tions of severa l elements tha t ha d
been monitored a fter 30 months of exposure to
twice-a mbient [CO 2], gra dua lly diminished over the
subsequent five yea rs [33]. These trees, however,
were a lwa ys well wa tered a nd optima lly fertilized,
a nd therefore a n elementa l imba la nce in their
surroundings wa s subsided. In Norwa y spruce,
however, the cha nges in stoichiometry of needles
persisted even in fertilized trees over the four yea rs
exposure to twice-a mbient levels of [CO 2] (the
experiment used 'bra nch ba g' CO 2 exposure
technique) [42]. Only one study compa red modern
pla nts with those growing a t historica lly lower
a mbient [CO 2]. Herba rium specimens of 13 pla nt
species were a na lysed for 12 elements [48], including
Fe, Zn a nd Ca . All elements a re currently a t lower
levels tha n a t a ny time in the pa st three centuries;
nota bly, stoma ta l density ha s a lso decrea sed.
(The differences in other environmenta l conditions,
however, might also have contributed to these changes.)
This ra ises a n importa nt question of whether the
current higher [CO 2] ha s a lrea dy contributed to the
existing ‘hidden hunger ’problem. Over longer
timesca les, ha ve historic fluctua tions of [CO 2]
a ffected herbivores by cha nging the stoichiometry of
their resource? It is known tha t cha nges in pla nt
qua lity in twice-a mbient [CO 2] ca n strongly a ffect
herbivorous insects [49,50]. From a stoichiometric
 Opinion
perspective, a ll herbivores a re simila r, thus such
effects should not be confined only to insects.
Rumina nts, including livestock, a nd other gra zers
could a lso be a ffected. Therefore, it is impera tive to
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