Rising Atmospheric CO2 and Human Nutrition: Toward Globally Imbalanced Plant Stoichiometry

8/7/2019 Rising Atmospheric CO2 and Human Nutrition: Toward Globally Imbalanced Plant Stoichiometry

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TRENDS in Ecology & Evolution Vol.17 No.10 October 2002

http://tree.trends.com 0169-5347/02/$ see front matter 2002 Elsevier Science Ltd. All ri ghts r eserved. PII: S0169-5347(02)02587-9

457Opinion

The increas ing concentr at ion of atm ospheric car bon

dioxide CO2

and t he quality of our n utr ition ar e two

importa nt pr oblems tha t we ar e currently facing.

A link between t hese t wo problems, however, is not

apparent . Indeed, intensive and num erous studies on

th e effects of high [CO2] on plan ts h ave covered a wide

ra nge of issues, but its effects on plant s toichiometr y

(i.e. elementa l composition) h ave r eceived very litt le

at tent ion. Yet, plan ts a re t he foundat ion of our food

supply. The low concentr at ions of several essen tial

micronutr ients, su ch as iron (Fe), iodine (I) and

zinc (Zn), in m odern crops cont ribut e to th e pr oblem of

micronutr ient ma lnut rition (i.e. hidden h unger ), which

diminishes t he hea lth a nd economy of over th e half of

the worlds populat ion. Her e, by using t he t heory of

ecological stoichiometr y, I can link h igh [CO2] with plant

stoichiometry and t he quality of human nut rition. The

tools of ecological st oichiomet ry a re chem ical element s

and t heir rat ios in organisms and t he environment.

How can stoichiomet ry provide insight?

Analysing biological dynam ics from a chemical

element perspective has a dvantages in both its

simplicity a nd rigor ([1], I. Loladze, Ph D th esis,

Arizona Sta te Un iversity 2001). Acell contains

th ousands of complex subst an ces, but a ll life requires

~32 different chemical element s [2]. Life continuously

assem bles an d disassembles complex substa nces,

but it can n either create n or decompose chemical

elements, a nd it cannot convert one element into

another. These elementa l laws are rat her

self-evident, but ar e frequent ly overlooked in our

perception of biological dynam ics. Yet t he univer sa lity

an d cert aint y of these laws, which ar e valid on all

organizational scales, from molecules t o the

biospher e, provide a un ified fra mework th at h elps to

reveal pattern s hidden on disparate organizational

scales. The stoichiometr ic ar gumen t th at I discuss

here dr aws on mu ltiple scales, from t he str ucture of

carbohydrates t o a plant cell to an a gricultur al plot t o

globally r ising [CO2].

The need for essential elements and the problem of

micronutrient malnutrition

The hum an body needs at least 24 chemical elements.Although some of the element s, such as chromium (Cr),

Fe, I, s elenium (Se), or zin c (Zn), compr ise 3.5 billion people, mostly in th e developing world,

an d impa irs t he cognitive developmen t of children ,

causes productivity and educational losses, an d

increases morbidity and m ater nal morta lity[4].

Iodine deficiency is a public health problem in a t

least 130 count ries, with over seven hu ndr ed million

people sufferin g from goitre a nd t ens of millions

afflicted by brain dam age an d cretinism [4]. Near ly

half of the worlds population is a t r isk of ina dequat e

Zn inta ke [5]. Deficiencies of oth er ess ent ial

elements ar e also widespread, even in industr ial

count ries, but often a re not ma nifested in overt

clinical syndromes.

