Carbon monoxide hation by plants1

R. G. S. BIDWELL
AND GAILP. BEBEE
Department of Biology, Queen's University, Kirzgstorz, Ontario
Received January 23, 1974
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BIDWELL, R. G. S., and G. P. BEBEE. 1974. Carbon monoxide fixation by plants. Can. J. Bot. 52:
1841-1847.
Leaves of 35 species of temperate and tropical lants absorbed CO in light from air containing
6 ppm CO at an average rate of 0.19 pl/h g fresf: weight. CO absorption was measured by the
uptake of 14C0from a closed flowing gas system. CO u take by bean leaves varied consider-
ably with age. Uptake by nine species having widely digrent rates of absorption was exactly
roportional to CO concentration in the range 0 to 100 ppm CO. Absorbed CO was metabo-
Ezed either by oxidation to CO2 and fixation as such or by reduction and incorporation into
serine. Corn, a C4 lant, emphasized the former pathway and bean, a C3 plant, emphasized the
latter pathway. ~8 had various effects on the photosynthesis of leaves of different species;
ranging from being inhibitory a t concentrations as low as 65 pprn to exerting no influence, or
even permitting an increase in net CO2 fixation at 99y0 CO because of the absence of 0 2 .
Plants do not contribute significantly to the global CO balance because theu uptake rate is
low at the CO concentration normally encountered in interurban areas. However, their con-
tribution may become very im ortant in or near urban and polluted areas, where elevated CO
concentrations are frequently Pound.

BIDWELL, R. G . S., et G. P. BEBEE.1974. Carbon monoxide fixation by plants. Can. J. Bot. 52:
1841-1847.
Les feuilles de 35 es kces de plantes tempCrCes et tropicales absorbent du CO i la lumikre, au
For personal use only.

taux moyen de 0.19 pp/h g de poids frais, a partir d'air contenant 6 ppm de CO. Le taux d'ab-
sorption de CO a CtC mesurC par l'absorption de 14C0 dans un systeme gazeux en circulation.
L'absorption de CO par des feuilles de five prCsente une variation considkrable selon I'Bge des
feuilles. L'absorption par neuf espkces ayant des taux trks diffkrents d'absorption Ctait exacte-
ment proportionnelle a la concentration de CO entre 0 et 100 ppm de CO. Le CO absorbe est
mCtabolisC soit par oxydation en C02 puis fixation, soit par reduction et inco oration dans la
strine. Le premier sentier est plus frkquent chez le mais, une plante I C4, tan% ue le sccond
sentier est favoris6 par la fkve, une plante I Ca. Le CO a des effets divers sur la p%otosynthkse
dans les feuilles de diverses espkces; il peut Ctre inhibiteur I des concentrations aussi basses que
65 ppm, il eut n'avoir aucune influence, ou mCme provoquer une augmentation dans la fixation
nette de C& I une concentration de 9970 de CO, I cause de l'apsence 8 0 2 .
Les plantes ne contribuent pas de f a ~ o nsignificative ?I l'kquihbre global du CO, car leur taux
d'absorption est faible aux concentrations de CO qu'on rencontre normalement dans les zones
non urbaines. Cependant, leur contribution peut devenir importante aux endroits urbains et
polluCs oh des concentrations ClCvCes de CO se rencontrent souvent. [Traduit par le journal]

Introduction followed by its oxidation to CO2 and its subse-

Controversial reports about the ability of
plants to absorb carbon monoxide (Krall and
Tolbert 1957; Chappelle and Krall 1961; Chap-
pelle 1962a, 1962b; Delwiche 1970; Inman and
Ingersoll 1971; Hill 1971) and the fact that un-
known sinks appear to be absorbing large
amounts of Earth's CO led to a preliminary
study of the uptake of CO by leaves of higher
plants (Bidwell and Fraser 1972). It was shown
that plants may absorb sufficient CO in light or
darkness to constitute an appreciable global CO
sink. It was suggested that the photometabolism
of CO involved its fixation by a reductive path-
way into serine but that dark uptake of CO was
'Financial support from the Ontario Ministry of the
Environment and the National Research Council of
Canada is gratefully acknowledged.
quent release.
We have here attempted an analysis, based on
a study of 35 temperate and tropical species, of
the contribution by plants to the global CO
balance. With a view to establishing the pathway
of CO photofixation in leaves, we have also
examined the distribution of radioactivity among
products of 14C0 fixation by a C3 plant (bean)
and a C4 plant (corn) and the pattern of labelling
in radioactive serine formed from l4CO.
Materials and Methods
Healthy, mature leaves from greenhouse specimens or
naturally grown plants were used. Plants grown under
pollution stress (i.e., on roadsides or near large industrial
sites) were avoided. For a leaf ontogeny experiment, bean
plants (Phaseolus vulgaris var. pencil pod black wax) were
 1842 CAN 1. BOT. VOL. 52, 1974

grown in a growth cabinet (16 h, 1500 ft-c illumination, literature about the CO-absorbing capacity of
23"/18" daylnight temperature). certain plants. Widcly different values have been
l4CO uptake was estimated in light (3300 fl-c water-
screened incandescent) by measuring the decrease in reported for cucumber (Chappelle and Krall
radioactivity in a closed flowing gas system at 22-24" as 1961 ; Inman and Ingersoll 1971; Bidwell and
described previously (Bidwell and Fraser 1972). 14C0 Fraser 1972; this paper) and alfalfa (Hill 1971 ;
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was stored over dilute NaOH, and the flowing gas stream this paper). The data in Table 1 show that large
was frequently passed through a CO, absorber to remove variability sometimes occurred in measurements
I4CO2 that might be generated biologically or spon-
taneously from 14CO. Photosynthesis was monitored made on individual species at different times.
continuously by a UNOR I1 infrared C02 analyzer. The Considering the possibility that CO uptake
closed system was charged with measured aliquots of might vary with age, we measured the rate of its
I4CO, 12C0, or W 0 2 as required with a microsyringe absorption from 6 ppm CO in air by primary
through a rubber diaphragm. N o leaf was tested unless it
showed a normal and steady rate of photosynthesis. CO bean leaves from emergence until they became
concentration during the measurement of CO uptake was senescent. Measurements were made at the same
usually 6 ppnl (pllliter); the volume of the closed circu- time (forenoon) on leaves just detached from
lating gas system was 348 ml. The apparatus was fre- well-watered plants from the growth chamber to
quently checked for leaks, and correction was applied for minimize diurnal and other variations. The re-
a very low, constant leak (or absorption) of 14C0 from
the gas stream. Leaves that took up I4CO were always sults, shown in Fig. 1, indicate a significant trend
subsequently found t o be radioactive.
Products of 14CO metabolism were examined after TABLE 1
alcohol extraction followed by clxomatography and
radioautography of the alcohol-soluble fraction as Uptake of CO by leaves from 6 ppm CO in air
described by Bidwell and Fraser (1972). Insoluble residues -
For personal use only.