Global imbalance of essential elements and

plant stoichiometry

Hu ma n a ctivities profoundly alter th e global cycles of

several essential element s [1,7]. The pursu it of

higher agricultural yields, rath er tha n crop

qua lity, fertilizes soil disproportionat ely with N,

phosphoru s (P), an d potassiu m (K). Fossil-fuel

burn ing adds N and sulphur (S) via atmospheric

deposition a nd, together with changes in land use,

increas es [CO2]. Thus, hu man activities have been

alter ing the pool of a few essentia l elements in s evere

Rising atmosphericCO

2and human

nutrition:towardglobally imbalancedplant stoichiometry?Irakli Loladze

Terrestrial vascular plants obtain t heir 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 inunison wit h steadily increasing concentrations of CO

2[CO

2]. Thus, relative to

pre-industrial times, modern plants are experiencing a global elemental

imbalance. Could this imbalance affect the element al composition of plants,

the most important food source on Earth? Apart from an overall decline in

nitrogen concentrat ion, very little is known 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 knowledge,of published data supports the claim and shows

an overall decline of the (essential elements):C ratio. Therefore,high [CO2]

could intensify the already acute problem of micronutrient malnutrition.

Published on line: 8 August 2002

Irakli Loladze

Dept of Ecology and

Evolutionary Biology,

Princeton University,

Princeton, NJ 08544, USA.

e-mail:

[email protected]


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disproportion to others. Relative to pr e-industr ial

times, we ha ve been ra pidly creating a global

elemental imbalance. Can th is imbalance, in tur n,

affect u s by alter ing th e stoichiometr y of our

funda men ta l food source plant s? To an swer th is

question, I concentr at e her e on the role of rising [CO2]

for t he following thr ee rea sons.

First , unlike the contr oversy surr ounding the

effects of [CO2] on climate chan ge, the increase

in [CO2] itself is confirm ed by several indepen dent

sources [8]. Curr ently, every terr estrial plant is

exposed to ~30% higher [CO2] relative to

pre-indust rial times; during t his century [CO2]

levels could double or t riple over pre-indus tr ial

levels [8]. This increase is inst an ta neous on a

geological times cale and is unpr ecedented in th e

history of the hu man species. Because a modern tr ee

might experience th e doubling of [CO2] over its

lifetim e, such an increas e is also very fast on

evolutiona ry an d even ont ogenet ic tim escales.

Second, plant s build the bulk of their dry weight by

fixing C from CO2. Third, because of the gaseouspropert ies of CO

2and high mixing ra tes in the

atm osphere, no other h uma n impact compares to

rising [CO2] in its u niform ity. Plant s worldwide,

both agricultural a nd wild, are exposed to very

similar [CO2] concentra tions. For these r easons,

global pat tern s in th e changes of plant

stoichiomet ry can preva il in spite of local

environmen tal heterogeneity (tempera tur e,

hu midity, fert ilizers, et c.).

Plants in enriched CO2

atmospheres

The effects of high [CO2] on plant stoichiometry ha ve

received little a tten tion, but its effects on other plan tcharacteristics have been t horoughly studied.

Fr ee-Air CO2

Enr ichment (FACE) experiment s

have been r unn ing at 32 locations worldwide and

>2700 studies have been published in t he past decade

alone [9]. Doubling ambient [CO2] gener ally

stimulat es photosynthesis, enhan ces plant growth

and increases agricultura l yields, on a verage,

by 41% [1013]. These ben efits, however, become

quest iona ble if enr iched [CO2] alters crop

stoichiomet ry. Tha t chem ical composition of plant s

can change under increased [CO2] has been

suggested [e.g. 1,7,10], but m uch of th e experimen ta l

work h as ignored chemical elements and has

inst ead focused on complex compoun ds, ma ny of

which show litt le consisten cy in th eir res ponse to

high [CO2] [14,15]. Aclear pat ter n, however, exists

for N, t he only element wh ose concentr at ions in

plant s un der condit ions of high [CO2] have been

stu died extensively. The meta -ana lysis of th e

concentra tions of N in aboveground plant tissues

revealed, on average, a 14%decline in its

concentra tions under high [CO2] levels [16].

Microelement s, such as F e, I, and Zn, in plants a re

vital for hu man health, but little is known about

their response to high [CO2]. Not a single stu dy,

to my kn owledge, ana lyses th e effects of high [CO2]

on t he concentra tions of Se, which is an important

ant ioxidant, or Cr, which is extr emely import ant in

th e regula tion of blood-suga r levels and wh ich is

probably deficient in hu man nut rition [17].