were hydrolyzed gently (4 h at 100°C in 0.12 N HC1) and CO u take,

then strongly (18 h at 105°C in 3 N HC1). Hydrolysates Plant p1/11 n fllesll wt.
were dried under Nz at 40°, redissolved in water, and
analyzed by chromatography and radioautography. Abies sp.
Acer sacclmrinrrnz
Spots containing serine were cut from chromatograms Acer saccl~arrmz
and the distribution of 14C between carbons C-1 and ANirrrn cepn
C-2+3 was determined by radioactive assay before and Arctirim 171iltirs
after ninhydrin decarboxylation. The method of Bidwell Ave~lnsativcr
(1963) was modified as follows. Released COz was trapped Aznlea sp.
in ethanolamine :methyl cellosolve (1:2v/v) in a Citrirs parcrdisi
Vigreaux column and its radioactivity was measured Coleits blrrmei
C~icirnrisscrliviis
by scintillation counting using polyphenylene oxide C,vrromi~rmfcilcalirnt
(PPO) and p-bis-(2-(5-phenyloxazolyl))-benzene(POPOP) Dlrrrcrrs crrrotcr
in toluene (Winkenbach et 01. 1972). Fugopyrir171escirler~tirn~
Ficirs vcrrigur~~s
Frnxi~~lrs pe~~~isylvcr~iiccr
Results Gleditsicr rricrccr~irl~~rs
Hydrarlgeci sp.
Lycopersicu~iescirle~~rirm
Uptake of CO by Leaves Medicago sirriva
Leaves of 35 species of plants were tested for Pelnrgo~tirrrnsp.
their ability to absorb CO from a gas stream Plrcrseolrrs vrrlgnris
Plroeltix robele~rii
containing 6 ppm CO in air. From two to five Pilirrs resi~iosa
leaves were examined individually from each Plat~mgosp.
plant. Each leaf was allowed to absorb CO for Pop~rl~rs Prtr~~rrs
trer~~~iloides
~~igra
15 to 45 nlin; the rates of CO uptake were always Prrollrs virgiriicr~~a
constant within the limits of measurement. COz Syri~igavrrlgnris
Tageles rni~~imcr
uptake was monitored continuously throughout Tcrxrrs c a ~ ~ a d e t ~ s i s
CO uptake measurement. The results of the Trifoliimt prcrtertse
experiments are shown in Table I. It may be Triticlr~nnesrivir~n
Verbasc~rmtl~crps~rs
seen that the average rate of CO uptake for the Vibrrrtrrrm oplrlrrs
35 species was 0.19 pl/h g fresh weight of leaf. Zea mays
There was a wide variation in CO-absorbing Average CO uptake 0.19 pl/h g fresh wt.
capacity among species, but most absorbed some = 2.0 >( g/yr g
fresh we~ght
CO. There is considerable disagreement in the
 BIDWELL AND BEBEE: CARBON MONOXIDE FIXATION 1843

of declining CO uptake as the leaf aged, with an to fix 14Cby p-carboxylation, which indicates the
apparent (but not significant) peak at the 13th to conversion of 14C0 to 14C02.
the 19th day after leaf emergence. The threefold Since data of Bidwell and Fraser (1972) and
difference in CO uptake observed here would be
sufficient to account for most of the variation
observed in Table 1. However, many factors
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other than leaf age may also be important in

regulating CO uptake.
All the measurements in Table 1 were made at
6 ppm CO in air. Bidwell and Fraser (1972)
indicated that there was a tendency to propor-
tionality between CO uptake and CO concentra-
tion. To test this, the leaves of nine species1 that
had widely different rates of CO uptake were
01 I I I I
allowed to absorb CO from concentrations 0 5 10 15 20
ranging from 6 to 100 ppm CO in air. All Leaf age, days from emergence
measurements were corrected to a value of 1.0 FIG.1. C O uptake by primary leaves of bean as affected
for the rate of uptake at 6 ppm. Since the uptake +
by leaf age. The vertical bars show one standard
for all the leaves was very close to linear, all the deviation on either side of the mean of three or four
measurements.
data are plotted on a single curve shown in
Fig. 2. This curve shows clearly that CO uptake
is linear with CO concentration to at least
For personal use only.

100 ppm CO.

Metabolism of Absorbed 14C0
Leaves of bean (a C3 plant) and corn (a C4
plant) were allowed to absorb 14C0(1 35 ppm in
air, 58 Ci/mol) for various times in light. Alco-
hol-soluble products of lqCO metabolism were
separated and measured as described, with the
results shown in Tables 2 and 3. Hydrolysates of
the insoluble residues were examined chromato-
graphically; only small (not measurable) amounts
of 14C were found in most of the compounds
released by either weak or strong hydrolysis. CO concentration, pprn
Some labelled glucose was found in the weak FIG.2. C O uptake by leaves of nine species (see text)
hydrolysates of both corn and bean leaves. The as affected by CO concentration. The vertical bars show
amounts were not large and we did not measure i one standard deviation on either side of the mean.
them because the spots were diffuse, but visual
comparison of radioautographs showed that TABLE 2
bean incorporated several times more 14C into Soluble products of 14C0fixation by bean leaves.
Data as nCi/g fresh weight
glucose than did corn under comparable con-
ditions. Duration of I4CO fixation, min
Most of the fixed 14C was converted into Radioactivity
sucrose in both bean and corn leaves. Bean leaves in : 5 10 60 240
(Table 2) showed evidence of fixation via COz Sucrose 5.09 6.97 68.5 208
(PGA formation) and via serine (serine, but not PGA 0.414 0.328 1.18 0.472
Glycine 0 0 0 f
glycine, formation). Corn leaves (Table 3) showed Serine 0.949 2.301 4.72 18.4
no evidence for fixation via serine but did appear Alanine 0.063 0 2.13 10.7
Aspartate 0.040 0.009 0.774 1.34
'The species tested were Acer saccfrarrrm, Arctiurn Malate 0.117 0.153 2.84 4.89
min~rs,Frcrxinrrs pei~irsylvarrico,Hydrangea sp., Pelorgoni- Glutamate 0 0.004 0.472 1.90
zrm sp., Plantago major, Pr~rillrs~ligro,Trijolir~nrpraterzse, Unknowns 0.544 0.373 8.66 31.4
and Triticum aestiv~rm.
 1844 CAN. 1. BOT. VOL. 52, 1974

the data in Table 2 suggest that bean leaves may
fix CO by incorporating it into serine, samples of
radioactive serine from chromatograms of bean
leaves that had fixed 14C0 in light were degraded
by ninhydrin. The results are shown in Table 4.
Can. J. Bot. Downloaded from www.nrcresearchpress.com by UNIV OF NORTH CAROLINA AT on 11/11/14
by hydroxymethyl transferase) to form serine.
This is consistent with the absence of radioactive
glycine (Table 2). Corn leaves, which do not
emphasize the glycolate pathway, clearly do not
fix CO in this way, since no labelled serine was

Degradations of alanine-U-14C showed that
14C02recovery in this technique was 82 f 2% of
theoretical. Degradations of serine-3-14C showed
that less than 17, of its radioactivity was recov-
ered as 14C02. The data in Table 4 have been
corrected for the 18% lost in the analysis.
The results show that serine was not pre-
dominantly carboxyl-labelled, as it would be if it
were produced directly from PGA or from
phosphohydroxypyruvate or glycolate derived
from labelled PGA or Calvin cycle intermediates.
Instead, serine was heavily labelled in C-2+3,
which is consistent with its formation by the
reduction of CO and its transfer to glycine (e.g.,
TABLE 3
Soluble products of 14C0fixation by corn leaves.
For personal use only.
formed in them (Table 3). These data do not
preclude the simultaneous operation at a low
rate of the alternative pathway in bean leaves;
that is, oxidation of CO t o C02 and its fixation
as such.
EfSect of CO on Plzotosytzthesis
Bidwell and Fraser (1972) reported that C O
inhibits CO2 uptake in leaves of certain plants
(especially grapefuit and phoenix palm) but not
in others. We therefore measured CO2 uptake,
as a function of CO concentration, in leaves of
Coleus, phoenix palm (Phoenix robelenii), grape-
fruit (Citrus paradisi), bean (Plzaseolus vzilgaris),
and spinach (Spinacia olerncea), with the results
shown in Table 5. CO strongly inhibited COz
uptake of phoenix palm and grapefruit, had some