The obscur ity of data might explain why no

compr ehen sive review exists a bout th e effects of

high [CO2

] on plan t st oichiomet ry an d why its role in

micronut rient ma lnutr ition has not been addressed.

As St erner and Elser [1] point out the limited and

diffuse da ta on element al compositionresult in

little awareness a nd little ability to perceive patter ns

of int erest , which in tu rn resu lt in little new da ta

being genera ted a nd little effort at compiling those

alr eady ava ilable. In lieu of rea l experiment s on

plant stoichiometry un der increased [CO2],

I ha ve run a th ought experim ent (see below).

Such experimen tsa re conventionally reser ved for

inherent ly simpler ph ysical ra ther tha n biological

system s, but th e reliance on stoichiomet ry simplifies

th e biology an d pr ovides su fficient rigor to gain

an insight in to the effect of increa sed [CO2] onplan t stoichiometr y.

A FACE thought experiment

Two un der pinn ings of ecological stoichiomet ry ar e

useful when ru nn ing a FACE experiment :

(1) a self-evident but importa nt fact tha t organisms

cannot creat e or convert elements ; and (2) the

proportions of element s in a pla nt cell can vary

widely, largely becaus e of th e pres ence of a lar ge

centra l vacuole, which is unique to plant cells [1];

for exam ple, Fe or Zn conten t can vary t enfold or m ore

in gra ss forage [18].

Suppose tha t a terr estrial vascular plant , forexample wheat , has been grown on two plots, Aa nd B,

in ident ical conditions, except t ha t [CO2] is ambient

in Abu t is doubled in B. If th e dry weight of th e

sta nding st ock in B is % higher tha n in A, are th e

stoichiometr ies of A plant s and B plant s different?

Even th ough t he a mounts of each individual element

in the soil were th e sam e in the two plots, th e higher

bioma ss in plot B is the r esult of stim ulat ed

photosynthesis tha t increased carbohydrat e

production. If the increase in car bohydrat es, the

chief const ituen t of plan ts, ha d been the only differen ce

between t he t wo plots, then the C, oxygen (O)

an d hydr ogen (H) cont ent in B plan ts would differ

very litt le from th at in A plant s (Box 1, Eqn II ). But

every other element would ha ve decreased by %

(Box 1, Eqn I II), which pr ovides a baseline

estimate of the potential shift in the plan t

stoichiometr y. This un derlines t he dichotomy

between C, O, H (which constitu te >90% of the d ry

weight of plant s) and other elements. Hen ce, pattern s

in t he chan ges of plant chemical composition should

be more evident on t he chemical scale of elemen ts

rat her t han on the coarser scales of complex

compounds , man y of which cont ain C, O, H a nd other

elements simultaneously.

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458 Opinion


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The dilution by carbohydrat es, however,

is unlikely to be the only difference between Aa nd

B plants. B plants might a dapt t o doubled [CO2]

by changing their tr an spira tion, root:shoot ra tio,

root morphology, root activit y or symbiotic

association with m ycorrhizae. Could t hese a dapta tions

equalize the stoichiometr ies of A and B plan ts byincreasing th e net uptake of every element by the

same percentage as t he net increase in C? I argue

here tha t these adapta tions could alter the %

decline caused by carbohydra te dilut ion,

but will not neut ra lize it.

The plots A and B a re monocultur es, as are m ost

sta ple crop fields; thus , by employing an y of the

adapt ations listed above, an individual B plant is

unlikely to gain an y advanta ge relative to its

almost iden tical neighbours . Moreover, none of th e

adaptationsper se can change the total ma ss of

any element in th e plot (except C, O an d H),

but t hey do alter condit ions in t he soil, including the

stoichiomet ry of soil nea r r oots a nd soil moistu re.

Because elements differ in their diffusion r ates and

upta ke kinetics, the net upta ke of each element

cannot increase by the sam e percentage. For

example, at higher concentra tions, [CO2] diffus es

into leaves more easily, thu s ena bling plant s to

nar row stomat al apert ures a nd consequently to lose

less water, tha t is to decreases t ra nspirat ion. This

effect has been well documen ted in experimen ts

with d oubled [CO2] on both C3 (e.g. rice and wh eat )

and C4 (e.g. maize and su garcane) plants with an

avera ge 23% redu ction of tr an spira tion [1113].

Reduced tr anspir ation leads to redu ced ma ss flow in

th e soil an d it can a lso increa se soil moistu re [19].

Thus, the two primary mechanisms that tran sport

element s to th e vicinity of roots, mas s flow and

diffusion, ar e alter ed in plot B. Mass flow is genera lly

more important for m obile elements, such as N,

an d diffusion is more import an t for imm obile

elements, such as P. Hence, the change in upt ake

rat es should be different among elements in plot B.

Fur ther more, increased photosynthesis puts

different ial interna l demands on elements . For

example, under h igh [CO2], plant dem and can

increas e for P but decrease for N [20,21]. To

summ ar ize, B plant s have higher C fixation ra tes,

altered intern al elementa l deman ds and chan ged

availability of elements n ear roots. Ther efore, A and

B plant s should differ not only in C:(oth er elemen ts)

rat ios but a lso in the r atios among other elements

(e.g. C:N, N:P an d P:Zn should also be different ).

In other words, th e change in t he st oichiometr y of

B plants should be nonuniform across element s.

Hence, A plants h aving the sam e stoichiometr y asB plants s hould be an exception. (If plant bioma ss

decreases in h igh [CO2], then a similar ar gument

can again sh ow that plant st oichiometr y chan ges.)

Ther efore, th e conclusion is tha t high [CO2],

as a rule, alters plant st oichiometr y.

Are overall patterns possible?

The above ar gument su ggests tha t th e chan ge in the

concentr at ion of elements (except C, O an d H) moves

in an opposite direction to the change in biomass,

but it does not exclude th e possibility th at levels of

some elements can increase or rem ain un changed

with an increase in biomass under high [CO2]. Forhum an n utr ition, however, it is importan t to know

whether overall patt erns would exist in high [CO2]

world. Terrest rial vascular plan ts worldwide sha re

what is funda ment ally the same physiology and ar e

exposed to essent ially the sam e [CO2], suggest ing

tha t overall patter ns in th e chan ges of plant

stoichiometr y ar e possible. Apa rticularly distur bing,

but plausible patter n is one in which the

concentr at ions of essen tial element s, including

those tha t ar e already deficient in t he diets of the

ha lf of the worlds populat ion, decreas e in plan ts.

As suggested a bove, both increased carbohydr at e

accumu lation and reduced mass flow can lead to this

patt ern. All else being equal, this pat tern would

mea n lower (nut rit ional value):(caloric value) of

crops an d the a ggra vation of the micronut rient

malnu trition problem. It would also increase th e

imperat ive to breed rice, wheat and other staple

crops with superior ability to concentr ate essential

elements such a s Fe, Zn, I and Se [6].

What do the scant published data reveal?

Motivat ed by the conclusion of th e th ought

experiment , I sea rched exten sively for p ublished

dat a on t he effects of high [CO2] on t he elemental

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459Opinion

In ecological stoichiometry, elemental vectors are very useful because theyprovide a simple m eans wi th w hich to apply the power of mass balance laws toevery element.

Let (a1,a

2,,a

n),(b

1,b

2,b

n) and (c

1,c

2,c

3,0,0) denote elemental vector s

for dr y A plants, dry B plants and carbohydrates respectively, where the firstthree term s represents carbon (C), oxygen (O) and hydrogen (H) concentration s

and other t erms represent concentrations of every other element. Then

.