Data as nCi/g fresh weight effect on Coleus, and had no effect on spinach
and bean. In fact, CO2 uptake from an at-
Duration of 14C0fixation, min mosphere of almost pure CO was somewhat
Radioactivity enhanced in spinach and bean. This was probably
in : 5 10 60 240 the result of reduced 02, which results in in-
Sucrose 0.333 0.445 1.20 46.5 creased photosynthesis and reduced photorespi-
PGA. 0 0 0 0 ration (Jackson and Volk 1970). As would be
Gly cine 0 0 0 0
Serine 0 0 0 0.180 expected, CO concentration had no effect on
Alanine 0 0 0 0.553 COz fixation from atmospheres consisting of
Aspartate 0.027 + 4- 0.261 mixtures of N2 and CO. In those plants in which
Malate
Glutamate
0.022
0
+0 -k
0
0.562
0.567 15 to 30 min treatment with pure CO strongly
Unknowns 0 0 0 0.378 inhibited photosynthesis, no recovery took place
during at least 1 h of post-CO treatment in air.
TABLE 4 In the Coleus leaf, hbwever, where pure CO
Results of ninhydrin decarboxylation of radioactive serine
inhibition was not so strong, the inhibition was
(percentage of total radioactivity removed) from bean fully reversed on flushing of the leaf with air.
leaves that had fixed 14C0in light This suggests that inhibition may have been due
to a CO effect on stomata, which would not
Duration of 14C0fixation, min rapidly reopen during air treatment if their
10 60 240 closure in susceptible plants had trapped a
substantial amount of CO in the intercellular
6.6 4.3 1.2
14.0 8 .O 2.3 spaces of the leaves.
14.2 7.3 4.4
1.8 8.5 3.4 Discussion
4.0 10.6
1.5 The data in Table 1 and Fig. 2 permit a rough
3.1
9.2 estimate of the role of plants in maintaining the
13.9 global CO balance. The average CO concentra-
12.4 tion in air over land masses has been found to be
Average 8.1 +5.3 7.7_+2.3 2.8k1.4 in the range of 0.1 to 1.0 ppm (Junge 1963;
Corrected for loss 9.8 9.4 3.4
Robbins et al. 1968). Given linearity of absorp-
 BIDWELL AND BEBEE: CARBON MONOXIDE FIXATION 1845

tion with concentration (Fig. 2), this indicates and Dittmer 1966; Jaffe 1968, 1970; Hexter and
that plants absorb CO, on the average, at about Goldsmith 1971). Under these circumstances the
1/10 the rate shown in Table 1, which was rate of CO absorption by plants may be greater
measured at 6 ppm. The global mass of metabo- bv a factor of 10 to 100. This fact should be ~ ~

lizing leaves may be estimated as shown in cAnsidered when comparing the reported CO-
Table 6. The total global CO uptake by leaves absorbing capacity of soil, which depends on
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may then be calculated as follows. measurements made at 80 to 130ppm CO

(Inman et al. 1971). Inman and Ingersoll(l971)
2.0 X g/g fresh wt. year
X 10-I X 1.56 X 1017g fresh wt. TABLE 6
= 3.1 X 10'3 g per year. Total global mass of metabolizing leaves of higher plants

Global CO production is not easy to measure. Vegetation Area,a Leaf wt.: Total leaf
However, analysis of the literature suggests that zone km2 LAP g/cm2 mass, g
the figure of 3 X 1014g per year given in Table 7 Tropical 4.1 X107 9 C 0.02 7.4 x10'6
is as close as we can presently come. Subtropical 4.5X107 6.4C 0.02 5.8 X106
It is apparent that plants only absorb a little Temperate 3.1X107 9.3d 0.02 5.8 X10L6
over 1/ 10 of the total CO produced in the world. Total leaf mass active throughout the year
tropical + subtropical + 5/12 X
Furthermore, they produce over twice as much temperate" 1 .56X1017
as they absorb. CO production by plants appears aData of Good (1964).
to take place primarily from the degradation of bLeaf area index: .
CData of Odum er al. (1963).
chlorophyll and phenolic compounds and as dData of Whittaker (1966) and Satoo (1970).
eAverage of 37 measurements.
For personal use only.