Let Mdenote the total dry weight of A p lants. If the % increase in bi omass ofB plants is solely because of the increase in carbohydrates, then m ass balanceyield s (Eqn I):

M(a1,a

2,,a

n) + M(c

1,c

2,c

3,0,0) = (1 + )M(b

1,b

2,,b

n) [Eqn I]

Thus, and . The percentage change in

concentration s of C, O and H is but because

the content of these three elements in plants and carbohydrates is similar,(i.e. a

i c

i), it follo ws that (Eqn II)

ai bi, i= 1,2,3 [Eqn II]

For the rest of th e elements, the percentage change equals to (Eqn III)

[Eqn III]..,...,4,1

1 nja

b

j

j=

+

=

1,2,3,1

1 =

+

= ia

ca

a

b

i

ii

i

i

.,...,4,1

nja

bj

j =

+

=

1,2,3,

1=

+

+= i

cab iii

1111

=== n

i

n

i

n

i cba

Box 1.Elemental vectors:the shift in the stoichiometry of B plants

because of carbohydrate dilution


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composition of plant s. The data ar e sur prisingly

scant . I hope that the scarcity and importance of the

dat a will encour age the genera tion of new dat a on the

changes in plan t st oichiomet ry caused by a globally

altered environment. It is star tling that, among

thousa nds of publications on doubled [CO2], only one

investigated it s effects on the gr ain s toichiometr y of

rice, the worlds m ost importa nt crop [22]. This st udy

foun d decrea sed concentr at ions of four out of five

meas ur ed elements in br own rice grains (N, onavera ge, dropped by 14%, P by 5%, Fe by 17%, Zn by

28%, but calcium (Ca) increa sed by 32%). One can

only hope tha t subsequ ent st udies will not show such

a distu rbing drop in th e levels of Fe and Zn. If high

[CO2] does decrease F e or Zn cont ent in var ious r ice

cultivars, even by a few percent, th e consequen ces for

the economy and h ealth of regions with str ong dietar y

dependence on rice, such as south east Asia, could be

dra stic. For exam ple, rice provides 76% of all calorie

inta kes for Ban gladesh [3], the worlds eighth most

populous count ry, wher e micronut rient deficiency

alrea dy lowers by 5% its gross domest ic product [23].

For t he worlds second m ost import an t crop,

wheat, dat a a re a lso very limited, but exist for a t

least five cultivar s. All th ree st udies sh ow

stat istically significant changes in grain

stoichiomet ry [2426] (Fig. 1). On a vera ge, the

concent ra tion of every measu red elemen t except

K declined. No similar da ta , to my knowledge,

has been published on other import ant crops such as

ma ize or r ye. Ironically, relat ively more da ta exist on

nonstaple crops [2735] and other terr estrial

vascular pla nt s [21,3647], par ticular ly on their

foliar content . All stu dies foun d sta tist ically

significan t chan ges in the st oichiomet ry of plan t

tissu es. Although t he levels of a few element s

increased in some stu dies, the concentra tion of every

element , on aver age, decrea sed (Fig. 1). (Note th at

th e decrease in foliar N is close to the 14% decrease

seen for N in aboveground pa rt s, as r eported in a

meta -analysis by Cotr ufo et al. [16].) I will not

cont empla te her e on th e consequences of th ese

changes to hum an nu trition and health , but I hope

tha t it is clear t hat further resear ch on th e effects of

high [CO2] on plan t st oichiomet ry is vital.

Further questions

Are th ere positive aspects of high [CO2] for h uma n

nutr ition, other t han the expected increases in

agricultur al yields? Some vitam ins, such as A or C,

are based entirely on t he elements C, O an d H; hence,

an increase in t he levels of those vita mins is n ot

const ra ined s toichiometr ically. For example,

vitamin C increa sed by 5% in ora nge juice har vested

from optima lly fertilized tr ees grown under

twice-am bient [CO2] [15]. If th e overa ll conten t of

elements (except C, O an d H) decrea ses, then it ispossible tha t levels of harm ful heavy metals, such as

lead (Pb) or m ercur y (Hg), would follow th e sa me

tr end. If high [CO2], however, aggra vates t he dieta ry

deficiency of essential elemen ts t hen none of the

above mentioned or an y oth er ben efits could induce

hum an bodies to ma ke up th e deficit.