by-products of the synthesis of bile pigments /Temperate vegetation is only active during 5 months of the year.
(Troxler et al. 1970; Huff et al. 1972; Troxler and
~ o k o s1973), as well as by other pathways TABLE 7
(Wittenberg 1960; Westlake et al. 1961; Loewus Global CO production
and Delwiche 1963; Pickwell et al. 1964; Chap-
man and Tocher 1966). Source Amount, g/yr
This would seem to indicate that plants are of Technological and natural sources 2X 1Ol4,a
little importance in the global balance of CO. Oceans 0.09X10L4,b
However, it must be emphasized that CO ab- Plants O.9X1OL4,C
Troposphere Od
sorption by leaves varies with CO concentration.
Total 3 X loL4
The value used in the above calculation is a low
one; average values of 5 to 9 ppm CO are "Data of Jaffe (1970) and Robinson and Robbins (1968).
bData of Swinnerton er al. (1970).
reported in the atmosphere of cities, with maxi- ;F$p;;t;X;; appear to be about
;;JY;:;Lction
mum values reaching well over 100 ppm (Altman troposphere is a self-balancing system (Weinstock and Niki 1972).
so the

TABLE 5
The effect of CO on photosynthesis at saturating C02 (300 to 500 p m), 3300 ft-c incandescent illumination, 22 to 2TC.
Leaves were kept for 15 to 20 min in each concentration of CO gefore measurement of C02 uptake. Recovery time
(in air) after exposure to 99% CO was 60 to 90 min

coa
0 0
(control) 65 100 125 200 300 99% (recovery)
Grapefruit 265b 89c -
-
78 59 -
-
39 8
Phoenix palm 84 88 70 50 14 15
Coleus 170 - 102 - 102 86 62 101
Spinach 256 106 - 104 103 - 122 -
Bean 247 - 101 - 98 100 119 -
Bean in N2 29 3 - 108 - 101 - 100 -
aCO measured in ppm exce t where otherwise indicated.
bFi ures represent pglmol Zo3per gram of control.
CC& uptake expressed as percentage of control.
 1846 CAN. 1. BOT. VOL. 52,
tested over 200 soil microorganisms isolated in
pure culture. Of these, only 16 cultures, all fungi,
absorbed atmospheric CO. On the other hand,
nearly all plants tested do absorb CO from very
low concentrations, and their absorptive capacity
rises with increasing concentration. In addition,
Can. J. Bot. Downloaded from www.nrcresearchpress.com by UNIV OF NORTH CAROLINA AT on 11/11/14
plants suffer little or no ill effects, in photosyn-
thesis at least, from concentrations of CO
within the ranges normally found even in heavily
polluted places (Table 5). For these reasons the
role that plants play in the global CO balance is
very difficult to assess but may, in fact, be quite
considerable.
The data of Bidwell and Fraser (1972) together
with those in Tables 2 to 4 of this paper indicate
that illuminated plants are capable both of
oxidizing CO to CO2 and of reducing it and
incorporating it into serine. Bean leaves convert
CO to CO2 in darkness and release it as such
(Bidwell and Fraser 1972). The pathway to
sucrose may be via C02 or via serine; the data
suggest that bean leaves emphasize the serine
For personal use only.
pathway, while corn leaves emphasize the CO2
pathway. Most of the metabolized CO remains
in the soluble fractions. Only a small portion
enters the insoluble compounds, mainly as glu-
cose polymers.
Our attention has been drawn to a paper by
H. P. Kortschak and L. G. Nickel1 (1973). Their
data for sugarcane leaves are closely similar to
our data for corn leaves and support the conclu-
sion that C4 plants do not rapidly metabolize
CO. Icortschak and Nickell also conclude that
plants do not constitute a inajor global CO sink.
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