Do changes in plan t st oichiomet ry th emselves

persist over year s? Becau se sta ple crops ha ve a life

span of only a few months, t his quest ion is m ore suited

for per ennia ls. In leaves of ora nge tr ees, declines

in the concentra tions of several elements t hat had

been monitored after 30 mont hs of exposur e to

twice-am bient [CO2], gradu ally diminished over th esubsequen t five year s [33]. These tr ees, however,

were always well water ed and optimally fert ilized,

and t herefore an elementa l imbalance in their

surr oundings was subsided. In Norway spr uce,

however, the changes in st oichiomet ry of needles

persist ed even in fert ilized trees over the four yea rs

exposur e to twice-ambien t levels of [CO2] (th e

experiment u sed 'bra nch bag' CO2

exposure

technique) [42]. Only one stu dy compa red m odern

plant s with t hose growing at h istorically lower

am bient [CO2]. Herba rium specimens of 13 plant

species were an alysed for 12 element s [48], including

Fe, Zn and Ca. All element s ar e cur ren tly at lower

levels than at any time in the past t hree centuries;

notably, stomata l density has a lso decreased.

(The differences in other en vironment al conditions,

however, might also have cont ribut ed to these chan ges.)

This raises an importan t question of whether the

curr ent h igher [CO2] has already contr ibuted to the

existing hidden hu nger problem. Over longer

timescales, ha ve historic fluctua tions of [CO2]

affected h erbivores by changing th e stoichiometr y of

their r esource? It is known t hat changes in plant

quality in t wice-ambient [CO2] can st rongly affect

her bivorous in sects [49,50]. Fr om a s toichiometr ic



460 Opinion

TRENDS in Ecology & Evolution

N P K Ca S Mg

Element

Changeinmeanconcentration(%)

Fe Zn Mn Cu

25.0

15.0

5.0

5.0

Fig. 1. Changes (%) in the mean concentration of essential elements in plants grow n in twi ce-ambient

atmosph eric [CO2] relative to those grow n at ambient levels [all plants (foli ar), green; wheat (grains),

yellow ]. The figure is based on 25 studies covering 19 herbaceous and 11 woody plant species,

and five wh eat cultivars [21,2447], in which mult iple elements w ere measured under increased

concentration s of atmosph eric carbon diox ide [CO2]. If several [CO

2] levels were repor ted, the data for

the levels closest to the ambi ent and twice-amb ient were used. The studies wit h superenriched or

naturally high [CO2] were excluded. Mu ltipl e data for a single species or a cultiv ar were averaged

before calculating m eans. Error bars indicate the standard error of the mean; for foliar data, n= 30 for

nitro gen (N), phosphoro us (P), and potassium (K), 29 for calcium (Ca), 26 for magnesium (Mg),

14 for iron (Fe) and manganese (Mn), 12 for zinc (Zn), 9 for sulphu r (S) and copper (Cu); for wh eat

grains,n= 5 for N, P, K, Ca, Mg, Fe and Zn, and 3 for S and Mn. Up on requ est, I will gl adly pr ovide a

detailed table wit h all the data on which this figur e is based.

Acknowledgements

I thank M. Iarova for help

in the data compilation

and discussions. I am also

grateful to S. Levin,

E.Palson, N. Yarova,

E.Zea, and three

anonymous reviewers for

helpful comm ents. This

work was supported by

NSF grant DEB-0083566.


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461Opinion

perspective, all her bivores a re similar, thu s such

effects should not be confined only to insects.

Rumin an ts, including livestock, an d oth er gra zers

could a lso be affected. Therefore, it is imper at ive to

recognize and quant ify at the ear ly stage how the

changing environment shifts th e stoichiometr y of

plants th e foundat ion of hum an n utr ition an d the

base of virtu ally all food webs in na tur e.

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Rising Atmospheric CO2 and Human Nutrition: Toward Globally Imbalanced Plant Stoichiometry